Volume 7, ID es20240003 (01-07), 2024
Doi: https://doi.org/10.32435/envsmoke-2024-0003
Environmental Smoke, e-ISSN: 2595-5527
“A leading multidisciplinary peer-reviewed journal”
Full Article:
Déborah Elena Galvão Martins¹,²* (https://orcid.org/0000-0002-3829-4388); Israel Hidenburgo Aniceto Cintra¹ (https://orcid.org/0000-0001-5822-454X); Silvio Felipe Barbosa Lima³ (https://orcid.org/0000-0001-7892-5773); Victória Maria Rodrigues de Sousa¹ (https://orcid.org/0000-0002-0612-9054); Flavio de Almeida Alves-Júnior² (https://orcid.org/0000-0003-3002-6845)
¹Laboratório de Crustáceos (LABCRUS), Instituto Socioambiental e dos Recursos Hídricos (ISARH), Universidade Federal Rural da Amazônia (UFRA), Avenida Presidente Tancredo Neves, nº 2501, Terra Firme, CEP: 66077-830, Belém, Pará, Brasil.
²Universidade Federal do Pará, Núcleo de Ecologia Aquática e Pesca (NEAP), Rua Augusto Corrêa, s/n, Guamá, CEP: 66075-110, Belém, Pará, Brasil. Programa de Pós-Graduação em Ecologia Aquática e Pesca (PPGEAP) da Universidade Federal do Pará (UFPA), Belém, Pará, Brasil.
³Universidade Federal de Campina Grande (UFCG), Centro de Formação de Professores, Unidade Acadêmica de Ciências Exatas e Naturais, Rua Sérgio Moreira de Figueiredo, Casas Populares, Cajazeiras, CEP: 58900-000, Paraíba, Brasil.
*Corresponding author: deborah.martins@ufra.edu.br
Submitted on: 09 Feb. 2024
Accepted on: 25 Mar. 2024
Published on: 05 Apr. 202
License: https://creativecommons.org/licenses/by/4.0/
In this study we report a new occurrence of Paragonimus Braun, 1899 in the Amazon province, recovered from a new host, the semi-terrestrial sesarmid crab Armases benedicti (Rathbun, 1897). Additionally, we would like to alert the health authorities to the presence of trematodes in the urban area of Belém-PA. The specimens of A. benedicti were manually collected on the banks of the Guamá River (01°28’22.6”S; 048°26’49.79”W) in January 2024. We accounted for 42 specimens of A. benedicti, with one male showing the presence of an excysted metacercariae of Paragonimus sp. in the seminal tube. Despite the low number of individuals, the occurrence of this parasite in the region raises the possible parasitism in other organisms such as mollusks, other crustaceans and fish, which are directly consumed by humans. Thus, this paper focuses in warning the risk of contamination of the population, especially by pulmonary paragonimiasis, however, further studies and new samples are needed to identify this parasite in species level and describe its life cycle in the region.
Keywords: Parasites. Armases benedict. New host interaction. Guamá River. Fish-borne trematodes.
1 Introduction
The transmission of diseases through the consumption of contaminated food is widely observed in underdeveloped and developing countries. This is associated with the deficiency or absence of basic sanitation and low water quality, which is a strong agent for the dissemination of parasites between animals and the population (GIBODA et al., 1991; TOLEDO et al., 2022). Trematodes of the family Paragonimidae Dollfus, 1939 are widely reported in the literature as parasites in several species of invertebrates (intermediate hosts) and vertebrates, including humans (final host) (DIAS et al., 2003). Within this family, the genus Paragonimus Braun, 1899 is recorded as the endoparasites of mollusks, crustaceans, fish, birds, rodents, bats, cats, dogs, and humans, which can be parasitized by the consumption of undercooked crab and fish (PHYO MYINT et al., 2020; MARTINS et al., 2023).
Human paragonimiasis is a pulmonary disease that affects millions of people around the world, especially in Africa, Europe and Asia. It is acquired by the presence of some species of Paragonimus such as: P. africanus Voelker & Vogel, 1965, P. heterotremus Chen & Hsia, 1964, P. kellicotti Ward, 1908, P. gondiwanensis Bayssade-Dufour; Hermette; Šundić & Radujković, 2014; P. mexicanus Miyazaki & Ishii, 1968, P. miyazakii Kamo, Nishida, Hatsushika & Tomimura, 1961, P. skrjabini Chen, 1959, P. uterobilateralis Voelker & Vogel, 1965 and P. westermani (Kerbert, 1878) Braun, 1899, which cause respiratory problems such as coughing, tuberculosis and lung necrosis. In rare cases, the parasites can affect the central nervous system, causing paralysis, convulsions and brain damage (LEMOS et al., 2007; BLAIR, 2022).
In Brazil, several cases of contamination of domestic animals and humans by trematodes were reported in the literature: Costa et al. (1984), Bogéa et al. (2005), Oliveira et al. (2005), Siqueira Batista et al. (2006), Lemos et al. (2007), Pinto & Melo (2012) and Martins et al. (2023). However, in the Amazon region, especially in the state of Pará, only the papers performed by Benigno et al. (2014) and Martins et al. (2023) reported the presence of trematodes in metacercariae stages as parasites of fish and shrimp respectively, which can lead to risks for human health through inadequate consumption. Based on this, in this study we report the presence of an excysted metacercariae of Paragonimus sp. in a new host, the semi-terrestrial sesarmid crab Armases benedicti (Rathbun, 1897), collected from the urban area of Belém-PA, Brazil. Additionally, we would like to alert the health authorities to the presence of trematodes in the urban area of Belém-PA, with the risk of contamination by trematoda from fish consumption in the region.
2 Material and Methods
The specimens of A. benedicti were manually collected in January 2024 on the banks of the Guamá River (01°27’54.2”S; 048°26’02.6”W) (Figure 1), one of the main rivers crossing the city of Belém, in the State of Pará. This river shows highly eutrophic characterization, with muddy and turbid waters, and the strong presence of clay particles in suspension since the domestic waste from the Belém metropolitan area, as well as chemical elements from the factories located along the Guamá River (COSTA et al., 2022; MARTINS et al., 2023).
Figure 1. Map indicating the metropolitan region of Belém-PA, Brazil. Black star = sampling point. Land use source: MapBiomas (2023).
Access on: https://drive.google.com/file/d/1SKNZGpVITu9N6WaL7iGDrgCzWU1u5u1m/preview.
After the specimens were collected, they were transported alive to the Carcinology laboratory (LABCRUS) of the Federal Rural University of the Amazon (UFRA), where the individuals were identified and sexed. Afterwards, the specimens were dissected in the carapace region under a stereomicroscope to search for parasites in gills, hepatopancreas and gonads. In the specimen that showed trematode, the tissues were removed, transferred to Petri dishes containing saline solution (NaCl 0.85%) and analyzed by means of optical microscopy to determine whether metacercariae were present, by counting and photographing, using a Motic Moticam5® Camera. For the fixation of metacercariae, we used AFA (Acetone - Formaldehyde - Alcohol).
3 Results and Discussion
42 specimens (22 males and 20 females) of A. benedicti (Figure 2A) were collected, which only one male showed the presence of one excysted metacercariae of Paragonimus sp. in the seminal tube (Figure 2B), this parasite was observed contain 837.92 μm in size (Figure 2C). The presence of metacercariae in invertebrates at the base of the food chain may indicate a risk to the biosafety of the environment, due to strong sewage contamination in the region, directly affecting the organisms that decompose organic matter (i.e. mollusks, shrimps and crabs). The latter become intermediate hosts for trematodes and end up spreading diseases to other hosts, including the human population. According to Doanh; Horii; Nawa (2013), for some species of Paragonimus, the stage of metacercariae can be found excysted in semi-terrestrial brachyuran crabs, as the case of P. proliferus Hsia & Chen, l964, however, in order to identify the parasite reported in this paper at species level, further molecular studies are needed, as well as more specimens for later identification.
Figure 2. A) The crab host Armases benedicti (Rathbun, 1897) (male), B) Metacercariae of Paragonimus sp. Braun, 1899 found in the seminal tube of A. benedicti, C) Paragonimus sp. in the highlighted dorsal view. Scale bars = A) 5 mm and C) 100 μm.
Access on: https://drive.google.com/file/d/1v8e_oas_iDOUZbJxpTqy1gWIDfd_kf21/preview.
In Brazil, several studies in central and southern regions have reported the presence of trematodes in mollusk hosts, especially as endoparasites of the snail species Melanoides tuberculata (Müller, 1774), which act as an intermediate host for the species: Centrocestus formosanus, Opisthorchis felineus (Rivolta,1884) and Opisthorchis viverrini (Poirier, 1886). These species (parasite and host) can be found in urban areas associated with eutrophicated rivers and lakes (PINTO; MELO, 2010; 2012).
Many cases indicating the presence of trematodes in domestic animals are observed in the literature (COSTA et al., 1984; BORAY, 1985, 1986; OLIVEIRA et al., 2005 and references therein); with these parasites causing zoonotic diseases which can lead to the widespread dissemination of these parasites to the environment and other individuals, including humans, who become infected through contact with the feces of these animals (MARTINS et al., 2023).
In studies performed by Chieffi et al. (1990), Dias et al. (1992) and Lemos et al. (2007), observed clinical cases with parasitism by trematodes in humans, with reports of Ascocotyle sp. Looss, 1899, Clonorchis sinensis (Cobbold, 1875), Fasciola hepatica Linnaeus, 1758 and Paragonimus westermani (Kerbert, 1878) in the states of Bahia, Minas Gerais, Rio de Janeiro and São Paulo. The first documented case of human paragonimiasis promoted by P. westermani was observed in the state of Bahia by Lemos et al. (2007), with a patient presenting pulmonary degradation and tuberculosis acquired through the consumption of contaminated shrimp and fish. Additionally, the direct consumption of undercooked or raw shrimp and fish (i.e. salads, sushi) may cause a risk of contamination by trematoda (PHYO MYINT et al., 2020; MARTINS et al., 2023).
The first contamination of humans by trematode is associated with the consumption of contaminated and undercooked fish, when the parasite completes its life cycle in the definitive host (in organs like the liver, spleen, bladder, lungs and brain).
Later the cysts are released into the environment, where, due to the lack of basic sanitation, the new parasites are free to search for new hosts (intermediate and definitive) in aquatic environments, covering especially mollusks, crustaceans and fish (PHYO MYINT et al., 2020; MARTINS et al., 2023). This case is intensified by the migration of parasitized people to other regions of the world where they introduce parasites into new environments, thus increasing the range of occurrence of the parasite species and raising the number of new parasitized people, hence causing a serious public health issue (DIAS et al., 1992; BELIZARIO et al., 2001).
Studies performed by Doanh et al. (2007; 2016), Sugiyama et al. (2009) Calvopina et al. (2018) and Banzai et al. (2021), reported the presence of Paragonimus spp. using invertebrates, especially freshwater crabs, as intermediate hosts. The occurrence of Paragonimus sp. in urban areas presents the risk of contamination to other organisms that consume these invertebrates, especially fish, which afterwards will become one of the definitive hosts and be directly consumed by humans. Despite the high level of urbanization and eutrophication of the Guamá River, several shrimp and fish species are commonly consumed by the population (i.e. Brachyplatystoma rousseauxii (Castelnau, 1855), Hypophthalmus marginatus Valenciennes, 1840, Plagioscion squamosissimus (Heckel, 1940) and Macrobrachium amazonicum Heller, 1862).
The presence of Paragonimus sp. in the city of Belém may be associated with the high urbanization process and the lack of basic sanitation, which can lead to the risk of contamination of the population by the inadequate consumption of fish from the Guamá River.
4 Conclusions
This paper reinforces the warning to health authorities about the presence of Paragonimus sp. observed in a new invertebrate host species (Armases benedicti) in the urban areas of Belém-PA. From this host, Paragonimus sp. can reach fish in the entire food chain and even be consumed by humans. In this case, the parasite can cause serious health issues, especially pulmonary paragonimiasis, resulting from the inadequate consumption of parasitized fish collected in the region.
CREDIT AUTHORSHIP CONTRIBUTION STATEMENT
DEGM, VMRS and FAAJ conceived the research ideas, designed the study and writing the manuscript; IHAC and SFBL performed the first draft of this manuscript and revisions along the main text.
DECLARATION OF INTEREST
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence this study.
FUNDING SOURCE
No financial contribution was used for the development of this article.
ACKNOWLEDGEMENTS
The authors would like to thank the National Center for Research and Conservation of Northern Marine Biodiversity - CEPNOR / ICMBio for the support and laboratory for this study. Also, we would like to thank the anonymous reviewers for their precious comments in this manuscript.
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