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International Journal of Livestock Research eISSN : 2277-1964 NAAS Score -5.36
Vol 7 (8) Aug’17
Hosted@www.ijlr.org DOI 10.5455/ijlr.20170610051314
Page1
Review Article
Prebiotics - The New Feed Supplement for Dairy Calf
A. K. Singh1*, Shilpi Kerketta2, R. K. Yogi1, Abhay Kumar3 and Lamella Ojha4
1Ph D Scholar (Animal Nutrition), N.D.R.I, Karnal, Haryana, INDIA
2Scientist (LPM), KVK, Neemach, INDIA
3Scientist (LPM), KVK Balrampur, Chhattissgarh, INDIA
4MVSc Scholar (Animal Nutrition), N.D.R.I, Karnal, Haryana, INDIA
*Corresponding author: vetabhi04@gmail.com
Rec. Date:
May 06, 2017 12:35
Accept Date:
Jun 10, 2017 17:13
Published Online:
July 24, 2017
DOI
10.5455/ijlr.20170610051314
Abstract
There are many factors such as dietary and management which, have been shown to markedly affect the
structure and activities of gut microbial communities in livestock animals. Under stressed conditions,
direct-fed microbials may be used to reduce the risk or severity of scours caused by disruption of the
normal intestinal environment. . Prebiotics are nondigestible dietary ingredients, usually oligosaccharides
(OS), which provide a health benefit to the host by directly modulating the gut microbiota. The observable
benefits of prebiotics may also be minimal in generally healthy calves In coming days, it is expected that
prebiotics could be the part of diets in both ruminants and non-ruminants for enabling modulation of gut
microfloravis a vis animals productivity in ecological ways. This review mainly focused on the benefits of
probiotics/prebiotics on the GI microbial ecosystem in ruminants, which is deeply involved in nutrition and
health for the animal. However, it is necessary to conduct more research with prebiotics as feed additives
to understand the detailed mechanisms of action and identify better alternatives for animal production and
health.
Key words: Calf, Gut Microbiota, Health, Prebiotics, Productivity
How to cite: Singh, A., Kerketta, S., Yogi, R., Kumar, A., & Ojha, L. (2017). Prebiotics: The New Feed
Supplement for Dairy Calf. International Journal of Livestock Research, 7(8), 1-17.
http://dx.doi.org/10.5455/ijlr.20170610051314
Introduction
It is well known that dairy calves are future herd. So the performance of the calf is totally dependent on
the managemental practices during first three months. It plays a key role in the economy of dairy farms
because they increase operating costs and reduce long-term productivity of the animal. Hence, the
maintenance of calf health and optimizing calf growth are key objectives especially at early stages of life
(Ghosh and Mehla, 2012).The dairy calf encounters potentially stressful situations in its first few months
International Journal of Livestock Research eISSN : 2277-1964 NAAS Score -5.36
Vol 7 (8) Aug’17
Hosted@www.ijlr.org DOI 10.5455/ijlr.20170610051314
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of life such as weaning, and commingling. Stress can lead to suppression of the immune system and
increase the risk of disease in the presence of a pathogen (Salak-Johnson and McGlone, 2014).Weaning
calves suffer from stress of digestive tract upset because of the shift from a liquid to a solid diet and
change in digestive tract microflora. This diet transition sometimes results in establishment of less
desirable intestinal microflora leading to poor performance (Bach et al., 2011). Further, there are more
disturbances in rumen microbiota by use of various antibiotics for combating the tract infection. In
extension the commingling phase of a dairy calf’s life, the transition from individual housing to group
housing, has been shown to increase the risk of bovine respiratory disease, decrease leukocyte function,
and decrease average daily gain (Hulbert and Ballou, 2012). These disease and conditions are so stressful
that calf is sometimes unable to cope up and may lead to mortality or stunted growth in future life. So to
overcome these situations various preventive measures as well treatments are practiced. In recent years
there have been many advances in the prevention and treatment of calf problems. Here at this point
nutritional quality of a feed needs to be improved. As nutritional quality is not only influenced by nutrient
content but also by many other aspects such as, hygiene, content of anti-nutritional factors, digestibility,
palatability and effect on intestinal health. Hence, the use of feed additives has been an important part of
achieving this success (Fanelli, 2012).Feed additives are materials that are used to enhance the
effectiveness of nutrients and exert their effects in the gut or on the gut wall cells to the animal
(McDonald et al., 2010). A large number of feed products as additives are available to prevent scours and
promote gut health and animal growth rates. They are used for the purpose of promoting animal growth
through their effect in increasing feed quality and palatability (Fanelli, 2012). The actual benefits of these
products are hard to quantify, but clearly they modify and protect the gut health in periods of stress and
disease. There are a number of feed additives that are used in animal feeds such as antibiotics, probiotics,
oligosaccharides, enzymes and organic acids. Along with this the most common milk additives are
probiotics, prebiotics, rennet, sodium bentonite, antibiotics, vitamins and minerals (Schouten, 2005).
Since long time among the various feed additives antibiotic is the most frequently and extensively used in
livestock diets due to its therapeutic importance (Cho et al., 2011). Antibiotics helps in checking
diarrhoea and enhance body weight gain by modifying gut microflora in growing calves (Novak and Katz,
2006).But the growing concern of the consumers for clean and safe products have restricted the use of
antibiotic as feed additive as growth promoters. Hence this led to initiation of many alternative strategies
for maximizing production by maintaining the animals health and performance. At the same time
maximizing health and well-being of the animals and minimize the impact of the industry on the
environment (Fanelli, 2012). Among feed additives prebiotics as a natural additive can be used as an
alternative to antibiotics maintain optimum ruminal digestion of feed.
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The Introduction of Prebiotics
Prebiotics are defined as ‘non-digestible food ingredients that beneficially affects the host by selectively
stimulating the growth and/or activity of one or a limited number of bacteria in the colon that can
improve host health’ (Gibson and Roberfroid, 1995). Prebiotics are selectively fermented, dietary
ingredients that result in specific changes in the composition and/or activity of the gastrointestinal
microbiota, thus conferring benefit(s) upon host health. Unlike probiotics, prebiotics target the
microbiota already present within the ecosystem, acting as a ‘food’ for the target microbes with
beneficial consequences for host (Hardy et al., 2013). The use of prebiotics is a promising approach for
enhancing the role of endogenous beneficial microbiota in the gut. One of the reasons prebiotics are
effective is because they are resistant to gastric acidity, absorption, and hydrolysis by enzymes produced
in the gastrointestinal tract (Patel and Goyal, 2012). They are, however, fermented by intestinal
microflora which promotes proliferation of commensal microorganisms. Lactobacilli and Bifidobacteria
are the most common microbial target genera in prebiotics application. A growing interest exists in the
health-promoting benefits of prebiotics. Multiple mechanisms of action for prebiotics have been
postulated, particularly enhancement of probiotic growth in the gut (Macfarlane et al., 2006).
Bifidobacteria produce various glycosidases which are enzymes that hydrolyze glycosidic bonds of
polysaccharides like most prebiotics, hence prebiotics’ ability to be readily fermented (Russo et al.,
2012). The fermentation products of prebiotics by intestinal microflora also provide benefit by immune
modulation, improved energy efficiency and digestibility, and decreased intestinal pH which suppresses
pathogenic bacteria (Mizota, 1996; Roodposhti and Dabiri, 2012). Prebiotics themselves have a positive
influence on immune parameters in the gut-associated lymphoid tissues, secondary lymphoid tissues,
and peripheral circulation (Bodera, 2008). Prebiotics may promote T Helper 1 and regulatory T cell-
dependent immune responses over T helper 2 responses (Patel and Goyal, 2012). Types of prebiotics
used in the livestock industry include indigestible sugars, ex. fructooligosaccharides (FOS),
galactooligosacchardies, mannan oligosaccharides, beta glucans, inulin and lactulose (Gibson et al.,
1995; Kleesen et al., 2001).All the above probiotics have their own function and are helpful in
improving the health and performance of calves.
Mannan Oligosaccharides
Production and Composition
Mannan oligosaccharides are short-chain, low molecular weight carbohydrate fragments of the yeast cell
wall, particularly Saccharomyces cerevisiae. Mannans represent approximately 30% of the cell wall
weight and are found on the outer parts of the cell wall (Kollár et al., 1997). They are comprised of many
International Journal of Livestock Research eISSN : 2277-1964 NAAS Score -5.36
Vol 7 (8) Aug’17
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α-1, 2 and α-1, 3 N-linked glycan side chains attached to a α-1, 6 linked mannose monomer backbone
(Kollár et al., 1997). To obtain these cell wall derivatives, yeast cells are lysed and the yeast culture that
is obtained is centrifuged to isolate the cell wall components. The cell wall components are then washed
and spray dried (Spring et al., 2000). The most important antigenic component of the cell wall are the
mannans of the yeast cell surface (Ballou, 1970).
Mechanisms
One of the primary functions of mannan oligosaccharides is to provide competitive binding for gram
negative bacteria. Gram negative bacteria have mannose-specific type-1 fimbriae that attach to D-
mannose receptors on the epithelium of the gastrointestinal tract (Friman et al., 1996; Ofek et al., 1977).
The presence of mannan oligosaccharides can provide an alternate binding site for these pathogens which
then block them from colonizing the epithelium and the complex exits the tract without causing harm
(Spring, 2000).Mannanoligosaccharides have the ability to alter the composition of the intestinal flora,
transport time, digestibility, absorption, and intestinal health of calves in this way (McGuirk, 2008).
Improved intestinal health and the inhibition of pathogenic microbes may contribute to smaller fecal
scores and fewer incidence of scours. Pathogenic bacteria produce toxins that cause intestinal
hyperactivity, secretion, and diarrhea (Giannella, 1983). In addition to competitive binding, mannan
oligosaccharides may also promote immune function such as phagocytosis and oxidative burst
(Magalhães et al., 2008). A potential mechanism for the immunomodulatory effects of mannan
oligosaccharides was described by Franklin et al., 2005. The authors proposed that collectins may be
responsible for this immunomodulatory function. One of the three types of collectins present in cattle are
mannose-binding proteins that can bind to mannose, N-acetylmannosamine, or N-acetylglucosamine.
Mannanoligosaccharides may promote the production of these mannose binding proteins. After binding,
this complex can act as an opsonin and improve phagocytosis or activate thecomplement system (Neth et
al., 2002).
Beta Glucans
Production and Composition
Beta glucans are other carbohydrate components of the yeast cell wall of Saccharomyces cerevisiae.
Beta glucans are also components of fungi and cereal grains like barley and oats (McGuirk, 2010). Beta
glucans are glucose polymers consisting of β-1, 3 and β-1, 6 linked D-glucopyranosyl units (Wang et al.,
2008).They account for 50 to 60% of the yeast cell wall weight. In contrast from mannan
oligosaccharides, glucans are found towards the inside of the cell wall. They provide structure and
rigidity to the cell wall that allows organization of the other cell wall components (Kollár et al., 1997).
International Journal of Livestock Research eISSN : 2277-1964 NAAS Score -5.36
Vol 7 (8) Aug’17
Hosted@www.ijlr.org DOI 10.5455/ijlr.20170610051314
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The efficacy of beta glucans may be modulated by the degree of branching, the molecular mass, and the
tertiary structure (Russo et al., 2012).
Mechanisms
Beta glucans that are large in molecular weight have been found to directly affect phagocytic, cytotoxic,
and antimicrobial activities of leukocytes, particularly macrophages. They also promote oxidative burst
responses by helping to produce reactive oxygen and nitrogen intermediates and clear apoptotic cells by
up-regulating the FS receptor (Gantner et al., 2005; Brown and Gordon, 2003). In addition to promoting
innate immune responses, betaglucans increase production of proinflammatory cytokines and
chemokines. Cytokines and chemokines stimulated by beta glucan-activated cells include IL-1β, IL-6,
and TNF-α (Vetvicka and Yvin, 2004). These cytokines and chemokines aid in the recruitment of
additional leukocytes to the site of infection.
The mechanism by which beta glucans can stimulate these immune responses is credited to the Dectin-1
receptor. The Dectin-1 receptor is expressed on monocytes, macrophages, neutrophils, dendritic cells,
and splenic T cells and can recognize carbohydrates with β-1,3 andβ-1,6 glucan linkages (Sonck et al.,
2009). When beta glucan binds to Dectin-1, the motif becomes phosphorylated, which sends a signal to
induce phagocytosis and respiratory burst (Brown and Gordon, 2003). On the other hand, cytokine and
chemokine production may be attributed to Toll-like receptor 2 (Brown and Gordon, 2003). To produce
TNF-α and IL-12, both Dectin-1 and Toll-like receptor 2 were required. TNF-α has many functions, one
of them being to aid in the oxidative burst response of neutrophils.IL-12 is important in stimulating
production of IFN-γ and promoting the T helper 1 immune response (Manetti et al., 1993).
Inulin
Production and Composition
Inulin is a natural b-(2-1)-linked fructo-oligosaccharide with up to 60 units common in plants used in the
Western diet (Van Loo et al., 1995).Inulin belong to a class of carbohydrates known as fructans. The
main sources of inulin that are used are chicory and Jerusalem artichoke. Purified inulin can also be
produced from tubers of the Jerusalem artichoke or Chicory. It contains 6–10% sugars, such as glucose,
fructose and sucrose, which are native to the chicory roots (Niness, 1999). Inulin belongs to the fructan
group. This consists of fructose subunits linked by β-2, 1 bonds containing, at the reducing end, a single
molecule of glucose. Glucose is linked by α-1, 2 bonds to a fructose chain (Kolida and Gibson, 2007). β-
2,1- linkages not only determine the specific properties of inulin, but also protect it from digestion in the
upper part of GIT (gastrointestinal tract) and are responsible for its reduced caloric value and the effect
of dietary fiber (Niness, 1999).
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Mechanisms
Inulin has effects on immune system either directly or indirectly. An indirect effect of inulin as
prebiotics is to the stimulation of the development of beneficial gut microbiota strains, and the inhibition
of the proliferation of pathogenic bacteria. This causes changes in composition of the intestinal
microfloral population like by increasing the number of bifidobacteria, there will be increased
competition with pathogenic bacteria for binding sites on the intestinal epithelium and for nutrients, thus
inhibiting survival of the pathogenic strains. Further the beneficial gut microbiota bacteria may also
cross the intestinal barrier into the Peyer’s patches, and activate immune cells there (Berg,
1985).However, the direct effect involves the stimulatory effect on phagocytosis carried out by the
phagocytic cells in blood (Wójcik et al., 2007), as well as non-specific mechanisms of humoral
immunity (Milewski et al., 2007).
Inulin also helps in production of Short Chain Fatty Acids (SCFA)from the fermentation of dietary fiber
which also have significant impact on the immune system by acidification of the colonic environment,
acidification of the colon favoring mucin production as well as binding to SCFA receptors on immune
cells within the gut-associated lymphoid tissues(GALT) (Lomax and Calder, 2009).The increased
concentration of SCFA results in a higher number (Kelly-Quagliana et al., 1998) of natural killer (NK)
cells and stimulates their activity. It is believed that inulin enhanced with oligofructose (OF) causes
beneficial changes in the immune function of GALT (Roller et al., 2004).It has been found in the earlier
studies that inulin enriched with oligofructose enhances the cytotoxicity of NK cells produced in the
spleen, intensifies cytokine production by spleen cells, and has stimulating properties on the immune
response to carcinogenic agents (Watzl et al., 2005).
Lactulose
Lactulose is a semi-synthetic disaccharide (Schumann, 2002) that is mainly fermented by beneficial
bacteria like lactobacilli or bifidobacteria (Mitsuoka et al., 1987). Lactulose a “bifidus factor” is
composed of galactose and fructose, which can be produced by the isomerization of lactose. It is a
prebiotic carbohydrate which stimulates the growth of health-promoting bacteria in the gastrointestinal
tract, such as bifidobacteria and lactobacilli and at the same time inhibits growth of pathogenic bacteria
such as Salmonella. Lactulose is generally prepared from an alkaline solution of lactose. The glucose
(Glu) moiety of lactose is isomerized to Fru, leading to the lactulose production. Different reactions and
schemes for the production of lactulose have been developed. Not only chemical isomerization, but also
enzymatic isomerization methods utilizing b-galactosidases have been developed (Schuster-Wolff-
Bühring et al., 2010).
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Mechanisms
Lactulose as a prebiotics have a positive effect on feed intake and body weight in calves. It has been
reported that the average daily milk replacer intake in pre weaned calves was significant higher in
feeding group with lactulose. An increased intake of crude protein and energy was achieved in calves,
due to the feeding of lactulose. Further a positive trend ongrowth was observed with increase average
daily gain (ADG) (Fleige et al., 2007). In addition it was also reported that here was significantly
increased feed consumption and a tendency for improved daily weight gain for calves fed 3% lactulose
and a probiotic bacteria strain with their milk replacer (Fleige et al., 2007). In accordance to the longer
villi lactulose also tended to increase the number of proliferative cells in ileum. Lactulose alters the
microbial balance and the biochemical composition of caecal contents in animals. Several in-vivo
studies have demonstrated that lactulose favours the growth of gram positive cocci and rods mostly
belonging to the genera Bifidobacterium and Lactobacillus (Bouhnik et al., 2004), while bacterial counts
of galactosidase- negative microorganisms like subspecies of the genera Clostridium and Bacteroides
have been shown to decrease (Hoffmann and Bircher, 1969; Mizota et al., 2002). In extension
metabolism of lactulose leads to an enhanced production of acetic acid, lactic acid, gas, short chain fatty
acids (SCFA) and the caecal pH has been shown to drop down to pH-values of about 5.0 (MacFarlane et
al., 2006). Further lactulose increased permeability of intestinal mucosa and an enhanced solubility of
minerals in the colon at low pH (MacFarlane et al., 1991; Seki et al., 2007).
Effects of Prebiotics on Calf Performance
Dairy calf performance is important for productivity later in life. Prebiotics have been shown to improve
performance measures such as average daily gain, feed intake, and digestibility. Prebiotics mainly used
in calves feeding have carbohydrate as main nutrient which produces volatile fatty acids, which further
may increase nutrient digestibility and subsequently increase feed efficiency. However, in a study
conducted with calves fed mannan oligosaccharides, no differences in volatile fatty acid production
were observed (Hill et al., 2009) and no differences were seen in dogs supplemented with
fructooligosaccharides or mannan oligosaccharides (Swanson et al., 2002).
In a study, calves supplemented with beta glucan had increased rumen pH and nutrient digestibility
(Kim et al., 2011). Mannan oligosaccharides (MOS) have improved performance in nursery pigs
(Dvorak et al., 1998) and weight gain and grain intake in dairy calves (Dvorak and Jacques, 1997). In
addition, investigation continues into the potential relationship between oligosaccharides and human
intestinal function (Jenkins et al., 1999) and their role in modulation of human gastrointestinal
microflora (Gibson, 1999).Increased average daily gain in weight and a tendency for improved feed
efficiency in calves was also found when fed galactosyl-lactose in milk replacer (Quigley et al., 1997).
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Similarly, an increase in body weight gain per calf per day, feed intake per calf per day, and feed
conversion efficiency were observed by Ghosh and Mehla (2012) when calves were administered 4 g/d
of a mannan oligosaccharide supplement. Although feed cost per calf per day was increased with
prebiotic supplementation, these costs were off-set by the increases in performance. Studies comparing
prebiotic supplement to antibiotics, found no differences in overall body weight gain, feed intake, or
feed efficiency, indicating that prebiotics may be a viable alternative for prophylactic antibiotic use
(Donovan et al., 2002). The synthetic disaccharide lactulose feeding has the tendency to increase
growth performance of preruminant calves and improves the intestinal microflora by stimulating the
growth of selected probiotic bacteria in the gut. In a trial conducted by Fleige et al. (2007), it was
found that the average daily live weight gain tended to be higher for group fed with lactulose at the rate
of 3% (1350 g/day) than group with no lactulose (1288 g/day). There is evidence that prebiotics may
modulate feeding behavior, indicated by results of studies showing improved body weight gain or feed
intake. In addition, studies have shown that prebiotic-supplemented calves increase intake at a faster
rate than un-supplemented calves (Heinrichs et al., 2003; Terré et al., 2006; Morrison et al., 2010).
Feeding fructooligosaccharides enhances the growth performance of veal calves by decreasing feed
conversion ratios and increasing carcass weight (Grand et al., 2013).There is down regulation of mRNA
expression of genes involved in inflammation in the intestine of the preruminant calves when they are
supplemented milk with the prebiotics inulin and lactulose (Masanetz et al., 2011). Prebiotics have
pronounced role in many minerals absorption and transportation. Prebiotics increase the production of
Short Chain Fatty Acids (SCFA) which shift the lumen pH towards acidic and, thereby increasing the
solubilisation of minerals. Butyrate acts as an energy source for intestinal epithelial cells and improves
their absorptive capacity.
Generally, prebiotics increase the absorption of Ca, Mg, Fe, Zn and Cu. They also increase the
absorption of Na+ and colonic water. Other researchers have observed an increased capacity of calcium
transporters (calbindin) in the colon (Ohta et al., 1998). Agave fructansas prebiotics prevents bone loss
and improves bone formation (Garcia-Vieyra et al., 2014).Further it was seen that the iron
bioavailability in corn and soybean meal was increased due to prebiotic supplementation (Yasuda et al.,
2006).
Effect of Prebiotics on Calf Health
Prebiotics such as mannan oligosaccharides prevent attachment of pathogenic bacteria whereas mannan
oligosaccharides and beta glucanscan improve the immune system of the calf. (FOS) in combination
with spray-dried bovine serum to calves reduced the incidence and severity of enteric disease (Quigley
et al., 2002). It has been suggested that this sugar prevents the adhesion of Enterobacteriaceae, most
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notably Escherichia coli and Salmonella, to the intestinal epithelium (Heartmink et al., 1997).
Supplementation of MOS, FOS, and GL may improve the growth performance of calves in both the
pre- or post weaning stage.
Indeed many studies have shown an increase in normal fecal scores and a decrease in the incidence of
scours with prebiotic supplementation. Pre-weaned calves fed milk replacer supplemented with
mannanoligosacchardies reported to have a good fecal scores compared with calves that received no
supplement (Heinrichs et al., 2003). Dairy calves fed a yeast culture derived from Saccharomyces
cerevisiae had more incidences of normal fecal scores and had fewer incidences of fever, diarrhea, and
health disorders as compared to controls (Magalhães et al., 2007). Furthermore, Ghosh and Mehla (2012)
reported that a mannan oligosaccharide supplementation reduced fecal coliform counts. Prebiotics may
exert cancer protective effects at the cellular level following SCFA formation. SCFA induce apoptosis in
colon adenoma and cancer cell lines (Hague et al., 1994).
Lactulose has an effect on the morphology of intestine. It was found that there was a reduction of ileal
villus height and decrease in the depth of the crypts when compared with control, due to lactulose
treatment of approximately 14% lactulose fed group (L1) and 20% lactulose fed group (L3). (Fleige et
al., 2007)
Effect of Prebiotics on Immune Function
The administration of prebiotics has been associated with immunomodulatory effects encompassing
innate, adaptive immunity as a result of the interaction with the microbiota (Gibson, 2008). Most
information about the effects of prebiotics on the immune system comes from experimental trials with
inulin and FOS. Prebiotics act like growth factor to particular commensal bacteria, which inhibit the
adherence and invasion of pathogens in the colonic epithelia by competing for the same glycoconjugates
present on the surface of epithelial cells, altering the colonic pH, favoring the barrier function, improving
the mucus production, producing short-chain fatty acids and inducing cytokine production (Korzenik and
Podolsky, 2006). The gut-associated lymphoid tissue (GALT) is the biggest tissue in the immune system
comprising 60% of all lymphocytes in the body. It contains Peyer's patches (PP), lamina propria (LP) and
intraepithelial lymphocytes (IEL) forming a unique immune network (MowatandViney, 1997). PP
contains follicle-associated epithelium (FAE) that covers M-cells responsible for transporting the antigen
onto the lymphatic tissue where dendritic, Tand B-cells are found (Mowat, 2003). LP is the region
between the epithelium and the muscle and contains mast cells, dendritic cells, macrophages and B- and
T-cells (MacDonald, 2003). The consumption of prebiotics can modulate immune parameters in GALT,
secondary lymphoid tissues and peripheral circulation (Bodera, 2008). Necrotizing enterocolitis (NEC) is
a major cause of morbidity and mortality in premature infants. Prebiotic administration manipulates the
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intestinal bacterial community, accelerating the growth of commensal bacteria. Prebiotic supplemented
formula increase stool colony counts of bifidobacteria and lactobacilli in preterm neonates without
adversely affecting weight gain (Srinivasjois et al., 2009). FOS is being increasingly included in food
products and infant formulae due to their laxative effect. Their consumption increases faecal bolus and the
frequency of depositions, reducing instances of constipation, considered one of the growing problems
associated with inadequate fiber diet consumption in the modern society and neonates (Sabater-Molina et
al., 2009). There are sufficient experimental data to support the hypothesis that prebiotic mixture
substantially contributes to the improvement of infant formulae. The immune-modulatory effect of
specific prebiotic oligosaccharides viz. GOS, FOS and pectin-derived acidic oligosaccharides was
studied. The supplementation exerted immunemodulatory effect during the early phase of a murine
immune response(Vos et al., 2010).They also seem to promote a positive modulation of the immune
system (Delgado et al., 2011).
Lactulose feeding had an immunomodulatory effect on the composition of T-cell subsets in different
immune compartments and had minor effects on pro- and anti inflammatory cytokine mRNA expression.
A significantly greater number of blood lymphocytes were detected in the 3% lactulose group than in the
control group. The expression results in male calves indicated that the transcription of IgA Fc receptor in
the ileal mucosa of the 1% lactulose treatment group increased significantly and also tended to increase in
the 3% lactulose group. Furthermore, decreases in IL-10 and interferon-γ mRNA expression were
observed in the ileum. The CD4-presenting lymphocytes were decreased significantly in the ileum and
mesenteric lymph node, whereas CD8-presenting lymphocytes were increased in the blood of females
(Fleige et al., 2007).
Fermentable substances such as inulin or lactulose have been proposed to stimulate the immune system
and health by modulation of the intestinal flora and its fermentation products. In a study, effects of inulin
and lactulose on the intestinal health and hematology of calves have been investigated. Only inulin was
able to increase hemoglobin concentration and hematocrit mRNA expression of inflammation-related
markers in the intestine was also affected by both prebiotics hinting at a decreased inflammatory status.
This may be due to a possible decrease in intestinal pathogen load. mRNA expression of interleukin 8
were increased by lactulose in mesenteric lymph nodes. In the ileum, expression of a proliferation marker
was increased by inulin while an apoptosis-related gene was increased by both prebiotics (Masanetz et al.,
2011). Prebiotics supplementation may influence innate immune responses, such as phagocytosis and
oxidative burst, cytokine production, and antibody response may be influenced. Mice supplemented with
10% oligofructose or inulin had increased peritoneal macrophage phagocytosis and macrophage
superoxide production compared to control mice (Trushina et al., 2005).
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Table 1: Effect of Prebiotics on Calf
Young
calves
MOS @ 4 g/d of Bio-Mos
Stimulate calf starter intake. Presence
of Cl. perfringensandE. coli,and
Salmonella spp. Decreases.
(Terre et al., 2007)
Calves
Cellulo oligosaccharides
@ 5 g/day pre weaning
and 10g/day post weaning
Daily gain
Feed efficiency
Clostridium coccoides–
Eubacteriumrectale group was higher
in the feces
(Uneyo et al.,2015)
Veal calves
Calf milk replacer with
and without 3 or 6 g of
scFOS
Growth performance
Carcass quality
Faecalconc of SCFAs
Microbial fermentation
(Grand et al.,2013)
Calves
mannan oligosaccharide
(MOS) mixed in the
whole milk @ 4 g of Bio-
Mos per calf daily
consumed 19.9% more calf starter
BW gain
(Hasunuma et al.,
2011)
Young
calves
MOS @ 4 g/d of Bio-Mos
Stimulated calf starter intake.
Presence of Cl. Perfringens and
E.coli, and Salmonella spp. and
Cryptosporidium spp. not effected
effect
(Terre et al., 2007)
Calves
MOS in milk replacer @
2-4 g/day/head
Prevents the bacteria from attaching
to intestinal epithelial cells
(Karol et al., 2011)
Calves
MOS milk replacer @ 4g
/day/head
Better growth performance
FCR Scour
Feed cost/kg B wt gain
(Ghosh et al., 2011)
Neonatal
calves
Prebio-Support@ 20g/day
Enhance the immune system by
evoking a direct antibody response
(Heinrichs et al.,
2011)
Calves
Prebio Support containing
DHNA
Bifidobacter population
Fecal water , fecal ammonia and
S
SCFAs Fecal Consistency better
(Fujisawa et al.,
2009)
Macrophage phagocytosis was also increased when calves were supplemented with β 1,4mannobiose
compared to control calves (Ibuki et al., 2010). An in vitro study in humans found an increase in
neutrophil oxidative burst response and microbicidal activity with beta glucan supplementation (Wakshull
et al., 1999). Peritoneal neutrophil respiratory burst activity and neutrophil number were also increased in
mice supplemented with oat beta glucan (Murphy et al., 2007).
The fermentation products produced by prebiotics such as butyrate (Nilsson et al., 2010), may indirectly
effect anti-inflammatory cytokines. Butyrate is one of the most prevalent fermentation products in the
rumen and has been shown to increase the production of anti-inflammatory cytokines (Schley and Field,
2002). Secretion of anti-inflammatory IL-10 was increased in elderly humans supplemented with
galactooligosaccharides (Vulevic et al., 2008).Fructooligosaccharide-supplemented rats had increased
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TGF-β in cecal tissue compared with control rats as well as an increase in commensal microflora counts,
Lactobacilli and Bifidobacteria (Hoentjen et al., 2005).
Antibody production of IgA which plays a role in mucosal immunity and IgG, important in memory
responses, may also be influenced by prebiotics. Ileal IgA concentrations from dogs supplemented with
both mannan oligosaccharides and fructooligosaccharides were increased compared with control animals
in a study done by Swanson et al., 2002. Secretion of IgA in peyer’s patch cells of fructooligosaccharide-
supplemented mice with was increased in a dose-dependent manner compared with controls (Hosono et
al., 2003). Hydrolyzed yeast-fed neonatal calves challenged with both Hog cholera, a viral pathogen, and
Erysipelothrixinsidiossa, a bacterium, had increased bacterial- and viral-specific IgA and IgG
concentrations compared with challenged calves without supplementation (Kim et al., 2011). Increases in
total IgG have also been observed. Beta glucan supplementation increased total IgG concentrations of
immunosuppressed mice (Yun et al., 1997). Serum IgG concentrations were improved by 32% and 23%
compared to controls in two trials involving mannan oligosaccharide-supplemented piglets (Lazarevic et
al., 2010). In a third trial by the same researcher, Holstein calves fed mannan oligosaccharides had an
increase in serum IgG concentrations of 39% (Lazarevic et al., 2010).
Conclusion
Dietary supplementation of prebiotics is a valuable approach in improving gut health attributes like
bifidogenecity, hindgut fermentation, gut mucosal integrity, mineral bioavailability, lipid and glucose
homeostasis and immune response. They have added benefits in terms of easy accessibility, easier
integration into feeding system and exploitation of non-viable dietary components. Moreover, they can be
fortified in wide range of feeds. However, to obtain optimal results, standardization concerning specific
choice of prebiotic, dietary inclusion level, adaptation period, chemical structure (degree of
polymerization, linear or branched, type of linkages between monometric sugars), origin of prebiotic,
route of administration, animal factor (species, age, stage of production and health status) and proper
managemental care is required. In this perspective it would be possible to compare data from different
experiments and to provide the basis for more refined clinical trials. Future research required focusing on
determining the mechanism of action, evaluating prebiotic interaction and elucidating how the genetic and
bacterial profiles of the host can influence treatment responsiveness. Moreover, as better information on
structure to function information accrues as well as individual metabolic profiles of target bacteria are
compiled, it may be easier to select prebiotics for specific purpose. With the new generation of molecular
microbiological tools now becoming available, it will be possible to gain definitive information on the
species rather than genera that are influenced by the test prebiotic. The more we identify and characterize
the bacterial genera, species and even strains that compose the intestinal microbiota, the more we can
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understand both qualitatively and quantitatively, changes in that composition, their physiological roles
and mechanisms of effects. Good management practices to optimize nutrition, immune status, and
decrease the risk of disease are vital. The use of prebiotics may be a viable option to increase the
proliferation of commensal bacteria in the gastrointestinal tract, modulate feeding behavior, and increase
immune function to optimize calf health.
References
1. Berg, R. D. 1985. Indigenous intestinal microflora and the host immune response. EOS J. Immunol.
Immunopharmacol., 4: 161–168.
2. Bach, A., Tejero, C. and Ahedo, J. 2011. Effects of group composition on the incidence of respiratory
afflictions in group-housed calves after weaning. J. Dairy Sci. 94:2001-2006.
3. Ballou, C.E. 1970. A study of the immunohistochemistry of three yeast mannans. J. Biol. Chem.
245:1197-1203.
4. Ballou, M.A. 2015. Dietary strategies to improve the health of dairy calves. Pages 91-102 in Proc. of
the Rum. Nutr. Symp., Gainesville, Fla.
5. Bodera, P. 2008. Influence of prebiotics on the human immune system (GALT). Recent Pat. Inflamm.
Allergy Drug Discov. 2:19-153.
6. Bouhnik, Y., Attar, A., Joly, F. A., Riottot, M., Dyard, F., and Flourié, B. 2004. Lactulose ingestion
increases faecal bifidobacterial counts: a randomised double-blind study in healthy humans. Eur J
ClinNutr. 58, 1658-1664.
7. Brown, G.D. and Gordon, S. 2003. Fungal β-glucans and mammalian immunity. Immunity. 19:311-
315.
8. Cho, J.H., Zhao, P.Y. and Kim, I.H. 2011. Probiotics as a Dietary Additive for Pigs. J Anim Vet
Adv.10: 2127-2134.
9. Cota, M.A. and Whitefield, T.R. (1998) Xylooligosaccharides utilization by ruminal anaerobic
bacterium Selemonasruminantium. Curr Microbiol. 36:183-189.
10. Delgado, G.T.C., Tamashiro, W.M.S.C., Junior, M.R.M., Moreno, Y.M.F. and Pastore, G.M. 2011.
The putative effects of prebiotics as immunomodulatory agents. Food Res. Int. 44:3167-3173.
11. Dvorak, R. A., and Jacques, K. A. 1997. Effect of adding mannan oligosaccharide (BioMos) to the
milk replacer for calves. J. Anim. Sci. 75(1):22.
12. Dvorak,R.A., Jacques, K. A. and Newman, K. E. 1998. Mannanoligosaccharide, fructooligosaccharide
and Carbadox for pigs 0-21 days post-weaning. J. Anim. Sci. 76(2):64.
13. Fanelli, A. 2012. Direct-Fed Microbials (DFMs) in horses and poultry: effects on digestibility,
nutritional value of animal products and animal health. Graduate School of Veterinary Sciences for
Animal Health and Food Safety. Doctoral Program in Animal Nutrition and Food Safety.
Universitàdegli Studi di Milano.
14. Fleige, S., Preißinger, W., Meyer, H. H. D. and Pfaffl, M. W. 2007. Effect of lactulose on growth
performance and intestinal morphology of pre-ruminant calves using a milk replacer containing
Enterococcus faecium. Animal. 1:367–373.
15. Franklin, S.T., Newman, M.C., Newman, K.E. and Meek, K.I. 2005. Immune parameters of dry cows
fed mannan oligosaccharide and subsequent transfer of immunity to calves. J. Dairy Sci. 88:766-775.
16. Friman, V., Adlerberth, I., Connell, H., Svanborg, C., Hanson, L.A. and Wold, A.E. 1996. Decreased
expression of mannose-specific adhesins by Escherichia coli in the colonic microflora of
immunoglobulin A-deficient individuals. Infect. Immun. 64:2794-2798.
17. Fujisawa, T., Sadatoshi, A., Ohashi, Y., Orihashi, T., Sakai, K., Sera, K. and Kanbe, M. 2010.
Influences of Prebio Support™ (Mixture of Fermented Products of Lactobacillus gasseriOLL2716 and
PropionibacteriumfreudenreichiiET-3 on the Composition and Metabolic Activity of Fecal Microbiota
International Journal of Livestock Research eISSN : 2277-1964 NAAS Score -5.36
Vol 7 (8) Aug’17
Hosted@www.ijlr.org DOI 10.5455/ijlr.20170610051314
Page14
in Calves. Bioscience Microflora. 29 (1): 41–45.
18. Gantner, B.N., Simmons, R.M. and Underhill, D.M. 2005. Dectin-1 mediates macrophage recognition
of Candida albicans yeast but not filaments. Embo J. 24:1277-1286.
19. Garcia-Vieyra, M.I., del Real, A. and Lopez, M.G. 2014. Agave fructans: Their effect on mineral
absorption and bone mineral content. J. Med. Food. 17: 1247-1255.
20. Ghosh, S., and Mehla, R.K. 2012. Influence of dietary supplementation of prebiotics
(mannanoligosaccharide) on the performance of crossbred calves. Trop Anim Health Prod. 44:617-
622.
21. Giannella, R.A. 1983. Escherichia coli heat stable enterotoxin: Biochemical and physiological -
effects in the intestine. Proc. in Food and Nutrition Sciences. 7:147-153.
22. Gibson, G. R. 1999. Dietary modulation of the human gut microflora using the prebiotics oligofructose
and inulin. J. Nutr. 129:1438–1441.
23. Gibson, G.R. and Roberfroid, M.B. 1995. Dietary modulation of the human colonic microbiota:
Introducing the concept of prebiotics. J. Nutr. 125:1401-1412.
24. Gibson, G.R., Beatty, E.R., Wand, X. and Cumings, J.H. 1995. Selective stimulation of Bifidobacteria
in the human colon by oligofructose and inulin. Gastroenterology. 108, 975-982.
25. Grand, E., Respondek, F., Martineau, C., Detilleux, J. and Bertrand, G.2013. Effects of short-chain
fructooligosaccharides on growth performance of preruminant veal calves. J Dairy Sci. 96(2):1094-
101.
26. Hardy H., Harris J., Lyon E., Beal J. and FoeyA D. 2013. Probiotics, Prebiotics and
Immunomodulation of Gut Mucosal Defences: Homeostasis and Immunopathology. Nutrients. 5(6):
1869–1912.
27. Hartemink, R., Van Laere, K.M.J. and Rombouts, F.M. 1997. Growth of enterobacteria on fructo-
oligosaccharides. J. Appl. Microbiol. 83:367–374.
28. Hasunuma, T., Kawashima, K., Nakayama, H., Murakami, T., Kanagawa, H., Ishii, T., Akiyama, K.,
Yasuda, K., Terada, F. and Kushibiki, S. 2011. Effect of cellooligosaccharide or synbiotic feeding on
growth performance, fecal condition and hormone concentrations in holstein calves. AnimSci
J. 82:543–548.
29. Heinrichs, A.J., Jones, C.M., Elizondo-Salazar, J.A. and Terrill, S.J. 2009. Effects of a prebiotics
supplement on health of neonatal dairy calves. Livest. Sci. 125:149-154.
30. Heinrichs, A.J., Jones, C.M. and Heinrichs, B.S. 2003. Effects of mannan oligosaccharide or
antibiotics in neonatal diets on health and growth of dairy calves. J. Dairy Sci. 86:4064-4069.
31. Hill, T.M., Bateman, H.G., Aldrich, J.M. and Schlotterbeck, R.L. 2008. Oligosaccharides for dairy
calves. Prof. Anim. Sci. 24:460-464.
32. Hoentjen, F., Welling, G.W., Harmsen, H.J.M., Zhang, X., Snart, J., Tannock, G.W., Lien, K.,
Churchill, T.A., Lupicki, M. and Dieleman, L.A. 2005. Reduction of colitis by prebiotics in HLA-B27
transgenic rats is associated with microflora changes and immunomodulation. Inflamm. Bowel Dis.
11:977-985.
33. Hoffmann,K. and Bircher, J. 1969. Veränderung der bakteriellen
DarmbesiedelungnachLaktulosegaben. Schweizerische Medizinische Wochenschrift, 99, 608-609.
34. Hosono, A., Ozawa, A., Kato, R., Ohnishi, Y., Nakanishi, Y., Kimura, T. and Nakamura, R. 2003.
Dietary fructooligosaccharides induce immunoregulation of intestinal IgA secretion by murine peyer’s
patch cells. Biosci. Biotechnol. Biochem. 67:758-764.
35. Hulbert and Ballou, 2012. Innate immune responses and health of individually reared Holstein calves
after placement into transition-pens 23 d after weaning. J. Dairy Res. 79:333-340.
36. Ibuki, M., Kovacs-Nolan, J., Fukui, K., Kanatani, H. and Mine, Y. 2010. β 1-4 mannobiose enhances
in Neonatal Diets on Health and Growth of Dairy Calves. J. Dairy Sci. 86:4064–4069.
37. Jenkins, D. J. A., Kendall, C. W. C. and Vuksan, V. 1999. Inulin, oligofructose and intestinal function.
J. Nutr. 129: 1431–1433.
38. Kelly - Quagliana K.A., Buddington R.K., Van Loo J., Nelson P.D. (1998). Immunomodulation by
International Journal of Livestock Research eISSN : 2277-1964 NAAS Score -5.36
Vol 7 (8) Aug’17
Hosted@www.ijlr.org DOI 10.5455/ijlr.20170610051314
Page15
oligofructose and inulin. Faseb J., 12, pp. 904.
39. Kim, M.H., Seo, J.K., Yun, C.H., Kang, S.J., Ko, J.Y. and Ha, J.K. 2011. Effects of hydrolyzed yeast
supplementation in calf starter on immune responses to vaccine challenge in neonatal calves. Animal.
5:953-960.
40. Kleesen, B., Hartmann, C. and Blaut, M. 2001. Oligofructose and long-chain inulin: influence on the
gut microbial ecology of rats associated with human faecal flora. Br. J. Nutr. 80:1-11.
41. Kolida, S. and Gibson, G. R. 2007. Prebiotic Capacity of Inulin-Type Fructans.J. Nutr. 137: 2503–
2506.
42. Korzenik, J.R. andPodolsky, D. K. 2006. Selective use of selective nonsteroidal anti-inflammatory
drugs in inflammatory bowel disease. Clin Gastroenterol Hepatol. 4(2):157-9.
43. Lomax, A.R. and Calder, P.C. 2009. Prebiotics, immune function, infection and inflammation: a
review of the evidence. Br. J. Nutr. 101: 633–658.
44. Lazarevic, M., Spring, P., Shabanovic, M., Tokic, V. and Tucker, L.A. 2010. Effect of gut active
carbohydrates on plasma IgG concentrations in piglets and calves. Animal. 4:938-943.
45. MacDonald, T.T.2003, The mucosal immune system. Parasite Immunol. 25(5), 235-246.
46. MacFarlane, S., MacFarlane, G. T. and Cummings, J. H. 2006. Prebiotics in the gastrointestinal tract.
Aliment. Pharmacol. 24, 701-714.
47. Magalhães, V.J.A, Susca, F., Lima, F.S., Branco, A.F., Yoon, I. and Santos, J.E.P. 2008. Effect of
feeding yeast culture on performance, health, and immunocompetence of dairy calves. J. Dairy Sci.
91:1497-1509.
48. Manetti, R., Parronchi, P., Giudizi, M.G., Piccinni, M.P., Maggi, E., Trinchieri, G. and Romagnani, S.
1993. Natural killer cell stimulatory factor (IL-12) induces T helper type 1 (Th1)-specific immune
responses and inhibits the development of IL-4-producing Th cells. J. Exp. Med. 177:1199-1204.
49. Masanetz, S., Preißinger, W., Meyer, H. H. D. and Pfaffl, M. W. 2011. Effects of the prebiotics inulin
and lactulose on intestinal immunology and hematology of preruminant calves. Animal. 5(7):1099–
1106.
50. McDonald, P., Edwards, R.A., Greenhalgh, J.F.D., Morgan, C.A. and Sinclair, L.A.2010. Animal
Nutrition (7th edn.) Pearson Books.
51. McGuirk, S.M. 2008. Reducing dairy calf mortality. Pages 126-131 in Proc. of the AABP Annual
Conf., Charlotte, NC.
52. McGuirk, S.M. 2010. Approaches to enhancing the gastrointestinal health of calves. Pages 16-21 in
Proc. of the AABP Annual Conf., Albuquerque, NM.
53. Milewski, S., Wójcik, R., Małaczewska, J., Trapkowska, S. and Siwicki, A.K. 2007: Effect of β-
1.3/1.6-D-glucan on meat performance and non-specific humoral defense mechanisms in lambs. Med
Wet 3: 36-363
54. Mitsuoka, T., Hidaka, H. and Eida, T. 1987. Effect of fructo-oligosaccharides on intestinal microflora.
Nahrung. 31(5-6):427-36.
55. Mizota, T. 1996. Lactulose as a growth promoting factor for Bifidobacterium and its physiological
aspects. Bull. Int. Dairy Fed. 313:43-48.
56. Mizota, T., Mori, T., Yaeshima, T., Yanagida, T., Iwatsuki, M. and Ishibashi, N. 2002. Effects of low
dosages of lactulose on the intestinal function of healthy adults. Milchwissenschaft, 57: 312-315.
57. Mowat, A. M., and Viney, J. L. 1997. The anatomical basis of intestinal immunity. Immunol. Rev.
156:145–166.
58. Mowat, A.M. 2003. Anatomical basis of tolerance and immunity to intestinal antigens. Nat Rev
Immunol 3: 331–341.
59. Murphy, E.A., Davis, J.M., Brown, A.S., Carmichael, M.D., Ghaffar, A. and Mayer, E.P. 2007. Oat β-
glucan effects on neutrophil respiratory burst activity following exercise. Med. Sci. Sport Exer.
39:639-644.
60. Niness, K.R. 1999. Inulin and oligofructose: What are they? J. Nutr. 129: 1402–1406.
61. Neth, O., Jack, D.L., Johnson, M., Klein, N.J. and Turner, M.W. 2002. Enhancement of complement
International Journal of Livestock Research eISSN : 2277-1964 NAAS Score -5.36
Vol 7 (8) Aug’17
Hosted@www.ijlr.org DOI 10.5455/ijlr.20170610051314
Page16
activation and opsonophagocytosis by complexes of mannose-binding lectin with mannose-binding
lectin-associated serine protease after binding to Staphylococcus aureus. J. Immunol. 169:4430-4436.
62. Novak, J., and Katz, .J. A. 2006. Probiotics and prebiotics for gastrointestinal infections. Curr. Infect.
Dis. Rep. 8:103.–109.
63. Ofek, I., Mirelman, D. and Sharon, N. 1977. Adherence of Escherichia coli to human mucosal cells
mediated by mannose receptors. Nature. 265:623-625.
64. Ohta, A., Motohashi, Y., Sakai, K., Hirayama, M., Adachi, T. and Sakuma, K. 1998. Dietary
fructooligosaccharides increase calcium absorption and levels of mucosal calbindin-D9k in the large
intestine of gastrectomized rats. Scand. J. Gastroenterol. 33:1062-1068.
65. Patel, S. and Goyal, A. 2012. The current trends and future perspectives of prebiotics research: a
review. Biotech. 2:115-125.
66. Quigley, J. D., Drewry, J. J., Murray, L. M. and Ivey, S. J. 1997. Body weight gain, feed efficiency,
and fecal scores of dairy calves in response to galactosyl-lactose or antibiotics in milk replacers. J.
Dairy Sci. 80:1751–1754.
67. Quigley, J.D., Kost, C.J. and Wolfe, T.A. 2002. Effects of spray-dried animal plasma in milk replacers
or additives containing serum and oligosaccharides on growth and health of calves. J. Dairy Sci.
85:413-421.
68. Roller, M., Rechkemmer, G. and Watzl, B. (2004). Prebiotic inulin enriched with oligofructose in
combination with the probiotics Lactobacillus rhamnosus and Bifidobacteriumlactis modulates
intestinal immune functions in rats. J. Nutr. 134: 153–156.
69. Roodposhti, P.M. and Dabiri, N. 2012. Effects of probiotic and prebiotic on average daily gain, fecal
shedding of Escherichia Coli, and immune system status in newborn female calves. Asian-Aust. J.
Anim. Sci. 25:1255-1261.
70. Russo, P., López, P., Capozzi, V., Fernández de Palencia, P., Dueñas, M.T., Spano, G. and Fiocco, D.
2012. Beta-glucans improve growth, viability and colonization of probiotic microorganisms. Int. J.
Mol. Sci. 13:6026-6039.
71. Sabater-Molina, M., Larque, E., Torrella, F. and Zamora, S. 2009. Dietary fructooligosaccharides and
potential benefits on health. J Physiol Biochem. 65:315–328.
72. Salak-Johnson, J.L. and McGlone, J.J. 2014. Making sense of apparently conflicting data: Stress and
immunity in swine and cattle. J. Anim. Sci. 85:81-88.
73. Schley, P.D. and Field, C.J. 2002. The immune-enhancing effects of dietary fibres and prebiotics. Br.
J. Nutr. 87(2):S221-S230.
74. Schouten, B.W. 2005. Calf rearing – a review of the prevention and treatments of disease of this
valuable calf. Side papers. http://www.side.org.nz/Papers
75. Schumann, C. 2002. Medical, nutritional and technological properties of lactulose. An update. Eur J
Nutr. 41 (1): 17–25.
76. Schuster-Wolff-Bühring, R., Fischer, L. and Hinrichs, J. 2010. Production and physiological action of
the disaccharide lactulose. Int Dairy J. 2(11):731-741.
77. Seki, N., Hamano, H., Iiyama, Y., Asano, Y., Kokubo, S. and Yamauchi, K. (2007). Effect of lactulose
on calcium and magnesium absorption: a study using stable isotopes in adult men. J Nutr Sci
Vitaminol. 53, 5-12.
78. Sonck, E., Stuyven, E., Goddeeris, B. and Cox, E. 2009. Identification of the porcine C-type lectin
dectin-1. Vet. Immunol. Immunopathol. 130:131-134.
79. Spring, P., Wenk, C., Dawson, K.A. and Newman, K.E. 2000. The effects of dietary
mannanonoligosaccharides on cecal parameters and the concentrations of enteric bacteria in the ceca
of Salmonella-challanged broiler chicks. Poultry Sci. 79:205- 211.
80. Srinivasjois, R., Rao, S. and Patole, S. 2009. Prebiotic supplementation of formula in preterm
neonates: a systematic review and meta-analysis of randomized controlled trials. Clin Nutr. 28:237–
242.
81. Swanson, K.S., Grieshop, C.M., Flickinger, E.A., Bauer, L.L., Healy, H.P., Dawson, K.A., Mercher,
International Journal of Livestock Research eISSN : 2277-1964 NAAS Score -5.36
Vol 7 (8) Aug’17
Hosted@www.ijlr.org DOI 10.5455/ijlr.20170610051314
Page17
N.R. and Fahey, G.C. 2002. Supplemental fructooligosaccharides and mannanoligosaccharides
influence immune function, ileal and total tract nutrient digestibilities, microbial populations, and
concentrations of protein catabolites in the large bowel of dogs. J. Nutr. 132:980-989.
82. Terré, M., Calvo, M.A., Adelantado, C., Kocher, A. and Bach, A. 2007. Effects of mannan
oligosaccharides on performance and microorganism fecal counts of calves following an enhanced-
growth feeding program. Anim. Feed Sci. Technol. 137:115-125.
83. Trushina, E.N., Marynova, E.A., Nikitiuk, D.B., Mustafina, O.K. and Baigarin, E.K. 2005. The
influence of dietary inulin and oligofructose on the cell-mediated and humoral immunity in rats. Vopr.
Pitan. 74:22-27.
84. Uyeno, Y, Shigemori, S. and Shimosato, T. 2015. Effect of Probiotics/Prebiotics on Cattle Health and
Productivity. Microbes Environ. 30(2): 126–132.
85. Van Loo, J, Coussement, P. , de Leenheer, L., Hoebregs, H. and Smits, G. 1995. On the presence of
inulin and oligofructose as natural ingredients in the Western diet. Crit Rev Food Sci Nutr . 35: 525–
552.
86. Vetvicka, V. and Yvin, J. 2004. Effects of marine β-1,3glucan on immune reactions. Int.
Immunopharmacol. 4:721-730.
87. Vos, A.P., Knol, J., Stahl, B., M'Rabet, L. and Garssen, J. 2010. Specific prebiotic oligosaccharides
modulate the early phase of a murine vaccination response. Int Immunopharmacol. 10(5):619–25.
88. Vulevic, J., Drakoularakou, A., Yaqoob, P., Tzortzis, G. and Gibson, G.R. 2008. Modulation of the
fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-
GOS) in healthy elderly volunteers. Am. J. Clin. Nutr. 88:1438-1446.
89. Watzl, B., Girrbach, S. and Roller, M. 2005. Inulin, oligofructose and immunomodulation. Brit. J.
Nutr. 93: 49–55.
90. Wakshull, E., Brunke-Reese, D., Lindermuth, J., Fisette, L., Nathans, R.S., Crowley, J.J., Tufts, J.,
Mackin, W. and Adams, D.S. 1999. PGG-glucan, a soluble beta-(1,3)-glucan, enhances the oxidative
burst response, microbial activity, and activates an NF-kappa B-like factor in human PMN: evidence
for a glycosphingolipid beta-(1,3)-glucan receptor. Immunopharmacology. 41:89-107.
91. Wang, Z., Guo, Y., Yuan, J. and Zhang, B. 2008. Effect of dietary β-1,3/1,6-glucan supplementation
on growth performance, immune response and plasma prostaglandin E2, growth hormone and ghrelin
in weanling piglets. Asian-Aust. J. Anim. Sci. 21(5):707-714.
92. Wójcik, R., Małaczewska, J., Trapkowska,S.and Siwicki, A.K. 2007. Influence of ß-1,3/1,6-D- glucan
on non-specific cellular defence mechanisms in lambs. Med. Weter.63: 84–86.
93. Yasuda, K., Roneker, K.R., Miller, D.D., Welch, R.M. and Lei, X.G. 2006. Supplemental dietary
inulin affects the bioavailability of iron in corn and soybean meal to young pigs.J. Nutr. 136: 3033-
3038.
94. Yun, C.H., Estrada, A., VanKessel, A., Gajadhar, A.A., Redmond, M.J. and Laarveld, B. 1997. Β-(1-
3, 1-4) oat glucan enhances resistance to Eimeriavermiformis infection in immunosuppressed mice.
Int. J. Parasitol. 27:329-337.