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Elemental Contamination in Brown Mussels (Perna perna) Marketed in Southeastern Brazil

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Abstract

Perna perna mussels, abundant throughout the Brazilian coast, are routinely applied as bioindicators in environmental monitoring actions due to their sessile and filter-feeding characteristics. In addition, they are noteworthy for their food importance, especially for coastal populations. In this context, the aim of this study was to investigate elemental contamination in commercially marketed and highly consumed P. perna samples from the highly impacted Guanabara Bay, Rio de Janeiro, Brazil. A total of 30 mussels were sampled, and elemental concentrations (As, Cd, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Se, V, and Zn) were determined in adductor muscle samples by inductively coupled plasma mass spectrometry (ICP-MS). Human consumption risks were assessed by comparisons to Brazilian and international legislations. No significant differences between sex were observed for all analyzed elements. Even when analyzing only the adductor muscle, all mussel samples exceeded the Brazilian limit for Cr, while 12 samples exceeded the limit for Se. When compared to other regulatory agencies, As and Zn levels were higher than the limits set by China, New Zealand, and the USA. Estimated daily dietary intake values were not above limits imposed by the Food and Agriculture Organization of the United Nations/World Health Organization for any of the assessed elements, although it is important to note that only the adductor muscle was assessed. Therefore, continuous metal and metalloid monitoring in bivalves in the study region is suggested, as metal transport and bioavailability, especially in coastal estuaries such as Guanabara Bay, which are currently undergoing significant changes due to anthropogenic activities.

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References

  1. Alloway BJ, Ayres DC (1997) Chemical principles of environmental pollution. Blackie Academic & Professional, London

    Google Scholar 

  2. Coleman N, Castrejon A, Blaine C, Chemmachel T (2017) The toxicology of essential and nonessential metals. Lulu Publishing Services

  3. Rosa AH, Fraceto LF, Moschini-Carlos V (2012) Meio Ambiente e Sustentabilidade. Bookman, Porto Alegre

    Google Scholar 

  4. Streit B (1998) Bioaccumulation of contaminants in fish. In: Braunbeck T, Hinton DE, Streit B (eds) Fish Ecotoxicology. Birkhäuser Verlag Basel, pp 353–387

  5. Fujiki M, Tajima S (1992) The pollution of Minamata Bay by mercury. Water Sci Technol 25(11):133–140

    Article  CAS  Google Scholar 

  6. Freire C, Ramos R, Lopez-Espinosa MJ, Díez S, Vioque J, Ballester F, Fernández MF (2010) Hair mercury levels, fish consumption, and cognitive development in preschool children from Granada, Spain. Environ Res 110:96–104. https://doi.org/10.1016/j.envres.2009.10.005

    Article  CAS  PubMed  Google Scholar 

  7. WHO (2017) Mercury and health. https://www.who.int/news-room/fact-sheets/detail/mercury-and-health. Accessed 20 July 2020.

  8. MacFarquhar JK, Broussard DL, Melstrom P, Hutchinson R, Wolkin A, Martin C, Burk RF, Dunn JR, Green AL, Hammond R, Schaffner W, Jones TF (2010) Acute selenium toxicity associated with a dietary supplement. Arch Intern Med 170(3):256–261

    Article  Google Scholar 

  9. Ebrahimi M, Taherianfard M (2011) The effects of heavy metals exposure on reproductive systems of cyprinid fish from Kor River. Iran J Fish Sci 10(1):13–24

    Google Scholar 

  10. Yee-Duarte JA, Ceballos-Vázquez BP, Arellano-Martínez M, Camacho-Mondragón MA, Uría-Galicia E (2018) Histopathological alterations in the gonad of Megapitaria squalida (Mollusca: Bivalvia) inhabiting a heavy metals polluted environment. J Aquat Anim Health 30:144–154. https://doi.org/10.1002/aah.10015

    Article  PubMed  Google Scholar 

  11. Lavradas RT, Rocha RCC, Bordon ICAC, Saint’Pierre TD, Godoy JM, Hauser-Davis RA (2016) Differential metallothionein, reduced glutathione and metal levels in Perna perna mussels in two environmentally impacted tropical bays in southeastern Brazil. Ecotoxicol Environ Saf 129:75–84. https://doi.org/10.1016/j.ecoenv.2016.03.011

    Article  CAS  PubMed  Google Scholar 

  12. Campolim MB, Henriques MB, Barbieri E (2018) Al, Cd, Cr, Cu, Fe, Mn, Ni, Pb, and Zn in mussels collected in Santos Bay, São Paulo, Brazil: limits required by local legislation. Bol Inst Pesca 44(4):1–8. https://doi.org/10.20950/1678-2305.2018.44.4.374

    Article  CAS  Google Scholar 

  13. Barbosa IS, Brito GB, Santos GL, Santos LN, Teixeira LSG, Araujo RGO, Korn MGA (2019) Multivariate data analysis of trace elements in bivalve molluscs: characterization and food safety evaluation. Food Chem 273:64–70. https://doi.org/10.1016/j.foodchem.2018.02.063

    Article  CAS  PubMed  Google Scholar 

  14. Azevedo JAM, Barros AB, Mirando PRB, Costa JG, Nascimento VX (2019) Biomonitoring of heavy metals (Fe, Zn, Cu, Mn, Cd and Cr) in oysters: Crassostrea rhizophorae of mangrove areas of Alagoas (Brazil). Braz Arch Biol Technol 63:1–11

    Google Scholar 

  15. Marques HLA (1998) Criação comercial de mexilhões. Nobel, São Paulo

    Google Scholar 

  16. Resgalla C Jr, Weber LI, Conceição MB (2008) O Mexilhão Perna perna (L.): biologia, ecologia e aplicações. Interciência, Rio de Janeiro

    Google Scholar 

  17. IBGE (2016) Produção da Pecuária Municipal. IBGE, Rio de Janeiro

    Google Scholar 

  18. Galvão P, Longo R, Torres JPM, Malm O (2015) Estimating the potential production of the brown mussel Perna perna (Linnaeus, 1758) reared in three tropical bays by different methods of condition indices. J Mar Biol 2015:1–11. https://doi.org/10.1155/2015/948053

    Article  Google Scholar 

  19. Ferreira JF, Magalhães ARM (2004) Cultivo de mexilhões. In Poli CR, Poli ATB, Andreatta ER, Beltrame E (ed) Aquicultura: experiências brasileiras. Multitarefa, pp 221–250.

  20. Maia CB, Almeida ACM, Moreira FR (2006) Avaliação do teor de chumbo em mexilhões da espécie Perna perna na região metropolitana da cidade do Rio de Janeiro. J Braz Soc Ecotoxicol 1(2):195–198

    Article  Google Scholar 

  21. Barroso RM, Wiefels AC (2010) O mercado de pescado da região metropolitana do Rio de Janeiro – 2010. INFOPESCA

  22. Neto JAB, Peixoto TCS, Smith BJ, Mcalister JJ, Patchineelam SM, Patchineelam SR, Fonseca EM (2013) Geochronology and heavy metal flux to Guanabara Bay, Rio de Janeiro state: a preliminary study. An Acad Bras Ciênc 85(4):1317–1327. https://doi.org/10.1590/0001-3765201394612

    Article  CAS  Google Scholar 

  23. O Globo (2015) Expansão da maricultura em Jurujuba, que já foi premiada pela ONU, agora preocupa navegantes. https://oglobo.globo.com/rio/bairros/expansao-da-maricultura-em-jurujuba-que-ja-foi-premiada-pela-onu-agora-preocupa-navegantes-15961888. Accessed 27 January 2021.

  24. Lage H, Jablonski S (2008) Mussel Perna perna extraction and commercialization in Guanabara Bay, Brazil. Atlântica 30(2):161–169

    Google Scholar 

  25. Lunetta JE (1969) Fisiologia da reprodução dos mexilhões (Mytilus perna-Mollusca lamellibranchia). Bolm Zool Biol Mar 26:33–111

    Google Scholar 

  26. Heil N (2009) National wild fish health survey – laboratory procedures manual. 5.0. Edition. U.S. Fish and Wildlife Service, Warm Springs

    Google Scholar 

  27. Eurachem (1998) The fitness for purpose of analytical methods. Eurachem Guide, First English Edition 1.0.

  28. Inmetro (2016) Orientação sobre validação de métodos analíticos: documento de caráter orientativo. DOQ-CGCRE-008.

  29. Brazil (2009) Apparent per capital consumption of fish in Brazil, 1996–2009.

  30. IBAMA (2006) Instrução Normativa n° 105, de 20 de julho de 2006. Diário Oficial da União.

  31. Campolim MB, Henriques MB, Petesse ML, Rezende KFO, Barbieri E (2017) Metal trace elements in mussels in Urubuqueçaba Island, Santos Bay, Brazil. Pesqui Agropecu Bras 52(12):1131–1139. https://doi.org/10.1590/s0100-204x2017001200001

    Article  Google Scholar 

  32. Carvalho CEV, Cavalcante MPO, Gomes MP, Faria VV, Rezende CE (2001) Distribuição de metais pesados em mexilhões (Perna perna, L.) da Ilha de Santana, Macaé, SE, Brasil. Ecotoxicology and Environmental Restoration 4(1):1–5

    Google Scholar 

  33. Ferreira AG, Machado ALS, Zalmon IR (2004) Temporal and spatial variation on heavy metal concentrations in the bivalve Perna perna (LINNAEUS, 1758) on the Northern Coast of Rio de Janeiro State, Brazil. Braz Arch Biol Technol 47(2):319–327

    Article  CAS  Google Scholar 

  34. Kehrig HA, Costa M, Moreira I, Malm O (2006) Total and methyl mercury in different species of molluscs from two estuaries in Rio de Janeiro State. J Braz Chem Soc 17(7):1409–1418

    Article  CAS  Google Scholar 

  35. Orren MJ, Eagle GA, Hennig HFKO, Green A (1980) Variations in trace metal content of the mussel Choromytilus meridionalis (Kr.) with season and sex. Mar Pollut Bull 11:253–257

    Article  CAS  Google Scholar 

  36. Baptista Neto JA, Smith BJ, McAllister JJ, Silva MAM (2005) Fontes e transporte de metais pesados para a Enseada de Jurujuba (Baía de Guanabara) SE – Brasil. Rev Tamoios 2:11–21

    Google Scholar 

  37. Baptista Neto JA, Silva MAM (1996) Caracterização dos Sedimentos de Fundo e Dinâmica Sedimentar da Enseada de Jurujuba (Baía de Guanabara), Niterói, RJ. Pesquisas 23(1/3):7–16

    Google Scholar 

  38. Lino AS, Galvão PMA, Longo RTL, Azevedo-Silva CE, Dorneles PR, Torres JPM, Malm O (2016) Metal bioaccumulation in consumed marine bivalves in Southeast Brazilian coast. J Trace Elem Med Biol 34:50–55. https://doi.org/10.1016/j.jtemb.2015.12.004

    Article  CAS  PubMed  Google Scholar 

  39. Francioni E, Wagener ALR, Calixto RC, Bastos GC (2004) Evaluation of Perna perna (Linné, 1758) as a tool to monitoring trace metals contamination in estuarine and coastal waters of Rio de Janeiro, Brazil. J Braz Chem Soc 15(1):103–110

    Article  CAS  Google Scholar 

  40. Kehrig HA, Costa M, Malm O (2007) Estudo da contaminação por metais pesados em peixes e mexilhão da Baía de Guanabara – Rio de Janeiro. Trop Oceanogr 35(1):32–50

    Google Scholar 

  41. Belabed BE, Laffray X, Dhib A, Fertouna-Belakhal M, Turki S, Aleya L (2013) Factors contributing to heavy metal accumulation in sediments and in the intertidal mussel Perna perna in the Gulf of Annaba (Algeria). Mar Pollut Bull 74(1):477–489. https://doi.org/10.1016/j.marpolbul.2013.06.004

    Article  CAS  PubMed  Google Scholar 

  42. Diop M, Howsam M, Diop C, Goossens JF, Diouf A, Amara R (2016) Assessment of trace element contamination and bioaccumulation in algae (Ulva lactuca), mussels (Perna perna), shrimp (Penaeus kerathurus), and fish (Mugil cephalus, Sarotherondon melanotheron) along the Senegalese coast. Mar Pollut Bull 103(1):339–343. https://doi.org/10.1016/j.marpolbul.2015.12.038

    Article  CAS  PubMed  Google Scholar 

  43. Legraa MH, Er-Raioui H, Dartige AY, Zamel MLC, Abidine MMO, Sidoumou Z, Saleck AM (2019) Assessment of metallic contamination of the Northern Atlantic coast of Mauritania (Coastal Fringe “Levrier Bay”), using Perna perna. Int J Civ Eng Technol 10(4):782–795

    Google Scholar 

  44. Castillo I, Acosta V, Martínez G, Núñez M (2005) Niveles de metales pesados em gónadas y músculo aductor del mejillón marrón, Perna perna, cultivado en la ensenada de Turpialito, Golfo de Cariaco, estado Sucre, Venezuela. Zootec Trop 23(2):141–154

    Google Scholar 

  45. PNQA (2021) Indicadores de Qualidade – Índice de Balneabilidade. http://pnqa.ana.gov.br/indicadores-balneabilidade.aspx. Accessed 27 January 2021.

  46. Niterói (2017) Praias de Niterói alcançam maior índice de balneabilidade desde 2013. http://www.niteroi.rj.gov.br/index.php?option=com_content&view=article&id=5092&Itemid=1. Accessed 7 July 2020.

  47. Niterói (2019) “Praia Hoje” traz informações sobre balneabilidade na orla da cidade. http://www.niteroi.rj.gov.br/index.php?option=com_content&view=article&id=5778&Itemid=1. Accessed 7 July 2020.

  48. Conti ME, Stripeikis J, Finoia MG, Tudino MB (2011) Baseline trace metals in bivalve molluscs from the Beagle Channel, Patagonia (Argentina). Ecotoxicology 20:1341–1353

    Article  CAS  Google Scholar 

  49. Tapia J, Vargas-Chacoff L, Bertrán C, Carrasco G, Torres F, Pinto R, Urzúa S, Valderrama A, Letelier L (2010) Study of the content of cadmium, chromium and lead in bivalve molluscs of the Pacific Ocean (Maule Region, Chile). Food Chem 121:666–671

    Article  CAS  Google Scholar 

  50. ANVISA (1965) Decreto n° 55871, de 26 de março de 1965. Modifica o Decreto n° 50040, de 24 de janeiro de 1961 referente a normas regulamentadoras do emprego de aditivos para alimentos, alterado pelo Decreto n° 691, de 13 de março de 1962. Diário Oficial da União.

  51. ANVISA (2013) Resolução da Diretoria Colegiada – RDC no 42, de 29 de agosto de 2013. Dispõe sobre o Regulamento Técnico MERCOSUL sobre Limites Máximos de Contaminantes Inorgânicos em Alimentos. Diário Oficial da União.

  52. EC (2006) Commission Regulation (EC) no. 1881/2006 of 19 December 2006. Setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Union.

  53. FAO/WHO (2000) Evaluation of certain food additives and contaminants: fifty-third report of the Joint FAO/WHO Expert Committee on Food Additives. WHO Technical Report Series no. 896.

  54. FSANZ (2017) Australia New Zealand Food Standards Code – Schedule 19 – maximum levels of contaminants and natural toxicants. https://www.legislation.gov.au/Details/F2017C00333. Accessed 8 August 2020.

  55. MAFF (1998) Monitoring and surveillance of non-radioactive contaminants in the aquatic environment and activities regulating the disposal of wastes at sea, 1995 and 1996. Aquatic Environment Monitoring Report no. 51. CEFAS.

  56. MHPRC (2012) National food safety standard: maximum levels of contaminants in food. GB 2762-2012.

  57. USEPA (2007) Risk-based concentration Table.

  58. Hauser-Davis RA, Bordon ICAC, Oliveira TF, Ziolli RL (2016) Metal bioaccumulation in edible target tissues of mullet (Mugil liza) from a tropical bay in Southeastern Brazil. J Trace Elem Med Biol 36:38–43. https://doi.org/10.1016/j.jtemb.2016.03.016

    Article  CAS  PubMed  Google Scholar 

  59. Linos A, Petralias A, Christophi CA, Christoforidou E, Kouroutou P, Stoltidis M, Veloudaki A, Tzala E, Makris K, Karagas MR (2011) Oral ingestion of hexavalent chromium through drinking water and cancer mortality in an industrial area of Greece - an ecological study. Environmental Health 10:1–8. https://doi.org/10.1186/1476-069X-10-50

    Article  CAS  Google Scholar 

  60. Xing WZ, Qun CJ, Yuan CL, Hui YZ, Hui HS, Zheng Y (2011) Environmental impact and site-specific human health risks of chromium in the vicinity of a ferro-alloy manufactory, China. J Hazard Mater 190:980–985. https://doi.org/10.1016/j.jhazmat.2011.04.039

    Article  CAS  Google Scholar 

  61. Avelar WEP, Mantelatto FLM, Tomazelli AC, Silva DML, Shuhama T, Lopes JLC (2000) The marine mussel Perna perna (Mollusca, Bivalvia, Mytilidae) as an indicator of contamination by heavy metals in the Ubatuba Bay, São Paulo, Brazil. Water Air Soil Pollut 118:65–72

    Article  CAS  Google Scholar 

  62. Cullen WR, Reimer KJ (2017) Arsenic is everywhere: cause for concern? Royal Society of Chemistry, Cambridge

    Google Scholar 

  63. IARC (2012) A review of human carcinogens. Part C: Arsenic, metals, fibres, and dusts/ IARC Working Group on the Evaluation of Carcinognic Risks to Humans.

  64. Catharino MGM, Vasconcellos MBA, Kirschbaum AA, Gasparro MR, Minei CC, Sousa ECPM, Seo D, Moreira EG (2012) Biomonitoring of coastal regions of São Paulo State, Brazil, using mussels Perna perna. J Radioanal Nucl Chem 291:113–117. https://doi.org/10.1007/s10967-011-1291-8

    Article  CAS  Google Scholar 

  65. Igic PG, Lee E, Harper W, Roach KW (2002) Toxic effects associated with consumption of zinc. Mayo Clin Proc 77:713–716

    Article  Google Scholar 

  66. Porea TJ, Belmont JW, Maboney DH (2000) Zinc-induced anemia and neutropenia in an adolescent. J Pediatr 136(5):688–690. https://doi.org/10.1067/mpd.2000.103355

    Article  CAS  PubMed  Google Scholar 

  67. FAO/WHO (2004) Summary of evaluations performed by the Joint FAO/WHO expert Committee on Food Additives (JECFA 1956-2003): first through sixty first meetings. ILSI Press International Life Sciences Institute

  68. FAO/WHO (2011) Evaluation of certain food additives and contaminants: seventy-fourth report of the Joint FAO/WHO Expert Committee on Food Additives. WHO Technical Report Series no. 966.

  69. EVM (2002) Review of cobalt. Expert Group on Vitamins and Minerals Secretariat revised August, EVM/00/07.

  70. FAO/WHO (2011) Evaluation of certain contaminants in food: seventy-second report of the Joint FAO/WHO Expert Committee on Food Additives. WHO Technical Report Series no. 959.

  71. FAO/WHO (2011) Evaluation of certain food additives and contaminants: seventy-third report of the Joint FAO/WHO Expert Committee on Food Additives. WHO Technical Report Series no. 960.

  72. WHO (2005) Ecosystems and human well-being: heath synthesis. World Health Organization

  73. Brasil (2006) Decreto de 13 de julho de 2006. Altera a denominação, competência e composição da Comissão Nacional de Desenvolvimento Sustentável das Comunidades Tradicionais e dá outras providências. http://www.planalto.gov.br/ccivil_03/_Ato2004-2006/2006/Dnn/Dnn10884.htm. Accessed 27 August 2020.

  74. Brasil (2007) Decreto no 6.040, de 7 de fevereiro de 2007. Institui a política nacional de desenvolvimento sustentável dos povos e comunidades tradicionais. http://www.planalto.gov.br/ccivil_03/_ato2007-2010/2007/decreto/d6040.htm. Accessed 27 August 2020.

  75. EC (2021) The challenge of climate change to the European coastal areas. https://ec.europa.eu/environment/iczm/state_coast.htm. Accessed 30 January 2021.

  76. Wijngaard RR, Perk M, Grift B, Nijs TCM, Bierkens MFP (2017) The impact of climate change on metal transport in a lowland catchment. Water Air Soil Pollut 228:107. https://doi.org/10.1007/s11270-017-3261-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Machado AS, Zarfl C, Toffolon M, Cronin K, O'Shea FT (2016) Could climate change affect metal pollution in estuaries? 7th SETAC World Congress/SETAC North America 37th Annual Meeting. Orlando.

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Funding

This study was funded by the Áreas de Apoio à Pesquisa/Fundação Oswaldo Cruz (PAEF/FIOCRUZ IOC-023-FIO-18) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (Finance code 001), Brazil. CP Santos and TD Saint’Pierre acknowledge grants from the CNPq (303336/2017-0 and 311820/2017-4) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) (E-26/202.673/2019).

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Conceptualization: AGL Oliveira, RA Hauser-Davis, and CP Santos. Methodology: AGL Oliveira, RCC Rocha, and TD Saint’Pierre. Data curation: AGL Oliveira and RA Hauser-Davis. Investigation: AGL Oliveira, RA Hauser-Davis, and CP Santos. Formal analysis: RA Hauser-Davis, CC Mello-Silva, and CP Santos. Writing, review and editing: AGL Oliveira, TD Saint’Pierre, RA Hauser-Davis, CC Mello-Silva, and CP Santos. Supervision: CC Mello-Silva and CP Santos. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Rachel Ann Hauser-Davis.

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This study was authorized by the Brazilian Institute of the Environment and Renewable Natural Resources (IBAMA, license no. 68263-1 and 68263-2) and National System for the Management of Genetic Heritage and Associated Traditional Knowledge (SisGen, no. A20BC45) and approved by the Animal Ethics Committee of the Oswaldo Cruz Foundation (CEUA, Fiocruz no. L-008/2018) in accordance with the guidelines of the Brazilian College for Animal Experiments (COBEA).

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de Oliveira, A.G.L., Rocha, R.C.C., Saint’Pierre, T.D. et al. Elemental Contamination in Brown Mussels (Perna perna) Marketed in Southeastern Brazil. Biol Trace Elem Res 200, 402–412 (2022). https://doi.org/10.1007/s12011-021-02644-y

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