Abstract
The present study aimed to compare the effects of indoor versus outdoor aerobic exercise through the evaluation of pollution exposure, changes in cognitive function, and biochemical variables in elderly individuals. Forty-eight volunteers, aged 60 years or older, were randomly assigned to 4 groups: control indoor, control outdoor, indoor exercise, and outdoor exercise (n = 12/group). Atmospheric concentration of 5 pollutants was monitored. Cognitive function and biochemical analysis were done after 12 weeks. All pollutants measured were significantly higher outdoor (p < 0.05). Temperature was not different between indoor and outdoor environment along 12 weeks (p > 0.05). Indoor aerobic exercise presented lower concentration of pollutants, improved cognitive function, and enhanced brain-derived neuro factor (BDNF) levels when compared to outdoor (p < 0.05). Indoor aerobic exercise showed significant glycemic reduction compared to other groups (p < 0.05). Indoor aerobic exercise presents lower concentration of pollutants than outdoor and provides better benefits to the management of glycemia, improves cognition, and enhances BDNF levels.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability statement
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
References
An R, Zhang S, Ji M, Guan C (2018) Impact of ambient air pollution on physical activity among adults: a systematic review and meta-analysis. Perspect Public Health 138(2):111–121. https://doi.org/10.1177/1757913917726567
Andrade M de F, de Miranda RM, Fornaro A, Kerr A, Oyama B, de Andre PA, Saldiva P (2012) Vehicle emissions and PM 2.5 mass concentrations in six Brazilian cities. Air Quality, Atmosphere and Health 5(1):79–88. https://doi.org/10.1007/s11869-010-0104-5
Batista AF, Frony-Germano L, Clarke JR, Silva NMLe, Brito-Moreira J, Boehnke SE, Winterborn A, Coe BC, Lablans A, Vital JF, Marques SA, Martinez AM, Gralle M, Holscher C, Klein WL, Houzel J-C, Ferreira ST, Munoz DP, De Felice FG (2018) The diabetes drug liraglutide reverses cognitive impairment in mice and attenuates insulin receptor and synaptic pathology in a non-human primate model of Alzheimer’s disease. J Pathol 245:85–100. https://doi.org/10.1002/path.5056
Block ML, Calderón-Garcidueñas L (2009) Air pollution: mechanisms of neuroinflammation & CNS disease Michelle. Trends Neurosci 32(9):506–516. https://doi.org/10.1016/j.tins.2009.05.009.Air
Bos I, Jacobs L, Nawrot TS, de Geus B, Torfs R, IntPanis L, Degraeuwe B, Meeusen R (2011) No exercise-induced increase in serum BDNF after cycling near a major traffic road. Neurosci Lett 500(2):129–132. https://doi.org/10.1016/j.neulet.2011.06.019
Bos I, De Boever P, Vanparijs J, Pattyn N, Panis LI, Meeusen R (2013) Subclinical effects of aerobic training in urban environment. Med Sci Sports Exerc 45(3):439–447. https://doi.org/10.1249/MSS.0b013e31827767fc
Bos I, De Boever P, IntPanis L, Meeusen R (2014) Physical activity, air pollution and the brain. Sports Med 44(11):1505–1518. https://doi.org/10.1007/s40279-014-0222-6
Calderón-Garcidueñas L, Reed W, Maronpot RR, Henríquez-Roldán C, Delgado-Chavez R, Calderón-Garcidueñas A, Dragustinovis I, Franco-Lira M, Aragón-Flores M, Solt AC, Altenburg M, Torres-Jardón R, Swenberg JA (2004) Brain inflammation and Alzheimer’s-like pathology in individuals exposed to severe air pollution. Toxicol Pathol 32(6):650–658. https://doi.org/10.1080/01926230490520232
Cassilhas RC, Lee KS, Fernandes J, Oliveira MGM, Tufik S, Meeusen R, De Mello MT (2012) Spatial memory is improved by aerobic and resistance exercise through divergent molecular mechanisms. Neuroscience 202:309–317. https://doi.org/10.1016/j.neuroscience.2011.11.029
Cassilhas RC, Tufik S, De Mello MT (2016) Physical exercise, neuroplasticity, spatial learning and memory. Cell Mol Life Sci 73(5):975–983. https://doi.org/10.1007/s00018-015-2102-0
CETESB (2016) Report of air quality in the São Paulo State 2015. Governo Do Estado de São Paulo, São Paulo
Cunningham C, O’ Sullivan R, Caserotti P, Tully MA (2020) Consequences of physical inactivity in older adults: a systematic review of reviews and meta-analyses. Scand J Med Sci Sports 30(5):816–827. https://doi.org/10.1111/sms.13616
De la Rosa A, Solana E, Corpas R, Bartrés-Faz D, Pallàs M, Vina J, Sanfeliu C, Gomez-Cabrera MC (2019) Long-term exercise training improves memory in middle-aged men and modulates peripheral levels of BDNF and Cathepsin B. Sci Rep 9(1):1–11. https://doi.org/10.1038/s41598-019-40040-8
De Sousa RAL (2017) Brief report of the effects of the aerobic, resistance, and high-intensity interval training in type 2 diabetes mellitus individuals diabetes mellitus. Int J Diabetes Dev Ctries 38:138–145. https://doi.org/10.1007/s13410-017-0582-1
De Sousa RAL, Caria ACI, De Jesus Silva FM, Diniz e Magalhães CO, Freitas DA, Lacerda ACR, Mendonça VA, Cassilhas RC, LeiteHR (2020b) High-intensity resistance training induces changes in cognitive function, but not in locomotor activity or anxious behavior in rats induced to type 2 diabetes. Physiol Behav 223(June):1–7. https://doi.org/10.1016/j.physbeh.2020.112998
De Sousa RAL, Hagenbeck KF, Arsa G, Pardono E (2020c) Moderate / high resistance exercise is better to reduce blood glucose and blood pressure in middle-aged diabetic subjects. Rev Bras Educ Fís Esporte 34(1):165–175
De Sousa RAL, Harmer AR, Freitas DA, Mendonça VA, Lacerda ACR, Leite HR (2020d) An update on potential links between type 2 diabetes mellitus and Alzheimer’s disease. Mol Biol Rep 47:6347–6356. https://doi.org/10.1007/s11033-020-05693-z
De Sousa RAL, Peixoto MFD, Leite HR, de Oliveira LRS, Freitas DA, da Silva-Júnior FA, Oliveira HS, Rocha-Vieira E, Cassilhas RC, de Oliveira DB (2020e) Neurological consequences of exercise during prenatal Zika virus exposure to mice pups. Int J Neurosci 21:1–11. https://doi.org/10.1080/00207454.2020.1860970
De Sousa RAL, Improta-caria AC, Aras-júnior R, De Oliveira EM, Soci ÚPR, Cassilhas RC (2021a) Physical exercise effects on the brain during COVID-19 pandemic: links between mental and cardiovascular health. Neurol Sci 42(4):1325–1334
De Sousa RAL, Rodrigues CM, Mendes BF, Improta-caria AC, Peixoto MFD, Cassilhas RC (2021c) Physical exercise protocols in animal models of Alzheimer’ s disease: a systematic review. Metab Brain Dis 36:85–95. https://doi.org/10.1007/s11011-020-00633-z
De Sousa RAL, Azevedo LM, Improta-Caria A, Freitas DA, Leite HR, Pardono E (2020a) Type 2 diabetes individuals improve Creactive protein levels after high-intensity weight lift training. Sci Sports 1–7. https://doi.org/10.1016/j.scispo.2020.05.008
De Sousa RAL, Rocha-Dias I, de Oliveira LRS, Improta-Caria AC, Monteiro-Junior RS, Cassilhas RC (2021b) Molecular mechanisms of physical exercise on depression in the elderly: a systematic review. Mol Biol Rep 1–10. https://doi.org/10.1007/s11033-021-06330-z
Ferrari N, Bae-Gartz I, Bauer C, Janoschek R, Koxholt I, Mahabir E, Appel S, Alejandre Alcazar MA, Grossmann N, Vohlen C, Brockmeier K, Dötsch J, Hucklenbruch-Rother E, Graf C (2017) Exercise during pregnancy and its impact on mothers and offspring in humans and mice. J Dev Orig Health Dis 9(1):1–14. https://doi.org/10.1017/S2040174417000617
Forny-germano L, Lyra NM, Batista F, Brito-moreira J, Gralle XM, Boehnke SE, Coe BC, Lablans A, Marques SA, Martinez AMB, Klein WL, Houzel XJ, Ferreira ST, Munoz DP, De Felice FG (2014) Alzheimer ’ s disease-like pathology induced by amyloid-B oligomers in nonhuman primates. Neurobiol Dis 34(41):13629–13643. https://doi.org/10.1523/JNEUROSCI.1353-14.2014
Freitas DA, Rocha-Vieira E, Soares BA, Nonato LF, Fonseca SR, Martins JB, Mendonça VA, Lacerda AC, Massensini AR, Poortamns JR, Meeusen R, Leite HR (2018) High intensity interval training modulates hippocampal oxidative stress, BDNF and inflammatory mediators in rats. Physiol Behav 184:6–11. https://doi.org/10.1016/j.physbeh.2017.10.027
Gatto NM, Henderson VW, Hodis HN, John JAS, Lurmannd F, Chen J-C, Mack WJ (2008) Components of air pollution and cognitive function in middle- aged and older adults in Los Angeles. Neurotoxicology 40:1–7. https://doi.org/10.1016/j.neuro.2013.09.004.Components
Improta-Caria AC, Nonaka CKV, Cavalcante BRR, De Sousa RAL, Júnior RA, Souza BS de F (2020) Modulation of microRNAs as a potential molecular mechanism involved in the beneficial actions of physical exercise in Alzheimer disease. Int J Mol Sci 21(14):1–35. https://doi.org/10.3390/ijms21144977
Karvonen J, Vuorimaa T (1988) Heart rate and exercise intensity during sports activities. Practical Application. Sports Med 312:303–312
Klein AB, Williamson R, Santini MA, Clemmensen C, Ettrup A, Rios M, Knudsen GM, Aznar S (2011) Blood BDNF concentrations reflect brain-tissue BDNF levels across species. Int J Neuropsychopharmacol 14(3):347–353. https://doi.org/10.1017/S1461145710000738
Kuehn BM (2018) Pollution exposure counteracts exercise benefits: exercise in green spaces, pollution reductions recommended. Circulation 137(14):1516–1517. https://doi.org/10.1161/CIRCULATIONAHA.118.034313
Lezak M, Howieson DB, Loring DW (2004) Neuropsychological assessment, 4th edn. Oxford University Press, New York
Lourenco MV, Frozza RL, de Freitas GB, Zhang H, Kincheski GC, Ribeiro FC, Gonçalves RA, Clarke JR, Beckman D, Staniszevski A, Berman H, Guerra LA, Forny-Germano L, Meier S, Wilcock DM, De Souza JM, Alves-Leon SV, Prado VF, Prado MAM, … De Felice FG (2019) Exercise-linked FNDC5/irisin rescues synaptic plasticity and memory defects in Alzheimer’s models. Nat Med 165–175. https://doi.org/10.1038/s41591-018-0275-4
Melo CS, Rocha-Vieira E, Freitas DA, Soares BA, Rocha-Gomes A, Riul TR, Mendonça VA, Lacerda ACR, Camargos ACR, Carvalho LED, De Sousa RAL, Leite HR (2019) A single session of high-intensity interval exercise increases antioxidants defenses in the hippocampus of Wistar rats. Physiol Behav 211(March):112675. https://doi.org/10.1016/j.physbeh.2019.112675
Miller KA, Siscovick DS, Sheppard L, ShepherdSullivan KJH, Anderson GL, Kaufman JD (2007) Long-term exposure to air pollution and incidence of cardiovascular events in women. N Engl J Med 356(5):447–458
Misra C, Singh M, Shen S, Sioutas C, Hall P (2002) Development and evaluation of a personal cascade impactor sampler (PCIS). J Aerosol Sci 33:1027–1047
Oroji B, Solgi E, Sadighzadeh A (2018) Assessment of air pollution in exercise centers and health risks. Environ Health Eng Manag 5(3):153–157. https://doi.org/10.15171/ehem.2018.21
Pedersen BK, Saltin B (2015) Exercise as medicine - evidence for prescribing exercise as therapy in 26 different chronic diseases. Scand J Med Sci Sports 25:1–72. https://doi.org/10.1111/sms.12581
Peters R, Ee N, Peters J, Booth A, Mudway I, Anstey KJ (2019) Air pollution and dementia: a systematic review. J Alzheimer’s Dis 70(s1):S145–S163. https://doi.org/10.3233/JAD-180631
Qin F, Yang Y, Wang S tao, Dong Y nan, Xu M xiao, Wang Z wei, Zhao J xiu (2019) Exercise and air pollutants exposure: a systematic review and meta-analysis. Life Sci 218(11):153–164. https://doi.org/10.1016/j.lfs.2018.12.036
Roe J, Aspinall P (2011) The restorative benefits of walking in urban and rural settings in adults with good and poor mental health. Health Place 17(1):103–113. https://doi.org/10.1016/j.healthplace.2010.09.003
Schikowski T, Altuğ H (2020) The role of air pollution in cognitive impairment and decline. Neurochem Int 136(February):104708. https://doi.org/10.1016/j.neuint.2020.104708
Sioutas C (2004) Development of new generation personal monitors for fine particulate matter (PM) and its metal content. Mickey Leland National Urban Air Toxics Research Center 2:1–22
Sousa RALD, Improta-Caria AC, Souza B S de F (2021d) Exercise–linked irisin: Consequences on mental and cardiovascular health in type 2 diabetes. Int J Mol Sci 22(4):1–15. https://doi.org/10.3390/ijms22042199
Sousa RAL, Freitas DA, Leite HR (2019) Cross-talk between obesity and central nervous system: role in cognitive function. Interv Obes Diabetes 3(1):1–3. https://doi.org/10.31031/IOD.2019.03.000551
Vaynman S, Ying Z, Gomez-pinilla F (2004) Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20:2580–2590. https://doi.org/10.1111/j.1460-9568.2004.03720.x
Weber KT, Janicki JS (1986) Cardiopulmonary exercise testing: physiologic principles and clinical applications. WB Saunders, Philadelphia (vol. 1)
Wilker EH, Preis SR, Beiser AS, Wolf PA, Au R, Kloog I, Li W, Schwartz J, Koutrakis P, DeCarli C, Seshadri S, Mittleman MA (2015) Long-term exposure to fine particulate matter, residential proximity to major roads and measures of brain structure Elissa. Stroke 46(5):1161–1166. https://doi.org/10.1161/STROKEAHA.114.008348.Long-term
Wu A, Ying Z, Gomez-Pinilla F (2004) The interplay between oxidative stress and brain-derived neurotrophic factor modulates the outcome of a saturated fat diet on synaptic plasticity and cognition. Eur J Neurosci 19(7):1699–1707. https://doi.org/10.1111/j.1460-9568.2004.03246.x
Acknowledgements
The authors are grateful to Department of Physical Education – Universidade Federal dos Vales do Jequitinhonha e Mucuri (UVFJM), School of Physical Education, Physiotherapy and Occupational Therapy (EEFFTO) – Universidade Federal de Minas Gerais (UFMG), Department of Psychobiology – Universidade Federal de São Paulo (UNIFESP), Associação Fundo de Incentivo à Pesquisa – AFIP, and to Biorender.com.
Funding
This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (grant number 2013/05018–5), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (grant number 478229/2013–5). Ricardo Augusto Leoni De Sousa received fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil—Finance Code 001.
Author information
Authors and Affiliations
Contributions
Ricardo Cardoso Cassilhas: conceptualization, methodology, investigation, formal analysis, writing, reviewing, and editing. Ricardo Augusto Leoni De Sousa: conceptualization, methodology, investigation, formal analysis, and writing. Luciana Caxa: conceptualization, methodology, investigation, formal analysis, writing, reviewing, and editing. Valter Viana: conceptualization, methodology, investigation, and formal analysis. Romain Meeusen: conceptualization, methodology, investigation, and formal analysis. Fábio Luiz Gonçalves: conceptualization, methodology, investigation, and formal analysis. Caíque Olegário Diniz e Magalhães: conceptualization, methodology, investigation, and formal analysis. Sérgio Tufik: conceptualization, methodology, investigation, and formal analysis. Marco Fabrício Dias Peixoto: conceptualization, methodology, investigation, and formal analysis. Renato Sobral Monteiro-Junior: conceptualization, methodology, investigation, and formal analysis. Marco Túlio de Mello: conceptualization, methodology, investigation, formal analysis, writing, resources, supervision, writing, reviewing, and editing.
Corresponding author
Ethics declarations
Ethical approval
This study was approved by the Research Ethics Committee of the Sao Paulo University under the protocol number 2141/11 in accordance with the Declaration of Helsinki and the CONSORT guidelines. This protocol was also registered at clinicaltrials.gov (#NCT02304731).
Consent to participate
Informed consent was taken from all patients.
Consent for publication
All authors approved the final version of the manuscript for publication.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Cassilhas, R.C., De Sousa, R.A.L., Caxa, L. et al. Indoor aerobic exercise reduces exposure to pollution, improves cognitive function, and enhances BDNF levels in the elderly. Air Qual Atmos Health 15, 35–45 (2022). https://doi.org/10.1007/s11869-021-01083-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11869-021-01083-x