Malaria Transmission, Infection, and Disease at Three Sites with Varied Transmission Intensity in Uganda: Implications for Malaria Control

Moses R. Kamya Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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Emmanuel Arinaitwe Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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Humphrey Wanzira Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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Agaba Katureebe Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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Chris Barusya Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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Simon P. Kigozi Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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Maxwell Kilama Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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Andrew J. Tatem Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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Philip J. Rosenthal Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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Chris Drakeley Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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Steve W. Lindsay Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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Sarah G. Staedke Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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David L. Smith Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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Bryan Greenhouse Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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Grant Dorsey Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda; Infectious Diseases Research Collaboration, Kampala, Uganda; Department of Geography and Environment, University of Southampton, Southampton, United Kingdom; Department of Medicine, San Francisco General Hospital, University of California, San Francisco, California; London School of Hygiene and Tropical Medicine, London, United Kingdom; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom; Department of Zoology, University of Oxford, United Kingdom; Sanaria Institute for Global Health and Tropical Medicine, Rockville, Maryland

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The intensification of control interventions has led to marked reductions in malaria burden in some settings, but not others. To provide a comprehensive description of malaria epidemiology in Uganda, we conducted surveillance studies over 24 months in 100 houses randomly selected from each of three subcounties: Walukuba (peri-urban), Kihihi (rural), and Nagongera (rural). Annual entomological inoculation rate (aEIR) was estimated from monthly Centers for Disease Control and Prevention (CDC) light trap mosquito collections. Children aged 0.5–10 years were provided long-lasting insecticidal nets (LLINs) and followed for measures of parasite prevalence, anemia and malaria incidence. Estimates of aEIR were 2.8, 32.0, and 310 infectious bites per year, and estimates of parasite prevalence 7.4%, 9.3%, and 28.7% for Walukuba, Kihihi, and Nagongera, respectively. Over the 2-year study, malaria incidence per person-years decreased in Walukuba (0.51 versus 0.31, P = 0.001) and increased in Kihihi (0.97 versus 1.93, P < 0.001) and Nagongera (2.33 versus 3.30, P < 0.001). Of 2,582 episodes of malaria, only 8 (0.3%) met criteria for severe disease. The prevalence of anemia was low and not associated with transmission intensity. In our cohorts, where LLINs and prompt effective treatment were provided, the risk of complicated malaria and anemia was extremely low. However, malaria incidence was high and increased over time at the two rural sites, suggesting improved community-wide coverage of LLIN and additional malaria control interventions are needed in Uganda.

Author Notes

* Address correspondence to Moses R. Kamya, Department of Medicine, Makerere University College of Health Sciences, P.O. Box 7072, Kampala, Uganda. E-mail: mkamya@infocom.co.ug

Financial support: Funding was provided by the National Institutes of Health as part of the International Centers of Excellence in Malaria Research (ICMER) program (U19AI089674).

Authors' addresses: Moses R. Kamya, Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda, E-mail: mkamya@infocom.co.ug. Emmanuel Arinaitwe, Humphrey Wanzira, Agaba Katureebe, Chris Barusya, Simon P. Kigozi, and Maxwell Kilama, Infectious Diseases Research Collaboration, Kampala, Uganda, E-mails: emmy3md@yahoo.com, wanzirah@yahoo.com, agabaik@gmail.com, cbarusya@gmail.com, skigozi@yahoo.com, and kilamam@gmail.com. Andrew J. Tatem, Department of Geography and Environment, University of Southampton, Southampton, UK, E-mail: andy.tatem@gmail.com. Philip J. Rosenthal, Bryan Greenhouse, and Grant Dorsey, Department of Medicine, San Francisco General Hospital, University of California, San Francisco, CA, E-mails: prosenthal@medsfgh.ucsf.edu, bgreenhouse@medsfgh.ucsf.edu, and gdorsey@medsfgh.ucsf.edu. Chris Drakeley and Sarah G. Staedke, London School of Hygiene and Tropical Medicine, London, UK, E-mails: chris.drakeley@lshtm.ac.uk and sarah.staedke@lshtm.ac.uk. Steve W. Lindsay, School of Biological and Biomedical Sciences, Durham University, Durham, UK, E-mail: s.w.lindsay@durham.ac.uk. David L. Smith, Department of Zoology, University of Oxford, Oxford, UK, and Sanaria Institute of Global Health and Tropical Medicine, Rockville, MD, E-mail: david.smith@zoo.ox.ac.uk.

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