Top

International Journal of Public Health

Published in:

01-11-2015 | Review

Considering treatment of male genital schistosomiasis as a tool for future HIV prevention: a systematic review

Authors: Chalotte Willemann Stecher, Per Kallestrup, Eyrun Floerecke Kjetland, Birgitte Vennervald, Eskild Petersen

Published in: International Journal of Public Health | Issue 7/2015

Abstract

Objectives

Male genital schistosomiasis (MGS) is a neglected manifestation of Schistosoma haematobium infection with ignored implications on reproductive health and a differential diagnosis to sexually transmitted infections in endemic regions. MGS may have associations with HIV transmission and acquisition, and treatment could be a neglected chance of HIV prevention. This review summarizes current knowledge on epidemiology, clinical manifestations, diagnosis and treatment of MGS as a hypothesized risk factor for HIV transmission. Future research areas of global interest are suggested.

Methods

PubMed published literature was reviewed based on the MOOSE guidelines. All publications on MGS were included regardless of publication year and study design. Furthermore, all publications were searched for information on possible HIV association.

Results

The 40 identified publications related to MGS were dominated by case reports and observational studies. No randomized clinical trials have been conducted to date, and very scant information related to possible associations with HIV transmission was presented.

Conclusions

Clinical, randomized studies and epidemiological studies covering the possible association between MGS and HIV are urgently needed. Furthermore, field diagnostic tools should be developed and future mass treatment programs should include adults to reduce morbidity and prevent HIV acquisition.

Systematic review registration number

CRD42015016252.

Aboul TE, Saad SM, Arafa AF, Ghorab MM (1977) Can bilharziasis of the seminal vesicles be a cause of obstructive infertility? Fertil Steril 28(7):775–776PubMed

Adisa J, Egbujo EM, Yahaya BA, Echejoh G (2012) Primary infertility associated with schistosoma mansoni: a case report from the Jos plateau, north central Nigeria. Afr Health Sci 12(4):563–565PubMedCentralPubMed

Al Adnani MS (1985) Schistosomiasis, metaplasia and squamous cell carcinoma of the prostate: histogenesis of the squamous cancer cells determined by localization of specific markers. Neoplasma 32(5):613–622PubMed

Alexis R, Domingo J (1986) Schistosomiasis and adenocarcinoma of prostate: a morphologic study. Hum Pathol 17(7):757–760CrossRefPubMed

Al-Saeed O, Sheikh M, Kehinde EO, Makar R (2003) Seminal vesicle masses detected incidentally during transrectal sonographic examination of the prostate. J Clin Ultr JCU 31(4):201–206. doi:10.1002/jcu.10158 CrossRef

Barlow CH, Meleney HE (1949) A voluntary infection with Schistosoma haematobium. Am J Trop Med Hyg 29(1):79–87PubMed

Bornman MS, Kok EL, Otto BS, Du Toit D, Du Plessis DJ (1992) Improved semen quality after treatment for schistosomiasis. South Afr Med J Suid Afr Tydskrif vir Geneeskunde 81(8):437–438

Capron A, Dessaint JP (1992) Immunologic aspects of schistosomiasis. Annu Rev Med 43:209–218. doi:10.1146/annurev.me.43.020192.001233 CrossRefPubMed

Carey FM, Quah SP, Hedderwick S, Finnegan D, Dinsmore WW, Maw RD (2001) Genital schistosomiasis. Int J STD AIDS 12(9):609–611CrossRefPubMed

Chakraborty H et al (2001) Viral burden in genital secretions determines male-to-female sexual transmission of HIV-1: a probabilistic empiric model. AIDS Lond Eng 15(5):621–627CrossRef

Cioli D (1998) Chemotherapy of schistosomiasis: an update. Parasitol Today Personal Ed 14(10):418–422CrossRef

Cohen RJ, Edgar SG, Cooper K (1995) Schistosomiasis and prostate cancer. Pathology 27(2):115–116CrossRefPubMed

Cohen MS et al (1997) Reduction of concentration of HIV-1 in semen after treatment of urethritis: implications for prevention of sexual transmission of HIV-1. AIDSCAP Malawi Research Group. Lancet 349(9069):1868–1873CrossRefPubMed

Colley DG, Secor WE (2007) A schistosomiasis research agenda. PLoS Neglect Trop Dis 1(3):e32. doi:10.1371/journal.pntd.0000032 CrossRef

Corachan M, Valls ME, Gascon J, Almeda J, Vilana R (1994) Hematospermia: a new etiology of clinical interest. Am J Trop Med Hyg 50(5):580–584PubMed

Dauda MM, Rafindadi AH (2006) Testicular schistosomiasis simulating malignancy. Tropical doctor 36(3):182–183. doi:10.1258/004947506777978271 CrossRefPubMed

Doehring E, Ehrich JH, Bremer HJ (1986) Reversibility of urinary tract abnormalities due to Schistosoma haematobium infection. Kidney Int 30(4):582–585CrossRefPubMed

Downs JA et al (2011) Urogenital schistosomiasis in women of reproductive age in Tanzania’s Lake Victoria region. Am J Trop Med Hyg 84(3):364–369. doi:10.4269/ajtmh.2011.10-0585 PubMedCentralCrossRefPubMed

Durand F, Brion JP, Terrier N, Pinel C, Pelloux H (2004) Funiculitis due to Schistosoma haematobium: uncommon diagnosis using parasitologic analysis of semen. Am J Trop Med Hyg 70(1):46–47PubMed

Edington GM, Nwabuebo I, Junaid TA (1975) The pathology of schistosomiasis in Ibadan, Nigeria with special reference to the appendix, brain, pancreas and genital organs. Trans R Soc Trop Med Hyg 69(1):153–156CrossRefPubMed

Elem B, Patil PS (1987) Haemospermia: observations in an area of endemic bilharziasis. Br J Urol 60(2):170–173CrossRefPubMed

Fataar S, Rudwan M, Bassiony H, Satyanath S (1990) CT of genitourinary calcification due to schistosomiasis. Australas Radiol 34(3):234–237CrossRefPubMed

Feldmeier H, Poggensee G (1993) Diagnostic techniques in schistosomiasis control: a review. Acta Trop 52(4):205–220CrossRefPubMed

Feldmeier H, Leutscher P, Poggensee G, Harms G (1999) Male genital schistosomiasis and haemospermia. Trop Med Int Health TM IH 4(12):791–793CrossRefPubMed

Fincham JE, Markus MB, Mansvelt EP (1999) Could non-selective anthelmintic treatment programmes contribute to control of the spread of HIV infection and AIDS? Trans R Soc Trop Med Hyg 93(5):536CrossRefPubMed

Gelfand M, Ross CM, Blair DM, Castle WM, Weber MC (1970) Schistosomiasis of the male pelvic organs. Severity of infection as determined by digestion of tissue and histologic methods in 300 cadavers. Am J Trop Med Hyg 19(5):779–784PubMed

Gelfand M, Ross MD, Blair DM, Weber MC (1971) Distribution and extent of schistosomiasis in female pelvic organs, with special reference to the genital tract, as determined at autopsy. Am J Trop Med Hyg 20(6):846–849PubMed

Ghoneim MA (2002) Bilharziasis of the genitourinary tract. BJU Int 89(Suppl 1):22–30CrossRefPubMed

Hawary A, Taylor R, McEwans A, Napier-Hemy R (2012) Change of semen quality after foreign travel: a rare presentation of genital schistosomiasis. Int Urol Nephrol 44(1):51–53. doi:10.1007/s11255-010-9816-6 CrossRefPubMed

Hayes R, Watson-Jones D, Celum C, van de Wijgert J, Wasserheit J (2010) Treatment of sexually transmitted infections for HIV prevention: end of the road or new beginning? AIDS Lond Eng 24(Suppl 4):S15–S26. doi:10.1097/01.aids.0000390704.35642.47 CrossRef

Ibisomi L, Mudege NN (2014) Childlessness in Nigeria: perceptions and acceptability. Cult Health Sex 16(1):61–75. doi:10.1080/13691058.2013.839828 CrossRefPubMed

Inyang-Etoh PC, Ejezie GC, Useh MF, Inyang-Etoh EC (2009) Efficacy of a combination of praziquantel and artesunate in the treatment of urinary schistosomiasis in Nigeria. Trans R Soc Trop Med Hyg 103(1):38–44. doi:10.1016/j.trstmh.2008.08.002 CrossRefPubMed

Jorulf H, Lindstedt E (1985) Urogenital schistosomiasis: CT evaluation. Radiology 157(3):745–749. doi:10.1148/radiology.157.3.3933048 CrossRefPubMed

Jourdan PM, Holmen SD, Gundersen SG, Roald B, Kjetland EF (2011a) HIV target cells in Schistosoma haematobium-infected female genital mucosa. Am J Trop Med Hyg 85(6):1060–1064. doi:10.4269/ajtmh.2011.11-0135 PubMedCentralCrossRefPubMed

Jourdan PM, Roald B, Poggensee G, Gundersen SG, Kjetland EF (2011b) Increased vascularity in cervicovaginal mucosa with Schistosoma haematobium infection. PLoS Neglect Trop Dis 5(6):e1170. doi:10.1371/journal.pntd.0001170 CrossRef

Kallestrup P et al (2005) Schistosomiasis and HIV-1 infection in rural Zimbabwe: effect of treatment of schistosomiasis on CD4 cell count and plasma HIV-1 RNA load. J Infect Dis 192(11):1956–1961. doi:10.1086/497696 CrossRefPubMed

Kaul R et al (2008) The genital tract immune milieu: an important determinant of HIV susceptibility and secondary transmission. J Reprod Immunol 77(1):32–40. doi:10.1016/j.jri.2007.02.002 CrossRefPubMed

Khafagy H, Khalil HM (1970) The schistosomal circumoval precipitin test in cases of chronic prostatitis. Trans R Soc Trop Med Hyg 64(6):909–911CrossRefPubMed

Kini S, Dayoub N, Raja A, Pickering S, Thong J (2009) Schistosomiasis-induced male infertility. BMJ Case Rep. doi:10.1136/bcr.01.2009.1481

Kjetland EF et al (1996) Female genital schistosomiasis due to Schistosoma haematobium. Clinical and parasitological findings in women in rural Malawi. Acta Trop 62(4):239–255CrossRefPubMed

Kjetland EF et al (2005) Simple clinical manifestations of genital Schistosoma haematobium infection in rural Zimbabwean women. Am J Trop Med Hyg 72(3):311–319PubMed

Kjetland EF et al (2006) Association between genital schistosomiasis and HIV in rural Zimbabwean women. AIDS Lond Eng 20(4):593–600. doi:10.1097/01.aids.0000210614.45212.0a CrossRef

Kjetland EF et al (2010) The first community-based report on the effect of genital Schistosoma haematobium infection on female fertility. Fertil Steril 94(4):1551–1553. doi:10.1016/j.fertnstert.2009.12.050 CrossRefPubMed

Kjetland EF, Leutscher PD, Ndhlovu PD (2012) A review of female genital schistosomiasis. Trends Parasitol 28(2):58–65. doi:10.1016/j.pt.2011.10.008 CrossRefPubMed

Kjetland EF, Hegertun IE, Baay MF, Onsrud M, Ndhlovu PD, Taylor M (2014a) Genital schistosomiasis and its unacknowledged role on HIV transmission in the STD intervention studies. Int J STD AIDS 25(10):705–715. doi:10.1177/0956462414523743 CrossRefPubMed

Kjetland EF et al (2014b) Classification of the lesions observed in female genital schistosomiasis. Int J Gynaecol Obstet Off Organ Int Fed Gynaecol Obstet 127(3):227–228. doi:10.1016/j.ijgo.2014.07.014 CrossRef

Knopp S, Becker SL, Ingram KJ, Keiser J, Utzinger J (2013) Diagnosis and treatment of schistosomiasis in children in the era of intensified control. Expert Rev Anti Infect Therapy 11(11):1237–1258. doi:10.1586/14787210.2013.844066 CrossRef

Kramer CV, Zhang F, Sinclair D, Olliaro PL (2014) Drugs for treating urinary schistosomiasis. Cochrane Database Sys Rev 8:CD000053. doi:10.1002/14651858.CD000053.pub3

Lembeli CM, Venkataramaiah NR (1981) Schistosoma haematobium ova in semen. J Urol 125(4):603PubMed

Leutscher P, Ramarokoto CE, Reimert C, Feldmeier H, Esterre P, Vennervald BJ (2000) Community-based study of genital schistosomiasis in men from Madagascar. Lancet 355(9198):117–118. doi:10.1016/s0140-6736(99)04856-4 CrossRefPubMed

Leutscher PD et al (2005) Increased prevalence of leukocytes and elevated cytokine levels in semen from Schistosoma haematobium-infected individuals. J Infect Dis 191(10):1639–1647. doi:10.1086/429334 CrossRefPubMed

Leutscher PD, van Dam GT, Reimert CM, Ramarakoto CE, Deelder AM, Ornbjerg N (2008) Eosinophil cationic protein, soluble egg antigen, circulating anodic antigen, and egg excretion in male urogenital schistosomiasis. Am J Trop Med Hyg 79(3):422–426PubMed

Leutscher PD, Host E, Reimert CM (2009) Semen quality in Schistosoma haematobium infected men in Madagascar. Acta Trop 109(1):41–44. doi:10.1016/j.actatropica.2008.09.010 CrossRefPubMed

Logan S et al (2013) Acute schistosomiasis in travelers: 14 years’ experience at the Hospital for Tropical Diseases, London. Am J Trop Med Hyg 88(6):1032–1034. doi:10.4269/ajtmh.12-0646 PubMedCentralCrossRefPubMed

Lucey DR, Dorsky DI, Nicholson-Weller A, Weller PF (1989) Human eosinophils express CD4 protein and bind human immunodeficiency virus 1 gp120. J Exp Med 169(1):327–332CrossRefPubMed

Mbabazi PS, Andan O, Fitzgerald DW, Chitsulo L, Engels D, Downs JA (2011) Examining the relationship between urogenital schistosomiasis and HIV infection. PLoS Neglect Trop Dis 5(12):e1396. doi:10.1371/journal.pntd.0001396 CrossRef

McKenna G, Schousboe M, Paltridge G (1997) Subjective change in ejaculate as symptom of infection with Schistosoma haematobium in travellers. BMJ Clin Res Ed 315(7114):1000–1001CrossRef

Ming-Chai C, Chi-Yuan C, Pei-Yu C, Jen-Chun H (1980) Evolution of colorectal cancer in schistsosomiasis: transitional mucosal changes adjacent to large intestinal carcinoma in colectomy specimens. Cancer 46(7):1661–1675CrossRefPubMed

Mohammed AZ, Edino ST, Samaila AA (2007) Surgical pathology of schistosomiasis. J Natl Med Assoc 99(5):570–574PubMedCentralPubMed

Moss GB et al (1995) Human immunodeficiency virus DNA in urethral secretions in men: association with gonococcal urethritis and CD4 cell depletion. J Infect Dis 172(6):1469–1474CrossRefPubMed

Mwanakasale V, Vounatsou P, Sukwa TY, Ziba M, Ernest A, Tanner M (2003) Interactions between Schistosoma haematobium and human immunodeficiency virus type 1: the effects of coinfection on treatment outcomes in rural Zambia. Am J Trop Med Hyg 69(4):420–428PubMed

Ndeffo Mbah ML et al (2013a) Cost-effectiveness of a community-based intervention for reducing the transmission of Schistosoma haematobium and HIV in Africa. Proc Natl Acad Sci USA 110(19):7952–7957. doi:10.1073/pnas.1221396110 PubMedCentralCrossRefPubMed

Ndeffo Mbah ML, Poolman EM, Drain PK, Coffee MP, van der Werf MJ, Galvani AP (2013b) HIV and Schistosoma haematobium prevalences correlate in sub-Saharan Africa. Trop Med Int Health TM IH 18(10):1174–1179. doi:10.1111/tmi.12165 CrossRefPubMed

Norseth HM et al (2014) The colposcopic atlas of schistosomiasis in the lower female genital tract based on studies in Malawi, Zimbabwe, Madagascar and South Africa. PLoS Neglect Trop Dis 8(11):e3229. doi:10.1371/journal.pntd.0003229 CrossRef

Obel N, Black FT (1994) Microscopic examination of sperm as the diagnostic clue in a case of Schistosoma haematobium infection. Scand J Infect Dis 26(1):117–118CrossRefPubMed

Ochodo EA et al (2015) Circulating antigen tests and urine reagent strips for diagnosis of active schistosomiasis in endemic areas. Cochrane Database System Rev 3:CD009579. doi:10.1002/14651858.CD009579.pub2

Ogunbanjo BO, Osoba AO, Ochei J (1989) Infective factors of male infertility among Nigerians. Afr J Med Med Sci 18(1):35–38PubMed

Omer EF (1985) Inflammatory conditions and semen quality among subfertile Sudanese males. Trop Doct 15(1):27–28PubMed

Patil PS, Elem B (1988) Schistosomiasis of the prostate and the seminal vesicles: observations in Zambia. J Trop Med Hyg 91(5):245–248PubMed

Perignon A, Pelicot M, Consigny PH (2007) Genital schistosomiasis in a traveler coming back from Mali. J Travel Med 14(3):197–199. doi:10.1111/j.1708-8305.2007.00124.x CrossRefPubMed

Poggensee G, Feldmeier H (2001) Female genital schistosomiasis: facts and hypotheses. Acta Trop 79(3):193–210CrossRefPubMed

Poggensee G, Kiwelu I, Saria M, Richter J, Krantz I, Feldmeier H (1998) Schistosomiasis of the lower reproductive tract without egg excretion in urine. Am J Trop Med Hyg 59(5):782–783PubMed

Poggensee G, Feldmeier H, Krantz I (1999) Schistosomiasis of the female genital tract: public health aspects. Parasitol Today Personal Ed 15(9):378–381CrossRef

Politch JA et al (2012) Highly active antiretroviral therapy does not completely suppress HIV in semen of sexually active HIV-infected men who have sex with men. AIDS Lond Eng 26(12):1535–1543. doi:10.1097/QAD.0b013e328353b11b CrossRef

Price MA et al (2003) Addition of treatment for trichomoniasis to syndromic management of urethritis in Malawi: a randomized clinical trial. Sex Transm Dis 30(6):516–522CrossRefPubMed

Rambau PF, Chandika A, Chalya PL, Jackson K (2011) Scrotal swelling and testicular atrophy due to schistosomiasis in a 9-Year-Old Boy: a case report. Case Rep Infect Dis 2011:787961. doi:10.1155/2011/787961 PubMedCentralPubMed

Renaud G, Devidas A, Develoux M, Lamothe F, Bianchi G (1989) Prevalence of vaginal schistosomiasis caused by Schistosoma haematobium in an endemic village in Niger. Trans R Soc Trop Med Hyg 83(6):797CrossRefPubMed

Richter J (2000) Evolution of schistosomiasis-induced pathology after therapy and interruption of exposure to schistosomes: a review of ultrasonographic studies. Acta Trop 77(1):111–131CrossRefPubMed

Rollinson D (2009) A wake up call for urinary schistosomiasis: reconciling research effort with public health importance. Parasitology 136(12):1593–1610. doi:10.1017/S0031182009990552 CrossRefPubMed

Sadiq ST et al (2002) The effects of antiretroviral therapy on HIV-1 RNA loads in seminal plasma in HIV-positive patients with and without urethritis. AIDS Lond Eng 16(2):219–225CrossRef

Sadiq ST et al (2005) The effects of urethritis on seminal plasma HIV-1 RNA loads in homosexual men not receiving antiretroviral therapy. Sex Transm Infect 81(2):120–123. doi:10.1136/sti.2004.010249 PubMedCentralCrossRefPubMed

Secor WE (2012) The effects of schistosomiasis on HIV/AIDS infection, progression and transmission. Cur Opinion HIV AIDS 7(3):254–259. doi:10.1097/COH.0b013e328351b9e3 CrossRef

Shebel HM, Elsayes KM, El Abou AHM, Elguindy YM, El-Diasty TA (2012) Genitourinary schistosomiasis: life cycle and radiologic-pathologic findings. Radiogr A Rev Radiol Soc North Am 32(4):1031–1046. doi:10.1148/rg.324115162

Silva IM et al (2005) Therapeutic failure of praziquantel in the treatment of Schistosoma haematobium infection in Brazilians returning from Africa. Mem Inst Oswaldo Cruz 100(4):445–449. doi:10.1590/S0074-02762005000400018 CrossRefPubMed

Smith JH, Kamel IA, Elwi A, Von Lichtenberg F (1974) A quantitative post mortem analysis of urinary schistosomiasis in Egypt. I. Pathology and pathogenesis. Am J Trop Med Hyg 23(6):1054–1071PubMed

Stroup DF et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283(15):2008–2012CrossRefPubMed

Ugwu EO, Odoh GU, Obi SN, Ezugwu FO (2014) Acceptability of artificial donor insemination among infertile couples in Enugu, southeastern Nigeria. Int J Women’s Health 6:201–205. doi:10.2147/IJWH.S56324 CrossRef

van Delft F, Visser L, Polderman A, van Lieshout L (2007) Cough and alterations in semen after a tropical swim. Neth J Med 65(8):304–306PubMed

Vennervald BJ, Dunne DW (2004) Morbidity in schistosomiasis: an update. Cur Opinion Infect Dis 17(5):439–447CrossRef

Venz S, Ruckner R (1992) An advanced stage of a bilharziasis infection in CT diagnosis. RoFo Fortschritte auf dem Gebiete der Rontgenstrahlen und der Nuklearmedizin 157(5):530. doi:10.1055/s-2008-1033057 CrossRefPubMed

Vilana R, Corachan M, Gascon J, Valls E, Bru C (1997) Schistosomiasis of the male genital tract: transrectal sonographic findings. J Urol 158(4):1491–1493CrossRefPubMed

Wolff H, Anderson DJ (1988) Male genital tract inflammation associated with increased numbers of potential human immunodeficiency virus host cells in semen. Andrologia 20(5):404–410CrossRefPubMed

Zwang J, Olliaro PL (2014) Clinical efficacy and tolerability of praziquantel for intestinal and urinary schistosomiasis-a meta-analysis of comparative and non-comparative clinical trials. PLoS Neglect Trop Dis 8(11):e3286. doi:10.1371/journal.pntd.0003286 CrossRef

Title: Considering treatment of male genital schistosomiasis as a tool for future HIV prevention: a systematic review
Authors: Chalotte Willemann Stecher
Per Kallestrup
Eyrun Floerecke Kjetland
Birgitte Vennervald
Eskild Petersen
Publication date: 01-11-2015
Publisher: Springer Basel
Published in: International Journal of Public Health / Issue 7/2015
Print ISSN: 1661-8556
Electronic ISSN: 1661-8564
DOI: https://doi.org/10.1007/s00038-015-0714-7

At a glance: The STEP trials

Springer Medicine

Considering treatment of male genital schistosomiasis as a tool for future HIV prevention: a systematic review

Abstract

Objectives

Methods

Results

Conclusions

Systematic review registration number

At a glance: The STEP trials

Springer Medicine

Abstract

Objectives

Methods

Results

Conclusions

Systematic review registration number

Please log in to get access to this content

Other articles of this Issue 7/2015

Comparing Israeli and Palestinian polio vaccination policies and the challenges of silent entry of wild poliovirus in 2013–14: a ‘natural experiment’

Climate change: an opportunity for health promotion practitioners?

The mental health impact of bed bug infestations: a scoping review

Hepatitis C in key populations in Latin America and the Caribbean: systematic review and meta-analysis

Socioeconomic position during childhood and physical activity during adulthood: a systematic review

Global health and environmental pollution