Intestinal Trematode Research Articles

Echinostomes and Other Intestinal Trematode Infections.

Intestinal trematodes are among the most common types of parasitic worms. About 76 species belonging to 14 families have been recorded infecting humans. Infection commonly occurs when humans eat raw or undercooked foods that contain the infective metacercariae. These parasites are diverse in regard to their morphology, geographical distribution and life cycle, which make it difficult to study the parasitic diseases that they cause. Many of these intestinal trematodes have been considered as endemic parasites in the past. However, the geographical limits and the population at risk are currently expanding and changing in relation to factors such as growing international markets, improved transportation systems, new eating habits in developed countries and demographic changes. These factors make it necessary to better understand intestinal trematode infections. This chapter describes the main features of human intestinal trematodes in relation to their biology, epidemiology, host-parasite relationships, pathogenicity, clinical aspects, diagnosis, treatment and control.

Immunology and pathology of echinostomes and other intestinal trematodes.

Intestinal trematodes constitute a major group of helminths that parasitize humans and animals with relevant morbidity and mortality. Despite the importance of the intestinal trematodes in medical and veterinary sciences, immunology and pathology of these helminth infections have been neglected for years. Apart from the work focused on the members of the family Echnistomatidae, there are only very isolated and sporadic studies on the representatives of other families of digeneans, which makes a compilation of all these studies necessary. In the present review, the most salient literature on the immunology and pathology of intestinal trematodes in their definitive hosts in examined. Emphasis will be placed on members of the echinostomatidae family, since it is the group in which the most work has been carried out. However, we also review the information on selected species of the families Brachylaimidae, Diplostomidae, Gymnophallidae, and Heterophyidae. For most of these families, coverage is considered under the following headings: (i) Background; (ii) Pathology of the infection; (iii) Immunology of the infection; and (iv) Human infections.

Trematode parasites as indicators of an animal component in the diet of the Water Vole Arvicola amphibius.

The intestinal trematode fauna of the Water Vole Arvicola amphibius, (previously A. terrestris), was investigated to determine whether it might provide evidence of an animal component in the diet of this aquatic herbivorous small mammal. Interrogation of the electronic Host-Parasite Database of the Natural History Museum London revealed the presence of fourteen species of intestinal trematode in water voles, infection with each of which would require the ingestion of tissue from an animal intermediate host. The results obtained using these parasite indicators provide convincing evidence of animal components in the diet of A. amphibius and support anecdotal reports of water voles feeding on animal material in the field.

Elucidating the life cycle of opossum parasites: DNA sequences reveal the involvement of planorbid snails as intermediate hosts of Rhopalias spp. (Trematoda: Echinostomatidae) in Brazil.

Echinostomatid digeneans belonging to the genus Rhopalias are intestinal trematodes found mainly in opossums in the New World. The genus comprises seven species, but their life cycles and intermediate hosts have been unknown until now. During our long-term study carried out in freshwater habitats within the state of Minas Gerais, Southeast Brazil, echinostomatid cercariae lacking collar spines were found in planorbid snails Biomphalaria glabrata, Biomphalaria straminea, Drepanotrema lucidum and Gundlachia ticaga in six different batches of snail samples collected between 2010 and 2019. Morphologically, the larvae reported herein are morphologically consistent with each other and characterized by the presence of 2-3 large ovoid or spherical corpuscles in each main duct of the excretory system, resembling to Cercaria macrogranulosa previously described from the same region of Brazil. Partial sequences of the ITS (ITS1-5.8S-ITS2) region and 28S gene of the nuclear ribosomal RNA operon, and partial sequences of mitochondrial nad1 and cox1 genes were obtained and compared with the data available for members of the family Echinostomatidae. Nuclear markers indicate that all samples of cercariae evaluated in the present study can be assigned to Rhopalias, but distinct from North American isolates of Rhopalias macracanthus, Rhopalias coronatus and Rhopalias oochi (divergence 0.2-1.2% in 28S and 0.8-4.7% in ITS). The lack of differences verified in both 28S and ITS in 5 out 6 studied samples suggested that they belong to the same species. However, nad1 sequences revealed that our cercariae correspond to three distinct species of Rhopalias (interspecific divergence: 7.7-9.9%), named here as Rhopalias sp. 1, found in B. straminea and G. ticaga, Rhopalias sp. 2 found in B. glabrata and D. lucidum, and Rhopalias sp. 3 also found in D. lucidum. They also differ by 10.8-17.2% from a North American isolate of R. macracanthus sequenced in this study. The cox1 sequences obtained for Rhopalias sp. 1 and Rhopalias sp. 2 (but not Rhopalias sp. 3) reveal that they are distinct from North American isolates of R. macracanthus (genetic divergence 16.3-16.5% and 15.6-15.7%, respectively), R. coronatus (9.2-9.3% and 9.3-9.5%) and Rhopalias oochi (9.0% and 9.5-10.1%). Encysted metacercariae with general morphology similar to that of the body of cercariae were found in tadpoles of Rhinella sp. from the same stream where snails harbored Rhopalias sp. 2, suggesting that the amphibians could act as second intermediate hosts of species of Rhopalias. Data obtained provide the first insights into the life cycle of this unusual echinostomatid genus.

Potential for Emergence of Foodborne Trematodiases Transmitted by an Introduced Snail (Melanoides tuberculata) in California and Elsewhere in the United States.

We document that 3 human-infectious trematodes and their introduced first intermediate host snail (Melanoides tuberculata) are widespread throughout southern California. We surveyed 41 fishing localities, 19 of which harbored snails infected with zoonotic trematodes. Two of the parasites, Haplorchis pumilio and Centrocestus formosanus, are fishborne intestinal trematodes recognized as being important human pathogens in other areas of the world; the third, Philophthalmus gralli, can infect the human eye. An additional 5 species detected infecting M. tuberculata are likely of little direct threat to people; however, they may be recently introduced to the Americas, highlighting the risk that additional pathogenic trematodes transmitted by the snail in its native range could be introduced to the United States. The current, possible human-infection risk in California clarifies the need to consider the introduced snail and its parasites from a public health perspective anywhere in the United States the snail has been introduced.

Changes in resident microbiota associated with mice susceptibility or resistance to the intestinal trematode Echinostoma caproni.

Echinostoma caproni (Trematoda: Echinostomatidae) is an intestinal trematode with no tissue phases in the definitive host that has been extensively used as an experimental model to study the factors that determine resistance against intestinal helminths. In E. caproni infections in mice, interleukin-25 (IL-25) plays a critical role and it is required for the resistance to infection. However, little is known on the factors that determine its production. Primary E. caproni infection in mice is characterized by the development of chronic infections and elevated worm recovery, in relation to a local Th1 response with elevated production of interferon-γ. However, partial resistance against secondary E. caproni infections in ICR (Institute of Cancer Research) mice is developed after the chemotherapeutic cure of a primary infection and the innately produced IL-25 after pharmacological treatment. In this paper, we analyse the potential role of intestinal microbiota in the production of IL-25, and the subsequent resistance to infection. For this purpose, we analysed the production of IL-25 under conditions of experimental dysbiosis and also the changes in the resident microbiota in primary infections, pharmacological curation and secondary infections. The results obtained showed that resident microbiota play a major role in the production of IL-25 and the appearance of members of the phylum Verrucomicrobia as a consequence of the curation of the primary infection could be related to the partial resistance to secondary infection.

Fasciolopsis buski Detected in Humans in Bihar and Pigs in Assam, India.

The foodborne intestinal trematode Fasciolopsis buski causes the neglected zoonotic disease fasciolopsiasis. We detected F. buski infection in 14 pediatric patients in Sitamarhi, Bihar, and in pigs in Sivasagar, Assam, India. Proper diagnostic methods and surveillance are urgently needed to accurately estimate the true burden of this disease in India.

Community structure of intestinal adult trematodes (Platyhelminthes) in six species of Haemulon (Osteichthyes) in Puerto Morelos Reef National Park, Quintana Roo, Mexico

Haemulids (grunts) represent one of the most diverse families of marine fishes. Even though haemulids are well represented in Mexico along the Pacific and Gulf of Mexico coasts, as well as in the Caribbean Sea, their trematode fauna has been scarcely studied. Here, 8 species of Haemulon from the Puerto Morelos Reef National Park (PMRNP), Quintana Roo were analyzed to describe their trematode species composition and the patterns of their community structure at both, infracommunity and component community levels. Eleven species of trematodes from the gastrointestinal tract of their hosts were identified. Overall, 16 new host records are reported in this study. Eight of the 11 trematode species are reported in the PMRNP for the first time. All trematode species were considered as rare species, with prevalence values < 20%. Species accumulation curves showed that 3 of the 6 host species, i.e., H. flavolineatum, H. plumierii, and H. sciurus , reached an asymptote, and only their trematode community structure was analyzed. Communities were species-poor and dominated by a single trematode species, with low diversity values at both, infracommunity and component community levels. Trematode communities differ among species of grunts analyzed in this study, indicating that ecological factors such as feeding habits, geographic distribution, and host vagility play a major role structuring these communities.

Monsters in our food: Foodborne trematodiasis in the Philippines and beyond

Foodborne trematodiasis is a neglected tropical disease (NTD) caused by zoonotic trematodes that persist mainly in impoverished areas in the Asia-Pacific region. Globally, about 2 million disability life years (DALYs) are lost due to these parasitic infections. Four groups of foodborne trematodes are known to cause significant illness: fish-borne liver fluke infections caused by Opisthorchis and Clonorchis spp.; water vegetable-borne Fasciola spp. infections; crustacean-vectored paragonimiasis; and those caused by intestinal trematodes. In the Philippines, endemic foodborne trematodes of public health concern include Paragonimus westermani, some members of Heterophyidae and Echinostomatidae, and Fasciola hepatica/ F. gigantica. Opisthorchis viverrini and Clonorchis sinensis have also been reported in the country. Data on the epidemiology of these zoonotic illnesses remain scarce and in need of research attention in the Philippines. Culturally rooted eating behaviors in endemic areas are important risk factors to acquiring and perpetuating foodborne trematodiasis. The combination of mass drug administration (MDA), provision of clean water and maintenance of good sanitation and hygiene (WASH), community health education towards modification of risky behaviors, surveillance, and veterinary public health interventions have been shown to be effective in combatting these zoonotic parasitoses. An integrated control and prevention program anchored on the One Health paradigm is a must to address these illnesses. This paper aims to review the biology and epidemiology of, and public health interventions against zoonotic foodborne trematodiasis in the Philippines and its neighboring countries.

MORPHOLOGICAL AND MOLECULAR IDENTIFICATION OF ZOONOTIC TREMATODE METACERCARIAE (Haplorchis taitui) IN FRESHWATER FISH IN IRAN

The intestinal trematode, Haplorchis taichui (Nishigori, 1924), is an important in public health that causes infection in humans and animals especially in Asia and in parts of Africa and the Americas. Haplorchis taitui metacercariae were found in the gills of Cyprinion macrostomus (Heckel) and Capoeta barroisi persica (Karaman) collected from the Shapour River. Morphological excysted metacercariae were identified as wet mounts under a stereomicroscope. Then, the samples were subjected to molecular analysis. The result showed that 69% of examined fish (n = 30) were diagnosed infected with encysted metacercariae in gills. The mean intensity was 8.3 ± 16.9 parasites per fish. The morphometrical values agree with the findings of other studies with the small differences and polymerase chain reaction product length and nucleotide sequence analysis of 18S ribosomal deoxyribonucleic acid gene showed a similarity of over 99% between the specimens and the Haplorchis taichui (Nishigori, 1924) recorded in GenBank.

Exploring Neotropical anuran parasites: a morphological, life cycle and phylogenetic study of Catadiscus marinholutzi (Trematoda: Diplodiscidae).

Amphistome species belonging to the genus Catadiscus are poorly studied intestinal trematodes found primarily in Neotropical anurans. Herein, developmental stages of an amphistome species found during herpetological and malacological surveys in a temporary marsh pond from Brazil were subjected to morphological (light and scanning electron microscopy) and molecular analyses. Adult parasites recovered from anurans were identified as Catadiscus marinholutzi. Amphistome cercariae found in the planorbid snails Drepanotrema depressissimum and Drepanotrema lucidum from the same waterbody were used for experimental and molecular studies. Immature parasites, morphologically compatible with members of Catadiscus, were experimentally obtained in laboratory-reared tadpoles. Sequencing of a partial region of 28S rDNA gene of both adult and cercariae revealed 100% similarity between these developmental stages, confirming their conspecificity. Phylogenetic analyses were attempted for the first time to reveal the position of a species of Catadiscus in the superfamily Paramphistomoidea. Catadiscus marinholutzi falls in a virtual polytomy together with other paramphistomoids, which leaves its phylogenetic relationships within the group unclear. Moreover, the high genetic divergence to Diplodiscus spp. (10.06–10.84%) cast doubts on the placement of Catadiscus within Diplodiscidae. Hence the species composition of the Diplodiscidae should be re-evaluated in further studies using a broader spectrum of related taxa.

Intestinal parasitic infections in a population ofBaAka Pygmies inhabiting the Congo Basin inthe Central African Republic.

Pygmy tribes inhabit tropical environment of Central Africa. After expulsion from their original habitat by the Bantu people, they settled in a local forest ecosystem where they live with very low sanitary standards. Their actual morbidity remains unknown. The aim of the study was to analyze the prevalence of intestinal parasitic infections in BaAka Pygmies inhabiting the Congo Basin in the Central African Republic. The study was conducted in 2015, and involved a group of 950 Pygmies living inthe Sangha-Mbaere and Lobaye prefectures. Single stool samples were collected from study participants, fixed in 10% formalin, transported from Africa to Europe, and analyzed by light microscopy using 5 different diagnostic methods (direct smear, decantation with distilled water, Fülleborne's flotation, Kato-Miura thick smear, DiaSyS/PARASYS system sedimentation) at the Military Institute of Medicine in Warsaw, Poland. Microscopic examination revealed infections with 14 different species of intestinal nematodes, cestodes, trematodes and protozoa. According to the study findings, 90.5% of BaAka Pygmies were found to be infected with intestinal parasites, and 70.8% had mixed infections. Most of the pathogenic intestinal parasites were nematodes (85.0%), with Asrcaris lumbricoides (29.8%), hookworm (29.4%) and Trichuris trichiura (10.7%) being predominant. Poor sanitation, limited the high prevalence of intestinal parasitic infections in the community of Pygmies. The negative test results may prove the effectiveness of periodic deworming campaigns chich, implemented by non-governmental organizations, are voluntary with respect to the informed consent principle.

Interleukin-25-mediated resistance against intestinal trematodes does not depend on the generation of Th2 responses

BackgroundThe cytokine interleukin-25 (IL-25) is recognized as the most relevant initiator of protective T helper 2 (Th2) responses in intestinal helminth infections. This cytokine induces resistance against several species of intestinal helminths, including the trematode Echinostoma caproni. E. caproni has been extensively used as an experimental model to study the factors determining resistance to intestinal infections. In the study reported here, we assessed the role of IL-25 in the generation of resistance in mice infected with E. caproni.MethodsThe factors that determine the production of IL-25 in mice experimentally infected with E. caproni were determined, as were the consequences of IL-25 production in terms of polarization of the immune response and resistance to infection.ResultsOur results show that the role of IL-25 in the polarization of the immune response differs between the primary and secondary immune responses. IL-25 is required for the development of a Th2 phenotype in primary E. caproni infections, but it can also promote the differentiation to Th2 memory cell subsets that enhance type-2 immunity in memory responses. However, the development of Th2 responses does not induce resistance to infection. The Th2 phenotype does not elicit resistance, and IL-25 is responsible for the resistance regardless of its type-2 cytokine activity and activation of signal transducer and activator of transcription (STAT6). Alternative activation of macrophages induced by IL-25 can be implicated in the resistance to infection.ConclusionsIn contrast to primary infection, secondary infection elicits a type-2 immune response even in the absence of IL-25 expression. Despite the development of a type-2 response, mice are susceptible to secondary infection associated with the lack of IL-25. Resistance to infection is due to the production of IL-25, which acts autonomously from Th2 response in terms of parasite clearance.Graphical

Cluster of Parasite Infections by the Spatial Scan Analysis in Korea.

This study was performed to find out the clusters with high parasite infection risk to discuss the geographical pattern. Clusters were detected using SatScan software, which is a statistical spatial scan program using Kulldorff’s scan statistic. Information on the parasitic infection cases in Korea 2011–2019 were collected from the Korea Centers for Disease Control and Prevention. Clusters of Ascaris lumbricoides infection were detected in Jeollabuk-do, and T. trichiura in Ulsan, Busan, and Gyeongsangnam-do. C. sinensis clusters were detected in Ulsan, Daegu, Busan, Gyeongsangnam-do, and Gyeongsangbuk-do. Clusters of intestinal trematodes were detected in Ulsan, Busan, and Gyeongsangnam-do. P. westermani cluster was found in Jeollabuk-do. E. vermicularis clusters were distributed in Gangwon-do, Jeju-do, Daegu, Daejeon, and Gwangju. This clustering information can be referred for surveillance and control on the parasitic infection outbreak in the infection-prone areas.

Morphological and Molecular Characterization of Apharyngostrigea pipientis Faust, 1918 (Trematoda: Diplostomidea) from Ardeacinerea jouyi, Egretta intermedia and Nycticorax nycticorax in Korea

An intestinal strigeiid trematode, Apharyngostrigea pipientis, was detected from Ardea cinerea jouyi, Egretta intermedia and Nycticorax nycticorax between July, 2006 and June, 2020 in Daejeon metropolitan city and Kangwondo, Republic of Korea. It was observed with a light and scanning electron microscope (SEM), and molecularly analyzed with 18S rRNA genes. The infection rate of the strigeiid trematode was 25.9% (7/27). The body is cylindrical in whole mount, greatly elongated in outline and shows a strong dorsal curvature. The overall measurements are: length 4.1-4.8 ㎜; fore-body 1.00-1.20 ㎜ by 0.8-0.9 ㎜; hind-body 3.2-3.6 ㎜ by 0.43-0.46 ㎜. The body is covered by a relatively thick cuticle, devoid of spines. The oral sucker leads into a short esophagus that is devoid of a muscular pharynx. The holdfast organ is enormously developed. The vitelline follicles distributed dorsal wall of fore-body and hind-body. This strigeiid trematode especially differs from other species of genus Apharyngostrigea in morphology. Although these A. pipientis are several morphological distinctions from Apharyngostrigea cornu, the partial sequence of 18S rRNA showed the sequence homology of A. pipientis (99.9%) and A. cornu (99.8%), and this result revealed their conspecific relationship between A. cornu and A. pipientis. This is the first report of A. pipientis in the Republic of Korea.

Ileal proteomic changes associated with IL-25-mediated resistance against intestinal trematode infections

BackgroundEchinostoma caproni (Trematoda: Echinostomatidae) is an intestinal trematode, which has been extensively used to investigate the factors that determine the rejection of intestinal helminths. In this sense, several studies have shown that IL-25 is critical for the development of resistance against E. caproni in mice. In fact, treatment of mice with recombinant IL-25 generates resistance against primary E. caproni infection. However, the mechanisms by which IL-25 induces resistance remain unknown.MethodsTo study the mechanisms responsible for resistance elicited by IL-25, we analyzed the ileal proteomic changes induced by IL-25 in mice and their potential role in resistance. To this purpose, we compared the protein expression profiles in the ileum of four experimental groups of mice: naïve controls; E. caproni-infected mice; rIL-25-treated mice; and rIL-25-treated mice exposed to E. caproni metacercariae.ResultsQuantitative comparison by 2D-DIGE showed significant changes in a total of 41 spots. Of these, 40 validated protein spots were identified by mass spectrometry corresponding to 24 proteins.ConclusionsOur results indicate that resistance to infection is associated with the maintenance of the intestinal epithelial homeostasis and the regulation of proliferation and cell death. These results provide new insights into the proteins involved in the regulation of tissue homeostasis after intestinal infection and its transcendence in resistance.

Bilharzial Colonic Polyps: Case Presentation

Background: Schistosomiasis is a contagion caused by intestinal and urinary blood trematodes affecting around 200 million people worldwide. Adult worms colonize human blood vessels for years, successfully escaping the immune system while excreting hundreds to thousands of eggs daily. The chronic infection can cause anemia, retarded growth, hepatosplenomegaly, neurological sequlae and even death. For Diagnosis of schistosomiasis, microscopic examination of human wastes as well as tissues remains the gold standard owing to the characteristic shape and size of the eggs. Objective: to present a case of bilharzial polyps presented to endoscopy unit of the department of Tropical Medicine, Faculty of Medicine, Alexandria University, Egypt for colonoscopy and mistaken for IBD with suspicious polypoidal transfromation versus malignant process. Methodolgy: Snare polypectomy was done and tissues were sent for histopathological evaluation which revealed multiple fresh and calcified bilharzial ova seen in mucosa and submucosa. Conclusion: This unusual long standing case will give us the chance to recall schistosomiasis, its occurrence as colon polyps, clinical presentation and means of management.

Mitochondrial Genome Sequence of Echinostoma revolutum from Red-Crowned Crane (Grus japonensis).

Echinostoma revolutum is a zoonotic food-borne intestinal trematode that can cause intestinal bleeding, enteritis, and diarrhea in human and birds. To identify a suspected E. revolutum trematode from a red-crowned crane (Grus japonensis) and to reveal the genetic characteristics of its mitochondrial (mt) genome, the internal transcribed spacer (ITS) and complete mt genome sequence of this trematode were amplified. The results identified the trematode as E. revolutum. Its entire mt genome sequence was 15,714 bp in length, including 12 protein-coding genes, 22 transfer RNA genes, 2 ribosomal RNA genes and one non-coding region (NCR), with 61.73% A+T base content and a significant AT preference. The length of the 22 tRNA genes ranged from 59 bp to 70 bp, and their secondary structure showed the typical cloverleaf and D-loop structure. The length of the large subunit of rRNA (rrnL) and the small subunit of rRNA (rrnS) gene was 1,011 bp and 742 bp, respectively. Phylogenetic trees showed that E. revolutum and E. miyagawai clustered together, belonging to Echinostomatidae with Hypoderaeum conoideum. This study may enrich the mitochondrial gene database of Echinostoma trematodes and provide valuable data for studying the molecular identification and phylogeny of some digenean trematodes.

Review of Successful Control of Parasitic Infections in Korea.

Korea had been one of hyperendemic countries of human parasitic infections until 1970s. In 1966, the Law for the Prevention of Parasitic Diseases was enacted, and the nationwide anti-parasitic control program began in 1969. The initiation of the national program was supported financially by Japan. The program included screening of whole students in Korea and treatment of all egg positive cases twice a year, and ended in 1995. In addition to student program, deworming campaign was run in the community, and 8 national status surveys were implemented from 1971 to 2012. Whole helminth egg positive rate was 84.3% in 1971 and decreased to 2.6% in 2012. Ascaris and other intestinal nematodes, Paragonimus, Taenia, and intestinal protozoa had decreased significantly throughout the country, but Clonorchis sinensis and intestinal trematodes are still prevalent locally in endemic areas. Lymphatic filariasis had been endemic in Jeju-do and other southern islands but elimination was endorsed in 2008. The control of parasitic infection in Korea was successful with statistical prevalence data, which can be a benchmarking model. In conclusion, the successful control in Korea could be achieved by social agreement of the priority, professional guidelines and systematic approach with good anthelminthics supply, and simultaneous economic growth.

The Occurrence and Diversity of Intestinal Digenetic Trematodes in Stray Cats, Felis Catus, In Egypt

Stray cats act as good indicators of fish-borne trematodes in the environment. Large populations of stray cats, Felis catus, are widespread in Giza, Egypt. Therefore, a total of 47 stray cats from some urban districts in Giza, Egypt were necropsied during the period from December 2018 to April 2019 and their intestines were examined for the detection of digenetic trematodes. Six cats were parasitized with 7 species of trematodes with an overall prevalence of 12.77%. Recovered species were belonging to heterophyids (Heterophyes heterophyes, Pygidiopsis summa, Procerovum varium, Ascocotyle sp.), cyathocotylids (Prohemistomum vivax and Mesostephanus appendiculatus), and echinostomatid (Echinochasmus liliputanus) in prevalences of 6.38% (3/47), 2.13% (1/47), and 6.38% (3/47), respectively. Mixed infections with heterophyids were noticed in two infected cats. Meanwhile, a mixed infection with H. heterophyes and the echinostomatid was recorded in one cat. Moreover, all trematode-infected cats had concomitant infections with cestode and/or nematode parasites. Therefore, veterinarians and authorized agencies must consider great hygienic measures and sanitary control programs to avoid the potential risk and zoonotic importance of such parasites.