An Inventory of the Sand Flies (Diptera: Psychodidae) of Rudbar County, a New Focus of Leishmaniasis in Northern Iran, with a Taxonomic Note on the Subgenus Larroussius
AbstractBackground: Different forms of leishmaniasis are significant infectious diseases in Iran. While, Rudbar County of Guilan Province has been introduced as a new cutaneous leishmaniasis focus, there are few published data about the phlebotomine sand flies (Diptera: Psychodidae) of the province.Methods: To study the phlebotomine fauna of Rudbar County, the sampling was performed in 12 collection sites by light traps, sticky traps and manual aspirators throughout August–December 2015. Sand flies were removed from the sticky traps, rinsed in acetone and stored in 80% ethanol along with the collections of light traps and hand catches.Results: In total, 2186 sand flies were collected and ten species representing two genera were morphologically identified: Phlebotomus (Adlerius) halepensis (0.27%), Ph. (Larroussius) kandeladii (0.10%), Ph. (Lar.) neglectus (0.91%), Ph. (Lar.) perfiliewi (53.88%), Ph. (Lar.) tobbi (43.45%), Ph. (Paraphlebotomus) sergenti (0.82%), Ph. (Phlebotomus) papatasi (0.10%), Sergentomyia (Parrotomyia) baghdadis (0.27%), Se. (Sintonius) clydei (0.05%), Se. (Sin.) tiberiadis (0.10%). The species Ph. halepensis, Ph. neglectus, Ph. perfiliewi, Se. baghdadis, Se. clydei and Se. tiberiadis were reported for the first time in Guilan Province. This study also verified the presence of Ph. neglectus (Ph. major krimensis as a synonym and morphotype) in Iran. Moreover, the taxonomy of the subgenus Larroussius of the province was discussed.Conclusion: The prevalence of suspected or proven cutaneous and visceral leishmaniasis vectors is noteworthy. The study of ecology of sand flies and detecting the exact vectors of leishmaniasis and phlebotomine fever by molecular specific tests in Guilan Province are recommended.
2. Lane RP (1993) Sandflies (Phlebotom-inae). In: Lane RP, Crosskey RW (Eds) Med¬ical Insects and Arachnids. Chapman and Hall, London, pp. 78–119.
3. Ready PD (2013) Biology of phlebotom-ine sand flies as vectors of disease agents. Annu Rev Entomol. 58: 227–250.
4. Maroli M, Feliciangeli MD, Bichaud L, Charrel RN, Gradoni L (2013) Phlebotomine sandflies and the spread-ing of leishmaniases and other diseases of public health concern. Med Vet En-tomol. 27: 123–147.
5. Kasiri H, Javadian E, Seyedi-Rashti MA (2000) Check-list of Phlebotominae sand¬flies (Diptera: Psychodidae) of Iran. Bull Soc Pathol Exot. 93: 129–130 (French).
6. Javadian E, Mesghali A (1975) Check-list of phlebotomine sandflies (Diptera: Psy¬chodidae) of Iran. Bull Soc Pathol Exot. 68: 207–209.
7. Artemiev MM (1978) Sandflies (Diptera, Psychodidae, Phlebotominae) of Af-ghan¬istan. Malaria and Leishmania In-stitute, Ministry of Public Health, Af-ghanistan, Kabul.
8. Secombe AK, Ready PD, Huddleston LM (1993) A Catalogue of Old World Phlebotomine Sandflies (Diptera: Psy-chodidae, Phlebotominae). Occasional Pa¬pers on Systematic Entomology No. 8, The Natural History Museum, Lon-don.
9. Badakhshan M, Sadraei J, Moin-Vaziri V (2011) Morphometric and morphologi-cal variation between two different pop¬ulations of Phlebotomus major s.l. from endemic and non-endemic foci of visceral leishmaniasis in Iran. J Vector Ecol. 36: 153–158.
10. Akhoundi M, Parvizi P, Baghaei A, De-paquit J (2012) The subgenus Adlerius Nitzulescu (Diptera, Psychodidae, Phlebotomus) in Iran. Acta Trop. 122: 7–15.
11. Zahraei-Ramazani AR, Kumar D, Yaghoobi-Ershadi MR, Naghian A, Jafa¬ri R, Shirzadi MR, Abdoli H, So-leimani H, Shareghi N, Ghanei M, Arandian MH, Hanafi-Bojd AA (2013) Sand flies of the subgenus Adlerius (Diptera: Psy¬chodidae) in an endemic focus of vis¬ceral leishmaniasis and in¬troduction of Phlebotomus (Adlerius) comatus as a new record for Iran. J Ar¬thropod-Borne Dis. 7: 1–7.
12. Zahraei-Ramazani A, Kumar D, Mir-hendi H, Sundar S, Mishra R, Moin-Vaziri V, Soleimani H, Shirzadi MR, Jafari R, Hanafi-Bojd AA, Hamedi Shahraky S, Yaghoobi-Ershadi MR (2015) Morpho¬logical and genotypic variations among the species of the subgenus Adlerius (Diptera: Psychodi-dae, Phlebotomus) in Iran. J Arthro-pod-Borne Dis. 9: 84–97.
13. Saghafipour A, Rasi Y, Abai MR, Oshaghi MA, Farzinnia B (2011) Fau-na and month¬ly activity of sand flies at zoonotic cutaneous leishmaniasis focus in Qom¬rood District of Qom Province in 2009. Qom Univ Med Sci J. 5: 30–37 (Persian).
14. Yaghoobi-Ershadi MR (2012) Phlebotom¬ine sand flies (Diptera: Psy-chodidae) in Iran and their role on Leishmania trans¬mission. J Arthropod-Borne Dis. 6: 1–17.
15. Karimi A, Hanafi-Bojd AA, Yaghoobi-Ershadi MR, Akhavan AA, Ghezel-bash Z (2014) Spatial and temporal distribu¬tions of phlebotomine sand flies (Dip¬tera: Psychodidae), vectors of leishman¬iasis, in Iran. Acta Trop. 132: 131–139.
16. Moradi-Asl E, Rassi Y, Hanafi-Bojd AA, Saghafipour A (2019) Spatial dis-tribu¬tion and infection rate of leish-maniasis vectors (Diptera: Psychodi-dae) in Ar¬da¬bil Province, northwest of Iran. Asia Pac J Trop Biomed. 9: 181–187.
17. Killick-Kendrick R (1990) Phlebotomine vectors of the leishmaniases: a review. Med Vet Entomol. 4: 1–24.
18. Absavaran A, Rassi Y, Parvizi P, Oshaghi MA, Abaie MR, Rafizadeh S, Mohebali M, Zarea Z, Javadian E (2009) Iden¬ti¬fication of sand flies of the subgenus Larroussius based on molecular and mor¬phological charac-ters in northwestern Iran. Iran J Ar-thropod-Borne Dis. 9: 22–35.
19. Adler S, Theodor O, Lourie EM (1930) On sandflies from Persia and Palestine. Bull Entomol Res. 21: 529–539.
20. Mesghali A (1961) Phlbotominae (Dip-tera) of Iran. I. A preliminary list, de-scrip¬tion of species and their distribu-tional data. Acta Med Iran. 4: 20–73.
21. Ramezankhani R, Kaveh F (2014) Data and Statistics of Communicable Dis-ease during 1385–1390. Andishmand Press, Tehran (Persian).
22. Golchay J, Sadr Eshkevari SH, Darjani A (1992) Leishmania tropica in Guilan Province, report of 3 cases. J Med Coll, Guilan Univ Med Sci. 1: 46–50 (Persian).
23. Nadim A, Javadian E, Seyedi-Rashti MA (1994) Epidemiology of Leish-mani¬ases in Iran. In: Ardehali S, Re-zaei HR, Nadim A (Eds) Leishmania Parasite and Leishmaniases. 2nd Ed. University Press, Tehran, pp. 176–208 (Persian).
24. Majidi-Shad B, Torabzadeh MT, For-ghanparast K, Ebadati N (2005) Cuta-neous leishmaniasis in Rudbar area, Gui¬lan Province. The Fifth National Ira¬nian Congress of Parasitology (NICOPA 5). 15–17 November 2005, pp. 452–453 (Persian).
25. Saidi S (1974) Viral antibodies in pre-school children from the Caspian area, Iran. Iran J Publ Health. 3: 83–91.
26. Tesh R, Saidi S, Javadian E, Nadim A, Seyedi-Rashti MA (1976) The distri-bution and prevalence of human infec-tion with Phlebotomus fever group vi-ruses in Iran. Iran J Publ Health. 5: 1–7.
27. Tesh R, Saidi S, Gajdamovic SJ, Ro-dhain F, Vesenjak-Hirjan J (1976) Se-rological studies on the epidemiology of sandfly fever in the Old World. Bull WHO. 54: 663–674.
28. Seyedi-Rashti MA, Nadim A, Naficy A (1971) Further report on lizard leish-man¬iasis in northern part of Iran. J Trop Med Hyg. 74: 70–71.
29. Perfil’ev PP (1966) Fauna of U.S.S.R. Diptera. Phlebotomidae (Sandflies). Sci¬entific translation, Jerusalem (Rus-sian, translation in 1968).
30. Nadim A, Javadian E (1976) Key for species identification of sandflies (Phlebotom¬inae; Diptera) of Iran. Iran J Publ Health. 5: 33–44.
31. Lewis DJ (1982) A taxonomic review of the genus Phlebotomus. Bull Br Mus Nat Hist (Ent). 45: 121–209.
32. Seyedi Rashti MA, Nadim A (1992) The genus Phlebotomus (Diptera: Psycho-didae: Phlebotominae) of the countries of the Eastern Mediterranean Region. Iran J Publ Health. 21: 11–50.
33. Rassi Y, Hanafi-Bojd AA (2006) Phlebotomine Sandflies, Vectors of Leishmaniases. Noavaran-e-Elm, Teh-ran (Persian).
34. Léger N, Pesson B, Madulo-Leblond G, Abonnenc E (1983) About the differ-entiation of females from Larroussius s. gen. Nitzulescu, 1931 in the Medi-ter¬ranean region. Ann Parasitol Hum Comp. 58: 611–623 (French).
35. Killick-Kendrick R, Tang Y, Killick-Kendrick M, Sang DK, Sirdar MK, Ke L, Ashford RW, Schorscher J, Johnson RH (1991) The identification of female sandflies of the subgenus Larroussius by the morphology of the spermathecal ducts. Parassitologia. 33: 335–347.
36. Tischler W (1949) Grundzüge der ter-restrischen Tierökologie. Friedrich Vieweg, Braunschweig (German).
37. Heydemann B (1955) Die Frage der topog¬raphischen Übereinstimmung des Le¬bens¬raumes von Pflanzen- und Tierg¬esellschaften. Verh Dtsch Zool Ges Er¬langen. 19: 444–452 (German).
38. World Health Organization (1975) Man-ual on Practical Entomology in Malar-ia. Part II. Methods and Techniques. WHO, Geneva.
39. Tarallo VD, Dantas-Torres F, Lia RP, Ot¬ranto D (2010) Phlebotomine sand fly population dynamics in a leishman-iasis endemic peri-urban area in south-ern It¬aly. Acta Trop. 116: 227–234.
40. World Health Organization (2010) Con-trol of the leishmaniasis. WHO Tech Rep Ser, no. 949.
41. Rispail P, Dereure J, Jarry D (2002) Risk zones of human leishmaniases in the western Mediterranean basin. Correla-tions between vector sand flies, bio¬cli-matology and phytosociology. Mem Inst Oswaldo Cruz. 97: 477–483.
42. Mesghali A, Seyedi-Rashti MA, Nadim A (1967) Epidemiology of cutaneous leishmaniasis in Iran. Part II. Natural lep¬tomonad infection of sandflies in the Meshed and Lotfabad areas. Bull Soc Pathol Exot. 60: 514–518.
43. Oshaghi MA, Rasolian M, Shirzadi MR, Mohtarami F, Doosti S (2010) First re-port on isolation of Leishmania tropica from sandflies of a classical urban cu-taneous leishmaniasis focus in south¬ern Iran. Exp Parasitol. 126: 445–450.
44. Rassi Y, Oshaghi MA, Mohammadi Azani S, Abaie MR, Rafizadeh S, Mohebai M, Mohtarami F, Zeinali MK (2011) Mo¬lecular detection of Leish-mania infec¬tion due to Leishmania ma¬jor and Leish¬mania turanica in the vectors and res¬ervoir host in Iran. Vec-tor-Born Zo¬on¬otic Dis. 11: 145–150.
45. Nadim A, Javadian E, Tahvildar-Bidruni GH, Mottaghi M, Abaei MR (1992) Epidemiological- aspects of kala-azar in Meshkin-Shar, Iran: Investigation on vectors. Iran J Publ Health. 21: 61–72.
46. Rassi Y, Javadian E, Nadim A, Zahraii A, Vatandoost H, Motazedian H, Azizi K, Mohebali M (2005) Phlebotomus (Larroussius) kandelakii the principal and proven vector of visceral leish¬man¬iasis in north west of Iran. Pak J Biol Sci. 8: 1802–1806.
47. Sahabi Z, Seyedi Rashti MA, Nadim A, Javadian E, Kazemeini M, Abai MR (1992) A preliminary report on the nat-ural leptomonad infection of Phleboto-mus major in an endemic fo¬cus of vis-ceral leishmaniasis (VL) in Fars Prov-ince, south of Iran. Iran J Publ Health. 21: 87–93.
48. Azizi K, Rassi Y, Javadian E, Motazedi-an MH, Asgari Q, Yaghoobi-Ershadi MR (2008) First detection of Leishma-nia infantum in Phlebotomus (Lar¬rous-sius) major (Diptera: Psychodi¬dae) from Iran. J Med Entomol. 45: 726–731.
49. Sanei Dehkordi A, Rassi Y, Oshaghi MA, Abai MR, Rafizadeh S, Yaghoobi-Er¬shadi MR, Mohebali M, Zarei Z, Moh¬tarami F, Jafarzadeh B, Ranjbarkhah A, Javadian E (2011) Molecular detec¬tion of Leishmania in-fantum in natu¬rally infected Phleboto-mus perfiliewi transcaucasicus in Bile-savar District, northwestern Iran. Iran J Arthropod-Borne Dis. 5: 20–27.
50. Oshaghi MA, Rassi Y, Hazratian T, Fal-lah E, Rafizadeh S (2013) Natural in-fection of wild caught Phlebotomus tobbi to Leishmania infantum in East Azerbaijan Province, northwestern Iran. J Vector Borne Dis. 50: 24–29.
51. Moradi-Asl E, Hanafi-Bojd AA, Rassi Y, Vatandoost H, Mohebali M, Yaghoobi-Ershadi MR, Habibzadeh S, Hazrati S, Rafizadeh S (2017) Situa-tional analy¬sis of visceral leishmania¬sis in the most important endemic area of the disease in Iran. J Arthropod-Borne Dis. 11: 482–496.
52. Kassiri H, Jahanifard E (2012) First re-port on Sergentomyia sintoni and Ser-gentomyia clydei (Diptera: Psychodi-dae): their natural promastigote infec-tion and some aspects of biology in Sistan-Baluchistan Province, South-east¬ern Iran. Asian Pac J Trop Dis. 2: 370–373.
53. Akhoundi M, Mirzaei A, Baghaei A, Al-ten B, Depaquit J (2013) Sand fly (Dip¬tera: Psychodidae) distribution in the endemic and non-endemic foci of visceral leishmaniasis in northwestern Iran. J Vector Ecol. 38: 97–104.
54. Lewis DJ, Mesghali A, Djanbakhsh B (1961) Observations on phlebotomine sandflies in Iran. Bull WHO. 25: 203–208.
55. Theodor O, Mesghali A (1964) On the phlebotominae of Iran. J Med Ento-mol. 1: 285–300.
56. Artemiev MM, Neronov VM (1984) Dis-tribution and Ecology of Sand-flies of the Old World (Genus Phleboto¬mus). USSR Academy of Siences, Moscow (Russian).
57. Léger N, Pesson B (1987) Taxonomy and geographic distribution of Phleboto¬mus (Adlerius) chinensis s.l. and P. (Lar¬roussius) major s.l. (Psy-chodidae-Diptera). Status of species present in Greece. Bull Soc Pathol Ex-ot. 80: 252–260 (French).
58. Xiong G-H, Jin C-F (1987) On the clas-sification of subgenus Larroussius Nitzules¬cu, 1931 and Phlebotomus wui stat. nov. Journal of Parasitology and Parasitic Diseases of China. 5: 45–48 (Chi¬nese).
59. Leng Y-J, Lane RP, Lewis DJ (1987) The identification of two phlebotomine sandflies from Xinjian. Annual Bulle-tin of the Guangdong Society of Para-sitol¬ogy. 8–9: 40–43 (Chinese).
60. Perfil’ev PP (1969) 7. Family Phlebotomi¬dae. In: Bei-Bienko GYa (Ed) Keys to the Insects of the Europe¬an Part of the USSR. Volume V. Dip¬tera and Siphon¬aptera Part I. Nauka Publishers, Lenin¬grad, pp. 197–204 (Sharma BR, trans¬lator. Amerind Pub¬lishing Co., New Del¬hi, 1989) (Rus¬sian).
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.