Tropical Medicine and International Health doi:10.1111/tmi.

13576

volume 00 no 00

Insecticide susceptibility of Phlebotomus argentipes sandflies,

vectors of visceral leishmaniasis in India
Diwakar S. Dinesh1 , Faizan Hassan1, Vijay Kumar1, Shreekant Kesari1, Roshan K. Topno1 and
Rajpal S. Yadav2
1 Division of Vector Biology and Control, ICMR-Rajendra Memorial Research Institute of Medical Sciences, Patna, India
2 Department of Control of Neglected Tropical Diseases, World Health Organization, Geneva, Switzerland

Abstract objectives Indoor residual spraying (IRS) with insecticides is the main vector control intervention
for the elimination of visceral leishmaniasis in India. After a change in IRS policy in 2015 due to
widespread resistance of Phlebotomus argentipes to DDT, IRS with DDT was replaced with alpha-
cypermethrin IRS in 2016. The objective of the present study was to evaluate the susceptibility of
P. argentipes to DDT and its alternatives, namely malathion and pirimiphos-methyl
(organophosphates); alpha-cypermethrin, deltamethrin, lambda-cyhalothrin and permethrin
(pyrethroids), and bendiocarb and propoxur (carbamates), in support of visceral leishmaniasis
elimination in India.
methods Phlebotomus argentipes sandflies were collected from the visceral-leishmaniasis endemic
states of Bihar, Jharkhand and West Bengal. In the WHO tube tests, the phenotypic susceptibility of
F1, 2-day old, non-blood fed females were determined against filter papers impregnated with DDT
4%, malathion 5%, pirimiphos-methyl 0.25%, alpha-cypermethrin 0.05%, deltamethrin 0.05%,
lambda-cyhalothrin 0.05%, permethrin 0.75%, bendiocarb 0.1% and propoxur 0.1%, which were
sourced from Universiti Sains Malaysia. The knockdown of sandflies after 1-h exposure and mortality
at 24 h after the 1-h exposure period were scored.
results Mean mortality of P. argentipes 24 h after exposure in tube tests was 22.6% for DDT and
≥ 98% for other insecticide-impregnated papers tested.
conclusion Phlebotomus argentipes continues to be highly resistant to DDT with no reversal of
resistance after DDT’s withdrawal from IRS. P. argentipes was fully susceptible to pyrethroid,
organophosphate and carbamate insecticides tested. Regular monitoring is warranted for insecticide
resistance management in sandfly vectors.

keywords carbamates, DDT, India, insecticide resistance, organophosphates, Phlebotomus

argentipes, pyrethroids, sandflies, visceral leishmaniasis

Sustainable Development Goals: Good Health and Well-Being; Sustainable Cities and Communities

dermal leishmaniasis (PKDL) cases were reported in India

Introduction
Visceral leishmaniasis (VL) is a neglected tropical disease
prevalent in more than one-third of the 200 countries or
territories reporting VL cases to WHO, including 45% of
countries in the South-east Asia region [1]. Visceral leish-
maniasis, also known as kala-azar, is endemic in South-
east Asia and is transmitted by the sandfly vector Phle-
botomus argentipes Annandale & Brunetti [2]. In India,
the four states of Bihar, Jharkhand, Uttar Pradesh and
West Bengal are endemic to VL, while some sporadic
cases are reported in other areas. Between 2015 and
2018, 4380–8500 new VL cases including post-kala-azar
[3]. In 2019, 633 administrative blocks in 54 districts
were endemically reporting a total of 4072 cases compris-
ing of 3128 VL cases, 817 VL-PKDL cases and 127 VL-
human immunodeficiency virus cases [4]. VL was tar-
geted to be eliminated in India by 2015 [5], but despite
substantial progress made is still prevalent in many dis-
tricts in the country. A new global road map for the elim-
ination of 20 NTDs, including VL, aims to eliminate VL
by 2030 [6].
Indoor residual spraying with insecticides has long
been the main vector control intervention against VL in
India. House spraying with dichloro-diphenyl-

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Tropical Medicine and International Health
D. S. Dinesh et al. Insecticide susceptibility of sandflies in India
trichloroethane (DDT), which was first introduced for
malaria eradication in 1958, was equally effective against
co-endemic VL by killing indoor resting sandflies. How-
ever, due to the emergence of resistance to DDT in
malaria vectors, IRS with DDT was discontinued in
1964, which led to the resurgence of VL in the late
1970s [7]. DDT was reintroduced by the National Kala-
azar Control Programme initiated in 1990–1991. Due to
widespread resistance of P. argentipes to DDT [8–10], in
2015 the Indian National Vector Borne Disease Control
Programme replaced DDT with alpha-cypermethrin for
indoor residual spraying on a pilot basis in seven districts
in the state of Bihar [8, 11]. In 2016, IRS with alpha-
cypermethrin was extended to cover all four VL-endemic
states in India.
The objectives of the present study were (a) to assess
any reversal of resistance of P. argentipes to DDT after
its complete withdrawal from IRS for VL control in
2016, (b) to determine the vector’s susceptibility to
alpha-cypermethrin and other pyrethroids after the first
introduction of alpha-cypermethrin for IRS for VL con-
trol in 2015, and (c) to assess its susceptibility to insec-
ticides in the organophosphate and carbamate classes.
These have never been applied for VL control in India
and could serve as future alternatives in case of resis-
tance of field populations of P. argentipes to pyre-
throids.
Methods
Study area and collection of sandflies
Females of sandflies were collected from six villages were
endemic to VL according to the criterion of having
reported >1 new VL case/10 000 population in the previ-
ous three years. The demographic details and the coordi-
nates of the villages are given in Table 1 and their
location is shown in Figure 1. One or two rounds of IRS
with alpha-cypermethrin (25 mg active ingredient/m2)
were applied consecutively in the three previous years in
five villages, except in Gulamehiyabagh village. The
household spray coverage was 89–100% in the sprayed
villages.
Test procedures
The phenotypic susceptibility of P. argentipes to insecti-
cides was evaluated in the laboratory by the WHO tube
test [12]. Female sandflies were collected in the morning
(06.00–08.00) from March to November 2018 using a
mechanical aspirator and a flashlight. Sandfly species were
identified by standard taxonomic key [13]. They were
2 © 2021 John Wiley & Sons Ltd
volume 00 no 00
then allowed to lay eggs in rearing pots held the insectary.
The replicates of emerging females (i.e. F1 generation)
aged 2 days, which were sugar-fed and starved for 2h
prior to testing, were used in the susceptibility tests.
The following quality-assured insecticide-impregnated
papers were sourced from the Vector Control Research
Unit, Universiti Sains Malaysia, Malaysia, which pro-
duces test papers and kits under WHO’s supervision:
• Organochlorine – DDT 4% and control papers treated
with Risella oil;
• Organophosphates – malathion 5% and pirimiphos-
methyl 0.25%, and control papers treated with olive
oil;
• Carbamates – bendiocarb 0.1% and propoxur 0.1%,
and control papers treated with olive oil;
• Pyrethroids – alpha-cypermethrin 0.05%, deltamethrin
0.05%, lambda-cyhalothrin, and permethrin 0.75%,
and control papers treated with silicone oil.
The susceptibility tests were performed with F1 gener-
ation females at 26
2°C and 70
10% relative
humidity. Each replicate consisted of 20
2 sandflies.
The knockdown of sandflies was scored one hour after
exposure with impregnated paper or control, after which
surviving sandflies were transferred to the holding tubes.
Cotton wool swabs soaked in 10% glucose solution
were put on the top side of the vertically held holding
tubes with live sandflies. The knocked down sandflies
were separately held in paper cups with sugar-soaked
cotton wool swabs to observe any revival during the
24-h holding period. Knockdown rates were recorded
after the 1-h exposure period and the delayed mortality
rates 24 h after the 1-h exposure period. Mortality was
recorded 24 h after the 1-h exposure period. Mortality
in treatments was corrected when mortality in the con-
trol was 5–20% using Abbott’s formula [14], that is,
corrected mortality = ([% mortality in test – % mortal-
ity in control] 9 100)/(100 – % mortality in control).
Experiments were discarded when mortality exceeded
20% in controls. Results were interpreted according to
WHO procedures for mosquito susceptibility tests: 98–
100% mortality indicates full susceptibility; mortality
<98% is suggestive of the presence of resistance and
requires confirmation, and mortality <90% confirms
resistance [12].
Ethics
The study was approved by the Scientific Advisory
Committee of the ICMR-Rajendra Memorial Research
Institute of Medical Sciences (RMRIMS), Patna (Project
ID: INT-130-VBC/2016).
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D. S. Dinesh et al. Insecticide susceptibility of sandflies in India

Table 1 Description of study villages in the states of Bihar, Jharkhand and West Bengal

No. of households
State District Block Village Geographical coordinates Population (no. of cattle sheds)

Bihar Saran Sonepor Rahar Diyar 250410 39.40″ N; 850080 56.12″ E 6167 788 (280)
Vaishali Lalganj Purkhauli 25°550 25.62″ N; 7268 1260 (1044)
85°110 24.30″ E
Nalanda Nalanda Dharampur 25°180 38.9″ N; 1126 204 (67)
85°190 25.8″ E
Patna Fatuha Gulmehiyabagha 250320 40.18″ N 2000 250 (250)
850160 16.59” E
Jharkhand Godda Sundar Pahadi Ghatiyari 240330 33.68” N; 406 128 (41)
860350 24.48″ E
West Bengal Malda Habibpur Tapsahar 250050 18.94″ N; 880210 46.38″ E 1126 225 (0)b
a
Unsprayed village.
b
Cattle sheds attached to the human dwellings under the same roof.

[16–19]. Similarly, IRS with alpha-cypermethrin in Mor-

Results
The results of the susceptibility tests are given in Table 2.
Because of similar results in susceptibility tests for a given
insecticide, the data for different villages were pooled for
analysis, but data are also presented for individual vil-
lages in Table S1.
Female P. argentipes were resistant to DDT with mean
24 h corrected mortality of 23% (range 12.7%–41%;
Table S1). The mean 1-h knockdown of P. argentipes
with different pyrethroids tested was within the range of
79.0–98.6%, while the mean 24-h mortality ranged from
98.6 to 100% in different villages, including the
unsprayed village of Gulamehiyabagh in Bihar.
For the two organophosphates, the mean knockdown
rate was 92% for malathion and 6.2% for pirimiphos-
methyl, and the mean mortality for each was 100%. For
carbamates, the mean knockdown rate was 98.4% for
bendiocarb and 99.2% for propoxur, while the mean-cor-
rected mortality rate was 100% for both.
Discussion
Previous studies had shown high level of resistance of
P. argentipes to DDT in South-east Asia [9]. The present
study in VL-endemic areas in India confirms that the
resistance of sandflies to DDT has not reversed 3–4 years
after stopping IRS with DDT. Although a 4-year-period
is possibly a short time to expect noticeable change in the
level of DDT resistance, a study in India had shown non-
reversal of DDT resistance in mosquitoes in Gujarat even
30 years after stopping IRS with DDT [15].
Field trials in Bangladesh, India and Nepal have shown
high entomological efficacy of IRS with pyrethroids,
alpha-cypermethrin or deltamethrin against P. argentipes
occo brought about a significant reduction in the density
of P. sergenti sandflies [20]. A large-scale study in 2015–
2016 in Bihar state, India using an integrated approach
involving VL case detection and treatment and two
annual rounds of IRS with alpha-cypermethrin showed a
significant decline in the incidence of VL [21]. In our
study villages, P. argentipes sandflies were fully suscepti-
ble to all pyrethroids tested, even in the unsprayed village
of Gulmehiyabagh. These findings corroborate high effi-
cacy of IRS with alpha-cypermethrin, a pyrethroid,
against sandfly vectors found in previous studies in
South-east Asia.
The development of resistance of sandfly vectors to
pyrethroids due to their continuing use in future may
pose a biological challenge in VL elimination efforts in
future. Detection of a non-synonymous mutation L1014F
in a voltage-gated sodium channel gene in the wild popu-
lation of P. argentipes in India that was found to be asso-
ciated with resistance to DDT and deltamethrin signals
pyrethroid tolerability and possible emergence of resis-
tance to pyrethroids [22]. Resistance has been detected in
the wild population of sandflies in areas where pyre-
throids have long been applied [23]. Therefore, system-
atic monitoring for pyrethroid resistance in sand fly
vectors is needed in VL elimination programmes.
The sandflies were fully susceptible to malathion and
pirimiphos-methyl in all alpha-cypermethrin sprayed vil-
lages, and also to bendiocarb and propoxur in the
unsprayed village of Gulamehiyabagh. These insecticides
had never been used in the VL-endemic areas in India for
vector control, although their use in agriculture pest con-
trol cannot be ruled out. P. argentipes collected from a
village in Bihar has been reported resistant to malathion
[24].

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D. S. Dinesh et al. Insecticide susceptibility of sandflies in India

Purkhauli
Rahar Diyar
BIHAR Gulmehiyabagh
Dharampur
Tapsahar

Ghatiyari

JHARKHAND

WEST BENGAL

Study village

Figure 1 Location of the study villages in the states of Bihar, Jharkhand and West Bengal in India.

A recent study in Bihar showed no significant reduction
in the density of P. argentipes even after two rounds of
spraying with alpha-cypermethrin with about 80% cover-
age [25]. Possible reasons for abundance of P. argentipes
post-spray in some areas are outdoor resting of P. argen-
tipes [26–27]; application of IRS rounds at inappropriate
times of the year leading to low impact on the sand fly
population; not spraying all cattle sheds, which sandflies
prefer to human dwellings as resting places; and selection
for resistance against alpha-cypermethrin in wild sandfly
populations in some areas. Currently, two rounds of
alpha-cypermethrin are recommended for control of VL
in endemic villages in India, which is confirmed by our
finding of high susceptibility of the vector to this insecti-
cide.
Considering that resistance of P. argentipes to alpha-
cypermethrin has been reported in other studies in VL-en-
demic villages in India and given the probability of future
resistance in areas that currently show full susceptibility,
IRS with alternative insecticides would be needed for
insecticide resistance management in order to maintain
the impact of vector control intervention in VL elimina-
tion in India. Two new insecticide formulations based on
clothianidin, a neonicotinoid insecticide, have been found

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D. S. Dinesh et al. Insecticide susceptibility of sandflies in India

Table 2 Susceptibility of P. argentipes to different insecticides in of vector control interventions. If resistance to the cur-
WHO tube test rently used insecticide, namely alpha-cypermethrin, devel-
ops in future, insecticides with alternative modes of
Corrected
No. of Knocked mortality 24-h action and new insecticides should be evaluated and reg-
Insecticide impregnated sandflies down post-exposure istered for use in IRS in India. Regular monitoring of
papers exposed at 1 h (%) (%) resistance in villages where VL incidence has fallen
below the public health threshold will be critical for
DDT 4% 163 6.1 23.0
containment preparedness in possible focal outbreaks.
Alpha-cypermethrin 220 98.6 100
0.05%
Deltamethrin 0.05% 100 79.0 100 Acknowledgements
Lambda-cyhalothrin 120 97.5 100
0.05% We thank Dr. V. P. Singh, Mr. R. Mandal, Mr. N.K.
Permethrin 0.75% 80 82.5 98.6 Sinha, Mr. S. A. Khan, Mr. B. B. Prasad, Mr. M. Kumar
Malathion 5% 163 92.0 100 and Mr. S. Kumar of the RMRIMS, Dr. H. K. Bhagat
Pirimiphos-methyl 182 6.2 100 and Mr. K. A. Ali of the vector-borne disease control
0.25% programmes of Bihar and West Bengal, respectively, for
Bendiocarb 0.1% 122 98.4 100
technical assistance during the study. Logistic support
Propoxur 0.1% 121 99.2 100
provided by the health officials of the states of Bihar,
West Bengal and Jharkhand is also acknowledged. This
highly efficacious in control of mosquito vectors [28–29] paper’s content is solely the responsibility of the authors
and maybe evaluated against sand fly vectors in India. and does not necessarily represent the official views of
There are no standardised WHO procedures for the their respective organisations.
determination of insecticide susceptibility specific to sand-
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Supporting Information
Additional Supporting Information may be found in the
online version of this article:
Table S1. Insecticide susceptibility in WHO tube test
of the F1 generation of females of P. argentipes collected
from different study villages.