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. 2022 Nov 30;2022:4570320. doi: 10.1155/2022/4570320

Beneficial Effects of Lactic Acid Bacteria on Animal Reproduction Function

Mohamad Yusril Nur Mahendra 2, Tri Bhawono Dadi 1, Juriah Kamaludeen 3,4, Herinda Pertiwi 2,✉
PMCID: PMC9729032  PMID: 36505731

Abstract

Considering the importance of a healthy uterus to the success of breeding, the beneficial effects of lactic acid bacteria on animal reproduction function are of particular interest. In recent decades, infertility has become a widespread issue, with microbiological variables playing a significant role. According to reports, dysbiosis of the vaginal microbiota is connected with infertility; however, the effect of the normal vaginal microbiota on infertility is unknown. In addition, lactic acid bacteria dominate the reproductive system. According to evidence, vaginal lactic acid bacteria play a crucial role in limiting the invasion of pathogenic bacteria by triggering anti-inflammatory chemicals through IL-8, IL-1, and IL-6; immunological responses through inhibition of the adherence of other microorganisms, production of inhibiting substances, and stimulation of mucus production; and also reproductive hormones by increased testosterone hormone release, enhanced the levels of luteinizing hormone, follicle stimulating hormone, the amount of prostaglandin E (2), and prostaglandin F2 alpha. The objective of this study was to compare the advantages of lactic acid bacteria in animal reproduction based on the most recent literature. The administration of a single strain or numerous strains of lactic acid bacteria has a favourable impact on steroidogenesis, gametogenesis, and animal fertility.

1. Introduction

Enhancing an animal's return requires high reproductive efficiency [1]. To breed regularly, animals must have functional ovaries, exhibit oestrous behaviour, mate, undergo ovulation, fertilization, conceive, support the embryo during gestation, give birth, continue oestrous cyclicity, and recover uterine function after giving birth [2]. According to Krpalkova et al. [3], infertility is a significant issue that causes economic losses and accounts for the biggest proportion of the total cost in the livestock production system. Economic losses related to infertility issues were the cost of veterinarian intervention, the predicted cost due to calf loss, the cost of cows killed, and the cost of milk loss [4].

The vagina has an inherent microbiome, and dysbiosis of vaginal microbiota or invasion by pathogens may affect fertility by directly reducing spermatozoa's motility or indirectly by producing organic injuries to the reproductive system [5]. The predominant bacterial genus in the vaginal tract is Lactobacillus sp. There is evidence that vaginal Lactobacillus sp. plays a crucial role in avoiding the invasion of pathogenic bacteria and dysbiosis of native microbiota [6]. These lactic acid bacteria's influence on fertility and their role in promoting fecundity could be discussed from two main perspectives: first, male fertility and the potential antioxidant impact of lactic acid bacteria on sperm parameters, testicular histopathology, and testosterone level and second, female fertility and the effect of lactic acid bacteria on maintaining the bacterial balance in the vagina, treatment of bacterial vaginosis, and the subsequent effect on amelioration of bacterial vaginosis [7].

2. Prebiotics, Probiotics, and Synbiotics

The World Health Organization (WHO) defines “probiotics” as living microorganisms that have a positive effect on the host's health [8]. According to the descriptions provided by the International Scientific Association for Probiotics and Prebiotics (ISAPP), the range of goods that could be categorized as probiotics includes helpful bacteria and other types. These include medications and enteral feedings for disease treatment, dietary supplements for health promotion, infant formulas such as milk powders, and even animal feedings [9].

In dairy cows, the reproductive tract can be separated into an upper and lower section based on bacterial presence [10]. The top portion, which includes the fallopian tubes, uterus, and endocervix, is often devoid of bacteria, whereas the bottom portion, which includes the ectocervix and vagina, contains bacteria. Aerobic, facultatively anaerobic, and obligately anaerobic bacteria can be found in the vaginal canal of dairy cows [11]. Plate culture research reveals that the major bacteria in the vaginal canal of healthy heifers are Enterococcus and Staphylococcus, followed by Enterobacteriaceae and Lactobacilli [12]. Moreover, recent research on the uterine microbiome of cows has revealed a vast difference between healthy and metritic or endometritic cows [10]. Regardless of health status, the majority of the uterine microbiota consists of Bacteroidetes, Fusobacteria, Firmicutes, Proteobacteria, and Tenericutes [13]. Also, the vaginal microbiota of cows contains numerous LAB species, such as Lactobacillus spp., Pediococcus spp., Leuconostoc spp., and Weissella spp., some of which were isolated and evaluated for their probiotic powers against urogenital infections [11, 12].

Probiotics are used as feed additives because they have positive effects on animals, such as boosting the immune system [14, 15], eliminating pathogenic bacteria by preventing colonization [16], preventing infection, and enhancing the overall health of the gastrointestinal tract (GIT) [17, 18]. In addition, the results of previous studies indicate that probiotics may be an alternative to antibiotics [19].

Through competing processes, the presence of LAB may have decreased the direct interaction of pathogens with epithelial cells [20]. Otero and Nader-Macas [21] observed that Lactobacillus spp. isolated from the bovine vaginal tract adhered to vaginal epithelial cells at pH 4.5 and 7. Intriguingly, surface layer proteins, which are substances released by probiotic bacteria such as L. helveticus, can also occupy the binding sites on epithelial cells, blocking them from pathogens [22]. Such proteins serve as an epithelial surface lining, hence increasing epithelial integrity and tight junctions [23]. Due to their increased affinity for cell receptors, lactobacilli competitively exclude the adherence of pathogens to the epithelium or even displace pathogens that are already linked to the epithelium [22, 24].

According to Nader-Macas et al. [25], LAB strains isolated from the vaginal tract are highly capable of generating H2O2. Lactobacilli from the vaginal tract of calves that produce H2O2 and lactic acid have the potential to be used as probiotics, with L. gasseri CRL1421 having the greatest potency to inhibit Staphylococcus aureus [21]. A few strains of LAB (mostly Lactobacillus fermentum) isolated from cow vaginal mucus have been shown to inhibit the growth of A. pyogenes in vitro. A. pyogenes is a known pathogen isolated from metritic cows [26]. Through the synthesis of pediocin, Pediococcus acidilactici isolated from healthy pregnant dairy cows inhibits L. innocua and E. faecalis [11]. In addition, pediocin PA, a bacteriocin generated by P. acidilactici, has been characterized as Listeria and other pathogen-inactivating agents [27]. Furthermore, Ohland and Macnaughton [22] found that lactobacilli might boost the expression of mucin, the primary component of the mucus layer, thereby inhibiting pathogens from entering the epithelium in in vitro experiments (Figure 1.). In addition, a recent study has revealed that higher MUC3 mucin secretion reduces the adherence of E. coli strains [28, 29].

Figure 1.

Figure 1

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Mechanisms of pathogen inhibition by LAB probiotics.

Some complex sugars are utilized as prebiotics to increase the likelihood of survival and persistence of bacteria in GIT [30]. Prebiotics are nondigestible compounds that, by modulating the makeup and activity of the gut microbiota, bestow a favourable physiological effect on the host [31]. Numerous substances have been evaluated to establish their prebiotic properties. The most prevalent prebiotics are fructooligosaccharides (FOSs), galactooligosaccharides (GOSs), and transgalactooligosaccharides (TOSs) [32].

The type of gut bacteria and the structure of prebiotics determine fermentation products [33]. Short-chain fatty acids (SCFAs), lactic acid, butyric acid, and propionic acid are produced by the fermentation of prebiotics by gut microbes. These products may have multiple physiological consequences. SCFAs, for instance, lower the pH of the colon [19]; propionate impacts T helper 2 in airways and macrophages, as well as dendritic cells in the bone marrow [34, 35]. Peptidoglycan is an additional prebiotic fermentation product that can enter the bloodstream and stimulate the innate immune system against pathogenic bacteria [35].

Synbiotics combine probiotics and prebiotics synergistically [36]. Understanding problems of sexual differentiation, reproduction, fertility, hypertension, obesity, and physiologic equilibrium, a synbiotic product has a positive effect on the host by enhancing the survival and implantation of live microbial dietary supplements in the gastrointestinal system [37]. In addition, testosterone is produced by Leydig cells through steroidogenesis, which are clustered in the testicular interstitium, by selectively boosting the growth and activating the metabolism of one or a restricted number of health-promoting bacteria [38]. The administration of synbiotics has similarly favourable effects on the gut microbiota. For instance, synbiotics have been shown to increase the number of Bifidobacteria and Lactobacillus, improve stool frequency and mucosal integrity, increase butyrate production, reduce proinflammatory response, and boost lipid metabolism [39–41]. In addition, synbiotics dramatically reduced the incidence of metabolic syndrome, cardiovascular risk factors, and insulin resistance markers among aged people [42].

3. Role of Lactic Acid Bacteria in Steroidogenesis and Gametogenesis

Steroidogenesis is the conversion of cholesterol to glucocorticoids, mineralocorticoids, and sex steroids, which govern physiology and development [43]. Understanding steroidogenesis and its regulation is essential for signals stimulated by luteinizing hormones. For example, it has been observed that probiotic Lactobacillus sp. treatment can increase male reproductive organ function and testosterone hormone release. Using Lactobacillus reuteri ATCC 6475 at a dose of 3.5 × 105 organisms per mouse per day, Poutahidis et al. [44] observed an increase in volume, core diameter, and interstitial Leydig cell area, leading to an increase in testosterone levels.

According to Baer [45], a decrease in testosterone levels results in a variety of negative effects, including a decrease in spermatogenesis, libido, and sexual function, an increase in body fat, a decrease in muscle and bone mass, low energy levels, fatigue, poor physical performance, depressed mood, and cognitive impairment. Gametogenesis is an important aspect of mammalian reproduction in which the germ cell lineage undergoes a series of complex developmental stages and produces mature gametes, spermatozoa, and oocytes [46]. In the same investigation, Poutahidis et al. [44] found that the sperm of mice treated with L. reuteri had significantly higher concentration and activity than age-matched control animals.

Previous studies showed that pretreatment of mice with Lactobacillus rhamnosus G. G. at 109 CFU/ml twice daily for three consecutive days enhanced the amount of basal mucosal prostaglandin E(2) [47], whereas the presence of PGE2 could induce steroidogenesis, production of progesterone, estrone, and estradiol, steroidogenic acute regulatory protein (StAR), and cytochrome P450 family 19 subfamily A member 1 (CYP19A1 gene); this is not the case for steroidogenic acute regulatory protein (StAR) and cytochrome P450 family 19 subfamily A member 1 (CYP19A1 gene) [48]. In addition, Dardmeh et al. [49] discovered that supplementation with Lactobacillus rhamnosus PB01 (DSM-14870) at a dose of 1 × 109 CFU enhanced the levels of luteinizing hormone (L H) (2.170.22 mIU/ml) and follicle-stimulating hormone (FSH) (7.722.05 mIU/ml) in mice. During oocyte meiotic maturation, the L H surge releases oocytes from meiotic prophase arrest and encourages the continuation of oocyte meiosis and completion of the first meiotic division, enhancing oogenesis performance [50].

4. Implication of Lactic Acid Bacteria on Animal Fertility-Related Parameters

There is a direct connection between animal uterine health and reproduction [51]. Fertility issues in animal production units (PAUs) are known to be multifactorial, including disorders in oogenesis, oocyte degeneration, ovulation disorders, failure of fertilization, inflammation of the ovary, disorders of the oviducts, alterations in the uterus such as metritis and endometritis, and early embryonic mortality [52].

When bacterial infection causes severe or prolonged endometrial inflammation, it develops uterine disorders [53]. In addition, proinflammatory substances, such as prostaglandins and cytokines, such as interleukin 1A (IL1A), interleukin 1B (IL1B), and C-X-C motif chemokine ligand 8 (CXCL8), were elevated in cows with preclinical and clinical endometritis [54].

Previous research by Peter et al. [55] using intrauterine supplementation of Lactobacillus buchneri DSM 32407 in cattle demonstrated an increase in tumour necrosis factor mRNA expression (TNF). After three weeks of treatment, the endometrial mRNA expression of many proinflammatory factors (CXCL1/2, CXCL3, CXCR2, IL1B, IL8, and PTPRC) was reduced. The production of CXCL5 is induced by TNF activation of cells [56]. CXCL5 is a chemoattractant that mediates neutrophil recruitment during inflammation and infection; it binds to CXCR2, which is mostly found on the surface of immunological cells, such as polymorphonuclear (PMN) leukocytes [57]. In addition, L. buchneri DSM 32407 supplementation increased total PMN infiltration, indicating that cows with high PMN infiltration within the uterus have greater fertility than cows with low PMN infiltration [10].

Similar research by Gartner et al. [58] demonstrated that Lactobacillus amylovorus isolated from bovine endometrial epithelial cells increased prostaglandin-endoperoxide synthase 2 (PTGS2) expression. The PTGS2 gene, which encodes cyclooxygenase 2 (COX-2) in the body, will play an essential role in oocyte competence acquisition. Moreover, in research utilizing knockout mice models, the elimination of PTGS2 resulted in many reproductive failures, including ovulation, fertilization, implantation, and decidualization damage, demonstrating that prostaglandins produced by COX-2 play an essential role in reproductive processes [59].

A study conducted by Dim et al. [60] using Lactobacillus acidophilus NRRL-4495 (108 CFU/ml) in chicks demonstrated improvement in semen quality, sperm concentration (5.82 × 109/ml), progressive motility (82.93%), live sperm (94.13%), dead sperm (5.87%), normal sperm (91.38%), and abnormal sperm (8.62%). Probiotics' role in producing trace minerals and vitamins in the birds' intestines, which boosts the quality of the sperm, may be responsible for the enhanced sperm quality.

Furthermore, probiotics are associated with fish reproduction by enhancing their fecundity rate [61, 62]. Direct effects are reportedly due to increasing expression of genes, encoding several hormones and improving gonadal growth, fecundity, and embryo survival [63]. Probiotics also increase follicle maturation and development and embryo quality. For example, several strains of Lb. rhamnosus reported have progressive effects on accelerating the fecundity in zebrafish (Danio rerio) models [61].

5. Combinatorial Effects of Lactic Acid Bacteria (as Multistrain Probiotic) on Animal Fertility Outcomes

Multistrain lactic acid probiotics may have a larger spectrum of effects and more mechanisms of action than single-strain probiotics. For example, multistrain probiotic supplementation with Lactobacillus sakei FUA3089, Pediococcus acidilactici FUA3138, and Pediococcus acidilactici FUA3140, with a cell count of 108–109 CFU/dose, was able to produce greater concentrations of PGE2 and prostaglandin F2 alpha metabolite (PGFM) in cattle [20, 64].

The concentration of plasma PGFM is typically used to evaluate the release of endometrial PGF2 secretion once it has a longer half-life in peripheral circulation [65]. This prostaglandin F2 aids the ovulatory process and promotes optimal gamete transport, thereby enhancing fertility [66]. This multistrain probiotic is also used to lower the prevalence of uterine infections associated with elevated vaginal mucus secretory IgA (sIgA) levels [67]. Secretory IgA (SIgA) plays an important role in the protection and homeostatic regulation of intestinal, respiratory, and urogenital mucosal epithelia, separating the outside environment from the inside of the body, which is involved in preventing opportunistic pathogens from entering and disseminating in the systemic compartment, as well as tightly regulating the symbiotic relationship between commensals and the host [68].

Metritis causes infertility in multiple ways: first, by delaying the return to cyclicity after delivery; second, by disrupting the uterine environment; and third, by impeding embryo development [69, 70]. Genis et al. [71] revealed that a combination of L. rhamnosus, P. acidilactici, and L. reuteri produced by CECT (Coleccion Espanola de Cultivos Tipo, CSIC Valencia, Spain) at a ratio of 25 : 25 : 2 had the greatest capacity to modulate E. coli infection and secretion of inflammation markers (IL-8, IL-1, and IL-6) in vitro when compared to individual LAB strains (Table 1).

Table 1.

Effect of lactic acid bacteria on animal reproduction.

Animals Strain Methods Effects References
Bovine L. rhamnosus CECT 278, P. acidilactici CECT 5915, and L. reuteri DSM 20016 Probiotics were administered 1 × 108 CFU/mL in vitro and ex vivo endometrial tissue Reduced the secretion of inflammation markers (IL-8, IL-1β, and IL-6) [72]
Bovine P. acidilactici CECT 5915, L. rhamnosus CECT 278, L. reuteri DSM 20016, and L. sakei DSM 20100 Probiotics were administered 1 × 108 CFU/mL in vitro endometrial tissue LAB has great potential to modulate endometrial infection and inflammation [59]
Bovine L. sakei FUA3089, P. acidilactici FUA3138, and P. acidilactici FUA3140 Probiotic is given intravaginally at a dose of 108–109 CFU Lowered the incidence of metritis and total uterine infections [20]
Dairy cow L. sakei FUA3089 as well as P. acidilactici FUA3138 and FUA3140 Probiotic is given intravaginally at a dose of 1010–1012 CFU Lowered the occurrence of purulent vaginal discharges (PVD) [60]
Dairy cow L. rhamnosus CECT 278, P. acidilactici CECT 5915, and L. reuteri DSM 20016 Probiotic is given intravaginally at a dose of 4.5 × 1010 CFU Showed a lower expression of B-defensins and MUC1 in the endometrium [61]
Swine L. acidophilus and Kluyveromyces fragilis (L-4 UCLV) Probiotic is given orally at a dose of 9 × 107 CFU Improved health of breeding sows and their offspring [62]
Chicken L. plantarum SK3494 Probiotic is given orally at a dose of 1.0 × 109 CFU/mL Improved egg production and performance of laying hens [63]
Chicken Enterococcus faecalis UGRA10 Probiotic is given orally at a dose of 108 Improved egg production and performance of laying hens [64]
Chicken E. faecium DSM 7134 Probiotic is given orally at a dose of 1.0 × 1010 viable spores/g Increased egg production of laying hens [65]
Mice L. rhamnosus PB01 (DSM-14870) Probiotic is given orally at a dose of 1 × 109 CFU Increased serum testosterone, LH, and FSH levels [49]
Mice L. plantarum 2621 Probiotic is given intravaginally at a dose of 108 CFU/20 µl Protection of the vaginal epithelium [66]
Mice L. acidophilus ATCC 4356 Probiotic is given orally at a dose of 1 × 109 CFU Probiotics have antioxidant effects on the testis [67]
Mice L. plantarum ATCC 8014 Probiotic is given orally at a dose of 107 CFU Improved testicular kisspeptin and AR expression, Leydig cell count, and effectively increasing epididymal sperm motility and viability [68]
Mice L.rhamnosus HN001 and L. acidophilus GLa-14 Probiotic is given orally at a dose of 0.32–1.28 × 1011 CFU Reduced the number of Gardnerella vaginalis detected in the vagina [69]
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Reactive oxygen species (ROS) plays a key role in sperm motility. Physiological production at low concentrations has favourable effects on sperm activities and plays a crucial role in sperm metabolism [72]. In the meantime, the excessive production of reactive oxygen species may overwhelm protective mechanisms and cause alterations in lipid and protein layers of the sperm plasma membrane, resulting in lipid damage, protein damage, DNA damage, motility impairment, and alterations in capacity and acrosome reaction [73, 74]. Sperm cell membranes are rich in polyunsaturated fatty acids and vulnerable to oxygen-free radical-induced damage caused by lipid peroxidation [11].

Genis et al. [75] found that a combination of Lactobacillus spp., Bacillus spp., beer yeast, and photosynthetic bacteria culture which are commercially produced by Chuangbo Modern Natural Agriculture Group (Shanghai, China), has antioxidant properties in response to oxidative stress; they also have a potential action to restore the quality of the sperm damaged by diet stress and show significant decreases in lipid peroxidation and nitric oxide (NO) free radical, and significant increases in superoxide dismutase (SOD) and glutathione peroxidase (GSH-Px).

6. Conclusion

Single and multiple strains of lactic acid bacteria supplementation improved steroidogenesis, gametogenesis, and fertility by limiting the invasion of pathogenic bacteria and increasing anti-inflammatory agents, immunological responses, and reproductive hormones.

Data Availability

Information about lactic acid bacteria for animal reproduction function were retrieved from a literature search of electronic databases such as the PubMed, Elsevier, Research Gate, Academia, and Google Scholar. The keywords used to perform the search were lactic acid bacteria, animal reproduction, fertility, and infertility. The research data are presented in the table in the article. Supportive data for discussion and comparison were taken from previous studies, which have been cited from recent journals related to the focus of this article. These data are publicly available and accessible online. Detailed sources are provided in References of the manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  • 1.Khaton R., Sarder M. J. U., Gofur M. R. Biometrical studies of reproductive organs of dairy cows of different genotypes in Bangladesh. The Asian Journal of Animal Science . 2015;9(6):388–395. doi: 10.3923/ajas.2015.388.395. [DOI] [Google Scholar]
  • 2.Abdisa T. Review on the reproductive health problem of dairy cattle. Journal of Dairy & Veterinary Sciences . 2018;5(1) doi: 10.19080/JDVS.2018.05.555655.555655 [DOI] [Google Scholar]
  • 3.Krpalkova L., O’ Mahony N., Carvalho A., Campbell S., Walsh J. Evaluating the economic profit of reproductive performance through the integration of a dynamic programming model on a specific dairy farm. Czech Journal of Animal Science . 2020;65(4):124–134. doi: 10.17221/38/2020-cjas. [DOI] [Google Scholar]
  • 4.Tamador E., Angara E. Economic impact of infertility in crossbred dairy cows: the case of eastern nile locality, Sudan. Indian Journal of Research . 2014;3:195–197. [Google Scholar]
  • 5.Sellami H., Znazen A., Sellami A., et al. Molecular detection of Chlamydia trachomatis and other sexually transmitted bacteria in semen of male partners of infertile couples in Tunisia: the effect on semen parameters and spermatozoa apoptosis markers. PLoS One . 2014;9(7) doi: 10.1371/journal.pone.0098903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Zhang F., Dai J., Chen T. Role of Lactobacillus in female infertility via modulating sperm agglutination and immobilization. Frontiers in Cellular and Infection Microbiology . 2020;10 doi: 10.3389/fcimb.2020.620529.620529 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Younis N., Mahasneh A. Probiotics and the envisaged role in treating human infertility. Middle East Fertility Society Journal . 2020;25(1):33–39. doi: 10.1186/s43043-020-00039-y. [DOI] [Google Scholar]
  • 8.Fijan S. Microorganisms with claimed probiotic properties: an overview of recent literature. International Journal of Environmental Research and Public Health . 2014;11(5):4745–4767. doi: 10.3390/ijerph110504745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Hill C., Guarner F., Reid G., et al. The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology & Hepatology . 2014;11(8):506–514. doi: 10.1038/nrgastro.2014.66. [DOI] [PubMed] [Google Scholar]
  • 10.Gilbert R. O., Santos N. R. Dynamics of postpartum endometrial cytology and bacteriology and their relationship to fertility in dairy cows. Theriogenology . 2016;85(8):1367–1374. doi: 10.1016/j.theriogenology.2015.10.045. [DOI] [PubMed] [Google Scholar]
  • 11.Wang Y., Ametaj B. N., Ambrose D. J., Gänzle M. G. Characterisation of the bacterial microbiota of the vagina of dairy cows and isolation of pediocin-producing Pediococcus acidilactici. BMC Microbiology . 2013;13(1):19–29. doi: 10.1186/1471-2180-13-19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Otero C., Saavedra L., Silva De Ruiz C., Wilde O., Holgado A. R., Nader-Macías M. E. Vaginal bacterial microflora modifications during the growth of healthy cows. Letters in Applied Microbiology . 2000;31(3):251–254. doi: 10.1046/j.1365-2672.2000.00809.x. [DOI] [PubMed] [Google Scholar]
  • 13.Santos T. M. A., Gilbert R. O., Bicalho R. C. Metagenomic analysis of the uterine bacterial microbiota in healthy and metritic postpartum dairy cows. Journal of Dairy Science . 2011;94(1):291–302. doi: 10.3168/jds.2010-3668. [DOI] [PubMed] [Google Scholar]
  • 14.Yan F., Polk D. Probiotics and immune health. Current Opinion in Gastroenterology . 2011;27(6):496–501. doi: 10.1097/mog.0b013e32834baa4d. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Sofyan MS., Rosman N., Krisnu B., Kamaludeen J., Dadi TB., Pertiwi H. Management of feline idiopathic cystitis (FIC) using probiotic combination treatment. Indian Veterinary Journal . 2020;96(12):20–22. [Google Scholar]
  • 16.Buffie C. G., Pamer E. G. Microbiota-mediated colonization resistance against intestinal pathogens. Nature Reviews Immunology . 2013;13(11):790–801. doi: 10.1038/nri3535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Varankovich N., Nickerson M., Korber D. Probiotics-based strategies for therapeutic and prophylactic use against multiple gastrointestinal diseases. Frontiers in Microbiology . 2015;6:1–14. doi: 10.3389/fmicb.2015.00685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Pertiwi H., Sidik R., Sabdoningrum EK., Dadi T. B. Carcass quality of broiler supplemented with spirulina, kelor leaves (Moringa oliefera) and probiotic. Indian Veterinary Journal . 2019;96(11):39–41. [Google Scholar]
  • 19.Heravi R. M., Kermanshahi H., Sankian M., et al. Screening of Lactobacilli bacteria isolated from gastrointestinal tract of broiler chickens for their use as probiotic. African Journal of Microbiology Research . 2011;5:1858–1868. [Google Scholar]
  • 20.Deng Q. Alberta, Canada: University of Alberta; 2014. Application of Intravaginal Lactic Acid Bacteria to Lower Uterine Infections and Improve Reproductive Performance of Postpartum Dairy Cows. Doctoral thesis. [Google Scholar]
  • 21.Otero M. C., Nader-Macas M. E. Inhibition of Staphylococcus aureus by H2O2-producing Lactobacillus gasseri isolated from the vaginal tract of cattle. Animal Reproduction Science . 2006;96(1-2):35–46. doi: 10.1016/j.anireprosci.2005.11.004. [DOI] [PubMed] [Google Scholar]
  • 22.Ohland C. L., Macnaughton W. K. Probiotic bacteria and intestinal epithelial barrier function. American Journal of Physiology - Gastrointestinal and Liver Physiology . 2010;298(6):807–819. doi: 10.1152/ajpgi.00243.2009. [DOI] [PubMed] [Google Scholar]
  • 23.Sherman P. M., Ossa J. C., Johnson-Henry K. Unraveling mechanisms of action of probiotics. Nutrition in Clinical Practice . 2009;24(1):10–14. doi: 10.1177/0884533608329231. [DOI] [PubMed] [Google Scholar]
  • 24.Boris S., Barbés C. Role played by lactobacilli in controlling the population of vaginal pathogens. Microbes and Infection . 2000;2(5):543–546. doi: 10.1016/s1286-4579(00)00313-0. [DOI] [PubMed] [Google Scholar]
  • 25.Nader-Macas M. E. F., Otero M. C., Espeche M. C., Maldonado N. C. Advances in the design of probiotic products for the prevention of major diseases in dairy cattle. Journal of Industrial Microbiology & Biotechnology . 2008;35(11):1387–1395. doi: 10.1007/s10295-008-0438-2. [DOI] [PubMed] [Google Scholar]
  • 26.Otero M. C., Morelli L., Nader-Macías M. E. Probiotic properties of vaginal lactic acid bacteria to prevent metritis in cattle. Letters in Applied Microbiology . 2006;43(1):91–97. doi: 10.1111/j.1472-765x.2006.01914.x. [DOI] [PubMed] [Google Scholar]
  • 27.Woraprayote W., Kingcha Y., Amonphanpokin P., et al. Anti-listeria activity of poly (lactic acid)/sawdust particle biocomposite film impregnated with pediocin PA-1/AcH and its use in raw sliced pork. International Journal of Food Microbiology . 2013;167(2):229–235. doi: 10.1016/j.ijfoodmicro.2013.09.009. [DOI] [PubMed] [Google Scholar]
  • 28.Mack D. R., Ahrne S., Hyde L., Wei S., Hollingsworth M. A. Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut . 2003;52(6):827–833. doi: 10.1136/gut.52.6.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Pan Q., Tian Y., Li X., et al. Enhanced membrane-tethered mucin 3 (MUC3) expression by a tetrameric branched peptide with a conserved TFLK motif inhibits bacteria adherence. Journal of Biological Chemistry . 2013;288(8):5407–5416. doi: 10.1074/jbc.m112.408245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Bednarczyk M., Stadnicka K., Kozłowska I., et al. Influence of different prebiotics and mode of their administration on broiler chicken performance. Animal . 2016;10(8):1271–1279. doi: 10.1017/s1751731116000173. [DOI] [PubMed] [Google Scholar]
  • 31.Bindels L. B., Delzenne N. M., Cani P. D., Walter J. Towards a more comprehensive concept for prebiotics. Nature Reviews Gastroenterology & Hepatology . 2015;12(5):303–310. doi: 10.1038/nrgastro.2015.47. [DOI] [PubMed] [Google Scholar]
  • 32.Davani-Davari D., Negahdaripour M., Karimzadeh I., et al. Prebiotics: definition, types, sources, mechanisms, and clinical applications. Foods . 2019;8(3):p. 92. doi: 10.3390/foods8030092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Zhou Z., Zhang Y., Zheng P., Chen X., Yang Y. Starch structure modulates metabolic activity and gut microbiota profile. Anaerobe . 2013;24:71–78. doi: 10.1016/j.anaerobe.2013.09.012. [DOI] [PubMed] [Google Scholar]
  • 34.Trompette A., Gollwitzer E. S., Yadava K., et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nature Medicine . 2014;20(2):159–166. doi: 10.1038/nm.3444. [DOI] [PubMed] [Google Scholar]
  • 35.Stinson L. F., Payne M. S., Keelan J. A. Planting the seed: origins, composition, and postnatal health significance of the fetal gastrointestinal microbiota. Critical Reviews in Microbiology . 2017;43(3):352–369. doi: 10.1080/1040841x.2016.1211088. [DOI] [PubMed] [Google Scholar]
  • 36.Slavin J. Fiber and prebiotics: mechanisms and health benefits. Nutrients . 2013;5(4):1417–1435. doi: 10.3390/nu5041417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Miller W. L., Auchus R. J. The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocrine Reviews . 2011;32(1):81–151. doi: 10.1210/er.2010-0013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Pandey K. R., Naik S. R., Vakil B. V. Probiotics, prebiotics and synbiotics- a review. Journal of Food Science & Technology . 2015;52(12):7577–7587. doi: 10.1007/s13197-015-1921-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Björklund M., Ouwehand A. C., Forssten S. D., et al. Gut microbiota of healthy elderly NSAID users is selectively modified with the administration of Lactobacillus acidophilus NCFM and lactitol. The age . 2012;34(4):987–999. doi: 10.1007/s11357-011-9294-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Granata M., Brandi G., Borsari A., Gasbarri R., Gioia D. D. Synbiotic yogurt consumption by healthy adults and the elderly: the fate of bifidobacteria and LGG probiotic strain. International Journal of Food Sciences & Nutrition . 2013;64(2):162–168. doi: 10.3109/09637486.2012.718742. [DOI] [PubMed] [Google Scholar]
  • 41.Macfarlane S., Cleary S., Bahrami B., Reynolds N., Macfarlane G. T. Synbiotic consumption changes the metabolism and composition of the gut microbiota in older people and modifies inflammatory processes: a randomised, double-blind, placebo-controlled crossover study. Alimentary Pharmacology & Therapeutics . 2013;38(7):804–816. doi: 10.1111/apt.12453. [DOI] [PubMed] [Google Scholar]
  • 42.Cicero A. F. G., Fogacci F., Bove M., Giovannini M., Borghi C. Impact of a short-term synbiotic supplementation on metabolic syndrome and systemic inflammation in elderly patients: a randomized placebo-controlled clinical trial. European Journal of Nutrition . 2021;60(2):655–663. doi: 10.1007/s00394-020-02271-8. [DOI] [PubMed] [Google Scholar]
  • 43.Bremer A. A., Miller W. L. Regulation of steroidogenesis. Cellular Endocrinology in Health and Disease . 2014;13:207–227. doi: 10.1016/b978-0-12-408134-5.00013-5. [DOI] [Google Scholar]
  • 44.Poutahidis T., Springer A., Levkovich T., et al. Probiotic microbes sustain youthful serum testosterone levels and testicular size in aging mice. PLoS One . 2014;9(1) doi: 10.1371/journal.pone.0084877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Baer J. T. Testosterone replacement therapy to improve health in older males. The Nurse Practitioner . 2012;37(8):39–44. doi: 10.1097/01.npr.0000415874.61843.a6. [DOI] [PubMed] [Google Scholar]
  • 46.Du J., Gao Q. Q., Huang C., et al. In vitro spermatogenesis from pluripotent stem cells. Human Reproductive and Prenatal Genetics . 2019;5:105–128. doi: 10.1016/b978-0-12-813570-9.00005-x. [DOI] [Google Scholar]
  • 47.Lam E. K., Tai E. K., Koo M. W., et al. Enhancement of gastric mucosal integrity by Lactobacillus rhamnosus GG. Life Sciences . 2007;80(23):2128–2136. doi: 10.1016/j.lfs.2007.03.018. [DOI] [PubMed] [Google Scholar]
  • 48.Wang J., Shen X., Huang X. h., Zhao Z. M. Follicular fluid levels of prostaglandin E2 and the effect of prostaglandin E2 on steroidogenesis in granulosa-lutein cells in women with moderate and severe endometriosis undergoing in vitro fertilization and embryo transfer. Chinese Medical Journal . 2012;125(22):3985–3990. [PubMed] [Google Scholar]
  • 49.Dardmeh F., Alipour H., Gazerani P., van der Horst G., Brandsborg E., Nielsen H. I. Lactobacillus rhamnosus PB01 (DSM 14870) supplementation affects markers of sperm kinematic parameters in a diet-induced obesity mice model. PLoS One . 2017;12(10) doi: 10.1371/journal.pone.0185964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Arroyo A., Kim B., Yeh J. Luteinizing hormone action in human oocyte maturation and quality: signaling pathways, regulation, and clinical impact. Reproductive Sciences . 2020;27(6):1223–1252. doi: 10.1007/s43032-019-00137-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Rojas Canadas E., Herlihy M., Kenneally J., et al. Associations between postpartum phenotypes, cow factors, genetic traits, and reproductive performance in seasonal-calving, pasture-based lactating dairy cows. Journal of Dairy Science . 2020;103(1):1016–1030. doi: 10.3168/jds.2018-16001. [DOI] [PubMed] [Google Scholar]
  • 52.Córdova A. I., Guerra Liera J. E., Villa Mancera E. A., et al. Reproductive disorders and low fertility in cows. International Journal of Recent Scientific Research . 2017;08(05):16900–16902. doi: 10.24327/ijrsr.2017.0805.0241. [DOI] [Google Scholar]
  • 53.LeBlanc S. J. Interactions of metabolism, inflammation, and reproductive tract health in the postpartum period in dairy cattle. Reproduction in Domestic Animals . 2012;47:18–30. doi: 10.1111/j.1439-0531.2012.02109.x. [DOI] [PubMed] [Google Scholar]
  • 54.Pothmann H., Flick P., Tichy A., Gabler C., Drillich M. Messenger RNA expression of selected factors at different sites of the bovine endometrium associated with uterine health. Frontiers in Veterinary Science . 2021;8 doi: 10.3389/fvets.2021.649758.649758 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Peter S., Gärtner M. A., Michel G., et al. Infuence of intrauterine administration of Lactobacillus buchneri on reproductive performance and pro-infammatory endometrial mRNA expression of cows with subclinical endometritis. Scientific Reports . 2018;8(1):p. 5473. doi: 10.1038/s41598-018-22856-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Liu Y., Mei J., Gonzales L., et al. IL-17A and TNF-α exert synergistic effects on expression of CXCL5 by alveolar type II cells in vivo and in vitro. The Journal of Immunology . 2011;186(5):3197–3205. doi: 10.4049/jimmunol.1002016. [DOI] [PubMed] [Google Scholar]
  • 57.Sokol C. L., Luster A. D. The chemokine system in innate immunity. Cold Spring Harbor Perspectives in Biology . 2015;7(5) doi: 10.1101/cshperspect.a016303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Gartner M. A., Bondzio A., Braun N., Jung M., Einspanier R., Gabler C. Detection and characterisation of Lactobacillus sp.p. in the bovine uterus and their influence on bovine endometrial epithelial cells in vitro. PLoS One . 2015;10(3) doi: 10.1371/journal.pone.0119793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.da Luz C. M., da Broi M. G., Donabela F. C., Paro de Paz C. C., Meola J., Navarro P. A. PTGS2 down-regulation in cumulus cells of infertile women with endometriosis. Reproductive BioMedicine Online . 2017;35(4):379–386. doi: 10.1016/j.rbmo.2017.06.021. [DOI] [PubMed] [Google Scholar]
  • 60.Dim C. E., Ekere S. O., Ugwuoke J. I., Ndofor-Foleng H. M., Onyimonyi A. E. Bio-appraisal of three strains of Lactobacillus based probiotics on the growth traits and semen characteristics of local toms. African Journal of Biotechnology . 2020;19(5):276–281. doi: 10.5897/ajb2020.17101. [DOI] [Google Scholar]
  • 61.Hasan K. N., Banerjee G. Recent studies on probiotics as beneficial mediator in aquaculture: a review. The Journal of Basic and Applied Zoology . 2020;81(1):p. 53. doi: 10.1186/s41936-020-00190-y. [DOI] [Google Scholar]
  • 62.Carnevali O., Avella M., Gioacchini G. Effects of probiotic administration on zebrafish development and reproduction. General and Comparative Endocrinology . 2013;188:297–302. doi: 10.1016/j.ygcen.2013.02.022. [DOI] [PubMed] [Google Scholar]
  • 63.Gioacchini G., Valle L. D., Benato F., et al. Interplay between autopha gy and apoptosis in the development of Danio rerio follicles and the effects of a probiotic. Reproduction, Fertility and Development . 2013;25(8):1115–1125. doi: 10.1071/rd12187. [DOI] [PubMed] [Google Scholar]
  • 64.Kim S. O., Harris S. M., Duffy D. M. Prostaglandin E2 (EP) receptors mediate PGE2-specific events in ovulation and luteinization within primate ovarian follicles. Endocrinology . 2014;155(4):1466–1475. doi: 10.1210/en.2013-2096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Martin I., Membrive C. M. B., Vettorato L. F., Binelli M., Oba E., Ferreira J. C. P. Plasma PGFM and progesterone concentrations, luteolysis moment and estrous cycle length in Nelore cows submitted to uterine biopsies. Arquivo Brasileiro de Medicina Veterinária e Zootecnia . 2015;67(5):1210–1216. doi: 10.1590/1678-4162-8221. [DOI] [Google Scholar]
  • 66.Ambrose D. J., Gobikrushanth M., Zuidhof S., Kastelic J. P. Low-dose natural prostaglandin F2α (dinoprost) at timed insemination improves conception rate in dairy cattle. Theriogenology . 2015;83(4):529–534. doi: 10.1016/j.theriogenology.2014.10.034. [DOI] [PubMed] [Google Scholar]
  • 67.Deng Q., Odhiambo J. F., Farooq U., Lam T., Dunn S. M., Ametaj B. N. Intravaginal lactic acid bacteria modulated local and systemic immune responses and lowered the incidence of uterine infections in periparturient dairy cows. PLoS One . 2015;10(4) doi: 10.1371/journal.pone.0124167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 68.Corthésy B. Multi-faceted functions of secretory IgA at mucosal surfaces. Frontiers in Immunology . 2013;4:p. 185. doi: 10.3389/fimmu.2013.00185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 69.Giuliodori M. J., Magnasco R. P., Becu-Villalobos D., Lacau-Mengido I. M., Risco C. A., de la Sota R. L. Metritis in dairy cows: risk factors and reproductive performance. Journal of Dairy Science . 2013;96(6):3621–3631. doi: 10.3168/jds.2012-5922. [DOI] [PubMed] [Google Scholar]
  • 70.Genís S., Bach À., Fàbregas F., Arís A. Potential of lactic acid bacteria at regulating Escherichia coli infection and inflammation of bovine endometrium. Theriogenology . 2016;85(4):625–637. doi: 10.1016/j.theriogenology.2015.09.054. [DOI] [PubMed] [Google Scholar]
  • 71.Genis S., Sánchez-Chardi A., Bach À., Fàbregas F., Arís A. A combination of lactic acid bacteria regulates Escherichia coli infection and inflammation of the bovine endometrium. Journal of Dairy Science . 2017a;100(1):479–492. doi: 10.3168/jds.2016-11671. [DOI] [PubMed] [Google Scholar]
  • 72.Tafuri S., Ciani F., Iorio E. L., Esposito L., Cocchia N. New discoveries in embryology . Vol. 2. London, UK: InTech; 2015. Reactive oxygen species (ROS) and male fertility; pp. 19–40. [Google Scholar]
  • 73.Saraswat S., Kharche S. D., Jindal S. K. Impact of reactive oxygen species on spermatozoa: a balancing act between beneficial and detrimental effects. Iranian Journal of Applied Animal Science . 2014;4(2):247–255. [Google Scholar]
  • 74.Chen X. L., Gong L. Z., Xu J. X. Antioxidative activity and protective effect of probiotics against high-fat diet-induced sperm damage in rats. Animal . 2013;7(2):287–292. doi: 10.1017/s1751731112001528. [DOI] [PubMed] [Google Scholar]
  • 75.Genís S., Bach A., Aris A. Effects of intravaginal lactic acid bacteria on bovine endometrium: implications in uterine health. Veterinary Microbiology . 2017b;204:174–179. doi: 10.1016/j.vetmic.2017.04.025. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

Information about lactic acid bacteria for animal reproduction function were retrieved from a literature search of electronic databases such as the PubMed, Elsevier, Research Gate, Academia, and Google Scholar. The keywords used to perform the search were lactic acid bacteria, animal reproduction, fertility, and infertility. The research data are presented in the table in the article. Supportive data for discussion and comparison were taken from previous studies, which have been cited from recent journals related to the focus of this article. These data are publicly available and accessible online. Detailed sources are provided in References of the manuscript.

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