Neck Circumference as a Screening Measure for Identifying Children With High Body Mass Index Olubukola O.

Nafiu, Constance Burke, Joyce Lee, Terri Voepel-Lewis, Shobha Malviya and Kevin K. Tremper Pediatrics 2010;126;e306; originally published online July 5, 2010; DOI: 10.1542/peds.2010-0242

The online version of this article, along with updated information and services, is located on the World Wide Web at:
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PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright 2010 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

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Neck Circumference as a Screening Measure for Identifying Children With High Body Mass Index
WHATS KNOWN ON THIS SUBJECT: BMI is a poor descriptor of central adiposity, a well-described risk factor for poor cardiometabolic phenotype. Other surrogates of body fatness are being investigated. WHAT THIS STUDY ADDS: The authors provide data on the usefulness of neck circumference measurements for identifying children with high BMI. They provide age- and gender-specic neck circumference cut points for identifying children who are overweight or obese.
AUTHORS: Olubukola O. Nau, MD,a Constance Burke, BSN,a Joyce Lee, MD, MPH,b Terri Voepel-Lewis, MSN,a Shobha Malviya, MD,a and Kevin K. Tremper, MDa
Departments of aAnesthesiology and bPediatric Endocrinology, University of Michigan, Ann Arbor, Michigan KEY WORDS neck circumference, childhood obesity, body mass index, central adiposity ABBREVIATIONS WCwaist circumference NCneck circumference ROCreceiver operating characteristic AUCarea under the curve LRpositive likelihood ratio LRnegative likelihood ratio www.pediatrics.org/cgi/doi/10.1542/peds.2010-0242 doi:10.1542/peds.2010-0242 Accepted for publication Apr 8, 2010 Address correspondence to Olubukola O. Nau, MD, 1500 E Medical Centre Dr, University of Michigan Health System, Room UH 1H247, Ann Arbor, MI 48109-0048. E-mail: onau@med.umich.edu PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright 2010 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no nancial relationships relevant to this article to disclose.

abstract
OBJECTIVES: Overweight in children is most commonly described by using BMI. Because BMI does not adequately describe regional (central) adiposity, other indices of body fatness are being explored. Neck circumference (NC) is positively associated with obstructive sleep apnea, diabetes, and hypertension in adults. NC also has positive correlation with BMI in adults. The possible role of NC in screening for high BMI in children is not well characterized. The aims of this investigation were to examine the correlation between BMI and NC in children and to determine the best NC cutoff that identies children with high BMI. METHODS: Children who were aged 6 to 18 years and undergoing elective noncardiac surgeries were the subjects of this study. Trained research assistants collected clinical and anthropometric data from all patients. We calculated Pearson correlation coefcients between NC and other indices of obesity. We then determined by receiver operating characteristic analyses the optimal NC cutoff for identifying children with high BMI. RESULTS: Among 1102 children, 52% were male. NC was signicantly correlated with age, BMI, and waist circumference in both boys and girls, although the correlation was stronger in older children. Optimal NC cutoff indicative of high BMI in boys ranged from 28.5 to 39.0 cm. Corresponding values in girls ranged from 27.0 to 34.6 cm. CONCLUSIONS: NC is signicantly correlated with indices of adiposity and can reliably identify children with high BMI. NC is a simple technique that has good interrater reliability and could be used to screen for overweight and obesity in children. Pediatrics 2010;126:e306e310

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Childhood overweight and obesity remains a worldwide public health concern.1 The most widely used tool for dening overweight and obesity in both adults and children is BMI, which is dened as an individuals weight in kilograms divided by the square of their height in meters (BMI kg/m2).2 Despite the ease of use and popularity of BMI as an anthropometric tool, it is becoming increasingly clear that it is not a good proxy for regional adiposity.3 Regional deposition of fat, especially in the upper body segment, is a better predictor of some obesityrelated complications, such as hypertension, diabetes, and heart disease.4 Many studies have demonstrated the value of waist circumference (WC) as an index of central obesity.5,6 Other investigators have shown that WC, either singly or in combination with BMI, may have a stronger relation to some health outcomes than BMI alone.7,8 Neck circumference (NC) has also been used as a potential proxy for obesity and cardiovascular disease in adults.9,10 Very few investigators11 have attempted to use NC to screen for high BMI in children; therefore, the objectives of this study were to examine the correlation between NC and BMI in children, to examine the ability of NC to identify correctly children with high BMI, and to determine the best NC cut point for identifying children of various ages as overweight/obese. Our a priori hypothesis was that a signicant proportion of children with high NC would also be overweight or obese.

cause of increased difculty with compliance while measuring anthropometric parameters in younger children. In addition, previous investigators12 showed that landmarking is more difcult in children who are younger than 5, leading to poor interrater and intrarater reliability of NC measurements. Children with goiter or other neck masses, neck deformity, or tracheostomy or cervical collar were excluded from this study. Measurements Trained research assistants took all clinical and anthropometric measurements. Height was measured to the nearest 0.1 cm by using a wallmounted stadiometer with the patients shoeless and head held in Frankfurt horizontal plane. Body weight was measured, to the nearest 0.1 kg, by using a calibrated electronic weighing scale with patients lightly clad in hospital gowns. NC was measured by using a exible tape, with the children in the standing position, head held erect, at the level of the thyroid cartilage. WC was measured (to the nearest 0.1 cm) with the children standing, at the end of normal expiration, by using an inelastic tape at a point midway between the inferior margin of the lowest rib and the iliac crest. Measurements were obtained with the tape snug but not compressing the skin. BMI was calculated for all patients and was converted to age- and gender-specic percentiles according to the 2000 Centers for Disease Control and Prevention growth curves.13 Operational Denition of Terms Children with a BMI 85th percentile were classied as having normal weight, whereas children with BMI 85th percentile were classied as being overweight/obese.13 We also stratied children into 2 age groups: young children (age 10 years) and older children (age 10 years).

Statistical Analysis Data analyses were performed with SPSS 17.0 for Windows and MedCalc 7.4.1.1 (written by Frank Schoonjans, Mariakerke, Belgium). Means and SDs of age and anthropometric variables were compared along gender lines. Pearson correlation coefcient was used to explore the association between NC and other continuous variables, such as age, WC, BMI, and baseline blood pressure. Receiver operating characteristic (ROC) analyses14 were used to determine the predictive validity of NC as well as evaluate optimal cutoff values for identifying overweight or obese children. ROC curves determine the discriminatory power of a screening measure for correctly identifying individuals on the basis of their classication by a reference test. The ROC curve is a plot of true-positive rate (sensitivity) against the false-positive rate (1 specicity). A good test will have its ROC curve skewed to the upper left corner.15 The area under the curve (AUC) describes the probability that a test will correctly identify a pair of patients who do and do not have a disease and were randomly selected from a population; a perfect score will have an AUC of 1, whereas an AUC of 0.5 means that the test performs no better than chance. For this study, patients with true-positive results were those with high BMI and high NC. Patients with false-positive results were those with high NC and low BMI. Patients with false-negative results were those with low NC and high BMI. Sensitivity was calculated as true-positive results/ (true-positive results false-negative results); specicity was calculated as true-negative results/(true-negative results false-positive results). Cutoff values and the corresponding AUC as well as the likelihood ratios (positive [LR] and negative [LR]) for NC that were predictive of overweight/
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METHODS
After institutional review board approval, we prospectively recruited 1102 children who were aged 6 to 18 years and undergoing elective, noncardiac surgical procedures at the Mott Childrens Hospital, University of Michigan, for inclusion in this study. We chose a lower cutoff age of 6 years bePEDIATRICS Volume 126, Number 2, August 2010

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TABLE 1 Baseline Characteristics of the Children According to Age Group, BMI Category, and
Gender
Variable Young Children (Age 10 y) Normal BMI (n 404) Boys Age, y Weight, kg Height, cm BMI, kg/m2 WC, cm NC, cm SBP, mm Hg DBP, mm Hg Girls Age, y Weight, kg Height, cm BMI, kg/m2 WC, cm NC, cm SBP, mm Hg DBP, mm Hg 7.7 1.5 26.6 9.3 127.0 14.4 16.4 1.4 59.1 6.3 28.1 1.9 101.3 14.2 60.9 8.3 7.8 1.4 25.5 6.3 126.9 11.8 15.7 1.6 58.2 6.0 26.9 2.0 103.0 11.9 61.7 8.3 High BMI (n 248) 7.6 1.4 37.6 13.2 130.7 14.2 23.1 4.7 73.7 15.0 31.2 4.4 108.4 14.2 63.4 9.3 7.7 1.4 36.9 13.4 130.0 13.9 22.8 4.4 73.3 13.4 29.9 3.0 109.0 14.2 63.8 8.1 P Older Children (Age 10 y) Normal BMI (n 282) 14.0 2.1 51.4 12.2 163.2 13.7 19.1 2.4 73.4 8.6 33.1 3.1 115.2 13.0 64.9 9.3 14.3 2.1 48.9 10.6 156.1 13.5 19.4 2.6 72.2 8.0 30.9 2.3 110.7 12.7 65.7 8.8 High BMI (n 168) 13.7 1.9 77.6 21.4 164.4 12.9 28.9 5.8 96.9 14.6 37.6 4.1 118.7 14.8 66.5 8.7 13.7 2.1 69.3 17.7 158.6 11.0 28.4 5.7 93.3 15.8 34.3 3.5 118.0 11.7 67.9 9.6 P

.510 .001 .029 .001 .001 .001 .001 .022 .967 .001 .062 .001 .001 .001 .001 .055

.236 .001 .199 .001 .001 .001 .041 .172 .050 .001 .118 .001 .001 .001 .001 .078

itively correlated with blood pressure in both genders. There was a strong positive correlation between all of the anthropometric parameters in both young and older children, although the correlation coefcients were higher in older children (Table 3). In addition, NC seems to correlate better with BMI and WC in boys than in girls. Similarly, there was a closer correlation between NC and the other anthropometric indices in older than in younger children (Table 3). Table 4 shows the AUC for each 1-year age group including the optimal NC cutoffs and the corresponding sensitivities and specicities for classifying children into high BMI groups in boys. The likelihood ratios for each cutoff points are also shown. For example, LR for a 6-year-old boy with NC 28.5 cm indicates that he is 3.6 times more likely to be overweight or obese than a 6-year-old boy with NC values below
TABLE 3 Pearson Correlation Coefcients of
the Anthropometric Indices by Age and Gender
Age, y Boys 6 7 8 9 10 11 12 13 14 15 16 17 18 Girls 6 7 8 9 10 11 12 13 14 15 16 17 18 BMI-WC 0.77 0.76 0.84 0.89 0.88 0.71 0.89 0.92 0.84 0.89 0.92 0.94 0.88 0.57 0.86 0.86 0.78 0.84 0.94 0.85 0.88 0.88 0.91 0.94 0.91 0.83 BMI-NC 0.59 0.57 0.66 0.83 0.73 0.68 0.75 0.67 0.74 0.76 0.74 0.84 0.87 0.47 0.82 0.87 0.76 0.82 0.88 0.75 0.72 0.58 0.56 0.74 0.81 0.70 WC-NC 0.59 0.57 0.69 0.85 0.74 0.68 0.73 0.65 0.76 0.75 0.82 0.86 0.86 0.50 0.82 0.83 0.64 0.74 0.7 0.77 0.68 0.62 0.65 0.71 0.85 0.74 P .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001 .001

SBP indicates systolic blood pressure; DBP, diastolic blood pressure.

obesity were computed along age and gender lines. The LR of a positive test result is sensitivity divided by 1 specicity and indicates how much the odds of a disease increase when a test is positive. Conversely, the LR indicates 1 sensitivity divided by specicity and indicates how much the odds of a disease decrease when a test is negative.

RESULTS
A total of 1102 children met the criteria for inclusion in this study; the majority (70.6%) underwent outpatient surgery. The distribution of surgical specialties were as follows: orthopedics, 22.6%; urology, 12.7%; general surgery, 13.8%; otorhinolaryngology, 19.4%; ophthalmology, 6.7%; and others, 24.8%. The mean age of patients in this series was 10.7 3.6 years. The mean NC in young boys with normal BMI was signicantly greater than for young girls with normal BMI (28.1 1.9 vs 26.9 2.0 cm; P .001). Similarly, NC in overweight/obese young boys was 2 cm greater than for young girls of comparable BMI category (31.2 4.4 vs 29.9 3.0 cm; P .001). Table 1
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details the remaining baseline characteristics of the study population stratied according to age group, BMI category, and gender. As expected, all of the anthropometric parameters were signicantly higher in overweight/ obese children than in their normal weight peers. Similarly, baseline systolic blood pressure was signicantly higher in overweight/obese children than their lean peers in both young and older children. Table 2 presents the Pearson correlation coefcients between NC and some clinical and anthropometric parameters for boys and girls. NC showed a strong positive correlation with age, BMI, WC, and height and weight in both boys and girls. In addition, NC was posTABLE 2 Relationship Between NC and Other
Anthropometric Variables by Gender
Variable Boys r Age Weight Height BMI WC, cm 0.66 0.81 0.66 0.71 0.77 P .001 .001 .001 .001 .001 r 0.61 0.84 0.63 0.78 0.83 NC, cm Girls P .001 .001 .001 .001 .001

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TABLE 4 AUCs, Optimal Cutoff Values, Sensitivities, and Specicities for NC Associated With Overweight/Obesity in 6- to 18-Year-Old Boys
Age, y 6 7 8 9 10 11 12 13 14 15 16 17 18 n 95 62 61 49 49 39 36 50 52 37 24 21 17 AUC (95% CI) 0.84 (0.770.92) 0.80 (0.790.89) 0.92 (0.790.96) 0.97 (0.880.99) 0.94 (0.820.98) 0.92 (0.790.98) 0.96 (0.840.99) 0.79 (0.660.89) 0.79 (0.660.89) 0.91 (0.770.98) 0.89 (0.690.98) 0.84 (0.620.96) 0.98 (0.811.00) Cutoff 28.5 28.7 29.0 30.5 32.0 32.2 32.5 33.5 36.0 37.0 38.0 38.6 39.0 Sensitivity (95% CI) 68.8 (54.382.8) 79.3 (63.392.0) 72.4 (53.087.3) 89.6 (79.498.2) 85.7 (57.298.2) 75.3 (47.292.6) 93.7 (69.999.8) 81.8 (59.794.8) 60.0 (36.180.9) 78.9 (48.890.9) 75.0 (34.996.8) 66.7 (32.495.5) 100.0 (47.8100.0) Specicity (95% CI) 81.8 (69.190.1) 69.7 (51.381.4) 90.6 (75.098.0) 87.8 (71.896.6) 94.2 (80.899.3) 95.6 (78.199.1) 80.0 (56.394.3) 67.9 (47.684.9) 93.8 (79.299.2) 94.4 (72.799.9) 81.3 (54.496.0) 93.3 (68.199.8) 100.0 (73.5100.0) LR 3.60 2.60 7.70 7.20 15.00 17.30 4.60 2.60 9.60 14.20 4.00 10.00 NC LR 0.42 0.30 0.30 0.01 0.15 0.26 0.08 0.27 0.43 0.22 0.31 0.36 0.00

CI indicates condence interval.

this cut point. Corresponding ROC data for girls are detailed in Table 5.

DISCUSSION
In this prospective study of children aged 6 to 18 years, NC, WC, and BMI all were highly correlated with each other within each genderage group. NC also performed well as an index of high BMI in young children and adolescents of both genders. Obesity is arguably the most serious chronic health problem facing children in the United States and has been aptly described as a potential cause for the decline in life expectancy during the 21st century.16 Many studies have linked increased adverse health outcomes with BMI 85th (overweight) and 95th (obese) percentiles.12,17 One of the rst steps toward

controlling the childhood obesity epidemic is to make available monitoring tools that are low-cost, quick and easy to use, and generally acceptable to both patients and health practitioners. Various methods are available for assessing obesity in adults and children. Some techniques such as height, weight, WC, and hip girths and computations waist-to-hip ratio and BMI are applicable in physician clinics or primary health care facilities. WC has been shown to be especially useful as an index of central adiposity and performs better than BMI in predicting abnormal cardiometabolic phenotypes18; however, WC measurement may be time-consuming and culturally or environmentally problematic, especially in the winter months because clothes have to be removed for its accurate

measurement. In addition, WC may be affected by postprandial abdominal distension. Several adult studies have documented the value of NC as a simple screening tool for identifying individuals with high BMI.10 The association of NC with central obesity and abnormal metabolic prole in adults has also been documented.19 Very few pediatric investigators have explored the potential value of NC measurement as an index of high BMI.11,12 Consistent with previous ndings in Turkish children,11 the results of this investigation showed that NC performed well as an index of high BMI in young and older children of both genders; therefore, NC could be a useful screening instrument for identifying overweight or

TABLE 5 AUCs, Optimal Cutoff Values, Sensitivities, and Specicities for NC Associated With Overweight/Obesity in 6- to 18-Year-Old Girls
Age, y 6 7 8 9 10 11 12 13 14 15 16 17 18 n 59 49 60 48 46 35 31 51 29 30 28 28 16 AUC (95% CI) 0.79 (0.690.88) 0.92 (0.800.98) 0.86 (0.750.94) 0.87 (0.730.94) 0.86 (0.720.94) 0.94 (0.800.99) 0.86 (0.690.96) 0.86 (0.730.94) 0.85 (0.670.96) 0.64 (0.450.81) 0.85 (0.670.96) 0.92 (0.750.98) 0.77 (0.500.88) Cutoff 27.0 27.1 27.9 29.3 30.5 31.0 31.1 31.3 32.0 33.0 33.4 34.5 34.6 Sensitivity (95% CI) 62.9 (42.680.6) 87.5 (61.798.4) 86.7 (69.396.2) 72.7 (39.094.0) 79.9 (54.993.4) 80.0 (78.295.6) 68.6 (41.389.0) 82.4 (56.696.3) 83.3 (35.999.6) 66.7 (34.990.1) 81.8 (48.297.7) 83.3 (35.999.6) 60.0 (48.293.4) Specicity (95% CI) 84.8 (71.193.7) 87.9 (71.896.6) 70.0 (50.685.3) 85.1 (74.697.0) 70.3 (49.886.2) 90.0 (68.398.8) 100.0 (78.2100.0) 76.5 (58.889.3) 86.9 (66.497.2) 55.6 (30.878.5) 70.5 (44.089.7) 100.0 (84.6100.0) 83.3 (51.697.6) LR 4.10 7.20 2.90 6.70 2.70 8.00 NC 3.50 6.40 1.50 2.80 NC 3.00 LR 0.44 0.14 0.19 0.31 0.30 0.22 0.31 0.23 0.12 0.60 0.26 0.17 0.60

CI indicates condence interval.

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obese children as well as children who are at risk for central fat distribution, an important predictor of poor cardiovascular health. NC measurement is inexpensive, is easier to obtain than other markers of adiposity (WC and BMI), and has good interrater reliability. In addition, NC measurement may be predictive of obstructive sleep apnea, especially in obese children. Certain limitations exist in this study and should be considered in interpreting the data. The cross-sectional nature of the study to some extent limits its interpretation as to causality of associations. Also, single NC measureREFERENCES
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ment could be considered a small limitation; however, NC measurement was previously12 shown to have good interrater and intrarater reliability in the age group included in our study. Finally, analyses that are based on ROC calculations, predictive values, and likelihood ratios depend on the overall disease prevalence14; therefore, conclusions reached in this study may not be applicable to a population with far lower childhood overweight/obesity prevalence. Nonetheless, our data, the rst to show the clinical relevance of NC measurement in a large sample of US children, could prove immensely useful to practitioners who care for

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CONCLUSIONS
NC correctly identied a high proportion of young children and adolescents who were overweight or obese. NC is a simple technique that has good interrater reliability and could be used to screen for overweight and obesity in children. Our NC cutoffs, which correctly identied the majority of children with high BMI, could be used as a reference for boys and girls who are aged 6 to 18 years. Additional studies to evaluate the usefulness of NC as an index of adiposity in younger children are warranted.

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Neck Circumference as a Screening Measure for Identifying Children With High Body Mass Index Olubukola O. Nafiu, Constance Burke, Joyce Lee, Terri Voepel-Lewis, Shobha Malviya and Kevin K. Tremper Pediatrics 2010;126;e306; originally published online July 5, 2010; DOI: 10.1542/peds.2010-0242
Updated Information & Services References including high resolution figures, can be found at: http://pediatrics.aappublications.org/content/126/2/e306.full.h tml This article cites 16 articles, 4 of which can be accessed free at: http://pediatrics.aappublications.org/content/126/2/e306.full.h tml#ref-list-1 Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: http://pediatrics.aappublications.org/site/misc/Permissions.xht ml Information about ordering reprints can be found online: http://pediatrics.aappublications.org/site/misc/reprints.xhtml

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