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Chlamydia trachomatis as the Cause of Infectious Infertility: Acute, Repetitive or Persistent Long-Term Infection?

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Biology of Chlamydia

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 412))

Abstract

Chlamydia trachomatis is the most frequently detected agent of sexually transmitted infections worldwide. Infection of the lower female genital tract (FGT) can cause cervicitis and if ascending to the upper FGT may result in serious sequelae such as pelvic inflammatory disease (PID), salpingitis and tubal factor infertility (TFI). The factors leading to this complication are still not completely understood. We elaborate four different models for host–pathogen interactions in C. trachomatis infections that may promote disease development: (1) acute infection, (2) repeated infections, (3) chronic/persistent infections and (4) non-inflammatory colonization. Whereas experimental data exist for all of these models in vitro, ex vivo and in vivo, we were interested in seeing what clinical evidence we have supporting one or the other model. We particularly focused on data that favour the one or the other model for TFI development in C. trachomatis infection and speculate on future studies that could integrate in vitro findings for a better characterization of the situation in vivo.

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Abbreviations

BV:

Bacterial vaginosis

DFO:

Deferoxamine

EB:

Elementary body

EP:

Ectopic pregnancy

FGT:

Female genital tract

HSP60:

Heat-shock protein 60

IFN-γ:

Interferon-γ

OmpA:

Outer membrane protein A

PID:

Pelvic inflammatory disease

RB:

Reticulate body

TFI:

Tubal factor infertility

References

  • Aghaizu A, Reid F, Kerry S, Hay PE, Mallinson H, Jensen JS, Kerry S, Kerry S, Oakeshott P (2014) Frequency and risk factors for incident and redetected Chlamydia trachomatis infection in sexually active, young, multi-ethnic women: a community based cohort study. Sex Transm Infect. 90(7):524–528

    Article  PubMed  Google Scholar 

  • Al-Younes HM, Rudel T, Meyer TF (1999) Characterization and intracellular trafficking pattern of vacuoles containing Chlamydia pneumoniae in human epithelial cells. Cell Microbiol 1(3):237–247

    Article  CAS  PubMed  Google Scholar 

  • Al-Younes HM, Rudel T, Brinkmann V, Szczepek AJ, Meyer TF (2001) Low iron availability modulates the course of Chlamydia pneumoniae infection. Cell Microbiol 3(6):427–437

    Article  CAS  PubMed  Google Scholar 

  • Bahar-Shany K, Brand H, Sapoznik S, Jacob-Hirsch J, Yung Y, Korach J, Perri T, Cohen Y, Hourvitz A, Levanon K (2014) Exposure of fallopian tube epithelium to follicular fluid mimics carcinogenic changes in precursor lesions of serous papillary carcinoma. Gynecol Oncol 132(2):322–327

    Article  CAS  PubMed  Google Scholar 

  • Bakken IJ, Skjeldestad FE, Nordbø SA (2007) Chlamydia trachomatis infections increase the risk for ectopic pregnancy: a population-based, nested case-control study. Sex Transm Dis 34(3):166–169

    Article  PubMed  Google Scholar 

  • Batteiger BE, Tu W, Ofner S, Van Der Pol B, Stothard DR, Orr DP, Katz BP, Fortenberry JD (2010) Repeated Chlamydia trachomatis genital infections in adolescent women. J Infect Dis 201(1):42–51

    Article  PubMed  Google Scholar 

  • Bavoil PM (2014) What’s in a word: the use, misuse, and abuse of the word “persistence” in Chlamydia biology. Front Cell Infect Microbiol 4:27

    Article  PubMed  PubMed Central  Google Scholar 

  • Beatty WL, Morrison RP, Byrne GI (1994) Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol Rev 58(4):686–699

    PubMed  PubMed Central  CAS  Google Scholar 

  • Belland RJ, Nelson DE, Virok D, Crane DD, Hogan D, Sturdevant D, Beatty WL, Caldwell HD (2003) Transcriptome analysis of chlamydial growth during IFN-gamma-mediated persistence and reactivation. Proc Natl Acad Sci USA. 100(26):15971–15976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bragina EY, Gomberg MA, Dmitriev GA (2001) Electron microscopic evidence of persistent chlamydial infection following treatment. J Eur Acad Dermatol Venereol 15(5):405–409

    Article  CAS  PubMed  Google Scholar 

  • Byrne GI, Lehmann LK, Landry GJ (1986) Induction of tryptophan catabolism is the mechanism for gamma-interferon-mediated inhibition of intracellular Chlamydia psittaci replication in T24 cells. Infect Immun 53(2):347–351

    PubMed  PubMed Central  CAS  Google Scholar 

  • Caldwell HD, Wood H, Crane D et al (2003) Polymorphisms in Chlamydia trachomatis tryptophan synthase genes differentiate between genital and ocular isolates. J Clin Invest. 111(11):1757–1769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carey AJ, Beagley KW (2010) Chlamydia trachomatis, a hidden epidemic: effects on female reproduction and options for treatment. Am J Reprod Immunol 63(6):576–586

    Article  CAS  PubMed  Google Scholar 

  • Carey AJ, Huston WM, Cunningham KA, Hafner LM, Timms P, Beagley KW (2013) Characterization of in vitro Chlamydia muridarum persistence and utilization in an in vivo mouse model of Chlamydia vaccine. Am J Reprod Immunol 69(5):475–485

    Article  CAS  PubMed  Google Scholar 

  • Clark RB, Schatzki PF, Dalton HP (1982) Ultrastructural analysis of the effects of erythromycin on the morphology and developmental cycle of Chlamydia trachomatis HAR-13. Arch Microbiol 133(4):278–282

    Article  CAS  PubMed  Google Scholar 

  • Craig AP, Kong FY, Yeruva L, Hocking JS, Rank RG, Wilson DP, Donovan B (2015) Is it time to switch to doxycycline from azithromycin for treating genital chlamydial infections in women? Modelling the impact of autoinoculation from the gastrointestinal tract to the genital tract. BMC Infect Dis 15:200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Clercq E, Kalmar I, Vanrompay D (2013) Animal models for studying female genital tract infection with Chlamydia trachomatis. Infect Immun 81(9):3060–3067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dean D, Suchland RJ, Stamm WE (2000) Evidence for long-term cervical persistence of Chlamydia trachomatis by omp1 genotyping. J Infect Dis 182(3):909–916

    Article  CAS  PubMed  Google Scholar 

  • Deka S, Vanover J, Dessus-Babus S, Whittimore J, Howett MK, Wyrick PB, Schoborg RV (2006) Chlamydia trachomatis enters a viable but non-cultivable (persistent) state within herpes simplex virus type 2 (HSV-2) co-infected host cells. Cell Microbiol 8(1):149–162

    Article  CAS  PubMed  Google Scholar 

  • Deka S, Vanover J, Sun J, Kintner J, Whittimore J, Schoborg RV (2007) An early event in the herpes simplex virus type-2 replication cycle is sufficient to induce Chlamydia trachomatis persistence. Cell Microbiol 9(3):725–737

    Article  CAS  PubMed  Google Scholar 

  • Dill BD, Dessus-Babus S, Raulston JE (2009) Identification of iron-responsive proteins expressed by Chlamydia trachomatis reticulate bodies during intracellular growth. Microbiology 155(Pt 1):210–219

    Article  CAS  PubMed  Google Scholar 

  • Dreses-Werringloer U, Padubrin I, Jürgens-Saathoff B, Hudson AP, Zeidler H, Köhler L (2000) Persistence of Chlamydia trachomatis is induced by ciprofloxacin and ofloxacin in vitro. Antimicrob Agents Chemother 44(12):3288–3297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frazer LC, O’Connell CM, Andrews CW Jr, Zurenski MA, Darville T (2011) Enhanced neutrophil longevity and recruitment contribute to the severity of oviduct pathology during Chlamydia muridarum infection. Infect Immun 79(10):4029–4041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geisler WM (2015) Diagnosis and management of uncomplicated Chlamydia trachomatis infections in adolescents and adults: summary of evidence reviewed for the 2015 Centers for Disease Control and Prevention Sexually Transmitted Diseases Treatment Guidelines. Clin Infect Dis 61(Suppl 8):S774–S784

    Article  PubMed  Google Scholar 

  • Geisler WM, Lensing SY, Press CG, Hook EW 3rd (2013) Spontaneous resolution of genital Chlamydia trachomatis infection in women and protection from reinfection. J Infect Dis 207(12):1850–1856

    Article  PubMed  PubMed Central  Google Scholar 

  • Geisler WM, Uniyal A, Lee JY, Lensing SY, Johnson S, Perry RC, Kadrnka CM, Kerndt PR (2015) Azithromycin versus doxycycline for urogenital Chlamydia trachomatis infection. N Engl J Med 373(26):2512–2521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gieffers J, Rupp J, Gebert A, Solbach W, Klinger M (2004) First-choice antibiotics at subinhibitory concentrations induce persistence of Chlamydia pneumoniae. Antimicrob Agents Chemother 48(4):1402–1405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golden MR, Whittington WL, Handsfield HH et al (2005) Effect of expedited treatment of sex partners on recurrent or persistent gonorrhea or chlamydial infection. N Engl J Med 352(7):676–685

    Article  CAS  PubMed  Google Scholar 

  • Gratrix J, Singh AE, Bergman J, Egan C, Plitt SS, McGinnis J, Bell CA, Drews SJ, Read R (2015) Evidence for increased Chlamydia case finding after the introduction of rectal screening among women attending 2 Canadian sexually transmitted infection clinics. Clin Infect Dis 60(3):398–404

    Article  PubMed  Google Scholar 

  • Hall JV, Sun J, Slade J, Kintner J, Bambino M, Whittimore J, Schoborg RV (2014) Host nectin-1 is required for efficient Chlamydia trachomatis serovar E development. Front Cell Infect Microbiol. 4:158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harper A, Pogson CI, Jones ML, Pearce JH (2000) Chlamydial development is adversely affected by minor changes in amino acid supply, blood plasma amino acid levels, and glucose deprivation. Infect Immun 68(3):1457–1464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hillis SD, Owens LM, Marchbanks PA, Amsterdam LF, Mac Kenzie WR (1997) Recurrent chlamydial infections increase the risks of hospitalization for ectopic pregnancy and pelvic inflammatory disease. Am J Obstet Gynecol 176(1 Pt 1):103–107

    Article  CAS  PubMed  Google Scholar 

  • Hogan RJ, Mathews SA, Mukhopadhyay S, Summersgill JT, Timms P (2004) Chlamydial persistence: beyond the biphasic paradigm. Infect Immun 72(4):1843–1855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hosenfeld CB, Workowski KA, Berman S, Zaidi A, Dyson J, Mosure D, Bolan G, Bauer HM (2009) Repeat infection with Chlamydia and gonorrhea among females: a systematic review of the literature. Sex Transm Dis 36(8):478–489

    Article  PubMed  Google Scholar 

  • Igietseme JU, Portis JL, Perry LL (2001) Inflammation and clearance of Chlamydia trachomatis in enteric and nonenteric mucosae. Infect Immun 69(3):1832–1840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jerchel S, Knebel G, König P, Bohlmann MK, Rupp J (2012) A human fallopian tube model for investigation of C. trachomatis infections. J Vis Exp 66:4036

    Google Scholar 

  • Johnson FW, Hobson D (1977) The effect of penicillin on genital strains of Chlamydia trachomatis in tissue culture. J Antimicrob Chemother 3(1):49–56

    Article  CAS  PubMed  Google Scholar 

  • Kahane S, Friedman MG (1992) Reversibility of heat shock in Chlamydia trachomatis. FEMS Microbiol Lett 76(1–2):25–30

    Article  CAS  PubMed  Google Scholar 

  • Kavanagh K, Wallace LA, Robertson C, Wilson P, Scoular A (2013) Estimation of the risk of tubal factor infertility associated with genital chlamydial infection in women: a statistical modelling study. Int J Epidemiol 42(2):493–503

    Article  PubMed  Google Scholar 

  • Kelver ME et al. (1996) Estrogen regulation of lactoferrin expression in human endometrium. Am J Reprod Immunol 36(5):243–247

    Article  CAS  PubMed  Google Scholar 

  • Kessler M, Zielecki J, Thieck O, Mollenkopf HJ, Fotopoulou C, Meyer TF (2012) Chlamydia trachomatis disturbs epithelial tissue homeostasis in fallopian tubes via paracrine Wnt signaling. Am J Pathol 180(1):186–198

    Article  CAS  PubMed  Google Scholar 

  • Kintner J, Lajoie D, Hall J, Whittimore J, Schoborg RV (2014) Commonly prescribed β-lactam antibiotics induce C. trachomatis persistence/stress in culture at physiologically relevant concentrations. Front Cell Infect Microbiol 4:44

    Google Scholar 

  • Klöckner A, Otten C, Derouaux A et al (2014) AmiA is a penicillin target enzyme with dual activity in the intracellular pathogen Chlamydia pneumoniae. Nat Commun 5:4201

    Article  CAS  PubMed  Google Scholar 

  • Kramer MJ, Gordon FB (1971) Ultrastructural analysis of the effects of penicillin and chlortetracycline on the development of a genital tract Chlamydia. Infect Immun 3(2):333–341

    PubMed  PubMed Central  CAS  Google Scholar 

  • Land JA, Van Bergen JE, Morré SA, Postma MJ (2010) Epidemiology of Chlamydia trachomatis infection in women and the cost-effectiveness of screening. Hum Reprod Update 16(2):189–204

    Article  CAS  PubMed  Google Scholar 

  • Levanon K, Ng V, Piao HY et al (2010) Primary ex vivo cultures of human fallopian tube epithelium as a model for serous ovarian carcinogenesis. Oncogene 29(8):1103–1113

    Article  CAS  PubMed  Google Scholar 

  • Lewis ME, Belland RJ, AbdelRahman YM et al (2014) Morphologic and molecular evaluation of Chlamydia trachomatis growth in human endocervix reveals distinct growth patterns. Front Cell Infect Microbiol. 4:71

    Article  PubMed  PubMed Central  Google Scholar 

  • Liechty ER, Bergin IL, Bassis CM, Chai D, LeBar W, Young VB, Bell JD (2015) The levonorgestrel-releasing intrauterine system is associated with delayed endocervical clearance of Chlamydia trachomatis without alterations in vaginal microbiota. Pathog Dis 73(8):ftv070

    Google Scholar 

  • Low N, Egger M, Sterne JA, Harbord RM, Ibrahim F, Lindblom B, Herrmann B (2006) Incidence of severe reproductive tract complications associated with diagnosed genital chlamydial infection: the Uppsala Women’s Cohort Study. Sex Transm Infect. 2(3):212–218

    Article  Google Scholar 

  • Macleod J, Salisbury C, Low N et al (2005) Coverage and uptake of systematic postal screening for genital Chlamydia trachomatis and prevalence of infection in the United Kingdom general population: cross sectional study. BMJ 330(7497):940

    Article  PubMed  PubMed Central  Google Scholar 

  • Marks E, Tam MA, Lycke NY (2010) The female lower genital tract is a privileged compartment with IL-10 producing dendritic cells and poor Th1 immunity following Chlamydia trachomatis infection. PLoS Pathog 6(11):e1001179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marrazzo JM, White CL, Krekeler B, Celum CL, Lafferty WE, Stamm WE, Handsfield HH (1997) Community-based urine screening for Chlamydia trachomatis with a ligase chain reaction assay. Ann Intern Med 127(9):796–803

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto A, Manire GP (1970) Electron microscopic observations on the effects of penicillin on the morphology of Chlamydia psittaci. J Bacteriol 101(1):278–285

    PubMed  PubMed Central  CAS  Google Scholar 

  • Menon S, Timms P, Allan JA, Alexander K, Rombauts L, Horner P, Keltz M, Hocking J, Huston WM (2015) Human and pathogen factors associated with Chlamydia trachomatis-related infertility in women. Clin Microbiol Rev 28(4):969–985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morrison RP, Caldwell HD (2002) Immunity to murine chlamydial genital infection. Infect Immun 70(6):2741–2751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morrison RP, Belland RJ, Lyng K, Caldwell HD (1989) Chlamydial disease pathogenesis. The 57-kD chlamydial hypersensitivity antigen is a stress response protein. J Exp Med 170(4):1271–1283

    Article  CAS  PubMed  Google Scholar 

  • Newman L, Rowley J, Vander Hoorn S et al (2015) Global estimates of the prevalence and incidence of four curable sexually transmitted infections in 2012 based on systematic review and global reporting. PLoS ONE 10(12):e0143304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paavonen J, Puolakkainen M, Paukku M, Sintonen H (1998) Cost-benefit analysis of first-void urine Chlamydia trachomatis screening program. Obstet Gynecol 92(2):292–298

    PubMed  CAS  Google Scholar 

  • Patton DL, Askienazy-Elbhar M, Henry-Suchet J, Campbell LA, Cappuccio A, Tannous W, Wang SP, Kuo CC (1994) Detection of Chlamydia trachomatis in fallopian tube tissue in women with postinfectious tubal infertility. Am J Obstet Gynecol 171(1):95–101

    Article  CAS  PubMed  Google Scholar 

  • Perfettini JL, Darville T, Dautry-Varsat A, Rank RG, Ojcius DM (2002) Inhibition of apoptosis by gamma interferon in cells and mice infected with Chlamydia muridarum (the mouse pneumonitis strain of Chlamydia trachomatis). Infect Immun 70(5):2559–2565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perry LL, Su H, Feilzer K, Messer R, Hughes S, Whitmire W, Caldwell HD (1999) Differential sensitivity of distinct Chlamydia trachomatis isolates to IFN-gamma-mediated inhibition. J Immunol 162(6):3541–3548

    PubMed  CAS  Google Scholar 

  • Peters RP, Dubbink JH, van der Eem L (2014) Cross-sectional study of genital, rectal, and pharyngeal Chlamydia and gonorrhea in women in rural South Africa. Sex Transm Dis 41(9):564–569

    Article  PubMed  Google Scholar 

  • Phillips Campbell R, Kintner J, Whittimore J, Schoborg RV (2012) Chlamydia muridarum enters a viable but non-infectious state in amoxicillin-treated BALB/c mice. Microbes Infect 14(13):1177–1185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips DM, Swenson CE, Schachter J (1984) Ultrastructure of Chlamydia trachomatis infection of the mouse oviduct. J Ultrastruct Res 3:244–256

    Article  Google Scholar 

  • Phillips-Campbell R, Kintner J, Schoborg RV (2014) Induction of the Chlamydia muridarum stress/persistence response increases azithromycin treatment failure in a murine model of infection. Antimicrob Agents Chemother 58(3):1782–1784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Picard MD, Bodmer JL, Gierahn TM et al (2015) Resolution of Chlamydia trachomatis infection is associated with a distinct T-cell response profile. Clin Vaccine Immunol 22(11):1206–1218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pospischil A, Borel N, Chowdhury EH, Guscetti F (2009) Aberrant chlamydial developmental forms in the gastrointestinal tract of pigs spontaneously and experimentally infected with Chlamydia suis. Vet Microbiol 135(1–2):147–156

    Article  PubMed  Google Scholar 

  • Prusty Böhme L, Bergmann B, Siegl C, Krause E, Mehlitz A, Rudel T (2012) Imbalanced oxidative stress causes chlamydial persistence during non-productive human herpes virus co-infection. PLoS ONE 7(10):e47427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramsey KH, Miranpuri GS, Sigar IM, Ouellette S, Byrne GI (2001) Chlamydia trachomatis persistence in the female mouse genital tract: inducible nitric oxide synthase and infection outcome. Infect Immun 69(8):5131–5137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rank RG, Yeruva L (2014) Hidden in plain sight: chlamydial gastrointestinal infection and its relevance to persistence in human genital infection. Infect Immun 82(4):1362–1371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raulston JE (1997) Response of Chlamydia trachomatis serovar E to iron restriction in vitro and evidence for iron-regulated chlamydial proteins. Infect Immun 65(11):4539–4547

    PubMed  PubMed Central  CAS  Google Scholar 

  • Raulston JE, Miller JD, Davis CH, Schell M, Baldwin A, Ferguson K, Lane H (2007) Identification of an iron-responsive protein that is antigenic in patients with Chlamydia trachomatis genital infections. FEMS Immunol Med Microbiol 51(3):569–576

    Article  CAS  PubMed  Google Scholar 

  • Riley MM, Zurenski MA, Frazer LC, O’Connell CM, Andrews CW Jr, Mintus M, Darville T (2012) The recall response induced by genital challenge with Chlamydia muridarum protects the oviduct from pathology but not from reinfection. Infect Immun 80(6):2194–2203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savy M, Hennig BJ, Doherty CP et al (2010) Haptoglobin and sickle cell polymorphisms and risk of active trachoma in Gambian children. PLoS ONE 5(6):e11075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scott Lamontagne D, Baster K, Emmett L et al (2007) Incidence and reinfection rates of genital chlamydial infection among women aged 16-24 years attending general practice, family planning and genitourinary medicine clinics in England: a prospective cohort study by the Chlamydia Recall Study Advisory Group. Sex Transm Infect. 83(4):292–303

    Article  CAS  PubMed  Google Scholar 

  • Shemer Y, Sarov I (1985) Inhibition of growth of Chlamydia trachomatis by human gamma interferon. Infect Immun 48(2):592–596

    PubMed  PubMed Central  CAS  Google Scholar 

  • Slade J, Hall JV, Kintner J, Schoborg RV (2016) Chlamydial pre-infection protects from subsequent herpes simplex virus-2 challenge in a murine vaginal super-infection model. PLoS ONE 11(1):e0146186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stephens RS (2003) The cellular paradigm of chlamydial pathogenesis. Trends Microbiol 11(1):44–51

    Article  CAS  PubMed  Google Scholar 

  • Tan C, Hsia RC, Shou H, Carrasco JA, Rank RG, Bavoil PM (2010) Variable expression of surface-exposed polymorphic membrane proteins in in vitro-grown Chlamydia trachomatis. Cell Microbiol 12(2):174–187

    Article  CAS  PubMed  Google Scholar 

  • Tanami Y, Yamada Y (1973) Miniature cell formation in Chlamydia psittaci. J Bacteriol 114(1):408–412

    PubMed  PubMed Central  CAS  Google Scholar 

  • Thompson CC, Carabeo RA (2011) An optimal method of iron starvation of the obligate intracellular pathogen, Chlamydia trachomatis. Front Microbiol 2:20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torrone E, Papp J, Weinstock H, Centers for Disease Control and Prevention (CDC) (2014) Prevalence of Chlamydia trachomatis genital infection among persons aged 14-39 years–United States, 2007-2012. MMWR Morb Mortal Wkly Rep 63(38):834–838

    Google Scholar 

  • Trebach JD, Chaulk CP, Page KR, Tuddenham S, Ghanem KG (2015) Neisseria gonorrhoeae and Chlamydia trachomatis among women reporting extragenital exposures. Sex Transm Dis 42(5):233–239

    Article  PubMed  PubMed Central  Google Scholar 

  • van Liere GA, Hoebe CJ, Wolffs PF, Dukers-Muijrers NH (2014) 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 14:274

    Article  PubMed  PubMed Central  Google Scholar 

  • van Valkengoed IG, Morré SA, van den Brule AJ, Meijer CJ, Bouter LM, Boeke AJ (2004) Overestimation of complication rates in evaluations of Chlamydia trachomatis screening programmes—implications for cost-effectiveness analyses. Int J Epidemiol 33(2):416–425

    Article  PubMed  Google Scholar 

  • Vanover J, Sun J, Deka S, Kintner J, Duffourc MM, Schoborg RV (2008) Herpes simplex virus co-infection-induced Chlamydia trachomatis persistence is not mediated by any known persistence inducer or anti-chlamydial pathway. Microbiology 154(Pt 3):971–978

    Article  CAS  PubMed  Google Scholar 

  • Vanover J, Kintner J, Whittimore J, Schoborg RV (2010) Interaction of herpes simplex virus type 2 (HSV-2) glycoprotein D with the host cell surface is sufficient to induce Chlamydia trachomatis persistence. Microbiology 156(Pt 5):1294–1302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vardhan H, Bhengraj AR, Jha R, Singh Mittal A (2009) Chlamydia trachomatis alters iron-regulatory protein-1 binding capacity and modulates cellular iron homeostasis in HeLa-229 cells. J Biomed Biotechnol. 2009:342032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Versteeg B, van Rooijen MS, Schim van der Loeff MF, de Vries HJ, Bruisten SM (2014) No indication for tissue tropism in urogenital and anorectal Chlamydia trachomatis infections using high-resolution multilocus sequence typing. BMC Infect Dis 14:464

    Article  PubMed  PubMed Central  Google Scholar 

  • Walker J, Tabrizi SN, Fairley CK et al (2012) Chlamydia trachomatis incidence and re-infection among young women—behavioural and microbiological characteristics. PLoS One 7(5):e37778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wallace LA, Scoular A, Hart G, Reid M, Wilson P, Goldberg DJ (2008) What is the excess risk of infertility in women after genital chlamydia infection? A systematic review of the evidence. Sex Transm Infect. 84(3):171–175

    Article  CAS  PubMed  Google Scholar 

  • Wolf K, Fischer E, Hackstadt T (2000) Ultrastructural analysis of developmental events in Chlamydia pneumoniae-infected cells. Infect Immun 68(4):2379–2385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wyrick PB (2000) Intracellular survival by Chlamydia. Cell Microbiol 2(4):275–282

    Article  CAS  PubMed  Google Scholar 

  • Wyrick PB (2010) Chlamydia trachomatis persistence in vitro: an overview. J Infect Dis 201(Suppl 2):S88–S95

    Article  CAS  PubMed  Google Scholar 

  • Wyrick PB, Knight ST (2004) Pre-exposure of infected human endometrial epithelial cells to penicillin in vitro renders Chlamydia trachomatis refractory to azithromycin. J Antimicrob Chemother 54(1):79–85

    Article  CAS  PubMed  Google Scholar 

  • Xu F, Stoner BP, Taylor SN, Mena L, Tian LH, Papp J, Hutchins K, Martin DH, Markowitz LE (2011) Use of home-obtained vaginal swabs to facilitate rescreening for Chlamydia trachomatis infections: two randomized controlled trials. Obstet Gynecol 118(2 Pt 1):231–239

    Article  PubMed  Google Scholar 

  • Yeruva L, Spencer N, Bowlin AK, Wang Y, Rank RG (2013a) Chlamydial infection of the gastrointestinal tract: a reservoir for persistent infection. Pathog Dis 68(3):88–95

    Article  CAS  PubMed  Google Scholar 

  • Yeruva L, Melnyk S, Spencer N, Bowlin A, Rank RG (2013b) Differential susceptibilities to azithromycin treatment of chlamydial infection in the gastrointestinal tract and cervix. Antimicrob Agents Chemother 57(12):6290–6294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshimura K, Yoshimura M, Kobayashi T, Kubo T, Hachisuga T, Kashimura M (2009) Can bacterial vaginosis help to find sexually transmitted diseases, especially chlamydial cervicitis? Int J STD AIDS 20(2):108–111

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Huang Y, Gong S, Yang Z, Sun X, Schenken R, Zhong G (2015) In vivo and ex vivo imaging reveals a long-lasting chlamydial infection in the mouse gastrointestinal tract following genital tract inoculation. Infect Immun 83(9):3568–3577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Infectious Diseases and Microbiology, University of Lübeck, Ratzeburger Allee 160, 23538, Lübeck, Germany

    Larissa Schuchardt & Jan Rupp

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  1. Larissa Schuchardt
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  2. Jan Rupp
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Correspondence to Jan Rupp .

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  1. Institute of Microbiology and Hygiene, Universitätsklinikum Freiburg, Freiburg, Germany

    Georg Häcker

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Schuchardt, L., Rupp, J. (2016). Chlamydia trachomatis as the Cause of Infectious Infertility: Acute, Repetitive or Persistent Long-Term Infection?. In: Häcker, G. (eds) Biology of Chlamydia . Current Topics in Microbiology and Immunology, vol 412. Springer, Cham. https://doi.org/10.1007/82_2016_15

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