Previous Article in Journal
Genetic Diversity and Phylogeography of Plasmodium vivax Transmission-Blocking Vaccine Candidate Genes pvs47 and pvs48/45 in Honduras
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Human Anisakiosis Risk and Presence of Food-Spoiling Parasites Through the Consumption of the Atlantic Chub Mackerel, Scomber colias, Sold in Spanish Supermarkets

1
Parasites & Health Research Group, Department of Pharmacy, Technological Pharmacy and Parasitology, Faculty of Pharmacy and Food Sciences, Universitat de València, Burjassot, 46100 València, Spain
2
Department of Preventive Medicine and Public Health, Food Sciences, Toxicology and Forensic Medicine, Faculty of Pharmacy and Food Sciences, Universitat de València, Burjassot, 46100 València, Spain
*
Author to whom correspondence should be addressed.
Parasitologia 2025, 5(3), 37; https://doi.org/10.3390/parasitologia5030037
Submission received: 18 April 2025 / Revised: 8 July 2025 / Accepted: 17 July 2025 / Published: 22 July 2025

Abstract

The Atlantic chub mackerel, Scomber colias, is sold in Spain, as well as another species of the genus, like the Atlantic mackerel, S. scombrus, often mistaken to be the same fish. This study aims to analyse the risk of human anisakiosis through the consumption of S. colias, and to clarify if these two species differ regarding this risk. A total of 250 S. colias (125 originating from the Atlantic and 125 from the Mediterranean) were helminthologically analysed using conventional parasitological techniques. Concerning Ascaridoid nematodes, the prevalence of Anisakis type I was higher in the Atlantic than in the Mediterranean. The presence of three other helminth parasites stands out, two other Ascaridoid nematodes, the larvae of Contracaecum spp. and Hysterothylacium spp., the latter a food-spoiling and non-pathogenic parasite. The other helminth found was the intestinal adult of the acanthocephalan Rhadinorhynchus pristis, also non-pathogenic. The comparison of the current results with previously published ones by our research group on S. scombrus show that Anisakis type I prevalence was higher in S. scombrus than in S. colias, making the correct differentiation between them necessary, given their varying risk of human anisakiosis. Furthermore, fish label information is important to prevent the risk of anisakiosis for consumers.

1. Introduction

Two fish species of the genus Scomber are sold in Spain: the Atlantic chub mackerel, Scomber colias, and the Atlantic mackerel, or simply mackerel, S. scombrus. Although they have distinct organoleptic properties, these species are often sold as the same fish. This confusion can be found among sellers as well as consumers, mainly due to the many denominations that both fish have been given locally. Moreover, some fish markets in Spain sell the Atlantic chub mackerel caught in the Mediterranean or in the Atlantic as S. japonicus, while this fish, named chub mackerel or Pacific chub mackerel is another fish species that is not found outside the Pacific Ocean (https://www.fishbase.se/summary/Scomber-japonicus.html, accessed on 8 October 2024). This error concerning the scientific name adds to the confusion, especially for consumers, making it necessary to consult the scientific name of the fish on the labels before purchase. In general, although at first glance the two species seem to be the same fish, they can be differentiated through some morphological characteristics. Compared to the Atlantic mackerel, the Atlantic chub mackerel has a less slender and chubbier body; bigger eyes; a blue-greenish dorsal part with dark, wider and more closely spaced transversal stripes; visible silver spots in the ventral part; and softer, less consistent flesh (https://www.fishbase.se/summary/Scomber-japonicus.html, https://www.fishbase.se/summary/54736, accessed on 8 October 2024).
The consumption of fish has many nutritional benefits and a positive impact on human health. The Atlantic chub mackerel as well as the Atlantic mackerel are oily fish, being very much appreciated because of their taste and the texture of their flesh. As oily fish, they are a good source of polyunsaturated fatty acids and omega 3, which help prevent cardiovascular diseases. They have a high protein content, while the carbohydrate content is low. As they are fatty fish, they contain a higher amount of liposoluble vitamins (A, D, and E) than vitamins of the B group [1].
Given the many ways in which they can be prepared, they enjoy a great deal of culinary appreciation [2]. Both fish are usually eaten after having been oven-baked, fried, or grilled, as well as conserved in tins. However, their raw consumption has been increasing, being marinated with lemon juice and vinegar, smoked, as ceviche, sushi, and tartar, but the consumption of fish, especially raw fish, can pose several health risks for consumers. Fish may carry several biological pathogens, such as viruses, bacteria, and parasites, that cause certain foodborne diseases worldwide [3], e.g., Anisakid parasites, if the preventive measures are not properly applied.
Nevertheless, neither of the two Scomber species is usually among the main carriers of Anisakid parasites in Spain, although the consumption of these fish may pose the risk of human parasitisation. Anisakidosis, considered an emerging disease in several countries, such as Spain, is a parasitic disease caused by the consumption of insufficiently heat-treated or not sufficiently frozen parasitised fish. It is caused by nematodes of the family Anisakidae, mainly Anisakis simplex s.s. and other cryptic species included in the Anisakis simplex (s.l.) complex, which is the reason why anisakiosis, or anisakiasis, is the most common denomination of this parasitosis [4,5]. Humans act as accidental hosts in the biological cycle of Anisakids. The symptomatology of human anisakidosis may include gastrointestinal discomfort and/or allergic reactions, which can even occur after the fish has been heat-treated, as some Anisakid proteins, causing the allergies, are thermoresistant [6,7].
Spain has the highest incidence of anisakidosis cases in Europe and the second highest worldwide after Japan where cases occur mainly through traditional raw fish dishes such as sushi and sashimi [8]. In Spain, although the number of reported cases of anisakidosis is about 150 per year [8], this parasitosis is underdiagnosed; a predictive model based only on the consumption of raw anchovies marinated in vinegar, a typical and very popular local dish called “boquerones”, estimated the annual number of cases in Spain to be above 8000 [9].
To prevent anisakidosis, it is advisable to apply the preventive measures recommended by EFSA (European Food Safety Authority) in Commission Regulation (EU) No 1276/2011 of 8 December 2011 amending Annex III to Regulation (EC) No 853/2004 of the European Parliament and of the Council as regards the treatment to kill viable parasites in fishery products for human consumption (https://eur-lex.europa.eu/eli/reg/2011/1276/oj/eng, accessed on 21 January 2025). These measures include, for example, cooking fish at a core temperature of 60 °C or more for at least one minute, respectively, freezing the fish at −20 °C for no less than 24 h, or −35 °C for no less than 15 h.
The main objective of this study is to analyse the presence of Ascaridoid nematodes and other helminth parasites in S. colias, and, in particular, concerning the risk of human anisakiosis through their consumption. Moreover, as two Scomber species, S. colias and S. scombrus are frequently consumed in Spain, a secondary objective focuses on the potential differences in human anisakiosis risk after their consumption.

2. Materials and Methods

2.1. Samples and Parasitological Procedures

The fish analysed herein correspond to the Atlantic chub mackerel, S. colias, purchased at branches of nationwide Spanish supermarket chains, chosen at random, but with different weights and lengths and captured in various seasons in the Atlantic Ocean and the Mediterranean Sea. The fish were purchased fresh and uneviscerated, and all available information about the fish specimens was obtained from the fish crate labels at the selling point (scientific and common names, date of capture, and origin, including FAO major fishing area, subarea, and division).
The material of S. colias consisted of 250 specimens originating from the northeast Atlantic (n = 125), FAO zone 27, subareas VIII and IX, and from the western Mediterranean (n = 125), FAO zone 37, division 1.1. The sampling took place in the following years: 2011 (n = 54), 2012 (n = 57), 2018 (n = 91), and 2022 (n = 48). The range of days passed since the date of capture and the date of the analysis (Table 1), which also corresponds to the hypothetical date of consumption, was between 1 and 8 days. A part of the S. colias sample, concretely 108 individuals [10] (wrongly identified in that publication as S. japonicus), was previously analysed by our research team. However, the current study includes the statistical and epidemiological analysis of a total of 250 S. colias specimens as an entirely new sample, and consequently the results obtained will be different.
All fish specimens were preserved at 4 °C in the laboratory. Before their dissection, each fish was measured and weighed, and these individual data, together with those obtained from the fish crate labels, were introduced in the corresponding database. After the dissection of each specimen, the viscera were transferred to a Petri dish containing saline solution NaCl 0.9% examined under a stereoscopic microscope and helminths were collected. The flesh, after visual inspection, underwent artificial enzymatic digestion [11]. The resulting product from the digestion was also examined under a stereoscopic microscope.
All helminths collected were identified based on their morphology and morphometry and according to the most relevant descriptions of the scientific literature. Larvae of Ascaridoid nematodes, found in the viscera and/or flesh, were cleared in Amann lactophenol in non-permanent whole mounts and were identified at the genus level considering their main morphological characteristics [12,13] as follows: the position of the excretory pore, the arrangement and separation of the digestive tract into the oesophagus, ventricle and the presence/absence of structures such as intestinal caeca and the oesophageal appendix, as well as the shape of the tail. In the case of the genus Anisakis, the differentiation between two groups of larvae (Anisakis type I and type II) was also carried out. A molecular diagnosis of each specimen at the specific level was not carried out, as the study is mainly aimed at informing consumers about the presence of Ascariodid nematode larvae and how to minimise the risk of anisakiosis through the consumption of the Atlantic chub mackerel. Adult acanthocephalan specimens, the other kind of helminths found in the intestine only, were initially preserved in 70% ethanol, stained with alcoholic hydrochloric carmine, differentiated with acidified ethanol, dehydrated in an alcohol series, cleared with xylene and mounted in Canada balsam. These helminths were then identified at the specific level according to their morphological and morphometric characteristics [14,15,16].

2.2. Statistical Analysis

The number of parasitised hosts, prevalence, mean intensity ±SD, and range of parasitisation were analysed according to Bush et al. [17], also considering the geographical origin of the fish, for the total and each genus of nematode Ascaridoid larvae identified, as well as for the other helminths found in the fish analysis.
The potential risk of human anisakiosis was assessed through the analysis of the influence of intrinsic (parasitisation site, weight, and length) and extrinsic factors (origin, season, and days after capture) on the prevalence and intensity of larvae identified as Anisakis type I. The extrinsic factor “season of capture” has been divided into two categories, “autumn”, which corresponds to captures made between November and December, and “winter–spring” for captures made from January to June. The complete statistical analysis comprised the comparison of prevalence (χ2 test) and intensity (Mann–Whitney U test in the case of season of capture, weight and length groups, and Wilcoxon Z test in the case of parasitisation sites—viscera and flesh). The possible influence of the number of days after capture (which corresponds to the theoretical day of consumption) on the presence of larvae in the flesh was also analysed by Binary Logistic Regression (BLR), considering parasitised hosts only. Furthermore, Spearman’s rank correlation coefficient (Rho) was also applied to analyse the potential influence of quantitative intrinsic factors (weight and length) on the Anisakis type I intensity, as well as their influence on the proportion of larvae in the flesh. In this latter case, and with the aim to shed light on whether there is a correlation between the fish size and the presence of Anisakis type I in the flesh of the Atlantic chub mackerel, Spearman’s rank correlation coefficient was applied once more. The correlation was carried out considering the quantitative values of weight and length of the fish as independent variables. The logarithm (X/1 − X) of the proportion number of Anisakis type I in the flesh relative to the total number of Anisakis type I in each fish was considered as the dependent variable, considering only parasitised fish with the presence of Anisakis type I in the flesh, i.e., only the parasitised fish specimens which presented Anisakis type I larvae in the flesh, with X being the centesimal expression of the percentages.
Statistical significance was established at p < 0.05. The IBM SPSS Statistics 29.02 for Windows software package was used for statistical analysis.

3. Results

The helminthological analysis of the 250 Atlantic chub mackerel specimens showed the presence of three Ascaridoid nematode larva morphotypes belonging to the families Anisakidae, Anisakis type I (n = 799) and Contracaecum spp. (n = 3), and Raphidascarididae, Hysterothylacium spp. (n = 12). Larvae of Anisakis type I were found in the viscera and other cavities, as well as in the flesh of Atlantic chub mackerel specimens caught in the Atlantic and in the Mediterranean. However, larvae of Contracaecum spp. and Hysterothylacium spp. were found in the viscera and other body cavities only, not in the flesh, and those of Contracaecum were found in the Mediterranean fish only.
Apart from Ascaridoid nematode larvae, 330 adults of acantocephalan helminths were found in the intestine of Atlantic chub mackerels from both origins. Unfortunately, the other helminths (trematodes in 8 fish, cestodes in 5, and other nematodes in another 5) were not identified at that moment and the material was not preserved. The acanthocephalans were identified as Rhadinorhynchus pristis (Rhadinorhynchidae) based on the most relevant morphological and morphometric characterisation of some of the helminths (only females) analysed (Figure 1): a proboscis with various rows of approximately 24 hooks each (root: 20.4–28.0 µm; length: 53.5–124.9 µm); body length: 18.0–75.0 mm; body width at proboscis area: 208.4–286.5 µm, at the mid-body area: 390.7–677.3 µm, and at the posterior area: 338.6–781.5 µm.

3.1. Origin of the Fish Caught

Data concerning prevalence and mean intensity of Ascaridoid nematode larvae and R. pristis with respect to their geographic origin are shown in Table 2 and Table 3. The origin of the fish caught presented statistically significant differences with respect to prevalences and mean intensity of the total Ascaridoid nematode larvae, larvae of Anisakis type I and the acanthocepalan, always reaching a higher parasitisation rate in the fish originating from the Atlantic than in those of Mediterranean origin. The statistical parameters were as follows: χ2 = 11.7, p < 0.001, Odds Ratio (OR) = 2.7–95% CI 1.6–4.7 in the Ascaridoid nematode larvae; χ2 = 17.4, p < 0.001, OR = 3.5–95% CI 2.0–6.4 in Anisakis type I larvae; and χ2 = 10.9, p = 0.001, OR = 2.8–95% CI 1.5–5.0 in R. pristis.

3.2. Parasitisation Sites of Anisakis Type I Larvae

Parasitisation prevalence by Anisakis type I larvae in the viscera was higher than in the flesh (Table 4), with statistically significant differences in the Atlantic origin (χ2 = 30.6, p < 0.001) as well as in the Mediterranean (χ2 = 10.2, p = 0.001). The same result was obtained concerning the larval burden in both origins (Table 5), Z = 6.1, p < 0.001 in the Atlantic sample and Z = 3.4, p = 0.001 in the Mediterranean sample.

3.3. Season of Capture

The season of capture (Table 4 and Table 5) had no significant influence neither on the prevalence of Anisakis type I larvae in either origin of capture, although there were slightly, but interesting, differences in this parasitisation parameter: the prevalence was higher in the winter–spring season in the fish from the Atlantic, while in the Mediterranean it was higher in autumn. However, the analysis of the larval intensity showed statistical significant differences, being higher in the larval burden in fish caught in autumn in both origins, the Atlantic (U = 62.0; p < 0.001) and the Mediterranean (U = 20.5; p = 0.07).

3.4. Fish Size

The results of Spearman’s rank correlation coefficient (Rho) relating the intensity of Anisakis type I larvae parasitism to the weight and length values of the Atlantic chub mackerel showed statistically significant results only in the Mediterranean population: a positive correlation between the number of larvae and the weight (Rho = 0.7, p < 0.001) and length (Rho = 0.7, p < 0.001) of the fish.
On the other hand, Spearman’s rank correlation coefficient showed a negative correlation between the migration of Anisakis type I larvae to the flesh and the variables weight (Rho = −0.662, p = 0.019) and length (Rho = −0.636, p = 0.026) of the Atlantic sample. Therefore, it can be affirmed that the lower the weight and the shorter the length of the fish, the more migration of Anisakis type I larvae into the flesh of specimens of Atlantic origin. In fish from the Mediterranean Sea, this analysis could not be carried out as only three Anisakis type I larvae were found in the flesh.

3.5. Days Passed After Capture

As the Atlantic chub mackerel presented low numbers of Anisakis type I in the flesh, 12 (1–7 days passed after capture) in the Atlantic and only 3 (1–3 days passed after capture) in the Mediterranean specimens, it was not possible to analyse whether there was increased migration of larvae into the flesh along the days passed since the day of capture.

4. Discussion

The analysis of the 250 Atlantic chub mackerel specimens in this study revealed the presence of three Ascaridoid nematode larvae, with Anisakis type I being the most prevalent and the most abundant. However, the other two morphotypes, Contracaecum spp., also with zoonotic potential and present only in fish from the Mediterranean, and Hysterothylacium spp. showed a low degree of parasitisation.
The chub mackerel species most studied is the Pacific chub mackerel, S. japonicus, in Japan and Korea, due to its high commercial value as well as the tradition of consuming it raw. However, the high prevalence and parasite burden of Anisakid larvae reported make its raw consumption a public health concern [18,19]. Nevertheless, there are also several studies carried out on the Atlantic chub mackerel, S. colias, sometimes wrongly identified as S. japonicus, mainly in the Atlantic Ocean, but also in the Mediterranean Sea. These studies have reported results which diverge from ours concerning the risk of potential human anisakiosis. Debenedetti et al. [10] found in the global study of 108 specimens, in the case of Anisakis type I, a prevalence of 19% and a mean intensity (mI) of 9.6 in fish caught in the Atlantic Ocean, and a prevalence of 14% and an mI of 1.2 in the Mediterranean Sea. These values are lower than those of the current study, except for the prevalence in the Mediterranean Sea which is similar. In fish caught from the east Atlantic areas, some studies reported higher values of prevalence, but lower mI values than in the present study, such as: 92% and an mI of 10.9 in the Azores [20]; 54–70% and an mI of 1.9–2.2 in Madeira Island [20,21]; 67% and an mI of 9.4 in the ICES areas [22]; 56–62% and an mI of 5.1 in Morocco [20,23]; and 85% and an mI of 21.7 off the Portuguese coast, the only study that reported a higher mI value than in the current study in the Atlantic areas [24]. Only the studies carried out in the Canary Islands and Mauritania reported a lower prevalence, 12–27% and an mI of 1.3–2.1 and 12% and an mI of 1.7, respectively [20,25]. Concerning the Mediterranean sample, similar comparative results have been obtained, with reports of higher prevalences than those of the present study: 96–100% and an mI of 9.1–15.1 in Sardinia [26,27]; 75–100% and an mI of 13.8–18.4 in the Aegean Sea [28,29]; 57% in Moroccan waters [23]; 67–100% and an mI of 10.5–254.1 in the Adriatic Sea [30,31,32]; 56% and in the Tyrrhenian Sea [33]; and 42% and an mI of 5.8 off the Libyan coast [34]. Moreover, surprisingly, a very high prevalence (43%) of Hysterotylacium spp. was also reported in Libyan waters [34].
On the other hand, concerning the finding of the acanthocephalan R. pristis, this helminth, sometimes synonymized with R. tenuicornis, has been reported in previous studies from the Atlantic Ocean (Madeira, continental Portugal and the north of Africa) parasitising S. colias (reported as S. japonicus) and S. scombrus [14,15,35,36], making it the only Rhadinorhynchid acanthocephalan present in the Atlantic chub mackerel, at least in those waters. It is noteworthy that this is the first time that S. colias has been reported to be parasitised by this acanthocephalan in the Mediterranean Sea.
Larvae of Hysterothylacium spp., the adults of the acanthocephalan R. pristis, as well as the other adults of trematodes, cestodes, and other nematodes, but not identified at the genus level, found in the intestine or other body cavities of the Atlantic chub mackerel, should be considered food-spoiling parasites, since they are not zoonotic parasites but may prompt consumers to reject the fish.
The results obtained in this regional study from Valencia can easily be extrapolated to the whole of Spain, as the nationwide supermarket chains surveyed sell fish originating from almost the same fishing areas.

4.1. Influence of the Origin of the Fish Caught

As in previous studies carried out on the Atlantic chub mackerel [20,23,37], as well as on other fish species, such as the Atlantic mackerel [38] and the horse mackerel [39], the Anisakis type I prevalence as well as its burden in the sample caught in the Atlantic Ocean were higher than in the Mediterranean sample.
Generally, the higher parasitisation found in the Atlantic Ocean is likely to be due to the larger size of the Atlantic, which means that there are a higher abundance of definitive and intermediate hosts in this area [40,41], i.e., its ecosystem is more suitable for the development of the Anisakid life cycle, e.g., the lower temperature of the Atlantic waters when compared to the Mediterranean [42]. Moreover, it should be highlighted that the sample analysed from the Mediterranean Sea in the current study originated from FAO zone 37, division 1.1—specifically, the Balearic region, which traditionally has a lower presence of Anisakid larvae than other Mediterranean regions, such as the Aegean, Adriatic and Tyrrhenian Seas [28,29,30,31,32,33].

4.2. Influence of the Season of Capture

The influence of the season of capture on the Anisakis type I parasitisation was statistically significant only when considering the entire sample, showing a higher parasitisation in individuals caught in autumn. This result agrees with those reported by Abattouy et al. in Morocco [23], where the highest prevalence was found in winter and autumn. However, some other studies in the Mediterranean found a higher parasitisation rate in the Atlantic chub mackerels caught in summer off the Libyan coast [34] and Southern Albania (Adriatic Sea) [32]. These possible seasonal fluctuations of parasitisation could be related to the mean intensity or scarcity and temporary fluctuations of the intermediate host [43], zooplankton (small euphausiid crustaceans) infected by Anisakis spp., and to the seasonal variability of abiotic and biotic environmental factors that influence the migration of cetaceans [22,30].

4.3. Influence of the Fish Size

The influence of the size of the Atlantic chub mackerel (length and weight) did apparently not have any clear influence on the Anisakis type I parasitisation. These results are similar to other previously reported results concerning this fish species [8,34]. Only studies concerning Portugal [21] and the Adriatic Sea [37] reported a positive influence of the fish size on parasitisation. However, the higher parasitisation of larger specimens has also been demonstrated in previous studies [10,38,44,45,46], validating the hypothesis that larger fish individuals, as they are higher up in the food chain, are more likely to be parasitised, due to the greater ingestion of potential intermediate or paratenic hosts and the accumulation of parasites, with the ensuing accumulation of larvae with time, leading to a higher level of abundance and prevalence [47].

4.4. Parasitisation Sites and Migration

Although the natural microhabitat of Anisakid larvae in fish is their viscera and other body cavities [48], it has been suggested that migration, mainly of Anisakis spp., to the flesh while the fish is alive is more frequent in fatty fish than in white fish species [49]. Even though the Atlantic chub mackerel is a blue fish, parasitisation of the viscera is still higher than in the flesh. On the other hand, as human parasitisation by Anisakids is due to the consumption of flesh rather than viscera, it is important to know whether certain factors, such as temperature [10,50], pH [51], fish size [52,53], or even the days passed between the catch and consumption, could affect the migration of larvae to the flesh. Some authors reported that Anisakis spp. larvae are able to migrate from the visceral organs to the flesh after the death of the host, suggesting that this movement may be facilitated by the cold storage or processing of uneviscerated fish [38,44,45,54], in contrast to other research suggesting that keeping the fish at a low temperature could reduce larval migration [50].
In the case of Atlantic chub mackerel, no relation between the migration of larvae to the flesh and the days passed after the catch was found. This lack of relation could be due to the low prevalence of Anisakis type I in the flesh, or that, as suggested in other previous studies in some blue fish [50,55], larvae migrate to the flesh even intra vitam, and consequently, the days passed before consumption may not be as decisive in larval migration in the case of Atlantic chub mackerel. However, studies carried out in other Scomber species, such as Atlantic mackerel [38], but also in blue whiting [44] and European hake [45], reported a positive correlation between the days passed after the catch and the migration of larvae to the flesh, also suggesting that this migration could be facilitated by the cold storage of the fish or by its processing without prior evisceration. In our opinion, this could also occur in the Atlantic chub mackerel, although this has not been found in the present study, emphasising the importance of the consumption of fresh fish versus long storage without evisceration or convenient freezing. Concerning the fish size, migration to the flesh in the case of parasitised fish showed a negative correlation in the Atlantic sample. This result supports the hypothesis that the percentage of larvae in the flesh should be inversely related to the fish size as the migratory distance to the flesh increases with the fish size, as previously reported in other fish. The sardine is an example of a blue fish, although the total presence of larvae in the flesh is very low [46]; blue whiting [53] and hake [45] are examples of white fish. However, it is important to consider that other factors, such as the number of total larvae in the fish, could be related to the number of larvae in the flesh [45].

4.5. Scomber colias vs. Scomber scombrus: Human Anisakiosis Risk Comparison

The comparative analysis of the results of the present study with those reported by [38] and [10] in their study of 231 Atlantic mackerel specimens, S. scombrus, originating from the northeast Atlantic (n = 140) and the western Mediterranean (n = 91), and analysed in the same way as the current study of S. colias, showed that both the global prevalence and mean intensity of Anisakis type I larvae were higher than in the Atlantic chub mackerel, and that these two parameters of parasitisation were also higher in the Atlantic sample than in the Mediterranean. Moreover, in S. scombrus, in addition to presenting a greater parasitism of larvae in the flesh, contrary to what occurred in S. colias, a significant correlation between the presence of larvae in the flesh and the number of days passed between the catch and the analysis was found. Additionally, larvae of Contracaecum spp. were not found in the Atlantic mackerel sample, and larvae of Hysterothylacium spp. were found only in the Atlantic sample, although the prevalence of these two genera of Ascaridoid nematodes is low in both Scomber species. Furthermore, although the acantocephalan R. pristis has previously been reported to parasitize both Scomber species, after the analysis of almost 500 specimens it has been reported in the S. colias sample only. These results emphasise the importance for consumers to be able to differentiate both Scomber species at the selling point due to the lower Anisakid parasitisation of, particularly, Anisakis type I, in the Atlantic chub mackerel, and, consequently, a lower risk of human anisakidosis through its consumption. Nevertheless, a potential risk of infection cannot be discarded, and therefore, even the Atlantic chub mackerel should be consumed after implementing appropriate preventive measures. To date, freezing and heating remain the most efficient methods to kill Anisakid larvae in fresh fishery products, as referred to in European legislation [56], with a cooking temperature of 60 °C or higher for 1 min in the centre of the piece, or, if they are to be consumed raw or semi-raw, to be frozen at −20 °C for at least 5 days.

5. Conclusions

The human anisakiosis risk through the consumption of the Atlantic chub mackerel can be confirmed as an intermediate risk. Furthermore, this risk decreases when the fish originate from the Mediterranean Sea as opposed to the Atlantic Ocean, and if, within the Mediterranean Sea, they originate from the Balearic division as opposed to others in the central and eastern Mediterranean. Additionally, it is important for consumers to check the information on the crate label at the selling point to certify the Scomber species and its origin, as these are important factors that can influence the risk of anisakiosis for humans. However, although the consumption of the Atlantic chub mackerel does not pose a high risk for humans, consumers are still advised to take preventive measures to reduce this risk.

Author Contributions

Conceptualization, M.V.F.; Formal Analysis, M.V.F., E.M. and Á.L.D.; Investigation, M.V.F., I.R., A.T., E.M., Á.L.D., S.S.-D. and M.T.; Resources, M.V.F. and M.T.; Data Curation, M.V.F.; Writing—Original Draft Preparation, M.V.F., I.R., A.T. and E.M.; Writing—Review and Editing, M.V.F.; Visualisation, M.V.F., I.R., A.T., E.M., Á.L.D., S.S.-D. and M.T.; Supervision, M.V.F.; Project Administration, M.V.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The database used to carry out the present study is not publicly available due to internal policy of our departments. However, the database could be available, after a justification of its use, upon request from the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. MAGRAMA (Ministerio de Agricultura, Alimentación y Medio Ambiente). Ministerio de Agricultura, Alimentación y Medio Ambiente. El Mercado de la Caballa en España. 2017. Available online: https://www.mapa.gob.es/en/pesca/temas/mercados-economia-pesquera/informecaballa2017_tcm38-437224.pdf (accessed on 21 January 2025).
  2. Illescas, J.L.; Bacho, O.; Ferrer, S. Pescados y Mariscos. Guía Práctica; Empresa Nacional Mercasa: Madrid, Spain, 2008; p. 211. [Google Scholar]
  3. Ziarati, M.; Zorriehzahra, M.J.; Hassantabar, F.; Mehrabi, Z.; Dhawan, M.; Sharun, K.; Emran, T.B.; Dhama, K.; Chaicumpa, W.; Shamsi, S. Zoonotic diseases of fish and their prevention and control. Vet. Q. 2022, 42, 95–118. [Google Scholar] [CrossRef] [PubMed]
  4. Buchmann, K.; Mehrdana, F. Effects of anisakid nematodes Anisakis simplex (s.l.), Pseudoterranova decipiens (s.l.) and Contracaecum osculatum (s.l.) on fish and consumer health. Food Waterborne Parasitol. 2016, 4, 13–22. [Google Scholar] [CrossRef]
  5. Adroher-Auroux, F.J.; Benítez-Rodríguez, R. Anisakiasis and Anisakis: An underdiagnosed emerging disease and its main etiological agents. Res. Vet. Sci. 2020, 132, 535–545. [Google Scholar] [CrossRef] [PubMed]
  6. 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] [PubMed]
  7. Audicana, M.T.; Ansotegui, I.J.; Kennedy, M.W. Anisakis simplex: Dangerous-dead and alive? Trends Parasitol. 2002, 18, 20–25. [Google Scholar] [CrossRef] [PubMed]
  8. Herrador, Z.; Daschner, A.; Perteguer, M.J.; Benito, A. Epidemiological scenario of anisakidosis in Spain based on associated hospitalizations: The tipping point of the iceberg. Clin. Inf. Dis. 2019, 69, 69–76. [Google Scholar] [CrossRef] [PubMed]
  9. Bao, M.; Pierce, G.J.; Pascual, S.; González-Muñoz, M.; Mattiucci, S.; Mladineo, I.; Cipriani, P.; Bušelić, I.; Strachan, N.J. Assessing the risk of an emerging zoonosis of worldwide concern: Anisakiasis. Sci. Rep. 2017, 7, 43699. [Google Scholar] [CrossRef] [PubMed]
  10. Debenedetti, A.L.; Madrid, E.; Trelis, M.; Codes, F.J.; Gil-Gómez, F.; Sáez-Durán, S.; Fuentes, M.V. Prevalence and risk of anisakid larvae in fresh fish frequently consumed in Spain: An overview. Fishes 2019, 4, 13. [Google Scholar] [CrossRef]
  11. Llarena-Reino, M.; Piñeiro, C.; Antonio, J.; Outeriño, L.; Vello, C.; González, A.F.; Pascual, S. Optimization of the pepsin digestion method for anisakids inspection in the fishing industry. Vet. Parasitol. 2013, 191, 276–283. [Google Scholar] [CrossRef] [PubMed]
  12. Berland, B. Identification of larval nematodes from fish. In Nematode Problems in North Atlantic Fish; Report from a Work-shop in Kiel, 3–4 April 1989; Möller, H., Ed.; International Council for Exploration of the Sea: Kiel, Germany, 1989; pp. 15–22. [Google Scholar]
  13. Grabda, J. Marine Fish Parasitology: An Outline; PWN-Polish Scientific Publisher: Warszawa, Poland, 1991; p. 306. [Google Scholar]
  14. De Oliveira-Rodrigues, H.; Noronha, D.; Carvalho-Varela, M. Alguns acantocéfalos de peixes do Oceano Atlántico, costa continental portuguesa e costa do norte da África. Mem. Inst. Oswaldo Cruz 1975, 73, 209–214. [Google Scholar] [CrossRef]
  15. Arandas-Rêgo, A. Rhadinorhynchus pristis (Rudolphi, 1802) acanthocephalan parasite of fishes, Scomber scombrus and S. japonicus. Some observations on the scanning electron microscope. Mem. Inst. Oswaldo Cruz 1987, 82, 287–288. [Google Scholar] [CrossRef]
  16. Monks, S. Phylogeny of the Acanthocephala based on morphological characters. Syst. Parasitol. 2001, 48, 81–116. [Google Scholar] [CrossRef] [PubMed]
  17. 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] [PubMed]
  18. Suzuki, J.; Murata, R.; Hosaka, M.; Araki, J. Risk factors for human Anisakis infection and association between the geographic origins of Scomber japonicus and anisakid nematodes. Int. J. Food Microbiol. 2010, 137, 88–93. [Google Scholar] [CrossRef] [PubMed]
  19. Bak, T.J.; Jeon, C.H.; Kim, J.H. Occurrence of anisakid nematode larvae in chub mackerel (Scomber japonicus) caught off Korea. Int. J. Food Microbiol. 2014, 191, 149–156. [Google Scholar] [CrossRef] [PubMed]
  20. Costa, G.; Cavallero, S.; D’Amelio, S.; Paggi, L.; García-Santamaría, M.T.; Borges-Perera, C.; Santos, M.J.; Khadem, M. Helminth parasites of the Atlantic chub mackerel, Scomber colias Gmelin, 1789 from Canary Islands, Central North Atlantic, with comments on their relations with other Atlantic regions. Acta Parasitol. 2011, 56, 98–104. [Google Scholar] [CrossRef]
  21. Costa, G.; Pontes, T.; Mattiucci, S.; D’Amélio, S. The occurrence and infection dynamics of Anisakis larvae in the black-scabbard fish, Aphanopus carbo, chub mackerel, Scomber japonicus, and oceanic horse mackerel, Trachurus picturatus from Madeira, Portugal. J. Helminthol. 2003, 77, 163–166. [Google Scholar] [CrossRef] [PubMed]
  22. Rodríguez, H.; Abollo, E.; González, A.F.; Pascual, S. Scoring the parasite risk in highly-valuable fish species from southern ICES areas. Fish. Res. 2018, 202, 134–139. [Google Scholar] [CrossRef]
  23. Abattouy, N.; Valero, A.; Benajiba, M.H.; Lozano, J.; Martín-Sánchez, J. Anisakis simplex s.l. parasitization in mackerel (Scomber japonicus) caught in the North of Morocco—Prevalence and analysis of risk factors. Int. J. Food Microbiol. 2011, 150, 136–139. [Google Scholar] [CrossRef] [PubMed]
  24. Santos, M.J.; Castro, R.; Cavaleiro, F.; Rangel, L.; Palm, H.W. Comparison of anisakid infection levels between two species of Atlantic mackerel (Scomber colias and S. scombrus) off the Atlantic Portuguese coast. Sci. Mar. 2017, 81, 179–185. [Google Scholar] [CrossRef]
  25. Martin-Carrillo, N.; García-Livia, K.; Baz-González, E.; Abreu-Acosta, N.; Dorta-Guerra, R.; Valladares, B.; Foronda, P. Morphological and molecular identification of Anisakis spp. (Nematoda: Anisakidae) in commercial fish from the Canary Islands coast (Spain): Epidemiological data. Animals 2022, 12, 2634. [Google Scholar] [CrossRef] [PubMed]
  26. 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] [PubMed]
  27. Casti, D.; Scarano, C.; Piras, M.C.; Merella, P.; Muglia, S.; Piras, F.; Garippa, G.; Spanu, C.; De Santis, E.P.L. Occurrence of nematodes of the genus Anisakis in Mediterranean and Atlantic fish marketed in Sardinia. Ital. J. Food Saf. 2017, 6, 6185. [Google Scholar] [CrossRef] [PubMed]
  28. Chaligiannis, I.; Lalle, M.; Pozio, E.; Sotiraki, S. Anisakidae infection in fish of the Aegean Sea. Vet. Parasitol. 2012, 184, 362. [Google Scholar] [CrossRef] [PubMed]
  29. Pekmezci, G.Z.; Onuk, E.E.; Bolukbas, C.S.; Yardimci, B.; Gurler, A.T.; Acici, M.; Umur, S. Molecular identification of Anisakis species (Nematoda: Anisakidae) from marine fishes collected in Turkish waters. Vet. Parasitol. 2014, 201, 82–94. [Google Scholar] [CrossRef] [PubMed]
  30. Mladineo, I.; Poljak, V. Ecology and genetic structure of zoonotic Anisakis spp. from Adriatic commercial fish species. Appl. Environ. Microbiol. 2014, 80, 1281–1290. [Google Scholar] [CrossRef] [PubMed]
  31. Goffredo, E.; Azzarito, L.; Di Taranto, P.; Mancini, M.E.; Normanno, G.; Didonna, A.; Faleo, S.; Occhiochiuso, G.; D’Attoli, L.; Pedarra, C.; et al. Prevalence of anisakid parasites in fish collected from Apulia region (Italy) and quantification of nematode larvae in flesh. Int. J. Food Microbiol. 2019, 292, 159–170. [Google Scholar] [CrossRef] [PubMed]
  32. Ozuni, E.; Vodica, A.; Castrica, M.; Brecchia, G.; Curone, G.; Agradi, S.; Miraglia, D.; Menchetti, L.; Balzaretti, C.M.; Andoni, E. Prevalence of Anisakis larvae in different fish species in southern Albania: Five-year monitoring (2016–2020). Appl. Sci. 2021, 11, 11528. [Google Scholar] [CrossRef]
  33. Gazzonis, A.L.; Cavallero, S.; Zanzani, S.A.; Olivieri, E.; Malandra, R.; Ranghieri, V.; D’Amelio, S.; Manfredi, M.T. Anisakis sp. and Hysterothylacium sp. larvae in anchovies (Engraulis encrasicolus) and chub mackerel (Scomber colias) in the Mediterranean Sea: Molecular identification and risk factors. Food Control 2017, 80, 366–373. [Google Scholar] [CrossRef]
  34. Cavallero, S.; El Sherif, R.A.; Pizzarelli, A.; El Fituri, A.A.; El Showhdi, M.; Benmosa, F.; D’Amelio, S. Occurrence of Anisakis and Hysterothylacium nematodes in Atlantic chub mackerels from Libyan coasts. Helminthologia 2019, 56, 347–352. [Google Scholar] [CrossRef] [PubMed]
  35. Arandas-Rêgo, A.; Carvalho-Varela, M.; Mendonça, M.M.; Afonso-Roque, M.M. Helminofauna da sarda (Scomber scombrus L. ) peixe da costa continental Portuguesa. Mem. Inst. Oswaldo Cruz 1985, 80, 97–100. [Google Scholar] [CrossRef]
  36. Costa, G.; Pontes, T.; Arandas-Rêgo, A. Prevalence, intensity and abundance of Rhadinorhynchus pristis (Acanthocephala, Rhadinorhynchidae) in chub mackerel, Scomber japonicus (Pisces, Scombridae) from Madeira Island. Acta Parasitol. 2004, 49, 41–44. [Google Scholar]
  37. Debenedetti, A.L.; Codes, F.; Laza, S.; Hernández, S.; Madrid, E.; Trelis, M.; Fuentes, M.V. Ascaridoid nematodes in horse mackerel, Trachurus trachurus, sold in Spanish supermarkets—Factors able to diminish consumer risk. Fish. Res. 2020, 230, 105669. [Google Scholar] [CrossRef]
  38. Madrid, E.; Gil, F.; García, M.; Debenedetti, Á.L.; Trelis, M.; Fuentes, M.V. Potential risk analysis of human anisakiasis through the consumption of mackerel, Scomber scombrus, sold at Spanish supermarkets. Food Control 2016, 66, 300–305. [Google Scholar] [CrossRef]
  39. Arthur, J.R.; Margolis, L.; Whitaker, D.J.; McDonald, T.E. A quantitative study of economically important parasites of walleye pollock (Theragra chalcogramma) from British Columbian waters and effects of post-mortem handling on their abundance in the musculature. Can. J. Fish. Aquat. Sci. 1982, 39, 710–726. [Google Scholar] [CrossRef]
  40. Boily, F.; Marcogliese, D.J. Geographical variations in abundance of larval anisakine nematodes in Atlantic cod (Gadus morhua) and American plaice (Hippoglossoides platessoides) from the Gulf of St. Lawrence. Can. J. Fish. Aquat. Sci. 1995, 52, 105–115. [Google Scholar] [CrossRef]
  41. Højgaard, D.P. Impact of temperature, salinity and light on hatching of eggs of Anisakis simplex (Nematoda, Anisakidae), isolated by a new method, and some remarks on survival of larvae. Sarsia 1998, 83, 21–28. [Google Scholar] [CrossRef]
  42. Smith, J.W.; Wootten, R. Anisakis and anisakiasis. Adv. Parasitol. 1978, 16, 93–163. [Google Scholar] [CrossRef] [PubMed]
  43. Levsen, A.; Svanevik, C.S.; Cipriani, P.; Mattiucci, S.; Gay, M.; Hastie, L.C.; Buchmann, K.; Højgaard, D.P.; González, A.F.; Pascual, S.; et al. A survey of zoonotic nematodes of commercial key fish species from major European fishing grounds Introducing the FP7 PARASITE exposure assessment study. Fish. Res. 2018, 202, 4–21. [Google Scholar] [CrossRef]
  44. Madrid, E.; Galán-Puchades, M.T.; Fuentes, M. 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] [PubMed]
  45. Fuentes, M.V.; Madrid, E.; Cuesta, C.; Gimeno, C.; Baquedano-Rodríguez, M.; Soriano-Sánchez, I.; Bolívar, A.M.; Sáez-Durán, S.; Trelis, M.; Debenedetti, Á.L. Anisakid nematodes and potential risk of human anisakiasis through the consumption of hake, Merluccius spp., sold fresh in Spanish supermarkets. Pathogens 2022, 11, 622. [Google Scholar] [CrossRef] [PubMed]
  46. Fuentes, M.V.; Madrid, E.; Meliá, L.V.; Casañ, F.; Sáez-Durán, S.; Trelis, M.; Debenedetti, Á.L. Nematode parasites of the European pilchard, Sardina pilchardus (Walbaum, 1792): A genuine human hazard? Animals 2022, 12, 1877. [Google Scholar] [CrossRef] [PubMed]
  47. Strømnes, E.; Andersen, K. “Spring rise” of whaleworm (Anisakis simplex; Nematoda, Ascaridoidea) third stage larvae in some fish species from Norwegian waters. Parasitol. Res. 2000, 86, 619–624. [Google Scholar] [CrossRef] [PubMed]
  48. Nagasawa, K. The life cycle of Anisakis simplex: A review. In Intestinal Anisakiasis in Japan; Ishikura, H., Kikuchi, K., Eds.; Springer: Tokyo, Japan, 2010; pp. 31–40. [Google Scholar]
  49. Smith, J.W. The abundance of Anisakis simplex L3 in the body-cavity and flesh of marine teleosts. Int. J. Parasitol. 1984, 14, 491–495. [Google Scholar] [CrossRef]
  50. Cipriani, P.; Acerra, V.; Bellisario, B.; Sbaragli, G.L.; Cheleschi, R.; Nascetti, G.; Mattiucci, S. Larval migration of the zoonotic parasite Anisakis pegreffii (Nematoda: Anisakidae) in European anchovy, Engraulis encrasicolus: Implications to seafood safety. Food Control 2016, 59, 148–157. [Google Scholar] [CrossRef]
  51. Šimat, V.; Miletić, J.; Bogdanović, T.; Poljak, V.; Mladineo, I. Role of biogenic amines in the post-mortem migration of Anisakis pegreffii (Nematoda: Anisakidae Dujardin, 1845) larvae into fish fillets. Int. J. Food Microbiol. 2015, 214, 179–186. [Google Scholar] [CrossRef] [PubMed]
  52. Young, P.C. The relationship between the presence of larval anisakine nematodes in cod and marine mammals in British home waters. J. Appl. Ecol. 1972, 9, 459–485. [Google Scholar] [CrossRef]
  53. Cruz, C.; Barbosa, C.; Saraiva, A. Distribution of larval anisakids in blue whiting off Portuguese fish market. Helminthologia 2007, 44, 21–24. [Google Scholar] [CrossRef]
  54. Abollo, E.; Gestal, C.; Pascual, S. Anisakis infestation in marine fish and cephalopods from Galician waters: An updated perspective. Parasitol. Res. 2001, 87, 492–499. [Google Scholar] [CrossRef] [PubMed]
  55. Bušelić, I.; Botić, A.; Hrabar, J.; Stagliĉić, N.; Cipriani, P.; Mattiucci, S.; Mladineo, I. Geographic and host size variations as indicators of Anisakis pegreffii infection in European pilchard (Sardina pilchardus) from the Mediterranean Sea: Food safety implications. Int. J. Food Microbiol. 2018, 266, 126–132. [Google Scholar] [CrossRef] [PubMed]
  56. EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards); Koutsoumanis, K.; Allende, A.; Alvarez-Ordonez, A.; Bover-Cid, S.; Chemaly, M.; De Cesare, A.; Herman, L.; Hilbert, F.; Lindqvist, R.; et al. Re-evaluation of certain aspects of the EFSA Scientific Opinion of April 2010 on risk assessment of parasites in fishery products, based on new scientific data. Part 1: ToRs1 3. EFSA J. 2024, 22, e8719. [Google Scholar] [CrossRef] [PubMed]
Figure 1. (AF), view of the proboscis of several Rhadinorhynchus pristi specimens. (B), the arrow points at the typical spineless area that separates the proboscis and the trunk.
Figure 1. (AF), view of the proboscis of several Rhadinorhynchus pristi specimens. (B), the arrow points at the typical spineless area that separates the proboscis and the trunk.
Parasitologia 05 00037 g001
Table 1. Days passed since the date of capture and the date of the analysis of Scomber colias.
Table 1. Days passed since the date of capture and the date of the analysis of Scomber colias.
Number of DaysAtlanticMediterranean
12326
22119
32624
4199
52220
61213
7211
8---3
Table 2. Prevalence (P%) of Ascaridoid nematode larvae and Rhadinorhynchus pristis in Scomber colias analysed with respect to geographic origin.
Table 2. Prevalence (P%) of Ascaridoid nematode larvae and Rhadinorhynchus pristis in Scomber colias analysed with respect to geographic origin.
Origin of CaptureTotal AscaridoidAnisakis Type IContracaecum spp.Hysterothylacium spp.Rhadinorhynchus pristis
nP% (CI 95%)nP% (CI 95%)nP% (CI 95%)nP% (CI 95%)nP% (CI 95%)
Atlantic (n = 125)5241.6
(38.6–44.6)
5241.6
(38.6–44.6)
--21.6
(0.8–2.4)
4536.0
(33.1–38.9)
Mediterranean (n = 125)2620.8
(18.4–23.3)
2116.8
(14.5–19.1)
32.4
(1.5–3.3)
32.4
(1.5–3.3)
2116.8
(14.5–19.1)
n, number of parasitised fish specimens; CI, confidence interval.
Table 3. Mean intensity (mI) ± SD and range of Ascaridoid nematode larvae and Rhadinorhynchus pristis in Scomber colias analysed with respect to geographic origin.
Table 3. Mean intensity (mI) ± SD and range of Ascaridoid nematode larvae and Rhadinorhynchus pristis in Scomber colias analysed with respect to geographic origin.
Origin of CaptureTotal AscaridoidAnisakis Type IContracaecum spp.Hysterothylacium spp.Rhadinorhynchus pristis
mI ± SD
(range)
mI ± SD
(range)
mI ± SD
(range)
mI ± SD
(range)
mI ± SD
(range)
Atlantic14.3 ± 18.2
(1–95)
14.1 ± 18.1
(1–95)
-
4.5 ± 3.5
(2–7)
3.2 ± 3.7
(1–15)
Mediterranean2.2 ± 2.2
(1–9)
2.4 ± 2.3
(1–9)
1.0 ± 0
(1–3)
1.0 ± 0
(1)
8.8 ± 10.6
(1–44)
Table 4. Prevalence (P%) of Anisakis type I in Scomber colias analysed with respect to geographic origin, microhabitat, and season of capture.
Table 4. Prevalence (P%) of Anisakis type I in Scomber colias analysed with respect to geographic origin, microhabitat, and season of capture.
Origin of CaptureVisceraFleshAutumnWinter–Spring
nP% (CI 95%)nP% (CI 95%)nP% (CI 95%)nP% (CI 95%)
Atlantic5140.8
(37.8–43.8)
129.6
(7.8–11.4)
4240.8
(37.5–44.0)
1045.5
(38.3–52.6)
Mediterranean1814.4
(12.3–16.5)
32.4
(1.5–3.3)
1019.6
(15.9–23.4)
1114.9
(12.1–17.7)
n = number of parasitised fish specimens; CI = confidence interval.
Table 5. Mean intensity (mI) ±SD and range of Anisakis type I in Scomber colias analysed with respect to geographic origin, microhabitat, and season of capture.
Table 5. Mean intensity (mI) ±SD and range of Anisakis type I in Scomber colias analysed with respect to geographic origin, microhabitat, and season of capture.
Origin of CaptureVisceraFleshAutumnWinter-Spring
mI ± SD
(range)
mI ± SD
(range)
mI ± SD
(range)
mI ± SD
(range)
Atlantic13.9 ± 17.9
(1–93)
2.0 ± 1.4
(1–5)
6.9 ± 19.0
(1–95)
0.8 ± 1.9
(1–7)
Mediterranean2.7 ± 2.5
(1–9)
1.0 ± 0
(1)
0.8 ± 2.8
(1–9)
0.2 ± 0.4
(1–2)
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Fuentes, M.V.; Royo, I.; Tellols, A.; Madrid, E.; Debenedetti, Á.L.; Sáez-Durán, S.; Trelis, M. Human Anisakiosis Risk and Presence of Food-Spoiling Parasites Through the Consumption of the Atlantic Chub Mackerel, Scomber colias, Sold in Spanish Supermarkets. Parasitologia 2025, 5, 37. https://doi.org/10.3390/parasitologia5030037

AMA Style

Fuentes MV, Royo I, Tellols A, Madrid E, Debenedetti ÁL, Sáez-Durán S, Trelis M. Human Anisakiosis Risk and Presence of Food-Spoiling Parasites Through the Consumption of the Atlantic Chub Mackerel, Scomber colias, Sold in Spanish Supermarkets. Parasitologia. 2025; 5(3):37. https://doi.org/10.3390/parasitologia5030037

Chicago/Turabian Style

Fuentes, Màrius Vicent, Irina Royo, Alba Tellols, Elena Madrid, Ángela Lilia Debenedetti, Sandra Sáez-Durán, and María Trelis. 2025. "Human Anisakiosis Risk and Presence of Food-Spoiling Parasites Through the Consumption of the Atlantic Chub Mackerel, Scomber colias, Sold in Spanish Supermarkets" Parasitologia 5, no. 3: 37. https://doi.org/10.3390/parasitologia5030037

APA Style

Fuentes, M. V., Royo, I., Tellols, A., Madrid, E., Debenedetti, Á. L., Sáez-Durán, S., & Trelis, M. (2025). Human Anisakiosis Risk and Presence of Food-Spoiling Parasites Through the Consumption of the Atlantic Chub Mackerel, Scomber colias, Sold in Spanish Supermarkets. Parasitologia, 5(3), 37. https://doi.org/10.3390/parasitologia5030037

Article Metrics

Back to TopTop