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Journals
Pathogens
Special Issues
Tackling Foodborne Parasitic Infections
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Tackling Foodborne Parasitic Infections

A special issue of Pathogens (ISSN 2076-0817). This special issue belongs to the section "Parasitic Pathogens".

Deadline for manuscript submissions: closed (31 October 2020) | Viewed by 21242

Special Issue Editors

Prof. Dr. Sarah Gabriël

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Guest Editor
Department of Veterinary Public Health and Food Safety, Faculty of Veterinary Medicine, Ghent University
Interests: foodborne parasites; veterinary public health; Taenia spp; Anisakidae; Sarcocystis spp.
Prof. Dr. Pierre Dorny

E-Mail Website
Guest Editor
Institute of Tropical Medicine, Department of Biomedical Sciences, Veterinary Helminthology Unit
Interests: zoonotic parasites; tropical veterinary medicine; diagnosis; epidemiology

Special Issue Information

Dear colleagues,

Though a substantial amount of research efforts has focussed on foodborne hazards, foodborne parasitic infections have been largely neglected. While foodborne parasitic infections have drastically decreased in industrialised countries as a result of improved sanitation and hygiene, they still persist in many developing countries, often due to poverty-related factors. In addition, human migration/travel and globalization of the food industry have the potential to increase the risk for re-introducing foodborne parasitic infections. Such changes include increased human migration/travel, whereby people are more exposed to exotic pathogens. They may get infected in endemic areas but develop clinical symptoms only upon returning to their home countries/travelling to non-endemic areas (e.g., neurocysticercosis), or get infected and transmit the infection to other people when returning/travelling to non-endemic areas. Increased international trade, transportation and distribution systems have increased the importation of food products from endemic areas. This, in combination with changes in culinary habits towards more raw food consumption, has increased exposure to otherwise exotic parasites. Climate changes have altered the distribution or suitability of intermediate hosts, allowing parasites to establish in new areas. In addition, the growing demand for animal/fish proteins globally has resulted in increased importation of animal/fish products in the developed world and intensification of production in developing countries, often under suboptimal food safety standards. The latter is in contrast with the trend towards more organic farming in the EU, allowing animals more outside access and, as such, more potential exposure to foodborne parasitic infections. Overall, these changes will lead to a global increase in human and animal cases of foodborne parasitic infections. Still, the lack of adequate systems for routine diagnosis, monitoring, and reporting in the veterinary and medical sectors, combined with a scarcity of active knowledge has led to the under-recognition and under-reporting of foodborne parasites. Tackling these challenges will require multidisciplinary inputs, including efforts from the scientific community to increase knowledge on disease occurrence and risk factors, novel insights into diagnostics and control/prevention, and the development of monitoring and surveillance systems that are applicable to endemic areas and non-endemic, at risk areas.

Prof. Dr. Sarah Gabriël
Prof. Dr. Pierre Dorny
Guest Editors

Manuscript Submission Information

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Keywords

  • foodborne parasites
  • diagnostics
  • control
  • global changes

Published Papers (7 papers)

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Research

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10 pages, 5862 KiB  
Article
Occurrence of Echinococcusgranulosussensulato and Other Taeniids in Bhutan
by Puspa M. Sharma, Nirmal K. Thapa, Pema Tshomo, Tshewang Dema, Cristian A. Alvarez Rojas, Tenzin Tenzin, Ratna B. Gurung, Tshering Norbu, Lhatru Lhatru, Phurpa Namgyel, Chimi Jamtsho, Kinzang Dukpa, Yoenten Phuentshok, Krishna P. Sharma, Sonam Pelden and Peter Deplazes
Pathogens 2021, 10(3), 330; https://doi.org/10.3390/pathogens10030330 - 11 Mar 2021
Cited by 3 | Viewed by 2423
Abstract
The present research shows the results of a national study documenting the occurrence and genetic diversity of Echinococcus and Taenia species across Bhutan. Environmental dog faecal samples (n = 953) were collected from 2016 to 2018 in all 20 Bhutanese districts, mainly in [...] Read more.
The present research shows the results of a national study documenting the occurrence and genetic diversity of Echinococcus and Taenia species across Bhutan. Environmental dog faecal samples (n = 953) were collected from 2016 to 2018 in all 20 Bhutanese districts, mainly in urbanised areas. Cystic echinococcosis cysts were isolated from 13 humans and one mithun (Bos frontalis). Isolation of taeniid eggs from faeces was performed by sieving/flotation technique, followed by DNA isolation, PCR and sequence analyses for species identification (gene target: small subunit of ribosomal RNA). Genetic diversity of E. granulosuss.s. was based on the sequence (1609 bp) of the cox1 gene. A total of 67 out of 953 (7%) dog faecal samples were positive for at least one taeniid species. From the 670 free-roaming dog faecal samples, 40 (5.9%) were positive for taeniid DNA, 22 (3.2%) of them were identified as E. granulosuss.s. and four (0.5%) as E. ortleppi (G5). From the 283 faecal samples originating from yak-grazing areas, 27 (9.5%) were taeniid positive, including eight (2.8%) infected with E. granulosuss.s. and four (1.4%) with E. ortleppi. E. granulosuss.s. was identified in all isolates from human and the cyst from mithun. A haplotype network (cox1 gene) from E. granulosuss.s, including isolates from 12 dogs, two human and one mithun, revealed eight different haplotypes. The most common cox1 haplotype was the globally distributed Eg01, followed by Eg40 and Eg37 (previously described in China). Five new cox1 haplotypes (EgBhu1–5) originated from human, dogs, and a mithun were identified. The study indicated the contamination of urban areas and pastures with Echinococcus eggs in seven districts in Bhutan. The molecular characterisation of E. granulosuss.l. revealed different E. granulosuss.s. haplotypes as well as E. ortleppi. The transmission of T. multiceps was documented only in the western part of the country. Considering the zoonotic feature of E. granulosus s.s. and E. ortleppi and the economic impact of coenurosis caused by T. multiceps (also known as gid) in Bhutan, the findings of this study represent a significant contribution towards an epidemiological baseline for the establishment of a national control programme. Full article
(This article belongs to the Special Issue Tackling Foodborne Parasitic Infections)
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13 pages, 1960 KiB  
Article
Correlation of NHR-48 Transcriptional Modulator Expression with Selected CYP Genes’ Expression during Thiabendazole Treatment of Anisakis simplex (s.l.)?—An In Vitro Study
by Elżbieta Łopieńska-Biernat, Robert Stryiński, Łukasz Paukszto and Jan P. Jastrzębski
Pathogens 2020, 9(12), 1030; https://doi.org/10.3390/pathogens9121030 - 09 Dec 2020
Cited by 1 | Viewed by 1892
Abstract
Anisakis simplex (s.l.) is a complex of three sibling (biological) species of parasitic nematodes of marine mammals, including A. berlandi, A. pegreffii and A. simplex (s.s.). It is characterized by a complex life cycle in which humans can become accidental hosts by [...] Read more.
Anisakis simplex (s.l.) is a complex of three sibling (biological) species of parasitic nematodes of marine mammals, including A. berlandi, A. pegreffii and A. simplex (s.s.). It is characterized by a complex life cycle in which humans can become accidental hosts by consuming dishes made of raw or undercooked fish containing L3 larvae, which in many regions of the world is related to the national or regional culinary tradition. This has spurred scientific efforts to develop new methods for treating the disease, called anisakiasis, and to neutralize invasive L3. Thiabendazole (TBZ) is a wide-spectrum anthelminthic with a higher efficacy than albendazole, a drug whose long-term use induces resistance in many parasitic species. Cytochromes P450 participate in TBZ metabolism, and the expression of their genes is controlled by nuclear hormone receptors (NHR). This study aimed to examine the effects of TBZ on the above-described pathway in invasive larvae of A. simplex (s.l.). The efficacy of TBZ against A. simplex (s.l.) larvae was observed for the first time. Larvae were cultured in vitro for 72 h in a medium containing TBZ at five concentrations from 0.5 to 1.5 mM. However, the survival curves did not significantly differ from each other. This means that all of the concentrations of TBZ had a similar effect on the A. simplex (s.l.) L3 larvae during in vitro culture. Nevertheless, TBZ modified the expression of nhr-48, cyp13a3 and cyp1a1 genes in the L3 of A. simplex (s.l.). Full article
(This article belongs to the Special Issue Tackling Foodborne Parasitic Infections)
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18 pages, 3078 KiB  
Article
Development and Application of Novel Chemiluminescence Immunoassays for Highly Sensitive Detection of Anisakis simplex Proteins in Thermally Processed Seafood
by Maciej Kochanowski, Mirosław Różycki, Joanna Dąbrowska, Jacek Karamon, Jacek Sroka, Ewelina Antolak, Aneta Bełcik and Tomasz Cencek
Pathogens 2020, 9(10), 777; https://doi.org/10.3390/pathogens9100777 - 23 Sep 2020
Cited by 3 | Viewed by 2737
Abstract
The third-stage larvae (L3) of Anisakis simplex are the most important source of hidden allergens in seafood products. However, there exist no commercial methods for detecting Anisakis proteins in food. Furthermore, only a few methods have been validated for the detection of A. [...] Read more.
The third-stage larvae (L3) of Anisakis simplex are the most important source of hidden allergens in seafood products. However, there exist no commercial methods for detecting Anisakis proteins in food. Furthermore, only a few methods have been validated for the detection of A. simplex in thermally processed food. The aims of our study are (i) the development and validation of high-sensitivity chemiluminescent (CL) immunoassays for the detection of A. simplex proteins in processed seafood, (ii) and A. simplex antigen detection in common seafood products from Polish markets. We developed and validated CL sandwich ELISA (S-ELISA) and CL competitive ELISA (C-ELISA) methods for A. simplex proteins detection in food, with respective detection limits of 0.5 and 5 ng/mL. The usefulness of the assays for detecting A. simplex proteins in highly processed food was evaluated by examination of autoclaved canned fish spiked with A. simplex larvae (1–8 larvae/200 g). Commercial real-time PCR was unable to detect A. simplex in autoclaved samples at all levels of enrichment with Anisakis larvae. CL-S-ELISA was used to test various types of seafood products from Polish markets. Among all tested products (n = 259), 28% were positive. A. simplex antigens were found mostly (n = 39) in smoked fish products: mackerel, herring, cod, and hake. Other positive samples were found in marinated herrings, canned cod livers, canned mackerels, and surimi sticks. In tuna, Atlantic argentine, anchovy, sardine, sprat, and squid products, A. simplex antigens were not detected. This study provides novel effective tools for the detection of A. simplex proteins in processed food and highlights the potential allergic hazards for Anisakis-sensitized Polish consumers of seafood. Full article
(This article belongs to the Special Issue Tackling Foodborne Parasitic Infections)
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15 pages, 610 KiB  
Article
A Sensitive, One-Way Sequential Sieving Method to Isolate Helminths’ Eggs and Protozoal Oocysts from Lettuce for Genetic Identification
by Annina R. Guggisberg, Cristian A. Alvarez Rojas, Philipp A. Kronenberg, Nadia Miranda and Peter Deplazes
Pathogens 2020, 9(8), 624; https://doi.org/10.3390/pathogens9080624 - 31 Jul 2020
Cited by 19 | Viewed by 3732
Abstract
Different helminths and protozoa are transmitted to humans by oral uptake of environmentally resistant parasite stages after hand-to-mouth contact or by contaminated food and water. The aim of this study was to develop and validate a method for the simultaneous detection of parasite [...] Read more.
Different helminths and protozoa are transmitted to humans by oral uptake of environmentally resistant parasite stages after hand-to-mouth contact or by contaminated food and water. The aim of this study was to develop and validate a method for the simultaneous detection of parasite stages from fresh produce (lettuce) by a one-way isolation test kit followed by genetic identification (PCR, sequencing). Three sentinel zoonotic agents (eggs of Toxocara canis, Echinococcus multilocularis and oocysts of Toxoplasma gondii) were used to investigate the practicability and sensitivity of the method. The detection limits (100% positive results) in the recovery experiments were four Toxocara eggs, two E. multilocularis eggs and 18 T. gondii oocysts (in 4/5 replicates). In a field study, helminth DNA was detected in 14 of 157 lettuce samples including Hydatigera taeniaeformis (Syn. Taenia taeniaeformis) (four samples), T. polyacantha (three), T. martis (one), E. multilocularis (two) and Toxocara cati (four). Toxoplasma gondii was detected in six of 100 samples. In vivo testing in mice resulted in metacestode growth in all animals injected with 40–60 E. multilocularis eggs, while infection rates were 20–40% with 2–20 eggs. The developed diagnostic strategy is highly sensitive for the isolation and genetic characterisation of a broad range of parasite stages from lettuce, whereas the sensitivity of the viability tests needs further improvement. Full article
(This article belongs to the Special Issue Tackling Foodborne Parasitic Infections)
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12 pages, 382 KiB  
Communication
Molecular Characterization of Echinococcus granulosus sensu lato from Humans in Slovenia
by Barbara Šoba, Špela Gašperšič, Darja Keše and Tadeja Kotar
Pathogens 2020, 9(7), 562; https://doi.org/10.3390/pathogens9070562 - 12 Jul 2020
Cited by 12 | Viewed by 2687
Abstract
The larval form of tapeworms of the Echinococcus granulosus sensu lato species cluster cause an important zoonotic infection, cystic echinococcosis (CE). Molecular characterization of the cluster’s isolates from different hosts greatly contributes to a better understanding of its transmission dynamics. To date, no [...] Read more.
The larval form of tapeworms of the Echinococcus granulosus sensu lato species cluster cause an important zoonotic infection, cystic echinococcosis (CE). Molecular characterization of the cluster’s isolates from different hosts greatly contributes to a better understanding of its transmission dynamics. To date, no genetic information is available on CE in Slovenia. In this work, we characterized isolates from human CE cases. Parasite samples from 18 patients were collected, together with the patients’ demographic and clinical data. Genomic DNA was analyzed by conventional PCR and sequencing at four mitochondrial loci (cytochrome c oxidase subunit 1, cox1; NADH dehydrogenase subunit 1, nad1; NADH dehydrogenase subunit 5, nad5; and small ribosomal RNA, rrnS). Thirteen isolates were successfully amplified and sequenced. Seven (58.8%) patients were infected with E. granulosus sensu stricto (s.s.) G1, five (38.5%) with E. canadensis G7 and one (7.7%) with E. granulosus s.s. G3. Echinococcus canadensis G7, the pig genotype, was identified exclusively in autochthonous Slovenes, while the patients originating from the Western Balkans were all infected with E. granulosus s.s. Our findings suggest that pigs are important intermediate hosts for human CE in Slovenia. Full article
(This article belongs to the Special Issue Tackling Foodborne Parasitic Infections)
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Review

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33 pages, 1181 KiB  
Review
Currently Available Monitoring and Surveillance Systems for Taenia spp., Echinococcus spp., Schistosoma spp., and Soil-Transmitted Helminths at the Control/Elimination Stage: A Systematic Review
by Ganna Saelens and Sarah Gabriël
Pathogens 2020, 9(1), 47; https://doi.org/10.3390/pathogens9010047 - 06 Jan 2020
Cited by 4 | Viewed by 5030
Abstract
An increasing global focus on neglected tropical diseases (NTDs) has resulted in the set up of numerous control and elimination activities worldwide. This is partly true for Taenia solium taeniasis/cysticercosis, the most important foodborne parasitic infection. Despite substantial progress, adequate monitoring and surveillance [...] Read more.
An increasing global focus on neglected tropical diseases (NTDs) has resulted in the set up of numerous control and elimination activities worldwide. This is partly true for Taenia solium taeniasis/cysticercosis, the most important foodborne parasitic infection. Despite substantial progress, adequate monitoring and surveillance (M&S) are required to sustain a status of control/elimination. This is often lacking, especially for T. solium. Therefore, the objective was to conduct a systematic literature review of the currently available M&S systems at the control/elimination stage of the four top-ranked helminth NTDs. Specifically, Taenia spp., Echinococcus spp., Schistosoma spp., and soil-transmitted helminths (STHs) were considered to determine if there are any similarities between their M&S systems and whether certain approaches can be adopted from each other. The systematic review demonstrated that rigorous M&S systems have been designed for the control/elimination stage of both STHs and schistosomiasis, particularly in China. On the other hand, a concept of M&S for Taenia spp. and Echinococcus spp. has not been fully developed yet, due to a lack of epidemiological data and the fact that many endemic countries are far away from reaching control/elimination. Moreover, accurate diagnostic tools for all four diseases are still imperfect, which complicates proper M&S. Finally, there is an urgent need to develop and harmonize/standardize M&S activities in order to reliably determine and compare the epidemiological situation worldwide. Full article
(This article belongs to the Special Issue Tackling Foodborne Parasitic Infections)
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Other

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5 pages, 214 KiB  
Brief Report
No Confirmed Cases of Taenia solium Taeniasis in a Group of Recently Arrived Sub-Saharan Migrants to Italy
by Lorenzo Zammarchi, Marta Tilli, Antonia Mantella, Annarita Botta, Alessandra Nicoletti, Héctor Hugo García, Yesenia Castillo, Donatella Aquilini, Sara Boccalini and Alessandro Bartoloni
Pathogens 2019, 8(4), 296; https://doi.org/10.3390/pathogens8040296 - 14 Dec 2019
Cited by 3 | Viewed by 2115
Abstract
One-hundred and sixty-four migrants from Sub-Saharan Africa to Italy were screened with the Taenia solium specific enzyme-linked immunosorbent assay coproantigen (ELISA CoAg) and four (2.4%) were recorded as positive, but with optical density values near to the cut-off. No ELISA CoAg positive samples [...] Read more.
One-hundred and sixty-four migrants from Sub-Saharan Africa to Italy were screened with the Taenia solium specific enzyme-linked immunosorbent assay coproantigen (ELISA CoAg) and four (2.4%) were recorded as positive, but with optical density values near to the cut-off. No ELISA CoAg positive samples were confirmed by parasitological methods. Low positivity could be attributed to false positive result or cross-reaction with other Taenia species. Further studies are needed to assess the role of migration on sporadic autochthonous transmission of T. solium taeniasis/cysticercosis in Europe. Full article
(This article belongs to the Special Issue Tackling Foodborne Parasitic Infections)
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