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Cuban Journal of Agricultural Science

Print version ISSN 0864-0408On-line version ISSN 2079-3480

Cuban J. Agric. Sci. vol.54 no.2 Mayabeque Apr.-June 2020  Epub June 01, 2020

 

REVIEW ARTICLE

Probiotic potential of Lactobacillus salivarius in animals of zootechnical interest

1Centro de Estudios Biotecnológicos, Universidad de Matanzas. Autopista Varadero km 3 ½, Matanzas, Cuba.

Abstract

Probiotics are living microorganisms that, when consumed in adequate amounts, confer benefits tohost health. Lactic acid bacteria are the most widely used, especially those of Lactobacillus genus. One of the species of this genus is Lactobacillus salivarius, capable of colonizing the digestive tract of humans and animals. It resists gastric barriers of acid pH and bile, and produces antimicrobial substances, such as organic acids and bacteriocins that inhibit different pathogenic microorganisms. This bacterium attaches to epithelial cells and stimulates the immune system. For these reasons, there is a lot of research aimed to evaluating the effect of Lactobacillus salivarius in monocultures or multi-strains, on microbiological, physiological, productive and health indicators in animals of zootechnical interest. There is evidence of the results of the selection process of strains from the digestive tract of animals, in which they are candidates for their in vitro and in vivo probiotic activity. This review has the objective of evaluating the probiotic potential of Lactobacillus salivarius and its effect on poultry, pig farming and calf rearing. In addition, some future considerations are recommended for its use as a probiotic additive in animal production.

Key words: probiotics; Lactobacillus salivarius; poultry; pigs; calves

INTRODUCTION

Probiotics are living microorganisms that, when consumed in adequate amounts, confer benefits to host health (Guarner and Schaafsma 1998). Obtaining probiotic biopreparations, from the isolation and selection of beneficial microorganisms of the digestive tract of animals, is the beginning of their application in animal production. These zootechnical additives are provided in order to be used as animal growth promoters (AGP), since they improve the gastrointestinal microbiota composition and food use efficiency, stimulate the immune system and inhibit pathogenic microorganisms, without the use of antibiotics (Hou etal. 2015).

Lactobacillus is the most widely used genus of all the bacterial probiotics (Castañeda 2018). Lactobacillus salivarius is especially known for its probiotic properties and considerable functional diversity of chromosomes and plasmids (Cousin et al. 2017, Harris et al. 2018 and Lee et al. 2017). This bacterium is found in the microbial population of the digestive tract of animals of zootechnical interest, such as chickens (Garrigaet al. 1998), pigs (Nemcova et al. 1997 and Korhonen et al. 2007), ducks (Ehrmannet al. 2002) and calves (Schneider et al. 2000).

Different strains of L. salivarius species have the ability to modulate the balance of the intestinal microbiota, produce antimicrobial and anticancer substances, stimulate immune system response, increase tract enzymatic activity, produce short chain fatty acids and decrease pH. Hence, productive indicators and health of animals of zootechnical interest improve (Messaoudiet al. 2013, Zhang et al. 2013 and Chaves et al. 2017). Therefore, the objective of the current research was to assess results of studies on probiotic potential of Lactobacillus salivarius and its effect on poultry, pig farming and calf rearing.

PROBIOTIC PROPERTIES OF LACTOBACILLUS SALIVARIUS

Table 1 presents researches carried out by different authors with strains of Lactobacillussalivarius, demonstrating their in vitro probiotic properties. Thesestudies have confirmed that this bacterium develops mechanisms that favor its resistance to adverse conditions of the gastrointestinal ecosystem.Inaddition, it has the ability to adhere to the intestinal mucosa, allowing to exclude pathogenic microorganisms and stimulate the immune system. It is also demonstrated that it produces antimicrobial substances, especially organic acids, bacteriocins, and hydrogen peroxide, and specific enzymes that could contribute to improve digestibility of diet components, and thereby increase the productive performance and animal health. It is known that this bacterium produces the enzyme hydrolase bile salt, which helps to resist the presence of bile and subsequently colonize the intestine.

Table 1 In vitro probiotic properties of Lactobacillus salivarius. 

Strain Probioticcharacteristics Reference
Lactobacillus salivarius subsp. salivarius CRL1384 It produces bacteriocins that inhibits the growth of ListeriaandSalmonella Audisioand Apella (2006)
L. salivarius They produce bacteriocins of classIIb, salivaricin T, salivaricin P and ABP-118 and those of classIId, known as bactofencin A. Barret et al. (2007), Messaoudiet al. (2013), Guinaneet al. (2015)
L. salivarius UCO-979C-1 They are resistant to low pH (pH 2.6), because they protect themselves by the production of high levels of exopolysaccharides surrounding the cells Sanhueza et al. (2015)
L. salivarius They produce peptidase proteins(LysMand M23B) with antistaphylococcic potential Kang et al. (2017)
Lactobacillus salivarius C-7 and C-65 They are resistant to acid pH and the presence of biliary salts. They show great capacity of adherence and growth speed, produce organic acids, inhibit in vitro pathogenic microorganisms (Escherichia coli 0157:H7, Listeria innocua, Listeria monocytogenes, Salmonella enteritidis, Staphylococcus aureus ATCC- 29737, Enterobacter cloacae ATCC-13047, Klebsiella spp. ATCC-11296, Staphylococcus epidermidis ATCC-12228, Proteus vulgaris ATCC-13315,and Salmonella thyphimuriumATCC-14028). Rondón et al. (2008), Rondón et al. (2012)
Lactobacillussalivarius SMXD51 It produces a very active bacteriocin in front of Campylobacter jejuniand inhibits Pseudomonas aeruginosa PAO1, by reducing transepithelial electric resistance and provoking damages to the F-actin from the cytoskeleton of pathogen cells Messaoudiet al. (2012)
L. salivariusB37 and B60 They produce different immunomodulator factors, capable of suppressing the production of Interleukin 8 (IL-8) by gastric epithelial cells, induced by the presence of Helicobacter pylori Panpetchet al. (2016)
L. salivarius CECT 5713 They reduce the presence of Streptococcus mutans Sañudo et al. (2017)
L. salivarius ATCC 11741 Wasfiet al. (2018)
L. salivariusMG242 It inhibits growth of vaginal pathogens Gardnerella vaginalisandCandida albicans Kang et al. (2018)
L. salivariusLs-BU2 It has antimicrobial activity in front of Escherichia coli Moradiet al. (2019)
L. salivarius It produces hydrolase bile salt for deconjugate bile salts Xuet al. (2019)
L. salivarius It adheres to intestinal mucosa Wang et al. (2017), Martín et al. (2019)

These in vitro studies are carried out with the purpose of selecting the strains with the highest probiotic potential. However, its use should not be considered until its effect on animals is evaluated. Table 1 shows results of the application of Lactobacillus salivarius in poultry, pigs and calves, in which the advantages of using this bacterium as a modulator of intestinal microbiota have been demonstrated.

EFFECT OF LACTOBACILLUS SALIVARIUS ON POULTRY

Dumonceauxet al. (2006), Rondón et al. (2008) and Nouri et al. (2010) conducted studies of microorganisms within chicken intestines, and determined that Lactobacillussalivarius is among the three predominant species, together with L. crispatus and L.buchneri.

Sornplanget al. (2015) evaluated the probiotic effect of two L. salivarius strains (L61 and L55) and their mixture in newly hatched broilers. After infection with Salmonellaenteritidis (SE), broilers were treated with this additive for seven days. Results demonstrated that the treatment with L. salivarius L61 and L. salivarius L55, alone or combined, increased survival rate after SE infection, increased heterophilic phagocytosis and phagocytic index (PI), and, at the same time, it caused the reduction of this pathogen in caecal tonsils. It is argued that these bacteria, besides acids, produce bacteriocins, which destroy the cytoplasmic membrane integrity through the formation of pores. This causes the exit of small compounds or the alteration of the proton motive force, necessary for energy production, synthesis of proteins or nucleic acids (Chikindaset al. 1993).

Other authors, such as Shokryazdanet al. (2017), applied a mixture of three Lactobacillussalivarius strains (CI1, CI2 and CI3), from the intestine of broilers. Supplementation with this mixture at a concentration of 0.5 or 1 g.kg-1 of diet for 42 d, improved liveweight, weight gain, and feed conversion. Total cholesterol, LDL cholesterol, and triglycerides decreased, and beneficial bacteria population, such as lactobacilli and bifidobacteria, increased. Harmful bacteria, such as E. coli, and caecal bacterial enzymes, including β-glucosidase and β-glucuronidase, also decreased.

Clavijo and Flórez (2017) reported that the gastrointestinal microbiome of animals is related to pathogenic control. A mixture of Lactobacillus ingluviei UMNPBX19 and Lactobacillus salivarius UMNPBX2 was applied to turkeys with Salmonella Heidelberg. As a result, in vivo studies revealed that these probiotics significantly reduced the spread of Salmonella in the liver and gizzard, as well as colonization of caecum (1.9- and 3.9-Log CFU.g-1) in relation to control (Vazhakkattuet al. 2019).

These microbial cultures were also inoculated in ovo. Studies carried out by Bednarczyk et al. (2016) and Siweket al. (2018) reported that this application of probiotics could provide efficient colonization of embryonic microbiome with commensal bacteria during the perinatalperiod. Aleksandrzak-Piekarezyk (2019) injectedin ovobiopreparations of Lactobacillus plantarum IBB3036 and Lactobacillus salivarius IBB3154 ​​into fertilized eggs from Cobb500 hens, and evaluated the permanence of these bacteria in the GIT of chickens using PCR technique. These authors verified that L. salivarius increased its population significantly in the intestines of chickens, while L. plantarum gradually decreased in this ecosystem.

Chen et al. (2017) studied the probiotic effect of Lactobacillus salivarius and Pediococcuspentosaceus strains in specific-pathogen-free (SPF) poultry. As a result, probiotics increased liveweight, daily mean gain, crude protein apparent digestibility, abdominal fat content, and Lactobacillus population in the caecum. Besides, plasmaammonia content, ammonia emission in feces, pH and the amount of Escherichia coli in the caecal content of poultry decreased. This indicates that this microorganism can contribute to the decrease of greenhouse gasemissions.

It was verified that the application of L. salivarius DSPV 001P in poultry diet, under low temperature conditions (18-22ºC during the first three weeks and between 8-12ºC in the rest), caused an increase of animal liveweight (2905 ± 365.4 g), with respect to control group (2724 ± 427.0 g). There were no differences in feed intake, and feed conversion was improved during the six weeks of the experiment. Likewise, probiotic supplementation reduced mortality and the presence of L. salivarius strain was detected for 28 d in the GIT content of these animals (Blajmanet al. 2017).

With the aim of evaluating the antibacterial effect of Lactobacillus salivarius SMXD51 and the mechanisms it uses for controllingCampylobacter jejuni in broilers, Saint-Cyr etal. (2017) developed an experiment with 30 chickens,artificially infected with these pathogenic bacteria, orally treated with MRS broth or with a bacterial suspension (107 CFU in MRS broth) of probiotic bacteria. The 73% of chickens treated with the probiotic culture showed lower values of Campylobacter ​​than those of control group.

Babot et al. (2018), among other authors, used Lactobacillus salivarius in formulations with multi-strain probiotics. In their study, they mixed Lactobacillus salivarius LET201, Lactobacillus reuteri LET210, Enterococcus faecium LET301, Propionibacteriumacidipropionici LET103 and Bifidobacteriuminfantis CRL1395 for their application in broilers. They concluded that the combination of these strains was effective for protecting epithelial cells from cytotoxicity from the mixture of soy agglutinin, wheat germ agglutinin and concanavalin A.

Dec et al. (2014) evaluated the probiotic properties of Lactobacillus strains, isolated from feces or cloacae of domestic geese. Among the 104 isolates, examined and previously identified by analysis of the 16S-23S region of rDNA, Lactobacillus salivarius (35%) dominated, followed by Lactobacillus johnsonii (18%) and Lactobacillus ingluviei (11%). Antimicrobial activity towards Salmonella enteritidis, Escherichia coli, Clostridium perfringens, Staphylococcus aureus, Pasteurellamultocida and Riemerellaanatipestifer was evaluated. Lactobacillus salivariusand Lactobacillus plantarumdemonstrated a particularly strong antagonism towards all indicator strains, especially due to the production of lactic acid by these bacteria.

Pérez et al. (2012) evaluated the effect of SUBTILPROBIO® and PROBIOLACTIL® probiotic mixture in laying hens. Animals that received it had higher production throughout the period. There were differences (P <0.05), since a higher layingpercentage was obtained and the number of eggs per animal increased.

The probiotic activity of Lactobacillus salivarius cultures in productive indicators should be analyzed from the perspective of the influence these microorganisms exert on digestive physiology of animals. The establishment of the eubiosis of the ecosystem, with better fermentative and microbiological patterns in the GIT, the stimulation of the immune state of fowls through a higher humoral response and a larger size of lymphoid organs, are just some reasons that led animals to express weight gain, with better body composition and physiological maturity (Rondónet al. 2018).

EFFECT OF LACTOBACILLUS SALIVARIUS IN PIGS

According to authors such as Pieper et al. (2006), in pigs, Lactobacillus salivarius, L. fermentum and L. acidophilusstrains are the most abundant lactobacilli of the ileum microbial community during weaning period. In particular, L. salivarius is used in monocultures or mixtures with probiotic potential in these animals.

Riboulet-Bisso et al. (2012) stated that the application of L. salivarius UCC118 WT reduced the number of Gram-negative bacteria present in the intestine of pigs. These results were also confirmed by Yeo et al. (2016), who used Lactobacillus salivarius LS6 strain, which prevents the disruption of the integrity of the intestinal epithelium of these animals by inhibiting adherence of pathogenic bacteria, such as enterotoxigenic Escherichia coli K88.

Sayan et al. (2018) developed an experiment in piglets to evaluate the effect of oral supplementation of Lactobacillus salivarius on the improvement of intestinal health, live weight, diarrhea incidence, bacterial population and intestinal morphology, by defying animals with enterotoxigenic Escherichia coli F4+. As a result, pigs treated with the probiotic increased live weight, daily mean gain and weight gain, and diarrhea incidence decreased. Lactobacillipopulation in feces increased and histomorphology improved, as the height of microvilli in the duodenum and jejunum increased.

This strain was also used in probiotic mixtures to evaluate its antimicrobial activity in pigs contaminated with Salmonella enterica and Serovar typhimurium. The mixture was constituted with strains of Lactobacillus murinus, Lactobacillus salivarius subsp. salivarius, Lactobacillus pentosus and Pediococcuspentosaceous. Animals treated with the probiotic showed a reduction of incidence, severity and duration of diarrheas. The number of Salmonella in feces was also decreased (P <0.01) at 15 d post-infection (Casey et al. 2007).

In order to evaluate the probiotic activity of the biopreparation with Lactobacillussalivarius C-65 in productive and health indicators in pigs, an experiment was carried out with a completely randomized design in which two treatments were included: I) basal diet (control) and II (basal diet + biopreparation C65). As a result of the use of this bio-preparation, eubiosis state of the gastrointestinal tract improved, which contributed to increase (P ≤ 0.05) live weight of animals at five weeks and daily weight gain. In addition, there was a decrease of feed conversion and diarrhea incidence of animals treated with the additive (Rondónet al. 2013).

Socorro (2016) evaluated the influence of PROBIOLACTIL® (Lactobacillus salivarius C-65 strain), SUBTILPROBIO® (Bacillussubtilis C-31 strain) and the mixture of both additives on productive and health indicators in pigs during rearing and pre-fattening stages. As a result, it was found that the additives and their mixture improved all indicators with respect to control. The superior effects occurred in pigsconsuming PROBIOLACTIL®. The evaluated biopreparations had beneficial action on animals, since they improved eubiosis of the gastrointestinal tract, which contributed to increase (P ≤ 0.05) live weight (27.15 kg/25.59 kg), daily weight gain of animals (408.65 g / 445.27 g), weight gain (18.70 kg/17.16 kg) and feed conversion (2.90/2.44). In addition, diarrhea incidence decreased in treated animals.

EFFECT OF LACTOBACILLUS SALIVARIUS ON CALVES

Flores (2015) evaluated the effect of a probiotic on productive and health indicators of lactating calves of Mambí de Cuba breed. This additive (PROBIOLACTIL®) was prepared with Lactobacillus salivarius C-65 strain and calves between 7 and 9 d of birth were used. As a result, the calves that consumed food additive showed a lower diarrhea incidence and parasitic diseases. Furthermore, improvements (P ≤ 0.05) were observed in live weight increase with respect to control group.

Soto et al. (2015) evaluated the effect of a probiotic mixture of Lactobacillus casei DSPV318T, Lactobacillus salivarius DSPV315T and Pediococcusacidilactici DSPV006T on hematological and immunological parameters, and on biochemical profiles ofliver and kidney of calves, before and after their infection with Salmonella DS5. These authors demonstrated that neutrophil/lymphocyte levels were increased, which shows that stimulation of the specific immune response occurred. There were no changes in the remaining indicators.

The aforementioned results indicate the need of using these additives in calves, mainly during the first weeks of life and after their separation from the cow, since they can prevent infection with pathogenic bacteria resulting in the presence of diarrhea.

Rondónet al. (2019) used henequen pulp (rich in inulin), with the addition of final molasses as a source of reducing sugars, yeast hydrolyzate, as nitrogen source and PROBIOLACTIL®, as inoculum for Lactobacillussalivariussupplementation. This symbiotic biopreparation was provided to calves during the rearing stage. It was demonstrated that the application of the additive improvedlive weight indicators, mean daily gain, weight gain and feed conversion. Likewise, this additive influenced on animal health by reducing diarrhea occurrence from the first weeks of the experiment. These results demonstrate that this bacterium can also be used in the treatment of agro-industrial residues for their use as animal feed, because it improves their nutritional quality, digestibility and conservation.

The effect of Sorbial probiotic (contains Lactobacillus salivarius) on calves was evaluated by Socaet al. (2011), who reported that animals treated with this probiotic increased live weight and daily mean gain (758 g/animal/d). However, they did not indicate differences in hematological indicators.

Resultsof the application of L. salivarius in the diet and the evaluation of performance of microbiological, immunological, fermentative, hematological and morphometric indicators in animals, demonstrate its multifactorial effect. Its supplementation in the diet causes different interrelated processes and, as a consequence, leads to improvements in physiology, performance and health of poultry, pigs and calves.

This bacterium was also isolated from the vagina and nipple canal of cows (Fernández et al. 2016 and Kang et al. 2018), so that, in the future, its antimicrobial activity against pathogenic microorganisms could be evaluated in these environments, with the purpose of preventing postpartum infections of the urogenital system and mastitis.

CONCLUSIONS

Lactobacillus salivarius is a bacterium with probiotic potential, which is found in the digestive tract of animals of zootechnical interest. Researches conducted up to this moment describe its immunomodulatory properties and the effect they cause on the digestive tract of animals, by producing antimicrobial substances in the presence of pathogenic microorganisms, adhering and colonizing the mucosa, improving nutrient digestibility and causing an increase of productive and health indicators in species consuming this probiotic.

REFERENCES

Aleksandrzak-Piekarczyk, T., Puzia, W., Żylińska, J., Cieśla, J., Gulewicz, K., Bardowski, J.K. & Górecki, R.K. 2019. "Potential of Lactobacillus plantarum IBB3036 and Lactobacillus salivarius IBB3154 to persistence in chicken after in ovo delivery". MicrobiologyOpen, 8(1): e620-e632, ISSN: 2045-8827, DOI: https://doi.org/10.1002/mbo3.620Links ]

Audisio, M.K. & Apella, M.C. 2006. "Bacteriocin-like substance produced by Lactobacillus salivarius subsp. salivarius CRL1384 with anti-Listeria and anti-Salmonella effects". Research Journal of Microbiology, 1(1): 61-69, ISSN: 18164935, DOI: https://doi.org/10.3923/jm.2006.61.69Links ]

Babot, J.D., Argañaraz-Martínez, E., Saavedra, L., Apella, M.C & Chaia, A.P. 2018. "Compatibility and safety of five lectinbinding putative probiotic strains for the development of a multi-strain protective culture for poultry". Beneficial Microbes, 9(6): 927-935, ISSN: 1876-2883, DOI: https://doi.org/10.3920/BM2017.0199Links ]

Barrett, E., Hayes, M., O’Connor, P., Gardiner, G., Fitzgerald, G.F., Stanton, C., Ross, R.P. & Hill, C. 2007. "Salivaricin P, one of a family of two-component antilisterial bacteriocins produced by intestinal isolates of Lactobacillus salivariu"s. Applied and Environmental Microbiology, 73(11): 3719-3723, ISNN: 1098-5336, DOI: https://doi.org/10.1128/AEM.00666-06Links ]

Bednarczyk, M., Stadnicka, K., Kozłowska, I., Abiuso, C., Tavaniello, S. & Dankowiakowska, A. 2016. "Influence of different prebiotics and mode of their administration on broiler chicken performance". Animal, 10(8): 1271-1279, ISSN: 1751-7311, DOI: https://doi.org/10.1017/S1751731116000173Links ]

Blajman, J.E., Olivero, C.A., Fusari, M.L., Zimmermann, J.A., Rossler, E., Berisvil, A.P. , Romero Scharpen, A., Astesana, D.M., Soto, L.P., Signorini, M.L., Zbrun, M.V. & Frizzo, L.S. 2017. "Impact of lyophilized Lactobacillus salivarius DSPV 001P administration on growth performance, microbial translocation, and gastrointestinal microbiota of broilers reared under low ambient temperature". Research in Veterinary Science, 114: 388-394, ISSN: 0034-5288, DOI: https://doi.org/10.1016/j.rvsc.2017.07.011Links ]

Casey, P., Gardiner, G.E., Casey, G., Bradshaw, B., Lawlor, P.G., Lynch, P.B., Leonard, F.C., Stanton, C., Ross, R.P., Fitzgerald, G.F. & Hill, C. 2007. "A five-strain probiotic combination reduces pathogen shedding and alleviates disease signs in pigs challenged with Salmonella enterica serovar typhimurium". Applied and Environmental Microbiology, 73(6): 1858-1863, ISSN: 1098-5336, DOI: https://doi.org/10.1128/AEM.01840-06Links ]

Castañeda, C. 2018. "Probiotics: an update". Revista Cubana de Pediatría, 90(2): 286 - 298, ISSN: 1561-3119 [ Links ]

Chaves, B.D., Brashears, M.M. & Nightingale, K.K. 2017. "Applications and safety considerations of Lactobacillus salivarius as a probiotic in animal and human health". Journal of Applied Microbiology, 123: 18-28, ISSN: 1364-5072, DOI: https://doi.org/10.1111/jam.13438Links ]

Chen, F.I., Zhu, L.I. & Qiu, H.I.I. 2017. "Isolation and probiotic potential of Lactobacillus salivarius and Pediococcus pentosaceus in specific pathogen free chickens". Brazilian Journal of Poultry Science, 19(2): 325-332, ISSN: 1806-9061, DOI: https://doi.org/10.1590/1806-9061-2016-0413Links ]

Chikindas, M.L., García-Garcera, M.J., Driesessen, A.J.M., Ledeboer, A.M., Nissen-Mejer, J., Nes, I.F., Abee, T., Konings, W.N. & Venema, G. 1993. "PediocinPA-1, a bacteriocin from Pediococcus acidilactici PAC1.0 forms hydrophilic pores in the cytoplasmic membrane of target cells". Applied and Environmental Microbiology, 59(11): 3577-3584, ISSN: 1098-5336 [ Links ]

Clavijo, V. & Flórez, M.J.V. 2017. "The gastrointestinal microbiome and its association with the control of pathogens in broiler chicken production: a review". Poultry Science, 97(3): 1006-1021, ISSN: 1525-3171, DOI: https://doi.org/10.3382/ps/pex359Links ]

Cousin, F.J., Lynch, D.B., Chuat, V., Bourin, M.J.B., Casey, P.G., Dalmasso, M., Harris, H.M.B., McCann, A. & O’Toole, P.W. 2017. "A long and abundant non-coding RNA in Lactobacillus salivarius". Microbial Genomics, 3(9): 1-14, ISSN: 2057-5858, DOI: https://doi.org/10.1099/mgen.0.000126Links ]

Dec, M., Puchalski, A., Urban-Chmiel, A. & Wernicki, A. 2014. "Screening of Lactobacillus strains of domestic goose origin against bacterial poultry pathogens for use as probiotics". Poultry Science, 93(10): 2464-2472, ISSN: 1525-3171, DOI: https://doi.org/10.3382/ps.2014-04025Links ]

Dumonceaux, T.J., Hill, J.E., Hemmingsen, S.M. & Van Kessel, A.G. 2006. "Characterization of intestinal microbiota and response to dietary virginiamycin supplementation in the broiler chicken". Applied and Environmental Microbiology, 72(4): 2815-2823, ISSN: 1098-5336, DOI: https://doi.org/10.1128/AEM.72.4.2815-2823.2006Links ]

Ehrmann, M.A., Kurzak, P., Bauer, J. & Vogel, R.F. 2002. "Characterization of lactobacilli towards their use as probiotic adjuncts in poultry". Journal of Applied Microbiology, 92: 966-975, ISSN: 1364-5072, DOI: https://doi.org/10.1046/j.1365-2672.2002.01608.xLinks ]

Fernández, L., Cárdenas, N., Arroyo, R., Manzano, S., Jiménez, E., Martín, V. & Rodríguez, JM. 2016. "Prevention of infectious mastitis by oral administration of Lactobacillus salivarius PS2 during late pregnancy". Clinical Infectious Diseases, 62(5): 568-573, ISSN: 1058-4838, DOI: https://doi.org/10.1093/cid/civ974Links ]

Flores, R. 2015. Evaluación del efecto de un probiótico en indicadores productivos y de salud en terneros lactantes. Diploma Thesis. Universidad de Matanzas, Cuba [ Links ]

Garriga, M., Pascual, M., Monfort, J.M. & Hugas, M. 1998. "Selection of lactobacilli for chicken probiotic adjuncts". Journal of Applied Microbiology, 84(1): 125-132, ISSN: 1364-5072, DOI: https://doi.org/10.1046/j.1365-2672.1997.00329.xLinks ]

Guarner, F. & Schaafsma, G.J. 1998. "Probiotics". International Journal of Food Microbiology, 39(3): 237-238, ISSN: 0168-1605, DOI: https://doi.org/10.1016/s0168-1605(97)00136-0Links ]

Guinane, C.M., Piper, C., Draper, L.A., O’Connor, P.M., Hill, C., Ross, R.P. & Cotter, P.D. 2015. "Impact of environmental factors on bacteriocin promoter activity in gut derived Lactobacillus salivarius". Applied and Environmental Microbiology, 81(22): 7851-7859, ISSN: 1098-5336, DOI: https://doi.org/10.1128/AEM.02339-15Links ]

Harris, H.M.B., Bourin, M.J.B, Claesson, M.J. & O’Toole, P.W. 2017. "Phylogenomics and comparative genomics of Lactobacillus salivarius, a mammalian gut commensal". Microbial Genomics, 3(8): 1-16, ISSN: 2057-5858, DOI: https://doi.org/10.1099/mgen.0.000115Links ]

Hou, C.H., Zeng, X., Yang, F., Liu, H. & Qiao, S. 2015. "Study and use of the probiotic Lactobacillus reuteri in pigs: a review". Journal of Animal Science and Biotechnology, 6(1): 14-22, ISSN: 2049-1891, DOI: https://doi.org/10.1186/s40104-015-0014-3Links ]

Kang, C.H., Han, S.H., Kim, Y., Paek, N. & So, J.S. 2018. "In vitro probiotic properties of Lactobacillus salivarius MG242 isolated from human vagina". Probiotics and Antimicrobial Proteins, 10(2): 343-349, ISSN: 1867-1306, DOI: https://doi.org/10.1007/s12602-017-9323-5Links ]

Kang, M.S., Lim, H.S., Oh, J.S., Lim, Y.J., Wuertz-Kozak, K., Harro, J.M., Shirtliff, M.E. & Achermann, Y. 2017. "Antimicrobial activity of Lactobacillus salivarius and Lactobacillus fermentum against Staphylococcus aureus". Pathogens and Disease, 75(2): 1-10, ISSN: 2049-632X, DOI: https://doi.org/10.1093/femspd/ftx009Links ]

Korhonen, J.M., Sclivagnotis, Y. & von Wright, A. 2007. "Characterization of dominant cultivable lactobacilli and their antibiotic resistance profiles from faecal samples of weaning piglets". Journal of Applied Microbiology, 103(6): 2496-2503, ISSN: 1364-5072, DOI: https://doi.org/10.1111/j.1365-2672.2007.03483.xLinks ]

Lee, J.Y., Han, G.G., Kim, E.B. & Choi, Y.J. 2017. "Comparative genomics of Lactobacillus salivarius strains focusing on their host adaptation". Microbiological Research, 205: 48-58, ISSN: 0944-5013, DOI: https://doi.org/10.1016/j.micres.2017.08.008Links ]

Martín, C., Fernández-Vega, I., Suárez, J.E. & Quirós, L.M. 2019. "Adherence of Lactobacillus salivarius to heLa cells promotes changes in the expression of the genes involved in biosynthesis of their ligands". Frontiers in Immunology, 10: 3019-3030, ISSN: 1664-3224, DOI: https://doi.org/10.3389/fimmu.2019.03019Links ]

Messaoudi, S., Madi, A., Prévost, H., Feuilloley, M., Manai, M., Dousset, X. & Connil, N. 2012. "In vitro evaluation of the probiotic potential of Lactobacillus salivarius SMXD51". Anaerobe, 18(6): 584-589, ISSN: 1095-8274, DOI: https://doi.org/10.1016/j.anaerobe.2012.10.004Links ]

Messaoudi, S., Manai, M., Kergourlay, G., Prévost, H., Connil, N., Chobert, J.M. & Dousset, X. 2013. "Lactobacillus salivarius: Bacteriocin and probiotic activity". Food Microbiology, 36(2): 296-304, ISSN: 1095-9998, DOI: https://doi.org/10.1016/j.fm.2013.05.010Links ]

Moradi, M., Tajik, H., Mardani, K & Ezati, P. 2019. "Efficacy of lyophilized cell-free supernatant of Lactobacillus salivarius (Ls-BU2) on Escherichia coli and shelf life of ground beef". Veterinary Research Forum, 10(3): 193-198, ISSN: 2322-3618, DOI: https://doi.org/10.30466/vrf.2019.101419.2417Links ]

Nemcova, R., Laukova, A., Gancarcikova, S. & Kastel, R. 1997. "In vitro studies of porcine lactobacilli for possible use". Berliner und Munchener Tierarztliche Wochenschrift, 110(11-12): 413-417, ISSN: 0005-9366 [ Links ]

Nouri, M., Rahbarizadeh, F., Ahmadvand, D., Moosakhani, F., Sadeqzadeh, E., Lavasani, S. & Khoddami Vishteh, V. 2010. "Inhibitory Effects of Lactobacillus salivarius and Lactobacillus crispatus isolated from chicken gastrointestinal tract on Salmonella enteritidis and Escherichia coli growth". Iranian Journal of Biotechnology, 8(1): 32-37, ISSN 1728-3043 [ Links ]

Panpetch, W., Spinler, J.K., Versalovic, J. & Tumwasorn, S. 2016. "Characterization of Lactobacillus salivarius strains B37 and B60 capable of inhibiting IL-8 production in Helicobacter pylori stimulated gastric epithelial cells". BMC Microbiology, 16(1): 242-252, ISSN: 1471-2180, DOI: https://doi.org/10.1186/s12866-016-0861-xLinks ]

Pérez, M., Laurencio, M., Milián, G., Rondón, A., Arteaga, F., Rodríguez & M., Borges, Y. 2012. "Evaluación de una mezcla probiótica en la alimentación de gallinas ponedoras de una unidad de producción comercial". Pastos y Forrajes, 35(3): 311-320, ISSN 0864-0394 [ Links ]

Pieper, R., Janczyk, P., Schumann, R. & Souffrant, W.B. 2006. "The intestinal microflora of piglets around weaning - with emphasis on lactobacilli". Archiva Zootehnica, 9: 28-40, ISSN: 2344-4592 [ Links ]

Riboulet-Bisso, E., Sturme, M.H.J., Jeffery, I.B., O’Donnell, M.M., Neville, B.A., Forde, B.M., Claesson, M.J., Harris, H., Gardiner, G.E., Casey, P.G., Lawlor, P.G., O’Toole, P.W. & Ross, R.P. 2012. "Effect of Lactobacillus salivarius bacteriocin Abp118 on the mouse and pig intestinal microbiota". PLoS ONE, 7(2): e31113, ISSN: 1932-6203, DOI: https://doi.org/10.1371/journal.pone.0031113Links ]

Rondón, A.J., del Valle, A., Milián, G., Arteaga, F., Rodríguez, M., Valdivia, A. & Marlene Martínez . 2019. "Obtención de un biopreparado simbiótico (mezcla de pulpa de Agave fourcroydes Lem. y PROBIOLACTIL®) para su aplicación en terneros". Revista Agrisost, 25(2): 1-9, ISSN: 1025-0247 [ Links ]

Rondón, A.J., Milián, G., Arteaga, F., Boucourt, R., Ranilla, M.J., Riaño, J., Samaniego, L.M., Rodríguez, Z., Pérez, M. & Rodríguez, M. 2012. "Identificación y actividad antimicrobiana de cepas de Lactobacillus de origen avícola". Cuban Journal of Agricultural Science, 46(4): 403-409, ISSN: 2079-3480 [ Links ]

Rondón, A.J., Milián, G., Arteaga, F., Samaniego, L.M., Bocourt, R., Laurencio, M., Rodríguez, M. & Pérez, M. 2018. "Probiotic effect of Lactobacillus salivarius on microbiological and immune indicators in chickens". Revista de la Sociedad Venezolana de Microbiología, 38(1): 21-26, ISSN: 1315-2556, DOI: https://doi.org/10.1590/1806-9061-2016-0413Links ]

Rondón, A.J., Ojito, Y., Arteaga, F., Laurencio, M., Milián, G. & Pérez, Y. 2013. "Probiotic effect of Lactobacillus salivarius C-65 on productive and health indicators of lactating piglets". Cuban Journal of Agricultural Science, 47(4): 401 - 407, ISSN: 2079-3480 [ Links ]

Rondón, A.J., Samaniego, L.M., Bocourt, R., Rodríguez, S., Milián, G., Ranilla, M.J., Laurencio, M. & Pérez, M. 2008. "Isolation, identification and partial characterization of the probiotic properties of Lactobacillus spp. strains obtained from the gastrointestinal tract of broilers". Ciencia y Tecnología Alimentaria, 6(1): 17-22, ISSN: 1135-8122, DOI: https://doi.org/10.1080/11358120809487628Links ]

Saint-Cyr, M.J., Haddad, N., Taminiau, B., Poezevara, T., Quesne, S., Amelot, M., Daube, M., Chemaly, M., Dousset, X. & Guyard-Nicodème, M. 2017. "Use of the potential probiotic strain Lactobacillus salivarius SMXD51 to control Campylobacter jejuni in broilers". International Journal of Food Microbiology, 247(17): 9-17, ISSN: 0168-1605, DOI: https://doi.org/10.1016/j.ijfoodmicro.2016.07.003Links ]

Sanhueza, E., Paredes-Osses, E., González, C.L. & García, A. 2015. "Effect of pH in the survival of Lactobacillus salivarius strain UCO_979C wild type and the pH acid acclimated variant". Electronic Journal of Biotechnology, 18: 343-346, DOI: https://doi.org/10.1016/j.ejbt.2015.06.005Links ]

Sañudo, A.I., Luque, R., Díaz-Ropero, M.P., Fonollá, J. & Bañuelos, O. 2017. "In vitro and in vivo anti-microbial activity evaluation of inactivated cells of Lactobacillus salivarius CECT 5713 against Streptococcus mutan"s. Archives of Oral Biology, 84: 58-63, ISSN: 0003-9969, DOI: https://doi.org/10.1016/j.archoralbio.2017.09.014Links ]

Sayan, H., Assavacheep, P., Angkanaporn, K. & Assavacheep, A. 2018. "Effect of Lactobacillus salivarius on growth performance, diarrhea incidence, fecal bacterial population and intestinal morphology of suckling pigs challenged with F4+ enterotoxigenic Escherichia coli". Asian-Australasian Journal of Animal Sciences, 31(8): 1308-1314, ISSN: 1976-5517, DOI: https://doi.org/10.5713/ajas.17.0746Links ]

Schneider, R., Rosmini, M., Eherman, M. & Vogel, R. 2000. Aplicación de técnicas de RAPD y análisis del 16S rDNA para la identificación de bacterias lácticas componentes de la microbiota aislada de terneros criados en condiciones artificiales. In: VI Congreso Latinoamericano de Microbiología de los Alimentos, Buenos Aires, Argentina, p.75 [ Links ]

Shokryazdan, P., Faseleh Jahromi, M., Liang, J.B., Ramasamy, K., Sieo, C.C. & Ho, Y.W. 2017. "Effects of a Lactobacillus salivarius mixture on performance, intestinal health and serum lipids of broiler chicken"s. PLoS ONE, 12(5): e0175959, ISSN: 1932-6203, DOI: https://doi.org/10.1371/journal.pone.0175959Links ]

Siwek, M., Slawinska, A., Stadnicka, K., Bogucka, J., Dunislawska, A. & Bednarczyk M. 2018. "Prebiotics and synbiotics - in ovo delivery for improved lifespan condition in chicken". BMC Veterinary Research, 14(1): 402-419, ISSN: 1746-6148, DOI: https://doi.org/10.1186/s12917-018-1738-zLinks ]

Soca, M., Ojeda, F., C., E.R & Soca, M. 2011. "Effect of the Sorbial® probiotic on the productive performance and health of grazing calves". Pastos y Forrajes, 34(4): 463-472, ISSN: 0864-0394 [ Links ]

Socorro, M. 2016. Evaluación del efecto probiótico del PROBIOLACTlL®, SUBTILPROBIO® y su mezcla en indicadores productivos y de salud en cerdos lactantes y en preceba. MSc. Thesis. Universidad de Matanzas, Cuba [ Links ]

Sornplang, P., Leelavatcharamas, V. & Soikum, C. 2015. "Heterophil phagocytic activity stimulated by Lactobacillus salivarius L61 and L55 supplementation in broilers with Salmonella Infection". Asian-Australasian Journal of Animal Sciences, 28(11): 1657-61, ISSN: 1976-5517, DOI: https://doi.org/10.5713/ajas.15.0359Links ]

Soto, L.P., Astesana, D.M., Zbrun, M.V., Blajman, J.E., Salvetti, N.R., Berisvil, A.P., Rosmini, M.R., Signorini, M.L. & Frizzo, L.S. 2015. "Probiotic effect on calves infected with Salmonella Dublin: haematological parameters and serum biochemical profile". Beneficial Microbes, 30: 1-12, ISSN: 1876-2883, DOI: https://doi.org/10.3920/BM2014.0176Links ]

Vazhakkattu, J.T., Nair, D.V.T., Noll, S., Johnson, T., Cardona, C. & Kollanoor, A.J. 2019. "Effect of turkey-derived beneficial bacteria Lactobacillus salivarius and Lactobacillus ingluviei on a multidrug-resistant Salmonella Heidelberg strain in turkey poults". Journal of Food Protection, 82(3): 435-440, ISSN: 0362-028X, DOI: https://doi.org/10.4315/0362-028X.JFP-18-286Links ]

Wang, R., Jiang, L., Zhang, M., Zhao, L., Hao, Y., Guo, H., Sang, Y., Zhang, H. & Ren, F. 2017. "The adhesion of Lactobacillus salivarius REN to a human intestinal epithelial cell line requires s-layer proteins". Scientific Reports, 7: 44029, ISSN: 2045-2322, DOI: https://doi.org/10.1038/srep44029Links ]

Wasfi, R., Abd El-Rahman, O.A., Zafer, M.M. & Ashour, H.M. 2018. "Probiotic Lactobacillus sp. inhibit growth, biofilm formation and gene expression of caries-inducing Streptococcus mutans". Journal of Cellular and Molecular Medicine, 22(3): 1972-1983, ISSN: 1582-4934, DOI: https://doi.org/10.1111/jcmm.13496Links ]

Xu, F., Hu, X.J., Singh, W., Geng, W., Tikhonova, I. & Lin, J. 2019. "The complex structure of bile salt hydrolase from Lactobacillus salivarius reveals the structural basis of substrate specificity". Scientific Reports, 9: 12438, ISSN: 2045-2322, DOI: https://doi.org/10.1038/s41598-019-48850-6Links ]

Yeo, S., Lee, S., Park, H., Shin, H. & Holzapfel, W. & Sung, H.Ch. 2016. "Development of putative probiotics as feed additives: validation in a porcine-specific gastrointestinal tract model". Applied Microbiology and Biotechnology, 100(23): 10043-10054, ISSN: 0175-7598, DOI: https://doi.org/10.1007/s00253-016-7812-1Links ]

Zhang, M., Wang, F., Jiang, L., Liu, R., Zhang, L., Lei, X., Li, J., Jiang, J. Guo, H., Fang, B., Zhao, L. & Ren, F. 2013. "Lactobacillus salivarius REN inhibits rat oral cancer induced by 4-nitroquioline 1-oxide". Cancer Prevention Research, 6(7): 686-694, ISSN: 1940-6215, DOI: https://doi.org/10.1158/1940-6207.CAPR-12-0427Links ]

Received: January 27, 2020; Accepted: March 06, 2020

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