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Anisakid Presence in the European Conger, Conger conger, from Spanish Mediterranean Waters †

by
Xavier Roca-Geronès
1,
Lídia Sarrà-Alarcón
2,
Eulàlia Delgado
2,
Maria Magdalena Alcover
1,
Margarida Casadevall
2 and
Roser Fisa
1,*
1
Secció de Parasitologia, Departament de Biologia, Sanitat i Medi Ambient, Facultat de Farmàcia i Ciències de l’Alimentació, Universitat de Barcelona, 08028 Barcelona, Spain
2
Department de Ciències Ambientals, Facultat de Ciències, Universitat de Girona, 17003 Girona, Spain
*
Author to whom correspondence should be addressed.
In memory of Dr. Isabel de Montoliu Sanllehy (1955–2023), lecturer and researcher at the Department of Biology, Health and Environment of the Universitat de Barcelona, who passed away on 14 March 2023.
Pathogens 2023, 12(11), 1326; https://doi.org/10.3390/pathogens12111326
Submission received: 6 October 2023 / Revised: 2 November 2023 / Accepted: 3 November 2023 / Published: 8 November 2023
(This article belongs to the Special Issue Anisakiasis and Anisakidae)

Abstract

:
The European conger, Conger conger, is a benthic marine fish species with a geographical distribution extending through the northeastern Atlantic and the Mediterranean. Despite being extensively distributed and widely appreciated by Spanish consumers, studies regarding parasite presence in this fish are scarce. In the present work, a hundred and eight specimens from the Mediterranean coast of northeastern Spain (Catalan waters) were surveyed for the presence of nematode parasites. Several species were morphologically identified: third-stage larvae of Anisakis type I (sensu Berland, 1961) (n = 131), third-stage larvae of Anisakis type II (sensu Berland, 1961) (n = 18), third- and fourth-stage larvae and adults of Hysterothylacium spp. (n = 48), adults of Cucullanus sp. (n = 391), and adults of Cristitectus congeri (n = 69). Moreover, some fish and decapode species were also observed as part of the host’s diet, with the most detected preys being Micromesistius poutassou, Sardina pilchardus, Macropipus sp., and Goneplax rhomboides. This represents the first survey of nematode parasites infecting C. conger from the northeastern Spanish Mediterranean waters. Among the parasite species detected, the presence of Anisakis species should be highlighted as the ingestion of C. conger parasitized with these larvae could potentially lead to anisakiasis in consumers.

1. Introduction

The European conger, Conger conger (Linnaeus, 1758), is a benthic marine fish species inhabiting rocky and sandy bottoms between 5 to 1000 m in depth and presenting sex segregation in some areas [1,2,3]. It is a large opportunistic predator, with a diet including a wide range of crustaceans, fish, and cephalopods [4], which vary in relation to the host’s living depth and its reproductive cycle [5].
The geographical distribution of the European conger extends through the northeastern Atlantic, from Norway and Iceland to Senegal, including the Macaronesian archipelagos, and the Mediterranean and Black Seas [6]. This species is of great importance in commercial and recreational fisheries on both Atlantic and Mediterranean coasts [6,7]. In 2021, the total world catches of C. conger were 9480.6 t [8], with Spain being one of the countries with the highest number of catches through the years [9,10].
Studies regarding the parasite fauna of C. conger in the Mediterranean Sea and the northeastern Atlantic have identified several species corresponding to different phyla. Some of the nematodes identified include Anisakis Dujardin, 1845, Cucullanus Müller, 1777 or Cristitectus Petter, 1970 species. Regarding digenids, Helicometra Odhner, 1902, Lecithochirium Lühe, 1901 and Prosorhynchus Odhner, 1905 species, among others, have been detected, while Tetraphillidids and Trypanorhyincha species have been observed corresponding to cestodes [11,12,13,14,15].
Among all these species, the European Food Safety Authority (EFSA) considers A. simplex s.l. as an important “biological hazard” in seafood products [16]. This species can cause anisakiasis in humans when raw or undercooked fish is consumed, provoking severe gastrointestinal and/or allergic symptoms [17,18]. In Spanish waters, the parasite community of the European conger has been poorly studied, despite being extensively distributed and widely appreciated by consumers.
The aim of the present study was to survey the commonly consumed C. conger from the Mediterranean coast of northeastern Spain (Catalan waters) for the presence of nematode species. Moreover, special emphasis was placed on analyzing the content of the host’s stomach to analyze its diet in this area.

2. Materials and Methods

2.1. Host Sampling and Parasite Collection

A parasitological analysis focused on nematode species was carried out on 108 specimens of C. conger collected during the years 2011–2012 from the Catalan Mediterranean coasts, in the northeastern Spanish waters, corresponding to the FAO (Food and Agriculture Organization of the United Nations) fishing area 37.1.1. After measuring total length and weight, fish were dissected and weighed again. The total length, total weight, and eviscerated weight of the 108 European conger (C. conger) specimens analyzed are shown in Table 1. The viscera were isolated and organs including the stomach, intestine, liver, and gonads were separated in petri dishes containing physiological saline solution. Each part was examined for the presence of nematodes under a stereomicroscope using a fiber optical illuminator. In addition, the external part of the musculature surrounding the host’s belly flaps was also inspected.
Parasites were morphologically identified by observing the main structures of their anterior and posterior ends. The presence of a tooth, the shape of the ventricle, and the morphology of the posterior end were used to identify Anisakis and Hysterothylacium Ward & Magath, 1917 species following the criteria of Berland [19] and Hartwich [20]. For the identification of Cucullanus, the shape of the anterior end, the form of the oesophagus, and the sexual structures of the caudal end were used according to Berland [19]. Finally, following Petter’s [21] and Quinteiro et al.’s [22] criteria, species of Cristitectus were identified by examining the morphology of their anterior end, containing the cuticular ridges, and the posterior end.

2.2. Host Diet

The host’s stomach samples, including the entire contents, were weighed after the removal of surface water by blotting with tissue paper. Prey items were carefully separated, counted, and weighed individually. All components were divided into fish (Osteichthyes) or crustacean (Decapoda) and identified to the lowest taxonomic level possible using the identification guides and keys provided by Zariquiey [23] and Fischer et al. [24]. When it was impossible to identify the prey at the species level due to missing parts, classification was carried out at the next level (for example, family). Fragmented prey was counted using a part of their body that was easy to determine (for example, telson for Decapodes). If the prey was too fragmented, it was considered as a single prey. A group of not-determined prey was included for each taxonomic group when the prey presented advanced levels of digestion.

2.3. Epidemiological Concepts and Statistical Analysis

Estimated prevalence (P), mean intensity, and mean abundance (A), as descriptive epidemiological terms [25], were calculated using the Quantitative Parasitology Software 3.0 [26] in the 95% confidence interval (CI) for each parameter (2000 bootstrap replications).
Spearman’s Rho (Rho) nonparametric test was applied to analyze the correlation between larval abundance and fish total length and weight. All parameters and variables were tabulated for their analysis in SPSS v22 software.

3. Results

3.1. Host Parasitic Infection

The nematode analysis of the host’s viscera resulted in the identification of 657 specimens, which were morphologically identified as third-stage larvae (L3) of Anisakis type I (sensu Berland, 1961) (n = 131), L3 of Anisakis type II (sensu Berland, 1961) (n = 18), adults of Cucullanus sp. (n = 391), adults of Cristitectus congeri Petter, 1970 (n = 69), and species of Hysterothylacium (n = 48) (Figure 1). Specimens of Hysterothylacium were found in three different evolutionary stages, L3 (n = 7), fourth-stage larvae (L4) (n = 38), and adults (n = 3). Nematodes were mostly found in the visceral cavity, including the stomach, the intestine, and the liver, for species of Anisakis and Cucullanus, and the stomach and the intestine for specimens of Hysterothylacium spp. and C. congeri. Moreover, some specimens were also found encysted on the surface of the musculature surrounding the viscera.
The analysis results of the descriptive epidemiological variables of host parasitisation by nematodes are shown in Table 2. Cucullanus sp. and Anisakis type I (sensu Berland, 1961) species were the most prevalent parasites (P = 79.6% and P = 33.3%, respectively) with mean abundance values of 3.6 for the former species and 1.2 for the latter.
Spearman’s correlation analysis showed a significant positive correlation (p < 0.01) between host length and weight and the total abundance of all nematodes identified (ρ = 0.4 for both parameters). When comparing the two biometric parameters with the number of specimens of the different nematode species, a significant positive correlation (p < 0.01) was detected for Anisakis type I (sensu Berland, 1961) (ρ = 0.5), Anisakis type II (sensu Berland, 1961) (ρ = 0.3), and Cucullanus sp. (ρ = 0.3).

3.2. Host Prey Items

A total of 78 individuals of European conger contained food in their stomachs (72.2%). Fish items (n = 79) were found in 53 C. conger specimens (49.1%) while crustacean remains (n = 65) were observed in 35 hosts (32.4%). Among them, a total of 40 prey taxa were identified, with 24 belonging to osteichthyes and 16 to decapods (Table 3). Regarding fish species, Micromesistius poutassou (Risso, 1827) (n = 15) and Sardina pilchardus (Walbaum, 1792) (n = 8) were the most frequent prey while 32 remains (40.52%) could not be determined. Macropipus Prestandrea, 1833 specimens (n = 22) and Goneplax rhomboides (Linnaeus, 1758) (n = 8) were the most detected crustaceans, with 19 decapod remains (29.2%) unable to be identified.

4. Discussion

Several nematode species have been identified parasitizing the European conger in Mediterranean and Atlantic waters [12,14]. In the present study, we report for the first time the identification of five nematode species in C. conger specimens from the Mediterranean coast of northeastern Spain (Catalan coast), corresponding to Anisakis type I (sensu Berland, 1961), Anisakis type II (sensu Berland, 1961), Hysterothylacium spp., Cucullanus sp., and C. congeri (Table 2). The four former species have been identified in a wide range of hosts worldwide, including several fish and cephalopod species [27,28,29,30,31], while C. congeri is known to be a specialist nematode of conger eels [21,22]. The Anisakis larvae found in the studied fish were denominated Anisakis type I and type II (sensu Berland, 1961) as they were only identified following morphological criteria. However, specimens of Anisakis type I (sensu Berland, 1961) probably correspond to Anisakis pegreffii Campana-Rouget & Biocca, 1955, included in the A. simplex sensu lato complex, as it is the most frequent species of the complex identified on the Catalan coast [32,33,34]. In the same line, molecular methodologies could confirm the identification of Anisakis type II as Anisakis physeteris Baylis, 1923 [32,33,34].
In other regions of the Spanish Mediterranean area, only Muñoz et al. [35] from the central Eastern coast (Valencian waters) have analyzed the parasitological fauna of C. conger, identifying Cucullanus hians (Dujardin, 1845) Petter, 1974, Cucullanus longispiculum De Oliveira Rodrigues, Carvalho Varela, Sodre’ Rodrigues & Cristofaro, 1973 and species of Dichelyne Jägerskiöld, 1902. For both species of the genus Cucullanus, prevalence (58% and 43%, respectively) and mean intensity (2 for both species) values were lower in comparison with the results obtained in the present work (79.6% and 4.6 for Cucullanus sp.). It should be noted that, despite the geographical area, where anisakid nematodes are habitually identified in other fish species such as the blue whiting or the surmullet [36,37,38], and the high number of hosts analyzed (78), species of Anisakis or Hysterotylacium were not detected [35].
In other Mediterranean areas, such as the Sardinian waters and the Aegean Sea, nematode species detected in our work were also identified [14,36]. In Sardinia, values of prevalence and mean abundance for Anisakis simplex s.l. (P = 11.5; A = 0.1), Cucullanus bioccai Orecchia & Paggi, 1987 (P = 46.2; A = 2.9), and C. congeri (P = 7.7; A = 0.1) were lower compared to those observed in the present study (Table 2). On the other hand, Hysterothylacium spp. (P = 61.5; A = 2.0) presented higher values in comparison with those herein obtained (P = 26.9; A = 0.4). The presence of A. physeteris was scarce in both Mediterranean areas [14]. In the Aegean Sea, the nematode species identified corresponded only to A. simplex s.l. and C. hians [39]. For both species, prevalence was lower (15.38% and 7.69%, respectively) while mean intensity was higher (3.5 and 6, respectively) compared to the values of our work (Table 2). It is noteworthy that the number of analyzed hosts in the current investigation was higher than the previous Mediterranean studies [14,35,39], standing out as representative in terms of nematode analysis of the European conger.
In the Atlantic area, including the Spanish coast and the Madeira Islands, several authors have identified A. simplex s.l. parasitizing C. conger, showing in all cases lower prevalence (from 1.1% to 9%) and mean abundance values (from 0.01 to 1.3) [12,15,40]. These epidemiological values contrast with the remarkably high prevalence and mean abundance values of A. simplex s.l. observed in other fish species from the northeastern Atlantic waters [32,38,41]. On the other hand, in the Atlantic waters, prevalence and intensity of Cucullanus species and C. congeri were variable, detecting higher and lower values in comparison with our work [11,12,15,22,40].
The variability of the nematode epidemiological terms between areas could depend on the biotic and abiotic conditions of the host habitat, which could lead to particular environmental conditions [12,40]. Moreover, host population isolation and differences in their trophic chain could also be an important differentiation factor [40]. In this sense, the opportunistic predatory behavior of the C. conger was confirmed by the high variability detected between the prey items of the host diet, including a wide number of taxa for both fish and crustaceans (Table 3). This variability has also been observed in other Atlantic and Mediterranean areas, where fish and crustacean species identified in the host’s stomach were also very diverse [4,42,43,44], being the most detected prey items of our study (M. poutassou, S. pilchardus, Macropipus sp., and G. rhomboides) absent or very scarce.
The remarkable presence of Anisakis type I (sensu Berland, 1961) in the European conger of the present work (P = 33.3%) could be related to the ingestion of M. poutassou, which is known to be a fish species habitually infested with this parasite in the studied area [32,45,46]. On the other hand, S. pilchardus, the other fish species identified as a habitual prey of the European conger from the Catalan coast, is not frequently parasitized with Anisakis type I (sensu Berland, 1961) in this region [47,48].
From all of the nematode species identified in the present study, Anisakis type I (sensu Berland, 1961) is the most important in terms of public health as it can cause gastric and/or allergic anisakiasis in humans [17,18]. In Spain, several cases have been reported in recent years [49,50]. Most of the gastric and intestinal cases are associated with the consumption of marinated anchovies, a typical dish in Spanish cuisine. Additionally, other species such as hake and sardine have also been reported as a source of infection [50,51,52].
Conger conger has not been documented as the source of anisakiasis in northeastern Atlantic and Mediterranean countries, but it should be taken into account as a possible cause of the disease due to the notable detection of Anisakis type I (sensu Berland, 1961). The analysis carried out in the present work was focused on the viscera and the external part of the anteroventral muscle, which has been documented as the most parasitized portion of the flesh in several fish species, such as the blue whiting, the grey gurnard, or the beaked redfish [32,53,54]. Although the number of larvae decreases in the posterior part of the musculature [32,53,54], a deeper examination of the flesh using specific methodologies, e.g., the UV-press method or the pepsin digestion, might increase the number of A. simplex s.l. identified in the European conger herein studied.
Moreover, in South Korea, where the common conger species is Conger myriaster (Brevoort, 1856), several gastric and allergic anisakiasis cases have been documented after the raw ingestion of this fish [55,56]. In China, A. simplex s.l. has been detected in the same host species with high prevalence and intensity values [57].
The epidemiological results of the European conger herein obtained reinforce the consideration of C. conger in terms of health risk, as values are in some cases higher than some fish species from the Catalan coast, such as the blue whiting or the Atlantic mackerel, among others [32,48]. As occurring in other fish species [32,58], special emphasis should be placed on the biggest C. conger specimens, as the host’s length and weight have been positively correlated with Anisakis type I (sensu Berland, 1961) abundance. Furthermore, globalization has led to worldwide changes in eating habits, and together with the increasing consumption of fish products, especially raw forms like sushi or ceviche, the number of anisakiasis cases has also increased worldwide [59,60]. In this context, due to its extensive distribution and popularity, Spanish consumers should be warned of the risk of consuming raw or undercooked C. conger.

5. Conclusions

Our research provides the first parasite identification focused on nematode species in C. conger from the Mediterranean coast of northeastern Spain. Anisakis type I (sensu Berland, 1961) and Cucullanus sp. were the most frequent nematode parasites, presenting remarkable prevalence and mean abundance values. In this sense, Spanish consumers should be aware of the possible presence of Anisakis type I (sensu Berland, 1961) in Mediterranean European conger due to the gastrointestinal and/or allergic illness that this parasite can cause. The presence of this nematode species in the hosts herein studied might be related to the ingestion of M. poutassou, which was identified as one of the most habitual prey of the European conger. In addition, a wide number of fish and crustacean species were identified as prey items of the C. conger diet, confirming the opportunistic predatory behavior of this fish species.

Author Contributions

Conceptualization, X.R.-G., M.C. and R.F.; methodology, L.S.-A. and E.D.; validation, M.C.; formal analysis, X.R.-G. and M.C.; investigation, X.R.-G., M.M.A., L.S.-A., E.D., M.C. and R.F.; resources, M.C. and R.F.; data curation, X.R.-G., M.C. and R.F.; writing—original draft preparation, X.R.-G.; review and editing, X.R.-G., M.M.A., M.C. and R.F.; supervision, M.C. and R.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Generalitat de Catalunya Project 2021 SGR 00359.

Institutional Review Board Statement

The fish used in the abovementioned study were obtained at the Palamós fish market, once unloaded from the fishing boats. It was already dead when we picked it up, so there was not a need for any ethical approval as there was no issue of mistreatment or euthanasia.

Informed Consent Statement

Not applicable.

Data Availability Statement

All relevant data are provided in the present study.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Tortonese, E. Fauna d’Italia. Osteichthyes (Pesci Ossei); Calderini: Bologna, Italy, 1970. [Google Scholar]
  2. Santos, R.V.S.; Silva, W.M.M.L.; Novoa-Pabon, A.M.; Silva, H.M.; Pinho, M.R. Long-Term Changes in the Diversity, Abundance and Size Composition of Deep Sea Demersal Teleosts from the Azores Assessed through Surveys and Commercial Landings. Aquat. Living Resour. 2019, 32, 25. [Google Scholar] [CrossRef]
  3. Casadevall, M.; Sarrà-Alarcón, L.; Delgado, E.; Matallanas, J. The Sexual Segregation of the European Eel, Conger conger (Linnaeus, 1758) (Anguilliformes, Congridae) and Female Semelparity in the North-West Mediterranean. J. Fish. Res. 2017, 1, 5–14. [Google Scholar]
  4. Xavier, J.C.; Cherel, Y.; Assis, C.A.; Sendão, J.; Borges, T.C. Feeding Ecology of Conger Eels (Conger conger) in North-East Atlantic Waters. J. Mar. Biol. Assoc. UK 2010, 90, 493–501. [Google Scholar] [CrossRef]
  5. Cau, A.; Manconi, P. Relationship of Feeding, Reproductive Cycle and Bathymetric Distribution in Conger conger. Mar. Biol. 1984, 81, 147–151. [Google Scholar] [CrossRef]
  6. Bauchot, M.L.; Saldanha, L. Congridae. In Fishes of the Northeastern Atlantic and Mediterranean; Whitehead, J.P., Bauchot, M.L., Hureau, J.C., Nielsen, J., Tortonese, E., Eds.; UNESCO: Paris, France, 1986; Volume 2, pp. 567–574. [Google Scholar]
  7. Santos, R.; Medeiros-Leal, W.; Pinho, M. Synopsis of Biological, Ecological and Fisheries-Related Information on Priority Marine Species in the Azores Region. Arquipelago 2020, 1, 1–138. [Google Scholar] [CrossRef]
  8. FAO Fisheries and Aquaculture. Available online: https://www.fao.org/fishery/en/aqspecies/2994/en (accessed on 2 October 2023).
  9. Medeiros-Leal, W.; Santos, R.; Novoa-Pabon, A.; Silva, H.; Pinho, M. Population Structure of the European Conger Conger conger from the Mid-North Atlantic Ocean Inferred from Bathymetric Distribution, Length Composition and Movement Patterns Analyses. Fish. Manag. Ecol. 2021, 28, 468–477. [Google Scholar] [CrossRef]
  10. Piñeiro, C.G.; Casas, M.; Bañón, R. The Deep-Water Fisheries Exploited by Spanish Fleets in the Northeast Atlantic: A Review of the Current Status. Fish. Res. 2001, 51, 311–320. [Google Scholar] [CrossRef]
  11. Saraiva, A.; Cruz, C.; Santos, M.J.; Ferreira, S. Nematode Parasites from Digestive Tract of Conger Conger conger L. from the Northwest Coast of the Iberian Peninsula. Bull. Eur. Fish. Pathol. 2000, 20, 163–166. [Google Scholar]
  12. Costa, G.; Santos, M.J.; Costa, L.; Biscoito, M.; Pinheiro De Carvalho, M.A.A.; Melo-Moreira, E. Helminth Parasites from the Stomach of Conger Eel, Conger conger, from Madeira Island, Atlantic Ocean. J. Parasitol. 2009, 95, 1013–1015. [Google Scholar] [CrossRef]
  13. Bartoli, P.; Bray, R.A.; Gibson, D.I. Opecoelidae (Digenea) from Western Mediterranean Fishes: Three Rare Species. Syst. Parasitol. 2003, 55, 81–95. [Google Scholar] [CrossRef]
  14. Culurgioni, J.; D’Amico, V.; Coluccia, E.; Mulas, A.; Figus, V. Metazoan Parasite Fauna of Conger Eel Conger conger L. from Sardinian Waters (Italy). Ittiopatologia 2006, 3, 253–261. [Google Scholar]
  15. Sanmartin Duran, M.; Quinteiro, P.; Ubeira, F. Nematode Parasites of Commercially Important Fish in NW Spain. Dis. Aquat. Organ. 1989, 7, 75–77. [Google Scholar] [CrossRef]
  16. EFSA Panel on Biological Hazards. Scientific Opinion on Risk Assessment of Parasites in Fishery Products. EFSA J. 2010, 8, 1–91. [Google Scholar] [CrossRef]
  17. Audícana, M.T.; Ansotegui, I.J.; Fernández de Corres, L.; Kennedy, M.W. Anisakis simplex: Dangerous Dead and Alive? Trends Parasitol. 2002, 18, 20–25. [Google Scholar] [CrossRef] [PubMed]
  18. Mattiucci, S.; D’Amelio, S. Anisakiasis. In Helminth Infections and Their Impact on Global Public Health; Bruschi, F., Ed.; Springer-Verlag: Viena, Austria, 2014; pp. 325–365. [Google Scholar]
  19. Berland, B. Nematodes from Some Norwegian Marine Fishes. Sarsia 1961, 2, 1–50. [Google Scholar] [CrossRef]
  20. Hartwich, G. Keys to Genera of the Ascaridoidea. In CIH Keys to the Nematode Parasites of Vertebrates; Anderson, R.C., Chabaud, A.G., Willmott, S., Eds.; Commonwealth Agricultural Bureaux: Slough, UK, 1974; Volume 2, pp. 1–15. [Google Scholar]
  21. Petter, A.J. Quelques Spirurides de Poissons de La Région Nantaise. Ann. Parasitol. Hum. Comp. 1970, 45, 31–46. [Google Scholar] [CrossRef]
  22. Quinteiro, P.; Fernández, J.A.; Sanmartín, M.L. First Description of the Male and New Data on the Female of Cristitectus congeri Petter, 1970 (Nematoda: Cystidicolidae). Syst. Parasitol. 1989, 14, 37–41. [Google Scholar] [CrossRef]
  23. Zariquiey Alvarez, R. Crustáceos Decápodos Ibéricos. Invest. Pesq. 1968, 32, 1–510. [Google Scholar]
  24. Fischer, W.; Schneider, M.; Bauchot, M.-L. Fiches FAO d’Identification des Espèces pour Les Besoins de La Pêche: Méditerranée et Mer Noir Zone de Pêche 37; Organisation des Nations Unies pour l’Alimentation et l’Agriculture: Rome, Italy, 1987. [Google Scholar]
  25. Bush, A.O.; Lafferty, K.D.; Lotz, J.M.; Shostak, A.W. Parasitology Meets Ecology on Its Own Terms: Margolis et al. Revisited. J. Parasitol. 1997, 83, 575–583. [Google Scholar] [CrossRef]
  26. Rózsa, L.; Reiczigel, J.; Majoros, G. Quantifying Parasites in Samples of Hosts. J. Parasitol. 2000, 86, 228–232. [Google Scholar] [CrossRef]
  27. Alburqueque, R.A.; Palomba, M.; Santoro, M.; Mattiucci, S. Molecular Identification of Zoonotic Parasites of the Genus Anisakis (Nematoda: Anisakidae) from Fish of the Southeastern Pacific Ocean (off Peru Coast). Pathogens 2020, 9, 910. [Google Scholar] [CrossRef] [PubMed]
  28. Palomba, M.; Mattiucci, S.; Crocetta, F.; Osca, D.; Santoro, M. Insights into the Role of Deep-Sea Squids of the Genus Histioteuthis (Histioteuthidae) in the Life Cycle of Ascaridoid Parasites in the Central Mediterranean Sea Waters. Sci. Rep. 2021, 11. [Google Scholar] [CrossRef] [PubMed]
  29. Mattiucci, S.; Nascetti, G. Advances and Trends in the Molecular Systematics of Anisakid Nematodes, with Implications for Their Evolutionary Ecology and Host-Parasite Co-Evolutionary Processes. Adv. Parasitol. 2008, 66, 47–148. [Google Scholar] [CrossRef] [PubMed]
  30. Roca-Geronès, X.; Montoliu, I.; Godínez-González, C.; Fisa, R.; Shamsi, S. Morphological and Genetic Characterization of Hysterothylacium Ward & Magath, 1917 (Nematoda: Raphidascarididae) Larvae in Horse Mackerel, Blue Whiting and Anchovy from Spanish Atlantic and Mediterranean Waters. J. Fish Dis. 2018, 41, 1463–1475. [Google Scholar] [CrossRef] [PubMed]
  31. Moravec, F.; Justine, J. Lou New Records of Cucullanid Nematodes from Marine Fishes off New Caledonia, with Descriptions of Five New Species of Cucullanus (Nematoda, Cucullanidae). Parasite 2020, 27, 1–23. [Google Scholar] [CrossRef]
  32. Roca-Geronès, X.; Segovia, M.; Godínez-González, C.; Fisa, R.; Montoliu, I. Anisakis and Hysterothylacium Species in Mediterranean and North-East Atlantic Fishes Commonly Consumed in Spain: Epidemiological, Molecular and Morphometric Discriminant Analysis. Int. J. Food Microbiol. 2020, 325, 108642. [Google Scholar] [CrossRef]
  33. Mattiucci, S.; Cipriani, P.; Levsen, A.; Paoletti, M.; Nascetti, G. Molecular Epidemiology of Anisakis and Anisakiasis: An Ecological and Evolutionary Road Map. Adv. Parasito.l 2018, 99, 93–263. [Google Scholar] [CrossRef]
  34. Piras, M.C.; Tedde, T.; Garippa, G.; Virgilio, S.; Sanna, D.; Farjallah, S.; Merella, P. Molecular and Epidemiological Data on Anisakis Spp. (Nematoda: Anisakidae) in Commercial Fish Caught off Northern Sardinia (Western Mediterranean Sea). Vet. Parasitol. 2014, 203, 237–240. [Google Scholar] [CrossRef]
  35. Muñoz, M.V.; Fernández, J.P.; Orts, M.E.; Carbonell, E. Sobre Algunos Nematodos Cucullanidos Parásitos de Conger conger (L.) En Aguas Del Litoral Valenciano. Rev. Iber. Parasitol. 1988, 48, 275–281. [Google Scholar]
  36. Cuéllar, M.C.; Fontanilla, J.C.; Pérez-Fuentes, J.; Pérez-Tauler, M.P. Biología y Epidemiología de La Anisakidosis Larvaria. Enfermedad Arenque. Cienc. Vet. 1991, 4, 57–63. [Google Scholar]
  37. Barcala, E.; Ramilo, A.; Ortega, N.; Picó, G.; Abollo, E.; Pascual, S.; Muñoz, P. Occurrence of Anisakis and Hysterothylacium Larvae in Commercial Fish from Balearic Sea (Western Mediterranean Sea). Parasitol. Res. 2018, 117, 4003–4012. [Google Scholar] [CrossRef] [PubMed]
  38. Molina-Fernández, D.; Rubio-Calvo, D.; Adroher, F.J.; Benítez, R. Molecular Epidemiology of Anisakis Spp. in Blue Whiting Micromesistius poutassou in Eastern Waters of Spain, Western Mediterranean Sea. Int. J. Food. Microbiol. 2018, 282, 49–56. [Google Scholar] [CrossRef] [PubMed]
  39. Akmirza, A. Metazoan Parasite Fauna of Conger Eel (Conger conger L.) near Gökçeada, Northeasten Aegean Sea, Turkey. Kafkas Univ. Vet. Fak. Derg. 2012, 18, 845–848. [Google Scholar] [CrossRef]
  40. Sanmartín, M.L.; Alvarez, M.F.; Peris, D.; Iglesias, R.; Leiro, J. Helminth Parasite Communities of the Conger Eel in the Estuaries of Arousa and Muros (Galicia, North-West Spain). J. Fish Biol. 2000, 57, 1122–1133. [Google Scholar] [CrossRef]
  41. Santos, M.J.; Castro, R.; Cavaleiro, F.; Rangel, L.; Palm, H.W. Comparison of Anisakid Infection Levels between Two of Atlantic Mackerel (Scomber colias and S. scombrus) off the Atlantic Portuguese Coast. Sci. Mar. 2017, 81, 179–185. [Google Scholar] [CrossRef]
  42. Saldanha, L.; Almeida, A.J.; Andrade, F.; Guerreiro, J. Observations on the Diet of Some Slope Dwelling Fishes of Southern Portugal. Int. Rev. Gesamten. Hydrobiol. 1995, 80, 217–234. [Google Scholar] [CrossRef]
  43. Morato, T.; Solà, E.; Grós, M.P.; Menezes, G. Diets of Forkbeard (Phycis phycis) and Conger Eel (Conger conger) off the Azores during Spring of 1996 and 1997. Arquipelago 1999, 17, 51–64. [Google Scholar]
  44. Matić-Skoko, S.; Ferri, J.; Tutman, P.; Skaramuca, D.; Dikić, D.; Lisičić, D.; Franić, Z.; Skaramuca, B. The Age, Growth and Feeding Habits of the European Conger Eel, Conger conger (L.) in the Adriatic Sea. Mar. Biol. Res. 2012, 8, 1012–1018. [Google Scholar] [CrossRef]
  45. Madrid, E.; Galán-Puchades, M.T.; Fuentes, M.V. Risk Analysis of Human Anisakidosis Through the Consumption of the Blue Whiting, Micromesistius poutassou, Sold at Spanish Supermarkets. Foodborne Pathog. Dis. 2012, 9, 934–938. [Google Scholar] [CrossRef]
  46. Osanz-Mur, A.C. Presencia de Larvas de Anisákidos (Nematoda: Ascaridoidea) en Pescado de Consumo Capturado en la Zona Pesquera de Tarragona. Ph.D. Thesis, Universitat Autonoma de Barcelona, Bellaterra, Spain, 2001. [Google Scholar]
  47. Rello, F.J.; Adroher, F.J.; Valero, A. Hysterothylacium aduncum, the Only Anisakid Parasite of Sardines (Sardina pilchardus) from the Southern and Eastern Coasts of Spain. Parasitol. Res. 2008, 104, 117–121. [Google Scholar] [CrossRef]
  48. Gutiérrez-Galindo, J.F.; Osanz-Mur, A.C.; Mora-Ventura, M.T. Occurrence and Infection Dynamics of Anisakid Larvae in Scomber scombrus, Trachurus trachurus, Sardina pilchardus, and Engraulis encrasicolus from Tarragona (NE Spain). Food Control 2010, 21, 1550–1555. [Google Scholar] [CrossRef]
  49. Herrador, Z.; Daschner, Á.; Perteguer, M.J.; Benito, A. Epidemiological Scenario of Anisakidosis in Spain Based on Associated Hospitalizations: The Tip of the Iceberg. Clin. Inf. Dis. 2019, 69, 69–76. [Google Scholar] [CrossRef] [PubMed]
  50. Roca-Geronès, X.; Alcover, M.M.; Godínez-González, C.; González-Moreno, O.; Masachs, M.; Fisa, R.; Montoliu, I. First Molecular Diagnosis of Clinical Cases of Gastric in Spain. Genes 2020, 11, 452. [Google Scholar] [CrossRef] [PubMed]
  51. López-Serrano, M.C.; Gomez, A.A.; Daschner, Á.; Moreno-Ancillo, Á.; Suarez de Parga, J.M.; Caballero, M.T.; Barranco, P.; Cabañas, R. Gastroallergic Anisakiasis: Findings in 22 Patients. J. Gastroenterol. Hepatol. 2000, 15, 503–506. [Google Scholar] [CrossRef] [PubMed]
  52. González Quijada, S.; González Escudero, R.; Arias García, L.; Gil Martín, A.R.; Vicente Serrano, J.; Corral Fernández, E. Manifestaciones Digestivas de La Anisakiasis: Descripción de 42 Casos. Rev. Clin. Esp. 2005, 205, 311–315. [Google Scholar] [CrossRef]
  53. Klapper, R.; Kuhn, T.; Münster, J.; Levsen, A.; Karl, H.; Klimpel, S. Anisakid Nematodes in Beaked Redfish (Sebastes mentella) from Three Fishing Grounds in the North Atlantic, with Special Notes on Distribution in the Fish Musculature. Vet. Parasitol. 2015, 207, 72–80. [Google Scholar] [CrossRef]
  54. Levsen, A.; Karl, H. Anisakis simplex (s.l.) in Grey Gurnard (Eutrigla gurnardus) from the North Sea: Food Safety Considerations in Relation to Fishing Ground and Distribution in the Flesh. Food Control 2014, 36, 15–19. [Google Scholar] [CrossRef]
  55. Choi, S.J.; Lee, J.C.; Kim, M.J.; Hur, G.Y.; Shin, S.Y.; Park, H.S. The Clinical Characteristics of Anisakis Allergy in Korea. Korean J. Intern. Med. 2009, 24, 160–163. [Google Scholar] [CrossRef]
  56. Sohn, W.M.; Na, B.K.; Kim, T.H.; Park, T.J. Anisakiasis: Report of 15 Gastric Cases Caused by Anisakis Type I Larvae and a Brief Review of Korean Anisakiasis Cases. Korean J. Parasitol. 2015, 53, 465–470. [Google Scholar] [CrossRef]
  57. Chen, H.X.; Zhang, L.P.; Gibson, D.I.; Lü, L.; Xu, Z.; Li, H.T.; Ju, H.D.; Li, L. Detection of Ascaridoid Nematode Parasites in the Important Marine Food-Fish Conger myriaster (Brevoort) (Anguilliformes: Congridae) from the Zhoushan Fishery, China. Parasit Vectors 2018, 11, 274. [Google Scholar] [CrossRef]
  58. Cipriani, P.; Sbaraglia, G.L.; Paoletti, M.; Giulietti, L.; Bellisario, B.; Palomba, M.; Bušelić, I.; Mladineo, I.; Nascetti, G.; Mattiucci, S. The Mediterranean European Hake, Merluccius merluccius: Detecting Drivers Influencing the Anisakis Spp. Larvae Distribution. Fish Res. 2018, 202, 79–89. [Google Scholar] [CrossRef]
  59. Audicana, M.T.; Kennedy, M.W. Anisakis simplex: From Obscure Infectious Worm to Inducer of Immune Hypersensitivity. Clin. Microbiol. Rev. 2008, 21, 360–379. [Google Scholar] [CrossRef]
  60. Mattiucci, S.; Palomba, M.; Nascetti, G. Anisakis. In Encyclopedia of Infection and Immunity; Elsevier: Amsterdam, The Netherlands, 2022; Volume 2, pp. 408–423. [Google Scholar]
Figure 1. Microphotographs showing anterior, central, and posterior regions of the nematodes found in C. conger specimens: (ac) anterior (a), central (b), and posterior (c) regions of L3 of Anisakis type I (sensu Berland, 1961); (df): anterior (d), central (e), and posterior (f) regions of L3 of Anisakis type II (sensu Berland, 1961) (gi): anterior (g), central (h), and posterior (i) regions of an adult of Hysterothylacium spp.; (jl): anterior (j), central (k), and posterior (l) regions of an adult male of Cucullanus sp.; (mo): anterior (m), central (n), and posterior (o) regions of an adult female of Cucullanus sp.; (pr): anterior (p), central (q), and posterior (r) regions of an adult of C. congeri. t: tooth, o: esophagus, v: ventricle, i: intestine, m: mucron, an: anus, l: labia, ic: intestinal caecum, vap: ventricular appendix, spi: spicules, bc: buccal capsule, d:deirids, nr: nerve ring; Scale bar 50 µm in all microphotographs with the exception of b, h and l (100 µm).
Figure 1. Microphotographs showing anterior, central, and posterior regions of the nematodes found in C. conger specimens: (ac) anterior (a), central (b), and posterior (c) regions of L3 of Anisakis type I (sensu Berland, 1961); (df): anterior (d), central (e), and posterior (f) regions of L3 of Anisakis type II (sensu Berland, 1961) (gi): anterior (g), central (h), and posterior (i) regions of an adult of Hysterothylacium spp.; (jl): anterior (j), central (k), and posterior (l) regions of an adult male of Cucullanus sp.; (mo): anterior (m), central (n), and posterior (o) regions of an adult female of Cucullanus sp.; (pr): anterior (p), central (q), and posterior (r) regions of an adult of C. congeri. t: tooth, o: esophagus, v: ventricle, i: intestine, m: mucron, an: anus, l: labia, ic: intestinal caecum, vap: ventricular appendix, spi: spicules, bc: buccal capsule, d:deirids, nr: nerve ring; Scale bar 50 µm in all microphotographs with the exception of b, h and l (100 µm).
Pathogens 12 01326 g001
Table 1. Biometric parameters of the 108 C. conger analyzed.
Table 1. Biometric parameters of the 108 C. conger analyzed.
ParameterMean ± SDRange
Total length (cm)75.3 ± 26.7180.0–29.8
Total weight 1 (g)1252.1 ± 1972.115,000.0–31.9
Eviscerated weight 2 (g)976.3 ± 1293.78200.0–27.4
1 n = 107; 2 n = 106.
Table 2. Descriptive epidemiological results of C. conger infection with larvae of nematode species.
Table 2. Descriptive epidemiological results of C. conger infection with larvae of nematode species.
Parasite SpecieNPrevalence %
(95% CI)
Mean Intensity
(95% CI)
Mean Abundance
(95% CI)
Anisakis type I (sensu Berland, 1961)13133.3 (25.1–42.7)3.6 (2.7–4.6)1.2 (0.7–1.8)
Anisakis type II (sensu Berland, 1961)1810.2 (5.6–17.5)1.6 (1.2–2.1)0.2 (0.05–0.29)
Cucullanus sp.39179.6 (71.0–86.2)4.5 (3.6–5.5)3.6 (2.8–4.5)
Cristitectus congeri6913.0 (7.8–20.7)4.9 (3.2–6.7)0.6 (0.06–1.2)
Hysterothylacium spp.4826.9 (19.4–36.0)1.7 (1.3–2.0)0.4 (0.3–0.6)
Table 3. Fish and crustacean species detected in the stomach of the 78 C. conger specimens with food remains.
Table 3. Fish and crustacean species detected in the stomach of the 78 C. conger specimens with food remains.
SpeciesN. of Preys (%)Range
Fish-Osteichthyes
      Dalophis imberbis (Delaroche, 1809)1 (1.3)-
      Species of Serranus Cuvier, 1816 1 (1.3)-
      Serranus cabrilla (Linnaeus, 1758)2 (2.5)1–1
      Merluccius merluccius (Linnaeus, 1758)1 (1.3)-
      Mullus surmuletus Linnaeus, 17581 (1.3)-
      Mullus barbatus Linnaeus, 17581 (1.3)-
      Gnathophis mystax (Delaroche, 1809)1 (1.3)-
      Family Scombridae Rafinesque, 18151 (1.3)-
      Micromesistius poutassou (Risso, 1827) 15 (19.0)1–4
      Sardina pilchardus (Walbaum, 1792) 8 (10.1)1–3
      Phycis blennoides (Brünnich, 1768)1 (1.3)-
      Conger conger (Linnaeus, 1758)2 (2.5)1–1
      Family Argentinidae Bonaparte, 18461 (1.3)-
      Argentina sphyraena Linnaeus, 17582 (2.5)- 1
      Family Gonostomatidae Cocco, 18381 (1.3)-
      Boops boops (Linnaeus, 1758)1 (1.3)-
      Lepidorhombus boscii (Risso, 1810)1 (1.3)-
      Peristedion cataphractum (Linnaeus, 1758)1 (1.3)-
      Scyliorhinus canicula (Linnaeus, 1758)1 (1.3)-
      Trachyrhynchus trachyrhynchus (Risso, 1810)1 (1.3)-
      Species of Apterichtus Duméril, 18061 (1.3)-
      Pagrus pagrus (Linnaeus, 1758)1 (1.3)-
      Diplodus sargus sargus (Linnaeus, 1758)1 (1.3)-
Crustacea-Decapod
      Scyllarus pygmaeus (Spence Bate, 1888)1 (1.5)-
      Species of Processa Leach, 18152 (3.1)1–1
      Processa canaliculata Leach, 18151 (1.5)-
      Processa edulis (Risso, 1816)1 (1.5)-
      Species of Macropipus Prestandrea, 1833 11 (16.9)1–3
      Macropipus puber (Linnaeus, 1767)11 (16.9)1–4
      Liocarcinus depurator (Linnaeus, 1758)2 (3.1)1–1
      Goneplax rhomboides (Linnaeus, 1758) 8 (12.3)1–4
      Solenocera membranacea (Risso, 1816)1 (1.5)-
      Species of Alpheus Fabricius, 17981 (1.5)-
      Alpheus glaber (Olivi, 1792)1 (1.5)-
      Alpheus macrocheles (Hailstone, 1835)1 (1.5)-
      Galathea strigosa Linnaeus, 1761)1 (1.5)-
      Munida intermedia A. Milne-Edwards & Bouvier, 18992 (3.1)- 1
      Aristeus antennatus (Risso, 1816)1 (1.5)-
      Calappa granulata (Linnaeus, 1758)1-
N.: number; 1 The two specimens were found in the same host.
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Roca-Geronès, X.; Sarrà-Alarcón, L.; Delgado, E.; Alcover, M.M.; Casadevall, M.; Fisa, R. Anisakid Presence in the European Conger, Conger conger, from Spanish Mediterranean Waters. Pathogens 2023, 12, 1326. https://doi.org/10.3390/pathogens12111326

AMA Style

Roca-Geronès X, Sarrà-Alarcón L, Delgado E, Alcover MM, Casadevall M, Fisa R. Anisakid Presence in the European Conger, Conger conger, from Spanish Mediterranean Waters. Pathogens. 2023; 12(11):1326. https://doi.org/10.3390/pathogens12111326

Chicago/Turabian Style

Roca-Geronès, Xavier, Lídia Sarrà-Alarcón, Eulàlia Delgado, Maria Magdalena Alcover, Margarida Casadevall, and Roser Fisa. 2023. "Anisakid Presence in the European Conger, Conger conger, from Spanish Mediterranean Waters" Pathogens 12, no. 11: 1326. https://doi.org/10.3390/pathogens12111326

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