Ann. Anim. Sci., Vol. 18, No. 2 (2018) 335–350 DOI: 10.

2478/aoas-2018-0005

Application of complex probiotics in swine nutrition –

a review

Wen Chao Liu1#, Mao Ye1#, Jia Hao Liao1, Zhi Hui Zhao1, In Ho Kim2♦, Li Long An1♦

1
Department of Animal Science, College of Agriculture, Guangdong Ocean University, Zhanjiang,
Guangdong 524088, P. R. China
2
Department of Animal Resource and Science, Dankook University, Cheonan, Choongnam 31116,
South Korea
♦
Corresponding authors: [email protected]; [email protected]
#
These authors contributed equally to this work

Abstract
The use of probiotics as alternatives to antibiotics for farm animals is gaining more and more inter-
est during recent years. Probiotics are living microorganisms that provide a wide variety of health
benefits to the host when ingested in adequate amounts. The bacterial strains most frequently used
as probiotic agents are Bacillus, lactic acid bacteria, Enterococcus and Saccharomyces cerevisiae.
It has been suggested that multi-strain probiotics might be more effective than mono-strain pro-
biotics due to the additive and synergistic effects, and many previous studies demonstrated that
dietary complex probiotics supplementation had growth promoting effects on pigs. However, the
effect of complex probiotics in practice is not always consistent, the effect of probiotic could be
affected by strain composition, dosage, feed formula, and the age of animals. In this review, we
will give an overview on the current use of complex probiotics for weaning, growing and finishing
pigs and sows.

Key words: complex probiotics, growing and finishing pigs, growth promotion, sows, weaning pigs

The gut of domestic animals is home to a dynamic microbial population that

forms a complex ecosystem and has a symbiotic relationship with the host (Fouhse
et al., 2016). The gut microbiota were established as playing key roles in disease
prevention by developing and maintaining proper gut structure and immune function
(Swanson, 2016). Disturbances in the gut microbial ecosystem during the rearing of
animals can dramatically increase risk of respiratory diseases and diarrheas. During
the past several decades, the antibiotics were used to balance the disturbances of
gut microbiota, reduce the pathogen infection and decrease incidence of intestinal
disease (Thacker, 2013). However, antibiotic resistance is a looming public health
crisis, in particular, the antibiotic growth promoters (AGP) have been forbidden in
the European Union, Korea, and Japan. As a result, there is an increasing interest
336 W.Ch. Liu et al.

concerning alternatives to AGP in livestock industry. Recently, an intensive amount

of researches have focused on probiotics supplement in swine production (Fuller,
2012). The application of probiotics provides a potential alternative strategy to the
use of AGP.

Figure 1. Overview on the mode of actions of probiotics

Probiotics are living microorganisms, and when consumed in adequate amounts

can confer a health benefit to the host (FAO/WHO, 2002). Many claims relating
to probiotic properties have been made, varying from the competitive exclusion of
pathogenic bacteria, modulation of gut microflora, immunomodulation, improve-
ment of intestinal development and antioxidant status, alleviation of weaning stress
etc. (Figure 1). However, it has been previously suggested that multi-strain probiot-
ics might be more effective than mono-strain probiotics due to the additive and syn-
ergistic effects (Chen et al., 2012). Nevertheless, the effect of multi-strain probiotics
in practice is not always consistent, the properties of probiotics are strain-specific,
and the efficacy of probiotic could be influenced by dosage, feed composition, and
the age of animals. Therefore, in order to provide an overview of the previous reports
using various strain composition probiotics, the current review aims to summarize
and update the evidence on the application of complex probiotics in swine produc-
tion.

The application of complex probiotics in weaning pigs

The weaning period in pigs represents a time of gastrointestinal and immunologi-
cal instability, which is so-called weaning stress. It results in a critical period of low
voluntary feed intake and an increased susceptibility to infection (Lallès et al., 2007).
Numerous previous studies demonstrated that the complex probiotics could alleviate
weaning stress and promote intestinal health.
 Complex probiotics for swine nutrition 337

Improves growth performance

The most common probiotics for pigs are yeast (Saccharomyces cerevisiae),
Lactobacillus spp. and Bacillus spp., therefore, the most commonly used complex
probiotics are lactobacilli complex, Bacillus complex and other combinations (Ta-
ble 1). Giang et al. (2010 a) reported that pigs fed diets with Lactobacillus complex
(Enterococcus faecium 6H2, 3 × 108 cfu/g, Lactobacillus acidophilus C3, 4 × 106
cfu/g, and Lactobacillus plantarum 1K8, 2 × 106 cfu/g) had higher average daily gain
(ADG), average daily feed intake (ADFI), and lower feed/gain ratio during early
weaning period (d 0-14). Ahmed et al. (2014) reported that inclusion of Bacillus
complex, Bioplus 2B® (B. subtilis and B. licheniformis, 3.2 × 106 cfu/g), increased
the ADG and ADFI throughout the experiment period (d 0–28 after weaning). Dong
et al. (2014) suggested that dietary complex probiotics (L. plantarum and B. sub-
tilis, 4.3 × 109 and 1.0 × 108 cfu/g) had positive effects on reducing the feed/gain
ratios during d 0–14 and d 0–35 after weaning. Zhao and Kim (2015) reported that
dietary lactobacilli complex (L. reuteri and L. plantarum, 1 × 106 cfu/g complex)
supplementation improved the ADG during d 0–28 in weaning pigs. In addition, Cai
et al. (2015) demonstrated that dietary Bacillus-based probiotics supplementation
(B. subtilis and B. amyloliquefaciens) at 1.5 × 105 cfu/g concentration improved
ADG during d 0–14 after weaning, and showed positive effects on increasing gain/
feed ratios during d 0–42. Kim et al. (2017) reported that dietary complex probiotics
(L. acidophilus K31, 1.2 × 106 cfu/g, B. subtilis K42, 1.5 × 107 cfu/g, and S. cerevi-
siae K47, 3.0 × 104 cfu/g) supplementation improved the gain/feed ratios during d
0–35 in weaning pigs. However, on the contrary, Huang et al. (2004) reported that
dietary lactobacilli mixture (2.0 ×108 cfu/g) supplementation (L. gasseri, L. fermen-
tum, L. reuteri and L. acidophilus) had no significant effect on ADG and feed/gain
ratio during d 0–14 and d 15–21 in weaning pigs. Mair et al. (2010) suggested that
addition of 1.0×109 cfu/g complex probiotics (Enterococcus faecium, L. salivarius, L.
reuteri and Bifidobacterium thermophilum) to post-weaning pigs diets had no effects
on ADG, ADFI and feed conversion ratio (FCR) throughout the 28-day experiment
period. In another study carried out by Lähteinen et al. (2015), they also demonstrated
that feeding weaning pigs with multispecies lactobacillus formulation (L. amylovorus;
L. mucosae; L. salivarius; L. reuterii and L. johnsonii) at the level of 1.7 × 109 cfu/g did
not influence the body weight (BW) and ADG through a 21-day feeding trial.
In summary of these previous findings, it is indicated that the effects of complex
probiotics in weaning pigs are not always consistent, and the efficacy of complex
probiotics could be affected by strain composition and inclusion levels. Moreover,
according to the results of previous reports, it should be noted that the beneficial ef-
fects of probiotics on growth performance were always observed in the early period
after weaning. It may be due to the dramatic changes in gut after weaning, and the
gut needs time to adapt to the new situation, when the most critical phase after wean-
ing is passed, a normal intestinal function has been re-established (Heo et al., 2013).
As such, compared to later period after weaning, the efficiency of probiotics should
be expected to be higher when the pigs are confronted with stress during the early
days (d 0–14) after weaning. Therefore, the effects of complex probiotics are also
associated with the age of weaning pigs.
338 W.Ch. Liu et al.

Table 1. Effects of complex probiotics on growth performance in weaning pigs

Supplied Treatment effects (%, differ-
Period
dose ence to control)
Composition (after Reference
(cfu/g
weaning) ADG ADFI G:F
of feed)
Enterococcus faecium 6H2, 3×108 d 0–35 +9.23** +1.12ns +6.17** Giang et al.
Lactobacillus acidophilus C3, 4×106 (2010 a)
Lactobacillus plantarum 1K8 2×106
Lactobacillus acidophilus, 4.0×108 d 0–28 +12.08** +6.09* +5.80** Choi et al.
Bacillus subtilis, 4.8×109 (2011 a)
Saccharomyces cerevisiae 1.0×104
Lactobacillus plantarum GF103, 4.3×109 d 0–35 +10.50ns –15.39** +23.23** Dong et al.
Bacillus subtilis B27 1.0×108 (2014)
Bacillus subtilis, 3.2×107 d 0–28 +16.05** –1.90ns +15.50* Ahmed et al.
Bacillus licheniformis 3.2×107 (2014)
Bacillus subtilis, 1.5×105 d 0–42 +1.67ns +0.33ns +2.03* Cai et al.
Bacillus amyloliquefaciens 1.5×105 (2015)
Lactobacillus reuteri, 1×106 d 0–28 +8.75* –0.82ns +9.65ns Zhao and
Lactobacillus plantarum 1×106 Kim (2015)
Lactobacillus amylovorus, 1.7×109 d 0–21 +4.76ns - - Lähteinen et
Lactobacillus mucosae, al. (2015)
Lactobacillus salivarius,
Lactobacillus reuterii,
Lactobacillus johnsonii
Lactobacillus acidophilus, 4.0×108 d 0–28 +5.96** +3.20ns +3.27** Choi et al.
Bacillus subtilis, 4.8×109 (2016)
Saccharomyces cerevisiae 1.0×104
Lactobacillus acidophilus K31, 1.2×106 d 0–35 +4.35ns +1.81ns +6.22* Kim et al.
Bacillus subtilis K 42, 1.5×107 (2017)
Saccharomyces cerevisiae K47 3.0×104
Bacillus subtilis, 1.5×105 d 0–43 –0.43ns –6.51ns +5.25* Jaworski et
Bacillus amyloliquefaciens 1.5×105 al. (2017)
Note: ns – no significance; * – P<0.05; ** – P<0.01.

Promotes nutrient digestibility and intestinal development

In addition to growth promoting properties, it has been well documented that the
probiotics also exert positive effect on nutrient digestibility. For instance, many pre-
vious studies proved that dietary complex probiotics supplementation could enhance
the apparent total tract digestibility (ATTD) of dry matter of weaning pigs (Giang
et al., 2010 b; Choi et al., 2011 a; Giang et al., 2012; Ahmed et al., 2014; Choi et
al., 2016). Also, other studies reported that dietary complex probiotics supplementa-
tion stimulated the ATTD of nitrogen or gross energy in weaning pigs (Choi et al.,
2011a; Cai et al., 2015; Zhao and Kim, 2015). The probiotics are known to be related
to competitive exclusion against pathogenic microorganisms on the gastrointestinal
tract epithelium of pigs, and they improve host microbial balance and gut health,
 Complex probiotics for swine nutrition 339

consequently promoting the nutrient digestibility (Fuller, 2012; Zhao and Kim,
2015). Regarding the lactobacilli complex probiotics, the increased number of lac-
tobacilli in the gut would potentially increase the activity of useful enzymes such as
β-galactosidase, which will add to the beneficial effects on nutrient utilization (Full-
er, 2012). In addition, Bacillus can also produce some useful enzymes (α-amylase,
arabinase, levansucrase, cellulase, maltase, dextranase, alkaline protease, neutral
protease and β-glucanase) in the animal gut, and Saccharomyces is able to produce
antimicrobial substances and enhance gut function (Hentges, 1992), which can ex-
plain the improved nutrient digestibility in weaning pigs by feeding probiotics.
Villus height and crypt depth were indirect indicators of the maturity and func-
tional capacity of enterocytes, and longer villi provided an increased absorptive area
in the small intestine (Hampson, 1986). Weaning leads to villus atrophy due to the in-
crease of apoptosis and the decrease of replacement of enterocytes within the crypts.
Previous study has demonstrated that villus height was decreased in weaning transi-
tion with a consequent impairment of nutrient utilization and absorption (Boudry et
al., 2004). Probiotics have been proved to contribute to the gut health of weaning
piglets by enhancing the intestinal development. Cai et al. (2015) reported that die-
tary supplementation of B. subtilis-based multi-strain probiotics (1.5 × 105 cfu/g) led
to longer villi of duodenum and jejunum in weaning pigs (Table 2). Also, Choi et al.
(2016) found that inclusion of L. acidophilus, B. subtilis and S. cerevisiae complex
(4.0 × 108; 4.8 × 109; 1.0 × 104 cfu/g respectively) in weaning diet improved the villus
length of duodenum, jejunum and ileum. The enhanced gut morphology could also
account for significant improvement in the nutrient digestibility of pigs fed complex
probiotics. However, failure to observe any positive effects of complex probiotics
on intestinal morphology has also been reported (Walsh et al., 2007; Choi et al.,
2011 b). The inconsistency may be attributed to the strains and the health status of
the piglets.

Table 2. Effects of Bacillus subtilis and Bacillus amyloliquefaciens complex on nutrient digestibility
and villus height of small intestine in weaning pigs1
Items CON TRT SEM P-value
Apparent total tract digestibility (%)

Dry matter 72.62 73.73 0.64 0.171

Nitrogen 69.75 b 72.10 a 0.85 0.038
Gross energy 73.36 73.89 0.65 0.560
Villus height (μm)
Duodenum 462.6 b 548.3 a 17.93 0.002
Jejunum 455.5 b 543.3 a 13.82 0.001
Ileum 471.8 520.4 28.61 0.167
Source: Cai et al. (2015). J. Anim. Sci., 93: 4336–4342.
1
Abbreviations: CON, basal diets (antibiotics-free); TRT, supplied 1.5 × 105 cfu/g complex probiotics; SEM,
standard error of means.
a, b – means in the same row with different letters differ (P<0.05).
340 W.Ch. Liu et al.

Modulates the gut microbial balance

Probiotics are known to benefit the host intestinal balance by creating gut micro-
ecological conditions, and suppressing harmful microorganisms and favoring benefi-
cial microorganisms (Fuller, 2012). Specifically, lactobacilli can reduce the harmful
effects of pathogens by producing organic acids, hydrogen peroxide and antimicro-
bial substances (Lidbeck and Nord, 1993). Bacillus and Saccharomyces can also pro-
duce antimicrobial substances and exert antagonistic effects against several bacterial
pathogens including E. coli. (Spriet et al., 1987; Czerucka and Rampal, 2002). The
release of antimicrobial substances, such as bacteriocins, which inhibit the growth
of pathogenic bacteria, or production of enzymes were able to hydrolyze bacterial
toxins (Buts, 2004). Some probiotics produce nutrients and growth factors which are
stimulatory to beneficial microorganisms of the intestinal microbiota (Fuller, 2012).
Also, most probiotic strains can competitively exclude pathogenic bacteria through
their higher affinity for nutrients or adhesion sites in the gut (Chaucheyras-Durand
and Durand, 2010). Finally, some probiotics like Saccharomyces cerevisiae can me-
tabolize or aid in the detoxification of certain inhibitory compounds such as amines
or nitrates or scavenge for oxygen, which is of great importance in gut anaerobic
ecosystems (Chaucheyras-Durand et al., 2008). These mechanisms can explain the
effects of probiotics in modulating the intestinal microbial balance. Likewise, Choi
et al. (2011 b) reported that a complex probiotics preparation (L. acidophilus 4.0 ×
108 cfu/g, B. subtilis 4.8 × 109 cfu/g and S. cerevisiae 1.0 × 107 cfu/g) were effec-
tive in reducing the coliform and Clostridium and improving the Lactobacillus spp.
population in the ileum and Bifidobacterium spp. population in the cecum in weaning
pigs. Ahmed et al. (2014) demonstrated that dietary Lactobacillus-based multi-strain
probiotics (3.2 × 107 cfu/g) supplementation could decrease fecal S. typhimurium and
E. coli counts, whereas increase fecal Lactobacillus spp. concentration in weaning
pigs at 21 and 28 d of age. Choi et al. (2016) reported that dietary multi-species
probiotics (L. acidophilus 4.0 × 108, B. subtilis 4.8 × 109 and S. cerevisiae 1.0 ×
104 cfu/g) improved cecal Lactobacillus spp. populations, but reduced the cecal E.
coli counts in weaning pigs (d 28). Similar effects of complex probiotics were also
reported by Kim et al. (2017). However, the strains composition might have differ-
ent effectiveness in modulation of gut microbial balance, therefore, the effects of
various strain combinations should be validated from study to study. In general, it
has to be kept in mind that the microbial results of most previous studies were based
on cultural plate count methods. The modern molecular biological methods, such as
PCR-DGGE, q-PCR, FISH and metagenomic sequencing are required for further
studies on the effects of complex probiotics on intestinal microbial communities of
piglets, and to explore the underlying mechanism.

Immunomodulation
Probiotic bacteria are also associated with the enhanced immune system of ani-
mals. Stimulation of unspecific immune functions is considered as one of the main
modes of action of probiotics (Fuller, 2012). The immune system of weaning pigs
is poorly developed, and the young pigs are susceptible to diseases (Lallès et al.,
2007). The immunoglobulins (IgM, IgG and IgA) act as an important part of the
 Complex probiotics for swine nutrition 341

immune response to bind with specific antigens. Various immunoglobulin isotypes

can offer a conception about the complex humoral immune response (Lefranc and
Lefranc, 2001). Several previous studies reported that the complex probiotics were
capable to act as an immunomodulators by enhancing the serum immunoglobulin
levels in weaning pigs. For instance, Dong et al. (2014) demonstrated that L. plan-
tarum and B. subtilis in combination improved the serum IgA during the first 2 weeks
after weaning. Ahmed et al. (2014) showed that serum IgG values were significantly
increased in the Bacillus-based probiotics (Bioplus 2B®) treated group in E. coli
KCTC2571 challenged piglets. Moreover, it has been suggested that administration
of lactobacilli-based multi-strain probiotics could also alter the cytokine gene ex-
pression in intestinal mucosa of piglets, and these alterations resulted in both pro-
and anti-inflammatory responses, including up-regulation on IL-4 and interferon α
(INF-α) expression in cecum and down-regulation on IL-8 and tumor necrosis factor
(TNF) expression in colon (Lähteinen et al., 2015).
Probiotics play a role in defining and maintaining the delicate balance between
necessary and excessive defense mechanisms including innate and adaptive immune
responses (Oelschlaeger, 2010). Points of interaction with the immune regulation for
probiotics include bacteria direct interaction with intestinal epithelial cells, or follow-
ing internalization by M cells through interaction with dendritic cells and follicle-as-
sociated epithelial cells, initiating responses mediated by macrophages and T and B
lymphocytes (Chaucheyras-Durand and Durand, 2010). According to previous stud-
ies, these functions were achieved with probiotics-derived components, for instance,
a Lactobacillus rhamnosus GG-derived soluble protein, p40, was shown to reduce
TNF-α, IL-6, IFN-γ gene expression of intestinal epithelial cell (Yan et al., 2011). In
another report, two active compounds produced by Lactobacillus reuteri RC-14, cy-
clic dipeptides cyclo (L-Tyr-LPro) and cyclo (L-Phe-L-Pro), were shown to inhibit the
staphylococcal quorum-sensing system agr and decrease the expression of toxic shock
syndrome toxin-1 in Staphylococcus aureus MN8, a pathogen in menstrual toxic shock
syndrome (Li et al., 2011). Therefore, regulation of gene and protein expression and
signaling pathways by probiotic-derived compounds in the host cells might be the ma-
jor mechanisms underlying probiotic action leading to immunomodulation.

The application of complex probiotics in growing and finishing pigs

In general, supplementing swine diets with probiotics has given more positive
and consistent effects in weaned piglets than in growing or finishing pigs, which
may be due to their inducing better digestibility of feed, improved immunity, and
increased resistance to intestinal disorders than young pigs. However, some positive
influences of complex probiotics on meat quality and fecal noxious gas emission
have been documented. Moreover, it has been suggested that the effects of complex
probiotics could be affected by energy and nutrient density of feed (Chen et al., 2005;
Chen et al., 2006; Wang et al., 2009; Meng et al., 2010).

Impacts on growth performance

Chen et al. (2005) reported that dietary 0.2% complex probiotics (L. acidophilus
1.0×107 cfu/g, S. cerevisae 4.3×106 cfu/g and B. subtilis 2.0×106 cfu/g) improved the
342 W.Ch. Liu et al.

ADG in growing pigs. Chen et al. (2006) suggested that the complex probiotics at
a supplemental level of 0.2% (B. subtilis, 1.0×107 cfu/g; B. coagulans, 2.0×106 cfu/g
and L. acidophilus, 5.0×106 cfu/g) could increase the ADG of finishing pigs. Meng
et al. (2010) found the ADG and gain-to-feed ratio (G:F) of growing-finishing pigs
were improved by dietary 0.2% probiotics mixture (B. subtilis, 1.0 × 1010 cfu/g and
Clostridium butyricum 1.0 × 109 cfu/g) throughout a 10-week experimental period.
At the same time, they suggested that energy and nutrient density of diets influenced
the effects of complex probiotics on the gastrointestinal (GI) tract and on subsequent
pig performance, and the use of probiotics in higher energy and nutrient density diets
was more favorable than in lower energy and nutrient density diets. Similarly, Yan
and Kim (2013) also found that the effects of complex probiotics affected energy and
nutrient density of diets in growing pigs. In addition, Jørgensen et al. (2016) dem-
onstrated dietary B. licheniformis (DSM 5749) and B. subtilis (DSM 5750) complex
(3.2 × 109 cfu/g of probiotics product) at a concentration of 400 mg/kg improved the
ADG while reduced the feed-to-gain ratio (F:G) at 70-120 d of age, also, the data of
their study indicated an interactive effect of the probiotics and energy density diets.
Balasubramanian et al. (2016) proved that Bacillus-based probiotic (B. coagulance
1 × 109 cfu/g, B. licheniformis 5 × 108 cfu/g, and B. subtilis 1 × 109 cfu/g) exerted
beneficial effects on ADG and G:F overall growing-finishing period (25–110 kg).
However, inconsistent results have been also reported. For example, Munoz et al.
(2007) suggested that dietary supplementation of 0.05% B. subtilis and B. licheni-
formis complex (BioPlus 2B®) in finishing pigs diets improved the average daily
feed intake (ADFI), but had no effects on ADG and G:F. Wang et al. (2009) reported
that addition of various levels (0, 0.05, 0.10, 0.20%) of BioPlus 2B® had no obvious
impacts on ADG and G:F of growing pigs. Giang et al. (2011) also reported that
Bacillus combined with Saccharomyces or Bacillus, Saccharomyces and Lactic acid
bacteria complex did not alter the growth performance during finisher period (50–90
kg). The variation in the results of these studies can be ascribed to several factors,
including the age of the pigs, the dose and strains of complex probiotics, and the
feed formula. In addition, probiotic administration strategies can also impact the ef-
fects of the probiotics (Giang et al., 2011; Jørgensen et al., 2016). Importantly, the
increased resistance against gastrointestinal infections was a key mechanism behind
the growth enhancing effect of probiotics in animals. In fact, as the pigs became
older, the digestive system and immunity were developed, thus increasing the resist-
ance to intestinal disorders and infections. As such, the lack of growth promotion
was probably due to a good level of hygiene in swine house. Therefore, it can be
concluded that the feeding environment and health status are important factors in
determining the effectiveness of probiotics in growing or finishing pigs.

Improves meat quality

Previous studies provided evidences that the complex probiotics could improve
the meat quality by modifying meat color and reducing drip loss and thiobarbituric
acid reactive substances (TBARS) values. For instance, Kim et al. (2008) reported
that dietary 0.1% complex probiotics (Phaffia rhodozyma 1.0 × 108 cfu/g, S. cerevi-
siae 1.0 × 108 cfu/g, L. crispatus 1.0 × 108 cfu/g, Enterococcus faecium 1.0 × 108
 Complex probiotics for swine nutrition 343

cfu/g, L. plantarum 1.0 × 108 cfu/g) supplementation in finishing pigs diets reduced
drip loss and increased meat redness (a*). Ko and Yang (2008) demonstrated that
inclusion of 0.5% and 1.0% green tea probiotics containing L. acidophilus 3.2×108
cfu/g, L. plantarum 2.2×108 cfu/g, B. subtilis 4.5×109 cfu/g and S. cerevisiae 5.2×108
cfu/g significantly reduced the TBARS value of loin meat. Meng et al. (2010) also
suggested that 0.2% complex probiotics (B. subtilis, 1.0 × 1010 cfu/g and Clostridium
butyricum 1.0 × 109 cfu/g) improved the sensory color and meat color (redness, a*).
Additionally, according to Balasubramanian et al. (2016), the sensory color could be
increased, whereas the drip loss of right loin muscle could be reduced by feeding Ba-
cillus-based probiotic mixture (B. coagulance 1 × 109 cfu/g, B. licheniformis 5 × 108
cfu/g, and B. subtilis 1 × 109 cfu/g). Meat color is the single most important sensory
attribute affecting consumer purchasing decisions of red meats, because they associ-
ate a red color with freshness (Morrissey et al., 1994). Changes in a* (redness) and
b* (yellowness) values over a period of time describe meat color deterioration from
red to brown, and reflect the myoglobin concentration and its redox state in meat
(Mancini and Hunt, 2005). Drip loss is commonly assessed as indicative of meat
quality, and the TBARS is a frequently used method for measurement of lipid oxida-
tion, the lower TBARS value, the less oxidation has taken place (Yang et al., 2006).
Moreover, it has been suggested that some Bacillus and Lactobacillus strains could
produce antioxidants and had antioxidant effect. Therefore, it is assumed that the
beneficial effects of complex probiotics on meat quality, which were observed from
these previous studies, are possibly due to the antioxidant properties of probiotics.

Mitigation of fecal noxious gas emission

The noxious gases such as ammonia (NH3), hydrogen sulfide (H2S) and total
mercaptan are major aerial pollutants originating from livestock operations, and
swine is one of the principal contributors among farm animals (Eriksen et al., 2010).
Moreover, airborne pollutants in swine production can increase the susceptibility to
common and important respiratory diseases, and have to be considered in terms of
environmental risk assessments, and the manure is the main source of airborne pol-
lutants in the farm (Jongbloed and Lenis, 1998). It has been suggested that improving
the nutrient utilization, altering the intestinal microbiota ecosystem, and reducing
the pH of manure were the effective strategies to decrease the levels of pollutants
from animal manure (Ferket et al., 2002). Probiotics can benefit the gut microbiota
ecosystem and improve the gut health status, thus mitigating the emission of nox-
ious gas from animal manure (Table 3). Chen et al. (2005) proved that dietary 0.2%
complex probiotic (L. acidophilus, S. cerevisae and B. subtilis) decreased the fecal
NH3-N concentration by 10% in growing pigs. Chen et al. (2006) suggested that
addition of Bacillus-based probiotic to finishing pig diets reduced the fecal NH3-N
and butyric acid content by 17.1% and 24.4%, respectively. According to Wang et
al. (2009), probiotic supplements containing B. subtilis and B. licheniformis spores
(BioPlus 2B®) reduce NH3 emissions by about 50% with inclusion rates ranging
from 0.05% to 0.2% in growing pigs, meanwhile, they suggested that B. subtilis gen-
erates subtilin, which may reduce urease generating microbiota in the gastrointesti-
nal lumen thereby attenuating NH3 releases. Chu et al. (2011) reported that dietary
344 W.Ch. Liu et al.

0.2% multi-strain probiotics (Aspargillus spp., Saccharomyces spp. and Lactobacil-

lus spp.) significantly decreased the fecal amine and propionate content in growing
pigs. Liu et al. (2018) found that complex probiotics (B. subtilis and S. cerevisae)
supplementation in growing pigs diets at 6.0 × 107 cfu/g concentration reduced fe-
cal NH3, H2S and total mercaptans emission. However, some studies failed to show
beneficial effects on fecal gas emission (Han and Shin, 2005; Balasubramanian et al.,
2016). Therefore, further investigations are needed to confirm the beneficial effects
of complex probiotics on fecal noxious gas emission, and to illustrate the underlying
mechanism of these effects.

Table 3. Positive effects of complex probiotics on fecal noxious gas emission in growing and finishing
pigs
Positive effect on noxious gas
Composition Growth stage Reference
emission
Lactobacillus acidophilus, Growing pigs NH3-N↓10% Chen et al. (2005)
Saccharomyces cerevisae,
Bacillus subtilis
Bacillus subtilis, Finishing pigs NH3-N↓17.1%; Chen et al. (2006)
Bacillus coagulans, butyric acid↓24.4%
Lactobacillus acidophilus
Bacillus subtilis, Growing pigs NH3↓50%; Wang et al. (2009)
Bacillus licheniformis H2S↓38.4%
Aspargillus spp., Growing pigs Amine↓28.9%; Chu et al. (2011)
Saccharomyces spp., propionate↓21.7%
Lactobacillus spp.
Bacillus subtilis, Finishing pigs H2S↓27.3%* Balasubramanian et
Bacillus coagulans, al. (2016)
Bacillus licheniformis
Bacillus subtilis, Growing pigs NH3↓7.9%; H2S↓12.5%; Liu et al. (2018)
Saccharomyces cerevisae total mercaptans↓10.7%
Note: *A tendency effect: P=0.062.

The application of complex probiotics in gestating and lactating sows

Sows are subjected to many stressors during their breeding life, such as repeat
services, gestation, farrowing, changes of housing, lactation and weaning, and these
stressors can greatly influence the balance of the intestinal microbiota, thus affect-
ing the reproductive performance of sows (Stamati et al., 2006). Considering the
beneficial effects on intestinal microbial balance, dietary administration of probiot-
ics may relieve the stress of gestation and lactation sows (Chaucheyras-Durand and
Durand, 2010). On the other hand, nutrient utilization and absorption during gesta-
tion and lactation had a significant impact on the number of stillborn piglets, the
number of nursing pigs born alive, and the BW of suckling pigs at birth and weaning
(Alexopoulos et al., 2004; Liu et al., 2017). The improvement of nutrient utilization
by feeding probiotics in sows can also benefit the milk yield and litter performance,
which would improve the overall pig production (Stamati et al., 2006). Furthermore,
 Complex probiotics for swine nutrition 345

epidemiological studies suggest that the administration of probiotics to mothers can

affect the health of their infants, including their immune system and development
(Fanaro et al., 2003; Schultz et al., 2004). Earlier study proved that administration of
probiotic supplement to the sows during gestation and lactation had a positive effect
on gut flora and function of piglets, which has an enormous impact on the subsequent
performance, suggesting that the colonization of the gut microbial in neonatal piglets
could be influenced by the gut flora of sows (Mori et al., 2011).
With respect to the application of complex probiotics in sows, Alexopoulos et
al. (2004) reported that dietary BioPlus 2B® (B. licheniformis and B. subtilis com-
plex) at 400 g/ton of feed to sows during gestation and lactation (the interval from
2 weeks prior to the farrowing up to weaning), which improved certain blood and
milk composition parameters, suckling piglet health and performance, as well as sub-
sequent reproductive performance of the sows. Another study which was carried out
by Link et al. (2007), suggested that dietary BioPlus 2B® supplementation at a level
of 400 g/ton from 2 weeks before farrowing until weaning increased the blood total
lipids and cholesterol of lactating sows at d 15 after parturition. Silva et al. (2010)
demonstrated that the use of complex probiotics (Bifidobacterium bifidum 3.33 ×
106 cfu/g, Enterococcus faecium 1.66 × 106 cfu/g, L. acidophilus 3.33 × 106 cfu/g,
L. plantarum 1.66 × 105 cfu/g) in the diet of sows in late gestation and during lactation
improved the piglets growth performance and intestinal development, and decreased
the incidence of diarrhea. The improved gut development of suckling pigs was prob-
ably due to the probiotics supplementation which promoted the intestinal microbial
balance of sows, and enhanced sows metabolism, thereby improving the colostrum
and milk composition (Scharek et al., 2007; Kim et al., 2013). Milenković et al.
(2011) indicated that supplementation of 0.2% complex probiotics (L. acidophilus,
B. subtilis and yeast S. cerevisiae) during 2 weeks before farrowing and overall lac-
tation period increased the piglets BW at weaning and ADG during suckling. Mori
et al. (2011) reported that administration of multispecies microbial supplements (107
and 108 cfu/g) to pregnant sows changes the fecal SCFAs composition and gut mi-
crobiota in their offsprings. Bula et al. (2012) suggested that inclusion of 400 g/ton
of feed BioPlus 2B® in late gestation and lactation (from two weeks before farrowing
to weaning) diets reduced the sows BW loss during lactation, improved the number
of weaned piglets and weaned litter weight. Baker et al. (2013) found the use of
2 strains of Bacillus subtilis mixture (3.75 × 105 total cfu/g of feed) in 6 weeks before
and throughout the lactation period, could increase the piglet numbers of total born
and born alive, and improve the initial litter weight and litter weaning weight, as well
as increase the probiotics counts, and suppress the harmful bacteria concentration in
the piglets small intestine at d 3 and 10 after birth. According to Link et al. (2016),
dietary supplementation of 400 ppm BioPlus 2B® from 2 weeks before farrowing to
weaning improved the weaning BW and reduced the diarrhea score for nursing pig-
lets. Additionally, Hayakawa et al. (2016) suggested that addition of Bacillus mesen-
tericus 1 × 108 cfu/g, Clostridium butyricum 1 × 108 cfu/g and Enterococcus faecalis
1 × 109 cfu/g mixture to late gestation (3 weeks before farrowing) and lactation diets
increased the sows feed intake and litter weight at birth. Finally, it should be noted
that, although numerous previous studies showed beneficial effects of complex pro-
346 W.Ch. Liu et al.

biotics on performance of sows and their offsprings, the underlying mode of action
is not fully understood yet. Therefore, more details are needed to study and reveal
the mode of action of these effects, thus providing new insight into animal nutrition,
as well as human fertility.

Conclusions and implications

In conclusion, the available data from previous studies suggested that the use
of complex probiotics could improve the growth performance in weaning, growing
and finishing pigs, as well as the reproductive performance of sows. The beneficial
effects of complex probiotics were related to various modes of action, including
competitive exclusion of pathogenic bacteria, modulation of gut microbiota, immu-
nomodulation, anti-oxidation. However, the effects of complex probiotics in prac-
tice is not always consistent, the efficacy of complex probiotics could be influenced
by strain composition, dosage, formula, feeding environment, nutritional level of
feed, the age and health status of animals. Therefore, more studies on the efficacy
of complex preparations in pigs are required, also, randomized, double-blind, case-
controlled, placebo-controlled studies, as well as further studies on optimal supple-
mentation stages and doses, are needed. More importantly, to ensure the bioactivity
of probiotics during feed processing, coating techniques such as microencapsulation
should be developed to maintain bacterial stability.

References

A h m e d S.T., H o o n J., M u n H., Y a n g C. (2014). Evaluation of Lactobacillus and Bacillus-based

probiotics as alternatives to antibiotics in enteric microbial challenged weaned piglets. Afr. J. Mi-
crobiol. Res., 8: 96–104.
A l e x o p o u l o s C., G e o r g o u l a k i s I.E., T z i v a r a A., K r i t a s S.K., S i o c h u A., K y r i a -
k i s S.C. (2004). Field evaluation of the efficacy of a probiotic containing Bacillus licheniformis
and Bacillus subtilis spores, on the health status and performance of sows and their litters. J. Anim.
Physiol. Anim. Nutr., 88: 381–392.
B a k e r A.A., D a v i s E., S p e n c e r J.D., M o s e r R., R e h b e r g e r T. (2013). The effect of a Ba-
cillus-based direct-fed microbial supplemented to sows on the gastrointestinal microbiota of their
neonatal piglets. J. Anim. Sci., 91: 3390–3399.
B a l a s u b r a m a n i a n B., L i T.S., K i m I.H. (2016). Effects of supplementing growing-finishing pig
diets with Bacillus spp. probiotic on growth performance and meat-carcass grade quality traits. Rev.
Bras. Zootecn., 45: 93–100.
B o u d r y G., P é r o n V., L e H u ë r o u - L u r o n I., L a l l è s J.P., S è v e B. (2004). Weaning induces
both transient and long-lasting modifications of absorptive, secretory, and barrier properties of piglet
intestine. J. Nutr., 134: 2256–2262.
B u l a S., O s i t i s U., S t r i k a u s k a S., D e g o l a L. (2012). Impact of a probiotic supplement on the
weight loss of sows and weaning weight of piglets. J. Environ. Sci. Eng., A1: 1122.
B u t s J.P. (2004). Exemple d’un médicament probiotique: Saccharomyces boulardii lyophilisé. In:
Rambaud J.C., Buts J.P., Corthier G., Flourié B. (Eds). Flore microbienne intestinale. John Libbey
Eurotext, Montrouge, France, pp. 221–244.
C a i L., I n d r a k u m a r S., K i a r i e E., K i m I.H. (2015). Effects of a multi-strain Bacillus species-
-based direct-fed microbial on growth performance, nutrient digestibility, blood profile, and gut
health in nursery pigs fed corn-soybean meal-based diets. J. Anim. Sci., 93: 4336–4342.
C h a u c h e y r a s - D u r a n d F., D u r a n d H. (2010). Probiotics in animal nutrition and health. Benef.
Microbes, 1: 3–9.
 Complex probiotics for swine nutrition 347

C h a u c h e y r a s - D u r a n d F., W a l k e r N.D., B a c h A. (2008). Effects of active dry yeasts on the

rumen microbial ecosystem: past, present and future. Anim. Feed Sci. Technol., 145: 5–26.
C h e n C., T s e n H., L i n C., Yu B., C h e n C. (2012). Oral administration of a combination of select
lactic acid bacteria strains to reduce the Salmonella invasion and inflammation of broiler chicks.
Poultry Sci., 91: 2139–2147.
C h e n Y.J., S o n K.S., M i n B.J., C h o J.H., K w o n O.S., K i m I.H. (2005). Effects of dietary
probiotic on growth performance, nutrients digestibility, blood characteristics and fecal noxious gas
content in growing pigs. Asian-Austral. J. Anim. Sci., 18: 1464–1468.
C h e n Y.J., M i n B.J., C h o J.H., K w o n O.S., S o n K.S., K i m H.J., K i m I.H. (2006). Effects of
dietary Bacillus-based probiotic on growth performance, nutrients digestibility, blood characteristics
and fecal noxious gas content in finishing pigs. Asian-Austral. J. Anim. Sci., 19: 587–592.
C h o i J.Y., K i m J.S., I n g a l e S.L., K i m K.H., S h i n d e P.L., K w o n I.K., C h a e B.J. (2011 a).
Effect of potential multimicrobe probiotic product processed by high drying temperature and antibi-
otic on performance of weaning pigs. J. Anim. Sci., 89: 1795–1804.
C h o i J.Y., S h i n d e P.L., I n g a l e S.L., K i m J.S., K i m Y.W., K i m K.H., K w o n I.K., C h a e B.J.
(2011 b). Evaluation of multi-microbe probiotics prepared by submerged liquid or solid substrate
fermentation and antibiotics in weaning pigs. Livest. Sci., 138: 144–151.
C h o i Y., G o e l A., H o s s e i n d o u s t A., L e e S., K i m K., J e o n S., N o h H., K y o n g K w o n I.,
C h a e B. (2016). Effects of dietary supplementation of Ecklonia cava with or without probiotics
on the growth performance, nutrient digestibility, immunity and intestinal health in weaning pigs.
Ital. J. Anim. Sci., 15: 62–68.
C h u G.M., L e e S.J., J e o n g H.S., L e e S.S. (2011). Efficacy of probiotics from anaerobic microflora
with prebiotics on growth performance and noxious gas emission in growing pigs. Anim. Sci. J., 82:
282–290.
C z e r u c k a D., R a m p a l P. (2002). Experimental effects of Saccharomyces boulardii on diarrheal
pathogens. Microbes Infect., 4: 733–739.
D o n g X., Z h a n g N., Z h o u M., T u Y., D e n g K., D i a o Q. (2014). Effects of dietary probiotics
on growth performance, faecal microbiota and serum profiles in weaned piglets. Anim. Prod. Sci.,
54: 616–621.
E r i k s e n J., A d a m s e n A.P.S., N ø r g a a r d J.V., P o u l s e n H., J e n s e n B.B., P e t e r s e n S.O.
(2010). Emissions of sulfur-containing odorants, ammonia, and methane from pig slurry: effects of
dietary methionine and benzoic acid. J. Environ. Qual., 39: 1097–1107.
F a n a r o S., C h i e r i c i R., G u e r r i n i P., V i g i V. (2003). Intestinal microflora in early infancy:
composition and development. Acta Paediatr., 92: 48–55.
FAO/WHO (2002). Joint FAO/WHO working group report on drafting guidelines for the evaluation of
probiotics in food. London, Ontario, Canada, April 30 and May1, 2002.
F e r k e t P.R., Va n H e u g t e n E., Va n K e m p e n T., A n g e l R. (2002). Nutritional strategies to
reduce environmental emissions from nonruminants. J. Anim. Sci., 80: E168–E182.
F o u h s e J.M., Z i j l s t r a R.T., W i l l i n g B.P. (2016). The role of gut microbiota in the health and
disease of pigs. Anim. Front., 6: 30–36.
F u l l e r R. (2012). Probiotics: the scientific basis. Springer Science & Business Media.
G i a n g H.H., V i e t T.Q., O g l e B., L i n d b e r g J.E. (2010 a). Effects of different probiotic com-
plexes of lactic acid bacteria on growth performance and gut environment of weaned piglets. Livest.
Sci., 133: 182–184.
G i a n g H.H., V i e t T.Q., O g l e B., L i n d b e r g J.E. (2010 b). Growth performance, digestibility, gut
environment and health status in weaned piglets fed a diet supplemented with potentially probiotic
complexes of lactic acid bacteria. Livest. Sci., 129: 95–103.
G i a n g H.H., V i e t T.Q., O g l e B., L i n d b e r g J.E. (2011). Effects of supplementation of probiotics
on the performance, nutrient digestibility and faecal microflora in growing-finishing pigs. Asian-
Austral. J. Anim. Sci., 24: 655–661.
G i a n g H.H., V i e t T.Q., O g l e B., L i n d b e r g J.E. (2012). Growth performance, digestibility, gut
environment and health status in weaned piglets fed a diet supplemented with a complex of lactic
acid bacteria alone or in combination with Bacillus subtilis and Saccharomyces boulardii. Livest.
Sci., 143: 132–141.
H a m p s o n D.J. (1986). Alterations in piglet small intestinal structure at weaning. Res. Vet. Sci., 40:
32–40.
348 W.Ch. Liu et al.

H a n Y.K., S h i n H.T. (2005). Effects of antibiotics, copper sulfate and probiotics supplementation
on performance and ammonia emission from slurry in growing pigs. J. Anim. Sci. Technol., 47:
537–546.
H a y a k a w a T., M a s u d a T., K u r o s a w a D., T s u k a h a r a T. (2016). Dietary administration of
probiotics to sows and/or their neonates improves the reproductive performance, incidence of post-
weaning diarrhea and histopathological parameters in the intestine of weaned piglets. Anim. Sci. J.,
87: 1501–1510.
H e n t g e s D.J. (1992). Gut flora and disease resistance, Probiotics, Springer, pp. 87–110.
H e o J.M., O p a p e j u F.O., P l u s k e J.R., K i m J.C., H a m p s o n D.J., N y a c h o t i C.M. (2013).
Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control post-
weaning diarrhoea without using in-feed antimicrobial compounds. J. Anim. Physiol. Anim. Nutr.,
97: 207–237.
H u a n g C.H., Q i a o S.Y., L i D.F., P i a o X.S., R e n J.P. (2004). Effects of lactobacilli on the perfor-
mance, diarrhea incidence, VFA concentration and gastrointestinal microbial flora of weaning pigs.
Asian-Austral. J. Anim. Sci., 17: 401–409.
J a w o r s k i N.W., O w u s u - A s i e d u A., W a l s h M.C., M c C a n n J.C., L o o r J.J., S t e i n H.H.
(2017). Effects of a 3 strain-based direct-fed microbial and dietary fiber concentration on growth
performance and expression of genes related to absorption and metabolism of volatile fatty acids in
weanling pigs. J. Anim. Sci., 95: 308–319.
J o n g b l o e d A.W., L e n i s N.P. (1998). Environmental concerns about animal manure. J. Anim. Sci.,
76: 2641–2648.
J ø r g e n s e n J.N., L a g u n a J.S., M i l l á n C., C a s a b u e n a O., G r a c i a M.I. (2016). Effects of
a Bacillus-based probiotic and dietary energy content on the performance and nutrient digestibility
of wean to finish pigs. Anim. Feed Sci. Technol., 221: 54–61.
K i m K., L i m J., S h i n M., C h o i Y., L e e S., C h o S. (2008). Effect of dietary combined probiotics
(Any-Lac®) supplementation contained with Phaffia rhodozyma on the growth performances and
meat quality of pigs. J. Anim. Sci. Technol., 50: 657–666.
K i m J.S., H o s s e i n d o u s t A., L e e S.H., C h o i Y.H., K i m M.J., L e e J.H., K w o n I.K.,
C h a e B.J. (2017). Bacteriophage cocktail and multi-strain probiotics in the feed for weanling
pigs: effects on intestine morphology and targeted intestinal coliforms and Clostridium. Animal,
11: 45–53.
K i m S.W., W e a v e r A.C., S h e n Y.B., Z h a o Y. (2013). Improving efficiency of sow productivity:
nutrition and health. J. Anim. Sci. Biotechnol., 4: 26.
K o S.Y., Y a n g C.J. (2008). Effect of green tea probiotics on the growth performance, meat quality and
immune response in finishing pigs. Asian-Austral. J. Anim. Sci., 21: 1339–1347.
L ä h t e i n e n T., R i n t t i l ä T., K o o r t J.M., K a n t R., L e v o n e n K., J a k a v a - V i l j a n e n M.,
B j ö r k r o t h J., P a l v a A. (2015). Effect of a multispecies lactobacillus formulation as a feeding
supplement on the performance and immune function of piglets. Livest. Sci., 180: 164–171.
L a l l è s J., B o s i P., S m i d t H., S t o k e s C.R. (2007). Weaning – a challenge to gut physiologists.
Livest. Sci., 108: 82–93.
L e f r a n c M., L e f r a n c G. (2001). The immunoglobulin factsbook. Academic Press.
L i J., W a n g W., X u S.X., M a g a r v e y N.A., M c c o r m i c k J.K. (2011). Lactobacillus reuteri-
produced cyclic dipeptides quench agr-mediated expression of toxic shock syndrome toxin-1 in
staphylococci. Proc. Natl. Acad. Sci. USA, 108: 3360–3365.
L i d b e c k A., N o r d C.E. (1993). Lactobacilli and the normal human anaerobic microflora. Clin. In-
fect. Dis., 16: S181–S187.
L i n k R., K o v a č G., F o l t y s V., K i r c h n e r o v a K. (2007). Composition of sow’s milk and se-
lected metabolic indices after administration of probiotics. Res. Pig Breed., 1: 40–42.
L i n k R., R e i c h e l P., K y z e k o v á P. (2016). The influence of probiotics on reproductive param-
eters of sows and health of their sucklings. Folia Vet., 60: 43–46.
L i u W.C., Yu n H.M., P i S.H., K i m I.H. (2017). Supplementing lactation diets with herbal extract
mixture during summer improves the performance of sows and nursing piglets. Ann. Anim. Sci.,
17: 835–847.
L i u W.C., D e v i S., P a r k J.W., K i m I.H. (2018). Effects of complex probiotic supplementation in
growing pigs diets with and without palm kernel expellers on growth performance, nutrient digest-
 Complex probiotics for swine nutrition 349

ibility, blood parameters, fecal microbial shedding and noxious gas emission. Anim. Sci. J., 89:
552–560.
M a i r C., P l i t z n e r C., D o m i g K.J., S c h e d l e K., W i n d i s c h W. (2010). Impact of inulin and
a multispecies probiotic formulation on performance, microbial ecology and concomitant fermenta-
tion patterns in newly weaned piglets. J. Anim. Physiol. Anim. Nutr., 94: e164–e177.
M a n c i n i R.A., H u n t M. (2005). Current research in meat color. Meat Sci., 71: 100–121.
M e n g Q.W., Y a n L., A o X., Z h o u T.X., W a n g J.P., L e e J.H., K i m I.H. (2010). Influence of
probiotics in different energy and nutrient density diets on growth performance, nutrient digestibil-
ity, meat quality, and blood characteristics in growing-finishing pigs. J. Anim. Sci., 88: 3320–3326.
M i l e n k o v i ć M., M i l a n o v i ć V., M i l o š e v i ć B., S t e f a n o v s k i S. (2011). Probiotic Farm
Pack Y in feed for sows and piglets: effect on initial piglet’s body weight. Maced. J. Anim. Sci., 1:
347–450.
M o r i K., I t o T., M i y a m o t o H., O z a w a M., W a d a S., K u m a g a i Y., M a t s u m o t o J.,
N a i t o R., N a k a m u r a S., K o d a m a H. (2011). Oral administration of multispecies microbial
supplements to sows influences the composition of gut microbiota and fecal organic acids in their
post-weaned piglets. J. Biosci. Bioeng., 112: 145–150.
M o r r i s s e y P.A., B u c k l e y D.J., S h e e h y P., M o n a h a n F.J. (1994). Vitamin E and meat qual-
ity. P. Nutr. Soc., 53: 289–295.
M u n o z D., L a n z A., L u c e r o P., S o r i a F., R e n t e r i a F., C u a r o n J.A., C o r r e a N., M a r -
t i n e z S. (2007). Strategies for enhancing microbiological gut's barrier: BMD y BioPlus 2B,
J. Anim. Sci., 85 (Suppl. 1): 150.
O e l s c h l a e g e r T.A. (2010). Mechanisms of probiotic actions – A review. Int. J. Med. Microbiol.,
300: 57–62.
S c h a r e k L., G u t h J., F i l t e r M., S c h m i d t M.F. (2007). Impact of the probiotic bacteria En-
terococcus faecium NCIMB 10415 (SF68) and Bacillus cereus var. toyoi NCIMB 40112 on the
development of serum IgG and faecal IgA of sows and their piglets. Arch. Anim. Nutr., 61: 223–234.
S c h u l t z M., G ö t t l C., Y o u n g R.J., I w e n P., Va n d e r h o o f J.A. (2004). Administration of
oral probiotic bacteria to pregnant women causes temporary infantile colonization. J. Pediatr. Gastr.
Nutr., 38: 293–297.
S i l v a M.L.F., L i m a J.A.D.F., C a n t a r e l l i V.D.S., A m a r a l N.D.O., Z a n g e r ô n i m o M.G.,
F i a l h o E.T. (2010). Probiotics and antibiotics as additives for sows and piglets during nursery
phase. Rev. Bras. Zootecn., 39: 2453–2459.
S p r i e t S.M., D e c u y p e r e J.A., H e n d e r i c k x H.K. (1987). Effect of Bacillus toyoi (ToyoCerin)
on the gastro intestinal microflora, concentration of some bacterial metabolites, digestibility of the
nutrients and the small intestinal mean retention time in pigs. Meded. Fac. Landbouwkd. Rijksuniv.
Gent., 52: 71–75.
S t a m a t i S., A l e x o p o u l o s C., S i o c h u A., S a o u l i d i s K., K y r i a k i s S.C. (2006). Pro-
biosis in sows by administration of Bacillus toyoi spores during late pregnancy and lactation:
effect on their health status/performance and on litter characteristics. Int. J. Probiotics Prebiotics,
1: 33–40.
S w a n s o n K.S. (2016). Gut microbiota, diet, and health: Application to livestock and companion ani-
mals. Anim. Front., 6: 4–7.
T h a c k e r P.A. (2013). Alternatives to antibiotics as growth promoters for use in swine production:
a review. J. Anim. Sci. Biotechnol., 4: 35.
W a l s h M.C., S a d d o r i s K.L., S h o l l y D.M., H i n s o n R.B., S u t t o n A.L., A p p l e g a t e T.J.,
R i c h e r t B.T., R a d c l i f f e J.S. (2007). The effects of direct fed microbials delivered through
the feed and/or in a bolus at weaning on growth performance and gut health. Livest. Sci., 108:
254–257.
W a n g Y., C h o J.H., C h e n Y.J., Y o o J.S., H u a n g Y., K i m H.J., K i m I.H. (2009). The effect
of probiotic BioPlus 2B® on growth performance, dry matter and nitrogen digestibility and slurry
noxious gas emission in growing pigs. Livest. Sci., 120: 35–42.
Y a n F., C a o H.W., C o v e r T.L., W a s h i n g t o n M.K., S h i Y., L i u L.S., C h a t u r v e d i R.,
P e e k Jr R.M., W i l s o n K.T., P o l i k D.B. (2011). Colon-specific delivery of a probiotic-derived
soluble protein ameliorates intestinal inflammation in mice through an EGFR-dependent mecha-
nism. J. Clin. Invest., 121: 2242–2252.
350 W.Ch. Liu et al.

Y a n L., K i m I.H. (2013). Effect of probiotics supplementation in diets with different nutrient densities
on growth performance, nutrient digestibility, blood characteristics, faecal microbial population and
faecal noxious gas content in growing pigs. J. Appl. Anim. Res., 41: 23–28.
Y a n g Y.X., K i m Y.J., J i n Z., L o h a k a r e J.D., K i m C.H., O h h S.H., L e e S.H., C h o i J.Y.,
C h a e B.J. (2006). Effects of dietary supplementation of astaxanthin on production performance,
egg quality in layers and meat quality in finishing pigs. Asian-Austral. J. Anim. Sci., 19: 1019–1025.
Z h a o P.Y., K i m I.H. (2015). Effect of direct-fed microbial on growth performance, nutrient digest-
ibility, fecal noxious gas emission, fecal microbial flora and diarrhea score in weanling pigs. Anim.
Feed Sci. Technol., 200: 86–92.

Received: 15 IX 2017
Accepted: 9 I 2018