More than 800,000 women in the United States are estimated to be diagnosed with pelvic inflammatory disease (PID) each year.1,2 Tubo-ovarian abscess is a complication of PID that occasionally involves other adjacent pelvic organs. Although studies in the 1990s showed that approximately 10–30% of hospitalized patients with PID have tubo-ovarian abscess,3,4 the reported prevalence of tubo-ovarian abscess decreased to 2.4% by 2006.5 Tubo-ovarian abscess is a serious and potentially life-threatening condition requiring aggressive medical and surgical therapies. Approximately 25–30% of all patients require surgical intervention, according to data from large case series.3,6–8 Data from the 1960s and 1970s suggest a mortality rate ranging from 1.7 to 7.1%9–11; the Centers for Disease Control and Prevention reported that mortality from PID was less than 1% in 2017.12
Treatment of PID complicated by tubo-ovarian abscess includes broad-spectrum antibiotics, minimally invasive drainage procedures, and potentially surgery. A recent study reported clinical experience with laparoscopic surgery to treat PID with or without tubo-ovarian abscess.6 The potential benefits over laparotomy include less invasiveness, smaller incisions and less postoperative pain. In the guidelines on PID and tubo-ovarian abscess published by the Japan Society of Obstetrics and Gynecology in 2011 and 2014, there are no specific criteria or recommendations for surgical intervention.13,14 American, European, and Australian guidelines for PID treatment also show no recommendation for surgical procedures.15–17 However, the 2011 UK National Guideline for the Management of PID state that laparoscopy may help with early resolution of the disease by dividing adhesions and draining pelvic abscesses.18
A small case series suggested better outcomes with a laparoscopic approach than with laparotomy.19 However, previous observational reports could not adequately adjust for patients' background characteristics, including severity, preexisting comorbidities, and hospital characteristics.6,20,21 The aim of this study was to use data from a nationwide Japanese inpatient database to compare surgical outcomes after laparoscopy compared with laparotomy in patients with PID and tubo-ovarian abscess.
For this retrospective cohort study, we used the Diagnosis Procedure Combination database, a national inpatient database for acute-care inpatients in Japan, the details of which have been described elsewhere.22 Briefly, approximately 1,200 hospitals, including all 82 academic hospitals, participate in the database and provide data for approximately 8,000,000 admissions annually, which represents approximately 50% of all acute-care inpatients in Japan. Academic hospitals are obliged to participate in the database, whereas the participation of community hospitals is voluntary. The database contains discharge abstracts and administrative reimbursement data for inpatient episodes, as well as the following: unique hospital identifiers; dates of admission and discharge; patient details (age, sex, body height, and weight); smoking status (nonsmoker, or both current and past smoker); type of admission (planned or emergency); primary and secondary diagnoses; preexisting comorbidities on admission and complications after admission; medical procedures, including types of surgery (Japanese original codes); medications and devices used; in-hospital mortality; pregnancy status (pregnant or not); and gestational age on admission and delivery during hospitalization. Diagnoses, comorbidities, and complications are recorded using International Classification of Diseases, 10th Revision (ICD-10) codes and text data in Japanese. The database contains no laboratory data or findings on gynecologic examination (including results of ultrasonic echography or magnetic resonance imaging, and vaginal bacteriologic culture). Attending physicians are encouraged to record the diagnoses accurately by linking data entries with reimbursement for health care costs. A previous study showed that the validity of the diagnostic records in the Diagnosis Procedure Combination database is generally high, and that the sensitivity and specificity of the primary diagnoses are 50–80% and 96%, respectively. The specificity and sensitivity of procedures were found to exceed 90%.23
We identified all adult patients aged 18 years or older who were diagnosed with PID (ICD-10 code, N739 and N980) with or without tubo-ovarian abscess (ICD-10 code, N709) and were treated in a participating hospital from July 2010 to March 2016. We excluded patients who were pregnant, had cancer, or for whom data were missing. We compared outcomes in included patients undergoing laparoscopic surgery compared with laparotomy.
We categorized age as 19 and younger, 20–29, 30–39, 40–49, 50–59, and 60 years and older. The database also provides important clinical scores, including Japan Coma Scale scores. The Japan Coma Scale correlates well with the Glasgow Coma Scale score, with consciousness scored at 100 points on the Japan Coma Scale being equivalent to a score of 6–9 on the Glasgow Coma Scale. We used the Japan Coma Scale score as a confounder because we estimated patients' severity based on whether alert consciousness was present. We categorized the Japan Coma Scale scores into two groups: alert (Japan Coma Scale=0) and disturbance of consciousness (Japan Coma Scale=1–300).24,25
Assessed outcomes included operation duration; number of blood transfusions; postoperative length of hospital stay; postoperative complications including bowel injuries, urinary tract injury (ICD-10 code, S3710), wound infection (T814), and deep vein thrombosis or pulmonary thromboembolism (I801, I802, I269); revision surgery during the same hospitalization; and in-hospital deaths. We selected these outcomes because they are important and objective short-term perioperative outcomes. The database did not include long-term outcomes, such as the rate of infertility, ectopic pregnancy, and chronic pelvic pain after discharge.
We performed one-to-one propensity-score matching between the laparoscopy and laparotomy groups.26 We estimated propensity scores with a logistic regression model for the likelihood of undergoing laparoscopic surgery as a function of the following variables: age, body mass index, disturbance of consciousness on admission (Japan Coma Scale=1–300), smoking, teaching hospital, use of ambulance, use of intensive care unit just after admission, emergency surgery, need for hysterectomy, preoperative length of stay, diagnosis of Chlamydia trachomatis or Neisseria gonorrhoeae infection, tubo-ovarian abscess, type of antibiotics as initial treatment, and preexisting comorbidities on admission (diabetes mellitus, bacterial vaginosis, ovarian tumor or cyst, ovarian endometrioma, endometriosis, adenomyosis, uterine myoma, diverticulitis, appendicitis, inflammatory bowel disease, diffuse peritonitis, and sepsis). Inflammatory bowel disease included Crohn's disease and ulcerative colitis. However, unobserved variables such as size of the tubo-ovarian abscess, laboratory data including blood testing, severity of intrapelvic adhesions, and surgeons' skill were not included when estimating propensity scores because the database we used did not include these variables.
The propensity score–matched analysis was performed using nearest-neighbor matching without replacement within a caliper of 0.25 standard deviations of pooled propensity scores.26 After matching, we assessed the balance of the baseline variables in the matched patient groups with the standardized difference. We considered an absolute standardized difference at least 10% to indicate a meaningful imbalance.27
Comparing outcomes between the laparoscopy and laparotomy groups, categorical variables were shown as numbers and percentages and were compared using Fisher exact test. Continuous variables were shown as mean and standard deviation or median and interquartile range, and these data were compared using Student t test or the Mann–Whitney U test. We also estimated risk differences and 95% CIs for the primary and secondary outcomes (excluding length of hospital stay). All statistical analyses were performed using Stata 15.0. All tests were 2-tailed, and the threshold for significance was P<.05.
This study was approved by the Institutional Review Board of The University of Tokyo, which waived the requirement for informed patient consent because of the anonymous nature of the data.
During the study period, we identified 30,917 hospitalized patients with a diagnosis of PID or tubo-ovarian abscess in 1,206 hospitals and identified 27,841 of these patients as eligible. Of the eligible patients, 2,284 (8.2%) had undergone percutaneous or transvaginal minimally invasive drainage procedures only and 4,419 (15.9%) had undergone surgical interventions (including 3,670 by laparotomy and 749 by laparoscopy). Forty-three percent (1,017/2,463) of the patients underwent minimally invasive drainage to treat tubo-ovarian abscess. Sixty-three (1.4%), 18 (0.4%), and 16 (0.4%) patients were diagnosed as having appendicitis, diverticulitis, and inflammatory bowel disease in addition to PID, respectively. Hysterectomy was performed for 28.6% (n=1,262) of the surgical patients. Among patients who underwent hysterectomy, approximately 95% were aged 40 years or older (n=1,196/1,262), and 57% (n=716/1,262) had gynecologic benign comorbidities that included uterine leiomyomas, adenomyosis, ovarian tumors, and endometriosis. Additionally, 22% (n=282) of the patients who underwent hysterectomy also had tubo-ovarian abscess on admission, and the rate of tubo-ovarian abscess complication was higher in the laparotomy group (272/1,188; 22.9%), compared with the laparoscopy group (10/74; 13.5%). Propensity-score matching created 740 pairs in the laparotomy and laparoscopy groups (Fig. 1).
Table 1 shows the baseline characteristics of the unmatched and propensity score–matched groups. In the unmatched group, the laparoscopy group was significantly more likely to have younger patients, ovarian cysts, endometriosis, emergency surgery, and less likely to have obesity, admission to the intensive care unit immediately after admission, diabetes mellitus, adenomyosis, uterine leiomyomas, hysterectomy and shorter preoperative length of hospital stay compared with the laparotomy group. The distributions of the variables in the propensity score–matched groups were well-balanced.
Table 2 shows the postsurgical complications among all eligible women before propensity-score matching. There were significantly more patients with postsurgical complications in the laparotomy group compared with the laparoscopy group (P<.001). Although bowel injury and wound infection were major causes of complications in both groups, bowel injury was more likely to occur in the laparotomy group.
Table 3 shows a comparison of outcomes between laparoscopic surgery and laparotomy in the propensity score–matched groups. Compared with the laparotomy group, the laparoscopy group was significantly associated with fewer blood transfusions and shorter operation duration. We also found significant differences between the laparoscopy and laparotomy groups for postoperative length of hospital stay (laparoscopy group: median 5 days [interquartile range 4–8 days], laparotomy group: median 7 days [interquartile range 6–10 days]; P<.001). There were no significant differences between the groups regarding surgical complications, revision surgeries during the same hospitalization, and mortality.
Laparoscopic surgery may have clinical advantages over laparotomy in patients with moderate to severe PID requiring surgical intervention. We observed fewer blood transfusions, shorter operation duration, and decreased postoperative length of hospital stay in patients undergoing laparoscopy, but found no significant differences in surgical complications, revision surgery, or in-hospital mortality. Propensity-score matching was able to adjust for differences in patients' baseline characteristics and disease severity. For example, after matching pairs, the rate of postsurgical complications decreased from 6.6% to 3.9% in the laparotomy group, indicating that patients undergoing laparotomy had higher baseline preoperative PID severity.
Invasive treatments (including surgery and drainage procedures) are reportedly required in approximately 25–30% of patients with moderate to severe PID with tubo-ovarian abscess.3,6–8 In our study, 24.1% of patients underwent invasive treatments (including 15.9% undergoing surgery and 8.2% undergoing minimally-invasive drainage procedures, only), and these results are comparable with previous reports.3,6–8
Increasing numbers of physicians performing advanced laparoscopic surgery should allow for expanded minimally invasive approaches to PID, including abscess debridement or washout. However, current evidence is limited regarding the usefulness of laparoscopic procedures in patients with severe PID, with available evidence from small studies only.19,28,29
More than one quarter of the surgical patients underwent hysterectomy in this study. Although we could not confirm the indications for hysterectomy owing to limitations of the database, 95% were at least 40 years of age and presumably not interested in future fertility. Approximately half of these patients also had concurrent gynecologic benign comorbidities that may have contributed to the decision to perform hysterectomy. Finally, because one quarter had a tubo-ovarian abscess, the severity of pelvic inflammation and clinical concern about the effectiveness of antibiotics may have led to the decision about hysterectomy.30–32
A recent retrospective study of patients with tubo-ovarian abscess in Turkey reported that 26% of patients who underwent surgical treatment required subtotal or total hysterectomy,6 a percentage similar to findings in our study. Historically, total abdominal hysterectomy and bilateral salpingo-oophorectomy was performed to achieve complete removal of all infected tissue.3,33 Studies have shown that more conservative surgical interventions resulted in 10–20% of patients requiring revision surgery.34–36 In our study, the proportion of patients requiring revision surgery was low after both open and laparoscopic surgery. This may be attributable to recent advances in treatment strategies, including initial use of broad-spectrum antibiotics, developments in surgical techniques and devices, and intensive perioperative management.
The strengths of this study are the large sample size and the use of sophisticated statistical methods to reduce confounding bias in an observational study such as this. However, our study has several limitations. First, we used a retrospective and observational design, which precluded randomization. Even though propensity-score matching was performed to balance patients' background characteristics and adjust for confounding factors, there may still have been unmeasured confounders, including the results of laboratory tests, bacterial culture, size of intrapelvic abscess, and the presence of ruptured tubo-ovarian abscess. Second, because we used an administrative claim database as a data source, the recorded diagnoses may have been less accurate than for a planned cohort study. Third, we were unable to determine surgeons' skill and experience. Surgeries for tubo-ovarian abscess can be very complicated because of extensive intrapelvic adhesions and surrounding necrotic and inflamed tissues. Accordingly, consultation with skilled surgeons is recommended, especially for laparoscopic surgeries. Fourth, selection bias is possible secondary to intraoperative conversion of surgical procedures. The database allowed us to identify patients who initially underwent laparoscopic surgery but then received laparotomy to repair bowel or ureteral injury. We confirmed there were no such patients. However, we could not identify patients for whom initial laparoscopic surgery was converted to laparotomy because of adhesions, without bowel or ureteral injury; these patients were recorded as undergoing laparotomy. Also, our results cannot be directly generalized to patients with PID with or without tubo-ovarian abscess managed in non–Diagnosis Procedure Combination hospitals because the clinical data we used were all from Diagnosis Procedure Combination hospitals. Finally, we were unable to investigate long-term outcomes because the database does not provide postdischarge outcomes.
1. Sutton MY, Sternberg M, Zaidi A, St Louis ME, Markowitz LE. Trends in pelvic inflammatory disease hospital discharges and ambulatory visits, United States, 1985–2001. Sex Transm Dis 2005;32:778–84.
2. Centers for Disease Control. PID fact sheet. Atlanta (GA): Department of Health and Human Services; 2007.
3. Wiesenfeld HC, Sweet RL. Progress in the management of tuboovarian abscesses. Clin Obstet Gynecol 1993;36:433–44.
4. McNeeley SG, Hendrix SL, Mazzoni MM, Kmak DC, Ransom SB. Medically sound, cost-effective treatment for pelvic inflammatory disease and tuboovarian abscess. Am J Obstet Gynecol 1998;178:1272–8.
5. Mollen CJ, Pletcher JR, Bellah RD, Lavelle JM. Prevalence of tubo-ovarian abscess in adolescents diagnosed with pelvic inflammatory disease in a pediatric emergency department. Pediatr Emerg Care 2006;22:621–5.
6. Güngördük K, Guzel E, Asicioğlu O, Yildirim G, Ataser G, Ark C, et al. Experience of tubo-ovarian abscess in western Turkey. Int J Gynaecol Obstet 2014;124:45–50.
7. Lareau SM, Beigi RH. Pelvic inflammatory disease and tubo-ovarian abscess. Infect Dis Clin North Am 2008;22:693–708.
8. Reed SD, Landers DV, Sweet RL. Antibiotic treatment of tuboovarian abscess: comparison of broad-spectrum beta-lactam agents versus clindamycin-containing regimens. Am J Obstet Gynecol 1991;164:1556–61.
9. Rivlin ME, Hunt JA. Ruptured tuboovarian abscess: is hysterectomy necessary? Obstet Gynecol 1977;50:518–22.
10. Pedowitz P, Bloomfield RD. Ruptured adnexal abscess (tuboovarian) with generalized peritonitis. Am J Obstet Gynecol 1964;88:721–9.
11. Mickal A, Sellmann AH. Management of tubo-ovarian abscess. Clin Obstet Gynecol 1969;12:252–64.
12. Centers for Disease Control and Prevention. Pelvic inflammatory disease (PID)—CDC fact sheet. Available at: https://www.cdc.gov/std/pid/stdfact-pid-detailed.htm
. Retrieved February 15, 2019.
13. Minakami H, Hiramatsu Y, Koresawa M, Fujii T, Hamada H, Iitsuka Y, et al. Guidelines for obstetrical practice in Japan: Japan society of Obstetrics and Gynecology (JSOG) and Japan Association of Obstetricians and Gynecologists (JAOG) 2011 edition. J Obstet Gynaecol Res 2011;37:1174–97.
14. Minakami H, Maeda T, Fujii T, Hamada H, Iitsuka Y, Itakura A, et al. Guidelines for obstetrical practice in Japan: Japan society of Obstetrics and Gynecology (JSOG) and Japan Association of Obstetricians and Gynecologists (JAOG) 2014 edition. J Obstet Gynaecol Res 2014;40:1469–99.
15. Workowski KA, Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep 2015;64:1–137.
16. Ross J, Guaschino S, Cusini M, Jensen J. 2017 European guideline for the management of pelvic inflammatory disease. Int J STD AIDS 2018;29:108–14.
17. Sexual Health Society of Victoria. National management guidelines for pelvic inflammatory disease. Available at: https://www.mshc.org.au/HealthProfessional/MSHCTreatmentGuidelines/PelvicInflammatoryDisease(PID)#.W3UoCZP7Sb9
. Retrieved February 15, 2019.
18. Clinical Effectiveness Group, British Association for Sexual Health and HIV. UK national guideline for the management of pelvic inflammatory disease 2011. Available at: https://www.bashh.org/documents/3572.pdf
. Retrieved February 15, 2019.
19. Yang CC, Chen P, Tseng JY, Wang PH. Advantages of open laparoscopic surgery over exploratory laparotomy in patients with tubo-ovarian abscess. J Am Assoc Gynecol Laparosc 2002;9:327–32.
20. Roberts W, Dockery JL. Operative and conservative treatment of tubo-ovarian abscess due to pelvic inflammatory disease. South Med J 1984;77:860–3.
21. Chu L, Ma H, Liang J, Li L, Shen A, Wang J, et al. Effectiveness and adverse events of early laparoscopic therapy versus conservative treatment for tubo-ovarian or pelvic abscess: a single-center retrospective cohort study. Gynecol Obstet Invest 2019;4:1–9.
22. Matsui H, Jo T, Fushimi K, Yasunaga H. Outcomes after early and delayed rehabilitation for exacerbation of chronic obstructive pulmonary disease: a nationwide retrospective cohort study in Japan. Respir Res 2017;18:68.
23. Yamana H, Moriwaki M, Horiguchi H, Kodan M, Fushimi K, Yasunaga H. Validity of diagnoses, procedures, and laboratory data in Japanese administrative data. J Epidemiol 2017;27:476–82.
24. Tagami T, Matsui H, Fushimi K, Yasunaga H. Validation of the prognostic burn index: a nationwide retrospective study. Burns 2015;41:1169–75.
25. Tagami T, Matsui H, Fushimi K, Yasunaga H. Prophylactic antibiotics may improve outcome in patients with severe burns requiring mechanical ventilation: propensity score analysis of a Japanese nationwide database. Clin Infect Dis 2016;62:60–6.
26. Austin PC. Optimal caliper widths for propensity-score matching when estimating differences in means and differences in proportions in observational studies. Pharm Stat 2011;10:150–61.
27. Austin PC. Using the standardized difference to compare the prevalence of a binary variable between two groups in observational research. Commun Stat Simul Comput 2009;38:1228–34.
28. Molander P, Cacciatore B, Sjöberg J, Paavonen J. Laparoscopic management of suspected acute pelvic inflammatory disease. J Am Assoc Gynecol Laparosc 2000;7:107–10.
29. Goh WC, Beh ST, Chern B, Yap LK. A three year review on surgical treatment of tubo-ovarian abscess. Med J Malaysia 2002;57:292–7.
30. Elizur SE, Lebovitz O, Weintraub AY, Eisenberg VH, Seidman DS, Goldenberg M, et al. Pelvic inflammatory disease in women with endometriosis is more severe than in those without. Aust N Z J Obstet Gynaecol 2014;54:162–5.
31. Booth M, Beral V, Maconochie N, Carpenter L, Scott C. A case-control study of benign ovarian tumours. J Epidemiol Community Health 1992;46:528–31.
32. Terao M, Koga K, Fujimoto A, Wada-Hiraike O, Osuga Y, Yano T, et al. Factors that predict poor clinical course among patients hospitalized with pelvic inflammatory disease. J Obstet Gynaecol Res 2014;40:495–500.
33. Kaplan AL, Jacobs WM, Ehresman JB. Aggressive management of pelvic abscess. Am J Obstet Gynecol 1967;98:482–7.
34. Landers DV, Sweet RL. Tubo-ovarian abscess: contemporary approach to management. Rev Infect Dis 1983;5:876–84.
35. Ginsburg DS, Stern JL, Hamod KA, Genadry R, Spence MR. Tubo-ovarian abscess: a retrospective review. Am J Obstet Gynecol 1980;138:1055–8.
36. Sweet RL. Pelvic inflammatory disease. In: Sweet RL, Gibbs RS, editors. Infectious diseases of the female genital tract. 5th ed. Philadelphia (PA): Lippincott Williams and Wilkins; 2009:220–44.