Anda di halaman 1dari 29

Dokter Muda THT-KL Periode Juni 2020

Fakultas Kedokteran Universitas Andalas

Journal Reading

Vertigo and dizziness in adolescents: Risk factors


and their population attributable risk

Oleh:
Hengki Prasetia 1840312468
Zahra Indria Zenti 1840312705
Muhammad Reno Akhyar Marpaung 1940312161

Preseptor:
Dr. Ade Asyari, Sp.THT-KL(K) FICS

BAGIAN TELINGA HIDUNG TENGGOROK BEDAH KEPALA LEHER


FAKULTAS KEDOKTERAN UNIVERSITAS ANDALAS
RSUP DR M. DJAMIL PADANG
2020
Dokter Muda THT-KL Periode Juni 2020 2
Fakultas Kedokteran Universitas Andalas

Vertigo dan Pusing pada Remaja:


Faktor Risiko dan Populasi Berisiko.

ABSTRAK
Tujuan: Untuk menilai faktor risiko yang berkaitan dengan vertigo dan pusing pada remaja
serta untuk mengevaluasi kharakteristik berbagai jenis vertigo. Memahami relevansi faktor
risiko dan populasi remaja yang mengalami vertigo dan pusing guna untuk merancang strategi
pencegahan.
Desain Studi: Populasi sampel terdiri dari anak sekolah usia 12 sampai 19 tahun, yang
diinstruksikan untuk mengisi kuesioner tentang berbagai jenis vertigo dan faktor risiko yang
terkait. Kuesioner secara khsusu menanyakan adanya vertigo, vertigo berputar, vertigo
berayun, pusing ortostatik, dan pusing yang tidak spesifik. Selanjutnya beberapa faktor risiko
yang dibahas antara lain jenis kelamin, stres, nyeri otot sekitar leher dan bahu, durasi tidur,
migrain, asupan kopi dan alkohol, aktivitas fisik, dan kebiaaan merokok.
Hasil: Jenis kelamin, stres, nyeri otot di sekitar leher dan bahu, durasi tidur, dan migraine
dikelompokan sebagai faktor risiko independen, dengan risiko relatif 1,17 untuk jeni kelamin
perempuan; 1,07 untuk stres; 1,24 untuk nyeri otot; dan 1,09 untuk migrain. Populasi risiko
yang dijelaskan oleh faktor risiko ini sekitar 26%, dengan nyeri otot, stres, dan migrain
masing-masing sebesar 11%, 4%, dan 3%.
Kesimpulan: Beberapa faktor risiko pada dewasa juga ditemukan pada remaja. Faktor risiko
yang dapat diterima untuk pencegahan berkisar 17% dari total risiko populasi. Oleh karena
itu, intervensi terhadap faktor risiko ini sangat diperlukan.

PENDAHULUAN dan pusing pada remaja sama seperti pada


Gejala pusing dan vertigo merupakan orang dewasa [8], sepengetahuan penulis
keluhan yang sangat umum, dengan hanya ada data terbatas tentang faktor risiko
prevalensi kasus 30% untuk pusing dan 10% potensial pada remaja dan anak-anak.
untuk vertigo[1]. Beberapa faktor risiko Beberapa penelitian dengan fokus utama
yang mendukung terjadinya vertigo atau pada persepsi kesehatan umum pada remaja
pusing telah diamati secara konsisten pada telah melaporkan bahwa perempuan lebih
populasi dewasa atau lanjut usia. Vertigo sering mengalami pusing dalam 6 bulan
sering dikaitkan dengan migrain [2], jenis terakhir dibandingkan laki-laki [9,10]. Satu
kelamin wanita [3,4] dan gangguan studi lebih lanjut dari 31 anak-anak usia 6
psikologis seperti depresi [5, 6] dan sampai 17 tahun menggambarkan hubungan
kecemasan [7]. Meskipun keluhan vertigo yang signifikan dari vertigo dengan sakit
Dokter Muda THT-KL Periode Juni 2020 3
Fakultas Kedokteran Universitas Andalas

kepala [11]. Salah satu batasan dari studi ini kuesioner dengan lengkap dan dapat
adalah, bahwa mereka tidak membedakan dijadikan sampel untuk dianalisis.
antara tipe vertigo dan / atau jenis pusing. Penelitian ini telah disetujui oleh
Penelitian ini dilakukan pada 1482 siswa Petugas Keamanan Data dan Komite Etika
sekolah tata bahasa (rentang usia: 12 hingga dari Fakultas Kedokteran Universitas Ludwig
19 tahun) bertujuan untuk menggambarkan Maximilians Munich dan Kementerian
faktor-faktor risiko potensial untuk terjadinya Bavaria untuk Pengajaran dan Budaya.
berbagai jenis vertigo dan pusing serta untuk Setiap siswa yang berpartisipasi dan orangtua
memperkirakan risiko populasi pada remaja. atau wali mereka memberikan persetujuan
tertulis dalam pelaksanaan penelitian ini.
METODE
Populasi Penilaian tipe vertigo dan vertigo.
Populasi penelitian untuk studi cross- Prevalensi periode pusing atau vertigo
sectional ini diambil dari studi intervensi dinilai dengan pertanyaan "Apakah Anda
headache MUKIS (Mu’nchner Untersuchung menderita pusing atau vertigo selama 3 bulan
zu Kopfschmerzen bei Gymnasiasten- terakhir?" yang bisa dijawab dengan "ya"
Intervensi-Studie), yang dijelaskan secara atau "tidak". Jika dijawab "ya", siswa
rinci di artikel lain [12]. Untuk studi ini, 12 diminta untuk lebih menentukan jenis
dari 47 sekolah tata bahasa umum di wilayah vertigo: "berputar vertigo seperti di dalam
yang lebih besar di Munich, Jerman, setuju carrousel" (spinning-vertigo), "bergoyang
untuk berpartisipasi. Alasan untuk tidak vertigo seperti di atas perahu kecil" (swaying
berpartisipasi adalah beban pekerjaan vertigo), "perasaan akan kehabisan tenaga
administrasi terkait dan ketidakmampuan ketika cepat berdiri" (pusing ortostatik), atau
untuk mengatur studi di lingkungan sekolah. "tidak satu pun dari ketiga jenis yang
Studi ini dilakukan antara November ditanyakan sebelumnya" (pusing yang tidak
2011 dan Januari 2012. Seorang anggota tim ditentukan).
penulis akan mengunjungi sekolah yang
bersedia, kemudian menginstruksikan siswa Penilaian posisi dan gerakan tubuh yang
untuk mengisi kuesioner. Secara keseluruhan terkait dengan jenis vertigo.
total sampel berjumlah 1.661 siswa yang Posisi tubuh dan gerakan yang terkait
berasal dari kelas 8, 9, dan 10 dan hanya dengan berbagai jenis vertigo dinilai oleh
1.482 siswa (usia rata-rata 14.47 ± 1.08, pertanyaan-pertanyaan berikut, yang dapat
kisaran 12 sampai 19 tahun) yang mengisi dijawab dengan “ya” atau “tidak”: Vertigo
adalah: a) dipicu atau diperburuk oleh
Dokter Muda THT-KL Periode Juni 2020 4
Fakultas Kedokteran Universitas Andalas

gerakan kepala, b) dipicu oleh perubahan atau minuman keras per bulan. Definisi
posisi (misalnya berdiri dari berbaring), c) peminum kopi dan konsumsi alkohol dipilih
juga hadir saat duduk atau berbaring, d) menurut Milde-Busch, et.al.[14], yang
hanya hadir saat berdiri atau berjalan. menemukan hubungan konsumsi kopi dan
alkohol tinggi dengan sakit kepala pada
Penilaian faktor risiko potensial remaja. Aktivitas fisik dinilai dengan
Stres kronis dinilai oleh indeks stres pertanyaan tentang frekuensi aktivitas fisik
global, yang didasarkan pada 12 dari 57 item mingguan di luar jam sekolah. Indeks
yang termasuk dalam TICS (Trier Inventory ekivalen metabolik dari aktivitas yang
of Chronic Stress)[13]. Frekuensi dalam 3 dilaporkan dihitung dan dikategorikan
bulan terakhir untuk masing-masing item ini sebagai tinggi, sedang, atau rendah oleh
ditunjukkan dengan nilai 0 (tidak pernah) tertile spesifik sampel dari distribusi sesuai
hingga 4 (sangat sering). Skor rata-rata dengan prosedur yang disarankan oleh Kujala
individu dari 12 item dihitung dan diubah et al. [15]. Siswa dengan tertile terendah
berdasarkan nilai norma spesifik kelompok diasumsikan tidak aktif secara fisik, dan yang
usia (rata-rata = 50; SD = 10). Untuk nilai-t lain aktif secara fisik. Siswa diberi label
individu, ditentukan apakah nilai berada "merokok" ketika menjawab pertanyaan
dalam kisaran normal distribusi-t, di bawah "Apakah Anda merokok?" dengan "ya".
atau di atas rata-rata. Stres kronis ditetapkan Siswa ditanya tentang durasi tidur mereka
apabila nilai akhir di atas kisaran normal. yang biasa (dalam jam). Durasi rata-rata
Reliabilitas yang baik (Cronbach's alpha dari tidur per hari dihitung dan dibagi menjadi “>
indeks tekanan global: 0,91), validitas 8 jam tidur per hari” dan “8 jam tidur per
konstruk tinggi dan korelasi skala tinggi telah hari”. Dikotomi ini dipilih sesuai dengan
ditemukan [13]. rekomendasi untuk durasi tidur American
Nyeri otot di daerah leher dan bahu Academy of Sleep Medicine [16]. Untuk
dinilai oleh pertanyaan "Apakah Anda penilaian migrain, para siswa ditanya tentang
menderita nyeri otot di daerah kepala, leher menderita sakit kepala dalam 6 bulan
dan bahu?" yang bisa dijawab dengan "ya" terakhir. Ketika menjawab dengan "ya",
atau "tidak". pertanyaan tentang gejala sakit kepala
Peminum kopi didefinisikan sebagai digunakan untuk mengklasifikasikan jenis
mereka yang dilaporkan minum setidaknya sakit kepala berdasarkan kriteria yang
satu cangkir kopi per minggu. Konsumsi ditetapkan oleh Klasifikasi Internasional
alkohol ditentukan dengan mengonsumsi Penyakit Kepala - edisi ke-3 (ICHD-III beta)
setidaknya satu gelas bir, anggur, atau koktail [17] sebagai migrain, tension type headache,
Dokter Muda THT-KL Periode Juni 2020 5
Fakultas Kedokteran Universitas Andalas

kemungkinan migrain, kemungkinan tension dinilai dalam model regresi log-binomial


type headache dan sakit kepala lain-lain yang disesuaikan. Rasio risiko dengan 95%
seperti yang dijelaskan dalam publikasi indeks kepercayaan diperkirakan.
sebelumnya [18]. Untuk menilai dampak potensial dari
faktor-faktor risiko yang diidentifikasi pada
Metode statistik tingkat populasi, population attributable risk
Posisi dan gerakan tubuh (gerakan fractions (populasi diatribusikan fraksi
kepala, perubahan posisi, duduk atau risiko) diperkirakan. Perkiraan ini tidak
berbaring, berdiri atau berjalan) terkait hanya mempertimbangkan kekuatan asosiasi,
dengan jenis vertigo (orthostatic dizziness tetapi juga prevalensi paparan pada populasi
(pusing ortostatik), spinning vertigo (vertigo yang diselidiki. Pendekatan berbasis model
berputar), swaying vertigo (pusing yang seperti fraksi yang dapat diatribusikan rata-
bergoyang), dan pusing yang tidak rata [19] dianggap sebagai penduga yang
ditentukan) dianalisis dengan menghitung paling kuat untuk PARF. Kami
proporsi siswa yang melaporkan posisi tubuh menggunakan kode untuk perangkat lunak
tertentu atau pergerakan dan interval statistik R yang disediakan oleh Ru¨ckinger
kepercayaan-95% yang sesuai (95% -CI) et al. [20] untuk menghitung PARF dengan
dalam empat kelompok tipe vertigo. metode ini.
Prevalensi dengan 95% indeks
kepercayaan dari segala jenis vertigo dan HASIL
vertigo berdasarkan paparan faktor risiko Usia rata-rata siswa yang mengambil bagian
(jenis kelamin, stres kronis, nyeri otot, dalam penelitian ini adalah 14,48 tahun (SD
konsumsi kopi, konsumsi alkohol, aktivitas = 1,08) berkisar antara 12 hingga 19 tahun.
fisik, merokok, durasi tidur pendek, dan 55% (N = 809) adalah perempuan dan 45%
migrain) dihitung. Hubungan antara faktor- (N = 673) adalah laki-laki. Analisis terperinci
faktor risiko yang diidentifikasi dinilai dalam tentang prevalensi vertigo dan pusing dalam
uji korelasi phi. Dalam model regresi log- studi MUKIS telah dipublikasikan
binomial univariat rasio risiko yang tidak sebelumnya [8]. Singkatnya, total 72% dari
disesuaikan dengan 95% indeks kepercayaan siswa melaporkan semacam vertigo / pusing
dihitung untuk hubungan antara faktor-faktor dalam 3 bulan terakhir. Dari 52% ini
risiko yang diidentifikasi dan vertigo. Untuk menderita pusing ortostatik, 12% dari vertigo
menjelaskan keterkaitan antara faktor-faktor yang berputar, 12% dari vertigo yang
risiko, asosiasi independen untuk faktor- berayun dan 16% dari pusing yang tidak
faktor risiko yang terkait untuk vertigo
Dokter Muda THT-KL Periode Juni 2020 6
Fakultas Kedokteran Universitas Andalas

spesifik, dengan beberapa siswa melaporkan dilaporkan secara signifikan lebih sering
lebih dari satu jenis gejala vertigo. menderita semua jenis vertigo kecuali untuk
vertigo yang tidak ditentukan. Durasi tidur
Posisi dan gerakan tubuh terkait dengan yang berkurang (<8 jam / hari) hanya terkait
tipe vertigo dengan vertigo yang berayun. Akhirnya,
Perubahan posisi adalah faktor yang pasien yang didiagnosis migrain secara
paling umum untuk memicu vertigo tanpa signifikan lebih sering mengalami vertigo,
perbedaan yang konsisten antara jenis-jenis terutama pusing ortostatik dan vertigo yang
vertigo. Hubungan dengan gerakan kepala berayun.
dan duduk atau berbaring terutama diamati
pada spinning and swaying vertigo (vertigo Hubungan univariat dan antara faktor
berputar dan bergoyang). Semua jenis vertigo risiko yang diidentifikasi dan vertigo yang
secara merata dilaporkan hadir ketika berdiri telah disesuaikan
atau berjalan oleh sekitar setengah dari siswa Tabel 3 menunjukkan hubungan
(Tabel 1). univariat dan saling disesuaikan antara faktor
risiko yang diidentifikasi (jenis kelamin, stres
Faktor risiko vertigo dan berbagai jenis kronis, nyeri otot, migrain) dan vertigo.
vertigo Rasio risiko yang tidak disesuaikan berkisar
Konsumsi kopi dan alkohol, merokok, antara 1,22 untuk migrain hingga 1,35 untuk
dan aktivitas fisik tidak terkait dengan nyeri otot. Karena semua faktor risiko yang
vertigo (lihat Tabel dalam File S1). Tabel 2 diidentifikasi terkait secara signifikan antara
menggambarkan hasil pada faktor-faktor satu sama lain (p <0,001 untuk semua
risiko yang secara signifikan terkait dengan kombinasi), model yang saling disesuaikan
terjadinya vertigo secara umum dan berbagai dihitung. Setelah penyesuaian, asosiasi
jenis vertigo. Siswa perempuan melaporkan independen diamati untuk semua faktor
vertigo lebih sering daripada siswa laki-laki risiko. Nyeri otot tampaknya menjadi faktor
sehubungan dengan semua jenis vertigo risiko independen terkuat untuk vertigo.
kecuali untuk vertigo berputar dan vertigo
yang tidak spesifik. Lebih lanjut, semua tipe Populasi risiko yang dapat diatribusikan
vertigo secara bermakna dikaitkan dengan (Population attributable risk fraction
peningkatan stres seperti yang ditunjukkan /PARF)
oleh skor TICS yang tinggi kecuali vertigo Tabel 4 menunjukkan PARF dari faktor
yang tidak spesifik. Juga, pasien dengan risiko yang diidentifikasi. Secara total faktor-
nyeri otot di daerah leher dan bahu faktor risiko ini menyumbang 26% dari
Dokter Muda THT-KL Periode Juni 2020 7
Fakultas Kedokteran Universitas Andalas

risiko populasi. Nyeri otot, stres kronis, dan pada remaja telah melaporkan dominasi
migrain mungkin dapat diterima untuk perempuan dalam keluhan kesehatan umum
intervensi pencegahan. Proporsi beban termasuk perasaan pusing [9, 10], sedangkan
penderita vertigo terkait faktor-faktor risiko satu penelitian retrospektif gagal
ini adalah sebesar 17%. mengidentifikasi perbedaan gender pada
remaja <18 tahun [24]. Kekuatan efek dalam
DISKUSI studi ini, dilaporkan sebagai odds rasio,
Dalam populasi remaja dengan ukuran berkisar antara 0,39 dan 1,79. Pengamatan
yang cukup besar dan beban tinggi menderita kami cocok dengan gender-spesifik
vertigo, kami menilai berbagai faktor risiko perempuan yang dilaporkan untuk penyakit
yang mungkin. Beberapa faktor risiko yang vertigo yang paling umum pada remaja,
dilaporkan pada orang dewasa dapat seperti migrain vestibular [11, 24-26].
dikonfirmasi pada remaja termasuk jenis Hubungan signifikan antara jenis
kelamin wanita, stres, nyeri otot di daerah kelamin perempuan dengan vertigo terutama
leher dan bahu, dan migrain, serta dijelaskan oleh vertigo tipe ortostatik dan
berkurangnya durasi tidur (hanya untuk pusing yang berayun. Pusing ortostatik telah
vertigo yang berayun). Setelah penilaian terbukti menjadi gejala umum pada populasi
timbal balik, karena keterkaitan faktor-faktor orang dewasa dengan prevalensi berkisar
risiko ini, peningkatan risiko yang terkait antara 5 hingga 13% [27]. Menariknya kedua
dengan faktor-faktor ini berada di kisaran 7 studi menunjukkan prevalensi pusing
hingga 24%. Dampak potensial dari ortostatik tertinggi pada kelompok usia
penghapusan faktor-faktor risiko yang dapat termuda <29 tahun mencapai hingga 22%.
dicegah (stres kronis, nyeri otot dan migrain) Lebih lanjut kedua studi menunjukkan
berjumlah 17%. dominasi perempuan dari pusing ortostatik.
Pusing ortostatik dapat dihasilkan dari
Spesifitas Jenis kelamin beragam patologi seperti hipotensi ortostatik
Penelitian ini menunjukkan hubungan awal (IOH), intoleransi ortostatik kronis,
vertigo yang signifikan dengan jenis kelamin intoleransi ortostatik disautonomis (hipotensi
perempuan dalam kelompok usia antara 12- ortostatik), dan sindrom tachycardia
19 tahun, yang cocok dengan data untuk ortostatik postural (POTS) termasuk
populasi yang lebih tua [4, 21-23]. intoleransi olahraga [28, 29]. Etiologi yang
Keterbatasan data hanya terbatas tentang paling umum pada anak-anak dan remaja
perbedaan gender pada remaja mengenai dianggap sebagai IOH [30-32], meskipun
penyakit vertigo. Dua dari tiga penelitian tidak ada data epidemiologis terperinci yang
Dokter Muda THT-KL Periode Juni 2020 8
Fakultas Kedokteran Universitas Andalas

tersedia. IOH adalah bentuk intoleransi beberapa penelitian melaporkan tidak ada
ortostatik jinak dengan integritas otonom perbedaan gender dalam prevalensi gangguan
yang jarang menyebabkan ketidaksadaran somatoform pada remaja [39, 41] yang lain
[30, 32]. Salah satu faktor risiko untuk IOH [38, 42]. Data vertigo somatoform pada
dianggap sebagai habitus asthenik [31]. remaja jarang, meskipun tampaknya menjadi
Dapat diterima bahwa siswa perempuan lebih salah satu diagnosis paling sering di antara
sering berhubungan dengan jenis habitus ini remaja dengan gejala vertigo [43]. Hanya
dan dengan demikian menjelaskan dominasi satu penelitian yang melaporkan dominasi
perempuan dalam penelitian ini. POTS lebih perempuan pada somatoform vertigo [44],
lanjut telah terbukti memiliki dominasi yang sesuai dengan temuan penelitian ini.
perempuan pada remaja [33, 34]. Sebuah Sensitivitas peningkatan pelaporan sensasi
penjelasan yang mungkin untuk toleransi tubuh secara umum [42, 45] dan / atau gaya
ortostatik yang lebih rendah pada wanita pelaporan yang berbeda dari gejala
disarankan oleh Fu et al. [35] Sementara somatoform [46] telah disarankan untuk
respons saraf simpatis selama ortostasis menghasilkan dominasi wanita seperti itu.
serupa pada pria dan wanita, Fu et al. Pada migrain, dominasi perempuan
menemukan volume stroke yang lebih kecil yang dimulai pada masa pubertas umumnya
karena pengisian jantung yang lebih rendah diterima [47-50]. Ini terutama dijelaskan oleh
pada wanita. Mereka menyatakan bahwa ini perubahan hormon karena banyak penelitian
dapat membanjiri cadangan vasomotor untuk telah menunjukkan hubungan antara sakit
vasokonstriksi atau mengendapkan penarikan kepala dan siklus menstruasi [51-53].
simpatis yang dimediasi secara netral. Demikian pula, dominasi wanita seperti itu
Sayangnya, kuesioner yang digunakan dalam juga terlihat pada migrain vestibular pada
penelitian ini tidak dapat membedakan antara orang dewasa [2], serta pada remaja [44],
kemungkinan patologi yang mendasarinya. yang sesuai dengan temuan penelitian ini.
Swaying vertigo sering digambarkan Karena studi spesifik tentang etiologi
sebagai gejala somatoform dan / atau fobia perbedaan gender dalam migrain vestibular
vertigo [36] dan dalam perpanjangan yang tidak ada, hanya dinyatakan mekanisme yang
lebih rendah dari migrain vestibular [37]. sama seperti pada migrain klasik.
Secara umum gangguan somatoform di
kalangan remaja dianggap umum [38, 39]. Nyeri Otot
Terdapat laporan tentang perbedaan gender Pada orang dewasa, nyeri otot dan
dalam gangguan somatoform remaja gejala vertigo sering hidup berdampingan
meskipun tetap kontroversial [40]. Sementara [54-56] Sepengetahuan kami, ini adalah studi
Dokter Muda THT-KL Periode Juni 2020 9
Fakultas Kedokteran Universitas Andalas

pertama yang menunjukkan hubungan terkait whiplash [64, 65] dan pada gangguan
tersebut dalam populasi remaja. Nyeri otot servikal degeneratif [66] Karena gangguan
adalah faktor risiko identifikasi terkuat untuk degeneratif tidak berperan pada remaja,
vertigo (lihat Tabel 3), terhitung 11% dari cedera whiplash dapat terjadi pada remaja.
risiko vertigo dalam populasi penelitian (lihat Sayangnya, kuesioner yang digunakan dalam
Tabel 4). Dalam praktik klinis koeksistensi penelitian ini tidak termasuk pertanyaan
nyeri leher dan bahu dengan vertigo tentang riwayat trauma.
seringkali memiliki konsekuensi bahwa Penjelasan alternatif dari koeksistensi
vertigo dikaitkan dengan tulang belakang vertigo dan nyeri otot di daerah leher dan
leher dan didiagnosis sebagai "cervical bahu bisa jadi bahwa nyeri otot servikal
vertigo" [57-59], yang dalam literatur terjadi secara reaktif terhadap vertigo,
merupakan diagnosis yang sangat bisa misalnya dimediasi oleh stres. Faktor
diperdebatkan [58, 60, 61] Aferen psikologis termasuk stres dapat
proprioseptif, sebagian besar berasal dari otot menyebabkan rasa sakit akut dan kronis pada
leher, telah disarankan untuk diproyeksikan orang dewasa [67] dan juga pada remaja [68,
ke nuklei vestibular dan memodifikasi 69] Selain itu, pasien dengan gangguan
aktivitas mereka sesuai dengan perubahan somatoform yang umum di antara remaja
posisi kepala. [62] Karena itu, propriosepsi dengan keluhan vertigo [43, 44], juga sering
yang terganggu dari segmen servikal dapat mengalami nyeri otot [70], sehingga
menyebabkan sensasi vertigo [61] gangguan somatoform yang mendasarinya
Menariknya distribusi, morfologi, dan dapat lebih menjelaskan hubungan vertigo
kepadatan spindle otot pada otot-otot tulang dan nyeri otot. Akhirnya perlu dicatat, bahwa
belakang leher tampaknya tidak berubah migrain juga diketahui berhubungan dengan
dengan usia [63], sehingga mekanisme yang nyeri otot di daerah leher dan bahu [71, 72]
dapat menyebabkan "cervical vertigo" bisa Menariknya hubungan untuk nyeri otot dan
serupa pada remaja dan orang dewasa. vertigo bahkan bertahan setelah penyesuaian
"Cervical vertigo" sebagai entitas independen untuk stres dan migrain, menunjukkan bahwa
meskipun masih menjadi bahan perdebatan nyeri otot merupakan faktor risiko
dan dalam banyak kasus gejala vertigo dapat independen. Patofisiologi yang tepat dari
dikaitkan dengan sejumlah diagnosis yang asosiasi ini masih belum diketahui dan
berbeda [58, 60, 61] merupakan bidang yang menarik untuk
Asosiasi lebih lanjut dari nyeri otot di penelitian di masa depan. Namun demikian,
daerah leher dan bahu dengan vertigo dan / intervensi yang mengarah pada pengurangan
atau pusing telah ditunjukkan pada kelainan nyeri otot mungkin juga bisa mengurangi
Dokter Muda THT-KL Periode Juni 2020 10
Fakultas Kedokteran Universitas Andalas

beban vertigo. Demikian pula, pasien-pasien migrain vestibular [36, 37], yang juga telah
ini mungkin juga mendapat manfaat dari terbukti sangat terkait dengan stres [77-79]
pencegahan stres dan pengobatan migrain Selanjutnya, swaying vertigo adalah
yang efektif. satu-satunya jenis vertigo yang menunjukkan
hubungan yang signifikan dengan durasi
Stres & durasi tidur tidur. Diketahui bahwa mengurangi durasi
Stres diketahui terkait dengan vertigo tidur pada remaja dapat menyebabkan, antara
dan pusing pada kelompok studi yang lebih lain, keluhan seperti pusing [80, 81] Kurang
tua [73], serta dalam kelompok yang lebih tidur pada remaja juga dapat dikaitkan
muda [74] Demikian pula dengan penelitian dengan stres secara umum [81-83],
ini, Torsheim dan Wold [74] menemukan menunjukkan kemungkinan interaksi dua
hubungan yang kuat antara stres terkait arah antara durasi tidur dan stres dengan
sekolah dan gejala pusing pada kelompok vertigo. Namun, risiko relatif untuk kurang
usia 11-15 tahun. Kekuatan efek dalam tidur hanya berubah sedikit setelah
penelitian ini, dengan rasio odds hingga 5,4, penyesuaian untuk stres (data tidak
jauh lebih tinggi daripada dalam penelitian ditampilkan), menunjukkan bahwa stres tidak
kami. Namun, penulis menggunakan rasio terdapat dalam jalur sebab akibat.
odds untuk menggambarkan risiko relatif,
yang melebih-lebihkan kekuatan efek untuk Migrain
hasil umum dan menggunakan hasil yang Dalam 35% [11] hingga 60% [84]
tidak spesifik ("pusing"). Arah kausal antara gejala vertigo remaja telah dilaporkan
stres dan vertigo tidak dapat disimpulkan. menyertai sakit kepala. Terutama remaja
Beberapa penulis berpendapat bahwa stres dengan migrain, jenis sakit kepala kedua
menyebabkan gejala vertigo [73], sementara yang paling umum pada remaja [85], 15%
yang lain berdebat untuk sebab yang terbalik hingga 25% juga mengalami semacam
[75] Sementara gejala pusing dan vertigo vertigo atau pusing [44, 86, 87] Demikian
pada anak-anak sama umumnya pada orang pula, dalam penelitian ini 85% dari semua
dewasa [8], kelainan vestibular pada anak- siswa yang memenuhi kriteria sakit kepala
anak tampaknya jarang. [43, 76] Karena itu, migrain juga mengalami beberapa jenis
arah kausal dimana stres menyebabkan gejala vertigo. Sayangnya, struktur kuesioner tidak
vertigo tampaknya lebih mungkin. Ini juga memungkinkan membedakan sekuens
didukung oleh peningkatan skor TICS pada temporal dari terjadinya sakit kepala dan
siswa yang mengalami swaying vertigo, vertigo dengan benar. Karena itu, kita tidak
suatu ciri khas dari somatoform vertigo atau bisa mengatakan apakah kedua gejala itu
Dokter Muda THT-KL Periode Juni 2020 11
Fakultas Kedokteran Universitas Andalas

kebetulan dan mana yang mendahului yang memungkinkan pengembangan terapi


mana. Ketika melihat tipe vertigo secara pencegahan pada anak-anak sekolah dengan
individual, pusing ortostatik menunjukkan mediasi awal strategi koping dan jika
hubungan terkuat dengan migrain. Studi memungkinkan pencegahan stres. Sebagai
menunjukkan bahwa pasien migrain lebih contoh, efektivitas program pencegahan satu
sering menderita masalah ortostatik dan kali, berbasis kelas untuk sakit kepala dapat
sinkop daripada populasi yang sehat [88] ditunjukkan oleh publikasi sebelumnya
Telah dipostulatkan bahwa hipersensitivitas dalam ruang lingkup studi MUKIS. [12]
dopamin berkontribusi terhadap patofisiologi
migrain yang mengarah pada penghambatan Kelebihan dan keterbatasan penelitian
pelepasan norepinefrin yang dimediasi Kelebihan penelitian ini adalah ukuran
dopamin, yang kemudian kembali populasi dan analisis dari tipe vertigo yang
menghasilkan hipotensi [89] Ini bisa spesifik. Tidak seperti kebanyakan studi
menjelaskan korelasi signifikan dari migrain sebelumnya, kami memperhitungkan saling
dengan pusing ortostatik dalam penelitian ini. ketergantungan antara faktor-faktor risiko
dengan penyesuaian timbal balik. Lebih
Kontribusi faktor risiko terhadap risiko lanjut dengan menilai PARF kami
total populasi vertigo mengidentifikasi proporsi potensi
Kontribusi faktor risiko individu pengurangan risiko total vertigo dengan
terhadap risiko populasi dijelaskan oleh strategi pencegahan.
kekuatan efek dan prevalensi faktor risiko: Keterbatasan penelitian ini mirip
faktor risiko yang lemah mungkin sangat dengan sebagian besar studi kuesioner cross-
relevan pada tingkat populasi jika umum, section. Misalnya, penyebab untuk nyeri otot
sementara faktor risiko yang kuat mungkin atau stres dan vertigo tidak dapat
hampir tidak relevan jika faktor risiko jarang dikesampingkan. Keterbatasan lebih lanjut,
terjadi. Kontribusi faktor risiko dapat sehubungan dengan konsep intervensi,
diungkapkan oleh PARF. Secara total, faktor mungkin, bahwa kami tidak menganalisis
risiko yang diidentifikasi menyumbang 26% lebih lanjut faktor-faktor yang menyebabkan
dari risiko vertigo pada remaja. Proporsi stres pada anak-anak sekolah. Tetapi
faktor risiko yang berpotensi menerima diketahui dari penelitian sebelumnya bahwa
intervensi preventif adalah sebesar 17%. faktor seperti pekerjaan sekolah, kontak
Faktor risiko yang paling menjanjikan untuk sosial, dan intimidasi merupakan faktor
ditargetkan, sehubungan dengan risiko total utama untuk stres yang dirasakan sendiri [90]
populasi, adalah nyeri otot dan stres. Hal ini
Dokter Muda THT-KL Periode Juni 2020 12
Fakultas Kedokteran Universitas Andalas

KESIMPULAN faktor-faktor risiko ini, kekuatan asosiasi ini


Kesimpulannya, jenis kelamin wanita, adalah sederhana. Faktor-faktor risiko ini
nyeri otot pada daerah leher dan bahu, stres, relevan, karena mereka sering terjadi pada
durasi tidur, dan migrain tampaknya menjadi remaja. Pada tingkat populasi, total PARF
faktor risiko yang signifikan untuk untuk faktor-faktor risiko yang dapat
pengembangan berbagai jenis pusing atau diterima untuk pencegahan berjumlah 17%,
vertigo pada remaja antara usia 12 dan 19 sehingga strategi pencegahan tampaknya
tahun. Mengikuti penyesuaian timbal balik diperlukan.
karena hubungan timbal balik di antara
Dokter Muda THT-KL Periode Juni 2020
Fakultas Kedokteran Universitas Andalas 13

LAMPIRAN TABEL
Tabel 1. Pergerakan dan posisi tubuh sebagai pemicu berbagai jenis vertigo.

Tabel 2. Prevalensi vertigo dan jenis vertigo spesifik pada murid yang memiliki atau tidak
factor risiko.
Dokter Muda THT-KL Periode Juni 2020
Fakultas Kedokteran Universitas Andalas 14

Tabel 3. Risiko relatif untuk vertigo berdasarkan jenis kelamin, stres kronis, nyeri otot, dan
migrain.

Tabel 4. Populasi yang diatribusikan fraksi risiko dari faktor risiko independen
RESEARCH ARTICLE

Vertigo and dizziness in adolescents: Risk


factors and their population attributable risk
Filipp M. Filippopulos1,2*, Lucia Albers3, Andreas Straube1,2, Lucia Gerstl4,
Bernhard Blum1, Thyra Langhagen4,2, Klaus Jahn2,5, Florian Heinen4, Rüdiger von Kries3,
Mirjam N. Landgraf4
1 Department of Neurology, University Hospital, LMU, Munich, Germany, 2 German Center for Vertigo and
Balance Disorders, LMU, Munich, Germany, 3 Institute of Social Paediatrics and Adolescents Medicine,
Division of Epidemiology, LMU, Munich, Germany, 4 Department of Paediatric Neurology and Developmental
Medicine, Hauner Children’s Hospital, LMU, Munich, Germany, 5 Department of Neurology, Schön Klinik Bad
Aibling, Bad Aibling, Germany
a1111111111
* filipp.filippopulos@med.uni-muenchen.de
a1111111111
a1111111111
a1111111111
a1111111111 Abstract
Objectives
To assess potential risk factors for vertigo and dizziness in adolescents and to evaluate their
OPEN ACCESS variability by different vertigo types. The role of possible risk factors for vertigo and dizziness
Citation: Filippopulos FM, Albers L, Straube A, in adolescents and their population relevance needs to be addressed in order to design pre-
Gerstl L, Blum B, Langhagen T, et al. (2017) ventive strategies.
Vertigo and dizziness in adolescents: Risk factors
and their population attributable risk. PLoS ONE 12
Study design
(11): e0187819. https://doi.org/10.1371/journal.
pone.0187819 The study population consisted of 1482 school-children between the age of 12 and 19 years,
Editor: Jong-Ling Fuh, Taipei Veterans General who were instructed to fill out a questionnaire on different vertigo types and related potential
Hospital, TAIWAN risk factors. The questionnaire specifically asked for any vertigo, spinning vertigo, swaying ver-
Received: July 26, 2017 tigo, orthostatic dizziness, and unspecified dizziness. Further a wide range of potential risk fac-
tors were addressed including gender, stress, muscular pain in the neck and shoulder region,
Accepted: October 26, 2017
sleep duration, migraine, coffee and alcohol consumption, physical activity and smoking.
Published: November 13, 2017

Copyright: © 2017 Filippopulos et al. This is an Results


open access article distributed under the terms of
Gender, stress, muscular pain in the neck and shoulder region, sleep duration and migraine
the Creative Commons Attribution License, which
permits unrestricted use, distribution, and were identified as independent risk factors following mutual adjustment: The relative risk
reproduction in any medium, provided the original was 1.17 [1.10–1.25] for female sex, 1.07 [1.02–1.13] for stress, 1.24 [1.17–1.32] for muscu-
author and source are credited.
lar pain, and 1.09 [1.03–1.14] for migraine. The population attributable risk explained by
Data Availability Statement: All relevant data are these risk factors was 26%, with muscular pain, stress, and migraine accounting for 11%,
within the paper and its Supporting Information
4%, and 3% respectively.
files.

Funding: The study was supported by an Conclusion


unrestricted fund of the DMKG (German Headache
Society). The authors have no financial Several established risk factors in adults were also identified in adolescents. Risk factors
relationships relevant to this article to disclose. amenable to prevention accounted for 17% of the total population risk. Therefore, interven-
Competing interests: The authors have declared tions targeting these risk factors may be warranted.
that no competing interests exist.

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 1 / 15


Risk factors of vertigo and dizziness in adolescents

Introduction
In general population dizziness and vertigo symptoms constitute a very common complaint
with a lifetime prevalence for dizziness of up to 30% and for vertigo of up to 10% [1]. Several
risk factors favouring the occurrence of vertigo or dizziness have been consistently observed in
adult or elderly populations. Vertigo is often associated to migraine [2], female gender [3, 4]
and psychological disorders such as depression [5, 6] and anxiety [7]. Although vertigo and
dizziness complaints in adolescents are as common as in adults [8], to our knowledge there is
only limited data about potential risk factors in adolescents and children. A couple of studies
with main focus on general health perception in adolescents have reported that females experi-
enced dizziness more often in the last 6 months than males [9, 10]. One further study of 31
children between 6 and 17 years of age described a significant association of vertigo with head-
ache [11]. One limitation of these studies though is, that they do not distinguish between dif-
ferent vertigo and/or dizziness types.
The present study in 1482 grammar school students (age range: 12 to 19 years) aimed to
delineate potential risk factors for the occurrence of different types of vertigo and dizziness
and to estimate their population attributable risk fractions in adolescents.

Methods
Population
The study population for this cross-sectional study was drawn from the headache interven-
tions study MUKIS (Münchner Untersuchung zu Kopfschmerzen bei Gymnasiasten–Inter-
ventions-Studie), which is described in detail elsewhere [12]. For this study, 12 out of 47 public
grammar schools in the greater area of Munich, Germany, agreed to participate. Reasons for
non-participation were its related administrative work load and inability to organize the study
in the school setting.
The study was conducted between November 2011 and January 2012 when a member of
the author team instructed the students to fill out a questionnaire during a visit of the specific
school. In total 1661 students attending the 8th, 9th, and 10th school grade filled out the ques-
tionnaire and a total of 1482 students (mean age: 14.47±1.08, range 12–19 years) completed
the full questionnaire and were included for the analysis.
The study was approved by the Data Safety Officer and the Ethics Committee of the Medical
Faculty of the Ludwig-Maximilians-University Munich and the Bavarian Ministry for Teach-
ing and Culture. All participating students and their parents/guardians gave written informed
consent to participate in the study.

Assessment of vertigo and vertigo types


Period prevalence of dizziness/vertigo was assessed by the question “Did you suffer from dizzi-
ness or vertigo during the last 3 months?” which could be answered with “yes” or “no”. If
answered “yes”, students were asked to further specify the vertigo type: “spinning vertigo like
in a carrousel” (spinning vertigo), “swaying vertigo like on a small boat” (swaying vertigo),
“feeling of impending black out when rapidly standing up” (orthostatic dizziness), or “neither
of the three types” (unspecified dizziness).

Assessment of body positions and movements related to vertigo types


The body positions and movements related to different vertigo types were assessed by the fol-
lowing questions, which could be answered with “yes” or “no”: The vertigo is a) triggered or

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 2 / 15


Risk factors of vertigo and dizziness in adolescents

aggravated by head movements, b) triggered by change of position (e.g. standing up from lay-
ing), c) also present when sitting or lying down, d) only present when standing or walking.

Assessment of potential risk factors


Chronic stress was assessed by the global stress index, which is based on 12 of the 57 items
included in the TICS (Trier Inventory of Chronic Stress) [13]. The frequency within the past 3
months for each of these items was indicated on a 5-point rating scale from 0 (never) to 4
(very often). Individual mean scores of all 12 items were calculated and t-transformed based
on age-group specific norm values (mean = 50; SD = 10). For the individual t-value, it was
determined whether the value was within normal range of the t-distribution, below or above
average. Chronic stress was assumed when the value was above the normal range. A good reli-
ability (Cronbach´s alpha of the global stress index: 0.91), high construct validity and high
scale correlation has been found [13].
Muscular pain in the neck and shoulder region was assessed by the question “Do you suffer
from muscle pain in the head, neck and shoulder region?” which could be answered with “yes”
or “no”.
Coffee drinkers were defined as those reported drinking at least one cup of coffee per week.
Alcohol consumption was defined by consuming at least one glass of beer, wine/champagne,
or cocktails/liquor per month. The definition of coffee drinkers and of alcohol consumption
was selected according to Milde-Busch et al. [14], who found associations of high coffee and
alcohol consumption with headache in adolescents. Physical activity was assessed by questions
on the frequency of weekly physical activity outside of school hours. Metabolic equivalent indi-
ces of the reported activities were calculated and categorized as high, moderate, or low by sam-
ple-specific tertiles from the distribution according to the procedure suggested by Kujala et al.
[15]. Students in the lowest tertile were assumed to be physically inactive, and the others as
physically active. Students were labeled as “smoking” when answering to the question “Do you
smoke?” with “yes”. Students were asked about their usual sleep duration (in hours). The aver-
age sleep duration per day was calculated and dichotomized into “>8 h sleep per day” and “
8 h sleep per day”. This dichotomy was chosen according to the recommendations for sleep
duration of the American Academy of Sleep Medicine [16].
For the assessment of migraine students were asked about suffering from any headache in
the last 6 months. When answering with “yes”, questions on headache symptoms were used to
classify the headache type based on criteria set by the International Classification of Headache
Disorders– 3rd edition (ICHD-III beta) [17] as either migraine, tension type headache, proba-
ble migraine, probable tension type headache and miscellaneous headache as described in a
previous publication [18].

Statistical methods
Body positions and movements (head movements, change of position, sitting or lying, stand-
ing or walking) related to vertigo types (orthostatic dizziness, spinning vertigo, swaying vertigo
and unspecified dizziness) were analyzed by calculating the proportion of students reporting a
specific body position/movement and the corresponding 95%-confidence intervals (95%-CI)
in the four groups of vertigo types.
Prevalence with 95%-CI of any vertigo and vertigo types by exposure to risk factors (gender,
chronic stress, muscular pain, coffee consumption, alcohol consumption, physical inactivity,
smoking, short sleep duration, and migraine) were calculated. The association among the
identified risk factors was assessed in phi correlation tests. In univariate log-binomial regres-
sion model unadjusted risk ratios with 95%-CIs were calculated for the association between

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 3 / 15


Risk factors of vertigo and dizziness in adolescents

the identified risk factors and vertigo. To account for the intercorrelation between risk factors,
independent associations for associated risk factors for vertigo were assessed in mutual
adjusted log-binomial regression models. Risk ratios with 95% CIs were estimated.
To assess the potential impact of the identified risk factors on a population level, population
attributable risk fractions (PARF) were estimated. This estimate considers not only the
strength of the association, but additionally the prevalence of exposure in the investigated pop-
ulation. Model-based approaches like the average attributable fraction [19] are considered the
most robust estimators for the PARF. We used codes for the statistical software R provided by
Rückinger et al. [20] to calculate the PARF with this method.

Results
The mean age of the students who took part in the present study was 14.48 years (SD = 1.08)
ranging from 12 to 19 years of age. 55% (N = 809) were female and 45% (N = 673) were male.
A detailed analysis of the prevalence of vertigo and dizziness in the MUKIS study has been
published previously [8]. In summary, a total 72% of the student reported some kind of ver-
tigo/dizziness in the last of 3 months. From these 52% suffered from orthostatic dizziness, 12%
from spinning vertigo, 12% from swaying vertigo and 16% of unspecified dizziness, with some
of the students reporting more than one kind of vertigo symptom.

Body positions and movements related to vertigo types


Change of position was the most prevalent factor for triggering vertigo without a consistent
difference between the vertigo types. A relation to head movements and sitting or lying was
mainly observed in spinning and swaying vertigo. All vertigo types were equally reported to be
present when standing or walking by about half of the students (Table 1).

Risk factors for vertigo and different vertigo types


Coffee and alcohol consumption, smoking, and physical activity were not associated with ver-
tigo (see Table in S1 File). Table 2 delineates results on the risk factors significantly associated
with the occurrence of vertigo in general and the different vertigo types. Female students
reported vertigo more often than male students with respect to all vertigo types except for spin-
ning vertigo and unspecific vertigo. Further, all vertigo types were significantly associated with
increased stress as indicated by an elevated TICS score except for unspecified vertigo. Also,
patients with muscular pain in the neck and shoulder region reported significantly more often

Table 1. Body positions and movements as a trigger for different vertigo types.
Vertigo triggered or aggravated by Vertigo triggered by Vertigo also present when Vertigo only present when
head movements change of position sitting or lying standing or walking
%
[95%CI]
Orthostatic 41.9 87.2 22.7 40.7
dizziness [38.0–45.8] [84.5–89.5] [19.5–26.3] [36.8–44.7]
Spinning vertigo 56.6 73.4 47.6 47.4
[48.3–64.6] [64.9–80.6] [38.9–56.6] [39.0–56.0]
Swaying vertigo 58.6 79.7 46.8 46.0
[50.4–66.3] [72.3–85.6] [38.5–55.3] [37.9–54.3]
Unspecified 37.8 75.8 24.5 41.0
dizziness [30.9–45.2] [69.3–81.3] [18.5–31.7] [33.9–48.5]

CI = confidence interval

https://doi.org/10.1371/journal.pone.0187819.t001

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 4 / 15


Risk factors of vertigo and dizziness in adolescents

Table 2. Prevalence of vertigo and specific vertigo types in students exposed/unexposed to potential risk factors.
Risk factor Vertigo Vertigo Types
N = 1066
Orthostatic dizziness Spinning vertigo Swaying vertigo Unspecified dizziness
N = 766 N = 173 N = 179 N = 232
% % % % %
[95%-CI] [95%-CI] [95%-CI] [95%-CI] [95%-CI]
(N) (N) (N) (N) (N)
Gender Female 79.3 57.9 12.3 15.2 17.6
N = 809 [76.3– [54.4–61.3] [10.2–14.8] [12.8–17.9] [15.1–20.5]
82.0]
(642) (469) (100) (123) (143)
Male 63 44.1 10.8 8.3 13.2
N = 673 [59.2– [40.3–47.9] [8.6–13.5] [6.4–10.7] [10.8–16.0]
66.6]
(424) (297) (73) (56) (89)
Chronic Stress–global stress index from Above normal 85.7 63.2 17.9 21.3 19.0
TICS1 range
N = 351 [81.5– [57.9–68.2] [14.1–22.4] [17.2–26.1] [15.1–23.6]
89.1]
(301) (222) (63) (75) (67)
Within normal 67.6 48.1 9.7 9.2 14.5
range
N = 1131 [64.8– [45.1–51.0] [8.0–11.6] [7.6–11.0] [12.6–16.8]
70.3]
(765) (544) (110) (104) (165)
Muscular pain in the neck and shoulder Yes 83.3 59.9 14.3 17.8 17.8
region N = 656 [80.2– [56.0–63.6] [11.7–17.3] [15.0–21.0] [15.0–21.0]
86.1]
(547) (393) (94) (117) (117)
No 62.8 45.1 9.5 7.5 13.9
N = 826
[59.4– [41.7–48.6] [7.6–11.8] [5.8–9.5] [11.6–16.5]
66.1]
(519) (373) (79) (62) (115)
Short sleep duration in average <8 hours 75.4 54.7 13.4 16.1 14.4
N = 497 [71.3–79.1] [50.2–59.1] [10.6–16.8] [13.0–19.6] [11.5–17.9]
(375) (272) (67) (80) (72)
in average 8 70.1 50.1 10.7 10.0 16.2
hours
N = 985 [67.1–72.9] [46.9–53.3] [8.9–12.9] [8.2–12.1] [14.0–18.7]
(691) (494) (106) (99) (160)
Migraine Yes 84.7 62.2 15.2 19.2 16.4
N = 249 [79.5– [55.8–68.2] [11.1–20.4] [14.6–24.8] [12.2–21.7]
88.8]
(211) (155) (38) (48) (41)
No 69.3 49.5 10.9 10.6 15.4
N = 1233 [66.6– [46.7–52.3] [9.2–12.8] [8.9–12.5] [13.5–17.6]
71.8]
(855) (611) (135) (131) (191)

N = number; CI = confidence interval. Significant differences (non-overlapping 95%-CIs) are printed in bold.
1
TICS = Trier Inventory of Chronic Stress

https://doi.org/10.1371/journal.pone.0187819.t002

to suffer from all vertigo types except for unspecified vertigo. A reduced sleep duration
(<8hours/day) was only associated with swaying vertigo. Finally, patients diagnosed with

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 5 / 15


Risk factors of vertigo and dizziness in adolescents

Table 3. Relative risk for vertigo by gender, chronic stress, muscular pain and migraine.
Any vertigo
Univariate Mutually adjusted
model model
RR RR
[95%-CI] [95%-CI]
Gender (female) 1.26 1.17
[1.18–1.35] [1.10–1.25]
Chronic stress–global stress index from TICS1 (Above 1.27 1.07
normal range) [1.20–1.34] [1.02–1.13]
Muscular pain in the neck and shoulder region 1.33 1.24
[1.25–1.41] [1.17–1.32]
Migraine 1.22 1.09
[1.15–1.30] [1.03–1.14]
https://doi.org/10.1371/journal.pone.0187819.t003

migraine experienced significantly more often vertigo, especially orthostatic dizziness and
swaying vertigo.

Univariate and mutually adjusted associations between identified risk


factors and vertigo
Table 3 shows the univariate and mutually adjusted associations between the identified risk
factors (gender, chronic stress, muscular pain, migraine) and vertigo. Unadjusted risk ratios
ranged from 1.22 for migraine to 1.35 for muscular pain. As all identified risk factors were sig-
nificantly associated among each other (p<0.001 for all combinations), a mutually adjusted
model was calculated. Following adjustment, independent associations were observed for all
risk factors. Muscular pain appeared to be the strongest independent risk factor for vertigo.

Population attributable risk fractions (PARF)


Table 4 shows the PARF of the identified risk factors. In total these risk factors accounted for
26% of the population risk. Muscular pain, chronic stress, and migraine are possibly amenable
to preventive interventions. The proportions of the burden of suffering from vertigo related to
these risk factors amounted to 17%.

Discussion
In an adolescent population of considerable size and a high burden of suffering from vertigo,
we assessed a broad range of possible risk factors. Several risk factors reported in adults could
be confirmed in adolescents including female sex, stress, muscular pain in the neck and shoul-
der region, and migraine, as well as a reduced sleep duration (only for swaying vertigo). After

Table 4. Population attributable risk fraction of independent risk factors.


Risk factors PARF (%)
Gender (female) 8.75
Chronic stress–global stress index from TICS1 (Above normal range) 4.22
Muscular pain in the neck and shoulder region 10.64
Migraine 2.76
Total 26.37
https://doi.org/10.1371/journal.pone.0187819.t004

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 6 / 15


Risk factors of vertigo and dizziness in adolescents

mutual assessment, because of intercorrelation of these risk factors, the risk increment related
to these factors was in the range of 7 to 24%. The potential impact of removal of the risk factors
amenable to prevention (chronic stress, muscular pain and migraine) amounted to 17%.

Gender specificity
The present study shows a significant association of vertigo with female sex in an age group
between 12–19 years, which matches data for older populations [4, 21–23]. There is only lim-
ited data on gender differences in adolescents concerning vertigo diseases. Two of three studies
in adolescents have reported a female predominance in general health complaints including
the feeling of being dizzy [9, 10], whereas one retrospective study failed to identify gender dif-
ferences in adolescents <18 years [24]. The strength of the effect in these studies, reported as
odds ratios, ranged between 0.39 and 1.79. Our observation matches the female gender-speci-
ficity reported for most common vertigo diseases in adolescents, such as vestibular migraine
[11, 24–26].
The significant association of female sex with vertigo was mainly explained by the vertigo
types orthostatic dizziness and swaying vertigo. Orthostatic dizziness has been shown to be a
common symptom in adult populations with the prevalence ranging between 5 to 13% [27].
Interestingly both studies showed the highest prevalence of orthostatic dizziness in the youn-
gest age group <29 years reaching up to 22%. Further both studies show a female predomi-
nance of orthostatic dizziness. Orthostatic dizziness can result from a diversity of pathologies
such as initial orthostatic hypotension (IOH), chronic orthostatic intolerance, dysautonomic
orthostatic intolerance (orthostatic hypotension), and postural orthostatic tachycardia syn-
drome (POTS) including exercise intolerance [28, 29]. The most common etiology in children
and adolescents is considered to be IOH [30–32], although no detailed epidemiological data is
available. IOH is a benign form of orthostatic intolerance with autonomic integrity that rarely
leads to unconsciousness [30, 32]. One risk factor for IOH is considered to be a asthenic habi-
tus [31]. It may be accepted that female students more often correspond to this kind of habitus
and thus explain the female predominance in the present study. Further POTS has been
shown to have a female predominance in adolescents [33, 34]. A possible explanation for
lower orthostatic tolerance in women is suggested by Fu et al. [35]. While sympathetic neural
responses during orthostasis are similar in men and women, Fu et al. found a smaller stroke
volume due to lower cardiac filling in women. They postulate that this may overwhelm the
vasomotor reserve for vasoconstriction or precipitate neutrally mediated sympathetic with-
drawal. Unfortunately, the questionnaire used in the present study could not differentiate
between possible underlying pathologies.
Swaying vertigo is often described as a symptom of somatoform and/or phobic vertigo [36]
and in lesser extend of vestibular migraine [37]. In general somatoform disorders among ado-
lescents are considered to be common [38, 39]. Reports on gender differences in somatoform
disorders of adolescents though remain controversial [40]. While some studies report no gen-
der differences in the prevalence of somatoform disorders in adolescents [39, 41] others do
[38, 42]. Data on somatoform vertigo in adolescents is sparse, although it seems to be one of
the most frequent diagnosis among adolescents with vertigo symptoms [43]. Only one study
reports a female predominance in somatoform vertigo [44], which matches the findings of the
present study. A general increased sensitivity of reporting body sensations [42, 45] and/or a
different reporting style of somatoform symptoms [46] have been suggested to result into such
an female predominance.
In migraine, a female predominance starting in puberty is generally accepted [47–50]. This
is mainly explained by hormonal changes as numerous studies have shown associations

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 7 / 15


Risk factors of vertigo and dizziness in adolescents

between headache and the menstrual cycle [51–53]. Similarly, such a female predominance is
also seen in vestibular migraine in adults [2], as well as in adolescents [44], which matches the
findings of the present study. As specific studies on the etiology of such gender differences in
vestibular migraine are missing, only similar mechanisms as in classical migraine can be
postulated.

Muscular pain
In adults muscular pain and vertigo symptoms often coexist [54–56]. To our knowledge this is
the first study to show such an association in an adolescent population. Muscular pain was the
strongest identified risk factor for vertigo (see Table 3), accounting for 11% of the vertigo risk
in the study population (see Table 4). In clinical practice the coexistence of neck and shoulder
pain with vertigo has often the consequence that the vertigo is attributed to the cervical spine
and diagnosed as “cervical vertigo” [57–59], which in the literature constitutes a highly debat-
able diagnosis [58, 60, 61]. Proprioceptive afferences, mostly originating from the neck‘s mus-
cle spindles, have been suggested to project to vestibular nuclei and modify their activity
according to position changes of the head [62]. In consequence, a disturbed proprioception
from the cervical segments could lead to a vertigo sensation [61]. Interestingly the distribution,
morphology, and density of muscle spindles in muscles of the cervical spine seem not to
change with age [63], so that the mechanisms that may lead to “cervical vertigo” could be simi-
lar in adolescents and adults. “Cervical vertigo” as an independent entity though remains a
matter of debate and in many cases the vertigo symptoms can be attributed to a number of dif-
ferential diagnoses [58, 60, 61].
Further associations of muscular pain in the neck and shoulder region with vertigo and/or
dizziness have been shown in whiplash associated disorders [64, 65] and in degenerative cervi-
cal disorders [66]. As degenerative disorders do not play a role in adolescents, whiplash inju-
ries could occur in adolescents. Unfortunately, the questionnaire used in the present study did
not include questions about trauma history.
An alternative explanation of the coexistence of vertigo and muscular pain in the neck and
shoulder region could be that the cervical muscular pain occurs reactively to the vertigo, e.g.
mediated by stress. Psychological factors including stress can lead to acute and chronic pain
conditions in adults [67] as well as in adolescents [68, 69]. Additionally, patients with somato-
form disorders, which are common among adolescents with vertigo complaints [43, 44], also
frequently experience muscular pain [70], so that an underlying somatoform disorder could
further explain the association of vertigo and muscular pain. Finally it is notable, that migraine
is also known to be associated to muscular pain in the neck and shoulder region [71, 72]. Inter-
estingly the association for muscular pain and vertigo even persisted after adjustment for stress
and migraine, suggesting that muscular pain constitutes an independent risk factor. The exact
pathophysiology of this association remains unknown and poses an interesting field for future
research. Nevertheless, interventions leading to a reduction of muscular pain might also
reduce the burden of vertigo. Similarly, these patients might also benefit from stress prevention
and effective migraine treatment.

Stress & sleep duration


Stress is known to be associated with vertigo and dizziness in older study groups [73], as well
as in younger groups [74]. Similarly to the present study, Torsheim and Wold [74] found a
strong association between school-related stress and dizziness symptoms in an age group of
11–15 years. The strength of the effect in this study, with odds ratios up to 5.4, is considerably
higher than in our study. However, the authors used the odds ratio to describe the relative risk,

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 8 / 15


Risk factors of vertigo and dizziness in adolescents

which overestimates the strength of the effect for common outcomes and used an unspecific
outcome (“dizziness”). The causal direction between stress and vertigo is inconclusive. Several
authors suggest that stress leads to vertigo symptoms[73], while others argue for a reversed
causation [75]. While dizziness and vertigo symptoms in children are as common as in adults
[8], underlying vestibular disorders in children seem to be rare [43, 76]. Therefore, the causal
direction that stress leads to vertigo symptoms seems to be more likely. This is also supported
by the elevated TICS score in students experiencing swaying vertigo, a typical characteristic of
somatoform vertigo or vestibular migraine [36, 37], which has also been shown to be strongly
associated to stress [77–79].
Further swaying vertigo was the only vertigo type that showed a significant association with
sleep duration. It is known that reduced sleep duration in adolescents can lead, among others,
to complaints such as dizziness [80, 81]. Sleep deprivation in adolescents can also be associated
with stress in general [81–83], suggesting a possible bi-directional interaction between sleep
duration and stress with vertigo. However, the relative risk for sleep deprivation changed only
marginally after adjustment for stress (data not shown), suggesting that stress is not in the causal
pathway.

Migraine
In 35% [11] to 60% [84] of adolescents vertigo symptoms have been reported to accompany
headaches. Especially adolescents with migraine, the second most common headache type in
adolescents [85], 15% to 25% also experience some kind of vertigo or dizziness [44, 86, 87]. Sim-
ilarly, in the present study 85% of all students fulfilling the criteria of migraine headache also
experienced some kind of vertigo. Unfortunately, the questionnaire structure did not allow dis-
tinguishing the temporal sequence of the occurrence of headache and vertigo properly. There-
fore, we cannot say whether both symptoms were a coincidence and which preceded which.
When looking at the vertigo types individually, orthostatic dizziness showed the strongest asso-
ciation with migraine. Studies show that migraine patients more often suffer from orthostatic
problems and syncopes than the healthy population [88]. It has been postulated that dopamine
hypersensitivity contributes to the pathophysiology of migraine leading to a dopamine mediated
inhibition of norepinephrine release, which then again results into hypotension [89]. This could
explain the significant correlation of migraine with orthostatic dizziness in the present study.

Contribution of the risk factors to the total population risk of vertigo


The contribution of the individual risk factors to the population risk is explained by the
strength of the effect and by the prevalence of the risk factor: a weak risk factor may be highly
relevant on the population level if common, while a strong risk factor may be almost irrelevant
if the risk factor is rare. The contribution of the risk factors can be expressed by the PARF. In
total, the identified risk factors accounted for 26% of the risk of vertigo in adolescents. The
proportion of risk factors potentially amenable to preventive interventions amounted to 17%.
The most promising risk factors to be targeted, with respect to total population risk, were mus-
cular pain and stress. This may allow establishing preventive therapies in school children by
early mediation of coping strategies and if possible stress prevention. For example, the effec-
tiveness of a one-time, classroom-based prevention program for headache could be demon-
strated by a previous publication within the scope of the MUKIS study [12].

Strength and limitations of the study


The strength of the study is the population size and the analysis of specific vertigo types. Unlike
most previous studies, we took account of interdependencies between the risk factors by

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 9 / 15


Risk factors of vertigo and dizziness in adolescents

mutual adjustment. Further by assessing the PARF we identified the proportion of the poten-
tial total risk reduction of vertigo by preventive strategies.
The limitations of the present study are similar to most cross-section questionnaire studies.
E.g., reversed causation for muscular pain or stress and vertigo cannot be ruled out. A further
limitation, with respect to conceptualize interventions, may be, that we did not further analyze
the factors causing stress in school children. But it is known from previous studies that factors
such as school work, social contacts, and bullying constitute main factors for self-perceived
stress [90].

Conclusion
In conclusion, female gender, muscular pain in the neck and shoulder region, stress, sleep
duration, and migraine seem to be significant risk factors for the development of different diz-
ziness or vertigo types in adolescents between 12 and 19 years of age. Following mutual adjust-
ment because of intercorrelation among these risk factors, the strength of these associations
was modest. These risk factors are nevertheless relevant, because they are common in adoles-
cents. On the population level, the total PARF for risk factors amenable to prevention
amounted to 17%, so that preventive strategies appear to be warranted.

Supporting information
S1 File. Table. Prevalence of vertigo and specific vertigo types in students exposed/unex-
posed to potential risk factors, that were not significantly associated with vertigo/vertigo
types.
(DOCX)
S2 File. Dataset.
(CSV)
S3 File. Questionnaire in German (original language).
(DOC)
S4 File. Questionnaire in English.
(DOC)

Acknowledgments
We would like to thank all participating students and teachers, the Bavarian Ministry of Edu-
cation and the DMKG (German Headache Society) for giving us the opportunity to perform
this study.

Author Contributions
Conceptualization: Filipp M. Filippopulos, Andreas Straube, Lucia Gerstl, Klaus Jahn, Florian
Heinen, Rüdiger von Kries, Mirjam N. Landgraf.
Data curation: Lucia Albers.
Formal analysis: Lucia Albers, Rüdiger von Kries.
Investigation: Filipp M. Filippopulos, Lucia Gerstl, Bernhard Blum, Thyra Langhagen, Mir-
jam N. Landgraf.
Methodology: Andreas Straube, Lucia Gerstl, Klaus Jahn, Florian Heinen, Rüdiger von Kries,
Mirjam N. Landgraf.

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 10 / 15


Risk factors of vertigo and dizziness in adolescents

Project administration: Andreas Straube, Florian Heinen.


Software: Lucia Albers.
Supervision: Filipp M. Filippopulos, Andreas Straube, Klaus Jahn, Florian Heinen, Rüdiger
von Kries.
Writing – original draft: Filipp M. Filippopulos.
Writing – review & editing: Filipp M. Filippopulos, Lucia Albers, Andreas Straube, Bernhard
Blum, Thyra Langhagen, Rüdiger von Kries, Mirjam N. Landgraf.

References
1. Murdin L, Schilder AG. Epidemiology of balance symptoms and disorders in the community: a system-
atic review. Otol Neurotol. 2015; 36(3):387–92. https://doi.org/10.1097/MAO.0000000000000691
PMID: 25548891
2. Lempert T, Neuhauser H. Epidemiology of vertigo, migraine and vestibular migraine. J Neurol. 2009;
256(3):333–8. https://doi.org/10.1007/s00415-009-0149-2 PMID: 19225823
3. Jönsson R, Sixt E, Landahl S, Rosenhall U. Prevalence of dizziness and vertigo in an urban elderly pop-
ulation. J Vestib Res. 2004; 14(1):47–52. PMID: 15156096
4. Maarsingh OR, Dros J, Schellevis FG, van Weert HC, Bindels PJ, Horst HE. Dizziness reported by
elderly patients in family practice: prevalence, incidence, and clinical characteristics. BMC Fam Pract.
2010; 11(1):2.
5. Neuhauser H, Von Brevern M, Radtke A, Lezius F, Feldmann M, Ziese T, et al. Epidemiology of vestibu-
lar vertigo A neurotologic survey of the general population. Neurology. 2005; 65(6):898–904. https://doi.
org/10.1212/01.wnl.0000175987.59991.3d PMID: 16186531
6. Monzani D, Casolari L, Guidetti G, Rigatelli M. Psychological distress and disability in patients with ver-
tigo. J Psychosom Res. 2001; 50(6):319–23. PMID: 11438113
7. Wiltink J, Tschan R, Michal M, Subic-Wrana C, Eckhardt-Henn A, Dieterich M, et al. Dizziness: Anxiety,
health care utilization and health behavior—: Results from a representative German community survey.
J Psychosom Res. 2009; 66(5):417–24. https://doi.org/10.1016/j.jpsychores.2008.09.012 PMID:
19379958
8. Langhagen T, Albers L, Heinen F, Straube A, Filippopulos F, Landgraf MN, et al. Period Prevalence of
Dizziness and Vertigo in Adolescents. PLoS One. 2015; 10(9):e0136512. https://doi.org/10.1371/
journal.pone.0136512 PMID: 26361225
9. Torsheim T, Ravens-Sieberer U, Hetland J, Välimaa R, Danielson M, Overpeck M. Cross-national vari-
ation of gender differences in adolescent subjective health in Europe and North America. Soc Sci Med.
2006; 62(4):815–27. http://dx.doi.org/10.1016/j.socscimed.2005.06.047. https://doi.org/10.1016/j.
socscimed.2005.06.047 PMID: 16098649
10. Erginoz E, Alikasifoglu M, Ercan O, Uysal O, Ercan G, Albayrak Kaymak D, et al. Perceived health sta-
tus in a Turkish adolescent sample: risk and protective factors. Eur J Pediatr. 2004; 163(8):485–94.
https://doi.org/10.1007/s00431-004-1446-5 PMID: 15160291
11. Weisleder P, Fife TD. Dizziness and headache: a common association in children and adolescents. J
Child Neurol. 2001; 16(10):727–30. https://doi.org/10.1177/088307380101601004 PMID: 11669345
12. Albers L, Heinen F, Landgraf M, Straube A, Blum B, Filippopulos F, et al. Headache cessation by an
educational intervention in grammar schools: a cluster randomized trial. Eur J Neurol. 2015; 22(2):270–
e22. https://doi.org/10.1111/ene.12558 PMID: 25244562
13. Schulz P, Scholtz W, Becker P. Trier Inventory for the Assessment of Chronic Stress. Hofgrefe, Goettin-
gen. 2004.
14. Milde-Busch A, Blaschek A, Borggräfe I, Heinen F, Straube A, Von Kries R. Associations of Diet and
Lifestyle With Headache in High-School Students: Results From a Cross-Sectional Study. Headache:
The Journal of Head and Face Pain. 2010; 50(7):1104–14.
15. Kujala UM, Taimela S, Viljanen T. Leisure physical activity and various pain symptoms among adoles-
cents. Br J Sports Med. 1999; 33(5):325–8. PMID: 10522634
16. Paruthi S, Brooks LJ, D’Ambrosio C, Hall WA, Kotagal S, Lloyd RM, et al. Recommended amount of
sleep for pediatric populations: a consensus statement of the American Academy of Sleep Medicine.
Journal of clinical sleep medicine: JCSM: official publication of the American Academy of Sleep Medi-
cine. 2016; 12(6):785.

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 11 / 15


Risk factors of vertigo and dizziness in adolescents

17. Society HCCotIH. The international classification of headache disorders, (beta version). Cephalalgia.
2013; 33(9):629–808. https://doi.org/10.1177/0333102413485658 PMID: 23771276
18. Fritsche G, Hueppe M, Kukava M, Dzagnidze A, Schuerks M, Yoon MS, et al. Validation of a German
Language Questionnaire for Screening for Migraine, Tension-Type Headache, and Trigeminal Auto-
nomic Cephalgias. Headache. 2007; 47(4):546–51. https://doi.org/10.1111/j.1526-4610.2007.00758.x
PMID: 17445104
19. Eide GE, Gefeller O. Sequential and average attributable fractions as aids in the selection of preventive
strategies. J Clin Epidemiol. 1995; 48(5):645–55. PMID: 7730921
20. Rückinger S, von Kries R, Toschke AM. An illustration of and programs estimating attributable fractions
in large scale surveys considering multiple risk factors. BMC Med Res Methodol. 2009; 9(1):7.
21. Sloane P. Dizziness in primary care. Results from the National Ambulatory Medical Care Survey. J Fam
Pract. 1989; 29(1):33–8. PMID: 2738548
22. Aggarwal N, Bennett D, Bienias J, Mendes dLC, Morris M, Evans D. The prevalence of dizziness and its
association with functional disability in a biracial community population. J Gerontol A Biol Sci Med Sci.
2000; 55(5):M288. PMID: 10819319
23. Neuhauser HK. Epidemiology of vertigo. Curr Opin Neurol. 2007; 20(1):40–6. https://doi.org/10.1097/
WCO.0b013e328013f432 PMID: 17215687
24. Yin M, Ishikawa K, Wong WH, Shibata Y. A clinical epidemiological study in 2169 patients with vertigo.
Auris Nasus Larynx. 2009; 36(1):30–5. https://doi.org/10.1016/j.anl.2008.03.006 PMID: 18486378
25. Choung Y-H, Park K, Moon S-K, Kim C-H, Ryu SJ. Various causes and clinical characteristics in vertigo
in children with normal eardrums. Int J Pediatr Otorhinolaryngol. 2003; 67(8):889–94. PMID: 12880669
26. Riina N, Ilmari P, Kentala E. Vertigo and imbalance in children: a retrospective study in a Helsinki Uni-
versity otorhinolaryngology clinic. Arch Otolaryngol Head Neck Surg. 2005; 131(11):996–1000. https://
doi.org/10.1001/archotol.131.11.996 PMID: 16301372
27. Radtke A, Lempert T, von Brevern M, Feldmann M, Lezius F, Neuhauser H. Prevalence and complica-
tions of orthostatic dizziness in the general population. Clin Auton Res. 2011; 21(3):161–8. https://doi.
org/10.1007/s10286-010-0114-2 PMID: 21279415
28. Stewart JM. Orthostatic intolerance in pediatrics. J Pediatr. 2002; 140(4):404–11. http://dx.doi.org/10.
1067/mpd.2002.122727. https://doi.org/10.1067/mpd.2002.122727 PMID: 12006953
29. Stewart JM. Transient orthostatic hypotension is common in adolescents. J Pediatr. 2002; 140(4):418–
24. http://dx.doi.org/10.1067/mpd.2002.122643. https://doi.org/10.1067/mpd.2002.122643 PMID:
12006955
30. Stewart JM, Clarke D. “He’s Dizzy when he Stands Up.” An Introduction to Initial orthostatic Hypoten-
sion. J Pediatr. 2011; 158(3):499. https://doi.org/10.1016/j.jpeds.2010.09.004 PMID: 20970148
31. Wieling W, Krediet C, Van Dijk N, Linzer M, Tschakovsky M. Initial orthostatic hypotension: review of a
forgotten condition. Clin Sci. 2007; 112:157–65. https://doi.org/10.1042/CS20060091 PMID: 17199559
32. Jarjour IT, editor Postural tachycardia syndrome in children and adolescents. Semin Pediatr Neurol;
2013: Elsevier.
33. Thieben MJ, Sandroni P, Sletten DM, Benrud-Larson LM, Fealey RD, Vernino S, et al., editors. Postural
orthostatic tachycardia syndrome: the Mayo clinic experience. Mayo Clin Proc; 2007: Elsevier.
34. Raj SR. The postural tachycardia syndrome (POTS): pathophysiology, diagnosis & management.
Indian Pacing Electrophysiol J. 2006; 6(2):84. PMID: 16943900
35. Fu Q, Witkowski S, Okazaki K, Levine BD. Effects of gender and hypovolemia on sympathetic neural
responses to orthostatic stress. American Journal of Physiology-Regulatory, Integrative and Compara-
tive Physiology. 2005; 289(1):R109–R16. https://doi.org/10.1152/ajpregu.00013.2005 PMID: 15761188
36. Strupp M, Brandt T. Diagnosis and treatment of vertigo and dizziness. Dtsch Arztebl. 2008; 105
(10):173.
37. Dieterich M, Brandt T. Episodic vertigo related to migraine (90 cases): vestibular migraine? J Neurol.
1999; 246(10):883–92. https://doi.org/10.1007/s004150050478 PMID: 10552234
38. Lieb R, Pfister H, Mastaler M, Wittchen HU. Somatoform syndromes and disordersin a representative
population sample of adolescents and young adults: prevalence, comorbidity and impairments. Acta
Psychiatr Scand. 2000; 101(3):194–208. PMID: 10721868
39. Wittchen H- U, Nelson CB, Lachner G. Prevalence of mental disorders and psychosocial impairments
in adolescents and young adults. Psychol Med. 1998; 28(1):109–26. PMID: 9483687
40. Wool CA, Barsky AJ. Do women somatize more than men?: Gender differences in somatization. Psy-
chosomatics. 1994; 35(5):445–52. https://doi.org/10.1016/S0033-3182(94)71738-2 PMID: 7972659
41. Mullick MS. Somatoform disorders in children and adolescents. Bangladesh Med Res Counc Bull.
2002; 28(3):112–22. PubMed PMID: PMID: 14509383.

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 12 / 15


Risk factors of vertigo and dizziness in adolescents

42. Garber J, Walker LS, Zeman J. Somatization symptoms in a community sample of children and adoles-
cents: Further validation of the Children’s Somatization Inventory. Psychological Assessment: A Journal
of Consulting and Clinical Psychology. 1991; 3(4):588.
43. Jahn K, Langhagen T, Schroeder A, Heinen F. Vertigo and Dizziness in Childhood− Update on Diagno-
sis and Treatment. Neuropediatrics. 2011; 42(04):129–34.
44. Langhagen T, Schroeder AS, Rettinger N, Borggraefe I, Jahn K. Migraine-related vertigo and somato-
form vertigo frequently occur in children and are often associated. Neuropediatrics. 2013; 44(01):055–8.
45. Garralda ME. Somatisation in Children. Journal of Child Psychology and Psychiatry. 1996; 37(1):13–
33. https://doi.org/10.1111/j.1469-7610.1996.tb01378.x PMID: 8655655
46. Kroenke K, Spitzer RL. Gender differences in the reporting of physical and somatoform symptoms. Psy-
chosom Med. 1998; 60(2):150–5. PMID: 9560862
47. Stewart WF, Simon D, Shechter A, Lipton RB. Population variation in migraine prevalence: a meta-anal-
ysis. J Clin Epidemiol. 1995; 48(2):269–80. PMID: 7869073
48. Hirtz D, Thurman D, Gwinn-Hardy K, Mohamed M, Chaudhuri A, Zalutsky R. How common are the
“common” neurologic disorders? Neurology. 2007; 68(5):326–37. https://doi.org/10.1212/01.wnl.
0000252807.38124.a3 PMID: 17261678
49. Lipton RB, Stewart WF, Diamond S, Diamond ML, Reed M. Prevalence and burden of migraine in the
United States: data from the American Migraine Study II. Headache: The Journal of Head and Face
Pain. 2001; 41(7):646–57.
50. Smitherman TA, Burch R, Sheikh H, Loder E. The prevalence, impact, and treatment of migraine and
severe headaches in the United States: a review of statistics from national surveillance studies. Head-
ache: The Journal of Head and Face Pain. 2013; 53(3):427–36.
51. Johannes C, Linet M, Stewart W, Celentano D, Lipton R, Szklo M. Relationship of headache to phase of
the menstrual cycle among young women A daily diary study. Neurology. 1995; 45(6):1076–82. PMID:
7783866
52. Silberstein S, Merriam G. Physiology of the menstrual cycle. Cephalalgia. 2000; 20(3):148–54. https://
doi.org/10.1046/j.1468-2982.2000.00034.x PMID: 10997766
53. MacGregor E, Frith A, Ellis J, Aspinall L, Hackshaw A. Incidence of migraine relative to menstrual cycle
phases of rising and falling estrogen. Neurology. 2006; 67(12):2154–8. https://doi.org/10.1212/01.wnl.
0000233888.18228.19 PMID: 16971700
54. Attry S, Gupta VK, Marwah K, Bhargav S, Gupta E, Vashisth N. “Cervical Vertigo-Pathophysiology and
Management: An Update". IOSR Journal of Dental and Medical Sciences (IOSR-JDMS). 2016; 1
(15):98–107.
55. De Jong J, Bles W. Cervical dizziness and ataxia. Disorders of posture and gait Amsterdam: Elsevier.
1986:185–206.
56. Wrisley DM, Sparto PJ, Whitney SL, Furman JM. Cervicogenic dizziness: a review of diagnosis and
treatment. J Orthop Sports Phys Ther. 2000; 30(12):755–66. https://doi.org/10.2519/jospt.2000.30.12.
755 PMID: 11153554
57. Somefun O, Giwa O, Bamgboye B, Okeke-Igbokwe II, Azeez AA. Vestibular disorders among adults in
a tertiary hospital in Lagos, Nigeria. Eur Arch Otorhinolaryngol. 2010; 267(10):1515–21. https://doi.org/
10.1007/s00405-010-1272-5 PMID: 20464409
58. Yacovino DA, Hain TC, editors. Clinical characteristics of cervicogenic-related dizziness and vertigo.
Semin Neurol; 2013: Thieme Medical Publishers.
59. Reid SA, Rivett DA. Manual therapy treatment of cervicogenic dizziness: a systematic review. Man
Ther. 2014; 10(1):4–13. https://doi.org/10.1016/j.math.2004.03.006 PMID: 15681263
60. Brandt T. Cervical vertigo–reality or fiction? Audiol Neurootol. 1996; 1(4):187–96. PMID: 9390801
61. Brandt T, Bronstein A. Cervical vertigo. J Neurol Neurosurg Psychiatry. 2001; 71(1):8–12. https://doi.
org/10.1136/jnnp.71.1.8 PMID: 11413255
62. Cullen KE, Roy JE. Signal processing in the vestibular system during active versus passive head move-
ments. J Neurophysiol. 2004; 91(5):1919–33. https://doi.org/10.1152/jn.00988.2003 PMID: 15069088
63. Boyd-Clark L, Briggs C, Galea M. Muscle spindle distribution, morphology, and density in longus colli
and multifidus muscles of the cervical spine. Spine (Phila Pa 1976). 2002; 27(7):694–701.
64. Radanov BP, Sturzenegger M, Di Stefano G. Long-term outcome after whiplash injury: a 2-year follow-
up considering features of injury mechanism and somatic, radiologic, and psychosocial findings. Medi-
cine. 1995; 74(5):281–97. PMID: 7565068
65. Partheni M, Constantoyannis C, Ferrari R, Nikiforidis G, Voulgaris S, Papadakis N. A prospective cohort
study of the outcome of acute whiplash injury in Greece. Clin Exp Rheumatol. 2000; 18(1):67–70.
PMID: 10728446

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 13 / 15


Risk factors of vertigo and dizziness in adolescents

66. Hain TC. Cervicogenic causes of vertigo. Curr Opin Neurol. 2015; 28(1):69–73. https://doi.org/10.1097/
WCO.0000000000000161 PMID: 25502050
67. Linton SJ. A review of psychological risk factors in back and neck pain. Spine (Phila Pa 1976). 2000; 25
(9):1148–56.
68. Murphy S, Buckle P, Stubbs D. A cross-sectional study of self-reported back and neck pain among
English schoolchildren and associated physical and psychological risk factors. Appl Ergon. 2007; 38
(6):797–804. https://doi.org/10.1016/j.apergo.2006.09.003 PMID: 17181995
69. Diepenmaat A, Van der Wal M, De Vet H, Hirasing R. Neck/shoulder, low back, and arm pain in relation
to computer use, physical activity, stress, and depression among Dutch adolescents. Pediatrics. 2006;
117(2):412–6. https://doi.org/10.1542/peds.2004-2766 PMID: 16452360
70. Ursin H. Sensitization, somatization, and subjective health complaints. Int J Behav Med. 1997; 4
(2):105–16. https://doi.org/10.1207/s15327558ijbm0402_1 PMID: 16250733
71. Blaschek A, Milde-Busch A, Straube A, Schankin C, Langhagen T, Jahn K, et al. Self-reported muscle
pain in adolescents with migraine and tension-type headache. Cephalalgia. 2012; 32(3):241–9. https://
doi.org/10.1177/0333102411434808 PMID: 22250208
72. Anttila P, Metsähonkala L, Mikkelsson M, Helenius H, Sillanpää M. Comorbidity of other pains in school-
children with migraine or nonmigrainous headache. J Pediatr. 2001; 138(2):176–80. https://doi.org/10.
1067/mpd.2001.112159 PMID: 11174613
73. Andersson G, Yardley L. Time-series Analysis of the Relationship between Dizziness and Stress.
Scand J Psychol. 2000; 41(1):49–54. PMID: 10731843
74. Torsheim T, Wold B. School-Related Stress, School Support, and Somatic Complaints A General Popu-
lation Study. J Adolesc Res. 2001; 16(3):293–303.
75. Jacob RG, Furman JM. Psychiatric consequences of vestibular dysfunction. Curr Opin Neurol. 2001; 14
(1):41–6. PMID: 11176216
76. O’Reilly RC, Morlet T, Nicholas BD, Josephson G, Horlbeck D, Lundy L, et al. Prevalence of vestibular
and balance disorders in children. Otol Neurotol. 2010; 31(9):1441–4. https://doi.org/10.1097/MAO.
0b013e3181f20673 PMID: 20729773
77. Lempert T, Olesen J, Furman J, Waterston J, Seemungal B, Carey J, et al. Vestibular migraine: diag-
nostic criteria. J Vestib Res. 2012; 22(4):167–72. https://doi.org/10.3233/VES-2012-0453 PMID:
23142830
78. Furman JM, Marcus DA, Balaban CD. Vestibular migraine: clinical aspects and pathophysiology. Lan-
cet Neurol. 2013; 12(7):706–15. https://doi.org/10.1016/S1474-4422(13)70107-8 PMID: 23769597
79. Pollak L, Klein C, Stryjer R, Kushnir M, Teitler J, Flechter S. Phobic postural vertigo: a new proposed
entity. Isr Med Assoc J. 2003; 5(10):720–3. PMID: 14719468
80. Paiva T, Gaspar T, Matos MG. Sleep deprivation in adolescents: correlations with health complaints
and health-related quality of life. Sleep Med. 2015; 16(4):521–7. https://doi.org/10.1016/j.sleep.2014.
10.010 PMID: 25754385
81. Chung K-F, Cheung M-M. Sleep-wake patterns and sleep disturbance among Hong Kong Chinese ado-
lescents. Sleep. 2008; 31(2):185. PMID: 18274265
82. Schraml K, Perski A, Grossi G, Simonsson-Sarnecki M. Stress symptoms among adolescents: The role
of subjective psychosocial conditions, lifestyle, and self-esteem. J Adolesc. 2011; 34(5):987–96. https://
doi.org/10.1016/j.adolescence.2010.11.010 PMID: 21147499
83. Lund HG, Reider BD, Whiting AB, Prichard JR. Sleep patterns and predictors of disturbed sleep in a
large population of college students. J Adolesc Health. 2010; 46(2):124–32. https://doi.org/10.1016/j.
jadohealth.2009.06.016 PMID: 20113918
84. Humphriss RL, Hall AJ. Dizziness in 10 year old children: an epidemiological study. Int J Pediatr Otorhi-
nolaryngol. 2011; 75(3):395–400. https://doi.org/10.1016/j.ijporl.2010.12.015 PMID: 21239067
85. Lewis DW. Headaches in children and adolescents. Curr Probl Pediatr Adolesc Health Care. 2007; 37
(6):207–46. https://doi.org/10.1016/j.cppeds.2007.03.003 PMID: 17591579
86. Balatsouras DG, Kaberos A, Assimakopoulos D, Katotomichelakis M, Economou NC, Korres SG. Etiol-
ogy of vertigo in children. Int J Pediatr Otorhinolaryngol. 2007; 71(3):487–94. https://doi.org/10.1016/j.
ijporl.2006.11.024 PMID: 17204337
87. Fendrich K, Vennemann M, Pfaffenrath V, Evers S, May A, Berger K, et al. Headache prevalence
among adolescents–the German DMKG headache study. Cephalalgia. 2007; 27(4):347–54. https://doi.
org/10.1111/j.1468-2982.2007.01289.x PMID: 17376112
88. Thijs R, Kruit M, Van Buchem M, Ferrari M, Launer L, Van Dijk J. Syncope in migraine The population-
based CAMERA study. Neurology. 2006; 66(7):1034–7. https://doi.org/10.1212/01.wnl.0000204186.
43597.66 PMID: 16606915

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 14 / 15


Risk factors of vertigo and dizziness in adolescents

89. Peroutka SJ. Dopamine and migraine. Neurology. 1997; 49(3):650–6. PMID: 9305317
90. Milde-Busch A, Blaschek A, Heinen F, Borggräfe I, Koerte I, Straube A, et al. Associations between
stress and migraine and tension-type headache: results from a school-based study in adolescents from
grammar schools in Germany. Cephalalgia. 2011; 31(7):774–85. https://doi.org/10.1177/
0333102410390397 PMID: 21233282

PLOS ONE | https://doi.org/10.1371/journal.pone.0187819 November 13, 2017 15 / 15

Anda mungkin juga menyukai