Considerable progress has been made over the last decade in the understanding of mechanisms responsible for the ontogenetic changes of mammalian intestine. This review presents the current knowledge about the development of intestinal transport function in the context of intestinal mucosa ontogeny. The review predominantly focuses on signals that trigger and/or modulate the developmental changes of intestinal transport. After an overview of the proliferation and differentiation of intestinal mucosa, data about the bidirectional traffic (absorption and secretion) across the developing intestinal epithelium are presented. The largest part of the review is devoted to the description of developmental patterns concerning the absorption of nutrients, ions, water, vitamins, trace elements, and milk-borne biologically active substances. Furthermore, the review examines the development of intestinal secretion that has a variety of functions including maintenance of the fluidity of the intestinal content, lubrication of mucosal surface, and mucosal protection. The age-dependent shifts of absorption and secretion are the subject of integrated regulatory mechanisms, and hence, the input of hormonal, nervous, immune, and dietary signals is reviewed. Finally, the utilization of energy for transport processes in the developing intestine is highlighted, and the interactions between various sources of energy are discussed. The review ends with suggestions concerning possible directions of future research.

https://www.physiology.org/doi/pdf/10.1152/physrev.2000.80.4.1633

Development of Intestinal Transport Function in Mammals

This study investigated intestinal physiology of piglets at weaning. Piglets (n = 60) weaned at 21 d were food deprived for 2 d and then tube-fed using 2 different diets (a conventional diet vs. a wheat-enriched diet). They were slaughtered at d 0, 2, 5, 8, or 15 postweaning. Jejunum, ileum, and colon were mounted in Ussing chambers. In addition, segments of the proximal jejunum of 4 growing pigs were studied 35 d after weaning. Secretory function was assessed by basal short-circuit current (Isc) and secretagogue-stimulated Isc. Glucose absorption was measured by the increase in Isc after the addition of glucose. Epithelial barrier function was measured by transmucosal resistance (R) and horseradish peroxidase (HRP) fluxes across the epithelium. There were no significant differences between the pigs fed the 2 diets for any of the parameters studied. As already reported, a transient villous atrophy was observed. At the same time, we observed an increased basal Isc in jejunum and colon, increased glucose absorption and a dramatic drop of R in jejunum. These parameters had returned to preweaning values by d 5. Weaning was also followed by long-lasting modifications. In jejunum, responses to the secretagogues and glucose absorption were decreased at wk 2 after weaning and were not different between d 15 and 35. Ileal transmucosal resistance increased on d 5 and was stable thereafter. HRP flux in jejunum declined on d 2 and stayed at this low level throughout the experiment. We conclude that weaning induces transient dramatic changes in intestinal physiology but is also a period of maturation of the intestine.

/pdf/weaning-induces-both-transient-and-long-lasting-4ko2neqyow.pdf

Weaning Induces Both Transient and Long-Lasting Modifications of Absorptive, Secretory, and Barrier Properties of Piglet Intestine

The post-weaning period in pigs is characterized by an immediate but transient drop in feed intake resulting in severe undernutrition and growth check. This in turn affects various aspects of small intestinal architecture and function leading to gut-associated disorders and often diarrhea. Among these, villus atrophy and digestive enzyme activity depression have been documented. More recent investigations clearly demonstrate early signs of local inflammation including immune cell infiltration and increased pro-inflammatory cytokine gene expression, signs of cytoprotection through up-regulation of so-called heat shock proteins, indications of tissue alterations by proteases (stromelysin) and finally epithelial functional disorders in mineral absorption/secretion and perme- ability. This is followed by a regenerative phase, probably stimulated by feed intake resumption, resulting in down-regulation of many intestinal indicators. However, some of them then display new spatio-temporal adult-type adaptive patterns of maturation. A limited number of substances, partic- ularly nitrogenous compounds and complex preparations of animal origin (colostrum, plasma) have proven to be successful, at least partly, in minimizing post-weaning intestinal disturbances. Thus further research in intestinal physiology, in association with microbiology and immunology, is war- ranted to strengthen our understanding of the mechanisms of gut disorders in order to provide a better rational basis for designing suitable alternatives to in-feed antibiotics for pigs.

/pdf/gut-function-and-dysfunction-in-young-pigs-physiology-1hrvzmh37f.pdf

Gut function and dysfunction in young pigs: physiology

The nutritional and immunological importance of colostrum for the survival and development of the neonatal pig are reviewed. The pig is born with low body energy stores and devoid of serum immunoglobulins. Colostrum provides the piglet with both energy and maternal antibodies but its fat and protein composition is very variable. Colostrum is very digestible, and both colostral energy and nitrogen (N) are retained with a very high efficiency. Colostrum production by the sow assessed from the weight gain of the litter from birth to 24 h of age is very variable (from 1900 to 5300 g). There is no clear effect of litter size or parity, suggesting that colostrum production is a characteristic of the sow. Within a litter, colostrum consumption by the individual piglets varies considerably. It is independent of birth order, but related positively to birth weight and negatively to litter size. Other factors influencing colostrum consumption, including cold stress, premature birth and birth hypoxia, are discussed. Because of the epitheliochorial nature of the porcine placenta, the new-born piglet must acquire maternal immunoglobulin G (IgG) from ingested colostrum for passive immune protection until the immune system of the piglet becomes fully developed. Colostrum IgG concentrations in milk vary widely between individual sows both in initial concentration and in the rate at which concentrations decline during the first 24 h of life. The piglet can only absorb intact IgG prior to gut closure, which occurs in the first 24 h of life and is induced by intakes of colostrum which are insufficient to maintain piglet live-weight. As a result, the amounts of intact IgG absorbed by the piglet vary widely. The effects of colostrum consumption on neonatal survival are discussed. Consumption of colostrum in amounts sufficient to meet the energy requirement of the piglet is a major determinant for survival. Since most neonatal losses occur in the first 2 days of life, before acquisition of a maternal IgG for immune protection becomes important for survival, piglet serum IgG concentration does not correlate well with early survival but is important in later resistance to disease challenge. It is concluded that colostrum production is a good marker for the maternal quality of the sow. Future research should focus on the ability of the sow to produce more colostrum and on the possible delayed effects of passive immunisation on the health and performance of piglet at weaning and later in life.

/pdf/nutritional-and-immunological-importance-of-colostrum-for-1es6e1erac.pdf

Nutritional and immunological importance of colostrum for the new-born pig

Over the last 50 yr, the study of intesti- nal peptide transport has rapidly evolved into a field with exciting nutritional and biomedical applications. In this review, we describe from a historical and cur- rent perspective intestinal peptide transport, the im- portance of peptides to whole-body nutrition, and the cloning and characterization of the intestinal peptide transporter, PepT1. We focus on the nutritional signifi- cance of peptide transport and relate these findings to livestock and poultry. Amino acids are transported into the enterocyte as free AA by a variety of AA transport- ers that vary in substrate specificity or as di- and trip- eptides by the peptide transporter, PepT1. Expression of PepT1 is largely restricted to the small intestine in most species; however, in ruminants, peptide transport and activity is observed in the rumen and omasum. The extent to which peptides are absorbed and utilized is still unclear. In ruminants, peptides make a contri- bution to the portal-drained visceral flux of total AA and are detected in circulating plasma. Peptides can be utilized by the mammary gland for milk protein synthesis and by a variety of other tissues. We discuss the factors known to regulate expression of PepT1 in- cluding development, diet, hormones, diurnal rhythm, and disease. Expression of PepT1 is detected during embryological stages in both birds and mammals and increases with age, a strategic event that allows for the immediate uptake of nutrients after hatch or birth. Both increasing levels of protein in the diet and dietary protein deficiencies are found to upregulate the peptide transporter. We also include in this review a discus- sion of the use of dietary peptides and potential alter- nate routes of nutrient delivery to the cell. Our goal is to impart to the reader the nutritional implications of peptide transport and dietary peptides and share dis- coveries that shed light on various biological processes, including rapid establishment of intestinal function in early neonates and maintenance of intestinal function during fasting, starvation, and disease states.

Board-invited review: Peptide absorption and utilization: Implications for animal nutrition and health.

In vitro brush-border transport of three monosaccharides by pig intestine was studied as a function of postnatal age from immediately after birth before suckling to after weaning. Rates of transport normalized to tissue weight or surface area for glucose (Glc), galactose (Gal), and fructose (Fru) were highest at birth, with a steep decline after the onset of suckling, probably caused by any combination of three or more factors: reduced transporter site density, shifts in relative abundances of different monosaccharide transporters, and/or changes in activities of individual transporters. Whereas highest rates of Glc and Fru transport shifted from proximal to midintestine after weaning, Gal transport remained highest in proximal intestine. Postnatal increases in Km values for Gal, but not Glc, indicate there are multiple aldohexose transporters that undergo separate developmental trajectories. The presence of Fru transport in neonatal pigs may reflect a more advanced state of development than neonatal rats and rabbits, or may be an adaptation for early weaning. Changes in Fru-to-Glc and Gal-to-Glc transport ratios before weaning suggest transporter development is partly genetically hard-wired, apparently to prepare pigs for weaning. Curiously, Fru-to-Glc transport ratios were lower than those of rat and rabbit, but closely paralleled those of the carnivorous cat.

Postnatal development of monosaccharide transport in pig intestine

Omnivorous mammals are able to adaptively modulate rates of intestinal nutrient transport to match changes in diet. Because adaptive responses during suckling, when dietary composition is relatively constant, have not been adequately determined, we measured in vitro sugar and amino acid uptake [nmol/(mg tissue.min)] in suckling pigs fed milk replacers with either lactose (LAC) or a 60:40 mixture of maltodextrin and sucrose (MDS). The MDS-fed pigs initially grew slower, but had intestinal dimensions similar to those of LAC-fed siblings when normalized to body weight. Carrier-mediated uptake for three monosaccharides (glucose, galactose, fructose) did not differ between LAC- and MDS-fed pigs at 5, 10, 15 and 20 d of age. Interdiet differences in rates of leucine and proline uptake, despite identical types and concentration of protein in both milk replacers, are indicative of non-specific responses to diet during suckling. Uptake capacities (grams of monosaccharide absorbed per 24 h) never exceeded estimates of monosaccharide intake by more than fourfold and were less than aldohexose intake during early suckling. Our results indicate 1) age-related changes in rates of nutrient uptake are genetically programmed and little influenced by diet; 2) any responses to diet are nonspecific and likely involve a shift in the timing of the genetic program; and 3) at birth and throughout suckling, pigs are capable of absorbing limited quantities of alternative nutrients.

Anna A. Puchal

Papers

Postnatal development of monosaccharide transport in pig intestine

Intestinal Amino Aicd and Monosaccharide Transport in Suckling Pigs Fed Milk Replacers with Different Sources of Carbohydrate

Hydrolysis and absorption of two monophosphate derivatives of ascorbic acid by channel catfish Ictalurus punctatus intestine

Transport of l-proline by chicken cecum during development