Weaning and stunting affect nitrogen and carbon stable isotope natural abundances in the hair of young children

Abstract

Natural abundances of stable nitrogen and carbon isotopes (δ 15 n and δ 13 C) can vary with both dietary intake and metabolic (specifically catabolic) state. In low-income countries, weaning is a period of dietary transition from milk to plant-based foods and a high-risk period for malnutrition. We explored how diet and malnutrition impact hair δ 15 n and δ 13 C in young children by an observational, crosssectional study in Cox's Bazar District, Bangladesh [255 children, 6-59 months with 19.6% wasted (7.1% severely) and 36% stunted (9.8% severely)]. Hair δ 15 n and δ 13 C exhibited exponential decreases with age, with the loss of one trophic level (3.3‰ and 0.8‰, respectively) from 6 to 48 months, which we associate with the shift from exclusive breastfeeding to complete weaning. After adjustment for age and breastfeeding status, hair isotopic values were unaffected by wasting but lower in severe stunting (−0.45‰ to −0.6‰, P < 0.01). In this population of young children, whose isotopic values in hair primarily depended on age, we failed to observe any effect of wasting, likely due to opposite, compensating effects between dietary and metabolic changes involved. In contrast, we evidenced low δ 15 n and δ 13 C values in severely stunted children that likely indicate chronic exposure to diets low in animal products. The natural abundances of stable carbon and nitrogen heavy isotopes (δ 13 C and δ 15 N) in body proteins reflect those of the diet, plus a small discrimination factor, known as the trophic step, which is due to the preferential elimination of light isotopes and is smaller for carbon (+1‰) than for nitrogen (+3-4‰) 1,2. Since δ 13 C and δ 15 N values in the body primarily reflect those of the diet, they have long been used in ecology and archaeology to reconstruct trophic webs and characterize ancient diets 3-6. More recently, they have been used in epidemiology as biomarkers to assess the consumption of fish, animal products, and sugar 7-13. In this regard, measuring isotopic natural abundances in hair has several advantages. Hair is easily and non-invasively sampled and its isotopic values correlate well with those in other body proteins. Moreover, hair keratin is an ideal isotopic archive because it is produced sequentially and is inert after synthesis 14,15 , provided that a sufficient number of follicles is sampled to limit the potential bias due to the presence of a small proportion of hair in the telogen phase, i.e. not growing 15-17. Considering an average hair growth rate of 1 cm per month 17,18 and a one-week delay between hair synthesis and bulb exit 19 , the 5 mm of hair closest to the scalp contains isotopic information for the period between −3 and −1 weeks before sampling.

Carbon, nitrogen, and oxygen stable isotopes in modern tooth enamel: A case study from Gorongosa National Park, central Mozambique

“…Tooth enamel is, therefore, one of the only archives in the vertebrate body that records dietary information from early life stages (i.e., infant to youngadult) and that is also preserved in the fossil record. To reconstruct the adult diet and avoid the isotopic effect of breast milk consumption (Fuller et al, 2006;Tsutaya and Yoneda, 2015;Dailey-Chwalibóg et al, 2020;Chinique de Armas et al, 2022), we targeted the latest-forming permanent tooth (i.e., usually M3) in each specimen (for details refer to Supplementary Data Sheet 1 and Supplementary Table 1).…”

Reconstructing Hominin Diets with Stable Isotope Analysis of Amino Acids: New Perspectives and Future Directions

“…Moreover, a growing number of projects using modern human and primate hair and teeth, within appropriate ethically designed studies, have been used to better understand patterns of bulk isotope variation connected to the environment (Macho and Lee-Thorp 2014 ), season (Oelze 2016 ), weaning (Dailey-Chwalibóg et al. 2020 ), and physiological stress ( D'Ortenzio et al. 2015 , Crowley et al.…”

The “post-weanling’s conundrum”: exploring the impact of infant and child feeding practices on early mortality in the Bronze Age burial cave of Moro de Alins, north-eastern Iberia, through stable isotope analysis

“…It is likely, however, that opposite compensating effects between dietary and metabolic changes have masked δ 15 N and δ 13 C disparities and instances of opposing covariance (catabolic change) thus preventing detection of existing protein and/or calorie deficits during exclusive breastfeeding and/or weaning among non-survivors. For example, a δ 15 N increase due to muscle wasting resulting from severe protein malnutrition during weaning would be blurred by an antagonistic δ 15 N decrease from the introduction of low-trophic-level cereals (Dailey-Chwalibóg et al 2020), especially while maternal breastmilk still provided from one-third to half of a child's energy needs. Similarly, a metabolic decrease in δ 13 C values may be partially blurred by an overlapping decrease as a result of the introduction of complementary foods of lower trophic level.…”

“…However, research has recently suggested that juvenile bone collagen may not be a reliable source for reconstructing past early lifeways (e.g., Beaumont 2020;Beaumont et al 2018;Fernández-Crespo et al 2018). The fractionation process through which δ 13 C and δ 15 N isotopes are incorporated into body tissues can be affected by in vivo metabolic activity (e.g., Minagawa and Wada 1984) resulting from malnutrition, illness, or other physiological factors (e.g., Dailey-Chwalibóg et al 2020;Fuller et al 2005;Neuberger et al 2013). Although the effect of growth on stable isotope ratios is not supported by some studies (Waters-Rist and Katzenberg 2010), it seems that bone collagen, especially if growth is stunted, may fail to adequately record dietary and physiological isotope signatures (e.g., Beaumont et al 2018).…”