Skip to main content Accessibility help

Cutaneous Leishmaniasis in dogs: is high seroprevalence indicative of a reservoir role?



American cutaneous leishmaniasis (ACL) is a complex disease with a rich diversity of animal host species. This diversity imposes a challenge, since understanding ACL transmission requires the adequate identification of reservoir hosts, those species able to be a source of additional infections. In this study we present results from an ACL cross-sectional serological survey of 51 dogs (Canis familiaris), where we used diagnostic tests that measure dog's exposure to Leishmania spp. parasites. We did our research in Panamá, at a village that has undergone significant ecosystem level transformations. We found an ACL seroprevalence of 47% among dogs, and their exposure was positively associated with dog age and abundance of sand fly vectors in the houses of dog owners. Using mathematical models, which were fitted to data on the proportion of positive tests as function of dog age, we estimated a basic reproductive number (R 0 ± s.e.) of 1·22 ± 0·09 that indicates the disease is endemically established in the dogs. Nevertheless, this information by itself is insufficient to incriminate dogs as ACL reservoirs, given the inability to find parasites (or their DNA) in seropositive dogs and previously reported failures to experimentally infect vectors feeding on dogs with ACL parasites.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Cutaneous Leishmaniasis in dogs: is high seroprevalence indicative of a reservoir role?
      Available formats

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Cutaneous Leishmaniasis in dogs: is high seroprevalence indicative of a reservoir role?
      Available formats

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Cutaneous Leishmaniasis in dogs: is high seroprevalence indicative of a reservoir role?
      Available formats


This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (, which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

* Corresponding author. Institute of Tropical Medicine (NEKKEN), Nagasaki University, 852-8523 Sakamoto 1-12-4, Nagasaki, Japan. E-mail:


Hide All
Aguilar, C. M., Rangel, E. F., Garcia, L., Fernandez, E., Momen, H., Grimaldi Filho, G. and Vargas, Z. d. (1989). Zoonotic cutaneous leishmaniasis due to Leishmania (Viannia) braziliensis associated with domestic animals in Venezuela and Brazil. Memorias Do Instituto Oswaldo Cruz 84, 1928.
Alexander, B., Agudelo, L. A., Navarro, F., Ruiz, F., Molina, J., Aguilera, G. and Quiñones, M. L. (2001). Phlebotomine sandflies and leishmaniasis risks in Colombian coffee plantations under two systems of cultivation. Medical and Veterinary Entomology 15, 364373.
Alexander, J. B. (1987). Dispersal of phlebotomine sand flies (Diptera: Psychodidae) in a Colombian coffee plantation. Journal of Medical Entomology 24, 552558.
Alvar, J., Vélez, I. D., Bern, C., Herrero, M., Desjeux, P., Cano, J., Jannin, J., Boer, M. d. and the, W. H. O. L. C. T. (2012). Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 7, e35671.
Anderson, R. M. and May, R. M. (1991). Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford.
Aragão, H. d. B. (1927). Leishmaniose tegumentar e sua transmissão pelos phlebotomos. Memorias Do Instituto Oswaldo Cruz 20, 177195.
Ashford, R. W. (1997). The leishmaniases as model zoonoses. Annals of Tropical Medicine and Parasitology 91, 693701.
Boggild, A. K., Ramos, A. P., Espinosa, D., Valencia, B. M., Veland, N., Miranda-Verastegui, C., Arevalo, J., Low, D. E. and Llanos-Cuentas, A. (2010). Clinical and demographic stratification of test performance: a pooled analysis of five laboratory diagnostic methods for American Cutaneous Leishmaniasis. The American Journal of Tropical Medicine and Hygiene 83, 345350.
Bolker, B. M. (2008). Ecological Models and Data in R. Princeton University Press, Princeton.
Branscum, A. J., Gardner, I. A. and Johnson, W. O. (2005). Estimation of diagnostic-test sensitivity and specificity through Bayesian modeling. Preventive Veterinary Medicine 68, 145163.
Bretscher, M., Supargiyono, S., Wijayanti, M., Nugraheni, D., Widyastuti, A., Lobo, N., Hawley, W., Cook, J. and Drakeley, C. (2013). Measurement of Plasmodium falciparum transmission intensity using serological cohort data from Indonesian schoolchildren. Malaria Journal 12, 21.
Calzada, J. E., Saldaña, A., Rigg, C., Valderrama, A., Romero, L. and Chaves, L. F. (2013). Changes in phlebotomine sand fly species composition following insecticide thermal fogging in a rural setting of Western Panamá. PLoS ONE 8, e53289.
Carey, J. R. (2001). Insect biodemography. Annual Review of Entomology 46, 79110.
Carey, J. R. (2003). Longevity: the Biology and Demography of Life Span. Princeton University Press, Princeton, NJ, USA.
Castro, E. A., Thomaz-Soccol, V., Augur, C. and Luz, E. (2007). Leishmania (Viannia) braziliensis: epidemiology of canine cutaneous leishmaniasis in the State of Paraná (Brazil). Experimental Parasitology 117, 1321.
Chaves, L. F., Calzada, J. E., Rigg, C., Valderrama, A., Gottdenker, N. L. and Saldaña, A. (2013). Leishmaniasis sand fly vector density reduction is less marked in destitute housing after insecticide thermal fogging. Parasites & Vectors 6, 164.
Chaves, L. F. (2010). An entomologist guide to demystify pseudoreplication: data analysis of field studies with design constraints. Journal of Medical Entomology 47, 291298.
Chaves, L. F. and Hernandez, M.-J. (2004). Mathematical modelling of American Cutaneous Leishmaniasis: incidental hosts and threshold conditions for infection persistence. Acta Tropica 92, 245252.
Chaves, L. F., Hernandez, M.-J., Dobson, A. P. and Pascual, M. (2007). Sources and sinks: revisiting the criteria for identifying reservoirs for American cutaneous leishmaniasis. Trends in Parasitology 23, 311316.
Chaves, L. F., Cohen, J. M., Pascual, M. and Wilson, M. L. (2008a). Social exclusion modifies climate and deforestation impacts on a vector-borne disease. PLoS Neglected Tropical Diseases 2, e176.
Chaves, L. F., Hernandez, M.-J. and Ramos, S. (2008b). Simulación de modelos matemáticos como herramienta para el estudio de los reservorios de la Leishmaniasis Cutánea Americana. Divulgaciones matemáticas 16, 125154.
Chaves, L. F., Calzada, J. E., Valderama, A. and Saldaña, A. (2014). Cutaneous Leishmaniasis and Sand Fly fluctuations are associated with El Niño in Panamá. PLoS Neglected Tropical Diseases 8, e3210.
Christensen, H. A. and de Vasquez, A. M. (1982). The tree-buttress biotope: a pathobiocenose of Leishmania braziliensis . The American Journal of Tropical Medicine and Hygiene 31, 243251.
Christensen, H. A. and Herrer, A. (1972). Detection of Leishmania braziliensis by xenodiagnosis. Transactions of the Royal Society of Tropical Medicine and Hygiene 66, 798799.
Christensen, H. A. and Herrer, A. (1973). Attractiveness of sentinel animals to vectors of leishmaniasis in Panama. The American Journal of Tropical Medicine and Hygiene 22, 578584.
Christensen, H. A. and Herrer, A. (1979). Susceptibility of Sand Flies (Diptera: Psychodidae) to trypanosomatidae from two-toed sloths (Edentata:Bradypodidae). Journal of Medical Entomology 16, 424427.
Christensen, H. A. and Herrer, A. (1980). Panamanian Lutzomyia (Diptera: Psychodidae) host attraction profiles. Journal of Medical Entomology 17, 522528.
Christensen, H. A., Fairchild, G. B., Herrer, A., Johnson, C. M., Young, D. G. and Vasquez, A. M. d. (1983). The ecology of cutaneous leishmaniasis in the republic of Panama. Journal of Medical Entomology 20, 463484.
Cohen, J. (1960). A coefficient of agreement for nominal scales. Educational and Psychological Measurement 20, 3746.
Colombo, F., Odorizzi, R. F. N., Laurenti, M., Galati, E. B., Canavez, F. and Pereira-Chioccola, V. (2011). Detection of Leishmania (Leishmania) infantum RNA in fleas and ticks collected from naturally infected dogs. Parasitology Research 109, 267274.
Dantas-Torres, F. (2007). The role of dogs as reservoirs of Leishmania parasites, with emphasis on Leishmania (Leishmania) infantum and Leishmania (Viannia) braziliensis. Veterinary Parasitology 149, 139146.
Dantas-Torres, F., de Paiva-Cavalcanti, M., Figueredo, L. A., Melo, M. F., da Silva, F. J., da Silva, A. L., Almeida, E. L. and Brandão-Filho, S. P. (2010). Cutaneous and visceral leishmaniosis in dogs from a rural community in northeastern Brazil. Veterinary Parasitology 170, 313317.
Dendukuri, N. and Joseph, L. (2001). Bayesian approaches to modeling the conditional dependence between multiple diagnostic tests. Biometrics 57, 158167.
Dereure, J., Espinel, I., Barrera, C., Guerrini, F., Martini, A., Echevarria, R., Guderian, R. H. and Le Pont, F. (1994). Leishmaniose en Equateur. 4. Infestation naturelle du chien par Leishmania panamensis . Annales de la Societe belge de Medicine tropicale 74, 2933.
Dutari, L. and Loaiza, J. (2014). American cutaneous leishmaniasis in Panama: a historical review of entomological studies on anthropophilic Lutzomyia sand fly species. Parasites & Vectors 7, 218.
Dye, C., Vidor, E. and Dereure, J. (1993). Serological diagnosis of leishmaniasis: on detecting infection as well as disease. Epidemiology & Infection 110, 647656.
Falqueto, A., Sessa, P. A., Varejão, J. B. M., Barros, G. C., Momen, H. and Grimaldi Júnior, G. (1991). Leishmaniasis due to Leishmania braziliensis in Espírito Santo state, Brazil: further evidence on the role of dogs as a reservoir of infection for humans. Memorias Do Instituto Oswaldo Cruz 86, 499500.
Faraway, J. J. (2004). Linear Models with R. CRC Press, Boca Raton.
Faraway, J. J. (2006). Extending the Linear Model with R: Generalized Linear, Mixed Effects and Nonparametric Regression Models. CRC Press, Boca Raton.
Fung, H. L., Calzada, J., Saldaña, A., Santamaria, A. M., Pineda, V., Gonzalez, K., Chaves, L. F., Garner, B. and Gottdenker, N. (2014). Domestic dog health worsens with socio-economic deprivation of their home communities. Acta Tropica 135, 6774.
Garcia, L., Kindt, A., Bermudez, H., Llanos-Cuentas, A., De Doncker, S., Arevalo, J., Quispe Tintaya, K. W. and Dujardin, J.-C. (2004). Culture-independent species typing of neotropical Leishmania for clinical validation of a PCR-based assay targeting heat shock protein 70 genes. Journal of Clinical Microbiology 42, 22942297.
Garnham, P. C. C. (1965). The Leishmanias, with special reference to the role of animal reservoirs. American Zoologist 5, 141151.
Gil, J. F., Hoyos, C. L., Cimino, R. O., Krolewiecki, A. J., Lopez Quiroga, I., Cajal, S. P., Juarez, M., Garcia Bustos, M. F., Mora, M. C., Marco, J. D. and Nasser, J. R. (2011). Role of three ELISA tests using promastigote homogenates of Leishmania braziliensis, L. amazonensis and L. guyanensis in the diagnosis of tegumentary leishmaniasis. Medicina 71, 420428.
González, K., Calzada, J. E., Saldaña, A., Rigg, C., Alvarado, G., Rodríguez-Herrera, B., Kitron, U. D., Adler, G. H., Gottdenker, N. L., Chaves, L. F. and Baldi, M. (2015). Survey of wild mammal hosts of Cutaneous Leishmaniasis parasites in Panamá and Costa Rica. Tropical Medicine and Health 43, 7578.
Hernández, D., Rojas, E., Scorza, J. V. and Jorquera, A. (2006). Infectividad del perro (Canis familiaris) para Lutzomyia youngi en Trujillo, Venezuela. Biomedica 26, s242s248.
Herrer, A. and Christensen, H. A. (1976a). Epidemiological patterns of Cutaneous Leishmaniasis in Panama: III. Endemic persistence of the disease. The American Journal of Tropical Medicine and Hygiene 25, 5458.
Herrer, A. and Christensen, H. A. (1976b). Natural Cutaneous Leishmaniasis among dogs in Panama. The American Journal of Tropical Medicine and Hygiene 25, 5963.
Herrer, A. and Christensen, H. A. (1980). Leishmania braziliensis in the Panamanian two-toed sloth, Choloepus hoffmanni . The American Journal of Tropical Medicine and Hygiene 29, 11961200.
Krebs, C. J. (1998). Ecological Methodology. New York: Benjamin Cummings.
Landis, J. R. and Koch, G. G. (1977). The measurement of observer agreement for categorical data. Biometrics 33, 159174.
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™) in dogs with and without signs of the disease. Acta Tropica 107, 205207.
Levins, R. (1968). Evolution in Changing Environments. Some Theoretical Explorations. Princeton University Press, Princeton.
Levins, R. (2006). Strategies of abstraction. Biology & Philosophy 21, 741755.
Marco, J., Barroso, P., Mimori, T., Locatelli, F., Tomatani, A., Mora, M., Cajal, S., Nasser, J., Parada, L., Taniguchi, T., Korenaga, M., Basombrio, M. and Hashiguchi, Y. (2012). Polymorphism-specific PCR enhances the diagnostic performance of American tegumentary leishmaniasis and allows the rapid identification of Leishmania species from Argentina. BMC Infectious Diseases 12, 191.
Marco, J. D., Padilla, A. M., Diosque, P., Fernández, M. M., Malchiodi, E. L. and Basombrío, M. A. (2001). Force of infection and evolution of lesions of canine tegumentary leishmaniasis in Northwestern Argentina. Memorias Do Instituto Oswaldo Cruz 96, 649652.
Miranda, A., Saldaña, A., González, K., Paz, H., Santamaría, G., Samudio, F. and Calzada, J. E. (2012). Evaluation of PCR for cutaneous leishmaniasis diagnosis and species identification using filter paper samples in Panama, Central America. Transactions of the Royal Society of Tropical Medicine and Hygiene 106, 544548.
Morrison, A. C., Ferro, C., Morales, A., Tesh, R. B. and Wilson, M. L. (1993). Dispersal of the sand fly Lutzomyia longipalpis (Diptera: Psychodidae) at an endemic focus of Visceral Leishmaniasis in Colombia. Journal of Medical Entomology 30, 427435.
OIE (2008). Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, 6th Edn. Office International de Epizooties, Paris, France.
Padilla, A. M., Marco, J. D., Diosque, P., Segura, M. A., Mora, M. C., Fernández, M. M., Malchiodi, E. L. and Basombrío, M. A. (2002). Canine infection and the possible role of dogs in the transmission of American tegumentary leishmaniosis in Salta, Argentina. Veterinary Parasitology 110, 110.
Pan, W. (2001). Akaike's information criterion in generalized estimating equations. Biometrics 57, 120125.
Pedroso, A. M. (1913). Leishmania local de cão. Annais Paulistas de Medicina e Cirurgia 1, 3340.
Pineda, V., Saldaña, A., Monfante, I., Santamaría, A., Gottdenker, N. L., Yabsley, M. J., Rapoport, G. and Calzada, J. E. (2011). Prevalence of trypanosome infections in dogs from Chagas disease endemic regions in Panama, Central America. Veterinary Parasitology 178, 360363.
Pirmez, C., Coutinho, S. G., Marzochi, M. C. A., Nunes, M. P. and Grimaldi, G. (1988). Canine American cutaneous leishmaniasis: a clinical and immunological study in dogs naturally infected with Leishmania braziliensis braziliensis in an endemic area of Rio de Janeiro, Brazil. The American Journal of Tropical Medicine and Hygiene 38, 5258.
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., Carson, C., Reithinger, R., Garcez, L. M. and Courtenay, O. (2013). Evaluation of rK39 rapid diagnostic tests for Canine Visceral Leishmaniasis: longitudinal study and meta-analysis. PLoS Neglected Tropical Diseases 7, e1992.
Quintana, M. G., Salomon, O. D., De Grosso, M. and Lizarralde, S. (2010). Distribution of Phlebotomine Sand Flies (Diptera: Psychodidae) in a Primary Forest-Crop Interface, Salta, Argentina. Journal of Medical Entomology 47, 10031010.
Reithinger, R. and Davies, C. R. (1999). Is the domestic dog (Canis familiaris) a reservoir host of American cutaneous leishmaniasis? A critical review of the current evidence. The American Journal of Tropical Medicine and Hygiene 61, 530541.
Reithinger, R. and Davies, C. R. (2002). American cutaneous leishmaniasis in domestic dogs: an example of the use of the polymerase chain reaction for mass screening in epidemiological studies. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, S1/123S121/126.
Reithinger, R., Lambson, B. E., Barker, D. C. and Davies, C. R. (2000). Use of PCR to detect Leishmania (Viannia) spp. in dog blood and bone marrow. Journal of Clinical Microbiology 38, 748751.
Reithinger, R., Lambson, B. E., Barker, D. C., Counihan, H., Espinoza, J. C., González, J. S. and Davies, C. R. (2002). Leishmania (Viannia) spp. dissemination and tissue tropism in naturally infected dogs (Canis familiaris). Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 7678.
Reithinger, R., Espinoza, J. C. and Davies, C. R. (2003a). The transmission dynamics of canine american cutaneous Leishmaniasis in Huánuco, Perú. The American Journal of Tropical Medicine and Hygiene 69, 473480.
Reithinger, R., Espinoza, J. C., Llanos-Cuentas, A. and Davies, C. R. (2003b). Domestic dog ownership: a risk factor for human infection with Leishmania (Viannia) species. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 141145.
Reithinger, R., Grijalva, M. J., Chiriboga, R. F., Alarcón de Noya, B., Torres, J. R., Pavia-Ruz, N., Manrique-Saide, P., Cardinal, M. V. and Gürtler, R. E. (2010). Rapid detection of Trypanosoma cruzi in human serum by use of an immunochromatographic dipstick test. Journal of Clinical Microbiology 48, 30033007.
Rojas, E. and Scorza, J. V. (1990). Xenodiagnóstico con Lutzomyia youngi en casos Venezolanos de leishmaniasis cutánea por Leishmania braziliensis . Memorias Do Instituto Oswaldo Cruz 84, 2934.
Saldaña, A., Chaves, L. F., Rigg, C. A., Wald, C., Smucker, J. E. and Calzada, J. E. (2013). Clinical Cutaneous Leishmaniasis rates are associated with household Lutzomyia gomezi, Lu. panamensis, and Lu. trapidoi abundance in Trinidad de Las Minas, Western Panama. The American Journal of Tropical Medicine and Hygiene 88, 572574.
Sokal, R. R. and Rohlf, F. J. (1994). Biometry: the Principles and Practices of Statistics in Biological Research, 3rd Edn. W. H. Freeman, New York, USA.
Southwood, T. R. E. (1978). Ecological Methods. Chapman & Hall, London.
Stewart, L., Gosling, R., Griffin, J., Gesase, S., Campo, J., Hashim, R., Masika, P., Mosha, J., Bousema, T., Shekalaghe, S., Cook, J., Corran, P., Ghani, A., Riley, E. M. and Drakeley, C. (2009). Rapid assessment of malaria transmission using age-specific sero-conversion rates. PLoS ONE 4, e6083.
Telford, S. R. Jr., Herrer, A. and Christensen, H. A. (1972). Enzootic cutaneous leishmaniasis in eastern Panama. 3. Ecological factors relating to the mammalian hosts. Annals of Tropical Medicine and Parasitology 66, 173179.
Thatcher, V. E. and Hertig, M. (1966). Field studies on the feeding habits and diurnal shelters of some phlebotomus sandflies (Diptera: Psychodidae) in Panama. Annals of the Entomological Society of America 59, 4652.
Travi, B. L., Tabares, C. J. and Cadena, H. (2006). Leishmania (Viannia) braziliensis infection in two Colombian dogs: a note on infectivity for sand flies and response to treatment. Biomedica 26, s249s253.
Venables, W. N. and Ripley, B. D. (2002). Modern Applied Statistics with S. Springer, New York, USA.
Vergel, C., Walker, J. and Saravia, N. G. (2005). Amplification of human DNA by primers targeted to Leishmania kinestoplast DNA and Post-Genome considerations in the detection of parasites by a polymerase chain reaction. The American Journal of Tropical Medicine and Hygiene 72, 423429.
Viana, M., Mancy, R., Biek, R., Cleaveland, S., Cross, P. C., Lloyd-Smith, J. O. and Haydon, D. T. (2014). Assembling evidence for identifying reservoirs of infection. Trends in Ecology & Evolution 29, 270279.
Young, D. G. and Duncan, M. A. (1994). Guide to the Identification and Geographic Distribution of Lutzomyia Sand Flies in Mexico, the West Indies, Central and South America (Diptera: Psychodidae). Associated Publishers, Gainesville, FL, USA.


Type Description Title
Supplementary materials

Calzada supplementary material
Calzada supplementary material 1

 Unknown (1.8 MB)
1.8 MB


Altmetric attention score

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