fmicb-10-00057 February 7, 2019 Time: 18:21 # 1 REVIEW published: 11 February 2019 doi: 10.3389/fmicb.2019.00057 Edited by: Vittorio Capozzi,… [620748]

fmicb-10-00057 February 7, 2019 Time: 18:21 # 1
REVIEW
published: 11 February 2019
doi: 10.3389/fmicb.2019.00057
Edited by:
Vittorio Capozzi,
University of Foggia, Italy
Reviewed by:
Marianna Roselli,
The Council for Agricultural Research
and Economics, Italy
Soraya Chaturongakul,
Mahidol University, Thailand
*Correspondence:
Djamel Drider
[anonimizat]
Specialty section:
This article was submitted to
Food Microbiology,
a section of the journal
Frontiers in Microbiology
Received: 31 August 2018
Accepted: 14 January 2019
Published: 11 February 2019
Citation:
Vieco-Saiz N, Belguesmia Y,
Raspoet R, Auclair E, Gancel F,
Kempf I and Drider D (2019) Benefits
and Inputs From Lactic Acid Bacteria
and Their Bacteriocins as Alternatives
to Antibiotic Growth Promoters
During Food-Animal Production.
Front. Microbiol. 10:57.
doi: 10.3389/fmicb.2019.00057
Benefits and Inputs From Lactic Acid
Bacteria and Their Bacteriocins as
Alternatives to Antibiotic Growth
Promoters During Food-Animal
Production
Nuria Vieco-Saiz1,2, Yanath Belguesmia1, Ruth Raspoet2, Eric Auclair2,
Frédérique Gancel1, Isabelle Kempf3,4and Djamel Drider1*
1EA7394-ICV, Institut Charles Viollette, Université de Lille, Villeneuve-d’Ascq, France,2Phileo Lesaffre Animal Care,
Marcq-en-Barœul, France,3Laboratoire de Ploufragan-Plouzané-Niort, Agence Nationale de Sécurité Sanitaire de
l’Alimentation, de l’Environnement et du Travail (ANSES), Ploufragan, France,4Université Bretagne Loire, Rennes, France
Resistance to antibiotics is escalating and threatening humans and animals worldwide.
Different countries have legislated or promoted the ban of antibiotics as growth
promoters in livestock and aquaculture to reduce this phenomenon. Therefore, to
improve animal growth and reproduction performance and to control multiple bacterial
infections, there is a potential to use probiotics as non-antibiotic growth promoters.
Lactic acid bacteria (LAB) offer various advantages as potential probiotics and can
be considered as alternatives to antibiotics during food-animal production. LAB
are safe microorganisms with abilities to produce different inhibitory compounds
such as bacteriocins, organic acids as lactic acid, hydrogen peroxide, diacetyl, and
carbon dioxide. LAB can inhibit harmful microorganisms with their arsenal, or through
competitive exclusion mechanism based on competition for binding sites and nutrients.
LAB endowed with specific enzymatic functions (amylase, protease : : 🙂 can improve
nutrients acquisition as well as animal immune system stimulation. This review aimed
at underlining the benefits and inputs from LAB as potential alternatives to antibiotics in
poultry, pigs, ruminants, and aquaculture production.
Keywords: probiotics, animal health, lactic acid bacteria, antibiotic alternatives, microbiota, immunity
INTRODUCTION
Livestock production is one of the fastest growing aspects of the agricultural sector. During the
last decades, production, and consumption of animal products have largely increased (Speedy,
2003). This increase will continue in the near future in order to satisfy the high demand for
livestock products, such as meat, milk, eggs, and fish, especially in industrialized countries
(OECD/FAO, 2018). The dominant livestock types are pig with 112.33 million of tons (MT), poultry
(109.02 MT), and cattle, which includes beef and buffalo meat (67.99 MT) representing 91.80% of
meat production in the world (FAOSTAT, 2013). While fish captures, and aquaculture production
reached 158 MT (FAOSTAT, 2013).
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Vieco-Saiz et al. Lactic Acid Bacteria as Alternatives to Antibiotics
In veterinary medicine, antibiotics are used to fight clinical
and subclinical infectious diseases. Notably, in some countries,
they are also used as antimicrobial growth promoters (AGPs).
To this end, antibiotics are supplied in subtherapeutic doses to
provide benefits for livestock by improving growth rate, reducing
mortality, and enhancing animal reproductive performance
(Marshall and Levy, 2011). Antibiotics mostly used for AGP
applications include tetracyclines, ionophores, and penicillins
(American Meat Institution, 2013). In Europe, different
antimicrobials have been used (Butaye et al., 2003), but the
Regulation (EC) No 1831/2003 stated that “Antibiotics, other
than coccidiostats or histomonostats, shall not be authorized
as feed additives” and these are now banned in the EU.
Global antibiotic consumption in livestock was estimated to
be approximately 63,000 to over 240,000 metric tons yearly
(World Bank, 2017), and these quantities may certainly increase
because of the high consumption level registered in the emerging
economies (World Bank, 2017). However, a substantial decline
of the sales of antimicrobials for food-producing species
has been observed in some countries (ESV AC, 2017). As a
consequence, this overuse of antibiotics will contribute to
spreading antimicrobial resistance worldwide.
Antibiotics can affect the intestinal microbiota and host
physiology by (i) preventing pathogen colonization, (ii)
impacting the immune system, (iii) increasing fat absorption
by decreasing the hydrolysis of conjugated bile salts, and (iv)
enhancing the use of nutrients as a result of an alteration of the
intestinal wall and lamina propria (Niewold, 2007; Lee et al.,
2011). The balance existing between beneficial and non-beneficial
bacteria in the gastrointestinal tract (GIT) of a healthy animal can
be modified upon alteration of the bacterial proportions causing
pathogen infections from different external sources (Kers et al.,
2018; Pluske et al., 2018). Pathogenic bacteria can negatively
act on the animal health and welfare, as well as on their growth
and reproduction performances. Some of these can reach the
human gastrointestinal tract through the food chain (Newell
et al., 2010), which meanwhile can lead to antibiotic resistance
transmission (Soucy et al., 2015). Resistance to antibiotics is a
serious concern for humanity. To reduce this phenomenon, the
EU ban of antibiotics as growth promoters, should be globalized
worldwide. Consequently, some countries such as Mexico,
New Zealand, and South Korea have adopted the EU approach.
Other countries such as United States, Canada, or Japan have
established guidelines and recommendations to reduce the
use of AGP in animal productions (Laxminarayan et al., 2015;
Brown et al., 2017; Liao and Nyachoti, 2017). To help fighting
against antibiotic resistance, the international organizations have
ruled through global action plans aimed at ensuring treatment
and prevention of infectious diseases with safe and effective
medicines (WHO, 2015).
Ban of antibiotics as AGPs is economically and negatively
impacting the livestock sector because of different and
uncontrolled bacterial diseases (Laxminarayan et al., 2015).
To help control increasing resistance to antibiotics, innovative
alternatives are urgently needed for food-animal production
(Seal et al., 2013; Cheng et al., 2014; Kogut, 2014; Czaplewski
et al., 2016). Related to that, the EU has recently recommendedthe use of alternative strategies in food-producing animals
to limit antimicrobial resistance (AMR), and this resulted in
temporarily and satisfactory achievements as observed in some
EU countries. The strategies adopted included (i) national
reduction targets, (ii) benchmarking of antimicrobial use, and
(iii) controls on prescription and restrictions on use of specific
critically important antimicrobials, together with improvements
to animal husbandry and disease prevention and control
measures (Murphy et al., 2017). According to studies by Allen
et al. (2013), Czaplewski et al. (2016), Seal et al. (2018), additional
means expected to replace AGPs in livestock sector are prebiotics,
antimicrobial peptides (AMPs), bacteriophages and their gene
products, antibodies, vaccines, and natural compounds such as
polyphenols and particularly probiotics. The current adopted
definition of probiotics from FAO/WHO (2002) states that
probiotics are “live microorganisms, providing health benefits
for the host, when they are administered in adequate amounts.”
Microorganisms with probiotic grade must be devoid of any
adverse effects (cytotoxicity, antibiotic resistance, hemolysis),
and endowed with beneficial claims. Probiotics are known to
act in strain-dependent manner and inhibit pathogenic bacteria
through different mechanisms as reported in different studies
(Kabir, 2009; Alloui et al., 2013; Pandiyan et al., 2013; Dowarah
et al., 2017). Regarding to the functions allocated to probiotics,
it has been established that numerous phylogenetic analyses
associated to experimental data have revealed some paradigm for
host-adaptation (Frese et al., 2011).
According to Krajmalnik-Brown et al. (2012), the animal
intestinal microbiota is a key organ, which plays a determinant
role in the harvesting, storage, and expenditure of energy
obtained from the diet. Notably, these functions can influence
the health and weight modification of the animal (Krajmalnik-
Brown et al., 2012). Note therefore, that another report from
FAO (2013) reported the possibility of probiotics application for
animal nutrition as gut ecosystem enhancers. Interestingly, Yirga
(2015) and Seal et al. (2018) reported and argued on the use of
lactic acid bacteria (LAB)-probiotics in promoting the growth
and reproduction performances and the survival rate and health
status of animals. Related to LAB-probiotics, Table 1 shows the
list of these strains potentially usable as antibiotics replacers
because of their multifaceted functions.
Lactic acid bacteria are suitable for livestocks as probiotics
because of their capabilities to modify the environment, in which
they have been delivered, by producing different metabolites
among which a wide range of inhibitory substance and even
competitive exclusion (Gaggìa et al., 2010; FAO, 2016). It
should be noted that LAB-probiotics belong to Lactobacillus
(Lb.), Pediococcus (Ped.), Lactococcus (Lc.), Enterococcus
(Ent.), Streptococcus (Str.), and Leuconostoc (Leuc. ) species.
Nevertheless, Lactobacillus species remain the upmost studied
and used ones (Martínez Cruz et al., 2012). Mechanisms of
pathogens inhibition by LAB-probiotics include (i) production
of inhibitory compounds, (ii) prevention of the pathogens
adhesion, (iii) competition for nutrients, (iv) modulation
of the host immune system, (v) improvement of nutrient
digestibility, feed conversion, and (vi) reduction of toxin
bioavailability ( Figure 1 ).
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TABLE 1 | Probiotic genera used in animal farming.
Animal Yeast Bacteria Fungi Microalgae
LAB Non-LAB
Poultry Candida,
Saccharomyces
KluyveromycesLactobacillus
Streptococcus
Pediococcus
Enterococcus
WeissellaBacillus
BifidobacteriumAspergillus –
Pig Saccharomyces
KluyveromycesLactobacillus
Pediococcus
Enterococcus
WeissellaClostridium
Bacillus
Bifidobacterium– –
Ruminant Saccharomyces
Trichosporon,
KluyveromycesLactobacillus
EnterococcusMegasphaera
Bacillus
Prevotella
Propionibacterium
BifidobacteriumAspergillus –
Aquaculture Saccharomyces
DebaryomycesLactobacillus
Lactococcus
Leuconostoc
Enterococcus
Pediococcus
Carnobacterium
WeissellaBacillus
Enterobacter
Pseudomonas
Streptomyces
Alteromonas
Clostridium
Roseobacter
Eubacterium
Brevibacterium
Microbacterium
Staphylococcus
Streptomyces
Micrococcus
PsychrobacterAspergillus Tetraselmis,
Phaeodactylum
Data summarized from (Kabir, 2009; Seo et al., 2010; Hai, 2015; FAO, 2016; Banerjee and Ray, 2017; Carnevali et al., 2017; Liao and Nyachoti, 2017).
FIGURE 1 | Mechanisms of pathogen inhibition by LAB-probiotics.
PATHOGEN INHIBITION
The commonly encountered pathogenic or zoonotic bacteria
in food-animal farming are Escherichia coli ,Salmonellaenterica ,Campylobacter jejuni ,Vibrio anguillarum ,Clostridium
perfringens ,Aeromonas salmonicida ,Pseudomonas spp., and
Edwardsiella spp. ( Table 2 ). Whilst some of these pathogens,
such as V. anguillarum , and C. jejuni are most often encountered
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TABLE 2 | Most frequently encountered bacterial infections among producers in
animal production.
Animal Potentially reported as pathogenic or
zoonotic bacteria
Poultry Escherichia coli
Salmonella enterica
Clostridium perfringens
Campylobacter jejuni
Swine Streptococcus suis
Pasteurella multocida
Escherichia coli
Ruminants Salmonella abortusovis
Brucella ovis
Campylobacter
Enterotoxigenic Escherichia coli
Aquaculture Aeromonas salmonicida (Furunculosis)
Vibrio anguillarum (Vibriosis)
Pseudomonas spp.
Streptococcus spp.
Edwardsiella spp.
Data obtained from OIE – World Organization for Animal Health
(http://www.oie.int/en/animal-health-in-the-world/oie-listed-diseases-2006/).
in fish and poultry, respectively, other bacteria can affect various
hosts provoking different pathologies in several food-producing
animals. These are the cases of E. coli and S. enterica which
can afflict poultry, swine, ruminants, and humans ( Table 2 ).
As above-cited, LAB-probiotics can limit the dissemination of
pathogenic bacteria by mechanisms involving production of
inhibitory compounds and competitive exclusion.
Production of Inhibitory Compounds
The LAB can produce a wide range of inhibitory compounds to
reduce pathogens invasion ( Table 3 ). These include AMPs such
as bacteriocins, organic acids, ethanol, diacetyl, carbon dioxide,
and hydrogen peroxide (Liao and Nyachoti, 2017).
Bacteriocins are ribosomally synthesized AMPs produced
by both Gram-negative and Gram-positive bacteria (Drider
and Rebuffat, 2011). Bacteriocins produced by LAB referred
here as LAB-bacteriocins are most often devoid of cytotoxic
traits (Belguesmia et al., 2010), and endowed with antagonistic
functions as well as additional beneficial attributes (Drider et al.,
2016; Chikindas et al., 2018). LAB-bacteriocins are emerging
as a novel wave of antibiotics with potent in vitro and in vivo
activities (Stern et al., 2008; Rihakova et al., 2010; Al Atya
et al., 2016; Jiang et al., 2016; Caly et al., 2017; Seddik et al.,
2017). In contrast to traditional antibiotics, LAB-bacteriocins
target specific species and do not affect other population within
the same ecosystem. LAB-bacteriocins are known to exert
either bacteriostatic or bactericidal activity toward sensitive
organisms. Their modes of action have been widely but not
thoroughly investigated. Recent insights on modes of action
are reviewed elsewhere (Cavera et al., 2015; Drider et al., 2016;
Woraprayote et al., 2016; Ben Lagha et al., 2017; Perez et al.,
2018). Combinations of LAB-bacteriocins and antibiotics are
emerging as novel therapeutic options for food-producing
animals (Naghmouchi et al., 2010, 2011, 2013; Al Atya et al.,
2016). Different reports have established the main advantages andsynergistic actions of LAB-bacteriocins with other biomolecules.
These are the case of enterocin AS-48 and ethambutol against
Mycobacterium tuberculosis (Aguilar-Pérez et al., 2018), nisin
and citric acid against Staphylococcus aureus and Listeria
monocytogenes (Zhao et al., 2017), nisin and beta-lactams against
Salmonella enterica serovar Typhimurium (Rishi et al., 2014;
Singh et al., 2014), and Garvicin KA-farnesol against a set of
Gram-positive and Gram-negative bacteria (Chi and Holo, 2018).
Orally administration of these substances is a challenge because
of their enzymatic degradation. This case was reported in vivo for
lacticin 3147 and nisin (Gardiner et al., 2007; Gough et al., 2018).
Organic acids, including short chain fatty acids, lactic and
formic acids, were shown to inhibit potentially pathogenic
bacteria of importance for livestock animals. LAB are producing
lactic acid as the main product of sugar metabolism (Russo
et al., 2017). However, LAB metabolically known as hetero-
fermentative species can concomitantly produce other end-
products such as acetic acid (Oude Elferink et al., 2001; Schnürer
and Magnusson, 2005). Organic acids are known to act by
reducing the intracellular pH and inhibiting the active transport
of excess internal protons which requires cellular adenosine
triphosphate (ATP) consumption leading to cellular energy
depletion (Ricke, 2003). The main targets of organic acids
are the bacterial cell wall, cytoplasmic membrane, and specific
metabolic functions (e.g., replication and protein synthesis) of
pathogenic microorganisms leading to their disturbance and
death (Surendran Nair et al., 2017; Zhitnitsky et al., 2017).
Lactic acid produced by LAB induces an unfavorable local
microenvironment for pathogenic bacteria (Dittoe et al., 2018).
Wang C. et al. (2015) showed that concentrations of 0.5% (v/v)
lactic acid could completely inhibit growth of pathogens such as
Salmonella spp., E. coli orL. monocytogenes . Nevertheless, these
acids do not affect animal epithelial cells because of the mucus
layer that creates a gradient of pH (Allen and Flemström, 2005).
Feeding with organic acids such as propionic has some limits
because their dissociation before they reach the small intestine
(Hume et al., 1993).
Ethanol produced by hetero-fermentative LAB is generated
from the glycolysis pathway (Elshaghabee et al., 2016). Ethanol
affects the membrane fluidity and integrity resulting in bacterial
cell death due to plasma membrane leakage (Ingram, 1989). Oh
and Marshall (1993) reported that ethanol concentration at 5%
inhibited L. monocytogenes replication.
Diacetyl is produced from citrate uptake and metabolism
in LAB. Notably Lb. plantarum, Lb. helveticus, Lb. bulgaricus,
Ent. faecalis, and mainly Leuc. mesenteroides and Lc. lactis
biovar diacetylactis are the most commonly known LAB species
producing diacetyl (García-Quintáns et al., 2008; Singh, 2018).
Diacetyl interferes with arginine utilization by reacting with the
arginine-binding protein of Gram-negative bacteria (Lindgren
and Dobrogosz, 1990), while carbon dioxide liberated in the near
environment by LAB creates an anaerobic environment where
aerobic bacteria cannot grow (Singh, 2018).
Some species of LAB are able to produce hydrogen peroxide
(H2O2) and can inhibit pathogenic bacteria devoid of
catalase (Mitchell et al., 2015), through superoxide anion
chain reaction enhancing toxic oxidation. H 2O2bactericidal
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TABLE 3 | Examples of antimicrobial compounds produced by LAB.
Molecule Examples Producers Spectrum Reference
Bacteriocins Nisin Lc. lactis subsp. lactis Broad spectrum: Gram-positive bacteria without
nisinaseJuncioni de Arauz
et al., 2009
Pediocin PA-1 Ped. acidilactici Broad spectrum: Gram-positive bacteria Rodríguez et al., 2002
Enterocin AS48 Ent. faecalis Gram-positive bacteria and E. coli, Salmonella enterica
Bacillus subtilis, B. cereus, B. circulans,
Corynebacterium glutamicum, C. bovis,
Mycobacterium phlei, Nocardia corallina, Micrococcus
luteus, Micrococcus lysodeikticus, S. aureus,
Enterococcus faecalis, Ent. faecium, Enterobacter
cloacae, E. coli, Klebsiella pneumoniae, Proteus
inconstans, Salmonella Typhimurium , Shigella sonnei,
Pseudomonas fluorescens, P . aeruginosaKarpi ´nski and
Szkaradkiewicz, 2013;
Grande Burgos et al.,
2014
Enterolysin A Ent. faecalis Lb. sakei, Lb. brevis, Lb. curvatus, Lc. cremoris,
Lb. lactis, Ped. pentosaceus, Ped. acidilactici, Ent.
faecium, Ent. faecalis, L. innocua, L. ivanovii, Bacillus
subtilis, B. cereus, S. carnosus, Propionibacterium
jenseniiKarpi ´nski and
Szkaradkiewicz, 2013
Bacteriocin-like
inhibitory
substance (BLIS)Ped. acidilactici Kp10
Leuc. mesenteroides
406
Lc. lactis subsp. lactis
CECT-4434L. monocytogenes
L. monocytogenes
Staphylococcus aureusWong et al., 2017;
Arakawa et al., 2016;
Souza Vera et al., 2018
Antibiotic Reutericyclin Lb. reuteri Gram-positive bacteria ( Lactobacillus, Bacillus,
Enterococcus, Staphylococcus, andListeria )Rattanachaikunsopon
and Phumkhachorn,
2010; Singh, 2018
Reuterin Lb. reuteri DSM 20016 Gram-positive ( Clostridium andStaphylococcus ) and
Gram-negative ( Escherichia, Salmonella, Shigella )
bacteria, against the yeast, Saccharomyces cerevisiae ,
and against the protozoan, Trypanosoma cruziStevens et al., 2011
Organic acids Lactic acid, Acetic acid LAB Broad spectrum: bacteria affected by pH
Hydrogen peroxide Ped. acidilacti Leuc.
mesenteroides
Lb. brevis
Lb. plantarum
Lb. caseiBroad spectrum: Catalase negative bacteria Whittenbury, 1964
Others Ethanol Bifidobacterium longum
Ent. faecalis
Lb. acidophilus
Lb. fermentum
Lb. plantarum
Weissella confusaBroad spectrum: bacteria affected by membrane
dissociationsElshaghabee et al.,
2016
Diacetyl Lb. plantarum
Lb. helveticus
Lb. bulgaricus
Ent. faecalis
Leuc. mesenteroidesListeria, Salmonella, Escherichia coli, Yersinia, and
Aeromonas.Singh, 2018
Carbon dioxide Heterofermentative LAB Broad spectrum: Aerobic bacteria Singh, 2018
action depends on the concentrations and environmental
factors such as pH and temperature (Surendran Nair
et al., 2017). Lc. lactis and Ent. faecium species were
reported to produce H 2O2with strong antimicrobial
effects (Y ang et al., 2012).
Reuterin, is a secondary metabolite associated with glycerol
metabolism by Lb. reuteri. This potent inhibitory compound
has a broad spectrum of activity exerted in a pH-independent
manner. Reuterin is known to inhibit DNA replication and
is resistant to proteolytic and lipolytic enzymes (Singh, 2018).
In terms of spectrum of activity, reuterin was shown tobe active against E. coli, Staphylococcus aureus , and Candida
spp. (Helal et al., 2016).
Competitive Exclusion
Competitive exclusion (CE) can occur after addition of any
culture containing at least one non-pathogenic bacteria to the
gastrointestinal tract of animals. This will decrease the number
of pathogenic bacteria, through direct or indirect competition for
nutrients and adhesion for sites in the gut (Callaway et al., 2008).
These LAB-probiotics are able to form biofilms and communicate
through Quorum Sensing (QS) upon producing and releasing of
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autoinducers (Tannock et al., 2005). Pathogens are not able to
adhere to the intestinal mucosa, which blocks the development
of their population by the constant flow of digesta (Callaway
et al., 2008; Yirga, 2015; Liao and Nyachoti, 2017). Some studies
aimed at highlighting this mechanism are briefly described below.
Carter et al. (2017) reported the protective effect exerted by
the combination of 5 107CFU/mL of Lb. salivarius 59 and
Ent. faecium PXN33 by reducing Salmonella Enteritidis S1400
colonization in chicks. Penha Filho et al. (2015) reported the
effect of 1105CFU of a Lb.-based probiotic suspension on
reducing Salmonella colonization when this strain was provided
to chicks from 1 to 7 days of age. Arruda et al. (2016) showed that
a commercial probiotic of Lactobacillus spp. decreased prevalence
ofClostridium difficile infections in pigs when administrated at
a concentration of 7.5 109CFU. Sha et al. (2016a) showed
through feeding trial assays that 1 109CFU/mL of Lb. pentosus
HC-2 strongly inhibited the growth of Vibrio parahaemolyticus in
the intestine of shrimp.
Modulation of the Host Immune System
Lactic acid bacteria have been widely described for their
capabilities to enhance the animal immune system, by positively
affecting the innate and adaptive immune response (Tellez
et al., 2012; Tsai et al., 2012; Ashraf and Shah, 2014) by
helping protect from pathogen disorders (Ashraf and Shah,
2014). The innate immune system induces immediate defense
against infection, but also activates a long-lasting adaptive
immunity. Components of the innate system recognize the
molecular patterns associated with pathogens through pattern
recognition receptors (PRRs). The recognition of these patterns
by PRR leads to the induction of inflammatory responses and
innate host defenses. In addition, the detection of microbes
by PRR expressed in antigen-presenting cells, particularly
dendritic cells (DC), leads to the activation of adaptive immune
responses, by means of T and B cells (Iwasaki and Medzhitov,
2015). Various immune cells types, including granulocytes,
macrophages, DCs, and T and B lymphocytes, are involved with
inflammatory responses which are mediated by several cytokines
like TNF a, IL-1 b, IL-6, IL-8, and IL-15 interleukins. The anti-
inflammatory/suppressive responses are mediated for their part
by IL-10, IL-12, and TGF b(Hardy et al., 2013). LAB have different
immunomodulatory properties associated with their capabilities
to induce cytokine production, impact immunomodulation by
innate or adaptive immune responses (Kiczorowska et al., 2017a).
Those immunomodulation abilities are considered as a crucial
criterion for probiotic assessment, through various mechanisms
(Wells, 2011; Hardy et al., 2013).
Enhancing Innate Immune Response
The primary mechanism of innate immunity stands as physical
and chemical barriers such as the intestinal epithelial cells (IECs),
which prevent pathogens spreading and subsequent infections
(Riera Romo et al., 2016). Depending on the presence of changing
mucus layer, probiotics will be able to interact with IECs and
DCs (Lebeer et al., 2010). IECs are the first defense barriers
(Dowarah et al., 2017) and they are supposed to be the first and
most important target cells for probiotic action (Lebeer et al.,2008). Probiotic strains have been shown to have beneficial effects
related to the nutritional function of the intestinal epithelium
(Lebeer et al., 2008). They also improve intestinal barrier function
by stimulating: (i) the production of antimicrobial mucus and
peptides such as defensins (Y ang et al., 1999; Schlee et al.,
2008), (ii) increased immune responses, (iii) improved expression
and/or localization of tight junction proteins, (iv) preventing
apoptosis of epithelial cells, and (v) induction of cytoprotective
molecules (Ewaschuk et al., 2008; Anderson et al., 2010; Mathias
et al., 2010; Madsen, 2012). In chicks, Lb. plantarum LTC-113
(1109CFU) can up-regulate cellular junctions to impede
pathogens colonization as Salmonella (Wang et al., 2018).
In addition, other cellular components of the innate immune
system such as monocytes and macrophages, prevent the invasion
of pathogens by secreting pro-inflammatory cytokines and
cytotoxic molecules. Natural Killer (NK) cells produce cytokines
such as interferon (IFN- g) and various interleukins (IL): IL-10,
IL-3, etc. (Vivier et al., 2011). In weaning pigs, administration
ofLb. brevis ZLB004 (2109CFU/kg of feed) increased the
level of IFN- g(Liu et al., 2015). Lactobacilli strains as Lb.
fermentum, Lb. salivarius, Lb. crispatus , and Lb. gasseri have
been reported to modulate positively the secretion level of the
pro and anti-inflammatory interleukins IL-6, IL-8, and IL-10 in
order to regulate the inflammation and restore the physiological
equilibrium of food-producing animals (Pérez-Cano et al., 2010;
Luongo et al., 2013; Sun et al., 2013; Rizzo et al., 2015). IL-8 is a
pro-inflammatory cytokine which directly recruits macrophages
and leukocytes into inflammatory regions by chemosensing
(Riera Romo et al., 2016). A Lb. acidophilus strain stimulated
anti-inflammatory properties in enterotoxigenic E. coli (ETEC)
infected piglets when administered at 1 108CFU in the feed.
This strain was also able to down-regulate pro-inflammatory
cytokines IL-8 and TNF- ain vivo based on animals experiments
(Li et al., 2016). The same trend in IL-8 levels was also observed in
Aeromonas hydrophila infected carp ( Cyprinus carpio Huanghe
var.) when fed with 1 107CFU g/L Lb. delbrueckii strain
(Zhang et al., 2017). Conversely the combination at 1 107
CFU each/g feed pellet of Lc. lactis BFE920 and Lb. plantarum
FGL0001 induced IL-8 and IL-6 increase in Streptococcus iniae –
infected Japanese flounder fish (Beck et al., 2015). Walter (2008)
and Brisbin et al. (2011) support that discrepancies in the
immunomodulation effects were ascribed to the Lactobacillus
strains selected, their dosage, and also to the animal conditions.
Zhang et al. (2017) established that Lb. delbrueckii at 1107CFU
g/L increased levels of anti-inflammatory cytokines IL-10 and
TGF- bin the intestine and enhanced immunity of A. hydrophila-
infected Cyprinus carpio Huanghe var.
Enhancing Adaptive Immune Response
The adaptive immune response depends on B- and
T-lymphocytes, which induce antigen-specific response.
Association of Lb. plantarum (1107CFU/kg of feed) and
Clostridium butyricum (1106CFU/kg of feed) on production
performance and immune function in broilers revealed the
increase of IgG and IgA levels in chickens fed with these
beneficial probiotics (Han et al., 2018). In direct line, Lb.
plantarum B2984 was shown to stimulate immunoglobulin
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production (IgM and IgA) against Salmonella infection in
pigs during orally challenged animal trials (Naqid et al.,
2015). Feeding piglets with a strain of Lb. rhamnosus ATCC
7469, at a concentration of 109CFU/mL, prevented acute
infectious diarrhea by stimulating the adaptive immune system
subsequently to produce an increase in the concentration of
lamina propria CD3CCD4CCD8T cells (Zhu et al., 2014).
In chicken, feed supplementation with 1 109CFU/kg of Lb.
acidophilus LA5 increased the production of CD4C, CD8C,
and TCR1CT cell in GI tract but also in peripheral blood
(Asgari et al., 2016). The administration of 1010CFU/mL
Lactobacillus spp. could efficiently activate the immunity
of mucosa in chickens by increasing the levels of IgA and
IgG (Rocha et al., 2012). In young calves, administration of
1.85107CFU/L of Lactobacillus species has been shown
to improve weight gain and immunocompetence (Al-Saiady,
2010). In summary, LAB were reported to improve the host
resistance and production performance as delineated in Section
“Production Performance, ” by enhancing the immune response
(Kiczorowska et al., 2017a).
Improvement of Nutrient Digestibility and
Feed Conversion
Feed digestibility reflects the amount of absorbed feed and
the nutrient’s availability used for the animal growth and
reproduction (ILCA, 1990). It is possible to measure the apparent
or real digestibility by comparing nutrients contained in the
feces from nutrients contained in the dietary intake, or adding
external markers (such as titanium dioxide, chromium oxide
and rare-earth elements) into feed (ILCA, 1990; Safwat et al.,
2015). The improvement of this nutrient digestibility is measured
by an indirect method: feed conversion ratio, a correlation
between weight of feed administered over the lifetime of an
animal and weight gained, which is a valuable indicator of
feeding systems efficiency (Wenk et al., 1980; Fry et al., 2018).
LAB-probiotics improved nutrient digestibility because of their
highly fermentative activities. Indeed, they can enhance the
whole digestive process, the metabolic utilization of nutrients,
and improve the feed efficiency by producing digestive enzymes
(e.g., amylases, chitinases, lipases, phytases, proteases) or by
just generating volatile fatty acids and B-vitamins: riboflavin,
biotin, B12 vitamin (Russo et al., 2014; Liao and Nyachoti, 2017;
Sharifuzzaman and Austin, 2017). In addition, LAB-probiotics
can indirectly modify the gut microsystem (FAO, 2016) by
helping in the assimilation of nutrients through activation of
the host immune cells and increasing the number of antibodies
leading to animal welfare improvement (Forte et al., 2016).
Reduction of Toxin Bioavailability
Protective effects of LAB-probiotics can result in inhibition of
toxin expression in pathogens (Liao and Nyachoti, 2017). It was
also reported that LAB can constitute natural barriers against
mycotoxins considered as potentially harmful compounds for
animals (Tsai et al., 2012; Peng et al., 2018). Several investigators
reported that Lb. plantarum, Lb. acidophilus, Lb. paracasei, and
Ent. faecium could mitigate the effect of aflatoxins for improvinghuman and animal health (Gratz et al., 2007; Ahlberg et al., 2015;
Abbès et al., 2016; Damayanti et al., 2017; Li et al., 2017).
Lactic acid bacteria act as a biological barrier in the
intestinal tract, decreasing availability of ingested mycotoxins
and neutralizing their adverse effects. Detoxifying capabilities of
LAB are associated with their capacities to bind and sequester
mycotoxins, boosting their excretion by digestive system in the
feces (Zoghi et al., 2014; Damayanti et al., 2017; Li et al., 2017).
Mycotoxins can bind to viable and non-viable bacterial surface by
adhesion to their cell wall components (Damayanti et al., 2017; Li
et al., 2017), and aflatoxin B1 (AFB1), for example, was bound to
LAB by non-covalent interactions (Haskard et al., 2001). Tests
aimed at controlling mycotoxins have been carried out with
Lb. casei DSM20011, Lb. casei Shirota (Liew et al., 2018), Lb.
rhamnosus strains LGG and LC 705 (El-Nezami et al., 1998, 2002;
Nybom et al., 2007), Lb. acidophilus 24 (Pizzolitto et al., 2012),
and Lb. plantarum Lb. brevis ,Lb. sanfranciscensis , from LOCK
collection (Piotrowska, 2014). Piotrowska (2014) suggested that
the binding to mycotoxins, particularly to ochratoxin was
ascribed to hydrophobic properties of the cell wall, and also by
electron donor-acceptor and Lewis acid-base interactions. LAB
have additional anti-mycotoxin mechanisms based on a study
performed on mice wherein the diet was supplemented with
Lb. plantarum C88 (11010CFU/mL). This supplementation
weakened oxidative stress induced by aflatoxin AFB1. Likewise,
this strain decreased lipid peroxidation in serum and the liver due
to hepatic damage caused by AFB1 toxicity (Li et al., 2017). LAB
produce exopolysaccharides, which are important compounds
capable of inhibiting bacterial toxins as reported by Ruas-
Madiedo et al. (2010) for the interactions between Lb. rhamnosus
GG against Bacillus cereus. Further mechanisms including pH
decrease and blockage of QS have been reported during co-
existence of C. perfringens type A and LAB particularly Lb.
acidophilus CGMCC 11878 and Lb. fermentum CGMCC12029
(Guo et al., 2017).
BENEFITS FOR ANIMALS AND FOOD
CHAIN
In addition to the above listed positive effects attributed to LAB
potentially utilizable as probiotics, we noted further beneficial
effects on the health of various livestock animals and quality
of animal products. These effects are animal-dependent and
consist of enhancing body weight gain, improve gut microbial
balance, improve reproductive performance, and increase overall
productivity ( Figure 2 ).
Disease Management
Different investigators have reported the potential effect of
LAB to decrease the risk of infections and intestinal disorders
associated with pathogens such as Salmonella spp., E. coli,
Campylobacter, orClostridium spp. LAB-probiotics were used
preventively and therapeutically to treat infections by these
pathogens (Tellez et al., 2012; Layton et al., 2013; O’Bryan et al.,
2014; Gómez et al., 2016; Park et al., 2016).
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FIGURE 2 | Beneficial effects due to LAB-probiotics administration.
Poultry
Many studies were dedicated to LAB used in poultry. Indeed,
Wang et al. (2018) inoculated hatched chicks with 1 109CFU
Lb. plantarum LTC-113 strain, which provided anti- Salmonella
Typhimurium protection by limiting the gut colonization and
stabilizing the expression of tight junction genes in intestinal
epithelial cells among treated chickens making them more
resistant to the infection. As previously mentioned, CE is
an effective mechanism protecting newly hatched birds from
enteropathogen colonization in poultry (Kabir, 2009). Similarly,
Olnood et al. (2015) showed that 5 108CFU of Lb. johnsonii
reduced numbers of Salmonella enterica serovar Sofia and
C. perfringens in challenged 1-day-old Cobb broilers (Olnood
et al., 2015). Another study reported that administration of
1109CFU (50:50) Lb. salivarius 59 and Ent. faecium PXN33
in combination decreased the levels of colonization in birds by
Salmonella (Carter et al., 2017). On the other hand, strains of
C. perfringens are responsible for production of the necrotic
enteritis toxins and/or enzymes. Colonization of poultry mucosa
byC. perfringens occurs during the early life of the birds
(M’Sadeq et al., 2015). Several Lactobacillus (Lb. acidophilus, Lb.
fermentum, Lb. plantarum, Lb. reuteri , and Lb. salivarius ) and
Enterococcus strains ( Ent. faecium and Ent. faecalis ) can inhibit
C. perfringens in vitro (Caly et al., 2015). The administration
of certain LAB strains do not generate systematically benefits
for poultry, as underpinned for Lb. plantarum PCS 20 against
Campylobacter jejuni (Santini et al., 2010), or Lb. johnsonii
FI9785 against Salmonella Enteritidis (La Ragione et al., 2004).
Therefore, the screening has to be performed in defined
conditions and the results are strictly strain-dependent.Lactic acid bacteria-bacteriocins improve growth performance
ofC. perfringens -challenged chickens allowing weight to recover
at similar levels of healthy birds. For instance, this effect was
observed when chickens challenged with C. perfringens were
treated with pediocin A from Ped. pentosaceus (Grilli et al.,
2009), or when E. coli infected chickens were receiving plantaricin
from Lb. plantarum F1 (Ben Lagha et al., 2017). Notably, anti-
C. perfringens divercin bacteriocin, produced by Carnobacterium
divergens AS7 improved growth performance and welfare in
treated chickens (Józefiak et al., 2012).
Swine
Numerous benefits have been described in pig upon LAB
administration specifically with lactobacilli (Y ang F. et al., 2015;
Valeriano et al., 2016; Dowarah et al., 2017). For pigs, the
highest death loss is due to diarrhea caused by ETEC and
Salmonella (Liao and Nyachoti, 2017). Feed supplementation
with various species of Lactobacillus including Lb. johnsonii, Lb.
mucosae , and Lb. plantarum improved the gut microbial profile
and microbial metabolites production, leading to gut health
improvement, and reduced pathogens colonization of intestinal
mucosa (Dowarah et al., 2017). Subsequently, these investigators
showed that weaned piglets treated with 2 109CFU/g of Ped.
acidilactici FT28 rather than Lb. acidophilus NCDC-15 resulted
in the reduction of diarrhea due to dietary and environmental
changes (Dowarah et al., 2018). Decrease of ETEC number
was observed when a fermented food from reuteran-producer
Lb. reuteri LTH5794 at a concentration of 1 107CFU/g
was administered to weaning pigs. The studied strain was
able to produce exopolysaccharides such as reuteran or levan
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impeding ETEC adhesion to the mucosa (Y ang Y. et al., 2015).
However, a study from Andersen et al. (2017) showed that no
protective effect was observed in newly born piglets treated
with commercially available probiotic Lb. paracasei F19 strain
(2.6108CFU/kg) and a newly characterized Ped. pentosaceus
(1.31010CFU/kg) developed to inhibit E. coli F18-inducing
diarrhea (Andersen et al., 2017).
Streptococcus suis is involved in a wide range of infections in
pigs such as meningitis, arthritis, endocarditis, pneumonia, and
septicemia (Ben Lagha et al., 2017). This bacterium has been
reported to be sensitive to nisin, a well-known and the only
bacteriocin marketed now (Lebel et al., 2013).
Ruminants
Administration of LAB can prevent development of ruminal
acidosis by creating optimal conditions for lactic acid consuming
bacteria such as Megasphaera elsdenii orPropionibacterium
spp. (Chaucheyras-Durand and Durand, 2010). Addition of Lb.
acidophilus, Lb. salivarius, and Lb. plantarum at concentrations
of 107–108CFU/g, reduced the incidence of diarrhea in young
calves (Signorini et al., 2012). LAB species including Lb. paracasei
and Lb. plantarum, and those isolated from honey like Lb.
kunkeei, Lb. apinorum, Lb. mellis, Lb. mellifer, Lb. apis hadin vitro
activities against mastitis pathogens such as Staphylococcus
aureus, Staphylococcus epidermidis, Streptococcus uberis , orE. coli
(Piccart et al., 2016; Diepers et al., 2017). LAB-probiotics were
also successfully used to relieve symptoms of diseases such as
coccidiosis, an important parasitic disease of young ruminant
livestock, caused by Eimeria . These LAB-probiotics minimized
the impact of this disease by reducing the risk of dissemination of
this parasite (Giannenas et al., 2012). On the other hand, Cao et al.
(2007) reported on the effectiveness of intra-mammary infusion
of nisin for treating mastitis caused by Staphylococcus aureus
in dairy cows.
Aquaculture
In aquaculture, Lb. strains such as Lb. murinus orLb.
pentosus displayed antagonism against V. harveyi and
V. parahaemolyticus . Other potential LAB-probiotics such
asEnt. faecium NRW-2 (1107CFU/g of feed) were reportedly
active against Vibrio spp. strains through their highly elevated
capacities of adhesion and competition for nutrients. These
bacteria were reported to decrease the presence of Vibrio in
shrimp (Sha et al., 2016b). Fish fed with Lb. delbrueckii became
more resilient to Aeromonas infections. It was suggested that
1106CFU/g of Lb. delbrueckii action was linked to their
stimulation properties of the shrimp larval gut immune system
(Zhang et al., 2017). Araújo et al. (2016) isolated several strains
ofPed. acidilactici from rainbow trout ( Oncorhynchus mykiss )
feed and larvae. Some of these strains have wide action spectra
and showed antagonistic activities against several fish pathogens
including Lc. garvieae, Streptococcus iniae, Carnobacterium
maltaromaticum, and A. salmonicida .
Nisin Z-producing Lc. lactis WFLU12 provided protection
against infections caused by Streptococcus parauberis in olive
flounder fish (Nguyen et al., 2017). While Lb. pentosus
39 produces a bacteriocin active against the fish pathogenA. hydrophila , suggesting this LAB could be used as a natural
biopreservative agent (Anacarso et al., 2014).
LAB-Probiotics in Treatment of Viral Infections
Lactic acid bacteria-probiotics were described as potent
organisms to treat viral infections (Al kassaa et al., 2014; Arena
et al., 2018a,b). Leyva-Madrigal et al. (2011) reported the
capabilities of Ped. pentosaceus and Staphylococcus haemolyticus
(1106CFU/g feed) to treat white spot syndrome virus (WSSV)
in white leg prawns ( Litopenaeus vannamei ). A modified Lb.
plantarum conferred resistance to yellow head virus in shrimps
(Thammasorn et al., 2017). In piglets, Lb. plantarum N4 was
shown to be active against transmissible Gastroenteritis Virus
when provided in a preventive manner (Y ang Y. et al., 2017)
and Lb. plantarum 25F, reduced viral infectivity of Porcine
Epidemic Diarrhea Virus (PEDV) (Sirichokchatchawan et al.,
2018). The effects of Lb. casei CMPUJ 415 and B. adolescentis
DSM 20083 on rotavirus has been demonstrated by a reduction
on the production of a viral enterotoxin protein (NSP4)
(Olaya Galán et al., 2016). Roselli et al. (2017) listed numerous
examples of LAB-probiotics with antiviral activities such as
Lb. casei MEP221106 or MEP221114, Lb. rhamnosus CRL1505.
Nevertheless, Sachsenrödder et al. (2014) hypothesized the
administration of probiotics as Ent. faecium NCIMB10415
do not have an effect on the virus composition present in the
pigs’ gut. For this reason, several studies focus on producing
recombinant LAB for vaccination as it is the case of recombinant
Lb. casei ATCC 393 against PEDV (Wang X. et al., 2017) or Lb.
plantarum NC8 against H9N2 avian influenza virus (Y ang W.
et al., 2017) boosting the immune system presenting antigens.
Production Performance
Lactobacilli produce lactic acid and proteolytic enzymes, which
enhance nutrient digestion in the GIT and feed supplementation
with Lactobacillus strains can induce weight gain in livestock
animals (Angelakis, 2017), in a strain strain-specific dependent
manner (Drissi et al., 2017). For instance, Lb. delbrueckii, Lb.
acidophilus, Lb. casei, Lb. agilis, Lb. salivarius ,Lb. fermentum, and
Lb. ingluviei were described as weight enhancers (Drissi et al.,
2017). The last two species were associated with a substantial
weight gain effect in ducks and chicks (Million et al., 2012;
Drissi et al., 2017). LAB-probiotics improved the feed conversion
efficiency by modifying the intestinal microbiota, limiting the
growth of pathogens, promoting non-pathogenic bacteria, and
enhancing nutrients use and digestion (Y ang Y. et al., 2015). Some
LAB-probiotics provided similar benefits as antibiotics in terms
of weight gain, feed intake, and feed efficiency, as in the case of
Lb. plantarum P-8 (2106CFU/mL) (Wang L. et al., 2015).
Baldwin et al. (2018) showed that a LAB-probiotics
consortium containing Lb. ingluviei, Lb. agilis, and Lb. reuteri
strains improved weight gain when they were inoculated early
at the hatchery, modifying intestinal microbiota and decreasing
the pathogenic taxa numbers in chicks (Baldwin et al., 2018).
On the other hand, a feed supplementation with 1 106CFU/g
feed Lb. johnsonii BS15 in broilers enhanced digestive abilities,
promoting growth performance, and lowering body fat content
(Wang H. et al., 2017).
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Another study carried out on pigs fed with Lb. plantarum
ATCC 4336, Lb. fermentum DSM 20016, and Ent. faecium ATCC
19434 at concentrations of 1011CFU/kg resulted in a weight gain
due to the ability of these strains, mainly Lb.ones, to produce
enzymes enhancing feed digestion, besides lactic acid production
(Veizaj-Delia et al., 2010). Lan et al. (2016) showed that a strain
ofLb. acidophilus increased digestibility in weaning piglets of
14 days-old and improved their growth performance.
However, supplementation of feed with LAB-probiotics did
not induce any effect on the animal weight in all cases. Wang et al.
(2012) showed that Lactobacillus orPediococcus fermented maize
feed can modify the microbiota but did not affect pig’s production
performances. This variability is related to a heterogeneity
between trials. Nonetheless, for pigs, environmental factors such
as pen, litter : : :the sow and piglet are closely related according to
Zimmermann et al. (2016).
Concerning ruminants, calves fed with a mixture of
1109CFU of Lb. casei DSPV 318T, Lb. salivarius DSPV
315T, and Ped. acidilactici DSPV 006T exhibited higher daily
weight gain, total feed intake, and starter diet intake (Frizzo
et al., 2010). Furthermore, calves fed with 6.8 108CFU of
Lb. acidophilus and Lb. plantarum fortified milk (Gupta et al.,
2015) or 11010CFU of Lb. plantarum DSPV 354T (Soto
et al., 2014) consumed more milk, in addition to body weight
gain and growth performance. A similar effect has been reported
for post weaning lambs. When they were fed with Pediococci
(1106CFU/g) an increased intake of dry matter feed and better
growth performances were shown (Saleem et al., 2017).
In the aquaculture sector, Zheng et al. (2017) showed a
size improvement in white shrimps ( Litopenaeus vannamei )
when their diet was supplemented with 1 109CFU/mL of
Lb. plantarum. Furthermore, Lb. delbrueckii also enhanced the
production performance of Cyprinus carpio Huanghe var., when
added at a concentration of 1067CFU/g in feed (Zhang et al.,
2017). In abalones ( Haliotis discus hannai Ino) feed intake and
growth increases were observed when Lb. pentosus was supplied
at concentration of 1035CFU/g (Gao et al., 2018).
Improvement of the Quality of Livestock
Products
There are several examples of Lactobacillus spp. as probiotic
improving meat quality in chickens, including tenderness,
appearance, texture, and juiciness among other parameters (Park
et al., 2016). It is known that addition of LAB to broiler’s
feed reduced the cholesterol content of meat (Popova, 2017).
Administration of Lb. salivarius SMXD51, at a concentration of
107CFU/mL, can partially prevent the impact of Campylobacter
in chickens due to ability of this strain to produce an anti-
Campylobacter bacteriocin with strong activity against four tested
Campylobacter jejuni strains (Messaoudi et al., 2012; Saint-
Cyr et al., 2017). In addition, the probiotics can improve the
production and quality of eggs. Thus, the supplementation of
Ped. acidilactici MA 18/5M (108CFU/kg feed) to the chicken
feed revealed an effect on the eggs’ quality by increasing their
weight, eggshell thickness and decreasing cholesterol on the egg
yolk (Mikulski et al., 2012).In pigs, Ped. acidilactici was shown to improve meat quality
(Dowarah et al., 2018). Kiczorowska et al. (2017b) compared
four groups of cows and demonstrated that cows under an
intensive production system receiving a probiotic treatment [ Lb.
casei ,Lb. plantarum (5106CFU/mL)], and S. cerevisiae
(5103CFU/mL) produced higher milk quality with higher
protein content and fat that contained a higher amount
of unsaturated fatty acids conversely to cows in intensive
production system. It was shown that supplementation of feed
with 4109CFU Lb. acidophilus NP51 and Propionibacterium
freudenreichii NP24 increased milk production and improved
apparent digestibility of dietary nutrient (Boyd et al., 2011).
Fish Reproduction
Probiotics are associated with fish reproduction by enhancing
their fecundity rate (Banerjee and Ray, 2017; Carnevali et al.,
2017). The direct effects are reportedly due to increasing
expression of genes encoding several hormones and enhancing
gonadal growth, fecundity, and embryo survival (Gioacchini
et al., 2010, 2012). Probiotics also enhance follicules maturation
and development, and embryo quality. For example, several
strains of Lb. rhamnosus can improve the fecundity in zebrafish
(Danio rerio) model (Hai, 2015; Banerjee and Ray, 2017).
Water Quality
The quality of water on the fish farms is clearly an important
factor to avoid the spread of diseases. The parameters to measure
this quality are based on the pH of the water and the amounts
of CO 2, ammonia, nitrate, and phosphorus found in it. Lb.
plantarum and Lb. casei reportedly maintained or improved
water quality during fish production (Banerjee and Ray, 2017).
A major concern is related to water pollution with heavy
metals provoking fish diseases. This can be avoided by the
use of some LAB-probiotics such as Lb. plantarum CCFM639,
which restored the integrity of damaged tight junction proteins
and maintained intestinal permeability leading to decrease of
aluminum-induced gut injuries (Yu et al., 2016). Yu et al. (2017)
also reported reduction of aluminum accumulation in tilapia
tissues and lower death rate upon incorporation of 108CFU/g
Lb. plantarum to the feed.
SYNBIOTICS
Synbiotics are defined as combination of probiotics and
prebiotics that beneficially affect the host by improving survival
and settlement of live microbial dietary supplements in the
gastrointestinal tract. This happens by selectively stimulating
the growth and/or by activating the metabolism of one or
a limited number of health-promoting bacteria, and thus
improving host welfare (Gibson et al., 2004). A prebiotic
that confers gastrointestinal health benefits could support the
growth of a probiotic which has activity against a potential
pathogen (Allen et al., 2013).
Guerra-Ordaz et al. (2014) reported a synergistic effect when
Lb. plantarum (21010CFU) and lactulose (10 g/kg feed)
were concomitantly used to treat colibacillosis in pigs, reducing
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diarrhea and improving the average daily weight gain. Y asuda
et al. (2007) showed that Lb. casei subsp. casei (1107CFU/kg
feed) and dextran (5%, w/w) in combination improved the
milk yield and milk components in cows, and they hypothesize
the symbiotic association had a prophylactic effect inhibiting
mastitis development. Data from Naqid et al. (2015) suggested
caution on the use of synbiotics because intra-interaction can
occur within the combination and reduce the expected activity.
Mookiah et al. (2014) showed same body weight increase in
chickens treated with multi-strain Lactobacillus probiotic at
1109CFU/g or prebiotic (isomalto-oligosaccharides; 5 or
10 g/kg of feed) separately or their association as synbiotic.
Szczurek et al. (2018) showed that synbiotic composed of whey
lactose and Lb. agilis did not show any advantage when compared
to each compound alone.
In fish, the administration of Ent. faecalis and mannan-
oligosaccharides enhanced growth, immune response, and
survival of Rainbow trout ( Oncorhynchus mykiss ) to the infection
ofA. salmonicida (Rodriguez-Estrada et al., 2013). In Tilapia,
there is an effect against A. hydrophila when the combination of
1108CFU Lb. brevis JCM 1170 or Lb. plantarum JCM 1149
and fructo-oligosaccharides (1 g/kg feed) were added to the feed,
but the same combination did not improve animal growth or feed
conversion (Liu et al., 2017).
CONCLUSION AND FUTURE DESIGN OF
LAB-PROBIOTICS
This review highlighted numerous advantages from LAB-
probiotics used in animal farming and production. After
the indiscriminate use of antibiotics in livestock to increase
the animal performance, resistance to these molecules has
dramatically escalated. To help reduce this worldwide concern,
the use of LAB-probiotics stands as an efficient and promising
alternative. Different benefits have been observed in animals
fed with various LAB-probiotics. As supported by a variety of
studies, LAB-probiotics can control the development of bacterial
diseases, increase weight gain in healthy and affected animals,
stimulate the quality of the (by-) products of this industry
or even improve aquaculture water quality. LAB-probiotics
can control bacterial infections by excretion of inhibitory
compounds, or by other mechanisms including competitive
exclusion, decreasing bioavailability of toxins, strengtheningintestinal barrier or positively stimulating the immune system.
Their actions are exerted in strain and host-specific manners.
Finally, there are a variety of synergistic effects when combining
LAB with other probiotic species, prebiotics, or enzymes.
In terms of future design, recombinant LAB-probiotics may
offer additional advantages. Pioneering studies have already
opened this avenue. Indeed, it has been reported that Lb.
plantarum NC8 can produce a recombinant dendritic cell-
targeting peptide with activity against H9N2 avian influenza
virus in chickens (Shi et al., 2016; Wang X. et al., 2017).
Also, this recombinant dendritic cell-targeting peptide can
be used synergistically to enhance vaccine humoral immune
responses and to reduce viral replication in chicken lungs
(Shi et al., 2016).
ETHICS STATEMENT
All authors of this paper have read and approved the final
version submitted. The contents of this manuscript have not been
copyrighted or published previously. No procedures performed
in these studies have been conducted in human participants
and/or animals.
AUTHOR CONTRIBUTIONS
All authors listed have made a substantial, direct and intellectual
contribution to the work, and approved it for publication.
FUNDING
NV-S received an ANRT Ph.D. grant funded by Phileo
Business Unit from Lesaffre International. This work was
partly supported by Sincolistin ANR grant coordinated by DD
(ANR-15-CE21-0015).
ACKNOWLEDGMENTS
The authors are indebted to Dr. Bruce Seal (Oregon State
University Cascades) for his permanent enthusiastic critical
reading of the manuscript and English improvement.
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Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
The handling Editor declared a past co-authorship with one of the authors DD.
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