Susceptibility of Phlebotomus papatasi (Diptera: Psychodidae) against DDT and Deltamethrin in an Endemic Focus of Zoonotic Cutaneous Leishmaniasis in Iran
-
Amrollah Azarm
,
Hassan Vatandoost
,
Mona Koosha
,
Amir Ahmad Akhavan
,
Mehdi Mohebali
,
Zahra Saeidi
,
Awat Dehghan
,
Mohammad Ali Oshaghi
Abstract
Background: Phlebotomus papatasi (Diptera: Psychodidae) is the main vector of zoonotic cutaneous leishmaniasis (ZCL) in Iran. The nonstandard use of pesticides against pests, particularly in agriculture, indirectly has caused the development of resistance and, consequently, the threat of control measures in ZCL endemic areas. Up to 2023, several reports of resistance in Ph. papatasi have been declared in the old world. The purpose of this study was to measure the lethal time (LT50 and LT90) of Ph. papatasi sand flies in the ZCL endemic center of Esfahan to DDT and deltamethrin insecticides.
Methods: Sand flies were collected in Borkhar and were tested using WHO adult mosquito test kit against DDT 4% and deltamethrin 0.0002%. The sand fly’s survival was recorded during exposure time in 225, 450|, 900, 1800, and 3600-seconds’ intervals for DDT and Deltamethrin and they were allowed to recover for 24 hours. Then LT50 and LT90 were analyzed using probit software. Phlebotomus papatasi were identified using morphological keys and other sand flies’ species were excluded from the analysis.
Results: The insecticide against female Ph. papatasi revealed hundred percent mortality when exposed to DDT 4% and deltamethrin 0.0002%. The LT50 and LT90 were 19.32 and 22.74 minutes for DDT 4% and 39.92 and 51.33 minutes for deltamethrin 0.0002% respectively.
Conclusion: Results of this study revealed that Ph. papatasi is still susceptible to DDT and deltamethrin. This data provides valuable knowledge to implement effective control strategies against ZCL main vector and help to manage insecticide resistance in the region.
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19. Killick-Kendrick R, Leaney A, Peters W, Rioux J, Bray R (1985) Zoonotic cutaneous leishmaniasis in Saudi Arabia: the incrimination of Phlebotomus papatasi as the vector in the Al-Hassa Oasis. Trans R Soc Trop Med Hyg. 79(2): 252–255.
20. Jezek J, Tkoc M, Obona J, Manko P, van Harten A (2022) Subfamily Phlebotominae (Psychodidae, Diptera) of the United Arab Emirates–some new faunistic data. Acta Mus Siles Sci Natur. 71: 207–222.
21. Tabbabi A (2019) Review of leishmaniasis in the Middle East and North Africa. Afr Health Sci. 19(1): 1329–1337.
22. Hassan MaM, Widaa SO, Osman OM, Numiary MSM, Ibrahim MA, Abushama HM (2012) Insecticide resistance in the sand fly, Phlebotomus papatasi from Khartoum State, Sudan. Parasit Vectors. 5(1): 1–10.
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28. Singh R, Lal S, Saxena VK (2008) Breeding ecology of visceral leishmaniasis vector sandfly in Bihar state of India. Acta Trop. 107(2): 117–120.
29. Fawaz E, Zayed A, Fahmy N, Villinski J, Hoel D, Diclaro Jn (2016) Pyrethroid insecticide resistance mechanisms in the adult Phlebotomus papatasi (Diptera: Psychodidae). J Med Entomol. 53(3): 620–628.
30. Vatandoost H, Raeisi A, Saghafipour A, Nikpour F, Nejati J (2019) Malaria situation in Iran: 2002–2017. Malar J. 18(1): 1–7.
31. Theodor O, Mesghali A (1964) On the phlebotominae of Iran. J Med Entomol. 1(3): 285–300.
32. Lewis DJ (1982) A taxonomic review of the genus Phlebotomus (Diptera: Psychodidae). Syst Entomol. 1: 53–60.
33. Buchta JN, Zarndt BS, Garver LS, Rowland T, Shi M, Davidson SA, Rowton ED (2015) Blood-feeding behaviors of Anopheles stephensi but not Phlebotomus papatasi are influenced by actively warming guinea pigs (Cavia porcellus) under general anesthesia1. J Am Mosq Control Assoc. 31(2): 149–154.
34. Wilhelm TJ (2014) Visceral leishmaniasis. Chirurg. 90(10): 833–837.
35. Rassi Y, Asadollahi H, Abai MR, Kayedi MH, Vatandoost H (2020) Efficiency of two capture methods providing live sand flies and assessment the susceptibility status of Phlebotomus papatasi (Diptera: Psychodidae) in the foci of cutaneous leishmaniasis, Lorestan Province, western Iran. J Arthropod Borne Dis. 14(4): 408–415.
36. Balaska S, Fotakis EA, Chaskopoulou A, Vontas J (2021) Chemical control and insecticide resistance status of sand fly vectors worldwide. PLoS Negl Trop Dis. 15(8): e0009586.
37. Schlein Y, Jacobson R (1998) Resistance of Phlebotomus papatasi to infection with Leishmania donovani is modulated by components of the infective bloodmeal. Parasitol. 117(5): 467–473.
38. Ashraf F, Weedall GD (2022) Characterization of the glutathione S‐transferase genes in the sand flies Phlebotomus papatasi and Lutzomyia longipalpis shows expansion of the novel glutathione S‐transferase xi (X) class. Insect Mol Biol. 31(4): 417–433.
39. Faraj C, Ouahabi S, Adlaoui EB, El Elkohli M, Lakraa L, El Rhazi M, Ameur B (2012) Insecticide susceptibility status of Phlebotomus (Paraphlebotomus) sergenti and Phlebotomus (Phlebotomus) papatasi in endemic foci of cutaneous leishmaniasis in Morocco. Parasit Vectors. 5: 51.
40. Elnaiem D, Aboud M, Mubarek SE, Hassan H, Ward R (1999) Impact of pyrethroid‐impregnated curtains on Phlebotomus papatasi sandflies indoors at Khartoum, Sudan. Med Vet Entomol. 13(2): 191–197.
41. Fotakis EA, Giantsis IA, Demir S, Vontas JG, Chaskopoulou A (2018) Detection of pyrethroid resistance mutations in the major leishmaniasis vector Phlebotomus papatasi. J Med Entomol. 55(5): 1225–1230.
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2. Salimi M, Saghafipour A, Parsa HH, Khosravi M, Shirzadi MR (2019) Economic burden evaluation of cutaneous leishmaniasis in Iran. Shiraz E-Med J. 20(6): e82810.
3. Ahmadpour M, Varasteh Moradi H, Rezaei HR, Oshaghi MA, Hosseinzadeh Colagar A (2017) Modeling of the geographical distribution effects of great gerbil (Rhombomis opimus) on distribution of sandfly Phlebotomus papatasi in Golestan Province. J Anim Environ. 4: 73–80.
4. Ahmadpour M, Varasteh Moradi H, Rezaei HR, Oshaghi MA, Hapeman P, Hosseinzadeh Colagar A (2020) Genetic diversity and structure of the Great Gerbil, Rhombomys opimus, in Iran (Mammalia: Rodentia). Zool Middle East. 66(1): 1–12.
5. Hajjaran H, Mohebali M, Abaei MR, Oshaghi MA, Zarei Z, Charehdar S, Mirjalali H, Sharifdini M, Teimouri A (2013) Natural infection and phylogenetic classification of Leishmania spp. infecting Rhombomys opimus, a primary reservoir host of zoonotic cutaneous leishmaniasis in northeast Iran. Trans R Soc Trop Med Hyg. 107(9): 550–557.
6. Bakhshi H, Oshaghi M, Abai M, Rassi Y, Akhavan A, Sheikh Z, Mohtarami F, Saidi Z, Mirzajani H, Anjomruz M (2013) Molecular detection of Leishmania infection in sand flies in border line of Iran–Turkmenistan: restricted and permissive vectors. Exp Parasitol. 135(2): 382–387.
7. Rassi Y, Oshaghi MA, Azani SM, Abai MR, Rafizadeh S, Mohebai M, Mohtarami F, Zeinali MK (2011) Molecular detection of Leishmania infection due to Leishmania major and Leishmania turanica in the vectors and reservoir host in Iran. Vector Borne Zoonotic Dis. 11(2): 145–150.
8. Mollalo A, Sadeghian A, Israel GD, Rashidi P, Sofizadeh A, Glass GE (2018) Machine learning approaches in GIS-based ecological modeling of the sand fly Phlebotomus papatasi, a vector of zoonotic cutaneous leishmaniasis in Golestan Province, Iran. Acta Trop. 188: 187–194.
9. Yaghoobi-Ershadi M, Javadian E, Tahvildare-Bidruni G (1995) Leishmania major MON-26 isolated from naturally infected Phlebotomus papatasi (Diptera: Psychodidae) in Isfahan Province, Iran. Acta Trop. 59(4): 279–282.
10. Dhiman RC, Yadav RS (2016) Insecticide resistance in phlebotomine sandflies in Southeast Asia with emphasis on the Indian subcontinent. Infect Dis Poverty. 5(1): 106.
11. Flanley CM, Ramalho-Ortigao M, Coutinho-Abreu IV, Mukbel R, Hanafi HA, El-Hossary SS, Fawaz EEY, Hoel DF, Bray AW, Stayback G, Shoue DA, Kamhawi S, Karakuş M, Jaouadi K, Yaghoobie-Ershadi MR, Kruger A, Amro A, Kenawy MA, Dokhan MR, Warburg A, Hamarsheh O, McDowell MA (2018) Population genetics analysis of Phlebotomus papatasi sand flies from Egypt and Jordan based on mitochondrial cytochrome b haplotypes. Parasit Vectors. 11(1): 214.
12. Karmaoui A, Salem AB, Sereno D, El Jaafari S, Hajji L (2022) Geographic distribution of Meriones shawi, Psammomys obesus, and Phlebotomus papatasi the main reservoirs and principal vector of zoonotic cutaneous leishmaniasis in the Middle East and North Africa. Parasite Epidemiol Control. 17: e00247.
13. Trajer A, Hammer T, Padisak J (2018) Reflection of the Neogene–Quaternary phylogeography in the recent distribution limiting climatic factors of eight Mediterranean Phlebotomus species (Diptera: Psychodidae). J Nat His. 52(27-28): 1763–1784.
14. Maleki-Ravasan N, Oshaghi MA, Afshar D, Arandian MH, Hajikhani S, Akhavan AA, Yakhchali B, Shirazi MH , Rassi Y , Jafari R , Aminian K, Fazeli-Varzaneh RA, Durvasula R (2015) Aerobic bacterial flora of biotic and abiotic compartments of a hyperendemic Zoonotic Cutaneous Leishmaniasis (ZCL) focus. Parasit Vectors. 8(1): 1–22.
15. Oshaghi MA, Ravasan NM, Javadian E, Rassi Y, Sadraei J, Enayati AA, Zare Z, Emami SN (2009) Application of predictive degree day model for field development of sandfly vectors of visceral leishmaniasis in northwest of Iran. J Vector Borne Dis. 46(4): 247–255.
16. Kykalova B, Ticha L, Volf P, Loza Telleria E (2021) Phlebotomus papatasi antimicrobial peptides in larvae and females and a gut-specific defensin upregulated by Leishmania major infection. Microorganisms. 9(11): 2307.
17. Al-Obaidi MJ, Ibrahim K, Adnan T, Abd Al Hadi E, Akram E, Qazi Z (2013) Epidemiological study to investigate a possible vector of visceral leishmaniasis in the Central Region of Iraq. Al-Mustansiriyah J Sci. 26(6): 1–12.
18. Sofizadeh A, Rassi Y, Vatandoost H, Hanafi-Bojd AA, Mollalo A, Rafizadeh S, Akhavan AA (2017) Predicting the distribution of Phlebotomus papatasi (diptera: psychodidae), the primary vector of zoonotic cutaneous leishmaniasis, in Golestan province of Iran Using ecological niche modeling: comparison of MaxEnt and GARP models. J Med Entomol. 54(2): 312–320.
19. Killick-Kendrick R, Leaney A, Peters W, Rioux J, Bray R (1985) Zoonotic cutaneous leishmaniasis in Saudi Arabia: the incrimination of Phlebotomus papatasi as the vector in the Al-Hassa Oasis. Trans R Soc Trop Med Hyg. 79(2): 252–255.
20. Jezek J, Tkoc M, Obona J, Manko P, van Harten A (2022) Subfamily Phlebotominae (Psychodidae, Diptera) of the United Arab Emirates–some new faunistic data. Acta Mus Siles Sci Natur. 71: 207–222.
21. Tabbabi A (2019) Review of leishmaniasis in the Middle East and North Africa. Afr Health Sci. 19(1): 1329–1337.
22. Hassan MaM, Widaa SO, Osman OM, Numiary MSM, Ibrahim MA, Abushama HM (2012) Insecticide resistance in the sand fly, Phlebotomus papatasi from Khartoum State, Sudan. Parasit Vectors. 5(1): 1–10.
23. Kleinschmidt I, Bradley J, Knox TB, Mnzava AP, Kafy HT, Mbogo C, Ismail BA, Bigoga JD, Adechoubou A, Raghavendra K, Cook J, Malik EM, Nkuni ZJ, Macdonald M, Bayoh N, Ochomo E, Fondjo E, Awono-Ambene HP, Etang J, Akogbeto M, Bhatt RM, Chourasia MK, Swain DK, Kinyari T, Subramaniam K, Massougbodji A, Okê-Sopoh M, Ogouyemi-Hounto A, Kouambeng C, Abdin MS, West P, Elmardi K, Cornelie S, Corbel V, Valecha N, Mathenge E, Kamau L, Lines J, Donnelly MJ (2018) Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: a WHO-coordinated, prospective, international, observational cohort study. Lancet Infect Dis. 18(6): 640–649.
24. Shirani-Bidabadi L, Oshaghi MA, Enayati AA, Akhavan AA, Zahraei-Ramazani AR, Yaghoobi-Ershadi MR, Rassi Y, Aghaei-Afshar A, Koosha M, Arandian MH, Ghanei M, Ghassemi M, Vatandoost H (2022) Molecular and biochemical detection of insecticide resistance in the Leishmania vector, Phlebotomus papatasi (Diptera: Psychodidae) to dichlorodiphenyltrichloroethane and pyrethroids, in central Iran. J Med Entomol. 59(4): 1347–1354.
25. World Health Organization (2016) Monitoring and managing insecticide resistance in Aedes mosquito populations: interim guidance for entomologists. World Health Organization. Available at: https://apps.who.int/iris/handle/10665/204588.
26. World Health Organization (2016) Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. 2nd edition. Available at: https://apps.who.int/iris/bitstream/handle/10665/250677/ 9789241511575-eng.pdf
27. Kishore K, Kumar V, Kesari S, Dinesh D, Kumar A, Das P, Bhattacharya SK (2006) Vector control in leishmaniasis. Indian J Med Res. 123(3): 467–472.
28. Singh R, Lal S, Saxena VK (2008) Breeding ecology of visceral leishmaniasis vector sandfly in Bihar state of India. Acta Trop. 107(2): 117–120.
29. Fawaz E, Zayed A, Fahmy N, Villinski J, Hoel D, Diclaro Jn (2016) Pyrethroid insecticide resistance mechanisms in the adult Phlebotomus papatasi (Diptera: Psychodidae). J Med Entomol. 53(3): 620–628.
30. Vatandoost H, Raeisi A, Saghafipour A, Nikpour F, Nejati J (2019) Malaria situation in Iran: 2002–2017. Malar J. 18(1): 1–7.
31. Theodor O, Mesghali A (1964) On the phlebotominae of Iran. J Med Entomol. 1(3): 285–300.
32. Lewis DJ (1982) A taxonomic review of the genus Phlebotomus (Diptera: Psychodidae). Syst Entomol. 1: 53–60.
33. Buchta JN, Zarndt BS, Garver LS, Rowland T, Shi M, Davidson SA, Rowton ED (2015) Blood-feeding behaviors of Anopheles stephensi but not Phlebotomus papatasi are influenced by actively warming guinea pigs (Cavia porcellus) under general anesthesia1. J Am Mosq Control Assoc. 31(2): 149–154.
34. Wilhelm TJ (2014) Visceral leishmaniasis. Chirurg. 90(10): 833–837.
35. Rassi Y, Asadollahi H, Abai MR, Kayedi MH, Vatandoost H (2020) Efficiency of two capture methods providing live sand flies and assessment the susceptibility status of Phlebotomus papatasi (Diptera: Psychodidae) in the foci of cutaneous leishmaniasis, Lorestan Province, western Iran. J Arthropod Borne Dis. 14(4): 408–415.
36. Balaska S, Fotakis EA, Chaskopoulou A, Vontas J (2021) Chemical control and insecticide resistance status of sand fly vectors worldwide. PLoS Negl Trop Dis. 15(8): e0009586.
37. Schlein Y, Jacobson R (1998) Resistance of Phlebotomus papatasi to infection with Leishmania donovani is modulated by components of the infective bloodmeal. Parasitol. 117(5): 467–473.
38. Ashraf F, Weedall GD (2022) Characterization of the glutathione S‐transferase genes in the sand flies Phlebotomus papatasi and Lutzomyia longipalpis shows expansion of the novel glutathione S‐transferase xi (X) class. Insect Mol Biol. 31(4): 417–433.
39. Faraj C, Ouahabi S, Adlaoui EB, El Elkohli M, Lakraa L, El Rhazi M, Ameur B (2012) Insecticide susceptibility status of Phlebotomus (Paraphlebotomus) sergenti and Phlebotomus (Phlebotomus) papatasi in endemic foci of cutaneous leishmaniasis in Morocco. Parasit Vectors. 5: 51.
40. Elnaiem D, Aboud M, Mubarek SE, Hassan H, Ward R (1999) Impact of pyrethroid‐impregnated curtains on Phlebotomus papatasi sandflies indoors at Khartoum, Sudan. Med Vet Entomol. 13(2): 191–197.
41. Fotakis EA, Giantsis IA, Demir S, Vontas JG, Chaskopoulou A (2018) Detection of pyrethroid resistance mutations in the major leishmaniasis vector Phlebotomus papatasi. J Med Entomol. 55(5): 1225–1230.
42. Rashti MS, Panah HY, Mohamadi HS, Jedari M (1992) Susceptibility of Phlebotomus papatasi (Diptera: Psychodidae) to DDT in some foci of cutaneous leishmaniasis in Iran. J Am Mosq Control Assoc. 8(1): 99–100.
43. Yaghoobi-Ershadi MR, Moosa-Kazemi SH, Zahraei-Ramazani AR, Jalai-Zand A, Akhavan AA, Arandian M, Abdoli H, Houshmand B, Nadim A, Hosseini M (2006) Evaluation of deltamethrin-impregnated bed nets and curtains for control of zoonotic cutaneous leish-maniasis in. Bull Soc Pathol Exot. 99(1): 43–48.
44. Salim Abadi Y, Sanei-Dehkordi A, Hakimi Parizi M, Aghaei Afshar A, Sharifi I, Gorouhi MA, Shirani Bidabadi L, Alizadeh I (2022) Baseline susceptibility of a wild strain of main vectors of leishmaniasis to WHO-recommended insecticides in southeastern Iran. Parasit Vectors. 15(1): 42.
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| Files | ||
| Issue | Vol 17 No 4 (2023) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v17i4.15296 | |
| Keywords | ||
| Insecticide Phlebotomus papatas Susceptibilit Iran | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Azarm A, Vatandoost H, Koosha M, Akhavan A, Mohebali M, Saeidi Z, Dehghan A, Oshaghi M. Susceptibility of Phlebotomus papatasi (Diptera: Psychodidae) against DDT and Deltamethrin in an Endemic Focus of Zoonotic Cutaneous Leishmaniasis in Iran. J Arthropod Borne Dis. 2024;17(4):333–343.
