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Sequelae/long-term outcomes

After one episode of PID, a significant proportion of women, up to one in four, will experience long-term complications including infertility, ectopic pregnancy, and chronic pelvic pain (defined as pain lasting >6 months).

After repeated episodes, this proportion increases to almost one in two. This was first shown in the seminal paper by Westrom et al. who reported on the long-term reproductive outcomes for 1844 women with abnormal laparoscopies. These in­dividuals were followed up for a total of 13,400 woman-years, and compared to 657 women with normal laparoscopy (controls) fol­lowed for 3,958 woman-years (71). Of these women, 16% of the pa­tients and 2.7% of controls failed to conceive. A total of 10.8% of patients and 0% of controls had confirmed tubal factor infertility. Each repeated episode of PID doubled the rate of tubal factor infer­tility. After one episode, the rate was 8%, increasing to 19.5% after two episodes, and 40% after three or more episodes of PID. The ec­topic pregnancy rate for first pregnancy was 9.1% among patients and 1.4% in control subjects (P Charlett A. The rate of diagnosis and demog­raphy of pelvic inflammatory disease in general practice: England and Wales. Int J STD AIDS 1999;10:448-51.

7. Public Health England. Rates of pelvic inflammatory disease (PID) in England (2000-2013). HPR 2015;9:22.

8. Centers for Disease Control and Prevention. Pelvic inflamma­tory disease—initial visits to physicians’ offices among women aged 15-44 years, United States, 2004-2013. Sexually Transmitted Disease Surveillance 2014. Available at: http://www.cdc.gov/std/ stats14/figures/e.htm. (Accessed 16th July 2019).

9. Rekart, ML, Gilbert, M, Meza, R, et al. Chlamydia public health programs and the epidemiology of pelvic inflammatory disease and ectopic pregnancy. JInfectDis 2013;207:30-38.

10. Bender N, Herrmann B, Andersen B, et al.

Chlamydia infec­tion, pelvic inflammatory disease, ectopic pregnancy and infer­tility: cross-national study. Sex Transm Infect 2011;87:601-608.

11. Burnett AM, Anderson CP, Zwank MD. Laboratory-confirmed gon­orrhea and/or chlamydia rates in clinically diagnosed pelvic inflam­matory disease and cervicitis. Am J Emerg Med 2012;30:1114-17.

12. Trent M, Bass D, Ness RB, Haggerty C. Recurrent PID, subse­quent STI, and reproductive health outcomes: findings from the PID evaluation and clinical health (PEACH) study. Sex Transm Dis 2011;38:879-81.

13. Sweet RL. Treatment of acute pelvic inflammatory disease. Infect Dis Obstet Gynecol 2011;2011:561909.

14. Ness RB, Hillier SL, Kip KE, et al. Douching, pelvic inflammatory disease, and incident gonococcal and chlamydial genital infection in a cohort of high-risk women. Am JEpidemiol 2005;161:186-95.

15. McCormack W Pelvic inflammatory disease. N Engl J Med 1994;330:115-19.

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17. Bevan CD, Johal BJ, Mumtaz G, Ridgway GL, Siddle NC. Clinical, laparoscopic and microbiological findings in acute salpin­gitis: report on a United Kingdom cohort. Br J Obstet Gynaecol 1995;102:407-14.

18. Soper DE, Brockwell NJ, Dalton HP, Johnson D. Observations concerning the microbial etiology of acute salpingitis. Am J Obstet Gynecol 1994;170:1008-14.

19. Price MJ, Ades AE, Soldan K, et al. The natural history of Chlamydia trachomatis infection in women: a multi-parameter evidence synthesis. Health Technol Assess 2016;20:1-250.

20. Taylor BD, Darville T, Haggerty CL. Does bacterial vaginosis cause pelvic inflammatory disease? Sex Transm Dis 2013;40:117-22.

21. Walker CK, Workowski KA, Washington AE, Soper D, Sweet R. Anaerobes in pelvic inflammatory disease: implications for the Centers for Disease Control and Prevention’s guidelines for treat­ment of sexually transmitted diseases.

Clin Infect Dis 1999;28 Suppl 1:S29-36.

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23. Ness RB, Kip KE, Hillier SL, et al. A cluster analysis of bacterial vaginosis-associated microflora and pelvic inflammatory disease. Am JEpidemiol 2005;162:585-90.

24. Hillier SL, Kiviat NB, Hawes SE, et al. Role of bacterial vaginosis- associated microorganisms in endometritis. Am J Obstet Gynecol 1996;175:435-41.

25. Haggerty CL, Hillier SL, Bass DC, Ness RB. Bacterial vaginosis and anaerobic bacteria are associated with endometritis. Clin Infect Dis 2004;39:990-95.

26. Lareau SM, Beigi RH. Pelvic inflammatory disease and tubo- ovarian abscess. Infect Dis Clin North Am 2008;22:693-708.

27. Hjorth SV, Bjornelius E, Lidbrink P, et al. Sequence-based typing of Mycoplasma genitalium reveals sexual transmission. J Clin Microbiol 2006;44:2078-83.

28. 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.

29. Haggerty CL, Taylor BD. Mycoplasma genitalium: an emerging cause of pelvic inflammatory disease. Infect Dis Obstet Gynecol 2011;2011:959816.

30. Cohen CR, Manhart LE, Bukusi EA, et al. Association be­tween Mycoplasma genitalium and acute endometritis. Lancet 2002;359:765-66.

31. Lis R, Rowhani-Rahbar A, Manhart LE. Mycoplasma genitalium infection and female reproductive tract disease: a meta-analysis. Clin InfectDis 2015;61:418-26.

32. Geisler WM. Duration of untreated, uncomplicated Chlamydia trachomatis genital infection and factors associated with chla­mydia resolution: a review of human studies. J Infect Dis 2010;201 Suppl 2;S104-13.

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34. Kunz G, Leyendecker G. Uterine peristaltic activity during the menstrual cycle: characterization, regulation, function and dys­function.

ReprodBiomed Online 2002; 4 Suppl 3:5-9.

35. Taylor BD, Darville T, Tan C, Bavoil PM, Ness RB, Haggerty CL. The role of chlamydia trachomatis polymorphic membrane proteins in inflammation and sequelae among women with pelvic inflam­matory disease. InfectDis Obstet Gynecol 2011;2011:989762.

36. Tuffrey M, Alexander F, Taylor Robinson D. Severity of sal­pingitis in mice after primary and repeated inoculation with a human strain of Chlamydia trachomatis. J Exp Pathol (Oxford) 1990;71:403-10.

37. Lanjouw E, Ouburg S, de Vries HJ, Stary, A, Radcliffe K, Unemo M. Background review for the 2015 European guideline on the management of Chlamydia trachomatis infections. Int J STD AIDS 2015;Nov 24:0956462415618838.

38. Miettinen A, Heinonen PK, Teisala K, Hakkarainen K, Punnonen R. Serologic evidence for the role of Chlamydia trachomatis, Neisseria gonorrhoeae, and Mycoplasma hominis in the etiology of tubal factor infertility and ectopic pregnancy. Sex Transm Dis 1990;17:10-14.

39. Wiesenfeld HC, Hillier SL, Meyn LA, Amortegui AJ, Sweet RL. Subclinical PID and infertility. Obstet Gynecol 2012;120:37-43.

40. Ross J, Judlin P, Jensen J. 2012 European guideline for the manage­ment ofpelvic inflammatory disease. Int J STD AIDS 2014;25:1-22.

41. Miettinen AK, Heinonen PK, Laippala P, Paavonen J. Test per­formance of erythrocyte sedimentation rate and C-reactive pro­tein in assessing the severity of acute pelvic inflammatory disease. Am J Obstet Gynecol 1993;169:1143-49.

42. Yudin MH, Hillier SL, Wiesenfeld HC, Krohn MA, Amortegui AA, Sweet RL. Vaginal polymorphonuclear leukocytes and bac­terial vaginosis as markers for histologic endometritis among women without symptoms of pelvic inflammatory disease. Am J Obstet Gynecol 2003;188:318-23.

43. Short VL, Totten PA, Ness RB, Astete SG, Sheryl F, Haggerty CL. Clinical presentation of Mycoplasma genitalium infection versus Neisseria gonorrhoeae infection among women with pelvic in­flammatory disease.

Clin InfectDis 2010;48:41-47.

44. Peipert JF, Ness RB, Blume J, et al. Clinical predictors of endomet­ritis in women with symptoms and signs of pelvic inflammatory disease. Am J Obstet Gynecol 2001;184:856-63.

45. Eschenbach DA, Wolner-Hanssen P, Hawes SE, Pavletic A, Paavonen J, Holmes KK. Acute pelvic inflammatory disease: as­sociations of clinical and laboratory findings with laparoscopic findings. Obstet Gynecol 1997;89:184-92.

46. Simms I, Warburton F, Westrom L. Diagnosis of pelvic inflamma­tory disease: time for a rethink. Sex Transm Infect 2003;79:491-94.

47. Taylor BD, Ness RB, Darville T, Haggerty CL. Microbial correlates of delayed care for pelvic inflammatory disease. Sex Transm Dis 2011;38:434-38.

48. Brunham R, Gottlieb SL, Paavonen J. Pelvic inflammatory disease. N Engl J Med 2015;372:2039-48.

49. Morris GC, Stewart CMW, Schoeman SA, Wilson JD. A cross-sec­tional study showing differences in the clinical diagnosis of pelvic inflammatory disease according to the experience of clinicians: im­plications for training and audit. Sex Transm Infect 2014;90:445-51.

50. Jaiyeoba O, Soper DE. A practical approach to the diagnosis of pelvic inflammatory disease. Infect Dis Obstet Gynecol 2011;2011:753037.

51. Hemila M, Henriksson L, Ylikorkala O. Serum CRP in the diag­nosis and treatment of pelvic inflammatory disease. Arch Gynecol Obstet 1987;241:177-82.

52. Cacciatore B, Leminen A, Ingman-Friberg S, Ylostalo P, Paavonen J. Transvaginal sonographic findings in ambulatory patients with sus­pected pelvic inflammatory disease. Obstet Gynecol 1992;80:912-16.

53. Molander P, Sjoberg J, Paavonen J, Cacciatore B. Transvaginal power Doppler findings in laparoscopically proven acute pelvic inflammatory disease. Ultrasound Obstet Gynecol 2001;17:233-38.

54. Tukeva TA, Aronen HJ, Karjalainen PT, Molander P, Paavonen T, Paavonen J. MR imaging in pelvic inflammatory disease: com­parison with laparoscopy and US. Radiology 1999;210:209-16.

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57. Kivia, NB, Wolner-Hanssen P, Eschenbach DA, et al. Endometrial histopathology in patients with culture-proved upper genital tract infection and laparoscopically diagnosed acute salpingitis. Am J Surg Pathol 1990;14:167-75.

58. Mitchell C, Prabhu M. Pelvic inflammatory disease: current con­cepts in pathogenesis, diagnosis and treatment. Infect Dis Clin North Am 2013;27:793-809.

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60. Hillis SD, Joesoef R, Marchbanks PA, Wasserheit JN, Cates W, Westrom L. Delayed care of pelvic inflammatory dis­ease as a risk factor for impaired fertility. Am J Obstet Gynecol 1993;168:1503-509.

61. Dunbar-Jacob J, Sereika SM, Foley SM, Bass DC, Ness RB. Adherence to oral therapies in pelvic inflammatory disease. J Womens Health 2004;13:285-91.

62. European Medicines Agency. Disabling and potentially permanent side effects lead to suspension or restrictions of quinolone and fluoro­quinolone antibiotics. EMA/175398/2019. (https://www.ema.europa. eu/en/medicines/human/referrals/quinolone-fluoroquinolone- containing-medicinal-products). Accessed 16th July 2019.

63. 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.

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65. Bissessor M, Tabrizi SN, Twin J, et al. Macrolide resistance and azithromycin failure in a mycoplasma genitalium-infected cohort and response of azithromycin failures to alternative antibiotic re­gimens. Clin Infect Dis 2015;60:1228-36.

66. Reed SD, Landers DV, Sweet RL. Antibiotic treatment of tuboovarian abscess: comparison of broad-spectrum beta-lactam agents versus clindamycin-containing regimens. Am J Obstet Gynecol 1991;164:1556-61.

67. Gjelland K, Ekerhovd E, Granberg S. Transvaginal ultrasound- guided aspiration for treatment of tubo-ovarian abscess: a study of 302 cases. Am J Obstet Gynecol 2005;193:1323-30.

68. Cohen CR, Sinei S, Reilly M et al. Effect of human immunodefi­ciency virus type 1 infection upon acute salpingitis: a laparoscopic study. J Infect Dis 1998;178:1352-58.

69. Mugo NR, Kiehlbauch JA, Nguti R, et al. Effect of human im­munodeficiency virus-1 infection on treatment outcome of acute salpingitis. Obstet Gynecol 2006;107:807-12.

70. Farley TM, Rosenberg MJ, Rowe PJ, Chen JH, Meirik O. Intrauterine devices and pelvic inflammatory disease. Lancet 1992;3:280-87.

71. Centers for Disease Control and Prevention. U.S. Selected prac­tice recommendations for contraceptive use, 2013: adapted from

the World Health Organization Selected Practice Recommenda­tions for Contraceptive Use, 2nd edition. June 21, 2013. Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/rr6205a1.

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72. Tepper NK, Steenland MW, Gaffield ME, Marchbanks PA, Curtis KM. Retention of intrauterine devices in women who acquire pelvic inflammatory disease: a systematic review. Contraception 2013;87:655-60.

73. Westrom L, Joesoef R, Reynolds G, Hagdu A, Thompson SE. Pelvic inflammatory disease and fertility. A cohort study of 1,844 women with laparoscopically verified disease and 657 con­trol women with normal laparoscopic results. Sex Transm Dis 1992;19:185-92.

74. Ness RB, Trautmann G, Richter HE, et al. Effectiveness of treat­ment strategies of some women with pelvic inflammatory dis­ease: a randomized trial. Obstet Gynecol 2005;106:573-80.

75. Scholes D, Stergachis A, Heidrich F, Andrilla H, Holmes KK, Stamm W. Prevention of pelvic inflammatory disease by screening for cervical chlamydial infection. N Engl J Med. 1998;334:1362-66.

76. Ostergaard L, Andersen B, Moller JK, Olesen F. Home sampling versus conventional swab sampling for screening of Chlamydia trachomatis in women: a cluster-randomized 1-year follow-up study. Clin InfectDis 2000;31:951-57.

77. Oakeshott P, Kerry S, Aghaizu A et al. Randomised controlled trial of screening for Chlamydia trachomatis to prevent pelvic inflam­matory disease: the POPI (prevention of pelvic infection) trial. BMJ (Clin Res Ed) 2010;340:c1642.

78. Trent M, Chung S, Burke M, Walker A, Ellen JM. Results of a randomized controlled trial of a brief behavioral intervention for pelvic inflammatory disease in adolescents. J Pediatr Adolesc Gynecol 2010;23:96-101.

79. Ness RB, Randall H, Richter HE, et al. Condom use and the risk of recurrent pelvic inflammatory disease, chronic pelvic pain, or in­fertility following an episode of pelvic inflammatory disease. Am J Public Health 2004;94:1327-29.

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Source: Arulkumaran S., Ledger W., Denny L., Doumouchtsis S. (eds.). Oxford Textbook of Obstetrics and Gynaecology. Oxford University Press,2020. — 928 p.. 2020
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