Amelioration of the periparturient relaxation of immunity to parasites through a reduction in mammalian reproductive effort

LA Jones, P Sakkas, JGM Houdijk, DP Knox, I Kyriazakis

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

The degree of periparturient relaxation of immunity to gastrointestinal parasites has a nutritional basis, as overcoming protein scarcity through increased protein supply improves lactational performance, enhances local immune responses and reduces worm burdens. Herein lactating rats, re-infected with Nippostrongylus brasiliensis, are used to test the hypothesis that a similar and rapid improvement of immunity can be achieved through reducing nutrient demand at times of dietary protein scarcity. Reducing litter size from 12 to three pups during lactation resulted, as expected, in cessation of maternal body weight loss and increased pup body weight gain compared with dams which continued to nurse 12 pups. This increase in performance concurred with a rapid decrease in parasitism; within 3 days post nutrient reduction, a 87% reduction in the number of worm eggs found in the colon and 83% reduction in worm burdens was observed, which concurred with increased local immune responses, i.e. 70% more mast cells and 44% more eosinophils in the small intestinal mucosa, to levels similar to those in dams nursing three pups throughout. However, there were no concurrent changes in goblet cell hyperplasia, serum anti-N. brasiliensis-specific antibody levels or mRNA expression of IL-4, IL-10 or IL-13 in the mesenteric lymph nodes. To our knowledge the current study is the first to employ a litter reduction strategy to assess the rate of immune improvement upon overcoming nutrient scarcity in a non-ruminant host. These data support the hypothesis that periparturient relaxation of immunity to gastrointestinal nematodes can be reduced by restoring nutrient adequacy and, importantly, that this improvement can occur very rapidly.
Original languageEnglish
Pages (from-to)1127 - 1134
Number of pages8
JournalInternational Journal for Parasitology
Volume42
Issue number13-14
DOIs
Publication statusPrint publication - Dec 2012

Fingerprint

pups
immunity
Nippostrongylus brasiliensis
parasites
nutrients
immune response
body weight
goblet cells
gastrointestinal nematodes
mast cells
nurses
interleukin-4
eosinophils
intestinal mucosa
interleukin-10
hyperplasia
litters (young animals)
litter size
dietary protein
colon

Keywords

  • Eoninophils
  • Mast cells
  • Nippostrongylus brasiliensis
  • Nutrient demand
  • Worm burden

Cite this

@article{35f7726ce1b24fb8ba38f50d5ff0bb77,
title = "Amelioration of the periparturient relaxation of immunity to parasites through a reduction in mammalian reproductive effort",
abstract = "The degree of periparturient relaxation of immunity to gastrointestinal parasites has a nutritional basis, as overcoming protein scarcity through increased protein supply improves lactational performance, enhances local immune responses and reduces worm burdens. Herein lactating rats, re-infected with Nippostrongylus brasiliensis, are used to test the hypothesis that a similar and rapid improvement of immunity can be achieved through reducing nutrient demand at times of dietary protein scarcity. Reducing litter size from 12 to three pups during lactation resulted, as expected, in cessation of maternal body weight loss and increased pup body weight gain compared with dams which continued to nurse 12 pups. This increase in performance concurred with a rapid decrease in parasitism; within 3 days post nutrient reduction, a 87{\%} reduction in the number of worm eggs found in the colon and 83{\%} reduction in worm burdens was observed, which concurred with increased local immune responses, i.e. 70{\%} more mast cells and 44{\%} more eosinophils in the small intestinal mucosa, to levels similar to those in dams nursing three pups throughout. However, there were no concurrent changes in goblet cell hyperplasia, serum anti-N. brasiliensis-specific antibody levels or mRNA expression of IL-4, IL-10 or IL-13 in the mesenteric lymph nodes. To our knowledge the current study is the first to employ a litter reduction strategy to assess the rate of immune improvement upon overcoming nutrient scarcity in a non-ruminant host. These data support the hypothesis that periparturient relaxation of immunity to gastrointestinal nematodes can be reduced by restoring nutrient adequacy and, importantly, that this improvement can occur very rapidly.",
keywords = "Eoninophils, Mast cells, Nippostrongylus brasiliensis, Nutrient demand, Worm burden",
author = "LA Jones and P Sakkas and JGM Houdijk and DP Knox and I Kyriazakis",
year = "2012",
month = "12",
doi = "10.1016/j.ijpara.2012.09.010",
language = "English",
volume = "42",
pages = "1127 -- 1134",
journal = "International Journal for Parasitology",
issn = "0020-7519",
publisher = "Elsevier",
number = "13-14",

}

Amelioration of the periparturient relaxation of immunity to parasites through a reduction in mammalian reproductive effort. / Jones, LA; Sakkas, P; Houdijk, JGM; Knox, DP; Kyriazakis, I.

In: International Journal for Parasitology, Vol. 42, No. 13-14, 12.2012, p. 1127 - 1134.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Amelioration of the periparturient relaxation of immunity to parasites through a reduction in mammalian reproductive effort

AU - Jones, LA

AU - Sakkas, P

AU - Houdijk, JGM

AU - Knox, DP

AU - Kyriazakis, I

PY - 2012/12

Y1 - 2012/12

N2 - The degree of periparturient relaxation of immunity to gastrointestinal parasites has a nutritional basis, as overcoming protein scarcity through increased protein supply improves lactational performance, enhances local immune responses and reduces worm burdens. Herein lactating rats, re-infected with Nippostrongylus brasiliensis, are used to test the hypothesis that a similar and rapid improvement of immunity can be achieved through reducing nutrient demand at times of dietary protein scarcity. Reducing litter size from 12 to three pups during lactation resulted, as expected, in cessation of maternal body weight loss and increased pup body weight gain compared with dams which continued to nurse 12 pups. This increase in performance concurred with a rapid decrease in parasitism; within 3 days post nutrient reduction, a 87% reduction in the number of worm eggs found in the colon and 83% reduction in worm burdens was observed, which concurred with increased local immune responses, i.e. 70% more mast cells and 44% more eosinophils in the small intestinal mucosa, to levels similar to those in dams nursing three pups throughout. However, there were no concurrent changes in goblet cell hyperplasia, serum anti-N. brasiliensis-specific antibody levels or mRNA expression of IL-4, IL-10 or IL-13 in the mesenteric lymph nodes. To our knowledge the current study is the first to employ a litter reduction strategy to assess the rate of immune improvement upon overcoming nutrient scarcity in a non-ruminant host. These data support the hypothesis that periparturient relaxation of immunity to gastrointestinal nematodes can be reduced by restoring nutrient adequacy and, importantly, that this improvement can occur very rapidly.

AB - The degree of periparturient relaxation of immunity to gastrointestinal parasites has a nutritional basis, as overcoming protein scarcity through increased protein supply improves lactational performance, enhances local immune responses and reduces worm burdens. Herein lactating rats, re-infected with Nippostrongylus brasiliensis, are used to test the hypothesis that a similar and rapid improvement of immunity can be achieved through reducing nutrient demand at times of dietary protein scarcity. Reducing litter size from 12 to three pups during lactation resulted, as expected, in cessation of maternal body weight loss and increased pup body weight gain compared with dams which continued to nurse 12 pups. This increase in performance concurred with a rapid decrease in parasitism; within 3 days post nutrient reduction, a 87% reduction in the number of worm eggs found in the colon and 83% reduction in worm burdens was observed, which concurred with increased local immune responses, i.e. 70% more mast cells and 44% more eosinophils in the small intestinal mucosa, to levels similar to those in dams nursing three pups throughout. However, there were no concurrent changes in goblet cell hyperplasia, serum anti-N. brasiliensis-specific antibody levels or mRNA expression of IL-4, IL-10 or IL-13 in the mesenteric lymph nodes. To our knowledge the current study is the first to employ a litter reduction strategy to assess the rate of immune improvement upon overcoming nutrient scarcity in a non-ruminant host. These data support the hypothesis that periparturient relaxation of immunity to gastrointestinal nematodes can be reduced by restoring nutrient adequacy and, importantly, that this improvement can occur very rapidly.

KW - Eoninophils

KW - Mast cells

KW - Nippostrongylus brasiliensis

KW - Nutrient demand

KW - Worm burden

U2 - 10.1016/j.ijpara.2012.09.010

DO - 10.1016/j.ijpara.2012.09.010

M3 - Article

VL - 42

SP - 1127

EP - 1134

JO - International Journal for Parasitology

JF - International Journal for Parasitology

SN - 0020-7519

IS - 13-14

ER -