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Research Article

The effect of enriched versus depleted housing on eucalyptus smoke-induced cardiovascular dysfunction in mice

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Received 19 Nov 2023, Accepted 30 Apr 2024, Published online: 22 May 2024

References

  • Bailoo JD, Murphy E, Boada-Saña M, Varholick JA, Hintze S, Baussière C, Hahn KC, Göpfert C, Palme R, Voelkl B, et al. 2018. Effects of cage enrichment on behavior, welfare and outcome variability in female mice. Front Behav Neurosci. 12:232. doi: 10.3389/fnbeh.2018.00232.
  • Blair C, Raver C, Granger D, Mills-Koonce R, Hibel L, . 2011. Allostasis and allostatic load in the context of poverty in early childhood. Dev Psychopathol. 23(3):845–857. doi: 10.1017/S0954579411000344.
  • Bor J. 2016. Capitalizing on natural experiments to improve our understanding of population health. Am J Public Health. 106(8):1388–1389. doi: 10.2105/AJPH.2016.303294.
  • Brauner AE, Kurijaka DT, Ibragimov A, Baldwin AL. 2010. Impact of cage size and enrichment (tube and shelf) on heart rate variability in rats. Scand J Lab Anim Sci. 37:185–201.
  • Buckley CL, Stokes AJ. 2011. Mice lacking functional TRPV1 are protected from pressure overload cardiac hypertrophy. Channels. 5(4):367–374. doi: 10.4161/chan.5.4.17083.
  • Centers for Disease Control and Prevention. 2018. Social determinants of health: know what affects health. Retrieved from https://www.cdc.gov/socialdeterminants/index.htm.
  • Chen H, Samet JM, Bromberg PA, Tong H. 2021. Cardiovascular health impacts of wildfire smoke exposure. Part Fibre Toxicol. 18(1):2–22. doi: 10.1186/s12989-020-00394-8.
  • Claudel SE, Adu-Brimpong J, Banks A, Ayers C, Albert MA, Das SR, de Lemos JA, Leonard T, Neeland IJ, Rivers JP, et al. 2018. Association between neighborhood-level socioeconomic deprivation and incident hypertension: a longitudinal analysis of data from the Dallas heart study. Am Heart J. 204:109–118. doi: 10.1016/j.ahj.2018.07.005.
  • de Brito JN, Pope ZC, Mitchell NR, Schneider IE, Larson JM, Horton TH, Pereira MA. 2020. The effect of green walking on heart rate variability: a pilot crossover study. Environ Res185:109408. doi: 10.1016/j.envres.2020.109408.
  • DeFlorio-Barker S, Crooks J, Reyes J, Rappold AG. 2019. cardiopulmonary effects of fine particulate matter exposure among older adults, during Wildfire and Non-Wildfire Periods, in the United States 2008–2010. Environ Health Perspect. 127(3):37006. PMID: 30875246; PMCID: PMC6768318. doi: 10.1289/EHP3860.
  • Diez Roux AV, Merkin SS, Arnett D, Chambless L, Massing M, Nieto FJ, Sorlie P, Szklo M, Tyroler HA, Watson RL. 2001. Neighborhood of residence and incidence of coronary heart disease. N Engl J Med. 345(2):99–106. doi: 10.1056/NEJM200107123450205.
  • Ford CD, Sims M, Higginbotham JC, Crowther MR, Wyatt SB, Musani SK, Payne TJ, Fox ER, Parton JM. 2016. Psychosocial factors are associated with blood pressure progression among African Americans in the Jackson Heart Study. Am J Hypertens. 29(8):913–924. doi: 10.1093/ajh/hpw013.
  • Forte M, Marchitti S, Di Nonno F, Stanzione R, Schirone L, Cotugno M, Bianchi F, Schiavon S, Raffa S, Ranieri D, et al. 2022. NPPA/atrial natriuretic peptide is an extracellular modulator of autophagy in the heart. Autophagy. 19(4):1087–1099. doi: 10.1080/15548627.2022.2115675.
  • Ganatra S, Dani SS, Kumar A, Khan SU, Wadhera R, Neilan TG, Thavendiranathan P, Barac A, Hermann J, Leja M, et al. 2022. Impact of social vulnerability on comorbid cancer and cardiovascular disease mortality in the United States. JACC CardioOncol. 4(3):326–337. doi: 10.1016/j.jaccao.2022.06.005.
  • Gaskill BN, Gordon CJ, Pajor EA, Lucas JR, Davis JK, Garner JP. 2013. Impact of nesting material on mouse body temperature and physiology. Physiol Behav. 17110-111:87–95. doi: 10.1016/j.physbeh.2012.12.018.
  • Giral M, Armengol C, Gavaldà A. 2022. Physiologic effects of housing rats in metabolic cages. Comp Med. 72(5):298–305. doi: 10.30802/AALAS-CM-22-000026.
  • Gordon CJ. 1985. Relationship between autonomic and behavioral thermoregulation in the mouse. Physiol Behav. 34(5):687–690. doi: 10.1016/0031-9384(85)90365-8.
  • Gordon CJ. 2017. The mouse thermoregulatory system: its impact on translating biomedical data to humans. Physiol Behav. 1179:55–66. doi: 10.1016/j.physbeh.2017.05.026.
  • Hacker K, Auerbach J, Ikeda R, Philip C, Houry D, . 2022. Social determinants of health—an approach taken at CDC. J Public Health Manag Pract. 28(6):589–594. doi: 10.1097/PHH.0000000000001626.
  • Hadley MB, Henderson SB, Brauer M, Vedanthan R. 2022. Protecting cardiovascular health from wildfire smoke. Circulation. 146(10):788–801. doi: 10.1161/CIRCULATIONAHA.121.058058.
  • Hargrove MM, Kim YH, King C, Wood CE, Gilmour MI, Dye JA, Gavett SH. 2019. Smoldering and flaming biomass wood smoke inhibit respiratory responses in mice. Inhal Toxicol. 31(6):236–247. doi: 10.1080/08958378.2019.1654046.
  • Hazari MS, Phillips K, Stratford KM, Khan M, Thompson L, Oshiro W, Hudson G, Herr DW, Farraj AK. 2021. Exposure to intermittent noise exacerbates the cardiovascular response of wistar-kyoto rats to ozone inhalation and arrhythmogenic challenge. Cardiovasc Toxicol. 21(4):336–348. doi: 10.1007/s12012-020-09623-0.
  • Healthy People. 2030. U.S. Department of Health and Human Services, Office of Disease Prevention and Health Promotion. Retrieved from https://health.gov/healthypeople/objectives-and-data/social-determinants-health.
  • Hjalmarson A. 2007. Heart rate: an independent risk factor in cardiovascular disease. European Heart Journal Supplements. 9(suppl_F):F3–F7. doi: 10.1093/eurheartj/sum030.
  • Ho KW, Ward NJ, Calkins DJ. 2012. TRPV1: a stress response protein in the central nervous system. Am J Neurodegener Dis. 1(1):1–14.
  • Joseph P, Kutty VR, Mohan V, Kumar R, Mony P, Vijayakumar K, Islam S, Iqbal R, Kazmi K, Rahman O, et al. 2022. Cardiovascular disease, mortality, and their associations with modifiable risk factors in a multi-national South Asia cohort: a PURE substudy. Eur Heart J. 43(30):2831–2840. 7 doi: 10.1093/eurheartj/ehac249.
  • Kalliokoski O, Teilmann AC, Jacobsen KR, Abelson KS, Hau J. 2014. The lonely mouse - single housing affects serotonergic signaling integrity measured by 8-OH-DPAT-induced hypothermia in male mice. PLOS One. 9(12):e111065. doi: 10.1371/journal.pone.0111065.
  • Kim YH, Tong H, Daniels M, Boykin E, Krantz QT, McGee J, Hays M, Kovalcik K, Dye JA, Gilmour MI. 2014. Cardiopulmonary toxicity of peat wildfire particulate matter and the predictive utility of precision cut lung slices. Part Fibre Toxicol. 11(1):29. doi: 10.1186/1743-8977-11-29.
  • Koizumi A, Tsukada M, Wada Y, Masuda H, Weindruch R. 1992. Mitotic activity in mice is suppressed by energy restriction-induced torpor. J Nutr. 122(7):1446–1453. doi: 10.1093/jn/122.7.1446.
  • Krieger J, Higgins DL. 2002. Housing and health: time again for public health action. Am J Public Health.92(5):758–768. doi: 10.2105/ajph.92.5.758.
  • Kulesskaya N, Rauvala H, Voikar V. 2011. Evaluation of social and physical enrichment in modulation of behavioural phenotype in C57BL/6J female mice. PLOS One. 6(9):e24755. doi: 10.1371/journal.pone.0024755.
  • Kurhanewicz N, Ledbetter A, Farraj A, Hazari M. 2018. TRPA1 mediates the cardiac effects of acrolein through parasympathetic dominance but also sympathetic modulation in mice. Toxicol Appl Pharmacol.347:104–114. doi: 10.1016/j.taap.2018.03.027.
  • Lee J, Tsunetsugu Y, Takayama N, Park BJ, Li Q, Song C, Komatsu M, Ikei H, Tyrväinen L, Kagawa T, et al. 2014. Influence of forest therapy on cardiovascular relaxation in young adults. Evid Based Complement Alternat Med. 2014:834360–834367. doi: 10.1155/2014/834360.
  • Lima PMA, Reis TO, Wanner SP, Chianca DA, Jr, de Menezes RC. 2022. The role of peripheral transient receptor potential vanilloid 1 channels in stress-induced hyperthermia in rats subjected to an anxiogenic environment. J Therm Biol. 106:103191. May doi: 10.1016/j.jtherbio.2022.103191.
  • Martin BL, Thompson LC, Kim YH, Snow SJ, Schladweiler MC, Phillips P, Harmon M, King C, Richards J, George I, Kyle Martin W , Haykal-Coates N, Gilmour MI, Kodavanti UP, Hazari MS, Farraj AK. 2020. A single exposure to eucalyptus smoke sensitizes rats to the postprandial cardiovascular effects of a high carbohydrate oral load. Inhal Toxicol. ;32(8):342–353. doi: 10.1080/08958378.2020.1809572.
  • Mathar I, Kecskes M, Van der Mieren G, Jacobs G, Camacho Londoño JE, Uhl S, Flockerzi V, Voets T, Freichel M, Nilius B, et al. 2014. Increased β-adrenergic inotropy in ventricular myocardium from Trpm4-/- mice. Circ Res. 114(2):283–294. 17 doi: 10.1161/CIRCRESAHA.114.302835.
  • Mathar I, Vennekens R, Meissner M, Kees F, Van der Mieren G, Camacho Londoño JE, Uhl S, Voets T, Hummel B, van den Bergh A, et al. 2010. Increased catecholamine secretion contributes to hypertension in TRPM4-deficient mice. J Clin Invest. 120(9):3267–3279. doi: 10.1172/JCI41348.
  • Nobari TZ, Whaley SE, Blumenberg E, Prelip ML, Wang MC. 2018. Severe housing-cost burden and obesity among preschool-aged low-income children in Los Angeles County. Prev Med Rep. 13:139–145. doi: 10.1016/j.pmedr.2018.12.003.
  • Olsson IA, Dahlborn K. 2002. Improving housing conditions for laboratory mice: a review of “environmental enrichment”. Lab Anim. 36(3):243–270. doi: 10.1258/002367702320162379.
  • Palatini P, Julius S. 2004. Elevated heart rate: a major risk factor for cardiovascular disease. Clin Exp Hypertens. 26(7–8):637–644. doi: 10.1081/ceh-200031959.
  • Palatini P. 2011. Role of elevated heart rate in the development of cardiovascular disease in hypertension. Hypertension. 58(5):745–750. doi: 10.1161/HYPERTENSIONAHA.111.173104.
  • Perez MV, Pavlovic A, Shang C, Wheeler MT, Miller CL, Liu J, Dewey FE, Pan S, Thanaporn PK, Absher D, et al. 2015. Systems genomics identifies a key role for hypocretin/orexin receptor-2 in human heart failure. J Am Coll Cardiol. 66(22):2522–2533. doi: 10.1016/j.jacc.2015.09.061.
  • Rajagopalan S, Al-Kindi SG, Brook RD. 2018. Air pollution and cardiovascular disease: state-of-the-art review. J Am Coll Cardiol. 72(17):2054–2070. doi: 10.1016/j.jacc.2018.07.099.
  • Rappold AG, Cascio WE, Kilaru VJ, Stone SL, Neas LM, Devlin RB, Diaz-Sanchez D. 2012. Cardio-respiratory outcomes associated with exposure to wildfire smoke are modified by measures of community health. Environ Health. 11(1):71. doi: 10.1186/1476-069X-11-71.
  • Schipper L, van Heijningen S, Karapetsas G, van der Beek EM, van Dijk G. 2020. Individual housing of male C57BL/6J mice after weaning impairs growth and predisposes for obesity. PLOS One. 15(5):e0225488. doi: 10.1371/journal.pone.0225488.
  • Schmidt S, Haase M, Best L, Groth M, Lindner J, Witte OW, Kaleta C, Frahm C. 2022. Restoring age-related cognitive decline through environmental enrichment: a transcriptomic approach. Cells.11(23):3864. doi: 10.3390/cells11233864.
  • Schneider M, Kraemmer MM, Weber B, Schwerdtfeger AR. 2021. Life events are associated with elevated heart rate and reduced heart complexity to acute psychological stress. Biol Psychol. 163:108116. doi: 10.1016/j.biopsycho.2021.108116.
  • Sharp J, Azar T, Lawson D. 2014. Effects of a complex housing environment on heart rate and blood pressure of rats at rest and after stressful challenges. J Am Assoc Lab Anim Sci. 53(1):52–60.
  • Shaw M. 2004. Housing and public health. Annu Rev Public Health. 25(1):397–418. doi: 10.1146/annurev.publhealth.25.101802.123036.
  • Sims M, Kershaw KN, Breathett K, Jackson EA, Lewis LM, Mujahid MS, Suglia SF, 2020. Importance of housing and cardiovascular health and well-being: a scientific statement from the American Heart Association. Circ Cardiovasc Qual Outcomes. 13(8):e000089. doi: 10.1161/HCQ.0000000000000089.
  • Slater AM, Cao L. 2015. A protocol for housing mice in an enriched environment. J Vis Exp. 8(100):e52874. doi: 10.3791/52874.
  • Smith JA, Zhao W, Wang X, Ratliff SM, Mukherjee B, Kardia SLR, Liu Y, Roux AVD, Needham BL. 2017. Neighborhood characteristics influence DNA methylation of genes involved in stress response and inflammation: the multi-ethnic study of atherosclerosis. Epigenetics. 12(8):662–673. doi: 10.1080/15592294.2017.1341026.
  • Späni D, Arras M, König B, Rülicke T. 2002. Higher heart rate of laboratory mice housed individually vs in pairs. Lab Anim. 37(1):54–62. doi: 10.1258/002367703762226692.
  • Hazari MS, Stratford KM, Krantz QT, King C, Krug J, Farraj AK, Gilmour MI. 2018. Comparative cardiopulmonary effects of particulate matter- and ozone-enhanced smog atmospheres in mice. Environ Sci Technol. 52(5):3071–3080. 6doi: 10.1021/acs.est.7b04880.
  • Stratford K, Haykal-Coates N, Thompson L, Krantz QT, King C, Krug J, Gilmour MI, Farraj A, Hazari M. 2018. Early-life persistent Vitamin D deficiency alters cardiopulmonary responses to particulate matter-enhanced atmospheric smog in adult mice. Environ Sci Technol. 52(5):3054–3061. doi: 10.1021/acs.est.7b04882.
  • Thompson LC, Kim YH, Martin BL, Ledbetter AD, Dye JA, Hazari MS, Gilmour MI, Farraj AK. 2018. Pulmonary exposure to peat smoke extracts in rats decreases expiratory time and increases left heart end systolic volume. Inhal Toxicol. 30(11–12):439–447. doi: 10.1080/08958378.2018.1551443.
  • van Eijl S, van Oorschot R, Olivier B, Nijkamp FP, Bloksma N. 2006. Stress and hypothermia in mice in a nose-only cigarette smoke exposure system. Inhal Toxicol. 18(11):911–918. doi: 10.1080/08958370600822672.
  • Watanabe S, Al Omran A, Shao AS, Liang J. 2022. Social isolation model: A noninvasive rodent model of stress and anxiety. J Vis Exp. 11(189). doi: 10.3791/64567.
  • Zhang A, Hughes JT, Brown A, Lawton PD, Cass A, Hoy W, O'Dea K, Maple-Brown LJ. 2016. Resting heart rate, physiological stress and disadvantage in Aboriginal and Torres Strait Islander Australians: analysis from a cross-sectional study. BMC Cardiovasc Disord. 16(1):36. 11 doi: 10.1186/s12872-016-0211-9.