Epidemiology of subpatent Plasmodium falciparum infection: implications for detection of hotspots with imperfect diagnostics

Mosha, Jacklin F; Sturrock, Hugh JW; Greenhouse, Bryan; Greenwood, Brian; Sutherland, Colin J; Gadalla, Nahla; Atwal, Sharan; Drakeley, Chris; Kibiki, Gibson; Bousema, Teun; Chandramohan, Daniel; Gosling, Roly

doi:10.1186/1475-2875-12-221

Cited by 114Malaria Research and ControlBird parasitology and diseasesTravel-related health issues

Epidemiology of subpatent Plasmodium falciparum infection: implications for detection of hotspots with imperfect diagnostics

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Mosha, Jacklin F, Sturrock, Hugh JW, Greenhouse, Bryan, Greenwood, Brian, Sutherland, Colin J, Gadalla, Nahla, Atwal, Sharan, Drakeley, Chris +4 more·2013·Malaria Journal

DOI 10.1186/1475-2875-12-221PMC PMC3701503

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Abstract

BACKGROUND: At the local level, malaria transmission clusters in hotspots, which may be a group of households that experience higher than average exposure to infectious mosquitoes. Active case detection often relying on rapid diagnostic tests for mass screen and treat campaigns has been proposed as a method to detect and treat individuals in hotspots. Data from a cross-sectional survey conducted in north-western Tanzania were used to examine the spatial distribution of Plasmodium falciparum and the relationship between household exposure and parasite density. METHODS: Dried blood spots were collected from consenting individuals from four villages during a survey conducted in 2010. These were analysed by PCR for the presence of P. falciparum, with the parasite density of positive samples being estimated by quantitative PCR. Household exposure was estimated using the distance-weighted PCR prevalence of infection. Parasite density simulations were used to estimate the proportion of infections that would be treated using a screen and treat approach with rapid diagnostic tests (RDT) compared to targeted mass drug administration (tMDA) and Mass Drug Administration (MDA). RESULTS: Polymerase chain reaction PCR analysis revealed that of the 3,057 blood samples analysed, 1,078 were positive. Mean distance-weighted PCR prevalence per household was 34.5%. Parasite density was negatively associated with transmission intensity with the odds of an infection being subpatent increasing with household exposure (OR 1.09 per 1% increase in exposure). Parasite density was also related to age, being highest in children five to ten years old and lowest in those > 40 years. Simulations of different tMDA strategies showed that treating all individuals in households where RDT prevalence was above 20% increased the number of infections that would have been treated from 43 to 55%. However, even with this strategy, 45% of infections remained untreated. CONCLUSION: The negative relationship between household exposure and parasite density suggests that DNA-based detection of parasites is needed to provide adequate sensitivity in hotspots. Targeting MDA only to households with RDT-positive individuals may allow a larger fraction of infections to be treated. These results suggest that community-wide MDA, instead of screen and treat strategies, may be needed to successfully treat the asymptomatic, subpatent parasite reservoir and reduce transmission in similar settings.

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Pregnancy poses a unique challenge for falciparum malaria diagnosis because parasites sequester in the placenta and circulating parasitaemia is very low and therefore undetectable by peripheral blood smear microscopy or rapid diagnostic test.
“Pregnancy poses a unique challenge for falciparum malaria diagnosis, as parasites sequester in the placenta and the circulating parasitaemia is very low and therefore undetectable by peripheral blood smear microscopy or rapid diagnostic test [7–10].”
From Intermittent preventive treatment with Sulphadoxine-Pyrimethamine (IPTp-SP) is associated with protection against sub-microscopic P. falciparum infection in pregnant women during the low transmission dry season in southwestern Cameroon: A Semi - longitudinal study (2022) · cites this paper as [10]
Submicroscopic P. falciparum infections may negatively affect health and constitute reservoirs for continued disease transmission because they are usually asymptomatic and remain untreated during pregnancy.
“Such submicroscopic infections may negatively affect health and constitute reservoirs for continued disease transmission [10] since they are usually asymptomatic and therefore remain untreated during pregnancy.”
From Intermittent preventive treatment with Sulphadoxine-Pyrimethamine (IPTp-SP) is associated with protection against sub-microscopic P. falciparum infection in pregnant women during the low transmission dry season in southwestern Cameroon: A Semi - longitudinal study (2022) · cites this paper as [10]
The possibility of overestimating ITN use due to self-reporting cannot be excluded.
“The possibility of overestimating ITNs use due to self-reporting cannot be excluded as the participant may try to please the interviewer [10].”
From Intermittent preventive treatment with Sulphadoxine-Pyrimethamine (IPTp-SP) is associated with protection against sub-microscopic P. falciparum infection in pregnant women during the low transmission dry season in southwestern Cameroon: A Semi - longitudinal study (2022) · cites this paper as [10]
These infections could become an emergency or evolve to severe disease if undetected or diagnosis was delayed.
“and could, therefore, become an emergency [10] or evolve to severe disease if undetected or diagnosis was delayed.”
From Intermittent preventive treatment with Sulphadoxine-Pyrimethamine (IPTp-SP) is associated with protection against sub-microscopic P. falciparum infection in pregnant women during the low transmission dry season in southwestern Cameroon: A Semi - longitudinal study (2022) · cites this paper as [10]
Low-density parasitemias serve as a reservoir for continued transmission of malaria and may contribute to negative health.
“These low-density parasitemias serve as a reservoir for continued transmission of the disease and may contribute to negative health. 9-11”
From What is the burden of submicroscopic malaria in pregnancy in central India? (2015) · cites this paper as [10]

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Submicroscopic and Asymptomatic Plasmodium Parasitaemia Associated with Significant Risk of Anaemia in Papua, Indonesia
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PET-PCR method for the molecular detection of malaria parasites in a national malaria surveillance study in Haiti, 2011
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Effect of transmission intensity on hotspots and micro-epidemiology of malaria in sub-Saharan Africa
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Malaria hotspots defined by clinical malaria, asymptomatic carriage, PCR and vector numbers in a low transmission area on the Kenyan Coast
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Detecting Malaria Hotspots: A Comparison of Rapid Diagnostic Test, Microscopy, and Polymerase Chain Reaction
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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
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The essential role of infection-detection technologies for malaria elimination and eradication
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Evaluation of the operational challenges in implementing reactive screen-and-treat and implications of reactive case detection strategies for malaria elimination in a region of low transmission in southern Zambia
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High-resolution metabolomics to discover potential parasite-specific biomarkers in a Plasmodium falciparum erythrocytic stage culture system
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A Quality Control Program within a Clinical Trial Consortium for PCR Protocols To Detect Plasmodium Species
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Optimal Population-Level Infection Detection Strategies for Malaria Control and Elimination in a Spatial Model of Malaria Transmission
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Using health facility-based serological surveillance to predict receptive areas at risk of malaria outbreaks in elimination areas
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Plasmodium falciparum transcription in different clinical presentations of malaria associates with circulation time of infected erythrocytes
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An assessment of the supply, programmatic use, and regulatory issues of single low-dose primaquine as a Plasmodium falciparum gametocytocide for sub-Saharan Africa
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Efficiency of a Malaria Reactive Test-and-Treat Program in Southern Zambia: A Prospective, Observational Study
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School-Based Countrywide Seroprevalence Survey Reveals Spatial Heterogeneity in Malaria Transmission in the Gambia
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Antibody responses to a suite of novel serological markers for malaria surveillance demonstrate strong correlation with clinical and parasitological infection across seasons and transmission settings in The Gambia
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High cases of submicroscopic Plasmodium falciparum infections in a suburban population of Lagos, Nigeria
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Operational strategies of anti-malarial drug campaigns for malaria elimination in Zambia’s southern province: a simulation study
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Spatial Distribution of Falciparum Malaria Infections in Zanzibar: Implications for Focal Drug Administration Strategies Targeting Asymptomatic Parasite Carriers
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Challenges in Laboratory Diagnosis of Malaria in a Low-Resource Country at Tertiary Care in Eastern Nepal: A Comparative Study of Conventional vs. Molecular Methodologies
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Diagnostic performance and comparison of ultrasensitive and conventional rapid diagnostic test, thick blood smear and quantitative PCR for detection of low-density Plasmodium falciparum infections during a controlled human malaria infection study in Equatorial Guinea
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Use of epidemiological and entomological tools in the control and elimination of malaria in Ethiopia
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Clustering of asymptomatic Plasmodium falciparum infection and the effectiveness of targeted malaria control measures
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Performance evaluation of the highly sensitive histidine‐rich protein 2 rapid test for Plasmodium falciparum malaria in North-West Tanzania
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What is the burden of submicroscopic malaria in pregnancy in central India?
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Individual, household and neighborhood risk factors for malaria in the Democratic Republic of the Congo support new approaches to programmatic intervention
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Point prevalence of asymptomatic Plasmodium infection and the comparison of microscopy, rapid diagnostic test and nested PCR for the diagnosis of asymptomatic malaria among children under 5 years in Ghana
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Application of GIS to predict malaria hotspots based on Anopheles arabiensis habitat suitability in Southern Africa
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GIS-based stratification of malaria risk zones for Zimbabwe
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A Novel Model of Asymptomatic Plasmodium Parasitemia That Recapitulates Elements of the Human Immune Response to Chronic Infection
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Sample size and power calculations for detecting changes in malaria transmission using antibody seroconversion rate
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Operational research on malaria control and elimination: a review of projects published between 2008 and 2013
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Cost-effectiveness analysis of malaria rapid diagnostic test incentive schemes for informal private healthcare providers in Myanmar
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Evaluation of loop-mediated isothermal amplification as a surveillance tool for malaria in reactive case detection moving towards elimination
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Variation in infection length and superinfection enhance selection efficiency in the human malaria parasite
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Piloting a programme tool to evaluate malaria case investigation and reactive case detection activities: results from 3 settings in the Asia Pacific
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Molecular detection of P. vivax and P. ovale foci of infection in asymptomatic and symptomatic children in Northern Namibia
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Validation of three geolocation strategies for health-facility attendees for research and public health surveillance in a rural setting in western Kenya
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Study protocol for a cluster-randomized split-plot design trial to assess the effectiveness of targeted active malaria case detection among high-risk populations in Southern Lao PDR (the AcME-Lao study)
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An active and targeted survey reveals asymptomatic malaria infections among high-risk populations in Mondulkiri, Cambodia
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Core components, concepts and strategies for parasitic and vector-borne disease elimination with a focus on schistosomiasis: A landscape analysis
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Infectivity of Plasmodium falciparum in Malaria-Naive Individuals Is Related to Knob Expression and Cytoadherence of the Parasite
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Intermittent preventive treatment with Sulphadoxine-Pyrimethamine (IPTp-SP) is associated with protection against sub-microscopic P. falciparum infection in pregnant women during the low transmission dry season in southwestern Cameroon: A Semi - longitudinal study
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Dynamics of Afebrile Plasmodium falciparum Infections in Mozambican Men
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Significance of nested PCR testing for the detection of low-density malaria infection amongst febrile patients from the Malaria Elimination Demonstration Project in Mandla, Madhya Pradesh, India
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Utility of pf/pan RDT for diagnosis in the prevention of re-establishment of malaria in Sri Lanka
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Lessons for improved COVID-19 surveillance from the scale-up of malaria testing strategies
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Advancing digital methods in the fight against communicable diseases
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Prevalence of subpatent Plasmodium falciparum infections in regions with varying transmission intensities and implications for malaria elimination in Mainland TanzaniaPreprint
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Self-citation

Authors: Mosha, J. F., Sturrock, H. J., Greenhouse, B., Greenwood, B., Sutherland, C. J., Gadalla, N., Atwal, S., Drakeley, C., Kibiki, G., Bousema, T., Chandramohan, D., & Gosling, R.
Affiliations: National Institute for Medical Research (TZ)
University of California, San Francisco (US)
London School of Hygiene & Tropical Medicine (GB)
Kilimanjaro Christian Medical Centre (TZ)
Radboud University Medical Center (NL)
Corresponding author: Mosha, Jacklin F
ORCID: Mosha, Jacklin F
Sturrock, Hugh JW
Greenhouse, Bryan
Greenwood, Brian
Sutherland, Colin J
Gadalla, Nahla
Drakeley, Chris
Kibiki, Gibson
Bousema, Teun
Chandramohan, Daniel
Gosling, Roly
Venue: Malaria Journal
Publisher: Springer Science and Business Media LLC
Published: 2013-07-01
Volume: 12
Issue: 1
Pages: 221-221
ISSN: 1475-2875 (ISSN-L)
DOI: 10.1186/1475-2875-12-221
PMC: PMC3701503
OpenAlex: W2144009871
Cited by: 114
References: 40
Citations by year: 2026: 2 · 2025: 1 · 2024: 5 · 2023: 5 · 2022: 6 · 2021: 12 · 2020: 6 · 2019: 5 · 2018: 14 · 2017: 11 · 2016: 18 · 2015: 14 · 2014: 14 · 2013: 1
FWCI: 15.98
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/2.0 (tdm)
Locations: Malaria Journal (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
IHI Repository (acceptedVersion)
LSHTM Research Online (London School of Hygiene and Tropical Medicine) (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Radboud Repository (Radboud University) (submittedVersion)
Radboud Repository (Radboud University) (submittedVersion, other-oa)
Funders: Bill and Melinda Gates Foundation (OPP1013170)
Wellcome Trust (084289MA)
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
Life Sciences › Immunology and Microbiology › Parasitology › Bird parasitology and diseases
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Travel-related health issues
Keywords: Plasmodium falciparum, malaria hotspots, parasite density, household exposure, spatial distribution of infection, rapid diagnostic tests, mass drug administration, screen-and-treat, asymptomatic malaria, parasite reservoir, transmission intensity, northwestern Tanzania
MeSH terms: Adolescent, Adult, Blood, Child, Child, Preschool, Female, Humans, Infant, Male, Middle Aged, Plasmodium falciparum, Tanzania, DNA, Protozoan, Polymerase Chain Reaction, Malaria, Falciparum, Young Adult, Asymptomatic Infections, Parasite Load

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Epidemiology of subpatent Plasmodium falciparum infection: implications for detection of hotspots with imperfect diagnostics

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