Review Article

The Environmental Variables Associated with Distribution of Canine Visceral Leishmaniasis in Dogs in Ardabil Province, Northwestern Iran: A Systematic Review


Background: Visceral leishmaniasis (VL) is a zoonotic disease that currently occurs in some parts of Europe, Asia, Africa, and America. This study aimed to determine the distribution of the canine visceral leishmaniasis in dogs (Canis lupus familiaris) in northwestern Iran.

Methods: The data were collected from 1994 to 2018 in Ardabil Province from electronic databases. An extensive literature search was conducted in different international and national databases, including Cochrane, MEDLINE/PubMed, Scopus, Web of Science, and Iran Medex to find articles with the words “visceral leishmaniasis in Ardabil” in their titles, and “canine visceral leishmaniasis in Ardabil” or “accidental reservoir hosts of visceral leishmaniasis in Ardabil” in their subtitles, irrespective of the type and duration of study. The GIS software and MaxEnt model were used to determine the ecologically suitable niches for the disease.

Results: In total, 9088 dogs were examined, and the overall prevalence rate of CVL in dogs was estimated to be 14.56%. The most ecologically suitable areas of CVL occurrence were identified in four hotspots in Meshkinshahr, Germi, and two spots in Parsabad counties. The results of jackknife test showed that the environmental and climate variables with the highest gain, when used in isolation, were Isothermality, Bio3, Bio13, and Bio 4.

Conclusion: A widely epidemic CVL has emerged among dogs, making a lot of risks on inhabitants of this area and increasing the probability of an outbreak of VL in humans.

1. Oryan A, Akbari M (2016). Worldwide risk factors in leishmaniasis. Asian Pac J Trop Med, 9(10): 925-932.
2. Moradi-Asl E, Rassi Y, Hanafi-Bojd AA et al (2019). Spatial distribution and infec-tion rate of leishmaniasis vectors (Dip-tera: Psychodidae) in Ardabil Province, Northwest of Iran. Asian Pac J Trop Bio-med, 9(5):181-187.
3. Moradi-Asl E, Rassi Y, Adham D, Hanafi-Bojd AA et al (2018). Spatial distribution of sand flies (Diptera: Psychodidae; Lar-roussius group), the vectors of visceral leishmaniasis in Northwest of Iran. Asian Pac J Trop Biomed, 8(9):425-430.
4. Mohebali M, Moradi-Asl E, Rassi Y (2018). Geographic distribution and spatial anal-ysis of Leishmania infantum infection in domestic and wild animal reservoir hosts of zoonotic visceral leishmaniasis in Iran: A systematic review. J Vector borne Dis, 55(3): 173-183.
5. Saul J, Semiao S (1996). Canine visceral leishmaniasis in Evora district. A Seroep-idemiological Study. Protogal, 9:74-9.
6. Reiner SL, Locksley RM (1995). The regula-tion of immunity to Leishmania major. Annu Rev Immunol, 13(1):151–77.
7. Solcà MdS, Bastos LA, Guedes CES et al (2014). Evaluating the Accuracy of Mo-lecular Diagnostic Testing for Canine Visceral Leishmaniasis Using Latent Class Analysis. PLoS ONE, 9(7): e103635.
8. Riboldi E, Carvalho F, Romão P et al (2018). Molecular Method Confirms Canine Leishmania Infection Detected by Serolog-ical Methods in Non-Endemic Area of Brazil. Korean J Parasitol, 56(1): 11–19.
9. Chappuis F, Sundar S, Hailu A et al (2007). Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat Rev Microbiol, 5(11):873-882.
10. Terán-Angel G, Schallig H, Zerpa O et al (2007). The direct agglutination test as an alternative method for the diagnosis of canine and human visceral leishmaniasis. Biomédica, 27(3):447–53.
11. da Silva DA, de Fátima Madeira M, Abrantes TR et al (2013). Assessment of serological tests for the diagnosis of ca-nine visceral leishmaniasis. Vet J,195(2):252–3.
12. Nadim A, Javadian E, Mohebali M et al (2008). Leishmania parasite and leishmani-asis. Acad Publish Cent, Tehran, Iran. Markaze Nashre Daneshgahi Publ.
13. Baneth G, & Aroch I (2008). Canine leish-maniasis: a diagnostic and clinical chal-lenge. Vet J, 175(1): 14-15.
14. Solano-Gallego L, Koutinas A, Miró G et al (2009). Directions for the diagnosis, clini-cal staging, treatment and prevention of canine leishmaniosis. Vet Parasitol, 165(1-2):1–18.
15. Fakhar M, Rahmati B, Gohardehi S et al (2011). Molecular and seroepidemiologi-cal survey of visceral leishmaniasis among humans and domestic dogs in Mazanda-ran province, north of Iran. Iran J Parasi-tol,6(4):51-9.
16. Ozensoy S, Ozbel Y, Turgay N et al (1998). Serodiagnosis and epidemiology of vis-ceral leishmaniasis in Turkey. Am J Trop Med Hyg, 59(3):363–369.
17. Dantas-Torres F, de Brito MEF, Brandão-Filho SP (2006). Seroepidemiological sur-vey on canine leishmaniasis among dogs from an urban area of Brazil. Vet Parasi-tol,140(1-2):54–60.
18. Jaffe CL, Baneth G, Abdeen ZA et al (2004). Leishmaniasis in Israel and the Palestini-an authority. Trends Parasitol, 20(7):328–32.
19. Bokai S, Mobedi I, Edrissian Gh (1998). Seroepidemiological study of canine vis-ceral leishmaniasis in Meshkin-Shahr, northwest of Iran. Arch Inst Razi ,41(6):48–9
20. Tagi-zade TA, Gasanzade GB, Saf’ianova VM et al (1989). [Visceral leishmaniasis in Ordubad district, Nakhichevan ASSR]. Med Parazitol(Mosk),3:22–7.
21. Gavgani ASM, Mohite H, Edrissian GHet al (2002). Domestic dog ownership in Iran is a risk factor for human infection with Leishmania infantum. Am J Trop Med Hyg, 67(5):511–5.
22. Alvar J, Cañavate C, Molina R et al (2004). Canine leishmaniasis. Adv Parasitol, 57:1-88.
23. Mohebali M, Hajjaran H, Hamzavi Y et al (2005). Epidemiological aspects of canine visceral leishmaniosis in the Islamic Re-public of Iran. Vet Parasitol, 129(3-4):243–51.
24. Moshfe A, Mohebali M, Edrissian G et al (2008). Seroepidemiological study on ca-nine visceral leishmaniasis in Meshkin-Shahr district, Ardabil province, north-west of Iran during 2006-2007. Iran J Parasitol, 3(3):1–10.
25. Khanmohammadi M, Fallah E, Rahbari S et al (2010). Study on seroprevalence of Ca-nine Visceral Leishmaniasis (CVL) in ownership dogs of Sarab, east Azerbai-jan, Province, northwest of Iran with In-direct Immuno Fluorescence Antibody Test (IFAT) and its health importance in 2008-2009. J Anim Vet Adv, 9(1):139–43.
26. Mohammadi-Ghalehbin B, Hatam GR, Sarkari B et al (2011). A Leishmania in-fantum FML-ELISA for the detection of symptomatic and asymptomatic canine visceral leishmaniasis in an endemic area of Iran. Iran J Immunol, 8(4):244–50.
27. Barati M, Mohebali M, Alimohammadian MH et al (2015). Canine visceral leish-maniasis: seroprevalence survey of asymptomatic dogs in an endemic area of northwestern Iran. J Parasit Dis, 39(2):221–4.
28. Moradi-Asl E, Hanafi-Bojd AA, Rassi Yet al (2017). Situational analysis of visceral leishmaniasis in the most important en-demic area of the disease in Iran. J Ar-thropod Borne Dis,11(4):482-492.
29. Phillips SJ, Anderson RP, Schapire RE (2006). Maximum entropy modeling of species geographic distributions. Ecol Modell,190(3-4):231–59.
30. Molaei S, Dalimi A, Mohamadi B et al (2016). Study of Canine Visceral Leish-maniasis in Symptomatic and Asympto-matic Domestic Dogs in Meshkinshahr City, Iran. J Ardabil Univ Med Sci,16(1):105–115.
31. Mohebali M (2013). Visceral leishmaniasis in Iran: review of the epidemiological and clinical features. Iran J Parasitol, 8(3):348-358.
32. Mohebali M, Hamzavi Y, Edrissian GH et al (2001). Seroepidemiological study of vis-ceral leishmaniasis among humans and animal reservoirs in Bushehr province, Islamic Republic of Iran 2001. East Medi-terr Health J,7(6):912-917.
33. Sadeghi H (2003). The prevalence of sero-logic leishmaniasis in flock and domestic dogs of nomads in Ardebil province in 2002 by using of DAT method. J Ardabil Uni Med, 3(5):25–40.
34. Mohebali M, Taran M, Zarei Z (2004). Rap-id detection of Leishmania infantum infec-tion in dogs: comparative study using an immunochromatographic dipstick rk39 test and direct agglutination. Vet Parasi-tol,121(3-4):239–45.
35. Mohebali M, Khamesipour A, Mobedi I et al (2004). Double-blind randomized effi-cacy field trial of alum precipitated auto-claved Leishmania major vaccine mixed with BCG against canine visceral leish-maniasis in Meshkin-Shahr district, IR Iran. Vaccine, 22(29-30):4097–100.
36. Mahami M, Moheb Ali M, Keshavarz H et al (2006). A seroepidemiological survey of visceral leishmaniasis (KALA-AZAR) in Germi district, Ardabil Province. J Sch Public Heal Inst Public Heal Res,4(1):45–55.
37. Mohebali M, Edrissian GHH, Nadim A et al (2006). Application of direct agglutination test (DAT) for the diagnosis and seroep-ide-miological studies of visceral leish-maniasis in Iran. Iran J Parasitol,1:15–25.
38. Taran M, Mohebali M, Modaresi MH et al (2007). Diagnosis of canine visceral leishmaniasis by ELISA using K39sub recombinant antigen. Iran J Public Health,36(2):1–6.
39. Moshfe A, Mohebali M, Edrissian G et al (2009). Canine visceral leishmaniasis: asymptomatic infected dogs as a source of L. infantum infection. Acta Trop,112:101–5.
40. Salahi-Moghaddam A, Mohebali M, Mosh-fae A et al (2010). Ecological study and risk mapping of visceral leishmaniasis in an endemic area of Iran based on a geo-graphical information systems approach. Geospat Health, 5(1):71–77.
41. Sharifdini M, Mohebali M, Keshavarz H et al (2011). Neospora caninum and Leish-mania infantum co-infection in domestic dogs (Canis familiaris) in Meshkin-Shahr district, Northwestern Iran. Iran J Arthro-pod Borne Dis,5(2):60-70.
42. Mohammadiha A, Haghighi A, Mohebali M et al (2013). Canine visceral leishmaniasis: a comparative study of real-time PCR, conventional PCR, and direct agglutina-tion on sera for the detection of Leish-mania infantum infection. Vet Parasi-tol,192(1-3):83–90.
43. Alis A, Sharifi M, Mohebali M et al (2013). Evaluation of canine anti-Leishmania IgG subclasses and their relation with skin signs in naturally infected dogs in the northwest of Iran. Turkish J Vet Anim Sci,37(5):512–515.
44. Jalilnavaz MR, Abai MR, Vatandoost H et al (2016). Application of flumethrin pour-on on reservoir dogs and its efficacy against sand flies in endemic focus of visceral leishmaniasis, Meshkinshahr, Iran. J Arthropod Borne Dis, 10(1):78-86.
45. Ghaffarinejad P, Nahrevanian H, Mohebali M et al ( 2015). Diagnosis of Leishmania infantum using Direct Agglutination Test and rKE16 Dipstick Rapid Test in Do-mestic Dogs from Ardabil Province, Iran. J Parasitol Res,10(3):102–110.
46. Farahmand M, Khalaj V, Mohebali M et al (2015). Comparison of recombinant A2-ELISA with rKE16 dipstick and direct agglutination tests for diagnosis of vis-ceral leishmaniasis in dogs in Northwest-ern Iran. Rev Soc Bras Med Trop, 48(2):188–93.
47. Shokri A, Fakhar M, Teshnizi SH (2017). Canine visceral leishmaniasis in Iran: a systematic review and meta-analysis. Acta Trop,165:76–89.
48. Fakhar M, Motazedian MH, Asgari Q et al (2011). Asymptomatic domestic dogs are carriers of Leishmania infantum: possible reservoirs host for human visceral leish-maniasis in southern Iran. Comp Clin Path, 21(5):801–807.
49. Haddadzade HR, Fattahi R, Mohebali M et al (2013). Seroepidemiologcal investiga-tion of visceral leishmaniasis in stray and owned dogs in Alborz province, Central Iran using direct agglutination test. Iran J Parasitol,8(1):152-157.
50. Malmasi A, Janitabar S, Mohebali M et al (2014). Seroepidemiologic survey of ca-nine visceral leishmaniasis in Tehran and Alborz Provinces of Iran. J Arthropod Borne Dis ,8(2):132-138.
51. Coura-Vital W, Reis AB, Reis LES et al (2013). Canine visceral leishmaniasis: in-cidence and risk factors for infection in a cohort study in Brazil. Vet Parasitol,197(3-4):411–417.
52. Silva AF da, Damasceno ÁRA, Prado WS et al (2017). Leishmania infantum infection in dogs from maroon communities in the Eastern Amazon. Ciência Rural,47(1): e20160025.
53. Moraes-Silva E, Antunes FR, Rodrigues MS et al (2006). Domestic swine in a visceral leishmaniasis endemic area produce anti-bodies against multiple Leishmania infan-tum antigens but apparently resist to L. infantum infection. Acta Trop, 98(2):176–182.
54. Edrissian GH, Ahanchin AR, Gharachahi AM et al (1993). Seroepidemiological studies of visceral leishmaniasis and search for animal reservoirs in Fars prov-ince, southern Iran. Iran J Med Sci,18:99–105.
55. Moradi Asl E, Mohebali M, Mohammadi-ghalehbin B et al (2014). Study on Changes in Epidemiological Patterns and Parameters of Visceral Leishmaniasis in Patients Referred to Health Care Centers of Meshkin Shahr during 2001-2012:(A Retrospective Study). J Ardabil Univ Med Sci,14(1):63–70.
56. Avizeh R, Mohebali M, Sheikholslami M (2007). Seroepidemiological investigation of visceral leishmaniasis in dogs of Ah-vaz district, Iran. Arch Razi Inst,62(1):31–37.
57. Fallah E, Farshchian M, Khanmohammadi M (2011). Molecular and seroepidemio-logical study of Leishmania infantum infec-tion among humans, dogs and wild ca-nines from Azarshahr (new endemic fo-cus), Iran. Afr J Microbiol Res, 5(10):1237–1242.
58. Aflatoonian MR, Akhtardanesh B, Sharifi I et al (2015) . Seroepidemiology of Canine Visceral Leishmaniosis in Kerman City, 2011. J Kerman Univ Med Sci,19(6):531-539.
59. Campos R, Santos M, Tunon G et al (2017). Epidemiological aspects and spatial dis-tribution of human and canine visceral leishmaniasis in an endemic area in northeastern Brazil. Geospat Health, 12(1):503.
60. Miranda S, Roura X, Picado A et al (2008). Characterization of sex, age, and breed for a population of canine leishmaniosis diseased dogs. Res Vet Sci,85(1):35–38.
61. Mahshid M, Baharak A, Iraj S et al (2014) . Seroprevalence of canine visceral leish-maniasis in southeast of Iran. J Parasit Dis, 38(2):218–222.
62. Fakhar M, Kia AA, Gohardehi S et al (2014). Emergence of a new focus of visceral leishmaniasis due to Leishmania infantum in Golestan Province, north-eastern of Iran. J Parasit Dis,38(3):255–259.
63. Kalayou S, Tadelle H, Bsrat A et al (2011). Serological Evidence of Leishmania donovani Infection in Apparently Healthy Dogs us-ing Direct Agglutination Test (DAT)and rk39 Dipstick Tests in Kafta Humera, north‐west Ethiopia. Transbound Emerg Dis,58(3):255–262.
64. Sousa S, Lopes AP, Cardoso L et al (2011). Seroepidemiological survey of Leishmania infantum infection in dogs from north-eastern Portugal. Acta Trop,120(1-2):82–87.
65. Heidarpour M, Pourtaghi M, Khoshnegah J (2014). Prevalence and risk factors for canine leishmaniasis in Mashhad, north east of Iran. Iran J Vet Sci Technol ,4(1):37–46.
66. Gharekhani J, Heidari H, Hajian-Bidar H et al (2016). Prevalence of anti-Leishmania in-fantum antibodies in dogs from West of Iran. J Parasit Dis,40(3):964–967.
67. Chamaillé L, Tran A, Meunier A et al (2010). Environmental risk mapping of canine leishmaniasis in France. Parasit Vec-tors,3:31.
IssueVol 49 No 6 (2020) QRcode
SectionReview Article(s)
Canine visceral leishmaniasis; Dogs; Iran

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How to Cite
MORADI-ASL E, MOHEBALI M, RASSI Y, VATANDOOST H, SAGHAFIPOUR A. The Environmental Variables Associated with Distribution of Canine Visceral Leishmaniasis in Dogs in Ardabil Province, Northwestern Iran: A Systematic Review. Iran J Public Health. 2020;49(6):1033-1044.