Unsuspected chronic pelvic inflammatory disease in the infertile female
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1 FERTILITY AND STERILITY Copyright c 1983 The American Fertility Society Printed in U.SA. Unsuspected chronic pelvic inflammatory disease in the infertile female David L. Rosenfeld, M.D. * Steven M. Seidman, M.D. Richard A. Bronson, M.D. Gerald M. Scholl, M.D. Division of Human Reproduction, Department of Obstetrics and Gynecology, North Shore University Hospital, Cornell University Medical College, Manhasset, New York Diagnostic laparoscopy performed during an infertility evaluation identified 80 patients with hydrosalpinges (12% of all laparoscopic examinations performed for infertility). Despite these findings, only 20 (25%) of these patients reported a prior episode of acute pelvic inflammatory disease (PID), and only 18 (22.5%) had complaints of pelvic pain. Compared with a matched group of infertility patients with no endoscopic evidence of prior pelvic infection, those patients with hydrosalpinges were more likely to have used an intrauterine device and were less likely to have used an oral contraceptive. Since "silent" PID is a potential cause of infertility, endoscopic visualization of the female reproductive organs should be considered during the infertility evaluation. Moreover, in view of its insidious nature, the diagnosis of PID should be considered in a young sexually active patient with gynecologic complaints. Fertil Steril 39:44, 1983 The common occurrence of asymptomatic pelvic inflammatory disease (PID) and its sequelae have only recently been recognized. I - 3 Physicians evaluating an infertile female frequently perform diagnostic endoscopy on the basis of a history of pelvic pain or prior infection. This retrospective study was undertaken to evaluate prior gynecologic history in patients with chronic PID documented at the time of laparoscopy. MATERIALS AND METHODS The records of all patients undergoing diagnostic laparoscopy performed by the authors between Received February 5, 1982; revised and accepted August 12, *Reprint requests: David L. Rosenfeld, M.D., Department of Obstetrics and Gynecology, North Shore University Hospital, 300 Community Drive, Cornell University Medical College, Manhasset, New York Rosenfeld et ai. Unsuspected chronic PID January 1977 and January 1981 as part of an infertility evaluation were reviewed. All patients had prior assessment of insemination and ovulatory factors. A history of pelvic pain, prior gynecologic infections, age at first coitus, prior contraceptive usage, pregnancy history, and other pelvic surgery were extracted from the records. Patients with infertility and unilateral or bilateral hydrosalpinges were compared with a randomly selected group of infertility patients who had no evidence of prior pelvic infection, noted at the time of laparoscopy. The duration of contraceptive use and the number of sexual partners could not be determined from these records. The results were analyzed statistically by X 2 analysis. Laparoscopy was performed in patients with more than 1 year of infertility who had normal insemination and ovulatory factors or who failed to conceive after adequate treatment of these conditions.
2 Table 1. Characteristics of Control and Study Populations U No. of patients Mean age Mean duration of infer tility (months) Primary infertility Secondary infertility Age at first coitus Infertility Infertility patients with patients with hydrosalpinges out hydrosal (study group) pinges (controls) (20--39) 40 (2-144) (16-30) UDifferences not statistically significant. RESULTS (24-46) 38.5 (6-120) (16-36) Of the 663 patients undergoing diagnostic laparoscopy as part of an evaluation for infertility from January 1977 to January 1981, 80 patients had hydrosalpinges (12% of all laparoscopic examinations performed because of infertility). All patients in this study were residents of an affluent suburban community. The patients' ages, duration of infertility, and prior reproductive histories were similar in both the study and control populations and are listed in Table 1. The study group was found to have a younger age at first coitus; however, this finding was not statistically significant. Laparoscopic findings in the control group are listed in Table 2. The medical histories of the 80 patients with hydrosalpinges are compared with those in the control group in Table 3. Only 20 patients (25%) with laparoscopically documented chronic PID recollected a prior episode of acute PID. There were no significant differences between the two groups in prior pregnancy history, therapeutic abortion, pelvic surgery, or appendicitis. Four patients (5%) in the study group, however, had had a prior ectopic pregnancy. There was only one ectopic pregnancy in the control group. This difference, however, although suggestive, was not significant. The study group was five times more likely to have used an intrauterine device (IUD) (27.5% versus 5%; P < 0.001) and less likely to have used an oral contraceptive (OC) (36% versus 57.5%; P < 0.025) or mechanical method of contraception (7.5% versus 24%; P < 0.01). The duration of contraceptive use could not be determined from this study. The 20 study patients with a history of prior acute PID were compared with the remaining 60 patients within the study group who had no history of prior infection, and the results are shown in Table 4. Patients with a prior history of acute PID were more likely to have been users ofiuds (10 of20 patients [50%] versus 12 of60 [20%]) and have symptoms of chronic pelvic pain (7 of 20 [35%] versus 11 of60 [18%]). While those patients with chronic PID and no history of prior acute PID were more likely to have had a voluntary pregnancy termination (12 of60 [20%] versus 1 of 20 [5%]), this difference was not statistically significant. Of the 80 patients with documented chronic PID, 20 patients had no prior history of pelvic infection, IUD use, termination of pregnancy, prior incomplete abortion or puerperal sepsis, appendicitis, or pelvic surgery, all factors which may suggest a potential cause. Despite the presence of hydrosalpinges, only 18 patients (22.5%) had pelvic pain. DISCUSSION The demonstration of hydrosalpinges at the time of laparoscopic examination for infertility in 12% of all such examinations among this group of patients from an affluent suburban community reinforces current estimates of sexually transmitted disease and emphasizes the insidious nature ofpid. The current epidemic ofvenereally transmitted diseases has had and will continue to have a large and far-reaching impact on the present and future health of younger members of our society.4 Recent estimates suggest that between 500,000 and 1 million women in the United States will suffer from acute salpingitis or its sequelae each year.l, 5, 6 These sequelae include not only sterility but also chronic pelvic pain and ectopic pregnancy. The overall impact on public health is substantial. Westrom 7 has shown previously that approximately 20% of patients known to have acute salpingitis later become infertile. An estimated 60,000 females will be rendered infertile in the United States each year because ofpid. 1 In addi- Table 2. Clinical Diagnosis in Control Population U Endometriosis Pelvic adhesionsb Myomata Normal pelvic organ Asherman's syndrome c Ovarian cyst UEighty patients. bpostsurgicai. CHysteroscopic diagnosis Rosenfeld et al. Unsuspected chronic PID 45
3 Table 3. Comparison of Prior Medical, Surgical, and Contraceptive History and Pelvic Symptoms in Infertility Patients with Proven Chronic Pelvic Inflammatory Disease and Controls Study ~oup (80 patients) Control group (SO patients) Relative risk Pvalue History acute PID Therapeutic abortion NSc Incomplete abortion NS Ectopic pregnancy NS Puerperal infection NS Appendicitis NS Prior pelvic surgery 19 a 14b 1.5 NS Contraceptive use Oral IUD Mechanical Symptom of pelvic pain NS aincludes six patients with laparotomy for removal of a tuboovarian abscess and four patients with salpingectomy for ectopic pregnancy. bincludes one patient with a salpingectomy for an ectopic pregnancy. CNot significant. tion, there is nearly a fourfold increase in the risk of subsequent ectopic pregnancy in these patients. The number of ectopic pregnancies has tripled in the United States from 1967 to 1977 in parallel with the increase in sexually transmitted diseases.5 An estimated 50% of all ectopic pregnancies are secondary to existing PID. Four of the 80 patients (5%) with chronic PID in the study previously had had an ectopic pregnancy. Since nontuberculous PID does not occur in the absence of sexual exposure,5 the change in adolescent sexual patterns in this country will have future medical and social implications. 8 This problem is suggested by the earlier age at first coitus in our study population with chronic PID. Unfortunately, the number of sexual partners or the frequency of coitus, variables which might be relevant to this review, could not be determined in this retrospective study. According to Curran,5 if the current rates of sexually transmitted disease continue, by the year 2000 over 10% of all young women who reached reproductive age in 1970 will have been sterilized by PID alone, a doubling of the current estimate of the prevalence of nonsurgical sterility. In the present study, 27.5% of those infertile patients (22 of 80) with chronic PID had previously used an IUD, more than a fivefold increase over the IUD usage in the control population. Of those 20 patients with a history of prior acute PID, 10 (50%) were previous IUD users. In those 80 infertile patients with no laparoscopic evidence of pelvic infection, 46 (57.5%) had used an OC, as compared with 29 (35%) of the 80 patients in the study group. 46 Rosenfeld et ai. Unsuspected chronic PID Contraceptive usage has been shown to influence the risk of pelvic infection. 9 While no longterm prospective study has demonstrated an increase in infertility in women who had used IUDs, the IUD has been demonstrated to increase the risk of pelvic infection 1.5- to 9.2-fold, as compared with the risk of nonusers of contraception. 1O, 11 OCs, on the contrary, decrease the risk of pelvic infection to 0.6, as compared with the risk of women using no contraception. Moreover, OC use will lower the risk for acute PID in women who have a positive gonococcal cervical culture. 12 Table 4. Comparison of Prior Medical, Surgical, and Contraceptive History and Pelvic Symptoms in Infertility Patients with Proven Chronic Pelvic Inflammatory Disease Both With and Without a Prior History of Acute Pelvic Inflammatory Disease History of No histo~ acute PID of acute P D P value No. of patients NSd Therapeutic abortion 1 12 NS Incomplete abortion 2 8 NS Ectopic pregnancy 1 3 NS Puerperal infection 2 3 NS Appendicitis 2 7 NS Prior pelvic sur- 7 a 12b NS gery Contraceptive usec Oral 7 22 NS IUD Mechanical Symptom of pel NS vic pain aincludes six patients with laparotomies for unilateral tuboovarian abscesses and one patient with an ectopic pregnancy. bincludes three patients with ectopic pregnancies. cincludes one patient who had used both an oral contraceptive and a diaphragm. dnot significant.
4 Women who have never been pregnant and used an IUD are at greater risk of developing PID than are previously pregnant women.13, 14 This relative risk must be considered prior to the insertion of an IUD in a woman desiring future pregnancies. Another risk factor for pelvic infection is pregnancy termination. Nearly 1 million legal abortions are performed each year in the United States, and approximately 0.5% of these are complicated by acute salpingitis within 3 weeks of the operation. 1 Nevertheless, in the present study, there was no significant difference in the number of pregnancy terminations in the study patients (16%) and the control group (11 %). Despite an awareness of the severe sequelae of PID and the recognition that prompt diagnosis and treatment may lessen the subsequent impact of the acute infection,7 many patients are seen for treatment of infertility with no history that would suggest a prior pelvic infection. Seventyfive percent of 80 patients in the present study undergoing diagnostic laparoscopy for infertility who were found to have chronic PID ("silent PID") had no history of a prior episode of acute pelvic infection. Twenty percent of this group had nothing in their medical histories (acute PID, pregnancy termination, IUD use, pelvic surgery, appendicitis, puerperal sepsis) to suggest a possible cause for the chronic PID. The liberal use of laparoscopy for evaluation of acute pelvic pain documented the difficulty of diagnosing PID on the basis of clinical factors alone. I, 2, 15, 16 Previous investigators have demonstrated a low level of accuracy in diagnosis based solely on clinical criteria such as history, physical examination, and common laboratory tests. I, 2, 15, 16 Laparoscopy has demonstrated that nearly one-third of patients with a clinical diagnosis of acute PID had other problems or no disease at all.2, 15, 16 Moreover, in a Swedish study,2 15% of confirmed cases of acute salpingitis were initially suspected clinically to be other disorders. The routine use of laparoscopy in the diagnosis of acute salpingitis shows 95% accuracy.2 There is often a poor correlation between the clinical picture and the laparoscopic diagnosis of patients with suspected acute salpingitis, which may affect medical judgment and delay appropriate treatment, possibly worsening the long-term prognosis. Symptoms and signs are variable and often atypical. Many patients with tubal infections are afebrile and have a benign clinical course. 1, 2, 15 Some patients with tubal infection have no symptoms at all.3 Nevertheless, while Westrom has noted a very high pregnancy rate after infections with only mild tubal inflammatory changes {97.4%),7 there is as yet no documentation that early laparoscopic diagnosis of acute salpingitis would improve treatment and decrease long-term disabilityp PID can be initiated by any of several organisms. Swedish investigators have demonstrated that the intensity of symptoms as well as the severity of tubal inflammation may show considerable variation for different microbiologic organisms The relationship of Chlamydia trachomatis infection and "silent" PID has been noted. I, 19, Henry-Suchet et al.24 isolated C. trachomatis from the fallopian tubes of infertile women with no history of prior salpingitis but with occluded tubes noted at the time of laparoscopy. Svensson et al.25 have demonstrated that salpingitis associated with C. trachomatis is clinically more indolent, with a longer mean duration of pain and less fever than in patients with gonococcal salpingitis. Studies in young adult women in industrialized Western countries have demonstrated a high prevalence of genital infection with C. trachomatis. 19 Serologic evidence suggests that approximately 20% of all salpingitis cases in the United States are associated with C. trachomatis. 23 In a group of infertile patients, Punnonen et al.26 have demonstrated a higher prevalence of chlamydial antibodies among infertile women than among pregnant controls. In summary, the frequent occurrence of unsuspected "silent" chronic PID in infertile patients stresses the need for thorough evaluation based on more than historic and clinical criteria alone. The liberal use of laparoscopy is encouraged in infertile patients despite the absence of historic factors that might suggest tubal disease. Moreover, the silent nature of PID, as well as the increased prevalence within our society, makes new efforts at surveillance and treatment mandatory. The effects of contraception on future reproduction must be considered by individuals utilizing family planning methods. REFERENCES 1. Westrom L: Incidence, prevalence, and trends of acute pelvic inflammatory disease and its consequences in industrialized countries. Am J Obstet Gyneco1138:88, 1980 Rosenfeld et al. Unsuspected chronic PID 47
5 2. Jacobson L: Differential diagnosis of acute pelvic inflammatory disease. Am J Obstet GynecoI138:1006, Henry-Suchet J, Loffredo V: Chlamydial and mycoplasma genital infections in salpingitis and tubal sterility. Lancet 1:539, St. John RK, Brown ST, Tyler CW Jr: Pelvic inflammatory disease. Am J Obstet Gynecol 138:845, Curran JW: Economic consequences of pelvic inflammatory disease in the United States. Am J Obstet Gynecol 138:848, Feldman YM, Nikitas JA: Pelvic inflammatory disease. NY State J Med 80:635, Westrom L: Effect of acute pelvic inflammatory disease on fertility. Am J Obstet Gyneco1121:707, Zelnik M, Kantner JF: Sexual activity, contraceptive use and pregnancy among metropolitan-area teenagers: Fam Plann Perspect 12:230, Burkman RT: Association between intrauterine device and pelvic inflammatory disease. Obstet Gynecol 57:269, Senanayake F, Kramer DC: Contraception and the etiology of pelvic inflammatory disease: new perspectives. Am J Obstet Gynecol 138:852, Burkman RT: Intrauterine device use and the risk of pelvic inflammatory disease. Am J Obstet Gynecol 138:861, Eschenbach DA, Harnisch JF, Holmes KK: Pathogenesis of acute pelvic inflammatory disease: role of contraception and other risk factors. Am J Obstet Gynecol 128:838, Eschenbach DA, Holmes KK: Acute pelvic inflammatory disease: current concepts in pathogenesis, etiology and management. Clin Obstet Gynecol 18:35, Westrom L, Bengtsson LP, Mardh PA: The risk of pelvic inflammatory disease in women using intrauterine contraceptive devices as compared to non-users. Lancet 2:221, Jacobson L, Westrom L: Objectivized diagnosis of acute pelvic inflammatory disease. Am J Obstet Gynecol 105: 1088, Bartsich EG, Dillon TF: Acute pelvic inflammatory disease: laparoscopic assessment. NY State J Med 81:25, Ledger WJ: Laparoscopy in the diagnosis and management of patients with suspected salpingo-oophoritis. Am J Obstet GynecoI138:1012, Holmes KK, Eschenbach DA, Knapp JJ: Salpingitis: overview of etiology and epidemiology. Am J Obstet Gynecol 138:893, Mardh P: An overview of infectious agents of salpingitis, their biology, and recent advances in methods of detection. Am J Obstet Gynecol 138:933, Eschenbach DA, Buchanan TM, Pollock HM, Forsyth PS, Alexander ER, Lin J, Wang S, Wentworth BB, McCormick WM, Holmes KK: Polymicrobial etiology of acute pelvic inflammatory disease. N Engl J Med 293:166, Sweet RL, Mills J, Hadley KW, Blumenstock E, Schachter J, Robbie MO, Draper DL: Use of laparoscopy to determine the microbiologic etiology of acute salpingitis. Am J Obstet Gynecol 134:68, Lukasik J: A comparative evaluation of the bacteriological flora of the uterine cervix and fallopian tubes in cases of salpingitis. Am J Obstet Gynecol 87:1028, Sweet RL, Draper DL, Schachter J, James J, Hadley KW, Brooks SF: Microbiology and pathogenesis of acute salpingitis as determined by laparoscopy: what is the appropriate site of sample? Am J Obstet GynecoI138:985, Henry-Suchet J, Catalan F, Loffredo V, Serfaty D, Siboulet A, Perol Y, Sanson MJ, Debache C, Pigeau F, Coppin R, DeBrux J, Poynard T: Microbiology of specimens obtained by laparoscopy from controls and from patients with pelvic inflammatory disease or infertility with tubal obstruction: Chlamydia trachomatis and Ureaplasma urealyticum. Am J Obstet Gynecol 138:1022, Svensson L, Westrom L, Ripa KT, Mardh P: Differences in some clinical and laboratory parameters in acute salpingitis related to culture.and serologic findings. Am J ObstetGynecoI138:1017, Punnonen R, Terho P, Nikkanen V, Meurman 0: Chlamydial serology in infertile women by immunofluorescence. Fertil Steril 31:656, Rosenfeld et al. Unsuspected chronic PID
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