Anda di halaman 1dari 70

TELAAH JURNAL

ASUHAN KEBIDANAN PADA KEHAMILAN

MATA KULIAH CRITIKAL ANALYSIS DALAM PRAKTIK


KEBIDANAN

Kelompok 1

Disusun Oleh :

1. Rosa Amelinda (P25202010002)


2. Siti Ropiah (P25202010003)
3. Riza Jatur Rahmah (P25202010004)
4. Khusnul Maghfiroh (P25202010007)
5. Eka Widya Novika S (P25202010008)

Dosen Pengampu :

Evi Pratami, M.Keb

KEMENTERIAN KESEHATAN REPUBLIK INDONESIA


POLITEKNIK KESEHATAN KEMENKES SURABAYA
JURUSAN KEBIDANAN
PROGRAM STUDI PENDIDIKAN PROFESI BIDAN
TAHUN 2020
TELAAH JURNAL KEHAMILAN

1. CLARITY JURNAL 1 JURNAL 2 JURNAL 3 JURNAL 4 JURNAL 5


(Rosa Amelinda) (Siti Ropi’ah) (Riza Jatur R) (Khusnul Maghfiroh) (Eka Widya N)

Judul Using Text Messaging Relationships Effects of Maternal Pregnancy duration and Determinant factors
to Improve Access to Between Physical Mental Health on breast cancer risk of anaemia among
Prenatal Health Activity and Engagement in pregnant women
Information in Urban Quality of Life in Favorable Health attending antenatal
African American and Pregnant Women Practices During care clinic in
Afro-Caribbean in the Second and Pregnancy (Pengaruh Northwest Ethiopia
Immigrant Pregnant Third Trimester kesehatan mental ibu
Women: Mixed pada keterlibatan
Methods Analysis of dalam praktek
Text4baby Usage.
kesehatan yang
menguntungkan
selama kehamilan)

Penulis Tenya M Blackwell, Justyna Krzepota, Jeanne L. Alhusen, Anders Husby, Jan Tadesse Hailu,
LeConte J Dill, Lori A Dorota Sadowska, PhD, CRNP, RN, Wohlfahrt1 , Nina Øyen Simachew Kassa,
Hoepner, Laura A Geer and Elzbieta Lauren Ayres, BSN, & Mads Melbye Bayeh Abera,
Biernat RN, CCRN, Kelli Wondemagegn Mulu
DePriest, BSN, RN and Ashenafi
Genanew
Tahun 2020 2018 2016 2018 2019

1.1 Latar Belakang Program kesehatan Masalah pada Kurang pemahaman Kanker payudara Prevalensi anemia di
Masalah seluler(mHealth tingkat aktivitas pada factor-faktor yang merupakan kanker antara wanita hamil
Text4Baby (T4B) diakui fisik yang tidak yang mempengaruhi ganas paling umum diperkirakan 38% di
dapat memberikan akses memadai adalah kemampuan ibu untuk pada wanita dan
seluruh dunia, 36,9%
bagi wanita hamil untuk kontek penting terlibat dalam praktek penyebab utama beban
mendapat informasi dalam hubungan kesehatan yang penyakit di seluruh di Afrika dan 23% di
kesehatan, perawatan, kualitas hidup pada menguntungkan selama dunia1. Baik jumlah Ethiopia Penelitian ini
dan sumber daya. wanita. Studi kehamilan. dan waktu melahirkan bertujuan untuk
Namun, sedikit yang terbaru belakang seorang wanita telah mengetahui hubungan
diketahui tentang apakah ini telah lama diketahui obesitas dan komposisi
wanita hamil imigran memberikan memengaruhi risiko tubuh dengan waktu
Afrika-Amerika dan informasi penting kanker payudaranya,
pubertas pada anak
Afro-Karibia perkotaan pada perubahan tetapi bagaimana
di Amerika Serikat yang terjadi pada faktor-faktor ini laki-laki dan
adalah pengguna yang kesehatan yang memengaruhi etiologi perempuan.
menerima metode berhubungan kanker payudara belum
komunikasi kesehatan dengan kualitas dipahami dengan baik.
inovatif atau hambatan hidup, baik selama
budaya dan sistematis kehamilan maupun
yang menghambat niat dalam periode
mereka untuk perinatal.
menggunakan T4B.
1.2 Jalan Keluar Untuk menguji Untuk Untuk mengetahui Untuk mendapatkan Tujuan dari penelitian
intervensi pendidikan mendapatkan informasi tentang efek ini adalah untuk
factor-faktor
kesehatan ibu Text for informasi tentang perlindungan kehamilan menilai prevalensi dan
Baby (T4B) untuk hubungan antara predisposisi terhadap risiko kanker faktor determinan
melihat apakah aktivitas fisik dan payudara anemia pada wanita
keterlibatan wanita
intervensi tersebut kualitas hidup hamil di Northwest
meningkatkan akses ke diantara wanita dalam praktik
Ethiopia.
perawatan dan informasi hamil di Poland.
kesehatan yang
kesehatan prenatal,
melakukan identifikasi menguntungkan selama
perilaku kesehatan pada
kehamilan.
wanita hamil, dan
menentukan
kemungkinan wanita
hamil di Brooklyn
tengah akan mengakses
T4B sebagai saluran
layak informasi
kesehatan prenatal.
Keyakinan subjektif dan
normatif mereka tentang
sumber informasi
kesehatann prenatal,
persepsi mereka tentang
kegunaan dan
kompabilitas T4B, dan
faktor-faktor seperti
kepuasan dan visibilitas
T4B akan
mempengaruhi
penerimaan dan niat
perilaku ibu hamil untuk
menggunakan program
T4B untuk
meningkatkan akses
perawatan dan informasi
kesehatan dan
melahirkan.
1.3 Ilustrasi Wanita hamil imigran Penelitian ini Pendidikan kesehatan
Afrika Amerika dan memberikan harus diberikan
Afro-Karibia di sumbangsih bagi tentang faktor-faktor
perkotaan Brooklyn pengetahuan
yang memperburuk
mengalami sejumlah tentang hubungan
faktor penentu sosial dan antara aktivitas anemia selama
ekologis seperti fisik dan kualitas kehamilan.
rendahnya tingkat melek hidup pada
kesehatan, pendapatan, kehamilan.
dan bahasa yang Hasilnya
menjadi hambatan untuk memperlihatkan
mengakses prenatal perlunya perbaikan
yang berkualitas. T4B pada perawatan
adalah program pesan perinatal dan
teks yang memberikan promosi program
pesan perawatan aktivitas fisik pada
prenatal untuk wanita wanita.
hamil dan ibu primi.
Meskipun intervensi
mHealth telah diusulkan
sebagai solusi efektif
untuk meningkatkan
kesehatan ibu dan, studi
ini menunjukkan bahwa
penggunaan mHealth
untuk informasi
kesehatan pranatal
cukup umum, sedangkan
penelusuran internet,
Google, dan penggunaan
aplikasi terkait
kehamilan paling
banyak digunakan.
Menerima pesan
elektronik kesehatan
pranatal melalui SMS
adalah cara yang positif
dan sangat cocok untuk
memberikan informasi
kepada wanita hamil di
Brooklyn tengah;
Namun, lebih banyak
penelitian dengan
populasi yang lebih
besar dan pemodelan
langsung pengujian
konstruksi teoritis
diperlukan untuk
sepenuhnya menilai
persepsi. Kegunaan dan
keuntungan relatif T4B
dalam populasi ini.
Tujuan penelitian ini
penting untuk
menggunakan upaya
mHealth Meskipun ada
niat moderat untuk
menggunakan program
T4B harus terlebih
dahulu dirancang dan
disesuaikan dengan
dimasukkannya
kemungkinan karena
fasilitasi pada wanita
yang mengakses yang
ditargetkan untuk
memastikan bahwa
pesan dan konten adalah
informasi yang relevan,
memperoleh lebih
banyak kendali, dan
menjangkau lebih sehat
dan untuk populasi
berbasis tempat tertentu.
1.4 Contoh Informasi pesan teks Clark dan Gross Pada studi lain Beberapa penelitian Hasil serupa
kesehatan merupakan mendemonstrasika menunjukkan bahwa telah menunjukkan dilaporkan oleh
metode yang cukup n bahwa 39% wanita hamil dengan perubahan persisten penelitian yang
efektif untuk wanita yang kesehatan mental yang dalam ekspresi gen, dilakukan di Gondar
menjangkau pada melaporkan buruk (mengalami gejala struktur epigenetik, dan dan Ethiopia barat,
populasi tertentu. Hal ini berpartisipasi depresi, dukungan social komposisi sel induk Kemungkinan
sejalan dengan dalam beberapa yang buruk dan epitel di kelenjar susu penyebabnya anemia
penelitian (Dallas, dkk, bentuk latihan karakteristik setelah kehamilan. pada ibu hamil
2019) yang berjudul mingguan sebelum sosiodemografi tertentu) Namun, mekanisme mungkin karena status
Text-Messaging, Online hamil melaporkan cenderung tidak terlibat yang diusulkan untuk sosial ekonomi yang
Peer Support Group, and tidak melakukan dalam praktek kesehatan perlindungan kanker rendah, kurangnya
Coaching Strategies to aktivitas yang sama yang menguntungkan payudara akibat informasi yang
Optimize the HIV selama kehamilan. selama kehamilan. kehamilan belum memadai tentang gizi
Prevention Continuum Menurut data didukung atau selama kehamilan dan
for Youth: Protocol for a evenson, hanya direplikasi. aksesibilitas ke
Randomized Controlled 15,8% wanita fasilitas perawatan
Trial menunjukkan hamil di USA, kesehatan dan
adanya keefektifan dilaporkan aktif pendidikan rendah.
pesan teks sebagai beraktifitas fisik,
langkah pencegahan sesuai dengan
HIV dikalangan rekomendasi.
remaja.sejalan dengan
penelitian yang
dilakukan di Kanada,
Arab saudi
menunjukkan wanita
hamil mendapat manfaat
positif dari penggunaan
mHealth mengenai akses
ke layanan kesehatan
prenatal, peningkatan
perilaku pencarian
informasi, dan telah
memberikan dukungan
selama kehamilan.
2. ACCURACY

2.1 Nama Jurnal JMIR MHEALTH International journal Journal of Midwifery Nature communications Tropical Diseases,
AND UHEALTH of environment Travel Medicine and
and Women’s Health
research and public Vaccines
health.

2.2 Tahun Terbit 2019 2019 2016 2018 2019

2.3 Quartil Q2 Q2 Q1 Q1 Q2

3. PRECISION

3.1 Kelengkapan Artikel ini sudah Lengkap, terdapat Informasi yang termuat Artikel ini sudah cukup Pada jurnal ini
Informasi cukup lengkap, pendahuluan, metode, Lengkap, terdapat lengkap, karena sudah informasi lengkap.
karena sudah hasil, dan pembahasan pendahuluan, metode, menyertakan Abstrak, Terdiri dari abstrak,
menyertakan Abstrak, dan kesimpulan. hasil, dan pembahasan Latar Belakang,
pendahuluan, metode,
Latar Belakang, dan simpulan. Metode, Analisis, Hasil,
Metode, Analisis, Pembahasan hingga hasil, pembahasan dan
Hasil, Pembahasan Kesimpulan. kesimpulan.
hingga Kesimpulan.
3.2 Informasi Dalam artikel ini Terdapat tabel sebagai Terdapat tabel sebagai Terdapat tabel sebagai Pada jurnal ini telah
Spesifik memuat gambar layar media penyajian hasil media penyajian hasil media penyajian hasil disertai dengan tabel
contoh teks yang penelitian. penelitian. penelitian. Karakteristik sosial
dikirim ke ibu haamil, demografi ibu hamil
terdapat tabel yang mengikuti
komponen kuisioner pelayanan ANC, tabel
berdasarkan skala, Tingkat anemia dan
terdapat tabel infeksi parasit usus
karakteristik pada wanita hamil,
demografis pasien tabel Karakteristik
yang berpartisipasi Kebidanan & Medis
dalam kelompok ibu hamil yang
fokus dan wawancara, mengikuti pelayanan
terdapat tabel ANC, tabel Analisis
karakteristik multivariat
demografis pasien menunjukkan faktor
dalam kelompok penentu anemia pada
survei, serta terdapat wanita hamil
narasi dari hasil
wawancara.
4. RELEVANCE
4.1 Keterkaitan Ide Ide yang ada pada Terhubung, Ide yang ditulis dalam Ide yang terdapat pada Bahwa ide yang ada
latar belakang Untuk mengetahui penelitian latar belakang pada latar belakang
menunjukkan aktivitas fisik wanita menunjukkan adanya menunjukkan berhubungan dengan
keterkaitan mengenai hamil maka responden hubungan kebutuhan
keterkaitan mengenai rumusan masalah atau
pesan teks untuk harus menjawab yang signifikan untuk
meningkatkan akses pertanyaan yang di peningkatan Durasi kehamilan pertanyaan yang ada
informasi kesehatan bagi beberapa pemahaman tentang terhadap risiko kanker yaitu tentang faktor
prenatal. katogori yaitu rumah factor-faktor payudara penentu anemia pada
tangga, berhubungan predisposisi praktik wanita hamil.
dengan pekerjaan, kesehatan.
olahraga, transportasi,
dan ketidak aktifan.
Yang diukur dengan
pengeluaran energi
rasio pengeluaran
energi (MET).
4.2 Up to date Penelitian ini Update: Update. Artikel ini termasuk Artikel ini termasuk
termasuk penelitian Selama hamil seorang Informasi yang dalam artikel update. dalam artikel update.
up to date, karna ibu rentan untuk diberikan lebih lengkap Hal ini dikarenakan Hal ini dikarenakan
penelitian ini adalah merasakan malas dan spesifik dari sampai saat ini masih
sampai saat ini masih
studi pertama yang beraktivitas, namun penelitian sebelumnya banyaknya yang
meneliti perubahan sebenarnya aktivitas menderita penyakit banyaknya ibu hamil
dalam sikap, penting untuk kanker payudara. dengan anemia
keyakinan, dan kesehatan ibu sendiri.
persepsi di antara
wanita hamil imigran
perkotaan Afrika-
Amerika dan Afrika-
Karibia setelah
terpapar T4B, dan ini
memberikan wawasan
baru dengan
memeriksa
bagaimana niat
penggunaan T4B
dapat mempengaruhi
penggunaan dan
keuntungan.
4.3 Pengembangan Ide dalam penelitian Relevan : korelasi Relevan. Ide dalam penelitian ini Ide dalam penelitian
Ide ini dapat masalah antara Pengembangan ide dikembangkan lebih ini dikembangkan
dikembangkan ke aktivitas fisik dan dalam penelitian lebih luas dengan meneliti lebih luas dengan
berbagai lokasi yang kualitas hidup pada luas. meneliti tingkat
efek biologis berbeda
minim akan akses wanita hamil masih pengetahuan tentang
kesehatan dibidang menimbulkan banyak Depresi perintal yang diperkenalkan anemia pada ibu hamil
lainnya. pertanyaan yang perlu berpengaruh pada sekitar minggu ke 34 di pedesaan untuk
diselesaikan. kesehatan mental ibu kehamilan memegang mendapatkan
hamil. Wanita yang informasi tentang
kunci untuk memahami
berpenghasilan faktor penyebab
rendah mengalami perlindungan kanker
payudara terkait anemia pada ibu hamil
gejala depresi dalam
kehamilan. kehamilan.
Pengetahuan ibu
tentang praktik
kesehatan.
5. DEPTH

5.1 Jumlah Masalah Komponen pada Aktivitas fisik dan Usia muda (16-19 Masalah yang Masalah yang muncul
yang Muncul kuisioner kualitas hidup. tahun), obesitas muncul pada artikel pada artikel ini ada 6
- Skala sikap kehamilan, yaitu jumlah yaitu masalah tempat
- Skala kepercayaan meningkatnya gejala kejadian kanker
tinggal, makanan, usia,
- Skala kemudahan depresi, penurunan payudara dan waktu
penggunaan dukungan social. tindak lanjut status pendidikan,
- Skala kesesuaian menurut jumlah infeksi cacing
persalinan, usia tambang, penyakit
persalinan pertama, sebelumnya
dan lama kehamilan
terakhir.
5.2 Faktor-Faktor Sampel: Kriteria inklusi: kriteria inklusi: Kriteria inklusi : 1. Kriteria inklusi:
yang Bermakna 58 orang. Terbagi -kehamilan trimester Wanita hamil Semua wanita
menjadi 2 kelompok II dan III. Ibu hamil yang mampu Tidak memiliki hamil yang datang ke
(kelompok -stuju untuk berbicara Bahasa riwayat penyakit klinik antenatal untuk
wawancara : 9 orang, mengikuti penelitian. Inggris kanker payudara pertama kalinya
dan kelompok survei : Populasi:wanita hamil Sampel : 2,3 juta 2. Kriteria eksklusi:
Usia ibu hamil 16 tahun
49 orang) Sample:157 wanita wanita hamil di Wanita hamil yang
keatas
Inklusi : hamil trimester II dan Denmark, 1,6 juta menggunakan obat
- wanita hamil yang 189 wanita hamil Ibu hamil pada wanita hamil di anthelmintik
melakukan perawatan trimester III trimester kedua Norwegia 3. sampel yang dimbil
prenatal di SUNY sebanyak 743
Downstate Kehamilan tunggal
- berusia 18-45
tahun.
- Memiliki ponsel
dengan kemampuan
pesan teks
Mampu
berkomunikasi bahasa
inggris
6. BREDTH

6.1 Pandangan Penelitian ini penting Hasilnya Studi ini mengindikasi Hasil penelitian ini Hasil penelitian ini
terhadap hasil untuk menggunakan memperlihatkan adanya hubungan yang bermakna. kehamilan bermakna. Wanita
Pengamatan. upaya mHealth perlunya perbaikan signifikan antara gejala cukup bulan pada usia hamil di daerah
Meskipun ada niat pada perawatan depresi dengan dini dan peningkatan
pedesaan lebih
moderat untuk perinatal dan promosi dukungan social rendah jumlah persalinan3,4
menggunakan program aktivitas fisik yang mengakibatkan mengakibatkan mungkin menderita
program T4B harus pada wanita. kurang terlibatnya ibu penurunan risiko kanker anemia dibandingkan
terlebih dahulu Tidak ada perbedaan hamil dalam praktik payudara, sedangkan penduduk perkotaan,
dirancang dan signifikan secara kesehatan yang aborsi tidak wanita hamil di petani
disesuaikan dengan statistik pada laporan menguntungkan selama mempengaruhi risiko mungkin menderita
dimasukkannya total nilai dari kehamilannya. Gejala kanker payudara anemia dengan wanita
kemungkinan karena pengeluaran energy. depresi dapat
bukan petani, wanita
fasilitasi pada wanita Bagaimanapun, dipengaruhi oleh
yang mengakses yang aktivitas fisik yang kondisi tubuh ibu, hamil yang tidak sakit
ditargetkan untuk intensif berbeda status gizi, perubahan lebih kecil
memastikan bahwa signifikan (p≤0,05) hormon, penyakit yang kemungkinannya
pesan dan konten tergantung pada diderita sebelumnya, untuk mengalami
adalah informasi yang trimester pada kondisi ekonomi, usia anemia dibandingkan
relevan, memperoleh kehamilan. ibu, tingkat pendidikan dengan yang
lebih banyak kendali, Analisis dari tipe dan jumlah kehamilan. sebelumnya sakit
dan menjangkau lebih aktivitas Sedangkan dukungan medis, Wanita hamil
sehat dan untuk menunjukkan nilai social dapat yang tidak makan
populasi berbasis MET/minggu tidak dipengaruhi oleh status
sayuran lebih
tempat tertentu berbeda antara grup perkawinan dan kondisi
rumahtangga, aktivas keluarga. cenderung mengalami
pekerjaan, olahraga, anemia dibandingkan
dan transportasi. wanita hamil yang
Bagaimanapun makan sayuran,
tampak bahwa Wanita hamil yang
pengeluaran energi tidak makan daging
yang lebih tinggi
lebih mungkin
(p≤0,01) pada wanita
trimester tiga mengalami anemia
kehamilan. dibandingkan mereka
yang makan daging,
wanita hamil yang
tidak terinfeksi parasit
cacing tambang

7. LOGICALNE
SS

7.1 Berfikir logis Pada penelitian ini Sebuah penemuan Kondisi kesehatan Pada penelitian ini Anemia adalah
menunjukkan bahwa menarik dari studi mental ibu hamil menunjukkan bahwa konsentrasi
butuh dorongan bagi kami yaitu adalah sangat berpengaruh Pengubah terkuat yang hemoglobin darah
ibu hamil untuk wanita yang hamil pada kemampuannya diketahui dari risiko yang rendah dan telah
mengakses informasi yang menilai kualitas untuk terlibat dalam kanker payudara wanita terbukti menjadi
seputar kesehatan hidup lebih tinggi praktik kesehatan yang adalah riwayat masalah kesehatan
selama hamil pada daripada kesehatan menguntungkan selama reproduksinya. Dengan masyarakat yang
T4B. Studi ini fisik (pada trimester II kehamilan (exercise demikian, kehamilan mempengaruhi negara
termasuk studi survei dan III) dikategorikan dan istirahat, cukup bulan pada usia berkembang dan maju.
yang kuat, dari sebagai energi yang kebutuhan nutrisi yang dini dan peningkatan Salah satu faktor ibu
metode pengambilan lebih tinggi disaat terpenuhi, gaya hidup jumlah persalinan hamil dengan anemia
sampel dan analisis, aktivitas yang yang sehat, tindakan mengakibatkan antara lain infeksi
data kualitatif dengan berhubungan dengan antisipasi dini, penurunan risiko kanker parasit dan kebiasaan
kelompok fokus, pekerjaan. Penjelasan kemudahan dalam payudara, sedangkan makan selama
kunci informan dan untuk temuan ini mengakses perawatan aborsi tidak kehamilannya.
observasi. Selain itu, terlihat sangat jelas , kesehatan dan akses mempengaruhi risiko Penelitian ini
pengembangan survei wanita dengan fisik mendapatkan informasi kanker payudara. menunjukkan bahwa
secara teoritis dengan lebih baik akan bisa seputar kehamilan). wanita hamil yang
penerimaan inovasi bekerja lebih. Dalam beberapa tidak makan sayuran,
teknologi. Namun Bagaimanapun juga, karakteristik daging, dan wanita
pada penelitian ini penjelasan untuk sosiodemografi yang hamil yang terinfeksi
terdapat keterbatasan penomena ini bisa terkait terdapat risiko dengan parasit cacing
yaitu ukuran sampel saja lebih rumit. lebih tinggi untuk tambang lebih
yang kecil. mengalami penurunan cenderung mengalami
tekanan perinatal, anemia
termasuk kemiskinan,
status perkawinan
lajang, tingkat
pendidikan yang lebih
rendah, dan usia muda.
Jika ada factor tersebut
yang dialami oleh ibu
hamil akan
berpengaruh pada
kesehatan mentalnya,
bisa jadi ibu
mengalami gejala
depresi dan gejala
depresi mempengaruhi
kondisi kehamilannya.
Oleh karena itu, ibu
hamil tidak dianjurkan
mengalami stress yang
berlebihan, selain
berpengaruh pada
kondisi tubuhnya juga
berpengaruh pada
kondisi janinnya.

8. SIGNIFICANCE

8.1 Informasi yang Hipotesa dari Penemuan Penelitian ini sesuai Telah dihipotesiskan Pada penelitian ini
lebih signifikan penelitian ini sejalan menjelaskan dengan hipotesa. Ibu bahwa kehamilan sesuai dengan
dengan hasil hubungan antara hamil dengan usia pertama seorang wanita hipotesa, didapatkan
penelitian ini, aktivitas fisik dan muda, obesitas, tingkat memiliki pengaruh hasil bahwa Faktor
menunjukkan pesan kualitas kehidupan pendidikan rendah, khusus pada penentu anemia pada
teks untuk yang mana harus di gejala depresi, pembentukan kembali ibu hamil antara lain
meningkatkan akses lakukan dengan dukungan social struktur jaringan wanita hamil di daerah
Informasi kesehatan sangat hati-hati, rendah, status ekonomi payudara, dan hal ini pedesaan, petani, ibu
Prenatal. dikarenakan rendah merupakan mungkin menjelaskan hamil yang tidak
rendahnya nilai factor yang signifikan penurunan risiko kanker makan sayuran, ibu
korelasi koefisien. pada kurangnya payudara di kemudian hamil yang tidak
Penelitian kami tidak ketertarikan ibu hamil hari. makan daging, ibu
menyelesaikan dengan praktik hamil yang
masalah yang kesehatan yang berpendidikan rendah,
dibicarakan tetapi menguntungkan. hamil yang terinfeksi
penemuan ini dengan parasit cacing
menekankan tambang
kebutuhan untuk
menaikkan
keasadaran dari
pentingya aktifitas
fisik selama
kehamilan.
8.2 Menemukan Bukti menunjukkan - Gejala depresi dan Faktor penting dalam Faktor penting dalam
faktor penting. bahwa peran artikel ini adalah artikel ini adalah
dukungan social
komunikasi kesehatan panjang kehamilan Faktor penentu
dapat menigkatkan rendah. minimal yang terkait anemia pada ibu hamil
pengetahuan dan dengan penurunan antara lain wanita
kesadaran sasaran, risiko kanker payudara hamil di daerah
Solusi kesehatan, jangka panjang menjadi pedesaan, petani, ibu
mempengaruhi 34 minggu, sedangkan hamil yang tidak
persepsi, keyakinan, panjang kehamilan 33 makan sayuran, ibu
dan sikap yang dapat minggu atau kurang hamil yang tidak
mengubah tidak memberikan makan daging, ibu
norma,memperkuat penurunan risiko. hamil yang
pengetahuan sikap, berpendidikan rendah,
dan perilaku. hamil yang terinfeksi
dengan parasit cacing
tambang

8.3 Pertanyaan Bagaimana Bagaiman hubungan - Adakah pengaruh Adakah pengaruh Faktor manakah yang
mana yang penggunaan pesan aktifitas fisik dengan dukungan social durasi kehamilan mempengaruhi anemia
lebih signifikan teks dapat kualitas hidup. rendah pada terhadap resiko kanker pada ibu hamil?
meningkatkan akses keterlibatan ibu payudara
informasi kesehatan hamil dalam praktik
prenatal? kesehatan yang
menguntungkan?
- Adakah pengaruh
gejala depresi pada
keterlibatan ibu
hamil dalam praktik
kesehatan yang
menguntungkan?
8.4 Diantara ide Ide dan konsep cukup Kualitas hidup lebih Ide dan konsep dalam Ide dan konsep cukup Faktor penentu anemia
dan konsep, signifikan. penting sebagai energi penelitian cukup signifikan. pada ibu hamil antara
manakah yang yang lebih tinggi signifikan. lain wanita hamil di
lebih signifikan disaat aktivitas yang
daerah pedesaan,
berhubungan dengan
pekerjaan. petani, ibu hamil yang
tidak makan sayuran,
ibu hamil yang tidak
makan daging, ibu
hamil yang
berpendidikan rendah,
hamil yang terinfeksi
dengan parasit cacing
tambang

9. Fairness Menurut saya jurnal Menurut saya, jurnal Menurut saya, jurnal ini Menurut saya jurnal ini Menurut saya jurnal
ini sudah memberikan kurang jelas pada memberikan penjelasan sudah memberikan ini sudah bagus,
penjelasan yang baik populasi karena tidak secara detail dengan penjelasan yang baik Jurnal ini sebaiknya
secara keseluruhan di jelaskan secara batasan-batasan secara keseluruhan dan disosialisasikan dan
dan mudah dipahami signifikan berapa penelitian. dan sangat mudah dipahami sesuai dikembangkan agar
sesuai kaidah jumlah populasi pada dianjurkan untuk dibaca kaidah penulisan yang menambah
penulisan yang benar. penelitian. oleh nakes benar. Namun tidak pengetahuan dan
Namun sesuai dengan dijelaskan mengapa bahan pertimbangan
judulnya terdapat mengambil responden bagi tenaga kesehatan
Afrika-Amerika di dua wilayah untuk melakukan
mungkin bisa Denmark dan asuhan kebidanan
dijelaskan mengapa Norwegia. pada ibu hamil dengan
mengambil responden anemia. melihat masih
imigran Afrika masih banyaknya ibu
Amerika. hamil yang anemia
serta kurangnya
pengetahuan tentang
anemia.
10. Belajar Aktif Abtrak : Abstrak Jurnal ini sebaikanya Jurnal ini sebaiknya di Menurut saya jurnal ini Menurut saya jurnal
sudah cukup lengkap. disampaikan kepada sosialisasikan kepada sudah bagus, dan sesuai ini sudah bagus, dan
Latar Belakang : pada tenaga kesehatan tenaga kesehatan dan dengan isu sekarang. sesuai dengan isu
latar belakang tidak sebagai acuan dalam dikembangkan untuk Jurnal ini sudah
sekarang. Jurnal ini
dijelaskan mengapa melakukan menambah memberikan penjelasan
yang diambil sebagai penyuluhan pada ibu pengetahuan serta hasil penelitian dengan sudah memberikan
responden adalah sehingga ibu sadar dituntut untuk berperan baik dan mudah penjelasan hasil
imigran Amerika- akan pentingnya aktif dalam dipahami serta telah penelitian dengan baik
Afrika aktifitas fisik. menjelaskan langkah memenuhi kaidah
dan mudah dipahami
Sampel: Sampel dan asuhan pada penulisan yang benar.
terlalu sedikit. Atau layanan esensial bagi Namun kurangnya serta telah memenuhi
mungkin juga bisa kesehatan perempuan. penelitian sebelumnya kaidah penulisan yang
pengambilan sampel Penyedia layanan yang membahas hal ini benar. implementasi
pada lebih dari 1 kesehatan, peneliti, dan sasaran sudah
klinik agar didapat pembuat kebijakan, dan tepat, namun pada
sampel yang lebih pengelola rencana pembahasan kurang
banak. kesehatan harus
spesifik dijelaskan
bekerjasama untuk
mewujudkan tentang faktor penentu
peningkatan kualitas anemia pada ibu hamil.
pelayanan pada asuhan
ibu dan anak.
JMIR MHEALTH AND UHEALTH Blackwell et al

Original Paper

Using Text Messaging to Improve Access to Prenatal Health


Information in Urban African American and Afro-Caribbean
Immigrant Pregnant Women: Mixed Methods Analysis of
Text4baby Usage

Tenya M Blackwell1, BS, MS, DrPH; LeConte J Dill2, MPH, DrPH; Lori A Hoepner1, MPH, DrPH; Laura A Geer1,
MHS, PhD
1
Department of Environmental and Occupational Health Sciences, SUNY Downstate Health Sciences University, School of Public Health, Brooklyn,
NY, United States
2
Department of Social and Behavioral Sciences, College of Global Public Health, New York University, New York, NY, United States

Corresponding Author:
Tenya M Blackwell, BS, MS, DrPH
Department of Environmental and Occupational Health Sciences
SUNY Downstate Health Sciences University
School of Public Health
450 Clarkson Avenue
Brooklyn, NY
United States
Phone: 1 7182703101
Email: tblackwell@arthurasheinstitute.org

Abstract
Background: The Text4baby (T4B) mobile health (mHealth) program is acclaimed to provide pregnant women with greater
access to prenatal health care, resources, and information. However, little is known about whether urban African American and
Afro-Caribbean immigrant pregnant women in the United States are receptive users of innovative health communication methods
or of the cultural and systematic barriers that inhibit their behavioral intent to use T4B.
Objective: This study aimed to understand the lived experiences of urban African American and Afro-Caribbean immigrant
pregnant women with accessing quality prenatal health care and health information; to assess usage of mHealth for seeking
prenatal health information; and to measure changes in participants’ knowledge, perceptions, and behavioral intent to use the
T4B mHealth educational intervention.
Methods: An exploratory sequential mixed methods study was conducted among pregnant women and clinical professionals
for a phenomenological exploration with focus groups, key informants, interviews, and observations. Qualitative themes were
aligned with behavioral and information technology communications theoretical constructs to develop a survey instrument used.
repeated-measures pre- and post-test design to evaluate changes in participants’ knowledge, attitudes, and beliefs, of mHealth
and T4B after a minimum of 4 weeks’ exposure to the text message–based intervention. Triangulation and mixing of both
qualitative and quantitative data occurred primarily during the survey development and also during final analysis.
Results: A total of 9 women participated in phase 1, and 49 patients signed up for T4B and completed a 31-item survey at
baseline and again during follow-up. Three themes were identified: (1) patient-provider engagement, (2) social support, and (3)
acculturation. With time as a barrier to quality care, inadequate patient-provider engagement left participants feeling indifferent
about the prenatal care and information they received in the clinical setting. Of 49 survey participants, 63% (31/49) strongly
agreed that T4B would provide them with extra support during their pregnancy. On a Likert scale of 1 to 5, participants’ perception
of the usefulness of T4B ranked at 4.26, and their perception of the compatibility and relative advantage of using T4B ranked at
4.41 and 4.15, respectively. At follow-up, there was a 14% increase in participants reporting their intent to use T4B and a 28%
increase from pretest and posttest in pregnant women strongly agreeing to speak more with their doctor about the information
learned through T4B.
Conclusions: Urban African American and Afro-Caribbean immigrant pregnant women in Brooklyn endure a number of social
and ecological determinants like low health literacy, income, and language that serve as barriers to accessing quality prenatal

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 1


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

health care and information, which negatively impacts prenatal health behaviors and outcomes. Our study indicates a number of
systematic, political, and other microsystem-level factors that perpetuate health inequities in our study population.

(JMIR Mhealth Uhealth 2020;8(2):e14737) doi: 10.2196/14737

KEYWORDS
Text4baby; mHealth; pregnancy; text messaging; health information; prenatal health; disparities

Available literature displays use of mHealth for smoking


Introduction cessation [12], physical activity [13], diet and weight loss [14],
Poor Birth Outcomes in Brooklyn, New York and managing chronic disease such as diabetes [15]. mHealth
text messaging services (SMS) have impacted pregnant women
Women and children of color in Brooklyn, New York, suffer in a number of ways.
inequities in health because of disproportionately higher rates
of adverse birth outcomes such as low birth weight (LBW) and Research in Canada, Saudi Arabia, and Argentina show pregnant
preterm birth. In 2014, the overall LBW (<2500 kg) rate for women positively benefiting from the use of mHealth through
Brooklyn was 8.2% compared with 8.5% for all of New York increased access to prenatal health services, improved
City and 8.1% for the state of New York [1,2]. In 2012, the information-seeking behaviors, and has provided support
national rate for LBW was at 7.99% [3]. African American throughout pregnancy with increased prenatal health knowledge
women have a 3 to 4 times higher risk than non-Hispanic/Latino and improved access to care [16-18]. Pregnant women or those
whites for adverse infant health outcomes such as LBW [4], caring for their first child are highly likely to use mHealth to
and according to Martins et al, infants born to non-Hispanic increase their prenatal health information–seeking behaviors as
black women have the highest rates of LBW (13.1%), 2 or more they have a stronger need and desire to obtain pregnancy- and
times greater than that for infants born to women of other race child health–related information [8,19,20].
and ethnic groups [4]. Much of the current literature around mHealth for pregnant
The Role of Communication women examines participants’ interests, acceptance, and the
feasibility of text messaging for improving perinatal and
Health communication researchers attest that the public health
postnatal care. For many immigrant populations, language and
community has a limited understanding of what health
speech are important factors of consideration for any health
communication can offer to the elimination of health inequities
communication endeavor either through providers or through
[5]. Evidence shows that health communication can increase
technology. A recent cross-sectional study in Germany
the intended audience’s knowledge and awareness of a health
highlights the importance of culturally tailored text messaging
issue, problem, or solution; influence perceptions, beliefs, and
and the consideration of users’ health beliefs and health literacy
attitudes that may change social norms; prompt action;
levels in message development [21]. Similarly, in a systematic
demonstrate or illustrate healthy skills; reinforce knowledge,
review, researchers underline the importance of the
attitudes, or behavior; show the benefit of behavior change;
accommodation of local languages and preferences in the
advocate a position on a health issue or policy; increase demand
content of effective text messaging programs [22].
or support for health services; refute myths and misconceptions;
and strengthen organizational relationships [5]. Dobson et al’s qualitative study corroborates the benefits of
culturally tailored mHealth programs for improved diet and
However, Freimuth and Quinn assert that health communication
exercise in pregnant women [22]; the feasibility and
alone, without environmental support, is not effective at
acceptability of a text messaging program aimed at smoking
sustaining behavioral changes at the individual level [6].
cessation for pregnant women [16] demonstrates that high
High-quality communication and a positive patient-provider
acceptance and perceived feasibility of mHealth indicate a
relationship are critical components of patient-centered quality
willingness to use and benefit from such services.
care [7]. Furthermore, engaged patients who communicate with
their providers are more likely to be treated with respect, receive These studies provide a framework for this work and depict the
adequate health information, and engage in health behaviors need to first understand users’ perceptions, acceptance, and
such as physical activity and healthy dietary behaviors [8,9]. overall intent to use mHealth for the purpose of accessing
prenatal health information.
Pregnant Women and Mobile Health
Mobile health (mHealth) has evolved as the branch of electronic Text4baby
health broadly defined as the use of mobile computing and Despite a high level of activity and interest around text
communication technologies in health care and public health messaging apps, the documented evidence on their effectiveness
[10]. It has over the last decade become a new tool used in the remains limited [23]. The Text4baby (T4B) program was
delivery of health services for disease management and designed to offer support, improve health literacy, increase
prevention in a variety of health arenas and as an innovative expectations for successful pregnancy, build the knowledge and
means to supplement traditional health communications skills to manage one’s own health, and prevent health risks by
targeting doctors, nurses, patients, or even the lay population avoiding behavioral risk factors including smoking and drinking.
[11]. Launched in 2012, it is a US mHealth information text

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 2


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

messaging service led by the US Centers for Disease Control text messaging studies have adequately incorporated the use of
and Prevention that sends free text messages to women who are theory to examine the impact, acceptance, feasibility, and
pregnant or have children younger than 1 year, providing them behavioral intent to use mHealth. The current landscape of
with information and reminders to improve their health and the mHealth and T4B research using information technology (IT)
health of their babies [17]. theories is limited [33]. There are many factors that can
influence the use of technology as a channel for prenatal health
Research on T4B has focused primarily on the content and
information within low-income urban and immigrant
frequency of the T4B messages in comparison with messages
populations, and researchers strongly point to the need for
from other pregnancy-related apps [17]. Enrollment and health
multidisciplinary frameworks that capture the complexities of
literacy among potential T4B participants have also been a focus
using mobile sources in health information behaviors [34].
of T4B evaluation [24], along with its use to promote influenza
vaccination among pregnant women [18], and for the design of Marton and Chun [35] demonstrate that an integration of
interventions to improve physical activity in pregnant women theoretical perspectives from the health sciences, social sciences,
[25]. communication, and information sciences research is necessary
to fully understand this complex behavior. This study will
Evans et al [26] emerged as a seminal empirical investigator of
leverage theoretically motivated constructs from research in
the impact of T4B on knowledge and behavioral outcomes of
consumer behavior and health information and communications
pregnant women. The earliest research published was a pilot
technology to assess participants’ knowledge, attitudes, beliefs,
study conducted with pregnant women in Fairfax County,
and behavioral intent to use T4B. Our research will add to the
Virginia, who presented for care at their local health department
current body of literature around T4B by first assessing its
[17,27]. Through a randomized controlled trial (RCT), Evans
impact on participants’ perceptions of its feasibility, acceptance,
et al found increased odds of participants feeling prepared for
compatibility, and usefulness. We seek to further fill empirical
motherhood in those exposed to T4B versus normal prenatal
gaps by utilizing theoretically motivated constructs to examine
care [26,28]. In other works, Evans et al [26] conducted an RCT
our study populations’ intent to use the T4B program for
of a group of military health service participants. Researchers
prenatal health information. This will allow practitioners and
sought to evaluate differences in adequate use of prenatal care,
program developers to predict the use of the T4B program in
as defined by the Adequacy of Prenatal Care Utilization Index,
this population to design better strategies that encourage its use
in T4B participants compared with participants not receiving
for maternal health education and risk communication in
the T4B messages; however, others attest the study’s ability to
ethnically, culturally, and socioeconomically diverse immigrant
accurately measure true behavior change [27].
communities in Brooklyn. Therefore, our research demonstrates
Effective health behavioral change programs should be guided how theory and explicit testing of mediators can be used for
by strong theoretical models [29-32]. To date, few mHealth and evaluations of T4B [36]. See Figure 1.
Figure 1. Screenshot of Text4baby messages.

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 3


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

Theoretical Underpinnings from subgroups within the black community and how these
Previous works on the individual adoption of ITs have identified differences shape pregnant women’s experiences in Brooklyn,
that a number of consumer characteristics and perceptions New York. This site is also a location where scientists,
influence adoption of IT [13]. A recent systematic review of physicians, and researchers hold expertise in risk communication
consumer health technology acceptance research points to of reproductive health issues, perinatal epidemiology, and
studies that have assessed the effects of age, income, and environmental exposure assessment specifically with the use
education on health technology acceptance; however, theoretical of biological markers. Geer et al, while characterizing important
constructs have not yet been fully considered in consumer health environmental risk factors in our target population, have
technology acceptance studies [13,37]. A combination of the indicated a need for further study and exposure reduction efforts
Theory of Planned Behavior [38,39] and Technology tailored specifically to this community [43]. Our research at
Acceptance Model was used to examine the influence of this site will expound the knowledge on innovative risk
participants’ subjective norms and perceived behavioral control communication and health promotion efforts that are most
(attitudes and beliefs) on their ability and intention to use T4B suitable and receptive for the population of pregnant women.
[40,41]. Constructs from Roger’s Diffusion of Innovation The authors have chosen not to use a pseudonym for the research
Theory were also explored in identifying valuable predictors site/research partner. Some scholars [44] agree that removing
for T4B intent [42]. In this research, our goal was to understand identifying information erases important contextual information
what it is like to be an urban and/or immigrant pregnant woman that is valuable to the research. To not anonymize location of
with accessing prenatal health care and information in Brooklyn, the research recognizes that SUNY Downstate sits within
New York, and to utilize behavioral and technology assimilation specific social, historical, cultural, environmental, geographical,
of theoretical constructs in tandem with qualitative data to and symbolic moments and meanings [45].
develop a survey instrument to measure pregnant women’s The study and protocol were approved by the Institutional
knowledge, perceptions, and behavioral intent to use the T4B Review Boards of the State University of New York Downstate
health communication program. Medical Center. Each participant signed an informed consent
The overall purpose of this study was to test a maternal health form before participation.
education intervention (T4B) to see if it improves access to This study used multiple methods of inquiry including both
prenatal health care and information, improves prenatal qualitative phenomenology and IT constructs to explore the
health-seeking behaviors in pregnant women, and determines views of pregnant women in Brooklyn, New York, on prenatal
the likelihood that pregnant women in central Brooklyn would health care and text messaging programs such as T4B to inform
adopt T4B as a viable channel for prenatal health information. the development of a quantitative instrument to measure changes
The underlying assumptions are that patients’ knowledge about in their knowledge, attitudes, beliefs, and intent to use T4B.
mHealth and T4B, their attitudes toward text messaging for
prenatal health, their subjective and normative beliefs about Methods
prenatal health information sources, their perceptions on the
usefulness and compatibility of T4B, and factors such as Overview
satisfaction and visibility of T4B will affect their acceptance of A sequential mixed approach [46] was used to first gain
and behavioral intent to use the T4B program for improved knowledge about the experiences of urban African American
access to prenatal and maternal health care and information. and Afro-Caribbean immigrant pregnant women with accessing
Research Site prenatal health care and prenatal health information at an urban
metropolitan health center in New York City. We also sought
Study participants were recruited from the SUNY Downstate
to understand participants’ perceptions about the use of mHealth
Medical Center University Hospital located in the East Flatbush
and the T4B text messaging program as a source of prenatal
section of Brooklyn, New York. East Flatbush is a community
health information and resources. We then conducted a
located in the central region of Brooklyn with a population of
repeated-measures pre- and post-test design study to measure
154,575 persons. A total of 88.00% (136,026/154,575) of the
changes in participants’ knowledge, attitudes, and beliefs on
population of East Flatbush is black, with 53% of residents born
key prenatal health behaviors, perceptions, and intent to use the
outside the United States, and almost 10% are reported to have
T4B text messaging program.
limited English proficiency. In East Flatbush, 15.6% of live
births receive late or no prenatal care, and according to the NYC Recruitment and Sampling
Department of Health and Mental Hygiene, 1 in 8 births in this The sampling techniques for the qualitative phase were driven
population are delivered preterm. The Maternal Fetal Medical by the study’s socioecological framework, which was used to
Division of the Department of Obstetrics and Gynecology at aid in the exploration and discovery of factors that serve as
Downstate provides perinatal and gynecological services for barriers or facilitators of access to prenatal care and the use of
pregnant and nonpregnant black and Afro-Caribbean women. mHealth communications among pregnant women in this
This location was chosen because of its vastly diverse urban community. Sample participants were pregnant women receiving
and immigrant black population with migrants from a number prenatal care and clinical providers of prenatal health care
of Afro-Caribbean countries including Haiti; Trinidad; and services at SUNY Downstate. Various nonprobability sampling
Jamaica, West Indies. Our research at this location offers an techniques were used during the early phase of inquiry. We
opportunity to study different social and cultural perspectives used purposeful maximum variation sampling to recruit pregnant

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 4


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

participants who (1) were aged 18 to 45 years, (2) owned a cell attitudes, beliefs, and use of mHealth and T4B; and (5) health
phone with text messaging capabilities, and (3) could information–seeking behaviors and sources.
communicate fluently in English. Creswell and Plano Clark
[47] render that maximum variation sampling captures the
Qualitative Data Collection
variation in experiences and perspectives from study Focus groups and one-on-one interviews with pregnant women
participants. They further specify that if participants are took place in a secured location at Downstate, and for
purposefully chosen to be different at onset, then the variation convenience, they were scheduled to coincide with patients’
in views will be reflected and will provide a more prenatal visits. Key informant interviews took place at
comprehensive picture of the phenomena under study [47]. We informant’s offices. Interviews averaged between 60 and 90
also chose purposive sample for participants who were able to min, with time allotted for refreshments for the pregnant
communicate fluently in English as we found that participants participants. Participants gave oral responses to the set of
from our target population who were not proficient in speaking open-ended questions. We completed a total of 2 focus groups
or reading English showed difficulty in understanding consent and 1 in-depth interview with patients and 2 separate key
forms and pretest survey questions. Many patients at Downstate informant interviews with providers. Data collection ended once
who primarily spoke Haitian creole attempted to use a mobile saturation was reached and no new information emerged as
interpretation app to translate the survey but naturally were interviews transpired. Interview data were triangulated with 3
unsuccessful. Therefore, we only recruited participants with patient observations in the natural setting of the clinic
adequate English proficiency. Expert sampling is a type of environment. Participant observations offer researchers an
purposive sampling technique that is used as expert opportunity to gain a firsthand encounter with the phenomena
elicitation—acquiring knowledge from professionals who under interest rather than relying solely on a secondhand account
possess a particular expertise [48]. We used this form of provided by participants [51]. We conducted 3 patient
purposive sampling to select clinicians from the obstetrics and observations in the clinic waiting areas during the data collection
gynecology clinic at Downstate Medical Center with experience phase. We observed patient engagement, attitudes, temperament,
providing prenatal care services to our study population as key and the receipt of prenatal health education provided from a
informants to our study. registered nurse educator from Downstate. Participants’
observation also permitted within-method triangulation and
Their expert perspective helped broaden our scope of increased validation of the dataset [51]. Care was taken to ensure
understanding the experiences of pregnant women through the research ethics, protecting patients’ anonymity, confidentiality,
eyes of both patients and providers. and respecting their wishes were met. Moms received a US $20
A total of 22 participants agreed to be in the study; however, 9 Target gift card and a round trip metro transit card (worth US
women were successfully recruited and participated in 2 focus $5.50) as incentive. Participants provided written consent to
groups, 1 one-on-one interview, and 2 key informant interviews. participate and agreed to be audio recorded during the
For phenomenological research, Creswell et al [49] recommend interviews.
a range of 5 to 25 participants; Fitzgerald et al [50] recommend
Quantitative Data Collection
a minimum sample size of 6. Our overall sample size of 9 falls
within the recommendations of these qualitative research A convenience sample of 49 pregnant women was recruited
scholars. Moreover, 7 of the 9 participants were patients at the during standard visits to undergo the T4B mHealth intervention.
clinic. Inclusion criteria were the same for phases 1 and 2 to include
pregnant women receiving care at SUNY Downstate, aged 18
The 2 key informants were clinical staff yielding a total of 9 to 45 years, who owned a cell phone with text messaging
participants for the descriptive phenomenology. Participants capabilities and were able to communicate in English.
were directly approached by the study investigator while waiting Participants were recruited while waiting for care in either the
to be seen at the clinic. They were initially recruited to clinic triage area and while waiting to see the doctor after triage
participate in semistructured focus groups; however, difficulty or waiting to receive a sonogram. Thematic findings generated
with coordinating and scheduling focus groups at the from the qualitative analysis were aligned with constructs from
convenience of the pregnant patients led to one-on-one in-depth consumer behavior, communications technology, and diffusion
interviews with patients as an alternative for data collection. theories to develop a 32-item survey for a repeated-measures
Qualitative data collection took place from March 2016 to June test of perceived usefulness, perceived behavioral control, and
2016. relative advantage of using T4B.
A standard demographic survey was completed during the The instrument was a self-administered questionnaire that
consent process to gather data on participant age, education leveraged the constructs from other validated instruments [27]
level, country of origin, race, ethnicity, insurance provider, and while also drawing on the suggested theoretical measures used
marital status. A total of 2 discussion guides were created for for research on technology acceptance [39,43], consumer
patients and providers to guide the focus groups and interviews behavior [42], and mobile technology diffusion [33,52]. The
with open-ended questions and probes to introduce selected a 32-item survey is a composite of 8 scales representing 8
priori themes: (1) access and barriers to prenatal health care and dependent variables and was administered as a pre-/post-test to
information; (2) health disparities and the built environment; assess changes in participants’ perceptions regarding the
(3) cultural, familial, and social relationships; (4) knowledge, statements. Following consent, participants were invited to use
their mobile phones to enroll in the T4B program and partake

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 5


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

in 2 surveys, 1 on the day of recruitment and a second follow-up Participants were asked to rate their agreement with statements
survey after a minimum of 4 weeks of receiving the text such as “Info from Text4baby will help me ask more questions
messages. Recruitment for the quantitative phase took place to the doctors and nurses at the clinic” and “online sources are
between October 2016 and March 2017 and continued on a useful for searching for prenatal health information.”
rolling basis until the minimum desired number of participants
Perceived Ease of Use Scale (Behavioral Control)
was reached. Upon receiving consent, we administered the
pretest survey and then assisted participants to follow the steps A 7-item scale was used to measure participant’s perceived
for signing up for T4B. After which, participants provided behavioral control for using mHealth and if they find mHealth
contact information to be reached after 4 weeks to complete a easy to engage. With a maximum score of 35, example measures
posttest survey during a subsequent prenatal visit. After a included the following: “it is easy for me to get prenatal health
minimum of 4 weeks, participants were contacted to coordinate information on my mobile phone” and “I have all the skills and
with their next prenatal visit to complete the follow-up survey. knowledge I need to use the Text4baby program.”
The posttest survey was identical to the initial baseline survey Compatibility Scale
with the addition of 1 item to assess participants’ self-report of
The compatibility scale was a 2-item scale that contained
actual reading of the text messages. Participants received a US
questions to assess the degree to which participants utilize
$20 gift card and a roundtrip transit card (worth US $5.50) for
mobile technology, particularly text messaging to communicate
their participation.
throughout their daily lives. Measured on a 5-point Likert scale,
Quantitative Measures and Instrumentation the compatibility scale asked questions such as “I communicate
regularly with friends and family through text messages.”
Attitudes Scale
This scale contained a battery of questions to assess participants’ Relative Advantage Scale
attitudes regarding key prenatal health behaviors such as diets, We wanted to assess whether participants perceived T4B to be
taking prenatal vitamins, smoking, drinking, and seeking advantageous to them for the purposes of acquiring prenatal
prenatal care and information through mHealth. Participants health information and resources. The relative advantage scale
were asked to rate their agreement with a series of statements containing 3 items was also measured on a Likert scale. Example
on a 5-point Likert scale of 1 to 5 from “strongly disagree” to measures included “using Text4baby will allow me to reach
“strongly agree.” The scale contained 8 items. The minimum healthier prenatal health goals” and “Text4baby messages will
possible score for the attitude scale was 8, and the maximum be a better source of prenatal health information for me.”
score was 40. A higher score was a reflection of a more strongly Visibility Scale
positive attitude toward the behavioral statements captured in
the items. The lack of awareness or visibility of T4B was a huge concept
that was discovered during the qualitative phase of this study.
Beliefs Scale Many of the participants had not heard of T4B despite its
The beliefs scale contained 2 items that measured participants’ widespread promotion and local advertisement. We chose to
subjective norm—the perceptions of family, peers, and persons assess visibility with a 2-item scale that contained a battery of
of influence—on the use of mHealth and T4B to obtain prenatal questions to assess participants’ agreement on whether they
health information. have seen or heard of others using T4B or if people they know
depend more on the internet and mHealth for health information.
The scale had a minimum score of 2 and a maximum score of
10. Variables specific to beliefs were adapted from previous Intent
studies of behavioral factors influencing text messaging intention Unlike other studies [33], we did not assess the strength of the
[42]. Example belief variables included the following: “family previously mentioned constructs in predicting participants’
and friends who are important to me would welcome using behavioral intent to use T4B; however, we measured behavioral
Text4baby for prenatal health information,” and they were intent using 2 items to determine the level of agreement with
measured on a 5-point scale ranging from strongly disagree to statements such as “I plan to use Text4baby for prenatal health
strongly agree. care and information measured on a 5-point Likert scale of
Perceived Usefulness Scale ‘strongly disagree’ to ‘strongly agree’.”
The perceived usefulness construct contained 6 items to assess See Tables 1 and 2 for a description of survey questionnaire
the degree to which participants perceived T4B to be useful to components and corresponding alpha coefficients.
them. The maximum score possible for the scale was 30.

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 6


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

Table 1. Questionnaire components by scale.


Scale Item Components measured Theoretical origin Response options
Attitude 1-8 Feelings on health behaviors like smoking, drinking, diet, TPBa Strongly disagree–strongly agree
health care utilization
Perceived Usefulness 11-16 Intrinsic motivations to use T4Bb due to perceived benefits TAMc Strongly disagree–strongly agree
of using
Perceived Ease of Use 17-23 Behavioral control and abilities to use text messaging for TPB, TAM Strongly disagree–strongly agree
prenatal health info
Compatibility 24-25 Perceptions whether text messaging and T4B fits into the DOId Strongly disagree–strongly agree
everyday lives
Relative advantage 26-28 Perceptions of the benefits of using T4B DOI Strongly disagree–strongly agree
Visibility 29-30 knowledge and awareness of T4B DOI Strongly disagree–strongly agree
Intent 31-32 Plans and intentions to use T4B TPB, TAM DOI Strongly disagree–strongly agree

a
TPB: Theory of Planned Behavior.
b
T4B: Text4baby.
c
TAM: Technology Acceptance Model.
d
DOI: Diffusion of Innovation Theory.

Table 2. Cronbach alpha coefficients for questionnaire by scale.


Scale Alpha coefficient Items, n Mean scale ranka
Attitude scale .661 8 —b
Beliefs scale .883 2 4.08
Perceived Usefulness scale .835 6 4.26
Perceived Ease of Use scale .718 7 3.95
Compatibility scale .806 2 4.41
Relative advantage scale .880 3 4.15
Visibility scale .193 2 —
Intent scale .914 2 4.28

a
Mean rank on a scale of 1-5 strongly disagree–strongly agree analyzed by Wilcoxon sign rank test.
b
Not applicable.

A total of 392 significant statements were extracted from 5


Analysis transcripts and broken into 9 a priori theme clusters. These
Qualitative Data Analysis clusters of significant statements were then coded using coding
methods described by Miles et al [55] and analyzed to identify
A total of 5 qualitative data sources were generated from the
emergent themes.
focus groups and interviews. Audio recordings from each
interview were transcribed and uploaded using the NVivo Quantitative Data Analysis
(version 11.0 QSR International) [53] qualitative data SPSS version 24 (IBM) was used to analyze the quantitative
management software. To ensure analytic rigor, we followed dataset. The 32- items in the instrument were analyzed both as
Colaizzi’s 7-step phenomenological approach for extracting, single Likert-type items in which frequency distributions,
organizing, and analyzing our narrative dataset [54]. With this measures of central tendency, and variance were among the
approach, significant statements made by interviewees were descriptive statistics used to summarize the variables. The 7
taken from the transcripts and grouped together to formulate subscales were also analyzed as composite Likert scales in which
themes that describe key elements of experiencing the nonparametric tests of comparison were run. Reliability of each
phenomenon, or area being studied Creswell et al [49]. scale—defined as how well a set of items within a scale
Significant statements are those most outstanding comments, measured the same underlying constructs—was determined
sentences, or quotes taken from participants that describe how based on the internal reliability using Cronbach alpha coefficient
they experienced the phenomenon [54]. Subsequently, similar [56]. Changes in participants’ attitudes and perceptions as a
significant statements are placed into clusters of meanings (or result of exposure to T4B messages between baseline and
themes). follow-up were analyzed using a matched-pairs Wilcoxon

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 7


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

sign-ranked test. We chose this statistical test over a paired (n=49) was 28 years. Approximately two-thirds (63%) of the
sample t test because of the ordinal nature of the Likert-type participants were US born, whereas the remaining were born
subscales. in either Trinidad and Tobago; Haiti; or Jamaica, West Indies
(36.7%). In addition, 15 participants (30.6%) reported that they
Results were married, and 65.3% of the participants reported not being
married or living with partner. Of the 38 participants, 38.8%
Overview had a high school diploma or the equivalent general education
A total of 58 participants were successfully recruited from the diploma, 20.4% attended technical school, and 14.3% reported
OB/GYN clinic at SUNY Downstate Medical Center for this having a 4-year college degree. A high proportion (87.8%) of
study. Moreover, 9 participants, including 7 pregnant women participants had public health insurance such as Medicaid or
and 2 clinicians, participated in the qualitative phase, and 49 Family Health Plus, whereas 4.1% (n=2) of the participants
pregnant women participated in phase 2 and completed the reported having private insurance through an employer. See
pretest and posttest surveys. The average age of the participants Tables 3 and 4 for demographic characteristics of focus group
and survey participants.

Table 3. Demographic characteristics of patients participating in focus groups and interviews.


Demographics Value, n (%)
Maternal age
20-29 4 (57)
30-39 2 (29)
40-45 1 (14)
Maternal education

High school diploma or GEDa 3 (43)

Technical school 1 (14)


College, 4-year degree 3 (43)
Maternal ethnicity
African American 6 (86)
Hispanic 1 (14)
Maternal country of birth
United States 2 (29)
Jamaica 2 (29)
Haiti 2 (29)
Trinidad 1 (13)
Maternal marital status
Married 0 (0)
Not married 7 (100)
Maternal insurance type
Public 6 (86)
Private 1 (14)

a
GED: general education diploma.

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 8


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

Table 4. Demographic characteristics of patients participating in the survey.


Demographics Value, n (%)
Age (years; n=49)
<20 3 (6)
20-34 38 (77)
35+ 6 (12)
Education (n=38)
Some high school 2 (4)

High school diploma or GEDa 19 (39)

Technical school 10 (20)


College, 4-year degree 7 (14)
Ethnicity (n=47)
African American 22 (45)
Caribbean West Indian 24 (49)
Other 1 (2)
US born (n=49)
Yes 31 (63)
No 18 (37)
Marital status (n=47)
Married 15 (31)
Single 32 (65)
Insurance (n=45)
Public 43 (88)
Private 2 (4)

a
GED: general education diploma.

This caused huge barriers in communication and engagement


Prenatal Experiences With the US Health Care System between pregnant women and providers. During an observation
A total of 3 major themes were garnered from the interviews in the waiting areas, we noticed high levels of frustration marked
and observations: (1) inadequate patient-provider engagement, by signs of huffing and puffing, constant complaints,
(2) social support, and (3) acculturation. Our qualitative findings restlessness, and high irritability, as captured in this observation
showed that time served as a huge barrier impeding an adequate field note:
level of engagement and communication between pregnant
women and clinicians at the Downstate prenatal health clinic. Patients were very irate with the wait time – says “its
Participants reported expending a large amount of miserable in here.” They report that the doctors are
time—sometimes more than 4 and 5 hours from arrival to very good and very thorough with providing
departure waiting for prenatal care. This often left many of them information and addressing concerns when asked but
feeling frustrated, impatient, and with a poor temperament having to wait so long; being pregnant, tired and
regarding the care they receive. One participant described hungry made them very angry.
dissatisfaction with her experiences, with waiting times for care Participant 2 from focus group #2 described the actual amount
creating great amount of frustration with the prenatal health of time spent in the office with doctors as “like an assembly
system: line”:
I get here earlier and then you’re still here until 1 in I feel, every time I come here I’m drained...I’m
the afternoon you know…Like…I don’t understand there...say the appointment starts from 10
that part… o’clock...I’m there at 8 o’clock...and I’m still there
Another participant chimed: to 1 o’clock...hmp...just to see him for four minutes.
As patients are moved in and out so quickly, women felt as
and after…being somewhere for 4 or 5 hours you just though they are not given enough opportunity to speak with
wanna eat and go home their doctors and ask questions or given sufficient time to engage
with providers in a manner that leads to acquiring information

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 9


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

or addressing any concerns they may have. They are reluctant to prenatal care. However, although such programs facilitate
to engage. When asked about the relationship between access to clinical prenatal care, we found that the women in our
themselves and the doctor, the women in this study perceived study more importantly emphasized the social determinants of
that “here…there’s so much of a rush…they don’t put too much prenatal health, including social systems and mHealth that
time in to do that.” Some participants expressed a desire for provided support and information and improved participants’
clinicians to “be more communicative” and articulated prenatal health-seeking behaviors.
dissatisfaction with their care as captured in the following
Women noted that the advice, information, and support from
statement:
their circle of family, friends, and other pregnant women in
Well I think the doctors need to be more…umm like Web-based chat groups made them feel more prepared for
communicative with the patients, not just come and motherhood. For many women, the internet or other mHealth
then just check you and then {oh ok everything is fine apps were a major source of prenatal health information. In the
I will give you like another appointment like next current age of mobile and digital technology, it is not surprising
week}…that’s not good. that interviewees unanimously mentioned extensive use of the
We found differences of perception between participants who internet, Google, and sites such as BabyCenter as primary go-to
were either US born, who had migrated to the United States sources for prenatal health information and also to fact-check
less than 2 years, or within 5 years or greater. Discontent over doctors. Participants were attracted to online forums and groups
the quality of prenatal care and information received came for pregnant women “with whom participants could relate” and
predominantly from younger participants, those born in the communicate with to share and learn from others’ experience:
United States, and those more acculturated. Notably, the Sometimes you go in the chat rooms...you see people
attitudes and experiences of participants who were newer doing their methods of what works...but...it gives you
immigrants were much more positive. Potentially, their increased something, it gives you a little more confidence too
exposure to the systematic and structural racism known to sometimes...you know...just to see the same amount
perpetuate the US health care industry have led to such negative of weeks or people going through the same symptoms
perspective of their prenatal health experiences. With regard to that I am...
the prenatal care she receives, 1 participant who migrated more
Similarly, a second participant expounded:
recently expressed:
Yea there’s this app called baby prep baby pregnancy
I’m from the Caribbean so…that seems like…top of
or something app, I have it on my phone...You talk to
the class to me…I’m from Trinidad…so I am content,
people all over the world...and all you have to do is
it would too that I have never seen better than this.
put in your due date, they’ll like link you up with a
So my experience would be different so to me its
bunch of people who are in your time in your
ok…its great
pregnancy...and everybody have the same
During the key informant interviews, clinical providers similarities...you know going through the same thing
described the practices at Downstate and reported that immigrant so you’ll feel more comfortable hearing from other
and pregnant women have a great deal of access to prenatal care people...around your time or whatever but doctor
through various insurance programs such as New York State wise...I don’t know
Medicaid and other pregnancy assistance programs such as
There was a sense of trust, comfort, and pleasure with being
Prenatal Care Assistance Program (PCAP), a prenatal care
able to go online for information, and many of the participants
program developed to provide comprehensive perinatal care to
spoke of the increased access they have via their mobile phones.
low-income, high-risk pregnant women. Informants shared that
The women showed strongly positive attitudes toward the use
women migrated from various countries—many Caribbean and
of T4B and articulated that receiving push messages targeted
African countries—presenting in their third term of pregnancy
specifically to their stages of pregnancy as a benefit that would
and near delivery. One clinician explained:
even save them time from seeking information on their own.
Many walk in here straight off a plane. They’re far
gone in the pregnancy and then umm with NO
Quantitative Findings
insurance. Attitudes and Beliefs Statements
There was emphasis on women appearing for services late in In general, initial attitudes toward T4B and key prenatal health
the pregnancy for the provision of care despite the lack of health behaviors were mostly neutral among pregnant women in the
insurance. study, as indicated by a mean rank score of 3.71 on the attitude
The provider also added: scale (alpha coefficient .661). A score of 4 would indicate
overall agreement. Survey results show that approximately 10%
We had a subset of patients who would travel here of respondents neither agreed nor disagreed with the statements
from out of the country, they would come here and a on the scale. Approximately 84% of the participants strongly
lot of them had their prenatal records, they would get agreed with the statement that eating 5 or more fruits and
emergency Medicaid, deliver, have their postpartum vegetables per day is important to the health of their baby, which
visit and then leave and go home reflect a 22% increase from pre- and post-test (P=.02). After
Social programs such as state Medicaid and PCAP make T4B exposure, there was a 26% increase in the amount of
provisions for women who are pregnant to qualify for access women who strongly agreed that visiting their health care
http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 10
(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

provider on a regular basis will help them be a healthy new initially had no opinion, indicated by them neither agreeing nor
mother (P=.03). There was also a 38% increase (P=.03) between disagreeing with the statement decreased from 10% and 16%
presurvey and postsurvey in the proportion of participants who before using T4B to 6.1% post T4B. T4B had low visibility
strongly agreed that using T4B will help them to have more within our study participants. A small percentage (8.2%)
support during pregnancy. During posttest, 51.0% of survey reported having seen or heard of someone using T4B. A larger
respondents strongly agreed with the statement “text4baby will proportion of respondents neither agreed nor disagreed (30.6%)
help me to get new information about prenatal health” as and others either disagreed or strongly disagreed (24.5% and
opposed to 39% during pretest—reflecting an increase of nearly 16.3%, respectively) about having seen or heard of T4B use.
27%. Although many participants neither agreed nor disagreed
on whether relatives and those close to them would support the
Behavioral Intent to Use Text4baby
use of mHealth and T4B (20%), after exposure results showed Study participants largely reported their intent to use the T4B
a 12% increase in those who strongly agreed with that statement. program (rank score 4.28). A total of 47% and 46%,
respectively, agreed and strongly agreed that they plan to use
Perceived Usefulness and Perceived Behavioral Control T4B for accessing prenatal health care and information.
Statements
Similarly, 91.8% of the participants strongly agreed to speak
The perceived usefulness of T4B improved in survey more to their doctor about information they learn through T4B.
respondents after exposure to the text messages. Initially, a
moderate proportion of participants neither agreed nor disagreed
that the T4B messages will help to have a healthier pregnancy
Discussion
(26.5%). During the same time, 28.6% of respondents strongly Mixed Findings and Implications (for Research, Policy,
agreed. However, at posttest, the proportion of participants who and Practice)
strongly agreed increased to 46.9% (P=.02). These results
indicate a positive shift in attitude regarding T4B’s usefulness. The number of mHealth educational interventions for pregnant
In contrast, strong agreement with the statement “online sources women is rapidly evolving, but research in this area—although
are helpful for searching prenatal health information” declined growing— is still limited. Before this study, there existed no
from initial testing to follow-up (from 46.9% to 40.8%). At the knowledge as to what determinants influenced T4B usage
same time, the proportion of respondents who neither agreed intentions and if participants’ attitudes, beliefs, and perceptions
nor disagreed increased from 6.1% to 14.3%, indicating a shift would improve as a result of receiving the text messages. There
to more neutral attitudes in the usefulness of T4B. The are no studies that theoretically measure constructs of consumer
proportion of women who believed that they find it easy to health behavior, technology acceptance, and diffusion to
receive prenatal health information on their mobile phone conceptualize intent to use the T4B mHealth program. This is
increased slightly from 57.1% to 59.2%. In addition, the the first study to examine changes in attitudes, beliefs, and
proportion of women who strongly agreed that T4B messages perceptions among urban African American and Afro-Caribbean
will allow them to have greater control over their prenatal health immigrant pregnant women after exposure to T4B, and it
care increased by 56% between pretest and posttest from 28.6% provides novel insights by examining how T4B usage intentions
of participants to 51% (P=.02). However, in contrast, there was may be influenced by perceived usefulness, relative advantage,
a slight increase in strong agreement that “I have the skills perceived behavioral controls, and its compatibility within this
needed to use Text4baby,” and there was an increase from 4% study’s population.
to 14% in those having no opinion on that statement. Despite the growing number of research endeavors investigating
Approximately 10% of the women surveyed agreed that reading mHealth and T4B [9,57,58], none have used a sequential
English is sometimes difficult for them. exploratory mixed methods design incorporating qualitative
Compatibility, Relative Advantage, and Visibility phenomenology followed by repeated-measures pre-/post-test
design around T4B intervention. Our investigation revealed that
Statements
pregnant women often felt that the information they received
A large percentage (85%) of respondents either agreed or during prenatal visits was not adequate at meeting their health
strongly agreed with the compatibility of T4B messages by communication needs; however, they believed that mHealth
self-reporting regular use and communication via text and T4B could increase their access to health care and
messaging. A small portion (6%) either disagreed or strongly information. When asked how receptive they were to using T4B
disagreed with the statement “I communicate regularly with and receiving prenatal health text messages on their cellphones,
friends and family through text messages,” suggesting high respondents replied:
usage of text messaging for communication and a strong
compatibility with T4B’s mode of disseminating information. I wouldn’t mind that cause...these phones now a days
Participant’s perceptions about the relative advantage of using who don’t have messages just popping up out of
T4B improved after receiving the T4B messages. Overall, everywhere; yea I think it great cause instead of like
participants agreed (mean score 4.15) with the items on the going to google...and trying to type you just receive
relative advantage scale. There were significant increases in the a text and they tell you click the link I think it’s easier
proportion of respondents who strongly agreed with the Survey respondents were later asked to rate on a 5-point Likert
statement “using Text4baby will allow me to reach healthier scale their level of agreement with the statement “Text4baby
prenatal health goals” and the proportion of respondents who will help me to get new information about prenatal health.”

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 11


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

Although 51% of the participants strongly agreed, approximately examination and prediction of T4B use through an initial
10% of the participants remained neutral after having received assessment of patients’ knowledge and perceptions regarding
the T4B messages. A 2012 study of pregnant women attending its use. Second, the study of consumer health behavior and IT
public hospitals and antenatal care centers in Argentina found uses the factors associated with mHealth, and text message use
that a vast majority (95.9%) of the women reported willingness provides strategic targets for prevention and intervention through
to receive SMS messages during pregnancy [59]. A study of the design of cogent strategies that encourage its use among
pregnant women and health care professionals also revealed patients at Downstate.
that pregnant women believed 3 SMS messages per week was
New York State Department of Health is currently in year 3 of
an appropriate and preferred dose of SMS message to receive
a 5-year endeavor to redesign health care delivery systems for
during pregnancy [9].
residents in the State Delivery Systems Reform Incentive
We found that pregnant women often placed greater value on Payment program. There is a renewed focus on nonclinical
their social support system over clinical prenatal care services social determinants of health and the provision of value-based
for complete and quality care. This included family, peers, social care by community health organizations that provide health
networks, and online communities for pregnant women and education and promotion services for people with low
government social programs such as the Woman, Infant, and socioeconomic status. This research implies opportunities for
Children nutritional assistance programs. This was most notable health policy decisionmakers to further investigate, develop,
as many women expressed great dissatisfaction with the lack and implement nontraditional patient-centered prenatal health
of engagement they have with providers. Other researchers have care services that are better positioned to address the many
suggested that one potential explanation for improved outcomes health, education, and communication barriers faced by low
amongst pregnant black women is the provision of social income pregnant women in Brooklyn New York. This research
support, coping strategies, and stress reduction through group also implies the use of mHealth and text messaging to
prenatal care [60]. communication environmental health and prenatal risk
assessment messages for women in Brooklyn; and for
With regard to care and information, responds alluded to using
environmental and population health surveillance as early
mHealth as a support to check information provided to them by
warning signs of emerging public health threats, and as
doctors:
emergency information systems in natural disasters or pandemics
I even look up certain things that I don’t feel that’s [36].
right that the doctor, whatever the doctor say I look
it over just to make sure they not giving the wrong
Strengths and Limitations
information cause you know sometimes...people do The strengths of this study include the robust survey; sampling
make mistakes...you know...but...but just to make sure and analysis methods; and the triangulation of the qualitative
I’m ok and my baby’s is safe...I’ll look it over...do the data with focus groups, key informants, and observations. In
research...that’s...that’s what it’s about the internet addition, the development of a survey based on theoretically
is everything for me lol. driven constructs of technology acceptance, innovation
Our findings extend prior research [61] which showed that diffusion, and theory of planned behavior offers added strength.
quality prenatal care must equally weigh on other nonclinical There are a number of limitations to this study, namely, the
factors, such as interpersonal care processes like attitude and small sample size and the use of convenience sample, which
emotional support; and structure of care including access and can introduce sampling biases such as nonresponse and selection
physical setting; and care provider characteristics as a part of bias. This does not allow us to generalize to other populations
quality clinical prenatal care. Overall, our findings corroborate of pregnant women; however, results may be indicative to
with others to confirm high acceptability [16] and feasibility similar urban and immigrant populations. The nature of pretest
[17] for T4B and similar text messaging interventions for and posttest designs can also introduce biases due to response
pregnant women. Given the high population of Afro-Caribbean shift and maturation.
immigrants with limited English proficiency and multiple Conclusions
dialects spoken, we believe that a tailored mHealth program
T4B is a text messaging program that provides prenatal care
should be considered for this population to supplement access
messages to pregnant women and new mothers. It uses a
to information and resources. Patient-centered approaches that
partnership model with health care facilities often serving as
leverage partnerships between health care providers and
local implementation partners [36]. Although mHealth
community-based organizations could provide patients with
interventions have been proposed as effective solutions to
access to culturally competent doulas and other community
improve maternal and neonatal health [56], this study showed
health workers in a novel way to increase engagement, support,
that the use of mHealth for prenatal health information was
and educational opportunities during pregnancy.
quite common, whereas internet searches, Google, and
Future Implications pregnancy-related app usage was most widespread. Receiving
This research has a number of important implications for prenatal health electronic messages through texting is a positive
research, policy, and practice around mHealth and T4B. First, avenue and highly compatible to provide pregnant women in
it provides a framework for more robust evaluation of the effects central Brooklyn with information; however, more research
of T4B in this population of pregnant women by fostering an with a larger population and direct modeling of testing of the
theoretical constructs is needed to fully assess the perceived

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 12


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

usefulness and relative advantage of T4B in this population. pregnancy goals, it is important that any mHealth endeavor
Although there was moderate intent to use the T4B program must first be designed and tailored with the inclusion of those
possibly because of its facilitation in women accessing targeted to ensure that the messages and content are relevant
information, gaining more control, and reaching healthier and for a specific place-based population.

Acknowledgments
This study presents the original dissertation research funded by the University Hospital of Brooklyn SUNY Downstate Medical
Center President’s Health Disparities fund. The contents of this publication are solely the responsibility of the authors and do not
necessarily represent the official views of SUNY Downstate Medical Center. The authors would like to thank the clinicians and
staff in the Department of Obstetrics and Gynecology at SUNY Downstate as well as their graduate research assistant Ludmila
Ferruzzi for their support of this work. The authors especially like to thank the study participants for their time and effort.

Conflicts of Interest
None declared.

References
1. Li W, Huynh M, Lee E. New York City Department of and Mental Hygiene. Summary of Vital Statistics, 2014 URL: https:/
/www1.nyc.gov/assets/doh/downloads/pdf/vs/2014sum.pdf [accessed 2018-10-29] [WebCite Cache ID 73Xn7AfCI]
2. New York State Department of Health. New York State Health Indicator Report - Percentage Low Birth Weight URL:
https://www.health.ny.gov/statistics/chac/birth/b37.htm [accessed 2018-10-30] [WebCite Cache ID 73Xo5H4oA]
3. Martin J, Hamilton BE, Osterman MJ, Curtin SC, Matthews TJ. Births: final data for 2012. Natl Vital Stat Rep 2013 Dec
30;62(9):1-68 [FREE Full text] [Medline: 25671704]
4. Matthews TJ, MacDorman MF, Thoma ME. Infant mortality statistics from the 2013 period linked birth/infant death data
set. Natl Vital Stat Rep 2015 Aug 06;64(9):1-30 [FREE Full text] [Medline: 26270610]
5. Thomas SB, Fine MJ, Ibrahim SA. Health disparities: the importance of culture and health communication. Am J Public
Health 2004 Dec;94(12):2050. [doi: 10.2105/ajph.94.12.2050] [Medline: 15612166]
6. Freimuth VS, Quinn SC. The contributions of health communication to eliminating health disparities. Am J Public Health
2004 Dec;94(12):2053-2055. [doi: 10.2105/ajph.94.12.2053] [Medline: 15569949]
7. Attanasio L, Kozhimannil KB. Patient-reported communication quality and perceived discrimination in maternity care.
Med Care 2015 Oct;53(10):863-871 [FREE Full text] [doi: 10.1097/MLR.0000000000000411] [Medline: 26340663]
8. Guendelman S, Broderick A, Mlo H, Gemmill A, Lindeman D. Listening to communities: mixed-method study of the
engagement of disadvantaged mothers and pregnant women with digital health technologies. J Med Internet Res 2017 Jul
05;19(7):e240 [FREE Full text] [doi: 10.2196/jmir.7736] [Medline: 28679489]
9. Huberty J, Dinkel D, Beets MW, Coleman J. Describing the use of the internet for health, physical activity, and nutrition
information in pregnant women. Matern Child Health J 2013 Oct;17(8):1363-1372. [doi: 10.1007/s10995-012-1160-2]
[Medline: 23090284]
10. Cené CW, Roter D, Carson KA, Miller ER, Cooper LA. The effect of patient race and blood pressure control on
patient-physician communication. J Gen Intern Med 2009 Sep;24(9):1057-1064 [FREE Full text] [doi:
10.1007/s11606-009-1051-4] [Medline: 19575270]
11. Roter DL, Stewart M, Putnam SM, Lipkin M, Stiles W, Inui TS. Communication patterns of primary care physicians. J
Am Med Assoc 1997;277(4):350-356. [Medline: 9002500]
12. Rai A, Chen L, Pye J, Baird A. Understanding determinants of consumer mobile health usage intentions, assimilation, and
channel preferences. J Med Internet Res 2013 Aug 02;15(8):e149 [FREE Full text] [doi: 10.2196/jmir.2635] [Medline:
23912839]
13. Free C, Phillips G, Felix L, Galli L, Patel V, Edwards P. The effectiveness of M-health technologies for improving health
and health services: a systematic review protocol. BMC Res Notes 2010 Oct 06;3:250 [FREE Full text] [doi:
10.1186/1756-0500-3-250] [Medline: 20925916]
14. Free C, Whittaker R, Knight R, Abramsky T, Rodgers A, Roberts IG. Txt2stop: a pilot randomised controlled trial of mobile
phone-based smoking cessation support. Tob Control 2009 May;18(2):88-91. [doi: 10.1136/tc.2008.026146] [Medline:
19318534]
15. Fukuoka Y, Vittinghoff E, Jong SS, Haskell W. Innovation to motivation--pilot study of a mobile phone intervention to
increase physical activity among sedentary women. Prev Med 2010;51(3-4):287-289 [FREE Full text] [doi:
10.1016/j.ypmed.2010.06.006] [Medline: 20600263]
16. Aranda-Jan CB, Mohutsiwa-Dibe N, Loukanova S. Systematic review on what works, what does not work and why of
implementation of mobile health (mHealth) projects in Africa. BMC Public Health 2014 Mar 21;14:188 [FREE Full text]
[doi: 10.1186/1471-2458-14-188] [Medline: 24555733]

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 13


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

17. US Department of Health and Human Services. 2014. Using Health Text Messages to Improve Consumer Health Knowledge,
Behaviors, and Outcomes URL: https://www.hrsa.gov/sites/default/files/archive/healthit/txt4tots/environmentalscan.pdf
[accessed 2015-03-24]
18. Gazmararian JA, Yang B, Elon L, Graham M, Parker R. Successful enrollment in Text4Baby more likely with higher health
literacy. J Health Commun 2012;17(Suppl 3):303-311. [doi: 10.1080/10810730.2012.712618] [Medline: 23030578]
19. Ferrer-Roca O, Cárdenas A, Diaz-Cardama A, Pulido P. Mobile phone text messaging in the management of diabetes. J
Telemed Telecare 2004;10(5):282-285. [doi: 10.1258/1357633042026341] [Medline: 15494086]
20. Wallwiener S, Müller M, Doster A, Laserer W, Reck C, Pauluschke-Fröhlich J, et al. Pregnancy eHealth and mHealth: user
proportions and characteristics of pregnant women using Web-based information sources-a cross-sectional study. Arch
Gynecol Obstet 2016 Nov;294(5):937-944. [doi: 10.1007/s00404-016-4093-y] [Medline: 27084763]
21. Jang J, Dworkin J, Hessel H. Mothers' use of information and communication technologies for information seeking.
Cyberpsychol Behav Soc Netw 2015 May;18(4):221-227. [doi: 10.1089/cyber.2014.0533] [Medline: 25803204]
22. Dobson R, Whittaker R, Bartley H, Connor A, Chen R, Ross M, et al. Development of a culturally tailored text message
maternal health program: TextMATCH. JMIR Mhealth Uhealth 2017 May 20;5(4):e49 [FREE Full text] [doi:
10.2196/mhealth.7205] [Medline: 28428159]
23. Abroms LC, Johnson PR, Heminger CL, Van Alstyne JM, Leavitt LE, Schindler-Ruwisch JM, et al. Quit4baby: results
from a pilot test of a mobile smoking cessation program for pregnant women. JMIR Mhealth Uhealth 2015 Jan 23;3(1):e10
[FREE Full text] [doi: 10.2196/mhealth.3846] [Medline: 25650765]
24. Bahanshal S, Coughlin S, Liu B. For You and Your Baby (4YYB): adapting the centers for disease control and prevention's
Text4Baby program for Saudi Arabia. JMIR Res Protoc 2017 Mar 28;6(2):e23 [FREE Full text] [doi: 10.2196/resprot.5818]
[Medline: 28246065]
25. Bushar JA, Kendrick JS, Ding H, Black CL, Greby SM. Text4baby influenza messaging and influenza vaccination among
pregnant women. Am J Prev Med 2017 Dec;53(6):845-853 [FREE Full text] [doi: 10.1016/j.amepre.2017.06.021] [Medline:
28867143]
26. Evans WD, Wallace JL, Snider J. Pilot evaluation of the text4baby mobile health program. BMC Public Health 2012 Dec
26;12:1031 [FREE Full text] [doi: 10.1186/1471-2458-12-1031] [Medline: 23181985]
27. Huberty J, Rowedder L, Hekler E, Adams M, Hanigan E, McClain D, et al. Development and design of an intervention to
improve physical activity in pregnant women using Text4baby. Transl Behav Med 2016 Jun;6(2):285-294 [FREE Full text]
[doi: 10.1007/s13142-015-0339-7] [Medline: 27356999]
28. Remick AP, Kendrick JS. Breaking new ground: the text4baby program. Am J Health Promot 2013;27(3 Suppl):S4-S6
[FREE Full text] [doi: 10.4278/ajhp.27.3.c2] [Medline: 23286662]
29. van Velthoven MH, Majeed A, Car J. Text4baby - national scale up of an mHealth programme. Who benefits? J R Soc
Med 2012 Nov;105(11):452-453 [FREE Full text] [doi: 10.1258/jrsm.2012.120176] [Medline: 23257962]
30. Ybarra ML, Holtrop JS, Ba ci Bosi AT, Emri S. Design considerations in developing a text messaging program aimed at
smoking cessation. J Med Internet Res 2012 Jul 24;14(4):e103 [FREE Full text] [doi: 10.2196/jmir.2061] [Medline:
22832182]
31. Lichtenstein E, Zhu S, Tedeschi GJ. Smoking cessation quitlines: an underrecognized intervention success story. Am
Psychol 2010;65(4):252-261 [FREE Full text] [doi: 10.1037/a0018598] [Medline: 20455619]
32. Johnson WD, Diaz RM, Flanders WD, Goodman M, Hill AN, Holtgrave D, et al. Behavioral interventions to reduce risk
for sexual transmission of HIV among men who have sex with men. Cochrane Database Syst Rev 2008(3):CD001230.
[doi: 10.1002/14651858.CD001230.pub2] [Medline: 18646068]
33. Gaglio B, Smith TL, Estabrooks PA, Ritzwoller DP, Ferro EF, Glasgow RE. Using theory and technology to design a
practical and generalizable smoking reduction intervention. Health Promot Pract 2010 Sep;11(5):675-684. [doi:
10.1177/1524839908324778] [Medline: 19116418]
34. Almatari A, Noorminshah A, Ali S. Journal of Information Systems Research and Innovation (JISRII)5 (2013). 2013.
Factors influencing students' intention to use mlearning URL: https://seminar.utmspace.edu.my/jisri/download/Vol5/
Pub1_Factors_to_Use_Mobile_learning.pdf
35. Marton C, Wei Choo C. A review of theoretical models of health information seeking on the web. J Doc 2012 Apr
20;68(3):330-352. [doi: 10.1108/00220411211225575]
36. Sondaal SF, Browne JL, Amoakoh-Coleman M, Borgstein A, Miltenburg AS, Verwijs M, et al. Assessing the effect of
mHealth interventions in improving maternal and neonatal care in low-and middle-income countries: a systematic review.
PLoS One 2016;11(5):e0154664 [FREE Full text] [doi: 10.1371/journal.pone.0154664] [Medline: 27144393]
37. Warren J, Kvasny L, Hecht M, Burgess D, Ahluwalia J, Okuyemi K. Barriers, control and identity in health information
seeking among African American women. J Health Dispar Res Pract 2009;3(3):5 [FREE Full text]
38. Ajzen I. From Intention to Actions: A theory of Planned Behavior. In: Action Control. New York, NY: Springer; 1985:a.
39. Ajzen I. The theory of planned behavior. Organizational Behavior and Human Decision Processes 1991 Dec;50(2):179-211.
[doi: 10.1016/0749-5978(91)90020-t]
40. Davis FD. Perceived usefulness, perceived ease of use, and user acceptance of information technology. MIS Q 1989
Sep;13(3):319-340. [doi: 10.2307/249008]

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 14


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

41. Davis FD. User acceptance of information technology: system characteristics, user perceptions and behavioral impacts. Int
J Man Mach Stud 1993 Mar;38(3):475-487. [doi: 10.1006/imms.1993.1022]
42. Rogers E. Diffusion of innovations5.1.38 (2003). 2003. Elements of diffusion URL: https://teddykw2.files.wordpress.com/
2012/07/everett-m-rogers-diffusion-of-innovations.pdf
43. Geer LA, Persad MD, Palmer CD, Steuerwald AJ, Dalloul M, Abulafia O, et al. Assessment of prenatal mercury exposure
in a predominately Caribbean immigrant community in Brooklyn, NY. J Environ Monit 2012 Mar;14(3):1035-1043. [doi:
10.1039/c2em10835f] [Medline: 22334237]
44. Thomson D, Bzdel L, Golden-Biddle K, Reay, Trish & Estabrook, Carole A. Central questions of anonymization: a case
study of secondary use of qualitative data. Forum Qual Soc Res 2005;6(1):- [FREE Full text]
45. Dill LJ. "Wearing My Spiritual Jacket": the role of spirituality as a coping mechanism among African American youth.
Health Educ Behav 2017 Oct;44(5):696-704. [doi: 10.1177/1090198117729398] [Medline: 28882071]
46. Hubbard W, Sandmann L. Using diffusion of innovation concepts for improved program evaluation. Journal of Extension
2007:154-161.
47. Yu CH. Designing and Conducting Mixed Methods Research. In: Organizational Research Methods. Thousand Oaks, CA:
Sage Publications; Aug 15, 2008:801-804.
48. Leard Dissertation. Purposive Sampling URL: http://dissertation.laerd.com/purposive-sampling.php
49. Creswell JW, Hanson WE, Clark Plano VL, Morales A. Qualitative research designs. Counsel Psychol 2016 Jun
30;35(2):236-264. [doi: 10.1177/0011000006287390]
50. Fitzgerald EM, Cronin SN, Boccella SH. Anguish, yearning, and identity: toward a better understanding of the pregnant
Hispanic woman's prenatal care experience. J Transcult Nurs 2016 Sep;27(5):464-470. [doi: 10.1177/1043659615578718]
[Medline: 25838327]
51. Merriam S, Tisdell EJ. Qualitative Research: A Guide to Design and Implementation, 4th Edition. New York: Wiley Inc;
2015:-.
52. Phan K, Daim T. Exploring technology acceptance for mobile services. J Ind End Manag 2011 Jul 14;4(2). [doi:
10.3926/jiem.2011.v4n2.p339-360]
53. Evans W, Nielsen PE, Szekely DR, Bihm JW, Murray EA, Snider J, et al. Dose-response effects of the text4baby mobile
health program: randomized controlled trial. JMIR Mhealth Uhealth 2015;3(1):e12 [FREE Full text] [doi:
10.2196/mhealth.3909] [Medline: 25630361]
54. Colaizzi PF. Psychological research as the phenomenologist views. In: Existential-Phenomenological Alternatives for
Psychology. Oxford United Kingdom: Oxford University Press; 1978:48-71.
55. Miles M, Huberman M, Saldana J. Sage publications. 2013. Qualitative data analysis URL: http://www.theculturelab.umd.edu/
uploads/1/4/2/2/14225661/miles-huberman-saldana-designing-matrix-and-network-displays.pdf
56. Geer LA, Curbow BA, Anna DH, Lees PS, Buckley TJ. Development of a questionnaire to assess worker knowledge,
attitudes and perceptions underlying dermal exposure. Scand J Work Environ Health 2006 Jun;32(3):209-218 [FREE Full
text] [doi: 10.5271/sjweh.1001] [Medline: 16804624]
57. Foster J, Miller L, Isbell S, Shields T, Worthy N, Dunlop AL. mHealth to promote pregnancy and interconception health
among African-American women at risk for adverse birth outcomes: a pilot study. Mhealth 2015;1:20 [FREE Full text]
[doi: 10.3978/j.issn.2306-9740.2015.12.01] [Medline: 28293578]
58. Cormick G, Kim NA, Rodgers A, Gibbons L, Buekens PM, Belizán JM, et al. Interest of pregnant women in the use of
SMS (short message service) text messages for the improvement of perinatal and postnatal care. Reprod Health 2012;9:9
[FREE Full text] [doi: 10.1186/1742-4755-9-9] [Medline: 22866753]
59. Sword W, Heaman MI, Brooks S, Tough S, Janssen PA, Young D, et al. Women's and care providers' perspectives of
quality prenatal care: a qualitative descriptive study. BMC Pregnancy Childbirth 2012 Apr 13;12:29 [FREE Full text] [doi:
10.1186/1471-2393-12-29] [Medline: 22502640]
60. Scott KA, Britton L, McLemore MR. The ethics of perinatal care for black women: dismantling the structural racism in
"Mother Blame" narratives. J Perinat Neonatal Nurs 2019;33(2):108-115. [doi: 10.1097/JPN.0000000000000394] [Medline:
31021935]
61. Whittaker R. Issues in mHealth: findings from key informant interviews. J Med Internet Res 2012;14(5):e129 [FREE Full
text] [doi: 10.2196/jmir.1989] [Medline: 23032424]

Abbreviations
IT: information technology
LBW: low birth weight
mHealth: mobile health
RCT: randomized controlled trial
T4B: Text4baby

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 15


(page number not for citation purposes)
XSL• FO
RenderX
JMIR MHEALTH AND UHEALTH Blackwell et al

Edited by G Eysenbach; submitted 17.05.19; peer-reviewed by J Constantin, P Ware, C Calyx; comments to author 10.07.19; revised
version received 01.11.19; accepted 16.12.19; published 13.02.20
Please cite as:
Blackwell TM, Dill LJ, Hoepner LA, Geer LA
Using Text Messaging to Improve Access to Prenatal Health Information in Urban African American and Afro-Caribbean Immigrant
Pregnant Women: Mixed Methods Analysis of Text4baby Usage
JMIR Mhealth Uhealth 2020;8(2):e14737
URL: http://mhealth.jmir.org/2020/2/e14737/
doi: 10.2196/14737
PMID:

©Tenya M Blackwell, LeConte J Dill, Lori A Hoepner, Laura A Geer. Originally published in JMIR mHealth and uHealth
(http://mhealth.jmir.org), 13.02.2020. This is an open-access article distributed under the terms of the Creative Commons Attribution
License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any
medium, provided the original work, first published in JMIR mHealth and uHealth, is properly cited. The complete bibliographic
information, a link to the original publication on http://mhealth.jmir.org/, as well as this copyright and license information must
be included.

http://mhealth.jmir.org/2020/2/e14737/ JMIR Mhealth Uhealth 2020 | vol. 8 | iss. 2 | e14737 | p. 16


(page number not for citation purposes)
XSL• FO
RenderX
International Journal of
Environmental Research
and Public Health

Article
Relationships between Physical Activity and Quality
of Life in Pregnant Women in the Second and
Third Trimester
Justyna Krzepota 1, * , Dorota Sadowska 2 and Elżbieta Biernat 3
1 Department of Physical Culture and Health Promotion, University of Szczecin, al. Piastów 40b, blok 6,
71-065 Szczecin, Poland
2 Department of Physiology, Institute of Sport—National Research Institute, ul. Trylogii 2/16,
01-982 Warsaw, Poland; sadowska.dorota@hotmail.com
3 Department of Tourism, Collegium of World Economy, Warsaw School of Economics, al. Niepodległości 162,
02-554 Warsaw, Poland; elzbieta.biernat@sgh.waw.pl
* Correspondence: justyna.krzepota@usz.edu.pl

Received: 26 October 2018; Accepted: 3 December 2018; Published: 5 December 2018 

Abstract: Background: The problem of an inadequate level of physical activity (PA) is important
in the context of its relationship with the quality of life (QoL) of pregnant women. The aim of this
study was to analyze the relationships between PA and QoL among pregnant women. Methods:
The study analyzed 346 questionnaires filled in by pregnant women (157 in the second trimester
and 189 in the third). The tool used for assessment of PA was the Pregnancy Physical Activity
Questionnaire-Polish version (PPAQ-PL). The quality of life (QoL) was assessed by the World Health
Organization Quality of Life Questionnaire-short form (WHOQoL-Bref). The results obtained from
the PPAQ-PL and WHOQoL-Bref questionnaires for women in the second and third trimesters of
pregnancy and intergroup differences were analyzed. Results: There was a significant correlation
in the group of women in the second trimester of pregnancy between quality of life in the physical
health domain and the intensity and type of physical activity. The women who rated their quality of
life higher in this domain declared higher energy expenditures (EE) associated with vigorous activity
(R = 0.159, p ≤ 0.05), as well as with occupational activity (R = 0.166; p ≤ 0.05) and sport/exercise activity
(R = 0.187; p ≤ 0.05). In women in the third trimester, higher EE related to sport/exercise activity
coincided with higher assessments of the overall quality of life (R = 0.149, p ≤ 0.05) and general health
(R = 0.170, p ≤ 0.05). In the case of the psychological domain (R = 0.161, p ≤ 0.05) and social relationship
domain (R = 0.188; p ≤ 0.05) of QoL, positive correlations occurred with EE related to vigorous activity.
In contrast, high assessment of physical health domain coincided with higher EE related to occupational
activity (R = 0.174; p ≤ 0.05). Conclusions: Our study makes an important contribution to knowledge
concerning the correlations between PA and QoL in pregnancy. The results suggest the need for
improvement in prenatal care and promotion of PA programs for pregnant women.

Keywords: physical activity in pregnancy; PPAQ; quality of life; WHOQoL-Bref; pregnant women

1. Introduction
The prevalence of an insufficient level of physical activity (PA) in pregnant women has been
demonstrated in studies using representative samples in different countries [1–4]. Despite the
well-documented benefits of involvement in PA in this period of life [5–7], it is emphasized that
pregnancy continues to be one of the causes of a substantial reduction in PA [8–10].
Over the past two decades, most studies which have focused on these problems have estimated
that most pregnant women do not participate in recommended PA. Clark and Gross [11] demonstrated

Int. J. Environ. Res. Public Health 2018, 15, 2745; doi:10.3390/ijerph15122745 www.mdpi.com/journal/ijerph
Int. J. Environ. Res. Public Health 2018, 15, 2745 2 of 12

that 39% of women who reported participating in some forms of weekly exercise before pregnancy
did not report pursuing any similar activities during pregnancy. Similarly, Fell et al. [12], in a
comparative study of women’s levels of PA during early pregnancy and during the year before
pregnancy, observed that most women reduced their PA levels during the first 20 weeks of pregnancy
compared with their level of activity during the year prior to pregnancy.
According to the data presented by Evenson et al. [1], only 15.8% of pregnant women in the USA
reported being active, in accordance with the recommendations. In a cohort study conducted in Brazil,
Domingues and Barros [2] estimated that only 4.3% of women were active during the whole pregnancy.
Furthermore, [13] found that only 14.6% of women in mid-pregnancy in Norway were involved in
the exercise ≥3 times a week, >20 min at moderate intensity. According to Santo et al. [4], merely 9%
of 1584 pregnant women met the American College of Obstetrics and Gynecology ACOG guidelines.
Furthermore, nearly half of the women reported PA < 1 day/week during the third trimester. Similarly,
Haakstad et al. [3] found that only 11% of pregnant women followed ACOG guidelines regarding PA.
The problem of inadequate levels of PA is particularly important in the context of the relationship
of PA to the quality of life (QoL) of pregnant women. Recently published studies have provided
important information on changes that occur in health-related QOL (HRQoL), both during pregnancy
and [14] in the perinatal period [15]. A problem that remains to be discussed is the explanation of
the relationships between PA and the quality of life of pregnant women [16–20]. No unambiguous
findings have been published to date in this area, since interpretation is difficult due to the use of
different measurement tools, both for the evaluation of PA during pregnancy and the quality of
life. For example, some researchers have used the results obtained with the Global Physical Activity
Questionnaire (GPAQ) and 36-Item Short-Form Health Survey (SF-36) [20], while others have used
the Pregnancy Physical Activity Questionnaire (PPAQ) and the abridged World Health Organization
Quality of Life (WHOQoL-Bref) [16,18]. In addition to these tools, other questionnaires have been
popular and are frequently used in the assessment of the quality of life, with an extensive review and
discussion of their use being presented by Mogos et al. [21].
Despite many analyses, the problem of correlations between PA and the quality of life of pregnant
women remains to be solved and still raises many questions that need to be addressed. To the best of
our knowledge, the few studies that have used the PPAQ and WHOOoL-Bref tools [16,18] have failed
to analyze the Polish population. Therefore, the aim of this study was to obtain information about the
relationships between PA and QoL among pregnant women in Poland. The QoL was evaluated by a
reliable questionnaire used in surveys of pregnant women (WHOQoL-Bref) [16,22–24], whereas PA
was measured using the increasingly popular PPAQ questionnaire [25–34]. Furthermore, we hope
that the choice of the above measurement tools will allow for replication of the study results and
comparison with future research conducted on a wider scale.

2. Material and Methods


The study analyzed 346 questionnaires filled in correctly by pregnant women (157 in the second
trimester and 189 in the third). The data were directly distributed among pregnant women who
participated in activities for pregnant women organized within antenatal classes or in fitness clubs in
Szczecin and Warsaw, Poland. The survey was anonymous and conducted only in places where consent
was obtained. The respondents consisted only of volunteers. In each case, the survey supervisor
presented the purpose and scope of the research to the respondents and instructed them on how to
complete the questionnaires. The method “pen and paper” was used in the study. The respondents
were given unlimited time to fill in the questionnaires.
The analysis excluded three questionnaires in which the first trimester of pregnancy was declared.
Furthermore, the questionnaires which were not filled in completely or were filled in incorrectly
were rejected (contrary to the instructions). 400 questionnaires were distributed to women, 346 of
which were fully and properly completed. 21 questionnaires were incompletely or incorrectly filled in,
and 29 questionnaires were not returned. The project was approved by a local Bioethics Committee.
Int. J. Environ. Res. Public Health 2018, 15, 2745 3 of 12

The age of the respondents was 30.4 ± 3.6 years. Over 90% of study participants were college
graduates (91.9%), 8.1% graduated from high school, 81.5% were married, 17.3% were single, while 1.2%
were divorced. Furthermore, 88.2% were childless, 10.1% had 1 child and 1.7% had 2 or more children.
The tool used for assessment of PA was the Pregnancy Physical Activity Questionnaire-Polish
version (PPAQ-PL) [32–34]. The original version of PPAQ was designed by Chasan-Taber et al. [35].
The questionnaire is used by pregnant women to self-assess their PA in the current trimester.
In PPAQ-PL, the respondents were asked to report the time spent on participation in 32 types of
activities grouped under the following categories: household/caregiving (12 activities), occupational
(5 activities), sports/exercise (9 activities = 7 questions + two open questions, allowing the respondent
to add any activities not previously listed), transportation (3 activities), and inactivity (3 activities).
The questionnaire measures energy expenditure related to total activity and total activity of light intensity
and above expressed in Metabolic Equivalent of Task (MET) units (MET-h·week−1 ). Based on the energy
expenditure, each of these activities was additionally classified according to intensity: (a) sedentary
activity [<1.5 METs], (b) light intensity activity [1.5–<3.0 METs], (c) moderate intensity activity [3.0–6.0
METs], (d) vigorous-intensity activity [>6.0 METs]. The MET values were assigned according to the
values presented in the questionnaire instruction and the Compendium of Physical Activities [36].
The methodological basis for the assessment of the quality of life (QoL) was provided by the
abridged World Health Organization Quality of Life Questionnaire (WHOQoL-Bref), a Polish version
provided by Wołowicka and Jaracz [37]. The WHOQoL-Bref questionnaire assesses self-reported QoL
and general health of respondents. The WHOQoL-Bref questionnaire consists of 26 questions. The first
two questions were analyzed separately. They concerned self-assessed overall quality of life and general
health of the respondents. The remaining 24 questions assessed four domains of the QoL (physical
health domain: 7 questions, psychological domain: 6 questions, social relationships domain: 3 questions,
and environmental domain: 8 questions). The respondents were asked to mark their answers using
a five-level rating scale (from 1 to 5 points, in a positive direction: the higher the number of points,
the better quality of life). The QoL in the domains was expressed as mean values, calculated according
to the key and guidelines provided by the authors [37].
STATISTICA 12.5 software was used for statistical analysis. The significance of the analyzed
variables in women in the second and third trimesters of pregnancy was evaluated by means of the
Mann-Whitney U-test. Correlations between the variables were analyzed using Spearman’s rank
correlation test, with correlation coefficients calculated for each pair of variables. The level of statistical
significance was set at p ≤ 0.05.

3. Results
The results obtained from the PPAQ-PL and WHOQoL-Bref questionnaires for the women in the
second and third trimesters of pregnancy and intergroup differences (between the second and third
trimesters) are presented in Tables 1 and 2.
No statistically significant differences in the declared values of total energy expenditure (total
activity and total activity of light intensity and above) were found among the women surveyed (Table 1).
However, it was shown that the PA intensity differed significantly (p ≤ 0.05) depending on the trimester
of pregnancy. This concerns in particular sedentary activity (group of women in the second trimester:
30.4 ± 21.6 MET-h/week, group of women in the third trimester: 35.5 ± 23.1 MET-h/week) and
moderate activity (42.7 ± 45.2 and 39.4 ± 52.8 MET-h/week, respectively).
Analysis of the type of activities showed that the MET-h/week values did not differ between
the groups studied for household/caregiving, occupational activity, transportation and sports/exercise.
However, it was noticeable that higher energy expenditure (p ≤ 0.01) in women in the third trimester
of pregnancy was observed for the activities related to inactivity (51.4 ± 28.87 MET-h/week) compared
to those in the second trimester (42.7 ± 24.9 MET-h/week).
Int. J. Environ. Res. Public Health 2018, 15, 2745 4 of 12

Table 1. Means (M), standard deviations (SD), medians, and 25th and 75th percentiles for the
Pregnancy Physical Activity Questionnaire (PPAQ-PL) and intergroup comparisons (the second and
third trimesters) using the Mann–Whitney U-test.

PPAQ-PL (MET-h/week)
Factors Trimester
M ± SD 25th Median 75th p
Total Activity Scores:
2nd 183.3 ± 75.2 129.1 166.8 220.7
Total activity 0.721
3rd 192.1 ± 99.3 130.4 168.8 227.2
Total activity of light 2nd 152.9 ± 75.9 99.7 143.3 184.2
0.838
intensity and above
3rd 156.6 ± 95.5 99.2 136.9 188.7
by Intensity:
2nd 30.4 ± 21.6 15.4 29.4 43.4
Sedentary (<1.5 METs) 0.025 *
3rd 35.5 ± 23.1 17.9 29.4 46.2
2nd 110.4 ± 547.4 73.3 104.7 140.7
Light (1.5–<3.0 METs) 0.355
3rd 117.8 ± 55.3 73.5 109.8 151.6
Moderate (3.0–6.0 2nd 42.7 ± 45.2 17.9 30.9 50.2
0.022 *
METs)
3rd 39.4 ± 52.8 13.7 23.7 46.9
2nd 1.78 ± 4.2 0.0 0.0 0.8
Vigorous (>6.0 METs) 0.937
3rd 1.6 ± 4.3 0.0 0.0 0.8
by Type:
2nd 56.4 ± 39.8 33.6 43.5 67.6
Household/Caregiving 0.316
3rd 59.1 ± 40.1 33.9 50.1 70.4
2nd 37.8 ± 60.9 0.00 0.00 74.9
Occupational activity 0.337
3rd 33.2 ± 61.4 0.0 0.0 67.2
2nd 12.8 ± 11.8 7.2 12.8 21.2
Sports/Exercise 0.212
3rd 14.5 ± 12.7 5.0 11.0 19.7
2nd 30.9 ± 31.1 10.7 21.4 36.8
Transportation 0.505
3rd 33.84 ± 34.5 10.7 22.6 42.0
2nd 42.7 ± 24.9 24.2 38.2 57.4
Inactivity 0.005 **
3rd 51.4 ± 28.87 29.6 44.9 70.0
MET-Metabolic Equivalent of Task; * p ≤ 0.05; ** p ≤ 0.01.

The WHOQoL-Bref results indicated no differences in the self-rated quality of life of the women
surveyed (Table 2). Pregnant women in both the second and third trimesters rated their quality of life
in the psychological domain as the highest (16.48 ± 1.88 in the second trimester and 16.56 ± 1.64 in the
third trimester), whereas the lowest ratings were recorded for the environmental domain (15.89 ± 1.96
and 15.78 ± 1.91, respectively).
The next stage of the statistical analysis focused on investigating whether there is a correlation
between intensity and types of PA assessed using PPAQ-PL and domains of the QoL assessed using
WHOQoL-Bref in women in the second (Table 3) and third (Table 4) trimesters of pregnancy.
Int. J. Environ. Res. Public Health 2018, 15, 2745 5 of 12

Table 2. Medians, 25th and 75th percentiles, means (M) and standard deviations (SD) for the Quality of
Life-Bref Questionnaire (WHOQoL-Bref) and intergroup comparisons (2nd and 3rd trimesters) using
the Mann–Whitney U-test.

WHOQoL-Bref
Trimester M ± SD 25th Median 75th p
Factors
2nd 4.34 ± 0.61 4.00 4.00 5.00
Overall quality of life 0.300
3rd 4.41 ± 0.65 4.00 4.00 5.00
2nd 4.13 ± 0.67 4.00 5.00 5.00
General health 0.507
3rd 4.19 ± 0.65 4.00 4.00 5.00
WHO Domain
2nd 16.06 ± 2.16 15.00 16.00 18.00
Physical health 0.187
3rd 15.80 ± 01.99 14.00 16.00 17.00
2nd 16.48 ± 1.88 15.00 17.00 17.00
Psychological 0.552
3rd 16.56 ± 1.64 15.00 17.00 17.00
2nd 16.47 ± 2.21 16.00 16.00 19.00
Social relationships 0.274
3rd 16.14 ± 2.60 15.00 16.00 17.00
2nd 15.89 ± 1.96 15.00 16.00 17.00
Environmental 0.781
3rd 15.78 ± 1.91 15.00 16.00 17.00

Table 3. Spearman’s correlation coefficients between the Pregnancy Physical Activity questionnaire
(PPAQ-PL) and Quality of Life-Bref Questionnaire (WHOQoL-Bref) in women in the second trimester
of pregnancy.
Overall Quality of

General Health

WHOQoL-Bref Domain
WHOQoL-Bref
Physical Health

Environmental
Relationships
psychological
Life

Social

PPAQ-PL

Total Activity Scores:


Total activity −0.003 0.005 0.057 0.020 0.071 −0.061
Total activity of light
0.002 0.007 0.089 0.037 0.129 −0.037
intensity and above
by Intensity
Sedentary (<1.5 METs) −0.040 −0.028 −0.041 −0.072 −0.104 −0.073
Light (1.5–<3.0 METs) 0.029 −0.025 0.129 0.061 0.091 0.011
Moderate (3.0–6.0 METs) −0.035 0.043 0.029 −0.003 0.128 −0.073
Vigorous (>6.0 METs) −0.065 0.043 0.159 * 0.072 0.122 0.079
by Type
Household/Caregiving 0.0125 −0.059 −0.116 −0.143 −0.008 −0.035
Occupational activity 0.003 0.047 0.166 * 0.117 0.105 0.040
Sports/Exercise 0.035 0.081 0.187 * 0.103 0.153 0.103 *
Transportation 0.020 0.053 0.111 0.155 0.166 * 0.054
Inactivity 0.022 −0.017 −0.151 * −0.075 −0.097 −0.004
MET-Metabolic Equivalent of Task; * p ≤ 0.05.
Int. J. Environ. Res. Public Health 2018, 15, 2745 6 of 12

Table 4. Spearman’s correlation coefficients between the Pregnancy Physical Activity questionnaire
(PPAQ-PL) and Quality of Life-Bref Questionnaire (WHOQoL-Bref) in women in the third trimester
of pregnancy.

Overall Quality of

General Health
WHOQoL-Bref Domain
WHOQoL-Bref

Physical Health

Environmental
Relationships
Psychological
Life

Social
PPAQ-PL

Total activity −0.068 0.052 0.048 0.003 0.036 −0.094


Total activity of light
−0.049 0.049 0.085 −0.029 −0.009 −0.073
intensity and above
Sedentary (<1.5 METs) −0.090 −0.018 −0.125 0.020 0.0463 −0.068
Light (1.5–<3.0 METs) −0.053 −0.013 0.065 −0.068 −0.019 −0.133
Moderate (3.0–6.0 METs) 0.010 0.140 0.117 0.054 0.040 0.099
Vigorous (>6.0 METs) 0.029 0.041 0.073 0.161 * 0.188 * −0.072
Household/Caregiving −0.112 0.056 −0.023 0.023 −0.037 −0.059
Occupational activity 0.050 0.038 0.174 * −0.024 −0.013 0.034
Sports/Exercise 0.149 * 0.170 * 0.101 0.087 0.067 0.131
Transportation −0.064 −0.0083 0.068 −0.060 0.033 −0.124
Inactivity −0.077 −0.034 −0.128 −0.028 0.028 −0.096
MET-Metabolic Equivalent of Task; * p ≤ 0.05.

There was a significant correlation in the group of women in the second trimester of pregnancy
for physical health domain with intensity and the type of activities (Table 3). The women who rated
their quality of life higher in this domain declared higher energy expenditures associated with vigorous
activity (R = 0.159, p ≤ 0.05), as well as with occupational activity (R = 0.166; p ≤ 0.05) and sport/exercise
activity (R = 0.187; p ≤ 0.05).
Furthermore, a negative correlation was found between physical health domain and inactivity
(R = −0.151, p ≤ 0.05). This means that higher assessment of quality of life in this domain coincided
with lower energy expenditure related to inactivity. Individual positive correlations were also
documented between social relationship domain and transportation activity (R = 0.166, p ≤ 0.05) and
between environmental domain and sport/exercise activity (R = 0.103, p ≤ 0.05).
In women in the third trimester, higher energy expenditures related to sport/exercise activity
coincided with higher assessments of the overall quality of life (R = 0.149, p ≤ 0.05) and general health
(R = 0.170, p ≤ 0.05). In the case of the psychological domain (R = 0.161, p ≤ 0.05) and social relationship
domain (R = 0.188; p ≤ 0.05) of QoL, positive correlations occurred with energy expenditure related to
vigorous activity. In contrast, high assessment of the physical health domain coincided with higher energy
expenditure related to occupational activity (R = 0.174; p ≤ 0.05).

4. Discussion
The aim of this study was to investigate relationships between PA and QoL in women in the
second and third trimesters of pregnancy. The respondents’ declarations from the PPAQ-PL and
WHOQoL-Bref questionnaires were analyzed. Although studies have used these questionnaires in
recent years [16,18], this is, to our knowledge, the first such study in Poland. Such research is also
important because previous findings concerning PA in women in various stages of pregnancy have
been ambiguous. Some authors have found increases in PA, for example, Huberty et al. [10] in the first
and second trimesters, and Ko, Chen, Lin [38] from the second trimester, while others have documented
a decline in overall PA [38] in the first trimester, Evenson and Wen [39] in the third trimester,
and a decreasing percentage of physically active women in consecutive trimesters of pregnancy [2].
Int. J. Environ. Res. Public Health 2018, 15, 2745 7 of 12

Borodulin et al. [8] argued that the overall physical activity level slightly decreased between 17–22
and 27–30 weeks of gestation, particularly in duration and volume of care, outdoor household,
and recreational activity. Santos et al. [40] emphasized that a decline in PA from the first to the second
trimester concerned total, light and moderate intensities, while Richardsen et al. [41], documented a
decline in moderate and vigorous PA in the period between early pregnancy and mid-pregnancy.
Similar to findings published by Mourady et al. [16], our findings showed that the respondents in
different trimesters of pregnancy did not differ in terms of total PA, and total activity of light intensity
and above. However, they differed in the intensity of activities, especially in energy expenditure during
moderate activity (in favor of those in the second trimester). The women in the third trimester of
pregnancy reported significantly more energy expenditure on sedentary activity and inactivity, which is
not an isolated phenomenon in the world [10]. According to Santos et al. [40], energy expenditure
for particular types of PA (e.g., occupational activity, household activity, sports activity) changes
significantly in individual trimesters of pregnancy. Pregnant women spent most of their weekly
time on domestic, occupational and leisure time activities, except for sports activities. Similarly,
the majority of the respondents’ energy expenditure in the respondents surveyed in our study was
spent on household/caregiving activities. This suggests that despite many campaigns to raise awareness
of Polish women, such as: Pregnancy: Conscious Maternity, Find Out Whether You Are a Conscious
Parent, or Different State, Different Treatment (Cia˛ża-Świadome Macierzyństwo, Sprawdź czy jesteś
świadomym rodzicem, Odmienny stan, odmienne traktowanie), the role of the benefits of PA during
pregnancy remains underestimated. In the public’s opinion, healthy nutrition is more often perceived
as more important for the health of mothers and children than involvement in physical activity [42].
Therefore, the low levels of energy expenditure related to sport/exercise activity found in the present
study in both groups of women surveyed seem unsurprising. Perhaps, as argued by Clarke and
Gross [11] and Guelfi et al. [43], women perceive relaxation as a safer behavior, which is more
beneficial for ensuring full-term pregnancy rather than regular exercise and maintaining an active
lifestyle. The reasons also include misconceptions about physical exercise [44], the inconveniences
of late pregnancy, fatigue, poor moods, or being absorbed in numerous occupational duties [45,46].
There are also other determinants that represent barriers to physical exercise. For example, low physical
activity during pregnancy occurs more often in mature and married women, as well as those financially
less well-off and the less educated [47]. It seems, however, that regardless of the adversities, the role of
physicians is also critical as they have the greatest effect on the beliefs of pregnant women, including
their ideas on exercise during pregnancy [48]. Unfortunately, as Santos et al. [40] argued, medical
staff often fail to recommend PA during pregnancy. Furthermore, according to Krans et al. [48], a low
percentage of physicians help their patients to prepare physical exercise programs. Despite their
knowledge, physicians do not always explain the need for physical exercise, both during pregnancy
and in later decades of life [49]. They do not inform patients that it is necessary to consult both
physicians and coaches before starting physical exercise in order to exclude medical contraindications
and choose the right type of exercises and the load.
Knowledge about the quality of life plays a significant role both in diagnosis and patient care [50].
Despite being ambiguous, studies have widely documented the correlations between physical activity
and quality of life. According to the literature review published by Poudevigne et al. [47], there is
scientific evidence that inactivity during pregnancy is associated with poorer mood, whereas increasing
participation in sports or physical activity from the period of pregnancy to that after birth leads
to better overall well-being [51]. Mourady et al. [16] demonstrated that total and light intensity
of PA are positively significantly correlated with the psychological domain of quality of life and
social relationships; while sedentary PA is significantly correlated only with social relationships.
Arizabaleta et al. [19] documented improvements in HRQoL in the physical component summary,
physical function domain, the bodily pain domain and general health domain following a three-month
program of aerobic exercise. However, there are also publications that showed no improvements in
self-rated QoL caused by regular exercise such as water exercise [22].
Int. J. Environ. Res. Public Health 2018, 15, 2745 8 of 12

Analysis of QoL of the women surveyed showed that there were no significant differences in
self-rated domains of WHOOoL-Bref between pregnant women in the second and third trimesters of
pregnancy. Similarly, Mourady et al. [16], who analyzed all the trimesters, also found no differences
except in the environmental domain. In this case, the quality of life was significantly higher in the
women in the third trimester compared to those in the first trimester.
In our study, we found higher QoL scores in the environment domain in women in the second
trimester who declared higher sport/exercise activity. It should also be noted that sport/exercise activity
of the respondents studied was also positively correlated with the physical domain in women in the
second trimester and with overall quality of life and general health in women in the third.
Our findings are consistent with those presented by Mourady et al. [16], who showed that
sports/exercise was significantly correlated with the majority of quality of life domains such as general
quality of life, physical and psychological health, social relationships and the environmental domain.
This is unsurprising since apart from its well-documented health benefits, sport [5–7] offers joy,
relaxation and enhances psychological well-being [52]. Obviously, there have also been studies in the
literature that have failed to support such findings. For example, Gustafsson et al. [53] indicated that
a 12-week exercise program including aerobic and strength training during pregnancy is unlikely to
influence the psychological and self-perceived well-being of healthy pregnant women. Kolu et al. [17]
showed a decline in the overall HRQoL index during pregnancy, although they emphasized that this
decrease was lower in women who were physically active during pregnancy. Nascimento et al. [23]
argued that physical exercise does not significantly affect the perception of the quality of life of
pregnant women because, regardless of their participation in the exercise program, the quality of life
of women (in the physical and social domains) during pregnancy fell significantly.
An interesting finding of our study is that pregnant women who assessed QoL as higher in
the field of physical health (both in the second and third trimester) were characterized by a higher
energy expenditure during occupational activity. The explanation for this finding seems to be obvious;
women with better self-rated physical well-being tend to work more. We are aware, however, that the
explanation for this phenomenon may be more complex. The study published by Blum et al. [51]
showed that women with older infants or no other children reported higher household/caregiving and
lower occupation pre-pregnancy to postpartum activity. Physical activity in pregnancy may depend
on the socio-economic status and support of a partner, friends or family [54,55]. These factors may, to a
large extent, determine the quality of life [56]. Unfortunately, due to the lack of the above-mentioned
information in our study, the impact of these factors was impossible to determine. Some limitations
of this study should be mentioned and taken into consideration. First of all, a limited number of
participants and the place where the women were selected (fitness clubs and antenatal classes) lead
to a lack of representativeness of the total population with possible effects on the results. This in
turn makes it impossible to draw general conclusions for the whole population of pregnant women.
Furthermore, the lack of detailed information on socio-economic and psychological factors and data
about pathologies makes the interpretation of the results difficult.

5. Conclusions
In conclusion, our study (the first study in Poland that has used reliable, internationally recognized
questionnaires (PPAQ-PL and WHOQoL-Bref) makes an important contribution to the knowledge
concerning the correlations between PA and QoL in women during different periods of pregnancy.
The study showed that total activity and total activity of light intensity and above did not differentiate
between women in the second and third trimesters of pregnancy. However, it indicated higher values
of moderate activity in women in the second trimester of pregnancy and higher values of sedentary
activity and inactivity in women in the third trimester. Our findings concerning the relationships
between physical activity and quality of life should be approached with caution, due to the low values
of correlation coefficients. The low MET values for sport/exercise recorded in both groups of women
can indicate the need for improving the prenatal care, especially in terms of promotion of physical
Int. J. Environ. Res. Public Health 2018, 15, 2745 9 of 12

activity programs for pregnant women and encouraging women to participate in these programs.
In terms of intervention activities, special attention should be given to barriers existing at the level
of the provider, the patient, and practice [57]. Researchers [58] have specified concrete actions that
should be taken by prenatal care providers in order to promote prenatal PA, suggesting, among other
things, providing information by healthcare providers about both guidelines and contraindications
for the involvement in physical activity during pregnancy. Most guidelines from around the world,
gathered by Evenson et al. [59], promoted moderate-intensity physical activity during pregnancy and
defined its frequency and duration/time. The latest physical activity guidelines published by the
U.S. Department of Health and Human Services USDHHS in 2018 [60], indicate 150 min (2 h and
30 min) of moderate-intensity aerobic activity a week during pregnancy and the postpartum period.
Recommending aerobic activity should be spread throughout the week.
Undoubtedly, our study does not exhaust the problems discussed but its findings emphasize
the need for raising awareness of the importance of physical activity during pregnancy. We believe
that further research on a larger sample with the consideration of socio-economic factors and a
comprehensive inventory of pregnancy-related symptoms, along with a mechanism for assessing their
effect on function [61] is needed to provide deeper understanding and identify correlations between
PA and determinants of QoL in pregnant women.

Author Contributions: J.K. prepared the study design, searched the literature, wrote the background and
discussion of the study, gathered the necessary data, prepared it for analysis, described the results of the study
and prepared the manuscript. D.S. searched the literature, refined the data, performed the statistical analysis,
and described its results. E.B. searched the literature, corrected and improved the manuscript of the study for the
final version. All authors have read and approved the final manuscript.
Funding: This research received no external funding.
Acknowledgments: The authors would like to thank all the women who participated in the study and Katarzyna
Sempolska, who contributed to data acquisition.
Conflicts of Interest: The authors declare no conflict of interest.

References
1. Evenson, K.R.; Savitz, A.; Huston, S.L. Leisure-time physical activity among pregnant women in the US.
Paediatr. Perinat. Epidemiol. 2004, 18, 400–407. [CrossRef] [PubMed]
2. Domingues, M.R.; Barros, A.J.D. Leisure-time physical activity during pregnancy in the 2004 Pelotas Birth
Cohort Study. Rev. Saude Publica 2007, 41, 173–180. [CrossRef] [PubMed]
3. Haakstad, L.A.H.; Voldner, N.; Henriksen, T.; Bø, K. Why do pregnant women stop exercising in the third
trimester? Acta Obstet. Gynecol. Scand. 2009, 88, 1267–1275. [CrossRef] [PubMed]
4. Santo, E.C.; Forbes, P.W.; Oken, E.; Belfort, M.B. Determinants of physical activity frequency and provider
advice during pregnancy. BMC Pregnancy Childbirth 2017, 17, 286. [CrossRef] [PubMed]
5. Melzer, K.; Schutz, Y.; Soehnchen, N.; Othenin-Girard, V.; Martinez de Tejada, B.; Irion, O.; Boulvain, M.;
Kayser, B. Effects of recommended levels of physical activity on pregnancy outcomes. Am. J. Obstet. Gynecol.
2010, 202, 266.e1-6. [CrossRef] [PubMed]
6. Hinman, S.K.; Smith, K.B.; Quillen, D.M.; Smith, M.S. Exercise in Pregnancy: A Clinical Review. Sports Health
2015, 7, 527–531. [CrossRef] [PubMed]
7. Brown, W. The benefits of physical activity during pregnancy. J. Sci. Med. Sport 2002, 5, 37–45. [CrossRef]
8. Borodulin, K.; Evenson, K.R.; Wen, F.; Herring, A.H.; Benson, A. Physical activity patterns during pregnancy.
Med. Sci. Sports Exerc. 2008, 40, 1901–1908. [CrossRef]
9. Clarke, P.E.; Rousham, E.K.; Gross, H.; Halligan, A.W.F.; Bosio, P. Activity patterns and time allocation
during pregnancy: A longitudinal study of British women. Ann. Hum. Biol. 2005, 32, 247–258. [CrossRef]
10. Huberty, J.L.; Buman, M.P.; Leiferman, J.A.; Bushar, J.; Adams, M.A. Trajectories of objectively-measured
physical activity and sedentary time over the course of pregnancy in women self-identified as inactive.
Prev. Med. Rep. 2016, 3, 353–360. [CrossRef]
11. Clarke, P.E.; Gross, H. Women’s behaviour, beliefs and information sources about physical exercise in
pregnancy. Midwifery 2004, 20, 133–141. [CrossRef] [PubMed]
Int. J. Environ. Res. Public Health 2018, 15, 2745 10 of 12

12. Fell, D.B.; Joseph, K.S.; Armson, B.A.; Dodds, L. The impact of pregnancy on physical activity level. Matern.
Child Health J. 2009, 13, 597–603. [CrossRef] [PubMed]
13. Gjestland, K.; Bø, K.; Owe, K.M.; Eberhard-Gran, M. Do pregnant women follow exercise guidelines?
Prevalence data among 3482 women, and prediction of low-back pain, pelvic girdle pain and depression.
Br. J. Sports Med. 2013, 47, 515–520. [CrossRef] [PubMed]
14. Bai, G.; Raat, H.; Jaddoe, V.W.V.; Mautner, E.; Korfage, I.J. Trajectories and predictors of women’s
health-related quality of life during pregnancy: A large longitudinal cohort study. PLoS ONE 2018, 13,
e0194999. [CrossRef] [PubMed]
15. Emmanuel, E.N.; Sun, J. Health related quality of life across the perinatal period among Australian Women.
J. Clin. Nurs. 2014, 23, 1611–1619. [CrossRef] [PubMed]
16. Mourady, D.; Richa, S.; Karam, R.; Papazian, T.; Moussa, F.H.; El Osta, N.; Kesrouani, A.; Azouri, J.;
Jabbour, H.; Hajj, A.; et al. Associations between quality of life, physical activity, worry, depression and
insomnia: A cross-sectional designed study in healthy pregnant women. PLoS ONE 2017, 12, e0178181.
[CrossRef] [PubMed]
17. Kolu, P.; Raitanen, J.; Luoto, R. Physical activity and health-related quality of life during pregnancy:
A secondary analysis of a cluster-randomised trial. Matern. Child Health J. 2014, 18, 2098–2105. [CrossRef]
[PubMed]
18. Bahadoran, P.; Mohamadirizi, S. Relationship between physical activity and quality of life in pregnant
women. Iran. J. Nurs. Midwifery Res. 2015, 20, 282–286. [PubMed]
19. Arizabaleta, A.V.M.; Buitrago, L.O.; de Plata, A.C.A.; Escudero, M.M.; Ramírez-Vélez, R. Aerobic exercise
during pregnancy improves health-related quality of life: A randomised trial. J. Physiother. 2010, 56, 253–258.
[CrossRef]
20. Tendais, I.; Figueiredo, B.; Mota, J.; Conde, A. Physical activity, health-related quality of life and depression
during pregnancy. Cad. Saúde Pública 2011, 27, 219–228. [CrossRef] [PubMed]
21. Mogos, M.F.; August, E.M.; Salinas-Miranda, A.A.; Sultan, D.H.; Salihu, H.M. A systematic review of quality
of life measures in pregnant and postpartum mothers. Appl. Res. Qual. Life 2013, 8, 219–250. [CrossRef]
[PubMed]
22. Vallim, A.L.; Osis, M.J.; Cecatti, J.G.; Baciuk, É.P.; Silveira, C.; Cavalcante, S.R. Water exercises and quality of
life during pregnancy. Reprod. Health 2011, 8, 14. [CrossRef] [PubMed]
23. Nascimento, S.L.; Surita, F.G.; Parpinelli, M.; Siani, S.; Pinto e Silva, J.L. The effect of an antenatal physical
exercise programme on maternal/perinatal outcomes and quality of life in overweight and obese pregnant
women: A randomised clinical trial. BJOG 2011, 118, 1455–1463. [CrossRef] [PubMed]
24. Vachkova, E.; Jezek, S.; Mares, J.; Moravcova, M. The evaluation of the psychometric properties of a specific
quality of life questionnaire for physiological pregnancy. Health Qual. Life Outcomes 2013, 11, 214. [CrossRef]
[PubMed]
25. Sattler, M.C.; Jaunig, J.; Watson, E.D.; van Poppel, M.N.M.; Mokkink, L.B.; Terwee, C.B.; Dietz, P. Physical
Activity Questionnaires for Pregnancy: A Systematic Review of Measurement Properties. Sport Med. 2018,
48, 2317–2346. [CrossRef] [PubMed]
26. Matsuzaki, M.; Haruna, M.; Nakayama, K.; Shiraishi, M.; Ota, E.; Murayama, R.; Murashima, S.; Yeo, S.
Adapting the Pregnancy Physical Activity Questionnaire for Japanese Pregnant Women. J. Obstet. Gynecol.
Neonatal Nurs. 2014, 43, 107–116. [CrossRef] [PubMed]
27. Matsuzaki, M.; Haruna, M.; Ota, E.; Yeo, S.A.; Murayama, R.; Murashima, S. Translation and cross-cultural
adaptation of the pregnancy physical activity questionnaire (PPAQ) to Japanese. Biosci. Trends 2010, 4,
170–177. [PubMed]
28. Xiang, M.; Konishi, M.; Hu, H.; Takahashi, M.; Fan, W.; Nishimaki, M.; Ando, K.; Kim, H.K.; Tabata, H.;
Arao, T.; et al. Reliability and Validity of a Chinese-Translated Version of a Pregnancy Physical Activity
Questionnaire. Matern. Child Health J. 2016, 20, 1940–1947. [CrossRef] [PubMed]
29. Cirak, Y.; Yilmaz, G.D.; Demir, Y.P.; Dalkilinc, M.; Yaman, S. Pregnancy physical activity questionnaire
(PPAQ): Reliability and validity of Turkish version. J. Phys. Ther. Sci. 2015, 27, 3703–3709. [CrossRef]
[PubMed]
30. Ota, E.; Haruna, M.; Yanai, H.; Suzuki, M.; Anh, D.D.; Matsuzaki, M.; Tho le, H.; Ariyoshi, K.; Yeo, S.A.;
Murashima, S. Reliability and validity of the Vietnamese version of the pregnancy physical activity
questionnaire (PPAQ). Southeast Asian J. Trop. Med. Public Health 2008, 39, 562–570. [PubMed]
Int. J. Environ. Res. Public Health 2018, 15, 2745 11 of 12

31. Silva, F.T.; Araujo Júnior, E.; Santana, E.F.M.; Lima, J.W.; Cecchino, G.N.; Silva Costa, F.D. Translation
and cross-cultural adaptation of the Pregnancy Physical Activity Questionnaire (PPAQ) to the Brazilian
population. Ceska Gynekol. 2015, 80, 290–298. [PubMed]
32. Krzepota, J.; Sadowska, D.; Sempolska, K.; Pelczar, M. Measuring physical activity during
pregnancy—Cultural adaptation of the pregnancy physical activity questionnaire (PPAQ) and assessment of
its reliability in Polish conditions. Ann. Agric. Environ. Med. 2017, 24, 640–643. [CrossRef] [PubMed]
33. Krzepota, J.; Sadowska, D. Pregnant and active—Suitability of the pregnancy physical activity questionnaire
for measuring the physical activity of pregnant women in Poland. Fam. Med. Prim. Care Rev. 2017, 19, 29–33.
[CrossRef]
34. Krzepota, J.; Sadowska, D. Kwestionariusz Aktywności Fizycznej Kobiet w Cia˛ży—Wersja polska (PPAQ-PL).
Med. Ogólna I Nauk. O Zdrowiu 2017, 23, 100–106. [CrossRef]
35. Chasan-Taber, L.; Schmidt, M.D.; Roberts, D.E.; Hosmer, D.; Markenson, G.; Freedson, P.S. Development
and validation of a Pregnancy Physical Activity Questionnaire. Med. Sci. Sports Exerc. 2004, 36, 1750–1760.
[CrossRef]
36. Ainsworth, B.E.; Haskell, W.L.; Whitt, M.C.; Irwin, M.L.; Swartz, A.M.; Strath, S.J.; O’Brien, W.L.;
Bassett, D.R., Jr.; Schmitz, K.H.; Emplaincourt, P.O.; et al. Compendium of physical activities: An update of
activity codes and MET intensities. Med. Sci. Sports Exerc. 2000, 32, S498–S504. [CrossRef]
37. Wołowicka, L.; Jaracz, K. Polska wersja WHOQOL-WHOQOL 100 i WHOQOL BREF. In Jakość Życia w
Naukach Medycznych; Wydawnictwo Akademii Medycznej: Poznań, Poland, 2001; pp. 259–281.
38. Ko, Y.L.; Chen, C.P.; Lin, P.C. Physical activities during pregnancy and type of delivery in nulliparae. Eur. J.
Sport Sci. 2016, 16, 347–380. [CrossRef]
39. Evenson, K.R.; Wen, F. Prevalence and correlates of objectively measured physical activity and sedentary
behavior among US pregnant women. Prev. Med. 2011, 53, 39–43. [CrossRef]
40. Santos, P.C.; Abreu, S.; Moreira, C.; Santos, R.; Ferreira, M.; Alves, O.; Moreira, P.; Mota, J. Physical activity
patterns during pregnancy in a sample of Portuguese women: A longitudinal prospective study. Iran. Red
Crescent Med. J. 2016, 18, e22455. [CrossRef]
41. Richardsen, K.R.; Mdala, I.; Berntsen, S.; Ommundsen, Y.; Martinsen, E.W.; Sletner, L.; Jenum, A.K.
Objectively recorded physical activity in pregnancy and postpartum in a multi-ethnic cohort: Association
with access to recreational areas in the neighbourhood. Int. J. Behav. Nutr. Phys. Act. 2016, 13, 78. [CrossRef]
42. Weir, Z.; Bush, J.; Robson, S.C.; McParlin, C.; Rankin, J.; Bell, R. Physical activity in pregnancy: A qualitative
study of the beliefs of overweight and obese pregnant women. BMC Pregnancy Childbirth 2010, 10, 18.
[CrossRef] [PubMed]
43. Guelfi, K.J.; Wang, C.; Dimmock, J.A.; Jackson, B.; Newnham, J.P.; Yang, H. A comparison of beliefs about
exercise during pregnancy between Chinese and Australian pregnant women. BMC Pregnancy Childbirth
2015, 15, 345. [CrossRef] [PubMed]
44. Evenson, K.R.; Bradley, C.B. Beliefs about exercise and physical activity among pregnant women. Patient Educ.
Couns. 2010, 79, 124–129. [CrossRef] [PubMed]
45. Hegaard, H.K.; Kjaergaard, H.; Damm, P.P.; Petersson, K.; Dykes, A.K. Experiences of physical activity
during pregnancy in Danish nulliparous women with a physically active life before pregnancy. A qualitative
study. BMC Pregnancy Childbirth 2010, 10, 33. [CrossRef] [PubMed]
46. Duncombe, D.; Wertheim, E.H.; Skouteris, H.; Paxton, S.J.; Kelly, L. Factors related to exercise over the course
of pregnancy including women’s beliefs about the safety of exercise during pregnancy. Midwifery 2009, 25,
430–438. [CrossRef] [PubMed]
47. Poudevigne, S.; Connor, P.J.O. A Review of Physical Activity Patterns in Pregnant Women and Their
Relationship to Psychological Health. Sport Med. 2006, 36, 19–38. [CrossRef]
48. Krans, E.E.; Gearhart, J.G.; Dubbert, P.M.; Klar, P.M.; Miller, A.L.; Replogle, W.H. Pregnant women’s beliefs
and influences regarding exercise during pregnancy. J. Miss. State Med. Assoc. 2005, 46, 67–73. [PubMed]
49. Biernat, E.; Buchholtz, S. Poor health and contraindications—The most common barriers to physical activity
in poles aged 50+. Health Probl. Civiliz. 2017, 11, 135–141. [CrossRef]
50. Bossola, M.; Murri, R.; Onder, G.; Turriziani, A.; Fantoni, M.; Padua, L. Physicians’ knowledge of
health-related quality of life and perception of its importance in daily clinical practice. Health Qual.
Life Outcomes 2010, 8, 43. [CrossRef] [PubMed]
Int. J. Environ. Res. Public Health 2018, 15, 2745 12 of 12

51. Blum, J.W.; Beaudoin, C.M.; Caton-Lemos, L. Physical activity patterns and maternal well-being in
postpartum women. Matern. Child Health J. 2004, 8, 163–169. [CrossRef] [PubMed]
52. Costa, D.D.; Rippen, N.; Dritsa, M.; Ring, A. Self-reported leisure-time physical activity during pregnancy
and relationship to psychological well-being. J. Psychosom. Obstet. Gynecol. 2003, 24, 111–119. [CrossRef]
53. Gustafsson, M.K.; Stafne, S.N.; Romundstad, P.R.; Mørkved, S.; Salvesen, K.Å.; Helvik, A. The effects of an
exercise programme during pregnancy on health-related quality of life in pregnant women: A Norwegian
randomised controlled trial. BJOG 2016, 123, 1152–1160. [CrossRef] [PubMed]
54. Harrison, A.L.; Taylor, N.F.; Shields, N.; Frawley, H.C. Attitudes, barriers and enablers to physical activity in
pregnant women: A systematic review. J. Physiother. 2018, 64, 24–32. [CrossRef] [PubMed]
55. Muzigaba, M.; Kolbe-Alexander, T.L.; Wong, F. The perceived role and influencers of physical activity among
pregnant women from low socioeconomic status communities in South Africa. J. Phys. Act. Health 2014, 11,
1276–1283. [CrossRef] [PubMed]
56. Ramírez-Vélez, R. Pregnancy and health-related quality of life: A cross sectional study. Colomb. Med. 2011,
42, 476–481.
57. Jansink, R.; Braspenning, J.; van der Weijden, T.; Elwyn, G.; Grol, R. Primary care nurses struggle with
lifestyle counseling in diabetes care: A qualitative analysis. BMC Fam. Pract. 2010, 11, 41. [CrossRef]
58. Downs, D.S.; Chasan-Taber, L.; Evenson, K.R.; Leiferman, J.; Yeo, S. Physical activity and pregnancy: Past and
present evidence and future recommendations. Res. Q. Exerc. Sport 2012, 83, 485–502. [CrossRef] [PubMed]
59. Evenson, K.R.; Barakat, R.; Brown, W.J.; Dargent-Molina, P.; Haruna, M.; Mikkelsen, E.M.; Mottola, M.F.;
Owe, K.M.; Rousham, E.K.; Yeo, S. Guidelines for Physical Activity during Pregnancy: Comparisons From
Around the World. Am. J. Lifestyle Med. 2014, 8, 102–121. [CrossRef] [PubMed]
60. U.S. Department of Health and Human Services. Physical Activity Guidelines for Americans, 2nd ed.; U.S.
Department of Health and Human Services: Washington, DC, USA, 2018. Available online: https://health.
gov/paguidelines/second-edition/pdf/Physical_Activity_Guidelines_2nd_edition.pdf (accessed on 30
November 2018).
61. Foxcroft, K.F.; Callaway, L.K.; Byrne, N.M.; Webster, J. Development and validation of a pregnancy symptoms
inventory. BMC Pregnancy Childbirth 2013, 13, 3. [CrossRef] [PubMed]

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Journal of Midwifery & Women’s Health www.jmwh.org
Original Research

Effects of Maternal Mental Health on Engagement in Favorable


Health Practices During Pregnancy
Jeanne L. Alhusen, PhD, CRNP, RN, Lauren Ayres, BSN, RN, CCRN, Kelli DePriest, BSN, RN

Introduction: A woman’s health practices during pregnancy are associated with maternal and neonatal outcomes. Yet limited research has ex-
amined predictors of a woman’s engagement in favorable health practices, particularly in pregnant women at greatest risk for adverse outcomes.
We examined the role of mental health on engagement in favorable health practices during pregnancy in a sample of pregnant, low-income,
predominantly African American women.
Methods: A convenience sample of pregnant women was obtained from 3 obstetric clinics within a large Mid-Atlantic academic health system.
Pregnant women (N = 166) completed measures of depression, social support, and engagement in favorable health practices during their second
trimester. Six domains of health practices (ie, balance of rest and exercise, safety measures, nutrition, substance use, health care access, access
to pregnancy-related information) were assessed by the Health Practices in Pregnancy Questionnaire-II. Multiple linear regression was used to
examine predictors of engagement in favorable health practices.
Results: Fifty-nine percent of the study participants experienced depressive symptomatology during pregnancy. Multivariate linear regression
modeling demonstrated that increased depressive symptoms, decreased social support, young age, and prepregnancy overweight or obesity were
significant predictors of nonengagement in favorable health practices during pregnancy.
Discussion: Findings suggest that pregnant women with poor mental health (eg, depressive symptomatology, poor social support) and specific
sociodemographic characteristics (eg, young age, prepregnancy overweight or obesity) were less likely to engage in favorable health practices
during pregnancy. Health care providers are uniquely positioned to assess a woman’s mental health and related indicators to optimize pregnancy
and neonatal outcomes.
J Midwifery Womens Health 2016;61:210–216  c 2016 by the American College of Nurse-Midwives.

Keywords: African American, antenatal depression, health practices, obesity, pregnancy, social support

INTRODUCTION mental health and engagement in healthy practices has largely


Pregnancy represents a critical time period during which focused on specific health practices such as use of alcohol, to-
maternal health practices contribute significantly to maternal, bacco use, and illicit substances. Depression in pregnancy has
neonatal, and early childhood outcomes. Favorable health been associated with alcohol use, tobacco use, and substance
practices associated with positive outcomes include main- use.1,4–6 In a study of low-income, predominantly African
taining a health prepregnancy weight, gaining an appropriate American women, depressive symptoms during pregnancy
amount of weight during pregnancy, consuming a variety of were associated with an increased risk of cigarette smoking.7
foods with adequate intake of specific nutrients, engaging In addition, poor health practices such as smoking, substance
in regular physical activity, limiting alcohol consumption, use, or alcohol use may exacerbate depressive symptoms and
avoiding tobacco and illicit substance use, taking appropriate vice versa.8–10 While an important contribution, knowledge
vitamin and mineral supplementation, and using safe food of individual health practices limits our understanding of
handling practices.1 Despite the recognition that a woman’s the contribution of mental health to a more comprehensive
health practices during pregnancy are important for maternal picture of a woman’s ability to engage in favorable health
and fetal health, as well as neonatal outcomes, there is limited practices.
research examining predictors of favorable health practices A growing body of research suggests there is a relationship
during pregnancy. It is important to better understand factors between poor antenatal mental health and adverse maternal,
that influence a woman’s ability to engage in favorable health neonatal, and early childhood outcomes.11,12 There are several
practices during pregnancy, particularly among women at plausible mechanisms by which depression may contribute
highest risk for poor outcomes, in an effort to best support to adverse perinatal outcomes. First, evidence supports de-
them in achieving a healthy pregnancy. Thus, the purpose pression as a stressor leading to changes in the hypothalamic-
of the current study was to examine predictors of a woman’s pituitary-adrenal (HPA) axis with resultant inflammation
engagement in favorable health practices during pregnancy. and dysregulation of cortisol. These changes may lead to early
Perinatal depression affects an estimated 7% to 20% of contractions and preterm birth.12,13 Maternal obesity also is
women with rates as high as 35% to 40% in low-income associated with an increased risk of adverse maternal and fetal
and minority women.2,3 Limited research examining perinatal outcomes.14 Maternal obesity and depression are individually
associated with an increased risk of poor pregnancy out-
comes, and research suggests their combined presence has the
Address correspondence to: Jeanne Alhusen, PhD, CRNP, RN, 525 N. greatest impact on the risk of adverse neonatal outcomes.15
Wolfe Street, Suite 528, Baltimore, MD 21205. E-mail: Jalhuse1@jhu.edu

210 1526-9523/09/$36.00 doi:10.1111/jmwh.12407 


c 2016 by the American College of Nurse-Midwives
✦ Pregnancy represents a critical time period during which maternal health practices contribute significantly to maternal,
neonatal, and early childhood outcomes.
✦ It is important to better understand factors that influence a woman’s ability to engage in favorable health practices during
pregnancy, particularly among women at highest risk for poor outcomes in an effort to best support them in achieving
optimal pregnancy outcomes.
✦ Most pregnant women access health care during the perinatal period, making it an opportune time to assess facilitators
and barriers to favorable health practices.
✦ Findings from this study suggest that a woman’s mental health is strongly associated with her ability to engage in favorable
health practices during pregnancy.

A recent systematic review was conducted to summarize the description of the study, written informed consent was ob-
relation between psychological factors and gestational weight tained and participants were interviewed in a private area
gain. Synthesized results from 35 studies did not find an asso- within the clinic with only the researcher and the participant
ciation between gestational weight gain and depressive symp- present. The study instruments were read aloud to the women
toms. Findings were in contrast to evidence from studies of and took approximately 30 minutes to complete. All study par-
nonpregnant women, which supports an association between ticipants were compensated $15 for their time and expertise.
depression and weight,16,17 although many studies of this as-
sociation have been underpowered.16 Importantly, studies ex-
amining the link between depression and gestational weight Measures
gain are limited by small sample sizes and participants with Study measures included a measure of demographics created
mild depressive symptomatology.18 Finally, limited research by the study team, the Prenatal Psychosocial Profile (PPP),20
suggests depression is associated with an increase in tobacco the Edinburgh Postnatal Depression Scale (EPDS),21 and the
use and illicit substance use during pregnancy; thus, the rela- Health Practices in Pregnancy Questionnaire-II (HPQ-II).22
tion between depression and adverse neonatal outcomes may The PPP consists of 3 subscales that assess social support,
be mediated by harmful substance use.19 stress, and self-esteem. For the purpose of this study, the
Pregnancy represents a critical time period in that poor 11-item social support subscale was used to measure each
health practices are clearly associated with short-term and woman’s perceived social support. Using a Likert-type scale
long-term health consequences for both woman and child. of 1 (“very dissatisfied”) to 6 (“very satisfied”), each woman
There is a significant need for an enhanced understanding of was asked to rate her level of satisfaction with the support
predictors of health practices that extends beyond examining she received from her partner. Scores on the social support
substance use. Illuminating these relationships is important subscale range from 11 to 66, with higher scores indicative
not only to enhance our understanding of the factors that of a higher perception of social support. If the woman did
predict these behaviors but also to identify factors that not report contact with a partner, she completed the scale
might be amenable to interventions. Most pregnant women based on perceived support from a close family member.
access health care during the perinatal period, making it an Sample items include: “Helps me out when I’m in a pinch,”
opportune time to assess facilitators and barriers to optimal and “Takes me seriously when I have concerns.” Validity
health practices. and reliability of each subscale has been supported in several
studies that have included ethnically diverse rural and urban
METHODS women with reliability estimates of subscales ranging from
.78 to .98.20 Adequate reliability was demonstrated in the
Sample current study (Cronbach’s ␣ = .96).
A convenience sample of pregnant women was recruited from Depressive symptomatology was measured using the
3 obstetric clinics in Baltimore, Maryland. These clinics were EPDS, the well-validated and most widely utilized screening
affiliated with a major academic health system and served tool for depressive symptoms in the perinatal period.23
predominantly low-income, urban women. Eligibility re- The EPDS contains 10 items and focuses less on somatic
quirements included English-speaking pregnant women aged symptoms associated with depression making it particularly
16 years and older and in their second trimester of pregnancy valuable during the perinatal period.24 Women are asked to
with a singleton pregnancy. rate their responses in a Likert-type format and represent
Institutional review board approval was received from how they’ve felt over the past 7 days. Sample items include, “I
Johns Hopkins Medical Institution prior to study recruitment. have been able to laugh and see the funny side of things,” and
“I have felt sad or miserable.” Each item is scored 0 (eg, “not
at all,” “never”) to 3 (eg, “most of the time,” “quite a lot”) and
Procedure
the total scale score ranges from 0 to 30 with higher scores
The study was discussed with eligible participants during indicative of higher depressive symptomatology. The EPDS
their routine prenatal care appointments. After a complete has been used with racial and ethnic minority women, and
Journal of Midwifery & Women’s Health r www.jmwh.org 211
several studies have supported its use during pregnancy.23,25 Table 1. Participant Sociodemographic and Clinical
For this analysis, we used the most widely recommended Characteristics (N = 166)
cutoff score for depressive symptomatology during pregnancy Characteristic n ()
(ie, ⬎ 12). Consistent with the participating clinics’ protocols, Age, mean (range), y 23.3 (16-39)
any woman with a positive response to item #10 (“The thought
16-19 46 (28)
of harming myself has occurred to me”) on the EPDS or scor-
ing greater than 12 on the EPDS was referred to the clinic so- 20-24 58 (35)
cial worker and health care provider for further evaluation and 25-29 35 (21)
treatment. A sensitivity rate of 82% with a specificity of 95% 30-39 27 (16)
has been previously demonstrated with this cutoff point in a Race
similar population.26 The Cronbach’s ␣ for the current study
African American 155 (93)
was .91.
The HPQ-II contains 34 items that ask about health White non-Hispanic 9 (5)
practices in 6 domains including balance of rest and exercise, Other 2 (2)
safety measures, nutrition, substance use, health care access, Education
and access to pregnancy-related information.22 Responses
Less than high school 110 (67)
range from 1 (“never”) to 5 (“always” or “daily”) or a word or
phrase that indicates the woman’s level of engagement in a High school graduate/GED 45 (27)
specific activity (eg, 1—No alcoholic drinks while pregnant Some college/trade school 5 (3)
to 5—More than 3 alcoholic drinks at one sitting). Sample College/Trade school graduate 6 (3)
items include, “Since becoming pregnant, I have exercised Marital status
regularly”; “Since becoming pregnant, I have taken herbal
Single 90 (54)
remedies other than those recommended to me by my doctor
or midwife”; and “Since becoming pregnant, I have eaten Partnered/not married 56 (34)
5 servings of fruits or vegetables in a day.” The total scale Married 17 (10)
score ranges from 34 to 170, with a higher score indicative of Divorced 2 (1)
greater engagement in favorable health practices. Consistent
Widowed 1 (1)
with scoring recommendations, this scale was analyzed as a
continuous measure.22 Content validity was established by a Employment status
diverse sample of pregnant women and maternal-child health Unemployed 127 (77)
experts,22,27 and Cronbach’s ␣ for the current study was .90. Employed full-time 25 (15)
Employed part-time 14 (8)
Total household income
Analysis
Under $10,000 76 (46)
Data were analyzed using PASW Statistics 22, Release Version $10,001-$20,000 66 (40)
22.0.0 (SPSS: An IBM Company). Data analysis began with
$20,001-$30,000 12 (7)
descriptive and exploratory statistical analyses, and study
variables were examined to assess distributions, to identify $30,001-$40,000 8 (5)
any outliers, and to determine the need for transformation. ⬎ $40,000 4 (2)
There were no missing data. A series of generalized linear Gravidity
models were conducted and included variables that had P Multiparous 112 (68)
values less than .15 in bivariate analyses or were deemed
Primiparous 54 (32)
theoretically relevant.
Prepregnancy BMI classification, (kg/m2 )
Underweight (⬍ 18.5) 7 (5)
RESULTS Normal (18.5-24.9) 42 (26)
Over a period of 6 months, 174 eligible women were ap- Overweight (25.9-29.9) 60 (36)
proached to participate, and 166 (96%) completed the study Obese (30.0 and above) 55 (33)
instruments. The 8 women declining study participation
reported time concerns. As depicted in Table 1, the majority
of women identified as being African American (93%), single
(54%), and unemployed (77%). Approximately 28% of the
Predictors of Health Practices During Pregnancy
women were adolescents (defined in this study as 16 to 19
years of age) at the time of data collection. Two-thirds (66%) Table 2 presents the mean scores and standard deviations
of the women reported less than a high school diploma, (SDs) for all study measures. Scores are presented for
and nearly half of the women (46%) reported a total annual adolescents and all other age groups. The mean score on
income of less than $10,000. Nearly two-thirds of the women the HPQ-II was 121.2 (SD, 19.6; range, 78-159), and the
had a body mass index (BMI) category that classified them as median was 122.0. An examination of HPQ-II scores by
overweight or obese prepregnancy. age group classification revealed significant differences with

212 Volume 61, No. 2, March/April 2016


Table 2. Participant Scores on Study Instruments (N = 166)
Adolescents All Other Age Groups
(n = ) (n = )
Health Indicator (Score Range) Mean (SD) Mean (SD) P Value
a
Depressive symptomatology 13.7 (8.6) 13.9 (7.6) .21
Social supportb 34.1 (15.9) 40.6 (16.8) ⬍ 0.001
Engagement in favorable health practicesc 117.2 (21.9) 123.4 (18.8) ⬍ 0.001
a
Edinburgh Postnatal Depression Scale score range is 0-30.
b
Prenatal Psychosocial Profile score range is 11-66.
c
Health Practices in Pregnancy Questionnaire-II score range is 34-170.

adolescents reporting lower levels of engagement in favorable DISCUSSION


health practices when compared to women in all other age Findings from this study suggest that a woman’s mental
categories (117.2 vs 123.4, P ⬍ .001). Specifically, adolescents health is strongly associated with her ability to engage in
were significantly less likely to report concerns about their favorable health practices during pregnancy. In this sample,
health or questions about their pregnancies to a physician or 59% of the women reported depressive symptomatology.
midwife than women in all other age classifications. Further, Existing research demonstrates several sociodemographic
adolescents were more likely to report using marijuana, characteristics associated with a higher risk of perinatal de-
sleeping less than 7 hours at night, and missing more than pression, including poverty, single marital status, lower levels
one prenatal appointment (all P ⬍ .001 with Bonferroni of education, and young age.28–30 Findings from this study are
correction) than women in all other age classifications. similar to those of Lindgren who found that pregnant women
Importantly, 59% (n = 98) of the participants exceeded with increased depressive symptoms were less likely to engage
the cutoff score of greater than 12 on the EPDS, indicative in favorable health practices.27 Importantly, the majority of
of depressive symptomatology, and there were no significant the participants in the current study reported living in poverty
differences by age group classification. Finally, the mean score which precludes comparisons across many study samples.
on the social support subscale was 38.5 (SD = 16.7, range Research has demonstrated an association between
12-56), and adolescents reported significantly less social depression and smoking in pregnancy,31,32 and results from
support than women in all other age groups (34.1 vs 40.6, the current study suggest that depressive symptoms are
P ⬍ .001). associated with less favorable health practices across multiple
Participant scores on the HPQ-II and EPDS were strongly domains (ie, rest and exercise, safety measures, nutrition,
negatively correlated (r = −0.80; P ⬍ .001; Figure 1) suggest- substance use, health care access, access to pregnancy-related
ing that those participants with higher depressive symptoma- information) further highlighting the importance of screen-
tology reported less engagement in favorable health practices. ing for depression during pregnancy. Further studies with
Engagement in favorable health practices during pregnancy larger numbers of diverse adolescents in particular are needed
was strongly positively correlated with social support (r = to better understand the association between mental health
0.75, P ⬍ .001), suggesting that those women who perceived and engagement in favorable health practices.
greater social support reported engaging in more favorable Extant research also supports a link between social sup-
health practices than those women who perceived less social port and perinatal depression. That is, women reporting the
support. With regard to sociodemographic indicators, en- absence of a supportive partner are at significantly increased
gagement in favorable health practices during pregnancy was risk for perinatal depression.36 Social support is widely
positively correlated with adolescent age (r = 0.28, P ⬍ .001), associated with positive health outcomes.37 In a sample of
income (r = 0.31, P ⬍ .001), education (r = 0.47, P ⬍ .001), rural Hispanic women at risk for postpartum depression,
prepregnancy BMI classification of overweight or obese social support from a significant other and family member
(r = 0.32, P ⬍ .001), and was not significantly associated with were significant predictors of nutrition self-care.38
marital status or gravidity. Perceived social support was lower in the women in this
All measured sociodemographic characteristics, prepreg- sample than in other studies.39,40 An important finding in
nancy obesity, depressive symptomatology, and social the current study was that adolescents perceived less social
support were considered for inclusion in a multivariate support from a partner or close family member than women
linear regression model predicting engagement in favorable in all other age groups. Further, they were less likely to report
health practices during pregnancy. In the final model, age, asking a health care provider if they had questions related
prepregnancy obesity, depressive symptomatology, and social to the pregnancy or if there was something they didn’t un-
support were significant predictors. Specifically, younger age derstand. Research indicates that women who perceive more
(ie, 16-19 years), prepregnancy obesity, increased depressive social support are more likely to seek health information than
symptomatology, and decreased social support were all women who perceive less social support, yet this relationship
significant predictors of less favorable health practices during in adolescents heretofore was largely unexplored.37 In the
pregnancy (all P ⬍ .001). The final model accounted for current study, there were not significant differences in de-
67.8% of the total variance in overall engagement in favorable pressive symptomatology between adolescents and other age
health practices during pregnancy. groups, yet adolescents were less likely to engage in favorable

Journal of Midwifery & Women’s Health r www.jmwh.org 213


Figure 1. The Relation Between Engagement in Favorable Health Practices and Depressive Symptomatology
Scatterplot of the relation between health practices during pregnancy and depressive symptomatology. Higher scores on the HPQ-II indicative of
engagement in more favorable health practices. Higher scores on the EPDS indicative of greater depressive symptomatology.

health practices. A greater understanding of the role of classifications. Finally, a mixed-methods study conducted
social support and engagement in favorable health practices among a sample of low-income pregnant women, with a
is an important area of continued inquiry, particularly for mean prepregnancy BMI of 28.0, demonstrated that excessive
low-income women who have less formal support systems in weight gain was common, nutritional knowledge was poor,
place. Qualitative studies exploring how pregnant adolescents and few women engaged in healthy behaviors.45 Taken
define social support, who they turn to for support, and together, this research suggests that low-income women with
what resources they are inclined to access for pregnancy- prepregnancy obesity are in need of additional supports to
related information are needed to best address their unique optimize healthy behaviors during pregnancy.
needs. This study has several important limitations. First, study
Maternal obesity is a well-established risk factor for a measures were collected via self-report in a cross-sectional
number of adverse pregnancy, neonatal, and early childhood manner precluding our ability to make inferences about their
outcomes.41,42 Importantly, more than two-thirds of the causal relationships. Also, as is true in many studies that rely
women in this sample had a prepregnancy BMI classified as on self-report, tobacco use and substance use may have been
overweight or obese, and the presence of this classification underreported. Further, we did not have access to accurate
was an independent predictor of lower engagement in fa- data on weight gain during pregnancy, which is an important
vorable health practices during pregnancy. In a large sample consideration. Despite this, the final model explained a large
of women trying to conceive, obese women were more amount of variance in health practices during pregnancy.
likely to engage in unhealthy weight loss practices, including Finally, study findings are based on a convenience sample and
smoking.43 In a sample of low-income women, diet quality therefore cannot be generalized beyond this group of women.
(assessed via 24-hour diet recall) was not significantly related Nonetheless, this study provides compelling evidence of the
to prepregnancy BMI, yet women with low dietary quality important relations among social support, depressive symp-
had significantly more depression and less social support.44 tomatology, and engagement in favorable health practices
Importantly, the study was not powered to assess differences during pregnancy in a sample of low-income, predominantly
in dietary quality among depressed women of varied BMI African American women.

214 Volume 61, No. 2, March/April 2016


Clinical Implications engagement in favorable health practices during pregnancy.
Improving mental health care, particularly for low-income
The American College of Obstetricians and Gynecologists
women who face unique barriers to care, has significant im-
recommends that health care providers screen women at least
plications for the well-being of women, children, and families.
once during the perinatal period for depression and anxiety
As the work on health care reform continues, maternal-child
symptoms, acknowledging that perinatal depression often
health care providers are urged to play an active role in
goes unrecognized because changes in sleep, energy, and
further elucidating what should constitute essential services
appetite may be attributed to physiologic changes associated
for women’s health. Health care providers, researchers,
with pregnancy.33 Thus, it is particularly important that
policymakers, and health plan administrators must work
health care providers are assessing mental health early in the
together if we are to realize improvements in maternal and
perinatal period, given its association with health practices as
childhood outcomes during the perinatal period.
well as maternal and early childhood outcomes.
Low-income perinatal women, particularly adolescents,
face many barriers to treatment for depression and its re- AUTHORS
lated sequelae.34 Health care providers are urged to provide
Jeanne Alhusen, PhD, CRNP, RN, is an Assistant Professor in
critical linkages to gateway organizations, such as the local
the School of Nursing at Johns Hopkins University.
department of health, outpatient mental health programs,
and community-based organizations that include mental Lauren Ayres, BSN, RN, CCRN, is a registered nurse and fam-
health services as a component of care. Providing a referral ily nurse practitioner student in the School of Nursing at Johns
to a local home visiting (HV) program is another important Hopkins University.
consideration in optimizing health outcomes. While mental
Kelli DePriest, BSN, RN, is a registered nurse and doctoral stu-
health is not a primary focus of many home visiting programs,
dent in the School of Nursing at Johns Hopkins University.
research supports that a positive relationship between the
home visitor and the woman is beneficial to maternal mental
health, particularly among adolescents.34,35
CONFLICT OF INTEREST

Policy Implications The authors have no conflicts of interest to disclose.


The Patient Protection and Affordable Care Act46 expanded
health care coverage for millions of women, yet there are REFERENCES
many opportunities to further improve perinatal health,
1.Lindgren K. A comparison of pregnancy health practices of women in
and these will be discussed in context of the current study’s inner-city and small urban communities. J Obstet Gynecol Neonatal
findings. To optimize maternal health, experts have recom- Nurs. 2003;32:313-321.
mended that prenatal care be delivered within the context 2.Alhusen JL, Gross D, Hayat MJ, Rose L, Sharps P. The role of mental
of a medical home and that every woman in the United health on maternal-fetal attachment in low-income women. J Obstet
States should be provided access to a medical home.47,48 This Gynecol Neonatal Nurs. 2012;41(6):E71-E81.
would eliminate the fragmented health care delivery that 3.Witt WP, DeLeire T, Hagen EW, et al. The prevalence and determi-
nants of antepartum mental health problems among women in the
disproportionately impacts low-income women, allowing
USA: a nationally representative population-based study. Arch Wom-
them to utilize the medical home before, during, and beyond ens Ment Health. 2010;13(5):425-437.
pregnancies. Health care services should include primary 4.Haskins A, Bertone-Johnson E, Pekow P, Carbone E, Chasan-Taber L.
and preventive care, family planning, health education, Correlates of smoking cessation at pregnancy onset among Hispanic
and social services.48 This would allow for higher levels of women in Massachusetts. Am J Health Promot. 2010;25(2):100-108.
care coordination improving access to necessary supports. 5.Skagerstrom J, Chang G, Nilsen P. Predictors of drinking dur-
Further, greater attention could be given to the behavioral ing pregnancy: a systematic review. J Womens Health (Larchmt).
2011;20(6):901-913.
and psychosocial needs of each woman. In this model, the
6.Powers JR, McDermott LJ, Loxton DJ, Chojenta CL. A prospective
health educator is responsible for providing health pro- study of prevalence and predictors of concurrent alcohol and tobacco
motion activities either individually or in a group setting use during pregnancy. Matern Child Health J. 2013;17(1):76-84.
(eg, CenteringPregnancy), and the activities are focused on 7.Neggers Y, Goldenberg R, Cliver S, Hauth J. The relationship between
nutritional counseling, weight management, stress reduction, psychosocial profile, health practices, and pregnancy outcomes. Acta
and relevant behavioral modifications.48 Those women with, Obstet Gynecol Scand. 2006;85(3):277-285.
8.Forray A, Gotman N, Kershaw T, Yonkers KA. Perinatal smoking and
for example, significant dietary issues could be referred to
depression in women with concurrent substance use. Addict Behav.
a dietitian for further evaluation and treatment. This model 2014;39(4):749-756.
better targets health promotion activities while capitalizing on 9.Alhusen JL, Ray E, Sharps P, Bullock L. Intimate partner violence dur-
each provider’s strengths (eg, obstetricians aren’t providing ing pregnancy: Maternal and neonatal outcomes. Journal of Women’s
comprehensive nutritional counseling).48 Health. 2015;24:100-106.
10.Connelly CD, Hazen AL, Baker-Ericzen MJ, Landsverk J, Horwitz
SM. Is screening for depression in the perinatal period enough? The
CONCLUSION co-occurrence of depression, substance abuse, and intimate partner
violence in culturally diverse pregnant women. J Womens Health
Nearly two-thirds of the women in this sample reported (Larchmt). 2013;22(10):844-852.
depressive symptomatology, and depressive symptomatology 11.Grote NK, Bridge JA, Gavin AR, Melville JL, Iyengar S, Katon WJ. A
was significantly associated with poor social support and less meta-analysis of depression during pregnancy and the risk of preterm

Journal of Midwifery & Women’s Health r www.jmwh.org 215


birth, low birth weight, and intrauterine growth restriction. Arch Gen 29.Koleva H, Stuart S. Risk factors for depressive symptoms in adoles-
Psychiatry. 2010;67(10):1012-1024. cent pregnancy in a late-teen subsample. Arch Womens Ment Health.
12.Alder J, Fink N, Bitzer J, Hosli I, Holzgreve W. Depression and anx- 2014;17(2):155-158.
iety during pregnancy: a risk factor for obstetric, fetal and neonatal 30.Tzilos GK, Zlotnick C, Raker C, Kuo C, Phipps MG. Psychosocial fac-
outcome? A critical review of the literature. J Matern Fetal Neonatal tors associated with depression severity in pregnant adolescents. Arch
Med. 2007;20(3):189-209. Womens Ment Health. 2012;15(5):397-401.
13.Goedhart G, Snijders AC, Hesselink AE, van Poppel MN, Bonsel GJ, 31.Lancaster CA, Gold KJ, Flynn HA, Yoo H, Marcus SM, Davis MM.
Vrijkotte TG. Maternal depressive symptoms in relation to perinatal Risk factors for depressive symptoms during pregnancy: A systematic
mortality and morbidity: results from a large multiethnic cohort study. review. Am J Obstet Gynecol. 2010;202(1):5-14.
Psychosom Med. 2010;72(8):769-776. 32.Alhusen JL, Lucea MB, Bullock L, Sharps P. Intimate partner violence,
14.Lutsiv O, Mah J, Beyene J, McDonald SD. The effects of morbid obesity substance use, and adverse neonatal outcomes among urban women.
on maternal and neonatal health outcomes: a systematic review and J Pediatr. 2013;163:471-476.
meta-analyses. Obes Rev. 2015;16(7):531-546. 33.American College of Obstetricians and Gynecologists. Screening for
15.McDonald SD, McKinney B, Foster G, Taylor V, Lutsiv O, Pul- perinatal depression. Committee opinion no. 630. Obstet Gynecol.
lenayegum E. The combined effects of maternal depression and excess 2015;125:1268-1271.
weight on neonatal outcomes. Int J Obes (Lond). 2015;39(7):1033- 34.Hodgkinson S, Beers L, Southammakosane C, Lewin A. Addressing
1040. the mental health needs of pregnant and parenting adolescents. Pedi-
16.Luppino FS, de Wit LM, Bouvy PF, et al. Overweight, obesity, and de- atrics. 2014;133(1):114-122.
pression: a systematic review and meta-analysis of longitudinal studies. 35.Howard KS, Brooks-Gunn J. The role of home-visiting programs in
Arch Gen Psychiatry. 2010;67(3):220-229. preventing child abuse and neglect. Future Child. 2009;19(2):119-146.
17.Zhao G, Ford ES, Dhingra S, Li C, Strine TW, Mokdad AH. Depression 36.Lancaster CA, Gold KJ, Flynn HA, Yoo H, Marcus SM, Davis MM.
and anxiety among US adults: associations with body mass index. Int Risk factors for depressive symptoms during pregnancy: a systematic
J Obes (Lond). 2009;33(2):257-266. review. Am J Obstet Gynecol. 2010;202(1):5-14.
18.Kapadia MZ, Gaston A, Van Blyderveen S, et al. Psychological an- 37.Guillory J, Niederdeppe J, Kim H, et al. Does social support predict
tecedents of excess gestational weight gain: a systematic review. BMC pregnant mothers’ information seeking behaviors on an educational
Pregnancy Childbirth. 2015;15(1):107. website? Matern Child Health J. 2014;18(9):2218-2225.
19.Orr ST, James SA, Blackmore Prince C. Maternal prenatal depressive 38.Kim Y. The Self-Care Ability for Health Practices in Rural Hispanic
symptoms and spontaneous preterm births among African-American Women Experiencing Depressive Symptoms During Postpartum.
women in Baltimore, Maryland. Am J Epidemiol. 2002;156(9):797- Azusa, CA: Azusa Pacific University; 2014.
802. 39.Jesse DE, Walcott-McQuigg J, Mariella A, Swanson MS. Risks and pro-
20.Curry MA, Campbell RA, Christian M. Validity and reliability testing tective factors associated with symptoms of depresison in low-income
of the prenatal psychosocial profile. Res Nurs Health. 1994;17:127- African American and Caucasian women during pregnancy. J Mid-
135. wifery Womens Health. 2005;50:405-410.
21.Cox JL, Holden JM, Sagovsky R. Detection of postnatal depression. De- 40.Bloom T, Curry MA, Durham L. Abuse and psychosocial stress as fac-
velopment of the 10-item Edinburgh postnatal depression scale. Br J tors in high utilization of medical services during pregnancy. Issues
Psychiatry. 1987;150:782-786. Ment Health Nurs. 2007;28(8):849-866.
22.Lindgren K. Testing the health practices in pregnancy questionnaire- 41.Aviram A, Hod M, Yogev Y. Maternal obesity: implications for preg-
II. J Obstet Gynecol Neonatal Nurs. 2005;34:465-472. nancy outcome and long-term risks—a link to maternal nutrition. Int
23.Davis K, Pearlstein T, Stuart S, O’Hara M, Zlotnick C. Analysis of brief J Gynaecol Obstet. 2011;115(Suppl 1):S6-10.
screening tools for the detection of postpartum depression: compar- 42.Bryant AS, Worjoloh A, Caughey AB, Washington AE. Racial/ethnic
isons of the PRAMS 6-item instrument, PHQ-9, and structured inter- disparities in obstetric outcomes and care: prevalence and determi-
views. Arch Womens Ment Health. 2013;16(4):271-277. nants. Am J Obstet Gynecol. 2010;202(4):335-343.
24.Ryan D, Milis L, Misri N. Depression during pregnancy. Can Fam 43.Berenson AB, Pohlmeier AM, Laz TH, Rahman M, McGrath CJ. Nutri-
Physician. 2005;51(8):1087-1093. tional and weight management behaviors in low-income women try-
25.Alhusen JL, Gross D, Hayat MJ, Rose L, Sharps P. The role of mental ing to conceive. Obstet Gynecol. 2014;124(3):579-584.
health on maternal-fetal attachment in low-income women. J Obstet 44.Fowles ER, Stang J, Bryant M, Kim S. Stress, depression, social sup-
Gynecol Neonatal Nurs. 2012;41(6):E71-E81. port, and eating habits reduce diet quality in the first trimester in
26.Tandon SD, Cluxton-Keller F, Leis J, Le HN, Perry DF. A compari- low-income women: a pilot study. J Acad Nutr Diet. 2012;112(10):
son of three screening tools to identify perinatal depression among 1619-1625.
low-income African American women. J Affect Disord. 2012;136 45.Hackley B, Kennedy HP, Berry DC, Melkus GD. A mixed-methods
(1-2):155-162. study on factors influencing prenatal weight gain in ethnic-minority
27.Lindgren K. Relationships among maternal-fetal attachment, prena- women. J Midwifery Womens Health. 2014;59(4):388-398.
tal depression, and health practices in pregnancy. Res Nurs Health. 46.Mar 23, The Patient Protection and Affordable Care Act (PPACA).
2001;24:203-217. 2010; Pub. L. No. 111–148, 124 Stat.
28.Liu CH, Tronick E. Rates and predictors of postpartum depression 47.Pies C, Kotelchuck M. Bringing the MCH life course perspective to life.
by race and ethnicity: results from the 2004 to 2007 New York Matern Child Health J. 2014;18(2):335-338.
City PRAMS survey (pregnancy risk assessment monitoring system). 48.Lu MC. Healthcare reform and women’s health: a life-course perspec-
Matern Child Health J. 2013;17(9):1599-1610. tive. Curr Opin Obstet Gynecol. 2010;22(6):487-491.

216 Volume 61, No. 2, March/April 2016


ARTICLE
DOI: 10.1038/s41467-018-06748-3 OPEN

Pregnancy duration and breast cancer risk


Anders Husby 1,2, Jan Wohlfahrt1, Nina Øyen1,3,4 & Mads Melbye 1,5,6

Full-term pregnancies reduce a woman’s long-term breast cancer risk, while abortions have
been shown to have no effect. The precise minimal duration of pregnancy necessary to lower
a woman’s breast cancer risk is, however, unknown. Here we provide evidence which point to
1234567890():,;

the protective effect of pregnancy on breast cancer risk arising precisely at the 34th preg-
nancy week. Using a cohort of 2.3 million Danish women, we found the reduction in breast
cancer risk was not observed for pregnancies lasting 33 weeks or less, but restricted to those
pregnancies lasting 34 weeks or longer. We further found that parity, socioeconomic status,
and vital status of the child at birth did not explain the association, and also replicated our
finding in data from 1.6 million women in Norway. We suggest that a distinct biological effect
introduced around week 34 of pregnancy holds the key to understand pregnancy-associated
breast cancer protection.

1 Department of Epidemiology Research, Statens Serum Institut, DK-2300 Copenhagen, Denmark. 2 Department of Biomedical Data Science, Stanford

University School of Medicine, Stanford, CA 94305, USA. 3 Department of Global Public Health and Primary Care, Faculty of Medicine, University of Bergen,
N-5020 Bergen, Norway. 4 Department of Medical Genetics, Haukeland University Hospital, N-5021 Bergen, Norway. 5 Department of Clinical Medicine,
University of Copenhagen, DK-2100 Copenhagen, Denmark. 6 Department of Medicine, Stanford University School of Medicine, Stanford, CA 94305, USA.
Correspondence and requests for materials should be addressed to M.M. (email: mme@ssi.dk)

NATURE COMMUNICATIONS | (2018)9:4255 | DOI: 10.1038/s41467-018-06748-3 | www.nature.com/naturecommunications 1


ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/s41467-018-06748-3

B
reast cancer is the most common malignant cancer in risk reduction per birth), pregnancies lasting 34 weeks or longer
women and a major cause of disease burden worldwide1. were associated with a substantially reduced risk (on average
Both the number and timing of a woman’s childbirths have 12.9% (95% CI: 11.4% to 14.3%) risk reduction per birth).
long been known to influence her breast cancer risk2, but how Additionally, to examine the role of breastfeeding, we investigated
these factors influence breast cancer etiology is not well under- the effect of stillbirths, which are not breastfeed, and found that
stood. Previously, full-term pregnancies in early life (<30 years) both live births and stillbirths were associated with reduced breast
have consistently been associated with a long-term reduced risk of cancer risk, but only if delivered at week 34 or later (Table 2).
breast cancer3,4. Conversely, a transient increased breast cancer We replicated the analyses in a similar cohort of 1,635,839
risk immediately following full-term pregnancies have been Norwegian women with altogether 2,420,518 pregnancies identi-
observed5. Induced abortions and other pregnancies of short fied in the National Registry and the Norwegian Medical Birth
duration have, on the other hand, been shown not to influence Registry. The women were followed for 35,171,205 person-years,
breast cancer risk6,7. We hypothesized that by investigating in which 24,095 developed invasive breast cancer.
pregnancies of intermediate to long duration in early life Figure 2b illustrates the long-term RR of breast cancer after an
(including stillbirths, preterm, and term livebirths) we could early age childbirth compared with one childbirth less, according
determine the minimal duration of pregnancy associated with a to duration of pregnancy, in the Norwegian cohort. As shown, we
reduced risk of breast cancer and thereby potentially point to found a pattern identical to the results obtained in the Danish
underlying mechanisms of the protective effect. cohort. In the Norwegian cohort, the average reduction in long-
Taking advantage of the Danish national registries on child- term breast cancer risk associated with a pregnancy lasting
births and cancer, we established a nationwide cohort including 33 weeks or less were 2.9% (95% CI: −7.7% to 12.6%), whereas
2.3 million women with detailed information on reproductive the reduction with pregnancies lasting 34 weeks or more were
history from 1978 to 2014, and assessed the association between 14.5% (95% CI: 13.1% to 15.8%).
the duration of a pregnancy and the long-term risk of breast When we combined the Danish and Norwegian cohorts
cancer. We replicated this analysis in an equivalent Norwegian (Fig. 2c), the reduction in long-term breast cancer risk associated
cohort of 1.6 million women. with early childbirth was 2.4% (95% CI: −5.6% to 9.7%) for
pregnancies lasting 33 weeks or less and 13.6% (95% CI: 12.6%
to 14.5%) for pregnancies lasting 34 weeks or longer. The reduced
Results
risk of breast cancer for pregnancies lasting 34 weeks or more
Cohort description and age at pregnancy. The Danish cohort
could have been modified by the number of previous pregnancies
consisted of 2,311,332 women, with altogether 3,275,559 child-
lasting 33 weeks or less, but the risk reduction was similar for no
births. The women were followed for 46,128,328 person-years
previous births <34 weeks, 13.5% (95% CI: 12.5% to 14.5%); one
(average 20.0 years follow-up per woman) and 61,349 (2.7%)
previous birth <34 weeks, 16.9% (95% CI: 10.2% to 23.1%); or two
developed breast cancer. We focused on follow-up from 10 years
or more previous births <34 weeks, 37.7% (95% CI: 7.5%
or more after pregnancy, to highlight the long-term effect of
to 58.1%). Furthermore, to avoid a possible distinct effect of a
pregnancy on breast cancer risk. Table 1 shows number of breast
woman’s first childbirth on cancer risk, we focused on the effect
cancer events and follow-up time according to number of
of a second, third, or any additional childbirth, among women in
childbirths, age at first childbirth, and duration of latest
Denmark and Norway (Supplementary Fig. 2), and found that the
pregnancy.
reduction in long-term breast cancer risk associated with early
Figure 1 shows the long-term relative risk (RR) of breast cancer
age childbirth was 1.2% (95% CI: −11.2% to 12.4%) for
after first childbirth by age at delivery, adjusted for different
pregnancies lasting 33 weeks or less and 16.3% (95% CI: 14.9%
socioeconomic variables. Overall, we found a first childbirth
to 17.8%) for pregnancies lasting 34 weeks or longer.
before 30 years of age to decrease the long-term breast cancer
We performed additional sensitivity analyses to evaluate the
risk. Further, to investigate the effect of both first and subsequent
association between a specific duration of a pregnancy and a
childbirths in early age on long-term breast cancer risk, we
woman’s long-term breast cancer risk (see Supplementary Fig. 3
estimated the effect of first, second, and third childbirth,
for effect of relative birthweight and Supplementary Fig. 4 for
compared with one childbirth less (Supplementary Fig. 1). For
effect of induced abortions and childbirths). Adjusting for
childbirths before 30 years of age, women’s long-term breast
individual-level socioeconomic differences, we found no strong
cancer risk was reduced for the first childbirth (on average 5.0%
confounding effect of socioeconomic factors on breast cancer risk
(95% CI: 2.1% to 7.8%)), the second (on average 6.4% (95% CI:
in the analysis of pregnancy duration (Supplementary Fig. 5). In
3.9% to 8.8%)), and the third childbirth (on average 9.4% (95%
analysis of threshold models, where all risk reduction occur in
CI: 6.4% to 12.2%)). For childbirths at 30 years or later, we did
pregnancies lasting longer than a specific duration, we further-
not observe a consistent, overall reduced long-term breast cancer
more found the best fit of data for a threshold of 34 weeks
risk (first birth: −8.7% (95% CI: −12.8% to −4.8%), second birth:
duration of pregnancy (Supplementary Fig. 6A). The same
3.4% (95% CI: 0.7% to 6.0%), third birth: 5.3% (95% CI: 2.7%
conclusion was reached when allowing the protective effect in
to 7.8%)).
the models to vary by parity and country (Supplementary Fig. 6B
and Supplementary Fig. 6C).
Pregnancy duration and breast cancer risk. We speculated
whether the observed reduced long-term breast cancer risk fol-
lowing any birth at an early age varied by pregnancy duration. To Discussion
study this, we included information on pregnancy duration. The strongest known modifier of a woman’s breast cancer risk is
Figure 2a shows the long-term RR of breast cancer after an early her reproductive history. Thus, early age full-term pregnancies
age childbirth compared with one childbirth less, by pregnancy and an increasing number of childbirths3,4 result in a lowered
duration. We noted a distinctive difference in the cancer risk breast cancer risk, whereas abortions do not influence breast
associated with pregnancies lasting 34 weeks and longer com- cancer risk6,7. Previous studies on preterm birth and breast cancer
pared with pregnancies lasting 33 weeks or less. Whereas preg- risk have nevertheless not had statistical power to show any
nancies 33 weeks or less were not associated with long-term specific effect of pregnancy duration on breast cancer risk8–11. In
breast cancer risk (on average 2.3% (95% CI: −10.0% to 13.2%) the present study, we provide evidence that the protection

2 NATURE COMMUNICATIONS | (2018)9:4255 | DOI: 10.1038/s41467-018-06748-3 | www.nature.com/naturecommunications


NATURE COMMUNICATIONS | DOI: 10.1038/s41467-018-06748-3 ARTICLE

Table 1 Breast cancer events and person-years according to number of childbirths, age at first childbirth, and duration of latest
pregnancy in the Danish and the Norwegian cohorta

Cohort characteristic The Danish cohort The Norwegian cohort


Breast cancer events Persons-years in 1000s Breast cancer events Persons-years in 1000s
(%) (%) (%) (%)
Number of childbirths
0 8028 (13.1) 23,370 (50.7) 2880 (13.9) 13,861 (55.1)
1 10,523 (17.1) 4418 (9.6) 2996 (14.4) 1850 (7.3)
2 28,046 (45.7) 11,938 (25.9) 8582 (41.3) 5268 (20.9)
3 11,468 (18.7) 4888 (10.6) 4639 (22.3) 2965 (11.8)
4 2667 (4.3) 1175 (2.5) 1313 (6.3) 901 (3.6)
≥5 617 (1.0) 340 (0.7) 367 (1.8) 324 (1.3)
Age at first childbirth (years)
Nulliparous 8028 (13.1) 23,370 (50.7) 2880 (13.9) 13,861 (55.1)
<20 8538 (13.9) 4109 (8.9) 3021 (14.5) 2490 (9.9)
20–21 9630 (15.7) 4535 (9.8) 3692 (17.8) 2682 (10.7)
22–23 10,150 (16.5) 4569 (9.9) 3320 (16.0) 2221 (8.8)
24–25 8956 (14.6) 3814 (8.3) 2957 (14.2) 1695 (6.7)
26–27 6373 (10.4) 2531 (5.5) 1979 (9.5) 1018 (4.0)
28–29 4087 (6.7) 1489 (3.2) 1247 (6.0) 579 (2.3)
≥30 5587 (9.1) 1712 (3.7) 1681 (8.1) 621 (2.5)
Duration of latest pregnancy (weeks)b
Nulliparous 8028 (13.1) 23,370 (50.7) 2880 (13.9) 13,861 (55.1)
20–27 34 (0.1) 12 (0.0) 29 (0.1) 16 (0.1)
28–29 38 (0.1) 18 (0.0) 22 (0.1) 15 (0.1)
30 33 (0.1) 14 (0.0) 20 (0.1) 13 (0.1)
31 33 (0.1) 16 (0.0) 40 (0.2) 18 (0.1)
32 54 (0.1) 26 (0.1) 44 (0.2) 25 (0.1)
33 78 (0.1) 35 (0.1) 62 (0.3) 36 (0.1)
34 101 (0.2) 54 (0.1) 92 (0.4) 61 (0.2)
35 178 (0.3) 81 (0.2) 154 (0.7) 100 (0.4)
36 360 (0.6) 163 (0.4) 262 (1.3) 170 (0.7)
37 719 (1.2) 332 (0.7) 507 (2.4) 334 (1.3)
38 1626 (2.7) 798 (1.7) 1254 (6.0) 792 (3.1)
39 3091 (5.0) 1519 (3.3) 2959 (14.2) 1795 (7.1)
40 6369 (10.4) 3062 (6.6) 3902 (18.8) 2523 (10.0)
41 2846 (4.6) 1446 (3.1) 2877 (13.8) 1886 (7.5)
≥42 1288 (2.1) 685 (1.5) 1777 (8.6) 1222 (4.9)
Missing duration of pregnancy in birth 1493 (2.4) 662 (1.4) 638 (3.1) 471 (1.9)
register
Childbirths registered in civil registersc 34,980 (57.0) 13,835 (30.0) 3217 (15.5) 1799 (7.1)
aAll events and person-years from 10 years after latest childbirth
bPregnancies registered to have lasted less than 20 weeks or more than 45 gestational weeks were also included in the analysis as separate categories (see Statistical analyses), but constituted
combined only <0.01% and 0.13% of observation time in Denmark and Norway, respectively
cChildbirths
registered in the civil registration systems, but not in the Birth Registers. Predominantly childbirths before January 1, 1978 in Denmark and January 1, 1967 in Norway. After these dates only
3.34% and 3.85% of childbirths are not reported in the Medical Births Registers, in Denmark and Norway, respectively

introduced by a pregnancy takes place around a specific preg- pregnancies. Taken together this gives little support to the
nancy week. Using Danish nationwide registers, we found the hypothesis of a decisive and particularly distinct effect on
minimal pregnancy length associated with a substantial reduced mammary tissue caused by the first pregnancy that associates
risk of long-term breast cancer to be 34 weeks, whereas a preg- with later breast cancer risk.
nancy length of 33 weeks or less did not confer a reduction in Multiple studies have pointed to persistent changes in gene
risk. The exact same result was obtained in a Norwegian repli- expression14,15, epigenetic structure16–20, and epithelial stem cell
cation cohort based on similar nationwide register data. composition18,21 in the mammary gland following pregnancy.
It has been hypothesized that a woman’s first pregnancy has a However, the mechanisms proposed for pregnancy-induced
special influence on mammary tissue structural remodeling12, breast cancer protection have neither been substantiated or
and that this might explain the reduced risk of breast cancer later replicated. Our novel finding that pregnancy-induced breast
in life. It has specifically been suggested that pregnancy-induced cancer protection is obtained within a narrow time window, late
differentiation of breast cells at this first pregnancy might make in pregnancy, will enable a meticulous investigation of the causal
them less sensitive to influences from external carcinogenic sti- factor behind this striking effect. Furthermore, a precise char-
muli13. However, we found that additional childbirths further acterization of the factor responsible for the effect will be helped
reduce breast cancer risk and that the effect observed by these by our observation that each early age pregnancy offers cumu-
additional births is at a similar level as observed for the first birth. lative protection against breast cancer. Altogether, our results can
In addition, the specific effect of a pregnancy lasting 34 weeks or open a path to explore the specific biological mechanism behind
longer on later breast cancer risk was also evident in subsequent the impact of pregnancies on subsequent breast cancer risk.

NATURE COMMUNICATIONS | (2018)9:4255 | DOI: 10.1038/s41467-018-06748-3 | www.nature.com/naturecommunications 3


ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/s41467-018-06748-3

Our observations are in line with findings from mammalian status of the infant at birth do not influence the long-term breast
breast cancer models that show a protective effect of pregnancy cancer risk.
introduced close to term22. In theory, late-pregnancy stimuli that Breastfeeding, and in particular the total breastfeeding dura-
transform the breast tissue to a stage represented by a lowered tion, has been proposed to protect against breast cancer25 and
breast cancer risk could originate from both the mother and the could potentially explain the association with pregnancy length.
fetus. However, findings by us and others provide little evidence However, at least two of our findings strongly argue against this
for a fetal involvement since infant sex23, infant absolute being the case. First, we found an equivalent protective effect on
birthweight10,24 or, as we show, fetal growth restriction and vital breast cancer risk of stillbirths and live births from the 34th
gestational week. Second, the pregnancy-induced risk reduction
1.15 of breast cancer was restricted to young women below 30 years of
No socioeconomic adjustment age at childbirth, whereas the total breastfeeding duration is
1.10 Adjusted for employment status shortest for mothers younger than 30 years26 and does not vary
Adjusted for educational attainment
Adjusted for disposable household income
markedly by gestational length of pregnancy27.
1.05 Adjusted for all socioeconomic covariates High levels of alcohol consumption are found to be associated
with an increased risk of breast cancer28,29, and there are reports
Relative risk

1.00 of an association between heavy alcohol consumption and pre-


term birth30,31, why alcohol consumption could be a potential
0.95 factor in the association between pregnancy duration and breast
cancer risk. There are however large differences in alcohol con-
0.90 sumption between Denmark and Norway, with studies of
drinking patterns finding that this is the case both with regards to
0.85 drinking frequency and volume32,33, with differences in alcohol
<20 20−21 22−23 24−25 26−27 28−29 30+
consumption being especially pronounced during pregnancy30,34.
Given the marked differences in alcohol consumption between
Age at first childbirth (years)
Denmark and Norway, and the identical findings on the asso-
Fig. 1 Effect of different socioeconomic factors on long-term relative risk of ciation between pregnancy duration and breast cancer risk, we
breast cancer after first childbirth in Denmark compared with nulliparous, find it unlikely that alcohol consumption serves as a major
by age at delivery. Error bars indicate 95% confidence intervals

a Denmark
1.20
1.10
Relative risk

1.00

0.90

0.80

20−27 28−29 30 31 32 33 34 35 36 37 38 39 40 41 42+

b Norway
1.20
1.10
Relative risk

1.00

0.90

0.80

20−27 28−29 30 31 32 33 34 35 36 37 38 39 40 41 42+

c Denmark and Norway


1.20
1.10
Relative risk

1.00

0.90

0.80

20−27 28−29 30 31 32 33 34 35 36 37 38 39 40 41 42+

Duration of pregnancy (weeks)

Fig. 2 Long-term relative risk of breast cancer after an early age childbirth compared with one childbirth less, according to duration of pregnancy. a
Denmark, b Norway, and c combined. Error bars indicate 95% confidence intervals

4 NATURE COMMUNICATIONS | (2018)9:4255 | DOI: 10.1038/s41467-018-06748-3 | www.nature.com/naturecommunications


NATURE COMMUNICATIONS | DOI: 10.1038/s41467-018-06748-3 ARTICLE

196737 and the Cancer Registry is considered accurate and close to complete with
Table 2 Long-term relative risk of breast cancer after an regard to cancer diagnoses from 195338.
early age childbirth compared with one childbirth less, The research project was approved by institutional review for inclusion on
according to the duration of pregnancy and type of Statens Serum Institutes permit for research projects given by the Danish Data
childbirth in the Danish cohort Protection Agency (permit No. 2015-57-0102) and approved by the Regional Ethics
Committee of Western Norway (permit 252.06).

Type of childbirtha Duration of Pregnancy


Subjects. We established a cohort of all Danish women born between January 1,
<34 weeks ≥34 weeks 1935 and December 31, 2002. Using the CRS number, we linked information on
each woman’s childbirths with the corresponding pregnancy duration (gestational
Unadjusted for socioeconomic factors
week of delivery), and information on whether she developed invasive breast
Live birth 0.99 (0.87–1.12) 0.87 (0.86–0.89) cancer. We furthermore established a cohort of all Norwegian women born
Stillbirth 0.84 (0.54–1.30) 0.69 (0.51–0.94) between January 1, 1935 and December 31, 1994, with equivalent information on
Adjusted for socioeconomic factorsb reproductive history and breast cancer.
Live birth 0.99 (0.87–1.12) 0.87 (0.85–0.88)
Stillbirth 0.84 (0.54–1.30) 0.69 (0.51–0.94) Statistical analyses. Incidence rate ratios (in the following termed RR) of breast
Unadjusted and adjusted for socioeconomic factors (with corresponding 95% confidence
cancer by pregnancy history were estimated by log-linear Poisson regression in the
intervals) Danish cohort, the Norwegian cohort, and the combined cohort. In Denmark, each
aOf the total number of childbirths in the Danish cohort with known duration of pregnancy 3442 woman was followed from January 1, 1978, or from her 12th birthday, whichever
(0.18%) were stillbirths before week 34, 5970 (0.31%) were stillbirths at week 34 or later, came later, until breast cancer, death, emigration or December 31, 2014, whichever
30,437 (1.56%) were live births before week 34 and 1,912,529 (97.96%) were live births at came first. In Norway, each woman was followed from January 1, 1967, or from her
week 34 or later
bAdjustment for disposable household income, level of educational attainment, and employment 12th birthday, whichever came later, until breast cancer, death, emigration or
status December 31, 2006, whichever came first. All analyses were adjusted for effects of
current age and time period in 5-year categories.
Pregnancy history was modeled by time-dependent variables as described
previously4. Thus, instead of describing history by the total number of childbirths
confounding factor for the association between pregnancy dura- (i.e., RR of cancer in women with 1, 2, 3, or 4 births compared with women with 0
tion and maternal breast cancer risk. births), pregnancy history was evaluated by the RR for women with n births
Using prospective national registers ensured high validity, compared with women with n−1 births (i.e., RR of cancer for 1 birth compared
with 0, 2 births compared with 1, and 3 births compared with 2). This
negligible selection bias, and minimal misclassification of reparameterization allows for a focus on the effect of each additional birth on
women’s number of childbirths, and timing of these births. In cancer risk. The RRs were assumed to be the same regardless of birth number, and
addition, the gestational duration of pregnancy is determined by the presented RRs are therefore RRs for each additional birth. To allow for a
medical professionals at the time of pregnancy which ensures different short-term and long-term effect of pregnancy, RRs were allowed to vary
according to time since birth (<10 years, ≥10 years) for parous women. In the
proper classification of the pregnancy duration. The long follow- presentation of the model we focused on the parameters related to the long-term
up and the nationwide scope of the study furthermore provided effect of pregnancy. We furthermore allowed RRs to be different for childbirths at
high statistical power, and the replication using Norwegian younger (<30 years) and older maternal age (≥30 years) to focus on early age
national registers underlined the validity of the findings. Finally, pregnancies which have previously been associated with long-term reduced risk of
socioeconomic status and other potential confounding factors did breast cancer3,4. The previously used method (4) was extended to include
pregnancy duration. In the previous approach the effect of each birth was stratified
not explain the association of minimal pregnancy duration and according to time since birth and age at childbirth, but in this extended approach it
long-term breast cancer risk. was further stratified by pregnancy duration. Thus, RRs were allowed to vary by
In conclusion, we found that each pregnancy in early age, and duration of the pregnancy in weeks, by the following categories: 20–27, 28–29, 30,
not only the first, is associated with a significant long-term pro- 31, …, 41, 42–45 weeks, missing duration of pregnancy, duration of pregnancy not
reported, extremely early births (<20 weeks), and extremely late births (>45 weeks).
tective effect against breast cancer. Furthermore, only pregnancies The four last categories are further described in Table 1, Supplementary Table 1,
lasting 34 weeks or longer were associated with a reduction in and Supplementary Table 2.
breast cancer risk. The reduction in breast cancer risk was present In the analysis of pregnancy duration, all parameters described above were
regardless of whether the pregnancy ended in stillbirth or live included simultaneously. For example, for biparous women whose first birth
occurred in early age at week 38 and whose second birth occurred in late age at
birth, and therefore cannot be explained by breastfeeding. This week 40, their pregnancy history was modeled by four parameters: the short-term
suggests that a specific biological effect operating around week 34 and long-term effect of an early age birth at week 38, and the short-term and long-
of pregnancy induces long-term breast cancer protection. term effect of a late age birth at week 40. Thus, when estimating the long-term
effect of the early age pregnancy at week 38, the model also included the short-term
effect of an early age pregnancy at week 38, the short-term effect of an late age
Methods pregnancy at week 40, and the long-term of an late age pregnancy at week 40.
Population registries. We established a population-based cohort of Danish The analysis of pregnancy duration was based on follow-up time from January
women by linking data from the Civil Registration System (CRS) with data from 1, 1978 in Denmark, and from January 1, 1967 in Norway, when the respective
the Medical Birth Registry and the Danish Cancer Registry. The CRS contains Medical Birth Registers began recording gestational week of birth. Childbirths
detailed demographic information on all Danish residents, including linkage of registered in civil registrations systems were incorporated in the analyses to adjust
women to their children’s dates of birth. Since April 1, 1968, all Danish residents for the effects of pregnancies before start of the Medical Birth Registers.
who were alive or born thereafter have been assigned a unique identification In analysis of the effect of age at childbirth on breast cancer risk, RRs were
number in the CRS. This number permits information from different national allowed to vary according to age at delivery in the categories <20, 20–21, 22–23,
registries to be linked together. All live and stillbirths in Denmark, with dates of 24–25, 26–27, 28–29 and ≥30 years. In analyses of the adjustment effect of
birth, have been registered since 1973 in the Medical Birth Registry. Since 1978, socioeconomic status, each socioeconomic variable was added as an additional
gestational week at time of birth has been recorded. For sensitivity analyses, we variable.
obtained information on induced abortions in Denmark from the National Registry All analyses were performed using SAS version 9.4 and procedure GENMOD.
of Induced Abortions, where induced abortions have been mandatory reported to
since 1939.
Information on breast cancer diagnoses was retrieved from the Danish Cancer Socioeconomic factors and risk of breast cancer. Using nationwide registries
Registry, which contains information on all cancers diagnosed in Denmark since from Statistics Denmark on educational attainment, employment and disposable
1943 and is considered close to complete35. From Statistics Denmark we acquired household income starting from respectively 1970, 1976, and 1990, we were able to
time-varying, individual-level socioeconomic data to address covariates potentially create a time-varying, three factor adjustment for socioeconomic status. The fol-
associated with reproduction and breast cancer36; educational attainment (since lowing categories of the three variables for socioeconomic status were used:
1970), employment status (since 1976), and disposable household income (since Educational attainment: primary schooling; high school; high school with
1990). technical or mercantile focus; short basic education; higher education of short
In Norway, we linked data from the National Registry, the Medical Birth duration; higher education of intermediate duration; academic bachelor degree;
Registry of Norway, and the Cancer Registry of Norway. The Medical Birth academic master’s degree; and academic doctoral degree or equivalent educational
Registry has registered all births (including gestational week of delivery) since degree.

NATURE COMMUNICATIONS | (2018)9:4255 | DOI: 10.1038/s41467-018-06748-3 | www.nature.com/naturecommunications 5


ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/s41467-018-06748-3

Employment status: business owner, ten or more employees; business owner, 2. MacMahon, B. et al. Age at first birth and breast cancer risk. Bull. World
five to nine employees; business owner, one to four employees; business owner, no Health Organ. 43, 209–221 (1970).
employees; business owner, unknown number of employees; co-working spouse; 3. Albrektsen, G., Heuch, I., Hansen, S. & Kvåle, G. Breast cancer risk by age at
executive officer in business, organization or public office; employee in job which birth, time since birth and time intervals between births: exploring interaction
necessitates advanced skills; employee in job which necessitates intermediate skills; effects. Br. J. Cancer 92, 167–175 (2005).
employee in job which necessitates basic skills; employee, other; employee, 4. Wohlfahrt, J. & Melbye, M. Age at any birth is associated with breast cancer
unknown position; unemployed for more than 6 months; social security recipient risk. Epidemiology 12, 68–73 (2001).
because of disability; in educational program; disability pensioner; pensioner; early
5. Lambe, M. et al. Transient increase in the risk of breast cancer after giving
retirement pensioner; social security recipient; other; children under the age of 15
birth. N. Engl. J. Med. 331, 5–9 (1994).
years; housewife (only categorized 1976–1990).
6. Melbye, M. et al. Induced abortion and the risk of breast cancer. N. Engl. J.
Disposable household income: groups of 10%-percentiles according to the 5-
Med. 336, 81–85 (1997).
year disposable household income distribution.
7. Beral, V. et al. Breast cancer and abortion: collaborative reanalysis of data from
53 epidemiological studies, including 83 000 women with breast cancer from
Birthweight and maternal risk of breast cancer. In order to investigate the effect 16 countries. Lancet 363, 1007–1016 (2004).
of birthweight relative to gestational age in pregnancies of different duration, we 8. Melbye, M., Wohlfahrt, J., Andersen, A. M., Westergaard, T. & Andersen, P.
combined data on gestational age and birthweight from the Danish Medical Birth K. Preterm delivery and risk of breast cancer. Br. J. Cancer 80, 609–613 (1999).
Registry compiled from 1978 and onwards. We defined a birth small for gestational 9. Kaijser, M., Akre, O., Cnattingius, S. & Ekbom, A. Preterm birth, birth weight,
age (SGA) if the birthweight was below the 10th percentiles of births at the given and subsequent risk of female breast cancer. Br. J. Cancer 89, 1664–1666
gestational week, in the corresponding 5-year period. We then stratified by weight (2003).
category (SGA vs. 10–100th percentile of birthweights at same week) and assessed 10. Hajiebrahimi, M., Cnattingius, S., Lambe, M. & Bahmanyar, S. Pregnancy
risk of breast cancer after a pregnancy of given duration, grouped into the following history and risk of premenopausal breast cancer—a nested case–control study.
lengths of pregnancy: week 20–33, week 34–36, week 37, 38, 39, 40, 41, and week Int. J. Epidemiol. 45, 816–824 (2016).
42 or longer. To estimate RR of breast cancer by both relative birthweight and
11. Kessous, R. et al. Preterm delivery and future maternal risk of female
gestational period, we extended the model so that the pregnancy effect also varied
malignancies. Arch. Gynecol. Obstet. 295, 205–210 (2017).
by relative birthweight.
12. Russo, J., Moral, R., Balogh, G. A., Mailo, D. & Russo, I. H. The protective role
of pregnancy in breast cancer. Breast Cancer Res. 7, 131 (2005).
Threshold model analysis of pregnancy duration and risk of breast cancer. 13. Russo, J. & Russo, I. H. The etiopathogenesis of breast cancer prevention.
Our estimates of the effect of an early age pregnancy stratified by the duration of Cancer Lett. 90, 81–89 (1995).
pregnancy (Fig. 2c) suggest that pregnancies lasting 34 gestational weeks are 14. Russo, J., Balogh, G. A. & Russo, I. H. Full-term pregnancy induces a specific
necessary to obtain a long-term reduced risk of breast cancer. To substantiate this genomic signature in the human breast. Cancer Epidemiol. Biomark. Prev. 17,
conclusion we compared the observed pattern in Fig. 2c with week-specific 51–66 (2008).
threshold models, where breast cancer risk reduction is achieved only by preg- 15. Asztalos, S. et al. Gene expression patterns in the human breast after
nancies with a specific minimal duration or longer. The threshold model with the pregnancy. Cancer Prev. Res. 3, 301–311 (2010).
least difference in fit from the observed pattern in Fig. 2c is interpreted as providing 16. Russo, J. et al. Pregnancy-induced chromatin remodeling in the breast of
the best estimate for the critical length of pregnancy necessary for the long-term postmenopausal women. Int. J. Cancer 131, 1059–1070 (2012).
breast cancer risk reduction. 17. Ghosh, S. et al. Genome-wide DNA methylation profiling reveals parity-
The model used in Supplementary Figure 6 is in the following termed Mfig2C. In associated hypermethylation of FOXA1. Breast Cancer Res. Treat. 147,
this model, the long-term effect of each early age pregnancy with duration of the
653–659 (2014).
pregnancy w, is modeled as βw, with w noting the gestational week categories
18. Huh, S. J. et al. Age- and pregnancy-associated DNA methylation changes in
described in the paper. We compared Mfig2C with simple week-specific threshold
mammary epithelial cells. Stem Cell Rep. 4, 297–311 (2015).
models (Mthreshold(w0)) by which a certain threshold of pregnancy duration is
19. dos Santos, C. O., Dolzhenko, E., Hodges, E., Smith, A. D. & Hannon, G. J. An
associated with a decreased risk of breast cancer. In that model the long-term effect
epigenetic memory of pregnancy in the mouse mammary gland. Cell Rep. 11,
of each early-age pregnancy according to the duration of the pregnancy w is
modeled as β∙I(w ≥ w0), i.e., by one parameter. With regard to the other parameters 1102–1109 (2015).
in the model, the two models are similar, i.e., a total difference of 14 parameters. 20. Katz, T. A. et al. Targeted DNA methylation screen in the mouse mammary
We furthermore compared models that allowed for difference in the pregnancy genome reveals a parity-induced hypermethylation of Igf1r that persists long
effect according to parity (primiparity, multiparity) and country (Denmark, after parturition. Cancer Prev. Res. 8, 1000–1009 (2015).
Norway). All models were compared by the deviance (i.e., the difference in 21. Choudhury, S. et al. Molecular profiling of human mammary gland links
−2∙loglikelihood between two models). breast cancer risk to a p27(+) cell population with progenitor characteristics.
Supplementary Figure 6 shows the deviance between Mfig2C and the week- Cell Stem Cell 13, 117–130 (2013).
specific MThreshold(w0) models for different threshold values (in gestational weeks), 22. Sinha, D. K., Pazik, J. E. & Dao, T. L. Prevention of mammary carcinogenesis
w0, when using the simple week-specific threshold model (Supplementary Fig. 6A), in rats by pregnancy: effect of full-term and interrupted pregnancy. Br. J.
when allowing for difference in effect according to parity (Supplementary Fig. 6B) Cancer 57, 390–394 (1988).
and when further allowing for difference in effect according to both parity and 23. Wohlfahrt, J. & Melbye, M. Gender of offspring and long-term maternal
country (Supplementary Fig. 6C). The best fit were in all three situations found breast cancer risk. Br. J. Cancer 82, 1070–1072 (2000).
using a threshold value of 34 weeks. 24. Wohlfahrt, J. & Melbye, M. Maternal risk of breast cancer and birth
characteristics of offspring by time since birth. Epidemiology 10, 441–444
(1999).
Data availability 25. Collaborative Group on Hormonal Factors in Breast Cancer. Breast cancer
The data that support the findings of this study are archived at governmental institutions and breastfeeding: collaborative reanalysis of individual data from 47
in Denmark and Norway, and can be obtained through application to the relevant data epidemiological studies in 30 countries, including 50 302 women with breast
agencies. In Denmark, data from the Medical Birth Registry and the Danish Cancer cancer and 96 973 women without the disease. Lancet 360, 187–195 (2002).
Registry were retrieved from the Health Data Agency (accession No. FSEID-00002894), 26. Vestermark, V., Hogdall, C. K., Plenov, G., Birch, M. & Toftager-Larsen, K.
while information on income, educational attainment, employment status, and dis- The duration of breast-feeding. A longitudinal prospective study in Denmark.
posable household income was retrieved from Statistics Denmark (accession No. Scand. J. Public Health 19, 105–109 (1991).
706117). In Norway, data from the Medical Birth Registry of Norway was retrieved from 27. Maastrup, R. et al. Breastfeeding progression in preterm infants is influenced
the Norwegian Institute of Public Health (accession No. 06/930-235) and breast cancer by factors in infants, mothers and clinical practice: the results of a National
data was retrieved from the Cancer Registry of Norway (accession No. 02/16-623.1). Cohort Study with high breastfeeding initiation rates. PLoS One 9, e108208
(2014).
Received: 16 May 2018 Accepted: 20 September 2018 28. Hamajima, N. et al. Alcohol, tobacco and breast cancer—collaborative
reanalysis of individual data from 53 epidemiological studies, including 58,515
women with breast cancer and 95,067 women without the disease. Br. J.
Cancer 87, 1234–1245 (2002).
29. Tjønneland, A. et al. Alcohol intake and breast cancer risk: the European
Prospective Investigation into Cancer and Nutrition (EPIC). Cancer Causes
Control 18, 361–373 (2007).
References 30. Albertsen, K., Andersen, A.-M. N., Olsen, J. & Grønbæk, M. Alcohol
1. Fitzmaurice, C. et al. The Global Burden of Cancer 2013. JAMA Oncol. 1,
consumption during pregnancy and the risk of preterm delivery. Am. J.
505–527 (2015).
Epidemiol. 159, 155–161 (2004).

6 NATURE COMMUNICATIONS | (2018)9:4255 | DOI: 10.1038/s41467-018-06748-3 | www.nature.com/naturecommunications


NATURE COMMUNICATIONS | DOI: 10.1038/s41467-018-06748-3 ARTICLE

31. Nykjaer, C. et al. Maternal alcohol intake prior to and during pregnancy and the study design, planned statistical analysis, oversaw the conduct of the statistical
risk of adverse birth outcomes: evidence from a British cohort. J. Epidemiol. analysis, interpreted the study results, and revised the manuscript. N.Ø. contributed
Community Health 68, 542–549 (2014). to classification of register data, contributed to the study design, interpreted the study
32. Popova, S., Lange, S., Probst, C., Gmel, G. & Rehm, J. Estimation of national, results, and revised the manuscript. M.M. conceived the study, contributed to the
regional, and global prevalence of alcohol use during pregnancy and fetal study design, interpreted the study results, and revised the manuscript. All authors
alcohol syndrome: a systematic review and meta-analysis. Lancet Glob. Health had access to all of the data and take full responsibility for the integrity of the data,
5, e290–e299 (2017). the accuracy of the data analysis, the finished article and the decision to submit the
33. Wilsnack, R. W., Wilsnack, S. C., Kristjanson, A. F., Vogeltanz-Holm, N. D. & article.
Gmel, G. Gender and alcohol consumption: patterns from the multinational
GENACIS project. Addiction 104, 1487–1500 (2009). Additional information
34. Alvik, A., Heyerdahl, S., Haldorsen, T. & Lindemann, R. Alcohol use before Supplementary Information accompanies this paper at https://doi.org/10.1038/s41467-
and during pregnancy: a population-based study. Acta Obstet. Gynecol. Scand. 018-06748-3.
85, 1292–1298 (2006).
35. Storm, H. H., Michelsen, E. V., Clemmensen, I. H. & Pihl, J. The Danish Competing interests: The authors declare no competing interests.
Cancer Registry—history, content, quality and use. Dan. Med. Bull. 44,
535–539 (1997). Reprints and permission information is available online at http://npg.nature.com/
36. Danø, H. et al. Fertility pattern does not explain social gradient in breast reprintsandpermissions/
cancer in denmark. Int. J. Cancer 111, 451–456 (2004).
37. Irgens, L. M. The Medical Birth Registry of Norway. Epidemiological research Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in
and surveillance throughout 30 years. Acta Obstet. Gynecol. Scand. 79, published maps and institutional affiliations.
435–439 (2000).
38. Larsen, I. K. et al. Data quality at the Cancer Registry of Norway: an overview
of comparability, completeness, validity and timeliness. Eur. J. Cancer 45,
1218–1231 (2009). Open Access This article is licensed under a Creative Commons
Attribution 4.0 International License, which permits use, sharing,
adaptation, distribution and reproduction in any medium or format, as long as you give
Acknowledgments appropriate credit to the original author(s) and the source, provide a link to the Creative
The study was supported by The Health Foundation (Helsefonden), A.P. Møller og Commons license, and indicate if changes were made. The images or other third party
Hustru Chastine Mc-Kinney Møllers Fond til almene Formaal, The Danish Cancer material in this article are included in the article’s Creative Commons license, unless
Society, The Danish Medical Research Council, and the “Små Forsk” Start grant from indicated otherwise in a credit line to the material. If material is not included in the
Research Council Norway and University of Bergen, Norway. The funders had no role in article’s Creative Commons license and your intended use is not permitted by statutory
study design, data collection, data analysis, interpretation of results, writing of the report, regulation or exceeds the permitted use, you will need to obtain permission directly from
and in the decision to submit the article for publication. the copyright holder. To view a copy of this license, visit http://creativecommons.org/
licenses/by/4.0/.
Author contributions
A.H. classified register data, performed statistical analysis, contributed to the study © The Author(s) 2018
design, interpreted the study results, and drafted the manuscript. J.W. contributed to

NATURE COMMUNICATIONS | (2018)9:4255 | DOI: 10.1038/s41467-018-06748-3 | www.nature.com/naturecommunications 7


Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2019) 5:13
https://doi.org/10.1186/s40794-019-0088-6

RESEARCH Open Access

Determinant factors of anaemia among


pregnant women attending antenatal care
clinic in Northwest Ethiopia
Tadesse Hailu1*, Simachew Kassa2, Bayeh Abera1, Wondemagegn Mulu1 and Ashenafi Genanew3

Abstract
Background: Anaemia is a low blood haemoglobin concentration and has been shown to be a public health
problem affecting both developing and developed countries. Pregnant women are the most vulnerable groups to
anaemia due to several factors, including parasitic infection and feeding habits during their pregnancy. The aim of
this study was to assess the prevalence and determinant factors of anemia in pregnant women in Northwest
Ethiopia.
Methods: A cross-sectional study was conducted among pregnant women from February, 2017 to June, 2017. The
data on determinant factors were collected using a structured questionnaire. The hemoglobin level and intestinal
parasites were determined using Hemocue HB 201 and formol ether concentration techniques, respectively. Data
was entered and analyzed using SPSS version 23 statistical software. Bivariate and multivariate regressions were
computed and odds ratio was determined at 95% confidence interval.
Results: The study consists of 743 participants with a median age of 25 years were included. The prevalence of
anemia among pregnant women was 79 (10.6%). The prevalence of mild, moderate and severe anaemia were 78
(99.8%), 1 (0.1%) and 1 (0.1%), respectively. Pregnant women of rural dwellers (AOR = 3.72, CI =1.51–9.18), farmer in
occupation (AOR = 3.51, CI = 1.75–7.01), and not educated (AOR = 2.25, CI = 1.13–4.48) were significantly associated
with increased risk of anemia.
Conclusion: Anaemia is still a problem amongst pregnant women in the study area though much has been done
to increase the hemoglobin level during pregnancy. Health education should be given on factors that aggravate
anaemia during pregnancy.
Keywords: Amaemia, Pregnancy, West Gojjam, Parasitic infection

Introduction Generally, pregnant women with Hgb level < 11 g/dl are
Anaemia is a condition of lower red blood cells and considered to be anaemic [1].
haemoglobin (Hgb) level than normal [1]. The preva- Several factors might contribute to the causes of
lence of anemia among pregnant women is estimated to anemia among pregnant women. For instance, geo-
be 38% worldwide, 36.9% in Africa and 23% in Ethiopia helminth infections during pregnancy may be associated
[1, 2]. Anaemia can be classified into three catagories, with maternal anaemia. Hookworm is known to be
mild, moderate and severe. The Hgb level for each class causes of anaemia among pregnant women and hook-
of anaemia during pregnancy are 10.0–10.9 g/dL (mild), worm infection mainly aggravates anemia in pregnant
7–9.9 g/dL (moderate) and < 7 g/dL (severe) [2]. women [3]. Infections by geo-helminthes lead to malnu-
trition, iron deficiency anaemia, and increased vulner-
ability to other infections in infected pregnant women
[4]. The complication may not end up with the maternal
* Correspondence: tadessehailu2005@yahoo.com; tadessehailu89@gmail.com
1
Department of Medical Laboratory Science, College of Medicine and Health
anaemia but also causes a complication on the child in-
Sciences, Bahir Dar University, P.O. Box: 79, Bahir Dar City, Ethiopia cluding; low pregnancy weight gain and intrauterine
Full list of author information is available at the end of the article

© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2019) 5:13 Page 2 of 7

growth retardation, followed by low birth weight and For Hgb the cutoff criterion levels below which indicat-
higher perinatal mortality rates [5]. ing aneamia is the WHO cut-off of > 110 g/L for non
Pregnant woman that live in rural areas [6], lack of raw anemic, 100-109 g/L for mild anemic, 70–90 g/dL mod-
vegetables in their diet [7], illnesses [6] and low levels of erate and < 70 g/dL for severe anemic for pregnant
education [8] are also major determinants of anemia. women [2].
Malnutrition is also one of the major causes of an-
aemia among pregnant women in Ethiopia [9]. Working Intestinal parasites investigation
to improve the nutritional status of pregnant women Freshly passed stool specimens were collected using a
through supplementation of vitamin A, iron, and iodine clean plastic cup at the health institutions. The stool
is important to minimize the risk of anemia [10]. cups were labeled with their card number. Laboratory
A lot has been done to minimize the risk of anaemia, professionals took part in all processes of stool collection
but the complication of anaemia is still a problem and examination. The stool samples were processed for
amongst pregnant women especially in a rural set up. microscopic examination using Formol Ether Concen-
The true prevalence and the determinant factors of an- tration Technique (FECT). The stool examination was
aemia were not well addressed in the study area. There- done in the health institutions laboratory. In FECT, stool
fore, the present study tried to address the stated sample (0.5 g) was transferred into 10 mL of normal sa-
information gaps so as to give evidence based action. line in a glass container and mix thoroughly. Two layers
of gauze were placed in a funnel and strained the con-
Methods tents into a 15 mL centrifuge tube. Then, 2.5 mL of 10%
Study design, period and area formaldehyde and 1 mL of ether were added to a test
A cross sectional study was conducted from February, tube. The test tubes were mixed well and centrifuged at
2017 to June, 2017 among pregnant women in West 1000 rpm for three minutes. The supernatant was re-
Gojjam Zone, Northwest Ethiopia. The average elevation moved and the sediment was mixed well, prepared on
of the zone is 2,300 m. The annual temperature of the two slides one for saline and the other for iodine, and
study area ranges between 16.68 to 37.6 °C. covered with a cover slide and sow under microscope.
All pregnant women attending antenatal clinic for the
first time during the study period were included in the Data quality assurance
study. Pregnant women undertaking anthelmintic drugs To ensure reliable data collection, training on data col-
during the data collection time were excluded from the lection, laboratory examination and explanation about
study. Purposive sampling technique was used to include the study was given before sample collection for midwif-
743 study subjects. The samples were collected in five ery and laboratory personnel. Filled questionnaires were
woredas as of West Gojjam Zone including: Mecha, collected after checking for their consistency and com-
Debub Achefer, Bure, Jabi-tihinana and Finot-selam by pleteness. Application of standard procedures during
considering urban and rural settings. One health center data collection process and accuracy of test results was
was selected in each Woreda based on their laboratory supervised by the principal investigator. Specimens were
facilities. The sample size in each health institution was cross checked by principal investigators to increase the ac-
150 which was proportionally allocated by considering curacy of laboratory results. The direct stool microscopy
the population in the catchment areas. was examined earlier to FECT as soon as the sample ar-
rives. To eliminate observer bias, stool slides were exam-
Data collection ined independently with two experienced laboratory
Questionnaires professionals and 10% of the FECT slides were randomly
A structured questionnaire was used to obtain socio- selected and read by other laboratory professionals as a
demographic information and determinant factors by quality control.
interviewing pregnant women. The questionnaire was
filled by midwifery health professionals. Data analysis
Data was entered and analyzed using SPSS version 23
Haemoglobin determination statistical software. The overall magnitude of geo-
The blood samples were collected from a finger prick by helminthic infection was calculated using descriptive
blood lancet. Haemoglobin (Hgb) value was determined statistics of the sample through frequencies and cross
using a portable Hgb spectrophotometer, Hemocue Hb tabulations. Strength of association between geo-
201 analyzer (HemoCue, Angelholm, Sweden) and spe- helminthic and determinant factors was calculated by
cially designed microcuvette (the Hemocue Hb 201 bivariate analysis. The association was analyzed by
Microcuvette, Hemocue, Angelholm, Sweden). Then, the multivariate logistic regression to avoid confounding ef-
Hgb value was then used to assess the status of anaemia. fect and calculating the odds ratios (OR) with 95%
Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2019) 5:13 Page 3 of 7

confidence intervals (CI). In all statistical tests, the dif- 9.4, 0.4 and 0.1%, respectively. Mild anaemia had high
ferences were considered to be statistically significant if prevalence 77 (97.5%) among anaemic pregnant women
p-value less than 0.05. (Table 2).

Ethical consideration
The proposal was ethically approved by an institutional Prevalence of intestinal parasitosis
review board of Bahir Dar University, College of Medi- The overall prevalence of intestinal parasitosis among
cine and Health Science. A written informed consent pregnant women was 276 (37.1%). Hookworm has the
was obtained from every study participant. Participants highest prevalence 138 (50%) among the parasitic in-
tested positive for any parasitic infections got appropri- fected pregnant women followed by E. histolytica 113
ate treatment accordingly from the responsible body. (40.9%) and G. lamblia 53 (19.2%) (Table 2). The
prevalence of anaemia among hookworm, E.histoly-
Results tica/dipar and G. lamblia infected pregnant women
Sociodemographic characteristics of the study subjects were 39 (28.3%), 28 (24.8%) and 23 (43.4%), respect-
A total of 743 pregnant women took part in this study ively (Table 2).
with a median age of 25 years. The majority (96.2%) of
study participants was in the age range 15–35 years.
Pregnant women who were rural dwellers and farmers Obstetrics and medical condition of study participants
in their occupation accounted 61.2%) and 21.5%, re- There were 509 (68.5%) multi gravid and 420 (56.5%)
spectively (Table 1). second trimester pregnancy study participants. The
prevalence of anaemia among Multi gravid, one parity
Prevalence of anaemia and third trimester were 57 (11.2%), 21 (13.2%) and 31
The mean Hgb concentration was 12.8 ± 2.97 g/dL with (13.4%), respectively. The prevalence of anaemia was
a range of 6 to 17.9 g/dL. The total prevalence of an- 77.8 and 18.1% among pregnant women who had a pre-
aemia among pregnant women was 79 (10.6%). The vious malaria attack and history of intestinal parasitic in-
prevalence of mild, moderate and severe anaemia was fection, respectively (Table 3).
Table 1 Socio demographic characteristics of pregnant women who attended ANC services in West Gojjam Zone, Northwest
Ethiopia
Variables Total Hgb > 11 g/dL Hgb < 11 g/dL X2, p- value
[N,%] [N,%]
Age in years 15–35 715 [96.2] 646 [90.3] 69 [9.7] 19.20, 0.001
36–45 28 [3.8] 18 [64.3] 10 [35.7]
Religion Christian 736 [99] 657 [89.3] 79 [10.7] NA
Muslim 7 [1] 7 [100] 0
Residence Rural 455 [61.2] 383 [88.4] 72 [11.6] 7.73, 0.001
Urban 288 [38.8] 281[97.6] 7 [2.4]
Woreda of Fenote Selam 150 [20.2] 108 [72] 42 [28] 64.91, 0.001
West Gojam
Jabitihenane 151 [20.3] 143 [94.7] 8 [5.3]
Bure 142 [19.1] 133 [93.7] 9 [6.3]
Debub Achefer 150 [20.2] 134 [89.3] 16 [10.7]
Mecha 150 [20.2] 146 [97.3 4 [2.7]
Occupation Farmer 160 [21.5] 130 [81.3] 30 [18.7] 14.10, 0.001
Non-Farmer 583 [91.6] 534 [71.9] 49 [8.4]
Education Illiterate 372 [50.1] 308 [82.8] 64 [17.2] 17.79, 0.04
Read & Write 205 [27.6] 203 [99] 2 [1]
Primary 88 [11.4] 82 [97.6] 6 [2.4]
Junior 9 [1.2] 8 [88.9] 1 [11.1]
Secondary 80 [10.8] 75 [93.6] 5 [6.4]
> complete 20 [2.7] 19 [95] 1 [5]
Total 743 [100] 664 [89.4] 79 [10.6]
Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2019) 5:13 Page 4 of 7

Table 2 The level of anaemia and intestinal parasitic infection among pregnant women in West Gojjam, Northwest Ethiopia
Types of IP Level of anaemia
Total Non-anaemic [N,%] Mild Moderate Severe Total anaemia
[N,%] [N,%] [N,%] [N,%] [N,%]
Hookworm Pos 138 [18.6] 99 [71.7] 39 [28.3] 0 0 39 [5.2]
Neg 605 [81.4] 565 [93.4] 38 [6.2] 1 [0.2] 1 [0.2] 40 [5.4]
G. lamblia Pos 53 [7.1] 30 [56.6] 23 [43.4] 0 0 23 [3.1]
Neg 690 [93.2] 634 [91.8] 54 [7.8] 1[0.2] 1 [0.2] 56 [7.5]
E. histolytica Pos 113 [15.2] 85 [75.2] 26 [23] 1 [0.9] 1 [0.9] 28 [3.8]
Neg 630 [84.8] 579 [91.9] 51 [8.1] 0 0 51 [6.8]
All Parasite Pos 278 [37.4] 222 [79.9] 55 [19.8] 1 [0.3] 0 56 [7.5]
Neg 465 [62.6] 442 [95.1] 20 [4.3] 2 [0.4] 1 [0.2] 23 [3.1]
Total 743 [100] 743 [100] 664 [89.4] 75 [10.1] 3 [0.4] 1 [0.1]
Pos Positive; Neg Negative

Determinant factors for anaemia in pregnancy Pregnant women were 2.25 times more likely become
Pregnant women in rural areas were 3.72 times more anaemic than not the illiterate once (AOR = 2.25
likely to be anaemic than urban dwellers (AOR = 3.72 [95%CI:1.13–4.48]). Those pregnant women infected
[95%CI:1.51–9.18]). Likewise, farmer pregnant women with hookworm parasites were 3.81 times more likely to
were 3.51 times more likely to be anaemic with non- develop anaemia than pregnant women who were not
farmer ones (AOR = 3.51 [95%CI:1.75–7.01]). In the infected with hookworm parasites (AOR = 3.81 [95%CI,
same way, non previously medically ill pregnant women 2.06–7.06]) (Table 4).
were 85% less likely to be anaemic than previously med-
ically ill ones (AOR = 0.15[95%CI:0.08–0.28]. Pregnant Discussion
women who did not eat raw vegetables were 8.94 times Anaemia is an important complication during preg-
more likely to become anemic than pregnant women nancy, especially in a rural set up. The impacts of an-
who ate raw vegetables (AOR = 8.94 [95%C:2.86–10.55]). aemia rest upon not only on the health of pregnant
Pregnant women who didn’t eat meat were 11.49 times women, but also on her offspring. In the present study,
more likely to be anaemic than those who ate meat the overall magnitude of anaemia among pregnant
(AOR = 11.49 [95% CI:2.51–12.53]) (Table 4). Illiterate women was 10.6%. This result was comparable with

Table 3 Obstetrical & Medical characteristics of pregnant women who attended ANC service in West Gojjam Zone, Northwest
Ethiopia
Variables Frequency [N,%] Hgb > 11 g/dL[N,%] Hgb < 11 g/dL [N,%] X2, p-value
Gravidity Primigravida 234 [31.5] 212 [90.6] 22 [9.4] 0.55, 0.52
Multi gravid 509 [68.5] 457 [88.8] 57 [11.2]
Parity No 241 [32.4] 218 [90.5] 23 [9.5] 1.48, 0.69
1 159 [21.4] 138 [86.8] 21 [13.2]
2–3 224 [30.2] 201 [89.7] 23 [10.3]
>4 119 [16] 107 [89.9] 12 [10.1]
Trimester First 142 [19] 135 [95.1] 7 [4.9] 7.22, 0.30
Second 326 [44] 285 [87.4] 41 [12.6]
Third 275 [37] 244 [88.7] 31 [11.3]
History of malaria infection Yes 9 [1.2] 2 [22.2] 7 [77.8] 43.22, 0.00
No 734 [98.8] 662 [90.2] 72 [9.8]
History intestinal parasite infection Yes 276 [37.1] 226 [18.9] 50 [18.1] 25.88, 0.00
No 467 [62.9] 428 [93.8] 29 [6.2]
History of previous illness Yes 115 [15.5] 72 [62.6] 43 [37.4] 24.14, 0.00
No 628 [84.5] 592 [94.3] 36 [5.7]
Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2019) 5:13 Page 5 of 7

Table 4 Multivariate analysis showing the Determinant factors of anaemia among pregnant women in West Gojjam zone, 2017
Variables Anemia present COR[95%CI] AOR[95%CI] P value
Yes (N) No (N)
Address Rural 72 383 7.55[3.42–.16.65] 3.72[1.51–9.18] 0.004
Urban 7 281 1 1
Occupation Farmer 30 130 2.52[1.54–4.12] 3.51[1.75–7.01] 0.001
Non Farmer 49 534 1 1
Eating raw vegetables No 75 490 6.66[2.40–18.47] 8.94[2.86–10.53] 0.001
Yes 4 174 1 1
Age 15–35 69 646 1
36–45 10 18 5.20[2.31–11.71 4.46[1.57–12.69] 0.005
Eating meat No 76 568 4.28[1.32–13.88] 11.49[2.51–12.53] 0.002
Yes 3 96 1
Previous illness Yes 43 72 9.82[5.92–16.29] 0.15[0.08–0.28] 0.001
No 36 592 1 1
Educational status Illiterate 64 308 4.93[2.75–8.83] 2.25[1.13–4.48] 0.02
Not illiterate 15 356 1 1
Hookworm infection Yes 41 97 6.31[3.86–10.31] 3.81[2.06–7.06] 0.001
No 38 567 1 1

previous studies done in Amhara Regional State study, the level of Hgb is varied by gravidity, parity and
(15.89%) [11], Gondar city (16.6%) [12] and Iran (13.1%) trimesters. This result was similar with different findings
[13]. The current prevalence was also considerably lower conducted previously in Southern Ethiopia [16], South-
than previous reports from Jimma, Southern Ethiopia east Ethiopia [22], Ghana [25] and Iran [28].
(38.2%) [14], Tigray (36.1%) [15], Southern Ethiopia In the current study, pregnant women living in
(23.2%) [16], Jordan (34.7%) [17], Vietnam (43.2%) [18] , rural areas were 3.72 times more likely to be an-
and Southeastern Nigeria (76.9%) [19]. The possible ex- aemic as compared to those living in urban areas.
planation for the difference might be geographical vari- Similar results were reported by studies conducted
ation of factors across different areas. The lower in Gondar [12], and southwest Ethiopia [22]. The
prevalence in the present study could be attributed to possible reason might be due to low socioeconomic
gradual improvement of lifestyle and living standards status, lack of adequate information about nutrition
and health seeking behavior by the effort of government during pregnancy and accessibility to health care fa-
to achieve the sustainable development goal aimed to re- cilities and illiteracy.
duce the maternal mortality. Lack of awareness about anaemia and its impact dur-
In the present study, most of the anaemic pregnant ing pregnancy may be a major factor becoming anaemic
women had mild anaemia. This finding was comparable of pregnant women. In the present study, farmer preg-
with a result obtained previously in Northwest Ethiopia nant women were 3.51 times more likely to be anaemic
[20, 21], Southeast Ethiopia [22] and Pakistan [23], but dif- with that of non farmer pregnant women. A similar re-
ferent from other reports [24]. The difference may be due sult was obtained in a study done in India [29]. Pregnant
to a regular supply of iron and folic acid supplimentation women who did not get formal education were 2.25
and anti-helminthic drugs in the present study. times more likely for anaemic than from those who got
Parasitic infection has a devastating effect on the level of formal education. Similar findings were reported in India
Hgb and causes anaemia since they affect iron absorption [19] and China [30].
by the intestine and consumes the red blood cells [25]. In Pregnant women who did not eat raw vegetables were
the present study, pregnant women who had previous med- 8.94 times more likely to have anemia compared to
ical illness, malaria infection and intestinal parasitic infec- pregnant women who eat raw vegetables. This finding is
tion were more likely to become anaemic. This was consistent with different parts of Ethiopia [20, 31, 32].
consistent with previously conducted in Southern Ethiopia The possible reason might be due to poor dietary diver-
[16], Ghana [25], Nigeria [26], and Venezuela [27]. sity which leads to a deficiency of minerals and vitamins
The level of Hgb may be varied during the course of which may increase bio-availability of iron. Pregnancy is
pregnancy by several obstetric factors. In the present the most nutritionally demanding period in a woman’s
Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2019) 5:13 Page 6 of 7

life. Consequently, pregnant women are advised to eat a Ethics approval and consent to participate
more diversified diet than usual. To conduct this research, the research proposal was ethically approved by
the research and ethical review committee of Bahir Dar University, College of
Pregnant women who didn’t eat meat were 11.49 times Medicine and Health Sciences.
more likely to be anaemic than those who eat meat. This
finding was consistent with other studies in which preg- Consent for publication
Not applicable.
nant women conducted in Ethiopia who ate red meat
[31, 32] and Pakistan [23]. The increased concentration Competing interests
of Hgb is with the fact that red meat is an important The authors declare that they have no competing interests.
source of heme iron [33] which is a major component of
Author details
red blood cells. 1
Department of Medical Laboratory Science, College of Medicine and Health
Soil transmitted helminths like hookworm infection Sciences, Bahir Dar University, P.O. Box: 79, Bahir Dar City, Ethiopia.
2
causes anaemia during pregnancy. In the current study, Department of Midwifery, College of Medicine and Health Sciences, Bahir
Dar University, P.O. Box: 79, Bahir Dar City, Ethiopia. 3Department of
pregnant women infected with hookworm parasites were Pharmacy, College of Medicine and Health Sciences, Bahir Dar University, P.O.
3.81 times more anaemic than non hookworm infected Box: 79, Bahir Dar City, Ethiopia.
pregnant women. This finding was consistent with previ-
Received: 13 March 2019 Accepted: 1 July 2019
ous studies conducted among pregnant women in East
Wollega, Oromia, Ethiopia [34] and Northwest Ethiopia
[35]. This study did not include all health institutions References
due to the absence of full antenatal care service includ- 1. De Maeyer EM, Dallman P, Gurney JM, Hallberg L, Sood SK, Srikantia SG.
Preventing and controlling iron deficiency anemia through primary health
ing detection of intestinal parasitosis and determination care, a guide for health administrators and programme managers; 1989.
of the Hgb level. 2. Hemoglobin concentration for the diagnosis of anemia and assessment of
severity, https://www.who.int/vmnis/indicators/haemoglobin.pdf: World
Health Organization; 2011.
3. Stephenson LS, Latham MC, Ottesen EA. Malnutrition and parasitic helminth
Conclusion infections. Parasitology. 2000;121:23–38.
Anaemia is one of the major complications during preg- 4. Obiamuiwe BA, Nmorsi P. Human gastro-intestinal parasites in Bendel State,
nancy. Most pregnant women had mild anaemia in the Nigeria. Nig J Parasitol. 1990;32:177–83.
5. Khor GL. Update on the prevalence of malnutrition among children in
present study. Factors related to obstetric conditions,
NMCJ, vol. 5; 2003. p. 113–22.
nutrition, parasitic infection were the main risk factors. 6. Okafor IM, Okpokam DC, Antai AB, Usanga EA. Iron Status of Pregnant
Therefore, awareness should be built among pregnant Women in Rural and Urban Communities of Cross River State, South-South
Nigeria. Nig J Physiol Sci. 2017;31:121–5.
women targeting on their feeding habits, parasitic infec-
7. Diamond-Smith NG, Gupta M, Kaur M, Kumar R. Determinants of Persistent
tion and hygienic conditions to minimize the outcomes Anemia in Poor, Urban Pregnant Women of Chandigarh City, North India: A
of anaemia during pregnancy. Mixed Method Approach. Food Nutr Bull. 2016;37:132–43.
8. Taner CE, Ekin A, Solmaz U, Gezer C, Çetin B, Keleşoğlu M, Merve Bayrak
Erpala MB, Özeren M. Prevalence and risk factors of anemia among
Abbreviations pregnant women attending a high-volume tertiary care center for delivery.
FECT: Formol Ether Concentration Technique; Hgb: Haemoglobin J Turk Ger Gynecol Assoc. 2015;16:231–6.
9. Berhane Y, Gossaye Y, Emmelin M, Hogberg H. Women's Health in Rural
Setting in Societal Transition in Ethiopia. Soc Sci Med. 2001;53:1525–39.
Acknowledgements 10. Jennings J, Hirbaye MB. Review of Incorporation of Essential Nutrition
We should like to thank the Amhara Regional Health Bureau and West Actions into Public Health Programs in Ethiopia, the food and nutrition
Gojjam health office for their invaluable collaboration and support in the technical assistance project, 2008. https://www.fantaproject.org/.../FANTA-
undertaking of this study. We are most grateful to thank the head of health Review-Incorporation-ENA-Ja.
institutions in facilitating the pregnant women participation. 11. Kassa GM, Muche AA, Berhe AK, Fekadu GA. Prevalence and determinants of
anemia among pregnant women in Ethiopia; a systematic review and
meta-analysis. BMC Hematolology. 2017;17:17.
Authors’ contributions
12. Alem M, Enawgaw B, Gelaw A, Kena T, Seid M, Olkeba Y. Prevalence of
TH carried out developing the proposal, data entry, analysis, writes up, and
anemia and associated risk factors among pregnant women attending
editing the manuscript. SK participated in developing, reviewing and editing
antenatal care in Azezo Health Center Gondar town, Northwest Ethiopia.
the proposal and data analysis and editing of the manuscript. BA involved in
Interdiscipl Histopathol. 2013;1:137–44.
evaluating the proposal, and critically reviewing and editing the manuscript.
13. Barooti E, Rezazadehkermani M, Sadeghirad B, Motaghipisheh S, Tayeri S,
WM involved in critically reviewing and evaluating the proposal and
Arabi M, Salahi S, Haghdoost A. Prevalence of Iron Deficiency Anemia
reviewing and editing the manuscript. AG involved in reviewing, editing the
among Iranian Pregnant Women; a Systematic Review and Meta-analysis. J
proposal and the manuscript. All authors read and approved the final
Reprod Infertil. 2010;11:17–24.
manuscript.
14. Belachew T, Legesse Y. Risk factors for anemia among pregnant women
attending antenatal clinic at Jimma University Hospital, southwest Ethiopia.
Funding Ethiop Med J. 2006;44:211–20.
The research project was funded by Bahir Dar University. 15. Gebre A, Mulugeta A. Prevalence of Anemia and Associated Factors among
Pregnant Women in North Western Zone of Tigray, Northern Ethiopia: A
Cross-Sectional Study. J Nut Metab 2015;2015:7.
Availability of data and materials 16. Lebso M, Anato A, Loha E. Prevalence of anemia and associated factors
To generate findings of this particular study, data was collected and among pregnant women in Southern Ethiopia: A community based cross-
analyzed. sectional study. PLoS ONE. 2017;12:e0188783.
Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2019) 5:13 Page 7 of 7

17. Al-Mehaisen L, Khader Y, Al-Kuran O, Abu Issa F, Amarin Z. Maternal anemia


in rural Jordan: room for improvement. Anemia. 2011;2011:7.
18. Uneke CJ, Duhlinska DD, Igbinedion EB. Prevalence and public-health
significance of HIV infection and anaemia among pregnant women
attending antenatal clinics in southeastern Nigeria. J Health Popul Nutr.
2007;25:328–35.
19. Levy A, Fraser D, Katz M, Mazor M, Sheiner E. Maternal anemia during
pregnancy is an independent risk factor for low birth weight and preterm
delivery. Eur J Obstet Gynecol Reprod Biol. 2005;122:182–6.
20. Derso T, Abera Z, Tariku A. Magnitude and associated factors of anemia
among pregnant women in Dera District: a cross-sectional study in
northwest Ethiopia. BMC Res Notes. 2017;10:359.
21. Melku M, Addis Z, Alem M, Enawgaw B. Prevalence and Predictors of
Maternal Anemia during Pregnancy in Gondar, Northwest Ethiopia: An
Institutional Based Cross-Sectional Study. Anemia. 2014;2014:108593.
22. Kefiyalew F, Zemene E, Asres Y, Gedefaw L. Anemia among pregnant
women in Southeast Ethiopia: prevalence, severity and associated risk
factors. BMC Res Notes. 2014;7:771.
23. Baig-Ansari N, Badruddin SH, Karmaliani R, Harris H, Jehan I, Pasha O, Moss N,
McClure EM, Goldenberg RL. Anemia prevalence and risk factors in pregnant
women in an urban area of Pakistan. Food Nutr Bull. 2008;29:132–9.
24. Gedefaw L, Ayele A, Asres Y, Mossie A. Anemia and Associated Factors
Among Pregnant Women Attending Antenatal Care Clinic in Wolayita Sodo
Town, Southern Ethiopia. Ethiop J Health Sci. 2015;25:155–62.
25. Tay KSC, Nani EA, Walana W. Parasitic infections and maternal anaemia
among expectant mothers in the Dangme East District of Ghana. BMC Res
Notes. 2017;10:3.
26. Akinbo FO, Olowookere TA, Okaka CE, Oriakhi MO. Co-infection of malaria
and intestinal parasites among pregnant women in Edo State, Nigeria. J
Med Trop. 2017;19:43–8.
27. Rodríguez-Morales AJ, Barbella AR, Case C, Melissa Arria M, Ravelo M, Perez
H, Oscar U, Gervasio G, Rubio N, Maldonado A, Aguilera Y, Viloria A, Blanco
JJ, Colina M, Hernández E, Araujo E, Cabaniel G, Benitez J, Rifakis P. Intestinal
Parasitic Infections among Pregnant Women in Venezuela. Infect Dis Obstet
Gynecol 2006;2006:23125.
28. Mirzaie F, Eftekhari N, Goldozeian S, Mahdavinia J. Prevalence of anemia risk
factors in pregnant women in Kerman, Iran. Iran J Reprod Med. 2010;8:66–9.
29. Singh V, Rai D, Thakur S, Singh VN. Study of iron deficiency anaemia in farm
women of lucknow district in Uttar Pradesh, India. Plant Archives. 2017;17:
125–8.
30. Ma AG, Schouten E, Wang Y, Li Y, Sun YY, Wang QZ. Anemia prevalence
among pregnant women and birth weight in five areas in China. Med Princ
Pract. 2009;18:368–72.
31. Gebremedhin S, Enquselassie F. Correlates of anemia among women of
reproductive age in Ethiopia: evidence from Ethiopian DHS. Ethiop J Health
Dev. 2005;25:22–30.
32. Alene KA, Dohe AM. Prevalence of Anemia and Associated Factors among
Pregnant Women in an Urban Area of Eastern Ethiopia. Anemia. 2014;2014:7.
33. Obse N, Mossie A, Fau-Gobena T, Gobena T. Magnitude of anemia and
associated risk factors among pregnant women attending antenatal care in
Shalla Woreda, West Arsi Zone, Oromia Region, Ethiopia. Ethiop J Health Sci.
2013;23:165–73.
34. Mengist HM, Zewdie O, Belew A. Intestinal helminthic infection and anemia
among pregnant women attending ante-natal care (ANC) in East Wollega,
Oromia. Ethiopia. BMC Res Notes. 2017;10:440.
35. Kumera G, Haile K, Abebe N, Marie T, Eshete T. Anemia and its association
with coffee consumption and hookworm infection among pregnant
women attending antenatal care at Debre Markos Referral Hospital,
Northwest Ethiopia. PLoS One. 2018;13(11):e0206880.

Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.

Anda mungkin juga menyukai