650
Views
14
CrossRef citations to date
0
Altmetric
Review

Review of Chlamydia trachomatis viability methods: assessing the clinical diagnostic impact of NAAT positive results

, , , &
Pages 739-747 | Received 22 Mar 2018, Accepted 06 Jul 2018, Published online: 19 Jul 2018

References

  • Newman L, Rowley J, Vander Hoorn S, et al. Global estimates of the prevalence and incidence of four curable sexually transmitted infections in 2012 based on systematic review and global reporting. PloS One. 2015;10(12):e0143304. PubMed PMID: 26646541; PubMed Central PMCID: PMC4672879.
  • Elwell C, Mirrashidi K, Engel J. Chlamydia cell biology and pathogenesis. Nat Rev Microbiol. 2016 Jun;14(6):385–400. PubMed PMID: 27108705; PubMed Central PMCID: PMC4886739.
  • Bennett J, Dolin R, Blaser M. Mandell, Douglas, and Bennett’s principles and practice of infectious diseases. 8th ed. Philadelphia (PA): Elsevier Saunders; 2015.
  • Wyrick PB. Chlamydia trachomatis persistence in vitro: an overview. J Infect Dis. 2010 Jun 15;201 Suppl 2:S88–S95. PubMed PMID: 20470046; PubMed Central PMCID: PMC2878585.
  • Gaydos CA, Quinn TC, Willis D, et al. Performance of the APTIMA combo 2 assay for detection of Chlamydia trachomatis and Neisseria gonorrhoeae in female urine and endocervical swab specimens. J Clin Microbiol. 2003 Jan;41(1):304–309. PubMed PMID: 12517865; PubMed Central PMCID: PMC149571.
  • Gaydos CA, Theodore M, Dalesio N, et al. Comparison of three nucleic acid amplification tests for detection of Chlamydia trachomatis in urine specimens. J Clin Microbiol. 2004 Jul;42(7):3041–3045. PubMed PMID: 15243057; PubMed Central PMCID: PMC446239.
  • 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 Mar;39(3):1008–1016. PubMed PMID: 11230419; PubMed Central PMCID: PMC87865.
  • Van Der Pol B, Quinn TC, Gaydos CA, et al. Multicenter evaluation of the AMPLICOR and automated COBAS AMPLICOR CT/NG tests for detection of Chlamydia trachomatis. J Clin Microbiol. 2000 Mar;38(3):1105–1112. PubMed PMID: 10699004; PubMed Central PMCID: PMC86350.
  • Hoebe CJ, Rademaker CW, Brouwers EE, et al. Acceptability of self-taken vaginal swabs and first-catch urine samples for the diagnosis of urogenital Chlamydia trachomatis and Neisseria gonorrhoeae with an amplified DNA assay in young women attending a public health sexually transmitted disease clinic. Sex Transm Dis. 2006 Aug;33(8):491–495. PubMed PMID: 16547452.
  • Moncada J, Schachter J, Liska S. Evaluation of self-collected glans and rectal swabs from men who have sex with men for detection of Chlamydia trachomatis and Neisseria gonorrhoeae by use of nucleic acid amplification tests. J Clin Microbiol. 2009 Jun;47(6):1657–1662. PubMed PMID: 19369445; PubMed Central PMCID: PMC2691064.
  • van der Helm JJ, Hoebe CJ, van Rooijen MS, et al. High performance and acceptability of self-collected rectal swabs for diagnosis of Chlamydia trachomatis and Neisseria gonorrhoeae in men who have sex with men and women. Sex Transm Dis. 2009 Aug;36(8):493–497. PubMed PMID: 19617869.
  • van Dommelen L, Dukers-Muijrers N, van Tiel FH, et al. Evaluation of one-sample testing of self-obtained vaginal swabs and first catch urine samples separately and in combination for the detection of Chlamydia trachomatis by two amplified DNA assays in women visiting a sexually transmitted disease clinic. Sex Transm Dis. 2011 Jun;38(6):533–535. PubMed PMID: 21217415.
  • Bogosian G, Bourneuf EV. A matter of bacterial life and death. EMBO Rep. 2001 Sep;2(9):770–774. PubMed PMID: 11559589; PubMed Central PMCID: PMC1084037.
  • Dukers-Muijrers NH, Morré SA, Speksnijder A, et al. Chlamydia trachomatis test-of-cure cannot be based on a single highly sensitive laboratory test taken at least 3 weeks after treatment. PloS One. 2012;7(3):e34108. PubMed PMID: 22470526; PubMed Central PMCID: PMC3314698.
  • Dukers-Muijrers NH, Speksnijder AG, Morré SA, et al. Detection of anorectal and cervicovaginal Chlamydia trachomatis infections following azithromycin treatment: prospective cohort study with multiple time-sequential measures of rRNA, DNA, quantitative load and symptoms. PloS One. 2013;8(11):e81236. PubMed PMID: 24278400; PubMed Central PMCID: PMC3835673.
  • Renault CA, Israelski DM, Levy V, et al. Time to clearance of Chlamydia trachomatis ribosomal RNA in women treated for chlamydial infection. Sex Health. 2011 Mar;8(1):69–73. PubMed PMID: 21371385.
  • Versteeg B, Bruisten SM, Heijman T, et al. Monitoring therapy success of urogenital Chlamydia trachomatis infections in women: a prospective observational cohort study. PloS One. 2017;12(9):e0185295. PubMed PMID: 28934342; PubMed Central PMCID: PMC5608402.
  • Lanjouw E, Ouburg S, de Vries HJ, et al. 2015 European guideline on the management of Chlamydia trachomatis infections. Int J STD AIDS. 2016 Apr;27(5):333–348. PubMed PMID: 26608577.
  • Nwokolo NC, Dragovic B, Patel S, et al. 2015 UK national guideline for the management of infection with Chlamydia trachomatis. Int J STD AIDS. 2016 Mar;27(4):251–267. PubMed PMID: 26538553.
  • Workowski KA, Bolan GA, Centers for Disease C, et al. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep. 2015 Jun 5;64(RR–03):1–137. PubMed PMID: 26042815.
  • Ding A, Challenor R. Rectal Chlamydia in heterosexual women: more questions than answers. Int J STD AIDS. 2014 Jul;25(8):587–592. PubMed PMID: 24352134.
  • Dukers-Muijrers NH, Schachter J, van Liere GA, et al. What is needed to guide testing for anorectal and pharyngeal Chlamydia trachomatis and Neisseria gonorrhoeae in women and men? Evidence and opinion. BMC Infect Dis. 2015 Nov 17;15:533. PubMed PMID: 26576538; PubMed Central PMCID: PMC4650297.
  • Peters RP, Dubbink JH, van der Eem L, et al. Cross-sectional study of genital, rectal, and pharyngeal Chlamydia and gonorrhea in women in rural South Africa. Sex Transm Dis. 2014 Sep;41(9):564–569. PubMed PMID: 25118973.
  • van Liere GA, Hoebe CJ, Niekamp AM, et al. Standard symptom- and sexual history-based testing misses anorectal Chlamydia trachomatis and Neisseria gonorrhoeae infections in swingers and men who have sex with men. Sex Transm Dis. 2013 Apr;40(4):285–289. PubMed PMID: 23486492.
  • van Liere GA, Hoebe CJ, Wolffs PF, et al. High co-occurrence of anorectal chlamydia with urogenital chlamydia in women visiting an STI clinic revealed by routine universal testing in an observational study; a recommendation towards a better anorectal chlamydia control in women. BMC Infect Dis. 2014 May 19; 14:274. PubMed PMID: 24885306; PubMed Central PMCID: PMC4032161.
  • Dubbink JH, de Waaij DJ, Bos M, et al. Microbiological characteristics of Chlamydia Trachomatis and Neisseria Gonorrhoeae infections in South African women. J Clin Microbiol. 2016 Jan;54(1):200–203. PubMed PMID: 26511740; PubMed Central PMCID: PMC4702750.
  • Dewart CM, Bernstein KT, DeGroote NP, et al. Prevalence of rectal chlamydial and gonococcal infections: a systematic review. Sex Transm Dis. 2017 Nov 1. DOI:10.1097/OLQ.0000000000000754. PubMed PMID: 29465688.
  • Musil K, Currie M, Sherley M, et al. Rectal chlamydia infection in women at high risk of chlamydia attending Canberra Sexual Health Centre. Int J STD AIDS. 2016 Jun;27(7):526–530. PubMed PMID: 25957326.
  • Chandra NL, Broad C, Folkard K, et al. Detection of Chlamydia trachomatis in rectal specimens in women and its association with anal intercourse: a systematic review and meta-analysis. Sex Transm Infect. 2018 Feb 3. DOI:10.1136/sextrans-2017-053161. PubMed PMID: 29431148.
  • van Liere G, Dukers-Muijrers N, Levels L, et al. High proportion of anorectal Chlamydia trachomatis and Neisseria gonorrhoeae after routine universal urogenital and anorectal screening in women visiting the sexually transmitted infection clinic. Clin Infect Dis. 2017 Jun 15;64(12):1705–1710. PubMed PMID: 28369227.
  • Rank RG, Yeruva L. Hidden in plain sight: chlamydial gastrointestinal infection and its relevance to persistence in human genital infection. Infect Immun. 2014 Apr;82(4):1362–1371. PubMed PMID: 24421044; PubMed Central PMCID: PMC3993372.
  • Yeruva L, Spencer N, Bowlin AK, et al. Chlamydial infection of the gastrointestinal tract: a reservoir for persistent infection. Pathog Dis. 2013 Aug;68(3):88–95. PubMed PMID: 23843274; PubMed Central PMCID: PMC3751173.
  • Geisler WM. Duration of untreated, uncomplicated Chlamydia trachomatis genital infection and factors associated with chlamydia resolution: a review of human studies. J Infect Dis. 2010 Jun 15;201 Suppl 2:S104–13. PubMed PMID: 20470048.
  • Morre SA, van den Brule AJ, Rozendaal L, et al. The natural course of asymptomatic Chlamydia trachomatis infections: 45% clearance and no development of clinical PID after one-year follow-up. Int J STD AIDS. 2002 Dec;13 Suppl 2:12–18. PubMed PMID: 12537719.
  • Molano M, Meijer CJ, Weiderpass E, et al. The natural course of Chlamydia trachomatis infection in asymptomatic Colombian women: a 5-year follow-up study. J Infect Dis. 2005 Mar 15;191(6):907–916. PubMed PMID: 15717266; eng.
  • Dirks JA, Van Liere GA, Bogers S, et al. Natural course of Chlamydia trachomatis bacterial load in the time interval between screening and treatment in anogenital samples. PloS One. 2015;10(12):e0145693. PubMed PMID: 26713628; PubMed Central PMCID: PMC4701017.
  • van Rooijen MS, Schim van der Loeff MF, Morré SA, et al. Spontaneous pharyngeal Chlamydia trachomatis RNA clearance. A cross-sectional study followed by a cohort study of untreated STI clinic patients in Amsterdam, The Netherlands. Sex Transm Infect. 2015 May;91(3):157–164. PubMed PMID: 25237127.
  • Vodstrcil LA, McIver R, Huston WM. The epidemiology of Chlamydia trachomatis organism load during genital infection: a systematic review. J Infect Dis. 2015 May 15;211(10):1628–1645. PubMed PMID: 25492913.
  • Gordon FB, Harper IA, Quan AL, et al. Detection of Chlamydia (Bedsonia) in certain infections of man. I. Laboratory procedures: comparison of yolk sac and cell culture for detection and isolation. J Infect Dis. 1969 Oct;120(4):451–462. PubMed PMID: 4186430.
  • Evans RT, Woodland RM. Detection of chlamydiae by isolation and direct examination. Br Med Bull. 1983 Apr;39(2):181–186. PubMed PMID: 6191821.
  • Rota TR, Nichols RL. Chlamydin trachomatis in cell culture. I. Comparison of efficiencies of infection in several chemically defined media, at various pH and temperature values, and after exposure to diethylaminoethyl-dextran. Appl Microbiol. 1973 Oct;26(4):560–565. PubMed PMID: 4751801; PubMed Central PMCID:PMC379848.
  • Benes S, McCormack WM. Comparison of methods for cultivation and isolation of Chlamydia trachomatis. J Clin Microbiol. 1982 Nov;16(5):847–850. PubMed PMID: 6185530; PubMed Central PMCID: PMC272489.
  • Ripa KT, Mardh PA. Cultivation of Chlamydia trachomatis in cycloheximide-treated mccoy cells. J Clin Microbiol. 1977 Oct;6(4):328–331. PubMed PMID: 562356; PubMed Central PMCID: PMC274768.
  • Scidmore MA. Cultivation and laboratory maintenance of Chlamydia trachomatis. Curr Protoc Microbiol. 2005 Jul:Chapter 11:Unit 11A 1. DOI:10.1002/9780471729259.mc11a01s00. PubMed PMID: 18770550.
  • Barnes RC. Laboratory diagnosis of human chlamydial infections. Clin Microbiol Rev. 1989 Apr;2(2):119–136. PubMed PMID: 2650858; PubMed Central PMCID: PMC358106.
  • Thejls H, Gnarpe J, Gnarpe H, et al. Expanded gold standard in the diagnosis of Chlamydia trachomatis in a low prevalence population: diagnostic efficacy of tissue culture, direct immunofluorescence, enzyme immunoassay, PCR and serology. Genitourin Med. 1994 Oct;70(5):300–303. PubMed PMID: 8001937; PubMed Central PMCID: PMC1195269.
  • Meyer T. Diagnostic procedures to detect Chlamydia trachomatis infections. Microorganisms. 2016 Aug 5;4(3). PubMed PMID: 27681919; PubMed Central PMCID: PMC5039585. DOI:10.3390/microorganisms4030025
  • Shao L, Guo Y, Jiang Y, et al. Sensitivity of the standard Chlamydia trachomatis culture method is improved after one additional in vitro passage. J Clin Lab Anal. 2016 Sep;30(5):697–701. PubMed PMID: 26987564.
  • Laalami S, Zig L, Putzer H. Initiation of mRNA decay in bacteria. Cell Mol Life Sci. 2014 May;71(10):1799–1828. PubMed PMID: 24064983; PubMed Central PMCID: PMC3997798.
  • Cenciarini-Borde C, Courtois S, La Scola B. Nucleic acids as viability markers for bacteria detection using molecular tools. Future Microbiol. 2009 Feb;4(1):45–64. 10.2217/17460913.4.1.45. PubMed PMID: 19207099.
  • Keer JT, Birch L. Molecular methods for the assessment of bacterial viability. J Microbiol Methods. 2003 May;53(2):175–183. PubMed PMID: 12654489.
  • VanGuilder HD, Vrana KE, Freeman WM. Twenty-five years of quantitative PCR for gene expression analysis. Biotechniques. 2008 Apr;44(5):619–626. PubMed PMID: 18474036.
  • Ferreira R, Borges V, Borrego MJ, et al. Global survey of mRNA levels and decay rates of Chlamydia trachomatis trachoma and lymphogranuloma venereum biovars. Heliyon. 2017 Jul;3(7):e00364. PubMed PMID: 28795162; PubMed Central PMCID: PMC5541142.
  • Peuchant O, Duvert JP, Clerc M, et al. Effects of antibiotics on Chlamydia trachomatis viability as determined by real-time quantitative PCR. J Med Microbiol. 2011 Apr;60(Pt 4):508–514. PubMed PMID: 21183597.
  • Mpiga P, Ravaoarinoro M. Effects of sustained antibiotic bactericidal treatment on Chlamydia trachomatis-infected epithelial-like cells (HeLa) and monocyte-like cells (THP-1 and U-937). Int J Antimicrob Agents. 2006 Apr;27(4):316–324. PubMed PMID: 16527461.
  • Storm M, Gustafsson I, Herrmann B, et al. Real-time PCR for pharmacodynamic studies of Chlamydia trachomatis. J Microbiol Methods. 2005 Jun;61(3):361–367. PubMed PMID: 15767012.
  • Dreses-Werringloer U, Padubrin I, Jurgens-Saathoff B, et al. Persistence of Chlamydia trachomatis is induced by ciprofloxacin and ofloxacin in vitro. Antimicrob Agents Chemother. 2000 Dec;44(12):3288–3297. PubMed PMID: 11083629; PubMed Central PMCID: PMC90194.
  • Pitt R, Alexander S, Ison C, et al. Phenotypic antimicrobial susceptibility testing of Chlamydia trachomatis isolates from patients with persistent or successfully treated infections. J Antimicrob Chemother. 2017 Nov 30. DOI:10.1093/jac/dkx454. PubMed PMID: 29207004.
  • Lau A, Kong F, Fairley CK, et al., Treatment efficacy of azithromycin 1 g single dose versus doxycycline 100 mg twice daily for 7 days for the treatment of rectal chlamydia among men who have sex with men - a double-blind randomised controlled trial protocol. Bmc Infect Dis. 2017 Jan 6;17(1):35. DOI:10.1186/s12879-016-2125-7. PubMed PMID: 28061753; PubMed Central PMCID: PMC5217553.
  • Shaw EI, Dooley CA, Fischer ER, et al. Three temporal classes of gene expression during the Chlamydia trachomatis developmental cycle. Mol Microbiol. 2000 Aug;37(4):913–925. PubMed PMID: 10972811.
  • Belland RJ, Zhong G, Crane DD, et al. Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc Natl Acad Sci USA. 2003 Jul 8;100(14):8478–8483. PubMed PMID: 12815105; PubMed Central PMCID: PMC166254.
  • Nicholson TL, Olinger L, Chong K, et al. Global stage-specific gene regulation during the developmental cycle of Chlamydia trachomatis. J Bacteriol. 2003 May;185(10):3179–3189. PubMed PMID: 12730178; PubMed Central PMCID: PMC154084.
  • Witkin SS, Minis E, Athanasiou A, et al. Chlamydia trachomatis: the persistent pathogen. Clin Vaccine Immunol. 2017 Oct;24(10). PubMed PMID: 28835360; PubMed Central PMCID: PMC5629669. DOI:10.1128/CVI.00203-17.
  • Hellyer TJ, DesJardin LE, Hehman GL, et al. Quantitative analysis of mRNA as a marker for viability of mycobacterium tuberculosis. J Clin Microbiol. 1999 Aug 13;37(2):290–295. /received 10/21/rev-request 10/28/accepted. PubMed PMID: 9889206; PubMed Central PMCID: PMC84288.
  • Rudi K, Moen B, Dromtorp SM, et al. Use of ethidium monoazide and PCR in combination for quantification of viable and dead cells in complex samples. Appl Environ Microbiol. 2005 Feb;71(2):1018–1024. PubMed PMID: 15691961; PubMed Central PMCID: PMC546808.
  • Nogva HK, Dromtorp SM, Nissen H, et al. Ethidium monoazide for DNA-based differentiation of viable and dead bacteria by 5ʹ-nuclease PCR. Biotechniques. 2003 Apr;34(4):804–8, 810, 812–3. PubMed PMID: 12703305.
  • Nocker A, Cheung CY, Camper AK. Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. J Microbiol Methods. 2006 Nov;67(2):310–320. PubMed PMID: 16753236.
  • Coffman GL, Gaubatz JW, Yielding KL, et al. Demonstration of specific high affinity binding sites in plasmid DNA by photoaffinity labeling with an ethidium analog. J Biol Chem. 1982 Nov 25;257(22):13205–13207. PubMed PMID: 6754713.
  • Rudi K, Naterstad K, Dromtorp SM, et al. Detection of viable and dead Listeria monocytogenes on gouda-like cheeses by real-time PCR. Lett Appl Microbiol. 2005;40(4):301–306. PubMed PMID: 15752222.
  • Wang S, Levin RE. Discrimination of viable Vibrio vulnificus cells from dead cells in real-time PCR. J Microbiol Methods. 2006 Jan;64(1):1–8. PubMed PMID: 15932774.
  • Hein I, Flekna G, Krassnig M, et al. Real-time PCR for the detection of Salmonella spp. in food: an alternative approach to a conventional PCR system suggested by the FOOD-PCR project. J Microbiol Methods. 2006 Sep;66(3):538–547. PubMed PMID: 16564585.
  • Rogers GB, Stressmann FA, Koller G, et al. Assessing the diagnostic importance of nonviable bacterial cells in respiratory infections. Diagn Microbiol Infect Dis. 2008 Oct;62(2):133–141. PubMed PMID: 18692341.
  • Elizaquivel P, Aznar R, Sanchez G. Recent developments in the use of viability dyes and quantitative PCR in the food microbiology field. J Appl Microbiol. 2014 Jan;116(1):1–13. PubMed PMID: 24119073.
  • Moreno L, Aznar R, Sanchez G. Application of viability PCR to discriminate the infectivity of hepatitis A virus in food samples. Int J Food Microbiol. 2015 May 18;201:1–6. PubMed PMID: 25720326.
  • Wang L, Li Y, Mustapha A. Detection of viable Escherichia coli O157: h7by ethidium monoazide real-time PCR. J Appl Microbiol. 2009 Nov;107(5):1719–1728. PubMed PMID: 19457030.
  • Delgado-Viscogliosi P, Solignac L, Delattre JM. Viability PCR, a culture-independent method for rapid and selective quantification of viable Legionella pneumophila cells in environmental water samples. Appl Environ Microbiol. 2009 Jun;75(11):3502–3512. PubMed PMID: 19363080; PubMed Central PMCID: PMC2687295.
  • Inoue H, Fujimura R, Agata K, et al. Molecular characterization of viable Legionella spp. in cooling tower water samples by combined use of ethidium monoazide and PCR. Microbes Environ. 2015;30(1):108–112. PubMed PMID: 25736979; PubMed Central PMCID: PMC4356457.
  • Yanez MA, Nocker A, Soria-Soria E, et al. Quantification of viable Legionella pneumophila cells using propidium monoazide combined with quantitative PCR. J Microbiol Methods. 2011 May;85(2):124–130. PubMed PMID: 21329735.
  • Janssen KJ, Hoebe CJ, Dukers-Muijrers NH, et al. Viability-PCR shows that NAAT detects a high proportion of DNA from non-viable Chlamydia trachomatis. PLoS One. 2016;11(11):e0165920. PubMed PMID: 27812208; PubMed Central PMCID: PMC5094775.
  • Dukers-Muijrers NH, Wolffs PF, Eppings L, et al. Design of the FemCure study: prospective multicentre study on the transmission of genital and extra-genital Chlamydia trachomatis infections in women receiving routine care. BMC Infect Dis. 2016 Aug 8;16:381. PubMed PMID: 27502928; PubMed Central PMCID: PMC4977887.
  • Cangelosi GA, Meschke JS. Dead or alive: molecular assessment of microbial viability. Appl Environ Microbiol. 2014 Oct;80(19):5884–5891. PubMed PMID: 25038100; PubMed Central PMCID: PMC4178667.
  • van den Broek IVF, Land JA, van Bergen JEAM, et al. Chlamydia trachomatis antibody testing in vaginal mucosal material versus blood samples of women attending a fertility clinic and an STI clinic. Obstet Gynecol Int. 2014;2014:1–9. PubMed PMID: 24757446; PubMed Central PMCID: PMC3976833.
  • Yamamoto S, Azuma E, Muramatsu M, et al. Significance of extracellular vesicles: pathobiological roles in disease. Cell Struct Funct. 2016 Nov 25;41(2):137–143. PubMed PMID: 27679938.
  • Yamamoto S, Niida S, Azuma E, et al. Inflammation-induced endothelial cell-derived extracellular vesicles modulate the cellular status of pericytes. Sci Rep. 2015 Feb 17;5:8505. PubMed PMID: 25687367; PubMed Central PMCID: PMC4330530.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.