Background

The “First 1000 Days” and “Developmental Origins of Health and Disease” theories emphasize the critical role of early-life nutrition and growth in sha** long-term health outcomes [1, 2]. Therefore, investigating the factors influencing child growth to identify early targets for malnutrition prevention and intervention, and promote optimal growth in early life, has long been a focus for pediatricians and society. While genetic and environmental factors are known to be essential in sha** growth trajectories [3], there is currently no definitive conclusion on how these factors specifically influence child growth. In particular, considering the stagewise nature of child growth, exposure and susceptibility to risk factors might vary at different stages. For example, the effects of introducting complementary foods usually emerge after 6 months of age [4], while some perinatal factors, such as maternal nutrition and illness, as well as neonatal complications, could tend to affect or have a greater impact on younger infants. At present, specific risk factors influencing infant growth stratified by age are yet to be elucidated. In addition, previous studies have focused primarily on the factors influencing the growth of high-risk infants, particularly preterm and low birth weight infants [5, 6]. There are limited studies that have explored the factors affecting early-life growth in term infants, as they are typically considered “healthy” from birth [7]. However, given that term infants account for the vast majority of the population (90%) [8], investigating the factors associated with their growth could make a significant contribution to the overall health status of the population.

A substantial body of research on preterm infants has established a clear link between lower gestational age (GA) at birth and elevated risks of neonatal morbidity and mortality, as well as detrimental effects on both short-term and long-term physical growth and neurological development [9, 10]. Moreover, over the past decade, the impact of GA on the health of term infants has gained increasing attention. Given the heightened risk of neonatal complications and hospitalization for infants born at less than 39 weeks of gestation, the American College of Obstetricians and Gynecologists introduced the “39-week rule” in 2009 to reduce nonmedically indicated elective cesarean delivery before 39 weeks [11]. Additionally, growing evidence suggests that, similar to late preterm infants (GA 34–36 weeks), early-term births (GA 37–38 weeks) also exhibit impairment in long-term neurological outcomes [12, 13]. These findings reinforced the recommendation to delay delivery until 39 weeks. However, the existing evidence primarily focuses on the association between early-term birth and perinatal and long-term neurological risks, with limited literature on the correlation between early-term birth and physical growth and nutritional status in children. There is currently scarce research on whether early-term birth is correlated with adverse physical growth and an increased risk of malnutrition.

Early life nutrition has always been considered the most important regulable environmental factor affecting the growth of infants [14]. However, given the heterogeneity in research related to nutrition and its impact on growth outcomes [15] and the complex and intertwined relationships between different feeding practices (such as breastfeeding and complementary feeding) [16], there is currently no clear conclusion regarding the influence of early-life feeding practices on the risk of malnutrition and physical growth at different stages of infancy.

Therefore, this study aims to explore the associations of GA at birth (early-term: 37–38 weeks, and full-term: GA 39–41 weeks) and feeding pattern (exclusive breastfeeding, mixed feeding and exclusive formula-feeding) with anthropometric indicators and the risk of malnutrition in singleton term infants at two stages of infancy (0–5 months and 6–12 months) while controlling for potential influencing factors.

Methods

Study design

This was a multicenter cross-sectional study. The data utilized in this study, including information on breastfeeding practices, birth characteristics, physical and nutritional indicators, etc., were collected through the survey of “Infant Body Composition Study” [29] and (3) in addition to excess nutritional intake and a sedentary lifestyle, other potential causes and mechanisms leading to obesity have not yet been fully elucidated [30]. The finding of the association between early-term delivery and a greater risk of overweight and obesity in infants may have important implications for the early intervention of overweight and obesity. However, the underlying mechanisms of the association between early-term birth and the risk of overweight and obesity remain unclear and require further exploration. Previous studies reported a correlation between smaller gestational age and slower length growth in late preterm infants (GA 34–36 weeks) [5, 31], which aligns with the association of early-term birth with poorer length growth in early-term infants observed in this study. Specifically, the significantly lower length growth accompanied by relatively normal weight growth in early-term infants than in full-term infants might be a direct cause of the increased risk of overweight and obesity in early-term infants. Even so, the potential mechanisms underlying the association between early-term birth and adverse linear growth and overweight and obesity remain unclear, necessitating further clinical and laboratory research. Overall, this study contributes to the growing body of evidence on the potential health risks of early-term delivery for offspring [12, 13], indicating that nonmedically indicated elective cesarean delivery before 39 weeks should be avoided.

MSAM (wasting) among infants under six months remains a major global health concern. Recent analyses of data from Demographic Health Survey in 56 countries estimates that 21.3% of infants under six months are wasted [32]. These infants are at increased risk of mortality, morbidity and poor growth and development in both the short and long term. Early-life nutrition plays a pivotal role in influencing the growth and development of infants [33] and is one of the most significant modifiable environmental factors [4]. Among these factors, breastfeeding has been convinced to be the most important intervention for improving malnutrition in infants and young children [34]. In addition, exclusive breastfeeding is a crucial public health intervention that not only provides optimal nutrition but also provides economic, social, and health benefits [35, 36]. However, evidence on the effect of breastfeeding promotion on growth and nutrition is equivocal [37]. This might be attributed to the ambiguity in defining breastfeeding practices (exclusive breastfeeding, predominant breastfeeding, and any/partial breastfeeding, etc.), as well as differences in age, ethnicity, and economic environments (low-, middle-, and high-income settings). However, the duration, intensity, and quantity and exclusivity of breastfeeding have been shown to be important in quantifying the benefits of breastfeeding for both children and mothers [38]. Our study suggested that compared to exclusive formula-feeding and mixed feeding, exclusive breastfeeding was linked to higher WLZ and the lowest risk of moderate and severe acute malnutrition in infants under 6 months old, without an increased risk of overweight and obesity. These findings emphasize the importance of the exclusivity of breastfeeding in infants under 6 months of age, highlighting the continued support and promotion of exclusive breastfeeding in this age group [35]. Similar to our findings, Rebhan et al. also demonstrated the lower WLZ in infants who were not breastfed compared to infants who were breastfed before 6 months of age [16]. However, a systematic review and meta-analysis indicated that breastfeeding interventions led to a slight but significant reduction in body mass index/Weight-for-Height Z-scores (Z-score mean difference: -0.06, 95%CI: -0.12, 0.00)) in children under 5 years [39]. Nonetheless, this effect was observed only in low- and high-income countries, but not in middle-income countries. Additionally, this effect was not observed in infants under 6 months of age. Considering that: (1) our study was an observational study, not an intervention study promoting breastfeeding; (2) our study was conducted in China, a middle-income country, rather than low- and high-income countries; (3) our study included infants aged 0–12 months, rather than children under 5 years old; these factors may contribute to the discrepancies in our findings compared to the aforementioned meta-analyses [39]. Nonetheless, the findings of our study provide additional evidence supporting the beneficial effects of exclusive breastfeeding during the first six months of life [34, 35]. However, the specific mechanisms for this correlation are yet to be elucidated. Breastfeeding might promote infant growth and nutrition through its nutritional properties and by reducing incidence and severity of potentially growth-affecting infections, especially diarrhoea and respiratory diseases [36]. Moving forward, further investigation is crucial to explore the evidence and potential mechanisms behind the nutritional and growth benefits of exclusive breastfeeding in infants under 6 months old in China and similar middle-income countries.

The strengths of this study lie in several key aspects. First, the research was carried out using a substantial sample of singleton term infants from medical centers located in four cities in northern China, with the demographic characteristics of the sample comparable to those of a national study [40]. Moreover, the feeding and nutritional practices were in line with international recommendations [18]. As a result, the data obtained from this study can be considered representative of healthy singleton term infants without significant growth restrictions in China and in countries with similar economic and cultural backgrounds. Second, this study accounted for important influencing factors that could impact infant growth at various stages, integrating them as covariates in the models. Furthermore, sensitivity analysis was performed to ensure the robustness and reliability of the research findings. Third, the evidence from this study is compelling and enhances our comprehension of the health risks associated with early-term infants and the benefits of exclusive breastfeeding, some of which were previously overlooked. This includes the link between early-term birth and a heightened risk of overweight and obesity, emphasizing the necessity for targeted interventions to prevent nonmedically indicated early-term deliveries.

The present study also has several limitations that should be considered when interpreting the findings. First, the observational design of the study restricts the ability to establish causality between perinatal factors and infant growth. Second, the reliance on maternal self-reports of feeding practices may introduce bias. Third, potential perinatal factors that could influence postnatal growth, such as the quantity and quality of complementary food and family social and economic circumstances, may not have been documented. Further cohort studies are needed to validate the impact and duration of gestational age at birth and early feeding practices on the short-term and long-term health of children.

Conclusions

In conclusion, this study revealed the link between early-term birth and an elevated risk of overweight and obesity during infancy, as well as the correlation between exclusive breastfeeding and a reduced risk of moderate and severe acute malnutrition in infants under 6 months of age. These findings highlight the significance of avoiding nonmedically indicated deliveries before 39 weeks and further advocating for exclusive breastfeeding before 6 months of age.