Skip to main content Accessibility help
×
Home

How can schistosome circulating antigen assays be best applied for diagnosing male genital schistosomiasis (MGS): an appraisal using exemplar MGS cases from a longitudinal cohort study among fishermen on the south shoreline of Lake Malawi

  • S. A. Kayuni (a1) (a2), P. L. A. M. Corstjens (a3), E. J. LaCourse (a1), K. E. Bartlett (a1), J. Fawcett (a1), A. Shaw (a1), P. Makaula (a4), F. Lampiao (a5), L. Juziwelo (a6), C. J. de Dood (a3), P. T. Hoekstra (a7), J. J. Verweij (a8), P. D. C. Leutscher (a9), G. J. van Dam (a7), L. van Lieshout (a7) and J. R. Stothard (a1)...

Abstract

We provide an update on diagnostic methods for the detection of urogenital schistosomiasis (UGS) in men and highlight that satisfactory urine-antigen diagnostics for UGS lag much behind that for intestinal schistosomiasis, where application of a urine-based point-of-care strip assay, the circulating cathodic antigen (CCA) test, is now advocated. Making specific reference to male genital schistosomiasis (MGS), we place greater emphasis on parasitological detection methods and clinical assessment of internal genitalia with ultrasonography. Unlike the advances made in defining a clinical standard protocol for female genital schistosomiasis, MGS remains inadequately defined. Whilst urine filtration with microscopic examination for ova of Schistosoma haematobium is a convenient but error-prone proxy of MGS, we describe a novel low-cost sampling and direct visualization method for the enumeration of ova in semen. Using exemplar clinical cases of MGS from our longitudinal cohort study among fishermen along the shoreline of Lake Malawi, the portfolio of diagnostic needs is appraised including: the use of symptomatology questionnaires, urine analysis (egg count and CCA measurement), semen analysis (egg count, circulating anodic antigen measurement and real-time polymerase chain reaction analysis) alongside clinical assessment with portable ultrasonography.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      How can schistosome circulating antigen assays be best applied for diagnosing male genital schistosomiasis (MGS): an appraisal using exemplar MGS cases from a longitudinal cohort study among fishermen on the south shoreline of Lake Malawi
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      How can schistosome circulating antigen assays be best applied for diagnosing male genital schistosomiasis (MGS): an appraisal using exemplar MGS cases from a longitudinal cohort study among fishermen on the south shoreline of Lake Malawi
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      How can schistosome circulating antigen assays be best applied for diagnosing male genital schistosomiasis (MGS): an appraisal using exemplar MGS cases from a longitudinal cohort study among fishermen on the south shoreline of Lake Malawi
      Available formats
      ×

Copyright

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

Author for correspondence: S. A. Kayuni, E-mail: seke.kayuni@lstmed.ac.uk

References

Hide All
Alharbi, MH, Condemine, C, Christiansen, R, LaCourse, EJ, Makaula, P, Stanton, MC, Juziwelo, L, Kayuni, S and Stothard, JR (2019) Biomphalaria pfeifferi snails and intestinal schistosomiasis, Lake Malawi, Africa, 2017–2018. Emerging Infectious Disease 25, 613615. Available at http://wwwnc.cdc.gov/eid/article/25/3/18-1601.
Ashton, RA, Stewart, BT, Petty, N, Lado, M, Finn, T, Brooker, S and Kolaczinski, JH (2011) Accuracy of circulating cathodic antigen tests for rapid mapping of Schistosoma mansoni and S. haematobium infections in Southern Sudan. Tropical Medicine & International Health 16, 10991103.
Ayele, B, Erko, B, Legesse, M, Hailu, A and Medhin, G (2008) Evaluation of circulating cathodic antigen (CCA) strip for diagnosis of urinary schistosomiasis in Hassoba school children, Afar, Ethiopia. Parasite 15, 6975.
Bärenbold, O, Garba, A, Colley, DG, Fleming, FM, Haggag, AA, Ramzy, RMR, Assaré, RK, Tukahebwa, EM, Mbonigaba, JB, Bucumi, V, Kebede, B, Yibi, MS, Meité, A, Coulibaly, JT, N'Goran, EK, Tchuem Tchuenté, L-A, Mwinzi, P, Utzinger, J and Vounatsou, P (2018) Translating preventive chemotherapy prevalence thresholds for Schistosoma mansoni from the Kato-Katz technique into the point-of-care circulating cathodic antigen diagnostic test. PLOS Neglected Tropical Diseases 12, e0006941. Available at https://doi.org/10.1371/journal.pntd.0006941.
Candido, RRF, Morassutti, AL, Graeff-Teixeira, C, St. Pierre, TG and Jones, MK (2018) Chapter six – exploring structural and physical properties of schistosome eggs: potential pathways for novel diagnostics? In Rollinson, D & Stothard, JR (eds), Advances in Parasitology. Elsevier, London, United Kingdom: Academic Press, pp. 209237.
CDC (2014) Epi Info™ 7. Available at https://www.cdc.gov/epiinfo/.
Cheesbrough, M (2009) District Laboratory Practice in Tropical Countries, Part 1, Second Edition Updated. 2nd Edn. The Edinburgh Building, Cambridge, UK: Cambridge University Press.
Christinet, V, Lazdins-Helds, JK, Stothard, JR and Reinhard-Rupp, J (2016) Female genital schistosomiasis (FGS): from case reports to a call for concerted action against this neglected gynaecological disease. International Journal for Parasitology 46, 395404.
Colley, DG, Bustinduy, AL, Secor, WE and King, CH (2014) Human schistosomiasis. Lancet 383, 22532264. (Accessed 2014/7/4/).
Colley, DG, Andros, TS and Campbell, CH Jr (2017) Schistosomiasis is more prevalent than previously thought: what does it mean for public health goals, policies, strategies, guidelines and intervention programs? Infectious Diseases of Poverty 6, 6363. Available at https://www.ncbi.nlm.nih.gov/pmc/PMC5361841/.
Corachan, M, Valls, ME, Gascon, J, Almeda, J and Vilana, R (1994) Hematospermia: a new etiology of clinical interest. American Journal of Tropical Medicine and Hygiene 50, 580584.
Corstjens, PLAM, van Lieshout, L, Zuiderwijk, M, Kornelis, D, Tanke, HJ, Deelder, AM and van Dam, GJ (2008) Up-converting phosphor technology-based lateral flow assay for detection of Schistosoma circulating anodic antigen in serum. Journal of Clinical Microbiology 46, 171176.
Corstjens, PL, De Dood, CJ, Kornelis, D, Fat, EM, Wilson, RA, Kariuki, TM, Nyakundi, RK, Loverde, PT, Abrams, WR, Tanke, HJ, Van Lieshout, L, Deelder, AM and Van Dam, GJ (2014) Tools for diagnosis, monitoring and screening of Schistosoma infections utilizing lateral-flow based assays and upconverting phosphor labels. Parasitology 141, 18411855.
Corstjens, PL, Nyakundi, RK, de Dood, CJ, Kariuki, TM, Ochola, EA, Karanja, DM, Mwinzi, PN and van Dam, GJ (2015) Improved sensitivity of the urine CAA lateral-flow assay for diagnosing active Schistosoma infections by using larger sample volumes. Parasites & Vectors 8, 241.
Corstjens, PLAM, Hoekstra, PT, de Dood, CJ and van Dam, GJ (2017) Utilizing the ultrasensitive Schistosoma up-converting phosphor lateral flow circulating anodic antigen (UCP-LF CAA) assay for sample pooling-strategies. Infectious Diseases of Poverty 6, 155. Available at https://doi.org/10.1186/s40249-017-0368-1.
Dam, GJv and Deelder, AM (1996) Glycoproteins of parasites: Schistosoma glycoconjugates and their role in host-parasite pathological interactions. In Montreuil, J, Vliegenthart, JFG and Schachter, H (eds), New Comprehensive Biochemistry. Amsterdam: Elsevier, pp. 159182.
El-Ghareeb, AS, Abd El Motaleb, GS, Waked, NM, Osman Hany Kamel, N and Aly, NS (2016) Circulating cathodic antigen cassette test versus haematuria strip test in diagnosis of urinary schistosomiasis. Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology 40, 11931198.
Gryseels, B, Polman, K, Clerinx, J and Kestens, L (2006) Human schistosomiasis. Lancet 368, 11061118.
Hokke, CH and van Diepen, A (2017) Helminth glycomics – glycan repertoires and host-parasite interactions. Molecular and Biochemical Parasitology 215, 4757.
Hotez, PJ, Brindley, PJ, Bethony, JM, King, CH, Pearce, EJ and Jacobson, J (2008) Helminth infections: the great neglected tropical diseases. The Journal of Clinical Investigation 118, 13111321.
Kayuni, S, Lampiao, F, Makaula, P, Juziwelo, L, Lacourse, EJ, Reinhard-Rupp, J, Leutscher, PDC and Stothard, JR (2019) A systematic review with epidemiological update of male genital schistosomiasis (MGS): a call for integrated case management across the health system in sub-Saharan Africa. Parasite Epidemiology and Control 4, e00077.
Kenguele, HM, Adegnika, AA, Nkoma, AM, Ateba-Ngoa, U, Mbong, M, Zinsou, J, Lell, B and Verweij, JJ (2014) Impact of short-time urine freezing on the sensitivity of an established Schistosoma real-time PCR assay. American Journal of Tropical Medicine and Hygiene 90, 11531155.
Kipandula, W and Lampiao, F (2015) Semen profiles of young men involved as bicycle taxi cyclists in Mangochi District, Malawi: a case-control study. Malawi Medical Journal 27, 151153. Available at http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4761707/.
Kirkwood, B and Sterne, JA (2006) Essential Medical Statistics. 2nd Edn. Oxford, UK: Blackwell Science Ltd, Blackwell Publishing Company.
Knopp, S, Becker, SL, Ingram, KJ, Keiser, J and Utzinger, J (2013) Diagnosis and treatment of schistosomiasis in children in the era of intensified control. Expert Review of Anti-Infective Therapy 11, 12371258.
Knopp, S, Corstjens, PLAM, Koukounari, A, Cercamondi, CI, Ame, SM, Ali, SM, de Dood, CJ, Mohammed, KA, Utzinger, J, Rollinson, D and van Dam, GJ (2015) Sensitivity and specificity of a urine circulating anodic antigen test for the diagnosis of Schistosoma haematobium in low endemic settings. PLOS Neglected Tropical Diseases 9, e0003752.
Le, L and Hsieh, MH (2017) Diagnosing urogenital schistosomiasis: dealing with diminishing returns. Trends in Parasitology 33, 378387.
Leutscher, P, Ramarokoto, C-E, Reimert, C, Feldmeier, H, Esterre, P and Vennervald, BJ (2000) Community-based study of genital schistosomiasis in men from Madagascar. The Lancet 355, 117118.
Leutscher, PDC, Pedersen, M, Raharisolo, C, Jensen, JS, Hoffmann, S, Lisse, I, Ostrowski, SR, Reimert, CM, Mauclere, P and Ullum, H (2005) Increased prevalence of leukocytes and elevated cytokine levels in semen from Schistosoma haematobium-infected individuals. Journal of Infectious Diseases 191, 16391647. Available at <Go to ISI>://WOS:000228465000009.
Leutscher, PDC, Ramarokoto, CE, Hoffmann, S, Jensen, JS, Ramaniraka, V, Randrianasolo, B, Raharisolo, C, Migliani, R and Christensen, N (2008 a) Coexistence of urogenital schistosomiasis and sexually transmitted infection in women and men living in an area where Schistosoma haematobium is endemic. Clinical Infectious Diseases 47, 775782. Available at <Go to ISI>://WOS:000258570800007.
Leutscher, PDC, van Dam, GTJ, Reimert, CN, Ramarakoto, CE, Deelder, AM and Ornbjerg, N (2008 b) Eosinophil cationic protein, soluble egg antigen, circulating anodic antigen, and egg excretion in male urogenital schistosomiasis. American Journal of Tropical Medicine and Hygiene 79, 422426. Available at <Go to ISI>://WOS:000259307800019.
Madden, FC (1911) Two rare manifestations of bilharziasis. Lancet 178, 754755.
Madsen, H, Bloch, P, Makaula, P, Phiri, H, Furu, P and Stauffer, J (2011) Schistosomiasis in Lake Malaŵi Villages. EcoHealth 8, 163176. Available at https://liverpool.idm.oclc.org/login?url=http://search.ebscohost.com/login.aspx?direct=true&db=eih&AN=71507686&site=eds-live&scope=site.
Makaula, P, Sadalaki, JR, Muula, AS, Kayuni, S, Jemu, S and Bloch, P (2014) Schistosomiasis in Malawi: a systematic review. Parasites & Vectors 7, 20. Available at <Go to ISI>://WOS:000348945500001.
Martino, P, Galosi, AB, Bitelli, M, Consonni, P, Fiorini, F, Granata, A, Gunelli, R, Liguori, G, Palazzo, S, Pavan, N, Scattoni, V and Virgili, G (2014) Practical recommendations for performing ultrasound scanning in the urological and andrological fields. Archivio Italiano di Urologia, Andrologia 86, 5678.
McManus, DP, Dunne, DW, Sacko, M, Utzinger, J, Vennervald, BJ and Zhou, X-N (2018) Schistosomiasis. Nature Reviews Disease Primers 4, 13. Available at https://doi.org/10.1038/s41572-018-0013-8.
Midzi, N, Butterworth, AE, Mduluza, T, Munyati, S, Deelder, AM and van Dam, GJ (2009) Use of circulating cathodic antigen strips for the diagnosis of urinary schistosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 4551.
Midzi, N, Mduluza, T, Mudenge, B, Foldager, L and Leutscher, PDC (2017) Decrease in seminal HIV-1 RNA load after praziquantel treatment of urogenital schistosomiasis coinfection in HIV-positive men – an observational study. Open Forum Infectious Diseases 4, ofx199.Available at http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5695621/.
Minetti, C, Lacourse, EJ, Reimer, L and Stothard, JR (2016) Focusing nucleic acid-based molecular diagnostics and xenomonitoring approaches for human helminthiases amenable to preventive chemotherapy. Parasitology Open 2, e16. Available at https://www.cambridge.org/core/article/focusing-nucleic-acidbased-molecular-diagnostics-and-xenomonitoring-approaches-for-human-helminthiases-amenable-to-preventive-chemotherapy/96FC1B26746FB44767049EF5D4B605C1.
NAC (2015) Malawi AIDS Response Progress Report. Lilongwe, Malawi: Malawi National AIDS Commission. Available at http://www.unaids.org/sites/default/files/country/documents/MWI_narrative_report_2015.pdf.
NSO (2011) Malawi Demographic and Health Survey 2010. Zomba, Malawi and Calverton, Maryland, USA: NSO and ICF Macro. Available at http://www.nsomalawi.mw/images/stories/data_on_line/demography/MDHS2010/MDHS2010%20report.pdf.
NSO (2018) 2018 Malawi Population and Housing Census – Preliminary Report. Zomba, Malawi: National Statistical Office. Available at http://www.nsomalawi.mw/images/stories/data_on_line/demography/census_2018/2018%20Population%20and%20Housing%20Census%20Preliminary%20Report.pdf (Accessed: 21/04/2019).
Obeng, BB, Aryeetey, YA, de Dood, CJ, Amoah, AS, Larbi, IA, Deelder, AM, Yazdanbakhsh, M, Hartgers, FC, Boakye, DA, Verweij, JJ, van Dam, GJ and van Lieshout, L (2008) Application of a circulating-cathodic-antigen (CCA) strip test and real-time PCR, in comparison with microscopy, for the detection of Schistosoma haematobium in urine samples from Ghana. Annals of Tropical Medicine & Parasitology 102, 625633.
Ochodo, EA, Gopalakrishna, G, Spek, B, Reitsma, JB, Lieshout, L, Polman, K, Lamberton, P, Bossuyt, PMM and Leeflang, MMG (2015) Circulating antigen tests and urine reagent strips for diagnosis of active schistosomiasis in endemic areas. Cochrane Database of Systematic Reviews. Article number: CD009579. doi: 10.1002/14651858.CD009579.pub2. Available at http:https://dx.doi.org/10.1002/14651858.CD009579.pub2.
Peters, PA, Mahmoud, AA, Warren, KS, Ouma, JH and Siongok, TK (1976) Field studies of a rapid, accurate means of quantifying Schistosoma haematobium eggs in urine samples. Bulletin of the World Health Organization 54, 159162. Available at https://www.ncbi.nlm.nih.gov/pmc/PMC2366435/.
Poulton, K and Webster, B (2018) Development of a lateral flow recombinase polymerase assay for the diagnosis of Schistosoma mansoni infections. Analytical Biochemistry 546, 6571. Available at http://www.sciencedirect.com/science/article/pii/S0003269718300708.
Ramarakoto, CE, Leutscher, PDC, van Dam, G and Christensen, NO (2008) Ultrasonographical findings in the urogenital organs in women and men infected with Schistosoma haematobium in northern Madagascar. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 767773. Available at <Go to ISI>://WOS:000258201600006.
Rollinson, D, Knopp, S, Levitz, S, Stothard, JR, Tchuem Tchuente, LA, Garba, A, Mohammed, KA, Schur, N, Person, B, Colley, DG and Utzinger, J (2013) Time to set the agenda for schistosomiasis elimination. Acta Tropica 128, 423440.
Ross, AG, Bartley, PB, Sleigh, AC, Olds, GR, Li, Y, Williams, GM and McManus, DP (2002) Schistosomiasis. New England Journal of Medicine 346, 12121220.
Rubaba, O, Chimbari, MJ, Soko, W, Manyangadze, T and Mukaratirwa, S (2018) Validation of a urine circulating cathodic antigen cassette test for detection of Schistosoma haematobium in uMkhanyakude district of South Africa. Acta Tropica 182, 161165.
Sanneh, B, Joof, E, Sanyang, AM, Renneker, K, Camara, Y, Sey, AP, Jagne, S, Baldeh, I, Ceesay, SJ, Sambou, SM and Ogoussan, K (2017) Field evaluation of a schistosome circulating cathodic antigen rapid test kit at point-of-care for mapping of schistosomiasis endemic districts in The Gambia. PLoS One 12, e0182003.
Schwartz, E, Pick, N, Shazberg, G and Potasman, I (2002) Hematospermia due to schistosome infection in travellers: diagnostic and treatment challenges. Clinical Infectious Diseases 35, 14201424. Available at http://dx.doi.org/10.1086/344063.
Squire, B and Stothard, JR (2014) Schistosomiasis. In Beeching, N & Gill, G (eds), Tropical Medicine: Lecture Notes, 7th Edn. Chichester, UK: Wiley-Blackwell, pp. 151162.
Stauffer, JR, Madsen, H and Rollinson, D (2014) Introgression in Lake Malaŵi: increasing the threat of human urogenital schistosomiasis? EcoHealth 11, 251254. Available at http://dx.doi.org/10.1007/s10393-013-0882-y.
Stecher, CW, Kallestrup, P, Kjetland, EF, Vennervald, B and Petersen, E (2015) Considering treatment of male genital schistosomiasis as a tool for future HIV prevention: a systematic review. International Journal of Public Health 60, 839848. Available at http://www.ncbi.nlm.nih.gov/pubmed/26298443.
Stothard, JR, Sousa-Figueiredo, JC, Standley, C, Van Dam, GJ, Knopp, S, Utzinger, J, Ameri, H, Khamis, AN, Khamis, IS, Deelder, AM, Mohammed, KA and Rollinson, D (2009) An evaluation of urine-CCA strip test and fingerprick blood SEA-ELISA for detection of urinary schistosomiasis in schoolchildren in Zanzibar. Acta Tropica 111, 6470. Available at http://www.sciencedirect.com/science/article/pii/S0001706X09000540.
Stothard, JR, Sousa-Figueiredo, JC and Navaratnam, AM (2013) Advocacy, policies and practicalities of preventive chemotherapy campaigns for African children with schistosomiasis. Expert Review of Anti-Infective Therapy 11, 733752.
Stothard, JR, Stanton, MC, Bustinduy, AL, Sousa-Figueiredo, JC, Van Dam, GJ, Betson, M, Waterhouse, D, Ward, S, Allan, F, Hassan, AA, Al-Helal, MA, Memish, ZA and Rollinson, D (2014) Diagnostics for schistosomiasis in Africa and Arabia: a review of present options in control and future needs for elimination. Parasitology 141, 19471961.
Stothard, JR, Campbell, SJ, Osei-Atweneboana, MY, Durant, T, Stanton, MC, Biritwum, N-K, Rollinson, D, Ombede, DRE and Tchuem-Tchuenté, L-A (2017) Towards interruption of schistosomiasis transmission in sub-Saharan Africa: developing an appropriate environmental surveillance framework to guide and to support ‘end game’ interventions. Infectious Diseases of Poverty 6, 10. Available at https://doi.org/10.1186/s40249-016-0215-9.
Teesdale, CH and Chitsulo, L (1985) Schistosomiasis in Malawi – a review. Tropenmedizin Und Parasitologie 36, 16. Available at <Go to ISI>://WOS:A1985AFQ4400001.
Ukwandu, NCD and Nmorsi, OPG (2004) The perception, beliefs and practices toward genitourinary schistosomiasis by inhabitants of selected endemic areas (Edo/Delta States) in south-eastern Nigeria. Revista do Instituto de Medicina Tropical de Sao Paulo 46, 209216. Available at http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0036-46652004000400007&nrm=iso.
UNAIDS (2016) GLOBAL AIDS UPDATE 2016. Geneva, Switzerland: Joint United Nations Programme on HIV/AIDS. Available at http://www.unaids.org/sites/default/files/media_asset/global-AIDS-update-2016_en.pdf (Accessed 1 December 2016).
Utzinger, J, Becker, SL, van Lieshout, L, van Dam, GJ and Knopp, S (2015) New diagnostic tools in schistosomiasis. Clinical Microbiology and Infection 21, 529542.
van Dam, GJ, Seino, J, Rotmans, JP, Daha, MR and Deelder, AM (1993) Schistosoma mansoni circulating anodic antigen but not circulating cathodic antigen interacts with complement component C1q. European Journal of Immunology 23, 28072812.
van Dam, GJ, Claas, FH, Yazdanbakhsh, M, Kruize, YC, van Keulen, AC, Ferreira, ST, Rotmans, JP and Deelder, AM (1996) Schistosoma mansoni excretory circulating cathodic antigen shares Lewis-x epitopes with a human granulocyte surface antigen and evokes host antibodies mediating complement-dependent lysis of granulocytes. Blood 88, 42464251.
van Dam, GJ, Wichers, JH, Ferreira, TMF, Ghati, D, van Amerongen, A and Deelder, AM (2004) Diagnosis of schistosomiasis by reagent strip test for detection of circulating cathodic antigen. Journal of Clinical Microbiology 42, 54585461. Available at https://jcm.asm.org/content/jcm/42/12/5458.full.pdf.
van Delft, F, Visser, L, Polderman, A and van Lieshout, L (2007) Cough and alterations in semen after a tropical swim. Netherlands Journal of Medicine 65, 304306.
van Diepen, A, Van der Velden, NS, Smit, CH, Meevissen, MH and Hokke, CH (2012) Parasite glycans and antibody-mediated immune responses in Schistosoma infection. Parasitology 139, 12191230.
van Lieshout, L, Polderman, AM and Deelder, AM (2000) Immunodiagnosis of schistosomiasis by determination of the circulating antigens CAA and CCA, in particular in individuals with recent or light infections. Acta Tropica 77, 6980. Available at http://www.sciencedirect.com/science/article/pii/S0001706X00001157.
Vilana, R, Corachan, M, Gascon, J, Valls, E and Bru, C (1997) Schistosomiasis of the male genital tract: transrectal sonographic findings. Journal of Urology 158, 14911493.
Webster, BL, Alharbi, MH, Kayuni, S, Makaula, P, Halstead, F, Christiansen, R, Juziwelo, L, Stanton, MC, LaCourse, EJ, Rollinson, D, Kalua, K and Stothard, JR (2019) Schistosome interactions within the Schistosoma haematobium group, Malawi. Emerging Infectious Disease Journal 25. 12451247. Available at https://wwwnc.cdc.gov/eid/article/25/6/19-0020_article.
WHO (1991) Basic Laboratory Methods in Medical Parasitology. Geneva, Switzerland: World Health Organization.
WHO (2000) Ultrasound in schistosomiasis: a practical guide to the standard use of ultrasonography for assessment of schistosomiasis-related morbidity: Second International Workshop, 22–26 October 1996, Niamey, Niger.
WHO (2001) WHO. Resolution on Schistosomiasis and soil-transmitted helminth infections. WHA 54.19. Available at http://www.who.int/neglected_diseases/mediacentre/WHA_54.19_Eng.pdf.
WHO (2010) WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th Edn. Geneva, Switzerland: World Health Organization, p. 286.
WHO (2012) WHO. Resolution on Elimination of Schistosomiasis WHA65.21 WHO Neglected Tropical Diseases. Available at http://www.who.int/neglected_diseases/Schistosomiasis_wha65/en/.
WHO (2013) Schistosomiasis: Progress Report 2001–2011, Strategic Plan 2012–2020. Geneva: World Health Organization. Available at www.apps.who.int/iris/bitstream/10665/78074/1/9789241503174_eng.pdf.
WHO (2015) Female Genital Schistosomiasis: A Pocket Atlas for Clinical Health-Care Professionals. Geneva: World Health Organisation.
WHO (2018) Schistosomiasis. Factsheets. Geneva, Switzerland: World Health Organization. Available at http://www.who.int/en/news-room/fact-sheets/detail/schistosomiasis (Accessed 29 December).
Yirenya-Tawiah, DR, Ackumey, MM and Bosompem, KM (2016) Knowledge and awareness of genital involvement and reproductive health consequences of urogenital schistosomiasis in endemic communities in Ghana: a cross-sectional study. Reproductive Health 13, 117. Available at http://dx.doi.org/10.1186/s12978-016-0238-5.

Keywords

How can schistosome circulating antigen assays be best applied for diagnosing male genital schistosomiasis (MGS): an appraisal using exemplar MGS cases from a longitudinal cohort study among fishermen on the south shoreline of Lake Malawi

  • S. A. Kayuni (a1) (a2), P. L. A. M. Corstjens (a3), E. J. LaCourse (a1), K. E. Bartlett (a1), J. Fawcett (a1), A. Shaw (a1), P. Makaula (a4), F. Lampiao (a5), L. Juziwelo (a6), C. J. de Dood (a3), P. T. Hoekstra (a7), J. J. Verweij (a8), P. D. C. Leutscher (a9), G. J. van Dam (a7), L. van Lieshout (a7) and J. R. Stothard (a1)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed