overlapping ages likely explains the slight wiggle in the final WHO standards(for both boys and girls) as also observed in other references. Body mass index-for-age.Body mass index is the ratio weight (in kg)/recumbent length or standing height(in m2).To address the difference between length and height,the approach used for constructing the BMI-for-age standards was different from that described for length/height-for-age.Because BMI is a ratio with squared length or height in the denominator,adding 0.7 cm to the height values and back- transforming them after fitting was not feasible.The solution adopted was to construct the standards for the younger and the older children separately based on two sets of data with an overlapping range of ages below and above 24 months.To construct the BMI-for-age standard based on length (0 to 2 years).the longitudinal sample's length data and the cross-sectional sample's height data (18 to 30 months)were combined after adding 0.7 cm to the height values.Analogously,to construct the standard from 2 to 5 years,the cross-sectional sample's height plus the longitudinal sample's length data (18 to 24 months)were combined after subtracting 0.7 cm from the length values.Thus,a common set of data from 18 to 30 months was used to generate the BMI standards for the younger and the older children.The resulting disjunction between the two standards thus in essence reflects the 0.7 cm difference between length and height.This does not mean,however,that a child at a specific age will have the same length-and height-based BMI-for-age z-score as this is mathematically impossible given the nature of the BMI ratio. An age power transformation as described for the other age-based standards was required before constructing the length-based BMI-for-age curves.No such transformation was necessary for the height-based BMI-for-age.The WHO length-and height-based BMI-for-age standards do not overlap, i.e.the length-based interval ends at 730 days and the height-based interval starts at 731 days.Cubic spline fitting was achieved with variable degrees of freedom for the length-versus height-based standards,and also for the boys'versus girls'final curves. Technical aspects of the standards.The method used to construct the WHO standards generally relied on the Box-Cox power exponential distribution and the final selected models simplified to the LMS model.As a result,the computation of percentiles and z-scores for these standards uses formulae based on the LMS method.However,a restriction was imposed on all indicators to enable the derivation of percentiles only within the interval corresponding to z-scores between -3 and 3.The underlying reasoning is that percentiles beyond +3 SD are invariant to changes in equivalent z-scores. The loss accruing to this restriction is small since the inclusion range corresponds to the 0.135th to 99.865th percentiles The weight-based indicators presented right-skewed distributions.When modelled correctly,right skewness has the effect of making distances between positive z-scores increase progressively the farther away they are from the median,while distances between negative z-scores decrease progressively.The LMS method fits skewed data adequately by using a Box-Cox normal distribution, which follows the empirical data closely.The drawback,however,is that the outer tails of the distribution are highly affected by extreme data points even if only very few.A restricted application of the LMS method was thus used for the construction of the WHO weight-based indicators,limiting the Box-Cox normal distribution to the interval corresponding to z-scores where empirical data were available (i.e.between-3 SD and 3 SD).Beyond these limits,the standard deviation at each age (or length/height)was fixed to the distance between +2 SD and +3 SD,respectively.This approach avoids making assumptions about the distribution of data beyond the limits of the observed values. Epidemiological aspects of the standards.As expected,there are notable differences with the NCHS/WHO reference that vary by age,sex,anthropometric measure and specific percentile or z-score curve.Differences are particularly important in infancy.Stunting will be greater throughout childhood when assessed using the new WHO standards compared to the NCHS/WHO reference.The growth pattern of breastfed infants will result in a substantial increase in rates of underweight during the first half of infancy and a decrease thereafter.For wasting,the main difference is during infancy XiX-
- xix - overlapping ages likely explains the slight wiggle in the final WHO standards (for both boys and girls) as also observed in other references. Body mass index-for-age. Body mass index is the ratio weight (in kg)/recumbent length or standing height (in m2 ). To address the difference between length and height, the approach used for constructing the BMI-for-age standards was different from that described for length/height-for-age. Because BMI is a ratio with squared length or height in the denominator, adding 0.7 cm to the height values and backtransforming them after fitting was not feasible. The solution adopted was to construct the standards for the younger and the older children separately based on two sets of data with an overlapping range of ages below and above 24 months. To construct the BMI-for-age standard based on length (0 to 2 years), the longitudinal sample's length data and the cross-sectional sample's height data (18 to 30 months) were combined after adding 0.7 cm to the height values. Analogously, to construct the standard from 2 to 5 years, the cross-sectional sample's height plus the longitudinal sample's length data (18 to 24 months) were combined after subtracting 0.7 cm from the length values. Thus, a common set of data from 18 to 30 months was used to generate the BMI standards for the younger and the older children. The resulting disjunction between the two standards thus in essence reflects the 0.7 cm difference between length and height. This does not mean, however, that a child at a specific age will have the same length- and height-based BMI-for-age z-score as this is mathematically impossible given the nature of the BMI ratio. An age power transformation as described for the other age-based standards was required before constructing the length-based BMI-for-age curves. No such transformation was necessary for the height-based BMI-for-age. The WHO length- and height-based BMI-for-age standards do not overlap, i.e. the length-based interval ends at 730 days and the height-based interval starts at 731 days. Cubic spline fitting was achieved with variable degrees of freedom for the length- versus height-based standards, and also for the boys' versus girls' final curves. Technical aspects of the standards. The method used to construct the WHO standards generally relied on the Box-Cox power exponential distribution and the final selected models simplified to the LMS model. As a result, the computation of percentiles and z-scores for these standards uses formulae based on the LMS method. However, a restriction was imposed on all indicators to enable the derivation of percentiles only within the interval corresponding to z-scores between -3 and 3. The underlying reasoning is that percentiles beyond ±3 SD are invariant to changes in equivalent z-scores. The loss accruing to this restriction is small since the inclusion range corresponds to the 0.135th to 99.865th percentiles. The weight-based indicators presented right-skewed distributions. When modelled correctly, right skewness has the effect of making distances between positive z-scores increase progressively the farther away they are from the median, while distances between negative z-scores decrease progressively. The LMS method fits skewed data adequately by using a Box-Cox normal distribution, which follows the empirical data closely. The drawback, however, is that the outer tails of the distribution are highly affected by extreme data points even if only very few. A restricted application of the LMS method was thus used for the construction of the WHO weight-based indicators, limiting the Box-Cox normal distribution to the interval corresponding to z-scores where empirical data were available (i.e. between -3 SD and 3 SD). Beyond these limits, the standard deviation at each age (or length/height) was fixed to the distance between ±2 SD and ±3 SD, respectively. This approach avoids making assumptions about the distribution of data beyond the limits of the observed values. Epidemiological aspects of the standards. As expected, there are notable differences with the NCHS/WHO reference that vary by age, sex, anthropometric measure and specific percentile or z-score curve. Differences are particularly important in infancy. Stunting will be greater throughout childhood when assessed using the new WHO standards compared to the NCHS/WHO reference. The growth pattern of breastfed infants will result in a substantial increase in rates of underweight during the first half of infancy and a decrease thereafter. For wasting, the main difference is during infancy
when wasting rates will be substantially higher using the new WHO standards.With respect to overweight,use of the new WHO standards will result in a greater prevalence that will vary by age, sex and nutritional status of the index population. The growth standards presented in this report provide a technically robust tool that represents the best description of physiological growth for children under five years of age.The standards depict normal early childhood growth under optimal environmental conditions and can be used to assess children everywhere,regardless of ethnicity,socioeconomic status and type of feeding. XX
xx when wasting rates will be substantially higher using the new WHO standards. With respect to overweight, use of the new WHO standards will result in a greater prevalence that will vary by age, sex and nutritional status of the index population. The growth standards presented in this report provide a technically robust tool that represents the best description of physiological growth for children under five years of age. The standards depict normal early childhood growth under optimal environmental conditions and can be used to assess children everywhere, regardless of ethnicity, socioeconomic status and type of feeding
1. INTRODUCTION Growth charts are an essential component of the paediatric toolkit.Their value resides in helping to determine the degree to which physiological needs for growth and development are met during the important childhood period.Beyond their usefulness in assessing children's nutritional status,many governmental and United Nations agencies rely on growth charts to measure the general well-being of populations,formulate health and related policies,and plan interventions and monitor their effectiveness. The origin of the WHO Child Growth Standards dates back to the early 1990s when a group of experts was appointed to conduct a meticulous evaluation of the National Center for Health Statistics/World Health Organization(NCHS/WHO)growth reference that had been recommended for international use since the late 1970s (WHO.1995).The limitations of the NCHS/WHO reference have been documented (WHO Working Group on Infant Growth,1994;de Onis and Yip,1996;de Onis and Habicht,1996).The data used to construct the reference covering birth to three years of age came from a longitudinal study of children of European ancestry from a single community in the USA.These children were measured every three months,which is inadequate to describe the rapid and changing rate of growth in early infancy.Also,the statistical methods available at the time the NCHS/WHO growth curves were constructed were too limited to correctly model the pattern and variability of growth.As a result,the NCHS/WHO curves do not adequately represent early childhood growth. The initial phase of the expert group's work documented the deficiencies of the reference and led to a plan for developing new growth charts that would show how children should grow in all countries rather than merely describing how they grew at a particular time and place.The experts underscored the importance of ensuring that the new growth charts were consistent with "best"health practices (Garza and de Onis,2004). A logical outcome of this plan was the WHO Multicentre Growth Reference Study (MGRS),which was implemented between 1997 and 2003(de Onis et al.,2004a).The MGRS is unique in that it was purposely designed to produce a standard rather than a reference.Although standards and references both serve as a basis for comparison,each enables a different interpretation.Since a standard defines how children should grow,deviations from the pattern it describes are evidence of abnormal growth. A reference,on the other hand,does not provide as sound a basis for such value judgments,although in practice references often are mistakenly used as standards The MGRS data provide a solid foundation for developing a standard because they are based on healthy children living under conditions likely to favour achievement of their full genetic growth potential.Furthermore,the mothers of the children selected for the construction of the standards engaged in fundamental health-promoting practices,namely breastfeeding and not smoking(de Onis etal.,2004b). A second feature of the study that makes it attractive as a basis for an internationally applicable standard is that it included children from a diverse set of countries:Brazil,Ghana,India,Norway, Oman and the USA.By selecting privileged,healthy populations the study reduced the impact of environmental variation.Assessment of differences in linear growth among the child populations of the MGRS shows a striking similarity among the six sites,with only about 3%of variability in length being due to differences among sites compared to 70%due to differences among individuals (WHO Multicentre Growth Reference Study Group,2006a).Thus,excluding any site has little effect on the 3rd,50th,and 97th percentile values,and pooling data from all sites is entirely justified.The remarkable similarity in growth during early childhood across human populations is consistent with genomic comparisons among diverse continental groups reporting a high degree of inter-population homogeneity (Rosenberg,2002;King and Motulsky,2002;Jorde and Wooding,2004).Nevertheless, the MGRS sample has considerable built-in ethnic or genetic variability in addition to cultural variation in how children are nurtured,which further strengthens the standards'universal applicability. -1
- 1 - 1. INTRODUCTION Growth charts are an essential component of the paediatric toolkit. Their value resides in helping to determine the degree to which physiological needs for growth and development are met during the important childhood period. Beyond their usefulness in assessing children's nutritional status, many governmental and United Nations agencies rely on growth charts to measure the general well-being of populations, formulate health and related policies, and plan interventions and monitor their effectiveness. The origin of the WHO Child Growth Standards dates back to the early 1990s when a group of experts was appointed to conduct a meticulous evaluation of the National Center for Health Statistics/World Health Organization (NCHS/WHO) growth reference that had been recommended for international use since the late 1970s (WHO, 1995). The limitations of the NCHS/WHO reference have been documented (WHO Working Group on Infant Growth, 1994; de Onis and Yip, 1996; de Onis and Habicht, 1996). The data used to construct the reference covering birth to three years of age came from a longitudinal study of children of European ancestry from a single community in the USA. These children were measured every three months, which is inadequate to describe the rapid and changing rate of growth in early infancy. Also, the statistical methods available at the time the NCHS/WHO growth curves were constructed were too limited to correctly model the pattern and variability of growth. As a result, the NCHS/WHO curves do not adequately represent early childhood growth. The initial phase of the expert group's work documented the deficiencies of the reference and led to a plan for developing new growth charts that would show how children should grow in all countries rather than merely describing how they grew at a particular time and place. The experts underscored the importance of ensuring that the new growth charts were consistent with "best" health practices (Garza and de Onis, 2004). A logical outcome of this plan was the WHO Multicentre Growth Reference Study (MGRS), which was implemented between 1997 and 2003 (de Onis et al., 2004a). The MGRS is unique in that it was purposely designed to produce a standard rather than a reference. Although standards and references both serve as a basis for comparison, each enables a different interpretation. Since a standard defines how children should grow, deviations from the pattern it describes are evidence of abnormal growth. A reference, on the other hand, does not provide as sound a basis for such value judgments, although in practice references often are mistakenly used as standards. The MGRS data provide a solid foundation for developing a standard because they are based on healthy children living under conditions likely to favour achievement of their full genetic growth potential. Furthermore, the mothers of the children selected for the construction of the standards engaged in fundamental health-promoting practices, namely breastfeeding and not smoking (de Onis et al., 2004b). A second feature of the study that makes it attractive as a basis for an internationally applicable standard is that it included children from a diverse set of countries: Brazil, Ghana, India, Norway, Oman and the USA. By selecting privileged, healthy populations the study reduced the impact of environmental variation. Assessment of differences in linear growth among the child populations of the MGRS shows a striking similarity among the six sites, with only about 3% of variability in length being due to differences among sites compared to 70% due to differences among individuals (WHO Multicentre Growth Reference Study Group, 2006a). Thus, excluding any site has little effect on the 3rd, 50th, and 97th percentile values, and pooling data from all sites is entirely justified. The remarkable similarity in growth during early childhood across human populations is consistent with genomic comparisons among diverse continental groups reporting a high degree of inter-population homogeneity (Rosenberg, 2002; King and Motulsky, 2002; Jorde and Wooding, 2004). Nevertheless, the MGRS sample has considerable built-in ethnic or genetic variability in addition to cultural variation in how children are nurtured, which further strengthens the standards' universal applicability
Introduction A key characteristic of the new standards is that they explicitly identify breastfeeding as the biological norm and establish the breastfed child as the normative model for growth and development (WHO Multicentre Growth Reference Study Group,2006b).Another distinguishing feature of the new standards is that they include windows of achievement for six gross motor developmental milestones which are presented elsewhere (WHO Multicentre Growth Reference Study Group,2006c).Although WHO in the past issued recommendations concerning attained physical growth,it had not previously made any recommendations for assessing motor development. This report presents the first set of WHO Child Growth Standards and describes the methods used to construct the standards for length/height-for-age,weight-for-age,weight-for length,weight-for-height and BMI-for-age.It also compares the new standards with the NCHS/WHO growth reference (WHO, 1983)and the 2000 CDC growth charts (Kuczmarski,2002).Electronic copies of the WHO growth charts and tables together with tools developed to facilitate their use are available on the Web: www.who.int/childgrowth/en
2 Introduction A key characteristic of the new standards is that they explicitly identify breastfeeding as the biological norm and establish the breastfed child as the normative model for growth and development (WHO Multicentre Growth Reference Study Group, 2006b). Another distinguishing feature of the new standards is that they include windows of achievement for six gross motor developmental milestones which are presented elsewhere (WHO Multicentre Growth Reference Study Group, 2006c). Although WHO in the past issued recommendations concerning attained physical growth, it had not previously made any recommendations for assessing motor development. This report presents the first set of WHO Child Growth Standards and describes the methods used to construct the standards for length/height-for-age, weight-for-age, weight-for length, weight-for-height and BMI-for-age. It also compares the new standards with the NCHS/WHO growth reference (WHO, 1983) and the 2000 CDC growth charts (Kuczmarski, 2002). Electronic copies of the WHO growth charts and tables together with tools developed to facilitate their use are available on the Web: www.who.int/childgrowth/en
2. METHODOLOGY 2.1 Design of the WHO Multicentre Growth Reference Study The MGRS (July 1997-December 2003)was a population-based study that took place in the cities of Davis,California,USA;Muscat,Oman;Oslo,Norway;and Pelotas,Brazil;and in selected affluent neighbourhoods of Accra,Ghana and South Delhi,India.The MGRS protocol and its implementation in the six sites are described in detail elsewhere (de Onis et al.,2004a).Briefly,the MGRS combined a longitudinal component from birth to 24 months with a cross-sectional component of children aged 18-71 months.In the longitudinal component,mothers and newborns were screened and enrolled at birth and visited at home a total of 21 times on weeks 1,2,4 and 6;monthly from 2-12 months;and bimonthly in the second year.In the cross-sectional component,children aged 18-71 months were measured once,except in the two sites (Brazil and USA)that used a mixed-longitudinal design in which some children were measured two or three times at three-month intervals.Both recumbent length and standing height were measured for all children aged 18-30 months.Data were collected on anthropometry,motor development,feeding practices,child morbidity,perinatal factors,and socioeconomic,demographic and environmental characteristics(de Onis et al.,2004b). The study populations lived in socioeconomic conditions favourable to growth and where mobility was low,>20%of mothers followed WHO feeding recommendations and breastfeeding support was available(de Onis et al.,2004b).Individual inclusion criteria were:no known health or environmental constraints to growth,mothers willing to follow MGRS feeding recommendations (i.e.exclusive or predominant breastfeeding for at least 4 months,introduction of complementary foods by the age of 6 months,and continued partial breastfeeding up to at least 12 months),no maternal smoking before and after delivery,single term birth,and absence of significant morbidity (de Onis et al.,2004b). As part of the site-selection process in Ghana,India and Oman,surveys were conducted to identify socioeconomic characteristics that could be used to select groups whose growth was not environmentally constrained (Owusu et al.,2004;Bhandari et al.,2002;Mohamed et al.,2004).Local criteria for screening newborns,based on parental education and/or income levels,were developed from those surveys.Pre-existing survey data for this purpose were available from Brazil,Norway and the USA.Of the 13 741 mother-infant pairs screened for the longitudinal component,about 83%were ineligible (WHO Multicentre Growth Reference Study Group,2006d).Families'low socioeconomic status was the most common reason for ineligibility in Brazil,Ghana,India and Oman,whereas parental refusal was the main reason for non-participation in Norway and USA (WHO Multicentre Growth Reference Study Group,2006d).For the cross-sectional component,69%of the 21 510 subjects screened were excluded for reasons similar to those observed in the longitudinal component. Term low-birth-weight (<2500 g)infants (2.3%)were not excluded.Since it is likely that in well-off populations such infants represent small but normal children,their exclusion would have artificially distorted the standards'lower percentiles.Eligibility criteria for the cross-sectional component were the same as those for the longitudinal component with the exception of infant feeding practices.A minimum of three months of any breastfeeding was required for participants in the study's cross- sectional component. 2.2 Anthropometry methods Data collection teams were trained at each site during the study's preparatory phase,at which time measurement techniques were standardized against one of two MGRS anthropometry experts.During the study,bimonthly standardization sessions were conducted at each site.Once a year the anthropometry expert visited each site to participate in these sessions (de Onis et al.,2004c).Results from the anthropometry standardization sessions have been reported elsewhere (WHO Multicentre Growth Reference Study Group,2006e).For the longitudinal component of the study,screening teams measured newborns within 24 hours of delivery,and follow-up teams conducted home visits until 24 months of age.The follow-up teams were also responsible for taking measurements in the cross- sectional component involving children aged 18-71 months (de Onis et al.,2004b). -3-
- 3 - 2. METHODOLOGY 2.1 Design of the WHO Multicentre Growth Reference Study The MGRS (July 1997–December 2003) was a population-based study that took place in the cities of Davis, California, USA; Muscat, Oman; Oslo, Norway; and Pelotas, Brazil; and in selected affluent neighbourhoods of Accra, Ghana and South Delhi, India. The MGRS protocol and its implementation in the six sites are described in detail elsewhere (de Onis et al., 2004a). Briefly, the MGRS combined a longitudinal component from birth to 24 months with a cross-sectional component of children aged 18–71 months. In the longitudinal component, mothers and newborns were screened and enrolled at birth and visited at home a total of 21 times on weeks 1, 2, 4 and 6; monthly from 2–12 months; and bimonthly in the second year. In the cross-sectional component, children aged 18–71 months were measured once, except in the two sites (Brazil and USA) that used a mixed-longitudinal design in which some children were measured two or three times at three-month intervals. Both recumbent length and standing height were measured for all children aged 18–30 months. Data were collected on anthropometry, motor development, feeding practices, child morbidity, perinatal factors, and socioeconomic, demographic and environmental characteristics (de Onis et al., 2004b). The study populations lived in socioeconomic conditions favourable to growth and where mobility was low, ≥20% of mothers followed WHO feeding recommendations and breastfeeding support was available (de Onis et al., 2004b). Individual inclusion criteria were: no known health or environmental constraints to growth, mothers willing to follow MGRS feeding recommendations (i.e. exclusive or predominant breastfeeding for at least 4 months, introduction of complementary foods by the age of 6 months, and continued partial breastfeeding up to at least 12 months), no maternal smoking before and after delivery, single term birth, and absence of significant morbidity (de Onis et al., 2004b). As part of the site-selection process in Ghana, India and Oman, surveys were conducted to identify socioeconomic characteristics that could be used to select groups whose growth was not environmentally constrained (Owusu et al., 2004; Bhandari et al., 2002; Mohamed et al., 2004). Local criteria for screening newborns, based on parental education and/or income levels, were developed from those surveys. Pre-existing survey data for this purpose were available from Brazil, Norway and the USA. Of the 13 741 mother-infant pairs screened for the longitudinal component, about 83% were ineligible (WHO Multicentre Growth Reference Study Group, 2006d). Families’ low socioeconomic status was the most common reason for ineligibility in Brazil, Ghana, India and Oman, whereas parental refusal was the main reason for non-participation in Norway and USA (WHO Multicentre Growth Reference Study Group, 2006d). For the cross-sectional component, 69% of the 21 510 subjects screened were excluded for reasons similar to those observed in the longitudinal component. Term low-birth-weight (<2500 g) infants (2.3%) were not excluded. Since it is likely that in well-off populations such infants represent small but normal children, their exclusion would have artificially distorted the standards’ lower percentiles. Eligibility criteria for the cross-sectional component were the same as those for the longitudinal component with the exception of infant feeding practices. A minimum of three months of any breastfeeding was required for participants in the study’s crosssectional component. 2.2 Anthropometry methods Data collection teams were trained at each site during the study's preparatory phase, at which time measurement techniques were standardized against one of two MGRS anthropometry experts. During the study, bimonthly standardization sessions were conducted at each site. Once a year the anthropometry expert visited each site to participate in these sessions (de Onis et al., 2004c). Results from the anthropometry standardization sessions have been reported elsewhere (WHO Multicentre Growth Reference Study Group, 2006e). For the longitudinal component of the study, screening teams measured newborns within 24 hours of delivery, and follow-up teams conducted home visits until 24 months of age. The follow-up teams were also responsible for taking measurements in the crosssectional component involving children aged 18–71 months (de Onis et al., 2004b)