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Fish-borne nematodiases in South America: neglected emerging diseases

Published online by Cambridge University Press:  25 October 2017

J.C. Eiras ,
G.C. Pavanelli ,
R.M. Takemoto  and
Y. Nawa
J.C. Eiras
Affiliation:
Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Portugal and Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR/CIMAR), Matosinhos, Portugal
G.C. Pavanelli
Affiliation:
Unicesumar, Programa de pós-graduação em Promoção da Saúde, Maringá, Brasil
R.M. Takemoto*
Affiliation:
Universidade Estadual de Maringá, Nupelia, Maringá, Brasil
Y. Nawa
Affiliation:
Tropical Diseases Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand
*
Author for correspondence: R.M. Takemoto, E-mail: takemotorm@nupelia.uem.br
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Abstract

Fish-borne zoonotic nematodes may infect humans when fish or squid are ingested raw or inadequately cooked. Human infections may have serious consequences, including the unexpected deaths of infected people. This kind of disease is poorly known in general, and the characteristics of such infections in South American countries as a whole have never been assessed. In this paper the present status of fish-borne nematodiases in humans in South American countries is characterized. Potentially zoonotic nematode species are very common in both freshwater and marine fish in South America. Reports of human infections have only been found in some countries, and their incidence (especially with anisakids and Gnathostoma spp.) varies from country to country. Apparently they are more abundant in countries with strong traditions of eating raw fish, and are more frequent on the western coast of South America. So far fish-borne nematodes have been reported in Argentina, Brazil, Chile, Colombia, Ecuador and Peru. In recent years, cases of human infection have appeared in probably underestimated numbers. People need to be clearly informed about risky feeding habits, and physicians need to learn more about zoonotic diseases.

Type
Review Article
Information
Journal of Helminthology , Volume 92 , Issue 6 , November 2018 , pp. 649 - 654
Copyright
Copyright © Cambridge University Press 2017 

Introduction

Human infections with fish-borne nematodes have been reported worldwide and some are considered to be emerging diseases (Cross, Reference Cross1992; Stephen et al., Reference Stephen, de Bernardis and Baños2003; Butt et al., Reference Butt, Aldridge and Sander2004; Nawa & Nakamura-Uchiyama, Reference Nawa and Nakamura-Uchiyama2004; Murrell & Fried, Reference Murrell and Fried2007; Herman & Chiodini, Reference Herman and Chiodini2009). Fish-borne nematodiases are acquired by the consumption of live, raw, smoked, lightly cooked or marinated fish and/or squid and may be caused by infections with Anisakis spp., Pseudoterranova spp., Gnathostoma spp., Capillaria philippinensis (which is considered to be Calodium philippinensis by some authors) and, more rarely, with Hysterothylacium aduncum, Contracaecum spp., Eustrongylides spp. and Dioctophyme renale (Cross, Reference Cross1992; Yagi et al., Reference Yagi, Nagasawa, Ishikura, Nakagawa, Sato, Kikuchi and Ishikura1996; Barriga et al., Reference Barriga, Salazar and Barriga1999; Cabrera et al., Reference Cabrera, Luna-Pineda and Suárez-Ognio2003; Ignatovic et al., Reference Ignatovic, Stojokovic, Kutlesic and Tasic2003; Shamsi & Butcher, Reference Shamsi and Butcher2011; Eberhard & Ruiz-Tiben, Reference Eberhard and Ruiz-Tiben2014; Cornaglia et al., Reference Cornaglia, Jean, Bertrand, Aumaître, Roy and Nickel2016). In an exceptional case, infection with Angiostrongylus cantonensis after ingestion of raw fish was reported in France by Thobois et al. (Reference Thobois, Broussolle, Aimard and Chazot1996). Sometimes those infections may be highly pathogenic and can even cause the deaths of infected people (Cross, Reference Cross1992). In South America there are reports of infection with Anisakis spp., Pseudoterranova spp., D. renale (just one case reported) and Gnathostoma spp. Most of these cases were reported from Peru, Chile and Ecuador, i.e. countries where people have a strong tradition of eating raw or undercooked fish, as in the form of the traditional recipe called ‘ceviche’. In some other countries there are also reports of a few cases, but in most of them there are no reports of human infections. Serious concerns about this problem have been reviewed in countries such as Peru (Barriga et al., Reference Barriga, Salazar and Barriga1999; Cabrera & Trillo-Altamirano, Reference Cabrera and Trillo-Altamirano2004), Ecuador (Lazo, Reference Lazo2004), Chile (Jofré et al., Reference Jofré, Neira, Noemi and Cerva2008; Tuemmers et al., Reference Tuemmers, Nuñez, Willgert and Serri2014) and Brazil (Okamura et al., Reference Okamura, Pérez and Filho1999; Lima dos Santos, Reference Lima dos Santos2010; Knoff et al., Reference Knoff, São Clemente, Karling, Gazarini, Gomes, Pavanelli, Takemoto and Eiras2013b; Eiras et al., Reference Eiras, Pavanelli, Takemoto, Yamaguchi, Karling and Nawa2016a). However, a general overview of human infections with fish-borne nematodes in all the South American countries in total has never been produced. We present an overview of fish-borne nematodiases in South America, focusing on the characterization of the fish-borne zoonotic nematodiases in each country, and discussing the relative incidence of infection and diversity of parasite species in different South American countries, along with the causes of infection and the measures taken to control human infections with fish-borne nematodes.

Materials and methods

Fish-borne nematodiasis cases reported in the literature were gathered by an extensive Internet electronic search using appropriate keywords, e.g. nematode, human infections, emerging diseases, neglected diseases, anisakiasis, gnathostomiasis, capillariasis, sushi, sashimi, ceviche, traveller diseases, Gnathostoma, Pseudoterranova, Anisakis, Capillaria, etc., as well as various combinations of these keywords with all the South American countries. The Internet search engines PubMed, Medline, Google and Google Scholar were used as much as possible and the reference of every paper was checked in order to identify useful and reliable publications. We believe that nearly all the reported cases in South America have been tracked.

Considering several Gnathostoma species responsible for human diseases, we only refer to the specific names of specimens which were identified by morphological or molecular means, because serological methods alone are insufficient to differentiate the causative pathogens at the species level (Nopparatana et al., Reference Nopparatana, Setasuban, Chaicumpa and Tapchaisri1991; Ishiwata et al., Reference Ishiwata, Camacho, Ogata, Nakamura-Uchiyama, Hiromatsu and Nawa2003). Therefore, when the species identification is only based on serological methods, the cases are referred to as Gnathostoma sp. in table 1 and the corresponding presumptive species identified by serology are indicated in brackets.

Table 1. Human cases of fish-borne nematodiases in South American countries. Parasites are listed in alphabetical order, secondly by alphabetical order of the country and, for the same country, by chronological order of description.

aThe worms were not observed. The diagnosis was highly probable but based only on symptomatology.

bThis case was reported without immunodiagnosis and the validity of the description was questioned by Joob & Wiwanitki (Reference Joob and Wiwanitki2014). The same case was commented on by Rodrigues-Morales et al. (Reference Rodrigues-Morales, Cárdenas-Giraldo, Manrique-Castaño and Martinez-Pulgarín2014). See replies by Orduna et al. (Reference Orduna, Lloveras, Echazarreta, Garro, González and Falcone2014a, Reference Orduna, Lloveras, Echazarreta, Garro, González and Falconeb).

cDescribed as Toxocara sp. by Beltrán and co-workers (Beltrán, Reference Beltrán2000; Beltrán et al., Reference Beltrán, Náquira and Zuritas2001) – quoted from Cabrera & Trillo-Altamirano (Reference Cabrera and Trillo-Altamirano2004).

dThis case was described in Paraguay. The patient arrived in Paraguay from Chile the day after eating ‘ceviche’, and did not eat raw fish in Paraguay. Therefore, we consider that the infection was acquired in Chile and diagnosed in Paraguay.

Sometimes fish-borne nematodiasis cases have been reported among travellers returning from different South American countries. In those cases, the country of infection is considered to be the country where the infection was presumably acquired in South America and not necessarily the travellers’ place of residence.

Results

The number of cases of infection, parasite species, country and references are indicated in table 1. In total, there are reports of 49 cases of anisakidiasis, 1 case of dioctophymiasis and 93 cases of gnathostomiasis in South America. Anisakid infections are predominant in Chile and Peru, whereas gnathostomiasis is predominant in Peru, followed by Brazil and Ecuador.

Discussion

In South America there are 13 countries, among which only two, Bolivia and Paraguay, have no coastlines. The distribution of human infections with fish-borne nematodes per country revealed that there are no reports of infection in several countries (Bolivia, French Guiana, Guyana, Paraguay, Suriname, Uruguay and Venezuela), i.e, just over half of the South American countries. This fact does not necessarily mean that infections do not occur in those countries. Several researchers pointed out that, due to the reasons discussed further on, human infections are probably underestimated. Concerning the specific cases of Bolivia and Paraguay, the occurrence of infections with marine parasites is rather unlikely because they do not have a coastline, and therefore eating sea fish is not as common as in other countries. Furthermore, feeding habits in Paraguay do not include the eating of raw fish (Canese, Reference Canese1998), such behaviour being essential to prevent infection.

Some of the cases listed in table 1 refer to infections in returned travellers who became infected in South America and whose infections were detected after returning to their native countries. These were the cases of ‘anisakiasis’ from Chile to Belgium (Verhame & Ramboer, Reference Verhamme and Ramboer1988); Gnathostoma sp. (G. binucleatum?) from Brazil or Colombia to Belgium (Theunissen et al., Reference Theunissen, Bottieau, Van Gompel, Siozopoulou and Bradbury2016), from Peru to Brazil (Dani et al., Reference Dani, Mota, Sanchotene, Piñeiro-Maceda and Maia2009), from Peru to Switzerland (Chappuis et al., Reference Chappuis, Farinelli and Loutan2001) and from Peru to Germany (Bommer, Reference Bommer2004); and Gnasthostoma sp. from Colombia to Argentina (Orduna et al., Reference Orduna, Lloveras, Echazarreta, Garro, González and Falcone2013), from Brazil to France (Cornaglia et al., Reference Cornaglia, Jean, Bertrand, Aumaître, Roy and Nickel2016) and to Japan (Nawa, unpublished data, in Nawa & Nakamura-Uchiyama, Reference Nawa and Nakamura-Uchiyama2004), from Ecuador to Peru and from ‘Caribbe’ to Peru (Villar de Cipriani, Reference Villar de Cipriani2003). Similarly, infections acquired abroad and detected in South American countries were not considered, as in the case of a patient who was infected with Gnathostoma sp. in the United States but the infection was detected in Colombia (Jurado et al., Reference Jurado, Palacios, López, Baldión and Matijacevic2015).

As can be seen in table 1, the human infections are mostly due to anisakids (Anisakis spp. and Pseudoterranova spp.) and Gnathostoma spp. Besides these three genera, one case of infection with D. renale was reported in Brazil (Lisboa, Reference Lisboa1945). A case of intestinal capillariasis, presumably acquired in Colombia and detected in Spain (Dronda et al., Reference Dronda, Chavez, Sanz and Lopez-Velez1993), was not considered because of the uncertainity of infection in Colombia. In this case the reported patient had a history of frequent travel to other countries in South and Central America. Other fish-borne zoonotic nematode species (Eustrongylides spp., Contracaecum spp., H. aduncum and, more rarely, A. cantonensis) have not been reported to date.

Besides the data indicated in table 1, there are several other sources of information about the occurrence of these diseases. Weitzel et al. (Reference Weitzel, Sugiyama, Yamasaki, Ramirez, Rosas and Mercado2015) reported that about 30 cases of pseudoterranoviasis have been reported in Chile. Likewise, Ollague (Reference Ollague1985) reported an epidemic of gnathostomiasis (about 200 registered cases) in Guayaquil, Ecuador, and Lazo (Reference Lazo2004) reported that in the year 1990 the cases of human gnathostomiasis in Ecuador exceeded 2000. Therefore, if those cases are taken into account besides the cases reported in table 1, the approximate distribution of fish-borne nematodiases cases in total by country is: 1 case in Colombia, 3 in Argentina, 9 in Brazil, 59 in Peru, about 64 in Chile and over 2233 in Ecuador. In one case there are doubts about the country of infection (Brazil or Colombia – Theunissen et al., Reference Theunissen, Bottieau, Van Gompel, Siozopoulou and Bradbury2016), and another case was referred to as occurring in the ‘Caribe’ (Villar de Cipriani, Reference Villar de Cipriani2003). Most probably these figures do not correspond to the real situation. According to a number of researchers (Barriga et al., Reference Barriga, Salazar and Barriga1999; Okamura et al., Reference Okamura, Pérez and Filho1999; Cabrera et al., Reference Cabrera, Luna-Pineda and Suárez-Ognio2003; Cabrera & Trillo-Altamirano, Reference Cabrera and Trillo-Altamirano2004; Jofré et al., Reference Jofré, Neira, Noemi and Cerva2008; Cardia & Bresciani, Reference Cardia and Bresciani2012; Eiras et al., Reference Eiras, Pavanelli, Takemoto, Yamaguchi, Karling and Nawa2016a), fish-borne nematodiases are generally underestimated in South American countries, partially because physicians apparently have little experience and lack the training for diagnosis/treatment of fish-borne diseases. This is also considered to be case in other countries such as Australia (Shamsi, Reference Shamsi2014) and some European countries, as can be seen in a report from Belgium (Verhame & Ramboer, Reference Verhamme and Ramboer1988).

In terms of the distribution of anisakid infections, except for three cases in Brazil and two in Argentina, all cases were reported in just two countries, Chile and Peru. This is likely due to the consumption of ‘ceviche’, the traditional raw fish dish, which is commonly consumed in those countries, but is not so common in the countries of the east coast of South America. Another important concern is the possible importance of consumption of raw fish prepared according to traditional Japanese dishes, such as ‘sushi’ and ‘sashimi’. Eiras et al. (Reference Eiras, Pavanelli, Takemoto, Yamaguchi, Karling and Nawa2016a) discussed this problem in Brazil in detail, showing that the number of ‘Japanese’ restaurants has increased exponentially in the past few years. We have no such detailed data concerning the other South American countries but some authors are concerned about the possible importance of these restaurants for the propagation of fish-borne nematodiases in humans (Adams et al., Reference Adams, Leja, Jinneman, Beeh, Yuen and Wekell1994; Mercado et al., Reference Mercado, Torres, Muñoz and Apt2001; Cabrera & Trillo-Altamirano, Reference Cabrera and Trillo-Altamirano2004; Jofré et al., Reference Jofré, Neira, Noemi and Cerva2008; Florencia et al., Reference Florencia, Barcan, Nemirovsky and De Paz Sierra2011; Torres-Frenzel & Torres, Reference Torres-Frenzel and Torres2014). No doubt this problem deserves the attention of sanitary authorities and researchers to clarify its impact on public health. At the moment, based on the available data, it can be presumed that human infections on the west coast of South America are mainly due to the consumption of ‘ceviche’, whereas those on the east coast are due principally to ‘Japanese’ or similar restaurants.

According to Mercado et al. (Reference Mercado, Torres, Gil and Goldin2006) the majority of fish-borne nematodiases in Chile, a country with a high incidence rate, are due to infection with Pseudoterranova spp., the most frequent nematode in the muscles of marine fish in this country. The emergence of anisakidosis due to A. physeteris was probably related to the El Niño along the Peruvian coast in 1997–98 (Cabrera & Suárez-Ognio, Reference Cabrera and Suárez-Ognio2002). During El Niño, due to the decrease in numbers of fish from colder waters, there was an increase in the catch of Coryphaena hippurus (common dolphinfish, also known as Mahi-mahi), which is often infected with species of Anisakidae and is commonly used to prepare ‘ceviche’ (Cabrera & Suárez-Ognio, Reference Cabrera and Suárez-Ognio2002). El Niño and its biological consequences, therefore, affect the prevalence of species of Anisakidae in fish, and the availability of fish species to fishermen may be an important factor for the mechanisms of human infections with fish-borne nematodes (Cabrera & Suárez-Ognio, Reference Cabrera and Suárez-Ognio2002). This question deserves further research.

Concerning infection with Gnathostoma spp., most of the cases occurred in Peru (Álvarez et al., Reference Álvarez, Morales and Bravo2011) and especially in Ecuador (Lazo, Reference Lazo2004; Nawa et al., Reference Nawa, Maleewong, Intapan, Díaz-Camacho, Xiao, Ryan and Feng2015), where gnathostomiasis is considered to be an endemic disease. The absence of gnathostomiasis in Chile is puzzling. Assuming that the infections are acquired by consuming ‘ceviche’, it seems that freshwater fish, which are the intermediate/paratenic hosts for Gnathostoma spp., are not commonly used to prepare this dish in Chile.

Several species of Gnathostoma are assumed to cause human infections in South America. In addition to the well-known G. binucleatum as the causative pathogen (Theunissen et al., Reference Theunissen, Bottieau, Van Gompel, Siozopoulou and Bradbury2016), G. spinigerum is also referred to as a human pathogen in the Americas (Chappuis et al., Reference Chappuis, Farinelli and Loutan2001; Bommer, Reference Bommer2004; Vargas et al., Reference Vargas, Kahler, Dib, Cavaliere and Jeunon-Sousa2012). However, according to recent molecular studies by Almeyda-Artigas et al. (Reference Almeyda-Artigas, Dolores and Mas-Coma2000) and Léon-Règagnon et al. (Reference Léon-Règagnon, Osorio-Sara, García-Prieto, Akahane, Lamothe-Argumedo, Koga, Messina-Robles and Alvarez-Guerrero2002), the Gnathostoma species involved in human infections in Mexico and Ecuador are all G. binucleatum, with the suggestion that G. spinigerum does not exist in the Americas. At times, G. doloresi has also been wrongly considered as a human pathogen in South America, because Mimori et al. (Reference Mimori, Tada, Kawabata, Ollague, Calero and De Chong1987) used crude somatic extract antigen of G. doloresi for immunodiagnosis of gnathostomiasis in Ecuador. At present, therefore, all gnathostomiasis cases in the South American countries are attributed to G. binucleatum.

An important question directly related to human infections concerns the number and specific diversity of fish species infected with potentially zoonotic nematodes. In a recent survey, Eiras et al. (Reference Eiras, Velloso and Pereira Júnior2016b) listed the parasites of 685 different marine fish species from South America and found that 185 species were infected with potentially zoonotic nematodes. Earlier, Eiras et al. (Reference Eiras, Pavanelli and Takemoto2010) listed the parasites of freshwater fish from Brazil and showed that 74 fish species were infected with various species of zoonotic nematodes. Furthermore, some of the most commercially important fish species often present high values of prevalence and intensity of infection (Felizardo et al., Reference Felizardo, Knoff, Pinto and Gomes2009; Knoff et al., Reference Knoff, São Clemente, Fonseca, Felizardo, Lima, Pinto and Gomes2013a; Mattos et al., Reference Mattos, Lopes, Verícimo, Alvares and São Clemente2014; Rodrigues et al., Reference Rodrigues, Pantoja, Guimarães, Benigno, Palha and Biondi2015). Therefore, the potential of those fish species for causing human infections is high.

An important factor is that physicians in general do not have sufficient knowledge about this problem in South American countries, as stated above, and some authors think that the number of real cases is much higher than reported. Furthermore, Alvarez et al. (Reference Álvarez, Morales and Bravo2011) reported that the number of gnathostomiasis cases in Peru has increased significantly in recent years, Tuemmers et al. (Reference Tuemmers, Nuñez, Willgert and Serri2014) reported that, in Chile, health problems from ‘sushi’ consumption more than doubled during 4 months of 2013 compared to the same period in 2012, and Torres et al. (Reference Torres, Canales, Concha, Cofre and Tellez2000) mentioned the increase of anisakiasis in Chile. Thus, the need to inform people about the risks of eating raw fish is obvious.

Some procedures may be adopted to reduce the risk of human contamination. First, the ingestion of fish after being cooked adequately (60°C for at least 10 min) is a certain way of preventing infection. If fish are to be consumed raw, the most efficient ways of preventing infections are those advised by the US Food and Drug Administration (FDA): storing the fish at a temperature of −20°C or lower for 7 days (total time), or at −35°C or lower for 15 h. These procedures may need some modification according to the size of the fish, fish species, target parasites, etc. (US Food and Drug Administration, 2011).

Any attempt to reduce, or even to eliminate, human infections with fish-borne nematodes has to take into account a number of important measures integrating three factors: changing feeding behaviour, providing clear information to people and increasing the knowledge of physicians. We should realize that winning such a ‘battle’ is not easy, especially in countries where eating raw fish dishes is an old and highly conservative tradition. The successful example of The Netherlands, where human infection due to the strong tradition of eating raw herring (‘maatjes’) was practically eliminated by compulsory freezing of the fish (Verhamme & Ramboer, Reference Verhamme and Ramboer1988), demonstrates that it is possible to eliminate such infections.

Acknowledgements

The authors acknowledge colleagues who helped with the literature survey: P. Torres, C. Menghi and M.S. Arita. The authors thank Dr Ken MacKenzie for literary revision of the manuscript.

Financial support

This paper was supported by MCTI (Ministery of Science and Technology, Portugal), CAPES-MEC (Ministery of Education, Brazil), CNPq (National Centre for Research and Development, Brazil), FAPS (Foundation for Research in São Paulo State, Brazil). The participation of J.C.E. was partially supported by the European Regional Development Fund (ERDF) through the COMPETE – Operational Competitiveness Programme, by national funds through FCT (Foundation for Science and Technology) under the project ‘Pest-C/MAR/LA0015/2001’ and by CESUMAR (Centro Universitário Cesumar, Brazil).

Conflict of interest

None.

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Figure 0

Table 1. Human cases of fish-borne nematodiases in South American countries. Parasites are listed in alphabetical order, secondly by alphabetical order of the country and, for the same country, by chronological order of description.