Skip to main content Accessibility help
×
Home

Transmission, reservoir hosts and control of zoonotic visceral leishmaniasis

  • R. J. QUINNELL (a1) and O. COURTENAY (a2)

Summary

Zoonotic visceral leishmaniasis (ZVL) caused by Leishmania infantum is an important disease of humans and dogs. Here we review aspects of the transmission and control of ZVL. Whilst there is clear evidence that ZVL is maintained by sandfly transmission, transmission may also occur by non-sandfly routes, such as congenital and sexual transmission. Dogs are the only confirmed primary reservoir of infection. Meta-analysis of dog studies confirms that infectiousness is higher in symptomatic infection; infectiousness is also higher in European than South American studies. A high prevalence of infection has been reported from an increasing number of domestic and wild mammals; updated host ranges are provided. The crab-eating fox Cerdocyon thous, opossums Didelphis spp., domestic cat Felis cattus, black rat Rattus rattus and humans can infect sandflies, but confirmation of these hosts as primary or secondary reservoirs requires further xenodiagnosis studies at the population level. Thus the putative sylvatic reservoir(s) of ZVL remains unknown. Review of intervention studies examining the effectiveness of current control methods highlights the lack of randomized controlled trials of both dog culling and residual insecticide spraying. Topical insecticides (deltamethrin-impregnated collars and pour-ons) have been shown to provide a high level of individual protection to treated dogs, but further community-level studies are needed.

Copyright

Corresponding author

*Corresponding author: Institute of Integrative & Comparative Biology, University of Leeds, Leeds LS2 9JT, United Kingdom. Tel: +44-113-3432824. Fax: +44-113-3432835. Email: R.J.Quinnell@leeds.ac.uk

References

Hide All
Addy, M. and Nandy, A. (1992). 10 years of kala-azar in West Bengal. 1. Did post-kala-azar dermal leishmaniasis initiate the outbreak in 24-Parganas. Bulletin of the World Health Organization 70, 341346.
Adler, S. and Theodor, O. (1932). Investigations on Mediterranean kala-azar, VI. Canine visceral leishmaniasis. Proceedings of the Royal Society of London B 110, 402412.
Alencar, J. E. (1961). [Prevention of calazar in Ceara, Brazil]. Revista do Instituto de Medicina Tropical de Sao Paulo 3, 175180.
Alencar, J. E., Almeida, Y. M., Silva, Z. F., Paiva, A. S. and Da Fonseca, M. F. (1974). [Current aspects of kala-azar in Ceara]. Revista Brasileira de Malariologia e Doencas Tropicais 26, 2753.
Alexander, B. and Maroli, M. (2003). Control of phlebotomine sandflies. Medical and Veterinary Entomology 17, 118.
Alvar, J., Aparicio, P., Aseffa, A., Den Boer, M., Canavate, C., Dedet, J. P., Gradoni, L., Ter Horst, R., Lopez-Velez, R. and Moreno, J. (2008). The relationship between leishmaniasis and AIDS: the second 10 years. Clinical Microbiology Reviews 21, 334359.
Amela, C., Mendez, I., Torcal, J. M., Medina, G., Pachon, I., Canavate, C. and Alvar, J. (1995). Epidemiology of canine leishmaniasis in the Madrid region, Spain. European Journal of Epidemiology 11, 157161.
Anderson, R. M. and May, R. M. (1982). Coevolution of hosts and parasites. Parasitology 85, 411426.
Anderson, R. M. and May, R. M. (1991). Infectious Diseases of Humans. Dynamics and Control. Oxford University Press, Oxford.
Andrade, H. M., De Toledo, V. D. C. P., Marques, M. J., Silva, J. C. F., Tafuri, W. L., Mayrink, W. and Genaro, O. (2002). Leishmania (Leishmania) chagasi is not vertically transmitted in dogs. Veterinary Parasitology 103, 7181.
Antinori, S., Cascio, A., Parravicini, C., Bianchi, R. and Corbellino, M. (2008). Leishmaniasis among organ transplant recipients. Lancet Infectious Diseases 8, 191199.
Antoniou, M., Messaritakis, I., Christodoulou, V., Ascoksilaki, I., Kanavakis, N., Sutton, A. J., Carson, C. and Courtenay, O. (2009). Increasing incidence of zoonotic visceral leishmaniasis on Crete, Greece. Emerging Infectious Diseases 15, 932934.
Ashford, D. A., David, J. R., Freire, M., David, R., Sherlock, I., Eulalio, M. D., Sampaio, D. P. and Badaro, R. (1998). Studies on control of visceral leishmaniasis: Impact of dog control on canine and human visceral leishmaniasis in Jacobina, Bahia, Brazil. American Journal of Tropical Medicine and Hygiene 59, 5357.
Ashford, R. W. (1996). Leishmaniasis reservoirs and their significance in control. Clinics in Dermatology 14, 523532.
Ashford, R. W. (2000). The leishmaniases as emerging and re-emerging zoonoses. International Journal for Parasitology 30, 12691281.
Baneth, G., Koutinas, A. F., Solano-Gallego, L., Bourdeau, P. and Ferrer, L. (2008). Canine leishmaniosis – new concepts and insights on an expanding zoonosis: part one. Trends in Parasitology 24, 324330.
Baneth, G. and Shaw, S. E. (2002). Chemotherapy of canine leishmaniosis. Veterinary Parasitology 106, 315324.
Bern, C., Maguire, J. H. and Alvar, J. (2008). Complexities of assessing the disease burden attributable to leishmaniasis. PLoS Neglected Tropical Diseases 2, e313.
Bettini, S., Gradoni, L. and Pozio, E. (1978). Isolation of Leishmania strains from Rattus rattus in Italy. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 441442.
Bettini, S., Pozio, E. and Gradoni, L. (1980). Leishmaniasis in Tuscany (Italy). 2. Leishmania from wild Rodentia and Carnivora in a human and canine leishmaniasis focus. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 7783.
Blanc, G. and Caminopetros, J. (1930). [Transmission of mediterranean kala-azar by a tick: Rhipicephalus sanguineus]. Comptes Rendus de l'Academie des Sciences 191, 11621164.
Boehme, C. C., Hain, U., Novosel, A., Eichenlaub, S., Fleischmann, E. and Loscher, T. (2006). Congenital visceral leishmaniasis. Emerging Infectious Diseases 12, 359360.
Braga, M. D. M., Coelho, I. C. B., Pompeu, M. M. L., Evans, T. G., Macaullife, I. T., Teixeira, M. J. and Lima, J. W. D. (1998). Canine kala-azar control: aftermath comparison of a fast deletion program of serum-reactive dogs by immuno-enzimatic essay with another of late deletion program of serum-reactive dogs by indirect immunofluorescence of filter paper eluate. Revista da Sociedade Brasileira de Medicina Tropical 31, 419424.
Burney, M. I., Wazir, Y. and Lari, F. A. (1979). Longitudinal study of visceral leishmaniasis in northern areas of Pakistan. Tropical Doctor 9, 110116.
Cabrera, M. A. A., Paula, A. A., Camacho, L. A. B., Marzochi, M. C. A., Xavier, S. C., Da Silva, A. V. M. and Jansen, A. M. (2003). Canine visceral leishmaniasis in Barra de Guaratiba, Rio de Janeiro, Brazil: assessment of risk factors. Revista do Instituto de Medicina Tropical de Sao Paulo 45, 7983.
Cerqueira, E. J. L., Sherlock, I., Gusmao, A., Barbosa Junior, A. D. A. and Nakatani, M. (2003). Experimental infection of Equus asinus with Leishmania chagasi Cunha & Chagas, 1937. Revista da Sociedade Brasileira de Medicina Tropical 36, 695701.
Chagas, E., Da Cunha, A. M., Ferreira, L. C., Deane, L., Deane, G., Guimaraes, F. N., Von Paumgartten, M. J. and Sa, B. (1938). [American visceral leishmaniasis.] Memorias do Instituto Oswaldo Cruz 33, 89–229.
Chappuis, F., Rijal, S., Soto, A., Menten, J. and Boelaert, M. (2006). A meta-analysis of the diagnostic performance of the direct agglutination test and rK39 dipstick for visceral leishmaniasis. British Medical Journal 333, 723726.
Christophers, S. R., Shortt, H. E. and Barraud, P. J. (1924). The development of the parasite of Indian kala-azar in the sandfly Phlebotomus argentipes Annandale and Brunetti. Indian Journal of Medical Research 12, 605607.
Corredor, A., Gallego, J. F., Tesh, R. B., Pelaez, D., Diaz, A., Montilla, M. and Palau, M. T. (1989). Didelphis marsupialis, an apparent wild reservoir of Leishmania donovani chagasi in Colombia, South America. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 195195.
Costa, C. H. N., Gomes, R. B. B., Silva, M. R. B., Garcez, L. M., Ramos, P. K. S., Santos, R. S., Shaw, J. J., David, J. R. and Maguire, J. H. (2000). Competence of the human host as a reservoir for Leishmania chagasi. Journal of Infectious Diseases 182, 9971000.
Costa, C. H. N., Tapety, C. M. M. and Werneck, G. L. (2007). Control of visceral leishmaniasis in urban areas: randomized factorial intervention trial. Revista da Sociedade Brasileira de Medicina Tropical 40, 415419.
Costa, C. H. N. and Vieira, J. B. F. (2001). Changes in the control program of visceral leishmaniasis in Brazil. Revista da Sociedade Brasileira de Medicina Tropical 34, 223228.
Courtenay, O., Gillingwater, K., Gomes, P. A. F., Garcez, L. M. and Davies, C. R. (2007). Deltamethrin-impregnated bednets reduce human landing rates of sandfly vector Lutzomyia longipalpis in Amazon households. Medical and Veterinary Entomology 21, 168176.
Courtenay, O., Kovacic, V., Gomes, P. A. F., Garcez, L. M. and Quinnell, R. J. (2009). A long-lasting topical deltamethrin treatment to protect dogs against visceral leishmaniasis. Medical and Veterinary Entomology 23, 245256.
Courtenay, O., Macdonald, D. W., Lainson, R., Shaw, J. J. and Dye, C. (1994). Epidemiology of canine leishmaniasis – a comparative serological study of dogs and foxes in Amazon Brazil. Parasitology 109, 273279.
Courtenay, O., Quinnell, R. J. and Dye, C. (2001). The role of foxes (Carnivora: Canidae) in the maintenance and transmission of Leishmania infantum: implications for peridomestic control. Proceedings of Round Table on Canine Leishmaniasis, World Leishmaniasis Conference II.
Courtenay, O., Quinnell, R. J., Garcez, L. M. and Dye, C. (2002 a). Low infectiousness of a wildlife host of Leishmania infantum: the crab-eating fox is not important for transmission. Parasitology 125, 407414.
Courtenay, O., Quinnell, R. J., Garcez, L. M., Shaw, J. J. and Dye, C. (2002 b). Infectiousness in a cohort of Brazilian dogs: Why culling fails to control visceral leishmaniasis in areas of high transmission. Journal of Infectious Diseases 186, 13141320.
Courtenay, O., Santana, E. W., Johnson, P. J., Vasconcelos, I. A. B. and Vasconcelos, A. W. (1996). Visceral leishmaniasis in the hoary zorro Dusicyon vetulus: A case of mistaken identity. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 498502.
Coutinho, M. T. Z., Bueno, L. L., Sterzik, A., Fujiwara, R. T., Botelho, J. R., De Maria, M., Genaro, O. and Linardi, P. M. (2005). Participation of Rhipicephalus sanguineus (Acari: Ixodidae) in the epidemiology of canine visceral leishmaniasis. Veterinary Parasitology 128, 149155.
Coutinho, M. T. Z. and Linardi, P. M. (2007). Can fleas from dogs infected with canine visceral leishmaniasis transfer the infection to other mammals? Veterinary Parasitology 147, 320325.
Criado-Fornelio, A., Gutierrez-Garcia, L., Rodriguez-Caabeiro, F., Reus-Garcia, E., Roldan-Soriano, M. A. and Diaz-Sanchez, M. A. (2000). A parasitological survey of wild red foxes (Vulpes vulpes) from the province of Guadalajara, Spain. Veterinary Parasitology 92, 245251.
Cruz, I., Morales, M. A., Noguer, I., Rodriguez, A. and Alvar, J. (2002). Leishmania in discarded syringes from intravenous drug users. Lancet 359, 11241125.
Curi, N. H. D., Miranda, I. and Talamoni, S. A. (2006). Serologic evidence of Leishmania infection in free-ranging wild and domestic canids around a Brazilian National Park. Memorias do Instituto Oswaldo Cruz 101, 99101.
Da Costa, R. T., Franca, J. C., Mayrink, W., Nascimento, E., Genaro, O. and Campos-Neto, A. (2003). Standardization of a rapid immunochromatographic test with the recombinant antigens K39 and K26 for the diagnosis of canine visceral leishmaniasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 678682.
Da Costa-Val, A. P., Cavalcanti, R. R., Gontijo, N. D. F., Michalick, M. S. M., Alexander, B., Williams, P. and Melo, M. N. (2007). Canine visceral leishmaniasis: Relationships between clinical status, humoral immune response, haematology and Lutzomyia (Lutzomyia) longipalpis infectivity. Veterinary Journal 174, 636643.
Da Silva, A. V. M., Candido, C. D. D. S., Pereira, D. D. P., Brazil, R. P. and Carreira, J. C. A. (2008). The first record of American visceral leishmaniasis in domestic cats from Rio de Janeiro, Brazil. Acta Tropica 105, 9294.
Dantas-Torres, F. (2006). Do any insects other than phlebotomine sandflies (Diptera: Psychodidae) transmit Leishmania infantum (Kinetoplastida: Trypanosomatidae) from dog to dog? Veterinary Parasitology 136, 379380.
Dantas-Torres, F. and Brandao-Filho, S. P. (2006). Visceral leishmaniasis in Brazil: revisiting paradigms of epidemiology and control. Revista do Instituto de Medicina Tropical de Sao Paulo 48, 151156.
De Lima, H., Rodriguez, N., Barrios, M. A., Avila, A., Canizales, I. and Gutierrez, S. (2008). Isolation and molecular identification of Leishmania chagasi from a bat (Carollia perspicillata) in northeastern Venezuela. Memorias do Instituto Oswaldo Cruz 103, 412414.
Deane, L. M. and Deane, M. P. (1955). [Preliminary observations on the comparative importance of man, the dog and the fox (Lycalopex vetulus) as reservoirs of Leishmania donovani, in an endemic area for calazar, Ceara]. O Hospital 48, 7998.
Di Bella, C., Vitale, F., Russo, G., Greco, A., Milazzo, C., Aloise, G. and Cagnin, M. (2003). Are rodents a potential reservoir for Leishmania infantum in Italy? Journal of Mountain Ecology 7 (Suppl.), 125129.
Dietze, R., Barros, G. B., Teixeira, L., Harris, J., Michelson, K., Falqueto, A. and Corey, R. (1997). Effect of eliminating seropositive canines on the transmission of visceral leishmaniasis in Brazil. Clinical Infectious Diseases 25, 12401242.
Dipineto, L., Manna, L., Baiano, A., Gala, M., Fioretti, A., Gravino, A. E. and Menna, L. F. (2007). Presence of Leishmania infantum in red foxes (Vulpes vulpes) in southern Italy. Journal of Wildlife Diseases 43, 518520.
Donner, A. and Klar, N. (2000). Design and Analysis of Cluster Randomization Trials. Arnold, London.
Dos Santos, S. O., Arias, J., Ribeiro, A. A., Hoffmann, M. D., De Freitas, R. A. and Malacco, M. A. F. (1998). Incrimination of Lutzomyia cruzi as a vector of American Visceral Leishmaniasis. Medical and Veterinary Entomology 12, 315317.
Duprey, Z. H., Steurer, F. J., Rooney, J. A., Kirchhoff, L. V., Jackson, J. E., Rowton, E. D. and Schantz, P. M. (2006). Canine visceral leishmaniasis, United States and Canada, 2000–2003. Emerging Infectious Diseases 12, 440446.
Dye, C. (1996). The logic of visceral leishmaniasis control. American Journal of Tropical Medicine and Hygiene 55, 125130.
Dye, C., Killick-Kendrick, R., Vitutia, M. M., Walton, R., Killick-Kendrick, M., Harith, A. E., Guy, M. W., Canavate, M. C. and Hasibeder, G. (1992). Epidemiology of canine leishmaniasis – prevalence, incidence and basic reproduction number calculated from a cross-sectional serological survey on the island of Gozo, Malta. Parasitology 105, 3541.
Dye, C., Vidor, E. and Dereure, J. (1993). Serological diagnosis of leishmaniasis – on detecting infection as well as disease. Epidemiology and Infection 110, 647656.
Fallah, E., Farshchian, M., Mazlomi, A., Majidi, J., Kusha, A., Mardi, A. and Mahdipoorzareh, N. (2006). Study on the prevalence of visceral leishmaniasis in rodent's of Azarshahr district (new focus), northwest of Iran. Archives of Razi Institute 61, 2733.
Fernandez-Bellon, H., Solano-Gallego, L., Bardagi, M., Alberola, J., Ramis, A. and Ferrer, L. (2006). Immune response to Leishmania infantum in healthy horses in Spain. Veterinary Parasitology 135, 181185.
Ferroglio, E., Poggi, M. and Trisciuoglio, A. (2008). Evaluation of 65% permethrin spot-on and deltamethrin-impregnated collars for canine Leishmania infantum infection prevention. Zoonoses and Public Health 55, 145148.
Figueiredo, F. B., Gremiao, I. D. F., Pereira, S. A., Fedulo, L. P., Menezes, R. C., Balthazar, D. A., Schubach, T. M. P. and Madeira, M. F. (2008). First report of natural infection of a bush dog (Speothos venaticus) with Leishmania (Leishmania) chagasi in Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 200201.
Foglia Manzillo, V., Oliva, G., Pagano, A., Manna, L., Maroli, M. and Gradoni, L. (2006). Deltamethrin-impregnated collars for the control of canine leishmaniasis: Evaluation of the-protective effect and influence on the clinical outcome of Leishmania infection in kennelled stray dogs. Veterinary Parasitology 142, 142145.
Giffoni, J. H., De Almeida, C. E., Dos Santos, S. O., Ortega, V. S. and De Barros, A. T. M. (2002). Evaluation of 65% permethrin spot-on for prevention of canine visceral leishmaniasis: effect on disease prevalence and the vectors (Diptera: Psychodidae) in a hyperendemic area. Veterinary Therapeutics 3, 485492.
Gomes, R. B., Mendonca, I. L., Silva, V. C., Ruas, J., Silva, M. B., Cruz, M. S. P., Barral, A. and Costa, C. H. N. (2007). Antibodies against Lutzomyia longipalpis saliva in the fox Cerdocyon thous and the sylvatic cycle of Leishmania chagasi. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 127133.
Gradoni, L., Gramiccia, M., Mancianti, F. and Pieri, S. (1988). Studies on canine leishmaniasis control. 2. Effectiveness of control measures against canine leishmaniasis in the Isle of Elba, Italy. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 568571.
Gradoni, L., Maroli, M., Gramiccia, M. and Mancianti, F. (1987). Leishmania infantum infection rates in Phlebotomus perniciosus fed on naturally infected dogs under antimonial treatment. Medical and Veterinary Entomology 1, 339342.
Gradoni, L., Pozio, E., Gramiccia, M., Maroli, M. and Bettini, S. (1983). Leishmaniasis in Tuscany (Italy). 7. Studies on the role of the black rat, Rattus rattus, in the epidemiology of visceral leishmaniasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 427431.
Gramiccia, M. and Gradoni, L. (2005). The current status of zoonotic leishmaniases and approaches to disease control. International Journal for Parasitology 35, 11691180.
Guarga, J. L., Lucientes, J., Peribanez, M. A., Molina, R., Gracia, M. J. and Castillo, J. A. (2000 a). Experimental infection of Phlebotomus perniciosus and determination of the natural infection rates of Leishmania infantum in dogs. Acta Tropica 77, 203207.
Guarga, J. L., Moreno, J., Lucientes, J., Gracia, M. J., Peribanez, M. A., Alvar, J. and Castillo, J. A. (2000 b). Canine leishmaniasis transmission: higher infectivity amongst naturally infected dogs to sand flies is associated with lower proportions of T helper cells. Research in Veterinary Science 69, 249253.
Haddow, A. D., Curler, G. and Moulton, J. K. (2008). New records of Lutzomyia shannoni and Lutzomyia vexator (Diptera: Psychodidae) in eastern Tennessee. Journal of Vector Ecology 33, 393396.
Hamidi, A. N., Nadim, A., Edrissian, G. H., Tahvildar-Bidruni, G. and Javadian, E. (1982). Visceral leishmaniasis of jackals and dogs in northern Iran. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 756757.
Harris, M. P. (1994). Suspected transmission of leishmaniasis. Veterinary Record 135, 339339.
Hasibeder, G., Dye, C. and Carpenter, J. (1992). Mathematical modeling and theory for estimating the basic reproduction number of canine leishmaniasis. Parasitology 105, 4353.
Haydon, D. T., Cleaveland, S., Taylor, L. H. and Laurenson, M. K. (2002). Identifying reservoirs of infection: A conceptual and practical challenge. Emerging Infectious Diseases 8, 14681473.
Keck, N. and Dereure, J. (2003). Epidemiology of canine leishmaniasis by cross-sectional study in the French focus of Cevennes. Revue de Medecine Veterinaire 154, 599604.
Killick-Kendrick, R. (1999). The biology and control of phlebotomine sandflies. Clinics in Dermatology 17, 279289.
Kirkwood, B. R., Cousens, S. N., Victora, C. G. and De Zoysa, I. (1997). Issues in the design and interpretation of studies to evaluate the impact of community-based interventions. Tropical Medicine and International Health 2, 10221029.
Lacerda, M. M. (1994). The Brazilian Leishmaniasis Control Program. Memorias do Instituto Oswaldo Cruz 89, 489495.
Lachaud, L., Chabbert, E., Dubessay, P., Dereure, J., Lamothe, J., Dedet, J. P. and Bastien, P. (2002). Value of two PCR methods for the diagnosis of canine visceral leishmaniasis and the detection of asymptomatic carriers. Parasitology 125, 197207.
Lainson, R., Dye, C., Shaw, J. J., Macdonald, D. W., Courtenay, O., Souza, A. A. A. and Silveira, F. T. (1990). Amazonian visceral leishmaniasis – distribution of the vector Lutzomyia longipalpis (Lutz and Neiva) in relation to the fox Cerdocyon thous (Linn.) and the efficiency of this reservoir host as a source of infection. Memorias do Instituto Oswaldo Cruz 85, 135137.
Lainson, R. and Rangel, E. F. (2005). Lutzomyia longipalpis and the eco-epidemiology of American visceral leishmaniasis, with particular reference to Brazil – a review. Memorias do Instituto Oswaldo Cruz 100, 811827.
Lainson, R., Shaw, J. J., Silveira, F. T. and Braga, R. R. (1987). American visceral leishmaniasis – on the origin of Leishmania (Leishmania) chagasi. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 517517.
Lemos, E. M., Laurenti, M. D., Moreira, M. A. B., Reis, A. B., Giunchetti, R. C., Raychaudhuri, S. and Dietze, R. (2008). Canine visceral leishmaniasis: Performance of a rapid diagnostic test (Kalazar Detect (TM)) in dogs with and without signs of the disease. Acta Tropica 107, 205207.
Le Pont, F., Mouchet, J. and Desjeux, P. (1989). Leishmaniasis in Bolivia. 7. Infection of sentinel porcupines (Coendou prehensilis, L.) by Leishmania (Le.) chagasi. Memorias do Instituto Oswaldo Cruz 84, 575575.
Lukes, J., Mauricio, I. L., Schonian, G., Dujardin, J. C., Soteriadou, K., Dedet, J. P., Kuhls, K., Tintaya, K. W. Q., Jirku, M., Chocholova, E., Haralambous, C., Pratlong, F., Obornik, M., Horak, A., Ayala, F. J. and Miles, M. A. (2007). Evolutionary and geographical history of the Leishmania donovani complex with a revision of current taxonomy. Proceedings of the National Academy of Sciences, USA 104, 93759380.
Luppi, M. M., Malta, M. C. C., Silva, T. M. A., Silva, F. L., Motta, R. O. C., Miranda, I., Ecco, R. and Santos, R. L. (2008). Visceral leishmaniasis in captive wild canids in Brazil. Veterinary Parasitology 155, 146151.
Magalhaes, P. A., Mayrink, W., Da Costa, C. A., Melo, M. N., Dias, M., Batista, S. M., Michalick, M. S. and Williams, P. (1980). [Kala-azar in the Rio Doce, Minas Gerais area. Results of prophylactic measures]. Revista do Instituto de Medicina Tropical de Sao Paulo 22, 197202.
Maia-Elkhoury, A. N. S., Alves, W. A., Sousa-Gomes, M. L., Sena, J. M. and Luna, E. A. (2008). Visceral leishmaniasis in Brazil: trends and challenges. Cadernos de Saude Publica 24, 29412947.
Maroli, M., Mizzoni, V., Siragusa, C., D'Orazi, A. and Gradoni, L. (2001). Evidence for an impact on the incidence of canine leishmaniasis by the mass use of deltamethrin-impregnated dog collars in southern Italy. Medical and Veterinary Entomology 15, 358363.
Maroli, M., Pennisi, M. G., Di Muccio, T., Khoury, C., Gradoni, L. and Gramiccia, M. (2007). Infection of sandflies by a cat naturally infected with Leishmania infantum. Veterinary Parasitology 145, 357360.
Maroli, M., Rossi, L., Baldelli, R., Capelli, G., Ferroglio, E., Genchi, C., Gramiccia, M., Mortarino, M., Pietrobelli, M. and Gradoni, L. (2008). The northward spread of leishmaniasis in Italy: evidence from retrospective and ongoing studies on the canine reservoir and phlebotomine vectors. Tropical Medicine and International Health 13, 256264.
Martin-Sanchez, J., Acedo, C., Munoz-Perez, M., Pesson, B., Marchal, O. and Morillas-Marquez, F. (2007). Infection by Leishmania infantum in cats: epidemiological study in Spain. Veterinary Parasitology 145, 267273.
Masucci, M., De Majo, M., Contarino, R. B., Borruto, G., Vitale, F. and Pennisi, M. G. (2003). Canine leishmaniasis in the newborn puppy. Veterinary Research Communications 27, 771774.
Mauricio, I. L., Stothard, J. R. and Miles, M. A. (2000). The strange case of Leishmania chagasi. Parasitology Today 16, 188189.
May, R. M. and Anderson, R. M. (1983). Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society of London B 219, 281313.
Mazloumi Gavgani, A. S., Hodjati, M. H., Mohite, H. and Davies, C. R. (2002 a). Effect of insecticide-impregnated dog collars on incidence of zoonotic visceral leishmaniasis in Iranian children: a matched-cluster randomised trial. Lancet 360, 374379.
Mazloumi Gavgani, A. S., Mohite, H., Edrissian, G. H., Mohebali, M. and Davies, C. R. (2002 b). Domestic dog ownership in Iran is a risk factor for human infection with Leishmania infantum. American Journal of Tropical Medicine and Hygiene 67, 511515.
Meinecke, C. K., Schottelius, J., Oskam, L. and Fleischer, B. (1999). Congenital transmission of visceral leishmaniasis (kala azar) from an asymptomatic mother to her child. Pediatrics 104, e65.
Mello, D. A., Rego Junior, F. D. A., Oshozo, E. and Nunes, V. L. (1988). Cerdocyon thous (L.) (Carnivora, Canidae) naturally infected with Leishmania donovani chagasi (Cunha & Chagas, 1973) in Corumba (Mato Grosso do Sul State, Brazil). Memorias do Instituto Oswaldo Cruz 83, 259.
Michalsky, E. M., Rocha, M. F., Lima, A. C. V. M. D., Franca-Silva, J. C., Pires, M. Q., Oliveira, F. S., Pacheco, R. S., Dos Santos, S. L., Barata, R. A., Romanha, A. J., Fortes-Dias, C. L. and Dias, E. S. (2007). Infectivity of seropositive dogs, showing different clinical forms of leishmaniasis, to Lutzomyia longipalpis phlebotomine sand flies. Veterinary Parasitology 147, 6776.
Mohebali, M., Hajjaran, H., Hamzavi, Y., Mobedi, I., Arshi, S., Zarei, Z., Akhoundi, B., Naeini, K. M., Avizeh, R. and Fakhar, M. (2005). Epidemiological aspects of canine visceral leishmaniosis in the Islamic Republic of Iran. Veterinary Parasitology 129, 243251.
Mohebali, M., Poormohammadi, B., Kanani, H., Hajjaran, H. and Edrissian, G. H. (1998). Rodents: another group of animal hosts of visceral leishmaniasis in Meshkin-Shahr district, Islamic Republic of Iran. Eastern Mediterranean Health Journal 4, 376378.
Molina, R., Amela, C., Nieto, J., San-Andres, M., Gonzalez, F., Castillo, J. A., Lucientes, J. and Alvar, J. (1994). Infectivity of dogs naturally infected with Leishmania infantum to colonized Phlebotomus perniciosus. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 491493.
Molina, R., Gradoni, L. and Alvar, J. (2003). HIV and the transmission of Leishmania. Annals of Tropical Medicine and Parasitology 97, S29S45.
Molina, R., Lohse, J. M., Pulido, F., Laguna, F., Lopez-Velez, R. and Alvar, J. (1999). Infection of sand flies by humans coinfected with Leishmania infantum and human immunodeficiency virus. American Journal of Tropical Medicine and Hygiene 60, 5153.
Montoya-Lerma, J., Cadena, H., Oviedo, M., Ready, P. D., Barazarte, R., Travi, B. L. and Lane, R. P. (2003). Comparative vectorial efficiency of Lutzomyia evansi and Lu. longipalpis for transmitting Leishmania chagasi. Acta Tropica 85, 1929.
Moraes-Silva, E., Antunes, F. R., Rodrigues, M. S., Juliao, F. D., Dias-Lima, A. G., Lemos-de-Sousa, V., De Alcantara, A. C., Reis, E. A. G., Nakatani, M., Badaro, R., Reis, M. G., Pontes-de-Carvalho, L. and Franke, C. R. (2006). Domestic swine in a visceral leishmaniasis endemic area produce antibodies against multiple Leishmania infantum antigens but apparently resist to L. infantum infection. Acta Tropica 98, 176182.
Moreira, E. D., De Souza, V. M. M., Sreenivasan, M., Nascimento, E. G. and De Carvalho, L. P. (2004). Assessment of an optimized dog-culling program in the dynamics of canine Leishmania transmission. Veterinary Parasitology 122, 245252.
Mukhopadhyay, A. K. and Mishra, R. N. (1991). Development of Leishmania donovani in Phlebotomus argentipes and Ph. papatasi fed on kala-azar patients in Bihar. Indian Journal of Medical Research 93, 152154.
Napier, L. E. and Smith, R. O. (1926). The development of Leishmania donovani in the gut of the sandfly Phlebotomus papatasi. Indian Journal of Medical Research 14, 713716.
Napier, L. E., Smith, R. O., Das-Gupta, C. R. and Mukerji, S. (1933). The infection of Phlebotomus argentipes from dermal leishmanial lesions. Indian Journal of Medical Research 21, 173177.
Nunes, C. M., De Lima, V. M. F., De Paula, H. B., Perri, S. H. V., De Andrade, A. M., Dias, F. E. F. and Burattini, M. N. (2008). Dog culling and replacement in an area endemic for visceral leishmaniasis in Brazil. Veterinary Parasitology 153, 1923.
Oliva, G., Scalone, A., Foglia Manzillo, V., Gramiccia, M., Pagano, A., Di Muccio, T. and Gradoni, L. (2006). Incidence and time course of Leishmania infantum infections examined by parasitological, serologic, and nested-PCR techniques in a cohort of naive dogs exposed to three consecutive transmission seasons. Journal of Clinical Microbiology 44, 13181322.
Oliveira, A. M. and Melo, M. T. V. (1994). Vectors control importance on leishmaniasis transmission. Memorias do Instituto Oswaldo Cruz 89, 451456.
Oliveira, C. D. L., Morais, M. H. F. and Machado-Coelho, G. L. L. (2008). Visceral leishmaniasis in large Brazilian cities: challenges for control. Cadernos de Saude Publica 24, 29532958.
Oliveira, F. S., Pirmez, C., Pires, M. Q., Brazil, R. P. and Pacheco, R. S. (2005). PCR-based diagnosis for detection of Leishmania in skin and blood of rodents from an endemic area of cutaneous and visceral leishmaniasis in Brazil. Veterinary Parasitology 129, 219227.
Ostyn, B., Vanlerberghe, V., Picado, A., Dinesh, D. S., Sundar, S., Chappuis, F., Rijal, S., Dujardin, J. C., Coosemans, M., Boelaert, M. and Davies, C. (2008). Vector control by insecticide-treated nets in the fight against visceral leishmaniasis in the Indian subcontinent, what is the evidence? Tropical Medicine and International Health 13, 10731085.
Otero, A. C. S., Da Silva, V. O., Luz, K. G., Palatnik, M., Pirmez, C., Fernandes, O. and Palatnik de Sousa, C. B. (2000). Occurrence of Leishmania donovani DNA in donated blood from seroreactive Brazilian blood donors. American Journal of Tropical Medicine and Hygiene 62, 128131.
Otranto, D., Paradies, P., Lia, R. P., Latrofa, M. S., Testini, G., Cantacessi, C., Mencke, N., Galli, G., Capelli, G. and Stanneck, D. (2007). Efficacy of a combination of 10% imidacloprid/50% permethrin for the prevention of leishmaniasis in kennelled dogs in an endemic area. Veterinary Parasitology 144, 270278.
Owens, S. D., Oakley, D. A., Marryott, K., Hatchett, W., Walton, R., Nolan, T. J., Newton, A., Steurer, F., Schantz, P. and Giger, U. (2001). Transmission of visceral leishmaniasis through blood transfusions from infected English Foxhounds to anemic dogs. Journal of the American Veterinary Medical Association 219, 10761083.
Pagliano, P., Carannante, N., Rossi, M., Gramiccia, M., Gradoni, L., Faella, F. S. and Gaeta, G. B. (2005). Visceral leishmaniasis in pregnancy: a case series and a systematic review of the literature. Journal of Antimicrobial Chemotherapy 55, 229233.
Palatnik-de-Sousa, C. B. (2008). Vaccines for leishmaniasis in the fore coming 25 years. Vaccine 26, 17091724.
Palatnik-de-Sousa, C. B., Batista-de-Melo, L. M., Borja-Cabrera, G. P., Palatnik, M. and Lavor, C. C. (2004). Improving methods for epidemiological control of canine visceral leishmaniasis based on a mathematical model. Impact on the incidence of the canine and human disease. Anais da Academia Brasileira de Ciências 76, 583593.
Palatnik-de-Sousa, C. B., Dos Santos, W. R., Franca-Silva, J. C., Da Costa, R. T., Reis, A. B., Palatnik, M., Mayrink, W. and Genaro, O. (2001). Impact of canine control on the epidemiology of canine and human visceral leishmaniasis in Brazil. American Journal of Tropical Medicine and Hygiene 65, 510517.
Parrot, L., Donatien, A. and Lestoquard, F. (1930). [On the development of the parasite of canine visceral leishmaniasis in Phlebotomus major var perniciosus Newstead]. Bulletin de la Societe de Pathologie Exotique 23, 724726.
Petrisceva, P. A. (1971). The natural focality of leishmaniasis in the USSR. Bulletin of the World Health Organization 44, 567576.
Portus, M., Gallego, M., Riera, C., Aisa, M. J., Fisa, R. and Castillejo, S. (2002). Wild and domestic mammals in the life cycle of Leishmania infantum in southwest Europe. A literature review and studies performed in Catalonia (Spain). Revista Iberica de Parasitologia 62, 7276.
Pozio, E., Gradoni, L., Bettini, S. and Gramiccia, M. (1981). Leishmaniasis in Tuscany (Italy).5. Further isolation of Leishmania from Rattus rattus in the Province of Grosseto. Annals of Tropical Medicine and Parasitology 75, 393395.
Pozio, E., Maroli, M., Gradoni, L. and Gramiccia, M. (1985). Laboratory transmission of Leishmania infantum to Rattus rattus by the bite of experimentally infected Phlebotomus perniciosus. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 524526.
Quinnell, R. J., Courtenay, O., Garcez, L. and Dye, C. (1997). The epidemiology of canine leishmaniasis: transmission rates estimated from a cohort study in Amazonian Brazil. Parasitology 115, 143156.
Quinnell, R. J. and Dye, C. (1994). An experimental study of the peridomestic distribution of Lutzomyia longipalpis (Diptera, Psychodidae). Bulletin of Entomological Research 84, 379382.
Reithinger, R. (2008). Leishmaniases' burden of disease: ways forward for getting from speculation to reality. PLoS Neglected Tropical Diseases 2, e285.
Reithinger, R., Coleman, P. G., Alexander, B., Vieira, E. P., Assis, G. and Davies, C. R. (2004). Are insecticide-impregnated dog collars a feasible alternative to dog culling as a strategy for controlling canine visceral leishmaniasis in Brazil? International Journal for Parasitology 34, 5562.
Ribeiro, R. R., Moura, E. P., Pimentel, V. M., Sampaio, W. M., Silva, S. M., Schettini, D. A., Alves, C. F., Melo, F. A., Tafuri, W. L., Demicheli, C., Melo, M. N., Frezard, F. and Michalick, M. S. M. (2008). Reduced tissue parasitic load and infectivity to sand flies in dogs naturally infected by Leishmania (Leishmania) chagasi following treatment with a liposome formulation of meglumine antimoniate. Antimicrobial Agents and Chemotherapy 52, 25642572.
Ritmeijer, K., Davies, C., Van Zorge, R., Wang, S. J., Schorscher, J., Dongu'du, S. I. and Davidson, R. N. (2007). Evaluation of a mass distribution programme for fine-mesh impregnated bednets against visceral leishmaniasis in eastern Sudan. Tropical Medicine and International Health 12, 404414.
Rosypal, A. C., Troy, G. C., Zajac, A. M., Frank, G. and Lindsay, D. S. (2005). Transplacental transmission of a North American isolate of Leishmania infantum in an experimentally infected beagle. Journal of Parasitology 91, 970972.
Santiago, M. E. B., Vasconcelos, R. O., Fattori, K. R., Munari, D. P., Michelin, A. D. F. and Lima, V. M. F. (2007). An investigation of Leishmania spp. in Didelphis spp. from urban and peri-urban areas in Bauru (Sao Paulo, Brazil). Veterinary Parasitology 150, 283290.
Shaw, J. J. (2006). Further thoughts on the use of the name Leishmania (Leishmania) infantum chagasi for the aetiological agent of American visceral leishmaniasis. Memorias do Instituto Oswaldo Cruz 101, 577579.
Sherlock, I. A. (1996). Ecological interactions of visceral leishmaniasis in the State of Bahia, Brazil. Memorias do Instituto Oswaldo Cruz 91, 671683.
Shortt, H. E., Barraud, P. J. and Craighead, A. C. (1926). Transmission experiments in Indian kala-azar with Phlebotomus argentipes. Indian Journal of Medical Research 14, 589600.
Shortt, H. E., Smith, R. O. A., Swaminath, C. S. and Krishnan, K. V. (1931). Transmission of Indian kala-azar by the bite of Phlebotomus argentipes. Indian Journal of Medical Research 18, 13731375.
Silva, E. S., Pirmez, C., Gontijo, C. M. F., Fernandes, O. and Brazil, R. P. (2000). Visceral leishmaniasis in the crab-eating fox (Cerdocyon thous) in south-east Brazil. Veterinary Record 147, 421422.
Silva, F. L., Oliveira, R. G., Silva, T. M. A., Xavier, M. N., Nascimento, E. F. and Santos, R. L. (2009). Venereal transmission of canine visceral leishmaniasis. Veterinary Parasitology 160, 5559.
Smith, R. O. A., Hadler, K. C. and Ahmed, I. (1940). Further investigations on the transmission of kala-azar. Indian Journal of Medical Research 28, 585591.
Sobrino, R., Ferroglio, E., Oleaga, A., Romano, A., Millan, J., Revilla, A., Arnal, M. C., Trisciuoglio, A. and Gortazar, C. (2008). Characterization of widespread canine leishmaniasis among wild carnivores from Spain. Veterinary Parasitology 155, 198203.
Solano-Gallego, L., Morell, P., Arboix, M., Alberola, J. and Ferrer, L. (2001). Prevalence of Leishmania infantum infection in dogs living in an area of canine leishmaniasis endemicity using PCR on several tissues and serology. Journal of Clinical Microbiology 39, 560563.
Symmers, W. S. (1960). Leishmaniasis acquired by contagion – a case of marital infection in Britain. Lancet 1, 127132.
Toplu, N., Aydogan, A. and Oguzoglu, T. C. (2007). Visceral leishmaniosis and parapoxvirus infection in a Mediterranean monk seal (Monachus monachus). Journal of Comparative Pathology 136, 283287.
Travi, B., Arteaga, L. T., Leon, A. P. and Adler, G. H. (2002). Susceptibility of spiny rats (Proechimys semispinosus) to Leishmania (Viannia) panamensis and Leishmania (Leishmania) chagasi. Memorias do Instituto Oswaldo Cruz 97, 887892.
Travi, B. L., Jaramillo, C., Montoya, J., Segura, I., Zea, A., Goncalves, A. and Velez, I. D. (1994). Didelphis marsupialis, an important reservoir of Trypanosoma (Schizotrypanum) cruzi and Leishmania (Leishmania) chagasi in Colombia. American Journal of Tropical Medicine and Hygiene 50, 557565.
Travi, B. L., Osorio, Y., Becerra, M. T. and Adler, G. H. (1998 a). Dynamics of Leishmania chagasi infection in small mammals of the undisturbed and degraded tropical dry forests of northern Colombia. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 275278.
Travi, B. L., Osorio, Y., Guarin, N. and Cadena, H. (1998 b). Leishmania (Leishmania) chagasi: Clinical and parasitological observations in experimentally infected Didelphis marsupialis, reservoir of New World visceral leishmaniasis. Experimental Parasitology 88, 7375.
Travi, B. L., Tabares, C. J., Cadena, H., Ferro, C. and Osorio, Y. (2001). Canine visceral leishmaniasis in Colombia: Relationship between clinical and parasitologic status and infectivity for sand flies. American Journal of Tropical Medicine and Hygiene 64, 119124.
Travi, B. L., Velez, I. D., Brutus, L., Segura, I., Jaramillo, C. and Montoya, J. (1990). Lutzomyia evansi, an alternate vector of Leishmania chagasi in a Colombian focus of visceral leishmaniasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 676677.
Verçosa, B. L. A., Lemos, C. M., Mendonça, I. L., Silva, S. M. M. S., De Carvalho, S. M., Goto, H. and Costa, F. A. L. (2008). Transmission potential, skin inflammatory response, and parasitism of symptomatic and asymptomatic dogs with visceral leishmaniasis. BMC Veterinary Research 4, 45.
Vieira, J. B. and Coelho, G. E. (1998). [Visceral leishmaniasis or kala-azar: the epidemiological and control aspects]. Revista da Sociedade Brasileira de Medicina Tropical 31 (Suppl 2), 8592.
Xiong, G., Jin, C., Cheng, X., Su, Z. and Hong, Y. (1994). Deltamethrin bath of domestic dog in the prevention of sandfly bite. Endemic Disease Bulletin 9, 3234.
Xiong, G., Jin, C., Hong, Y., Su, Z., Xue, P., Xie, W., Zhang, A., Li, G. and Gao, B. (1995). Studies of the deltamethrin-medicated bath of domestic dogs for interrupting visceral leishmaniasis transmission. Zhongguo ji sheng chong xue yu ji sheng chong bing za zhi [Chinese Journal of Parasitology and Parasitic Diseases] 13, 178181.
Young, D. G. and Perkins, P. V. (1984). Phlebotomine sandflies of North America (Diptera, Psychodidae). Mosquito News 44, 263304.
Zaffaroni, E., Rubaudo, L., Lanfranchi, P. and Mignone, W. (1999). Epidemiological patterns of canine leishmaniosis in Western Liguria (Italy). Veterinary Parasitology 81, 1119.
Zhi-Biao, X. (1989). Present situation of visceral leishmaniasis in China. Parasitology Today 5, 224228.
Zulueta, A. M., Villarroel, E., Rodriguez, N., Feliciangeli, M. D., Mazzarri, M., Reyes, O., Rodriguez, V., Centeno, M., Barrios, R. M. and Ulrich, M. (1999). Epidemiologic aspects of American visceral leishmaniasis in an endemic focus in eastern Venezuela. American Journal of Tropical Medicine and Hygiene 61, 945950.

Keywords

Transmission, reservoir hosts and control of zoonotic visceral leishmaniasis

  • R. J. QUINNELL (a1) and O. COURTENAY (a2)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed