malaria topics for research paper

Malaria Journal publishes primary research from the full spectrum of malaria research. Subjects covered include any aspects of the biology of malaria parasites and their vectors; clinical features and disease pathophysiology; biochemistry and molecular biology; case management and treatment; drug development and drug resistance; immunology, immunogenetics and vaccine development; genomes and transcriptomes of malaria parasites and their vectors; epidemiology and transmission dynamics; vector control; health system, policy and planning issues relating to prevention and treatment; economic, sociological and anthropological issues; poverty and gender issues, land use and global environmental change; intersectoral issues; intervention studies and operational research; control policy and planning.

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Malaria Journal requires that all datasets on which the conclusions of the paper rely should be available to readers. We ask authors to ensure that their datasets are either deposited in publicly available repositories (where available and appropriate) or presented in the main manuscript or additional supporting files whenever possible. Please see Springer Nature’s information on recommended repositories .

For Therapeutic efficacy studies (any Plasmodium species) please use the STARTER checklist which can be found on the EQUATOR network website and submit the completed checklist as an additional file

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• if a collaboration group should be listed as an author, please list the Group name as an author. If you would like the names of the individual members of the Group to be searchable through their individual PubMed records, please include this information in the “Acknowledgements” section in accordance with the instructions below
• Large Language Models (LLMs), such as ChatGPT , do not currently satisfy our authorship criteria . Notably an attribution of authorship carries with it accountability for the work, which cannot be effectively applied to LLMs. Use of an LLM should be properly documented in the Methods section (and if a Methods section is not available, in a suitable alternative part) of the manuscript.
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The Abstract should not exceed 350 words. Please minimize the use of abbreviations and do not cite references in the abstract. Reports of randomized controlled trials should follow the CONSORT extension for abstracts. The abstract must include the following separate sections:

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List of abbreviations

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More examples of template data availability statements, which include examples of openly available and restricted access datasets, are available here .

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2022 Citation Impact 3.0 - 2-year Impact Factor 3.2 - 5-year Impact Factor 1.148 - SNIP (Source Normalized Impact per Paper) 1.237 - SJR (SCImago Journal Rank)

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Malaria Journal

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Home > Books > Infectious Diseases

Current Topics in Malaria

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Academic Editor

Fundación Universitaria Autónoma De Las Américas , Colombia

Published 30 November 2016

Doi 10.5772/61868

ISBN 978-953-51-2790-1

Print ISBN 978-953-51-2789-5

eBook (PDF) ISBN 978-953-51-4144-0

Copyright year 2016

Number of pages 506

Malaria is still the main vector-borne parasitic disease in the world. Fortunately, elimination of this disease was achieved in multiple countries during the last decades. During the last decade, a significant reduction of malaria in the Americas was achieved. Nevertheless, many challenges still are ahead in order to reach a higher control and to continue in the elimination toward a world free of ...

Malaria is still the main vector-borne parasitic disease in the world. Fortunately, elimination of this disease was achieved in multiple countries during the last decades. During the last decade, a significant reduction of malaria in the Americas was achieved. Nevertheless, many challenges still are ahead in order to reach a higher control and to continue in the elimination toward a world free of malaria in the next decades. This book tries to update the significant epidemiological and clinical research in many aspects with a multinational perspective. This book with 20 chapters is organized into 5 major sections: (I) Clinical and Epidemiological Aspects, (II) Basic Science, (III) Therapeutics and Antimalarials, (IV) Vaccines, and (V) Entomology and Vector Control.

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By Kevin Pometti

By Lyazzat Gumarova, Germaine Cornelissen, Borislav D Dimitrov and Franz Halberg

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By Yaw Asare Afrane, Mariangela Bonizzoni and Guiyun Yan

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Article Contents

Introduction, authors’ contributions, acknowledgements, competing interests, ethical approval, data availability, disclaimers, climate change, malaria and neglected tropical diseases: a scoping review.

• Article contents
• Figures & tables
• Supplementary Data

Petra Klepac, Jennifer L Hsieh, Camilla L Ducker, Mohamad Assoum, Mark Booth, Isabel Byrne, Sarity Dodson, Diana L Martin, C Michael R Turner, Kim R van Daalen, Bernadette Abela, Jennifer Akamboe, Fabiana Alves, Simon J Brooker, Karen Ciceri-Reynolds, Jeremy Cole, Aidan Desjardins, Chris Drakeley, Dileepa S Ediriweera, Neil M Ferguson, Albis Francesco Gabrielli, Joshua Gahir, Saurabh Jain, Mbaraka R John, Elizabeth Juma, Priya Kanayson, Kebede Deribe, Jonathan D King, Andrea M Kipingu, Samson Kiware, Jan Kolaczinski, Winnie J Kulei, Tajiri L Laizer, Vivek Lal, Rachel Lowe, Janice S Maige, Sam Mayer, Lachlan McIver, Jonathan F Mosser, Ruben Santiago Nicholls, Cláudio Nunes-Alves, Junaid Panjwani, Nishanth Parameswaran, Karen Polson, Hale-Seda Radoykova, Aditya Ramani, Lisa J Reimer, Zachary M Reynolds, Isabela Ribeiro, Alastair Robb, Kazim Hizbullah Sanikullah, David R M Smith, GloriaSalome G Shirima, Joseph P Shott, Rachel Tidman, Louisa Tribe, Jaspreet Turner, Susana Vaz Nery, Raman Velayudhan, Supriya Warusavithana, Holly S Wheeler, Aya Yajima, Ahmed Robleh Abdilleh, Benjamin Hounkpatin, Dechen Wangmo, Christopher J M Whitty, Diarmid Campbell-Lendrum, T Déirdre Hollingsworth, Anthony W Solomon, Ibrahima Socé Fall, Climate change, malaria and neglected tropical diseases: a scoping review, Transactions of The Royal Society of Tropical Medicine and Hygiene , 2024;, trae026, https://doi.org/10.1093/trstmh/trae026

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To explore the effects of climate change on malaria and 20 neglected tropical diseases (NTDs), and potential effect amelioration through mitigation and adaptation, we searched for papers published from January 2010 to October 2023. We descriptively synthesised extracted data. We analysed numbers of papers meeting our inclusion criteria by country and national disease burden, healthcare access and quality index (HAQI), as well as by climate vulnerability score. From 42 693 retrieved records, 1543 full-text papers were assessed. Of 511 papers meeting the inclusion criteria, 185 studied malaria, 181 dengue and chikungunya and 53 leishmaniasis; other NTDs were relatively understudied. Mitigation was considered in 174 papers (34%) and adaption strategies in 24 (5%). Amplitude and direction of effects of climate change on malaria and NTDs are likely to vary by disease and location, be non-linear and evolve over time. Available analyses do not allow confident prediction of the overall global impact of climate change on these diseases. For dengue and chikungunya and the group of non-vector-borne NTDs, the literature privileged consideration of current low-burden countries with a high HAQI. No leishmaniasis papers considered outcomes in East Africa. Comprehensive, collaborative and standardised modelling efforts are needed to better understand how climate change will directly and indirectly affect malaria and NTDs.

Human activity is driving incremental changes in climate patterns globally. The burning of coal, oil and natural gas; clearing land by cutting down forests; and intensified agriculture all release greenhouse gases, primarily CO 2 , methane and N 2 O. Deforestation also reduces capacity for CO 2 absorption. Increases in atmospheric concentrations of greenhouse gases are driving mean global temperatures upwards, with consequent effects including rising sea levels, changes in rainfall and increases in the frequency and intensity of extreme weather events. 1

Climate change will perturb human health in profound and long-lasting ways, both directly and indirectly. 2 Multiple direct and indirect mechanisms will contribute. Human physiology can be affected directly by changes in air temperature, humidity, stress and diet. Human behaviour can be altered by changing weather, changing economic circumstances, migration, natural disasters and access to or quality of healthcare. Environmental conditions also influence pathogen transmission, reproduction, development and genetics; the reproduction, development, genetics, behaviour, range, longevity and predation of vectors, intermediate hosts and reservoir hosts; and the feasibility and effectiveness of interventions. In fact, there is already empirical evidence of climate change having amplified more than one-half of all known human infectious diseases. 3

The impact of climate change is likely to be disproportionately borne by the poorest people, who are also disproportionately affected by malaria and neglected tropical diseases (NTDs; Table  1 ). In part because of this association with poverty, malaria and NTDs are often co-endemic. Many of these diseases are currently suitable for coordinated control via integrated programmes. 4–7

Diseases and organisms in scope for this review. Included diseases and associated aetiological agents, vectors, reservoir and intermediate hosts and routes of transmission are those listed in the NTD road map 2021–2030, 13 plus malaria. Noma was added to the NTD list in December 2023, 61 and therefore is not included here.

a Ancylostoma ceylanicum is a soil-transmitted helminth species previously believed to only infect dogs but now recognised as a zoonosis that causes symptomatic infections in humans; it was not included in the NTD road map 2021–2030 13 and therefore was not included in this review.

Developing an understanding of the likely effects of climate change on the epidemiology of malaria and NTDs is critical to minimising their health implications. This scoping review explores current predictions of the effects of historical and future climate change on malaria and NTDs, and the potential amelioration of these effects through climate change mitigation and adaptation strategies.

A comprehensive scoping review was conducted. To complete the review efficiently but with high fidelity, we used automation and artificial intelligence-based tools to help define search terms, translate them across different platforms, de-duplicate search results and conduct title-and-abstract screening. 8 We did not otherwise use artificial intelligence assistance. This report adheres to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses extension for Scoping Reviews guidance 9 ( Supplementary Table 1 ).

Search strategy

Searches were conducted in five electronic databases that index the published peer-reviewed and grey literature: PubMed, Scopus, Embase via Ovid, Global Index Medicus and the WHO's Institutional Repository for Information Sharing.

Databases were searched for papers published from 1 January 2010 to 12 October 2023. No language or other restrictions were applied. Using a combination of Medical Subject Heading (MeSH) and free-text terms, search vocabulary related to ‘climate change’, ‘malaria’ and ‘neglected tropical diseases’ was employed. Searches were designed and conducted in English and included scientific and lay expressions for diseases, pathogens, vectors, reservoir hosts and intermediate hosts; the search strategy was first constructed for PubMed, and the Systematic Review Accelerator Polyglot tool ( https://sr-accelerator.com/#/polyglot ) 10 was then used to translate strings into syntax appropriate for other databases. (Please see the Supplementary material for full search strings.) Using the citationchaser Shiny app ( https://www.eshackathon.org/software/citationchaser.html ), 11 forward and backward screening of relevant seed papers (e.g. reviews, commentaries) was undertaken in December 2023 to identify additional records. The review protocol was not published in advance.

Criteria for paper selection

Inclusion criteria applied to screening are shown in Table  2 . Papers not meeting these criteria were excluded.

Characteristics of included papers.

Papers were eligible for inclusion if they explicitly reported on the observed or modelled effects of historical or future climate change on outcomes framing the distribution, dynamics or transmission of malaria or NTDs; or the range, abundance or transmission potential of their vectors, reservoir hosts or intermediate hosts. Papers were also included if they explicitly reported on the observed or modelled effects of climate change mitigation and adaptation strategies on these outcomes. (‘Climate change mitigation’ was defined as actions intended to reduce the magnitude of climate change, and ‘adaptation’ as actions intended to reduce the vulnerability of human and natural systems to the effects of climate change or to cope with past or future climate change.)

Masters and PhD theses were eligible for inclusion if the analyses were not also presented elsewhere, but we did not specifically search thesis repositories.

Papers were excluded if (i) they did not include original analyses; (ii) they presented methods or protocols without results; (iii) they were clinical case reports; (iv) they were conference proceedings; (v) they were pre-prints (of papers being prepared for, or in the process of being considered by, peer-reviewed journals); or (vi) the full text could not be obtained. In contrast to the exclusion of clinical case reports, we included ecological case reports as potentially important indicators of pathogen or vector range expansion.

Screening and extraction procedures

The Covidence software package ( https://www.covidence.org/ ) was used to support record indexing, removal of duplicate records, title-and-abstract screening, full-text screening and compilation of extracted data.

After de-duplication, titles and abstracts of each record were independently screened by two researchers, with conflicts resolved by a third independent reviewer. Non-English records were translated or reviewed by a fluent speaker of that language.

The Covidence title-and-abstract screening module incorporates a machine-learning algorithm that ranks papers that are yet to be screened according to their acceptance likelihood: based on previous screening decisions, it pushes papers that are more likely to be accepted towards the top of the pile, for all reviewers. This accelerates the screening process by removing the need to screen all search results. The predetermined stopping rule was to discontinue title-and-abstract screening after three criteria were met: (i) more than twice the estimated fraction of relevant records from a previously published systematic review of climate change and NTDs 12 had been screened; (ii) all papers previously determined as relevant (‘seed’ papers) were identified; and (iii) two screeners had each rejected 50 papers in a row. The results of the backward and forward citation searches of seed papers were screened separately with the assistance of the same (trained) machine-learning algorithm, with screening of these records discontinued after a single screener had rejected 100 papers in a row.

Full texts were blind double-screened, with discrepant results arbitrated by an independent third reviewer.

Data from papers selected in the full-text review were independently extracted by one investigator using a pre-piloted standardised form, according to self-identified individual expertise, and checked by a second investigator. Data extraction was limited to the information provided in the published work; authors were not contacted for further clarification or provision of missing information. Extracted information included: first author, year, study title, diseases addressed in the publication, study design (cohort, field, model, laboratory research, ecological case report), whether the paper explicitly discussed adaptation or mitigation strategies, the time frame of the study (cross-sectional, prospective longitudinal, retrospective longitudinal; the length of the time series), location data, and the population, intervention/exposure, comparator and outcome (Table  2 ).

Structured assessment of the methodological limitations and risk of bias of included individual papers was not undertaken.

Data analyses and synthesis

Because of the heterogeneity of included studies in terms of designs, exposures, outcomes and quality, no meta-analyses were attempted. Data were narratively synthesised and thematically categorised to facilitate analysis.

Papers were grouped and synthesised by whether they (i) explored the effect of climate change on malaria and NTDs; or (ii) examined potential amelioration of these effects through climate change mitigation and adaptation. Studies that compared several future climate scenarios of different severities (different representative concentration pathways [RCPs], or different combinations of RCPs and shared socioeconomic pathways, for example; please see Box 1 and Figure  1 ) were defined as projections of the effect of mitigation.

Comparison of Intergovernmental Panel on Climate Change (IPCC) scenarios used in papers that met this review's inclusion criteria. The different categories of scenario (special report on emission scenarios [SRES; released in 2000]; representative concentration pathways [RCPs; 2014]; shared socioeconomic pathways [SSP; 2021]; scenarios from the IPCC Sixth Assessment Report Working Group III [AR6 WGIII; 2022]) are laid out in columns against the equivalent scenarios within the full RCP scheme, which are laid out in rows; some of the RCP scenarios (RCP1.9, RCP3.4 and RCP7) were added after the original 2014 publication of the RCP system. (The RCPs were the most commonly applied scenarios used in papers that met this review's inclusion criteria.) Further explanations of all of these scenario categories are included in Box 1 . 81–83

Climate change scenarios.

The Intergovernmental Panel on Climate Change (IPCC) has periodically published assessment reports on the scientific understanding of climate change, its projected effects and potential response strategies. As a part of these reports, the IPCC outlines future climate scenarios or pathways based on projections from Global Climate Models, for use in modelling. Papers meeting the inclusion criteria for this review used a variety of different future scenarios, so their outcomes and conclusions generally cannot be directly compared. Here, we summarise the history of IPCC climate scenarios, explain their interpretation and note how they relate to each other (Figure  1 ).

IP92 –the first global climate change scenarios, published by IPCC in 1992. These focused on projected future emissions of greenhouse gases (GHGs). 78

Special Report on Emission Scenarios (SRES)—released in 2000 and used in the IPCC's Third Assessment Report (TAR) and Fourth Assessment Report (AR4). The SRES covers a wide range of the main drivers of climate change, from demographic to technological and economic developments, and includes all relevant GHGs and sulphur, and their driving forces. 79 Four main narrative storylines with different contributions of drivers cover a range of possible outcomes:

A1: Rapid economic growth; population peaks mid-century then declines.

A2: Regionalised world; high population growth.

B1: Global sustainability focus; population peaks mid-century then declines.

B2: Local solutions emphasised; slow population growth.

Representative Concentration Pathways (RCPs)—Developed to replace the SRES, for use in climate models as part of the Fifth Assessment Report (AR5) of the IPCC in 2014. Rather than being based on storylines, RCPs describe possible GHG emissions and concentration levels in the atmosphere by 2100, ranging from very low (RCP2.6, radiative forcing peaks at 3 Wm −2 and then declines to 2.6 Wm −2 by 2100, also known as RCP3PD) to intermediate (RCP4.5 and RCP6.0, radiative forcing is stabilised at approximately 4.5 or 6.0 Wm −2 ), to very high (RCP8.5, radiative forcing continues to increase after 2100). RCPs use time series of emissions and concentrations of the full suite of GHGs, aerosols and chemically active gases, as well as projected land use/land cover and population growth. Compared with the SRES, RCP2.6 has no equivalent; RCP4.5 is similar to SRES B1 but median temperatures rise more quickly in RCP4.5 than in B1 in the first half of the twenty-first century, and then more slowly in the second half; RCP6.0 is similar to SRES B2, with median temperatures rising more quickly in RCP6.0 than in B2 from 2060–2090, but otherwise more slowly; and RCP8.5 is similar to SRES A1FI (A1 fossil-fuel intensive scenario), with median temperatures rising more slowly in RCP8.5 than in A1FI during 2035–2080, but more quickly during other periods. 80 , 81

Shared Socioeconomic Pathways (SSPs)—These scenarios were introduced in the IPCC's Sixth Assessment Report (AR6) published in 2021. SSPs are integrated scenarios that combine socioeconomic narratives with emission pathways, describing different plausible futures of societal development based on varying assumptions about demographic, economic, social and technological factors. Briefly, these include:

SSP1 (Sustainability): represents a future in which there is rapid economic growth, low population growth and widespread adoption of environmentally friendly technologies. It is also called ‘Taking the Green Road’ and emphasises sustainable development, international cooperation and a focus on environmental stewardship.

SSP2 (Middle of the Road): represents a future in which trends continue along historic trajectories with moderate economic growth, intermediate population growth and technological progress occurring at a moderate pace. It assumes some improvements in living standards and governance but also incorporates challenges and disparities.

SSP3 (Regional Rivalry): represents a future characterised by high population growth, slow economic development and fragmented governance. Also termed ‘A Rocky Road’, it envisions regions prioritising national interests over global cooperation, resulting in regional rivalries, conflicts and limited efforts to address climate change.

SSP4 (Inequality): represents a future marked by high population growth, slow economic development and high income inequality. It assumes limited international cooperation and emphasises national interests and security concerns over environmental issues. Also termed ‘A Road Divided’, this scenario suggests challenges in achieving sustainable development and addressing climate change due to social disparities.

SSP5 (Fossil-Fuelled Development): represents a future with high population growth, rapid economic development and reliance on fossil fuels. Also termed ‘Taking the Highway’, it envisions limited environmental regulations and technological innovation, leading to high GHG emissions and significant impact from climate change. 82

AR6 WGIII —scenario categories C1-C8 (published in 2022 by the IPCC's Sixth Assessment Report AR6 Working Group III) refer to potential mitigation pathways used to reduce GHG emissions and limit global warming. These scenarios relate to warming levels in the twenty-first century:

C1 (1.5°C, no/limited overshoot). Limits warming to 1.5°C by 2100 (with >50% likelihood). Roughly corresponds to SSP1-1.9 (very low).

C2 (1.5°C, high overshoot). After a high overshoot, warming returns to 1.5°C by 2100 (with >50% likelihood). Roughly corresponds to SSP1-2.6 (low).

C3 (Likely below 2°C). Limits warming to 2°C by 2100 (with >67% likelihood).

C4 (Below 2°C). Limits warming to 2°C by 2100 (with >50% likelihood).

C5 (Below 2.5°C). Limits warming to 2.5°C by 2100 (with >50% likelihood).

C6 (Below 3°C). Limits warming to 3°C by 2100 (with >50% likelihood). Roughly corresponds to SSP2-4.5 (intermediate).

C7 (Below 4°C). Limits warming to 4°C by 2100 (with >50% likelihood). Roughly corresponds to SSP3-7.0 (high).

C8 (Above 4°C). Exceeds warming of 4°C by 2100 (with >50% likelihood). Roughly corresponds to SSP5-8.5 (very high). 83

Based on the volume of literature meeting the inclusion criteria, papers were further grouped by disease into malaria, dengue and chikungunya, other vector-borne NTDs and other non-vector-borne NTDs. Dengue and chikungunya are bracketed as an NTD group in the 2021–2030 NTD road map. 13 We categorised as ‘vector-borne NTDs’ those for which vector control was a recommended control strategy in the 2021–2030 NTD road map. 13

We obtained data on the burden of malaria and NTDs by country, quantified as disability-adjusted life years (DALYs, the cumulative number of years lost by a defined population due to illness, disability and death from a particular cause or group of causes), from the 2019 Global Burden of Disease study. 14 To account for different national levels of health service delivery, we used the healthcare access and quality index (HAQI). This employs data on 32 causes of death from which mortality would be avoidable in the presence of effective healthcare; a high index is a marker of better healthcare. HAQIs were obtained from the 2019 Global Burden of Disease data. 15 To account for countries’ exposure, sensitivity and ability to adapt to the negative impacts of climate change, we used the 2021 vulnerability score from the Notre Dame Global Adaptation Initiative (ND-GAIN; available at: https://gain-new.crc.nd.edu/ranking/vulnerability ). The ND-GAIN measures vulnerability by considering six life-supporting sectors: food, water, health, ecosystem service, human habitat and infrastructure. Countries ranked higher in the index are those that are less vulnerable. After removing papers that examined outcomes at the global level, local polynomial regression was undertaken to predict the number of disease group-specific publications relevant to each country as a function of the country's (i) DALYs for that group of diseases, (ii) HAQI and (iii) climate vulnerability score. As there were <1000 datapoints available for each regression, we used locally estimated scatterplot smoothing (LOESS) for these analyses.

Database searches yielded 31 560 records. Forward and backward citation searching yielded an additional 11 133 (of which 8587 were within the specified publication range), producing a combined total of 42 693 records (40 147 within the specified range). After removal of 14 879 duplicates, 27 814 records were available for title-and-abstract screening. The stopping rules for title-and-abstract screening were met after 9013 records had been examined; of these 9013, 7442 (83%) were excluded on the basis that their titles and abstracts indicated a failure to meet the inclusion criteria. Full-text papers were therefore sought for 1571 records (17% of 9013), of which 1543 (98%) were able to be retrieved. Following full-text review, 511 papers (33% of 1543) were included for data extraction; these are summarised in Supplementary Table 2 . Extracted data are presented in full in Supplementary Table 3 . A flow diagram is included as Figure  2 .

Records included and excluded at each review stage.

Papers that met the inclusion criteria considered outcomes relevant to malaria (185 papers), dengue and chikungunya (181), the leishmaniases (53), schistosomiasis (29), Chagas disease (19), foodborne trematodiases (17), lymphatic filariasis (14), snakebite envenoming (11), rabies (9), human African trypanosomiasis (8), Buruli ulcer (6), echinococcosis (4), onchocerciasis (2), leprosy (1), scabies (1) and soil-transmitted helminthiases (1). No papers meeting the inclusion criteria considered outcomes relevant to dracunculiasis; mycetoma, chromoblastomycosis or other deep mycoses; taeniasis/cysticercosis; trachoma; or yaws (Figure  3A ).

Number of papers by year and total number of papers meeting the inclusion criteria for each (A) disease or disease group, and (B) type of study.

The vast majority of papers used modelling to study the effect of climate change (435 papers). There were 72 field study papers, 54 laboratory research reports, 28 ecological case reports, 10 cohort studies and seven other types of study (Figure  3 B; multiple study types were possible in a single paper). There was little variation in the numbers of papers from year to year (Figure  3 A and B, left plots).

Among papers meeting the inclusion criteria, a total of 174 (35%) considered the possible ameliorating effect of climate change mitigation for any outcome, 24 (5%) considered adaption strategies and two considered both. Sixty-nine papers considered mitigation in relation to malaria outcomes. Nine explicitly considered adaptation strategies for malaria outcomes. Fifty-three papers addressed climate change mitigation and nine considered adaptation strategies in relation to dengue and chikungunya; four of the papers, including mitigation analyses for dengue and chikungunya, also considered malaria outcomes in the light of climate change mitigation. Sixty other papers addressed climate change mitigation or adaptation with respect to NTD outcomes.

There was wide variation in the geographical coverage of papers by disease (Figure  4 ). Apart from malaria, dengue and chikungunya, and schistosomiasis, there were <10 papers per disease per country for every country, with many endemic countries not featured in any papers for several NTDs. We also observed distinct distribution patterns for malaria, dengue and chikungunya, and schistosomiasis. Most papers examining the impact of climate change on malaria focused on countries in Africa, Brazil, China or India. Dengue and chikungunya papers were focused on Australia, China, India, countries in Europe and the USA, many of which are countries where these diseases may spread in future years. Several schistosomiasis papers focused on China. For leishmaniasis, papers meeting our inclusion criteria considered countries that were widely distributed around the globe, with the exception of countries in East Africa.

Geographical coverage of papers by disease. Colours represent the total number of papers that met the inclusion criteria, per disease, across countries.

The observed variation in geographical coverage of papers across diseases prompted us to further investigate the links between study location, number of papers, disease burden and country vulnerability to climate change. Given the discrepancy in the number of papers between diseases, we grouped these into four categories: (i) malaria; (ii) dengue and chikungunya; (iii) other vector-borne NTDs (Chagas disease, dracunculiasis, human African trypanosomiasis, leishmaniasis, lymphatic filariasis, onchocerciasis, schistosomiasis, trachoma); and (iv) non-vector-borne NTDs (Buruli ulcer, echinococcosis, foodborne trematodiases, leprosy, rabies, scabies/tungiasis, soil-transmitted helminthiases, snakebite envenoming, taeniasis and cysticercosis).

Our analysis showed different patterns across groups of diseases. For malaria there were clear trends towards more papers covering countries with a high malaria DALY burden, low HAQI and high vulnerability to climate change (Figure  5 , first column). For dengue and chikungunya, there was a trend towards increasing numbers of papers covering areas with high burden, but at low DALY burden there was an increase in papers due to the relatively large number of studies looking at potential expansion of these diseases into new areas (Figure  5 , second column). This also meant that there was a relative abundance of papers studying these diseases in areas where there is good access to healthcare, and where the climate vulnerability score is low. For the remaining vector-borne NTDs (Figure  5 , third column), there was a suggestion of an increasing numbers of papers addressing countries with increasing burden and decreasing HAQI, but no suggestion that analyses were more commonly focused on areas with high climate vulnerability. For the non-vector-borne NTD group, papers more frequently considered countries with high DALY burden for that disease, high HAQI and low climate vulnerability (Figure  5 , fourth column).

Numbers of papers meeting the inclusion criteria by disease or disease group, compared with country-level (A) DALYs for the disease or disease group; (B) health access and quality index; and (C) climate vulnerability score. Studies with outcomes reported at global level (for all countries) were removed for these analyses. Each circle represents one country; superimposition of multiple circles makes some look darker than others. Lines show locally estimated scatterplot smoothing (LOESS)-generated local polynomial regression.

Detailed analysis of the full text of papers meeting the inclusion criteria revealed additional insights. For malaria, the consensus among papers that met the inclusion criteria was that global warming will extend the area in which transmission is possible to some areas where it was previously too cold for vector or parasite development, while conditions in some currently endemic areas may become too severe to maintain transmission. Zones suitable for transmission may shift both poleward and upwards in altitude. Future expansion could be balanced by more frequent droughts, making environmental conditions unsuitable for transmission in some previously endemic areas, including parts of the Sahel. 16 Other papers concluded that malaria transmission seasons will last longer, as more months of the year will have a suitable climate. 17 While these changes could place a greater proportion of the global population at risk, 18 the potential net impact of climate change on the global burden of malaria remains unclear; 19–22 papers that met the inclusion criteria were vastly different and difficult to compare with each other. Making predictions for regional and global populations was previously difficult because of a general lack of high-resolution monthly incidence data. 23 There is likely to be small-scale heterogeneity in effects on the ground.

One aspect of climate change that is already impacting malaria transmission is the increasing frequency of extreme weather events. Severe flooding in Pakistan in 2022 and cyclones in Mozambique and Madagascar in 2023 were accompanied by local spikes in malaria cases, driven by breeding of Anopheles mosquitos in flood waters. 24

For dengue and chikungunya, a significant proportion of papers that met our inclusion criteria described subnational studies with subdecadal time frames. Models with broader geographic and temporal boundaries predict dramatic expansion in the future range of relevant Aedes vector species, 25–27 in line with trends that are already being observed. 28–30 Some local retreat from geographies currently occupied by Aedes spp. is also predicted. 31 Alongside the overall increase in vector range, considerable increases are projected in the number of future dengue cases under more adverse climate change scenarios (Box 1 ) in some models. 30 , 32 Other models predict a plateauing of dengue in highly endemic regions by 2050. 28 There is undoubtedly uncertainty about the magnitude and direction of future geographic expansion.

For the leishmaniases, 53 papers that met the inclusion criteria considered relevant outcomes. However, there are many different pathogens and vector species contributing to this complex of diseases (Table  1 ), making a reliable, complete picture very difficult to draw. Several large-scale models predict changes in the range of relevant sandfly species around the Mediterranean and in the Americas, with transmission in the latter extending as far north as southern Canada in some future climate scenarios. 33–37 The number of people in North America living in areas in which leishmaniasis is transmitted could double from 2010 to 2080 under SRES B2. 37 The paucity of information on the potential impact of climate change on leishmaniasis in Africa (Figure  4 ) was striking.

For schistosomiasis, one model predicted increased prevalence and intensity of infection in some areas of East Africa over the next few decades, particularly in Rwanda, Burundi, south-west Kenya and eastern Zambia, with concurrent substantial decreases in risk in parts of Kenya, southern South Sudan and eastern Democratic Republic of the Congo. 38 Decreases in transmission are predicted for China, 39 although the possibility was also invoked that disease will re-emerge in parts of mainland China where it was previously eliminated. 40 This concern may account for the relative concentration of publications that focused on China (Figure  4 ).

There were few papers on the remaining NTDs, with a bias towards vector-borne diseases, possibly due to the existence of established methodologies for examining vector suitability and its links to climate. Climate impacts on these other NTDs, whether through environmental changes or societal ones, such as changes in time to diagnosis due to changes in access to health systems, 41 remain largely unexplored.

For thousands of years, societies have been shaped and reshaped by epidemics, with Ebola virus disease, COVID-19 and mpox presenting only the most recent striking examples. A distinct feature of the climate crisis is the pace of change in underlying global ecosystems. This generates uncertainty about the future epidemiology of multiple diseases: not only those that have historically manifested as epidemics, but also those formerly considered as stable and endemic, and those being driven towards elimination or eradication. Climate change will simultaneously reshape the epidemiology of many non-infectious diseases, threaten health infrastructure, affect the health workforce and alter other foundational determinants of human health. These parallel effects will exacerbate the challenge presented by the evolving epidemiology of infectious diseases. 42 , 43

Malaria and many NTDs have relatively complex life cycles, involving overlapping webs of interactions between humans and vertebrate and invertebrate animals. Multiple points of exposure to ecological, biological and social systems increase the probability that climate change will alter disease incidence or prevalence. 43 , 44 This environmental sensitivity makes prediction of future scenarios both difficult and important. The perceived difficulty is borne out in the literature identified here: for most of the outcomes in scope, projections of the effects of future climate change at large scale are scarce. Projections that do exist incorporate considerable uncertainty.

Of all potential outcomes framed for this review, those related to malaria, dengue and chikungunya, and the leishmaniases, were the most studied. Yet even for malaria, long-term projections of future transmission scenarios remain inadequate for robust planning. Beyond the expected short-term effects of extreme weather events on local disease incidence, 45 it is difficult to be definitive 46 –global incidence and attributable deaths may go up, down or stay about the same, depending on multiple factors, including the success or otherwise of nascent vaccination programmes. 6 The arboviral NTDs, dengue and chikungunya, on the other hand, are generally predicted to continue their current surge. 28 , 29 Global expansion in the population at risk of the leishmaniases seems likely. The predicted effect of climate change on these diseases suggests that effects on vectors of other vector-borne NTDs will be similarly important to understand.

For many of the NTDs that we grouped as ‘non-vector-borne’, however, limitations in our capacity for prediction stem in part from gaping deficiencies in our understanding of disease transmission at steady state. Data published only after the searches were conducted for this review pin responsibility for Mycobacterium ulcerans transmission in southeastern Australia on the mosquito Aedes notoscriptus , 47 whereas transmission by mosquitos was previously hypothesised but unproven, and analogous work has not yet been published for Buruli ulcer-endemic areas of the Americas, Japan, Papua New Guinea or West Africa. Postulated mechanisms for the transmission of leprosy are still based on circumstantial evidence. 13 The nematode worm Dracunculus medinensis , the target of a global eradication programme that began in 1980, was only relatively recently discovered to infect paratenic and definitive hosts other than humans. 48 These gaps in our knowledge have lingered because funding for research on NTDs is thin 49 and spread across a very large number of pathogens (Table  1 ), some of which are probably relatively rare. 50 , 51

Multiplying that disease-specific uncertainty are uncertainties surrounding future climate scenarios and their secondary impacts (including, for example, on conflict, migration and demography), which are further clouded by our joint hope that individual and collective behaviours will change sufficiently to allow greenhouse gas concentrations to fall and thereby effectively mitigate climate change. This uncertainty for virtually every parameter of NTD transmission models 52 makes decadal projections of future NTD prevalence or incidence feel ill-advised. Unfortunately, without those projections, NTDs are likely to continue to be given very limited attention in climate-related discussions, including, for example, in the Assessment Reports of the Intergovernmental Panel on Climate Change. 53 Better understanding of NTD transmission dynamics, and estimates—even if heavily caveated—of the potential impacts of climate change, are precisely what is needed now.

The current work builds on previously published reviews, 12 , 43 , 54 but continues to have some limitations. First, although we undertook screening of titles and abstracts by two independent observers, our use of tags to highlight certain characteristics of papers within the Covidence platform may have unmasked some second screeners to the first screener's decision.

Second, screening for mitigation and adaptation strategies was challenging; the process required considerable judgement. It is possible that relevant sources were overlooked in the >42 000 records that our searches identified.

Third, we did not critically quality-appraise the methodology used for each included paper (e.g. number, size and origin of datasets; appropriateness of climate models, such as use of downscaling; and inclusion of all potentially relevant variables). Many studies had low power, did not consider all potential explanatory variables or confounders, or were otherwise methodologically weak. To be useful as a summary of coverage within the published literature, our visualisations imply that all studies contribute equally to the evidence base, whereas they do not.

Fourth, under-ascertainment is an issue for many diseases, but is particularly problematic for malaria and NTDs; their concentration in impoverished populations means that patients with these diseases have HAQIs that are far from ideal. Under-ascertainment is a specifically identified issue for dengue, in which second infections may be considerably more likely to produce disease that leads to clinical presentation and therefore registration. 55

Fifth, to be included in this review, a paper had to explicitly juxtapose climate change and relevant outcomes. Some authors may have made tenuous arguments linking weather-related variables (such as temperature or rainfall) to climate change, resulting in inclusion; others may not have been explicit in framing climate change implications when doing so would have been justifiable.

Sixth, it is likely that source data were used more than once in groups of papers with the same or related outcome measures for overlapping geographies and overlapping timespans.

Seventh, we did not specifically look for the impact of climate change mediated through internal displacement and migration of people; 56 changes in institutional capacity and service provision; 57 , 58 vector microbiome, genetics or gene expression; or pathogen genetics or gene expression. 59 , 60 All of these mechanisms may be important.

Eighth, as for any review, our searches had a fixed date range and were not exhaustive within that range. Not all possible intermediate and reservoir hosts (e.g. for rabies) were specifically included. Insect species with postulated but unproven vectorial capacity were excluded; Culex pipiens is a known vector of lymphatic filariasis in Egypt but papers considering it in other contexts were set aside. Studies in press were excluded by design; we were aware of forthcoming work on the impact of climate change on several diseases that had been submitted for peer review but were not yet published when our searches closed. The December 2023 addition of noma to the WHO's list of NTDs 61 occurred too late for noma to be included in our searches.

Ninth, the high degree of heterogeneity (in questions examined, methods used and so on) precluded quantitative synthesis.

Tenth, projecting disease burdens forward over long timescales means that future changes in treatment and control strategies would ideally also be taken into account. This is difficult to do. Authors of studies from the early part of our 2010–2023 publication window may not have foreseen the scale-up in intervention coverage that has occurred for many diseases in the past 10–15 y.

Despite uncertainty around data, some general conclusions and recommendations are proposed here. It can be inferred from existing data, first, that climate change is likely to have profound direct and indirect implications for malaria, dengue and chikungunya, leishmaniasis and at least several other vector-borne NTDs, even if the amplitude and direction of the effects will probably vary by disease and location, be non-linear 22 , 62–64 and evolve with time. Changes of two kinds will be apparent: diseases will move around, and where endemicity is constant, there will be local increases or decreases in incidence or prevalence. There is a pressing need to safeguard previous global health gains by scaling up proven interventions and achieving impact before future changes render those interventions ineffective. 65 Second, the lack of predictability, even over relatively short timescales, calls for existing surveillance and intervention systems to be reinforced and regularly reviewed. Integrated surveillance and intervention systems, covering multiple diseases 66 and taking a One Health approach, 67 could offer efficiencies. Third, communities should be consulted and involved in these reviews of surveillance and intervention systems, and in research undertaken at the interface of infectious diseases and climate change, to maximise the relevance of such efforts despite changing human populations. Fourth, integrating climate resilience into health systems is critical. This should encompass investing in health infrastructure, fostering cross-sector collaboration, adapting to the needs of displaced populations, improving access to health products and accelerating research and development to fill known gaps. 68 A particular requirement is access to existing and new countermeasures to limit future expansions in disease burden. Fifth, we do not know enough.

Recommendations for future research.

Research to fill current knowledge gaps on the likely impacts of climate change, mitigation and adaptation strategies on malaria and NTDs should:

where projections are modelled, be based on clearly defined climate scenarios, and include multiple scenarios, ideally using the most recent categories defined by the IPCC, in order to facilitate comparisons across studies, diseases and geographies.

where projections are modelled, incorporate not only climate scenarios but also sociodemographic and population density projections. This may require developments in methodology to ensure that demographic transitions underpinning the epidemiological models are in line with those assumed in the projections.

where projections are modelled, ideally incorporate detailed analyses of the likely impact of climate change mitigation and adaptation strategies, which are currently rare, and the modelled effectiveness of existing and new interventions (vector control, vaccines, treatments) under multiple climate scenarios.

explore the potential impacts of climate change on a broader set of NTDs and geographies, prioritising places with the highest disease burdens and the people most vulnerable to the future impacts of climate change.

recognise that, because of the paucity of data, it will remain challenging to estimate the impact of climate change and other secular trends on NTDs, and to anticipate potential interactions between climate change and the impact of interventions. Therefore, new methodologies are needed, based on plausible biological assumptions. This will require distinct study types to prepare for modelling, including prospective population-based investigations, laboratory studies, biological experiments (e.g. mosquito or egg survival) and social science that can be performed in suitable locations to inform projections and provide a data source for future estimates of change. Investigating methods to extrapolate laboratory findings to field settings would be beneficial.

prioritise standardisation and collaboration, including across disciplines. Specifically for modelling, we propose the development and adoption of standardised frameworks for future projections, using, where possible, standardised survey or case data, and an open collaborative model in which source data and contributions to code can be tracked, to speed up and unify research while protecting the rights of countries that generate primary data and acknowledging all collaborators.

facilitate leadership of scientists in affected areas to undertake and communicate research and its implications. An understanding of local context and closer relationships with stakeholders will lead to higher quality analyses with increased uptake in local decision-making processes.

where projections are developed, provide actionable data for policymaking at national and subnational levels. For example, studies focusing on climate-driven dengue expansion to new locations (both in high-income and low- and middle-income countries) should investigate appropriate methods of surveillance, which could be targeted at high-risk areas in a cost-efficient manner. (Risk here could be interpreted in multiple ways: relating to the potential for increases in vector abundance, infection, severe disease or outcomes such as lost gross domestic product (GDP), for example.)

Based on our analysis, we also propose several key recommendations to guide future studies (Box 2 ). The most important of these is for standardisation and collaboration. Our scope included 21 diseases and disease groups, at least 76 distinct pathogens, 373 venomous snakes and humans everywhere; there is insufficient modelling capacity globally for this to be investigated on a competitive basis, particularly when the appropriate modelling methodologies change with the level of endemicity and results are needed at multiple scales. Indeed, our analysis suggests that existing studies may not be sufficiently focused on areas where the need to plan for adaptation may be greatest. We recommend holistic approaches to risk assessment, incorporating more of the available data and recruiting more of the available brainpower to undertake ensemble analyses with agreed best-practice methodology. Modelling efforts should incorporate consideration of humans, pathogens, vectors, intermediate and reservoir hosts and the effect of relevant interventions, as appropriate, to generate predictions over decadal time frames—and not ignore populations where these diseases are currently endemic. Collectively, these measures should reduce potential duplication and hopefully produce more complete and more accurate estimates of future vulnerability, exposure and impact. Open-source collaborative modelling platforms 17 , 23 could facilitate contributions from as many relevant stakeholders as are willing to engage, and allow tailoring of consistently high-quality outputs for specific audiences. Collaboration could include involvement of affected communities through citizen science: in vector surveillance, for example. Accessible global databases on disease and vector occurrence 69–75 should be harnessed and adapted to cover additional diseases. Broader use of remotely sensed climate data should be explored, particularly where locally acquired data are unavailable or microclimates are of relevance. Long-term time-series data should be pooled and re-analysed to tease out the relative contributions of deliberate interventions, secular trends, seasonality and climate change. Production of detailed risk and distribution maps should be facilitated to help plan local control and elimination efforts. The fact that many NTDs are targeted for eradication, interruption of transmission or elimination as a public health problem by 2030 should not dissuade us from taking a long-term view of this work; 43 global health ambitions are not always realised, and the best possible current understanding of counterfactual scenarios should help decision-makers to target resources and chart the most appropriate course.

Conclusions

It is difficult to have immersed ourselves in this literature as we have without acquiring a deepened sense of foreboding over the adverse influence that we as a species are visiting on our planet and its most vulnerable people. Adverse changes have already occurred in the incidence or prevalence of infectious diseases that cause death or profound morbidity. Women, children, older people, indigenous groups and ethnic minorities, migrants and the very poor have contributed least but are likely to experience most of the effects of the climate crisis, 76 notably including through any increase in the burden of malaria or NTDs. An emerging opportunity to correct this inequity arises through financial commitments to NTD control and elimination made at the 28th United Nations Climate Change Conference in December 2023. 77 Allocation of these resources should be guided by informed scenario analyses of current and future disease burden. The work described in this review is a start; convening stakeholders globally to advance the research agenda must be our next collective move.

CLD, TDH, AWS and ISF conceived the overall study design, which was elaborated by PK, JLH, CLD, MA, MB, IB, SD, DLM, CMRT, KRvD, TDH, AWS and ISF, with review by all authors; PK, JLH, CLD, MA, MB, IB, SD, CMRT, KRvD and AWS screened titles and abstracts, located full texts and undertook full-text review; PK and JLH identified seed papers and undertook backward and forward citation searches; PK, JLH, CLD, MA, MB, IB, SD, CMRT, KRvD, JA, AD, DSE, JG, MRJ, AMK, JK, WJK, TLL, JSM, JP, NP, AR, LJR, ZMR, GSGS and AWS extracted data; PK, JLH, KRvD, JFM, CNA, HSR, DRMS and TDH conducted quantitative analyses and constructed figures; PK, KRvD, KCR, CNA and AWS prepared the first draft of the manuscript, which was critically revised by all authors. All authors reviewed and approved the final manuscript. PK and AWS are the paper's guarantors.

We are grateful to Abdisalan M. Noor, lead author of the climate chapter of the World Malaria Report 2023, for his leadership in this space, and to Paul Courtright for assistance with translation from Korean to English.

This work was supported by Reaching the Last Mile; The Fred Hollows Foundation; Bill & Melinda Gates Foundation and the European Commission. PK, SK, CNA and TDH were supported by funding from the Bill & Melinda Gates Foundation [INV-030046], via the NTD Modelling Consortium. TDH is supported by funding from the Li Ka Shing Foundation. JLH acknowledges funding from USAID through an Interagency Agreement with CDC awarded to DLM. KRvD and RL acknowledge funding from the European Union's Horizon Europe research and innovation programme [grant agreement no. 101057554] (Horizon Europe project IDAlert, https://idalertproject.eu ); IDAlert is part of the EU climate change and health cluster ( https://climate-health.eu ). BA, AFG, JK, VL, AR, KHS, RV, SW, AY, DCL, AWS and ISF are staff members of, and CLD and CMRT are consultants to, the WHO. JA was supported by an appointment to the Research Participation Program at the Centers for Disease Control and Prevention, administered by the Oak Ridge Institute for Science and Education through an interagency agreement between the U.S. Department of Energy and the Centers for Disease Control and Prevention. SK, AMK, JSM, MRJ, TLL and GSGS were supported by funding from the Bill & Melinda Gates Foundation [INV-016807]. NMF was supported by funding from Wellcome, the Jameel Institute and the MRC Centre for Global Infectious Disease Analysis. JFM is supported by grant funding from the Bill & Melinda Gates Foundation and Gavi. RSN and KP are staff members of the Pan American Health Organization.

SD is and JC was an employee of The Fred Hollows Foundation; SJB is an employee of the Bill & Melinda Gates Foundation. Their participation in this work was in their personal capacity. All other authors declare no competing interests.

Not required.

All data relevant to the study are available in Supplementary Table 2 and Supplementary Table 3 . Code available upon request.

The authors alone are responsible for the views expressed in this article and they do not necessarily represent the views, decisions or policies of the institutions with which they are affiliated. The boundaries and names shown and the designations used on the maps in this article do not imply the expression of any opinion whatsoever on the part of the authors, or the institutions with which they are affiliated, concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries.

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• chikungunya fever
• dengue fever
• cost of illness
• leishmaniasis
• tropical disease
• climate change

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• Malaria is typically transmitted in tropical and subtropical areas.
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Altitude and climatic factors including temperature, humidity, and rainfall impact where malaria spreads. Malaria is typically transmitted in tropical and subtropical areas, where

• Anopheles mosquitoes can survive and multiply, and
• Malaria parasites can complete their growth cycle in the mosquitoes ("extrinsic incubation period").

Temperature is particularly critical. For example, at temperatures below 20°C (68°F), Plasmodium falciparum (which causes severe malaria) cannot complete its growth cycle in the Anopheles mosquito. Therefore, it cannot spread in these areas.

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In many countries where malaria spreads, you will not find it in all parts of the country. Even within tropical and subtropical areas, you will not find malaria

• At very high altitudes,
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• In some countries where spread has been interrupted through successful control/elimination programs.

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Most cases of malaria occur in sub-Saharan Africa, but it also occurs in parts of Oceania (such as Papua New Guinea) and in parts of Central and South America and Southeast Asia.

In cooler regions, spread is less intense and more seasonal. There, P. vivax might be more prevalent because it is more tolerant of lower average temperatures.

In many temperate areas, such as western Europe and the United States, economic development and public health measures have succeeded in eliminating malaria. However, most of these areas have Anopheles mosquitoes that can spread malaria, and reintroduction of the disease remains a risk.

Malaria is a serious disease caused by a parasite that infects the Anopheles mosquito. You get malaria when bitten by an infective mosquito.

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Institute of Medicine (US) Committee for the Study on Malaria Prevention and Control; Oaks SC Jr., Mitchell VS, Pearson GW, et al., editors. Malaria: Obstacles and Opportunities. Washington (DC): National Academies Press (US); 1991.

Malaria: Obstacles and Opportunities.

• Hardcopy Version at National Academies Press

1 Conclusions and Recommendations

• DEFINING THE PROBLEM

The outlook for malaria control is grim. The disease, caused by mosquito-borne parasites, is present in 102 countries and is responsible for over 100 million clinical cases and 1 to 2 million deaths each year. Over the past two decades, efforts to control malaria have met with less and less success. In many regions where malaria transmission had been almost eliminated, the disease has made a comeback, sometimes surpassing earlier recorded levels. The dream of completely eliminating malaria from many parts of the world, pursued with vigor during the 1950s and 1960s, has gradually faded. Few believe today that a global eradication of malaria will be possible in the foreseeable future.

Worldwide, the number of cases of malaria caused by Plasmodium falciparum , the most dangerous species of the parasite, is on the rise. Drug-resistant strains of P. falciparum are spreading rapidly, and there have been recent reports of drug resistance in people infected with P. vivax , a less virulent form of the parasite. Furthermore, mosquitoes are becoming increasingly resistant to insecticides, and in many cases, have adapted so as to avoid insecticide-treated surfaces altogether.

In large part because of the spread of drug and insecticide resistance, there are fewer tools available today to control malaria than there were 20 years ago. In many countries, the few remaining methods are often applied inappropriately. The situation in many African nations is particularly dismal, exacerbated by a crumbling health infrastructure that has made the implementation of any disease control program difficult.

Malaria cases among tourists, business travelers, military personnel, and migrant workers in malarious areas have been increasing steadily in the last several years, posing new concerns that the disease will be introduced to currently nonmalarious areas. Recent epidemics have claimed tens of thousands of lives in Africa, and there is an increasing realization that malaria is a major impediment to socioeconomic development in many countries. Unless practical, cost-effective strategies can be developed and successfully implemented, malaria will continue to exact a heavy toll on human life and health around the world.

Although often considered a single disease, malaria is more accurately viewed as many diseases, each shaped by subtle interactions of biologic, ecologic, social, and economic factors. The species of parasite, the behavior of the mosquito host, the individual's immune status, the climate, human activities, and access to health services all play important roles in determining the intensity of disease transmission, who will become infected, who will get sick, and who will die.

Gem miners along the Thailand-Cambodia border, American tourists on a wildlife safari in East Africa, villagers living on the central highlands in Madagascar, residents of San Diego County, California, a young pregnant woman in Malawi, Swiss citizens living near Geneva International Airport, children in Africa south of the Sahara, and a U.S. State Department secretary in Tanzania seem to have little in common, yet they are all at risk of contracting malaria. Because of the disease's variable presentations, each will be affected differently, as illustrated below.

• For the hundreds of thousands of Thai seasonal agricultural workers who travel deep into the forest along the Thailand-Cambodia border to mine for gems, malaria is the cost of doing business. These young men are exposed to aggressive forest mosquitoes, and within two to three weeks after arriving, almost every miner will get malaria. Many gem miners seek medications to prevent and self-treat mild cases of the disease. But because malaria in this part of the world is resistant to most antimalarial drugs, the few effective drugs are reserved for the treatment of confirmed cases of malaria. To complicate matters, there are no health services in the forest to treat patients, and the health clinics in Thailand are overburdened by the high demand for treating those with severe malaria, most of whom are returning gem miners. A similar scenario involving over 400,000 people exists among gold miners in Rondonia, Brazil.
• Each year, over seven million U.S. citizens visit parts of the world where malaria is present. Many, at the recommendation of their travel agent or physician, take antimalarial medications as a preventive measure, but a significant number do not. Tourists and other travelers who have never been exposed to malaria, and therefore have never developed protective immunity, are at great risk for contracting severe disease. Ironically, it is not the infection itself that poses the biggest danger, but the chance that treatment will be delayed because of misdiagnosis upon the individual's return to the United States. Most U.S. doctors have never seen a patient with malaria, are often confused by the wide array of symptoms, and are largely unaware that malaria in a nonimmune person can be a medical emergency, sometimes rapidly fatal.
• Prior to 1950, malaria was the major cause of death in the central highlands of the African island nation of Madagascar. In the late 1950s, an aggressive program of indoor insecticide spraying rid the area of malaria-carrying mosquitoes, and malaria virtually disappeared. By the 1970s, confident of a victory in the battle against malaria, Madagascar began to phase out its spraying program; in some areas spraying was halted altogether. In the early 1980s, the vector mosquitoes reinvaded the central highlands, and in 1986 a series of devastating epidemics began. The older members of the population had long since lost the partial immunity they once had, and the younger island residents had no immunity at all. During the worst of the epidemics, tens of thousands of people died in one three-month period. The tragedy of this story is that it could have been prevented. A cheap antimalarial drug, chloroquine, could have been a powerful weapon in Madagascar, where drug resistance was not a significant concern. Because of problems in international and domestic drug supply and delivery, however, many people did not receive treatment and many died. In the last 18 months, surveillance has improved, spraying against the mosquito has resumed, and more effective drug distribution networks have been established. Malaria-related mortality has declined sharply as a result.
• Malaria, once endemic in the southern United States, occurs relatively infrequently. Indeed, there have been only 23 outbreaks of malaria since 1950, and the majority of these occurred in California. But for each of the past three years, the San Diego County Department of Health Services has had to conduct an epidemiologic investigation into local transmission of malaria. An outbreak in the late summer of 1988 involved 30 persons, the largest such outbreak in the United States since 1952. In the summer of 1989, three residents of San Diego County—a migrant worker and two permanent residents—were diagnosed with malaria; in 1990, a teenager living in a suburb of San Diego County fell ill with malaria. All of the cases were treated successfully, but these incidents raise questions about the possibility of new and larger outbreaks in the future. Malaria transmission in San Diego County (and in much of California) is attributed to the presence of individuals from malaria-endemic regions who lack access to medical care, the poor shelter and sanitation facilities of migrant workers, and the ubiquitous presence of Anopheles mosquitoes in California.
• A 24-year-old pregnant Yao woman from the Mangochi District in Malawi visited the village health clinic monthly to receive prenatal care. While waiting to be seen by the health provider, she and other women present listened to health education talks which were often about the dangers of malaria during pregnancy, and the need to install screens around the house to keep the mosquitoes away, to sleep under a bednet, and to take a chloroquine tablet once a week. Toward the end of her second trimester of pregnancy, the woman returned home from her prenatal visit with her eight tablets of chloroquine wrapped in a small packet of brown paper. She promptly gave the medicine to her husband to save for the next time he or one of their children fell ill. The next week she developed a very high malarial fever and went into labor prematurely. The six-month-old fetus was born dead.
• Over a two-week period in the summer of 1989, five Swiss citizens living within a mile of Geneva International Airport presented at several hospitals with acute fever and chills. All had malaria. Four of the five had no history of travel to a malarious region; none had a history of intravenous drug use or blood transfusion. Apart from their symptoms, the only thing linking the five was their proximity to the airport. A subsequent epidemiologic investigation suggested that the malaria miniepidemic was caused by the bite of stowaway mosquitoes en route from a malaria- endemic country. The warm weather, lack of systematic spraying of aircraft, and the close proximity of residential areas to the airport facilitated the transmission of the disease.
• Malaria is a part of everyday life in Africa south of the Sahara. Its impact on children is particularly severe. Mothers who bring unconscious children to the hospital often report that the children were playing that morning, convulsed suddenly, and have been unconscious ever since. These children are suffering from the most frequently fatal complication of the disease, cerebral malaria. Other children succumb more slowly to malaria, becoming progressively more anemic with each subsequent infection. By the time they reach the hospital, they are too weak to sit and are literally gasping for breath. Many children are brought to hospitals as a last resort, after treatment given for “fever” at the local health center has proved ineffective. Overall, children with malaria account for a third of all hospital admissions. A third of all children hospitalized for malaria die. In most parts of Africa, there are no effective or affordable options to prevent the disease, so children are at high risk until they have been infected enough times to develop a partial immunity.
• A 52-year-old American woman, the secretary to the U.S. ambassador in Tanzania, had been taking a weekly dose of chloroquine to prevent malaria since her arrival in the country the year before. She arrived at work one morning complaining of exhaustion, a throbbing headache, and fever. A blood sample was taken and microscopically examined for malaria parasites. She was found to be infected with P. falciparum , and was treated immediately with high doses of chloroquine. That night, she developed severe diarrhea, and by morning she was found to be disoriented and irrational. She was diagnosed as having cerebral malaria, and intravenous quinine treatment was started. Her condition gradually deteriorated—she became semicomatose and anemic, and approximately 20 percent of her red blood cells were found to be infected with malaria parasites. After continued treatment for several days, no parasites were detected in her blood. Despite receiving optimal care, other malaria-related complications developed and she died just nine days after the illness began. The cause of death: chloroquine-resistant P. falciparum .

These brief scenarios give a sense of the diverse ways that malaria can affect people. So fundamental is this diversity with respect to impact, manifestation, and epidemiology that malaria experts themselves are not unanimous on how best to approach the disease. Malariologists recognize that malaria is essentially a local phenomenon that varies greatly from region to region and even from village to village in the same district. Consequently, a single global technology for malaria control is of little use for specific conditions, yet the task of tailoring strategies to each situation is daunting. More important, many malarious countries do not have the resources, either human or financial, to carry out even the most meager efforts to control malaria.

These scenarios also illustrate the dual nature of malaria as it affects U.S. policy. In one sense, it is a foreign aid issue; a devastating disease is currently raging out of control in vast, heavily populated areas of the world. In another sense, malaria is of domestic public health concern. The decay of global malaria control and the invasion of the parasite into previously disease-free areas, coupled with the increasing frequency of visits to such areas by American citizens, intensify the dangers of malaria for the U.S. population. Tourists, business travelers, Peace Corps volunteers, State Department employees, and military personnel are increasingly at risk, and our ability to protect and cure them is in jeopardy. What is desperately needed is a better application of existing malaria control tools and new methods of containing the disease.

In most malarious regions of the world, there is inadequate access to malaria treatment. Appropriate health facilities may not exist; those that do exist may be inaccessible to affected populations, may not be supplied with effective drugs, or may be staffed inappropriately. In many countries, the expansion of primary health care services has not proceeded according to expectations, particularly in the poorest (and most malarious) nations of the tropical world.

In some countries, antimalarial interventions are applied in broad swaths, without regard to underlying differences in the epidemiology of the disease. In other countries, there are no organized interventions at all. The malaria problem in many regions is compounded by migration, civil unrest, poorly planned exploitation of natural resources, and their frequent correlate, poverty.

During the past 15 years, much research has focused on developing vaccines for malaria. Malaria vaccines are thought to be possible in part because people who are naturally exposed to the malaria parasite acquire a partial immunity to the disease over time. In addition, immunization of animals and humans by the bites of irradiated mosquitoes infected with the malaria parasite can protect against malaria infection. Much progress has been made, but current data suggest that effective vaccines are not likely to be available for some time.

Compounding the difficulty of developing more effective malaria prevention, treatment, and control strategies is a worldwide decline in the pool of scientists and health professionals capable of conducting field research and organizing and managing malaria control programs at the country level. With the change in approach from malaria eradication to malaria control, many malaria programs “lost face,” admitting failure and losing the priority interest of their respective ministries of health. As external funding agencies lost interest in programs, they reduced their technical and financial support. As a consequence, there were fewer training opportunities, decreased contacts with international experts, and diminished prospects for improving the situation. Today, many young scientists and public health specialists, in both the developed and developing countries, prefer to seek higher-profile activities with better defined opportunities for career advancement.

It is against this backdrop of a worsening worldwide malaria situation that the Institute of Medicine was asked to convene a multidisciplinary committee to assess the current status of malaria research and control and to make recommendations to the U.S. government on promising and feasible strategies to address the problem. During the 18-month study, the committee reviewed the state of the science in the major areas of malariology, identified gaps in knowledge within each of the major disciplines, and developed recommendations for future action in malaria research and control.

Organization

Chapter 2 summarizes key aspects of the individual state-of-the-science chapters, and is intended to serve as a basic introduction to the medical and scientific aspects of malaria, including its clinical signs, diagnosis, treatment, and control. Chapter 3 provides a historical overview of malaria, from roughly 3000 B.C. to the present, with special emphasis on efforts in this century to eradicate and control the disease. The state-of-the-science reviews, which start in Chapter 4 , begin with a scenario titled “Where We Want To Be in the Year 2010.” Each scenario describes where the discipline would like to be in 20 years and how, given an ideal world, the discipline would have contributed to malaria control efforts. The middle section of each chapter contains a critical review of the current status of knowledge in the particular field. The final section lays out specific directions for future research based on a clear identification of the major gaps in scientific understanding for that discipline. The committee urges those agencies that fund malaria research to consult the end of each state-of-the-science chapter for suggestions on specific research opportunities in malaria.

Sponsorship

This study was sponsored by the U.S. Agency for International Development, the U.S. Army Medical Research and Development Command, and the National Institute of Allergy and Infectious Diseases of the National Institutes of Health.

• CONCLUSIONS AND RECOMMENDATIONS

A major finding of the committee is the need to increase donor and public awareness of the growing risk presented by the resurgence of malaria. Overall, funding levels are not adequate to meet the problem. The committee believes that funding in the past focused too sharply on specific technologies and particular control strategies (e.g., indiscriminate use of insecticide spraying). Future support must be balanced among the needs outlined in this report. The issue for prioritization is not whether to select specific technologies or control strategies, but to raise the priority for solving the problem of malaria. This is best done by encouraging balanced research and control strategies and developing a mechanism for periodically adjusting support for promising approaches.

This report highlights those areas which the committee believes deserve the highest priority for research or which should be considered when U.S. support is provided to malaria control programs. These observations and suggestions for future action, presented below in four sections discussing policy, research, control, and training, represent the views of a multidisciplinary group of professionals from diverse backgrounds and with a variety of perspectives on the problem.

The U.S. government is the largest single source of funds for malaria research and control activities in the world. This investment is justified by the magnitude of the malaria problem, from both a foreign aid and a public health perspective. The increasing severity of the threat of malaria to residents of endemic regions, travelers, and military personnel, and our diminishing ability to counter it, should be addressed by a more comprehensive and better integrated approach to malaria research and control. However, overall U.S. support for malaria research and control has declined over the past five years. The committee believes that the amount of funding currently directed to malaria research and control activities is inadequate to address the problem.

Over the past 10 years, the majority of U.S. funds available for malaria research have been devoted to studies on immunity and vaccine development. Although the promise of vaccines remains to be realized, the committee believes that the potential benefits are enormous. At the same time, the relative paucity of funds available for research has prevented or slowed progress in other areas. Our incomplete knowledge about the basic biology of malaria parasites, how they interact with their mosquito and human hosts, and how human biology and behavior affect malaria transmission and control remains a serious impediment to the development and implementation of malaria control strategies. The committee believes that this situation must be addressed without reducing commitment to current research initiatives. The committee further believes that such research will pay long-term dividends in the better application of existing tools and the development of new drugs, vaccines, and methods for vector control.

The committee recommends that increased funds be made available so that U.S. research on malaria can be broadened according to the priorities addressed in this report, including laboratory and field research on the biology of malaria parasites, their mosquito vectors, and their interaction with humans.

The committee believes that the maximum return on investment of funds devoted to malaria research and control can be achieved only by rigorous review of project proposals. The committee further believes that the highest-quality review is essential to ensure that funding agencies spend their money wisely. The committee believes that all U.S.-supported malaria field activities, both research and control, should be of the highest scientific quality and relevance to the goals of malaria control.

The committee recommends decisions on funding of malaria research be based on scientific merit as determined by rigorous peer review, consistent with the guidelines of the National Institutes of Health or the United Nations Development Program/World Bank/ World Health Organization Special Programme for Research and Training in Tropical Diseases, and that all U.S.-supported malaria field projects be subject to similar rigorous review to ensure that projects are epidemiologically and scientifically sound.

Commitment and Sustainability

For malaria control, short-term interventions can be expected to produce only short-term results. The committee believes that short-term interventions are justified only for emergency situations. Longer-term interventions should be undertaken only when there is a national commitment to support sustained malaria surveillance and control.

The committee recommends that malaria control programs receive sustained international and local support, oriented toward the development of human resources, the improvement of management skills, the provision of supplies, and the integration of an operational research capability in support of an epidemiologically sound approach to malaria control.

Surveillance

During the major effort to eradicate malaria from many parts of the world that began in the late 1950s and ended in 1969, it was important to establish mechanisms to detect all malaria infections. As a result, systems were established in many countries to collect blood samples for later microscopic examination for the presence of parasites. Each year, the results from more than 140 million slides are reported to the World Health Organization, of which roughly 3 to 5 percent are positive for malaria. This approach seeks to answer the question posed 30 years ago: How many people are infected with the malaria parasite? It does not answer today's questions: Who is sick? Where? Why? The committee concludes that the mass collection of blood slides requires considerable resources, poses serious biosafety hazards, deflects attention from the treatment of ill individuals, and has little practical relevance for malaria control efforts today.

Instead of the mass collection of slides, the committee believes that the most effective surveillance networks are those that concurrently measure disease in human populations, antimalarial drug use, patterns of drug resistance, and the intensity of malaria transmission by vector populations. The committee believes that malaria surveillance practices have not received adequate recognition as an epidemiologic tool for designing, implementing, and evaluating malaria control programs.

The committee recommends that countries be given support to orient malaria surveillance away from the mass collection and screening of blood slides toward the collection and analysis of epidemiologically relevant information that can be used to monitor the current situation on an ongoing basis, to identify high-risk groups, and to detect potential epidemics early in their course.

Inter-Sectoral Cooperation

The committee believes that insufficient attention has been paid to the impact that activities in non-health-related sectors, such as construction, industry, irrigation, and agriculture, have on malaria transmission. Conversely, there are few assessments of the impact of malaria control projects on other public health initiatives, the environment, and the socioeconomic status of affected populations. Malaria transmission frequently occurs in areas where private and multinational businesses and corporations (e.g., hotel chains, mining operations, and industrial plants) have strong economic interests. Unfortunately and irresponsibly, some local and multinational businesses contribute few if any resources to malaria control in areas in which they operate.

The committee recommends greater cooperation and consultation between health and nonhealth sectors in the planning and implementation of major development projects and malaria activities. It also recommends that all proposed malaria control programs be analyzed for their potential impact on other public health programs, the environment, and social and economic welfare, and that local and multinational businesses be recruited by malaria control organizations to contribute substantially to local malaria control efforts.

New Tools for Malaria Control

The committee believes that, as a policy directive, it is important to support research activities to develop new tools for malaria control. The greatest momentum for the development of new tools exists in vaccine and drug development, and the committee believes it essential that this momentum be maintained. The committee recognizes that commendable progress has been made in defining the characteristics of antigens and delivery systems needed for effective vaccines, but that the candidates so far tested fall short of the goal. Much has been learned which supports the hope that useful vaccines can be developed. To diminish activity in vaccine development at this stage would deal a severe blow to one of our best chances for a technological breakthrough in malaria control.

The committee recommends that vaccine development continue to be a priority of U.S.-funded malaria research.

Only a handful of drugs are available to prevent or treat malaria, and the spread of drug-resistant strains of the malaria parasite threatens to reduce further the limited pool of effective drugs. The committee recognizes that there is little economic incentive for U.S. pharmaceutical companies to undertake antimalarial drug discovery activities. The committee is concerned that U.S. government support of these activities, based almost entirely at the Walter Reed Army Institute of Research (WRAIR), has decreased and is threatened with further funding cuts. The committee concludes that the WRAIR program in antimalarial drug discovery, which is the largest and most successful in the world, is crucial to international efforts to develop new drugs for malaria. The benefits of this program in terms of worldwide prevention and treatment of malaria have been incalculable.

The committee strongly recommends that drug discovery and development activities at WRAIR receive increased and sustained support.

The next recommendation on policy directions reflects the committee's concern about the lack of involvement in malaria research by the private sector. The committee believes that the production of candidate malaria vaccines and antimalarial drugs for clinical trials has been hampered by a lack of industry involvement. Greater cooperation and a clarification of the contractual relationships between the public and private sectors would greatly enhance the development of drugs and vaccines.

The committee recommends that mechanisms be established to promote the involvement of pharmaceutical and biotechnology firms in the development of malaria vaccines, antimalarial drugs, and new tools for vector control.

Coordination and Integration

The committee is concerned that there is inadequate joint planning and coordination among U.S.-based agencies that support malaria research and control activities. Four government agencies and many nongovernmental organizations in the United States are actively involved in malaria-related activities. There are also numerous overseas organizations, governmental and nongovernmental, that actively support such activities worldwide.

The complexity and variability of malaria, the actual and potential scientific advances in several areas of malariology, and most important the worsening worldwide situation argue strongly for an ongoing mechanism to assess and influence current and future U.S. efforts in malaria research and control.

The committee strongly recommends the establishment of a national advisory body on malaria.

In addition to fulfilling a much needed coordinating function among U.S.-based agencies and between the U.S. and international efforts, the national advisory body could monitor the status of U.S. involvement in malaria research and control, assess the relevant application of knowledge, identify areas requiring further research, make recommendations to the major funding agencies, and provide a resource for legislators and others interested in scientific policy related to malaria. The national advisory body could convene specific task-oriented scientific working groups to review research and control activities and to make recommendations, when appropriate, for changes in priorities and new initiatives.

The committee believes that the national advisory body should be part of, and appointed by, a neutral and nationally respected scientific body and that it should actively encourage the participation of governmental and nongovernmental organizations, industry, and university scientists in advising on the direction of U.S. involvement in malaria research and control.

The increasing magnitude of the malaria problem during the past decade and the unpredictability of changes in human, parasite, and vector determinants of transmission and disease point strongly to the need for such a national advisory body, which can be responsive to rapidly changing problems, and advances in scientific research, relating to global efforts to control malaria.

Malaria Research Priorities

Malaria control is in crisis in many areas of the world. People are contracting and dying of severe malaria in unprecedented numbers. To address these problems, the committee strongly encourages a balanced research agenda. Two basic areas of research require high priority. Research that will lead to improved delivery of existing interventions for malaria, and the development of new tools for the control of malaria.

Research in Support of Available Control Measures

Risk Factors for Severe Malaria People who develop severe and complicated malaria lack adequate immunity, and many die from the disease. Groups at greatest risk include young children and pregnant women in malaria endemic regions; nonimmune migrants, laborers, and visitors to endemic regions; and residents of regions where malaria has been recently reintroduced. For reasons that are largely unknown, not all individuals within these groups appear to be at equal risk for severe disease. The committee believes that the determinants of severe disease, including risk factors associated with a population, the individual (biologic, immunologic, socioeconomic, and behavioral), the parasite, or exposure to mosquitoes, are likely to vary considerably in different areas.

The committee recommends that epidemiologic studies on the risk factors for severe and complicated malaria be supported.

Pathogenesis of Severe and Complicated Malaria Even with optimal care, 20 to 30 percent of children and adults with the most severe form of malaria—primarily cerebral malaria—die. The committee believes that a better understanding of the disease process will lead to improvements in preventing and treating severe forms of malaria. The committee further believes that determining the indications for treatment of severe malarial anemia is of special urgency given the risk of transmitting the AIDS virus through blood transfusions, the only currently available treatment for malarial anemia. Physicians need to know when it is appropriate to transfuse malaria patients.

The committee recommends greater support for research on the pathogenesis of severe and complicated malaria, on the mechanisms of malarial anemia, and on the development of specific criteria for blood transfusions in malaria.

Social Science Research The impact of drugs to control disease or programs to reduce human-mosquito contact is mediated by local practices and beliefs about malaria and its treatment. Most people in malaria- endemic countries seek initial treatment for malaria outside of the formal health sector. Programs that attempt to influence this behavior must understand that current practices satisfy, at some level, local concerns regarding such matters as access to and effectiveness of therapy, and cost. These concerns may lead to practices at odds with current medical practice. Further, many malaria control programs have not considered the social, cultural, and behavioral dimensions of malaria, thereby limiting the effectiveness of measures undertaken. The committee recognizes that control programs often fail to incorporate household or community concerns and resources into program design. In most countries, little is known about how the demand for and utilization of health services is influenced by such things as user fees, location of health clinics, and the existence and quality of referral services. The committee concludes that modern social science techniques have not been effectively applied to the design, implementation, and evaluation of malaria control programs.

The committee recommends that research be conducted on local perceptions of malaria as an illness, health-seeking behaviors (including the demand for health care services), and behaviors that affect malaria transmission, and that the results of this research be included in community-based malaria control interventions that promote the involvement of communities and their organizations in control efforts.

Innovative Approaches to Malaria Control Malaria control programs will require new ideas and approaches, and new malaria control strategies need to be developed and tested. There is also a need for consistent support of innovative combinations of control technologies and for the transfer of new technologies from the laboratory to the clinic and field for expeditious evaluation. Successful technology transfer requires the exchange of scientific research, but more importantly, must be prefaced by an improved understanding of the optimal means to deliver the technology to the people in need (see Chapter 11 ).

The committee recommends that donor agencies provide support for research on new or improved control strategies and into how new tools and technologies can be better implemented and integrated into on-going control efforts.

Development of New Tools

Antimalarial Immunity and Vaccine Development Many people are able to mount an effective immune response that can significantly mitigate symptoms of malaria and prevent death. The committee believes that the development of effective malaria vaccines is feasible, and that the potential benefits of such vaccines are enormous. Several different types of malaria vaccines need to be developed: vaccines to prevent infection (of particular use for tourists and other nonimmune visitors to endemic countries), prevent the progression of infection to disease (for partially immune residents living in endemic areas and for nonimmune visitors), and interrupt transmission of parasites by vector populations (to reduce the risk of new infections in humans). The committee believes that each of these directions should be pursued.

The committee recommends sustained support for research to identify mechanisms and targets of protective immunity and to exploit the use of novel scientific technologies to construct vaccines that induce immunity against all relevant stages of the parasite life cycle.

Drug Discovery and Development Few drugs are available to prevent or treat malaria, and the spread of drug-resistant strains of malaria parasites is steadily reducing the limited pool of effective chemotherapeutic agents. The committee believes that an inadequate understanding of parasite biochemistry and biology impedes the process of drug discovery and slows studies on the mechanisms of drug resistance.

The committee recommends increased emphasis on screening compounds to identify new classes of potential antimalarial drugs, identifying and characterizing vulnerable targets within the parasite, understanding the mechanisms of drug resistance, and identifying and developing agents that can restore the therapeutic efficacy of currently available drugs.

Vector Control Malaria is transmitted to humans by the bites of infective mosquitoes. The objective of vector control is to reduce the contact between humans and infected mosquitoes. The committee believes that developments are needed in the areas of personal protection, environmental management, pesticide use and application, and biologic control, as well as in the largely unexplored areas of immunologic and genetic approaches for decreasing parasite transmission by vectors.

The committee recommends increased support for research on vector control that focuses on the development and field testing of methods for interrupting parasite transmission by vectors.

Malaria Control

Malaria is a complex disease that, even under the most optimistic scenario, will continue to be a major health threat for decades. The extent to which malaria affects human health depends on a large number of epidemiologic and ecologic factors. Depending on the particular combination of these and other variables, malaria may have different effects on neighboring villages and people living in a single village. All malaria control programs need to be designed with a view toward effectiveness and sustainability, taking into account the local perceptions, the availability of human and financial resources, and the multiple needs of the communities at risk. If community support for health sector initiatives is to be guaranteed, the public needs to know much more about malaria, its risks for epidemics and severe disease, and difficulties in control.

Unfortunately, there is no “magic bullet” solution to the deteriorating worldwide malaria situation, and no single malaria control strategy will be applicable in all regions or epidemiologic situations. Given the limited available financial and human resources and a dwindling pool of effective antimalarial tools, the committee suggests that donor agencies support four priority areas for malaria control in endemic countries.

The committee believes that the first and most basic priority in malaria control is to prevent infected individuals from becoming severely ill and dying. Reducing the incidence of severe morbidity and malaria-related mortality requires a two-pronged approach. First, diagnostic, treatment, and referral capabilities, including the provision of microscopes, training of technicians and other health providers, and drug supply, must be enhanced. Second, the committee believes that many malaria-related deaths could be averted if individuals and caretakers of young children knew when and how to seek appropriate treatment and if drug vendors, pharmacists, physicians, nurses, and other health care providers were provided with up-to-date and locally appropriate treatment and referral guidelines. The development and implementation of an efficient information system that provides rapid feedback to the originating clinic and area is key to monitoring the situation and preventing epidemics.

The committee believes that the second priority should be to promote personal protection measures (e.g., bednets, screens, and mosquito coils) to reduce or eliminate human-mosquito contact and thus to reduce the risk of infection for individuals living in endemic areas. At the present time, insecticide-treated bednets appear to be the most promising personal protection method.

In many environments, in addition to the treatment of individuals and use of personal protection measures, community-wide vector control is feasible. In such situations, the committee believes that the third priority should be low-cost vector control measures designed to reduce the prevalence of infective mosquitoes in the environment, thus reducing the transmission of malaria to populations. These measures include source reduction (e.g., draining or filling in small bodies of water where mosquito larvae develop) or the application of low-cost larval control measures. In certain environments, the use of insecticide-impregnated bednets by all or most members of a community may also reduce malaria transmission, but this approach to community-based malaria control remains experimental.

The committee believes that the fourth priority for malaria control should be higher cost vector control measures such as large-scale source reduction or widespread spraying of residual insecticides. In certain epidemiologic situations, the use of insecticides for adult mosquito control is appropriate and represents the method of choice for decreasing malaria transmission and preventing epidemics (see Chapter 7 and Chapter 10 ).

The committee recommends that support of malaria control programs include resources to improve local capacities to conduct prompt diagnosis, including both training and equipment, and to ensure the availability of antimalarial drugs.

The committee recommends that resources be allocated to develop and disseminate malaria treatment guidelines for physicians, drug vendors, pharmacists, village health workers, and other health care personnel in endemic and non-endemic countries. The guidelines should be based, where appropriate, on the results of local operational research and should include information on the management of severe and complicated disease. The guidelines should be consistent and compatible among international agencies involved in the control of malaria.

The committee recommends that support for malaria control initiatives include funds to develop and implement locally relevant communication programs that provide information about how to prevent and treat malaria appropriately (including when and how to seek treatment) and that foster a dialogue about prevention and control.

Organization of Malaria Control

One of the major criticisms of malaria control programs during the past 10 to 15 years has been that funds have been spent inappropriately without an integrated plan and without formal evaluation of the efficacy of control measures instituted. In many instances, this has led to diminished efforts to control malaria.

The committee strongly encourages renewed commitment by donor agencies to support national control programs in malaria- endemic countries.

The committee recommends that U.S. donor agencies develop, with the advice of the national advisory body, a core of expertise (either in-house or through an external advisory group) to plan assistance to malaria control activities in endemic countries.

The committee believes that the development, implementation, and evaluation of such programs must follow a rigorous set of guidelines. These guidelines should include the following steps:

Identification of the problem

Determine the extent and variety of malaria. The paradigm approach described in Chapter 10 should facilitate this step.

Analyze current efforts to solve malaria problems.

Identify and characterize available in-country resources and capabilities.

Development of a plan

Design and prioritize interventions based on the epidemiologic situation and the available resources.

Design a training program for decision makers, managers, and technical staff to support and sustain the interventions.

Define specific indicators of the success or failure of the interventions at specific time points.

Develop a specific plan for reporting on the outcomes of interventions.

Develop a process for adjusting the program in response to successes and/or failures of interventions.

Review of the comprehensive plan by a donor agency review board

Modification of the plan based on comments of the review board

Implementation of the program

Yearly report and analysis of outcome variables

To guide the implementation of the activities outlined above, the committee has provided specific advice on several components, including an approach to evaluating malaria problems and designing control strategies (the paradigm approach), program management, monitoring and evaluation, and operational research.

Paradigm Approach

Given the complex and variable nature of malaria, the committee believes that the epidemiologic paradigms (see Chapter 10 ), developed in conjunction with this study, may form the basis of a logical and reasoned approach for defining the malaria problems and improving the design and management of malaria control programs.

The committee recommends that the paradigm approach be field tested to determine its use in helping policymakers and malaria program managers design and implement epidemiologically appropriate and cost-effective control initiatives.

The committee recognizes that various factors, including the local ecology, the dynamics of mosquito transmission of malaria parasites, genetically determined resistance to malaria infection, and patterns of drug use, affect patterns of malaria endemicity in human populations and need to be considered when malaria control strategies are developed. In most endemic countries, efforts to understand malaria transmission through field studies of vector populations are either nonexistent or so limited in scope that they have minimal impact on subsequent malaria control efforts. The committee recognizes that current approaches to malaria control are clearly inadequate. The committee believes, however, that malaria control strategies are sometimes applied inappropriately, with little regard to the underlying differences in the epidemiology of the disease.

The committee recommends that support for malaria control programs include funds to permit a reassessment and optimization of antimalarial tools based on relevant analyses of local epidemiologic, parasitologic, entomologic, socioeconomic, and behavioral determinants of malaria and the costs of malaria control.

Poor management has contributed to the failure of many malaria control programs. Among the reasons are a chronic shortage of trained managers who can think innovatively about health care delivery and who can plan, implement, supervise, and evaluate malaria control programs. Lack of incentives, the absence of career advancement options, and designation of responsibility without authority often hinder the effectiveness of the small cadre of professional managers that does exist. The committee recognizes that management technology is a valuable resource that has yet to be effectively introduced into the planning, implementation, and evaluation of most malaria control programs.

The committee recommends that funding agencies utilize management experts to develop a comprehensive series of recommendations and guidelines as to how basic management skills and technology can be introduced into the planning, implementation, and evaluation of malaria control programs.

The committee recommends that U.S. funding of each malaria control program include support for a senior manager who has responsibility for planning and coordinating malaria control activities. Where such an individual does not exist, a priority of the control effort should be to identify and support a qualified candidate. The manager should be supported actively by a multidisciplinary core group with expertise in epidemiology , entomology, the social sciences, clinical medicine, environmental issues, and vector control operations.

Monitoring and Evaluation

Monitoring and evaluation are essential components of any control program. For malaria control, it is not acceptable to continue pursuing a specific control strategy without clear evidence that it is effective and reaching established objectives.

The committee recommends that support for malaria control programs include funds to evaluate the impact of control efforts on the magnitude of the problem and that each program be modified as necessary on the basis of periodic assessments of its costs and effectiveness.

Problem Solving (Operational Research) and Evaluation

At the outset of any malaria prevention or control initiative and during the course of implementation, gaps in knowledge will be identified and problems will arise. These matters should be addressed through clearly defined, short-term, focused studies. Perhaps the most difficult aspects of operational research are to identify the relevant problem, formulate the appropriate question, and design a study to answer that question.

The committee recommends that a problem-solving (operational research) component be built into all existing and future U.S.-funded malaria control initiatives and that support be given to enhance the capacity to perform such research. This effort will include consistent support in the design of focused projects that can provide applicable results, analysis of data, and dissemination of conclusions.

The committee concludes that there is a need for additional scientists actively involved in malaria-related research in the United States and abroad. To meet this need, both short- and long-term training at the doctoral and postdoctoral levels must be provided. This training will be of little value unless there is adequate long-term research funding to support the career development of professionals in the field of malaria.

The committee recommends support for research training in malaria.

Whereas the curricula for advanced degree training in basic science research and epidemiology are fairly well defined, two areas require attention, especially in the developing world: social sciences and health management and training.

The committee recommends that support be given for the development of advanced-degree curricula in the social sciences, and in health management and training, for use in universities in developing and developed countries.

The availability of well-trained managers, decision makers, and technical staff is critical to the implementation of any malaria prevention and control program. The development of such key personnel requires a long term combination of formal training, focused short courses, and a gradual progression of expertise.

The committee recommends support for training in management, epidemiology , entomology, social sciences, and vector control. Such training for malaria control may be accomplished through U.S.-funded grant programs for long-term cooperative relationships between institutions in developed and developing countries; through the encouragement of both formal and informal linkages among malaria- endemic countries; through the use of existing training courses; and through the development of specific training courses.

The committee recommends further that malaria endemic countries be supported in the development of personnel programs that provide long-term career tracks for managers, decision makers, and technical staff, and that offer professional fulfillment, security, and competitive financial compensation.

• Cite this Page Institute of Medicine (US) Committee for the Study on Malaria Prevention and Control; Oaks SC Jr., Mitchell VS, Pearson GW, et al., editors. Malaria: Obstacles and Opportunities. Washington (DC): National Academies Press (US); 1991. 1, Conclusions and Recommendations.
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How climate change will affect malaria transmission

A new model for predicting the effects of climate change on malaria transmission in Africa could lead to more targeted interventions to control the disease according to a new study.

Previous methods have used rainfall totals to indicate the presence of surface water suitable for breeding mosquitoes, but the research led by the University of Leeds used several climatic and hydrological models to include real-world processes of evaporation, infiltration and flow through rivers.

This groundbreaking approach has created a more in-depth picture of malaria-friendly conditions on the African continent.

It has also highlighted the role of waterways such as the Zambezi River in the spread of the disease with almost four times the population estimated to live in areas suitable for malaria for up to nine months of the year than was previously thought.

The research entitled "Future malaria environmental suitability in Africa is sensitive to hydrology" was funded by the Natural Environment Research Council and is published today (9 May 2024) in the journal Science .

Dr Mark Smith an Associate Professor in Water Research in the Leeds' School of Geography and lead author of the study said: "This will give us a more physically realistic estimate of where in Africa is going to become better or worse for malaria.

"And as increasingly detailed estimates of water flows become available, we can use this understanding to direct prioritisation and tailoring of malaria interventions in a more targeted and informed way. This is really useful given the scarce health resources that are often available."

Malaria is a climate-sensitive vector-borne disease that caused 608,000 deaths among 249 million cases in 2022.

95% of global cases are reported in Africa but reductions in cases there have slowed or even reversed in recent years, attributed in part to a stall in investments in global responses to malaria control.

The researchers predict that the hot and dry conditions brought about by climate change will lead to an overall decrease in areas suitable for malaria transmission from 2025 onwards.

The new hydrology-driven approach also shows that changes in malaria suitability are seen in different places and are more sensitive to future greenhouse gas emissions than previously thought.

For example, projected reductions in malaria suitability across West Africa are more extensive than rainfall-based models suggested, stretching as far east as South Sudan, whereas projected increases in South Africa are now seen to follow watercourses such as the Orange River.

Co-author of the study Professor Chris Thomas from the University of Lincoln said: "The key advancement is that these models factor in that not all water stays where it rains, and this means breeding conditions suitable for malaria mosquitoes too can be more widespread -- especially along major river floodplains in the arid, savannah regions typical of many regions in Africa.

"What is surprising in the new modelling is the sensitivity of season length to climate change -- this can have dramatic effects on the amount of disease transmitted."

Simon Gosling, Professor of Climate Risks & Environmental Modelling at the University of Nottingham, co-authored the study and helped to coordinate the water modelling experiments used in the research. He said: "Our study highlights the complex way that surface water flows change the risk of malaria transmission across Africa, made possible thanks to a major research programme conducted by the global hydrological modelling community to compile and make available estimates of climate change impacts on water flows across the planet.

"Although an overall reduction in future risk of malaria might sound like good news, it comes at a cost of reduced water availability and a greater risk of another significant disease, dengue."

The researchers hope that further advances in their modelling will allow for even finer details of waterbody dynamics which could help to inform national malaria control strategies.

Dr Smith added: "We're getting to the point soon where we use globally available data to not only say where the possible habitats are, but also which species of mosquitoes are likely to breed where, and that would allow people to really target their interventions against these insects."

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• Pests and Parasites
• Environmental Issues
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• Global climate model
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• Infiltration (hydrology)
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Materials provided by University of Leeds . Note: Content may be edited for style and length.

Journal Reference :

• Mark W. Smith, Thomas Willis, Elizabeth Mroz, William H. M. James, Megan J. Klaar, Simon N. Gosling, Christopher J. Thomas. Future malaria environmental suitability in Africa is sensitive to hydrology . Science , 2024; 384 (6696): 697 DOI: 10.1126/science.adk8755

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Environmental Changes Are Fueling Human, Animal and Plant Diseases, Study Finds

Biodiversity loss, global warming, pollution and the spread of invasive species are making infectious diseases more dangerous to organisms around the world.

By Emily Anthes

Several large-scale, human-driven changes to the planet — including climate change, the loss of biodiversity and the spread of invasive species — are making infectious diseases more dangerous to people, animals and plants, according to a new study.

Scientists have documented these effects before in more targeted studies that have focused on specific diseases and ecosystems. For instance, they have found that a warming climate may be helping malaria expand in Africa and that a decline in wildlife diversity may be boosting Lyme disease cases in North America.

But the new research, a meta-analysis of nearly 1,000 previous studies, suggests that these patterns are relatively consistent around the globe and across the tree of life.

“It’s a big step forward in the science,” said Colin Carlson, a biologist at Georgetown University, who was not an author of the new analysis. “This paper is one of the strongest pieces of evidence that I think has been published that shows how important it is health systems start getting ready to exist in a world with climate change, with biodiversity loss.”

In what is likely to come as a more surprising finding, the researchers also found that urbanization decreased the risk of infectious disease.

The new analysis, which was published in Nature on Wednesday, focused on five “global change drivers” that are altering ecosystems across the planet: biodiversity change, climate change, chemical pollution, the introduction of nonnative species and habitat loss or change.

The researchers compiled data from scientific papers that examined how at least one of these factors affected various infectious-disease outcomes, such as severity or prevalence. The final data set included nearly 3,000 observations on disease risks for humans, animals and plants on every continent except for Antarctica.

The researchers found that, across the board, four of the five trends they studied — biodiversity change, the introduction of new species, climate change and chemical pollution — tended to increase disease risk.

“It means that we’re likely picking up general biological patterns,” said Jason Rohr, an infectious disease ecologist at the University of Notre Dame and senior author of the study. “It suggests that there are similar sorts of mechanisms and processes that are likely occurring in plants, animals and humans.”

The loss of biodiversity played an especially large role in driving up disease risk, the researchers found. Many scientists have posited that biodiversity can protect against disease through a phenomenon known as the dilution effect.

The theory holds that parasites and pathogens, which rely on having abundant hosts in order to survive, will evolve to favor species that are common, rather than those that are rare, Dr. Rohr said. And as biodiversity declines, rare species tend to disappear first. “That means that the species that remain are the competent ones, the ones that are really good at transmitting disease,” he said.

Lyme disease is one oft-cited example. White-footed mice, which are the primary reservoir for the disease, have become more dominant on the landscape, as other rarer mammals have disappeared, Dr. Rohr said. That shift may partly explain why Lyme disease rates have risen in the United States. (The extent to which the dilution effect contributes to Lyme disease risk has been the subject of debate, and other factors, including climate change, are likely to be at play as well.)

Other environmental changes could amplify disease risks in a wide variety of ways. For instance, introduced species can bring new pathogens with them, and chemical pollution can stress organisms’ immune systems. Climate change can alter animal movements and habitats, bringing new species into contact and allowing them to swap pathogens .

Notably, the fifth global environmental change that the researchers studied — habitat loss or change — appeared to reduce disease risk. At first glance, the findings might appear to be at odds with previous studies, which have shown that deforestation can increase the risk of diseases ranging from malaria to Ebola. But the overall trend toward reduced risk was driven by one specific type of habitat change: increasing urbanization.

The reason may be that urban areas often have better sanitation and public health infrastructure than rural ones — or simply because there are fewer plants and animals to serve as disease hosts in urban areas. The lack of plant and animal life is “not a good thing,” Dr. Carlson said. “And it also doesn’t mean that the animals that are in the cities are healthier.”

And the new study does not negate the idea that forest loss can fuel disease; instead, deforestation increases risk in some circumstances and reduces it in others, Dr. Rohr said.

Indeed, although this kind of meta-analysis is valuable for revealing broad patterns, it can obscure some of the nuances and exceptions that are important for managing specific diseases and ecosystems, Dr. Carlson noted.

Moreover, most of the studies included in the analysis examined just a single global change drive. But, in the real world, organisms are contending with many of these stressors simultaneously. “The next step is to better understand the connections among them,” Dr. Rohr said.

Emily Anthes is a science reporter, writing primarily about animal health and science. She also covered the coronavirus pandemic. More about Emily Anthes

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Research explains new method to engineer immune cells that could treat multiple cancer patients

by Linda Wang, University of California, Los Angeles

Immunotherapies have revolutionized cancer treatment by harnessing the body's own immune system to attack cancer cells and halt tumor growth. However, these therapies often need to be tailored to each individual patient, slowing down the treatment process and resulting in a hefty price tag that could soar well into the hundreds of thousands of dollars per patient.

To tackle these limitations, UCLA researchers have developed a new, clinically guided method to engineer more powerful immune cells called invariant natural killer T cells, or iNKT cells, that can be used for an "off-the-shelf" cancer immunotherapy in which immune cells from a single cord-blood donor can be used to treat multiple patients.

This novel technology , described in a study published in Nature Biotechnology , marks a major step toward enabling the mass production of cell therapies like CAR-T cell therapy, making these life-saving treatments more affordable and accessible to a broader range of patients.

The study's senior author, Lili Yang, a professor of microbiology, immunology and molecular genetics and a member of the Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research at UCLA and of the UCLA Health Jonsson Comprehensive Cancer Center, breaks down why this new system is poised to finally help a universal cell product advance to a clinical trial.

What are the key developments of this paper?

In 2021, our team reported a method for producing large numbers of iNKT cells using blood stem cells. That system required the use of three-dimensional thymic organoids and supportive cells, which posed both a manufacturing and regulatory challenge that prevented that method from ever reaching clinical application.

Now, we've developed a technology that can produce large quantities of iNKT cells from blood stem cells in a feeder-free and serum-free manner. This update to the method eliminates the previous hurdles, bringing us closer than ever to delivering an "off-the-shelf" cancer immunotherapy to patients.

How did you reach these findings?

Our team isolated the blood stem cells , which can self-replicate and produce all kinds of blood and immune cells, from 15 donor cord-blood samples representing diverse genetic backgrounds. We then genetically engineered each of those cells to develop into useful iNKT cells and estimate that one cord-blood donation can produce between 1,000 to 10,000 doses of a therapy—making the system really well suited to create an "off-the-shelf" immunotherapy.

Next, our team equipped the iNKT cells with chimeric antigen receptors, or CARs, molecules that enable immune cells to recognize and kill a specific type of cancer, to target seven cancers that included both blood cancers and solid tumors.

The CAR-iNKT cells showed a robust anti-tumor efficacy against all seven cancers, indicating their promising potential for treating a wide spectrum of cancers. Then in a multiple myeloma model, we demonstrated the CAR-iNKT cells' ability to halt tumor growth without causing complications that can sometimes occur when donor cells are transplanted into a patient.

Why are iNKT cells so special?

We consider invariant natural killer T cells to be the special forces of the immune cells because they're stronger and faster than conventional T cells and can attack tumors using multiple weapons. It's ideal to use iNKT cells as an "off-the-shelf" cancer immunotherapy because they don't carry the risk of graft-versus-host disease, a condition in which transplanted cells attack the recipient's body and the reason most cell-based immunotherapies have to be created on a patient-specific basis.

What excites you about these developments?

No "off-the-shelf" cell therapy has ever been approved by the U.S. Food and Drug Administration. With this new technology, not only have we shown a high output of iNKT cells, but we've also proven that the CAR-equipped iNKT cells don't lose their tumor-fighting efficacy after being frozen and thawed, which is a key requirement for the widespread distribution of a universal cell product.

While CAR-T cell therapies have been a transformative treatment for certain blood cancers like leukemia and lymphoma, it has been challenging to develop a cancer immunotherapy for solid tumors. This is in part because solid tumors have an immunosuppressive tumor microenvironment, meaning the immune cell function is impaired in the environment.

iNKT cells can change the tumor microenvironment by selectively and effectively depleting the most immunosuppressive cells in its surroundings—giving them the unique opportunity to attack solid tumors. We're extremely excited that this technology has a potential broad application to target a range of blood cancers, solid tumors and other conditions such as autoimmune diseases.

What's the biggest bottleneck in cancer immunotherapy?

The biggest bottleneck right now for immunotherapies, particularly cell therapies, is manufacturing. As of 2023, the FDA has approved six autologous CAR-T cell therapies with an average cost of around $300,000 per patient, per treatment. Using this novel technology to scale up iNKT cell production, there's a real possibility that the price per dose of immunotherapy can drop significantly to $5,000.

By definition, an "off-the-shelf" product would be readily on hand in clinical settings, so my hope is that this new system will result in a reality where all patients who need the treatment will be able to receive it immediately.

What are the next steps in the study?

Our team is advancing this multiple myeloma model project into an IND-enabling study this year, which would result in a Phase 1, first-in-human clinical trial of this technology.

Since this flexible platform allows us to switch the CARs to target different cancers, our team has since adapted this same system to target ovarian cancer, one of the deadliest gynecologic cancers. This represents a big leap from targeting blood cancers to solid tumors , but we're hopeful to bring this project to a clinical trial over the next couple of years.

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The Economics of Infertility: Evidence from Reproductive Medicine

WHO estimates that as many as 1 in 6 individuals of reproductive age worldwide are affected by infertility. This paper uses rich administrative population-wide data from Sweden to construct and characterize the universe of infertility treatments, and to then quantify the private costs of infertility, the willingness to pay for infertility treatments, as well as the role of insurance coverage in alleviating infertility. Persistent infertility causes a long-run deterioration of mental health and couple stability, with no long-run “protective” effects (of having no child) on earnings. Despite the high private non-pecuniary cost of infertility, we estimate a relatively low revealed private willingness to pay for infertility treatment. The rate of IVF initiations drops by half when treatment is not covered by health insurance. The response to insurance is substantially more pronounced at lower income levels. At the median of the disposable income distribution, our estimates imply a willingness to pay of at most 22% of annual income for initiating an IVF treatment (or about a 30% chance of having a child). At least 40% of the response to insurance coverage can be explained by a liquidity effect rather than traditional moral hazard, implying that insurance provides an important consumption smoothing benefit in this context. We show that insurance coverage of infertility treatments determines both the total number of additional children and their allocation across the socioeconomic spectrum.

We are grateful for helpful comments from seminar participants at the University of Michigan, Stanford University, University of Zurich, the Becker Friedman Health Economics Initiative Annual Conference, and the Whistler Junior Health Economics Summit. We thank Iliriana Shala at the Research Institute for Industrial Economics for excellent research assistance. We also gratefully acknowledge support from the National Science Foundation (CAREER SES-2144072, Persson), 2022 Stanford Discovery Innovation Fund (Polyakova), the National Institute on Aging (K01AG05984301, Polyakova), and the Sweden-America Foundation (Moshfegh). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Science Foundation or the National Institute on Aging. The views expressed herein are those of the authors and do not necessarily reflect the views of the National Bureau of Economic Research.

MARC RIS BibTeΧ

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