Visceral leishmaniasis among children in an endemic area of northwestern Iran between 2016 and 2017: An epidemiological study
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摘要
Objective: To clarify the epidemiological aspects of visceral leishmaniasis in Kaleybar and Khoda-Afarin districts, north-west of Iran.Methods: A total of 1 420 human(children under 12 years) samples, 101 domestic dogs samples(Canis familiaris), and 577 female sand fly samples were collected. Sera of human and dogs were tested using the direct agglutination test, and sand flies were identified at species level using the microscopic method. Furthermore, a structured questionnaire was applied to evaluate the correlation between the potential risk factors and the related clinical signs/symptoms with the human and dogs' seropositivity.Results: Totally, 2.18% of human samples were positive at titers≥1: 800; among them, 13 cases(41.94%) were above 1:3 200, and clinical symptoms were observed in all of them except for an 11-year old girl. Anti-Leishmania infantum antibodies were found at titer≥1: 320 in 9.90% of dogs' samples, half of them had at least one sign of canine visceral leishmaniasis. Moreover, 10 Phlebotomus species were identified in the study areas, and Phlebotomus(Larroussius) major group was the predominant species. There are significant correlations between the presence of anti-Leishmania infantum antibodies and the fever(P<0.001), anemia(P=0.001) and weight loss(P=0.016) in children. On the other hand, significant correlations were revealed between the Leishmania infection and the shelter(P=0.039), cutaneous lesion(P=0.005), lymphadenopathy(P=0.001) and weight loss(P<0.001) in the infected dogs.Conclusions: Visceral Leishmania infection is prevalent in rural areas of Kaleybar and KhodaAfar districts located in East-Azerbaijan province, therefore active detection and treatment of visceral leishmaniasis cases should not be neglected.
Objective: To clarify the epidemiological aspects of visceral leishmaniasis in Kaleybar and Khoda-Afarin districts, north-west of Iran.Methods: A total of 1 420 human(children under 12 years) samples, 101 domestic dogs samples(Canis familiaris), and 577 female sand fly samples were collected. Sera of human and dogs were tested using the direct agglutination test, and sand flies were identified at species level using the microscopic method. Furthermore, a structured questionnaire was applied to evaluate the correlation between the potential risk factors and the related clinical signs/symptoms with the human and dogs' seropositivity.Results: Totally, 2.18% of human samples were positive at titers≥1: 800; among them, 13 cases(41.94%) were above 1:3 200, and clinical symptoms were observed in all of them except for an 11-year old girl. Anti-Leishmania infantum antibodies were found at titer≥1: 320 in 9.90% of dogs' samples, half of them had at least one sign of canine visceral leishmaniasis. Moreover, 10 Phlebotomus species were identified in the study areas, and Phlebotomus(Larroussius) major group was the predominant species. There are significant correlations between the presence of anti-Leishmania infantum antibodies and the fever(P<0.001), anemia(P=0.001) and weight loss(P=0.016) in children. On the other hand, significant correlations were revealed between the Leishmania infection and the shelter(P=0.039), cutaneous lesion(P=0.005), lymphadenopathy(P=0.001) and weight loss(P<0.001) in the infected dogs.Conclusions: Visceral Leishmania infection is prevalent in rural areas of Kaleybar and KhodaAfar districts located in East-Azerbaijan province, therefore active detection and treatment of visceral leishmaniasis cases should not be neglected.
Objective: To clarify the epidemiological aspects of visceral leishmaniasis in Kaleybar and Khoda-Afarin districts, north-west of Iran.Methods: A total of 1 420 human(children under 12 years) samples, 101 domestic dogs samples(Canis familiaris), and 577 female sand fly samples were collected. Sera of human and dogs were tested using the direct agglutination test, and sand flies were identified at species level using the microscopic method. Furthermore, a structured questionnaire was applied to evaluate the correlation between the potential risk factors and the related clinical signs/symptoms with the human and dogs' seropositivity.Results: Totally, 2.18% of human samples were positive at titers≥1: 800; among them, 13 cases(41.94%) were above 1:3 200, and clinical symptoms were observed in all of them except for an 11-year old girl. Anti-Leishmania infantum antibodies were found at titer≥1: 320 in 9.90% of dogs' samples, half of them had at least one sign of canine visceral leishmaniasis. Moreover, 10 Phlebotomus species were identified in the study areas, and Phlebotomus(Larroussius) major group was the predominant species. There are significant correlations between the presence of anti-Leishmania infantum antibodies and the fever(P<0.001), anemia(P=0.001) and weight loss(P=0.016) in children. On the other hand, significant correlations were revealed between the Leishmania infection and the shelter(P=0.039), cutaneous lesion(P=0.005), lymphadenopathy(P=0.001) and weight loss(P<0.001) in the infected dogs.Conclusions: Visceral Leishmania infection is prevalent in rural areas of Kaleybar and KhodaAfar districts located in East-Azerbaijan province, therefore active detection and treatment of visceral leishmaniasis cases should not be neglected.
引文
[1]World Health Organization.Leishmaniasis,the disease.[Online]Available from:https://www.who.int/Leishmaniasis/disease/en/.[Accessed on 10February 2019].
[2]World Health Organization.Fact sheet,leishmaniasis.[Online]Available from:https://www.who.int/news-room/fact-sheets/detail/Leishmaniasis.[Accessed on 10 February 2019].
[3]Masoori L,Kheirandish F,Haghighi A,Mohebali M,Akhoundi B,Taghipour N,et al.Molecular-based detection of Leishmania infantum in human blood samples in a new focus of visceral leishmaniasis in Lorestan Province,Iran.J Arthropod Borne Dis 2018;12(1):67.
[4]Mohebali M.Visceral leishmaniasis in Iran:Review of the epidemiological and clinical features.Iran J Parasitol 2013;8(3):348-358.
[5]Ready PD.Epidemiology of visceral Leishmaniasis.Clin Epidemiol 2014;6:147-154.
[6]Mohebali M,Hajjaran H,Hamzavi Y,Mobedi I,Arshi S,Zarei Z,et al.Epidemiological aspects of canine visceral leishmaniasis in the Islamic Republic of Iran.Vet parasitol 2005;129(3-4):243-251.
[7]Mohebali M,Edrissian GH,Shirzadi MR,Akhoundi B,Hajjaran H,Zarei Z,et al.An observational study on the current distribution of visceral leishmaniasis in different geographical zones of Iran and implication to health policy.Travel Med Infect Dis 2011;9(2):67-74.
[8]Sharifi I,Aflatoonian MR,Daei Parizi MH,Hosseininasab A,Mostafavi M,Bamorovat M,et al.Visceral leishmaniasis in Southeastern Iran:Anarrative review.Iran J Parasitol 2017;12(1):1-11.
[9]Ozbel Y,Oskam L,Ozensoy S,Turgay N,Alkan MZ,Jaffe CL,et al.Asurvey on canine leishmaniasis in western Turkey by parasite,DNA and antibody detection assays.Acta Trop 2000;74(1):1-6.
[10]Badirzadeh A,Mohebali M,Asadgol Z,Soong L,Zeinali M,Mokhayeri Y,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):513-518.
[11]El Harith A,Kolk A,Leeuwenburg J,Muigai R,Huigen E,Jelsma T,et al.Improvement of a direct agglutination test for field studies of visceral leishmaniasis.J Clin Microbiol 1988;26(7):1321-1325.
[12]Mohebali M.Epidemiological status of visceral leishmaniasis in Iran:experiences and review of literature.J Clinic Experiment Pathol S 2012;3143:1-5.
[13]Parvizi P,Mazloumi-Gavgani AS,Davies CR,Courtenay O,Ready PD.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):891-897.
[14]Theodor O,Mesghali A.On the Phlebotominae of Iran.J Med Entomol1964;1:285-300.
[15]Léger N,Pesson B,Madulo-Leblond G,Abonnenc E.Sur la différenciation des femelles du sous-genre larroussius nitzulescu,1931-(Diptera-Phlebotomidae)de la région méditerranéenne.Ann Parasitol Hum Comp 1983;58(6):611-623.
[16]Zahraei-Ramazani A,Wannigama DL.Phlebotominae sand fliesmorphological and molecular approaches:Morphological and genotypic variations in the population of the subgenus Adlerius(Diptera:Psychodidae:Phlebotominae).B?l?i,Moldova:LAP LAMBERT Academic Publishing;2016.
[17]Haddadzade H,Fattahi R,Mohebali M,Akhoundi B,Ebrahimzade E.Seroepidemiologcal investigation of visceral leishmaniasis in stray and owned dogs in Alborz province,central Iran using direct agglutination test.Iran J Parasitol 2013;8(1):152-157.
[18]Mohebali M,Hajjaran H,Hamzavi Y,Mobedi I,Arshi S,Zarei Z,et al.Epidemiological aspects of canine visceral leishmaniosis in the Islamic Republic of Iran.Vet Parasitol 2005;129(3-4):243-251.
[19]Sisko-Kraljevic K,Jeroncic A,Mohar B,Punda-Polic V.Asymptomatic Leishmania infantum infections in humans living in endemic and nonendemic areas of Croatia,2007 to 2009.Euro Surveill 2013;18(29):20533.
[20]Sakru N,Korkmaz M,Ozbel Y,Ertabaklar H,Sengul M,Toz SO.Investigation of asymptomatic visceral leishmaniasis cases using western blot in an endemic area in Turkey.New Microbiol 2007;30(1):13-18.
[21]Badaro R,Jones TC,Lorenco R,Cerf BJ,Sampaio D,Carvalho EM,et al.A prospective study of visceral leishmaniasis in an endemic area of Brazil.J Infect Dis 1986;154(4):639-649.
[22]Moreno J,Alvar J.Canine leishmaniasis:Epidemiological risk and the experimental model.Trends Parasitol 2002;18(9):399-405.
[23]Baneth G,Koutinas AF,Solano-Gallego L,Bourdeau P,Ferrer L.Canine leishmaniosis-new concepts and insights on an expanding zoonosis:Part one.Trends Parasitol 2008;24(7):324-330.
[24]Solano-Gallego L,Morell P,Arboix M,Alberola J,Ferrer L.Prevalence of Leishmania infantum infection in dogs living in an area of canine leishmaniasis endemicity using PCR on several tissues and serology.JClin Microbiol 2001;39(2):560-563.
[25]Sousa S,Lopes AP,Cardoso L,Silvestre R,Schallig H,Reed SG,et al.Seroepidemiological survey of Leishmania infantum infection in dogs from northeastern Portugal.Acta Trop 2011;120(1-2):82-87.
[26]Yaghoobi-Ershadi M.Phlebotomine sand flies(Diptera:Psychodidae)in Iran and their role on Leishmania transmission.J Arthropod Borne Dis2012;6(1):1-17.
[27]Azizi K,Rassi Y,Javadian E,Motazedian MH,Rafizadeh S,Yaghoobi Ershadi MR,et al.Phlebotomus(Paraphlebotomus)alexandri:A probable vector of Leishmania infantum in Iran.Ann Trop Med Parasitol 2006;100(1):63-68.
[28]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 Public Health 2004;33(4):1-2.
[29]Nadim A,Navid-Hamidid A,Javadian E,Bidruni GT,Amini H.Present status of kala-azar in Iran.Am J Trop Med Hyg 1978;27(1 Pt 1):25-28.
[30]Killick-Kendrick R.Phlebotomine vectors of the Leishmaniases:Areview.Med Vet Entomol 1990;4(1):1-24.
[31]Lesnikova EV,Sabitov EA.Evidence for the transmission of the causative agent of visceral leishmaniasis by the sandfly Phlebotomus(Adlerius)turanicus Artemiev,1974 in Turkmenistan.Med Parazitol(Mosk)1995;(3):24-28.
[32]Dergacheva TI.Ecological characteristics of subgenera Larroussius and Adelius(Diptera,Phlebotominae)sandflies-vectors for pathogens of visceral leishmaniasis.Med Parazitol(Mosk)2001;3:26-31.
[33]Kravchenko V,Wasserberg G,Warburg A.Bionomics of phlebotomine sandflies in the Galilee focus of cutaneous leishmaniasis in northern Israel.Med Vet Entomol 2004;18(4):418-428.
[34]Akhoundi M,Parvizi P,Baghaei A,Depaquit J.The subgenus Adlerius nitzulescu(Diptera,Psychodidae,Phlebotomus)in Iran.Acta Trop 2012;122(1):7-15.
[35]Depaquit J,Bounamous A,Akhoundi M,Augot D,Sauvage F,Dvorak V,et al.A taxonomic study of Phlebotomus(Larroussius)perfiliewi s.l.Infect Genet Evol 2013;20:500-508.
[36]Parvizi P,Naddaf SR,Alaeenovin E.Molecular typing and phylogenetic analysis of some species belonging to Phlebotomus(Larroussius)and Phlebotomus(Adlerius)subgenera(Diptera:Psychodidae)from two locations in Iran.Iran J Arthropod Borne Dis 2010;4(2):1-10.
[37]Oshaghi MA,Ravasan NM,Javadian EA,Mohebali M,Hajjaran H,Zare Z,et al.Vector incrimination of sand flies in the most important visceral leishmaniasis focus in Iran.Am J Trop Med Hyg 2009;81(4):572-527.
[38]Nadim A,Javadian E.Key for species identification of sandflies(Phlebotomine;Diptera)of Iran.Iran J Public Health 1976;5(1):35-44..
[39]Seyyedi Rashti MA,Nadim A.The genus Phlebotomus(Diptera:Psychodidae:Phlebotominae)of the countries of the Eastern Mediterranean Region.Iran J Publ Health 1992;21:11-50.
[40]Absavaran A,Rassi Y,Parvizi P,Oshaghi M,Abaie M,Rafizadeh S,et al.Identification of sand flies of the subgenus Larroussius based on molecular and morphological characters in north western Iran.Iran JArthropod Borne Dis 2009;3(2):22-35.
[41]Rassi Y,Dehkordi AS,Oshaghi MA,Abai MR,Mohtarami F,Enayati A,et al.First report on natural infection of the Phlebotomus tobbi by Leishmania infantum in northwestern Iran.Exp Parasitol 2012;131(3):344-349.
[42]Rassi Y,Javadian E,Nadim A,Zahraii A,Vatandoost H,Motazedian H,et al.Phlebotomus(Larroussius)kandelakii the principal and proven vector of visceral leishmaniasis in north west of Iran.Pak J Biol Sci 2005;8(12):1802-1806.
[2]World Health Organization.Fact sheet,leishmaniasis.[Online]Available from:https://www.who.int/news-room/fact-sheets/detail/Leishmaniasis.[Accessed on 10 February 2019].
[3]Masoori L,Kheirandish F,Haghighi A,Mohebali M,Akhoundi B,Taghipour N,et al.Molecular-based detection of Leishmania infantum in human blood samples in a new focus of visceral leishmaniasis in Lorestan Province,Iran.J Arthropod Borne Dis 2018;12(1):67.
[4]Mohebali M.Visceral leishmaniasis in Iran:Review of the epidemiological and clinical features.Iran J Parasitol 2013;8(3):348-358.
[5]Ready PD.Epidemiology of visceral Leishmaniasis.Clin Epidemiol 2014;6:147-154.
[6]Mohebali M,Hajjaran H,Hamzavi Y,Mobedi I,Arshi S,Zarei Z,et al.Epidemiological aspects of canine visceral leishmaniasis in the Islamic Republic of Iran.Vet parasitol 2005;129(3-4):243-251.
[7]Mohebali M,Edrissian GH,Shirzadi MR,Akhoundi B,Hajjaran H,Zarei Z,et al.An observational study on the current distribution of visceral leishmaniasis in different geographical zones of Iran and implication to health policy.Travel Med Infect Dis 2011;9(2):67-74.
[8]Sharifi I,Aflatoonian MR,Daei Parizi MH,Hosseininasab A,Mostafavi M,Bamorovat M,et al.Visceral leishmaniasis in Southeastern Iran:Anarrative review.Iran J Parasitol 2017;12(1):1-11.
[9]Ozbel Y,Oskam L,Ozensoy S,Turgay N,Alkan MZ,Jaffe CL,et al.Asurvey on canine leishmaniasis in western Turkey by parasite,DNA and antibody detection assays.Acta Trop 2000;74(1):1-6.
[10]Badirzadeh A,Mohebali M,Asadgol Z,Soong L,Zeinali M,Mokhayeri Y,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):513-518.
[11]El Harith A,Kolk A,Leeuwenburg J,Muigai R,Huigen E,Jelsma T,et al.Improvement of a direct agglutination test for field studies of visceral leishmaniasis.J Clin Microbiol 1988;26(7):1321-1325.
[12]Mohebali M.Epidemiological status of visceral leishmaniasis in Iran:experiences and review of literature.J Clinic Experiment Pathol S 2012;3143:1-5.
[13]Parvizi P,Mazloumi-Gavgani AS,Davies CR,Courtenay O,Ready PD.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):891-897.
[14]Theodor O,Mesghali A.On the Phlebotominae of Iran.J Med Entomol1964;1:285-300.
[15]Léger N,Pesson B,Madulo-Leblond G,Abonnenc E.Sur la différenciation des femelles du sous-genre larroussius nitzulescu,1931-(Diptera-Phlebotomidae)de la région méditerranéenne.Ann Parasitol Hum Comp 1983;58(6):611-623.
[16]Zahraei-Ramazani A,Wannigama DL.Phlebotominae sand fliesmorphological and molecular approaches:Morphological and genotypic variations in the population of the subgenus Adlerius(Diptera:Psychodidae:Phlebotominae).B?l?i,Moldova:LAP LAMBERT Academic Publishing;2016.
[17]Haddadzade H,Fattahi R,Mohebali M,Akhoundi B,Ebrahimzade E.Seroepidemiologcal investigation of visceral leishmaniasis in stray and owned dogs in Alborz province,central Iran using direct agglutination test.Iran J Parasitol 2013;8(1):152-157.
[18]Mohebali M,Hajjaran H,Hamzavi Y,Mobedi I,Arshi S,Zarei Z,et al.Epidemiological aspects of canine visceral leishmaniosis in the Islamic Republic of Iran.Vet Parasitol 2005;129(3-4):243-251.
[19]Sisko-Kraljevic K,Jeroncic A,Mohar B,Punda-Polic V.Asymptomatic Leishmania infantum infections in humans living in endemic and nonendemic areas of Croatia,2007 to 2009.Euro Surveill 2013;18(29):20533.
[20]Sakru N,Korkmaz M,Ozbel Y,Ertabaklar H,Sengul M,Toz SO.Investigation of asymptomatic visceral leishmaniasis cases using western blot in an endemic area in Turkey.New Microbiol 2007;30(1):13-18.
[21]Badaro R,Jones TC,Lorenco R,Cerf BJ,Sampaio D,Carvalho EM,et al.A prospective study of visceral leishmaniasis in an endemic area of Brazil.J Infect Dis 1986;154(4):639-649.
[22]Moreno J,Alvar J.Canine leishmaniasis:Epidemiological risk and the experimental model.Trends Parasitol 2002;18(9):399-405.
[23]Baneth G,Koutinas AF,Solano-Gallego L,Bourdeau P,Ferrer L.Canine leishmaniosis-new concepts and insights on an expanding zoonosis:Part one.Trends Parasitol 2008;24(7):324-330.
[24]Solano-Gallego L,Morell P,Arboix M,Alberola J,Ferrer L.Prevalence of Leishmania infantum infection in dogs living in an area of canine leishmaniasis endemicity using PCR on several tissues and serology.JClin Microbiol 2001;39(2):560-563.
[25]Sousa S,Lopes AP,Cardoso L,Silvestre R,Schallig H,Reed SG,et al.Seroepidemiological survey of Leishmania infantum infection in dogs from northeastern Portugal.Acta Trop 2011;120(1-2):82-87.
[26]Yaghoobi-Ershadi M.Phlebotomine sand flies(Diptera:Psychodidae)in Iran and their role on Leishmania transmission.J Arthropod Borne Dis2012;6(1):1-17.
[27]Azizi K,Rassi Y,Javadian E,Motazedian MH,Rafizadeh S,Yaghoobi Ershadi MR,et al.Phlebotomus(Paraphlebotomus)alexandri:A probable vector of Leishmania infantum in Iran.Ann Trop Med Parasitol 2006;100(1):63-68.
[28]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 Public Health 2004;33(4):1-2.
[29]Nadim A,Navid-Hamidid A,Javadian E,Bidruni GT,Amini H.Present status of kala-azar in Iran.Am J Trop Med Hyg 1978;27(1 Pt 1):25-28.
[30]Killick-Kendrick R.Phlebotomine vectors of the Leishmaniases:Areview.Med Vet Entomol 1990;4(1):1-24.
[31]Lesnikova EV,Sabitov EA.Evidence for the transmission of the causative agent of visceral leishmaniasis by the sandfly Phlebotomus(Adlerius)turanicus Artemiev,1974 in Turkmenistan.Med Parazitol(Mosk)1995;(3):24-28.
[32]Dergacheva TI.Ecological characteristics of subgenera Larroussius and Adelius(Diptera,Phlebotominae)sandflies-vectors for pathogens of visceral leishmaniasis.Med Parazitol(Mosk)2001;3:26-31.
[33]Kravchenko V,Wasserberg G,Warburg A.Bionomics of phlebotomine sandflies in the Galilee focus of cutaneous leishmaniasis in northern Israel.Med Vet Entomol 2004;18(4):418-428.
[34]Akhoundi M,Parvizi P,Baghaei A,Depaquit J.The subgenus Adlerius nitzulescu(Diptera,Psychodidae,Phlebotomus)in Iran.Acta Trop 2012;122(1):7-15.
[35]Depaquit J,Bounamous A,Akhoundi M,Augot D,Sauvage F,Dvorak V,et al.A taxonomic study of Phlebotomus(Larroussius)perfiliewi s.l.Infect Genet Evol 2013;20:500-508.
[36]Parvizi P,Naddaf SR,Alaeenovin E.Molecular typing and phylogenetic analysis of some species belonging to Phlebotomus(Larroussius)and Phlebotomus(Adlerius)subgenera(Diptera:Psychodidae)from two locations in Iran.Iran J Arthropod Borne Dis 2010;4(2):1-10.
[37]Oshaghi MA,Ravasan NM,Javadian EA,Mohebali M,Hajjaran H,Zare Z,et al.Vector incrimination of sand flies in the most important visceral leishmaniasis focus in Iran.Am J Trop Med Hyg 2009;81(4):572-527.
[38]Nadim A,Javadian E.Key for species identification of sandflies(Phlebotomine;Diptera)of Iran.Iran J Public Health 1976;5(1):35-44..
[39]Seyyedi Rashti MA,Nadim A.The genus Phlebotomus(Diptera:Psychodidae:Phlebotominae)of the countries of the Eastern Mediterranean Region.Iran J Publ Health 1992;21:11-50.
[40]Absavaran A,Rassi Y,Parvizi P,Oshaghi M,Abaie M,Rafizadeh S,et al.Identification of sand flies of the subgenus Larroussius based on molecular and morphological characters in north western Iran.Iran JArthropod Borne Dis 2009;3(2):22-35.
[41]Rassi Y,Dehkordi AS,Oshaghi MA,Abai MR,Mohtarami F,Enayati A,et al.First report on natural infection of the Phlebotomus tobbi by Leishmania infantum in northwestern Iran.Exp Parasitol 2012;131(3):344-349.
[42]Rassi Y,Javadian E,Nadim A,Zahraii A,Vatandoost H,Motazedian H,et al.Phlebotomus(Larroussius)kandelakii the principal and proven vector of visceral leishmaniasis in north west of Iran.Pak J Biol Sci 2005;8(12):1802-1806.