ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Joshi A, Narain JP, Prasittisuk C, Bhatia R, Hashim G, Jorge A, Banjara M, Kroeger A, 2008. Can visceral leishmaniasis be eliminated from Asia? J Vector Borne Dis 45: 105–111.
-
2.
Sundar S, Mondal D, Rijal S, Bhattacharya S, Ghalib H, Kroeger A, Boelaert M, Desjeux P, Richter-Airijoki H, Harms G, 2008. Implementation research to support the initiative on the elimination of kala azar from Bangladesh, India and Nepal—the challenges for diagnosis and treatment. Trop Med Int Health 13: 2–5.
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3.
Bern C, Chowdhury R, 2006. The epidemiology of visceral leishmaniasis in Bangladesh: prospects for improved control. Indian J Med Res 123: 275–288.
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4.
Salam MA, Khan MG, Bhaskar KR, Afrad MH, Huda MM, Mondal D, 2012. Peripheral blood buffy coat smear: a promising tool for diagnosis of visceral leishmaniasis. J Clin Microbiol 50: 837–840.
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5.
Dantas-Torres F, de Brito ME, Brandão-Filho SP, 2006. Seroepidemiological survey on canine leishmaniasis among dogs from an urban area of Brazil. Vet Parasitol 140: 54–60.
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Desjeux P, 2004. Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 27: 305–318.
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7.
Shamboul KM, El Bagir AM, El Sayed MO, Saeed SAK, Abdalla H, Omran OF, 2009. Identification of Leishmania donovani from infected dogs at a dormant focus of VL in Blue Nile State, Sudan. J Genet Eng Biotechnol 7: 27–31.
-
8.
Kalayou S, Tadelle H, Bsrat A, Abebe N, Haileselassie M, Schallig HD, 2011. Serological evidence of Leishmania donovani infection in apparently healthy dogs using direct agglutination test (DAT) and rk39 dipstick tests in Kafta Humera, north-west Ethiopia. Transbound Emerg Dis 58: 255–262.
-
9.
Dereure J, El-Safi SH, Bucheton B, Boni M, Kheir MM, Davoust B, Pratlong F, Feugier E, Lambert M, Dessein A, Dedet JP, 2003. Visceral leishmaniasis in eastern Sudan: parasite identification in humans and dogs; host-parasite relationships. Microbes Infect 5: 1103–1108.
-
10.
Nawaratna SS, Weilgama DJ, Rajapaksha K, 2009. Cutaneous leishmaniasis in Sri Lanka: a study of possible animal reservoirs. Int J Infect Dis 13: 513–517.
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11.
Bhattarai NR, Auwera GV, Rijal S, Picado A, Speybroeck N, Khanal B, De Doncker S, Das ML, Ostyn B, Davies C, Coosemans M, Berkvens D, Boelaert M, Dujardin JC, 2010. Domestic animals and epidemiology of visceral leishmaniasis, Nepal. Emerg Infect Dis 16: 231–237.
-
12.
Sharma NL, Mahajan VK, Negi AK, Verma GK, 2009. The rK39 immunochromatic dipstick testing: a study for K39 seroprevalence in dogs and human leishmaniasis patients for possible animal reservoir of cutaneous and visceral leishmaniasis in endemic focus of Satluj river valley of Himachal Pradesh (India). Indian J Dermatol Venereol Leprol 75: 52–55.
-
13.
Alam MS, Ghosh D, Khan MG, Islam MF, Mondal D, Itoh M, Haque R, 2011. Survey of domestic cattle for anti-Leishmania antibodies and Leishmania DNA in a visceral leishmaniasis endemic area of Bangladesh. BMC Vet Res 7: 27.
-
14.
Alam MZ, Yasin MG, Kato H, Sakurai T, Katakura K, 2013. PCR-based detection of Leishmania donovani DNA in a stray dog from a visceral leishmaniasis endemic focus in Bangladesh. J Vet Med Sci 75: 75–78.
-
15.
Burns JM Jr, Shreffler WG, Benson DR, Ghalib HW, Badaro R, Reed SG, 1993. Molecular antibody in African and American visceral leishmaniasis. Proc Natl Acad Sci USA 90: 775–779.
-
16.
Schönian G, Nasereddin A, Dinse N, Schweynoch C, Schallig HD, Presber W, Jaffe CL, 2003. PCR diagnosis and characterization of Leishmania in local and imported clinical samples. Diagn Microbiol Infect Dis 47: 349–358.
-
17.
Mary C, Faraut F, Lascombe L, Dumon H, 2004. Quantification of Leishmania infantum DNA by a real-time PCR assay with high sensitivity. J Clin Microbiol 42: 5249–5255.
-
18.
Hall T, 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98.
-
19.
Altman DG, 2001. Practical Statistics for Medical Research. London, United Kingdom: Chapman and Hall.
-
20.
Gavgani AS, Mohite H, Edrissian GH, Mohebali M, Davies CR, 2002. Domestic dog ownership in Iran is a risk factor for human infection with Leishmania infantum. Am J Trop Med Hyg 67: 511–515.
-
21.
Dereure J, Boni M, Pratlong F, Osman M, Boucheton B, El-Safi S, Feugier E, Musa MK, Daroust B, Dessein A, Dededt JP, 2000. Visceral leishmaniasis in Sudan: first identification of Leishmania from dogs. Trans R Soc Trop Med Hyg 94: 154–155.
-
22.
Hassan MM, Osman OF, El-Raba'a FM, Schallig HD, Elnaiem DE, 2009. Role of the domestic dog as a reservoir host of Leishmania donovani in eastern Sudan. Parasit Vectors 2: 26.
-
23.
Karayiannis S, Ntais P, Messaritakis I, Tsirigotakis N, Dokianakis E, Antoniou M, 2015. Detection of Leishmania infantum in red foxes (Vulpes vulpes) in Central Greece. Parasitology 142: 1574–1578.
-
24.
Pasa S, Vardarl AT, Erol N, Karakus M, Toz S, Atasoy A, Balcıoğlu IC, Tuna GE, Ermis OV, Ertabaklar H, Ozbel Y, 2015. Detection of Leishmania major and Leishmania tropica in domestic cats in the Ege Region of Turkey. Vet Parasitol 212: 389–392.
-
25.
Oliveira FM, Costa LH, Barros TL, Ito PKRK, Colombo FA, Carvalhoa C, Pedroa WA, Queiroza LH, Nunesa CM, 2015. First detection of Leishmania spp. DNA in Brazilian bats captured strictly in urban areas. Acta Trop 150: 176–181.
-
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Singh N, Mishra J, Singh R, Singh S, 2013. Animal reservoirs of visceral leishmaniasis in Bihar. Indian J Parasitol 99: 64–67.
-
27.
Lachaud L, Chabbert E, Dubessay P, Reynes J, Lamothe J, Bastein P, 2001. Comparison of various sample preparation methods of PCR diagnosis of visceral leishmaniasis using peripheral blood. J Clin Microbiol 38: 613–617.
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Sundar S, Rai M, 2002. Laboratory diagnosis of visceral leishmaniasis. Clin Diagn Lab Immunol 9: 951–958.
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29.
Fallah E, Khanmohammadi M, Rahbari S, Farshchian M, Farajnia S, Hamzavi F, Mohammadpour A, 2011. Serological survey and comparison of two polymerase chain reaction (PCR) assays with enzyme-linked immunosorbent assay (ELISA) for the diagnosis of canine visceral leishmaniasis in dogs. Afr J Biotechnol 10: 648–656.
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Mohammadiha A, Mohebali M, Haghighi A, Mandian R, Abadi AR, Zarei Z, Yeganeh F, Kazemi B, Taghipour N, Akhoundi B, 2013. Comparison of real-time PCR and conventional PCR with two DNA targets for detection of Leishmania (Leishmania) infantum infection in human and dog blood samples. Exp Parasitol 133: 89–94.
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Molecular and Serological Evidence of Leishmania Infection in Stray Dogs from Visceral Leishmaniasis–Endemic Areas of Bangladesh
Shirin Akter
Shirin Akter
Laboratory of Parasitology, Department of Disease Control, Graduate School of Veterinary Medicine, Hokkaido University, Hokkaido, Japan.
Department of Parasitology, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh, Bangladesh.
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Mohammad Zahangir Alam
Mohammad Zahangir Alam
Department of Parasitology, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh, Bangladesh.
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Ryo Nakao
Ryo Nakao
Laboratory of Parasitology, Department of Disease Control, Graduate School of Veterinary Medicine, Hokkaido University, Hokkaido, Japan.
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Md. Golam Yasin
Md. Golam Yasin
Department of Parasitology, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh, Bangladesh.
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Hirotomo Kato
Hirotomo Kato
Laboratory of Parasitology, Department of Disease Control, Graduate School of Veterinary Medicine, Hokkaido University, Hokkaido, Japan.
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Ken Katakura
Ken Katakura
Laboratory of Parasitology, Department of Disease Control, Graduate School of Veterinary Medicine, Hokkaido University, Hokkaido, Japan.
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Visceral leishmaniasis (VL), or kala-azar, is mainly caused by two closely related Leishmania species, Leishmania infantum and Leishmania donovani. Leishmania infantum is responsible for zoonotic VL, with dogs as the main reservoir host in the Mediterranean, the Middle East, Asia, and South America. In the Indian subcontinent, VL is caused by L. donovani and is considered anthroponotic, although the only known vector, the sand fly, is zoophilic in nature. The role of domestic and stray dogs in VL transmission is still unclear in this area. We screened 50 stray dogs from VL-endemic areas of Bangladesh for serological and molecular evidence of Leishmania infection. We detected anti-Leishmania antibodies in six (12%) dog serum samples using rK39 immunochromatographic tests. We observed Leishmania kinetoplast DNA in 10 (20%) buffy coat DNA samples by real-time polymerase chain reaction (PCR), five of which were positive based on internal transcribed spacer 1-PCR. A sequencing analysis of the amplified products confirmed that the parasitic DNA was derived from L. donovani. Our findings support the hypothesis that stray dogs are an animal reservoir for L. donovani in this endemic region. Further studies are required to determine the precise role of dogs in the epidemiology of VL in Bangladesh.
Author Notes
Financial support: This work was supported in part by the Global Center of Excellence Program for International Collaboration Centers for Zoonosis Control, JSPS KAKENHI grant nos. 22405037 and 24380163 from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT) and a special grant by the Program for Leading Graduate Schools “Fostering Global Leaders in Veterinary Science for Contributing to One Health” (F01), MEXT, Japan.
Authors' addresses: Shirin Akter, Laboratory of Parasitology, Department of Disease Control, Graduate School of Veterinary Medicine, Hokkaido University, Hokkaido, Japan, and Department of Parasitology, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh, Bangladesh, E-mail: shirin@vetmed.hokudai.ac.jp. Mohammad Zahangir Alam and Md. Golam Yasin, Department of Parasitology, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh, Bangladesh, E-mails: mzalam@bau.edu.bd and golam.yasin@yahoo.com. Ryo Nakao, Hirotomo Kato, and Ken Katakura, Laboratory of Parasitology, Department of Disease Control, Graduate School of Veterinary Medicine, Hokkaido University, Hokkaido, Japan, E-mails: ryo.nakao@vetmed.hokudai.ac.jp, hkato@vetmed.hokudai.ac.jp, and kenkata@vetmed.hokudai.ac.jp.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Joshi A, Narain JP, Prasittisuk C, Bhatia R, Hashim G, Jorge A, Banjara M, Kroeger A, 2008. Can visceral leishmaniasis be eliminated from Asia? J Vector Borne Dis 45: 105–111.
-
2.
Sundar S, Mondal D, Rijal S, Bhattacharya S, Ghalib H, Kroeger A, Boelaert M, Desjeux P, Richter-Airijoki H, Harms G, 2008. Implementation research to support the initiative on the elimination of kala azar from Bangladesh, India and Nepal—the challenges for diagnosis and treatment. Trop Med Int Health 13: 2–5.
-
3.
Bern C, Chowdhury R, 2006. The epidemiology of visceral leishmaniasis in Bangladesh: prospects for improved control. Indian J Med Res 123: 275–288.
-
4.
Salam MA, Khan MG, Bhaskar KR, Afrad MH, Huda MM, Mondal D, 2012. Peripheral blood buffy coat smear: a promising tool for diagnosis of visceral leishmaniasis. J Clin Microbiol 50: 837–840.
-
5.
Dantas-Torres F, de Brito ME, Brandão-Filho SP, 2006. Seroepidemiological survey on canine leishmaniasis among dogs from an urban area of Brazil. Vet Parasitol 140: 54–60.
-
6.
Desjeux P, 2004. Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 27: 305–318.
-
7.
Shamboul KM, El Bagir AM, El Sayed MO, Saeed SAK, Abdalla H, Omran OF, 2009. Identification of Leishmania donovani from infected dogs at a dormant focus of VL in Blue Nile State, Sudan. J Genet Eng Biotechnol 7: 27–31.
-
8.
Kalayou S, Tadelle H, Bsrat A, Abebe N, Haileselassie M, Schallig HD, 2011. Serological evidence of Leishmania donovani infection in apparently healthy dogs using direct agglutination test (DAT) and rk39 dipstick tests in Kafta Humera, north-west Ethiopia. Transbound Emerg Dis 58: 255–262.
-
9.
Dereure J, El-Safi SH, Bucheton B, Boni M, Kheir MM, Davoust B, Pratlong F, Feugier E, Lambert M, Dessein A, Dedet JP, 2003. Visceral leishmaniasis in eastern Sudan: parasite identification in humans and dogs; host-parasite relationships. Microbes Infect 5: 1103–1108.
-
10.
Nawaratna SS, Weilgama DJ, Rajapaksha K, 2009. Cutaneous leishmaniasis in Sri Lanka: a study of possible animal reservoirs. Int J Infect Dis 13: 513–517.
-
11.
Bhattarai NR, Auwera GV, Rijal S, Picado A, Speybroeck N, Khanal B, De Doncker S, Das ML, Ostyn B, Davies C, Coosemans M, Berkvens D, Boelaert M, Dujardin JC, 2010. Domestic animals and epidemiology of visceral leishmaniasis, Nepal. Emerg Infect Dis 16: 231–237.
-
12.
Sharma NL, Mahajan VK, Negi AK, Verma GK, 2009. The rK39 immunochromatic dipstick testing: a study for K39 seroprevalence in dogs and human leishmaniasis patients for possible animal reservoir of cutaneous and visceral leishmaniasis in endemic focus of Satluj river valley of Himachal Pradesh (India). Indian J Dermatol Venereol Leprol 75: 52–55.
-
13.
Alam MS, Ghosh D, Khan MG, Islam MF, Mondal D, Itoh M, Haque R, 2011. Survey of domestic cattle for anti-Leishmania antibodies and Leishmania DNA in a visceral leishmaniasis endemic area of Bangladesh. BMC Vet Res 7: 27.
-
14.
Alam MZ, Yasin MG, Kato H, Sakurai T, Katakura K, 2013. PCR-based detection of Leishmania donovani DNA in a stray dog from a visceral leishmaniasis endemic focus in Bangladesh. J Vet Med Sci 75: 75–78.
-
15.
Burns JM Jr, Shreffler WG, Benson DR, Ghalib HW, Badaro R, Reed SG, 1993. Molecular antibody in African and American visceral leishmaniasis. Proc Natl Acad Sci USA 90: 775–779.
-
16.
Schönian G, Nasereddin A, Dinse N, Schweynoch C, Schallig HD, Presber W, Jaffe CL, 2003. PCR diagnosis and characterization of Leishmania in local and imported clinical samples. Diagn Microbiol Infect Dis 47: 349–358.
-
17.
Mary C, Faraut F, Lascombe L, Dumon H, 2004. Quantification of Leishmania infantum DNA by a real-time PCR assay with high sensitivity. J Clin Microbiol 42: 5249–5255.
-
18.
Hall T, 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98.
-
19.
Altman DG, 2001. Practical Statistics for Medical Research. London, United Kingdom: Chapman and Hall.
-
20.
Gavgani AS, Mohite H, Edrissian GH, Mohebali M, Davies CR, 2002. Domestic dog ownership in Iran is a risk factor for human infection with Leishmania infantum. Am J Trop Med Hyg 67: 511–515.
-
21.
Dereure J, Boni M, Pratlong F, Osman M, Boucheton B, El-Safi S, Feugier E, Musa MK, Daroust B, Dessein A, Dededt JP, 2000. Visceral leishmaniasis in Sudan: first identification of Leishmania from dogs. Trans R Soc Trop Med Hyg 94: 154–155.
-
22.
Hassan MM, Osman OF, El-Raba'a FM, Schallig HD, Elnaiem DE, 2009. Role of the domestic dog as a reservoir host of Leishmania donovani in eastern Sudan. Parasit Vectors 2: 26.
-
23.
Karayiannis S, Ntais P, Messaritakis I, Tsirigotakis N, Dokianakis E, Antoniou M, 2015. Detection of Leishmania infantum in red foxes (Vulpes vulpes) in Central Greece. Parasitology 142: 1574–1578.
-
24.
Pasa S, Vardarl AT, Erol N, Karakus M, Toz S, Atasoy A, Balcıoğlu IC, Tuna GE, Ermis OV, Ertabaklar H, Ozbel Y, 2015. Detection of Leishmania major and Leishmania tropica in domestic cats in the Ege Region of Turkey. Vet Parasitol 212: 389–392.
-
25.
Oliveira FM, Costa LH, Barros TL, Ito PKRK, Colombo FA, Carvalhoa C, Pedroa WA, Queiroza LH, Nunesa CM, 2015. First detection of Leishmania spp. DNA in Brazilian bats captured strictly in urban areas. Acta Trop 150: 176–181.
-
26.
Singh N, Mishra J, Singh R, Singh S, 2013. Animal reservoirs of visceral leishmaniasis in Bihar. Indian J Parasitol 99: 64–67.
-
27.
Lachaud L, Chabbert E, Dubessay P, Reynes J, Lamothe J, Bastein P, 2001. Comparison of various sample preparation methods of PCR diagnosis of visceral leishmaniasis using peripheral blood. J Clin Microbiol 38: 613–617.
-
28.
Sundar S, Rai M, 2002. Laboratory diagnosis of visceral leishmaniasis. Clin Diagn Lab Immunol 9: 951–958.
-
29.
Fallah E, Khanmohammadi M, Rahbari S, Farshchian M, Farajnia S, Hamzavi F, Mohammadpour A, 2011. Serological survey and comparison of two polymerase chain reaction (PCR) assays with enzyme-linked immunosorbent assay (ELISA) for the diagnosis of canine visceral leishmaniasis in dogs. Afr J Biotechnol 10: 648–656.
-
30.
Mohammadiha A, Mohebali M, Haghighi A, Mandian R, Abadi AR, Zarei Z, Yeganeh F, Kazemi B, Taghipour N, Akhoundi B, 2013. Comparison of real-time PCR and conventional PCR with two DNA targets for detection of Leishmania (Leishmania) infantum infection in human and dog blood samples. Exp Parasitol 133: 89–94.
-
31.
Bensoussan E, Nasereddin A, Jonas F, Schnur LF, Jaffe CL, 2006. Comparison of PCR assays for diagnosis of cutaneous leishmaniasis. J Clin Microbiol 44: 1435–1439.
-
32.
Hamarsheh O, Nasereddin A, Damaj S, Sawalha S, Al-Jawabreh H, Azmi K, Amro A, Ereqat S, Abdeen Z, Al-Jawabreh A, 2012. Serological and molecular survey of Leishmania parasites in apparently healthy dogs in the West Bank, Palestine. Parasit Vectors 5: 183.
-
33.
Wang JY, Ha Y, Gao CH, Wang Y, Yang YT, Chen HT, 2011. The prevalence of canine Leishmania infantum infection in western China detected by PCR and serological tests. Parasit Vectors 4: 69.
-
34.
Massunari GK, Voltarelli EM, dos Santos DR, dos Santos AR, Poiani LP, de Oliveira O, Violato RJ, Matsuo R, Teodoro U, Lonardoni MV, Silveira TG, 2009. A serological and molecular investigation of American cutaneous leishmaniasis in dogs, three years after an outbreak in the northwest of Paran'a State, Brazil. Cad Saude Publica 25: 97–104.
-
35.
Lemos EM, Laurenti MD, Moreira MAB, Reis AB, Giunchetti RC, 2008. Canine visceral leishmaniasis: performance of a rapid diagnostic test (Kalazar Detect™) in dogs with and without signs of the disease. Acta Trop 107: 205–207.
-
36.
Lima VMF, Fattori KR, Michelin AF, Neto LS, Vasconcelos RO, 2010. Comparison between ELISA using total antigen and immunochromatography with antigen rK39 in the diagnosis of canine visceral leishmaniasis. Vet Parasitol 173: 330–333.
-
37.
Quinnell RJ, Carson C, Reithinger R, Garcez LM, Courtenay O, 2013. Evaluation of rK39 rapid diagnostic tests for canine visceral leishmaniasis: longitudinal study and meta-analysis. PLoS Negl Trop Dis 7: e1992.
-
38.
Mettler M, Grimm F, Capelli G, Camp H, Deplazes P, 2005. Evaluation of enzyme-linked immunosorbent assays, an immunofluorescent-antibody test, and two rapid tests (immunochromatographic-dipstick and gel tests) for serological diagnosis of symptomatic and asymptomatic Leishmania infections in dogs. J Clin Microbiol 43: 5515–5519.
-
39.
Chance ML, Evans DA, 1999. The leishmaniases—the agent. Gilles HM, ed. Protozoal Diseases. London, United Kingdom: Arnold, 419–425.
-
40.
Paltrinieri S, Solano-Gallego L, Fondati A, Lubas G, Gradoni L, Castagnaro M, Crotti A, Maroli M, Oliva G, Roura X, Zatelli A, Zini E, 2010. Guidelines for diagnosis and clinical classification of leishmaniasis in dogs. J Am Vet Med Assoc 236: 1184–1191.
-
41.
Duprey ZH, Steurer FJ, Rooney JA, Kirchhoff LV, Jackson JE, Rowton ED, Schantz PM, 2006. Canine visceral leishmaniasis, United States and Canada, 2000–2003. Emerg Infect Dis 12: 440–446.
-
42.
Haddadzade HR, Fattahi R, Mohebali M, Akhoundi B, Ebrahimzade E, 2013. Seroepidemiological investigation of visceral leishmaniasis in stray and owned dogs in Albroz Province, central Iran using direct agglutination test. Iran J Parasitol 8: 152–157.
-
43.
Mohebali M, Hajjaran H, Hamzavi Y, Mobedi I, Arshi S, Zarei Z, Akhoundi B, Naeini KM, Avizeh R, Fakhar M, 2005. Epidemiological aspects of canine visceral leishmaniosis in the Islamic Republic of Iran. Vet Parasitol 129: 243–251.
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