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

Author:

Keven John B.12,Katusele Michelle2,Vinit Rebecca2,Rodríguez-Rodríguez Daniela34,Hetzel Manuel W.34,Robinson Leanne J.2567,Laman Moses2,Karl Stephan28,Foran David R.9,Walker Edward D.1

Affiliation:

1. 1Department of Microbiology and Molecular Genetics, and Department of Entomology, Michigan State University, East Lansing, Michigan;

2. 2Vector-borne Diseases Unit, Papua New Guinea Institute of Medical Research, Madang, Papua New Guinea;

3. 3Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland;

4. 4Department of Epidemiology and Public Health, University of Basel, Basel, Switzerland;

5. 5Vector-Borne Diseases and Tropical Public Health Group, Burnet Institute, Melbourne, Victoria, Australia;

6. 6Division of Population Health and Immunity, Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia;

7. 7Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia;

8. 8Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, Queensland, Australia;

9. 9School of Criminal Justice and Department of Integrative Biology, Michigan State University, Michigan

Abstract

ABSTRACT. 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.

Publisher

American Society of Tropical Medicine and Hygiene

Subject

Virology,Infectious Diseases,Parasitology

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