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J APPL POULT RES 2006. 15:341-351
© 2006 Poultry Science Association
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Review Articles

Prospects in Salmonella Control: Competitive Exclusion, Probiotics, and Enhancement of Avian Intestinal Immunity

L. Revolledo*, A. J. P. Ferreira*,1 and G. C. Mead{dagger}

* Department of Pathology, Faculty of Veterinary Medicine, University of Sao Paulo, Av. Prof Orlando Marques de Paiva 87, CEP 05508 – 000, Sao Paulo, SP Brazil; and {dagger} Royal Veterinary College, Boltons Park, Hawkshead Road, Potters Bar, Herts EN6 1NB, United Kingdom

Correspondence: 1 Corresponding author: ajpferr{at}usp.br


   SUMMARY
TOP
 SUMMARY
DESCRIPTION OF PROBLEM
 COLONIZATION OF THE GI...
 ROLE OF CE TREATMENT
 PROBIOTICS AND THEIR PROTECTIVE...
 AVIAN INTESTINAL IMMUNITY
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Salmonella infections are mainly asymptomatic in poultry but are associated with widespread human illness from this source. Therefore, there is continuing interest in finding ways of preventing flock infection and, hence, contamination of poultry products with salmonellas. This review considers aspects of Salmonella carriage in poultry and host interactions that may be exploitable in the future to improve existing control measures. These include factors involved in colonization of the gastrointestinal tract, the role of competitive exclusion and probiotic treatments, and enhancement of intestinal immunity.

Key Words: Salmonella infection • gut colonization • probiotic • competitive exclusion • avian intestinal immunity


   DESCRIPTION OF PROBLEM
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
COLONIZATION OF THE GI...
 ROLE OF CE TREATMENT
 PROBIOTICS AND THEIR PROTECTIVE...
 AVIAN INTESTINAL IMMUNITY
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Salmonellosis is one of the most widespread zoonoses throughout the world, and human infections are often associated with the consumption of contaminated poultry products [1, 2, 3, 4, 5, 6, 7]. In recent years, many incidents have been attributed to raw or undercooked eggs [8, 9], but broilers are also a considerable reservoir of infection for man [10]. Control measures are difficult to use effectively because there are numerous potential sources of Salmonella infection and product contamination in an integrated poultry enterprise. Salmonella can be transmitted vertically and horizontally [11] and may contaminate eggs and carcasses. In the live bird, carriage is usually asymptomatic, and the organisms are shed, sometimes intermittently, in the feces.

Knowledge of the factors that affect Salmonella colonization in the gastrointestinal (GI) tract of poultry may also provide a basis for improved control measures. Consideration of this aspect led to the development of means to increase colonization resistance by manipulating the composition of the intestinal microbiota [12]. The protective effect is usually termed competitive exclusion (CE), a process by which an organism is prevented from colonizing a given environment because of the prior presence of other organisms that are better able to establish and maintain themselves in that environment [13]. The phenomenon has been widely tested in poultry as a means of controlling colonization by paratyphoid salmonellas [14, 15, 16, 17, 18], and potential benefits have been demonstrated under laboratory and field conditions. Although protection of chicks is mainly due to bacterial competition [19], CE treatment may also play an important role in mucosal immunity stimulation, which could contribute significantly to host resistance. The local immune response in the GI tract has been scarcely studied in relation to CE treatment and is likely to involve a variety of factors, including the role of native microflora, host M cells, and secretory IgA (SIgA).

Probiotics, defined as live cultures of microorganisms administered orally, act beneficially on host health; inhibit pathogens; enhance intestinal immunity; and have a protective effect on the gut microflora [20]. There is strong scientific evidence supporting that certain components of the gut microflora are involved in protection of the host against infectious diseases [21].

Factors affecting intestinal colonization of poultry by salmonellas are reviewed in this article, and considerations are given to possible means of increasing host resistance to Salmonella infection by use of CE products or probiotic treatment and their relationship with enhancement of intestinal immunity in the bird.


   COLONIZATION OF THE GI TRACT
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 COLONIZATION OF THE GI...
ROLE OF CE TREATMENT
 PROBIOTICS AND THEIR PROTECTIVE...
 AVIAN INTESTINAL IMMUNITY
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Microbial colonization of the GI tract normally begins soon after hatching and especially when chicks start eating [22]. The organisms present initially are facultative anaerobes and certain clostridia [23]. Salmonellas are not native members of the gut microbiota, but young chicks are readily colonized, and the organisms may persist in the host for some weeks or during all of the rearing period. They become localized in the cecal tonsils and can occur in the upper part of the small intestine and in the gizzard and proventriculus [24]. According to Bailey [25], several factors affect the susceptibility of chickens to Salmonella colonization: a) young birds are more susceptible than older birds, b) survival of Salmonella during passage through the gastric barrier with colonization depending on Salmonella strain and challenge dose [26], c) health and disease status of the birds [27], d) competition between salmonellas and other bacteria, e) environmental stresses that increase susceptibility to colonization [28], f) heritable factors that play a part in the relative resistance of different breeds of bird to Salmonella colonization [29, 30, 31], and g) any medication or antimicrobial feed additives that change the composition of the microbiota in the GI tract, thereby increasing host susceptibility to colonization [32, 33].

There is scant information about the mechanism of colonization, but key factors include the ability of the organism to multiply in the intestinal lumen and penetrate the mucous layer after attachment to the epithelium. Physical attachment has been suggested as the primary mechanism of gut colonization by salmonellas [34], and there is evidence to suggest that fimbriae are involved in the case of Salmonella enteritidis and Salmonella infantis [35, 36]. Attachment of salmonellas to the cecal epithelium has been demonstrated by scanning electron microscopy [34]. Even if adhesion to the cecal wall is not essential for colonization, the presence of low numbers of attached salmonellas would allow fresh cecal contents to become inoculated from this source after periodic emptying and refilling of the cecum. The process may be an important factor in the persistence of salmonellas in the ceca [35]. In addition, the binding of cell-surface adhesives on microorganisms is a critical early step in microbial infection and pathogenesis [37]. The possibility that some Salmonella serotypes use different colonization mechanisms (e.g., Salmonella kedougou) [38] needs to be further investigated, and the genes responsible need to be identified. The presence of genes that are involved in colonization has been demonstrated [39].

Some Salmonella serotypes are more efficient to colonize or invade the GI tract and to localize in organs than others [35, 40, 41]. For example, Salmonella montevideo persists in the gut and is shed in the feces for a longer period than Salmonella typhimurium. Because most birds infected with salmonellas become symptomless carriers, they constitute a reservoir of the organisms that is a potential human health hazard. Also, by contaminating the environment, these birds are responsible for increasing the number of infected individuals.

In poultry, the ceca are favored sites for colonization by enteropathogens, such as Salmonella, because chemical and physical conditions are relatively constant, and there is an abundant supply of nutrients from endogenous and exogenous sources. However, the ceca also contain the largest and most complex microbiota of any region of the GI tract, and it is with these organisms that salmonellas must compete for their survival. The composition of the microbiota changes considerably with age. In the young chick, only a few bacterial species are present initially, and it can take more than 4 wk for the microbiota to reach maturity [23, 42, 43]. The predominant culturable bacteria in the chicken ceca are obligate anaerobes [43, 44]. At least 38 different types of anaerobic bacteria have been isolated [44, 45]. The slow rate of development of the gut microbiota is exacerbated by the conditions of commercial chick production. Once the eggs are laid, there is no further contact with the mother hen, and chicks are hatched and reared initially in clean, sanitized conditions that decrease considerably the opportunity for colonization by native microorganisms. Therefore, the chick remains susceptible to any salmonellas that may gain access to the production environment. This was apparent almost 50 yr ago in a study on the effect of age on the resistance of chicks to Salmonella challenge [46].


   ROLE OF CE TREATMENT
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 COLONIZATION OF THE GI...
 ROLE OF CE TREATMENT
PROBIOTICS AND THEIR PROTECTIVE...
 AVIAN INTESTINAL IMMUNITY
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
The work of Nurmi and Rantala in 1973 [12] highlighted the link between susceptibility to Salmonella infection and the delayed development of the microbiota in the GI tract of young chickens. The CE concept involves introduction of intestinal bacteria from mature chickens into newly hatched chicks, implying the prevention of entry of one agent into a given environment because that space is already occupied [47, 48]. It also provided a simple, practical solution to the problem through the early establishment of an adult-type microflora that markedly increased the resistance of the bird to Salmonella colonization. The protective effect depends upon the administration of viable bacteria that should include aerobes, anaerobes, and facultative bacteria cultures. Treated flocks can be expected to have fewer Salmonella-positive birds than untreated controls and less cecal colonization in those birds that become infected [49]. The complexity of the protective microbiota appears to be important. Attempts to use simpler defined mixtures of treatment bacteria, including conventional probiotic preparations, have been less successful [50].

Some bacteria, such as segmented filamentous and clostridia seem important to induce the development of immune response [51]. The components of the bacterial cell wall, such as peptidoglycan and lipopolyssacharide, have been shown to play and important role in the activation of the immune system [52]. Microbial colonization of the digestive tract also affects the composition of the gut-associated lymphoid tissue (GALT), increasing the number of intraepithelial lymphocytes and immunoglobulin producing cells, in follicles and lamina propria [53]. It can be suggested that CE products might activate the mucosal immune system and enhance Salmonella exclusion.

Several commercial CE products have become available [49, 54] and are based on anaerobic cultures of cecal material from suitable adult donor birds that have been extensively screened to ensure the absence of avian and human pathogens. The products are of undefined composition, but most of them have been partially characterized and include the principal organisms that occur naturally in the ceca of adult chickens. Products aimed at protecting chickens against Salmonella colonization may also be used for turkeys, because there is reciprocal protection between the 2 species [55, 56].

After CE treatment, the factors involved in protecting recipient birds against Salmonella are likely to be the same as those affecting the normal adult microbiota. These have been reviewed by Schneitz and Mead [57] and include a) creation of a restrictive physiological environment, involving microbial production of volatile fatty acids (VFA) and a low oxidation-reduction potential; b) competition among different microbes for receptor sites; c) elaboration of antibiotic-like substances, such as bacteriocins by some microorganisms; and d) microbial competition for essential nutrients. It seems unlikely that any single mechanism is wholly responsible for the protective effect of CE treatment. Although the precise identity of the key protective organisms is unknown, there is evidence that they occur at levels of 107 to 108/g of wet weight of cecal or fecal material in donor birds [58, 59].

Several studies have demonstrated that dietary sugars such as lactose, mannose, and fructooligosaccharides may sometimes reduce levels of Salmonella colonization in chicks [33, 59, 60, 61, 62, 63, 64]. The effective substances are those that are not digested in the small intestine and reach the lower bowel, where they serve as substrates for microbial growth, leading to enhanced production of inhibitory VFA or preferential growth of organisms such as Bifidobacteria. The CE treatment can also be enhanced by dietary sugars [62, 64, 65, 66], although slight scouring or sticky droppings can result and would discourage commercial use.

As an intervention measure, CE treatment is of particular value in controlling horizontal transmission of Salmonella among chicks. For optimum efficacy, however, chicks need to be free from Salmonella before treatment and reared under conditions of good biosecurity, especially during the first 2 d after treatment when the administered organisms are becoming established. Advantages of the treatment include the ease of application (usually by spray inoculation in the hatchery) and the protection provided against any salmonellas capable of invading the GI tract [49]. The response to treatment is relatively rapid, and there appears to be full compatibility with other intervention measures such as vaccination and treatment of feed with organic acids. The CE treatment is particularly appropriate for the broiler, for which any period of Salmonella shedding leads to external contamination of the bird and subsequent spread of the organisms among processed carcasses.


   PROBIOTICS AND THEIR PROTECTIVE EFFECT
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 COLONIZATION OF THE GI...
 ROLE OF CE TREATMENT
 PROBIOTICS AND THEIR PROTECTIVE...
AVIAN INTESTINAL IMMUNITY
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
The term probiotic was first used to describe "substances secreted by one microorganism which stimulate the growth of another" [67]. Later, the term was defined as "organisms and substances which contribute to intestinal microbial balance" [68]. This definition was modified in 1989 to "a live microbial food supplements which beneficially affects the host animal by improving its microbial balance" [20]. In 1998, probiotics were defined as "foods which contain live bacteria which are beneficial to health" [69], whereas in 2002 they were described as "microbial cell preparations or components of microbial cells that have a beneficial effect on health and well-being" [70]. These definitions emphasize that probiotics are live, nonpathogenic, bacteria-denominated, direct-fed microbials that contribute to improved health and balance of the GI tract [71]. Despite these numerous definitions, it has been demonstrated that probiotics inhibit the in vitro growth of many enteric pathogens [72]. Probiotic bacteria have the ability to bind to intestinal mucus, and it has been suggested that adhesion may be a key for exerting their protective effect [73]. Other potential mechanisms include modulation of toxin production or action [74], production of inhibitory metabolites [75], immunomodulation [76], and modulation of cytokine patterns [77].

The anti-infectious effect of probiotic has been reported previously, and one mechanism may be the nonspecific stimulation of immunity. The increase of local IgA levels resulting from ingestion of the probiotic formula may contribute to enhancement of the mucosal resistance against GI infections [78].

Many probiotics have been shown to reduce colonization and shedding of Salmonella and Campylobacter in poultry [79, 80]. The immunological properties of probiotics have been extensively studied, demonstrating that certain lactobacilli enhance systemic and mucosal immunity to enteropathogens, leading to the production of SIgA [81, 82, 83]. Probiotics have modulating effects on the immune system of layer hens and meat-type chickens [84], such as mucosal immunity, intestinal permeability, protective action on mucus, reinforcement of intestinal mucosal barrier, and others. The beneficial effect of the probiotics depends on the host health state, which is an effective tool to prevent colonization by enteropathogens [85, 86].


   AVIAN INTESTINAL IMMUNITY
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 COLONIZATION OF THE GI...
 ROLE OF CE TREATMENT
 PROBIOTICS AND THEIR PROTECTIVE...
 AVIAN INTESTINAL IMMUNITY
CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Mechanisms involved in the development of intestinal immunity in birds have been reviewed [87]. The mucosal immune system is composed of the mucosa-associated lymphoid tissue (MALT), which is found in the nasal passage, the bronchial and genital tracts, and the GALT.

The GALT is a multilayered tissue that is continuously exposed to food antigens, normal gut microbiota, and any ingested pathogens. In chickens, not only are the cecal tonsils the main sites of cecal lymphoid tissue, but they also constitute the largest area of GALT. The lymphocytes present are composed of 45 to 55% B cells and 35% T cells and, thus, are involved in antibody production and cell-mediated immune functions [88]. Various specialized cellular types and lymphoid organs have evolved in the GALT to defend the host against invading pathogens.

The SIgA, the best-defined part of the mucosal immune system, initially mediates defense of the intestinal mucosal surface against enteric pathogens [89]. The mucosal defense system includes 3 components: immune exclusion (a term coined for noninflammatory surface protection), immune regulation, and immune elimination [90]. By interacting with innate, nonspecific defense factors, antibodies that reach the mucosal lumen provide an exclusion effect in which binding of SIgA to the antigen interferes with surface attachment and colonization by pathogens [91].

Young chicks have very few Ig-producing cells in the intestine, but the number increases in response to microbial colonization of the GI tract [92], possibly because of B-cell mitogenic activity of bacterial lipopolysaccharide [93]. This may have a bearing on the relationship between slow gut colonization by normal flora and the establishment of a Salmonella infection [12, 94]. The gut microbiota is important for early stimulation and maturation of the cellular component of the intestinal immune system. Indigenous microbes modulate the immune response by increasing or decreasing the amounts of mediators secreted by immunocompetent cells associated with the intestine and by stimulation of T helpers and suppressors [95, 96, 97, 98, 99]. The microbiota also provides a substantial amount of antigenic material for the mucosal immune system and can influence the oral immunological response [100, 101].

Antigenic material is taken up by the GALT and presented directly to cells of the immune system by enterocytes [102]. Alternatively, antigens can move across or between enterocytes [103] or through specialized areas of the follicle-associated epithelium, termed M cells [104]. These enterocytes have developed an M-cell phenotype [99]. Under normal circumstances, material transported by M cells is taken up by antigen-presenting cells, including B cells and macrophages [90], but recent attention has focused on dendritic cells that have a central role in presenting antigens to T cells and initiating immune responses [105]. Some characteristics of the different kinds of intestinal cells associated to immune response are summarized in Table 1Go.


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  		Table 1. Some important cells in the intestinal tract associated with mucosal immunity
 
The limited studies on antigen uptake from the lumen in the avian GALT have been inconclusive [96]. Manipulation of the gut microbiota with CE products and probiotics has the potential to enhance the intestinal immune response in treated birds, especially in relation to local activation of SIgA secretion. Although differences exist among animal species in the operation of the immune system, the system is functionally very similar in all cases [106], and information on the topic from any source can be used for further understanding of the avian intestinal immune system. Because mucosal intestinal immunity is modulated by the interaction of microflora with the gut immune system, it is likely that changes in the gut during aging affect this micro-environment [107]. In chickens, the posthatch period is of a major immunological importance because the chick is immediately exposed to environmental antigens, and the population of GALT by B cells begins as early as 4 d posthatch and is further increased over the first 2 wk of age [108].

Mucosal immunity is an important aspect of the overall immune system because it operates in tissues that are routinely involved in the host’s defenses against infectious disease as well as tolerance to the gut microbiota and dietary antigens. The intestinal immune response to Salmonella that leads to protective immunity involves a complex interaction between cytokines, leukocytes, epithelial cells, and other factors in the GALT [109, 110, 111, 112]. Cytokines have been demonstrated to play a critical role in induction and expression of SIgA responses at mucosal surfaces [113]. Enhancement of the local immune system in chicks via the use of CE, probiotics, or other substances with immunological activity, may have a significant effect on the control of salmonellas. Based in the first line of defense, the nonspecific immune response proposed model for the reactions involved is shown in Figure 1Go.


Figure 1
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  		Figure 1. Proposed interactions between competitive exclusion products, probiotics or immunostimulants, and avian intestinal immunity. SIgA = secretory IgA; CE = competitive exclusion; IEC = intraepithelial cell; IEL = intestinal intraepithelial lymphocyte; LPL = lamina propria lymphocytes (activated T lymphocytes); dendritic cell or macrophage = antigen-presenting cells (APC); LB = B lymphocyte; LT = T lymphocyte; M cells = cells for the transport of antigens from the intestinal lumen into the gut-associated lymphoid tissue; SC = secretory component; endocytosis = process in which a substance gains entry into a cell without passing through the cell membrane; transcytosis = process of transport of substances across an epithelium layer by uptake on one side of the epithelial cell into a coated vesicle that might then be sorted through the trans-Golgi network and transported to the opposite side of the cell.

Proposed Mechanisms. Antigen uptake: 1. Antigen can be recognized directly by IEL, signals are sent to LT in the lamina propria. 2. When antigen is taken in by M cells using transcytosis process, there are 2 possible mechanisms to stimulate the immune response: a) antigen is directly taken in by macrophages or dendritic cells, which are able to process and present to LT in the lamina propria, or b) antigen activates B cells, which stimulate LT in the lamina propria. 3. Antigen uptake can be made by IEC using endocytosis process. The IEC are able to act as APC and process the antigen, antigen is presented to LT in the lamina propria. SIgA production: activated LT (LPL) produces cytokines, which stimulate LB activation, and finally plasma cells, produce IgA. The IgA acquires the secretory component on the IEC and is able to internalize into IEC; finally SIgA is available in the intestinal lumen to exert surface protection.

 

   CONCLUSIONS AND APPLICATIONS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 COLONIZATION OF THE GI...
 ROLE OF CE TREATMENT
 PROBIOTICS AND THEIR PROTECTIVE...
 AVIAN INTESTINAL IMMUNITY
 CONCLUSIONS AND APPLICATIONS
REFERENCES AND NOTES
 
  1. Salmonella colonization of poultry is not a new problem, but it involves many different factors, and, therefore, better control strategies are always being sought. Genetic selection of resistant stock could make an important contribution to Salmonella control. Although resistance is heritable, other mechanisms involving major histocompatibility complex (MHC) genes, expression, and immune responses may also be important.
  2. Further research will be required to clarify the genetics of Salmonella resistance in poultry and to investigate genetic control of the immune response as well as possible interactions between innate and acquired immunity.
  3. The protective effect of the gut microflora is an important element in the health of the host that ensures the local immunity. Their development depends on the contact with environmental antigens, as CE products, probiotics, or other immunostimulants that can contribute to immune exclusion and prevention of pathogen colonization. Disturbances in the microbiota balance in the gut lead to the growth of salmonellas and their possible invasion of internal organs. The CE treatment is already used in some countries as part of an overall Salmonella control program and needs to be complemented by high standards of hygiene and disinfection at all stages of the production chain. Present commercial probiotic products contain a mixture of viable bacteria, some of which may play a part in the development of colonization resistance through their effects on intestinal immunity.
  4. Salmonella infection induces significant changes in the lymphocyte populations, which are directly related to the immune response. On the other hand, dosing birds with lactic-acid bacteria may enhance a SIgA response that could help to clear pathogens from the GI tract by inhibiting adherence to mucosal surfaces. It can be suggested that the most important anti-infectious effect of CE products and probiotics is the nonspecific stimulation of immunity and the increase in local SIgA, which may contribute to enhancement of the mucosal resistance against infection with enteric pathogens.
  5. The immune-modulation effect of bacteria contained in CE products and probiotics is an alternative for the prevention of Salmonella infections maintaining the integrity of the gut and the stability of their microflora.
  6. More work is needed to elucidate the immune response of the host to Salmonella infections, the complete role of humoral and cellular immunity in the protection offered by CE products and probiotics, along with appropriate means of enhancement of the immune response in a directed and predetermined way.


   ACKNOWLEDGMENTS
 
The authors thank Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (CNPq) for a fellowship to L. Revolledo, Claudette A. Ferreira for technical support related to intestinal immunity, and Alfonso Gozalo, Carmen Michaud, and Edith Fernandez-Baca for various assistance and for reviewing the manuscript. This work is part of a doctoral dissertation that will be presented to the Department of Pathology, School of Veterinary Medicine, University of São Paulo, Brazil.


   REFERENCES AND NOTES
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 COLONIZATION OF THE GI...
 ROLE OF CE TREATMENT
 PROBIOTICS AND THEIR PROTECTIVE...
 AVIAN INTESTINAL IMMUNITY
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 

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