Infection agents of Didelphidae (Didelphimorphia) of Brazil: an underestimated matter in zoonoses research
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Matheus M. Bitencourt
and
Alexandra M. R. Bezerra
Abstract
Zoonoses are diseases or infections naturally transmissible from vertebrate animals to humans, and can be bacterial, viral or parasitic. The growth of urbanization, industrialization and the advance of agriculture and livestock facilitate the spread of infectious and parasitic agents from wild animals to the human population and to their domestic animals. Among the various reservoirs of zoonotic agents, we find that didelphid species, due to their high capacity for adaptation in urban environments, as an important study case. We reviewed the literature data on the pathogens, including with zoonotic potential of marsupial species occurring in Brazil, accounted for infections by agents that we categorized into Bacteria, Viruses, Protozoa, and Helminths. Aiming identifies possible knowledge gaps, we also surveyed the origin of studied samples and the institutions leading the researches on host didelphids. Among the hosts, the genus Didelphis in the cycles of these agents stands out. Moreover, we found that the majority of reported cases are in the Southeastern Brazil, mean the data from other Brazilian localities and didelphid species could be underestimated. Most studies took place in graduate programs of public research institutions, emphasizing the importance of the funding public research for the Brazilian scientific development.
1 Introduction
Currently, three orders of marsupials are recognized in South America: Microbiotheria, Paucituberculata and Didelphimorphia (Gardner 2008), the last being the most diverse and consisting of a single family, Didelphidae, containing four subfamilies: Glironiinae, Caluromyinae, Didelphinae, and Hyladelphinae (Voss and Jansa 2009). In Brazil, there are 15 genera and 66 species, distributed across all biomes (Abreu et al. 2021; Gardner 2008; Quintela et al. 2020). However, this number is expected to increase with new taxonomic reviews and surveys in areas that have not been sampled or isolated, such as the northern and western Amazon and in southern Pampas biomes (Melo and Sponchiado 2012; Pavan 2019). These species are mostly nocturnal and have omnivorous diet, which may include fruits, nectar, invertebrates and even small vertebrates (Conceição and Bocchiglieri 2017; Dos Santos 2012). Reproductive strategies can vary according to the type of habitat and the availability of resources (Begon et al. 2006), in addition, didelphid marsupials can occupy a large number of habitats, including environments modified by man, and are commonly found inhabiting peridomiciliary areas, which denotes the importance of this taxon as a potential natural reservoir of zoonotic agents (Cantor et al. 2010; Diniz et al. 2008).
Reservoir is a complex ecological system that can be formed by one or more species, responsible for maintaining a parasite in nature (Brasil 2020), while zoonoses are diseases or infections naturally transmissible from vertebrate animals to humans, and can be bacterial, viral or parasitic (WHO 2021). There are more than 200 zoonoses types, some are preventable by vaccination, such as rabies, or another method (WHO 2021). Currently, the infectious diseases most dangerous to humans were originated from birds and mammals, such as rabies, Ebola, yellow fever, AIDS and Covid-19 (Weiss 2001; WHO 2021). The urban expansion and the advance of the agribusiness facilitate the spilling over of infectious and parasitic agents from wild animals to the human population and its domesticated animals (Corrêa and Passos 2001). It occurs mainly due resources competition, favoring the adaptability of wild animals in anthropic environments and increasing the probability of contact among the different species, including the zoophagy (Cantor et al. 2010; Da Silva et al. 2018). In Brazil, this is particularly worrisome, since the country suffered severe environmental degradation in the last years, with deforestations and burnt areas (Silva et al. 2020) and weakening environmental laws (Bragagnolo et al. 2017).
Multiple approaches in zoonotic studies meet the One Health concept of integrating human health, animal health and the environmental, aim gather data for prediction and control of zoonotic diseases (WHO 2017). Given the background, we aim investigate the zoonotic potential of didelphid species occurring in Brazil. We survey the didelphid as hosts of pathogens potentially infectious to humans, and discussed these data in the context of geographical prevalence.
2 Materials and methods
We carried out a survey in the scientific “Periódicos da CAPES” (http://www.periodicos.capes.gov.br/), “Biblioteca Virtual em Saúde” (https://www.bvsdip.icict.fiocruz.br/), “PubMed” (http://www.ncbi.nlm.nih.gov/pubmed/), “BioOne” (https://bioone.org/), “Scopus” (https://www.scopus.com), and “Google Scholar” (https://scholar.google.com.br/), using the combinations of the keywords Didelphimorphia, Brazil and marsupial, combined with the words: bacterium, virus, protozoa, helminth, nematode, platyhelminth, diseases and zoonoses (in both Portuguese and English languages). We only consider studies that provide geographic coordinates or inform the municipalities/cities of the collection site. For studies that have neighboring locations, we use a midpoint between their coordinates. We discard publications that do not identify the hosts at least at the genus level, while the identification at the species level of the marsupials were hypothesized taking into account their geographic distribution, based on Melo and Sponchiado (2012).
We organized the studies in relation to species of marsupial, locality, etiological agent and methodology used, in the latter we categorize into serological tests, culture, PCR (Polymerase Chain Reaction), and fresh microscopy/research. The marsupial nomenclature follows Abreu et al. (2021) in cases where the exact host identification might be unable to update, we have kept the original identification of the original studies. For the counting of institutions linked to projects on pathogenic agents in marsupials, we used only the institution of the first author of each study found. For the map preparation we divided the pathogens into four groups: bacteria, viruses, protozoa and helminths; and the hosts were divided by genus level. Maps were made using the QGIS program version 2.18.9 ‘Las Palmas’ (QGIS 2017).
3 Results
We found 119 studies showing didelphids infected with pathogenic agents, including with zoonotic potential (Supplementary material). Of the genera of marsupials that occur in Brazil, nine were mentioned in the surveyed studies (Figures 1 –3). The Southeastern region accounts most cases. The Supplementary material lists the positive cases of marsupials for pathogenic agents, methods, in addition to the locations, with the most specific coordinates possible, and the research institutions where the studies were carried out. Table 1 summarizes the characteristics of the main zoonoses found in marsupials in the Brazil, based on the number of records.
Maps with positive locations for pathogenic agents found in species of the genus Didelphis. The referenced points are listed in the complementary data. Photo credit: Alexandra M.R. Bezerra.
Maps with positive locations for pathogenic agents found in species of the genera Caluromys, Gracilinanus, Lutreolina, and Marmosa, respectively. The referenced points are listed in the complementary data. Photo credits: Caluromys lanatus by André F. Mendonça, Gracilinanus agilis and Marmosa (Micoureus) constantiae by Alexandra M. R. Bezerra, and Lutreolina crassicaudata by Flávio H. G. Rodrigues.
Maps with positive locations for pathogenic agents found in species of the genera Marmosops, Metachirus, Monodelphis, Philander, and Thylamys, respectively. The referenced points are listed in the complementary data. Photo credits: Marmosops ocellatus, Monodelphis domestica, Thylamys karimii by Alexandra M. R. Bezerra, and Metachirus nudicaudatus and Philander opossum by Paola da Mata.
Summary information on the main zoonoses found in marsupials in Brazil.
| Disease | Etiological agent | Symptoms | Transmission | Main hosts | References |
|---|---|---|---|---|---|
| Leptospirosis | Leptospira | Anorexia, fever, muscle pain, nausea, vomiting, constipation or diarrhea, arthralgia, conjunctival hyperemia or hemorrhage, photophobia and eye pain | Contact with urine from infected animals | Rodentia, Artiodactyla, Didelphimorphia, Carnivora, Chiroptera and Primates | Costa et al. (2001), Brasil (2020), Martins and Spink (2020) |
| Salmonellosis | Salmonella | Abdominal pain, diarrhea, low hyperthermia and emesis rarely progressing to lethal clinical events | Consumption of contaminated food and through contact with infected animals. | Mammals, birds and reptiles | Sant’ana et al. (2008), Shinohara et al. (2008) |
| Lyme-borreliosis | Borrelia | Erythema migrans, chronic atrophic acrodermatitis, Lyme arthritis, borrelian lymphocytoma, neuroborreliosis and Lyme carditis, in addition to asymptomatic infection | Through the tick bite | Rodentia and Didelphimorphia | Berglund et al. (1995), Stanek and Strle (2009), Stanek et al. (2012) |
| Anaplasmosis | Anaplasma | Fever, compromised general status, headache, myalgia, arthralgia and, to a lesser extent, maculopapular eruption | Through the tick bite | Rodentia, Cervidae, Bovidae and Canidae | Dumler et al. (2001), Abarca et al. (2008) |
| Ehrlichiosis | Ehrlichia | Fever, compromised general status, headache, myalgia, arthralgia and, to a lesser extent, maculopapular eruption | Through the tick bite | Rodentia, Cervidae, Bovidae and Canidae | McQuiston et al. (1999), Abarca et al. (2008) |
| Rocky mountain spotted fever | Rickettsia | Fever, headache, intense myalgia, nausea and vomiting, later appearing the maculopapular rash | Through the tick bite | Rodentia, Canidae and Equidae | Abramson and Givner (1999), Moraes-Filho et al. (2009) |
| Brucellosis | Brucella | Chills, headaches, constipation, generalized pain and, in the case of chronic infections, decreased fertility | Direct contact with infected animals and consumption of unpasteurized milk products | Rodentia, Carnivora, Cetacea, Bovidae, Suidae and Equidae | Ariza et al. (1995), Galinska and Zagórski (2013) |
| Bartonellosis, trench fever, cat scratch disease | Bartonella | Fever, malaise, headache, and anorexia may accompany lymphadenopathy | Through bites and scratches from infected animals and by the bite of fleas and lice | Felidae, Rodentia and Bovidae | Abbott et al. (1997), Spach and Koehler (1998) |
| Mycoplasmosis | Mycoplasma | Sore throat, cough, headache, malaise, chills, fever, rash and pneumonia | Through droplets | Rodentia, Carnivora and birds | Waites and Talkington (2004), Prezotto et al. (2015), De Sousa et al. (2017) |
| Bubonic plague | Yersinia | Headache, fever, generalized pain, myalgia, anorexia, nausea, vomiting, mental confusion, conjunctival congestion, rapid and irregular pulse, tachycardia, hypotension and prostration | Through the bite of infected fleas or by ingesting contaminated water and food, depending on the species | Rodentia, Didelphimorphia, Lagomorpha and Artiodactyla | Salyers and Whitt (2002), Dias et al. (2021) |
| Dengue, yellow fever | Flavivirus | Headache, myalgia, prostration, arthralgia, anorexia, asthenia, retroorbital pain, nausea, vomiting, exanthema, itchy skin, which may worsen to hemorrhagic manifestations and circulatory collapse | Through mosquito bites | Primates | Ribeiro and Antunes (2009), Brasil (2020) |
| Rabies | Lyssavirus | Slight increase in temperature, anorexia, headache, nausea, sore throat, numbness, irritability, restlessness and feeling of anguish. Hyperesthesia and paresthesia may occur in the path of peripheral nerves | Through the saliva of an infected animal | Chiroptera, Carnivora and Primates | De Lima and Gagliani (2014), Brasil (2020) |
| Hepatitis | Hepatovirus | Jaundice and dark urine | Ingestion of food and water contaminated with excreta and secretions | Mammals | Pereira and Gonçalves (2003), Smith and Simmonds (2018) |
| Hantaviruses | Hantavirus | Fever, hypotension, oliguria, polyuria and convalescence | Inhalation of aerosols contaminated with excreta and secretions from infected animals | Rodentia | Schönrich et al. (2008), Mattar et al. (2015) |
| Rotavirus gastroenteritis | Rotavirus | Severe watery diarrhea, fever, loss of appetite, stomach pain and vomiting | Ingestion of food and water contaminated with excreta and secretions | Mammals and birds | Cardoso et al. (1989), Dhama et al. (2015) |
| Measles | Morbillivirus | Fever, dry cough, runny nose, non-purulent conjunctivitis and Koplik’s spots | Contact with infected secretions | Mammals | Quadros et al. (2020), Takeda et al. (2020) |
| Other viroses | Ex: Alphavirus, Bunyavirus, Orthobunyavírus, Orthopoxvirus, Sigmatorquevirus, Alphatorquevirus | Febre, tosse, dor de cabeça e na garganta, coriza e perda de olfato e/ou paladar. Fever, cough, headache and throat, runny nose and loss of smell and/or taste | Contact with infected secretions and excreta | Vertebrates | Vasconcelos et al. (1991), Silva and Angerami (2008) |
| Leishmaniasis | Leishmania | Skin lesions, which may present with long-lasting fever, weight loss, asthenia, adynamia and anemia | Through the bite of several species of sandflies | Rodentia, Didelphimrphia, Carnivora and Pilosa | Carvalho et al. (2002), Brasil (2020) |
| Toxoplasmosis | Toxoplasma | Asymptomatic, but infection during pregnancy can lead to miscarriage, motor and mental retardation, or loss of vision | Ingestion of raw or undercooked meat or consumption of contaminated water and food | Felidae | Lopes and Berto (2012), Brasil (2020) |
| Chagas disease | Trypanosoma | Fever, malaise, headache, asthenia, hyporexia, edema, lymph node hypertrophy | Through triatomine feces | Mammals | Brasil (2020), Rodrigues et al. (2020) |
| Neosporosis | Neospora | – | Ingestion of raw or undercooked meat or consumption of contaminated water and food | Canidae, Mustelidae, Artiodactyla, Rodentia, Equidae and birds | Collery (1996), Tranas (1999), Dubey (2003) |
| Sarcocystosis | Sarcocystis | Fever, anorexia, prostration, pale mucous membranes, runny nose and eyes, dyspnea, salivation, which can cause death. These symptoms are usually more severe in immunocompromised patients | Ingestion of raw or undercooked meat | Mammals | Poulsen and Stensvold (2014), Dubey (2015) |
| Cryptosporidiosis | Cryptosporidium | Watery diarrhea, weight loss, cramps, nausea, vomiting, headaches and low-grade fever | Consumption of contaminated food and water | Mammals | Fayer et al. (2000), Xiao and Feng (2008) |
| Worms diseases | Platyhelminthes, Nematoda, Acanthocephala | Abdominal pain, nausea, vomiting, diarrhea, poor appetite, weight loss and anemia | Consumption of contaminated food and water, and direct contact with larvae in the soil | Vertebrates | Carneiro and Antunes 2010 |
We account 40 research institutions conducting studies on pathogenic agents in marsupials, with the Instituto Oswaldo Cruz (IOC), Rio de Janeiro state, being the institution with the largest number of studies, followed by the Universidade de São Paulo (USP) and the Universidade Estadual de São Paulo (UNESP), São Paulo state, all in the Southeastern region of Brazil. The other institutions presented a maximum of three studies on the topic (Figure 4). The most used methodology was serology, except for the helminths, which the fresh microscopy prevails (Table 2). Recently (last decade mainly), occurred the increased use of PCR in some studies, including it as complementary to the former methods (Carneiro 2018; Carreira et al. 2012; Fornazari et al. 2018; Laforente et al. 2021; Rocha et al. 2013).
Number of studies carried out on pathogenic infections and zoonotic diseases in marsupials by institutions and Brazilian regions (Northern in lilac, Northeastern in light blue, Central in coral, Southeastern in yellow, and Southern in green). Acronyms: APTA (Agência Paulista de Tecnologia dos Agronegócios), IAM (Instituto Aggeu Magalhães), IEC (Instituto Evandro Chagas), IGM (Instituto Gonçalo Moniz), INPA (Instituto Nacional de Pesquisa da Amazônia, IOC (Instituto Oswaldo Cruz), IRR (Instituto René Rachou), PUC Goiás (Pontifícia Universidade Católica de Goiás), UCDB (Universidade Católica Dom Bosco), UEL (Universidade Estadual de Londrina), UENF (Universidade Estadual do Norte Fluminense), UESC (Universidade Estadual De Santa Cruz), UFBA (Universidade Federal da Bahia), UFCE (Universidade Federal do Ceará), UFCG (Universidade Federal de Campina Grande), UFERSA (Universidade Federal Rural do Semi-Árido), UFF (Universidade Federal Fluminense), UFMG (Universidade Federal de Minas Gerais), UFMS (Universidade Federal do Mato Grosso do Sul), UFOP (Universidade Federal de Ouro Preto), UFPA (Universidade Federal do Pará), UFPE (Universidade Federal de Pernambuco), UFPEL (Universidade Federal de Pelotas), UFPR (Universidade Federal do Paraná), UFRA (Universidade Federal Rural da Amazônia), UFRGS (Universidade Federal do Rio Grande do Sul), UFRJ (Universidade Federal do Rio de Janeiro), UFRPE (Universidade Federal Rural de Pernambuco), UFRRJ (Universidade Federal Rural do Rio de Janeiro), UFSCAR (Universidade Federal de São Carlos), UFU (Universidade Federal de Uberlândia), UFV (Universidade Federal de Viçosa), UNB (Universidade de Brasília), UNESP (Universidade Estadual Paulista), UNICAMP (Universidade Estadual de Campinas), UNIRP (Centro Universitário de Rio Preto), UNIVASF (Universidade Federal do Vale do São Francisco), and USP (Universidade de São Paulo). *RTI (Royal Tropical Institute) and USDA (United States Department of Agriculture) in dark blue, they are Netherland and American institutions, respectively.
Methods that were positive in studies of zoonoses in marsupials in Brazil (see Supplementary material for details).
| Etiological agents | Culture | Serology | PCR | Microscopy |
|---|---|---|---|---|
| Anaplasma | – | – | 2 | – |
| Bartonella | – | – | 1 | – |
| Borrelia | – | 1 | – | 1 |
| Brucella | – | 1 | – | – |
| Ehrlichia | – | – | 4 | – |
| Leptospira | 2 | 15 | 5 | – |
| Mycoplasma | – | – | 3 | – |
| Rickettsia | – | 12 | – | – |
| Salmonella | 1 | – | – | – |
| Yersinia | 3 | 2 | – | – |
| Helminths | – | – | 1 | 54 |
| Cryptosporidium | – | – | – | 1 |
| Eimeria | – | – | – | 9 |
| Leishmania | 3 | 8 | 21 | – |
| Neospora | – | 2 | 1 | – |
| Sarcocystis | 3 | – | 4 | – |
| Toxoplasma | – | 33 | 2 | – |
| Trypanosoma | 45 | 42 | 16 | 4 |
| Alphavirus | – | 1 | – | – |
| Bunyavirus | – | 1 | – | – |
| Flavivirus | – | 3 | – | – |
| Hantavirus | – | – | 1 | – |
| Hepatovirus | – | 3 | 1 | – |
| Lyssavirus | – | 7 | – | – |
| Morbillivirus | 1 | 1 | 1 | – |
| Orthobunyavírus | – | 1 | – | – |
| Orthopoxvirus | – | 1 | 5 | – |
| Rotavirus | – | 1 | – | – |
| Sigmatorquevirus Alphatorquevirus | – | – | 1 | – |
3.1 Infections caused by bacteria
Infections with Leptospira Noguchi, 1917, and Salmonella Lignieres, 1900 were found in the genera Caluromys Allen, 1900, Didelphis Linnaeus, 1758, Marmosa Gray, 1821, and Marmosops Matschie, 1916 (Casagrande et al. 2011; Da Silva et al. 2013; Fernandes et al. 2020; Fornazari et al. 2018; Horta et al. 2016; Jorge 2009; Mesquita et al. 2018; Rocha et al. 2020). As for bacteria of the genus Borrelia Swellengrebel, 1907, cases were confirmed in D. aurita Wied-Neuwied, 1826 in the Southeastern region (Abel et al. 2000; Montandon et al. 2014). Eight species of marsupials, including three species of the genus Didelphis, were found infected by Rickettsia spp. from states of the Northern and Southeastern Brazil (Barbieri 2016; Milagres et al. 2010; Silveira et al. 2015; Szabó et al. 2013; Terassini 2010; Ueno et al. 2020). The other Rickettsia spp infected marsupials were: two species of the genus Gracilinanus Gardner & Creighton, 1989, from Northern, Northeastern, and Southeastern (Coelho et al. 2016; Paiva et al. 2017; Terassini 2010), two species of the genus Monodelphis Burnett, 1830 from Northeastern and Southeastern (Paiva et al. 2017; Szabó et al. 2013), and an unidentified species of the genus Marmosa from Northern region of Brazil (Terassini 2010).
Brucella Meyer and Shaw, 1920 and Bartonella Strong et al., 1915 infections were found in D. albiventris Lund, 1840 from São Paulo state (Antunes et al. 2010), while Bartonella only was found in D. albiventris and D. aurita from Rio de Janeiro state (Alcantara et al. 2020), both Southeastern Brazil. Individuals of Monodelphis domestica and D. albiventris were found infected with Yersinia sp. in Northeastern Brazil (Almeida et al. 1987, 1989). The bacteria Mycoplasma Nowak, 1929 was found in individuals of D. albiventris from Southern and Central Brazil (Gonçalves et al. 2020; Massini et al. 2019; Pontarolo et al. 2021). Two species of marsupials, Gracilinanus agilis (Burmeister, 1854) and Thylamys macrurus (Olfers, 1818), were positive for infection by Anaplasma Theiler, 1910, both from Central Brazil (De Sousa et al. 2017b). Ehrlichia Moshkovski, 1945, was found in four species, being D. aurita from Southeastern region, and G. agilis, M. domestica (Wagner, 1842), and T. macrurus from Central Brazil (De Sousa et al. 2017b; Guimarães et al. 2018).
3.2 Infections caused by virus
The genus Flavivirus, which includes species that can cause various diseases including the dengue, was found in individuals of D. albiventris from Southeastern region (Ázara 2013), and of D. marsupialis Linnaeus, 1758 and P. opossum (Linnaeus, 1758) from Northern Brazil (Bernal et al. 2021). The genus Lyssavirus, which can cause rabies, were confirmed for D. aurita, D. albiventris, and Lutreolina crassicaudata (Desmarest, 1804), all in Southeastern Brazil (Almeida et al. 2001; Araujo et al. 2014; Bacchiega 2014).
In the Didelphis the following viruses were also found: Alphavirus, Orthobunyavirus, Morbillivirus, Sigmatorquevirus, Alphatorquevirus, Parvovirus, Hepatovirus, Rotavirus, and Orthopoxvirus, the latter being also found in Caluromys philander (Linnaeus, 1758) (Almeida et al. 2001; Bernal et al. 2021; Carneiro 2018; De Souza et al. 2018a,b; Lavorente et al. 2021; Linhares et al. 1986; Miranda et al. 2017; Peres et al. 2016, 2018; Soares et al. 1987). Individuals of P. opossum were positive for Bunyavirus infection in Northern Brazil (Bernal et al. 2021). Hantavirus was registered in D. aurita, Marmosa (Micoureus) paraguayana (Tate, 1931), and Monodelphis iheringi (Thomas, 1888), all records from Southeastern Brazil (De Araujo et al. 2012).
3.3 Infections caused by helminths
Helminths parasitizing didelphid marsupials in isolated points of all regions of Brazil, with large areas without studies. The following genres were registered: Ancylostoma Dubini, 1843, Aspidodera Railliet and Henry, 1912, Brachylaema Dujardin, 1843, Capillaria Zeder, 1800, Centrorhynchus Lühe, 1911, Cruzia Travassos, 1917, Didelphodiplostomum Dubois, 1944, Didelphonema Wolfgang, 1953, Didelphostrongylus Prestwood, 1976, Dirofilaria Railliet and Henry, 1911, Echinostoma Rudolphi, 1809, Gnathostoma Owen, 1837, Gongylonemoides Freitas and Lent, 1937, Gracilioxyuris Feijó, Tores, Maldonado Jr. and Lanfredi, 2008, Hamanniella Travassos, 1915, Mathevotaenia Akhumyan, 1946, Oligacanthorhynchus Travassos, 1915, Physaloptera mirandai Lent and Freitas, 1937, Plagiorchis Lühe, 1899, Pterygodermatites Quentin, 1969, Rhopalias Stiles and Hassall, 1898, Spirura Blanchard, 1849, Strongyloides Grassi, 1879, Travassostrongylus Orloff, 1933, Trichuris Roederer, 1761, Toxocara Stiles, 1905, Turgida Schulz, 1927, and Viannaia Travassos, 1914, occurring in D. albiventris, D. aurita, Gracilinanus microtarsus (Wagner, 1842), G. agilis, L. crassicaudata, M. m. paraguayana, Metachirus myosuros (Temminck, 1824), Philander frenatus (Olfers, 1818), and P. opossum (Antunes 2005; Araujo 2011; Bernal et al. 2015; Boullosa et al. 2017; Cardia et al. 2016; Cirino et al. 2020; Feijó et al. 2008; Gomes et al. 2003; Santos-Rondon et al. 2002; Silva et al. 2017; Torres et al. 2007). Although not all helminths presented here have been found to infect humans, we consider them to have zoonotic potentials (Antunes 2005).
3.4 Infections caused by protozoa
The genus Leishmania Ross, 1903, responsible for leishmaniasis, was confirmed in the genera Didelphis, Gracilinanus, Marmosa, Marmosops, and Monodelphis, with most occurrences in the species D. albiventris (Arias et al. 1981; Brandão-Filho et al. 2003; Cardoso et al. 2015; Carreira et al. 2012; De Alcântara 2006; Lainson and Shaw 1969; Lima et al. 2013; Monteiro 2010; Nascimento 2017; Neto 2006; Quaresma et al. 2011; Quintal 2010; Richini-Pereira et al. 2014; Schallig et al. 2007; Sherlock 1996; Sherlock et al. 1984; Silva et al. 2016; Trueb et al. 2018; Yoshida et al. 1985). The protozoan Trypanosoma Gruby, 1843 was found in Caluromys, Didelphis, Gracilinanus, Lutreolina, Marmosa, Marmosops, Metachirus Burmeister, 1854, Monodelphis, Philander Brisson, 1762, and Thylamys Gray, 1843, being confirmed in all regions of Brazil (Alencar et al. 1977; Barreto and Siqueira 1962; Barros et al. 2020; Bernal et al. 2015; Cominetti 2010; Corrêa and Barreto 1964; Da Costa et al. 2015; Dario et al. 2017; De Oliveira 2008; Fernandes et al. 1989; Ferreira 2015; Guimarães and Jansen 1943; Herrera et al. 2005, 2007, 2011; Lainson et al. 2008; Liaño 2013; Lima et al. 2012; Maldonado 2014; Mello 1982; Miles et al. 1983; Nantes et al. 2019; Pereira et al. 2021; Pinho et al. 2000; Portugal 2009; Rocha et al. 2013; Rodrigues and Melo 1942; Roque et al. 2008; Trueb et al. 2018).
For the species Toxoplasma gondii (Nicolle and Manceaux, 1908), the following genera were reported as hosts: Didelphis, Gracilinanus, Marmosa, Marmosops, and Monodelphis, with the most occurrences in the Northeastern Brazil (Brito Junior et al. 2020; De Oliveira 2011; De Siqueira 2010; Ferraroni and Marzochi 1980; Fornazari et al. 2011; Fournier 2013; Horta et al. 2016; Vitaliano et al. 2014; Yai et al. 2003). The genera Cryptosporidium Tyzzer, 1907 and Sarcocystis Lankester, 1882, and the species Neospora caninum Dubey, Carpenter, Speer, Topper and Uggla, 1988 were found only in Didelphis spp. from Southeastern and Northeastern Brazil (Cesar 2011; Da Silva 2016; Dubey et al. 2001a,b; Gallo et al. 2018; Gondim et al. 2017, 2019; Horta et al. 2016; Yai et al. 2003). The protozoan Eimeria Schneider, 1875 was reported infecting Gracilinanus agilis (Strona 2016) in Southeastern, and the genera Didelphis, Gracilinanus, Marmosa, and Monodelphis in Northeastern region (Fehlberg et al. 2018).
4 Discussion
The growth in environmental degradation caused mainly by human occupation and lack of basic sanitation, could be responsible for a higher incidence of zoonoses, due to the increase contact among people and wild animals (Neto et al. 2007); particularly worry is in relation to the mammalian species, as they share several pathogens with the humans (Mills 2006). Although several studies on zoonotic agents have been carried out with different mammalian taxonomic orders in South America (Capellão et al. 2015; Corrêa et al. 2013; Moratelli and Calisher 2015; Povill et al. 2018), the data are still qualitative and geographically underestimated. As well as the present study, previous authors (Capellão et al. 2015; Corrêa et al. 2013; Moratelli and Calisher 2015) found large geographic gaps regarding the analyzed specimens, especially in the Northern, Central and Southern of Brazil.
Of the 66 species of Didelphidae occurring in Brazil, 24 of them showed positive results for the infection of zoonotic agents, with great emphasis on the species of the genus Didelphis, mainly D. albiventris and D. aurita, known for being very well adapted to urban environments (Da Cruz and Margarido 2003; Graipel and Santos-Filho 2006). The low amount of infections found in other species could be due to the scarcity of studies to detect potential pathogens by using these species as model, but also the fact that most studies was carried out by research institutions located in the Southeastern Brazil (e.g., Instituto Oswaldo Cruz/Fiocruz, Universidade de São Paulo, and Universidade Estadual Paulista), and studying species occurring in the same region. Another highlight is the great representativeness of dissertations and theses among the surveyed studies. It corroborates the role of graduate programs in building a more accurate portrait of the Brazilian reality, by contributing to better knowledge on the studied subject and, consequently, in the improvement both mitigation measures and prevention strategies (Severino 2006).
Regarding infections by bacteria and helminths, most were concentrated in the Southeastern Brazil, with few isolated points in the Northern and Northeastern due mainly to the incidence of outbreaks, such as the bubonic plague in Paraíba state during 1980s (De Almeida 1989). Marsupials showed a greater diversity of pathogenic bacteria compared to other groups of mammals, such as bats and armadillos, highlighting the incidence of bacteria of the genus Leptospira (Capellão et al. 2015; Corrêa et al. 2013). The genus Didelphis contains most positive cases for viruses in Brazil, probably due they are larger species compared to the other didelphids and have wide distribution (Gardner 2008), being easily found in urban and rural areas (i.e., mainly the species D. aurita – Boullosa et al. 2017, and D. albiventris – Almeida et al. 2008, pers. obs.), which could facilitate the collection samplings for histopathological, serological, and PCR analysis. As the agents can express different infectious load or pathology, different techniques have dissimilar detection capabilities (Lainson and Shaw 2010). Almost all tested Didelphis individuals were positives for the presence of Lyssavirus, which is transmitted through the bite of infected animals (Murphy and Bauer 1974). The incidence of these viruses is usually higher in bats, especially in Southeastern Brazil, where also most studies are concentrated (Moratelli and Calisher 2015).
Most infections in marsupials have been caused by protozoa, with a large number of cases for the Northern and Northeastern regions. This may be facilitated due to the characteristic of transmissions, which occur mainly through arthropods, having been favored with the historical deforestation observed in these regions (Norris 2004). In Brazil, several areas are endemic for some protozoa diseases (Lopes and Chapadeiro 1983; Queiroz et al. 2004; Silveira et al. 1996). The South American marsupials are considered the oldest hosts of the protozoan Trypanosoma cruzi (Stevens et al. 1998) which lodges in the anal glands of the hosts, being asymptomatic (Urdaneta-Morales and Nironi 1996). Similar factors are verified in relation to Leishmania, with a high incidence of infection in marsupials in Brazil and other American countries, mainly in areas with anthropic impact (Carreira et al. 2012). The ancient history of the relationship of didelphid marsupials with these protozoa may be the reason for the high number of positive results, when compared with the other groups of etiological agents. In any case, it is evident the need to monitoring both hosts and the quality of their habitats. Natural environments have been systematically devastated in the last two centuries, leading to a drastic increase in the contact of wild animals with domesticated animals and humans (Burkett-Cadena and Vittor 2018; Wolfe et al. 2005), which could greatly contribute to the spilling over of several zoonoses, such as the one caused by the Coronavirus SARS-CoV 2 (Rothan and Byrareddy 2020).
5 Concluding remarks
Preliminary studies on the impact of zoonotic agents may prevent outbreaks and new pandemics from appearing (Baharoon and Memish 2019; WHO 2021). The present study shows the need of monitor hosts and vectors, mainly in endemic areas for zoonoses. Long-term studies in parasitology and population/community ecology of hosts, using different techniques for diagnosis of infections and the host species identification, including the voucher preservation by depositing it in scientific collections, should be considered priorities (Thompson et al. 2021). We highlighted the importance of marsupials as being one of the main reservoirs of zoonotic agents, with infections by bacteria, viruses, protozoa, and helminths. Public research institutions, especially those linked to graduate programs, are of unequal importance in providing, through their researches, measures for the eradication of the diseases, as well as to guarantee quality responses for other biodiversity science areas (Overbeck et al. 2018). The maintenance of these institutions is extremely important for Brazilian science, requiring a continuous increase in science funds (Bolânos-Villegas et al. 2020). Paradoxically, Brazilian science has suffered in the last years severe cut off budgets, with a consequent loss of ongoing research and graduate student dropout (Martelli-Júnior et al. 2019; Oliveira et al. 2020), and threats to the biodiversity heritage (Fernandes et al. 2017).
Funding source: Conselho Nacional de Desenvolvimento Científico e Tecnológicoico
Award Identifier / Grant number: DCR 300461/2016-0
Award Identifier / Grant number: graduate scholarship 130627/2020-8
Funding source: Fundação Amazônia de Amparo a Estudos e Pesquisas
Award Identifier / Grant number: ICAAF 018/2016
Funding source: Programa de Capacitação Institucional (2018-2023), MPEG/CNPq
Award Identifier / Grant number: 302015/2021-3
Acknowledgments
Thanks are due to José de Sousa e Silva Júnior “Cazuza” for providing the space and use of equipment in the Mammalogy section of the Museu Paraense Emílio Goeldi; Comments of Gleomar Maschio and two anonymous reviewers improved the manuscript. The authors also thank André F. Mendonça, Flávio H. G. Rodrigues, and Paola da Mata for allowing them to use their pictures.
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Author contributions: MMB and AMRB designed the study, performed the analysis and interpretation of these data: MMB wrote the manuscript; AMRB critically reviewed the manuscript for intellectual content; MMB and AMRB are guarantors of the article. All authors read and approved the final manuscript.
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Research funding: This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (DCR 300461/2016-0 for AMRB), Fundação Amazônia de Amparo a Estudos e Pesquisas (ICAAF 018/2016 for ARMB), and by the Programa de Capacitação Institucional (2018-2023), MPEG/CNPq (302015/2021-3).
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Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
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Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/mammalia-2021-0134).
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Articles in the same Issue
- Frontmatter
- Ecology
- Infection agents of Didelphidae (Didelphimorphia) of Brazil: an underestimated matter in zoonoses research
- Habitat type impacts small mammal diversity in the Ukaguru Mountains, Tanzania
- Roosting ecology of insectivorous bats in a tropical agricultural landscape
- Bats in wetlands: composition and structure of assemblage in Reserva Natural Don Luis, Esteros del Iberá, Argentina
- Bats can reach 3626 m a.s.l. in Papua New Guinea: altitudinal range extensions for six rainforest bat species
- Original record of deposited skins of hedgehogs (Erinaceidae) at red fox den
- Conservation
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- Growth, weights, and measurements of female wild sheep from Iran
- Ethology
- How fishing cats Prionailurus viverrinus Bennett, 1833 fish: describing a felid’s strategy to hunt aquatic prey
- Biogeography
- New altitudinal records of Panthera onca (Carnivora: Felidae) in the Andean region of Ecuador
- Taxonomy/Phylogeny
- Taxonomic status and phylogenetic position of Oxymycterus juliacae Allen 1900 (Rodentia: Cricetidae)
