Microalgae supplementation to late gestation sows and its effects on the health status of weaned piglets fed diets containing high- or low-quality protein sources

Highlights

• Fish oil supplementation reduced fever response following LPS challenge in sows.

• A high-quality protein diet increased anti-inflammatory cytokines concentrations.

• Offspring diet appears more influential on offspring health than maternal diet.

• Acute phase response appears sensitive to maternal treatment.

• Acquired immune response does not appear sensitive to maternal treatment.

Abstract

Maternal stress, such as a bacterial infection occurring in late gestation, may predispose offspring to a variety of diseases later in life. It may also alter programming of developing systems within the fetus, such as the hypothalamic-pituitary-adrenal (HPA) axis and immune system. Dietary supplementation during the last trimester of pregnancy with immune-modulating compounds may be a means of reducing potential adverse effects of maternal stress on the developing fetus. Essential omega-3 polyunsaturated fatty acids (n-3 PUFA) such as docosahexanoic acid (DHA) and eicosapentanoic acid are well-known for their immune-modulating and anti-inflammatory properties. Sources of these n-3 PUFA include fish products such as fish oil and microalgae, which may be a suitable alternative to fish-based products. The aim of this study was to determine the effect of supplementing gestating sow diets with n-3 PUFA and inducing an immune stress challenge in late gestation on piglet growth and immune responsiveness when placed on either a high- or low-quality protein diet after weaning. Forty-eight sows were fed gestation diets containing either 3.12% microalgae, 3.1% fish oil or a corn oil control diet containing 1.89% corn oil starting on gestation day (gd) 75. On gd112, half the sows in each treatment were immune stress challenged with bacterial lipopolysaccharide (LPS) endotoxin (10 μg/kg administered i.m). After farrowing, piglet BW gain was monitored weekly during lactation and pigs were weaned at 21 days of age. One week after weaning, four piglets per sow were immune stress challenged with LPS (40 μg/kg administered i.m.). At the same time, four piglets per sow were vaccinated with the novel antigens chicken ovalbumin (OVA) and Candida cellular antigen (CAA) and received booster vaccinations two weeks later. Four weeks after the initial vaccination, a transdermal hypersensitivity immune challenge was performed using the same antigens. Blood samples were also collected to quantify IgG antibody responses to both antigens. PUFA enrichment in sow blood and piglet brain was detected after sows were on feed for 40 days. Piglet growth was increased in pigs fed a high-quality diet in nursery phase 1. Concentrations of the cytokines IL-1ra, IL-6 and IL-10 were elevated in pigs fed a high-quality protein diet following LPS immune challenge. Overall, it appears that in the current study piglet nursery diet quality was more important for determining piglet health and growth than maternal diet and immune stress.

Introduction

Maintaining piglet health is important around weaning to promote growth and maximize the efficiency of the animal. At weaning, piglets are suddenly stressed as they are removed from their dams and placed into an environment with a potentially high pathogen load (Campbell et al., 2013; Martínez-Miró et al., 2016). In addition, their immune system is not fully developed at this time, and they therefore rely on maternal antibodies for immunity (Campbell et al., 2013). Stress encountered early in life, including microbial infection, can compromise piglet growth and immune function and can affect the long-term health of the animal (Campbell et al., 2013).

To help newly weaned pigs reach their growth potential and mount efficient and appropriate immune responses, the industry standard is to include high-quality, expensive protein sources such as whey protein or purified protein isolates to the diets of newly weaned pigs (Goodband et al., 2014). However, researchers have explored the possibility of including simple, less expensive protein sources such as soybean or canola meals in weanling pig diets to reduce feed costs without compromising growth or health (Collins et al., 2017; Skinner et al., 2014).

Sows are sensitive to stress, and environmental and social changes as well as microbial infections during gestation can disrupt pregnancy and result in abortion, increase number of stillbirths, and/or decrease litter sizes (Peltoniemi et al., 2016). The stress response, mediated by the hypothalamic-pituitary-adrenal (HPA) axis, is activated during Gram-negative microbial infections (Martínez-Miró et al., 2016; Veru et al., 2014) by cell wall lipopolysaccharide (LPS). Activation of the HPA axis produces several signalling neuropeptides and hormones, ultimately resulting in the production of cortisol from the adrenal glands.

The production of maternal cortisol can have negative effects on the developing fetus in utero. Maternal cortisol can cross into fetal circulation despite placental protective mechanisms (Marques et al., 2015). Fetal exposure to maternal stress during gestation can negatively affect offspring growth, stress responsiveness, and immune regulation and function (Götz et al., 2007; Marques et al., 2015; Solano et al., 2016). Limiting the effects of maternal stress on the developing offspring may therefore be an important for ensuring normal piglet health and preventing the occurrence of disease in the peri-weaning period.

Supplementing the maternal diet with immune-modulating compounds such as omega-3 polyunsaturated fatty acids (n-3 PUFA) may be beneficial during pregnancy as a way to reduce inflammation and limit potential adverse effects of maternal cortisol on fetal development (Carroll et al., 2003; Fisher et al., 2014; Liu et al., 2013). Omega-3 PUFA, known for their anti-inflammatory properties, have been shown to affect the differentiation, trafficking and activity of immune cells, decreasing inflammation and favoring tissue resolution (Calder, 2013; Fisher-Heffernan et al., 2015). While acute inflammation may be beneficial, chronic inflammation can contribute to tissue pathology and compromise tissue function (Dhabhar, 2014). Thus, inclusion of n-3 PUFA in maternal diets at an optimal n-6 to n-3 PUFA ratio may be a way of modulating offspring immunity and providing enhanced protection against pathogens that contribute to inflammatory disease.

Most dietary sources of n-3 PUFA are fish-based; however, there is growing interest in finding alternative sources of n-3 PUFA. A promising source of n-3 PUFA is microalgae, which can be grown in tightly controlled conditions (Robertson et al., 2015; Yaakob et al., 2014) and can be rich in either docosahexanoic acid (DHA), eicosapentanoic acid or both, depending on the species (Singh and Saxena, 2015). As algae products become better characterized, they may also become an economical source of n-3 PUFA for livestock diets. While the use of supplements containing n-3 PUFA in sow diets has been explored (Rooke et al., 1998; Shen et al., 2015), there is limited information about the use of microalgae as a source of n-3 PUFA in sow diets and the subsequent effects on the offspring (Gázquez et al., 2017; Posser et al., 2018). Therefore, this study aimed to assess the stress and acquired immune responses of offspring from sows supplemented with dietary fish oil, microalgae or corn oil and challenged with LPS endotoxin in late gestation, when these piglets were weaned onto a high- or low-quality protein nursery diet.