Toxicity of spike fragments SARS-CoV-2 S protein for zebrafish: A tool to study its hazardous for human health?

Detalhes bibliográficos
Autor(a) principal: Ventura Fernandes, Bianca H.
Data de Publicação: 2022
Outros Autores: Feitosa, Natália Martins, Barbosa, Ana Paula, Bomfim, Camila Gasque, Garnique, Anali M.B., Rosa, Ivana F. [UNESP], Rodrigues, Maira S. [UNESP], Doretto, Lucas B. [UNESP], Costa, Daniel F. [UNESP], Camargo-dos-Santos, Bruno [UNESP], Franco, Gabrielli A. [UNESP], Neto, João Favero [UNESP], Lunardi, Juliana Sartori [UNESP], Bellot, Marina Sanson [UNESP], Alves, Nina Pacheco Capelini [UNESP], Costa, Camila C. [UNESP], Aracati, Mayumi F. [UNESP], Rodrigues, Letícia F. [UNESP], Cirilo, Rafaela Hemily [UNESP], Colagrande, Raul Marcelino [UNESP], Gomes, Francisco I.F., Nakajima, Rafael T. [UNESP], Belo, Marco A.A., Giaquinto, Percília Cardoso [UNESP], de Oliveira, Susana Luporini [UNESP], Eto, Silas Fernandes, Fernandes, Dayanne Carla, Manrique, Wilson G., Conde, Gabriel [UNESP], Rosales, Roberta R.C., Todeschini, Iris, Rivero, Ilo, Llontop, Edgar, Sgro, Germán G., Oka, Gabriel Umaji, Bueno, Natalia Fernanda, Ferraris, Fausto K., de Magalhães, Mariana T.Q., Medeiros, Renata J., Mendonça-Gomes, Juliana M., Junqueira, Mara Souza, Conceição, Kátia, Pontes, Leticia Gomes de, Condino-Neto, Antonio, Perez, Andrea C., Barcellos, Leonardo J.G., Júnior, José Dias Correa, Dorlass, Erick Gustavo, Camara, Niels O.S., Durigon, Edison Luiz, Cunha, Fernando Q., Nóbrega, Rafael H. [UNESP], Machado-Santelli, Glaucia M., Farah, Chuck S., Veras, Flavio P., Galindo-Villegas, Jorge, Costa-Lotufo, Letícia V., Cunha, Thiago M., Chammas, Roger, Carvalho, Luciani R., Guzzo, Cristiane R., Malafaia, Guilherme, Charlie-Silva, Ives
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1016/j.scitotenv.2021.152345
http://hdl.handle.net/11449/231582
Resumo: Despite the significant increase in the generation of SARS-CoV-2 contaminated domestic and hospital wastewater, little is known about the ecotoxicological effects of the virus or its structural components in freshwater vertebrates. In this context, this study evaluated the deleterious effects caused by SARS-CoV-2 Spike protein on the health of Danio rerio, zebrafish. We demonstrated, for the first time, that zebrafish injected with fragment 16 to 165 (rSpike), which corresponds to the N-terminal portion of the protein, presented mortalities and adverse effects on liver, kidney, ovary and brain tissues. The conserved genetic homology between zebrafish and humans might be one of the reasons for the intense toxic effects followed inflammatory reaction from the immune system of zebrafish to rSpike which provoked damage to organs in a similar pattern as happen in severe cases of COVID-19 in humans, and, resulted in 78,6% of survival rate in female adults during the first seven days. The application of spike protein in zebrafish was highly toxic that is suitable for future studies to gather valuable information about ecotoxicological impacts, as well as vaccine responses and therapeutic approaches in human medicine. Therefore, besides representing an important tool to assess the harmful effects of SARS-CoV-2 in the aquatic environment, we present the zebrafish as an animal model for translational COVID-19 research.
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spelling Toxicity of spike fragments SARS-CoV-2 S protein for zebrafish: A tool to study its hazardous for human health?Acute respiratory syndromeCoronavirusDanio rerioEnvironmental impactsInfection diseasesDespite the significant increase in the generation of SARS-CoV-2 contaminated domestic and hospital wastewater, little is known about the ecotoxicological effects of the virus or its structural components in freshwater vertebrates. In this context, this study evaluated the deleterious effects caused by SARS-CoV-2 Spike protein on the health of Danio rerio, zebrafish. We demonstrated, for the first time, that zebrafish injected with fragment 16 to 165 (rSpike), which corresponds to the N-terminal portion of the protein, presented mortalities and adverse effects on liver, kidney, ovary and brain tissues. The conserved genetic homology between zebrafish and humans might be one of the reasons for the intense toxic effects followed inflammatory reaction from the immune system of zebrafish to rSpike which provoked damage to organs in a similar pattern as happen in severe cases of COVID-19 in humans, and, resulted in 78,6% of survival rate in female adults during the first seven days. The application of spike protein in zebrafish was highly toxic that is suitable for future studies to gather valuable information about ecotoxicological impacts, as well as vaccine responses and therapeutic approaches in human medicine. Therefore, besides representing an important tool to assess the harmful effects of SARS-CoV-2 in the aquatic environment, we present the zebrafish as an animal model for translational COVID-19 research.Ministério da Ciência, Tecnologia e InovaçãoFundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)Laboratório de Controle Genético e Sanitário Diretoria Técnica de Apoio ao Ensino e Pesquisa Faculdade de Medicina da Universidade de São PauloLaboratório Integrado de Biociências Translacionais (LIBT) Instituto de Biodiversidade e Sustentabilidade (NUPEM) Universidade Federal do Rio de Janeiro (UFRJ)Department of Microbiology Institute of Biomedical Sciences University of Sao PauloDepartment of Cell Biology Institute of Biomedical Sciences University of São PauloReproductive and Molecular Biology Group Department of Morphology Institute of Biosciences Sao Paulo State UniversityDepartment of Structural and Functional Biology Institute of Biosciences of Botucatu São Paulo State UniversityDepartment of Preventive Veterinary Medicine São Paulo State University (UNESP)Department of Pharmacology Center of Research in Inflammatory Diseases Ribeirao Preto Medical School University of São PauloBrasil UniversityUniversidade Estadual Paulista Júlio de Mesquita Filho Instituto de Biociências - Departamento de FisiologiaUniversidade Estadual Paulista Júlio de Mesquita FilhoPostgraduate Program in Health Sciences PROCISA Federal University of RoraimaImmunochemistry Laboratory Butantan InstituteAquaculture Health Research and Extension Group GRUPESA Aquaculture Health Laboratory LABSA Department of Veterinary Medicine Federal University of Rondônia, Rolim de Moura campusDepartment of Preventive Veterinary Medicine São Paulo State UniversityDepartment of Cell and Molecular Biology Ribeirao Preto Medical School University of São PauloDepartamento de Bioquímica Instituto de Química Universidade de São PauloPontifícia Universidade Católica de Minas GeraisDepartamento de Ciências Biomoleculares Faculdade de Ciências Farmacêuticas de Ribeirão Preto Universidade de São PauloDepartment of Pharmacology and Toxicology Oswaldo Cruz Foundation, FIOCRUZDepartment of Biochemistry and Immunology Institute of Biological Sciences Federal University of Minas GeraisLaboratory of Physiology INCQS/Fiocruz Zebrafish Facility Departament of Pharmacology and Toxicology National Institute for Quality Control in HealthTransplantation Immunobiology Lab Department of Immunology Institute of Biomedical Sciences Universidade de Sao PauloCenter for Translational Research in Oncology Cancer Institute of the State of Sao Paulo Faculty of Medicine University of São PauloLaboratory of Peptide Biochemistry Federal University of São PauloLaboratory of Human Immunology Department Immunology Institute Biomedical Sciences University São PauloDepartment of Pharmacology Universidade Federal de Minas GeraisGraduate Program of Pharmacology Federal University of Santa MariaLaboratory of Fish Physiology Graduate Program of Bioexperimentation and of Environmental Sciences University of Passo FundoLaboratório do Estudo da Interação Químico Biológica e da Reprodução Animal LIQBRA, Bloco O3,174Departamento de Morfologia Instituto de Ciências Biológicas Universidade Federal de Minas GeraisCenter of Research in Inflammatory Diseases Ribeirão Preto Medical School University of Sao PauloDepartment of Pharmacology Ribeirao Preto Medical School University of São PauloFaculty of Biosciences and Aquaculture Nord UniversityDepartment of Pharmacology Institute of Biomedical Sciences Universidade de São PauloCentro de Investigação Translacional em Oncologia Instituto do Câncer do Estado de São Paulo Faculdade de Medicina da Universidade de São PauloDisciplina de Endocrinologia do Departamento de Clinica Medica e Laboratório de Hormônios e Genética Molecular, LIM 42Biological Research Laboratory Goiano Federal Institute, Urutaí CampusReproductive and Molecular Biology Group Department of Morphology Institute of Biosciences Sao Paulo State UniversityDepartment of Structural and Functional Biology Institute of Biosciences of Botucatu São Paulo State UniversityDepartment of Preventive Veterinary Medicine São Paulo State University (UNESP)Universidade Estadual Paulista Júlio de Mesquita Filho Instituto de Biociências - Departamento de FisiologiaUniversidade Estadual Paulista Júlio de Mesquita FilhoDepartment of Preventive Veterinary Medicine São Paulo State UniversityMinistério da Ciência, Tecnologia e Inovação: 0459/20FAPESP: 2014/04294-1FAPESP: 2017/17303-7FAPESP: 2018/07098-0FAPESP: 2019/00195-2FAPESP: 2019/12234-2FAPESP: 2019/14285-3FAPESP: 2019/18356-2FAPESP: 2019/19939-1FAPESP: 2019/21739-0FAPESP: 2020/04680-0FAPESP: 2020/05761-3CNPq: 303263/2018-0CNPq: 307743/2018-7CNPq: 426531/2018-3Universidade de São Paulo (USP)Universidade Federal do Rio de Janeiro (UFRJ)Universidade Estadual Paulista (UNESP)Brasil UniversityFederal University of RoraimaButantan InstituteFederal University of RondôniaPontifícia Universidade Católica de Minas GeraisOswaldo Cruz FoundationUniversidade Federal de Minas Gerais (UFMG)National Institute for Quality Control in HealthUniversity São PauloFederal University of Santa MariaUniversity of Passo FundoLIQBRANord UniversityDisciplina de Endocrinologia do Departamento de Clinica Medica e Laboratório de Hormônios e Genética MolecularGoiano Federal InstituteVentura Fernandes, Bianca H.Feitosa, Natália MartinsBarbosa, Ana PaulaBomfim, Camila GasqueGarnique, Anali M.B.Rosa, Ivana F. [UNESP]Rodrigues, Maira S. [UNESP]Doretto, Lucas B. [UNESP]Costa, Daniel F. [UNESP]Camargo-dos-Santos, Bruno [UNESP]Franco, Gabrielli A. [UNESP]Neto, João Favero [UNESP]Lunardi, Juliana Sartori [UNESP]Bellot, Marina Sanson [UNESP]Alves, Nina Pacheco Capelini [UNESP]Costa, Camila C. [UNESP]Aracati, Mayumi F. [UNESP]Rodrigues, Letícia F. [UNESP]Cirilo, Rafaela Hemily [UNESP]Colagrande, Raul Marcelino [UNESP]Gomes, Francisco I.F.Nakajima, Rafael T. [UNESP]Belo, Marco A.A.Giaquinto, Percília Cardoso [UNESP]de Oliveira, Susana Luporini [UNESP]Eto, Silas FernandesFernandes, Dayanne CarlaManrique, Wilson G.Conde, Gabriel [UNESP]Rosales, Roberta R.C.Todeschini, IrisRivero, IloLlontop, EdgarSgro, Germán G.Oka, Gabriel UmajiBueno, Natalia FernandaFerraris, Fausto K.de Magalhães, Mariana T.Q.Medeiros, Renata J.Mendonça-Gomes, Juliana M.Junqueira, Mara SouzaConceição, KátiaPontes, Leticia Gomes deCondino-Neto, AntonioPerez, Andrea C.Barcellos, Leonardo J.G.Júnior, José Dias CorreaDorlass, Erick GustavoCamara, Niels O.S.Durigon, Edison LuizCunha, Fernando Q.Nóbrega, Rafael H. [UNESP]Machado-Santelli, Glaucia M.Farah, Chuck S.Veras, Flavio P.Galindo-Villegas, JorgeCosta-Lotufo, Letícia V.Cunha, Thiago M.Chammas, RogerCarvalho, Luciani R.Guzzo, Cristiane R.Malafaia, GuilhermeCharlie-Silva, Ives2022-04-29T08:46:15Z2022-04-29T08:46:15Z2022-03-20info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1016/j.scitotenv.2021.152345Science of the Total Environment, v. 813.1879-10260048-9697http://hdl.handle.net/11449/23158210.1016/j.scitotenv.2021.1523452-s2.0-85122092948Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengScience of the Total Environmentinfo:eu-repo/semantics/openAccess2022-04-29T08:46:16Zoai:repositorio.unesp.br:11449/231582Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T16:26:08.471Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Toxicity of spike fragments SARS-CoV-2 S protein for zebrafish: A tool to study its hazardous for human health?
title Toxicity of spike fragments SARS-CoV-2 S protein for zebrafish: A tool to study its hazardous for human health?
spellingShingle Toxicity of spike fragments SARS-CoV-2 S protein for zebrafish: A tool to study its hazardous for human health?
Ventura Fernandes, Bianca H.
Acute respiratory syndrome
Coronavirus
Danio rerio
Environmental impacts
Infection diseases
title_short Toxicity of spike fragments SARS-CoV-2 S protein for zebrafish: A tool to study its hazardous for human health?
title_full Toxicity of spike fragments SARS-CoV-2 S protein for zebrafish: A tool to study its hazardous for human health?
title_fullStr Toxicity of spike fragments SARS-CoV-2 S protein for zebrafish: A tool to study its hazardous for human health?
title_full_unstemmed Toxicity of spike fragments SARS-CoV-2 S protein for zebrafish: A tool to study its hazardous for human health?
title_sort Toxicity of spike fragments SARS-CoV-2 S protein for zebrafish: A tool to study its hazardous for human health?
author Ventura Fernandes, Bianca H.
author_facet Ventura Fernandes, Bianca H.
Feitosa, Natália Martins
Barbosa, Ana Paula
Bomfim, Camila Gasque
Garnique, Anali M.B.
Rosa, Ivana F. [UNESP]
Rodrigues, Maira S. [UNESP]
Doretto, Lucas B. [UNESP]
Costa, Daniel F. [UNESP]
Camargo-dos-Santos, Bruno [UNESP]
Franco, Gabrielli A. [UNESP]
Neto, João Favero [UNESP]
Lunardi, Juliana Sartori [UNESP]
Bellot, Marina Sanson [UNESP]
Alves, Nina Pacheco Capelini [UNESP]
Costa, Camila C. [UNESP]
Aracati, Mayumi F. [UNESP]
Rodrigues, Letícia F. [UNESP]
Cirilo, Rafaela Hemily [UNESP]
Colagrande, Raul Marcelino [UNESP]
Gomes, Francisco I.F.
Nakajima, Rafael T. [UNESP]
Belo, Marco A.A.
Giaquinto, Percília Cardoso [UNESP]
de Oliveira, Susana Luporini [UNESP]
Eto, Silas Fernandes
Fernandes, Dayanne Carla
Manrique, Wilson G.
Conde, Gabriel [UNESP]
Rosales, Roberta R.C.
Todeschini, Iris
Rivero, Ilo
Llontop, Edgar
Sgro, Germán G.
Oka, Gabriel Umaji
Bueno, Natalia Fernanda
Ferraris, Fausto K.
de Magalhães, Mariana T.Q.
Medeiros, Renata J.
Mendonça-Gomes, Juliana M.
Junqueira, Mara Souza
Conceição, Kátia
Pontes, Leticia Gomes de
Condino-Neto, Antonio
Perez, Andrea C.
Barcellos, Leonardo J.G.
Júnior, José Dias Correa
Dorlass, Erick Gustavo
Camara, Niels O.S.
Durigon, Edison Luiz
Cunha, Fernando Q.
Nóbrega, Rafael H. [UNESP]
Machado-Santelli, Glaucia M.
Farah, Chuck S.
Veras, Flavio P.
Galindo-Villegas, Jorge
Costa-Lotufo, Letícia V.
Cunha, Thiago M.
Chammas, Roger
Carvalho, Luciani R.
Guzzo, Cristiane R.
Malafaia, Guilherme
Charlie-Silva, Ives
author_role author
author2 Feitosa, Natália Martins
Barbosa, Ana Paula
Bomfim, Camila Gasque
Garnique, Anali M.B.
Rosa, Ivana F. [UNESP]
Rodrigues, Maira S. [UNESP]
Doretto, Lucas B. [UNESP]
Costa, Daniel F. [UNESP]
Camargo-dos-Santos, Bruno [UNESP]
Franco, Gabrielli A. [UNESP]
Neto, João Favero [UNESP]
Lunardi, Juliana Sartori [UNESP]
Bellot, Marina Sanson [UNESP]
Alves, Nina Pacheco Capelini [UNESP]
Costa, Camila C. [UNESP]
Aracati, Mayumi F. [UNESP]
Rodrigues, Letícia F. [UNESP]
Cirilo, Rafaela Hemily [UNESP]
Colagrande, Raul Marcelino [UNESP]
Gomes, Francisco I.F.
Nakajima, Rafael T. [UNESP]
Belo, Marco A.A.
Giaquinto, Percília Cardoso [UNESP]
de Oliveira, Susana Luporini [UNESP]
Eto, Silas Fernandes
Fernandes, Dayanne Carla
Manrique, Wilson G.
Conde, Gabriel [UNESP]
Rosales, Roberta R.C.
Todeschini, Iris
Rivero, Ilo
Llontop, Edgar
Sgro, Germán G.
Oka, Gabriel Umaji
Bueno, Natalia Fernanda
Ferraris, Fausto K.
de Magalhães, Mariana T.Q.
Medeiros, Renata J.
Mendonça-Gomes, Juliana M.
Junqueira, Mara Souza
Conceição, Kátia
Pontes, Leticia Gomes de
Condino-Neto, Antonio
Perez, Andrea C.
Barcellos, Leonardo J.G.
Júnior, José Dias Correa
Dorlass, Erick Gustavo
Camara, Niels O.S.
Durigon, Edison Luiz
Cunha, Fernando Q.
Nóbrega, Rafael H. [UNESP]
Machado-Santelli, Glaucia M.
Farah, Chuck S.
Veras, Flavio P.
Galindo-Villegas, Jorge
Costa-Lotufo, Letícia V.
Cunha, Thiago M.
Chammas, Roger
Carvalho, Luciani R.
Guzzo, Cristiane R.
Malafaia, Guilherme
Charlie-Silva, Ives
author2_role author
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dc.contributor.none.fl_str_mv Universidade de São Paulo (USP)
Universidade Federal do Rio de Janeiro (UFRJ)
Universidade Estadual Paulista (UNESP)
Brasil University
Federal University of Roraima
Butantan Institute
Federal University of Rondônia
Pontifícia Universidade Católica de Minas Gerais
Oswaldo Cruz Foundation
Universidade Federal de Minas Gerais (UFMG)
National Institute for Quality Control in Health
University São Paulo
Federal University of Santa Maria
University of Passo Fundo
LIQBRA
Nord University
Disciplina de Endocrinologia do Departamento de Clinica Medica e Laboratório de Hormônios e Genética Molecular
Goiano Federal Institute
dc.contributor.author.fl_str_mv Ventura Fernandes, Bianca H.
Feitosa, Natália Martins
Barbosa, Ana Paula
Bomfim, Camila Gasque
Garnique, Anali M.B.
Rosa, Ivana F. [UNESP]
Rodrigues, Maira S. [UNESP]
Doretto, Lucas B. [UNESP]
Costa, Daniel F. [UNESP]
Camargo-dos-Santos, Bruno [UNESP]
Franco, Gabrielli A. [UNESP]
Neto, João Favero [UNESP]
Lunardi, Juliana Sartori [UNESP]
Bellot, Marina Sanson [UNESP]
Alves, Nina Pacheco Capelini [UNESP]
Costa, Camila C. [UNESP]
Aracati, Mayumi F. [UNESP]
Rodrigues, Letícia F. [UNESP]
Cirilo, Rafaela Hemily [UNESP]
Colagrande, Raul Marcelino [UNESP]
Gomes, Francisco I.F.
Nakajima, Rafael T. [UNESP]
Belo, Marco A.A.
Giaquinto, Percília Cardoso [UNESP]
de Oliveira, Susana Luporini [UNESP]
Eto, Silas Fernandes
Fernandes, Dayanne Carla
Manrique, Wilson G.
Conde, Gabriel [UNESP]
Rosales, Roberta R.C.
Todeschini, Iris
Rivero, Ilo
Llontop, Edgar
Sgro, Germán G.
Oka, Gabriel Umaji
Bueno, Natalia Fernanda
Ferraris, Fausto K.
de Magalhães, Mariana T.Q.
Medeiros, Renata J.
Mendonça-Gomes, Juliana M.
Junqueira, Mara Souza
Conceição, Kátia
Pontes, Leticia Gomes de
Condino-Neto, Antonio
Perez, Andrea C.
Barcellos, Leonardo J.G.
Júnior, José Dias Correa
Dorlass, Erick Gustavo
Camara, Niels O.S.
Durigon, Edison Luiz
Cunha, Fernando Q.
Nóbrega, Rafael H. [UNESP]
Machado-Santelli, Glaucia M.
Farah, Chuck S.
Veras, Flavio P.
Galindo-Villegas, Jorge
Costa-Lotufo, Letícia V.
Cunha, Thiago M.
Chammas, Roger
Carvalho, Luciani R.
Guzzo, Cristiane R.
Malafaia, Guilherme
Charlie-Silva, Ives
dc.subject.por.fl_str_mv Acute respiratory syndrome
Coronavirus
Danio rerio
Environmental impacts
Infection diseases
topic Acute respiratory syndrome
Coronavirus
Danio rerio
Environmental impacts
Infection diseases
description Despite the significant increase in the generation of SARS-CoV-2 contaminated domestic and hospital wastewater, little is known about the ecotoxicological effects of the virus or its structural components in freshwater vertebrates. In this context, this study evaluated the deleterious effects caused by SARS-CoV-2 Spike protein on the health of Danio rerio, zebrafish. We demonstrated, for the first time, that zebrafish injected with fragment 16 to 165 (rSpike), which corresponds to the N-terminal portion of the protein, presented mortalities and adverse effects on liver, kidney, ovary and brain tissues. The conserved genetic homology between zebrafish and humans might be one of the reasons for the intense toxic effects followed inflammatory reaction from the immune system of zebrafish to rSpike which provoked damage to organs in a similar pattern as happen in severe cases of COVID-19 in humans, and, resulted in 78,6% of survival rate in female adults during the first seven days. The application of spike protein in zebrafish was highly toxic that is suitable for future studies to gather valuable information about ecotoxicological impacts, as well as vaccine responses and therapeutic approaches in human medicine. Therefore, besides representing an important tool to assess the harmful effects of SARS-CoV-2 in the aquatic environment, we present the zebrafish as an animal model for translational COVID-19 research.
publishDate 2022
dc.date.none.fl_str_mv 2022-04-29T08:46:15Z
2022-04-29T08:46:15Z
2022-03-20
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1016/j.scitotenv.2021.152345
Science of the Total Environment, v. 813.
1879-1026
0048-9697
http://hdl.handle.net/11449/231582
10.1016/j.scitotenv.2021.152345
2-s2.0-85122092948
url http://dx.doi.org/10.1016/j.scitotenv.2021.152345
http://hdl.handle.net/11449/231582
identifier_str_mv Science of the Total Environment, v. 813.
1879-1026
0048-9697
10.1016/j.scitotenv.2021.152345
2-s2.0-85122092948
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Science of the Total Environment
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.source.none.fl_str_mv Scopus
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
repository.mail.fl_str_mv
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