IMMUNOLOGY, HEALTH, AND DISEASE
Benefits of probiotics and/or prebiotics for antibiotic-reduced poultry
H. S. Al-Khalaifah1
Environment and Life sciences Research Centre, Kuwait Institute for Scientific Research, P.O. Box 24885, 13109
Safat- KUWAIT
ABSTRACT Antibiotics have been used for many
years as growth promoters. They contribute to build
the immunocompetence (i.e. ability of the body to pro-
duce a normal immune response following exposure to
an antigen) of birds against infectious diseases and as
growth promoters. Antibiotics have been widely used
as growth promoters in the field of animal produc-
tion since 1940s. There is a hypothesis that is effect is
brought about by dynamic biological interaction with
the micro-flora in the intestine. In 1951, the United
States Food and Drug Administration approved the
use of antibiotics as animal additives to prevent dis-
ease in general and, in some cases, to improve effi-
ciency without veterinary prescription. In the 1950s
Key words: antibiotics, poultry, prebiotics, probiotics
INTRODUCTION
Over more than six decades dietary antibiotics have
been used not only as a means to control infectious dis-
eases but also to improve growth performance and feed
efficiency (Gadde et al., 2018). The wider use of antibi-
otics as feed additives in the long run can contribute
to the development of bacteria resistant to drugs used
to treat infections which are of a potential risk if they
are transferred to humans. For this reason, the World
Health Organization (WHO, 1997) and the Economic
and Social Committee of the European Union (1998)
concluded that the use of antimicrobials in food animals
is a public health issue. The European Union banned
the use of all in-feed antibiotics as growth promoters
in 2006 (Castanon, 2007). In 2009, government agen-
cies in the USA such as the Food and Drug Adminis-
tration (FDA) testified that the use of antibiotics for
growth promotion should be eliminated (FDA, 2009).
However, probiotics have not been approved by FDA
yet. Although safe and effective, this treatment cannot
become the standard of care, nor can be implemented
in hospital formularies (Janvier et al., 2013).

C 2018 Poultry Science Association Inc.
Received October 29, 2017.
1
Corresponding author: hkhalifa@kisr.edu.kw
3807
and 1960s, each European state approved its own na-
tional regulations about the use of antibiotics in ani-
mal feeds. However, using antibiotics may develop bac-
teria resistant to these drugs. Accordingly, the use of
antibiotics has been minimized and replaced by ef-
fective dietary supplements such as probiotics and/or
prebiotics that are claimed to enhance growth and
positively modulate the immune response. The cur-
rent review paper sheds light on the benefits of us-
ing probiotics and/or prebiotics in poultry feed ver-
sus the risk of using antibiotics and the mechanisms by
which they exert their effects, as well as the economic
analysis of using these beneficial additives in poultry
feed.
2018 Poultry Science 97:3807–3815
http://dx.doi.org/10.3382/ps/pey160
Accordingly, the use of antibiotics has been mini-
mized and replaced by effective dietary supplements
such as probiotics and/or prebiotics that are claimed
to enhance growth and positively modulate the immune
response.
Benefit of Probiotics and Prebiotics
The inclusion of antibiotics as growth promoters was
effectively banned in 2006, throughout the European
Union, because some microbes developed resistance to
these antibiotics (Europe Union Commision, 2005), and
dietary probiotics and/or prebiotics have been used as
immunomodulators and alternatives to antibiotics.
Probiotics and prebiotics maybe classified as func-
tional food; that which affects bodily functions in a
positive manner so as to improve health or if its ef-
fect extends to the physiological or psychological lev-
els going beyond the traditional nutritional effect.
Probiotics are live microorganisms which when ad-
ministered in adequate amounts confer a beneficial
health effect on the host. Lactic acid bacteria (LAB),
Bacillus and Bifidobacteria are the most common types
of probiotics (Parvez et al., 2006; Roberfroid, 2000).
Prebiotics are non-digestible food ingredients that stim-
ulate the growth and/or activity of beneficial microflora
3808 AL-KHALAIFAH
in the digestive system. Typically, prebiotics are car-
bohydrates (such as oligosaccharides), but they may
be non-carbohydrates. Prebiotics are selectively fer-
mented in the colon by beneficial bacteria such as
Bifidobacterium and Lactobacillus. The probiotic bacte-
ria exert competitive effect in the gut and produce bac-
teriocins, which have an antimicrobial effect on other
bacteria (Patterson and Burkholder, 2003).
Effect on Production Parameters and use of
in-ovo technology in Chickens
There are many reports concerning the effect of us-
ing probiotics including Lactobacillus, Bifidobacterium,
Bacillus, Streptococcus, Pediococcus, Enterococcus, and
yeast such as Saccharomyces cerevisiae on the different
performance parameters in chickens including immune
status and feed efficiency in broilers.
Body weight gain and increased feed intake as a result
of dietary probiotics supplementation were reported.
For example, Mountzouris et al. (2007), supplemented
broiler chickens with a probiotics mixture at 1 g/kg
of feed from 1 to 42 d of age. The probiotic mixture
included microbes that were isolated from the gut of
healthy chickens. These included Lactobacillus reuteri,
Enterococcus faecium, Bifidobacterium animalis, Pe-
diococcus acidilactici and Lactobacillus salivarius. The
probiotic product had a total bacterial count, expressed
as colony-forming units of 2 × 1012 CFU/kg of product.
The authors showed that the dietary probiotics in the
feed of broiler chickens significantly promoted growth
performance. Similarly, supplementing broiler chickens
with a probiotic mixture of Bacillus licheniformis
and Bacillus subtilis spores at 0.05% of feed signifi-
cantly improved the feed conversion ratio, compared
to the unsupplemented control group, the supple-
mented probiotic contained 2.3 × 108 CFU/g Bacillus
licheniformis and 2.3 × 108 CFU/g Bacillus subtilis
spores in equal rates, at a level of 0.5 g/kg (Midilli et al.,
2008). In addition, Bacillus coagulans-supplemented
broiler feed significantly improved final and daily
weight gain, feed conversion ratio and survival rate,
when compared to the un-supplemented control group,
and is recommended to replace growth promoters in
broiler production (Awad et al., 2009; Cavazzoni et al.,
1998; Francesca et al., 2010; Hume, 2011; Huyghebaert
et al., 2011; Kral et al., 2012; Sohail et al., 2011; Taheri
et al., 2010; Zhou et al., 2010).
Jin et al. (2000) supplemented broiler diet with
0.1% dried culture of Lactobacillus acidophilus or
0.1% dried culture of a mixture of 12 Lactobacillus
strains (two strains of L. acidophilus, three strains of
L. fermentum, one strain of L. crispatus, and six strains
of L. brevis). The results showed that the body weight
gain was significantly increased in the supplemented
group compared to the control group. Al-Zenki et al.
(2009) investigated the effect of commercial probiotics
on the performance of Salmonella spp. in broilers. They
used Aviguard, Saccharomyces cerevisiae and Pedio-
coccus acidilactici. The results showed that probiotic
treatments significantly decreased Salmonella spp. and
had no effect on the production parameters of broiler
chickens. Similarly, Tellez et al. (2012) reported that
Lactobacillus probiotic significantly reduced Salmonella
spp. when administered in high amounts during broiler
production. These results agree with other studies that
investigated the effect of probiotics administration in
poultry on the occurrence of Salmonella spp. (Hume,
2011; Taheri et al., 2010; Tellez et al., 2012; Vicente
et al., 2008; Vila et al., 2009).
The beneficial effect of using prebiotics is well doc-
umented in the literature. For example, Ammerman
et al. (1989) investigated the effect of supplementing
broiler chickens with 0.375% oligofructose on the body
weight gain and percentage carcass and breast weight.
The authors reported that the supplemented diet pro-
duced heavier birds at 47 d of age, improved percent-
age carcass and breast weights, and reduced percent-
age fat pad, compared to the control group. Cengiz
et al. (2012) investigated the effects of a dietary pre-
biotic (Agrimos) for a period of 14 d on the intesti-
nal micro-flora and growth performance of male broiler
chicks. A significant decrease (6.2 vs. 5.5 log10cfu/g) in
Enterobacteriaceae (P < 0.01) and increase (5.5 vs. 5.9
log10cfu/g) in Lactobacilli count was noted in prebiotic-
supplemented groups on day 7. Dietary prebiotic sup-
plementation also significantly improved digestibility.
Also, the dietary supplementation of 0.2% Aspergillus
prebiotic meal against the horizontal transmission of
Salmonella spp. in turkeys and chickens was evaluated
by Londero et al. (2011). They suggested that the ad-
dition of Aspergillus meal as a prebiotic at 0.2% may
have a beneficial effect in reducing Salmonella spp. lev-
els and may enhance overall food safety of poultry meat.
The effect of the fermentation product of Aspergillus
oryzae, as a prebiotic and a Lactobacillus-based probi-
otic, individually and in combination as a synbiotic, on
broiler performance and litter quality was investigated
(Chegeni, 2012). The author used prebiotic at 1.8, 1.0
and 1.0 g/kg and probiotic at 0.9, 0.5 and 0.25 g/kg
to a corn, soy-based diet during starter, grower and
finisher periods, respectively. The prebiotic improved
body weight gain and feed conversion efficiency after
36 d significantly (P < 0.05) by 1 and nearly 2% re-
spectively, whereas the probiotic had no significant ef-
fect. The synbiotic improved body weight gain and feed
conversion efficiency significantly (P < 0.05) by 3.0 and
2.1% respectively.
Recently, Palamidi et al. (2016) investigated the
effect of dietary viable or heat inactivated probiotic
forms (PF) combined or not with avilamycin (AV) used
as a growth promoter, on broiler growth performance,
nutrient digestibility, digestive enzyme activities, and
expression of immune response related genes. The
authors used 450 one-day-old Cobb male broilers
allocated in 6 treatments according to a 3 × 2 factorial
arrangement with 5 replicates of 15 broilers. The results
of their study showed that viable probiotic, as well
as inactivated probiotic alone or in combination with
 PROBIOTICS AND/OR PREBIOTICS IN POULTRY
avilamycin, improved nutrient digestibility and that di-
etary additives affected growth performance positively
and induced an anti-inflammatory response at cecal
level. In another study of Hutsko et al. (2016), the au-
thors suggested a positive effect of probiotic (commer-
cial mixture) and prebiotic supplementation (mannan
oligosaccharide) on the intestinal microenvironment.
The authors supplemented young turkeys with two
commercial probiotics or a commercial mannan
oligosaccharide and investigated the transcription of
MUC2, the primary mucin protein produced by goblet
cells within the small intestine. The intestinal morphol-
ogy was also studied immediately post-hatch through
day 11. The results of the study revealed an increase in
the height and area of the villus upon supplementation
with the probiotics and the prebiotics. Also, the MUC2
transcription increased from d zero to d 4 post-hatch.
Chickens reared under harsh environmental condi-
tions such as high temperatures are subjected to im-
munological stress. Dietary probiotics and prebiotics
have been used to modulate the immune response in
poultry. Their effect may include immuno-stimulation,
anti-inflammatory reactions, exclusion and killing of
pathogens in the intestinal tract, and reduction of bac-
terial contamination on processed broiler carcasses. The
balanced interaction between the intestinal microbiota,
epithelium, and immune system provides resistance to
enteric pathogens (Patterson and Burkholder, 2003).
Recently, scientists from Nottingham Trent Univer-
sity fed 240 broiler chickens with different doses (200
and 800 g/t) of a yeast-based feed supplement and mon-
itored them every day for 42 d. Their findings suggest
that the feed supplement containing a carbohydrate
fraction Antigen found in yeast resulted in the birds
having greater natural defense to harmful bacteria en-
tering their guts, and this effect could be age-dependent
with younger birds having increased secretion capac-
ity of mucin, a substance secreted by the gut lining,
which can help defend against infectious agents (Lea
et al., 2012). It was demonstrated that Bacillus subtilis
facilitates the growth of another probiotic organism,
L. reuteri, through the production of catalase and sub-
tilisin (Hosoi et al., 2000). The authors examined the
effect of Bacillus subtilis on the growth of L. reuteri
co-cultured aerobically in vitro and showed that addi-
tion of B. subtilis to the culture medium resulted in
an increase in the number of viable cells of Lactobacilli
tested. This increase in lactobacilli is due to the fact
that the produced catalase by Bacillus subtilis exhibits
a growth-promoting effect on Lactobacilli. Also, a ser-
ine protease from Bacillus subtilis, subtilisin, improved
the growth and viability of L. reuteri in the absence of
hydrogen peroxide in the in vitro culture (Hosoi et al.,
2000).
Probiotics were administered in ovo in broiler chicks
with a mixed Eimeria infection, to study its effect on
hatchability, performance, immune organ weights and
lesion scores. They proceeded to inject 210 eggs with
probiotic bacteria. Post-hatch, on the third day, half of
the chicks were challenged with a mixed inoculum of
3809
Eimeria. Tissue samples and measurements were taken
on days 3, 9 and 15. No significance was observed for
hatchability, body weight, body weight gain or immune
organ weights prior to Eimeria challenge. However the
non-challenged birds; administered with the probiotics,
showed significantly higher body weight, body weight
gain or immune organ weights, whereas no differences
were observed in the challenged groups. Also birds re-
ceiving probiotics had lower mortality, with reduction in
lesions. Overall, this is an indication that supplementa-
tion of probiotics in ovo may improve performance and
offer immunity against infection (Pender et al. 2016).
In another study, in ovo technology was made use
of to deliver prebiotics (inulin; Pre1)and synbiotics
(bi2 tos; Pre2)into the air chamber of chicken eggs ob-
tained from 32-wk-old Ross 308 chickens, at 12d in-
cubation, and their effects on the immune system de-
velopment was evaluated; with emphasis on lymphoid
organs. The observations made were that the adminis-
tration of prebiotics of in ovo, did not adversely affect
immune system. Pre2 caused a reduction in the cor-
tex/medulla ratio of thymus on day 21 post hatching.
Enhanced B-cell proliferation in secondary lymphatic
organs occurred due to formation of germinal centers
in the spleen on day 21 and 35. Thus, administration of
these pre- and synbiotic at day 12 of incubation resulted
in modulation of central and peripheral organ develop-
ment. However, the effects were more prominent with
synbiotic treatment than with prebiotics (Madej et al.,
2015).
The use of probiotics and prebiotics may not always
provide a positive response in poultry production. In
contrast to the above, laying hens and broilers infected
with salmonella enterica serovar Enteritidis (SE) were
divided into groups fed control, probiotics, prebiotics
and synbiotics. The results showed that laying hens
and broilers fed probiotics and synbiotics did not
influence SE infection (Murate et al., 2015).
In a study on the digestive potency of pancreas, cock-
erels of different ages were injected in ovo a combination
of probiotics and synbiotics. The results showed that
the probiotics and synbiotics increased body weight but
did not change the feed conversion ratio (Pruszynska-
Oszmalek et al., 2015).
However, there are some studies in the literature
showing no benefits of using probiotics and prebiotics
in poultry production. For example, A total of 108 one-
day-old commercial broilers chicks were divided into
six groups; probiotic/prebiotic non-challenged, probi-
otic/prebiotic challenged, non-treated challenged and
non-treated non-challenged. The study was conducted
to test the protective properties of commercial probi-
otic (Lacto G) and prebiotic (Immunolin) on perfor-
mance, lesion scores and immunological parameters in
Eimeria tenella infected broiler chickens. The results
obtained showed that probiotic/prebiotic supplementa-
tion did not improve body weight or feed conversion
ratio, lesions scores were significantly reduced and to
some extent the negative effects of coccidiosis was re-
duced (Abu-Akkada and Awad, 2015).
3810 AL-KHALAIFAH
In addition, Houshmand et al., (2012), conducted an
experiment to determine the effects of prebiotics on per-
formance, immunity and some stress indicators. The
broilers were fed two levels of proteins, stocked at a nor-
mal or high stocking density. The treatments consisted
of two levels of prebiotic, dietary CP and stocking den-
sity. The results showed that no significance was seen on
performance, immunity and stress indicators like blood
glucose, cholesterol, corticosterone etc. whereas protein
levels influenced performance and stocking density re-
sulted in better feed conversion ratio (FCR).
Mechanisms of Action
Proposed mechanisms by which the indigenous in-
testinal bacteria inhibit pathogens include competition
for colonization sites on the intestinal epithelium, com-
petition for nutrients, and production of toxic com-
pounds such as volatile fatty acids and bacteriocins or
modulation of the immune system. The inhibition pro-
cess may comprise one, several, or all of these mech-
anisms in a balanced way (Rolfe, 1991).These mecha-
nisms will be subsequently discussed briefly.
The mechanism of competition for colonization sites
on the intestinal epithelium is mediated through
polysaccharide-containing components attached to the
cell wall (Soerjadi et al., 1982). An acidic polysaccha-
ride cell wall component mediates adherence of com-
mon bacteria to each other and to the intestinal ep-
ithelium preventing other bacteria from attaching to
the epithelium, effectively blocking all receptor sites
(Fuller, 1975). The competition between probiotic and
pathogenic bacteria is complex and very competitive.
Competition for available binding sites on the intesti-
nal mucosa is also influenced by the pH of the luminal
contents. Also, Fuller (1977, 1978) demonstrated that
an acid pH favors the survival of acid loving bacteria
such as the Lactobacilli. Therefore, larger numbers of
the Lactobacilli will bind to the intestinal mucosal ep-
ithelial cells and exclude pathogens such as Salmonella
spp. and E. coli. Furthermore, the composition of the
medium in which the probiotic is growing will influence
the adhesion of the organism to the mucosal epithelium
and affect its resistance to acid (Fuller, 1975).
Competing for available nutrients as a means to con-
trol intestinal bacterial populations is probably not the
most effective mechanism. Rolfe (1991) indicated that
there were many environmental factors that affected
the availability of nutrient either from the diet of the
host or through the manipulation of dietary ingredients
that enhanced the growth of certain microbial popu-
lations, which might have resulted in the exclusion of
other bacterial species. A normal balance of bacteria
in the gastrointestinal tract is capable of utilizing all of
the potential carbon sources in the environment (Freter
et al., 1983). It has been shown that by manipulating
the lactose concentration in the diets of chickens, one
can selectively provide an advantage for the enhance-
ment of L. reuteri (Casas et al., 1998; 1993).
The production of antimicrobial compounds such as
bacteriocins has been also described. Bacteriocins are
bacterially produced peptides that are active against
other bacteria and have been an important criterion
in the selection of a probiotic strain. Colicin is a type
of bacteriocin which is produced by and toxic to some
strains of E. coli and closely related bacteria (Braun et
al., 1994; Parker et al., 1992). This competitive action
regulates the balance of the gut micro flora.
Probiotic bacteria are capable of enhancing both
specific and nonspecific immune responses by acti-
vating macrophages, increasing cytokine production
by intraepithelial lymphocytes (IEL), and increasing
the levels of immunoglobulins, especially IgA. Casas
et al. (1998) reported that turkeys given L. reuteri
had enhanced humoral antibody levels against S. ty-
phimurium, and this appeared to be highly correlated
with increased numbers of ileum IEL CD4+ (helper)
T-cells that function to expand the humoral immune
response. On the other hand, the number of ileum IEL
CD8+ (cytotoxic) T-cells was not different in L. reuteri-
fed turkeys. The ileum CD4+ /CD8+ ratio in L. reuteri-
fed turkeys increased from 2 to 3.5, but in the duode-
num, where few to no L. reuteri reside, the CD4+ /CD8+
ratio was not affected. Dalloul et al (2004) reported
that a Lactobacillus-based probiotic treatment given to
chickens challenged with Eimeria acervulina sporulated
oocysts resulted in larger numbers of IEL CD3+ , CD4+ ,
and CD8+ than that to the chickens on a control diet.
Probiotic-fed chickens also showed fewer faecal oocysts
than the controls. In addition, Haghighi et al (2006)
reported that serum and intestinal antibodies increased
in chickens after the administration of probiotics. Also,
mannan-oligosaccharide and probiotic supplementation
elevated IgG and IgM levels in turkeys (Cetin et al.,
2005) and broiler chickens (Alavi et al., 2012).
On the other hand, it was suggested that some of
the effects of probiotics and prebiotics may be brought
about by the modulation of the amount and type of
chemical mediators called eicosanoids. Eicosanoids reg-
ulate the production of cytokines, which control the
nature and intensity of the inflammatory immune re-
sponses (Miles and Calder, 1998). Munyaka et al. (2012)
investigated the effect of yeast-derived carbohydrates
(YDC) on the performance and innate immune re-
sponses of broiler chickens. The authors used a standard
broiler diet containing monensin (control), monensin +
bacitracin methylene disalicylate, and YDC treatment
at 0.02%, 0.01%, and 0.005% for starter, grower, and
finisher, respectively. The results showed that the ex-
pression of toll-like receptor 4 (TLR4) was down reg-
ulated in the YDC group compared with control in
the ileum. The expression of interleukin-12 (IL-12) and
interferon gamma-Y (IFN-γ ) were down regulated in
the YDC treatment only in the cecal tonsils. Com-
pared with the control, the expression of interleukin-10
(IL-10) in both the ileum and the cecal tonsils was down
regulated in the YDC treatment. Serum IgG and H: L
ratios were lower and higher respectively, in the YDC
treatment compared with the other treatments.
 PROBIOTICS AND/OR PREBIOTICS IN POULTRY
It was also suggested that some of the immunomod-
ulatory effects of probiotics and prebiotics may also in-
clude changes in intracellular signalling pathways and
transcription factor activity. This involves alteration of
the genetic expression of key adhesion molecules in-
volved in direct signalling pathways as well as alteration
in cytokine gene expression. It was concluded that the
dietary supplementation of probiotics and prebiotics en-
hances the expression of messenger RNA (mRNA) of
genes related to the innate immune response.
Effect on Meat Quality
Studies on the modulatory effect of dietary sup-
plementation with probiotics on the lipid profile in
broilers are limited. Salma et al. (2007) reported that
the dietary supplementation of bacteria (Rhodobacter
capsulatus) could improve fatty acid profile in broil-
ers. Yang et al. (2010) found that dietary Clostridium
butyricum at 1.6 × 1010 cfu/g moderately decreased the
ratio of n-6:n-3 fatty acids in breast muscles and in-
creased eicosapentaenoic acid (EPA(and total n-3 fatty
acids. In the same study, supplemented C. butyricum in
the diet significantly reduced the shear force of broiler
meat. A positive correlation between intra muscular
fat content of breast muscle and shear force was also
observed in this study. In a study conducted by Ma-
teova et al. (2008), a decrease in serum cholesterol level
and total lipids was observed after feeding Lactobacillus
fermentum probiotic at 109 cfu/g and oligosaccharide
prebiotics to broilers. Similar results were obtained by
Jin et al. (1998), where serum cholesterol levels were
significantly lower in broilers fed with diets enriched
with Lactobacillus cultures.
The supplementation of probiotics (Bacillus,
Lactobacillus, Streptococcus, Clostridium, Saccha-
romyces, and Candida spp.) to broiler diets improved
the characteristics of carcass and meat quality in male
broilers (Endo and Nakano, 1999). Also, Mahajan et al.
(2000) reported that the use of probiotics (Lactobacillus
acidophilus and Streptococcus faecium) increased mois-
ture, protein, ash, water holding capacity, emulsion
capacity and stability in broiler meats.
In general, probiotic supplementation improves meat
quality of the produced broilers.
Effect on Oxidative Status and Heat Stress
The effect of cyclic heat stress in broilers fed
prebiotics and probiotics is well documented in the lit-
erature. For example, Sohail et al. (2010) investigated
some of the biological markers of heat stress in
challenged broilers as modulated by dietary supple-
mentation of mannan-oligosaccharide (MOS) and a
Lactobacillus-based probiotic (LBP) at 6 × 107 cfu
per gram of product, either alone or in combination.
Birds were immunized against Newcastle and infectious
bursal disease viruses. From d 22, the birds were either
3811
kept at the thermoneutral zone (TN) or exposed to
heat stress (HS) to the conclusion of study, d 42. Re-
sults revealed that dietary supplementations decreased
the serum cortisol and cholesterol concentrations and
increased thyroxine concentration compared with the
HS group without supplementation. The percentage
of the C-reactive protein-positive birds was higher in
the HS group compared with the TN group. Dietary
supplementations improved humoral immunity against
Newcastle disease virus and infectious bursal disease
virus during HS. The authors concluded that dietary
supplementation of either MOS or LBP alone or in
combination can reduce some of the detrimental effects
of heat stress in broilers. In addition, a similar exper-
iment was conducted by Sohail et al. (2011) to study
the oxidative status of broilers under cyclic heat stress
(HS) as modulated by supplementation of mannan-
oligosaccharides (MOS) and a probiotic mixture at
6 × 107 CFU per gram of product. The probiotic
mixture contained Lactobacillus plantarum, Lactobacil-
lus acidophilus, Lactobacillus bulgaricus, Lactobacillus
rhamnosus, Bifidobacterium bifidum, Streptococcus
thermophilus, Enterococcus faecium, Aspergillus oryzae,
and Candida pintolopesii. The author showed that heat
stress increased total oxidants and total antioxidants
and decreased paraoxonase and arylesterase, with
no change in ceruloplasmin, aspartate aminotrans-
ferase, and alanine aminotransferase activities. Dietary
supplementation decreased total oxidants and total
antioxidants, with no effect on the activities of other
enzymes. Heat stress did not influence serum copper,
zinc, and manganese concentrations of birds when com-
pared with those in the thermoneutral group. However,
MOS increased concentrations of all the trace minerals.
It was concluded that MOS or PM supplementation,
alone or combined, may reduce some of the detrimental
effects of heat stress. Also, the prebiotic mannano-
ligosacharide, with a mixture of probiotics, was found
to enhance body weight, reduce feed consumption, and
improve the immunity of the gut in broiler chickens
which were subjected to chronic heat stress (Sohail
et al., 2012). Similarly, Ashraf et al. (2013) reported
that a mixture of mannan oligosaccharide and pro-
biotics improved intraepithelial lymphocytes count,
goblet cells count and differentiation of intestinal
microflora in broilers reared under cyclic heat stress.
Effect of Cecal Volatile Fatty Acids
In newly hatched chicks in commercial hatcheries,
the volatile fatty acid concentration and pH are not
sufficient to chemically suppress pathogens (1980;
Barnes et al., 1979), and therefore, supplementation of
probiotic microorganisms will be very beneficial. It is
critical to apply probiotic products as early as possible
to achieve the best results in the poultry industry.
As soon as a chicken hatches into an environment
that is heavily contaminated by bacteria, viruses, and
3812 AL-KHALAIFAH
protozoans, which emerge from the surface of the
eggshells, it must begin to develop protective gut mi-
croflora (Rinttilä and Apajalahti, 2013). The microflora
that is beneficial, contributes to the formation and
development of the intestinal immune system and also
helps in the activation of innate and adaptive immune
responses (Adil and Magray, 2012). Under normal con-
ditions, a 35-wk period is required for the development
of a stable population of gut associated bacteria, and
it is in the ceca where the greatest numbers reside.
In the ceca, an anaerobic environment develops and
favors the growth of organisms such as Bifidobacterium
spp. and Bacteriodes spp. Along with these bacteria,
other lactic acid bacteria create a micro-ecology that
can be characterized by an acid pH resulting from the
production of undissociated volatile fatty acids in the
caeca (acetic, butyric, propionic, and lactic acids) and
antimicrobial substances that effectively exclude or
kill many different pathogens (Sarra et al., 1992). The
effect of undissociated short chain volatile fatty acids is
well documented in many studies. They present in high
concentrations with acid pH and exert antimicrobial
effect. These acids are lipophilic penetrating the
bacterial cell wall and produce H+ ions which in turn
destroy the internal physiology of the bacterial cell.
In a study by Mookiah et al., 2014, broiler chickens
were fed diets supplemented with probiotics, prebiotics
and synbiotics. It was observed that the prebiotics and
probiotics increased caecal populations of lactobacilli
and bifidobacteria and decreased caecal E.coli at 21
days of age whereas it increased caecal volatile fatty
acids at 21 and 42 days of age. The synbiotics did not
show any such synergistic effect.
Polymannuronate, is an alginate which has been
isolated from marine brown algae and is considered
a potentially useful prebiotic. It is known to exclude
pathogenic and harmful microbes and also selectively
colonize beneficial microbes. In this study, 540 one-d-
old Arbor Acres male broilers were fed diets of corn and
soybean meal basal diet supplemented with 0, 1, 2, 3,
and 4 g/Kg polymannuronate. It was observed that
by increasing the levels of dietary polymannuronate,
led to a reduction in E.coli (P < 0.01) and increased
lactic acid bacteria (P = 0.04). Also the broilers were
found to have a higher concentration of acetic acid
(P < 0.01). Thus, the production of lactic acid,
acetic acid and volatile fatty acids (VFA) can lower
intestinal pH, creating an environment which hin-
ders the growth of harmful bacteria (Zhu et al.,
2015).
Based on the above, probiotic supplementation af-
fects the balance of cecal volatile fatty acids, which in
turn exert antimicrobial effect in poultry.
Economic Analysis of using Probiotics
The decision to use specific types of probiotics and/or
prebiotics is governed by the costs of these products and
ease of their applications against their potential bene-
fits to improve production performance and to increase
overall profits. Currently, there is a wide spectrum of
commercial probiotics and prebiotics for poultry avail-
able in the market. These additives are commonly used
at small dosages. In general, the cost of probiotics or
prebiotics ranges from US $1 to 20 per kg, depending
on the commercial company and the active ingredients
in the product (Young, 2008). If growth performance
and feed efficiency are increased in commercial farming,
then the costs of production are likely to be reduced.
Also, if the chicken flock is able to resist disease and sur-
vive until they are of marketable size, the subsequent
cost of medication and overall production costs would
be reduced drastically. For example, Torres-Rodriguez
et al. (2007) reported that the economic analysis of us-
ing probiotics dietary supplement in turkeys indicated
a lower cost per kilogram of live turkeys after includ-
ing their probiotic cost, 59.90 and 58.37 cents/kg of live
turkeys for the control and probiotic treatment respec-
tively. In the same study, the combination of a higher
daily weight gain and a small reduction in the feed con-
version ratio associated with the addition of the probi-
otic may have contributed to the lower cost of produc-
tion, even after considering the costs for the addition
of the probiotic, with an estimated additional income
per turkeys hen of about US 10 cents, representing an
economic alternative to improve poultry production. In
Anjum et al. (2005) studied the economic efficiency of
using protexin probiotic in broiler. The authors fed di-
ets containing protexin at 100 and 110 g/t in starter
and 50 and 55 g/t in finisher diets, respectively. The re-
sults of the study suggested that protexin supplementa-
tion is beneficial for better weight gains, feed efficiency
and economic efficiency in broiler chicks. The results
of this study revealed that per bird total return aver-
age on sale was $1.59 at total average expenditure of
$0.982. The net per bird income was $0.611 on average.
This indicated that supplementation of broiler starter
and finisher diets with protexin at 100 g/t in starter
and 50 g/t in finisher diets were economically bene-
ficial and encouraging where treated groups generated
more profit than the control group (Anjum et al., 2005).
According to Rosen (1995), supplementing broiler diet
with bacitracin probiotic increased in live weight from
1.5 to 2.6 kg over weeks 5 to 8 of the growth period, this
elevated the annual net profit per 1,000 birds by £60. In
addition, Gutierrez-Fuentes et al. (2013) evaluated the
effect of a commercial lactic acid bacteria-based pro-
biotic (FloraMax-B11) on growth performance, bone
qualities and morphometric analysis of broiler chick-
ens. The authors also estimated the cost benefit of us-
ing this probiotic in their study. The results showed
an increase in body weight and improvement in feed
conversion upon using the probiotic. The cost benefit
analysis showed that the increase in body weight of
100 g, when converted to a cost benefit ratio, suggested
that for every $ 1 spent on this probiotic there was a
cost benefit of 1:22.57.
 PROBIOTICS AND/OR PREBIOTICS IN POULTRY
However, there are studies in the literature show-
ing no benefit of using Probiotics and prebiotics
in poultry feed. For example, a total of 200 day-
old commercial broiler chicks were experimentally
divided into five dietary treatments; control (T1),
probiotic in the feed (100 g/tonne) (T2), prebiotic
in the feed (500 g/tonne) (T3), probiotic + prebiotic
(100 g/tonne+500 g/tonne) (T4) and probiotic + pre-
biotic (50 g/tonne+250 g/tonne) (T5). The economics
of this usage was calculated in terms of Return Over
Feed Cost (ROFC) and European Efficiency Index
(EPEI). It was seen that a diet supplemented with
symbiotic (100% level) proved to be more efficient in
terms of EPEI and ROFC (50% level) than prebiotics
or probiotic alone (Saiyed et al., 2015).
In conclusion, the economic analysis data obtained
from probiotic studies in broilers indicated that probi-
otic supplementation may not always be more feasible
and economical to obtain maximum profitability from
broiler production and hence further research in the
field is currently ongoing.
ACKNOWLEDGMENTS
The author would like to extend sincere thanks to the
Kuwait Institute for Scientific Research (KISR) and Kuwait
Foundation for the Advancement of Sciences (KFAS) for
their technical and financial support of the current study.
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