Therya_notes_NE9

THERYA NOTES 2024, Vol. 5 : 150-156 DOI: 10.12933/therya_notes-24-163 ISSN 2954-3614

The family Didelphidae as a host of zoonotic pathogens

La familia Didelphidae como hospedero de patógenos zoonóticos

Víctor Sánchez-Cordero1, Ángel Rodríguez-Moreno1, José Juan Flores-Martínez 1, and Gabriel Gutiérrez-Granados2*

1Laboratorio de Sistemas de Información Geográfica, Instituto de Biología, Universidad Nacional Autónoma de México. Circuito Zona Deportiva s/n, C. P. 04510, Coyoacán. Ciudad de México, México. E-mail: victor@ib.unam.mx (V-SC); tanicandil@hotmail.com (A-RM); jj@ib.unam.mx (JJF-M).

2Unidad Multidisciplinaria de Investigación Experimental Zaragoza, Facultad de Estudios Superiores Zaragoza, Universidad Nacional Autónoma de México. Batalla 5 de mayo s/n, C. P. 09230, Iztapalapa. Ciudad de México, México. E-mail: gabriel.gutierrez@zaragoza.unam.mx (GG-G).

*Corresponding author

The family Didelphidae has often been associated with transmission cycles of zoonotic diseases, such as Leishmaniasis and Chagas disease. In this work, we review the scientific literature published from 1994 to 2024 on studies of the family Didelphidae and its pathogens. Of the 5 terrestrial genera of the family Didelphidae analyzed, 86 % reported Didelphis as a host of various pathogens. In this genus, a larger number of pathogen groups have been reported, including bacteria, viruses, nematodes, fungi, and helminths, as well as protozoa that cause Chagas and Leishmaniasis diseases. Didelphis albiventris and D. virginiana are the species with the highest number of pathogen species documented to date (12 and 9, respectively). This information highlights the importance of understanding the role of the family Didelphidae in zoonotic cycles, considering that several species of the family have adapted to anthropized environments.

Key words: Didelphis; marsupials; opossums; synanthropic; zoonoses.

La familia Didelphidae ha sido frecuentemente asociada a ciclos de transmisión de enfermedades zoonóticas, por ejemplo, Leishmaniasis y Chagas. En este trabajo se realizó una revisión de la literatura científica publicada de 1994 a 2024 sobre estudios realizados en la familia Didelphidae y sus patógenos. Los resultados mostraron que, de los 5 géneros terrestres analizados de la familia Didelphidae, el 86 % reportaron a Didelphis como hospedero de diversos patógenos. En este género se han reportado mayor número de grupos, incluyendo la presencia de bacterias, virus, nematodos, hongos y helmintos, además de los protozoarios que provocan las enfermedades de Chagas y Leishmaniasis. Didelphis albiventris y D. virginiana son las especies en las que más patógenos se han documentado hasta el momento (12 y 9, respectivamente). Esta información destaca la importancia de comprender el papel de la familia Didelphidae en los ciclos zoonóticos, considerando que varias especies de la familia se han adaptado a los ambientes antropizados.

Palabras clave: Didelphis; marsupiales; sinantrópico; zarigüeyas; zoonosis.

Zoonotic diseases (ZDs) are caused by pathogens such as viruses, bacteria, protozoa, helminths, or fungi found initially in wild species and that reach human populations through their interaction with them (Plowright et al. 2017; Ellwanger and Chies 2021). Increased exposure to these pathogens is driven by climate change, pollution, land-use changes, and human incursions into wild systems during food gathering, hunting, or logging (Rahman et al. 2020; Morand and Lajaunie 2021; Choo et al. 2023; Tumelty et al. 2023).

The family Didelphidae comprises about 95 species of marsupials distributed in the Americas (Gardner 2019) and is recognized for including species that host various zoonotic parasites (Jansen et al. 2010; Bezerra-Santos et al. 2021; Bitencourt and Bezerra 2022). This is relevant because zoonotic diseases are expanding their distribution range (Kilpatrick and Randolph 2012; Han et al. 2016), and several didelphid species can establish populations in rural, semi-urban, and urban areas (Costa-Neto et al. 2019; Simioni et al. 2022). This makes didelphids one of the main hosts in the life cycles of pathogens that cause zoonotic diseases (Ávila-Jiménez et al. 2024).

The genus Didelphis has attracted considerable interest in the scientific community because pathogens that affect human populations have been documented in this genus; for example, the protozoan Trypanosoma cruzi, which transmits Chagas disease (Robertson 1929). This work aims to review the scientific literature on the family Didelphidae as a host of pathogens that cause zoonotic diseases.

A literature review was carried out using the Scopus and Web of Science search engines. The search included articles published in the past 30 years (1994–2024) because molecular techniques have improved since the 1990s, making it possible to document the presence of pathogens in mammals accurately. Although protozoa have been documented in the Didelphidae family since the early 20th century, such as Trypanosoma or Leishmania, defining 1994 as the lower limit of the search does not exclude the documentation of these or other parasites that were already diagnosed previously through direct observation in blood or using immunological tests. The search included the following words: zoonotic, disease, emerging (and their equivalent words in Spanish) with 5 of the main terrestrial genera of the family Didelphidae: Didelphis, Caluromys, Philander, Chironectes, Lutreolina, and the arboreal genus Marmosa. These genera were selected because they have been documented to include synanthropic species. From each study found, the locality where the work was conducted was extracted to determine the region where most of the research is being performed on the subject. The results were captured on a map of the Americas in QGIS version 3.22 (QGIS 2021). In addition, a cloud of words that appeared most frequently in the studies was constructed. This analysis was limited to the 50 most frequent words to make this representation as concise as possible. The analyses were carried out in RStudio (R Core Team 2022), with the support of the bibliometrix library (Aria and Cuccurullo 2017) and wordcloud2 (Lang and Chien 2018).

The literature search showed that 73 studies have been carried out on pathogens in the family Didelphidae between 1994 and 2024 (Table 1). The countries where most research has been carried out are Brazil (43 % of studies), the USA (30 %), and México (11 %), while Panamá and Venezuela are the countries with the lowest scientific production, with 3 and 2 studies, respectively (Figure 1). In general, there is an increasing trend in the number of publications per year, with 2020, 2022, and 2023 standing out as the years with the highest production (Figure 2a). In México, the Universidad Autónoma de Yucatán is the academic institution with the highest number of publications on the subject (Figure 2b).

According to the cloud, the words most frequently reported are Trypanosoma cruzi, zoonosis, opossum, Chagas disease, and Didelphis virginiana (Figure 3). A reference to public health also appears in this word cloud, although less frequently. In total, 27 pathogens carried by the family Didelphidae have been documented. Of these, 33 % correspond to helminths, 33.3 % to bacteria, 18 % to protozoa, 7.4 % to ectoparasites, 3.7 % to fungi, and 3.7 % to viruses (Table 1). Ninety-six percent of pathogens have been identified at the species level and 4 % at the genus level. Pathogens have been documented in Didelphis albiventris, D. aurita, D. marsupialis, D. virginiana, Marmosa mexicana, Monodelphis domestica, Lutreolina crassicaudata, Philander frenatus, and P. oposum. Of all the species with pathogen records, D. albiventris and D. virginiana have the highest number of pathogen species recorded (12 and 9 species, respectively), while only 1 pathogen species has been recorded in M. mexicana, M. domestica, L. crassicaudata, P. frenatus, and P. oposum (Table 1). Didelphis albiventris and D. virginiana are also the species with the highest diversity of pathogen groups, including nematodes, protozoa, bacteria, helminths, and fungi (Table 1).

Didelphids have been studied historically as potential hosts of zoonotic agents (Bezerra-Santos et al. 2021). The countries with the highest scientific production on the subject in the past 30 years are Brazil, the United States, and México, while scientific production for Central American countries such as Nicaragua, Belize, and Honduras were not documented in the search carried out. This may be due to the difficulties in obtaining funds for research in the latter countries (Ríos and Herrero 2005). However, these findings could be biased since the search used only 2 search engines. Future studies should contemplate identifying the regions with the highest and lowest scientific production using other massive search engines, such as Google Scholar, during the documentation phase.

On the other hand, Didelphidae is one of the most abundant mammal families in the Americas, with a distribution that ranges from South America to the United States (Ceballos 2014). This wide distribution contributes to a greater dispersal of zoonotic diseases (Bezerra-Santos et al. 2021; Choo et al. 2023). In the family, Didelphis is the genus in which the relationship with its pathogens has been studied most intensely (Table 1). This highlights some information gaps regarding other genera of didelphids genera with a broad distribution, such as Philander. The genus Didelphis has been recognized as an important host group of protozoa, bacteria, viruses, and helminths (Bezzerra-Santos et al. 2021). Its role as host is particularly relevant as it is synanthropic and constantly interacts with domestic animals and human populations (Guzman-Marin et al. 2016; Guimarães et al. 2022; Rojas-Sánchez et al. 2023). This underlines the importance of implementing a detailed management program in anthropized environments to avoid threatening their populations while reducing their potential impact on public health, given their role as hosts of zoonotic pathogens (Zepeda-Espinosa et al. 2019; Cáceres et al. 2020). The genus Didelphis is a host of the etiological agents of Chagas disease and Leishmaniasis, classified as diseases of poverty frequently associated with areas lacking urban infrastructure (Ghorbani and Farhoudi 2017). Likewise, permanent efforts are being made to contain intestinal diseases caused by helminths, as they can cause anemia and death, mainly in children, in several regions of the Americas (Lustigman et al. 2012). It is worth highlighting that zoonoses have impacts not only at the health level but also in the socioeconomic context and human development in general (Narrod et al. 2012).

Although the conservation status of most species in the Didelphidae family is Least Concern according to the International Union for Conservation of Nature (IUCN 2024), further research is needed to better understand the ecological dynamics of this group and its pathogens, particularly its association with the human population (de Oliveira-Carneiro et al. 2019; Bezerra-Santos et al. 2021; Ávila-Jiménez et al. 2024). Additionally, screening tests should be performed on rescued or relocated animals to start monitoring this family in cities and clarify its importance in the transmission cycles of zoonotic diseases.

Acknowledgements

The authors wish to thank the anonymous reviewers for their comments on an early version of this document, which helped substantially improve it. M. E. Sánchez-Salazar translated the manuscript into English.

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Associated editor: Itandehui Hernández Aguilar.

Submitted: March 6, 2024; Reviewed: May 18, 2024.

Accepted: June 10, 2024; Published on line: June 19, 2024.

Table 1. Pathogens documented in species of the family Didelphidae.

Species	Pathogen agent	Taxonomic group	References
Didelphis albiventris	Angiostrongylus cantonensis	Nematode	Vielmo et al. (2022)
	Babesia sp.	Protozoon	Perles et al. (2023)
	Ctenocephalides felis	Siphonapter	Lignon et al. (2023)
	Ehrlichia canis	Bacterium	Bertão-Santos et al. (2023)
	Helminths	Helminth	Vielmo et al. (2022)
	Helicobacter sp.	Bacterium	Cardia-Caserta et al. (2023)
	Leishmania sp.	Protozoon	Lima et al. (2013); Cutolo et al. (2014); Ratzlaff et al. (2023)
	Leptospira borgpetersenii	Bacterium	Jorge et al. (2012)
	Paracoccidioides brasiliensis	Fungus	Richini-Pereira et al. (2008)
	Toxoplasma gondii	Protozoon	Richini-Pereira et al. (2016)
	Trichinella spiralis	Nematode	Castaño-Zubieta et al. (2014)
	Trypanosoma cruzi	Protozoon	Tenório et al. (2014); Zitelli et al. (2021)
Didelphis aurita	Hepatovirus A	Virus	Carneiro et al. (2018)
	Leishmania sp.	Protozoon	Ratzlaff et al. (2023)
	Nematodes and trematodes	Nematode, Platyhelminth	Teodoro et al. (2019)
	Intestinal parasites	Platyhelminth, Nematode	Teodoro et al. (2019); Bezerra-Santos et al. (2020a); Bezerra-Santos et al. (2020c); Alonso et al. (2024)
	Trichinella sp.	Nematode	Jurkevicz et al. (2022)
Didelphis marsupialis	Anaplasma phagocytophilum	Bacterium	Rojero-Vázquez et al. (2017)
	Babesia sp.	Protozoon	Calchi et al. (2023)
	Bartonella sp.	Bacterium	Calchi et al. (2023); Rojas-Jaimes and Valle-Mendoza (2023)
	Borrelia puertoricensis	Bacterium	López et al. (2023)
	Leishmania sp.	Protozoon	Schallig et al. (2007); Ávila-Jiménez et al. (2024)
	Leptospira sp.	Bacterium	Haro et al. (2021)
	Toxoplasma gondii	Protozoon	Bezerra-Santos et al. (2020b)
	Trypanosoma cruzi	Protozoon	Travi et al. (1994); Ramírez et al. (2013); Roque et al. (2013); Cantillo-Barraza et al. (2015); de Buhr et al. (2018); Bilheiro et al. (2022); Pineda et al. (2022); Tineo-González et al. (2023)
Didelphis virginiana	Anaplasma phagocytophilum	Bacterium	Rojero-Vázquez et al. (2017)
	Ectoparasites	Siphonapters, Mites	Castellaw et al. (2011); Canto-Osorio (2020); Glebskiy et al. (2022); Ferreira et al. (2023)
	Leptospira sp.	Bacterium	Richardson and Gauthier (2003); Grimm et al. (2020); Helman et al. (2023)
	Rickettsia sp.	Bacterium	Dzul-Rosado et al. (2021); Blanton et al. (2022)
	Salmonella enterica	Bacterium	Ruiz-Piña et al. (2002); Haro et al. (2021)
	Toxoplasma gondii	Protozoon	Suzán and Ceballos (2005); Houk et al. (2010); Horta et al. (2016); Torres-Castro et al. (2016)
	Trypanosoma cruzi	Protozoon	Hodo and Hamer (2017); Vandermark et al. (2018); Kramm et al. (2019); Zecca et al. (2020)
	Intestinal parasites	Platyhelminths, Nematodes	Aragón-Pech et al. (2018); Ruiz-Piña et al. (2002)
	Paragonimus mexicanus	Platyhelminth	García-Márquez et al. (2010)
Marmosa mexicana	Trypanosoma cruzi	Protozoon	Haro et al. (2021)
Monodelphis domestica	Babesia sp.	Bacterium	Calchi et al. (2023)
Lutreolina crassicaudata	Strongyloides sp.	Nematode	Cardia et al. (2016)
	Toxoplasma gondii	Protozoon	Richini-Pereira et al. (2016)
Philander frenatus	Toxoplasma gondii	Protozoon	Zitelli et al. (2021)
Philander opossum	Trypanosoma cruzi	Protozoon	Roque et al. (2013); Haro et al. (2021)