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Prevalence of Chlamydia trachomatis endocervical infection in systemic lupus erythematosus patients and evaluation of the risk for HPV-induced lesions

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Abstract

Chlamydia trachomatis (CT) is the most common bacterial cause of sexually transmitted disease. It has been associated with arthritis and it is a risk factor for human papillomavirus (HPV)-induced lesions. There are few studies on the frequency of CT infection among systemic lupus erythematosus (SLE) patients. The aim of this study was to determine the prevalence of endocervical CT infection among SLE patients and evaluate whether or not CT infection is a risk factor for HPV-induced lesions. A cross-sectional study included a group of patients who fulfilled the American College Rheumatology criteria for a definite diagnosis of SLE and a control group of non-SLE female individuals from Bahia, Brazil. Polymerase chain reaction was used on endocervical swab specimens to test for CT; a gynecological examination including a cervical cytology and biopsy was done for the identification of HPV lesions. A total of 105 SLE patients were studied, and the control group was composed of 104 age-matched apparently normal women. The prevalence of CT endocervical infection was 3.0 % [confidence interval (CI) 95 % = 0.6–8.0 %] in the SLE group and 5.0 % (95 % CI = 2.0–11.0 %) in the control group; the prevalence ratio was 0.60 (95 % CI = 0.1–2.5). The prevalence of vulvar condyloma was higher among SLE patients (11.0 vs. 1.0 %, p < 0.001), as were the prevalences of low-grade lesion (12.0 vs. 1.0 %, p < 0.001) and cervical intraepithelial neoplasia 1 (9.0 vs. 1.0 %, p = 0.02). There was no association between the presence of HPV lesions and CT infections. However, the small number of patients with CT prevents a definite conclusion from being drawn. The prevalence of endocervical CT infection in women with SLE is low and similar to that of the normal population. This suggests that this infection has no role in the pathogenesis of SLE or the development of HPV-induced lesions.

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References

  1. CDC Grand Rounds (2011) Chlamydia prevention: challenges and strategies for reducing disease burden and sequelae. MMWR Morb Mortal Wkly Rep 60(12):370–373

    Google Scholar 

  2. Oakeshott P, Kerry S, Aghaizu A, Atherton H, Hay S, Taylor-Robinson D et al (2010) Randomised controlled trial of screening for Chlamydia trachomatis to prevent pelvic inflammatory disease: the POPI (prevention of pelvic infection) trial. BMJ 340:c1642. doi:10.1136/bmj.c1642

  3. Unemo M, Rossouw A, James V, Jenkins C (2009) Can the Swedish new variant of Chlamydia trachomatis (nvCT) be detected by UK NEQAS participants from seventeen European countries and five additional countries/regions in 2009? Euro Surveill 14(19):pii=19206. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19206

  4. Wilson JS, Honey E, Templeton A, Paavonen J, Mardh PA, Stray-Pedersen B (2002) A systematic review of the prevalence of Chlamydia trachomatis among European women. Hum Reprod Update 8(4):385–394

    Article  PubMed  CAS  Google Scholar 

  5. de Codes JS, Cohen DA, de Melo NA, Teixeira GG, Leal AS, Silva TJ et al (2006) Screening of sexually transmitted diseases in clinical and non-clinical settings in Salvador, Bahia, Brazil. Cad Saude Publica 22(2):325–334

    Article  PubMed  Google Scholar 

  6. Eleuterio RMN, Eleuterio J Jr, Giraldo PC, Muniz AMV (2007) Cervicite por Chlamydia trachomatis em mulheres sexualmente ativas atendidas em um serviço privado de ginecologia na cidade de Fortaleza. Rev Bras Anal Clin (4):287–290

  7. Fernandes AM, Daher G, Nuzzi RX, Petta CA (2009) Chlamydia trachomatis and Neisseria gonorrhoeae among women in a family planning clinic. Rev Bras Ginecol Obstet 31(5):235–240

    Article  PubMed  Google Scholar 

  8. Igansi C (2005) Prevalência de Papilomavírus Humano (HPV) e Chlamydia trachomatis e sua associação com lesões cervicais em uma amostra de mulheres assintomáticas de Porto Alegre. Universidade Federal do Rio Grande do Sul (Thesis)

  9. Kitumnuaypong T, Scalzi LV, Nalbant S, Von Feldt JM, Schumacher HR Jr (2004) Is there a role for Chlamydia pneumoniae infection in systemic lupus erythematosus and in the associated atherosclerotic cardiovascular disease? Clin Exp Rheumatol 22(3):339–342

    PubMed  CAS  Google Scholar 

  10. Dejmoková H, Drazdakowá M, Mares Z et al (2005) Chlamydia trachomatis and Chlamydophilla pneumoniae antibodies in a cohort of rheumatic patients. Ceska Revmatologie 13(1):3–7

    Google Scholar 

  11. Fernandez RN, Ximenes AC, Alves MF (2005) Detecção do DNA de Chlamydia trachomatis em espondiloartropatias e artrite reumatóide. Rev Bras Reumatol 45(5):1–12

    Google Scholar 

  12. Keat AC, Thomas BJ, Taylor-Robinson D, Pegrum GD, Maini RN, Scott JT (1980) Evidence of Chlamydia trachomatis infection in sexually acquired reactive arthritis. Ann Rheum Dis 39(5):431–437

    Article  PubMed  CAS  Google Scholar 

  13. Kuipers JG, Sibilia J, Bas S, Gaston H, Granfors K, Vischer TL et al (2009) Reactive and undifferentiated arthritis in North Africa: use of PCR for detection of Chlamydia trachomatis. Clin Rheumatol 28(1):11–16

    Article  PubMed  CAS  Google Scholar 

  14. Sweet RL, Gibbs RS (2009) Chlamydial infectious. In: Sweet RL, Gibbs RS (eds) Infectious disease of the female genital tract, 5th edn. Lippincott Williams and Wilkins, Philadelphia, pp 18–40

    Google Scholar 

  15. Zeidler H, Kuipers J, Kohler L (2004) Chlamydia-induced arthritis. Curr Opin Rheumatol 16(4):380–392

    Article  PubMed  Google Scholar 

  16. Giuliano AR, Denman C, de Guernsey ZJ, Navarro Henze JL, Ortega L, Djambazov B et al (2001) Design and results of the USA-Mexico border human papillomavirus (HPV), cervical dysplasia, and Chlamydia trachomatis study. Rev Panam Salud Publica 9(3):172–181

    Article  PubMed  CAS  Google Scholar 

  17. Lehtinen M, Ault KA, Lyytikainen E, Dillner J, Garland SM, Ferris DG et al (2011) Chlamydia trachomatis infection and risk of cervical intraepithelial neoplasia. Sex Transm Infect 87(5):372–376

    Google Scholar 

  18. Marcolino LD, Polettini J, Tristão AR, Marques MEA et al (2008) Coinfecção de Chlamydia trachomatis e HPV em mulheres com condiloma cuminado. DST J Bras Doenças Sex Transm 20(2):87–92

    Google Scholar 

  19. Doria A, Canova M, Tonon M, Zen M, Rampudda E, Bassi N et al (2008) Infections as triggers and complications of systemic lupus erythematosus. Autoimmun Rev 8(1):24–28

    Article  PubMed  CAS  Google Scholar 

  20. Navarra SV, Leynes MS (2010) Infections in systemic lupus erythematosus. Lupus 19(12):1419–1424

    Article  PubMed  CAS  Google Scholar 

  21. Zandman-Goddard G, Shoenfeld Y (2005) Infections and SLE. Autoimmunity 38(7):473–485

    Article  PubMed  CAS  Google Scholar 

  22. Zonana-Nacach A, Camargo-Coronel A, Yanez P, Sanchez L, Jimenez-Balderas FJ, Fraga A (2001) Infections in outpatients with systemic lupus erythematosus: a prospective study. Lupus 10(7):505–510

    Article  PubMed  CAS  Google Scholar 

  23. Klumb EM, Pinto A, Jesus G, Araujo JM, Jascone L, Gayer C et al (2010) Are women with lupus at higher risk of HPV infection? Lupus 19(13):1485–1491

    Google Scholar 

  24. Santana IU, Gomes AN, Lyrio LD, Rios Grassi MF, Santiago MB (2011) Systemic lupus erythematosus, human papillomavirus infection, cervical pre-malignant and malignant lesions: a systematic review. Clin Rheumatol 30(5):665–672

    Article  PubMed  Google Scholar 

  25. Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40(9):1725

    Article  PubMed  CAS  Google Scholar 

  26. Hammes LS, Naud P, Passos EP, Matos J, Brouwers K, Rivoire W et al (2007) Value of the international federation for cervical pathology and colposcopy (IFCPC) terminology in predicting cervical disease. J Low Genit Tract Dis 11(3):158–165

    Article  PubMed  Google Scholar 

  27. Solomon D, Davey D, Kurman R, Moriarty A, O’Connor D, Prey M et al (2002) The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA 287(16):2114–2119

    Article  PubMed  Google Scholar 

  28. Richart RM (1990) A modified terminology for cervical intraepithelial neoplasia. Obstet Gynecol 75(1):131–133

    PubMed  CAS  Google Scholar 

  29. Gerber S, Tonna SD, Delaloye JF (2008) A new classification of vulvar intraepithelial neoplasia (VIN). Rev Med Suisse 4(176):2281–2285

    PubMed  Google Scholar 

  30. Santos C, Teixeira F, Vicente A, Astolfi-Filho S (2003) Detection of Chlamydia trachomatis in endocervical smears of sexually active women in Manaus-AM, Brazil, by PCR. Braz J Infect Dis 7(2):91–95

    Article  PubMed  CAS  Google Scholar 

  31. Mahony JB, Luinstra KE, Sellors JW, Chernesky MA (1993) Comparison of plasmid- and chromosome-based polymerase chain reaction assays for detecting Chlamydia trachomatis nucleic acids. J Clin Microbiol 31(7):1753–1758

    PubMed  CAS  Google Scholar 

  32. al-Janadi M, al-Balla S, al-Dalaan A, Raziuddin S (1993) Cytokine profile in systemic lupus erythematosus, rheumatoid arthritis, and other rheumatic diseases. J Clin Immunol 13(1):58–67

    Article  PubMed  CAS  Google Scholar 

  33. Crow MK, Kirou KA (2007) Cytokines and interferons in lupus. In: Wallace DJ, Hahn BH (ed) Dubois’Lupus Erythematosus, 7th edn. Lippincott William and Wilkins, Philadelphia, pp 161–175

  34. Cheng C, Cruz-Fisher MI, Tifrea D, Pal S, Wizel B, de la Maza LM (2011) Induction of protection in mice against a respiratory challenge by a vaccine formulated with the Chlamydia major outer membrane protein adjuvanted with IC31(R). Vaccine 29(13):2437–2443

    Article  PubMed  CAS  Google Scholar 

  35. Gondek DC, Roan NR, Starnbach MN (2009) T cell responses in the absence of IFN-gamma exacerbate uterine infection with Chlamydia trachomatis. J Immunol 183(2):1313–1319

    Article  PubMed  CAS  Google Scholar 

  36. Morrison RP (2003) New insights into a persistent problem—chlamydial infections. J Clin Invest 111(11):1647–1649

    PubMed  CAS  Google Scholar 

  37. Sun G, Pal S, Weiland J, Peterson EM, de la Maza LM (2009) Protection against an intranasal challenge by vaccines formulated with native and recombinant preparations of the Chlamydia trachomatis major outer membrane protein. Vaccine 27(36):5020–5025

    Article  PubMed  CAS  Google Scholar 

  38. Leung PS, Park O, Matsumura S, Ansari AA, Coppel RL, Gershwin ME (2003) Is there a relation between Chlamydia infection and primary biliary cirrhosis? Clin Dev Immunol 10(2–4):227–233

    Article  PubMed  CAS  Google Scholar 

  39. Tam LS, Chan AY, Chan PK, Chang AR, Li EK (2004) Increased prevalence of squamous intraepithelial lesions in systemic lupus erythematosus: association with human papillomavirus infection. Arthritis Rheum 50(11):3619–3625

    Article  PubMed  Google Scholar 

  40. Tam LS, Chan PK, Ho SC, Yu MM, Yim SF, Cheung TH et al (2010) Natural history of cervical papilloma virus infection in systemic lupus erythematosus—a prospective cohort study. J Rheumatol 37(2):330–340

    Article  PubMed  Google Scholar 

  41. Madeleine MM, Anttila T, Schwartz SM, Saikku P, Leinonen M, Carter JJ et al (2007) Risk of cervical cancer associated with Chlamydia trachomatis antibodies by histology, HPV type and HPV cofactors. Int J Cancer 120(3):650–655

    Article  PubMed  CAS  Google Scholar 

  42. Simonetti AC, Melo JH, de Souza PR, Bruneska D, de Lima Filho JL (2009) Immunological’s host profile for HPV and Chlamydia trachomatis, a cervical cancer cofactor. Microbes Infect 11(4):435–442

    Article  PubMed  CAS  Google Scholar 

  43. Tamim H, Finan RR, Sharida HE, Rashid M, Almawi WY (2002) Cervicovaginal coinfections with human papillomavirus and Chlamydia trachomatis. Diagn Microbiol Infect Dis 43(4):277–281

    Article  PubMed  Google Scholar 

  44. Calil LN, Igansi CN, Meurer L, Edelweiss MI, Bozzetti MC (2011) Chlamydia trachomatis and human papillomavirus coinfection: association with p16INK4a and Ki67 expression in biopsies of patients with pre-neoplastic and neoplastic lesions. Braz J Infect Dis 15(2):126–131

    Article  PubMed  Google Scholar 

  45. Claas EC, Melchers WJ, Niesters HG, van MR, Stolz E, Quint WG (1992) Infections of the cervix uteri with human papillomavirus and Chlamydia trachomatis. J Med Virol 37(1):54–57

    Article  PubMed  CAS  Google Scholar 

  46. Edelman M, Fox A, Alderman E, Neal W, Shapiro A, Silver EJ et al (2000) Cervical papanicolaou smear abnormalities and Chlamydia trachomatis in sexually active adolescent females. J Pediatr Adolesc Gynecol 13(2):65–69

    Article  PubMed  CAS  Google Scholar 

  47. Mitrani-Rosenbaum S, Tsvieli R, Lavie O, Boldes R, Anteby E, Shimonovitch S et al (1994) Simultaneous detection of three common sexually transmitted agents by polymerase chain reaction. Am J Obstet Gynecol 171(3):784–790

    PubMed  CAS  Google Scholar 

  48. Reesink-Peters N, Ossewaarde JM, Van Der Zee AG, Quint WG, Burger MP, Adriaanse AH (2001) No association of anti-Chlamydia trachomatis antibodies and severity of cervical neoplasia. Sex Transm Infect 77(2):101–102

    Article  PubMed  CAS  Google Scholar 

  49. Lyrio LD. Prevalence oF endocervical HPV in systemic lupus erythematosus Thesis presented at Escola Bahiana de Medicina e Saúde Pública, Bahia, Brazil; 2011

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Acknowledgments

We thank Dr. Martha Silveira and Adelvani Boa Morte, librarians at Centro de Pesquisas Gonçalo Moniz/Fundação Oswaldo Cruz, Salvador; Drs. Eliana de Paula Santos, Margarida Santos Matos, Ana Paula Monteiro, Mrs. Caroline Gaspar and all other staff of the Escola Bahiana de Medicina e Saúde Pública. MS receives a grant from the National Council for Scientific and Technological Development (CNPq).

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Correspondence to Mittermayer Barreto Santiago.

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This article is part of Licia CostaPinto M.Sc Thesis of Bahiana School of Medicine and Public Health Post-Graduate Course.

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CostaPinto, L., Olavarria, V.G., Grassi, M.F.R. et al. Prevalence of Chlamydia trachomatis endocervical infection in systemic lupus erythematosus patients and evaluation of the risk for HPV-induced lesions. Rheumatol Int 33, 631–636 (2013). https://doi.org/10.1007/s00296-012-2419-z

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