Application of Prebiotics and Probiotics in Poultry Production1
J. A. Patterson2and K. M. Burkholder
Department of Animal Sciences, Purdue University, West Lafayette, Indiana 47907
immune system provide resistance to enteric pathogens.
Recent data suggest that resistance is not solely due to
the sum of the components, but that cross-talk between
these components is also involved in modulating this
resistance. Inhibition of pathogens by the intestinal mi-
crobiota has been called bacterial antagonism, bacterial
interference, barrier effect, colonization resistance, and
competitive exclusion. Mechanisms by which the indige-
nous intestinal bacteria inhibit pathogens include compe-
duction of toxic compounds, or stimulation of the im-
mune system. These mechanisms are not mutually
exclusive, and inhibition may comprise one, several, or
has been associated with improved health, and lactic acid
The intestinal microbiota, epithelium, and
(Key words: intestinal microbiota, poultry, prebiotic, probiotic)
2003 Poultry Science 82:627–631
and the associated contamination of poultry products for
human consumption (human food safety). With increas-
ingconcerns aboutantibiotic resistance,the banon subth-
erapeutic antibiotic usage in Europe and the potential for
a ban in the United States, there is increasing interest in
finding alternatives to antibiotics for poultry production.
Prebiotics and probiotics are two of several approaches
that have potential to reduce enteric disease in poultry
and subsequent contamination of poultry products. Pro-
2000), has been defined as “a live microbial feed supple-
ment which beneficially affects the host animal by im-
proving its intestinal balance” (Fuller, 1989). Prebiotics
are defined as “a nondigestible food ingredient that bene-
ficially affects the host by selectively stimulating the
growth and/or activity of one or a limited number of
2003 Poultry Science Association, Inc.
Received for publication September 8, 2002.
Accepted for publication January 27, 2003.
1Paper 16972 of the Purdue University Agricultural Programs.
bacteria (lactobacilli and bifidobacteria) have been impli-
cated as the causative agents for this improved health.
Research over the last century has shown that lactic acid
bacteria and certain other microorganisms can increase
resistance to disease and that lactic acid bacteria can be
drates. Increased bacterial resistance to antibiotics in hu-
mans has caused an increase in public and governmental
interest in eliminating sub-therapeutic use of antibiotics
in livestock. An alternative approach to sub-therapeutic
antibiotics in livestock is the use of probiotic microorgan-
isms, prebiotic substrates that enrich certain bacterial
populations, or synbiotic combinations of prebiotics and
probiotics. Research is focused on identifying beneficial
bacterial strains and substrates along with the conditions
under which they are effective.
bacteria in the colon” (Gibson and Roberfroid, 1995).
Combinations of prebiotics and probiotics are known
Probiotic and prebiotic foods have been consumed for
centuries, either as natural components of food, or as
fermented foods. Interest in intestinal microbiology and
the dietary use of prebiotics and probiotics blossomed in
the late 1800s and early 1900. The growing enthusiasm
was motivated Escherich’s isolation of Escherichia coli in
the late 1800s, as well as active research on the benefits
of feeding lactic acid bacteria and lactose near the turn of
the 20th century (Rettger and Cheplin, 1921). Metchnikoff
noticed the longevity of Bulgarians who consumed yo-
gurt, and in 1907, he proposed that the indigenous bacte-
ria were harmful and that ingestion of lactic acid bacteria
in yogurt had a positive influence on health (Stavric and
Kornegay, 1995; Rolfe, 2000). Numerous in vivo and in
vitro studies since then have shown that the commensal
intestinal microbiota inhibit pathogens, that disturbances
of the intestinal microbiota can increase susceptibility to
infection, and that addition of prebiotics and probiotics
increase resistance to infection (Stavric and Kornegay,
1995; Rolfe, 2000).
Intestinal pathogens encounter a multifaceted defense
sections of the intestinal tract, as well as the intestinal
microbiota, epithelium, and immune systems. Although
PATTERSON AND BURKHOLDER
not reviewed here, there is extensive information on the
et al., 1998; Mayer, 1998; Muir, 1998; Hershberg and
Mayer, 2000; Shanahan, 2000; Erickson and Hubbard,
2000; Jeurissen et al., 2000; Spellberg and Edwards, 2001;
Tomsand Prowrie,2001), theintestinal epithelium(Glick,
1995; Fontaine et al, 1996; Dai, et al., 2000; Freitas and
Cayuela, 2000; Deplancke and Gaskins, 2001; McCracken
and Lorenz, 2001) and their interactions. Stress also has
detrimental effects on the immune system and intestinal
epithelium (Blecha, 2000; Matteri et al., 2000; Maunder,
2000; Soderholm and Perdue, 2001; Tache et al., 2001) and
the neuro-endocrine system is intimately involved in the
response of immune and epithelial systems to stress
(Cook, 1994; Kohm and Sanders, 2000; Levite, 2001; Pe-
trovsky, 2001). Additionally, there is information on
cross-talk between pathogens and epithelial tissues, re-
colonization by pathogens (Goosney et al., 2000; Sanso-
netti, 2001). Recently, Hooper et al. (2001) have shown
that cross-talk between Bacteroides thetaiotaomicron and
the epithelium results in epithelial secretion of specific
that other intestinal bacteria, including probiotic bacteria,
may interact with the epithelium in a similar manner to
enhance the ability of these microorganisms to colonize
the mucosal lining.
Intestinal microbial populations have been character-
jen et al., 1998; Van der Wielen et al., 2000). Although
Bacteroides and Bifidobacterium predominate in the human
nate in the chicken intestinal tract (Apajalahti et al., 1998;
Van der Wielen et al., 2000). However, recent molecular
techniques indicate that only 20 to 50% of the bacterial
species present in the intestinal tract have been cultured.
terial populations or general changes in microbial com-
munity structure should enhance our understanding of
intestinal microbial ecology, including the influence of
probiotics and prebiotics (Apajalahti et al., 1998; Neth-
erwood et al., 1999; Gong et al., 2002; Zhu et al., 2002).
ing resistance to infection and reduction in resistance
when the intestinal microbiota is disturbed is important
in understanding the microbe-host relationship. What
constitutes the balanced and disturbed populations is not
clear; however, lactobacilli and bifidobacterial species
seem to be sensitive to stress, and these populations tend
to decrease when a bird is under stress. Proposed mecha-
nisms of pathogen inhibition by the intestinal microbiota
ditions and compounds (volatile fatty acids, low pH, and
bacteroicins), competition for binding sites on the intesti-
nal epithelium, and stimulation of the immune system
(Fuller, 1989; Gibson and Fuller, 2000; Rolfe, 2000). These
are not mutually exclusive mechanisms, and some micro-
organisms may effect change with a single mechanism,
whereas others may use several mechanisms.
TABLE 1. Characteristics of ideal probiotics and prebiotics1
Be of host origin
Withstand processing and storage
Resist gastric acid and bile
Adhere to epithelium or mucus
Persist in the intestinal tract
Produce inhibitory compounds
Modulate immune response
Alter microbial activities
Be neither hydrolyzed or absorbed
by mammalian enzymes or tissues
Selectively enrich for one
or a limited number of beneficial bacteria
Beneficially alter the intestinal microbiota
and their activities
Beneficially alter luminal or systemic aspects
of the host defense system
1Adapted from Simmering and Blaut, 2001.
PROBIOTICS AND PREBIOTICS
otics are shown in Tables 1 and 2. Proposed mechanisms
by which probiotics and prebiotics act include competi-
tion for substrates, production of toxic compounds that
inhibit pathogens, and competition for attachment sites.
Extensive research conducted with humans and rodent
models has shown a reduction in pathogen colonization,
alteration of microbial populations, alteration of the im-
mune system, prevention of cancer, and reduction of tri-
glycerides, cholesterol, and odor compounds (ammonia,
skatole, indole, p-cresol, andphenol) associated with pro-
biotic and prebiotic use (Walker and Duffy, 1998; Gibson
and Fuller, 2000, Simmering and Blaut, 2001). More re-
search and commercial application of probiotics and pre-
biotics has occurred in Japan and Europe than in the
A variety of microbial species have been used as probi-
otics, including species of Bacillus, Bifidobacterium, Entero-
coccus, E. coli, Lactobacillus, Lactococcus, Streptococcus, a
variety of yeast species, and undefined mixed cultures.
Lactobacillus and Bifidobacterium species have been used
most extensively in humans, whereas species of Bacillus,
Enterococcus, and Saccharomyces yeast have been the most
common organisms used in livestock (Simon et al., 2001).
However, there has been a recent increase in research
on feeding Lactobacillus to livestock (Gusils et al., 1999;
Pascual et al., 1999; Jin et al., 2000; Tellez et al., 2001).
The dominant prebiotics are fructooligosaccharide
products (FOS, oligofructose, inulin). However, trans-ga-
lactooligosaccharides, glucooligosaccharides, glycooligo-
sacchriades, lactulose, lactitol, maltooligosaccharides,
xylo-oligosaccharides, stachyose, raffinose, and sucrose
thermal oligosaccharides have also been investigated
(Monsan and Paul, 1995; Orban et al., 1997; Patterson et
al., 1997; Piva, 1998; Collins and Gibson, 1999). Although
mannan oligosaccharides (MOS) have been used in the
same manner as the prebiotics listed above, they do not
selectively enrich for beneficial bacterial populations. In-
USE OF ANTIMICROBIALS IN PRODUCTION
stead, they are thought to act by binding and removing
pathogens from the intestinal tract and stimulation of the
immune system (Spring et al., 2000).
The competitive exclusion approach of inoculating 1-
function and disease resistance (Nisbet, 1998; Stern et al.,
2001). Although competitive exclusion fits the definition
of probiotics, the competitive exclusion approach instan-
taneously provides the chick with an adult intestinal mi-
crobiota instead of adding one or a few bacterial species
to an established microbial population. Inoculating 1-d-
old chicks with competitive exclusion cultures or more
classicalprobiotics servesasa nicemodel fordetermining
the modes of action andefficacy of these microorganisms.
Because ofthe susceptibility of1-d-old chicksto infection,
this practice is also of commercial importance. By using
this model, a number of probiotics (Owings et al., 1989;
Jin et al., 1998; Line et al., 1998; Nisbet, 1998; Netherwood
et al., 1999; Fritts et al., 2000) and prebiotics (Chambers
et al., 1997; Fukata et al., 1999) have been shown to reduce
colonization and shedding of Salmonella and Campylo-
Studies with probiotics have been difficult to assess
because many of the earlier studies were not statistically
analyzed, experimental protocols were not clearly de-
fined, microorganisms were not identified, and viability
of the organisms was not verified (Stavric and Kornegay,
1995). In many cases the environmental and stress status
feed withdrawal have been shown to increase pathogen
colonization (Bailey et al., 1991; Line et al., 1997; Craven,
2000). Bailey et al. (1991) clearly showed the importance
of stress on reduction of Salmonella colonization by fruc-
tooligosaccharides. In this study, unstressed birds and
fructooligosaccharide-treated stressed birds had low lev-
els of colonization, whereas stressed control birds had
high levels of Salmonella. Orban et al. (1997) using mild
heat stress showed that temperature and level of trace
minerals and vitamins influences performance responses
to sucrose thermal oligosaccharide caramel.
Using an organ culture challenge model, we (Burk-
holder andPatterson, unpublished data) haveshown that
fasting for 24 h increases attachment of Salmonella to the
ileum by 1.5 logs. Although horizontal transfer of patho-
gens to uninfected birds has been clearly demonstrated
(Gast and Holt, 1999), little concern has been shown for
horizontal transfer of probiotic organisms to untreated
TABLE 2. Beneficial effects of probiotics and prebiotics1
Modify intestinal microbiota
Stimulate immune system
Reduce inflammatory reactions
Prevent pathogen colonization
Enhance animal performance
Decrease carcass contamination
Decrease ammonia and urea excretion
Increase production of VFA
Increase biomass and stool bulking
Increase B vitamin synthesis
Improve mineral absorption
Lower serum cholesterol
Lower skatol, indole, phenol, etc
1Adapted from Stavric and Kornegay (1995); Jenkins et al. (1999); Monsan and Paul (1995); Piva (1998);
Simmering and Blaut (2001).
birds. Thus, frequently birds on control and probiotic
that probiotic organisms can be horizontally transferred
to control birds unless birds are physically separated.
Sub-therapeutic antibiotics are discussed in detail else-
tic antibiotics not only influence intestinal microbial pop-
ulations and activities but also affect animal metabolism
and specifically alter intestinal function (Anderson et al.,
2000). As would be expected, antibiotics are more effec-
tive when the animal is producing well below its genetic
potential and may have only statistically significant im-
Because stress status is important in detecting growth
performance responses, it is important to include growth
promotant antibiotics as a positive control treatment in
probiotic and prebiotic studies. Studies in which there is
no response to the growth promotant antibiotic should
not be considered negative for the probiotic or prebi-
Pathogens have to overcome numerous obstacles in
order to colonize the intestinal tract and cause an infec-
tion. In addition to the physical restraints of low gastric
have to overcome the inhibitory effects of the intestinal
microbiota, the physical barrier of the epithelium, and
the response of host immune tissues. The concept that
cross-talk between these systems and between pathogens
and the epithelium occurs is well established. Recent data
demonstrate that at least some species of non-pathogenic
intestinal microbiota also communicate with the epithe-
lium and immune system, modulating tissue physiology
ics alter the intestinal microbiota and immune system to
reduce colonization by pathogens in certain conditions.
As with growth promotant antibiotics, environmental
otics. These products show promise as alternatives for
antibiotics as pressure to eliminate growth promotant
antibiotic use increases. Defining conditions under which
under these conditions is important for the effective use
prebiotics and probiotics in the future.
PATTERSON AND BURKHOLDER
Anderson, D. B., V. J. McCracken, R. I. Aminov, J. M. Simpson,
News Inf. 20:1115N–1122N.
P. H. Nurminen, and W. E. Holben. 1998. Effective recovery
of bacterial DNA and percent-guanine-plus-cytosine-based
analysis of community structure in the gastrointestinal tract
of broiler chickens. Appl. Environ. Microbiol. 64:4084–4088.
Bailey, J. S., L. C. Blankenship, and N. A Cox. 1991. Effect of
fructooligosaccharide on Salmonella colonization of the
chicken intestine. Poult. Sci. 70:2433–2438.
Blecha, F. 2000. Neuroendocrine responses to stress. Pages 111–
119 in The Biology of Animal Stress. G. P. Moberg and J. A.
Mench, ed. CABI, New York.
Chambers, J. R., J. L. Spencer, and H. W. Modler. 1997. The
influence of complex carbohydrates on Salmonella typhimu-
rium colonization, pH, and density of broiler ceca. Poult. Sci.
Collins, M. D., and G. R. Gibson. 1999. Probiotics, prebiotics,
and synbiotics: approaches for modulating the microbial
ecology of the gut. Am. J. Clin. Nutr. 69(Suppl. 1):1042S–
Cook, H. J. 1994. Neuroimmune signaling in regulation of intes-
tinal transport. Am. J. Physiol. 266:G167–G178.
ium perfringens and fecal shedding in diet-stressed and un-
stressed broiler chickens. Poult. Sci. 79:843–849.
Dai, D., N. N. Nanthkumar, D. S. Newburg, and W. A. Walker.
2000. Role of oligosaccharides and glycoconjugates in intesti-
nal host defense. J. Pediatric Gastroenterol. Nutr. 30:S23–S33.
Deplancke, B., and H. R. Gaskins. 2001. Microbial modulation
of innate defense: Goblet cells and the intestinal mucus layer.
Am. J. Clin. Nutr. 73(Suppl. 1):1131S–1141S.
Erickson, K. L., and N. E. Hubbard. 2000. Symposium: Probiotic
bacteria: implications for human health. Probiotic immuno-
modulation in health and disease. Am. Soc. Nutr. Sci.
rat harboring a human bacterial flora: Effect of inulin in the
diet. Br. J. Nutr. 75:881–892.
Freitas, M., and C. Cayuela. 2000. Microbial modulation of host
intestinal glycosylation patterns. Microb. Ecol. Health Dis.
Fritts, C. A., J. H. Kersey, M. A. Motl, E. C. Kroger, F. Yan, J.
Si, Q. Jiang, M. M. Campos, A. L. Waldroup, and P. W.
live performance and microbiological status of broiler chick-
ens. J. Appl. Poult. Res. 9:149–155.
Fukata, T., K. Sasai, T. Miyamoto, and E. Baba. 1999. Inhibitory
effects of competitive exclusion and fructooligosaccharide,
singly and in combination, on Salmonella colonization of
chicks. J. Food Prot. 62:229–233.
Fuller,R. 1989.Probiotics inman andanimals. J.Appl. Bacteriol.
Gast, R. K., and P. S. Holt. 1999. Experimental horizontal trans-
mission of Salmonella enteritidis strains (phage types 4, 8, and
13A) in chicks. Avian Dis. 43:774–778.
Gibson, G. R., and R. Fuller. 2000. Aspects of in vitro and in
vivo research approaches directed toward identifying probi-
otics and prebiotics for human use. J. Nutr. 130:391S–395S.
Gibson, G. R., and M. B. Roberfroid. 1995. Dietary modulation
of the human colonic microbiota: introducing the concept of
prebiotics. J. Nutr. 125:1401–1412.
Glick, B. 1995. The immune system of poultry. Poultry Produc-
tion. P. Hunton, ed. Elsevier Science, Amsterdam.
Gong, J., R. J. Forster, H. Yu, J. R. Chambers, P. M. Sabour, R.
Wheatcroft, and S. Chen. 2002. Diversity and phylogenetic
analysis of bacteria in the mucosa of chicken ceca and com-
parison with bacteria in the cecal lumen. FEMS Microbiol.
Enteropathogenic E. coli (EPEC) interactions with the host.
Ann. Rev. Cell Dev. Biol. 16:173–189.
Gusils, C., S. N. Gonzales, and G. Oliver. 1999. Some probiotic
properties of chicken lactobacilli. Can. J. Microbiol. 45:981–
Hershberg, R. M., and L. F. Mayer. 2000. Antigen processing
and presentation by intestinal epithelial cells—polarity and
complexity. Immunol. Today 21:123–128.
Hooper, L. V., M. H. Wong, A. Thelin, L. Hansson, P. G. Falk,
microbial relationships in the intestine. Science 291:881–884.
Jenkins, D. J. A., C. W. C. Kendall, and V. Vuksan. 1999. Inulin,
oligofructose and intestinal function. J. Nutr. 129:1431S–
Jeurissen, S. H. M, A. G. Boonstsra-Blom, S. O. Al-Garib, L.
infection in poultry: A review. Vet. Q. 22:204–208.
Jin, L. A. Y. W. Ho, N. Abdullah, and S. Jalaludin. 1998. Growth
performance, intestinal microbial populations, and serum
cholesterol of broilers fed diets containing Lactobacillus cul-
tures. Poult. Sci. 77:1259–1263.
Jin, L. Z., Y. W. Ho, N. Abdulla, and S. Jalaludin. 2000. Digestive
and bacterial enzyme activities in broilers fed diets supple-
mented with Lactobacillus cultures. Poult. Sci. 79:886–891.
Kitagaw, H., Y. H. Iratsuka, T. Imagawa, and M. Uehara. 1998.
ens. J. Anat. 192:293–298.
Kohm, A. P., and V. M. Sanders. 2000. Norepinephrine: A mes-
senger from the brain to the immune system. Immunol. To-
Levite, M. 2001. Nervous immunity: Neurotransmitters, extra-
cellular K+and T-cell function. Trends Immunol. 22:2–5.
Line, J. E., J. S. Bailey, N. A. Cox, and N. J. Stern. 1997. Yeast
associated with broiler chickens subjected to transport stress.
Poult. Sci. 76:1227–1231.
Line, E. J., J. S. Bailey, N. A. Cox, N. J. Stern, and T. Tompkins.
1998. Effect of yeast-supplemented feed on Salmonella and
Campylobacter populations in broilers. Poult. Sci. 77:405–410.
Matteri, R.L., J.A. Carroll,and C.J. Dyer.2000. Neuroendocrine
responses to stress. Pages 43–63 in The Biology of Animal
Stress. G. P. Moberg and J. A. Mench, ed. CABI, New York.
Maunder, R. 2000. Mediators of stress effects in inflammatory
bowel disease: Not the usual suspects. J. Psychosom. Res.
Mayer, L. 1998. Current concepts in mucosal immunity I. Anti-
gen presentation in the intestine: New rules and regulations.
Am. J. Physiol. 274:G7–G9.
McCracken, V. J., and R. G. Lorenz. 2001. The gastrointestinal
ecosystem: A precarious alliance among epithelium, immu-
nity and microbiota. Cell. Microbiol. 3:1–11.
Monsan, P., and F. Paul. 1995. Oligosaccharide feed additives.
Feeding. R. J. Wallace and A. Chesson, ed. VCH, New York.
Muir, W. I. 1998. Avian intestinal immunity: basic mechanisms
and vaccine design. Poult. Avian Biol. Rev. 9:87–106.
Netherwood, T., H. J. Gilbert, D. S. Parker, and A. G. O’Donnell.
1999. Probiotics shown to change bacterial community struc-
ture in the avian gastrointestinal tract. Appl. Envion. Micro-
Nisbit, D. J. 1998. Use of competitive exclusion in food animals.
J. Am. Vet. Med. Assoc. 213:1744–1746.
Effect of sucrose thermal oligosaccharide caramel, dietary
vitamin-mineral level, and brooding temperature on growth
USE OF ANTIMICROBIALS IN PRODUCTION
Owings, W. J., D. L. Reynolds, R. J. Hasiak, and P. R. Ferket.
1989. Influence of dietary supplements with Streptococcus
characteristics, and intestinal microbial colonization. Poult.
Pascual, M., M. Hugas, J. I. Badiola, J. M. Monfort, and M.
Garriga. 1999. Lactobacillus salivarius CTC2197 prevents Sal-
monella enteritidis colonization in chickens. Appl. Environ.
Patterson, J. A., J. I. Orban, A. L. Sutton, and G. N. Richards.
1997. Selective enrichment of bifidobacteria in the intestinal
tract of broilers by thermally produced kestoses and effect
on broiler performance. Poult. Sci. 76:497–500.
immune interaction. Immunol. Cell Biol. 79:350–357.
Piva, A. 1998. Non-conventional feed additives. J. Anim. Feed
Rettger, L. F., and H. A. Cheplin. 1921. A Treatise on the Trans-
formation of the Intestinal Flora, with Special Reference to
the Implantation of Bacillus acidophlus. Yale University Press,
New Haven, CT.
Rolfe, R. D. 2000. The role of probiotic cultures in the control
of gastrointestinal health. J. Nutr. 130:396S–402S.
Rosen, G. D. 1995. Antibacterials in poultry and pig nutrition.
Feeding. R. J. Wallace and A. Chesson, ed. VCH, New York.
Sansonetti, P. J. 2001. Rupture, invasion and inflammatory de-
struction of the intestinal barrier by Shigella, making sense
of prokaryote-eucaryote cross-talks. FEMS Microbiol. Rev.
Savage, D. C. 1987. Factors influencing biocontrol of bacterial
pathogens in the intestine. Food Technol. 41:82–87.
Schat, K. A., and T. J. Myers, 1991. Avian Intestinal Immunity.
Crit. Rev. Poult. Biol. 3:19–34.
contents. Am. J. Physiol. 278:G191–G196.
Simmering, R., and M. Blaut. 2001. Pro- and prebiotics—the
Simon, O., A. Jadamus, and W. Vahjen. 2001. Probiotic feed
additives—effectiveness and expected modes of action. J.
Anim. Feed Sci. 10:51–67.
Soderholm, J. D., and M. H. Perdue. 2001. Stress and the gastro-
intestinal tract II. Stress and intestinal barrier function. Am.
J. Physiol. 280:G7–G13.
and infectious diseases. Clin. Infect. Dis. 32:76–102.
nella-challenged broiler chicks. Poult. Sci. 79:205–211.
Stavric, S., and E. T. Kornegay. 1995. Microbial probiotics for
pigs and poultry. Pages 205–231 in Biotechnology in Animal
Feeds and Animal Feeding. R. J. Wallace, and A. Chesson,
ed. VCH, New York.
Stern, N. J., N. A. Cox, J. S. Bailey, M. E. Berrang, and M. T.
Musgrove. 2001. Comparison of mucosal competitive exclu-
sion and competitive exclusion treatment to reduce Salmo-
nella and Campylobacter spp. Colonization in broiler chickens.
Poult. Sci. 80:156–160.
Tache, Y., V. Martinez, M. Million, and L. Wang. 2001. Stress
and the gastrointestinal tract III. Stress-related alterations of
gut motor function: role of brain corticotrophin-releasing
factor receptors. Am. J. Physiol. 280:G173–G177.
Tellez, G., V. M. Petrone, M. Excorcia, T. Y. Morishita, C. W.
Cobb, and L. Villasenor. 2001. Evaluation of avian-specific
probiotics and Salmonella enteritidis-, Salmonella typhimurium-
, and Salmonella heidelberg-specific antibodies on cecal coloni-
zation and organ invasion of Salmonella enteritidis in broilers.
J. Food Prot. 64:287–291.
by regulatory T cells. Microbes Infect. 3:929–935.
Vahjen, W., K. Glaser, K. Schafer, and O. Simon. 1998. Influence
of xylanase-supplemented feed on the development of se-
lected bacterial groups in the intestinal tract of broiler chicks.
J. Agric. Sci. 130:489–500.
Van der Wielen, P. W. J. J., S. Biesterveld, S. Notermans, H.
Hofstra, B. A. P. Urlings, and F. van Knapen. 2000. Role of
volatile fatty acids in development of the cecal microflora in
broiler chicken during growth. Appl. Environ. Microbiol.
tion: role of probiotics and prebiotics. J. Nutr. Biochem.
Zhu, S. Y., T. Zhong, Y. Pandya, and R. D. Joerger. 2002. 16S
rRNA-basedanalysis ofmicrobiota fromthe cecumof broiler
chickens. Appl. Environ. Microbiol. 68:124–137.