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Year : 2022  |  Volume : 59  |  Issue : 3  |  Page : 253-258

A note on the insecticide susceptibility status of secondary malaria vector An. annularis in Jharkhand state of India

1 ICMR-National Institute of Malaria Research, Field Unit, Ranchi, Jharkhand, India
2 Indian Council of Medical Research, Ramligaswami Bhawan, New Delhi, India
3 ICMR-National Institute of Malaria Research, New Delhi, India

Date of Submission23-Aug-2021
Date of Acceptance18-Apr-2022
Date of Web Publication08-Dec-2022

Correspondence Address:
M K Das
ICMR-National Institute of Malaria Research, Field Unit, Ranchi, Jharkhand
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0972-9062.345179

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Background & objectives: An. annularis van der Wulp (1884) is the secondary malaria vector of importance in India. In Jharkhand state it is present in almost all the districts abundantly and transmits malaria. The development of resistance to Dichlorodipheny ltrichloroethane (DDT) in An. annularis was reported from various parts of India. The main objective of this study was to generate information on insecticide susceptibility status of An. annularis to DDT, malathion, deltamethrin and permethrin in different districts of Jharkhand state.
Methods; Adult An. annularis female mosquitoes were collected form villages of six tribal districts Simdega (Kurdeg and Simdega CHC), Khunti (Murhu and Khunti CHCs), Gumla (Bharno and Gumla CHCs), West Singhbhum (Chaibasa and Bada Jamda CHCs), Godda (Poraiyahat and Sunderpahari (CHCs) and Sahibganj (Borio and Rajmahal CHCs). Insecticide susceptibility status was determined by using WHO tube test method against prescribed discriminatory dosages of insecticides, DDT - 4.0%, malathion - 5.0%, deltamethrin - 0.05% and permethrin - 0.75%.
Results: An. annularis was reported resistant to DDT in six districts, possible resistant to malathion in districts Gumla, Khuntiand Sahibganj and susceptible to deltamehrin (98% to100% mortality) and permethrin (100% mortality).
Interpretation & conclusion: An. annularis, the secondary vector species is associated with the transmission of malaria reported resistant to DDT and susceptible to pyrerthroids deltamethrin and permethrin. In view of large-scale distribution of long-lasting insecticidal nets (LLINs) in all the districts, the response to synthetic pyrethroid needs to be periodically monitored to assess the effectiveness.

Keywords: Malaria; An. annularis; resistance; susceptibility; vector control

How to cite this article:
Das M K, Rahi M, Kumar G, Raghavendra K. A note on the insecticide susceptibility status of secondary malaria vector An. annularis in Jharkhand state of India. J Vector Borne Dis 2022;59:253-8

How to cite this URL:
Das M K, Rahi M, Kumar G, Raghavendra K. A note on the insecticide susceptibility status of secondary malaria vector An. annularis in Jharkhand state of India. J Vector Borne Dis [serial online] 2022 [cited 2023 Feb 2];59:253-8. Available from: http://www.jvbd.org//text.asp?2022/59/3/253/345179

  Introduction Top

In India, about 0.34 million malaria cases were reported in 2018 of which approximately 7% originated from Jharkhand state. Jharkhand is situated in the eastern part of India and is surrounded by Chhattisgarh in West, Bihar in North, West Bengal in the East and Odisha in the South. The forest, hilly terrain, favorable climate, difficult to reach areas, migration and social unrest are the main contributing factors to the malaria burden in Jharkhand. An estimated 54 million tribals belonging to about 40 ethnic communities (constituting around 28% of the total population of Jharkhand) reside in the forest areas. This tribal population accounts for 8% of the total population of India but contributes to 30% of all malaria cases. Introduction of new tools, bivalent rapid diagnostic test (RDT) kits for diagnosis, artemisinin-based combination therapy (ACT) for the treatment of P. falciparum malaria, and long-lasting insecticidal nets (LLINs) with continued indoor residual spraying (IRS) has reduced the annual parasite incidence (API) of Jharkhand state from 6.20 in 2010 to 2.49 in 2018. Despite these improvements malaria remains a major public health challenge causing morbidity and mortality in this region. The state has relatively stable malaria transmission with yearly average slide positivity rate (determined from both passive and active surveillance) of 15% over the last three years. P. falciparum accounts for 44% of the cases while P vivax accounts for 56%.

Indoor residual spraying of insecticides and universal coverage of population with pyrethroid-LLINs are the two main vector control strategies in Jharkhand state. While most of districts in the state are under IRS with DDT (organochlorine) since the inception of the vector control program in early 1950s. DDT and synthetic pyrethroids have been used for IRS in the malaria control program in the state. In 2016 α-cypermethrin was sprayed for kala-azar control in districts Dumka, Godda, Sahibganj and Pakur. In other 20 districts, DDT was used. The development of DDT resistance and continuous reduction of susceptibility to pyrethroids in malaria vectors poses a serious threat to the Vector Borne Disease Control Program.

Five classes of insecticides, which share three modes of action are approved by the World Health Organization (WHO) for use in mosquito control programmes[1]. The development of insecticide resistance among Anopheles vectors in malaria control warrants the need for regular monitoring of insecticide susceptibility/resistance, primarily in the districts where malaria is endemic and remains a continuous burden mainly in forested tribal areas.

In India malaria is transmitted by ten vector species. Six are considered vectors of primary importance, viz., An. baimai, An. culicifacies, An. fluviatilis, An. minimus, An. stephensi, and An. sundaicus for transmitting malaria in different eco-geographical regions of the country and other four species An. annularis, An. nivipes, An. philippnensis and An. varunaare are secondary vectors for transmitting malaria in limited geographic areas[2]. In Jharkhand state, An. culicifacies and An. annularis are the most dominant primary and secondary malaria vector species though An. annularis is not yet considered as an important vector and its role cannot be discounted in the transmission of malaria[3]. Two other efficient primary malaria vectors with limited distribution, An. fluviatilis and An. minimus are prevalent in the hilly forested region of the state.

An. annularis Van Der Wulp (1984) belongs to subgenus cellia, annularis group of Neocellia series. The species is considered to be an important vector in certain parts of India[4]. An. annularis was incriminated in Ferozepur, Punjab[5]. The role of An. annularis in malaria transmission as a local vector in different parts of India was well established i.e., in the coastal areas of Odisha, Bihar, West Bengal, Andhra Pradesh, Uttar Pradesh and Punjab[6],[7],[8],[9],[10]. The role of An. annularis as malaria vector was also established by gut or gland positive mosquitoes from different parts of India[11],[12],[13],[14]. In Birbhum district of Bengal, 49,698 An. annularis were dissected of which 8 had sporozoites (~0.02%) in the salivary glands[15]. In Odisha, 1048 An. annularis mosquitoes were dissected with 3 gut infections[16]. In Assam 11 natural infections reported (7 gland and 4 guts) out of 20.043 dissections[17]. In 1942, 20,844 mosquitoes were dissected in Chilka lake area of Odisha and found 1 gut infection[18]. In 1943 sporozoite rate of 0.08% was recorded (7 gland infections) out of 9183 dissections in coastal plains of Odisha and established An. annularis as a principal vector of malaria in this area[6].

An. annularis was incriminated as a vector of malaria in rural West Bengal and by PCR method in collections from different districts of Odisha. An. annularis collected from Ranchi and West Singhbhum districts of Jharkhand state were incriminated in our laboratory by ELISA techniques[19],[20].

Cytological studies on An. annularis found it to be species complex of two sibling species exhibiting the diagnostic inversion genotypes A and B[21]. In Jharkhand state cytological study on An. annularis revealed the presence of species Aby polymer chain reaction - Restriction fragment length polymorphism (PCR-RFLP) of ribosomal DNA internal transcribed spacer 2 (ITS2) and domain 3 (D3)[22].

An. annularis is abundantly present throughout the year and transmits malaria and recently has been presumed to be an important vector of malaria in Jharkhand state. An. annularis became increasingly important due to their high density and its role in malaria transmission throughout the year (unpublished result, National Institute of Malaria Research annual report, 2007–2008). The species thus should have a definite role in transmission of malaria in this region though more evidence needs to be generated. This species co-exists with other malaria vector species and is also a target for the same vector control interventions. Thus, management of this species will be important in view of the possible role of this species in epidemiology of the disease. As the species is under similar selection of insecticides in use in public health in vector control as other primary vector species, it was felt pertinent to assess the impact of vector control interventions on An. annularis. Hence, a study was conducted in 2017 and 2018 in six districts of the state to assess the status of insecticide resistance to the commonly used insecticides in malaria vector control interventions.

  Material & Methods Top

Study area

The present study was conducted in villages in 12 Community Health Centres (CHCs) in six districts during 2017 and 2018. The districts (CHCs) were Simdega (Kurdeg and Simdega), Gumla (Bharno and Gumla), Khunti (Khunti and Murhu), West Singhbhum (Chaibasa and Bada Jamda), Godda (Poraiyahat and Sunderpahari) and Sahibganj (Rajmahal and Borio) respectively [Figure 1]. In each district, two CHCs and five to six villages in different terrains i.e., plain, hilltop, foothill and forest, were selected for the susceptibility tests. The study districts are dominated by ethnic tribes and the most dominated tribes were Ho, Munda, Oraon, Santhal, Gonds, Bhumij, Kols, Kharmalo, Kharwar, Kharia, Birhor, Birjia, Chick, and Baraik. The climate is humid and subtropical in the north to tropical wet and dry with an average annual rainfall of about 1000–1500 mm and temperature varying between 25°C to 38°C. The study area has many rivers, ponds, terrace paddy fields, rivulets which provide sufficient breeding grounds for mosquitoes particularly anopheline species. To date, DDT (organochlorine) and synthetic pyrethroids have been used for IRS in malaria control program in the state. DDT is being used for IRS for malaria vector control in the state since the inception of the national vector-borne disease control program in 1950s.
Figure 1: Map of Jharkhand, India showing location of districts where insecticide resistance studies were conducted.

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Mosquito collection, identification and susceptibility test

Full-fed adult indoor resting female anopheles’ mosquitoes were collected from cattle sheds, human dwelling and mixed dwellings in each village in the morning during 5.00 h-6.00 h using a mouth aspirator and torch light. The mosquitoes collected were kept in a 30 x 30 cm cloth cage with a wet cloth wrapped around the cage and brought to the laboratory. The field collected mosquitoes were provided with 10% glucose solution soaked in cotton pad.

The species of mosquitoes were identified morphologically using standard identification keys of anophelines[23],[24],[25],[26],[27]. Susceptibility tests were performed on blood fed female using WHO kits. The temperature and humidity of the lab was maintained at 27+–2oC and 70–80% respectively. Insecticide impregnated papers of DDT (4%), malathion (5%), deltamethrin (0.05%) and permethrin (0.75%) were obtained from University SANS Malaysia, Penang, Malaysia. No insecticide paper was used beyond five times of exposure. Female mosquitoes were exposed in at least 3–4 test replicates against the given insecticide for 1 h followed by 24 h holding period. Parallel controls were run for the respective insecticide class. Mortality was determined by scoring the dead and alive mosquitoes at the end of 24 h holding period. The result was expressed in percent mortality. If the control mortality remained between 5–20%, the test mortality was corrected by using Abott’s formula and expressed as corrected percent mortality. The test was discarded if the control mortality was >20%. Data was interpreted following the WHO criteria: mortality of 98–100% is designated as ‘susceptible’, <90% as ‘confirmed resistant’ and mortality between 90–97% as ‘possible resistance’ (WHO, 2016)[28].

Ethical statement: Not applicable

  Results Top

[Table 1] summarizes the susceptibility status of An, annularis to DDT, malathion, deltamethrin and permethrin. An, annularis was reported confirmed resistant to DDT in all the 12 CHCs of 6 districts viz., Simdega (Simdega and Kurdeg), Gumla (Bharno and Gumla), Khunti (Khunti and Murhu), West Singhbhum (Chaibasa and Badajamda), Godda (Poraiyahat and Sunderpahari) and Sahibganj (Borio and Rajmahal). To malathion, the species reported possible resistance with mortality in the range of 91–97% in 3 CHCs of 3 districts viz., Sahibganj (Borio CHC), Khunti (Khunti CHC) and Gumla (Bharno CHC), whereas it was found susceptible to malathion in Simdega, Khunti, West Singhbhum and Godda districts with mortality of more than 98%. To deltamethrin and permethrin, it was found to be completely susceptible in all the six districts [Figure 2].
Figure 2: Map showing insecticide susceptibility status of An, annularis to discriminatory dosages of DDT, malathion, deltamethrin and permethrin in six districts (average mortality in 2 CHCs studied in each district) of Jharkhand state, India. [CR; confirmed resistance, PR; possible resistance, S; susceptible].

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Table 1: Insecticide susceptibility status of An. annularis to discriminatory dosages of DDT, malathion, deltamethrin and permethrin in six districts of Jharkhand state, India (2017-2018)

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  Discussion Top

Effective vector control depends on effective insecticidal interventions and vector susceptibility to insecticides. Targeting the mosquito vector is the most effective way to prevent malaria transmission in our country. Indoor residual spraying and long-lasting insecticidal nets (LLINs) in the control of vectors continue to be the mainstay of malaria control program by National Vector Borne Disease Control Programme (NVBDCP) in India. There are about 125 mosquito species with documented resistance to one or more insecticide[29]. Monitoring of vector susceptibility to insecticides at regular interval has become imperative to insure judicious use of insecticides against vector species in the control programme. The resistance of the species to DDT is well established in many parts of the country[6]. The present finding highlights the current insecticide susceptibility status of malaria vector An, annularis in Jharkhand state. The species was reported as the secondary vector and vector of prominence in states of Odisha, Jharkhand, West Bengal, Andhra Pradesh.

To DDT, An, annularis exhibited resistance in all the six surveyed districts viz., Simdega, Gumla, Khunti, West Singhbhum, Sahibganj and Godda. An annularis reported resistance to DDT was first time in the district Meerut of Uttar Pradesh[30] and later in Jharkhand state in districts Dhanbad[31] and Hazaribagh[32] but was reported susceptible in Cuttack and Koraput districts[33] of Odisha and presence of cross resistance to HCH[34]. An, annularis developed double resistance to DDT and Dieldrin in Cachar and Sibsagar district in Assam[35], Sundergarh and Koraput districts of Odisha[36],[37]. An, annularis was reported resistant to DDT in Gajapati, Nabarangpur and Rayagada districts of Odisha (personal communication with Dr. RK Hazra) and Bikaner district of Rajasthan[38] and recently in Kamrup and Baksa districts of Assam[39]. Recently, our studies carried out at Gumla district showed An, annularis was resistant to DDT and susceptible to other insecticide[40]. In Koderma district this species was also found resistant to DDT[41]. This species was also reported resistant to DDT and susceptible to other insecticides in the Gadchiroli district of Maharashtra states[42]. An, annularis has also been found susceptible to DDT, malathion, fenitrothion, deltamethrin in different states of India[43]. Our study corroborates the finding of DDT resistance to An, annularis in different states of India.

To malathion, An, Annularis showed possible resistance in Gumla (Bharno CHC), Khunti (Khunti CHC) and Sahibganj (Borio CHC) districts, This species has also been found susceptible to malathion in all other districts and also in districts of the states of Maharashtra, Odisha and Rajasthan. The species was reported resistant in district East Singhbhum and under possible resistance category in West Singhbhum and Gumla districts of Jharkhand. In Gadchiroli district in Maharashtra and Bikaner district in Rajasthan it has been reported to be possible resistant[44]. Our study showed that, An, annularis was susceptible to deltamethrin and permethrin in all the six districts of Jharkhand state.

  Conclusion Top

Two important conclusions can be derived from the present study. (1) An, annularis could be the prominent malaria vector in Jharkhand state owing to its distribution and contemplated role in transmission, and (2) as the species reported confirmed resistance to DDT, possible resistance to malathion and complete susceptibility to deltamethrin and permethrin, present pyrethroid based interventions in use in the state will be effective against An, annularis but continued use may render the population resistant. Hence, for effective vector control management there is a need for regular monitoring of insecticide resistance in this species. As specific control strategy for secondary vectors is absent and as these species are also epidemiologically important in certain localized situations, there is a need for renewed focus on such species especially in view of the ongoing efforts towards malaria elimination.

Conflict of interest: None

  Acknowledgements Top

We are thankful to the Director, National Institute of Malaria Research, Delhi for the encouragement in preparing the manuscript. The present investigation received financial support from the Indian Council of Medical Research, New Delhi. The authors are thankful for the assistance given in the field by Mr. Dipak Kumar Mallick, Ram Bachan Gupta, and Mr Saroj Kumar Das. Miss Reeta Kumari is also thankfully acknowledged for her assistance in drafting the manuscript. The authors are also thankful to SPO and his staff for providing information on malaria incidence. The DMO and his staff of different districts of the State Vector Borne Disease Control Programme are also acknowledged for their valuable support in the field.

  References Top

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