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. 2024
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.
REFERENCES
BANZAI, A.; SUGIYAMA, H.;
HASEGAWA, M.; MORISHIMA, Y.; KAWAKAMI, Y. Paragonimus westermani metacercariae
in two freshwater crab species in Kagoshima Prefecture, Japan, as a possible
source of infection in wild boars and sika deer. The Journal of
Veterinary Medical Science, v. 83, n. 3, p. 412-418, 2021. Available from: https://doi.org/10.1292/jvms.20-0576
BENIGINO, R.N.M.; KNOFF, M.;
MATOS, E.R.; GOMES, D.C.; PINTO, R.M.; SÃO CLEMENTE, S.C. Morphological aspects
of Clinostomidae metacercariae
(Trematoda: Digenea) in Hoplerytrinus unitaeniatus
and Hoplias malabaricus
(Pisces: Erythrinidae) of the Neotropical region, Brazil. Anais da Academia Brasileira de Ciências, v. 86, n. 2, p. 733-744,
2014. Available from: http://dx.doi.org/10.1590/0001-3765201420130025
BELIZARIO, J.V.; BERSABE, M.J.; HILOMEN, V.Y.; PALLER, G.V.; BUGAYON,
M.G. Intestinal heterophyidiasis: an emerging
food-borne parasitic zoonosis in southern Philippines. The Southeast Asian Journal of Tropical Medicine and Public Health,
v. 32, p. 36-42, 2001. Available from: https://pubmed.ncbi.nlm.nih.gov/12041601.
BLAIR, D. Lung flukes of the genus Paragonimus: ancient and
re-emerging pathogens. Parasitology, 149(10), 1286-1295, 2022.
Available from: http://dx.doi.org/10.1017/S0031182022000300
BOGÉA,
T.; CORDEIRO, F.M.; GOUVEIA, J.S. Melanoides
tuberculatus (Gastropoda: Thiariidae)
as intermediate host of Heterophyidae
(Trematoda: Digenea) in Rio
de Janeiro metropolitan area,
Brazil. Revista do Instituto de Medicina
Tropical de São Paulo, v. 47, n. 2, p. 87-90, 2005. Available
from: https://doi.org/10.1590/S0036-46652005000200005
BORAY, J.C.
Flukes of domestic animals. In: GAAFAR, S.M.; HOWARD, W.E.; MARSH, R.E. (Orgs).
Parasites, pests and predators: Word
Animal Sciences. Volume B2. Glenfield: Elsevier Science Publishers, v. 91,
n. 2, 1985. Available from: https://www.cambridge.org/core/services/aop-cambridge-core/content/view/3034DD6A30AFAA1F284152C79B632616/S0031182000057292a.pdf/div-class-title-par-volume-91-issue-2-cover-and-back-matter-div.pdf. Accessed on: 08 Jan. 2024.
BORAY, J.C. Trematode
infections of domestic animals. In: CAMPBELL, W.C.; Rew, R.S. (Orgs).
Chemotherapy of Parasitic Disease. New York: Plenum Press, 1986.
CALVOPINA, M.; ROMERO-ALVAREZ, D.; RENDON, M.;
TAKAGI, H.; SUGIYAMA, H. Hypolobocera guayaquilensis
(Decapoda: Pseudothelphusidae): A New Crab
Intermediate Host of Paragonimus mexicanus in Manabí Province, Ecuador. Korean Journal of Parasitology, v. 56,
n. 2, p. 189-194, 2018. Available from: https://doi.org/10.3347/kjp.2018.56.2.189
CHIEFFI, P.;
LEITE, O.H.; DIAS, R.M.D.S.; TORRES, D.M.A.V.; MANGINI, A.C.S. Human parasitism
by Phagicola
sp. (Trematoda,
Heterophyidae) in São Paulo State,
Brazil. Revista do Instituto de Medicina
Tropical, v. 32, n. 4, p. 285-288, 1990. Available
from: https://doi.org/10.1590/S003646651990000400008
COSTA, H.M.A.; LIMA, W.S.; COSTA, J.O. Phagicola arnaldoi (Travassos, 1928) Travassos,
1929 (Trematoda, Heterophyidae)
em Canis familiaris.
Arquivo Brasileiro de Medicina
Veterinária e Zootecnia, v. 36, p. 591-595, 1984. Available
from: https://www.scielo.br/j/abmvz/. Accessed on: 15 Jan. 2024.
COSTA, G.M.M.; RIBEIRO, H.M.C.; PANTOJA, D.N.S.M. Classificação do nível
de trofia de um trecho do Rio Guamá, Belém - Pará. Revista Geoaraguaia, v. 12, n. 1, p. 176-191,
2022. Available from: https://periodicoscientificos.ufmt.br/ojs/index.php/geo/article/view/11681. Accessed
on: 11 Jan. 2024.
DIAS, R.M.D.S.; MANGINI, A.C.S.; TORRES, D.M.A.G.V.; VELLOSA, S.A.G.;
SILVA, R.M.; SILVA, M.I.P.G. Introdução de Clonorchis sinensis por imigrantes do leste
asiático no Brasil e a suspensão da obrigatoriedade de exames laboratoriais
para obtenção de vistos de permanência. Revista
Brasileira de Análises Clínicas, v. 24, n. 2, p. 29-30, 1992. Available from: https://pesquisa.bvsalud.org/portal/resource/pt/lil-119549. Accessed on: 18 Jan. 2024.
DIAS,
M.L.G.G.; EIRAS, J.C.; MACHADO, M.H.; SOUZA, F.T.; PAVANELI, G.C. The life
cycle of Clinostomum complanatum
Rudolphi, 1814 (Digenea, Clinostomidae) on the
floodplain of the high Paraná River, Brazil. Parasitology Research, v. 89, p. 506-508, 2003. Available from: https://doi.org/10.1007/s00436-002-0796-z
DOANH, P.N.; SHINOHARA, A.; HORII, Y.; HABE, S.; NAWA, Y.; THE, D.T.;
LE, N.T. Morphological and molecular identification of two Paragonimus spp., of which metacercariae concurrently found in a land crab, Potamiscus tannanti,
collected in Yenbai Province, Vietnam. Parasitology Research, v. 100, p. 1075-1082,
2007. Available from: https://doi.org/10.1007/s00436-006-0411-9
DOANH, P.N.; HORII, Y.; NAWA, Y. Paragonimus and Paragonimiasis in Vietnam: an Update. Korean Journal of Parasitology, v. 51,
n. 6, p. 621-627, 2013. Available from: http://dx.doi.org/10.3347/kjp.2013.51.6.621
DOANH, P.N.; TU, A.L.; BUI, T.D.;
LOAN, T.H.; NONAKA, N.; HORII, Y.; BLAIR, D.; NAWA, Y. Molecular and
morphological variation of Paragonimus westermani in Vietnam with records of new second
intermediate crab hosts and a new locality in a northern province. Parasitology, v. 143, n. 12, p. 1639-1646,
2016. Available from: https://doi.org/10.1017/S0031182016001219
GIBODA, M.; DITRICH, O.; SCHOLZ,
T.; VIENGSAY, T.; BOUAPHANH, S. Human Opisthorchis
and Haplorchis
infections in Laos, Transactions of the
Royal Society of Tropical Medicine and Hygiene, v. 85, n. 4, p. 538-540,
1991. Available from: https://doi.org/10.1016/0035-9203(91)90248-W
LEMOS, A.C.M.;
COELHO, J.C.; MATOS, E.D.; MONTAL, G.; AGUIAR, F.; BADARÓ, R. Paragonimiasis:
first case reported in Brazil. Brazilian
Journal of Infectious Diseases, v. 11, n. 1, p. 153-156, 2007. Available
from: https://doi.org/10.1590/S1413-86702007000100031
MAPBIOMAS
PROJECT. Collection 8 of the Annual Land Cover and Land Use Maps of Brazil
(1985-2022), MapBiomas,
v. 1, 2023. Available from: https://doi.org/10.58053/MapBiomas/VJIJCL
MARTINS, D.E.G.;
CINTRA, I.H.A.; MARTINS, M.G.; ALVES-JÚNIOR, F.A. presence of metacercariae of Opisthorchis
sp. Blanchard, 1895 (Trematoda: Opisthorchiidae) in
new host Macrobrachium amazonicum (heller,
1862), from the northern Brazil: an emerging risk to humans by the shrimp
consumption. Environmental smoke, v.
6, n. 2, p. 36-45, 2023. Available from: https://doi.org/10.32435/envsmoke-2023-0016
OLIVEIRA, P.M.A.; PIRES, P.R.R.; GINJA, M.J.; PIRES, I.; CARDOSO, L.;
ANTUNES, L.; RODRIGUES, M. Opisthorchis felineus in cat: case report. Arquivo Brasileiro de Medicina Veterinária
e Zootecnia, v. 57, n. 4, p. 556-558, 2005. Available
from: https://doi.org/10.1590/S0102-09352005000400020
PINTO, H.A.; MELO, A.L. Melanoides
tuberculata (Mollusca: Thiaridae) as an intermediate host of Centrocestus formosanus (Trematoda:
Heterophyidae) in Brazil. Revista do Instituto de Medicina Tropical de São Paulo, v. 52, n. 4,
p. 207-210, 2010. Available from: https://doi.org/10.1590/S0036-46652010000400008
PINTO, H. A.; MELO, A. L. Metacercariae of Centrocestus formosanus (Trematoda: Heterophyidae) in Australoheros facetus
(Pisces: Cichlidae) in Brazil. Revista
Brasileira de Parasitologia Veterinária, v. 21, n. 3, p. 334-337, 2012. Available from: https://doi.org/10.1590/S1984-29612012000300032
PHYO MYINT,
E.E.; SEREEMASPUN, A.; ROCKLÖV, J.; NITHIKATHKUL, C. Discovery of Carcinogenic
Liver Fluke Metacercariae in Second Intermediate
Hosts and Surveillance on Fish-Borne Trematode Metacercariae
Infections in Mekong Region of Myanmar. International
Journal of Environmental Research and Public Health, v. 17, n. 11, 2020.
Available from: https://doi.org/10.3390/ijerph17114108
SIQUEIRA-BATISTA,
R.; GOMES, A.P.; ALBUQUERQUE, V.S.; PINA-COSTA, A.; ROCHA-MELLO, A.;
GUIMARÃES-PEREIRA, E.; RAMOS-OLIVEIRA, F.; RUBIÃO, E.C.N. História natural da
infecção por Paragonimus:
abordagem clínica e ecológica. Pulmão, v. 15, n. 4, p. 270-276, 2006. Available from:
https://www.sopterj.com.br/wp-content/themes/_sopterj_redesign_2017/_revista/2006/n_04/10.pdf
SUGIYAMA, H.;
UMEHARA, A.; MORISHIMA, Y.; YAMASAKI, H.; KAWANAKA, M. Detection of Paragonimus metacercariae in the Japanese freshwater crab, Geothelphusa dehaani, bought at retail fish markets in Japan. Japanese Journal of Infectious Diseases, v. 62, n. 4, p. 324-325,
2009. Available from: https://www.niid.go.jp/niid/JJID/62/324.pdf. Accessed on: 10 Jan. 2024.
TOLEDO, R.; ÁLVAREZ-IZQUIERDO,
M.; ESTEBAN, J.G.; MUÑOZ-ANTOLI, C. Neglected food-borne trematodiases:
echinostomiasis and gastrodiscoidiasis.
Parasitology, v. 149, n. 10, p.
1319-1326, 2022. Available from: https://doi.org/10.1017/S0031182022000385