The relationship between dietary fat sources and immune response in poultry and pigs: An updated review

Livestock Science ∎ (∎∎∎∎) ∎∎∎–∎∎∎

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The relationship between dietary fat sources and immune response in poultry and pigs: An updated review S. Swiatkiewicz a,n, A. Arczewska-Wlosek a, D. Jozefiak b a b

National Research Institute of Animal Production, ul. Krakowska 1, 32-083 Balice, Poland Department of Animal Nutrition and Feed Management, Poznań University of Life Sciences, Wołyńska 33, 60-637 Poznań, Poland

art ic l e i nf o

a b s t r a c t

Article history: Received 13 January 2015 Received in revised form 22 July 2015 Accepted 27 July 2015

The aim of this review paper is to present and discuss the current experimental findings describing the effects of dietary oils on the functions of immune cells and the efficacy of different mechanisms of the immune system in poultry and pigs. The majority of experiments of this kind have focussed on dietary sources of n-3 polyunsaturated long-chain fatty acids (n-3 PUFAs). Their results have shown a significant association between dietary fat (i.e., the level of n-3 PUFAs as well as n-6:n-3 PUFAs ratio in the diet) and different mechanisms of immune response. Dietary supplementation with rich sources of n-3 PUFAs, especially with fish oil, can have a beneficial, modulating influence on the immune system; specifically they appear to decrease acute and chronic inflammatory immune reactions and simultaneously to improve indices of specific immune response. However, several studies demonstrated that anti-inflammatory properties of n-3 PUFAs do not always result in improvement of growth or egg performance. & 2015 Elsevier B.V. All rights reserved.

Keywords: Poultry Pigs Dietary fat n-3 Polyunsaturated fatty acids Immunomodulation Immune response

Contents 1. 2.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results of studies on the effects of dietary fats on immunity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Poultry experiments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Experiments on pigs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conflict of interest statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Effective functioning of the immune system is important for protection against infectious diseases, which can negatively affect the production performance and welfare of livestock animals. However, there is some experimental evidence that long-term selection for improved performance (i.e., superior growth rate, carcass weight, and other production traits), may be accompanied by negative physiological consequences, for instance by disadvantageous changes in immune functions and lower resistance of animals to pathogenic factors (Qureshi and Havenstein, 1994; Li et al., 1999; Kramer et al., 2003; Huff et al., 2005; Genovese et al., n

Corresponding author. Fax: þ 48 122856733. E-mail address: [email protected] (S. Swiatkiewicz).

1 2 2 6 8 9 9

2006). For example, in comparing the immunocompetence of fastgrowing commercial broilers (Ross 308) and a line of chickens unselected over decades, it was found that long-term genetic selection for increased growth performance adversely affected the adaptive arm of immune response, i.e., antibody production against sheep red blood cells (SRBC) and lymphoid organ relative weights (Cheema et al., 2003). At the same time, such selection enhanced cell-mediated and inflammatory responses (phytohemagglutinin-P (PHA-P)-induced toe-web swelling response and numbers of inflammatory exudate cells) that are less effective for bacterial diseases and often unfavourable for feed consumption, muscle protein accretion and growth performance (Cheema et al., 2003). Meta-analysis of results from different poultry trials has shown that selection for rapid growth performance significantly reduces responses to a variety of immune challenges and may

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Please cite this article as: Swiatkiewicz, S., et al., The relationship between dietary fat sources and immune response in poultry and pigs: An updated review. Livestock Science (2015), http://dx.doi.org/10.1016/j.livsci.2015.07.017i

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have adverse effects on immune functions (van der Most et al., 2011). Because the nutritional cost of immune functions is relatively high, adequate nutrition is an important factor for the development and effective work of the immune system. Animal requirement for several nutrients, such as certain amino acids, minerals, and vitamins, in order to obtain optimal immune function may be higher than those required for the achievement of maximal growth performance or feed efficiency (Rama Rao et al., 2003; Biswas et al., 2006; Jankowski et al., 2014). However, adding excessive amounts of specific nutrients does not always improve animals’ immune response (Klasing, 2007). In recent years, interest in the use of feed components or feed additives with immunomodulatory properties has increased significantly, especially in conditions of intensive poultry and pig production, where many stressful factors have an adverse effect on animal metabolic status and health (Gallois et al., 2009; El Enshasy and Hatti-Kaul, 2013; Darabighane and Nahashon, 2014). Nutritional immunomodulation can be defined as diet supplementation with specific nutrients or feed additives to influence certain aspects of immune function in order to achieve a given goal (Korver, 2012), i.e., efficient functioning of the immune system and resistance to infectious challenges such as viral, bacterial, or protozoan pathogens. The use of certain dietary sources of fatty acids in animal nutrition is not only a well-documented method for the production of functional food enriched with high contents of n-3 polyunsaturated long-chain fatty acids (n-3 PUFAs) (Pietras and Orczewska-Dudek, 2013; Yanovych et al., 2013; Zdunczyk and Jankowski, 2013), but can also be one of the most efficient nutritional methods of immune-function modulation (Calder, 2001). The effects of dietary fatty acids on immunity are probably due to their importance in a variety of molecular mechanisms, for instance in the synthesis of eicosanoids and cytokines (i.e., mediators of inflammatory response), as well as in T lymphocyte signalling pathways by altering the molecular composition of lipid rafts (Calder, 1998; Miles and Calder, 1998; Calder, 2003; Stulnig, 2003; Stulnig and Zeyda, 2004; Fritsche, 2006; Komprda, 2012; Bederska-Łojewska et al., 2013). A proper n-6:n-3 PUFAs balance in the diet may be important for optimal functioning of the immune system. It should be especially stressed that too high a n-6:n-3 PUFA ratio, often observed in livestock diets, can lead to an increase in the production of pro-inflammatory mediators (cytokines) such as tumour necrosis factor α (TNF), interleukin-1 (IL-1), and interleukin-6 (IL-6) and thus excessively enhance inflammatory response (Simopoulos, 2002), which can negatively affect feed intake (Klasing, 1988; Ferket and Gernat, 2006). Accordingly, the aim of this review paper is to present and discuss the results of recent studies on poultry and pigs evaluating the immune response of animals fed diets supplemented with different fat sources, i.e., oils containing different proportions of n-3 and n-6 fatty acids. As well, the potential for improving production indices in animals as a result of immunomodulation through dietary sources of n-3 PUFAs is discussed.

2. Results of studies on the effects of dietary fats on immunity 2.1. Poultry experiments Several studies in poultry evaluating the effect of dietary oils with different concentrations of n-3 PUFAs (Table 1) have shown positive responses on the modulation of immune response in order to reduce inflammation, enhance health status, and increase growth performance or egg performance (Tables 2 and 3). The goal of early studies by Fritsche et al. (1991a, 1991b) and Fritsche and Cassity (1992) was to compare the immune functions of chickens

Table 1 Approximate composition of common fats used in poultry and pig nutrition. Fat

Main fatty acids and their approximate content

n-6:n-3 Ratio

Sunflower oil Maize oil

C18:1–18%, C18:2 n-6–65%, C18:3 n-3–0.5% 130 C16:0–13%, C18:1–32%, C18:2 n-6–45%, 45 C18:3 n-3–1.0% 20 Lard C16:0–25%, C18:0–14%, C18:1 –42%, C18:2 n-6–10%, C18:3 n-3–0.5% Soybean oil C18:1–22%, C18:2 n-6–52%, C18:3 n-3–10% 5.2 Rapeseed oil C18:1–56%, C18:2 n-6–22%, C18:3 n-3–10% 2.2 Flaxseed oil C18:1–20%, C18:2 n-6–16%, C18:3 n-3–53% 0.30 0.10 Fish (menhanden) oil C16:0–18%, C16:1–11%, C18:1–12%, C18:2 n-6–1.5%, C18:3 n-3–1%, C20:4 n-6– 1%, C20:5 n-3–15%, C22:5 n-3–2%, C22:6 n3–9%,

fed diets containing different fat sources. The fatty acid composition of immune organs clearly reflected the composition of the dietary fat used (Fritsche et al., 1991b). The authors found that humoral immune response was significantly more efficient (i.e., antibody titres against SRBC were higher) when birds were fed a diet containing a high level of very long chain n-3 PUFAs source (7% fish oil), as opposed to other examined dietary fat sources (lard, maize oil, canola oil, linseed oil). At the same time, proliferative responses to concanavalin A and pokeweed mitogen were significantly lower, and eicosanoid production by isolated immune cells was reduced, in chicks fed diets containing oils rich in n-3 PUFAs (Fritsche et al., 1991a; Fritsche and Cassity, 1992). Selvaraj and Cherian (2004a) showed increased anti-bovine serum albumin (BSA) immunoglobulin concentrations in blood, as well as reduced delayed-type hypersensitivity response, measured as the swelling reaction of the wing web skin to M. butyricum antigen, in broiler chickens fed diets containing rich n-3 PUFAs sources (linseed or fish oil). This modulating influence of oils rich in n-3 PUFAs was due to reduced synthesis of pro-inflammatory cytokines and reduced antigen-presenting cell activity, and was positively reflected, at least in the case of fish oil, in feed intake and body weight gains (Selvaraj and Cherian, 2004a). Similar positive changes in immune response were observed by these same authors in laying hens fed diets containing rapeseed and linseed or fish oil; however, these effects were not reflected in feed intake (Selvaraj and Cherian, 2004b). Similar results indicating a modulating effect of n-3 PUFAs on inflammation and immune response were also reported by Wang et al. (2000), who demonstrated that laying hens fed dietary linseed or menhaden fish oil had reduced splenocyte proliferative response to ConA, as well as increased the proportion of IgM þ lymphocytes in the spleen and the concentration of serum IgG, compared to hens fed animal fat or sunflower oil. Similarly, Puthpongsiriporn and Scheideler (2005) reported that a low dietary ratio of linoleic to linolenic acid (n-6:n3 PUFAs ratio), achieved through supplementation of the diet with linseed oil, increased humoral immune response (i.e., antibody production to Newcastle disease-ND and infectious bursal diseaseIBD vaccines), with no effect on growth performance in pullet chicks. In a study with laying hens, Guo et al. (2004) observed higher anti-BSA antibody production and serum lysozyme activity, as well as lower in vitro prostaglandin E2 (PGE2) production by peripheral blood leucocytes, with no effect on egg performance, when dietary oils rich in n-3 PUFAs (fish oil and linseed oil in comparison to maize oil) were added to the diet for laying hens. The authors indicated that the mechanism of obtained changes in immune response (i.e., enhancement of humoral immunity by n-3 PUFAs, as well as an increase in PGE2 synthesis and reduction in serum lysozyme activity and antibody production by n-6 PUFAs) were related to modulation of eicosanoid synthesis by dietary oils

Please cite this article as: Swiatkiewicz, S., et al., The relationship between dietary fat sources and immune response in poultry and pigs: An updated review. Livestock Science (2015), http://dx.doi.org/10.1016/j.livsci.2015.07.017i

Main findings

Source of dietary fats

Animals

Studied characteristics

Maize, linseed, or fish oil (up to 2% in the diet)

Broiler chickens

Conjugated linoleic acid (1.5% in the diet), sunflower, linseed, or fish oil (4.5% in the diet)

Broiler chickens

Maize, poultry, or fish oil (4.5% in the diet)

Broiler chickens

Maize or fish oil (4.5% in the diet)

Broiler chickens

Fish oil (0%, 1.5%, 3%, or 6% in the diet)

Broiler chickens Broiler chickens

Inflammatory response and specific immunity in birds injected Increasing levels of dietary fish oil reduced the growth-suppressing effect of heat-killed S. aureus or S. typhimurium LPS injection through a with IBV vaccine, S. typhimurium lipopolysaccharide (LPS), or modulating effect on inflammatory response (a shift away from inheat-killed S. aureus flammatory response and toward humoral and cell-mediated responses). Immune response following immunisation with M. butyricum Increased anti-BSA immunoglobulin serum content, reduced delayedantigen or bovine serum albumin (BSA) type hypersensitivity response (swelling reaction of the wing web skin to M. butyricum antigen), as well as improved growth performance in birds fed diets with linseed or fish oil Immune function in cyclophosphamide-immunosuppressed Ameliorated immunosuppression, i.e., enhanced anti-NDV titres, lysochickens zyme activity, and performance, as well as reduced production of prostaglandin 2 (PGE2), in birds fed diets with fish oil Immune response following LPS challenge Fish oil alleviated inflammatory response, i.e., reduced production of pro-inflammatory cytokines (of IL-6, TNF-α), alleviated the mRNA abundance elevation of nuclear factor kappa B (NFκB), reduced lymphocyte proliferation, and improved feed conversion efficiency. Antibody titres against sheep red blood cells (SRBC) Enhanced antibody titres against SRBC in birds fed a diet supplemented with fish oil Nuclear factor kappa B (NFκB) gene expression and the down- Alleviated immune stress, i.e., reduced PGE2 production, activity of cystream pathways of intracellular signalling in spleen following clooxygenase 2, and activity of phospholipase C in the spleen; alleviated LPS challenge mRNA abundance elevation of NFκB following LPS stimulation in birds fed diets with fish oil Humoral immune response (antibody titres against SRBC) Fish oil increased antibody titres following immunisation with SRBC.

Maize or fish oil (4.5% in the diet)

Fish oil (0%, 1.5%, 3%, or 6% in the diet) Fish oil (0%, 1%, 2%, or 4% in the diet) Fish oil (0%, 3%, 5%, or 6% in the diet)

Linseed, soybean, and maize oil (used to formulate n-6:n-3 PUFAs dietary ratio of 12:1, 9:1, 6:1, or 3:1)

Broiler chickens Broiler chickens Broiler chickens Broiler chickens

Palm, sunflower, tuna oil (used to formulate Broiler chickens n-6:n-3 PUFAs dietary ratios of 1.5:1, 5.5:1, 45:1) Fish oil (0%, 2.5%, or 5.5% in the diet) Broiler chickens Fish oil (0%, 0.5%, 1.0%, 1.75%, 3.75%, or 7.0% Broiler in the diet) chickens

Humoral immune response (antibody titres against SRBC) Immune tissue weight, immune cell phenotypes, phagocytosis, and cell proliferation T-cell and cytokine mRNA expression in the thymus, blood T lymphocyte subset characteristics

Immune response to infectious bursal disease (IBD) challenged birds Immune response of IBD challenged birds Expression of cyclooxygenase enzymes (COX-1, COX-2), PGE2 concentration, apoptosis and proliferation in ovaries

Broiler chickens

Immune response in birds vaccinated against Newcastle disease (ND) and IBD

Soybean, olive, or fish oil (2.15‒3% in the diet)

Broiler chickens

Humoral immune response and IFN-γ gene expression

Fish oil (0%, 1.5%, or 2.0% in the diet)

Broiler chickens

Weights of immune organs and humoral immune response following challenge with various antigens

Maize or fish oil (4% in the diet)

Broiler chickens Broiler

Proinflammatory eicosanoid production

Soybean, linseed, or sardine oil (7% in the

Immune response in birds non-vaccinated or vaccinated against

Korver and Klasing (1997)

Selvaraj and Cherian (2004a)

He et al. (2007)

Yang et al. (2008)

Saleh et al. (2009) Yang et al. (2011)

Hosseini-Mansoub (2011) Fish oil enhanced antibody titres (IgM) following immunisation and Hosseini-Mansoub and increased body weight gain in chickens fed diets with 1% or 2% fish oil. Bahrami (2011) Al-Khalifa et al. (2012) Reduced bursal weights, lymphocyte proliferation, and percentage of monocytes engaged in phagocytosis, with no effect on immune cell phenotypes, in birds fed high levels of fish oil A decreasing n-6:n-3 PUFAs ratio quadratically lowered mRNA expres- Chen et al. (2012) sion of a cluster of differentiation antigens (CD)4 þ receptor and TLR-3 in the thymus, linearly reduced concentrations of blood CD4 þ, CD8þ and CD4 þ:CD8 þ ratios, and linearly improved body weight gain in first 3 weeks of age. A high level of tuna oil (5.5%, 1.5:1 n-6:n-3 PUFAs ratio) increased IBD Maroufyan et al. (2012) antibody titres at 7 and 14 d following challenge, with no positive effect on growth performance. Increased serum white blood cell count and IL-2 concentration at 7 days Maroufyan et al. (2013) following IBD challenge in birds fed diets with 5.5% fish oil Eilati et al. (2013) Reduced COX-1 and COX-2 protein and mRNA expression, as well as reduced concentrations of inflammatory prostaglandin (PGE2) in ovaries of hens fed diets with fish oil; lower doses of fish oil increased laying performance. Increased heterophil:lymphocyte ratio, reduced weights of the bursa of Sadeghi et al. (2013) Fabricius and spleen, and reduced antibody titres against ND and IBD viruses in broilers fed diets with soybean oil Increased IFN-γ gene expression and antibody titres against ND in birds Sadeghi et al. (2014) fed diets with fish oil. The best growth performance was noted in broilers fed with dietary soybean oil. No effect of dietary fish oil on antibody titres following avian influenza Seidavi et al. (2014) and ND vaccination or following injection of SRBC antigen, or on relative weights of thymus, spleen, and bursa of Fabricius Reduced PGE2 plasma concentration, with no effect on growth perfor- Liu et al. (2014) mance, in broilers fed diets supplemented with fish oil Increased antibody production in vaccinated birds fed diet containing Pinto et al. (2014)

3

Soybean oil (0%, 2%, or 4% in the diet

References

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Please cite this article as: Swiatkiewicz, S., et al., The relationship between dietary fat sources and immune response in poultry and pigs: An updated review. Livestock Science (2015), http://dx.doi.org/10.1016/j.livsci.2015.07.017i

Table 2 Results of selected studies on the effects of dietary fats on immune response in broiler chickens.

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soybean oil (high levels of n-6 PUFAs). No effect of dietary oils on cellular immune response (lymphocyte proliferation) ND chickens diet)

Source of dietary fats

Table 2 (continued )

Animals

Studied characteristics

Main findings

References

4

(Guo et al., 2004). Ebeid et al. (2008) found that the effect of n-3 PUFAs was dependant on their dietary level, as a moderate level of fish oil (2.5% in the diet) increased antibody titres against SRBC, whereas no influence was exerted by higher dietary n-3 PUFAs concentrations (3.5% or 5% of fish oil). However, Seidavi et al. (2014) found no significant effect of dietary fish oil on the humoral immune response of broilers challenged with different antigens. Similarly, no clear influence of salmon fish oil as a source of n-3 PUFAs on antibody production against ND, IBD, and infectious bronchitis (IB) was observed in an experiment with leghorn pullet chicks (Pilevar et al., 2011). Sadeghi et al. (2013) reported that the dietary addition of soybean oil as a rich source of n-6 PUFAs negatively affected immune response (antibody production, relative weights of immune organs) in chickens vaccinated against ND and IBD viruses. In their subsequent work the same authors found that chickens fed dietary fish oil, in comparison with soybean or olive oil, had higher levels of antibody titres against ND and increased IFN-γ gene expression; however, the best growth performance was observed as a result of dietary soybean oil treatment (Sadeghi et al., 2014). In contrast, Pinto et al. (2014) demonstrated greater antibody production in broilers vaccinated against ND when their diet was supplemented with soybean oil (a rich source of n-6 PUFAs) in comparison with fish oil, with no differences in cellular immune response (lymphocyte proliferation). The results of a study with broilers injected with S. aureus or S. typhimurium liposaccharide (LPS) showed that fish oil, in comparison with maize oil, reduced inflammatory response and either improved or had no effect on indices of specific immune response (Korver and Klasing, 1997). Moreover, this immunomodulation mitigated the growth-suppressing effect of injections of immunogen. Thus, as the authors indicated, their findings provided insight into a potential dietary method (diet supplementation with fish oil as a source of n-3 PUFAs) to modulate sensitivity and reduce losses in body weight gain, feed consumption, and feed conversion efficiency that might occur during infectious challenges (Korver and Klasing, 1997). He et al. (2007) demonstrated that dietary fish oil alleviates the immunosuppressive effect of cyclophosphamide in chickens, i.e., increased anti-NDV titres, lysozyme activity, and growth performance, as well as reducing production of PGE2. Sijben et al. (2003), however, found increased mRNA expression of proinflammatory cytokine IFN-γ in LPS-stimulated chickens fed diets supplemented with fish oil, and the authors concluded that innate responses can be modulated by dietary fats differently in birds than in mammals. To compare the effect of dietary sources of n-6 and n-3 PUFAs on nuclear factor kappa B (NFκB) gene expression and downstream pathways of intracellular signalling in spleens of chickens following LPS stimulation, Yang et al. (2011) supplemented the diet with maize or fish oil. They found that dietary fish oil reduced PGE2 production, cyclooxygenase 2 activity, and phospholipase C activity in spleens, as well as alleviated the mRNA abundance elevation of NFκB following LPS stimulation. These results showed that fish oil, as a rich source of n-3 PUFAs, could alleviate immune stress in birds at the level of transcription (i.e., expression of NFκB, which is involved in cellular responses to stimuli) (Yang et al., 2011). Similar results were found in an earlier study by the same authors (Yang et al., 2008), in which modulation of the pro-inflammatory response by fish oil in chickens following LPS challenge was reflected in improved feed conversion. Correspondingly, Liu et al. (2014) demonstrated that dietary fish oil, in comparison with maize oil, reduced concentrations of plasma PGE2 in chickens; however, this modulatory effect was not reflected in growth performance. Eilati et al. (2013), evaluated in a dose-response study, the effect of fish oil (0%, 0.5%, 1.0%, 1.75%, 3.75%, or 7.0% in the diet) on the expression of cyclooxygenase enzymes (COX-1,

Please cite this article as: Swiatkiewicz, S., et al., The relationship between dietary fat sources and immune response in poultry and pigs: An updated review. Livestock Science (2015), http://dx.doi.org/10.1016/j.livsci.2015.07.017i

Source of dietary fats

Animals

Studied characteristics

Main findings

Sunflower, linseed, animal, or menhaden fish oil Laying hens and their Immune response of the offspring of hens fed diets Reduced splenocyte proliferative response and thymus lymphocyte (5% in the diet) offspring containing oils with various fatty-acid compositions proliferation in response to T-cell mitogen (ConA), as well as an elevated proportion of IgMþ lymphocytes in spleen, in chicks fed diets including linseed or fish oil. Dietary fish oil increased serum IgG activity. Maize (2%, 4%, or 6% in the diet), linseed (2%, 4%, Laying hens Immune response (antibody production, serum ly- Positive effect of oils rich in n-3 PUFAs (fish oil and linseed oil) on or 6%), or fish oil (1%, 3%, or 5%) sozyme activity, in vitro PGE2 synthesis by blood anti-BSA antibody production and serum lysozyme activity. In comparison to fish oil, maize oil significantly increased PGE2 leukocytes) synthesis. No effect of dietary oil source and level on egg performance Fish oil (0%, 1.25%, 2.5%, 3.5%, or 5.0% in the diet) Laying hens Humoral immune response (antibody titre against Dietary level of 2.5% fish oil increased antibody titres against SRBC SRBC) with no effect on egg performance; no effect of higher dietary levels (3.5% and 5%) of fish oil on immune response Fish oil (used to formulate n-6:n-3 PUFAs dietary Male, female broiler Cell and humoral immune response following chal- No effect of dietary fish oil on humoral response (total level of anratios of 4:1, 6:1, 8:1, or 16:1) breeders lenge with various antigens tibodies following SRBC injection). Greatest thickness of the toe web (cell immune response) following injection of PHA-P at a dietary n-6:n-3 ratio of 8. A reduced ratio of linoleic to linolenic acid in the diet achieved by Linseed and maize oil (used to formulate ratios Leghorn pullet chicks Antibody production and mitogenic lymphocyte (1-16 wks of age) proliferation following vaccination the addition of linseed oil, increased humoral antibody response to of linoleic to linolenic acid in the diet of 2:1, ND and IBD vaccines, with no effect on the proliferation of lym4:1, 8:1, or 17:1) phocytes in response to ConA and S. typhimurium LPS; no effect of dietary linseed oil (up to 4.4%) on growth performance Growing geese Serum immunoglobulin concentrations Increased IgA, IgG, and IgM in geese fed diets with a low ratio of Peanut, sunflower, and linseed oil (used to forn-6:n-3 PUFAs mulate n-6:n-3 PUFAs dietary ratios of 3:1, 6:1, 9:1, or 12:1)

References Wang et al. (2000)

Guo et al. (2004)

Ebeid et al. (2008)

Khatibjoo et al. (2011)

Puthpongsi-riporn and Scheideler (2005)

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Please cite this article as: Swiatkiewicz, S., et al., The relationship between dietary fat sources and immune response in poultry and pigs: An updated review. Livestock Science (2015), http://dx.doi.org/10.1016/j.livsci.2015.07.017i

Table 3 Results of selected studies on the effects of dietary fats on immune response in laying hens, broiler breeders and geese.

Wang et al. (2012)

5

Tanghe et al. (2014)

Luo et al. (2013)

Leonard et al. (2010)

Farmer et al. (2010)

Mitre et al. (2005)

Expression of proinflammatory cytokines in piglets

Immune response of piglets from sows fed different dietary oils, at weaning and post-weaning Palm, linseed, echium, or fish oil (1% Late-pregnant and lactatin the diet) ing sows and piglets

Immune response of piglets Pregnant and lactating sows

Lard or fish oil (7% in the sows and Late-pregnant and lactatpiglets diets) ing sows and piglets

Linseed(10% in the diet), linseed meal (6.5%), or linseed oil (3.5%)

Fish oil (100 g/ sow/day)

Immune response of sows immunised against ovalbumin (OVA) and their litters

Shark liver oil increased levels of IgG and Aujeszky antibodies in both the blood and colostrum of sows following vaccination, as well as in piglet blood. Beneficial effect of linseed, linseed meal, or oil, as a source of n-3 PUFAs, on immune response (increased production of antibodies against OVA) and survival rate of piglets Increased percentage of leukocytes and lymphocytes phagocytising E. coli, as well as reduced serum IgA concentrations in piglets suckling sows supplemented with fish oil; no effect of dietary treatments on growth performance of piglets Reduced IL-6 and TNF-α production in muscles and increased growth performance in piglets from fish oil fed to dams; converse effect in post-weaning pigs: fish oil in the diet for weaned pigs increased splenic expression of pro-inflammatory cytokines and reduced growth performance. No major effects of the supplementation of maternal diet with different n-3 PUFA sources on the adaptive and innate immunity of piglets Late-pregnant and lactating sows Late-pregnant and lactating sows Shark liver oil (32 g/sow/day)

Immune status of sows and their litters

Main findings Studied characteristics Animals

The results of several studies demonstrated that supplementation of the diets of gestating and lactating sows with rich sources of n-3 PUFAs can modulate the immune status of their progeny (Table 4). Fritsche et al. (1993) found that substituting menhaden fish oil for lard in a sow’s gestation and lactation diet (7%) significantly increased the content of n-3 PUFAs in the immune cells of nursing piglets and reduced in vitro pro-

Dietary oils

2.2. Experiments on pigs

Table 4 Results of selected studies on the effects of dietary fats on the immune response of sows and their offspring.

COX-2), PGE2 concentration, apoptosis and proliferation in the ovaries of laying hens. The authors found that dietary fish oil reduced COX-1 and COX-2 protein and mRNA expression and concentrations of PGE2 in ovaries, as well as improving laying performance. They concluded that the lower doses of fish oil reduce inflammatory PG and may be an effective tool in preventing ovarian carcinogenesis (Eilati et al., 2013). Chen et al. (2012) reported that the modulating effect of decreasing the n-6:n-3 dietary fatty acid ratio (achieved by adding various amounts of linseed, soybean, and maize oils) on the functioning of immune cells was reflected in increases in body weight in broiler chickens during the first 3 weeks of age. Results of a study by Maroufyan et al. (2012) showed the beneficial influence of a high dietary level of fish oil (5.5%, 1.5:1 n-6:n-3 PUFAs ratio) on humoral immune response measured as antibody titres in IBD-challenged broilers; however, this effect was not positively reflected in growth performance indices. To investigate the effect of n-3 PUFAs on selected immune indices of male and female adult broiler breeders, Khatibjoo et al. (2011) supplemented diets with increasing levels of fish oil to achieve n-6:n-3 PUFAs dietary ratios of 16, 8, 6 and 4. The authors reported that cell immune response, measured as thickness of the toe web following an injection of PHA-P, was significantly affected by dietary fish oil, and was greatest when the birds were fed diets containing an n-6:n-3 ratio of 8:1. In contrast, the effect of dietary n-6:n-3 ratios on total antibody levels following an SRBC injection was not significant. As the authors indicated, the suppression of delayed-type hypersensitivity response (toe web thickness index) by the source of n-3 PUFAs (fish oil) could be due to reductions in levels of arachidonic acid and arachidonic-acid-derived eicosanoids and thus to decreased mitogen-presenting cell activity as well as to the direct effect of n-3 PUFAs on the expression of major histocompatibility complex class II antigen on cellular membranes and T-cell proliferation (Khatibjoo et al., 2011). A recent study by Koppenol et al. (2015) evaluated the transgenerational modulating effect of supplementing maternal diets with n-3 PUFAs, i.e., eicosapentaenoic acid (EPA, C20:6 n-3) and docosahexaenoic acid (DHA, C22:5 n-3) on the immune response of chickens. The authors observed no influence of fish oil, as a source of EPA and DHA, in a broiler breeder diet, either on concentrations of plasma pro-inflammatory cytokines in offspring immunised with human serum albumin, or on antibody titres against NDV vaccine. However, on the basis of some small changes in acute phase protein production in the offspring, they concluded that supplementation of a broiler breeder diet with n-3 PUFAs plays a rather minor role in the perinatal programming of immune responses in chickens (Koppenol et al., 2015). The results of an in vitro study (Babu et al., 2009) showed that uptake of n-3 PUFAs, i.e., α-linolenic acid (ALA) and DHA, increased clearance of S. enterica (measured by the plating of sorted viable infected cells) by chicken macrophages (HD11 cells), with no effect on NO or O2  production by HD11 cells. Wang et al. (2011) demonstrated that EPA and DHA inhibited the in vitro proliferation of lipopolysaccharide in LPS-stimulated B lymphocytes in chickens, as well as suppressing the ability of LPS-stimulated B cells to secrete IgA immunoglobulin.

References

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Dietary oils

Animals

Studied characteristics

Main findings

References

Maize or fish oil (7% in the diet)

Weaning pigs

Immune response following challenge with E. coli LPS

Liu et al. (2003)

Maize (6% in the diet) or fish oil (5%)

Weaning pigs

Immune response following immunisation with LPS

Linseed (10% in the diet)

TNF-α gene expression

Flax oil

Growing-finishing barrows Post-weaning male pigs Finishing pigs

Dietary fish oil reduced concentrations of proinflammatory cytokines (IL1β) and improved growth performance in pigs challenged with E. coli LPS, with no effect on lymphocyte proliferation or antibody response to BSA. Fish oil reduced tumour necrosis factor (TNF-α) cytokine production in pigs challenged with LPS. Reduced TNF-α gene expression in pigs fed with linseed diets

Maize or fish oil (5% in the diet)

Weaned pigs

Maize or fish oil (5% in the diet)

Weaned pigs

Maize or fish oil (5% in the diet)

Weaning pigs

Fish oil (0%, 0.5%, 1%, 2% in the diet)

Soybean and linseed oil (3% oils in the diet, used Growing-finishing to formulate n-6:n-3 PUFAs ratios of 1:1, 2.5:1, pigs 5:1, or 10:1) Vegetable or marine oil (3% in the diet)

Weaning pigs

Camelina oil-cakes (12% in the diet)

Finishing pigs

Dietary fish oil modulated immune response, i.e., reduced ex vivo interleukin-1 beta production by peripheral blood mononuclear cells. Plasma immunoglobulin concentrations Increased IgM and IgG plasma concentrations in pigs fed diets supplemented with linseed oil Intestinal integrity and production of proinflammatory Dietary fish oil inhibited TLR4 and NOD2 signalling pathways (downcytokines following immunisation with Escherichia coli regulation of intestinal TNFα and PGE2 concentrations, caspase-3 and heat LPS shock protein expression, mRNA expression of intestinal TLR4 and protein expression of intestinal NFκB p65) and improved intestinal integrity under an inflammatory condition. Production of pro-inflammatory cytokines and muscle Fish oil increased muscle protein mass in inflammatory conditions (LPS atrophy following immunisation with E. coli LPS challenge) by decreasing the expression of muscle pro-inflammatory cytokines. Less severe liver injury (improved serum biochemical parameters and less TLR4 and NOD signalling pathways under an insevere histological liver damage), reduced hepatic mRNA expression of flammatory condition in a LPS-induced liver injury TLR4, myeloid differentiation factor 88, IL-1 receptor-associated kinase model 1 and TNF-α receptor-associated factor 6, NOD1, NOD2 and receptor-interacting serine/threonine-protein kinase 2, as well as reduced hepatic protein expression of NF-κB p65, leading to reduced hepatic proinflammatory mediators, in pigs fed with fish oil Indices of inflammatory immune response Reduced serum concentrations of IL-6 and IL-1beta inflammatory cytokines, as well as downregulated expression levels of IL-6, IL-1beta and TNF-α mRNA in the skeletal muscle and adipose tissue of pigs fed diets with an n-6:n-3 PUFAs ratio of 1:1 Immune response (TNF-α activity) between days 0 and Immune stress induced by weaning (measured as increase of TNF-α ac28 post-weaning tivity) was ameliorated by dietary n-3 PUFAs source (marine oil). Protein and gene expression of pro-inflammatory Reduced protein and gene expression of interleukin 1-beta (IL-1β), TNF-α, cytokines IL-6, IL-8, and COX-2 in the spleens of pigs fed diet containing camelina oil cakes Pro-inflammatory cytokine production

Gaines et al. (2003) Huang et al. (2008) Merle et al. (2011) Habeanu et al. (2011) Liu et al. (2012)

Liu et al. (2013)

Chen et al. (2013)

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Table 5 Results of selected studies on the effects of dietary fats on the immune response of growing-finishing pigs.

Duan et al. (2014)

Li et al. (2014) Taranu et al. (2014)

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inflammatory eicosanoid release by the piglets’ immune cells. Farmer et al. (2010) showed that feeding different sources of linen (i.e., linseed, linseed meal, or linseed oil) as a source of n-3 PUFAs to late-pregnant and lactating sows improved the immune response of their litter, measured as production of antibodies against ovalbumin, which was reflected in turn in an increased survival rate for piglets, though there was no increase in their growth performance. Similarly, a positive effect of n-3 PUFAs on immune response, measured as enhanced percentage of leukocytes and lymphocytes phagocytising E. coli, was not reflected in body weight gains in an experiment by Leonard et al. (2010). Luo et al. (2013) demonstrated reduced pro-inflammatory IL-6 and TNF-α expression in muscles and an enhanced growth rate in piglets from sows fed a diet containing 7% fish oil. However, they observed that weaned pigs the diet with 7% fish oil were characterised by increased splenic expression of pro-inflammatory cytokines and decreased growth performance. As the authors indicated, these contrary effects of 7% fish oil in the diet of sows or weaned pigs could be due to the different amounts of n-3 PUFAs received by the piglets (i.e., to the much lower content of n-3 PUFAs in milk than in the weaned pigs’ diet) (Luo et al., 2013). Thus, they concluded that moderate n-3 PUFAs intake in dams’ milk might exert a positive influence on piglets’ growth rate through reduction of pro-inflammatory cytokine expression. However, too high intake of n-3 PUFAs (i.e., 7% fish oil directly in the diet) could promote pro-inflammatory cytokine production and negatively affect growth performance (Luo et al., 2013), probably due to increased energy density of the feed, which in turn enhances metabolic or post-prandial inflammation (Margioris, 2009). Mitre et al. (2005) reported a positive effect of shark liver oil, a rich source of n-3 PUFAs, in a diet for gestating and lactating sows on the level of IgG and Aujeszky antibodies in the blood and colostrum of sows following vaccination, as well as in piglet blood. This effect was reflected in piglet growth performance; however, the authors indicated that litter size in the experimental treatment was lower and birth weight higher than in the control group, making it difficult to clearly identify the role of sow supplementation with shark liver oil on the piglets’ body weight gain (Mitre et al., 2005). Contradictory results were reported recently by Tanghe et al. (2014), who found no major effect of different sources of n-3 PUFAs (linseed, echium, or fish oil) in a diet for gestating and lactating sows on the adaptive and innate immunity of their offspring. It is supposed that lack of consistency in the effects of dietary PUFA n-3 on immune indices and growth performance of animals may be the result of differences in experimental conditions. Under optimal circumstances, existing on some of experimental farms, animals perform at close to 100% of their genetic potential, so it is difficult to observe beneficial effect of dietary PUFA n-3 addition on immune response and growth performance (Khadem et al., 2014). The results of a study with post-weaning pigs (Merle et al., 2011) showed that fish oil exerts immunomodulatory properties by decreasing interleukin-1 beta (IL-1β) production by peripheral blood mononuclear cells (Table 5). Corresponding results were obtained by Li et al. (2014), who reported that immune stress (i.e., an increase in plasma TNF-α cytokine concentration), induced by weaning was ameliorated by dietary marine oil containing large amounts of n-3 PUFAs, albeit with no positive effect on performance indices. However, in an experiment by Liu et al. (2003), the downregulating effect of fish oil on immune system activation, measured as production of pro-inflammatory cytokines, of weaned pigs challenged with E. coli lipopolysaccharide (LPS), did not result in improved growth performance. In a study by Thies et al. (1999), the modulating effect of dietary fish oil in weaned pigs was related to a reduced proportion of phagocytes engaged in the uptake of E.

coli and to reduced natural killer cell activity by blood lymphocytes. Liu et al. (2012) demonstrated that dietary fish oil improved intestinal integrity under an inflammatory condition (E. coli LPS challenge) by alleviating intestinal inflammatory response (i.e., by reduction of intestinal TNFα and PGE2 concentrations, caspase-3 and heat shock protein expression, the mRNA expression of intestinal TLR4 and the protein expression of intestinal NFκB p65). The same authors reported that the inhibition of muscle pro-inflammatory cytokine concentration by dietary fish oil was reflected in increased muscle protein mass in weaned pigs challenged with E. coli LPS (Liu et al., 2013). This modulation of immune status is of great importance for the swine industry, given that increased numbers of inflammatory reactions, leading to the depression of feed intake and growth rate in pigs, are often being observed during the post-weaning period (Pie et al., 2004; Campbell et al., 2013). Chen et al. (2013) demonstrated that dietary fish oil, in comparison with maize oil, had a hepatoprotective effect by reducing pro-inflammatory mediators in a LPS-induced liver injury model. Weaning pigs fed fish oil had improved serum biochemical parameters and less severe histological liver damage. In addition, it reduced the hepatic mRNA expression of TLR4, myeloid differentiation factor 88, IL-1 receptor-associated kinase 1, TNF-α receptor-associated factor 6, and NOD1, NOD2 and receptor-interacting serine/threonine-protein kinase 2, as well as reducing the hepatic protein expression of NF-κB p65 (Chen et al., 2013). Chytilova et al. (2013) determined the effect of linseed oil, a rich source of linolenic acid (C18:3 n-3), on the gene expression level of selected cytokines in gnotobiotic piglets infected by enterotoxigenic E. coli (ETEC) an found that linseed oil possessed significant anti-inflammatory properties, i.e., it reduced the level of mRNA expression of selected pro-inflammatory cytokines (IL-1α and IL-8) when used in combination with probiotic bacteria (L. plantarum). The immunomodulatory effect of n-3 PUFAs has also been observed in growing-finishing pigs (Table 5). Taranu et al. (2014) reported that fatteners fed diet with 12% camelina oil cakes, a rich source of n-3 PUFAs (mainly C18:3 n-3), had reduced the protein and gene expression of such pro-inflammatory cytokines as IL-1β, TNF-α, IL-6, and IL-8, as well as COX-2, in the spleen, with no effect on growth performance. Corresponding results were found by Zhan et al. (2009), who evaluated the immune status of growingfinishing pigs fed a diet enriched, for 0, 30, 60, and 90 days before slaughter, with 10% linseed, another rich source of n-3 PUFAs. The authors showed that dietary linseed linearly (during the feeding period) reduced the gene expression of pro-inflammatory cytokines in muscles, adipose tissue, and the spleen, along with the serum concentration of TNF-α. Moreover, growth performance responded quadratically to the duration of linseed diet feeding, so that the greatest body weight gain was found in pigs fed linseed for 60 days (Zhan et al., 2009).

3. Conclusions Effective functioning of the immune system is required for protection against infectious diseases, which can negatively affect the performance and welfare of livestock animals. In summing up the findings from the literature discussed in this review, it can be stated that dietary n-3 PUFAs possess immunomodulatory properties, and that oils which are rich sources of n-3 PUFAs may beneficially modulate the immune systems of poultry and pigs, i.e., may decrease acute and chronic inflammatory immune reactions and improve indices of specific immune responses. It should be stressed that the use of fish oil, as a direct source of n-3 PUFAs, yields better results in terms of immune response than the use of

Please cite this article as: Swiatkiewicz, S., et al., The relationship between dietary fat sources and immune response in poultry and pigs: An updated review. Livestock Science (2015), http://dx.doi.org/10.1016/j.livsci.2015.07.017i

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rapeseed or linseed oil rich in α-linolenic acid, a precursor of n-3 PUFAs. The dietary addition of 2-4% fish oil, decreasing n-6:n-3 ratio in the diet to 2–3, is the recommendation level in terms of immunomodulation. However, several studies demonstrated that anti-inflammatory properties of n-3 PUFAs do not always result in improvement of growth or egg performance.

Conflict of interest statement The authors confirm that this work involves no conflict of interest.

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Please cite this article as: Swiatkiewicz, S., et al., The relationship between dietary fat sources and immune response in poultry and pigs: An updated review. Livestock Science (2015), http://dx.doi.org/10.1016/j.livsci.2015.07.017i