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Sexually Transmitted Diseases:
doi: 10.1097/OLQ.0b013e31816d1f6d

Laboratory Aspects of Screening Men for Chlamydia trachomatis in the New Millennium

Gaydos, Charlotte A. MS, MPH, DrPH*; Ferrero, Dennis V. MPH†; Papp, John PhD‡

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From the *Division of Infectious Diseases, Department of Medicine, Johns Hopkins University, Baltimore, Maryland; †Department of Biological Sciences, University of the Pacific, Stockton, California; and ‡Centers for Disease Control and Prevention, Atlanta, Georgia.

Correspondence: Charlotte A. Gaydos, MS, MPH, DrPH, Division of Infectious Diseases, School of Medicine, 1147/1159 Ross Research Building, 720 Rutland Avenue, Baltimore, MD 21205-2196. E-mail:

Received for publication November 13, 2007, and accepted February 11, 2008.

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Objective: To describe and review the methods for laboratory diagnosis of Chlamydia trachomatis in men.

Background: Men provide a reservoir for continued transmission of C. trachomatis to women, thus representing a population for potential targeted screening. Although there are no formal recommendations by professional organizations for screening men for chlamydia, guidance has been provided by the Centers for Disease Control and Prevention for sites wishing to screen men, who are primarily asymptomatic.

Methods: Review of the published literature for diagnostic laboratory tests for C. trachomatis in men.

Results: The laboratory test of choice for screening men is a nucleic acid amplification test (NAAT), and the specimen of choice is first-catch urine. The NAAT has sufficient sensitivity and specificity, and urine provides a noninvasive specimen; together, this combination provides the achievement of sensitivities of >90% to 97% and high specificity (99%). Populations of men, such as those in detention, Job Corps training, emergency departments, the military, and high schools can offer accessible target populations for easily implemented chlamydia screening.

Conclusion: Screening more men with NAAT assays may provide the possibility of reducing the overall burden of chlamydia in both men and women.

CHLAMYDIA TRACHOMATIS IS THE MOST common reportable bacterial sexually transmitted disease (STD) in the United States, with estimates being 3 to 4 million new cases per year and actual numbers being reported at 976,445 cases in 2005.1 Although most chlamydia-associated morbidity is in women, men provide a reservoir for continued transmission for new and recurrent infection among women, and thus, represent a population for targeted screening, especially if they are asymptomatic.2 The Centers for Disease Control and Prevention (CDC) has not made any formal recommendations for screening men for chlamydia, but has recently offered guidance for sites currently screening or planning to institute male screening.3 The guidelines include jailed men over 30 years of age, men attending STD clinics, men attending Job Corps training, men in the military, and men in human immunodeficiency syndrome clinics, as well as men entering juvenile facilities with >2% prevalence and men in emergency departments, high schools, and adolescent clinics with high chlamydia prevalences in the community.3 Men who are not seeking care in STD and other clinics may require screening, if significant impact into the chlamydia epidemic in this country is desired.2 For many years, clinician-collected urethral swabs from men were the only diagnostic specimens, and these may have posed a barrier for screening men for C. trachomatis. However, now that urine-based nucleic acid amplification tests (NAATs) are available, these have been shown to perform better than urethral culture, enzyme immunoassay (EIA), direct fluorescent assay (DFA), or nucleic acid probe for detection of chlamydia 4–10. Availability of noninvasive chlamydia testing may potentially lead to more widespread screening of asymptomatic men in the community.2,11 This review will examine laboratory screening methods for detection of chlamydia in men, who have sex with women, with emphasis on male populations that may benefit most from different screening approaches and diagnostic tools for screening. An extensive and systemic review of the accuracy and efficacy of screening tests for chlamydia, mostly for women, has also been published.12 For men who have sex with men, rectal samples may be the specimen of choice, as urethral swabs or urine samples may miss many infections; however, these samples are not yet Food and Drug Administration (FDA)-cleared for NAAT assays, although some laboratories have performed verification studies and are using them.

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Overview of Laboratory Tests

Available tests for the detection of chlamydia in men include culture in tissue culture cells, DFA tests, EIA, nucleic acid probe hybridization, and the NAATs: polymerase chain reaction (PCR), strand displacement amplification (SDA), and transcription-mediated amplification (TMA). Although all of these tests can be performed with urethral swabs, only the NAATs and the MicroTrak II (Trinity Biotech) EIA urine test are FDA-cleared for use with first void urine (FVU) samples. The NAATs are considered the most sensitive tests for urine specimens. Urine is the specimen of choice when using NAAT assays because the sensitivity and specificity are not significantly different between urine and urethral swabs, and urine specimens are noninvasive.10 Although chlamydia are Gram-negative obligate intracellular bacteria, they cannot be visualized at all by Gram stain. The leukocyte esterase test (LET) is a nonspecific test, which tests for inflammation by detecting the esterase enzyme from white cells in urine, has been previously recommended as a screening tool for men, but is not sensitive compared with NAATs, and is no longer recommended.13,14 Rapid, antigen point-of-care tests are not yet of sufficient sensitivity for use with urine specimens. The recommendation for screening symptomatic and especially asymptomatic men is to use a NAAT assay on a “first void” part (15–20 mL) of a urine (FVU) sample.3

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Isolation of C. trachomatis in cultured cells has long been considered the gold standard for the detection of chlamydia in clinical specimens, but the sensitivity may vary from 60% to 85%.15,16 Culture sensitivity depends on many additional factors such as methodology, type of stain used, shell vials versus microwell plate format, and whether blind passage is used. The moderate-to-poor sensitivity of C. trachomatis culture limits its diagnostic use and the need to obtain a urethral swab followed by extensive laboratory processing restricts it from use in screening. In contrast, C. trachomatis culture is recommended for medicolegal cases for detection of chlamydia in cases of investigations of sexual abuse because of its near-perfect specificity.17 The use of NAATs for medicolegal investigations has received some attention,18,19 and the demonstrated accuracy may allow acceptance of these tests in the future by the legal system.

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Direct Fluorescent Assay

Development of monoclonal antibodies to the major outer membrane protein of C. trachomatis permitted the implementation of a specific DFA test.20,21 As with other tests, the performance of the DFA to detect C. trachomatis from male urethral specimens varies about the reference test. Multisite studies that used culture as a reference demonstrated a sensitivity and specificity of 92% and 98%, respectively (Microtrak package Insert). When compared with NAATs, the DFA has an approximate sensitivity and specificity of 80% to 85% and >99%.22 The DFA test is FDA-cleared for the detection of C. trachomatis infections in the male urethra, pharynx, and rectum. Persons who have receptive anal intercourse are at risk of rectal C. trachomatis infections, and the CDC has recommended annual screening for such individuals.23

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Enzyme Immunoassay

The advent of EIA tests for direct detection of antigen in patient samples provided less-expensive alternatives to tissue culture. However, although this technology offered increased throughput, the sensitivity of the best EIA is comparable with culture.24–26 EIA also suffers from reduced specificity, which may give false-positive reactions. Confirmatory assays that can use blocking assays are recommended. There was further innovation in the early 1990s with the first automated urine test. The MicroTrak II (Trinity Biotech) EIA was FDA-cleared, however, only for men, and was not implemented as a screening tool.

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Probe Hybridization

The first molecular FDA-approved DNA test for C. trachomatis was the nonamplified direct probe test (Pace 2, GenProbe, San Diego, CA). A comparison of this hybridization test with amplified technology indicated lower sensitivity for chlamydia for this assay.27 This assay cannot be used for urine samples. Although probe hybridizations increased further through-put, the sensitivity is comparable to culture and EIA.22

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Leukocyte Esterase Test

The LET is a rapid dipstick test for use with urine specimens to detect urinary infections. It determines the presence of the esterase enzyme produced by polymorphonuclear white cells, which accumulate in urine during any bacterial infection. It is a nonspecific test for diagnosing urethritis because it only detects polymorphonuclear cells and not the etiology. The dipstick has an absorbent area containing indoxylcarbonate ester, which is hydrolyzed by esterase forming a purple color.28 It has been used as a screening test for symptomatic adolescent men; it should not be used for specimens from women, older men, or asymptomatic men.9,13,14,28 Previous studies have shown that the sensitivity of the LET for chlamydia varied widely from 31% to 100% and specificity ranges from 83% to 100%. Studies showing higher sensitivity were performed with smaller numbers of individuals. Large studies in asymptomatic men have indicated a sensitivity of 57.9% with a specificity of 78.3%13; sensitivity of 58.9%, specificity of 94.9%11; and sensitivity of 45.8%, specificity of 97.4%.14 Positive predictive values (PPVs) ranged from 13.8% to 38.4%. Thus, LET is not recommended as a screening test for C. trachomatis infection in men.3

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Rapid Tests

Although there are a number of rapid antigen tests on the market, none are of sufficient sensitivity to be recommended for screening for chlamydia, especially in asymptomatic men. These “point-of-care tests” were designed to be performed while the patient waits for results. One study reported sensitivities for Testpack, Surecell, and Clearview of 70%, 67.3%, and 67.7%, respectively, for urine from asymptomatic men.29 However, Testpack and Surecell are no longer available, but the Clearview (Unipath, Mountain View, CA) assay is still manufactured. It is FDA-cleared for use with male urethral swabs and female cervical swabs, but not urine; is a moderate complexity test; and is not a waived test for Clinical Laboratory Improvement Act (CLIA)-approved laboratories. Additionally, the QuickVue Chlamydia Test (Quidel Corp., San Diego, CA) is another rapid test that is marketed, but it is only intended for women (endocervical swabs or cytobrushes). The Chlamydia Optical Immunoassay (Thermo Scientific, Waltham, MA, previously called Biostar) is another example of a rapid test and has been shown to be useful, when patients are not likely to return for test results; however, this assay is not approved for men and is only FDA-cleared for use with female endocervical specimens.30 For men, however, the sensitivity for chlamydia was low for urine specimens in clinical trials when compared with NAATs (∼42.7%).31 A modeling study favored the use of a lower sensitivity rapid test if treatment can be given before infected persons infect their partners.32 In general, the rapid tests have very low sensitivities, compared with DNA amplification assays (i.e., 50%–70%) and cannot be used with noninvasive specimen types. Most rapid kit evaluations that received FDA clearance were compared with culture, which being approximately 65% to 85% sensitive, made the package insert report artificially higher sensitivity than if they were compared with NAATs.33

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Nucleic Acid Amplification Tests

C. trachomatis was the one of the first difficult-to-culture pathogens for which there was a research PCR34 and the first in which a commercial PCR assay was available.4,35 There are many published studies using several different types of NAATs; commercially available technologies that can detect chlamydia, as well as Neisseria gonorrhoeae.7,8,10,36–38 NAATs were the first tests sensitive enough to be used with urine samples and have included PCR, (Amplicor, Roche Molecular Diagnostics, Branchburg, NJ); ligase chain reaction (LCx Uriprobe, Abbott Laboratories, Abbott Park, IL); transcription-mediated amplification {TMA; AMPTIMA Combo2 and [AMPLIFIED-C. trachomatis (AMP-CT)] GenProbe}; and strand displacement amplification (SDA; ProbeTec ET, Becton Dickinson, Sparks, MD). Ligase chain reaction assays were removed from the market in 2002, but many validations and epidemiologic studies have been previously performed using male urine, attesting to the high sensitivity and specificity of NAATs in general.38,39 All of these amplification methods offer high sensitivities of detection, usually well above 90% to 92%, while maintaining very high specificity.38,40 NAATs have yet to be FDA-cleared for the detection of infections in the rectum and oropharynx.

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Polymerase Chain Reaction

This assay can be used as a manual microwell format or as an automated method (COBAS). The sensitivity was 88.6% for male urethral swabs, and 90.3% for male urines in the clinical trial for chlamydia7 (Table 1). Another study of only men reported a sensitivity of 92.8% and a specificity of 94.7% for male urine compared with culture, but after DFA analysis of culture-negative samples that were PCR-positive, the sensitivity could be considered to be 95% and the specificity to be 99.1%.4

Table 1
Table 1
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Strand Displacement Amplification

The clinical trial demonstrated sensitivity for chlamydia of 94.6% for male urethral swabs, and 94.5% for male urine8 (Table 1). Compared with cell culture and an expanded gold standard of 2 positive nonculture tests,41 a recent clinical trial using M-5 (Remel, Inc., Lenexa, KS) as a transport medium demonstrated a sensitivity of 100% for male urethral swabs.18

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Transcription-Mediated Hybridization

The originally produced Genprobe AMPLIFIED CT (AMP-CT) assay42,43 is no longer produced and has been replaced by the APTIMA Combo2 assay, which has added target capture technology, and also simultaneously detects N. gonorhoeae.44 The sensitivity ranges from 95% to 97% (Table 1). The somewhat lower specificities presented in the clinical trial may be artificially low, because this assay seems to be slightly more sensitive than other NAATs and confirmation of uniquely positive samples by another NAAT can be problematic. Unique positives can often be confirmed by another primer set using the same assay.38,40 A recently FDA-cleared APTIMA C. trachomatis assay is a “stand alone” chlamydia assay that demonstrated excellent sensitivity for male urethra and urine samples.10 Using 2 comparator tests as a gold standard,41 the sensitivity for urethral swabs was 97% and the specificity was 96% and for urine samples 96% and 98%, respectively10 (Table 1).

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Patient Symptom Status

When men are symptomatic and are attending a clinic, they should receive a complete urogenital examination, with either urethral or urine samples obtained for diagnostic testing using the most sensitive and specific test available, i.e., a NAAT test, which has been recommended by the CDC as the test of choice.45 When populations of asymptomatic men, who are nonhealthcare-seeking, are being screened, the use of noninvasive samples, such as urine, is recommended.3 Such samples eliminate the requirement for a clinician for sample collection and their use can be cost-effective, especially when surveying large numbers of persons.46–54 When these noninvasive samples are used to screen asymptomatic persons for chlamydia, only a NAAT test can be used because none of the other older tests have high-enough sensitivity.

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Is it Necessary to Confirm Positive NAATs in Screening Populations of Low Prevalence?

The prevalence of C. trachomatis infections in certain male populations may be considerable less than that observed in women. In such situations, the accuracy of a screening test may be questioned because the PPV is adversely affected when tests with specificities less than 100% are used in populations with low prevalent disease.55 Given the potential impact of false-positive test results, the CDC-recommended routine additional testing of positive specimens be performed when the prevalence is low and resulting PPV is <90%.45 Preferably, an additional test would be sufficiently dissimilar from the original test so as not to simply reproduce the error. The application of routine additional testing was thought to improve the PPV. However, recent data suggest that such approaches may not be entirely valid and recommend that CDC revisit such guidance.56

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Use of NAAT Assays Has the Ability to Influence the Epidemiology of Chlamydia in Male Population Groups

The number of infections detected by NAAT may be up to 80% higher than those found with the use of older tests.15,27 NAATs are quite accurate in screening asymptomatic men, even though the burden of bacterial load may be low.46,47,52 A national household survey sample demonstrated a prevalence of 2.8%.53 A large screening program in 4 cities in the United States demonstrated a chlamydia prevalence of 7% in mostly asymptomatic men.2 High prevalence (4%–5%) of chlamydia infections in male military recruits has been demonstrated.47,54 Recent surveys of young adults and adolescents in the Adolescent Health Study originally enrolled in schools using NAAT technology also indicated substantial prevalence of chlamydia in men aged 18 to 26 years (overall, 3.67%; white men, 1.38%; black men, 11.12%).46 A large citywide school survey has indicated prevalence for men of 2.5%.57 Screening in nontraditional settings such as the National Job Training Program for men has indicated that the overall chlamydia prevalence was 8.2%.58 Detention centers, jails, urban shelters, community cohorts of injection drug users, and emergency departments have also been screened for chlamydia in men with prevalences as high as 14.3% to 15% and encouraging results for a high proportion of infected men receiving treatment.57–63 Urine-based screening for chlamydia is also acceptable to men in screening settings.47,64,65 Without NAAT testing of urine from men, these studies would not have been able to be performed. Increasing public health interest in screening men is an important prevention message to reduce reservoirs of infection available for transmission to women.

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Laboratory-Based Methods to Decrease Costs of NAAT Assays

NAATs assays are more expensive than older nonculture, nonamplified tests and are often too expensive for many public health programs. Although most cost-effectiveness studies have been performed for screening women,66–69 male cost-effectiveness studies have indicated that they are cost-effective for preventing sequelae in women.48,49 The extremely high cost of NAATS relative to other FDA-cleared technologies and competing responsibilities created difficulty in the public health sector in implementing NAAT screening. Early attempts at cost-effectiveness alternatives has allowed laboratories outside of the United States to implement cost-saving strategies.70 These strategies combined lower-sensitivity tests (EIA) with NAATs reflux testing of remnant specimens in the gray-zone to increase sensitivity of the lower-sensitivity test. These strategies are not FDA-approved and would require a verification study sufficient to satisfy CLIA before the results could be used to guide patient management.

There are pooling methods that have been explored to lower the cost per sample tested in which several prepared patients samples are mixed together and tested in one test unit of a NAAT.71–76 Pooling techniques are highly sensitive and specific for chlamydia detection.71–76 These techniques are not FDA-cleared, however, and any NAAT pooling methodology requires verification studies by CLIA-approved laboratories before use. If the test unit assay containing all the pooled samples is negative, all samples are considered to be negative. Positive pool results require retesting all samples in the pool individually to determine which one (s) is positive. Because most specimens in testing situations are negative, the technique can ultimately save significant costs. Formulas exist to calculate the number of samples to pool to achieve the greatest cost savings for a particular prevalence.72 Pooling algorithms are recommended for screening male urine samples, especially where the prevalence is not expected to be high.3

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Other Laboratory Considerations

NAATS measure DNA or RNA rather than live organisms; therefore, care should be used in using amplification tests for test-of-cure assays. Residual nucleic acid from cells rendered noninfectious by antibiotic therapy may give a “positive” amplified test for up to 3 weeks after therapy, when the patient is actually cured of viable organisms.77,78 Ordinarily, the CDC does not recommend a test-of-cure test for either men or women.23

There are also potential difficulties unique to processing urine samples for preparation for NAAT testing, especially if the package insert directions are not closely followed. Centrifugation is required for all NAAT assays except for APTIMA Combo2. There is the potential for too much urine to be left on the pellet that could potentially interfere with the test result. There also is the potential for the pellet to be lost in the processing, resulting in a false-negative test (Dr. Julius Schachter, personal communication). Care must be taken when urine samples from men are processed for NAAT testing for chlamydia, especially male urine is less cellular in general than female urine. Additionally, inhibition of amplification in urine samples have been reported for some older NAAT assays, and the use of inhibition controls are recommended for these assays.79

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Future Approaches to Screen Men

There is considerable interest in the use of the Internet to reach target populations and the potential for home-based specimen collection as a means to facilitate screening.80,81 These novel approaches may be an important adjunct to current control methods. Individuals who consider themselves at risk for infection and would otherwise not seek medical attention for an asymptomatic infection may perform home specimen collection and mail the specimen directly to the laboratory. It was thought that urine would be the most suitable specimen for male home collection but country-specific postal regulations require strict packaging of liquids intended for diagnostic medical services. A recent study on male self-collected penile/meatal dry swabs yielded comparable results to clinician-collected swabs and FVU when tested for C. trachomatis.82. Results for this type of specimen collection have varied and are not all favorable.83,84 Although additional studies on the use and performance of male self-collected penile/meatal swabs are required, they may someday be an important specimen type for screening men for C. trachomatis as using self-obtained vaginal samples in women for chlamydia screening.85

In summary, NAAT assays are the test of choice for testing men for Chlamydia, and urine is the specimen of choice. For those programs interested in testing men in various high-prevalence venues, guidance is available from the CDC.3 Future research is needed to definitively make official recommendations for screening men.

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