1921
Volume 98, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

It has been postulated that impaired host immunity due to HIV infection reduces parasite egg excretion. /HIV interactions have also been shown to differ by sex. We hypothesized that egg excretion would vary based on both HIV status and sex. We examined data from more than 1,700 participants in eight studies conducted in northwest Tanzania between 2010 and 2016. infection was defined by circulating anodic antigen (CAA) serum levels ≥ 30 pg/mL and/or egg positivity in either stool by Kato Katz method or urine by filtration. We used multivariable analyses to determine the impact of confounding factors such as sex, age, previous praziquantel treatment, and worm burden as measured by serum CAA level, on the relationship between egg excretion and HIV status. HIV-infected individuals were significantly less likely to excrete schistosome eggs than HIV-uninfected individuals, even after controlling for worm burden and sex (OR = 0.6 [0.4, 0.9], = 0.005). Furthermore, after controlling for worm burden and HIV status, women had lower odds of egg excretion than men (OR = 0.4 [0.3, 0.5], < 0.001). Sensitivity of egg microscopy was lower in HIV-infected women than HIV-uninfected men (41% versus 61%, < 0.001), whereas sensitivity in women remained low in both groups (33% versus 37%, = 0.664). Our study is the first to report that women with infection excrete fewer eggs than men for a given worm burden, regardless of HIV the status. These findings suggest that guidelines for use of microscopy to diagnose infections in HIV-infected individuals and in women merit reconsideration.

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References

  1. WHO, 2017. Schistosomiasis Factsheet. Available at: http://www.who.int/mediacentre/factsheets/fs115/en/. Accessed April 15, 2017.
  2. Doehring E, Feldmeier H, Daffalla AA, , 1983. Day-to-day variation and circadian rhythm of egg excretion in urinary schistosomiasis in the Sudan. Ann Trop Med Parasitol 77: 587594. [Google Scholar]
  3. Birrie H, Medhin G, Erko B, , 1994. Variability of egg excretion in Schistosoma mansoni infection in Ethiopia: a case report. East Afr Med J 71: 545547. [Google Scholar]
  4. Agnew A, 1996. Age-dependent reduction of schistosome fecundity in Schistosoma haematobium but not Schistosoma mansoni infections in humans. Am J Trop Med Hyg 55: 338343. [Google Scholar]
  5. Bethony J, 2002. Additive host genetic factors influence fecal egg excretion rates during Schistosoma mansoni infection in a rural area in Brazil. Am J Trop Med Hyg 67: 336343. [Google Scholar]
  6. De Vlas SJ, Gryseels B, Van Oortmarssen GJ, Polderman AM, Habbema JDF, , 1993. A pocket chart to estimate true Schistosoma mansoni prevalences. Parasitol Today 9: 306307. [Google Scholar]
  7. Van Lieshout L, Polderman AM, 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 Trop 77: 6980. [Google Scholar]
  8. Doenhoff MJ, Chiodini PL, Hamilton JV, , 2004. Specific and sensitive diagnosis of schistosome infection: can it be done with antibodies? Trends Parasitol 20: 3539. [Google Scholar]
  9. Corstjens PL, van Lieshout L, Zuiderwijk M, Kornelis D, Tanke HJ, Deelder AM, van Dam GJ, , 2008. Up-converting phosphor technology-based lateral flow assay for detection of Schistosoma circulating anodic antigen in serum. J Clin Microbiol 46: 171176. [Google Scholar]
  10. Corstjens PL, 2014. Tools for diagnosis, monitoring and screening of Schistosoma infections utilizing lateral-flow based assays and upconverting phosphor labels. Parasitol 141: 18411855. [Google Scholar]
  11. Corstjens PL, Nyakundi RK, de Dood CJ, Kariuki TM, Ochola EA, Karanja DM, Mwinzi PNM, van Dam GJ, , 2015. Improved sensitivity of the urine CAA lateral-flow assay for diagnosing active Schistosoma infections by using larger sample volumes. Parasit Vectors 8: 241. [Google Scholar]
  12. Wilson AR, van Dam GJ, Kariuki TM, Farah IO, Deelder AM, Coulson PS, , 2006. The detection limits for estimates of infection intensity in schistosomiasis mansoni established by a study in non-human primates. Int J Parasitol 36: 12411244. [Google Scholar]
  13. Utzinger J, Becker SL, van Lieshout L, van Dam GJ, Knopp S, , 2015. New diagnostic tools in schistosomiasis. Clin Microbiol Infect 21: 529542. [Google Scholar]
  14. De Clercq D, Sacko M, Vercruysse J, Diarra A, Landoure A, vanden Bussche V, Gryseels B, Deelder A, , 1995. Comparison of the circulating anodic antigen detection assay and urine filtration to diagnose Schistosoma haematobium infections in Mali. Trans R Soc Trop Med Hyg 89: 395397. [Google Scholar]
  15. Van Lieshout L, Polman K, Gryseels B, Deelder AM, , 1998. Circulating anodic antigen levels in two areas endemic for schistosomiasis mansoni indicate differences in worm fecundity. Trans R Soc Trop Med Hyg 92: 115119. [Google Scholar]
  16. Cai YC, 2014. Field comparison of circulating antibody assays versus circulating antigen assays for the detection of schistosomiasis japonica in endemic areas of China. Parasit Vectors 7: 138. [Google Scholar]
  17. Knopp S, 2015. Sensitivity and specificity of a urine circulating anodic antigen test for the diagnosis of Schistosoma haematobium in low endemic settings. PLoS Negl Trop Dis 9: e0003752. [Google Scholar]
  18. van Dam GJ, 2015. An ultra-sensitive assay targeting the circulating anodic antigen for the diagnosis of Schistosoma japonicum in a low-endemic area, People’s Republic of China. Acta Trop 141: 190197. [Google Scholar]
  19. Balahbib A, 2017. Selecting accurate post-elimination monitoring tools to prevent reemergence of urogenital schistosomiasis in Morocco: a pilot study. Infect Dis Poverty 6: 75. [Google Scholar]
  20. Vonghachack Y, 2017. Comparison of novel and standarddiagnostic tools for the detection of Schistosoma mekongi infection in Lao People’s Democratic Republic and Cambodia. Infect Dis Poverty 6: 127. [Google Scholar]
  21. Doenhoff MJ, Hassounah OA, Lucas SB, , 1985. Does the immunopathology induced by schistosome eggs potentiate parasite survival? Immunol Today 6: 203206. [Google Scholar]
  22. Karanja DM, Colley DG, Nahlen BL, Ouma JH, Secor WE, , 1997. Studies on schistosomiasis in western Kenya: I. Evidence for immune-facilitated excretion of schistosome eggs from patients with Schistosoma mansoni and human immunodeficiency virus coinfections. Am J Trop Med Hyg 56: 515521. [Google Scholar]
  23. Muok EM, Simiyu EW, Ochola EA, Ng’ang’a ZW, Secor WE, Karanja DM, Mwinzi PM, , 2013. Association between CD4+ T-lymphocyte counts and fecal excretion of Schistosoma mansoni eggs in patients coinfected with S. mansoni and human immunodeficiency virus before and after initiation of antiretroviral therapy. Am J Trop Med Hyg 89: 4245. [Google Scholar]
  24. 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: 420428. [Google Scholar]
  25. Sanya RE, Muhangi L, Nampijja M, Nannozi V, Nakawungu PK, Abayo E, Webb EL, Elliott AM, , 2015. Schistosoma mansoni and HIV infection in a Ugandan population with high HIV and helminth prevalence. Trop Med Int Health 20: 12011208. [Google Scholar]
  26. Fontanet AL, Woldemichael T, Sahlu T, van Dam GJ, Messele T, Rinke de Wit T, Masho W, Yeneneh H, Coutinho RA, van Lieshout L, , 2000. Epidemiology of HIV and Schistosoma mansoni infections among sugar-estate residents in Ethiopia. Ann Trop Med Parasitol 94: 145155. [Google Scholar]
  27. Kleppa E, Klinge KF, Galaphaththi-Arachchige HN, Holmen SD, Lillebo K, Onsrud M, Gundersen SG, Taylor M, Ndhlovu P, Kjetland EF, , 2015. Schistosoma haematobium infection and CD4+ T-cell levels: a cross-sectional study of young South African women. PLoS One 10: e0119326. [Google Scholar]
  28. Kallestrup P, Zinyama R, Gomo E, Butterworth AE, van Dam GJ, Erikstrup C, Ullum H, , 2005. Schistosomiasis and HIV-1 infection in rural Zimbabwe: implications of coinfection for excretion of eggs. J Infect Dis 191: 13111320. [Google Scholar]
  29. Mazigo HD, Dunne DW, Wilson S, Kinung’hi SM, Pinot de Moira A, Jones FM, Morona D, Nuwaha F, , 2014. Co-infection with Schistosoma mansoni and human immunodeficiency virus-1 (HIV-1) among residents of fishing villages of north-western Tanzania. Parasit Vectors 7: 587. [Google Scholar]
  30. Ssetaala A, 2015. Schistosoma mansoni and HIV acquisition in fishing communities of Lake Victoria, Uganda: a nested case–control study. Trop Med Int Health 20: 11901195. [Google Scholar]
  31. Downs JA, 2012. Association of schistosomiasis and HIV infection in Tanzania. Am J Trop Med Hyg 87: 868873. [Google Scholar]
  32. Downs JA, 2017. Schistosomiasis and human immunodeficiency virus in men in Tanzania. Am J Trop Med Hyg 96: 856862. [Google Scholar]
  33. van Dam GJ, Claudia J, Lewis M, Deelder AM, van Lieshout L, Tanke HJ, van Rooyen LH, Corstjens PL, , 2013. A robust dry reagent lateral flow assay for diagnosis of active schistosomiasis by detection of Schistosoma circulating anodic antigen. Exp Parasitol 135: 274282. [Google Scholar]
  34. Ndyomugyenyi R, Minjas JN, , 2001. Urinary schistosomiasis in schoolchildren in Dar-es-Salaam, Tanzania, and the factors influencing its transmission. Ann Trop Med Parasitol 95: 697706. [Google Scholar]
  35. Delmas M-C, Jadand C, De Vincenzi I, Deveau C, Persoz A, Sobel A, Kazatchkine M, Brunet JB, Meyer L, , 1997. Gender differences in CD4+ cell counts persist after HIV-1 infection. AIDS 11: 10711073. [Google Scholar]
  36. Loupa CV, Rodriguez B, McComsey G, Gripshover B, Salata RA, Valdez H, Lisgaris MV, Fulton SA, Lederman MM, , 2006. Gender differences in human immunodeficiency virus (HIV) RNA and CD4 cell counts among new entrants to HIV care. Clin Microbiol Infect 12: 389391. [Google Scholar]
  37. Cheever AW, Kamel IA, Elwi AM, Mosimann JE, Danner R, , 1977. Schistosoma mansoni and S. haematobium infections in Egypt. Am J Trop Med Hyg 26: 702716. [Google Scholar]
  38. Wilson S, Jones FM, van Dam GJ, Corstjens PL, Riveau G, Fitzsimmons CM, Sacko MBJ, Vennervald BJ, Dunne DW, , 2014. Human Schistosoma haematobium antifecundity immunity is dependent on transmission intensity and associated with immunoglobulin G1 to worm-derived antigens. J Infect Dis 210: 20092016. [Google Scholar]
  39. Stete K, Krauth SJ, Coulibaly JT, Knopp S, Hattendorf J, Müller I, Lohourignon LK, Kern WV, N’Goran EK, Utzinger J, , 2012. Dynamics of Schistosoma haematobium egg output and associated infection parameters following treatment with praziquantel in school-aged children. Parasit Vectors 5: 298. [Google Scholar]
  40. Kallestrup P, Zinyama R, Gomo E, Butterworth AE, van Dam GJ, Gerstoft J, Erikstrup C, Ullum H, , 2006. Schistosomiasis and HIV in rural Zimbabwe: efficacy of treatment of schistosomiasis in individuals with HIV coinfection. Clin Infect Dis 42: 17811789. [Google Scholar]
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  • Received : 09 Oct 2017
  • Accepted : 15 Dec 2017
  • Published online : 05 Feb 2018

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