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Published in: BMC Infectious Diseases 1/2016

Open Access 01-12-2016 | Research article

Molecular evidence of high rates of asymptomatic P. vivax infection and very low P. falciparum malaria in Botswana

Authors: Thato Motshoge, Grace K. Ababio, Larysa Aleksenko, John Read, Elias Peloewetse, Mazhani Loeto, Tjantilili Mosweunyane, Kentse Moakofhi, Davies S. Ntebele, Simon Chihanga, Mpho Motlaleng, Anderson Chinorumba, Moses Vurayai, Jeffrey M. Pernica, Giacomo M. Paganotti, Isaac K. Quaye

Published in: BMC Infectious Diseases | Issue 1/2016

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Abstract

Background

Botswana is one of eight SADC countries targeting malaria elimination by 2018. Through spirited upscaling of control activities and passive surveillance, significant reductions in case incidence of Plasmodium falciparum (0.96 – 0.01) was achieved between 2008 and 2012. As part of the elimination campaign, active detection of asymptomatic Plasmodium species by a highly sensitive method was deemed necessary. This study was carried out to determine asymptomatic Plasmodium species carriage by nested PCR in the country, in 2012.

Method

A cross-sectional study involving 3924 apparently healthy participants were screened for Plasmodium species in 14 districts (5 endemic: Okavango, Ngami, Tutume, Boteti and Bobirwa; and 9 epidemic: North East, Francistown, Serowe-Palapye, Ghanzi, Kweneng West, Kweneng East, Kgatleng, South East, and Good Hope). Venous blood was taken from each participant for a nested PCR detection of Plasmodium species.

Results

The parasite rates of asymptomatic Plasmodium species detected were as follows: Plasmodium falciparum, 0.16 %; Plasmodium vivax, 4.66 %; Plasmodium malariae, (Pm) 0.16 %; Plasmodium ovale, 0 %, mixed infections (P. falciparum and P. vivax), 0.055 %; and (P. vivax and P. malariae), 0.027 %, (total: 5.062 %). The high proportion of asymptomatic reservoir of P. vivax was clustered in the East, South Eastern and Central districts of the country. There appeared to be a correlation between the occurrence of P. malariae infection with P. vivax infection, with the former only occurring in districts that had substantial P. vivax circulation. The median age among 2–12 year olds for P. vivax infection was 5 years (Mean 5.13 years, interquartile range 3–7 years). The odds of being infected with P. vivax decreased by 7 % for each year increase in age (OR 0.93, 95 % CI 0.87–1.00, p = 0.056).

Conclusion

We have confirmed low parasite rate of asymptomatic Plasmodium species in Botswana, with the exception of P.vivax which was unexpectedly high. This has implication for the elimination campaign so a follow up study is warranted to inform decisions on new strategies that take this evidence into account in the elimination campaign.
Literature
1.
go back to reference Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526(7572):207–11.CrossRefPubMedPubMedCentral Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526(7572):207–11.CrossRefPubMedPubMedCentral
2.
go back to reference WHO Malaria Policy Advisory Committee and Secretariat. Malaria Policy Advisory Committee to the WHO: conclusions and recommendations of seventh biannual meeting (March 2015). Malar J. 2015;14:295. 015-0787-z.CrossRefPubMedCentral WHO Malaria Policy Advisory Committee and Secretariat. Malaria Policy Advisory Committee to the WHO: conclusions and recommendations of seventh biannual meeting (March 2015). Malar J. 2015;14:295. 015-0787-z.CrossRefPubMedCentral
3.
go back to reference Moonasar D, Nuthulaganti T, Kruger PS, Mabuza A, Rasiswi ES, Benson FG, et al. Malaria control in South Africa 2000-2010: beyond MDG6. Malar J. 2012;11:294. 2875-11-294.CrossRefPubMedPubMedCentral Moonasar D, Nuthulaganti T, Kruger PS, Mabuza A, Rasiswi ES, Benson FG, et al. Malaria control in South Africa 2000-2010: beyond MDG6. Malar J. 2012;11:294. 2875-11-294.CrossRefPubMedPubMedCentral
4.
go back to reference Simon C, Moakofhi K, Mosweunyane T, Jibril HB, Nkomo B, Motlaleng M, et al. Malaria control in Botswana, 2008-2012: the path towards elimination. Malar J. 2013;12:458. 2875-12-458.CrossRefPubMedPubMedCentral Simon C, Moakofhi K, Mosweunyane T, Jibril HB, Nkomo B, Motlaleng M, et al. Malaria control in Botswana, 2008-2012: the path towards elimination. Malar J. 2013;12:458. 2875-12-458.CrossRefPubMedPubMedCentral
5.
go back to reference Cohen JM, Moonen B, Snow RW, Smith DL. How absolute is zero? An evaluation of historical and current definitions of malaria elimination. Malar J. 2010;9:213. 2875-9-213.CrossRefPubMedPubMedCentral Cohen JM, Moonen B, Snow RW, Smith DL. How absolute is zero? An evaluation of historical and current definitions of malaria elimination. Malar J. 2010;9:213. 2875-9-213.CrossRefPubMedPubMedCentral
6.
go back to reference Thomson MC, Mason SJ, Phindela T, Connor SJ. Use of rainfall and sea surface temperature monitoring for malaria early warning in Botswana. Am J Trop Med Hyg. 2005;73(1):214–21.PubMed Thomson MC, Mason SJ, Phindela T, Connor SJ. Use of rainfall and sea surface temperature monitoring for malaria early warning in Botswana. Am J Trop Med Hyg. 2005;73(1):214–21.PubMed
7.
go back to reference Ouedraogo AL, Bousema T, Schneider P, de Vlas SJ, Ilboudo-Sanogo E, Cuzin-Ouattara N, et al. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PLoS One. 2009;4(12):e8410.CrossRefPubMedPubMedCentral Ouedraogo AL, Bousema T, Schneider P, de Vlas SJ, Ilboudo-Sanogo E, Cuzin-Ouattara N, et al. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PLoS One. 2009;4(12):e8410.CrossRefPubMedPubMedCentral
8.
go back to reference Krotoski WA, Collins WE, Bray RS, Garnham PC, Cogswell FB, Gwadz RW, et al. Demonstration of hypnozoites in sporozoite-transmitted Plasmodium vivax infection. Am J Trop Med Hyg. 1982;31(6):1291–3.PubMed Krotoski WA, Collins WE, Bray RS, Garnham PC, Cogswell FB, Gwadz RW, et al. Demonstration of hypnozoites in sporozoite-transmitted Plasmodium vivax infection. Am J Trop Med Hyg. 1982;31(6):1291–3.PubMed
9.
go back to reference Mendis K, Sina BJ, Marchesini P, Carter R. The neglected burden of Plasmodium vivax malaria. Am J Trop Med Hyg. 2001;64(1-2 Suppl):97–106.PubMed Mendis K, Sina BJ, Marchesini P, Carter R. The neglected burden of Plasmodium vivax malaria. Am J Trop Med Hyg. 2001;64(1-2 Suppl):97–106.PubMed
10.
go back to reference malERA Consultative Group on Diagnoses and Diagnostics. A research agenda for malaria eradication: diagnoses and diagnostics. PLoS Med. 2011;8(1):e1000396.CrossRef malERA Consultative Group on Diagnoses and Diagnostics. A research agenda for malaria eradication: diagnoses and diagnostics. PLoS Med. 2011;8(1):e1000396.CrossRef
11.
go back to reference Harris I, Sharrock WW, Bain LM, Gray KA, Bobogare A, Boaz L, et al. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar J. 2010;9:254. 2875-9-254.CrossRefPubMedPubMedCentral Harris I, Sharrock WW, Bain LM, Gray KA, Bobogare A, Boaz L, et al. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar J. 2010;9:254. 2875-9-254.CrossRefPubMedPubMedCentral
12.
go back to reference Laishram DD, Sutton PL, Nanda N, Sharma VL, Sobti RC, Carlton JM, Laishram DD, Sutton PL, Nanda N, Sharma VL, Sobti RC, Carlton JM, et al. The complexities of malaria disease manifestations with a focus on asymptomatic malaria. Malar J. 2012;11:29. 2875-11-29.CrossRefPubMedPubMedCentral Laishram DD, Sutton PL, Nanda N, Sharma VL, Sobti RC, Carlton JM, Laishram DD, Sutton PL, Nanda N, Sharma VL, Sobti RC, Carlton JM, et al. The complexities of malaria disease manifestations with a focus on asymptomatic malaria. Malar J. 2012;11:29. 2875-11-29.CrossRefPubMedPubMedCentral
13.
go back to reference Okell LC, Bousema T, Griffin JT, Ouedraogo AL, Ghani AC, Drakeley CJ. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun. 2012;3:1237.CrossRefPubMedPubMedCentral Okell LC, Bousema T, Griffin JT, Ouedraogo AL, Ghani AC, Drakeley CJ. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun. 2012;3:1237.CrossRefPubMedPubMedCentral
14.
go back to reference Moreira CM, Abo-Shehada M, Price RN, Drakeley CJ. A systematic review of sub-microscopic Plasmodium vivax infection. Malar J. 2015;14(1):360. 015-0884-z.CrossRefPubMedPubMedCentral Moreira CM, Abo-Shehada M, Price RN, Drakeley CJ. A systematic review of sub-microscopic Plasmodium vivax infection. Malar J. 2015;14(1):360. 015-0884-z.CrossRefPubMedPubMedCentral
15.
go back to reference Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, et al. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol. 1993;61(2):315–20.CrossRefPubMed Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, et al. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol. 1993;61(2):315–20.CrossRefPubMed
16.
go back to reference Howes RE, Reiner Jr RC, Battle KE, Longbottom J, Mappin B, Ordanovich D, et al. Plasmodium vivax Transmission in Africa. PLoS Negl Trop Dis. 2015;9(11):e0004222.CrossRefPubMedPubMedCentral Howes RE, Reiner Jr RC, Battle KE, Longbottom J, Mappin B, Ordanovich D, et al. Plasmodium vivax Transmission in Africa. PLoS Negl Trop Dis. 2015;9(11):e0004222.CrossRefPubMedPubMedCentral
17.
go back to reference Delgado-Ratto C, Soto-Calle VE, Van den Eede P, Gamboa D, Rosas A, Abatih EN, et al. Population structure and spatio-temporal transmission dynamics of Plasmodium vivax after radical cure treatment in a rural village of the Peruvian Amazon. Malar J. 2014;13:8. 2875-13-8.CrossRefPubMedPubMedCentral Delgado-Ratto C, Soto-Calle VE, Van den Eede P, Gamboa D, Rosas A, Abatih EN, et al. Population structure and spatio-temporal transmission dynamics of Plasmodium vivax after radical cure treatment in a rural village of the Peruvian Amazon. Malar J. 2014;13:8. 2875-13-8.CrossRefPubMedPubMedCentral
18.
go back to reference Liu W, Li Y, Shaw KS, Learn GH, Plenderleith LJ, Malenke JA, et al. African origin of the malaria parasite Plasmodium vivax. Nat Commun. 2014;5:3346.PubMedPubMedCentral Liu W, Li Y, Shaw KS, Learn GH, Plenderleith LJ, Malenke JA, et al. African origin of the malaria parasite Plasmodium vivax. Nat Commun. 2014;5:3346.PubMedPubMedCentral
19.
go back to reference Paupy C, Makanga B, Ollomo B, Rahola N, Durand P, Magnus J, et al. Anopheles moucheti and Anopheles vinckei are candidate vectors of ape Plasmodium parasites, including Plasmodium praefalciparum in Gabon. PLoS One. 2013;8(2):e57294.CrossRefPubMedPubMedCentral Paupy C, Makanga B, Ollomo B, Rahola N, Durand P, Magnus J, et al. Anopheles moucheti and Anopheles vinckei are candidate vectors of ape Plasmodium parasites, including Plasmodium praefalciparum in Gabon. PLoS One. 2013;8(2):e57294.CrossRefPubMedPubMedCentral
20.
go back to reference Prugnolle F, Rougeron V, Becquart P, Berry A, Makanga B, Rahola N, et al. Diversity, host switching and evolution of Plasmodium vivax infecting African great apes. Proc Natl Acad Sci U S A. 2013;110(20):8123–8.CrossRefPubMedPubMedCentral Prugnolle F, Rougeron V, Becquart P, Berry A, Makanga B, Rahola N, et al. Diversity, host switching and evolution of Plasmodium vivax infecting African great apes. Proc Natl Acad Sci U S A. 2013;110(20):8123–8.CrossRefPubMedPubMedCentral
21.
go back to reference Golassa L, Baliraine FN, Enweji N, Erko B, Swedberg G, Aseffa A. Microscopic and molecular evidence of the presence of asymptomatic Plasmodium falciparum and Plasmodium vivax infections in an area with low, seasonal and unstable malaria transmission in Ethiopia. BMC Infect Dis. 2015;15:310. 015-1070-1.CrossRefPubMedPubMedCentral Golassa L, Baliraine FN, Enweji N, Erko B, Swedberg G, Aseffa A. Microscopic and molecular evidence of the presence of asymptomatic Plasmodium falciparum and Plasmodium vivax infections in an area with low, seasonal and unstable malaria transmission in Ethiopia. BMC Infect Dis. 2015;15:310. 015-1070-1.CrossRefPubMedPubMedCentral
22.
go back to reference Chihanga S, Haque U, Chanda E, Mosweunyane T, Moakofhi K, Jibril HB, et al. Malaria elimination in Botswana, 2012-2014: achievements and challenges. Parasit Vectors. 2016;9:99. 016-1382.CrossRefPubMedPubMedCentral Chihanga S, Haque U, Chanda E, Mosweunyane T, Moakofhi K, Jibril HB, et al. Malaria elimination in Botswana, 2012-2014: achievements and challenges. Parasit Vectors. 2016;9:99. 016-1382.CrossRefPubMedPubMedCentral
23.
go back to reference Miller LH, Mason SJ, Clyde DF, McGinniss MH. The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med. 1976;295(6):302–4.CrossRefPubMed Miller LH, Mason SJ, Clyde DF, McGinniss MH. The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med. 1976;295(6):302–4.CrossRefPubMed
24.
go back to reference Gething PW, Elyazar IR, Moyes CL, Smith DL, Battle KE, Guerra CA, et al. A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Negl Trop Dis. 2012;6(9):e1814.CrossRefPubMedPubMedCentral Gething PW, Elyazar IR, Moyes CL, Smith DL, Battle KE, Guerra CA, et al. A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Negl Trop Dis. 2012;6(9):e1814.CrossRefPubMedPubMedCentral
25.
26.
go back to reference Young MD, Johnson Jr TH. A malaria survey of Liberia. J Natl Malar Soc. 1949;8(4):247–66. illust.PubMed Young MD, Johnson Jr TH. A malaria survey of Liberia. J Natl Malar Soc. 1949;8(4):247–66. illust.PubMed
27.
go back to reference Mendes C, Dias F, Figueiredo J, Mora VG, Cano J, de Sousa B, et al. Duffy negative antigen is no longer a barrier to Plasmodium vivax--molecular evidences from the African West Coast (Angola and Equatorial Guinea). PLoS Negl Trop Dis. 2011;5(6):e1192.CrossRefPubMedPubMedCentral Mendes C, Dias F, Figueiredo J, Mora VG, Cano J, de Sousa B, et al. Duffy negative antigen is no longer a barrier to Plasmodium vivax--molecular evidences from the African West Coast (Angola and Equatorial Guinea). PLoS Negl Trop Dis. 2011;5(6):e1192.CrossRefPubMedPubMedCentral
28.
go back to reference Lo E, Yewhalaw D, Zhong D, Zemene E, Degefa T, Tushune K, et al. Molecular epidemiology of Plasmodium vivax and Plasmodium falciparum malaria among Duffy-positive and Duffy-negative populations in Ethiopia. Malar J. 2015;14:84. 015-0596-4.CrossRefPubMedPubMedCentral Lo E, Yewhalaw D, Zhong D, Zemene E, Degefa T, Tushune K, et al. Molecular epidemiology of Plasmodium vivax and Plasmodium falciparum malaria among Duffy-positive and Duffy-negative populations in Ethiopia. Malar J. 2015;14:84. 015-0596-4.CrossRefPubMedPubMedCentral
29.
go back to reference Ngassa Mbenda HG, Das A. Molecular evidence of Plasmodium vivax mono and mixed malaria parasite infections in Duffy-negative native Cameroonians. PLoS One. 2014;9(8):e103262.CrossRefPubMedPubMedCentral Ngassa Mbenda HG, Das A. Molecular evidence of Plasmodium vivax mono and mixed malaria parasite infections in Duffy-negative native Cameroonians. PLoS One. 2014;9(8):e103262.CrossRefPubMedPubMedCentral
30.
go back to reference Ryan JR, Stoute JA, Amon J, Dunton RF, Mtalib R, Koros J, et al. Evidence for transmission of Plasmodium vivax among a duffy antigen negative population in Western Kenya. Am J Trop Med Hyg. 2006;75(4):575–81.PubMed Ryan JR, Stoute JA, Amon J, Dunton RF, Mtalib R, Koros J, et al. Evidence for transmission of Plasmodium vivax among a duffy antigen negative population in Western Kenya. Am J Trop Med Hyg. 2006;75(4):575–81.PubMed
31.
go back to reference Menard D, Barnadas C, Bouchier C, Henry-Halldin C, Gray LR, Ratsimbasoa A, et al. Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc Natl Acad Sci U S A. 2010;107(13):5967–71.CrossRefPubMedPubMedCentral Menard D, Barnadas C, Bouchier C, Henry-Halldin C, Gray LR, Ratsimbasoa A, et al. Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc Natl Acad Sci U S A. 2010;107(13):5967–71.CrossRefPubMedPubMedCentral
32.
go back to reference Adekunle AI, Pinkevych M, McGready R, Luxemburger C, White LJ, Nosten F, et al. Modeling the dynamics of Plasmodium vivax infection and hypnozoite reactivation in vivo. PLoS Negl Trop Dis. 2015;9(3):e0003595.CrossRefPubMedPubMedCentral Adekunle AI, Pinkevych M, McGready R, Luxemburger C, White LJ, Nosten F, et al. Modeling the dynamics of Plasmodium vivax infection and hypnozoite reactivation in vivo. PLoS Negl Trop Dis. 2015;9(3):e0003595.CrossRefPubMedPubMedCentral
35.
go back to reference Cotter C, Sturrock HJ, Hsiang MS, Liu J, Phillips AA, Hwang J, et al. The changing epidemiology of malaria elimination: new strategies for new challenges. Lancet. 2013;382(9895):900–11.CrossRefPubMed Cotter C, Sturrock HJ, Hsiang MS, Liu J, Phillips AA, Hwang J, et al. The changing epidemiology of malaria elimination: new strategies for new challenges. Lancet. 2013;382(9895):900–11.CrossRefPubMed
Metadata
Title
Molecular evidence of high rates of asymptomatic P. vivax infection and very low P. falciparum malaria in Botswana
Authors
Thato Motshoge
Grace K. Ababio
Larysa Aleksenko
John Read
Elias Peloewetse
Mazhani Loeto
Tjantilili Mosweunyane
Kentse Moakofhi
Davies S. Ntebele
Simon Chihanga
Mpho Motlaleng
Anderson Chinorumba
Moses Vurayai
Jeffrey M. Pernica
Giacomo M. Paganotti
Isaac K. Quaye
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2016
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-016-1857-8

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