Measures to Control Phlebotomus argentipes and Visceral Leishmaniasis in India

  • Richard M. Poché Genesis Laboratories, 10122 NE Frontage Road, Wellington, CO 80549, USA
  • Rajesh Garlapati Genesis Laboratories India Private Limited, Patna, Bihar, India
Visceral leishmaniasis, Leishmania donovani, Phlebotomus argentipes, sand flies, vector control


Visceral leishmaniasis is a deadly parasitic disease that is transmitted via the bite of a female sand fly, Phlebotomus argentipes. The highest burden of this disease is in northern India. In 2005, India embarked on an initiative with Ne­pal, Bangladesh, and the World Health Organization to eliminate visceral leishmaniasis by 2015. With the goal of 1 case in 10,000 people still unmet, it is prudent to evaluate the tools that have been used thus far to reduce vector numbers and cases of the disease. Herein, we present a review of studies conducted on vector-control strategies in India to combat visceral leishmaniasis including indoor residual spraying, insecticide-treated bed nets, environmental modification, and feed-through insecticides. This review suggests that the quality of indoor residual spraying may enhance control measures while a combination of spraying, nets, and feed-through insecticides would best confront the diverse habitats of P. argentipes.


Addy M, Nandy A (1992) Ten years of kala- azar in West Bengal, part I: did post- kala-azar dermal leishmaniasis initiate the outbreak in 24-Parganas? Bull World Health Org. 70(3): 341–346.

Alvar J, Yactayo S, Bern C (2006) Leish- maniasis and poverty. Trends Parasi- tol. 22(12): 552–557.

Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, den Boer M, WHO Leishmaniasis Control Team (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS One. 7(5): e35671.

Beard J (2006) DDT and human health. Sci Total Environ. 355(1-3): 78–89. Beckvar N, Lotufo GR (2011) DDT and oth-er Organohalogen Pesticides in Aquat- ic Organisms. In: Beyer WN, Meador JP (Eds) Environmental Contaminants in Biota: Interpreting Tissue Concen- trations. Vol 2. CRC Press, New York, pp. 47–101.

Bern C, Joshi AB, Jha SN, Das ML, High- tower A, Thakur GD, Bista MB (2000) Factors associated with visceral leish-maniasis in Nepal: bed-net use is strongly protective. Am J Trop Med Hyg. 63(3-4): 184–188.

Bern C, Hightower AW, Chowdhury R, Ali M, Amann J, Wagatsuma Y, Haque R, Kurkjian K, Vaz LE, Begum M, Akter T, Cetre-Sossah CB, Ahluwalia IB, Dotson E, Secor WE, Breiman RF, Maguire JH (2005) Risk factors for ka- la-azar in Bangladesh. Emerg Infect Dis. 11(5): 655–662.

Bern C, Chowdhury R (2006) The epidemi- ology of visceral leishmaniasis in Bangladesh: prospects for improved control. Indian J Med Res. 123(3):275–288.

Bhunia, GS, Kesari S, Chatterjee N, Kumar V, Das P (2013) The burden of vis- ceral leishmaniasis in India: challenges in using remote sensing and GIS to understand and control. ISRN Infect Dis. 2013: Article ID 675846.

Blus LJ (2003) Organochlorine Pesticides.In: Hoffman DJ, Rattner BA, Burton GA Jr, Cairns J Jr. (Eds) Handbook of Ecotoxicology Vol. 2. Lewis Publish- ers, New York, pp. 313–340.

Boelaert M, Meheus F, Sanchez A, Singh SP, Vanlerberghe V, Picado A, Meessen B, Sundar S (2009) The poor- est of the poor: a poverty appraisal of households affected by visceral leish- maniasis in Bihar, India. Trop Med Int Health. 14(6): 639–644.

CDC (2012) Malaria: Indoor residual spray- ing. Available at: malaria/malaria_worldwide/reduction/ irs.html (Accessed: 26 March 2015).

Cerf BJ, Jones TC, Badaro R, Sampaio D, Teixeira R, Johnson WD (1987) Mal- nutrition as a risk factor for severe vis- ceral leishmaniasis. J Infect Dis.156(6): 1030–1033.

Chappuis F, Sundar S, Hailu A, Ghalib H, Rijal S, Peeling RW, Alvar J, Boelaert M (2007) Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat Rev Microbiol. 5(11):873–882.

Chowdhury R, Huda MM, Kumar V, Das P, Joshi AB, Banjara MR, Akhter S, Kroeger A, Krishnakumari B, Petzold M, Mondal D, Das ML (2011a) The Indian and Nepalese programmes of indoor residual spraying for the elimi- nation of visceral leishmaniasis: per- formance and effectiveness. Ann Trop Med Parasitol. 105(1): 31–35.

Chowdhury R, Dotson E, Blackstock AJ, McClintock S, Maheswary NP, Faria S, Islam S, Akter T, Kroeger A, Akh- ter S, Bern C (2011b) Comparison of insecticide-treated nets and indoor re- sidual spraying to control the vector of visceral leishmaniasis in Mymensingh district, Bangladesh. Am J Trop Med Hyg. 84(5): 662–667.

Clem A (2010) A current perspective on leishmaniasis. J Glob Infect Dis. 2(2):124–126.

Cohn BA, La Merrill M, Krigbaum NY, Yeh G, Park J-S, Zimmermann L, Cirillo PM (2015) DDT exposure in utero and breast cancer. J Clin Endocrinol Metab.100(8) 5-72 doi:


Das M, Banjara M, Chowdhury R, Kumar V, Rijal S, Joshi A, Akhter S, Das P, Kroeger A (2008) Visceral leishmania- sis on the Indian sub-continent: a mul- ti-centre study of the costs of three in- terventions for the control of the sand fly vector, Phlebotomus argentipes. Ann Trop Med Parasitol. 102(8): 729–741.

Derbali M, Polyakova L, Boujaâma A, Bur- russ D, Cherni S, Barhoumi W, Chelbi I, Poché R, Zhioua E (2014) Labora- tory and field evaluation of rodent bait treated with fipronil for feed through and systemic control of Phlebotomus papatasi. Acta Trop. 135: 27–32.

Desjeux P (1996) Leishmaniasis. Public health aspects and control. Clin Der- matol. 14(5): 417–423.

Dhiman RC, Raghavendra K, Kumar V, Kesari S, Kishore K (2003) Suscepti- bility status of Phlebotomus argentipes to insecticides in districts Vaishaii and Patna (Bihar). J Commun Dis. 35(1):49–51.

Dinesh DS, Das P, Picado A, Davies C, Speybroeck N, Ostyn B, Boelaert M, Coosemans M (2008) Long-lasting in- secticidal nets fail at household level to reduce abundance of sandfly vector Phlebotomus argentipes in treated house in Bihar (India). Trop Med Int Health. 13(7): 953–958.

Dinesh DW, Kumari S, Kumar V, Das P (2014) The potentiality of botanicals and their products as an alternative to chemical insecticides to sand flies (Diptera: Psychodidae): a review. J Vector Borne Dis. 51(1): 1–7.

Garlapati RB, Abbasi I, Warburg A, Poché D, Poché R (2012) Identification of bloodmeals in wild caught blood fed Phlebotomus argentipes (Diptera: Psy- chodidae) using cytochrome b PCR and reverse line blotting in Bihar, In- dia. J Med Entomol. 49(3): 515–521.

Guerin PJ, Olliaro P, Sundar S, Boelaert M, Croft SL, Desjeux P, Wasunna MK, Bryceson AD (2002) Visceral leish- maniasis: current status of control, di- agnosis, and treatment, and a proposed research and development agenda. Lancet Infect Dis. 2(8): 494–501.

Huda MM, Mondal D, Kumar V, Das P, Sharma SN, Das ML, Roy L, Gurung CK, Banjara MR, Akhter S, Mahe- swary NP, Kroeger A, Chowdhury R (2011) Toolkit for monitoring and evaluation of indoor residual spraying for visceral leishmaniasis control in the India subcontinent: application and results. J Trop Med. 2011: 876742.

Ingenloff K, Garlapati R, Poché D, Singh MI, Remmers JL, Poché RM (2013) Feed- through insecticides for the control of the sand fly Phlebotomus argentipes. Med Vet Entomol. 27(1): 10–18.

Jeronimo SMB, de Queiroz Sousa A, Person RD (2006) Leishmaniasis. In: Guerrant RL, Walker DH, Weller PF (Eds) Tropical Infectious Diseases: Princi- ples, Pathogens and Practice. Vol. 1. Churchill Livingstone Elsevier, Edin- burgh, Scotland, pp. 1095–1113.

Joshi A, Narain JP, Prasittisuk C, Bhatia R, Hashim G, Jorge A, Banjara M, Kroeger AJ (2008) Can visceral leish- maniasis be eliminated from Asia? Vector Borne Dis. 45(2): 105–111.

Joshi AB, Das ML, Akhter S, Chowdhury R, Mondal D, Kumar V, Das P, Kroeger A, Boelaert M, Petzold M (2009) Chemical and environmental vector control as a contribution to the elimi- nation of visceral leishmaniasis on the India subcontinent: cluster randomized controlled trials in Bangladesh, India and Nepal. BMC Med. 7: 54.

Kishore K, Kumar V, Kesari S, Bhattacharya SK, Das P (2004) Susceptibility of Phlebotomus argentipes against DDT in endemic districts of north Bihar, In- dia. J Commun Dis. 36(1): 41–44.

Kishore K, Kumar V, Kesari S, Dinesh DS, Kumar AJ, Das P, Bhattacharya SK (2006) Vector control in leishmaniasis. Indian J Med Res. 123(3): 467–472.

Kulkarni MA, Malima R, Mosha FW, Msangi S, Mrema E, Kabula B, Lawrence B, Kinung'hi S, Swilla J, Kisinza W, Rau ME, Miller JE, Schellenberg JA, Max- well C, Rowland M, Magesa S, Drake- ley C (2007) Efficacy of pyrethroid- treated nets against malaria vectors and nuisance-biting mosquitoes in Tanzania in areas with long-term insecticide- treated net use. Trop Med Int Health.12(9): 1061–1073.

Kumar V, Kesari SK, Sinha NK, Palit A, Ranjan A, Kishore K, Saran R, Kat SK (1995) Field trial of an ecological ap- proach for the control of Phlebotomus argentipes using mud and lime plaster. India J Med Res. 101: 154–156.

Kumar NP, Srinivasan R, Jambulingam P (2012) DNA barcoding for identifica- tion of sand flies (Diptera: Psychodi- dae) in India. Mol Ecol Resour. 12(3):414–420.

Lengeler C (2004) Insecticide-treated bed nets and curtains for preventing ma- laria. Cochrane Database Syst Rev. 2: CD000363.

Malaviya P, Hasker E, Singh RP, Van Geer- truyden JP, Boelaert M, Sundar S (2013) Village health workers in Bi- har, India: an untapped resource in the struggle against kala-azar. Trop Med Int Health. 18(2): 188–193.

Malaviya P, Hasker E, Picado A, Mishra M, Van Geertruyden JP, Das ML, Boela- ert M, Sundar S (2014) Exposure to Phlebotomus argentipes (Diptera, Psy- chodidae, Phlebotominae) sand flies in rural areas of Bihar, India: the role of housing conditions. PLoS One. 9(9): e106771.

Maroli M, Feliciangeli MD, Bichaud L, Charrel RN, Gradoni L (2013) Phlebotomine sandflies and the spread- ing of leishmaniasis and other diseases of public health concern. Med Vet En- tomol. 27(2): 123–147.

Mascari TM, Mitchell MA, Rowton ED, Foil LD (2008) Ivermectin as a rodent feed- through insecticide for control of im- mature sand flies (Diptera: Psychodi- dae). J Am Mosq Control Assoc. 24 (2): 323–326.

Mascari TM, Stout RW, Foil LD (2013) Oral treatment of rodents with fipronil for feed-through and systemic control of sand flies (Diptera: Psychodidae). J Med Entomol. 50(1): 122–125.

Mondal D, Huda MM, Karmoker MK, Ghosh D, Matlashewski G, Nabi SG, Kroeger A (2013) Reducing visceral leishmaniasis by insecticide impreg- nation of bed-nets, Bangladesh. Emerg Infect Dis. 19(7): 1131–1134.

Moore EM, Lockwood DN (2010) Treat- ment of visceral leishmaniasis. J Glob Infect Dis. 2(2): 151–158.

Mubayi A, Castillo-Chavez C, Chowell G, Kribs-Zaleta C, Ali Siddiqui N, Kumar N, Das P (2010) Transmission dy- namics and underreporting of kala-azar in the Indian state of Bihar. J Theor Biol. 262(1): 177–185.

Mukhopadhyay AK, Saxena NBL, Narasim- ham MVVL, World Health Organiza- tion Division of Control of Tropical Diseases (1992) Susceptibility status of Phlebotomus argentipes to DDT in some kala-azar-endemic districts of Bihar, India. Available at: http://www. (Ac- cessed 26 March 2015).

NVBDCP (2014) National road map for ka- la-azar elimination. Available at: http:// pdf (Accessed 10 June 2015).

Ostyn B, Vanlerberghe V, Picado A, Dinesh DS, Sundar S, Chappuis F, Rijal S, Dujardin JC, Coosemans M, Boelaert M, Davies C (2008) Vector control by insecticide-treated nets in the fight against visceral leishmaniasis in the Indian subcontinent, what is the evi- dence? Trop Med Int Health. 13(8):1073–1085.

Perry D, Dixon K, Garlapati R, Gendernalik A, Poché D, Poché R (2013) Visceral leishmaniasis prevalence and associ- ated risk factors in the Saran district of Bihar, India from 2009 to July of 2011. Am J Trop Med Hyg. 88(4):778–784.

Picado A, Kumar V, Das M, Burniston I, Roy L, Suman R, Dinesh D, Coose-mans M, Sundar S, Shreekant K, Boe- laert M, Davies C, Cameron M (2009) Effect of untreated bed nets on blood- fed Phlebotomus argentipes in kala- azar endemic foci in Nepal and India. Mem Inst Oswaldo Cruz. 104(8):1183–1186.

Picado A, Das ML, Kumar V, Kesari S, Dinesh DS, Roy L, Rijal S, Das P, Rowland M, Sundar S, Coosemans M, Boelaert M, Davies CR (2010a) Effect of village-wide use of long-lasting in- secticidal nets on visceral leishmania- sis in India and Nepal: a cluster ran- domized trial. PLoS Negl Trop Dis.4(1): e587.

Picado A, Singh SP, Rijal S, Sundar S, Ostyn B, Chappuis F, Uranw S, Gid- wani K, Khanal B, Rai M, Paudel IS, Das ML, Kumar R, Srivastava P, Dujardin JC, Vanlerberghe V, Ander- sen EW, Davies CR, Boelaert M (2010b) Longlasting insecticidal nets for prevention of Leishmania donovani infection in India and Nepal: paired cluster randomised trial. BMJ. 29 (341): c6760.

Picado A, Ostyn B, Singh SP, Uranw S, Hasker E, Rijal S, Sundar S, Boelaert M, Chappuis F (2014) Risk factors for visceral leishmaniasis and asympto- matic Leishmania donovani infection in India and Nepal. PloS One. 9(1): e87641.

Poché D, Garlapati R, Ingenloff K, Remmers J, Poché R (2011) Bionomics of phlebotomine sand flies from three vil- lages in Bihar, India. J Vector Ecol.36(1): S106–117.

Poché RM, Garlapati R, Elnaiem DEA, Per- ry D, Poché D (2012) The role of Pal- myra palm trees (Borassus flabellifer) and sand fly distribution in northeastern India. J Vector Ecol. 37(1): 148–153.

Poché RM, Garlapati R, Singh MI, Poché DM (2013) Evaluation of fipronil oral

dosing to cattle for control of adult and larval sand flies under controlled con- ditions. J Med Entomol. 50(4): 833–837.

Rahman KM, Islam S, Rahman MW, Kenah E, Ghalib CM, Zahid MM, Maguire J, Rahman M, Haque R, Luby SP, Bern C (2010) Increasing incidence of post- kala-azar dermal leishmaniasis in a population-based study in Bangladesh. Clin Infect Dis. 50(1): 73–76.

Ramesh V, Mukherjee A (1995) Post-kala- azar dermal leishmaniasis. Int J Der- matol. 34(2): 85–91.

Ranjan A, Sur D, Singh VP, Siddique NA, Manna B, Lal CS, Sinha PK, Kishore K, Bhattacharya SK (2005) Risk fac- tors for India kala-azar. Am J Trop Med Hyg. 73(1): 74–78.

Sharma VP, Dhiman RC (1993) Neem oil as a sand fly (Diptera: Psychodidae) re- pellent. J Am Mosq Control Assoc.9(3): 364–366.

Sharma U, Singh S (2008) Insect vectors of Leishmania: distribution, physiology and their control. J Vector Borne Dis.45(4): 255–272.

Sharpe RM, Stewart D (2004) How strong is the evidence of a link between envi- ronmental chemicals and adverse ef- fects on human reproductive health? BMJ. 328(7437): 447–451.

Siddigui NA, Kumar N, Ranjan A, Pandey K, Das VN, Verma RB, Das P (2010) Awareness about kala-azar disease and related preventative attitudes and prac- tices in highly endemic rural area of India. Southeast Asian J Trop Med Public Health. 41(1): 1–12.

Singh R, Das RK, Sharma SK (2001) Re- sistance of sandflies to DDT in kala- azar endemic districts of Bihar, India. Bull World Health Org. 79(8): 793.

Singh SP, Reddy DC, Mishra RN, Sundar S (2006) Knowledge, attitude, and prac- tices related to kala-azar in rural area of Bihar state, India. Am J Trop Med Hyg. 75(3): 505–508.

Singh SP, Hasker E, Picado A, Gidwani K, Malaviya P, Singh RP, Boelaert M, Sundar S (2010) Risk factors for vis- ceral leishmaniasis in India: further ev- idence on the role of domestic animals. Trop Med Int Health. 15(S2): 29–35.

Singh RK, Mittal PK, Dhiman RC (2012) Insecticide susceptibility status of Phlebotomus argentipes, a vector of visceral leishmaniasis in different foci in three states of India. J Vector Borne Dis. 49(4): 254–257.

Sparling DW (2010) Ecotoxicology of Or- ganic Contaminants to Amphibians. In: Sparling DW, Linder G, Bishop CA, Krest SK (Eds) Ecotoxicology of Amphibians and Reptiles Vol. 2. CRC Press, New York, pp. 261–288.

Stauch A, Duerr HP, Picado A, Ostyn B, Sundar S, Rijal S, Boelaert M, Dujar- din JC, Eichner M (2014) Model-based investigations of different vector-re- lated intervention strategies to elimi- nate visceral leishmaniasis on the India subcontinent. PLoS Negl Trop Dis.

(4): e2810.

Stockdale L, Newton R (2013) A review of preventative methods against human leishmaniasis infection. PLoS Negl Trop Dis. 7(6): e2278.

Thakur CP (2000) Socio-economics of vis- ceral leishmaniasis in Bihar (India).Trans R Soc Trop Med Hyg. 94(2):156–157.

Thakur CP (2007) A new strategy for elimi- nation of kala-azar from rural Bihar. India J Med Res. 126(5): 447–451.

van den Berg H (2009) Global status of DDT and its alternatives for use in vector control to prevent disease. Envi- ron Health Perspect. 117(11): 1656–1663.

Wasserberg G, Poché R, Miller D, Chenault M, Zollner G, Rowton ED (2011) Im- idacloprid as a potential agent for the systemic control of sand flies. J Vec Ecol. 36(S1): 148–156.

WHO (2010) Control of the leishmaniases.

World Health Organization technical report series. Available at: http://

_eng.pdf (Accessed 22 March 2015). Wilson AL, Dhiman RC, Kitron U, Scott

TW, van den Berg H, Lindsay SW (2014) Benefit of insecticide-treated nets, curtains and screening on vector borne diseases, excluding malaria: a systematic review and meta-analysis. PLoS Negl Trop Dis. 8(10): e3228.

Wilson AL, Boelaert M, Kleinschmidt I, Pinder M, Scott TW, Tusting LS, Lindsay SW (2015) Evidence-based vector control? Improving the quality of vector control trials. Trends Parisi- tol. 31(8): 380–390.

How to Cite
Poché RM, Garlapati R. Measures to Control Phlebotomus argentipes and Visceral Leishmaniasis in India. J Arthropod Borne Dis. 10(2):113-126.
Review Article