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Ijpo 242
Ijpo 242
ORIGINALRESEARCH doi:10.1111/ijpo.242
ORIGINALRESEARCH
identify obesity as defined by body adiposity in
children and adolescents: a systematic review
and meta-analysis
A. Javed1, M. Jumean2, M. H. Murad3, D. Okorodudu4, S. Kumar1, V. K. Somers5,
O. Sochor5,6 and F. Lopez-Jimenez5
1
Department of Pediatric and Adolescent Medicine, Division of Pediatric Endocrinology Mayo Clinic, Rochester, MN, USA;
2
Department of Cardiovascular Diseases Tufts Medical Center, Boston, MA, USA; 3Division of Preventive, Occupational, and
Aerospace Medicine, Department of Medicine, Mayo Clinic, Rochester, MN, USA; 4Department of Internal Medicine, Duke
University Medical Center, Durham, NC, USA; 5Division of Cardiovascular Diseases, Department of Medicine, Mayo Clinic,
Rochester, MN, USA; 6International Clinical Research Center – Department of Cardiovascular Diseases, St. Anne’s University
Hospital Brno, Brno, Czech Republic
Summary
Background: The ideal means of identifying obesity in children and adolescents has not been deter-
mined although body mass index (BMI) is the most widely used screening tool.
Objective: We performed a systematic review and meta-analysis of studies assessing the diagnostic
performance of BMI to detect adiposity in children up to 18 years.
Methods: Data sources were EMBASE, MEDLINE, Cochrane, Database of Systematic Reviews
Cochrane CENTRAL, Web of Science and SCOPUS up to March 2013. Studies providing measures of
diagnostic performance of BMI and using body composition technique for body fat percentage measurement
were included.
Results: Thirty-seven eligible studies that evaluated 53 521 patients, with mean age ranging from 4 to 18
years were included in the meta-analysis. Commonly used BMI cut-offs for obesity showed pooled sensitivity
to detect high adiposity of 0.73 (confidence interval [CI] 0.67–0.79), specificity of 0.93 (CI 0.88–0.96) and
diagnostic odds ratio of 36.93 (CI 20.75–65.71). Males had lower sensitivity. Moderate heterogeneity was
observed (I2 = 48%) explained in meta-regression by differences across studies in race, BMI cut-off, BMI
reference criteria (Center for Disease Control vs. International Obesity Task Force) and reference standard
method assessing adiposity.
Conclusion: BMI has high specificity but low sensitivity to detect excess adiposity and fails to identify over
a quarter of children with excess body fat percentage.
Address for correspondence: Dr F Lopez-Jimenez, Division of Cardiovascular Diseases, Department of Medicine, Mayo Clinic, 200 First
Street SW, Rochester, MN 55905, USA. E-mail: Lopez@mayo.edu
© 2014 The Authors
Pediatric Obesity © 2014 World Obesity. Pediatric Obesity ••, ••–••
2 | A. Javed et al.
widespread office-based use, yet sufficiently reliable has been conducted. The present meta-analysis
ORIGINALRESEARCH
to detect obesity at an early stage. aims to assess an overall estimate of validity of BMI
Obesity is defined as a medical condition in which for detection of obesity as defined by excess adipos-
excess body fat accumulation can impact health ity in children and adolescents up to the age of 18
negatively (10). However, current assessment of years, while recognizing that BMI is not used to
obesity is based on BMI which relies on body weight diagnose obesity in children less than 2 years of age.
regardless of body composition, and is calculated by
dividing the individual’s weight in kilograms by the Materials and methods
height in meter squared. Due to its simplicity and Search strategy and selection criteria
epidemiologic data showing an association between
increased BMI and cardiovascular events (11), BMI The predefined inclusion criteria for study selection
has been used in the clinical setting despite carrying were: (i) the study must have assessed the diagnos-
the inherent flaw of failing to distinguish between lean tic performance of BMI to identify excess adiposity in
and fat mass (12–14), both of which contribute to children aged 0–18 years; (ii) provided a 2 × 2 diag-
BMI. Despite ethnic and racial differences in adipos- nostic table to allow for meta-analysis or information
ity, recommendations from several organizations, to calculate these values; and (iii) used a reference
including the American Academy of Pediatrics, standard for body composition (e.g. DXA, ADP, HW).
advise the use of BMI for age with national reference Studies were excluded if they only assessed
data to diagnose paediatric obesity in the clinical cardiometabolic risk factors without use of any ref-
setting (15–19). However, previous studies have erence standard methods for measuring adiposity.
highlighted the limitations of BMI, both in adults and We searched the databases EMBASE (1988 to
in the growing child (20–22). Further limitations of March 2013), MEDLINE (1950 to March 2013),
BMI as a universal screening tool include the type of Web of Science (1993 to March 2013), Cochrane,
BMI reference criteria used (e.g. National reference Database of Systematic Reviews (from inception),
for age data vs. Center for Disease Control [CDC] Cochrane CENTRAL (from inception) and SCOPUS
(23) vs. International Obesity Task Force [IOTF]) (24), (1996 to March 2013). The search was conducted by
pubertal stage and racial/ethnic differences between a librarian with expertise in meta-analyses with input
the individual patient and cohort (12,25). from investigators. Three domains were considered
The cut-off value used to diagnose obesity in chil- absolute criteria during the search: (i) BMI or equi-
dren involves working out the distribution for a par- valent (e.g. Quetelet Index, BMI); (ii) diagnostic per-
ticular population and arbitrarily choosing particular formance or equivalent (e.g. sensitivity, specificity,
values, often the 85th or 95th centiles, to categorize predictive values); and (iii) measurement of body fat
those with the highest BMIs (26). Several studies or equivalent (for example DXA, ADP, HW, BIA, body
have illustrated discrepancies between prevalence of composition). The detailed search strategy is pro-
obesity within a population using different reference vided (Supporting Information Appendix S1).
growth curves (27,28). We eliminated irrelevant articles from our primary
Previous studies in children have analysed the per- search on the basis of information in title and
formance of BMI to detect obesity when compared abstract (Fig. 1). The remaining studies were read in
with techniques considered reference standard their entirety by a single investigator (AJ) and those
methods for measurement of body adiposity, e.g. not meeting inclusion criteria were excluded. The
dual energy X-ray absorptiometry (DXA), hydrostatic search was supplemented with cross-references
weighing (HW), air-displacement plethysmography from selected articles. A particular effort was made
(ADP), isotope dilution, bioelectrical impedance to contact authors of articles with equivocal informa-
analysis (BIA) and skin-fold thickness measurement tion and investigators known to conduct research on
(29); however, these techniques are rarely used in BMI diagnostic performance asking for studies that
clinical practice because of their cumbersome nature may fulfil our inclusion criteria.
and lack of reference data on ‘normal’ cut-offs for
Quality assessment/data abstraction
body fat percentage (BF%) values in children.
While a systematic review assessing the perfor- Thirty of the studies were selected from our pri-
mance of BMI in prediction of adverse cardiovascular mary search based solely on title and abstract,
risk has been performed (11), no meta-analysis gen- and independently reviewed by another investigator
erating estimates of pooled sensitivity and accuracy (FL-J) and agreement coefficient determined. The
of BMI vs. reference standard methods of measuring Quality Assessment of Diagnostic Accuracy Studies
excess body fat or adiposity, such as BIA, DXA etc., (QUADAS) tool, a 0- to 14-point scale considering
ORIGINALRESEARCH
Figure 1 Study flow chart illustration. Of the 1488 potentially relevant abstracts, 33 articles were included in the
meta-analysis along with four articles added via cross-reference.
Pooled sensitivity Pooled specificity Positive likelihood Negative likelihood Diagnostic odds ratio
ratio ratio
Overall 0.73 (CI0.67–0.79) 0.93 (CI0.88–0.96) 10.58 (CI6.08–18.41) 0.29 (CI0.23–0.35) 36.93 (CI20.75–65.71)
Males 0.67 (CI0.56–0.76) 0.94 (CI0.84–0.98) 11.17 (4.22–29.54) 0.34 (CI0.27–0.47) 31.37 (11.53–85.31)
Females 0.71 (CI0.62–0.79) 0.95 (CI0.88–0.98) 14.56 (CI6.33–33.45) 0.30 (CI0.23–0.40) 48.02 (21.09–109.4)
CI, confidence interval.
(32) with a value of 0% indicating no observed het- (Fig. 1). The concordance assessment using a
ORIGINALRESEARCH
erogeneity and >50% denoting substantial heteroge- sample of abstracts showed perfect agreement (cor-
neity. Data analysis was conducted using the relation coefficient of 1.0) between co-authors (AJ
statistical program Stata (Version 11, StataCorp, and FL-J) when selecting studies based on title and
College Station, TX, USA). abstract. The studies included in the final analysis
To explain heterogeneity, we conducted multiva- evaluated a total of 53 521 patients, with a mean age
riable meta-regression in which the outcome variable ranging from 4 to 18 years. Gender-specific data
was the log of DOR and the explanatory variables were present in 34 of the 37 studies, including
were covariates known to affect BMI (21). These 18 429 males and 22 781 females.
variables were chosen a priori as potential causes of Meta-analysis showed pooled sensitivity to detect
between-study heterogeneity and included: (i) BMI high adiposity of 0.73 (95% confidence interval [CI]
cut-off values to define obesity, (ii) BF% cut-off values 0.67–0.79) and pooled specificity of 0.93 (CI 0.88–
to define obesity, (iii) gold standard used to assess 0.96). LR+ was 10.58 (CI 6.08–18.41), LR− was 0.29
BF%, (iv) race and (v) quality assessment score. (CI 0.23–0.35) and DOR was 36.93 (CI 20.75–
Studies were grouped based on BMI definition of 65.71). Receiver operating curve of BMI to detect
excess adiposity using (i) BMI cut-off values into adiposity is shown in Fig. 2. In males, BMI showed
≥95th percentile, ≥85th percentile or other, or (ii) CDC pooled sensitivity of 0.67 (CI 0.56–0.76) and pooled
definition or national reference criteria vs. the IOTF specificity of 0.94 (CI 0.84–0.98). LR+ was 11.17
definition of obesity. When more than one BMI cut-off (4.22–29.54), LR− was 0.34 (CI 0.27–0.47) and DOR
values were reported, the diagnostic accuracy of was 31.37 (11.53–85.31). As for females, BMI
BMI using the CDC or national reference criteria was showed pooled sensitivity of 0.71(CI 0.62–0.79),
used for the overall pooled analysis. Studies were pooled specificity of 0.95 (CI 0.88–0.98), LR+ of
also grouped based on BF% groups using cut-off 14.56 (CI 6.33–33.45), LR− of 0.30 (CI 0.23–0.40)
values to define obesity by adiposity and not by BMI, and DOR of 48.02 (21.09–109.4) (Table 1).
as follows: (i) BF% of 20–25% in males and <30% in Moderate heterogeneity was observed across
females, (ii) other definitions of BF% cut-off, (iii) ≥95th studies (I2 = 48%), explored through multi variable
percentile BF% cut-off. These BF% cut-offs were meta-regression. While race, BMI cut-off value,
based on definitions of obesity by fat content previ- national or CDC vs. IOTF reference criteria, definition
ously used in study populations assessing adiposity of BMI and reference standard method used to
at the individual level, and mostly derived from adult measure adiposity explained heterogeneity, body fat
data shown to correlate with metabolic risk. Studies cut-off used or study quality did not (Appendix S2).
included in the meta-analysis used different methods The characteristics of individual studies selected for
as reference standard to assess body composition. meta-analysis are presented in Table 2.
Based on comparable accuracy, studies that used
DXA, HW, ADP and isotope dilution measurement of
Discussion
total body water were grouped together and the
pooled estimates were reported and compared with This is the first systematic review and meta-analysis
those studies that used lower accuracy measures as assessing diagnostic performance of BMI in identify-
the reference standard method (BIA and skin-fold) ing excess body fat as compared with reference
(33–35). For studies reporting diagnostic accuracy of standard techniques of measuring adiposity, e.g.
BMI when compared with more than one BF com- DXA, ADP etc., in children. The results show that BMI
position measure, data from the higher accuracy BF has high specificity in identifying paediatric obesity,
composition method were used in overall pooled but moderate sensitivity. Pooled results from the 37
analysis. Given geographic differences in body com- studies showed sensitivity of 73%, suggesting over a
position, studies were grouped based on race of the quarter of children not labelled as obese by BMI
study population into Caucasian, Asian, Hispanic or might indeed have excess adiposity.
Black. Finally, studies were categorized into two These results have implications for clinicians,
subgroups based on QUADAS score into optimal or public health and policymakers as well as the indi-
suboptimal groups (cut-off score = 10) (Table 2). vidual child. Suboptimal recognition of obesity at this
crucial time translates into missed opportunities to
institute appropriate lifestyle interventions to mitigate
Results
future health risks (65).
The search strategy yielded 1488 potential studies. Previous studies report low sensitivity and high
Subsequently, 37 articles met all inclusion criteria specificity of BMI in children (14,17,38,40,42,49,52)
Author Quality Population/ n Mean age Age SD/ % % Reference Dx criteria Dx criteria Prevalence Sensitivity Specificity
score location (years) SEM± Male Female standard according according according % %
method to reference to BMI to reference
standard standard
Eto et al. (36) 9 Japan 486 4.35 0.70 47.94 52.06 BIA 20% BF (M) 90th percentile 18.07 32.98 95.95
25% BF (F)
Wickramasinghe 11 Australia 96 9.43 2.25 45.83 54.17 DD 20% BF (M) 95th percentile 50.00 11.75 100.00
et al. (37) 30% BF (F)
Sri Lankan 42 9.28 3.18 64.29 35.71 DD 20% BF (M) 95th percentile 54.76 13.40 100.00
migrants living 30% BF (F)
in Australia
da Veiga et al. (25) 11 Brazil 1540 (10–17.9) 46.5 53.5 BIA 25% BF (M) 95th percentile 16.60 28.90 99.22
30% BF (F)
Sardinha et al. (38) 10 Portugal 55 (10–11) * 100 0 DXA 25% BF 19 kg m−2 27.3% 96 86
52 (12–13) * 100 0 DXA 25% BF 19.4 kg m−2 86 76
58 (14–15) * 100 0 DXA 25% BF 24 kg m−2 50 92
54 (10–11) * 0 100 DXA 30% BF 19.6 kg m−2 44.8% 83 87
60 (12–13) * 0 100 DXA 30% BF 21.2 kg m−2 N/A 67 97
49 (14–15) * 0 100 DXA 30% BF 21.9 kg m−2 N/A 77 89
Neovius et al. (39) 10 Sweden 474 16.84 0.26 42.19 57.81 ADP 25% BF (M) 85th percentile 29.93 48.48 94.37
30% BF (F)
Reilly et al. (40) 9 United Kingdom 238 8.50 0.40 51.68 48.32 SF 25% BF in males z score = 2 ∼ 97.7th 6.72 43.75 98.65
32% BF in females percentile
Taylor et al. (41) 10 New Zealand 368 11.89 1.97 48.64 51.36 DXA 25% BF in males Male z score = 24.99 86.18 93.11
35% BF in females 0.41 ∼ 65.8th percentile
Female z score =
0.89 ∼ 79.1th percentile
Marshall et al. (42) 10 Canada 540 10.88 0.40 49.3 50.7 HW BF >20% in males, >120% value of BMI 14.10 71.10 91.60
>25% in females
Nichols & Cadogan 10 Island of Tobago 3749 14.50 1.66 42.9 57.1 BIA BF >25% in males, >95th percentile 30.11 57.12 93.58
2009 (43) >30% in females
Fu et al. (44) 10 Singapore 623 8.35 0.24 51.5 49.5 BIA BF >95th percentile IOTF criteria extrapolated 75.00 95.80
adult > 30 kg m−2
Li et al. (13) 7 China 587 9.64 0.50 47.5 52.5 BIA BF >25% males, BMI cut-off of 20 kg m−2 34.80 26.40 99.20
>30% females used
Candido et al. (45) 10 Brazil 159 pre-pubertal 6–15 47.7 52.3 BIA >85th percentile Differing cut-offs based on 87.50 99.30
girl least misclassification
121 pubertal girl 88.90 88.50
123 post-pubertal 78.00 84.90
girl
183 pre-pubertal 95.00 92.00
boy
Diagnostic performance of BMI to identify obesity
Table 2 Continued
Author Quality Population/ n Mean age Age SD/ % % Reference Dx criteria Dx criteria Prevalence Sensitivity Specificity
score location (years) SEM± Male Female standard according according according % %
Bedogni et al. (46) 8 Italy 934 10.00 1.00 49.89 50.11 BIA 85th percentile 95th percentile N/A 39.00 99.00
A. Javed et al.
Gaskin & Walker (47) 9 Jamaica 303 7.75 55.45 44.55 Sum SF 85th percentile Predicted 25 kg m−2 at 3.63 50.10 99.12
age 18
306 11.81 0.35 55.45 44.55 Sum SF 85th percentile Predicted 25 kg m−2 9.48 72.69 97.36
at age 18
Ghosh (48) 9 India 450 7.46 1.16 0 100 SF 85th percentile 95th percentile N/A 49.00 94.00
Lazarus et al. (49) 9 Australia 230 12.17 51.74 48.26 DXA 85th percentile 95th percentile N/A 29.00 99.00
Mei et al. (50) 8 NHANES III 4285 2–5 SF 85th percentile 85th percentile N/A 78.30 88.30
NHANES III 3279 6–11 SF 85th percentile 85th percentile 92.70 91.50
NHANES III 3189 12–15 SF 85th percentile 85th percentile 84.70 90.50
America, Italy, 162 4.76 0.58 33.33 66.66 DXA 85th percentile 85th percentile 88.50 79.40
New Zealand
America, Italy, 466 8.52 1.43 41.42 58.58 DXA 85th percentile 85th percentile 98.60 67.70
New Zealand
ADP, air-displacement plethysmography; BF, body fat; BIA, bioelectrical impedance analysis; BMI, body mass index; DD, deuterium dilution; Dx, Diagnostic; DXA, dual energy X-ray absorptiometry; F, female; HW, hydrostatic weighing;
IOTF, International Obesity Task Force; M, male; NHANES, National Health and Nutrition Examination Survey; N/A, not available; SD, standard deviation; SEM, standard error of the mean; SF, skin-fold. Sensitivity results ranged from
11.75% in an Australian population [Wickramasinghe et al. (37)] to 100% in Caucasian populations [Mei et al. (50), Candido et al. (45)]. Specificity ranged from 66.7% in a New Zealand population [Duncan et al. (53)] to a value of 100%
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ORIGINALRESEARCH
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Appendix S1. Search strategy.
64. Neovius M, Rasmussen F. Evaluation of BMI-based Appendix S2. Diagnostic performance of BMI
classification of adolescent overweight and obesity: choice across predefined subgroups.