Next Article in Journal
Two Multidrug-Resistant Escherichia coli Isolates from Blood Cultures After Cervical Conization in a Patient with Cervical Intraepithelial Neoplasia Grade II: Phenotypic and Genomic Characterization
Previous Article in Journal
Influenza A(H3N2) Subclade K: Epidemiology, Molecular Evolution and Vaccine Effectiveness in Europe
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Pathogens
Volume 15
Issue 5
10.3390/pathogens15050475
pathogens-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

New Findings on the Hosts and Distribution of Eustrongylides excisus (Nematoda: Dioctophymatidae) and Other Zoonotic Parasites in Fish Species from an Uninvestigated Subalpine Lake, Varese Lake (Northwestern Italy)

by
Michele Macrelli
1,
Martina Ossola
1,*,
Giovanni Sala
1,
Damiano Accurso
1,
Monica Caffara
2,
Andrea Gustinelli
2,
Marco Farioli
3 and
Cristian Salogni
1
1
Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia Romagna “Bruno Ubertini”, 25124 Brescia, Italy
2
Department of Veterinary Medical Sciences, Alma Mater Studiorum University of Bologna, 40064 Ozzano dell’Emilia, Italy
3
Department of Veterinary Public Health and Food Safety of Animal Origin Products, Agenzia di Tutela della Salute dell’Insubria, 21100 Varese, Italy
*
Author to whom correspondence should be addressed.
Pathogens 2026, 15(5), 475; https://doi.org/10.3390/pathogens15050475
Submission received: 18 March 2026 / Revised: 22 April 2026 / Accepted: 24 April 2026 / Published: 28 April 2026
(This article belongs to the Section Parasitic Pathogens)
Versions Notes

Abstract

The increasing consumption of fish has raised public health concerns regarding fish-borne zoonotic helminths (FBZHs), which are recognized as significant food-borne parasites worldwide. In freshwater environments, Clinostomum complanatum, Opisthorchis felineus, Pseudamphistomum truncatum, Dibothriocephalus latus and Eustrongylides excisus are of particular concern in Italy and neighbouring countries. This study aimed to assess the prevalence of these FBZHs in five commercially and ecologically relevant freshwater fish species from Lake Varese, a heavily anthropized and understudied basin in northern Italy. A total of 59 fish were examined via necropsy and stereomicroscopic inspection of skeletal muscles. Only Eustrongylides spp. larvae were detected, with a prevalence of 16.9%. Molecular analysis (ITS region) identified them as E. excisus. This study reports, for the first time in Western Europe, E. excisus in Sander lucioperca (p = 12.5%) and Esox lucius (p = 8.3%). The highest prevalence occurred in Silurus glanis (p = 37.5%), followed by Perca fluviatilis (p = 25.0%), while Tinca tinca showed no infection. These findings confirm that among the FBZHs considered, E. excisus is currently present and expanding both in host range and geography in Italian lakes, underscoring the need for updated epidemiological data to support risk assessment, food safety and zoonotic parasite control in freshwater fisheries.

1. Introduction

In recent decades, the global demand for fish and seafood has steadily increased. This trend is driven by shifting dietary habits, increased health awareness, and culinary practices that include raw or lightly cooked fish. As a result, fish-borne parasitic infections have become an emerging concern for food safety and public health [1]. According to the Food and Agriculture Organization (FAO), global per capita fish consumption has reached approximately 20.7 kg per year [2], with an upward trend especially evident in Europe. This rising consumption has amplified awareness of the risks posed by fish-borne zoonotic helminths (FBZHs), which are now recognized among the most significant food-borne parasites worldwide. More than 50 species of FBZHs are known to cause human infections through the consumption of raw or undercooked fish containing viable parasites [3]. According to the most recent available estimates, the World Health Organization (WHO) reported around 56 million cases of parasitic infection linked to fish consumption in 2012 [4].
While most attention has historically focused on marine species, helminths in freshwater fish also pose relevant zoonotic risks. All wild-caught freshwater fish should be considered potential reservoirs of viable zoonotic parasites [5]. Although freshwater fisheries represent a small share of total consumption in the EU, they remain highly significant for lake-dwelling populations and tourists seeking traditional lake-based dishes [3].
Among freshwater FBZHs, Clinostomum complanatum, Contracaecum rudolphii, Opisthorchis felineus, Pseudamphistomum truncatum, Dibothriocephalus latus and Eustrongylides excisus, have emerged as parasites of particular concern in Europe. These species have been reported in more than 32 fish hosts across various water basin—including rivers and lakes—in Italy (Table 1), France, Switzerland and Germany [3,6,7,8].
Their ability to infect fish species of commercial and dietary relevance, combined with their environmental persistence and zoonotic potential, highlight the urgent need for targeted parasitological surveillance in underinvestigated freshwater environments. One such area is Lake Varese, a mid-sized subalpine lake in northern Italy of ecological and recreational relevance. Updated epidemiological data from this basin are essential to support effective food safety management and guide evidence-based decision-making. Therefore, this study aims to (i) investigate the presence of larvae of Eustrongylides spp., C. complanatum, C. rudolphii, D. latus, O. felineus, and P. truncatum in five wild fish species of commercial and ecological relevance from Lake Varese, and (ii) assess the prevalence and anatomical localization of the detected parasites in the infected specimens.

2. Materials and Methods

2.1. Study Area

This study was conducted at Lake Varese (45°49′ N, 8°44′ E), located in northwestern Italy (Lombardy region). It is a monomictic subalpine lake of glacial origin located at an elevation of 236 m above sea level [10]. This eutrophic lake has a mean depth of 11 m, a maximum depth of 26 m, a surface area of 14.8 km2, a volume of 153 million cubic metres (m3), and a theoretical renewal time of 1.7–1.9 years [11,12]. The lake receives inflow from two tributaries, the Brabbia Channel and the Tinella Stream, with annual average discharges of 23 × 106 and 10 × 106 m3 yr−1 respectively, and has a single outflow, the Bardello Stream, with an annual average discharge of 80.4 × 106 m3 yr−1 [13]. This basin provides valuable habitats for a wide range of flora and fauna, and it contributes to the local economy through recreational and professional fishing, as well as water-related industries.

2.2. Fish Collection

This study was conducted from June 2024 to March 2025, with fish sampled at two sites, one located in the southern part of the lake and the other in the northern part.
Five fish species were selected for this study: pike (Esox lucius italicus), pike-perch (Sander lucioperca), European perch (Perca fluviatilis), tench (Tinca tinca), and wels catfish (Silurus glanis). These species were selected based on their abundance and position in the lake food chain [14] and their recognized commercial and recreational importance [15,16]. All selected fish species are susceptible to hosting larvae or metacercariae of the zoonotic parasites under investigation. As no prior data were available on the presence of these parasites in Lake Varese, no minimum sample size per species was defined.
Fish were obtained from a local professional fisherman, refrigerated at 0–4 ± 1 °C, and transported to the laboratory for analysis.

2.3. Morphological and Anatomopathological Examination

Post mortem examinations were carried out within 12 h of fish collection. Each specimen was identified according to the ichthyofauna identification guidelines of the Italian Ministry of the Environment and Protection of Land and Sea [17], then measured for total length (from the tip of the snout to the tip of the tail) and weighed. External examinations were performed to detect large encysted larvae on the skin, gills, fins, and buccal cavity. Skeletal muscles and internal organs were carefully dissected for visual inspection.

2.4. Parasitological Identification and Molecular Analysis

To detect encysted plerocercoid, nematode larvae, and metacercariae, skeletal muscles and subcutaneous tissues were transversely sliced into 5 mm thick sections using a scalpel, compressed between glass slides, and examined by transillumination under a stereomicroscope (Nikon Stereoscopic Microscope SMZ745, Nikon Corporation, Tokyo, Japan), following the protocol described by Smagulova et al. [18]. The entire fillet was examined for all species except for S. glanis; due to the large body size of this species, only representative portions of the fillet from the anterior and posterior parts of the body were analysed. Acid–pepsin digestion was not performed. Isolated nematode larvae were subsequently identified at the genus level based on morphological features, following the identification keys by Moravec [19]. All detected parasites were counted, their locations recorded, and observed microscopically (Microscope Eclipse E200, Nikon Corporation, Tokyo, Japan) before preservation in 70% ethanol for subsequent molecular analyses of the ITS rDNA following the protocol of Prearo et al. [20].

2.5. Statistical Analysis

Prevalence (p), mean intensity (MI), and mean abundance (MA) of Eustrongylides spp. infestation were calculated following Bush et al. [21]. Prevalence values are presented with their 95% confidence intervals (CIs), calculated according to Bush et al. [21].
To explore potential differences in parasitism between the two sampling locations, Fisher’s exact test was applied, and odds ratios (ORs) with 95% confidence intervals (CI) were computed.
Due to the limited overall sample size and the unbalanced distribution of individuals across fish species—particularly the very low number of infected specimens in several groups—the assumptions required for valid inferential statistical analyses were not met. Therefore, no formal statistical tests were performed, and the results are presented descriptively. The significance level that would have been applied for inferential analyses was set at α = 0.05.
Descriptive statistics, including mean values and standard deviations (SDs) for fish weight and length, were computed for each species. All statistical analyses and data management were performed using Microsoft Excel (version 2019).

3. Results

3.1. Fish Collection Results

A total of 59 fish were collected: 12 specimens of E. lucius, 8 specimens of S. lucioperca, 19 specimens of P. fluviatilis, 4 specimens of T. tinca, and 16 specimens of S. glanis.
Slightly more than half of the specimens were collected from the northern part of the lake (52.5%; 31/59). Most specimens (67.8%; 40/59) were captured during the summer months of 2024, while the remaining fish were collected in spring (15.3%; 9/59), autumn (15.3%; 9/59), and winter (1.7%; 1/59) until March 2025. The variation in fish numbers across seasons reflects both practical constraints and ecological factors. For example, heavy rainfall throughout the 2024 fishing season [22] reduced fishing effort and the number of successful catches in winter. The uneven sampling distribution across seasons did not allow for an assessment of seasonal trends.
Differences in the number of individuals collected per species may reflect their relative abundance in the lake, although species-specific seasonal behaviors could also have contributed.

3.2. Morphological and Anatomopathological Results

This study included specimens of various ages, resulting in a wide standard deviation (SD) for both weight and total length within each species (Table 2).
At the anatomopathological level, the only observed cutaneous alterations were skin reddening, cutaneous and fin lacerations, all consistent with handling and capture. No lesions suggestive of disease were observed in the gills or internal organs of any specimens analyzed.

3.3. Parasitological Identification and Molecular Analysis Results

The only FBZHs observed were reddish Eustrongylides spp. nematode larvae, detected in 16.9% of the fish (10/59) (Table 2). The prevalence of Eustrongylides spp. was 37.5% in S. glanis (95% CI: 18.5–61.4), 10.5% in P. fluviatilis (95% CI: 2.9–31.4), 12.5% in S. lucioperca (95% CI: 2.2–47.1), and 8.3% in E. lucius (95% CI: 1.5–35.4). No larvae were detected in T. tinca. The mean intensity of infestation ranged from 1 (S. lucioperca; E. lucius) to 6.3 (S. glanis), while mean abundance ranged from 0.13 (S. lucioperca) to 2.75 (S. glanis).
Larvae were located in the coelomic cavity of E. lucius and S. glanis, and in the muscles of S. lucioperca and P. fluviatilis. The highest level of infestation in the coelomic cavity was observed in a S. glanis hosting 14 larvae, while the greatest number in musculature was found in a P. fluviatilis with 4 larvae, all situated in the antero-ventral region. The larvae measured 2.0–5.0 cm and were all detected macroscopically, with no additional larvae found under stereomicroscopic examination.
The ITS region of the rDNA was successfully amplified and sequenced. Sequence similarity searches performed using the NCBI BLAST+ (https://blast.ncbi.nlm.nih.gov/Blast.cgi, accessed on 18 March 2026) against the NCBI nucleotide database showed 100% identity with reference sequences of E. excisus available in GenBank, allowing for the identification of the specimens at the species level and confirming the morphological identification of the larvae collected. The obtained ITS rDNA sequences were deposited in GenBank under accession number PZ314426.
Subjects sampled in the northern site showed a higher prevalence of parasitism (25.8%; 8/31) compared to those from the southern site (7.1%; 2/28). Although Fisher’s exact test did not reveal a statistically significant association between geographic area and parasitism, an odds ratio of 4.52 (95% CI: 0.87–23.50; Fisher’s exact test p = 0.0838) suggests a trend toward a higher risk of parasitism in subjects from the North.
Due to the limited overall sample size and the low number of infected individuals per species (ranging from 0 to 6), no statistically robust comparison of infection levels among fish species could be performed.
No larvae of C. complanatum, O. felineus, P. truncatum, and D. latus were detected.

4. Discussion

The results of this study provide the first evidence of E. excisus in Lake Varese. This parasite was first reported in an Italian subalpine lake in 2020 and then identified in the nearby Lake Maggiore in 2023 [20]. These findings suggest that E. excisus may have already been present in Lake Varese but remained undetected due to a lack of targeted investigations. Indeed, recent research has documented an expanding distribution of E. excisus in Italy, potentially driven by the rising population of cormorants (Phalacrocorax carbo sinensis) around inland water bodies [23]. A marked rise in the breeding population of cormorants has also been documented around Lake Varese since 2002. The increase is mainly attributed to the proximity of the lake to a Marsh Nature Reserve, which serves as a major nesting site for waterbirds [24]. In 2021, more than 500 cormorant nests were recorded in this Reserve during the winter season. This large and largely sedentary cormorant population may contribute to the presence of E. excisus in nearby, still underinvestigated water bodies. In response to this population growth and its documented impact on freshwater fish communities, the Lombardy Regional Authority implemented control measures, including targeted culling [25]. Continued monitoring will be essential to assess whether these measures also affect the distribution and prevalence of E. excisus in the region.
As described by Castiglione et al. [26], water eutrophication and increasing temperatures are additional risk factors that may have contributed to creating a favourable environment for the survival and expansion of Eustrongylides spp. in Italian lakes.
E. excisus were isolated from four out of five freshwater fish species selected for their commercial and ecological relevance in this area. This study is the first to report S. lucioperca and E. lucius as hosts for E. excisus in Western Europe. Previously, E. excisus was reported in pike-perch in Serbia [27] and Ukraine [28], with prevalence rates of 14.0% (3/21) and 58.1% (43/74), respectively. Eustrongylides spp. were reported in the European pike in Ukraine [28], with a prevalence rate of 58.9% (69/117), considerably higher than the 8.3% recorded in our study.
S. glanis showed the highest prevalence of E. excisus infection (37.5%) and the highest mean intensity (6.3). Similar findings were reported in Lake Massaciuccoli in central Italy (p = 75.0%; 42/56; MI = 5.7) [26].
No comparable data are available for S. glanis in other subalpine lakes in northern Italy. Given its feeding habits, which include fish and invertebrates, and its capacity to rapidly adapt to new habitats, S. glanis may represent an ideal target species for assessing the presence of Eustrongylides spp. in the freshwater basins investigated.
The prevalence observed in P. fluviatilis (10.5%) was comparable to that reported for the same species in other subalpine lakes in northern Italy, ranging from 4.3% (3/70) to 25.3% (38/150) [23]. The detection of Eustrongylides spp. larvae in the musculature of P. fluviatilis is particularly significant, as this species is often consumed raw (e.g., perch carpaccio).
Analysis indicated that juvenile individuals were also infected. Due to their small size and susceptibility to predation by definitive hosts, these individuals play an important role in perpetuating the life cycle of Eustrongylides spp. In contrast, larger fish, such as wels catfish, are generally too large to be preyed upon by piscivorous birds and may therefore act as a dead end for parasite transmission. Large predatory fish like S. glanis, serving as paratenic hosts, can concentrate the parasitic load.
No Eustrongylides spp. larvae were found in T. tinca; however, due to the limited number of tench specimens examined, the presence of this parasite in this species cannot be ruled out. To date, only one study in central Italy reported tench as a potential host for Eustrongylides spp., with a very low prevalence (0.13%; 6/19,809) [29]. This suggests that tench (family Tincidae) may be among the less susceptible species, as they mainly feed on plant material and zooplankton [30]. Accordingly, tench could be considered an accidental host, acquiring infection only in heavily contaminated environments [31].
As highlighted in the present study, a comprehensive visual examination of both the coelomic cavity and skeletal muscles represents an important and practical method for detecting Eustrongylides spp. larvae in infected fish. Although the musculature is frequently reported as the primary site for larval detection, larvae may also be present in other anatomical locations, as observed in S. glanis in this study. In this species, 3–5 cm reddish were identified in the coelomic cavity, and in some cases could be mistaken for blood vessels. Interestingly, a similar larval distribution was reported in S. glanis from Lake Massaciuccoli [26], suggesting that Eustrongylides spp. Larvae may have difficulty migrating from the coelomic cavity to their predilection site in this host.
According to European legislation, the presence of visible parasites during visual inspection renders fish unfit for human consumption [32]. Clinical symptoms of human eustrolngyliasis typically appear within 24 h after ingestion of raw or undercooked freshwater fish harbouring third- or fourth-stage larvae [33]. The disease usually manifests with gastrointestinal symptoms, including acute abdominal pain and gastritis, although rare cases may progress to intestinal perforation. Extraintestinal signs, including subcutaneous or cutaneous nodules, have also been reported [23]. Although limited data are available on the impact of different processing methods on the survival of Eustrongylides spp. larvae in freshwater fish, cooking at 60 °C at the core for 10 min or freezing at –20 °C at the core for 24 h appears to be effective in inactivating the parasite [26].
With the exception of D. latus, this is the first study to investigate the presence of C. complanatum, O. felineus, P. truncatum, and C. rudolphii, in Lake Varese. D. latus was first identified in P. fluviatilis in 1955 (p = 80%) and later in 1973 (p = 13.5%) [7]. In 1967, a water restoration project was initiated by the Varese Province to reduce external nutrient loads. Measures included the construction of a sewage collection network, an O-ring diversion system, and a centralized wastewater treatment plant. Wastewaters received tertiary treatment in 1986, and water diversion was completed in 1994 [34].
The absence of D. latus plerocercoid larvae in fish from Lake Varese was previously reported in 2001 [35] and 2009 [36], and our data confirm this result. These findings contrast with the epidemiological data obtained from other large subalpine lakes near Lake Varese, such as Lake Maggiore, Como, and Iseo, where D. latus is considered endemic [7]. The spatial distribution of D. latus in these lakes has been linked to ineffective sewage treatment systems, which allow for contamination by eggs released from infected humans [37].
The absence of O. felineus metacercariae in the fish analysed was expected. In Italy, O. felineus metacercariae have been reported only in the muscles T. tinca from Lakes Bolsena and Bracciano, with prevalences of 75% (33/44) and 95% (83/87) respectively. Between 2003 and 2011, 211 human cases of opisthorchiasis were linked to the consumption of raw tench fillets from these lakes. Epidemiological investigations following these outbreaks identified snails of the genus Bithynia and T. tinca as intermediate hosts, and stray cats along the lake shores as definitive hosts. The stray cat population has been estimated at 280–360 individuals around Lake Bracciano and approximately 1000 around Lake Bolsena [38]. Lake Varese, with a lower number of tench and fewer stray cats along its shores, can therefore be considered at lower risk for O. felineus, a conclusion supported by our data.
Humans can play a significant role in the epidemiology of this parasite. In particular, practices such as releasing small tench on lakeshores or improperly disposing of fish leftovers from restaurants can facilitate the parasite’s life cycle by allowing infected fish to be consumed by cats and dogs, which serve as definitive hosts [6].
P. truncatum and C. complanatum have recently been reported in Italy, respectively in T. tinca and P. fluviatilis, in two other subalpine lakes of the Lombardy region that share ecological characteristics with Lake Varese, including comparable fish communities, similar intermediate hosts and analogous shoreline vegetation [39,40]. However, neither P. truncatum nor C. complanatum were detected in the fish analysed in the present study. Further investigations are needed to identify the biological and ecological factors influencing the geographical expansion of these food-borne trematodes.

5. Conclusions

The present study highlights the importance of monitoring underinvestigated freshwater ecosystems, which may serve as reservoirs for zoonotic parasites. This study reports, for the first time, the presence of E. excisus in pike-perch (S. lucioperca) and northern pike (E. lucius) in Western Europe, confirming its ongoing geographic and host expansion across Italian lakes. These findings underline the growing public health relevance of this fish-borne zoonotic parasite.
Although no human cases of eustrongyliasis have been documented in Europe to date, veterinary authorities must continue to raise awareness and provide training to relevant stakeholders to prevent the emergence of this and other freshwater food-borne parasitic diseases. A comprehensive visual examination of both the coelomic cavity and skeletal muscles remains an effective and practical approach for detecting Eustrongylides spp. larvae and should be systematically performed during inspections of fish from Italian lakes.
Early detection and surveillance in underinvestigated freshwater ecosystems are crucial for identifying reservoirs of FBZHs and developing ad hoc control strategies to prevent disease outbreaks and limit their spread. Controlling these parasites requires a One Health approach, based on strong collaboration between the human, animal and environment health sectors. Enhancing water quality and wastewater infrastructure, managing interactions between intermediate and definitive hosts, and educating the public to interrupt parasite transmission cycles are key strategies for their control.

Author Contributions

Conceptualization, M.F., C.S., G.S. and D.A.; methodology, C.S., G.S. and D.A.; validation, C.S. and G.S.; formal analysis, M.O. and C.S.; investigation, C.S., M.M., G.S. and D.A.; resources, M.F., C.S. and G.S.; data curation, C.S. and G.S.; writing—original draft preparation, M.M. and M.O.; writing—review and editing, M.M., M.O., C.S., M.C. and A.G.; visualization, M.O.; supervision, C.S.; project administration, M.F. and C.S.; funding acquisition, M.F., G.S. and C.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Agenzia di Tutela della Salute dell’Insubria, “Progetto One Health—Il pesce come indicatore di qualità delle acque”.

Institutional Review Board Statement

All fish samples included in the study were obtained exclusively from commercial fishing activities and were acquired already dead. Therefore, no experimental procedures involving live animals were performed. In accordance with Istituto Zooprofilattico Sperimentale Lombardia Emilia Romagna (IZSLER) regulations, institutional Ethic Committee approval was not required. All samples were acquired from a professional fisherman who holds the legal permits for fishing activities in Lake Varese. No protected species nor any species threatened with extinction were included in the study.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author due to institutional data protection policies.

Acknowledgments

The authors acknowledge Agenzia di Tutela della Salute dell’Insubria, particularly Marco Magrini and Mario Esposito, for their valuable administrative support and coordination throughout the project.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:
CIConfidence Interval
FAOFood and Agriculture Organization
FBZHFish-borne zoonotic helminth
ITSInternal Transcribed Spacer
MAMean abundance
MIMean intensity
No.Number
PPrevalence
SDStandard deviation
WHOWorld Health Organization

References

  1. Franssen, F.; Gerard, C.; La Carbona, S.; Robertson, L.J.; Pauls, P. Control of Fishborne Parasites in the Food Industry. Food Prot. Trends 2019, 39, 334–337. [Google Scholar]
  2. FAO. The State of World Fisheries and Aquaculture 2024—Blue Transformation in Action; FAO: Rome, Italy, 2024. [Google Scholar]
  3. Menconi, V.; Lazzaro, E.; Bertola, M.; Guardone, L.; Mazzucato, M.; Prearo, M.; Bilska-Zajac, E.; Cortinovis, L.; Manfrin, A.; Arcangeli, G.; et al. The Occurrence of Freshwater Fish-Borne Zoonotic Helminths in Italy and Neighbouring Countries: A Systematic Review. Animals 2023, 13, 3793. [Google Scholar] [CrossRef] [PubMed]
  4. Tesfaye, Z.; Hiko, A.; Belina, D.; Firdisa, M. Assessments and Identification of Selected Fish-Borne Zoonotic Parasites in Nile Tilapia and African Catfish Species in Lakes of Haramaya District, Ethiopia. Aquac. Res. 2023, 1, 2638123. [Google Scholar] [CrossRef]
  5. EFSA Panel on Biological Hazards (BIOHAZ). Scientific Opinion on risk assessment of parasites in fishery products. EFSA J. 2010, 8, 1543. [Google Scholar] [CrossRef]
  6. Pozio, E.; Armignacco, O.; Ferri, F.; Gomez Morales, M.A. Opisthorchis felineus, an emerging infection in Italy and its implication for the European Union. Acta Trop. 2013, 126, 54–62. [Google Scholar] [CrossRef]
  7. Králová-Hromadová, I.; Radačovská, A.; Čisovská Bazsalovicsová, E.; Kuchta, R. Ups and downs of infections with the broad fish tapeworm Dibothriocephalus latus in Europe from 1900 to 2020: Part I. Adv. Parasitol. 2021, 114, 75–166. [Google Scholar] [CrossRef]
  8. Duflot, M.; Pozet, F.; Le Bouquin, S.; Richomme, C.; Bourgau, O.; Blasco-Costa, I.; Gay, M. Distribution of Clinostomum complanatum in two commercially important freshwater fish, perch and rudd, in France. Food Waterborne Parasitol. 2025, 40, e00281. [Google Scholar] [CrossRef] [PubMed]
  9. Papalini, C.; Gómez-Morales, M.A.; Mercuri, A.; Stolaj, E.; Brancaleoni, M.G.; Fusco Moffa, I.; Lo Vaglio, G.; Ludovisi, A.; Marucci, G.; Francisci, D. A new human opisthorchiasis outbreak in central Italy: A never-ending story. Infection 2024, 53, 175–181. [Google Scholar] [CrossRef]
  10. Chirico, N.; António, D.C.; Pozzoli, L.; Marinov, D.; Malagó, A.; Sanseverino, I.; Beghi, A.; Genoni, P.; Dobricic, S.; Lettieri, T. Cyanobacterial blooms in Lake Varese: Analysis and characterization over ten years of observations. Water 2020, 12, 675. [Google Scholar] [CrossRef]
  11. Premazzi, G.; Dalmiglio, A.; Cardoso, A.C.; Chiaudani, G. Lake management in Italy: The implications of the Water Framework Directive. Lakes Reserv. Res. Manag. 2003, 8, 41–59. [Google Scholar] [CrossRef]
  12. Ambrosetti, W.; Barbanti, L.; Sala, N. Residence time and physical processes in lakes. J. Limnol. 2023, 62, 1–15. [Google Scholar] [CrossRef]
  13. Zaccara, S.; Canziani, A.; Roella, V.; Crosa, G. A northern Italian shallow lake as a case study for eutrophication control. Limnology 2007, 8, 155–160. [Google Scholar] [CrossRef]
  14. Regione Lombardia. Atto integrativo dell’Accordo Quadro di Sviluppo Territoriale (L.R. 29 Novembre 2019 n.19) “Salvaguardia e risanamento del lago di Varese”—Allegato 1. Available online: https://www.atovarese.it/wp-content/uploads/2019/12/Allegato-1-PV-15-Scenario-di-riferimento.pdf (accessed on 9 April 2026).
  15. Fipas Federazione Italiana Pesca Sportiva Attività Subacquee Nuoto Pinnato. Prontuario Pesca del Bacino n° 5. Available online: https://www.fipsasva.it/sites/default/files/bacino-vlc/24-01-24-prontuario_pesca_bacino_ndeg_5_2024.pdf (accessed on 9 April 2026).
  16. Vasconi, M. Freshwater Fish of Northern Italy: From the Valorization of Wild Unexploited Species to New Farming Perspectives. Ph.D. Thesis, Università degli Studi di Milano, Milan, Italy, 2024. [Google Scholar]
  17. Ministero dell’Ambiente e della Tutela del Territorio. Pesci delle Acque Interne d’Italia. Available online: https://www.mase.gov.it/portale/documents/d/guest/qcn_20-pdf (accessed on 9 April 2026).
  18. Smagulova, A.; Bulashev, A.; Jazina, K.; Uakhit, R.; Lider, L.; Bekenova, A.; Valeeva, D.; Kiyan, V. Foodborne Helminths in Imported Fish: Molecular Evidence from Fish Products in the Kazakhstan Market. Foods 2025, 14, 3466. [Google Scholar] [CrossRef]
  19. Moravec, F. Parasitic Nematodes of Freshwater Fishes of Europe, 1st ed.; Springer: Dordrecht, The Netherlands, 1994. [Google Scholar]
  20. Prearo, M.; Menconi, V.; Bondavalli, B.; Gabetti, A.; Maganza, A.; Abbà, M.; Bezzo Llufrio, T.; Zanoli, A.; Esposito, G.; Pastorino, P. Distribution and prevalence of Eustrongylides excisus in the lake fish fauna of Piedmont (northwestern Italy). Ittiopatologia 2023, 20, 27–53. [Google Scholar]
  21. 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]
  22. Centro Geofisico Prealpino. Sintesi Metereologica 2024 a Varese. Available online: https://www.astrogeo.va.it/statistiche/2024/clima_2024.pdf (accessed on 15 March 2026).
  23. Maganza, A.; Mossotto, C.; Gabetti, A.; Gozlan, R.E.; Combe, M.; Esposito, G.; Bondavalli, F.; Bertoli, M.; Pizzul, E.; Pastorino, P.; et al. Expanding Host Range: First Record of Eustrongylides excisus in Padogobius bonelli (Gobiidae) from the Po River (Northwest Italy). Fishes 2025, 10, 254. [Google Scholar] [CrossRef]
  24. Regione Lombardia. Interventi di Controllo Selettivo del Cormorano nel Territorio Lombardo, nel Periodo 1 Ottobre 2023–15 Marzo 2028. Available online: https://areadocumentale.servizirl.it/atti/download/AAAAYLyV6YuQkJS0wLnMrhAjyMKU9LdQdg2IKqobyJieraYWZgiPpnVTF6pRUx9KrkE/tUUhxLjzxSXWSABHPKoPWBpGKoVZyZYsccY8jTViRsYTVMqEH8x+lytnrF9BcAwqYAAAAIBiykfcWI6mGw8odm+aDJyaLDWm4/QhbEuRtxc3t82hezy5FgoVa3VlJJgpn0UWjiZI01qdnr6pTrO0+LDRUQpqWR5EvwsE0h4LQr11tkCA874VCKAE90S1QoHJKBesqtizguo4X3MFKjynbtBtAzwkqx14IwEfZM16s3lYrnQw4wAAAAjwIKoxAdKTHw== (accessed on 15 March 2026).
  25. Regione Lombardia. Deliberazione n. XII/414—Autorizzazione al Controllo Selettivo del Cormorano (Phalacrocorax carbo sinensis) nel Periodo Compreso tra il 1 Ottobre 2023 ed il 15 Marzo 2024, ai Sensi dell’Art. 9, Comma 1, Lett. A, della DIR. 2009/147/CE, degli Artt. 19 e 19 bis della L. 157/92 e dell’Art. 41 della L.R. 26/93. Available online: https://areadocumentale.servizirl.it/atti/download/AAAAWD9uni9K+iqGQA39X8aDc8uvZIMgoLSbC+uuhQoshDz0ygnqc8k2Ar102HUjRI1ZF9KRLF++T1h6lRSHhBoOvy9yHV0b8UolopZ7Bh34QR7vENMyeUskoGUAAACAPDdPoihVYh9APUqnDh02LsRdnrUIKXGsTYK9IEyZ2FERGjDsExLfmWgdxWjXAayf5OeHQvowuH/Yx9bBFpk8B3PEEp3bZ6ADxhCd6E8sHPBiO3bJWCEfCfQ0JQylb8PflhnX/Jy1c7BXDLjuDgQMtn1SQYSwxQPG/dFyXZtUwWwAAAAIxb7y0s+eK7w= (accessed on 15 March 2026).
  26. Castiglione, D.; Di Maggio, M.; Guardone, L.; Ricci, E.; Tinacci, L.; Guglielmone, G.; Coltraro, M.; Susini, F.; Armani, A. Eustrongylides excisus in fish species caught in the Massaciuccoli Lake (Northwest Tuscany, Italy): Implications for freshwater fish quality and public health. Food Control 2023, 153, 109894. [Google Scholar] [CrossRef]
  27. Bjelić-Čabrilo, O.; Novakov, N.; Ćirković, M.; Kostić, D.; Popović, E.; Aleksić, N.; Lujić, J. The first determination of Eustrongylides excisus Jägerskiöld, 1909—larvae (Nematoda: Dioctophymatidae) in the pike-perch Sander lucioperca in Vojvodina (Serbia). Helminthologia 2013, 50, 291–294. [Google Scholar] [CrossRef]
  28. Honcharov, S.L.; Soroka, N.M.; Pashkevich, I.Y.; Dubovyi, A.I.; Bondar, A.O. Infection of predatory fish with larvae of Eustrongylides excisus (Nematoda, Dioctophymatidae) in the Delta of the Dnipto River and the Dnipro-Buh Estuary in Southern Ukraine. Vestn. Zool. 2018, 52, 137–144. [Google Scholar] [CrossRef]
  29. Franceschini, R.; Guardone, L.; Armani, A.; Ranucci, D.; Roila, R.; Valiani, A.; Susini, F.; Branciari, R. Five-years management of an emerging parasite risk (Eustrongylides sp., Nematoda) in a fishery supply chain located on Trasimeno Lake (Italy). Food Control 2022, 136, 108858. [Google Scholar] [CrossRef]
  30. Alaş, A.; Altındağ, A.; Yılmaz, M.; Kırpık, M.A.; Ak, A. Feeding Habits of Tench (Tinca tinca L., 1758) in Beyşehir Lake (Turkey). Turk. J. Fish. Aquat. Sci. 2010, 10, 187–194. [Google Scholar] [CrossRef]
  31. Di Maggio, M.; Coltraro, M.; Tinacci, L.; Guardone, L.; Ricci, E.; Corradini, C.; Susini, F.; Armani, A. Mapping the occurrence of Eustrongylides spp. in fish species caught from six lakes in Central Italy (Tuscany and Latium regions): Implications for local fishery supply chains. Heliyon 2024, 10, e30733. [Google Scholar] [CrossRef]
  32. European Parliament. Regulation (EC) No. 853/2004 of the European Parliament and of the Council of 29 April 2004 Laying Down Specific Hygiene Rules for Food of Animal Origin. Available online: https://eur-lex.europa.eu/eli/reg/2004/853/oj/eng (accessed on 15 March 2026).
  33. Honcharov, S.L.; Soroka, N.M.; Galat, M.V.; Zhurenko, O.V.; Dubovyi, A.I.; Dzhmil, V.I. Eustrongylides (Nematoda: Dioc-tophymatidae): Epizootology and special characteristics of the development biology. Helminthologia 2022, 59, 127–142. [Google Scholar] [CrossRef] [PubMed]
  34. Premazzi, G.; Cardoso, A.C.; Rodari, E.; Austoni, M.; Chiaudani, G. Hypolimnetic withdrawal coupled with oxygenation as lake restoration measures: The successful case of Lake Varese (Italy). Limnetica 2005, 24, 123–132. [Google Scholar] [CrossRef]
  35. Peduzzi, R.; Boucher-Rodoni, R. Resurgence of human bothriocephalosis (Diphyllobothrium latum) in the subalpine lake region. J. Limnol. 2001, 60, 41–44. [Google Scholar] [CrossRef]
  36. Gustinelli, A.; Menconi, V.; Prearo, M.; Caffara, M.; Righetti, M.; Scanzio, T.; Raglio, A.; Fioravanti, M.L. Prevalence of Diphyllobothrium latum (Cestoda: Diphyllobothriidae) plerocercoids in fish species from four Italian lakes and risk for the consumers. Int. J. Food Microbiol. 2016, 235, 109–112. [Google Scholar] [CrossRef]
  37. Menconi, V.; Pastorino, P.; Momo, I.; Mugetti, D.; Bona, M.C.; Levetti, S.; Tomasoni, M.; Pizzul, E.; Ru, G.; Dondo, A.; et al. Occurrence and spatial distribution of Dibothriocephalus latus (Cestoda: Diphyllobothriidea) in lake Iseo (northern Italy): An update. Int. J. Environ. Res. Public Health 2020, 17, 5070. [Google Scholar] [CrossRef]
  38. De Liberato, C.; Scaramozzino, P.; Brozzi, A.; Lorenzetti, R.; Di Cave, D.; Martini, E.; Lucangeli, C.; Pozio, E.; Berrilli, F.; Bossù, T. Investigation on Opisthorchis felineus occurrence and life cycle in Italy. Vet. Parasitol. 2011, 177, 67–71. [Google Scholar] [CrossRef] [PubMed]
  39. Dorigo, L.; Saccà, E.; Beraldo, P. First report for Friuli Venezia Giulia of Clinostomum complanatum (Rudolphi, 1814) (Digenea, Clinostomidae) and finding of the species in Cobitis bilineata canestrini, 1886 and Telestes muticellus (Bonaparte, 1837). Gortania 2023, 44, 65–70. [Google Scholar] [CrossRef]
  40. Menconi, V.; Manfrin, C.; Pastorino, P.; Mugetti, D.; Cortinovis, L.; Pizzul, E.; Pallavicini, A.; Prearo, M. First report of Clinostomum complanatum (Trematoda: Digenea) in european perch (Perca fluviatilis) from an Italian subalpine lake: A risk for public health? Int. J. Environ. Res. Public Health 2020, 17, 1389. [Google Scholar] [CrossRef]
Table 1. Life cycle, host range and human cases in Italy of the investigated parasites.
Table 1. Life cycle, host range and human cases in Italy of the investigated parasites.
ParasiteClass1st Intermediate Host2nd Intermediate HostFinal HostHuman SusceptibilityHuman Cases in Italy
Eustrongylides
spp.		NematodeAquatic
oligochaetes		Planktivorous, benthivorous freshwater fishPiscivorous
birds		Accidental hostNone reported
D. latusCestodeCrustacean
copepods		Freshwater fishFish-eating
mammals		Can act as
definitive host		Since 1980:
2–10 cases/year
(Subalpine lakes) [7]
O. felineusTrematodeFreshwater
gastropods
(Genus Bithynia)		Freshwater fish
(Cyprinid)		Fish-eating
mammals		Can act as
definitive host		Since 2003:
periodic outbreaks (Central Italy) [9]
P. truncatumTrematodeFreshwater
gastropods
(Genus Bithynia)		Freshwater fish
(Cyprinid)		Fish-eating
mammals		Can act as
definitive host		None reported
C. complanatumTrematodeFreshwater
gastropods
(Lymnaeidae)		Freshwater fish,
amphibians		Fish-eating
mammals
and birds		Accidental hostNone reported
Table 2. Total length (cm) and weight (g) of fish collected (No.) Prevalence (p), mean intensity (MI) and mean abundance (MA) of Eustrongylides spp. infestation, their standard deviations (SDs), and location of Eustrongylides spp.
Table 2. Total length (cm) and weight (g) of fish collected (No.) Prevalence (p), mean intensity (MI) and mean abundance (MA) of Eustrongylides spp. infestation, their standard deviations (SDs), and location of Eustrongylides spp.
Fish SpeciesFish Specimen DataEustrongylides spp.
Collected No.Weight (g)Weight SD (g)Length (cm)Length SD (cm)pMIMALocation
T. tinca41768.5 ± 1068.91090.741.8 ± 15.015.40 (0/4)---
E. lucius121575.1 ± 727.91286.557.2 ± 10.919.28.3% (1/12)10.08coelomic cavity
S. lucioperca8328.5 ± 250.3361.230.5 ± 6.39.112.5% (1/8)1.00.13muscles
P. fluviatilis1970.0 ± 7.316.317.4 ± 0.51.110.5% (2/19)2.50.26muscles
S. glanis164307.6 ± 1393.62844.181.6 ± 12.926.337.5% (6/16)6.32.75coelomic cavity
Total59 16.9%
(10/59)
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

Macrelli, M.; Ossola, M.; Sala, G.; Accurso, D.; Caffara, M.; Gustinelli, A.; Farioli, M.; Salogni, C. New Findings on the Hosts and Distribution of Eustrongylides excisus (Nematoda: Dioctophymatidae) and Other Zoonotic Parasites in Fish Species from an Uninvestigated Subalpine Lake, Varese Lake (Northwestern Italy). Pathogens 2026, 15, 475. https://doi.org/10.3390/pathogens15050475

AMA Style

Macrelli M, Ossola M, Sala G, Accurso D, Caffara M, Gustinelli A, Farioli M, Salogni C. New Findings on the Hosts and Distribution of Eustrongylides excisus (Nematoda: Dioctophymatidae) and Other Zoonotic Parasites in Fish Species from an Uninvestigated Subalpine Lake, Varese Lake (Northwestern Italy). Pathogens. 2026; 15(5):475. https://doi.org/10.3390/pathogens15050475

Chicago/Turabian Style

Macrelli, Michele, Martina Ossola, Giovanni Sala, Damiano Accurso, Monica Caffara, Andrea Gustinelli, Marco Farioli, and Cristian Salogni. 2026. "New Findings on the Hosts and Distribution of Eustrongylides excisus (Nematoda: Dioctophymatidae) and Other Zoonotic Parasites in Fish Species from an Uninvestigated Subalpine Lake, Varese Lake (Northwestern Italy)" Pathogens 15, no. 5: 475. https://doi.org/10.3390/pathogens15050475

APA Style

Macrelli, M., Ossola, M., Sala, G., Accurso, D., Caffara, M., Gustinelli, A., Farioli, M., & Salogni, C. (2026). New Findings on the Hosts and Distribution of Eustrongylides excisus (Nematoda: Dioctophymatidae) and Other Zoonotic Parasites in Fish Species from an Uninvestigated Subalpine Lake, Varese Lake (Northwestern Italy). Pathogens, 15(5), 475. https://doi.org/10.3390/pathogens15050475

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop