Persistent organic pollutants (POPs) important to human health include polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs), polychlorinated biphenyls (PCBs) including both dioxin-like PCBs (DL-PCBs) and non–dioxin-like PCBs, organochlorine pesticides (OCPs), and polybrominated diphenyl ethers (PBDEs). A previous review comprehensively considered the persistence, long-range atmospheric transport, bioaccumulation in biota, food-web biomagnifications, and adverse effects upon human and ecosystem health as the main reasons why PCDD/Fs, PCBs, and OCPs attracted considerable attention worldwide 1. The four major endpoints of toxicological concern for these compounds include endocrine disruption in humans and wildlife 2–5, reproductive and developmental toxicity 6, central nervous system effects 7, 8, and damage to the immune system of top-predator species 9. These chemicals are typically hydrophobic and lipophilic, so they are readily sequestered in adipose tissue and are bioaccumulated/biomagnified into higher trophic levels in the food web. It is well accepted that dietary intake is the major route for human exposure to these chemicals, compared to other routes such as inhalation and dermal contact 10–13.
Numerous researchers have shown that human dietary exposure to POPs is largely attributable to consumption of aquatic products 13–17. It is likewise well established that eating aquatic products also offers many nutritional benefits. Fish and shellfish provide high-quality protein and other essential nutrients, are low in saturated fat, and are a highly recommended dietary source for omega-3 fatty acids. Because of this high nutritional value, fish and shellfish have thus become an important part of a healthy diet worldwide 18. Given the dietary importance and widespread popularity of aquatic products, we have attempted here to conduct preliminary estimates of daily dietary intakes of the four typical pollutant groups through consumption of aquatic products. In addition, to assess human health risk from the four pollutant groups, we compare these estimated daily intake rates for aquatic consumption with various applicable standards, limits, or similar health advisories set by different organizations or countries worldwide. It should be noted that the range of aquatic products targeted in the current review includes marine and freshwater fish and shellfish, and species will be specified wherever appropriate throughout the review.
Data related to the concentrations of these four typical pollutant groups in aquatic products from major aquaculture countries were collected from the following world regions: Africa—Egypt and Tanzania; North and South America—Brazil, Canada, Chile, and the United States; Asia—China, India, Indonesia, Japan, South Korea, and Vietnam; Europe—Belgium, Denmark, Norway, Spain, Sweden, and Switzerland; and Oceania—Australia (Sydney). Wherever possible, data were obtained preferentially from the most recent available literature (published after 2000). Information and statistics regarding consumption rates for aquatic products from different world regions were obtained from the database compiled and maintained by the United Nations Food and Agriculture Organization (FAO; http://faostat.fao.org/site/610/default.aspx#ancor). The estimated daily intake (EDI) for PCDD/Fs and DL-PCBs is calculated as EDI (pg toxic equivalent [TEQ]/kg body weight [bw]/d), and is based upon aquatic consumption (g/d) · contaminant concentration (pg TEQ/g)/bw (60 kg for Asian consumers and 70 kg for European, African, and American consumers). The EDI for PCBs, OCPs, and PBDEs is calculated as EDI (ng/kg bw/d), and is based upon aquatic product consumption (g/d) · contaminant concentration (ng/g)/bw (60 kg for Asian consumers and 70 kg for European, African, and American consumers), of which contaminant concentrations were primarily derived from 50th and 90th percentile concentrations, and utilizing mean concentrations whenever median values were not available (Supplemental Data, Tables S1–S5). Data comparison among groups was done using nonparametric tests (Kruskal–Wallis H and Mann–Whitney U) with statistical significance p < 0.05 under SPSS version 13.0.
Several guidelines have been established by different international organizations to assess POPs intake risk for human health. These include the World Health Organization (WHO)-specified tolerable daily intakes for dioxins plus dioxin-like PCBs of 1–4 pg World Health Organization toxic equivalent (WHO-TEQ)/kg bw/d 5; the European Commission, Health and Consumer Protection Scientific Committee on Food has recommended a tolerable weekly intake for dioxins plus dioxin-like PCBs of 14 pg WHO-TEQ/kg bw/week (2 pg WHO-TEQ/kg bw/d) 19; the Korea Food and Drug Administration has proposed a tolerable daily intake of 4 pg WHO-TEQ/kg bw/d for dioxins plus dioxin-like compounds 20; the United Kingdom Committee on Toxicity of Chemicals in Food, Consumer Products and the Environment has proposed a tolerable daily intake of 2 pg WHO-TEQ/kg bw/d 20; and the Joint FAO/WHO Expert Committee on Food Additives has recommended a tolerable monthly intake of 70 pg WHO-TEQ/kg bw/month (2.33 pg WHO-TEQ/kg bw/d) 21. Regarding regulations for intake of PCBs and OCPs, Health Canada has recommended a tolerable intake level of 1,000 ng/kg bw/d for PCBs 22. For residues in edible commodities, the U.S. Food and Drug Administration developed the action levels of 2,000 ng/g wet weight for PCBs (23; www.epa.gov/ost/fishadvice/volume2/index.html). China has established a maximum residue level for DDTs (500 ng/g wet weight) and HCHs (100 ng/g wet weight) (24; http://down.foodmate.net/standard/sort/3/5949.html). The European Union has established a maximum admissible concentration of 50 ng/g wet weight for DDTs, 25 ng/g wet weight for lindane, 10 ng/g wet weight for hexachlorobenzene (HCB), and 10 ng/g wet weight for other HCH isomers 25. The FAO/WHO has recommended acceptable daily intakes and provisional tolerable daily intakes of 1.0 × 104 ng/kg bw/d and 5,000 ng/kg bw/d for DDTs and HCHs, respectively (26; http://www.who.int/ipcs/publications/jmpr/jmpr_pesticide/en/index.html). The U.S. Environmental Protection Agency has developed screening values (SVs) for contaminants such as PCBs, OCPs, and PBDEs. These are defined as concentrations of targeted analytes in fish and shellfish tissue which can be used as threshold values to evaluate possible risk associated with consumption of contaminated fish or seafood and to indicate that more intensive investigation should be conducted 27, 28. The following equations are used to calculate SVs:
Hazard ratios (HRs) are calculated by dividing the average daily exposure (EDI) by the screening values. A ratio greater than unity indicates that the average daily exposure level exceeds the SVs 29. With respect to PBDEs, although several authors have recently published toxicity data for PBDEs 30–33, applicable risk assessment guidelines and regulations for PBDEs are thus far quite limited. In the United States, the Agency for Toxic Substances and Disease Registry (ATSDR) has derived a minimal risk level of 3.0 × 104 ng/kg bw/d for acute-duration oral exposure and 7,000 ng/kg bw/d for intermediate-duration oral exposure to lower brominated phenyl ethers (BDEs), respectively. The ATSDR has also derived a minimal risk level of 1.0 × 107 ng/kg bw/d for intermediate-duration oral exposure to BDE-209 based on a no observable adverse effect level of 1.0 × 109 ng/kg bw/d for developmental toxicity in rats exposed to BDE-209 for 19 d during gestation (http://www.atsdr.cdc.gov/mrls/index.html#bookmark02). Darnerud et al. have recommended a lowest observed adverse effect level of 1.0 = 106 ng/kg bw/d, based on the most sensitive endpoints of toxic effects of PBDEs 34, 35.
RESULTS AND DISCUSSION
Concentration levels of all the contaminants varied among different regions and different types of aquatic products (Fig. 1). Generally, levels of dioxins in marine fish, mollusks, crustaceans, and freshwater fish from Europe, and freshwater fish from America, were higher than those in other regions. Marine fish from Asia and Europe, and freshwater fish from America, contained higher loadings of PCBs and OCPs; marine fish and freshwater fish from America, Europe, and Asia showed higher levels of PBDEs. Detailed concentration data are given in Supplemental Data, Tables S1–S5. Some distribution patterns associated with individual pollutant groups are described below.
The highest level of dioxins was found in Saginaw Bay, Michigan, USA. It was reported that this particular region received many organic and inorganic materials from industrial releases, as well as urban and agricultural runoff and domestic sewage. Contaminants such as PCDDs, PCDFs, and PCBs in the Saginaw Bay area have been shown to induce adverse environmental effects on local people and wildlife 36. These results are in general agreement with previously reported findings of Wagrowski and Hites 37. Marine fish samples from Frierfjorden, Norway also contained very high levels of PCDD/Fs. In a situation somewhat similar to the industrial contamination at Saginaw Bay, the Hydro Porsgrunn factory in Frierfjorden, Norway discharged wastes containing high levels of PCDD/PCDFs. It was estimated that the total amount of TEQPCDD/Fs flowing into Frierfjorden was about 56 to 107 kg from 1951 to 1990 38, 39. As a result, aquatic product consumption among local residents had been constrained by PCDF/PCDD contamination 39.
The highest PCB level was found in freshwater fish samples from four river basins located in the southeastern United States, where industrial discharge from chemical manufacturing plants, military facilities, pulp and paper mills, coal-fired power plants, urban and agriculture runoff, mine drainage, and municipal wastewater effluents had inevitably resulted in deterioration of the environment around the four river basins 40. Furthermore, high levels of PCBs were also found in the livers of bluefin tuna collected from coastal waters of Japan. Japan consumes more tuna than any other country, about a quarter of the total annual world tuna fishery resource (http://www.jsof.gov.cn/art/2008/8/27/art_128_29752.html). Bluefin tuna farming was first developed in Japan in the 1970s 41. These circumstances of species preference and extensive tuna diet make it worthwhile to focus further on contaminants in bluefin in Japan, together with potential health risks from excessive human consumption. In similar fashion, Ueno et al. 42 reported that high PCB concentrations were detected in livers of skipjack tuna collected from offshore waters around Japan. The concentration levels of PCBs in aquatic products collected from China were quite low compared with those from other countries (Supplemental Data, Table S3), which is in line with the fact that the amounts of PCBs manufactured and used in China were relatively minor. It was reported that China produced only 8,000 tons of PCBs (0.6% of the total global production) during the1960s and 1970s 43–44. The United States consumed the largest quantity of PCBs (46% of the total global consumption), followed by Russia (7.9%), Germany (7.1%), Japan (4.1%), France (4.1%), and Canada (3.1%), which consistently corresponds to the residual levels of PCBs in aquatic products from these countries (Supplemental Data, Table S3). In contrast, the highest PBDE level was found in freshwater fish samples from Lake Mjøsa in Norway, probably due to the release of PBDEs into the water from a textile manufacturer in the town of Lillehammer 45. Globally, the levels of OCPs in mussel samples collected from the coast of the Egyptian Red Sea were significantly higher than those from other regions, which may be attributed to the use of large amounts of OCPs in this region 46. It is also important to note that relatively lower OCP residual levels typically seen in biota samples from some tropical regions, such as India and some African countries, do not necessarily equate with less usage of OCPs in these regions. Rather, there are indications that perhaps higher temperatures in these countries facilitate more rapid volatilization and higher elimination rates in biota 47, 48.
Generally, all the contaminants in marine fish and freshwater fish were more abundant than those in the other three types of aquatic species, including cephalopods, crustaceans, and mollusks, except mollusk samples from China and Egypt (Fig. 1), probably because of fish being at higher trophic levels and having higher lipid contents than other aquatic species. The levels of the contaminants under investigation were also different in developed and developing countries. Figure 2 shows that the levels of dioxins (sum of PCDD/Fs and DL-PCBs), PCBs, PBDEs, and OCPs were higher in industrialized countries than those in less industrialized regions due to their special status as by-products in industrial processes involving incineration, chlorine bleaching of paper and pulp, and the manufacture of some pesticides, herbicides, and fungicides 49, or large amounts of usage in industrial production. This tendency has been further confirmed by global pollution monitoring studies of PCDD/Fs and DL-PCBs, in which comparatively higher levels of these contaminants have been detected in highly industrialized countries around the East and South China Seas such as Japan, Korea, Taiwan, Hong Kong, and coastal China 42. By comparison, OCPs, because of their widespread applications in agriculture and sanitation, exhibited certain spatial distributional patterns. For example, in some developing countries such as India, China, and Egypt, large amounts of technical hexachlorocyclohexanes (HCHs) have been used for these purposes 50. Certain OCPs, such as HCHs, are more liable to undergo atmospheric transport due to their higher values of Henry's Law constant and vapor pressure.
On the whole, the levels of contaminants in aquatic products are influenced by numerous factors, such as the nature of the environments being sampled, the types of aquatic products being investigated, and the different characteristics and usage patterns of the pollutants being sought. Except for some situations that are heavily influenced by the existence of point-source pollution, levels of these persistent pollutants in aquatic products tend to show a positive correlation with usage amount in each country or continent. For example, the levels of PCDD/Fs, PCBs, and PBDEs were higher in aquatic products from industrialized countries than those from less industrialized countries. Regarding OCPs, some developing countries had also used large amounts of them; however, some more volatile OCP constituents, such as HCBs and HCHs, are readily distilled to colder regions, resulting in lower than expected levels in aquatic products from tropical regions.
The estimated dietary intake based on median concentrations (EDI50) for people from different regions was highly variable in different types of aquatic products (Fig. 3 and Supplemental Data, Tables S7–S11). Compared with the global distribution of concentration levels of pollutants in aquatic products, the EDI of pollutants for global populations showed some similarities, e.g., EDI50 through marine fish and freshwater fish were relatively higher than those through other types of aquatic products. Pollutant intake via cephalopods for Japanese, mollusks for Chinese, and crustaceans for Norwegian consumers were also very high (Fig. 3). The definition of EDI suggests that EDI depends not only on pollutant concentration in aquatic products but also on consumption of different species of aquatic products for people in each region. As shown in Figure 4, the correlation coefficients between EDI50 and pollutant concentrations in aquatic products and between EDI50 and fish consumption varied widely for different pollutants. For example, the concentrations of OCPs and PCBs in marine fish and concentrations of PCBs and PBDEs in freshwater fish were decisive factors in determining pollutant intake for global populations (p < 0.01 for EDI50 vs concentration and p > 0.01 for EDI50 vs consumption). In contrast, both the concentrations and consumption levels of OCPs in freshwater fish, dioxins in marine and freshwater fish, and PBDEs in marine fish were equally important in determining their intakes for people (p < 0.01 for both EDI50 vs concentration and consumption).
The EDI50 values of DL-PCBs and PCDD/Fs through consumption of marine fish and crustaceans collected from Frierfjorden, Norway were much higher than those from other regions. As discussed above, this region had very significant point-source pollution from PCDDs, PCDFs, and PCBs, which has resulted in recommendations that people should limit their consumption of fish 36. Consumption of marine fish and crustaceans by Norwegian people is at the high end of the global range (Supplemental Data, Table S6). Similarly, the highest exposure level for PCBs was found in Japan's consumers via marine fish collected from Japanese coastal waters, which was also due to high PCB concentrations and large marine fish consumption for the Japanese population 51. Among all species of aquatic products, PBDE intake through marine and freshwater fish for global populations was much higher, which can be ascribed to higher marine and freshwater consumption rates on a global scale. According to statistics data by the FAO of the United Nations, the total production of marine fish and freshwater fish in 2007 amounted to 6.76 × 107 and 4.06 × 107 tons, accounting for 48 and 29%, respectively, of total aquaculture production. The highest PBDE intake was, for Norwegians, via consumption of freshwater fish collected from Lake Mjøsa, Norway, which was also attributed to point-source pollution. Because China has the largest fishery production in the world and a long history of OCP usage, the Chinese population is exposed to the highest level of OCPs through consuming mollusks.
Figure 5 shows the EDI50 values for all the target analytes and aquatic products on the continent level. As discussed above, the daily intake correlated with both the concentrations of POPs and consumption rates of aquatic products. Generally, Europeans uptake more dioxins than people in other continents (Fig. 5). Asians and Americans are exposed to higher levels of PCBs and OCPs via aquatic product consumption than other populations (Fig. 5). It is noteworthy that the uptake levels of PBDEs are all extremely low for all global consumers compared with those of other pollutants, which was previously attributed to the possibility that large portions of PBDEs used as ingredients of brominated fire retardants may have remained in currently used and/or disposed commercial products 52. African people, in general, uptake very small amounts of POPs through aquatic products probably because they consume small quantities of aquatic products and the loadings of POPs are low in Africa. It should be noted that intakes of the sum of PBDEs, PCBs, and OCP via marine fish, cephalopods, mollusks, crustaceans, and freshwater fish account for 55.8, 13.6, 7.4, 0.8, and 22.4%, respectively, of the total intake (Fig. 6), indicating that consumption of marine fish is the predominant route of human exposure to these contaminants.
Compared with the criteria for DL-PCBs and PCDD/Fs, EDI50 and EDI90 (except intakes via mollusks for people in France) for dioxins in all types of aquatic products except marine fish were lower than 4 pg WHO-TEQ/kg bw/d. Due to high residues of dioxins and high consumption of marine fish, human exposure to dioxins via marine fish was higher than that through other aquatic products. The EDII50 and EDI90 of dioxin intakes via marine fish were in the range of 0.07 to 12.8 and 0.13 to 43.8 pg WHO-TEQ/kg bw/d, with mean values of 2.6 and 9.1 pg WHO-TEQ/kg bw/d, respectively. Furthermore, 53% of EDI90 were higher than 4 pg WHO-TEQ/kg bw/d. Exposure to PCDD/Fs and DL-PCBs through aquatic products, excluding marine fish, for most people in the world is in the range of levels lower than 4 pg WHO-TEQ/kg bw/d. Nevertheless, dioxin intakes via marine fish should be taken seriously especially for people in Norway and France. As for OCPs and PCBs, the non-cancer hazard ratio (HRn) and cancer hazard ratio (HRc) based on the 50th and 90th percentile concentrations of OCPs (except HRc based on the 90th percentile concentration (1.5) for Chinese people via freshwater fish) were much lower than one, indicating minimum risk from exposure to OCPs through aquatic products. Additionally, the levels of DDTs and HCHs in most samples, except bivalves collected from Egypt, were all lower than the limits set by the Chinese government (600 ng/g wet weight) and FAO/WHO (15,000 ng/kg bw/d) for the sum of DDTs and HCHs. Additionally, 4.2 and 40% of the samples studied had levels lower than the European Union limit (85 ng/g wet weight) based on the 50th and 90th percentile concentrations, respectively. However, the mean values of the HRn and HRc for PCBs were 0.68 and 1.3 from the 50th percentile concentration, and 2.7 and 5.2 from the 90th percentile concentration, indicating that there is some cancer risk for humans due to PCBs intake through consumption of aquatic products (Fig. 7). However, if marine fish were excluded from the assessment, the mean values of HRn (50th percentile: 0.05; 90th percentile: 0.19) and HRc (50th percentile: 0.20, 90th percentile: 0.77) were lower than one, suggesting that higher hazard risk was derived from marine fish compared with other types of aquatic products. In contrast, the levels of PCBs were far below the limits of 1,000 ng/kg bw/d set by Health Canada and the maximum level of 2,000 ng/g wet weight set by the U.S. Food and Drug Administration. The HRn values for PBDEs were all several orders of magnitude lower than one, and the estimated daily intakes of PBDEs compiled herein were all much lower than the limits described above, including minimal risk level for acute-duration oral exposure (3.0 × 104 ng/kg bw/d), intermediate-duration oral exposure to lower brominated phenyl ethers (BDEs) (7,000 ng/kg bw/d), and intermediate-duration oral exposure to deca BDE (1.0 × 107 ng/kg bw/d) developed by the ATSDR, and the lowest observed adverse effect level (1.0 × 106 ng/kg bw/d) recommended by Darnerud et al. (Supplemental Data, Table S10). In all, health risk is minimal for PBDEs intake via aquatic consumption based on the current regulations and guidelines.
Generally speaking, risk derived from dioxins, OCPs, and PBDEs through consumption of aquatic products (excluding marine fish for dioxins) is in the acceptable level against existing criteria. In contrast, risk derived from dioxins through consumption of marine fish is relatively higher and may cause hazard to consumers, especially to people in Norway and France. Polychlorinated biphenyls might pose threats to human health via aquatic products, particularly marine fish consumption, based on cancer and noncancer hazard ratio assessment. The health risk assessment based on concentration levels and consumption data from each country is not definitive because concentration data were limited and consumption data were largely out of date. Furthermore, numerous guidelines and regulations related to human health risk assessments, which are somewhat variable, have been set by different organizations and governments. Therefore, the assessment results based these criteria are mostly qualitative and intended to provide general trends only.
Total amount of PHCs in global aquatic products
The total amounts of persistent halogenated compounds (PHCs), sum of PCBs, OCPs, and PBDEs annually accumulated in global aquatic products were estimated based on the 50th and 90th percentile concentrations compiled in this review, and the total fishery production data of 2007 in each continent, available at http://www.fao.org/fishery/statistics/software/fishstat/en (Supplemental Data, Table S12). The total amounts accumulated in global aquatic products are 2.1 and 5.6 tons/year for PCBs, 0.21 and 0.96 tons/year for PBDEs, and 4.7 and 12.8 tons/year for OCPs, based on the 50th and 90th percentile concentrations, respectively. Therefore, the amounts of PHCs accumulated in global aquatic products were 7.0 and 19.4 tons/year from the 50th and 90th percentile concentrations. The amounts of PHCs in aquatic products from Asia, America, Europe, Africa, and Oceania account for 75.3, 14.5, 7.6, 2.4, and 0.15% of the global total based on the 50th percentile concentration. It is interesting to note that the total global amount of PBDEs used in 2001 alone was approximately 67,390 tons 53, and the amounts of PCBs and sum of DDTs and HCHs used were 1,200,000 and 16,800,000 tons, respectively 54, 55, indicating that the amount of PHCs stored in aquatic products appears to be an extremely small fraction of the total present in the environment. Other environmental media or even commercial products, such as electronics and furniture, may contain vast amounts of PHCs. For example, electronic waste still holds the majority of PBDEs ever produced 56.
Generally, the levels of dioxins, PCBs, OCPs, and PBDEs in aquatic products are somewhat consistent with the amounts of these compounds used in each country or continent. As by-products in industrial processes or industrial chemicals, PCDD/Fs, DL-PCBs, PCBs, and PBDEs were all quite abundant in aquatic products from industrialized countries such as Norway, Spain, the United States, and Canada. With respect to OCPs, because they have been used abundantly in agriculture and sanitation in some developing countries such as China, India, and Egypt, levels of OCPs were also considerably high in aquatic products from developing countries. Estimated daily intakes of PCDD/Fs, DL-PCBs, OCPs, and PBDEs for global residents through consumption of aquatic products (excluding marine fish for dioxins) are in the acceptable range against existing regulations and guidelines, with the following descending magnitude of exposure: first, Europeans > Asians > Americans > Oceanians > Africans for the sum of PCDD/Fs and DL-PCBs; second, Asians > Americans > Europeans > Oceanians > Africans for OCPs; and third, Americans > Europeans > Asians for PBDEs. In contrast, dietary intake of PCBs through aquatic product consumption, especially via marine fish, appears to be at sufficiently high levels to cause cancer risk for global consumers, with the exposure levels following the order of Asians > Europeans > Americans > Oceanians. It should be noted that although the levels of PCBs and OCPs in recent years have shown a declining trend in the general environment 57–60, obvious fresh inputs exist in some regions around the world 40, 51, 61–65, which merits greater awareness and attention. Furthermore, we suggest that all countries should strive, on a more global scale, to better harmonize their various regulations and guidelines for these ubiquitous pollutants, in order to allow the development of more comprehensive and accurate risk assessment models, as well as dietary exposure pathways, for protecting public health.
Table S1. Levels of PCDD/Fs.
Table S2. Levels of DL-PCBs.
Table S3. Levels of PCBs.
Table S4. Levels of PBDEs.
Table S5. Levels of OCPs.
Table S6. Consumption of aquatic products for global consumers.
Table S7. Estimated daily intake of PCDD/Fs.
Table S8. Estimated daily intake of DL-PCBs.
Table S9. Estimated daily intake and cancer and noncancer hazard ratio for PCBs.
Table S10. Estimated daily intake and non-cancer hazard ratio for PBDEs.
Table S11. Estimated daily intake and cancer and noncancer hazard ratio for OCPs.
Table S12. The total amounts of dioxins, PCBs, OCPs, and PBDEs stored in global aquatic products. (338 KB DOC)
Financial support for the present study was provided by the National Natural Science Foundation of China (40821003, U0633005, and 40588001). Thanks also go to Michael Watson for his input to, and technical editing of, the manuscript. This is contribution IS-1239 from GIGCAS.