Diversity of endocervical microbiota associated with genital Chlamydia trachomatis infection and infertility among women visiting obstetrics and gynecology clinics in Malaysia


Autoři: Heng Choon Cheong aff001;  Polly Soo Xi Yap aff001;  Chun Wie Chong aff002;  Yi Ying Cheok aff001;  Chalystha Yie Qin Lee aff001;  Grace Min Yi Tan aff001;  Sofiah Sulaiman aff003;  Jamiyah Hassan aff003;  Negar Shafiei Sabet aff004;  Chung Yeng Looi aff005;  Rishein Gupta aff006;  Bernard Arulanandam aff006;  Sazaly AbuBakar aff001;  Cindy Shuan Ju Teh aff001;  Li Yen Chang aff001;  Won Fen Wong aff001
Působiště autorů: Department of Medical Microbiology, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia aff001;  School of Pharmacy, Monash University Malaysia, Jalan Lagoon Selatan, Bandar Sunway, Selangor, Malaysia aff002;  Department of Obstetrics and Gynecology, Faculty of medicine, University of Malaya, Kuala Lumpur, Malaysia aff003;  Faculty of Medicine, SEGi University, Kota Damansara, Selangor, Malaysia aff004;  School of Bioscience, Taylor’s University, Subang Jaya, Selangor, Malaysia aff005;  Center of Excellence in Infection Genomics, South Texas Center for Emerging Infectious Diseases, University of Texas at San Antonio, San Antonio, Texas, United States of America aff006;  Tropical Infectious Disease Research and Education Center, University of Malaya, Kuala Lumpur, Malaysia aff007
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224658

Souhrn

The cervical microbiota constitutes an important protective barrier against the invasion of pathogenic microorganisms. A disruption of microbiota within the cervical milieu has been suggested to be a driving factor of sexually transmitted infections. These include Chlamydia trachomatis which frequently causes serious reproductive sequelae such as infertility in women. In this study, we profiled the cervical microbial composition of a population of 70 reproductive-age Malaysian women; among which 40 (57.1%) were diagnosed with genital C. trachomatis infection, and 30 (42.8%) without C. trachomatis infection. Our findings showed a distinct compositional difference between the cervical microbiota of C. trachomatis-infected subjects and subjects without C. trachomatis infection. Specifically, significant elevations of mostly strict and facultative anaerobes such as Streptococcus, Megasphaera, Prevotella, and Veillonella in the cervical microbiota of C. trachomatis-positive women were detected. The results from the current study highlights an interaction of C. trachomatis with the environmental microbiome in the endocervical region.

Klíčová slova:

Chlamydia infection – Lactobacillus – Microbiome – Pseudomonas infections – Ribosomal RNA – Streptococcal infections – Prevotella infection


Zdroje

1. Newman L, Rowley J, Vander Hoorn S, Wijesooriya NS, Unemo M, Low N, et al. Global Estimates of the Prevalence and Incidence of Four Curable Sexually Transmitted Infections in 2012 Based on Systematic Review and Global Reporting. PLoS One. 2015;10(12):e0143304. doi: 10.1371/journal.pone.0143304 26646541; PubMed Central PMCID: PMC4672879.

2. Unemo M, Bradshaw CS, Hocking JS, de Vries HJC, Francis SC, Mabey D, et al. Sexually transmitted infections: challenges ahead. Lancet Infect Dis. 2017;17(8):e235–e79. Epub 2017/07/14. doi: 10.1016/S1473-3099(17)30310-9 28701272.

3. Ngeow YF, Rachagan SP, Ramachandran S. Prevalence of chlamydial antibody in Malaysians. J Clin Pathol. 1990;43(5):400–2. Epub 1990/05/01. doi: 10.1136/jcp.43.5.400 2196283; PubMed Central PMCID: PMC502444.

4. Ravindran J, Tan YI, Ngeow YF. The prevalence of Chlamydia trachomatis in patients with pelvic inflammatory disease. Med J Malaysia. 1998;53(1):16–21. Epub 2000/09/01. 10968132.

5. Yeow TC, Wong WF, Sabet NS, Sulaiman S, Shahhosseini F, Tan GM, et al. Prevalence of plasmid-bearing and plasmid-free Chlamydia trachomatis infection among women who visited obstetrics and gynecology clinics in Malaysia. BMC Microbiol. 2016;16:45. Epub 2016/03/19. doi: 10.1186/s12866-016-0671-1 26987367; PubMed Central PMCID: PMC4797335.

6. Lau CY, Qureshi AK. Azithromycin versus doxycycline for genital chlamydial infections: a meta-analysis of randomized clinical trials. Sex Transm Dis. 2002;29(9):497–502. Epub 2002/09/10. doi: 10.1097/00007435-200209000-00001 12218839.

7. Miller KE. Diagnosis and treatment of Chlamydia trachomatis infection. Am Fam Physician. 2006;73(8):1411–6. 16669564.

8. Spiliopoulou A, Lakiotis V, Vittoraki A, Zavou D, Mauri D. Chlamydia trachomatis: time for screening? Clin Microbiol Infect. 2005;11(9):687–9. doi: 10.1111/j.1469-0691.2005.01187.x 16104982.

9. Walker J, Tabrizi SN, Fairley CK, Chen MY, Bradshaw CS, Twin J, et al. Chlamydia trachomatis incidence and re-infection among young women—behavioural and microbiological characteristics. PLoS One. 2012;7(5):e37778. doi: 10.1371/journal.pone.0037778 22662220; PubMed Central PMCID: PMC3360595.

10. Brunham RC, Rey-Ladino J. Immunology of Chlamydia infection: implications for a Chlamydia trachomatis vaccine. Nat Rev Immunol. 2005;5(2):149–61. doi: 10.1038/nri1551 15688042.

11. Moss NJ, Ahrens K, Kent CK, Klausner JD. The decline in clinical sequelae of genital Chlamydia trachomatis infection supports current control strategies. J Infect Dis. 2006;193(9):1336–8; author reply 8–9. doi: 10.1086/503114 16586376.

12. Mackern-Oberti JP, Motrich RD, Breser ML, Sanchez LR, Cuffini C, Rivero VE. Chlamydia trachomatis infection of the male genital tract: an update. J Reprod Immunol. 2013;100(1):37–53. doi: 10.1016/j.jri.2013.05.002 23870458.

13. Manavi K. A review on infection with Chlamydia trachomatis. Best Pract Res Clin Obstet Gynaecol. 2006;20(6):941–51. doi: 10.1016/j.bpobgyn.2006.06.003 16934531.

14. Wilkowska-Trojniel M, Zdrodowska-Stefanow B, Ostaszewska-Puchalska I, Redzko S, Przepiesc J, Zdrodowski M. The influence of Chlamydia trachomatis infection on spontaneous abortions. Adv Med Sci. 2009;54(1):86–90. doi: 10.2478/v10039-009-0008-5 19403438.

15. Rours GI, Duijts L, Moll HA, Arends LR, de Groot R, Jaddoe VW, et al. Chlamydia trachomatis infection during pregnancy associated with preterm delivery: a population-based prospective cohort study. Eur J Epidemiol. 2011;26(6):493–502. doi: 10.1007/s10654-011-9586-1 21538042; PubMed Central PMCID: PMC3115062.

16. Kaminska D, Gajecka M. Is the role of human female reproductive tract microbiota underestimated? Benef Microbes. 2017;8(3):327–43. Epub 2017/05/16. doi: 10.3920/BM2015.0174 28504576.

17. Cribby S, Taylor M, Reid G. Vaginal microbiota and the use of probiotics. Interdiscip Perspect Infect Dis. 2008;2008:256490. Epub 2008/01/01. doi: 10.1155/2008/256490 19343185; PubMed Central PMCID: PMC2662373.

18. Gong Z, Luna Y, Yu P, Fan H. Lactobacilli inactivate Chlamydia trachomatis through lactic acid but not H2O2. PLoS One. 2014;9(9):e107758. Epub 2014/09/13. doi: 10.1371/journal.pone.0107758 25215504; PubMed Central PMCID: PMC4162611.

19. Mastromarino P, Di Pietro M, Schiavoni G, Nardis C, Gentile M, Sessa R. Effects of vaginal lactobacilli in Chlamydia trachomatis infection. Int J Med Microbiol. 2014;304(5–6):654–61. Epub 2014/05/31. doi: 10.1016/j.ijmm.2014.04.006 24875405.

20. Nardini P, Nahui Palomino RA, Parolin C, Laghi L, Foschi C, Cevenini R, et al. Lactobacillus crispatus inhibits the infectivity of Chlamydia trachomatis elementary bodies, in vitro study. Sci Rep. 2016;6:29024. Epub 2016/06/30. doi: 10.1038/srep29024 27354249; PubMed Central PMCID: PMC4926251.

21. Gillet E, Meys JF, Verstraelen H, Bosire C, De Sutter P, Temmerman M, et al. Bacterial vaginosis is associated with uterine cervical human papillomavirus infection: a meta-analysis. BMC Infect Dis. 2011;11:10. Epub 2011/01/13. doi: 10.1186/1471-2334-11-10 21223574; PubMed Central PMCID: PMC3023697.

22. Brotman RM, Bradford LL, Conrad M, Gajer P, Ault K, Peralta L, et al. Association between Trichomonas vaginalis and vaginal bacterial community composition among reproductive-age women. Sex Transm Dis. 2012;39(10):807–12. Epub 2012/09/26. doi: 10.1097/OLQ.0b013e3182631c79 23007708; PubMed Central PMCID: PMC3458234.

23. Gallo MF, Macaluso M, Warner L, Fleenor ME, Hook EW 3rd, Brill I, et al. Bacterial vaginosis, gonorrhea, and chlamydial infection among women attending a sexually transmitted disease clinic: a longitudinal analysis of possible causal links. Ann Epidemiol. 2012;22(3):213–20. Epub 2011/12/24. doi: 10.1016/j.annepidem.2011.11.005 22192490.

24. Bautista CT, Wurapa EK, Sateren WB, Morris SM, Hollingsworth BP, Sanchez JL. Association of Bacterial Vaginosis With Chlamydia and Gonorrhea Among Women in the U.S. Army. Am J Prev Med. 2017;52(5):632–9. Epub 2016/11/07. doi: 10.1016/j.amepre.2016.09.016 27816380.

25. Gosmann C, Anahtar MN, Handley SA, Farcasanu M, Abu-Ali G, Bowman BA, et al. Lactobacillus-Deficient Cervicovaginal Bacterial Communities Are Associated with Increased HIV Acquisition in Young South African Women. Immunity. 2017;46(1):29–37. doi: 10.1016/j.immuni.2016.12.013 28087240; PubMed Central PMCID: PMC5270628.

26. van der Veer C, Bruisten SM, van der Helm JJ, de Vries HJ, van Houdt R. The Cervicovaginal Microbiota in Women Notified for Chlamydia trachomatis Infection: A Case-Control Study at the Sexually Transmitted Infection Outpatient Clinic in Amsterdam, The Netherlands. Clin Infect Dis. 2017;64(1):24–31. Epub 2016/08/28. doi: 10.1093/cid/ciw586 27567124.

27. Filardo S, Di Pietro M, Porpora MG, Recine N, Farcomeni A, Latino MA, et al. Diversity of Cervical Microbiota in Asymptomatic Chlamydia trachomatis Genital Infection: A Pilot Study. Front Cell Infect Microbiol. 2017;7:321. Epub 2017/08/05. doi: 10.3389/fcimb.2017.00321 28770172; PubMed Central PMCID: PMC5509768.

28. Balle C, Lennard K, Dabee S, Barnabas SL, Jaumdally SZ, Gasper MA, et al. Endocervical and vaginal microbiota in South African adolescents with asymptomatic Chlamydia trachomatis infection. Sci Rep. 2018;8(1):11109. Epub 2018/07/25. doi: 10.1038/s41598-018-29320-x 30038262; PubMed Central PMCID: PMC6056523.

29. Tamarelle J, de Barbeyrac B, Le Hen I, Thiebaut A, Bebear C, Ravel J, et al. Vaginal microbiota composition and association with prevalent Chlamydia trachomatis infection: a cross-sectional study of young women attending a STI clinic in France. Sex Transm Infect. 2018. Epub 2018/01/24. doi: 10.1136/sextrans-2017-053346 29358524.

30. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75(23):7537–41. Epub 2009/10/06. doi: 10.1128/AEM.01541-09 PubMed Central PMCID: PMC2786419. 19801464

31. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8(4):e61217. Epub 2013/05/01. doi: 10.1371/journal.pone.0061217 23630581; PubMed Central PMCID: PMC3632530.

32. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550. Epub 2014/12/18. doi: 10.1186/s13059-014-0550-8 25516281; PubMed Central PMCID: PMC4302049.

33. Davies B, Turner KM, Frolund M, Ward H, May MT, Rasmussen S, et al. Risk of reproductive complications following chlamydia testing: a population-based retrospective cohort study in Denmark. Lancet Infect Dis. 2016;16(9):1057–64. doi: 10.1016/S1473-3099(16)30092-5 27289389.

34. Group NHW, Peterson J, Garges S, Giovanni M, McInnes P, Wang L, et al. The NIH Human Microbiome Project. Genome Res. 2009;19(12):2317–23. Epub 2009/10/13. doi: 10.1101/gr.096651.109 19819907; PubMed Central PMCID: PMC2792171.

35. Wiesenfeld HC, Hillier SL, Krohn MA, Landers DV, Sweet RL. Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clin Infect Dis. 2003;36(5):663–8. Epub 2003/02/21. doi: 10.1086/367658 12594649.

36. Biagi E, Vitali B, Pugliese C, Candela M, Donders GG, Brigidi P. Quantitative variations in the vaginal bacterial population associated with asymptomatic infections: a real-time polymerase chain reaction study. Eur J Clin Microbiol Infect Dis. 2009;28(3):281–5. Epub 2008/09/03. doi: 10.1007/s10096-008-0617-0 18762999.

37. Turovskiy Y, Sutyak Noll K, Chikindas ML. The aetiology of bacterial vaginosis. J Appl Microbiol. 2011;110(5):1105–28. Epub 2011/02/22. doi: 10.1111/j.1365-2672.2011.04977.x 21332897; PubMed Central PMCID: PMC3072448.

38. Nelson TM, Borgogna JL, Brotman RM, Ravel J, Walk ST, Yeoman CJ. Vaginal biogenic amines: biomarkers of bacterial vaginosis or precursors to vaginal dysbiosis? Front Physiol. 2015;6:253. Epub 2015/10/21. doi: 10.3389/fphys.2015.00253 26483694; PubMed Central PMCID: PMC4586437.

39. 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;2018:8349601. Epub 2018/04/26. doi: 10.1155/2018/8349601 29692813; PubMed Central PMCID: PMC5859802.

40. Di Pietro M, Filardo S, Porpora MG, Recine N, Latino MA, Sessa R. HPV/Chlamydia trachomatis co-infection: metagenomic analysis of cervical microbiota in asymptomatic women. New Microbiol. 2018;41(1):34–41. Epub 2018/01/10. 29313867.

41. Witkin SS. Vaginal microbiome studies in pregnancy must also analyse host factors. BJOG. 2019;126(3):359. Epub 2018/05/24. doi: 10.1111/1471-0528.15300 29791773.

42. DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One. 2008;3(8):e3056. Epub 2008/08/30. doi: 10.1371/journal.pone.0003056 18725970; PubMed Central PMCID: PMC2516597.

43. You Y-A, Yoo JY, Kwon EJ, Kim YJ. Blood Microbial Communities During Pregnancy Are Associated With Preterm Birth. Frontiers in Microbiology. 2019;10(1122). doi: 10.3389/fmicb.2019.01122 31214131

44. Takada K, Komine-Aizawa S, Kuramochi T, Ito S, Trinh QD, Pham NTK, et al. Lactobacillus crispatus accelerates re-epithelialization in vaginal epithelial cell line MS74. Am J Reprod Immunol. 2018;80(3):e13027. Epub 2018/08/26. doi: 10.1111/aji.13027 30144195.

45. 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. Epub 2013/06/14. doi: 10.1186/1471-2334-13-271 23758857; PubMed Central PMCID: PMC3684509.

46. Shi Y, Chen L, Tong J, Xu C. Preliminary characterization of vaginal microbiota in healthy Chinese women using cultivation-independent methods. J Obstet Gynaecol Res. 2009;35(3):525–32. Epub 2009/06/17. doi: 10.1111/j.1447-0756.2008.00971.x 19527394.

47. Sirichoat A, Buppasiri P, Engchanil C, Namwat W, Faksri K, Sankuntaw N, et al. Characterization of vaginal microbiota in Thai women. PeerJ. 2018;6:e5977. Epub 2018/12/01. doi: 10.7717/peerj.5977 30498641; PubMed Central PMCID: PMC6252066.

48. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A. 2011;108 Suppl 1:4680–7. Epub 2010/06/11. doi: 10.1073/pnas.1002611107 20534435; PubMed Central PMCID: PMC3063603.

49. Tamrakar R, Yamada T, Furuta I, Cho K, Morikawa M, Yamada H, et al. Association between Lactobacillus species and bacterial vaginosis-related bacteria, and bacterial vaginosis scores in pregnant Japanese women. BMC Infect Dis. 2007;7:128. Epub 2007/11/08. doi: 10.1186/1471-2334-7-128 17986357; PubMed Central PMCID: PMC2212641.

50. Macklaim JM, Gloor GB, Anukam KC, Cribby S, Reid G. At the crossroads of vaginal health and disease, the genome sequence of Lactobacillus iners AB-1. Proc Natl Acad Sci U S A. 2011;108 Suppl 1:4688–95. Epub 2010/11/10. doi: 10.1073/pnas.1000086107 21059957; PubMed Central PMCID: PMC3063587.

51. Kindinger LM, Bennett PR, Lee YS, Marchesi JR, Smith A, Cacciatore S, et al. The interaction between vaginal microbiota, cervical length, and vaginal progesterone treatment for preterm birth risk. Microbiome. 2017;5(1):6. Epub 2017/01/21. doi: 10.1186/s40168-016-0223-9 28103952; PubMed Central PMCID: PMC5244550.

52. Stafford GP, Parker JL, Amabebe E, Kistler J, Reynolds S, Stern V, et al. Spontaneous Preterm Birth Is Associated with Differential Expression of Vaginal Metabolites by Lactobacilli-Dominated Microflora. Front Physiol. 2017;8:615. Epub 2017/09/08. doi: 10.3389/fphys.2017.00615 28878691; PubMed Central PMCID: PMC5572350.

53. Borgdorff H, Tsivtsivadze E, Verhelst R, Marzorati M, Jurriaans S, Ndayisaba GF, et al. Lactobacillus-dominated cervicovaginal microbiota associated with reduced HIV/STI prevalence and genital HIV viral load in African women. ISME J. 2014;8(9):1781–93. Epub 2014/03/07. doi: 10.1038/ismej.2014.26 24599071; PubMed Central PMCID: PMC4139719.

54. Molenaar MC, Singer M, Ouburg S. The two-sided role of the vaginal microbiome in Chlamydia trachomatis and Mycoplasma genitalium pathogenesis. J Reprod Immunol. 2018;130:11–7. Epub 2018/08/28. doi: 10.1016/j.jri.2018.08.006 30149363.

55. van Houdt R, Ma B, Bruisten SM, Speksnijder A, Ravel J, de Vries HJC. Lactobacillus iners-dominated vaginal microbiota is associated with increased susceptibility to Chlamydia trachomatis infection in Dutch women: a case-control study. Sex Transm Infect. 2018;94(2):117–23. Epub 2017/09/28. doi: 10.1136/sextrans-2017-053133 28947665; PubMed Central PMCID: PMC6083440.

56. Mohan B, Zaman K, Anand N, Taneja N. Aerococcus Viridans: A Rare Pathogen Causing Urinary Tract Infection. J Clin Diagn Res. 2017;11(1):DR01–DR3. Epub 2017/03/10. doi: 10.7860/JCDR/2017/23997.9229 28273968; PubMed Central PMCID: PMC5324413.

57. Higgins A, Garg T. Aerococcus urinae: An Emerging Cause of Urinary Tract Infection in Older Adults with Multimorbidity and Urologic Cancer. Urol Case Rep. 2017;13:24–5. Epub 2017/04/25. doi: 10.1016/j.eucr.2017.03.022 28435789; PubMed Central PMCID: PMC5393163.

58. Zhang Q, Kwoh C, Attorri S, Clarridge JE 3rd. Aerococcus urinae in urinary tract infections. J Clin Microbiol. 2000;38(4):1703–5. Epub 2000/04/04. 10747177; PubMed Central PMCID: PMC86536.

59. Carlstein C, Marie Soes L, Jorgen Christensen J. Aerococcus christensenii as Part of Severe Polymicrobial Chorioamnionitis in a Pregnant Woman. Open Microbiol J. 2016;10:27–31. Epub 2016/03/26. doi: 10.2174/1874285801610010027 27014376; PubMed Central PMCID: PMC4787314.

60. Vartivarian SE, Papadakis KA, Anaissie EJ. Stenotrophomonas (Xanthomonas) maltophilia urinary tract infection. A disease that is usually severe and complicated. Arch Intern Med. 1996;156(4):433–5. Epub 1996/02/26. 8607729.

61. Denton M, Kerr KG. Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clin Microbiol Rev. 1998;11(1):57–80. Epub 1998/02/11. 9457429; PubMed Central PMCID: PMC121376.

62. Kebschull JM, Zador AM. Sources of PCR-induced distortions in high-throughput sequencing data sets. Nucleic Acids Res. 2015;43(21):e143. Epub 2015/07/19. doi: 10.1093/nar/gkv717 26187991; PubMed Central PMCID: PMC4666380.


Článek vyšel v časopise

PLOS One


2019 Číslo 11