Introduction

Seafood, such as marine fish, crustaceans, bivalves, and algae, is a rich source of protein, vitamins, minerals, and polyunsaturated fatty acids. It forms a crucial part of many dietary patterns in the world1,2,3 and can help prevent chronic diseases, improve glycemic control, enhance the immune system, and sustain proper brain function in humans4. Several dietary recommendations recommend at least two servings of fish and seafood per week to gain essential nutrients, promote neurodevelopment in children, and prevent coronary heart disease2. Despite the significant health benefits, seafood consumption can also lead to health problems due to the presence of toxic metals and persistent organic pollutants (POPs)5.

Metals are typically categorized as essential, probably essential, and non-essential. Copper (Cu), zinc(Zn), iron (Fe), and selenium (Se) are nutritionally crucial elements that play a significant role in human metabolism. Although nickel (Ni) and vanadium (V) are not essential to human health, they may be beneficial at low exposure levels. Arsenic (As), mercury (Hg), chromium (Cr), cadmium (Cd), and lead (Pb) have no nutritional value at low concentrations and may be harmful. Furthermore, both essential and probably essential elements can cause toxic effects at high concentrations5,6,7.

Studies have shown various degrees of heavy metal pollution in the seafood from many coastal areas due to rapid industrialization and urbanization8. Trace metals in aquatic environments can accumulate in marine organisms and be transferred to humans via the food chain9. Many coastal marine environments in China have been affected by metal contamination, which is influenced by environmental conditions, pollution sources, and economic development10. Heavy metals, such as As, Cd, Cr, and Pb from natural and anthropogenic sources may continuously enter marine environments in recent years11. Since heavy metals are non-biodegradable and persistent contaminants in the aquatic environment, they can easily accumulate in marine organisms12. These heavy metals are transferred to humans upon consumption, posing severe health hazards by adversely affecting the brain, the central nervous system, the cardiovascular system, the kidneys, the reproductive system, and the immune system13. Besides non-cancerous effects, certain metals (e.g., As, Cd, Pb, and Hg) also cause mutations, teratogenic effects, and carcinogenic outcomes in living organisms14. The health risk of heavy metals contamination is a growing global concern, and various studies have focused on human exposure due to contaminated seafood consumption15,16.

The consumption of heavy metals can have both carcinogenic and non-carcinogenic impacts on human health. In order to assess the potential health hazards linked to prolonged ingestion of chemical contaminants in food, the United States Environmental Protection Agency (USEPA) has devised the Target Hazard Quotient (THQ) and Combined THQ (CTHQ) for quantitative evaluation. Carcinogenic metals are associated with cancer slope factors (CSF) to estimate lifetime target cancer risks (TR). A THQ below 1 generally poses no obvious risk to humans, while a value equal to or greater than 1 indicates a potential health risk. Previous studies have confirmed the validity of these methods in assessing the risk to human health17,18,19. This study applies these techniques to estimate the health risks associated with seafood consumption. Analyzing the concentrations of multiple heavy metals in different seafood species and comprehending their ecological implications are crucial for safeguarding marine ecosystems.

Located on the mainland of southern China, Hainan Island is the second largest island in the country. Hainan Island is well-suited for tropical marine fisheries due to its rich aquatic resources, extensive fishing grounds, diverse species, rapid growth, and lengthy fishing season. Previous studies have shown that As, Pb, Cd, Cu, and Cr concentrations were 10.3 mg/kg dw, 23 mg/kg dw, 0.1 mg/kg dw, 25 mg/kg dw, and 140 mg/kg dw, respectively in coastal sediments20. The popularity of Hainan as a tourist destination has gradually increased since the construction of the Hainan International Tourism Island and Hainan Free Trade Port. Haikou, located at the northernmost tip of Hainan Island, is the capital city of Hainan Province and offers an abundance of marine products. Haikou's industrial economy has experienced steady growth in recent years. Haikou's seafood is not only consumed locally but also distributed to other provinces within China and exported to international markets21. Variations in heavy metal concentrations may be attributed to factors such as habitat differences, seasonal changes, dietary habits, and trophic levels of marine organisms15,22. The geographical location of the area is situated within the tropics and is characterized by tropical monsoon climate with warm winter, long summer, and high precipitation. The growth of Hainan International Tourism Island and coastal tourism in Haikou has led to population concentration and resource depletion, causing increased pollution in Haikou Bay23. Previous studies have evaluated the metal concentrations daily consumption (DC) and potential health risks only about fish in Haikou24,25. However, our research is comprehensive, incorporating crustaceans, bivalves, and algae. Crustaceans and bivalves were more likely to accumulating heavy metals, which live in the lower areas of the habitat (i.e., sediment). At present, The levels of heavy metals in crustaceans, bivalves, and algae in this area have not been reported in the past decade. Therefore, the toxic heavy metal (As, Cd, Cr, and Pb) content in different kinds of four commonly consumed seafood (fish, crustaceans, bivalve and alga) from Haikou markets were compared, and the possible health risks associated with dietary heavy metal exposure were evaluated. The results could help understand the current situation regarding heavy metals pollution and aid the development of targeted response measures to preserve marine ecosystems and protect public health.

Materials and methods

Sampling and preparation

One hundred and twenty-six samples of twenty-three mostly consumed seafood species, divided into four groups (fish, crustacean, bivalve, and alga), were randomly collected from 6 markets located in the four district of Haikou city. Immediately after the collection, clean plastic bags were used to transport all samples to the lab, kept in an airtight insulating box with ice bags. These samples were washed with tap water first and then deionized water to remove adhesive materials before dissection. To make further use of the samples, only edible parts were collected with ceramic knives, homogenized, and placed in polyethylene bottles at − 20 °C.

Sample digestion and elements analysis

Samples of 0.200–1.000 g were transferred to digestion vessels with 5 mL HNO3 (ultra-pure grade; Suzhou Crystal Clear Chemical Co. Ltd, Suzhou, China) and placed in a vapor block for 0.5 h predigestion at 100 ℃. The samples were digested using a Multiwave PRO microwave (Anton Paar, Graz, Austria). The temperature was increased to 100 ℃ for 10 min, after which it was maintained at 170 ℃ for 20 min. Then, the temperature was increased to 180 ℃ for 5 min, which was maintained for 60 min, followed by cooling to 60 ℃ or lower. The samples were removed from the microwave and placed in a vapor block for 120 min at 160 ℃ to remove the acids from the digests. The vessels were cooled to room temperature after digestion. The digested solution was diluted to 25 mL with ultrapure water obtained via a water purification system (Medium-Q300, Hitech Instruments CO., Ltd, Shanghai, China) and subjected to inductively coupled plasma-mass spectrometry (ICP-MS) (PE NexION300, PerkinElmer, Waltham, Mass, USA). The ICP-MS conditions included an (radio frequency) RF power of 1300 W, a pump rate of 20 rpm, and plasma, nebulizer, and auxiliary argon flow rates of 16.00 L/min, 0.99 L/min, and 1.20 L/min, respectively. The multi-element standard stock solution (GNM-M25748-2013, 1000 mg/L) was obtained from the National Center for Analysis and Testing of Nonferrous Metals and Electronic Materials (Beijing, China). The elemental concentrations were measured using external calibration solutions corrected for internal standard response factors. The concentrations of trace metals were expressed as mg/kg wet weight (ww).

Quality assurance and control

The certified reference materials, including prawns (GBW10050) and scallops (GBW10024), were purchased from the Chinese Academy of Geological Sciences (Lang fang), Institute of Geophysical and Geochemical Exploration, and used for quality control. Blank trials were run in parallel.

Health risk assessment

The target hazard quotient (THQ), combined target hazard quotient (CTHQ), and target cancer risk (TR) were used to evaluate the health risk of seafood consumption by Haikou inhabitants (Formulas (1)–(3))26:

$$THQ = \frac{EF \times ED \times C \times DC}{{RfD \times BW \times AT}}$$
(1)

THQ indicates the non-carcinogenic hazard quotients of the metals in the selected seafood, EF denotes the exposure frequency (365 days/year), ED is the exposure duration (77.4 years, assumed as the average life expectancy of Hainan people)27, C is the concentration of each metal in individual seafood samples (mg/kg, ww), and DC is the average daily consumption of aquatic products by the urban residents in Haikou, Hainan province, China (68.8 × 10–3 kg/day 25.10 kg/365)21. RfD is the inorganic As (InAs), Cd, Cr, and Pb oral reference dose for the non-carcinogenic effect (3 × 10–4, 1 × 10–3, 3 × 10–3, and 3.5 × 10–3 mg/kg body weight/day, respectively), using values from the Integrated Risk Information System (IRIS) of the United States Environmental Protection Agency (USEPA)28, except for Pb29. BW is the average adult body weight of the population in Hainan Province, China (54.0 kg)30, and AT is the average exposure time for non-carcinogens or carcinogens (365 days/year for EF, namely EF × ED)26,31. If the THQ value > 1, the daily exposure of the targeted toxicant at the present level likely produced a deleterious effect over a lifetime. Conversely, if the THQ value ˂ 1, the substance was assumed to have no obvious risks during a person's lifetime32.

$$CTHQ = THQ_{InAs} + THQ_{Cd} + THQ_{Cr} + THQ_{Pb}$$
(2)

The combined target hazard quotient (CTHQ) evaluates the combined non-carcinogenic risk of the four selected metals in each seafood species.

$$TR = \frac{EF \times ED \times C \times DC \times CSF}{{BW \times AT}}$$
(3)

Target cancer risk (TR) is expressed as the carcinogenic risk of each heavy metal via the consumption of different kinds of seafood, and CSF is the carcinogenic slope factor of InAs, Cd, Cr, and Pb regarding the carcinogenic effect (1.5, 6.3, 0.5, and 0.0085 (mg/kg body weight/day)−1, respectively)29,33. The following cancer risk levels were determined according to the TR values: TR ≤ 1 × 10–6 very low (level I), 1 × 10–6 ˂ TR ≤ 1 × 10–4 low (level II), 1 × 10–4 ˂ TR ≤ 1 × 10–3 moderate (level III), 1 × 10–3 ˂ TR ≤ 0.1 high (level IV), and TR > 0.1 very high risk (level V). Cancer risk was considered acceptable for developing cancer at levels I and II, and unacceptable at levels III to V over a lifetime34.

Results and discussion

Heavy metal concentrations

Table 1 shows the As, Cd, Cr, and Pb concentrations in the various seafood species. Based on 126 marine organisms, the median metal concentrations were As > Cd > Cr > Pb, which were similar to the results of previous studies35. The heavy metal concentrations observed in the examined species included As at 0.41–27.05 mg/kg ww (Fig. 1), Cd at ND (not detected) to 4.79 mg/kg ww (Fig. 2), Cr at ND to 0.86 mg/kg ww (Fig. 3), and Pb, ND to 0.63 mg/kg ww (Fig. 4). These results suggested that the metal concentrations varied with the metal type and organism species. Moreover, the seafood products in Haikou City displayed considerable As and Cd contamination, while Cr and Pb presented low levels in all the selected seafood samples. Previous studies have shown severe As and Cd enrichment factors in the Hainan river sediments, followed by Cr and Pb. This indicates the significant impact of human activity in recent years36. As the river discharged into the sea, the heavy metals present in the river sediments would contaminate the sea water, leading to an elevation in the concentration of heavy metals in the marine environment. Notably, a previous study indicated the presence of As (0.53–20.94 mg/kg ww) and Cd (ND-9.64 mg/kg ww) in seafood from sanmen bay35. The Cr concentration in this study was consistent with research conducted by Zhao et al.32 in Xiamen, China, while the Pb concentration range was similar with Liu35. Milenkovic et al.37 reported high Pb concentrations in sea fish (0.1–6.56 mg/kg ww) and shrimp (0.25–1.13 mg/kg ww) from Serbian markets. We found that the median metal concentrations were As > Cd > Cr > Pb in this study, the results of this research is inconsistent with Feng et al.25. Additionally, Cadmium was present in all four types of aquatic products in our study, however, Liu et al.38 reported that cadmium was not detected in fishes. To examine the differences between the four seafood groups egarding heavy metal accumulation, a Kruskal–Wallis Test was used to compare the heavy metal concentration distribution in fish, crustaceans, bivalves, and algae. The results revealed significant differences (P < 0.05) between the metal groups in the different seafood species. The crustaceans displayed the highest As and Cd concentrations. The As bioaccumulation could mostly be ascribed to human activities, such as industrial effluents, agricultural fertilizer39, and intensive cultivation both in greenhouses and outdoors40. Due to volcanic cone and lava cover on the north and south banks of the Qiong Zhou Strait, the naturally occurring As and Cd may be related to the settlement of atmospheric particulate matter caused by rock weathering41,42. Crustaceans, as scavengers and omnivores, typically inhabit the benthic regions of lakes and seas, where they are able to accumulate trace elements from detritus and the food chain43,44. Simultaneously, the head of crustaceans accumulates trace elements due to its multiple internal organs45.Furthermore, crustaceans are benthic organisms whose legs are usually buried, stirring up the surficial sediment where they reside, possibly leading to higher metal absorption46,47. The Cr and Pb concentrations were highest in the bivalve mollusks, which feed on the water they filter while maintaining a sedentary lifestyle48, allowing them to easily absorb toxic heavy metals. Bivalvesalso live in sediment and can actively assimilate heavy metals via filter feeding on organic and inorganic particles47,49. Metals mainly assimilate in fish via the ingestion of suspended particulate matter, ion exchange across lipophilic membranes during breathing, and via the food chain50, possibly explaining why their tissues contain lower heavy metal levels than bivalves and crustaceans.

Table 1 The arsenic (As), cadmium (Cd), chromium (Cr), and lead (Pb) (mg/kg ww) concentrations in the seafood purchased from Haikou markets.
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Fig. 1
figure 1

The range of median As in the four seafood species.

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Fig. 2
figure 2

The range of median Cd in the four seafood species.

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Fig. 3
figure 3

The range of median Cr in the four seafood species.

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Fig. 4
figure 4

The range of median Pb in the four seafood species.

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The targeted metal concentrations were compared against the legal limits established by the China Food and Drug Administration (CFDA) (2017) and European Commission (EC) (2006) to assess the seafood quality. A total As concentration was detected in this study. Yet the forms of As in food are usually different, with organic As reportedly less toxic than InAs and is estimated as 10% of the total As32,51. Therefore, the InAs concentration for 58.0% of the fish species and 59.1% of the crustaceans exceeded the safety limits set by the CFDA standards52 (0.1 mg/kg for fish, 0.5 mg/kg for crustaceans). Furthermore, 31.8% of the crustacean samples and 28.2% of the bivalve samples displayed higher Cd concentrations than the CFDA standards (0.5 mg/kg for crustaceans, 2.0 mg/kg for bivalves), while the Cd concentrations surpassing the EC limitation53 (0.05 mg/kg for fish, 0.5 mg/kg for crustaceans, 1.0 mg/kg for bivalves) in the fish, crustacean, and bivalve samples were 2.0%, 31.8%, and 33.3%, respectively. Previous studies have also reported high standard-exceeding Cd and As concentration rates of seafood products separately from the Tuscany coast located in northern Italy and Shenzhen, China54,55. The Cr and Pb levels in all the targeted seafood samples were below the Chinese and the EC standard guideline values.

Besides environmental conditions, pollution sources, and economic development that were mentioned in this study, the health risk of seafood consumption around the City of Haikou may also be affected by potential factors such as local biotic interactions and time-lagged abiotic conditions. Some scholars have suggested that some examples of novel and promising approaches that have been used for tracking these potential factors, such as further source apportionment studies using environmental forensics tools. Identifying the sources of anthropogenic heavy metals that contribute to their accumulation at any given site is a key step in developing successful emission control strategies and targeting contaminated sites for remediation. Heavy metal stable isotopes (e.g. Copper, Lithium, and Zinc) have been increasingly used for this purpose56,57,58,59.

Health risk assessment based on the THQ and TR

Target hazard quotient (THQ)

To define the potential health risks, it is necessary to integrate the toxicity and concentration information for every pollutant. Table 2 summarizes the THQ and CTHQ of the four metals in the different seafood species. The THQ values of Cr and Pb were below 1 in all the samples, indicating no related risk to local residents when consuming the tested seafood species. The toxicological profile of As only focused on inorganic chemical species due to the relative non-toxicity of organic As compounds60,61. The THQ values of InAs and Cd ranged from 0.18–11.49 and ND-6.1, respectively. Six seafood species displayed median InAs THQ values greater than 1, comprising fish (reddish fish), crustaceans (Mantis Shrimp, Orchid Crab, and Redspot Swimming Crab), bivalves (Scallops), and algae (Sea Lettuce). Median Cd THQ values above 1 were only found in the bivalve species, including scallops, fan shells, and oysters. Although calculating the THQ index does not provide a quantitative estimate of the dangers associated with an exposed population, this methodology provided preliminary information on the potential health risks of consuming different marine organisms. The results suggested that the inhabitants might be exposed to health risks by ingesting InAs and Cd via the consumption of the species mentioned above.

Table 2 The target hazard quotient (THQ) and combined target hazard quotient (CTHQ) values of the arsenic (As), cadmium (Cd), chromium (Cr), and lead (Pb) in 23 seafood species and their non-carcinogenic effect on Haikou residents.
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Humans are often exposed to more than one pollutant at a time, which can lead to additive and interactive effects62. As shown in Table 2, the CTHQ values of several seafood species exceeded 1, including one fish species (Reddish Fish), three crustacean species (Mantis Shrimp, Orchid Crab, and Redspot Swimming Crab), four bivalve species (Razor clams, Scallops, Fan shells, and Oysters), and one algal species (Sea Lettuce), suggesting that consumption induced non-carcinogenic effects. Therefore, consumption of local seafood may adversely affect the health of local residents, especially crustacean and bivalve species, since their close relationship with polluted bottom sediment may promote the bioaccumulation of hazardous materials.

Target cancer risk (TR)

As shown in Table 3, the TR values of InAs, Cd, Cr, and Pb ranged from 7.9E−05 to 5.2E−03, ND to 3.8E−02, ND to 5.5E−04, and ND to 6.9E−06, respectively. The median TR values of InAs in all the species exceeded 1 × 10–4, indicating that InAs posed an extremely high carcinogenic risk to those consuming the 23 seafood species examined in this study, which was consistent with previous studies63. According to the International Agency for Research on Cancer, InAs and its compounds are group I carcinogens64. Exposure to InAs has been associated with multiple health consequences, including coronary heart disease (CHD) and lung, bladder, and skin cancer65.

Table 3 The target cancer risk (TR) values of the arsenic (As), cadmium (Cd), chromium (Cr), and lead (Pb) in 23 seafood species and their carcinogenic effect on Haikou residents.
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The median TR of Cd in all the bivalve and algal species, as well as three crustacean species (Mantis Shrimp, Orchid Crab, and Redspot Swimming Crab), were significantly higher than the acceptable levels, while these values were below 1 × 10–4 in all the fish species, except for Japanese Scad and Pacific Saury. The Cr levels in five bivalve species (Razor Clams, White Clams, Fan Shells, Oysters, and Blood Clams) presented a level III cancer risk. The results also suggested that Cd posed a high cancer risk to local residents upon consumption of these seafood species. Several epidemiological studies have shown a link between the Cd exposure level and breast cancer66. Conversely, the carcinogenic risk presented by Pb via seafood consumption were all at levels I and II. This means that it was acceptable for human over their lifetime.

It is imperative to monitor these metals in seafood from Haikou. Furthermore, previous researches has shown that humans can also be exposed to toxic metals through other food sources such as rice, vegetables, fruit, and water67,68,69. The potential risk to human health from heavy metals depends on the total exposure to these chemical compounds. Therefore, The authorities concerned should be strengthen management, such as rational control of pollutant discharges from the production sector, regular monitoring of metal concentrations, reduction of environmental pollution in rivers and enhanced awareness-raising for factory managers. However, this study was limited by the fact that sampling was not possible at the sites for objective reasons and subsequent studies could be further improved with adequate funding or other conditions.

Conclusions

This study shown that coastal residents in the City of Haikou were critically exposed to heavy metals via seafood consumption. The results indicated that the As and Cd levels in various fish, crustacean, and bivalve samples exceed the Chinese national standards and EC limits. Nine types of seafood pose a non-carcinogenic risk whether InAs and Cd are ingested alone or in combination with the other two target metals (Cr and Pb). The cancer risk assessment results of InAs indicated a carcinogenic risk in all the species, Cd in all the bivalve and algal species and several crustacean (Mantis Shrimp, Orchid Crab, Redspot Swimming Crab) and fish species (Japanese Scad, Pacific Saury), and Cr in most bivalve species (Razor Clams, White Clams, Fan Shells, Oysters, Blood Clams). To prevent excessive heavy metal ingestion that can negatively impact public health, considering that other species of exposure risks are not included in this study, the overall risk of metal exposure could be even higher. Therefore, future research should consider the practical assessment of metal exposure risk to seafood consumers in coastal areas.