High body mass index, overweight, and obesity in

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There are many different BMI references that can be used to ... Different reports may use the same term but define it quite differently. ... Strictly speaking, obesity refers to excess body fatness and .... Monteiro, 2006; Del-Rio-Navarro et al., 2007; Inokuchi et al., .... et al., 2003; Huerta et al., 2007; Jackson et al., 2007; Janssen.
High body mass index, overweight, and obesity in children: Definitions, terminology, and interpretation University Press Scholarship Online Oxford Scholarship Online Childhood Obesity Prevention: International Research, Controversies and Interventions Jennifer A. O'Dea and Michael Eriksen

Print publication date: 2010 Print ISBN-13: 9780199572915 Published to Oxford Scholarship Online: January 2011 DOI: 10.1093/acprof:oso/9780199572915.001.0001

High body mass index, overweight, and obesity in children: Definitions, terminology, and interpretation Katherine M. Flegal Cynthia L. Ogden

DOI:10.1093/acprof:oso/9780199572915.003.0001

Abstract and Keywords Studies in a variety of countries have shown increases in the prevalence of overweight and obesity among children in recent years. These increases have given rise to concern about children's health and well-being. The terminology used in these studies varies considerably. However, whatever the terminology used, such studies are generally based on weight (expressed as body mass index (BMI), a measure of weight for height, calculated as weight in kilograms divided by the square of height in meters) and not on body fatness per se. There are many different BMI references that can be used to define childhood overweight or obesity for population surveillance purposes using a variety of BMI cut-points. BMI is a screening tool, not a diagnostic tool. Children with a BMI over these cut-points do not necessarily have clinical Page 1 of 29

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High body mass index, overweight, and obesity in complications or health risks related to over-fatness. More inchildren: Definitions, terminology, and depth assessment of individual children is required to ascertain health status. The definitions based on BMI interpretation generally used are working definitions that are valuable for general public health surveillance, screening, and similar purposes. Terminology and measures used in studies of weight and adiposity in children and in adults is a complex area. Considerable confusion arises from the disparate uses of the descriptive terms ‘overweight’ and ‘obesity’ in children. Different reports may use the same term but define it quite differently. This chapter examines some of the definitions and terminology in use today and some of the underlying issues in arriving at consistent and coherent definitions. Keywords:   body mass index, BMI, overweight, obesity, children, diagnosis, measurement, interpretation

Chapter summary Studies in a variety of countries have shown increases in the prevalence of overweight and obesity among children in recent years. These increases have given rise to concern about children’s health and well-being. The terminology used in these studies varies considerably. However, whatever the terminology used, such studies are generally based on weight (expressed as body mass index (BMI), a measure of weight for height, calculated as weight in kilograms divided by the square of height in meters) and not on body fatness per se. There are many different BMI references that can be used to define childhood overweight or obesity for population surveillance purposes using a variety of BMI cut-points. BMI is a screening tool, not a diagnostic tool. Children with a BMI over these cut-points do not necessarily have clinical complications or health risks related to over-fatness. More indepth assessment of individual children is required to ascertain health status. The definitions based on BMI generally used are working definitions that are valuable for general public health surveillance, screening, and similar purposes.

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High body mass index, overweight, and obesity in Introduction children: Definitions, terminology, and Terminology and measures used in studies of weight and interpretation adiposity in children and in adults is a complex area. Considerable confusion arises from the disparate uses of the descriptive terms ‘overweight’ and ‘obesity’ in children. Different reports may use the same term but define it quite differently. In this chapter, we examine some of the definitions and terminology in use today and some of the underlying issues in arriving at consistent and coherent definitions. Strictly speaking, obesity refers to excess body fatness and overweight to weight in excess of a weight standard. In practice, measurement of body fat is difficult both in clinical applications and in population studies. In addition, there are no well-accepted standards for body fatness for children (or for adults) (WHO Expert Committee on Physical Status: The Use and Interpretation of Anthropometry, 1995). As a result, although many discussions revolve around the effects of excess fat, a measure of weight rather than fatness is almost always used. The most common metric in use today is body mass index (BMI), weight in kilogram divided by the square of height in meters. This index was originally devised by the Belgian statistician Adolphe Quetelet (1796–1874), who applied it to adults, not to children (Weigley, 2000). For adults, the index describes the relation of weight to height, in effect adjusting weight for height. It was subsequently shown for adults that if adiposity was independent of height, then BMI would be highly correlated with (p.4) adiposity (Benn, 1971; Keys et al., 1972; Khosla & Lowe, 1967). For adults, BMI provides a way to translate weights at different heights into a common metric. The use of BMI for children is a more recent development (Cole, 1979; Dietz & Robinson, 1998; Neovius et al., 2004). For children, BMI varies with age. Because of this, for children, BMI values are compared to reference values that are generally age- and usually also sex-specific and need to be further transformed in order to be put on a common footing. This is most often done by translating BMI-for-age into a zscore or a percentile relative to some specified distribution of BMI-for-age. Generally some smoothing process is applied to an empirical BMI distribution to generate smooth percentiles,

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High body mass index, overweight, and obesity in and because BMI distributions are not infrequently skewed, a children: Definitions, terminology, and normalizing transformation is also applied, often as part of the smoothing process itself (Cole, 1990). interpretation A normalizing transformation allows for flexible calculation of z-scores. A z-score or standard deviation score represents the number of standard deviation units above or below the mean, so that, for example a z-score of 2 refers to a value that is two standard deviations above the mean. To calculate a z-score value, a normal transformation of the distribution of BMI for that age and sex group is applied and the z-score is calculated relative to the mean and standard deviation of the normalized BMI distribution. Z-scores and percentiles have a 1 to 1 equivalence in a normal distribution; any percentile can be translated to a z-score and vice versa. At a given age, a specified z-score interval represents the same difference in normalized BMI units at any z-score level, unlike percentiles (WHO Expert Committee, 1995, p. 176). However, if BMI distributions are skewed, as they not infrequently are, then a specified z-score interval does not represent a constant difference in absolute BMI units at a given age. In addition, to the extent that standard deviations vary across ages, a specified interval between two z-scores may represent a difference in absolute BMI units that is not constant across ages. The effect is that a BMI z-score or percentile reflects an extensive series of transformations of the original weight and height data for a child. Weight and height are transformed into a BMI value and the BMI value in turn is transformed into an age- and sex-specific z-score based on a normalizing transformation of a smoothed version of observed reference data. A BMI z-score or percentile represents a measure of weight, adjusted for height, sex, and age, relative to a smoothed reference distribution, and not simply a measure of weight and height for a child. Not surprisingly, as body weight is correlated with fat mass and percentage body fat, BMI also tends to be correlated with percentage body fat (Wellens et al., 1996). However, as body weight is also correlated with muscle and lean mass, BMI tends to be correlated with muscle and lean mass as well and may be correlated with height within age groupings. Thus BMI is correlated with fatness but is not a precise measure of fatness. Additional complexities arise with children, where the Page 4 of 29

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High body mass index, overweight, and obesity in indicator is not BMI itself, rather a sex- and age-specific children: Definitions, terminology, and percentile of BMI (Dietz & Bellizzi, 1999; Dietz & Robinson, 1998). The same BMI percentile does not represent the same interpretation percentage body fatness at different ages, for boys and girls, or among different race-ethnic groups. A BMI-for-age above a given value may be labeled obesity, but it is still a measure of excess weight, not necessarily of excess fat. Because of the wide variation in terminology, in this chapter we sometimes refer to ‘high BMI-for-age’ rather than to overweight or obesity. Reference data sets

High BMI-for-age is defined relative to a reference distribution of BMI. There are numerous reference data sets for BMI in childhood. In many countries, BMI reference data are used or recommended as part of monitoring children’s growth (Al-Isa & Thalib, 2008; Ben et al., 2008; Cacciari et al., 2002; Cacciari et al., 2006; Cole et al., 1995; Cole & Roede, 1999; Conde & Monteiro, 2006; Del-Rio-Navarro et al., 2007; Inokuchi et al., 2006; Ji, 2005; Kato et al., 2008; Kuczmarski et al., 2000; (p.5) Mast et al., 2002; Ozturk et al., 2008; Rolland-Cachera et al., 1991; Savva et al., 2001; Williams, 2000). Such reference data are often based on representative data from a given country. For example, data for weight, height, BMI, and head circumference from 37,000 children from surveys representative of England, Scotland, and Wales were used to develop the 1990 British growth reference (Cole et al., 1998). In the United States, the Centers for Disease Control and Prevention (CDC) 2000 growth charts for the U.S. were developed from five nationally representative survey data sets (the National Health Examination Surveys II and III in the 1960s, the National Health and Nutrition Examination Survey (NHANES) I and II in the 1970s, and NHANES III, 1988–94) (Kuczmarski et al., 2002). They include sex-specific BMI-forage growth curves for ages 2 through 19 years by single month of age (Kuczmarski, et al., 2002). All weight data from children ages 6 and above in 1988–94 were excluded because of the observed increase in weight in those years (Troiano & Flegal, 1998). The 2000 CDC charts are revised versions of the 1977 National Center for Health Statistics (NCHS) growth charts (Kuczmarski, et al., 2002).

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High body mass index, overweight, and obesity in In 2006 the World Health Organization (WHO) released a new children: Definitions, terminology, and set of growth charts for children from birth to 5 years of age, based on data from the Multicentre Growth Reference Study interpretation (MGRS) conducted by WHO (WHO, 2006). The WHO charts are based on different principles from the aforementioned national growth charts. The WHO charts are intended to serve as growth standards, describing how children should grow. In contrast, national charts are generally descriptive, describing how children in the reference population did grow. The WHO charts are based on a selective sample of children from six sites around the world, consisting of children who were not subjected to socioeconomic constraints on growth, who were healthy term singleton births, whose mothers did not smoke before or after pregnancy, and who were fed according to MGRS feeding recommendations for breast and complementary feeding. The growth of these children was considered to represent optimal growth. Although the children were selected in a different fashion than for other national and international references, the WHO charts are otherwise constructed along similar lines to other charts and consist of descriptive percentiles from this select population. WHO subsequently used most of the same NHANES data that had been used for the CDC growth charts in order to develop a growth reference for older children and adolescents (de Onis et al., 2007), with modifications to delete the heavier children in the NHANES data sets. Reference sets of charts, such as the 1990 UK reference, the 2000 CDC Growth Charts and the WHO charts, are intended for clinical use in monitoring children’s growth over the entire range of growth. For example, an important use of the WHO charts is to monitor and assess acute undernutrition (Seal & Kerac, 2007). The use of selected percentiles of such charts to define overweight and obesity is a secondary purpose. There are also several sets of BMI reference data that are intended specifically to define childhood overweight or obesity, rather than to be used for clinical monitoring of growth patterns. These include only a few cut-off values. One reference set of BMI values that has been widely used consists of sex-specific smoothed 85th and 95th percentiles for single year of age from 6 to 19 years, based on data from the first National Health and Nutrition Examination Survey (NHANES I, 1971–74) in the United States, developed by Must et al. (Must et al., 1991). In 1995, a WHO Expert Committee Page 6 of 29

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High body mass index, overweight, and obesity in recommended the use of these reference values (WHO Expert children: Definitions, terminology, and Committee on Physical Status: the Use and Interpretation of Anthropometry, 1995). Although the 1991 Must et al. reference interpretation values were considered to represent the 85th and 95th percentiles of the distribution of BMI in NHANES I, in fact, because of some slight oversmoothing of the data for girls, the Must et al. values for the 85th percentile are systematically lower than the empirical 85th percentile from the same data set and are more similar to the 80th percentile than to the 85th (Flegal, 1999). (p.6) As a result when the Must et al. values are used the prevalence of BMI above the 85th percentile tends to be high for adolescent girls. In 2000, Cole and colleagues published a set of smoothed sexspecific BMI cut-off values based on six nationally representative data sets from Brazil, Great Britain, Hong Kong, the Netherlands, Singapore, and the United States (Cole et al., 2000). The U.S. data used were the same as those from which the 2000 CDC growth charts were derived, excluding NHANES III data. The selection of data sets was based on specified criteria including a large nationally representative sample, minimum age ranges of 6 to 18 years, and appropriate quality control. These values, often referred to as the International Obesity Task Force (IOTF) cut-off values, represent cut-off points chosen as the percentiles that matched the adult cut-offs of a BMI of 25 and 30 at age 18 years. The IOTF, then headquartered at the Rowett Research Institute (UK), was an ad hoc independent group of scientists from different countries that was constituted in 1996 with the mission to inform the world about the urgency of the problem of obesity and to persuade governments to act. (The IOTF later merged with the International Association for the Study of Obesity.) The Cole (IOTF) reference grew out of a 1997 workshop held by the IOTF and was developed to provide a suggested common basis for prevalence estimates internationally. The goal was to develop BMI criteria that could be used for international comparisons of prevalence without depending on using solely U.S. reference data and without using a specified percentile, such as the 85th or 95th percentile of a specific population. The IOTF cut-offs were not intended as clinical definitions and were not intended to replace national reference data, but rather to provide a common set of definitions that researchers and policy makers Page 7 of 29

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High body mass index, overweight, and obesity in in different countries could use for descriptive and children: Definitions, terminology, and comparative purposes internationally. It should be further noted that the IOTF recommendations were based on a small interpretation number of data sets that were available at the time and were not intended as a comprehensive or final analysis. Several discussions on the use of national versus international reference data have been published (Chinn & Rona, 2002; Reilly, 2002; Onyango, 2008).

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High body mass index, overweight, and obesity in Selection of cut-off values children: Definitions, terminology, and In adults, the cut-offs to define obesity or overweight are based on fixed BMI values approximately related to health risk interpretation (NIH, 1998). In children there are no risk-based fixed values of BMI used to determine cut-off values, because it is unclear what risk-related criteria to use. The long time span before most adverse outcomes appear makes finding risk related cutoffs difficult (Ayer & Steinbeck, 2010; Lloyd et al., 2010). Consequently, in childhood statistical definitions of high BMIfor-age in terms of percentiles or z-scores relative to a specified reference population are often used to define high BMI-for-age (Barlow & Dietz, 1998; Himes & Dietz, 1994). Despite their common use, the rationale for using the 85th and 95th percentiles has not been very clearly spelled out. In terms of z-scores, for younger children WHO has defined obesity as a z-score above 3 and overweight as a z-score above 2, but not with an explicit justification for these precise cut-off values (World Health Organization, 2008). Cut-off values are not necessarily exact. For both adults and children, many cutoff values of percentiles or z-scores for BMI end in 5 or 0. The propensity to choose values ending in 5 or 0 has been repeatedly noted in studies of blood pressure measurements and has been demonstrated to occur in other situations, including clinic arrival times and even in pathology reports (Hayes, 2008, 2009; Himes, 1999). This digit preference may also affect the choice of cut-off values for BMI. One feature of statistical definitions that has been little remarked on is that they include the assumption that in the reference population, the prevalence is exactly the same for every sex and age group. For example, if obesity is defined as a BMI-for-age at or above the 95th percentile, then in the reference population, 5% of 6-year-olds are considered obese, 5% of 7-year-olds are considered obese, and so forth up to 5% of 19-year-olds. This is also the case with the definitions that are keyed (p.7) to the adult BMI values of 25 and 30 at age 18. Those definitions are also percentiles that are constant over age and sex in the reference distribution, even though the exact percentile level is not specified. The variety of reference data and cut-off values mean that there is a plethora of different definitions of childhood overweight or obesity for calculating prevalence estimates. Numerous articles have compared the use of different Page 9 of 29

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High body mass index, overweight, and obesity in definitions with the same population (Abrantes et al., 2003; Alchildren: Definitions, terminology, and Sendi et al., 2003; Chinn & Rona, 2002; Flegal et al., 2001; Fu et al., 2003; Huerta et al., 2007; Jackson et al., 2007; Janssen interpretation et al., 2005; Kain et al., 2002; Mei et al., 2008; O'Neill et al., 2007; Serra-Majem et al., 2007; Telford et al., 2008; Valerio et al., 2003; Vidal et al., 2006; Vieira et al., 2007; Wang & Adair, 2001; Wang & Wang, 2002; Willows et al., 2007; Yngve et al., 2008; Zimmermann et al., 2004). For example, in one analysis, three different sets of BMI reference values were used to estimate the prevalence of overweight among children in the United States (Flegal et al., 2001). The three sets of BMI reference values resulted in similar but not identical estimates (Flegal et al., 2001). For young girls, estimates based on the Must et al. reference values (1991) were much higher than estimates based on the CDC (Kuczmarski et al., 2002) and Cole (2000) references. The Cole (IOTF) reference gave rise to lower estimates for young children and higher estimates for older children than the Must and CDC references. As seen repeatedly, the various definitions do not give the same results. The direction of the difference between two definitions for a given age and sex value can be determined simply by comparing the BMI values for the two definitions, but this does not show the average effect on prevalence estimates over a broader age range or the magnitude of the effect.

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High body mass index, overweight, and obesity in Terminology children: Definitions, terminology, and The terminology used in different studies varies considerably. Some refer to ‘overweight’, some to ‘obesity’ and some to ‘at interpretation risk for overweight’. Even when the same term is used (e.g. ‘overweight’) the meaning of that term is often not the same in different countries or across studies. In 1995 a WHO expert committee listed ‘heaviness’ as a descriptive term to describe high BMI and noted that the term ‘overweight’ used for high BMI implied obesity (WHO Expert Committee, 1995, p. 163). The convention of using the term overweight for BMI levels indicative of possible obesity was also followed by several expert committees in the United States in the 1990s (Barlow & Dietz, 1998; Himes & Dietz, 1994). These committees recommended using a BMI-for-age at or above the 95th percentile of a specified reference population to screen for obesity in adolescents and younger children, noting that these values were not designed to provide clinical cut-points, but rather to serve as screening values. The committee recommendations were that children and adolescents with BMI values at or above the 95th percentile of a suitable reference population undergo an in-depth assessment, stating that ‘in-depth assessments are required to distinguish positively screened adolescents who are truly obese, to identify underlying diagnoses and to provide a basis for prescribing treatment’. The 1994 expert committee drew a distinction between overweight and obesity. According to their report (Himes & Dietz, 1994), ‘The committee reserved the use of the term obesity for a condition characterized by excess body fat. … the committee elected to define excess body mass as overweight and to rely on additional measures to distinguish those who are obese from those who are overweight but may not be obese’. The same expert committees considered that children with BMI values between the 85th and 95th percentiles might also possibly be obese, although with a lower probability. Thus for these children, it was recommended that they be referred to a second-level screen, including consideration of family history, blood pressure, total cholesterol, large prior increment in BMI, and concern about weight. These children would be referred for the in-depth evaluation only if they were positive for any of the items on the second-level screen. The committees used the Page 11 of 29

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High body mass index, overweight, and obesity in designation of ‘at risk for overweight’ for BMI values children: Definitions, terminology, and between the 85th and the 95th percentiles of BMI for age. Although this is sometimes interpreted as a designation for a interpretation (p.8)

child who is at risk for becoming overweight in the future, that was not the original intention of the term. The category as defined by the expert committees (Barlow & Dietz, 1998; Himes & Dietz, 1994) was intended to identify children who might be obese, in the sense of excess body fat, but who should undergo a second-level screen (as described earlier) to evaluate whether they should be referred for an in-depth assessment. The term ‘possible risk of overweight’ has been used in a similar sense by WHO (2008). Following these expert committee recommendations, in the U.S., ‘overweight’ was defined as a BMI at or above the 95th percentile of the 2000 CDC growth charts, and ‘at risk for overweight’ was defined as a BMI between the 85th and the 95th percentile (Hedley et al., 2004; Ogden et al., 2002; Troiano & Flegal, 1998). Changes in terminology

More recent changes in terminology have been undertaken to be consistent with adult terminology and to emphasize the seriousness of the problem of high BMI among children, consistent with research indicating the importance of the role that medical language plays in perceptions of illness (Young et al., 2008). The Institute of Medicine report on ‘Preventing Childhood Obesity’ (Koplan et al., 2005) retained the 95th percentile as a cut-off value, but changed the terminology, stating that, ‘The committee recognizes that it has been customary to use the term “overweight” instead of “obese” to refer to children with BMI values above the age- and genderspecific 95th percentiles However, the term “obese” more effectively conveys the seriousness, urgency, and medical nature of this concern than does the term “overweight,” thereby reinforcing the importance of taking immediate action’. Following along these lines, a subsequent expert committee convened by the American Medical Association (Krebs et al., 2007) retained the two cut-off values of the 85th and 95th percentile recommended by previous committees but used different terminology, referring to BMI-for-age from the 85th up to the 95th percentile as ‘overweight’ and to BMI-forage at or above the 95th percentile as ‘obesity’, stating that ‘The compelling reasons for this revision are clinical. The term obesity denotes excess body fat more accurately and reflects

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High body mass index, overweight, and obesity in the associated serious health risks more clearly than does the children: Definitions, terminology, and term overweight, which is not recognized as a clinical term for high adiposity’. interpretation With these definitions, the two categories of overweight and obesity are mutually exclusive. As a result, the definition of overweight as a BMI-for-age at or above the 95th percentile by the 1994 committee and the definition of overweight by the 2007 committee as a BMI-for-age between the 85th and 95th percentile have no overlap. In further recognition of the importance of language, the committee also recommended the use of more ‘neutral’ terms when discussing weight issues with families, stating that ‘Therefore, the expert committee recommends the use of the clinical terms overweight and obesity for documentation and risk assessment but the use of different terms in the clinician’s office, to avoid an inference of judgment or repugnance.’ Some concerns have been raised regarding the possible adverse effects of labeling and stigmatization (Krebs et al., 2007; Whitlock et al., 2005). However, in 2005, the U.S. Preventive Services Task Force (USPSTF) found no direct evidence to make conclusions about potential harms, such as poorer selfconcept or disordered eating, from screening (Whitlock et al., 2005). Barriers to consensus

The issue of different definitions is not new but has been discussed extensively in various previous publications (for example Neovius et al., 2004). Guillaume’s summary from 1999 still applies today: ‘Available data allow neither a meaningful international estimation of the prevalence of (p.9) obesity nor international comparisons. Although associated with considerable problems, this situation can be improved with an international consensus which, by necessity, will be riddled with uncertainties and compromises’. (Guillaume, 1999). Although there are many different proposals, guidelines, and recommendations, a basic problem is the lack of strong evidence for any precise definition. The Endocrine Society clinical practice guidelines (August et al., 2008) make a strong recommendation for classifying children as overweight if their BMI is between the 85th and 95th percentiles and as obese if their BMI is at or above the 95th, but in contrast to the Page 13 of 29

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High body mass index, overweight, and obesity in strength of the recommendation, they describe the evidence children: Definitions, terminology, and for this recommendation as of ‘very low quality’. The U.S. Preventive Services Task Force report (Whitlock et al., 2005) interpretation summarized the considerable gaps in knowledge of the links between childhood weight and future health outcomes. One result of these gaps in knowledge is that the implications of a specific level of BMI for children’s future health are unclear. This was noted in the expert committee report (Himes & Dietz, 1994) published in 1994: ‘Unfortunately, little published information exists regarding specific degrees of overweight in adolescence and current or subsequent healthrelated outcomes …. Further, because of the low prevalence of the sequelae of obesity among adolescents, specific cutoff values for BMI or other measures of overweight in adolescence associated with health risks have not been established’. The same concern was echoed in 2005 in a commentary by the Childhood Obesity Task Force of the U.S. Preventive Services Task Force (Moyer et al., 2005), which stated: ‘We do not know the best way to identify children who are at risk for future adverse health outcomes due to obesity or overweight. Although BMI is a convenient and widely agreed-on measure of obesity, it is not clear what BMI at any given age is associated with future good health’. Reviews by Reilly (Reilly et al., 2003) and by Must and Strauss (Must & Strauss, 1999) delineate the numerous health risks associated with high BMI in children. Higher BMI among children is associated with higher levels of blood pressure, serum lipids, and other factors (Freedman et al., 1999) that in adults are associated with higher cardiovascular risk. Evidence linking children’s BMI levels to adult cardiovascular disease is limited and raises many methodological issues (Ayer & Steinbeck, 2010; Baker et al., 2007; Bibbins-Domingo et al., 2007; Lloyd et al., 2010). Increases in type 2 diabetes among children are of concern. However, available evidence suggests that the prevalence is still quite low and that many of these cases occur in children with very high BMIs, often in the range of 35 to 40, that would be considered grade 2 or grade 3 obesity in adults (Goran et al., 2008). A recent estimate of the incidence of type 2 diabetes among children in the UK arrived at an estimate of 0.53 cases per 100,000 children per year (Haines et al., 2007). Some research tracking childhood BMI Page 14 of 29

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High body mass index, overweight, and obesity in over time has suggested that the trajectory of BMI change children: Definitions, terminology, and may be a more important indicator of risk for adult disease than a given BMI at any one point in time. For example interpretation Bhargava et al. (2004) found that ‘Subjects with impaired glucose tolerance or diabetes typically had a low body-mass index up to the age of two years, followed by an early adiposity rebound (the age after infancy when body mass starts to rise) and an accelerated increase in body-mass index until adulthood. However, despite an increase in body-mass index between the ages of 2 and 12 years, none of these subjects were obese at the age of 12 years’. Similarly Barker et al. (2005) found that ‘The mean body size of children who had coronary events as adults was below average at birth. At two years of age the children were thin; subsequently, their bodymass index (BMI) increased relative to that of other children and had reached average values by 11 years of age’. Uses of these classifications

Definitions of overweight and obesity are used for several different purposes. For use within a single country for public health purposes such as surveillance, often a national reference will be (p.10) more suitable, allowing for comparison of children to a reference group of children from the same country. For international comparisons of prevalence, a consistent definition should be used across countries. However, it is not yet clear that any one definition is better than another for this purpose. A given definition may be more suitable for one country than for another country. Furthermore, given the limitations of BMI as a measure of body fatness and the likely variation by not only age and sex but also by race-ethnic groupings, any international comparisons should be interpreted cautiously, particularly those between dissimilar countries. The WHO charts are based on a sample selected to represent normal growth in healthy children but nonetheless suffer from some of the same issues that affect other definitions, including the use of BMI as an imperfect measure of adiposity and the difficulty in choosing an appropriate cut-off value. The IOTF definitions resolve the issue of choosing a cut-off value by linking to the adult levels, but this linkage serves only to choose the percentiles used as cut-off values and does not substitute for a functional definition. In general, although ‘overweight’ and ‘obesity’ are useful descriptive terms, it might be useful to consider ways of

Page 15 of 29

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High body mass index, overweight, and obesity in making more comprehensive comparisons of BMI distributions children: Definitions, terminology, and across countries without or in addition to these descriptive terms. interpretation Children are defined as overweight or obese for population surveillance and screening purposes, using a variety of BMI cut-points. However, these children do not necessarily have clinical complications or health risks related to over-fatness. According to the Centers for Disease Control and Prevention (Centers for Disease Control and Prevention): ‘In-depth assessments are required to determine if children and adolescents with BMI-for-age 〉 95th percentile are truly overfat and at increased risk for health complications’. Consistent with this approach, in the UK, different cut-off values are used for clinical use than for surveillance. The clinical guideline published by the National Institute for Health and Clinical Excellence (NICE) defined overweight and obesity for clinicians as the 91st and 98th percentiles, respectively (NICE, 2006). For purposes of surveillance, however, the 85th and 95th percentiles are used for government statistics (Jotangia et al., 2005). For specific conditions, BMI is an important part of a screening algorithm. For example, the American Diabetes Association (2000) recommends screening for diabetes in children with BMI at or above the 85th percentile and have in addition two of the following factors: 1) family history of type 2 diabetes; 2) membership in specified race-ethnic groups (American Indians, African Americans, Hispanic Americans, Asians/South Pacific Islanders); 3) signs of insulin resistance. For dyslipidemia, it is recommended that all children with BMI-for-age at or above the 85th percentile should be screened (Daniels & Greer, 2008). Despite recommendations that BMI be considered as a screening, rather than as a diagnostic tool (Barlow, 2007), BMI-based categories may be considered as diagnoses (for example, Benson et al., 2009), perhaps encouraged to some extent by recommendations for the use of clinical terminology. The use of BMI as part of a screening algorithm does not in fact require a particular definition or a particular label and can be separate from any definitions used for prevalence estimates. Considerable research efforts have been devoted to how to choose cut-points for screening, which is generally done taking into account the expected yield and a balance of Page 16 of 29

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High body mass index, overweight, and obesity in costs and benefits. Interventions are designed to reduce the children: Definitions, terminology, and risk of future events, and it might be decided to intervene in a given way for a given BMI level again without the need for a interpretation label. Current and future research efforts continue to address the relationship between BMI and body fat in the general population and in different race/ethnic groups. These efforts may clarify the use of BMI as an indicator of body fatness in children, as well as of the value of indicators other than BMI, such as waist circumference. Research continues on the development of risk-based cut-points. The percentile or z-score cut-points have digit preference, are statistically based, and are not based on a priori health risk. In addition, because the relationship between BMI and adiposity (p.11) varies by sex, age, and race/ethnicity, risk-based cut-points may also vary. It might be useful to consider what BMI cut-points best predict future health risks and how efficiently to screen for such risks. The answers may be different for different populations. In addition, rather than depending solely on BMI to make screening decisions, it is likely to be useful to also consider other factors, including not only race-ethnicity, sex, and age, but also factors such as family history. Further examination of the relation between various health measures and BMI measured on a continuous basis may provide additional valuable information (Bell et al., 2007). There has also been recent interest in extremely obese children, in part in the context of possible bariatric surgery for adolescents (Inge et al., 2007). The current reference distributions for BMI are generally not very suitable for use in classifying or tracking very heavy children. Most reference data sets use data from several decades ago and have few very heavy children. In addition, several charts deliberately excluded the heaviest children. For example, in the construction of the WHO charts, the data were trimmed before constructing the charts specifically in order to exclude heavier children (2006). Similarly, in the construction of the CDC charts, it was decided not to use the most recent data because the children in that survey were heavier on average than children in earlier surveys (Kuczmarski et al., 2002). In general, data are sparse at the extremes of the BMI distributions and modelling data in the extreme tails is difficult. The use of cut-off z-scores as high as 3 represent the 99.8th percentile, which is difficult to estimate with any Page 17 of 29

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High body mass index, overweight, and obesity in precision. The current reference populations for BMI may not children: Definitions, terminology, and provide reasonable cut-points for extremely obese children. Expressing high BMI values as a percentage of the 95th interpretation percentile can provide a flexible approach to describing and tracking heavier children (Flegal et al., 2009).

Conclusions Continued efforts to evaluate existing references in terms of growth over the whole range of body sizes are valuable and should not be limited just to evaluation of overweight and obesity (Roelants et al., 2009). Evidence suggests that the associations of childhood BMI with adult disease may be related to growth trajectories, not necessarily to BMI at any one point in time. The continued use of BMI-based definitions has many practical advantages, including familiarity and relative ease of obtaining weight and height measurements. However, some of the limitations of such definitions should also be recognized, including the statistical rather than clinical definition of cut-off values and the approximate nature of BMI as a measure of body fatness. Despite their limitations, BMIbased definitions of overweight and obesity provide working practical definitions that are valuable for general public health surveillance and screening. References Bibliography references: Abrantes, M.M., Lamounier, J.A., & Colosimo, E.A. (2003) Comparison of body mass index values proposed by Cole et al. (2000) and Must et al. (1991) for identifying obese children with weight-for-height index recommended by the World Health Organization. Public Health Nutrition 6(3), 307–311. Al-Isa, A.N. & Thalib, L. (2008) Body mass index of Kuwaiti adolescents aged 10–14 years: reference percentiles and curves. Eastern Mediterranean Health Journal 14(2), 333–343. Al-Sendi, A.M., Shetty, P., & Musaiger, A.O. (2003) Prevalence of overweight and obesity among Bahraini adolescents: a comparison between three different sets of criteria. European Journal of Clinical Nutrition 57(3), 471–474. American Diabetes Association (2000) Type 2 diabetes in children and adolescents. Diabetes Care 23(3), 381–389. Page 18 of 29

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High body mass index, overweight, and obesity in August, G.P., Caprio, S., Fennoy, I., et al. (2008) children: Definitions, terminology, and Prevention and treatment of pediatric obesity: an endocrine society clinical practice guideline based on expert opinion. The interpretation (p.12)

Journal of Clinical Endocrinology and Metabolism 93(12), 4576–4599. Ayer, J. & Steinbeck, K. (2010) Placing the cardiovascular risk of childhood obesity in perspective. International Journal of Obesity 34(1), 4–5. Baker, J.L., Olsen, L.W., & Sorensen, T.I. (2007) Childhood body-mass index and the risk of coronary heart disease in adulthood. New England Journal of Medicine 357(23), 2329– 2337. Barker, D.J., Osmond, C., Forsen, T.J., Kajantie, E., & Eriksson, J.G. (2005) Trajectories of growth among children who have coronary events as adults. New England Journal of Medicine 353(17), 1802–1809. Barlow, S.E. (2007) Expert committee recommendations regarding the prevention, assessment, and treatment of child and adolescent overweight and obesity: summary report. Pediatrics 120(Suppl 4), S164–S192. Barlow, S.E. & Dietz, W.H. (1998) Obesity evaluation and treatment: Expert Committee recommendations. The Maternal and Child Health Bureau, Health Resources and Services Administration and the Department of Health and Human Services. Pediatrics 102(3), E29. Bell, L.M., Byrne, S., Thompson, A., et al. (2007) Increasing body mass index z-score is continuously associated with complications of overweight in children, even in the healthy weight range. The Journal of Clinical Endocrinology and Metabolism 92(2), 517–522. Ben, A.H., Jelidi, J., Bouguerra, R., et al. (2008) Tunisian children reference for body mass index and prevalence of obesity. Tunisian Medicine 86(10), 906–911. Benn, R.T. (1971) Some mathematical properties of weight-forheight indices used as measures of adiposity. British Journal of Preventive and Social Medicine 25(1), 42–50.

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High body mass index, overweight, and obesity in Benson, L., Baer, H.J., & Kaelber, D.C. (2009) Trends in the children: Definitions, terminology, and diagnosis of overweight and obesity in children and adolescents: 1999–2007. Pediatrics 123(1), e153–e158. interpretation Bhargava, S.K., Sachdev, H.S., Fall, C.H., et al. (2004) Relation of serial changes in childhood body-mass index to impaired glucose tolerance in young adulthood. New England Journal of Medicine 350(9), 865–875. Bibbins-Domingo, K., Coxson, P., Pletcher, M.J., Lightwood, J., & Goldman, L. (2007) Adolescent overweight and future adult coronary heart disease. New England Journal of Medicine 357(23), 2371–2379. Cacciari, E., Milani, S., Balsamo, A., et al. (2002) Italian crosssectional growth charts for height, weight and BMI (6–20 y). European Journal of Clinical Nutrition 56(2), 171–180. Cacciari, E., Milani, S., Balsamo, A., et al. (2006) Italian crosssectional growth charts for height, weight and BMI (2 to 20 yr). Journal of Endocrinological Investigation 29(7), 581–593. Centers for Disease Control and Prevention. (2009) CDC growth chart training modules: overweight children and adolescents: recommendations to screen, assess and manage.http://www.cdc.gov/nccdphp/dnpa/growthcharts/ training/modules/module3/text/page4a.htm (Accessed 12 August 2009) Chinn, S. & Rona, R.J. (2002) International definitions of overweight and obesity for children: a lasting solution? Annals of Human Biology 29(3), 306–313. Cole, T.J. (1979) A method for assessing age-standardized weight-for-height in children seen cross-sectionally. Annals of Human Biology 6(3), 249–268. Cole, T.J. (1990) The LMS method for constructing normalized growth standards. European Journal of Clinical Nutrition 44(1), 45–60. Cole, T.J., Bellizzi, M.C., Flegal, K.M., & Dietz, W.H. (2000) Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 320(7244), 1240–1243.

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High body mass index, overweight, and obesity in Cole, T.J. & Roede, M.J. (1999) Centiles of body mass index for children: Definitions, terminology, and Dutch children aged 0–20 years in 1980 – a baseline to assess recent trends in obesity. Annals of Human Biology 26(4), 303– interpretation 308. Cole, T.J., Freeman, J.V., & Preece, M.A. (1995) Body mass index reference curves for the UK, 1990. Archives of Disease in Childhood 73(1), 25–29. Cole, T.J., Freeman, J.V., & Preece, M.A. (1998) British 1990 growth reference centiles for weight, height, body mass index and head circumference fitted by maximum penalized likelihood. Statistics in Medicine 17(4), 407–429. Conde, W.L. & Monteiro, C.A. (2006) Body mass index cutoff points for evaluation of nutritional status in Brazilian children and adolescents. Journal of Pediatrics (Rio J.) 82(4), 266–272. (p.13)

Daniels, S.R. & Greer, F.R. (2008) Lipid screening and cardiovascular health in childhood. Pediatrics 122(1), 198– 208. De Onis, M., Onyango, A.W., Borghi, E., Siyam, A., Nishida, C., & Siekmann, J. (2007) Development of a WHO growth reference for school-aged children and adolescents. Bulletin of World Health Organization 85(9), 660–667. Del-Rio-Navarro, B.E., Velazquez-Monroy, O., Santos-Preciado, J.I., et al. (2007) Mexican anthropometric percentiles for ages 10–18. European Journal of Clinical Nutrition 61(8), 963–975. Dietz, W.H. & Bellizzi, M.C. (1999) Introduction: the use of body mass index to assess obesity in children. American Journal of Clinical Nutrition 70(1), 123S–125S. Dietz, W.H. & Robinson, T.N. (1998) Use of the body mass index (BMI) as a measure of overweight in children and adolescents. Journal of Pediatrics 132(2), 191–193. Flegal, K.M. (1999) Curve smoothing and transformations in the development of growth curves. American Journal of Clinical Nutrition 70(1), 163S–165S. Flegal, K.M., Ogden, C.L., Wei, R., Kuczmarski, R.L., & Johnson, C.L. (2001) Prevalence of overweight in US children: comparison of US growth charts from the Centers for Disease Page 21 of 29

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High body mass index, overweight, and obesity in Control and Prevention with other reference values for body children: Definitions, terminology, and mass index. American Journal of Clinical Nutrition 73(6), 1086–1093. interpretation Flegal, K.M., Wei, R., Ogden, C.L., Freedman, D.S., Johnson, C.L., & Curtin, L.R. (2009) Characterizing extreme values of body mass index for age by using the 2000 Centers for Disease Control and Prevention growth charts. American Journal of Clinical Nutrition 90(5), 1314–1320. Freedman, D.S., Dietz, W.H., Srinivasan, S.R., & Berenson, G.S. (1999) The relation of overweight to cardiovascular risk factors among children and adolescents: the Bogalusa Heart Study. Pediatrics 103(6 Pt 1), 1175–1182. Fu, W.P., Lee, H.C., Ng, C.J., et al. (2003) Screening for childhood obesity: international vs population-specific definitions. Which is more appropriate? International Journal of Obesity 27(9), 1121–1126. Goran, M.I., Davis, J., Kelly, L., et al. (2008) Low prevalence of pediatric type 2 diabetes: where's the epidemic? Journal of Pediatrics 152(6), 753–755. Guillaume, M. (1999) Defining obesity in childhood: current practice. American Journal of Clinical Nutrition 70(1 Part 2), 126S–130S. Haines, L., Wan, K.C., Lynn, R., Barrett, T.G., & Shield, J.P. (2007) Rising incidence of type 2 diabetes in children in the U.K. Diabetes Care 30(5), 1097–1101. Hayes, S.J. (2008) Does terminal digit preference occur in pathology? Journal of Clinical Pathology 61(8), 975–976. Hayes, S.J. (2009) Benford's law in relation to terminal digit preference. Journal of Clinical Pathology 62(6), 575–576. Hedley, A.A., Ogden, C.L., Johnson, C.L., Carroll, M.D., Curtin, L.R., & Flegal, K.M. (2004) Prevalence of overweight and obesity among US children, adolescents, and adults, 1999– 2002. JAMA: the Journal of the American Medical Association 291(23), 2847–2850.

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High body mass index, overweight, and obesity in Himes, J.H. (1999) Agreement among anthropometric children: Definitions, terminology, and indicators identifying the fattest adolescents. International Journal of Obesity 23 Suppl (2), S18–S21. interpretation Himes, J.H. & Dietz, W.H. (1994) Guidelines for overweight in adolescent preventive services: recommendations from an expert committee. The Expert Committee on Clinical Guidelines for Overweight in Adolescent Preventive Services. American Journal of Clinical Nutrition 59(2), 307–316. Huerta, M., Gdalevich, M., Tlashadze, A., et al. (2007) Appropriateness of US and international BMI-for-age reference curves in defining adiposity among Israeli school children. European Journal of Pediatrics 166(6), 573–578. Inge, T.H., Xanthakos, S.A., & Zeller, M.H. (2007) Bariatric surgery for pediatric extreme obesity: now or later? International Journal of Obesity 31(1), 1–14. Inokuchi, M., Hasegawa, T., Anzo, M., & Matsuo, N. (2006) Standardized centile curves of body mass index for Japanese children and adolescents based on the 1978–1981 national survey data. Annals of Human Biology 33(4), 444– 453. (p.14)

Jackson, R.T., Rashed, M., Al-Hamad, N., Hwalla, N., & AlSomaie, M. (2007) Comparison of BMI-for-age in adolescent girls in 3 countries of the Eastern Mediterranean Region. Eastern Mediterranean Health Journal 13(2), 430–440. Janssen, I., Katzmarzyk, P.T., Srinivasan, S.R., et al. (2005) Utility of childhood BMI in the prediction of adulthood disease: comparison of national and international references. Obesity Research 13(6), 1106–1115. Ji, C.Y. (2005) Report on childhood obesity in China (1) – body mass index reference for screening overweight and obesity in Chinese school-age children. Biomedical and Environmental Sciences 18(6), 390–400. Jotangia, D., Moody, A., Stamatakis, E., & Wardle, H. (2005) Obesity among children under 11.London: Department of Health. http://www.dh.gov.uk/en/Publicationsandstatistics/ Publications/PublicationsStatistics/DH_4109245 (Accessed 12 November 2009.)

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High body mass index, overweight, and obesity in Kain, J., Uauy, R., Vio, F., & Albala, C. (2002) Trends in children: Definitions, terminology, and overweight and obesity prevalence in Chilean children: comparison of three definitions. European Journal of Clinical interpretation Nutrition 56(3), 200–204. Kato, N., Sato, K., Takimoto, H., & Sudo, N. (2008) BMI for age references for Japanese children – based on the 2000 growth survey. Asia-Pacific Journal of Public Health 20 Suppl 118–127. Keys, A., Fidanza, F., Karvonen, M.J., Kimura, N., & Taylor, H.L. (1972) Indices of relative weight and obesity. Journal of Chronic Diseases 25(6), 329–343. Khosla, T. & Lowe, C.R. (1967) Indices of obesity derived from body weight and height. British Journal of Preventive and Social Medicine 21(3), 122–128. Koplan, J.P., Liverman, C.T., & Kraak, V.I. (2005) Preventing childhood obesity: health in the balance: executive summary. Journal of the American Dietetic Association 105(1), 131–138. Krebs, N.F., Himes, J.H., Jacobson, D., Nicklas, T.A., Guilday, P., & Styne, D. (2007) Assessment of child and adolescent overweight and obesity. Pediatrics 120 Suppl 4 S193–S228. Kuczmarski, R.J., Ogden, C.L., Grummer-Strawn, L.M., et al. (2000) CDC growth charts: United States. Advance Data 314, 1–27. Kuczmarski, R.J., Ogden, C.L., Guo, S.S., et al. (2002) 2000 CDC growth charts for the United States: methods and development. Vital Health Statistics 11(246), 1–190. Lloyd, L.J., Langley-Evans, S.C., & McMullen, S. (2010) Childhood obesity and adult cardiovascular disease risk: a systematic review. International Journal of Obesity 34(1), 18– 28. Mast, M., Langnase, K., Labitzke, K., Bruse, U., Preuss, U., & Muller, M.J. (2002) Use of BMI as a measure of overweight and obesity in a field study on 5–7 year old children. European Journal of Nutrition 41(2), 61–67. Mei, Z., Ogden, C.L., Flegal, K.M., & Grummer-Strawn, L.M. (2008) Comparison of the prevalence of shortness, underweight, and overweight among US children aged 0 to 59

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High body mass index, overweight, and obesity in months by using the CDC 2000 and the WHO 2006 growth children: Definitions, terminology, and charts. Journal of Pediatrics 153(5), 622–628. interpretation Moyer, V.A., Klein, J.D., Ockene, J.K., Teutsch, S.M., Johnson, M.S., & Allan, J.D. (2005) Screening for overweight in children and adolescents: where is the evidence? A commentary by the childhood obesity working group of the US Preventive Services Task Force. Pediatrics 116(1), 235–238.

Must, A., Dallal, G.E., & Dietz, W.H. (1991) Reference data for obesity: 85th and 95th percentiles of body mass index (wt/ht2) and triceps skinfold thickness. American Journal of Clinical Nutrition 53(4), 839–846. Must, A. & Strauss, R.S. (1999) Risks and consequences of childhood and adolescent obesity. International Journal of Obesity 23 Suppl 2, S2–S11. National Institutes of Health (1998) Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults–the evidence report. Obesity Research 6 Suppl 2, 51S–209S. National Institute for Health and Clinical Excellence (2006) Obesity: the prevention, identification, assessment and management of overweight and obesity in adults and children. Clinical Guidelines CG43. (p.15) London: National Institute for Health and Clinical Excellence. http://www.nice.org.uk/ guidance/index.jsp?action=byID&o=11000 (Accessed 1 November 2009) Neovius, M., Linne, Y., Barkeling, B., & Rossner, S. (2004) Discrepancies between classification systems of childhood obesity. Obesity Reviews 5(2), 105–114. O'Neill, J.L., McCarthy, S.N., Burke, S.J., et al. (2007) Prevalence of overweight and obesity in Irish school children, using four different definitions. European Journal of Clinical Nutrition 61(6), 743–751. Ogden, C.L., Flegal, K.M., Carroll, M.D., & Johnson, C.L. (2002) Prevalence and trends in overweight among US children and adolescents, 1999–2000. JAMA: the Journal of the American Medical Association 288(14), 1728–1732.

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High body mass index, overweight, and obesity in Disclaimer: The findings and conclusions in this report are children: Definitions, terminology, and those of the authors and not necessarily those of the Centers for Disease Control and Prevention.  This is an updated and interpretation revised version of a previous publication: Flegal, K.M., Tabak, C.J., & Ogden, C.L. Overweight in children: definitions and interpretation. Health Education Research 2006 Dec 21(6): 755–760.

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