Abstract
Leishmania (Leishmania) major has been identified as the major causative agent of cutaneous leishmaniasis in Sindh Province of southern Pakistan. To make a rational approach for understanding the pathogen transmission cycles, the sand fly species and their natural blood meals in the endemic areas were examined. Total DNA was individually extracted from sand flies collected in four villages in Sindh Province. PCR–RFLP (restriction fragment length polymorphism) and sequence analysis of the 18S ribosomal RNA gene revealed that female sand flies identified were Sergentomyia clydei/Sergentomyia ghesquierei/Sergentomyia magna (68.6%), Sergentomyia dubia (17.1%), Phlebotomus papatasi (7.4%), Phlebotomus alexandri-like sand flies (3.4%) and Sergentomyia dentata (3.4%). PCR amplification of leishmanial kinetoplast DNA did not result in positive signals, suggesting that all 175 tested female sand flies were not infected with leishmanial parasites or contained undetectable levels of leishmanial DNA. Amplification and sequencing of the vertebrate cytochrome b gene in 28 blood-fed sand flies revealed that P. papatasi fed on cattle and wild rat whereas P. alexandri-like specimens fed on human, cattle, goat and dog. Although Sergentomyia sand flies are generally known to feed on cold-blooded animals, S. clydei, S. dubia and S. ghesquierei preferred humans, cattle, goat, sheep, buffalo, dog, donkey, wild rat and Indian gerbil. The epidemiological significance of the zoophilic feeding on various host species by Phlebotomus and Sergentomyia sand flies in Pakistan is further required to study for better understanding the zoonotic transmission of sand-fly-borne pathogens and for appropriate management of the vectors.
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References
Abbasi I, Cunio R, Warburg A (2009) Identification of blood meals imbibed by phlebotomine sand flies using cytochrome b PCR and reverse line blotting. Vector Borne Zoon Dis 9:79–86
Alexander B (2000) Sampling methods for phlebotomine sandflies. Med Vet Entomol 14:109–122
Alexander B, Maroli M (2003) Control of phlebotomine sandflies. Med Vet Entomol 17:1–18
Amaro F, Ciufolini MG, Venturi G, Fiorentini C, Alves MJ (2007) Phleboviruses laboratorial diagnosis (Toscana virus). Acta Med Port 20:341–345
Aransay AM, Scoulica E, Chaniotis B, Tselentis Y (1999) Typing of sandflies from Greece and Cyprus by DNA polymorphism of 18S rRNA gene. Insect Mol Biol 8:179–184
Aransay AM, Scoulica E, Tselentis Y, Ready PD (2000) Phylogenetic relationship of phlebotomine sandflies inferred from small subunit nuclear ribosomal DNA. Insect Mol Biol 9:157–168
Azizi K, Rassi Y, Javadian E, Motazedian MH, Rafizadeh S, Yaghoobi-Ershadi MR, Mohebali M (2006) Phlebotomus (Paraphlebotomus) alexandri: a probable vector of Leishmania infantum in Iran. Ann Trop Med Parasitol 100:63–68
Bhutto AM, Soomro FR, Katakura K (2008) Leishmaniasis in Sindh, Pakistan: outbreak and review of the literature. J Pak Assoc Dermatol 18:212–219
Bhutto AM, Soomro FR, Baloch JH, Matsumoto J, Uezato H, Hashiguchi Y, Katakura K (2009) Cutaneous leishmaniasis caused by Leishmania (L.) major infection in Sindh province, Pakistan. Acta Trop 111:295–298
Boakye DA, Tang J, Truc P, Merriweather A, Unnasch TR (1999) Identification of bloodmeals in haematophagous Diptera by cytochrome B heteroduplex analysis. Med Vet Entomol 13:282–287
Boussaa S, Boumezzough A, Sibold B, Alves-Pires C, Marquez FM, Glasser N, Pesson B (2009) Phlebotomine sandflies (Diptera: Psychodidae) of the genus Sergentomyia in Marrakech region, Morocco. Parasitol Res 104:1027–1033
Charrel RN, Izri A, Temmam S, de Lamballerie X, Parola P (2006) Toscana virus RNA in Sergentomyia minuta flies. Emerg Infect Dis 12:1299–1300
Desjeux P (2004) Leishmaniasis: current situation and new perspectives. Comp Immun Microbiol Infect Dis 27:305–318
El-Badry A, Al-Juhani A, Ibrahim EK, Al-Zubiany S (2008) Distribution of sand flies in El-Nekheil province, in Al-Madinah Al-Munawwarah region, western of Saudi Arabia. Parasitol Res 103:151–156
Geevarghese G, Arankalle VA, Jadi R, Kanojia PC, Joshi MV, Mishra AC (2005) Detection of Chandipura virus from sand flies in the genus Sergentomyia (Diptera: Phlebotomidae) at Karimnagar District, Andhra Pradesh, India. J Med Entomol 42:495–496
Guan LR, Xu YX, Li BS, Dong J (1986) The role of Phlebotomus alexandri Sinton, 1928 in the transmission of kala-azar. Bull World Health Org 64:107–112
Katakura K (2009) Molecular epidemiology of leishmaniasis in Asia (focus on cutaneous infections). Curr Opin Infect Dis 22:126–130
Kato H, Uezato H, Katakura K, Calvopiña M, Marco JD, Barroso PA, Gomez EA, Mimori T, Korenaga M, Iwata H, Nonaka S, Hashiguchi Y (2005) Detection and identification of Leishmania species within naturally infected sandflies in the Andean areas of Ecuador by a polymerase chain reaction. AmJTrop Med Hyg 72:87–93
Kato H, Uezato H, Gomez EA, Terayama Y, Calvopiña M, Iwata H, Hashiguchi Y (2007) Establishment of a mass screening method of sand fly vectors for Leishmania infection by molecular biological methods. AmJTrop Med Hyg 77:324–329
Killick-Kendrick R (1999) The biology and control of phlebotomine sandflies. Clin Dermatol 17:279–289
Konnai S, Mekata H, Odbileg R, Simuunza M, Chembensof M, Witola WH, Tembo ME, Chitambo H, Inoue N, Onuma M, Ohashi K (2008) Detection of Trypanosoma brucei in field-captured tsetse flies and identification of host species fed on by the infected flies. Vector Borne Zoon Dis 8:565–573
Lewis DJ (1974) The biology of Phlebotomidae in relation to leishmaniasis. Annu Rev Entomol 19:363–384
Lewis DJ (1982) A taxonomic review of the genus Phlebotomus (Diptera: Psychodidae). Bull Br Mus Nat Hist (Entomol) 45:121–209
Lewis DJ, Dyce AL (1988) Taxonomy of the Australian Phlebotominae (Diptera: Psychodidae) with revision of genus Sergentomyia from the region. Invert Taxon 2:755–804
Mahboudi F, Abolhassan M, Yaran M, Mobtaker H, Azizi M (2001) Identification and differentiation of Iranian Leishmania species by PCR amplification of kDNA. Scand J Infect Dis 33:596–598
Marco JD, Bhutto AM, Soomro FR, Baloch JH, Barroso PA, Kato H, Uezato H, Katakura K, Korenaga M, Nonaka S, Hashiguchi Y (2006) Multilocus enzyme electrophoresis and cytochrome b gene sequencing-based identification of Leishmania isolates from different foci of cutaneous leishmaniasis in Pakistan. AmJTrop Med Hyg 75:261–266
Molaei G, Andreadis TG, Armstrong PM, Anderson JF, Vossbrinck CR (2006) Host feeding patterns of Culex mosquitoes and West Nile virus transmission, northeastern United States. Emerg Infect Dis 12:468–474
Mukherjee S, Hassan MQ, Ghosh A, Ghosh KN, Bhattacharya A, Adhya S (1977) Short Report: Leishmania DNA in Phlebotomus and Sergentomyia species during a kala-azar epidemic. AmJTrop Med Hyg 57:423–425
Myint CK, Asato Y, Yamamoto Y, Kato H, Bhutto AM, Soomro FR, Memon MZ, Matsumoto J, Marco JD, Oshiro M, Katakura K, Hashiguchi Y, Uezato H (2008) Polymorphisms of cytochrome b gene in Leishmania parasites and their relation to types of cutaneous leishmaniasis lesions in Pakistan. J Dermatol 35:76–85
Pandey K, Pant S, Kanbara H, Shuaibu MN, Mallik AK, Pandey BD, Kaneko O, Yanagi T (2008) Molecular detection of Leishmania parasites from whole bodies of sandflies collected in Nepal. Parasitol Res 103:293–297
Parvizi P, Amirkhani A (2008) Mitochondrial DNA characterization of Sergentomyia sintoni populations and finding mammalian Leishmania infections in this sandfly by using ITS-rDNA gene. Iran J Vet Res 9:9–18
Sawabe K, Isawa H, Hoshino K, Sasaki T, Roychoudhury S, Higa Y, Kasai S, Tsuda Y, Nishiumi I, Hisai N, Hamao S, Kobayashi M (2010) Host-feeding habits of Culex pipiens and Aedes albopictus (Diptera: Culicidae) collected at the urban and suburban residential areas of Japan. J Med Entomol 47:442–450
Shakila A, Bilqees FM, Salim A, Moinuddin M (2006) Geographic distribution of cutaneous leishmaniasis and sand flies in Pakistan. Acta Parasitol Turcica 30:1–6
Steuber S, Abdel-Rady A, Clausen PH (2005) PCR–RFLP analysis: a promising technique for host species identification of blood meals from tsetse flies (Diptera: Glossinidae). Parasitol Res 97:247–254
Vincze T, Posfai J, Roberts RJ (2003) NEB cutter: a program to cleave DNA with restriction enzymes. Nucleic Acids Res 31:3688–3691
Yaghoobi-Ershadi MR, Javadian E, Kannani A (1995) Host preference pattern of phlebotomine sandflies of Borkhar rural district, Isfahan Province, Iran. Acta Trop 60:155–158
Acknowledgements
We acknowledge all staff of the Department of Dermatology and Leprosy Centre, Chandka Medical College/Hospital and Regional Health Office of Larkana district, Pakistan, for providing facilities, coordinating field activities and supporting specimen collection. We also thank Dr. Kato of Hokkaido University for valuable suggestion and Ms. Kotera for technical assistance. This work was supported in part by grants from the 21st Century COE program ‘Program of Excellence for Zoonosis Control’, global COE program ‘Establishment of International Collaboration Centres for Zoonosis Control’ and grant no. 183801780 from MEXT, Japan.
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Tiwananthagorn, S., Bhutto, A.M., Baloch, J.H. et al. Zoophilic feeding behaviour of phlebotomine sand flies in the endemic areas of cutaneous leishmaniasis of Sindh Province, Pakistan. Parasitol Res 111, 125–133 (2012). https://doi.org/10.1007/s00436-011-2808-3
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DOI: https://doi.org/10.1007/s00436-011-2808-3