Sexually Transmitted Diseases:
Should Asymptomatic Men Be Included in Chlamydia Screening Programs? Cost-Effectiveness of Chlamydia Screening Among Male and Female Entrants to a National Job Training Program
Blake, Diane R. MD*; Quinn, Thomas C. MD†‡; Gaydos, Charlotte A. DRPH†
From the *Department of Pediatrics, University of Massachusetts Medical School, Worcester, Massachusetts; †Department of Medicine, Johns Hopkins School of Medicine, Baltimore, Maryland; and ‡National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
The authors thank Linda Lambrecht for her technical assistance, and the many technicians from The Johns Hopkins University Chlamydia Research Laboratory who assisted with this project. The authors also thank the job training program staff and students who participated in the study.
Supported by the National Institute of Allergy and Infectious Diseases (Grant No. 5 K23 AI01750), Child Health Research Grant from the Charles H. Hood Foundation, and by the University of Massachusetts Center for AIDS Research Clinical Investigation Core (AI42845).
The contents are solely the responsibility of the authors and do not necessarily represent the official views of the National Institute of Allergy and Infectious Diseases.
Correspondence: Diane R. Blake, MD, Department of Pediatrics, University of Massachusetts Medical School, 55 Lake Avenue North, Worcester, MA 01655. E-mail: Diane.Blake@umassmed.edu.
Received for publication April 28, 2006, and accepted July 2, 2007.
Objective: To compare the cost-effectiveness of various chlamydia screening strategies within a population of male and female youth entering a national job training program.
Study Design: Cost-effectiveness analysis of various chlamydia screening strategies among a cohort of 4000 female and male New England job training students. Strategies for women include (a) no screening, (b) universal endocervical DNA probe screening, (c) universal urine based NAAT screening, and (d) universal endocervical NAAT screening. Strategies for men include (a) no screening, (b) selective urine NAAT screening of leukocyte esterase (LE)-positive urines, and (c) universal urine-based NAAT screening.
Results: Universal endocervical NAAT screening of women and universal urine NAAT screening of men were the most effective and cost-effective strategies individually and in combination. Endocervical NAAT screening of women prevented 23 more cases of PID and saved $27,000 more than endocervical DNA probe screening. Likewise, universal urine NAAT screening of men prevented 21 more cases of PID in their female partners and saved $16,000 more than selective urine NAAT screening of LE positive men.
Conclusions: Use of a sensitive NAAT to screen both men and women for chlamydia upon entry to a National Job Training Program is cost-effective, cost-saving, and provides a public health opportunity to substantially reduce chlamydia infections among youth at risk for sexually transmitted diseases.
IT IS NOW WELL established that Chlamydia trachomatis remains asymptomatic much, if not most, of the time.1–4 Asymptomatic, infected youth are generally unaware of the need for routine chlamydia screening,5–7 which is recommended for all sexually active women age 25 and younger.8 Official recommendations for universal screening of sexually active men have not yet been made. Yet when left untreated, chlamydia can lead to serious and costly sequelae, particularly for infected women.9,10 An estimated 30% to 40% of untreated chlamydia infections progress to pelvic inflammatory disease (PID), 11–14 and common sequelae of PID include ectopic pregnancy, infertility, and chronic pelvic pain,15–18 with estimated annual costs exceeding $3.1 billion.19 Although considerably less common than PID, untreated chlamydia in men may progress to epididymitis.20,21
Many teens have reported that they would prefer to receive chlamydia screening at their own doctor’s office.22,23 Nevertheless, a large proportion of teens does not have access to primary care.22–25 Routine chlamydia screening of male and female youth upon entry to a national, federally funded, job training program provides an opportunity to reduce the prevalence of chlamydia by detecting and treating asymptomatic infections in individuals who otherwise might not seek screening. For a number of years, the national job-training program had been screening all female entrants for chlamydia using an endocervical DNA probe and all male entrants with a urine leukocyte esterase (LE) dipstick. Only those men with a positive LE were tested with a urethral chlamydia DNA probe. Recently, the job-training program instituted universal chlamydia screening of male entrants using a urine-based NAAT and began screening female entrants using an endocervical NAAT. The introduction of urine-based nucleic acid amplification tests (NAATs) improves the feasibility of performing chlamydia screening without delay because entering students can provide a urine specimen during their admission nursing visit rather than waiting for an appointment with a health-care provider.
Previous economic analyses have demonstrated that routine chlamydia screening of sexually active female youth is cost-effective.11,26–32 However, cost-effectiveness analyses performed on sexually active male youth populations have yielded conflicting results.27,33–35 The purpose of this study was to perform a chlamydia screening cost-effectiveness analysis for all youth (female and male) entering a national job training program, which will allow for a direct economic comparison of female and male chlamydia screening strategies, including the recently adopted strategy at the national job training program.
Decision Analysis Models
Chlamydia screening decision trees were constructed for hypothetical cohorts of 2000 female and 2000 male students entering New England job training centers each year. Probabilities and costs were estimated for each node and were derived from primary data collection, published data, and unpublished Massachusetts and job training program health data. All costs were adjusted to 2005 US dollars, and future costs were discounted at a rate of 3%.36 Cost to charge ratios were used to calculate costs where only charge data were available. This analysis was conducted from the public health care perspective and included only direct medical costs.
The models incorporated programmatic costs of screening and treatment of infected students and their sexual partners as well as medical cost savings from prevented cases of PID and its sequelae in women and epididymitis in men. We used a 10-year time horizon to incorporate all expected future sequelae of PID. Our primary outcome of interest was the number of cases of PID prevented. We report on the total costs associated with PID prevention and the incremental costs of each screening strategy compared with no screening.
To estimate the prevalence of chlamydia, female and male youth, ages 16–24 years, entering a job training program site located in New England between February 2001 and February 2004 were invited to participate in a chlamydia prevalence study utilizing urine-based nucleic acid amplification tests. Primary data collection in the form of a prevalence study was needed because the more sensitive methods for detecting chlamydia were not routinely used at that time. All participants provided written informed consent. The requirement for parental permission was waived due to the minimal risk nature of the study and the infeasibility of obtaining parental permission. Study protocol and consent procedures were approved by the University of Massachusetts Committee for the Protection of Human Subjects in Research.
At the time of their nursing admission evaluation, participants completed a brief data form and then collected the first 10–15 mL of urine into a 50 mL urine collection cup (if female) or a 15-mL plastic centrifuge tube (if male). Urine samples were transported to The Johns Hopkins University Chlamydia Research Laboratory in Baltimore, MD where they were tested for chlamydia using either the LCx (Abbott Laboratories, Abbott Park, IL) or BDProbeTec (Becton Dickinson, Sparks, MD) NAAT. Assays were performed according to manufacturers’ directions.
The true chlamydia prevalence was calculated by dividing the observed chlamydia prevalence by the estimated sensitivity of the urine NAAT (women: 84.0%, see appendix; men: 91.333) and then multiplying by the specificity of the urine NAAT (women: 98.7%, see appendix; men: 98.0%33).
Chlamydia test results were transmitted to the principle investigator who promptly notified the job training program health services with all positive results. Infected students who were still enrolled in the program were immediately treated with 1 g of azithromycin according to Centers for Disease Control and Prevention guidelines.8 Those who had left the program were contacted by phone; if students could not be located, the disease intervention specialist at the State Department of Public Health was contacted. At the time of test result notification, students were asked how many sexual partners they had had during the past 2 months (0, 1, 2, >2) and were encouraged to refer their partners for treatment. Although “>2 partners” could represent a large range of partners, “>2” was coded as “3 partners” for analysis purposes. Consequently, it is likely that we have underestimated the number of recent past and future partners at risk for infection.
We made the assumption that a student would have at least as many partners over the ensuing 12 months (at-risk future partners) as he or she reported having in the past 2 months. The 12 month time horizon for infectiousness is consistent with previous estimates that have indicated that an untreated person infected with chlamydia remains infectious for an average of 12 months.37,38 We made the assumption that the proportion of at risk future partners who enter the partnership already infected with chlamydia is similar to the prevalence of chlamydia in the men and women participating in the prevalence study.
Not all future female partners who become infected with chlamydia will be at risk of developing PID because they may receive routine screening and treatment for chlamydia before PID can develop. Forty-six percent of a subset of women from this prevalence study reported that they had received STD screening in the past year (Blake et al., unpublished data). Because it is unclear how long it takes for PID to develop, we estimated that half of this proportion (23%) of infected future female partners would be diagnosed and treated for their chlamydia infection through routine screening before PID could develop. This reduces the rate of PID development among infected future women to 23% [0.30 PID rate × (1 − 0.23 treated for chlamydia via routine screening) = 0.23]. To be conservative, we used a 20% rate of PID development among infected future partners in our analysis.
As part of the job training program protocol at the time that this study was conducted, entering female students were required to have a pelvic examination with a Pap smear and endocervical DNA probe (PACE2, GenProbe, San Diego, CA) for chlamydia and Gonorrhea sent within 14 days of admission. Since completion of this study, the job training program has replaced the endocervical DNA probe with an endocervical NAAT (BDProbeTec, Becton Dickinson, Sparks, MD). Because some students do not receive a pelvic examination due to menstruation on the day of their physical examination or they leave the program before their scheduled physical, we assessed the proportion of women who were screened with an endocervical DNA probe during our prevalence study. This proportion represented the “capture rate” for screening tests that require a speculum examination.
Probability estimates were derived from primary data collection, published data, and unpublished state and job training program health data. Probability estimates for chlamydia prevalence, screening test sensitivity and specificity, and the occurrence of PID and its sequelae as well as other relevant estimates are found in Table 1. Modified meta-analyses were performed to estimate the overall sensitivity and specificity of the DNA probe and the 2 nucleic acid amplification tests used in this study and are found in the appendix.
Screening costs include the cost of the NAAT, cost of the DNA probe, and cost of materials and labor for leukocyte esterase (LE) testing on male urine (Table 2). Time to perform the LE test was estimated at 2½ minutes33 and multiplied by the licensed practical nurse (LPN) hourly rate.
Treatment costs include treatment of newly diagnosed cervicitis and urethritis at job training program entry, partner treatment, and treatment of PID, its sequelae, and epididymitis (Table 2). Students who test positive for chlamydia are sent a pass to the Wellness Center. A treatment and education visit was estimated to require 15-minutes with the Wellness Center LPN, which was multiplied by the LPN hourly rate. The public health government rate for 1 g of azithromycin was used for students treated at the training program, and the wholesale price was used for those treated outside of the program. A 15-minute phone call initiated by the Wellness Center LPN to notify an infected student who had left the job-training program before results were received was multiplied by the LPN hourly rate. The cost of a Disease Intervention Specialist (DIS) contacting and referring infected students who could not be contacted by the Wellness Center LPN for treatment was estimated by multiplying an average of 2 hours of DIS time by the midrange salary of a DIS. Partner treatment costs included the cost of a 25-minute office visit, which was estimated using the UMass Memorial Medicaid reimbursement rate for a Level 4 office visit, and the wholesale price for 1 g of azithromycin (Table 2).
Inpatient costs for treatment of PID and epididymitis as well as infertility, ectopic pregnancy, and chronic pelvic pain treatment costs were estimated from the Northeast regional data of the Health Care Utilization Project (HCUP) 2003 and the literature (Table 2).9,15,21,29,31,66,73,74 Outpatient costs for treatment of PID and epididymitis were estimated using the UMass Memorial Medicaid reimbursement rate for a Level 5 (40 minute) initial office visit and a Level 4 (25 minute) follow up visit. The cost of a ceftriaxone injection and a course of doxycycline were estimated from the literature.71,72
The cost-effectiveness analyses (CEAs) were conducted using TreeAge Pro 2007 (TreeAge Software, Williamstown, MA) decision analysis software. Individual CEAs were performed for a cohort of 2000 female students and for a cohort of 2000 male students entering New England job training centers per year. For female students, the screening strategies included (a) no screening, (b) universal endocervical DNA probe screening, (c) universal urine NAAT screening and (d) universal endocervical NAAT screening. For male students, the screening strategies included (a) no screening, (b) selective urine NAAT screening of LE positives, and (c) universal urine NAAT screening. Additionally, male and female screening strategies were assorted in a variety of combinations to assess the incremental cost-effectiveness of each screening combination.
Chlamydia prevalence threshold analyses were conducted for each gender to determine the prevalence at which each screening strategy becomes most cost-effective. Where parameter estimates were based on assumptions rather than actual values, univariate and bivariate sensitivity analyses were performed to assess the effect of a range of possible parameter values.
Characteristics of Study Participants
Four hundred fifty female and 450 male job-training students were recruited for the prevalence study. Participant characteristics are detailed in Table 3. None of the nonsexually active students tested positive for chlamydia; therefore, only the sexually active students were included in the analyses reported. Female chlamydia prevalence was 17.7%, and male chlamydia prevalence was 7.8%.
The average number of female partners that infected men reported having in the past 2 months was 1.6. Likewise, the average number of male partners that infected women reported having in the past 2 months was 1.4.
Screening was based on a hypothetical cohort of 2000 female students entering New England Job Training Centers each year. Strategy 1: If no chlamydia screening were performed, then 106 women per year were estimated to develop PID and 20 past, present, and future male partners were estimated to develop epididymitis for a total cost of $200,000. Strategy 2: Endocervical DNA probe screening reduced the number of PID cases to 42 and the number of epididymitis cases to 6 for a total cost of $138,000. Strategy 3: Urine NAAT screening further reduced the number of PID cases to 28 and epididymitis cases to 3 for a total cost of $127,000. Strategy 4: Endocervical NAAT screening resulted in just 19 PID cases and 1 epididymitis case with a total cost of $111,000 and an overall savings of $89,000 (Table 4).
Screening was based on a hypothetical cohort of 2000 male students entering New England Job Training Centers each year. Strategy 1: If no chlamydia screening were performed, then 5 men per year were estimated to develop epididymitis and 81 past, present, and future female partners were estimated to develop PID for a total cost of $149,000. Strategy 2: Selective NAAT screening of men whose urine LE result is trace + or greater reduced the number of epididymitis cases to 2 and the number of PID cases among past, present, and future female partners to 53 for a total cost of $113,000. Strategy 3: Universal urine NAAT screening further reduced the number of epididymitis cases to 1 and the number of PID cases among female partners to 32 for a total cost of $97,000 and an overall savings of $52,000 as compared to no screening (Table 4).
Prevalence Threshold Analyses
Regardless of chlamydia prevalence, endocervical DNA probe and urine NAAT were never cost saving as compared with all other strategies; however, the “No Screening” strategy became less expensive than endocervical NAAT screening when the prevalence was less than 6.3%. Nevertheless, at the 6.3% prevalence threshold, endocervical NAAT screening still prevented 31 cases of PID when compared with “No Screening.”
Selective NAAT screening of LE positive men became more cost saving than universal NAAT screening when the prevalence of chlamydia was less than 4%. Screening of any type no longer saved money when the prevalence was less than 1.5%.
Endocervical DNA probe screening became more cost saving than endocervical NAAT screening under the following conditions: a NAAT processing fee greater than $25, rate of PID development less than 13%, PID sequelae treatment costs less than $250, or rate of silent PID developing in infected students before screening and treatment greater than 22%. In all these conditions, the endocervical NAAT still prevented more PID than the endocervical DNA probe. Likewise, the endocervical NAAT always prevented more PID than “No Screening,” but no longer saved money under the following conditions: a NAAT processing fee greater than $54, rate of PID development less than 16%, or PID sequelae treatment costs less than $455. Given that the processing cost for the urine NAAT is the same as for the endocervical NAAT, the less sensitive urine NAAT never saved money compared with the endocervical NAAT.
Intention to Test.
Urine screening occurs at the nursing admission visit, but the physical examination with pelvic examination is scheduled within 14 days of admission. Consequently, in our sample of 450 women, 118 (26%) did not receive endocervical DNA Probe screening within 14 days of admission to the job training program. The most common reasons for lack of DNA probe screening were that the pelvic exam was deferred because the patient was menstruating or she had left the job training program soon after arrival and never had an admission physical. As a result, if estimates of proportion of infections detected were adjusted for likelihood of receiving a speculum examination with endocervical NAAT screening (74%), then the endocervical NAAT detection rate would drop to 69% (sensitivity of 93.3% × 74% screened = 69%). In this more realistic scenario, the urine NAAT with its nearly 100% “capture rate” would prevent more PID cases (78 vs. 64) and save $12,000 more than the endocervical NAAT with a 74% “capture rate.” However, if the endocervical NAAT capture rate were as high as 90%, then the number of PID cases prevented by endocervical NAAT would be the same as by urine NAAT.
Effect of Rate of Refusal.
If none of the female students who declined participation in the urine NAAT prevalence study (n = 100) was infected with chlamydia, then the true chlamydia prevalence in female job training students would drop to 14.3% (17.7% of 417 sexually active female participants screened = 74 infections; 74 ÷ 517 = 14.3%), which is well above the threshold of 6.3% where “No Screening” becomes more cost saving than endocervical NAAT screening. If, on the other hand, the chlamydia prevalence of those who refused urine NAAT screening during the prevalence study was twice as high as that of those who participated, then the overall prevalence would rise to 21.2%.
As the endocervical NAAT “capture rate” (proportion of students receiving pelvic examinations and thus endocervical NAAT screening) decreased, the urine NAAT sensitivity required to make urine NAAT more cost-effective than endocervical NAAT also decreased (Fig. 1).
Selective NAAT screening of LE positive men became more cost saving than universal NAAT screening under the following conditions: a NAAT processing fee greater than $23, average number of future female partners less than 0.4, chlamydia transmission rate from men to women less than 34%, PID rate less than 14%, LE sensitivity greater than 79%, or PID sequelae treatment costs less than $650.
Effect of Future Female Partners Entering the Relationship Already Infected.
Given that 17.7% of the job training program female students in this study were infected with chlamydia, it is reasonable to estimate that the probability of an index male’s future female partner already having a chlamydia infection is 17.7%. This would reduce the average number of uninfected future female partners to 1.3, yet universal NAAT screening would still remain the most cost-saving strategy.
Effect of Rate of Refusal.
If none of the male students who declined participation in the urine NAAT prevalence study (n = 86) was infected with chlamydia, then the true chlamydia prevalence would drop to 6.6%, which is above the threshold of 4.0% where universal NAAT screening is more cost saving than selective NAAT screening. Alternatively, if the chlamydia prevalence of those who refused was twice as high as that of those who participated, then the overall prevalence would rise to 9.4%.
As NAAT processing cost increased, the selective NAAT screening strategy became more cost saving than universal NAAT screening at higher PID sequelae costs (Fig. 2). Likewise, as NAAT processing cost increased, more future partners would be required for universal NAAT screening to remain more cost saving than selective NAAT screening (Fig. 3).
Female and Male Screening Strategy Combinations
The combination that saved the most money while preventing the most number of PID cases was endocervical NAAT screening of women + universal urine NAAT screening of men (Table 5). Although the screening costs for this strategy combination are higher than for other strategy combinations, the improved sensitivity and thus the cost savings due to PID prevention more than compensate for the increased screening costs. Table 5 also demonstrates that the combination of endocervical DNA probe screening of women + universal urine NAAT screening of men yields similar cost savings and PID prevention as the combination of endocervical NAAT screening of women + selective NAAT screening of men whose LE is positive. In other words, if it were necessary to reduce upfront screening costs, then PID prevention and overall cost savings are similar whether one chooses the more sensitive (but more expensive) test to screen women and the less sensitive (but less expensive) test to screen men or one chooses the more sensitive (more expensive) test to screen men and the less sensitive (less expensive) test to screen women.
This economic analysis of chlamydia screening strategies for sexually active students entering a national job training program has demonstrated that universal NAAT screening of female and male students upon training program entry was not only cost-effective, but also cost saving. For women, endocervical NAAT screening prevented 23 cases of PID and saved $27,000 as compared with DNA Probe screening. For men, universal NAAT screening prevented 21 cases of PID in past, present, and future partners and saved $16,000, when compared with selective NAAT screening of LE positive students. To ensure that only sexually active students are screened for chlamydia, information about sexual history will need to be included in the screening health history that students complete at their nursing admission.
Several previous studies with different populations of women have demonstrated the cost-effectiveness of annual NAAT-based chlamydia screening.11,26–32 However, only a few comparable studies have been conducted for men, and these have reported conflicting results.27,33–35 Furthermore, only 1 other study has evaluated the cost-effectiveness of simultaneously screening women and men.27 The current study goes 1 step further by directly comparing the cost-effectiveness of female screening to male screening via various strategy combinations. To our knowledge, this is the first study to do so.
When we directly compared the cost-effectiveness of female screening strategies to male screening strategies, our results demonstrated that the incremental number of PID cases prevented by choosing the more sensitive chlamydia test to screen male students was potentially equivalent to the incremental number of PID cases prevented by choosing the more sensitive chlamydia test to screen female students. The reason for this counterintuitive finding is because when a male infection is detected and treated, it potentially averts infection of (and PID in) multiple future female partners. Whereas, when a female infection is detected, only 1 case of PID is potentially averted, and only if she has not already developed silent PID before receiving treatment. While very worthwhile, screening and treating infected women is a secondary prevention strategy. In contrast, treating the reservoir of infected young men serves as a means of primary prevention for their future female sexual partners. Economic analyses that have not shown universal NAAT screening to be cost-effective in men did not take future partners into account.34,35
We have previously demonstrated in a male detention setting that screening all sexually active men for chlamydia upon admission is cost-effective, primarily due to the prevention of PID in future partners who will not be infected as a result of screening and treatment of the index male during detention.33 This point was recently highlighted by Fisman and Edmunds who used simulation studies to demonstrate that future transmissibility of an asymptomatic sexually transmitted infection is an important factor in determining whether asymptomatic screening is cost-effective.76 In their model, asymptomatic screening was not cost-effective when future transmissibility was not accounted for, but became increasingly more cost-effective with every generation of partners who avoided infection as a result of asymptomatic screening and treatment of the index case.76 Our study is limited by not using a dynamic model as Fisman and Edmunds did. Our model only accounts for the first generation of future partners; however, the job training programs are not closed systems with regard to sexual networks. Consequently, the mixing that occurs when a job-training student has intercourse with a nonjob-training student violates an assumption intrinsic to a dynamic model: with every generation screened in a closed system, the population prevalence will be reduced. To use a dynamic model, we would need to evaluate populationwide chlamydia screening beyond the job-training program.
As with any cost-effectiveness analysis, the results of this analysis are strongly influenced by the assumptions made and the parameter estimates used in the model. The parameter estimate most strongly driving the cost savings associated with male screening is the number of female sexual partners. Furthermore, the number of future sexual partners is more influential than the number of recent past or present sexual partners. Given that adolescents are known to engage in serial monogamy and concurrent partnerships, 39,77,78 it is reasonable to postulate that if the average young person reports 1.6 partners in the past 2 months, then he is likely to have an additional 1.6 partners in the future 2–12 months. The number of sexual partners reported in this study is consistent with previous estimates.27,39
The other parameter estimates driving the results were the NAAT testing fee, chlamydia transmission rate, LE sensitivity, probability of developing PID and cost of PID sequelae (which is related to probability of PID sequelae developing). NAAT processing fees are much more likely to drop than to rise given the greater degree of automation offered in each new generation of these tests. Chlamydia transmission rates reported in the literature57–59 are well above the threshold where selective NAAT screening became more cost saving than universal NAAT screening. Most studies have demonstrated an LE sensitivity of <80%.52 The 1 study that found an LE sensitivity of 80% was conducted with a sample size of only 10 chlamydia-positive participants.53
The final 2 parameter estimates driving the results of this study, probability of developing PID and cost and probability of developing PID sequelae, have been the subject of debate. Some authors have suggested that estimates used in CEAs have overestimated the true values of these parameters.66,79 van Valkengoed et al. concluded that the actual probability of clinical PID, ectopic pregnancy, and tubal factor infertility following a chlamydia infection are less than 1%.79 However, their estimates were based on medical register rates from Amsterdam, the Netherlands, which may not be generalizable to the United States. Additionally, they did not include subacute PID or chronic pelvic pain in the complication estimates because they assert that these 2 outcomes are not well documented.79
Rein et al. have estimated that the lifetime cost per case of PID and its sequelae ranges from $1105 to $1235 in 1998 dollars ($1275–$1424 in 2005 dollars).66 Rein’s estimate was also included in a natural history model developed by Yeh that follows a woman through a series of health transitions over time. Yeh concluded that the lifetime estimate of PID costs per woman lies between $1060 and $3180 in 2000 dollars ($1168–$3505 in 2005 dollars).10 However, Rein and Gift have asserted that 2 of the studies referenced by Yeh overestimated costs such that it may be more appropriate to use a narrower range of $1060–$1410 ($1168–$1554 in 2005 dollars).80 Our cost and probability estimates for development, treatment, and sequelae of PID sum to a lifetime PID cost estimate of $1730 in 2005 dollars, which is just above the revised range recommended by Rein and Gift, and our sensitivity analyses have demonstrated that even using the lower bound of $1168, NAAT screening remained the more cost saving strategy.
Perhaps the most compelling finding from our study is not how much money is saved or expended as a consequence of chlamydia screening but rather that use of a more expensive and more sensitive screening test in place of a less expensive, less sensitive screening test is just as cost-effective for male screening as for female screening, suggesting that NAAT based chlamydia screening of men is a judicious use of limited screening resources.
Our results have limited generalizability beyond a job training setting or perhaps a military setting because they assume a higher treatment rate (due to the residential nature of the national job training program) than is often achieved in the community. Yet, they are important because they demonstrate the feasibility, effectiveness, and cost-effectiveness of screening a population that is at particularly high risk for chlamydia infection. Furthermore, in analyses not reported, a subset of this same cohort reported that only 52% had a primary care provider, only 38% (46% of women and 30% of men) had been tested for an STD in the past year, and only 22% recalled being tested for chlamydia in the past year (Blake et al., unpublished data). This suggests that approximately two-thirds of the students would not otherwise have received chlamydia screening if they had not entered the job-training program.
The results reported in this study are based on a cohort of 4000 students entering New England job training centers annually. Nationally, 64,000 students enter job training centers annually, and recent national estimates for chlamydia prevalence in job training students suggest that the average male prevalence is 8.2% and average female prevalence is 15.8%.49,81 If the other parameter estimates used for this cohort are true for other parts of the country, then the National Job Training Program’s current policy of screening all entering job training students for chlamydia using a NAAT will prevent 704 annual cases of PID and save $688,000 when compared with the previous policy of DNA Probe chlamydia screening among women and LE screening among men.
In conclusion, universal NAAT screening of both female and male youth entering a national job training program offered the most cost-effective screening policy for preventing PID in these young women and in the recent past, present, and future female partners of these young men.
The modified meta-analytic procedure has been previously described.33 Using the same procedure, a Medline search was conducted for all articles reporting the performance of endocervical PACE2, endocervical BDProbeTec, urine LCx, and urine BDProbeTec for detecting chlamydia among women between 1966 and July 1, 2004. Twenty articles met criteria for inclusion in the weighted sensitivity and specificity analysis of urine LCx47,48,82–96 and urine BDProbeTec,40–42 4 articles met criteria for inclusion in the endocervical BDProbeTec sensitivity and specificity analysis,41–44 and 8 articles met criteria for inclusion in the PACE2 sensitivity and specificity analysis.44–48,50,51,90
The pooled sensitivities were calculated for PACE2, LCx, and BDProbeTec by using the total number of infected participants for each test as the denominator and the total number of infections detected by the respective test as the numerator. Likewise, the pooled specificities were calculated by using the total number of uninfected participants for each test as the denominator and the total number of true negatives for each respective test as the numerator.
Eight thousand five hundred six women who were tested for chlamydia with endocervical PACE 2, 821 were infected (prevalence = 9.7%), and 565 were detected (sensitivity = 68.8%). Of the 7685 uninfected women, the PACE2 correctly identified 7669 (specificity = 99.8%). Two thousand six hundred eighty-two women were tested for chlamydia with endocervical BDProbeTec, 231 were infected (prevalence = 8.6%), and 216 were detected (sensitivity = 93.5%). Of the 2451 uninfected women, the BDProbeTec correctly identified 2425 (specificity = 98.9%). Fifteen thousand seven hundred twelve women were tested for chlamydia with a urine LCx, 1366 were infected (prevalence = 8.7%), and 1149 were detected (sensitivity = 84.1%). Of the 14,346 uninfected women, the LCx correctly identified 14,328 (specificity = 99.9%). Thousand nine hundred forty women were tested for chlamydia with a urine BDProbeTec, 183 were infected (prevalence = 9.4%), and 153 were detected (sensitivity = 83.6%). Of the 1757 uninfected women, the BDProbeTec correctly identified 1735 (specificity = 98.7%).
Sensitivity and specificity of the LCx and BDProbeTec were weighted to estimate the true chlamydia prevalence because each test was used for a portion of the prevalence study. The pooled sensitivity and specificity for each test were weighted according to how many participants were studied resulting in a sensitivity of 84.0% and a specificity of 99.7%.
1. Mertz KJ, Voigt RA, Hutchins K, et al; Jail STD Prevalence Monitoring Group. Findings from STD screening of adolescents and adults entering corrections facilities: Implications for STD control strategies. Sex Transm Dis 2002; 29:834–839.
2. Nsuami M, Cammarata CL, Brooks BN, et al. Chlamydia and gonorrhea co-occurrence in a high school population. Sex Transm Dis 2004; 31:424–427.
3. Rogers SM, Miller HG, Miller WC, et al. NAAT-identified and self-reported gonorrhea and chlamydial infections: Different at-risk population subgroups? Sex Transm Dis 2002; 29:588–596.
4. Kahn R, Moseley K, Thilges J, et al. Community-based screening and treatment for STDs: Results from a mobile clinic initiative. Sex Transm Dis 2003; 30:654–658.
5. Blake DR, Kearney MH, Oakes JM, et al. Improving participation in chlamydia screening programs: Perspectives of high-risk youth. Arch Pediatr Adolesc Med 2003; 157:523–529.
6. Kellock DJ, Piercy H, Rogstad KE. Knowledge of Chlamydia trachomatis infection in genitourinary medicine clinic attenders. Sex Transm Infect 1999; 75:36–40.
7. Devonshire P, Hillman R, Capewell S, et al. Knowledge of Chlamydia trachomatis genital infection and its consequences in people attending a genitourinary medicine clinic. Sex Transm Infect 1999; 75:409–411.
8. Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines 2002. MMWR Recomm Rep 2002; 51:1–78.
9. Washington AE, Katz P. Cost of and payment source for pelvic inflammatory disease. Trends and projections, 1983 through 2000. JAMA 1991; 266:2565–2569.
10. Yeh JM, Hook EW III, Goldie SJ. A refined estimate of the average lifetime cost of pelvic inflammatory disease. Sex Transm Dis 2003; 30:369–378.
11. Paavonen J, Puolakkainen M, Paukku M, et al. Cost-benefit analysis of first-void urine Chlamydia trachomatis screening program. Obstet Gynecol 1998; 92:292–298.
12. 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.
13. Jones RB, Mammel JB, Shepard MK, et al. Recovery of Chlamydia trachomatis from the endometrium of women at risk for chlamydial infection. Am J Obstet Gynecol 1986; 155:35–39.
14. Stamm WE, Guinan ME, Johnson C, et al. Effect of treatment regimens for Neisseria gonorrhoeae on simultaneous infection with Chlamydia trachomatis. N Engl J Med 1984; 310:545–549.
15. Haddix AC, Hillis SD, Kassler WJ. The cost effectiveness of azithromycin for Chlamydia trachomatis infections in women. Sex Transm Dis 1995; 22:274–280.
16. 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.
17. Westrom L, Joesoef R, Reynolds G, et al. Pelvic inflammatory disease and fertility. A cohort study of 1844 women with laparoscopically verified disease and 657 control women with normal laparoscopic results. Sex Transm Dis 1992; 19:185–192.
18. Westrom L, Bengtsson LP, Mardh P-A. Incidence, trends, and risks of ectopic pregnancy in a population of women. Br Med J (Clin Res Ed) 1981; 282:15–18.
19. Siegel J. Estimates of the economic burden of STDs: Review of the literature with updates. In: Eng TR, Butler WT, eds. The Hidden Epidemic. Washington, DC: National Academy Press, 1997:330–356.
20. Kaufman RE, Wiesner PJ. Nonspecific urethritis. N Engl J Med 1974; 291:1175–1177.
21. Washington AE, Johnson RE, Sanders LL Jr. Chlamydia trachomatis infections in the United States: What are they costing us? JAMA 1987; 257:2070–2072.
22. Blake DR, Fletcher KE, Fortenberry JD, et al. Predictors of job corps students’ readiness to receive chlamydia testing. Paper Presented at: The 2004 National STD Prevention Conference; 2004; Philadelphia, PA.
23. Blake DR, Fletcher KE, Fortenberry JD, et al. Determinants of detained male youth’s willingness to be tested for chlamydia [abstract]. J Adolesc Health 2003; 32:144–145.
24. Institute of Medicine Committee on Prevention and Control of Sexually Transmitted Disease. The Hidden Epidemic: Confronting Sexually Transmitted Disease. Washington, DC: National Academy Press, 1997.
25. Rietmeijer C, Bull SS, Ortiz CG, et al. Patterns of general health care and STD services use among high-risk youth in Denver participating in community-based urine chlamydia screening. Sex Transm Dis 1998; 25:457–463.
26. Mehta SD, Bishai D, Howell MR, et al. Cost-effectiveness of five strategies for gonorrhea and chlamydia control among female and male emergency department patients. Sex Transm Dis 2002; 29:83–91.
27. Wang LY, Burstein GR, Cohen DA. An economic evaluation of a school-based sexually transmitted disease screening program. Sex Transm Dis 2002; 29:737–745.
28. Howell MR, Quinn TC, Brathwaite W, et al. Screening women for Chlamydia trachomatis in family planning clinics: The cost-effectiveness of DNA amplification assays. Sex Transm Dis 1998; 25:108–117.
29. Marrazzo JM, Celum CL, Hillis SD, et al. Performance and cost-effectiveness of selective screening criteria for Chlamydia trachomatis in women: Implications for a national chlamydia control strategy. Sex Transm Dis 1997; 24:131–141.
30. Genc M, Mardh P-A. A cost-effectiveness analysis of screening and treatment for Chlamydia trachomatis infection in asymptomatic women. Ann Intern Med 1996; 124(1 Pt 1):1–7.
31. Howell MR, Gaydos JC, McKee KT Jr, et al. Control of Chlamydia trachomatis infections in female army recruits: Cost-effectiveness of screening and treatment in training cohorts to prevent pelvic inflammatory disease. Sex Transm Dis 1999; 26:519–526.
32. Howell MR, McKee KT Jr, Gaydos JC, et al. Point-of-entry screening for C. trachomatis in female army recruits. Who derives the cost savings? Am J Prev Med 2000; 19:160–166.
33. Blake DR, Gaydos CA, Quinn TC. Cost-effectiveness analysis of screening adolescent males for chlamydia on admission to detention. Sex Transm Dis 2004; 31:85–95.
34. Ginocchio RH, Veenstra DL, Connell FA, et al. The clinical and economic consequences of screening young men for genital chlamydial infection. Sex Transm Dis 2003; 30:99–106.
35. Mrus JM, Biro FM, Huang B, et al. Evaluating adolescents in juvenile detention facilities for urogenital chlamydial infection: Costs and effectiveness of alternative interventions. Arch Pediatr Adolesc Med 2003; 157:696–702.
36. Lipscomb J, Weinstein M, Torrance G. Time preference. In: Gold M, Siegel J, Russell L, et al., eds. Cost-Effectiveness in Health and Medicine. New York: Oxford University Press, 1996:214–246.
37. Blanchard J. Populations, pathogens, and epidemic phases: Closing the gap between theory and practice in the prevention of sexually transmitted diseases. Sex Transm Infect 2002; 78 (Suppl 1):i183–i188.
38. Jolly A, Wylie JL. Gonorrhoea and chlamydia core groups and sexual networks in Manitoba. Sex Transm Infect 2002; 78 (Suppl 1):i145–i151.
39. Santelli JS, Brener ND, Lowry R, et al. Multiple sexual partners among US adolescents and young adults. Fam Plan Perspect 1998; 30:271–275.
40. Chan EL, Brandt K, Olienus K, et al. Performance characteristics of the Becton Dickinson ProbeTec System for direct detection of Chlamydia trachomatis and Neisseria gonorrhoeae in male and female urine specimens in comparison with the Roche Cobas System. Arch Pathol Lab Med 2000; 124:1649–1652.
41. Van Der Pol B, Ferrero DV, Buck-Barrington L, et al. Multicenter evaluation of the BDProbeTec ET system for detection of Chlamydia trachomatis and Neisseria gonorrhoeae in urine specimens, female endocervical swabs, and male urethral swabs. J Clin Microbiol 2001; 39:1008–1016.
42. McCartney R, Walker J, Scoular A. Detection of Chlamydia trachomatis in genitourinary medicine clinic attendees: Comparison of strand displacement amplification and the ligase chain reaction. Br J Biomed Sci 2001; 58:235–238.
43. Van Dyck E, Ieven M, Pattyn S, et al. Detection of Chlamydia trachomatis and Neisseria gonorrhoeae by enzyme immunoassay, culture, and three nucleic acid amplification tests. J Clin Microbiol 2001; 39:1751–1756.
44. Pollara C, Terlenghi L, De Franscesco MA, et al. Comparative evaluation of BDProbeTec ET, LCx and PACE 2 assays for the detection of Chlamydia trachomatis in urogenital specimens. Eur J Clin Microbiol Infect Dis 2003; 22:512–514.
45. Semeniuk H, Zentner A, Read R, et al. Evaluation of sequential testing strategies using non-amplified and amplified methods for detection of Chlamydia trachomatis in endocervical and urine specimens from women. Diagn Microbiol Infect Dis 2002; 42:43–51.
46. Wylie JL, Moses S, Babcock R, et al. Comparative evaluation of chlamydiazyme, PACE 2, and AMP-CT assays for detection of Chlamydia trachomatis in endocervical specimens. J Clin Microbiol 1998; 36:3488–3491.
47. Carroll KC, Aldeen WE, Morrison M, et al. Evaluation of the abbott LCx ligase chain reaction assay for detection of Chlamydia trachomatis and Neisseria gonorrhoeae in urine and genital swab specimens from a sexually transmitted disease clinic population. J Clin Microbiol 1998; 36:1630–1633.
48. Lauderdale T-L, Landers L, Thorneycroft I, et al. Comparison of the PACE 2 assay, two amplification assays, and clearview EIA for detection of Chlamydia trachomatis in female endocervical and urine specimens. J Clin Microbiol 1999; 37:2223–2229.
49. Black CM, Marrazzo JM, Johnson RE, et al. Head-to-head multicenter comparison of DNA probe and nucleic acid amplification tests for Chlamydia trachomatis infection in women performed with an improved reference standard. J Clin Microbiol 2002; 40:3757–3763.
50. Modarress KJ, Cullen AP, Jaffurs WJ Sr, et al. Detection of Chlamydia trachomatis and Neisseria gonorrhoeae in swab specimens by the hybrid capture II and PACE 2 nucleic acid probe tests. Sex Transm Dis 1999; 26:303–308.
51. Pasternack R, Vuorinen P, Kuukankorpi A, et al. Detection of Chlamydia trachomatis infections in women by Amplicor PCR: Comparison of diagnostic performance with urine and cervical specimens. J Clin Microbiol 1996; 34:995–998.
52. Blake DR, Lemay CA, Gaydos CA, et al. Performance of urine leukocyte esterase in asymptomatic male youth: Another look with nucleic acid amplification testing as the gold standard for chlamydia detection. J Adolesc Health 2005; 36:337–341.
53. Anestad G, Berdal B, Scheel O, et al. Screening urine samples by leukocyte esterase test and ligase chain reaction for chlamydial infections among asympotmatic men. J Clin Microbiol 1995; 33:2483–2484.
54. 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.
55. 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.
56. Bowden FJ. Reappraising the value of urine leukocyte esterase testing in the age of nucleic acid amplification. Sex Transm Dis 1998; 25:322–326.
57. Quinn TC, Gaydos CA, Shepherd M, et al. Epidemiologic and microbiologic correlates of Chlamydia trachomatis infection in sexual partnerships. JAMA 1996; 276:1737–1742.
58. Lin J-SL, Donegan SP, Heeren TC, et al. Transmisssion of Chlamydia trachomatis and Neisseria gonorrhoeae among men with urethritis and their female sex partners. J Infect Dis 1998; 178:1707–1712.
59. Viscidi R, Bobo L, Hook EWR, et al. Transmission of Chlamydia trachomatis among sex partners assessed by polymerase chain reaction. J Infect Dis 1993; 168:488–492.
60. Zimmerman HL, Potterat JJ, Dukes RL, et al. Epidemiologic differences between chlamydia and gonorrhea. Am J Public Health. 1990; 80:1338–1342.
61. 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.
62. Katz BP, Danos CS, Quinn TS, et al. Efficiency and cost-effectiveness of field follow-up for patients with Chlamydia trachomatis infection in a sexually transmitted diseases clinic. Sex Transm Dis1988; 15:11–16.
63. Hook EWR, Spitters C, Reichart CA, et al. Use of a cell culture and a rapid diagnostic assay for Chlamydia trachomatis screening. JAMA. 1994; 272:867–870.
64. Bachman LH, Richey C, Waites K, et al. Patterns of Chlamydia trachomatis testing and follow-up at a university hosptial medical center. Sex Transm Dis 1999; 26:496–499.
65. Westrom L, Eschenbach DA. Pelvic inflammatory disease. In: Holmes KK, Sparling PF, Mardh P-A, et al., eds. Sexually Transmitted Diseases, 3rd ed. New York: McGraw-Hill, 1999:783–809.
66. Rein DB, Kassler WJ, Irwin KL, et al. Direct medical cost of pelvic inflammatory disease and its sequelae: Decreasing, but still substantial. Obstet Gynecol 2000; 95:397–402.
67. Ness RB, Soper DE, Holley RL, et al. Effectiveness of inpatient and outpatient treatment strategies for women with pelvic inflammatory disease: Results from the Pelvic Inflammatory Disease Evaluation and Clinical Health (PEACH) randomized trial. Am J Obstet Gynecol 2002; 186:929–937.
68. Shafer M-A, Pantell RH, Schachter J. Is the routine pelvic examination needed with the advent of urine-based screening for sexually transmitted diseases? Arch Pediatr Adolesc Med 1999; 153:119–125.
69. Simonsen L, Conn L, Pinner RW, et al. Trends in infectious disease hospitalizations in the United States, 1980–1994. Arch Intern Med 1998; 158:1923–1928.
70. Hirsch MB, Mosher WD. Characteristics of infertile women in the United States and their use of infertility services. Fertil Steril 1987; 47:618–625.
71. Thompson Medical Economics. Drug Topics Redbook Update. Montvale, NJ: Thompson Medical Economics, 2002.
72. The Medical Letter. The choice of antibacterial drugs. Med Lett Drugs Ther 1999; 41:95–104.
73. VanderLaan B, Karande V, Krohm C, et al. Cost considerations with infertility therapy: Outcome and cost comparison between health maintenance organization and preferred provider organization care based on physician and facility cost. Hum Reprod 1998; 13:1200–1205.
74. van Valkengoed IGM, Postma MJ, Morre SA, et al. Cost effectiveness analysis of a population based screening programme for asymptomatic Chlamydia trachomatis infections in women by means of home obtained urine specimens. Sex Transm Infect 2001; 77:276–282.
75. Petitta A, Hart SM, Bailey EM. Economic evaluation of three methods of treating urogenital chlamydial infections in the emergency department. Pharmacotherapy 1999; 19:648–654.
76. Fisman DN, Edmunds J. The importance of transmissibility in evaluating cost-effectiveness of STI prevention: Lessons from simulation studies. Paper Presented at: The 16th Biennial Meeting of the International Society for Sexually Transmitted Disease Research (ISSTDR), July 11, 2005, Amsterdam, The Netherlands.
77. Rosenberg MD, Gurvey JE, Adler N, et al. Concurrent sex partners and risk for sexually transmitted diseases among adolescents. Sex Transm Dis 1999; 26:208–212.
78. Norris AE, Ford K. Sexual experiences and condom use of heterosexual, low-income African American and Hispanic youth practicing relative monogamy, serial monogamy, and nonmonogamy. Sex Transm Dis 1999; 26:17–25.
79. van Valkengoed IG, Morre SA, van den Brule AJC, et al. Overestimation of complication rates in evaluations of Chlamydia trachomatis screening programmes—Implications for cost-effectiveness analyses. Int J Epidemiol 2004; 33:416–425.
80. Joesoef M, Mosure D. Prevalence of Chlamydia in young men in the United States from newly implemented universal screening in a national job training program. Sex Transm Dis 2006; 33:636–639.
81. Rein DB, Gift TL. A refined estimate of the lifetime cost of pelvic inflammatory disease. Sex Transm Dis 2004; 31:325.
82. Joesoef M, Mosure D. Trends in Chlamydia trachomatis infections in young women entering a national job training program, 1998–2004. Paper Presented at: The 16th Biennial Meeting of the International Society for Sexually Transmitted Disease Research, July 12, 2005, Amsterdam, The Netherlands.
83. Gaydos CA, Howell MR, Quinn TC, et al. Use of ligase chain reaction with urine versus cervical culture for detection of Chlamydia trachomatis in an asymptomatic military population of pregnant and nonpregnant females attending papanicolaou smear clinics. J Clin Microbiol 1998; 36:1300–1304.
84. Stary A, Schuh E, Kerschbaumer M, et al. 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.
85. Pasternak R, Vuorinen P, Pitkajarvi T, et al. Comparison of manual Amplicor PCR, COBAS Amplicor PCR, and LCx assays for detection of Chlamydia trachomatis infection in women by using urine specimens. J Clin Microbiol 1997; 35:402–405.
86. Buimer M, van Doornum GJJ, Ching S, et al. Detection of Chlamydia trachomatis and Neisseria gonorrhoeae by ligase chain reaction-based assays with clinical specimens from various sites: Implications for diagnostic testing and screening. J Clin Microbiol 1996; 34:2395–2400.
87. Bassiri M, Hu HY, Domeika MA, et al. Detection of Chlamydia trachomatis in urine specimens from women by ligase chain reaction. J Clin Microbiol 1995; 33:898–900.
88. van Doornum GJJ, Buimer M, Prins M, et al. Detection of Chlamydia trachomatis infection in urine samples from men and women by ligase chain reaction. J Clin Microbiol 1995; 33:2042–2047.
89. Goessens WH, Mouton JW, van der Meijden WI, et al. Comparison of three commercially available amplification assays, AMP CT, LCx, and COBAS AMPLICOR, for detection of Chlamydia trachomatis in first-void urine. J Clin Microbiol 1997; 35:2628–2633.
90. van Doornum GJJ, Schouls LM, Pijl A, et al. Comparison between the LCx probe system and the COBAS Amplicor system for detection of Chlamydia trachomatis and Neisseria gonorrhoeae infections in patients attending a clinic for treatment of sexually transmitted diseases in Amsterdam, The Netherlands. J Clin Microbiol 2001; 39:829–835.
91. Doing KM, Curtis K, Long JW, et al. Prospective comparison of the Gen-probe PACE 2 assay and the Abbott ligase chairn reaction for the direct detection of Chlamydia trachomatis in a low prevalence population. J Med Microbiol 1999; 48:507–510.
92. Schachter J, Moncada J, Whidden R, et al. Noninvasive tests for diagnosis of Chlamydia trachomatis infection: Application of ligase chain reaction to first-catch urine specimens of women. J Infect Dis 1995; 172:1411–1414.
93. Chernesky MA, Jang D, Lee H, et al. Diagnosis of Chlamydia trachomatis infections in men and women by testing first-void urine by ligase chain reaction. J Clin Microbiol 1994; 32:2682–2685.
94. Ridgway GL, Mumtaz G, Robinson AJ, et al. Comparison of the ligase chain reaction with cell culture for the diagnosis of Chlamydia trachomatis infection in women. J Clin Pathol 1996; 49:116–119.
95. Morre SA, Van Valkengoed IG, Moes RM, et al. Determination of Chlamydia trachomatis prevalence in an asymptomatic screening population: Performances of the LCx and COBAS Amplicor tests with urine specimens. J Clin Microbiol 1999; 37:3092–3096.
96. Puolakkainen M, Hiltunen-Back E, Reunala T, et al. Comparison of performances of two commercially available tests, a PCR assay and a ligase chain reaction test, in detection of urogenital Chlamydia trachomatis infection. J Clin Microbiol 1998; 36:1489–1493.
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