The use of Lactobacillus as an alternative of antibiotic growth promoters in pigs: a
Runjun Dowarah, A.K. Verma, Neeta Agarwal
Reference: ANINU 125
To appear in: Animal Nutrition Journal
Received Date: 19 August 2016
Revised Date: 28 October 2016
Accepted Date: 5 November 2016
Please cite this article as: Dowarah R, Verma AK, Agarwal N, The use of Lactobacillus as an alternative
of antibiotic growth promoters in pigs: a review, Animal Nutrition Journal (2016), doi: 10.1016/
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The use of Lactobacillus as an alternative of antibiotic growth promoters in pigs: a review
, A.K. Verma and Neeta Agarwal
CAFT in Animal Nutrition, Indian Veterinary Research Institute, Izatnagar-243122, India
E-mail address: firstname.lastname@example.org
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Antibiotics often supplemented in feed, used as a growth promoter may cause their
residual effect in animal produce and also trigger antibiotic resistance in bacteria, which is of
serious concern among swine farming entrepreneurs. As an alternative, supplementing probiotics
gained interest in recent years. Lactobacillus being most commonly used probiotic agent which
improves growth performance, feed conversion efficiency, nutrient utilization, intestinal
microbiota, gut health and regulate immune system in pigs. The characteristics of Lactobacillus
spp. and their probiotic effects in swine production are reviewed here under.
Key words: Diarrhea score, Gut microbiota, Lactobacilli, Probiotics
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Various stress factors including nutritional, environmental and weaning etc. at different
stages of life affect the animal productivity and health. Weaning stress in piglets being the major
cause for economic loss to pig farmers (Wilson et al., 1989). As the weaned piglets have limited
digestive capacity, which triggers fermentation of undigested protein by opportunistic pathogens
(mainly Escherichia coli, Salmonella) normally existing in gastrointestinal tract (GIT) which
leads to production of branch chain fatty acids (BCFA) and ammonia nitrogen (Garcia et al.,
2014). The BCFA and NH
-N are the toxic metabolites to intestinal mucosa, which damage
intestinal mucosa thereby ultimately results in diarrhea (Fuller, 1989; Jensen, 1998). This may
usually causes a reduction in villous height and digestive enzyme activity for the first few days
after weaning (Pluske et al., 1995). The common practice of supplementing antibiotics in
livestock for improved animal performance was condemned due to its adverse effects on animal
as well as human, the ultimate consumer of the animal produce. Since then, it has been the
greatest challenge to farmers to rear healthy piglets devoid of antibiotics supplementation.
However, these stress factors in livestock sector need to be addressed for profitable livestock
In this scenario, latest reports indicate probiotic supplementation in swine seems to be
better alternative for antibiotic use addressing the safe animal produce as well as to combat
economic losses in pig farming. The term “Probiotics” is derived from a Greek word ‘biotikos’
meaning ‘for live’, which was first coined by Parker (1974) and define as the live
microorganisms, when they were administered in adequate amounts, confer a health benefits on
the host (FAO/WHO, 2002). At present, probiotics are classified by the US Food and Drug
Administration as generally recognized as safe (GRAS) ingredients. Among various probiotic
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bacteria, Lactobacillus is most commonly used probiotic agent (McCony and Gilliland, 2007).
Lactobacilli are gram-positive, non-motile, non-spore forming, acid-tolerant, non-respiring rod
shaped (bacillus), or spherical (coccus) bacteria which produce lactic acids as the major
metabolic end-product of carbohydrate fermentation (Cho et al., 2009). In farm animal they
confer good intestinal health by stimulating the growth of a healthy microbiota (Walter, 2008),
preventing intestinal colonization of enteric pathogens (Huang et al., 2004; Lee et al., 2012),
reduced faecal noxious gas emission (Hong et al., 2002), production of antimicrobial substances,
antibiotic resistance patterns, improving digestive ability and antibody mediated immune
response, and demonstrable efficacy and safety (Wang et al., 2012; Hou et al., 2015). Probiotics
are generally host-species specific (Dunne et al., 1999) and believed to be more effective in its
natural habitat i.e., target species (Kailasapathy and Chin, 2000). However, selection of probiotic
microbes is one of the most important criteria to get a positive response. The objective of this
paper is to enlighten the efficacy of various Lactobacillus spp. as probiotic in swine production.
2 Microorganism commonly used as probiotics
The microorganisms commonly used as probiotics in livestock are presented in Table 1.
The genus Lactobacillus has been reported as one of the major bacterial groups found in GIT
(Dibner and Richards, 2005). Till now, no report was found on safety concerns related to
Lactobacilli in animals. The genera Biﬁdobacteria is found to be inhabitant of GIT of both
animals and humans, which helps in maintaining microbial balance in the GIT by reducing the
harmful pathogenic microbes thereby, associated with good health status of the host (Huang et al.,
2004). The genus Enterococcus belongs to the lactic acid bacteria (LAB) group and found
naturally in food products, which are normal commensals of human and animal. E. faecium is the
most common in the animal GIT, while in human E. faecium and E. faecalis are prevalent
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(Fisher and Phillip, 2009). These three species of Enterococcus are commonly used probiotics in
animal/ livestock feeding.
Bacillus are Gram-positive, spores-forming microorganisms, commonly associated with
soil, water and air, and present in the intestinal tract due to involuntary ingestion of contaminated
feed. Though some of the Bacillus species are used as a probiotic, speculation exists for their
ability to produce toxins (Gaggia et al., 2010).The yeasts are also comprised as a residual
microbial system of the intestinal microbiome where Saccharomyces cerevisiae is widely present
in the nature and used in food and beverage industry for its fermentation properties. It is also
used as a probiotic especially in ruminants and pig feeding (Kumar et al., 2012).
3 Mode of action of Lactobacilli as probiotic
Lactobacilli stimulate rapid growth of beneficial microbiota in the GIT which become
abundant and induce competitive exclusion of pathogenic bacteria either by occupying binding
sites on intestinal mucosa or competing for nutrients and absorption sites with pathogenic
bacteria (Malago and Koninkx, 2011; Zhao and Kim, 2015); by rapid utilization of energy source
which may reduce the log phase of bacterial growth. Most of the enteric pathogens adhere to the
intestinal epithelium through colonization thereby develop diseases (Walker, 2000).
Consequently, the probiotic lactobacilli have the ability to adhere the gut epithelium and thus
compete with pathogens for adhesion receptors i.e., glycol-conjugates (Umesaki et al., 1997).
Probiotic bacteria produce organic acids, hydrogen peroxide, lactoferrin and bacteriocin which
may exhibit either bactericidal or bacteriostatic properties (Jin et al., 1997; Pringsulaka et al.,
2015). Lactobacillus have proven to be capable of acting as immune-modulators by enhancing
macrophage activity (Perdigon et al., 1986), increasing the local antibody levels (Yasui et al.,
1989), inducing the production of interferon (De Simone et al., 1986) and activating killer cells
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(Kato et al., 1984). They prevent the proliferation of coliform bacteria thus amine production
diminishes which produced due to decarboxylation of amino acids by coliform bacteria.
4 Selection of lactobacilli for feeding as Probiotics
The followings are the criteria that can be used for the selection of microbial strains as
1) Resistance to in vitro/in vivo conditions: they should be resistant to acidic pH and bile
salt. After administration, the microbes should not be killed by the defense mechanisms of
the host and should be resistant to the specific conditions occurring in the body.
2) Origin of the strain: Probiotics are generally host-species specific (Dunne et al., 1999). It
is believed that probiotic organism is more effective if it is naturally occurring in the target
species (Kailasapathy and Chin, 2000). The strains should be properly isolated and identified
3) Biosafety: Lactobacillus, Bifidobacteria and Enterococcus are the microbes which fall in
the category of generally recognized as safe (GRAS) and are most widely used
microorganisms as probiotics.
4) Viability/survivability and resistance during processing (e.g., heat tolerance or storage):
Thermophilic/thermo-tolerant organisms have an advantage as they withstand higher
temperature during processing and storage.
However, other criteria might also be considered for selection of mono or multi strains
bacteria as probiotics like as probiotic-symbiotic interaction, stimulation of healthy microbiota
and suppression of harmful bacteria. Adopting these predetermined criteria, it could be possible
to select the best strains of probiotics which could be effective therapeutically and nutritionally.
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5 Mode of feeding probiotics
Mode of feeding probiotic affects the response of animal to the probiotic feeding.
Generally cultures are fed either in form of lyophilized powder or live cells. When a lyophilized
culture fed to the animal, it has to rejuvenate before expressing its biological activity which takes
some time and also the viability of the culture is not assured. Whereas, when live culture is fed,
the probiotic starts its biological activity immediately and the viability of the culture is assured.
Further, cells can lose their viability and metabolic activity during lyophilisation. Therefore, a
probiotic product is effective only when it contains viable as well as metabolic active cells.
6 Use of probiotic Lactobacilli spp. for swine production
Lactobacillus spp. has been reported as one of the major bacterial groups found in
porcine gastrointestinal tract (Dibner and Richards, 2005). But all the species and strains of
Lactobacillus cannot be equally effective as probiotic. Different species and even strains of
species of microbes behave differently (Newbold et al., 1995). Therefore, source of microbe to
be used as probiotic is one of the important factors to yield good response. A microbe fed
exogenously as probiotic when enters the GIT has to compete with existing microbiome
ecosystem in GIT (Verdenelli et al., 2009). These unfavorable circumstances in the GIT may
hamper the proliferation of the microbe used as probiotic. To combat this problem, it is
suggested that the microbe isolated from the host animal when used as probiotic gives better
response. Host specificity was observed among Lactobacilli isolated from human and animal
sources (Morelli, 2000). Hence, evaluating new sources of probiotics from swine origin is utmost
necessary to improve pig farming. Lactobacillus acidophilus 30SC isolated from swine showed
excellent acid resistance and bile tolerance compared to commercial probiotics strains that are
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presently used in dairy products (Oh et al., 2011). The scenario of using LAB as probiotic for
swine production is illustrated considering recent reports across the world (Figure 1 & Table 2).
6.1 Improved performance
In swine, the use of probiotics improves intestinal well-being which leads to improve
performance. Higher growth rate and improved feed efficiency ratio results in improve
profitability due to greater output and reduction in overhead costs (Campbell, 1997). However,
age and weight at weaning are closely related to post-weaning growth rate. The administration of
probiotics, soon after birth could be effective as probiotic bacteria by enhancing intestinal barrier
function which restrict colonization of pathogenic bacteria to intestinal mucosa. This is evident
with better absorption of nutrients and immunoglobulins of the colostrum, enabling better
sustainability of the piglet, and minor loss of piglets at its first days of life (Abrahao et al., 2004).
Supplementation of lactobacilli has resulted in improved growth and feed efficiency in nursery
(Fialho et al., 1998) and weaning (Mishra et al., 2014) piglets.
A healthy intestinal tract has a dominance of LAB, however, this equilibrium within the
intestinal tract is troubled when the animal is in stressful condition like castration, weaning, high
temperature and humidity and change of feed (Jin et al., 1997). This could be improved by
continuous feeding of lactobacilli, which encourages rapid growth of other beneficial bacteria
and reduce the growth of pathogenic bacteria by competitive exclusion (Pan and Yu, 2014).
Feeding of probiotics (Lactobacillus spp.) to weaning piglets resulted in an increased growth rate
due to high feed intake and better feed conversion ratio. Supplementation of complex probiotics,
including yeast (Saccharomyces cerevisiae) and Lactobacillus spp. have been reported to
improve growth performance of weaned piglets (Hong et al., 2002; Chen et al., 2005). Positive
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effects on growth, feed conversion efficiency and nutrient digestibility were also observed in
grower-finisher pigs with supplementation of probiotic Bacillus subtilis, Saccharomyces
boulardi and L. acidophilus C3 (Giang et al., 2011). Where, the effect of probiotic (Lactobacillus
reuteri) in weaning piglets was comparable with antimicrobial growth promoter (Apramycin) in
gain, feeding efficiency and nutrient digestibility (Ahmed et al., 2014). This might be due to
increase activity of digestive enzymes like β-galactosidase by the supplementation of lactobacilli,
which stimulate gastrointestinal peristalsis and promote apparent nutrient digestibility (Wang et
al., 2011; Zhao and Kim, 2015).
Effect of probiotic was also observed in sow with increased feed intake, number and
growth of piglets at weaning (Pollmann et al., 2005) and also improve composition of milk
(Alexopoulos et al., 2004). There is a lack of study conducted on sow to see the effect of
lactobacilli as probiotics, so it important to give emphasis on research in this aspect for better
swine production. Supplementation of L. johnsonii XS4 (previously isolated from
gastrointestinal tract of sow) from 90
day of pregnancy up to weaning day (25th day of
lactation) significantly increased litter weight at birth, litter weight after 20 days of farrowing,
the number of piglets at weaning and weaning weight of piglets (Wang et al., 2014).
6.2 Control of Post-weaning Diarrhea
At the time of weaning, entero-pathogens takes upper hand as weaning of the piglets
reduce digestibility of high protein diet which results increase production of BCFA and ammonia
-N) leading to more incidence of diarrhea (Garcia et al., 2014). The BCFA and
-N are the main toxic metabolites for intestinal mucosa and tagger of post weaning diarrhea
in piglets (Williums et al., 2005). E. coli are the major enteropathogen of post-weaning diarrhea
and causes 26% cases of neonatal diarrhea (Hoefling, 1989). Addition of lactobacilli as probiotic
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in the diet results beneficial fermentation resulting increased concentration of short chin fatty
acids and lactic acid in GIT. These may reduce pH of the gut which in turn decrease growth of
opportunistic entero-pathogens as they need alkaline medium to proper growth and
6.3 Effect in intestinal microflora and gut health
Microflora in the digestive system plays a very important role in the defense mechanism
of the body. The major intestinal microflora of pig are Lactobacilli, Bifidobacteria, Streptococci,
Bacteriodes, Clostridiums perfringes and E. coli may vary with age. One of the important ability
of stable microflora in gastrointestinal tract is colonization resistance. About 4 to 6 weeks is
needed to establish a stable microflora in the GIT (Mul and Perry, 1994). However,
supplementation of Lactobacilli in neonatal piglets helps in early development of stable gut
microbflora, stimulation of immune system and prevents diarrhea. When piglets are weaned, the
intestinal microflora of piglets is altered due to dietary and environmental change after weaning
of piglets (Jensen, 1998). The entero-pathogenic E. coli are markedly increased in the anterior
small intestine resulting post weaning diarrhea. Oral administration of L. fermentum I5007 in
formula-fed piglets improved intestinal health and reduced the number of potential entero-
pathogens like E. coli and Clostridia in neonatal piglets (Liu et al., 2014). Addition of complex
lactobacilli previously isolated from GIT of piglet (L. gasseri, L. reuteri, L. acidophilus, L.
fermentum, L. johnsonii and L. mucosae) increased number of lactobacilli and bifidobacterium,
also reduced E. coli and aerobic bacteria counts in jejunum, ileum, cecum and colon mucosa
(Huang et al., 2004; Chiang et al., 2015). The effect was also persisted in grower-finisher pigs
(Giang et al., 2011). Since, lactobacilli produced lactic acid, hydrogen peroxide and lactoferrin
which may exhibit antagonistic activity against E. coli and Enterobacteria (Li et al., 2015). In
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addition, earlier report also revealed that dietary supplementation of complex of lactic acid
bacteria increased concentrations of lactic acid and acetic acid in ileum and colon (Giang et al.,
2010) of weaning piglets, whereas, faecal NH
-N and butyric acid concentration was decreased
in grower-finisher pigs (Chen et al., 2006). The increased concentration of lactic acid in
supplemented group lowered the gut pH in treated groups as lactic acid act as an acidifying agent
(Williams et al., 2005; Thu et al., 2011). This indicates that supplementation of various
Lactobacilli sp. modulates gut microbial profile and thereby affected microbial metabolite
production which results better gut health.
6.4 Improved immune status
The probiotics have the capacity to modulate the immune system of animal by enhancing
the systematic antibody response to soluble antigens in the serum (Christensen et al., 2002). The
immune-modulatory effects can even be achieved by dead probiotic bacteria or just probiotics
derived components like peptidoglycan fragments or DNA. Dietary supplementation with
probiotics enhanced humoral and cell mediated immune responses (Shu and Gill, 2002) with
increased the serum concentration of IgM (Dong et al., 2013) and IgG (Ahmed et al., 2014)
growing pigs. Probiotic supplementation in sow also increased IgG level in colostrum and
plasma of piglets (Jang et al., 2013). Since, probiotics facilitate the suppression of lymphocyte
proliferation and cytokine production by T cells which down regulating the expression of pro-
inflammatory cytokines such as tumor necrosis factor-α (Isolauri et al., 2001). L. fermentum
enhanced T-cell differentiation, induced cytokine expression in the ileum of E. coli challenged
piglets with increased pro-inflammatory cytokines and percentage of CD4
lymphocyte subset in
blood (Wang et al., 2009). However, it is difficult to confirm that probiotics contribute
significantly to the immune system of the host. The main reason behind this caveat is that
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probiotics differ from antibiotics in that they are not intended to eradicate invasive pathogens in
the gastrointestinal tract. Therefore, such observed improvements or positive effects are always
hindered due to the animal’s immune status and the various applied situations.
6.5 Antioxidant status
An abnormality in the antioxidant defense system can increase the susceptibility of pigs
to stress, resulting in decreased performance and reduced immune function. As a result of
incomplete reduction of oxygen, the reactive oxygen are formed which includes superoxide
anion, hydroxyl radical, hydrogen peroxide and singlet oxygen. A physiological concentration of
reactive oxygen species (ROS) is required for normal cell function, energy production,
phagocytosis and intercellular signaling regulation. Early weaning of piglets cause oxidative
stress by producing excessive quantities of ROS which not only damage proteins, lipids and
DNA but also decline intestinal antioxidant enzyme activities under NF-κB, p65 and Nrf2/
Keap1 signals (Yin et al., 2014; Yin et al., 2015). The probiotic cell have defenses mechanisms
against the damaging effects of ROS by involving both in enzymatic (superoxide dismutase and
catalase) and non-enzymatic components. The lactic acid bacteria diminish the activity of ROS
through the production of superoxide dismutase (Stecchini et al., 2001) that converts superoxide
radicals to oxygen and hydrogen peroxide. Some of the species of LAB may also produce
catalase, which can destroy hydrogen peroxide at a very high rate that blocks formation of
peroxyl radicals (Knauf et al., 1992) while some lactobacilli produced non-enzymatic
antioxidants such as glutathione and thioredoxin to reduce reactive oxygen intermediates (de
Vos, 1996). Supplementation of Lactobacilli sp. increased serum concentration of superoxide
dismutase, glutathione peroxidase and catalase in suckling (Cai et al., 2014) and weaning piglets
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(Wang et al., 2012) whereas, total antioxidant capacity, hepatic catalase, muscle superoxide
dismutase improved in grower-finisher pigs (Wang et al., 2009).
6.6 Effect on intestinal morphology
The gastrointestinal tract is the main digestive and absorptive organ in animal. The GIT
permits the uptake of dietary substances into systemic circulation and it also excludes pathogenic
compounds simultaneously (Gaskins, 1997). There is a reduction in villous height (villous
atrophy) and crypt depth at weaning (Pluske et al., 1996). As weaning leads to temporary
starvation which resulted villous atrophy, reduces mucosal protein content and digestive
McCracken and Kelly, 1984). Hence, improve feed intake immediately after
weaning reduced the histological changes of small intestinal morphology (Pluske et al., 1996).
As feeding of probiotic increased daily feed intake thus it had positive effect on development of
intestinal epithelium. However, the effects of probiotic on villus height may change depending
upon species of microorganism. Longer villi (V) height, deeper crypt (C) depth and smaller V: C
ratio was observed in pigs supplementation with L. acidophilus (Rodrigues et al., 2007), L.
plantarum (Suo et al., 2012) and P. acidolactici (Giancamillo et al., 2008). However, no change
in the crypt depth was observed with Enterococcus faecium (Scharek et al., 2007).
In conclusion, the data available from various studies and application of Lactobacilli in
swine husbandry clearly indicate that various Lactobacilli spp. have a great potential as an
alternative of antibiotics. More attention should be paid for utilizing effects of different probiotic
preparations and corresponding feeding strategy in pigs.
Conflict of interest
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The authors declare that they have no completing of interests.
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Table 1: List of microorganisms commonly used as probiotics in animal feed
Lactobacillus L. acidophilus
L. delbrueckii sub sp. bulgaricus
L. salivarius sub sp. thermophilus
Lactococus L. cremoris
Pediococcus P. acidilactici
P. pentosaceus subsp. pentosaceous
Bifidobacterium B. bifidum
Enterococcus E. faecium
Yeast Saccharomyces cerevisiae
Source: Dunne et al., 2001; Sekhon and Jairath, 2010
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Table 2: Effect of feeding different Lactobacillus sp. in various categories of pig
Used group Strain Effect of feeding Reference
Nursery piglets B. pseudolongum & L. acidophilus Improved weight gain, feed conversion and
fecal condition Abe et al., 1995
L. reuteri & Bifidobacterium
pseudolongum Better feed conversion ratio with no
differences in final weight, weight gain and
Afonso et al., 2013
L. fermentum Increased average daily gain; reduced
diarrhea incidence and numbers
of Clostridium sp; reduced mRNA
expression of IL-1β in the ileum
Liu et al., 2014
Weaned piglets L. gasseri, L. reuteri, L. acidophilus
& L. fermentum Better growth performance, increased
lactobacilli with decreased E. coli counts
and reduced post weaning diarrhea
Huang et al., 2004
L. reuteri, B. subtillis & B.
licheniformis Increased nutrient digestibility, reduced
faecal Salmonella and E. coli number,
improved serum IgG level
Ahmed et al., 2014
L. gasseri, L. reuteri, L. acidophilus
and L. fermentum Better ADG, ADFI and CP digestibility;
improved serum speciﬁc anti-OVA IgG Yu et al., 2008
L. fermentum Enhanced superoxide dismutase,
glutathione peroxidase and catalase Wang et al., 2012
Wang et al., 2009
L. reuteri, L. salivarius, L.
plantarum and Yeast complex Improved ADG, ADFI and gain/feed,
digestibility of DM and N Shon et al., 2005
E. faecium, L. acidophilus,
Pediococcus pentosaceus and L.
Improved growth, FCR, digestibility of
nutrients Giang et al., 2011
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