Inflammation-associated responses in piglets induced with post-weaning colibacillosis are influenced by dietary protein level

doi:10.1016/j.livsci.2010.02.026

Livestock Science

Volume 131, Issue 1, June 2010, Pages 58-64

https://doi.org/10.1016/j.livsci.2010.02.026 Get rights and content

Abstract

Forty piglets (average body weight = 5.32 kg) were used to investigate the effect of dietary crude protein (CP) content on immunological responses following a challenge with enterotoxigenic Escherichia coli (ETEC) K88. Pigs, housed 4 per pen, were randomly allotted to 2 diets: 1) a high, 225 g/kg CP diet (HCP) or 2) a low, 176 g/kg CP diet (LCP) supplemented with crystalline amino acids. Pigs were orally challenged with 6 mL of an ETEC K88 suspension containing 10¹⁰ cfu/mL on d 8 after weaning. Blood samples were collected from 10 pigs (1 pig/pen) on d 7 (at weaning), −24 h, 8 h, 72 h and 7 d after the challenge for determination of plasma urea N (PUN) and serum concentrations of tumor necrosis factor alpha (TNF-α) and interleukin 1 beta (IL-1β) and haptoglobin (Hp). Tumor necrosis factor alpha, IL-1β and Hp were measured as indicators of inflammatory responses. The concentrations of serum TNF-α at 8 h, 72 h and 7 d after challenge were similar to the level observed at 24 h before challenge but higher (P < 0.05) than the weaning level. Pigs fed the LCP diet had lower (P = 0.032) concentrations of IL-1β (72 vs. 116 pg/mL) at 8 h post-challenge compared with those fed the HCP diet. Likewise, pigs fed the LCP diet tended to have lower (P = 0.088) concentration of Hp (9 vs. 25 mg/dL) compared with those fed the HCP diet at 8 h post-challenge. Compared with the weaning concentration, PUN concentration at 72 h after ETEC challenge was higher (P < 0.05) in pigs fed the HCP diet. The results indicate that the LCP diet supplemented with crystalline amino acids reduced inflammatory responses, as indicated by serum IL-1β, in piglets infected with ETEC K88.

Introduction

Post-weaning colibacillosis, a disease associated with proliferation of enterotoxigenic Escherichia coli (ETEC), is a major source of revenue loss to the swine industry due to losses resulting from mortality, growth stasis and treatment-associated cost (Amezcua et al., 2002, Fairbrother et al., 2005, Cutler et al., 2007). Previous studies showed improvements in indicators of animal well being when nursery pigs were fed low crude protein (CP), amino acid (AA) supplemented diets such as a reduction in ETEC population and the amount of toxic nitrogenous metabolites in the gut lumen (Nyachoti et al., 2006, Htoo et al., 2007, Wellock et al., 2008). Utilization of low protein diets as a means of managing post-weaning diarrhea requires that such diets do not compromise piglets' performance. It was recently demonstrated that a low CP (170 g/kg) diet supplemented with lysine, methionine, threonine, tryptophan, isoleucine and valine according to the ideal protein ratio supported similar piglets performance up to 106 d of age (Heo et al., 2008).

Enterotoxigenic E. coli K88 infection has been associated with inflammatory responses in piglets and porcine's intestinal cell lines (Bosi et al., 2004, Roselli et al., 2007). Stimulation of the immune system, including inflammatory responses, is an important defense mechanism in animals. However, it has been associated with production penalties such as partitioning of dietary nutrients away from growth toward synthesis of proteins and cells of the immune system (Klasing and Korver, 1997). Fimbrial colonization factor antigen and heat labile enterotoxin of E. coli K88 are potent stimulators of the immune system (Nataro & Kaper, 1998, Nagy & Fekete, 2005) suggesting that it is intestinal colonization by ETEC K88 that triggers immune responses (Verdonck et al., 2002). Thus, diets with low CP level may help to reduce ETEC-associated inflammatory reactions in piglets by reducing ETEC proliferation and subsequent colonization of the gut.

Pro-inflammatory cytokines, interleukin1 beta (IL-1β), interleukin 6 (IL-6) and tumor necrosis factor-alpha (TNF-α), are important mediators of inflammatory responses including production of acute phase proteins (APP) such as haptoglobin (Hp) (Dube et al., 2001, Burger & Dayer, 2002, Chen et al., 2003). Previously, it was demonstrated in an ETEC challenge model that plasma Hp concentration was reduced in piglets fed a low CP diet compared with those fed a high CP diet on d 3 after challenge and the authors suggested that this might be due to protein scarcity in pigs fed the low CP diet (Houdijk et al., 2007). It is unknown whether a low CP diet supplemented with AA based on the ideal protein ration will produce similar result. Likewise, there is paucity of information on the effect of dietary CP content on circulating pro-inflammatory cytokines in pigs.

This study investigated the effect of dietary CP content on inflammatory responses in weaned pigs challenged with ETEC K88 using serum pro-inflammatory cytokines (IL-1β and TNF-α) and Hp as response criteria. Additional data on the effect of dietary protein content on growth performance, animal health and gut microbiology were reported elsewhere (Opapeju et al., 2009).

Section snippets

Animals and housing

The experimental protocol was approved by the Protocol Management and Review Committee of the University of Manitoba Animal Care Committee. Pigs were cared for in accordance with the guidelines of the Canadian Council on Animal Care (CCAC, 1993).

Forty crossbred [Duroc × (Yorkshire × Landrace)] piglets, male and female, weaned at 17 ± 1 d of age (average initial body weight = 5.32 ± 0.24 kg, mean ± SD) and obtained from 7 litters were used in a 14-d experiment. On arrival, piglets were weighed and randomly

Results

There was an effect of time (P = 0.007) on serum TNF-α concentration (Fig. 1). The TNF-α concentration was higher (P < 0.05) at 8 h, 72 h and 7 d after challenge compared with the weaning level but similar to the concentration at 24 h before challenge. In pigs fed the HCP diet, serum TNF-α concentration increased (P = 0.046) at 24 h before challenge compared with the weaning concentration and remained elevated till 7 d after challenge. However, pigs fed the LCP diet had similar serum TNF-α concentration

Discussion

Manipulation of dietary protein content has been suggested as one of the nutritional means of managing post-weaning colibacillosis (Ball & Aherne, 1987, Nyachoti et al., 2006). Enterotoxigenic E. coli K88 infection induces intestinal inflammation (Bosi et al., 2004) and high levels of dietary CP promote proliferation of ETEC (Wellock et al., 2008) in piglets. Thus, it was hypothesized in the current study that a reduction in dietary CP level would reduce the amount of substrate available for

Acknowledgements

Special thanks to Dr. Juan Carlos Rodriguez-Lecompte for reviewing this manuscript.

This project was supported by research grant from Agri-Food Research and Development Initiative and Evonik Degussa Industries. Florence Opapeju is a recipient of R. J. Parker graduate fellowship and Alexander Graham Canadian Graduate Scholarship from Natural Sciences and Engineering Research Council of Canada.

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Inflammation-associated responses in piglets induced with post-weaning colibacillosis are influenced by dietary protein level

Abstract

Introduction

Section snippets

Animals and housing

Results

Discussion

Acknowledgements

J. Nutr.

J. Nutr.

J. Nutr.

J. Nutr.

Livest. Sci.

Livest. Sci.

Livest. Prod. Sci.

J. Nutr.

Livest. Sci.

Vet. Immunol. Immunopathol.

Int. J. Med. Microbiol.

Animal

J. Nutr.

Am. J. Clin. Nutr.

J. Nutr.

Vaccine

Livest. Sci.

Animal

Biology of multifunctional cytokines — IL-6 and related molecules (IL-1 and TNF)

FASEB J.

Presentation of postweaning Escherichia coli diarrhea in southern Ontario, prevalence of hemolytic E. coli serogroups involved, and their antimicrobial resistance patterns

Can. J. Vet. Res.

Carbohydrate and lignin contents of plant materials used in animal feeding

Anim. Feed Sci. Technol.

Influence of dietary nutrient density, level of feed-intake and weaning age on young-pigs.2. Apparent nutrient digestibility and incidence and severity of diarrhea

Can. J. Anim. Sci.

Spray-dried plasma improves growth performance and reduces inflammatory status of weaned pigs challenged with enterotoxigenic Escherichia coli K88

J. Anim. Sci.

Cytokines, acute-phase proteins, and hormones: IL-1 and TNF-α production in contact-mediated activation of monocytes by T lymphocytes

Ann. N. Y. Acad. Sci.

Guide to care and use of experimental animals

Serum acute phase proteins and swine health status

Can. J. Vet. Res.