J. G. M. Houdijk

Nutrient partitioning between reproductive and immune functions in animals.

The physiological processes that underlie the reproductive cycle impose considerable metabolisable protein (MP) demands on a female, especially during the periparturient period. When MP supply falls short of MP demand (i.e. MP becomes scarce), certain, if not all, bodily functions are expected to be penalised. It has been proposed that partitioning of scarce MP is prioritised to reproductive rather than to immune functions. In other words, at times of MP scarcity, the penalty on expression of immunity would be expected to be greater than that on reproduction. This hypothesis forms a nutritional basis for the occurrence of periparturient breakdown of immunity to parasites (BIP), which can be observed in many host-parasite systems. In the present review we explore this nutritional basis, using periparturient sheep infected with the abomasal nematode Teladorsagia circumcincta as an example, and attempt to quantify its occurrence. Evidence supporting the nutritional basis of periparturient BIP is reviewed, covering experiments in which nutrient supply (from both exogenous and endogenous sources) and/or nutrient demand were manipulated. Quantitatively, MP requirements for expression of immunity to T. circumcincta were estimated to be about 1 g/kg metabolic body weight (body weight 0.75) per d, approximately 5% of the maximum MP requirements of periparturient sheep. The major component of this requirement was assumed to be for replenishing irreversible plasma protein losses into the gastrointestinal tract. Although confirmation of this estimate is required, such estimates may be used to improve the known MP requirements of periparturient animals, enabling the extent and the consequences of periparturient BIP to be minimised.

Can an increased intake of metabolizable protein affect the periparturient relaxation in immunity against teladorsagia circumcincta in sheep

Within the overall hypothesis that the periparturient relaxation of immunity (PPRI) to gastrointestinal parasites has a nutritional basis, we studied whether an increased intake of metabolizable protein (MP) could affect the expression of immunity to Teladorsagia (Ostertagia) circumcincta of twin-bearing and -rearing Greyface ewes. Two sets of iso-energetic diets were formulated to provide either 85% (L-) or 130% (H-) of the MP requirements during the last 6 weeks of pregnancy (-P) and the first 6 weeks of lactation (-L). Thirty ewes were allocated to LP or HP. Six ewes of each group were slaughtered after lambing (S(0)); the remaining 24 ewes of each group were allocated to either LL or HL, thus creating four treatment combinations during lactation (LP/LL, LP/HL, HP/LL and HP/HL; n=12). Six ewes of each treatment combination were slaughtered at Week 3 (S(3)) or at Week 6 (S(6)) in lactation. The HP ewes were heavier at lambing, produced heavier lambs, had lower faecal egg counts (FECs), a lower concentration of plasma pepsinogen, a higher concentration of plasma albumin during late pregnancy and more abomasal globule leukocytes (GLs) but similar worm burdens at S(0) compared to the LP ewes. The LP/HL and HP/HL ewes had a higher calculated milk production than the LP/LL and HP/LL ewes. FECs increased for each treatment combination during the first 3 weeks of lactation. This increase concurred with fewer abomasal GLs at S(3) compared to S(0). The LP/HL and HP/HL ewes had a higher proportion of immature worms and more abomasal GLs than the LP/LL and HP/LL ewes at S(6). The FECs continued to increase during the second 3 weeks of lactation for the LP/LL ewes only, which concurred with an elevated plasma pepsinogen concentration and an absence of abomasal GLs at S(6). The plasma pepsinogen concentration decreased rapidly for the LP/HL ewes during lactation. We conclude that an increased intake of MP could enhance the expression of immunity to T. circumcincta of twin-bearing and -rearing Greyface ewes.

Is the allocation of metabolisable protein prioritised to milk production rather than to immune functions in Teladorsagia circumcincta-infected lactating ewes?

It has been suggested that the periparturient breakdown of immunity to parasites has a nutritional basis. Our overall hypothesis is that it results from a prioritised scarce nutrient allocation to reproductive functions (e.g. milk production) rather than to immune functions. We tested this hypothesis by offering five levels of dietary metabolisable protein, ranging from 0.65 to 1.25 times their assumed requirements, for 4 weeks post-parturition to twin-rearing Greyface ewes, experimentally infected with Teladorsagia circumcincta. We hypothesised that the initial increments of metabolisable protein supply would increase milk production without affecting the degree of breakdown of immunity whilst later increments would reduce the degree of breakdown of immunity. The first two increments of metabolisable protein supply indeed increased milk production and did not affect final worm burdens, but in contrast to the expectation, reduced faecal egg counts and total egg output. The last two increments of metabolisable protein supply did not further affect milk production and egg output, but resulted in reduced final worm burdens. Metabolisable protein supply did not affect plasma IgG and IgE antibody against somatic L(3) antigen but the first three increments reduced plasma pepsinogen and plasma IgA antibody. The last increment did not further reduce plasma pepsinogen but increased plasma IgA. Metabolisable protein supply did not systematically affect abomasal mucosal mast cell, globule leukocyte and eosinophil counts. Our results support the view that the priority of scarce metabolisable protein allocation to milk production over immune functions may be gradual rather than absolute. The contrast between effects of metabolisable protein supply on faecal egg count and final worm burden points towards the possibility that if different effector responses regulate fecundity and worm expulsion, then they would differ in their sensitivity towards changes in the degree of nutrient scarcity.

Effects of dietary protein supply, weaning age and experimental enterotoxigenic Escherichia coli infection on newly weaned pigs: performance

An experiment was conducted to investigate the effects of post-weaning dietary protein supply and weaning age on the performance of pigs in the absence of in-feed antimicrobial growth promoters (AGP) when artificially challenged with enterotoxigenic Escherichia coli (ETEC), a pathogen associated with post-weaning colibacillosis (PWC). The experiment consisted of a complete 2 × 2 × 2 factorial combination of two weaning ages (4 v. 6 week), two levels of dietary protein (H, 230 g CP/kg v. L, 130 g CP/kg) and challenge with ETEC (+ v. -). An additional four treatments were added to test for the effects of protein source (DSMP, dried skimmed milk powder v. SOYA, soybean meal) and AGP inclusion (yes v. no) on challenged pigs of both weaning ages. At weaning (day 0), pigs were assigned to one of the experimental treatments for 2 weeks. On day 14 post-weaning, the same standard grower ration was fed to all animals until 10 weeks of age. On day 3 post weaning, challenged pigs were administered per os with 109 cfu ETEC. The ETEC challenge had a detrimental short-term effect on performance, decreasing average daily gain (ADG) (days 3 to 6; P = 0.014) in both 4- and 6-week weaned animals. Compared with their non-infected counterparts, challenged 4-week weaned pigs on the H diet demonstrated a larger decrease in ADG immediately post infection than those on the L diet, -42% and -25%, respectively (P = 0.088). This effect was smaller in the 6-week weaned pigs, -26% and -19% for the H and L diets, respectively. Pigs fed SOYA had lower (P < 0.001) daily intake and ADG (day 0 to 14) than those fed DSMP, with 6-week weaned pigs being affected to a greater extent than 4-week weaned pigs. In the absence of AGP, increasing weaning age and decreasing dietary protein level, especially in earlier weaned pigs, may help to minimise the effects of PWC on performance, particularly in sub-optimal environments.

The expression of immunity to Teladorsagia circumcincta in ewes and its relationship to protein nutrition depend on body protein reserves

We hypothesized that expression of immunity to gastrointestinal nematodes and its relationship with dietary metabolizable protein (MP) supply in ewes depended on body protein--but not on body fat reserves. Twin-bearing ewes were trickle infected with Teladorsagia circumcincta. Three mid-pregnancy feeding treatments were used, calculated to maintain body reserves (HH), maintain body protein- and lose body fat reserves (HL), or lose body reserves (LL), and followed by 2 isoenergetic, periparturient feeding treatments, calculated to provide either scarce (LP) or adequate (HP) amounts of MP. At the end of the mid-pregnancy feeding treatment, HL- and LL-ewes had a smaller backfat depth (approximately body fat reserves) than HH-ewes, and LL-ewes had a smaller muscle depth (approximately body protein reserves) and higher faecal egg counts (FEC) than HH- and HL-ewes. Overall, LL-ewes had higher periparturient FEC than HH- and HL-ewes, and LP-ewes had higher periparturient FEC than HP-ewes. However, LL-ewes offered the LP feed had higher periparturient FEC than ewes on any of the other combinations of feeding treatments. Feeding treatments affected plasma pepsinogen but not plasma IgA. The results support the view that body protein- but not body fat reserves may overcome consequences of dietary MP scarcity on periparturient breakdown of immunity to gastrointestinal nematodes.

The consequences of non-starch polysaccharide solubility and inclusion level on the health and performance of weaned pigs challenged with enterotoxigenic Escherichia coli

The inclusion of insoluble NSP (iNSP) in weaner pig diets has been reported to decrease post-weaning colibacillosis (PWC). Conversely, soluble NSP (sNSP) have been shown to exacerbate PWC. The present study investigated the effect of NSP solubility and inclusion level on the health and performance of newly weaned pigs challenged with enterotoxigenic Escherichia coli (ETEC), using NSP sources known not to affect digesta viscosity, in a 2 x 2 x 2 factorial combination of NSP solubility (iNSP v. sNSP), inclusion level (low (L; 50 g/kg) v. high (H; 150 g/kg)) and ETEC challenge (infected v. sham). Infection had no effect on pig health, but reduced performance to a larger extent in pigs on the L diets compared with those on the H diets. The inclusion of sNSP significantly decreased the occurrence of diarrhoea (P < 0.001) and improved gut health, as indicated by a lower caecal digesta pH (P = 0.008) and increased (P = 0.002) Lactobacillus:coliform ratio, when compared with the iNSP diet on day 14 post-weaning. There was no effect of NSP solubility on ETEC shedding, digesta viscosity or pig performance. Pigs on the H diets had fewer cases of diarrhoea and shed fewer ETEC than those on the L diets. Increasing NSP inclusion significantly increased colonic Lactobacillus:coliform ratio, volatile fatty acid concentration and caecal digesta viscosity, but decreased performance. These results suggest that sNSP per se are not detrimental to pig health and that increasing the concentration of NSP in weaner diets that do not increase digesta viscosity may have a beneficial effect on gut health and protect against PWC.

Consequences of protein supplementation for anorexia, expression of immunity and plasma leptin concentrations in parasitized ewes of two breeds.

The periparturient relaxation of immunity (PPRI) against parasites in ewes has a nutritional basis. We investigated whether ewes experience a reduction in food intake (anorexia) during PPRI and if the magnitude of anorexia is affected by host production potential and dietary protein supplementation. We also investigated whether nematode infection is linked to plasma leptin concentrations in periparturient ewes. The experiment was a 2 x 2 x 2 factorial design. Two breeds of twin-bearing/lactating ewes (Greyface cross, G (n 32) and Scottish Blackface, B (n 32)) were used. Half of the ewes were trickle infected with 30,000 larvae of the abomasal parasite Teladorsagia circumcincta per week and the other half were not. During the experiment, all ewes had ad libitum access to a low-protein diet that provided less protein than the recommended allowance. In addition, half of the ewes received a protein supplement that resulted in protein intakes that exceeded recommendations. Nematode infection resulted in a breakdown of immunity to parasites and a reduction in food intake in both breeds. The breeds differed in the extent of PPRI (G ewes having higher faecal egg counts than B ewes), but not in the magnitude of anorexia. Protein supplementation resulted in a reduction in faecal egg counts, but had no effect on the magnitude of anorexia. Plasma leptin concentrations changed significantly over time, but were not affected by protein supplementation or infection. It is concluded that infection with T. circumcincta in periparturient ewes results in anorexia that is not alleviated by protein supplementation and seems unrelated to plasma leptin concentrations.

Manipulating small ruminant parasite epidemiology through the combination of nutritional strategies.

It is increasingly being recognized that non-chemical parasite control strategies may need to be combined to control more effectively gastrointestinal parasitism, result in resilient production systems and reduce reliance on anthelmintics. Here, we consider if and how metabolizable protein (MP) supplementation and anti-parasitic plant secondary metabolites (PSM) may modulate parasite epidemiology through intervention in pasture contamination, development of infection on pasture and larval challenge as target processes. We then propose that combining two or more non-chemical parasite control strategies may have additive effects on host resistance, especially if the individual strategies target different drivers of parasite epidemiology, different processes in the parasite life cycle or different phases of acquired immunity to parasites. This epidemiological framework is used to review recent findings on combining maternal MP supplementation and grazing the PSM-rich bioactive forage chicory as an example of combining nutritional treatments to manipulate parasite epidemiology in a temperate production system. In the absence of available data for combined nutritional strategies in tropical production systems, we make predictions on the consequences of combining such strategies in these systems. We conclude that currently published studies on combining nutritional strategies under temperate conditions show potential to improve additively host resilience and reduce reliance on anthelmintics; however, effects on epidemiology have to date not shown the additive results hypothesized. The framework developed may assist further in evaluating combined (nutritional) strategies to manipulate parasite epidemiology.

Changes in food intake and circulating leptin due to gastrointestinal parasitism in lambs of two breeds.

A reduction in food intake is a prominent feature of many infectious diseases. However, the underlying mechanisms of parasite-induced anorexia in sheep are poorly understood. Here, we tested the hypotheses (a) that the degree of parasite-induced anorexia in lambs is influenced by their growth potential and (b) that nematode infection results in elevated plasma leptin concentration in lambs. The hypotheses were tested with Suffolk x Greyface (S) and Scottish Black-face (B) lambs that are known to differ in their growth potential (S lambs are of greater growth potential than B lambs). During a primary parasite infection, 24 out of 48 lambs per breed were trickle-infected with 7,000 infective Teladorsagia circumcincta larvae per day, 3 d/wk, for a period of 12 wk (experiment I). The lambs were then dewormed, and after a 2-wk interval, half of the 24 lambs per breed that were previously infected were reinfected for another 12 wk with the same parasite and dose as used in the primary infection (experiment II). In both experiments, infected lambs were fed grass pellets for ad libitum intake, whereas noninfected lambs were fed grass pellets for either ad libitum or restricted intakes. The S lambs were more susceptible than B lambs to nematode infection, as judged from the differences in fecal egg counts (P = 0.007). Parasitized lambs of the more susceptible breed (S) showed anorexia [i.e., a decrease in intake of 13% compared with uninfected controls (P = 0.01)], whereas no significant reduction in food intake was observed in lambs of the more resistant breed (B). Reexposure to nematode infection of previously infected animals tended to result in renewed anorexia in S lambs but not in B lambs (P = 0.08) in a similar extent as during primary infection. Plasma leptin concentrations did not differ between ad libitum-fed infected and control lambs but were greater in infected than in noninfected lambs at a similar level of food intake during both the primary (P = 0.02) and the secondary parasitic infection (P = 0.004) in both breeds. The results show that leptin may be involved in the response of lambs to infection but that it is unlikely that leptin alone is responsible for the parasite-induced anorexia in lambs.

Consequences of infection pressure and protein nutrition on periparturient resistance to Teladorsagia circumcincta and performance in ewes.

The consequences of protein nutrition on the degree of periparturient relaxation of immunity to nematode parasites in sheep may be more pronounced at higher levels of infection pressure. Here, we investigated interactive effects of metabolizable protein (MP) nutrition and infection pressure on resistance and lactational performance of ewes. Twin-rearing ewes were trickle infected with either 1000, 5000 or 10,000 infective Teladorsagia circumcincta larvae and fed either at 0.8 (low protein, LP) or 1.3 (high protein, HP) times their estimated MP requirement. Expected interactions between feeding treatment and infection pressure were not observed. Periparturient relaxation of immunity, as indicated by variation in faecal egg counts, was higher in LP ewes than in HP ewes and FEC showed an inverse relationship with infection pressure indicating possible density dependency effects on worm fecundity. Plasma pepsinogen concentration linearly increased with infection pressure. Daily total nematode egg excretion, assessed at week three of lactation, was not significantly affected by infection pressure but was reduced by 65% in HP ewes compared to LP ewes. MP supplementation improved lamb performance but had little effect on ewe body weight and plasma protein concentrations, whilst lactational performance, as judged from lamb performance, tended to be reduced with increased infection pressure. The results suggest periparturient MP supplementation to ewes reduces nematode egg excretion independent of infection pressure and improves lactational performance of parasitized ewes even in the presence of moderate MP scarcity.