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.
Highlights
IntroductionIn Papua New Guinea (PNG) where malaria is endemic,[1] long-lasting impregnated bed nets (LLINs) that target the mosquito vectors are the primary malaria intervention method, supplemented with an increased supply of rapid immunologic diagnostic test kits and antimalarial drugs at local health centers.[2,3,4] Immediately after nationwide implementation of the LLIN-based malaria control program in 2005, a considerable decline in the rates of malaria transmission and infection was observed nationally.[5,6,7,8] in recent years (2016–2017) infection rates have either persisted (plateaued) or rebounded despite high LLIN coverage.[9,10] Physiological or genetic resistance to the pyrethroid insecticides in the LLIN has not been detected in the Anopheles vector populations in PNG.[11,12,13] decreased bioefficacy of the LLINs distributed between 2013 and 2019 against pyrethroid-susceptible vectors in natural populations in PNG has been observed and is believed to be a factor causing persistent malaria transmission in PNG.[14]
The current study was the first to apply this method of investigation to Anopheles vectors of malaria in Papua New Guinea (PNG)
This study differed from the previous ones in the number of microsatellite loci used to construct a genetic profile
Summary
In Papua New Guinea (PNG) where malaria is endemic,[1] long-lasting impregnated bed nets (LLINs) that target the mosquito vectors are the primary malaria intervention method, supplemented with an increased supply of rapid immunologic diagnostic test kits and antimalarial drugs at local health centers.[2,3,4] Immediately after nationwide implementation of the LLIN-based malaria control program in 2005, a considerable decline in the rates of malaria transmission and infection was observed nationally.[5,6,7,8] in recent years (2016–2017) infection rates have either persisted (plateaued) or rebounded despite high LLIN coverage.[9,10] Physiological or genetic resistance to the pyrethroid insecticides in the LLIN has not been detected in the Anopheles vector populations in PNG.[11,12,13] decreased bioefficacy of the LLINs distributed between 2013 and 2019 against pyrethroid-susceptible vectors in natural populations in PNG has been observed and is believed to be a factor causing persistent malaria transmission in PNG.[14]. The phenomenon of persistent transmission in the presence of high LLIN coverage in PNG might be caused by mosquito behaviors such as outdoor and early evening human-biting and opportunistic host selection, which enable mosquitoes to evade the indoordeployed LLINs.[15,16,17] In addition, multiple and nonrandom
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