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Mercury (Hg) concentration in fish commercialized in the São Luís fish market (MA) and potential exposure of consumers

Abstract

Fish consumption is the main path of human exposure to Hg and may represent a risk to public health, even with low Hg concentrations in fish, if consumption rates are high. This study quantifies, for the first time, the Hg concentrations in nine most commercialized species in the São Luís (MA) fish market, where fish consumption is high, and estimates human exposure. Average Hg concentrations were highest in carnivorous species, yellow hake (Cynoscion acoupa) (0.296 mg kg-1), the Atlantic croaker (Micropogonias undulatus) (0.263 mg kg-1), whereas lowest concentrations were recorded in iliophagous Mullets (Mugil curema) (0.021 mg kg-1) and the Shorthead drum Larimus breviceps (0.025 mg kg-1). Significant correlations were observed between Hg concentrations and fish length in two species: the Coco-Sea catfish (Bagre bagre) and the Atlantic bumper (Chloroscombrus crysurus), but not in the other species, since they presented relatively uniform size of individuals and/or a small number of samples. Risk coefficients, despite the relatively low Hg concentrations, suggest that consumers should limit their consumption of Yellow hake and Atlantic croaker, as they can present some risk to human health (EDI > RfD and THQ > 1), depending on the frequency of their consumption and the consumer’s body weight.

Key words
Contamination; fish; human exposure; risk assessment

INTRODUCTION

Health and well-being result from the interactions of different determining factors of social, economic, cultural and political nature, but mostly on environmental health, including access to sanitation and exposure to pollutants. A systemic and inter-sectorial approach to environmental and social impacts is required to grasp the causal relationships between pollutant exposure and their effects on human health. This approach breaks with the classical model aimed at an understanding of the health-disease process proper (Netto et al. 2006NETTO GF, CARNEIRO FF & ARAGÃO LGT. 2006. Saúde e Ambiente: reflexões para um novo ciclo do SUS. In: CASTRO A & MAL M. SUS - Ressignificando a Promoção da Saúde. São Paulo: HUCITEC/OPAS, pp. 152-157., Gurgel et al. 2009GURGEL AM, MEDEIROS ACLV, ALVES PC, SILVA JM, GURGEL IGD & AUGUSTO LGS. 2009. Framework dos cenários de risco no complexo da implantação de uma refinaria de petróleo em Pernambuco. Ciên Saúde Colet 14: 2027-2038., Barbosa et al. 2011BARBOSA SCT, COSTA MF, BARLETTA M, DANTAS DV, KEHRING HA & MALM O. 2011. Total mercury in the fish Trichiuru slepturus from a tropical estuary in relation to length, weight, and season. Neotrop Ictiol 9: 183-190.).

A relevant issue to be addressed in this new approach is the finding that the concentration of metals and organic substances has increased considerably due to a combination of anthropogenic releases from urban wastes and industrial and mining effluents (Santos et al. 2019SANTOS TTL, MARINS RV & SILVA DIAS FJ. 2019. Carbon influence on metal distribution in sediment of Amazonian macrotidal estuaries of northeastern Brazil. Environ Monit Assess 191: 552. https://doi.org/10.1007/s10661-019-7626-6.
https://doi.org/10.1007/s10661-019-7626-...
) and the remobilization of the deposited pollutants accumulated during the past century, the so-called “legacy of contamination”. Among these pollutants, Hg stands out as being of significant environmental importance due to its ubiquity and toxicity. The mobility, bioavailability and consequently toxicity of this Hg legacy will depend not only on the bulk quantity of the pollutant released, but on the effect of environmental changes, which are highly influence changes in physical-chemical and microbiological conditions of aquatic ecosystems, resulting from direct human interventions (e.g. eutrophication) or indirectly as a response to global climate change (Lacerda et al. 2020LACERDA LD, MARINS RV & DIAS FJS. 2020. An Arctic Paradox: Response of fluvial Hg inputs and its bioavailability to global climate change in an extreme coastal environment. Front Earth Sci 8: 93. https://doi.org/10.3389/feart.2020.00093.
https://doi.org/10.3389/feart.2020.00093...
).

Consumption of fish and shellfish is the main pathway of Hg and its highly toxic methyl-Hg to humans (BCS 2007BCS. 2007. Human health risk assessment of mercury in fish and health benefits of fish consumption. Bureau of Chemical Safety, Food Directorate, Health Products and Food Branch, 76p. Ontario. http://hc-sc.gc.ca/fn-an/pubs/mercur/merc_fish_ poisson_e.html. Assessed on 21 November 2022.
http://hc-sc.gc.ca/fn-an/pubs/mercur/mer...
, Barbosa & Dorea 1998BARBOSA AC & DOREA JG. 1998. Indices of mercury contamination during breast feeding in the Amazon Basin. Environ Toxicol Pharmacol 6: 71-79., Castilho et al. 1998, Vieira et al. 2013VIEIRA SM, ALMEIDA R, HOLANDA IBB, MUSSY MH, GALVÃO RCF, CRISPIM PTB, DÓREA JG & BASTOS WR. 2013. Total and methyl-mercury in hair and milk of mothers living in the city of Porto Velho and in villages along the Rio Madeira, Amazon, Brazil. Intern J Hyg Environ Health 216: 682-689., 2015). In addition, fish is the basis of the livelihood of riverine populations of many areas in the world, a fact which consequently expose them to high levels of Methyl-Hg associated with fish consumption (Oliveira et al. 2010OLIVEIRA RC, DOREA JG, BERNARDI JV, BASTOS WR, ALMEIDA R & MANZATTO AG. 2010. Fish consumption by traditional subsistence villagers of the Rio Madeira (Amazon): impact on hair mercury. Ann Human Biol 37: 629-642.).

São Marcos Bay (Supplementary Material Figure S1), where the second largest harbor complex in Latin America is located, and its adjacent continental shelf supply a diversified fluvial and estuarine fish to humans. Large pelagic and small schooling species from coastal waters, support moderate-to high commercial and artisan fisheries that are of substantial economic value, as well as a significant portion of the local diet of local consumers. Fish and shellfish respond to 69% of the total protein consumption of the local population, from which 85% corresponds to fishes, 52% of consumers eat fish 2-3 times per week and average week consumption varies from 1 to 2 kg, average of 0.142 kg day-1 in this high consumption group (Silva et al. 2012SILVA IA, LIMA MFV, BRANDÃO VM, DIAS ICL, SILVA MI & LACERDA LM. 2012. Perfil de consumidores do pescado comercializado em mercados do Município De São Luís, Maranhão, Brasil. Cad Pesq 19: 59-63.). Therefore, Hg concentrations in these fisheries raise awareness about the health of this estuarine-marine ecosystem and eventual human exposure. Mercury accumulates in tissues of aquatic organisms and can be biomagnified through the food chain and may attain concentrations that are potentially harmful to human health (Doney 2010DONEY SC. 2010. The growing human footprint on coastal and open-ocean biogeochemistry. Science 328: 1512-1516., Bisi et al. 2012BISI TL, LEPOINT G, AZEVEDO AF, DORNELES PR, FLACH L, DAS K, MALM O & LAILSON-BRITO J. 2012. Trophic relationships and mercury biomagnification in Brazilian tropical coastal food webs. Ecol Indicators 18: 291-302.). Recent studies on trace metal concentrations in São Marcos Bay, reported mobilization of metals associated with environmental changes (Santos et al. 2019SANTOS TTL, MARINS RV & SILVA DIAS FJ. 2019. Carbon influence on metal distribution in sediment of Amazonian macrotidal estuaries of northeastern Brazil. Environ Monit Assess 191: 552. https://doi.org/10.1007/s10661-019-7626-6.
https://doi.org/10.1007/s10661-019-7626-...
), suggesting an increase in their bioavailability and bioaccumulation, probably explaining previously reported high concentrations in the Bay’s local biota (Carvalho et al. 2000CARVALHO GP, CAVALCANTE PRS, CASTRO ACL & ROJAS MOAI. 2000. Preliminary assessment of heavy metal levels in Mytella falcata (Klappenbach, 1965, Bivalvia, Mytilidae) from Bacanga River Estuary. Rev Bras Biol 60: 11-16., Rojas et al. 2014ROJAS MOAI, CAVALCANTE PRS, SOUZA RC & DOURADO ECS. 2014. Teores de zinco e cobre em ostra (Crassostrea rhizophorae) e sururu (Mytella falcata) do estuário do rio Bacanga em São Luís (MA). Bol Lab Hidrobiol 2014: 20-27.).

Taking these previous results into consideration, this study emphasizes the concentration of Hg in commercialized fish in the São Luis fish market, which is still unreported, notwithstanding the large proportion of fish on the local population’s diet. The observed concentrations of Hg in commercialized fish associated with answers of a questionnaire applied to local consumers on their food habits, were used to assess Hg exposure risk to humans due to fish consumption using different risk indexes.

MATERIALS AND METHODS

One hundred and twenty-five individuals (125) of the nine (9) fish species were selected from the most frequent items sold in the São Luis fish market and the local consumer’s diet, based on questionnaires (n = 574) completed by local consumers between 2017 and 2019. The questionnaires consisted of questions about individual weight of consumer, number of fish meals per week and the preferred fish species. Taxonomic identification, trophic status and diet of the selected species were obtained from FishBase (2022)FISHBASE. 2022. http://www.fishbase.org. Assessed on 21 November 2022.
http://www.fishbase.org...
. Individual weight and length were determined by digital scale (0.1 g precision) and measuring tape (0.1 cm precision), respectively (Table I).

Table I
Common and scientific names and number of individuals analyzed of the most commercialized fish species in the São Luis Market, northern Brazil. Trophic position according to FishBase (2022)FISHBASE. 2022. http://www.fishbase.org. Assessed on 21 November 2022.
http://www.fishbase.org...
. Preference in diet from answers to local questionaries (n = 1.212).

Samples were prepared according to Adair & Cobb (1999)ADAIR BM & COBB GP. 1999. Improved preparation of small biological samples for mercury analysis using cold vapor atomic absorption spectroscopy. Chemosphere 12: 2951-2958.. Muscle samples individually freeze-dried upon arrival in the laboratory. Moisture content was calculated for each species and used to report the results on a wet weight basis. All species showed average moisture content of 74 ± 7.2%. Duplicate dry samples (0.5 g) were digested in Teflon® tubes containing 10 mL of analytical grade MERCK® HNO3 (65%), at room temperature for one hour and then placed in a MARS CEM microwave digester at 200 °C for 30 minutes. After digestion, 1 mL of H2O2 was added to each tube, transferred, and diluted in volumetric flasks to 100 mL. Total Hg concentrations were quantified by cold vapor atomic absorption spectrophotometry (CV-AAS) in a NIC RA-3 (NIPPON®) spectrophotometer. The average linearity coefficient of the calibration curves (R2) obtained using a MERCK® Hg calibration solution (1,000 ng L-1), was 0.9998 ± 0.0001. The average limit of detection (LOD) was 0.001 mg kg-1, calculated as three times the standard deviation of the reagent blanks divided by the slope of the calibration curve. Validation of the methods was obtained by simultaneous analysis, in duplicate, of certified reference material (Mussel Tissue ERM-CE 278K) with recovery of 95.1 ± 5.8% (n = 14) (Supplementary Material Table SI).

Human health assessment

We estimated the local fish safe level (FSLlocal) which is the maximum Hg concentration (mg kg-1 wet weight) in edible fish tissue that is safe to consume considering the local fish consumption rate (CRlocal) and the Hg reference dose (RfD). The local fish safe level (FSLlocal) was estimated using the equation (1) according to USEPA (2001)USEPA. 2001. United States Environmental Protection Agency. Water quality criterion for the protection of human health: Methylmercury final. EPA-823-R-:303. USEPA, Washington, DC., where BW is the consumer’s body weight in kg, CRlocal is the local daily fish consumption rate (kg day-1) and RfD is the reference dose of 0.0001 mg kgbw -1 day-1.

​​ FSLlocal=BW×RfDCRlocal (1)

To estimate the maximum monthly number of meals (CRmm) of each fish species that can be consumed without risk of deleterious health effects, we first modified the equation (1) to solve for the maximum safe daily fish consumption rate (CRmax) as follows, equation 1.2. where CRmax is expressed in kg day -1, and Cfish (mg kg-1) is the Hg concentration in the seafood product.

C R m a x = B W × R f D C f i s h (1.2)

After these steps, CRmm (meals per month) was calculated using equation 2 where Tap is the averaging time period (365.25 days per 12 months or 30.44 days month-1), and MS is the average meal size (kg meal-1) (USEPA 2000USEPA. 2000. United States Environmental Protection Agency. Guidance for assessing chemical contaminant data for use in fish advisories. Vol. 1: Fish sampling and analysis. EPA 823-B-00-007. Office of Science and Technology Office of Water, USEPA, Washington, DC.). For our calculation, we assumed an average fish meal size of 150 g of raw fish for adults, which roughly provides the daily calories recommendation of 190 kcal per fish portion according to the Brazilian Health Ministry (BRASIL 2014BRASIL. 2014. Guia alimentar. Como ter uma alimentação saudável. Ministério da Saúde. Available at: https://bvsms.saude.gov.br/bvs/publicacoes/guia_alimentar_alimentacao_saudavel_1edicao.pdf.
https://bvsms.saude.gov.br/bvs/publicaco...
). We assumed an average fish meal size of 75 g for children, defined here as under 6 years old.

​ ​CRmm=CRmax×TapMS (2)

Equation (3), was used to estimated the daily Hg intake (EDIHg mg kgBW -1 day-1) for two scenarios: a) Adults and children consuming fish at a daily consumption rates (CRlocal kg day-1) of 0.142 kg day -1, which is the local fish intake estimated through questionnaire application (Silva et al. 2012SILVA IA, LIMA MFV, BRANDÃO VM, DIAS ICL, SILVA MI & LACERDA LM. 2012. Perfil de consumidores do pescado comercializado em mercados do Município De São Luís, Maranhão, Brasil. Cad Pesq 19: 59-63.), and b) adults and children consuming fish at a daily consumption rate of 0.030 kg day-1, which is the per capita consumption rate for the Brazilian population (IBGE 2020IBGE - INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. 2020. Pesquisa de Orçamentos Familiares 2017-2018: Avaliação nutricional da disponibilidade domiciliar de alimentos no Brasil. Rio de Janeiro. Available at: https://sidra.ibge.gov.br/tabela/2393#resultado.
https://sidra.ibge.gov.br/tabela/2393#re...
), where Cfish (mg kg-1) is the Hg concentration in the seafood product, and BW is the consumer body weight (65.5 kg for adults (locally obtained by the questionnaires) and 15 kg for children).

​​ EDIHg=Cfish×CRlocalBW (3)

We also estimated the target hazard quotient (THQ) using equation (4) according to the United States Environmental Protection Agency (US EPA) methodology based on the Region III risk-based concentration table (USEPA 2022USEPA. 2022. United States Environmental Protection Agency. Regional Screening Levels for Chemical Contaminants at Superfund Sites. https://www.epa.gov/risk/regional-screening-levels-rsls-users-guide#special. Accessed on July, 2022.
https://www.epa.gov/risk/regional-screen...
). The THQ represents the chronic non-carcinogenic health risk posed by exposure to Hg from ingested seafood. A THQ lower than 1 represents no expected health effects while a THQ higher than 1 represents a potential for adverse health effects, where EF is the exposure frequency (365 days.yr-1), ED is the exposure duration (77 years for adults, and 6 years for children), and AT is the averaging exposure time (EF × ED).

T H Q = E F × C R l o c a l × E D × C f i s h R f D × B W × A T (4)

Statistical analysis

Outliers were identified and removed from subsequent statistical analysis. The Shapiro-Wilk test was employed to test normality assumptions. Non-parametric tests were used to compare length, weight and Hg concentrations among species (Kruskal-Wallis) and Mann-Whitney test was employed to compare differences between males and females of Cynoscion acoupa. Bioaccumulation curves were used to observe the relationship between size and Hg concentrations and the influence of feeding ecology of the sampled species (with n≥10) on their Hg content. All significant tests were conducted using an alpha value of 0.05 (95% confidence). Graphs and statistical tests were performed using Microsoft® Office 2016 and Copyright© StatSoft. Inc. (1984-2011).

RESULTS & DISCUSSION

The most important commercialized fish species in the São Luis market were sampled in this study, based on the extensive survey of Silva et al. (2012)SILVA IA, LIMA MFV, BRANDÃO VM, DIAS ICL, SILVA MI & LACERDA LM. 2012. Perfil de consumidores do pescado comercializado em mercados do Município De São Luís, Maranhão, Brasil. Cad Pesq 19: 59-63., this survey suggests a relatively large fish consumption per capita of about 2 kg per week, about 0.142 kg per day. This consumption rate is 5 times greater than the average per capita consumption for Brazilian population (0.027 kg day-1), and three times greater than the average fish consumption rate for the northeast region (Sartori & Amancio 2012SARTORI AGO & AMANCIO RD. 2012. Pescado: importância nutricional e consumo no Brasil. Segur Alimen Nutr 19: 83-93.). The nine (9) major species and their relative preference in the local consumers’ diet, and their trophic position are shown in Table I. Total Hg concentrations and the human health risk assessment parameters are shown in Tables II and III.

Table II
Mean (standard deviation), and 95th percentiles of Hg (mg kg-1), and EDI (mg kgBW 1 day-1) for seafood species. The reference dose (RfD) for Hg is 0.0001 mg kgBW -1 day-1.
Table III
Mean, standard deviation, and 95th percentile values of THQ and CRmm (meals month -1) for each seafood species. Number of meals greater than 16 meals per month indicates no obvious human health risk by consuming the respective fish species (USEPA 2000USEPA. 2000. United States Environmental Protection Agency. Guidance for assessing chemical contaminant data for use in fish advisories. Vol. 1: Fish sampling and analysis. EPA 823-B-00-007. Office of Science and Technology Office of Water, USEPA, Washington, DC.). THQ smaller than 1 indicates no apparent risk of Hg exposure to consumers (USEPA 2022USEPA. 2022. United States Environmental Protection Agency. Regional Screening Levels for Chemical Contaminants at Superfund Sites. https://www.epa.gov/risk/regional-screening-levels-rsls-users-guide#special. Accessed on July, 2022.
https://www.epa.gov/risk/regional-screen...
).

No species presented Hg concentrations higher than the Brazilian safe limits for human consumption (ANVISA 2013ANVISA. 2013. Agência Nacional de Vigilância Sanitária. Resolução - RDC Nº 42, de 29 de agosto de 2013. Regulamento Técnico MERCOSUL sobre Limites Máximos de Contaminantes Inorgânicos em Alimentos. https://bvsms.saude.gov.br/bvs/saudelegis/anvisa/2013/rdc0042_29_08_2013.html.
https://bvsms.saude.gov.br/bvs/saudelegi...
). Even considering more restrict limits, such as 0.3 mg kg-1 established by USEPA (2000)USEPA. 2000. United States Environmental Protection Agency. Guidance for assessing chemical contaminant data for use in fish advisories. Vol. 1: Fish sampling and analysis. EPA 823-B-00-007. Office of Science and Technology Office of Water, USEPA, Washington, DC., for example, average Hg concentrations did not exceed it, guaranteeing commercialization even to more strongly regulated market. In addition, we found no significant difference between sex among the species studied. Highest average Hg concentrations were measured in the Yellow hake (Cynoscion acoupa) (0.296 ± 0.241 mg kg-1) with a relative participation in the total fisheries consumption by the local population, also highest among all species, of about 28.1%, depending on season. The Atlantic croaker (Micropogonias undulatus) presented the second highest Hg concentrations (0.263 ± 0.089 mg kg-1) with about 1.5% participation only in the consumers diet, whereas Scomberomorus regalis (0.107 ± 0.039 mg kg-1) responded to about 22.5% participation, the second in the consumers preference. On the other hand, the lowest concentrations were recorded in iliophagous Mullets (Mugil curema) (0.021 ± 0.010 mg kg-1), 8.7% of preference, and the Shorthead drum (Larimus breviceps) (0.025 ± 0.009 mg kg-1), with 12.9% preference. The other for species with intermediate Hg concentrations respond together to less than 26% participation in the local consumers’ diet (Silva et al. 2012SILVA IA, LIMA MFV, BRANDÃO VM, DIAS ICL, SILVA MI & LACERDA LM. 2012. Perfil de consumidores do pescado comercializado em mercados do Município De São Luís, Maranhão, Brasil. Cad Pesq 19: 59-63.).

Apart from fish preferences, the questionnaires also showed a mean adult individual body weight of the local consumers of 65.5 kg. Of the total 574 questionnaires, 501 responded to the quantity of fish meals per week. Of those 50.5% has at least one fish meal per week, 27.1% two meals, and 12.4% three fish meals per week, 10% of the answers indicated four to 7 fish meal per week and 14.4 responded “anytime” and could not made it more precise. This reflects the relatively high consumption rates suggested by Silva et al. (2012)SILVA IA, LIMA MFV, BRANDÃO VM, DIAS ICL, SILVA MI & LACERDA LM. 2012. Perfil de consumidores do pescado comercializado em mercados do Município De São Luís, Maranhão, Brasil. Cad Pesq 19: 59-63..

Significant correlations were observed between Hg concentrations and individual length in three species: the Coco Sea catfish (Bagre bagre), the mullet (M. curema) and the Atlantic bumper (Chloroscombrus crysurus) (Figure S2). All present low to intermediate Hg concentrations and sum up a relatively small proportion of the local consumers’ diet. In addition, given the relatively uniform size of individuals of most other species and/or the small number of samples, the relationship between Hg and size was not found. Therefore, to estimate the exposure risk, fish size was not taken onto consideration nor any standardization by size was performed to the original Hg concentrations found. Similarly, no statistical differences were observed in Hg concentrations between sexes of the studied species and thus sex, was not taken into consideration, also.

The results show the importance of feeding habits as a relevant element that drives Hg concentrations in organisms. Figure 1 shows the relationship between trophic status and Hg concentrations in the studied fish species. Mercury concentrations related exponentially with trophic position. Relatively large carnivorous species with the highest trophic levels (≥ 4.0) presented the highest Hg concentrations, whereas relatively small iliophagous and omnivores (M. curema and L. breviceps) presented the lowest Hg concentrations. This trend in the distribution of Hg concentrations with the highest found in carnivorous and the lowest in iliophagous or herbivores has been extensively reported in literature on fish Hg content in north and northeastern Brazil fish species (Bastos et al. 2015BASTOS WR, DÓREA JG, BERNARDI JVE, MANZATTO AG, LAUTHARTTE LC, MUSSY MH, LACERDA LD & MALM O. 2015. Mercury in fish of the Madeira River (temporal and spatial assessment), Brazilian Amazon. Environ Res 140: 191-197., Lacerda et al. 2016LACERDA LD, BEZERRA MF, COSTA BGB, BRAGA TM & GOYANNA FAA. 2016. Mercury distribution in fish commercialized at the Mucuripe market, Fortaleza, Ceará state, Brazil. Arq Ciênc Mar 49: 50-54. https://doi.org/10.32360/acmar.v49i1.6159.
https://doi.org/10.32360/acmar.v49i1.615...
, Moura et al. 2018MOURA VL, COSTA BGB & LACERDA LD. 2018. Distribuição de mercúrio na fauna estuarina do rio Jaguaribe – CE. Arq Ciênc Mar 51: 49-56. https://doi.org/10.32360/acmar.v51i1.20387.
https://doi.org/10.32360/acmar.v51i1.203...
, Moura & Lacerda 2022MOURA V & LACERDA LD. 2022. Mercury sources, emissions, distribution and bioavailability along an estuarine gradient under semiarid conditions in NE Brazil. Inter J Pollut Res Pub Health 19: 17092. https://doi.org/10.3390/ijprph192417092.
https://doi.org/10.3390/ijprph192417092...
).

Figure 1
Exponential relationship between Hg concentrations and trophic position of fish species most commercialized in the São Luís fish market, Maranhão, Northern Brazil.

All collected fishes, except M. curema, are carnivorous species, some however, small fish predating mostly on invertebrates, principally polychaetes, crustaceans, and mollusks C. acoupa is a large, mostly piscivore species, Ferreira et al. (2015)FERREIRA MS, MARQUES NA, RIBEIRO ROR, CONTE JR CA, CARNEIRO CS, SANTELLI RE, FREIRE AS, SÃO CLEMENTE SC & MÁRSICO ET. 2015. Total mercury in carnivorous fish from Brazilian Southeast. Bull Environ Contam Toxicol 95: 18-24. https://doi.org/10.1007/s00128-015-1470-3.
https://doi.org/10.1007/s00128-015-1470-...
found a fish occurrence frequency of 48.3% in the adult individuals’ stomachs of C. acoupa and this ecological characteristic explains the high Hg concentrations. Micropogonias undulatus and Scomberomorusregalis, also large carnivores with diet like C. acoupa (Mendes & Barthem 2010MENDES FLS & BARTHEM RB. 2010. Hábitos alimentares de bagres marinhos (Siluriformes: Ariidae) do Estuário Amazônico. Amazônia: Ci Desenv 5: 153-166.), also presented relatively high Hg concentrations. This pattern of larger fishes usually presenting higher Hg concentrations than smaller ones (Gorski et al. 2003GORSKI SM, CHITTARANJAN S, PLEASANCE ED, FREEMAN JD, ANDERSON CL, VARHOL RJ, COUGHLIN SM, ZUYDERDUYN SD, JONES SJM, MARRA MA. 2003. A SAGE approach to discovery of genes involved in autophagic cell death. Curr Biol 13: 358-363., Gewurtz et al. 2011GEWURTZ SB, BHAVSAR SP, JACKSON DA, AWAD E, WINTER JG, KOLIC TM, REINER EJ, MOODY R & FLETCHER R. 2011. Trends of legacy and emerging-issue contaminants in Lake Simcoe fishes. J Great Lakes Res 37: 148-159., Verdouw et al. 2011VERDOUW JJ, MACLEOD CK, NOWAK BF & LYLE JL. 2011. Implications of age, size and region on mercury contamination in estuarine fish species. Water Air Soil Pollut 214: 297-306.). The strong and positive correlation between Hg and fish length observed in B. bagre, C. chrysurus, and M. curema (Figure S2) shows the importance of size in affecting Hg concentrations.

The exposure risk for Hg through seafood consumption varied with species and consumer type. We estimated THQ, EDIHg, CRmax, and CRmm, for adults and children, using mean and 95th percentile values of Hg concentrations for each fish species, for two consumption scenarios: a) A per capita fish consumption of 30 g day-1; and b) A fish consumption rate of 142 g day-1 (Tables II, III). The 95th percentiles are the high-end exposure estimates and represent the plausible worst-case scenario (USEPA 2000USEPA. 2000. United States Environmental Protection Agency. Guidance for assessing chemical contaminant data for use in fish advisories. Vol. 1: Fish sampling and analysis. EPA 823-B-00-007. Office of Science and Technology Office of Water, USEPA, Washington, DC.). Under scenario “a”, THQ was slightly greater than 1 for C. acoupa and M. undulatus for adult consumers, while for children consumers a THQ greater than 1 was observed for C acoupa, M. undulatus, A. props, S. regalis, B. bagre, and M. furnieri (Table III). When considering the 95th percentile values, the same result was observed (Table III). Under scenario “b”, THQ was greater than 1 for C acoupa, M. undulatus, A. props, S. regalis, B. bagre, and M. furnieri for adult consumers, while for children a THQ greater than 1 was observed for all species (Table III). When considering the 95th percentile values, the same result was also observed (Table III). Similarly, under scenario “a”, the estimated daily intake (EDI) for adult consumers exceeded slightly the Hg reference dose (RfD) of 0.0001 mg kgBW day-1 for C. acoupa and M. undulatus (Table III). For children, EDI values greater than RfD were observed for C. acoupa, M. undulatus, A. props, S. regalis, B. bagre, and M. furnieri. When considering the 95th percentile values, a similar result was observed (Table II). Under scenario “b”, EDI values exceeded the RfD for C. acoupa, M. undulatus, A. props, S. regalis, B. bagre, and M. furnieri (Table II). For children under scenario “b”, the EDI for all sampled species exceeded the reference dose (Table II). A similar result was also observed when considering the 95th percentile values of Hg concentrations (Table II).

We calculated the number of seafood meals per month that can be safely consumed by children and adult consumers (Figure 2 and Table III). For adult consumers (average weight of 65.5 kg), four out of the nine studied species require some restriction of consumption. These species are M. undulatus, C. acoupa, A. proops, and S. regatta, with a maximum of 5.5, 10.6, 12.4, and 14 meals per month, respectively. For children consumers (average weight of 15 kg), seven out of nine studied species require some restriction of consumption. These species are M. undulatus, C. acoupa, A. proops, S. regatta, M. furnieri, B. bagre, and C. chrysurus, with a maximum of 2.5, 4.8, 5.7, 6.4, 10.2, 10.3, and 14.6 meals per month, respectively.

Figure 2
Estimated number of meals per month that can be safely consumed by Adult (Top) and Children (Bottom) in Maranhão State.

The estimated fish screening levels (FSL, mg kg-1) for adults and children consuming seafood under different scenarios are shown in Table IV. For adults and children consuming fish at a rate of 30 g per day (per capita consumption for Maranhão State), the Hg concentration of fish should not exceed 0.22 and 0.05 mg kg-1, respectively. These protective Hg levels are even lower if we assume a consumption rate of 142 g per day (São Luiz fish market consumption rate), 0.05 and 0.01 mg kg-1, for adults and children respectively. We observed that the higher the seafood consumption rate the lower the FSL, as shown by the FSL from different Brazilian fish-eating populations (Table IV), where the lowest FSL are observed in the Amazon riverine inhabitants, characterized by extremely high fish consumption rate.

Table IV
Fish screening levels for adults (65.5 kg of average body weight) and children (15 kg of average body weight) considering multiple fish consumption rates.

It becomes clear that the Hg exposure risk in humans, from seafood consumption, is strongly dependent of consumption rate, and consumer body weight, as well as the Hg burden in seafood. This is why relying solely on indices, such as THQ and EDI, is not enough to estimate the multiple scenarios of exposure in any given seafood consumer’s population. The maximum Hg levels established by regulatory agencies are also not protective of consumers, since fish with Hg concentrations much lower than these maximum limits still represent risks of Hg exposure to consumers, depending on consumption rates (Figure 2, Table III). In addition, to better inform about Hg exposure risks, it is important to provide consumers with the maximum number of meals that can be safely consumed for each one of the most consumed seafood types. As shown in Figure 3, we argue that it is more effective to provide consumers with species specific information to allow them to an informed decision as it relates to how much seafood they will consume.

Figure 3
Safe fish maximum amount consumed per month at different body weigths for Cynoscion acoupa from São Luiz fish market.

CONCLUSIONS

The results confirm the importance of fish in the São Luís population, well above the average Brazilian fish consumption and as high as those observed in the Amazon region. The most consumed species, yellow hake (C. acoupa) and croakers (Micropogonias spp.) are those with the highest Hg concentrations, but still below the maximum limits of 0.5 mg kg-1. However, we found that seafood from the São Luiz fish market can be an important source Hg exposure to consumers depending on the consumption rate and the type of consumer. Particularly for children, consuming seafood at a rate of 142 g day-1, we estimated EDI values greater than the reference dose for all species. On the other hand, at a lower consumption rate (30 g day-1, the average for MA state), we found EDI values to be lower than the reference dose for the following species: Bagre bagre, Micropogonias furnieri, Chloroscombrus chrysurus, Larimus breviceps, and Mugil Curema. Therefore, the rate of seafood consumption and the type of consumer (adult and children) are important metrics when assessing exposure risk to contaminants. This is why we found that most studied species could potentially pose some risk of Hg exposure to human consumers, even with Hg levels below the established safety limit of 0.5 mg kg-1.

It is important to note that these exposure estimates are for those consuming seafood consistently at moderate to high rates over a long period of time (12 consecutive months) and, thus, should be seen as the worst-case scenario rather than the norm. The estimated Fish Screening Level (FSL) for adults and children are 0.22 and 0.05 mg kg-1, respectively, which can be interpreted as the upper limit of Hg contamination in fish that does not require consumption restrictions.

An important observation is the apparent lack of relationship between size and Hg concentrations. Apart from the small number of samples, this my result form the uniform size of commercialized fish. A part of the population, mostly fishers and those buying catches directly from them, may consume smaller or large sizes, which may eventually alter their risk assessment. This calls for urgent evaluation of the variability of Hg concentrations in a broader range of size to increase precaution regarding Hg exposure through fish consumption.

Finally, we recommend using multiple exposure metrics and scenarios when assessing Hg exposure risk from seafood consumption and informing consumers of the maximum number of meals per month estimated to inform and protect seafood consumers.

ACKNOWLEDGMENTS

We thank the Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico - FUNCAP Proc. No. INT 00159-00009.01.00/19 and the Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA), for the financial support. LD Lacerda received a grant no. 302.362/2018-5 and INCT-TMCOcean no. 405.765/2022-3 from CNPq.

SUPPLEMENTARY MATERIAL

Figures S1, S2. Table SI.

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Publication Dates

  • Publication in this collection
    15 Apr 2024
  • Date of issue
    2024

History

  • Received
    06 Mar 2023
  • Accepted
    09 July 2023
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