Brazilian Protocol for Sexually Transmitted infections, 2020: pelvic inflammatory disease

Maria Luiza Bezerra Menezes Paulo Cesar Giraldo Iara Moreno Linhares Neide Aparecida Tosato Boldrini Mayra Gonçalves Aragon About the authors

Highlighted excerpt:

Pelvic inflammatory disease is one of the most significant sexually transmitted infections, and in most cases, it is a main consequence of cervicitis.

Abstract

Pelvic Inflammatory Disease is a topic included in the Clinical Protocol and Therapeutic Guidelines for Comprehensive Care for People with Sexually Transmitted Infections, published by the Brazilian Ministry of Health in 2020. Pelvic inflammatory disease is an upper female genital tract acute infection due to canalicular spread of endogenous cervicovaginal microorganisms and especially the sexually transmitted microorganisms. Standing out among the etiological agents involved are Chlamydia trachomatis and Neisseria gonorrhoeae. The main sequelae are chronic pelvic pain, infertility, and ectopic pregnancy. Clinical diagnosis is the most important practical approach. Antibiotic treatment must start immediately after the clinical suspicion. Guidelines for health service managers and health professionals on diagnostic tests, treatment, follow-up, counseling, notification, handling sexual partners and special populations are described. Given the increased availability of the molecular biology techniques in Brazil, C. trachomatis and N. gonorrhoeae screening are recommended as a disease prevention strategy.

Keywords:
Pelvic infection; Pelvic pain; Ectopic pregnancy; Infertility; Chlamydia trachomatis; Neisseria gonorrhoeae

FOREWORD

This article addresses pelvic inflammatory disease, included in the Clinical Protocol and Therapeutic Guidelines (PCDT) for Comprehensive Care for People with Sexually Transmitted Infections (STI), published by the Health Surveillance Secretariat of the Brazilian Ministry of Health. For the development of the PDCT, selection and analysis of available evidence were performed, followed by discussions with specialists. The PDCT was approved by the National Committee for Technology Incorporation to the Brazilian National Health System (Conitec)11. Brasil. Ministério da Saúde. Portaria MS/SCTIE nº 42, de 5 de outubro de 2018. Torna pública a decisão de aprovar o Protocolo Clínico e Diretrizes Terapêuticas para Atenção Integral às Pessoas com Infecções Sexualmente Transmissíveis (IST), no âm bito do Sistema Único de Saúde - SUS [Internet]. Diário Oficial da União, Brasília (DF), 2018 out 8 [cited 2020 out 2]; Seção 1:88. Available from:: http://bvsms.saude.gov.br/bvs/saudelegis/sctie/2018/prt0042_08_10_2018.html
http://bvsms.saude.gov.br/bvs/saudelegis...
and updated by the panel of specialists in STI in 2020.

EPIDEMIOLOGY

Pelvic inflammatory disease is defined as the clinical inflammatory and infectious syndrome arising from the ascent of microorganisms from the lower genital tract (vagina and cervix) to the upper genital tract, which may harm the endometrium, tubes, ovaries, pelvic peritoneum, and adjacent structures. Consequently, endometritis, salpingitis, oophoritis, and pelvic peritonitis can arise, depending on the infection's extent. Dissemination occurs predominantly through the canalicular route22. Ford GW, Decker CF. Pelvic inflammatory disease. Dis Mon [Internet]. 2016 Aug [cited 2020 Oct 2]; 62(8):301-5. Available from:: https://doi.org/10.1016/j.disamonth.2016.03.015
https://doi.org/10.1016/j.disamonth.2016...
,33. Paavonen J. Pelvic Inflammatory disease. From diagnosis to prevention. Dermatol Clin [Internet]. 1998 Oct [cited 2020 Oct 2]; 16(4):747-56. Available from:: https://doi.org/10.1016/s0733-8635(05)70041-3
https://doi.org/10.1016/s0733-8635(05)70...
.

Although the classical pelvic inflammatory disease definition includes only canalicular and spontaneous microorganism dissemination, not associated with surgical or procedures or pregnancy33. Paavonen J. Pelvic Inflammatory disease. From diagnosis to prevention. Dermatol Clin [Internet]. 1998 Oct [cited 2020 Oct 2]; 16(4):747-56. Available from:: https://doi.org/10.1016/s0733-8635(05)70041-3
https://doi.org/10.1016/s0733-8635(05)70...
, intrauterine devices (IUD) insertion, endometrium biopsy, curettage, among others, are also currently considered as responsible for the syndrome22. Ford GW, Decker CF. Pelvic inflammatory disease. Dis Mon [Internet]. 2016 Aug [cited 2020 Oct 2]; 62(8):301-5. Available from:: https://doi.org/10.1016/j.disamonth.2016.03.015
https://doi.org/10.1016/j.disamonth.2016...
.

Pelvic inflammatory disease is one of the most significant sexually transmitted infections, and a principal negative consequence of cervicitis. It is estimated that there is one case of pelvic inflammatory disease for every eight to ten women with Chlamydia trachomatis cervicitis33. Paavonen J. Pelvic Inflammatory disease. From diagnosis to prevention. Dermatol Clin [Internet]. 1998 Oct [cited 2020 Oct 2]; 16(4):747-56. Available from:: https://doi.org/10.1016/s0733-8635(05)70041-3
https://doi.org/10.1016/s0733-8635(05)70...
. The absence of rapid diagnosis and treatment or inadequate treatment increases the risk of severe complications, with negative consequences for women's health, as well as economic and social costs. Most sequelae involve infertility, ectopic pregnancy, and chronic pelvic pain44. Haggerty CL, Gottlieb SM, Taylor BD, Low N, XU F, Ness RB. Risk of sequelae after Chlamydia trachomatis genital infection in women. J Infect Dis [Internet]. 2010 Jun [cited 2020 Oct 2]; 201(Suppl 2):S134-55. Available from:: https://doi.org/10.1086/652395
https://doi.org/10.1086/652395...

5. World Bank. World development report 1993: investing in health, world development indicators [Internet]. New York: Oxford University Press; 1993 [cited 2020 Jul 20]. Available from:: https://openknowledge.worldbank.org/handle/10986/5976
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-66. Crossman SH. The challenge of pelvic inflammatory disease. Am Fam Physician [Internet]. 2006 Mar [cited 2020 Oct 2]; 73(5):859-64. [update: Am Fam Physician . 2006 Dec 15;74(12):2024]. Available from:: https://www.aafp.org/afp/2006/0301/p859.html
https://www.aafp.org/afp/2006/0301/p859....
. It has been reported that, after seven years from the first episode, 21.3% of women presented recurrence, 19% developed infertility, and 42.7% experienced chronic pelvic pain77. 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 [Internet]. 2011 Sep [cited 2020 Oct 2]; 38(9):879-81. Available from:: https://dx.doi.org/10.1097%2FOLQ.0b013e31821f918c
https://doi.org/10.1097%2FOLQ.0b013e3182...
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Existing prevalence data are underestimated, since pelvic inflammatory disease is not compulsorily notified, and, for this reason, the number of affected women is unknown88. French CE, Hughes G, Nicholson A, Yung M, Ross JD, Williams T, et al. Estimation of pelvic inflammatory disease diagnoses: trends in England, 2000-2008. Sex Transm Dis [Internet]. 2011 Mar [cited 2020 Oct 2]; 38(3):158-62. Available from:: https://doi.org/10.1097/olq.0b013e3181f22f3e
https://doi.org/10.1097/olq.0b013e3181f2...
. Also, many cases present mild or few clinical symptoms which are not noticed. Studies indicate that 10% to 40% of women with cervicitis caused by N. gonorrhoeae or C. trachomatis develop the pelvic inflammatory disease99. Bakken IJ, Ghaderi S. Incidence of pelvic inflammatory disease in a large cohort of women tested for Chlamydia trachomatis: a historical follow-up study. BMC Infect Dis [Internet]. 2009 Aug [cited 2020 Oct 2]; 9:130. Available from:: https://doi.org/10.1186/1471-2334-9-130
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,1010. Land JA, Van Bergen JEAM, Morré SA, Postma MJ. Epidemiology of Chlamydia trachomatis infection in women and the cost-effectiveness of screening. Hum Reprod Update [Internet]. 2010 Mar-Apr [cited 2020 Oct 2]; 16(2):189-204. Available from:: https://doi.org/10.1093/humupd/dmp035
https://doi.org/10.1093/humupd/dmp035...
. In Brazil, the true prevalence of the disease is unknown. Using Brazilian National Health System Hospital Information System, the hospitalization number of women with pelvic inflammatory disease from January 2005 to August 2006 was obtained. The hospitalization average per year was 45,343 cases. However, it is essential to highlight that such data reflects only severe cases of the syndrome, those that required hospital care, and they represent only a small fraction of the affected women since in most of them the infection elicits only light or moderate symptoms or is asymptomatic1111. Pinto VM, Szwarcwald CL, Baroni C, Stringati LL, Inocencio LA, Miranda AE. Chlamydia trachomatis prevalence and risk behaviors in parturient women aged 15 to 24 in Brazil. Sex Transm Dis [Internet]. 2011 Oct [cited 2020 Oct 2]; 38(10):957-61. Available from:: https://doi.org/10.1097/olq.0b013e31822037fc
https://doi.org/10.1097/olq.0b013e318220...
.

In a study conducted in the United States, 4.4% of 1,171 sexually active women between 18 and 44 years old had symptoms suggesting pelvic inflammatory disease1212. National Center for Health Statics. National health and nutrition examination survey 2013-2014 [Internet]. Washington, D.C.: Centers for Disease Control and Prevention; 2020 [cited 2020 Jul 22]. Available from:: https://www.cdc.gov/nchs/nhanes/index.htm
https://www.cdc.gov/nchs/nhanes/index.ht...
. From this result, it was estimated that for the period 2013-2014, 2.5 million women had pelvic inflammatory disease in the United States1313. Kreisel K, Torrone E, Bernstein K, Hong J, Gorwitz R. Prevalence of pelvic inflammatory disease in sexually experienced women of reproductive age -United States, 2013-2014. MMWR Morb Mortal Wkly Rep [Internet]. 2017 Jan [cited 2020 Oct 2]; 66(3):80-3. Available from:: http://dx.doi.org/10.15585/mmwr.mm6603a3
https://doi.org/10.15585/mmwr.mm6603a3...
. Another study suggests that 800,000 cases of the disease occur per year in that country1414. Das Breanne B, Ronda J, Trent M. Pelvic inflammatory disease: improving awareness, prevention, and treatment. Infect Drug Resist [Internet]. 2016 Aug [cited 2020 Oct 2]; 9:191-7. Available from:: https://dx.doi.org/10.2147%2FIDR.S91260
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. Sutton et al. (2005) estimated 1.2 million medical visits yearly due to pelvic inflammatory disease in developed countries1515. Sutton MY, Stemberg M, Zaidi A, St Louis ME, Markowitz LE. Trends in pelvic inflammatory disease hospital discharges and ambulatory visits, Unites States, 1885-2001. Sex Transm Dis [Internet]. 2005 Dec [cited 2020 Oct 2]; 32(12):778-84. Available from:: https://doi.org/10.1097/01.olq.0000175375.60973.cb
https://doi.org/10.1097/01.olq.000017537...
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The endocervix is classically considered a protecting barrier in the upper genital tract. Endocervical infection with sexually transmitted pathogens breaks this barrier providing access of vaginal bacteria to the upper genital organs, infecting endometrium, endosalpinx, pelvic peritoneum, and subjacent stroma22. Ford GW, Decker CF. Pelvic inflammatory disease. Dis Mon [Internet]. 2016 Aug [cited 2020 Oct 2]; 62(8):301-5. Available from:: https://doi.org/10.1016/j.disamonth.2016.03.015
https://doi.org/10.1016/j.disamonth.2016...
,33. Paavonen J. Pelvic Inflammatory disease. From diagnosis to prevention. Dermatol Clin [Internet]. 1998 Oct [cited 2020 Oct 2]; 16(4):747-56. Available from:: https://doi.org/10.1016/s0733-8635(05)70041-3
https://doi.org/10.1016/s0733-8635(05)70...
,1616. Carvalho NS, Takimura M, Von Lisigen R, Freitas B. Doença inflamatória pélvica. In: Fernandes CE, Sá MF. Tratado de ginecologia FEBRASGO. Rio de Janeiro: Elsevier; 2019. p. 287-96.. The reasons for which bacteria in the lower genital tract cause pelvic inflammatory disease in only some women are not entirely known. Still, they may be associated with genetic variations, retrograde menstruation, immune response, bacterial load and menstrual cycle hormonal oscillations, considering that the menstrual cervix mucous is less bacteriostatic1717. Korn AP, Hessol NA, Padian NS, Bolan GA, Donegan E, Landers DV, et al. Risk factors for plasma cell endometritis among women with cervical Neisseria gonorrhoeae, cervical Chlamydia trachomatis, or bacterial vaginosis. Am J Obstet Gynecol [Internet]. 1998 May [cited 2020 Oct 2]; 178(5):987-90. Available from:: https://doi.org/10.1016/s0002-9378(98)70536-8
https://doi.org/10.1016/s0002-9378(98)70...

18. Ness RB, Kip KE, Hillier SL, Soper DE, Stamm CA, Sweet RL, et al. A cluster analysis of bacterial vaginosis associated microflora and pelvic inflammatory disease. Am J Epidemiol [Internet]. 2005 Sep [cited 2020 Oct 2]; 162(6):585-90. Available from:: https://doi.org/10.1093/aje/kwi243
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-1919. Morré SA, Karimi O, Ouburg S. Chlamydia trachomatis: identification of susceptibility markers for ocular and sexually transmitted infection by immunogenetics. FEMS Immunol Med Microbiol [Internet]. 2009 Mar [cited 2020 Oct 2]; 55(2):140-53. Available from:: https://doi.org/10.1111/j.1574-695x.2009.00536.x
https://doi.org/10.1111/j.1574-695x.2009...
. The infection's progression by anaerobic agents determines a higher oxygen consumption and a local oxyreduction potential decrease, which, alongside tissue devitalization, provides an environment of microaerophilia or even anaerobiosis (Monif theory)1616. Carvalho NS, Takimura M, Von Lisigen R, Freitas B. Doença inflamatória pélvica. In: Fernandes CE, Sá MF. Tratado de ginecologia FEBRASGO. Rio de Janeiro: Elsevier; 2019. p. 287-96.. In such environment, the microorganisms that reached the upper genital tract start a slow-growing phase, and opportunistic anaerobic agents develop. The result is a polymicrobial infectious condition22. Ford GW, Decker CF. Pelvic inflammatory disease. Dis Mon [Internet]. 2016 Aug [cited 2020 Oct 2]; 62(8):301-5. Available from:: https://doi.org/10.1016/j.disamonth.2016.03.015
https://doi.org/10.1016/j.disamonth.2016...
,33. Paavonen J. Pelvic Inflammatory disease. From diagnosis to prevention. Dermatol Clin [Internet]. 1998 Oct [cited 2020 Oct 2]; 16(4):747-56. Available from:: https://doi.org/10.1016/s0733-8635(05)70041-3
https://doi.org/10.1016/s0733-8635(05)70...
,1616. Carvalho NS, Takimura M, Von Lisigen R, Freitas B. Doença inflamatória pélvica. In: Fernandes CE, Sá MF. Tratado de ginecologia FEBRASGO. Rio de Janeiro: Elsevier; 2019. p. 287-96..

From the observation that two-thirds of women with STI did not have any previous history of treatment for pelvic inflammatory disease, the concept of subclinical pelvic inflammatory disease was proposed, being as common as the clinical disease, and presenting the same etiology66. Crossman SH. The challenge of pelvic inflammatory disease. Am Fam Physician [Internet]. 2006 Mar [cited 2020 Oct 2]; 73(5):859-64. [update: Am Fam Physician . 2006 Dec 15;74(12):2024]. Available from:: https://www.aafp.org/afp/2006/0301/p859.html
https://www.aafp.org/afp/2006/0301/p859....
,2020. Wiesenfeld HC. Pelvic inflammatory disease: treatment in adults and adolescents [Internet]. [S.l.]: UpToDate; 2019 [cited 2020 Jul 22]. Available from:: https://www.uptodate.com/contents/pelvic-inflammatory-disease-treatment-in-adults-and-adolescents
https://www.uptodate.com/contents/pelvic...
.

Most cases arise from sexually transmitted pathogenic agents, such as N. gonorrhoeae and C. trachomatis77. 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 [Internet]. 2011 Sep [cited 2020 Oct 2]; 38(9):879-81. Available from:: https://dx.doi.org/10.1097%2FOLQ.0b013e31821f918c
https://doi.org/10.1097%2FOLQ.0b013e3182...
,2121. 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 [Internet]. 2009 Jan [cited 2020 Oct 2]; 48(1):41-7. Available from:: https://doi.org/10.1086/594123
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,2222. Sweet RL. Pelvic inflammatory disease: current concepts of diagnosis and management. Curr Infect Dis Rep [Internet]. 2012 Feb [cited 2020 Oct 2]. Available from:: https://doi.org/10.1007/s11908-012-0243-y
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. A minor fraction of acute disease is not sexually transmitted but associated with germs that colonize the lower genital tract or enteric ones such as Mycoplasma hominis, Ureaplasma urealyticum, Peptococcus spp., Peptoestreptococcus spp., Bacteroides spp., Escherichia coli, Streptococcus agalactiae, and Campylobacter spp., in addition to respiratory pathogens (for example, Haemophilus influenzae, Streptococcus pneumoniae, Group A streptococci and Staphylococcus aureus)2323. Workowski KA, Berman S; Centers for Disease Control and Prevention (CDC). Sexually transmitted diseases treatment guidelines, 2010. MMWR Recomm Rep [Internet]. 2010 Dec [cited 2020 Oct 2]; 59(RR-12):1-110. Available from:: https://www.cdc.gov/mmwr/preview/mmwrhtml/rr5912a1.htm?s
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24. Haggerty CL, Taylor BD. Mycoplasma genitalium: an emerging cause of pelvic inflammatory disease. Infect Dis Obstet Gynecol [Internet]. 2011 Dec [cited 2020 Oct 2]; 2011:959816. Available from:: https://dx.doi.org/10.1155%2F2011%2F959816
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25. Weinstein SA, Stiles BG. A review of the epidemiology, diagnosis and evidence-based management of Mycoplasma genitalium. Sex Health [Internet]. 2011 Jun [cited 2020 Oct 2]; 8(2):143-58. Available from:: https://doi.org/10.1071/sh10065
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26. McGowin CL, Anderson-Smits C. Mycoplasma genitalium: an emerging cause of sexually transmitted disease in women. PLoS Pathog [Internet]. 2011 May [cited 2020 Oct 2]; 7(5):e1001324. Available from:: https://dx.doi.org/10.1371%2Fjournal.ppat.1001324
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-2727. Brunham RC, Gottlieb SL, Paavonen J. Pelvic inflammatory disease. NEngl J Med [Internet]. 2015 May [cited 2020 Oct 2]; 372(21):2039-48. Available from:: https://doi.org/10.1056/NEJMra1411426
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. Facultative aerobic organisms in the microbiota are deemed potentially causing agents2727. Brunham RC, Gottlieb SL, Paavonen J. Pelvic inflammatory disease. NEngl J Med [Internet]. 2015 May [cited 2020 Oct 2]; 372(21):2039-48. Available from:: https://doi.org/10.1056/NEJMra1411426
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. Etiological agents of pelvic inflammatory disease are listed in Figure 1.

FIGURE 1:
Etiological agents of pelvic inflammatory disease.

The use of culture methods for microorganisms identification made it possible to understand better the composition of the healthy vaginal microbiota, in mostly women comprised of one or more species of Lactobacillus, which act to protect the vaginal environment2828. Zhou X, Bent SJ, Schneider MG, Davis CC, Islan MR, Forney LJ. Characterization of vaginal microbial communities in adult healthy women using cultivation independent methods. Microbiology (Reading) [Internet]. 2004 Aug [cited 2020 Oct 2]; 150(Pt 8):2565-73. Available from:: https://doi.org/10.1099/mic.0.26905-0
https://doi.org/10.1099/mic.0.26905-0...
. Unbalanced status, such as bacterial vaginosis, which comprises a reduction or lack of Lactobacillus sp., and increase in concentrations and variability of anaerobic microorganisms such as Gardnerella vaginalis and Mycoplasma sp., can contribute to the migration of microorganisms to the upper genital tract. It was already shown that bacterial vaginosis doubles the risk of pelvic inflammatory disease1818. Ness RB, Kip KE, Hillier SL, Soper DE, Stamm CA, Sweet RL, et al. A cluster analysis of bacterial vaginosis associated microflora and pelvic inflammatory disease. Am J Epidemiol [Internet]. 2005 Sep [cited 2020 Oct 2]; 162(6):585-90. Available from:: https://doi.org/10.1093/aje/kwi243
https://doi.org/10.1093/aje/kwi243...
,2929. Galask RP, Larsen B, Ohm MJ. Vaginal flora and its role in disease entities. Clin Obstet Gynecol [Internet]. 1976 Mar [cited 2020 Oct 2]; 19(1):61-81. Available from:: https://doi.org/10.1097/00003081-197603000-00008
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,3030. Srinivasan S, Hoffman NG, Morgan MT, Matsen FA, Fiedler TL, Hall RW, et al. Bacterial communities in women with bacterial vaginosis: high resolution phylogenetic analyses reveal relationships of microbiota to clinical criteria. PLoS One [Internet]. 2012 Jun [cited 2020 Oct 2]; 7(6):e37818. Available from:: https://doi.org/10.1371/journal.pone.0037818
https://doi.org/10.1371/journal.pone.003...
.

The microorganism insulation in the upper genital tract has been associated with disease stages. However, studies using molecular methods have shown microorganisms in healthy women's endometrium, including Lactobacillus species, Mycoplasma hominins, G. vaginalis, and Enterobacter sp., among others3131. Moller BR, Kritiansen FV, Thorsen P, Frost L, Mogensen SC. Sterility of the uterine cavity. Acta Obstet Gynecol Scand [Internet]. 1995 Mar [cited 2020 Oct 2]; 74(3):216-9. Available from:: https://doi.org/10.3109/00016349509008942
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,3232. Kyono K, Hashimoto T, Nagai Y, Sakuraba Y. Analysis of endometrial microbiota by 16S ribosomal RNA gene sequencing among infertile patients: asingle-center pilot study. Reprod Med Biol [Internet]. 2018 Jul [cited 2020 Oct 2]; 17(3):297-306. Available from:: https://dx.doi.org/10.1002%2Frmb2.12105
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. However, although healthy women can host such microorganisms, their role in health and disease stages is still unknown. The interactions between the infectious agent and genital tract immunity are probably determinant for the permanence in the health or changes to a disease stage. In addition, molecular techniques have identified new microorganisms, such as Atopobium vaginae. Studies have also identified new bacteria species and genera in the upper genital tract of women with pelvic inflammatory disease. Therefore, questions about the presence of a healthy microbiota in the upper genital tract and the possibility of mechanisms predisposing to physiologic vaginal flora unbalance that also predispose to infection need to be clarified. Such answers will undoubtedly lead to investigations on the best approach for diagnosis and treatment of pelvic inflammatory disease, as well as most efficient ways to prevent it3333. Sharma H, Tal R, Clark NA, Segars JH. Microbiota and pelvic inflammatory disease. Semin Reprod Med [Internet]. 2014 Aug [cited 2020 Oct 2]; 32(1):43-9. Available from:: https://dx.doi.org/10.1055%2Fs-0033-1361822
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Risk factors for pelvic inflammatory disease include:3434. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Doenças de Condições Crônicas e Infecções Sexualmente Transmissíveis. Protocolo clínico e diretrizes terapêuticas para atenção integral às pessoas com infecções sexualmente transmissíveis (IST) [Internet]. Brasília: Ministério da Saúde; 2015 [cited [cited 2020 out 2]]. Available from:: http://www.aids.gov.br/pt-br/pub/2015/protocolo-clinico-e-diretrizes-terapeuticas-para-atencao-integral-pessoas-com-infeccoes
http://www.aids.gov.br/pt-br/pub/2015/pr...
1) age group, as adolescents with multiple sexual partners, due to biological and behavioral factors characteristic in this phase, present risks three times greater for the development of acute pelvic inflammatory disease in comparison with women older than 25 years of age3535. Simms I, Stephenson JM, Mallinson H, Peeling RW, Thomas K, Gokhale R, et al. Risk factors associated with pelvic inflammatory disease. Sex Transm Infect [Internet]. 2006 Dec [cited 2020 Oct 2]; 82(6):452-7. Available from:: https://dx.doi.org/10.1136%2Fsti.2005.019539
https://doi.org/10.1136%2Fsti.2005.01953...
,3636. Hoenderboom BM, van Benthem BHB, van Bergen JEAM, Dukers-Muijrers NHTM, Götz HM, Hoebe CJPA, et al. Relation between Chlamydia trachomatis infection and pelvic inflammatory disease, ectopic pregnancy and tubal factor infertility in a Dutch cohort of women previously tested for chlamydia in a chlamydia screening trial. Sex Transm Infect [Internet]. 2019 Jun [cited 2020 Oct 2]; 95(4):300-6. Available from:: https://doi.org/10.1136/sextrans-2018-053778
https://doi.org/10.1136/sextrans-2018-05...
, regardless of education level and family income; 2) sexual behavior with multiple partners, early start of sexual activities and new partners3535. Simms I, Stephenson JM, Mallinson H, Peeling RW, Thomas K, Gokhale R, et al. Risk factors associated with pelvic inflammatory disease. Sex Transm Infect [Internet]. 2006 Dec [cited 2020 Oct 2]; 82(6):452-7. Available from:: https://dx.doi.org/10.1136%2Fsti.2005.019539
https://doi.org/10.1136%2Fsti.2005.01953...
; 3) using IUD, as women using such device present a slightly higher risk of pelvic inflammatory disease in the first 20 days of insertion, regardless of the type of IUD inserted - copper or levonorgestrel release3737. Meirik O. Intrauterine devices - upper and lower genital tract infections. Contraception [Internet]. 2007 Jun [cited 2020 Oct 2]; 75(Suppl 6):S41-7. Available from:: https://doi.org/10.1016/j.contraception.2006.12.017
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. This risk is reduced in women treated for STI before IUD insertion3838. Caddy S, Yudin MH, Hakim J, Money DM; Infectious Disease Committee; Special Contributor. Best practices to minimize risk of infection with intrauterine device insertion. J Obstet Gynaecol Can [Internet]. 2014 Mar [cited 2020 Oct 2]; 36(3):266-74. Available from:: https://doi.org/10.1016/s1701-2163(15)30636-8
https://doi.org/10.1016/s1701-2163(15)30...
.

CLINICAL ASPECTS

Clinical diagnosis is still the principal approach to pelvic inflammatory disease, despite the wide specter of clinical presentations. Around 65% of the cases can be oligosymptomatic and asymptomatic and later present infertility caused by tubal factors3939. Wiesenfeld HC, Sweet RL, Ness RB, Krohn MA, Amortegui AJ, Hillier SL. Comparison of acute and subclinical pelvic inflammatory disease. Sex Transm Dis [Internet]. 2005 Jul [cited 2020 Oct 2]; 32(7):400-5. Available from:: https://doi.org/10.1097/01.olq.0000154508.26532.6a
https://doi.org/10.1097/01.olq.000015450...
. The time course is usually acute, developing for several days. However, a more extensive manifestation can take place, from weeks to months. The typical disease symptoms are fever, abdominal pain, pelvic pain, dyspareunia, vaginal discharge, and dysuria or frequent urination3939. Wiesenfeld HC, Sweet RL, Ness RB, Krohn MA, Amortegui AJ, Hillier SL. Comparison of acute and subclinical pelvic inflammatory disease. Sex Transm Dis [Internet]. 2005 Jul [cited 2020 Oct 2]; 32(7):400-5. Available from:: https://doi.org/10.1097/01.olq.0000154508.26532.6a
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,4040. Jacobson L, Weström L. Objectivized diagnosis of acute pelvic inflammatory disease. Diagnostic and prognostic value of routine laparoscopy. Am J Obstet Gynecol [Internet]. 1969 Dec [cited 2020 Oct 2]; 105(7):1088-98. Available from:: https://doi.org/10.1016/0002-9378(69)90132-x
https://doi.org/10.1016/0002-9378(69)901...
. Abnormal uterine bleeding (post-intercourse bleeding, intermenstrual bleeding, and menorrhagia) in one-third or more of the cases is observed. Recent abdominal or pelvic pain, or both, intensifying during intercourse or vigorous movement, can be the only symptom. Pain starting during or right after menstruation is particularly suggestive4141. Ross J, Cole M, Evans C, Deirdre L, Dean G, Cousins D. United Kingdom national guideline for the management of pelvic inflammatory disease (2019 interim update) [Internet]. United Kingdom: British association for sexual health and HIV BASHH; 2019 [cited 2020 Jul 22]. Available from:: https://www.bashhguidelines.org/media/1217/pid-update-2019.pdf
https://www.bashhguidelines.org/media/12...
. Only a minority develop peritonitis or pelvic abscess, which generally manifest through intense pain, higher sensitivity to the examination, and systemic characteristics, such as fever4141. Ross J, Cole M, Evans C, Deirdre L, Dean G, Cousins D. United Kingdom national guideline for the management of pelvic inflammatory disease (2019 interim update) [Internet]. United Kingdom: British association for sexual health and HIV BASHH; 2019 [cited 2020 Jul 22]. Available from:: https://www.bashhguidelines.org/media/1217/pid-update-2019.pdf
https://www.bashhguidelines.org/media/12...

42. Workowski KA , Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep [Internet]. 2015 Jun [cited 2020 Oct 2]; 64(RR-03):1-137. Available from:: https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6403a1.htm
https://www.cdc.gov/mmwr/preview/mmwrhtm...
-4343. Ross J, Guaschino S, Cusini M, Jensen J. 2017 European guideline for the management of pelvic inflammatory disease. Int J STD AIDS [Internet]. 2018 Feb [cited 2020 Oct 2]; 29(2):108-14. Available from:: https://doi.org/10.1177/0956462417744099
https://doi.org/10.1177/0956462417744099...
. More rarely, an extension up to the liver capsule, causing perihepatitis (Fitz-Hugh Curtis syndrome) or sepsis, or both can occur2727. Brunham RC, Gottlieb SL, Paavonen J. Pelvic inflammatory disease. NEngl J Med [Internet]. 2015 May [cited 2020 Oct 2]; 372(21):2039-48. Available from:: https://doi.org/10.1056/NEJMra1411426
https://doi.org/10.1056/NEJMra1411426...
,4444. Curry A, Williams T, Penny ML. Pelvic inflammatory disease: diagnosis, management, and prevention. Am Fam Physician [Internet]. 2019 Sep [cited 2020 Oct 2]; 100(6):357-64. Available from:: https://www.aafp.org/afp/2019/0915/p357.html
https://www.aafp.org/afp/2019/0915/p357....
.

The clinical examination must include vital sign assessment; abdominal examination; vaginal speculum examination, with cervical inspection for friability (easy bleeding) and cervical mucopurulent discharge; bimanual vaginal examination, with cervical mobilization; and adnexal palpation (ovaries and uterine tube)4242. Workowski KA , Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep [Internet]. 2015 Jun [cited 2020 Oct 2]; 64(RR-03):1-137. Available from:: https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6403a1.htm
https://www.cdc.gov/mmwr/preview/mmwrhtm...
.

The sequelae are chronic pelvic pain, ectopic pregnancy, and infertility. Around 25% of the women with pelvic inflammatory disease will present chronic pelvic pain, 10% to 50% will be infertile, and 15% to 60% will have an ectopic pelvic inflammatory illness, generally caused by scars and adherence in the fallopian tubes77. 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 [Internet]. 2011 Sep [cited 2020 Oct 2]; 38(9):879-81. Available from:: https://dx.doi.org/10.1097%2FOLQ.0b013e31821f918c
https://doi.org/10.1097%2FOLQ.0b013e3182...
,4545. Weström 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 [Internet]. 1992 Jul-Aug [cited 2020 Oct 2]; 19(4):185-92. Available from:: https://journals.lww.com/stdjournal/Citation/1992/07000/Pelvic_Inflammatory_Disease_and_Fertility__A.1.aspx
https://journals.lww.com/stdjournal/Cita...
,4646. Lanjouw E, Ouburg S, 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 [Internet]. 2015 Nov [cited 2020 Oct 2]. Online ahead of print. Available from:: https://doi.org/10.1177/0956462415618838
https://doi.org/10.1177/0956462415618838...
. Such proportions increase typically with the number of infections, being very high in parts of Africa, Asia, and South America, where healthcare services are not easily accessible4747. Golden MR, Workowski KA , Bolan G. Developing a public health response to Mycoplasma genitalium. J Infect Dis [Internet]. 2017 Jul [cited 2020 Oct 2]; 216(Suppl 2):420-6. Available from:: https://doi.org/10.1093/infdis/jix200
https://doi.org/10.1093/infdis/jix200...
,4848. Fouks Y, Cohen Y, Tulandi T, Meiri A, Levin I, Almog B, et al. Complicated clinical course and poor reproductive outcomes of women with tubo-ovarian abscess after fertility treatments. J Minim Invasive Gynecol [Internet]. 2019 Jan [cited 2020 Oct 2]; 26(1):162-8. Available from:: https://doi.org/10.1016/j.jmig.2018.06.004
https://doi.org/10.1016/j.jmig.2018.06.0...
. There are also reports on pelvic inflammatory disease associated with a higher risk of cerebrovascular accident, ovary cancer, and acute small bowel obstruction4747. Golden MR, Workowski KA , Bolan G. Developing a public health response to Mycoplasma genitalium. J Infect Dis [Internet]. 2017 Jul [cited 2020 Oct 2]; 216(Suppl 2):420-6. Available from:: https://doi.org/10.1093/infdis/jix200
https://doi.org/10.1093/infdis/jix200...

48. Fouks Y, Cohen Y, Tulandi T, Meiri A, Levin I, Almog B, et al. Complicated clinical course and poor reproductive outcomes of women with tubo-ovarian abscess after fertility treatments. J Minim Invasive Gynecol [Internet]. 2019 Jan [cited 2020 Oct 2]; 26(1):162-8. Available from:: https://doi.org/10.1016/j.jmig.2018.06.004
https://doi.org/10.1016/j.jmig.2018.06.0...

49. Fehring RJ, Bouchard T, Meyers M. Influence of contraception use on the reproductive health of adolescents and young adults. Linacre Q [Internet]. 2018 May [cited 2020 Oct 2]; 85(2):167-77. Available from:: https://doi.org/10.1177/0024363918770462
https://doi.org/10.1177/0024363918770462...
-5050. Haumann A, Ongaro S, Detry O, Meunier P, Meurisse M. Acute pelvic inflammatory disease as a rare cause of acute small bowel obstruction. Acta Chir Belg [Internet]. 2019 Oct [cited 2020 Oct 2]; 119(5):328-30. Available from:: https://doi.org/10.1080/00015458.2018.1453438
https://doi.org/10.1080/00015458.2018.14...
.

DIAGNOSIS

Clinical diagnosis for pelvic inflammatory disease suspicion is conducted upon three major criteria associated with one minor criterion or one developed criterion3434. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Doenças de Condições Crônicas e Infecções Sexualmente Transmissíveis. Protocolo clínico e diretrizes terapêuticas para atenção integral às pessoas com infecções sexualmente transmissíveis (IST) [Internet]. Brasília: Ministério da Saúde; 2015 [cited [cited 2020 out 2]]. Available from:: http://www.aids.gov.br/pt-br/pub/2015/protocolo-clinico-e-diretrizes-terapeuticas-para-atencao-integral-pessoas-com-infeccoes
http://www.aids.gov.br/pt-br/pub/2015/pr...
, presented in Figure 2.

FIGURE 2:
Pelvic inflammatory disease diagnosis criteria.

Laboratory and image examinations help in diagnosis and severity assessment and are central in oligosymptomatic cases. However, in case of high clinical suspicion, treatment must not be delayed.

The following laboratory tests are recommended: complete blood count; erythrocyte sedimentation rate; C-reactive protein; bacterioscopic examination for bacterial vaginosis; endocervical swab culture with antibiogram; molecular biology for N. gonorrhoeae and C. trachomatis in material from the endocervix, urethra, laparoscopy, or culdocentesis; qualitative urine examination and urine culture, for dismissing urinary tract infection; hemoculture; pregnancy test, for rejecting the diagnosis of ectopic pregnancy; and imaging exams5151. World Health Organization - WHO. Diagnóstico laboratorial de doenças sexualmente transmissíveis, incluindo o vírus da imunodeficiência humana [Internet]. Brasília: Organização Mundial da Saúde; Ministério da Saúde; 2013 [cited 2020 jul 22]. 255 p. Available from:: https://www.who.int/reproductivehealth/publications/rtis/9789241505840/en/
https://www.who.int/reproductivehealth/p...
. Serological exams for C. trachomatis are not recommended for pelvic inflammatory disease diagnosis.

Pelvic ultrasound is the preferential imaging exam, as it is accessible and noninvasive, mainly for evaluating possible associated complications, such as tubo-ovarian abscesses, and for excluding differential diagnosis5252. Cicchiello LA, Hamper UM, Scoutt LM. Ultrasound evaluation of gynecologic causes of pelvic pain. Obstet Gynecol Clin North Am [Internet]. 2011 Mar [cited 2020 Oct 2]; 38(1):85-114, viii. Available from:: https://doi.org/10.1016/j.ogc.2011.02.005
https://doi.org/10.1016/j.ogc.2011.02.00...
. In pelvic inflammatory disease, the main suspicious sonographic finding is a thin layer of liquid filling the tubes, with or without free fluid in the pelvis. Tomography and resonance examinations can help in differential diagnosis of peritonitis4242. Workowski KA , Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep [Internet]. 2015 Jun [cited 2020 Oct 2]; 64(RR-03):1-137. Available from:: https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6403a1.htm
https://www.cdc.gov/mmwr/preview/mmwrhtm...
,5151. World Health Organization - WHO. Diagnóstico laboratorial de doenças sexualmente transmissíveis, incluindo o vírus da imunodeficiência humana [Internet]. Brasília: Organização Mundial da Saúde; Ministério da Saúde; 2013 [cited 2020 jul 22]. 255 p. Available from:: https://www.who.int/reproductivehealth/publications/rtis/9789241505840/en/
https://www.who.int/reproductivehealth/p...
.

Laparoscopy represents an accurate salpingitis diagnosis resource, enabling a complete bacteriologic diagnosis. However, it does not detect endometritis and less intense tube inflammation, and, thus, its daily use is not justifiable in the disease's initial phase, considering low sensitivity1818. Ness RB, Kip KE, Hillier SL, Soper DE, Stamm CA, Sweet RL, et al. A cluster analysis of bacterial vaginosis associated microflora and pelvic inflammatory disease. Am J Epidemiol [Internet]. 2005 Sep [cited 2020 Oct 2]; 162(6):585-90. Available from:: https://doi.org/10.1093/aje/kwi243
https://doi.org/10.1093/aje/kwi243...
,1919. Morré SA, Karimi O, Ouburg S. Chlamydia trachomatis: identification of susceptibility markers for ocular and sexually transmitted infection by immunogenetics. FEMS Immunol Med Microbiol [Internet]. 2009 Mar [cited 2020 Oct 2]; 55(2):140-53. Available from:: https://doi.org/10.1111/j.1574-695x.2009.00536.x
https://doi.org/10.1111/j.1574-695x.2009...
and associated morbidity4141. Ross J, Cole M, Evans C, Deirdre L, Dean G, Cousins D. United Kingdom national guideline for the management of pelvic inflammatory disease (2019 interim update) [Internet]. United Kingdom: British association for sexual health and HIV BASHH; 2019 [cited 2020 Jul 22]. Available from:: https://www.bashhguidelines.org/media/1217/pid-update-2019.pdf
https://www.bashhguidelines.org/media/12...

42. Workowski KA , Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep [Internet]. 2015 Jun [cited 2020 Oct 2]; 64(RR-03):1-137. Available from:: https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6403a1.htm
https://www.cdc.gov/mmwr/preview/mmwrhtm...
-4343. Ross J, Guaschino S, Cusini M, Jensen J. 2017 European guideline for the management of pelvic inflammatory disease. Int J STD AIDS [Internet]. 2018 Feb [cited 2020 Oct 2]; 29(2):108-14. Available from:: https://doi.org/10.1177/0956462417744099
https://doi.org/10.1177/0956462417744099...
. Laparoscopy had its great merit in the 1980s, as it led to the Gainesville clinical classification5353. Papavarnavas CP, Venter PF, van Staden MJ. Acute salpingitis laparoscopic and microbiological evaluation. S Afr Med J. 1990 Apr;77(8):403-4.; in practice, it still very used according to clinical and ultrasound findings, being necessary for treatment guidance, to wit: stage I - salpingitis without peritonitis; stage II - salpingitis with peritonitis; stage III - the presence of tubo-ovarian complex, divided in A (hydrosalpinx) and B (tubo-ovarian abscess); stage IV - ruptured tubo-ovarian abscess; and stage V - any of above, associated to genital tuberculosis.

In differential diagnosis, the list includes ectopic pregnancy, acute appendicitis, diverticulitis, urinary tract infection, ureteral lithiasis, ovarian cyst or uterine myoma torsion, ovarian cyst rupture, endometriosis, and ruptured endometrioma, among others22. Ford GW, Decker CF. Pelvic inflammatory disease. Dis Mon [Internet]. 2016 Aug [cited 2020 Oct 2]; 62(8):301-5. Available from:: https://doi.org/10.1016/j.disamonth.2016.03.015
https://doi.org/10.1016/j.disamonth.2016...
,1616. Carvalho NS, Takimura M, Von Lisigen R, Freitas B. Doença inflamatória pélvica. In: Fernandes CE, Sá MF. Tratado de ginecologia FEBRASGO. Rio de Janeiro: Elsevier; 2019. p. 287-96.,2222. Sweet RL. Pelvic inflammatory disease: current concepts of diagnosis and management. Curr Infect Dis Rep [Internet]. 2012 Feb [cited 2020 Oct 2]. Available from:: https://doi.org/10.1007/s11908-012-0243-y
https://doi.org/10.1007/s11908-012-0243-...
.

TREATMENT

Figure 3 presents guidance for pelvic inflammatory disease outpatient clinical management and indicates the need for urgency evaluation or hospital treatment3434. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Doenças de Condições Crônicas e Infecções Sexualmente Transmissíveis. Protocolo clínico e diretrizes terapêuticas para atenção integral às pessoas com infecções sexualmente transmissíveis (IST) [Internet]. Brasília: Ministério da Saúde; 2015 [cited [cited 2020 out 2]]. Available from:: http://www.aids.gov.br/pt-br/pub/2015/protocolo-clinico-e-diretrizes-terapeuticas-para-atencao-integral-pessoas-com-infeccoes
http://www.aids.gov.br/pt-br/pub/2015/pr...
.

FIGURE 3:
Flowchart for pelvic inflammatory disease clinical management.

Treatment must start immediately, aiming at avoiding late complications, such as infertility, ectopic pregnancy, and chronic pelvic pain5454. Hillis SD, Joesoef R, Marchbanks PA, Wasserheit JN, Cates W Jr, Westrom L. Delayed care of pelvic inflammatory disease as a risk factor for impaired fertility. Am J Obstet Gynecol [Internet]. 1993 May [cited 2020 Ocr 2]; 168(5):1503-9. Available from:: https://doi.org/10.1016/s0002-9378(11)90790-x
https://doi.org/10.1016/s0002-9378(11)90...
. Treatment of other common pelvic pain causes (ectopic pregnancy, acute appendicitis, ovarian cyst, and functional pain) is unlikely to be harmed by antimicrobial therapy for pelvic inflammatory disease4242. Workowski KA , Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep [Internet]. 2015 Jun [cited 2020 Oct 2]; 64(RR-03):1-137. Available from:: https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6403a1.htm
https://www.cdc.gov/mmwr/preview/mmwrhtm...
. In addition to antibiotics, analgesic and anti-inflammatory drugs can be used for decreasing symptomatology.

Outpatient treatment applies to women that present light clinical pictures without signs of pelvic peritonitis (Gainesville Stage I)5353. Papavarnavas CP, Venter PF, van Staden MJ. Acute salpingitis laparoscopic and microbiological evaluation. S Afr Med J. 1990 Apr;77(8):403-4.. Other clinical stages and criteria summarized in Figure 4 require hospital treatment3434. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Doenças de Condições Crônicas e Infecções Sexualmente Transmissíveis. Protocolo clínico e diretrizes terapêuticas para atenção integral às pessoas com infecções sexualmente transmissíveis (IST) [Internet]. Brasília: Ministério da Saúde; 2015 [cited [cited 2020 out 2]]. Available from:: http://www.aids.gov.br/pt-br/pub/2015/protocolo-clinico-e-diretrizes-terapeuticas-para-atencao-integral-pessoas-com-infeccoes
http://www.aids.gov.br/pt-br/pub/2015/pr...
.

FIGURE 4:
Criteria for recommending pelvic inflammatory disease hospital treatment.

Therapeutic schemes must present antimicrobial coverage for pelvic inflammatory disease etiological agents3434. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Doenças de Condições Crônicas e Infecções Sexualmente Transmissíveis. Protocolo clínico e diretrizes terapêuticas para atenção integral às pessoas com infecções sexualmente transmissíveis (IST) [Internet]. Brasília: Ministério da Saúde; 2015 [cited [cited 2020 out 2]]. Available from:: http://www.aids.gov.br/pt-br/pub/2015/protocolo-clinico-e-diretrizes-terapeuticas-para-atencao-integral-pessoas-com-infeccoes
http://www.aids.gov.br/pt-br/pub/2015/pr...
as shown in Figure 5. The antibiotic therapy must have a broad scope, be efficient against N. gonorrhoeae, C. trachomatis, and anaerobic organisms, especially Bacteroides fragilis, even if they are not confirmed in laboratory examination, and include bacterial vaginosis, Gram-negative bacteria, facultative bacteria, and streptococci5555. Jaiyeoba O, Lazenby G, Soper DE. Recommendations and rationale for the treatment of pelvic inflammatory disease. Expert Rev Anti Infect Ther [Internet]. 2011 Jan [cited 2020 Oct 2]; 9(1):61-70. Available from:: https://doi.org/10.1586/eri.10.156
https://doi.org/10.1586/eri.10.156...
,5656. Duarte R, Fuhrich D, Ross JD. A review of antibiotic therapy for pelvic inflammatory disease. Int J Antimicrob Agents [Internet]. 2015 Sep [cited 2020 Oct 2]; 46(3):272-7. Available from:: https://doi.org/10.1016/j.ijantimicag.2015.05.004
https://doi.org/10.1016/j.ijantimicag.20...
.

FIGURE 5:
Pelvic inflammatory disease treatment.

Among the broad-spectrum antibiotics with activity directed for such agents, beta-lactams, aminoglycosides, tetracyclines, lincosamides, and macrolides have been widely studied. They must be used in association with each other and can be administered through parenteral or oral route4242. Workowski KA , Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep [Internet]. 2015 Jun [cited 2020 Oct 2]; 64(RR-03):1-137. Available from:: https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6403a1.htm
https://www.cdc.gov/mmwr/preview/mmwrhtm...
,4343. Ross J, Guaschino S, Cusini M, Jensen J. 2017 European guideline for the management of pelvic inflammatory disease. Int J STD AIDS [Internet]. 2018 Feb [cited 2020 Oct 2]; 29(2):108-14. Available from:: https://doi.org/10.1177/0956462417744099
https://doi.org/10.1177/0956462417744099...
. Parenteral use may be suspended 24 hours after the end of the symptoms, and antimicrobial therapy through oral or intramuscular route must be extended up to 14 days.

In most studies, doxycycline is the antibiotic of choice for treating C. trachomatis. The combination of clindamycin and gentamicin presents moderate activity against N. gonorrhoeae and C. trachomatis in vitro, and second-generation cephalosporins (cefoxitin or cefotetan) associated with doxycycline shows excellent in vitro results. The ampicillin/sulbactam association is also a good choice5555. Jaiyeoba O, Lazenby G, Soper DE. Recommendations and rationale for the treatment of pelvic inflammatory disease. Expert Rev Anti Infect Ther [Internet]. 2011 Jan [cited 2020 Oct 2]; 9(1):61-70. Available from:: https://doi.org/10.1586/eri.10.156
https://doi.org/10.1586/eri.10.156...
,5656. Duarte R, Fuhrich D, Ross JD. A review of antibiotic therapy for pelvic inflammatory disease. Int J Antimicrob Agents [Internet]. 2015 Sep [cited 2020 Oct 2]; 46(3):272-7. Available from:: https://doi.org/10.1016/j.ijantimicag.2015.05.004
https://doi.org/10.1016/j.ijantimicag.20...
. Due to a high level of bacterial resistance, quinolones are not used for treating N. gonorrhoeae in Brazil5757. Bazzo ML, Golfetto L, Gaspar PC, Pires AF, Ramos MC, Franchini M, et al. First nationwide antimicrobial susceptibility surveillance for Neisseria gonorrhoeae in Brazil, 2015-16. J Antimicrob Chemother [Internet]. 2018 Jul [cited 2020 Oct 2]; 73(7):1854-61. Available from:: https://doi.org/10.1093/jac/dky090
https://doi.org/10.1093/jac/dky090...
.

For pelvic inflammatory disease treatment, PCDT indicates 500mg of ceftriaxone dosage in the recommended therapeutic schemes3434. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Doenças de Condições Crônicas e Infecções Sexualmente Transmissíveis. Protocolo clínico e diretrizes terapêuticas para atenção integral às pessoas com infecções sexualmente transmissíveis (IST) [Internet]. Brasília: Ministério da Saúde; 2015 [cited [cited 2020 out 2]]. Available from:: http://www.aids.gov.br/pt-br/pub/2015/protocolo-clinico-e-diretrizes-terapeuticas-para-atencao-integral-pessoas-com-infeccoes
http://www.aids.gov.br/pt-br/pub/2015/pr...
. This dosage was chosen in a decision by Conitec, based on a cost-benefit and financial impact evaluation of using ceftriaxone 250mg in the national territory5858. Ministério da Saúde (BR). Secretaria de Ciência, Tecnologia e Insumos Estratégicos. Comissão Nacional de Incorporação de Tecnologias no SUS (Conitec). Ceftriaxona 500mg para tratamento da Neisseria gonorrhoeae resistente à ciprofloxacina [Internet]. Brasília: Ministério da Saúde ; 2015 [cited [cited 2020 out 2]]. (Relatório de Recomendação, n. 154). 29 p. Available from:: http://conitec.gov.br/images/Relatorios/2015/Relatorio_Ceftriaxona_Gonorreia_final.pdf
http://conitec.gov.br/images/Relatorios/...
. International protocols recommend ceftriaxone dosage as 250mg, depending on the availability of the medication and N. gonorrhoeae antimicrobial susceptibility local evidences4242. Workowski KA , Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep [Internet]. 2015 Jun [cited 2020 Oct 2]; 64(RR-03):1-137. Available from:: https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6403a1.htm
https://www.cdc.gov/mmwr/preview/mmwrhtm...
.

Clinical improvement is likely to occur within up to three days from the start of the antimicrobial treatment. The cure is based on the end of signs and symptoms and normalization of inflammatory markers in laboratory tests. A study showed that if the evaluation is carried out with bacteriologic criteria after thirty days, there is still one or more bacterial agents in 40% of women77. 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 [Internet]. 2011 Sep [cited 2020 Oct 2]; 38(9):879-81. Available from:: https://dx.doi.org/10.1097%2FOLQ.0b013e31821f918c
https://doi.org/10.1097%2FOLQ.0b013e3182...
. If the clinical picture persists or worsens, a diagnostic revision must be considered. Laparoscopy, resonance, or tomography examinations can be conducted in such cases4242. Workowski KA , Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep [Internet]. 2015 Jun [cited 2020 Oct 2]; 64(RR-03):1-137. Available from:: https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6403a1.htm
https://www.cdc.gov/mmwr/preview/mmwrhtm...
,5151. World Health Organization - WHO. Diagnóstico laboratorial de doenças sexualmente transmissíveis, incluindo o vírus da imunodeficiência humana [Internet]. Brasília: Organização Mundial da Saúde; Ministério da Saúde; 2013 [cited 2020 jul 22]. 255 p. Available from:: https://www.who.int/reproductivehealth/publications/rtis/9789241505840/en/
https://www.who.int/reproductivehealth/p...
. Laparotomy is recommended in cases of adnexal masses unresponsive to treatment or rupturing. Culdotomy may be recommended if the abscess covers the bottom of the pouch of Douglas. In particular instances, tubo-ovarian abscesses can be drained with puncture guided through ultrasound3434. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Doenças de Condições Crônicas e Infecções Sexualmente Transmissíveis. Protocolo clínico e diretrizes terapêuticas para atenção integral às pessoas com infecções sexualmente transmissíveis (IST) [Internet]. Brasília: Ministério da Saúde; 2015 [cited [cited 2020 out 2]]. Available from:: http://www.aids.gov.br/pt-br/pub/2015/protocolo-clinico-e-diretrizes-terapeuticas-para-atencao-integral-pessoas-com-infeccoes
http://www.aids.gov.br/pt-br/pub/2015/pr...
.

A return medical appointment to the outpatient follow-up must be scheduled in the first week, suggesting a second appointment 30 days after hospital discharge. In reproductive planning, the use or removal of hormonal contraceptives and IUD should be evaluated3434. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Doenças de Condições Crônicas e Infecções Sexualmente Transmissíveis. Protocolo clínico e diretrizes terapêuticas para atenção integral às pessoas com infecções sexualmente transmissíveis (IST) [Internet]. Brasília: Ministério da Saúde; 2015 [cited [cited 2020 out 2]]. Available from:: http://www.aids.gov.br/pt-br/pub/2015/protocolo-clinico-e-diretrizes-terapeuticas-para-atencao-integral-pessoas-com-infeccoes
http://www.aids.gov.br/pt-br/pub/2015/pr...
,5959. Mitchell C, Prabhu M. Pelvic inflammatory disease: current concepts in pathogenesis, diagnosis and treatment. Infect Dis Clin North Am [Internet]. 2013 Dec [cited 2020 Oct 2]; 27(4):793-809. Available from:: https://doi.org/10.1016/j.idc.2013.08.004
https://doi.org/10.1016/j.idc.2013.08.00...
. We recommend sexual abstinence for 30 days and condoms usage during intercourse after this time period. IUD removal must not be necessarily conducted in light and moderate cases of pelvic inflammatory disease4141. Ross J, Cole M, Evans C, Deirdre L, Dean G, Cousins D. United Kingdom national guideline for the management of pelvic inflammatory disease (2019 interim update) [Internet]. United Kingdom: British association for sexual health and HIV BASHH; 2019 [cited 2020 Jul 22]. Available from:: https://www.bashhguidelines.org/media/1217/pid-update-2019.pdf
https://www.bashhguidelines.org/media/12...

42. Workowski KA , Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep [Internet]. 2015 Jun [cited 2020 Oct 2]; 64(RR-03):1-137. Available from:: https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6403a1.htm
https://www.cdc.gov/mmwr/preview/mmwrhtm...
-4343. Ross J, Guaschino S, Cusini M, Jensen J. 2017 European guideline for the management of pelvic inflammatory disease. Int J STD AIDS [Internet]. 2018 Feb [cited 2020 Oct 2]; 29(2):108-14. Available from:: https://doi.org/10.1177/0956462417744099
https://doi.org/10.1177/0956462417744099...
. Still, it must be considered if the user wishes to do it or if there is no clinical improvement after 72 hours from the antibiotic therapy or in cases of severe pelvic inflammatory disease3838. Caddy S, Yudin MH, Hakim J, Money DM; Infectious Disease Committee; Special Contributor. Best practices to minimize risk of infection with intrauterine device insertion. J Obstet Gynaecol Can [Internet]. 2014 Mar [cited 2020 Oct 2]; 36(3):266-74. Available from:: https://doi.org/10.1016/s1701-2163(15)30636-8
https://doi.org/10.1016/s1701-2163(15)30...
. However, when indicated, removal must only take place after two doses of the therapeutic scheme6060. Public Health Agency of Canada - PHAC. Pelvic inflammatory disease (PID). In: PHAC. Updates to the Canadian guidelines on sexually transmitted infections [Internet]. Ottawa: PHAC; 2008 [cited 2020 Jul 22]. 436 p. Available from:: https://fhs.mcmaster.ca/medicine/infectious_diseases/residents/docs/Canadian-STI-Guidelines2008.pdf
https://fhs.mcmaster.ca/medicine/infecti...
. In such cases, using barrier or hormonal contraceptive methods must be recommended.

The acute episode of pelvic inflammatory disease and its sequela results in high financial costs for women and the health system. Such expenses have increased substantially, considering many women will need assisted reproductive techniques6161. Jennings LK, Krywko DM. Pelvic inflammatory disease (PID). Stat Pearls [Internet]. 2020 Jun [cited 2020 Jul 22]. Available from:: https://www.ncbi.nlm.nih.gov/books/NBK499959 /
https://www.ncbi.nlm.nih.gov/books/NBK49...
.

SURVEILLANCE, PREVENTION, AND CONTROL

Like other STIs, pelvic inflammatory disease prevention and control must include counseling focused on the person and their sexual partners. The aim is self-recognition and minimizing risk factors for STI and new pelvic inflammatory disease episodes6262. Safrai M, Rottenstreich A, Shushan A, Gilad R, Benshushan A, Levin G. Risk factors for recurrent Pelvic Inflammatory Disease. Eur J Obstet Gynecol Reprod Biol [Internet]. 2020 Jan [cited 2020 Oct 2]; 244:40-4. Available from:: https://doi.org/10.1016/j.ejogrb.2019.11.004
https://doi.org/10.1016/j.ejogrb.2019.11...
. HIV, syphilis, and hepatitis B and C testing are recommended. In specific cases, vaccines for hepatitis A, hepatitis B, and HPV must be offered3434. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Doenças de Condições Crônicas e Infecções Sexualmente Transmissíveis. Protocolo clínico e diretrizes terapêuticas para atenção integral às pessoas com infecções sexualmente transmissíveis (IST) [Internet]. Brasília: Ministério da Saúde; 2015 [cited [cited 2020 out 2]]. Available from:: http://www.aids.gov.br/pt-br/pub/2015/protocolo-clinico-e-diretrizes-terapeuticas-para-atencao-integral-pessoas-com-infeccoes
http://www.aids.gov.br/pt-br/pub/2015/pr...
.

All sexual partners must be counseled and evaluated, offering testing and vaccination. Sexual partners of up to two months before the diagnosis must be empirically treated for N. gonorrhoeae and C. trachomatis with intramuscular ceftriaxone 500mg and azithromycin 1g through oral route in a single dose3434. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Doenças de Condições Crônicas e Infecções Sexualmente Transmissíveis. Protocolo clínico e diretrizes terapêuticas para atenção integral às pessoas com infecções sexualmente transmissíveis (IST) [Internet]. Brasília: Ministério da Saúde; 2015 [cited [cited 2020 out 2]]. Available from:: http://www.aids.gov.br/pt-br/pub/2015/protocolo-clinico-e-diretrizes-terapeuticas-para-atencao-integral-pessoas-com-infeccoes
http://www.aids.gov.br/pt-br/pub/2015/pr...
.

Pelvic inflammatory disease is not present in the Ministry of Health compulsory notification diseases, nor are the infections by N. gonorrhoeae, C. trachomatis, and Mycoplasma genitalium reported6363. Brasil. Ministério da Saúde. Portaria MS/SVS nº 33, de 14de julho de 2005. Inclui doenças à relação de notificação compulsória, define agravos de notificação imediata e a relação dos resultados laboratoriais que devem ser notificados pelos Laboratórios de Referência Nacional ou Regional [Internet]. Diário Oficial da União , Brasília (DF), 2005 jul 15 [cited [cited 2020 out 2]]; Seção 1:111. Available from:: http://bvsms.saude.gov.br/bvs/saudelegis/svs/2005/prt0033_14_07_2005.html
http://bvsms.saude.gov.br/bvs/saudelegis...
. Despite this, the notifications can be carried out by the Federal District, states, and municipalities, depending on local decisions.

Pelvic inflammatory disease is a substantial public health problem. Mass screening for N. gonorrhoeae and C. trachomatis showed a reduction of pelvic inflammatory disease in women. The Center for Disease Control and Prevention of the United States recommends annual screening, primarily for sexually active women younger than 25 years and women older than 25 years with C. trachomatis infection risk, including their respective sexual partners. They also consider the possibility of screening men in scenarios with high prevalence and resources4242. Workowski KA , Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep [Internet]. 2015 Jun [cited 2020 Oct 2]; 64(RR-03):1-137. Available from:: https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6403a1.htm
https://www.cdc.gov/mmwr/preview/mmwrhtm...
,6464. Wiesenfeld HC. Screening for Chlamydia trachomatis infections in women. NEngl J Med [Internet]. 2017 Feb [cited 2020 Oct 2]; 376(8):765-73. Available from:: https://doi.org/10.1056/nejmcp1412935
https://doi.org/10.1056/nejmcp1412935...
. In the Brazilian setting, screening N. gonorrhoeae and C. trachomatis is recommended in some situations: first prenatal care medical appointments of pregnant women aged 30 or less, people with STI diagnosis, people living with HIV, sexual violence situations, people using HIV pre-exposure (PrEP) and post-exposure (PEP) prophylaxis and people with receptive anal sexual practice without condom use3434. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Doenças de Condições Crônicas e Infecções Sexualmente Transmissíveis. Protocolo clínico e diretrizes terapêuticas para atenção integral às pessoas com infecções sexualmente transmissíveis (IST) [Internet]. Brasília: Ministério da Saúde; 2015 [cited [cited 2020 out 2]]. Available from:: http://www.aids.gov.br/pt-br/pub/2015/protocolo-clinico-e-diretrizes-terapeuticas-para-atencao-integral-pessoas-com-infeccoes
http://www.aids.gov.br/pt-br/pub/2015/pr...
.

A possibility to be assessed in future protocols is the inclusion of M. genitalium diagnosis for women with pelvic inflammatory disease, in addition to N. gonorrhoeae and C. trachomatis6565. Pinto-Sander N, Soni S. Mycoplasma genitalium infection. BMJ [Internet]. 2019 Oct [cited 2020 Oct 2]; 367:l5820. Available from:: https://doi.org/10.1136/bmj.l5820
https://doi.org/10.1136/bmj.l5820...
. European and North-American clinical guidelines included such investigation in women with pelvic inflammatory disease and men with non-gonococcal urethritides. Different studies showed M. genitalium association with cervicitis and pelvic inflammatory disease; however, there is no evidence of benefits for universal screening4141. Ross J, Cole M, Evans C, Deirdre L, Dean G, Cousins D. United Kingdom national guideline for the management of pelvic inflammatory disease (2019 interim update) [Internet]. United Kingdom: British association for sexual health and HIV BASHH; 2019 [cited 2020 Jul 22]. Available from:: https://www.bashhguidelines.org/media/1217/pid-update-2019.pdf
https://www.bashhguidelines.org/media/12...

42. Workowski KA , Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep [Internet]. 2015 Jun [cited 2020 Oct 2]; 64(RR-03):1-137. Available from:: https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6403a1.htm
https://www.cdc.gov/mmwr/preview/mmwrhtm...
-4343. Ross J, Guaschino S, Cusini M, Jensen J. 2017 European guideline for the management of pelvic inflammatory disease. Int J STD AIDS [Internet]. 2018 Feb [cited 2020 Oct 2]; 29(2):108-14. Available from:: https://doi.org/10.1177/0956462417744099
https://doi.org/10.1177/0956462417744099...
.

SPECIAL POPULATIONS

Pregnant women with pelvic inflammatory disease have a high risk of miscarriage, chorioamnionitis, and premature delivery4242. Workowski KA , Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep [Internet]. 2015 Jun [cited 2020 Oct 2]; 64(RR-03):1-137. Available from:: https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6403a1.htm
https://www.cdc.gov/mmwr/preview/mmwrhtm...
, and they must be hospitalized and undergo intravenous broad-spectrum antibiotic treatment immediately. Doxycycline and quinolones are a contraindication during pregnancy3434. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Doenças de Condições Crônicas e Infecções Sexualmente Transmissíveis. Protocolo clínico e diretrizes terapêuticas para atenção integral às pessoas com infecções sexualmente transmissíveis (IST) [Internet]. Brasília: Ministério da Saúde; 2015 [cited [cited 2020 out 2]]. Available from:: http://www.aids.gov.br/pt-br/pub/2015/protocolo-clinico-e-diretrizes-terapeuticas-para-atencao-integral-pessoas-com-infeccoes
http://www.aids.gov.br/pt-br/pub/2015/pr...
.

Despite having a higher risk of pelvic inflammatory disease and complications, children, prepubertal adolescents, and women living with HIV have a similar clinical presentation and must be conducted in the same way as the general population5959. Mitchell C, Prabhu M. Pelvic inflammatory disease: current concepts in pathogenesis, diagnosis and treatment. Infect Dis Clin North Am [Internet]. 2013 Dec [cited 2020 Oct 2]; 27(4):793-809. Available from:: https://doi.org/10.1016/j.idc.2013.08.004
https://doi.org/10.1016/j.idc.2013.08.00...
,6666. Greydanus DE, Dodich C. Pelvic inflammatory disease in the adolescent: a poignant, perplexing, potentially preventable problem for patients and physicians. Curr Opin Pediatr [Internet]. 2015 Feb [cited 2020 Oct 2]; 27(1):92-9. Available from:: https://doi.org/10.1097/mop.0000000000000183
https://doi.org/10.1097/mop.000000000000...
,6767. Solomon M, Tuchman L, Hayes K, Badolato G, Goyal MK. Pelvic inflammatory disease in a pediatric emergency department: epidemiology and treatment. Pediatr Emerg Care [Internet]. 2019 Jun [cited 2020 Oct 2]; 35(6):389-90. Available from:: https://doi.org/10.1097/pec.0000000000001148
https://doi.org/pec.0000000000001148...
.

ACKNOWLEDGMENTS

The authors acknowledge this work’s contribution by the members of the technical panel of specialists responsible for developing the 2020 PCDT for Comprehensive Care for People with STI.

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Publication Dates

  • Publication in this collection
    17 May 2021
  • Date of issue
    2021

History

  • Received
    01 Feb 2021
  • Accepted
    10 Mar 2021
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