BMI Trajectories During the First 2 Years, and Their Associations With Infant Overweight/Obesity: A Registered Based Cohort Study in Taizhou ...
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ORIGINAL RESEARCH published: 12 May 2021 doi: 10.3389/fped.2021.665655 BMI Trajectories During the First 2 Years, and Their Associations With Infant Overweight/Obesity: A Registered Based Cohort Study in Taizhou, China Tian Zhang 1† , Ying Song 1† , Haoyue Teng 1 , Yue Zhang 1 , Jianan Lu 1 , Linghua Tao 2 , Yanjie Jin 2,3 , Jieyun Yin 1* and Danhong Zhou 2* 1 Department of Epidemiology and Biostatics, Jiangsu Key Laboratory of Preventive and Translational Medicine for Geriatric Diseases, School of Public Health, Medical College of Soochow University, Suzhou, China, 2 Department of Gynaecology and Edited by: Obstetrics, Taizhou Woman and Children’s Hospital, Taizhou, China, 3 Beijing Longtengxinyang Information Technology Stefan Swartling Peterson, Company, Beijing, China Uppsala University, Sweden Reviewed by: Jiangmin Xu, Objective: The purpose of this study was to identify trajectories of body mass Winston-Salem State University, index (BMI) in toddlers from birth to 2 years old and examine their association with United States infantile overweight/obesity. Jolanta Pauk, Bialystok University of Methods: Data were collected from 19,054 children born in any hospital or community Technology, Poland healthcare center in Taizhou, China from 2018 to 2019 with at least three BMI *Correspondence: Jieyun Yin measurements after birth. The Latent Class Growth Mixture Model was used to identify jyyin@suda.edu.cn distinct BMI trajectories during the first 2 years of infants. Multiple logistic regression Danhong Zhou models were conducted to explore the associated factors of different BMI trajectories, yun839@163.com and log-binomial regression was performed to assess the association between the † These authors have contributed trajectories and overweight/obesity. equally to this work Results: Three heterogeneous BMI trajectories were identified and labeled as “lower” Specialty section: (36.21%, n = 6,899), “middle” (53.15%, n = 10,128) and “upper” (10.64%, n = 2,027), This article was submitted to Children and Health, respectively. Several characteristics of infants and their corresponding mothers were a section of the journal found to be correlated with infant BMI trajectories, including infant sex, mode of Frontiers in Pediatrics delivery and weight at birth, as well as maternal parity, early pregnancy BMI and Received: 08 February 2021 status of gestational diabetes mellitus. Furthermore, compared with those in the lower Accepted: 13 April 2021 Published: 12 May 2021 trajectory, infants in the middle [prevalence ratio (PR) = 2.63, 95% confidence interval Citation: (95%CI) = 2.17–2.63] or upper (PR = 2.98, 95%CI = 1.51–2.98) trajectory groups were Zhang T, Song Y, Teng H, Zhang Y, prone to be overweight/obesity at their final observation. Lu J, Tao L, Jin Y, Yin J and Zhou D (2021) BMI Trajectories During the Conclusion: Heterogeneous BMI trajectories were observed in our study. First 2 Years, and Their Associations Characteristics of both infants and their corresponding mothers could be potential With Infant Overweight/Obesity: A Registered Based Cohort Study in determinants of infant growth. Moreover, infants in the middle and upper trajectory Taizhou, China. groups were more likely to suffer overweight/obesity. Front. Pediatr. 9:665655. doi: 10.3389/fped.2021.665655 Keywords: BMI trajectory, infant, overweight, obesity, latent class growth mixture model Frontiers in Pediatrics | www.frontiersin.org 1 May 2021 | Volume 9 | Article 665655
Zhang et al. BMI Trajectories and Infant Obesity INTRODUCTION reach the following research objectives: (1) to identify the latent BMI growth trajectories from birth to 2 years by Overweight and Obesity, defined by the World Health conducting LCGMM; (2) to explore the associated factors of Organization (WHO) as an abnormal or excessive fat the identified BMI trajectories; (3) to examine the associations accumulation, present an alarming risk to health (1). Childhood between different trajectories of BMI and overweight/obesity overweight and obesity have become a major public health in infancy. concern (2). In China, a national survey reported that the prevalence of overweight and obesity in children aged 7–17 years had increased rapidly from 3.8% and 0.6% in 1995 to METHODS 14.3% and 4.1% in 2014, respectively (3). Excessive weight gain Study Population in early life is likely to lead to lifelong overweight and obesity A total of 29,274 singleton children who born in any hospital or (4). Meanwhile, childhood overweight/obesity is associated community healthcare center in Taizhou city from 01/01/2018- with greater risk and earlier onset of chronic disorders, such 31/12/2019 were recruited in our study. Information for as heart disease, asthma, type 2 diabetes, and psychosocial children and their corresponding mothers were collected through disorders (5–7). Thus, the early identification and intervention questionnaires or medical records. First, exclusion was made of overweight/obesity in infants is critical to their long-term for participants with uncompleted information of prenatal health conditions. characteristics [maternal BMI at early stage of pregnancy (n = Body mass index (BMI) is widely accepted to assess children’s 2,330)]. Second, we excluded infants with missing intrapartum weight status. As we known, BMI fluctuates in early life (8). In [mode of delivery (n = 169)] or postnatal data [missing for general, BMI rapidly increases during the 1st year after birth, follow-up during 0–2 years old (n = 3,176) and without then decreases until reaching a nadir around 6 years of age (also gender information (n = 3)], resulting in a total of 23,596 called the adiposity rebound); thereafter, BMI increases again participants. Third, we excluded 4,542 infants who received
Zhang et al. BMI Trajectories and Infant Obesity FIGURE 1 | Flow chart for selection process of the study. into four levels: primary school or below, junior school, high fits the data. For each model involving latent classes, posterior school, university or above. Maternal age at delivery was class-membership probabilities (PP) were also used to obtain a divided into four categories (600 IU/d). classified in each class with a PP above a threshold of 0.7, Outdoor activity duration was divided into three levels (0–1, 1–2, indicating the proportion of subjects unambiguously classified >2 h/day). in each latent class (13). These procedures indicated that a Other maternal characteristics were then retrieved from model with three trajectories (with cubic curve assumption) medical records. Maternal BMI at early pregnancy was classified was superior to models with fewer trajectories because of much following Chinese BMI classification standard as lean (BMI < smaller BIC values. Although models with 4 or 5 trajectories had 18.5 kg/m2 ), normal (18.5 ≤ BMI ≤ 23.9 kg/m2 ), overweight smaller BIC values than the three trajectories, the former models (24 ≤ BMI ≤ 27.9 kg/m2 ) and obese (BMI ≥ 28 kg/m2 ) (22). yielded trajectories with 0.7
Zhang et al. BMI Trajectories and Infant Obesity FIGURE 2 | BMI trajectories from birth to 2 years old identified from the LCGMM. 3 additionally adjusted for maternal factors, including parity, 14 and 49 years old [mean = 30.61, standard deviation (SD) = early pregnancy BMI, gestational diabetes mellitus (GDM), and 5.22]. Mothers who received education of high school or above gestational hypertension. Based on Model 3, model 4 further accounted for 67.15%. A slightly larger number of mothers gave included infants’ characteristics, such as mode of delivery, birth to a male infant (52.34%) or delivered by cesarean section outdoor activity duration, maternal feeding styles, SGA, infant (51.02%). Few mothers drank (0.18%) or smoked (0.10%) during age at the final observation, and intake of vitamin D. At last, pregnancy. Besides, the mean birth weight of the infants was subgroups analyses by sex were conducted to see whether there 3320.30 (SD = 393.87) grams and the mean gestational age at are any gender differences. All statistical tests were performed delivery was 38.99 (SD = 1.24) weeks. A total of 2,994 (15.71%) using SAS software (version 9.4, SAS Institute, Cary, NC, USA), infants were identified as overweight and 1,821 (9.56%) became and differences were considered statistically significant with two- obese at their final observation. Meanwhile, infants born from sided P ≤ 0.05. mothers with multiparity, higher BMI at early pregnancy, or GDM were more likely to be in the upper group. Also, infantile characteristics such as gender, gestational age, birth weight, and RESULTS outdoor time differed among three trajectory groups. BMI Trajectories A total of 19,054 singleton children delivered at 28–44 weeks Predictors of BMI Trajectories of gestation were enrolled in our study. The infants had a Table 2 presents the associations between prenatal as well total of 101,251 BMI measurements since birth, the median as infantile factors and their growth trajectories. Birth to a measurement times of each infant was 5 (interquartile range, multiparous mother [odds ratio (OR) = 1.28, 95% confidence 4–6). Three distinct BMI trajectory groups were identified interval (95%CI) = 1.15–1.42] was a risk factor for being in the (Figure 2). They were labeled as “lower” (n = 6,899, 36.21%), upper trajectory group. Maternal obesity (BMI ≥ 28 kg/m2 ) at “middle” (n = 10,128, 53.15%) and “upper” (n = 2,027, 10.64%), early stage of pregnancy (OR = 2.41, 95%CI = 1.95–2.97) and respectively. The lower trajectory started with relatively low BMI complicated with GDM (OR = 1.18, 95%CI = 1.03–1.35) were (12.97 kg/m2 ), then followed with a steady acceleration until the also associated with increased risk of belonging to the upper age of seven months (16.83 kg/m2 ). After peaking at 7 months, it trajectory. Besides, the highest BMI groups tended to include declined gradually and reached the lowest point at 17 months, infants who had exclusive breastfeeding (OR = 1.14, 95%CI = followed by an increase subsequently. The middle trajectory 1.03–1.26) or male gender (OR = 5.71, 95%CI = 5.10–6.39). started with a mid-level BMI (13.75 kg/m2 ), while the upper one However, vaginally delivered (OR = 0.60, 95%CI = 0.54–0.66) showed a higher level of BMI (14.44 kg/m2 ) at beginning. Both of and SGA (OR = 0.07, 95%CI = 0.05–0.10) infants were less likely them reached the climax at 7 months (“middle” = 18.47 kg/m2 , to be grouped into the upper trajectory. “upper” = 20.58 kg/m2 ) and the lowest point at 17 months after birth, which were parallel to the process of the lower one. The Association Between BMI Trajectories and slope and intercept of the specific trajectories were present in Infant Overweight/Obesity Supplementary Table 1.2. As shown in Table 3, 1.51, 28.88, and 88.11% of participants were overweight/obesity in the lower, the middle and the upper Baseline Characteristics trajectory groups, respectively. In comparison with children in Characteristics of infants and their mothers were illustrated in the lower trajectory, children in the middle trajectory group Table 1. In the included population, maternal age ranged between [prevalence ratio (PR) = 19.16, 95%CI = 15.89–23.39] and the Frontiers in Pediatrics | www.frontiersin.org 4 May 2021 | Volume 9 | Article 665655
Zhang et al. BMI Trajectories and Infant Obesity TABLE 1 | Characteristics of mother-child pairs by BMI trajectories. Variables Total population Lower trajectory Middle trajectory Upper trajectory P-value N = 19,054 n = 6,899 n = 10,128 n = 2,027 Maternal characteristics Maternal demographics Age (years) (mean ± SD) 30.61 ± 5.22 30.56 ± 5.31 30.66 ± 5.20 30.56 ± 4.99 0.415 Education, n (%) 0.123 Primary school or below 1,201 (6.30%) 474 (6.87%) 617 (6.09%) 110 (5.43%) Junior school 5,059 (26.55%) 1,826 (26.47%) 2,664 (26.30%) 569 (28.07%) High school 4,892 (25.68%) 1,739 (25.21%) 2,639 (26.06%) 514 (25.36%) University or above 7,902 (41.47%) 2,860 (41.45%) 4,208 (41.55%) 834 (41.14%) Parity, n (%)
Zhang et al. BMI Trajectories and Infant Obesity TABLE 1 | Continued Variables Total population Lower trajectory Middle trajectory Upper trajectory P-value N = 19,054 n = 6,899 n = 10,128 n = 2,027 Daily intake of vitamin D (IU/d), n (%) 0.254 0 ≤ vitamin D ≤ 400 16,423 (86.19%) 5,942 (86.13%) 8,736 (86.26%) 1,745 (86.09%) 400 < vitamin D ≤ 600 2,193 (11.51%) 777 (11.26%) 1,175 (11.60%) 241 (11.89%) 600 < vitamin D 438 (2.30%) 180 (2.61%) 217 (2.14%) 41 (2.02%) Outdoor activity duration (hours/d), n (%) 0.002 0–1 424 (2.23%) 138 (2.00%) 237 (2.34%) 49 (2.42%) 1–2 5,391 (28.29%) 1,890 (27.40%) 2,861 (28.25%) 640 (31.57%) ≥2 13,239 (69.48%) 4,871 (70.60%) 7,030 (69.41%) 1,338 (66.01%) Overweight, n (%) 2,994 (15.71%) 95 (1.38%) 2,278 (22.49%) 621 (30.64%)
Zhang et al. BMI Trajectories and Infant Obesity TABLE 2 | Association between prenatal and early life factors with middle and TABLE 2 | Continued upper BMI trajectories in comparison to the lower trajectory group. Variables Middle Upper Variables Middle Upper trajectory trajectory trajectory trajectory OR (95%CI) OR (95%CI) OR (95%CI) OR (95%CI) Yes 0.24 (0.22–0.27) 0.07 (0.05–0.10) Maternal characteristics Mode of delivery Maternal demographics Cesarean 1.00 (reference) 1.00 (reference) Age (years) Vaginal delivery 0.83 (0.78–0.89) 0.60 (0.54–0.66)
Zhang et al. BMI Trajectories and Infant Obesity of rising infant weight gain patterns (39), and the underlying DATA AVAILABILITY STATEMENT mechanisms remain unclear. Strengths of our study lie in the relatively large sample size The raw data supporting the conclusions of this article will be and the continuity of infant growth period up to 2 years old. made available by the authors, without undue reservation. Studies focusing on BMI trajectories were mainly children from western countries (18–20). Regional differences may exist in ETHICS STATEMENT BMI trajectories which vary in terms of dimensions, elevation, living habits, dietary habits, and socio-economic status. The The studies involving human participants were reviewed and participants in our study come from Taizhou, a south-eastern approved by ethic committee of Medical College of Soochow coastal city located in Zhejiang Province, China. The geographic University. Written informed consent to participate in this study location of the city is 120◦ 34’ E and 28◦ 50’ N. It has more than was provided by the participants’ legal guardian/next of kin. 5.97 million permanent residents, features a booming economy Written informed consent was obtained from the individual(s), and high population density. Given the paucity of data on growth and minor(s)’ legal guardian/next of kin, for the publication of trajectories in Asian population, our study enriched the field and any potentially identifiable images or data included in this article. may help develop intervention strategies to control the rapidly increasing prevalence of childhood obesity. AUTHOR CONTRIBUTIONS There remained some limitations in our current study. Firstly, other potential confounding factors, such as paternal JY and DZ has contributed to the design and concept of characteristics, genetics, environmental and dietary habits (40), the manuscript. TZ and YS were responsible for the analysis, were not assessed in the current study. Secondly, due to interpretation of data and manuscript drafting. HT, YZ, JL, LT, the nature of observational study, we cannot infer the causal and YJ were responsible for critical revision of the manuscript relationship between those possible risk factors and changes in for intellectual content. All authors were involved in writing infant BMI. Thirdly, children included in our study are from the paper and had final approval of the submitted and Taizhou city in China, and thus may not be representative for published versions. other parts of China and other nationalities. Considering these limitations, further studies are needed. FUNDING This study was supported by a Project of the Priority CONCLUSION Academic Program Development of Jiangsu Higher Education Three distinct latent BMI trajectories were identified for children Institutions (PAPD). from birth to 2 years old including the lower, middle and upper groups. Infants in the middle and upper trajectory groups SUPPLEMENTARY MATERIAL are more likely to be obese late in their life. Our results also underline the importance of the timely intervention on children The Supplementary Material for this article can be found overweight/obesity targeted at potential risk factors during both online at: https://www.frontiersin.org/articles/10.3389/fped. prenatal and postnatal period. 2021.665655/full#supplementary-material REFERENCES 6. Skinner AC, Perrin EM, Moss LA, Skelton JA. Cardiometabolic risks and severity of obesity in children and young adults. N Engl J Med. (2015) 1. WHO. Obesity. (2020). 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Catalano PM, Shankar K. Obesity and pregnancy: mechanisms of short term open-access article distributed under the terms of the Creative Commons Attribution and long term adverse consequences for mother and child. BMJ. (2017) License (CC BY). The use, distribution or reproduction in other forums is permitted, 356:j1. doi: 10.1136/bmj.j1 provided the original author(s) and the copyright owner(s) are credited and that the 28. Choi HJ, Lee HJ, Jang HB, Park JY, Kang JH, Park KH, et al. Effects of maternal original publication in this journal is cited, in accordance with accepted academic education on diet, anemia, and iron deficiency in Korean school-aged practice. No use, distribution or reproduction is permitted which does not comply children. BMC Public Health. (2011) 11:870. doi: 10.1186/1471-2458-11-870 with these terms. Frontiers in Pediatrics | www.frontiersin.org 9 May 2021 | Volume 9 | Article 665655
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