Sexually Transmitted Diseases:
The Clinical and Economic Consequences of Screening Young Men for Genital Chlamydial Infection
GINOCCHIO, RACHEL H. S. MPH*; VEENSTRA, DAVID L. PharmD, PhD†; CONNELL, FREDERICK A. MD, MPH*; MARRAZZO, JEANNE M. MD, MPH‡
From the *Department of Health Services, Maternal and Child Health; †Pharmaceutical Outcomes Research and Policy Program; and ‡Department of Medicine, University of Washington, Seattle, Washington
The authors thank Patty Belestra for providing the Medicaid fee schedules for Washington State.
Supported by a grant from the Department of Health and Human Services, Health Resources and Services Administration (HRSA), Maternal and Child Health Bureau (research and training grant no. T 76 MC 00011 to Rachel Ginocchio).
Correspondence: Jeanne M. Marrazzo, MD, MPH, Division of Allergy and Infectious Diseases, University of Washington, Harborview Medical Center, Mailstop #359931, 325 Ninth Avenue, Seattle, WA 98104. E-mail: firstname.lastname@example.org
Received April 2, 2002,
revised July 3, 2002, and accepted July 8, 2002.
Background: Wide-scale application of urine-based screening of asymptomatic men for chlamydial infection has not been thoroughly assessed.
Goal: The goal was to compare clinical and economic consequences of three strategies: (1) no screening, (2) screening with ligase chain reaction (LCR) assay of urine, and (3) prescreening urine with a leukocyte esterase test (LE) and confirming positives with LCR.
Study Design: We used a decision analytic model.
Results: At a chlamydia prevalence of 5%, the no screening cost was $7.44 per man screened, resulting in 522 cases of pelvic inflammatory disease (PID) per 100,000 men. LE-LCR was most cost-effective, preventing 242 cases of PID over no screening at an additional cost of $29.14 per male screened. The LCR strategy prevented 104 more cases of PID than LE-LCR but cost $22.62 more per male screened. For this to be more efficient than LE-LCR, the LCR assay cost needed to decline to ≤$18.
Conclusion: At a chlamydia prevalence of 5%, LE-LCR is the most efficient use of resources. If LCR cost decreases or chlamydia prevalence increases, the LCR strategy is favored.
AN ESTIMATED 4 MILLION genital chlamydial infections occur each year in the United States, and 74% of all reported cases occur among 15- to 24-year-olds. 1 Up to 90% of chlamydial infections in women and 60% in men are asymptomatic and can result in serious upper-genital-tract and neonatal sequelae. 2,3 The annual direct and indirect costs of treating chlamydial infections and their sequelae are estimated at $2.0 billion. 4
In 2000, reported rates of chlamydial infection among women (404.1 per 100,000) were four times greater than among men (102.8 per 100,000). 1 Low reported rates among men may reflect that asymptomatic men are unlikely to seek routine screening and that many sex partners of infected women are not tested. 1 While large-scale screening programs for women have affected major declines in Chlamydia trachomatis prevalence in some areas, 5 these trends have stabilized. Therefore, asymptomatic men infected with C trachomatis are likely an unaddressed source of infection for women. Inclusion of men in strategies to prevent chlamydial infection is a logical next step in preventing disease transmission to women. Use of nucleic acid amplification technology (NAAT) to detect C trachomatis in urine obviates the need for urethral swabs, formerly a considerable barrier to testing asymptomatic men. While NAAT is more sensitive and as specific as the most commonly used diagnostic tests, it is more expensive.
Few cost-effectiveness studies of C trachomatis screening have focused on men. Of these, many were done before NAAT became available, relied on cost and outcome estimates from outside the United States, accounted for only the direct cost of the diagnostic test, and did not include the cost of treatment and sequelae or did not include the outcome of subclinical pelvic inflammatory disease (PID). 6–10 None formally considered the utility of prescreening urine for nonspecific inflammation in order to direct NAAT testing for C trachomatis. We assessed the cost, effectiveness, and cost-effectiveness of three strategies for detection of C trachomatis in a population of asymptomatic young men, using current United States costs. The three strategies were: (1) NS: no screening; (2) LCR: testing all young men with ligase chain reaction [LCR] assay of urine; and (3) LE-LCR: testing all young men with a leukocyte esterase [LE] strip test of urine, followed by confirmatory LCR. While inexpensive, the LE strip has low specificity and variable sensitivity for chlamydial infection.
A decision tree was developed to model events, costs, and clinical outcomes of chlamydial infection in a hypothetical cohort of 100,000 asymptomatic young men. The cohort was based on two groups of asymptomatic men universally tested for C trachomatis with LCR of urine samples. The first group comprised 3982 asymptomatic men tested in a community-based screening effort. 11 The second comprised 1625 asymptomatic men seen in a sexually transmitted disease (STD) clinic. 12 Data from these groups were used to examine potential selective screening criteria for chlamydial infection and to estimate the associated predictive value of urine LE testing. As previously reported, only age <25 years and a positive urine LE test were associated with asymptomatic chlamydial infection in these men. 11,12 Outcomes assessed included untreated chlamydial infection of males and subsequent complications, transmission to female partners, development of PID, infertility, ectopic pregnancy, chronic pelvic pain, and neonatal transmission. The decision model was developed with use of DATA 3.5.6 software (TreeAge Software, Williamstown, MA). Key structural components of the tree are shown in Figure 1 (full model available upon request).
The analysis took the perspective of the healthcare payor and estimated direct medical costs. Current clinical guidelines were used to determine medical management (inpatient and outpatient visits, procedures, and medication). 13,14 The time horizon for events before the development of PID complications was 1 year. Infertility was assumed to be evaluated 10 years after contraction of C trachomatis infection, and ectopic pregnancy and chronic pelvic pain 5 years after. 2 All future costs and outcomes were discounted at a rate of 3% per year. 15
Probability estimates associated with chlamydial infection and sequelae were obtained from a review of current literature (Table 1). 2,3,5,6,8,9,11,12,16–26,28–43,46,53–64 The most plausible estimate was assigned a range of values to account for uncertainty. The C trachomatis prevalence of 5% used for young men in the base-case scenario was derived from recent studies using urine-based testing of asymptomatic men. 16–20 LE and LCR test performance measures were obtained from recent research on asymptomatic men in STD and non-STD clinic settings. 6,9,11,12,16,18,21–23 For transmission of C trachomatis, we accounted for data on the prevalence of coinfection in couples, 24–26 that transmission does not occur with every episode of intercourse, and that 35% of sexually active young men report two or more sex partners in the previous 3 months. 27 We conservatively estimated that each infected male transmitted C trachomatis to one female partner per year.
Although few firm data on clinical outcomes of partner management are available, we estimated that 75% of men returned to their provider for treatment after the detection of C trachomatis infection through screening 28 and that 50% of infected female partners were successfully contacted and treated. 29,30 Of those female partners who did not return for treatment, we assumed that 5% would have the infection detected through routine screening. 5 Of those not screened or whose screen was falsely negative, we estimated that 50% of men and 20% of women with C trachomatis were symptomatic. 2 We estimated that 20% of men with discharge or dysuria and 10% of women with nonspecific genitourinary complaints would seek care. These estimates were based on evidence that many young adults with health problems forego care 31 and that the nonspecific symptoms of chlamydial infection in women may not prompt evaluation.
Studies that demonstrate the role of C trachomatis in laparoscopically confirmed salpingitis or biopsy-confirmed endometritis were used to estimate that 25% of women with untreated cervical chlamydial infection develop PID. 32–34 Approximately 60% of all women with upper-genital-tract inflammation are thought to have subclinical PID. 33,35–37 Longitudinal and population-based studies estimate that tubal infertility occurs in 15% of women with laparoscopically confirmed salpingitis. 38,39 Of women with an ectopic pregnancy, 75% were estimated to seek outpatient laparoscopic treatment, 40 20% to use methotrexate, 41 and 5% to require inpatient surgery. 40 We estimated that 18% of women who have one episode of PID develop chronic pelvic pain. 42,43
We used Medicaid maximum allowable fee schedules for Washington state (WA) to derive cost estimates (Table 2). Fee schedules included the resource-based relative value reimbursement schedule (RBRVS) for physician and surgeon reimbursement, the prospective payment system (PPS) for hospital fees, the prospective payment system for ambulatory surgical center (ASC) reimbursement, the clinical diagnostic laboratory fee schedule, and the maximum allowable cost (MAC) prescription fee schedule. The 1999 Drug Topics Red Book44 was used for prescriptions not covered under WA Medicaid. To account for uncertainty in cost estimates, a plausible range was estimated by assessing costs used by other economic evaluations of C trachomatis screening. 8,9,45–47 To account for variation in published costs relative to WA Medicaid estimates, we used a range of −10% to +60% of the base-case estimates.
For each strategy, cost, effectiveness, and incremental cost-effectiveness were assessed. Total cost accounted for screening, treatment, and sequelae. Number of cases of PID prevented was the primary measure of effectiveness, but prevented cases of urethritis, epididymitis, infertility, ectopic pregnancy, chronic pelvic pain, neonatal conjunctivitis, and pneumonia were also evaluated. Incremental cost-effectiveness was defined as the incremental cost of preventing an additional case of PID with one strategy, compared to the next-most-effective strategy.
Sensitivity analyses were performed to evaluate uncertainty in the model. After one-way sensitivity analyses were conducted on all parameters, detailed one- and two-way sensitivity analyses were conducted on the prevalence of infection and the cost of the LCR assay—variables that showed the greatest impact on overall strategy cost and effectiveness.
As shown in Table 3, the LCR strategy was the most effective approach, preventing on average 66% more PID cases than no screening. In comparison, the LE-LCR strategy prevented 46% more PID cases than no screening. Costs associated with the three strategies are presented in Table 4. The cost to screen one man was $55.67 with the LCR strategy, compared to $31.91 with LE-LCR, due to the high cost of the LCR assay. Treatment costs of $1.14 per male screened were also highest for the LCR strategy, because use of LCR led to detection and treatment of more infected men. The $0.30 treatment cost associated with no screening represents young men who developed symptoms and sought care. Costs of sequelae due to untreated chlamydial infection were markedly different across strategies; those for no screening were three times that of the LCR strategy. The LE-LCR strategy showed a $3.34 cost savings in sequelae costs per male screened over no screening, and the LCR strategy showed an additional $1.41 savings over LE-LCR per male screened. In incremental analysis, the LE-LCR strategy cost $29.14 more per male screened than no screening and prevented 242 additional cases of PID. The LCR strategy cost $22.62 more than the LE-LCR strategy and prevented 104 additional cases of PID.
One-Way and Two-Way Sensitivity Analyses
One- and two-way sensitivity analyses examined how the prevalence of male infection and the cost of the LCR assay affected overall strategy cost. As prevalence increased, total program costs for each strategy differed. At a prevalence of 3%, no screening cost $4.47, LE-LCR cost $34.38, and LCR cost $57.80 per screened male. At a prevalence of 5%, no screening cost $7.44, LE-LCR cost $36.58, and LCR cost $59.20 per screened male. At a prevalence of 10%, no screening cost $14.89, LE-LCR cost $42.08, and LCR cost $62.72 per screened male. The LCR strategy became less expensive than LE-LCR above a prevalence of 60% and became less expensive than no screening above a prevalence of 70%.
Figure 2 shows the effect of varying the cost of the LCR assay on total strategy cost. At the base-case scenario prevalence (5%), the LCR strategy became less expensive than the LE-LCR strategy when the cost of the LCR assay fell below $4.20. At prevalences of 3% and 10%, the cost of the LCR must fall below $3.60 and $5.90, respectively, for the LCR strategy to be less expensive than LE-LCR.
Figure 3 shows the results of a two-way sensitivity analysis that examined the impact of varying both the prevalence of chlamydial infection among males and the cost of the LCR assay on total strategy cost. The dotted line indicates the point at which the LCR and LE-LCR strategies cost an equal amount. The area to the right of the line represents the prevalence and LCR assay cost at which the LCR strategy is less expensive than the LE-LCR strategy, and the area to the left of the line represents when the LE-LCR strategy is less expensive than LCR. Overall, as the prevalence of infection among males increases or as the cost of the LCR assay decreases, the LCR strategy becomes less expensive.
One-way sensitivity analyses examined how the prevalence of male infection and the cost of the LCR assay affected overall strategy effectiveness. As shown in Figure 4, at any prevalence of male infection, the LCR strategy was more effective in preventing cases of PID than was the LE-LCR strategy, which in turn was more effective than the no screening strategy. Varying the cost of the LCR assay had no effect on program effectiveness.
Incremental cost-effectiveness analysis.
At 5% prevalence, LE-LCR cost $12,041 to prevent an additional case of PID over no screening, and LCR cost $21,750 to prevent an additional case over LE-LCR. However, if the if the cost of the LCR assay fell to $18 or less, or if the prevalence of infection increased to 49%, the LCR strategy cost less to prevent an additional case of PID than the LE-LCR strategy.
We assessed the incremental cost-effectiveness of a variety of scenarios that account for some important analytic limitations. Inclusion of indirect costs or costs to private payors increased the cost of all strategies but did not significantly change the incremental cost-effectiveness of the strategies. When additional C trachomatis–associated sequelae (endometritis, perihepatitis, and proctitis) were included, the cost of the no screening strategy increased by 55% to $11.55 per male screened, LE-LCR increased by 6% to $38.78, and LCR increased by 2% to $60.59. In incremental analysis, LE-LCR became cost-saving over no screening at or above a prevalence of 41%, and the LCR strategy became cost-saving over LE-LCR at or above a prevalence of 44%. When costs of a clinic visit associated with screening in traditional healthcare settings were removed, LE-LCR became cost-saving over no screening at a prevalence of 23%, but the LCR strategy did not become cost-saving over the LE-LCR strategy until a prevalence of 62%. When costs from a recent economic evaluation of screening asymptomatic women were used, 48 both the LE-LCR and the LCR strategy became cost-saving at a prevalence of infection among men of 4% or higher.
We found that at a prevalence of chlamydial infection of 5% among asymptomatic men, prescreening urine for LE, followed by confirmatory testing with urine-based LCR, was the most cost-effective strategy. Relative to no screening, LE-LCR resulted in 242 fewer cases of PID per 100,000 males screened and cost $29.14 per male tested. While testing all men with LCR prevented more chlamydia-associated sequelae than LE-LCR, the additional cost was substantial ($22.62 per man screened). In sensitivity analysis, the cost of the LCR assay and the prevalence of C trachomatis infection in males critically impacted outcomes. In order for a strategy using only urine LCR screening to be more efficient than LE-LCR at the chlamydia prevalence in our base-case analysis (5%), the cost of the LCR assay needed to decline to $18 or less.
In general, our results concur with those of other investigators. Genc and colleagues 9 estimated that screening asymptomatic men with urine LE testing confirmed by a specific enzyme immunoassay (EIA) test was more cost-effective than screening with only EIA. Two other large studies also concluded that applying an initial nonspecific screening test (such as an LE test) followed by specific testing was the most cost-effective approach to screening asymptomatic men. 6,7 Our analysis extends this work in several ways. We evaluated the use of a nucleic acid amplification assay and, of critical importance, included costs of managing female partners of infected men. We accounted for outcomes of symptomatic and subclinical PID and incorporated new treatment protocols, including the use of methotrexate for ectopic pregnancy. All direct costs associated with chlamydial infection, not just the cost of diagnostic tests, were included (such as office visits, hospital fees, surgical procedures, laboratory work, medication). Finally, we performed extensive sensitivity analyses on cost variables to ensure applicability of the analysis to a wide array of settings and payor types.
Howell and colleagues 48 evaluated the use of urine LCR to screen a hypothetical asymptomatic cohort of 18,000 women and reported a cost-saving of $3,689 for use of an LCR strategy over no screening. When compared directly to our results, this suggests that the benefits of using LCR versus no screening are greater when women are screened than when men are screened. However, the two studies used significantly different probability and cost estimates. For example, Howell used a lower LCR assay cost ($5.32) than we did ($33.42), and higher costs for evaluating PID and associated sequelae. Our sensitivity analyses showed that such a cost structure favored the efficiency of the LCR strategy over no screening. When we recalculated our costs using estimates from the Howell study, we found that both the LE-LCR and LCR strategies became cost-saving over no screening at or above a C trachomatis prevalence of 4%. A comprehensive approach to assess the cost-effectiveness of screening young men versus women would be to use our probability and cost estimates to calculate total costs and outcomes for screening a comparable cohort of asymptomatic women.
Our study has several limitations. First, the validity of our model depends on the accuracy of the incorporated probabilities. Extensive sensitivity analyses mitigated some of this uncertainty. Second, our analysis was done from the perspective of the healthcare payor. An analysis from the societal perspective would include nonmedical direct costs, indirect costs, and intangible costs. Inclusion of indirect costs increased the overall cost of each strategy but did not significantly change the incremental cost of preventing an additional case of PID for either strategy. Third, we chose Medicaid reimbursements to Washington state providers and facilities. These cost values are likely to be lower than the cost to private health plans. Raising these estimates to more substantially represent private fee schedules did not change our general conclusions. Fourth, we did not include all C trachomatis–associated outcomes, such as urethritis, bartholinitis, endometritis, and perihepatitis in women and proctitis, prostatitis, and Reiter syndrome in men. Studies have also demonstrated an association between chlamydial infection and low birth weight, postpartum endometritis, premature rupture of membranes, and chorioamnionitis;3 enhanced risk of HIV transmission;49 and cervical cancer. 50 Inclusion of such events would favor the LCR strategy, since more of these expensive outcomes would be avoided.
Fifth, our base-case scenario modeled the cost of C trachomatis screening as a separate office visit. If screening were integrated with other health visits such as sports physicals, the cost of testing could be significantly less. Finally, partner management strategies have the potential to greatly impact reinfection rates in women. For our analysis, we used existing data available for traditional approaches to partner management. However, innovative methods for partner management are under study and may prove more effective and less costly.
Ten US regions that target women with large-scale C trachomatis screening programs have shown a 60% decline in reported cases of C trachomatis since 1988. 51 However, from 1997 to 1998, C trachomatis prevalence increased in nine of these regions. This increase is likely to be due solely to the use of more sensitive diagnostic methods or to expansion of screening programs to populations with higher prevalence. However, the implementation and evaluation of screening strategies aimed at males may be important to further control chlamydial infections in women, particularly when coupled with strategies to enhance partner management. 52 Our analyses indicate that for healthcare organizations that serve populations with a prevalence of male infection of approximately 5%, the LE-LCR strategy is a more efficient use of healthcare dollars than the LCR strategy. However, if the cost of the LCR assay decreases—or in populations with high chlamydia prevalence—the LCR option may be preferred.
1. Centers for Disease Control and Prevention. Sexually transmitted disease surveillance 2000. Atlanta: US Department of Health and Human Services, National Center for HIV, STD, and TB Prevention, Division of STD Prevention, 2001.
2. Stamm WE. Chlamydia trachomatis infections of the adult. In: Holmes K, ed. Sexually Transmitted Diseases. 3rd ed. New York: McGraw Hill, Health Professionals Division, 1999.
3. Hammerschlag MR. Chlamydial infections in infants and children. In: Holmes K, ed. Sexually Transmitted Diseases. 3rd ed. New York: McGraw Hill, Health Professionals Division, 1999.
4. Siegel JE. The economic burden of sexually transmitted diseases in the United States. In: Holmes K, ed. Sexually Transmitted Diseases. 3rd ed. New York: McGraw Hill, Health Professionals Division, 1999.
5. Centers for Disease Control and Prevention. Chlamydia trachomatis genital infections–United States, 1995. MMWR Morb Mortal Wkly Rep 1997; 46: 193–198.
6. Shafer MA, Schachter J, Moncada J, et al. Evaluation of urine-based screening strategies to detect Chlamydia trachomatis among sexually active asymptomatic young males. JAMA 1993; 270: 2065–2070.
7. Sellors JW, Mahony JB, Pickard L, et al. Screening urine with a leukocyte esterase strip and subsequent chlamydial testing of asymptomatic men attending primary care practitioners. Sex Transm Dis 1993; 20: 152–157.
8. Randolph AG, Washington AE. Screening for Chlamydia trachomatis in adolescent males: a cost-based decision analysis. Am J Public Health 1990; 80: 545–550.
9. Genc M, Ruusuvaara L, Mardh PA. An economic evaluation of screening for Chlamydia trachomatis in adolescent males. JAMA 1993; 270: 2057–2064.
10. Genc M, Domeika M, Mardh PA. Cost-effectiveness of screening for chlamydia using DNA amplification [letter]. JAMA 1994; 271: 1741.
11. Marrazzo JM, White CL, Krekeler B, et al. Community-based urine screening for Chlamydia trachomatis with a ligase chain reaction assay. Ann Intern Med 1997; 127: 796–803.
12. Marrazzo JM, Whittington WL, Celum CL, et al. Urine-based screening for Chlamydia trachomatis in men attending sexually transmitted disease clinics. Sex Transm Dis 2001; 28: 219–225.
13. Centers for Disease Control and Prevention. 1998 Guidelines for treatment of sexually transmitted diseases. MMWR Morb Mortal Wkly Rep 1998; 47: 1–111.
14. Institute for Clinical Systems Improvement. Diagnosis and Management of Infertility. Bloomington, MN: Institute for Clinical Systems Improvement, 1999.
15. Gold M, Siegel J, Russell L, Weinstein M, eds. Cost-Effectiveness in Health and Medicine. New York: Oxford Press, 1996.
16. Stary A, Tomazic-Allen S, Choueiri B, Burczak J, Steyrer K, Lee H. Comparison of DNA amplification methods for the detection of Chlamydia trachomatis in first-void urine from asymptomatic military recruits. Sex Transm Dis 1996; 23: 97–102.
17. St. Louis ME, Ku L, Aral SO, Williams S, Black C, Sonenstein F. Prevalence of Chlamydia trachomatis infection among young men in the United States: a representative national survey. In: Abstracts of the 13th International Society for STD Research Conference, July 1999, Denver, CO.
18. Werner MJ, Biro FM. Urinary leukocyte esterase screening for asymptomatic sexually transmitted disease in adolescent males. J Adolesc Health 1991; 12: 326–328.
19. Shafer MA, Schachter J, Moscicki AB, et al. Urinary leukocyte esterase screening test for asymptomatic chlamydial and gonococcal infections in males. JAMA 1989; 262: 2562–2566.
20. Schillinger JA, Gift T, Marrazzo JM, et al. Screening males for chlamydial infection: do we have the data to guide programs? Presented at the 2002 National STD Prevention Conference, Centers for Disease Control and Prevention, March 2002, San Diego, CA.
21. Anestad G, Berdal BP, Scheel O, et al. Screening urine samples by leukocyte esterase test and ligase chain reaction for chlamydial infections among asymptomatic men. J Clin Microbiol 1995; 33: 2483–2484.
22. Chernesky MA, Chong S, Jang D, Luinstra K, Sellors J, Mahony JB. Ability of commercial ligase chain reaction and PCR assays to diagnose Chlamydia trachomatis infections in men by testing first-void urine. J Clin Microbiol 1997; 35: 982–984.
23. Stary A, Schuh E, Kerschbaumer M, Gotz B, Lee H. Performance of transcription-mediated amplification and ligase chain reaction assays for detection of chlamydial infection in urogenital samples obtained by invasive and noninvasive methods. J Clin Microbiol 1998; 36: 2666–2670.
24. Quinn TC, Gaydos C, Shepherd M, et al. Epidemiologic and microbiologic correlates of Chlamydia trachomatis infection in sexual partnerships. JAMA 1996; 276: 1737–1742.
25. Lin JS, Donegan SP, Heeren TC, et al. Transmission of Chlamydia trachomatis and Neisseria gonorrhoeae among men with urethritis and their female sex partners. J Infect Dis 1998; 178: 1707–1712.
26. Viscidi RP, Bobo L, Hook EW3d, Quinn TC. Transmission of Chlamydia trachomatis among sex partners assessed by polymerase chain reaction. J Infect Dis 1993; 168: 488–492.
27. Santelli JS, Brener ND, Lowry R, Bhatt A, Zabin LS. Multiple sexual partners among US adolescents and young adults. Fam Plan Perspect 1998; 30: 271–275.
28. Schwebke JR, Sadler R, Sutton JM, Hook EW3rd. Positive screening tests for gonorrhea and chlamydial infection fail to lead consistently to treatment of patients attending a sexually transmitted disease clinic. Sex Transm Dis 1997; 24: 181–184.
29. Katz BP, Caine VA, Jones RB. Evaluation of field follow-up in a sexually transmitted disease clinic for patients at risk for infection with Neisseria gonorrhoeae and Chlamydia trachomatis. Sex Transm Dis 1992; 19: 99–104.
30. Zimmerman-Rogers H, Potterat JJ, Muth SQ, et al. Establishing efficient partner notification periods for patients with chlamydia. Sex Transm Dis 1999; 26: 49–54.
31. Ford CA, Bearman PS, Moody J. Foregone health care among adolescents. JAMA 1999; 282: 2227–2234.
32. Stamm WE, Guinan ME, Johnson C, Starcher T, Holmes KK, McCormack WM. Effect of treatment regimens for Neisseria gonorrhoeae on simultaneous infection with Chlamydia trachomatis. N Engl J Med 1984; 310: 545–549.
33. Paavonen J, Kiviat N, Brunham RC, et al. Prevalence and manifestations of endometritis among women with cervicitis. Am J Obstet Gynecol 1985; 152: 280–286.
34. Scholes D, Stergachis A, Heidrich FE, Andrilla H, Holmes KK, Stamm WE. Prevention of pelvic inflammatory disease by screening for cervical chlamydial infection. N Engl J Med 1996; 334: 1362–1366.
35. Jones RB, Mammel JB, Shepard MK, Fisher RR. Recovery of Chlamydia trachomatis from the endometrium of women at risk for chlamydial infection. Am J Obstet Gynecol 1986; 155: 35–39.
36. Brunham RC, Maclean IW, Binns B, Peeling RW. Chlamydia trachomatis: its role in tubal infertility. J Infect Dis 1985; 152: 1275–1282.
37. Patton DL, Askienazy-Elbhar M, Henry-Suchet J, et al. Detection of Chlamydia trachomatis in fallopian tube tissue in women with postinfectious tubal infertility. Am J Obstet Gynecol 1994; 171: 95–101.
38. Westrom 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 1992; 19: 185–192.
39. Abma JC, Chandra A, Mosher WD, Peterson LS, Piccinino LJ. Fertility, family planning, and women's health: new data from the 1995 National Survey of Family Growth. Vital Health Stat 1997: 1–114.
40. Young PL, Saftlas AF, Atrash HK, Lawson HW, Petrey FF. National trends in the management of tubal pregnancy, 1970–1987. Obstet Gynecol 1991; 78: 749–752.
41. Creinin MD, Washington AE. Cost of ectopic pregnancy management: surgery versus methotrexate. Fertil Steril 1993; 60: 963–969.
42. Safrin S, Schachter J, Dahrouge D, Sweet RL. Long-term sequelae of acute pelvic inflammatory disease: a retrospective cohort study. Am J Obstet Gynecol 1992; 166: 1300–1305.
43. Westrom L. Incidence, prevalence, and trends of acute pelvic inflammatory disease and its consequences in industrialized countries. Am J Obstet Gynecol 1980; 138: 880–892.
44. Medical Economics Company. Drug Topics Red Book. Montvale, NJ: Medical Economics Data, 1999.
45. Marrazzo JM, Celum CL, Hillis SD, Fine D, DeLisle S, Handsfield HH. Performance and cost-effectiveness of selective screening criteria for Chlamydia trachomatis infection in women: implications for a national chlamydia control strategy. Sex Transm Dis 1997; 24: 131–141.
46. Magid D, Douglas JM Jr, Schwartz JS. Doxycycline compared with azithromycin for treating women with genital Chlamydia trachomatis infections: an incremental cost-effectiveness analysis. Ann Intern Med 1996; 124: 389–399.
47. Haddix AC, Hillis SD, Kassler WJ. The cost effectiveness of azithromycin for Chlamydia trachomatis infections in women. Sex Transm Dis 1995; 22: 274–280.
48. Howell MR, Quinn TC, Brathwaite W, Gaydos CA. Screening women for Chlamydia trachomatis in family planning clinics: the cost-effectiveness of DNA amplification assays. Sex Transm Dis 1998; 25: 108–117.
49. Wasserheit JN. Epidemiological synergy: interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases. Sex Transm Dis 1992; 19: 61–77.
50. Zenilman JM. Chlamydia and cervical cancer: a real association? JAMA 2001; 285: 81–83.
51. Centers for Disease Control and Prevention. Sexually transmitted disease surveillance, 1998. Atlanta: US Department of Health and Human Services, National Center for HIV, STD, and TB Prevention, Division of STD Prevention, 1997.
52. Kretzschmar M, Welte R, van den Hoek A, Postma MJ. Comparative model-based analysis of screening programs for Chlamydia trachomatis infections. Am J Epidemiol 2001; 153: 90–101.
53. Martin DH, Mroczkowski TF, Dalu ZA, et al. A controlled trial of a single dose of azithromycin for the treatment of chlamydial urethritis and cervicitis. The Azithromycin for Chlamydial Infections Study Group. N Engl J Med 1992; 327: 921–925.
54. Hammerschlag MR, Golden NH, Oh MK, et al. Single dose of azithromycin for the treatment of genital chlamydial infections in adolescents. J Pediatr 1993; 122: 961–965.
55. Stamm WE, Hicks CB, Martin DH, et al. Azithromycin for empirical treatment of the nongonococcal urethritis syndrome in men: a randomized double-blind study. JAMA 1995; 274: 545–549.
56. Hopkins S. Clinical toleration and safety of azithromycin. Am J Med 1991; 91: 40S–45S.
57. Parks KS, Dixon PB, Richey CM, Hook EW3rd. Spontaneous clearance of Chlamydia trachomatis infection in untreated patients. Sex Transm Dis 1997; 24: 229–235.
58. Rolfs RT, Galaid EI, Zaidi AA. Pelvic inflammatory disease: trends in hospitalizations and office visits, 1979 through 1988. Am J Obstet Gynecol 1992; 166: 983–990.
59. Hirsch MB, Mosher WD. Characteristics of infertile women in the United States and their use of infertility services. Fertil Steril 1987; 47: 618–625.
60. Philips Z, Barraza-Llorens M, Posnett J. Evaluation of the relative cost-effectiveness of treatments for infertility in the UK. Hum Reprod 2000; 15: 95–106.
61. Westrom L, Bengtsson LP, Mardh PA. Incidence, trends, and risks of ectopic pregnancy in a population of women. BMJ (Clin Res Ed) 1981; 282: 15–18.
62. Mathias SD, Kuppermann M, Liberman RF, Lipschutz RC, Steege JF. Chronic pelvic pain: prevalence, health-related quality of life, and economic correlates. Obstet Gynecol 1996; 87: 321–327.
63. Ventura SJ, Mosher WD, Curtin SC, Abma JC, Henshaw S. Trends in pregnancies and pregnancy rates by outcome: estimates for the United States, 1976–96. Vital Health Stat 2000: 1–471.
64. Schachter J, Grossman M, Sweet RL, Holt J, Jordan C, Bishop E. Prospective study of perinatal transmission of Chlamydia trachomatis. JAMA 1986; 255: 3374–3377.
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