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Early nutrition and phenotypic development: 'catch-up' growth leads to elevated metabolic rate in adulthood.

ABSTRACT: Resting metabolic rate (RMR) is responsible for up to 50% of total energy expenditure, and so should be under strong selection pressure, yet it shows extensive intraspecific variation and a low heritability. Environmental conditions during growth are thought to have long-term effects through 'metabolic programming'. Here we investigate whether nutritional conditions early in life can alter RMR in adulthood, and whether this is due to growth acceleration or the change in diet quality that prompts it. We manipulated dietary protein levels during the main growth period of zebra finches (Taeniopygia guttata) such that an episode of poor nutrition occurred with and without growth acceleration. This produced different growth trajectories but a similar adult body mass. Only the diet that induced growth acceleration resulted in a significant (19%) elevation of RMR at adulthood, despite all the birds having been on the same diet after the first month. This is the first study to show that dietary-induced differences in growth trajectories can have a long-term effect on adult metabolic rate. It suggests that modification of metabolic efficiency may be one of the mechanisms mediating the observed long-term costs of accelerated growth, and indicates links between early nutrition and the metabolic syndrome.

SUBMITTER: Criscuolo F

PROVIDER: S-EPMC2602660 | biostudies-literature | 2008 Jul

REPOSITORIES: biostudies-literature

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Early nutrition and phenotypic development: 'catch-up' growth leads to elevated metabolic rate in adulthood.

Criscuolo François F Monaghan Pat P Nasir Lubna L Metcalfe Neil B NB

Proceedings. Biological sciences 20080701 1642

Resting metabolic rate (RMR) is responsible for up to 50% of total energy expenditure, and so should be under strong selection pressure, yet it shows extensive intraspecific variation and a low heritability. Environmental conditions during growth are thought to have long-term effects through 'metabolic programming'. Here we investigate whether nutritional conditions early in life can alter RMR in adulthood, and whether this is due to growth acceleration or the change in diet quality that prompts ...[more]

PMID: 18397870

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Project description:In light of global climate change, there is a pressing need to understand and predict the capacity of populations to respond to rising temperatures. Metabolic rate is a key trait that is likely to influence the ability to cope with climate change. Yet, empirical and theoretical work on metabolic rate responses to temperature changes has so far produced mixed results and conflicting predictions.Our study addresses this issue using a novel approach of comparing fish populations in geothermally warmed lakes and adjacent ambient-temperature lakes in Iceland. This unique 'natural experiment' provides repeated and independent examples of populations experiencing contrasting thermal environments for many generations over a small geographic scale, thereby avoiding the confounding factors associated with latitudinal or elevational comparisons. Using Icelandic sticklebacks from three warm and three cold habitats, we measured individual metabolic rates across a range of acclimation temperatures to obtain reaction norms for each population.We found a general pattern for a lower standard metabolic rate (SMR) in sticklebacks from warm habitats when measured at a common temperature, as predicted by Krogh's rule. Metabolic rate differences between warm- and cold-habitat sticklebacks were more pronounced at more extreme acclimation temperatures, suggesting the release of cryptic genetic variation upon exposure to novel conditions, which can reveal hidden evolutionary potential. We also found a stronger divergence in metabolic rate between thermal habitats in allopatry than sympatry, indicating that gene flow may constrain physiological adaptation when dispersal between warm and cold habitats is possible.In sum, our study suggests that fish may diverge toward a lower SMR in a warming world, but this might depend on connectivity and gene flow between different thermal habitats. A free Plain Language Summary can be found within the Supporting Information of this article.

Project description:Diarrhea and linear growth faltering continue to burden low-income countries and are among the most important contributors to poor health during early childhood. Diarrhea is thought to adversely affect linear growth, but catch-up growth can occur if no additional insults are experienced. We sought to characterize catch-up growth in relation to diarrhea burden in a multisite dataset of 1007 children. Using longitudinal anthropometry and diarrheal surveillance data from 7 cohort studies in 4 countries, we examined the relation between diarrhea prevalence and growth in 3- to 6-mo periods using linear mixed-effect models. Growth during each period was calculated as a function of age using linear splines. We incorporated the longitudinal prevalence of diarrhea in both current and previous periods into the model. Diarrhea during the current period was associated with slower linear and ponderal growth. Faster (catch-up) growth in length was observed in children with no diarrhea in age groups immediately after an age group in which diarrhea was experienced [age group >6-12 mo: 0.03 mm/mo for each percentage diarrhea prevalence in the previous period (95% CI: 0.007, 0.06) relative to 11.3 mm/mo mean growth rate; age group >12-18 mo: 0.04 mm/mo (95% CI: 0.02, 0.06) relative to 8.9 mm/mo mean growth rate; age group >18-24 mo: 0.04 mm/mo (95% CI: 0.003, 0.09) relative to 7.9 mm/mo mean growth rate]. The associations were stronger in boys than in girls when separate models were run. Similar results were observed when weight was the outcome variable. When diarrheal episodes are followed by diarrhea-free periods in the first 2 y of life, catch-up growth is observed that may allow children to regain their original trajectories. The finding of a greater effect of diarrhea on linear growth in boys than in girls was unexpected and requires additional study. Diarrhea burdens are high throughout the first 2 y of life in these study sites, therefore reducing the likelihood of catch-up growth. Extending diarrhea-free periods may increase the likelihood of catch-up growth and decrease the prevalence of stunting.

Project description:Nutrition in pregnancy and early childhood affects later blood pressure and precursors of atherosclerosis, but its influence on arterial stiffness is unexplored. This study determines whether exposure to improved nutrition during early life influences Augmentation index (AI) and pulse wave velocity (PWV) in mid-adulthood. We included 1221 adults (37-54y) who participated in a cluster-randomized nutritional supplementation trial of a protein-energy beverage (Atole), conducted between 1969-1977 in Guatemala. The comparison group received Fresco, a low-calorie protein-free beverage. In 2015-17, we measured anthropometry (weight, height, and waist-to-height ratio); AI and PWV (using carotid-femoral tonometry); blood pressure; fasting plasma glucose and serum lipids; and sociodemographic characteristics. Based on patterns of exposure, we characterized participants as fully, partially or unexposed to the intervention from conception to their second birthday (the 'first 1000 days'). We fit pooled and sex-specific models using intention-to-treat, difference-in-difference regression analysis to test whether exposure to the supplement in the first 1000 days was associated with AI and PWV in adulthood adjusting for basal and current sociodemographic variables and current life-style and cardio-metabolic risk factors. Prevalence of obesity in men and women was 39.6% and 19.6%, and prevalence of hypertension was 44.0% and 36.0%, respectively. Women had higher AI (34.4±9.6%) compared to men (23.0± 9.8%), but had similar PWV (7.60±1.13 m/s and 7.60±1.31, respectively). AI did not differ significantly across intervention groups. PWV was lower in individuals with full exposure to the supplement during the first 1000 days (-0.39m/s, 95% CI -0.87, 0.09; p = 0.1) compared to unexposed individuals. This difference was similar after adjusting for cardio-metabolic risk factors (-0.45m/s; 95%C-0.93, 0.01; p = 0.06). Exposure to improved nutrition during the first 1000 days was marginally associated with lower PWV, but not with AI.

Dataset Information

Early nutrition and phenotypic development: 'catch-up' growth leads to elevated metabolic rate in adulthood.

Publications

Early nutrition and phenotypic development: 'catch-up' growth leads to elevated metabolic rate in adulthood.

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