|Year : 2015 | Volume
| Issue : 7 | Page : 59-63
Triple insecticide resistance in Anopheles culicifacies: A practical impediment for malaria control in Odisha State, India
SS Sahu, K Gunasekaran, T Vijayakumar, P Jambulingam
Vector Control Research Centre (ICMR), Puducherry, India
|Date of Submission||15-Oct-2014|
|Date of Web Publication||17-Feb-2016|
S S Sahu
Vector Control Research Centre, Field Station (ICMR), Koraput, At-Hati Line, Near Collectorate, P.O./Dt.- Koraput 764 020, Odisha
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Background & objectives: In Odisha State, the control of malaria vectors has become dependent on synthetic pyrethroids, which are used for treatment of all approved long-lasting insecticidal nets (LLINs). The vast use of just one class of insecticide has led to the problem of resistance to insecticides in malaria vectors. One of the major malaria vectors in Odisha State is Anopheles culicifacies Giles. The aim of this study was to determine the resistance status of An. culicifacies to deltamethrin, a synthetic pyrethroid and other common insecticides used by the National Vector Borne Diseases Control Programme (NVBDCP) for indoor residual spraying in Odisha State.
Methods: Mosquitoes were collected during April 2014 - June 2014 from 15 randomly selected villages in five p0 lasmodium falciparum endemic southern districts of Odisha State. The blood-fed wild caught females were exposed to the diagnostic dosage of DDT (4.0%), malathion (5.0%) and deltamethrin (0.05%) for one hour. Mortality was recorded at 24 h after the exposure.
Results: Results indicated that An. culicifacies was resistant to all the three insecticides used in the malaria control programme in the five districts of Odisha State.
Interpretation & conclusions: Resistance management strategy by appropriate rotation of different groups of insecticides including carbamates and incorporating a synergist with synthetic pyrethroids for treating mosquito nets should be considered for the control of malaria vectors in the area, especially where An. culicifacies is predominant. Periodical monitoring of susceptibility/resistance status of An. culicifacies to different insecticides is warranted.
Keywords: Anopheles culicifacies - India - insecticide resistance - malaria - Odisha - vector
|How to cite this article:|
Sahu S S, Gunasekaran K, Vijayakumar T, Jambulingam P. Triple insecticide resistance in Anopheles culicifacies: A practical impediment for malaria control in Odisha State, India. Indian J Med Res 2015;142, Suppl S1:59-63
|How to cite this URL:|
Sahu S S, Gunasekaran K, Vijayakumar T, Jambulingam P. Triple insecticide resistance in Anopheles culicifacies: A practical impediment for malaria control in Odisha State, India. Indian J Med Res [serial online] 2015 [cited 2020 Feb 20];142, Suppl S1:59-63. Available from: http://www.ijmr.org.in/text.asp?2015/142/7/59/176621
Use of insecticides for reducing populations of malaria vectors has been the main strategy for control of malaria in India. Currently, 12 insecticides belonging to four chemical classes are recommended by WHO Pesticide Evaluation Scheme (WHOPES) for indoor residual spraying (IRS)  . The current strategy to control malaria vectors in India mainly includes IRS with DDT/synthetic pyrethroids and use of long lasting insecticide nets (LLINs) , . Anopheles culicifacies (Diptera: Culicidae) is the widespread malaria vector species found throughout the rural and peri-urban areas, contributing to about 65 per cent of malaria cases in India  . In the beginning, indoor residual spraying with DDT was used for the control of this species. But, gradually An. culicifacies developed resistance against DDT and it was the first mosquito species to develop resistance against this insecticide  . Soon after the introduction of malathion in the country in 1969, especially in DDT resistant areas, double resistance was reported in An. culicifacies in Gujarat and Maharashtra States in 1977  . In 1990s deltamethrin was introduced in the country for indoor residual spraying and treatment of mosquito nets. Consequently, reduced susceptibility to deltamethrin in An. culicifacies was reported for the first time from Ramnathapuram district, Tamil Nadu in 2002  .
Studies have been carried out on the susceptibility status of An. culicifacies in different parts of Odisha State  . The studies carried out during 2004 in eight districts of the State reported that An. culicifacies was resistant to DDT in all the eight districts, to malathion in four districts (Mayurbhanj, Bolangir, Nuapada and Kalahandi) and showed a tendency of developing multiple resistance to DDT, malathion and deltamethrin in three districts (Bolangir, Nuapada and Kalahandi)  . An entomological study was conducted in ten southern districts of the State when LLINs were just distributed and it showed that in eight districts, the response of An. culicifacies to deltamethrin was under 'verification required' category indicating its tendency towards development of resistance to deltamethrin  . In view of this indication of tolerance of this species to the synthetic pyrethroid in the event of four to five years of field use of LLINs in the districts, a study was undertaken in five of the ten southern districts of Odisha State to verify the susceptibility/resistance status of An. culicifacies to deltamethrin and also to the other two commonly used insecticides i.e. DDT and malathion.
| Material & Methods|| |
The study was conducted in five southern districts of Odisha State viz. Rayagada, Nowrangpur, Kalahandi, Malkangiri and Koraput. An. culicifacies was tested against the diagnostic dosage of DDT, malathion and deltamethrin during April to June 2014. Dry summer (March-June), wet rainy (July-October) and dry winter (November-February) are the three prevailing seasons. The districts have been hyperendemic for malaria since many years  . Plasmodium falciparum is the predominant species, with a proportion of >90 per cent of the total malaria cases , . Anopheles fluviatilis and An. culicifacies are the two malaria vector species prevalent in the five districts , . The villages in the districts are situated on foothills or plains and are characterized by presence of perennial streams, rivulets, ponds and paddy fields, which are the major breeding habitats of the two vector species. Majority of the villagers live in huts made of mud walls with either thatched or tiled roofs. The walls of the hut are usually of seven feet in height, with a gap of 2 to 3 feet between the side walls and roof. The cattle sheds are kept close by human dwellings. Human dwellings are sprayed with two rounds of DDT or synthetic pyrethroids every year. In addition, long lasting synthetic pyrethroid (deltamethrin) treated mosquito nets (LLINs) have been distributed in these districts since 2009 in a phased manner.
One community health centre (CHC) from each of the five districts was randomly selected. In each CHC, three villages, representing the respective CHC with reference to the density of An. culicifacies, were randomly selected for collection of An. culicifacies to determine its susceptibility/resistance status  .
Mosquito collections and susceptibility test: Female Anopheles mosquitoes were collected from cattle sheds and human dwellings in the study villages during early morning hours using mouth aspirator and flash light. The collected mosquitoes were transported to the laboratory at Vector Control Research Centre, Field Station, Koraput, Odisha, in a mosquito cage (one cubic foot) covered with a wet towel, identified to species based on morphological characters using a standard key  and separated according to their gonotrophic conditions. WHO kits were used to conduct the susceptibility test  . The temperature and relative humidity (RH) in the laboratory was maintained at 25 ± 2 °C and 70-85 per cent RH. Papers impregnated with DDT 4 per cent, malathion 5 per cent and deltamethrin 0.05 per cent were obtained from the University Sains Malaysia, Penang, Malaysia. The fully fed mosquitoes were exposed to the diagnostic dosage of the insecticides for one hour in 5 to 6 replicates, each replicate with 15 to 25 mosquitoes. Parallel controls were maintained for comparison (i.e. 2 to 3 replicates each with 15 to 25 mosquitoes)  . Number knocked down was recorded after one hour of exposure and after the exposure the mosquitoes were maintained in holding tubes with access to glucose food for 24 h at the same temperature and relative humidity. Mortality was scored after 24 h of holding. Since the control mortality in all the tests remained below 5 per cent, the test mortality was not corrected using Abbott's formula  . According to the WHO criteria  , a corrected mortality of >98 per cent is 'susceptible', <90 per cent is 'resistant' and 90-98 per cent is 'verification required'.
| Results & Discussion|| |
A total of 135, 130 and 131 female An. culicifacies mosquitoes in Rayagada, 105, 110 and 113 in Nawarangapur, 105, 111 and 131 in Kalahandi, 111, 105 and 119 in Malkangiri and 111,111 and 112 in Koraput district were exposed to DDT 4 per cent, malathion 5 per cent and deltamethrin 0.05 per cent, respectively. The test mortality of this vector species against the three insecticides are given in the [Table I]. The test mortality ranged between 11.4 and 15.3 per cent against DDT 4 per cent, 60.4 and 76.2 per cent against malathion 5 per cent, and 72.6 and 84.0 per cent against deltamethrin 0.05 per cent in these districts. The results showed that An. culicifacies was resistant to DDT, malathion and deltamethrin in all the five districts.
|Table 1. Response of An. culicifacies to DDT, malathion and deltamethrin in the five southern districts of Odisha State |
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Under the modified plan of operation implemented in 1977, the study districts continued to receive DDT indoor residual spraying, since annual parasite incidence (API) was >2 in all the districts  . From 2001 onwards, DDT was replaced with synthetic pyrethroids (deltamethrin/alphacypermethrin/lambdacyhalothrin)for indoor residual spraying in five of the 11 CHCs in Rayagada district and in seven of the 13 CHCs (where API >10) in Kalahandi district. (State National Vector Borne Diseases Control Programme Office, Bhubaneshwar, personal communication). Insecticide treated mosquito nets (ITMNs) were introduced during 2001 to 2008 in some of the CHCs of the five districts. In addition, long lasting synthetic pyrethroid (deltamethrin) treated mosquito nets (LLINs) were distributed in these districts from 2009 to 2013 in a phased manner.
An. culicifacies was reported to be resistant to DDT but susceptible to malathion and deltamethrin  during 1995 in Koraput district. Subsequently, during 2010-2011 the response of this species to deltamethrin in Rayagada, Kalahandi and Malkangiri districts was found to be resistant, in Nawarangpur district was under the 'verification required' category and in Koraput district was susceptible  as per the guidelines of WHO, 2013  . Resistance to DDT and malathion in An. culicifacies was confirmed during the current study. In addition, the current study confirmed the development of resistance in this species to deltamethrin in the five southern districts of the State. An. fluviatilis, the other malaria vector in the study area was susceptible to DDT, malathion and deltamethrin , . However, the susceptibility status of An. fluviatilis could not be assessed during the current study due to non-availability of adequate number of this species from the study area.
During the early part of 20 [th] century, indoor residual spraying of insecticides, particularly DDT, was the key component of malaria control and was responsible for the spectacular reduction in malaria incidence  . Over time and with widespread use in agriculture, mosquito resistance to DDT had emerged  . Between 1961 and 1966, the malaria rate in India increased three-fold; DDT resistance was a partial cause for this , . Several studies have been conducted on vector susceptibility to insecticides in different parts of the country , . Resistance to DDT in An. culicifacies is widespread in the country ,, and to malathion in the States of Maharashtra, Gujarat, Tamil Nadu and Uttar Pradesh ,,, . There are a few reports of decreased susceptibility in this vector to synthetic pyrethroids ,, . This species has developed resistance to DDT in 286 districts, to malathion in 81 and to pyrethroids in two districts in India  . A recent study conducted in four States (Andhra Pradesh, Odisha, Jharkhand and West Bengal) of India showed that An. culicifacies was resistant to DDT in 32 districts and to malathion in 14 districts, under verification required category in 10 districts and susceptible in eight districts. To deltamethrin this species was resistant in four districts, under verification required category in 11 districts and susceptible in 17 districts  .
One of the limitations of the study was that parallel data could not be generated for An. fluviatilis due to its non-availability in adequate number. Considering operational implication, generation of data was not done up to sibling species level in An. culicifacies, which might be another limitation. The spread of insecticide resistance, especially pyrethroid resistance as indicated by the current study and also the studies conducted in other parts of the country, is a major threat for the vector control programmes, as it is being extensively used for IRS and impregnation of bed nets in India. In this context, preservation of pyrethroid susceptibility in target vector population should be the key priority in the choice of vector control methods at this hour. Insecticide resistance management needs to be considered for vector control, including the selection of insecticides for IRS. Using the same insecticide for multiple successive IRS cycles may not be recommended; it is preferable to use a system of rotation with different groups of insecticides including carbamates in the area where An. culicifacies is resistant to deltamethrin  . Rotations should start with the insecticides to which there is the lowest frequency of resistance. In the areas of high coverage with LLINs, pyrethroids may not be a good option for IRS, as this will add to selection pressure. Further, using nets impregnated with a synthetic pyrethroid together with a synergist would be a better option against pyrethroid resistant malaria vectors. Mixture nets such as this may have application against resistant mosquitoes, particularly those whose resistance is based on oxidative metabolism  . Since, monitoring insecticide resistance is a necessary element of the implementation of insecticide-based vector control interventions, regular monitoring of susceptibility/resistance status of the malaria vectors to commonly used insecticides, at least once a year or preferably every six months  is warranted particularly in An. culicifacies predominant areas to strengthen the evidence base for the effectiveness of ongoing vector control interventions.
| Acknowledgment|| |
The technical assistance rendered by the staff of VCRC field station, Koraput, Odisha is acknowledged.
Conflicts of Interest: None.
| References|| |
World Health Organization (WHO). Pesticides and their application for the control of vectors and pests of public health importance
, 6 [th]
ed. Geneva: WHO; 2006.
World Health Organization (WHO). Test procedures for insecticide resistance monitoring in malaria vector mosquitoes.
Geneva: WHO; 2013.
Sharma VP. Fighting malaria in India. Curr Sci
Rahman J, Roy ML, Singh K. Development of increased tolerance to DDT in Anopheles culicifacies
Giles, in the Panch Mahal district of Bombay state, India. Indian J Malariol
Singh RK, Kumar G, Mittal PK. Insecticide susceptibility status of malaria vectors in India: a review. Int J Mosq Res
Mittal PK, Adak T, Singh OP, Raghavendra K, Subbarao SK. Reduced susceptibility to deltamethrin in Anopheles culicifacies sensu lato
in Ramanathapuram district, Tamil Nadu: selection of a pyrethroid resistant strain. Curr Sci
Sahu SS, Gunasekaran K, Raju HK, Vanamail P, Pradhan MM, Jambulingam P. Response of malaria vectors to the conventional insecticides in the southern districts of Odisha state, India. Indian J Med Res
Sharma SK, Upadhyay AK, Haque MA, Singh OP, Adak T, Subbarao SK. Insecticide susceptibility status of malaria vectors in some hyperendemic tribal districts of Odisha. Curr Sci
National Vector Borne Disease Control Programme. Malaria situation in India
. National Vector Borne Disease Control Programme, Directorate General of Health Services, Ministry of Health & Family Welfare, Government of India. Available from: www.nvbdcp.gov
, accessed on June 20, 2014.
Sahu SS, Gunasekaran K, Vanamail P, Jambulingam P. Persistent foci of falciparum
malaria among tribes over two decades in Koraput district of Odisha state, India. Malar J
Christophers SR. The fauna of British India, including Ceylon and Burma
. Diptera, vol. IV. Family Culicidae, Tribe Anophelini
. London: Taylor and Francis; 1933. p. 370.
Abbott WS. A method of computing the effectiveness of an insecticide. J Econ Entomol
Pattanayak S, Roy RG. Malaria in India and modified plan of operations for its control. J Common Dis
Sahu SS, Patra KP. A study on insecticides resistance in Anopheles fluviatilis
and Anopheles culicifacies
to HCH and DDT in the Malkangiri district of Orissa. Indian J Malariol
Mabaso ML, Sharp B, Lengeler C. Historical review of malarial control in southern African with emphasis on the use of indoor residual house-spraying. Trop Med Int Health
Chapin G, Wasserstrom R. Agricultural production and malaria resurgence in Central America and India. Nature
Raghavendra K, Vasantha K, Subbarao SK, Pillai MK, Sharma VP. Resistance in Anopheles culicifacies
sibling species B and C to malathion in Andhra Pradesh and Gujarat state, India. J Am Mosq Control Assoc
Singh RK, Dhiman RC, Mittal PK, Das MK. Susceptibility of malaria vectors to insecticides in Gumla district, Jharkhand state, India. J Vector Borne Dis
Sharma VP, Chandrahas RK, Ansari MA, Srivastava PK, Razdan RK, Batra CP, et al
. Impact of DDT and HCH spraying on malaria transmission in villages with DDT and HCH resistant Anopheles culicifacies. Indian J Malariol
Sharma SN, Shukla RP, Raghavendra K. Susceptibility status of An. fluviatilis
and An. culicifacies
to DDT, deltamethrin and lambda-cyhalothrin in district Nainital, Uttar Pradesh. Indian J Malariol
Gunasekaran K, Sahu SS, Jambulingam P, Das PK. DDT indoor residual spray, still an effective tool to control Anopheles fluviatilis
-transmitted Plasmodium falciparum
malaria in India. Trop Med Int Health
Vittal M, Bhate MR. Bioassay tests on the effectiveness of malathion spraying in Aurangabad town, Maharashtra. Indian J Malariol
Deobhankar RK, Pelkar ND. Magnitude of DDT resistance in Anopheles culicifacies
in Maharashtra State. J Commun Dis
Shukla RP, Sharma SN, Bhat SK. Malaria outbreak in Bhojpur PHC of district Moradabad, Uttar Pradesh,
India. J Commun Dis
Singh OP, Raghavendra K, Nanda N, Mittal PK, Subbarao SK. Pyrethroid resistance in Anopheles culicifacies
in Surat district Gujarat, west India. Curr Sci
Singh RK, Mittal PK, Gourshettiwar MP, Pande SJ, Dhiman RC. Susceptibility of malaria vectors to insecticides in Gadchiroli district (Maharashtra), India. J Vector Borne Dis
Raghavendra K, Barik TK, Sharma SK, Das MK, Dua VK, Pandey A, et al
. A note on the insecticide susceptibility status of principal malaria vector Anopheles culicifacies
in four States of India. J Vector Borne Dis
Raghavendra K, Verma V, Srivastava HC, Gunasekaran K, Sreehari U, Das AP. Persistance of DDT, malathion & deltamethrin resistance in Anopheles culicifacies
after their sequential withdrawal from indoor residual spraying in Surat district, India. Indian J Med Res
Pennetier C, Bouraima A, Chandre F, Piameu M, Etang J, Rossignol M, et al
. Efficacy of Olyset [®]
Plus, a new long-lasting insecticidal net incorporating permethrin and piperonil-butoxide against multi-resistant malaria vectors. P l0 o s0 o0 ne
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