Insecticide resistance in phlebotomine sandflies in Southeast Asia with emphasis on the Indian subcontinent

Studies of insecticide resistance in India

Kala-azar has been endemic in the Indian continent since 1824 and has caused devastating epidemics. During the initial years of the anti-malaria campaign in India (1953–1958) the incidence of kala-azar also declined sharply apparently due to the collateral benefit of IRS with DDT [14]. In 1979, resistance in P. papatasi [3] was confirmed from Muzaffarpur district of Bihar. No mortality of P. papatasi was recorded when exposing the sandflies to 4 % DDT for one hour (LC50 ?4 % × 24 h) whereas P. argentipes was susceptible (LC50 0.48 % × 1 h). The LC50 value for dieldrin was 0.32 % × 1 h for P. papatasi and 0.16 % for P. argentipes. Thereafter, interest in studying the susceptibility of sandflies to insecticides, particularly to DDT, grew in areas endemic for kala-azar and reports began to arrive after 1979.

The geographical locations of studies undertaken on susceptibility of sandflies to DDT or other insecticides are given in Fig. 1. Susceptibility of P. argentipes to DDT was also studied in West Bengal in 1959 [15] when the sandflies were found to be fully susceptible (95–100 %). Kaul et al. [16] published preliminary findings on the susceptibility status of P. argentipes and P. papatasi collected from Bihar; P. argentipes was found to be susceptible and P. papatasi to be resistant with LC50 values from 0.5 to 0.6 × 1 h for P.argentipes but ?2 % × 1 h for P. papatasi. In 1979 detailed results were published by Joshi et al. [3] who confirmed the presence of resistance in P. papatasi. These two studies led to a realization of the problem of resistance in sandflies in India; thereafter many studies were undertaken in different parts of India following standard procedure [17], the findings of which are summarized in Table 1.

Dhanda et al. [18] tested susceptibility of P. papatasi in Muzaffarpur district, Bihar, India and found only 14.15 % mortality with 4 % DDT while 82.7–95 % with 5 % malathion papers with 1 hour exposure. As most of the control measures were directed towards P. argentipes, the vector of kala-azar, the findings did not influence any change to the strategy for kala-azar control. Dasgupta et al. [19] also corroborated high degree of resistance in P. papatasi (no mortality out of 170 sandflies tested) from Begusarai and Muzaffarpur districts in Bihar.

Using WHO test papers Dhiman and Mittal [20] evaluated resistance in F1 generation of P. papatasi collected from Midnapur districts in West Bengal and Ghaziabad district, Uttar Pradesh, India. P. papatasi showed a high degree of resistance to both 4 % DDT (16.7 % mortality in Ghaziabad and 75 % mortality in West Bengal) and 5 % malathion (58.6 % in West Bengal).

In Panchmahal district of Gujarat, India only 9.2 % mortality against 0.4 % dieldrin (with 2 h exposure) and 18 % mortality with 4 % DDT in P. papatasi was reported [21]. In Bikaner, Rajasthan (India) a high degree of resistance in P. papatasi to DDT, dieldrin and propoxur was reported while full susceptibility to malathion, fenitrothion and permethrin [22].

In a study in Pali and Barmer districts of Rajasthan, India, Singh et al. [23] reported that P. papatasi was resistant to 4 % DDT (79.5 % mortality) but susceptible to dieldrin, malathion, fenitrothion and propoxur. Since DDT had been extensively used in the area, the result indicated development of resistance due to insecticide pressure.

Mukhopadhyay et al. [24] observed resurgence of P. argentipes and P. papatasi sandflies in northern Bihar following indoor residual spraying with DDT and provided a clue to the possible development of resistance in sandflies. Later on, Mukhopadhyay et al. [4] for the first time reported development of tolerance in P.argentipes from Samastipur district in Bihar.

After the report of tolerance in P. argentipes to DDT, studies were undertaken on the impact of DDT house spraying on field populations of the vector species in Bihar, Uttar Pradesh and West Bengal in India and in Bangladesh and Nepal [25–27].

Joshi and Rai [28] studied the impact of DDT spraying on field populations of P. argentipes and P. papatasi in Varanasi district, India (1987–1988) and found that P. argentipes was susceptible to DDT and “in the absence of selection pressure even P. papatasi appears to be sensitive to DDT”.

In West Bengal, P. argentipes was found susceptible to DDT while P. papatasi was resistant in the field as well as under laboratory conditions [29]. Using 4 % DDT papers, 0–96 % mortality in P. papatasi was recorded in different areas.

In 1991, the National Malaria Eradication Programme of India reported 82–100 % mortality in P. argentipes collected from Sahibganj district (Jharkhand, formerly a part of Bihar state) against DDT test papers [30].

Basak and Tandon [31] and Chandra et al. [32] found resistance in P.argentipes from 24 Parganas (West Bengal), India while 100 % susceptibility from Hoogly district of West Bengal. Recently, in a study undertaken in two villages of Maldah district, West Bengal, India, Kumar et al. [33] found 40–61.5 % mortality of P. argentipes against 4 % DDT indicating development of resistance.

Amalraj et al. [34] reported tolerance in P. argentipes and P. papatasi from Pondicherry, southern India against DDT and malathion but resistance to permethrin. The study also suggested that bendiocarb, a carbamate compound, may be used against populations of P. argentipes resistant to organophosphates and pyrethroids.

In 2001, various levels of susceptibility of P. argentipes to DDT were reported by Singh et al. [35]: 71–78 % mortality in Vaishali district to 100 % mortality in Patna and Samastipur districts and borderline resistance in sandfly populations of Darbhanga and other parts of Vaishali district, where verification of the resistance levels was suggested.

Dhiman et al. [36] also reported resistance in P. argentipes from Vaishali district, Bihar to DDT while susceptibility to malathion and deltamethrin. Dinesh et al. [37] reported 43 % mortality with 4 % DDT in P. argentipes collected from three districts of Bihar. A recent study undertaken in 42 villages of six districts of Bihar in India [38] revealed that P. argentipes has developed resistance to DDT, susceptible to tolerance to malathion and full susceptibility to deltamethrin. Interestingly, this study showed even 100 % susceptibility of P. argentipes to DDT in a few villages in Patna and Muzaffarpur districts that are less endemic for VL and thus not exposed to insecticide pressure.

In other parts of India, Singh et al. [39] reported resistance to DDT (89.5 % mortality) in P. argentipes from Gadchiroli (Maharashtra), Ramgarh (Jharkhand), and Lalganj and Patna (Bihar, India) and full susceptibility to malathion and deltamethrin.

Rao et al [40] found P. argentipes to be highly susceptible (98–100 % mortality) to DDT in Nainital and Almora districts of Uttarakhand.