ARTICLE. Crossing Growth Percentiles in Infancy and Risk of Obesity in Childhood

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1 ARTICLE Crossing Growth Percentiles in Infancy and Risk of Obesity in Childhood Elsie M. Taveras, MD, MPH; Sheryl L. Rifas-Shiman, MPH; Bettylou Sherry, PhD, RD; Emily Oken, MD, MPH; Jess Haines, PhD, MHSc, RD; Ken Kleinman, ScD; Janet W. Rich-Edwards, ScD; Matthew W. Gillman, MD, SM Objective: To examine the associations of upward crossing of major percentiles in weight-for-length in the first 24 months of life with the prevalence of obesity at ages 5 and 10 years. Design: Longitudinal study. Setting: Multisite clinical practice. Participants: We included children aged from 1 month to less than 11 years with length/height and weight measurements from January 1, 1980, through December 31, Main Exposure: The number of major weight-forlength percentiles crossed during each of four 6-month intervals, that is, 1 to 6 months, 6 to 12 months, 12 to 18 months, and 18 to 24 months. Main Outcome Measures: Odds and observed prevalence of obesity (body mass index [calculated as weight in kilograms divided by height in meters squared] 95th percentile) at ages 5 and 10 years. Results: Crossing upwards 2 or more weight-forlength percentiles was common in the first 6 months of life (43%) and less common during later age intervals. Crossing upwards 2 or more weight-for-length percentiles in the first 24 months was associated with elevated odds of obesity at ages 5 years (odds ratio, 2.08; 95% CI, ) and 10 years (1.75; ) compared with crossing less than 2 major percentiles. Obesity prevalence at ages 5 and 10 was highest among children who crossed upwards 2 or more weight-for-length percentiles in the first 6 months of life. Conclusions: Crossing upwards 2 or more major weightfor-length percentiles in the first 24 months of life is associated with later obesity. Upward crossing of 2 weightfor-length percentiles in the first 6 months is associated with the highest prevalence of obesity 5 and 10 years later. Efforts to curb excess weight gain in infancy may be useful in preventing later obesity. Arch Pediatr Adolesc Med. 2011;165(11): Author Affiliations are listed at the end of this article. THE OBESITY EPIDEMIC HAS spared no age group, includingyoungchildren. 1,2 Recent evidence suggests that even infants experienced a dramatic rise in excess weight in the past 20 years, 2 and that already by 3 years of age obese children have elevated levels of inflammatory markers linked to heart disease later in life. 3 Epidemiologic studies 4-7 have also shown that excess weight gain in the first half of infancy predicts later obesity and higher blood pressure. These data imply that For editorial comment see page 1043 contributors to the epidemic can be found as early as infancy and suggest that identification of children in the earliest stages of life who are at highest risk is potentially crucial to stemming the rising tide of obesity. 2,8,9 One limitation of these previous studies is the variety of metrics used to characterize weight gain during infancy. There is a need for potentially practical clinical tools to identify infants at highest risk. During well-child visits, 10 clinicians routinely use the Centers for Disease Control and Prevention (CDC) growth charts to document serial measures of weight and length and to screen for abnormalities in weight status. The CDC growth charts include predefined major percentile lines to highlight the 5th, 10th, 25th, 50th, 75th, 90th, and 95th percentiles for age and sex. 11 In toddlers and school-age children, clinicians often use upward crossing of 2 major percentile lines in weight-for-length or body mass index (calculated as weight in kilograms divided by height in meters squared) to identify children at risk of developing obesity. Mei et al 12 found that crossing weight-for-length percentiles during the first 2 years of life is more common than at older ages. Given the high rate of shifting in weight-for-length, they concluded that upward crossing of weight-forlength percentiles in infancy is not of concern. To our knowledge, however, no 993

2 Table 1. Number of Weight-for-Length Measurements Within Each of Four 6-Month Age Intervals in the First 24 Months of Life a No. of Weight-for-Length Crossings (N= ) Age, mo Overall Boys Girls Total a Data are from children with weight-for-length crossings. previous studies have examined whether crossing major percentiles in the CDC growth charts during the first 24 months of life is associated with later obesity. The purpose of this longitudinal study was to examine associations of upward crossing of major percentiles in weight-for-length in the first 24 months of life with the prevalence of obesity at ages 5 and 10 years. METHODS SETTING AND SUBJECTS We culled longitudinal data from a clinical database of well-child visits by children. The study population consisted of children younger than 11 years of age who were seen for well-child visits at any of the 14 health centers of Harvard Vanguard Medical Associates/Atrius Health in eastern Massachusetts from January 1, 1980, through December 31, Throughout the study period, Harvard Vanguard Medical Associates used a completely electronic medical record system that contained demographic and growth data. Details of the data collection methods have been previously published. 2,13 To be included in the analyses, children needed at least 2 measurements within at least 1 of four 6-month intervals in the first 24 months of life, from which we could calculate the number of weight-for-length percentiles they crossed. Of the children, had at least 2 measurements within 1 of these 6-month intervals. Of these children, had either 5- or 10-year anthropometric outcomes. The sample size for our final analyses included these children with weight-for-length measures between the ages of 1 and 24 months and height/weight measurements at 5 or 10 years. An individual child could contribute to each of the four 6-month intervals. Of note, because birth weight and especially length were not universally recorded in the outpatient electronic medical record, we could not use birth as a starting age. Instead, we used a well-child visit anytime in the first month of life, and we called this time point 1 month. The study protocol was approved by the institutional review board of Harvard Pilgrim Health Care. MEASUREMENTS Medical assistants at Harvard Vanguard Medical Associates health centers measured length or height and weight according to the written standardized protocol of the health centers. Weight was measured to the nearest 0.25 lb on a calibrated pediatric scale. Using a paper-and-pencil technique, medical assistants measured recumbent length in children younger than 24 months. In this technique, the child lies supine on a piece of paper atop an examination table with his or her face looking at the ceiling. The medical assistant draws a tick mark abutting the top of the child s head. The medical assistant then straightens the child s legs, flattens the child s knees, flexes the child s foot to 90, and marks the paper at the bottom of the child s heels. The medical assistant measures and records the distance between the marks, to the nearest quarter-inch, with a flexible tape. For children aged 5 and 10 years, they measured height standing, without shoes. In a validation study 14 among children aged birth to 24 months conducted at one of the participating Harvard Vanguard Medical Associates health centers, the paper-and-pencil method systematically overestimated children s length compared with a reference method (recumbent length measuring board). This bias did not depend meaningfully on the age or sex of the child. Thus, as previously described, 15 we used a regression correction factor to adjust for this systematic overestimation: [(0.953 length measured by paper-and-pencil method) 1.8 cm]. MAIN EXPOSURES Our main exposure was the number of major weight-for-length percentile lines crossed during each of the four 6-month intervals from 1 to 24 months of age. To estimate this value, we first chose weight and length measurements for each child that were closest to each starting time point, that is, 1 month, 6 months, 12 months, 18 months, and 24 months. We allowed 30 days more or less from the 1-, 6-, 12-, 18-, and 24-month visits. A child s measurements could contribute to more than 1 interval. For example, measurements from the 6-month visit would be used as the ending measurementsforthe1-to-6-monthageintervalandasthestartingmeasurement for the next age interval, 6 to 12 months. We then used the CDC 2000 growth charts 11 to assign an age- and sex-specific weight-for-length percentile to each child s measurement. We calculated the number of major percentile lines that the child crossed duringeachoffour6-monthintervals(ie, 1-6months, 6-12months, months, and months). We used the CDC s predefined major percentile lines to highlight the 5th, 10th, 25th, 50th, 75th, 90th, and 95th percentiles because these are the cut-points printed on the CDC growth charts and are commonly used by clinicians to track growth in primary care. For example, if a child s weightfor-length percentiles at ages 6 months and 12 months were 14th and45th, respectively, thenheorshecrossedupwards1majorpercentile (the 25th) in weight-for-length in that 6-month interval. If another child s weight-for-length percentiles at ages 6 and 12 months were 94th and 55th, respectively, then he or she crossed downwards 2 major percentiles (the 90th and 75th) in weight-forlength in the 6-month interval. Details of the sample sizes in each interval are presented in Table 1. In secondary analyses, we also examined ever crossing upwards 2 or more weight-for-length percentiles during any of the 4 intervals. For the secondary analyses, we included participants with weight-for-length measurements during all four 6-month intervals and outcome data at ages 5 or 10 years and complete covariate information. OUTCOME MEASURES From heights and weights at ages 5 and 10 years, we calculated body mass index. Our main outcome at ages 5 and 10 years was prevalence of obesity, defined as an age- and sex-specific body mass index at the 95th percentile or higher. 16 OTHER MEASURES From enrollment records, we extracted information on each child s date of birth, sex, visit dates, and race/ethnicity. Parental or clinician report of child s race/ethnicity was documented in the record using the categories white, black, His- 994

3 Table 2. Characteristics of Children Seen for Well-Child Care Visits in a Pediatric Group Practice Characteristic No. (%) Sex Male (51.1) Female (48.9) Race/ethnicity White (54.7) Black 5390 (12.1) Hispanic 1458 (3.3) Other 3172 (7.1) Missing (22.9) Obese a Atage5y(n=39107) 4523 (11.6) At age 10 y (n=22 407) 3608 (16.1) a Defined as body mass index 95th percentile for age and sex. panic, American Indian/Alaska Native, Asian, and other. Race/ ethnicity was missing for participants (22.9%). Comparison of them with the participants with nonmissing race/ethnicity data showed that the 2 groups did not differ by number of percentiles crossed upwards: 64% of children with nonmissing race/ethnicity data vs 65% of children with missing race/ethnicity data crossed upwards 2 or more weight-for-length percentiles in any of the four 6-month intervals in the first 24 months of life. STATISTICAL ANALYSIS In the primary analyses of crossing percentiles within each 6-month interval, we ran the observed prevalence of obesity at ages 5 and 10 years. We stratified the analyses according to starting weightfor-length percentile (ie, 25th, 25th-50th, 50th-75th, and 75th- 90th) and excluded children whose weight-for-length percentile was higher than the 90th percentile at the beginning of each 6-month interval because they could not cross upwards 2 major percentile lines during that interval. We used generalized linear mixed models (PROC GLIMMIX in SAS, version 9.2; SAS Institute, Inc, Cary, North Carolina) to test differences in the observed prevalence of obesity at ages 5 and 10 years associated with crossing upwards 2 or more major weight-for-length percentile lines in the first 6 months of life compared with crossing upwards 2 or more major weight-for-length percentiles at any other period (ie, 6-12 months, months, and months). All models used random effects to account for individuals who contributed at least 1 observation. In analyses of ever crossing upwards 2 or more major weightfor-length percentiles, we used SAS Proc MI (SAS Institute, Inc) to impute 10 values for missing race/ethnicity. After imputation, the data were combined and all analyses were performed using Proc MI ANALYZE (SAS Institute, Inc). In multivariable logistic regression, we adjusted for child s sex, year of outcome measurement, exact age at outcome measurement, and race/ethnicity to examine the odds of obesity (body mass index at the 95th percentile or higher vs at less than the 95th percentile) at ages 5 and 10 years. We report odds ratios and 95% CIs. All models were fit separately for boys and girls; we combined results and adjusted for sex because sex-specific estimates were similar. We conducted all analyses using SAS, version 9.2 (SAS Institute, Inc). RESULTS Table 2 shows the sex, race/ethnicity, and obesity prevalence among the participating children, and Table 3. Data on Children Who Crossed Upwards 0, 0, 1, or 2 or More Major Weight-for-Length Percentile Lines in Each of Four 6-Month Age Intervals in the First 24 Months of Life a No. of Major Weight-for-Length Percentile Lines Crossed, No. (%) of Children Age, mo Overall (21) 5961 (18) 6198 (18) (43) (27) 8530 (30) 6517 (23) 5495 (20) (31) 8036 (34) 5174 (22) 3223 (14) (43) 6345 (30) 3678 (17) 2306 (11) Boys (19) 2933 (17) 3188 (18) 7959 (46) (26) 4098 (29) 3412 (24) 3030 (21) (31) 4010 (34) 2582 (22) 1661 (14) (44) 3153 (29) 1773 (16) 1154 (11) Girls (22) 3028 (18) 3010 (18) 6667 (41) (28) 4432 (32) 3105 (22) 2465 (18) (31) 4026 (34) 2592 (22) 1562 (13) (42) 3192 (30) 1905 (18) 1152 (11) a Excluded children whose starting weight-for-length percentile was 90th because they could not cross upwards 2 major percentile lines. Crossing upwards 0 times means crossing downwards. Table 3 summarizes the number of children who crossed less than 0 (ie, moved downward across major percentiles), 0, 1, and 2 or more percentiles. Obesity prevalence was 11.6% at age 5 and 16.1% at age 10 years. In the first 6 months of life, 43% of participants crossed upwards 2 or more weight-for-length percentiles. Fewer children crossed upwards 2 or more weight-for-length percentiles after 6 months of age: 20% from 6 to 12 months, 14% from 12 to 18 months, and 11% from 18 to 24 months (Table 3). We observed similar crossing patterns for boys and girls (Table 3). Table 4 shows the observed prevalence of obesity at ages 5 and 10 years according to the number of percentile lines crossed in each of the four 6-month intervals, stratified by starting weight-for-length percentile. As expected, starting at a higher percentile at any time between 1 and 24 months was associated with higher obesity prevalence at 5 or 10 years than starting at a lower percentile (Table 4). For example, a 6-month-old child starting at the 75th to 90th percentile who crossed upwards 2 or more percentiles in the next 6 months had an observed obesity prevalence of 29.7% at age 5 years, much higher than the 7.4% in a 6-month-old child who instead started at less than the 25th percentile. Crossing upwards 2 or more percentiles in the first 6 months of life was associated with a high prevalence of obesity at ages 5 and 10 years. For example, at age 5, the prevalence was 32.9% for 1-month-old infants whose weight-for-length started at the 75th to 90th percentile and crossed 2 or more percentiles by age 6 months. This prevalence was higher, compared with the prevalence of 29.7% for those crossing between 6 and 12 months of age, 32.0% for 12 to 18 months, and 31.8% for 18 to 24 months (Table 4). At age 10 years, we also observed a high prevalence of obesity in children with upward crossing of 2 or more percentiles in the first 6 months of life 995

4 Table 4. Prevalence of Obesity at Ages 5 and 10 Years According to Starting Weight-for-Length Percentile and the Number of Weight-for-Length Percentile Lines Crossed a Prevalence (%), by Starting Weight-for-Length Percentile and No. of Percentile Lines Crossed 25th 25th-50th 50th-75th 75th-90th Age, mo Obesity at age 5 years Obesity at age 10 years a Excluded children whose starting weight-for-length percentile was 90th because they could not cross upwards 2 major percentile lines. Obesity is defined as a body mass index 95th percentile for age and sex. and who were in the 75th to 90th percentile at baseline (34.6%) (Table 4 and Figure). In secondary analyses, we found that (64.4%) of children had ever crossed upwards 2 or more percentiles in the first 24 months of life. In covariateadjusted regression analyses, we found elevated odds of obesity at ages 5 years (odds ratio, 2.08; 95% CI, ) and 10 years (1.75; ) among children who had ever crossed upwards 2 or more major weight-forlength percentiles in the first 24 months of life vs those who had crossed less than 2 major weight-for-length percentiles in the first 24 months of life (Table 5). COMMENT In this study of more than children with more than weight-for-length measurements between the ages of 1 and 24 months, we found that crossing upwards 2 or more weight-for-length percentiles in the first 24 months of life was associated with elevated odds of obesity at ages 5 and 10 years compared with children who crossed fewer than 2 major weight-for-length percentiles. Upward crossing of 2 or more major weight-forlength percentiles in the first 6 months of life not only was common but also was associated with high risks of obesity 5 and 10 years later. In 2004, Mei et al 12 reported that crossing growth percentiles from 0 to 24 months of age was common among participants in the California Child Health and Development Study. In the first 6 months of life, 62% of children crossed 2 major weight-for-length percentiles either upward or downward. The authors concluded that because of the high rate of shifting in weight-for-length during infancy, concern about overweight in infancy was unnecessary. Similar to Mei et al, we found high rates of crossing of major weight-for-length percentiles in the first 6 months of life. However, we found that crossing of weight-for-length in the first 6 months of life was of consequence. Upward crossing of at least 2 percentile lines from 1 to 6 months predicted a prevalence of obesity at ages 5 and 10 years that ranged from 11.5% to 34.6%. With few exceptions, these frequencies were higher, albeit not always significantly, than those associated with crossing during any of the other 6-month intervals. Within each interval, crossing at least 2 lines was associated with higher risks than crossing fewer lines. In addition, similar to a study predicting obesity at age 12 years from measures at 2 to 5 years of age, 17 we observed that having ever crossed upwards 2 or more major weight-forlength percentiles in the first 24 months of life was associated with 2-fold higher odds of obesity at age 5 years and 75% higher odds at age 10 years. Our findings extend a growing body of literature indicating that weight gain in the first few months of life contributes to the development of obesity. 18,19 Previous studies of both contemporary 20,21 and historical 22 cohorts and 2 recent systematic reviews 4,5 of infant growth and obesity have concluded that infants at the highest end of the weight or body mass index distribution, and infants who grew most rapidly (usually measured as weight gain), were more likely to be obese later in life. Many of these studies, however, have been limited by their relatively small sample sizes, 23 by lack of data among children younger than 24 months, 17 or by reliance on weight measures alone without length measurements. 5,20-22,24 Our large sample size of children with weight and length measures who were younger than 24 months allowed precise estimates within strata defined both by starting weight-for-length percentiles and number of percentile lines crossed. One feature of our study lends itself to potential clinical application. Assessing how many percentiles a child crosses has more clinical utility and is more practical than calculating an epidemiologic exposure measure, such as change in weight-for-length z score, as many studies have done. Because pediatric clinicians routinely document serial measures of weight and length and screen for abnormalities in weight status using the published CDC growth charts, crossing percentiles could be used to assess early risk of obesity in pediatric primary care of infants younger than 24 months. Nevertheless, it remains to be seen whether interventions based on such early identification result in improvements in child health. 996

5 B% of Children Obese at Age 10 y A% of Children Obese at Age 5 y mo 6-12 mo mo mo Table 5. Odds of Obesity at Ages 5 and 10 Years Among Children Who Had Ever Crossed Upwards 2 or More vs Less Than 2 Major Weight-for-Length Percentiles in the First 24 Months of Life Odds Ratio (95% CI) 20 Obesity at 5 Years Obesity at 10 Years P <.001 < Characteristic Ever crossed upwards 2 major 2.08 ( ) 1.75 ( ) weight-for-length percentiles in the first 24 mo (vs crossed 2 major weight-for-length percentiles) Female vs male 0.96 ( ) 0.72 ( ) Race/ethnicity vs white Black 1.83 ( ) 2.48 ( ) Hispanic 1.67 ( ) 1.66 ( ) Other 0.95 ( ) 1.02 ( ) Age at outcome, mo 1.00 ( ) 1.01 ( ) Visit year at outcome 1.04 ( ) 1.03 ( ) < Starting Weight-for-Length Percentile Figure. Prevalence of obesity (defined as body mass index 95th percentile) at ages 5 (A) and 10 (B) years associated with crossing upwards 2 or more major weight-for-length percentile lines (Centers for Disease Control and Prevention growth charts) during each of four 6-month age intervals in the first 24 months of life, according to the category of starting weight-for-length percentile at the start of each interval. Data are from well-child visits among children. Even if crossing weight-for-length percentiles can serve as a tool for pediatric clinicians to identify excess gainers in infancy, there is still the need to identify modifiable determinants of excess gain in adiposity and what the proper response should be. 8 A robust literature has emerged regarding prenatal and perinatal predictors of childhood adiposity, 6,25-30 but few studies have examined whether these factors also predict weight gain in early infancy. Furthermore, there is a need to examine tradeoffs of more rapid vs less rapid weight gain for different outcomes. At least among infants born preterm, more rapid weight gain in early infancy predicts better neurocognitive outcomes in childhood. 31,32 Whether this same situation holds with term infants is less clear. 33 Thus, the amount of weight gain that optimizes both neurocognitive and obesity risk may differ by gestational age. Investigating these potential determinants of excess infant adiposity gain could lead to intervention strategies in clinical and public health settings to prevent childhood obesity and its consequences. When interpreting our study, several limitations should be considered. First, the ambulatory care records we examined infrequently contained birth weight. Rather, we used weights and lengths in the first month of life. Thus, our estimates of crossing percentiles in the first 6 months of life do not reflect any shifts that may have occurred between birth and the first well-child care visit. Second, we used clinically measured lengths, which tend to overestimate actual length. To overcome this limitation, we used the regression estimate from our previous validation study to statistically correct for this systematic overestimation. Third, race/ethnicity was missing for approximately 20% of the children in this study, although we did not observe differences in rates of crossing percentiles among children with and without complete race/ ethnicity data. Finally, all participants in this study had health insurance and access to primary care during the first 24 months of life (1-24 months) and during childhood (5- or 10-year visit). Our results may not be generalizable to more disadvantaged populations with less access to primary care. CONCLUSIONS Upward crossing of major weight-for-length percentiles in infancy, especially in the first 6 months of life, is associated with high rates of obesity at ages 5 and 10 years. These results raise the possibility of using this metric as a practical tool to identify children who may be at high risk of obesity in pediatric settings where clinicians already weigh, measure, and plot growth for infants at regular intervals. Our findings and those of the growing literature in this area support the need to identify modifiable determinants of excess gain in adiposity in infancy that can inform the design of clinical and public health interventions to modify these determinants. Accepted for Publication: May 10, Author Affiliations: Obesity Prevention Program, Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute (Drs Taveras, Oken, Kleinman, and Gillman, and Ms Rifas-Shiman), and Division of General Pediatrics, Children s Hospital Boston (Dr Taveras), Boston, Massachusetts; Division of 997

6 Nutrition, Physical Activity, and Obesity, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia (Dr Sherry); Department of Family Relations and Applied Nutrition, University of Guelph, Guelph, Ontario (Dr Haines); Connors Center for Women s Health and Gender Biology, Brigham and Women s Hospital (Dr Rich-Edwards), and Department of Nutrition, Harvard School of Public Health (Dr Gillman), Boston, Massachusetts. Correspondence: Elsie M. Taveras, MD, MPH, Obesity Prevention Program, Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, 133 Brookline Ave, 6th Floor, Boston, MA (elsie_taveras@hphc.org). Author Contributions: Study concept and design: Taveras, Sherry, Oken, and Gillman. Acquisition of data: Oken and Gillman. Analysis and interpretation of data: Taveras, Rifas-Shiman, Sherry, Oken, Haines, Kleinman, and Rich-Edwards. Drafting of the manuscript: Taveras. Critical revision of the manuscript for important intellectual content: Rifas-Shiman, Sherry, Oken, Haines, Kleinman, Rich-Edwards, and Gillman. Statistical analysis: Rifas-Shiman, Kleinman, and Rich-Edwards. Obtained funding: Taveras and Gillman. Administrative, technical, and material support: Taveras and Sherry. Study supervision: Gillman. Financial Disclosure: None reported. Funding/Support: This work was supported by grant M from the CDC, National Center for Chronic Disease Prevention and Health Promotion. Disclaimer: This work is solely the responsibility of the authors and does not represent official views of the CDC. Previous Presentation: The abstract of this manuscript was published as part of the proceedings of the 2008 Pediatric Academic Societies Annual Meeting; May 3-6, 2008; Honolulu, Hawaii. REFERENCES 1. 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