Reeves 2006


Published on

Published in: Health & Medicine
  • Be the first to comment

  • Be the first to like this

No Downloads
Total views
On SlideShare
From Embeds
Number of Embeds
Embeds 0
No embeds

No notes for slide

Reeves 2006

  1. 1. ARTICLE IN PRESS Manual Therapy 11 (2006) 192–196 Original article Musculoskeletal adaptations to resistance training in old age N.D. ReevesÃ, M.V. Narici, C.N. Maganaris Institute for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, MMU Cheshire, Alsager Campus, Hassall Road, Alsager, Cheshire ST7 2HL, UK Received 27 October 2005; accepted 6 April 2006 Abstract Muscle weakness experienced in old age has many detrimental consequences for activities of daily life. Given the serious problems presented by weakness in old age, strategies to prevent or mitigate this process are of paramount importance. In recent years resistance training has emerged as an effective method for increasing strength in the elderly. Despite this, little is known regarding the muscular, neural and tendinous adaptations that occur with resistance training in old age. Hence, we have conducted a series of experiments to investigate these adaptations. We have found increases in maximal isometric and concentric torque by 9–37% after resistance training in older people (65–81 years). Associated with these strength gains were increases in agonist muscle neural drive without any change in the co-activation of antagonist muscles. Resistance training can cause increases in muscle size and also adaptations to the internal muscle structure. Tendons of older adults adapt to resistance training by increasing their stiffness and Young’s modulus. In conclusion, many of the musculoskeletal factors characterizing ageing can be at least partially mitigated by resistance training. r 2006 Elsevier Ltd. All rights reserved. Keywords: Old age; Exercise; Muscle; Tendon Ageing is characterized by a loss of muscle size known 1999; Frontera et al., 2000). This is primarily important as senile sarcopenia and a progressive decline in strength because the extensors of the knee and ankle are the that accelerates after the sixth decade of life. Cross- major muscle groups responsible for locomotion and sectional comparisons of young and older adults have will therefore impact upon many activities of daily shown that adults 70–80 years of age are 40% weaker living. For example, the loss of leg extension power with in terms of knee extension and plantarflexion torque as ageing has been shown to correlate with the decline in compared to young adults 20–30 years of age (Roos maximal gait velocity (Rantanen and Avela, 1997). As et al., 1999; Klein et al., 2001; Macaluso et al., 2002; maximal leg extension power (normalized to body mass) Morse et al., 2004). Senile sarcopenia affecting various declines, the maximal attainable gait velocity also muscle groups is evident from cross-sectional studies declines. Power (the product of joint torque and showing that muscle size is 20% smaller in older adults velocity) declines at a faster rate than joint torque with as compared to young adults (Klein et al., 2001; Narici ageing (Skelton et al., 1994), likely due to the fact that et al., 2003; Morse et al., 2004). The extensor muscle not only strength (joint torque) declines with ageing but groups, particularly the knee and ankle extensors are also the velocity of muscle shortening. Given the most severely affected by ageing-induced declines in detrimental consequences of muscle weakness in old strength and size (Winegard et al., 1996; Lynch et al., age described above, it is of paramount importance to find ways in which this ageing-induced strength decline ÃCorresponding author. Tel.: +44 161 2475429; can be delayed or even reversed to a certain extent. fax: +44 161 2476375. In relatively recent years resistance exercise training E-mail address: (N.D. Reeves). has been shown as an effective method for reducing 1356-689X/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2006.04.004
  2. 2. ARTICLE IN PRESS N.D. Reeves et al. / Manual Therapy 11 (2006) 192–196 193 ageing-induced muscle weakness (for review see Maca- luso and De Vito, 2004). Perhaps contrary to popular belief, strength gains can be achieved in old age and have been observed in 70–80 year old adults following resistance exercise training programmes (e.g. Fiatarone et al., 1990). Many studies however, have assessed strength only in terms of the repetition maximum on the exercise device used for training. Whilst this will clearly provide an important indication of any possible strength gains occurring with exercise training, due to the specific nature of the task it is likely to overestimate the ‘‘true’’ strength gains. Dynamometry based measurements of isometric and dynamic torque are required to accurately quantify any training-induced changes following ex- ercise programmes in older adults. Furthermore, it is important to understand the origin of any possible strength gains with resistance training and identify the adaptations occurring in the different motor system components of older adults. In order to address the above issues we have conducted a series of studies Fig. 1. Knee extensor torque–velocity relationship pre- and post- investigating the musculoskeletal adaptations to resis- training. Values are means and SD. * and ** denote significantly tance training in older adults. (Po0:05 and Po0:01, respectively) increased torque after 14 weeks of Nine older adults completed a 14-week resistance resistance training. Modified from the data presented in Reeves et al. exercise training programme and nine older adults (2005). served as non-exercising controls (aged 65–81 years). The training programme was performed using resistance exercise machines (Technogym, Gambettola Italy). Ex- group, there were no changes in concentric or eccentric ercises were performed for the major muscle groups of torque, but there was a significant decrease in isometric the upper and lower body in order to provide a whole- torque post-intervention. The strength gains brought body conditioning stimulus. The major muscle groups of about by resistance training may be partly attributed to interest from an experimental perspective in the present increased agonist (knee extensor muscles) neural drive. study were the knee extensors. This muscle group Measurements of electromyographic (EMG) activity was studied because of its crucial role in all locomotor taken from the vastus lateralis muscle showed increases activities. The main exercises performed to target the ranging from 28% to 38% compared to pre-training knee extensors were the leg-press and leg-extension. A values. During voluntary contractions, muscle force and 5-repetition maximum (5RM) was established for each torque is produced not only by the agonist muscles but exercise (the maximum load that could be raised and also by the antagonist muscles, which are co-activated. lowered under control, 5 times only). The training load During knee extension contractions, antagonist muscle corresponded to 80% of the 5RM and the repetition co-activation (knee flexors) has been shown to be higher maximum was tested every 2 weeks in order to maintain in the elderly compared to young adults (Macaluso the same relative training load. Two series of 10 et al., 2002). This may be regarded as a strategy to repetitions were performed for each exercise and maintain a higher degree of knee joint stability in the sessions were performed three times each week for 14 elderly. However, co-activation also functions to apply weeks. Pre- and post-intervention maximal isometric, an opposing torque to the intended direction of effort. concentric and eccentric knee extension torque was Higher levels of antagonist muscle co-activation there- assessed using an isokinetic dynamometer. This device fore contribute to strength deficits in old age. Some allows torque measurements to be taken in all modes of studies suggest that resistance exercise training in older contraction whilst allowing the external angular velocity adults can reduce the level of antagonist muscle co- to be manipulated. These measurements enable con- activation (Hakkinen et al., 1998; Hakkinen et al., struction of the torque–velocity relationship (Fig. 1). 2001), an independent factor that would serve to After training, older adults significantly increased increase strength. In our study however, the level of maximal isometric torque by 9% and maximal con- antagonist muscle co-activation was unaltered by centric torque by 22–37% across the angular velocities resistance training, indicating that only changes in tested (Reeves et al., 2005). In contrast to isometric and agonist muscle activation contributed to the observed concentric torque, resistance training did not signifi- strength gains. An interesting finding is that older adults cantly alter eccentric torque (Fig. 1). In the control did not increase eccentric torque after resistance
  3. 3. ARTICLE IN PRESS 194 N.D. Reeves et al. / Manual Therapy 11 (2006) 192–196 training. Explanations for this finding may include the number has increased both in-series (increased fascicle preservation of eccentric force with ageing and under- length) and in-parallel (pennation angle increase) and loading of the eccentric contraction phase during have implications for maximal force production and the training. It has been shown from both animal and operating range length range of the muscle. Pennation is human studies that eccentric force is relatively well a strategy to allow more contractile material to be preserved with ageing in relation to isometric and packed along the length of the muscle, so theoretically a concentric force (Vandervoort et al., 1990; Phillips et greater number of sarcomeres in-parallel suggests that al., 1991; Hortobagyi et al., 1995). This relative force the muscle would be able to generate a greater preservation may reduce the adaptability of this muscle maximum force. Although an increased number of contraction type in response to exercise training. As sarcomeres in-series suggests that the muscle may be illustrated by the force-velocity relationship (Fig. 1), able to produce force over a greater length range as higher forces can be generated during eccentric contrac- compared to the situation before training with fewer tions as compared to during isometric and concentric sarcomeres in-series, in vivo this is limited by joint contractions (Cook and McDonagh, 1995). During constraints. Resistance training programmes for older exercise training using the constant external load devices adults can therefore not only increase gross muscle area employed in our study, the repetition maximum is but also cause alterations to the internal muscle limited by the concentric contraction and therefore the structure. In addition to changes in gross muscle area, eccentric contraction phase of the same movement will changes in muscle architecture are another muscular- be under-loaded and may partly explain the lack of based factor contributing to the strength gains observed adaptation in this contraction type with training. after resistance training. A number of studies have shown that skeletal muscle Whilst most attention may intuitively be focused on can still adapt to an exercise training stimulus even in the muscular adaptations to resistance training pro- old age (e.g. Fiatarone et al., 1990; Hakkinen et al., grammes, potential adaptations occurring in other 1998; Harridge et al., 1999). Using imaging techniques musculoskeletal structures should be considered. For such as magnetic resonance imaging (MRI) and example, tendons are the force-transmitting structures computed tomography (CT) enlargement of muscle connecting muscle to bone, thus allowing the effective anatomical cross-sectional area (ACSA) by 5–17% has transformation of contractile force in the muscle to joint been reported in the elderly after resistance training movement. Tendons are not inextensible bodies, but programmes lasting 3 months (Brown et al., 1990; elongate when they are subjected to the tensile load Ferri et al., 2003). Indeed data from our laboratory generated by muscle contraction (for review see Butler et agrees with these reports as we have found increased al., 1978). The tendon’s dimensions and mechanical ACSA of the vastus lateralis muscle by 3–10% along the properties influence the degree of deformation that will length of the muscle following 14 weeks of resistance take place in response to the application of a given training (Reeves et al., 2004b). These findings suggest a tensile load. Information on the modification of tendon certain degree of reversal to the muscle atrophy mechanical properties with changes in activity level is experienced with ageing. Although the enlargement of scanty as compared to the information available on muscle size with resistance training is a major factor skeletal muscle. Some inferences however, can be drawn contributing to the observed strength gains, it is not the from in vitro experiments on isolated tissues. In vitro sole factor. As discussed above, neural factors con- studies suggest that ageing reduces tendon stiffness, tribute substantially to increases in strength and other causing a greater tendon elongation for any given force muscular and tendinous factors are also involved. In applied compared to younger tendons (Tkaczuk, 1968; most human muscles, fascicles do not lie parallel to the Noyes and Grood 1976). Indeed the findings from length of the muscle but insert into the tendinous sheath experiments performed on humans in our laboratory known as the aponeurosis at an angle. The internal agree with in vitro reports (Maganaris, 2001). Animal arrangement of muscle fascicles is referred to as muscle models (Woo et al., 1980, 1981, 1982; Buchanan and architecture. We have previously observed that Marsh, 2001) have shown that when tendons undergo muscle architecture is altered in old age. Gastrocnemius exercise loading above that normally experienced under muscle fascicles were found to be shorter by 10% in the habitual conditions, they respond by increasing their elderly compared to young adults and the angle at which stiffness (i.e. they become more resistant to elongation, the fascicles inserted into the aponeurosis, known as the shown by a steeper slope of the force-elongation curve). pennation angle, was smaller by 13% in the elderly By using ultrasound imaging to scan tendon elongation (Narici et al., 2003). We have recently shown in the in vivo during an isometric contraction, we investigated vastus lateralis muscle that following 14 weeks of the influence of resistance training on the mechanical resistance training muscle fascicle lengths increase by properties (stiffness and Young’s modulus—stiffness 9% and pennation angles increase by 30% (Reeves normalized to the tendon’s dimensions) of the patellar et al., 2004a). These findings suggest that sarcomere tendon in older adults. After 14 weeks of resistance
  4. 4. ARTICLE IN PRESS N.D. Reeves et al. / Manual Therapy 11 (2006) 192–196 195 training we found that both tendon stiffness and the factors characterizing ageing can be at least partially normalized stiffness, Young’s modulus increased by mitigated by resistance training. 65% and 69%, respectively (Reeves et al., 2003). The increase in the tendon Young’s modulus suggests that The support received from Technogym and funding the stiffness increase occurred to due a change in the provided by the Italian Space Agency is acknowledged. material properties of the tendon. These findings indicate a certain degree of reversal of the ageing effects on human tendons. The modification of tendon References mechanical properties following resistance training in old age have a number of important functional Brown AB, McCartney N, Sale DG. Positive adaptations to weight- implications. Firstly, depending upon their degree of lifting training in the elderly. Journal of Applied Physiology elongation they can influence the speed of force 1990;69(5):1725–33. transmission. The increase in tendon stiffness found Buchanan CI, Marsh RL. Effects of long-term exercise on the biomechanical properties of the Achilles tendon of guinea fowl. after training would be expected to increase the velocity Journal of Applied Physiology 2001;90(1):164–71. of force transmission and indeed this was shown as a Butler DL, Grood ES, Noyes FR, Zernicke RF. Biomechanics of faster rate of torque development at the level of the ligaments and tendons. Exercise and Sport Sciences Reviews 1978; whole joint system. This may suggest that movements 6:125–81. Cook CS, McDonagh MJ. Force responses to controlled stretches of requiring a rapid generation of joint torque would electrically stimulated human muscle-tendon complex. Experimen- benefit, such as the motor response to a loss of balance. tal Physiology 1995;80(3):477–90. Tendon stiffness and any changes with resistance Ferri A, Scaglioni G, Pousson M, Capodaglio P, Van Hoecke J, Narici training can affect the extent of muscle fibre shortening. MV. Strength and power changes of the human plantar flexors and The increase in tendon stiffness observed after resistance knee extensors in response to resistance training in old age. Acta training would be expected to reduce the extent to which Physiologica Scandinavica 2003;177(1):69–78. Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA, fibres in the knee extensor muscles could shorten. This Evans WJ. High-intensity strength training in nonagenarians. was in fact the case as we observed that the vastus Effects on skeletal muscle. JAMA 1990;263(22):3029–34. lateralis muscle fascicles shortened less after training, Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ, however, it was estimated that the operating range of Roubenoff R. Aging of skeletal muscle: a 12-yr longitudinal study. Journal of Applied Physiology 2000;88(4):1321–6. this muscle remained unchanged (Reeves et al., 2004a). Hakkinen K, Kallinen M, Izquierdo M, Jokelainen K, Lassila H, This finding was attributed to the fact that the changes Malkia E, et al. Changes in agonist-antagonist EMG, muscle CSA, occurring in both the muscle and tendon had opposite and force during strength training in middle-aged and older people. effects on fascicle shortening, interacting in order to Journal of Applied Physiology 1998;84(4):1341–9. maintain the muscle’s operating range constant pre- to Hakkinen K, Kraemer WJ, Newton RU, Alen M. Changes in post-intervention. After the resistance training pro- electromyographic activity, muscle fibre and force production characteristics during heavy resistance/power strength training in gramme the patellar tendons of older adults demon- middle-aged and older men and women. Acta Physiologica strated a reduced strain (tendon elongation during Scandinavica 2001;171(1):51–62. contraction expressed relative to the resting tendon Harridge SD, Kryger A, Stensgaard A. Knee extensor strength, length) for any given level of tendon stress (tendon force activation, and size in very elderly people following strength divided by tendon CSA). Given that tendon strain injury training. Muscle and Nerve 1999;22(7):831–9. Hortobagyi T, Zheng D, Weidner M, Lambert NJ, Westbrook S, or rupture is likely to occur at a given level of tendon Houmard JA. The influence of aging on muscle strength and strain when the integrity of the molecular bonds are muscle fiber characteristics with special reference to eccentric disrupted, this finding would suggest that the likelihood strength. Journals of Gerontology Series A—Biological Sciences of tendon strain injury in older adults might be reduced and Medical Sciences 1995;50(6):B399–406. Klein CS, Rice CL, Marsh GD. Normalized force, activation, and after a period of resistance training. coactivation in the arm muscles of young and old men. Journal of In summary, substantial strength gains can be Applied Physiology 2001;91(3):1341–9. achieved by older adults following resistance training Lynch NA, Metter EJ, Lindle RS, Fozard JL, Tobin JD, Roy TA, programmes. Strength gains can be attributed to neural, et al. Muscle quality. I. Age-associated differences between arm muscular and tendinous factors. Agonist muscle neural and leg muscle groups. Journal of Applied Physiology 1999;86(1): drive increases, whilst the co-activation of antagonist 188–94. Macaluso A, De Vito G. Muscle strength, power and adaptations to muscles remains unchanged after training. The muscular resistance training in older people. European Journal of Applied adaptations to resistance training include enlargement Physiology 2004;91(4):450–72. of gross muscle area and increases in fascicle lengths and Macaluso A, Nimmo MA, Foster JE, Cockburn M, McMillan NC, De pennation angles. The adaptations to training are not Vito G. Contractile muscle volume and agonist-antagonist limited to the muscular system as tendon stiffness coactivation account for differences in torque between young and older women. Muscle and Nerve 2002;25(6):858–63. increases after resistance training. In conclusion, the Maganaris CN. In vivo tendon mechanical properties in young adults musculoskeletal system retains its capacity for adapta- and healthy elderly. Active Life Span Research Symposium. The tion into old age and many of the musculoskeletal Plasticity of the Motor System: Adaptations to Increased Use,
  5. 5. ARTICLE IN PRESS 196 N.D. Reeves et al. / Manual Therapy 11 (2006) 192–196 Disuse and Ageing, Manchester Metropolitan University, UK; Reeves ND, Maganaris CN, Narici MV. Plasticity of dynamic muscle 2001. performance with strength training in elderly humans. Muscle and Morse CI, Thom JM, Davis MG, Fox KR, Birch KM, Narici MV. Nerve 2005;31(3):355–64. Reduced plantarflexor specific torque in the elderly is associated Roos MR, Rice CL, Connelly DM, Vandervoort AA. Quadriceps with a lower activation capacity. European Journal of Applied muscle strength, contractile properties, and motor unit firing rates Physiology 2004;92(1-2):219–26. in young and old men. Muscle and Nerve 1999;22(8):1094–103. Narici MV, Maganaris CN, Reeves ND, Capodaglio P. Effect of aging Skelton DA, Greig CA, Davies JM, Young A. Strength, power and on human muscle architecture. Journal of Applied Physiology related functional ability of healthy people aged 65–89 years. Age 2003;95(6):2229–34. and Ageing 1994;23(5):371–7. Noyes FR, Grood ES. The strength of the anterior cruciate ligament in Tkaczuk H. Tensile properties of human lumbar longitudinal humans and Rhesus monkeys. Journal of Bone and Joint Surgery ligaments. Acta Orthopaedica Scandinavica 1968;S115:1. of America 1976;58(8):1074–82. Vandervoort AA, Kramer JF, Wharram ER. Eccentric knee strength Phillips SK, Bruce SA, Woledge RC. In mice, the muscle weakness due of elderly females. ournal of Gerontology 1990;45(4):B125–8. to age is absent during stretching. Journal of Physiology (London) Winegard KJ, Hicks AL, Sale DG, Vandervoort AA. A 12-year 1991;437:63–70. follow-up study of ankle muscle function in older adults. Journals Rantanen T, Avela J. Leg extension power and walking speed in of Gerontology Series A—Biological Sciences and Medical very old people living independently. Journals of Gerontology Sciences 1996;51(3):B202–7. Series A—Biological Sciences and Medical Sciences 1997;52(4): Woo SL, Ritter MA, Amiel D, Sanders TM, Gomez MA, Kuei SC, M225–31. et al. The biomechanical and biochemical properties of swine Reeves ND, Maganaris CN, Narici MV. Effect of strength training on tendons—long term effects of exercise on the digital extensors. human patella tendon mechanical properties of older individuals. Connective Tissue Research 1980;7(3):177–83. Journal of Physiology (London) 2003;548(Part 3):971–81. Woo SL, Gomez MA, Amiel D, Ritter MA, Gelberman RH, Akeson Reeves ND, Narici MV, Maganaris CN. In vivo human muscle WH. The effects of exercise on the biomechanical and biochemical structure and function: adaptations to resistance training in old properties of swine digital flexor tendons. Journal of Biomechanical age. Experimental Physiology 2004a;89(6):675–89. Engineering 1981;103(1):51–6. Reeves ND, Narici MV, Maganaris CN. Effect of resistance training Woo SL, Gomez MA, Woo YK, Akeson WH. Mechanical properties on skeletal muscle-specific force in elderly humans. Journal of of tendons and ligaments. II. The relationships of immobilization Applied Physiology 2004b;96(3):885–92. and exercise on tissue remodeling. Biorheology 1982;19(3):397–408.