Suboptimal Adherence to Repeat Testing Recommendations for Men and Women With Positive Chlamydia Tests in the United States,

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1 MAJOR ARTICLE Suboptimal Adherence to Repeat Testing Recommendations for Men and Women With Positive Chlamydia Tests in the United States, Karen W. Hoover, 1 Guoyu Tao, 1 Melinda B. Nye, 2 and Barbara A. Body 2 1 Division of STD Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia; and 2 Laboratory Corporation of America Holdings, Burlington, North Carolina Background. Chlamydia is prevalent among young persons in the United States. Infected persons have a high prevalence of infection several months later, most likely from reinfection. Retesting of all men and women with a positive test is recommended 3 months after treatment. A test-of-cure is recommended for pregnant women 3 4 weeks after treatment. Methods. We analyzed chlamydia testing data from a large US laboratory to estimate test positivity by patient demographic characteristics and diagnoses, and patterns of repeat testing of men and nonpregnant women with a positive test and tests-of-cures of pregnant women with a positive test. Results. During the study period, 7.0% of 0.40 million tests performed in men and 4.0% of 2.92 million tests performed in women were positive. Among young women, positivity rates were highest among those aged years, ranging from 8.5% to 10.0%. Retesting rates of persons with a positive test were suboptimal, with 22.3% of men and 38.0% of nonpregnant women retested. Although 60.1% of pregnant women with a positive test were retested, only 22.0% received a test-of-cure within the 4-week recommended time frame. Repeat tests were positive in 15.9% of men, 14.2% of nonpregnant women, and 15.4% of pregnant women. Conclusions. Analyses of laboratory testing data provided important insights into chlamydia testing, retesting, and positivity among a diverse US population of men and women. Too few persons were retested as recommended, and interventions are needed to increase both healthcare provider and patient adherence to recommendations for retesting men and women with positive tests. Keywords. chlamydia; testing; retesting; positivity. More than 1 million chlamydia cases have been reported annually to the Centers for Disease Control and Prevention (CDC) since 2006 [1]. Chlamydial infection is usually asymptomatic in both men and women, but if undiagnosed and untreated it can lead to serious reproductive health complications in women. It is also associated with increased risk of Received 18 May 2012; accepted 24 August 2012; electronically published 16 October Correspondence: Karen Hoover, MD, MPH, National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, 1600 Clifton Rd NE, MS E-80, Atlanta, GA (khoover@cdc.gov). Clinical Infectious Diseases 2013;56(1):51 7 Published by Oxford University Press on behalf of the Infectious Diseases Society of America DOI: /cid/cis771 human immunodeficiency virus (HIV) acquisition and transmission [2, 3]. US guidelines recommend annual screening of all sexually active women aged 25 years, pregnant women, and older women who might have risk factors such as multiple sex partners or a new sex partner [4 7]. Routine screening of sexually active young men is not recommended because it is challenging for programs with limited resources, lack of knowledge of community prevalence, and lack of studies on the impact of routine male screening on rates of chlamydia and outcomes in women [8]. However, it should be considered as a secondary focus to prevent chlamydial infection and sequelae among women. Annual screening of sexually active men who have sex with men (MSM) is recommended for Retesting Men and Women with Chlamydia CID 2013:56 (1 January) 51

2 urethral chlamydia when insertive intercourse is reported and rectal chlamydia when receptive anal intercourse is reported [4, 9, 10]. Despite these recommendations, testing rates have been suboptimal in women and MSM, including HIV-infected MSM [11 15]. Among women diagnosed and treated for chlamydia, several studies have reported a high prevalence of repeated infection several months later [16 19]. Although repeated infection could be due to antibiotic therapy failure, most are thought to be caused by reinfection from an existing untreated partner or new infected sex partner [17, 19]. Repeated chlamydial infection can increase the risk of adverse outcomes of pelvic inflammatory disease, infertility, and ectopic pregnancy [20 22]. CDC guidelines recommend repeat testing of men and women 3 months after treatment, even if the person s sex partners have been treated [4]. If retesting at 3 months is not possible, men and women should be retested at their next clinical encounter. Although a test-of-cure (TOC) is not recommended for men or nonpregnant women, it is recommended for all pregnant women 3 4 weeks after treatment [4, 7]. Assessment of trends in chlamydia testing, positivity, and retesting have been challenging because only limited data have been available. Previous studies have assessed trends in chlamydia testing and positivity, but they have been small or have been done in high-risk populations [23 25]. We estimated the positivity of tests for chlamydia among men and women performed by a large US laboratory that provides a significant proportion of laboratory testing across the United States. We also assessed adherence to retesting recommendations for all infected men and women, and to TOC recommendations for infected pregnant women. METHODS We obtained chlamydia testing data from a US laboratory that provides laboratory testing in all 50 states and Puerto Rico. These data included all chlamydia tests performed in men and women from 1 July 2008 through 31 July Variables in the data set included patient name, age, insurance type, geographic location, associated International Classification of Diseases, Ninth Revision (ICD-9) codes (available for >99% of tests), test type, specimen site, and test result. We assessed retesting patterns for patients who had tests on multiple dates using a combination of patient characteristics to create a de-identified data set to monitor testing over time. The study protocol was approved by the Institutional Review Board at the CDC. Among all chlamydia tests performed by this laboratory from 2008 through 2010, we estimated the number and positivity of tests by sex, age, insurance type, US geographic region of residence, pregnancy status, reason for being tested (diagnosis or screening), and test type. Pregnant women were identified in the data set by ICD-9 codes for pregnancy. A chlamydia test was classified as diagnostic if its associated ICD-9 coding indicated the patient had symptoms or signs of infection such as vaginal, cervical or urethral discharge; dysuria; pelvic pain; or abnormal vaginal bleeding [13] and as screening if its coding was for a preventive, screening, or other type of service. We also calculated the proportion of men and women who had 1, 2, or more tests during the 2-year study period. Using data from the US Census Bureau, we estimated the proportion of persons in the United States in aged years who had private insurance and Medicaid insurance, and the proportion that resided in the South [26]. To estimate repeat testing rates, we limited the analysis to men and women who were tested by the laboratory in the first half of the 2-year study period, from 1 July 2008 through 31 July 2009, to allow at least 12 months of follow-up time for each person. Among men, nonpregnant women, and pregnant women with an initial negative test or their first positive test during this period, we estimated the number and percentage retested through the end of the 2-year study period, 31 July 2010, and the positivity of follow-up tests. We also stratified the number of persons and test positivity among those who had a repeat test by the time interval since an initial negative test or the first positive test: <22 days, days, days, days, days, and >360 days. We calculated the range, mean, and median time to a repeat test. Among pregnant women with a positive test, we also estimated the number and percentage who were retested 3 4 weeks later for a TOC, in accordance with CDC recommendations. We estimated the number of persons who were inappropriately retested within 21 days of a positive test, the period during which organisms that have been killed by antimicrobial therapy might not yet have been cleared and during which a false positive test result could be obtained [27, 28]. All analyses were performed using SAS version 9.2 (SAS Institute). Percentages of persons tested were compared using the χ 2 test, and a 2-sided P value of <.05 was considered to be statistically significant. RESULTS During the 2-year study period, 3.32 million tests were performed: 0.40 million were among men and 2.92 million among women (Table 1). Of the tests performed, 81.9% were for men and 73.3% for women with private insurance; 10.3% were for men and 21.8% for women with Medicaid insurance. In the United States among year-old men and women, 63.6% of men and 65.5% of women had private insurance in , and 10.0% of men and 14.3% of women had Medicaid insurance. Of the tests, 52.9% were in the South, 52 CID 2013:56 (1 January) Hoover et al

3 Table 1. Chlamydia Tests in Men and Women Performed by a Large Commercial Laboratory in the United States, (n = ) Men Women Characteristic No. (%) of Tests No. (%) of Positive Tests No. (%) of Tests No. (%) of Positive Tests Total (7.0) (4.0) Age, y < (3.1) 293 (2.3) (1.6) 2531 (5.6) (16.2) 8138 (12.4) (18.0) (9.4) (16.0) 7956 (12.3) (23.6) (5.5) (28.0) 7583 (6.7) (34.9) (2.1) (20.0) 2909 (3.6) (14.9) 3919 (0.9) > (16.6) 1250 (1.9) (6.9) 1073 (0.5) Insurance Private (81.9) (6.8) (73.3) (3.5) Medicaid (10.3) 3510 (8.5) (21.8) (5.9) Other (7.8) 2130 (6.7) (4.9) 4736 (3.3) Region South (46.4) (7.6) (53.8) (4.4) Other (53.6) (6.4) (46.2) (3.6) Pregnant Yes All ages (31.8) (4.1) Age y (7.0) Age y (1.5) No All ages (68.2) (4.0) Age y (7.3) Age y (1.9) Reason for test Diagnostic All ages (32.7) (8.2) (30.1) (4.1) Age y (15.2) (7.9) Age y (6.5) (1.9) Screening All ages (67.3) (6.4) (69.9) (4.0) Age y (11.2) (6.9) Age y (4.8) (1.7) Test type Nucleic acid amplification (88.6) (7.4) (76.0) (4.9) DNA probe (10.5) (3.8) (23.8) (1.3) Culture 3404 (0.8) 181 (5.3) 5752 (0.2) 178 (3.1) compared with 36.8% of US men and women who lived in the South. Among 0.40 million tests in men, overall 7.0% were positive (Table 1). Positivity of tests was highest among men aged years, ranging from 10.9% to 15.3% with a peak positivity of 15.3% among men aged years (Figure 1). Similar age trends were found for men with private insurance and those with Medicaid insurance (data not shown), but overall 6.8% of tests among privately insured men were positive compared with 8.5% of tests among Medicaid-insured men (P <.01). Tests performed for men with symptoms or signs of chlamydial infection were more likely to be positive (8.2%) compared with tests for screening (6.4%; P <.01). About 98% of tests for men were performed on either urine or urethral specimens. Most of the tests (88.6%) were nucleic acid amplification tests (NAATs). Among 2.92 million tests in women, overall 4.0% were positive. A larger number of tests were performed for women Retesting Men and Women with Chlamydia CID 2013:56 (1 January) 53

4 Figure 1. Positivity of chlamydia tests in men and women by age, aged 25 years (1.65 million) than for women aged <25 years (1.26 million). The proportion of positive tests was highest among younger women, with positivity rates ranging from 8.5% to 10.0% among those aged years, with a peak positivity of 10.0% among 16-year-olds (Figure 1). Positivity rates decreased from 7.4% among women aged 20 years to 2.8% by age 26 years, and rates remained low for older women. We found similar age trends for women with private insurance and Medicaid insurance (data not shown), but overall 3.5% of tests among privately insured women were positive compared with 5.9% among Medicaid-insured women (P <.01). A larger proportion of tests were performed for screening (69.9%) than diagnosis (30.1%), with slightly higher positivity rates among diagnostic tests (4.1% vs 4.0%). Most of the tests were NAATs (76.0%). Among 0.40 million men, 92.8% had only 1 test, 6.3% had 2 tests, and 0.9% had 3 or more tests. Among men who were tested in the first half of the study period, if a test was positive, 22.3% were retested, compared with 8.1% if the initial test was negative; a repeat test was more likely to be positive in men with a positive test (15.9%) than an initial negative one (5.5%; Table 2). The median time interval between the initial and repeat test was shorter if the test was positive (45 days) than negative (105 days). Table 2. Percentage Retested for Chlamydia and Positivity of Retests Among Men and Women With Any Positive Test or an Initial Negative Test, Men Nonpregnant Women Pregnant No. (%) Retested No. (%) Tested No. (%) Retested No. (%) Tested No. (%) Retested No. (%) Tested Characteristic (n = ) Positive (n = ) Positive (n = ) Positive Any positive test Time interval, d Overall 2853 (22.3) 453 (15.9) (38.0) 1964 (14.2) 9163 (60.1) 1409(15.4) < (25.6) 158 (21.6) 2459 (17.8) 554(22.5) 1495 (16.3) 432 (28.9) (42.9) 150 (12.3) 8125 (58.9) 929 (11.4) 6032 (65.8) 762 (12.6) (21.3) 119 (19.6) 2403 (17.4) 415 (17.3) 1206 (13.2) 179 (14.8) (3.0) 7 (8.1) 246 (1.8) 19 (7.7) 170 (1.9) 14 (8.2) (2.2) 8 (12.7) 224 (1.6) 19 (8.5) 107 (1.2) 9 (8.4) > (5.0) 11 (7.8) 331 (2.4) 28 (8.5) 153 (1.7) 13 (8.5) Median (range), d 45 (1 678) 42 (1 714) 42 (1 680) Mean, d Initial negative test Time interval, d Overall (8.1) 760 (5.5) (9.8) 3291 (3.7) (18.3) 2338 (3.5) < (10.2) 46 (3.3) 6947 (7.8) 156 (2.2) 4980 (7.5) 161 (3.2) (32.2) 194 (4.4) (32.2) 856 (3.0) (31.4) 645 (3.1) (36.1) 261 (5.3) (35.0) 1266 (4.0) (35.4) 720 (3.1) (6.0) 63 (7.7) 6539 (7.3) 271 (4.1) 5408 (8.1) 254 (4.7) (5.4) 75 (10.1) 5639 (6.3) 251 (4.5) 4321 (6.5) 189 (4.4) > (10.2) 121 (9.7) (11.5) 491 (4.8) 7421 (11.2) 369 (5.0) Median (range), d 105 (1 712) 112 (1 731) 119 (1 725) Mean, d CID 2013:56 (1 January) Hoover et al

5 Among 2.50 million women tested, 88.1% had only 1 test, 9.4% had 2 tests, and 2.5% had 3 or more tests. Among nonpregnant woman who were tested in the firsthalfofthestudy,ifa test was positive, 38.0% were retested, compared with 9.8% if the initial test was negative; a repeat test was more likely to be positive in women with a positive test (14.2%) than an initial negative one (3.7%; Table 2). The median time interval between the initial and repeat test was shorter if the test was positive (42 days) than negative (112 days). Nonpregnant women aged years with a positive test had a similar retesting rate to that of nonpregnant women aged years (38.0% vs 39.1%). Among pregnant woman who were tested in the first half of the study, if a test was positive, 60.1% were retested, compared with 18.3% if the initial test was negative; a repeat test was more likely to be positive in women with a positive test (15.4%) than an initial negative one (3.5%; Table 2). Among those with a positive test, 22.0% had a recommended TOC 3 4 weeks later. The median time interval between the initial test and TOC was shorter if the test was positive (42 days) than negative (119 days). Table 2 presents the proportion of men, nonpregnant women, and pregnant women with any positive chlamydia test or an initial negative test who were retested by time interval, the range of days between the initial test and the retest, and the mean and median time to retesting. A large proportion of men (17.8%), nonpregnant women (17.8%), and pregnant women (16.3%) were inappropriately retested during the first 22 days following a positive test. Among those retested, many men (42.9%) and nonpregnant women (58.9%) were retested earlier than the 3-month time interval recommended by CDC. DISCUSSION These data from a large laboratory provide insight into chlamydia testing of men and women in the United States, with a robust sample that included of large numbers of tests in persons with both private and public health insurance. These data also can be useful to monitor trends in test positivity among a population of persons whose demographic characteristics are comparable to those of the United States, and our finding of high prevalence of chlamydia among young women supports recommendations for routine screening of sexually active young women. These data can be used to monitor the effectiveness of interventions to increase testing and repeat testing of men and women with chlamydia. Our findings of less than optimal adherence to retesting recommendations are concerning, as this important recommendation is a key part of a strategy to decreasing chlamydia-related morbidity in high-risk persons [4]. Repeat testing of persons with a positive chlamydia test, who are at increased risk of becoming reinfected, is an important intervention to prevent morbidity and decrease chlamydia transmission in the community. Although repeat testing is recommended at 3 months after treatment, guidelines also recommend testing at any clinical encounter up to 12 months after treatment [4]. Repeat testing should be performed even if the patient s partner has been treated. Yet fewer than half of men and nonpregnant women with a positive chlamydia test had a repeat test 3 12 months later as recommended by CDC. A substantial proportion of repeat testing occurred within the first 3 months since the initial positive test, suggesting that these were confirmatory tests, which are not recommended for persons with a positive test; tests-of-cure, which are not recommended for men or nonpregnant women; or repeat screening tests performed too soon after the initial chlamydia diagnosis. Some clinicians might recommend that adolescents return earlier than 3 months for retesting to increase compliance for retesting. Interventions have been developed that were effective in increasing appropriate repeat testing of persons with positive tests [29, 30]. Improvement in repeat testing rates in other settings might be accomplished by wider implementation of such interventions, with evaluation of their effectiveness and planning for sustainability. Untreated chlamydial infection might result in adverse pregnancy and neonatal outcomes [4]. It is encouraging that a large proportion of pregnant women with a positive chlamydia test had a TOC, but only a small proportion had the test within the recommended 4 weeks after treatment. Also, very few pregnant women had a repeat test 3 12 months after a positive test, as is recommended for all men and women with a positive test. Fewer than half of all chlamydia tests were performed in women <25 years old, yet positivity rates were highest in this group. In the United States, only 38% of sexually active women aged years reported that they had received an annual chlamydia test in [31]. Chlamydia testing rates in younger women were low compared with the percentages of women receiving other recommended preventive services such as breast and cervical cancer screening [32], and steps should be taken to assure the provision of this important, cost-effective preventive healthcare service for all sexually active young women. Although in our study older women were less likely to have a positive test compared with younger women, a larger proportion received a diagnostic test for symptoms or signs of infection or a screening test for pregnancy than a routine screening test. We do not know how many older women had behavioral risk factors that would have been an indication for screening, such as a new sex partner or multiple sex partners. One study found that 44% of women aged years were tested for reasons other than pregnancy or sexually transmitted disease (STD) symptoms or signs [33]. The percentage of positive chlamydia tests in men, for both diagnostic testing and screening, was higher than the Retesting Men and Women with Chlamydia CID 2013:56 (1 January) 55

6 percentage of positive tests in women. There are no clinical guidelines recommending routine screening of men, and it is possible that having STD symptoms or a history of risk behavior, or having been informed by a partner that they might be at risk of an infection, might have motivated them to seek healthcare services and made them more likely to have been infected. On the other hand, routine annual screening of all sexually active young women is recommended, regardless of symptoms or risk history. The use of laboratory testing data to assess chlamydia testing and repeat testing presents a few limitations. Women in our database might have had an initial or repeat chlamydia test at a laboratory outside of the laboratory system we used, which would result in underestimates of repeat testing rates. The data did not include treatment information, so we assumed that repeat tests or tests-of-cure were performed in men and women following their treatment. One study found that the median time from diagnostic test to treatment was 13 days [34]. If a repeat test was performed to confirm an initial positive test, then we would have overestimated repeat and TOC rates. The data did not include variables for patient race and ethnicity. Finally, laboratory testing data cannot be used to discern reinfection and persistent infection. Lower than expected retesting rates suggest that many providers in the United States are not following CDC guidelines for repeat testing of women with chlamydial infection. Interventions are needed to increase provider awareness of guidelines and to increase rates of appropriate testing, repeat testing, and TOC. The low retesting rates might also be due to patient factors, and interventions are also required that help patients to understand the importance of retesting and that facilitate their timely return for a retest. Although it is important to increase repeat testing and TOC rates to identify infection in persons who are at a very high risk for reinfection, it is also essential to prevent reinfection through interventions such as expedited partner treatment and counseling to reduce risk behaviors. Notes Financial Support. This work was supported by the Centers for Disease Control and Prevention. Potential conflicts of interest. All authors: No reported conflicts. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed. References 1. Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance Atlanta, GA: US Department of Health and Human Services, Bernstein KT, Marcus JL, Nieri G, Philip SS, Klausner JD. Rectal gonorrhea and chlamydia reinfection is associated with increased risk of HIV seroconversion. 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