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Introduction to the immune system

For many years, researchers have been aware of the interaction between nutrition and the health status of animals. Although early research focused on the effects of nutrient deficiencies on the immune system, more recent work has shifted toward enhancement of the immune status of an animal by dietary supplementation. Before any discussion on the effects of nutrition on the immune system, a basic understanding is needed of its physiology. The immune system is a complex array of cells, tissues and signaling agents that work toward the common goal of protecting the body against foreign substances. Although bacteria and viruses are examples of foreign substances that can trigger an immune response, noninfectious foreign substances such as allergens, toxins and parasites also can elicit an immune response.

An animal’s immune system can be divided into two interactive components, innate immunity and adaptive immunity. Innate (also called native or natural) immunity includes physical barriers (skin and gastrointestinal tract), nonspecific phagocytic cells (neutrophils and macrophages), natural killer cells, blood proteins (complement system and inflammation mediators), and regulatory cytokines (Abbas, 2000). Components of innate immunity are present prior to exposure to the antigen. Innate immunity is capable of rapidly reacting to general structures common to groups of microbes and, therefore, may not distinguish between closely related foreign substances. The degree of damage caused by a pathogen is related to its ability to resist the defenses of the innate immunity.

In contrast to innate immunity, adaptive (also called acquired or specific) immunity is highly specific and increases in magnitude and defense capabilities with successive exposure to a particular macromolecule (Abbas, 2000). Four key features of adaptive immunity are specificity, diversity, memory and self/nonself recognition (Kuby, 1994).

Adaptive immunity is specific and, therefore, capable of distinguishing and reacting to subtle differences among antigens. Adaptive immunity also has the ability to react to a large diversity of macromolecules. After an initial exposure, adaptive immunity memory will result in a response to subsequent exposures to the same antigen that is not only more rapid, but also of increased magnitude.

Finally, adaptive immunity can recognize self versus nonself. This capability is vital in prevention of inappropriate response to self-antigen (Kuby, 1994). Due to the specificity of adaptive immunity, this type of response develops later than innate immunity and involves activation of lymphocytes.

The adaptive immune response can be divided into humoral and cell-mediated immunity, which act differently to eliminate various types of microbial challenges from the body. Humoral immunity is mediated by specific antibodies produced by Blymphocytes in response to specific antigens.

Humoral immunity is the primary defense against extracellular microbes and their toxins (Abbas, 2000). In contrast, cell-mediated immunity is mediated by T-lymphocytes that act upon intracellular microbes inaccessible to circulating antibodies (Abbas, 2000).

Innate and adaptive immunity do not act independently, but rather both are a part of a complex system that must act cooperatively for optimal protection from foreign invaders. Two critical links exist between innate and adaptive immunity. First, cells of the innate immune response act to further stimulate an adaptive immune response. For example, macrophages acting against microbes stimulate the specific immune response. Secondly, soluble factors produced during an adaptive immune response can augment innate immunity (Kuby, 1994; Abbas, 2000).

Numerous cell types are involved in an immune response. Within the adaptive immune system, the primary cell types are lymphocytes (including B and T-lymphocytes) and antigen-presenting cells (including macrophages, B-lymphocytes, and  dendritic cells). When activated, B-lymphocytes differentiate into plasma B cells, which secrete antibodies. T-lymphocytes are further divided into helper and inflammatory T cells, which activate other cells, and cytotoxic T cells that kill cells infected with viruses (Abbas, 2000). Antigenpresenting cells internalize antigens and then reexpress them on their cell membrane in the appropriate context to activate both humoral and cell-mediated immunity.

Interactions among the various cells of the immune system are mediated by cytokines, proteins secreted during an innate or adaptive immune response. Cytokines are secreted in response to inflammatory or antigenic stimuli. Cytokines can act on different cells, tissues, or organs in an endocrine, paracrine or autocrine fashion (Hall, 1998). The effects of cytokines can be either local or systemic (Hall, l998).

Since the focus of this review is the interaction of the diet with the immune system, and an intimate relationship exists between dietary ingredients and the gastrointestinal tract, it is also necessary to briefly discuss the mucosal immune system. The mucosal epithelia is a barrier between the internal and external environments, and therefore a first line of defense against antigenic invaders. The gut associated lymphoid tissue (GALT) is composed of cells residing in the lamina propria region of the gut, interspaced between epithelial cells (intraepithelial lymphocytes) and in organized lymphatic tissue (Peyer’s Patches and mesenteric lymph nodes) (Field et al., 1999). The GALT is the largest immune organ of the body (Jalkanen, 1990). The mucosal immune system is specialized to produce large quantities of immunoglobulin A (IgA). This is the only class of antibody that is efficiently secreted through the epithelial cells into the lumen of the gastrointestinal tract (Abbas, 2000).


Interaction of nutrition and immunity

Many nutrients have been implicated in either enhancement or suppression of the immune system. Early studies on the interaction of nutrition and immunity focused on the effects of protein-energy deprivation. Although protein and energy are not typically lacking in today’s companion animal diets, other nutrients may be provided at suboptimal levels due to inaccurate estimations of the maintenance requirement, inadequate supplementation levels, or a uniquely high requirement for a particular life stage or activity level. Three particular nutrients that are currently under investigation as potential dietary immune modulators that will be discussed in the remainder of this paper are omega-3 fatty acids, antioxidants, and nondigestible carbohydrates.


Effects of omega-3 fatty acids on the immune system

Fatty acid supplements have been used to manage skin inflammation in companion animals for many years. Recently, omega-3 fatty acids have received particular attention due to their anti-inflammatory effects when provided in optimal proportions with omega-6 (n-6) fatty acids. Sources of n-3 fatty acids for companion animal diets include coldwater fish oil and flax oil. In contrast, n-6 fatty acids are readily available in plant oils (corn, safflower, and soy) (Reinhart, 1996).

Eicosanoids are potent mediators of the inflammatory response. The eicosanoids that mediate inflammation include prostaglandins, thromboxanes, and leukotrienes (Reinhart et al., 1996). Both n-6 and n-3 fatty acids are precursors of eicosanoids. Fatty acids of the n-6 type result in synthesis of eicosanoids that have inflammatory effects (prostaglandins of the 2 series and leukotrienes of the 4 series), while eicosanoids synthesized from n-3 type fatty acids have antiinflammatory effects (3 series prostaglandins and 5 series leukotrienes) (Wander et al., 1997).

Omega-3 fatty acids have been used in veterinary medicine as supplements to control inflammatory responses associated with disease (Kearns et al., 1999), although the mechanism of action is not clearly understood. Defining the optimal ratio of n-6:n-3 fatty acids for companion animal diets is of current interest. Kearns et al. (1999) evaluated the effects of the n-6:n-3 ratio in both young and old Fox Terriers and Labrador Retrievers. After being fed a basal diet containing a n-6:n-3 ratio of 25:1 for 60 days, half the dogs were switched to a diet with an n-6:n-3 ratio of 5:1 for an additional 60 days. Omega-3 fatty acid supplementation increased prostaglandin E3, a less inflammatory eicosanoid, production from peritoneal macrophages of both young and old dogs. Supplementation with n-3 fatty acids has been suggested to increase oxidative stress of animals, possibly by decreasing vitamin E levels in the blood and tissue (Tappel, 1972). Serum malondialdehyde, an indicator of oxidative status, was significantly reduced in older dogs supplemented with n-3 fatty acids and α-tocopherol levels decreased 34%, although this was not significant (Kearns et al., 1999).

An n-6:n-3 ratio of 5:1 to 10:1 is recommended by Reinhart (1996) based on a study in which adult Beagles were fed diets containing various n-6:n-3 ratios. Neutrophils of dogs fed diets with the recommended ratios synthesized 30-33% less of the proinflammatory leukotriene B4 and 370-500% more of the less inflammatory leukotriene B5. In contrast, feeding diets containing an n-6:n-3 ratio of 1.4:1 to geriatric Beagles (9.5-11.5 years) resulted in a decline in delayed type hypersensitivity responsiveness (an in vivo measure of T-cell immunity) compared to dogs fed a diet with a 31:1 ratio (Wander et al., 1997). Stimulated mononuclear cells of dogs fed the 1.4:1 diet produced 52% less prostaglandin E2 and 20% lower plasma concentration of α-tocopherol compared to dogs fed a the 31:1 diet (Wander et al., 1997).


Effects of antioxidants on the immune system

Dietary antioxidants also have been implicated in modulation of the immune system. Feeding an antioxidant cocktail to puppies from weaning enhances humoral immune response to vaccinations (8 to 12 wks of age) against canine distemper, adenovirus type 2 and parvovirus. Puppies supplemented with antioxidants responded earlier to the vaccination (Devlin et al., 2000). A similar study evaluated the influence of antioxidants on immune function of kittens. Following weaning, kittens were fed either a standard diet formulation for growth or a standard diet supplemented with an antioxidant cocktail. Four weeks after routine vaccination against feline herpesvirus, feline panleukopeniavirus and feline calicivirus, kittens receiving the supplement developed a significantly stronger humoral anti-feline herpes virus immune response compared to control kittens (Devlin et al., 2001). These results suggest that dietary antioxidants may provide a higher level of protection against natural immune challenges (Devlin et al., 2001).

Two specific dietary antioxidants that affect the immune system are vitamin E and selenium (Se). Vitamin E is the major lipid-soluble antioxidant present in plasma and biological membranes. Vitamin E scavenges free radicals in early stages of lipid peroxidation (Burton et al., l983). Cells of the immune system are particularly sensitive to oxidant/antioxidant balance due to the relatively high percentage of polyunsaturated fatty acids in their plasma membrane and frequent exposure to high levels of reactive oxygen intermediates produced as by-products of their normal function (Meydani et al., 1998). Cells of the immune system also have a high concentration of vitamin E (polymorphonuclear leukocytes, 4.47±0.62; lymphocytes 3.89±0.85 µg/10 cells) compared to erythrocytes (1.40±0.14 µg/10 cells) (Hatam and Kayden, 1979).

In 1981, Langweiiler et al. reported that dogs fed vitamin E-deficient diets had diminished lymphocyte responsiveness in mitogen-induced blastogenesis. Lymphocytes from Beagle pups weaned at 6 wks of age onto vitamin E-deficient diets were poorly responsive to the mitogens phytohemagglutinin, concanavalin A and pokeweed, compared to lymphocytes of pups fed an adequate diet. In a subsequent study, these effects were shown to be due, at least in part, to the loss of antioxidant activity in the serum since the vitamin E deficiency-induced suppression of lymphocyte responsiveness could be alleviated by vitamin E, but also by the antioxidants ethoxyquin and 2-mercaptoethanol (Langweiler et al., 1983).

Recent studies have shown that some of the vitamin E biological effects (such as regulation of signal transduction) are independent of its antioxidant effect (Meydani et al., 1998). When young and old Beagles (20 dogs each) were fed diets containing either 27 or 280 IU vitamin E/kg diet for 8 wks, young dogs had a greater increase in plasma vitamin E levels compared to old dogs (50 vs. 20%, respectively). Although young dogs fed the low vitamin E diet had a significant decrease in mitogen stimulated lymphocyte proliferation during the 8 wk feeding period, no such change was observed in the old dogs fed this same vitamin E level (Meydani et al., l998). From these results it was concluded that young dogs were more sensitive to short term decreases in dietary vitamin E levels than old dogs, most likely due to lower storage levels of this vitamin (Meydani et al., 1998). Vitamin E also increases resistance to infection in mice (Heinzerling et al., 1974) and pigs (Ellis and Vorhies, 1986), although little evidence is available in companion animals. Whereas vitamin E can protect against lipid peroxidation in cell membranes, the seleno-enzyme glutathione peroxidase can reduce the level of lipid peroxidation within the cell (Bendich, 1988). Lessard et al. (1993) demonstrated that mitogen stimulated blastogenesis of lymphocytes collected from dogs fed a commercial diet was suppressed when incubated with serum from dogs fed vitamin E and Se-deficient diets. It can be concluded that deficiencies in vitamin E and Se may impair the capacity of the host to control infections.


Effects of dietary fiber on the immune system

Recent research not only has focused on the suppression of the immune system by nutritional deficiencies, but also enhancement via nutrient supplementation. Dietary fibers can elicit an effect on the immune system via a localized effect on the GALT, alteration in microbial populations (prebiotic effect), or a systemic effect on the immune system. In reality, these mechanisms do not act exclusively, but rather interact to cause an overall effect.

Both dietary fiber and its fermentation end products (short chain fatty acids) have been implicated in alterations of the immune system. Fiber type can affect both composition and function of the GALT, as demonstrated in 16 dogs randomly assigned to received diets containing either cellulose, a poorly fermentable fiber, or a highly fermentable fiber blend (beet pulp, gum arabic, and fructooligosaccharide) for 2 wks in a crossover design. Feeding highly fermentable fibers increased the CD4+/CD8+ ratio and decreased the proportion of B cells in peripheral blood but did not change natural killer cell activity or response to mitogens (Field et al., 1999). Cells from the mesenteric lymph node of dogs fed the low, then high fermentable fiber diets contained a higher proportion of CD4+ cells and had a higher response to the mitogens concanavalin A, phytohemagglutinin (PHA), pokeweed and a combination of phorbol myristate acetate plus ionomycin (Field et al., 1999). T-cell mitogen responses were higher for intraepithelial cells but lower for Peyer’s patches and lamina propria cells from dogs fed the low than high fermentable fiber diets, suggesting a lower T-cell response in these predominately B-cell tissues (Field et al., l999). Rats fed highly fermentable indigestible saccharides (glucomannan and curdlan) also had increased cecal mucosal secretion of IgA, while poorly fermentable cellulose reduced cecal mucosal secretion of IgA (Kudoh et al., 1999).

Nondigestible oligosaccharides have also been identified as potential dietary stimulants of the immune system. Nondigestible oligosaccharides elicit their effects on gastrointestinal health by promotion of a beneficial bacterial population (prebiotic effect) and(or) enhancement of the immune system. Fructans (including oligofructose (OF), inulin, and short chain fructooligosaccharides (scFOS) are prebiotic oligosaccharides that aid in pathogenic bacteria resistance by promoting beneficial bacterial growth. These beneficial bacteria compete against pathogens for nutrients and binding sites and produce antimicrobial compounds.

Inulin, a storage carbohydrate found in many plants and vegetables, is a prebiotic ingredient since it is specifically fermented in the colon by the beneficial bacteria Bifidobacterium and Lactobacillus (Meyer et al., 2000). These alterations in microbial populations, or the short chain fatty acids that are produced as a result of this change, can influence the immune system by inhibiting growth of harmful bacteria, reducing liver toxins, restoration of normal intestinal flora and by acting as immunomodulators (Meyer et al., 2000).

Oligofructose is a hydrolyzed product of inulin. Ingestion of only 5 g/day of OF by humans increased the number of bifidobacteria after only 11 days of supplementation (Rao, 2001). Sparkes et al. (1998a,
b) investigated the effects of supplemental OF on the duodenal and fecal bacterial populations of healthy cats. Adult cats were fed either 0 or 7.5 g/kg OF for 12 wk periods in a crossover design.

There were no differences in anaerobic or aerobic bacteria isolated from duodenal fluid aspirates due to OF supplementation (Sparkes et al., 1998a). The researchers surmised that the lack of effect of OF
on duodenal bacterial populations may have been attributed to wide variation among individual cats. Cats consuming 7.5 g OF/kg diet exhibited reduced (P<0.05) concentrations of E. coli (6.3 vs. 7.5 log10
CFU/g) and numerically reduced C. perfringens (4.9 vs. 6.6 CFU/g) in wet feces as compared to the OF-free control. Furthermore, OF supplementation increased fecal concentrations of lactobacilli (6.3 vs. 5.7 CFU/g) and Bacteroides (9.5 vs. 8.0 CFU/g) (Sparkes et al., l998b). This study indicated that low levels of OF supplementation can elicit a more remedial colonic microbial population in cats.

Short chain fructooligosaccharides are synthesized from sucrose by bacteria. Willard et al. (1994) reported that supplementation of diets for German Shepherds suffering from small intestinal bacterial overgrowth with 1% FOS decreased aerobes and facultative anaerobes in duodenal fluid (1,388,750 vs. 5,713,600 CFU/mL contents) and in duodenal mucosa (16,450 vs. 99,475 CFU/g tissue). These results indicate a positive health response and support a role for FOS in the maintenance of gut health.

Mannan oligosaccharides (MOS) are oligosaccharides derived from the cell wall of Saccharomyces cerevisiae. Mannan oligosaccharides can affect the immune system by a number of mechanisms including bacterial exclusion (Spring et al., 2000), neutralization of mycotoxins (Devegowda et al., 1994) and immunostimulation (Newman, 1994). Mannan oligosaccharides exclude many pathogenic bacteria by inhibiting intestinal binding. These bacteria interact with the mucosal surfaces via bacterial fimbriae and specific carbohydrates residues of surface glycoprotein present in animal cells. Many E. coli and salmonellae possess the mannose-sensitive type 1 fimbriae which undergo agglutination by MOS in vitro (Oyofo et al., 1989a; Finucane et al., 1999) and colonize in lower concentrations in animals supplemented with MOS (Spring et al., 2000; Oyofo et al., 1989b).


Mannan oligosaccharides can also protect the animal by neutralization of mycotoxins.

Supplementation of aflatoxin-affected broilers with a Saccharomyces cerevisiae culture results in alleviation of toxic effects (Devegowda et al., l994). Immunostimulation by MOS results in systemic increases in IgG in turkeys (Savage et al., 1996) and a numerical increase in circulating neutrophils in dogs following immunization (O’Carra, 1998). Swanson et al. (2001) found that dogs supplemented with 2 g MOS/day had a significant increase in percent serum lymphocytes and tended to have higher serum IgA concentrations compared to control dogs. In addition, dogs supplemented with 2 g FOS + 2 g MOS/day had significantly greater ileal IgA concentrations (Swanson, 2001).


Summary

Interactions between individual nutrients and the immune system abound. This paper has reviewed only a few of the many interactions that exist. Although historical research has focused on immunological defects caused by nutrient deficiencies, current research is investigating the potential for enhancement of the immune response through nutrient supplementation. Future research will focus on elucidating the role of specific nutrients on the immune system and their potential to improve the health of companion animals.


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