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Environmental Science and Pollution Research

, Volume 25, Issue 9, pp 8592–8607 | Cite as

The exposure to water with cigarette residue changes the anti-predator response in female Swiss albino mice

  • Letícia Silva Cardoso
  • Fernanda Neves Estrela
  • Thales Quintão Chagas
  • Wellington Alves Mizael da Silva
  • Denys Ribeiro de Oliveira Costa
  • Igor Pereira
  • Boniek Gontijo Vaz
  • Aline Sueli de Lima Rodrigues
  • Guilherme MalafaiaEmail author
Research Article

Abstract

Recent studies have shown that cigarette consumption affects much more than human health. Smoked cigarette butt (SCB) disposal into the environment can bring little-known negative biological consequences to mammals, since it contains many organic and inorganic toxic chemical constituents. Thus, we aim at assessing whether the ingestion of water with leached SCB for 60 days by female Swiss mice changes their defensive behavioral response to potential predators (cats and snakes). We worked with the following groups of animals: control (pollutant-free water), water with environmental concentration of SCB (1.9 μg/L of nicotine), and concentration 1000 times higher (EC1000×). Our data show that the treatments did not cause locomotor, visual, auditory, and olfactory deficit in the animals. However, we observed that the animals exposed to the pollutants did not present behavioral differences in the test session with or without the snake. On the other hand, animals in all groups showed defensive behavior when the test was conducted with the cat in the apparatus. However, female mice presented weaker response than the control. Thus, our data point towards the potential neurotoxic damage caused to mice who have ingested water with SCB residues, even at low concentrations.

Keywords

Cigarette Animal behavior Aquatic pollution Mammals Anti-predator responses 

Notes

Acknowledgments

The authors are grateful to the Brazilian National Council for Research (CNPq) (Brazilian research agency) (Proc. No 467801/2014-2) and the Instituto Federal Goiano for the financial support. Moreover, the authors are grateful to the CNPq for supporting scholarship to the students who developed this study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All the procedures were approved by The Ethics Committee on Animal Use of Goiano Federal Institute (Comissão de Ética no Uso de Animais do Instituto Federal Goiano), GO, Brazil (protocol No. 6181130516/2016). Meticulous efforts were made to assure that the animals suffered the least possible and to reduce external sources of stress, pain, and discomfort. The current study did not exceed the number of animals necessary to produce trustworthy scientific data. This article does not contain any studies with human participants performed by any of the authors.

References

  1. Alkhlaif Y, Bagdas D, Jackson A, Park AJ, Damaj IM (2017) Assessment of nicotine withdrawal-induced changes in sucrose preference in mice. Pharmacol Biochem Behav 161:47–52.  https://doi.org/10.1016/j.pbb.2017.08.013 CrossRefGoogle Scholar
  2. Amaral VC, Santos Gomes K, Nunes-de-Souza RL (2010) Increased corticosterone levels in mice subjected to the rat exposure test. Horm Behav 57(2):128–133.  https://doi.org/10.1016/j.yhbeh.2009.09.018 CrossRefGoogle Scholar
  3. American Public Health Association (APHA) (1997) Standard methods for the examination of water and wastewater, 20th edn. New York, APHA, AWWA, WPCR, p 1194Google Scholar
  4. Anisman H, Hayley S, Kelly O, Borowski T, Merali Z (2001) Psychogenic, neurogenic, and systemic stressor effects on plasma corticosterone and behavior: mouse strain dependent outcomes. Behav Neurosci 115(2):443–454.  https://doi.org/10.1037/0735-7044.115.2.443 CrossRefGoogle Scholar
  5. Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29(8):1123–1144.  https://doi.org/10.1016/j.neubiorev.2005.05.005 CrossRefGoogle Scholar
  6. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, Popovich PG (2006) Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 23(5):635–659.  https://doi.org/10.1089/neu.2006.23.635 CrossRefGoogle Scholar
  7. Bekele TT (2016) Investigation of toxicity of cigarette butts collected in Addis Ababa to Swiss albino mice (thesis). Addis Ababa University School of Graduate Studies, Department of Biochemistry, Addis Ababa, EthiopiaGoogle Scholar
  8. Benotti MJ, Brownawell BJ (2007) Distributions of pharmaceuticals in an urban estuary during both dry- and wet-weather conditions. Environ Sci Technol 41(16):5795–5802.  https://doi.org/10.1021/es0629965 CrossRefGoogle Scholar
  9. Berton F, Vogel E, Belzung C (1998) Modulation of mice anxiety in response to cat odor as a consequence of predators diet. Physiol Behav 65(2):247–254.  https://doi.org/10.1016/S0031-9384(98)00126-7 CrossRefGoogle Scholar
  10. Blanchard DC, Blanchard RJ (1988) Ethoexperimental approaches to the biology of emotion. Annu Rev Psychol 39(1):43–68.  https://doi.org/10.1146/annurev.ps.39.020188.000355 CrossRefGoogle Scholar
  11. Blanchard DC, Li CI, Hubbard D, Markham CM, Yang M, Takahashi LK, Blanchard RJ (2003) Dorsal premammillary nucleus differentially modulates defensive behaviors induced by different threat stimuli in rats. Neurosci Lett 345(3):145–148.  https://doi.org/10.1016/S0304-3940(03)00415-4 CrossRefGoogle Scholar
  12. Blanchard RJ, Blanchard DC, Rodgers J, Weiss SM (1990) The characterization and modeling of antipredator defensive behavior. Neurosci Biobehav Rev 14(4):463–472.  https://doi.org/10.1016/S0149-7634(05)80069-7 CrossRefGoogle Scholar
  13. Blanchard RJ, Blanchard DC (2003) Bringing defensive behaviors into the laboratory: a tribute to Paul MacLean. Physiol Behav 79(3):514–524CrossRefGoogle Scholar
  14. Canteras NS, Chiavegatto S, Ribeiro do Valle LE, Swanson LW (1997) Severe reduction of defensive behavior to a predator by discrete hypothalamic chemical lesions. Brain Res Bull 44(3):297–305.  https://doi.org/10.1016/S0361-9230(97)00141-X CrossRefGoogle Scholar
  15. Carola V, D'Olimpio F, Brunamonti E, Mangia F, Renzi P (2002) Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav Brain Res 134(1–2):49–57.  https://doi.org/10.1016/S0166-4328(01)00452-1 CrossRefGoogle Scholar
  16. Canteras NS, Simerly RB, Swanson LW (1994) Organization of projections from the ventromedial nucleus of the hypothalamus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J Comp Neurol. Oct 1; 348(1):41–79Google Scholar
  17. Cezario AF, Ribeiro-Barbosa ER, Baldo MV, Canteras NS (2008) Hypothalamic sites responding to predator threats—the role of the dorsal premammillary nucleus in unconditioned and conditioned antipredatory defensive behavior. Eur J Neurosci 28(5):1003–1015.  https://doi.org/10.1111/j.1460-9568.2008.06392.x CrossRefGoogle Scholar
  18. Cheng SB, Kuchiiwa S, Nagatomo I, Akasaki Y, Uchida M, Tominaga M, Hashiguchi W, Kuchiiwa T, Nakagawa S (2002) 2,3,7,8-Tetrachlorodibenzo-p-dioxin treatment induces c-Fos expression in the forebrain of the Long-Evans rat. Brain Res 931(2):176–180.  https://doi.org/10.1016/S0006-8993(02)02257-6 CrossRefGoogle Scholar
  19. Clotfelter ED, Bell AM, Levering KR (2004) The role of animal behavior in the study of endocrine-disrupting chemicals. Anim Behav 68(4):665–676.  https://doi.org/10.1016/j.anbehav.2004.05.004 CrossRefGoogle Scholar
  20. Dai J, Wang Z, Xu W, Zhang M, Zhu Z, Zhao X, Zhang D, Nie D, Wang L, Qiao Z (2017) Paternal nicotine exposure defines different behavior in subsequent generation via hyper-methylation of mmu-miR-15b. Sci Rep 7(1):7286.  https://doi.org/10.1038/s41598-017-07920-3. CrossRefGoogle Scholar
  21. De Oliveira Crisanto K, de Andrade WM, de Azevedo Silva KD, Lima RH, de Oliveira Costa MS, de Souza Cavalcante J, de Lima RR, do Nascimento ES Jr, Cavalcante JC (2015) The differential mice response to cat and snake odor. Physiol Behav 152(Pt A):272–279.  https://doi.org/10.1016/j.physbeh.2015.10.013 CrossRefGoogle Scholar
  22. Faimali M, Gambardella C, Costa E, Piazza V, Morgana S, Estévez-Calvar N, Garaventa F (2017) Old model organisms and new behavioral end-points: swimming alteration as an ecotoxicological response. Mar Environ Res 128:36–45.  https://doi.org/10.1016/j.marenvres.2016.05.006 CrossRefGoogle Scholar
  23. Fait BW, Thompson DC, Mose TN, Jatlow P, Jordt SE, Picciotto MR, Mineur YS (2017) Menthol disrupts nicotine’s psychostimulant properties in an age and sex-dependent manner in C57BL/6J mice. Behav Brain Res 334:72–77.  https://doi.org/10.1016/j.bbr.2017.07.027 CrossRefGoogle Scholar
  24. Focazio MJ, Kolpin DW, Barnes KK, Furlong ET, Meyer MT, Zaugg SD, Barber LB, Thurmann ME (2008) A national reconnaissance for pharmaceuticals and other organic wastewater contaminants in the United States—II untreated drinking water sources. Sci Total Environ 402(2-3):201–216.  https://doi.org/10.1016/j.scitotenv.2008.02.021 CrossRefGoogle Scholar
  25. Frings H, Frings M, Kivert A (1951) Behavior patterns of the laboratory mouse under auditory stress. J Mammal 32(1):60–76.  https://doi.org/10.2307/1375413 CrossRefGoogle Scholar
  26. Gotts JE, Chun L, Abbot J, Takasak N, Nishimura S, Calfee CS, Matthay MA (2017) Short-term cigarette smoke exposure increases acute lung injury in antibiotic treated pneumococcal pneumonia in mice. Am J Respir Crit Care Med 195:A2805Google Scholar
  27. Graeff FG (1994) Neuroanatomy and neurotransmitter regulation of defensive behaviors and related emotions in mammals. Braz J Med Biol Res 27(4):811–829Google Scholar
  28. Green ALR, Putschew A, Nehls T (2014) Littered cigarette butts as a source of nicotine in urban waters. J Hydrol 519:3466–3474.  https://doi.org/10.1016/j.jhydrol.2014.05.046 CrossRefGoogle Scholar
  29. Green CR, Rodgman A (1996) The tobacco chemists’ research conference: a half century forum for advances in analytical methodology of tobacco and its products. Recent Advances in Tobacco. Science 22:131–304Google Scholar
  30. Greene TM, Redding CL, Birkett MA (2014) Effects of rat visual, olfactory, or combined stimuli during cohousing on stress-related physiology and behavior in C57BL/6NCrl mice. J Am Assoc Lab Anim Sci 53(6):647–652Google Scholar
  31. Hacquemand R, Lacquot L, Brand G (2010) Comparative fear-related behaviors to predator odors (TMT and natural fox feces) before and after intranasal ZnSO4 treatment in mice. Front Behav Neurosc 4:188CrossRefGoogle Scholar
  32. Healton CG, Cummings MK, O’Connor RJ, Novotny TE (2011) Butt really? The environmental impact of cigarettes. Tobacco Control 20(Suppl 1):1CrossRefGoogle Scholar
  33. Itoh M, Tsuji T, Nakamura H, Yamaguchi K, Fuchikami J, Takahashi M, Morozumi Y, Aoshiba K (2014) Systemic effects of acute cigarette smoke exposure in mice. Inhal Toxicol 26(8):464–473.  https://doi.org/10.3109/08958378.2014.917346 CrossRefGoogle Scholar
  34. Johnson J, Wu V, Donovan M, Majumdar S, Rentería RC, Porco T, Van Gelder RN, Copenhagen DR (2010) Melanopsin-dependent light avoidance in neonatal mice. Proc Natl Acad Sci U S A 107(40):17374–17378.  https://doi.org/10.1073/pnas.1008533107 CrossRefGoogle Scholar
  35. Kalueff AV, Tuohimaa P (2005) The grooming analysis algorithm discriminates between different levels of anxiety in rats: potential utility for neurobehavioral stress research. J Neurosci Methods 143(2):169–177.  https://doi.org/10.1016/j.jneumeth.2004.10.001 CrossRefGoogle Scholar
  36. Kavaliers M, Choleris E (2001) Antipredator responses and defensive behavior: ecological and ethological approaches for the neurosciences. Neurosci Biobehav Rev 5(7–8):577–586CrossRefGoogle Scholar
  37. Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, Ikawa M, Okabe M, Ikeda T, Itohara S, Kikusui T, Mori K, Sakano H (2007) Innate versus learned odour processing in the mouse olfactory bulb. Nature 450(7169):503–508.  https://doi.org/10.1038/nature06281 CrossRefGoogle Scholar
  38. Korte SM (2001) Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci Biobehav Rev 25(2):117–142.  https://doi.org/10.1016/S0149-7634(01)00002-1 CrossRefGoogle Scholar
  39. Kunwar P, Zelikowky M, Remedios R, Cai H, Yilmaz M, Meister M, Anderson DJ (2015) Ventromedial hypothalamic neurons control a defensive emotion state. eLife 4:e06633CrossRefGoogle Scholar
  40. Lawal MS, Ologundudu SO (2013) Toxicity of cigarette filter leachates on Hymenochirus curtipes and Clarias gariepinus in Nigeria. J Environ Ext 11:7–14Google Scholar
  41. Lee W, Lee CC (2015) Developmental toxicity of cigarette butts—an underdeveloped issue. Ecotoxicol Environ Saf 113:362–368.  https://doi.org/10.1016/j.ecoenv.2014.12.018 CrossRefGoogle Scholar
  42. Macé E, Caplette R, Marre O, Sengupta A, Chaffiol A, Barbe P, Desrosiers M, Bamberg E, Sahel JA, Picaud S, Duebel J, Dalkara D (2015) Targeting channel rhodopsin-2 to ON-bipolar cells with vitreally administered AAV restores ON and OFF visual responses in blind mice. Mol Ther 23(1):7–16.  https://doi.org/10.1038/mt.2014.154 CrossRefGoogle Scholar
  43. Malafaia G, Estrela DC, Silva WAM, Guimarães ATB, Mendes BO, Rodrigues ASL, Menezes IPP (2015) Toxicity study in mice fed with corn produced in soil containing tannery sludge vermicompost and irrigated with domestic wastewater. Curr Sci 109(7):1326–1332Google Scholar
  44. Mangubat M, Lutfy K, Lee ML, Pulido L, Stout D, Davis R, Shin CS, Shahbazian M, Seasholtz S, Sinha-Hikim A, Sinha-Hikim I, O'Dell LE, Lyzlov A, Liu Y, Friedman TC (2012) Effect of nicotine on body composition in mice. J Endocrinol 212(3):317–326.  https://doi.org/10.1530/JOE-11-0350 CrossRefGoogle Scholar
  45. Markham CM, Blanchard DC, Cateras NS, Cuyno C, Blanchard RJ (2004) Modulation of predatory odor processing following lesions to the dorsal premammilary nucleus. Neurosci Lett 372(1-2):22–26.  https://doi.org/10.1016/j.neulet.2004.09.006 CrossRefGoogle Scholar
  46. Martinez RCR, Carvalho-Netto EF, Amaral VCS, Nunes-de-Souza RL, Canteras NS (2008) Investigation of the hypothalamic defensive system in the mouse. Behav Brain Res 192(2):185–190.  https://doi.org/10.1016/j.bbr.2008.03.042 CrossRefGoogle Scholar
  47. Mendes BO, Rabelo LM, de Silva BC, de Souza JM, da Silva Castro AL, da Silva AR, de Lima Rodrigues AS, Malafaia G (2017) Mice exposure to tannery effluents changes their olfactory capacity, and their response to predators and to the inhibitory avoidance test. Environ Sci Pollut Res Int 24(23):19234–19248.  https://doi.org/10.1007/s11356-017-9504-5 CrossRefGoogle Scholar
  48. Micevska T, Warne MS, Pablo F, Patra R (2006) Variation in, and causes of, toxicity of cigarette butts to a cladoceran and microtox. Arch Environ Contam Toxicol 50(2):205–212.  https://doi.org/10.1007/s00244-004-0132-y CrossRefGoogle Scholar
  49. Missouri Poison Center (2014) Nicotine—acute toxic hazard in e-cigarettes. (Available in: http://missouripoisoncenter.org/wp-content/uploads/2015/02/2014-Liquid-Nicotine.pdf. Accessed in: 02 April, 2017
  50. Moerman JW, Potts GE (2011) Analysis of metals leached from smoked cigarette litter. Tob Control 20:130–135CrossRefGoogle Scholar
  51. Moriwaki H, Kitajima S, Katahira K (2009) Waste on the roadside, “poi-sute” waste: its distribution and elution potential of pollutants into environment. Waste Manag 29(3):1192–1197.  https://doi.org/10.1016/j.wasman.2008.08.017 CrossRefGoogle Scholar
  52. Odermatt A, Gumy C (2008) Glucocorticoid and mineralocorticoid action: why should we consider influences by environmental chemicals? Biochem Pharmacol 76(10):1184–1193.  https://doi.org/10.1016/j.bcp.2008.07.019 CrossRefGoogle Scholar
  53. Osuala FI, Abiodun OA, Igwo-Ezikpe MN, Kemabonta KA, Otitoloju AA (2017) Relative toxicity of cigarette butts leachate and usefulness of antioxidant biomarker activity in Nile tilapia Oreochromis niloticus (Trewavas, 1983). Ethiop J\ Environ Stud Manag 10(1):75–88.  https://doi.org/10.4314/ejesm.v10i1.8 CrossRefGoogle Scholar
  54. Parker TT, Rayburn JA (2017) Comparison of electronic and traditional cigarette butt leachate on the development of Xenopus laevis embryos. Toxicol Rep 4:77–82.  https://doi.org/10.1016/j.toxrep.2017.01.003 CrossRefGoogle Scholar
  55. Patel V, Thomson GW, Wilson N (2013) Cigarette butt littering in city streets: a new methodology for studying and results. Tob Control 22(1):59–62.  https://doi.org/10.1136/tobaccocontrol-2012-050529 CrossRefGoogle Scholar
  56. Polosukhina A, Litt J, Tochitsky I, Nemargut J, Sychev Y, De Kouchkovsky I, Huang T, Borges K, Trauner D, Van Gelder RN, Kramer RH (2012) Photochemical restoration of visual responses in blind mice. Neuron 75(2):271–282.  https://doi.org/10.1016/j.neuron.2012.05.022 CrossRefGoogle Scholar
  57. Prut L, Belzung C (2003) The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 463(1–3):3–33.  https://doi.org/10.1016/S0014-2999(03)01272-X CrossRefGoogle Scholar
  58. Pyle G, Ford AT (2017) Behaviour revised: contaminant effects on aquatic animal behavior. Aquatic Toxiciol 182:226–228.  https://doi.org/10.1016/j.aquatox.2016.11.008 CrossRefGoogle Scholar
  59. Schneider S, Gadinger M, Fischer A (2012) Does the effect go up in smoke? A randomized controlled trial of pictorial warnings on cigarette packaging. Patient Educ Couns 86(1):77–83.  https://doi.org/10.1016/j.pec.2011.03.005 CrossRefGoogle Scholar
  60. Schwerdtfeger RMH, Menard JL (2008) The lateral hypothalamus and anterior hypothalamic nucleus differentially contribute to rat’s defensive responses in the elevated plus-maze and shock-probe burying tests. Physiol Behav 93(4-5):697–705.  https://doi.org/10.1016/j.physbeh.2007.11.011 CrossRefGoogle Scholar
  61. Seco Pon JP, Becherucci ME (2012) Spatial and temporal variations of urban litter in Mar del Plata, the major coastal city of Argentina. Waste Manag 32(2):343–348.  https://doi.org/10.1016/j.wasman.2011.10.012 CrossRefGoogle Scholar
  62. Singla N, Kaur R (2014) Potential of citronella oil as rodent repellent measured as aversion to food. Applied Biol Res 16(2):191–198CrossRefGoogle Scholar
  63. Slaughter E, Gersberg RM, Watanabe K, Rudolph J, Stransky C, Novotny TE (2011) Toxicity of cigarette butts, and their chemical components, to marine and freshwater fish. Tobacco Control 20(Suppl 1):i25–i29.  https://doi.org/10.1136/tc.2010.040170 CrossRefGoogle Scholar
  64. Stuart M, Lapworth D, Crane E, Hart A (2012) Review of risk from potential emerging contaminants in UK groundwater. Sci Total Environ 416:1–21.  https://doi.org/10.1016/j.scitotenv.2011.11.072 CrossRefGoogle Scholar
  65. Suárez-Rodríguez M, López-Rull I, Garcia CM (2012) Incorporation of cigarette butts into nests reduces nest ectoparasite load in urban birds: new ingredients for an old recipe? Biol Lett 9(1):20120931.  https://doi.org/10.1098/rsbl.2012.0931 CrossRefGoogle Scholar
  66. Suárez-Rodríguez M, Macías GC (2014) There is no such a thing as a free cigarette; lining nests with discarded butts brings short-term benefits, but causes toxic damage. J Evol Biol. 27(12):2719–2726.  https://doi.org/10.1111/jeb.12531 CrossRefGoogle Scholar
  67. Topal A, Atamanalp M, Oruç E, Halici HBH, Şişecioğlu M, Erol HS, Gergit A, Yilmaz B (2015) Neurotoxic effects of nickel chloride in the rainbow trout brain: assessment of c-Fos activity, antioxidant responses, acetylcholinesterase activity, and histopathological changes. Fish Physiol Biochem 41(3):625–634.  https://doi.org/10.1007/s10695-015-0033-1 CrossRefGoogle Scholar
  68. Uemasu K, Sato A, Tanimura K, Hasegawa K, Hamakawa Y, Sato S, Muro S (2017) Role of CCAAT/enhancer binding protein-α (C/EBPα) in airway epithelial cells during chronic cigarette smoke exposure in mice. Am J Respir Crit Care Med 195:A3057Google Scholar
  69. Valcárcel Y, Alonso SG, Rodríguez-Gil JL, Gil A, Catalá M (2011) Detection of pharmaceutically active compounds in the rivers and tap water of the Madrid Region (Spain) and potential ecotoxicological risk. Chemosphere 84(10):1336–1348.  https://doi.org/10.1016/j.chemosphere.2011.05.014 CrossRefGoogle Scholar
  70. Vianna DM, Borelli KG, Ferreira-Netto C, Macedo CE, Brandão ML (2003) Fos-like immunoreactive neurons following electrical stimulation of the dorsal periaquductal gray at freezing and escape thresholds. Brain Res Bull 62(3):179–189.  https://doi.org/10.1016/j.brainresbull.2003.09.010 CrossRefGoogle Scholar
  71. Wang L, Chen IZ, Lin D (2015) Collateral pathways from the ventromedial hypothalamus mediate defensive behaviors. Neuron 85(6):1344–1358.  https://doi.org/10.1016/j.neuron.2014.12.025 CrossRefGoogle Scholar
  72. World Health Organization (WHO) (2017) Tobacco. Available in: http://www.who.int/mediacentre/factsheets/fs339/en/. Access in: 5 Nov. 2017
  73. Wright SL, Rowe D, Reid MJ, Thomas KV, Galloway TS (2015) Bioaccumulation and biological effects of cigarette litter in marine worms. Sci Rep 5(1):14119.  https://doi.org/10.1038/srep14119 CrossRefGoogle Scholar
  74. Elhassan S, Bagdas D, Darmaj I (2017) Effects of nicotine metabolites on nicotine withdrawal behaviors in mice. Nicotine Tob Res 19(6):763–766.  https://doi.org/10.1093/ntr/ntx045 CrossRefGoogle Scholar
  75. Tuon T, Valvassori SS, Lopes-Borges J, Fries GR, Silva LA, Kapczinski F, Quevedo J, Pinho RA (2010) Effects of moderate exercise on cigarette smoke exposure-induced hippocampal oxidative stress values and neurological behaviors in mice. Neurosci Lett 475(1):16–19.  https://doi.org/10.1016/j.neulet.2010.03.030 CrossRefGoogle Scholar
  76. Ponzoni L, Moretti M, Sala M, Fasoli F, Mucchietto V, Lucini V, Cannazza G, Gallesi G, Castellana CN, Clementi F, Zoli M, Gotti C, Braida D (2015) Different physiological and behavioural effects of e-cigarette vapour and cigarette smoke in mice. Eur Neuropsychopharmacol 25(10):1775–1786.  https://doi.org/10.1016/j.euroneuro.2015.06.010 CrossRefGoogle Scholar
  77. Kao LS, Green CE (2008) Analysis of variance: is there a difference in means and what does it mean? J Surg Res 144(1):158–170.  https://doi.org/10.1016/j.jss.2007.02.053 CrossRefGoogle Scholar
  78. Kim H-Y (2015) Statistical notes for clinical researchers: post-hoc multiple comparisons. Restorative Dent Endodontics 40(2):172–176.  https://doi.org/10.5395/rde.2015.40.2.172 CrossRefGoogle Scholar
  79. Gastwirth JL, Gel YR, Miao W (2009) The impact of Levene’s test of equality of variance on statistical theory and practice. Stat Sci 24(3):343–360.  https://doi.org/10.1214/09-STS301 CrossRefGoogle Scholar
  80. Bewick V, Cheek L, Ball J (2004) Statistics review 10: further nonparametric methods. Crit Care 8(3):196–199.  https://doi.org/10.1186/cc2857 CrossRefGoogle Scholar
  81. Akil O, Oursler AE, Fan K, Lustig LR (2016) Mouse auditory brainstem response testing. Bio Protoc 6(6):e1768CrossRefGoogle Scholar
  82. Scimemi P, Santarelli R, Selmo A, Mammano F (2014) Auditory brainstem responses to clicks and tone bursts in C57Bl/6J mice. Acta Otorhinolaryngol Ital 34(4):264–271Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Letícia Silva Cardoso
    • 1
  • Fernanda Neves Estrela
    • 1
  • Thales Quintão Chagas
    • 1
  • Wellington Alves Mizael da Silva
    • 2
  • Denys Ribeiro de Oliveira Costa
    • 3
  • Igor Pereira
    • 3
  • Boniek Gontijo Vaz
    • 3
  • Aline Sueli de Lima Rodrigues
    • 2
  • Guilherme Malafaia
    • 1
    • 2
    • 4
    Email author
  1. 1.Biological Research LaboratoryGoiano Federal Institute—Urutá CamposUrutáBrazil
  2. 2.Post-Graduation Program in Cerrado Natural Resource Conservation and Biological Research LaboratoryGoiano Federal Institution—Urutaí CampusUrutaíBrazil
  3. 3.Post-Graduation Program in ChemistryGoiás Federal University—Samambaia CampusGoiâniaBrazil
  4. 4.Laboratório de Pesquisas BiológicasInstituto Federal Goiano—Campus UrutaíUrutaíBrazil

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