The immunobiology of gastrointestinal nematode infections in ruminants

Balic, Adam; Bowles, Vernon M; Meeusen, Elza Nicole Theresia

doi:10.1016/s0065-308x(00)45005-0

Cited by 198 publications

(177 citation statements)

References 163 publications

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“…MMC numbers, as expected (Balic et al, 2000), were lower in unvaccinated sheep and tended to be lower in sheep on the LP diet, especially in the intestine. The actual numbers were comparable with the 30 to 40 cells per 0.2 mm 2 observed by Houdijk et al (2005) in lactating sheep.…”

Section: Discussionsupporting

confidence: 82%

“…The typical pattern of response of the immune armoury under larval challenge has been described by Balic et al (2000). In animals with no previous exposure a nonspecific recruitment in mucosal tissues of eosinophils and production of IgA antibody is followed by increases in MMC and their de-granulated cell remnant, GL (Huntley et al, 1984;Pfeffer et al, 1996).…”

Section: Discussionmentioning

confidence: 97%

“…Subsequently, EOS recruitment to tissue and antibody production diminish, a pattern which has been observed in peripheral EOS numbers (Kimambo et al, 1988) and IgA antibodies (Cripps and Steel, 1978;Henderson and Stear, 2006). Balic et al (2000) interpreted changes in EOS numbers as indicating recruitment to mucosal tissue until the components of the mature protective immune armoury are able to exclude larvae from mucosal tissue. Circulating concentrations of antibodies have been shown to be highly correlated with rates of antibody production (Cripps and Steel, 1978) though the sensitivity of peripheral IgA to small changes in production in mucosal tissue is unclear (Sinski et al, 1995;Henderson and Stear, 2006).…”

Section: Discussionmentioning

confidence: 99%

“…This hypothesis involves an as yet unvalidated assumption that the pattern of involvement of cells of the immune response is identical in the two tissues and Balic et al (2000) cautioned that 'it may well be that present methods for quantifying MMC/GL numbers may not accurately reflect their number or activation status.' The present appears to be the first study in which cells have been measured in the two sites simultaneously and does suggest there may be differences in mechanism or timing of immune responses.…”

Section: Discussionmentioning

confidence: 99%

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The effect of vaccinating infection during pregnancy and dietary protein supply on the peri-parturient immune response of sheep to infection with Teladorsagia circumcincta and Trichostrongylus colubriformis larvae

Sykes

Xie

Stankiewicz

et al. 2007

Animal

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It is well established that dietary protein supply can influence the peri-parturient breakdown of immunity to nematode parasites but there is no information on the importance of exposure to nematode larvae during pregnancy for this response. We investigated this by exposing housed pregnant sheep, scanned as carrying two lambs, to a vaccinating infection with a trickle mixed infection of Teladorsagia circumcincta and Trichostrongylus colubriformis larvae (L3) or to no infection during weeks 29 to 24 relative to parturition. At the beginning of week 23 all sheep were treated with anthelmintic to remove any vaccinating worm burden and from week 22 to week þ6 received a trickle challenge infection with the same nematodes. Within each vaccinating treatment there were two nutritional treatments (no. ¼ 20 per subgroup) designed to provide 1.5 or 1.0 and 1.3 or 0.8 of metabolisable protein (MP) requirement during pregnancy and lactation, respectively. Five ewes were necropsied during weeks þ1 and þ3 to measure worm burdens and mucosal inflammatory cells and the remainder maintained until week þ6. Serum levels of total, IgA and IgE antibodies against L3 antigen of each nematode were measured.Scanning errors and lamb losses resulted in some ewes carrying and/or rearing only one lamb. Numbers of lambs reared was therefore introduced as a treatment effect. Vaccinating infection delayed the peri-parturient rise in faecal egg count (FEC) by an average of 2 weeks but its effect on FEC during the first 6 weeks of lactation was smaller and less persistent than that of dietary MP supply and single-v. twin-suckling.Populations of both nematodes were lower in association with high MP supply, vaccination and single suckling. These changes were associated with increases in numbers of mucosal mast cells (MMC) as a result of both increased MP supply and vaccination. Evidence for a more rapid return of host ability to limit populations of the abdominal nematode T. circumcincta than of the intestinal nematode T. colubriformis was associated with fewer eosinophils and more globule leucocytes (GL) in abomasal than in intestinal tissue.None of the serum antibody isotypes was affected by dietary protein supply. Total and IgA antibodies were maintained by a current larval (vaccinating) intake. IgA titres, however, increased progressively during pregnancy, especially in twin-bearing ewes. IgE titres appeared to be sensitive primarily to the reproductive cycle itself, peaking around parturition.This work supports the conclusion that availability of MP supply influences the recruitment and activity of cells of the immune armoury of the gastro-intestinal tract to nematode parasites. The precise outcome may differ with site and/or nematode species.

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Section: Discussionsupporting

confidence: 82%

Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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The effect of vaccinating infection during pregnancy and dietary protein supply on the peri-parturient immune response of sheep to infection with Teladorsagia circumcincta and Trichostrongylus colubriformis larvae

Sykes

Xie

Stankiewicz

et al. 2007

Animal

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“…Resistance against adult nematodes can be manifested as reduction in fecundity of females, changes in the morphology and or the expulsion of parasites whereas resistance against larval stages of nematodes is manifested as arrested development, reduced establishment and exclusion of immature nematodes [1,21]. The mechanisms that are involved in these immune processes are complex, and probably involve both acquired and innate immune factors including antibodies, inflammatory cell mediators, changes in mucus quality and associated factors.…”

Section: Introductionmentioning

confidence: 99%

Proteomic approach to identify candidate effector molecules during the in vitro immune exclusion of infectiveTeladorsagia circumcinctain the abomasum of sheep

Athanasiadou

Pemberton²,

Jackson³

et al. 2008

Vet. Res.

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-In the present study we have employed an in vitro organ challenge model to study the post-challenge responses in parasite naïve and immune gastric tissue of sheep, in an attempt to identify the host derived factors involved in immune exclusion of Teladorsagia circumcincta larvae. Proteins present in the epithelial cells and mucus from ovine abomasa following parasite challenge in previously naïve and immune animals were analysed through Matrix Assisted Laser Desorption/Ionization-Time of Flight (MALDI-Tof)-MS and shotgun proteomics. MALDI-ToF analysis of epithelial cell lysates revealed that a number of proteins identified were differentially expressed in naïve and immune cells. These included intelectin and lysozymes, which were present at higher levels in epithelial cell lysates derived from immune samples. A large number of proteins were identified in the mucosal wash from immune tissue which were not present in the mucosal wash of the naïve tissue. Some of these proteins were present in washes of immune tissue prior to the parasite challenge including immunoglobulin A, galectin 14 and 15 and sheep mast cell protease 1. However, other proteins, such as calcium activated chloride channel and intelectin were only detected in the washings from the challenged tissue. The latter may be related to an enhanced mucus release, which may result in entrapment of infective larvae and thus reduced establishment in tissue that has been previously challenged with the parasite. In conclusion, several proteins have been identified which may be involved, either directly or indirectly, in the exclusion and immune elimination of incoming infective larvae. In the present study, the usefulness of the in vitro model has been confirmed, and the global proteomic approach has identified proteins that had not previously been associated with parasite exclusion from abomasal mucosa, such as the calcium activated chloride channel.immunity / mucus / proteomics / sheep / Teladorsagia circumcincta

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Host resources and parasite traits interact to determine the optimal combination of host parasite‐mitigation strategies

Dean,

Childs,

Corripio‐Miyar

et al. 2024

Ecology and Evolution

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Organisms have evolved diverse strategies to manage parasite infections. Broadly, hosts may avoid infection by altering behaviour, resist infection by targeting parasites or tolerate infection by repairing associated damage. The effectiveness of a strategy depends on interactions between, for example, resource availability, parasite traits (virulence, life‐history) and the host itself (nutritional status, immunopathology). To understand how these factors shape host parasite‐mitigation strategies, we developed a mathematical model of within‐host, parasite‐immune dynamics in the context of helminth infections. The model incorporated host nutrition and resource allocation to different mechanisms of immune response: larval parasite prevention; adult parasite clearance; damage repair (tolerance). We also considered a non‐immune strategy: avoidance via anorexia, reducing intake of infective stages. Resources not allocated to immune processes promoted host condition, whereas harm due to parasites and immunopathology diminished it. Maximising condition (a proxy for fitness), we determined optimal host investment for each parasite‐mitigation strategy, singly and combined, across different environmental resource levels and parasite trait values. Which strategy was optimal varied with scenario. Tolerance generally performed well, especially with high resources. Success of the different resistance strategies (larval prevention or adult clearance) tracked relative virulence of larval and adult parasites: slowly maturing, highly damaging larvae favoured prevention; rapidly maturing, less harmful larvae favoured clearance. Anorexia was viable only in the short term, due to reduced host nutrition. Combined strategies always outperformed any lone strategy: these were dominated by tolerance, with some investment in resistance.Choice of parasite mitigation strategy has profound consequences for hosts, impacting their condition, survival and reproductive success. We show that the efficacy of different strategies is highly dependent on timescale, parasite traits and resource availability. Models that integrate such factors can inform the collection and interpretation of empirical data, to understand how those drivers interact to shape host immune responses in natural systems.

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The immunobiology of gastrointestinal nematode infections in ruminants

Cited by 198 publications

References 163 publications

The effect of vaccinating infection during pregnancy and dietary protein supply on the peri-parturient immune response of sheep to infection with Teladorsagia circumcincta and Trichostrongylus colubriformis larvae

The effect of vaccinating infection during pregnancy and dietary protein supply on the peri-parturient immune response of sheep to infection with Teladorsagia circumcincta and Trichostrongylus colubriformis larvae

Proteomic approach to identify candidate effector molecules during the in vitro immune exclusion of infectiveTeladorsagia circumcinctain the abomasum of sheep

Host resources and parasite traits interact to determine the optimal combination of host parasite‐mitigation strategies

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