Leishmania spp Infection in Patients and Great Gerbils (Rhombomys opimus) in a High-Risk Focus of Zoonotic Cutaneous Leishmaniasis in Central Iran: a Microscopic and Molecular Survey
-
Narges Marvi Moghadam
,
Mehdi Mohebali
,
Yavar Rassi
,
Ali Reza Zahraei-Ramazani
,
Mohammad Ali Oshaghi
,
Reza Jafari
,
Mahboubeh Fatemi
,
Mohammad Hossein Arandian
,
Hamid Abdoli
,
Nilufar Shareghi
,
Maryam Ghanei
,
Nilufar Jalali-Zand
,
Arshad Veysi
,
Javad Ramazanpoor
,
Kurosh Aminian
,
Ali Salehi
,
Ali Khamesipour
,
Amir Ahmad Akhavan
Abstract
Background: Zoonotic cutaneous leishmaniasis (ZCL) is an endemic disease in Varzaneh City where Leishmania major is the causative agent and the great gerbil, Rhombomys opimus, is the main reservoir host of the disease. Despite control efforts, ZCL outbreaks recur every few years. This study was conducted to revive information on the parasite/s species circulating between humans and the reservoirs in the region.
Methods: Leishmania infection in patients and R. opimus was studied using direct parasitological and molecular methods during 2019–2021. Nested-PCR and DNA sequencing were used for Leishmania parasite identification. Inter and intra-species variations in the Leishmania parasites were investigated using BLAST and MEGA7 software.
Results: All suspected patients (N=34) and 14 out of 36 great gerbils tested positive for Leishmania parasites via direct parasitological method. Nested-PCR method revealed all the patients were infected with L. major (94.1%) and mixed infection of L. major and Leishmania turanica (5.9%), and great gerbil specimens were infected with either L. major (44.4%), L. turanica (5.6%), or Leishmania gerbilli (5.6%) and also with mixed infection of L. major and L. turanica (30.5%), L. major and L. gerbilli (8.3%) and mix of all the three Leishmania species (5.6%).
Conclusion: The identical sequences of L. major in both human patients and rodents indicate that the great gerbils are the main reservoirs of L. major in Varzaneh City. The presence of L. turanica in patients would be of interest to carry out further studies to determine the role of this species in the persistence, signs, and treatment of ZCL in humans.
1. Sharifi I, Khosravi A, Mohammad Reza Af¬latoonian MR, Salarkia E, Bamorovat M, Karamoozian A, Nekoei Moghadam M, Sharifi F, Aghaei Afshar A, AghaKuchak Afshari S, Gharachorloo F, Shirzadi MR, Amiri B, Zainali M, Doosti S, Zamani O, Gouya MM (2023) Cutaneous leish¬man¬iasis situation analysis in the Islamic Re¬public of Iran in preparation for an elim¬ination plan. Front Public Health. 11: 1091709.
2. Razavi MR, Mohammad Reza Shirzadi MR, Mohebali M (2021) Human Cutaneous Leish¬maniosis in Iran, Up to Date-2019. J Arthropod-Borne Dis. 15(2): 143–151.
3. Karimi A, Jahanifard E, Abai MR, Rassi Y, Veysi A, Hanafi-Bojd AA, Hosseini M, Saeidi Z, Tavakoli M, Maleki M, Jafari R, Hejazi AR, Yaghoobi-Ershadi MR, Akha-van AA (2020) Epidemiological sur¬vey on Cutaneous Leishmaniasis in south-western Iran. J Vector Borne Dis. 57: 121–127.
4. Firooz A, Mortazavi H, Khamesipour A, Ghi¬asi M (2020) Old world cutaneous leish¬maniasis in Iran: clinical variants and treat¬ments. J Dermatolog Treat. 32(7): 673–683.
5. Rassi Y, Javadian E, Jalali M, Motazedian M, Vatndoost H (2004) Investigation on zoonotic cutaneous leishmaniasis, South-ern Iran. Iranian J Publ Health. 33(1): 31–35.
6. Fatemi M, Yaghoobi-Ershadi MR, Mohe-bali M, Saeidi Z, Veysi A, Gholampour F, Akhondi B, Karimi A, Arandian MH, Amin Mohammadi AM, Rassi Y, Zahraei-Ramazani A, Khamesipour A, Akhavan AA (2018) The potential role of humans in the transmission cycle of Leishmania major (Kinetoplastida: Trypanoso¬matida-e), the causative agent of the Old World zo¬onotic cutaneous leishmaniasis. J Med En¬tomol. 55(6): 1588–1593.
7. Jafari R, Najafzadeh N, Sedaghat M, Par-vizi P (2013) Molecular characterization of sand flies and Leishmania detection in main vector of zoonotic cutaneous leish-maniasis in Abarkouh District of Yazd Province, Iran. Asian Pac J Trop Med. 6 (10): 792–797.
8. Yaghoobi-Ershadi M (2012) Phlebotomine sand flies (Diptera: Psychodidae) in Iran and their role on Leishmania transmis¬sion. J Arthropod Borne Dis. 6(1): 1–17.
9. Yaghoobi-Ershadi MR, Akhavan AA (1999) Entomological survey of sandflies (Dip¬tera: Psychodidae) in a new focus of zo¬onotic cutaneous leishmaniosis in Iran. Acta Trop. 73(3): 321–326.
10. Yaghoobi-Ershadi MR, Javadian E, Tah-vil-dare-Bidruni GH (1994) The isolation of Leishmania major from Phlebotomus Paraph¬lebotomus) caucasicus in Isfahan Province, Islamic Republic of Iran. Trans R Soc Trop Med Hyg. 88: 518–519.
11. Akhavan AA, Yaghoobi-Ershadi MR, Mir¬hendi H, Alimohammadian M, Rassi Y, Shareghi N, Jafari R, Arandian MH, Abdoli H, Ghanei M, Jalali-Zand N (2010) Mo¬lecular epizootiology of rodent leish¬man¬iasis in a hyperendemic area of Iran. Iran J Public Health. 39(1): 1–7.
12. Kassiri H, Javadian E, Abdigoudarzi M (2011) Natural Leishmania Infection in Mer¬iones hurrianae and Tatera indica (Ro¬dentia: Cricetidae: Gerbillinae) in Sistan-Baluchistan Province, South–Eastern of Iran. Adv Stud Biol. 3(6): 247–256.
13. Dubrovsky Y (1979) Biology of great ger-bil-the principal carrier of zoonotic cuta-neous leishmaniasis. WHO Traveling Sem¬inar on leishmaniasis control ex-USSR Min¬istry of Health.
14. Akhavan AA, Yaghoobi-Ershadi MR, Khamesipour A, Mirhendi H, Alimoham-madian M, Rassi Y, Arandian MH, Jafari R, Abdoli H, Shareghi N, Ghanei M, Jalali-zand N (2010) Dynamics of Leish-mania infection rates in Rhombomys opi-mus (Rodentia: Gerbillinae) population of an endemic focus of zoonotic cutaneous leishmaniasis in Iran. Bull Soc Pathol Exot. 103(2): 84–89.
15. Hajjaran H, Mohebali M, Abai 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 zoon¬otic cutaneous leishmaniasis in northeast Iran. Trans R Soc Trop Med Hyg. 107(9): 550–557.
16. Bakhshi H, Oshaghi MA, Abai MR, Rassi Y, Akhavan AA, Mohebali M, Hajaran H, Mohtarami F, Mirzajani H, Maleki-Rav-asan N (2013) MtDNA cytb structure of Rhombomys opimus (Rodentia: Gerbelli-dae), the main reservoir of cutaneous leish¬maniasis in the borderline of Iran-Turk¬men¬istan. J Arthropod-Borne Dis. 7(2): 173–184.
17. Oshaghi MA, Rassi Y, Tajedin L, Abai MR, Akhavan AA, Enayati A, Mohtarami F (2011) Mitochondrial DNA diversity in the populations of great gerbils, Rhom-bomys opimus, the main reservoir of cu-taneous leishmaniasis. Acta Trop. 119(2–3): 165–171.
18. Gholamrezaei M, Mohebali M, Hanafi-Bojd AA, Sedaghat MM, Shirzadi MR (2016) Ecological Niche Modeling of main res¬ervoir hosts of zoonotic cutaneous leish¬maniasis in Iran. Acta Trop. 160: 44–52.
19. Yaghoobi-Ershadi MR, Akhavan AA, Mohe¬bali M (1996) Meriones libycus and Rhom¬bomys opimus (Rodentia: gerbillidae) are the main reservoir hosts in a newfocus of zoonotic cutaneous leishmaniasisin Iran. Trans R Soc Trop Med Hyg. 90: 503–504.
20. Golshani Asl F, Mohebali M, Jafari R, Akha¬van AA, Shirzadi MR, Zarei Z, Fadaei R, Ramezanpour J, Hassanpour Gh, Izadi Sh, Hajjaran H, Elikaee S (2022) Leishmania spp. infection in Rhombomys opimus and Meriones libycus as main reservoirs of zo¬onotic cutaneous leishmaniasis in cen¬tral parts of Iran: Progress and implica¬tions in health policy. Acta Trop. 226: 106267.
21. Darvish J (2011) Morphological compari-son of fourteen species of the genus Mer-iones Illiger (Rodentia: Gerbillinae) from Asia and North Africa. Iran J Anim Bio-syst. 7(1).
22. Veysi A, Vatandoost H, Yaghoobi-Er-shadi MR, Arandian M, Jafari R, Hosseini M, Rassi Y, Heidari K, Sadjadi A, Fadaei R, Ramazanpour J, Aminian K, Mr Shirzadi, Akhavan AA (2012) Comparative study on the effectiveness of Coumavec® and zinc phosphide in controlling zoonotic cu¬taneous leishmaniasis in a hyperendemic focus in central Iran. J Arthropod-Borne Dis. 6(1): 18–27.
23. Mohebali M, Nadim A, Khamesipour A
(2019) An overview of leishmanization ex¬perience: A successful control measure and a tool to evaluate candidate vaccines. Ac¬ta Trop. 200: 105173.
24. Alvar J, Croft SL, Kaye P, Khamesipour A, Sundar S, Reed SG (2010) Case study for a vaccine against leishmaniasis. Vac-cine. 31: B244-B249.
25. Etemad E (1978) Mammals of Iran, Vol. 1. Rodents and their Identification Keys. National Society of Guardianship of Nat-ural Resources and Human Environment, Tehran.
26. 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 (2020) Leishmania species: detection and identification by nested PCR assay from skin samples of rodent reservoirs. Exp Parasitol. 126(4): 552–556.
27. Kumar S, Stecher G, Tamura K (2016) Mo¬lecular evolutionary genetics analysis ver¬sion 7.0 for bigger datasets. Mol Biol Evol. 33(7): 1870–1874.
28. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 10(3): 512–526.
29. Bakhshi H, Oshaghi MA, Abai MR, Rassi Y, Akhavan AA, Sheikh Z, Mohtarami F, Saidi Z, Mirzajani H, Anjomruz M (2013) Molecular detection of Leishmania infec-tion in sand flies in border line of Iran-Turkmenistan: restricted and permissive vec¬tors. Exp Parasitol. 135(2): 382–387.
30. Nezamzadeh-Ezhiyeh H, Mirhendi H, Jafa¬ri R, Veysi A, Rassi Y, Oshaghi MA, Aran¬dian MH, Abdoli H, Bahrami S, Zahraei Ramazani AR, Fadaei R, Ramazanpoor J, Farsi M, Aminian K, Saeidi Z (2021) An eco-epidemiological study on zoonotic cu¬taneous leishmaniasis in central Iran. Iran J Public Health. 50(2): 350–359.
31. 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 vec¬tors and reservoir host in Iran. Vector Borne Zoonotic Dis. 11(2): 145–150.
32. Bordbar A, Parvizi P (2014) High infec-tion frequency, low diversity of Leishmania ma¬jor and first detection of Leishmania turanica in human in northern Iran. Acta Trop. 133: 69–72.
33. Strelkova MV (1996) Progress in studies on central asian foci of zoonotic cutane-ous. Folia Parasitol. 43: 1–6.
2. Razavi MR, Mohammad Reza Shirzadi MR, Mohebali M (2021) Human Cutaneous Leish¬maniosis in Iran, Up to Date-2019. J Arthropod-Borne Dis. 15(2): 143–151.
3. Karimi A, Jahanifard E, Abai MR, Rassi Y, Veysi A, Hanafi-Bojd AA, Hosseini M, Saeidi Z, Tavakoli M, Maleki M, Jafari R, Hejazi AR, Yaghoobi-Ershadi MR, Akha-van AA (2020) Epidemiological sur¬vey on Cutaneous Leishmaniasis in south-western Iran. J Vector Borne Dis. 57: 121–127.
4. Firooz A, Mortazavi H, Khamesipour A, Ghi¬asi M (2020) Old world cutaneous leish¬maniasis in Iran: clinical variants and treat¬ments. J Dermatolog Treat. 32(7): 673–683.
5. Rassi Y, Javadian E, Jalali M, Motazedian M, Vatndoost H (2004) Investigation on zoonotic cutaneous leishmaniasis, South-ern Iran. Iranian J Publ Health. 33(1): 31–35.
6. Fatemi M, Yaghoobi-Ershadi MR, Mohe-bali M, Saeidi Z, Veysi A, Gholampour F, Akhondi B, Karimi A, Arandian MH, Amin Mohammadi AM, Rassi Y, Zahraei-Ramazani A, Khamesipour A, Akhavan AA (2018) The potential role of humans in the transmission cycle of Leishmania major (Kinetoplastida: Trypanoso¬matida-e), the causative agent of the Old World zo¬onotic cutaneous leishmaniasis. J Med En¬tomol. 55(6): 1588–1593.
7. Jafari R, Najafzadeh N, Sedaghat M, Par-vizi P (2013) Molecular characterization of sand flies and Leishmania detection in main vector of zoonotic cutaneous leish-maniasis in Abarkouh District of Yazd Province, Iran. Asian Pac J Trop Med. 6 (10): 792–797.
8. Yaghoobi-Ershadi M (2012) Phlebotomine sand flies (Diptera: Psychodidae) in Iran and their role on Leishmania transmis¬sion. J Arthropod Borne Dis. 6(1): 1–17.
9. Yaghoobi-Ershadi MR, Akhavan AA (1999) Entomological survey of sandflies (Dip¬tera: Psychodidae) in a new focus of zo¬onotic cutaneous leishmaniosis in Iran. Acta Trop. 73(3): 321–326.
10. Yaghoobi-Ershadi MR, Javadian E, Tah-vil-dare-Bidruni GH (1994) The isolation of Leishmania major from Phlebotomus Paraph¬lebotomus) caucasicus in Isfahan Province, Islamic Republic of Iran. Trans R Soc Trop Med Hyg. 88: 518–519.
11. Akhavan AA, Yaghoobi-Ershadi MR, Mir¬hendi H, Alimohammadian M, Rassi Y, Shareghi N, Jafari R, Arandian MH, Abdoli H, Ghanei M, Jalali-Zand N (2010) Mo¬lecular epizootiology of rodent leish¬man¬iasis in a hyperendemic area of Iran. Iran J Public Health. 39(1): 1–7.
12. Kassiri H, Javadian E, Abdigoudarzi M (2011) Natural Leishmania Infection in Mer¬iones hurrianae and Tatera indica (Ro¬dentia: Cricetidae: Gerbillinae) in Sistan-Baluchistan Province, South–Eastern of Iran. Adv Stud Biol. 3(6): 247–256.
13. Dubrovsky Y (1979) Biology of great ger-bil-the principal carrier of zoonotic cuta-neous leishmaniasis. WHO Traveling Sem¬inar on leishmaniasis control ex-USSR Min¬istry of Health.
14. Akhavan AA, Yaghoobi-Ershadi MR, Khamesipour A, Mirhendi H, Alimoham-madian M, Rassi Y, Arandian MH, Jafari R, Abdoli H, Shareghi N, Ghanei M, Jalali-zand N (2010) Dynamics of Leish-mania infection rates in Rhombomys opi-mus (Rodentia: Gerbillinae) population of an endemic focus of zoonotic cutaneous leishmaniasis in Iran. Bull Soc Pathol Exot. 103(2): 84–89.
15. Hajjaran H, Mohebali M, Abai 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 zoon¬otic cutaneous leishmaniasis in northeast Iran. Trans R Soc Trop Med Hyg. 107(9): 550–557.
16. Bakhshi H, Oshaghi MA, Abai MR, Rassi Y, Akhavan AA, Mohebali M, Hajaran H, Mohtarami F, Mirzajani H, Maleki-Rav-asan N (2013) MtDNA cytb structure of Rhombomys opimus (Rodentia: Gerbelli-dae), the main reservoir of cutaneous leish¬maniasis in the borderline of Iran-Turk¬men¬istan. J Arthropod-Borne Dis. 7(2): 173–184.
17. Oshaghi MA, Rassi Y, Tajedin L, Abai MR, Akhavan AA, Enayati A, Mohtarami F (2011) Mitochondrial DNA diversity in the populations of great gerbils, Rhom-bomys opimus, the main reservoir of cu-taneous leishmaniasis. Acta Trop. 119(2–3): 165–171.
18. Gholamrezaei M, Mohebali M, Hanafi-Bojd AA, Sedaghat MM, Shirzadi MR (2016) Ecological Niche Modeling of main res¬ervoir hosts of zoonotic cutaneous leish¬maniasis in Iran. Acta Trop. 160: 44–52.
19. Yaghoobi-Ershadi MR, Akhavan AA, Mohe¬bali M (1996) Meriones libycus and Rhom¬bomys opimus (Rodentia: gerbillidae) are the main reservoir hosts in a newfocus of zoonotic cutaneous leishmaniasisin Iran. Trans R Soc Trop Med Hyg. 90: 503–504.
20. Golshani Asl F, Mohebali M, Jafari R, Akha¬van AA, Shirzadi MR, Zarei Z, Fadaei R, Ramezanpour J, Hassanpour Gh, Izadi Sh, Hajjaran H, Elikaee S (2022) Leishmania spp. infection in Rhombomys opimus and Meriones libycus as main reservoirs of zo¬onotic cutaneous leishmaniasis in cen¬tral parts of Iran: Progress and implica¬tions in health policy. Acta Trop. 226: 106267.
21. Darvish J (2011) Morphological compari-son of fourteen species of the genus Mer-iones Illiger (Rodentia: Gerbillinae) from Asia and North Africa. Iran J Anim Bio-syst. 7(1).
22. Veysi A, Vatandoost H, Yaghoobi-Er-shadi MR, Arandian M, Jafari R, Hosseini M, Rassi Y, Heidari K, Sadjadi A, Fadaei R, Ramazanpour J, Aminian K, Mr Shirzadi, Akhavan AA (2012) Comparative study on the effectiveness of Coumavec® and zinc phosphide in controlling zoonotic cu¬taneous leishmaniasis in a hyperendemic focus in central Iran. J Arthropod-Borne Dis. 6(1): 18–27.
23. Mohebali M, Nadim A, Khamesipour A
(2019) An overview of leishmanization ex¬perience: A successful control measure and a tool to evaluate candidate vaccines. Ac¬ta Trop. 200: 105173.
24. Alvar J, Croft SL, Kaye P, Khamesipour A, Sundar S, Reed SG (2010) Case study for a vaccine against leishmaniasis. Vac-cine. 31: B244-B249.
25. Etemad E (1978) Mammals of Iran, Vol. 1. Rodents and their Identification Keys. National Society of Guardianship of Nat-ural Resources and Human Environment, Tehran.
26. 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 (2020) Leishmania species: detection and identification by nested PCR assay from skin samples of rodent reservoirs. Exp Parasitol. 126(4): 552–556.
27. Kumar S, Stecher G, Tamura K (2016) Mo¬lecular evolutionary genetics analysis ver¬sion 7.0 for bigger datasets. Mol Biol Evol. 33(7): 1870–1874.
28. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 10(3): 512–526.
29. Bakhshi H, Oshaghi MA, Abai MR, Rassi Y, Akhavan AA, Sheikh Z, Mohtarami F, Saidi Z, Mirzajani H, Anjomruz M (2013) Molecular detection of Leishmania infec-tion in sand flies in border line of Iran-Turkmenistan: restricted and permissive vec¬tors. Exp Parasitol. 135(2): 382–387.
30. Nezamzadeh-Ezhiyeh H, Mirhendi H, Jafa¬ri R, Veysi A, Rassi Y, Oshaghi MA, Aran¬dian MH, Abdoli H, Bahrami S, Zahraei Ramazani AR, Fadaei R, Ramazanpoor J, Farsi M, Aminian K, Saeidi Z (2021) An eco-epidemiological study on zoonotic cu¬taneous leishmaniasis in central Iran. Iran J Public Health. 50(2): 350–359.
31. 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 vec¬tors and reservoir host in Iran. Vector Borne Zoonotic Dis. 11(2): 145–150.
32. Bordbar A, Parvizi P (2014) High infec-tion frequency, low diversity of Leishmania ma¬jor and first detection of Leishmania turanica in human in northern Iran. Acta Trop. 133: 69–72.
33. Strelkova MV (1996) Progress in studies on central asian foci of zoonotic cutane-ous. Folia Parasitol. 43: 1–6.
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How to Cite
1.
Marvi Moghadam N, Mohebali M, Rassi Y, Zahraei-Ramazani AR, Oshaghi MA, Jafari R, Fatemi M, Arandian MH, Abdoli H, Shareghi N, Ghanei M, Jalali-Zand N, Veysi A, Ramazanpoor J, Aminian K, Salehi A, Khamesipour A, Akhavan AA. Leishmania spp Infection in Patients and Great Gerbils (Rhombomys opimus) in a High-Risk Focus of Zoonotic Cutaneous Leishmaniasis in Central Iran: a Microscopic and Molecular Survey. J Arthropod Borne Dis. 2025;:253-263.
