Nonrandom Selection and Multiple Blood Feeding of Human Hosts by Anopheles Vectors: Implications for Malaria Transmission in Papua New Guinea

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  • 1 Department of Microbiology and Molecular Genetics, and Department of Entomology, Michigan State University, East Lansing, Michigan;
  • | 2 Vector-borne Diseases Unit, Papua New Guinea Institute of Medical Research, Madang, Papua New Guinea;
  • | 3 Swiss Tropical and Public Health Institute, Basel, Switzerland;
  • | 4 University of Basel, Basel, Switzerland;
  • | 5 Burnet Institute, Melbourne, Victoria, Australia;
  • | 6 Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia;
  • | 7 Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia;
  • | 8 Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, Queensland, Australia;
  • | 9 School of Criminal Justice and Department of Integrative Biology, Michigan State University, Michigan

Nonrandom selection and multiple blood feeding of human hosts by Anopheles mosquitoes may exacerbate malaria transmission. Both patterns of blood feeding and their relationship to malaria epidemiology were investigated in Anopheles vectors in Papua New Guinea (PNG). Blood samples from humans and mosquito blood meals were collected in villages and human genetic profiles (“fingerprints”) were analyzed by genotyping 23 microsatellites and a sex-specific marker. Frequency of blood meals acquired from different humans, identified by unique genetic profiles, was fitted to Poisson and negative binomial distributions to test for nonrandom patterns of host selection. Blood meals with more than one genetic profiles were classified as mosquitoes that fed on multiple humans. The age of a person bitten by a mosquito was determined by matching the blood-meal genetic profile to the villagers’ genetic profiles. Malaria infection in humans was determined by PCR test of blood samples. The results show nonrandom distribution of blood feeding among humans, with biased selection toward males and individuals aged 15–30 years. Prevalence of Plasmodium falciparum infection was higher in this age group, suggesting males in this age range could be super-spreaders of malaria parasites. The proportion of mosquitoes that fed on multiple humans ranged from 6% to 13% among villages. The patterns of host utilization observed here can amplify transmission and contribute to the persistence of malaria in PNG despite efforts to suppress it with insecticidal bed nets. Excessive feeding on males aged 15–30 years underscores the importance of targeted interventions focusing on this demographic group.

Author Notes

Address correspondence to John B. Keven, Biomedical and Physical Sciences Building Room 6179, 567 Wilson Road, Michigan State University, East Lansing, MI 48824-1312. E-mail: kevenjoh@msu.edu

Financial support: This study was supported by NIH/Fogarty International Center training grants D43TW009639 and D43TW010075 and WHO/Tropical Disease Research Program grant WCCPRD4426109 2016/639607. SK was supported by an NHMRC Career Development Fellowship (GNT1141441). LJR was supported by an NHMRC Early Career Fellowship (GNT1016443) and is currently supported by NHMRC Career Development Fellowship (GNT1161627). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Authors’ addresses: John B. Keven, Department of Microbiology and Molecular Genetics, and Department of Entomology, Michigan State University, East Lansin, MI, and Vector-borne Diseases Unit, Papua New Guinea Institute of Medical Research, Madang, Papua New Guinea, E-mail: kevenjoh@msu.edu. Michelle Katusele, Rebecca Vinit, and Moses Laman, Vector-borne Diseases Unit, Papua New Guinea, Institute of Medical Research, Madang, Papua New Guinea, E-mails: katuselemn@gmail.com, rebeccavinit31@gmail.com, and drmlaman@yahoo.com. Daniela Rodríguez-Rodríguez and Manuel W. Hetzel, Swiss Tropical and Public Health Institute, Basel, Switzerland, and University of Basel, Basel, Switzerland, E-mails: daniela.rodriguez@swisstph.ch and manuel.hetzel@swisstph.ch. Leanne J. Robinson, Vector-borne Diseases Unit, Papua, New Guinea, Institute of Medical Research, Madang, Papua New Guinea, Burnet Institute, Melbourne, Victoria, Australia, Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia, and Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia, E-mail: leanne.robinson@burnet.edu.au. Stephan Karl, Vector-borne Diseases Unit, Papua New Guinea, Institute of Medical Research, Madang, Papua New Guinea, and Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, Australia, E-mail: stephanunkarl@googlemail.com. David R. Foran, School of Criminal Justice, and Department of Integrative Biology, Michigan State University, East Lansing, MI, E-mail: foran@msu.edu. Edward D. Walker, Department of Microbiology and Molecular Genetics, and Department of Entomology, Michigan State University, East Lansing, MI, E-mail: walker@msu.edu.

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