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Differences in Classification Standards For the Prevalence of Overweight and Obesity in Children. A Systematic Review and Meta-Analysis

Abstract The prevalence of childhood obesity has increased dramatically all over the world in recent years. While obesity in adults can be easily measured using the BMI calculation, determining overweight and obesity in children is more controversial. The aim was to compare the three most used international classification systems (WHO 2007, CDC 2000 and Cole-IOTF) to determine overweight and obesity in infant and adolescent populations. We performed a systematic review in accordance with the PRISMA 2020 guidelines of articles comparing any of the three classification systems. The main findings were that the WHO 2007 criteria show the highest prevalence of overweight and obesity in the child and youth population. The prevalence of childhood overweight and obesity was determined to be higher in boys than in girls in most studies, when analysing the classifications of the WHO 2007, CDC 2000 and Cole-IOTF together. However, there was a higher prevalence of overweight and obesity in girls than in boys when only the CDC 2000 and Cole-IOTF criteria were considered. Both the results of the review and the great heterogeneity found in the meta-analysis show that it is necessary to unify the criteria for the classification of childhood overweight and obesity. International standards are insufficient for working with the current population. A working group should be created to address this issue and agree on the unification of a gold standard, taking into account the geographical region, the ethnic groups and the age groups of the child and youth population and above all, the secular growth.


Introduction
Overweight and obesity are defined as an abnormal or excessive accumulation of fat that can harm health. 1 Obesity has a multifactorial origin that involves both genetic and environmental factors. 2 Several studies showed that excess body fat increased the risk of multiple comorbidities, such as high blood pressure, coronary heart disease, type 2 diabetes, insulin resistance, and cancer. [3][4][5] Globally, the prevalence of obesity and overweight tripled in the child and youth populations from the mid-1970s (about 4%) to 2016 (greater than 18%). In 2016, more than 330 million children and adolescents were affected by overweight or obesity globally. It is estimated that by 2030 nearly 30% of all children will be affected by overweight or obesity. 6 For this reason, childhood obesity is a major public health problem worldwide. 7 Height and weight are the anthropometric variables that have traditionally been used to evaluate growth, other indicators such as Body Mass Index (BMI) have also been used. [8][9][10] BMI is a measure of weight relative to height (weight in kilograms divided by the square of height in meters). 11 Since BMI is easy to determine and correlates with body fatty tissue, it is the most frequently used parameter to assess excess body fat in children and adolescents. [12][13][14] In addition, BMI has been routinely used to analyse overweight and obesity in children and adults worldwide, as in addition to being practical and easy to calculate it is universally applicable. [15][16][17][18] "Overweight", "Obesity", "Children" and "Reference standards", combined using the Boolean operators "AND", "OR" and "NOT". The search strategies used can be found in the Supplementary Material.

Selection Process
All items retrieved from searches were imported into EndNote and duplicates were removed. Each of the authors independently reviewed the remaining articles by title and summary for inclusion and then performed a full text review for methodological reasons of exclusion, based on inclusion criteria.

Data Extraction and Quality Assessment
For each article, one author independently among authors extracted the specific condition, its prevalence or incidence, the classification method or methods used, the age ranges involved and the regions or countries where the study was carried out.
The Joanna Briggs Institute (JBI) checklist 30 for analytical cross-sectional studies was used to assess study quality as the percentage achieved on the checklist.

Synthesis Methods
The synthesis process began by analysing all the main findings and conclusions. Once the synthesis was completed, we classified the prevalence of overweight, obesity or excess weight by age, comparing them with the different international classification systems used. Figure 1 shows the flowchart we followed for the systematic literature review process and Table 1 shows the main results from the selected articles.

Statistical Analysis
We conducted an overall pooled prevalence of childhood overweight and obesity meta-analysis, as well as a subgroup metaanalysis. We assessed heterogeneity between studies using Cochran's Q test and I 2 index. In Cochran's Q test, we interpret significant heterogeneity when p < 0.05. For the I 2 index, high degree of heterogeneity was considered in values higher than 50%. 31 As the result of the test for heterogeneity was very high, we decided to use a random-effects meta-analysis to calculate the combined global prevalence of overweight and obesity with 95% CI. 32 To examine the individual influence of each study, we applied a leave-1-out sensitivity analysis. 33 Publication bias was assessed qualitatively by visual inspection of funnel plot and quantitatively by Egger's linear regression test. 34 Only the 19 studies that analysed the prevalence of overweight and obesity with the three international standards were included in the meta-analysis. Figure 1 shows that the literature search identified 729 results. After removing duplicates and performing the screening process for the remaining articles, we selected 84 articles for full-text review, of which 27 studies met the inclusion criteria. [23][24][25] Table 1 summarises the results obtained from the search of the selected studies. Table 2 shows the quality assessment of the studies.

CDC 2000 Vs Cole-IOTF Classification
The study by Mosellekgomo and van Staden 35 conducted in South Africa found that the CDC classification indicated a very higher prevalence of overweight and obesity in both males and females compared to the IOTF classification. The same occurred in the work of Goon et al 36 in Nigeria, where the prevalence found using the CDC was significantly higher than that found using the IOTF classification.

WHO 2007 Vs CDC 2000 Classifications
The study by Fetuga et al 37 in Nigeria, males had a significantly lower mean weight compared to females and a lower BMI compared to females. The prevalence of overweight + obesity was lower in both sexes when determined with CDC standards compared to WHO standards among individuals aged 6 to 16 years.

WHO 2007 Vs Cole-IOTF Classifications
In the study by Phan et al 38 in Vietnam, they identified that the height, weight and BMI for age of the male participants were slightly higher than the indices of the female participants. However, in this study population, they found that the percentage of body fat was significantly higher in girls compared to boys. The proportion of children affected by overweight, or obesity was higher in the age range of 11 to 12 years. In the category of obesity in children, the prevalence based on the WHO Z-score was approximately 10-15% higher than the prevalence based on the IOTF and the CDC. Also, the study carried out by Bergel Sanchís et al 39 in the countries of Mexico, Venezuela and Spain found that the WHO references overestimated the prevalence of underweight, overweight and obesity in relation to the cut-off points proposed by the IOTF.

WHO 2007 Vs CDC 2000 Vs Cole-IOTF Classifications
The study by Meyer et al 40 carried out in Argentina, when analysing the prevalence of obesity calculated with the different references, observed that the WHO reference gave the highest rates (29.3% compared to the CDC of 17.6% and    DovePress the IOTF of 10.1%). For obesity, the differences between references were significant in all comparisons, except between the IOTF and the CDC in both sexes and age groups.
The study by Shields and Tremblay 23 carried out in Canada, where it was found that in children aged 8 to 13 years, in terms of the prevalence of obesity, the cut-off points of the IOTF were uniformly higher than the cut-off points of the WHO. In addition, for children aged 10 and 11, the IOTF's obesity cut-off points were about 3 BMI units higher than those of WHO.
At all ages, WHO cut-off points assigned higher percentages of boys and girls affected by overweight/obesity than the IOTF and CDC cut-off points. 23 In the study by González-Casanova et al 24 carried out in Colombia, it was found that the WHO system generally yielded the highest prevalence estimates, while the IOTF system yields the lowest.
In the study by Hassapidou et al 41 conducted in Greece, it was generally observed that BMI was significantly higher in boys than in girls. Regarding overweight, the rates according to the IOTF criteria were significantly lower compared to those of the WHO and CDC, respectively. However, the CDC references showed a significantly higher prevalence of obesity compared to the IOTF and WHO, respectively. Also, in the study of Misra et al 42 conducted in India, the IOTF cut-off points showed high agreement with those of the CDC and WHO, respectively.
In the study by Ramírez et al 43 in Mexico, in general, the highest rates of prevalence of overweight and obesity in children were assessed with the WHO reference in both ethnic groups in all regions.
In the study by Ma et al 25 in China, boys were slightly taller and heavier than girls. According to the IOTF reference, 17.1% of all children were affected by overweight or obesity. According to CDC criteria, it was 22.9% of all children and   according to WHO criteria, it was 24.8% of the total. In this study, the WHO and CDC demonstrated a high level of agreement. However, the level of agreement between the WHO and IOTF and CDC was low. In the study by Silva et al 44 in Portugal, according to the IOTF, an overall prevalence of overweight was estimated at 18.7% and obesity at 13.5%. The overall prevalence of obesity and overweight was also found to be 14.9% and 20.6% using the WHO curves and 7.2% and 20.2% using the IOTF estimates. In another study carried out in Portugal by Minghelli et al 45 it was found that the WHO criteria followed by the IOTF estimated the higher prevalence values of overweight and obesity compared to CDC.
In the study by Medehouenou et al 46 in Canada, the prevalence of obesity was similar among boys and girls according to the CDC and WHO criteria. Also, in the study by Pop et al 47 in Romania, the prevalence of overweight and obesity was higher in boys for WHO, CDC and IOTF than in girls. Obesity had a higher prevalence with the WHO than with the CDC criteria, with the lowest prevalence being when the IOTF cut-off points were used.
In the study by Dereń et al 48 in Ukraine it was observed that overweight and obesity occurred more frequently among boys than girls. The IOTF and CDC classifications resulted in a lower incidence of overweight compared to the WHO criteria. In another study carried out in Ukraine by Dereń et al, 49 significantly more girls were affected by underweight compared to boys. Therefore, boys were more likely to be affected by overweight than girls.

WHO 2007 Vs CDC 2000 Vs Cole-IOTF Vs National Classifications
In the study by Baya et al 50 carried out in Bolivia both the CDC and WHO results indicated a higher prevalence of overweight than the BAP (national reference). In general, it was suggested that the references of the CDC, the IOTF and the WHO overestimated the prevalence of overweight in adolescents aged 13 to 18 years and the IOTF in children aged 12 to 14 years. Also, in the study by Shan et al 51 conducted in China, the combined prevalence of overweight and obesity according to the WHO reference was the highest among the four criteria (WHO, CDC, IOTF and Local-WGOC).
Another study that also included a national reference was that of Salehi-Abargouei et al 52 in Iran, where the use of the IOTF criteria revealed overweight among 10.8% of Iranian adolescents, without significant differences between the two sexes (9.7% of boys versus 11.7% of girls). The highest prevalence of obesity was obtained using the WHO criteria.
In the study by Bahk and Khang 53 in Korea among the four sets of criteria (WHO, CDC, IOTF and the Korean national reference KCDC), the WHO criteria showed the highest prevalence of overweight and obesity in all age groups. The IOTF criteria produced the lowest prevalence of obesity in all age categories. Also, El-Ghaziri et al 54 in Kuwait found no significant differences in the prevalence of healthy weight status and the combined prevalence of overweight and obesity among the WHO, CDC, and IOTF. All international approaches showed almost perfect agreement, the highest being between the CDC and WHO. The IOTF criteria showed high agreement with the WHO and CDC. In the study by Wickramasinghe et al 55 in Sri Lanka, the proportions of children affected by obesity classified by the WHO criteria were slightly higher than the proportion detected by IOTF cut-off values.

WHO 2007 Vs CDC 2000 Vs Cole-IOTF Vs Other Classifications
In the study by Heer et al 56 conducted in Mexico, the WHO standards showed the highest agreement with local standards. Both WHO and CDC showed better agreement with local scores than with IOTF values.

WHO 2007 Vs CDC 2000 Vs National Classifications
Finally, in the study carried out by Pérez-Bermejo et al 57 in Spain, significant differences were found in BMI values according to age between the two sexes at some ages, for this reason, the authors argued that, if the WHO reference were used, the rate of overweight and obesity would be double that of national references. Table 3 shows the main results of the meta-analysis. There were 19 studies that reported the prevalence of overweight ( Figure 2) and obesity ( Figure 3) analysed with the three standards under study. There was significant (Q = 1617.37) and substantial heterogeneity between studies (I 2 > 99% in all cases). Figure 4 shows the subgroup analysis. The difference between these subgroups was statistically significant.  Table 4 shows the leave-1-out sensitivity analysis of the influence of single study on the pooled prevalence of overweight and obesity in children. Therefore, no study has been excluded from the meta-analysis. Egger's test of bias was not significant, indicating that smaller studies not reported larger estimates of the prevalence of overweight and obesity (t = 1.17; p = 0.247). A funnel plot ( Figure 5) was used to assess possible publication bias, which showed no substantive asymmetry.

Discussion
The results of this literature review suggest that the choice of a BMI reference may significantly influence the decision to provide clinical advice or treatment, as well as estimates of the healthcare resources needed to counteract overweight and obesity. The percentage of children, young people and adolescents affected by overweight varies considerably depending on the BMI cut-off points across classifications and may also vary by age group and ethnicity. 40,59 The prevalence of childhood obesity has increased dramatically all over the world in recent years. It is associated with cardiovascular disease, hypertension, diabetes, osteoarthritis, and cancer. Children affected by obesity also have an increased risk that obesity will persist into adulthood. In addition, childhood obesity has also been associated with mental health problems in young people. While obesity in adults can be easily measured using the BMI calculation, determining overweight and obesity in children is more controversial. 59 When comparing the three most commonly used international classification systems, WHO 2007, CDC 2000 and Cole-IOTF, and the agreement between them, we observed that each selected study compares and analyses these systems differently. 35,36 The comparison between the WHO 2007 classification and CDC 2000 found that the prevalence of overweight and obesity was lower in both sexes when determined with CDC standards compared to WHO standards. 37 The WHO 2007 against Cole-IOTF classification was exclusively investigated in only two studies analysed. For obesity in children, prevalence based on WHO was approximately higher than prevalence based on IOTF. 38 WHO references were found to overestimate the prevalence of underweight, overweight, and obesity relative to the IOTF for the diagnosis of malnutrition. 39 The comparative studies between the three international classifications of WHO 2007, CDC 2000 and Cole-IOTF found that, when analysing the prevalence of obesity, those obtained with the WHO reference were higher compared to CDC and IOTF. 40 The differences were generally greater between WHO and IOTF references than between WHO and CDC references. Overall, WHO cut-offs yielded the highest prevalence estimates and IOTF cut-offs the lowest. 23,[40][41][42][43][44][45][46][48][49][50]59 Also BMI classification patterns by age tended to be similar between IOTF cut-offs and CDC in contrast to the WHO cut-offs, for all ages and sexes. 38  On the other hand, the authors argue that all international references tend to underestimate underweight, while they overestimate overweight. 51 The highest prevalence of obesity was obtained using the WHO criteria compared to CDC, IOTF and the national criterion in Iran. 52 Also, among the four sets of WHO, CDC, IOTF and National-KCDC criteria in Korea, the WHO criteria showed the highest prevalence of overweight and obesity in all age groups. 53 Studies analysing the WHO 2007 classification versus the national classifications determined that, if the WHO reference was used, the rate of overweight and obesity would double compared to the national reference. 57 Therefore, statistically significant differences in terms of the comparison of the different international references were found in the studies by González-Casanova et al, 24 Mosellekgomo and van Staden, 35 Goon et al, 36 Fetuga et al, 37 Meyer et al, 40 Hassapidou et al, 41 Pop et al, 47 Dereń et al, 48 Salehi-Abargouei et al, 52 Pérez-Bermejo et al 57 and López-Sánchez et al. 59 Furthermore, in the Southern European, 59 significant differences between obesity and overweight values were demonstrated between the Cole-IOTF classification with 32.3% and WHO 2007 with 37.3%, respectively. The divergences between the three international classification systems are due to the fact that they use different selection criteria, samples and data collection in different time periods, as in the case of the IOTF published in 2000, where the BMI cut-off points are set at ≥25 kg/m2 and <30 kg/m2 for overweight and BMI ≥30 kg/m2 for obesity. 22 In contrast, the WHO 2007 reference was composed of a sample collected in the 1970s and analysed between 1997 and 2003 where the diagnosis of overweight was set at BMI >+1 SD and ≤+2 SD and obesity at BMI >+2 SD. 15 Finally, the CDC 2000 classification was elaborated by the National Center for Health Statistics (NCHS) in the US paediatric population between 1963 and 1994 establishing overweight as BMI ≥P85 and <P95 and obesity as BMI >P95. 20 BMI is the accepted tool for evaluating overweight and obesity in children. However, it should be used with caution as BMI is not a measure of fat mass or the distribution of adipose tissue in the body. 59 There are several current trends as to which parameters should be considered more when diagnosing childhood overweight and obesity. Some authors study following the recommendations of the European Childhood Obesity Surveillance Initiative (COSI) of the WHO. 60  However, other authors prefer to use other anthropometric references or the estimation of compartments and body composition by electrical bioimpedance.
Among the limitations of this study, we consider the different results that can be obtained by using different strategies to determine overweight and obesity, and the uniqueness of each and every child, youth and adolescent when these strategies are applied. We observed differences by age group and ethnicity when evaluating and comparing the application of the various classifications, so this may be a cause of bias in the comparison of the results obtained in each study analysed.
Due to this disparity between the prevalence of childhood overweight and obesity according to the classification used, we must highlight the recent publication by Cole and Lobstein 61 where they developed an algorithm to harmonise the cut-off points according to BMI for age and sex of the WHO, CDC and IOTF and make them comparable. This tool allows the researcher to choose any of these three classifications and compare them with the others, making the results more comparable. This makes it a very interesting tool for minimising the possible biases of comparison between different populations and resolving hypotheses in future lines of research.

Conclusion
The prevalence of childhood overweight and obesity according to BMI was determined to be higher in boys than in girls in most studies, this was considered when analysing the classifications of the WHO 2007, CDC 2000 and Cole-IOTF  DovePress together. However, there was a higher prevalence of overweight and obesity in girls than in boys when only the CDC 2000 and Cole-IOTF criteria were considered. The WHO 2007 criteria were those with the highest prevalence of overweight in the child and youth populations compared to CDC 2000, Cole-IOTF and national or local criteria.
Both the results of the review and the great heterogeneity found in the meta-analysis show that it is necessary to unify the criteria for the classification of childhood overweight and obesity. International standards are insufficient for working with the current population. Further studies similar to that described above by Cole and Lobstein 61 comparing or constructing national or local references using BMI as a primary measure are needed or a working group should be created to address this issue and agree on the unification of a gold standard to address the current epidemic of childhood overweight and obesity, taking into account the geographical region, the ethnic groups and the age groups of the child and youth population and above all, the secular growth to stop working with a standard that has been very useful in the absence of others, but that should be updated.