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A review of avian probiotics.

Abstract: Probiotics have been used in poultry for decades and have become common in the pet bird industry. Desirable characteristics of probiotic organisms are that they are nonpathogenic, have the ability to adhere to intestinal epithelial cells, have the ability to colonize and reproduce in the host, have the ability to be host-specific, survive transit through the gastrointestinal tract and exposure to stomach acid and bile, produce metabolites that inhibit or kill pathogenic bacteria, modulate gastrointestinal immune responses, and survive processing and storage. Purported benefits in birds are disease prevention and promotion of growth. Recommendations for use in avian species are for periodic use to replenish normal flora, use after antibiotic therapy to reestablish normal flora, and use during periods of stress to counter effects of immunosuppression.

Key words: probiotics, Lactobacillus, avian, pet birds

Introduction

Probiotics have become increasingly prominent in both the human and animal health supplement industries. The currently accepted Food and Agriculture Organization/World Health Organization definition of a probiotic is "live microorganisms which, when administered in adequate amounts, confer a health benefit on the host." Until recently, the Food and Drug Administration (FDA) required products labeled as probiotics to be FDA-approved or indexed because the definition (and public perception) of probiotic inherently implies that the products meet FDA's definition of a drug: "articles intended for use in the diagnosis, cure, mitigation, treatment, or prevention of disease" and "articles (other than food) intended to affect the structure or any function of the body of man or other animals" (Food, Drug, and Cosmetic Act, section 201 (g)(1)). Now, the FDA has relaxed its regulations on probiotics, allowing them to be labeled as probiotics with approval only necessary if any efficacy claims are made on the label. Beneficial bacterial products have been used in the poultry industry for decades, labeled as "direct fed microbials" and in the pet bird industry as "nutritional supplements." Now that the FDA has changed its regulations, many products labeled as avian probiotics are being put on the market. A review of the avian probiotic literature is helpful to better evaluate these new products.

Historical Perspective

When reviewing the history of avian probiotics, the first several decades focus on poultry. The poultry industry has always been challenged by gastrointestinal disorders, the need for maximal feed conversion and growth rates, and difficulties and expenses of using antimicrobial treatments. Even back in the 1920s, researchers were experimenting with the use of beneficial bacterial supplements. (1) In the 1950s, many papers came out describing the normal bacterial flora of chickens and turkeys. Various species of lactobacilli and anaerobic coccoid bacteria were established as the predominant normal flora. (2-7) In the 1960s, germ-free environments and gnotobiotic chicks and poults became available, and research shifted to investigating the effects of introducing pure cultures of normal bacteria and pathogenic bacteria. It became apparent that certain normal bacteria helped gnotobiotic birds survive challenges with pathogens, but the effect was variable from strain to strain. (8) In 1973, Nurmi and Rantala published a paper describing protection of broiler chicks from Salmonella species infection by dosing them with a suspension of gut contents from adult chickens. (9) The "Nurmi concept" sparked vigorous research into the components of this effect and its mechanisms of action. Because of the potential for transmitting diseases along with beneficial organisms by using these "undefined" probiotics, research continued to develop defined probiotics that could be cultivated and administered in pure cultures. Also in 1973, Fuller began publishing his research on lactobacilli found attached to the crop epithelium of birds. His research provided insights into the variability of results seen when lactobacilli and other beneficial bacteria were administered to poultry. Before his publications, there were as many reports of no effect as there were reports of beneficial effects of selected beneficial bacteria. Fuller found that lactobacilli must attach themselves to the intestinal mucosal cells in order to confer their beneficial effects. (10,11) Research then shifted to examining adhesion and to further defining the characteristics that bacteria need to have to provide the most beneficial effects. In the past decade, research has continued to illuminate ways that probiotic bacteria influence the bird's health and how they exert their positive effects.

In the late 1960s and 1970s, the pet bird industry in the United States was expanding, due to importation and domestic captive breeding. By the late 1970s researchers began investigating the normal flora of pet birds. Most papers reported predominantly gram-positive bacterial flora and, as in poultry, most frequently, various species of lactobacilli and gram-positive cocci. (12-15) Researchers who questioned the importance of lactobacilli failed to use selective media or microaerophilic conditions in their protocol. (16) Aviculturists began to use probiotics developed for poultry or mammalian Lactobacillus species supplements. These products were labeled as nutritional supplements and their efficacy in psittacine birds was unknown. Three studies were done on the use of these products in psittacine birds in the late 1980s and 1990s, finding either no effect or a growth promotion effect only. (17-19) In 2003, a study reported significant improvement in growth rates, reduction of gram-negative bacteria, and increases in total Lactobacillus species counts in cockatiel {Nymphicus hollandicus) chicks given Lactobacillus salivarius isolated from adult cockatiel crop epithelial cells. (20) In 2009, a commercially available product containing Lactobacillus species was found to improve the ratio of gram-positive rods to gram-positive cocci in the feces of 3 species of macaws, based on results of fecal Gram stains. (21)

Desirable Characteristics of a Probiotic

After decades of probiotic research, a list of characteristics of the ideal probiotic was proposed. The probiotic should be nonpathogenic, have the ability to adhere to intestinal epithelial cells, have the ability to colonize and reproduce in the host, be host-specific, survive transit through the gastrointestinal tract and exposure to stomach acid and bile, produce metabolites that inhibit or kill pathogenic bacteria, modulate gastrointestinal immune responses, and survive processing and storage. (22)

Nonpathogenicity

All probiotic organisms in use today are categorized as Generally Regarded as Safe. Throughout the body of literature, although many studies have reported no significant benefit from the organisms used, none have reported adverse effects.

Ability to adhere

Researchers became aware of the importance of adherence through a series of papers published by Fuller. In these reports, all the avian species that were examined--chickens, turkeys, quail, ducks, pheasants, and pigeons--had Lactobacillus species that adhered to chicken crop epithelial cells in vitro. Lactobacillus species isolated from 10 different mammalian species did not. Other genera of bacteria isolated from birds did not adhere to chicken crop epithelial cells; only Lactobacillus species adhered. (10,11) Administration of mammalian lactobacilli to chickens in vivo had no effect, but administration of adherent lactobacilli from chickens resulted in better growth rates and resistance to gram-negative bacterial infections. (11,23,24) Since the discovery of epithelial adherence in avian lactobacilli, most researchers have found that strains of lactobacilli with a high level of adherence provide the greatest health benefits. (24-31) Conversely, nonadherent lactobacilli appear to have little or no benefit in birds. In a study of cockatiel chicks given an adherent cockatiel-derived salivarius, the control group was found to have nonadherent lactobacilli by 2 weeks of age, presumably from the environment. The groups given the adherent lactobacilli still performed significantly better, with faster growth rates, a 100-fold reduction in gram-negative bacteria, and higher total numbers of lactobacilli. (20)

Theories of why adherence is important for the probiotic effect include the need for resident bacteria to repopulate the intestinal tract when the crop empties, provision of a ready supply of beneficial bacteria to inoculate incoming food, competition with pathogens for epithelial binding sites, and cross-talk with epithelial cells to modulate cell function and morphology. (10,11,31-35) Epithelial-microbial cross-talk refers to the physiologic communication that occurs when a bacteria forms an adhesive link to an epithelial cell. Biochemical and morphologic changes take place in the epithelial cells, leading to conditions that either favor a pathogen's harmful effects or help protect the host from disease.

The ability to adhere, although important, is not the only determinant of probiotic efficacy. Several studies have been reported in which species-specific, adherent lactobacilli did not show significant beneficial effects, especially when attempting to prevent Salmonella species infection or reduce Salmonella shedding. (36-38) One study examined the nhibitory effects of 2 different adherent lactobacilli on epithelial attachment of 3 different Salmonella species. Lactobacillus fermentum reduced attachment of Salmonella Pullorum by 77% and had no effect on Salmonella Enteriditis or Salmonella Gallinarum, whereas Lactobacillus animalis was able to reduce attachment of Pullorum by 90%, Enteriditis by 88%, and Gallinarum by 78%. (27) The combination of several traits seems to determine an organism's effectiveness. (25)

Ability to colonize and reproduce

Successful probiotic organisms colonize, reproduce, and become the predominant flora in the bird. Colonization is favored by adherence, but some organisms with low levels of adherence have been found to colonize well because of rapid reproduction. (31) It can be assumed that when a probiotic organism can be recovered from feces or a cloacal swab several days after the end of administration, the organism has colonized the bird's intestinal tract.

Host species specificity

In human and animal probiotic research, species specificity of the probiotic strain is considered essential for effectiveness. Effects of administration of adherent lactobacilli from one species of bird to a different species of bird are not well studied. The vast majority of avian research reports have utilized chicken-derived bacterial strains in chickens. Although Fuller tested adherent lactobacilli isolated from various bird species for adherence to chicken crop epithelial cells in vitro, this was not tested in vivo. (10,11) In one study, adherent chicken-derived Lactobacillus species failed to decrease numbers of Salmonella species in turkey poults; however, as mentioned earlier, different lactobacilli strains have different levels of effectiveness against Salmonella species. (39) In another report, Lactobacillus reuteri isolated from chickens was found to reduce Salmonella species infection in both chicks and poults. (40) In studies of mammalian and chicken-derived lactobacilli in psittacine birds, adherence was not evaluated and either the dose of viable organisms given was not determined or live organisms could not be found in the probiotic administered. In one study, mammalian Lactobacillus acidophilus was administered to Quaker parakeets (Myiopsitta monachus) for 3 days. No significant difference was found between the flora of the controls and the treatment birds. Lactobacillus acidophilus was recovered from cloacal swabs in some birds during the treatment period but not after. No live organisms were found in the product used. (17) In a report on the use of a chicken-derived probiotic in various species of neonatal psittacine birds throughout their hand-feeding period, no significant changes in growth rate, aerobic cloacal flora, or resistance to disease were found. No live lactobacilli were ever cultured from the probiotic used. (18) In neonatal cockatiels, 2 different formulations of a chicken-derived lactobacillus-based nutritional supplement were administered from 14 to 42 days of age. Live lactobacilli were recovered from the probiotics, but actual numbers present were not titrated. The group receiving a gel formulation showed significantly increased growth rates but no significant reduction in numbers of Escherichia coli or Candida albicans. (19) By comparison, as mentioned earlier, cockatiels given an adherent cockatiel-derived salivarius from hatch to 6 weeks of age showed significantly increased growth rates, reduced levels of gram-negative bacteria, and increased total numbers of lactobacilli. (20) A Lactobacillus-based probiotic of undisclosed derivation given to 3 species of macaws--spix (Cyanopsitta spixii), Lear's (Anodorhynchus leari), and hyacinth (Anodorhynchus hyacinthinus)--caused a shift from predominantly gram-positive cocci flora back to predominantly gram-positive rod flora. (21) Given the endangered status of the 3 macaw species, the probiotic used here likely represents a cross-genus effect. These limited reports in psittacine birds seem to suggest that the probiotic effect depends on the presence of sufficient numbers of live organisms and cross-species effects do occur, but more dramatic benefits may be seen when using adherent or species-specific bacteria. More research is needed to make more definitive conclusions.

Ability to survive transit through the GI tract

To populate the entire intestinal tract, a probiotic organism must be able to survive passage through the acidic environment of the proventriculus and gizzard and survive in the presence of bile in the intestinal contents. As the crop mucosa sloughs with its adherent lactobacilli, those lactobacilli that survive arrival into the intestines are able to exert their beneficial effects in the lower gastrointestinal tract. Studies of potential probiotic organisms often include in vitro incubation in solutions adjusted to pH 3, solutions containing bile, and in vivo identification of the organism in the epithelial cells of the lower gastrointestinal tract. (25,27,31,41,42) The most effective probiotics are those that have been screened for these traits.

Production of inhibitory metabolites

Since the 1970s, it has been acknowledged that competition for binding sites is only one way that probiotic organisms inhibit pathogenic organisms. Initially researchers attributed inhibition to lowered pH of the intestinal contents due to lactic acid produced by lactobacilli. (11) Later it became apparent that low pH or lactic acid alone did not have the same inhibitory effect, and other inhibitory metabolites were discovered and investigated. (24,25,35,43) Lactobacillus reuteri was found to produce a metabolite called reuterin, which is actually bacteriocidal to many pathogenic bacteria. (44) Different lactobacilli vary in the types and amounts of metabolites they produce. One study tested in vitro inhibition of 2 pathogens, E. coli and Enteriditis, by supernatant solutions containing metabolites from 296 different strains of lactobacilli isolated from the intestinal tracts of chickens. They found 77 strains yielded inhibitory metabolites against one or both of the pathogens, and 35 of those showed strong inhibition against both pathogens. (25)

Ability to modulate the immune response

Probiotics have also been found to improve immune function and influence morphologic changes in the intestines that impact disease resistance. In humans and other mammals, lactobacilli stimulate immune system cells to produce cytokines, which modulate the immune response. (45-48) Similar responses have been found in poultry probiotic research. In chickens given lactobacilli, and then challenged with coccidia, oocyst shedding was reduced by as much as 75%. Cytokine levels and numbers of T cells were increased in the birds treated with lactobacilli. (49,50) Administration of probiotics to chickens can significantly increase antibody production, improve antibody titers achieved after vaccination, and increase local immune responses within the intestines. (51-55) Mononuclear cells in the cecal tonsil and spleen have been found to up-regulate immune system genes when exposed to Lactobacillus DNA and cell wall components. (56) Chickens fed a probiotic with multiple bacterial species showed a significant increase in goblet cells. (34) Goblet cells, with their production of the mucus layer in the intestinal tract, are thought to serve as a localized defense against pathogenic organisms as well as help repair damaged epithelial cells. (34,57) The study of probiotic effects on the immune system continues to be an active area of research in human, mammalian, and avian fields.

Ability to survive processing and storage

To be marketable, a probiotic organism must grow well in artificial media and then survive freeze-drying, storage, and reconstitution. Probiotics used in feed must be able to survive the storage conditions used for the feed and exposure to the feed itself. Because the efficacy of probiotics depends on delivery of live organisms at a determined dose level, the viability at the point of ingestion by the bird is very important. Probiotics need to be viability-tested for shelf life, storage conditions, and administration conditions.

Probiotic Benefits Documented in Birds

Disease prevention

Many studies in poultry have shown probiotics can prevent disease associated with administration of pathogenic organisms, reduce numbers of pathogenic organisms recovered from test birds, and reduce shedding of pathogenic organisms. (10,24,26,28,29,58-60) Most of these studies involved pretreatment with probiotics either before challenge or at the same time as challenge. In a comparison of probiotic pretreatment and treatment (probiotic given after challenge), pretreated birds showed much better survival and performance, although treatment provided some protection as well. In psittacine birds, the aforementioned study of a species-specific Lactobacillus given to cockatiels showed a significant reduction in potentially harmful gram-negative bacteria. (20) Several mechanisms of action described above are believed to combine to achieve the disease prevention abilities of probiotics. Researchers believe that other mechanisms of action will continue to be discovered.

Growth promotion

Improved growth rates are seen in chickens, turkeys, and cockatiels given probiotics. Reducing pathogenic organisms can help birds grow faster, but there are other mechanisms in play. Studies have shown that poultry with high numbers of certain urease-producing bacteria have reduced growth rates. Ammonia produced as a byproduct of ureolysis damages the intestinal mucosal cells. Lactobacilli have been shown to significantly decrease numbers of urease-producing bacteria, resulting in significantly better growth rates. (61) Probiotics also appear to improve digestion and absorption of nutrients, leading to better performance. (62,63) Digestive enzyme levels, such as amylase, have been found to increase significantly (64) and morphologic changes, including increased villus height and perimeter, intestinal muscle thickness, and crypt depth, have been shown with lactobacilli administration. (34,65,66) These morphologic changes are thought to increase the absorptive surface of the intestinal mucosa.

Multiple-Species Versus Single-Species Probiotics

There is considerable debate among probiotic researchers regarding the use of probiotics containing multiple species versus those containing a single species (primarily lactobacilli). When the Nurmi concept or CE concept was first discovered, researchers believed that a probiotic needed to mimic the full complement of native microflora to achieve competitive exclusion. (60, 67, 68) Studies using a single species of bacteria sometimes reported no significant effects. As more became known about lactobacilli and their properties, more studies focused on the use of lactobacilli alone, achieving very good results. (64,69-71) In the late 1990s, studies comparing effectiveness of different strains of various species of Lactobacillus have furthered the theory that a single-strain probiotic can be very effective if the Lactobacillus strain is carefully selected for positive traits. (25,26-27) However, some researchers believe that as mechanisms of action continue to be investigated, we will find that some bacterial species perform some functions whereas others perform other functions, all contributing to an overall beneficial effect. Currently multiple-species probiotics most frequently have some combination of lactobacilli (often a few different species or strains), Streptococcus species, Bifidobacterium species, Enterococcus species, and Bacillus species.

Recommendations for Probiotic Use

The body of literature concerning avian probiotics suggests that appropriate probiotic administration can both prevent gastrointestinal diseases and help mitigate existing infections. Prevention is much more effective than treatment, and recommendations in poultry are to give probiotics to newly hatched chicks to establish a healthy intestinal flora and promote development of intestinal immune defenses. In psittacine birds, parent birds feeding chicks in the nest provide normal flora as they feed their chicks. Appropriate probiotic use in parent birds may be indicated if their flora has been compromised. Hand-fed chicks do not receive normal flora from their parents, so probiotic administration would serve the same functions as it does in poultry chicks separated from the adults.

In psittacine birds, numbers of gram-negative bacteria increase with age while numbers of lactobacilli decrease with age. (15) This suggests that periodic treatment with a probiotic to replenish a normal microflora would be advisable, especially in pet birds with limited exposure to other members of their species.

Antibiotic treatment is known to eliminate normal flora in addition to the target pathogenic bacteria. One technique used in probiotic research to establish lactobacilli-free test subjects is to treat birds with various antibiotics prior to testing. (10,17) Probiotic use may be indicated after antibiotic treatment to reestablish normal flora.

Studies have shown that physiologic stress reduces the numbers of normal microflora and increases the numbers of abnormal or pathogenic organisms. (72-74) Stress also results in decreased intestinal immunity and damage to intestinal epithelium. (75-77) Because probiotics help stimulate local intestinal immunity, antibody production, and goblet cell population, their use in times of stress could help counteract these detrimental effects.

There is ample evidence that the appropriate application of probiotic organisms can provide significant benefits to birds. More research is needed to determine if bacterial strains can be found that adhere or colonize in multiple pet bird species. Because the commonly kept pet birds belong to hundreds of different species, it will be impractical to develop species-specific probiotics. Potential probiotic strains need to be screened and selected for positive traits, and minimum doses of viable organisms required to achieve desired results need to be determined. In vitro cell culture analysis of probiotic organisms has allowed rapid expansion of knowledge in the human, animal, and poultry fields. Development of similar techniques using tissues from psittacine birds would greatly facilitate the research that needs to be done.

Disclosure: The author is affiliated with Avian Health Products, producing species-specific probiotics.

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Jeanne Marie Smith, DVM

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