Abstract
The aim of this study was to evaluate cytotoxicity and genotoxicity in multiple organs of rats induced by municipal effluent released by submarine outfall in city of Santos. A total of 20 male Wistar rats were exposed to effluents by drinking water ad libitum at concentrations of 0, 10, 50, and 100 % for 30 days. Microscopic analysis revealed severe lesions such as necrosis and hemorrhagic areas in liver and kidney from animals exposed to effluent at 50 and 100 % concentration. DNA damage in peripheral blood, liver, and kidney cells were detected by comet assay at higher concentrations of effluent. Moreover, a decrease DNA repair capacity was detected in liver cells. Significant statistical differences (p < 0.05) for micronucleated cells from liver were noticed at 50 % concentration of effluent. Taken together, our results demonstrate that municipal effluent is able to induce cytotoxicity and genotoxicity in multiple organs of Wistar rats.
Similar content being viewed by others
References
Abessa DMS, Rachid BRF, Moser GAO, Oliveira AJFC (2012) Environmental effects of sewage oceanic disposal by submarine outfall: a review. O Mundo da saúde 36(4):643–661
Aguiar O Jr, Gollucke APB, Moraes BB, Pasquini G, Catharino RR, Riccio MF, Ihara SSM, Ribeiro DA (2011) Grape juice concentrate prevents oxidative DNA damage in peripheral blood cells of rats subjected to a high-cholesterol diet. Br J Nutr 105:694–702
Ajuwon OR, Katengua-Thamahane E, Rooyen JV, Oguntibeju OO, Marnewick JL (2013) Protective effects of Rooibos (Aspalathus linearis) and/or Red palm oil (Elaeis guineensis) supplementation on tert-butyl Hydroperoxide-induced oxidative hepatoxicity in wistar rats. Evid Based Complement Alternat Med, in press
Almeida TMB, Leitão RC, Andrade JD, Beçak W, Carrilho FJ, Sonohara S (2004) Detection of micronuclei formation and nuclear anomalies in regenerative nodules of human cirrhotic livers and relationship to hepatocellular carcinoma. Cancer Genet Cytogenet 150:16–21
Bakare AA, Patel S, Pandey AK, Bajpayee M, Dhawan A (2012) DNA and oxidative damage induced in somatic organs and tissues of mouse by municipal sludge leachate. Toxicol and Industrial Health 28(7):614–623
Bartolotta SA, Pacskowski MG, Hick A, Carballo MA (2011) Micronuclei assay in exfoliated buccal cells from individuals exposed to arsenic in Argentina. Arch Environ Contam Toxicol 61(2):337–343
Blanchard M, Teil MJ, Ollivon D, Lengeti L, Chevreuil M (2004) Polycyclic aromatic hydrocarbons and polychlorobiphenyls in wastewaters and sewage sludge from the Paris area (France). Environ Res 95:184–197
Cesar A, Choueri RB, Riba I, Morales-Caselles C, Pereira CDS, Santos AR, Abessa DMS, Del Valls TA (2007) Comparative sediment quality assessment in different littoral ecosystems from Spain (Gulf of Cadiz) and Brazil (Santos and Sao Vicente estuarine system). Environ Int 33:429–435
CETESB Relatório de qualidade das águas litorâneas no Estado de São Paulo. Balneabilidade das praias 2004 capítulo 4. Avaliable in http://www.cetesb.sp.gov.br. Acessed in 15/06/2013
Chandra S, Chauhan LK, Murthy RC, Gupta SK (2006) In vivo genotoxicity effects of industrial waste leachates in mice following oral exposure. Environ Mol Mutagen 47(5):325–333
Colman BP, Arnaout CL, Anciaux S, Gunsch CK, Hochella Jr MF, Kim B, Lowry GV, McGill BM, Reinsch BC, Richardson CJ, Unrine JM, Yin Liyan, Bernhardt ES (2014) Low concentrations of silver nanoparticles in biosolids cause adverse ecosystem responses under realistic field scenario. Plos One, in press
CONAMA (Conselho Nacional de Meio-Ambiente) (2005) Ministerio do Meio-Ambiente, Brasil. Resolution nº 357
CONAMA (Conselho Nacional de Meio-Ambiente) (2011) Ministerio do Meio-Ambiente, Brasil. Resolution nº 430
Farombi EO, Akintude JK, Nzute N, Adedara IA, Arojojoye O (2011) Municipal landfill leachate induces hepatotoxicity and oxidative stress in rats. Toxicol Ind Health 28(6):532–541
Goldsworthy TL, Fransson-Steen R, Maronpot RR (1996) Importance of and approaches to quantification of hepatocytes apoptosis. Toxicol Pathol 24(1):24–35
Grigoletto JC, Segura-Muñoz SI, Barbosa-Junior F, Sanches SM, Takayanagui AM (2011) Silver discharged in effluents from image-processing services: a risk to human and environmental health. Biol Trace Elem Res 144(1–3):316–326
Guzman P, Sotelo-Regil RC, Mohar A, Gonsebatt ME (2003) Positive correlation between the frequency of micronucleated cells and dysplasia in Papanicolaou smears. Environ Mol Mutagen 41(5):339–343
Harrison EZ, Oakes SR, Hysell M, Hay A (2006) Organic chemicals in sewage sludge. Sci Total Environ 367:481–497
Hou L, Zhang X, Wang D, Pereira MA, Kramer PM, Conran PB, Tao L (2011) Effect of chloroform on dichloroacetic and trichloroacetic acid-induced hypomethylation and expression of the c-myc gene and on their promotion of liver and kidney tumors in mice. Carcinogenesis 22(9):1511–1519
Jia P, Teng J, Zou J, Fang Y, Jiang S, Yu X, Kriegel AJ, Liang M, Ding X (2013) Intermittent exposure to xenón protects against gentamicin-induced nephrotoxicity. Plos One 8(5):e64329
Ju JH, Lee IS, Sim WJ, Eun H, Oh JE (2009) Analysis and evaluation of chlorinated persistent organic compounds and PAHs in sludge in Korea. Chemosphere 74:441–447
Kerwin JL, Wiens AM, Ericsson LHJ (1996) Identification of fatty acids by electroscopy mass spectrometry and tandem mass sprectrometry. J Mass Spectrom 31(2):184–192
Krishna G, Hayashi M (2000) In vivo rodent micronucleus assay: protocol, conduct and data interpretation. Mut Res 455:155–166
Lamparelli CC (2006) Desafios para o licenciamento e monitoramento ambiental de emissários a experiência de são Paulo. In: emissários submarinos projetos avaliações de impacto ambiental e monitoramento. São Paulo. SMA
Leite GS, Afonso RJCF, Aquino SF (2010) Caracterização de contaminantes presentes em sistemas de tratamento de esgoto por cromatografia líquida acoplada à espectrometria de massa tandem em alta resolução. Quim Nova 33(3):734–738
Lewis MA (1991) Chronic and sublethal toxicities of surfactants to aquatic animals: a review and risk assessment. Wat Res 25(1):101–113
Li G, Sang N, Zhao Y (2004) Micronuclei induced by municipal landfill leachate in mouse bone marrow cells in vivo. Environ Res 95:77–81
Li G, Sang N, Guo D (2006) Oxidative damage induced in hearts, kidneys and spleens of mice by landfill leachate. Chemosphere 65:1058–1063
Lindahl T, Wood RD (1999) Quality control by DNA repair. Science 286(5446):1897–1905
Lombi E, Donni E, Taheri S, Tavakkoli E, Jamting AK, McClure S, Naidu R, Miller BW, Scheckel KG, Vasilev K (2013) Transformation of four silver/silver chloride nanoparticle during anaerobic treatment of wastewater and post-processing of sewage sludge. Env Pol 176:193–197
Lundin C, North M, Erixon K, Walters K, Jenssen D, Goldman AS, Helleday T (2005) Methyl methanesulfonate (MMS) produces heat-labile DNA damage but no detectable in vivo DNA double-strand breaks. Nucleic Acids Res 33(12):3799–81
Luvizutto JFL, Solano MLM, Passareli D, Franchi CAS, Umbuzeiro GA, Camargo JLV (2010) Subchronic toxicity evaluation of a treated urban sewage sludge. J Toxicol Environ Health 73:916–925
Mally A, Chipman JK (2002) Non-genotoxic carcinogens: early effects on gap junctions, cell proliferations and apoptosis in the rat. Toxicology 180:233–248
Mandaji D (2008) Emissário submarino de Santos: Contribuição para sedimentos de fundo: Sedimentos metálicos. Dissertation, University of Sao Paulo
Mantis I, Voutsa D, Samara C (2005) Assessment of the environment hazard from municipal and industrial wastewater treatment sludge by employing chemical and biological methods. Eco Env 62:397–407
Maronpot RR, Yoshizawa K, Nyska A, Harada T, Flake G, Mueller G, Singh B, Ward JM (2010) Hepatic enzyme induction: histopathology. Toxicol Pathol 38:776–795
Martins CC, Bicego MC, Mahiques MM, Figueira RCL, Tessler MG, Montone RC (2011) Polycyclic aromatic hydrocarbons (PAHs) in a large South America industrial coastal area (Santos Estuary, Southeastern Brazil): sources and depositional history. Mar Poll Bull 63:452–458
Molina FD, Bertollo EM, Assis CM, Falleiros LR Jr, Campos SG, Maniglia JV, Taboga SR (2008) Apoptosis in tongue squamous cell carcinoma and its correlation with clinically occult cervical metastasis. Micron 39(7):910–914
Nohynek GJ, Dufour EK (2012) Nano-sized cosmetic formulations or solid nanoparticles in sunscreens: a risk for human health? Arch Toxicol 86:1063–1107
Ong TP, Heidor R, de Conti A, Dagli MLZ, Moreno FS (2006) Farnesol and geraniol chemopreventive activities during the inicial phases of hepatocarcinogenesis involve similar actions on cell proliferation and DNA damage, but distinct actions on apoptosis, plasma cholesterol and HMGCoA redutase. Carcinogenesis 27(6):1194–1203
Penteado JCP, Osmar A, Carvalho LRF (2006) Alquilbenzeno sulfonato linear: uma abordagem ambiental e analíca. Quim Nova 29(5):1038–1046
Pereira AM, Kramer PM, Conran PB, Tao L (2001) Effect of chloroform on dichloroacetic acid and trichloroacetic acid-induced hypomethylation and expression of the c-myc gene on their promotion of liver and kidney tumours in mice. Carcinogenesis 22(9):1511–1519
Pereira CDS, Martin-Diaz ML, Zanette J, Cesar A, Choueri RB, Abessa DMS, Catharino MGM, Vasconcellos MBA, Bainy ACD, Sousa ECPM, Valls TAD (2011) Integrated biomarker responses as environmental status descriptors of a coastal zone (Sao Paulo, Brazil). Ecotoxicol Environ Saf 74:1257–1264
Ribeiro DA, Marques MEA, Salvadori DMF (2006) Antimicrobial endodontic compounds do not modulate alkylation-induced genotoxicity and oxidative stress in vitro. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 102:e32–e36
Sang N, Li G (2005) Chromosomal aberrations induced in mouse bone marrow cells by municipal landfill leachate. Environ Toxicol Pharm 20:219–224
SEADE. Sao Paulo State. Secretaria de planejamento e desenvolvimento regional [internet] in: http://www.seade.gov.br/produtos/perfil/perfilMunEstado.php. Acessed 13 Feb 2014
Silva PRP, Barbisan LF, Dagli MLZ, Saldiva PHN (2012) Sewage sludge does not induce genotoxicity and carcinogenesis. Genet Mol Biol 35(3):657–663
Smith AH, Hopenhayn-Rich C, Warner M, Biggs ML, Moore L, Smith MT (1993) Rationale for selecting exfoliated bladder cell micronuclei as potential biomarkers for arsenic genotoxicity. J Toxicol Environ Health 40:223–234
Solano MLM, Lima PLA, Luvizutto JFL, Silva PRP, Umbuzeiro GA, Camargo JLV (2009) In vivo genotoxicity evaluation of a treated urban sewage sludge sample. Mut Res 676:69–73
Subtil EL, Mierzwa JC, Ortiz JP, Garcia RS, Garcia A, Alba JG (2012) Environmental response of wastewater inputs through SSO (Santos submarine outfall) utilizing an eutrophication numerical model. J Ship Ocen Eng 2:68–75
Sugano N, Minegish T, Kawamoto K, Ito K (2001) Nicotine inhibits UV-induced activation of the apoptotic pathway. Toxicol Lett 125:61–65
Swenberg JA (1993) Cell proliferation and chemical carcinogenesis: summary and future directions. Environ Health Perspect 101(Suppl 5):153–158
Tewari A, Chauhan LKS, Kumar D, Gupta SK (2005) Municipal leachate-induced genotoxicity in mice—a subacute study. Mutat Res 587:9–15
Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu J-C, Sasaki YF (2000) Single cell gel/comet assay: guideline for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35:206–221
Tran NH, Hu J, Li J, Ong SL (2014) Suitability of artificial sweeteners as indicator of raw wastewater contamination in surface water and underground. Wat res 48:443–456
Warne MSJ, Schifko AD (1999) Toxicity of laundry detergent components to a freshwater cladoceran and their contribution to detergent toxicity. Ecotoxicol Environ Saf 44:196–206
Zhang W, Liu W, Zhang J, Zhao H, Zhang Y, Quan X, Jin Y (2012) Characterisation of acute toxicity, genotoxicity and oxidative stress posed by textile effluent on zebrafish. J Environ Sci 24(11):2019–2027
Zhang J, Zhang Y, Liu W, Quan X (2013) Evaluation of removal effiency for acute toxicity and genotoxicty on zebrafish in anoxicoxic process from selected municipal wastewater treatment plants. Chemosphere 90:2662–2666
Zuloaga O, Navarro P, Bizkarguenaga E, Iparraguirre A, Vallejo A, Olivares M, Prieto A (2012) Overview of extraction, clean-up and detection techniques for the determination of organic pollutants in sewage sludge: a review. Anal Chim Acta 736:7–29
Acknowledgements
This work was supported by CNPq (National Counsel of Technological and Scientific Development). AC, CFGM, WV, and DAR are fellowships from CNPq. VHPS is a recipient form CAPES (Coordination for the Improvement of Higher Level—or Education—Personnel).
Conflict of interest
The authors declare that there are no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
da Silva, V.H.P., de Moura, C.F.G., Ribeiro, F.A.P. et al. Genotoxicity and cytotoxicity induced by municipal effluent in multiple organs of Wistar rats. Environ Sci Pollut Res 21, 13069–13080 (2014). https://doi.org/10.1007/s11356-014-3261-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-014-3261-5