Leishmania in Marsupials—An Overview of Infection Records in the Americas and Australia

Marsupials have been the subjects of studies of both experimental and natural infections with different species of Leishmania in the Americas as well as Australia. Over a century has passed since the first description of a mammal being infected with Leishmania and since then several reviews have been published on the systematics of the parasites as well as their hosts. Consequently, an update of this information is needed in order to assure correct identification of the species involved in each case. A comprehensive review was undertaken and included most of the records of marsupials being infected with Leishmania sp. Emphasis was placed on parasitological, eco epidemiological and taxonomic information of both the parasites and mammalian hosts. The clinical profiles of the infections varied from severe, which principally occurred in experimentally infected animals, to asymptomatic, which was typical of natural infections. Marsupials must be considered one of the most important groups of mammalian hosts of Leishmania sp. Important factors, such as their ancient origin, wide geographical distribution and susceptibility to infections by different species of Leishmania, but with considerable resistance to the disease, could indicate that didelphids play a key role in the evolution of Leishmania in the New World.

[1]  R. Booth,et al.  Marsupials , 2020, Exotic Animal Laboratory Diagnosis.

[2]  R. Gurgel-Gonçalves,et al.  Expanding the knowledge about Leishmania species in wild mammals and dogs in the Brazilian savannah , 2015, Parasites & Vectors.

[3]  Eliécer E. Gutiérrez,et al.  Phylogenetic Relationships of Mouse Opossums (Didelphidae, Marmosa) with a Revised Subgeneric Classification and Notes on Sympatric Diversity , 2014 .

[4]  A. Marcili,et al.  Survey of Leishmania Infantum Chagasi in Wild and Domestic Animals in Urban Area and Atlantic Rainforest Fragment in Northeast, Brazil , 2014 .

[5]  M. Brito,et al.  Small mammals as hosts of Leishmania spp. in a highly endemic area for zoonotic leishmaniasis in North-Eastern Brazil. , 2013, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[6]  C. Ocampo,et al.  Environmental factors associated with American cutaneous leishmaniasis in a new Andean focus in Colombia , 2012, Tropical medicine & international health : TM & IH.

[7]  J. C. Carreira,et al.  Natural infection of Didelphis aurita (Mammalia: Marsupialia) with Leishmania infantum in Brazil , 2012, Parasites & Vectors.

[8]  A. Paglia,et al.  Wild, synanthropic and domestic hosts of Leishmania in an endemic area of cutaneous leishmaniasis in Minas Gerais State, Brazil. , 2011, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[9]  L. Floeter-Winter,et al.  Leishmania spp. in Didelphis albiventris and Micoureus paraguayanus (Didelphimorphia: Didelphidae) of Brazil. , 2011, Veterinary parasitology.

[10]  J. Bickham,et al.  Molecular phylogenetics of Reig's short-tailed opossum (Monodelphis reigi) and its distributional range extension into Guyana , 2010 .

[11]  R. Voss,et al.  A Revision of the Didelphid Marsupial Genus Marmosa Part 1. The Species in Tate's ‘Mexicana’ and ‘Mitis’ Sections and Other Closely Related Forms , 2010 .

[12]  S. Jansa,et al.  Phylogenetic Relationships and Classification of Didelphid Marsupials, an Extant Radiation of New World Metatherian Mammals , 2009 .

[13]  F. Andrade-Narváez,et al.  Comparison of small mammal prevalence of Leishmania (Leishmania) mexicana in five foci of cutaneous leishmaniasis in the State of Campeche, Mexico. , 2009, Revista do Instituto de Medicina Tropical de Sao Paulo.

[14]  A. Dougall,et al.  New reports of Australian cutaneous leishmaniasis in Northern Australian macropods , 2009, Epidemiology and Infection.

[15]  A. L. Gardner Mammals of South America, Volume 1: Marsupials, Xenarthrans, Shrews, and Bats , 2008 .

[16]  D. Munari,et al.  An investigation of Leishmania spp. in Didelphis spp. from urban and peri-urban areas in Bauru (São Paulo, Brazil). , 2007, Veterinary parasitology.

[17]  G. Schoone,et al.  Didelphis marsupialis (common opossum): a potential reservoir host for zoonotic leishmaniasis in the metropolitan region of Belo Horizonte (Minas Gerais, Brazil). , 2007, Vector borne and zoonotic diseases.

[18]  G. R. Seamons,et al.  Mammal Species of the World: A Taxonomic and Geographic Reference (3rd edition) , 2006 .

[19]  C. Dickman,et al.  Marsupials: List of Contributors , 2006 .

[20]  W. Krause,et al.  The opossum : its amazing story , 2006 .

[21]  S. Jansa,et al.  On the Contents of Gracilinanus Gardner and Creighton, 1989, with the Description of a Previously Unrecognized Clade of Small Didelphid Marsupials , 2005 .

[22]  E. Douzery,et al.  New DNA data from a transthyretin nuclear intron suggest an Oligocene to Miocene diversification of living South America opossums (Marsupialia: Didelphidae). , 2005, Molecular phylogenetics and evolution.

[23]  R. Voss,et al.  An Introduction to Marmosops (Marsupialia: Didelphidae), with the Description of a New Species from Bolivia and Notes on the Taxonomy and Distribution of Other Bolivian Forms , 2004 .

[24]  K. Rose Cutaneous leishmaniasis in red kangaroos. , 2004, Australian veterinary journal.

[25]  S. Solari A new species of Monodelphis (Didelphimorphia: Didelphidae) from southeastern Peru , 2004 .

[26]  S. Jansa,et al.  Phylogenetic Studies on Didelphid Marsupials I. Introduction and Preliminary Results from Nuclear IRBP Gene Sequences , 2004, Journal of Mammalian Evolution.

[27]  B. Travi,et al.  Feeding success of Lutzomyia evansi (Diptera: Psychodidae) experimentally exposed to small mammal hosts in an endemic focus of Leishmania chagasi in northern Colombia. , 2003, Biomedica : revista del Instituto Nacional de Salud.

[28]  S. Jansa,et al.  PHYLOGENETIC STUDIES ON DIDELPHID MARSUPIALS II. NONMOLECULAR DATA AND NEW IRBP SEQUENCES: SEPARATE AND COMBINED ANALYSES OF DIDELPHINE RELATIONSHIPS WITH DENSER TAXON SAMPLING , 2003 .

[29]  M. Brito,et al.  Wild and synanthropic hosts of Leishmania (Viannia) braziliensis in the endemic cutaneous leishmaniasis locality of Amaraji, Pernambuco State, Brazil. , 2003, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[30]  Daniel Lew,et al.  Una nueva especie del género Monodelphis (Didelphimorphia: Didelphidae) de la Sierra de Lema, Venezuela , 2003 .

[31]  R. Cerqueira,et al.  MORPHOLOGICAL DIFFERENTIATION IN THE WHITE-EARED OPOSSUM GROUP (DIDELPHIDAE: DIDELPHIS) , 2002 .

[32]  M. Ulrich,et al.  Epidemiologic aspects of American visceral leishmaniasis in an endemic focus in Eastern Venezuela. , 1999, The American journal of tropical medicine and hygiene.

[33]  C. Davies,et al.  Natural infections of Leishmania peruviana in animals in the Peruvian Andes. , 1999, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[34]  B. Travi,et al.  Dynamics of Leishmania chagasi infection in small mammals of the undisturbed and degraded tropical dry forests of northern Colombia. , 1998, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[35]  B. Alexander,et al.  Detection of Leishmania (Viannia) braziliensis complex in wild mammals from Colombian coffee plantations by PCR and DNA hybridization. , 1998, Acta tropica.

[36]  B. Travi,et al.  Leishmania (Leishmania) chagasi: clinical and parasitological observations in experimentally infected Didelphis marsupialis, reservoir of New World visceral leishmaniasis. , 1998, Experimental parasitology.

[37]  Í. Sherlock Ecological interactions of visceral leishmaniasis in the state of Bahia, Brazil. , 1996, Memorias do Instituto Oswaldo Cruz.

[38]  J. Malcolm,et al.  Hierarchical genetic structure and gene flow in three sympatric species of Amazonian rodents , 1996, Molecular ecology.

[39]  J. Alvar,et al.  Infectivity of dogs naturally infected with Leishmania infantum to colonized Phlebotomus perniciosus. , 1994, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[40]  I. Velez,et al.  Didelphis marsupialis, an important reservoir of Trypanosoma (Schizotrypanum) cruzi and Leishmania (Leishmania) chagasi in Colombia. , 1994, The American journal of tropical medicine and hygiene.

[41]  E. Cupolillo,et al.  Description of Leishmania (Leishmania) forattinii sp. n., a new parasite infecting opossums and rodents in Brazil , 1993 .

[42]  Daryl E. Wilson,et al.  Mammal Species of the World: A Taxonomic and Geographic Reference , 1993 .

[43]  C. Greene,et al.  Experimental Visceral Leishmaniasis in the Opossum , 1989, Veterinary pathology.

[44]  R. Tesh,et al.  Epidemiology of visceral leishmaniasis in Colombia. , 1989, The American journal of tropical medicine and hygiene.

[45]  R. Tesh,et al.  Didelphis marsupialis, an apparent wild reservoir of Leishmania donovani chagasi in Colombia, South America. , 1989, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[46]  A. L. Gardner,et al.  A new generic name for Tate's (1933) Microtarsus group of South American mouse opossums (Marsupialia: Didelphidae) , 1989 .

[47]  W. Mr,et al.  A comparison of experimental visceral leishmaniasis in the opossum, armadillo and ferret. , 1989 .

[48]  W. Hanson,et al.  A comparison of experimental visceral leishmaniasis in the opossum, armadillo and ferret. , 1989, Laboratory animal science.

[49]  Ítalo A. Sherlock,et al.  Observações sobre calazar em Jacobina, Bahia. VI - Investigações sobre reservatórios silvestres e comensais , 1988 .

[50]  H. Momen,et al.  Leishmania mexicana in Didelphis marsupialis aurita in São Paulo State, Brazil. , 1985, Revista do Instituto de Medicina Tropical de Sao Paulo.

[51]  Rui Cerqueira,et al.  The distribution of Didelphis in South America (Polyprotodontia, Didelphidae) , 1985 .

[52]  G. Grimaldi júnior,et al.  Natural infection of the opossum Didelphis albiventris (Marsupialia, Didelphidae) with Leishmania donovani, in Brazil. , 1984, Memorias do Instituto Oswaldo Cruz.

[53]  J. Arias,et al.  The principal reservoir host of cutaneous leishmaniasis in the urban areas of Manaus, Central Amazon of Brazil. , 1981, Memorias do Instituto Oswaldo Cruz.

[54]  J. Shaw,et al.  Leishmaniasis in Brazil: XVI. Isolation and identification of Leishmania species from sandflies, wild mammals and man in north Para State, with particular reference to L. braziliensis guyanensis causative agent of "pian-bois". , 1981, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[55]  M. Miles,et al.  The opossum, Didelphis marsupialis (Marsupialia: Didelphidae), as a reservoir host of Leishmania braziliensis guyanensis in the Amazon Basin of Brazil. , 1981, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[56]  W. Hanson,et al.  Leishmania donovani in the oppossum (Didelphis marsupialis). , 1980, The Journal of parasitology.

[57]  J. Shaw,et al.  Some methods for the enzymic characterization of Latin-American Leishmania with particular reference to Leishmania mexicana amazonensis and subspecies of Leishmania hertigi. , 1980, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[58]  F. Corrêa,et al.  [Finding of Leishmania species in Didelphis marsupialis aurita in the state of São Paulo, Brazil. preliminary note]. , 1979, Revista do Instituto de Medicina Tropical de Sao Paulo.

[59]  E. Tikasingh Enzootic rodent leishmaniasis in Trinidad, West Indies. , 1974, Bulletin of the Pan American Health Organization.

[60]  A. Herrer,et al.  Detection of leishmanial activity in nature by means of sentinel animals. , 1973, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[61]  A. Herrer,et al.  Enzootic cutaneous leishmaniasis in eastern Panama. 3. Ecological factors relating to the mammalian hosts. , 1972, Annals of tropical medicine and parasitology.

[62]  A. Herrer,et al.  Enzootic cutaneous leishmaniasis in Eastern Panama. I. Investigation of the infection among forest mammals. , 1971, Annals of tropical medicine and parasitology.

[63]  M. Hertig,et al.  Behavior of Leishmania in Panamanian phlebotomine sandflies fed on infected animals. , 1970, Experimental parasitology.

[64]  J. Shaw,et al.  Leishmaniasis in Brazil. V. Studies on the epidemiology of cutaneous leishmaniasis in Mato Grosso State, and observations on two distinct strains of Leishmania isolated from man and forest animls. , 1970, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[65]  J. Shaw,et al.  Leishmaniasis in Brazil. 3. Cutaneous leishmaniasis in an opossum, Marmosa murina (Marsupialia, Didelphidae) from the lower Amazon region. , 1969, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[66]  E. Tikasingh Leishmaniasis in Trinidad. A preliminary report. , 1969, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[67]  R. Lainson,et al.  THE EPIDEMIOLOGY OF DERMAL LEISHMANIASIS IN BRITISH HONDURAS: II. RESERVOIR-HOSTS OF LEISHMANIA MEXICANA AMONG THE FOREST RODENTS. , 1964, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[68]  R. Lainson,et al.  Dermal Leishmaniasis in British Honduras: Some Host-reservoirs of L. brasiliensis mexicana , 1962, British medical journal.

[69]  A. Bolliger,et al.  Transmission of kala-azar to the Australian marsupials Trichosurus vulpecula and Pseudocheirus laniginosus. , 1948, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[70]  A. Bolliger,et al.  Transmission of Kala-Azar to the Pouch Young of the Common Australian Possum (Trichosurus vulpecula) , 1945, Nature.

[71]  G. H. Tate A systematic revision of the marsupial genus Marmosa : with a discussion of the adaptive radiation of the murine opossums (Marmosa). Bulletin of the AMNH ; v. 66, article 1 , 1933 .