Relationship Between Physical Activity and Intramyocellular Lipid Content Is Different Between Young and Older Adults

European Journal of Applied Physiology (2019) 119:113–122 https://doi.org/10.1007/s00421-018-4005-x ORIGINAL ARTICLE Relationship between physical activity and intramyocellular lipid content is different between young and older adults Maya Hioki1 · Nana Kanehira2 · Teruhiko Koike3 · Akira Saito4,5 · Hideyuki Takahashi6 · Kiyoshi Shimaoka7 · Hisataka Sakakibara1 · Yoshiharu Oshida3 · Hiroshi Akima3 Received: 26 March 2018 / Accepted: 1 October 2018 / Published online: 10 October 2018 © Springer-Verlag GmbH Germany, part of Springer Nature 2018 Abstract Purpose Intramyocellular lipid (IMCL) is influenced by physical exercise; however, whether the habitual level of physical activity affects resting IMCL content remains unclear. The purpose of this study was to determine the relationship between physical activity levels and resting IMCL content in young and older adults. Methods In total, 15 nonobese young adults (21.0 ± 0.0 years) and 15 older adults (70.7 ± 3.8 years) were recruited. Time spent performing physical activities for 10 days was assessed using a three-dimensional ambulatory accelerometer, and intensity was categorized as light [< 3.0 metabolic equivalents (METs)], moderate (3.0–6.0 METs), or vigorous (> 6.0 METs). Physical activity level was calculated as the product of METs and time spent performing physical activities (MET h) at each intensity level. The IMCL content in the vastus lateralis was determined using 1H-magnetic resonance spectroscopy after overnight fasting. Results No significant differences in IMCL content were observed between young and older adults. Vigorous intensity physical activity (time and MET h) was significantly lower in older than young adults (p < 0.01); this difference was not observed for light and moderate intensity physical activity. Light intensity physical activity (time and MET h) was significantly and inversely correlated with IMCL content in young adults (r = − 0.59 and r = − 0.58; both p < 0.05), but not in older adults. Conclusions These results suggest that daily light intensity physical activity reduces resting IMCL content in young adults, whereas no significant relationship was seen between daily physical activity and resting IMCL content in older adults. Keywords Metabolism · Metabolic equivalent · 1H-magnetic resonance spectroscopy · Aging · Skeletal muscle · Daily living Abbreviations MET Metabolic equivalent EMCL Extramyocellular lipid MET h Metabolic equivalent × hours VO FFA Free fatty acid 2 max Maximum oxygen uptake 1H-MRS Magnetic resonance spectroscopy VL Vastus lateralis IMCL Intramyocellular lipid IMTG Intramyocellular triglyceride Communicated by Fabio Fischetti. * Maya Hioki 4 Graduate School of Arts and Sciences, College of Arts [email protected] and Sciences, University of Tokyo, Komaba 3-8-1 Meguro-ku, Tokyo 153-8092, Japan 1 Graduate School of Medicine, Nagoya University, 65 5 Japan Society for the Promotion of Science, Kojimachi, Tsurumai, Showa-ku, Nagoya, Aichi 466-8550, Japan Chiyoda-ku, Tokyo, Japan 2 Department of Health and Nutrition, Tokaigakuen University, 6 Japan Institute of Sports Sciences, 3-15-1 Nishigaoka, 2-901 Nakahira, Tenpaku, Nagoya, Aichi 468-8514, Japan Kita-ku, Tokyo 115-0056, Japan 3 Research Center of Health, Physical Fitness and Sports, 7 Department of Human Wellness, Tokaigakuen University, Nagoya University, 1 Furo, Chikusa-ku, Nagoya, 21-233 Nishinohora, Ukigai, Miyoshi, Aichi 470-0207, Japan Aichi 464-8601, Japan Vol.:(0123456789)1 3 114 European Journal of Applied Physiology (2019) 119:113–122 Introduction decrease in the amount of mitochondria and/or lower enzyme activities involved in lipid oxidation. By contrast, Lipids, which are hydrophobic molecules, play an impor- physically active older adults have a high lipid oxidation tant physiologic role by supplying energy substrates dur- capacity and IMCL uptake (Rouffet et al. 2013). Increased ing physical activity. During light to vigorous intensity adiposity and lower habitual levels of physical activity physical activity, plasma free fatty acid (FFA) is the also affect lipid oxidation in older individuals (Boon et al. energy source responsible for approximately 20–80% of 2007). Therefore, physical activity levels might decrease the energy expended to produce adenosine triphosphate IMCL content significantly in older adults; however, this in mitochondria (Egan and Zierath 2013; Romijn et al. process remains poorly understood. 1993). Excessive FFA is re-esterified in myocytes and The present study therefore investigated the relation- stored as intramyocellular lipid (IMCL) for future use as ship between physical activity and resting IMCL content in a metabolic fuel (Coen and Goodpaster 2012; Jensen et al. young and older adults. Physical activity level was expressed 2001). 1H-magnetic resonance spectroscopy (1H-MRS) as time and MET h. We hypothesized that physical activity and muscle tissue samples obtained using needle biopsy (time and MET h) would correlate with resting IMCL con- have shown that IMCL decreases after aerobic endurance tent in young but not older adults. IMCL accumulation is a exercise (Bucher et al. 2014; Egger et al. 2013; Van Pro- major factor in inducing skeletal muscle insulin resistance eyen et al. 2011; White et al. 2003a, b) and resistance (Goodpaster and Sparks 2017). Therefore, elucidating dif- exercise (Koopman et al. 2006; Shepherd et al. 2014) in ferences in the relationship between physical activity and healthy participants. This evidence clearly shows that IMCL content in older and young adults is an important step IMCL is used as a fuel during endurance and resistance in understanding the causes of abnormal IMCL accumula- types of exercise. tion with aging, which may promote better health in adults. Exercise time and intensity are important determinants of the physiologic responses to exercise training (Garber et al. 2011). Plasma FFA oxidation accounts for almost all fat oxidation that occurs during light intensity exer- Methods VO cise (25% of maximum oxygen uptake [ 2 max]), whereas intramyocellular triglycerides (IMTGs) are an important Participants fuel during prolonged (> 90 min) moderate intensity exercise and provide 25% of total energy; however, they tend Fifteen young (eight men, seven women; all 21 years of age) to contribute less during low and high intensity exercise and 15 older adults (seven men, eight women; age range, (Egan and Zierath 2013). Sedentary and light intensity 65–78 years) who were living independently participated in physical activities comprise a relatively large portion the present study. Athletes with good endurance or resistance (97%) of the daily activities performed by men and women training (marathon runners or sprinters) who were partici- aged 20–79 years compared with moderate to vigorous pating in competitive sports were excluded from the study. intensity physical activity intensity (3%) (Colley et al. The older adults exercised once a week in local sports clubs 2011). Therefore, IMCL oxidation depends on the time designed specifically for older people. Participants with a and intensity of physical activities in daily living, i.e., history of heart disease (e.g., myocardial infarction, angina metabolic equivalents (METs) × hours (MET h). pectoris, cardiac insufficiency), cerebrovascular disease Aging induces an imbalance between muscle lipid (e.g., cerebral infarction, hemorrhage), or extreme hyper- delivery and oxidation (Chee et al. 2016). According tension (e.g., systolic blood pressure ≥ 180 mmHg, diastolic to Sial et al. (1996), when young and older adults per- blood pressure ≥ 110 mmHg) were excluded. The clinical formed similar, relatively intense, moderate exercise [50% histories of the older adults were assessed using question- VO 2 max ], FFA oxidation was lower and carbohydrate oxida- naires. Among four participants with type 2 diabetes, one tion was higher in older adults. Moreover, despite similar was receiving an α-glucosidase inhibitor and thiazolidin- physical activity patterns in older and young adults, IMCL edione, one a dipeptidyl peptidase inhibitor, and two were content was higher in older adults (Crane et al. 2010). medicated with metformin. The menstrual cycle histories These results suggest that aging may affect the relation- of the young women were determined using questionnaires. 1 ship between physical activity levels and IMCL content. H-MRS was performed during the follicular phase of their Our previous study (Hioki et al. 2016) demonstrated that menstrual cycle. fasting FFA correlated with IMCL in young but not older All participants provided written informed consent to par- adults. These results suggest that an imbalance between ticipate in this study, which was conducted according to the circulating FFA and IMCL can be caused by an age-related Declaration of Helsinki and approved by the Ethics Commit- tee of the Graduate School of Medicine, Nagoya University. 1 3 European Journal of Applied Physiology (2019) 119:113–122 115 Parts of the data have been previously reported (Akima et al. METs), and vigorous intensity (> 6.0 METs) (Kumahara 2015, 2016; Hioki et al. 2016; Yoshiko et al. 2017). et al. 2004). The accelerometer was worn on either the left or right Study design side of the belt at waist level during physical activity, but was not worn while bathing or sleeping. We instructed that The study protocol consisted of measuring body composi- the accelerometer was to be kept horizontal throughout the tion and assessing IMCL by 1H-MRS in the morning in all

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