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An Investigation the Relationship of Vaginal Microbial Bacteria Species with Bacterial Vaginosis and High-Risk Human Papillomavirus

Year 2022, Volume: 8 Issue: 3, 218 - 224, 03.10.2022
https://doi.org/10.30934/kusbed.1132919

Abstract

Objective: This study was aim to investigate the relationship of vaginal bacterial species with High-Risk Human Papillomavirus (HR-HPV) and bacterial vaginosis (BV).
Methods: One hundred and twenty-one women were included in the study. Gram stain was performed for the diagnosis of BV and evaluated according to the Nugent score. HR-HPV diagnosis was made by real-time PCR . Detection of vaginal microbial species and Gardnerella vaginalis subtypes were also performed by real-time PCR.
Results: The prevalence of BV was found as 38.8%. The mean number of species was found significantly higher in BV-positive samples compared to BV-intermediate and BV-negative samples (p=0.001). Lactobacillus iners (p=0.036), BVAB2 (p=0.043), Provetella spp. (p=0.015), Leptotrichia/Sneathia (p=0.001), Megaspheara (p=0.048) were found to be associated with bacterial vaginosis. Gardnerella vaginalis subtypes were evaluated in 50 randomly selected samples. The most common strain that was found was “clade 4”. The prevalence of HR-HPV was 9.9%. HPV 16 was the most common HR-HPV type (58.3%). There was no significant difference between the mean value of Lactobacillus sp. HR-HPV-positive and negative samples (p=0.23). No association was found between the specified species and HR-HPV-positive samples (p=0.436).
Conclusion: Bacterial diversity was greater in BV-positive patients and BV was significantly associated with Lactobacillus iners, Megaspheara, BVAB2, Provetella spp. and Leptotrichia / Sneathia.

Supporting Institution

This research was supported by Pamukkale University Scientific Research Projects Unit (Project number: 2017TIPF005)

Project Number

(Project number: 2017TIPF005)

References

  • Ling Z, Kong J, Liu F, et al. Molecular analysis of the diversity of vaginal microbiota associated with bacterial vaginosis. BMC Genomics. 2010;11:488. doi:10.1186/1471-2164-11-488.
  • Zhou X, Hansmann MA, Davis CC, et al. The vaginal bacterial communities of Japanese women resemble those of women in other racial groups. FEMS Immunol Med Microbiol. 2010;58(2):169-181. doi:10.1111/j.1574-695X.2009.00618.x.
  • Gillet E, Meys JF, Verstraelen H, et al. Bacterial vaginosis is associated with uterine cervical human papillomavirus infection: a meta-analysis. BMC Infect Dis. 2011;11:10. doi:10.1186/1471-2334-11-10.
  • Ciccarese G, Herzum A, Pastorino A, et al. Prevalence of genital HPV infection in STI and healthy populations and risk factors for viral persistence. Eur J Clin Microbiol Infect Dis. 2021;40(4):885-888. doi:10.1007/s10096-020-04073-6.
  • Martin DH. The microbiota of the vagina and its influence on women's health and disease. Am J Med Sci. 2012;343(1):2-9. doi:10.1097/MAJ.0b013e31823ea228.
  • Fredricks DN, Fiedler TL, Thomas KK, Oakley BB, Marrazzo JM. Targeted PCR for detection of vaginal bacteria associated with bacterial vaginosis. J Clin Microbiol. 2007;45(10):3270-3276. doi:10.1128/JCM.01272-07.
  • Balashov SV, Mordechai E, Adelson ME, et al. Identification, quantification and subtyping of Gardnerella vaginalis in noncultured clinical vaginal samples by quantitative PCR. J Med Microbiol. 2014;63(Pt2):162-175. doi:10.1007/s10096-020-04073-6.
  • Gad GFM, El-Adawy AR, Mohammed MS, Ahmed AF, Mohamed HA. Evaluation of different diagnostic methods of bacterial vaginosis. J Dent Med Sci. 2014;13(1):15-23. doi:10.9790/0853-13181523.
  • Lennard K, Dabee S, Barnabas SL, et al. Microbial composition predicts genital tract inflammation and persistent bacterial vaginosis in South African adolescent females. Infect Immun. 2017;86(1):e00410–17. doi:10.1128/IAI.00410-17.
  • Shipitsyna E, Roos A, Datcu R, et al. Composition of the vaginal microbiota in women of reproductive age-- sensitive and specific molecular diagnosis of bacterial vaginosis is possible? PLoS One. 2013;8(4):e60670. doi:10.1371/journal.pone.0060670.
  • Li XD, Wang CC, Zhang XJ, et al. Risk factors for bacterial vaginosis: results from a cross-sectional study having a sample of 53,652 women. Eur J Clin Microbiol Infect Dis. 2014;33(9):1525-1532. doi:10.1007/s10096-014-2103-1.
  • Ranjit E, Raghubanshi BR, Maskey S, Parajuli P. Prevalence of bacterial vaginosis and its association with risk factors among nonpregnant women: A hospital based study. Int J Microbiol. 2018:8349601. doi:10.1155/2018/8349601.
  • Wira CR, Rodriguez-Garcia M, Patel MV. The role of sex hormones in immune protection of the female reproductive tract. Nat Rev Immunol. 2015;15(4):217-230. doi:10.1038/nri3819.
  • Bautista CT, Wurapa E, Sateren WB, Morris S, Hollingsworth B, Sanchez JL. Bacterial vaginosis: a synthesis of the literature on etiology, prevalence, risk factors, and relationship with chlamydia and gonorrhea infections. Mil Med Res. 2016;3:4. doi:10.1186/s40779-016-0074-5.
  • Vodstrcil LA, Twin J, Garland SM, et al. The influence of sexual activity on the vaginal microbiota and Gardnerella vaginalis clade diversity in young women. PLoS One. 2017;12(2):e0171856. doi:10.1371/journal.pone.0171856.
  • Saraf VS, Sheikh SA, Ahmad A, Gillevet PM, Bokhari H, Javed S. Vaginal microbiome: normalcy vs dysbiosis. Arch Microbiol. 2021;203(7):3793-3802. doi:10.1007/s00203-021-02414-3.
  • Janulaitiene M, Paliulyte V, Grinceviciene S, et al. Prevalence and distribution of Gardnerella vaginalis subgroups in women with and without bacterial vaginosis. BMC Infect Dis. 2017;17(1):394. doi:10.1186/s12879-017-2501-y.
  • Zozaya-Hinchliffe M, Lillis R, Martin DH, Ferris MJ. Quantitative PCR assessments of bacterial species in women with and without bacterial vaginosis. J Clin Microbiol. 2010;48(5):1812-1819. doi:10.1128/JCM.00851-09.
  • Datcu R, Gesink D, Mulvad G, et al. Vaginal microbiome in women from Greenland assessed by microscopy and quantitative PCR. BMC Infect Dis. 2013;13:480. doi:10.1186/1471-2334-13-480.
  • Morrill S, Gilbert NM, Lewis AL. Gardnerella vaginalis as a cause of bacterial vaginosis: appraisal of the evidence from in vivo models. Front Cell Infect Microbiol. 2020;10:168. doi:10.3389/fcimb.2020.00168.
  • Schellenberg JJ, Links MG, Hill JE, et al. Molecular definition of vaginal microbiota in East African commercial sex workers. Appl Environ Microbiol. 2011;77(2):4066-4074. doi:10.1128/AEM.02943-10.
  • Tosun I, Alpay Karaoğlu S, Ciftçi H, et al. Biotypes and antibiotic resistance patterns of Gardnerella vaginalis strains isolated from healthy women and women with bacterial vaginosis. Mikrobiyol Bul. 2007;41(1):21-27.
  • Aroutcheva AA, Simoes JA, Behbakht K, Faro S. Gardnerella vaginalis isolated from patients with bacterial vaginosis and from patients with healthy vaginal ecosystems. Clin Infect Dis. 2001;33(7):1022-1027. doi:10.1086/323030.
  • Gültekin M, Zayifoglu Karaca M, Kucukyildiz I, et al. Initial results of population based cervical cancer screening program using HPV testing in one million Turkish women. Int J Cancer. 2018;142(9):1952-1958. doi:10.1002/ijc.31212.
  • Kulhan M, Kulhan NG, Seven Y, et al. Estimation of the prevalence and distribution of HPV genotypes and identification of related risk factors among Turkish women. Contemp Oncol (Pozn). 2017;21(3):218-223. doi:10.5114/wo.2017.69591.
  • Tunç SY, Onan MA, Turp AB, Kuşvuran ED, Fidan I, Güner H. Prevalence and types of cervical human papillomavirus among Turkish women and its relationship with demographic factors in a gynecology outpatient clinic. Eur J Gynaecol Oncol. 2016;37(1):53-58.
  • Niu J, Pan S, Wei Y, et al. Epidemiology and analysis of potential risk factors of high-risk human papillomavirus (HPV) in Shanghai China: A cross-sectional one-year study in non-vaccinated women. J Med Virol. 2022;94(2):761-770. doi:10.1002/jmv.27453.
  • Gao W, Weng J, Gao Y, Chen X. Comparison of the vaginal microbiota diversity of women with and without human papillomavirus infection: a cross-sectional study. BMC Infect Dis. 2013;13:271. doi:10.1186/1471-2334-13-271.
  • Lee JE, Lee S, Lee H, et al. Association of the vaginal microbiota with human papillomavirus infection in a Korean twin cohort. PLoS One. 2013;8(5):e63514. doi:10.1371/journal.pone.0063514.
  • Sanchez-Garcia EK, Contreras-Paredes A, Martinez-Abundis E, Garcia-Chan D, Lizano M, de la Cruz-Hernandez E. Molecular epidemiology of bacterial vaginosis and its association with genital micro-organisms in asymptomatic women. J Med Microbiol. 2019;68(9):1373-1382. doi:10.1099/jmm.0.001044.
  • Meng LT, Xue Y, Yue T, Yang L, Gao L, An RF. Relationship of HPV infection and BV, VVC, TV: a clinical study based on 1 261 cases of gynecologic outpatients. Zhonghua Fu Chan Ke Za Zhi. 2016;51(10):730-733. doi:10.3760/cma.j.issn.0529-567X.2016.10.004.

Vajinal Mikrobiyal Türlerin Bakteriyel Vajinozis ve Human Papillomavirus ile İlişkisinin Araştırılması

Year 2022, Volume: 8 Issue: 3, 218 - 224, 03.10.2022
https://doi.org/10.30934/kusbed.1132919

Abstract

Amaç: Bu çalışmada vajinal mikrobiyal bakteri türlerinin bakteriyel vajinozis (BV) ve yüksek riskli Human papillomavirus (HR-HPV) ile ilişkisinin araştırılması amaçlanmıştır.
Yöntem: Çalışmaya 121 kadın dahil edilmiştir. BV tanısı için Gram boyama yapıldı ve Nugent skoruna göre değerlendirildi. HR-HPV tespiti Real Time High Risk HPV kiti kullanılarak real-time PCR yöntemiyle gerçekleştirildi. Vajinal mikrobiyal türler ve Gardnerella vaginalis subtipleri de real-time PCR ile saptanmıştır.
Bulgular: Bakteriyel vajinozis görülme oranı %38,8 olarak bulunmuştur. Tür sayısı ortalaması; bakteriyel vajinoziste, BV ara değer ve BV negatif örneklere göre anlamlı olarak yüksek görülmüştür. (p=0,001). BVAB2 (p=0,043), Provetella spp. (p=0.015), Leptotrichia/Sneathia (p=0,001), Megaspheara (p=0,048), BV ile ilişkili olduğu görülmüştür. Rastgele seçilen 50 örnekte G.vaginalis subtipleri değerlendirilmiştir. En yaygın “clade 4” subtipi tespit edilmiştir. HR-HPV prevalansı %9,9 olarak saptanmıştır. En sık saptanan HR-HPV tipi HPV 16 %58,33’dü. HR-HPV pozitif ve negatif hastalarda Lactobacillus sp. ortalaması arasında anlamlı fark görülmemiştir (p=0.23). Belirlenen türler ile HR-HPV pozitifliği arasında ilişki saptanmamıştır (p=0,436).
Sonuç: BV tespit edilen kadınların vajenlerinde bakteri çeşitliliği daha fazlaydı. Bakteriyal vajinozis ile Megaspheara, BVAB2, Provetella spp. ve Leptotrichia/Sneathia’nın ilişkili olduğu bulunmuştur.

Project Number

(Project number: 2017TIPF005)

References

  • Ling Z, Kong J, Liu F, et al. Molecular analysis of the diversity of vaginal microbiota associated with bacterial vaginosis. BMC Genomics. 2010;11:488. doi:10.1186/1471-2164-11-488.
  • Zhou X, Hansmann MA, Davis CC, et al. The vaginal bacterial communities of Japanese women resemble those of women in other racial groups. FEMS Immunol Med Microbiol. 2010;58(2):169-181. doi:10.1111/j.1574-695X.2009.00618.x.
  • Gillet E, Meys JF, Verstraelen H, et al. Bacterial vaginosis is associated with uterine cervical human papillomavirus infection: a meta-analysis. BMC Infect Dis. 2011;11:10. doi:10.1186/1471-2334-11-10.
  • Ciccarese G, Herzum A, Pastorino A, et al. Prevalence of genital HPV infection in STI and healthy populations and risk factors for viral persistence. Eur J Clin Microbiol Infect Dis. 2021;40(4):885-888. doi:10.1007/s10096-020-04073-6.
  • Martin DH. The microbiota of the vagina and its influence on women's health and disease. Am J Med Sci. 2012;343(1):2-9. doi:10.1097/MAJ.0b013e31823ea228.
  • Fredricks DN, Fiedler TL, Thomas KK, Oakley BB, Marrazzo JM. Targeted PCR for detection of vaginal bacteria associated with bacterial vaginosis. J Clin Microbiol. 2007;45(10):3270-3276. doi:10.1128/JCM.01272-07.
  • Balashov SV, Mordechai E, Adelson ME, et al. Identification, quantification and subtyping of Gardnerella vaginalis in noncultured clinical vaginal samples by quantitative PCR. J Med Microbiol. 2014;63(Pt2):162-175. doi:10.1007/s10096-020-04073-6.
  • Gad GFM, El-Adawy AR, Mohammed MS, Ahmed AF, Mohamed HA. Evaluation of different diagnostic methods of bacterial vaginosis. J Dent Med Sci. 2014;13(1):15-23. doi:10.9790/0853-13181523.
  • Lennard K, Dabee S, Barnabas SL, et al. Microbial composition predicts genital tract inflammation and persistent bacterial vaginosis in South African adolescent females. Infect Immun. 2017;86(1):e00410–17. doi:10.1128/IAI.00410-17.
  • Shipitsyna E, Roos A, Datcu R, et al. Composition of the vaginal microbiota in women of reproductive age-- sensitive and specific molecular diagnosis of bacterial vaginosis is possible? PLoS One. 2013;8(4):e60670. doi:10.1371/journal.pone.0060670.
  • Li XD, Wang CC, Zhang XJ, et al. Risk factors for bacterial vaginosis: results from a cross-sectional study having a sample of 53,652 women. Eur J Clin Microbiol Infect Dis. 2014;33(9):1525-1532. doi:10.1007/s10096-014-2103-1.
  • Ranjit E, Raghubanshi BR, Maskey S, Parajuli P. Prevalence of bacterial vaginosis and its association with risk factors among nonpregnant women: A hospital based study. Int J Microbiol. 2018:8349601. doi:10.1155/2018/8349601.
  • Wira CR, Rodriguez-Garcia M, Patel MV. The role of sex hormones in immune protection of the female reproductive tract. Nat Rev Immunol. 2015;15(4):217-230. doi:10.1038/nri3819.
  • Bautista CT, Wurapa E, Sateren WB, Morris S, Hollingsworth B, Sanchez JL. Bacterial vaginosis: a synthesis of the literature on etiology, prevalence, risk factors, and relationship with chlamydia and gonorrhea infections. Mil Med Res. 2016;3:4. doi:10.1186/s40779-016-0074-5.
  • Vodstrcil LA, Twin J, Garland SM, et al. The influence of sexual activity on the vaginal microbiota and Gardnerella vaginalis clade diversity in young women. PLoS One. 2017;12(2):e0171856. doi:10.1371/journal.pone.0171856.
  • Saraf VS, Sheikh SA, Ahmad A, Gillevet PM, Bokhari H, Javed S. Vaginal microbiome: normalcy vs dysbiosis. Arch Microbiol. 2021;203(7):3793-3802. doi:10.1007/s00203-021-02414-3.
  • Janulaitiene M, Paliulyte V, Grinceviciene S, et al. Prevalence and distribution of Gardnerella vaginalis subgroups in women with and without bacterial vaginosis. BMC Infect Dis. 2017;17(1):394. doi:10.1186/s12879-017-2501-y.
  • Zozaya-Hinchliffe M, Lillis R, Martin DH, Ferris MJ. Quantitative PCR assessments of bacterial species in women with and without bacterial vaginosis. J Clin Microbiol. 2010;48(5):1812-1819. doi:10.1128/JCM.00851-09.
  • Datcu R, Gesink D, Mulvad G, et al. Vaginal microbiome in women from Greenland assessed by microscopy and quantitative PCR. BMC Infect Dis. 2013;13:480. doi:10.1186/1471-2334-13-480.
  • Morrill S, Gilbert NM, Lewis AL. Gardnerella vaginalis as a cause of bacterial vaginosis: appraisal of the evidence from in vivo models. Front Cell Infect Microbiol. 2020;10:168. doi:10.3389/fcimb.2020.00168.
  • Schellenberg JJ, Links MG, Hill JE, et al. Molecular definition of vaginal microbiota in East African commercial sex workers. Appl Environ Microbiol. 2011;77(2):4066-4074. doi:10.1128/AEM.02943-10.
  • Tosun I, Alpay Karaoğlu S, Ciftçi H, et al. Biotypes and antibiotic resistance patterns of Gardnerella vaginalis strains isolated from healthy women and women with bacterial vaginosis. Mikrobiyol Bul. 2007;41(1):21-27.
  • Aroutcheva AA, Simoes JA, Behbakht K, Faro S. Gardnerella vaginalis isolated from patients with bacterial vaginosis and from patients with healthy vaginal ecosystems. Clin Infect Dis. 2001;33(7):1022-1027. doi:10.1086/323030.
  • Gültekin M, Zayifoglu Karaca M, Kucukyildiz I, et al. Initial results of population based cervical cancer screening program using HPV testing in one million Turkish women. Int J Cancer. 2018;142(9):1952-1958. doi:10.1002/ijc.31212.
  • Kulhan M, Kulhan NG, Seven Y, et al. Estimation of the prevalence and distribution of HPV genotypes and identification of related risk factors among Turkish women. Contemp Oncol (Pozn). 2017;21(3):218-223. doi:10.5114/wo.2017.69591.
  • Tunç SY, Onan MA, Turp AB, Kuşvuran ED, Fidan I, Güner H. Prevalence and types of cervical human papillomavirus among Turkish women and its relationship with demographic factors in a gynecology outpatient clinic. Eur J Gynaecol Oncol. 2016;37(1):53-58.
  • Niu J, Pan S, Wei Y, et al. Epidemiology and analysis of potential risk factors of high-risk human papillomavirus (HPV) in Shanghai China: A cross-sectional one-year study in non-vaccinated women. J Med Virol. 2022;94(2):761-770. doi:10.1002/jmv.27453.
  • Gao W, Weng J, Gao Y, Chen X. Comparison of the vaginal microbiota diversity of women with and without human papillomavirus infection: a cross-sectional study. BMC Infect Dis. 2013;13:271. doi:10.1186/1471-2334-13-271.
  • Lee JE, Lee S, Lee H, et al. Association of the vaginal microbiota with human papillomavirus infection in a Korean twin cohort. PLoS One. 2013;8(5):e63514. doi:10.1371/journal.pone.0063514.
  • Sanchez-Garcia EK, Contreras-Paredes A, Martinez-Abundis E, Garcia-Chan D, Lizano M, de la Cruz-Hernandez E. Molecular epidemiology of bacterial vaginosis and its association with genital micro-organisms in asymptomatic women. J Med Microbiol. 2019;68(9):1373-1382. doi:10.1099/jmm.0.001044.
  • Meng LT, Xue Y, Yue T, Yang L, Gao L, An RF. Relationship of HPV infection and BV, VVC, TV: a clinical study based on 1 261 cases of gynecologic outpatients. Zhonghua Fu Chan Ke Za Zhi. 2016;51(10):730-733. doi:10.3760/cma.j.issn.0529-567X.2016.10.004.
There are 31 citations in total.

Details

Primary Language English
Subjects Medical Microbiology
Journal Section Original Article / Medical Sciences
Authors

Sedef Zeliha Öner 0000-0002-9964-2526

İlknur Kaleli 0000-0001-9689-8297

Babür Kaleli 0000-0002-5122-9329

Project Number (Project number: 2017TIPF005)
Publication Date October 3, 2022
Submission Date June 19, 2022
Acceptance Date August 25, 2022
Published in Issue Year 2022 Volume: 8 Issue: 3

Cite

APA Öner, S. Z., Kaleli, İ., & Kaleli, B. (2022). An Investigation the Relationship of Vaginal Microbial Bacteria Species with Bacterial Vaginosis and High-Risk Human Papillomavirus. Kocaeli Üniversitesi Sağlık Bilimleri Dergisi, 8(3), 218-224. https://doi.org/10.30934/kusbed.1132919
AMA Öner SZ, Kaleli İ, Kaleli B. An Investigation the Relationship of Vaginal Microbial Bacteria Species with Bacterial Vaginosis and High-Risk Human Papillomavirus. KOU Sag Bil Derg. October 2022;8(3):218-224. doi:10.30934/kusbed.1132919
Chicago Öner, Sedef Zeliha, İlknur Kaleli, and Babür Kaleli. “An Investigation the Relationship of Vaginal Microbial Bacteria Species With Bacterial Vaginosis and High-Risk Human Papillomavirus”. Kocaeli Üniversitesi Sağlık Bilimleri Dergisi 8, no. 3 (October 2022): 218-24. https://doi.org/10.30934/kusbed.1132919.
EndNote Öner SZ, Kaleli İ, Kaleli B (October 1, 2022) An Investigation the Relationship of Vaginal Microbial Bacteria Species with Bacterial Vaginosis and High-Risk Human Papillomavirus. Kocaeli Üniversitesi Sağlık Bilimleri Dergisi 8 3 218–224.
IEEE S. Z. Öner, İ. Kaleli, and B. Kaleli, “An Investigation the Relationship of Vaginal Microbial Bacteria Species with Bacterial Vaginosis and High-Risk Human Papillomavirus”, KOU Sag Bil Derg, vol. 8, no. 3, pp. 218–224, 2022, doi: 10.30934/kusbed.1132919.
ISNAD Öner, Sedef Zeliha et al. “An Investigation the Relationship of Vaginal Microbial Bacteria Species With Bacterial Vaginosis and High-Risk Human Papillomavirus”. Kocaeli Üniversitesi Sağlık Bilimleri Dergisi 8/3 (October 2022), 218-224. https://doi.org/10.30934/kusbed.1132919.
JAMA Öner SZ, Kaleli İ, Kaleli B. An Investigation the Relationship of Vaginal Microbial Bacteria Species with Bacterial Vaginosis and High-Risk Human Papillomavirus. KOU Sag Bil Derg. 2022;8:218–224.
MLA Öner, Sedef Zeliha et al. “An Investigation the Relationship of Vaginal Microbial Bacteria Species With Bacterial Vaginosis and High-Risk Human Papillomavirus”. Kocaeli Üniversitesi Sağlık Bilimleri Dergisi, vol. 8, no. 3, 2022, pp. 218-24, doi:10.30934/kusbed.1132919.
Vancouver Öner SZ, Kaleli İ, Kaleli B. An Investigation the Relationship of Vaginal Microbial Bacteria Species with Bacterial Vaginosis and High-Risk Human Papillomavirus. KOU Sag Bil Derg. 2022;8(3):218-24.