First Report of Natural Infection of Phlebotomus mongolensis to Leishmania major and Leishmania turanica in the Endemic Foci of Zoonotic Cutaneous Leishmaniasis in Iran
-
Azad Absavaran
,
Mehdi Mohebali
,
Vahideh Moin-Vaziri
,
Alireza Zahraei-Ramazani
,
Amir Ahmad Akhavan
,
Sayena Rafizadeh
,
Amirhossein Rassi
,
Alireza Barmaki
,
Yavar Rassi
Abstract
Background: The primary aim of this study is to determine infection to Leishmania parasites in the wild population of Phlebotomus caucasicus and Phlebotomus mongolensis using molecular methods in some important zoonotic cutaneous leishmaniasis foci in Iran.
Methods: Sand flies were collected from active colonies of rodent burrows from 16 trapping sites using sticky trap paper. In order to detect and identify of Leishmania parasites in females Ph. caucasicus and Ph. mongolensis, the Nested–PCR amplification of ITS2-rDNA region was performed to generate amplicon with 245bp for Leishmania major, 206bp for L. gerbilli and 141bp for L. turanica.
Results: In the current study we found DNA of different gerbil parasites such as L. major and L. turanica, and mixed infection of L. major/L. turanica in Ph. caucasicus and Ph. mongolensis. It should be noted that, in Iran, natural infection with Leishmania parasites is recorded for the first time in this study in Ph. mongolensis.
Conclusion: Both species of Ph. caucasicus and Ph. mongolensis not only may participate in the ZCL transmission cycle between reservoir hosts, but also results of this study support the role of these species as secondary vectors in the transmission of leishmaniasis to humans.
1. Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, denBoer M (2012) WHO Leishmaniasis Control Team. Leishmaniasis Worldwide and Glob¬al Esti¬mates of Its Incidence. PLoS One. 7(5): e35671.
2. World Health Organization (2022) Leish-maniasis. WHO, Geneva, Switzerland. Avail¬able at: https://www.who.int/news-room/fact-sheets/detail/leishmaniasis
3. World Health Organization (2021) Leish-maniasis. WHO, Geneva, Switzerland. Avail¬able at: https://www.who.int/news-room/fact-sheets/detail/leishmaniasis
4. Yaghoobi-Ershadi MR, Akhavan AA, Shir-zadi MR, Hosseini SZ, Salomon OD, Hanaf-Bojd AA, Rassi Y (2021) A feasibility study on using the facilities of health centers for devel¬oping a laboratory network on vectors and reservoir hosts of cutaneous leishmaniasis in Iran. J Arthropod Borne Dis. 15(3): 255–264.
5. Maroli M, Feliciangeli MD, Bichaud L, Char¬rel RN, Gradoni L (2013) Phlebotomine sand flies and the spreading of leishmaniasis and other diseases of public health concern. Med Vet Entomol. 27(2): 123–147.
6. Galati EAB, Galvis-Ovallos F, Lawyer Ph, Léger N, Depaquit J (2017) An illustrated guide for characters and terminology used in descriptions of Phlebotominae (Diptera, Psy¬chodidae). Parasite. 24: 26.
7. Galati EAB (2018) Phlebotominae (Dip¬tera, Psychodidae): classification, morphology and terminology of adults and identification of American taxa. In: Rangel EF, Shaw J (Eds.): Brazilian sand flies, Spring¬er, Cham, pp. 9–212.
8. Yaghoobi-Ershadi MR (2012) Phlebotom-ine sand flies (Diptera: Psycodidae) in Iran and their role on Leishmania transmission. J Arthropod-Borne Dis. 6(1): 1–17.
9. Akhoundi M, Parvizi P, Baghaei A, De-paquit J (2012) The subgenus Adlerius Nitzules¬cu (Diptera, Psychodidae, Phleboto¬mus) in Iran. Acta Trop. 122: 7–15.
10. Zahraei-Ramazani AR, Kumar D, Yaghoobi-Ershadi MR, Naghian A, Jafari R, Shirzadi MR, Abdoli H, Soleimani H, Shareghi N, Ghanei M, Arandian MH, Hanafi-Bojd AA (2013) Sand flies of the sub¬genus Ad¬lerius (Diptera: Psychodidae) in an endem¬ic focus of visceral leishmaniasis and introduction of Phlebotomus (Adlerius) co¬matus as a new record for Iran. J Arthropod Borne Dis. 7(1): 1–7.
11. Karimi A, Hanafi-Bojd AA, Yaghoobi-Er-shadi MR, Akhavan AA, Ghezelbash Z (2014) Spatial and temporal distributions of phlebotomine sand flies (Diptera: Psy¬chodi¬dae), vectors of leishmaniasis, in Iran. Acta Trop. 132: 131–139.
12. Zahraei-Ramazani AR, Kumar D, Mir-hendi H, Sundar SH, Rajnikan M, Moin-Vaziri V, Soleimani H, Shirzadi MR, Jafari R, Hanafi-Bojd AA, Hamedi-Shahraky S, Yaghoobi-Ershadi MR (2015) Morphological and genotypic variations among the species of the subgenus Adlerius (Dip¬tera: Psychodidae, Phlebotomus) in Iran. J Arthropod Borne Dis. 9(1): 84–97.
13. Absavaran A, Mohebali M, Moin-Vaziri V, Zahraei-Ramazani A, Akhavan AA, Mozaf¬farian F, Rafizadeh S, Rassi Y (2019) Morphometric discrimination between fe¬males of two isomorphic sand fly species, Phlebotomus caucasicus and Phlebotomus mongolensis (Diptera: Phlebotom¬inae) in en¬demic and non-en-demic foci of zoonotic cu¬taneous leishmaniasis in Iran. Asian Pac J Trop Med. 12(4): 153–162.
14. Yaghoobi-Ershadi MR, Javadian E, Tah-vildari-Bidruni GH (1994) The isolation of Leishmania major from Phlebotomus (Paraphlebotomus) caucasicus in Esfahan Province, Islamic Republic of Iran. Trans R Soc Trop Med Hyg. 88: 518–519.
15. Es-Sette N, Ajaoud M, Laamrani-Idrissi A, Mellouki F, Lemrani M (2014) Molecular detection and identification of Leishmania infection in naturally infected sand flies in a focus of cutaneous leishmaniasis in northern Morocco. Parasit Vectors. 7: 305.
16. Akhavan AA, Mirhendi H, Khamesipour A, Alimohammadian MH, Rassi Y, Bates P, Kamhawi S, Valenzuela JG, Arandian MH, Abdoli H, Jalali-zand N, Jafari R, Shareghi N, Ghanei M, Yaghoobi-Er¬shadi MR (2010) Leishmania species: de¬tection and identifica¬tion by nested PCR assay from skin samples of rodent reservoirs. Exp. Parasitol. 126: 552–556.
17. Parvizi P, Ready PD (2008) Nested PCRs and sequencing of nuclear ITS-rDNA frag¬ments detect three Leishmania species of ger¬bils in sandflies from Iranian foci of zoonotic cutaneous leishmaniasis. Trop Med Int Health. 13(9): 1159–1171.
18. Rassi Y, Abai MR, Oshaghi MA, Javadian E, Sanei A, Rafdzadeh S, Arzamani K (2012) First detection of Leishmania infantum in Phlebotomus kandelakii using molecular methods in north-eastern Islamic Republic of Iran. East Mediterr Health J. 18(4): 387–392.
19. Azizi K, Abedi F, Moemenbellah-Fard MD (2012) Identification and frequency dis¬tribution of Leishmania (L.) major infections in sand flies from a new endemic ZCL focus in southeast Iran. Parasitol Res. 111:1821–1826.
20. Azizi K, Fakoorziba MR, Jalali M, Moemenbel¬lah-Fard MD (2012) First molecu¬lar detection of Leishmania major within nat¬urally infected Phlebotomus salehi from a zo¬onotic cutaneous leish¬maniasis focus in southern Iran. Trop Biomed. 29(1): 1–8.
21. Roshanghalb M, Parvizi P (2012) Isolat¬ing and determining Leishmania major and Leishmania turanica in Phlebotomus papatasi in Golestan Province. J Mazand
Univ Med Sci. 22: 74–83.
22. Azizi K, Badzohreh A, Sarkari B, Fakoo-rziba MR, Kalantari M, Moemenbellah-Fard MD, Ali-Akbarpour M (2013) Nested poly¬merase chain reaction and se¬quence-based detection of Leishmania in¬fection of sand flies in recently emerged endemic focus of zoonotic cutaneous leishmaniasis, southern Iran. Iran J Med Sci. 38(2): 156–162.
23. Bakhshi H, Oshaghi MA, Abai MR, Rassi Y, Akhavan AA, Sheikh Z, Mohtarami F, Saidi Z, Mirzanjani H, Anjomruz M (2013) Molecular detection of Leishmania infection in sand flies in border line of Iran–Turkmenistan: Restricted and per¬mis¬sive vec¬tors. Exp Parasitol. 135: 382–387.
24. Parvizi P, Alaeenovin E, Mohammadi S, Bagh¬ban N (2013) Occurrence of low density of Leishmania infantum in sandflies from a new focus of visceral leishmaniasis in north¬west of Iran. J Vector Borne Dis. 50: 127–132.
25. Oshaghi MA, Rassi Y, Hazratian T, Fallah E, Rafizadeh S (2013) Natural infection of wild caught Phlebotomus tobbi to Leishmania infantum in East Azerbaijan Province, north¬western Iran J Vector Borne Dis. 50: 24–29.
26. Rafizadeh S, Saraei M, Abai MR, Oshaghi MA, Mohebali M, Peymani A, Naserpour-Farivar T, Bakhshi H, Rassi Y (2016) Mo¬lecular detection of Leishmania major and L. turanica in Phlebotomus papa¬tasi and first natural infection of P. salehi to L. major in north-east of Iran. J Arthropod-Borne Dis. 10(2): 141–147.
27. Naghian A, Oshaghi MA, Moein-Vaziri V, Rassi Y, Sedaghat MM, Mostafavi E, Veysi A, Soleimani H, Dehghan H, Zahraei-Ramazani A, Mirhendi H, Amini MH, Yaghoobi-Ershadi MR, Akhavan AA (2020) Molecular identification of Leishmania spe¬cies in Phlebotomus alex¬andri (Diptera: Psy-chodidae) in western Iran. J Arthropod Borne Dis. 14(1): 8–16.
28. Theodor O, Mesghali A (1964) On the Phlebotomine of Iran. J Med Entomol. 1: 285–300.
29. Lewis DJ (1982) A taxonomic review of the genus Phlebotomus (Diptera: Psychodi¬dae). Bull Br Mus (Natural History). 45: 121–209.
30. Seyedi-Rashti MA, Nadim A (1992) The genus Phlebotomus (Diptera: Psychodidae: Phlebotominae) of the countries of the East¬ern Mediterrenean Region. Iran J Public Health. 21(1–4): 11–50.
31. Nadim A, Faghih M (1968) The epidemi-ology of cutaneous leishmaniasis in the Esfa¬han Province of Iran: I. The reservoirs. 11. The human disease. Trans R Soc Trop Med Hyg. 61: 534–542.
32. Nadim A, Seyedi-Rashti MA (1971) A brief review of the epidemiology of various types of leishmaniasis in Iran. Acta Medica Iranica. 14: 99–106.
33. Yaghoobi-Ershadi MR, Javadian E (1996) Seasonal variation of Leishmania major infec¬tion rates in sandflies from rodent burrows in Esfahan Province, Iran. Med Vet Entomol. 10: 181–184.
34. Nadim A, Mesghali A, Amini H (1968) Epidemiology of cutaneous leishmaniasis in the Esfahan Province of Iran III. The vector. Trans R Soc Trop Med Hyg. 62: 543–549.
35. Nadim A, Seyedi-Rashti MA, Mesgali A (1968) Epidemiology of cutaneous leish-mani¬asis in Turkemen Sahara Iran. J Trop Med Hyg. 71: 238–239.
36. Yaghoobi-Ershadi MR, Javadian E, Tah-vildari-Bidruni GH (1995) Leishmania major MON-26 isolated from naturally infected Phlebotomus papatasi (Diptera: Psychodidae) in Esfahan Province, Iran. Acta Trop. 59: 279–282.
37. Strelkova MV, Shurkhal AV, Kellina OI (1990) A new species of Leishmania iso-lated from the great gerbil Rhombomys opimus. Parasitol. 101: 327–335.
38. Guan LR, Yang YQ, Qu JQ, Shen WX
(1995) Discovery and study of Leishmania turanica for the first time in China. Bull World Health Organ. 73: 667–672.
39. Rassi Y, Abai MR, Javadian E, Rafizadeh S, Imamian H, Mohebali M, Fateh M, Haj¬jaran H, Ismaili K (2008) Molecular data on vectors and reservoir hosts of zoonotic cuta¬neous leishmaniasis in central Iran. Bull Soc Pathol Exot. 101(5): 425–428.
40. Artemiev MM (1978) Sandflies (Diptera, Psychodidae, Phlebotominae) of Afghan¬istan. Malaria and Leishmania Institute, Ministry of Public Health, Afghanistan, Kabul.
41. Strelkova MV, Eliseev LN, Ponirovsky EN, Dergacheva TI, Annacharyeva DK, Ero¬khin PI, Evans DA (2001) Mixed leishmanial infections in Rhombomys opi¬mus: a key to the persistence of Leishmania major from one transmission season to the next. Ann Trop Med Parasitol. 95: 811–819.
42. Perfil'ev PP (1968) Phlebotominae. Trans-lation of Perfil'ev, 1966 by Israel Program of Scientific Translations. Jerusalem.
43. Adler S, Theodor O (1957) Transmission of disease agents by phlebotomine sand flies. Annu Rev Entomol. 2: 203–226.
44. Strelkova MV (1996) Progress in studies on Central Asian foci of zoonotic cutaneous leishmaniasis: a review. Folia Par¬asitol. 43: 1–6.
45. Sergiev VP (1979) Epidemiology of leish-maniasis in the USSR. In: Lumsden WHR, Evans DA, editors. Biology of the Ki¬net¬oplastida. London: Academic Press, pp. 197–212.
46. Rassi Y, Oshaghi MA, Azani SM, Abai MR, Rafizadeh S, Mohebai M, Mohtarami F, Zeinali MK (2011) Molecular detection of Leishmania infection due to Leish¬mania ma¬jor and Leishmania turanica in the vectors and reservoir host in Iran. Vector-Borne Zoo Dis. 11: 145–150.
47. Yaghoobi-Ershadi MR, Javadian E (1996) Seasonal variation of Leishmania major infec¬tion rates in sandflies from rodent burrows in Esfahan Province, Iran. Med Vet Entomol. 10: 181-184.
48. Ready PD (2013) Biology of phlebotom-ine sandflies as vectors of disease agents. An¬nu Rev Entomol. 58: 227–250.
49. Killick-Kendrick R (1990) Phlebtomine vectors of the leishmaniases: a review. Med Vet Entomol. 4: 1–24.
50. Killick-Kendrick R (1999) The biology and control of phlebotomine sandflies. Clin Dermatol. 17: 279–289.
2. World Health Organization (2022) Leish-maniasis. WHO, Geneva, Switzerland. Avail¬able at: https://www.who.int/news-room/fact-sheets/detail/leishmaniasis
3. World Health Organization (2021) Leish-maniasis. WHO, Geneva, Switzerland. Avail¬able at: https://www.who.int/news-room/fact-sheets/detail/leishmaniasis
4. Yaghoobi-Ershadi MR, Akhavan AA, Shir-zadi MR, Hosseini SZ, Salomon OD, Hanaf-Bojd AA, Rassi Y (2021) A feasibility study on using the facilities of health centers for devel¬oping a laboratory network on vectors and reservoir hosts of cutaneous leishmaniasis in Iran. J Arthropod Borne Dis. 15(3): 255–264.
5. Maroli M, Feliciangeli MD, Bichaud L, Char¬rel RN, Gradoni L (2013) Phlebotomine sand flies and the spreading of leishmaniasis and other diseases of public health concern. Med Vet Entomol. 27(2): 123–147.
6. Galati EAB, Galvis-Ovallos F, Lawyer Ph, Léger N, Depaquit J (2017) An illustrated guide for characters and terminology used in descriptions of Phlebotominae (Diptera, Psy¬chodidae). Parasite. 24: 26.
7. Galati EAB (2018) Phlebotominae (Dip¬tera, Psychodidae): classification, morphology and terminology of adults and identification of American taxa. In: Rangel EF, Shaw J (Eds.): Brazilian sand flies, Spring¬er, Cham, pp. 9–212.
8. Yaghoobi-Ershadi MR (2012) Phlebotom-ine sand flies (Diptera: Psycodidae) in Iran and their role on Leishmania transmission. J Arthropod-Borne Dis. 6(1): 1–17.
9. Akhoundi M, Parvizi P, Baghaei A, De-paquit J (2012) The subgenus Adlerius Nitzules¬cu (Diptera, Psychodidae, Phleboto¬mus) in Iran. Acta Trop. 122: 7–15.
10. Zahraei-Ramazani AR, Kumar D, Yaghoobi-Ershadi MR, Naghian A, Jafari R, Shirzadi MR, Abdoli H, Soleimani H, Shareghi N, Ghanei M, Arandian MH, Hanafi-Bojd AA (2013) Sand flies of the sub¬genus Ad¬lerius (Diptera: Psychodidae) in an endem¬ic focus of visceral leishmaniasis and introduction of Phlebotomus (Adlerius) co¬matus as a new record for Iran. J Arthropod Borne Dis. 7(1): 1–7.
11. Karimi A, Hanafi-Bojd AA, Yaghoobi-Er-shadi MR, Akhavan AA, Ghezelbash Z (2014) Spatial and temporal distributions of phlebotomine sand flies (Diptera: Psy¬chodi¬dae), vectors of leishmaniasis, in Iran. Acta Trop. 132: 131–139.
12. Zahraei-Ramazani AR, Kumar D, Mir-hendi H, Sundar SH, Rajnikan M, Moin-Vaziri V, Soleimani H, Shirzadi MR, Jafari R, Hanafi-Bojd AA, Hamedi-Shahraky S, Yaghoobi-Ershadi MR (2015) Morphological and genotypic variations among the species of the subgenus Adlerius (Dip¬tera: Psychodidae, Phlebotomus) in Iran. J Arthropod Borne Dis. 9(1): 84–97.
13. Absavaran A, Mohebali M, Moin-Vaziri V, Zahraei-Ramazani A, Akhavan AA, Mozaf¬farian F, Rafizadeh S, Rassi Y (2019) Morphometric discrimination between fe¬males of two isomorphic sand fly species, Phlebotomus caucasicus and Phlebotomus mongolensis (Diptera: Phlebotom¬inae) in en¬demic and non-en-demic foci of zoonotic cu¬taneous leishmaniasis in Iran. Asian Pac J Trop Med. 12(4): 153–162.
14. Yaghoobi-Ershadi MR, Javadian E, Tah-vildari-Bidruni GH (1994) The isolation of Leishmania major from Phlebotomus (Paraphlebotomus) caucasicus in Esfahan Province, Islamic Republic of Iran. Trans R Soc Trop Med Hyg. 88: 518–519.
15. Es-Sette N, Ajaoud M, Laamrani-Idrissi A, Mellouki F, Lemrani M (2014) Molecular detection and identification of Leishmania infection in naturally infected sand flies in a focus of cutaneous leishmaniasis in northern Morocco. Parasit Vectors. 7: 305.
16. Akhavan AA, Mirhendi H, Khamesipour A, Alimohammadian MH, Rassi Y, Bates P, Kamhawi S, Valenzuela JG, Arandian MH, Abdoli H, Jalali-zand N, Jafari R, Shareghi N, Ghanei M, Yaghoobi-Er¬shadi MR (2010) Leishmania species: de¬tection and identifica¬tion by nested PCR assay from skin samples of rodent reservoirs. Exp. Parasitol. 126: 552–556.
17. Parvizi P, Ready PD (2008) Nested PCRs and sequencing of nuclear ITS-rDNA frag¬ments detect three Leishmania species of ger¬bils in sandflies from Iranian foci of zoonotic cutaneous leishmaniasis. Trop Med Int Health. 13(9): 1159–1171.
18. Rassi Y, Abai MR, Oshaghi MA, Javadian E, Sanei A, Rafdzadeh S, Arzamani K (2012) First detection of Leishmania infantum in Phlebotomus kandelakii using molecular methods in north-eastern Islamic Republic of Iran. East Mediterr Health J. 18(4): 387–392.
19. Azizi K, Abedi F, Moemenbellah-Fard MD (2012) Identification and frequency dis¬tribution of Leishmania (L.) major infections in sand flies from a new endemic ZCL focus in southeast Iran. Parasitol Res. 111:1821–1826.
20. Azizi K, Fakoorziba MR, Jalali M, Moemenbel¬lah-Fard MD (2012) First molecu¬lar detection of Leishmania major within nat¬urally infected Phlebotomus salehi from a zo¬onotic cutaneous leish¬maniasis focus in southern Iran. Trop Biomed. 29(1): 1–8.
21. Roshanghalb M, Parvizi P (2012) Isolat¬ing and determining Leishmania major and Leishmania turanica in Phlebotomus papatasi in Golestan Province. J Mazand
Univ Med Sci. 22: 74–83.
22. Azizi K, Badzohreh A, Sarkari B, Fakoo-rziba MR, Kalantari M, Moemenbellah-Fard MD, Ali-Akbarpour M (2013) Nested poly¬merase chain reaction and se¬quence-based detection of Leishmania in¬fection of sand flies in recently emerged endemic focus of zoonotic cutaneous leishmaniasis, southern Iran. Iran J Med Sci. 38(2): 156–162.
23. Bakhshi H, Oshaghi MA, Abai MR, Rassi Y, Akhavan AA, Sheikh Z, Mohtarami F, Saidi Z, Mirzanjani H, Anjomruz M (2013) Molecular detection of Leishmania infection in sand flies in border line of Iran–Turkmenistan: Restricted and per¬mis¬sive vec¬tors. Exp Parasitol. 135: 382–387.
24. Parvizi P, Alaeenovin E, Mohammadi S, Bagh¬ban N (2013) Occurrence of low density of Leishmania infantum in sandflies from a new focus of visceral leishmaniasis in north¬west of Iran. J Vector Borne Dis. 50: 127–132.
25. Oshaghi MA, Rassi Y, Hazratian T, Fallah E, Rafizadeh S (2013) Natural infection of wild caught Phlebotomus tobbi to Leishmania infantum in East Azerbaijan Province, north¬western Iran J Vector Borne Dis. 50: 24–29.
26. Rafizadeh S, Saraei M, Abai MR, Oshaghi MA, Mohebali M, Peymani A, Naserpour-Farivar T, Bakhshi H, Rassi Y (2016) Mo¬lecular detection of Leishmania major and L. turanica in Phlebotomus papa¬tasi and first natural infection of P. salehi to L. major in north-east of Iran. J Arthropod-Borne Dis. 10(2): 141–147.
27. Naghian A, Oshaghi MA, Moein-Vaziri V, Rassi Y, Sedaghat MM, Mostafavi E, Veysi A, Soleimani H, Dehghan H, Zahraei-Ramazani A, Mirhendi H, Amini MH, Yaghoobi-Ershadi MR, Akhavan AA (2020) Molecular identification of Leishmania spe¬cies in Phlebotomus alex¬andri (Diptera: Psy-chodidae) in western Iran. J Arthropod Borne Dis. 14(1): 8–16.
28. Theodor O, Mesghali A (1964) On the Phlebotomine of Iran. J Med Entomol. 1: 285–300.
29. Lewis DJ (1982) A taxonomic review of the genus Phlebotomus (Diptera: Psychodi¬dae). Bull Br Mus (Natural History). 45: 121–209.
30. Seyedi-Rashti MA, Nadim A (1992) The genus Phlebotomus (Diptera: Psychodidae: Phlebotominae) of the countries of the East¬ern Mediterrenean Region. Iran J Public Health. 21(1–4): 11–50.
31. Nadim A, Faghih M (1968) The epidemi-ology of cutaneous leishmaniasis in the Esfa¬han Province of Iran: I. The reservoirs. 11. The human disease. Trans R Soc Trop Med Hyg. 61: 534–542.
32. Nadim A, Seyedi-Rashti MA (1971) A brief review of the epidemiology of various types of leishmaniasis in Iran. Acta Medica Iranica. 14: 99–106.
33. Yaghoobi-Ershadi MR, Javadian E (1996) Seasonal variation of Leishmania major infec¬tion rates in sandflies from rodent burrows in Esfahan Province, Iran. Med Vet Entomol. 10: 181–184.
34. Nadim A, Mesghali A, Amini H (1968) Epidemiology of cutaneous leishmaniasis in the Esfahan Province of Iran III. The vector. Trans R Soc Trop Med Hyg. 62: 543–549.
35. Nadim A, Seyedi-Rashti MA, Mesgali A (1968) Epidemiology of cutaneous leish-mani¬asis in Turkemen Sahara Iran. J Trop Med Hyg. 71: 238–239.
36. Yaghoobi-Ershadi MR, Javadian E, Tah-vildari-Bidruni GH (1995) Leishmania major MON-26 isolated from naturally infected Phlebotomus papatasi (Diptera: Psychodidae) in Esfahan Province, Iran. Acta Trop. 59: 279–282.
37. Strelkova MV, Shurkhal AV, Kellina OI (1990) A new species of Leishmania iso-lated from the great gerbil Rhombomys opimus. Parasitol. 101: 327–335.
38. Guan LR, Yang YQ, Qu JQ, Shen WX
(1995) Discovery and study of Leishmania turanica for the first time in China. Bull World Health Organ. 73: 667–672.
39. Rassi Y, Abai MR, Javadian E, Rafizadeh S, Imamian H, Mohebali M, Fateh M, Haj¬jaran H, Ismaili K (2008) Molecular data on vectors and reservoir hosts of zoonotic cuta¬neous leishmaniasis in central Iran. Bull Soc Pathol Exot. 101(5): 425–428.
40. Artemiev MM (1978) Sandflies (Diptera, Psychodidae, Phlebotominae) of Afghan¬istan. Malaria and Leishmania Institute, Ministry of Public Health, Afghanistan, Kabul.
41. Strelkova MV, Eliseev LN, Ponirovsky EN, Dergacheva TI, Annacharyeva DK, Ero¬khin PI, Evans DA (2001) Mixed leishmanial infections in Rhombomys opi¬mus: a key to the persistence of Leishmania major from one transmission season to the next. Ann Trop Med Parasitol. 95: 811–819.
42. Perfil'ev PP (1968) Phlebotominae. Trans-lation of Perfil'ev, 1966 by Israel Program of Scientific Translations. Jerusalem.
43. Adler S, Theodor O (1957) Transmission of disease agents by phlebotomine sand flies. Annu Rev Entomol. 2: 203–226.
44. Strelkova MV (1996) Progress in studies on Central Asian foci of zoonotic cutaneous leishmaniasis: a review. Folia Par¬asitol. 43: 1–6.
45. Sergiev VP (1979) Epidemiology of leish-maniasis in the USSR. In: Lumsden WHR, Evans DA, editors. Biology of the Ki¬net¬oplastida. London: Academic Press, pp. 197–212.
46. Rassi Y, Oshaghi MA, Azani SM, Abai MR, Rafizadeh S, Mohebai M, Mohtarami F, Zeinali MK (2011) Molecular detection of Leishmania infection due to Leish¬mania ma¬jor and Leishmania turanica in the vectors and reservoir host in Iran. Vector-Borne Zoo Dis. 11: 145–150.
47. Yaghoobi-Ershadi MR, Javadian E (1996) Seasonal variation of Leishmania major infec¬tion rates in sandflies from rodent burrows in Esfahan Province, Iran. Med Vet Entomol. 10: 181-184.
48. Ready PD (2013) Biology of phlebotom-ine sandflies as vectors of disease agents. An¬nu Rev Entomol. 58: 227–250.
49. Killick-Kendrick R (1990) Phlebtomine vectors of the leishmaniases: a review. Med Vet Entomol. 4: 1–24.
50. Killick-Kendrick R (1999) The biology and control of phlebotomine sandflies. Clin Dermatol. 17: 279–289.
| Files | ||
| Issue | Vol 16 No 4 (2022) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v16i4.12086 | |
| Keywords | ||
| Leishmaniasis Phlebotomus caucasicus Phlebotomus mongolensis L. major and L. turanica Iran | ||
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How to Cite
1.
Absavaran A, Mohebali M, Moin-Vaziri V, Zahraei-Ramazani A, Akhavan AA, Rafizadeh S, Rassi A, Barmaki A, Rassi Y. First Report of Natural Infection of Phlebotomus mongolensis to Leishmania major and Leishmania turanica in the Endemic Foci of Zoonotic Cutaneous Leishmaniasis in Iran. J Arthropod Borne Dis. 2023;16(4):315–324.
