https://doi.org/10.4081/ejtm.2023.12012
Can lifelong endurance exercise improve ageing through beneficial effects on circadian timing function, muscular performance and health status in men? Protocol for a comparative cross-sectional study
Submitted: 26 October 2023
Accepted: 21 November 2023
Published: 5 December 2023
Accepted: 21 November 2023
Abstract Views: 2439
PDF: 826
HTML: 8
HTML: 8
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
A well-synchronized circadian system is a manifestation of an individual's health. A gradual weakening of the circadian timing function characterizes aging. Regular exercise has been suggested as a modality to improve many detrimental changes associated with aging. Therefore, we aim to examine the benefits and risks of lifelong endurance exercise on age-dependent changes in the circadian time-keeping function, the performance of the muscular system and health status. The study protocol has a comparative cross-sectional design, including groups of senior (65 to 75 years old, n=16) and young (20-30 years old, n=16) endurance runners and triathletes. Age-matched groups of young and elderly sedentary men are included as controls. The circadian function is evaluated mainly by measurement of urinary 6-sulphatoxymelatonin, a metabolite of the hormone melatonin shown to participate in the modulation of sleep cycles. The 6-sulphatoxymelatonin will be assessed in urine samples collected upon awakening in the morning and in the late evening, as a marker of melatonin production. In addition, sleep/activity rhythms and sleep quality will be measured by wrist actigraphy. Performance of the muscular system will be assessed by examination of muscular strength and quantifying of gene expression in the skeletal muscle tissue samples. Health status and age-induced reduction in immune function are to be analysed via the balance of pro- and anti-inflammatory immune markers in the plasma and skeletal muscle, body composition, bone density and physical fitness.
Giacomoni M, Edwards B, Bambaeichi E. Gender differences in the circadian variations in muscle strength assessed with and without superimposed electrical twitches. Ergonomics. 2005 Sep 15-Nov 15;48(11-14):1473-87. PMID: 16338714.
DOI: https://doi.org/10.1080/00140130500101452
Küüsmaa M, Sedliak M, Häkkinen K. Effects of time-of-day on neuromuscular function in untrained men: Specific responses of high morning performers and high evening performers. Chronobiol Int. 2015;32(8):1115-24. Epub 2015 Sep 11. PMID: 26361893.
DOI: https://doi.org/10.3109/07420528.2015.1065269
Mora-Rodríguez R, García Pallarés J, López-Samanes Á, Ortega JF, Fernández-Elías VE. Caffeine ingestion reverses the circadian rhythm effects on neuromuscular performance in highly resistance-trained men. PLoS One. 2012;7(4):e33807. Epub 2012 Apr 4. PMID: 22496767; PMCID: PMC3319538.
DOI: https://doi.org/10.1371/journal.pone.0033807
Sedliak M, Finni T, Cheng S, Haikarainen T, Häkkinen K. Diurnal variation in maximal and submaximal strength, power and neural activation of leg extensors in men: multiple sampling across two consecutive days. Int J Sports Med. 2008 Mar;29(3):217-24. Epub 2007 Jul 5. PMID: 17614012.
DOI: https://doi.org/10.1055/s-2007-965125
Amaro-Gahete FJ, Jurado-Fasoli L, Triviño AR, Sanchez-Delgado G, De-la-O A, Helge JW, Ruiz JR. Diurnal Variation of Maximal Fat-Oxidation Rate in Trained Male Athletes. Int J Sports Physiol Perform. 2019 Sep 1;14(8):1140-1146. PMID: 30702364.
DOI: https://doi.org/10.1123/ijspp.2018-0854
Basti A, Yalçin M, Herms D, Hesse J, Aboumanify O, Li Y, Aretz Z, Garmshausen J, El-Athman R, Hastermann M, Blottner D, Relógio A. Diurnal variations in the expression of core-clock genes correlate with resting muscle properties and predict fluctuations in exercise performance across the day. BMJ Open Sport Exerc Med. 2021 Feb 10;7(1):e000876. PMID: 33680499; PMCID: PMC7878143.
DOI: https://doi.org/10.1136/bmjsem-2020-000876
Dyar KA, Ciciliot S, Wright LE, Biensø RS, Tagliazucchi GM, Patel VR, Forcato M, Paz MI, Gudiksen A, Solagna F, Albiero M, Moretti I, Eckel-Mahan KL, Baldi P, Sassone-Corsi P, Rizzuto R, Bicciato S, Pilegaard H, Blaauw B, Schiaffino S. Muscle insulin sensitivity and glucose metabolism are controlled by the intrinsic muscle clock. Mol Metab. 2013 Oct 23;3(1):29-41. Erratum in: Mol Metab. 2014 Dec;3(9):857. PMID: 24567902; PMCID: PMC3929910.
DOI: https://doi.org/10.1016/j.molmet.2014.09.002
Perrin L, Loizides-Mangold U, Skarupelova S, Pulimeno P, Chanon S, Robert M, Bouzakri K, Modoux C, Roux-Lombard P, Vidal H, Lefai E, Dibner C. Human skeletal myotubes display a cell-autonomous circadian clock implicated in basal myokine secretion. Mol Metab. 2015 Aug 6;4(11):834-45. PMID: 26629407; PMCID: PMC4632112.
DOI: https://doi.org/10.1016/j.molmet.2015.07.009
van Moorsel D, Hansen J, Havekes B, Scheer FAJL, Jörgensen JA, Hoeks J, Schrauwen-Hinderling VB, Duez H, Lefebvre P, Schaper NC, Hesselink MKC, Staels B, Schrauwen P. Demonstration of a day-night rhythm in human skeletal muscle oxidative capacity. Mol Metab. 2016 Jul 1;5(8):635-645. PMID: 27656401; PMCID: PMC5021670.
DOI: https://doi.org/10.1016/j.molmet.2016.06.012
Perrin L, Loizides-Mangold U, Chanon S, Gobet C, Hulo N, Isenegger L, Weger BD, Migliavacca E, Charpagne A, Betts JA, Walhin JP, Templeman I, Stokes K, Thompson D, Tsintzas K, Robert M, Howald C, Riezman H, Feige JN, Karagounis LG, Johnston JD, Dermitzakis ET, Gachon F, Lefai E, Dibner C. Transcriptomic analyses reveal rhythmic and CLOCK-driven pathways in human skeletal muscle. Elife. 2018 Apr 16;7:e34114. PMID: 29658882; PMCID: PMC5902165.
DOI: https://doi.org/10.7554/eLife.34114
Sedliak M, Finni T, Cheng S, Kraemer WJ, Häkkinen K. Effect of time-of-day-specific strength training on serum hormone concentrations and isometric strength in men. Chronobiol Int. 2007;24(6):1159-77. PMID: 18075805.
DOI: https://doi.org/10.1080/07420520701800686
Sedliak M, Finni T, Cheng S, Lind M, Häkkinen K. Effect of time-of-day-specific strength training on muscular hypertrophy in men. J Strength Cond Res. 2009 Dec;23(9):2451-7. PMID: 19910830.
DOI: https://doi.org/10.1519/JSC.0b013e3181bb7388
Sedliak M, Zeman M, Buzgó G, Cvecka J, Hamar D, Laczo E, Okuliarova M, Vanderka M, Kampmiller T, Häkkinen K, Ahtiainen JP, Hulmi JJ, Nilsen TS, Wiig H, Raastad T. Morphological, molecular and hormonal adaptations to early morning versus afternoon resistance training. Chronobiol Int. 2018 Apr;35(4):450-464. Epub 2017 Dec 28. PMID: 29283292.
DOI: https://doi.org/10.1080/07420528.2017.1411360
Mirizio GG, Nunes RSM, Vargas DA, Foster C, Vieira E. Time-of-Day Effects on Short-Duration Maximal Exercise Performance. Sci Rep. 2020 Jun 11;10(1):9485. PMID: 32528038; PMCID: PMC7289891.
DOI: https://doi.org/10.1038/s41598-020-66342-w
Cornelissen G, Otsuka K. Chronobiology of Aging: A Mini-Review. Gerontology. 2017;63(2):118-128. Epub 2016 Oct 22. PMID: 27771728.
DOI: https://doi.org/10.1159/000450945
Zhao J, Warman GR, Cheeseman JF. The functional changes of the circadian system organization in aging. Ageing Res Rev. 2019 Jul;52:64-71. Epub 2019 Apr 29. PMID: 31048031.
DOI: https://doi.org/10.1016/j.arr.2019.04.006
Cipolla-Neto J, Amaral FGD. Melatonin as a Hormone: New Physiological and Clinical Insights. Endocr Rev. 2018 Dec 1;39(6):990-1028. PMID: 30215696.
DOI: https://doi.org/10.1210/er.2018-00084
Khullar, A. The role of melatonin in the circadian rhythm sleep-wake cycle. Psychiatric Times. 2012;29(7):26-27,30-32.
Yoshida K, Hashiramoto A, Okano T, Yamane T, Shibanuma N, Shiozawa S. TNF-α modulates expression of the circadian clock gene Per2 in rheumatoid synovial cells. Scand J Rheumatol. 2013;42(4):276-80. Epub 2013 Mar 16. PMID: 23496259.
DOI: https://doi.org/10.3109/03009742.2013.765031
Yoshida K, Nakai A, Kaneshiro K, Hashimoto N, Suzuki K, Uchida K, Hashimoto T, Kawasaki Y, Tateishi K, Nakagawa N, Shibanuma N, Sakai Y, Hashiramoto A. TNF-α induces expression of the circadian clock gene Bmal1 via dual calcium-dependent pathways in rheumatoid synovial cells. Biochem Biophys Res Commun. 2018 Jan 8;495(2):1675-1680. Epub 2017 Dec 5. PMID: 29217191.
DOI: https://doi.org/10.1016/j.bbrc.2017.12.015
Narasimamurthy R, Hatori M, Nayak SK, Liu F, Panda S, Verma IM. Circadian clock protein cryptochrome regulates the expression of proinflammatory cytokines. Proc Natl Acad Sci U S A. 2012 Jul 31;109(31):12662-7. Epub 2012 Jul 9. PMID: 22778400; PMCID: PMC3411996.
DOI: https://doi.org/10.1073/pnas.1209965109
Spengler ML, Kuropatwinski KK, Comas M, Gasparian AV, Fedtsova N, Gleiberman AS, Gitlin II, Artemicheva NM, Deluca KA, Gudkov AV, Antoch MP. Core circadian protein CLOCK is a positive regulator of NF-κB-mediated transcription. Proc Natl Acad Sci U S A. 2012 Sep 11;109(37):E2457-65. Epub 2012 Aug 15. PMID: 22895791; PMCID: PMC3443185.
DOI: https://doi.org/10.1073/pnas.1206274109
de Souza Teixeira AA, Lira FS, Rosa-Neto JC. Aging with rhythmicity. Is it possible? Physical exercise as a pacemaker. Life Sci. 2020 Nov 15;261:118453. Epub 2020 Sep 18. PMID: 32956663; PMCID: PMC7500276.
DOI: https://doi.org/10.1016/j.lfs.2020.118453
Gabriel BM, Zierath JR. Circadian rhythms and exercise - re-setting the clock in metabolic disease. Nat Rev Endocrinol. 2019 Apr;15(4):197-206. PMID: 30655625.
DOI: https://doi.org/10.1038/s41574-018-0150-x
Choi Y, Cho J, No MH, Heo JW, Cho EJ, Chang E, Park DH, Kang JH, Kwak HB. Re-Setting the Circadian Clock Using Exercise against Sarcopenia. Int J Mol Sci. 2020 Apr 28;21(9):3106. PMID: 32354038; PMCID: PMC7247148.
DOI: https://doi.org/10.3390/ijms21093106
Schmitt EE, Johnson EC, Yusifova M, Bruns DR. The renal molecular clock: broken by aging and restored by exercise. Am J Physiol Renal Physiol. 2019 Nov 1;317(5):F1087-F1093. Epub 2019 Aug 28. PMID: 31461350; PMCID: PMC6879930.
DOI: https://doi.org/10.1152/ajprenal.00301.2019
Gaskell SK, Rauch CE, Parr A, Costa RJS. Diurnal versus Nocturnal Exercise-Effect on the Gastrointestinal Tract. Med Sci Sports Exerc. 2021 May 1;53(5):1056-1067. PMID: 33065594.
DOI: https://doi.org/10.1249/MSS.0000000000002546
Youngstedt SD, Elliott JA, Kripke DF. Human circadian phase-response curves for exercise. J Physiol. 2019 Apr;597(8):2253-2268. Epub 2019 Mar 18. PMID: 30784068; PMCID: PMC6462487.
DOI: https://doi.org/10.1113/JP276943
Elbaz M, Yauy K, Metlaine A, Martoni M, Léger D. Validation of a new actigraph motion watch versus polysomnography on 70 healthy and suspected sleepdisordered subjects. In Universite Paris Descartes. 2012. (Vol. 21, Issue 2001).
Littner M, Kushida CA, Anderson WM, Bailey D, Berry RB, Davila DG, Hirshkowitz M, Kapen S, Kramer M, Loube D, Wise M, Johnson SF; Standards of Practice Committee of the American Academy of Sleep Medicine. Practice parameters for the role of actigraphy in the study of sleep and circadian rhythms: an update for 2002. Sleep. 2003 May 1;26(3):337-41. PMID: 12749556.
DOI: https://doi.org/10.1093/sleep/26.3.337
Folkard S, Monk TH, Lobban MC. Towards a predictive test of adjustment to shift work. Ergonomics. 1979 Jan;22(1):79-91. PMID: 436816.
DOI: https://doi.org/10.1080/00140137908924591
Sousa VD, Rojjanasrirat W. Translation, adaptation and validation of instruments or scales for use in cross-cultural health care research: a clear and user-friendly guideline. J Eval Clin Pract. 2011 Apr;17(2):268-74. Epub 2010 Sep 28. PMID: 20874835.
DOI: https://doi.org/10.1111/j.1365-2753.2010.01434.x
Bily W, Franz C, Trimmel L, Loefler S, Cvecka J, Zampieri S, Kasche W, Sarabon N, Zenz P, Kern H. Effects of Leg-Press Training With Moderate Vibration on Muscle Strength, Pain, and Function After Total Knee Arthroplasty: A Randomized Controlled Trial. Arch Phys Med Rehabil. 2016 Jun;97(6):857-65. Epub 2016 Jan 4. PMID: 26763947.
DOI: https://doi.org/10.1016/j.apmr.2015.12.015
Kralik M, Cvecka J, Buzgo G, Putala M, Ukropcova B, Ukropec J, Killinger Z, Payer J, Kollarik B, Bujdak P, Raastad T, Sedliak M. Strength training as a supplemental therapy for androgen deficiency of the aging male (ADAM): study protocol for a three-arm clinical trial. BMJ Open. 2019 Sep 5;9(9):e025991. PMID: 31492775; PMCID: PMC6731925.
DOI: https://doi.org/10.1136/bmjopen-2018-025991
Sarabon N, Rosker J, Fruhmann H, Burggraf S, Loefler S, Kern H. Reliability of maximal voluntary contraction related parameters measured by a novel portable isometric knee dynamometer. Phys Medizin Rehabil Kurortmedizin. 2013;23(1).
DOI: https://doi.org/10.1055/s-0032-1331190
Sarabon N, Loefler S, Cvecka J, Sedliak M, Kern H. Strength training in elderly people improves static balance: a randomized controlled trial. Eur J Transl Myol. 2013;23(3).
DOI: https://doi.org/10.4081/bam.2013.3.85
Shanely RA, Zwetsloot KA, Triplett NT, Meaney MP, Farris GE, Nieman DC. Human skeletal muscle biopsy procedures using the modified Bergström technique. J Vis Exp. 2014 Sep 10;(91):51812. PMID: 25285722; PMCID: PMC4828068.
DOI: https://doi.org/10.3791/51812
Lavin KM, Perkins RK, Jemiolo B, Raue U, Trappe SW, Trappe TA. Effects of aging and lifelong aerobic exercise on basal and exercise-induced inflammation. J Appl Physiol (1985). 2020 Jan 1;128(1):87-99. Epub 2019 Nov 21. PMID: 31751180; PMCID: PMC6985808.
DOI: https://doi.org/10.1152/japplphysiol.00495.2019
Hopkins WG. A scale of magnitudes for effect statistics. Sportscience. 2002;5.
Hopkins WG, Marshall SW, Batterham AM, Hanin J. Progressive statistics for studies in sports medicine and exercise science. Med Sci Sports Exerc. 2009 Jan;41(1):3-13. PMID: 19092709.
DOI: https://doi.org/10.1249/MSS.0b013e31818cb278
Chan AW, Tetzlaff JM, Gøtzsche PC, Altman DG, Mann H, Berlin JA, Dickersin K, Hróbjartsson A, Schulz KF, Parulekar WR, Krleza-Jeric K, Laupacis A, Moher D. SPIRIT 2013 explanation and elaboration: guidance for protocols of clinical trials. BMJ. 2013 Jan 8;346:e7586. PMID: 23303884; PMCID: PMC3541470.
DOI: https://doi.org/10.1136/bmj.e7586
How to Cite
Berisha, G., Sedliak, M., Zeman, M., Hamar, D., Cvečka, J., Tirpáková, V., Vajda, M., Oreská, Ľudmila, Černáčková, A., Čupka, M., Šarabon, N., Protasi, F., Zampieri, S., Kern, H., Lofler, S., Musaro, A., Stebelová, K., & Okuliarová, M. (2023). Can lifelong endurance exercise improve ageing through beneficial effects on circadian timing function, muscular performance and health status in men? Protocol for a comparative cross-sectional study. European Journal of Translational Myology, 33(4). https://doi.org/10.4081/ejtm.2023.12012
Copyright (c) 2023 the Author(s)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.