Abstract
The chronic female disease endometriosis causes debilitating pain and lowered fertility. The aetiology is unknown, but indications of an infectious agent are present. This study investigates the possible involvement of a pathogenic virus in endometriosis patients and controls. DNA was purified from biopsies and subjected to highly sensitive PCR tests detecting human papillomavirus (HPV) types, the herpes family viruses HSV-1 and -2, CMV, and EBV, and the polyomaviruses SV40, JCV, BKV, KIV, WUV, and MCV. The prevalence of pathogenic DNA viruses in the human endometrium was generally low (0–10%). The virus prevalence was found to vary slightly when comparing the endometrium of healthy women and women with endometriosis. However, these were not significant differences, and no viruses were identified in endometriotic lesions. These results do not point towards any evidence that endometriosis is caused by these viruses.
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Acien P, Quereda F, Campos A, Gomez-Torres MJ, Velasco I, Gutierrez M (2002) Use of intraperitoneal interferon alpha-2b therapy after conservative surgery for endometriosis and postoperative medical treatment with depot gonadotropin-releasing hormone analog: a randomized clinical trial. Fertil Steril 78:705–711
Ali AFM, Fateen B, Ezzet A, Badawy H, Ramadan A, El-tobge A (2000) Laparoscopic intraperitoneal injection of human interferon-[alpha]2b in the treatment of pelvic endometriosis: a new modality. Obstet Gynecol 95:S47–S48
Allander T, Andreasson K, Gupta S, Bjerkner A, Bogdanovic G, Persson MAA, Dalianis T, Ramqvist T, Andersson B (2007) Identification of a third human polyomavirus. J Virol 81:4130–4136
Anderson RA, Scobie L, O’Neil BW, Grindlay GJ, Campo MS (1997) Viral proteins of bovine papillomavirus type 4 during the development of alimentary canal tumours. Vet J 154:69–78
Aubin F, Humbey O, Guerrini JS, Mougin C, Laurent R (2003) Non-melanoma skin cancers and human papillomavirus. Ann Dermatol Venereol 130:1131–1138
Ault KA (2006) Epidemiology and natural history of human papillomavirus infections in the female genital tract. Infect Dis Obstet Gynecol 2006(Suppl):40470
Badawy SZA, Etman A, Cuenca V, Montante A, Kaufman L (2001) Effect of interferon alpha-2b on endometrioma cells in vitro. Obstet Gynecol 98:417–420
Barbanti-Brodano G, Sabbioni S, Martini F, Negrini M, Corallini A, Tognon M (2004) Simian virus 40 infection in humans and association with human diseases: results and hypotheses. Virology 318:1–9
Béliard A, Noël A, Foidart J-M (2004) Reduction of apoptosis and proliferation in endometriosis. Fertil Steril 82:80–85
Bialasiewicz S, Whiley DM, Lambert SB, Gould A, Nissen MD, Sloots TP (2007) Development and evaluation of real-time PCR assays for the detection of the newly identified KI and WU polyomaviruses. J Clin Virol 40:9–14
Brown HL, Abernathy MP (1998) Cytomegalovirus infection. Semin Perinatol 22:260–266
Caldarelli-Stefano R, Vago L, Omodeo-Zorini E, Mediati M, Losciale L, Nebuloni M, Costanzi G, Ferrante P (1999) Detection and typing of JC virus in autopsy brains and extraneural organs of AIDS patients and non-immunocompromised individuals. J Neurovirol 5:125–133
Chen AC, Keleher A, Kedda MA, Spurdle AB, McMillan NA, Antonsson A (2009) Human papillomavirus DNA detected in peripheral blood samples from healthy Australian male blood donors. J Med Virol 81:1792–1796
Cinatl J Jr, Cinatl J, Vogel JU, Rabenau H, Kornhuber B, Doerr HW (1996) Modulatory effects of human cytomegalovirus infection on malignant properties of cancer cells. Intervirology 39:259–269
Comar M, Rizzardi C, de Zotti R, Melato M, Bovenzi M, Butel JS, Campello C (2007) SV40 multiple tissue infection and asbestos exposure in a hyperendemic area for malignant mesothelioma. Cancer Res 67:8456–8459
de Roda Husman A-M, Walboomers JMM, van den Brule AJC, Meijer CJLM, Snijders PJF (1995) The use of general primers GP5 and GP6 elongated at their 3′ ends with adjacent highly conserved sequences improves human papillomavirus detection by PCR. J Gen Virol 76:1057–1062
de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H (2004) Classification of papillomaviruses. Virology 324:17–27
Deragon JM, Sinnett D, Mitchell G, Potier M, Labuda D (1990) Use of gamma irradiation to eliminate DNA contamination for PCR. Nucleic Acids Res 18:6149
Dolcetti R, Masucci MG (2003) Epstein–Barr virus: induction and control of cell transformation. J Cell Physiol 196:207–218
Dörries K (2002) Latent and persistent polyomavirus infection. In: Kamel Khalili GLS (ed) Human polyomaviruses. Wiley-Liss, Inc., Wilmington, pp 197–235
Fedele CG, Ciardi M, Delia S, Echevarria JM, Tenorio A (1999) Multiplex polymerase chain reaction for the simultaneous detection and typing of polyomavirus JC, BK and SV40 DNA in clinical samples. J Virol Methods 82:137–144
Feng H, Shuda M, Chang Y, Moore PS (2008) Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 319:1096–1100
Forslund O, Antonsson A, Nordin P, Stenquist B, Goran Hansson B (1999) A broad range of human papillomavirus types detected with a general PCR method suitable for analysis of cutaneous tumours and normal skin. J Gen Virol 80:2437–2443
Galloway DA, McDougall JK (1983) The oncogenic potential of herpes simplex viruses: evidence for a ‘hit-and-run’ mechanism. Nature 302:21–24
Gaynor AM, Nissen MD, Whiley DM, Mackay IM, Lambert SB, Wu G, Brennan DC, Storch GA, Sloots TP, Wang D (2007) Identification of a novel polyomavirus from patients with acute respiratory tract infections. PLoS Pathog 3:e64
Giudice LC, Kao LC (2004) Endometriosis. Lancet 364:1789–1799
Gupta R, Warren T, Wald A (2007) Genital herpes. Lancet 370:2127–2137
Hu L, Hornung D, Kurek R, Ostman H, Blomberg J, Bergqvist A (2006) Expression of human endogenous gammaretroviral sequences in endometriosis and ovarian cancer. AIDS Res Hum Retroviruses 22:551–557
Khalili K, Del Valle L, Otte J, Weaver M, Gordon J (2003) Human neurotropic polyomavirus, JCV, and its role in carcinogenesis. Oncogene 22:5181–5191
Kutsuna T, Zheng H, Abdel-Aziz HO, Murai Y, Tsuneyama K, Furuta I, Takano Y (2008) High JC virus load in tongue carcinomas may be a risk factor for tongue tumorigenesis. Virchows Arch 452:405–410
Lefrancq T, Orain I, Michalak S, Hourseau M, Fetissof F (1999) Herpetic salpingitis and fallopian tube prolapse. Histopathology 34:548–550
Melin A, Sparen P, Bergqvist A (2007) The risk of cancer and the role of parity among women with endometriosis. Hum Reprod 22:3021–3026
Moens U, Johannessen M (2008) Human polyomaviruses and cancer: expanding repertoire. J Dtsch Dermatol Ges 6:704–708
Neske F, Blessing K, Pröttel A, Ullrich F, Kreth HW, Weissbrich B (2009) Detection of WU polyomavirus DNA by real-time PCR in nasopharyngeal aspirates, serum, and stool samples. J Clin Virol 44:115–118
Oppelt P, Renner SP, Strick R, Valletta D, Mehlhorn G, Fasching PA, Beckmann MW, Strissel PL (2009) Correlation of high-risk human papilloma viruses but not of herpes viruses or Chlamydia trachomatis with endometriosis lesions. Fertil Steril (in press)
Pietropaolo V, Fioriti D, Simeone P, Videtta M, Di Taranto C, Arancio A, Orsi N, Degener AM (2003) Detection and sequence analysis of human polyomaviruses DNA from autoptic samples of HIV-1 positive and negative subjects. Int J Immunopathol Pharmacol 16:269–276
Paavonen J, Teisala K, Heinonen PK, Aine R, Miettinen A, Lehtinen M, Gronroos P (1985) Endometritis and acute salpingitis associated with Chlamydia trachomatis and herpes simplex virus type two. Obstet Gynecol 65:288–291
Sahin F, Gerceker D, Karasartova D, Ozsan TM (2007) Detection of herpes simplex virus type 1 in addition to Epstein-Bar virus in tonsils using a new multiplex polymerase chain reaction assay. Diagn Microbiol Infect Dis 57:47–51
Sharp Colin ÂP, Norja Pi, Anthony I, Bell Jeanne ÂE, Simmonds P (2009) Reactivation and mutation of newly discovered WU, KI, and Merkel cell carcinoma polyomaviruses in immunosuppressed individuals. J Infect Dis 199:398–404
Sinaii N, Cleary SD, Ballweg ML, Nieman LK, Stratton P (2002) High rates of autoimmune and endocrine disorders, fibromyalgia, chronic fatigue syndrome and atopic diseases among women with endometriosis: a survey analysis. Hum Reprod 17:2715–2724
Siristatidis C, Nissotakis C, Chrelias C, Iacovidou H, Salamalekis E (2006) Immunological factors and their role in the genesis and development of endometriosis. J Obstet Gynaecol Res 32:162–170
Walboomers JMM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Muñoz N (1999) Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189:12–19
Watzinger F, Suda M, Preuner S, Baumgartinger R, Ebner K, Baskova L, Niesters HGM, Lawitschka A, Lion T (2004) Real-time quantitative PCR assays for detection and monitoring of pathogenic human viruses in immunosuppressed pediatric patients. J Clin Microbiol 42:5189–5198
Weaver BA (2006) Epidemiology and natural history of genital human papillomavirus infection. J Am Osteopathic Assoc 106:S2–S8
Weidmann M, Meyer-Konig U, Hufert FT (2003) Rapid detection of herpes simplex virus and varicella-zoster virus infections by real-time PCR. J Clin Microbiol 41:1565–1568
Wilson SS, Fakioglu E, Herold BC (2009) Novel approaches in fighting herpes simplex virus infections. Expert Rev Anti Infect Ther 7:559–568
zur Hausen H (2009) Papillomaviruses in the causation of human cancers—a brief historical account. Virology 384:260–265
Acknowledgments
We would like to thank Dr. Viviana Lutzky and Prof. Denis Moss from Queensland Institute of Medical Research, Brisbane, QLD, Australia, for donating positive control virus samples. Thanks are also due to Dr. Nigel McMillan for stimulating discussions. This work was supported by the Novo Nordisk Foundation, A. P. Møller’s Foundation for the Advancement of Medical Science, Aarhus Graduate School of Science, the Augustinus Foundation, the Harboe Foundation, Familien Hede Nielsen’s Foundation, Knud Højgaard’s Foundation, the Oticon Foundation, and Ingeniør Alexandre Haynman og hustru Nina Haynman’s Foundation, Denmark, Svenska Sällskapet för Medicinsk Forskning and the Mazda foundation, Sweden, and the Prostate Cancer Foundation, Australia.
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Vestergaard, A.L., Knudsen, U.B., Munk, T. et al. Low prevalence of DNA viruses in the human endometrium and endometriosis. Arch Virol 155, 695–703 (2010). https://doi.org/10.1007/s00705-010-0643-y
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DOI: https://doi.org/10.1007/s00705-010-0643-y