Skip to main content
Log in

Newly Isolated Lactobacilli strains from Algerian Human Vaginal Microbiota: Lactobacillus fermentum Strains Relevant Probiotic’s Candidates

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

Lactobacilli strains are considered as a preventive means for treatment of vaginal infections or post-antibiotic treatment to repopulate the vaginal mucosa. This study aimed at establishing the vaginal lactobacillus profile of Algerian women with different vaginal diseases. Afterwards, lactobacilli isolated from swabs were in vitro characterized for their probiotic hallmarks. This prospective study allowed isolation of 44 Lactobacillus strains and 160 potentially pathogens, among which are Escherichia coli (50 isolates), Staphylococcus sp. (38 isolates), Enterococcus sp. (16 isolates), and Candida sp. (56 isolates). All Lactobacilli strains were characterized for their antagonism, adhesion to polystyrene, and resistance to acidity and bile. Consequently, six Lactobacillus strains (Lb. fermentum 5LB4, 5LB10, 5LB12, Lb. plantarum 5LB2, 5LB11, and Lactobacillus sp. 4LB9) were moderately or weakly adherent, and 35 potentially pathogens exhibited weak to strong adhesion to polystyrene. Antagonism was recorded for 36 Lactobacillus strains towards E. coli 6E2, S. aureus 7S3, Enterococcus sp. 5EN8, and Candida albicans C1 used as indicator organisms. Finally, Lb. fermentum 9LB6, 4LB16, and 10LB1 and Lb. plantarum 9LB4 were remarkable for their inhibitory activity, absence of hemolytic potential, and for their resistance to acidity (pH 1.5) and bile (0.5%) harsh conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Petricevic L, Domig K, Nierscher F, Sandhofer M, Fidesser M, Kro-ndorfer I, Husslein P, Kneifel W, Kiss H (2014) Characterisation of the vaginal Lactobacillus microbiota associated with preterm delivery. Sci Rep 4(1):5136. https://doi.org/10.1038/srep05136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Al Kassaa I, Hamze M, Hober D, Chihib NE, Drider D (2014) Identification of vaginal lactobacilli with potential probiotic properties isolated from women in North Lebanon. Microb Ecol 67(3):722–734. https://doi.org/10.1007/s00248-014-0384-7

    Article  Google Scholar 

  3. Kamińska D, Gajecka M (2017) Is the role of human female reproductive tract microbiota underestimated? Benefic Microbes 8(3):327–343. https://doi.org/10.3920/BM2015.0174

    Article  Google Scholar 

  4. Witkin SS, Linhares IM (2017) Why do lactobacilli dominate the human vaginal microbiota? BJOG 124(4):606–611. https://doi.org/10.1111/1471-0528.14390

    Article  CAS  PubMed  Google Scholar 

  5. Zhou X, Brown CJ, Abdo Z, Davis CC, Hansmann MA, Joyce P, Foster JA, Forney LJ (2007) Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J 1(2):121–133. https://doi.org/10.1038/ismej.2007.12

    Article  CAS  PubMed  Google Scholar 

  6. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ (2011) Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 108(Supplement_1):4680–4687. https://doi.org/10.1073/pnas.1002611107

    Article  PubMed  Google Scholar 

  7. Lepargneur JP (2016) Lactobacillus crispatus as biomarker of the healthy vaginal tract. Ann Biol Clin 74:421–427

    Google Scholar 

  8. Petrova MI, Reid G, Vaneechoutte M, Lebeer S (2017) Lactobacillus iners: friend or foe? Trends Microbiol 25(3):182–191. https://doi.org/10.1016/j.tim.2016.11.007

    Article  CAS  PubMed  Google Scholar 

  9. Le Blanc R-M (2009) Détecter des infections génitales basses chez la femme. Option Biologie 424:19–20

    Google Scholar 

  10. Miller EA, Beasley DE, Dunn RR, Archie EA (2016) Lactobacilli dominance and vaginal pH: why is the human vaginal microbiome unique? Front Microbiol 7:1936. https://doi.org/10.3389/fmicb.2016.01936

    Article  PubMed  PubMed Central  Google Scholar 

  11. Tachedjian G, Aldunate M, Bradshaw CS, Cone RA (2017) The role of lactic acid production by probiotic Lactobacillus species in vaginal health. Res Microbiol. https://doi.org/10.1016/j.resmic.2017.04.001

  12. FAO/WHO (2006) Probiotics in food. Health and nutritional properties and guidelines for evaluation. FAO Food and Nutritional paper No. 85

  13. Newman D (1915) The treatment of cystitis by intravesical injections of lactic bacillus cultures. Lancet 186(4798):330–332. https://doi.org/10.1016/S0140-6736(01)53633-8

    Article  Google Scholar 

  14. van de Wijgert JH, Borgdorff H, Verhelst R, Crucitti T, Francis S, Verstraelen H, Jespers V (2014) The vaginal microbiota: what have we learned after a decade of molecular characterization? PLoS One 9(8):e105998. https://doi.org/10.1371/journal.pone.0105998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Onderdonk AB, Delaney ML, Fichorova N (2016) The human microbiome during bacterial vaginosis. Clin Microbiol Rev 29(2):223–238. https://doi.org/10.1128/CMR.00075-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Daliri EBM, Lee BH (2015) New perspectives on probiotics in health and disease. Food Sci Human Wellness 4(2):56–65. https://doi.org/10.1016/j.fshw.2015.06.002

    Article  Google Scholar 

  17. Donders GG, Zodzika J, Rezeberga D (2014) Treatment of bacterial vaginosis: what we have and what we miss. Expert Opin Pharmacother 15(5):645–657. https://doi.org/10.1517/14656566.2014.881800

    Article  CAS  PubMed  Google Scholar 

  18. Petrina MAB, Cosentino LA, Rabe LK, Hillier SL (2017) Susceptibility of bacterial vaginosis (BV)-associated bacteria to secnidazole compared to metronidazole, tinidazole and clindamycin. Anaerobe 47:115–119. https://doi.org/10.1016/j.anaerobe.2017.05.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Vasquez A, Ahrne S, Jeppsson B, Molin G (2005) Oral administration of Lactobacillus and Bifidobacterium strains of intestinal and vaginal origin to healthy human females: re-isolation from faeces and vagina. Microb Ecol Health Dis 17(1):15–20. https://doi.org/10.1080/08910600510031376

    Article  Google Scholar 

  20. Guiraud JP (2003) Microbiologie alimentaire. Dunod, Paris

    Google Scholar 

  21. Kos B, Šušković J, Vuković S, Šimpraga M, Frece J, Matošić S (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol 94(6):981–987. https://doi.org/10.1046/j.1365-2672.2003.01915.x

    Article  CAS  Google Scholar 

  22. Rosenberg M, Gutnick D, Rosenberg E (1980) Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9(1):29–33. https://doi.org/10.1111/j.1574-6968.1980.tb05599.x

    Article  CAS  Google Scholar 

  23. O’Toole G, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30(2):295–304. https://doi.org/10.1046/j.1365-2958.1998.01062.x

    Article  PubMed  Google Scholar 

  24. Ait Ouali F, Al Kassaa I, Cudennec B, Abdallah M, Bendali F, Sadoun D, Chihib NE, Drider D (2014) Identification of lactobacilli with inhibitory effect on biofilm formation by pathogenic bacteria on stainless steel surfaces. Int J Food Microbiol 191:116–124. https://doi.org/10.1016/j.ijfoodmicro.2014.09.011

    Article  CAS  PubMed  Google Scholar 

  25. Comité de l’Antibiogramme de la Société Française de Microbiologie (CFA-SFM). Recommandations 2015. Paris, France. Société Française de Microbiologie

  26. Bendali F, Durand A, Hébraud M, Sadoun D (2011) Lactobacillus paracasei subsp. paracasei: an Algerian isolate with antibacterial activity against enteric pathogens and probiotic fitness. J Food Nutr Res 50:139–149

    Google Scholar 

  27. Stepanovic S, Vukovic D, Dakic I, Savic B, Svabic-Vlahovic M (2000) A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 40(2):175–179. https://doi.org/10.1016/S0167-7012(00)00122-6

    Article  CAS  Google Scholar 

  28. Nunn KL, Forney LJ (2016) Unraveling the dynamics of the human vaginal microbiome. Yale J Biol Med 89(3):331–337

    PubMed  PubMed Central  Google Scholar 

  29. Kaewnopparat S, Dangmanee N, Kaewnopparat N, Srichana T, Chulasiri M, Settharaksa S (2013) In vitro probiotic properties of Lactobacillus fermentum SK5 isolated from vagina of a healthy woman. Anaerobe 22:6–13. https://doi.org/10.1016/j.anaerobe.2013.04.009

    Article  CAS  PubMed  Google Scholar 

  30. Sabia C, Anacarso I, Bergonzini A, Gargiulo R, Sarti M, Condò C, Messi P, de Niederhausern S, Iseppi R, Bondi M (2014) Detection and partial characterization of a bacteriocin-like substance produced by Lactobacillus fermentum CS57 isolated from human vaginal secretions. Anaerobe 26:41–45. https://doi.org/10.1016/j.anaerobe.2014.01.004

    Article  CAS  PubMed  Google Scholar 

  31. Baldwin EA, Walther-Antonio M, MacLean AM, Gohl DM, Beckman KB, Chen J, White B, Creedon DJ, Chia N (2015) Persistent microbial dysbiosis in preterm premature rupture of membranes from onset until delivery. Peer J 3:e1398. https://doi.org/10.7717/peerj.1398

    Article  CAS  PubMed  Google Scholar 

  32. Park TC, Lee HJ (2013) Pregnancy coexisting with uterus didelphys with a blind hemivagina complicated by pyocolpos due to Pediococcus infection: a case report and review of the published reports. J Obstet Gynaecol Res 39(7):1276–1279. https://doi.org/10.1111/jog.12049

    Article  PubMed  Google Scholar 

  33. Borges S, Barbosa J, Silva J, Teixeira P (2013) Evaluation of characteristics of Pediococcus spp. to be used as a vaginal probiotics. J Appl Microbiol 115(2):527–538. https://doi.org/10.1111/jam.12232

    Article  CAS  PubMed  Google Scholar 

  34. Borges S, Costa P, Silva J, Teixeira P (2013) Effects of processing and storage on Pediococcus pentosaceus SB83 in vaginal formulations: lyophilized powder and tablets. Biomed Res Int 680767

  35. Borges S, Teixeira P (2014) Pediococcus pentosaceus SB83 as a potential probiotic incorporated in a liquid system for vaginal delivery. Benefic Microbes 5(4):421–426. https://doi.org/10.3920/BM2013.0084

    Article  CAS  Google Scholar 

  36. Vicariotto F, Mogna L, Del Piano M (2014) Effectiveness of the two microorganisms Lactobacillus fermentum LF15 and Lactobacillus plantarum LP01, formulated in slow-release vaginal tablets, in women affected by bacterial vaginosis: a pilot study. J Clin Gastroenterol 48:106–112

    Article  Google Scholar 

  37. Martin R, Soberon N, Vaneechoutte M, Florez A, Vazquez F, Suarez J (2008) Characterizaton of indigenous vaginal lactobacilli from healthy women as probiotic candidates. Int Microbiol 11(4):261–266. https://doi.org/10.2436/20.1501.01.70

    Article  CAS  PubMed  Google Scholar 

  38. Strus M, Kucharska A, Kukla G, Wloch M, Maresz K, Heczko P (2005) The in vitro activity of vaginal Lactobacillus with probiotic properties against Candida. Infect Dis Obstet Gynecol 13(2):69–75. https://doi.org/10.1080/10647440400028136

    Article  PubMed  PubMed Central  Google Scholar 

  39. Hardy L, Cerca N, Jespers V, Vaneechoutte M, Crucitti T (2017) Bacterial biofilms in the vagina. Res Microbiol. https://doi.org/10.1016/j.resmic.2017.02.001

  40. Leccese Terraf MC, Juarez Tomás MS, Rault L, Le Loir Y, Even S, Nader-Macías ME (2017) In vitro effect of vaginal lactobacilli on the growth and adhesion abilities of uropathogenic Escherichia coli. Arch Microbiol 199(5):767–774. https://doi.org/10.1007/s00203-016-1336-z

    Article  CAS  PubMed  Google Scholar 

  41. Deidda F, Amoruso A, Nicola S, Graziano T, Pane M, Allesina S, Raiteri E, Del Piano M, Mogna L (2016) The in vitro effectiveness of Lactobacillus fermentum against different Candida species compared with broadly used azoles. J Clin Gastroenterol 50:S171–S174. https://doi.org/10.1097/MCG.0000000000000686

    Article  CAS  PubMed  Google Scholar 

  42. Gibbs RS (1987) Microbiology of the female genital tract. Am J Obstet Gynecol 156(2):491–495. https://doi.org/10.1016/0002-9378(87)90318-8

    Article  CAS  PubMed  Google Scholar 

  43. Akhi MT, Esmailkhani A, Sadeghi J, Niknafs B, Farzadi L, Akhi A, Nasab EN (2017) The frequency of Staphylococcus aureus isolated from endocervix of infertile women in northwest Iran. Int J Fertil Steril 11(1):28–32

    CAS  PubMed  Google Scholar 

  44. Rabia A, Chah N (2011) Antibiotic resistance of probiotics organisms and safety of probiotic dairy products. Int Food Res J 18:837–853

    Google Scholar 

  45. Delgado S, Flórez AB, Mayo B (2005) Antibiotic susceptibility of Lactobacillus and Bifidobacterium species from the human gastrointestinal tract. Curr Microbiol 50(4):202–207. https://doi.org/10.1007/s00284-004-4431-3

    Article  CAS  PubMed  Google Scholar 

  46. Lee YK (2014) What could probiotic do for us? Food Sci Human Wellness 3(2):47–50. https://doi.org/10.1016/j.fshw.2014.06.001

    Article  Google Scholar 

  47. Flourié B, Nancey S (2007) Propriétés fonctionnelles des probiotiques. Cahier de Nutrition Diététique 42:38–44. https://doi.org/10.1016/S0007-9960(07)91320-6

    Article  Google Scholar 

  48. Reid G, Bruce AW, Fraser N, Heinemann C, Owen J, Henning B (2001) Oral probiotics can resolve urogenital infections. FEMS Immunol Med Microbiol 30(1):49–52. https://doi.org/10.1111/j.1574-695X.2001.tb01549.x

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

Experiments performed at Charles Violette Institute (Lille University) were funded by CPER/FEDER Alibiotech program (2016-2020). Those performed in Algeria were funded by the Algerian Ministry of High Education and Scientific Research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Farida Bendali.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ouarabi, L., Chait, Y.A., Seddik, H.A. et al. Newly Isolated Lactobacilli strains from Algerian Human Vaginal Microbiota: Lactobacillus fermentum Strains Relevant Probiotic’s Candidates. Probiotics & Antimicro. Prot. 11, 43–54 (2019). https://doi.org/10.1007/s12602-017-9360-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-017-9360-0

Keywords

Navigation