Genetic Diversity of Schistosoma haematobium in Sub-Saharan Africa: A Systematic Review
Keywords:
Urogenital schistosomiasis, Schistosoma haematobium, sub-Saharan Africa, Genetic Diversity, Systematic Review
Abstract
Urogenital schistosomiasis caused by the parasite Schistosoma haematobium is the most common form of schistosomiasis. This parasite has a high potential for genetic exchange within parasite populations giving rise to the genetic diversity that is important for its survival. Genetic differences may lead to some parasite strains being more immunogenic which may have a negative impact on management and control of schistosomiasis. Therefore, understanding these genetic differences in the parasite may lead to better management of the disease. The aim of this review was to systematically review scientific literature on the genetic diversity and population structuring of S. haematobium and the methods used across sub-Saharan African countries. A literature search was done on PubMed, African Journals online and Google scholar using predefined search terms such as urinary schistosomiasis, S. haematobium, genetic diversity in sub-Saharan Africa in combination with Boolean operators (AND, OR). The search included studies published from 2000-2020 that emphasised on genetic diversity of S. haematobium in sub-Saharan Africa. A country in sub-Saharan Africa was included if had a study that determined the genetic diversity of S. haematobium Sixteen study articles from 18 sub-Saharan African countries met the inclusion criteria The genetic diversity of S. haematobium varied from low to high using different methods. Most studies conducted in these countries showed a high genetic diversity of S. haematobium 18/36 (50%) studies. Four methods namely, restriction fragment length polymorphism, randomly amplified polymorphic DNA, DNA barcoding and Microsatellite markers were used to determine diversity In these studies, measures of genetic diversity such as number of alleles per minute or allelic richness, heterozygosity, number of genotypes and unique haplotypes were used. Microsatellites were the most commonly used method and the studies reported number of alleles per locus ranging from 2-19 alleles per locus and heterozygosity of 6 to 71% in some studies. . The highest number of studies were conducted in West Africa Nigeria and Zimbabwe , 4/36(11%) each. Results show the need for continued monitoring of genetic variations in S. haematobium in sub- Saharan Africa. This will aid in understanding the epidemiology of disease, advancing novel treatment and vaccine strategies.References
1. Ismail HA, Hong S, Tag A, Bashir E, Mohamed R, Elgadir A, et al. Prevalence , risk factors , and clinical manifestations of schistosomiasis among school children in the White Nile River basin , Sudan. Parasit Vectors. 2014;7(478):1–11.
2. Quan J-H, ChoiI.-W, H.A.H.A. I, A.S. M, H.-G. J, J.-S. L, et al. Genetic diversity of Schistosoma haematobium eggs isolated from human Urine in Sudan. Korean J Parasitol. 2015;53(3):271–7.
3. Lawiye J., Vandi P V, Godly C, Midala A., Watirahel P, Enamola W. Prevalence and risk factors of Schistosoma haematobium infections among primary school children in Igbokuta Village, Ikorodu North Local Government, Lagos State. IOSR J Nurs Heal Sci. 2020;2(6):62–8.
4. Inobaya MT, Chau TN, Ng SK, MacDougall C, Olveda RM, Tallo VL, et al. Mass drug administration and the sustainable control of schistosomiasis: An evaluation of treatment compliance in the rural Philippines. Parasites and Vectors. 2018;11(1):1–11.
5. Poole H, Terlouw DJ, Naunje A, Mzembe K, Stanton M, Betson M, et al. Schistosomiasis in pre-school-age children and their mothers in Chikhwawa district , Malawi with notes on characterization of schistosomes and snails. Parasit Vectors. 2014;7(1):1–12.
6. Sacolo H, Chimbari M, Kalinda C. Knowledge, attitudes and practices on Schistosomiasis in sub-Saharan Africa: A systematic review. BMC Infect Dis. 2018;18(1).
7. Weerakoon KG. DNA Diagnostics for Schistosomiasis Control. Trop Med Infect Dis. 2018;3(81):1–20.
8. Mcmanus DP, Dunne DW, Sacko M, Zhou N, Vennervald BJ. Schistosomiasis. 2018;1–19.
9. Adenowo AF, Oyinloye BE, Ogunyinka BI, Kappo AP. Impact of human schistosomiasis in sub-Saharan Africa. Brazilian J Infect Dis [Internet]. 2015;19(2):196–205. Available from: http://dx.doi.org/10.1016/j.bjid.2014.11.004
10. Norton AJ, Gower CM, Lamberton PHL, Webster BL, Lwambo NJS, Blair L, et al. Genetic consequences of mass human chemotherapy for Schistosoma mansoni: Population structure pre-and post-praziquantel treatment in Tanzania. Am J Trop Med Hyg. 2010;83(4):951–7.
11. Sady H, Al-Mekhlafi HM, Webster BL, Ngui R, Atroosh WM, Al-Delaimy AK, et al. New insights into the genetic diversity of Schistosoma mansoni and S. haematobiumin Yemen. Parasites and Vectors [Internet]. 2015;8(1):1–14. Available from: http://dx.doi.org/10.1186/s13071-015-1168-8
12. Afifi M, Jiman-Fatani A, Al-Hussainy N, Al-Rabia M, Bogari A. Genetic diversity among natural populations of Schistosoma haematobium might contribute to inconsistent virulence and diverse clinical outcomes. J Microsc Ultrastruct [Internet]. 2016;4(4):222. Available from: http://dx.doi.org/10.1016/j.jmau.2016.04.002
13. Brouwer KC, Ndhlovu PD, Wagatsuma Y, Munatsi A, Shiff CJ. Urinary tract pathology attributed to Schistosoma haematobium: Does parasite genetics play a role? Am J Trop Med Hyg. 2003;68(4):456–62.
14. Ezeh C, Yin M, Li H, Zhang T, Xu B, Sacko M, et al. High genetic variability of Schistosoma haematobium in Mali and Nigeria. Korean J Parasitol. 2015;53(1):129–34.
15. Moendeg KJ, Ma J, Angeles M, Nakao R, Leonardo LR, Kendrich I, et al. Geographic strain differentiation of Schistosoma japonicum in the Philippines using microsatellite markers. 2017 [cited 2019 Apr 10]; Available from: https://doi.org/10.1371/journal.pntd.0005749
16. Kabuyaya M, Chimbari MJ, Manyangadze T, Mukaratirwa S. Efficacy of praziquantel on Schistosoma haematobium and re-infection rates among school-going children in the Ndumo area of uMkhanyakude district , KwaZulu-Natal , South Africa. 2017;1–9.
17. Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis Daniel. Lancet. 2015;383(9936):2253–64.
18. Kura K, Hardwick RJ, Truscott JE, Toor J, Hollingsworth TD, Anderson RM. The impact of mass drug administration on Schistosoma haematobium infection: what is required to achieve morbidity control and elimination? Parasites and Vectors [Internet]. 2020;13(1):1–10. Available from: https://doi.org/10.1186/s13071-020-04409-3
19. Webster BL, Emery AM, Webster JP, Gouvras A, Garba A, Diaw O, et al. Genetic Diversity within Schistosoma haematobium: DNA Barcoding Reveals Two Distinct Groups. PLoS Negl Trop Dis. 2012;6(10).
20. Webster BL, Rabone M, Pennance T, Emery AM, Allan F, Gouvras A, et al. Development of novel multiplex microsatellite polymerase chain reactions to enable high-throughput population genetic studies of Schistosoma haematobium. Parasites and Vectors [Internet]. 2015;8(1):1–5. Available from: http://dx.doi.org/10.1186/s13071-015-1044-6
21. El-Kady AM, EL-Amir MI, Hassan MH, Allemailem KS, Almatroudi A, Ahmad AlA. Genetic Diversity of Schistosoma haematobium in. Infect Drug Resist. 2020;13:3601–11.
22. Rollinson D, Webster JP, Webster B, Nyakaana S, Jrgensen A, Stothard JR. Genetic diversity of schistosomes and snails: Implications for control. Parasitology. 2009;136(13):1801–11.
23. Moher D, Liberati A, Tetzlaff J, Altman DG, Prisma T. Preferred reporting items for systematic reviews and meta-analyses : The PRISMA statement. 2010;8:336–41.
24. Rey O, Webster BL, Huyse T, Rollinson D, Broeck F Van Den, Onyekwere A, et al. Population genetics of African Schistosoma species To cite this version : HAL Id : hal-03128417 Population genetics of African Schistosoma species. 2021;
25. Webster BL, Culverwell CL, Khamis IS, Mohammed KA, Rollinson D, Stothard JR. Acta Tropica DNA barcoding of Schistosoma haematobium on Zanzibar reveals substantial genetic diversity and two major phylogenetic groups. Acta Trop [Internet]. 2012;128(2):206–17. Available from: http://dx.doi.org/10.1016/j.actatropica.2012.06.002
26. Umar S, Shinkafi SH, Hudu SA, Neela V, Suresh K, Nordin SA, et al. Prevalence and molecular characterisation of Schistosoma haematobium among primary school children in Kebbi State, Nigeria. Ann Parasitol [Internet]. 2017;63(2):133–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28822206
27. Glenn TC, Lance SL, Mckee AM, Webster BL, Emery AM, Zerlotini A, et al. Significant variance in genetic diversity among populations of Schistosoma haematobium detected using microsatellite DNA loci from a genome-wide database. Parasit Vectors [Internet]. 2013;6(1):1. Available from: Parasites & Vectors
28. Golan R, Gower CM, Emery AM, Rollinson D, Webster JP. Europe PMC Funders Group Isolation and characterization of the first polymorphic microsatellite markers for Schistosoma haematobium and their application in multiplex reactions of larval stages. 2014;8(3):647–9.
29. Gower CM, Gouvras AN, Lamberton PHL, Deol A, Shrivastava J, Mutombo PN, et al. Population genetic structure of Schistosoma mansoni and Schistosoma haematobium from across six sub-Saharan African countries: Implications for epidemiology, evolution and control. Acta Trop [Internet]. 2013;128(2):261–74. Available from: http://dx.doi.org/10.1016/j.actatropica.2012.09.014
30. Gower CM, Gabrielli AF, Sacko M, Dembelé R, Golan R, Emery AM, et al. Population genetics of Schistosoma haematobium: Development of novel microsatellite markers and their application to schistosomiasis control in Mali. Parasitology. 2011;138(8):978–94.
31. Ezeh C, Yin M, Li H, Zhang T, Xu B, Sacko M, et al. High genetic variability of Schistosoma haematobium in Mali and Nigeria. Korean J Parasitol. 2015;53(1):129–34.
32. Dabo A, Durand P, Morand S, Diakite M. Distribution and genetic diversity of Schistosoma haematobium within its bulinid intermediate hosts in Mali Distribution and genetic diversity of Schistosoma haematobium within its bulinid intermediate hosts in Mali. 1997;(October 2017).
33. Brouwer KC, Ndhlovu P, Munatsi A, Shiff CJ. Genetic Diversity of a Population of Schistosoma haematobium Derived from Schoolchildren in East Central Zimbabwe. J Parasitol. 2001;87(4):762.
34. Gasmelseed N, Karamino NE, Abdelwahed MO, Hamdoun AO, Elmadani AE. Genetic diversity of Schistosoma haematobium parasite IS NOT associated with severity of disease in an endemic area in Sudan. BMC Infect Dis. 2014;14(1):1–8.
35. Shrivastava J, Bao ZQ, Mcvean G, Webster JP. An insight into the genetic variation of Schistosoma japonicum in mainland China using DNA microsatellite markers. Mol Ecol. 2005;14(3):839–49.
36. Gulcher J. Microsatellite markers for linkage and association studies. Cold Spring Harb Protoc. 2012;7(4):425–32.
37. Webster BL, Webster JP, Gouvras AN, Garba A, Lamine MS, Diaw OT, et al. DNA ‘barcoding’ of Schistosoma mansoni across sub-Saharan Africa supports substantial within locality diversity and geographical separation of genotypes. Acta Trop [Internet]. 2013 Nov [cited 2019 Apr 10];128(2):250–60. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22935316
38. Le TH, Blair D, McManus DP. Mitochondrial genomes of human helminths and their use as markers in population genetics and phylogeny. Acta Trop. 2000;77(3):243–56.
39. Shiff C, Brouwer KC, Clow L. Schistosoma haematobium: Population genetics of S. haematobium by direct measurement of parasite diversity using RAPD ± PCR. Exp Parasitol. 2000;96(1):47–51.
40. Curtis J, Sorensen RE, Minchella DJ. Schistosome genetic diversity: The implications of population structure as detected with microsatellite markers. Parasitology. 2002;125(SUPPL.):51–9.
41. Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey S V. DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res. 1990;18(22):6531–5.
42. Barber KE, Mkoji GM, Loker ES. PCR-RFLP analysis of the ITS2 region to identify Schistosoma haematobium and S. Bovis from Kenya. Am J Trop Med Hyg. 2000;62(4):434–40.
43. Aula OP, McManus DP, Jones MK, Gordon CA. Schistosomiasis with a focus on Africa. Trop Med Infect Dis. 2021;6(3):1–40.
44. Onasanya A, Bengtson M, Oladepo O, Van Engelen J, Diehl JC. Rethinking the Top-Down Approach to Schistosomiasis Control and Elimination in Sub-Saharan Africa. Front Public Heal. 2021;9(February):1–6.
45. Webster BL, Rabone M, Pennance T, Emery AM, Allan F, Gouvras A, et al. Development of novel multiplex microsatellite polymerase chain reactions to enable high-throughput population genetic studies of Schistosoma haematobium. Parasites and Vectors [Internet]. 2015;8(1):1–5. Available from: http://dx.doi.org/10.1186/s13071-015-1044-6
2. Quan J-H, ChoiI.-W, H.A.H.A. I, A.S. M, H.-G. J, J.-S. L, et al. Genetic diversity of Schistosoma haematobium eggs isolated from human Urine in Sudan. Korean J Parasitol. 2015;53(3):271–7.
3. Lawiye J., Vandi P V, Godly C, Midala A., Watirahel P, Enamola W. Prevalence and risk factors of Schistosoma haematobium infections among primary school children in Igbokuta Village, Ikorodu North Local Government, Lagos State. IOSR J Nurs Heal Sci. 2020;2(6):62–8.
4. Inobaya MT, Chau TN, Ng SK, MacDougall C, Olveda RM, Tallo VL, et al. Mass drug administration and the sustainable control of schistosomiasis: An evaluation of treatment compliance in the rural Philippines. Parasites and Vectors. 2018;11(1):1–11.
5. Poole H, Terlouw DJ, Naunje A, Mzembe K, Stanton M, Betson M, et al. Schistosomiasis in pre-school-age children and their mothers in Chikhwawa district , Malawi with notes on characterization of schistosomes and snails. Parasit Vectors. 2014;7(1):1–12.
6. Sacolo H, Chimbari M, Kalinda C. Knowledge, attitudes and practices on Schistosomiasis in sub-Saharan Africa: A systematic review. BMC Infect Dis. 2018;18(1).
7. Weerakoon KG. DNA Diagnostics for Schistosomiasis Control. Trop Med Infect Dis. 2018;3(81):1–20.
8. Mcmanus DP, Dunne DW, Sacko M, Zhou N, Vennervald BJ. Schistosomiasis. 2018;1–19.
9. Adenowo AF, Oyinloye BE, Ogunyinka BI, Kappo AP. Impact of human schistosomiasis in sub-Saharan Africa. Brazilian J Infect Dis [Internet]. 2015;19(2):196–205. Available from: http://dx.doi.org/10.1016/j.bjid.2014.11.004
10. Norton AJ, Gower CM, Lamberton PHL, Webster BL, Lwambo NJS, Blair L, et al. Genetic consequences of mass human chemotherapy for Schistosoma mansoni: Population structure pre-and post-praziquantel treatment in Tanzania. Am J Trop Med Hyg. 2010;83(4):951–7.
11. Sady H, Al-Mekhlafi HM, Webster BL, Ngui R, Atroosh WM, Al-Delaimy AK, et al. New insights into the genetic diversity of Schistosoma mansoni and S. haematobiumin Yemen. Parasites and Vectors [Internet]. 2015;8(1):1–14. Available from: http://dx.doi.org/10.1186/s13071-015-1168-8
12. Afifi M, Jiman-Fatani A, Al-Hussainy N, Al-Rabia M, Bogari A. Genetic diversity among natural populations of Schistosoma haematobium might contribute to inconsistent virulence and diverse clinical outcomes. J Microsc Ultrastruct [Internet]. 2016;4(4):222. Available from: http://dx.doi.org/10.1016/j.jmau.2016.04.002
13. Brouwer KC, Ndhlovu PD, Wagatsuma Y, Munatsi A, Shiff CJ. Urinary tract pathology attributed to Schistosoma haematobium: Does parasite genetics play a role? Am J Trop Med Hyg. 2003;68(4):456–62.
14. Ezeh C, Yin M, Li H, Zhang T, Xu B, Sacko M, et al. High genetic variability of Schistosoma haematobium in Mali and Nigeria. Korean J Parasitol. 2015;53(1):129–34.
15. Moendeg KJ, Ma J, Angeles M, Nakao R, Leonardo LR, Kendrich I, et al. Geographic strain differentiation of Schistosoma japonicum in the Philippines using microsatellite markers. 2017 [cited 2019 Apr 10]; Available from: https://doi.org/10.1371/journal.pntd.0005749
16. Kabuyaya M, Chimbari MJ, Manyangadze T, Mukaratirwa S. Efficacy of praziquantel on Schistosoma haematobium and re-infection rates among school-going children in the Ndumo area of uMkhanyakude district , KwaZulu-Natal , South Africa. 2017;1–9.
17. Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis Daniel. Lancet. 2015;383(9936):2253–64.
18. Kura K, Hardwick RJ, Truscott JE, Toor J, Hollingsworth TD, Anderson RM. The impact of mass drug administration on Schistosoma haematobium infection: what is required to achieve morbidity control and elimination? Parasites and Vectors [Internet]. 2020;13(1):1–10. Available from: https://doi.org/10.1186/s13071-020-04409-3
19. Webster BL, Emery AM, Webster JP, Gouvras A, Garba A, Diaw O, et al. Genetic Diversity within Schistosoma haematobium: DNA Barcoding Reveals Two Distinct Groups. PLoS Negl Trop Dis. 2012;6(10).
20. Webster BL, Rabone M, Pennance T, Emery AM, Allan F, Gouvras A, et al. Development of novel multiplex microsatellite polymerase chain reactions to enable high-throughput population genetic studies of Schistosoma haematobium. Parasites and Vectors [Internet]. 2015;8(1):1–5. Available from: http://dx.doi.org/10.1186/s13071-015-1044-6
21. El-Kady AM, EL-Amir MI, Hassan MH, Allemailem KS, Almatroudi A, Ahmad AlA. Genetic Diversity of Schistosoma haematobium in. Infect Drug Resist. 2020;13:3601–11.
22. Rollinson D, Webster JP, Webster B, Nyakaana S, Jrgensen A, Stothard JR. Genetic diversity of schistosomes and snails: Implications for control. Parasitology. 2009;136(13):1801–11.
23. Moher D, Liberati A, Tetzlaff J, Altman DG, Prisma T. Preferred reporting items for systematic reviews and meta-analyses : The PRISMA statement. 2010;8:336–41.
24. Rey O, Webster BL, Huyse T, Rollinson D, Broeck F Van Den, Onyekwere A, et al. Population genetics of African Schistosoma species To cite this version : HAL Id : hal-03128417 Population genetics of African Schistosoma species. 2021;
25. Webster BL, Culverwell CL, Khamis IS, Mohammed KA, Rollinson D, Stothard JR. Acta Tropica DNA barcoding of Schistosoma haematobium on Zanzibar reveals substantial genetic diversity and two major phylogenetic groups. Acta Trop [Internet]. 2012;128(2):206–17. Available from: http://dx.doi.org/10.1016/j.actatropica.2012.06.002
26. Umar S, Shinkafi SH, Hudu SA, Neela V, Suresh K, Nordin SA, et al. Prevalence and molecular characterisation of Schistosoma haematobium among primary school children in Kebbi State, Nigeria. Ann Parasitol [Internet]. 2017;63(2):133–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28822206
27. Glenn TC, Lance SL, Mckee AM, Webster BL, Emery AM, Zerlotini A, et al. Significant variance in genetic diversity among populations of Schistosoma haematobium detected using microsatellite DNA loci from a genome-wide database. Parasit Vectors [Internet]. 2013;6(1):1. Available from: Parasites & Vectors
28. Golan R, Gower CM, Emery AM, Rollinson D, Webster JP. Europe PMC Funders Group Isolation and characterization of the first polymorphic microsatellite markers for Schistosoma haematobium and their application in multiplex reactions of larval stages. 2014;8(3):647–9.
29. Gower CM, Gouvras AN, Lamberton PHL, Deol A, Shrivastava J, Mutombo PN, et al. Population genetic structure of Schistosoma mansoni and Schistosoma haematobium from across six sub-Saharan African countries: Implications for epidemiology, evolution and control. Acta Trop [Internet]. 2013;128(2):261–74. Available from: http://dx.doi.org/10.1016/j.actatropica.2012.09.014
30. Gower CM, Gabrielli AF, Sacko M, Dembelé R, Golan R, Emery AM, et al. Population genetics of Schistosoma haematobium: Development of novel microsatellite markers and their application to schistosomiasis control in Mali. Parasitology. 2011;138(8):978–94.
31. Ezeh C, Yin M, Li H, Zhang T, Xu B, Sacko M, et al. High genetic variability of Schistosoma haematobium in Mali and Nigeria. Korean J Parasitol. 2015;53(1):129–34.
32. Dabo A, Durand P, Morand S, Diakite M. Distribution and genetic diversity of Schistosoma haematobium within its bulinid intermediate hosts in Mali Distribution and genetic diversity of Schistosoma haematobium within its bulinid intermediate hosts in Mali. 1997;(October 2017).
33. Brouwer KC, Ndhlovu P, Munatsi A, Shiff CJ. Genetic Diversity of a Population of Schistosoma haematobium Derived from Schoolchildren in East Central Zimbabwe. J Parasitol. 2001;87(4):762.
34. Gasmelseed N, Karamino NE, Abdelwahed MO, Hamdoun AO, Elmadani AE. Genetic diversity of Schistosoma haematobium parasite IS NOT associated with severity of disease in an endemic area in Sudan. BMC Infect Dis. 2014;14(1):1–8.
35. Shrivastava J, Bao ZQ, Mcvean G, Webster JP. An insight into the genetic variation of Schistosoma japonicum in mainland China using DNA microsatellite markers. Mol Ecol. 2005;14(3):839–49.
36. Gulcher J. Microsatellite markers for linkage and association studies. Cold Spring Harb Protoc. 2012;7(4):425–32.
37. Webster BL, Webster JP, Gouvras AN, Garba A, Lamine MS, Diaw OT, et al. DNA ‘barcoding’ of Schistosoma mansoni across sub-Saharan Africa supports substantial within locality diversity and geographical separation of genotypes. Acta Trop [Internet]. 2013 Nov [cited 2019 Apr 10];128(2):250–60. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22935316
38. Le TH, Blair D, McManus DP. Mitochondrial genomes of human helminths and their use as markers in population genetics and phylogeny. Acta Trop. 2000;77(3):243–56.
39. Shiff C, Brouwer KC, Clow L. Schistosoma haematobium: Population genetics of S. haematobium by direct measurement of parasite diversity using RAPD ± PCR. Exp Parasitol. 2000;96(1):47–51.
40. Curtis J, Sorensen RE, Minchella DJ. Schistosome genetic diversity: The implications of population structure as detected with microsatellite markers. Parasitology. 2002;125(SUPPL.):51–9.
41. Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey S V. DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res. 1990;18(22):6531–5.
42. Barber KE, Mkoji GM, Loker ES. PCR-RFLP analysis of the ITS2 region to identify Schistosoma haematobium and S. Bovis from Kenya. Am J Trop Med Hyg. 2000;62(4):434–40.
43. Aula OP, McManus DP, Jones MK, Gordon CA. Schistosomiasis with a focus on Africa. Trop Med Infect Dis. 2021;6(3):1–40.
44. Onasanya A, Bengtson M, Oladepo O, Van Engelen J, Diehl JC. Rethinking the Top-Down Approach to Schistosomiasis Control and Elimination in Sub-Saharan Africa. Front Public Heal. 2021;9(February):1–6.
45. Webster BL, Rabone M, Pennance T, Emery AM, Allan F, Gouvras A, et al. Development of novel multiplex microsatellite polymerase chain reactions to enable high-throughput population genetic studies of Schistosoma haematobium. Parasites and Vectors [Internet]. 2015;8(1):1–5. Available from: http://dx.doi.org/10.1186/s13071-015-1044-6
Published
2022-08-12
How to Cite
1.
Tembo R, Nkhoma P, Zulu M, Mwaba F, Yabe J, Halwiindi H, Kamwela M, Nalubamba K, Sikasunge C, Phri A. Genetic Diversity of Schistosoma haematobium in Sub-Saharan Africa: A Systematic Review. Journal of Agricultural and Biomedical Sciences [Internet]. 12Aug.2022 [cited 16Nov.2024];6(1). Available from: https://nscme.unza.zm/index.php/JABS/article/view/778
Section
Biomedical Sciences
Copyright: ©️ JABS. Articles in this journal are distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution License (CC BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.