Skip to main content
Log in

Mucociliary transport, differential white blood cells, and cyto-genotoxicity in peripheral erythrocytes in fish from a polluted urban pond

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The present study evaluated the water quality of a polluted pond through the analysis of in vitro mucociliary transport, hematological parameters, and biomarkers of cyto-genotoxicity in the Nile tilapia (Oreochromis niloticus). Blood and mucus samples were collected from ten specimens from the polluted pond and from ten specimens from a control area. The fish were anesthetized with 3% benzocaine, mucus was collected directly from the gills, and blood was drawn from the caudal artery. Blood smears were stained using the May-Grünwald Giemsa process for the differential leukocyte counts and to determine the frequency of leukocytes, thrombocytes, erythroblasts, micronuclei, and nuclear abnormalities. The results revealed low transportability in vitro, a high percentage of monocytes and eosinophils, and increased frequency of leukocytes and nuclear abnormalities in fish from the polluted pond. However, the frequency of thrombocytes and erythroblasts and the percentage of lymphocytes and neutrophils were significantly lower. It is possible to conclude that changes in fish are due to poor water quality and that these non-destructive biomarkers can be used for the biomonitoring of aquatic environments vulnerable to contamination.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • APHA (American Public Health Association) (2005) AWWA American Water Works Association WPCF-Water Pollution Control Federation, 21st edn. Standard Methods for the Examination of Water and Wastewater, Washington, DC

    Google Scholar 

  • Araújo ALS, Guimarães ET, Seriani R (2014) Mutagenesis in Tradescantia pallida as a biomarker of the effects of water polluted with urban effluent. Holos Environ 14(1):97–102. 10.14295/holos.v14i1.6911

    Article  Google Scholar 

  • Arkoosh M, Casillas E, Clemons E, Huffman P, Kagley A, Collier T, Stein J (2000) Increased susceptibility of juvenile chinook salmon to infectious disease after exposure to chlorinated and aromatic compounds found in contaminated urban estuaries. Mar Environ Res 50(1):470–471. https://doi.org/10.1016/S0141-1136(00)00225-7

    Article  Google Scholar 

  • Bacchett C, Cazenave J, Parma MJ (2011) Responses of biochemical markers in the fish Prochilodus lineatus exposed to a commercial formulation of endosulfan. Water Air Soil Pollut 216(1–4):39–49. https://doi.org/10.1007/s11270-010-0512-z

    Article  Google Scholar 

  • Beamish RJ (1972) Lethal pH for the white sucker Catostomus commersoni (Lacepede). Trans Am Fish Soc 101(2):355–358. https://doi.org/10.1577/1548-8659(1972)101<355:LPFTWS>2.0.CO;2

    Article  Google Scholar 

  • Bonnail E, Buruaem LM, Araujo GS, Abessa DM, Del Valls TA (2016) Multiple biomarker responses in Corbicula fluminea exposed to copper in laboratory toxicity tests. Arch Environ Contam Toxicol 2(71):278–285

    Article  Google Scholar 

  • Bucker A, Carvalho M, Conceição M, Alves-Gomes J (2012) Micronucleus test and comet assay in erythrocytes of the Amazonian electric fish Apteronotus bonapartii exposed to benzene. Ecotoxicol Environ Cont 7(1):65–73

    Google Scholar 

  • Carraschi SP, Florêncio T, Ignácio NF, Ikefuti CV, Cruz C, Ranzani-Paiva MJT (2016) Hematological and histopathological assessment of pacu (Piaractus mesopotamicus) after treatment of pathogens with veterinary medicinal products. Comp Clin Path 1(26):105–114

    Google Scholar 

  • Çavaş T (2008) In vivo genotoxicity of mercury chloride and lead acetate: micronucleus test on acridine orange stained fish cells. Food and Chem Toxicology 46(1):352–358

    Article  Google Scholar 

  • Çavas T, Ergene-Gözükara S (2005) Micronucleus test in fish cells: a bioassay for in situ monitoring of genotoxic pollution in the marine environment. Environ Mol Mut 46(1):64–70. https://doi.org/10.1002/em.20130

    Article  Google Scholar 

  • CETESB (Companhia Ambiental do Estado de São Paulo) (2009) Qualidade das águas interiores no Estado De São Paulo. Significado ambiental e sanitário das variáveis de qualidade das águas e dos sedimentos e metodologias analíticas e de amostragem. Serie Relatorios Apendice A. In: http://www.cetesb.sp.gov.br/

  • Clauss TM, Dove ADM, Arnold JE (2008) Hematologic disorder of fish. Vet Clin North Am Exot Anim Pract 11(3):445–462. https://doi.org/10.1016/j.cvex.2008.03.007

    Article  Google Scholar 

  • CONAMA (Conselho Nacional do Meio Ambiente) (2005) Dispõe sobre a classificação dos corpos de água e diretrizes ambientais para o seu enquadramento, bem como estabelece as condições e padrões de lançamento de efluentes, e da outras providencias. In: http://www.mma.gov.br/port/conama/legiabre.cfm?codlegi=459

  • Corrêa SADS, Abessa DMDS, Santos LGD, Silva EB, Seriani R (2017) Differential blood counting in fish as a non-destructive biomarker of water contamination exposure. Toxicol Environ Chem 99(3):482–491

    Article  Google Scholar 

  • Corredor-Santamaría W, Gómez MS, Velasco-Santamaría YM (2016) Using genotoxic and haematological biomarkers as an evidence of environmental contamination in the Ocoa River native fish, Villavicencio—Meta, Colombia. SpringerPlus 5(1):351. https://doi.org/10.1186/s40064-016-1753-0

    Article  Google Scholar 

  • Cruz AL, Prado TM, Maciel LAS, Couto RD (2015) Environmental effects on the gills and blood of Oreochromis niloticus exposed to rivers of Bahia, Brazil. Ecotoxicol Environ Saf 111:23–31. https://doi.org/10.1016/j.ecoenv.2014.09.022

    Article  CAS  Google Scholar 

  • Delbon MCE, Paiva MJTR (2012) Eugenol em juvenis de tilápia do Nilo: concentrações e administrações sucessivas. Bol Inst Pesca 38(1):43–52

    CAS  Google Scholar 

  • Duarte LFA, Souza CA, Nobre CR, Pereira CDS, Pinheiro MAA (2016) Multi-level biological responses in Ucides cordatus (Linnaeus, 1763) (Brachyura, Ucididae) as indicators of conservation status in mangrove areas from the western atlantic. Ecotoxicol Environ Saf 133:176–187. https://doi.org/10.1016/j.ecoenv.2016.07.018

    Article  CAS  Google Scholar 

  • Esteves FDA (2011) Fundamentos de limnologia, 3rd edn. Editora Interciência, Rio de Janeiro

    Google Scholar 

  • Felipe TRA, Súarez YR (2010) Caracterização e influência dos fatores ambientais nas assembleias de peixes de riachos em duas microbacias urbanas, Alto Rio Paraná. Biota Neotrop 10(2):144–151

    Article  Google Scholar 

  • Flores-Ramírez R, Pérez-Vázquez FJ, Rodríguez-Aguilar M, Medellín-Garibay SE, Brussel E, Cubillas-Tejeda AC, Díaz-Barriga F (2017) Biomonitoring of persistent organic pollutants (POPs) in child populations living near contaminated sites in Mexico. Sci Total Environ 579:1120–1126. https://doi.org/10.1016/j.scitotenv.2016.11.087

    Article  Google Scholar 

  • Fujimoto RY, Costa HC, Ramos FM (2012) Controle alternativo de helmintos de Astyanax cf. zonatus utilizando fitoterapia com sementes de abóbora (Cucurbita maxima) e mamão (Carica papaya). Pesq Vet Bras 32(1):5–10. https://doi.org/10.1590/S0100-736X2012000100002

    Article  Google Scholar 

  • García-Medina S, Razo-Estrada C, Galar-Martinez M, Cortéz-Barberena E, Manuel Gómez-Oliván LM, Álvarez-González I, Madrigal-Bujaidar E (2011) Genotoxic and cytotoxic effects induced by aluminum in the lymphocytes of the common carp (Cyprinus carpio). Comp Biochem Physiol Part C Toxicol Pharmacol 153(1):113–118. https://doi.org/10.1016/j.cbpc.2010.09.005

    Article  Google Scholar 

  • Gianotti EP (1986) Contaminaçäo das águas pelo zinco: a dureza da água como um fator de modificaçäo da toxicidade do zinco a peixes. Rev DAE 46(145):187–193

    Google Scholar 

  • Guardiola FA, Dioguardi M, Parisi MG, Trapani MR, Meseguer J, Cuesta A, Esteban MA (2015) Evaluation of waterborne exposure to heavy metals in innate immune defences present on skin mucus of gilthead seabream (Sparus aurata). Fish Shellfish Immunol 45(1):112–123. https://doi.org/10.1016/j.fsi.2015.02.010

    Article  CAS  Google Scholar 

  • Guardiola FA, Cuesta A, Esteban MA (2016) Using skin mucus to evaluate stress in gilthead seabream (Sparus aurata L.) Fish Shellfish Immunol 59:323–330. https://doi.org/10.1016/j.fsi.2016.11.005

    Article  CAS  Google Scholar 

  • Gupta SK, Pal AK, Sahu NP, Jha AK, Akhtar MS, Mandal SC, Prusty AK (2013) Supplementation of microbial levan in the diet of Cyprinus carpio fry (Linnaeus, 1758) exposed to sublethal toxicity of fipronil: effect on growth and metabolic responses. Fish Physiol Biochem 39(6):1513–1524. https://doi.org/10.1007/s10695-013-9805-7

    Article  CAS  Google Scholar 

  • Hedayati A, Darabitabar F (2017) Lethal and sub-lethal impacts of lead on some hematological, biochemical and immunological indices in Caspian roach (Rutilus rutilus). Pollution 3(1):21–27

    Google Scholar 

  • Javid A, Javed M, Abdullah S (2007) Nickel bio-accumulation in the bodies of Catla catla, Labeo rohita and Cirrhina mrigala during 96-hr LC50 exposures. Int J Agric Biol 9:139–142

    CAS  Google Scholar 

  • Jeney G, Nemcsok J, Jeney ZS, Olah J (1992) Acute effect of sublethal ammonia concentrations on common carp (Cyprinus carpio L.). II effect of ammonia on blood plasma transminases (GOT, GPT), G1DH enzyme activity, and ATP value. Aquaculture 104(1-2):149–156. https://doi.org/10.1016/0044-8486(92)90145-B

    Article  CAS  Google Scholar 

  • Kim AD, Gu MB, Allen HE, Cha D (2001) Physiochemical factors affecting the sensitivity of Ceriodaphnia bulba to copper. Environ Monit Assess 70(1/2):105–116. https://doi.org/10.1023/A:1010689432130

    Article  CAS  Google Scholar 

  • King M (1986) The role of mucus viscoelasticity in cough clearance. Biorheology 24:589–597

    Article  Google Scholar 

  • Kirschbaum AA, Seriani R, Pereira CD, Assunção A, Abessa DM, Rotundo MM, Ranzani-Paiva MJ (2009) Cytogenotoxicity biomarkers in fat snook Centropomus parallelus from Cananéia and São Vicente estuaries, SP, Brazil. Gen. Mol Biol 32(1):151–154

    Google Scholar 

  • Koreleff F (1970) Direct determination of ammonia in natural waters as indophenol blue. Information on techniques and methods for seawater analysis. ICES Interlaboratory Rep 3:19–22

    Google Scholar 

  • Kumar M, Kumar D, Kumar R (2017) Sublethal effects of cadmium and copper on the blood characteristics of catfish Clarias batrachus (Linn.) Int J Adv Res Biol Sci 4(1):123–128. https://doi.org/10.22192/ijarbs.2017.04.01.013

    Article  Google Scholar 

  • Lemly AD (2002) Symptoms and implications of selenium toxicity in fish: the belews lake case example. Aquat Toxicol 57(1):39–49

    Article  CAS  Google Scholar 

  • Lemos M, Lichtenfels AJFC, Amaro E, Macchione M, Martins MA, King M, Bohm GM, Saldiva PHN (1994) Quantitative pathology of nasal passages in rats exposed to urban levels of air pollution. Environ Res 66(1):87–95. https://doi.org/10.1006/enrs.1994.1046

    Article  CAS  Google Scholar 

  • Lichtenfels AJFC, Lorenzi-Filho G, Guimaraes ET, Macchione M, Saldiva PHN (1996) Effects of water pollution on the gill apparatus of fish. J Comp Pathol 115(1):47–60. https://doi.org/10.1016/S0021-9975(96)80027-2

    Article  CAS  Google Scholar 

  • Macchione M, King M, Lorenzi-Filho G, Guimaraes ET, Zin WA, Böhm GM, Saldiva PHN (1995) Rheological determinants of mucociliary transport in the nose of the rat. Resp Physiol 99(1):165–172. https://doi.org/10.1016/0034-5687(94)00080-J

    Article  CAS  Google Scholar 

  • Mazon AF, Monteiro EAS, Pinheiro GHD, Fernandes MN (2002) Hematological and physiological changes induced by short-term exposure to copper in the freshwater fish Prochilodus scrofa. Braz J Biol 62(4A):621–663. https://doi.org/10.1590/S1519-69842002000400010

    Article  CAS  Google Scholar 

  • Molokwu CN, Okpokwasili GC (2002) Effect of water hardness on egg hatchability and larval viability of Clarias gariepinus. Aquacult Int 10(1):57–64. https://doi.org/10.1023/A:1021395122919

    Article  CAS  Google Scholar 

  • Morris JT, Barber DC, Callaway JC, Chambers R, Hagen SC, Hopkinson CS, Wigand C (2016) Contributions of organic and inorganic matter to sediment volume and accretion in tidal wetlands at steady state. Earth’s Future 4(4):110–121. https://doi.org/10.1002/2015EF000334

    Article  Google Scholar 

  • Nicholson LC, Woods LC, Woiwode JG (1990) Intensive culture techniques for the striped bass and its hybrids. In: Harrell RM, Kerby JH, Minton RV (eds) Culture and propagation of striped bass and its hybrids. American Fisheries Society, Bethesda, pp 141–158

    Google Scholar 

  • Northcott ME, Beveridge MCM (1988) The development and structure of pharyngeal apparatus associated with filter feeding in tilapias (Oreochromis niloticus). J Zool 215(1):133–149. https://doi.org/10.1111/j.1469-7998.1988.tb04889.x

    Article  Google Scholar 

  • Passantino L, Cianciotta A, Patruno R, Ribaud MR, Jirillo E, Assantino GF (2005) Do fish thombocytes play an immunological role? Their cytoenzimatic profiles and fuction during an accidental piscine candidiasis in aquarium. Immunopharmcol Immunotoxicol New York 7:345–356

    Article  Google Scholar 

  • Pereira L, Fernandes MN, Martinez CB (2013) Hematological and biochemical alterations in the fish Prochilodus lineatus caused by the herbicide clomazone. Environ Toxicol Pharmacol 36(1):1–8. https://doi.org/10.1016/j.etap.2013.02.019

    Article  CAS  Google Scholar 

  • Pereira CDS, Maranho LA, Cortez FS, Pusceddu FH, Santos AR, Ribeiro DA, Guimarães LL (2016) Occurrence of pharmaceuticals and cocaine in a Brazilian coastal zone. Sci Total Environ 548:148–154

    Article  Google Scholar 

  • Pires-Neto RC, Lichtenfels AJ, Regina Soares S, Macchione M, Saldiva PHN, Dolhnikoff M (2006) Effects of São Paulo air pollution on the upper airways of mice. Environ Res 101(3):356–361. https://doi.org/10.1016/j.envres.2005.12.018

    Article  CAS  Google Scholar 

  • Prado LR, Felix C, Abessa DM, Buruaem LM, Abujamara LD, Kirschbaum AA, Turatti GCR, Ranzani-Paiva MJT, Correia AT, Seriani R (2014) Hematological parameters and nuclear abnormalities in peripheral erythrocytes ofAchirus lineatus (Pleuronectiformes: Achiridae). Comp Clin Pathol 361:1–7

    Google Scholar 

  • Pyle GG, Swanson SM, Lehmkuht DM (2002) The influence of water hardness, pH, and suspended solids on nickel toxicity to larva fathead minnows (Pimephales promelas). Water Air Soil Poll 133(1/4):215–226. https://doi.org/10.1023/A:1012973728628

    Article  CAS  Google Scholar 

  • Rosenfeld G (1947) Corante pancrômico para a hematologia e citologia clínica: nova combinação dos componentes do May-Grünwald e do Giemsa num só corante de emprego rápido. Memórias do Instituto Butantan 20(1):329–334

  • Rothenberg ME, Hogan SP (2006) The eosinophil. An. Rev Immunol 4:147–174

    Article  Google Scholar 

  • Rowley AF (1988) In: Rowley AF, Ratcliffe N (eds) Vertebrate blood cells. Cambridge, Cambridge University, pp 119–127

    Google Scholar 

  • Sadauskas-Henrique H, Duarte RM, Gagnon MM, Almeida-Val VMF (2017) Validation of a suite of biomarkers of fish health in the tropical bioindicator species, tambaqui (Colossoma macropomum). Ecol Indic 73:443–451. https://doi.org/10.1016/j.ecolind.2016.10.010

    Article  CAS  Google Scholar 

  • Saldiva PHN (1990) Aparelho mucociliar: aspectos funcionais e métodos de estudo. J Pneumol 16(3):161–170

    Google Scholar 

  • Seriani R, Ranzani-Paiva MJT, Silva-Souza AT, Napoleão SR (2011) Hematology, micronuclei and nuclear abnormalities in fishes from São Francisco river, Minas Gerais state, Brazil. Acta Scient Biol Sci 33(1):107–112

    Google Scholar 

  • Seriani R, Abessa DMS, Kirschbaum AA, Pereira CDS, Ranzani-Paiva MJT, Assunção A, Silveira FL, Romano P, Mucci JLN (2012a) Water toxicity and cyto-genotoxicity biomarkers in the fish Oreochromis niloticus (Cichlidae). J Braz Soc Ecotoxicol 7(2):67–72. https://doi.org/10.5132/jbse.2012.02.010

    Article  Google Scholar 

  • Seriani R, Abessa DMS, Kirschbaum AA, Pereira CDS, Romano P, Ranzani-Paiva MJT (2012b) Relationship between water toxicity and hematological changes in Oreochromis niloticus. Braz J Aquat Sci Technol 15(2):47–53

    Google Scholar 

  • Seriani R, Abessa DMS, Pereira CD, Kirschbaum AA, Assunção A, Ranzani-Paiva MJT (2013) Influence of seasonality and pollution on the hematological parameters of the estuarine fish Centropomus parallelus. Braz J Ocean 61(2):105–111. https://doi.org/10.1590/S1679-87592013000200003

    Article  Google Scholar 

  • Seriani R, Abessa DMS, Moreira LB, Cabrera JP, Sanches JQ, Silva CL, Amorim FA, Rivero DHRF, Silva FL, Fitorra LS, Carvalho-Oliveira R, Macchione M, Ranzani-Paiva MJT (2015a) In vitro mucus transportability, cytogenotoxicity, and hematological changes as non-destructive physiological biomarkers in fish chronically exposed to metals. Ecotoxicol Environ Saf 112:162–168. https://doi.org/10.1016/j.ecoenv.2014.11.003

    Article  CAS  Google Scholar 

  • Seriani R, Junqueira MS, Toledo AC, Corrêa AT, Silva LF, Martins MA, Saldiva PHS, Macchione M (2015b) Organic and inorganic fractions of diesel exhaust particles produce changes in mucin profile of mouse trachea explants. J Toxicol Environ Health Part A 78(4):215–225. https://doi.org/10.1080/15287394.2014.947456

    Article  CAS  Google Scholar 

  • Seriani R, Junqueira MDS, Toledo AC, Martins MA, Seckler M, Alencar AM, Negri EM, Silva LFF, Maud T, Saldiva PHS, Macchione M (2015c) Diesel exhaust particulates affect cell signaling, mucin profiles, and apoptosis in trachea explants of Balb/C mice. Environ Toxicol 30(11):1297–1308. https://doi.org/10.1002/tox.22000

    Article  CAS  Google Scholar 

  • Seriani R, Junqueira MS, Toledo AC, Corrêa AT, Silva LF, Martins MA, Macchione M (2015d) Organic and inorganic fractions of diesel exhaust particles produce changes in mucin profile of mouse trachea explants. Health, Part A. J Toxicol Environ 78(4):215–225

  • Sibanda T, Selvarajan R, Tekere M (2015) Urban effluent discharges as causes of public and environmental health concerns in South Africa’s aquatic milieu. Environ Sci Poll Res Int 22(23):18301–18317. https://doi.org/10.1007/s11356-015-5416-4

    Article  CAS  Google Scholar 

  • Silva AM, Abessa D, Pamplin PAZ, Bohrer-Morel MB (2017) Ecological risk assessment of a subtropical river influenced by discharges of residues from water and sewage treatment plants. Man Environ Quality An Int J 28(2):156–174

    Article  Google Scholar 

  • Simões LN, Gomide ATM, Almeida-Val VMF, Val AL, Gomes LC (2012) O uso do óleo de cravo como anestésico em juvenis avançados de tilápia do Nilo (Oreochromis niloticus). Acta Sci Anim Sci 34(2):175–181

    Article  Google Scholar 

  • Sinley JR, Goettl JP, Davies PH (1974) The effects of zinc on rainbow trout (Salmo gairdneri) in hard and soft water. Bull Environ Cont Toxicol 12(2):193–201. https://doi.org/10.1007/BF01684960

    Article  CAS  Google Scholar 

  • Sorensen EMB (1991) Metal poising in fish. CRC Press, Boca Ranton

  • Sorensen EM, Bauer TL (1984) A correlation between selenium accumulation in sunfish and changes in condition factor and organ weight. Environ Pollut A Ecol Biol 34(4):357–366. https://doi.org/10.1016/0143-1471(84)90113-2

    Article  CAS  Google Scholar 

  • Sorensen EMB, Harlan CW, Bell JS (1982) Renal changes in selenium-exposed fish. Am J Forensic Med Path 3(2):123–129. https://doi.org/10.1097/00000433-198206000-00007

    Article  CAS  Google Scholar 

  • Svobodova Z, Vykusova B, Machova J (1994) The effects of pollutants on selected haematological and biochemical parameters in fish. In: Muller R, Lloyd R (eds) Sublethal and chronic effects of pollutants on freshwater fish. FAO Fishing News Nooks, Oxford, pp 39–52

    Google Scholar 

  • Thomé RG, Silva PM, Santos HB (2016) Avaliação de genotoxidade da água de um rio urbano utilizando estudo de células sanguíneas de Danio rerio. Conexão Ciência (Online) 11(2):9–16

    Article  Google Scholar 

  • Thummabancha K, Onparn N, Srisapoome P (2016) Analysis of hematologic alterations, immune responses and metallothionein gene expression in Nile tilapia (Oreochromis niloticus) exposed to silver nanoparticles. J Immunotoxicol 13(6):909–917. https://doi.org/10.1080/1547691X.2016.1242673

    Article  CAS  Google Scholar 

  • Trindade SHK, Seriani R, Lorenzi-Filho G, Ferreira de Mello Júnior J, Sennes LU, Saldiva PHN, Macchione M (2018) Effects of organic and inorganic compounds of diesel exhaust particles on the mucociliary epithelium: An experimental study on the frog palate preparation. Ecotoxicology and Environmental Safety 148:608–614. https://doi.org/10.1016/j.ecoenv.2017.10.041

  • Vieira CED, Costa PG, Cabrera LC, Primel EG, Fillmann G, Bianchini A, Martinez CBR (2017) A comparative approach using biomarkers in feral and caged Neotropical fish: implications for biomonitoring freshwater ecosystems in agricultural areas. Sci Total Environ 586:598–609. https://doi.org/10.1016/j.scitotenv.2017.02.026

    Article  CAS  Google Scholar 

  • Weldetinsae A, Dawit M, Getahun A, Patil HS, Alemayehu E, Gizaw M, Abera D (2017) Aneugenicity and clastogenicity in freshwater fish Oreochromis niloticus exposed to incipient safe concentration of tannery effluent. Ecotoxicol Environ Saf 138:98–104. https://doi.org/10.1016/j.ecoenv.2016.10.026

    Article  CAS  Google Scholar 

  • Yoshizaki K, Brito JM, Toledo AC, Nakagawa NK, Piccin VS, Junqueira MS, Negri EM, Carvalho ALN, Ligeiro de Oliveira AP, Tavares de Lima W, Saldiva PHN, Mauad T, Macchione M (2010) Subchronic effects of nasally instilled diesel exhaust particulates on the nasal and airway epithelia in mice. Inhal Toxicol 22(7):610–617. https://doi.org/10.3109/08958371003621633

    Article  CAS  Google Scholar 

  • Yoshizaki K, Brito JM, Silva LF, Lino-dos-Santos-Franco A, Frias DP, Silva RCR, Macchione M (2017) The effects of particulate matter on inflammation of respiratory system: differences between male and female. Sci Total Environ 586:284–295. https://doi.org/10.1016/j.scitotenv.2017.01.221

    Article  CAS  Google Scholar 

  • Zieske JD, Bernstein IA (1982) Modification of cell surface glycoprotein: addition of fucosyl residues during epidermal differentiation. J Cell Biol 95(2):626–631

    Article  CAS  Google Scholar 

  • Zimmermann S, Moreira HLM, Vargas L, Ribeiro RP (2001) Fundamentos da moderna aquicultura. ULBRA, Canoas

    Google Scholar 

  • Zutshi B, Prasad SGR, Nagaraja R (2010) Alteration in hematology of Labeo rohita under stress of pollution from Lakes of Bangalore, Karnataka, India. Environ Monit Assess 168(1): 11–1, 19, DOI: https://doi.org/10.1007/s10661-009-1087-2

Download references

Acknowledgments

The authors would like to thank Dr. Rogerio Pazzeti for providing the frog palate and Dr. Mariângela Macchione for her help during frog palate preparation sampling. The authors are also grateful to Mrs. Sonia A.S. Feliciano and Mr. Guilherme F. Cavalheiro for their assistance in laboratorial procedures and to vivarium technicians Mr. Luiz Afonso, Mr. Davi Francisco, and Mr. Ivandir. D.M.S. Abessa thanks the Brazilian National Council for Scientific and Technological Development (CNPq) for the financial support. The authors would also like to thank Danielle Deremo Cosimo of Superior Translation Services for reviewing the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robson Seriani.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Diane Purchase

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

da Silva, E.B., da Silva Corrêa, S.A., de Souza Abessa, D.M. et al. Mucociliary transport, differential white blood cells, and cyto-genotoxicity in peripheral erythrocytes in fish from a polluted urban pond. Environ Sci Pollut Res 25, 2683–2690 (2018). https://doi.org/10.1007/s11356-017-0729-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-0729-0

Keywords

Navigation