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Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology logoLink to Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology
. 2020 Mar 2;44(2):355–363. doi: 10.1007/s12639-020-01205-9

Gastrointestinal parasites in the opossum Didelphis aurita: Are they a potential threat to human health?

Marcos Antônio Bezerra-Santos 1,, Carolina Silveira Fontes 1, Bárbara Cristina Félix Nogueira 1, Ricardo Seiti Yamatogi 1, Rafael Antonio Nascimento Ramos 2, Juliana Arena Galhardo 3, Luis Fernando Viana Furtado 4, Élida Mara Leite Rabelo 4, Jackson Victor de Araújo 1, Artur Kanadani Campos 1
PMCID: PMC7244705  PMID: 32508410

Abstract

Currently, a great proportion of the emerging infectious human diseases are zoonotic, with most of the pathogens originated from wildlife. In this sense, synanthropic animals such as marsupials play important role in the dissemination of pathogens due to their proximity to human dwellings. These hosts are affected by many gastrointestinal parasites, including species with zoonotic potential. The aim of this study was to assess the diversity of gastrointestinal parasites infecting the black-eared opossum D. aurita captured in urban areas of Southeastern, Brazil. In addition, the potential risk for the human population based on the One Health perspective has been discussed. Forty-nine marsupial specimens were captured with Tomahawk live traps and fecal samples were collected. The samples were evaluated by parasitological procedures. Eggs and oocysts were analyzed at different magnifications (400 × and 1000 ×), and their identification, together with adult nematodes, was established on morphological and morphometric data. Forty-three hosts (87.76%) scored positive for at least one gastrointestinal parasite, being 83.67% (41/49) for helminths, and 65.30% (32/49) for protozoa. For Cryptosporidium sp., only 13 samples were evaluated due to insufficient amount of feces obtained of some animals. A prevalence of 23.08% (3/13) was reported for this parasite. PCR analysis revealed Ancylostomatidae eggs to belong to the genus Ancylostoma. Our results demonstrated that multiparasitism is frequently found in these animals and a high percentage of potentially zoonotic parasites are observed, implying that D. aurita may be involved in zoonotic cycles in urban environments.

Keywords: Synanthropic animals, Nematodes, Trematodes, Protozoa, Zoonosis

Introduction

Currently, it is estimated that 60% of the emerging infectious human diseases are zoonotic, with more than 71% of those, originated from wild animals (Cutler et al. 2010). Over the time, several wildlife species have developed the synanthropic behavior, and animals (e.g., opossums, canids, birds) previously seen only in forest areas have been frequently observed in urban centers. The proximity among humans, domestic animals and synanthropic species has constantly increased, and the risk of transmission of zoonotic pathogens has been considered one of the most important issues debated on the One Health perspective (Thompson 2013; McFarlane et al. 2012; Pinto et al. 2006).

Amongst the synanthropic animals, the species Didelphis aurita Wied-Newied, 1826 (Didelphimorphia: Didelphidae) are marsupials well adapted to the anthropogenic activity. This species has semi arboreal behavior and occurs primarily in the Atlantic forest regions, being commonly found near human dwellings (Gardner 2008). The diet of this opossum is very diverse including fruits, insects and a great variety of small vertebrates. This opportunistic feeding behavior exposes these animals to a great number of gastrointestinal parasites, including those of zoonotic concern such as the genera Ancylostoma, Toxocara, Trichuris, Ascaris, Capillaria, Giardia and Cryptosporidium (Teodoro et al. 2019; Aragón-Pech et al. 2018; Pinto et al. 2014; Ceotto et al. 2009; Zanette et al. 2008).

Studies on gastrointestinal parasites in opossums are scarce, and information regarding host-parasite interactions between Didelphidae and their parasitic fauna are limited. The multiparasitism observed in these animals may affect their health, since the interactions among parasites are possibly linked to host susceptibility, duration of infection, risk of spreading, and clinical signs (Vaumourin et al. 2015). Thus, the description of those organisms in a given species is extremely important in order to get a better understanding of the relationship they have to each other, and with their hosts. Therefore, the aim of this study was to assess the diversity of gastrointestinal parasites infecting D. aurita captured in urban areas of Southeastern, Brazil. In addition, the potential risk for the human population based on the One Health perspective has been discussed.

Materials and methods

Study area

This study was performed in urban and periurban areas of the municipality of Viçosa (Latitude 20°45′14″South and Longitude 42°52′54″West), State of Minas Gerais, Brazil (Fig. 1). The area is featured by a Cwa climate, mesothermic, with hot and rainy summers and cold and dry winters. Annual average temperature varies from 20 °C to 22 °C and the region is 650 m above sea level, with an annual average rainfall of 1229 mm, and humidity of 77%.

Fig. 1.

Fig. 1

Points of capture of opossums positive for gastrointestinal parasites. The area where the black spots are concentrated is the urban extension of the municipality of Viçosa, Minas Gerais, Brazil

Animals and sampling

From January to June 2019, animals were captured through Tomahawk live traps (0.45 × 0.21 × 0.21 m), which were armed and checked daily (5PM and 7AM, respectively), totaling a sampling effort of 516 trap-nights. A mix of corn flour, canned fish and banana were used as bait. After capture, each individual was mechanically contained, classified by sex, age group (pups, subadults and adults), and marked with a small V cut at the right ear to identify recaptures (Morrant et al. 2010). Fresh fecal samples were collected from the trap or directly from the cloaca as soon as the animals defecated. After sampling procedures, each animal was released at the same site of capture.

Laboratorial procedures

Samples were individually evaluated by the simple flotation technique of Willis-Mollay (Willis 1921). On the other hand, the search for Cryptosporidium spp. oocysts was carried out by malachite green negative staining as previously described (Elliot et al. 1999). Positive samples for Eimeria spp. oocysts were placed in Petri dishes containing 2.5% Potassium dichromate (K2Cr2O7) and stored at 24 °C for seven days in order to allow sporulation (Duszynski and Wilber 1997). Eggs and oocysts were analyzed at different magnifications (400 × and 1000 ×) and measured with an Olympus CX31 microscope attached to a camera connected to the ToupView software version 3.7. The identification of eggs and oocysts was established on morphological and morphometric data previously described (Duszynski and Wilber 1997; Teixeira et al. 2007; Bowman 2010; Lainson and Shaw 1989). Adult nematodes recovered from feces of some animals were identified according to Adnet et al. (2009).

Molecular analysis was further performed for Ancylostomatidae. Individual eggs were isolated (Zuccherato et al. 2018) and genomic DNA was extracted according to Lake et al. (2009). Afterwards, DNA samples were screened by duplex PCR for Ancylostoma spp. and Necator americanus using primers that amplify a region of internal transcribed spacer 2 and the 28S ribosomal RNA (ITS2-28S rRNA). Forward primers AD1 (5′ CGA CTT TAG AAC GTT TCG GC 3′) and NA (5′ ATG TGC ACG TTA TTC ACT 3′), and the reverse primer NC2 (5′ TTA GTT TCT TTT CCT CCG CT 3′) were used for DNA amplification, resulting in 250 bp if positive for N. americanus, and in 130 bp if positive for Ancylostoma spp. (Sahimin et al. 2017). Reactions were performed using 0.2 µM of each primer, 1 U of Taq DNA polymerase (Phoneutria, Brasil), 200 µM of deoxynucleoside triphosphate (dNTPs), 1X reaction buffer, 5 µL of DNA sample, and ultrapure water to complete a 10 µL final volume. DNA of N. americanus and Ancylostoma spp. previously extracted from adult worms (Zuccherato et al. 2018; Furtado et al. 2014) were used as positive control, and nuclease free water as negative control. Electrophoresis in 1% agarose gel with 0.5 TAE buffer and GelRed ™ (Biotium, EUA) was performed to visualize the amplified products.

Data analysis

Descriptive statistics was performed to calculate the relative and absolute frequency of helminths and protozoa infections. The normality of data was checked using the Lilliefors test. Additionally, Chi square or Fisher exact test were used to analyze gastrointestinal parasite infections, as well as sex and ages of the infected animals using the R (Studio 2012) software. A 5% significance level was considered to all parameters tested (p < 0.05).

Opossums sites of capture were analyzed with the geographic information system program QGIS 3.4.12 (qgis.org). For the cartographic basis we used digital maps of Brazil, Minas Gerais and the city of Viçosa, and as ellipsoid of reference we used the SIRGAS2000 and the UTM coordinates system. The system extension on the fly was used to automatically convert the layers and points, and the satellite images (Google Satellite) were obtained with the complement QuickMapServices.

Results

Forty-nine animals (40 alive and 9 found dead) were captured during the whole study period in nine collection points. From those, 14 specimens (28.57%) were classified as adult female, 10 (20.40%) as adult male, 12 (24.49%) as subadult female, 12 (24.49%) as subadult male, and 1 (2.04%) as a pup. Of all samples analyzed, 87.76% (43/49) scored positive for at least one gastrointestinal parasite (Tables 1 and 2). Eggs of helminths were detected in 83.67% (41/49) of the samples (Fig. 2), whereas protozoa oocysts were observed in 65.30% (32/49) of the animals (Fig. 3). The Cryptosporidium search was performed only in 13 samples due to the insufficient amount of feces obtained from some animals. A frequency of 23.08% (3/13) was reported for this parasite. Additionally, adult nematodes (n = 53) recovered from feces were identified as Cruzia tentaculata (Fig. 4).

Table 1.

Absolute and relative frequencies for each gastrointestinal parasite found in Didelphis aurita

Parasite AF/N RF %
Ancylostoma spp. 32/49 65.30a
Ascaridoidea 10/49 20.41ab
Spiruroidea 2/49 4.08ab
Trematoda 8/49 16.33ab
Cruzia tentaculata 36/49 73.47b
Strongyloides spp. 7/49 14.29ab
Trichuris spp. 14/49 28.57ab
Capillaria spp. 6/49 12.24ab
Eimeria spp. 32/49 65.30ab
Isospora spp. 2/49 4.08ab
Cryptosporidium spp. 3/13* 23.08ab*

AF absolute frequency, RF relative frequency, N—number of animals evaluated

*Cryptosporidium spp. diagnosis was performed in 13 animals

abDifferent letters in the same collunm represent p < 0.05

Table 2.

Single and multiple infections by helminths and protozoa in Didelphis aurita

Parasites RF % AF/n
Ancylostoma spp. 2.33 1/43
Cruzia tentaculata 4.65 2/43
Eimeria spp. 4.65 2/43
Ancylostoma spp. +Ascaridoidea+Spiruroidea+ Eimeria spp. 2.33 1/43
C. tentaculata + Strongyloides spp.+ Trichuris spp.+ Ancylostoma spp.+Trematoda+ Eimeria spp. 4.65 2/43
C. tentaculata + Strongyloides spp.+ Capillaria spp.+ Ancylostoma spp.+Trematoda 2.33 1/43
C. tentaculata + Ancylostoma spp.+ Eimeria spp. 2.33 1/43
C. tentaculata + Trichuris spp.+ Ancylostoma spp.+Trematoda 2.33 1/43
C. tentaculata + Ancylostoma spp. 2.33 1/43
C. tentaculata + Trichuris spp.+ Ancylostoma spp.+ Eimeria spp. 2.33 1/43
C. tentaculata + Trichuris spp.+ Capillaria spp.+ Ancylostoma spp.+Ascaridoidea 2.33 1/43
C. tentaculata + Ancylostoma spp.+Ascaridoidea+ Eimeria spp. 2.33 1/43
C. tentaculata + Trichuris spp.+ Capillaria spp.+ Ancylostoma spp.+Ascaridoidea+ Eimeria spp. 2.33 1/43
C. tentaculata + Strongyloides spp.+ Ancylostoma spp.+ Eimeria spp. 2.33 1/43
C. tentaculata + Ancylostoma spp.+ Eimeria spp. 2.33 1/43
C. tentaculata +Ascaridoidea 2.33 1/43
C. tentaculata + Capillaria spp.+ Ancylostoma spp.+Ascaridoidea+ Eimeria spp. 2.33 1/43
C. tentaculata + Trichuris spp.+ Ancylostoma spp.+Ascaridoidea+ Eimeria spp. 2.33 1/43
C. tentaculata + Trichuris spp.+ Eimeria spp. 2.33 1/43
C. tentaculata + Ancylostoma spp. 2.33 1/43
C. tentaculata + Trichuris spp.+ Eimeria spp. 2.33 1/43
C. tentaculata + Ancylostoma spp.+ Eimeria spp. 2.33 1/43
C. tentaculata + Trichuris spp.+ Ancylostoma spp. 2.33 1/43
C. tentaculata + Ancylostoma spp.+Trematoda+ Eimeria spp. 4.65 2/43
C. tentaculata + Capillaria spp.+Trematoda+ Eimeria spp.+ Isospora spp. 2.33 1/43
C. tentaculata + Eimeria spp. 2.33 1/43
C. tentaculata + Ancylostoma spp.+ Eimeria spp. 11.63 5/43
C. tentaculata +Ascaridoidea+ Eimeria spp. 2.33 1/43
C. tentaculata + Strongyloides spp.+Ascaridoidea +Eimeria spp. 2.33 1/43
C. tentaculata + Ancylostoma spp.+Ascaridoidea+Spiruroidea+Trematoda+ Eimeria spp. 2.33 1/43
C. tentaculata + Ancylostoma spp. 2.33 1/43
C. tentaculata + Strongyloides spp.+ Trichuris spp.+ Ancylostoma spp.+ Eimeria spp. 2.33 1/43
Strongyloides spp.+ Trichuris spp.+ Ancylostoma spp.+ Eimeria spp.+ Isospora spp. 2.33 1/43
Trichuris spp.+ Capillaria spp.+ Ancylostoma spp.+ Eimeria spp. 2.33 1/43
Trichuris spp.+ Ancylostoma spp.+ Eimeria spp. 2.33 1/43
Total 100.0 43/43

RF relative frequency, AF absolute frequency, n—positivite samples

Fig. 2.

Fig. 2

Helminth eggs detected in fecal samples from Didelphis aurita. aCruzia tentaculata; bAncylostoma sp.; cStrongyloides sp.; d Spiruroidea; eTrichuris sp.; fCapillaria sp.; g Ascaridoidea; h Trematoda. Scale bar 25 µm

Fig. 3.

Fig. 3

Protozoa oocysts detected in fecal samples from Didelphis aurita. aEimeria auritanensis; bE. gambai; cE. philanderi; dE. caluromydis; eIsospora sp.; fCryptosporidium sp. Scale bar 10 µm

Fig. 4.

Fig. 4

Cruzia tentaculata adult male (a, b, c) and female (d, e, f) recovered from Didelphis aurita feces. a Anterior view of male showing buccal capsule, and esophagus; b Esophagus with bulb and intestinal diverticulum common in male and female; c Posterior region of male showing one pair of spicules, gubernaculum and caudal alae; d Anterior region of female showing buccal capsule and esophagus; e Mid region of female filled with eggs; f Posterior end of female showing anus and sharp caudal end. Scale bar 500 µm

In particular, PCR analysis of Ancylostomatidae eggs amplified a product of 130 bp, revealing Ancylostoma spp. in all analyzed samples. None of the parameters statistically checked presented significance, except for the parasitism by Ancylostoma spp. between male and female (p = 0.0233), and for the frequency between C. tentaculata and Ancylostoma spp. (p = 0.04211).

Discussion

This study reports a wide diversity of gastrointestinal parasites infecting D. aurita opossums from Southeastern Brazil. A very high frequency of helminths (83.67%) and protozoa (65.30%) was detected in the animals herein evaluated. This finding may be related to the omnivorous and opportunistic diet observed in Didelphis spp. (i.e. fruits, small vertebrates, invertebrates, seeds and rubbish remnants of human consumption), which may vary according to the environment (i.e. urban or forest fragments) where they are mostly inserted (Ceotto et al. 2009; Cáceres and Monteiro-Filho 2001). The great variety of gastrointestinal parasites herein observed, includes some species that may present zoonotic potential (Thamsborg et al. 2016; Mateus et al. 2014; Uehlinger et al. 2013; Youn 2009; Batchelor et al. 2008; Oryan et al. 2008; Lindsay et al. 1997). Furthermore, to our knowledge, the protozoa Cryptosporidium sp., Isospora sp., and the nematode Strongyloides sp. are new records for D. aurita.

The presence of potentially zoonotic nematodes in opossums of the genus Didelphis was previously reported in America (Teodoro et al. 2019; Aragón-Pech et al. 2018; Richardson and Campo 2005). In the present study, immature forms of Ancylostoma spp. were detected in 65.30% of D. aurita. Teodoro et al. (2019) recently identified eggs of the family Ancylostomatidae with a frequency of 41.07% and 100.0% in D. albiventris and D. aurita, respectively. Similarly, Aragón-Pech et al. (2018), evaluating gastrointestinal parasites in D. virginiana in Mexico, found 84.50% of the animals to be positive for Ancylostoma sp. These data suggest that Didelphis spp. opossums are commonly infected by parasites of this genus, which includes the species A. caninum, that causes a disease known as Cutaneous larva migrans in humans and is commonly detected in the feces of dogs (Feldmeier and Schuster 2012). Since the animals herein evaluated were all captured in urban sites where domestic animals, such as stray dogs are present, it is possible that opossums are involved in the cycle of A. caninum in urban environments; therefore, further studies on the molecular characterization of the Ancylostoma spp. infecting D. aurita should be performed, in order to identify whether the species that affect these animals are zoonotic or not.

Parasites of the family Trichuridae were frequently detected in the opossums herein evaluated. The genera Trichuris and Capilaria were previously reported in Didelphis spp. as Trichuris didelphis, T. marsupialis, T. minuta, Capilaria didelphis and C. longicauda (Costa-Neto et al. 2018; Noronha et al. 2002; Alden 1995). Both genera have representative species with zoonotic potential; however, it is not clear whether the species described in Didelphis spp. may infect humans. In our study, the specimens were classified as Trichuris sp. and Capillaria sp. according to morphological and morphometric analysis. The same was applied to Strongyloides sp. eggs, which in fresh fecal samples are characterized by the presence of a larva, an ellipsoid shape (40–85 μm in length), and a thin wall (Viney and Lok 2015).

Cruzia tentaculata was the most prevalent parasite detected in the animals. Similar results were observed in other studies performed in Brazil with the same opossum species, identifying frequencies of approximately 76.0% for this nematode (Teodoro et al. 2019; Costa-Neto et al. 2018). These findings suggest that C. tentaculata is the most prevalent gastrointestinal parasite in D. aurita opossums. However, information about the ecology of this species in marsupials are limited, and further studies are needed in order to determine their role regarding pathogenicity and effects on other populations of gastrointestinal parasites found in these animals. In the present study, male and female adult forms of the parasite were directly recovered from feces of four opossums. Since the transmission of Cruzia spp. is given by ingestion of eggs (Anderson 2000), it is not clear what the releasing of alive adult forms through feces means in the parasite life cycle.

Trematode eggs were found in eight animals in our study. Among the trematodes previously reported in Didelphis spp., Schistosoma mansoni found in D. albiventris (Kawazoe et al. 1978), and Brachylaima sp. found in D. aurita (Costa-Neto et al. 2018) are potentially zoonotic (Butcher and Grove 2001; Morgan et al. 2001). Eggs detected in the present work did not seem to be of none of these parasites. In fact, all the immature forms presented a peculiar ovoid shape measuring around 100 µm long by 50 µm wide. Such characteristics resemble some Rhopalias spp. (López-Caballero et al. 2019; Haverkost and Gardner 2008).

Oocysts belonging to three genera of Protozoa were herein detected. Eimeria spp. are the most prevalent coccidia in opossums, as reported in a previous study (Aragón-Pech et al. 2018). In fact, there are many species of this genus infecting Didelphis spp.; however, the extent to which most eimerians affect the health of these animals is unknown or not clear (Duszynski 2016). Isospora sp. is herein reported for the first time in D. aurita. This parasite was previously described in D. virginiana (Joseph 1974), and in D. marsupialis (Ernst et al. 1969). A third protozoan, herein identified as Cryptosporidium sp. is also a new record for D. aurita. However, the presence of this coccidian in the black eared opossum were hypothetically known, as it was already recorded in D. albiventris (Zanette et al. 2008), and due to the ubiquitous behavior this coccidia have (Bouzid et al. 2013).

The pathological effects of many parasites of wildlife are unknown or not investigated, and most of them co-inhabit in their hosts with other parasites (Vaumourin et al. 2015). The interactions among these organisms are hardly studied; however, it is known that these relationships may be antagonistic (when an individual inhibit the infection and/or development of other organism), or synergistic (when one parasite facilitates the entry and/or development of other parasites) (Telfer et al. 2010). In our study, most animals presented multiparasitism, and within this variety of parasites, it is hard to know the role that each individual has in animal health. Nevertheless, it is important to highlight that since many of those organisms have zoonotic potential, further studies regarding their identification at species level, as well as their potential to cause human disease, should be performed in order to find out what is the public health impact they have.

In the last decades, the concept of one health has been applied in many areas that involve humans, animals and the environment. In this aspect, Didelphis spp. are particularly important since these animals play relevant ecological role in nature, but they also are reservoirs of important zoonotic pathogens (Bermúdez et al. 2017; Cantor et al. 2010). The synanthropic habit observed in these animals is a reflex of the human activity in terms of deforestation, which consequently increases the opossum population in urban centers due to the destruction of their natural habitat. D. aurita in particular, inhabits mostly the Atlantic Forest remnants (Gardner 2008); however, this marsupial has been frequently found within the urban environments, as observed in our study. This finding is of substantial importance within the One Health concept, since the environmental degradation caused by anthropic activity, causes imbalance in the Didelphis spp. population (Pereira et al. 2017; Lucheis et al. 2009). As a result, the animals seek for new habitats, finding the human dwellings the perfect place to live due to the availability of food and shelter, which leads to the emergence of zoonotic pathogens from the wild to the cities.

This study provides data on the gastrointestinal parasites in D. aurita opossums, highlighting the species with zoonotic potential. Results herein obtained demonstrated that multiparasitism is commonly detected in these animals, and that C. tentaculata is the most prevalent nematode found parasitizing them. Additionally, our study indicated a high percentage of opossums infected by potentially zoonotic parasites such as Ancylostoma spp., Ascaridoidea and Trichuris spp. implying that D. aurita may be involved in zoonotic cycles in urban environments.

Acknowledgements

The authors acknowledge the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and the Graduate Program in Veterinary Medicine of the Universidade Federal de Viçosa (UFV) for the support provided. Finally, authors would like to thank Professor Gisele M. L. del Giúdice for providing traps to capture the animals.

Author’s contributions

MABS, CSF and BCFN collected samples and performed laboratory procedures. LFVF and EMLR performed the molecular procedures. AKC, RANR and RSY supervised the study. MABS, RSY and JAG analyzed the data. MABS wrote the first draft of the manuscript. AKC, RANR, RSY, LFVF, EMLR and JVA revised and performed corrections on the manuscript. All authors read and approved the final version of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The Ethics Committee for Animal Experimentation (ECAE) of the Universidade Federal de Viçosa (License Number: 80/2018) and the Biodiversity Information and Authorization System (SISBIO) (License Number: 64930-1) of the Brazilian Institute of Environment and Renewable Natural Resources (IBAMA) approved all procedures herein performed.

Footnotes

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