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Programmes to reduce pelvic inflammatory disease—the Swedish experience
THE
LANCET
Programmes experience Francis
Kamwendo,
to reduce pelvic inflammatory
Lars
Forslin,
Lennart
Bodin,
Dan
Lancet
1998;
351
(suppl
III):
25-28
Correspondence
a1125
toi Prof Dan Danielsson
Swedish
Danielsson
Pelvic inflammatory disease (I’ID) is the acute clinical of ascending genital-tract infection manifestation involving the endometrium, fallopian tubes, and/or adjacent pelvic structures.’ I’ID is a serious condition that almost exclusively affects sexually active women in their fertile years. Several million women worldwide have symptomatic PID each year, and a similar number probably have symptomless PID,’ and thus face an increased risk of infertility, ectopic pregnancy, and chronic pelvic pain.‘Ja” No widely accepted clinical criteria exist for PID, which complicates diagnosis.““’ Laparoscopic visualisation of inflamed fallopian tubes is considered the “gold standard” for diagnosis,’ though this technique has been found to miss some cases8 And, because of costcontainment and other reasons, laparoscopy is not available in many clinical situations. Incidence and prevalence rates, and trends therefore remain unknown. Studies based on hospital discharge surveys have found that at least 120-180 cases of acute PID per 10 000 women aged 15-24 years occur each year, with overall figures of 30-90 cases per 10 000 women aged 15-44 years.1a9z1u In addiiion to the woman’s morbidity, the costs of lost productivity and of hospital treatment are considerable, and include those for infertility, ectopic pregnancy, and chronic pelvic pain,“,” conditions that occur in about 20%, 9%, and 18% of women with syndromic PID, respectively.” Women treated in hospital for PID increased in many European countries during the 1960s and Figure 1: Cases of acute Percentage rates for isolation 197Os,lOJ4 and paralleled the epidemics of gonorrhoea and genital-tract chlamydial infection that began in the early 1960s. Although acute PID can have a polymicrobial aetiology, “-I’ it is the most common and most serious complication of genital chlamydial and gonococcal infections-the main cause of PID in about 80% of cases in women younger than 25 years.’ Strategies to detect, treat, and prevent lower genital-tract chlamydial and gonococcal infections are essential measures to reduce both symptomatic and clinically silent PID.
Department of Obstetrics and Gynaecology (F Kamwendo MD, L Foslin MD); Section of Biostatistics, Department of Occupational and Environmental Medicine (L Bodin PhD); and Department of Clinical Microbiology and Immunology (D Danielsson MD), hebro Medical Centre Hospital, S-701 85 orebro, Sweden
disease-the
The Swedish
experience
Under Swedish law, gonorrhoea and syphilis have been reportable as contagious diseases since 1919. Genital infection with Chlamydia trachomatis has been reported by diagnostic laboratories since 1982, and was made a notifiable disease in April, 1988.‘” This change in the law was preceded by intense discussions over the pros and cons, but because of the emerging HIV epidemic, the argument prevailed that treatable gonococcal and chlamydial infections could be used as realistic opportunities to counsel young people about sexually transmitted diseases including HIV. (STDs), Furthermore, genital chlamydial infection was established in the 1970s as an important aetiological agent of PID.‘9,20 Available figures on the incidence rates of gonorrhoea and genital chlamydial infections have helped determine the relation between these infections and the annual
PID treated of Neisseria
at iirebro gonorrhoeae
Medical Centre Hospital and Chlamydia trachomatis
1970-97 are shown
number of patients admitted to hospital for PID.” ” This relation is further illustrated by comparison of a 1970-97 study of patients hospitalised at our centre for acute PID (figure I), with incidence rates of gonorrhoea and genital chlamydia in the community (figure 2). The county of Grebro, with a mixed urban and rural population, is representative of a demographic cross section of Sweden for yearly incidence rates of gonorrhoea and genital chlamydia (figure 2). Thus, our long-term PID study may reflect the situation throughout Sweden. In the 28-year period represented in figure 1, almost 2650 patients were recruited from the same catchment diagnostic criteria used were similar area. The throughout the period.“,“’ Confirmation by laparoscopy was made in 60-65% of cases in the 1970s and 198Os, but, because of cost-containment policies, this procedure was used only in questionable cases in the 1990s. The Sexually
transmitted
diseases - Vol 351 - 1998
THE
LANCET
A Ct, Orebro county
Figure 2: Incidence of acute PID by age group in orebro Medical Centre Hospital catchment area Final data mints are for 1995-96. Inset shows national and brebro county incidence rates of lower genital-tract (Ct) infections
diagnostic criteria used correspond well with those other proposed, discussed, and analysed in publications.5,6,8 In a discussion of effective programmes to reduce PID, our long-term study may serve to illustrate certain issues, including: factors that influence PID epidemiology, antibiotic treatment, and the role of the male sex partner. Role of the intrauterine contraceptive device (IUCD) In our study, the number of patients admitted to hospital with PID varied less than 16% from year to year in the early 1970s and 198Os, by contrast with an almost 75% increase in the mid-1970s (figure 1). This increase mainly resulted from an indiscriminate use of IUCDs in young, sexually active, nulliparous women;25 findings that agree with those of others.‘“,” The majority of infections related to use of IUCDs were not associated with STDs but were caused by ascending indigenous vaginal flora (unpublished data). A national consensus was reached that IUCDs should not be prescribed to sexually active, nulliparous women. Subsequently, the number of PID cases fell to previous figures. Epidemiology of gonococcal and chlamydial P/D The incidence of gonorrhoea peaked in Sweden in 1970 with an annual incidence of almost 500 per 100 000 population. Since then, incidence has steadily declined in both women and men, and endemic gonorrhoea has now been eradicated in Sweden.” Cases diagnosed today are usually imported. In the late 196Os, and in 1970 when the gonorrhoea epidemic peaked, 40-45% of patients had gonococcal PID (figure l),z’,*4 and 15-l 7 % of women with untreated gonorrhoea developed acute PID. These figures changed substantially during the 1970s; the decline of gonococcal PID coincided with the falling incidence of gonorrhoea Sexually
transmitted
diseases - Vol 351 - 1998
per Byear
period
N gonorrhoeae
(Ng) and C trachomatis
in the community (figure 2). In fact, the incidence of gonococcal PID decreased proportionately further than that of urogenital gonorrhoea, which suggests that the decrease of gonorrhoea was real, and also that improved control of gonorrhoea in the community will result in a relatively greater decline in gonococcal PID. The results of our study support these suggestions: community gonorrhoea increased slightly both nationally and locally in &ebro county in the mid-1970s (figure 2), and corresponded to a local increase in gonococcal PID (figure 1). Despite the obvious decrease of gonococcal PID, the total number of patients hospitalised for PID did not change during the 1970s and early 1980s after exclusion of those related to IUCDs. A retrospective seroepidemiological study has shown that cases of PID due to chlamydia, an organism that was unknown at the time, were at least as common as gonococcal PID.*’ The extent of community genital chlamydial infections soon became obvious after introduction of improved culture techniques for diagnosis.‘R’2R and antigen-detection Screening strategies were adopted at family planning clinics, outpatient contraception clinics, antenatal clinics, &c. Identification and screening of symptom,-free rnen were facilitated by the option to use urine samples. Genital chlamydial infections in the community continuously declined as much as 65-75% after 1987 (figure 2). This decline coincided with a decrease in hospital-treated PID cases (figures 1 and ref 29). Today, incidence rates are only 25% of those in the early 1970s and 1980s. However, patients hospitalised for PID in Sweden and other countries probably represent the most severe cases. A fall in hospital-treated PID cases in the USA during the late 1980s and early 1990s has been interpreted to reflect changes in aetiology (an increasing proportion of more indolent chlamydial-associated PID) srrr26
THE
LANCET
and clinical management (from inpatient to outpatient) rather than true trends in disease incidence.‘O In Sweden, the admission to hospital of young women with suspected PID to minimise sequelae has been encouraged through continuing medical education. We cannot exclude, however, that the cost-containment policies and managed care implemented in Sweden in the mid-1990s may have had an impact on the number of hospital-treated PID patients over the past few years.
prevention of gonococcal and chlamydial infections are probably the most productive steps in prevention of PID, these pathogens cannot be found in about one-third of PID cases, in which the indigenous flora of the genital tract (mycoplasmas, anaerobes, enterobacteria, &c) may be implicated. Washington et a13’ did a comprehensive literature search to identify effective strategies for PID prevention, and examined relevant data on primary, secondary, and tertiary prevention. Primary prevention involves strategies to help individuals avoid exposure to infection with the two most pathogens-Neisseria gonorrhoeae important and Chlamydia trachomatis. Washington et aP5 analysed a wide range of suggested measures, such as “healthy” sexual behaviour (delayed sexual debut, reduced number of sexual partners, monogamous relationships, &c), and the use of mechanical and chemical barrier methods. They found that the long-term efficacy of these and other preventive measures had not been properly evaluated. They concluded, however, that increased public concern over HIV infection had had an impact on primary prevention. In fact, the decline in incidence of PID and in referrals of STDs reported from the Netherlands was ascribed to a change of heterosexual behaviour in the era of HIV/AIDS.‘” Secondary prevention involves keeping a lower genitaltract infection from either ascending to the upper genital tract or being further transmitted within the community. about 50% of women with gonococcal However, infections and 60-70% of those with chlamydial infections are symptom-free. These infections might be detected through partner notification by infected men but targeted screening programmes are more preferable. In Sweden, such programmes seem to have been successful in the eradication of endemic gonorrhoea, and in significantly reducing chlamydial infection,” which will have contributed to PID prevention, particularly in women younger than 25 years (figure 2). Direct evidence that a screening programme for chlamydial infection in women can contribute to the secondary prevention of PID was provided by Scholes et a1.37In a randomised, controlled trial of selective testing for cervical chlamydial infection, the incidence of PID was reduced by more than 50%. Tertiary prevention, as defined by Washington et ali5 involves preventing complications of upper-genital-tract infection, such as tubal dysfunction andior obstruction. Early effective antibiotic treatment to maintain tubal patency is emphasised by these authors and others.‘5m’7,31 The vague symptoms associated with chlamydial PID, however, often mean delay in seeking medical care and, thus, an increased risk of late sequelae. Gonococcal PID seems to have a more acute clinical course, which usually leads the patient to seek emergency treatment early. Falk,‘” in his comprehensive study of non-tuberculous acute salpingitis in the early 196Os, showed that women with gonococcal PID had a significantly better fertility prognosis than those with non-gonococcal PID.
Antibiotic treatment Effective antibiotic treatment of patients with PID is essential. Treatment must be started early, preferably within 2 days of the onset of abdominal pain, to avoid the serious sequelae of tubal infertility and ectopic pregnancy.?a4 However, most patients with PID delay in seeking medical care because of vague symptoms, which is especially true for women with chlamydial disease. Although most PID patients younger than 25 years of age may have a gonococcal and/or chlamydial infection, these women and especially women older than 25 years may have polymicrobial PID with microorganisms of the indigenous vaginal flora.‘5m’7 Broad-spectrum antimicrobial treatment is therefore essential, with a tetracycline plus a third-generation cephalosporin, plus metronidazole if an anaerobic abscess is suspected. This and similar schedules are recommended by the US Centers for Disease Control and Prevention3’ This regimen has been successfully used at our hospital since the mid-1970s. Recurrence rates were much lower in our centre“’ than those reported from another centre where treatment with tetracycline alone was given.’ The ma/e sexual partner In countries with legislation to control gonorrhoea, contact tracing and notification of the male sex partner(s) of a woman with gonococcal PID is usually mandatory. In our hospital, 40-45% of all patients treated for PID in the late 1960s and early 1970s had gonococcal disease.*’ However, male partners were not usually contacted by the STD outpatient clinic until after the patient was discharged from hospital. Thus, the opportunity was often missed to counsel and inform both patient and partners and to treat partners promptly while the patient was still in hospital. In a joint study in the mid-1980s of patients with gonococcal or chlamydial PID referred from various sources, we found that about two-thirds of male partners had a urethritis that was verified as gonococcal, chlamydial, or nongonococcalinon-chlamydial urethritis.32,33 We also found that, even if a woman with PID thought she had a monogamous sexual relationship, this was not always so for her male partner. From then, our policy has been prompt notification of partners for examination, treatment, information, and counselling while the patient is in hospital. The recurrence rate of PID has decreased in patients whose partners were managed in this way.z4 This and other similar studie? show that consideration of both the patient and her partner is an essential element in the management of PID.
Prevention
Conclusions Primary, secondary, and tertiary prevention strategies are all important to reduce PID and its sequelae. Counselling, education, and information campaigns, directed at both society as a whole and the individual to increase awareness of the consequences of sexual risk behaviour,
strategies
Measures being used or recommended for the prevention of PID will differ between countries because medical and cultural/social practices, ethical, legal, and economic factors must be considered. Although reduction and
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Sexually
transmitted
diseases * Vol 351 - 1998
THE
programmes. Early and effective antibiotic treatment of PID will reduce adverse effects on tubal patency, and inclusion of male sexual partners in management will reduce recurrence rates.?’ PID is the most common cause of tubal infertility,‘,’ and is also the strongest predictor for ectopic pregnancya-a disorder that steadily increased during the 1970s and 1980s in many European countries and the USA.‘-“,” Prevention of PID in women younger than 25 years, which was most obvious in our studies, would result in a decline of ectopic pregnancies, because this late sequelae of PID occurs more often in women older than 25 years4 In the past 4 years, we have experienced about a 40% decrease in ectopic pregnancies in Sweden and in our catchment area (unpublished data). This indicator further suggests that the decline of PID in Sweden has been real, and may be attributed to the strategies outlined.
18 19 20
21
22
23
24
References
10
11 12
13
14
15
16
17
Westrom L, i&xdh PA. Acute pelvic inflammatory disease. In: Holmes KK, Mardh PA, Spading PF, Wiesner PJ, eds. Sexually transmitted diseases, 2nd ed. New York: McGraw-Hill, 1990: 593-613. W&xx-Hansen P, Kiviat NB, Holmes KK. Atypical pelvic inflammatory disease: subacute, chronic or subclinical upper genital tract infection in women. In: Holmes KK, Mardh PA, Sparling PF, Wiener PJ, eds. Sexually transmitted diseases, 2nd ed. New York: McGraw-Hill, 1990: 615-620. Gates W, Rolfs RT, Aral SO. Sexually transmitted diseases, pelvic inflammatory disease and infertility: an epidemiologic update. Epidenziol Rev 1990; 12: 199-220. Hadgu A, Koch G, Westrom L. Analysis of ectopic pregnancy data using marginal and conditional models. Star Med 1997; 16: 2403-17. Hadgu A, Westrom L, Brook CA, Reynolds GH, Thompson SE. Predicting acute pelvic inflammatory disease: A multivariate analysis. Am J Obster Gynecol 1986; 155: 954-60. Kahn JG, Walker CK, Washington AE, Landers DV, Sweet RL. Diagnosing pelvic inflammatory disease. A comprehensive analysis and consideration for developing a new model. JAMA 1991; 266: 2594-604. Jacobson L, Westrom L. Objectivized diagnosis of acute pelvic inflammatory disease. AnzJ Obsret Gym-ml 1969; 105: 1088~98. Sellers J, Mahony J, Goldsmith C, et al. The accuracy of clinical findings and laparoscopy in pelvic inflammatory disease. Am J ObAtcr Gym01 1991; 164: 113-20. Wright N, Laemmle D. Acute pelvic inflammatory disease in an indigent population. AmJ Obstet Gynecol 1968; 101: 979-90. Westrom L. Incidence, prevalence and trends of acute pelvic inflammatory disease and its consequences in industrialized countries. AmJ Obstet Gynecol 1980; 138: X80-92. Curran J. Economic consequences of pelvic inflammatory disease in the United States. Am J Obstet Gynecol 1980; 138: 848-5 1. Washington AE, Katz P. Cost and payment source for pelvic inflammatory disease: trends and projections, 1983 through 2000. JAMA 1991; 266: 2565-69. Westrom L, Joesoef R, Reynolds G, Hadgu A, Thompson SE. Pelvic inflammatory disease and infertility. A cohort study of 1844 women with laparoscopically verified disease and 657 control women with normal laparoscopic results. Sex Transm Dis 1992; 19: 1X5-92. Adler MW. Trends for gonorrhea and pelvic inflammatory disease in England and Wales and for gonorrhea in a defined population. Am J Obsret Gym01 1980; 138: 901-04. Eschenbach DA, Buchanan TM, Pollock HM, et al. Polymicrobial etiology of acute pelvic inflammatory disease. N EnglJ Med 1975; 293: 166-71. Sweet RL, Draper DL, Hadley WK. Etiology of acute salpingitis: influence of episode, number and duration of symptoms. Obstet Gym01 1981; 58: 62-6X. Hemsell DL, Nobles BJ, Heard MC, Hemsell PG. Upper and lower
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27
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29 30
31
32
36
37
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reproductive tract bacteria in 126 women with acute pelvic inflammatory disease. Microbial susceptibility and clinical response to four therapeutic regimens. J ReprodMed 1988; 33: 799-805. Ripa T. Epidemiologic control of genital Chlamydia mchomatis infections. ScandJ Infect Di.s Suppl 1990; 69: 157-67. Eilard T, Brorson JE, Hamark B, Forsman L. Isolation of Chlamydia in acute salpingitis. &and J In& Dis Suppl 1976; 9: X2-84. Mardh PA, Ripa T, Svensson L, Westrom L. Chlamydia trachomatis infection in patients with acute salpingitis. NEnglJMed 1977; 296: 1377-79. 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 197X; 54: 247-50. Ripa T, Forslin L, Daniclsson D, Falk V. Frequency of gonococcal and chlamydial infections in patients with laparoscopically verified acute salpingitis in 1970 and 1980; epidemiological considerations. In: Mardh PA, Holmes KK, Oriel JD, Piot P, Schachter J, eds. Chlamydial Infections. Amsterdam: Elsevier Biomedical Press, 1982; 179-82. Westrom L, Svcnsson L, Wolner-Hansen I’, Mardh PA. Chlamydial and gonococcal infections in a defined population of women. ScandJ InfectDis Stcppl 1982; 32: 157-62. Kamwendo F, Forslin L, Bodin L, Danielsson D. Decreasing incidencrs of gonorrheaand chlamydia-associated acute pelvic inflammatoty disease. A 25-year study from an urban area of central Sweden. Sex Transm Dis 1996; 23: 384-91. Kamwendo F, Forslin L, D&&son D. Epidemiology and aetiology of acute non-tuberculous salpingitis: a comparison between the early 1970s and the early 1980s with special reference to gonorrhoea and use of intrauterine contraceptive device. Genitourirr Med 1990; 66: 324-29. Westrom L, Bengtsson LP, Mardh PA. The risk of pelvic inflammatory disease in women using intrauterine contraceptive devices as compared to non-users. Lancet 1976; ii: 221-24. Lee NC, Rubin GL, Borwki R. The intrauterine device and pelvic inflammatory disease revisited: new results from the women’s health study. Obstet Gynecol 1988; 72: 1-6. Kihlstrom E, Danielsson D. Advances in biology, management and prevention of infections caused by Chlamydia trachonzatis and Neissena gonowhoeae. Curr Opin Infect Dh 1994; 7: 25-33. Westrom L. Decrease in incidence of women treated in hospital for acute salpingitis in Sweden. Genirourin Med 1988; 64: 59-63. Division of STD Prevention. Sexually Transmitted Disease Surveillance, 1996. US Depatrm@nt of Health and Human Services, Public Health Service. Atlanta: Centers for Disease Control and Prevention, 1997. Centers for Disease Control and Prevention. 1998 guidelines for treatment of sexually transmitted diseases. MMWR Morb Movral IV’& Rep 199X; 46: 79-85. Johansson E, Moi H, For& L, Danielsson D. Prevalence of chlamydia infection, gonorrhoea and nonspecific urethritis in regular sexual partners of women with acute salpingitis [abstr 1 X3]. VII International Meeting of the International Society for STD Research; 1987: Atlanta, GA, USA. Kamwendo F, Johansson E, Moi H, Forslin L, Danieisson D. Gonorrhea, genital chlamydial infection and nonspecific urethritis in male partners of women hospitalized for acute pelvic inflammatory disease. Sex Transm Dis 1993; 20: 143-46. Sellers J, Mahony JB, Chernesky MA, Groves DJ, Rath DJ. Male contact tracing in a community-based study of confirmed acute pelvic inflammatory disease[abstr 1841. VII International Meeting of the International Society of STD Research; 1987: Atlanta, GA, USA. Washington AE, Gates Jr W, Wasserheit JN. Preventing pelvic inflammatory disease. JAMA 1991; 266: 2574-80. Coutinho RA, Rijsdijk AJ, van den Hoek JAR, Leentvaar-Kuijpers A. Decreasing incidence of PID in Amsterdam. Geniroutin Med 1992; 68: 353-55. Scholes D, Stergachis A, Heidrich FE, Andrilla H, Holmes KK, Stamm WE. Prevention of pelvic inflammatory disease by screening for cervical chlamydial infection. N EnglJMed 1996; 334: 1362-66. Falk V. Treatment of acute non-tuberculous salpingitis with antibiotics alone and in combination with glucocorticoids. Acza Obstel Gym01 &and 1965; 44 (suppI6): l-1 18. Washington AE, Berg AO. Preventing and managing pelvic inflammatory disease: Key questions, practices and evidence. 3 Fum Pratt 1996; 43: 2X3-93.
--Sexually
transmitted
diseases . Vol 35 1 * 1998
~11128
LANCET
Programmes experience Francis
Kamwendo,
to reduce pelvic inflammatory
Lars
Forslin,
Lennart
Bodin,
Dan
Lancet
1998;
351
(suppl
III):
25-28
Correspondence
a1125
toi Prof Dan Danielsson
Swedish
Danielsson
Pelvic inflammatory disease (I’ID) is the acute clinical of ascending genital-tract infection manifestation involving the endometrium, fallopian tubes, and/or adjacent pelvic structures.’ I’ID is a serious condition that almost exclusively affects sexually active women in their fertile years. Several million women worldwide have symptomatic PID each year, and a similar number probably have symptomless PID,’ and thus face an increased risk of infertility, ectopic pregnancy, and chronic pelvic pain.‘Ja” No widely accepted clinical criteria exist for PID, which complicates diagnosis.““’ Laparoscopic visualisation of inflamed fallopian tubes is considered the “gold standard” for diagnosis,’ though this technique has been found to miss some cases8 And, because of costcontainment and other reasons, laparoscopy is not available in many clinical situations. Incidence and prevalence rates, and trends therefore remain unknown. Studies based on hospital discharge surveys have found that at least 120-180 cases of acute PID per 10 000 women aged 15-24 years occur each year, with overall figures of 30-90 cases per 10 000 women aged 15-44 years.1a9z1u In addiiion to the woman’s morbidity, the costs of lost productivity and of hospital treatment are considerable, and include those for infertility, ectopic pregnancy, and chronic pelvic pain,“,” conditions that occur in about 20%, 9%, and 18% of women with syndromic PID, respectively.” Women treated in hospital for PID increased in many European countries during the 1960s and Figure 1: Cases of acute Percentage rates for isolation 197Os,lOJ4 and paralleled the epidemics of gonorrhoea and genital-tract chlamydial infection that began in the early 1960s. Although acute PID can have a polymicrobial aetiology, “-I’ it is the most common and most serious complication of genital chlamydial and gonococcal infections-the main cause of PID in about 80% of cases in women younger than 25 years.’ Strategies to detect, treat, and prevent lower genital-tract chlamydial and gonococcal infections are essential measures to reduce both symptomatic and clinically silent PID.
Department of Obstetrics and Gynaecology (F Kamwendo MD, L Foslin MD); Section of Biostatistics, Department of Occupational and Environmental Medicine (L Bodin PhD); and Department of Clinical Microbiology and Immunology (D Danielsson MD), hebro Medical Centre Hospital, S-701 85 orebro, Sweden
disease-the
The Swedish
experience
Under Swedish law, gonorrhoea and syphilis have been reportable as contagious diseases since 1919. Genital infection with Chlamydia trachomatis has been reported by diagnostic laboratories since 1982, and was made a notifiable disease in April, 1988.‘” This change in the law was preceded by intense discussions over the pros and cons, but because of the emerging HIV epidemic, the argument prevailed that treatable gonococcal and chlamydial infections could be used as realistic opportunities to counsel young people about sexually transmitted diseases including HIV. (STDs), Furthermore, genital chlamydial infection was established in the 1970s as an important aetiological agent of PID.‘9,20 Available figures on the incidence rates of gonorrhoea and genital chlamydial infections have helped determine the relation between these infections and the annual
PID treated of Neisseria
at iirebro gonorrhoeae
Medical Centre Hospital and Chlamydia trachomatis
1970-97 are shown
number of patients admitted to hospital for PID.” ” This relation is further illustrated by comparison of a 1970-97 study of patients hospitalised at our centre for acute PID (figure I), with incidence rates of gonorrhoea and genital chlamydia in the community (figure 2). The county of Grebro, with a mixed urban and rural population, is representative of a demographic cross section of Sweden for yearly incidence rates of gonorrhoea and genital chlamydia (figure 2). Thus, our long-term PID study may reflect the situation throughout Sweden. In the 28-year period represented in figure 1, almost 2650 patients were recruited from the same catchment diagnostic criteria used were similar area. The throughout the period.“,“’ Confirmation by laparoscopy was made in 60-65% of cases in the 1970s and 198Os, but, because of cost-containment policies, this procedure was used only in questionable cases in the 1990s. The Sexually
transmitted
diseases - Vol 351 - 1998
THE
LANCET
A Ct, Orebro county
Figure 2: Incidence of acute PID by age group in orebro Medical Centre Hospital catchment area Final data mints are for 1995-96. Inset shows national and brebro county incidence rates of lower genital-tract (Ct) infections
diagnostic criteria used correspond well with those other proposed, discussed, and analysed in publications.5,6,8 In a discussion of effective programmes to reduce PID, our long-term study may serve to illustrate certain issues, including: factors that influence PID epidemiology, antibiotic treatment, and the role of the male sex partner. Role of the intrauterine contraceptive device (IUCD) In our study, the number of patients admitted to hospital with PID varied less than 16% from year to year in the early 1970s and 198Os, by contrast with an almost 75% increase in the mid-1970s (figure 1). This increase mainly resulted from an indiscriminate use of IUCDs in young, sexually active, nulliparous women;25 findings that agree with those of others.‘“,” The majority of infections related to use of IUCDs were not associated with STDs but were caused by ascending indigenous vaginal flora (unpublished data). A national consensus was reached that IUCDs should not be prescribed to sexually active, nulliparous women. Subsequently, the number of PID cases fell to previous figures. Epidemiology of gonococcal and chlamydial P/D The incidence of gonorrhoea peaked in Sweden in 1970 with an annual incidence of almost 500 per 100 000 population. Since then, incidence has steadily declined in both women and men, and endemic gonorrhoea has now been eradicated in Sweden.” Cases diagnosed today are usually imported. In the late 196Os, and in 1970 when the gonorrhoea epidemic peaked, 40-45% of patients had gonococcal PID (figure l),z’,*4 and 15-l 7 % of women with untreated gonorrhoea developed acute PID. These figures changed substantially during the 1970s; the decline of gonococcal PID coincided with the falling incidence of gonorrhoea Sexually
transmitted
diseases - Vol 351 - 1998
per Byear
period
N gonorrhoeae
(Ng) and C trachomatis
in the community (figure 2). In fact, the incidence of gonococcal PID decreased proportionately further than that of urogenital gonorrhoea, which suggests that the decrease of gonorrhoea was real, and also that improved control of gonorrhoea in the community will result in a relatively greater decline in gonococcal PID. The results of our study support these suggestions: community gonorrhoea increased slightly both nationally and locally in &ebro county in the mid-1970s (figure 2), and corresponded to a local increase in gonococcal PID (figure 1). Despite the obvious decrease of gonococcal PID, the total number of patients hospitalised for PID did not change during the 1970s and early 1980s after exclusion of those related to IUCDs. A retrospective seroepidemiological study has shown that cases of PID due to chlamydia, an organism that was unknown at the time, were at least as common as gonococcal PID.*’ The extent of community genital chlamydial infections soon became obvious after introduction of improved culture techniques for diagnosis.‘R’2R and antigen-detection Screening strategies were adopted at family planning clinics, outpatient contraception clinics, antenatal clinics, &c. Identification and screening of symptom,-free rnen were facilitated by the option to use urine samples. Genital chlamydial infections in the community continuously declined as much as 65-75% after 1987 (figure 2). This decline coincided with a decrease in hospital-treated PID cases (figures 1 and ref 29). Today, incidence rates are only 25% of those in the early 1970s and 1980s. However, patients hospitalised for PID in Sweden and other countries probably represent the most severe cases. A fall in hospital-treated PID cases in the USA during the late 1980s and early 1990s has been interpreted to reflect changes in aetiology (an increasing proportion of more indolent chlamydial-associated PID) srrr26
THE
LANCET
and clinical management (from inpatient to outpatient) rather than true trends in disease incidence.‘O In Sweden, the admission to hospital of young women with suspected PID to minimise sequelae has been encouraged through continuing medical education. We cannot exclude, however, that the cost-containment policies and managed care implemented in Sweden in the mid-1990s may have had an impact on the number of hospital-treated PID patients over the past few years.
prevention of gonococcal and chlamydial infections are probably the most productive steps in prevention of PID, these pathogens cannot be found in about one-third of PID cases, in which the indigenous flora of the genital tract (mycoplasmas, anaerobes, enterobacteria, &c) may be implicated. Washington et a13’ did a comprehensive literature search to identify effective strategies for PID prevention, and examined relevant data on primary, secondary, and tertiary prevention. Primary prevention involves strategies to help individuals avoid exposure to infection with the two most pathogens-Neisseria gonorrhoeae important and Chlamydia trachomatis. Washington et aP5 analysed a wide range of suggested measures, such as “healthy” sexual behaviour (delayed sexual debut, reduced number of sexual partners, monogamous relationships, &c), and the use of mechanical and chemical barrier methods. They found that the long-term efficacy of these and other preventive measures had not been properly evaluated. They concluded, however, that increased public concern over HIV infection had had an impact on primary prevention. In fact, the decline in incidence of PID and in referrals of STDs reported from the Netherlands was ascribed to a change of heterosexual behaviour in the era of HIV/AIDS.‘” Secondary prevention involves keeping a lower genitaltract infection from either ascending to the upper genital tract or being further transmitted within the community. about 50% of women with gonococcal However, infections and 60-70% of those with chlamydial infections are symptom-free. These infections might be detected through partner notification by infected men but targeted screening programmes are more preferable. In Sweden, such programmes seem to have been successful in the eradication of endemic gonorrhoea, and in significantly reducing chlamydial infection,” which will have contributed to PID prevention, particularly in women younger than 25 years (figure 2). Direct evidence that a screening programme for chlamydial infection in women can contribute to the secondary prevention of PID was provided by Scholes et a1.37In a randomised, controlled trial of selective testing for cervical chlamydial infection, the incidence of PID was reduced by more than 50%. Tertiary prevention, as defined by Washington et ali5 involves preventing complications of upper-genital-tract infection, such as tubal dysfunction andior obstruction. Early effective antibiotic treatment to maintain tubal patency is emphasised by these authors and others.‘5m’7,31 The vague symptoms associated with chlamydial PID, however, often mean delay in seeking medical care and, thus, an increased risk of late sequelae. Gonococcal PID seems to have a more acute clinical course, which usually leads the patient to seek emergency treatment early. Falk,‘” in his comprehensive study of non-tuberculous acute salpingitis in the early 196Os, showed that women with gonococcal PID had a significantly better fertility prognosis than those with non-gonococcal PID.
Antibiotic treatment Effective antibiotic treatment of patients with PID is essential. Treatment must be started early, preferably within 2 days of the onset of abdominal pain, to avoid the serious sequelae of tubal infertility and ectopic pregnancy.?a4 However, most patients with PID delay in seeking medical care because of vague symptoms, which is especially true for women with chlamydial disease. Although most PID patients younger than 25 years of age may have a gonococcal and/or chlamydial infection, these women and especially women older than 25 years may have polymicrobial PID with microorganisms of the indigenous vaginal flora.‘5m’7 Broad-spectrum antimicrobial treatment is therefore essential, with a tetracycline plus a third-generation cephalosporin, plus metronidazole if an anaerobic abscess is suspected. This and similar schedules are recommended by the US Centers for Disease Control and Prevention3’ This regimen has been successfully used at our hospital since the mid-1970s. Recurrence rates were much lower in our centre“’ than those reported from another centre where treatment with tetracycline alone was given.’ The ma/e sexual partner In countries with legislation to control gonorrhoea, contact tracing and notification of the male sex partner(s) of a woman with gonococcal PID is usually mandatory. In our hospital, 40-45% of all patients treated for PID in the late 1960s and early 1970s had gonococcal disease.*’ However, male partners were not usually contacted by the STD outpatient clinic until after the patient was discharged from hospital. Thus, the opportunity was often missed to counsel and inform both patient and partners and to treat partners promptly while the patient was still in hospital. In a joint study in the mid-1980s of patients with gonococcal or chlamydial PID referred from various sources, we found that about two-thirds of male partners had a urethritis that was verified as gonococcal, chlamydial, or nongonococcalinon-chlamydial urethritis.32,33 We also found that, even if a woman with PID thought she had a monogamous sexual relationship, this was not always so for her male partner. From then, our policy has been prompt notification of partners for examination, treatment, information, and counselling while the patient is in hospital. The recurrence rate of PID has decreased in patients whose partners were managed in this way.z4 This and other similar studie? show that consideration of both the patient and her partner is an essential element in the management of PID.
Prevention
Conclusions Primary, secondary, and tertiary prevention strategies are all important to reduce PID and its sequelae. Counselling, education, and information campaigns, directed at both society as a whole and the individual to increase awareness of the consequences of sexual risk behaviour,
strategies
Measures being used or recommended for the prevention of PID will differ between countries because medical and cultural/social practices, ethical, legal, and economic factors must be considered. Although reduction and
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programmes. Early and effective antibiotic treatment of PID will reduce adverse effects on tubal patency, and inclusion of male sexual partners in management will reduce recurrence rates.?’ PID is the most common cause of tubal infertility,‘,’ and is also the strongest predictor for ectopic pregnancya-a disorder that steadily increased during the 1970s and 1980s in many European countries and the USA.‘-“,” Prevention of PID in women younger than 25 years, which was most obvious in our studies, would result in a decline of ectopic pregnancies, because this late sequelae of PID occurs more often in women older than 25 years4 In the past 4 years, we have experienced about a 40% decrease in ectopic pregnancies in Sweden and in our catchment area (unpublished data). This indicator further suggests that the decline of PID in Sweden has been real, and may be attributed to the strategies outlined.
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References
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Westrom L, i&xdh PA. Acute pelvic inflammatory disease. In: Holmes KK, Mardh PA, Spading PF, Wiesner PJ, eds. Sexually transmitted diseases, 2nd ed. New York: McGraw-Hill, 1990: 593-613. W&xx-Hansen P, Kiviat NB, Holmes KK. Atypical pelvic inflammatory disease: subacute, chronic or subclinical upper genital tract infection in women. In: Holmes KK, Mardh PA, Sparling PF, Wiener PJ, eds. Sexually transmitted diseases, 2nd ed. New York: McGraw-Hill, 1990: 615-620. Gates W, Rolfs RT, Aral SO. Sexually transmitted diseases, pelvic inflammatory disease and infertility: an epidemiologic update. Epidenziol Rev 1990; 12: 199-220. Hadgu A, Koch G, Westrom L. Analysis of ectopic pregnancy data using marginal and conditional models. Star Med 1997; 16: 2403-17. Hadgu A, Westrom L, Brook CA, Reynolds GH, Thompson SE. Predicting acute pelvic inflammatory disease: A multivariate analysis. Am J Obster Gynecol 1986; 155: 954-60. Kahn JG, Walker CK, Washington AE, Landers DV, Sweet RL. Diagnosing pelvic inflammatory disease. A comprehensive analysis and consideration for developing a new model. JAMA 1991; 266: 2594-604. Jacobson L, Westrom L. Objectivized diagnosis of acute pelvic inflammatory disease. AnzJ Obsret Gym-ml 1969; 105: 1088~98. Sellers J, Mahony J, Goldsmith C, et al. The accuracy of clinical findings and laparoscopy in pelvic inflammatory disease. Am J ObAtcr Gym01 1991; 164: 113-20. Wright N, Laemmle D. Acute pelvic inflammatory disease in an indigent population. AmJ Obstet Gynecol 1968; 101: 979-90. Westrom L. Incidence, prevalence and trends of acute pelvic inflammatory disease and its consequences in industrialized countries. AmJ Obstet Gynecol 1980; 138: X80-92. Curran J. Economic consequences of pelvic inflammatory disease in the United States. Am J Obstet Gynecol 1980; 138: 848-5 1. Washington AE, Katz P. Cost and payment source for pelvic inflammatory disease: trends and projections, 1983 through 2000. JAMA 1991; 266: 2565-69. Westrom L, Joesoef R, Reynolds G, Hadgu A, Thompson SE. Pelvic inflammatory disease and infertility. A cohort study of 1844 women with laparoscopically verified disease and 657 control women with normal laparoscopic results. Sex Transm Dis 1992; 19: 1X5-92. Adler MW. Trends for gonorrhea and pelvic inflammatory disease in England and Wales and for gonorrhea in a defined population. Am J Obsret Gym01 1980; 138: 901-04. Eschenbach DA, Buchanan TM, Pollock HM, et al. Polymicrobial etiology of acute pelvic inflammatory disease. N EnglJ Med 1975; 293: 166-71. Sweet RL, Draper DL, Hadley WK. Etiology of acute salpingitis: influence of episode, number and duration of symptoms. Obstet Gym01 1981; 58: 62-6X. Hemsell DL, Nobles BJ, Heard MC, Hemsell PG. Upper and lower
25
26
27
28
29 30
31
32
36
37
38
39
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reproductive tract bacteria in 126 women with acute pelvic inflammatory disease. Microbial susceptibility and clinical response to four therapeutic regimens. J ReprodMed 1988; 33: 799-805. Ripa T. Epidemiologic control of genital Chlamydia mchomatis infections. ScandJ Infect Di.s Suppl 1990; 69: 157-67. Eilard T, Brorson JE, Hamark B, Forsman L. Isolation of Chlamydia in acute salpingitis. &and J In& Dis Suppl 1976; 9: X2-84. Mardh PA, Ripa T, Svensson L, Westrom L. Chlamydia trachomatis infection in patients with acute salpingitis. NEnglJMed 1977; 296: 1377-79. 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 197X; 54: 247-50. Ripa T, Forslin L, Daniclsson D, Falk V. Frequency of gonococcal and chlamydial infections in patients with laparoscopically verified acute salpingitis in 1970 and 1980; epidemiological considerations. In: Mardh PA, Holmes KK, Oriel JD, Piot P, Schachter J, eds. Chlamydial Infections. Amsterdam: Elsevier Biomedical Press, 1982; 179-82. Westrom L, Svcnsson L, Wolner-Hansen I’, Mardh PA. Chlamydial and gonococcal infections in a defined population of women. ScandJ InfectDis Stcppl 1982; 32: 157-62. Kamwendo F, Forslin L, Bodin L, Danielsson D. Decreasing incidencrs of gonorrheaand chlamydia-associated acute pelvic inflammatoty disease. A 25-year study from an urban area of central Sweden. Sex Transm Dis 1996; 23: 384-91. Kamwendo F, Forslin L, D&&son D. Epidemiology and aetiology of acute non-tuberculous salpingitis: a comparison between the early 1970s and the early 1980s with special reference to gonorrhoea and use of intrauterine contraceptive device. Genitourirr Med 1990; 66: 324-29. Westrom L, Bengtsson LP, Mardh PA. The risk of pelvic inflammatory disease in women using intrauterine contraceptive devices as compared to non-users. Lancet 1976; ii: 221-24. Lee NC, Rubin GL, Borwki R. The intrauterine device and pelvic inflammatory disease revisited: new results from the women’s health study. Obstet Gynecol 1988; 72: 1-6. Kihlstrom E, Danielsson D. Advances in biology, management and prevention of infections caused by Chlamydia trachonzatis and Neissena gonowhoeae. Curr Opin Infect Dh 1994; 7: 25-33. Westrom L. Decrease in incidence of women treated in hospital for acute salpingitis in Sweden. Genirourin Med 1988; 64: 59-63. Division of STD Prevention. Sexually Transmitted Disease Surveillance, 1996. US Depatrm@nt of Health and Human Services, Public Health Service. Atlanta: Centers for Disease Control and Prevention, 1997. Centers for Disease Control and Prevention. 1998 guidelines for treatment of sexually transmitted diseases. MMWR Morb Movral IV’& Rep 199X; 46: 79-85. Johansson E, Moi H, For& L, Danielsson D. Prevalence of chlamydia infection, gonorrhoea and nonspecific urethritis in regular sexual partners of women with acute salpingitis [abstr 1 X3]. VII International Meeting of the International Society for STD Research; 1987: Atlanta, GA, USA. Kamwendo F, Johansson E, Moi H, Forslin L, Danieisson D. Gonorrhea, genital chlamydial infection and nonspecific urethritis in male partners of women hospitalized for acute pelvic inflammatory disease. Sex Transm Dis 1993; 20: 143-46. Sellers J, Mahony JB, Chernesky MA, Groves DJ, Rath DJ. Male contact tracing in a community-based study of confirmed acute pelvic inflammatory disease[abstr 1841. VII International Meeting of the International Society of STD Research; 1987: Atlanta, GA, USA. Washington AE, Gates Jr W, Wasserheit JN. Preventing pelvic inflammatory disease. JAMA 1991; 266: 2574-80. Coutinho RA, Rijsdijk AJ, van den Hoek JAR, Leentvaar-Kuijpers A. Decreasing incidence of PID in Amsterdam. Geniroutin Med 1992; 68: 353-55. Scholes D, Stergachis A, Heidrich FE, Andrilla H, Holmes KK, Stamm WE. Prevention of pelvic inflammatory disease by screening for cervical chlamydial infection. N EnglJMed 1996; 334: 1362-66. Falk V. Treatment of acute non-tuberculous salpingitis with antibiotics alone and in combination with glucocorticoids. Acza Obstel Gym01 &and 1965; 44 (suppI6): l-1 18. Washington AE, Berg AO. Preventing and managing pelvic inflammatory disease: Key questions, practices and evidence. 3 Fum Pratt 1996; 43: 2X3-93.
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