Evaluation of Different Attractive Traps for Capturing Sand Flies (Diptera: Psychodidae) in an Endemic Area of Leishmaniasis, Southeast of Iran

  • Saideh Yousefi Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran, Sirjan School of Medical Sciences, Sirjan, Iran
  • Ali Reza Zahraei-Ramazani Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
  • Yavar Rassi Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
  • Hassan Vatandoost Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran, Department of Chemical Pollutants and Pesticide, Institute for Environmental Research, Tehran University of Medical Sciences, Tehran, Iran
  • Mohammad Reza Yaghoobi-Ershadi Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
  • Mohammad Reza Aflatoonian Research Center for Tropical and Infectious Diseases, Kerman University of Medical Sciences, Kerman, Iran
  • Amir Ahmad Akhavan Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
  • Abbas Aghaei-Afshar Leishmaniasis Research Center, Kerman University of Medical Sciences, Kerman, Iran
  • Masoumeh Amin Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
  • Azim Paksa Department of Parasitology, Faculty of Medicine, Tabriz University of Medical Science, Tabriz, Iran
Control; Leishmaniasis; Plant component; Chemicals; Iran


Background: The attraction of phlebotomine sand flies to plant and animal hosts is due to the produced chemical compounds, affecting the olfactory receptors of the insects. Therefore, novel and effective methods, such as Attrac­tive Toxic Sugar Baits (ATSB) and Attractive Toxic Baits (ATB), are based on the effective materials that attract sand flies toward the host. The present study was designed to identify the attractive materials in plants and animals for using in ATSB and ATB.Methods: This cross-sectional study was carried out in July 2018 on endemic areas of leishmaniasis in Iran. Differ­ent baits, including mango, nectarine, grape, banana, melon and watermelon, defibrinated blood of cattle, sheep, goat and chicken, urine of cattle, sheep, goat and ultimately, simple and complex chemicals, such as CO2, 1-octanol, lactic acid and human sweat were placed inside the traps, and the rate of  the sand flies attraction to these materials was studied. Furthermore, data were analyzed using the Kruskal-Wallis test and Mann Whitney U test.Results: There was a significant difference in the sand flies attraction between the traps containing watermelon, urine of cattle, and sheep, and chemicals such as CO2 and human sweat and the control trap (p< 0.05).Conclusion: This study showed that watermelon and CO2 are the potential candidates for using in ATSB and ATB, respectively.


1. Depaquit J, Grandadam M, Fouque F, Andry P, Peyrefitte C (2010) Arthropod-borne viruses transmitted by Phlebotomine sand flies in Europe: a review. Euro surveill. 15(10): e19507.
2. Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, Boer M (2012) WHO Leishmaniasis Control Team. Leishmaniasis worldwide and global estimates of its incidence. PloS One. 7(5): e35671.
3. Murray HW, Berman JD, Davies CR, Saravia NG (2005) Advances in leishmaniasis. The Lancet. 366(9496): 1561–1577.
4. Myler PJ, Fasel N (2008) Leishmania: af-ter the genome. Caister Academic Press, Norfolk, UK, p. 306.
5. Postigo JAR (2010) Leishmaniasis in the World Health Organization Eastern Mediterranean Region. Int J Antimi-crob Agent. 36: 62–65.
6. Aghaei-Afshar A, Rassi Y, Sharifi I, Vatandoost H, Mollaie H, Oshaghi MA, Abai MR, Rafizadeh S (2014) First report on natural Leishmania infection of Phlebotomus sergenti due Leishmania tropica by high resolution melting curve method in South-eastern Iran. Asian Pac J Trop Med. 7(2): 93–96.
7. Yaghoobi-Ershadi MR (2016) Control of phlebotomine sand flies in Iran: a review article. J Arthropod Borne Dis. 10(4): 429–444.
8. Sharifi I, Aflatoonian MR, Fekri AR, Hakimi-Parizi M, Aghaei-Afshar A, Khosravi A, Sharifi F, Aflatoonian B, Kha-mesipour A, Dowlati Y, Modabber F, Nadim A ( 2015) A comprehensive review of cutaneous leishmaniasis in Kerman Province, southeastern Iran. Narrative review article. Iran J Public Health. 44(3): 299–307.
9. Aflatoonian MR, Sharifi I (2010) Prevalence rate of cutaneous leishmaniasis in Bam district during 20 years (1988–2007). J Kerman Univ Med Sci. 17(4): 297–306.
10. Shamsi-Meymandi S, Zandi S, Aghaie H, Heshmatkhah A (2011) Efficacy of CO2 laser for treatment of anthroponotic cutaneous leishmaniasis, compared with combination of cryotherapy and intra lesional meglumine antimoniate. J Eur Acad Dermatol Venereol. 25(5): 587–591.
11. Aghaei-Afshar A, Vatandoost H, Sharifi I, Mollaie H, Oshaghi MA (2013) First determination of impact and outcome indicators following indoor residual spraying (IRS) with deltamethrin in a new focus of anthroponotic cutaneous leishmaniasis (ACL) in Iran. Asian Pac J Trop Dis. 3: 5–9.
12. World Health Organization (2010) Control of the leishmaniases: report of a meeting of the WHO Expert Commitee on the Control of Leishmaniases, Geneva, 22–26 March 2010.
13. Qualls WA, Müller GC, Khallaayoune K, Revay EE, Zhioua E, Kravchenko VD, Arheart KL, Xue RD, Schlein Y, Hausmann A, Kline DL (2015) Control of sand flies with attractive toxic sugar baits (ATSB) and potential impact on non-target organisms in Morocco. Parasite Vectors. 8(1): 87.
14. Sharma U, Singh S (2008) Insect vectors of leishmania distribution, physiology and their control. J Vector Borne Dis. 45(4): 255–272.
15. Saghafipour A, Vatandoost H, Zahraei-Ramazani AR, Yaghoobi-Ershadi MR, Rassi Y, Karami-Jooshin M, Shirzadi MR, Akhavan AA (2017) Control of zoonotic cutaneous leishmaniasis vector, Phlebotomus papatasi, using attractive toxic sugar baits (ATSB). PloS One. 12(4): e0173558.
16. Schlein Y, Müller GC (2010) Experimental control of Phlebotomus papatasi by spraying attractive toxic sugar Bait (ATSB) on the vegetation. Trans R Soc Trop Med Hyg. 104(12): 766–771.
17. Mboera LEG, Knols BGJ, Braks MAH, Takken W (2000) Comparison of carbon dioxide-baited trapping systems for sampling outdoor mosquito populations in Tanzania. Med Vet Entomol. 14(3): 257–263.
18. Braks MAH, Meijerink J, Takken W (2001) The response of the malaria mosquito, Anopheles gambiae, to two components of human sweat, ammonia and l-lactic acid, in an olfacto meter. Physiol Entomol. 26(2): 142–148.
19. Schmied WH, Takken W, Killeen GF, Knols BG, Smallegange RC (2008) Evaluation of two counter flow traps for testing behaviour mediating compounds for the malaria vector Anopheles gambiae s.s. under semi-field conditions in Tanzania. Malar J. 7: 230.
20. Jawara M, Smallegange RC, Jeffries D, Nwakanma DC, Awolola TS, Knols BGJ, Takken W, Conway DJ (2009) Optimizing odor-baited trap methods for collecting mosquitoes during the malaria season in the Gambia. PLoS One. 4(12): e8167.
21. Machado VE, Corrêa AG, Goulart TM, Rocha Silva FB, Ortiz DGS, Pinto MC (2015) Attraction of the sand fly Nys-somyia neivai (Diptera: Psychodidae) to chemical compounds in a wind tunnel. Parasit Vectors. 8: 147.
22. Mong’are S, Ng'ang'a Z, Ngumbi P, Johnstone I, Ngure P (2015) Comparative analysis of the effectiveness of sand fly traps with different baits. Int J Pharm Biol Sci. 10(4): 16–24.
23. Asadi A, Haghdoosti A, Malaki N (2011) Kerman Province-Country divisions. Farmandari publication, Kerman. In Persian.
24. Seyedi-Rashti MA, Nadim A (1992) The genus Phlebotomus (Diptera: Psychodidae: Phlebotominae) of the countries of the Eastern Mediterranean Region. Iranian J Publ Health. 21: 1–4.
25. Amora SS, Bevilaqua CM, Feijo FM (2009) Control of phlebotomine (Diptera: Psychodidae) leishmaniasis vectors. Neotrop Entomol. 38(3): 303–310.
26. World Health Organization (WHO) (2002) Impact of Olyset long-lasting nets to control transmission of anthroponotic cutaneous leishmaniasis in central Iran: Final Technical Report. WHO, Eastern Mediterranean Region. Project No. SGS04–76.
27. Saeidi Z, Vatandoost H, Akhavan AA, Yaghoobi‐Ershadi MR, Rassi Y, Sheikh Z, Arandian MH, Jafari R, Sanei-Dehkordi AR (2012) Baseline susceptibility of a wild strain of Phlebotomus papatasi (Diptera: Psychodidae) to DDT and py¬rethroids in an endemic focus of zoonotic cutaneous leishmaniasis in Iran. Pest Manag Sci. 68(5): 669–675.
28. Joshi AB, Bhatt LR, Regmi S, Ashford RW (2003) An assessment of the effectiveness of insecticide spray in the control of visceral leishmaniasis in Nepal. J Nepal Health Res Council. 1: 1–6.
29. Hotez P, Savioli L, Fenwick A (2012) Neglected tropical diseases of the Middle East and North Africa: Review of their prevalence, distribution, and opportuni¬ties for control. PLoS Negl Trop Dis. 6(2): e1475.
30. Müller GC, Junnila A, Schlein Y (2010) Effective control of adult Culex pipiens by spraying an attractive toxic sugar baits solution in the vegetation near larval de¬velop¬mental sites. J Med Entomol. 47 (1): 63–66.
31. Muller GC, Schlein Y (2011) Different methods of using attractive toxic sugar baits (ATSB) for the control of Phlebotomus papatasi. J Vector Ecol. 36(1): 64–70.
32. Beier JC, Muller GC, Gu W, Arheart KL, Schlein Y (2012) Attractive toxic sugar bait (ATSB) methods decimate population of Anopheles malaria vectors in arid environments regardless of the local availability of favored sugar-source. Malar J. 11: 31.
33. Müller GC, Schlein Y (2004) Nectar and honeydew feeding of Phlebotomus papatasi in a focus of Leishmania major in Neot-Hakikar oasis. J Vector Ecol. 29 (1): 154–158.
34. Schlein Y, Müller GC (1995) Assessment of plant tissue feeding by sand flies (Diptera: Psychodidae) and mosquitoes (Diptera: Culicidae). J Med Entomol. 32(6): 882–887.
35. Foster WA (2008) Phytochemicals as population sampling lures. J Am Mosq Control Assoc. 24(1): 138–146.
36. Van-Handel E, Haegar JS, Hansen CW (1972) The sugars of some Florida nec-tars. Am J Bot. 59(10): 1030–1032.
37. Müller GC, Beier JC, Traore SF, Toure MB, Traore MM, Bah S, Doumbia S, Schlein Y (2010) Successful field trial of attractive toxic sugar bait (ATSB) plant-spraying methods against malaria vectors in the Anopheles gambiae com-plex in Mali, West Africa. Mal J. 9: 210.
38. Müller GC, Schlein Y (2008) Efficacy of toxic sugar baits against adult cistern-dwelling Anopheles claviger. Trans R Soc Trop Med. 102(5): 480–484.
39. Naranjo DP, Qualls WA, Müller GC, Samson DM, Roque D, Alimi T, Arheart K, Beier JC, Xue RD (2013) Evaluation of boric acid baits against Aedes albopictus (Diptera: Culicidae) in tropical environments. Parasitol Res. 112 (4): 1583–1587.
40. Xue RD, Ali A, Kline DL, Barnard DR (2008) Field evaluation of boric acid and fipronil-based bait stations against adult mosquitoes. J Am Mosq Control Assoc. 24(3): 415–418.
41. Pinto MC, Campbell-Lendrum DH, Lo-zovei AL (2001) Phlebotomine sand fly re¬sponses to carbon dioxide and human odour in the field. Med Vet Entomol. 15(2): 132–139.
42. Moncaza A, Gebresilassieb A, Kirstein O, Faiman R, Gebre-Michaelc T, Hailud A, Warburga A (2013) Attraction of phlebotom¬ine sand flies to baited and non-baited horizontal surfaces. Acta Trop. 126(3): 205–210.
43. Veronesi E, Pilani R, Carrieri M, Bellini R (2007) Trapping sand flies (Diptera: Psy¬chodidae) in the Emilia-Romagna re¬gion of northern Italy. J Vector Ecol. 32(2): 313–318.
44. Orshan L, Szekely D, Khalfa Z, Bitton S (2010) Distribution and seasonality of Phlebotomus sand flies in cutaneous leish¬maniasis foci, Judean Desert, Is-rael. J Med Entomol. 47(3): 319–328.
45. Hesam-Mohammadi M, Rassi Y, Abai MR, Akhavan AA, Karimi F, Rafiza-deh S, Sanei-Dehkordi A, Sharafkhah M (2014) Efficacy of different sampling methods of sand flies (Diptera: Psycho¬didae) in endemic focus of cutaneous leishmaniasis in Kashan District, Isfahan Province, Iran. J Arthropod Borne Dis. 8(2): 156–162.
46. Kravchenko V, Wasserberg G, Warburg A (2004) Bionomics of Phlebotomine sand flies in the Galilee focus of cuta-neous leishmaniasis in northern Israel. Med Vet Entomol. 18(4): 418–428.
47. Enrih M, Stjepan K, Mirta SB, Zeljka J (2007) Response of mosquitoes to dif-ferent synthetic and natural olfactory at¬tractants (Diptera: Culicidae). Entomol Gener. 30(4): 253–261.
48. Keweka EJ, Owini EA, Mwang’onde BJ, Mahande AM, Nyindo M, Mosha F (2011) The role of cow urine in the ovi¬posi¬tion site preference of Culicine and Anophe¬les mosquitoes. Parasit Vec¬tors. 4: 184.
How to Cite
Yousefi S, Zahraei-Ramazani AR, Rassi Y, Vatandoost H, Yaghoobi-Ershadi MR, Aflatoonian MR, Akhavan AA, Aghaei-Afshar A, Amin M, Paksa A. Evaluation of Different Attractive Traps for Capturing Sand Flies (Diptera: Psychodidae) in an Endemic Area of Leishmaniasis, Southeast of Iran. J Arthropod Borne Dis. 14(2):202–213.
Original Article