Potential Risk of Fish-Borne Nematode Infections in Humans in Brazil

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Food and Waterborne Parasitology 5 (2016) 1–6

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Food and Waterborne Parasitology

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Potential risk of ﬁsh-borne nematode infections in humans in Brazil – Current status based on a literature review

J.C. Eiras a,b,⁎,G.C.Pavanellic, R.M. Takemoto d,M.U.Yamaguchic,L.C.Karklingd,e,Y.Nawaf

a Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, Edifício FC4, 4169-007 Porto, Portugal b CIIMAR, Centro Interdisciplinar de Investigação Marinha e Ambiental, Porto, Portugal c Unicesumar, Programa de pós-graduação em Promoção da Saúde, Bloco 7, Avenida Guerner Dias, 1610 - Jardim Aclimação, Maringá, PR,87050-900, Brasil d UEM, Nupelia, Bloco G90, Av. Colombo, 5790 - zona 7, Maringá, PR CEP 87020-900, Brasil e UTFPR, Campus Dois Vizinhos, Estrada para Boa Esperança, Km 04, s/n, Comunidade de São Cristóvão, Dois Vizinhos, PR CEP 85660-000, Brazil f Tropical Diseases Research Center, Faculty of Medicine, Khon Kaen University, 123 Mitrapap Highway, Khon Kaen 40002, Thailand

article info abstract

Article history: A literature survey identified a variety of potentially zoonotic fish-borne nematode species in Received 22 May 2016 both marine and freshwater hosts which are common throughout Brazil. The few cases of Received in revised form 9 August 2016 fish-borne zoonotic nematodioses reported in humans in Brazil are summarized, and the Accepted 10 August 2016 possible routes of infection are discussed, such as the importance of restaurants specialized Available online 11 August 2016 in dishes containing raw or undercooked fish. The difficulties of diagnosing of human infections with fish-borne nematodes in Brazil are reviewed. Requirements for an integrated approach to Keywords: avoid the infection are discussed. It is concluded that, a) human fish-borne nematodiosis may Fish-borne nematodes constitute a problem of public health in Brazil; b) effective regulations to prevent the infection Human infection should be adopted; c) people must refrain from eating raw or undercooked fish dishes; and Zoonosis Public health d) an intensive campaign alerting people about the feeding risk behaviors shoul be undertaken. Brazil © 2016 The Authors. Published by Elsevier Inc. on behalf of International Association of Food and Waterborne Parasitology. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

1. Introduction

Fish borne nematodes infections in humans are common in countries where people have a traditional custom of consuming live, raw, smoked, lightly cooked or marinated fish and/or squid. This assumes that, i) the fish or squid must harbor infective stages of nematodes and, ii) they must be ingested in such conditions that live worms can reach the digestive tract of humans. Not only live worms but also dead worms can cause allergic reaction, sometimes with serious consequences including anaphylac- tic shock (Audicana et al., 2002). Several species of fish-borne nematodes are recognized as causative agents for human diseases: in the family Anisakidae; Anisakis, Pseudoterranova, Contracaecum and Hysterothylacium spp. are well known as human pathogens. In the family Gnathostomatidae, several Gnathostoma spp. are known to be infective to humans. In the family Capillariidae, Capillaria philippinensis is a fish-borne pathogen cappable of causing severe, sometimes fatal, diarrhea in the Philippines and Thailand, and sporadic cases have been reported from Taiwan, Japan and Korea (Cross and Belizario, 2007). In the family Dioctophymatidae, Eustrongylides spp. and Dioctophyme renale are fish-borne zoonotic nematodes rarely causing human disease.

⁎ Corresponding author at: Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, Edifício FC4, s/n, 4169-007 Porto, Portugal. E-mail addresses: [email protected] (J.C. Eiras), [email protected] (G.C. Pavanelli), [email protected] (R.M. Takemoto), [email protected] (M.U. Yamaguchi), [email protected] (L.C. Karkling), [email protected] (Y. Nawa).

http://dx.doi.org/10.1016/j.fawpar.2016.08.002 2405-6766/© 2016 The Authors. Published by Elsevier Inc. on behalf of International Association of Food and Waterborne Parasitology. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). 2 J.C. Eiras et al. / Food and Waterborne Parasitology 5 (2016) 1–6

Among those fish-borne nematodes, the most common species causing human infections are Anisakis spp., Pseudoterranova spp. and Gnathostoma spp., which are distributed worldwide (Arizono et al., 2011; Herman and Chiodini, 2009; Lamothe- Argumedo, 2006; Nawa et al., 2010; Torres et al., 2007). Infections with Hysterothylacium spp., Contracaecum spp., Eustrongylides spp. and Dioctophyme renale occur rarely and only a few cases have been described worldwide (Agrawal et al., 2014; Eberhard and Ruiz-Tiben, 2014; Ignatovic et al., 2003; Nagasawa, 2012; Yagi et al., 1996). In Brazil, little is known regarding human infections with fish-borne nematodes. Some publications discussed this issue by pointing out the possible risk of ingesting raw or undercooked fish (Cardia and Bresciani, 2012; Knoff et al., 2013; Lima dos Santos, 2010; Masson and Pinto, 1998; Okamura et al., 1999), or even dried or salted fish containing dead nematodes (Pereira et al., 2000; Prado and Capuano, 2006). Only few papers reported human infections with fish-borne nematodes (Amato Neto et al., 2007; Chaves et al., 2016; Dani et al., 2009; Eiras et al., 2015; Lisboa, 1945; Rosa da Cruz et al., 2010; Vargas et al., 2012). The fish diversity in Brazil, including both freshwater and marine species, is one of the richest in the world, especially concerning freshwater fish. According to Levêque et al. (2008), the Neotropical region has about 4050 species of fish, the majority of which are found in Brazil. Of marine fish, at least 1297 different species are distributed along the approximately 8500 km of Brazil's coastline (Menezes et al., 2003). The fish diversity is not a risk factor by itself for fish-borne nematode infections, and probably not all the species serve as hosts. However, the greater the number of fish species infected, especially in the case of economically important species, the greater the risk for humans of ingesting fish-infected nematodes. Taking into account these factors it is surprising that only a few cases of human infections with fish-borne nematodes have so far been reported in Brazil. This fact led the authors to produce the present study in order to clarify i) the existence of fish-borne nematodes with zoonotic potential in Brazil and the risk of infection with them, ii) the quantification of human infections known to date in Brazil, iii) the ability of physicians to diagnose human fishborne nematode infections and, iv) the general importance of this problem in the country, including the need for the adoption of effective prophylactic measures.

2. Materials and methods

The data presented here are based on a thorough bibliographical search. All the available faunistic lists were examined (Eiras et al., 2010; Luque et al., 2011; Moravec, 1998; Vicente et al., 1985; Vicente and Pinto, 1999) in order to detect reported fish infected with potentially zoonotic nematode species. Moreover, an electronic extensive bibliographical search was performed using several key words (fish nematodes, zoonosis, human health, Brazil, etc.) and several databases were searched (Web of Knowledge, Biological Abstracts and Helminthological Abstracts, Aquatic Science and Fisheries Abstracts). We successfully retrieve a large number of papers as shown in the results. These papers were too numerous to cite them all in the present work. The potential fish-borne zoonotic nematode species, the hosts (both freshwater and marine) and the sampling localities of the hosts are presented in Table 1. In addition, we extensively searched for the reports of human infection with fish-borne nematodes in Brazil. To the best of our knowledge, we identified all reported human cases of fish-borne nematode infections in Brazil.

3. Results

Fish-borne nematode parasites of zoonotic importance and respective fish hosts in Brazil are indicated in Table 1. Anisakis spp. were reported from 44 different host species, Pseudoterranova spp. from 16 hosts, Hysterothylacium spp. from 57 hosts, Eustrongylides spp. from 46 hosts, Contracaecum spp. from 89 hosts, Gnathostoma spp. from 2 hosts, and Dioctophyme renale from 3 hosts. The geographical distribution of the fish hosts species in both freshwater and marine environment is widely spread through the country's coastline and rivers belonging to almost all the hydrological basins. Moreover, the hosts include nearly all the economically important marine fish (Thunus thynus, Engraulis anchoita, Micropogonias furnieri, Pagrus pagrus, Scomber japonicus, Katsuwonus pelamis, Pomatomus saltatrix, etc.) and freshwater fish species (Pseudoplatystoma corruscans, P. fasciatum, Plagioscion squamosissimus, Salminus brasiliensis, Arapaima gigas, Cichla ocellaris, Piaractus mesopotamicus, etc.). Despite the infection of a large number of fish species with zoonotic nematodes the public health significance of this fact was not assessed. To reach definitive conclusions it would be necessary to take into account the intensity and prevalence of the infection for each species. However, the collected data demonstrate that zoonotic nematodes are not rare, as they occur in a large number of fish species. Therefore, it seems reasonable to classify infection of fish with zoonotic nematodes as “common” in Brazil. To date only a few cases fish-borne nematode infections in humans have been reported in Brazil. Dani et al. (2009) described the first case of gnathostomiosis in the country, and serological analysis suggested infection with the third stage larva of Gnathostoma binucleatum. However, this case involved a Brazilian patient who travelled to Peru and ate “Ceviche” three weeks before developing symptoms after having returned to Brazil. Therefore, this case seems to be an imported case in which a Brazilian was infected in Peru. A real autochthonous case of gnathostomiosis in Brazil was reported by Vargas et al. (2012).A man from Rio de Janeiro fishing in the Tocantins River caught a Cichla sp. fish and used it to prepare and consume “Sashimi”. Two weeks later he developed reddish lesions on his back, which disappeared after treatment with praziquantel. Later, the symptoms re-appeared and immunoblot analysis performed in Thailand showed positive antibody binding against Gnathostoma spinigerum antigen; since G. spinigerum is an Asian species of Gnathostoma and since G. spinigerum antigen can be used to diagnose G. binucleatum infection in Latin America (Nawa et al., 2015), this case appears to be the first indigenous case of gnathostomosis in Brazil. Recently, Chaves et al. (2016) reported a case of ocular gnathostomosis in Brazil. Several reports of possible gnathostomosis have appeared on internet-based descriptions by sport fishermen. Despite the convincing description of the symptoms and the epidemiological data strongly suggesting infection with Gnathostoma spp., these anecdotal reports were not J.C. Eiras et al. / Food and Waterborne Parasitology 5 (2016) 1–6 3

Table 1 Fish infecting nematodes with zoonotic potential in Brazil: parasite species and fish hosts. Marine fish were caught along the entire country's coastline. Freshwater fish were caught in rivers belonging to almost all the hydrological basins.

Zoonotic nematode spp. Fish hosts

Anisakis pegrefﬁi Campana-Rouget & Biocca, Thunnus thynnus 1955 (larva) Anisakis physeteris (Baylis, 1923) (larva) Auxis thazard, Genypterus blacodes Anisakis simplex (Rudolphi, 1809) (sensu lato) Cynoscion guatucupa, Engraulis anchoita, Genypterus blacodes, Lophius gastrophysus, Paralichthys isosceles, (larva) Trachurus lathami Anisakis typica (Diesing, 1860) (larva) Auxis thazard, Thunnus thynnus, Trichiurus lepturus Anisakis sp. (larva) Aluterus monoceros, Bagre bagre, Balistes vetula, Brevoortia aurea, Caranx latus, Carcharhinus signatus, Coryphaena hippurus, Cynoscion guatucupa, Cynoscion sp., Dipturus trachyderma, Euthynnus alleteratus, Galeorhinus galeus, Genypterus blacodes, Heptranchias perlo, Hexanchus griseus, Katsuwonus pelamis, Lutjanus compechanus, Macrodon ancylodon, Merluccius hubbsi, Micropogonias furnieri, Mullus argentinae, Mustelus canis, Nebris microps, Pagrus pagrus, Paralichthys isosceles, Percophis brasiliensis, Pomatomus saltatrix, Priacanthus arenatus , Prionotus punctatus, Pseudopercis numida, Scomber japonicus, S. scombrus, Scomberomorus cavalla, Selene setapinnis, Sphyraena guachancho, Squalus megalops, Trichiurus lepturus, Urophycis mystacea Anisakis sp. larva type I sensu Berland (1961) Katsuwonus pelamis, Lophius gastrophysus Anisakis sp. larva type II sensu Berland (1961) Katswonus pelamis Pseudoterranova decipiens (Krabbe, 1878) Genypterus blacodes (sensu lato) (larva) Pseudoterranova sp. (larva) Caranx hippos, C. latus, Cynoscion sp., Galeorhinus galeus, Genypterus blacodes, Macrodon ancylodon, Micropogonias furnieri, Mustelus canis, M. schmitti, Pagrus pagrus, Pomatomus saltatrix, Priacanthus arenatus, Scomber japonicus, Squalus megalops, Trichiurus lepturus, Tylosurus acus Contracaecum sp. (larva) Acestrorhampus macrolepis, Acestrorhynchus lacustris, Aluterus monoceros, Astronotus ocellatus, Astyanax altiparanae, A. bimaculatus, A. fasciatus, A. schubarti, Auchenipterus osteomystax, Bergiaria sp., Balistes capriscus, B. vetula, Brevoortia aurea, Brycon hilarii, Caranx hippos, C. latus, Carcharhinus brachyurus, C. signatus, Centropomus undecimalis, Cephalopholis fulva, Cichla kelberi, C. monoculus, C. piquiti, C. ocellaris, Crenicichla haroldoi, C. lepidota, Cyphocharax modestus, C. nagelii, Cynoscion striatus, Cynoscion sp., Dactylopterus volitans, Diapterus rhombeus, Dipturus trachyderma, Euthynnus alletteratus, Galeocharax humeralis, G. knerii, Galeorhinus galeus, Genidens barbus, Genypterus blacodes, Geophagus brasiliensis, Gymnotus carapo, Gymnotus sp., Heptranchias perlo, Hemisorubim platyrhynchos, Hexanchus griseus, Hoplerythrinus unitaeniatus, Hoplias malabaricus, Iheringichthys labrosus, Leporinus friderici, L. lacustris, Lophius astrophysus, Loricariichthys castaneus, Macrodon ancylodon, Markiana geayi, Menticirrhus americanus, Metynnis lippincottianus, Micropogonias furnieri, Moenkhausia sanctaeﬁlomenae, Mullus argentinae, Oligosarcus paranensis, Oligosarcus sp., Pachyurus bonariensis, P. ternetzi, Pagrus pagrus, Paralichthys isosceles, Paralonchurus brasiliensis, Parona signata, Zungaro zungaro, Pimelodus ortmanni, P. pohli, Plagioscion squamosissimus, Pomatomus saltatrix, Priacanthus arenatus, Prochilodus lineatus, Psellogrammus kennedyi, Pseudoplatystoma corruscans, P. fasciatum, Pirinampus pirinampu, Pygocentrus nattereri, Raphiodon vulpinus, Rhamdia quelen, Salminus brasiliensis, Serrasalmus marginatus, Tetragonopterus argenteus, Trachelyopterus striatulus, Trachurus lathami, Trichiurus lepturus, Urophycis brasiliensis, U. mystacea. Hysterothylacium deardorffoverstreetorum Cynoscion guatucupa, Paralichthys isosceles Knoff et al., 2012 Hysterothylacium eurycheilum (Olsen, 1952) Epinephelus guttatus Deardorff & Overstreet, 1981 Hysterothylacium fortalezae (Klein, 1973) Harengula clupeola, Scomberomorus brasiliensis, S. cavalla, S. maculatus Deardorff & Overstreet, 1981 Hysterothylacium sp. Anchoa marinii, A. tricolor, Archosargus rhomboidalis, Balistes vetula, Caranx latus, Ctenosciaena gracilicirrhus, Cichla kelberi, Crenicichla lepidota, Cynoscion guatucupa, Dactylopterus volitans, Galeocharax knerii, Genidens barbus, Genypterus blacodes, Gymnotus carapo, Gymnotus sp., Gymnothorax moringa, Hypophthalmus edentatus, Leporinus friderici, Lophius gastrophysus, Loricarichthys sp., Lutjanus analis, Macrodon ancylodon, Menticirrhus americanus, Merluccius hubbsi, Micropogonias furnieri, Mugil liza, Pagrus pagrus, Paralichthys isosceles, Parona signata, Peprilus paru, Percophis brasiliensis, Pinguipes brasilianus, Plagioscion squamosissimus, Prionotus punctatus, Pseudopercis numida, P. semifasciata, Pterodoras granulosus, Rhaphiodon vulpinus, Salminus brasiliensis, Scomber japonicus, S. scombrus, Selene setapinnis, Tetragonopterus chalceus, Trachelyopterus striatus, Trachurus lathami, Trichiurus lepturus, Tylosurus acus acus, Umbrina canosai, Uraspis secunda, Urophycis brasiliensis, U. mystacea Eustrongylides ignotus Jägerskiöld, 1909 (larva) Auchenipterus nigripinnis, Brycon hilarii, Galeocharax humeralis, Hemisorubim platyrhynchus, Hoplias malabaricus, Hoplias sp., Paratrygon sp., Pirinampus pirinrampu, Pseudoplatystoma corruscans, P. fasciatus, Pygocentrus nattereri, Raphiodon vulpinus, Salminus brasiliensis, Serrasalmus maculatus, S. marginatus, S. nattereri, S. spilopleura, Synbranchus laticaudatus, S. marmoratus. Eustrongylides sp. (larva) Acestrorhynchus lacustris, Arapaima gigas, Auchenipterus nigripinnis, Brycon hilarii, B. microlepis, Callichthys callichthys, Calophysus macropterus, Charax gibbosus, Cichla kelberi, C. monoculus, C. ocellaris, C. piquiti, Galeocharax humeralis, Gymnotus carapo, Hoplerythrinus unitaeniatus, Hoplias malabaricus, Leporellus vittatus, Leporinus copelandii, L. obtusidens, Lepthoplosternum pectorale, Oligosarcus sp., Paratrygon sp., Piaractus mesopotamicus, Pimelodus maculatus, Pirinampus pirinampu, Plagioscion squamosissimus, Pseudoplatystoma corruscans, P. fasciatum, Pseudoplatystoma sp., Pygocentrus nattereri, Raphiodon vulpinus, Salminus brasiliensis, Serrasalmus marmoratus, S. nattereri, Steindachneridion parahybae, Synbranchus marmoratus

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Table 1 (continued)

Zoonotic nematode spp. Fish hosts

Gnathostoma gracile Diesing, 1839 (larva) Arapaima gigas G. spinigerum Owen, 1836 (larva) Cichla sp. Dioctophyme renale Goese, 1782 Acestrorhynchus lacustris, Gymnotus silvius, Hoplosternum littorale confirmed by parasitological examination and cannot be accepted as cases of gnathostomosis. Human infection with dog hook- worms manifest skin lesions similar to those caused by Gnathosotoma and should be considered in differential diagnosis. Amato Neto et al. (2007) reported a group of possible cases of anisakidosis acquired by sport fishermen at Ilha do Bananal, Tocantins River. However, as was pointed out by Eiras et al. (2015), the fishermen ate “Sashimi” made from the freshwater Cichlidae fish which is unable to harbor marine parasites Anisakis sp. or Pseudoterranova sp. In addition, clinical features of the patients were not characteristic of anisakidosis, but rather have some similarities with the early stage of infection with Gnathostoma sp. (Herman and Chiodini, 2009). Until now, there is only one reliable description of an anisakidosis case in Brazil (Rosa da Cruz et al., 2010), involving a patient who had possibly eaten raw fish in a trip to Bahia State before developing epigastric pain, and early satiety. Endoscopic examination of the duodenum revealed inflamed mucosa and the presence of a 1.5 cm length larva which was removed by endoscopy. The worm was identified as an anisakid species. In Brazil there is only a single case report of infection with the zoonotic nematode Dioctophyme renale (giant kidney worm); the report describes infection of a female patient with D. renale in São Luís-MA (Lisboa, 1945).

4. Discussion

According to the data obtained from the literature there are only five human cases of fish-borne nematodosis in Brazil: two confirmed reports and one probable with Gnathostoma species (plus one imported case), one case with Anisakis sp., and one case with Dioctophyme renale. This number seems to be unrealistic when compared with the number of marine and freshwater fish species harbouring zoonotic nematodes (see Table 1). Many other species of fish may also serve as hosts for zoonotic nematode species. We, therefore, agree with the opinion of the European Food Safety Authorithy (EFSA), which states: “All wild caught seawater and freshwater fish must be considered at risk of containing any viable parasites of human health concern if these products are to be eaten raw or almost raw” and “For wild-caught fish, no sea fishing grounds can be considered free of A. simplex” (EFSA, 2010). These EFSA statements are based largely on observations of a high number of species worldwide, which were supported by multiple strong and irrefutable evidences. We believe that all fish species should be considered as potential sources of dangerous zoonotic nematodes, and should be processed properly for human consumption. Special attention is required for the possible infection with fishborne zoonotic nematodes in restaurants where fish are served raw or undercooked as traditional/ethnic recipies like “Sushi”, “Sashimi”, “Ceviche” and other extraordinary dishes originating from Asian countries. The number of ethnic/Asian restaurants has increased several folds worldwide in the last years, and are regarded as “fashionable” in many countries. A parasitological examination revealed the presence of high occurrence of zoonotic nematodes in such dishes (Torres-Frenzel and Torres, 2014). A direct relationship between the consumption of these dishes and the infection of humans with fish-borne nematodes has been reported repeatedly (Couture et al., 2003; Hochberg and Hamer, 2010; Jofré et al., 2008; Just et al., 2008; Nawa et al., 2005). In Brazil, in particular, it is obvious that the number of “Sushi” restaurants is increasing, mostly in the large cities. In São Paulo, the largest city in Brazil and in South America, having about 11 mil- lions inhabitants, there are approximately 600 “Sushi” restaurants (more than the traditional “rodízio” meat restaurants!) and about 400,000 individual portions of “Sushi” are produced per day. According to internet-based data (http://economia.uol.com. br/noticias/redacao/2013/06/28/franquias-de-comida-oriental-faturam-r-400-milhoes-em-um-ano-veja-opcoes.htm) the number of “Sushi” restaurants in the city increased by 9% from 2011 to 2012, and 17% from 2012 to 2013. We estimate that in Brazil there are probably about 11,000 “Sushi” restaurants. A huge variety of fish species are used to prepare “Sushi”. Some are especially valued like the bluefin tuna, big-eye tuna, yellowfin tuna, red snapper, Japanese yellowtail and salmon, which are commonly used for “Sushi”, and the majority of these can be found in Brazilian waters. However, many more species are used, including freshwater fish primarily in places that far from the sea. Another potential way of contamination is the consumption of “Ceviche”, the traditional recipe of Peru, prepared with raw fish marinated in citrus juice. We did not find detailed information about “Ceviche” restaurants in Brazil as was available for “Sushi”, but an internet search for “Ceviche ” specialized restaurants in the largest Brazilian cities surprisingly revealed the existence of a huge number of Peruvian restaurants specialized in “Ceviche” dishes. Like “Sushi” restaurants, it is generally assumed that people frequenting “Ceviche” restaurants are young and middle-aged people with higher than average economic power. We believe that the number of human infections in Brazil is probably much higher than generally presumed, and several concurrent factors may contribute to this. One important factor relates to the apparent lack of training in fish-borne disesases for physicians. Information obtained from a number of physicians, some of whom were teachers in university medical courses, lead to the conclusion that these aspects of training are not adequately covered during their medical education in Brazil (Cardia and Bresciani, 2012). Also, because of the scarcity of reported cases of human infections in Brazil, physicians seem to have little knowledge or experience on the symptomatology of infection in humans with the different kinds of fish-borne parasites, which may lead to misdiagnosis of the cases of infection (Okamura et al., 1999). Furthermore, the symptoms of some J.C. Eiras et al. / Food and Waterborne Parasitology 5 (2016) 1–6 5 cases of fish-borne nematodiases are similar to those of other conditions of different etiology, resulting in underestimation of fish- borne nematode infections. For instance, gastric anisakiasis may be confused with peptic ulcer or gastritis; the intestinal location of the parasites may mimic appendicitis, ileitis, diverticulitis, or even colonic tumour (Seguchi et al., 1995) among other diseases. Extra- intestinal location can be confused with acute peritonitis, tuberculous peritonitis, and pancreatic cancer. For detailed information on clinical features, diagnosis, pathological findings and treatment of fish-borne nematodiosis see Limbery and Cheah (2007) and Nawa et al. (2015). It is obvious that avoiding dishes containing raw, marinated or undercooked fish would avoid human infections with fish- borne nematodes. However, such a goal is obviously impossible to reach in numerous countries due to strong traditions. Further- more, the introduction of dishes, like “Sushi”, “Sashimi” or “Ceviche” in countries such as Brazil where they were not traditionally eaten, increased markedly in the last years. Therefore, the fight against infection with fish-borne nematodes should integrate several different measures including mass education about the risks of consuming raw fish to the people living in non-endemic or low risk-areas. The great majority of people in Brazil are not aware of this public health risk. A number of procedures may reduce greatly the risk of ingesting fish-borne nematodes. It is well known that Anisakis spp. migrate from the viscera to the muscle after the death of some species of the fish host (Cipriani et al., 2016; Silva and Eiras, 2003; Smith, 1984; Smith and Wootten, 1975; Tantanasi et al., 2012). Therefore, evisceration of the specimens immediately or shortly after catching is highly recommended. However, it is recognized that this procedure is difficult or even impossible to im- plement when fishermen are dealing with thousands of specimens. One way to detect infected fish is the examination of fillets by candling on a light table, but again this procedure is not very effective, even though it has been used commonly worldwide, with only 33% of heavily infected fish sometimes being detected (McClelland, 2002). The most efficient ways of preventing infections are the procedures advised by the US Food and Drug Administration (FDA) for treating raw fish: e.g. storing at temperature of −20 °C or lower for 7 days (total time) or −35 °C or lower for 15 h; (US FDA, 2011). These procedures may not be suitable for freezing large fish (e.g., thicker than 6 in.). It may be necessary to experimentally determine effective control parameters specific for freezing method, fish thickness, fish species, method of preparation, and target parasites (US FDA, 2011). Brining and pickling may also be used to control fish-borne nematodes. Here, the most important factor is the salt level of the brining or pickling solution, and duration necessary to kill the nematodes; for detailed information about these procedures see Adams et al. (1997). Following destruction of the worms by these measures the fish may be consumed raw or undercooked without risk of infection. If the untreated fish are not intended to be eaten raw, a cooking temperature of 60 °C for at least 10 min prevents infection. The website https://www.food.gov.uk/business-industry/fish-shellfish/freezing- requirement-guidance also provides useful information for the control of fish-borne nematode infection. In Brazil, the legislation related to prevention of infection is not very detailed. The rules concerning fish inspection state that the fish may be frozen at −25 °C and then must be kept at −15 °C, but the time of freezing at −25 °C is not defined. Therefore, the freezing of the potentially fish may not be enough for killing the parasites. Furthermore, specific legislation concerning fish- borne nematodes apparently do not exist in the country. In summary, it is concluded that:

i). in Brazil both marine and freshwater fish may be commonly infected with potentially zoonotic nematodes, and it is assumed that all the species of fish could be infected with such parasites. Therefore, the risk of ingesting zoonotic nematodes when eating raw or undercooked fish is considered high, and may constitute a public health problem. ii). the five cases of human fish-borne infection described within the country so far is extremely low, and it is believed that the real number of cases is probably much higher, in part due to the difficulty of diagnosis by physicians who are not familiar with the symptoms of the infection which frequently mimic conditions caused by other etiological agents. Therefore, improvement of the knowledge of physicians about this kind of zoonosis is particularly important. iii). consumers should refrain of eating, raw, undercooked or marinated fish, and should be educated about the risks of eating raw or undercooked fish, including those prepared as “Sushi”, “Sashimi”, “Ceviche”, and similar dishes.

Acknowledgements

This paper was supported by MEC/MCTI/CAPES/CNPq/FAPS. Participation of JC Eiras was partially supported by the European Regional Development Fund (ERDF) through the COMPETE – Operational Competitiveness Programme and national funds through FCT – Foundation for Science and Technology, under the project “Pest-C/MAR/LA0015/2011”, and by Cesumar (Centro Universitário Cesumar). The authors are grateful to the Editor whose comments and suggestions contributed to the improvement of the paper.

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