Potential Use of Lactobacillus gasseri G10 Isolated from Human Vagina along with Intrauterine Devices (IUD) to Prevent Pathogen Colonization

Yıl 2022, , 776 - 788, 31.08.2022

Busra Aktas

https://doi.org/10.16984/saufenbilder.1095584

Öz

Intrauterine devices (IUDs), well effective long-term contraception methods used around the world, are potential reservoir for pathogens and carry risk of reproductive-tract infections such as bacterial vaginosis and vulvovaginal candidiasis. A healthy vagina is dominated by Lactobacillus involved in protecting reproductive system against pathogens. This study aims to investigate the impact of L. gasseri G10 (G10), a vaginal isolate, and its Exopolysaccharide (EPS) on adherence of Staphylococcus aureus and Candida albicans to IUD-tail. Three conditions were simulated to examine if G10 with/without EPS is capable of displacing, excluding, and competing pathogen adhesion to IUD. Inhibitory impact of EPS at various concentrations on pathogen adherence was also evaluated with co-incubation. G10 blocked by co-incubation (97%) and displacement (46%) of S. aureus adherence to IUD tail and displaced C. albicans attached to IUD with about 99%. Compared with S. aureus, the biofilm formation by C. albicans was highly susceptible to EPS. All concentrations of EPS inhibited the adherence of C. albicans (81-97%); however, no significant reductions were observed in S. aureus adherence. Moreover, G10 and EPS together reduced the adherence of both S. aureus (>99%) and C. albicans (94-98%) through all three mechanisms. This study indicates that G10 and its EPS have the ability to inhibit adhesion of S. aureus and C. albicans to IUD and potential use in intravaginal products to prevent/manage IUD associated infections in women. The results suggest development of a new way of applying IUD along with probiotic agents alone or as synbiont.

Anahtar Kelimeler

Lactobacillus gasseri, intrauterine devices (IUD), Staphylococcus aureus, Candida albicans, vaginal probiotics

Kaynakça

• [1] A. Sundaram, B. Vaughan, K. Kost, A. Bankole, L. Finer, S. Singh, J. Trussell, “Contraceptive Failure in the United States: Estimates from the 2006-2010 National Survey of Family Growth” Perspectives on sexual and reproductive health, vol. 49, no. 1, pp. 7–16, 2017.
• [2] M. L. Kavanaugh, J. Jerman, “Contraceptive method use in the United States: trends and characteristics between 2008, 2012 and 2014” Contraception, vol. 97, no. 1, pp. 14–21, 2018.
• [3] K. J. Buhling, N. B. Zite, P. Lotke, and K. Black, “Worldwide use of intrauterine contraception: A review” Contraception, vol. 89, no. 3, pp. 162–173, 2014.
• [4] A. N. Aksoy, G. T. Sarikas, E. G. Gozgec, “The effect of copper intrauterine device use duration on uterine and ovarian blood flow parameters: A prospective cross-sectional study” Journal of Clinical Ultrasound, vol. 49, no. 2, pp. 124–128, 2021.
• [5] K. Peebles, F. M. Kiweewa, T. Palanee-Phillips, C. Chappell, D. Singh, K. E. Bunge, L. Naidoo, B. Makanani, N. Jeenarain, D. Reynolds, S. L. Hillier, E. R. Brown, J. M. Baeten, J. E. Balkus, “Elevated Risk of Bacterial Vaginosis Among Users of the Copper Intrauterine Device: A Prospective Longitudinal Cohort Study” C linical Infectious Diseases, vol. 73, no. 3, pp. 513–520, 2021.
• [6] S. Caddy, M. H.Yudin, J. Hakim, D. M. Money, “Best Practices to Minimize Risk of Infection With Intrauterine Device Insertion” Journal of Obstetrics and Gynaecology Canada, vol. 36, no. 3, pp. 258–265, 2014.
• [7] A. D. Saidu, K. A. Tunau, A. A. Panti, E. I. Nwobodo, Y. Mohammed, J. Amin, J. Garba, “Effect of hormonal and copper IUDs on genital microbial colonisation and clinical outcomes in North-Western Nigeria” International Journal of Reproduction, Contraception, Obstetrics and Gynecology, vol. 6, no. 6, pp. 2143–2147, 2017.
• [8] S. Abd, A.-K. Al-Kattan, D. T. Burhan, S. T. Burhan, “Biofilm Formation on Intrauterine Device and Associated Infections” Iraqi Postgraduate Medical Journal, vol. 12, no. 4, pp. 562–567, 2013.
• [9] S. L. Achilles, M. N. Austin, L. A. Meyn, F. Mhlanga, Z. M. Chirenje, S. L. Hillier, “Impact of contraceptive initiation on vaginal microbiota” American Journal of Obstetrics & Gynecology, vol. 218, no. 6, pp. 622.e1-622.e10, 2018.
• [10] The NIH HMP Working Group, “The NIH Human Microbiome Project” Genome Research, vol. 19, pp. 2317–2323, 2009.
• [11] T. Sungur, B. Aslim, C. Karaaslan, B. Aktas, “Impact of Exopolysaccharides (EPSs) of Lactobacillus gasseri strains isolated from human vagina on cervical tumor cells (HeLa)” Anaerobe, vol. 47, pp. 137–144, 2017.
• [12] J. Eleuterio, P. C. Giraldo, A. K. Silveira Gonçalves, R. M. Nunes Eleuterio, “Liquid-based cervical cytology and microbiological analyses in women using cooper intrauterine device and levonorgestrel-releasing intrauterine system” European Journal of Obstetrics & Gynecology and Reproductive Biology, vol. 255, pp. 20–24, 2020.
• [13] T. Madden, J. M. Grentzer, G. M. Secura, J. E. Allsworth, and J. F. Peipert, “Risk of Bacterial Vaginosis in Users of the Intrauterine Device: A Longitudinal Study” Sexually Transmitted Diseases, vol. 39, no. 3, pp. 217–222, 2012.
• [14] J. Ravel, I. Moreno, C. Simón, “Bacterial vaginosis and its association with infertility, endometritis, and pelvic inflammatory disease” American Journal of Obstetrics & Gynecology, vol. 224, no. 3, pp. 251–257, 2021.
• [15] A. E.-S. Abdou, E. A. E. A. Mohamad, A. M. Tawfiek, “Bacterial Infections and Biofilm Formation Associated with Intra Uterine Contraceptive Device among Females Attending Al-Glaa Teaching Hospital in Cairo” Egyptian Journal of Hospital Medicine, vol. 70, no. 5, pp. 882–890, 2018.
• [16] A. A. Elsharkawy, R. S. Abdel-latif, M. A. Kamel, “Biofilm Forming Bacteria Isolated from Intrauterine Devices and Their Susceptibility to Antibiotics” Egyptian Journal of Medical Microbiology, vol. 26, no. 3, pp. 145–152, 2017.
• [17] V. Pruthi, A. Al-Janabi, B. M. J. Pereira, “Characterization of biofilm formed on intrauterine devices” Indian Journal of Medical Microbiology, vol. 21, no. 3, pp. 161–165, 2003.
• [18] Z. Pa´l, E. Urba´n, E. Do´sa, A. Pa´l, E. Nagy, “Biofilm formation on intrauterine devices in relation to duration of use” Journal of Medical Microbiology, vol. 54, pp. 1199–1203, 2005.
• [19] E. E. Cho D. Fernando, “Fatal streptococcal toxic shock syndrome from an intrauterine device” Journal of Emergency Medicine, vol. 44, pp. 777–780, 2013.
• [20] M. Gottlieb, B. Long, A. Koyfman, “The Evaluation and Management of Toxic Shock Syndrome in the Emergency Department: A Review of the Literature” Journal of Emergency Medicine, vol. 54, no. 6, pp. 807–814, 2018.
• [21] C. D. Klug, C. R. Keay, and A. A. Ginde, “Fatal Toxic Shock Syndrome From an Intrauterine Device” Annals of Emergency Medicine, vol. 54, no. 5, pp. 701–703, 2009.
• [22] E. A. Omran, N. E. S. Youssef, A. H. Abdelfattah, S. A. Esmail, and A. M. Fouad, “Copper IUD increases virulence of non-albicans Candida species isolated from women with vulvovaginal candidiasis” European Journal of Contraception & Reproductive Health Care, vol. 25, no. 2, pp. 120–125, 2020.
• [23] J. de Cássia Orlandi Sardi, D. R. Silva, P. C. Anibal, J. J. C. M. de Campos Baldin, S. R. Ramalho, P. L. Rosalen, M. L. R. Macedo, J. F. Hofling, “Vulvovaginal Candidiasis: Epidemiology and Risk Factors, Pathogenesis, Resistance, and New Therapeutic Options” Current Fungal Infection Reports, vol. 15, no. 1, pp. 32–40, 2021.
• [24] B. Gonçalves, C. Ferreira, C. T. Alves, M. Henriques, J. Azeredo, and S. Silva, “Vulvovaginal candidiasis: Epidemiology, microbiology and risk factors” Critical Reviews in Microbiology, vol. 42, no. 6, pp. 905–927, 2016.
• [25] G. Donders, G. Bellen, E. Oerlemans, I. Claes, K. Ruban, T. Henkens, F. Kiekens, S. Lebeer “The use of 3 selected lactobacillary strains in vaginal probiotic gel for the treatment of acute Candida vaginitis: a proof-of-concept study” European Journal of Clinical Microbiology & Infectious Diseases, vol. 39, no. 8, pp. 1551–1558, 2020.
• [26] K. M. Zahran, M. N. Agban, S. H. Ahmed, E. A. Hassan, and M. A. Sabet, “Patterns of candida biofilm on intrauterine devices” Journal of Medical Microbiology, vol. 64, no. 4, pp. 375–381, 2015.
• [27] M. E. Auler, D. Morreira, F. F. O. Rodrigues, M. S. Abr Ão, P. F. R. Margarido, F. E. Matsumoto, E. G. Silva, B. C. M. Silva, R. P. Schneider, C. R. Paula “Biofilm formation on intrauterine devices in patients with recurrent vulvovaginal candidiasis Biofilm formation on IUDs in patients with vulvovaginal candidiasis” Medical Mycology, vol. 48, no. 1, pp. 211–216, 2010.
• [28] P. Lal, V. Agarwal, P. Pruthi, B. M. J. Pereira, M. R. K. Vikas, “Biofilm formation by Candida albicans isolated from intrauterine devices” Indian journal of microbiology, vol. 48, no. 4 , pp. 438–444, 2008.
• [29] F. Chassot, M. F. N. Negri, A. E. Svidzinski, L. Donatti, R. M. Peralta, T. I. E. Svidzinski, M. E. L.Consolaro “Can intrauterine contraceptive devices be a Candida albicans reservoir?” Contraception, vol. 77, no. 5, pp. 355–359, 2008.
• [30] B. Pippi, G. da R. M. Machado, V. Z. Bergamo, R. J. Alves, S. F. Andrade, and A. M. Fuentefria, “Clioquinol is a promising preventive morphological switching compound in the treatment of Candida infections linked to the use of intrauterine devices” Journal of Medical Microbiology, vol. 67, no. 11, pp. 1655–1663, 2018.
• [31] T. A. Georgescu, A.-C. Lisievici, O. Munteanu, F. L. Furtunescu, O. G. Bratu, C. Berceanu, R. E. Bohîlţea “Congenital systemic candidiasis: A comprehensive literature review and meta-analysis of 44 cases” Romanian Journal of Morphology and Embryology, vol. 61, no. 3, pp. 673–680, 2020.
• [32] L. C. F. Paiva, L. Donatti, E. V. Patussi, T. I. E. Svizdinski, M. E. Lopes-Consolaro, “Scanning electron and confocal scanning laser microscopy imaging of the ultrastructure and viability of vaginal Candida albicans and non-albicans species adhered to an intrauterine contraceptive device” Microscopy and Microanalysis, vol. 16, no. 5, pp. 537–549, 2010.
• [33] M. I. Petrova, “Lactobacillus species as biomarkers and agents that can promote various aspects of vaginal health” Frontiers in Physiology, vol. 6, p. 81, 2015.
• [34] L. Stoeker, S. Nordone, S. Gunderson, L. Zhang, A. Kajikawa, A. LaVoy, M. Miller, T. R. Klaenhammer, G. A. Dean “Assessment of Lactobacillus gasseri as a candidate oral vaccine vector” Clinical and Vaccine Immunology, vol. 18, no. 11, pp. 1834–1844, Sep. 2011.
• [35] E. Motevaseli, M. Shirzad, S. M. Akrami, A. S. Mousavi, A. Mirsalehian, M. H. Modarressi, “Normal and Tumour cervical cells respond differently to vaginal lactobacilli, independent of pH and lactate” Journal of Medical Microbiology, vol. 62, pp. 1065–1072, 2013.
• [36] P.-G. Larsson, B. Stray-Pedersen, K. R. Ryttig, S. Larsen, “Human lactobacilli as supplementation of clindamycin to patients with bacterial vaginosis reduce the recurrence rate; a 6-month, double-blind, randomized, placebo-controlled study” BMC Womens. Health, vol. 8, p. 3, 2008.
• [37] C. Parolin, A. Marangoni, L. Laghi, C. Foschi, R. A. Ñ. Palomino, N. Calonghi, R. Cevenini, B. Vitali “Isolation of Vaginal Lactobacilli and Characterization of Anti-Candida Activity” PLoS One, vol. 10, no. 6, p. e0131220, 2015.
• [38] G. Zárate M. E. Nader-Macias, “Influence of probiotic vaginal lactobacilli on in vitro adhesion of urogenital pathogens to vaginal epithelial cells” Letters in Applied Microbiology, vol. 43, no. 2, pp. 174–180, 2006.
• [39] B. S. Gan, J. Kim, G. Reid, P. Cadieux, J. C. Howard, “Lactobacillus fermentum RC‐14 Inhibits Staphylococcus aureus Infection of Surgical Implants in Rats” Journal of Infectious Diseases, vol. 185, no. 9, pp. 1369–1372, 2002.
• [40] H. Ekmekci, B. Aslim, D. O. Darilmaz, “Some factors affecting the autoaggregation ability of vaginal lactobacilli isolated from Turkish women” Archives of Biological Sciences, vol. 61, no. 3, pp. 407–412, 2009.
• [41] H. Ekmekçi, B. Aslim, and D. Önal Darilmaz, “Factors affecting the coaggregation ability of vaginal lactobacilli with Candida spp” Annals of Microbiology, vol. 59, no. 1, pp. 163–167, 2009.
• [42] G. I. Frengova, E. D. Simova, D. M. Beshkova, Z. I. Simov, “Production and monomer composition of exopolysaccharides by yogurt starter cultures” Canadian Journal of Microbiology, vol. 46, no. 12, pp. 1123–1127, 2000.
• [43] G. Tsanadis, S. N. Kalantaridou, A. Kaponis, E. Paraskevaidis, K. Zikopoulos, E. Gesouli, N. Dalkalitsis, I. Korkontzelos, E. Mouzakioti, D. E. Lolis “Bacteriological cultures of removed intrauterine devices and pelvic inflammatory disease” Contraception, vol. 65, pp. 339–342, 2002.
• [44] K. K. Foarde, D. W. Vanosdell, R. S. Steiber, “Investigation of gas-phase ozone as a potential biocide” Applied Occupational and Environmental Hygiene, vol. 12, no. 8, p. 535, 1997.
• [45] Y. Kim, S. Oh, S. H. Kim, “Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagic Escherichia coli O157:H7” Biochemical and Biophysical Research Communications, vol. 379, no. 2, pp. 324–329, 2009.
• [46] S. Bikric, B. Aslim, İ. Dincer, Z. Yuksekdag, S. Ulusoy, S. Yavuz, “Characterization of Exopolysaccharides (EPSs) Obtained from Ligilactobacillus salivarius Strains and Investigation at the Prebiotic Potential as an Alternative to Plant Prebiotics at Poultry” Probiotics and Antimicrobial Proteins, vol. 14, no. 1, pp. 49–59, 2022.
• [47] M. Aldunate, D. Srbinovski, A. C. Hearps, C. F. Latham, P. A. Ramsland, R. Gugasyan, R.A. Cone, G. Tachedjian “Antimicrobial and immune modulatory effects of lactic acid and short chain fatty acids produced by vaginal microbiota associated with eubiosis and bacterial vaginosis” Frontiers in Physiology, vol. 6, p. 164, 2015.
• [48] S. Borges, J. Silva, P. Teixeira, “The role of lactobacilli and probiotics in maintaining vaginal health” Archives of Gynecology and Obstetrics, vol. 289, pp. 479–489, 2014.
• [49] X. Zhou, T. Li, S. Fan, Y. Zhu, X. Liu, X. Guo, Y. Liang “The efficacy and safety of clotrimazole vaginal tablet vs. oral fluconazole in treating severe vulvovaginal candidiasis” Mycoses, vol. 59, no. 7, pp. 419–428, 2016.
• [50] M. Chiaruzzi, A. Barbry, A. Muggeo, A. Tristan, Is. Jacquemond, C. Badiou, L. Cluzeau, S. Bourdeau, T. Durand, A. Engelmann, D. Bosquet, M. Bes, C. Prigent-Combaret, J. Thioulouse, D. Muller, G. Lina “Vaginal Tampon Colonization by Staphylococcus aureus in Healthy Women Myriam” Applied and Environmental Microbiology, vol. 86, no. 18, pp. 1–9, 2020.
• [51] P. Mastromarino, P. Brigidi, S. Macchia, L. Maggi, F. Pirovano, V. Trinchieri, U “Characterization and selection of vaginal Lactobacillus strains for the preparation of vaginal tablets” Journal of Applied Microbiology, vol. 93, no. 5, pp. 884–893, 2002.
• [52] C. Ceresa, F. Tessarolo, I. Caola, G. Nollo, M. Cavallo, M. Rinaldi, L. Fracchia “Inhibition of Candida albicans adhesion on medical-grade silicone by a Lactobacillus-derived biosurfactant” Journal of Applied Microbiology, vol. 118, no. 5, pp. 1116–1125, 2015.
• [53] G. Reid, L.-A. Hawthorn, R. Mandatorifl, R. L. Cook, H. S. Beg, “Adhesion of Lactobacilli to Polymer Surfaces In Vivo and In Vitro” Microbial Ecology, vol. 16, pp. 241–251, 1988.
• [54] G. Reid C. Tieszer, “Use of lactobacilli to reduce the adhesion of Staphylococcus aureus to catheters” International Biodeterioration & Biodegradation, vol. 34, no. 1, pp. 73–83, 1994.
• [55] M. Koohestani, M. Moradi, H. Tajik, A. Badali, “Effects of cell-free supernatant of Lactobacillus acidophilus LA5 and Lactobacillus casei 431 against planktonic form and biofilm of Staphylococcus aureus” Veterinary Research Forum, vol. 9, no. 4, pp. 301–306, 2018.
• [56] F. Ait Ouali, I. Al Kassaa, B. Cudennec, M. Abdallah, F. Bendali, D. Sadoun, N.-E. Chihib, D. Drider “Identification of lactobacilli with inhibitory effect on biofilm formation by pathogenic bacteria on stainless steel surfaces” International Journal of Food Microbiology, 191, pp. 116–124, 2014.
• [57] S. Shanmughapriya, H. Sornakumari, A. Lency, S. Kavitha, K. Natarajaseenivasan, “Synergistic effect of amphotericin B and tyrosol on biofilm formed by Candida krusei and Candida tropicalis from intrauterine device users” Med. Mycol., vol. 52, no. 8, pp. 853–861, 2014.
• [58] G. Donnarumma, A. Molinaro, D. Cimini, C. De Castro, V. Valli, V. De Gregorio, M. De Rosa, C. Schiraldi “Lactobacillus crispatus L1: high cell density cultivation and exopolysaccharide structure characterization to highlight potentially beneficial effects against vaginal pathogens” BMC Microbiology, vol. 14, no. 1, p. 137, 2014.
• [59] D. Ren, C. Li Y. Qin, R. Yin, S. Du, F. Ye, C. Liu, H. Liu, M. Wang, Y. Li, Y. Sun, X. Li, M. Tian, N. Jin “Invitro evaluation of the probiotic and functional potential of Lactobacillus strains isolated from fermented food and human intestine” Anaerobe, vol. 30, pp. 1–10, 2014.
• [60] J. Woo J. Ahn, “Probiotic-mediated competition, exclusion and displacement in biofilm formation by food-borne pathogens” Letters in Applied Microbiology, vol. 56, no. 4, pp. 307–313, 2013.