Further Evidence for Plausible Transmission of Fishborne Trematodiases in the United States: Game Fish Carry Human-Infectious Trematodes and Are Eaten Raw (original) (raw)

Abstract

Historically, locally transmitted fishborne trematodiasis has not been a public health concern in the United States (US). However, the widespread introduction of the first intermediate host snail Melanoides tuberculata and 2 of the fishborne trematodes it transmits (Haplorchis pumilio and Centrocestus formosanus), along with their discovery at freshwater fishing localities throughout southern California, reveals a need to further evaluate the risk of local transmission of fishborne trematodiasis in the US. Here, we confirm that the trematode stages infectious to people (metacercariae) commonly infect and can be abundant in 7 commonly caught and eaten fish species at California fishing localities. Further, via an online social media search, we provide evidence that people throughout the US eat those same fish species in ways conducive to trematode transmission (namely, eating fish unfrozen and raw). These findings further indicate the plausibility for locally transmitted fishborne trematodiasis in the US.

Although fishborne trematodiases are globally important [1–4], local transmission has not been a general concern in the United States (US). This is because cases have been rarely reported [5], and because first intermediate host snails that transmit known human-pathogenic fishborne trematodes have historically been lacking in the US [6]. However, this situation has changed. First, the widespread invasion of an exotic snail (Melanoides tuberculata) has brought 2 human-pathogenic fishborne trematodes to the US [6–12]. Second, the snail and its fishborne parasites occur where people catch and eat fish [6]. Third, along with the recent increased popularity of culturally diverse foods [13], there has been an apparent nationwide spike in the consumption of raw fish (eg, as sushi, ceviche, and poke). These factors augment the likelihood of local transmission of fishborne trematodes in the US, warranting further assessment [6].

At least 11 species of human-infecting trematode use the M tuberculata snail as first intermediate host [14]. Native to Asia and Africa, the snail is now globally introduced [15–17], along with at least 3 zoonotic trematodes in the US [6–8, 10–12, 16, 18, 19]. Two of these, Haplorchis pumilio and Centrocestus formosanus, are fishborne. Their free-swimming stages (cercariae) exit infected snails and encyst in second intermediate host fish as metacercariae, which transmit to final hosts (birds and mammals, including humans) that eat infected fish [20, 21]. The adult trematodes, typically 1–2 mm long, infect the small intestine, causing symptoms ranging from mild abdominal discomfort to diarrhea, weight loss, lethargy, and possibly death (see [2, 22] and references therein). Given their impacts and wide distribution, particularly in eastern Asia and the western Pacific, these trematodes are recognized as globally important human pathogens [1].

Although H pumilio and C formosanus have been in the US for 10–20 years [7, 8, 11, 12], they have only recently received substantial attention from a public health perspective. Metz et al [6] documented that infected M tuberculata snails are common at southern California freshwater fishing localities. The authors noted that fish caught and eaten at those localities likely carry infectious metacercariae and emphasized the potential for human infection if fish were eaten in ways conducive to trematode transmission.

Here, we document that the metacercariae of these 2 introduced fishborne trematodes can be common in fishes that people catch and eat at southern California fishing localities. Further, by analyzing videos posted on social media, we confirm the nationwide practice and dissemination of transmission-permissive food preparation and consumption methods involving a range of freshwater fish species, including those known to harbor the fishborne trematodes. These findings underscore the plausibility for their transmission in the US.

MATERIALS AND METHODS

Fish Sampling and Parasitological Processing

In summer–autumn 2023, we obtained fresh fish that were collected and euthanized via routine electrofishing by the California Department of Fish and Wildlife at 5 fishing localities in San Diego County, California, where H pumilio and/or C formosanus were previously detected [6]: Miramar, Murray, Lower Otay, and San Vicente reservoirs, and Chollas Lake.

Because second intermediate host fish often exhibit infection prevalences near 100% (see, eg, [23, 24]), we necropsied a target of 5–10 individual fish per encountered species per locality. In total, we obtained 84 fish of 7 commonly eaten species. Two species were relatively well-sampled and collected from at least 4 of the 5 localities: bluegill (Lepomis macrochirus, n = 39) and largemouth bass (Micropterus salmoides, n = 28). The other 5 species were rarely encountered: green sunfish (Lepomis cyanellus, n = 3), bluegill-green sunfish hybrid (L macrochirus × L cyanellus, n = 3), redear sunfish (Lepomis microlophus, n = 3), black crappie (Pomoxis nigromaculatus, n = 7), and common carp (Cyprinus carpio, n = 1).

Following collection, we transported fish on ice to the laboratory, storing them at −20°C for ≥72 hours to prevent accidental infection during processing [25]. After thawing, we confirmed the species identity using reference [26] and recorded wet weight, standard length, total length, and sex.

We quantified the abundance of H pumilio and C formosanus metacercariae following standard procedures [27]. Squashing fish tissues between 2 glass plates permitted ready detection of encysted metacercariae (usually just over 100 µm diameter) and early stage, migrating “post-cercariae” at a dissecting microscope. We processed the whole body (fins, gills, internal organs, lateral musculature, head, eyes, and orobranchial chamber) and visually inspected the body cavity, peritoneum, and swim bladder for at least the first 5 fish per species. For bilaterally symmetrical structures (pectoral and pelvic fins, gills, lateral musculature, head, and eyes), we examined 1 side and doubled the count. For body parts too large for a squash plate, we quantified metacercariae in weighed subsamples and extrapolated total abundance using the whole to subsample mass ratio. Because these parasites do not typically infect internal organs [12, 28], we only examined the digestive tract, liver, heart, kidney, spleen, gall bladder, urinary bladder, peritoneum, and swim bladder for 1–5 individuals/host species to verify absence. Additionally, because processing largemouth bass heads was particularly time-consuming and yielded only a small proportion of metacercariae (6.9% [95% confidence interval {CI}, 5.4%–8.9%]; n = 14), we used this proportion to infer metacercariae abundance in the heads of the last half of bass (n = 14).

We initially identified H pumilio and C formosanus metacercariae morphologically using published descriptions (see, eg, [23, 29, 30]) and we saved voucher specimens in 95% ethanol for DNA confirmation (see below section “DNA Sequence Analysis”).

Data Analysis

We calculated prevalence as the proportion of infected fish [31] and used Wilson score 95% CIs [32].

For species with adequate sample sizes and body size variation, we examined how metacercaria abundance varied among localities and with fish size, using negative binomial generalized linear models in the R MASS package [33]. The global model included, as predictors, fish species, total length, fishing locality, and all 2-way and 3-way interactions.

We assessed H pumilio distribution within host bodies using multinomial logistic regression with the R package mclogit (version 0.9.6) [34]. The global model included, as predictors, host species, host weight, sex, fishing locality, and the 2-way interactions of weight with host species, sex, and fishing locality; individual host was a random effect. Included body parts were the head, gills, lateral musculature (“fillets”), caudal fin, and noncaudal fins.

We excluded San Vicente fish from the generalized linear model analyses due to the lack of largemouth bass and the very small size range of bluegill from that location.

We used Akaike information criterion (AIC) model selection for global and simplified models, considering those with ΔAIC ≤2 as “supported” [35]. Model adequacy was assessed using plots of Pearson residuals versus predicted values for the global models [35, 36].

DNA Sequence Analysis

We obtained ribosomal 28S and/or mitochondrial cytochrome c oxidase I (COI) sequences for each parasite species from each location and host species. Given their small size, we pooled 2 to 3 ethanol-fixed, morphologically identified metacercariae per individual host, rehydrating them in deionized water. We excised worms from their cysts with needles before DNA extraction using a 1-hour proteinase K digestion (Supplementary Table 1), using the resultant lysate for polymerase chain reaction.

We amplified 28S using primers dig12 and 1500R following the method in Tkach et al [37] (Supplementary Table 1) and amplified COI using primers JB3 and COI R-Trema [38], modified by adding sequencing tails (Supplementary Table 1). We used unidirectional Sanger sequencing (Eton Biosciences, San Diego, California), and manually trimmed sequences by eye. We compared sequences to GenBank sequences available as of 21 October 2024 via a blastn search.

Social Media Data Mining

We searched YouTube in January–February 2024 for videos of people in the US consuming raw freshwater fish. We anonymized personally identifiable information of retrieved videos, but note that ethical reviews are not required for data mining publicly available social media [39, 40].

As search terms, we used combinations of 6 dishes or consumption methods that frequently involve raw fish, and the common names of 155 state-managed freshwater fish found in states with known M tuberculata populations (Table 1, Supplementary Table 2). We excluded videos featuring store-bought fish, the eating of only washed fish eggs, and those that could not be confirmed as originating in the US or bordering water bodies.

Table 1.

Lists of Words Used in Combination to Search for YouTube Videos Portraying Risky Consumption Practices of Targeted Freshwater Fish Species From California

Please see Supplementary Table 2 for a list of fish species for all US states with known Melanoides tuberculata populations.

Table 1.

Lists of Words Used in Combination to Search for YouTube Videos Portraying Risky Consumption Practices of Targeted Freshwater Fish Species From California

Please see Supplementary Table 2 for a list of fish species for all US states with known Melanoides tuberculata populations.

For each video, we determined the food preparation method, classifying fish as being consumed “fresh” and raw if creators did not explicitly mention freezing (verbally or in writing) and there was no other evidence indicating freezing (eg, fish prepared and eaten outdoors soon after capture). We also recorded the number of views, fish capture/preparation location, body parts consumed, any cautionary warnings or food safety misinformation presented, and whether the video had been posted elsewhere online.

RESULTS

Trematode Metacercaria Prevalence, Abundance, and Host-Tissue Use

Each examined fish species harbored metacercariae (Figure 1), >99% of which morphologically corresponded to H pumilio or C formosanus. Species identities were confirmed by 28S DNA (508–706 bp) and/or COI DNA (593–752 bp) sequences from parasites from each examined fish species and from each locality (Supplementary Table 3). The putative H pumilio sequences closely matched GenBank records for that species from the native and introduced ranges (≥99.1% similarity for 28S and >97.5% for COI). Similarly, putative C formosanus sequences provided close matches to GenBank records (>99.8% 28S, >98.1% COI).

Figure 1.

The infectious stages (metacercariae) of 2 introduced, zoonotic trematodes occur in commonly captured and eaten freshwater fish species in southern California. A and B, Examples of the 2 most common host species sampled in this study, bluegill (Lepomis macrochirus) (A) and largemouth bass (Micropterus salmoides) (B). C–H, Examples of metacercariae of Haplorchis pumilio (left panels) and Centrocestus formosanus (right): in situ in a squash of a host fin or gills, with red arrowheads marking some visible metacercariae (C and D); isolated from host tissues (E and F); and extracted from the cyst, where G represents a young H pumilio metacercaria and H a more-developed C formosanus. All specimens were previously frozen and thawed. Scale in A and B is indicated by the 30-cm rulers. Photos were slightly enhanced to increase contrast and sharpness.

Haplorchis pumilio was the most common trematode. It infected each of the 7 examined fish species (including 5 new host records) and occurred at each of the 5 localities (Figure 2, Supplementary Figure 1). Haplorchis pumilio prevalence ranged from 80% to 100% per locality in both bluegill and largemouth bass, with an overall prevalence among all fish of 93% (95% CI, 85%–97%; 78/84 fish]). Mean H pumilio abundances varied among localities and species, ranging from 3 to 5166 in bluegill and 18 to 185 in largemouth bass (Figure 2, Supplementary Tables 4 and 5). Haplorchis pumilio abundance increased with fish size for both fish species at different rates among localities (Supplementary Figure 2, Supplementary Tables 4 and 5). Despite some variation with fish size and among species in the way H pumilio metacercariae were distributed within host bodies, most H pumilio metacercariae occurred in the connective tissue (including muscle tissue) of the fin bases (90% across all species), as consistent with prior research [12, 28, 41] (Figure 3, Supplementary Figure 3, Supplementary Tables 6 and 7).

Figure 2.

The abundance and prevalence of metacercariae of 2 zoonotic trematodes, Haplorchis pumilio and Centrocestus formosanus, in game fishes sampled at southern California fishing localities. A, Infection abundance and prevalence in the 2 most highly sampled fish species by locality. B, Infection abundance and prevalence in 5 rarely sampled fish species; these species were each collected at only a single locality, except for the redear sunfish, which was collected at 2 localities. Infection abundances are plotted as abundance +1 to permit log-scaling of axis (therefore, a load of 1 [=100] truly equals 0). Those locality and rare fish species names that are intuitively abbreviated in x-axis labels are spelled out in full in the key or, for the fishes, here: bluegill (Lepomis macrochirus), largemouth bass (Micropterus salmoides), green sunfish (Lepomis cyanellus), bluegill-green sunfish hybrid (Lepomis macrochirus × Lepomis cyanellus), redear sunfish (Lepomis microlophus), black crappie (Pomoxis nigromaculatus), and common carp (Cyprinus carpio). Supplementary Figure 1 shows the corresponding prevalences with 95% confidence intervals. Abbreviation: pptn, proportion.

Figure 3.

The proportional abundance of all counted Haplorchis pumilio metacercariae among different host tissues for each of the examined host species. When in fins, most metacercariae concentrate in fin bases, where they insert into host musculature. Host species names are intuitively abbreviated in the figure and are spelled out here: bluegill (Lepomis macrochirus), largemouth bass (Micropterus salmoides), green sunfish (Lepomis cyanellus), bluegill-green sunfish hybrid (Lepomis macrochirus × Lepomis cyanellus), redear sunfish (Lepomis microlophus), black crappie (Pomoxis nigromaculatus), and common carp (Cyprinus carpio). Supplementary Figure 3 shows H pumilio proportional abundance versus host size for bluegill and largemouth bass. Abbreviation: Orobranch. cav., orobranchial cavity.

Centrocestus formosanus infected bluegill and largemouth bass at 2 of the 5 localities and infected 2 of the rare fish species at 1 of those localities (Figure 2, Supplementary Figure 1). Where present, prevalence was 83%–100% in bluegill and largemouth bass, with an overall prevalence of 89% among all fish (95% CI, 75%–96%; 32/36). Abundance ranged from 0 to 146 metacercariae per fish of each species, with statistically indistinguishable mean abundances among the 2 localities in the adequately sampled bluegill fish (Figure 2, Supplementary Tables 8 and 9). Also in bluegill, abundance increased with fish total length, but only in 1 of the 2 supported models (Supplementary Figure 2, Supplementary Tables 8 and 9; P < .001). Low sample size (n = 11) precluded usefully examining the metacercaria abundance versus host size relationship for bass (Supplementary Figure 2). Consistent with prior work [28, 42], C formosanus metacercariae were primarily in the gills, with a few in surrounding tissue.

Evidence for Raw Fish Consumption

We documented consumption of target fish in the US in ways that permit trematode transmission in 125 videos from YouTube (Figure 4A). The videos were published between January 2008 and January 2024 across 110 channels from 108 content creators and had collectively amassed 4.7 million views (median, 1049 [range, 15–2 361 664]).

Figure 4.

Videos posted on YouTube indicate that people in the United States do eat raw, unfrozen fish, including each species that we document as harboring infectious metacercariae of Haplorchis pumilio and Centrocestus formosanus. A, Distribution of the 83 instances where videos showed different game fish being eaten raw (and never frozen) among fish taxonomic families (common names for family groups). Bar color indicates whether a family includes fish species known to host either parasite. B, Number of those videos filmed in different states (for the 49 videos where state could be inferred), and an indication of whether the Melanoides tuberculata snail or the snail and at least 1 of the fishborne trematode species it transmits have been reported from the state [6–12, 15–19].

We categorized videos into 2 categories, “raw-fish dish” and “shock factor.” Raw-fish dish videos represented 82% (103/125) of the videos and 99.5% of the total views. These videos followed a typical format where fish were caught and prepared for consumption in a dish that traditionally uses raw fish. Ironically, these videos were usually tagged or entitled with the popular social media tag “catch and cook.” Yet we classified 65% (67/103) of these videos as depicting the consumption of raw fish, with 59 involving raw and unfrozen fish. Additionally, 22% (11/50) of the individual video creators who ate raw, unfrozen fish stated that they had previously made the same dish. Raw-fish dishes most typically involved the consumption of the fish fillet (lateral body musculature).

In contrast, 22 “shock factor” videos showcased individuals eating, in a nonculinary manner, a range of tissues or organs including the eyes, body cavity organs, head, heart, spinal musculature, and occasionally even the whole fish. Of these videos, 32% (7/22) of consumption was instigated by bets or dares posed by onlookers.

We determined the geographic location to the state level of 49 videos showing people eating raw, unfrozen fish. Of those videos, 49% (24/49) were filmed in states with previous documentation of H pumilio and C formosanus, and an additional 27% (13/49) were filmed in states with only M tuberculata documentation (Figure 4B).

In total, video participants consumed at least 31 fish species. Fish known to host H pumilio and/or C formosanus were featured in 31 (25%) videos. More than half of these (18/31) involved consumption of raw, unfrozen fish. Additionally, 10 of those 31 videos were filmed in locations with known M tuberculata populations.

Many videos presented misinformation concerning the safe consumption of raw fish. The most common type of misinformation (16 videos) featured ceviche and the claim that marination with citrus juices cooks the fish, making it safer to eat. The second and third misconceptions, occurring in 3 videos each, were that “healthy fish” or those obtained from “clean streams” could be consumed raw. Finally, 1 video incorrectly stated that parasites could be detected by “candling,” where one visually examines the tissue held up to a strong light.

DISCUSSION

Our findings provide further evidence for the possible transmission of fishborne trematodiases in the US. Previous work established that the 2 introduced, fishborne trematodes (H pumilio and C formosanus) are widespread in the US in the first intermediate host snail, M tuberculata [6–8, 11, 19, 43]. Metz et al [6] then showed that M tuberculata snails infected by at least 1 of those trematode species can be common and widespread at freshwater fishing localities, as demonstrated in California. Our study expands on those findings to confirm that, in at least some of those same localities, the metacercariae of H pumilio and C formosanus infect fish species that are caught and eaten by people throughout the US. Moreover, we present evidence that people throughout the US sometimes prepare and eat these and other fish species in ways conducive to the transmission of fishborne trematodes.

Human-Infectious Metacercariae Are in Commonly Caught and Eaten Fish Species

We found metacercariae of 1 or both fishborne trematodes in game fish at every sampled locality. Haplorchis pumilio itself was found at each sampled locality, corresponding with it having been the most prevalent trematode in the prior survey of the first intermediate host throughout southern California [6]. Similarly, C formosanus was rare in that prior survey of M tuberculata and was detected in our survey from only 2 of the 5 localities. In any case, these findings clarify that the human-infectious stages of the 2 fishborne trematodes occur in fish in areas where people actively catch and eat fish.

Moreover, metacercariae of 1 or both trematodes infected each examined species of fish. Despite these trematodes already being known to infect many fish species as second intermediate host [9, 12, 28, 42–44], our study adds 5 additional human-consumed fish species as known hosts for H pumilio. These findings clarify that the infectious stages of the 2 fishborne trematodes occur in specific types of fish commonly caught and eaten throughout the US.

Together, the parasites also infected a high percentage of fish (often 100%) and sometimes did so at high abundances (hundreds to thousands of metacercariae per fish). Consequently, a fisherperson is very likely to capture infected fish harboring appreciable quantities of infectious metacercariae.

People in the US Eat Raw Freshwater Fish in Ways Conducive to Fishborne Trematode Transmission

For people eating freshwater fish infected with foodborne trematodes, the main factor likely modulating transmission risk is the mode of food preparation. For instance, freezing fish prior to use in raw fish preparations will inactivate metacercariae and prevent infection [25, 45]. However, 65% (81/125) of our analyzed videos depicted the consumption of raw, unfrozen fish, clearly opening the door to trematode infection.

Something that would seem to reduce infection risk by the 2 studied trematodes, when eating fish raw in a culinary manner, is the typical practice of eating the fish fillet (lateral musculature). This should help avoid C formosanus metacercariae, which reside in the gills, and possibly many H pumilio metacercariae, which are concentrated in the fin bases (both confirmed in this study). However, because the fish fin bases are embedded at the edges of a typical fish fillet, many H pumilio metacercariae could still be in or contaminate the fillet. In fact, human infections by each of these species have been documented in several Asian countries [1], clarifying that their localization in fish bodies does not preclude them being important for public health.

In contrast to the way eating a fillet might reduce infection risk, shock factor videos documented particularly transmission-conducive behavior. Here, people consumed a range of tissues, including the entire head or whole fish. This practice therefore involves ingesting many metacercariae that might be avoided by consuming only the fillet. Hence, while less common and less viewed than the raw-fish dish videos, shock factor fish-eating behavior should be kept in mind as a possible mode of transmission by clinicians and public health officials.

The risky food preparation behavior is likely more pervasive than the limited amount directly captured on social media. For instance, many video creators stated that they had previously made the same raw-fish dish before filming the video. That is, those videos were not of one-time, unusual events. Further, the nearly 5 million total views of the videos further suggest the widespread interest in, and practice of, eating freshwater fish raw in the US.

Misconceptions Concerning the Safety of Eating Raw Fish

We found several food safety misconceptions repeated in these videos. Among the most common erroneous claims were that (1) marination reliably kills parasites, (2) “healthy looking” fish are safe to eat, (3) fish from “clean streams” do not carry parasites, and (4) visual inspection of fish meats (eg, “candling”) can readily detect parasites. Contrary to these claims, acid marination does not reliably reduce infection risk [25, 46], fishes infected with foodborne parasites often have no detectable gross pathology [47], parasites often thrive in nonpolluted environments [48, 49], and many foodborne parasites (including the trematodes discussed here) are not visible in muscle tissues without high magnification [46, 50]. These misconceptions may be particularly important because they reflect infection risk by not only the 2 study species, but also by other fishborne parasites not encountered in our study. Hence, such food safety misconceptions should be considered in any efforts to mitigate the risk of transmission of fishborne trematodes or other fishborne parasites.

Risk of Local Transmission Is Likely Widespread in the US but Might Be Easily Mitigated

There is a plausible risk of transmission of H pumilio and C formosanus anywhere people eat freshwater fish from where the M tuberculata snail is present. Currently, M tuberculata is known from 17 states and Puerto Rico [16], and at least 1 of its fishborne trematodes infects the snail in at least 4 of those states: California, Utah, Texas, and Florida (Figure 4B) [6–8, 10, 12]. The lack of reports of the trematodes in the other 13 states likely reflects a lack of appropriate survey effort, given that final host birds can spread the trematodes across wide geographical ranges and because infected snails can transmit the trematodes to a broad range of fish. The potential risk is further supported by our finding that approximately three-quarters of the videos of raw fish consumption were filmed in states where the parasites or the first intermediate host snail are known to occur. Hence, the possibility of local transmission of H pumilio and C formosanus is likely widespread throughout the US.

Public education may be the most important control measure where fishborne trematodiases are endemic [1, 25]. Education concerning transmission risk and mitigation measures could be usefully undertaken wherever the snails are common, if not more broadly. We also suggest that clinicians should be informed, and that foodborne trematodiases be added to the lists of reportable diseases throughout the US to permit more accurate tracking of this emerging risk.

CONCLUSIONS

The fishborne intestinal trematodes Haplorchis pumilio and Centrocestus formosanus infect several species of commonly consumed freshwater fish at fishing sites in San Diego County, California, and almost certainly do so more widely throughout the US. Further, people throughout the country appear to engage in activities that facilitate transmission, including eating raw freshwater fish of species that harbor these trematodes. Consequently, locally transmitted fishborne trematodiasis is a plausible health concern in the US.

Public health officials should consider steps to increase public awareness of the risks and the simple measures that can effectively reduce that risk. In addition, informing clinicians about the potential for locally transmitted fishborne trematodiasis would improve diagnosis and tracking of these infections in the US.

Supplementary Data

Supplementary materials are available at The Journal of Infectious Diseases online (http://jid.oxfordjournals.org/). Supplementary materials consist of data provided by the author that are published to benefit the reader. The posted materials are not copyedited. The contents of all supplementary data are the sole responsibility of the authors. Questions or messages regarding errors should be addressed to the author.

Notes

Acknowledgments. We thank Matt Lucero and the California Department of Fish and Wildlife for providing us with fish, and 3 anonymous reviewers for evaluating the manuscript.

Author contributions. Project conception and supervision: R. F. H. and E. M. P. Data acquisition and analysis: E. M. P., R. F. H., and D. C. G. M. Manuscript drafting: E. M. P. and R. F. H. Manuscript editing: E. M. P., R. F. H., and D. C. G. M.

Financial support. This project received financial support from the National Institutes of Health (grant number 1R03AI156569-01 to R. F. H.).

References

1

Chai

J-Y

,

Jung

B-K

.

General overview of the current status of human foodborne trematodiasis

.

Parasitology

2022

;

149

:

1262

–

85

.

2

Sripa

B

,

Kaewkes

S

,

Intapan

PM

,

Maleewong

W

,

Brindley

PJ

.

Food-borne trematodiases in Southeast Asia: epidemiology, pathology, clinical manifestation and control

.

Adv Parasitol

2010

;

72

:

305

–

50

.

3

Furst

T

,

Keiser

J

,

Utzinger

J

.

Global burden of human food-borne trematodiasis: a systematic review and meta-analysis

.

Lancet Infect Dis

2012

;

12

:

210

–

21

.

4

World Health Organization (WHO) and the Food and Agriculture Organization of the United Nations (FOA)

.

Multicriteria-based ranking for risk management of food-borne parasites: report of a joint FAO/WHO expert meeting, 3–7 September 2012

.

Rome, Italy

:

FOA

,

2014

:

302

.

5

Fried

B

,

Abruzzi

A

.

Food-borne trematode infections of humans in the United States of America

.

Parasitol Res

2010

;

106

:

1263

–

80

.

6

Metz

DCG

,

Turner

AV

,

Nelson

AP

,

Hechinger

RF

.

Potential for emergence of foodborne trematodiases transmitted by an introduced snail (Melanoides tuberculata) in California and elsewhere in the United States

.

J Infect Dis

2023

;

227

:

183

–

92

.

7

Mitchell

AJ

,

Salmon

MJ

,

Huffman

DG

,

Goodwin

AE

,

Brandt

TM

.

Prevalence and pathogenicity of a heterophyid trematode infecting the gills of an endangered fish, the fountain darter, in two central Texas spring-fed rivers

.

J Aquat Anim Health

2000

;

12

:

283

–

9

.

8

Mitchell

AJ

,

Overstreet

RM

,

Goodwin

AE

,

Brandt

TM

.

Spread of an exotic fish-gill trematode

.

Fisheries

2005

;

30

:

11

–

6

.

9

McDermott

KS

,

Arsuffi

TL

,

Brandt

TM

,

Huston

DC

,

Ostrand

KG

.

Distribution and occurrence of the exotic digenetic trematode (Centrocestus formosanus), its exotic snail intermediate host (Melanoides tuberculatus), and rates of infection of fish in springs systems in western Texas

.

Southwest Nat

2014

;

59

:

212

–

20

.

10

Tolley-Jordan

L

,

Chadwick

M

,

Triplett

J

.

New records of digenetic trematodes infecting Melanoides tuberculata (O.F. Mueller, 1774) in Florida, USA

.

Bioinvasions Rec

2022

;

11

:

149

–

64

.

11

Tolley-Jordan

LR

,

Owen

JM

.

Habitat influences snail community structure and trematode infection levels in a spring-fed river, Texas, USA

.

Hydrobiologia

2008

;

600

:

29

–

40

.

12

Huston

DC

,

Worsham

MD

,

Huffman

DG

,

Ostrand

KG

.

Infection of fishes, including threatened and endangered species by the trematode parasite Haplorchis pumilio (Looss, 1896) (Trematoda: Heterophyidae)

.

Bioinvasions Rec

2014

;

3

:

189

–

94

.

13

Lee

JH

,

Hwang

J

,

Mustapha

A

.

Popular ethnic foods in the United States: a historical and safety perspective

.

Compr Rev Food Sci Food Saf

2014

;

13

:

2

–

17

.

14

Pinto

HA

,

Melo

AL

.

A checklist of trematodes (Platyhelminthes) transmitted by Melanoides tuberculata (Mollusca: Thiaridae)

.

Zootaxa

2011

;

2799

:

15

–

28

.

15

CABI

.

Datasheet: Melanoides tuberculata (red-rimmed melania) [original text by B Facon and JP Pointier]. Invasive species compendium

.

Wallingford, UK

:

CAB International

,

2020

.

16

Chalkowski

K

,

Abigail

M

,

Christopher

AL

,

Sarah

Z

.

Spread of an avian eye fluke, Philophthalmus gralli, through biological invasion of an intermediate host

.

J Parasitol

2021

;

107

:

336

–

48

.

17

Murray

HD

.

The introduction and spread of thiarids in the USA

.

Biologist (Charlest)

1971

;

53

:

133

–

5

.

18

Church

ML

,

Barrett

PM

,

Swenson

J

,

Kinsella

JM

,

Tkach

VV

.

Outbreak of Philophthalmus gralli in four greater rheas (Rhea americana)

.

Vet Ophthalmol

2013

;

16

:

65

–

72

.

19

Nollen

PM

,

Murray

HD

.

_Philophthalmus gralli_—identification, growth characteristics, and treatment of an oriental eyefluke of birds introduced into continental United States

.

J Parasitol

1978

;

64

:

178

–

80

.

20

Yanohara

Y

.

On analysis of transmission dynamics of trematode infection 1. Centrocestus formosanus infection in Miyakojima, Okinawa

.

Jpn J Parasitol

1985

;

34

:

55

–

70

.

21

Khalifa

R

,

El-Naffar

MK

,

Arafa

MS

.

Studies on heterophyid cercariae from Assiut Province Egypt. Part I. Notes on the life cycle of Haplorchis pumilio with a discussion on previously described species

.

Acta Parasitol Pol

1977

;

25

:

25

–

38

.

22

Chai

J-Y

,

Jung

B-K

.

Fishborne zoonotic heterophyid infections: an update

.

Food Waterb Parasitol

2017

;

8–9

:

33

–

63

.

23

Scholz

T

,

Aguirre-Macedo

ML

,

Salgado-Maldonado

G

.

Trematodes of the family Heterophyidae (Digenea) in Mexico: a review of species and new host and geographical records

.

J Nat Hist

2001

;

35

:

1733

–

72

.

24

Shaw

JC

,

Hechinger

RF

,

Lafferty

KD

,

Kuris

AM

.

Ecology of the brain trematode Euhaplorchis californiensis and its host, the California killifish (Fundulus parvipinnis)

.

J Parasitol

2010

;

96

:

482

–

90

.

25

Abdussalam

M

,

Käferstein

FK

,

Mott

KE

.

Food safety measures for the control of foodborne trematode infections

.

Food Control

1995

;

6

:

71

–

9

.

26

McGinnis

SM

,

Alcorn

D

.

Field guide to freshwater fishes of California

. (Rev ed) .

Berkeley

:

University of California Press

,

2006

.

27

Vidal-Martínez

VM

,

Aguirre-Macedo

ML

,

McLaughlin

JP

, et al.

Digenean metacercariae of fishes from the lagoon flats of Palmyra Atoll, Eastern Indo-Pacific

.

J Helminthol

2012

;

86

:

493

–

509

.

28

Lo

CT

,

Lee

K-M

.

Infectivity of the cercariae of Centrocestus formosanus and Haplorchis pumilio (Digenea: Heterophyidae) in Cyprinus carpio

.

Zool Stud

1996

;

35

:

305

–

9

.

29

Diaz

M

,

Hernandez

L

,

Bashirullah

A

.

Studies on the life cycle of Haplorchis pumilio (Looss, 1896) (Trematoda: Heterophyidae) in Venezuela

.

Revista Cientifica

2008

;

18

:

35

–

42

.

30

Han

E-T

,

Shin

E-H

,

Phommakorn

S

, et al.

Centrocestus formosanus (Digenea: Heterophyidae) encysted in the freshwater fish, Puntius brevis, from Lao PDR

.

Korean J Parasitol

2008

;

46

:

49

–

53

.

31

Bush

AO

,

Lafferty

KD

,

Lotz

JM

,

Shostak

AW

.

Parasitology meets ecology on its own terms: Margolis et al revisited

.

J Parasitol

1997

;

83

:

575

–

83

.

32

Newcombe

RG

.

Two-sided confidence intervals for the single proportion: comparison of seven methods

.

Stat Med

1998

;

17

:

857

–

72

.

33

Venables

WN

,

Ripley

BD

,

Venables

WN

.

Modern applied statistics with statistics and computing

. (4th ed) .

New York

:

Springer

,

2002

.

34

Elff

M

. mclogit: multinomial logit models, with or without random effects or overdispersion. R package vers. 0.9.6. http://melff.github.io/mclogit/. Accessed 29 May 2023.

35

Burnham

KP

,

Anderson

DR

.

Model selection and multimodel inference: a practical information-theoretic approach

. (2nd ed) .

New York

:

Springer

,

2002

.

36

Myers

RH

,

Montgomery

DC

,

Vining

GG

,

Robinson

TJ

.

Generalized linear models: with applications in engineering and the sciences

. (2nd ed) .

Hoboken, NJ

:

Wiley

,

2010

.

37

Tkach

VV

,

Littlewood

DTJ

,

Olson

PD

,

Kinsella

JM

,

Swiderski

Z

.

Molecular phylogenetic analysis of the Microphalloidea ward, 1901 (Trematoda: Digenea)

.

Syst Parasitol

2003

;

56

:

1

–

15

.

38

Miura

O

,

Kuris

AM

,

Torchin

ME

,

Hechinger

RF

,

Dunham

EJ

,

Chiba

S

.

Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse)

.

Int J Parasitol

2005

;

35

:

793

–

801

.

39

Monkman

GG

,

Kaiser

M

,

Hyder

K

.

The ethics of using social media in fisheries research

.

Rev Fis Sc Aquac

2018

;

26

:

235

–

42

.

40

Sbragaglia

V

,

Correia

RA

,

Coco

S

,

Arlinghaus

R

.

Data mining on YouTube reveals fisher group-specific harvesting patterns and social engagement in recreational anglers and spearfishers

.

ICES J Mar Sci

2020

;

77

:

2234

–

44

.

41

Sommerville

C

.

The life history of Haplorchis pumilio (Looss, 1896) from cultured tilapias

.

J Fish Dis

1982

;

5

:

233

–

41

.

42

Scholz

T

,

Salgado-Maldonado

G

.

The introduction and dispersal of Centrocestus formosanus (Nishigori, 1924) (Digenea: Heterophyidae) in Mexico: a review

.

Am Midl Nat

2000

;

143

:

185

–

200

.

43

Mitchell

AJ

,

Goodwin

AE

,

Salmon

MJ

,

Brandt

TM

.

Experimental infection of an exotic heterophyid trematode, Centrocestus formosanus, in four aquaculture fishes

.

N Am J Aquac

2002

;

64

:

55

–

9

.

44

Salgado-Maldonado

G

,

Cabañas-Carranza

G

,

Aguilar-Aguilar

R

.

A checklist of helminth parasites of freshwater fishes from the Lerma-Santiago river basin, Mexico

.

Comp Parasitol

2001

;

68

:

204

–

18

.

45

Franssen

F

,

Gerard

C

,

Cozma-Petruţ

A

, et al.

Inactivation of parasite transmission stages: efficacy of treatments on food of animal origin

.

Trends Food Sci Technol

2019

;

83

:

114

–

28

.

46

US Food and Drug Administration

.

Fish and fishery products hazards and controls guidance

.

Washington, DC

:

US Department of Health and Human Services, US Food and Drug Administration, Center for Food Safety and Applied Nutrition

,

2022

:

40

.

47

Hoffman

GL

.

Parasites of North American freshwater fishes

. (2nd ed) .

Ithaca, NY

:

Cornell University Press

,

1999

.

48

Marcogliese

DJ

.

Parasites of the superorganism: are they indicators of ecosystem health?

Int J Parasitol

2005

;

35

:

705

–

16

.

49

Hudson

PJ

,

Dobson

AP

,

Lafferty

KD

.

Is a healthy ecosystem one that is rich in parasites?

Trends Ecol Evol

2006

;

21

:

381

–

5

.

50

World Health Organization

.

Control of foodborne trematode infections.

Geneva, Switzerland

:

World Health Organization

,

1995

.

Author notes

Present affiliation: Smithsonian Environmental Research Center, Edgewater, Maryland, USA.

Present affiliation: School of Biological Sciences, University of Nebraska–Lincoln, Lincoln, Nebraska, USA.

Potential conflicts of interest. The authors: No reported conflicts of interest.

All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.

© The Author(s) 2025. Published by Oxford University Press on behalf of Infectious Diseases Society of America.

This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact [email protected] for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact [email protected].