Choosing interventions to eliminate forest malaria: preliminary results of two operational research studies inside Cambodian forests

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Abstract

Background

Rapid elimination of Plasmodium falciparum malaria in Cambodia is a goal with both national and international significance. Transmission of malaria in Cambodia is limited to forest environments, and the main population at risk consists of forest-goers who rely on forest products for income or sustenance. The ideal interventions to eliminate malaria from this population are unknown.

Methods

In two forested regions of Cambodia, forest-goers were trained to become forest malaria workers (FMWs). In one region, FMWs performed mass screening and treatment, focal screening and treatment, and passive case detection inside the forest. In the other region, FMWs played an observational role for the first year, to inform the choice of intervention for the second year. In both forests, FMWs collected blood samples and questionnaire data from all forest-goers they encountered. Mosquito collections were performed in each forest.

Results

Malaria prevalence by PCR was high in the forest, with 2.3–5.0% positive for P. falciparum and 14.6–25.0% positive for Plasmodium vivax among forest-goers in each study site. In vectors, malaria prevalence ranged from 2.1% to 9.6%, but no P. falciparum was observed. Results showed poor performance of mass screening and treatment, with sensitivity of rapid diagnostic tests equal to 9.1% (95% CI 1.1%, 29.2%) for P. falciparum and 4.4% (95% CI 1.6%, 9.2%) for P. vivax. Malaria infections were observed in all demographics and throughout the studied forests, with no clear risk factors emerging.

Conclusions

Malaria prevalence remains high among Cambodian forest-goers, but performance of rapid diagnostic tests is poor. More adapted strategies to this population, such as intermittent preventive treatment of forest goers, should be considered.

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Most cited references 37

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The role of submicroscopic parasitemia in malaria transmission: what is the evidence?

Jessica T Lin, David L Saunders, Steven R Meshnick (2014)

Achieving malaria elimination requires targeting the human reservoir of infection, including those with asymptomatic infection. Smear-positive asymptomatic infections detectable by microscopy are an important reservoir because they often persist for months and harbor gametocytes, the parasite stage infectious to mosquitoes. However, many asymptomatic infections are submicroscopic and can only be detected by molecular methods. Although there is some evidence that individuals with submicroscopic malaria can infect mosquitoes, transmission is much less likely to occur at submicroscopic gametocyte levels. As malaria elimination programs pursue mass screening and treatment of asymptomatic individuals, further research should strive to define the degree to which submicroscopic malaria contributes to the infectious reservoir and, in turn, what diagnostic detection threshold is needed to effectively interrupt transmission. Copyright © 2014 Elsevier Ltd. All rights reserved.

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The impact of targeted malaria elimination with mass drug administrations on falciparum malaria in Southeast Asia: A cluster randomised trial

Lorenz von Seidlein, Thomas J Peto, Jordi Landier … (2019)

Background The emergence and spread of multidrug-resistant Plasmodium falciparum in the Greater Mekong Subregion (GMS) threatens global malaria elimination efforts. Mass drug administration (MDA), the presumptive antimalarial treatment of an entire population to clear the subclinical parasite reservoir, is a strategy to accelerate malaria elimination. We report a cluster randomised trial to assess the effectiveness of dihydroartemisinin-piperaquine (DP) MDA in reducing falciparum malaria incidence and prevalence in 16 remote village populations in Myanmar, Vietnam, Cambodia, and the Lao People’s Democratic Republic, where artemisinin resistance is prevalent. Methods and findings After establishing vector control and community-based case management and following intensive community engagement, we used restricted randomisation within village pairs to select 8 villages to receive early DP MDA and 8 villages as controls for 12 months, after which the control villages received deferred DP MDA. The MDA comprised 3 monthly rounds of 3 daily doses of DP and, except in Cambodia, a single low dose of primaquine. We conducted exhaustive cross-sectional surveys of the entire population of each village at quarterly intervals using ultrasensitive quantitative PCR to detect Plasmodium infections. The study was conducted between May 2013 and July 2017. The investigators randomised 16 villages that had a total of 8,445 residents at the start of the study. Of these 8,445 residents, 4,135 (49%) residents living in 8 villages, plus an additional 288 newcomers to the villages, were randomised to receive early MDA; 3,790 out of the 4,423 (86%) participated in at least 1 MDA round, and 2,520 out of the 4,423 (57%) participated in all 3 rounds. The primary outcome, P. falciparum prevalence by month 3 (M3), fell by 92% (from 5.1% [171/3,340] to 0.4% [12/2,828]) in early MDA villages and by 29% (from 7.2% [246/3,405] to 5.1% [155/3,057]) in control villages. Over the following 9 months, the P. falciparum prevalence increased to 3.3% (96/2,881) in early MDA villages and to 6.1% (128/2,101) in control villages (adjusted incidence rate ratio 0.41 [95% CI 0.20 to 0.84]; p = 0.015). Individual protection was proportional to the number of completed MDA rounds. Of 221 participants with subclinical P. falciparum infections who participated in MDA and could be followed up, 207 (94%) cleared their infections, including 9 of 10 with artemisinin- and piperaquine-resistant infections. The DP MDAs were well tolerated; 6 severe adverse events were detected during the follow-up period, but none was attributable to the intervention. Conclusions Added to community-based basic malaria control measures, 3 monthly rounds of DP MDA reduced the incidence and prevalence of falciparum malaria over a 1-year period in areas affected by artemisinin resistance. P. falciparum infections returned during the follow-up period as the remaining infections spread and malaria was reintroduced from surrounding areas. Limitations of this study include a relatively small sample of villages, heterogeneity between villages, and mobility of villagers that may have limited the impact of the intervention. These results suggest that, if used as part of a comprehensive, well-organised, and well-resourced elimination programme, DP MDA can be a useful additional tool to accelerate malaria elimination. Trial registration ClinicalTrials.gov NCT01872702

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An innovative tool for moving malaria PCR detection of parasite reservoir into the field

Lydie Canier, Nimol Khim, Saorin Kim … (2013)

Background To achieve the goal of malaria elimination in low transmission areas such as in Cambodia, new, inexpensive, high-throughput diagnostic tools for identifying very low parasite densities in asymptomatic carriers are required. This will enable a switch from passive to active malaria case detection in the field. Methods DNA extraction and real-time PCR assays were implemented in an “in-house” designed mobile laboratory allowing implementation of a robust, sensitive and rapid malaria diagnostic strategy in the field. This tool was employed in a survey organized in the context of the MalaResT project (NCT01663831). Results The real-time PCR screening and species identification assays were performed in the mobile laboratory between October and November 2012, in Rattanakiri Province, to screen approximately 5,000 individuals in less than four weeks and treat parasite carriers within 24–48 hours after sample collection. An average of 240 clinical samples (and 40 quality control samples) was tested every day, six/seven days per week. Some 97.7% of the results were available <24 hours after the collection. A total of 4.9% were positive for malaria. Plasmodium vivax was present in 61.1% of the positive samples, Plasmodium falciparum in 45.9%, Plasmodium malariae in 7.0% and Plasmodium ovale in 2.0%. Conclusions The operational success of this diagnostic set-up proved that molecular testing and subsequent treatment is logistically achievable in field settings. This will allow the detection of clusters of asymptomatic carriers and to provide useful epidemiological information. Fast results will be of great help for staff in the field to track and treat asymptomatic parasitaemic cases. The concept of the mobile laboratory could be extended to other countries for the molecular detection of malaria or other pathogens, or to culture vivax parasites, which does not support long-time delay between sample collection and culture.

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Author and article information

Contributors

Amber Kunkel:

ORCID: http://orcid.org/0000-0002-8376-4713

agkunkel@gmail.com

Journal

Journal ID (nlm-ta): Malar J

Journal ID (iso-abbrev): Malar J

Title: Malaria Journal

Publisher: BioMed Central (London )

ISSN (Electronic): 1475-2875

Publication date (Electronic): 20 January 2021

Publication date PMC-release: 20 January 2021

Publication date Collection: 2021

Volume: 20

Electronic Location Identifier: 51

Affiliations

[1 ]GRID grid.418537.c, Epidemiology and Public Health Unit, , Institut Pasteur du Cambodge, ; Phnom Penh, Cambodia

[2 ]GRID grid.428999.7, ISNI 0000 0001 2353 6535, Emerging Diseases Epidemiology Unit, , Institut Pasteur, ; Paris, France

[3 ]GRID grid.452707.3, National Center for Parasitology, Entomology and Malaria Control, ; Phnom Penh, Cambodia

[4 ]GRID grid.418537.c, Malaria Molecular Epidemiology Unit, , Institut Pasteur du Cambodge, ; Phnom Penh, Cambodia

[5 ]Partners for Development, Phnom Penh, Cambodia

[6 ]Malaria Consortium, Phnom Penh, Cambodia

[7 ]World Health Organization, Cambodia Country Office, Phnom Penh, Cambodia

Author information

Amber Kunkel http://orcid.org/0000-0002-8376-4713

Article

Publisher ID: 3572

DOI: 10.1186/s12936-020-03572-3

PMC ID: 7818569

PubMed ID: 33472630

SO-VID: d5907678-b2cc-4f06-b693-f2b2bb2571b6

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 19 October 2020

Date accepted : 24 December 2020

Funding

Funded by: French Initiative 5%

Award ID: 17SANIN205

Award Recipient : Patrice Piola

Funded by: Regional Artemisinin-resistance Initiative

Award ID: QSE-M-UNOPS

Award Recipient : Patrice Piola

Funded by: Pasteur Foundation (US)

Custom metadata

ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: malaria,plasmodium falciparum,plasmodium vivax,cambodia,greater mekong subregion,forest,forest-goers,rapid diagnostic test,mass screening and treatment

Data availability:

ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: malaria, plasmodium falciparum, plasmodium vivax, cambodia, greater mekong subregion, forest, forest-goers, rapid diagnostic test, mass screening and treatment

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Choosing interventions to eliminate forest malaria: preliminary results of two operational research studies inside Cambodian forests

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Abstract

Background

Methods

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Conclusions

Related collections

Malaria vaccine development

Most cited references 37

The role of submicroscopic parasitemia in malaria transmission: what is the evidence?

The impact of targeted malaria elimination with mass drug administrations on falciparum malaria in Southeast Asia: A cluster randomised trial

An innovative tool for moving malaria PCR detection of parasite reservoir into the field

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