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The Journal of Nutrition Vol. 128 No. 6 June 1998,
pp. 947-953
Department of Large Animal Medicine and Nutrition, Utrecht University, 3508 TD Utrecht, the Netherlands and * Institute for Animal Science and Health, 8219 PH Lelystad, the Netherlands
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ABSTRACT |
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Abstract
Introduction
Methods
Results
Discussion
References
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Effects of weaning pigs to different diets have been investigated in terms of the changes in the small intestinal morphology, and in the absorption of short-chain fatty acids (SCFA) and sodium from the large intestine. One piglet from each of six litters containing nine pigs was sampled on the day of weaning; the other eight piglets were divided into four equal groups and fed different diets as follows: unweaned, weanling diet, or sow's milk at high or low level. Four and seven days after weaning, measurements of the intestinal tissue and contents were made; the plasma concentrations of SCFA, aldosterone and sodium were also measured. The villous height in the small intestine was highest in the unweaned group and greater in the high milk group than in either the weanling diet or low milk group (P < 0.001). Apparently, villous atrophy was due more to the level of feed intake than to the composition of the diet. The concentrations of SCFA in the large intestine and portal blood were highest in the weanling diet group and lowest in the low milk group. The low milk group tended to have higher blood concentrations of aldosterone (P = 0.15), which may have compensated for the low concentrations of SCFA in maintaining a higher percentage of dry matter in the intestine. Pigs fed weanling diet may use the energy from the SCFA to maintain a body weight comparable to that of pigs fed milk at a low level.
KEY WORDS: pigs · intestinal morphology · short-chain fatty acids · weaning
When pigs are weaned, they are subjected to many stresses, including being separated from the sow, being moved, and changing from a diet of milk to a solid diet. These stresses may contribute to the poor growth rate of pigs after weaning, either directly, or by inducing villous atrophy, which is observed in the small intestine (SI)3 after weaning and leads to postweaning maldigestion and malabsorption (Hampson and Kidder 1986 The influence of the composition of the diet and its physical state has been investigated by Hall and Byrne (1989) Whether the maldigestion and malabsorption due to the villous atrophy in the SI lead to diarrhea depends, on the amount of fluid entering the large intestine (LI) and on the capacity of the LI to compensate for the loss of fluid from the SI by enhanced absorption. It has been suggested that the absorption of electrolytes, (particularly of sodium) and water by the LI are facilitated by the action of short-chain fatty acids (SCFA) (Argenzio and Whipp 1979 We concluded from the results of a previous study (van Beers-Schreurs, H.M.G., Nabuurs, M. J. A., Vellenga, L., Wensing, T. and Breukink, H. J., unpublished data) that, although weaning was certainly associated with villous atrophy in the SI, it was uncertain whether the change was caused by separating the pigs from the sow or by the changes in the quantity and/or composition of the diet.
The aim of this study was to try to resolve this question by comparing unweaned pigs with pigs that were weaned either to a commercial weanling diet or to a diet of sow's milk fed at either a high or a low level. For this purpose, studies were made of the morphology of the SI of the different groups and of the concentrations of SCFA in the contents of the LI, in the blood of the cranial vena cava and in the portal blood. In the blood of the cranial vena cava, the concentration of aldosterone was measured because of its effect on the absorption in the LI. The function of the LI in absorbing water was studied in terms of the percentage of dry matter of its contents.
Animals.
Six litters of nine pigs were obtained from a conventional herd (Dutch Landrace × Yorkshire) of the Utrecht University. At 28 d of age, one piglet of each litter was sampled and killed, and the remaining eight pigs in each litter were randomly divided into four equal groups. The first unweaned group remained with the sow (UW); they were not offered any weanling diet but had access to feed spilled by the sow. A second group was given free access to a diet of sow's milk (SMH), the third group was weaned to the same source of sow's milk fed at a low level (SML), and the last group was weaned to a commercial weanling diet (WD).
Diets.
The volume of milk offered to the pigs in the SMH group was calculated to provide the dietary energy intake (DEintake) of weaned pigs as follows (NRC 1988): DEintake (kJ/d) = (455.5 BW
Experimental procedure.
The pigs were observed daily for signs of gastrointestinal, neurological, respiratory or locomotory disorders. On the day of weaning, one piglet was selected from each litter; 4 and 7 d later, one of the two pigs in each group was selected, weighed, premedicated with 0.5 mL stresnil/10 kg BW (Janssen Pharmaceutica, Beerse, Belgium) and anesthetised with halothane, oxygen and nitrous oxide administered through a face mask. A blood sample was taken from the cranial vena cava; after an incision had been made in the abdomen, a sample was taken from the portal vein. Blood (5 mL) was collected into a tube containing 0.05 mL heparin and 0.02 mL 1 mol/L NaOH, and 5 mL was collected into a tube containing only heparin. Samples of intestinal tissue for histological examination were removed from sites ~10, 25, 50, 75 and 95% along the small intestine. Samples of intestinal contents were taken into small weighed pots from the cecum, the centripetal gyri, the central flexure and the centrifugal gyri of the ascending colon. A part of these samples was used to measure the percentage of dry matter; the remainder was stored in 1 mol/L sodium hydroxide at Sample handling. Histological examination.
The tissues were pinned to a piece of cork, fixed in 10% buffered formalin solution, embedded in paraffin, sectioned and stained with hematoxylin and eosin as described by Nabuurs et al. (1993) Determination of the concentrations of SCFA.
The concentrations of SCFA in the samples of the contents of the LI, in the blood of the cranial vena cava and in the portal blood were measured by gas chromatography (Packard 430, Chrompack Nederland bv, Bergen op Zoom, the Netherlands) with a 2.7-m glass column packed with 17% neopentyl glycol adipate and 1% H3PO4 on Chromosorb WAW of 80/100 mesh; column temperature was 150°C, detector 200°C and injector 200°C; the carrier gas was nitrogen at a flow rate of 25 mL/min. The samples were centrifuged at 1000 × g for 10 min, and an equal volume of 1 mol/L NaOH was added to each sample of small intestinal contents or plasma. Pivalic acid (5 µL) was added to 50 µL of the mixture as an internal standard. Pivalic acid was added in a concentration comparable to the concentration expected for acetate, propionate and butyrate. After mixing and centrifuging, the sample was injected into the chromatograph. The mean concentrations of acetate, propionate and butyrate in the LI were obtained by averaging the concentrations measured at the four sites sampled. As mentioned for the villous height and crypt depth data, the great similarity in results at various sites made is possible to show averaged data only.
Percentage of dry matter.
The percentage of dry matter of the intestinal contents was determined by overnight drying in an oven at 101°C. The percentage was measured in each sample of the contents of the LI, and the mean values were obtained by averaging the measurements at the four sites along the LI.
Aldosterone and sodium.
The concentration of aldosterone in plasma was measured with a solid-phase 125I RIA designed for quantitative measurements in unextracted plasma (Diagnostic Products Corporation, Los Angeles, CA). The concentration of sodium was measured with the Synchron 5 (Beckman Instruments, Diagnostic Systems Group, Brea, CA).
Microbiological examination.
Samples of feces were taken 1, 3, 5 and 7 d after weaning and inoculated onto 5% sheep-blood agar plates for the detection of strains of Escherichia coli. The plates were cultured at 37°C for 20 h and any E. coli detected were typed. The samples of feces were tested for the presence of rotavirus by a modified ELISA (Ellens and de Leeuw 1977 Statistical analysis.
ANOVA was applied [Release 3.1, Genstat 5 (1994)] to each variable for each site at which it was measured (SCFA in cranial vena cava or portal blood) or for the average measurement over these sites (villous height SI, crypt depth SI, SCFA LI). The litters were considered as random blocks; group (UW, WD, SMH or SML), days after weaning and their interactions were taken as factors. Standard checks were applied to the assumptions of normality and homogeneity of variances. Fisher's t test was used as post-hoc test.
During the experiment, some of the weaned pigs excreted pasty feces, but none of the pigs were treated for any disease. On the day of weaning, the weight of the pigs was 8.23 ± 0.14 kg. At the end of the experiment, 7 d later, the six remaining unweaned pigs (UW) weighed 11.0 ± 0.35 kg, the six SMH pigs weighed 11.1 ± 0.49 kg, the six pigs in the WD group weighed 8.79 ± 0.16 kg and the six SML pigs weighed 8.46 ± 0.25 kg. The UW and SMH pigs weighed more than the WD- and SML-fed pigs (P < 0.05).
Intestinal morphology.
In spite of receiving large amounts of sow's milk, the SMH pigs had shorter villi 4 d after weaning and deeper crypts 7 d after weaning than the unweaned (UW) pigs (P < 0.05) (Fig. 1A, B). In the small intestines of the weaned pigs, the villi were significantly shorter in the WD and SML pigs than in the SMH pigs at d 4 and 7 (P < 0.001), and the crypts were significantly deeper in the WD pigs than in the SML pigs at d 4 (P < 0.05) (Fig. 1A, B).
Short-chain fatty acids.
Four days after weaning, the mean concentration of propionate in the LI of the SMH pigs was higher than in the UW pigs (P < 0.05); 7 d after weaning, the mean concentration of acetate was lower in the SMH pigs than in the UW pigs (P < 0.01) (Fig. 2). There were several differences among the mean concentrations of SCFA in the groups of weaned pigs (Fig. 2). The concentration of acetate was higher in the WD pigs than in either of the groups receiving sow's milk (P < 0.01), although the difference between the WD and SMH group was not significant after 4 d. After 4 d, the concentration of propionate was significantly higher in the SMH and WD pigs than in the SML pigs (P < 0.01), and it was also higher in the WD group than in the SMH group (P < 0.01) and the SML group (P < 0.001) after 7 d. After 4 d, the mean concentration of butyrate was higher in the SMH and WD pigs than in the SML pigs (P < 0.001 and P < 0.05, respectively); after 7 d, its concentration in the WD group was higher (P < 0.001) than in either the SMH or SML group (Fig. 2).
Dry matter of intestinal contents.
The percentages of dry matter of the large intestinal contents of the WD and SML groups were lower than that of the SMH group, but the differences were significant only 4 d after weaning (P < 0.05) (Fig. 4).
Weight of intestinal contents and tissue.
Both 4 and 7 d after weaning, the weight of the intestinal contents of the WD pigs was two or more times that of the other groups of pigs, and on both occasions, the contents of the LI of the SMH group weighed approximately twice as much as the contents of the LI of the SML group (Fig. 5A). The intestinal tissue of the WD and SMH groups weighed significantly more than that of the SML group (P < 0.002) except 4 d after weaning, when the difference between the SMH group and the UW group was not significant (Fig. 5B).
Aldosterone and sodium.
The concentration of aldosterone varied from 215.8 ± 50.94 µg/L at d 7 in the SMH-fed pigs to 399.50 ± 67.81 µg/L at d 4 in the pigs of the SML-fed group. The concentration of aldosterone was slightly, but not significantly, higher in the blood of the cranial vena cava of the SML pigs than in the WD pigs 4 d after weaning (P = 0.15).
Microbiology.
Strains of E. coli of OK types O138K81 and O138K82K88 negative were detected in the feces of pigs in all of the groups. However, <20% of the WD pigs and none of the SML pigs excreted E. coli 3 d after weaning and no pigs of either group excreted them subsequently.
The adverse stressful effects of weaning may be due to psychological, environmental or nutritional factors (Funderburke and Seerley 1990
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
, Kenworthy 1976, Nabuurs et al. 1993). Villous atrophy in the SI has been investigated largely from the nutritional (Hampson and Smith 1986), infectious (Lecce et al. 1982) and hormonal (Fabiansson 1986) standpoints, and it is not known whether the stresses of weaning contribute to the condition.
, Deprez et al. (1987) and Cera et al. (1988), and it has been concluded that feeding a dry pelleted meal after weaning leads to a decrease in the height of the villi. Leibbrandt et al. (1975) and Seve (1982) measured the food intake of pigs shortly after weaning and concluded that their intake of energy was insufficient for maintenance. Kelly et al. (1984) and McCracken and Kelly (1984) were the first to recognize that inadequate food intake immediately after weaning may also contribute to the changes in intestinal morphology.
, Roediger and Moore 1981) and aldosterone (Bywater 1983, Edmonds and Marriot 1967, Hirsch et al. 1985), and that these compounds may help to increase the percentage of dry matter in the contents of the LI.
MATERIALS AND METHODS
Abstract
Introduction
Methods
Results
Discussion
References
9.46 BW2 1531) × 4.184, where BW is the body weight (kg). The milk was obtained manually from sows from the same herd from which the pigs were obtained and from a conventional herd with the same strains of pigs. The sows had been injected intramuscularly with oxytocin to stimulate the let-down of the milk. Milk was collected into 500-mL plastic jars and stored at 20°C. To avoid differences in the composition of the milk obtained several days after parturition, the milk was pooled. Twenty-four hours before an experiment began, the milk supply for 1 d was placed in a refrigerator, thawed and mixed. One hour before each feeding time, the amount of milk required was gently warmed to ~35°C; the pigs were fed with milk every 4 h day and night and received no supplementary food. The composition of the sow's milk (mean ± SEM) was 50.4 ± 1.5 g protein, 80.3 ± 3.5 g fat and 47.3 ± 1.3 g lactose per kg milk. The gross energy content of the milk was 5.36 ± 0.26 kJ/g. The pigs of the SML group were fed sow's milk to provide an energy intake corresponding to the energy intake of the pigs in the WD group; water was available to them after they had finished the milk feed. The two littermates assigned to the same diet group were housed together. The pigs stimulated each other in drinking the milk from a trough. From the beginning, they drank the milk immediately after it was offered; there were no refusals in either the SMH or the SML pigs. The amount of weanling diet offered to the WD group was sufficient to correspond to the intake of metabolizable energy for weaned pigs as described by Le Dividich and Herpin (1994). The diet composition is provided in Table 1. The daily food intake of the weaned pigs of the WD group was measured by subtracting the weight of refusals from the amount of diet offered. The mean daily intake of metabolizable energy of the SMH fed pigs varied from 1324 ± 30 kJ/BW0.75 at d 1 to 1477 ± 42 kJ/BW0.75 at d 6. The mean daily intake of metabolizable energy of the WD- and SML-fed pigs varied from 203 ± 32 kJ/BW0.75 at d 1 to 770 ± 37 kJ/BW0.75 at d 6. There were no significant differences between the mean daily intake of metabolizable energy of the WD- and SML-fed pigs.
View this table:
Table 1.
Composition of the diet fed to the weanling diet group
20°C for analysis of SCFA. The cecum and colon were then removed from the abdomen and weighed; they were then washed free of intestinal contents and weighed again.
. The height of the villi and the depth of the crypts were measured with a microscope with an ocular micrometer. For each region, 10 fields were examined and averaged. Because of the similarity in the data of villous height between sites and of crypt depth between sites and to reduce the amount of data, mean values were determined by averaging the measurements at the five sites along the small intestine.
).
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
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Fig 1.
Villous height (panel A) and crypt depth (panel B) in the small intestines of unweaned pigs (UW), weaned pigs offered a high sow's milk diet (SMH), a weanling diet (WD) or a low sow's milk diet (SML) at weaning and d 4 and 7 after weaning. Values are means ± SEM, n = 6. Bars with the same letter differ, P < 0.05.
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Fig 2.
Concentrations of acetate, propionate and butyrate in the large intestines of unweaned pigs (UW), weaned pigs offered a high sow's milk diet (SMH), a weanling diet (WD) or a low sow's milk diet (SML) at weaning and at d 4 and 7 after weaning. Values are means ± SEM, n = 6. Within a diagram, bars with the same letter differ, P < 0.05.
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Fig 3.
Concentrations of acetate, propionate and butyrate in the portal blood of unweaned pigs (UW), weaned pigs offered a high sow's milk diet (SMH), a weanling diet (WD) or a low sow's milk diet (SML) at weaning, and at d 4 and 7 after weaning. Values are means ± SEM, n = 6. Within a diagram, bars with the same letter differ, P < 0.05.
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Fig 4.
Percentage of dry matter in the large intestines of unweaned pigs (UW), pigs offered a high sow's milk diet (SMH), a weanling (WD) or a low sow's milk diet (SML) at weaning and at d 4 and 7 after weaning. Values are means ± SEM, n = 6. Bars with the same letter differ, P < 0.05.
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Fig 5.
Weight of the contents (panel A) and of the tissue (panel B) of the cecum and colon of unweaned pigs (UW), pigs offered a high sow's milk diet (SMH), a weanling (WD) or a low sow's milk diet (SML) at weaning, and at d 4 and 7 after weaning. Values are means ± SEM, n = 6. Bars with the same letter differ, P < 0.05.
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Fig 6.
Concentrations of sodium in the blood of the cranial vena cava of unweaned pigs (UW), weaned pigs offered a high sow's milk diet (SMH), a weanling diet (WD) or a low sow's milk diet (SML) at weaning, and at d 4 and 7 after weaning. Values are means ± SEM, n = 6. Bars with the same letter differ, P < 0.05.
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Fig 7.
Percentage of pigs excreting rotaviruses and Escherichia coli in the feces of unweaned pigs (UW), weaned pigs offered a high sow's milk diet (SMH), a weanling diet (WD) or a low sow's milk diet (SML) at d 1, 3, 5 and 7 after weaning. Values are means of percentages ± SEM, n = 12 at d 1 and 3 and n = 6 at d 5 and 7, because half of the group had been killed at d 4. *Percentage of pigs excreting rotaviruses was higher in the WD and SML group than in the UW and SMH group at d 5.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
), and it is difficult to unravel the contributions made by these factors. There is an obvious nutritional stress when the pigs' diet of sow's milk is abruptly changed to a solid diet. An attempt was made to eliminate this nutritional stress at weaning by feeding the SMH group of pigs a high level of sow's milk, offered at frequent regular intervals during the day and night. The fact that these pigs had shorter villi in their small intestine than the unweaned pigs 4 d after weaning, and deeper crypts after 7 d, suggests that these changes may have been due to psychological or environmental stresses rather than a nutritional stress, although the difference between receiving milk from a trough or directly from the sow could have influenced our results. Furthermore, the immunologic composition of the pooled milk could have differed from sow's milk. The stress may have been caused by separating the pigs from the sow and transferring them to the pen for weaned pigs.
, Hall and Parsons 1989). In our experiment, it is unlikely that they were responsible in this case because there was no difference between the patterns of excretion of rotaviruses by the unweaned pigs and the pigs of the SMH group. Similarly, the larger differences in villous height between the UW and SMH pigs and the WD and SML pigs 4 d after weaning cannot be explained by the presence of rotaviruses because similar proportions of the pigs in the two pairs of groups were excreting rotaviruses 3 d after weaning. However, the differences observed after 7 d may be related to rotaviruses because more of the pigs in group SML than group SMH were excreting rotaviruses 5 d after weaning. The antibodies against rotaviruses, excreted with milk, could have helped to prevent the multiplying of the rotaviruses in the pigs of the SMH group and in the unweaned pigs.
, Nabuurs et al. 1993). Pluske (1993) suggested that feeding a starter diet after weaning may be a stimulus for this increase in the depth of the crypts. However, in this study, there was an increase in the depth of the crypts in the weaned pigs that were fed only sow's milk, suggesting that the separation of the pigs from the sow and their transfer to other pens were factors that contributed to the changes in their intestinal morphology after weaning. Pluske et al. (1996) observed that 5 d after weaning, pigs weaned to a restricted milk diet had shorter villi and shallower crypts than pigs weaned to a milk diet consumed ad libitum. The shorter villi in the pigs of the SML group compared with the SMH group are in accordance with this observation and may have been due to a lack of nutrients in the lumen of the SI, as has been suggested by Goodlad and Wright (1984) and Koga and Kimura (1978). However, although the SML pigs had shallower crypts than the SMH pigs, the difference was not significant. It is concluded that the height of the villi in the SI of the weaned pigs was influenced principally by the level of feed intake. Pluske (1993) also found that pigs fed a weanling diet had shorter villi and deeper crypts 5 d after weaning than pigs fed a diet of ewe's milk to provide the same intake of energy. In contrast, there were no significant differences between the height of the villi in the weaned pigs (WD) and the SML pigs either 4 or 7 d after weaning. The height of the villi was apparently influenced more by the level of feed intake than by the composition of the diet. The observation that the deepening of the crypts was more severe in the WD pigs than in the SML pigs is in agreement with the results of Pluske (1996).
) and may also be affected by malabsorption in the SI associated with villous atrophy (Bergman 1990). In spite of the two groups receiving essentially the same diet, the concentration of propionate in the LI of the SMH group was higher 4 d after weaning than that in the UW pigs at the expense of the concentration of acetate. It is proposed that the shift in molar proportions was due to the malabsorption associated with the villous atrophy in the SMH pigs 4 d after weaning.
) was not observed in our experiment. We doubt if there is any effect on intestinal morphology when pigs had free access to sow's milk at the same time, and if there was such an effect, it could have resulted in deeper crypts in the unweaned pigs after d 7 because the intake of spilled feed may have contributed to higher acetate concentrations at d 7 and not at d 4.
). The higher concentrations of acetate, propionate and butyrate observed in the LI of the WD pigs than in the SML pigs is in agreement with this observation, and the higher concentrations in the LI were accompanied by higher concentrations in the portal blood of the WD pigs.
, Ruppin et al. 1980). As a result, it might have been expected that the higher concentration of SCFA in the LI of the WD pigs would have resulted in a higher percentage of dry matter in their LI than in the LI of the SML pigs 4 d after weaning, but this was not the case. However, aldosterone also stimulates the absorption of sodium and water from the colon (Edmonds and Marriot 1967, Levitan and Ingelfinger 1965). The SML pigs had a (not significantly) higher concentration of aldosterone in their blood 4 d after weaning than the WD pigs, and this may have helped to increase the dry matter percentage in the contents of their LI.
). In accordance with this information, the pigs in the WD group not only had the highest concentrations of SCFA in their LI and portal blood but also had the highest concentration of sodium in the blood of the cranial vena cava both 4 and 7 d after weaning.
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FOOTNOTES |
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Manuscript received 7 August 1997. Initial reviews completed 29 August 1997. Revision accepted 9 February 1998.
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LITERATURE CITED |
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Abstract
Introduction
Methods
Results
Discussion
References
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social pressures at regrouping. In: Proceedings 9th International Pig Veterinary Society Congress, p. 473. 15-18 July, Barcelona, Spain (abs.).This article has been cited by other articles:
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