Entomological Monitoring and Evaluation: Diverse Transmission Settings of ICEMR Projects Will Require Local and Regional Malaria Elimination Strategies
Am. J. Trop. Med. Hyg., 93(Suppl 3), 2015, pp. 28–41
doi:10.4269/ajtmh.15-0009
Copyright © 2015 by The American Society of Tropical Medicine and Hygiene
Entomological Monitoring and Evaluation: Diverse Transmission Settings of ICEMR Projects
Will Require Local and Regional Malaria Elimination Strategies
Jan E. Conn,* Douglas E. Norris, Martin J. Donnelly, Nigel W. Beebe, Thomas R. Burkot, Mamadou B. Coulibaly,
Laura Chery, Alex Eapen, John B. Keven, Maxwell Kilama, Ashwani Kumar, Steve W. Lindsay, Marta Moreno,
Martha Quinones, Lisa J. Reimer, Tanya L. Russell, David L. Smith, Matthew B. Thomas,
Edward D. Walker, Mark L. Wilson, and Guiyun Yan
The Wadsworth Center, New York State Department of Health, Albany, New York; Department of Biomedical Sciences, School of Public Health,
State University of New York, Albany, New York; The W. Harry Feinstone Department of Molecular Microbiology and Immunology,
The Johns Hopkins Malaria Research Institute, Johns Hopkins University Bloomberg School of Public Health, Baltimore, Maryland;
Department of Vector Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom; Malaria Programme,
Wellcome Trust Sanger Institute, Hinxton, Cambridge, United Kingdom; The University of Queensland, Brisbane, Australia;
Commonwealth Scientific and Industrial Research Organisation (CSIRO), Brisbane, Australia; James Cook University, Cairns, Australia;
Malaria Research and Training Centre, Faculty of Medicine Pharmacy and Dentistry, University of Sciences, Techniques and
Technologies of Bamako, Bamako, Mali; Department of Chemistry, University of Washington, Seattle, Washington; National Institute of Malaria
Research, National Institute of Epidemiology Campus Chennai, Tamil Nadu, India; Papua New Guinea Institute of Medical Research,
Madang, Papua New Guinea; Infectious Diseases Research Collaboration, Kampala, Uganda; National Institute of Malaria Research,
Field Unit Goa, Goa, India; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom;
Division of Infectious Diseases, University of California, San Diego School of Medicine, La Jolla, California; George Palade Labs,
University of California, San Diego School of Medicine, La Jolla, California; Public Health Department, Faculty of Medicine,
National University of Colombia, Bogotá, Colombia; Papua New Guinea Institute of Medical Research, Goroka and Madang,
Papua New Guinea; Pacific Malaria Initiative Support Centre, School of Population Health, University of Queensland, Herston, Australia;
Australian Centre for Tropical and International Health, University of Queensland, Herston, Australia; Queensland Tropical Health Alliance,
Faculty of Medicine, Health and Molecular Sciences, James Cook University, Cairns, Australia; Department of Entomology,
Pennsylvania State University, University Park, Pennsylvania; Center for Infectious Disease Dynamics, Pennsylvania State University,
University Park, Pennsylvania; Spatial Ecology and Epidemiology Group, Department of Zoology, Oxford University, Oxford,
United Kingdom; Fogarty International Center, National Institutes of Health (NIH), Bethesda, Maryland; Sanaria Institute
for Global Health and Tropical Medicine, Rockville, Maryland; Department of Entomology, Michigan State University,
East Lansing, Michigan; Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, Michigan;
Program in Public Health, College of Health Sciences, University of California at Irvine, Irvine, California
Abstract. The unprecedented global efforts for malaria elimination in the past decade have resulted in altered vectorial
systems, vector behaviors, and bionomics. These changes combined with increasingly evident heterogeneities in malaria
transmission require innovative vector control strategies in addition to the established practices of long-lasting insecticidal
nets and indoor residual spraying. Integrated vector management will require focal and tailored vector control to achieve
malaria elimination. This switch of emphasis from universal coverage to universal coverage plus additional interventions
will be reliant on improved entomological monitoring and evaluation. In 2010, the National Institutes for Allergies and
Infectious Diseases (NIAID) established a network of malaria research centers termed ICEMRs (International Centers
for Excellence in Malaria Research) expressly to develop this evidence base in diverse malaria endemic settings. In this
article, we contrast the differing ecology and transmission settings across the ICEMR study locations. In South America,
Africa, and Asia, vector biologists are already dealing with many of the issues of pushing to elimination such as highly
focal transmission, proportionate increase in the importance of outdoor and crepuscular biting, vector species complexity,
and “sub patent” vector transmission.
INTRODUCTION
larly where vectors are primarily endophagic (indoor biting),
endophilic (indoor resting), and anthropophilic.6
As such, the goal of global malaria elimination will require
additional interventions and improvements in both the application of current control measures and entomological monitoring.7 The single biggest threat to sustainable malaria control is
insecticide resistance, which has reached alarmingly high levels
in some vector populations of Africa, India, and China (M. L.
Quiñones and others, unpublished data).2 Second, there are
indications of local adaptation in vector biting behavior, possibly in response to reliance on LLINs and IRS.3,5,8,9 Whether
this reflects a lack of vector ingress because of physical barriers, that is, mosquito-proof houses, adaptation of endophagic
vectors to exophagy (outdoor feeding), or selection on phenotypic plasticity, is unknown.10,11 It has been hypothesized that
in some areas endophagic populations may have been eliminated, leaving the inadequately controlled exophagic population.12 Also, in the Solomon Islands during the 1970s malaria
eradication campaign, late night biting of Anopheles koliensis
and Anopheles punctulatus, which had been common, virtually
The unprecedented global efforts for malaria elimination in
the past decade have resulted in the reduction of malaria cases
in several settings,1 but also in dramatic increases in resistance
to pyrethroids and other insecticides,2 changes in the relative
importance of outdoor (residual) malaria transmission, and
major shifts in biting time, for example, Anopheles farauti in
the Solomon Islands3 and Anopheles funestus in Benin and
Senegal.4,5 Together these new trends have already resulted in
quantifiable changes in human–vector interactions in several
endemic areas, and threaten to jeopardize future gains. Longlasting insecticidal nets (LLINs) and indoor residual spraying
(IRS) and have been the mainstays of malaria control and
have had a major impact on reducing global malaria, particu-
*Address correspondence to Jan E. Conn, Griffin Laboratory, T (...truncated)