Toxicity Produced by an Industrial Effluent from Mexico on the Common Carp (Cyprinus carpio)

  • Nely San Juan-Reyes
  • Leobardo Manuel Gómez-Oliván
  • Hariz Islas-Flores
  • Marcela Galar-Martínez
  • Sandra García-Medina
  • Ricardo Pérez-Pastén Borja


Pharmaceuticals are a set of chemical substances used in the diagnosis, treatment, and prevention of various diseases. The pharmaceutical industry generates large volumes of wastewater which vary as to characteristics and concentration; these effluents originate mainly as a result of production process and the cleaning of machinery and may contain organic solvents, catalysts, additants, reactants, intermediates, raw materials, and active pharmaceutical ingredients. Pharmaceutical industry emissions are well regulated in general but not in developing countries. Diverse studies have reported on the effects induced by pharmaceuticals on aquatic organisms. The use of cosmopolitan organisms to evaluate contamination has seen a remarkable development in recent years. Cyprinus carpio is used as a bioindicator species, since the cyprinids are quantitatively the most important group of teleost fishes cultured throughout the world for commercial purposes and are also very resistant organisms and easy to maintain. The present study aimed to evaluate the damage induced by an industrial effluent on common carp (Cyprinus carpio). Carp were exposed to the lowest observed adverse effect level (LOAEL, 0.1173%) for 12, 24, 48, 72, and 96 h, and biomarkers of oxidative stress (oxidative damage and activity of antioxidant enzymes), genotoxicity (comet assay and micronucleus test), and cytotoxicity (caspase-3 activity and TUNEL assay) were evaluated. Significant increases with respect to the control group (P < 0.05) were observed in oxidative stress and geno- and cytotoxicity biomarkers in C. carpio.


Toxicity Industrial effluent Damage Pharmaceuticals 


  1. APHA, AWWA, WPCF (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association/American Water Works Association/Water Environment Federation, Washington, DCGoogle Scholar
  2. Azzi A, Davies KJ, Kelly F (2004) Free radical biology–terminology and critical thinking. FEBS Lett 558:3–6CrossRefGoogle Scholar
  3. Baillie TA (2006) Future of toxicology metabolic activation and drug design: challenges and opportunities in chemical toxicology. Chem Res Toxicol 19:889–893CrossRefGoogle Scholar
  4. Bandala E, Espinosa M, Maldonado V, Meléndez-Zajgla J (2001) Inhibitor of apoptosis-1 (IAP-1) expression and apoptosis in non-small-cell lung cancer cells exposed to gemcitabine. Biochem Pharmacol 62:13–19CrossRefGoogle Scholar
  5. Beedanagari S, Vulimiri SV, Bhatia S, Mahadevan B (2014) Genotoxicity biomarkers: molecular basis of genetic variability and susceptibility. In: Gupta RC (ed) Biomarkers in toxicology, pp 729–742. Academic PressGoogle Scholar
  6. Blanco G, Martínez C, García-Martín E, Agúndez JA (2005) Cytochrome P450 gene polymorphisms and variability in response to NSAIDs. Clin Res Regul Aff 22:57–81CrossRefGoogle Scholar
  7. Bolognesi C, Cirillo S (2014) Genotoxicity biomarkers in aquatic bioindicators. Zoology 60:273–284Google Scholar
  8. Bolognesi C, Perrone E, Roggieri P, Pampanin DM, Sciutto A (2006) Assessment of micronuclei induction in peripheral erythrocytes of fish exposed to xenobiotics under controlled conditions. Aquat Toxicol 78:S93–S98CrossRefPubMedPubMedCentralGoogle Scholar
  9. Büege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310CrossRefPubMedPubMedCentralGoogle Scholar
  10. Burcham PC (2007) Modified protein carbonyl assay detects oxidised membrane proteins: a new tool for assessing drug- and chemically-induced oxidative cell injury. J Pharmacol Toxicol Methods 56:18–22CrossRefPubMedPubMedCentralGoogle Scholar
  11. Caminada D, Escher C, Fent K (2006) Cytotoxicity of pharmaceuticals found in aquatic systems: comparison of PLHC-1 and RTG-2 fish cell lines. Aquat Toxicol 79:114–123CrossRefPubMedPubMedCentralGoogle Scholar
  12. Canistro D, Melega S, Ranieri D, Sapone A, Gustavino B, Monfrinotti M, Rizzoni M, Paolini M (2012) Modulation of cytochrome P450 and induction of DNA damage in Cyprinus carpio exposed in situ to surface water treated with chlorine or alternative disinfectants in different seasons. Mutat Res Fundam Mol Mech Mutagen 729:81–89CrossRefGoogle Scholar
  13. Cao Y, Pearman AT, Zimmerman GA, McIntyre TM, Prescott SM (2000) Intracellular unesterified arachidonic acid signals apoptosis. Proc Natl Acad Sci 97:11280–11285CrossRefPubMedPubMedCentralGoogle Scholar
  14. Caracciolo AB, Topp E, Grenni P (2015) Pharmaceuticals in the environment: biodegradation and effects on natural microbial communities. A review. J Pharm Biomed Anal 106:25–36CrossRefGoogle Scholar
  15. Çavaş T, Ergene-Gözükara S (2005) Induction of micronuclei and nuclear abnormalities in Oreochromis niloticus following exposure to petroleum refinery and chromium processing plant effluents. Aquat Toxicol 74:264–271CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chan TA, Morin PJ, Vogelstein B, Kinzler KW (1998) Mechanisms underlying nonsteroidal antiinflammatory drug-mediated apoptosis. Proc Natl Acad Sci 95:681–686CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cycoń M, Borymski S, Żołnierczyk B, Piotrowska-Seget Z (2016) Variable effects of non-steroidal anti-inflammatory drugs (NSAIDs) on selected biochemical processes mediated by soil microorganisms. Front Microbiol 7:1969PubMedPubMedCentralGoogle Scholar
  18. Danial NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell 116:205–219CrossRefPubMedPubMedCentralGoogle Scholar
  19. de Lemos CT, Rödel PM, Terra NR, de Oliveira NCDA, Erdtmann B (2007) River water genotoxicity evaluation using micronucleus assay in fish erythrocytes. Ecotoxicol Environ Saf 66:391–401CrossRefGoogle Scholar
  20. Dennery PA (2007) Effects of oxidative stress on embryonic development. Birth Defects Res C Embryo Today 81:155–162CrossRefPubMedPubMedCentralGoogle Scholar
  21. Díaz-Torres E, Gibson R, González-Farías F, Zarco-Arista AE, Mazari-Hiriart M (2013) Endocrine disruptors in the Xochimilco wetland, Mexico City. Water Air Soil Pollut 224:1586CrossRefGoogle Scholar
  22. Doi H, Iwasaki H, Masubuchi Y, Nishigaki R, Horie T (2002) Chemiluminescence associated with the oxidative metabolism of salicylic acid in rat liver microsomes. Chem Biol Interact 140:109–119CrossRefPubMedPubMedCentralGoogle Scholar
  23. Félix-Cañedo TE, Durán-Álvarez JC, Jiménez-Cisneros B (2013) The occurrence and distribution of a group of organic micropollutants in Mexico City’s water sources. Sci Total Environ 454:109–118CrossRefPubMedPubMedCentralGoogle Scholar
  24. Galar-Martínez M, García-Medina S, Gómez-Olivan LM, Pérez-Coyotl I, Mendoza-Monroy DJ, Arrazola-Morgain RE (2016) Oxidative stress and genotoxicity induced by ketorolac on the common carp Cyprinus carpio. Environ Toxicol 31:1035–1043CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493–501CrossRefGoogle Scholar
  26. Gibson R, Durán-Álvarez JC, Estrada KL, Chávez A, Cisneros BJ (2010) Accumulation and leaching potential of some pharmaceuticals and potential endocrine disruptors in soils irrigated with wastewater in the Tula Valley, Mexico. Chemosphere 81:1437–1445CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gómez-Oliván LM, Neri-Cruz N, Galar-Martínez M, Vieyra-Reyes P, García-Medina S, Razo-Estrada C, Dublán-García O, Corral-Avitia AY (2012) Assessing the oxidative stress induced by paracetamol spiked in artificial sediment on Hyalella azteca. Water Air Soil Pollut 223:5097–5104CrossRefGoogle Scholar
  28. Gómez-Oliván LM, Galar-Martinez M, García-Medina S, Valdés-Alanís A, Islas-Flores H, Neri-Cruz N (2014a) Genotoxic response and oxidative stress induced by diclofenac, ibuprofen and naproxen in Daphnia magna. Drug Chem Toxicol 37:391–399CrossRefPubMedPubMedCentralGoogle Scholar
  29. Gómez-Oliván LM, Galar-Martínez M, Islas-Flores H, García-Medina S, SanJuan-Reyes N (2014b) DNA damage and oxidative stress induced by acetylsalicylic acid in Daphnia magna. Comp Biochem Physiol C Toxicol Pharmacol 164:21–26CrossRefPubMedPubMedCentralGoogle Scholar
  30. Gómez-Oliván LM, Neri-Cruz N, Galar-Martínez M, Islas-Flores H, García-Medina S (2014c) Binary mixtures of diclofenac with paracetamol, ibuprofen, naproxen, and acetylsalicylic acid and these pharmaceuticals in isolated form induce oxidative stress on Hyalella azteca. Environ Monit Assess 186:7259–7271CrossRefPubMedPubMedCentralGoogle Scholar
  31. González-González ED, Gómez-Oliván LM, Galar-Martínez M, Vieyra-Reyes P, Islas-Flores H, García-Medina S, Jiménez-Vargas JM, Razo-Estrada C, Pérez-Pastén R (2014) Metals and nonsteroidal anti-inflammatory pharmaceuticals drugs present in water from Madín Reservoir (Mexico) induce oxidative stress in gill, blood, and muscle of common carp (Cyprinus carpio). Arch Environ Contam Toxicol 67:281–295CrossRefPubMedPubMedCentralGoogle Scholar
  32. Gonzalez-Rey M, Bebianno MJ (2011) Non-steroidal anti-inflammatory drug (NSAID) ibuprofen distresses antioxidant defense system in mussel Mytilus galloprovincialis gills. Aquat Toxicol 105:264–269CrossRefGoogle Scholar
  33. Guengerich FP (2007) Cytochrome p450 and chemical toxicology. Chem Res Toxicol 21:70–83CrossRefGoogle Scholar
  34. Gunzler W, Flohe-Clairborne A (1985) Glutathione peroxidase. In: Green-Wald RA (ed) Handbook of methods for oxygen radical research. CRC Press, Boca Raton, pp 285–290Google Scholar
  35. Gustavino B, Scornajenghi KA, Minissi S, Ciccotti E (2001) Micronuclei induced in erythrocytes of Cyprinus carpio (teleostei, pisces) by X-rays and colchicine. Mutat Res Genet Toxicol Environ Mutagen 494:151–159CrossRefGoogle Scholar
  36. Halliwell B (1997) Antioxidants and human disease: a general introduction. Nutr Rev 55:S44–S49CrossRefGoogle Scholar
  37. Hannun YA (1996) Functions of ceramide in coordinating cellular responses to stress. Science 274:1855–1859CrossRefGoogle Scholar
  38. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770CrossRefGoogle Scholar
  39. Islas-Flores H, Gómez-Oliván LM, Galar-Martínez M, Colín-Cruz A, Neri-Cruz N, García-Medina S (2013) Diclofenac-induced oxidative stress in brain, liver, gill and blood of common carp (Cyprinus carpio). Ecotoxicol Environ Saf 92:32–38CrossRefPubMedPubMedCentralGoogle Scholar
  40. Islas-Flores H, Gómez-Oliván LM, Galar-Martínez M, García-Medina S, Neri-Cruz N, Dublán-García O (2014) Effect of ibuprofen exposure on blood, gill, liver, and brain on common carp (Cyprinus carpio) using oxidative stress biomarkers. Environ Sci Pollut Res 21:5157–5166CrossRefGoogle Scholar
  41. Islas-Flores H, Gómez-Oliván LM, Galar-Martínez M, Sánchez-Ocampo EM, SanJuan-Reyes N, Ortíz-Reynoso M, Dublán-García O (2017) Cyto-genotoxicity and oxidative stress in common carp (Cyprinus carpio) exposed to a mixture of ibuprofen and diclofenac. Environ Toxicol 32:1637–1650CrossRefPubMedPubMedCentralGoogle Scholar
  42. Jiang ZY, Hunt JV, Wolff SP (1992) Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein. Anal Biochem 202:384–389CrossRefPubMedPubMedCentralGoogle Scholar
  43. Jiang C, Geng J, Hu H, Ma H, Gao X, Ren H (2017) Impact of selected non-steroidal anti-inflammatory pharmaceuticals on microbial community assembly and activity in sequencing batch reactors. PLoS One 12:e0179236CrossRefPubMedPubMedCentralGoogle Scholar
  44. Jifa W, Yu Z, Xiuxian S, You W (2006) Response of integrated biomarkers of fish (Lateolabrax japonicus) exposed to benzo [a] pyrene and sodium dodecylbenzene sulfonate. Ecotoxicol Environ Saf 65:230–236CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kim IY, Hyun CK (2006) Comparative evaluation of the alkaline comet assay with the micronucleus test for genotoxicity monitoring using aquatic organisms. Ecotoxicol Environ Saf 64:288–297CrossRefPubMedPubMedCentralGoogle Scholar
  46. Kryston TB, Georgiev AB, Pissis P, Georgakilas AG (2011) Role of oxidative stress and DNA damage in human carcinogenesis. Mutat Res Fundam Mol Mech Mutagen 711:193–201CrossRefGoogle Scholar
  47. Kurokawa M, Kornbluth S (2009) Caspases and kinases in a death grip. Cell 138:838–854CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kylarová D, Procházková J, Mad'arová J, Bartoš J, Lichnovský V (2002) Comparison of the TUNEL, lamin B and annexin V methods for the detection of apoptosis by flow cytometry. Acta Histochem 104:367–370CrossRefPubMedPubMedCentralGoogle Scholar
  49. Lawen A (2003) Apoptosis—an introduction. BioEssays 25:888–896CrossRefPubMedPubMedCentralGoogle Scholar
  50. Levine RL, Williams JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357CrossRefPubMedPubMedCentralGoogle Scholar
  51. Lillenberg M, Yurchenko S, Kipper K, Herodes K, Pihl V, Lõhmus R, Ivask M, Kuu A, Kutti S, Litvin SV, Nei L (2010) Presence of fluoroquinolones and sulfonamides in urban sewage sludge and their degradation as a result of composting. Int J Environ Sci Technol 7:307–312CrossRefGoogle Scholar
  52. Luja-Mondragón M, Gómez-Oliván LM, SanJuan-Reyes N, Islas-Flores H, Orozco-Hernández JM, Heredia-García G, Galar-Martínez M, Dublán-García O (2019) Alterations to embryonic development and teratogenic effects induced by a hospital effluent on Cyprinus carpio oocytes. Sci Total Environ 660:751–764CrossRefPubMedPubMedCentralGoogle Scholar
  53. Matozzo V, Rova S, Marin MG (2012) The nonsteroidal anti-inflammatory drug, ibuprofen, affects the immune parameters in the clam Ruditapes philippinarum. Mar Environ Res 79:116–121CrossRefPubMedPubMedCentralGoogle Scholar
  54. Medeiros MHG (2008) DNA damage. In: Konigsberg-Fainstein M (ed) Free radicals and oxidative stress, pp 122–124. Medical Applications. Manual ModernoGoogle Scholar
  55. Minissi S, Ciccotti E, Rizzoni M (1996) Micronucleus test in erythrocytes of Barbus plebejus (Teleostei, Pisces) from two natural environments: a bioassay for the in situ detection of mutagens in freshwater. Mutat Res Genet Toxicol 367:245–251CrossRefGoogle Scholar
  56. Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175PubMedPubMedCentralGoogle Scholar
  57. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J (2000) Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-β. Nature 403:98CrossRefPubMedPubMedCentralGoogle Scholar
  58. Nava-Álvarez R, Razo-Estrada AC, García-Medina S, Gómez-Olivan LM, Galar-Martinez M (2014) Oxidative stress induced by mixture of diclofenac and acetaminophen on common carp (Cyprinus carpio). Water Air Soil Pollut 225:1873CrossRefGoogle Scholar
  59. Nelson DR (2004) Cytochrome P450 nomenclature, 2004. In: Cytochrome P450 protocols. Humana Press, Totowa, pp 1–10Google Scholar
  60. Neri-Cruz N, Gómez-Oliván LM, Galar-Martínez M, Romero-Figueroa MS, Islas-Flores H, García-Medina S, Jiménez-Vargas JM, SanJuan-Reyes N (2014) Oxidative stress in Cyprinus carpio induced by hospital wastewater in Mexico. Ecotoxicology 24:181–193CrossRefPubMedPubMedCentralGoogle Scholar
  61. NMX-AA-003-1980 (1980) Wastewater, sampling. Procuraduría Federal de Protección al Ambiente. Diario Oficial de la Federación (25 Mar)Google Scholar
  62. NOM-001-SEMARNAT-1996 (1996) Official Mexican norm setting the maximum permissible limits of contaminants in wastewaster discharges entering national waters and resources. Procuraduría Federal de Protección al Ambiente. Diario Oficial de la Federación (30 Oct)Google Scholar
  63. NOM-073-ECOL-1994 (1994) Official Mexican norm setting the maximum permissible limits of contaminants in wastewater discharges arising in the pharmacochemical and pharmaceutical industries and entering receiving water bodies. Secretaría de Desarrollo Social. Diario Oficial de la Federación (10 June)Google Scholar
  64. Oviedo-Gómez DGC, Galar-Martínez M, García-Medina S, Razo-Estrada C, Gómez-Oliván LM (2010) Diclofenac-enriched artificial sediment induces oxidative stress in Hyalella azteca. Environ Toxicol Pharmacol 29:39–43CrossRefPubMedPubMedCentralGoogle Scholar
  65. Parolini M, Binelli A, Cogni D, Riva C, Provini A (2009) An in vitro biomarker approach for the evaluation of the ecotoxicity of non-steroidal anti-inflammatory drugs (NSAIDs). Toxicol In Vitro 23:935–942CrossRefPubMedPubMedCentralGoogle Scholar
  66. Parolini M, Binelli A, Cogni D, Provini A (2010) Multi-biomarker approach for the evaluation of the cyto-genotoxicity of paracetamol on the zebra mussel (Dreissena polymorpha). Chemosphere 79:489–498CrossRefPubMedPubMedCentralGoogle Scholar
  67. Parvez S, Raisuddin S (2005) Protein carbonyls: novel biomarkers of exposure to oxidative stress-inducing pesticides in freshwater fish Channa punctata (Bloch). Environ Toxicol Pharmacol 20:112–117CrossRefPubMedPubMedCentralGoogle Scholar
  68. Pérez-Alvarez I, Islas-Flores H, Gómez-Oliván LM, Barceló D, López De Alda M, Pérez Solsona S, Sánchez-Aceves L, SanJuan-Reyes N, Galar-Martínez M (2018) Determination of metals and pharmaceutical compounds released in hospital wastewater from Toluca, Mexico, and evaluation of their toxic impact. Environ Pollut 240:330–341CrossRefPubMedPubMedCentralGoogle Scholar
  69. Radi R, Turrens JF, Chang LY, Bush KM, Crapo JD, Freeman BA (1991) Detection of catalase in rat heart mitochondria. J Biol Chem 266:22028–22034PubMedPubMedCentralGoogle Scholar
  70. Reed JC, Doctor KS, Godzik A (2004) The domains of apoptosis: a genomics perspective. Sci Signal 2004:re9CrossRefGoogle Scholar
  71. Rehman MSU, Rashid N, Ashfaq M, Saif A, Ahmad N, Han JI (2015) Global risk of pharmaceutical contamination from highly populated developing countries. Chemosphere 138:1045–1055CrossRefGoogle Scholar
  72. Rivera-Jaimes JA, Postigo C, Melgoza-Alemán RM, Aceña J, Barceló D, López De Alda M (2018) Study of pharmaceuticals in surface and wastewater from Cuernavaca, Morelos, Mexico: occurrence and environmental risk assessment. Sci Total Environ 613:1263–1274CrossRefGoogle Scholar
  73. Roos WP, Kaina B (2013) DNA damage-induced cell death: from specific DNA lesions to the DNA damage response and apoptosis. Cancer Lett 332:237–248CrossRefGoogle Scholar
  74. Sali T (2005) Prostaglandins. In: Vohr HW (ed) Encyclopedic reference of immunotoxicology. Springer, Heidelberg, pp 537–540CrossRefGoogle Scholar
  75. SanJuan-Reyes N, Gómez-Oliván LM, Galar-Martínez M, Vieyra-Reyes P, García-Medina S, Islas-Flores H, Neri-Cruz N (2013) Effluent from an NSAID-manufacturing plant in Mexico induces oxidative stress on Cyprinus carpio. Water Air Soil Pollut 224:1689CrossRefGoogle Scholar
  76. SanJuan-Reyes N, Gómez-Oliván LM, Islas-Flores H, Castro-Pastrana LI (2017) Control of environmental pollution caused by pharmaceuticals. In: Ecopharmacovigilance. Springer, Cham, pp 255–264CrossRefGoogle Scholar
  77. Sapone A, Gustavino B, Monfrinotti M, Canistro D, Broccoli M, Pozzetti L, Affatato A, Valgimigli L, Forti GC, Pedulli GF, Biagi GL, Abdel-Rahman SZ, Paolini M (2007) Perturbation of cytochrome P450, generation of oxidative stress and induction of DNA damage in Cyprinus carpio exposed in situ to potable surface water. Mutat Res Genet Toxicol Environ Mutagen 626:143–154CrossRefGoogle Scholar
  78. Saucedo-Vence K, Dublán-García O, López-Martínez LX, Morachis-Valdes G, Galar-Martínez M, Islas-Flores H, Gómez-Oliván LM (2015) Short and long-term exposure to diclofenac alter oxidative stress status in common carp Cyprinus carpio. Ecotoxicology 24:527–539CrossRefPubMedPubMedCentralGoogle Scholar
  79. Scorrano L, Penzo D, Petronilli V, Pagano F, Bernardi P (2001) Arachidonic acid causes cell death through the mitochondrial permeability transition implications for tumor necrosis factor-α apoptotic signaling. J Biol Chem 276:12035–12040CrossRefGoogle Scholar
  80. Sharma K, Kaushik G (2017) NSAIDS in the environment: from emerging problem to green solution. Ann Pharmacol Pharm 2:1077Google Scholar
  81. Siemens J, Huschek G, Siebe C, Kaupenjohann M (2008) Concentrations and mobility of human pharmaceuticals in the world's largest wastewater irrigation system, Mexico City–Mezquital Valley. Water Res 42:2124–2134CrossRefPubMedPubMedCentralGoogle Scholar
  82. Sreekanth D, Sivaramakrishna D, Himabindu V, Anjaneyulu Y (2009) Thermophilic treatment of bulk drug pharmaceutical industrial wastewaters by using hybrid up flow anaerobic sludge blanket reactor. Bioresour Technol 100:2534–2539CrossRefPubMedPubMedCentralGoogle Scholar
  83. Stegeman JJ, Livingstone DR (1998) Forms and functions of cytochrome P450. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 121:1–3CrossRefPubMedPubMedCentralGoogle Scholar
  84. Stephensen E, Svavarsson J, Sturve J, Ericson G, Adolfsson-Erici M, Förlin L (2000) Biochemical indicators of pollution exposure in shorthorn sculpin (Myoxocephalus scorpius), caught in four harbours on the southwest coast of Iceland. Aquat Toxicol 48:431–442CrossRefPubMedPubMedCentralGoogle Scholar
  85. Ternes TA, Joss A, Siegrist H (2004) Peer reviewed: scrutinizing pharmaceuticals and personal care products in wastewater treatment. Environ Sci Technol 38:392A–399ACrossRefPubMedPubMedCentralGoogle Scholar
  86. Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu JC, Sasaki YF (2000) Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35:206–221CrossRefGoogle Scholar
  87. US-EPA (2013) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. U.S. Environmental Protection Agency; Washington, DC, USAGoogle Scholar
  88. Valko M, Izakovic M, Mazur M, Rhodes CJ, Telser J (2004) Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem 266:37–56CrossRefPubMedPubMedCentralGoogle Scholar
  89. Van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149CrossRefPubMedPubMedCentralGoogle Scholar
  90. Vasquez MZ (2012) Recommendations for safety testing with the in vivo comet assay. Mutat Res Genet Toxicol Environ Mutagen 747:142–156CrossRefGoogle Scholar
  91. Velagaleti R, Burns PK (2006) The industrial ecology of pharmaceutical raw materials and finished products with emphasis on supply chain management activities. [cited 25 Jan 2019]. Available from
  92. WHO (1996) Revision of the WHO guidelines for drinking water quality. World Health Organization, GenevaGoogle Scholar
  93. Wilhelm Filho D, Torres MA, Zaniboni-Filho E, Pedrosa RC (2005) Effect of different oxygen tensions on weight gain, feed conversion, and antioxidant status in piapara, Leporinus elongatus (Valenciennes, 1847). Aquaculture 244:349–357CrossRefGoogle Scholar
  94. Wilhelm EA, Jesse CR, Leite MR, Nogueira CW (2009) Studies on preventive effects of diphenyl diselenide on acetaminophen-induced hepatotoxicity in rats. Pathophysiology 16:31–37CrossRefPubMedPubMedCentralGoogle Scholar
  95. Xu J, Zhao Z, Zhang X, Zheng X, Li J, Jiang Y, Kuang Y, Zhang Y, Feng J, Li C, Yu J, Li Q, Zhu Y, Liu Y, Xu P, Sun X (2014) Development and evaluation of the first high-throughput SNP array for common carp (Cyprinus carpio). BMC Genomics 15:307CrossRefPubMedPubMedCentralGoogle Scholar
  96. Zanger UM, Turpeinen M, Klein K, Schwab M (2008) Functional pharmacogenetics/genomics of human cytochromes P450 involved in drug biotransformation. Anal Bioanal Chem 392:1093–1108CrossRefPubMedPubMedCentralGoogle Scholar
  97. Zhang W, Xiao S, Ahn DU (2013) Protein oxidation: basic principles and implications for meat quality. Crit Rev Food Sci Nutr 53:1191–1201CrossRefPubMedPubMedCentralGoogle Scholar
  98. Zhang CZ, Spektor A, Cornils H, Francis JM, Jackson EK, Liu S, Meyerson M, Pellman D (2015) Chromothripsis from DNA damage in micronuclei. Nature 522:179CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Nely San Juan-Reyes
    • 1
    • 2
  • Leobardo Manuel Gómez-Oliván
    • 1
  • Hariz Islas-Flores
    • 1
  • Marcela Galar-Martínez
    • 2
  • Sandra García-Medina
    • 2
  • Ricardo Pérez-Pastén Borja
    • 2
  1. 1.Laboratorio de Toxicología Ambiental, Facultad de Química, Universidad Autónoma del Estado de MéxicoTolucaMexico
  2. 2.Laboratorio de Toxicología Acuática, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Unidad Profesional Adolfo López MateosMexico CityMexico

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