PCR Positivity of Gerbils and Their Ectoparasites for Leishmania Spp. in a Hyperendemic Focus of Zoonotic Cutaneous Leishmaniasis in Central Iran
-
Sahar Azarmi
,
Alireza Zahraei-Ramazani
,
Mehdi Mohebali
,
Yavar Rassi
,
Amir Ahmad Akhavan
,
Amrollah Azarm
,
Omid Dehghan
,
Samira Elikaee
,
Rahimeh Abdoli
,
Mohsen Mahmoudi
Abstract
Background: Various arthropods, including Rhipicephalus sanguineus and Ctenocephalides felis felis have been suggested as secondary vectors of Leishmania spp. many years ago. This study was conducted to determine zoonotic cutaneous leishmaniasis (ZCL) PCR positivity of reservoir hosts and their ectoparasites for Leishmania spp. in Segzi plain in Esfahan Province from October 2016 to October 2017.
Methods: Microscopic examination and nested PCR were used to detect and identify Leishmania spp. isolated from rodents' ear and ectoparasites, and then, the results were confirmed by two methods, PCR-restriction fragment length polymorphism and sequencing.
Results: Totally, 93 rodents (92 Rhombomys opimus and one Nesokia indica) and nine different species of ectoparasites (n=527) including fleas, mites, and ticks were collected during different seasons in the study area. Fourteen R. opimus were positive for Leishmania spp. by microscopic examination while one N. indica and 77 R. opimus were positive by nested PCR. The infection rate of rodents with Leishmania major and L. turanica was 39.79% (n=37) and 15.05% (n=14), respectively. Mixed natural infections with L. major and L. turanica were seen in rodents. Moreover, 72.22% of fleas (39/54), 75.0% of mites (5/8), and 100% of tick nymph (1/1) were PCR positive for Leishmania parasites.
Conclusions: The highest rate of infection with L. major and L. turanica in R. opimus populations was observed in summer and spring, respectively. It is suggested that the role of L. turanica and the probable role of ectoparasites in the epidemiology of disease should be investigated. A Xenodiagnostic test is recommended for future study.
1. 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: Ger¬bellidae), the Main Reservoir of Cuta¬ne¬ous Leishmaniasis in the Borderline of Iran-Turkmenistan. J Arthropod Borne Dis. 7(2): 173–184.
2. Norouzi B, Hanafi-Bojd AA, Moin-Vaziri V, Noorallahi A, Azari-Hamidian S (2020) 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. J Arthropod-Borne Dis. 14 (3): 302–316.
3. Ghatee MA, Taylor WR, Karamian M (2020) The geographical distribution of cuta¬ne¬ous leishmaniasis causative agents in Iran and its neighboring countries, a review. Front Public Health. 8: 11.
4. Owens SD, Oakley DA, Marryott K, Hatchett W, Walton R, Nolan TJ, Newton A, Steurer F, Schantz P, Giger U (2001) Transmission of visceral leishmaniasis through blood transfusions from infected English foxhounds to anemic dogs. J Amer¬ican Vet Med Ass. 219(8): 1076–1083.
5. Coutinho MTZ, Bueno LL, Sterzik A, Fu-jiwara RT, Botelho JR, De Maria M, Ge-naro O, Linardi PM (2005) Participation of Rhipicephalus sanguineus (Acari: Ix-odidae) in the epidemiology of canine vis¬ceral leishmaniasis. Vet Parasitol. 128 (1–2): 149–155.
6. McKenzie KK (1984) Study of the Trans-mission of Canine Leishmaniasis by the Tick, Rhipicephalus Sanguineus (Latreil-le) and an Ultrastructural Comparison of the Promastigotes. [PhD dissertation], Ok¬lahoma State University, Stillwater.
7. Ferreira MGPA, Fattori KR, Souza F, Lima VMF (2009) Potential role for dog fleas in the cycle of Leishmania spp. Vet par-asitol. 165(1–2): 150–154.
8. Leishmaniasis (Cutaneous and Visceral) (2017) Center for Food Security and Pub¬lic Health. Available at: www.cfsph.iastate.edu/Factsheets/pdfs/leishmaniasis.pdf.
9. Friedhoff K (1990) Interaction between par¬asite and tick vector. Int J Parasitol. 20 (4): 525–535.
10. Dantas-Torres F, Figueredo LA, Brandão-Filho SP (2006) Rhipicephalus san-guineus (Acari: Ixodidae), the brown dog tick, par¬asitizing humans in Brazil. Rev Soc Bra¬sileira Med Trop. 39(1): 64–67.
11. Sherlock I (1964) Nota sobre a trans¬mis-são da leishmaniose visceral no Brasil. Rev Brasileira Malariol. 16: 19–26.
12. Rey L (2001) Parasitologia: parasitos e doen¬ças parasitárias do homem nas Américas e na África / Parasitology: parasites and men parasitology diseases in America and Africa. 3rd ed. Guanabara Koogan, Rio de Janeiro.
13. Coutinho MTZ, Linardi PM (2007) Can fleas from dogs infected with canine vis-ceral leishmaniasis transfer the infection to other mammals? Vet parasitol. 147 (3–4): 320–325.
14. Flecknell P (2009) Laboratory animal an-aesthesia. 3rd ed. Academic Press.
15. Asmar M, Piazak N, Karimi Y (1979) Fleas, Identification keys of Fleas of Iran and Introduction-Hosts-Geografic Distribu¬tion. Pasteur Inst Iran [in Per-sian].
16. Walker AR, Bouattour A, Camicas JL, Es-trada-Peña A, Horak IG, Latif AA, Pe-gram RG, Preston PM (2003) Ticks of domestic animals in Africa: a guide to identification of species. Bioscience Re-ports, Edinburgh.
17. Pratt HD (2013) Anoplura: Pictoral key to some species on domestic rats in south-ern United States. Available at: https://www.cdc.gov/nceh/ehs/docs/pictorial_keys/lice-anoplura.pdf.
18. Mašán P, Fenďa P (2010) A Review of the Laelapid Mites Associated with Terres-trial Mammals in Slovakia, with a Key to the European Species (Acari: Meso-stigmata: Dermanyssoidea). Institute of Zoology, Slovak Academy of Sciences, Bratislava.
19. Etemad E (1978) Mammals of Iran, Ro-dents and their identification Keys. Na-tional Society of Guardianship of Nat-ural Resources and Human En¬viron-ment, Tehran [in Persian].
20. Akhavan AA, Mirhendi H, Khamesipour A, Alimohammadian MH, Rassi Y, Bates P, Kamhawi Sh, Valenzuela JG, Aran¬dian MH, Abdoli H, Jalili-Zand N, Jafari R, Shareghi N, Ghanei M, Yaghoobi-Er¬shadi MR (2010) Leishmania species: de¬tection and identification by nested PCR assay from skin samples of rodent res¬ervoirs. Exp Parasitol. 126(4): 552–556.
21. Akhavan AA, Yaghoobi-Ershadi MR, Khamesipour A, Mirhendi H, Alimo-ham¬madian M, Rassi Y, Arandian MH, Jafa¬ri R, Abdoli H, Shareghi N, Ghanei M, Jalili-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.
22. 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.
23. Jihene B, Meriam N (2017) Epidemiology of cutaneous leishmaniasis in Tunisia. In: Claborn D (Ed): The Epidemiology and Ecology of Leishmaniasis, Vol. 1. InTech, Croatia, pp. 79–91.
24. 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 in¬fec¬tion in sand flies in border line of Iran-Turkmenistan: restricted and permissive vectors. Exp Parasitol. 135(2): 382–387.
25. Strelkova MV (1996) Progress in studies on central asian foci of zoonotic cutaneous. Folia Parasitol. 43: 1–6.
26. Strelkova M, Eliseev L, Ponirovsky E, Derga¬cheva T, Annacharyeva D, Ero-khin P, Evans DA (2001) Mixed leishmanial infections in Rhombomys opimus: a key to the persistence of Leishmania major from one transmission season to the next. Ann Trop Med Parasitol. 95(8): 811–819.
27. Randall JA, Rogovin K, Parker PG, Eimes JA (2005) Flexible social structure of a desert rodent, Rhombomys opimus: philo¬patry, kinship, and ecological con-straints. Behav Ecol. 16(6): 961–973.
28. Zahraei-Ramazani A, Saghafipour A, Sed-aghat M, Absavaran A, Azarm A (2017) Molecular Identification of Phlebotomus caucasicus and Phlebotomus mon¬go¬len-sis (Diptera: Psychodidae) in a Hyperen-demic Area of Zoonotic Cutaneous Leish¬maniasis in Iran. J Med Entomol. 54(6): 1525–1530.
29. Doroodgar A, Sadr F, Razavi MR, Do-rood¬gar M, Asmar M, Doroodgar M (2015) A new focus of zoonotic cutaneous leish¬maniasis in Isfahan Province. Central Iran. Asian Pac J Trop Dis. 5: 54–58.
30. Blanc G, Caminopetros J (1930) Trans¬mis-sion of Mediterranean EA by a Tick. Compte Rendu de l'Academie des Sci-ences. 191(23): 1162–1164.
31. Otranto D, Dantas-Torres F (2010) Fleas and ticks as vectors of Leishmania spp. to dogs: caution is needed. Vet Parasitol. 168(1–2): 173–174.
32. Azarm A (2015) Molecular identification of dog fleas and study on the possibility of contamination of them with visceral leishmaniasis agent in Meshkinshar city. [A Thesis for MSc degree]. School of Med¬ical Sciences, Tarbiat Modares Uni-versity.
33. Khokhlova IS, Serobyan V, Krasnov BR, Degen AA (2009) Effect of host gender on blood digestion in fleas: mediating role of environment. Parasitol Res. 105 (6): 1667–1673.
34. Colombo FA, Odorizzi RM, Laurenti MD, Galati EA, Canavez F, Pereira-Chioc¬cola VL (2011) Detection of Leishmania (Leishmania) infantum RNA in fleas and ticks collected from naturally infected dogs. Parasitol Res. 109(2): 267–274.
35. Viol MA, Guerrero FD, de Oliveira BCM, de Aquino MCC, Loiola SH, de Melo GD, de Souza Gomes SH, Kanamura CT, Garcia MV, Adreotti R, de Lima VMF, Bresciani KDS (2016) Identification of Leishmania spp. promastigotes in the in¬testines, ovaries, and salivary glands of Rhipicephalus sanguineus actively in¬fest¬ing dogs. Parasitol Res. 115(9): 3479–3484.
36. Bilgic HB, Bakirci S, Kose O, Aksulu A, Hacilarlioglu S, Karagenc T (2016) De-termination the role of Rhipicephalus san¬guineus for transmission of Leishmania major to reservoir animals. Turkiye Parazitol Derg. 40: 179–184.
37. Rakhshanpour A, Malmasi A, Mohebali M, Nabian S, Mirhendi H, Zarei Z, Dalimi A, Mohammadiha A, Akhoundi B, Azarm A (2017) Transmission of Leishmania in¬fantum by Rhipicephalus sanguineus (Ac¬ari: Ixodidae) in dogs. Iran J Parasitol. 12(4): 482–489.
38. Dantas-Torres F (2011) Ticks as vectors of Leishmania parasites. Trends para¬si¬tol. 27(4): 155–159.
39. Tajedin L, Rassi Y, Oshaghi M, Telma¬dar-raiy Z, Akhavan AA, Abai MR, Aran-dian MH (2009) Study on ectoparasites of Rhombomys opimus, the main res¬er-voir of zoonotic cutaneous Leishman¬i¬a-sis in endemic foci in Iran. Iran J Ar-thropod Borne Dis. 3(1): 41–45.
40. Azarmi S, Zahraei-Ramazani AR, Mohe-bali M, Akhavan AA, Rassi Y, Parsaeian M, Saboori A, Zarei Z, Azarm A, Abdoli R, Abdoli H (2019) An Environmental Study on Ectoparasites of Rhombomys opimus (Rodentia: Gerbillinae); the Main Reservoir Host of Zoonotic Cutaneous Leishmaniasis in a Hyperendemic Foci in Segzi, Esfahan Province. J Res Envi¬ron Health. 4(4): 291–301.
2. Norouzi B, Hanafi-Bojd AA, Moin-Vaziri V, Noorallahi A, Azari-Hamidian S (2020) 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. J Arthropod-Borne Dis. 14 (3): 302–316.
3. Ghatee MA, Taylor WR, Karamian M (2020) The geographical distribution of cuta¬ne¬ous leishmaniasis causative agents in Iran and its neighboring countries, a review. Front Public Health. 8: 11.
4. Owens SD, Oakley DA, Marryott K, Hatchett W, Walton R, Nolan TJ, Newton A, Steurer F, Schantz P, Giger U (2001) Transmission of visceral leishmaniasis through blood transfusions from infected English foxhounds to anemic dogs. J Amer¬ican Vet Med Ass. 219(8): 1076–1083.
5. Coutinho MTZ, Bueno LL, Sterzik A, Fu-jiwara RT, Botelho JR, De Maria M, Ge-naro O, Linardi PM (2005) Participation of Rhipicephalus sanguineus (Acari: Ix-odidae) in the epidemiology of canine vis¬ceral leishmaniasis. Vet Parasitol. 128 (1–2): 149–155.
6. McKenzie KK (1984) Study of the Trans-mission of Canine Leishmaniasis by the Tick, Rhipicephalus Sanguineus (Latreil-le) and an Ultrastructural Comparison of the Promastigotes. [PhD dissertation], Ok¬lahoma State University, Stillwater.
7. Ferreira MGPA, Fattori KR, Souza F, Lima VMF (2009) Potential role for dog fleas in the cycle of Leishmania spp. Vet par-asitol. 165(1–2): 150–154.
8. Leishmaniasis (Cutaneous and Visceral) (2017) Center for Food Security and Pub¬lic Health. Available at: www.cfsph.iastate.edu/Factsheets/pdfs/leishmaniasis.pdf.
9. Friedhoff K (1990) Interaction between par¬asite and tick vector. Int J Parasitol. 20 (4): 525–535.
10. Dantas-Torres F, Figueredo LA, Brandão-Filho SP (2006) Rhipicephalus san-guineus (Acari: Ixodidae), the brown dog tick, par¬asitizing humans in Brazil. Rev Soc Bra¬sileira Med Trop. 39(1): 64–67.
11. Sherlock I (1964) Nota sobre a trans¬mis-são da leishmaniose visceral no Brasil. Rev Brasileira Malariol. 16: 19–26.
12. Rey L (2001) Parasitologia: parasitos e doen¬ças parasitárias do homem nas Américas e na África / Parasitology: parasites and men parasitology diseases in America and Africa. 3rd ed. Guanabara Koogan, Rio de Janeiro.
13. Coutinho MTZ, Linardi PM (2007) Can fleas from dogs infected with canine vis-ceral leishmaniasis transfer the infection to other mammals? Vet parasitol. 147 (3–4): 320–325.
14. Flecknell P (2009) Laboratory animal an-aesthesia. 3rd ed. Academic Press.
15. Asmar M, Piazak N, Karimi Y (1979) Fleas, Identification keys of Fleas of Iran and Introduction-Hosts-Geografic Distribu¬tion. Pasteur Inst Iran [in Per-sian].
16. Walker AR, Bouattour A, Camicas JL, Es-trada-Peña A, Horak IG, Latif AA, Pe-gram RG, Preston PM (2003) Ticks of domestic animals in Africa: a guide to identification of species. Bioscience Re-ports, Edinburgh.
17. Pratt HD (2013) Anoplura: Pictoral key to some species on domestic rats in south-ern United States. Available at: https://www.cdc.gov/nceh/ehs/docs/pictorial_keys/lice-anoplura.pdf.
18. Mašán P, Fenďa P (2010) A Review of the Laelapid Mites Associated with Terres-trial Mammals in Slovakia, with a Key to the European Species (Acari: Meso-stigmata: Dermanyssoidea). Institute of Zoology, Slovak Academy of Sciences, Bratislava.
19. Etemad E (1978) Mammals of Iran, Ro-dents and their identification Keys. Na-tional Society of Guardianship of Nat-ural Resources and Human En¬viron-ment, Tehran [in Persian].
20. Akhavan AA, Mirhendi H, Khamesipour A, Alimohammadian MH, Rassi Y, Bates P, Kamhawi Sh, Valenzuela JG, Aran¬dian MH, Abdoli H, Jalili-Zand N, Jafari R, Shareghi N, Ghanei M, Yaghoobi-Er¬shadi MR (2010) Leishmania species: de¬tection and identification by nested PCR assay from skin samples of rodent res¬ervoirs. Exp Parasitol. 126(4): 552–556.
21. Akhavan AA, Yaghoobi-Ershadi MR, Khamesipour A, Mirhendi H, Alimo-ham¬madian M, Rassi Y, Arandian MH, Jafa¬ri R, Abdoli H, Shareghi N, Ghanei M, Jalili-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.
22. 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.
23. Jihene B, Meriam N (2017) Epidemiology of cutaneous leishmaniasis in Tunisia. In: Claborn D (Ed): The Epidemiology and Ecology of Leishmaniasis, Vol. 1. InTech, Croatia, pp. 79–91.
24. 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 in¬fec¬tion in sand flies in border line of Iran-Turkmenistan: restricted and permissive vectors. Exp Parasitol. 135(2): 382–387.
25. Strelkova MV (1996) Progress in studies on central asian foci of zoonotic cutaneous. Folia Parasitol. 43: 1–6.
26. Strelkova M, Eliseev L, Ponirovsky E, Derga¬cheva T, Annacharyeva D, Ero-khin P, Evans DA (2001) Mixed leishmanial infections in Rhombomys opimus: a key to the persistence of Leishmania major from one transmission season to the next. Ann Trop Med Parasitol. 95(8): 811–819.
27. Randall JA, Rogovin K, Parker PG, Eimes JA (2005) Flexible social structure of a desert rodent, Rhombomys opimus: philo¬patry, kinship, and ecological con-straints. Behav Ecol. 16(6): 961–973.
28. Zahraei-Ramazani A, Saghafipour A, Sed-aghat M, Absavaran A, Azarm A (2017) Molecular Identification of Phlebotomus caucasicus and Phlebotomus mon¬go¬len-sis (Diptera: Psychodidae) in a Hyperen-demic Area of Zoonotic Cutaneous Leish¬maniasis in Iran. J Med Entomol. 54(6): 1525–1530.
29. Doroodgar A, Sadr F, Razavi MR, Do-rood¬gar M, Asmar M, Doroodgar M (2015) A new focus of zoonotic cutaneous leish¬maniasis in Isfahan Province. Central Iran. Asian Pac J Trop Dis. 5: 54–58.
30. Blanc G, Caminopetros J (1930) Trans¬mis-sion of Mediterranean EA by a Tick. Compte Rendu de l'Academie des Sci-ences. 191(23): 1162–1164.
31. Otranto D, Dantas-Torres F (2010) Fleas and ticks as vectors of Leishmania spp. to dogs: caution is needed. Vet Parasitol. 168(1–2): 173–174.
32. Azarm A (2015) Molecular identification of dog fleas and study on the possibility of contamination of them with visceral leishmaniasis agent in Meshkinshar city. [A Thesis for MSc degree]. School of Med¬ical Sciences, Tarbiat Modares Uni-versity.
33. Khokhlova IS, Serobyan V, Krasnov BR, Degen AA (2009) Effect of host gender on blood digestion in fleas: mediating role of environment. Parasitol Res. 105 (6): 1667–1673.
34. Colombo FA, Odorizzi RM, Laurenti MD, Galati EA, Canavez F, Pereira-Chioc¬cola VL (2011) Detection of Leishmania (Leishmania) infantum RNA in fleas and ticks collected from naturally infected dogs. Parasitol Res. 109(2): 267–274.
35. Viol MA, Guerrero FD, de Oliveira BCM, de Aquino MCC, Loiola SH, de Melo GD, de Souza Gomes SH, Kanamura CT, Garcia MV, Adreotti R, de Lima VMF, Bresciani KDS (2016) Identification of Leishmania spp. promastigotes in the in¬testines, ovaries, and salivary glands of Rhipicephalus sanguineus actively in¬fest¬ing dogs. Parasitol Res. 115(9): 3479–3484.
36. Bilgic HB, Bakirci S, Kose O, Aksulu A, Hacilarlioglu S, Karagenc T (2016) De-termination the role of Rhipicephalus san¬guineus for transmission of Leishmania major to reservoir animals. Turkiye Parazitol Derg. 40: 179–184.
37. Rakhshanpour A, Malmasi A, Mohebali M, Nabian S, Mirhendi H, Zarei Z, Dalimi A, Mohammadiha A, Akhoundi B, Azarm A (2017) Transmission of Leishmania in¬fantum by Rhipicephalus sanguineus (Ac¬ari: Ixodidae) in dogs. Iran J Parasitol. 12(4): 482–489.
38. Dantas-Torres F (2011) Ticks as vectors of Leishmania parasites. Trends para¬si¬tol. 27(4): 155–159.
39. Tajedin L, Rassi Y, Oshaghi M, Telma¬dar-raiy Z, Akhavan AA, Abai MR, Aran-dian MH (2009) Study on ectoparasites of Rhombomys opimus, the main res¬er-voir of zoonotic cutaneous Leishman¬i¬a-sis in endemic foci in Iran. Iran J Ar-thropod Borne Dis. 3(1): 41–45.
40. Azarmi S, Zahraei-Ramazani AR, Mohe-bali M, Akhavan AA, Rassi Y, Parsaeian M, Saboori A, Zarei Z, Azarm A, Abdoli R, Abdoli H (2019) An Environmental Study on Ectoparasites of Rhombomys opimus (Rodentia: Gerbillinae); the Main Reservoir Host of Zoonotic Cutaneous Leishmaniasis in a Hyperendemic Foci in Segzi, Esfahan Province. J Res Envi¬ron Health. 4(4): 291–301.
| Files | ||
| Issue | Vol 16 No 2 (2022) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v16i2.11803 | |
| Keywords | ||
| Ectoparasite ; Leishmania gerbilli Leishmania major Leishmania turanica Rhombomys opimus | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Azarmi S, Zahraei-Ramazani A, Mohebali M, Rassi Y, Akhavan AA, Azarm A, Dehghan O, Elikaee S, Abdoli R, Mahmoudi M. PCR Positivity of Gerbils and Their Ectoparasites for Leishmania Spp. in a Hyperendemic Focus of Zoonotic Cutaneous Leishmaniasis in Central Iran. J Arthropod Borne Dis. 2023;16(2):124–135.
