Bionomics of Phlebotomus argentipes in villages in Bihar, India with insights into efficacy of IRS-based control measures

Abstract

Background

Visceral leishmaniasis (VL) is a deadly vector-borne disease. Approximately 90% of Indian VL cases occur in Bihar, where the sand fly, Phlebotomus argentipes, is the principal vector. Sand fly control in Bihar consists of indoor residual spraying (IRS), the practice of spraying the inner walls of village dwellings with insecticides. Prior researchers have evaluated success of IRS-control by estimating vector abundance in village houses, but the number of sampling periods ( n = 2–3) were minimal, and outdoor-resting P. argentipes were neglected. We describe a large-scale field study, performed in 24 villages within two Bihari districts, during which P. argentipes were collected biweekly over 47-weeks, in cattle enclosures, houses, and outdoors in peri-domestic vegetation. The objectives of this study were to provide updated P. argentipes ecological field data, and determine if program-initiated IRS-treatment had led to noticeable differences in vector abundance.

Principal findings

P. argentipes ( n = 126,901) relative abundance was greatest during the summer months (June-August) when minimum temperatures were highest. P. argentipes were most frequently collected from cattle enclosures (~46% total; ~56% blood fed). Many sand flies were found to have taken blood from multiple sources, with ~81% having blood fed on humans and ~60% blood feeding on bovines. Nonparametric statistical tests were determined most appropriate for evaluating IRS-treatment. Differences in P. argentipes abundance in houses, cattle enclosures and vegetation were detected between IRS-treated and untreated villages in only ~9% of evaluation periods occurring during the peak period of human-vector exposure (June-August) and in ~8% of the total observations. No significant differences were detected between the numbers of P. argentipes collected in vegetation close to the experimental villages.

Conclusion

The results of this study provide updated data regarding P. argentipes seasonal abundance, spatial distribution, and host preferances, and suggest vector abundance has not significantly declined in IRS-treated villages. We suggest that IRS be supplemented with vector control strategies targeting exophagic, exophilic P. argentipes, and that disease surveillance be accompanied by rigorous vector population monitoring.

Author summary

Visceral leishmaniasis is a disease caused by a deadly vector-borne parasite ( Leishmania donovani) transmitted to man by phlebotomine sand flies. Indoor residual spraying (IRS), performed within village dwellings, is the primary means of sand fly control performed in Bihar, India and more explicit methods of evaluating the success of control are warranted. A field-based study was conducted to collect ecological sand fly data for use in evaluating the effectiveness of IRS in reducing relative sand fly abundance. Results indicate that sand flies blood feed primarily on humans and cattle and are most frequently found within cattle enclosures. Results further suggest IRS-treatment has a limited impact on vector density. Our approach incorporates detailed evaluation of sand fly spatial distribution (cattle enclosures, houses, vegetation), seasonal fluctuations in abundance, host blood meal preferences within Bihari villages, and dates of IRS performed within treated villages. Hence, this study provides an explicit means of monitoring vector populations and evaluating control measures in Bihar.