Pelvic inflammatory disease: pathogenesis, microbiology, and risk factors
- Jonathan Ross, MD
Jonathan Ross, MD
- Professor of Sexual Health and HIV
- Department of GU Medicine
- University Hospitals Birmingham NHS Foundation Trust
Pelvic inflammatory disease (PID) refers to acute infection of the upper genital tract structures in women, involving any or all of the uterus, oviducts, and ovaries; this is often accompanied by involvement of the neighboring pelvic organs. By convention, PID is initiated by a sexually transmitted agent, which ascends into the upper genital tract, distinguishing it from pelvic infections caused by trans-cervical medical procedures, pregnancy, and other primary abdominal processes that can extend to pelvic organs.
Overall, the prevalence of PID in the United States and many other resource-rich countries has decreased in the last decade [1,2]. In the United States, PID accounts for approximately 106,000 outpatient visits and 60,000 hospitalizations each year, and is a frequent cause for emergency department visits . Each woman with PID costs around $2000 USD to treat, rising to $6000 if she develops chronic pelvic pain .
The pathogenesis and microbiology of PID as well as risk factors for PID will be reviewed here. The clinical features, diagnosis, treatment, and sequelae of this disorder are discussed separately. (See "Clinical features and diagnosis of pelvic inflammatory disease" and "Treatment of pelvic inflammatory disease".)
The vaginal flora of most normal, healthy women includes a variety of potentially pathogenic bacteria . Among these are species of streptococci, staphylococci, Enterobacteriaceae (most commonly Klebsiella spp, Escherichia coli, and Proteus spp), and a variety of anaerobes. Compared with the dominant, non-pathogenic, hydrogen peroxide-producing Lactobacillus species, these other organisms are present in low numbers, and ebb and flow under the influence of hormonal changes (eg, pregnancy, menstrual cycle), contraceptive method, sexual activity, and other as yet unknown forces.
The endocervical canal functions as a barrier protecting the normally sterile upper genital tract from the organisms of the dynamic vaginal ecosystem. Endocervical infection with sexually transmitted pathogens can disrupt this barrier. Disturbance of this barrier provides vaginal bacteria access to the upper genital organs, infecting the endometrium, then endosalpinx, ovarian cortex, pelvic peritoneum, and their underlying stroma. The resulting infection may be subclinical or manifest as the clinical entity of pelvic inflammatory disease (PID). The reasons why lower genital tract bacteria cause PID in some women but not others is not fully understood but may relate to genetic variations in immune response, estrogen levels affecting the viscosity of cervical mucus, and bacterial load [5,6].
- Centers for Disease Control and Prevention (CDC). Pelvic Inflammatory Disease (PID). http://www.cdc.gov/std/pid/stats.htm (Accessed on January 05, 2015).
- French CE, Hughes G, Nicholson A, et al. Estimation of the rate of pelvic inflammatory disease diagnoses: trends in England, 2000-2008. Sex Transm Dis 2011; 38:158.
- Yeh JM, Hook EW 3rd, Goldie SJ. A refined estimate of the average lifetime cost of pelvic inflammatory disease. Sex Transm Dis 2003; 30:369.
- Galask RP, Larsen B, Ohm MJ. Vaginal flora and its role in disease entities. Clin Obstet Gynecol 1976; 19:61.
- Morré SA, Karimi O, Ouburg S. Chlamydia trachomatis: identification of susceptibility markers for ocular and sexually transmitted infection by immunogenetics. FEMS Immunol Med Microbiol 2009; 55:140.
- Ness RB, Kip KE, Hillier SL, et al. A cluster analysis of bacterial vaginosis-associated microflora and pelvic inflammatory disease. Am J Epidemiol 2005; 162:585.
- Molander P, Finne P, Sjöberg J, et al. Observer agreement with laparoscopic diagnosis of pelvic inflammatory disease using photographs. Obstet Gynecol 2003; 101:875.
- Gaitán H, Angel E, Diaz R, et al. Accuracy of five different diagnostic techniques in mild-to-moderate pelvic inflammatory disease. Infect Dis Obstet Gynecol 2002; 10:171.
- Rendtroff RC, Curran JW, Chandler RW, et al. Economic consequences of gonorrhea in women: experience from an Urban hospital. J Am Vener Dis Assoc 1974; 1:40.
- Forslin L, Falk V, Danielsson D. Changes in the incidence of acute gonococcal and nongonococcal salpingitis. A five-year study from an urban area of central Sweden. Br J Vener Dis 1978; 54:247.
- Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance 2013. Atlanta: U.S. Department of Health and Human Services; 2014. http://www.cdc.gov/std/stats13/default.htm (Accessed on January 21, 2015).
- HIV and Sexually Transmitted Infections Department. STI diagnoses and rates in England by gender, 2004-2013. Public Health England, 2014. https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/340430/Table_1_STI_diagnoses_and_rates_in_England_by_gender.pdf (Accessed on January 21, 2015).
- Mosure DJ, Berman S, Fine D, et al. Genital Chlamydia infections in sexually active female adolescents: do we really need to screen everyone? J Adolesc Health 1997; 20:6.
- Scholes D, Stergachis A, Heidrich FE, et al. Prevention of pelvic inflammatory disease by screening for cervical chlamydial infection. N Engl J Med 1996; 334:1362.
- National Chlamydia Screening Programme. http://www.chlamydiascreening.nhs.uk/ (Accessed on January 05, 2015).
- U.S. Preventive Services Task Force (USPSTF). http://www.uspreventiveservicestaskforce.org/Page/Name/tools-and-resources-for-better-preventive-care (Accessed on January 05, 2015).
- Hebb JK, Cohen CR, Astete SG, et al. Detection of novel organisms associated with salpingitis, by use of 16S rDNA polymerase chain reaction. J Infect Dis 2004; 190:2109.
- Eschenbach DA, Buchanan TM, Pollock HM, et al. Polymicrobial etiology of acute pelvic inflammatory disease. N Engl J Med 1975; 293:166.
- Thompson SE 3rd, Hager WD, Wong KH, et al. The microbiology and therapy of acute pelvic inflammatory disease in hospitalized patients. Am J Obstet Gynecol 1980; 136:179.
- Chow AW, Malkasian KL, Marshall JR, Guze LB. The bacteriology of acute pelvic inflammatory disease. Am J Obstet Gynecol 1975; 122:876.
- Sweet RL, Draper DL, Hadley WK. Etiology of acute salpingitis: influence of episode number and duration of symptoms. Obstet Gynecol 1981; 58:62.
- Soper DE, Brockwell NJ, Dalton HP, Johnson D. Observations concerning the microbial etiology of acute salpingitis. Am J Obstet Gynecol 1994; 170:1008.
- Sweet RL, Mills J, Hadley KW, et al. Use of laparoscopy to determine the microbiologic etiology of acute salpingitis. Am J Obstet Gynecol 1979; 134:68.
- Stemmer W. Uber die ursachen von eileiterentzundungen. Gentral fur Gynnak 1941; 65:1062.
- Leichliter JS, Chandra A, Aral SO. Correlates of self-reported pelvic inflammatory disease treatment in sexually experienced reproductive-aged women in the United States, 1995 and 2006-2010. Sex Transm Dis 2013; 40:413.
- Lee NC, Rubin GL, Grimes DA. Measures of sexual behavior and the risk of pelvic inflammatory disease. Obstet Gynecol 1991; 77:425.
- Flesh G, Weiner JM, Corlett RC Jr, et al. The intrauterine contraceptive device and acute salpingitis: a multifactor analysis. Am J Obstet Gynecol 1979; 135:402.
- Rein MF. Epidemiology of gonococcal infection. In: The Gonococcus, Roberts RB (Ed), Wiley and Sons, New York 1977. p.1.
- Westrom, L, Mardh PA. Epidemiology, etiology, and prognosis of acute salpingitis: A study of 1,457 laparoscopically verified cases. In: Nongonococcal Urethritis and Related Diseases, Hobson D, Holmes KK (Eds), Am Soc Microbiol, Washington DC 1977. p.84.
- Weström L. Incidence, prevalence, and trends of acute pelvic inflammatory disease and its consequences in industrialized countries. Am J Obstet Gynecol 1980; 138:880.
- Sonnenberg P, Clifton S, Beddows S, et al. Prevalence, risk factors, and uptake of interventions for sexually transmitted infections in Britain: findings from the National Surveys of Sexual Attitudes and Lifestyles (Natsal). Lancet 2013; 382:1795.
- Jackson SL, Soper DE. Pelvic inflammatory disease in the postmenopausal woman. Infect Dis Obstet Gynecol 1999; 7:248.
- Hillis SD, Nakashima A, Marchbanks PA, et al. Risk factors for recurrent Chlamydia trachomatis infections in women. Am J Obstet Gynecol 1994; 170:801.
- Weström L. Effect of acute pelvic inflammatory disease on fertility. Am J Obstet Gynecol 1975; 121:707.
- Eschenbach DA, Harnisch JP, Holmes KK. Pathogenesis of acute pelvic inflammatory disease: role of contraception and other risk factors. Am J Obstet Gynecol 1977; 128:838.
- 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.
- Gavin L, MacKay AP, Brown K, et al. Sexual and reproductive health of persons aged 10-24 years - United States, 2002-2007. MMWR Surveill Summ 2009; 58:1.
- Louv WC, Austin H, Perlman J, Alexander WJ. Oral contraceptive use and the risk of chlamydial and gonococcal infections. Am J Obstet Gynecol 1989; 160:396.
- Rubin GL, Ory HW, Layde PM. Oral contraceptives and pelvic inflammatory disease. Am J Obstet Gynecol 1982; 144:630.
- Ness RB, Keder LM, Soper DE, et al. Oral contraception and the recognition of endometritis. Am J Obstet Gynecol 1997; 176:580.
- Wølner-Hanssen P, Svensson L, Mårdh PA, Weström L. Laparoscopic findings and contraceptive use in women with signs and symptoms suggestive of acute salpingitis. Obstet Gynecol 1985; 66:233.
- Centers for Disease Control and Prevention, Workowski KA, Berman SM. Sexually transmitted diseases treatment guidelines, 2006. MMWR Recomm Rep 2006; 55:1.
- Lee NC, Rubin GL, Borucki R. The intrauterine device and pelvic inflammatory disease revisited: new results from the Women's Health Study. Obstet Gynecol 1988; 72:1.
- Grimes DA. Intrauterine device and upper-genital-tract infection. Lancet 2000; 356:1013.
- Altunyurt S, Demir N, Posaci C. A randomized controlled trial of coil removal prior to treatment of pelvic inflammatory disease. Eur J Obstet Gynecol Reprod Biol 2003; 107:81.
- Centers for Disease Control. Sexually Transmitted Diseases Treatment Guidelines 2010. http://www.cdc.gov/std/treatment/2010/default.htm.
- Ross J, Judlin P, Jensen J, International Union against sexually transmitted infections. 2012 European guideline for the management of pelvic inflammatory disease. Int J STD AIDS 2014; 25:1.
- Lee YC, Min D, Holcomb K, et al. Computed tomography guided core needle biopsy diagnosis of pelvic actinomycosis. Gynecol Oncol 2000; 79:318.
- Hall V, Talbot PR, Stubbs SL, Duerden BI. Identification of clinical isolates of actinomyces species by amplified 16S ribosomal DNA restriction analysis. J Clin Microbiol 2001; 39:3555.
- Fleury FJ. Adult vaginitis. Clin Obstet Gynecol 1981; 24:407.
- Ness RB, Hillier SL, Kip KE, et al. Bacterial vaginosis and risk of pelvic inflammatory disease. Obstet Gynecol 2004; 104:761.
- Neisseria gonorrhoeae
- Chlamydia trachomatis
- Mycoplasma genitalium
- Other initiating pathogens
- Mixed infection
- RISK FACTORS
- Multiple partners
- STI in the partner
- Previous PID
- Contraceptive method
- - Barrier contraception
- - Oral contraceptives
- - Intrauterine device and tubal ligation
- Other conditions
- INFORMATION FOR PATIENTS
- SUMMARY AND RECOMMENDATIONS