Elsevier

Nutrition

Volume 30, Issues 11–12, November–December 2014, Pages 1442-1447
Nutrition

Basic nutritional investigation
Effects of maternal over- and undernutrition on intestinal morphology, enzyme activity, and gene expression of nutrient transporters in newborn and weaned pigs

https://doi.org/10.1016/j.nut.2014.04.016Get rights and content

Abstract

Objectives

It has been suggested that maternal nutrition during gestation is involved in the offspring's intestinal development. The aim of this study was to evaluate the effects of maternal nutrition on digestive and absorptive function of offspring at both birth and weaning with pig as model.

Methods

Eighteen primiparous Landrace × Yorkshire gilts (ages 253 ± 9 d; body weight 148.6 ± 6.9 kg) were allocated to a normal nutrition (control) group as recommended by the National Research Council (NRC; 1998), an undernutrition (UN) group (75% of NRC recommendations), and an overnutrition (ON) group (150% of NRC recommendations); the nutritional treatments were introduced from day 1 of gestation to farrowing.

Results

By comparison, the small intestine weight (+33%; P < 0.01) and the ratio of small intestine weight to length (+25%; P < 0.05) for the ON group were higher than those for the control group. Meanwhile, the maternal ON treatment had significant effect on the activity of brush border lactase in the jejunum (+125%; P < 0.05) at birth. Expression of mRNA for SGLT1, GLUT2, PEPT1, and GLP2R were significantly increased (+1.7∼9.6-fold; P < 0.05) in jejunum of newborn or weaned piglets from the ON group; whereas maternal UN significantly affected small intestine weight (–28%; P < 0.01), length, and the ratio of weight to length (–11% and –19%; P < 0.05, respectively), and villus height (–29% and –22%; P < 0.05, respectively) in jejunum and ileum. Furthermore, maternal UN enhanced the activity of brush border lactase in the jejunum of newborn piglets (P < 0.05).

Conclusions

Maternal ON enhanced intestinal function via up-regulating digestive enzyme activities and gene expression of transporters in both newborn and weaning piglets. Maternal UN impaired fetal intestinal development that could be partially compensated during the neonatal period.

Introduction

An excess or deficiency of nutrients during gestation affects fetal development, leading to adult offspring adiposity and cardiovascular and metabolic dysfunction [1], [2]. Increasing evidence has led to the concept of “developmental programming,” which has shown that early nutrition has long-term effects on later health and the risk for common noncommunicable diseases, although the mechanisms involved are not well known [3].

The gut, which is susceptible to the early life environment, changes throughout one's lifetime. In addition to be genetically determined, intestinal morphology and function are always the results of adaptation to intrauterine environment, diet, or stress. The early forced adaptation may persist in later life, such as the unwanted increasing intestinal absorption of sugars, fatty acids, and cholesterol, leading to physiological or pathologic challenges in later life [4], [5].

Recently, there has been a growing interest concerning the effects of maternal nutrient excess on offspring because excessive nutrition during gestation may induce high birth weight, which results in rapid growth in postnatal life, adiposity, and hypertension, cardiovascular, and metabolic dysfunction [2], [6]. The larger fetuses induced by maternal overnutrition (ON) may have congenital advantages in nutrient utilization, which would be more obvious over time. Therefore, we investigated whether maternal ON may modify the intestinal development and function, which consequently enhances digestibility and absorption of nutrients for rapid growth.

In contrast, maternal undernutrition (UN) during gestation resulted in intrauterine growth restriction (IUGR) and newborns with low birth weight (LBW). LBW newborns have increased risk for the development of adult metabolic syndrome [7]. Moreover, IUGR neonates would have compensation growth, gradually reducing gaps of body weight and intestinal weight between IUGR and normal infants if IUGR neonates are supplied abundant food during the lactation period [8], [9]. However, it is not known whether the compensative growth is related to positive digestion and absorption function. Additionally, whether digestive and absorptive response to maternal nutrition could postnatally persist is warranting, especially considering that maternal nutrition during gestation has lasting effects on the offspring's jejunal vascularity and gene expression [6].

In this study, the effects of maternal ON or UN on digestive and absorptive functioning of intestine at both birth and weaning were determined by assessing activities and mRNA expression of digestive enzymes and gene expression of transporters such as SGLT1, GLUT2, and PEPT1 in the small intestine of piglets.

Section snippets

Materials and methods

The experimental procedures were approved by the University of Sichuan Agricultural Animal Care Advisory committee, and followed the current law of animal protection.

Body weight and SI index

Maternal ON significantly increased birth weight (+19%; P < 0.01) and weaned weight of piglets (+12%; P < 0.05); whereas maternal UN affected birth weight (–22%; P < 0.01) and weaned weight of piglets (–11%; P < 0.05). SI weight (+33%; P < 0.01) and the ratio of weight to length (weight per unit of length, ratio of SI weight to length in the ON and UN groups at weaning exhibited no significant differences compared with the CON group (P > 0.05) (Table 3).

Intestinal morphology

dered jejunal and ileal villi dered

Discussion

Maternal food intake is not only required for maintaining pregnancy but also determines fetal growth, which is positively correlated with maternal nutrition levels [13]. The higher birth weight caused by maternal ON generally lasts through postnatal life. It has been reported that higher birth weight neonates are vulnerable for heavier future body weight, which may suggest an increase in digestive and absorptive capabilities [14].

In this study, maternal ON during gestation significantly

Conclusion

Maternal ON enhanced intestinal function via up-regulation of digestive enzyme activities and gene expression of transporters in both newborn and weaning piglets; in contrast, maternal UN impaired fetal intestinal development that could be partially compensated during neonatal period.

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  • Cited by (0)

    This study was supported by grants from: 1) Research and Demonstration of High Efficiency and Low Consumption of Feed Processing Technology (201203015), China; 2) National Natural Science Foundation of China (31072044), China. MC, LC, and JW contributed equally to the work.

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