Skip to main content
Top
Published in: BMC Medicine 1/2019

Open Access 01-12-2019 | Malaria | Research article

From high to low malaria transmission in Zanzibar—challenges and opportunities to achieve elimination

Authors: A. Björkman, D. Shakely, A. S. Ali, U. Morris, H. Mkali, A. K. Abbas, A-W Al-Mafazy, K. A. Haji, J. Mcha, R. Omar, J. Cook, K. Elfving, M. Petzold, M. C. Sachs, B. Aydin-Schmidt, C. Drakeley, M. Msellem, A. Mårtensson

Published in: BMC Medicine | Issue 1/2019

Login to get access

Abstract

Background

Substantial global progress in the control of malaria in recent years has led to increased commitment to its potential elimination. Whether this is possible in high transmission areas of sub-Saharan Africa remains unclear. Zanzibar represents a unique case study of such attempt, where modern tools and strategies for malaria treatment and vector control have been deployed since 2003.

Methods

We have studied temporal trends of comprehensive malariometric indices in two districts with over 100,000 inhabitants each. The analyses included triangulation of data from annual community-based cross-sectional surveys, health management information systems, vital registry and entomological sentinel surveys.

Results

The interventions, with sustained high-community uptake, were temporally associated with a major malaria decline, most pronounced between 2004 and 2007 and followed by a sustained state of low transmission. In 2015, the Plasmodium falciparum community prevalence of 0.43% (95% CI 0.23–0.73) by microscopy or rapid diagnostic test represented 96% reduction compared with that in 2003. The P. falciparum and P. malariae prevalence by PCR was 1.8% (95% CI 1.3–2.3), and the annual P. falciparum incidence was estimated to 8 infections including 2.8 clinical episodes per 1000 inhabitants. The total parasite load decreased over 1000-fold (99.9%) between 2003 and 2015. The incidence of symptomatic malaria at health facilities decreased by 94% with a trend towards relatively higher incidence in age groups > 5 years, a more pronounced seasonality and with reported travel history to/from Tanzania mainland as a higher risk factor. All-cause mortality among children < 5 years decreased by 72% between 2002 and 2007 mainly following the introduction of artemisinin-based combination therapies whereas the main reduction in malaria incidence followed upon the vector control interventions from 2006. Human biting rates decreased by 98% with a major shift towards outdoor biting by Anopheles arabiensis.

Conclusions

Zanzibar provides new evidence of the feasibility of reaching uniquely significant and sustainable malaria reduction (pre-elimination) in a previously high endemic region in sub-Saharan Africa. The data highlight constraints of optimistic prognostic modelling studies. New challenges, mainly with outdoor transmission, a large asymptomatic parasite reservoir and imported infections, require novel tools and reoriented strategies to prevent a rebound effect and achieve elimination.
Appendix
Available only for authorised users
Literature
2.
go back to reference Maintaining momentum for malaria elimination. Lancet 2009; 374(9686): 266. Maintaining momentum for malaria elimination. Lancet 2009; 374(9686): 266.
4.
go back to reference Mendis K, Rietveld A, Warsame M, Bosman A, Greenwood B, Wernsdorfer WH. From malaria control to eradication: the WHO perspective. Trop Med Int Health. 2009;14(7):802–9.PubMedCrossRef Mendis K, Rietveld A, Warsame M, Bosman A, Greenwood B, Wernsdorfer WH. From malaria control to eradication: the WHO perspective. Trop Med Int Health. 2009;14(7):802–9.PubMedCrossRef
5.
go back to reference World Health Organization, Global Malaria Programme 2007. Malaria elimination: a field manual for low and moderate endemic countries. WHO Report. World Health Organization, Global Malaria Programme 2007. Malaria elimination: a field manual for low and moderate endemic countries. WHO Report.
6.
go back to reference Metselaar D, Thiel v. Classification of malaria. Trop Geogr Med. 1959;11:157–61. Metselaar D, Thiel v. Classification of malaria. Trop Geogr Med. 1959;11:157–61.
7.
go back to reference Schwartz E, Pener H, Issa SM, Golenser J. An overview of the malaria situation in Zanzibar. J Community Health. 1997;22(1):33–44.PubMedCrossRef Schwartz E, Pener H, Issa SM, Golenser J. An overview of the malaria situation in Zanzibar. J Community Health. 1997;22(1):33–44.PubMedCrossRef
8.
go back to reference Bhattarai A, Ali AS, Kachur SP, et al. Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med. 2007;4(11):e309.PubMedPubMedCentralCrossRef Bhattarai A, Ali AS, Kachur SP, et al. Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med. 2007;4(11):e309.PubMedPubMedCentralCrossRef
9.
go back to reference Smith DL, Hay SI. Endemicity response timelines for Plasmodium falciparum elimination. Mal J. 2009;8:87.CrossRef Smith DL, Hay SI. Endemicity response timelines for Plasmodium falciparum elimination. Mal J. 2009;8:87.CrossRef
10.
go back to reference Wooden J, Kyes S, Sibley CH. PCR and strain identification in Plasmodium falciparum. Parasitol Today. 1993;9(8):303–5.PubMedCrossRef Wooden J, Kyes S, Sibley CH. PCR and strain identification in Plasmodium falciparum. Parasitol Today. 1993;9(8):303–5.PubMedCrossRef
11.
go back to reference Xu W, Morris U, Aydin-Schmidt B, et al. SYBR green real-time PCR-RFLP assay targeting the Plasmodium cytochrome B gene - a highly sensitive molecular tool for malaria parasite detection and species determination. PLoS One. 2015;10(3):e0120210.PubMedPubMedCentralCrossRef Xu W, Morris U, Aydin-Schmidt B, et al. SYBR green real-time PCR-RFLP assay targeting the Plasmodium cytochrome B gene - a highly sensitive molecular tool for malaria parasite detection and species determination. PLoS One. 2015;10(3):e0120210.PubMedPubMedCentralCrossRef
12.
go back to reference Kamau E, Tolbert LS, Kortepeter L, et al. Development of a highly sensitive genus-specific quantitative reverse transcriptase real-time PCR assay for detection and quantitation of plasmodium by amplifying RNA and DNA of the 18S rRNA genes. J Clin Microbiol. 2011;49(8):2946–53.PubMedPubMedCentralCrossRef Kamau E, Tolbert LS, Kortepeter L, et al. Development of a highly sensitive genus-specific quantitative reverse transcriptase real-time PCR assay for detection and quantitation of plasmodium by amplifying RNA and DNA of the 18S rRNA genes. J Clin Microbiol. 2011;49(8):2946–53.PubMedPubMedCentralCrossRef
13.
14.
go back to reference Zanzibar Malaria Control (Elimination) Programme. Zanzibar Malaria Epidemic Early Detection System and Entomological Surveillance. Ministry of Health and Social Welfare. Annual and biannual reports 2005–2016. Zanzibar Malaria Control (Elimination) Programme. Zanzibar Malaria Epidemic Early Detection System and Entomological Surveillance. Ministry of Health and Social Welfare. Annual and biannual reports 2005–2016.
15.
go back to reference Jones CM, Haji KA, Khatib BO, et al. The dynamics of pyrethroid resistance in Anopheles arabiensis from Zanzibar and an assessment of the underlying genetic basis. Parasit Vectors. 2013;6:343.PubMedPubMedCentralCrossRef Jones CM, Haji KA, Khatib BO, et al. The dynamics of pyrethroid resistance in Anopheles arabiensis from Zanzibar and an assessment of the underlying genetic basis. Parasit Vectors. 2013;6:343.PubMedPubMedCentralCrossRef
16.
go back to reference Beier JC, Perkins PV, Koros JK, et al. Malaria sporozoite detection by dissection and ELISA to assess infectivity of afrotropical Anopheles (Dipteria : Culicidae). J Med Entomol. 1990;27:377–84.PubMedCrossRef Beier JC, Perkins PV, Koros JK, et al. Malaria sporozoite detection by dissection and ELISA to assess infectivity of afrotropical Anopheles (Dipteria : Culicidae). J Med Entomol. 1990;27:377–84.PubMedCrossRef
17.
go back to reference WHO. Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. Geneva: World Health Organization; 2016. SBN 9789241511575 WHO. Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. Geneva: World Health Organization; 2016. SBN 9789241511575
18.
go back to reference Haji KA, Thawer NG, Khatib BO, et al. Efficacy, persistence and vector susceptibility to pirimiphos-methyl (Actellic 300CS) insecticide for indoor residual spraying in Zanzibar. Parasit Vectors. 2015;8:628.PubMedPubMedCentralCrossRef Haji KA, Thawer NG, Khatib BO, et al. Efficacy, persistence and vector susceptibility to pirimiphos-methyl (Actellic 300CS) insecticide for indoor residual spraying in Zanzibar. Parasit Vectors. 2015;8:628.PubMedPubMedCentralCrossRef
19.
go back to reference Haji KA, Khatib BO, Smith S, et al. Challenges for malaria elimination in Zanzibar: pyrethroid resistance in malaria vectors and poor performance of long-lasting insecticide nets. Parasit Vectors. 2013;6:82.PubMedPubMedCentralCrossRef Haji KA, Khatib BO, Smith S, et al. Challenges for malaria elimination in Zanzibar: pyrethroid resistance in malaria vectors and poor performance of long-lasting insecticide nets. Parasit Vectors. 2013;6:82.PubMedPubMedCentralCrossRef
20.
go back to reference Drakeley CJ, Corran PH, Coleman PG, et al. Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci U S A. 2005;102(14):5108–13.PubMedPubMedCentralCrossRef Drakeley CJ, Corran PH, Coleman PG, et al. Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci U S A. 2005;102(14):5108–13.PubMedPubMedCentralCrossRef
21.
go back to reference Cook J, Kleinschmidt I, Schwabe C, et al. Serological markers suggest heterogeneity of effectiveness of malaria control interventions on Bioko Island, Equatorial Guinea. PLoS One. 2011;6(9):e25137.PubMedPubMedCentralCrossRef Cook J, Kleinschmidt I, Schwabe C, et al. Serological markers suggest heterogeneity of effectiveness of malaria control interventions on Bioko Island, Equatorial Guinea. PLoS One. 2011;6(9):e25137.PubMedPubMedCentralCrossRef
22.
go back to reference Ross A, Killeen G, Smith T. Relationships between host infectivity to mosquitoes and asexual parasite density in Plasmodium falciparum. Am J Trop Med Hyg. 2006;75(suppl2):32–7.PubMedCrossRef Ross A, Killeen G, Smith T. Relationships between host infectivity to mosquitoes and asexual parasite density in Plasmodium falciparum. Am J Trop Med Hyg. 2006;75(suppl2):32–7.PubMedCrossRef
23.
go back to reference Shakely D, Elfving K, Aydin-Schmidt B, et al. The usefulness of rapid diagnostic tests in the new context of low malaria transmission in Zanzibar. PLoS One. 2013;8(9):e72912.PubMedPubMedCentralCrossRef Shakely D, Elfving K, Aydin-Schmidt B, et al. The usefulness of rapid diagnostic tests in the new context of low malaria transmission in Zanzibar. PLoS One. 2013;8(9):e72912.PubMedPubMedCentralCrossRef
24.
go back to reference Msellem MI, Martensson A, Rotllant G, et al. Influence of rapid malaria diagnostic tests on treatment and health outcome in fever patients, Zanzibar: a crossover validation study. PLoS Med. 2009;6(4):e1000070.PubMedPubMedCentralCrossRef Msellem MI, Martensson A, Rotllant G, et al. Influence of rapid malaria diagnostic tests on treatment and health outcome in fever patients, Zanzibar: a crossover validation study. PLoS Med. 2009;6(4):e1000070.PubMedPubMedCentralCrossRef
25.
go back to reference Beer N, Ali AS, Rotlant G, et al. Adherence to artesunate-amodiaquine combination therapy for uncomplicated malaria in children in Zanzibar, Tanzania. Trop Med Int Health. 2009;7:766–74.CrossRef Beer N, Ali AS, Rotlant G, et al. Adherence to artesunate-amodiaquine combination therapy for uncomplicated malaria in children in Zanzibar, Tanzania. Trop Med Int Health. 2009;7:766–74.CrossRef
26.
go back to reference Martensson A, Stromberg J, Sisowath C, et al. Efficacy of artesunate plus amodiaquine versus that of artemether-lumefantrine for the treatment of uncomplicated childhood Plasmodium falciparum malaria in Zanzibar, Tanzania. Clin Infect Dis. 2005;41(8):1079–86.PubMedCrossRef Martensson A, Stromberg J, Sisowath C, et al. Efficacy of artesunate plus amodiaquine versus that of artemether-lumefantrine for the treatment of uncomplicated childhood Plasmodium falciparum malaria in Zanzibar, Tanzania. Clin Infect Dis. 2005;41(8):1079–86.PubMedCrossRef
27.
go back to reference Froberg G, Jornhagen L, Morris U, et al. Decreased prevalence of Plasmodium falciparum resistance markers to amodiaquine despite its wide scale use as ACT partner drug in Zanzibar. Malar J. 2012;11:321.PubMedPubMedCentralCrossRef Froberg G, Jornhagen L, Morris U, et al. Decreased prevalence of Plasmodium falciparum resistance markers to amodiaquine despite its wide scale use as ACT partner drug in Zanzibar. Malar J. 2012;11:321.PubMedPubMedCentralCrossRef
28.
go back to reference Howard SC, Omumbo J, Nevill C, Some ES, Donnelly CA, Snow RW. Evidence for a mass community effect of insecticide-treated bednets on the incidence of malaria on the Kenyan coast. Trans R Soc Trop Med Hyg. 2000;94(4):357–60.PubMedCrossRef Howard SC, Omumbo J, Nevill C, Some ES, Donnelly CA, Snow RW. Evidence for a mass community effect of insecticide-treated bednets on the incidence of malaria on the Kenyan coast. Trans R Soc Trop Med Hyg. 2000;94(4):357–60.PubMedCrossRef
29.
go back to reference Killeen GF, Smith TA, Ferguson HM, et al. Preventing childhood malaria in Africa by protecting adults from mosquitoes with insecticide-treated nets. PLoS Med. 2007;4(7):e229.PubMedPubMedCentralCrossRef Killeen GF, Smith TA, Ferguson HM, et al. Preventing childhood malaria in Africa by protecting adults from mosquitoes with insecticide-treated nets. PLoS Med. 2007;4(7):e229.PubMedPubMedCentralCrossRef
30.
go back to reference Beer N, Ali AS, de Savigny D, et al. System effectiveness of a targeted free mass distribution of long lasting insecticidal nets in Zanzibar, Tanzania. Malaria J. 2010;9:173.CrossRef Beer N, Ali AS, de Savigny D, et al. System effectiveness of a targeted free mass distribution of long lasting insecticidal nets in Zanzibar, Tanzania. Malaria J. 2010;9:173.CrossRef
31.
go back to reference Beer N, Ali AS, Shakely D, et al. High effective coverage of vector control interventions in children after achieving low malaria transmission in Zanzibar, Tanzania. Malaria J. 2013;12:38.CrossRef Beer N, Ali AS, Shakely D, et al. High effective coverage of vector control interventions in children after achieving low malaria transmission in Zanzibar, Tanzania. Malaria J. 2013;12:38.CrossRef
32.
go back to reference Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 2011;27(2):91–8.PubMedCrossRef Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 2011;27(2):91–8.PubMedCrossRef
33.
go back to reference Wondji CS, Coleman M, Kleinschmidt I, et al. Impact of pyrethroid resistance on operational malaria control in Malawi. Proc Natl Acad Sci U S A. 2012;109(47):19063–70.PubMedPubMedCentralCrossRef Wondji CS, Coleman M, Kleinschmidt I, et al. Impact of pyrethroid resistance on operational malaria control in Malawi. Proc Natl Acad Sci U S A. 2012;109(47):19063–70.PubMedPubMedCentralCrossRef
34.
go back to reference Bayoh MN, Mathias DK, Odiere MR, et al. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malaria J. 2010;9:62.CrossRef Bayoh MN, Mathias DK, Odiere MR, et al. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malaria J. 2010;9:62.CrossRef
35.
go back to reference Derua YA, Alifrangis M, Hosea KM, et al. Change in composition of the Anopheles gambiae complex and its possible implications for the transmission of malaria and lymphatic filariasis in North-Eastern Tanzania. Malar J. 2012;11:188.PubMedPubMedCentralCrossRef Derua YA, Alifrangis M, Hosea KM, et al. Change in composition of the Anopheles gambiae complex and its possible implications for the transmission of malaria and lymphatic filariasis in North-Eastern Tanzania. Malar J. 2012;11:188.PubMedPubMedCentralCrossRef
36.
go back to reference Moiroux N, Gomez MB, Pennetier C, et al. Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis. 2012;206(10):1622–9.PubMedCrossRef Moiroux N, Gomez MB, Pennetier C, et al. Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis. 2012;206(10):1622–9.PubMedCrossRef
37.
go back to reference Mwangangi JM, Mbogo CM, Orindi BO, et al. Shifts in malaria vector species composition and transmission dynamics along the Kenyan coast over the past 20 years. Malar J. 2013;12:13.PubMedPubMedCentralCrossRef Mwangangi JM, Mbogo CM, Orindi BO, et al. Shifts in malaria vector species composition and transmission dynamics along the Kenyan coast over the past 20 years. Malar J. 2013;12:13.PubMedPubMedCentralCrossRef
38.
go back to reference Noor AM, Kinyoki DK, Mundia CW, et al. The changing risk of Plasmodium falciparum malaria infection in Africa: 2000-10: a spatial and temporal analysis of transmission intensity. Lancet. 2014;383(9930):1739–47.PubMedPubMedCentralCrossRef Noor AM, Kinyoki DK, Mundia CW, et al. The changing risk of Plasmodium falciparum malaria infection in Africa: 2000-10: a spatial and temporal analysis of transmission intensity. Lancet. 2014;383(9930):1739–47.PubMedPubMedCentralCrossRef
39.
go back to reference Ceesay SJ, Casals-Pascual C, Nwakanma DC, et al. Continued decline of malaria in the Gambia with implications for elimination. PLoS One. 2010;5(8):e12242.PubMedPubMedCentralCrossRef Ceesay SJ, Casals-Pascual C, Nwakanma DC, et al. Continued decline of malaria in the Gambia with implications for elimination. PLoS One. 2010;5(8):e12242.PubMedPubMedCentralCrossRef
40.
go back to reference Karema C, Aregawi MW, Rukundo A, et al. Trends in malaria cases, hospital admissions and deaths following scale-up of anti-malarial interventions, 2000-2010, Rwanda. Malaria J. 2012;11:236.CrossRef Karema C, Aregawi MW, Rukundo A, et al. Trends in malaria cases, hospital admissions and deaths following scale-up of anti-malarial interventions, 2000-2010, Rwanda. Malaria J. 2012;11:236.CrossRef
41.
go back to reference Mmbando BP, Vestergaard LS, Kitua AY, Lemnge MM, Theander TG, Lusingu JP. A progressive declining in the burden of malaria in North-Eastern Tanzania. Malar J. 2010;9:216.PubMedPubMedCentralCrossRef Mmbando BP, Vestergaard LS, Kitua AY, Lemnge MM, Theander TG, Lusingu JP. A progressive declining in the burden of malaria in North-Eastern Tanzania. Malar J. 2010;9:216.PubMedPubMedCentralCrossRef
42.
go back to reference Kleinschmidt I, Schwabe C, Benavente L, et al. Marked increase in child survival after four years of intensive malaria control. Am J Trop Med Hyg. 2009;80(6):882–8.PubMedPubMedCentralCrossRef Kleinschmidt I, Schwabe C, Benavente L, et al. Marked increase in child survival after four years of intensive malaria control. Am J Trop Med Hyg. 2009;80(6):882–8.PubMedPubMedCentralCrossRef
43.
go back to reference Trape JF, Tall A, Sokhna C, et al. The rise and fall of malaria in a west African rural community, Dielmo, Senegal, from 1990 to 2012: a 22 year longitudinal study. Lancet Infect Dis. 2014;14(6):476–88.PubMedCrossRef Trape JF, Tall A, Sokhna C, et al. The rise and fall of malaria in a west African rural community, Dielmo, Senegal, from 1990 to 2012: a 22 year longitudinal study. Lancet Infect Dis. 2014;14(6):476–88.PubMedCrossRef
44.
go back to reference Zanzibar Malaria Control Programme. Malaria elimination in Zanzibar a feasibility assessment. Zanzibar: Ministry of Health and Social Welfare; 2009. Zanzibar Malaria Control Programme. Malaria elimination in Zanzibar a feasibility assessment. Zanzibar: Ministry of Health and Social Welfare; 2009.
45.
go back to reference Ahmed S, Galagan S, Scobie H, et al. Malaria hotspots drive hypoendemic transmission in the Chittagong Hill Districts of Bangladesh. PLoS One. 2013;8(8):e69713.PubMedPubMedCentralCrossRef Ahmed S, Galagan S, Scobie H, et al. Malaria hotspots drive hypoendemic transmission in the Chittagong Hill Districts of Bangladesh. PLoS One. 2013;8(8):e69713.PubMedPubMedCentralCrossRef
46.
go back to reference Harris I, Sharrock WW, Bain LM, 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. Malaria J. 2010;9:254.CrossRef Harris I, Sharrock WW, Bain LM, 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. Malaria J. 2010;9:254.CrossRef
47.
go back to reference Manjurano A, Okell L, Lukindo T, et al. Association of sub-microscopic malaria parasite carriage with transmission intensity in North-Eastern Tanzania. Malar J. 2011;10:370.PubMedPubMedCentralCrossRef Manjurano A, Okell L, Lukindo T, et al. Association of sub-microscopic malaria parasite carriage with transmission intensity in North-Eastern Tanzania. Malar J. 2011;10:370.PubMedPubMedCentralCrossRef
48.
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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
49.
go back to reference Ouedraogo AL, Bousema T, Schneider P, 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.PubMedPubMedCentralCrossRef Ouedraogo AL, Bousema T, Schneider P, 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.PubMedPubMedCentralCrossRef
50.
go back to reference Schneider P, Bousema JT, Gouagna LC, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007;76(3):470–4.PubMedCrossRef Schneider P, Bousema JT, Gouagna LC, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007;76(3):470–4.PubMedCrossRef
51.
go back to reference Bretscher MT, Maire N, Felger I, Owusu-Agyei S, Smith T. Asymptomatic Plasmodium falciparum infections may not be shortened by acquired immunity. Malar J. 2015;14:294.PubMedPubMedCentralCrossRef Bretscher MT, Maire N, Felger I, Owusu-Agyei S, Smith T. Asymptomatic Plasmodium falciparum infections may not be shortened by acquired immunity. Malar J. 2015;14:294.PubMedPubMedCentralCrossRef
54.
go back to reference O'Meara WP, Mwangi TW, Williams TN, McKenzie FE, Snow RW, Marsh K. Relationship between exposure, clinical malaria, and age in an area of changing transmission intensity. Am J Trop Med Hyg. 2008;79(2):185–91.PubMedPubMedCentralCrossRef O'Meara WP, Mwangi TW, Williams TN, McKenzie FE, Snow RW, Marsh K. Relationship between exposure, clinical malaria, and age in an area of changing transmission intensity. Am J Trop Med Hyg. 2008;79(2):185–91.PubMedPubMedCentralCrossRef
55.
go back to reference Kaneko A, Taleo G, Kalkoa M, Yamar S, Kobayakawa T, Bjorkman A. Malaria eradication on islands. Lancet. 2000;356(9241):1560–4.PubMedCrossRef Kaneko A, Taleo G, Kalkoa M, Yamar S, Kobayakawa T, Bjorkman A. Malaria eradication on islands. Lancet. 2000;356(9241):1560–4.PubMedCrossRef
56.
go back to reference Aregawi MW, Ali AS, Al-mafazy AW, et al. Reductions in malaria and anaemia case and death burden at hospitals following scale-up of malaria control in Zanzibar, 1999-2008. Malar J. 2011;10:46.PubMedPubMedCentralCrossRef Aregawi MW, Ali AS, Al-mafazy AW, et al. Reductions in malaria and anaemia case and death burden at hospitals following scale-up of malaria control in Zanzibar, 1999-2008. Malar J. 2011;10:46.PubMedPubMedCentralCrossRef
57.
go back to reference Molineaux L. Nature’s experiment: what implications for malaria prevention? Lancet. 1997;349(9066):1636–7.PubMedCrossRef Molineaux L. Nature’s experiment: what implications for malaria prevention? Lancet. 1997;349(9066):1636–7.PubMedCrossRef
58.
go back to reference Scott JA, Berkley JA, Mwangi I, et al. Relation between falciparum malaria and bacteraemia in Kenyan children: a population-based, case-control study and a longitudinal study. Lancet. 2011;378(9799):1316–23.PubMedPubMedCentralCrossRef Scott JA, Berkley JA, Mwangi I, et al. Relation between falciparum malaria and bacteraemia in Kenyan children: a population-based, case-control study and a longitudinal study. Lancet. 2011;378(9799):1316–23.PubMedPubMedCentralCrossRef
59.
go back to reference Björkman A, Cook J, Sturrock H, et al. Spatial distribution of falciparum malaria infections in Zanzibar: implications for focal drug administration strategies targeting asymptomatic parasite carriers. Clin Infect Dis. 2017;64:1236–43.PubMedPubMedCentralCrossRef Björkman A, Cook J, Sturrock H, et al. Spatial distribution of falciparum malaria infections in Zanzibar: implications for focal drug administration strategies targeting asymptomatic parasite carriers. Clin Infect Dis. 2017;64:1236–43.PubMedPubMedCentralCrossRef
60.
go back to reference Cook J, Xu W, Msellem M, Vonk M, et al. Mass screening and treatment on the basis of results of a Plasmodium falciparum-specific rapid diagnostic test did not reduce malaria incidence in Zanzibar. J Infect Dis. 2015;211:1476–83.PubMedCrossRef Cook J, Xu W, Msellem M, Vonk M, et al. Mass screening and treatment on the basis of results of a Plasmodium falciparum-specific rapid diagnostic test did not reduce malaria incidence in Zanzibar. J Infect Dis. 2015;211:1476–83.PubMedCrossRef
61.
go back to reference Aydin-Schmidt B, Morris U, Ding XC, et al. Field evaluation of a high throughput loop mediated isothermal amplification test for the detection of asymptomatic plasmodium infections in Zanzibar. PLoS One. 2017;12(1):e 0169037.CrossRef Aydin-Schmidt B, Morris U, Ding XC, et al. Field evaluation of a high throughput loop mediated isothermal amplification test for the detection of asymptomatic plasmodium infections in Zanzibar. PLoS One. 2017;12(1):e 0169037.CrossRef
62.
go back to reference Morris U, Khamis M, Aydin-Schmidt B, Abass AK, Msellem MI, Nassor MH, Gonzalez IJ, Martensson A, Ali AS, Bjorkman A, et al. Field deployment of loop-mediated isothermal amplification for centralized mass-screening of asymptomatic malaria in Zanzibar: a pre-elimination setting. Malar J. 2015;14:205.PubMedPubMedCentralCrossRef Morris U, Khamis M, Aydin-Schmidt B, Abass AK, Msellem MI, Nassor MH, Gonzalez IJ, Martensson A, Ali AS, Bjorkman A, et al. Field deployment of loop-mediated isothermal amplification for centralized mass-screening of asymptomatic malaria in Zanzibar: a pre-elimination setting. Malar J. 2015;14:205.PubMedPubMedCentralCrossRef
63.
go back to reference Morris U, Msellem M, Mkali H, Islam A, Aydin-Schmidt B, Jovel I, Shija S, Khamis M, Mohammed Ali S, Hodzic L, Magnusson E, Poirot E, Bennett A, Sachs M, Tärning J, Mårtensson A, Ali AS, Björkman A. A cluster randomised controlled trial of two rounds of mass drug administration in Zanzibar, a malaria pre-elimination setting – high coverage and safety, but no significant impact on transmission. Submitted to BMC medicine on 9th July 2018. Morris U, Msellem M, Mkali H, Islam A, Aydin-Schmidt B, Jovel I, Shija S, Khamis M, Mohammed Ali S, Hodzic L, Magnusson E, Poirot E, Bennett A, Sachs M, Tärning J, Mårtensson A, Ali AS, Björkman A. A cluster randomised controlled trial of two rounds of mass drug administration in Zanzibar, a malaria pre-elimination setting – high coverage and safety, but no significant impact on transmission. Submitted to BMC medicine on 9th July 2018.
64.
go back to reference Greenwood B. Review: intermittent preventive treatment--a new approach to the prevention of malaria in children in areas with seasonal malaria transmission. Trop Med Int Health. 2006;11(7):983–91.PubMedCrossRef Greenwood B. Review: intermittent preventive treatment--a new approach to the prevention of malaria in children in areas with seasonal malaria transmission. Trop Med Int Health. 2006;11(7):983–91.PubMedCrossRef
66.
Metadata
Title
From high to low malaria transmission in Zanzibar—challenges and opportunities to achieve elimination
Authors
A. Björkman
D. Shakely
A. S. Ali
U. Morris
H. Mkali
A. K. Abbas
A-W Al-Mafazy
K. A. Haji
J. Mcha
R. Omar
J. Cook
K. Elfving
M. Petzold
M. C. Sachs
B. Aydin-Schmidt
C. Drakeley
M. Msellem
A. Mårtensson
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Malaria
Published in
BMC Medicine / Issue 1/2019
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/s12916-018-1243-z

Other articles of this Issue 1/2019

BMC Medicine 1/2019 Go to the issue