Bioavailability of polycyclic aromatic hydrocarbons in Santos Bay (Brazil) and its adjacent continental shelf
DOI:
https://doi.org/10.1590/Keywords:
Biomarker of exposure, PAH metabolites, HPLC/F, fish metabolites, biomonitoringAbstract
This study evaluated the bioavailability of polycyclic aromatic hydrocarbons (PAHs) in Santos Bay (SB) and the
adjacent Santos Continental Shelf (SCS) in Brazil. Biliary metabolites were measured in several fish species to
establish a baseline for future monitoring programs. Bile samples from different species of fish were collected monthly
from July to December 2005 in SB, and in August 2005 and February 2006 on SCS. Metabolite concentrations
were determined using high-performance liquid chromatography with fluorescence detectors. Naphthalene,
phenanthrene, and benzo[a]pyrene metabolite concentrations ranged from 24 to 810 µg g-1 of bile, 1.8 to 68 µg g-1
of bile, and below the limit of quantitation to 1.3 µg g-1 of bile, respectively. Despite its high concentrations, the levels
of naphthalene metabolites were in regions of low-contamination, while benzo[a]pyrene metabolite were in the
same range as those reported in moderately contaminated areas, which may indicate pyrolytic contamination
by PAHs. No significant differences in the metabolite concentrations were found between the SB and the SCS
samples or during the periods of collection. Future studies with a single biomonitoring species should be conducted,
considering age, sex, and feeding condition of the individuals. The metabolite data presented in this study is an
important baseline information for this urbanized region, which hosts several sources of contaminants.
References
de Albergaria-Barbosa, A. C. R., Patire, V. F., Taniguchi, S.,
Fernandez, W. S., Dias, J. F. & Bícego, M. C. 2017.
Mugil curema as a PAH bioavailability monitor for
Atlantic west sub-tropical estuaries. Marine Pollution
Bulletin, 114(1), 609–614. DOI: https://doi.org/10.1016/
j.marpolbul.2016.09.039
de Albergaria-Barbosa, A. C. R., da Silva, D. A. M.,
da Silva Rocha, A. J., Taniguchi, S., Patire, V. F., Dias,
J. F., Fernandez, W. S. & Bícego, M. C. 2018. Evaluation
of polycyclic aromatic hydrocarbons bioavailability on
Santos Bay (Brazil) through levels of biliary metabolites.
Marine Pollution Bulletin, 129(2), 822–828. DOI:
https://doi.org/10.1016/j.marpolbul.2017.10.006
Anulación, B. F., Ylitalo, G. M., Sol, S. Y., da Silva, D. A. M.,
Lomax, D. P. & Johnson, L. L. 2020. Temporal trends
in aluminum smelter-derived polycyclic aromatic
hydrocarbons in outmigrant juvenile Chinook salmon
from Kitimat, British Columbia, Canada. Marine Pollution
Bulletin, 157, 111284. DOI: https://doi.org/10.1016/
j.marpolbul.2020.111284
Azevedo, J. S., Lopes, B., Katsumiti, A., Braga, E. S.,
Roche, H., Ribeiro, C. A. O. & Bebianno, M. J. 2012.
Evidence of contamination by oil and oil products in the
Santos-São Vicente estuary, São Paulo, Brazil. Brazilian
Journal of Oceanography, 60(2), 117–126. DOI:
https://doi.org/10.1590/s1679-87592012000200002
Barreto, I. S., de Albergaria-Barbosa, A. C. R., Patire, V. F.,
de Jesus Silva, M., Baldassin, P., Taniguchi, S.,
Montone, R. C., Gallo, H., Maranho, A. & Bícego, M. C.
Bioavailability of polycyclic aromatic hydrocarbons
to penguins on the coast of southeastern Brazil. Marine
Pollution Bulletin, 157, 111306. DOI: https://doi.org/
1016/j.marpolbul.2020.111306
Baumann, P. & Harshbarger, J. 1998. Long term trends
in liver neoplasm epizootics of brown bullhead in
the Black River, Ohio. Environmental Monitoring
and Assessment, 53, 213–223. DOI: https://doi.org/
1023/A:1005967631275
Beyer, J., Jonsson, G., Porte, C., Krahn, M. M. & Ariese, F.
Analytical methods for determining metabolites
of polycyclic aromatic hydrocarbon (PAH) pollutants
in fish bile: A review. Environmental Toxicology and
Pharmacology, 30(3), 224–244. DOI: https://doi.org/
1016/j.etap.2010.08.004
Black, J. J. 1983. Field and laboratory studies of
environmental carcinogenesis in Niagara River fish.
Journal of Great Lakes Research, 9(2), 326–334. DOI:
https://doi.org/10.1016/s0380-1330(83)71902-7
Bouloubassi, I. & Saliot, A. 1993. Investigation of
anthropogenic and natural organic inputs in estuarine
sediments using hydrocarbon markers (NAH,
LAB, PAH). Oceanologica Acta, 16(2), 145–161.
Britvić, S., Lucić, D. & Kurelec, B. 1993. Bile fluorescence
and some early biological effects in fish as indicators
of pollution by xenobiotics. Environmental Toxicology
and Chemistry, 12(4), 765–773. DOI: https://doi.org/
1002/etc.5620120418
Cetesb, S. P. 1999. Relatório anual da qualidade do ar no
estado de São Paulo 1998 (Relatórios ambientais).
São Paulo: Companhia de Tecnologia de Saneamento
Ambiental (Cetesb).
Collier, T. K., Anulación, B. F., Arkoosh, M. R., Dietrich, J. P.,
Incardona, J. P., Johnson, L. L., Ylitalo, G. M. &
Myers, M. S. 2013. Effects on fish of polycyclic aromatic
hydrocarbons (PAHS) and naphthenic acid exposures.
Fish physiology (Vol. 33, pp. 195–255). Elsevier. DOI:
https://doi.org/10.1016/b978-0-12-398254-4.00004-2
Collier, T. K. & Varanasi, U. 1991. Hepatic activities of
xenobiotic metabolizing enzymes and biliary levels
of xenobiotics in English sole (Parophrys vetulus)
exposed to environmental contaminants. Archives of
Environmental Contamination and Toxicology, 20(4),
–473. DOI: https://doi.org/10.1007/bf01065834
Colombo, J. C., Cappelletti, N., Lasci, J., Migoya, M. C.,
Speranza, E. & Skorupka, C. N. 2006. Sources, vertical
fluxes, and equivalent toxicity of aromatic hydrocarbons
in coastal sediments of the Río de la Plata estuary,
Argentina. Environmental Science & Technology,
(3), 734–740. DOI: https://doi.org/10.1021/es051672y
Eggensl, M. L., Vethaak, A. D., Leaverz, M. J.,
Horbach, G. J. M. J., Boon, J. P. & Seinen, W. 1996.
Differences in CYP1A response between flounder
(Platichthys flesus) and plaice (Pleuronectes platessa)
after long-term exposure to harbour dredged spoil in
a mesocosm study. Chemosphere, 32(7), 1357–1380.
DOI: https://doi.org/10.1016/0045-6535(96)00046-x
Escartín, E. & Porte, C. 1999a. Biomonitoring of PAH pollution
in high-altitude mountain lakes through the analysis of
PAHs bioavailability in a contaminated area
Ocean and Coastal Research 2023, v71(suppl 2):e23024 8
Patire et al.
fish bile. Environmental Science & Technology, 33(3),
–409. DOI: https://doi.org/10.1021/es980798a
Escartín, E. & Porte, C. 1999b. Hydroxylated PAHs in bile of
deep-sea fish. Relationship with xenobiotic metabolizing
enzymes. Environmental Science & Technology, 33(16),
–2714. DOI: https://doi.org/10.1021/es9902322
Fernández-Tajes, J., Flórez, F., Pereira, S., Rábade, T.,
Laffon, B. & Méndez, J. 2011. Use of three bivalve species
for biomonitoring a polluted estuarine environment.
Environmental Monitoring and Assessment, 177(1),
–300. DOI: https://doi.org/10.1007/s10661-010-1634-x
Fontes, M. K., de Campos, B. G., Cortez, F. S.,
Pusceddu, F. H., Moreno, B. B., Maranho, L. A.,
Lebre, D. T., Guimarães, L. L. & Pereira, C. D. S. 2019.
Seasonal monitoring of cocaine and benzoylecgonine in
a subtropical coastal zone (Santos Bay, Brazil). Marine
Pollution Bulletin, 149, 110545. DOI: https://doi.org/
1016/j.marpolbul.2019.110545
Fuchsman, P. C., Leigh, K. B. & Barber, T. R. 2001.
Ecological assessment of PAHs in fish. Sediments
guidance compendium. Palo Alto, CA: EPRI.
Guimarães, L. M., França, E. J. D., de Arruda, G. N. &
de Albergaria-Barbosa, A. C. R. 2020. Historical inputs
of polycyclic aromatic hydrocarbons in the preserved
tropical estuary of the Itapicuru River, Bahia, Brazil.
Marine Pollution Bulletin, 156, 111218. DOI: https://
doi.org/10.1016/j.marpolbul.2020.111218
Helcom. 2013. HELCOM core indicators: Final report of
the HELCOM CORESET project. Helsinki: Helsinki
Comission.
Hylland, K., Sandvik, M., Skåre, J. U., Beyer, J., Egaas, E. &
Goksøyr, A. 1996. Biomarkers in flounder (Platichthys
flesus): an evaluation of their use in pollution monitoring.
Marine Environmental Research, 42(1), 223–227.
DOI: https://doi.org/10.1016/0141-1136(95)00034-8
Kammann, U. 2007. PAH metabolites in bile fluids of
dab (Limanda limanda) and flounder (Platichthys
flesus): Spatial distribution and seasonal changes
(7 pp). Environmental Science and Pollution
Research — International, 14(2), 102–108. DOI:
https://doi.org/10.1065/espr2006.05.308
Kammann, U., Akcha, F., Budzinski, H., Burgeot, T.,
Gubbins, M. J., Lang, T., Menach, K. L., Vethaak, A. D. &
Hylland, K. 2017. PAH metabolites in fish bile: From
the Seine estuary to Iceland. Marine Environmental
Research, 124, 41–45. DOI: https://doi.org/10.1016/
j.marenvres.2016.02.014
Kim, B. S. M., Salaroli, A. B., de Lima Ferreira, P. A.,
Sartoretto, J. R., de Mahiques, M. M. & Figueira, R. C. L.
Spatial distribution and enrichment assessment
of heavy metals in surface sediments from Baixada
Santista, Southeastern Brazil. Marine Pollution
Bulletin, 103(1), 333–338. DOI: https://doi.org/
1016/j.marpolbul.2015.12.041
Krahn, M. M., Myers, M. S., Burrows, D. G. &
Malins, D. C. 1984. Determination of metabolites of
xenobiotics in the bile of fish from polluted waterways.
Xenobiotica; the Fate of Foreign Compounds in
Biological Systems, 14(8), 633–646. DOI: https://doi.org/
3109/00498258409151461
Krahn, M. M., Rhodes, L. D., Myers, M. S., Moore, L. K.,
MacLeod, W. D. & Malins, D. C. 1986. Associations
between metabolites of aromatic compounds in bile
and the occurrence of hepatic lesions in English sole
(Parophrys vetulus) from Puget Sound, Washington.
Archives of Environmental Contamination and Toxicology,
(1), 61–67. DOI: https://doi.org/10.1007/bf01055249
Krahn, M. M., Ylitalo, G. M., Buzitis, J., Bolton, J. L.,
Wigren, C. A., Chan, S.-L. & Varanasi, U. 1993.
Analyses for petroleum-related contaminants in marine
fish and sediments following the Gulf oil spill. Marine
Pollution Bulletin, 27, 285–292. DOI: https://doi.org/
1016/0025-326x(93)90035-i
Magalhães, C. A., Taniguchi, S., Lourenço, R. A. &
Montone, R. C. 2017. Organochlorine pesticides, PCBs,
and PBDEs in liver and muscle tissues of Paralonchurus
brasiliensis, Trichiurus lepturus and Cathorops spixii in
Santos Bay and surrounding area, São Paulo, Brazil.
Regional Studies in Marine Science, 16, 42–48. DOI:
https://doi.org/10.1016/j.rsma.2017.08.010
Martins, C. C., Bícego, M. C., Mahiques, M. M.,
Figueira, R. C. L., Tessler, M. G. & Montone, R. C.
Polycyclic aromatic hydrocarbons (PAHs) in a
large South American industrial coastal area (Santos
Estuary, Southeastern Brazil). Sources and depositional
history. Marine Pollution Bulletin, 63(5), 452–458.
DOI: https://doi.org/10.1016/j.marpolbul.2011.03.017
Martins, C. C., Mahiques, M. M., Bícego, M. C.,
Fukumoto, M. M. & Montone, R. C. 2007. Comparison
between anthropogenic hydrocarbons and magnetic
susceptibility in sediment cores from the Santos Estuary,
Brazil. Marine Pollution Bulletin, 54(2), 240–246.
DOI: https://doi.org/10.1016/j.marpolbul.2006.11.006
McCain, B. B., Malins, D. C., Krahn, M. M., Brown, D. W.,
Gronlund, W. D., Moore, L. K. & Chan, S.-L. 1990.
Uptake of aromatic and chlorinated hydrocarbons by
juvenile chinook salmon (Oncorhynchus tshawytscha)
in an urban estuary. Archives of Environmental
Contamination and Toxicology, 19(1), 10–16.
DOI: https://doi.org/10.1007/bf01059807
Medeiros, P. M. & Bícego, M. C. 2004a. Investigation
of natural and anthropogenic hydrocarbon inputs in
sediments using geochemical markers. I. Santos, SP –
Brazil. Marine Pollution Bulletin, 49(9), 761–769.
DOI: https://doi.org/10.1016/j.marpolbul.2004.06.001
Medeiros, P. M. & Bícego, M. C. 2004b. Investigation of natural
and anthropogenic hydrocarbon inputs in sediments
using geochemical markers. II. São Sebastião, SP –
Brazil. Marine Pollution Bulletin, 49(11), 892–899.
DOI: https://doi.org/10.1016/j.marpolbul.2004.06.002
Pulster, E. L., Gracia, A., Armenteros, M., ToroFarmer, G., Snyder, S. M., Carr, B. E., Schwaab, M. R.,
Nicholson, T. J., Mrowicki, J. & Murawski, S. A. 2020.
A first comprehensive baseline of hydrocarbon pollution
in Gulf of Mexico fishes. Scientific Reports, 10(1), 1–14.
DOI: https://doi.org/10.1038/s41598-020-62944-6
Rotchell, J., Bird, D. & Newton, L. 1999. Seasonal variation
in ethoxyresorufin O-deethylase (EROD) activity
in European eels Anguilla anguilla and flounders
Pleuronectes flesus from the Severn estuary and
Bristol channel. Marine Ecology Progress Series, 190,
–270. DOI: https://doi.org/10.3354/meps190263
da Silva, D. A. M., Buzitis, J., Krahn, M. M., Bícego, M. C. &
Pires-Vanin, A. M. S. 2006. Metabolites in bile of fish
from São Sebastião Channel, São Paulo, Brazil as
biomarkers of exposure to petrogenic polycyclic aromatic
PAHs bioavailability in a contaminated area
Ocean and Coastal Research 2023, v71(suppl 2):e23024 9
Patire et al.
compounds. Marine Pollution Bulletin, 52(2), 175–183.
DOI: https://doi.org/10.1016/j.marpolbul.2005.08.016
Silva, J. S., Alves, R. N., de Paulo, D. V., Jr., C. F. M.,
de Melo Alves, M. K. & Carvalho, P. S. M. 2021. Biliary
polycyclic aromatic hydrocarbons and enzymatic
biomarkers in Eugerres brasilianus along four tropical
estuaries. Marine Pollution Bulletin, 163, 111919.
DOI: https://doi.org/10.1016/j.marpolbul.2020.111919
Snyder, S. M., Olin, J. A., Pulster, E. L. & Murawski, S. A.
Spatial contrasts in hepatic and biliary PAHs in
Tilefish (Lopholatilus chamaeleonticeps) throughout
the Gulf of Mexico, with comparison to the Northwest
Atlantic. Environmental Pollution, 258, 113775.
DOI: https://doi.org/10.1016/j.envpol.2019.113775
Soclo, H. H., Garrigues, P. & Ewald, M. 2000. Origin of
polycyclic aromatic hydrocarbons (PAHs) in coastal
marine sediments: Case studies in Cotonou (Benin)
and Aquitaine (France) areas. Marine Pollution Bulletin,
(5), 387–396. DOI: https://doi.org/10.1016/s0025-
x(99)00200-3
Upshall, C., Payne, J. F. & Hellou, J. 1993. Induction of
MFO enzymes and production of bile metabolites in
rainbow trout (Oncorhynchus mykiss) exposed to waste
crankcase oil. Environmental Toxicology and Chemistry,
(11), 2105–2112. DOI: https://doi.org/10.1002/
etc.5620121118
Varanasi, U. 1989. Metabolism of polycyclic aromatic
hydrocarbons in the aquatic environment (1st ed.).
Boca Raton: CRC Press.
White, K. L. 1986. An overview of immunotoxicology
and carcinogenic polycyclic aromatic hydrocarbons.
Environmental Carcinogenesis Reviews, 4(2), 163–202.
DOI: https://doi.org/10.1080/10590508609373342
Yunker, M. B., Macdonald, R. W., Vingarzan, R.,
Mitchell, R. H., Goyette, D. & Sylvestre, S. 2002. PAHs in
the Fraser River basin: a critical appraisal of PAH ratios
as indicators of PAH source and composition. Organic
Geochemistry, 33(4), 489–515. DOI: https://doi.org/
1016/s0146-6380(02)00002-5
