Pediatric Pulmonology 44:6469 (2009)

Inter- and Intra-Rater Reliability of Neck Circumference Measurements in Children

Robert C. LaBerge, MD,1,2 Jean Philippe Vaccani, MD,2,3 Robert M. Gow, MBBS,2,4 Isabelle Gaboury, MSc,5 Lynda Hoey, RN,5 and Sherri L. Katz, MSc, MDCM2,6*
Summary. Rationale: Increased neck circumference is a risk factor for obstructive sleep apnea in adults. With rising obesity prevalence in children, it may be an important identier of obstructive sleep apnea in children. The reliability of measuring neck circumference in children has not been systematically evaluated. Objective: To determine the inter- and intra-rater reliability of neck circumference measurements in children aged 216 years. Methods: Children aged 216 years with limb fractures were recruited. Neck circumference was measured by three investigators each using two separate unmarked paper tapes in the 25 year age group (N 43), and three separate tapes in the 610 and 1116 year age groups (N 18 and 40). Results: Neck circumference measurements showed excellent inter-rater reliability for children 610 and 1116 years (ICC 0.952 and 0.989). Substantial variation was observed for the 25 year age group (ICC 0.701). Good intra-rater reliability was demonstrated for the three groups (ICC range: 0.776, 0.950). Repeatability coefcients were 2.53.4 cm in the youngest age group and were 1.21.4 cm in the 616 year age group. Conclusion: In children 616 years old, neck circumference shows very good inter and good intra-rater reliability. Multiple measurements are not required for precision and reliability. Pediatr Pulmonol. 2009; 44:6469. 2008 Wiley-Liss, Inc. Key words: obstructive sleep apnea; reliability; children; neck circumference; measurement.

INTRODUCTION

Obstructive sleep apnea (OSA) is a problem that is occurring with increasing frequency in childhood, likely related to the rising prevalence of obesity.13 Signicant complications of untreated OSA include learning difculties.47 behavioral problems,8,9 failure to thrive,10,11 pulmonary hypertension1215 and systemic hypertension.16,17 Early diagnosis can decrease morbidity,16 however the diagnosis of OSA is often delayed by months to years because of inadequate screening.12,18 OSA is difcult to diagnose on clinical grounds alone, as symptoms are poor predictors of OSA.19 There is a poor correlation between the presence of clinical signs and symptoms, and the existence and severity of OSA. There are therefore few tools available to community physicians to help them screen for this disorder. A denitive diagnosis of OSA is established by polysomnography (sleep study). This resource, however, is in limited supply. Overnight oximetry can be helpful as a screening tool, but lacks sensitivity20 and is not always readily available. Community physicians would benet from a simple, reliable and inexpensive clinical tool to screen children at risk for OSA, so that timely referrals can be made in an effort to reduce morbidity. In adults, large neck circumference (NC) identies individuals at increased risk for OSA.2125 NC has not been evaluated as a screening tool for OSA in children.
2008 Wiley-Liss, Inc.

1 Department of Pediatrics, Childrens Hospital of Eastern Ontario, Ottawa, Ontario, Canada. 2

Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada.

Department of Otolaryngology, Childrens Hospital of Eastern Ontario, Ottawa, Ontario, Canada.

4 Department of Cardiology, Childrens Hospital of Eastern Ontario, Ottawa, Ontario, Canada.

Childrens Hospital of Eastern Ontario Research Institute, Clinical Research Unit, Ottawa, Ontario, Canada.
6 Department of Respirology, Childrens Hospital of Eastern Ontario, Ottawa, Ontario, Canada.

The authors have no conicts of interest to declare. Grant sponsor: Childrens Hospital of Eastern Ontario Research Institute Surgical Fund. *Correspondence to: Sherri L. Katz, MSc, MDCM, Childrens Hospital of Eastern Ontario, 401 Smyth Road, Ottawa, Ontario, Canada K1H 8L1. E-mail: skatz@cheo.on.ca Received 17 July 2008; Revised 3 September 2008; Accepted 3 September 2008. DOI 10.1002/ppul.20944 Published online 5 December 2008 in Wiley InterScience (www.interscience.wiley.com).

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This study examines the intra- and inter-rater reliability in the measurement of NC of children between the ages of 216 years.
MATERIALS AND METHODS Study Population

Our study sample consisted of otherwise healthy children between the ages of 216 years, with an upper or lower limb fracture, who presented to the orthopedic clinic at the Childrens Hospital of Eastern Ontario (CHEO) between the months of November 2006 and February 2007. Children with craniofacial anomalies, neurological conditions or underlying cardiac or pulmonary disease were excluded. Children with limb fractures were chosen because this condition is acute and unrelated to upper airway anomalies or body habitus differences that would signicantly impact the measurement exercise. Children were 216 years of age to encompass a broad range of ages for normative data. Approval of the CHEO Research Ethics Board was obtained prior to the commencement of this study.
Recruitment

subject standard deviation. Using the Bland formula for repeatability study,28 the following assumptions were made: (i) a within-subject standard deviation of 10%; (ii) six measurements per subject in the 25 years of age group (nine measurements in the 616 years of age group); (iii) three raters. Using such assumptions, the sample size required to estimate the width of the 95% condence interval within 10% was 39 subjects for the 25 years of age group, and 24 subjects for each of the 610 and 1116 years of age groups.
Analysis

27

Children and parents were informed of the study on presentation to the orthopedic clinic. If interested, full informed consent was obtained by the research coordinator.
Data Collection

NC was measured with the childs head held erect and eyes facing forward, at the most prominent portion of the thyroid cartilage.26 This location was chosen, as it is the most easily palpable landmark of the pediatric airway. NC was measured with a blank disposable paper tape measure. The examiner marked the tape with a thin marker when a measurement was made and handed the tape to the study coordinator. Three independent examiners measured each participants NC. Participants under 6 years of age were measured twice by each examiner. Those participants aged 6 years and older were measured three times by each examiner. The differential number of measurements was based on the assumption that younger participants would tolerate fewer measurements. To avoid recall bias, blank tapes were employed. All tapes were color-coded for each examiner and labeled with a study participant number. After all measurements were made, two independent examiners determined the NC based on the tape measures. These examiners were blinded to the examiners and study participants identities.
Sample Size

ANOVA assumptions need to be met for the intra-class correlation coefcient (ICC) to be appropriate. Study design has provided independent observations, and data were tested for normality. The standard deviation of subject measurements was plotted against the mean to assess whether transformation of the variable was required. Normality of the distribution of the standard deviation of subject measurements was tested using Kolmogorov Smirnov test. The standard deviation within-subject, the repeatability coefcient and the ICC were calculated for the interand intra-rater reliability using a two-way ANOVA. Exploration of the estimates of intra-rater reliability was conducted in a similar fashion within each measurement occasion as well as across both measurement occasions. For inter-rater comparisons reliability was modeled against the rst (single), or average of two, or average of three measurements. This method was used to represent what would be done in a clinical situation.
RESULTS

Inspection of the plots of the subject standard deviation against subject mean for each of the three age groups indicates that the measurement error is independent of the magnitude of the measurement and that the observations do not require mathematical transformation (Fig. 1ac). Normal distribution of the measurement errors was assessed for each age group using KolmogorovSmirnov test (data not shown).
Inter-Rater Reliability

The sample size was chosen to estimate the study reliability coefcient assuming a pre-determined within-

Measurement of the NC in the 610 and 1116 year age groups showed excellent inter-rater reliability with ICCs of 0.95 and 0.99, respectively. The repeatability coefcients indicate that two repeated measurements by different raters will be within 1.39 cm 95% of the time for the 610 year group and within 1.07 cm for the 11 16-year-old group. The 25 year group showed a lower ICC (0.70) and the repeatability coefcient indicated that two raters measurements will differ by at most 2.48 cm,
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Fig. 1. ac: Scatter plot of subject standard deviation (cm) versus mean subject neck circumference (cm). Age group 25 years is depicted in panel a, 610 years in panel b, 1116 years in panel c.

95% of the time (Table 1). For the three study groups, the ICCs obtained using one or an average of two to three measurements concurred with the results obtained using a two-way ANOVA table. Additionally, the results showed that a marginal gain in reliability is obtained when multiple measurements are taken on subjects in the 610 and 1116 year groups (Table 2).
Intra-Rater Reliability

measurement occasions, and between the occasions (Table 3). Because of the small number of individuals in each age group who returned for a second occasion, the ICC point estimates, although good, show poor precision for the between occasion reliability when stratied by age group.

DISCUSSION

Intra-rater variability was analyzed for the rst measurement occasion, the second measurement occasion and as individual variability between the two measurement occasions that were separated by 1 month (Table 3). This provides an estimate of the immediate repeatability and the stability of the measurement reliability over timeallowing for any changes in the subjects that could occur between measurement occasions. On the rst occasion, intra-rater reliability for the 25 year age group was acceptable but showed the lowest ICC and largest repeatability coefcient (Table 1). The 610 and 11 16 year groups demonstrated higher intra-rater reliability (ICC 0.92 and 0.99, respectively). The difference between two repeated measurements of a rater was between 1.12 and 2.56 cm depending on age group. Stratied by raters, the reliability showed excellent stability on both

The pathophysiology of OSA in children, while incompletely understood, is classically related to dynamic narrowing of the upper airway, most often by adenotonsillar hypertrophy, as well as dysfunction of complex neuromotor control mechanisms that regulate upper airway patency.29 However, the etiology and incidence of childhood OSA are evolving to resemble adult disease with the increasing prevalence of childhood obesity.1,3033 In adults, OSA is linked to obesity.3438 In a prospective evaluation of adults, NC corrected for height was actually a better predictor of OSA than symptoms or general obesity, as assessed by body mass index (BMI). This implies that the relationship between OSA and obesity is dependent on the variation in NC and suggests that central fat deposition in the neck and viscera is more contributory than generalized adiposity38,39 to OSA development.

TABLE 1 Inter- and Intra-Rater Reliability Estimated on First Measurement Occasion Repeatability coefcient (cm) ICC (95% CI, average measures)

n Intra-rater Age group 25 610 1116 Inter-rater Age group 25 610 1116

Sw

237 162 387

0.928 0.666 0.440

2.63 1.88 1.25

0.689 (0.576, 0.801) 0.915 (0.860, 0.971) 0.985 (0.978, 0.992)

40 18 43

0.877 0.492 0.379

2.483 1.392 1.074

0.701 (0.554, 0.817) 0.952 (0.898, 0.980) 0.989 (0.981, 0.994)

n, number of subjects; Sw, within subject standard deviation; ICC, intra-class correlation coefcient; CI, condence interval.

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TABLE 2 Precision Gained by Repeat Measurements Inter-rater Age group 25 Single Average 2 Average 3 610 Single Average 2 Average 3 1116 Single Average 2 Average 3 Sw Repeatability coefcient (cm) ICC (95% CI)

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1.202 0.877 N/A 0.450 0.493 0.492 0.417 0.418 0.379

3.403 2.483 N/A 1.404 1.395 1.392 1.180 1.184 1.074

0.541 (0.357, 0.704) 0.701 (0.554, 0.817) N/A 0.953 (0.900, 0.980) 0.950 (0.895, 0.980) 0.952 (0.898, 0.980) 0.987 (0.978, 0.992) 0.986 (0.978, 0.992) 0.989 (0.981, 0.994)

Sw, within subject standard deviation; ICC, intra-class correlation coefcient; CI, condence interval.

As in adults, we therefore predict that NC is a more useful tool than BMI alone for predicting OSA risk in children. Until now, however, the accuracy of this measurement had yet to be assessed in a clinical setting. In addition, no normative data exists for North American children. German data from Feingold and Bossert in 197440 cannot be applied to our population because of the increased obesity in North American children since the time of that study. In this study, we were able to show that there is good inter and intra-rater reliability for the age groups 6 16 years old. Only one measurement per participant is required to gather reliable data. Limitations of this study however, include variability in inter-rater reliability for

the 25 year olds. It is possible that landmarking is more difcult in this age group, as may also be the case in some obese children with short necks. There may also be more difculty with compliance to measurements in the younger children. In addition, the sample size in the 25 and 610 year olds was small, which likely explains the wider condence interval around the estimate of intrarater reliability. However, intra-rater reliability estimates within and between each measurement occasion were found to be good to very good, and similar ndings were seen when the data were stratied by rater. This suggests that a single rater measurement is probably sufcient when estimating NC at a given occasion, in the older age groups. While trained measurers collected the data for

TABLE 3 Intra-Rater Reliability Estimates by Measurement Occasion, Age Group, and Rater Repeatability coefcient (cm) ICC (95% CI)

n Intra-rater 1st occasion By rater Rater 1 Rater 2 Rater 3 Intra-rater 2nd occasion By rater Rater 2 Rater 3 Intra-rater between occasions By rater Rater 2 Rater 3 Intra-rater between occasions By age group 25 610 1116

Sw

262 261 263

0.393 0.563 0.507

1.12 1.59 1.43

0.992 (0.989, 0.995) 0.983 (0.979, 0.989) 0.987 (0.982, 0.991)

50 37

0.441 0.596

1.25 1.67

0.987 (0.977, 0.998) 0.963 (0.927, 0.999)

49 44

0.931 0.723

2.63 2.05

0.941 (0.893, 0.989) 0.964 (0.931, 0.997)

6 8 17

0.904 0.806 0.784

2.558 2.280 2.218

0.776 (0.053, 0.965) 0.650 (0, 0.918) 0.950 (0.868, 0.982)

n, number of subjects; Sw, within subject standard deviation; ICC, intra-class correlation coefcient; CI, condence interval.

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Gozal D. Sleep and neurobehavioral characteristics of 5- to 7-year-old children with parentally reported symptoms of attentiondecit/hyperactivity disorder. Pediatrics 2003;111:554563. Nieminen P, Lopponen T, Tolonen U, Lanning P, Knip M, Lopponen H. Growth and biochemical markers of growth in children with snoring and obstructive sleep apnea. Pediatrics 2002;109:e55. Freezer NJ, Bucens IK, Robertson CF. Obstructive sleep apnoea presenting as failure to thrive in infancy. J Paediatr Child Health 1995;31:172175. Brouillette RT, Fernbach SK, Hunt CE. Obstructive sleep apnea in infants and children. J Pediatr 1982;100:3140. Tal A, Leiberman A, Margulis G, Sofer S, Tal A, Leiberman A, Margulis G, Sofer S. Ventricular dysfunction in children with obstructive sleep apnea: radionuclide assessment. Pediatr Pulmonol 1988;4:139143. Alchanatis M, Tourkohoriti G, Kakouros S, Kosmas E, Podaras S, Jordanoglou JB. Daytime pulmonary hypertension in patients with obstructive sleep apnea: the effect of continuous positive airway pressure on pulmonary hemodynamics. Respiration 2001; 68:566572. Skomro RP, Kryger MH. Clinical presentations of obstructive sleep apnea syndrome. Prog Cardiovasc Dis 1999;41:331340. Marcus CL, Greene MG, Carroll JL. Blood pressure in children with obstructive sleep apnea. Am J Respir Crit Care Med 1998; 157:10981103. Enright PL, Goodwin JL, Sherrill DL, Quan JR, Quan SF. Blood pressure elevation associated with sleep-related breathing disorder in a community sample of white and Hispanic children: the Tucson Childrens Assessment of Sleep Apnea study. Arch Pediatr Adolesc Med 2003;157:901904. Richards W, Ferdman RM. Prolonged morbidity due to delays in the diagnosis and treatment of obstructive sleep apnea in children. Clin Pediatr (Phila) 2000;39:103108. Dixon JB, Schachter LM, OBrien PE. Predicting sleep apnea and excessive day sleepiness in the severely obese: indicators for polysomnography. Chest 2003;123:11341141. Brouillette RT, Morielli A, Leimanis A, Waters KA, Luciano R, Ducharme FM. Nocturnal pulse oximetry as an abbreviated testing modality for pediatric obstructive sleep apnea. Pediatrics 2000;105:405412. Davies RJ, Stradling JR. The relationship between neck circumference, radiographic pharyngeal anatomy, and the obstructive sleep apnoea syndrome. Eur Respir J 1990;3:509514. Katz I, Stradling J, Slutsky AS, Zamel N, Hoffstein V. Do patients with obstructive sleep apnea have thick necks? Am Rev Respir Dis 1990;141:12281231. Hoffstein V, Mateika S. Differences in abdominal and neck circumferences in patients with and without obstructive sleep apnoea. Eur Respir J 1992;5:377381. Davies RJ, Ali NJ, Stradling JR. Neck circumference and other clinical features in the diagnosis of the obstructive sleep apnoea syndrome. Thorax 1992;47:101105. Sharma SK, Kurian S, Malik V, Mohan A, Banga A, Pandey RM, Handa KK, Mukhopadhyay S. A stepped approach for prediction of obstructive sleep apnea in overtly asymptomatic obese subjects: a hospital based study. Sleep Med 2004;5:351357. Hall JG, Froster-Iskenius UG, Allanson JE. The neck. Handbook of normal physical measurements. New York: Oxford University Press; 1989. pp. 216220. Bland JM, Altman DG, Bland JM, Altman DG. Measurement error [see comment] [republished from BMJ. 1996 Jun 29;312(7047):1654; PMID: 8664723]. Br Med J 1996;313:744. [Anonymous]. Bland formula for repeatability study. 2006. Ref Type: Internet Communication.

this study, NC measurement is simple, and can easily be learned and applied in general practice by community caregivers. Reliability data such as the results of this study form the basis of a solid foundation on which to build future research. This information is important for informing sample size, selecting primary outcomes and dening eligibility criteria.41,42 It has proven to be cost-effective in planning clinical trials.43 The data from this study will therefore support the next phase of our research, which aims to develop normative NC data and nally to determine if NC can be used as a risk assessment tool to predict OSA in children. Since our hypothesis is that obesity is responsible for the increasing prevalence of OSA, the failure to demonstrate good inter-rater reliability in the 25 year olds will not affect our future studies, which will focus on children older than 6 years, beyond the age of peak adenoid hypertrophy,44 in whom obesity may be a more signicant contributor to the pathophysiology of OSA. Ultimately, we hope to determine that NC can be used as a screening tool for community physicians to aid in the evaluation of children at increased risk for OSA. This will help decide which children require referral for more urgent polysomnography.
CONCLUSION

10.

11.

12. 13.

14.

15. 16.

17.

In children 616 years old, NC measurements have very good inter- and intra-rater reliability. Multiple repeat measurements are not required for precision and reliability for experienced, trained measurers.
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