Skip to main content
NCBI home page
Food and Waterborne Parasitology logoLink to Food and Waterborne Parasitology
. 2026 Feb 18;42:e00321. doi: 10.1016/j.fawpar.2026.e00321

Fish-borne trematode metacercarial infections as bioindicators for heavy-metal contamination in cyprinoid fish from Northeastern Thailand

Lakhanawan Charoensuk a, Chadon Nakmai b,c, Picha Suwannahitatorn d, Krissada Namboonrueng c,e, Somchai Pinlaor f,g, Suksanti Prakobwong c,h,⁎
PMCID: PMC12950442  PMID: 41778097

Abstract

In Southeast Asia, consumption of raw or undercooked cyprinoid fish poses dual health concerns: transmission of zoonotic fish-borne trematodes (FBTs) and exposure to heavy metals that have bioaccumulated in fish. We investigated the association between heavy-metal contamination and FBT metacercarial infections in cyprinoid fish from canals connected to the Huay Luang River, Udon Thani Province, Thailand, during the 2024 rainy season. In total, 1377 fish were examined for metacercariae using the pepsin digestion method. Concentrations of five heavy-metals (Cd, Zn, Cu, Ni, and Pb) were quantified by atomic absorption spectrometry (AAS) in infected fish, uninfected fish, water, sediment, and Bithynia snails. The overall prevalence of infection was 8.5%, with mean intensities of 1.6–3.6 metacercariae/infected fish. Infected fish contained significantly higher Cd (1.63 ppm), Cu (11.06 ppm), and Zn (68.51 ppm) than uninfected fish (P ≤ 0.001). Pearson correlation revealed positive associations between metacercarial prevalence and all metal concentrations, except Pb (P < 0.05). Multivariable regression identified Cd as the strongest predictor of infection intensity, with each 1-ppm increase associated with 5.36 additional metacercariae/infected fish (P < 0.001). Bioaccumulation factors were higher in infected fish for Cd (ratio 1.3), Zn (ratio 1.6), and Cu (ratio 1.4) compare to uninfected fish, while Pb was lower. Spatial analysis identified three sites where elevated Cd overlapped with high parasite intensity. These findings establish FBT metacercariae as site-specific bioindicators of heavy-metal accumulation, highlighting the public-health risk from co-exposure and their potential use in food safety and ecosystem monitoring.

Keywords: Fish-borne trematodes, Heavy metal contamination, Cadmium, Cyprinoid fish, metacercarial infection.

Graphical abstract

Unlabelled Image

Open in a new tab

Highlights

  • •

    Raw cyprinoid fish pose dual health risks: FBT parasites and heavy metals.

  • •

    Infected fish had significantly higher Cadmium (Cd), Copper (Cu), and Zinc (Zn).

  • •

    FBT prevalence correlated positively with Cd, Zn, Cu, and Ni levels.

  • •

    Cadmium (Cd) was the strongest predictor of parasite infection intensity.

  • •

    FBT metacercariae are potential bioindicators for heavy-metal accumulation.

1. Introduction

Fish-borne trematodes (FBTs) are neglected zoonotic parasites that pose a major public health concern in Southeast Asia, especially in regions where eating raw or undercooked freshwater fish is culturally ingrained (Nguyen et al., 2023; Sripa et al., 2021). FBT species such as Opisthorchis viverrini and Haplorchis taichui require freshwater snails and cyprinoid fish as intermediate hosts before reaching definitive hosts such as humans or other fish-eating mammals (Saijuntha et al., 2023). Chronic infection with the parasitic liver fluke, O. viverrini, is a leading cause of severe hepatobiliary complications, including cholangiocarcinoma (bile duct cancer), which remains endemic in northeastern Thailand due to regional dietary practices (Sripa et al., 2021). Despite ongoing public health efforts, transmission persists due to complex ecological and environmental factors. Emerging evidence suggests that heavy-metal contamination in aquatic habitats may influence host susceptibility and parasite transmission (Sures, 2008). Accordingly, FBT metacercarial infections are increasingly recognized not only as parasitic threats but also as potential bioindicators of heavy-metal pollution in freshwater ecosystems.

Heavy-metal contamination is an important ecological stressor influencing freshwater parasitic infections and a concurrent threat to human health through consumption of contaminated aquatic organisms (El-Hak et al., 2022; Radwan et al., 2022). Metals such as cadmium, copper, and zinc enter aquatic environments through industrial effluents, agricultural runoff, and improper waste disposal, leading to accumulation in water, sediment, and aquatic organisms (Awasthi et al., 2023). These metals are non-biodegradable and can bioaccumulate in fish tissues, impairing early development, growth, reproduction, immune function, and physiological responses (Mehana et al., 2020; Taslima et al., 2022). These physiological impairments may heighten host susceptibility to FBT metacercarial encystment (Oros, 2025). In a recent field study conducted in natural canals connected to the Huay Luang River in northeastern Thailand, metacercarial infection rates in cyprinoid fish were significantly associated with environmental contamination from agricultural runoff, fecal pollution, and improper waste disposal, highlighting a potential link between pollution exposure and parasite burden (Namboonrueng et al., 2024; Phitaktim et al., 2023). These findings suggest that metal pollution may indirectly increase the risk of parasitic infections in fish populations.

Beyond their role in disease, helminths such as trematodes, nematodes and acanthocephalans exhibit exceptional capacity to accumulate heavy metals at levels far exceeding those in host tissues, in monitoring the ecosystem pollutions and their relationship with each other (Mehana et al., 2020; Sures et al., 1998). Parasitized fish were found to exhibit distinct heavy-metal profiles, indicating that the presence of parasites may serve as a marker of localized contamination (Radwan et al., 2022). While helminths are established bioindicators of pollutants, little is known about whether FBT metacercariae specifically can serve this role in field settings. Therefore, this study aims to investigate the association between heavy-metal accumulation and FBT metacercarial infections in cyprinoid fish from natural canals in Udon Thani Province, northeastern Thailand. Concentrations of five heavy metals (Cd, Zn, Cu, Ni, and Pb) were quantified using atomic absorption spectrometry (AAS) in samples of water, canal sediment, Bithynia snails and fish tissues. Metacercariae in fish were obtained by the pepsin digestion method, identified and counted. The study could serve as basic information to provide evidence supporting the use of metacercarial infections as practical indicators for freshwater pollution monitoring and assessing potential public health risks from fish-borne exposure to heavy metals and zoonotic parasites.

2. Materials and methods

2.1. Study area and sample collection

The cross-sectional study was conducted during the rainy season from May to November 2024 in endemic areas of Udon Thani Province, northeastern Thailand. This province contains extensive irrigation canals connected to the Huay Luang River, which supports major agriculture and fisheries activities (Table 1). Sampling was conducted once per month at six canal sites located near urban areas, agricultural fields, and residential communities to represent habitats influenced by waste discharge and anthropogenic pollution. At each monthly visit, water, canal sediment, Bithynia snails, and cyprinoid fish were collected concurrently at all sites.

Table 1.

Sampling sites, geographic coordinates, prevalence, and intensity of FBT infection in cyprinoid fish.

Sampling site Coordinates (latitude, longitude) Location description Number of cyprinoid fish Number of FBT-infected fish (%) Intensity (metacercariae/infected fish)
1 17°29′29.3”N 102°45′54.0″E Subdistrict community with agricultural activity, located at the confluence of two rivers 244 10 (4.1%) 2.8
2 17°23′40.4”N 102°47′34.8″E Urban downtown area with high population density, mixed residential housing, commercial businesses, and government as well as non-government offices 231 14 (6.1%) 1.6
3 17°26′01.9”N 102°48′03.2″E Water gateway receiving flow from downtown areas, influenced by urban runoff 229 18 (7.9%) 2.7
4 17°26′59.4”N 102°48′50.8″E Rural community with agriculture, located 3.0 km downstream from the water gateway; situated at a river confluence where dark water was consistently observed during sampling 224 29 (12.9%) 3.6
5 17°28′04.1”N 102°51′50.6″E Rural agricultural community 15.2 km downstream from the water gateway, located at another confluence of rivers 217 36 (16.6%) 2.6
6 17°28′18.6”N 102°57′18.0″E Rural agricultural community 29.3 km downstream from the water gateway 232 10 (4.3%) 2.1
Total/Average 1377 117 (8.5%) 2.7
Open in a new tab

For the investigation of FBT metacercariae, a total of 1377 cyprinoid fish were captured, with at least 30 individuals collected per site using standardized gear such as gillnets, fish traps, and hand-casting nets to ensure adequate replication and minimize sampling bias. The sampled fish comprised three cyprinoid species commonly consumed in the study area: Cyclocheilichthys apogon (n = 562), Henicorhynchus siamensis (n = 559), and Barbonymus gonionotus (n = 256) (Supplementary Table 1). These species share overlapping ecological niches and similar habitat characteristics within irrigation canals, and have been frequently reported as intermediate hosts for O. viverrini metacercariae (Kaensa et al., 2025; Namboonrueng et al., 2024). Fish were stored on ice and transported to the laboratory for examination within 12 h.

For heavy-metal analysis, 117 cyprinoid fish infected with FBT metacercariae and 150 randomly selected uninfected fish were examined. At each of the six sites, all samples were collected simultaneously to allow direct comparison of heavy-metal contamination. Water, sediment, fish, and snail samples were collected in triplicate from three stations within each site during each monthly survey. In total, 126 water samples, 126 sediment samples, and 221 Bithynia snails were obtained. Water samples of 1000 mL were collected midstream at a depth of 20–30 cm in acid-washed polyethylene bottles, immediately acidified to pH < 2 with ultrapure nitric acid, and stored at 4 °C until analysis. Sediment samples were obtained using a stainless-steel grab sampler from three subsites at each location, homogenized, and stored in airtight containers to maintain sample integrity. Bithynia snails, the first intermediate host of fish-borne trematodes, were collected by handpicking and sieving aquatic vegetation and sediments to ensure adequate numbers for laboratory examination. Cercarial shedding was assessed by individually incubating live snails in dechlorinated water under natural daylight for 2 h and overnight, after which the water was examined under a stereomicroscope for emerging cercariae.

2.2. Investigation of FBTs metacercaria from cyprinoid fish

The 1377 cyprinoid fish were examined for metacercariae of FBTs using the standard pepsin digestion technique. Briefly, fish were homogenized and incubated in an artificial gastric solution containing 0.5% pepsin in 1.7% HCl at 37 °C for 2 h. The digested tissue was filtered through 300 μm and 180 μm meshes, repeatedly washed with 0.85% NaCl, and the resulting sediment was examined under a stereomicroscope. Metacercariae were identified based on morphology, including shape and sucker arrangement. The number of metacercariae/infected fish was recorded.

2.3. Heavy-metal analysis

Heavy metal concentrations (Cd, Cu, Zn, Pb, and Ni) were analyzed in 117 cyprinoid fish infected with fish-borne trematode metacercariae, 150 randomly selected uninfected fish, and associated samples of water, sediment, and Bithynia snails. Water samples were preserved with ultrapure nitric acid and stored at 4 °C until analysis. Solid samples were oven-dried (60 °C), homogenized, and digested using a nitric–perchloric acid mixture at 300 °C for 2 h, following established protocols for aquatic biological matrices (Khalefa et al., 2022; Atwah et al., 2025). Metal concentrations were quantified using a flame atomic absorption spectrometer (PinAAcle 900F, PerkinElmer, USA). Calibration curves exhibited excellent linearity (R2 > 0.995 for all metals). Analytical quality assurance included reagent blanks, duplicate analyses, and certified reference materials (AccuTrace™, AccuStandard Inc., USA), yielding recoveries of 92–106% and relative standard deviations below 5%. Limits of detection and quantification, calibration ranges, and additional quality-control parameters are summarized in Supplementary Table S2. All results were expressed in parts per million (ppm).

2.4. Bioaccumulation factor (BAF) calculation

Bioaccumulation factors (BAFs) for each heavy metal were calculated to assess the extent of accumulation in fish tissues relative to environmental concentrations. The BAF was computed using the formula described by Adolfsson-Erici et al. (Adolfsson-Erici et al., 2012):

BAF = Cfish/Cwater.

where Cfish is the concentration of a given heavy metal in fish tissue (ppm), and Cwater is the corresponding concentration in water (ppm). Separate BAF values were calculated for individual fish and presented as the average of all cyprinoid fish.

2.5. Data analysis

Descriptive statistics were used to summarize prevalence and infection intensity of FBT metacercaria in cyprinoid fish, and heavy metal concentrations. Data normality was assessed using the Kolmogorov–Smirnov test, and homogeneity of variance was evaluated prior to analysis. Where normality assumptions were violated, data were log-transformed before further statistical testing. Differences in mean metal concentrations between infected and uninfected fish were examined using Student's t-test. Pearson's correlation analysis was conducted to examine the relationship between heavy-metal concentrations in individual fish and FBT prevalence across sites. To control for multicollinearity and determine independent predictors of parasite burden, multivariable linear regression was applied using infection intensity as the dependent variable and the five metals (Ni, Cu, Cd, Zn, and Pb) as predictors. All statistical analyses were performed using SPSS version 23.0, with significance set at P < 0.05. Spatial distributions of Cd contamination in fish and metacercarial prevalence at each site were analyzed using ArcGIS Pro version 3.1.

3. Results

3.1. Prevalence and intensity of FBT infections

The prevalence and mean intensity of FBT metacercarial infections in cyprinoid fish are presented in Table 1. Among 1377 fish examined across six sites, 117 were infected, resulting in an overall prevalence of 8.5% and a mean intensity of 2.7 metacercariae/infected fish. Prevalence across sites ranged from 4.1% to 16.6%, while mean infection intensity ranged from 1.6 to 3.6 metacercariae/infected fish. Two trematode species were identified, O. viverrini and Haplorchis taichui, with H. taichui being the more common across sites. Comparisons among the three cyprinoid fish species examined (C. apogon, H. siamensis, and B. gonionotus) showed no significant differences in infection prevalence or heavy-metal concentrations (P > 0.05; Supplementary Table 1). In addition, no cercarial infections were detected in Bithynia snails examined using the cercarial shedding method.

3.2. Heavy-metal contamination in environmental and biological samples

Heavy-metal concentrations varied considerably across water, sediment, and biological samples collected from natural canals connected to the Huay Luang River (Table 2). Average Cd concentrations in water, which ranged up to 0.010 ppm (average 0.006 ppm), exceeded both the Thai (<0.005 ppm) and WHO (<0.003 ppm) safety thresholds. Heavy-metal analysis of tissues from the three fish species revealed substantial accumulation of, in particular, Zn (53.7 ± 29.8 ppm) and Cu (9.3 ± 6.3 ppm). Bithynia snails contained even higher concentrations of Zn (75.7 ± 35.8 ppm) and Cu (22.2 ± 14.4 ppm). Notably, Pb concentrations in waterbody sediment exceeded the Thai regulatory limit (5.2 ± 3.3 ppm).

Table 2.

Concentrations of heavy metals in water, cyprinoid fish tissue, Bithynia snail tissue, and canal sediments compared with regulatory reference limits.

Samples Metal Mean ± SD (ppm) Min–Max (ppm) Regulatory limit (ppm) Reference standard
Water (n = 126) Ni 0.034 ± 0.039 0.002–0.255 a ≤ 0.1 Thai PCD
Cu 0.025 ± 0.006 0.001–0.091 ≤ 0.1 Thai PCD
Cd 0.006 ± 0.002 a 0.002–0.010 a ≤ 0.005 Thai PCD
Zn 0.392 ± 0.200 0.061–0.846 ≤ 1.0 Thai PCD
Pb 0.019 ± 0.015 0.001–0.047 ≤ 0.05 Thai PCD
Cyprinoid fish tissue (n = 267) Ni 4.8 ± 2.2 1.4–9.4 Not specified –
Cu 9.3 ± 6.3 1.3–21.6 ≤ 30 FAO/WHO
Cd 1.4 ± 0.6 a 0.5–2.8 a ≤ 1.0 Thai MoPH
Zn 53.7 ± 29.8 14.8–160.4 a ≤ 100 FAO/WHO
Pb 9.0 ± 5.6 a 2.6–24.0 a ≤ 0.3 a FAO/WHO
Bithynia sp. Tissue (n = 221) Ni 6.4 ± 5.5 0.9–23.3 Not specified –
Cu 22.2 ± 14.4 6.4–82.3 Not specified –
Cd 1.9 ± 1.0 0.2–4.2 a ≤ 2.0 Thai MoPH
Zn 75.7 ± 35.8 24.6–171.1 Not specified –
Pb 9.8 ± 7.0 1.2–24.8 Not specified –
Canal sediment (n = 126) Ni 7.4 ± 6.7 1.37–36.9 a 22.7 WHO/Thai PCD
Cu 6.7 ± 4.6 0.1–18.9 31.5 WHO/Thai PCD
Cd 0.5 ± 0.3 0.1–1.6 a 1.0 WHO/Thai PCD
Zn 30.4 ± 16.9 4.4–81.7 120.0 WHO/Thai PCD
Pb 5.2 ± 3.3 a 1.0–15.1 a 35.8 WHO/Thai PCD
Open in a new tab

a = Values exceeding the corresponding regulatory guideline.

Regulatory reference limits are based on Thai Pollution Control Department (Thai PCD, 2015); FAO/WHO, 2011, FAO/WHO, 2019; Ministry of Public Health, Thailand (Thai MoPH, 2020).

Infected cyprinoid fish contained significantly higher concentrations of Cd (1.63 ± 0.71 ppm), Cu (11.06 ± 6.38 ppm), and Zn (68.51 ± 23.13 ppm) than uninfected specimens (1.23 ± 0.51 ppm, 8.00 ± 5.68 ppm, and 41.85 ± 16.70 ppm, respectively) (P ≤ 0.001 for all comparisons) (Table 3). No significant differences in metal concentrations were observed among the three cyprinoid species (Supplementary Table 1).

Table 3.

Heavy-metal concentrations in FBT-infected and uninfected cyprinoid fish.

Group n Ni (ppm) Cu (ppm) Cd (ppm) Zn (ppm) Pb (ppm)
Infected cyprinoid fish 117 5.53 ± 2.43 11.06 ± 6.38 1.63 ± 0.71 68.51 ± 23.13 8.13 ± 4.58
Un-infected cyprinoid fish 150 4.81 ± 1.81 8.00 ± 5.68 1.23 ± 0.51 41.85 ± 16.70 9.74 ± 5.53
All cyprinoid fish 267 4.84 ± 1.90 9.34 ± 6.18 1.41 ± 0.63 53.69 ± 23.84 9.03 ± 5.19
P-valuea 0.779 0.047 0.005 ≤0.001 0.692
Open in a new tab
a

= Independent t-test comparing infected and uninfected cyprinoid fish.

3.3. Correlation between heavy metals and the prevalence of metacercarial infection

Pearson correlation analysis revealed significant positive associations between the prevalence of FBT metacercariae in cyprinoid fish and the concentrations of Zn (r = 0.468, P = 0.002), Ni (r = 0.454, P = 0.003), Cu (r = 0.314, P = 0.043), and Cd (r = 0.367, P = 0.017) (Table 4). Pb concentration showed no significant relationship with metacercarial prevalence (r = 0.068, P = 0.669). These results indicate that elevated levels of several heavy metals are positively associated with infection prevalence in the study area.

Table 4.

Pearson correlation between heavy-metal concentrations and FBT metacercarial prevalence in cyprinoid fish, and multivariable regression analysis of heavy-metal concentrations in relation to infection intensity.

Heavy metal Pearson correlation (prevalence)
 Multivariable regression (intensity)
Correlation coefficient (r) P-value 95% CI Correlation coefficient (β) P-value 95% CI
Ni 0.454 0.003 0.16, 0.67 −1.19 <0.001 −1.50, −0.87
Cu 0.314 0.043 0.01, 0.57 −0.09 0.005 −0.15, −0.03
Cd 0.367 0.017 0.08, 0.64 5.36 <0.001 3.86, 6.86
Zn 0.468 0.002 0.18, 0.65 0.03 <0.001 0.02, 0.04
Pb −0.068 0.669 −0.30, 0.17 −0.09 <0.001 −012, −0.06
Open in a new tab

3.4. Multivariate and spatial analysis

Multivariate regression analysis revealed that metacercarial infection intensity in cyprinoid fish was strongly associated with heavy-metal contamination (Table 4). Cd emerged as the dominant predictor of parasite burden, with a one-ppm increase in Cd concentration corresponding to an average rise of 5.36 metacercariae/infected fish (P < 0.001). Zn also contributed significantly (β = 0.03, P < 0.001), although its effect was comparatively modest. By contrast, Ni (β = −1.19, P < 0.001), Cu (β = −0.09, P = 0.005), and Pb (β = −0.09, P < 0.001) appeared as negative predictors in the multivariable model. This apparent reversal reflects the strong multicollinearity among metals, particularly the very high correlations between Cd and Ni (r = 0.97) and Cd and Cu (r = 0.91). After controlling for the stronger drivers (Cd and Zn), the predictive influence of these co-occurring metals was masked.

Spatial mapping with ArcGIS identified three geographic sites (sampling sites 2, 4, and 6; Table 1) where elevated cadmium concentrations in cyprinoid fish coincided with high parasite intensity (Fig. 1). These overlapping patterns highlight Cd as the most influential contaminant driving metacercarial infections and demonstrate the geographic co-distribution of pollutants and parasite risk within the study area.

Fig. 1.

Fig. 1

Open in a new tab

GIS spatial analysis of cadmium contamination and prevalence of metacercarial infections in cyprinoid fish across sampling sites in Udon Thani Province, Thailand.

3.5. Bioaccumulation factor (BAF) in fish

Bioaccumulation analysis reinforced the link between metal exposure and FBT infection (Table 5). Infected fish showed consistently higher BAF values than uninfected counterparts: Cu 327.2 vs. 236.6 (ratio 1.4), Cd 296.0 vs. 223.9 (ratio 1.3), Zn 202.0 vs. 123.4 (ratio 1.6), and Ni 163.6 vs. 142.3 (ratio 1.1). In contrast, lead demonstrated a lower BAF in infected fish (437.2) compared with uninfected fish (523.5), ratio 0.8.

Table 5.

Bioaccumulation factors (BAF) in FBT-infected and uninfected fish

Heavy metals BAF
infected fish un-infected fish Ratio (infected/un-infected)
Ni 163.6 142.3 1.1
Cu 327.2 236.6 1.4
Cd 296.0 223.9 1.3
Zn 202.0 123.4 1.6
Pb 437.2 523.5 0.8
Open in a new tab

4. Discussion

This study provides the first field evidence from endemic northeastern Thailand confirming FBT metacercarial infections as a robust, integrated bioindicator for site-specific heavy metal contamination in freshwater cyprinoid fish. Sampling across six sites, chosen for their known links to community activities and environmental contamination (Namboonrueng et al., 2024), confirmed the endemic status of FBTs, particularly O. viverrini and H. taichui, with an overall prevalence of 8.5% and a mean intensity of 1.6–3.6 metacercariae/infected fish. Site-specific variation in prevalence reflected local differences in environmental conditions, particularly elevated cadmium concentrations in water. Sampling was conducted during the rainy season (May–November 2024), which showed no significant association with variations in metacercarial prevalence or heavy-metal or proximal human activities, as reported previously (Kaensa et al., 2025). The significant positive correlations observed between heavy metal concentrations—specifically cadmium, zinc, copper, and nickel—and both FBT prevalence and intensity are fundamental to these findings. Collectively, these results suggest that overall aquatic environmental quality, intensified by rainy season runoff, significantly influences parasite transmission dynamics.

Cadmium was established as the dominant ecological stressor. A 1-ppm increase in Cd concentration was associated with an average of 5.36 additional metacercariae/infected fish. This pattern suggests that cadmium may facilitate both initial and ongoing infection (Radwan et al., 2022; Sures et al., 2023). In addition, its concentration in water reached 0.010 ppm, exceeding both WHO and Thai PCD safety thresholds (≤0.005 ppm), a concerning finding given cadmium's well-documented toxicity to aquatic organisms and its long-term health risks in humans (Okereafor et al., 2020; Peng et al., 2023). Infected fish contained elevated levels of cadmium (1.63 ppm), copper (11.06 ppm), and zinc (68.51 ppm), consistent with experimental and field evidence that chronic metal exposure can impair growth and immune competence in fish through oxidative stress, endocrine disruption, and immunomodulatory effects (Brazova et al., 2015; Monteith and Skaar, 2021). Such metal-induced physiological stress may weaken host defenses, increasing susceptibility to parasite establishment, while simultaneously altering metabolic and detoxification pathways that influence metal uptake and retention. This imbalance in host immunity and metabolism provides a plausible explanation for the higher metal concentrations observed in infected individuals compared with uninfected counterparts (Sayyaf Dezfuli et al., 2023). In addition, heavy metals may indirectly shape trematode transmission by affecting the viability of free-living stages or modifying snail and fish host biology, thereby enhancing infection dynamics (Shah, 2005). The observed associations with nickel and copper further support a multifactorial interaction between metal contamination and host–parasite relationships in impacted freshwater environments.

Bioaccumulation factor analysis in this study offered further insight into the interplay between heavy metals and parasitic infection (Adolfsson-Erici et al., 2012). Infected fish had higher ratios than uninfected ones—1.3 for cadmium, 1.6 for zinc, and 1.4 for copper—suggesting greater metal accumulation or altered retention as a consequence of parasitism (Mehana et al., 2020; Moniruzzaman et al., 2023). This could be related to tissue damage from metacercarial encystment or parasite-induced metabolic changes that affect metal uptake and excretion (Eissa et al., 2025). Conversely, bioaccumulation may predispose fish to infection by impairing epithelial barriers and immune function, facilitating parasite establishment (Sayyaf Dezfuli et al., 2023). In contrast, lead showed no consistent association with infection, likely reflecting its strong binding to sediments and organic matter, low bioavailability, and relatively inefficient uptake in animal tissues (Lu and Xu, 2009; Pruter et al., 2018). Competitive interactions with cadmium and zinc may further limit Pb accumulation, obscuring any infection-related bioaccumulation pattern (Ferreira Fontes et al., 2000; Mahamadi and Nharingo, 2010). Elevated zinc and copper concentrations in Bithynia snails are noteworthy, as metal-induced stress can increase cercarial shedding or even cause snail mortality, thereby altering transmission rates (Morley et al., 2003; Radwan et al., 2020). However, no cercarial infections were detected in Bithynia snails in the present study, consistent with the generally low prevalence of infected snails reported in endemic settings (Rachprakhon and Purivirojkul, 2021). Copper, although an essential trace element in snails as a component of hemocyanin, has a narrow margin between physiological and toxic concentrations. Although copper is an essential trace element for snails as a component of hemocyanin, the threshold between physiological and toxic concentrations is narrow (Palacios et al., 2011). Bithynia snails efficiently accumulate metals from water, food, and sediment and mitigate excess exposure through metallothionein-mediated sequestration of cadmium and copper (Abdel-Halim et al., 2013). This strong metal-binding capacity reflects local contamination and supports the use of snails as bioindicators of environmental pollution, with indirect implications for parasite ecology in freshwater systems (Radwan et al., 2020). Taken together, snail metal burdens in this study indicate environmental exposure rather than active parasite transmission, complementing the fish-based evidence of contamination-driven host–parasite interactions.

Multivariate analysis demonstrated that heavy metals, particularly cadmium, are critical environmental factors influencing FBT metacercarial infections in cyprinoid fish. Cadmium was the strongest predictor of infection intensity, while zinc showed a smaller positive correlation (Brazova et al., 2015). Nickel, copper, and lead appeared as negative predictors due to multicollinearity, highly correlating with cadmium (Mikkonen et al., 2018). After the model accounted for the variance explained by cadmium, which emerged as the dominant and most influential predictor, the predictive influence of these co-occurring, highly correlated metals were statistically masked. Spatial mapping showed three sites, where high cadmium levels overlapped with high parasite intensity, underscoring localized contamination patterns. These results confirm that cadmium, largely derived from community nickel‑cadmium batteries (Khafaga et al., 2019), is the main driver of parasite transmission risk and is also a valuable ecological indicator (Mehana et al., 2020). Integrated surveillance targeting both heavy metal contamination and parasitic infections is necessary to safeguard ecosystem health and reduce human risk in endemic regions.

From a One Health perspective, the co-occurrence of bioaccumulated toxic metal residues and parasitic infections in commonly consumed fish presents a critical and complex public health concern (Okereafor et al., 2020). Chronic cadmium exposure, even at the low levels observed, is a concern due to its established associations to renal dysfunction, bone demineralization, and carcinogenesis (Khoshakhlagh et al., 2024). Recent systematic reviews report a significant association between cadmium exposure and increased susceptibility to liver disease as well as tumor development and progression in humans (Coradduzza et al., 2024; Zhang et al., 2025). Mechanistic studies further indicate that cadmium can promote hepatic inflammation, oxidative stress, and apoptosis, processes implicated in carcinogenic pathways (Men et al., 2021). In endemic settings, the co-exposure to cadmium and infection with the carcinogenic fish-borne trematode, O. viverrini may therefore plausibly contribute to an elevated risk of severe hepatobiliary disease and cholangiocarcinoma, although this relationship was not directly examined in the present study. The presence of heavy metals in fish thus reflets both environmental contamination and a direct pathway for human exposure through the food chain (Jamil Emon et al., 2023). Collectively, these findings illustrate how environmental pollution may exacerbates neglected tropical diseases through complex, interacting chemical and biological stressors, underscoring the need for integrated environmental and health surveillance (Charoensuk et al., 2024; Prakobwong et al., 2025). In endemic regions like northeastern Thailand, where raw or undercooked fish consumption remains common, coordinated interventions focusing on runoff control, risk communication, and cross-sectoral monitoring are essential to mitigate these overlapping chemical and biological hazards (Radwan et al., 2022).

This study was limited by its cross-sectional design and single-season sampling, which did not capture temporal variation in metal exposure or infection dynamics. As a cross-sectional study, we cannot establish temporal precedence or causality. Experimental studies exposing fish to controlled Cd levels and monitoring infection rates are needed to confirm causal mechanisms. The focus on a single province may limit generalizability to other endemic regions. Fish age could not be reliably determined because specimens were wild-caught, and although fish size was intentionally sampled within a narrow range to minimize variability, size- and age-structured analyses were not performed. In addition, physicochemical water quality parameters (e.g., pH, dissolved oxygen, temperature, turbidity, and suspended solids) were not assessed. These omissions are acknowledged as limitations and identified as priorities for future research.

5. Conclusions

This study provides integrated field evidence linking heavy-metal contamination to increased susceptibility of cyprinoid fish to trematode metacercarial infections in northeastern Thailand. Infected fish exhibited elevated concentrations of cadmium, copper, and zinc, with cadmium identified as the strongest predictor of infection intensity and bioaccumulation. Spatial analysis further revealed localized overlaps between high cadmium levels and FBT intensity, underscoring the ecological interaction between pollution and parasite transmission. These findings suggest that FBT metacercariae can serve as site-specific bioindicators of heavy-metal exposure and contamination risk. Integrated monitoring of chemical and biological hazards is therefore essential to protect freshwater ecosystems and reduce public health risks associated with fish-borne parasitic infections in endemic regions.

Declaration of generative AI in scientific writing

A generative artificial intelligence tool (ChatGPT; OpenAI, United States; GPT-5.2) was used during manuscript preparation for language editing only. The authors reviewed all AI-assisted content and are fully responsible for the final manuscript.

CRediT authorship contribution statement

Lakhanawan Charoensuk: Writing – review & editing, Writing – original draft, Visualization, Validation, Methodology, Investigation, Funding acquisition, Formal analysis, Data curation, Conceptualization. Chadon Nakmai: Writing – review & editing, Validation, Formal analysis, Data curation. Picha Suwannahitatorn: Writing – review & editing, Validation, Investigation, Formal analysis, Data curation, Conceptualization. Krissada Namboonrueng: Writing – review & editing, Validation, Investigation, Formal analysis, Data curation. Somchai Pinlaor: Writing – review & editing, Visualization, Validation, Funding acquisition, Conceptualization. Suksanti Prakobwong: Writing – review & editing, Writing – original draft, Visualization, Supervision, Project administration, Methodology, Investigation, Funding acquisition, Formal analysis, Conceptualization.

Ethical considerations

All animal procedures were approved by the Animal Ethics Committee of Udon Thani Rajabhat University (Approval No. AREC.UDRU.03/2024). The Institutional Review Board of the Faculty of Medicine, Vajira Hospital, exempted this study in accordance with international human research guidelines, including the Declaration of Helsinki, the Belmont Report, CIOMS, ICH-GCP, and 45 CFR 46.101(b) (Approval No. COE: 046/2025 X).

Funding

This work was supported by the Navamindradhiraj University research fund, Udon Thani Rajabhat University Research Fund and the Fundamental Fund of Khon Kaen University, which received funding from The National Science Research and Innovation Fund (NSRF), Thailand.

Declaration of competing interest

The authors confirm that there are no financial or personal relationships that could have inappropriately influenced the research presented in this manuscript.

Acknowledgements

We would like to acknowledge Prof. David Blair from the Reinventing University 2025 through Khon Kaen University, Thailand, for his comments and editing the manuscript.

Footnotes

Appendix A

Supplementary data to this article can be found online at https://doi.org/10.1016/j.fawpar.2026.e00321.

Appendix A. Supplementary data

Supplementary material 1 Species of cyprinoid fish and comparison of fish-borne trematode prevalence and heavy-metal concentrations among species

mmc1.docx (17.9KB, docx)

Supplementary material 2 Analytical performance parameters for heavy metal determination by flame AAS.

mmc2.docx (15.2KB, docx)

References

  1. Abdel-Halim K.Y., Abo El-Saad A.M., Talha M.M., Hussein A.A., Bakry N.M. Oxidative stress on land snail Helix aspersa as a sentinel organism for ecotoxicological effects of urban pollution with heavy metals. Chemosphere. 2013;93:1131–1138. doi: 10.1016/j.chemosphere.2013.06.042. [DOI] [PubMed] [Google Scholar]
  2. Adolfsson-Erici M., Akerman G., McLachlan M.S. Measuring bioconcentration factors in fish using exposure to multiple chemicals and internal benchmarking to correct for growth dilution. Environ. Toxicol. Chem. 2012;31:1853–1860. doi: 10.1002/etc.1897. [DOI] [PubMed] [Google Scholar]
  3. Atwah Mohamed A., Mohsen A.K., Abdelbaky Awad A., El Megeed Ola Hasan Abd, Aborasain Ali M., Salem Mai A., Soliman Mohamed A., Khalefa Hanan S., Abd-El Hanan H., Hafeez Mohamed Abdelsalam. Multifaceted analysis of cymothoids parasitism, environmental stressors and heavy metal bioaccumulation dynamics in mediterranean farmed fish in Egypt. Aquac. Int. 2025;33:1–24. [Google Scholar]
  4. Awasthi K.K., Yadav C.S., Sankhla M.S. The toxicity of everyday life: understanding the environmental risks to human health. Environ. Sci. Pollut. Res. Int. 2023;30:71897–71899. doi: 10.1007/s11356-023-27378-3. [DOI] [PubMed] [Google Scholar]
  5. Brazova T., Hanzelova V., Miklisova D., Salamun P., Vidal-Martinez V.M. Host-parasite relationships as determinants of heavy metal concentrations in perch (Perca fluviatilis) and its intestinal parasite infection. Ecotoxicol. Environ. Saf. 2015;122:551–556. doi: 10.1016/j.ecoenv.2015.09.032. [DOI] [PubMed] [Google Scholar]
  6. Charoensuk L., Chedtabud K., Chaipibool S., Laothong U., Suwannatrai A., Pinlaor S., Prakobwong S. Integrated one-health approach for prevention and control of Opisthorchis viverrini infection in rural Thailand: a 3-year study. Parasitol. Res. 2024;123:258. doi: 10.1007/s00436-024-08275-1. [DOI] [PubMed] [Google Scholar]
  7. Coradduzza D., Congiargiu A., Azara E., Mammani I.M.A., De Miglio M.R., Zinellu A., Carru C., Medici S. Heavy metals in biological samples of cancer patients: a systematic literature review. Biometals. 2024;37:803–817. doi: 10.1007/s10534-024-00583-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Eissa A.E., Mahdy O.A., Abouelhassan E.M., El Zlitne R.A., Mhara A.A., Al-Mokaddem A.K., Rashwan E.H., Ragab R.H., Younis N.A. Systemic infection of Prohemistomum vivax and Cyanodiplostomum encysted metacercariae in African catfish (Clarias gariepinus) from a heavily polluted drain at Giza, Egypt: morphological, molecular and histopathological study. Parasitol. Int. 2025;111 doi: 10.1016/j.parint.2025.103159. [DOI] [PubMed] [Google Scholar]
  9. El-Hak H.N.G., Ghobashy M.A., Mansour F.A., El-Shenawy N.S., El-Din M.I.S. Heavy metals and parasitological infection associated with oxidative stress and histopathological alteration in the Clarias gariepinus. Ecotoxicology. 2022;31:1096–1110. doi: 10.1007/s10646-022-02569-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. FAO/WHO . 2011. Joint FAO/WHO Food Standards Programme: Codex Alimentarius Commission—Maximum Levels for Contaminants in Foods. Rome (Ed.) [Google Scholar]
  11. FAO/WHO . WHO Press; 2019. Safety Evaluation of Certain Food Additives and Contaminants (JECFA) G. (Ed.) [Google Scholar]
  12. Ferreira Fontes M.P., de Matos A.T., da Costa L.M., Lima Neves J.C. Competitive adsorption of zinc, cadmium, copper, and lead in three highly-weathered Brazilian soils. Commun. Soil Sci. Plant Anal. 2000;31:2939–2958. doi: 10.1080/00103620009370640. [DOI] [Google Scholar]
  13. Jamil Emon F., Rohani M.F., Sumaiya N., Tuj Jannat M.F., Akter Y., Shahjahan M., Abdul Kari Z., Tahiluddin A.B., Goh K.W. Toxics. Vol. 11. 2023. Bioaccumulation and bioremediation of heavy metals in fishes-a review. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kaensa W., Charoensuk L., Nakmai C., Pinlaor S., Suwannatrai A.T., Laothong U., Prakobwong S. Distribution of Opisthorchis viverrini metacercariae and cyprinoid fish abundance in Nong Han wetland, Thailand. Parasite Epidemiol. Control. 2025;30 doi: 10.1016/j.parepi.2025.e00447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Khafaga A.F., Abd El-Hack M.E., Taha A.E., Elnesr S.S., Alagawany M. The potential modulatory role of herbal additives against Cd toxicity in human, animal, and poultry: a review. Environ. Sci. Pollut. Res. Int. 2019;26:4588–4604. doi: 10.1007/s11356-018-4037-0. [DOI] [PubMed] [Google Scholar]
  16. Khalefa Hanan S., Abdelsalam M.M.A. Mohamed, Mahmoud Mahmoud A., Ewiss M.A. Zaki. Immunological status of some edible fishes exposed to parasitic infections in relation to heavy metals pollution. J. Parasit. Dis. 2022;46:653–663. doi: 10.1007/s12639-022-01479-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Khoshakhlagh A.H., Mohammadzadeh M., Gruszecka-Kosowska A. The preventive and carcinogenic effect of metals on cancer: a systematic review. BMC Public Health. 2024;24:2079. doi: 10.1186/s12889-024-19585-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lu S.G., Xu Q.F. Competitive adsorption of Cd, Cu, Pb and Zn by different soils of eastern China. Environ. Geol. 2009;57:685–693. doi: 10.1007/S00254-008-1347-4. [DOI] [Google Scholar]
  19. Mahamadi C., Nharingo T. Competitive adsorption of Pb2+, Cd2+ and Zn2+ ions onto Eichhornia crassipes in binary and ternary systems. Bioresour. Technol. 2010;101:859–864. doi: 10.1016/j.biortech.2009.08.097. [DOI] [PubMed] [Google Scholar]
  20. Mehana E.E., Khafaga A.F., Elblehi S.S., Abd El-Hack M.E., Naiel M.A.E., Bin-Jumah M., Othman S.I., Allam A.A. Biomonitoring of heavy metal pollution using acanthocephalans parasite in ecosystem: an updated overview. Animals (Basel) 2020;10 doi: 10.3390/ani10050811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Men H., Young J.L., Zhou W., Zhang H., Wang X., Xu J., Lin Q., Tan Y., Zheng Y., Cai L. Early-life exposure to low-dose cadmium accelerates Diethylnitrosamine and diet-induced liver cancer. Oxidative Med. Cell. Longev. 2021;2021 doi: 10.1155/2021/1427787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mikkonen H.G., van de Graaff R., Clarke B.O., Dasika R., Wallis C.J., Reichman S.M. Geochemical indices and regression tree models for estimation of ambient background concentrations of copper, chromium, nickel and zinc in soil. Chemosphere. 2018;210:193–203. doi: 10.1016/j.chemosphere.2018.06.138. [DOI] [PubMed] [Google Scholar]
  23. Ministry of Public Health . Royal Thai Government Gazette; Thailand: 2020. Notification No. 414 B.E. 2563: Maximum Levels of Contaminants in Foods. [Google Scholar]
  24. Moniruzzaman M., Datta U., Saha N.C., Bhowmick A.R., Mukherjee J. Abiotic factors and heavy metals defining eco-physiological niche in fish. Sci. Total Environ. 2023;874 doi: 10.1016/j.scitotenv.2023.162328. [DOI] [PubMed] [Google Scholar]
  25. Monteith A.J., Skaar E.P. The impact of metal availability on immune function during infection. Trends Endocrinol. Metab. 2021;32:916–928. doi: 10.1016/j.tem.2021.08.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Morley N.J., Irwin S.W., Lewis J.W. Pollution toxicity to the transmission of larval digeneans through their molluscan hosts. Parasitology. 2003;126(Suppl):S5–26. doi: 10.1017/s0031182003003755. [DOI] [PubMed] [Google Scholar]
  27. Namboonrueng K., Charoensuk L., Pinlaor S., Laothong U., Suttiprapa S., Suwannatrai A.T., Prakobwong S. Environmental contamination of Opisthorchis viverrini eggs and its impact on transmission control in rural Northeast Thailand. Infect. Dis. (Lond.). 2024:1–10. doi: 10.1080/23744235.2024.2443010. [DOI] [PubMed] [Google Scholar]
  28. Nguyen T.T.B., Dermauw V., Bui D.T., Dahma H., Le D.T., Nguyen H.T.T., Do D.T., Dorny P., Losson B., Vandenberg O. Incidence of fish-borne trematode infections and associated factors: results from a cohort study in highly endemic communities in northern Vietnam. Parasitol. Res. 2023;122:1415–1425. doi: 10.1007/s00436-023-07846-y. [DOI] [PubMed] [Google Scholar]
  29. Okereafor U., Makhatha M., Mekuto L., Uche-Okereafor N., Sebola T., Mavumengwana V. Toxic metal implications on agricultural soils, plants, animals, aquatic life and human health. Int. J. Environ. Res. Public Health. 2020;17 doi: 10.3390/ijerph17072204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Oros A. Bioaccumulation and trophic transfer of heavy metals in marine fish: ecological and ecosystem-level impacts. J. Xenobiot. 2025;15 doi: 10.3390/jox15020059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Palacios O., Pagani A., Perez-Rafael S., Egg M., Hockner M., Brandstatter A., Capdevila M., Atrian S., Dallinger R. Shaping mechanisms of metal specificity in a family of metazoan metallothioneins: evolutionary differentiation of mollusc metallothioneins. BMC Biol. 2011;9:4. doi: 10.1186/1741-7007-9-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Peng C.Y., Ren C., Shen H.X., Wang Y.F., Duan H.J., Wang Y.L., Li X.H., Liu D.X., Ma J.H. Soil heavy metal contamination, sources, and health risk of typical drinking water sources in the suspended reach of the lower Yellow River. Huan Jing Ke Xue. 2023;44:6710–6719. doi: 10.13227/j.hjkx.202211271. [DOI] [PubMed] [Google Scholar]
  33. Phitaktim S., Wangka-orm C., Wesetsri S., Togari T., Sato S., M W. Assessment of surface water quality of Huai Luang River in Udon Thani, Thailand, using the water quality index. Int. J. Environ. Sci. Dev. 2023;14 [Google Scholar]
  34. Pollution Control Department . Ministry of Natural Resources and Environment; Bangkok: 2015. Sediment Quality Guidelines for Surface Water Bodies in Thailand. [Google Scholar]
  35. Prakobwong S., Charoensuk L., Chaipibool S., Chedtabud K., Laothong U., Suwannatrai A.T., Blair D., Pinlaor S. One health integrated strategies for sustainable control of Opisthorchis viverrini infections in rural endemic areas of Thailand. Infect. Dis. Poverty. 2025;14:42. doi: 10.1186/s40249-025-01315-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Pruter H., Franz M., Auls S., Czirjak G.A., Greben O., Greenwood A.D., Lisitsyna O., Syrota Y., Sitko J., Krone O. Chronic lead intoxication decreases intestinal helminth species richness and infection intensity in mallards (Anas platyrhynchos) Sci. Total Environ. 2018;644:151–160. doi: 10.1016/j.scitotenv.2018.06.297. [DOI] [PubMed] [Google Scholar]
  37. Rachprakhon P., Purivirojkul W. Very low prevalence of Opisthorchis viverrini s.l. cercariae in Bithynia siamensis siamensis snails from the canal network system in the Bangkok metropolitan region, Thailand. Parasite. 2021;28:2. doi: 10.1051/parasite/2020072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Radwan M.A., El-Gendy K.S., Gad A.F. Biomarker responses in terrestrial gastropods exposed to pollutants: a comprehensive review. Chemosphere. 2020;257 doi: 10.1016/j.chemosphere.2020.127218. [DOI] [PubMed] [Google Scholar]
  39. Radwan M., Abbas M.M., Afifi M.M., Mohammadein A., Al Malki S.J. Fish parasites and heavy metals relationship in wild and cultivated fish as potential health risk assessment in Egypt. Front. Environ. Sci. 2022;10 doi: 10.3389/fenvs.2022.890039. [DOI] [Google Scholar]
  40. Saijuntha W., Andrews R.H., Sithithaworn P., Petney T.N. Opisthorchis viverrini life cycle, distribution, systematics, and population genetics. Recent Results Cancer Res. 2023;219:7–25. doi: 10.1007/978-3-031-35166-2_2. [DOI] [PubMed] [Google Scholar]
  41. Sayyaf Dezfuli B., Lorenzoni M., Carosi A., Giari L., Bosi G. Teleost innate immunity, an intricate game between immune cells and parasites of fish organs: who wins, who loses. Front. Immunol. 2023;14 doi: 10.3389/fimmu.2023.1250835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Shah S.A.A. Alterations in the immunological parameters of tench (Tinca tinca L. 1758) after acute and chronic exposure to lethal and sublethal treatments with mercury, cadmium and lead. Turk. J. Vet. Anim. Sci. 2005;29:1163–1168. [Google Scholar]
  43. Sripa B., Suwannatrai A.T., Sayasone S., Do D.T., Khieu V., Yang Y. Current status of human liver fluke infections in the greater Mekong subregion. Acta Trop. 2021;224 doi: 10.1016/j.actatropica.2021.106133. [DOI] [PubMed] [Google Scholar]
  44. Sures B. Environmental parasitology. Interactions between parasites and pollutants in the aquatic environment. Parasite. 2008;15:434–438. doi: 10.1051/parasite/2008153434. [DOI] [PubMed] [Google Scholar]
  45. Sures B., Jurges G., Taraschewski H. Relative concentrations of heavy metals in the parasites Ascaris suum (Nematoda) and Fasciola hepatica (Digenea) and their respective porcine and bovine definitive hosts. Int. J. Parasitol. 1998;28:1173–1178. doi: 10.1016/s0020-7519(98)00105-2. [DOI] [PubMed] [Google Scholar]
  46. Sures B., Nachev M., Schwelm J., Grabner D., Selbach C. Environmental parasitology: stressor effects on aquatic parasites. Trends Parasitol. 2023;39:461–474. doi: 10.1016/j.pt.2023.03.005. [DOI] [PubMed] [Google Scholar]
  47. Taslima K., Al-Emran M., Rahman M.S., Hasan J., Ferdous Z., Rohani M.F., Shahjahan M. Impacts of heavy metals on early development, growth and reproduction of fish - a review. Toxicol. Rep. 2022;9:858–868. doi: 10.1016/j.toxrep.2022.04.013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Zhang H., Jing Y., Guan L., Luo J., Zeng M. The association between cadmium exposure and the risk of early liver disease: a systematic review and meta-analysis. Regul. Toxicol. Pharmacol. 2025;163 doi: 10.1016/j.yrtph.2025.105942. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary material 1 Species of cyprinoid fish and comparison of fish-borne trematode prevalence and heavy-metal concentrations among species

mmc1.docx (17.9KB, docx)

Supplementary material 2 Analytical performance parameters for heavy metal determination by flame AAS.

mmc2.docx (15.2KB, docx)

Articles from Food and Waterborne Parasitology are provided here courtesy of Elsevier

RESOURCES