A systematic review of mathematical models of mosquito-borne pathogen transmission: 1970–2010

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Abstract

Mathematical models of mosquito-borne pathogen transmission originated in the early twentieth century to provide insights into how to most effectively combat malaria. The foundations of the Ross–Macdonald theory were established by 1970. Since then, there has been a growing interest in reducing the public health burden of mosquito-borne pathogens and an expanding use of models to guide their control. To assess how theory has changed to confront evolving public health challenges, we compiled a bibliography of 325 publications from 1970 through 2010 that included at least one mathematical model of mosquito-borne pathogen transmission and then used a 79-part questionnaire to classify each of 388 associated models according to its biological assumptions. As a composite measure to interpret the multidimensional results of our survey, we assigned a numerical value to each model that measured its similarity to 15 core assumptions of the Ross–Macdonald model. Although the analysis illustrated a growing acknowledgement of geographical, ecological and epidemiological complexities in modelling transmission, most models during the past 40 years closely resemble the Ross–Macdonald model. Modern theory would benefit from an expansion around the concepts of heterogeneous mosquito biting, poorly mixed mosquito-host encounters, spatial heterogeneity and temporal variation in the transmission process.

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Most cited references 55

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Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti.

Louis Lambrechts, Krijn Paaijmans, Thanyalak Fansiri … (2011)

Most studies on the ability of insect populations to transmit pathogens consider only constant temperatures and do not account for realistic daily temperature fluctuations that can impact vector-pathogen interactions. Here, we show that diurnal temperature range (DTR) affects two important parameters underlying dengue virus (DENV) transmission by Aedes aegypti. In two independent experiments using different DENV serotypes, mosquitoes were less susceptible to virus infection and died faster under larger DTR around the same mean temperature. Large DTR (20 °C) decreased the probability of midgut infection, but not duration of the virus extrinsic incubation period (EIP), compared with moderate DTR (10 °C) or constant temperature. A thermodynamic model predicted that at mean temperatures 18 °C, larger DTR reduces DENV transmission. The negative impact of DTR on Ae. aegypti survival indicates that large temperature fluctuations will reduce the probability of vector survival through EIP and expectation of infectious life. Seasonal variation in the amplitude of daily temperature fluctuations helps to explain seasonal forcing of DENV transmission at locations where average temperature does not vary seasonally and mosquito abundance is not associated with dengue incidence. Mosquitoes lived longer and were more likely to become infected under moderate temperature fluctuations, which is typical of the high DENV transmission season than under large temperature fluctuations, which is typical of the low DENV transmission season. Our findings reveal the importance of considering short-term temperature variations when studying DENV transmission dynamics.

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Heterogeneities in the transmission of infectious agents: implications for the design of control programs.

M. E. Woolhouse, C. Dye, J F Etard … (1997)

From an analysis of the distributions of measures of transmission rates among hosts, we identify an empirical relationship suggesting that, typically, 20% of the host population contributes at least 80% of the net transmission potential, as measured by the basic reproduction number, R0. This is an example of a statistical pattern known as the 20/80 rule. The rule applies to a variety of disease systems, including vector-borne parasites and sexually transmitted pathogens. The rule implies that control programs targeted at the "core" 20% group are potentially highly effective and, conversely, that programs that fail to reach all of this group will be much less effective than expected in reducing levels of infection in the population as a whole.

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Lymphatic filariasis and onchocerciasis.

Mark Taylor, Achim Hoerauf, Moses J. Bockarie (2010)

Lymphatic filariasis and onchocerciasis are parasitic helminth diseases that constitute a serious public health issue in tropical regions. The filarial nematodes that cause these diseases are transmitted by blood-feeding insects and produce chronic and long-term infection through suppression of host immunity. Disease pathogenesis is linked to host inflammation invoked by the death of the parasite, causing hydrocoele, lymphoedema, and elephantiasis in lymphatic filariasis, and skin disease and blindness in onchocerciasis. Most filarial species that infect people co-exist in mutualistic symbiosis with Wolbachia bacteria, which are essential for growth, development, and survival of their nematode hosts. These endosymbionts contribute to inflammatory disease pathogenesis and are a target for doxycycline therapy, which delivers macrofilaricidal activity, improves pathological outcomes, and is effective as monotherapy. Drugs to treat filariasis include diethylcarbamazine, ivermectin, and albendazole, which are used mostly in combination to reduce microfilariae in blood (lymphatic filariasis) and skin (onchocerciasis). Global programmes for control and elimination have been developed to provide sustained delivery of drugs to affected communities to interrupt transmission of disease and ultimately eliminate this burden on public health. Copyright © 2010 Elsevier Ltd. All rights reserved.

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Author and article information

Journal

Journal ID (nlm-ta): J R Soc Interface

Journal ID (iso-abbrev): J R Soc Interface

Journal ID (publisher-id): RSIF

Journal ID (hwp): royinterface

Title: Journal of the Royal Society Interface

Publisher: The Royal Society

ISSN (Print): 1742-5689

ISSN (Electronic): 1742-5662

Publication date (Print): 6 April 2013

Publication date PMC-release: 6 April 2013

Volume: 10

Issue: 81

Electronic Location Identifier: 20120921

Affiliations

[1 ]Fogarty International Center, National Institutes of Health , Bethesda, MD, USA

[2 ]Department of Entomology, School of Veterinary Medicine, University of California , Davis, CA, USA

[3 ]Center for Vectorborne Diseases, School of Veterinary Medicine, University of California , Davis, CA, USA

[4 ]Department of Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California , Davis, CA, USA

[5 ]Division of Integrated Biodefense, Georgetown University Medical Center , Washington DC, USA

[6 ]Department of Microbiology and Immunology, Georgetown University Medical Center , Washington DC, USA

[7 ]Graduate School of Environmental Sciences and Global Center of Excellence Program on Integrated Field Environmental Science, Hokkaido University , Sapporo, Japan

[8 ]Programa de Investigación en Enfermedades Tropicales, Escuela de Medicina Veterinaria, Universidad Nacional , Heredia, Costa Rica

[9 ]Institute of Tropical Medicine (NEKKEN) and Global Center of Excellence Program on Tropical and Emergent Infectious Diseases, Nagasaki University , Nagasaki, Japan

[10 ]The Rubenstein School of Environment and Natural Resources, University of Vermont, Burlington, VT, USA

[11 ]Department of Defense , Fort Detrick, MD, USA

[12 ]Center for Disease Dynamics, Economics and Policy , Washington, DC, USA

[13 ]Emerging Pathogens Institute, University of Florida , Gainesville, FL, USA

[14 ]Department of Biology, University of Florida , Gainesville, FL, USA

[15 ]Department of Geography, University of Florida , Gainesville, FL, USA

[16 ]Department of Environmental Studies, Emory University , Atlanta, GA, USA

[17 ]Center for Communicable Disease Dynamics, Department of Epidemiology, Harvard School of Public Health , Boston, MA, USA

[18 ]Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health , Baltimore, MD, USA

[19 ]Malaria Research Institute, Johns Hopkins Bloomberg School of Public Health , Baltimore, MD, USA

[20 ]Malaria Drug Resistance and Chemotherapy Laboratory, Queensland Institute of Medical Research , Herston, Queensland, Australia

[21 ]Spatial Ecology and Epidemiology Group, Department of Zoology, Oxford University , Oxford, UK

[22 ]School of International and Public Affairs, Columbia University , New York, NY, USA

[23 ]Department of Microbiology and Immunology, Columbia University College of Physicians and Surgeons , New York, NY, USA

[24 ]Department of Ecology and Evolutionary Biology, Princeton University , Princeton, NJ, USA

[25 ]Center for Advanced Modeling, Department of Emergency Medicine, Johns Hopkins University , Baltimore, MD, USA

[26 ]Department of Biological Sciences, Eck Institute for Global Health, University of Notre Dame , Notre Dame, IN, USA

[27 ]Department of Infectious Disease Epidemiology, Imperial College , London, UK

[28 ]Department of Disease Control, London School of Hygiene and Tropical Medicine , London, UK

[29 ]School of Biological and Biomedical Sciences, Durham University , Durham, UK

[30 ]Department of Mathematics and Biomathematics Graduate Program, North Carolina State University , Raleigh, NC, USA

[31 ]Department of Geography and Environment, University of Southampton, Highfield, Southampton, UK

Author notes

e-mail: rcreiner@ 123456ucdavis.edu

e-mail: taperkins@ 123456ucdavis.edu

[†]

These authors contributed equally to this study.

Article

Publisher ID: rsif20120921

DOI: 10.1098/rsif.2012.0921

PMC ID: 3627099

PubMed ID: 23407571

SO-VID: bceed034-c41f-4f02-b9af-5fae6cb1371c

License:

© 2013 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the original author and source are credited.

History

Date received : 9 November 2012

Date accepted : 22 January 2013

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cover-date April 6, 2013

ScienceOpen disciplines: Life sciences

Keywords: infectious disease dynamics,vector-borne disease,epidemiology,dengue,west nile,filariasis

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ScienceOpen disciplines: Life sciences

Keywords: infectious disease dynamics, vector-borne disease, epidemiology, dengue, west nile, filariasis

A systematic review of mathematical models of mosquito-borne pathogen transmission: 1970–2010

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Abstract

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Vector Biology

Most cited references 55

Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti.

Heterogeneities in the transmission of infectious agents: implications for the design of control programs.

Lymphatic filariasis and onchocerciasis.

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