PROBIOTICS: BENEFITS AND EFFICIENCY IN POULTRY PRODUCTION

Ferreira, A.J.P.; Ferreira, C.A.; Petrella Neto, R.; Oliveira, D.R.; Nurmberger Júnior, R.; Lopes, V.C.B.A.

doi:10.1590/1808-1657v65n2p1391998

ABSTRACT

Several aspects related to the development and use of probiotics are presented in this study. The concepts, action mechanisms, efficiency in the chicken rate of growth with probiotics, control of enteric pathogens are approached with the purpose of elucidating the role of these bacteria in contrai and proliferation of the enteric microbiota and its relationship with the host and human being. Some of the main and/or newest approaches are discussed in this review.

KEY WORDS:
Probiotics; poultry production; poultry nutrition; chicken; poultry health

RESUMO

Vários aspectos relacionados ao desenvolvimento e uso de probióticos são apresentados neste estudo. Os conceitos, mecanismos de ação, eficiência no crescimento de aves, controle de patógenos entéricos são abordados com finalidade de elucidar a participação destas bactérias denominadas de probióticos na microbiota entérica das aves e sua relação com o hospedeiro e seres humanos. Algumas das principais e/ou mais recentes abordagens estão sendo discutidas nesta revisão.

PALAVRAS-CHAVE:
Probióticos; produção avícola; nutrição avícola; aves; sanidade

INTRODUCTION

The modem industry of animal food plays an outstanding role in the productivity and development of intensive animal breeding. The objective of animal breeding is high productivity at low cost for the breeder. This means inexpensive food and the best quality for consumers. This is achieved by converting the animal food energy into human foodstuffs.

The poultry production has reached high rates of growth based on two essential factors: an adequate and consistent supply of good quality animal food and disease contrai for keeping the bird in good health. As a result, there has been a broad development in the animal nutrition and animal health science.

Intestinal disorders, such as diarrhea, enteritis, coccidiosis, colibacillosis, bad absorption syndrome, cholera and salmonella infection are similar, because they result from deviations of the normal intestinal microbiota. Studies made in the last decades were not concerned about clarifying the role played by the bird intestinal microbiota, its composition and integrity, because they believed that the bird digestive tract would very little contribute to the overall nutrition. Today, it is known that the microbiota stability and maintenance are very important, as far as feeding and nutrition are concemed, for a good performance of chicken and poultry in general.

In poultry raising, additives are normally used to promote growth just as the antibiotics are. When intestinal disorders affect the poultry, some additives are used for treatment, such as: antibiotics, anticoccidial drugs, enzymes, probiotics and others. lt is known today that enzymes may play an important role in the nutrition of poultry. They are obtained from some cereais or can be produced by intestinal microorganisms. They provide for carbohydrate hydrolysis by increasing its water solubility and causing direct effects on the poultry performance. Generally, they are carbohydrases like glucanase, pectinase, cellulase, phytases and others (PARTRIDGE & WHYATT, 1995).

The aim of this review is to make a technical and scientific review on the use of probiotics and its effectiveness in the poultry performance. Researches have demonstrated that probiotics have become an innovative natural product with favorable effects for birds and consumers.

CONCEPTS

Probiotics are obtained from the culture of different bacterial species, their metabolites or combinations of yeasts and bacteria which are added to the food. The main objective of using probiotics is to stabilize and keep a certain bacterial population in the intestinal microbiota. The researches already done have nót been enough to elucidate the exact behavior of the animal microbiota or its foreign microorganisms, because of the intense change that may occur in this intestinal microbiota (FRETER et al., 1983). LEE (1985) checked four factors that might affect the stability of the intestinal microbiota ecosystem:

a) the diversity of microorganism species
b) the diversity of nutrients
c) the diversity of colonization
d) the resistance to colonization

a) the diversity of microorganism species increases with age, that is, the ecosystem of a grown-up bird is much more varied than that of a chick one day old. lt is because of this low diversity of intestinal microorganisms in the young birds that there is a greater incidence of enteric disturbances, because where there is a large number of bacterial species, there is a greater capacity of this ecosysten to compete with small changes. However, if this ecosystem changes, because of the presence of a pathogenic microorganism ora sudden feeding change, the diversity of bacterial species is reduced and the microorganism population becomes less stable.

b) Since many microorganisms prefer the sarne source of nutrients, there will be a diversity of species when the competition for these nutrients decreases. However, if one of these pathogenic microorganisms installs, the competition for the food will cause a reduction in diversity and, as a result, in the intestinal microbiota. Maybe there is not a competition for the food, but a contribution to the product of substrates that may favor digestion and increase the diversification of species. There is also the competition for nutrients between the bird and the installed microbiota. Microorganisms get used to the environment by competing with or taking advantage of it. However, microbiota acts in such a way that the bird may receive a better portion of ali the nutrients in the food. The relationship of microorganisms with the host is basically a competitive one and benefits the host when the bird's diet is highly digestible. The contrary occurs when the diet is less digestible, that is, the microorganism benefits from it. To obtain the energy used for growing, the bird's crop and intestinal microbiota break carbohydrates and produce lactic acid as an end product. The cecum microorganisms use the carbohydrates not digested by the host and produce volatile fatty acids. The amino acids are degraded in a different way through the intestinal tract. The bird's crop and cecum microbiota shows a slight trend towards degrading free lysin. That in the small intestine actively degrades lysin.

c) The diversity of colonization exists because of the great variation of chemical and physical conditions along the intestine. The microorganisms vary according to the type of nutrient and the pH that exists along the gastrointestinal, from the crop to the cloaca (FERKET, 1991). Oram-positive aerobic bacteria such as Lactobacillus and Streptococcus prevail in the bird's crop and intestine (FULLER, 1982). Other Oramnegative anaerobic bacteria, such as bacteroids and fusobacteria are present in the cecum and colon (SALINITRO, 1978).

d) The resistance to colonization is the capacity of the intestinal ecosystem to withstand the introduction of foreign organisms. A good nutrition produces a stable ecosystem that contributes to the health and growth of a bird. If there is a stable ecosystem, it will be more difficult to introduce pathogenic microorganisms. Some authors have already demonstrated that a young bird having a rnicrobiota that is little stable needs just one salmonella per 10g of food to cause infection in the first days of its life (SADLER et al., 1969, STUDART, 1984). Some components that may be added to the food, such as the probiotics, will influence the resistance to colonization.

ACTION MECHANISMS

The exact type of action of the probiotics is not yet known and most of them act because of the combination of several factors. We may consider four basic action mechanisms: competitive exclusion, production of antibiotics, production of organic acids and immunostimulation of resident cells. To obtain a competitive exclusion, birds are inoculated with sources of nonpathogenic bateria which will exclude harmful bacteria, thus providing prevention and making the digestive systen stable (WEINACK et al., 1985). Some specific species of lactic-acid producing bacteria compete with pathogens through a blockage of the microvillus edge receptors (KAUTZ, 1990). In addition, the probiotics protect the villus and the absorptive surface from irritating toxins produced by pathogenic organisms and also allow a regeneration of the injured intestinal mucosa (DOBROOOSZ et al., 1991).

The antibiotic producing probiotics act particularly against Salmonella sp., Shigella sp., Staphylococcus sp., Proteus sp. and Bacillus sp. Several species of lactobacillus, particularly L. acidophilus produce antibiotics known as acidolin and lactocidin; L. plantarum produces lactolin; Enterococcus faecium produces nisin and diplococcin (FOX, 1988). L. reuteri, found in the bird rnicrobiota (SARRA et al., 1985; DURHAMSE et al., 1994), produces reuterin (3- hydroxipropionaldehyde) which inhibits the growth of Salmonella sp., Campylobacter sp., Listeria sp. and Escherichia coli (TALARICO & DOBROGOSZ, 1990). The bacterial production of acetic and lactic acids reduces the intestinal pH, thus creating unfavorable conditions for the growth of pathogenic bacteria, besides acting on Oram-negative bacteria (KAUTZ, 1990). The lactobacillus species are very efficient in the production of lactic acid from the fermentation of glucose. Streptococcus and Pediococcus are good producers of organic acids while the bacilli and yeasts do not show the sarne metabolic capacity that originates these acids. Fatty acids produced in the cecum of birds that received lactose and probiotics acted effectively on S. typhimurium (ZIPRIN et al., 1990, CORRIER et al., 1990a, HINTON et al., 1990; CORRIER et al., 1990).

lt is believed that the immnostimulation may be one of the action mechanisms of probiotics, although it is not known exactly how these bacteria would act on the stimation of the bird's immune system (VELD et al., 1994). It is known that a balanced rnicrobiota is essential for an efficient immunocompetence of the birds. PERDIOON et al. (1990) reported that the oral administration of lactic-acid producing bacteria. increased the immunity of the intestinal mucosa or the production of lgA in response to enteropathogenic rnicroorganisms. These authors also found that some probiotics can accelerate the phagocytic function of the reticuloendothelial system. SPF birds (specific pathogen free) have a very small number of intraepithelial lymphocytes, plasma cells and Peyer plaques (KAUTZ, 1990). The yeasts act by multiplying themselves and producing nutritive metabolites. These metabolites, whose growth is optirnized during the culture, are responsible for increasing the performance (HIGGINBOTHAM,1991).

TYPES OF PROBIOTICS

A large number of probiotics are found in the US and European markets. However, there are few manufacturers of this product in Brazil, because of, to some extent, the high cost of its application and, possibly, probiotics are not widely used in our country. Probiotics are generally made up of simple live microorganisms or a combination of them.

Micoorganisms used in probiotics: Bacteria:

Lactobacillus acidophilus Lactobacillus subtilis strain natto Lactobacillus plantarum Lactobacillus casei

Lactobacillus lactis Lactobacillus bulgaris Bacillus subtilis Bacillus lincheniformis Bacillus toyoi Pediococcus sp.

Rhodopseudomonas sp. Enterococcus faecium Enterococcus faecalis Yeasts:

Saccharomyces cerevisae Torulopsis candida Rhodotorula rubra

EFFICIENCY - HOW TO DETERMINE

There are some difficulties to reach full probiotic efficiency. At present, the use of this product tends to be an empirical process, despite the evolution of researches in the last decade. There are some factors responsible for the probiotic effectiveness. The ideal probiotic should not contain microorganisms harmful to the birds and other animal species. The· above microorganisms already show an acceptable action.

The microorganisms should be capable of growing in the bird's intestine, colonizing the wall or growing in the intestinal fluids. The lactic acid producing bacteria (lactobacillus, enterococcus and pediococcus) adapt themselves to the intestinal microbiota. The bacilli and yeasts are almost never used, because the bacilli are strictly aerobic and may not colonize the intestine and be eliminated by the bird. Usually, the yeasts do not constitute the normal intestinal flora and may face difficulties to colonize it. The yeasts have been recognized as a source of proteins, vitamins and minerais with a considerable nutritional value. Microorganisms must be stable in food mixtures, particularly during a pelletization. Most of the lactobacillus species cannot stand the pelletization temperatures (70-80ºC). Some enterococci are a little more resistant, despite being unable to withstand, in a satisfactory manner, temperatures around 70ºC. The development of heat resistant species is possible.

The presence of antibiotics (growth promoters) in the food may inactivate the various probiotic bacterial species. As a result, "in vitro" tests shoud be run to evaluate the inhibiting effects of these growth promoters and establish possible conjugation of antibiotic and probiotic. It is obvious that the bacteria resistance may increase with the use of certain antibiotics.

HOW TO SELECT A PROBIOTIC

The selection of the most efficient, accessible and easier to use samples is being developed. The researches are based on "in vitro" and "in vivo"simulations to reach results that suit the current poultry production, that is, having favorable effects that may promote a microbiota balance in the host (HAVENARR & VELD, 1992). The selection parameters are also being assessed considering human health. In the future, there may be divisions of probiotics categories, that is, certain probiotic are specific to increase the resistance of the eggshell, others to increase the weight gained by poultry chickens for meat production and also to control a specific disease.

DISEASE CONTROL

Recent researches have explained the interference and/or effects of probiotics on diseases by controlling them and even explaining them. There are large-scale records of various effects caused by probiotics on salmonellae; CORRIER et al. (1993) challenging poultry chickens with Salmonella typhimurium which had been previously treated with a mixture of gram-positive and negative bacteria and dietetic lactose (fermentation substrate, found that the number of cecum salmonellas decreased considerably, there being a reduction of these microorganisms in 55% of the chickens. The addition of bifidobacteria and fructoligossacharides in animal food has resulted in an increased weight and also a protection against the colonization of salmonellas (MCKELLAR et al., 1993).

The use of bacterial cultures, which act on chickens by a competitive exclusion, causes a significant reduction in the prevalence of salmonella in the carcass (BLANKENSHIP et al., 1993; HIRN et al., 1992; FUKATA et al., 1993; BLANKENSHIP et al., 1991; CANTOR, 1990). Other researches have also shown the protective effect of probiotics on chickens against salmonella and their effectiveness at the field levei (STAVRIC, 1992; JOHNSON, 1992; MULDER, 1991). Certain competitive-exclusion products like Broilact and Aviguard prove to be very efficient in the prevention of intestinal colonization by Salmonella enteritidis phage type 4 (CAMERON & CARTER, 1992; NUOTIO et al., 1992); SCHNEITZ et al., 1991). The number of S. enteritidis phage type 13a was quickly reduced in poultry chicken with the association of five additives, namely, lactobacillus, lactose, organic acids, various probiotics and egg dust (OPITZ et al., 1993).

The production of organic acid by the bird normal microbiota using just lactose in the food has shown a protective effect, preventing the colonization of S. enteritidis (CORRIER et al., 1993). The use of some antibiotics (avoparcin, bacitracin, flavomicin, virginiamicin) in chickens protected by a grown-up bird's cecum microbiota was not effective in the elimination of S. typhimurium, while the birds that did not receive antibiotics in their food had a better result if they were associated with probiotics (HUMBERT et al., 1991). BABA et al. (1991) obtained positive results when treating birds with grown-up bird's cecum microbiota containing E.coli, as well as lactobacillus. The mixture of the two microorganisms was the most efficient to fight S. typhimurium, E. coli probably plays an important role in the competitive exclusion of certain bacteria. VANDEVOORDE et al. (1991) showed the lactobacillus antagonism against enterobacteria and S. typhimurium and attributed this to the production of lactic acid. However, contrary to salmonellas, lactobacilli are sensitive to the action of biliary salts. CORRIER et al. (1991), defying turkeys with Salmonella Senftenberg and using four treatments with anaerobic cecum cultures and/or with different proportions of lactose, obtained similar protection against salmonella in all the groups when they were compared with control groups. CORRIER et al. (1990) and CORRIER et al. (1990a) challenged four chicken groups with S. typhimurium, which had previously received lactose, and noticed an intense production of volatile fatty acids followed by a cecum pH reduction and, as a result, the inhibition of the salmonella colonization. A similar experiment carried out by HINTON et al. (1990) showed that chickens that received lactose in association with anaerobic bacteria achieved better results in the fight against S. typhimurium than chickens that had received lactose or bacteria separately.

HINTON et al. (1991) orally administered anaerobic cecum cultures and supplied food treated with organic (formic and propionic) acids for chickens. The birds were challenged with S. enteritidis phage type 4 that can withstand these organic acids. The experiment showed that a competitive exclusion protected the birds against infection, reducing the number of cecum salmonellas from 82% to 8%. Also, hepatic infection decreased from 15% to 13%. GUILLOT & YVORE (1990) proved that Bacillus IP 5832 (Paciflor) caused an increase in the resistance of chickens challenged with Eimeria tenella, but an effective control was not achieved against S. typhimurium.

Poultry chickens with necrotic enteritis showed remarkable recovery when treated with Broilact and also a considerable reduction in the number of Clostridium in bird feces (ELWINGER et al., 1992). KMET et al. (1993) studied the inhibition of Clostridium sp. from poultry origin and pathogenic E. coli by enterococcus and organic acids. They found that there is a remarkable drop of Clostridium sp. when acid formic is used in the 0.25% concentration. STERN et al. (1991) showed that the competitive exclusion was efficient to control Campylobacter jejuni.STANLEY et al. (1993) found that it is efficient to use Saccharomyces cerevisiae in the reduction of afflatoxicosis in poultry chickens. This was proved by the restoration of activities by some hepatic enzymes and by an increase in the concentration of albumin and total proteins.

COMBINATIONS OF PROBIOTICS WITH OTHER ADDITIVES

Some researches have covered the associations of probiotics with anticoccidial drugs, growth promoting antibiotics and others. However, other studies are required, because experiments so far developed have not shown conclusive results. RADA et al. (1994) studying the susceptibility of actobacillus probiotics associated with three different coccidiostatic products (monensin, maduramicin and robenidin) found that the bacterial growth had been partially inhibited by monensin. The lactobacillus samples were more susceptible to monensin and resistant to robenidin. The results indicate that the probiotics containing lactobacilli may only be combined with specific coccidiostatic products.

The use of Bacillus subtilis did not prove to be efficient when used in association with antibiotics (bacitracin and streptomycin) in female turkeys from 12 to 16 weeks of age. In this case, antibiotics increased their body weight and feeding efficiency (JIRAPHOCAKUL et al., 1990). On the other hand, a second experiment with male turkeys 20 weeks old showed that their body weight and feeding efficiency improved with the use of B. subtilis. Another experiment made by FETHIERE et al. (1987) associated an antibiotic and probiotic in the food of Cobb male chickens. It was found that their normal weight was not affected by the treatment. However, the food conversion improved with the use of antibiotics or in a ocmbination with a probiotic.

POULTRY PRODUCTION EFFECTS

Positive aspects in productivity, food conversion, gain in weight, food conversion and gain in weight have been found in recent researches. This is possible because of some mechanisms that lead to the utilization of food. For example, the probiotics and antibiotics increase the utilization of proteins by decreasing the nitrogen losses, increasing the dry fecal matter and metabolism. This results in a better use of the food and efficiency in the performance of birds (MORGAN & MUL, 1993, WENK, 1990). Poduction may also benefit from this, because the probiotics act as natural promoters, besides improving the health of birds in general (CHAPMAN, 1988). GIPPERT & BODROGI (1992) supplemented duck (Pekin) diets with a probiotic and found that the supplement had no effect on the mortality rate, but the body weight and food consumption increased while the feeding conversion decreased. A study by NAHASHON et al. (1994) showed that the phytease activity increased in all the diets that received lactobacillus. No difference was noticed in the calcium retention. However, a greater phosphorus retention was noticed in birds on a diet containing probiotic.

CAVAZZONI et al. (1993) conducted a comparative study between the antibiotic (avoparcin) and probiotic (B. coagulans) administered in poultry chickens and found out that there was no significant effect in the daily gain in weight. The food conversion was 9% better in the groups that received avoparcin, and also better in 6% for those that received probiotic. Another comparative study of an antibiotic and probiotic conducted by KHAN et al. (1992) showed that the gain in weight and the food consumption were less and the food conversion was greater in the groups that received probiotic supplement.

A study conducted by HUSSEIN & EL-ASHRY (1991) indicates that the addition of lactobacillus as a supplement to chicken food caused an increase in the daily gain in weight and efficient food conversion, as well as a reduction inthe occurrence of diarrhea and mortality.

The use oflactobacillus in egg-laying hens promoted a good performance (JADHAV et al., 1992), because the birds that receiv food with a greater quantity of probiotic produced a larger percentage of eggs. The gain in weight and egg weight were not affected. HAYAT et al. (1993) examined the reproductive performance of turkey hens that received yeast (S. cerevisiae) in their food and concluded that the supplementation made it possible to notice positive effects such as the reduction of embryo mortality, increase of fertile eggs and increase in the egg production.

HUMAN ASPECTS

Meat and egg production stands in the industrial poultry raising as the most important and growing segment. Because of the positive association of these two characteristics, animal nutrition is extremely relevant in bird development and performance. The use of probiotics in animal food as an innovative factor of today's technologies brings new expectations regarding their benefits. The human population that consumes these animal products is becoming more demanding each day and may have highly safe products in hand that will not cause any adverse reaction to the organism when, by any chance, probiotic praducts are used in lieu of traditional antibiotics (HEADON, 1992). The studies currently being conducted are supplying positive factors regarding the carcass quality and the reduction or elimination of prabable medicine residues in the meat and eggs to be consumed by the population. JORGENSEN (1988) found in his work some advantages in the use of prabiotics instead of antibiotics. One of them was the absence of carcass residues.

JUVEN et al. (1991) have been finding favorable effects in the use of lactobacillus and pediococcus to control enteropathogenic bacteria. There are coherent and remarkable reasons for selecting samples ofthese nonpathogenic microorganisms which are part of the normal bird's microbiota, because these probiotics produce braad-spectrum antagonic samples which act particularly on species that are pathogenic to man. OWINGS et al. (1990) compared the use of antimicrobial and probiotic products (Enterococcus faecium) in chickens and found that, in the experiments in which probiotics were used, the results were much more favorable. A feeding conversion and body weight impravement can be seen without significant chages in the yield, composition or characteristics of the carcass. Populating the cecum with Enterococcus faecium was more efficient in comparison with birds that received an antibiotic diet. Effects on the reduction of the bird's blood cholesterol leveis have been found. As a result, it also drops in the meat. There is also a reduction of malign neoplasias, possibly inhibiting enzymes that convert procarcinogens into carcinogens (VELD et al., 1994) when probiotics are used in humans (PEITERSEN, 1992; O' SULLIVAN et al., 1992; MITSUOKA, 1991).

CONCLUDING REMARKS

The main purpose of poultry raising is productivity associated with product quality. The main points for this success is feeding, sanitation and genetic potential of each bird species and lineage. The probiotics arrive as a revolutionary and natural product bringing important benefits, such as disease contrai and performance increase, without causing potential damages to consumers.

Good nutrition is responsible for the stability of the intestinal microbiota that promotes bird health and growth. When it has a stable ecosystem, there is no multiplication of pathogenic micraorganisms.

The probiotics do not act basically as competitive exclusion, but by increasing natural antibiotic praduction, praduction of organic acids and immunostimulation. The pracessing and use of probiotics is still regarded as an empirical factor which, sometimes, restricts the use of these products in animal production. It is important to note the probiotic action thraugh a defined (known bacteria) and undefined (unknown bacteria) micrabiota on Salmonella enteritidis and Salmonella typhimurium which allows the elimination of these bacteria from the carcass.

The association with other additives is still little known for a replacement of antibiotics when their use is carried out in a preventive way and the antibiotics are used for treatment of certain infectious diseases. The use of these praducts allows the reduction of residues in the carcass, besides other very relevant benefits, such as the contrai of salmonellosis, cholesterol reduction, production of anticarcinogenic and immunostimulation substances and greatly potentiate the bird vaccination pragrams.

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JADHAV, N. V.; SIDDIQUI, M. F.; SAKHARE, P. G. Effect of probiotic feeding on the performance of pullets. Indian J. Poult. Sei., v. 27, p. 163-164,1992.
JIRAPHOCAKUL, S.; SULLIVAN, T. W.; SHAHANI, K. M. Influence of a dried Baeillus subtilis culture and antibiotics on performance and intestinal microflora in. turkeys. Poult. Sei., v.69,p. 1966-1973, 1990.
JOHNSON, C. T. the use of antimicrobial and competitive exclusion combination in salmonellainfected pullet flocks. Int. J.. Food Microbial., v. 15,p.293-298, 1992.
JORGENSEN, M. Probiotic - a survey. An altemative to antibiotics in the feed of fur-bearing animais? Seientifur, v. 12, p. 247-249, 1988.
JUVEN, B. J.; MEINERSMANN, R. J.; STERN, N. J. Antagonistic effects of lactobacilli and pediococci to control intestinal colonization by human enteropathogens in live poultry. J. Appl. Bacteriol., v. 70, p. 95-103, 1991.
KAUTZ, W. Probiotics versus antibiotics - their functional difference. In: ANNUAL NORTH CAROLINA POULTRY NUTRITION CONFERENCE, 17., 1990, Charlotte-USA. Proceedings. p. 72-86.
KHAN, M. L.; ULLAH, I.; JAVED, M.T. Comparative study of probiotics, T. M. 50 Biovin-40 and Albac on the performance of broiler chicks. Pakist. Vet. J., v. 12, p. 145-147, 1992.
KMET, V.; STACHHOVA, M.; NEMCOVA, R.; JONECOVA, Z.; LAUKOVA, A. The interaction of intestinal microflora with avian enteric pathogens. Acta Vet. Brno, v. 62, p. S87-89, 1993.
LEE, A. Neglected Niches: The Microbial Ecology of the Gastrointestinal Tract. Adv. Microb. Ecol., v.8,p. 115-162, 1985.
MCKELLAR, R. C.; MODLER, H. W.; MULLIN, J. Characterization of growth and inulinase production by Bifidobacterium sp. on fructooligosaccharides. Bifidobacteria Microflora, v. 12, p. 75-86, 1993.
MITSUOKA, T. Beneficial microbial aspects (probiotics). In: INTERNATIONAL DAIRY CONGRESS, 23., 1991, Montreal - Canada. Proceedings. Montreal: International Dairy Federation, 1991. p. 1226-1237.
MORGAN, A. J. & MUL, A. J. Biotechnology on feed utilization. In: WORLD CONFERENCE ON OILSEED TECHNOLOGY AND UTILIZATION, 1993, Champaign - USA. Proceedings. Champaign: American Oil Chemists' Society, 1993. p. 359-364.
MULDER, R. W. A.<W. Probiotics as a tool against salmonella c_ombination. Misset World Poult., v. 7, p. 36-37, 1991.
NAHASHON, S. N.; NAKAUE, H. S.; MIROSH, L. W. Phitase activity, phosphorus and calcium retention, and performance of Single Comb White Leghom layers fed diets containing two leveis of avaiable phosphorus and supplemented with direct-fed-microbials. Poult. Sei., v. 73, p. 1552-1562, 1994.
NUOTIO, L.; SCHNEITZ, C.; HALONEN, U.; NURMI, E. Use of competitive exclusion to protect newly-hatched chicks against intestinal colonization and invasion by Salmonella enteritidis PT4. Br. Poult. Sei., v. 33, p. 775-779, 1992.
OPITZ, H. M.; EL-BEGEARMI, M.; FLEGG, P.; BEANE, D. Effectveness of five additives in chicks infected with Salmonella enteritidis phage type 13a. J. Appl. Poult. Res., v. 2, p. 147-153, 1993.
O'SULLIVAN, M. G.; THORNTON, G.; O'SULLIVAN, G. C.; COLLINS, J. K. Probiotic bacteria: myth or reality? Trends Food Sei. Technol., v. 3, p. 309-314, 1992.
OWINGS, W. J.; REYNOLDS, D. L.; HASIAK, R. J.; FERKET, P. R. Influence of dietary supplementation with Streptococcus faeeium M-74 on broiler body weight, feed conversion, carcass characteristics and intestinal microbial colonization. Poult. Sei., v. 69, p. 1257-1264, 1990.
PARTRIDGE, G. & WYATT, C. More flexibility with new generation of enzimes. World Poult., v. 46, p. 17-21, 1995.
PEITERSEN, N. Probiotic starter cultures for food products. In: In: LES BACTERIES LACTIQUES: ACTES DU COLLEQUE LACTIC 91, 1991, Caen - France. Actes. Caen: Centre de Publications de L' Universite de Caen, 1991. p. 227-233.
PERDIGON, G. S.; ALVAREZ; NADER DE MACIAS, M. E.; FOUX, M. E.; RUIZ HOLGADO, A. P. The oral administration of latie acid bacteria increase the mucosal intestinal immunity in response to enteropathogens. J. Food Prot., v. 53,p.404-410, 1990.
RADA, V.; RYCHLY, I.; VORISEK, K. Susceptibility of chicken intestinal lactobacilli to coccidiostats. Acta Vet. Brno, v. 63, p. 9-12, 1994.
SADLER, W.W.; BROWNELL, J. R.; FANELLI, M. J. Influence of age and inoculum levei on shed pattem of Salmonella typhimurium in chickens. Avian Dis., v. 13, p. 793-803, 1969.
SALINITRO, J. P.; BLAKE, I. G.; MUIRHEAD, P. A.; MAGLIO, M.; GOODMAN, J. R. Bacteria isolated from the duodenum, ileum and cecum of young chicks. Appl. Environ. Microbiol., v. 35, p. 782, 1978.
SARRA, P. G.; DELLAGLIO, F.; BOTTAZZI, B. Taxonomy of Lactobacilli isolated from the alimentary of chickens. System. Appl. Microbiol., v.6,p.86-89, 1985.
SCHNEITZ, C.; NUOTIO, L.; KIISKINEN, T.; NURMI, E. Pilot-scale testing of the competitive exclusion method in chickens. Br. Poult. Sei., v. 32, p. 881-884, 1991.
STANLEY, V. G.; OJO, R.; WOLDESENBET, S.; HUTCHINSON, D. H.; KUBENA, L. S. The use of Saccharomyces cerevisiae to suppress the effects of aflatoxicosis in broiler chicks. Poult. Sei., V. 72, p. 1867-1872, 1993
STAVRIC, S. Defined cultures and prospects. Int. J. Food Microbial., v. 15, p. 245-263, 1992.
STERN N. J.; COX, N. A.; BAILEY, J. S.; BLANKENSHIP, L. C.; MUSGROVE, M.; WILLIAMS, O. Update on Puerto Rico triai assessing efficacy of mucosal competitive exclusion (MCE) flora to contrai Campylobacter jejuni. Poult. Sei., v. 70, p. 117-119, 1991.
STUART. J. C. Agricultural group symposium. Prospects for the control of Salmonella sp. in the poultry industry. The intruduction of Salmonella sp. into poultry flocks. J. Sei. Food. Agric., v. 35, p. 632-639, 1984.
T ALARICO, T. L.; DOBROGOSZ, W. J. Purification and characterization of glycerol dehydratase from Lactobacillus reuteri. Appl. Environ. Microbial., v.56,p. 1195-1197, 1990.
V ANDEVOORDE, L.; CHRISTIAENS, H.; VERSTRAETE, W. In vitro apprasial of the probiotic value of intestinal lactobacilli. World J. Microbial. Biotechnol., v. 7, p. 587-592, 1991.
VELO, J. H. J.; HAVENAAR, R.; MARTEAU, P. Establishing a scientific basis for probiotic R & D. Trends Biotechnol., v. 12, p. 6-8, 1994.
WEINACK, O. M.; SNOEYENBOS, G. H. SOERJADI-LIEM, A. S. Further studies on competitive exclusion of Salmonella typhimurium by lactobacilli in chickens. Avian Dis., v. 29, p. 1273-1276, 1985.
WENK, C. Yeast culture, lactobacilli and a mixture of enzimes in diets for growing pigs and chickens under Swiss conditions: influence on the utilization of the nutrients and energy. In: BIOTECHNOLOGY IN THE FEED INDUSTRY. ALLTECH'S ANNUAL SYMPOSIUM, 6., 1990, Nicholasville-USA. Proceedings. Nicholasville: Alltech Technical, 1990. p. 315-330.
ZIPRIN, R. L.; CORRIER, D. E.; HINTON, A. JR.; BEIER, R. C.; SPATES, G. E.; DELOACH, J. R.; ELISSALDE, M. H. Intracloacal Salmonella typhimurium infection of broiler chikens: reduction of colonization with anaerobic organisms and dietary lactose. Avian Dis., v. 34, p.749-753, 1990.

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10 Feb 2025
Date of issue
Jul-Dec 1998

History

Received
19 Aug 1998

This is an article published in open access under a Creative Commons license.

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[29] HINTON, M.; MEAD, G. C.; IMPEY, C. S. Protection of chicks against environmental challenge with Salmonella enteritidis by competitive exclusion and acid-treated feed. Lett. Appl. Microbial., v. 12, p. 69-71, 1991.

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[31] HUMBERT, F.; LALANDE, F.; L'HOSPITALIER, R.; SALVAT, G.; BENNEJEAN, G. Effect of four antibiotic additives on the salm'onella contamination of chicks protected by an adult caecal flora. Avian Pathol., v. 20, p. 577-584, 1991.

[32] HUSSEIN, H. H. & EL-ASHRY, M.A. Some studies on the beneficial effects of lactobacillus concentrate supplementation on broiler performance. Egypt. J. Anim. Prod., v. 28, p. 85-91, 1991.

[33] JADHAV, N. V.; SIDDIQUI, M. F.; SAKHARE, P. G. Effect of probiotic feeding on the performance of pullets. Indian J. Poult. Sei., v. 27, p. 163-164,1992.

[34] JIRAPHOCAKUL, S.; SULLIVAN, T. W.; SHAHANI, K. M. Influence of a dried Baeillus subtilis culture and antibiotics on performance and intestinal microflora in. turkeys. Poult. Sei., v.69,p. 1966-1973, 1990.

[35] JOHNSON, C. T. the use of antimicrobial and competitive exclusion combination in salmonellainfected pullet flocks. Int. J.. Food Microbial., v. 15,p.293-298, 1992.

[36] JORGENSEN, M. Probiotic - a survey. An altemative to antibiotics in the feed of fur-bearing animais? Seientifur, v. 12, p. 247-249, 1988.

[37] JUVEN, B. J.; MEINERSMANN, R. J.; STERN, N. J. Antagonistic effects of lactobacilli and pediococci to control intestinal colonization by human enteropathogens in live poultry. J. Appl. Bacteriol., v. 70, p. 95-103, 1991.

[38] KAUTZ, W. Probiotics versus antibiotics - their functional difference. In: ANNUAL NORTH CAROLINA POULTRY NUTRITION CONFERENCE, 17., 1990, Charlotte-USA. Proceedings. p. 72-86.

[39] KHAN, M. L.; ULLAH, I.; JAVED, M.T. Comparative study of probiotics, T. M. 50 Biovin-40 and Albac on the performance of broiler chicks. Pakist. Vet. J., v. 12, p. 145-147, 1992.

[40] KMET, V.; STACHHOVA, M.; NEMCOVA, R.; JONECOVA, Z.; LAUKOVA, A. The interaction of intestinal microflora with avian enteric pathogens. Acta Vet. Brno, v. 62, p. S87-89, 1993.

[41] LEE, A. Neglected Niches: The Microbial Ecology of the Gastrointestinal Tract. Adv. Microb. Ecol., v.8,p. 115-162, 1985.

[42] MCKELLAR, R. C.; MODLER, H. W.; MULLIN, J. Characterization of growth and inulinase production by Bifidobacterium sp. on fructooligosaccharides. Bifidobacteria Microflora, v. 12, p. 75-86, 1993.

[43] MITSUOKA, T. Beneficial microbial aspects (probiotics). In: INTERNATIONAL DAIRY CONGRESS, 23., 1991, Montreal - Canada. Proceedings. Montreal: International Dairy Federation, 1991. p. 1226-1237.

[44] MORGAN, A. J. & MUL, A. J. Biotechnology on feed utilization. In: WORLD CONFERENCE ON OILSEED TECHNOLOGY AND UTILIZATION, 1993, Champaign - USA. Proceedings. Champaign: American Oil Chemists' Society, 1993. p. 359-364.

[45] MULDER, R. W. A.<W. Probiotics as a tool against salmonella c_ombination. Misset World Poult., v. 7, p. 36-37, 1991.

[46] NAHASHON, S. N.; NAKAUE, H. S.; MIROSH, L. W. Phitase activity, phosphorus and calcium retention, and performance of Single Comb White Leghom layers fed diets containing two leveis of avaiable phosphorus and supplemented with direct-fed-microbials. Poult. Sei., v. 73, p. 1552-1562, 1994.

[47] NUOTIO, L.; SCHNEITZ, C.; HALONEN, U.; NURMI, E. Use of competitive exclusion to protect newly-hatched chicks against intestinal colonization and invasion by Salmonella enteritidis PT4. Br. Poult. Sei., v. 33, p. 775-779, 1992.

[48] OPITZ, H. M.; EL-BEGEARMI, M.; FLEGG, P.; BEANE, D. Effectveness of five additives in chicks infected with Salmonella enteritidis phage type 13a. J. Appl. Poult. Res., v. 2, p. 147-153, 1993.

[49] O'SULLIVAN, M. G.; THORNTON, G.; O'SULLIVAN, G. C.; COLLINS, J. K. Probiotic bacteria: myth or reality? Trends Food Sei. Technol., v. 3, p. 309-314, 1992.

[50] OWINGS, W. J.; REYNOLDS, D. L.; HASIAK, R. J.; FERKET, P. R. Influence of dietary supplementation with Streptococcus faeeium M-74 on broiler body weight, feed conversion, carcass characteristics and intestinal microbial colonization. Poult. Sei., v. 69, p. 1257-1264, 1990.

[51] PARTRIDGE, G. & WYATT, C. More flexibility with new generation of enzimes. World Poult., v. 46, p. 17-21, 1995.

[52] PEITERSEN, N. Probiotic starter cultures for food products. In: In: LES BACTERIES LACTIQUES: ACTES DU COLLEQUE LACTIC 91, 1991, Caen - France. Actes. Caen: Centre de Publications de L' Universite de Caen, 1991. p. 227-233.

[53] PERDIGON, G. S.; ALVAREZ; NADER DE MACIAS, M. E.; FOUX, M. E.; RUIZ HOLGADO, A. P. The oral administration of latie acid bacteria increase the mucosal intestinal immunity in response to enteropathogens. J. Food Prot., v. 53,p.404-410, 1990.

[54] RADA, V.; RYCHLY, I.; VORISEK, K. Susceptibility of chicken intestinal lactobacilli to coccidiostats. Acta Vet. Brno, v. 63, p. 9-12, 1994.

[55] SADLER, W.W.; BROWNELL, J. R.; FANELLI, M. J. Influence of age and inoculum levei on shed pattem of Salmonella typhimurium in chickens. Avian Dis., v. 13, p. 793-803, 1969.

[56] SALINITRO, J. P.; BLAKE, I. G.; MUIRHEAD, P. A.; MAGLIO, M.; GOODMAN, J. R. Bacteria isolated from the duodenum, ileum and cecum of young chicks. Appl. Environ. Microbiol., v. 35, p. 782, 1978.

[57] SARRA, P. G.; DELLAGLIO, F.; BOTTAZZI, B. Taxonomy of Lactobacilli isolated from the alimentary of chickens. System. Appl. Microbiol., v.6,p.86-89, 1985.

[58] SCHNEITZ, C.; NUOTIO, L.; KIISKINEN, T.; NURMI, E. Pilot-scale testing of the competitive exclusion method in chickens. Br. Poult. Sei., v. 32, p. 881-884, 1991.

[59] STANLEY, V. G.; OJO, R.; WOLDESENBET, S.; HUTCHINSON, D. H.; KUBENA, L. S. The use of Saccharomyces cerevisiae to suppress the effects of aflatoxicosis in broiler chicks. Poult. Sei., V. 72, p. 1867-1872, 1993

[60] STAVRIC, S. Defined cultures and prospects. Int. J. Food Microbial., v. 15, p. 245-263, 1992.

[61] STERN N. J.; COX, N. A.; BAILEY, J. S.; BLANKENSHIP, L. C.; MUSGROVE, M.; WILLIAMS, O. Update on Puerto Rico triai assessing efficacy of mucosal competitive exclusion (MCE) flora to contrai Campylobacter jejuni. Poult. Sei., v. 70, p. 117-119, 1991.

[62] STUART. J. C. Agricultural group symposium. Prospects for the control of Salmonella sp. in the poultry industry. The intruduction of Salmonella sp. into poultry flocks. J. Sei. Food. Agric., v. 35, p. 632-639, 1984.

[63] T ALARICO, T. L.; DOBROGOSZ, W. J. Purification and characterization of glycerol dehydratase from Lactobacillus reuteri. Appl. Environ. Microbial., v.56,p. 1195-1197, 1990.

[64] V ANDEVOORDE, L.; CHRISTIAENS, H.; VERSTRAETE, W. In vitro apprasial of the probiotic value of intestinal lactobacilli. World J. Microbial. Biotechnol., v. 7, p. 587-592, 1991.

[65] VELO, J. H. J.; HAVENAAR, R.; MARTEAU, P. Establishing a scientific basis for probiotic R & D. Trends Biotechnol., v. 12, p. 6-8, 1994.

[66] WEINACK, O. M.; SNOEYENBOS, G. H. SOERJADI-LIEM, A. S. Further studies on competitive exclusion of Salmonella typhimurium by lactobacilli in chickens. Avian Dis., v. 29, p. 1273-1276, 1985.

[67] WENK, C. Yeast culture, lactobacilli and a mixture of enzimes in diets for growing pigs and chickens under Swiss conditions: influence on the utilization of the nutrients and energy. In: BIOTECHNOLOGY IN THE FEED INDUSTRY. ALLTECH'S ANNUAL SYMPOSIUM, 6., 1990, Nicholasville-USA. Proceedings. Nicholasville: Alltech Technical, 1990. p. 315-330.

[68] ZIPRIN, R. L.; CORRIER, D. E.; HINTON, A. JR.; BEIER, R. C.; SPATES, G. E.; DELOACH, J. R.; ELISSALDE, M. H. Intracloacal Salmonella typhimurium infection of broiler chikens: reduction of colonization with anaerobic organisms and dietary lactose. Avian Dis., v. 34, p.749-753, 1990.