Mycoplasma genitalium Infection and Female Reproductive Tract Disease: A Meta-analysis

Clinical Infectious Diseases

Volumn 61, Issue 3, 2015, Pages 418-426

  Lis, Rebecca ^a   Rowhani Rahbar, Ali ^a   Manhart, Lisa E ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

cervicitis; female infertility; Mycoplasma genitalium; pelvic inflammatory disease; pregnancy outcomes

Indexed keywords

ADVERSE OUTCOME; DISEASE ASSOCIATION; FEMALE; FEMALE INFERTILITY; GYNECOLOGIC DISEASE; HIGH RISK PATIENT; HUMAN; INFECTION RISK; META ANALYSIS; MIXED INFECTION; MYCOPLASMA GENITALIUM; MYCOPLASMOSIS; NONHUMAN; PEER REVIEW; PELVIC INFLAMMATORY DISEASE; PREGNANCY OUTCOME; PREMATURE LABOR; PRIORITY JOURNAL; PUBLISHING; REVIEW; SPONTANEOUS ABORTION; SYSTEMATIC REVIEW; UTERINE CERVICITIS; PREGNANCY;

FEMALE; HUMANS; INFERTILITY, FEMALE; MYCOPLASMA GENITALIUM; MYCOPLASMA INFECTIONS; PELVIC INFLAMMATORY DISEASE; PREGNANCY; PREGNANCY OUTCOME; UTERINE CERVICITIS;

EID: 84938604217     PISSN: 10584838     EISSN: 15376591     Source Type: Journal    
DOI: 10.1093/cid/civ312     Document Type: Review

References (81)

1. Taylor-Robinson D, Jensen JS. Mycoplasma genitalium: from Chrysalis to multicolored butterfly. Clin Microbiol Rev 2011; 24:498-514.
2. McGowin CL, Anderson-Smits C. Mycoplasma genitalium: an emerging cause of sexually transmitted disease in women. PLoS Pathog 2011; 7:e1001324.
3. Manhart LE, Gillespie CW, Lowens MS, et al. Standard treatment regimens for nongonococcal urethritis have similar but declining cure rates: a randomized controlled trial. Clin Infect Dis 2013; 56:934-42.
4. Schwebke JR, Rompalo A, Taylor S, et al. Re-evaluating the treatment of nongonococcal urethritis: emphasizing emerging pathogens-a randomized clinical trial. Clin Infect Dis 2011; 52:163-70.
5. Higgins JP, Altman DG, Gotzsche PC, et al. The Cochrane Collaboration's tool for assessing risk of bias in randomised trials. BMJ 2011; 343: d5928.
6. Sanderson S, Tatt ID, Higgins JP. Tools for assessing quality and susceptibility to bias in observational studies in epidemiology: a systematic review and annotated bibliography. Int J Epidemiol 2007; 36:666-76.
7. Lipsey MW, Wilson DB. Practical meta-analysis. Thousand Oaks, CA: SAGE Publications Inc, 2001.
8. Higgins JPT, Green S. Cochrane handbook for systematic reviews of interventions, version 5.1.0 [updated March 2011]. Available at: http:// handbook.cochrane.org/. Accessed 20 August 2014.
9. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994; 50:1088-101.
10. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315:629-34.
11. Carne CA, Gibbs J, Delaney A, et al. Prevalence, clinical features and quantification of genital non-viral infections. Int J STD AIDS 2013; 24:273-7.
12. Thurman AR, Musatovova O, Perdue S, Shain RN, Baseman JG, Baseman JB. Mycoplasma genitalium symptoms, concordance and treatment in high-risk sexual dyads. Int J STD AIDS 2010; 21:177-83.
13. Schlicht MJ, Lovrich SD, Sartin JS, Karpinsky P, Callister SM, Agger WA. High prevalence of genital mycoplasmas among sexually active young adults with urethritis or cervicitis symptoms in La Crosse, Wisconsin. J Clin Microbiol 2004; 42:4636-40.
14. Manhart LE, Critchlow CW, Holmes KK, et al. Mucopurulent cervicitis and Mycoplasma genitalium. J Infect Dis 2003; 187:650-7.
15. Pepin J, Labbe AC, Khonde N, et al. Mycoplasma genitalium: an organism commonly associated with cervicitis amongWest African sex workers. Sex Transm Infect 2005; 81:67-72.
16. Korte JE, Baseman JB, Cagle MP, et al. Cervicitis and genitourinary symptoms in women culture positive for Mycoplasma genitalium. Am J Reprod Immunol 2006; 55:265-75.
17. Pepin J, Sobela F, Khonde N, et al. The syndromic management of vaginal discharge using single-dose treatments: a randomized controlled trial in West Africa. Bull World Health Organ 2006; 84:729-38.
18. Gaydos C, Maldeis NE, Hardick A, Hardick J, Quinn TC. Mycoplasma genitalium as a contributor to the multiple etiologies of cervicitis in women attending sexually transmitted disease clinics. Sex Transm Dis 2009; 36:598-606.
19. Lusk MJ, Konecny P, Naing ZW, Garden FL, Cumming RG, Rawlinson WD. Mycoplasma genitalium is associated with cervicitis and HIV infection in an urban Australian STI clinic population. Sex Transm Infect 2011; 87:107-9.
20. Bjartling C, Osser S, Persson K. Mycoplasma genitalium in cervicitis and pelvic inflammatory disease among women at a gynecologic outpatient service. Am J Obstet Gynecol 2012; 206:476.e1-8.
21. Mobley VL, Hobbs MM, Lau K, Weinbaum BS, Getman DK, Sena AC. Mycoplasma genitalium infection in women attending a sexually transmitted infection clinic: diagnostic specimen type, coinfections, and predictors. Sex Transm Dis 2012; 39:706-9.
22. Oliphant J, Azariah S. Cervicitis: limited clinical utility for the detection of Mycoplasma genitalium in a cross-sectional study of women attending a New Zealand sexual health clinic. Sex Health 2013; 10:263-7.
23. Huppert JS, Mortensen JE, Reed JL, Kahn JA, Rich KD, Hobbs MM. Mycoplasma genitalium detected by transcription-mediated amplification is associated with Chlamydia trachomatis in adolescent women. Sex Transm Dis 2008; 35:250-4.
24. Vandepitte J, Bukenya J, Hughes P, et al. Clinical characteristics associated with Mycoplasma genitalium infection among women at high risk of HIV and other STI in Uganda. Sex Transm Dis 2012; 39:487-91.
25. Anagrius C, Lore B, Jensen JS. Mycoplasma genitalium: prevalence, clinical significance, and transmission. Sex Transm Infect 2005; 81:458-62.
26. Moi H, Reinton N, Moghaddam A. Mycoplasma genitalium in women with lower genital tract inflammation. Sex Transm Infect 2009; 85:10-4.
27. Palmer HM, Gilroy CB, Claydon EJ, Taylor-Robinson D. Detection of Mycoplasma genitalium in the genitourinary tract of women by the polymerase chain reaction. Int J STD AIDS 1991; 2:261-3.
28. Uno M, Deguchi T, Komeda H, et al. Mycoplasma genitalium in the cervices of Japanese women. Sex Transm Dis 1997; 24:284-6.
29. Casin I, Vexiau-Robert D, De La Salmoniere P, Eche A, Grandry B, Janier M. High prevalence of Mycoplasma genitalium in the lower genitourinary tract of women attending a sexually transmitted disease clinic in Paris, France. Sex Transm Dis 2002; 29:353-9.
30. Falk L, Fredlund H, Jensen JS. Signs and symptoms of urethritis and cervicitis among women with or without Mycoplasma genitalium or Chlamydia trachomatis infection. Sex Transm Infect 2005; 81:73-8.
31. Hogdahl M, Kihlstrom E. Leucocyte esterase testing of first-voided urine and urethral and cervical smears to identify Mycoplasma genitaliuminfected men and women. Int J STD AIDS 2007; 18:835-8.
32. Falk L. The overall agreement of proposed definitions of mucopurulent cervicitis in women at high risk of chlamydia infection. Acta Derm Venereol 2010; 90:506-11.
33. Manhart LE, Mostad SB, Baeten JM, Astete SG, Mandaliya K, Totten PA. High Mycoplasma genitalium organism burden is associated with shedding of HIV-1 DNA from the cervix. J Infect Dis 2008; 197:733-6.
34. Cohen CR, Mugo NR, Astete SG, et al. Detection of Mycoplasma genitalium in women with laparoscopically diagnosed acute salpingitis. Sex Transm Infect 2005; 81:463-6.
35. Moller BR, Taylor-Robinson D, Furr PM. Serological evidence implicating Mycoplasma genitalium in pelvic inflammatory disease. Lancet 1984; 1:1102-3.
36. Haggerty CL, Totten PA, Astete SG, Ness RB. Mycoplasma genitalium among women with nongonococcal, nonchlamydial pelvic inflammatory disease. Infect Dis Obstet Gynecol 2006; 2006:30184.
37. Short VL, Totten PA, Ness RB, Astete SG, Kelsey SF, Haggerty CL. Clinical presentation of Mycoplasma genitalium infection versus Neisseria gonorrhoeae infection among women with pelvic inflammatory disease. Clin Infect Dis 2009; 48:41-7.
38. Short VL, Jensen JS, Nelson DB, Murray PJ, Ness RB, Haggerty CL. Mycoplasma genitalium among young, urban pregnant women. Infect Dis Obstet Gynecol 2010; 2010:984760.
39. Taylor BD, Ness RB, Darville T, Haggerty CL. Microbial correlates of delayed care for pelvic inflammatory disease. Sex Transm Dis 2011; 38:434-8.
40. Simms I, Eastick K, Mallinson H, et al. Associations between Mycoplasma genitalium, Chlamydia trachomatis and pelvic inflammatory disease. J Clin Pathol 2003; 56:616-8.
41. Jurstrand M, Jensen JS, Magnuson A, Kamwendo F, Fredlund H. A serological study of the role of Mycoplasma genitalium in pelvic inflammatory disease and ectopic pregnancy. Sex Transm Infect 2007; 83:319-23.
42. Haggerty CL, Totten PA, Astete SG, et al. Failure of cefoxitin and doxycycline to eradicate endometrial Mycoplasma genitalium and the consequence for clinical cure of pelvic inflammatory disease. Sex Transm Infect 2008; 84:338-42.
43. Bjartling C, Osser S, Persson K. The association between Mycoplasma genitalium and pelvic inflammatory disease after termination of pregnancy. BJOG 2010; 117:361-4.
44. Lind K, Kristensen GB. Significance of antibodies to Mycoplasma genitalium in salpingitis. Eur J Clin Microbiol 1987; 6:205-7.
45. Taylor-Robinson D, Jensen JS, Svenstrup H, Stacey CM. Difficulties experienced in defining the microbial cause of pelvic inflammatory disease. Int J STD AIDS 2012; 23:18-24.
46. Cohen CR, Manhart LE, Bukusi EA, et al. Association between Mycoplasma genitalium and acute endometritis. Lancet 2002; 359:65-6.
47. Simms I, Eastick K, Mallinson H, et al. Associations between Mycoplasma genitalium, Chlamydia trachomatis, and pelvic inflammatory disease. Sex Transm Infect 2003; 79:154-6.
48. Oakeshott P, Aghaizu A, Hay P, et al. Is Mycoplasma genitalium in women the new chlamydia? A community-based prospective cohort study. Clin Infect Dis 2010; 51:1160-6.
49. Romero R, Kusanovic JP, Gomez R, et al. The clinical significance of eosinophils in the amniotic fluid in preterm labor. JMatern Fetal Neonatal Med 2010; 23:320-9.
50. Lu GC, Schwebke JR, Duffy LB, et al. Midtrimester vaginal Mycoplasma genitalium in women with subsequent spontaneous preterm birth. Am J Obstet Gynecol 2001; 185:163-5.
51. Choi SJ, Park SD, Jang IH, Uh Y, Lee A. The prevalence of vaginal microorganisms in pregnant women with preterm labor and preterm birth. Ann Lab Med 2012; 32:194-200.
52. Haghighi Hasanabad M, Mohammadzadeh M, Bahador A, Fazel N, Rakhshani H, Majnooni A. Prevalence of Chlamydia trachomatis and Mycoplasma genitalium in pregnant women of Sabzevar-Iran. Iran J Microbiol 2011; 3:123-8.
53. Edwards RK, Ferguson RJ, Reyes L, Brown M, Theriaque DW, Duff P. Assessing the relationship between preterm delivery and various microorganisms recovered from the lower genital tract. J Matern Fetal Neonatal Med 2006; 19:357-63.
54. Hitti J, Garcia P, Totten P, Paul K, Astete S, Holmes KK. Correlates of cervical Mycoplasma genitalium and risk of preterm birth among Peruvian women. Sex Transm Dis 2010; 37:81-5.
55. Kataoka S, Yamada T, Chou K, et al. Association between preterm birth and vaginal colonization by mycoplasmas in early pregnancy. J Clin Microbiol 2006; 44:51-5.
56. Labbe AC, Frost E, Deslandes S, Mendonca AP, Alves AC, Pepin J. Mycoplasma genitalium is not associated with adverse outcomes of pregnancy in Guinea-Bissau. Sex Transm Infect 2002; 78:289-91.
57. Oakeshott P, Hay P, Taylor-Robinson D, et al. Prevalence of Mycoplasma genitalium in early pregnancy and relationship between its presence and pregnancy outcome. BJOG 2004; 111:1464-7.
58. Averbach SH, Hacker MR, Yiu T, Modest AM, Dimitrakoff J, Ricciotti HA. Mycoplasma genitalium and preterm delivery at an urban community health center. Int J Gynaecol Obstet 2013; 123:54-7.
59. Vandepitte J, Muller E, Bukenya J, et al. Prevalence and correlates of Mycoplasma genitalium infection among female sex workers in Kampala, Uganda. J Infect Dis 2012; 205:289-96.
60. Tomusiak A, Heczko PB, Janeczko J, Adamski P, Pilarczyk-Zurek M, Strus M. Bacterial infections of the lower genital tract in fertile and infertile women from the southeastern Poland. Ginekol Pol 2013; 84:352-8.
61. Costoya A, Morales F, Borda P, et al. Mycoplasmateceae species are not found in Fallopian tubes of women with tubo-peritoneal infertility. Braz J Infect Dis 2012; 16:273-8.
62. Clausen HF, Fedder J, Drasbek M, et al. Serological investigation of Mycoplasma genitalium in infertile women. Hum Reprod 2001; 16: 1866-74.
63. Svenstrup HF, Fedder J, Kristoffersen SE, Trolle B, Birkelund S, Christiansen G. Mycoplasma genitalium, Chlamydia trachomatis, and tubal factor infertility-a prospective study. Fertil Steril 2008; 90:513-20.
64. Moller BR, Taylor-Robinson D, Furr PM, Toft B, Allen J. Serological evidence that chlamydiae and mycoplasmas are involved in infertility of women. J Reprod Fertil 1985; 73:237-40.
65. Grzesko J, Elias M, Maczynska B, Kasprzykowska U, Tlaczala M, Goluda M. Occurrence of Mycoplasma genitalium in fertile and infertile women. Fertil Steril 2009; 91:2376-80.
66. Arraiz RN, Colina Ch S, Marcucci JR, et al. Mycoplasma genitalium detection and correlation with clinical manifestations in population of the Zulia State, Venezuela [in Spanish]. Rev Chilena Infectol 2008; 25:256-61.
67. Holmes KK, Sparling PF, Stamm WE, et al. Sexually transmitted diseases. 4th ed. McGraw-Hill, 2008.
68. Paavonen J, Westrom L, Eschenbach DA. Pelvic inflammatory disease. In: Holmes KK, Sparling PF, Stamm WE, et al. eds. Sexually transmitted diseases. 4th ed. New York: McGraw-Hill, 2008:1017-50.
69. Trent M, Ellen JM, Frick KD. Estimating the direct costs of pelvic inflammatory disease in adolescents: a within-system analysis. Sex Transm Dis 2011; 38:326-8.
70. Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines 2010. Atlanta, GA: Division of STD Prevention, 2011.
71. Centers for Disease Control and Prevention. National prematurity awareness month. Available at: http://www.cdc.gov/Features/Pre matureBirth/. Accessed 16 May 2014.
72. Silver BJ, Guy RJ, Kaldor JM, Jamil MS, Rumbold AR. Trichomonas vaginalis as a cause of perinatal morbidity: a systematic review and metaanalysis. Sex Transm Dis 2014; 41:369-76.
73. Centers for Disease Control and Prevention. STD surveillance, 2010-chlamydia. Available at: http://www.cdc.gov/std/stats10/chlamydia.htm. Accessed 8 January 2014.
74. Centers for Disease Control and Prevention. Reproductive health: infertility FAQs. Available at: http://www.cdc.gov/reproductivehealth/ Infertility/index.htm. Accessed 16 May 2014.
75. Manhart LE, Gillespie CW, Lowens MS, et al. Standard treatment regimens for nongonococcal urethritis have similar but declining cure rates: a randomized controlled trial. Clin Infect Dis 2013; 56:934-42.
76. Mena LA, Mroczkowski TF, Nsuami M, Martin DH. A randomized comparison of azithromycin and doxycycline for the treatment of Mycoplasma genitalium-positive urethritis in men. Clin Infect Dis 2009; 48:1649-54.
77. Hardick A, Hardick J, Wood BJ, Gaydos C. Comparison between the Gen-Probe transcription-mediated amplification Trichomonas vaginalis research assay and real-time PCR for Trichomonas vaginalis detection using a Roche LightCycler instrument with female self-obtained vaginal swab samples and male urine samples. J Clin Microbiol 2006; 44:4197-9.
78. Wroblewski JK, Manhart LE, Dickey KA, Hudspeth MK, Totten PA. Comparison of transcription-mediated amplification and PCR assay results for various genital specimen types for detection of Mycoplasma genitalium. J Clin Microbiol 2006; 44:3306-12.
79. Hologic. Customer support. Available at: http://www.hologic.com/ support. Accessed 6 April 2015.
80. Wiesenfeld HC, Mancuso M, Hillier SL, Amortegui A, Sweet RL. The association between Mycoplasma genitalium and subclinical pelvic inflammatory disease. In: International Society for Sexually Transmitted Disease Research 2009. Abstract P3.36.
81. Wiesenfeld HC, Hiller SL, Meyn L, et al. Mycoplasma genitalium-is it a pathogen in acute pelvic inflammatory disease (PID)? Sex Transm Infect 2013; 89(suppl 1):A34.