Dietary protein and energy supplies differentially affect resistance to parasites in lactating mammals

Sakkas, Panagiotis; Houdijk, J.G.M.; Jones, Leigh Ann; Knox, Dave P.; Kyriazakis, Ι.

doi:10.1017/s0007114511001565

Cited by 11 publications

(18 citation statements)

References 54 publications

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“…In common eiders, females experience reduced adaptive immunity during incubation (Hanssen et al 2005). Finally, in wild and domesticated ungulates, females experience a well-known increase in susceptibility to gastrointestinal nematode parasitism at the onset of lactation, which is probably caused by protein deficiency (Festa-Bianchet 1989; Houdijk 2008; Jones et al 2011; Sakkas et al 2011). Hence, long-lived species may often be forced to balance the energetic costs of reproduction against other energetically intensive activities that promote survival.…”

Section: Discussionmentioning

confidence: 99%

Costs of reproduction in a long-lived female primate: injury risk and wound healing

Archie

Altmann

Alberts

2014

Behav Ecol Sociobiol

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SUMMARY Reproduction is a notoriously costly phase of life, exposing individuals to injury, infectious disease, and energetic tradeoffs. The strength of these costs should be influenced by life history strategies, and in long-lived species, females may be selected to mitigate costs of reproduction because life span is such an important component of their reproductive success. Here we report evidence for two costs of reproduction that may influence survival in wild female baboons—injury risk and delayed wound healing. Based on 29 years of observations in the Amboseli ecosystem, Kenya, we found that wild female baboons experienced the highest risk of injury on days when they were most likely to be ovulating. In addition, lactating females healed from wounds more slowly than pregnant or cycling females, indicating a possible tradeoff between lactation and immune function. We also found variation in injury risk and wound healing with dominance rank and age: older and low-status females were more likely to be injured than younger or high-status females, and older females exhibited slower healing than younger females. Our results support the idea that wild non-human primates experience energetic and immune costs of reproduction, and they help illuminate life history tradeoffs in long-lived species.

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Section: Discussionmentioning

confidence: 99%

Costs of reproduction in a long-lived female primate: injury risk and wound healing

Archie

Altmann

Alberts

2014

Behav Ecol Sociobiol

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“…Fourteen days prior to mating, all rats were infected subcutaneously in the hind limb with 1600 third-stage infective larvae of N. brasiliensis in 0.5 ml sterile PBS according to a previously established protocol [10]. A secondary infection with 1600 third-stage infective larvae (P; n = 12) was administered on day 2 of lactation (in average 24 days post conception).…”

Section: Methodsmentioning

confidence: 99%

Genome-Wide Transcriptomic Analysis of Intestinal Tissue to Assess the Impact of Nutrition and a Secondary Nematode Challenge in Lactating Rats

et al. 2011

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BackgroundGastrointestinal nematode infection is a major challenge to the health and welfare of mammals. Although mammals eventually acquire immunity to nematodes, this breaks down around parturition, which renders periparturient mammals susceptible to re-infection and an infection source for their offspring. Nutrient supplementation reduces the extent of periparturient parasitism, but the underlying mechanisms remain unclear. Here, we use a genome wide approach to assess the effects of protein supplementation on gene expression in the small intestine of periparturient rats following nematode re-infection.Methodology/Principal FindingsThe use of a rat whole genome expression microarray (Affymetrix Gene 1.0ST) showed significant differential regulation of 91 genes in the small intestine of lactating rats, re-infected with Nippostrongylus brasiliensis compared to controls; affected functions included immune cell trafficking, cell-mediated responses and antigen presentation. Genes with a previously described role in immune response to nematodes, such as mast cell proteases, and intelectin, and others newly associated with nematode expulsion, such as anterior gradient homolog 2 were identified. Protein supplementation resulted in significant differential regulation of 64 genes; affected functions included protein synthesis, cellular function and maintenance. It increased cell metabolism, evident from the high number of non-coding RNA and the increased synthesis of ribosomal proteins. It regulated immune responses, through T-cell activation and proliferation. The up-regulation of transcription factor forkhead box P1 in unsupplemented, parasitised hosts may be indicative of a delayed immune response in these animals.Conclusions/SignificanceThis study provides the first evidence for nutritional regulation of genes related to immunity to nematodes at the site of parasitism, during expulsion. Additionally it reveals genes induced following secondary parasite challenge in lactating mammals, not previously associated with parasite expulsion. This work is a first step towards defining disease predisposition, identifying markers for nutritional imbalance and developing sustainable measures for parasite control in domestic mammals.

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“…In mammals other than humans, there is a well‐recognized increase in susceptibility to helminths, or at least to helminth egg production, around parturition. Immune modulation resulting from hormonal changes (such as a reduction in circulating cortisol) , or nutritional changes, such as protein deficiency may contribute to this effect. In humans, data are conflicting, with studies showing increased or similar helminth egg counts between pregnant and nonpregnant women.…”

Section: Effects Of Pregnancy On Susceptibility To Helminths and On Tmentioning

confidence: 99%

Pregnancy and helminth infections

Mpairwe

Tweyongyere

Elliott

2014

Parasite Immunology

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It has been proposed that helminth infection may be particularly detrimental during pregnancy, through adverse effects on maternal anaemia and on birth outcomes, and that anthelminthic treatment during pregnancy will therefore be particularly beneficial. However, the few treatment trials that have been conducted have given, but little support to this notion and further trials in settings of nutritional stress are needed. It has also been proposed that prenatal exposure to helminth infection has an important effect on the development of the foetal immune response. There is evidence that this may impact, long-term, upon responses to helminth and nonhelminth antigens, and to allergens. Exposure to helminths in utero may also have nonspecific effects that may modify the offspring's susceptibility to diseases mediated by inflammation, including metabolic disorders. The mechanisms of such effects are not known, but they deserve to be explored as current epidemiological findings suggest the possibility of primary prevention for inflammatory conditions such as allergy, through intervention during pregnancy.

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Dietary protein and energy supplies differentially affect resistance to parasites in lactating mammals

Cited by 11 publications

References 54 publications

Costs of reproduction in a long-lived female primate: injury risk and wound healing

Costs of reproduction in a long-lived female primate: injury risk and wound healing

Genome-Wide Transcriptomic Analysis of Intestinal Tissue to Assess the Impact of Nutrition and a Secondary Nematode Challenge in Lactating Rats

Pregnancy and helminth infections

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