Review Article

Visceral Leishmaniasis in Iran: An Update on Epidemiological Features from 2013 to 2022

Abstract

Background: Visceral leishmaniasis (VL) is one of the most important neglected tropical diseases. The zoonotic form of VL is endemic in some areas of Iran. We aimed to determine the status of VL identified in humans and canines in different parts of Iran from 2013 to 2022.

Method: A national representative cross-sectional study was conducted in 10 provinces of Iran, including the national leishmaniasis reference lab. We employed the direct agglutination test (DAT) as a reliable serological method to detect anti-Leishmania infantum antibodies in humans and animal reservoir hosts. Additionally, a narrative literature review was conducted to identify relevant studies on VL seroprevalence in Iran from 2013 to 2023.

Results: The results of 21281 human and 5610 canine serum samples from 2013 to 2022 are reported. Altogether, 448 (2.1%, 95%CI: 2.0-2.3) human serum samples showed anti-L. infantum antibody levels of ≥1:3200. Of these samples, 13716 (64.5%) were collected actively, which showed a seroprevalence of 0.6% (95% CI: 0.5-0.8) and 7565 (35.5%) were collected passively, which showed a seroprevalence of 4.8% (95%CI: 4.3-5.3). Overall, 1035 (20.1%, 95%CI: 19.0-21.2) of 5160 domestic dogs (Canis familiaris) samples showed anti-L. infantum antibody levels of ≥1:320. Northwest (2.8%) and northeast (0.96%) regions had the highest human VL seroprevalence, while northwest (21.5%) and south (14.4%) regions had the highest canine VL seroprevalence.

Conclusion: Zoonotic VL, an endemic parasitic disease, is still present in several different distinct areas across Iran. While human VL cases have shown a declining trend over the last decade, the prevalence of canine VL remains significant.

1. Alvar J, Vélez ID, Bern C, et al. Leishmaniasis worldwide and global estimates of its incidence. PLoS One. 2012;7(5):e35671.
2. WHO, 2022: Leishmaniasis. Available from: https://www.who.int/news-room/fact-sheets/detail/leishmaniasis.
3. Ready PD. Biology of phlebotomine sand flies as vectors of disease agents. Annu Rev Entomol. 2013;58:227-250.
4. Wang H, Naghavi M, Allen C, et al. Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388(10053):1459-544.
5. Collaborators God, Bernabe E, Marcenes W, et al. Global, regional, and national levels and trends in burden of oral conditions from 1990 to 2017: a systematic analysis for the global burden of disease 2017 study. J Dent Res. 2020;99(4):362-73.
6. Badirzadeh A, Mohebali M, Asadgol Z, et al. The burden of leishmaniasis in Iran, acquired from the global burden of disease during 1990–2010. Asian Pac J Trop Dis. 2017;7(9):513-8.
7. Sharifi I, Khosravi A, Aflatoonian MR, et al. Cutaneous leishmaniasis situation analysis in the Islamic Republic of Iran in preparation for an elimination plan. Fron Public Health. 2023; 11 :1091709.
8. Edrissian GH, Nadim A, Alborzi A, Ardehali S. Visceral leishmaniasis: the Iranian experiences. Arch Iran Med. 1998; 1:22–26.
9. Sharifi I, Aflatonian MR, Daei Parizi MH, et al. Visceral Leishmaniasis in Southeastern Iran: A Narrative Review. Iran J Parasitol.2017; 12(1): 1-11.
10. Mohebali M, Edrissian GH, Nadim A, et al. Application of direct agglutination test (DAT) for the diagnosis and seroepidemiological studies of visceral leishmaniasis in Iran. Iran J Parasitol. 2006;1(1):15-25.
11. Rassi Y, Kaverizadeh F, Javadian E, Mohebali M. First report on natural promastigote infection of Phlebotomus caucasicus in a new focus of visceral leishmaniasis in North West of Iran. Iran J Publ Health. 2004;33(4):70-72 .
12. Akhoundi B, Mohebali M, Shojaee S, et al. Rapid detection of human and canine visceral leishmaniasis: assessment of a latex agglutination test based on the A2 antigen from amastigote forms of Leishmania infantum. Exp Parasitol. 2013; 133(3):307-13.
13. Akhoundi B, Mohebali M, Babakhan L, et al. Rapid detection of human Leishmania infantum infection: A comparative field study using the fast agglutination screening test and the direct agglutination test. Travel Med Infect Dis. 2010; 8(5):305-10.
14. Sarkari B, Rezaei Z, Mohebali M. Immunodiagnosis of Visceral Leishmaniasis: Current Status and Challenges: A Review Article. Iran J Parasitol. 2018; 13(3): 331-341.
15. Mohebali M, Keshavarz H, Shirmohammad S, et al. The diagnostic accuracy of direct agglutination test for serodiagnosis of human visceral leishmaniasis: a systematic review with meta-analysis. BMC Infect Dis. 2020; 20(1):946.
16. Mohebali M, Edrissian GH, Shirzadi M, et al. Integrated visceral leishmaniasis surveillance system in primary care for children in Meshkin-Shahr district, north-western Islamic Republic of Iran. East Mediterr Health J. 2010; 16 (10): 1050-1054.
17. Mohebali M. Visceral leishmaniasis in Iran: review of the epidemiological and clinical features. Iran J Parasitol. 2013; 8(3):348-358.
18. Rassi Y, Javadian E, Nadim A, et al. Phlebotomus perfiliewi transcaucasicus, a vector of Leishmania infantum in northwestern Iran. J Med Entomol. 2009;46(5):1094-8.
19. Azizi K, Rassi Y, Javadian E, et al. First detection of Leishmania infantum in Phlebotomus (Larroussius) major (Diptera: Psychodidae) from Iran. J Med Entomol. 2008; 45(4):726-31.
20. Azizi K, Rassi Y, Javadian E, et al. Phlebotomus (Paraphlebotomus) alexandri: a probable vector of Leishmania infantum in Iran. Ann Trop Med Parasitol. 2006; 100(1):63-8.
21. Sahabi Z, Rashti MS, Nadim A, et al. A Preliminary report on the natural leptomonad Infection of Phlebotomus major in an endemic focus of visceral Leishmaniasis (VL) in Fars province, south of Iran. Iranian J Public Health. 1992; 21(1-4):87-93.
22. Rashti MS, Sahabi Z, Notash AK. Phlebotomus (Larroussius) keshishiani Hchurenkova 1936, another vector of visceral leishmaniasis in Iran. Iranian J Publ Health. 1995; 24(1-2):25-30.
23. Jahangir A, Akhoundi B, Mohebali M, et al. Seroepidemiological survey of human visceral leishmaniasis in Ilam province, west of Iran in 2013. Iran J Parasitol. 2015 ;10(1):56-61.
24. Heidari A, Mohebali M, Kabir K, et al. Visceral leishmaniasis in rural areas of Alborz province of Iran and implication to health policy. Korean J Parasitol. 2015; 53(4):379-83.
25. Khazaei S, Mohebali M, Akhoundi B, et al. Seroprevalence survey of visceral leishmaniasis among children up to 12 years old and domestic dogs in rural areas of Dehloran District, Ilam Province of west part of Iran, 2014. Novelty Biomed. 2017; 5(2):78-84.
26. Abbaszadeh-Afshar MJ, Mohebali M, et al. Seroepidemiological survey of visceral leishmaniasis among nomadic tribes of Kerman province, southeastern Iran: An observational study for implication to health policy. J Biostat Epidemiol. 2015;1(3/4):105-11.
27. Ebrahimzade-Parikhani H, Mohebali M, Zarei Z, Akhoundi B, Kakoei Z. Seroprevalence of visceral leishmaniasis in children up to 12 years old among nomadic tribes from rural areas of Pars Abad, northwestern Iran: an observational study in 2015. J Arthropod Borne Dis. 2017; 11(2):331-337.
28. Shirmohammad S, Mohebali M, Ghalehbin BM,et al. Human visceral leishmaniasis: Seroprevalence survey of asymptomatic adults in an endemic area of Northwestern Iran. J Biostat Epidemiol. 2016;2(3):136-42.
29. Afshar MJA, Sharifi I, Bamorovat M, et al. Canine visceral leishmaniasis; A seroepidemiological survey in Jiroft district, southern Kerman province, southeastern Iran in 2015. Iran J Parasitol. 2018; 13(1):67-71.
30. Behniafar H, Moin-Vaziri V, Mohebali M, et al. Visceral leishmaniasis among children in an endemic area of northwestern Iran between 2016 and 2017: An epidemiological study. Asian Pac J Trop Med. 2019; 12(7):306-314.
31. Ghodrati S, Akhoundi B, Mohebali M, et al. A Sero-Epidemiological Study on Visceral Leishmaniasis among Volunteer Children and Adults in Rural Areas of Shahroud, Iran 2018–2019. J Arthropod Borne Dis. 2022; 16(3):217–224.
32. Shad IAN, Mahmoudi MR, Mohebali M, et al. Seroepidemiological Study of Visceral Leishmaniasis (Kala-azar) in Children under 12 Years Old in North of Iran: An Observational Study in 2019-2020. Iran J Parasitol. 2022; 17(3):317-24.
33. Sedaghatmanesh K, Khazan H, Akhoundi B, Khazaei S, Kakooei Z, Mohebali M. Seroprevalence of Visceral Leishmaniasis in Children Up To 12 Years Old of Rural Areas from Kermanshah Province, Western Part of Iran. Iran J Parasitol. 2023; 18(1):85-92.
34. Bamorovat M, Sharifi I, Mohammadi MA, et al. Canine visceral leishmaniasis in Kerman, southeast of Iran: a seroepidemiological, histopathological and molecular study. Iran J Parasitol. 2014; 9(3):342-349.
35. Tabatabaie F, Nasirikaleybar Y, Mohebali M, et al. Serological and molecular survey of zoonotic visceral leishmaniasis in stray dogs (Canis familiaris) from an endemic focus in Meshkin-Shahr district in Ardabil province, Iran. J Vector Borne Dis. 2021; 58(3):213-218.
36. Farahmand M, Nahrevanian H, Khalaj V, et al. Assessment of recombinant A2-Latex Agglutination Test (RA2-LAT) and RA2-ELISA for detection of canine visceral Leishmaniasis: a comparative field study with direct agglutination test in Northwestern Iran. Iran J Parasitol. 2018; 13(2):172-179.
37. Heidari A, Mohebali M, Vahed M, et al. Molecular and Seroepidemiological survey of visceral leishmaniasis in owned dogs (Canis familiaris) in new foci of rural areas of Alborz Province, Central Part of Iran: A cross-sectional study in 2017. J Arthropod Borne Dis. 2020; 14(1):38-46.
38. Soleimani A, Mohebali M, Gholizadeh S, et al. Molecular and serological evaluation of visceral leishmaniasis in domestic dogs and cats in Maragheh County, north‐west of Iran, 2018–2021. Vet Med Sci. 2022; 8(5):1898-1903.
39. Mohebali M, Malmasi A, Khodabakhsh M, et al. Feline leishmaniosis due to Leishmania infantum in Northwest Iran: The role of cats in endemic areas of visceral leishmaniosis. Vet Parasitol Reg Stud Reports. 2017; 9:13-6.
40. Fatollahzadeh M, Khanmohammadi M, Bazmani A, et al. Survey of feline visceral leishmaniasis in Azarshahr area, North West of Iran, 2013. J Parasit Dis. 2016; 40(3):683-7.
41. Mohebali M, Arzamani K, Zarei Z, et al. Canine visceral leishmaniasis in wild canines (fox, jackal, and wolf) in northeastern Iran using parasitological, serological, and molecular methods. J Arthropod Borne Dis. 2016; 10(4):538-545.
42. Nadim A, Javadian E, Tahvildar–Bidruni G, Mottaghi M. Epidemiological aspects of kala-azar in Meshkin shar, Iran: investigation on vectors. Iranian J Publ Health. 1992; 21(1-4):61-72.
43. Rassi Y, Javadian E, Nadim A, Zahraeii AR, Vatandoost H. Phlebotomus (Larroussius) kandelakii, the principal and proven vector of visceral leishmaniasis in north west of Iran. Pak J Biol Sci. 2005; 80:1–5.
44. Rassi Y, Abai M, Oshaghi M, et al. First detection of Leishmania infantum in Phlebotomus kandelakii using molecular methods in north-eastern Islamic Republic of Iran. East Mediterr Health J. 2012; 18 (4), 387-392.
45. Dehkordi AS, Rassi Y, Oshaghi M, et al. Molecular detection of Leishmania infantum in naturally infected Phlebotomus perfiliewi transcaucasicus in Bilesavar district, northwestern Iran. Iran J Arthropod Borne Dis. 2011; 5(1):20-27.
46. Oshaghi MA, Ravasan NM, Hide M, et al. Phlebotomus perfiliewi transcaucasicus is circulating both Leishmania donovani and L. infantum in northwest Iran. Exp Parasitol. 2009; 123(3):218-25.
47. Parvizi P, Mazloumi-Gavgani A, Davies C, Courtenay O, Ready P. Two Leishmania species circulating in the Kaleybar focus of infantile visceral leishmaniasis, northwest Iran: implications for deltamethrin dog collar intervention. Trans R Soc Trop Med Hyg. 2008; 102(9):891-7.
48. Oshaghi MA, Rassi Y, Hazratian T, Fallah E, Rafizadeh S. Natural infection of wild caught Phlebotomus tobbi to Leishmania infantum in East Azerbaijan province, northwestern Iran. J Vector Borne Dis. 2013; 50(1):24-29.
49. Rassi Y, Dehkordi AS, Oshaghi MA, et al. First report on natural infection of the Phlebotomus tobbi by Leishmania infantum in northwestern Iran. Exp Parasitol. 2012; 131(3):344-9.
50. Bahrami A, Rassi Y, Maleki N, et al. Leishmania infantum DNA detection in Phlebotomus tobbi in a new northern focus of visceral leishmaniasis in Iran. Asian Pac J Trop Dis. 2014; 4(2):110-114.
51. Javadian E, Mesghali A, Nadim A. Natural leptomonad infection of sand flies with its first occurrence in P. alexandri in Khuzistan Province, Iran. Coll Int CNRS. 1977; 239:203-5.
52. Rassi Y, Karami H, Abai MR, et al. First detection of Leishmania infantum DNA in wild caught Phlebotomus papatasi in endemic focus of cutaneous leishmaniasis, South of Iran. Asian Pac J Trop Biomed. 2013; 3(10):825-9.
53. Rostamian M, Bashiri H, Yousefinejad V, et al. Prevalence of human visceral leishmaniasis in Iran: A systematic review and meta-analysis. Comp Immunol Microbiol Infect Dis. 2021; 75:101604.
54. Mondiale de la Santé O, WHO. Weekly Epidemiological Record, 2022, vol. 97, 45 [full issue]. Weekly Epidemiological Record= Relevé épidémiologique hebdomadaire. 2022; 97(45):575-90.
55. Ready PD. Epidemiology of visceral leishmaniasis. Clin Epidemiol. 2014; 6:147-154.
56. Marcondes M, Day MJ. Current status and management of canine leishmaniasis in Latin America. Res Vet Sci. 2019; 123:261-72.
57. Davies C, Gavgani AM. Age, acquired immunity and the risk of visceral leishmaniasis: a prospective study in Iran. Parasitology. 1999; 119( Pt 3):247-57.
58. Shokri A, Fakhar M, Teshnizi SH. Canine visceral leishmaniasis in Iran: A systematic review and meta-analysis. Acta Trop. 2017; 165:76-89.
59. Mohebali M, Moradi-Asl E, Rassi Y. Geographic distribution and spatial analysis of Leishmania infantum infection in domestic and wild animal reservoir hosts of zoonotic visceral leishmaniasis in Iran: A systematic review. J Vector Borne Dis. 2018; 55(3):173-183.
60. WHO. Global vector control response 2017-2030. Geneva: World Health Organization; 2017.
61. Githeko AK, Lindsay SW, Confalonieri UE, Patz JA. Climate change and vector-borne diseases: a regional analysis. Bulletin of the World Health Organization. 2000; 78(9):1136-47.
62. Wamai RG, Kahn J, McGloin J, Ziaggi G. Visceral leishmaniasis: a global overview. J Glob Health. 2020; 14;2(1).
63. Patiño LH, Castillo-Castañeda AC, Muñoz M, et al. Development of an amplicon-based next-generation sequencing protocol to identify Leishmania species and other trypanosomatids in leishmaniasis endemic areas. Microbiol Spectr. 2021;9(2):e0065221.
64. de Arruda RMF, Cardoso DT, Teixeira-Neto RG, et al. Space-time analysis of the incidence of human visceral leishmaniasis (VL) and prevalence of canine VL in a municipality of southeastern Brazil: Identification of priority areas for surveillance and control. Acta Trop. 2019; 197:105052-105052.
65. Ciaramella P, Oliva Gd, De Luna R, et al. A retrospective clinical study of canine leishmaniasis in 150 dogs naturally infected by Leishmania infantum. Vet Rec. 1997; 141(21):539-43.
66. WHO. Report of the Second WHO Meeting on Emerging Infectious Diseases, Geneva, Switzerland, and 12-13 January 1995. World Health Organization; 1995.
67. Saini I, Joshi J, Kaur S. Unwelcome prevalence of leishmaniasis with several other infectious diseases. Int Immunopharmacol. 2022; 110:109059.
68. Kantzanou M, Karalexi MA, Theodoridou K, et al. Prevalence of visceral leishmaniasis among people with HIV: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2023; 42(1):1-12.
69. Medrano FJ, Hernández-Quero J, Jiménez E, et al. Visceral leishmaniasis in HIV-1-infected individuals: a common opportunistic infection in Spain? AIDS. 1992; 6(12):1499-503.
70. Rezaei Z, Sarkari B, Dehghani M, Layegh Gigloo A, Afrashteh M. High frequency of subclinical Leishmania infection among HIV-infected patients living in the endemic areas of visceral leishmaniasis in Fars province, southern Iran. Parasitol Res. 2018; 117(8):2591-5.
71. Shafiei R, Mohebali M, Akhoundi B, et al. Emergence of co-infection of visceral leishmaniasis in HIV-positive patients in northeast Iran: A preliminary study. Travel Med Infect Dis. 2014; 12(2):173-8.
Files
IssueVol 18 No 3 (2023) QRcode
SectionReview Article(s)
DOI https://doi.org/10.18502/ijpa.v18i3.13751
Keywords
Visceral leishmaniasis; Iran Direct agglutination test Human Canine

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
1.
Mohebali M, Edrissian G, Akhoundi B, Shirzadi M, Hassanpour G, Behkar A, Rassi Y, Hajjaran H, Keshavarz H, Gouya MM, Arshi S, Zeinali M, Zarei Z, Sharifi I, Kakooei Z. Visceral Leishmaniasis in Iran: An Update on Epidemiological Features from 2013 to 2022. Iran J Parasitol. 2023;18(3):279-293.