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Published in: European Journal of Applied Physiology 3/2015

01-03-2015 | Original Article

Once-weekly muscle endurance and strength training prevents deterioration of muscle oxidative function and attenuates the degree of strength decline during 3-week forearm immobilization

Authors: Toshiyuki Homma, Takafumi Hamaoka, Takuya Osada, Norio Murase, Ryotaro Kime, Yuko Kurosawa, Shiro Ichimura, Kazuki Esaki, Fumiko Nakamura, Toshihito Katsumura

Published in: European Journal of Applied Physiology | Issue 3/2015

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Abstract

Purpose

Muscle unloading causes muscle function deterioration, but the extent to which training frequency or volume can be reduced while preserving muscle function during muscle unloading is unknown. We examined the effects of low-volume muscle endurance and strength training on forearm muscle oxidative capacity, endurance, and strength during a 3-week immobilization.

Methods

Twenty-seven, healthy, male volunteers were divided into four groups: immobilization only (IMM); immobilization with endurance and strength training, once-weekly (IMM + EST1) or twice-weekly (IMM + EST2); and control, without immobilization or training (CNT). Endurance training involved dynamic handgrip exercise, at 30 % of maximal voluntary contraction (MVC), until exhaustion (~60 s). Strength training involved intermittent isometric handgrip exercise at 70 % MVC (40 s). Muscle oxidative capacity was evaluated after exercise using the phosphocreatine recovery time constant using 31phosphorus magnetic resonance spectroscopy. Endurance performance was evaluated according to the total work during dynamic handgrip exercise at 30 % MVC at 1 Hz until exhaustion.

Results

Muscle oxidative capacity and total work deterioration was restricted to the IMM (P < 0.05) group. MVC decreased in the IMM and IMM + EST1 (P < 0.05) groups. However, the MVC amplitude decrease in the IMM + EST1 group was smaller than that in the IMM (P < 0.05) group. MVC remained unchanged in the other groups.

Conclusion

During the 3-week immobilization, twice-weekly low-volume muscle endurance and strength training prevented deterioration in muscle strength, oxidative capacity, and endurance performance. Moreover, once-weekly muscle endurance and strength training prevented the deterioration of muscle oxidative capacity and endurance performance, and attenuated the degree of muscle strength decline.
Literature
go back to reference Akima H, Kawakami Y, Kubo K, Sekiguchi C, Ohshima H, Miyamoto A, Fukunaga T (2000) Effect of short-duration spaceflight on thigh and leg muscle volume. Med Sci Sports Exerc 32:1743–1747CrossRefPubMed Akima H, Kawakami Y, Kubo K, Sekiguchi C, Ohshima H, Miyamoto A, Fukunaga T (2000) Effect of short-duration spaceflight on thigh and leg muscle volume. Med Sci Sports Exerc 32:1743–1747CrossRefPubMed
go back to reference Akima H, Ushiyama J, Kubo J, Tonosaki S, Itoh M, Kawakami Y, Fukuoka H, Kanehisa H, Fukunaga T (2003) Resistance training during unweighting maintains muscle size and function in human calf. Med Sci Sports Exerc 35:655–662CrossRefPubMed Akima H, Ushiyama J, Kubo J, Tonosaki S, Itoh M, Kawakami Y, Fukuoka H, Kanehisa H, Fukunaga T (2003) Resistance training during unweighting maintains muscle size and function in human calf. Med Sci Sports Exerc 35:655–662CrossRefPubMed
go back to reference Alkner B, Tesch P (2004) Efficacy of a gravity-independent resistance exercise device as a countermeasure to muscle atrophy during 29-day bed rest. Acta Physiol Scand 181:345–357CrossRefPubMed Alkner B, Tesch P (2004) Efficacy of a gravity-independent resistance exercise device as a countermeasure to muscle atrophy during 29-day bed rest. Acta Physiol Scand 181:345–357CrossRefPubMed
go back to reference Belavý DL, Miokovic T, Armbrecht G, Richardson CA, Rittweger J, Felsenberg D (2009a) Differential atrophy of the lower-limb musculature during prolonged bed-rest. Eur J Appl Physiol 107:489–499CrossRefPubMed Belavý DL, Miokovic T, Armbrecht G, Richardson CA, Rittweger J, Felsenberg D (2009a) Differential atrophy of the lower-limb musculature during prolonged bed-rest. Eur J Appl Physiol 107:489–499CrossRefPubMed
go back to reference Belavý DL, Miokovic T, Armbrecht G, Rittweger J, Felsenberg D (2009b) Resistive vibration exercise reduces lower limb muscle atrophy during 56-day bed-rest. J Musculoskelet Neuronal Interact 9:225–235PubMed Belavý DL, Miokovic T, Armbrecht G, Rittweger J, Felsenberg D (2009b) Resistive vibration exercise reduces lower limb muscle atrophy during 56-day bed-rest. J Musculoskelet Neuronal Interact 9:225–235PubMed
go back to reference de Boer MD, Maganaris CN, Seynnes OR, Rennie MJ, Narici MV (2007) Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men. J Physiol 583:1079–1091CrossRefPubMedCentralPubMed de Boer MD, Maganaris CN, Seynnes OR, Rennie MJ, Narici MV (2007) Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men. J Physiol 583:1079–1091CrossRefPubMedCentralPubMed
go back to reference Deschenes M, Giles J, McCoy R, Volek J, Gomez A, Kraemer W (2002) Neural factors account for strength decrements observed after short-term muscle unloading. Am J Physiol Regul Integr Comp Physiol 282:R578–R583PubMed Deschenes M, Giles J, McCoy R, Volek J, Gomez A, Kraemer W (2002) Neural factors account for strength decrements observed after short-term muscle unloading. Am J Physiol Regul Integr Comp Physiol 282:R578–R583PubMed
go back to reference Edgerton V, Zhou M, Ohira Y, Klitgaard H, Jiang B, Bell G, Harris B, Saltin B, Gollnick P, Roy R, Day M, Greenisen M (1995) Human fiber size and enzymatic properties after 5 and 11 days of spaceflight. J Appl Physiol 78:1733–1739PubMed Edgerton V, Zhou M, Ohira Y, Klitgaard H, Jiang B, Bell G, Harris B, Saltin B, Gollnick P, Roy R, Day M, Greenisen M (1995) Human fiber size and enzymatic properties after 5 and 11 days of spaceflight. J Appl Physiol 78:1733–1739PubMed
go back to reference Ferretti G, Antonutto G, Denis C, Hoppeler H, Minetti A, Narici M, Desplanches D (1997) The interplay of central and peripheral factors in limiting maximal O2 consumption in man after prolonged bed rest. J Physiol 501:677–686CrossRefPubMedCentralPubMed Ferretti G, Antonutto G, Denis C, Hoppeler H, Minetti A, Narici M, Desplanches D (1997) The interplay of central and peripheral factors in limiting maximal O2 consumption in man after prolonged bed rest. J Physiol 501:677–686CrossRefPubMedCentralPubMed
go back to reference Hamaoka T, Katsumura T, Murase N, Kurosawa Y, Shimomitsu T, Kuwamori M, Kagaya A, Chance B (1998) Exercise induced improvement in muscle oxidative function in young females measured by 31phosphorus magnetic resonance spectroscopy (31P-MRS). Jpn J Appl Physiol 28:1–9 Hamaoka T, Katsumura T, Murase N, Kurosawa Y, Shimomitsu T, Kuwamori M, Kagaya A, Chance B (1998) Exercise induced improvement in muscle oxidative function in young females measured by 31phosphorus magnetic resonance spectroscopy (31P-MRS). Jpn J Appl Physiol 28:1–9
go back to reference Harris R, Hultman E, Nordesjo L (1974) Glycogen, glycolytic intermediates and high-energy phosphates determined in biopsy samples of musculus quadriceps femoris of man at rest. Methods and variance of values. Scand J Clin Lab Invest 33:109–120CrossRefPubMed Harris R, Hultman E, Nordesjo L (1974) Glycogen, glycolytic intermediates and high-energy phosphates determined in biopsy samples of musculus quadriceps femoris of man at rest. Methods and variance of values. Scand J Clin Lab Invest 33:109–120CrossRefPubMed
go back to reference Hickson R, Foster C, Pollock M, Galassi T, Rich S (1985) Reduced training intensities and loss of aerobic power, endurance, and cardiac growth. J Appl Physiol 58:492–499PubMed Hickson R, Foster C, Pollock M, Galassi T, Rich S (1985) Reduced training intensities and loss of aerobic power, endurance, and cardiac growth. J Appl Physiol 58:492–499PubMed
go back to reference Holm L, Reitelseder S, Pedersen T, Doessing S, Petersen S, Flyvbjerg A, Andersen J, Aagaard P, Kjaer M (2008) Changes in muscle size and MHC composition in response to resistance exercise with heavy and light loading intensity. J Appl Physiol 105:1454–1461CrossRefPubMed Holm L, Reitelseder S, Pedersen T, Doessing S, Petersen S, Flyvbjerg A, Andersen J, Aagaard P, Kjaer M (2008) Changes in muscle size and MHC composition in response to resistance exercise with heavy and light loading intensity. J Appl Physiol 105:1454–1461CrossRefPubMed
go back to reference Homma T, Hamaoka T, Murase N, Osada T, Murakami M, Kurosawa Y, Kitahara A, Ichimura S, Yashiro K, Katsumura T (2009) Low-volume muscle endurance training prevents decrease in muscle oxidative and endurance function during 21-day forearm immobilization. Acta Physiol (Oxf) 197:313–320CrossRef Homma T, Hamaoka T, Murase N, Osada T, Murakami M, Kurosawa Y, Kitahara A, Ichimura S, Yashiro K, Katsumura T (2009) Low-volume muscle endurance training prevents decrease in muscle oxidative and endurance function during 21-day forearm immobilization. Acta Physiol (Oxf) 197:313–320CrossRef
go back to reference Kawakami Y, Akima H, Kubo K, Muraoka Y, Hasegawa H, Kouzaki M, Imai M, Suzuki Y, Gunji A, Kanehisa H, Fukunaga T (2001) Changes in muscle size, architecture, and neural activation after 20 days of bed rest with and without resistance exercise. Eur J Appl Physiol 84:7–12CrossRefPubMed Kawakami Y, Akima H, Kubo K, Muraoka Y, Hasegawa H, Kouzaki M, Imai M, Suzuki Y, Gunji A, Kanehisa H, Fukunaga T (2001) Changes in muscle size, architecture, and neural activation after 20 days of bed rest with and without resistance exercise. Eur J Appl Physiol 84:7–12CrossRefPubMed
go back to reference Kitahara A, Hamaoka T, Murase N, Homma T, Kurosawa Y, Ueda C, Nagasawa T, Ichimura S, Motobe M, Yashiro K, Nakano S, Katsumura T (2003) Deterioration of muscle function after 21-day forearm immobilization. Med Sci Sports Exerc 35:1697–1702CrossRefPubMed Kitahara A, Hamaoka T, Murase N, Homma T, Kurosawa Y, Ueda C, Nagasawa T, Ichimura S, Motobe M, Yashiro K, Nakano S, Katsumura T (2003) Deterioration of muscle function after 21-day forearm immobilization. Med Sci Sports Exerc 35:1697–1702CrossRefPubMed
go back to reference Kushmerick M, Meyer R (1985) Chemical changes in rat leg muscle by phosphorus nuclear magnetic resonance. Am J Physiol 248:C542–C549PubMed Kushmerick M, Meyer R (1985) Chemical changes in rat leg muscle by phosphorus nuclear magnetic resonance. Am J Physiol 248:C542–C549PubMed
go back to reference LeBlanc A, Schneider V, Evans H, Pientok C, Rowe R, Spector E (1992) Regional changes in muscle mass following 17 weeks of bed rest. J Appl Physiol 73:2172–2178PubMed LeBlanc A, Schneider V, Evans H, Pientok C, Rowe R, Spector E (1992) Regional changes in muscle mass following 17 weeks of bed rest. J Appl Physiol 73:2172–2178PubMed
go back to reference LeBlanc A, Rowe R, Schneider V, Evans H, Hedrick T (1995) Regional muscle loss after short duration spaceflight. Aviat Space Environ Med 66:1151–1154PubMed LeBlanc A, Rowe R, Schneider V, Evans H, Hedrick T (1995) Regional muscle loss after short duration spaceflight. Aviat Space Environ Med 66:1151–1154PubMed
go back to reference Matsumura M, Ueda C, Shiroishi K, Esaki K, Ohmori F, Yamaguchi K, Ichimura S, Kurosawa Y, Kime R, Osada T, Murase N, Katsumura T, Hoshika A, Hamaoka T (2008) Low-volume muscular endurance and strength training during 3-week forearm immobilization was effective in preventing functional deterioration. Dyn Med 7:1CrossRefPubMedCentralPubMed Matsumura M, Ueda C, Shiroishi K, Esaki K, Ohmori F, Yamaguchi K, Ichimura S, Kurosawa Y, Kime R, Osada T, Murase N, Katsumura T, Hoshika A, Hamaoka T (2008) Low-volume muscular endurance and strength training during 3-week forearm immobilization was effective in preventing functional deterioration. Dyn Med 7:1CrossRefPubMedCentralPubMed
go back to reference McComas A (1994) Human neuromuscular adaptations that accompany changes in activity. Med Sci Sports Exerc 26:1498–1509CrossRefPubMed McComas A (1994) Human neuromuscular adaptations that accompany changes in activity. Med Sci Sports Exerc 26:1498–1509CrossRefPubMed
go back to reference McCully KK, Fielding RA, Evans WJ, Leigh JS Jr, Posner JD (1993) Relationships between in vivo and in vitro measurements of metabolism in young and old human calf muscles. J Appl Physiol 75:813–819PubMed McCully KK, Fielding RA, Evans WJ, Leigh JS Jr, Posner JD (1993) Relationships between in vivo and in vitro measurements of metabolism in young and old human calf muscles. J Appl Physiol 75:813–819PubMed
go back to reference Miles M, Clarkson P, Bean M, Ambach K, Mulroy J, Vincent K (1994) Muscle function at the wrist following 9 d of immobilization and suspension. Med Sci Sports Exerc 26:615–623CrossRefPubMed Miles M, Clarkson P, Bean M, Ambach K, Mulroy J, Vincent K (1994) Muscle function at the wrist following 9 d of immobilization and suspension. Med Sci Sports Exerc 26:615–623CrossRefPubMed
go back to reference Miokovic T, Armbrecht G, Felsenberg D, Belavý DL (2012) Heterogeneous atrophy occurs within individual lower limb muscles during 60 days of bed rest. J Appl Physiol 113:1545–1559CrossRefPubMed Miokovic T, Armbrecht G, Felsenberg D, Belavý DL (2012) Heterogeneous atrophy occurs within individual lower limb muscles during 60 days of bed rest. J Appl Physiol 113:1545–1559CrossRefPubMed
go back to reference Miokovic T, Armbrecht G, Gast U, Rawer R, Roth HJ, Runge M, Felsenberg D, Belavý DL (2014) Muscle atrophy, pain, and damage in bed rest reduced by resistive (vibration) exercise. Med Sci Sports Exerc 46:1506–1516CrossRefPubMed Miokovic T, Armbrecht G, Gast U, Rawer R, Roth HJ, Runge M, Felsenberg D, Belavý DL (2014) Muscle atrophy, pain, and damage in bed rest reduced by resistive (vibration) exercise. Med Sci Sports Exerc 46:1506–1516CrossRefPubMed
go back to reference Motobe M, Murase N, Osada T, Homma T, Ueda C, Nagasawa T, Kitahara A, Ichimura S, Kurosawa Y, Katsumura T, Hoshika A, Hamaoka T (2004) Noninvasive monitoring of deterioration in skeletal muscle function with forearm cast immobilization and the prevention of deterioration. Dyn Med 3:2CrossRefPubMedCentralPubMed Motobe M, Murase N, Osada T, Homma T, Ueda C, Nagasawa T, Kitahara A, Ichimura S, Kurosawa Y, Katsumura T, Hoshika A, Hamaoka T (2004) Noninvasive monitoring of deterioration in skeletal muscle function with forearm cast immobilization and the prevention of deterioration. Dyn Med 3:2CrossRefPubMedCentralPubMed
go back to reference Nielsen J, Suetta C, Hvid L, Schrøder H, Aagaard P, Ortenblad N (2010) Subcellular localization-dependent decrements in skeletal muscle glycogen and mitochondria content following short-term disuse in young and old men. Am J Physiol Endocrinol Metab 299:E1053–E1060CrossRefPubMed Nielsen J, Suetta C, Hvid L, Schrøder H, Aagaard P, Ortenblad N (2010) Subcellular localization-dependent decrements in skeletal muscle glycogen and mitochondria content following short-term disuse in young and old men. Am J Physiol Endocrinol Metab 299:E1053–E1060CrossRefPubMed
go back to reference Ohmori F, Hamaoka T, Shiroishi K, Osada T, Murase N, Kurosawa Y, Ichimura S, Homma T, Esaki K, Kime R, Katsumura T (2010) Low-volume strength and endurance training prevent the decrease in exercise hyperemia induced by non-dominant forearm immobilization. Eur J Appl Physiol 110:845–851CrossRefPubMed Ohmori F, Hamaoka T, Shiroishi K, Osada T, Murase N, Kurosawa Y, Ichimura S, Homma T, Esaki K, Kime R, Katsumura T (2010) Low-volume strength and endurance training prevent the decrease in exercise hyperemia induced by non-dominant forearm immobilization. Eur J Appl Physiol 110:845–851CrossRefPubMed
go back to reference Paganini A, Foley J, Meyer R (1997) Linear dependence of muscle phosphocreatine kinetics on oxidative capacity. Am J Physiol 272:C501–C510PubMed Paganini A, Foley J, Meyer R (1997) Linear dependence of muscle phosphocreatine kinetics on oxidative capacity. Am J Physiol 272:C501–C510PubMed
go back to reference Pesta D, Hoppel F, Macek C, Messner H, Faulhaber M, Kobel C, Parson W, Burtscher M, Schocke M, Gnaiger E (2011) Similar qualitative and quantitative changes of mitochondrial respiration following strength and endurance training in normoxia and hypoxia in sedentary humans. Am J Physiol Regul Integr Comp Physiol 301:R1078–R1087CrossRefPubMed Pesta D, Hoppel F, Macek C, Messner H, Faulhaber M, Kobel C, Parson W, Burtscher M, Schocke M, Gnaiger E (2011) Similar qualitative and quantitative changes of mitochondrial respiration following strength and endurance training in normoxia and hypoxia in sedentary humans. Am J Physiol Regul Integr Comp Physiol 301:R1078–R1087CrossRefPubMed
go back to reference Sako T, Hamaoka T, Higuchi H, Kurosawa Y, Katsumura T (2001) Validity of NIR spectroscopy for quantitatively measuring muscle oxidative metabolic rate in exercise. J Appl Physiol 90:338–344PubMed Sako T, Hamaoka T, Higuchi H, Kurosawa Y, Katsumura T (2001) Validity of NIR spectroscopy for quantitatively measuring muscle oxidative metabolic rate in exercise. J Appl Physiol 90:338–344PubMed
go back to reference Schulze K, Gallagher P, Trappe S (2002) Resistance training preserves skeletal muscle function during unloading in humans. Med Sci Sports Exerc 34:303–313CrossRefPubMed Schulze K, Gallagher P, Trappe S (2002) Resistance training preserves skeletal muscle function during unloading in humans. Med Sci Sports Exerc 34:303–313CrossRefPubMed
go back to reference Shackelford LC, LeBlanc AD, Driscoll TB, Evans HJ, Rianon NJ, Smith SM, Spector E, Feeback DL, Lai D (2004) Resistance exercise as a countermeasure to disuse-induced bone loss. J Appl Physiol 97:119–129CrossRefPubMed Shackelford LC, LeBlanc AD, Driscoll TB, Evans HJ, Rianon NJ, Smith SM, Spector E, Feeback DL, Lai D (2004) Resistance exercise as a countermeasure to disuse-induced bone loss. J Appl Physiol 97:119–129CrossRefPubMed
go back to reference Tesch P, Trieschmann J, Ekberg A (2004) Hypertrophy of chronically unloaded muscle subjected to resistance exercise. J Appl Physiol 96:1451–1458CrossRefPubMed Tesch P, Trieschmann J, Ekberg A (2004) Hypertrophy of chronically unloaded muscle subjected to resistance exercise. J Appl Physiol 96:1451–1458CrossRefPubMed
go back to reference Trappe S, Creer A, Minchev K, Slivka D, Louis E, Luden N, Trappe T (2008) Human soleus single muscle fiber function with exercise or nutrition countermeasures during 60 days of bed rest. Am J Physiol Regul Integr Comp Physiol 294:R939–R947CrossRefPubMed Trappe S, Creer A, Minchev K, Slivka D, Louis E, Luden N, Trappe T (2008) Human soleus single muscle fiber function with exercise or nutrition countermeasures during 60 days of bed rest. Am J Physiol Regul Integr Comp Physiol 294:R939–R947CrossRefPubMed
go back to reference Wang L, Mascher H, Psilander N, Blomstrand E, Sahlin K (2011) Resistance exercise enhances the molecular signaling of mitochondrial biogenesis induced by endurance exercise in human skeletal muscle. J Appl Physiol 111:1335–1344CrossRefPubMed Wang L, Mascher H, Psilander N, Blomstrand E, Sahlin K (2011) Resistance exercise enhances the molecular signaling of mitochondrial biogenesis induced by endurance exercise in human skeletal muscle. J Appl Physiol 111:1335–1344CrossRefPubMed
Metadata
Title
Once-weekly muscle endurance and strength training prevents deterioration of muscle oxidative function and attenuates the degree of strength decline during 3-week forearm immobilization
Authors
Toshiyuki Homma
Takafumi Hamaoka
Takuya Osada
Norio Murase
Ryotaro Kime
Yuko Kurosawa
Shiro Ichimura
Kazuki Esaki
Fumiko Nakamura
Toshihito Katsumura
Publication date
01-03-2015
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Applied Physiology / Issue 3/2015
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-014-3029-0

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