Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, Battle KE, Moyes CL, Henry A, Eckhoff PA, Wenger EA, Briet O, Penny MA, Smith TA, Bennett A, Yukich J, Eisele TP, Griffin JT, Fergus CA, Lynch M, Lindgren F, Cohen JM, Murray CLJ, Smith DL, Hay SI, 2015. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526: 207–211.
Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, Hinsley W, Bousema T, Drakeley CJ, Ferguson NM, Basáñez MG, Ghani AC, 2010. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med 7.
Lindblade K, Steinhardt L, Samuels A, Kachur SP, Slutsker L, 2013. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti Infect Ther 11: 623–639.
Ouédraogo AL, Gonçalves BP, Gnémé A, Wenger EA, Guelbeogo MW, Ouédraogo A, Gerardin J, Bever CA, Lyons H, Pitroipa X, Verhave JP, Eckhoff PA, Drakeley C, Sauerwein R, Luty AJ, Kouyaté B, Bousema T, 2015. Dynamics of the human infectious reservoir for malaria determined by mosquito feeding assays and ultrasensitive malaria diagnosis in Burkina Faso. J Infect Dis 213: 90–99.
Gerardin J, Ouédraogo AL, McCarthy K, Eckhoff P, Wenger E, 2015. Characterization of the infectious reservoir of malaria with an agent-based model calibrated to age-stratified parasite densities and infectiousness. Malar J 14: 231.
Bousema T, Okell L, Felger I, Drakeley C, 2014. Asymptomatic malaria infections: detectability, transmissibility and public health relevance. Nat Rev Microbiol 12: 833–840.
Newby G, Hwang J, Koita K, Chen I, Greenwood B, von Seidlein L, Shanks GD, Slutsker LM, Kachur SP, Wegbreit J, Ippolito MM, Poirot E, Gosling R, 2015. Review of mass drug administration for malaria and its operational challenges. Am J Trop Med Hyg 93: 125–134.
Bottius E, Guanzirolli A, Trape J, Rogier C, Konate L, Druilhe P, 1996. Malaria: even more chronic in nature than previously thought; evidence for subpatent parasitaemia detectable by the polymerase chain reaction. Trans R Soc Trop Med Hyg 90: 15–19.
Kyabayinze DJ, Tibenderana JK, Odong GW, Rwakimari JB, Counihan H, 2008. Operational accuracy and comparative persistent antigenicity of HRP2 rapid diagnostic tests for Plasmodium falciparum malaria in a hyperendemic region of Uganda. Malar J 7: 221.
Ochola LB, Vounatsou P, Smith TA, Mabaso MLH, Newton CRJC, 2006. The reliability of diagnostic techniques in the diagnosis and management of malaria in the absence of a gold standard. Lancet Infect Dis 6: 582–588.
World Health Organization, 2014. Malaria Rapid Diagnostics Test Performance: Results of WHO Product Testing of Malaria RDTs (Round 5). Vol 1. Available at: http://www.finddiagnostics.org/export/sites/default/resource-centre/reports_brochures/docs/malaria_rdt_results_Round5_eng.pdf.
Tiono AB, Guelbeogo MW, Sagnon N, Nébié I, Sirima SB, Mukhopadhyay A, Hamed K, 2013. Dynamics of malaria transmission and susceptibility to clinical malaria episodes following treatment of Plasmodium falciparum asymptomatic carriers: results of a cluster-randomized study of community-wide screening and treatment and a parallel entomology. BMC Infect Dis 13: 535.
Bell D, Wongsrichanalai C, Barnwell JW, 2006. Ensuring quality and access for malaria diagnosis: how can it be achieved? Nat Rev Microbiol 4: 682–695.
Cook J, Xu X, Msellem MI, Vonk M, Bergström B, Gosling R, Al-Mafazy AW, McElroy P, Molteni F, Abass AK, Garimo I, Ramsan M, Ali A, Mårtensson A, Björkman A, 2015. 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 211: 1476–1483.
Wu L, van den Hoogen LL, Slater H, Walker PGT, Ghani AC, Drakeley CJ, Okell LC, 2015. Comparison of diagnostics for the detection of asymptomatic Plasmodium falciparum infections to inform control and elimination strategies. Nature 528: S86–S93.
Okell LC, Ghani AC, Lyons E, Drakeley CJ, 2009. Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. J Infect Dis 200: 1509–1517.
Okell LC, Bousema T, Griffin JT, Ouédraogo AL, Ghani AC, Drakeley CJ, 2012. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun 3: 1237.
Jenkins R, Omollo R, Ongecha M, Sifuna P, Othieno C, Ongeri L, Kingora J, Ogutu B, 2015. Prevalence of malaria parasites in adults and its determinants in malaria endemic area of Kisumu County, Kenya. Malar J 14: 263.
Geiger C, Agustar HK, Compaoré G, Coulibaly B, Sié A, Becher H, Lanzer M, Jänisch T, 2013. Declining malaria parasite prevalence and trends of asymptomatic parasitaemia in a seasonal transmission setting in north-western Burkina Faso between 2000 and 2009–2012. Malar J 12: 27.
Owusu-Agyei S, Smith T, Beck HP, Amenga-Etego L, Felger I, 2002. Molecular epidemiology of Plasmodium falciparum infections among asymptomatic inhabitants of a holoendemic malarious area in northern Ghana. Trop Med Int Health 7: 421–428.
Koram KA, Owusu-Agyei S, Fryauff DJ, Anto F, Atuguba F, Hodgson A, Holfman SL, Nkrumah FK, 2003. Seasonal profiles of malaria infection, anaemia, and bednet use among age groups and communities in northern Ghana. Trop Med Int Health 8: 793–802.
Sama W, Owusu-Agyei S, Felger I, Dietz K, Smith T, 2006. Age and seasonal variation in the transition rates and detectability of Plasmodium falciparum malaria. Parasitology 132: 13–21.
Felger I, Maire M, Bretscher MT, Falk N, Tiaden A, Sama W, Beck HP, Owusu-Agyei S, Smith TA, 2012. The dynamics of natural Plasmodium falciparum infections. PLoS One 7: 1–10.
Bongo District Assembly, 2014. District Medium Term Development Plan (2010–2013). Ghana: Bongo District. Available at: https://s3.amazonaws.com/ndpc-static/CACHES/PUBLICATIONS/2016/04/16/UE_Bongo_2010-2013+DMTDP.pdf.
Ghana Statistical Service, 2014. 2010 Population and Housing Census: Bongo District. Ghana: Ghana Statistical Service. Available at: http://www.statsghana.gov.gh/docfiles/2010_District_Report/Upper%20East/Bongo.pdf.
Sakeah E, Doctor HV, McCloskey L, Bernstein J, Yeboah-Antwi K, Mills S, 2014. Using the community-based health planning and services program to promote skilled delivery in rural Ghana: socio-demographic factors that influence women utilization of skilled attendants at birth in northern Ghana. BMC Public Health 14: 344.
Akurugu BA, Zango MS, Abanyie SK, Ampofo S, Region UE, 2015. Assessing the impact of a dam on the livelihood of surrounding communities : a case study of Vea Dam in the Upper East Region of Ghana. J Environ Earth Sci 5: 20–26.
United Nations Children's Emergency Fund (UNICEF), 2012. UNICEF Annual Report 2012 for Ghana, WCARO. New York, NY: UNICEF. Available at: https://www.unicef.org/about/annualreport/files/Ghana_COAR_2012.pdf.
WHO/UNICEF/UNU, 2001. Iron Deficiency Anaemia: Assessment, Prevention and Control, a Guide for Programme Managers .Available at: http://www.who.int/nutrition/publications/micronutrients/anaemia_iron_deficiency/WHO_NHD_01.3/en/index.html.
WHO/NMH/NHD/MNM, 2011. Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity. Geneva, Switzerland: World Health Organization. Available at: http://apps.who.int/iris/bitstream/10665/85839/3/WHO_NMH_NHD_MNM_11.1_eng.pdf7.
GHS/MOH, 2013. Final Report: National Malaria Control Programme Ghana (Ministry of Health, Ghana Health Service). Ghana: MOH/GHS. Availabl at: https://www.ghanahealthservice.org/downloads/ghana_malaria_programme_review_final_report_june_2013.pdf.
World Health Organization, 2010. Basic Malaria Microscopy: Part I. Learner's Guide, 2nd edition. Geneva, Switzerland: World Health Organization.
Laishram DD, Sutton PL, Nanda N, Sharma VL, Sobti RC, Carlton JM, Joshi H, 2012. The complexities of malaria disease manifestations with a focus on asymptomatic malaria. Malar J 11: 29.
de Mast Q, Syafruddin D, Keijmel S, Olde Riekerink T, Deky O, Asih P, Swinkels D, van der Ven A, 2010. Increased serum hepcidin and alterations in blood iron parameters associated with asymptomatic P. falciparum and P. vivax malaria. Haematologica 95: 1068–1074.
Leoratti F, Durlacher R, Lacerda M, Alecrim M, Ferreira A, Sanchez M, Moraes S, 2008. Pattern of humoral immune response to Plasmodium falciparum blood stages in individuals presenting different clinical expressions of malaria. Malar J 7: 186.
Males S, Gaye O, Garcia A, 2008. Long-term asymptomatic carriage of Plasmodium falciparum protects from malaria attacks: a prospective study among Senegalese children. Clin Infect Dis 46: 516–522.
Duarte J, Deshpande P, Guiyedi V, Mecheri S, Fesel C, Cazenave P, Mishra G, Kombila M, Pied S, 2007. Total and functional parasite specific IgE responses in Plasmodium falciparum-infected patients exhibiting different clinical status. Malar J 6: 31.
Snounou G, Viriyakosol S, Xin PZ, Jarra W, Pinheiro L, do Rosario VE, Thaithong S, Brown KN, Zhu X, 1993. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol 61: 315–320.
Boonma P, Christensen PR, Suwanarusk R, Price RN, Russell B, Lek-Uthai U, 2007. Comparison of three molecular methods for the detection and speciation of Plasmodium vivax and Plasmodium falciparum .Malar J 6: 124.
Snounou G, Zhu X, Siripoon N, Jarra W, Thaithong S, Brown KN, Viriyakosol S, 1999. Biased distribution of msp1 and msp2 allelic variants in Plasmodium falciparum populations in Thailand. Trans R Soc Trop Med Hyg 93: 369–374.
Snow RW, Marsh K, 1998. New insights into the epidemiology of malaria relevant for disease control. Br Med Bull 54: 293–309.
Owusu EDA, Buabeng V, Dadzie S, Brown CA, Grobusch MP, Mens P, 2016. Characteristics of asymptomatic Plasmodium spp. parasitaemia in Kwahu-Mpraeso, a malaria endemic mountainous district in Ghana, west Africa. Malar J 15: 38.
Smith DL, Guerra CA, Snow RW, Hay SI, 2007. Standardizing estimates of the Plasmodium falciparum parasite rate. Malar J 6: 131.
Pegha Moukandja I, Biteghe Bi Essone JC, Sagara I, Kassa Kassa RF, Ondzaga J, Lékana Douki J-B, Bouyou Akotet M, Nkoghe Mba D, Touré Ndouo FS, 2016. Marked rise in the prevalence of asymptomatic Plasmodium falciparum infection in rural Gabon. PLoS One 11: e0153899.
Lalloo DG, Olukoya P, Olliaro P, 2006. Malaria in adolescence: burden of disease, consequences, and opportunities for intervention. Lancet Infect Dis 6: 780–793.
Yimer F, Animut A, Erko B, Mamo H, 2015. Past five-year trend, current prevalence and household knowledge, attitude and practice of malaria in Abeshge, south-central Ethiopia. Malar J 14: 230.
Stresman GH, Stevenson JC, Ngwu N, Marube E, Owaga C, Drakeley C, Bousema T, Cox J, 2014. High levels of asymptomatic and subpatent Plasmodium falciparum parasite carriage at health facilities in an area of heterogeneous malaria transmission intensity in the Kenyan highlands. Am J Trop Med Hyg 91: 1101–1108.
Rek J, Katrak S, Obasi H, Nayebare P, Katureebe A, Kakande E, Arinaitwe E, Nankabirwa JI, Jagannathan P, Drakeley C, Staedke SG, Smith DL, Bousema T, Kamya M, Rosenthal PJ, Dorsey G, Greenhouse B, 2016. Characterizing microscopic and submicroscopic malaria parasitaemia at three sites with varied transmission intensity in Uganda. Malar J 15: 470.
Doolan DL, Dobaño C, Baird JK, 2009. Acquired immunity to malaria. Clin Microbiol Rev 22: 13–36.
Langhorne J, Ndungu FMM, Sponaas A-M, Marsh K, 2008. Immunity to malaria: more questions than answers. Nat Immunol 9: 725–732.
Roca-Feltrer A, Schellenberg JRMA, Smith L, Carneiro I, 2009. A simple method for defining malaria seasonality. Malar J 8: 276.
Smith T, Charlwood JD, Kihonda J, Mwankusye S, Billingsley P, Meuwissen J, Lyimo E, Takken W, Teuscher T, Tanner M, 1993. Absence of seasonal variation in malaria parasitaemia in an area of intense seasonal transmission. Acta Trop 54: 55–72.
Tiono AB, Ouédraogo A, Ogutu B, Diarra A, Coulibaly S, Gansané A, Sirima SB, O'Neil G, Mukhopadhyay A, Hamed K, 2013. A controlled, parallel, cluster-randomized trial of community-wide screening and treatment of asymptomatic carriers of Plasmodium falciparum in Burkina Faso. Malar J 12: 79.
Dal-Bianco MP, Köster KB, Kombila UD, Kun JFJ, Grobusch MP, Ngoma GM, Matsiegui PB, Supan C, Ospina Salazar CL, Missinou MA, Issifou S, Lell B, Kremsner P, 2007. High prevalence of asymptomatic Plasmodium falciparum infection in Gabonese adults. Am J Trop Med Hyg 77: 939–942.
Baume CA, Franca-Koh AC, 2011. Predictors of mosquito net use in Ghana. Malar J 10: 2–7.
Baume CA, Marin C, Franca-Koh AC, 2009. NetMark 2008 Household Survey on Insecticide-Treated Nets in Ghana. AED/USAID. Available at: http://pdf.usaid.gov/pdf_docs/Pnado570.pdf.
Steketee RW, Nahlen BL, Parise ME, Menendez C, 2001. The burden of malaria in pregnancy in malaria-endemic areas. Am J Trop Med Hyg 64: 28–35.
Duffy PE, Fried M, 2005. Malaria in the pregnant woman. Curr Top Microbiol Immunol 295: 169–200.
Arahman SH, Mohamedani AA, Mirgani EM, Ibrahim AM, 1996. Gender aspects and women's participation in the control and management of malaria in central Sudan. Soc Sci Med 42: 1433–1446.
Müller I, Smith T, Mellor S, Rare L, Genton B, 1998. The effect of distance from home on attendance at a small rural health centre in Papua New Guinea. Int J Epidemiol 27: 878–884.
Reuben R, 1993. Women and malaria-special risks and appropriate control strategy. Soc Sci Med 37: 473–480.
van Eijk AM, Hill J, Noor AM, Snow RW, ter Kuile FO, 2015. Prevalence of malaria infection in pregnant women compared with children for tracking malaria transmission in sub-Saharan Africa: a systematic review and meta-analysis. Lancet Glob Health 3: e617–e628.
Chen I, Clarke SE, Gosling R, Hamainza B, Killeen G, Magill A, O'Meara W, Price RN, Riley EM, 2016. “Asymptomatic” malaria: a chronic and debilitating infection that should be treated. PLoS Med 13: e1001942.
Okell LC, Griffin JT, Kleinschmidt I, Hollingsworth TD, Churcher TS, White MJ, Bousema T, Drakeley CJ, Ghani AC, 2011. The potential contribution of mass treatment to the control of Plasmodium falciparum malaria. PLoS One 6.
von Seidlein L, Walraven G, Milligan PJM, Alexander N, Manneh F, Deen JL, Coleman R, Jawara M, Lindsay SW, Drakeley C, De Martin S, Olliaro P, Bennett S, van der Loeff MS, Okunoye K, Targett GA, McAdam KP, Doherty JF, Greenwood BM, Pinder M, 2003. The effect of mass administration of sulfadoxine-pyrimethamine combined with artesunate on malaria incidence: a double-blind, community-randomized, placebo-controlled trial in the Gambia. Trans R Soc Trop Med Hyg 97: 217–225.
Shekalaghe SA, Drakeley C, van den Bosch S, ter Braak R, van den Bijllaardt W, Mwanziva C, Semvua S, Masokoto A, Mosha F, Teelen K, Hermsen R, Okell L, Gosling R, Sauerwein R, Bousema T, 2011. A cluster-randomized trial of mass drug administration with a gametocytocidal drug combination to interrupt malaria transmission in a low endemic area in Tanzania. Malar J 10: 247.
Poirot E, Skarbinski J, Sinclair D, Kachur SP, Slutsker L, Hwang J, 2013. Mass drug administration for malaria. Cochrane Database Syst Rev 12: CD008846.
Kern SE, Tiono AB, Makanga M, Gbadoé AD, Premji Z, Gaye O, Sagara I, Ubben D, Cousin M, Oladiran F, Sander O, Ogutu B, 2011. Community screening and treatment of asymptomatic carriers of Plasmodium falciparum with artemether-lumefantrine to reduce malaria disease burden: a modelling and simulation analysis. Malar J 10: 210.
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Understanding the epidemiology of asymptomatic Plasmodium falciparum infections is critical for countries to move toward malaria elimination. Using different methods for parasite detection, we evaluated how seasonality, spatial location, and other factors affect the age-specific epidemiology of asymptomatic malaria in Bongo District, Ghana. Asymptomatic prevalence by microscopy decreased significantly from 42.5% at the end of the wet to 27.5% at the end of the dry season (P < 0.001). Using the 18S rRNA polymerase chain reactions (PCRs), all microscopy-negative samples were screened and prevalence of submicroscopic infections also decreased significantly from the wet (55.4%) to the dry (20.7%) season (P < 0.001). Combining detection methods, 74.4% and 42.5% of the population in the wet and dry seasons, respectively, had evidence of a P. falciparum infection. Interestingly in those > 20 years of age, we found evidence of infection in 64.3% of the population in the wet and 27.0% in the dry season. Using both microscopy and PCR, the asymptomatic P. falciparum reservoir peaks at the end of the wet season and infections in all age groups constitute the reservoir of malaria infection. At the end of the wet season, spatial heterogeneity in the prevalence and density of P. falciparum infections was observed between the two catchment areas surveyed in Bongo District. These results indicate that if elimination is to succeed, interventions will need to target not just P. falciparum infections in children but also in adults, and be implemented toward the end of the dry season in this area of West Africa.
Financial support: This research was supported by the Fogarty International Center at National Institutes of Health (Program on the Ecology and Evolution of Infectious Diseases (EEID), Grant number: R01-TW009670); and the National Institute of Allergy and Infectious Disease, National Institutes of Health (Grant number: R01-AI084156).
Authors' addresses: Kathryn E. Tiedje, School of BioSciences, Bio21 Institute/University of Melbourne, Melbourne, Australia, E-mail: firstname.lastname@example.org. Abraham R. Oduro, Godfred Agongo, Thomas Anyorigiya, Daniel Azongo, and Timothy Awine, Navrongo Health Research Center, Navrongo, Ghana, E-mails: email@example.com, firstname.lastname@example.org, email@example.com, firstname.lastname@example.org, and email@example.com. Anita Ghansah, Noguchi Memorial Institute for Medical Research, University of Ghana, Legon, Ghana, E-mail: firstname.lastname@example.org. Mercedes Pascual, Department of Ecology and Evolution, University of Chicago, Chicago, IL, E-mail: email@example.com. Kwadwo A. Koram, Noguchi Memorial Institute for Medical Research, University of Ghana, Legon, Ghana, E-mail: firstname.lastname@example.org. Karen P. Day, School of Biosciences, University of Melbourne, Melbourne, Australia, E-mail: email@example.com.