JOURNAL READING

Prediction of difficult tracheal intubations in thyroid surgery. Predictive value of

neck circumference to thyromental distance ratio

Disusun oleh:

Delina Widiyanti

1102015053

Pembimbing:

Dr. Rizky Ramadhana, Sp. An

TUGAS KEPANITERAAN KLINIK STASE ANESTESI

FAKULTAS KEDOKTERAN UNIVERSIAS YARSI

RSUD ARJAWINANGUN CIREBON

PERIODE 24 FEBRUARI 2020 –

28 MARET AGUSTUS 2020

ABSTRAK

Pendahuluan
Sulit Intubasi Trakeal (SIT) ikut berkontribusi dalam morbiditas dan mortalitas perioperatif.
Terdapat beberapa hasil penelitian yang saling bertentangan mengenai kriteria resiko yang paling
bisa diprediksi SIT pada pasien yang menjalani operasi thyroid.

Bahan dan Metode

Studi ini merupakan studi observasional prospektif pada 500 konsekutif pasien usia lebih dari sama
dengan 18 tahun untuk kemudian diidentifikasi prediktor SIT mereka. Berat badan, body mass index
(BMI), kemampuan untuk prognati atau protrusi, pergerakan kepala, gerakan membuka mulut,
Mallampati Score, thyromental distance (TMD), neck circumference to thytomental distance ratio
atau rasio lingkar leher dan jarak thyromental (NC/TMD), trakea deviasi pada chest x-ray (CXR),
mediastinal goiter, histologi dan riwayat SIT yang dianggap sebagai prediktor untuk SIT. Uji
korelasi Spearman’s rank dan analisis multiple logistic regression juga dilakukan.

Hasil

SIT berhasil diobservasi pada 9,6% dari seluruh pasien. Dibandingkan dnegan grup pasien tanpa SIT,
grup SIT memiliki nilai median terhadap berat badan, BMI, NC, NC/NMD, Mallampati score, el-
Ganzouri score, insidens mediastinum goiter, lebih tinggi secara signifikan serta lebih lebih rendah
2
terhadap TMD dan gerakan buka mulut. Terdapat korelasi yang signifikan antara BMI ≥ 30 kg/m
dan mallampati score ≥3, (R = 0.124, p = 0.00541), Cormack-Lehane ≥ 3 (R = 0.128, p = 0.00409),
NC ≥ 40 cm (R = 0.376, p<0.001), dan NC/TMD ≥ 5 (R = 0.103, p = 0.0207). Analisis logistic
regression membuktikan bahwa NC ≥ 40 cm pada level goiter, tetapi bukan pada rasio NC/TMD ≥ 5,
adalah prediktor terkuat dari SIT (p<001). Pada area yang terlibat operasi memiliki karakteristik
kurva terhadap NC/TMD lebih baik dibandingan dengan kurva NC.
Sensitivitas dan spesifitas dari NC/TMD juga lebih baik jika dibandingkan dengan

NC. Pada NC 40,00 cm dan NC/TMD 5,85 diperkirakan sebagai cut-off points.

Diskusi

Pada studi ini telah ditemukan bahwa NC adalah prediktor kuat dari SIT. Hasilnya juga
menunjukkan dapat disarankan bahwa NC/TMD bisa digunakan sebagai ukuran untuk
menentukan resiko SIT pada pasien yang akan menjalani operasi thyroid.

PENDAHULUAN

Sulit Intubasi Trakeal (SIT) turut berkontribusi memberikan morbiditas dan mortalitas
perioperatif. Identifikasi kriteria resiko SIT merupakan hal penting guna untuk merencanakan
cara terbaik untuk proses anestesi. Terdapat hasil yang bertentangan tentang kriteria resiko yang
paling bisa di prediksi pada pasien yang akan menjalani operasi thyroid. Lingkar leher atau neck
circumference (NC) terlihat sebagai prediktor yang penting untuk SIT pada populasi ini. Sebuah
studi kohort besar dari pasien-pasien yang menjalani thyroidectomy telah menemukan bahwa
ukuran leher (lingkar dan panjangnya) adalah salah satu dari prediktor utama terpenting SIT pada
operasi thyroid. Nilai cut-off untuk leher belum ditemukan. Hubungan lingkar leher dengan
panjangnya sebagai prediktor terhadap SIT juga belum pernah dievaluasi. Salah satu studi dari
populasi pasien obesitas ditemukan bahwa rasio NC dan jarak thyromental (NC/TMD)
merupakan metode yang lebih baik untuk memprediksikan SIT dibanding dengan indikasi lain
yang sudah ada.

Tujuan dari studi ini adalah untuk mengidentifikasi prediktor SIT dan untuk menguji nilai relatif
dari NC versus NC/TMD dalam memprediksi SIT pada pasien yang akan menjalani operasi
Thyroid.

BAHAN DAN METODE

Penyataan Etik

Studi ptrotokol telah disetujui oleh Komite Etik untuk Riset Klinis di Rumah Sakit Pendidikan
Padova (Reference number: 4133/AO/17) pada 6 April 2017. Studi protokol sesuai dengan the
1964 Declaration of Helsinki dan amandemen terakhirnya. Persetujuan tertulis didapat dari
setiap partisipan yang terlibat pada studi ini. Studi ini merupakan studi non-intervensi klinis,
sesuai peraturan yang ada, bagi pendaftar yang melakukan pendaftaran pada pendaftaran umum
atau sebelum pasien tersebut diikutsertakan tidak dianggap penting. Namun, kami memutuskan
untuk membuka pengajuan bagi para sukarelawan melalui ClinicalTrials.gov (reference number:
NCT03578601) dan telah kami akhiri pada 6 Juli 2018 terkait dengan kesulitan untuk registrasi
akun sampai proses merilis hasil pada website tersebut. Studi ini berlangsung pada 1 September
hingga 17 September 2017. Penulis-penulis mengkonfirmasi bahwa seluruh proses dan yang
terkait dengan percobaan pada intervensi penelitian sudah terdaftar.

Populasi

Pasien-pasien (usia 18 tahun) dijadwalkan operasi thyroid pada Rumah Sakit Pendidikan Padova
(Itali) dipertimbangkan. Pasien direkrut secara konsekutif hingga proses pengukuran sampel
telah dilakukan. Pasien yang memiliki ≥ 1 abnormalitas anatomi, patologi, dan riwayat bedah
sebelumnya menggunakan prosedur intubasi yang tidak standar atau fiberoptic awake intubation
dimasukkan kedalam kriteria eksklusi pada studi ini. Berat badan, BMI, kemampuan untuk
protrusi, pergerakan kepala, gerakan membuka mulut, Mallampati score, NC, TMD, NC/TMD,
deviasi trakea pada CXR, mediastinal goiter, histologi, dan riwayat SIT diukur sebagai prediktor
yang mungkin sebagai prediktor SIT. Analisis melibatkan metode dikotomisasi dan stratifikasi
baik variabel kontinu dan nonkontinu menjadi kategori resiko: BMI (<30 kg/m2, 30 kg/m2);
kemampuan untuk protrusi (bisa/tidak); pergerakan kepala (90 ̊, >90 ̊);gerakan buka mulut (<4
cm, 4 cm); Mallampati score: <III, III; NC (<40 cm, 40 cm); TMD (6.5 cm; >6.5 cm); NC/TMD
(<5; 5); trakea deviasi pada CXR (ada/tidak); mediastinal goiter (ada/tida) histologi
(jinak/ganas); riwayat SIT sebelumnya (ada/tida).

SIT didefinisikan sebagai maneuver yang dilakukan dengan posisi kepala yang tepat dan
external laryngeal manipulation yang menghasilkan: a) sulit laringoskopi (Cormack-Lehane
grade III atau IV); b) lebih dari satu upaya intubasi; c) dibutuhkannya alat dan atau perosedur
tambahan; d) pembatan dan perencanaan ulang.

Evaluasi jalan napas preoperatif dilakukan dengan melibatkan ahli anestesi yang tidak
diikutsertakan pada bagian perioperatif dalam studi ini.

Seluruh ahli anestesi mengikuti pedoman nasional dan internasional untuk tatalaksana SIT tidak
terduga pada dewasa.

Endpoints

Estimasi prevalensi SIT pada populasi pasien yang menjalani operasi thyroid dan identifikasi
prediktor SIT adalah endpoint utama pada studi ini. Pengukuran NC/TMD untuk memprediksi
SIT pada pasien yang menjalani operasi thyroid adalah endpoint kedua pada studi ini.

Analisis Statistik
Perkiraan kekuatan studi dan ukuran sampel brdasarkan asumsi dari perbedaan sebesar 4% insidens
dari sulit intubasi antara populasi umum pasien yang menjalani operasi dan populasi pasien yang
menjalani operasi thyroid. Kami menggunakan sebuah nilai alfa (α) 5%, kekuatan (1-
β error) adalah 95%, a drop out percentage yaitu 5%. Hasil analisisnya mengindikasi bahwa
ukuran sampel dari 515 pasien adalah penting untuk mengestimasi prevalensi SIT pada populasi
pasien operasi thyroid.

Data dari setiap variabel kontinu dianalisis untuk distribusi normal menggunakan tes
Kolmogorov-Smirnov. Hasil dari variabel kontinu dengan distribusi normal dinyatakan dengan
nilai rata-rata (standar deviasi); sedangkan hasil dengan distribusi non normal dinyatakan sebagai
nilai tengah (interquartile range). Analisis data distribusi baik normal atau non normal dilakukan
dengan uji two-tail Student’s t-test dan the Mann-Whitney U test secara respektif. Hasil analisis
pada variabel kategorik dilaporkan sebagai angka (persen) dan dibandingkan dengan beberapa
grup melalui Chi-square tests.

Untuk mengetahui kekuatan dan arah dari asosiasi antara dua variabel, kami menggunakan
Bravais-Pearson’s correlation test untuk variabel dengan distribusi normal dan Spearman’s
rank correlation test untuk variabel yang tidak memenuhi asumsi distribusi normal.

Untuk mengetahui hubungan antara variabel dependen kategorik seperti SIT dan satu atau lebih
variabel independen kategorik seperti SIT prediktor, kami menggunakan analisis logistic
regression untuk menghitung odds ratios (ORs) dengan confidence intervals (CIs) adalah 95%.
Kehadiran multikolinieritas dideteksi dengan variasi faktor inflasi. Menggunakan Akaike
information criterion, kami menunjukkan backward and forward stepwise regression untuk
memilih model terbaik.

Are yang termasuk kedalam kurva karakteristik pengoperasian penerima atau the receiver
operating characteristic (ROC) digunakan untuk menghitung predictive performance dari SIT
prediktor (seperti NC dan NC/TMD). Sensitifitas dan spesifitas digunakan untuk menentukan
cut-off points dari prediksi SIT.

Seluruh analisis statistik menggunakan R version 3.4.0 (2017-04-21). P-values <0.05

menandakan hasil signifikan.
HASIL

Total terdapat 515 pasien yang mengikuti studi ini dari 1 September 2017 sampai 17 September
2018. 15 pasien dieksklusi sebelum analisis final dilakukan (5 pasien menolak untuk pastisipasi,
10 pasien tidak memungkinkan memiliki airway yang baik sesuai standar). 500 pasien terlibat
hingga akhir studi. Data dari pasien-pasien ini diikutsertakan dalam analisis.

Hasil dari karakteristik demografis populasi terlihat pada tabel 1. SIT terjadi pada 9,6% dari
seluruh pasien. Kontrol jalan napas dapat dilakukan dengan sukses menggunakan video
laringoskopi pada 33,3% pasien, dengan Frova catheter pada 31.2%, fiberoptic intubation via i-
gel supraglottic airway pada 18.7%, dan blind intubation pada 16.6% pasien. Tidak terdapat
komplikasi.

Dibandingkan dengan pasien tanpa SIT, grup pasien dengan SIT memiliki nilai median yang lebih
tinggi secara signifikan pada berat badan, BMI, NC, NC/TMD, Mallampati score, el- Ganzouri
score, insidens mediastinal goiter, dan lebih rendah pada TMD dan gerakan buka mulut.

2
Hubungan antara BMI 30 kg/m dan Mallampati score 3 (R = 0.124, p = 0.00541), Cormack-
Lehane 3 (R = 0.128, p = 0.00409), NC 40 cm (R = 0.376, p<0.001), dan and NC/TMD 5 (R =
0.103, p = 0.0207) secara statistik signifikan. Hubungan antara adanya goiter jinak dan deviasi
trakea pada CXR (R = 0.108, p = 0.0159) dan antara goiter jinak dan mediastinal goiter (R =
0.116, p = 0.00928) secara statistik signifikan.

Analisis logistic regression menunjukkan NC 40 cm pada level goiter, namun tidak rasio
NC/TMD 5, adalah prediktor terkuat dari SIT (p<0.001). multikolinearitas tidak terdeteksi
menggunakan variance inflation factors.

Kurva ROC untuk NC/TMD menunjukkan hasil lebih baik dibanding kurva pada NC.

Sensitivitas dan spesifitas NC/TMD juga lebih tinggi dibandingkan dengan NC. Nilai NC 40.00
cm dan nilai NC/TMD 5.85 diprediksi sebagai cut-off points.

DISKUSI
Studi ini menunjukkan insidensi yang tinggi dari SIT pada populasi pasien operasi thyroid.
Hasilnya memperkirakan NC adalah prediktor kuat, namun rasio NC/TMD adalah asesmen
terbaik yang bisa digunakan untuk memprediksi resiko SIT.

Sebuah meta analisis telah menemukan bahwa insidens SIT pada pasien tanpa patologi jalan
napas adalah 6,2% pada pasien normal (tidak termasuk pasien obstetri dan pasien dengan
obesitas). Insidens SIT pada populasi pasien operasi thyroid adalah beragam. Beberapa studi
telah menemukan nilai insidens dari SIT adalah 5,3%-6,8%. Penelitian lain menemukan nilai
yang lebih tinggi yaitu 10%-13,6%. Pada populasi kami pasien operasi thyroid mengalami
peningkatan insidens SIT sebesar 9,6%.

Prediksi SIT memiliki kepentingan klinis yang tinggi, dan studi sebelumnya telah mengevaluasi
faktor resiko untuk SIT pada pasien operasi thyroid. Bertambahnya usia, Mallampati score yang
tinggi, Cormack Grade score III atau IV, menurunnya gerakan buka mulut (<4.4 cm), adanya goiter
ganas dan stenosis trakea (30%) merupakan prediktor independen untuk SIT. Peran dari NC dan
TMD juga telah diteliti. Dua studi mengidentifikasi NC sebagai prediktor independen untuk SIT pada
pasien operasi thyroid tanpa memperhitungkan nilai cut-off untuk kategori resiko. Hanya satu studi
yang menemukan bahwa TMD (<6.5 cm) berhubungan dengan peningkatan resiko SIT pada operasi
thyroid (OR [95%CI]: 2.326 [1.014–5.338], p = 0.046). Studi kami menemukan bahwa NC dan
memiliki perbedaan signifikansi pada SIT dibandingkan dengan pasien tanpa SIT, namun hanya NC
sebagai prediktor independen SIT pada populasi pasien operasi thyroid. Kalezić et al. menyatakan
bahwa peningkatan NC dan hubungan dengan penurunan panjang NC dapat berefek pada resiko SIT
pada operasi thyroid. Rasio NC/TMD dikembangkan oleh by Kim et al. berdasarkan asumsi bahwa
pasien dengan obesitas yang memiliki lingkar leher yang besar dan panjang leher yang pendek dapat
lebih membuat sulit intubasi dibandingkan pasien yang memiliki salah satunya. Obesitas dan
penyakit kelenjar thyroid pada pasien yang sama meningkatkan NC dan NC/TMD. Obesitas
berkontribusi dengan meningkatkan jumlah jaringan lunak leher. Sebuah studi menggunakan
magnetic resonance imaging menemukan bahwa proporsi yang lebih tinggi untuk peningkatan
jumlah jaringan lunak adalah karena peningkatan jumlah lemak, namun hal ini hanya berlaku pada
wanita dengan obesitas dibandingkan pada pria dengan obesitas. Namun, peningkatan jaringan lunak
diikuti oleh deposisi lemak pada leher tidak dapat secara penuh mencatat untuk lebih sulit secara
relatif untuk melihat pita suara selama direct laryngoscopy.
Peningkatan jumlah jaringan lunak pretrakeal pada leher lebih dapat mengganggu laryngoscopy
dengan menurunkan pergerakan anterior struktur faring. Brodsky et al. menemukan bahwa NC yang
lebih besar berhubungan dengan Mallampati score yang lebih besar juga (p = 0.0029) dan Grade 3
views selama laryngoscopy (p = 0.0375). Sama seperti yang kami temukan bahwa obesitas
berhubungan dengan Mallampati dan Cormack-Lehane scores yang lebih tinggi padapasien operasi
thyroid dengan SIT, dibandingkan dengan pasien tanpa SIT. NC, namun bukan TMD, dapat menjadi
indikasi jumlah jaringan lunak leher. TMD adalah mewakilkan ekstensi kepala yang tidak adekuat,
daripada ukuran submandibular space. Namun, NC/TMD daoat menggambarkan distribusi lemak
pada leher lebih baik jika hanya menggunakan NC saja. Studi kami menemukan bahwa NC/TMD
bukan sebagai faktor resiko independen SIT. Namun, hasil dari kurva ROC menganalisis bahwa
NC/TMD 5.85 memiliki nilai prediktif lebih baik dibandingkan NC. Nilai NC/TMD ini berbeda
dengan nilai NC/TMD 5 yang dikemukakan oleh Kim untuk pasien obesitas.

Penyakit kelenjar thyroid juga berkontribusi terhadap pembesaran NC dan SIT. Volume
kelenjar thyroid tidak berhubungan dengan SIT. Namun, goiter (OR [95%CI]: 2.513
[1.139–5.542], p = 0.022) dan berat thyroid (OR [95%CI]: 2.232 [1.075–4.636], p = 0.031)
adalah faktor resiko untuk SIT pada pasien operasi thyroid. Konsisten dengan hasil kami,
invasi dan infiltrasi dari volume kelenjar thyroid, memiliki efek pada leher dan
memprediksi SIT pada pasien operasi thyroid.

Studi ini memiliki beberapa limitasi. Pertama, kami tidak menggunakan Intubation Difficult
Scale untuk menstratifikasi resiko SIT. Keginaan scale ini dapat meningkatkan perbandingan
hasil dari studi ini terhadap hasil dari studi lain. Kedua, tidak ada evaluasi melalui pencitraan
(seperti ultrasound, computed tomography, magnetic resonance imaging scans) selain CRX yang
digunakan untuk menginvestigasi jaringan lunak leher, volume dan struktur kelenjar leher, dan
struktur daerah sekitar leher. CRX hanya metode pencitraan yang digunakan untuk seluruh
pasien yang akan menjalani operasi thyroid. Ketiga, sensitifitas dan spesifitas dinilai melalui satu
pengukuran. Evaluasi kombinasi pengukuran dapat meningkatkan lebih banyak lagi pada
sensitifitas untuk prediksi SIT. Keempat, perhitungan dilakukan oleh tim penelitian; mereka
sangat familiar dengan seluruh tes yang ada. Hasilnya pada praktik klinis dapat berbeda,
terutama ketika dikerjakan dengan tenaga yang kurang berpengalaman.
KESIMPULAN

Studi kami mengkonfirmasi peningkatan resiko SIT pada pasien operasi thyroid. Beberapa
prediktor harus dipertimbangkan pada praktek klinis, seperti penurunan gerakan membuka
mulut, Mallampati score yang tinggi, peningkatan NC, adanya riwayat sulit intubasi dan adanya
mediastinal goiter. Studi ini menemukan bahwa peningkatan NC 40 cm adalah prediktor terkuat
pada SIT. Hasilnya juga menyarankan bahwa NC/TMD 5,85 dapat digunakan sebagai
pengukuran stratifikasi resiko SIT pada pasien yang akan menjalani operasi thyroid. Pengukuran
NC dan NC/TMD dapat digunakan selama evaluasi perioperatif guna untuk memprediksikan SIT
pada pasien yang akan menjalani operasi thyroid.

RESEARCH ARTICLE

Prediction of difficult tracheal

intubations in thyroid surgery.
Predictive value of neck
circumference to thyromental distance
ratio
1☯ 1‡
Alessandro De Cassai *, Francesco Papaccio , Giorgia
1‡ 1‡ 2
Betteto , Chiara Schiavolin , Maurizio Iacobone ,
1☯
Michele Carron

1 Department of Medicine—DIMED, Section of Anesthesiology and Intensive Care,

a1111111111 University of Padova, Padova, Italy, 2 Department of Surgery, Oncology and
Gastroenterology, Endocrine Surgery Unit, University of Padua, Padua
a1111111111
a1111111111
☯ These authors contributed equally to this work.
a1111111111 ‡ These authors also contributed equally to this work. * alessandro.decassai@gmail.com

Abstract
Received: November 22, 2018

Accepted: February 12, 2019

OPEN ACCESS Published: February 27, 2019
Citation: De Cassai A, Papaccio F, Copyright: © 2019 De Cassai et al. This is an open access article distributed under the terms of the
Betteto G, Schiavolin C, Iacobone M, Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in
Carron M (2019) Prediction of difficult any medium, provided the original author and source are credited.
tracheal intubations in thyroid surgery.
Predictive value of neck circumference to Data Availability Statement: All relevant data are within the manuscript and its
thyromental distance ratio. PLoS ONE Supporting Information files.
14(2): e0212976.
https://doi.org/10.1371/journal. Funding: The author(s) received no specific funding for this work.
pone.0212976
Competing interests: The authors have declared that no competing interests exist.
Editor: Andrea Ballotta, IRCCS
Policlinico S.
Donato, ITALY

Introduction
Difficult tracheal intubation
(DTI) contributes to
perioperative morbidity and
mortality. There are conflicting
study results about the most
predictive DTI risk criteria in
patients undergoing thyroid
surgery.
Materials and methods
We conducted a prospective
observational study on 500
consecutive patients aged
�18 years to identify
predictors for DTI. Body
weight, body mass index
(BMI), inability to prog-nath,
PLOS ONE | https://doi.org/10.1371/journal.pone.0212976 February 27, 2019
head movement, mouth opening, Mallampati score, neck circumference
(NC), thyro-mental distance (TMD), neck circumference to thyromental
distance ratio (NC/TMD), tracheal deviation apparent on chest x-ray,
mediastinal goiter, histology and history of DTI were measured as possible
predictors of DTI. Spearman’s rank correlation test and multiple logistic
regression analysis were performed.
Results
DTI was observed in 9.6% of all patients. Compared with the group of patients
without DTI, the group of patients with DTI had significantly greater median
values for body weight, BMI, NC, NC/TMD, Mallampati score, el-Ganzouri score,
incidence of mediastinal goiter, and had reduced TMD and mouth opening.
2
Significant correlations between BMI �30 kg/m and the Mallampati score �3
(R = 0.124, p = 0.00541), Cormack-Lehane �3 (R = 0.128, p =
0.00409), NC �40 cm (R = 0.376, p<0.001), and NC/TMD �5 (R = 0.103, p =
0.0207) were found. The logistic regression analysis revealed that an NC �40
cm at the goiter level, but not an NC/TMD ratio �5, was the strongest predictor
of DTI (p<0.001). The area under the receiver operating characteristic curve for
NC/TMD was better than the curve for NC. The
1/1
 Difficult tracheal intubation in thyroid surgery

sensitivity and specificity of NC/TMD were also greater, compared with NC. An NC of
40.00 cm and an NC/TMD of 5.85 were the estimated cut-off points.

Discussion
This study found that NC was a strong predictor of DTI. The results also suggested that
NC/ TMD could be used as a measure to stratify the risk of DTI in patients undergoing
thyroid surgery.

Introduction
Difficult tracheal intubation (DTI) contributes to perioperative morbidity and mortality [1,2].
Identification of DTI risk criteria is essential while planning the best way to proceed with anes-
thesia [1]. There are conflicting study results about the most predictive DTI risk criteria in
patients undergoing thyroid surgery [3–7]. Neck circumference (NC) seems to be an impor-
tant predictor for DTI in this population of patients [5–7]. A study of a large cohort of patients
undergoing thyroidectomy found that the size of the neck (circumference and length) is one of
most important independent predictors of DTI in thyroid surgery [5]. Cut-off values for neck
width have not been established. The relationships between neck circumference and length as
predictors of DTI have also not been evaluated [5]. One study of a population of patients with
obesity found that the NC to thyromental distance (NC/TMD) ratio is a better method for pre-
dicting DTI than other established indices [8].
The aim of the study was to identify predictors for DTI and to examine the relative
value of NC versus NC/TMD for predicting DTI in patients undergoing thyroid surgery.

Materials and methods

Ethical statement
The study protocol was approved by the Ethics Committee for Clinical Research of the
Padova Medical Hospital (Reference number: 4133/AO/17) on April 06th, 2017. The study
protocol was in accordance with the 1964 Declaration of Helsinki and its later amendments.
Informed written consent was obtained from each participant included in the study. This is a
non-inter-ventional (observational) clinical study, based on routine care, for which the
registration at public registry is not necessary at or before the time of first patient enrollment.
However, we decided for a voluntary submission of our study at ClinicalTrials.gov (reference
number: NCT03578601) that was concluded on July 06th, 2018 due to difficulties encountered
from account creation to final record release at Clinicaltrials.gov. The study started on
September 01st, 2017 and ended on September 17th, 2018. The authors confirm that all
ongoing and related trials for this intervention are registered.

Population
Patients (� 18 years of age) scheduled for thyroid surgery at University Medical Hospital of
Padova (Italy) were considered. Patients were recruited consecutively until the sample size
was achieved. Patients with one or more anatomical abnormalities, pathologies, and previous
sur-gery suggesting use of a none-standard approach or fiberoptic awake intubation were
excluded from the study [9]. Body weight, body mass index (BMI), inability to prognath, head
move-ment, mouth opening, Mallampati score, NC, TMD (Fig 1), NC/TMD, tracheal deviation

PLOS ONE | https://doi.org/10.1371/journal.pone.0212976 February 27, 2019 2 / 12

 Difficult tracheal intubation in thyroid surgery

Fig 1. NC measurement and TMD measurement: NC measurement and TMD measurement.

https://doi.org/10.1371/journal.pone.0212976.g001

apparent on chest x-ray (radiograph) (CXR), mediastinal goiter (Fig 2), histology and history
of DTI were measured as possible predictors of DTI. The analysis included dichotomization
and stratification of continuous and non-continuous variables into “risk” categories: BMI
(<30 kg/m2, �30 kg/m2) [10]; inability to prognath (yes/no); head movement (�90˚, >90˚);
mouth opening (<4 cm, �4 cm); Mallampati score: <III, �III; NC (<40 cm, �40 cm) [11];
TMD (�6.5 cm; >6.5 cm); NC/TMD (<5; �5) [8]; tracheal deviation at CXR (yes/no); medi-
astinal goiter (yes/no) histology (benign/malignant); history of DTI (yes/no) [12].
DTI was defined as maneuver performed with a correct head position and
external laryn-geal manipulation resulting in: a) difficult laryngoscopy (Cormack-
Lehane grade III or IV); b) more than one intubation attempt; c) needing of no
standard devices and/ or procedures; d) withdrawal and procedure re-planning [9].

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 Difficult tracheal intubation in thyroid surgery

Fig 2. Mediastinal goiter and tracheal deviation at CXR: Asterisks: Mediastinal goiter shadow, arrow: Tracheal deviation.
https://doi.org/10.1371/journal.pone.0212976.g002

Preoperative airway evaluation was performed by the attending

anesthesiologist not involved in the perioperative part of this study.
All anesthesiologists followed the national [9] and the international [13]
guidelines for management of unanticipated DTI in adults.

Endpoints
The estimation of the prevalence of DTI in a population of patients undergoing thyroid sur-
gery and the identification of predictors for DTI were the main endpoints of the study. The

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 Difficult tracheal intubation in thyroid surgery

examination of NC/TMD for predicting DTI in patients undergoing thyroid surgery

was the secondary endpoint of the study.

Statistical analysis
The estimates of study power and sample size were based on an assumption of a difference
of 4% in the incidence of difficult intubation between the general population of patients
undergo-ing surgery [1] and the population of patients undergoing thyroid surgery [4], We use
an α-value of 5%, a power (1-β error) of 95%, a drop out percentage of 5%. The results of the
analy-sis indicated that a sample size of 515 patients was necessary to estimate the
prevalence of DTI in a population of patients undergoing thyroid surgery.
The data for each continuous variable were analyzed for a normal distribution using the
Kolmogorov-Smirnov test. Results for continuous variables with normal distributions were
expressed as mean (standard deviation) values; those with non-normal distributions were
expressed as median (interquartile range) values. Analysis of data with a normal or a non-
nor-mal distribution was performed using the two-tail Student’s t-test and the Mann-Whitney U
test, respectively. The results for analyses of categorical variables were reported as numbers
(percentages) and were compared between groups using Chi-square tests.
To determine the strength and direction of association between two variables, we used the
Bravais-Pearson’s correlation test for variables with a normal distribution and Spearman’s rank
correlation test for variables that did not meet the assumptions of a normal distribution.
To determine the relationships between the dependent categorical variable (i.e.,
DTI) and one or more independent categorical variables (i.e., DTI predictors), we
performed a multiple logistic regression analysis to calculate odds ratios (ORs) with
95% confidence intervals (CIs). The presence of multicollinearity was detected
using variance inflation factors. Using the Akaike information criterion, we
performed backward and forward stepwise regression to select the best model.
The area under the receiver operating characteristic (ROC) curve was used to examine the
predictive performance of DTI predictors (i.e. NC and NC/TMD). The sensitivity and specific-ity
plots were used to determine the cut-off points for DTI prediction [8,11].
All statistical analyses were performed using R version 3.4.0 (2017-04-21). P-
values <0.05 were considered to indicate a statistically significant result.

Results
st th
A total of 515 patients were enrolled in this study from 1 September 2017 to 17
September 2018. Fifteen patients were excluded before the final analysis was
performed (5 patients refused to participate, 10 patients had no standard approach
to the airway available). The remaining 500 patients completed the study (Fig 3). The
data from these patients were included in the analysis.
The results for the population’s demographic characteristics are presented in Table 1. DTI
occurred in 9.6% of all patients. Airway control was successfully achieved using videolaryngo-
scopy in 33.3%, a Frova catheter in 31.2%, fiberoptic intubation via i-gel supraglottic airway in
18.7%, and blind intubation in 16.6% of the patients. There were no complications.
Compared with the group of patients without DTI, the group of patients with DTI
had sig-nificantly greater median values for body weight, BMI, NC, NC/TMD,
Mallampati score, el-Ganzouri score, incidence of mediastinal goiter, and had
reduced TMD and mouth opening Table 1.
2
The correlations between BMI �30 kg/m and the Mallampati score �3 (R = 0.124,
p = 0.00541), Cormack-Lehane �3 (R = 0.128, p = 0.00409), NC �40 cm (R = 0.376, p<0.001),

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 Difficult tracheal intubation in thyroid surgery

Fig 3. TREND flowchart.

https://doi.org/10.1371/journal.pone.0212976.g003

and NC/TMD �5 (R = 0.103, p = 0.0207) were statistically significant. The

correlations between the presence of benign goiter and tracheal deviation on CXR
(R = 0.108, p = 0.0159) and between benign goiter and mediastinal goiter (R =
0.116, p = 0.00928) were statistically significant.
The logistic regression analysis revealed that an NC �40 cm at the goiter level,
but not an NC/TMD ratio �5, was the strongest predictor of DTI (p<0.001).
Multicollinearity was not detected using variance inflation factors Table 2.
The ROC curve for NC/TMD was better than the curve for NC (Fig 4).

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 Difficult tracheal intubation in thyroid surgery

Table 1. Characteristics patients.

Variable Patients
No DTI DTI
(n = 452) (n = 48)
Sex Male 100 (22.1) 14 (29.2)
Female 352 (77.9) 34 (70.8)
Age (y) 53.0 [43.00, 64.00] 46.61 [49.75, 62.25]
Weight (kg) 67.0 [60.0, 78.2] 75.0 [68.7, 85.0]
Height (m) 1.65 [1.60, 1.72] 1.68 [1.62, 1.73]
2
BMI (kg/m ) 24.2 [22.0, 27.2] 27.3 [24.4, 30.0]
2
BMI �30 kg/m 55 (12.2) 13 (27.1)
NC (cm) 36.5 [34.0, 40.0] 41 [40.0, 42.2]
NC �40 cm 135 [29.9] 37 [77.1]
TMD (cm) 8.0 [6.5, 9.0] 7.0 [6.0, 8.0]
TMD �6.5 93 (20.6) 18 (37.5)
NC/TMD 4.7 [3.9, 5.7] 6.0 [4.9, 7.0]
NC/TMD �5 265 (58.6) 39 (81.29
Mouth opening <4 cm 38 (8.4) 13 (27.1)
Inability to prognath 30 (6.69 3 (6.2)
Neck movement �90˚ 84 (18.69 14 (29.29
Mallampati score 1.0 [1.0, 2.0] 2.0 [2.0, 3.0]
Mallampati score �III 47 (10.4) 18 (37.5)
Past difficult intubation 2 (0.4) 4 (8.3)
el-Ganzouri score 1.0 [0.0, 2.0] 2.0 [1.0, 3.2]
el-Ganzouri score �4 35 (7.7) 13 (27.1)
Tracheal deviation at CXR 91 (20.1) 13 (27.1)
Mediastinal goiter 44 (9.7) 13 (27.1)
Malignancy at HP 118 (26.1) 15 (31.2)

The results for continuous variables are expressed as median (interquartile range) values. Categorical
variables are reported as numbers (percentages). Abbreviations: DTI: difficult tracheal intubation;
BMI: body mass index; NC: neck circumference; TMD: thyromental distance; NC/TMD: NC to
thyromental distance ratio; CXR: chest x-ray (radiograph); HP: histopathology

https://doi.org/10.1371/journal.pone.0212976.t001

The sensitivity and specificity of NC/TMD were also greater, compared with NC. An
NC of 40.00 cm and an NC/TMD of 5.85 were the estimated cut-off points (Fig 5).

Discussion
This study revealed a high incidence of DTI in this population of patients undergoing
thyroid surgery. The results indicated that NC was a strong predictor, but that the
NC/TMD ratio was the best assessment to use to predict the risk of DTI.
A meta-analysis found that the overall incidence of DTI in patients with no airway
pathol-ogy is 6.2% for normal patients (excluding obstetric patients and patients with
obesity) [14]. The incidence of DTI in populations of patients undergoing thyroid surgery
varies. Some stud-ies found similar values for incidence of DTI (5.3% to 6.8%) [3,5,15–
18]. Other studies found higher values (10% to 13.6%) [4,6,7,19,20]. Our population of
patients undergoing thyroid sur-gery had an increased incidence of DTI (9.6%).
Prediction of DTI has high clinical importance, and previous studies have evaluated risk
factors for DTI in patients undergoing thyroid surgery [3,5–7,19,20]. Increased age, a high

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 Difficult tracheal intubation in thyroid surgery

Table 2. Multiple linear regression analysis to explain the relationship between DTI and variables considered.
Variable Regression Model Fitted regression model
VIF OR 95%CI P-value OR 95%CI P-value
Sex (male) 1.268 1.56 0.68–3.52 0.288
2
BMI �30 kg/m 1.190 1.23 0.53–2.88 0.626
DTM �6.5 1.367 1.24 0.53–2.87 0.622
NC/TMD 1.191 1.52 0.62–3.66 0.354
Mouth opening <4 cm 1.210 2.67 1.06–6.74 0.037 2.97 1.24–7.10 0.014
Inability to prognath 1.248 0.39 0.08–2.12 0.244
Neck movement �90˚ 1.191 0.85 0.37–1.96 0.706
NC �40 cm 1.413 7.25 3.01–17.5 <0.001 6.68 3.12–14.3 <0.001
Mallampati �III 1.222 2.23 1.03–6.01 0.042 2.19 1.03–4.76 0.047
Past difficult intubation 1.231 20.9 1.91–229 0.012 12.6 1.55–103 0.017
Tracheal deviation at CXR 1.171 0.65 0.27–1.54 0.329
Mediastinal goiter 1.246 3.03 1.19–7.67 0.019 2.66 1.16–6.10 0.021
Malignancy at HP 1.157 1.95 0.89–4.27 0.095 1.73 0.82–3.61 0.144

The results for continuous variables are expressed as median (interquartile range) values. Categorical variables are reported as numbers
(percentages). Abbreviations: DTI: difficult tracheal intubation; BMI: body mass index; NC: neck circumference; TMD: thyromental distance;
NC/TMD: NC to thyromental distance ratio; CXR: chest x-ray (radiograph); HP: histopathology

https://doi.org/10.1371/journal.pone.0212976.t002

Mallampati score, a Cormack Grade score III or IV, a reduced mouth opening (<4.4 cm), a
cancerous goiter and a tracheal stenosis (�30%) are independent predictors for DTI [3,7,20].
The role of NC and TMD have also been investigated [5,6,18]. Two studies identified NC as
an independent predictor for DTI in thyroid surgery without estimating cut-off values for risk
categories [5,6]. Only one study found that TMD (<6.5 cm) was associated with an increased

Fig 4. Receiver operating characteristic (ROC) curves with area under ROC curve (AUC) values (95% confidence intervals) for neck
circumference (NC) measurement and the ratio of the NC to thyromental distance (NC/TMD).
https://doi.org/10.1371/journal.pone.0212976.g004

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 Difficult tracheal intubation in thyroid surgery

Fig 5. Values for sensitivity and specificity for neck circumference (NC) measurement with a 40-cm cut-off value and ratio of the NC to
thyromental distance (NC/ TMD) test with a cut-off value of 5.85.
https://doi.org/10.1371/journal.pone.0212976.g005

risk (OR [95%CI]: 2.326 [1.014–5.338], p = 0.046) of DTI in thyroid surgery patients [18]. Our
study found that both NC and TMD differed significantly in DTI compared with patients
without DTI, but only NC was an independent predictor of DTI in thyroid surgery patients.
Kalezić et al. suggested that an increased NC and an associated reduced NC length could affect
the risk of DTI in thyroid surgery patients [5]. The NC/TMD ratio was developed by Kim et al.
based on the assumption that patients with obesity who had both a large neck circumference
and a short neck length might be more difficult to intubate than patients with only a large neck
circumference or a short neck [8]. Obesity and thyroid gland disease in the same patient
increase NC and NC/TMD. Obesity contributes by increasing the amount of neck soft tissue
[8,21]. A study using magnetic resonance imaging found that the greater proportion of
increased soft tissue is due to increased fat, but this change is more likely to be present in
women with obesity than in men with obesity [22]. However, the increased soft tissue sus-
tained by fat deposition in the neck does not completely account for the relatively poorer abil-
ity to view the vocal cords during direct laryngoscopy. The increased amount of pre-tracheal
neck soft tissue most likely impairs laryngoscopy by reducing the anterior mobility of pharyn-
geal structures [21]. Brodsky et al. found that a larger NC is associated with a higher Mallam-
pati score (p = 0.0029) and Grade 3 views during laryngoscopy (p = 0.0375) [11]. Similarly, we
found that obesity was associated with higher Mallampati and Cormack-Lehane scores at lar-
yngoscopy in patients undergoing thyroid surgery with DTI, compared with those with no
DTI. NC, but not TMD, may be an indication of the amount of neck soft tissue. TMD is a sur-
rogate for inadequate head extension, rather than the size of the submandibular space [23].
However, NC/TMD might represent the distribution of fat in the neck better than NC alone
[8]. Our study found that NC/TMD was not an independent risk factor for DTI. However, the
results of the ROC curve analysis indicated that an NC/TMD �5.85 had better predictive per-
formance than NC. This NC/TMD value differs from the value of NC/TMD �5 proposed by
Kim for patients with obesity [8].
Thyroid gland disease also contributes to NC enlargement and DTI. Thyroid gland volume
is not correlated with DTI [17], However, goiter (OR [95%CI]: 2.513 [1.139–5.542], p = 0.022)

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 Difficult tracheal intubation in thyroid surgery

and thyroid weight (OR [95%CI]: 2.232 [1.075–4.636], p = 0.031) are independent risk
factors for DTI in thyroid surgery patients [18]. Consistent with our results, invasion and
infiltration of adjacent tissues by thyroid gland disease, more than expansion of thyroid gland
volume, affects the neck and predicts DTI in patients undergoing thyroid surgery [17].
This study had some limitations. First, we did not use an Intubation Difficult Scale to
strat-ify the risk of DTI [24]. Use of this scale would have increased the comparability of
the results of this study to the results of other studies. Second, no imaging evaluation
(e.g., ultrasound, computed tomography, magnetic resonance imaging scans) other than
CRX was used to inves-tigate the neck soft tissue, volume and structure of the gland,
and the surrounding structures. CRX was the only imaging method used for all patients
undergoing thyroid surgery. Third, sensitivity and specificity was assessed for single
measures. Evaluation of combinations of mea-sures might further increase the sensitivity
for prediction of DTI. Fourth, examinations were performed by the study team; they were
very familiar with all tests performed. The results in clinical practice might differ,
especially when rarely employed measures are used by less expe-rienced providers.

Conclusions
Our study confirms the increased risk of DTI in patients undergoing thyroid surgery.
Several predictors should be considered in clinical practice, such as reduced mouth
opening, a high Mallampati score, an increased NC, a history of difficult intubation
and a mediastinal goiter. This study found that increased NC �40 cm was the
strongest predictor of DTI. The results also suggested that NC/TMD �5.85 could be
used as a measure to stratify the risk of DTI in patients undergoing thyroid surgery.
Measurement of NC and NC/TMD should be considered during preoperative
evaluation in order to predict DTI in patients undergoing thyroid surgery.

Supporting information
S1 Checklist. Trend checklist for the “Prediction of difficult tracheal intubations in thy-
roid surgery. Predictive value of neck circumference to thyromental distance ratio” study.
(PDF)

S1 Protocol. Original protocol for the “Prediction of difficult tracheal

intubations in thy-roid surgery. Predictive value of neck circumference to
thyromental distance ratio” study in Italian language.
(PDF)
S2 Protocol. English translation of original protocol for the “Prediction of difficult tra-
cheal intubations in thyroid surgery. Predictive value of neck circumference to thyromental
distance ratio” study.
(PDF)
S1 Database. Study database.
(XLSX)

Author Contributions
Conceptualization: Alessandro De Cassai.
Data curation: Alessandro De Cassai, Francesco Papaccio, Michele Carron.
Formal analysis: Michele Carron.

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 Difficult tracheal intubation in thyroid surgery

Funding acquisition: Michele Carron.

Investigation: Giorgia Betteto, Chiara Schiavolin.
Methodology: Alessandro De Cassai.
Project administration: Alessandro De Cassai, Maurizio Iacobone.
Resources: Alessandro De Cassai.
Supervision: Alessandro De Cassai, Maurizio Iacobone.
Writing – original draft: Alessandro De Cassai, Michele Carron.
Writing – review & editing: Alessandro De Cassai, Michele Carron.

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