Correct samples for diagnostic tests in sexually transmitted diseases: which sample for which test? 1
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1 FEMS Immunology and Medical Microbiology 24 (1999) 455^459 Correct samples for diagnostic tests in sexually transmitted diseases: which sample for which test? 1 Angelika Stary * Outpatient's Center for Infectious Venero-dermatological Diseases and Fungal Infections, Franz Jonas-Platz 8/3/2/, A-1210 Vienna, Austria Received 16 June 1998; revised 3 March 1999; accepted 3 March 1999 Abstract Amplified DNA technology such as the polymerase chain reaction (PCR) and ligase chain reaction (LCR) are new techniques for the diagnosis of genital chlamydial infections in both men and women. These tests are highly sensitive and specific in detecting chlamydial genes in different specimen types such as genital samples as well as in non-invasive specimens such as urine and vulval smears. Due to the advantage of a high reliability of these techniques even when they are performed on non-invasive specimen types, amplification tests allow chlamydial diagnosis for screening especially high risk persons as the basis of chlamydia control programs. ß 1999 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved. 1. Introduction Genital pathogens primarily a ect the lower genital tract in men and women. The diagnosis of genital infections is mostly based on the detection of the microorganism itself, its antigens or genetic material (DNA, RNA) collected from the entrance of the lower genital tract (endocervix, vaginal epithelium or uid, and mucous membrane of the urethra) and for few infections on the detection of antibodies. The diagnosis of genital infections requires sensitive, speci c, widely available, inexpensive, and rapid tests that can be used for the diagnosis of sexually * Tel.: +43 (1) ; Fax: +43 (1) From the conference ``Recent Advances in the Diagnosis of Sexually Transmitted Diseases'', Istanbul, Turkey, June 10^ 13, transmitted diseases (STDs) in symptomatic and asymptomatic persons as well as for routine STD screening in core groups at high risk. The performance of assays for STD diagnosis depends on many di erent factors such as specimen collection, maintenance of cold chains and rapid transport to the laboratory, and optimal performance of the test itself. Isolation of pathogens by culture methods needs appropriate collection of cell scrapings, optimal transport and storage conditions for the specimens to preserve viable organisms. Culture usually has not a sensitivity of 100%, which means that not all infected individuals are detected. In contrast, molecular diagnostic methods using the arti cial ampli cation of DNA or RNA detect even a few microorganisms with a higher sensitivity than di erent culture techniques and increase the detection rate of truly infected persons. In addition to sensitivity, the speci city of assays for the diagnosis / 99 / $20.00 ß 1999 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved. PII: S (99)
2 456 A. Stary / FEMS Immunology and Medical Microbiology 24 (1999) 455^459 of sexually transmitted infections is of importance, showing the ability to avoid false-positive results and to identify persons who are not infected. Especially in low prevalence settings, the speci city of the diagnostic test has a major impact on the predictive value of a positive result [1]. In this paper new advances in the diagnosis of Chlamydia trachomatis and Neisseria gonorrhoeae, the most important bacterial genital pathogens in the industrialized world, will be discussed. 2. Diagnosis of C. trachomatis Chlamydias are considered the most common bacteria causing genital infections in the industrialized world and may lead to serious conditions such as pelvic in ammatory disease (PID) with consequences including infertility, ectopic pregnancy, and chronic pelvic pain. Screening of women at risk for STD can reduce half of the cases of PID [2]. For the diagnosis of C. trachomatis by culture only specimens from the site of infection are recommended for diagnosis. The adequacy of cells from the columnar region of cervical specimens not only a ects signi cantly the positivity rates of chlamydia diagnosis by culture, but also by the Chlamydiazyme assay as well as by the commercial PCR assay (Roche Molecular Systems) and mostly the direct uorescent antibody assay (DFA). Variations in specimen quality and the sensitivity of the diagnostic assay have a signi cant impact on determining the prevalence in a population [3]. Adequacy rates of cervical specimens reported from about 50 to 64% indicate the necessity of training and periodic retraining of clinicians obtaining cervical samples for chlamydia testing. A new advance in chlamydia diagnosis are methods using the arti cial ampli cation of nucleic acid or signals after hybridization. Ampli cation techniques such as the ligase chain reaction (LCR) and the polymerase chain reaction (PCR) have improved the sensitivity of diagnostic tests for the detection of a genital chlamydial infection. While the PCR uses primers, nucleotides and the enzyme Taq polymerase, the LCR is based on the ligation of oligonucleotide probes which serve as a copy of the original target sequence and are immediately adjacent to each other. In contrast to DNA ampli cation, assays have been developed using the arti cial ampli cation of ribosomal RNA. The QL replicase ampli cation captures the 16S rrna gene followed by QL replicase ampli cation. In a similar way, the transcription-mediated ampli cation assay (TMA) ampli es rrna sequences and replaces the DNA/RNA hybridization test PACE 2 for the diagnosis of C. trachomatis. The TMA uses two primers and two enzymes, reverse transcriptase, which creates a DNA copy of the target rrna, and a second enzyme, RNA polymerase, which recognizes the promoter sequence in the DNA template and initiates transcription. TMA is an isothermal process and does not require a thermocycler for the ampli cation step. Recent studies have demonstrated that nucleic acid ampli cation by LCR and PCR represents a highly sensitive and speci c approach for the detection of C. trachomatis in genital specimens of men and women, when compared to cell culture [4,5]. Beside PCR and LCR rst data of comparison studies with TMA show a high sensitivity for genital and urine swabs in both men and women [6]. Transport and storage conditions are less critical when compared with culture and transport media are usually provided by the manufacturer. While for the diagnosis of genital chlamydial infections by cell culture only samples from the site of infection with a su cient number of elementary bodies (EBs) are recommended, it has been shown that amplifying assays are highly e ective in identifying genital chlamydial infections in men and in women not only by testing invasive samples but also urine as a non-invasive specimen. Automated LCR and PCR assays on rst-void urine (FVU) of women detected up to 30% more chlamydia-infected women than did endocervical swab culture [4,5]. Urine testing by amplifying methods is also recommended for women, and the sensitivity of FVU is similar to that of cervical samples [8,9]. However, there seem to be di erences between male and female urine, with a better performance pattern for male than for female urine. A lower sensitivity has been observed for the performance of the TMA, as well as for other amplifying methods [6,10]. This may be due to a larger amount of inhibitory substances and a lower load of organisms. Since most of the organisms contaminating urine are no longer viable, urine as a non-invasive
3 A. Stary / FEMS Immunology and Medical Microbiology 24 (1999) 455^ sample is not an appropriate specimen for chlamydial diagnosis by cell culture, which gives a sensitivity of only about 30% [11]. Antigen testing of the urine sediment has been performed with di erent enzyme immunoassays (EIAs), but especially in asymptomatic persons with a low number of EBs the sensitivity has been shown to be rather poor [12,13]. The use of non-invasive specimens for the diagnosis of chlamydial infections has a major impact on the e ectiveness of control programs for both males and females [13,14]. Pooling of urine samples resulted in a sensitive, speci c, and cost-saving procedure of chlamydia testing by LCR when compared to individual sample testing and may therefore be a further advantage of urine samples [15]. Recently, it was demonstrated that vulval smears may also serve as suitable non-invasive specimens in women [16]. Compared with urine, the processing of vulval samples for the laboratory is uncomplicated and does not appear to be in uenced by inhibition problems or by a low load of EBs. Similar to urine, vulval swabs cannot be recommended for culture tests due to the low number of viable organisms, resulting in a sensitivity of up to 30%, nor for EIAs, due to the low number of EBs, resulting in a sensitivity of 40.7%. There are also data available using vaginal swabs as semi-invasive samples instead of cervical specimens, which also gave a high sensitivity of 91.8% [17]. Vulval or vaginal sampling may even be performed by the women themselves. So far, the results of the most recent studies indicate that di erent non-invasive specimen types are suitable samples for the highly sensitive amplifying assays LCR, PCR, and TMA and may be used especially for chlamydia testing for screening of asymptomatic population groups. 3. Diagnosis of N. gonorrhoeae The presumptive diagnosis of N. gonorrhoeae is based on the presence of typical intracellular Gram-negative diplococci with a sensitivity ranging between 40 and 98%, depending on the symptomatic status of the disease in men and women. Culture for gonococci is still regarded as the `gold standard' requiring the presence of viable bacteria, exact specimen collection and transport conditions, and a suitable culture medium. Diagnosis of N. gonorrhoeae by an oligonucleotide directed against rrna speci c for gonococci had a sensitivity and speci city of up to 100% when compared with culture technique [18]. In a study performed with a total of 502 men and women all infected individuals were detected by the Gen- Probe PACE 2 system, showing that the DNA probe assay was useful for gonococcal diagnosis in case of unreliable culture conditions [19]. However, there were some borderline results which had to be con- rmed by a commercially available probe competition assay to avoid false-positive results, especially in women. Similar to chlamydia, it has recently been reported that nucleic acid ampli cation methods such as PCR or LCR can detect N. gonorrhoeae in urogenital samples with high sensitivity and speci city when compared to culture, the current diagnostic gold standard [20^22]. As for C. trachomatis, LCR was e ective in identifying N. gonorrhoeae in FVU of infected women, and thus provides a practical alternative to culture for screening high risk populations [7,23]. Both multiplex PCR and LCR are highly sensitive for the detection of both C. trachomatis and N. gonorrhoeae from a single urine or genital swab, providing a more cost-e ective way of screening multiple pathogens [24,25]. The LCR assay is also highly e ective for the detection of N. gonorrhoeae in extragenital specimens of men and women [26]. The performance of LCR and culture for the detection of N. gonorrhoeae in 325 individuals (200 men and 125 women) in genital samples was compared to LCR testing in FVU and anorectal and pharyngeal samples were tested in a sub-population of 47 males and 22 females to examine whether extragenital gonorrhea can be detected by LCR. The performance of LCR applied to FVU was nearly as sensitive as LCR applied to urethral swabs (98% vs. 100%), suggesting that this non-invasive sample type can reliably be used. The bene t of improved sensitivity provided by LCR was more convincing in women where the best overall performance was provided by LCR in FVU samples. This fact may support the concept that N. gonorrhoeae infection is urogenital and not restricted to the endocervix. Although neither culture nor LCR provided a perfect diagnostic tool, the overall perform-
4 458 A. Stary / FEMS Immunology and Medical Microbiology 24 (1999) 455^459 ance of LCR in female FVU was the most e cient single test for the diagnosis of urogenital gonorrhea infection in women. It further indicates that even using a sensitive technique such as LCR which is able to detect a low organism load, the overall detection rate in women is nevertheless lower compared to men due to the complexity of multiple sites of infection and the occurrence of single infection at only one given site. The frequency of anorectal gonococcal infection was reported to range between 5 and 50% [27,28]. It can originate from receptive anal sexual practices in both sexes or from urogenital contamination in women. Our results suggest a relatively high frequency of anorectal infection in both men (13%) and women (45%) of this selected population, although the high positivity rate in women may be partly due to contamination. The 13^18% frequency of pharyngeal infection is similar to previous reports using culture or DNA probes for diagnosis [29,30]. At this location, LCR appeared to be a considerably more sensitive method than culture. In summary, the non-invasive nature of FVU and vulval specimens provides a signi cant advantage over the more labor-intensive and lengthy collection methods of urogenital swabs. Nevertheless, it is important to point out that the performance by LCR or PCR using FVU can be further improved if endogenous inhibitors present in urine which interferes with ampli ed nucleic acid technologies can be overcome. References [1] Schachter, J. and Chow, J.M. (1995) The fallibility of diagnostic tests for sexually transmitted diseases: the impact on behavioral and epidemiologic studies. Sex. Transm. Dis. 22, 191^196. [2] Scholes, D., Stergachis, A., Heidrich, F.E., Andrilla, H., Holmes, K.K. and Stamm, W.E. (1996) Prevention of pelvic in ammatory disease by screening for cervical chlamydial infection. New Engl. J. Med. 344, 1362^1366. [3] Welsh, L.E. et al. (1997) In uence of endocervical specimen adequacy on PCR and direct uorescent-antibody staining for detection of Chlamydia trachomatis infection. J. Clin. Microbiol. 35, 3078^3081. [4] Schachter, J., Stamm, W.E., Quinn, T.C., Andrews, W.W., Burczak, J.D. and Lee, H.H. (1994) Ligase chain reaction to detect Chlamydia trachomatis infection of the cervix. J. Clin. Microbiol. 32, 2540^2543. [5] Bass, C.A., Jungkind, D.L., Silverman, N.S. and Bondi, J.M. (1993) Clinical evaluation of a new polymerase chain reaction assay for detection of Chlamydia trachomatis in endocervical specimens. J. Clin. Microbiol. 31, (Suppl. 1) s2648^s2653. [6] Stary, A., Schuh, E., Kerschbaumer, M., Go«tz, B. and Lee, H. (1999) Performance of transcription mediated ampli cation and ligase chain reaction for detection of chlamydial infection in invasive and noninvasive urogenital samples. J. Clin. Microbiol. (submitted). [7] Lee, H.H., Chernesky, M.A. and Schachter, J. et al. (1995) Diagnosis of Chlamydia trachomatis genitourinary infection in women by ligase chain reaction assay of urine. Lancet 345, 213^216. [8] Chernesky, M.A., Jang, D. and Lee, H.H. et al. (1994) Diagnosis of Chlamydia trachomatis infections in men and women by testing rst-void urine by ligase chain reaction. J. Clin. Microbiol. 32, 2682^2685. [9] Quinn, T.C., Welsh, L., Lentz, A., Crotchfelt, K., Zenilman, J., Newhall, J. and Gaydos, Ch. (1996) Diagnosis by Amplicor PCR of Chlamydia trachomatis infection in urine samples from women and men attending sexually transmitted disease clinics. J. Clin. Microbiol. 34, 1401^1406. [10] Jensen, B., Thorson, P. and Moeller, B.R. (1997) Sensitivity of ligase chain reaction assay of urine from pregnant women for Chlamydia trachomatis. Lancet 349, 329^330. [11] Smith, T.F. and Weed, L.A. (1975) Comparison of urethral swabs, urine, and urinary sediment for the isolation of Chlamydia. J. Clin. Microbiol. 2, 134^135. [12] Taylor-Robinson, D. (1996) Tests for infection with Chlamydia trachomatis. Int. J. STD Aids 7, 19^26. [13] Stary, A., Tomazic-Allen, S., Choueiri, J., Burczak, J., Steyrer, K. and Lee, H. (1996) Comparison of DNA ampli cation methods for the detection of Chlamydia trachomatis in rst-void urine from asymptomatic military recruits. Sex. Transm. Dis. 23, 97^102. [14] Gaydos, C.A., Crotchfelt, K.A., Howell, M.R., Kralian, S., Hauptman, P. and Quinn, T.C. (1998) Molecular ampli cation assays to detect chlamydia infections in urine specimens from high school female students and to monitor the persistence of chlamydial DNA after therapy. J. Infect. Dis. 177, 417^424. [15] Kacena, K.A., Quinn, S.B., Howell, M.R., Madico, G.E., Quinn, T.C. and Gaydos, C.A. (1998) Pooling urine samples for ligase chain reaction screening for genital Chlamydia trachomatis infection in asymptomatic women. J. Clin. Microbiol. 36, (Suppl. 1) S481^S485. [16] Stary, A., Najim, B. and Lee, H.H. (1997) Vulval swabs as alternative specimens for ligase chain reaction detection of genital chlamydial infections in women. J. Clin. Microbiol. 35, 836^838. [17] Hook III, E.W., Smith, K., Mullen, C., Stephens, J., Rinehardt, L., Pate, M.S. and Lee, H.H. (1997) Diagnosis of genitourinary Chlamydia trachomatis infections by using the ligase chain reaction on patient-obtained vaginal swabs. J. Clin. Microbiol. 35, 2133^2135.
5 A. Stary / FEMS Immunology and Medical Microbiology 24 (1999) 455^ [18] Limberger, R.J., Biega, R., Evancoe, A., McCarthy, L., Slivienski, L. and Kirkwood, M. (1992) Evaluation of culture and the Gen-Probe PACE 2 assay for detection of Neisseria gonorrhoeae and Chlamydia trachomatis in endocervical specimens transported to a state health laboratory. J. Clin. Microbiol. 30, 110^116. [19] Stary, A., Kopp, W., Zahel, B., Nerad, S., Teodorowicz, L. and Ho«rting-Mu«ller, I. (1992) Comparison of DNA-Probe test and culture for the detection of Neisseria gonorrhoeae in genital samples. Sex. Transm. Dis. 20, 243^247. [20] Ching, S., Lee, H., Hook III, E.W. and Jacobs, M.R. (1995) Ligase chain reaction for detection of Neisseria gonorrhoeae in urogenital swabs. J. Clin. Microbiol. 33, 3111^3114. [21] Birkenmeyer, L. and Armstrong, A.S. (1992) Preliminary evaluation of the ligase chain reaction for speci c detection of Neisseria gonorroheae. J. Clin. Microbiol. 30, 3089^3094. [22] Ho, B.S.W., Feng, W.G., Wong, B.K.C. and Eggleston, S.I. (1992) Polymerase chain reaction for the detection of Neisseria gonorrhoeae in clinical samples. J. Clin. Pathol. 45, 439^442. [23] Smith, K.R., Ching, S.F., Lee, H., Ohhashi, Y., Hu, H.Y., Fisher III, H.C. and Hook III, E.W. (1995) Evaluation of ligase chain reaction for use with urine for identi cation of Neisseria gonorrhoeae in females attending a sexually transmitted disease clinic. J. Clin. Microbiol. 33, 455^457. [24] Crotchfelt, K.A., Welsh, L.A., DeBonville, D., Rosenstraus, M. and Quinn, T.C. (1997) Detection of Neisseria gonorrhoeae and Chlamydia trachomatis in genitourinary specimens from men and women by a coampli cation assay. J. Clin. Microbiol. 35, 1536^1540. [25] Carroll, K.C., Aldeen, W.E., Morrison, M., Anderson, R., Lee, D. and Mottice, S. (1998) 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. 36, 1630^1633. [26] Stary, A., Ching, S.F., Teodorowicz, L. and Lee, H. (1997) Comparison of ligase chain reaction and culture for detection of Neisseria gonorrhoeae in genital and extragenital specimens. J. Clin. Microbiol. 35, 239^242. [27] Thin, R.N. and Shaw, E.J. (1979) Diagnosis of gonorrhea in women. Br. J. Vener. Dis. 55, 10. [28] Hook, III, E.W. and Hands eld, H.H. (1990) Gonococcal infections in the adult. In: Sexually Transmitted Diseases (Holmes, K., Mardh, P.A., Sparling, P. and Wiesner, P., Eds.), pp. 149^165. McGraw-Hill, New York. [29] Tice, A.W. and Rodriguez, V.L. (1981) Pharyngeal gonorrhea. J. Am. Med. Assoc. 246, [30] Lewis, J.S., Fakile, O., Foss, E., Legarza, G., Leskys, A., Lowe, K. and Powning, D. (1993) Direct DNA probe assay for Neisseria gonorrhoeae in pharyngeal and rectal specimens. J. Clin. Microbiol. 31, 2783^2785.
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