Body mass index classification misses to identify children with an elevated waist-to-height ratio at 5 years of age

Abstract

Background

Abdominal adiposity is an important risk factor in the metabolic syndrome. Since BMI does not reveal fat distribution, waist-to-height ratio (WHtR) has been suggested as a better measure of abdominal adiposity in children, but only a few studies cover the preschool population. The aim of the present study was to examine BMI and WHtR growth patterns and their association regarding their ability to identify children with an elevated WHtR at 5 years of age.

Methods

A population-based longitudinal birth cohort study of 1540 children, followed from 0 to 5 years with nine measurement points. The children were classified as having WHtR standard deviation scores (WHtRSDS) <1 or ≥1 at 5 years. Student’s t-tests and Chi-squared tests were used in the analyses.

Results

Association between BMISDS and WHtRSDS at 5 years showed that 55% of children with WHtRSDS ≥1 at 5 years had normal BMISDS (p < 0.001). Children with WHtRSDS ≥1 at 5 years had from an early age significantly higher mean BMISDS and WHtRSDS than children with values <1.

Conclusions

BMI classification misses every second child with WHtRSDS ≥1 at 5 years, suggesting that WHtR adds value in identifying children with abdominal adiposity who may need further investigation regarding cardiometabolic risk factors.

Introduction

The number of overweight or obese children has increased rapidly worldwide in recent decades.1 Excess weight in childhood and adolescence has been shown to be associated with the metabolic syndrome (MetS),2 and according to one recent update, ~10% of children and adolescents have this syndrome.3 The MetS represents a number of cardiometabolic risk factors: obesity (predominantly abdominal), hypertension, insulin resistance, glucose intolerance and dyslipidaemia, which are all related to an increased risk of cardiovascular morbidity.4,5 Cardiometabolic risk factors have been found to exist already during preschool age, at the onset of overweight or obesity6 and may have their origins as early as in utero.7

Identification of children with the MetS, as early as possible during childhood has been suggested, for the possibility to introduce lifestyle modifications early in life.8,9 Although there is yet no consensus regarding the definition of the MetS in children,10 abdominal adiposity is an important risk factor. In 2007, the International Diabetes Federation (IDF) presented one definition with criteria for diagnosis in children. The criteria for children in the age group 10 to <16 years were abdominal adiposity and two or more of the following risk factors: elevated blood pressure, elevated plasma glucose, elevated triglycerides and low high-density lipoprotein (HDL).11 The IDF did not recommend diagnosis of the MetS in children younger than 10 years but suggested monitoring of abdominal adiposity.10,11 Other definitions including children as young as 2 years exist, one recently proposed by Ahrens et al.8 uses sex- and age-specific cutoff values for the different components of the MetS, and also in their definition, particular weighting is given to waist circumference.

Since children with obesity have a higher risk of developing the MetS, compared to children without obesity, it may be advantageous to screen for the MetS in children with excess weight.3 Although the prevalence of the MetS in children has increased, it is still relatively low, and it would not be cost effective to perform blood tests for cardiometabolic risk factors in all children at risk, therefore anthropometric measures have been suggested as good alternatives in screening.12,13

Body mass index (BMI) is the most commonly used surrogate measure of adiposity in children and in adults.14 Nevertheless, the value of BMI in cardiometabolic risk screening has been questioned since it does not distinguish between fat mass and fat-free mass.15 BMI also has a low correlation with fat distribution such as abdominal fat.16 Since abdominal adiposity is the most prevalent of the cardiometabolic risk markers, and its presence is a sign of disturbed fat metabolism,17 a measure that better relates to abdominal adiposity would be valuable in this screening.

Waist circumference (WC) and waist-to-height ratio (WHtR) have been suggested as surrogate measures of cardiometabolic risk factors and abdominal adiposity in children and adolescents.18,19,20,21,22 However, only a few studies cover the utility of BMI and WHtR in identifying abdominal adiposity in preschool children.23,24

The aim of the present study was to examine if BMI and WHtR growth patterns from an early age could identify children with an elevated WHtR at 5 years of age by using standard deviation score(s) (SDS) in children classified according to WHtRSDS at 5 years of age. The second aim was to study the association between BMISDS and WHtRSDS at 5 years of age, with the hypothesis that an elevated WHtR partly identifies other children than an elevated BMI does.

Methods

Study population and design

The present study is a longitudinal birth cohort study with a 5-year perspective, part of the ongoing population-based birth cohort study, the Halland Health and Growth Study (H2GS). The aim of the H2GS is to study factors that affect health and growth in children. From its start, the H2GS included 2666 children (1349 boys and 1317 girls), born in the south-western part of Sweden in the county of Halland between 1 October 2007 and 31 December 2008. All 3860 children born in the county within this time period, and visiting the child health care centers, were eligible to take part in the study without any exclusions. The families were recruited when visiting the child health care centers for the first time. Measurements of height, weight, and WC were collected at nine points, beginning at the age of 0–1 month. In connection with each visit, the parents filled in questionnaires regarding their child’s lifestyle and food habits, as well as background data. The study protocol, the representativeness of the sample, and the recruitment process were reported in detail elsewhere.25

In this part of the study, only children with complete growth data at 5 years of age were included. Due to lack of these data, 437 boys and 385 girls were excluded, as were children measured outside our decided age limits. For children below 12 months of age we used ±1.5 months, except at the measurement point 0–1 month (where 0–45 days was used instead). From 12 months of age, we used ±2.5 months. This excluded another 132 boys and 114 girls. In addition, children born preterm were excluded, 35 boys and 31 girls. As 3 girls and 5 boys were both measured outside the selected age limit and born preterm, and because they only were excluded once, the total remaining study population consisted of 750 boys and 790 girls. This study was approved by the regional ethical review board in Lund, Sweden (DNR: 299/2007). Written informed consent was obtained from the parents of all the participating children.

Measurements

Measurements of height, weight, and WC were done at 0–1, 3–4, 6, 12, 18, 24, 36, 48, and 60 months. All measuring was performed by trained child health care nurses. Stadiometers were used for measuring height. In children below 2 years of age, height was measured in a supine position, and after 2 years of age in a standing position (without shoes). Infants below 15 kg were weighed on baby scales in a supine position and thereafter on step scales, mechanical or electronic. Younger children were weighed without clothing and older children in underpants. WC was measured midway between the lowest rib and the top of the iliac crest, at the end of a gentle expiration (without clothing). In children below 2 years of age, WC was measured in a supine position and thereafter in a standing position. Within the framework of the project, the inter- and intra-operator reliability for WC has been studied in children mainly younger than 24 months. The intra-class correlation coefficients were 0.98 both within and between those who made the measurements, although one of the persons was less experienced.

BMI was calculated as weight (kg)/(height in m)2 and was then transformed into age- and gender-specific SDS, using the estimated mean and standard deviation (SD) functions based on Swedish reference data.26 SDS represents the difference between the observed and estimated mean BMI divided by the SD, and with regard to age and gender. WHtR was calculated as WC (cm)/height (cm) and was then transformed into age- and gender-specific SDS using the estimated mean and standard deviation functions based on Swedish reference data.27

Classifications

The children were classified as having WHtRSDS <1 or ≥1 at 60 months of age according to Swedish reference values.27 In this population a WHtRSDS of 1 corresponded to a crude WHtR value of 0.51 in both boys and girls. For associations between BMISDS and WHtRSDS at 60 months, the children were also classified as having BMISDS either for normal weight (including underweight) or overweight/obesity according to BMI cutoff values by the International Obesity Task Force (IOTF),28 which were transformed to corresponding BMISDS; 1.26 and 1.20 for overweight and 2.44 and 2.22 for obesity, in boys and girls, respectively (corresponding SDS for underweight, the second grade of thinness, were −2.44 and −2.22 for boys and girls, respectively).

Birth weight, birth length as well as gestational age were collected from the Swedish medical birth register. Children were classified as small for gestational age (SGA), appropriate for gestational age (AGA) or large for gestational age (LGA). SGA was defined as birth weight or birth length ≤−2 SDS for gestational age, and LGA was defined as birth weight or birth length ≥2 SDS for gestational age, according to Swedish reference standards.29

Statistics

Student’s t-tests were performed to compare the mean values of BMISDS and WHtRSDS at the different measurement points in the WHtRSDS groups (BMISDS <age>, WHtRSDS <age>). Chi-squared tests were made for the study of associations between BMISDS and WHtRSDS at 60 months. In all statistical analyses except for the Chi-squared tests boys and girls were analysed separately.

IBM SPSS Statistics (IBM Corp, Armonk, New York, v.20.0) was used for all statistical analyses. A p-value <0.05 was considered statistically significant. Conversions of crude values to BMISDS and WHtRSDS, as well as the construction of graphs were made in Matlab (The MathWorks, Natick, Massachusetts v.9.0.0.341360R2016a).

Results

Of the 750 boys, 86.8% had WHtRSDS<1 and 13.2%, had values ≥1, at 5 years of age (Table 1). The corresponding values for the 790 girls were 83.3%, and 16.7%, respectively.

Table 1 Characteristics of the study population by gender

WHtRSDS values ≥1 at 5 years corresponded to crude WHtR values between 0.51 and 0.59 in the boys and between 0.51 and 0.66 in the girls. BMISDS classification showed that among the boys, 2.4% had underweight, 87.6% had normal weight, 8.5% had overweight, and 1.5% had obesity. The corresponding values for the girls were, 1.6. 85.7, 9.6, and 3.0%. Mean values of BMI and BMISDS were at 5 years significantly higher in children with WHtRSDS ≥1 compared to in children with WHtRSDS <1 (p < 0.001). There were no significant differences in mean birth weight (MBW) and proportion of children born SGA or LGA between the different WHtRSDS groups.

Association between BMISDS and WHtRSDS

Overweight/obesity according to BMISDS was to a high proportion associated with an elevated WHtRSDS, where 104/175 (59%) children with overweight/obesity according to BMISDS had ≥1 in WHtRSDS. However, 127/1365 (9%) of children with normal weight according to BMISDS had ≥1 in WHtRSDS, representing 55% of all children with WHtRSDS≥1 (p < 0.001) (Table 2). In these 55% of the children, the crude WHtR values were between 0.51 and 0.56 compared to 0.51 and 0.66 in the group with overweight/obesity and WHtRSDS ≥1.

Table 2 Correlation between WHtRSDS and BMISDS in children at 60 months of age

In further analyses, we compared the subgroup of children with normal weight according to BMISDS and ≥1 in WHtRSDS at 5 years, to children with overweight/obesity and ≥1 in WHtRSDS at the same age. We found that the group of children with normal BMISDS and elevated WHtRSDS had a significantly lower mean birth weight, 3504 g vs. 3725 g (p < 0.001), and 56% of the children were girls compared to 59% girls (p = 0.143) in the group with overweight/obesity and an elevated WHtRSDS. When comparing the growth patterns between 0 and 5 years in the two groups, it was shown that the subgroup of children with normal weight according to BMISDS and an elevated WHtRSDS had lower mean BMISDS values (p < 0.05) at every measurement point when compared to the children with overweight/obesity and an elevated WHtRSDS. Their mean BMISDS passed 1, the cutoff for overweight only at the 3–4 months measurement point, compared to at 3–4, 36, 48, and 60 months in the group with overweight/obesity and an elevated WHtRSDS. The mean WHtRSDS values in the two groups differed significantly first at the last two measurement points where the group with overweight/obesity and an elevated WHtRSDS had higher values (p < 0.05).

BMISDS growth patterns for children with normal or elevated WHtRSDS at 5 years of age

Boys and girls with WHtRSDS ≥1 at 5 years of age had significantly higher mean BMISDS than children with <1 in WHtRSDS at every measurement point. The boys passed the 1 SDS line at ~48 months and the girls passed it at ~54 months (Fig. 1, Table 3). Children with <1 in WHtRSDS remained relatively stable at all measurement points without any upward SDS line crossing.

Fig. 1
figure1

Growth patterns based on mean body mass index standard deviation scores (BMISDS) (a, b) and mean waist-to-height ratio standard deviation scores (WHtRSDS) (c, d) from 0 to 60 months and by gender, in children classified according to Swedish WHtRSDS reference values at 60 months of age.27 Blue lines represent children with WHtRSDS ≥1, green lines represent children with WHtRSDS <1 at 5 years

Table 3 Mean differences in BMISDS over time and by gender between combinations of children with WHtRSDS ≥1 or <1 at 60 months of age

In the BMISDS graphs, both boys and girls in both of the WHtRSDS groups had a peak in BMISDS at the 3–4 months measurement point (Fig. 1).

WHtRSDS growth patterns for children with normal or elevated WHtRSDS at 5 years of age

Children with WHtRSDS ≥1 at 5 years of age had significantly higher mean WHtRSDS than children with <1 in WHtRSDS at every measurement point, except at the first measurement point in the girls. The boys crossed the 1 SDS line between 36 and 48 months and the girls crossed it at ~48 months. (Fig. 1, Table 4). Children with <1 in WHtRSDS remained relatively stable at all measurement points without any upward SDS line crossing.

Table 4 Mean differences in WHtRSDS over time and by gender between combinations of children with WHtRSDS ≥1 or <1 at 60 months of age

Discussion

In the present study, consisting of 1540 Swedish preschool children we examined BMISDS and WHtRSDS growth patterns and their association, in children classified according to WHtRSDS at 5 years of age. The main finding was that 55% of children with WHtRSDS ≥1 at 5 years of age had normal BMISDS. This may be worrying, since in children 6 years and older, a WHtR value of 0.5 has been recommended as a cutoff for central obesity and cardiometabolic risk factors.19,21 All children with WHtRSDS ≥1 in our study had crude WHtR values ≥0.51. Khoury et al.,30 recently showed that children aged 5–18 years had a worsened cardiometabolic risk and a higher frequency of cardiometabolic risk factors, with increasing values in WHtR. In their study, the children were classified into three groups based on WHtR values, <0.5, 0.5 to <0.6 and ≥0.6. Since the children in our study with WHtRSDS ≥1 all had values ≥0.51, also children in our cohort may have risk factors associated with abdominal adiposity.

When studying BMISDS and WHtRSDS growth patterns, we found that children with WHtRSDS ≥1 at 5 years had significantly higher mean BMISDS and WHtRSDS from an early age, when compared to children with values below 1. This shows that some correlation between WHtR and BMI exist during the 5-year period.

When specifically studying BMISDS growth patterns in the subgroup of children with a normal BMISDS and an elevated WHtRSDS at 5 years, it was shown that they had lower mean BMISDS at every measurement point in comparison with children with overweight/obesity and an elevated WHtRSDS. They passed 1 SDS in BMI only at the 3–4 months measurement point. This suggests that BMI besides being unable to identify most of the children with an elevated WHtRSDS at 5 years, also failed to identify them at most of the time points during the 5-year period.

Our study indicates that when BMI is used alone as a measure of overweight and obesity, children with elevated waist-to-height ratio who may need further investigation regarding cardiometabolic risk factors may be missed. This is in line with studies that have found WHtR to be better than BMI in assessing cardiometabolic risk factors.21,30,31 There are also studies that contradict these results.32,33 The benefits with the use of WHtR may also differ in children with overweight compared with those in children with obesity. Morandi et al. have shown that WHtR, WC, BMI, and Z-BMI were not good predictors of metabolic impairments in obese adolescents.34 Future studies in preschool children may reveal if this applies to children with obesity in this age group as well.

The association between cardiometabolic risk factors and abdominal adiposity in preschool children is not clear. In school children, insulin sensitivity has been shown to be negatively correlated with abdominal subcutaneous adipose tissue (SAT) and not with abdominal visceral adipose tissue (VAT),35 suggesting that abdominal SAT is an important risk factor. In 5-year-old children, measurements of WC have been shown to correlate with abdominal SAT but not with VAT when verified by MRI.36 This indicates that WHtR may be an important measure in early identification of children who may need further investigation regarding cardiometabolic risk factors. The measurements and calculations needed for WHtR are easily made and reproduced,14,19,37 and anthropometric measures are cost effective alternatives in screening of individuals at risk for the MetS.12,13

Our results indicate that WHtR in preschool children adds value regarding identification of central obesity, which represents an important risk factor in the MetS. The MetS have been shown to originate already at the onset of overweight or obesity in young children,6,38 and screening for risk factors during preschool age have recently been suggested in other studies as well.6,8 However, more studies regarding the association between abdominal fat associated with cardiometabolic risk factors are needed in the youngest children. Since the cutoff value 0.5 in WHtR for central obesity associated with cardiometabolic risk is recommended for children 6 years and older, clinically relevant values for children below 6 years are needed as well.

Since it has been shown earlier that children born SGA often develop central obesity later in life,39 we expected a higher proportion of children born SGA in the WHtRSDS ≥1 groups than in the other groups, this was not the case, and may depend on the relatively small number of children born SGA in these groups due to the population-based design of the study.

The peak in BMISDS that was observed in the BMISDS graphs at 3–4 months in both boys and girls indicates a difference at that age between the Swedish reference and the study population. This difference was also observed in another Swedish study, who compared their data with the current Swedish BMI reference.40 The reason for this difference is not yet clear, it may be due to smoothing of the data in the Swedish reference or due to a secular trend in the studied population compared to the reference population.

A major limitation of the current study was our absence of measures of body fat distribution for validation of WHtR and BMI in this child cohort. We also lack data regarding cardiometabolic risk factors. This information would have been able to confirm if children with an elevated WHtR had signs of the MetS already at these young ages. Another limitation of the current study was that we had to exclude children because of missing growth data or because they were measured outside our decided age limit, they could represent a possible bias. This was mainly due to the inclusion of only measurements close to the measurement points, and wider limits for this would affect precision. The main strength of this study was the population-based longitudinal design, as longitudinal studies of BMI and WHtR in the preschool population still are limited.

In conclusion, we found that every second child with a WHtRSDS of ≥1 at 5 years of age were normal weight according to BMISDS. Our results indicate that WHtR to a large extent identifies other children than BMI does. Abdominal adiposity is an important risk factor in the metabolic syndrome, and it has been shown in other studies that children as young as 5 years with elevated WHtR may have cardiometabolic risk factors. Therefore, our results suggest that WHtR adds value in identifying children with abdominal adiposity who may need further investigation regarding cardiometabolic risk factors.

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Acknowledgements

We are grateful to the children and their parents for participating in this study, and the nurses at the child health care centers for data collection. This work was supported by grants from Region Halland, Research and Development Center Spenshult, Her Royal Highness Crown Princess Lovisa’s Association for Child Care/Axel Tielmans Memorial Fund and Halmstad University.

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Each author has met the Pediatric Research authorship requirements. J.R., J.D., G.A.T., B.A., S.B., A.B., C.S.N., and A.L. have contributed substantially to conception and design of the study. J.R., J.D., G.A.T., B.A., and S.B. have contributed substantially to the acquisition of data. A.L., J.R., J.D., and S.B. have analysed and interpreted the data. All authors have revised the manuscript critically for important intellectual content and have had final approval of the version to be published.

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Correspondence to Annelie Lindholm.

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Lindholm, A., Roswall, J., Alm, B. et al. Body mass index classification misses to identify children with an elevated waist-to-height ratio at 5 years of age. Pediatr Res 85, 30–35 (2019). https://doi.org/10.1038/s41390-018-0188-4

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