Association between the proportion of Plasmodium falciparum and Plasmodium vivax infections detected by passive surveillance and the magnitude of the asymptomatic reservoir in the community: a pooled analysis of paired health facility and community data.


Journal

The Lancet. Infectious diseases
ISSN: 1474-4457
Titre abrégé: Lancet Infect Dis
Pays: United States
ID NLM: 101130150

Informations de publication

Date de publication:
08 2020
Historique:
received: 15 10 2019
revised: 23 01 2020
accepted: 28 01 2020
pubmed: 12 4 2020
medline: 8 9 2020
entrez: 12 4 2020
Statut: ppublish

Résumé

Passively collected malaria case data are the foundation for public health decision making. However, because of population-level immunity, infections might not always be sufficiently symptomatic to prompt individuals to seek care. Understanding the proportion of all Plasmodium spp infections expected to be detected by the health system becomes particularly paramount in elimination settings. The aim of this study was to determine the association between the proportion of infections detected and transmission intensity for Plasmodium falciparum and Plasmodium vivax in several global endemic settings. The proportion of infections detected in routine malaria data, P(Detect), was derived from paired household cross-sectional survey and routinely collected malaria data within health facilities. P(Detect) was estimated using a Bayesian model in 431 clusters spanning the Americas, Africa, and Asia. The association between P(Detect) and malaria prevalence was assessed using log-linear regression models. Changes in P(Detect) over time were evaluated using data from 13 timepoints over 2 years from The Gambia. The median estimated P(Detect) across all clusters was 12·5% (IQR 5·3-25·0) for P falciparum and 10·1% (5·0-18·3) for P vivax and decreased as the estimated log-PCR community prevalence increased (adjusted odds ratio [OR] for P falciparum 0·63, 95% CI 0·57-0·69; adjusted OR for P vivax 0·52, 0·47-0·57). Factors associated with increasing P(Detect) included smaller catchment population size, high transmission season, improved care-seeking behaviour by infected individuals, and recent increases (within the previous year) in transmission intensity. The proportion of all infections detected within health systems increases once transmission intensity is sufficiently low. The likely explanation for P falciparum is that reduced exposure to infection leads to lower levels of protective immunity in the population, increasing the likelihood that infected individuals will become symptomatic and seek care. These factors might also be true for P vivax but a better understanding of the transmission biology is needed to attribute likely reasons for the observed trend. In low transmission and pre-elimination settings, enhancing access to care and improvements in care-seeking behaviour of infected individuals will lead to an increased proportion of infections detected in the community and might contribute to accelerating the interruption of transmission. Wellcome Trust.

Sections du résumé

BACKGROUND
Passively collected malaria case data are the foundation for public health decision making. However, because of population-level immunity, infections might not always be sufficiently symptomatic to prompt individuals to seek care. Understanding the proportion of all Plasmodium spp infections expected to be detected by the health system becomes particularly paramount in elimination settings. The aim of this study was to determine the association between the proportion of infections detected and transmission intensity for Plasmodium falciparum and Plasmodium vivax in several global endemic settings.
METHODS
The proportion of infections detected in routine malaria data, P(Detect), was derived from paired household cross-sectional survey and routinely collected malaria data within health facilities. P(Detect) was estimated using a Bayesian model in 431 clusters spanning the Americas, Africa, and Asia. The association between P(Detect) and malaria prevalence was assessed using log-linear regression models. Changes in P(Detect) over time were evaluated using data from 13 timepoints over 2 years from The Gambia.
FINDINGS
The median estimated P(Detect) across all clusters was 12·5% (IQR 5·3-25·0) for P falciparum and 10·1% (5·0-18·3) for P vivax and decreased as the estimated log-PCR community prevalence increased (adjusted odds ratio [OR] for P falciparum 0·63, 95% CI 0·57-0·69; adjusted OR for P vivax 0·52, 0·47-0·57). Factors associated with increasing P(Detect) included smaller catchment population size, high transmission season, improved care-seeking behaviour by infected individuals, and recent increases (within the previous year) in transmission intensity.
INTERPRETATION
The proportion of all infections detected within health systems increases once transmission intensity is sufficiently low. The likely explanation for P falciparum is that reduced exposure to infection leads to lower levels of protective immunity in the population, increasing the likelihood that infected individuals will become symptomatic and seek care. These factors might also be true for P vivax but a better understanding of the transmission biology is needed to attribute likely reasons for the observed trend. In low transmission and pre-elimination settings, enhancing access to care and improvements in care-seeking behaviour of infected individuals will lead to an increased proportion of infections detected in the community and might contribute to accelerating the interruption of transmission.
FUNDING
Wellcome Trust.

Identifiants

pubmed: 32277908
pii: S1473-3099(20)30059-1
doi: 10.1016/S1473-3099(20)30059-1
pmc: PMC7391005
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

953-963

Subventions

Organisme : Medical Research Council
ID : MC_EX_MR/J002364/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 204693/Z/16/Z
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2020 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY-NC-ND 4.0 license. Published by Elsevier Ltd.. All rights reserved.

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Auteurs

Gillian Stresman (G)

Department of Infection Biology, London School of Hygiene & Tropical Medicine, London, UK. Electronic address: gillian.stresman@lshtm.ac.uk.

Nuno Sepúlveda (N)

Department of Infection Biology, London School of Hygiene & Tropical Medicine, London, UK; Centre of Statistics and Its Applications, University of Lisbon, Lisbon, Portugal.

Kimberly Fornace (K)

Department of Disease Control, London School of Hygiene & Tropical Medicine, London, UK.

Lynn Grignard (L)

Department of Infection Biology, London School of Hygiene & Tropical Medicine, London, UK.

Julia Mwesigwa (J)

Medical Research Council Unit The Gambia at London School of Hygiene & Tropical Medicine, Fajara, The Gambia; Department of Global Health, University of Antwerp, Antwerp, Belgium.

Jane Achan (J)

Medical Research Council Unit The Gambia at London School of Hygiene & Tropical Medicine, Fajara, The Gambia.

John Miller (J)

PATH Malaria Control and Elimination Partnership in Africa (MACEPA), National Malaria Elimination Centre, Ministry of Health, Chainama Grounds Lusaka, Zambia.

Daniel J Bridges (DJ)

PATH Malaria Control and Elimination Partnership in Africa (MACEPA), National Malaria Elimination Centre, Ministry of Health, Chainama Grounds Lusaka, Zambia.

Thomas P Eisele (TP)

Center for Applied Malaria Research and Evaluation, Department of Tropical Medicine, Tulane University School of Public Health and Tropical Medicine, New Orleans, LA, USA.

Jacklin Mosha (J)

National Institute for Medical Research, Mwanza Medical Research Centre, Mwanza, Tanzania.

Pauline Joy Lorenzo (PJ)

Department of Parasitology, Research Institute for Tropical Medicine, Research Drive, Alabang, Muntinlupa, Metro Manila, Philippines.

Maria Lourdes Macalinao (ML)

Department of Parasitology, Research Institute for Tropical Medicine, Research Drive, Alabang, Muntinlupa, Metro Manila, Philippines.

Fe Esperanza Espino (FE)

Department of Parasitology, Research Institute for Tropical Medicine, Research Drive, Alabang, Muntinlupa, Metro Manila, Philippines.

Fitsum Tadesse (F)

Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, Netherlands.

Jennifer C Stevenson (JC)

Macha Research Trust, Choma District, Zambia; Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.

Antonio M Quispe (AM)

School of Medicine, Universidad Continental, Huancayo, Peru.

André Siqueira (A)

Fundação de Medicina Tropical Dr Heitor Vieira Dourado, Manaus, Brazil; Programa de Pós-graduação em Medicina Tropical, Universidade do Estado do Amazonas, Manaus, Brazil; Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil.

Marcus Lacerda (M)

Fundacao de Medicine Tropical Dr. Heitor Viera Dourado, Manaus, Brazil; Institutos Nacionais de Ciencia e Technologia (INCT), Instituto Elimina, Manaus, Brazil.

Shunmay Yeung (S)

Department of Clinical Research, London School of Hygiene & Tropical Medicine, London, UK.

Siv Sovannaroth (S)

National Center for Parasitology, Entomology and Malaria Control, Phnom Penh, Cambodia.

Emilie Pothin (E)

Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, University of Basel, Basel, Switzerland; Clinton Health Access Initiative, Boston, MA, USA.

Joanna Gallay (J)

Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, University of Basel, Basel, Switzerland.

Karen E Hamre (KE)

Centers for Disease Control and Prevention, Center for Global Health, Division of Parasitic Diseases and Malaria, Malaria Branch, Atlanta, GA, USA; CDC Foundation, Atlanta, GA, USA.

Alyssa Young (A)

Clinton Health Access Initiative, Port-au-Prince, Haiti.

Jean Frantz Lemoine (JF)

Programme National de Contrôle de la Malaria, Ministère de la Santé Publique et de la Population (MSPP), Port-au-Prince, Haiti.

Michelle A Chang (MA)

Centers for Disease Control and Prevention, Center for Global Health, Division of Parasitic Diseases and Malaria, Malaria Branch, Atlanta, GA, USA.

Koukeo Phommasone (K)

Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit (LOMWRU), Microbiology Laboratory, Mahosot Hospital, Vientiane, Laos.

Mayfong Mayxay (M)

Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit (LOMWRU), Microbiology Laboratory, Mahosot Hospital, Vientiane, Laos; Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, UK; Institute of Research and Education Development, University of Health Sciences, Vientiane, Laos.

Jordi Landier (J)

Aix Marseille Univ, IRD, INSERM, SESSTIM, Marseille, France.

Daniel M Parker (DM)

Department of Population Health and Disease Prevention and Department of Epidemiology, University of California, Irvine, CA, USA.

Lorenz Von Seidlein (L)

Oxford Tropical Medicine Research Unit, Mahidol University Bangkok, Thailand; Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, UK.

Francois Nosten (F)

Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, UK; Shoklo Malaria Research Unit, Mae Sot, Thailand.

Gilles Delmas (G)

Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, UK; Shoklo Malaria Research Unit, Mae Sot, Thailand.

Arjen Dondorp (A)

Oxford Tropical Medicine Research Unit, Mahidol University Bangkok, Thailand; Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, UK.

Ewan Cameron (E)

Telethon Kids Institute, Perth Children's Hospital, Nedlands, WA, Australia; Curtin University, Bentley, WA, Australia.

Katherine Battle (K)

Institute for Disease Modelling, Seattle, WA, USA.

Teun Bousema (T)

Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, Netherlands.

Peter Gething (P)

Telethon Kids Institute, Perth Children's Hospital, Nedlands, WA, Australia; Curtin University, Bentley, WA, Australia.

Umberto D'Alessandro (U)

Department of Disease Control, London School of Hygiene & Tropical Medicine, London, UK; Medical Research Council Unit The Gambia at London School of Hygiene & Tropical Medicine, Fajara, The Gambia.

Chris Drakeley (C)

Department of Infection Biology, London School of Hygiene & Tropical Medicine, London, UK.

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