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. Author manuscript; available in PMC: 2012 Apr 13.
Published in final edited form as: Exp Gerontol. 2010 Mar 18;45(6):400–409. doi: 10.1016/j.exger.2010.03.008

Preservation of eccentric strength in older adults: Evidence, mechanisms and implications for training and rehabilitation

Marc Roig 1,2, Donna L MacIntyre 1,2,3, Janice J Eng 1,3, Marco V Narici 4, Constantinos N Maganaris 4, W Darlene Reid 1,3
PMCID: PMC3326066  CAMSID: CAMS2184  PMID: 20303404

Abstract

Overall reductions in muscle strength typically accompany the aging process. However, older adults show a relatively preserved capacity of producing eccentric strength. The preservation of eccentric strength in older adults is a well-established phenomenon, occurring indiscriminately across different muscle groups, independent of age-related architectural changes in muscle structure and velocity of movement.

The mechanisms for the preservation of eccentric strength appear to be mechanical and cellular in origin and include both passive and active elements regulating muscle stiffness. The age-related accumulation of non-contractile material in the muscle-tendon unit increases passive stiffness, which might offer mechanical advantage during eccentric contractions. In addition, the preserved muscle tension and increased instantaneous stiffness of old muscle fibers during stretch increase active stiffness, which might enhance eccentric strength.

The fact that the preservation of eccentric strength is present in people with chronic conditions when compared to age-matched healthy controls indicates that the aging process per se does not exclusively mediate the preservation of eccentric strength. Physical inactivity, which is common in elderly and people with chronic conditions, is a potential factor regulating the preservation of eccentric strength.

When compared to concentric strength, the magnitude of the preservation of eccentric strength in older adults ranges from 2% to 48% with a mean value from all studies of 21.6%. This functional reserve of eccentric strength might be clinically relevant, especially to initiate resistance training and rehabilitation programs in individuals with low levels of strength.

1. Introduction

Skeletal muscles produce tension through three types of muscle contractions. During isometric contractions, the muscle is actively held at a fixed fiber length. In contrast, dynamic muscle contractions can be divided into concentric contractions, involving the shortening of the muscle, and eccentric contractions, consisting of the active lengthening of the muscle by external forces. While it is well accepted that there is a progressive decline in muscle strength with aging, recent studies report a relative preservation of the capacity to produce eccentric torque (Horstmann et al., 1999; Hortobagyi et al., 1995; Klass et al., 2005; Porter et al., 1997; Porter et al., 1995; Poulin et al., 1992; Pousson et al., 2001; Vandervoort et al., 1990) and strength (Phillips et al., 1998), in older adults. In other words, when the age-related reduction of contractile capacity is considered in terms of different types of muscle contractions, the degree to which concentric and isometric strength is reduced is more pronounced than eccentric strength (fig. 1). Interestingly, this eccentric preservation is also reported in patients with chronic conditions when compared to age-matched healthy controls (Clark et al., 2006; Damiano et al., 2001; Eng et al., 2009; Griffin et al., 1994; Knutsson et al., 1997; Mathur et al., 2007; Ponichtera et al., 1992).

Fig. 1.

Fig. 1

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Common patterns of strength decline over the lifespan for concentric, isometric and eccentric strength. The percentage of decline is estimated after normalizing to isometric strength at 20 years of age. Note the smaller proportionate decline of eccentric strength with aging (Adapted from Vandervoort et al., 2009 with permission).

An understanding of why older adults exhibit this relative maintenance of eccentric strength could be relevant to practical applications such as training and rehabilitation of the elderly. For example, some authors suggest that the high efficiency of eccentric contractions (i.e. intense muscle work is achieved at a lower metabolic expense) (LaStayo et al., 2000) renders them a powerful tool for restoring muscle strength in people with a limited capacity to train at high intensities such as older adults (Hortobagyi and De Vita, 2000; LaStayo et al., 2003a) and patients with chronic conditions (Dibble et al., 2006; Engardt et al., 1995; Marcus et al., 2008; Rooyackers et al., 2003). Furthermore, although the exact magnitude of this preservation has not yet been quantified, it is reasonable to surmise that this reserve of eccentric strength could be beneficial for the undertaking of resistance-training programs in people with reduced levels of muscle force (Roig et al., 2008a).

Although the preservation of eccentric strength in older adults is well reported in the literature, some conflicting data exist (Lindle et al., 1997). Moreover, the myriad of methods used to estimate the magnitude of strength deficits in these studies indicates that a more exhaustive analysis of the results is required. Further, no consensus has been reached regarding the underlying mechanisms governing this preservation nor is there a clear understanding of the implications of this phenomenon for practical applications such as training and rehabilitation of the elderly. The aim of this paper is to review the evidence for the preservation of eccentric strength in older adults and analyze potential underlying mechanisms governing this phenomenon. Emphasis will be placed on the preservation of eccentric strength in patients with chronic conditions as a paradigm to explore these potential mechanisms. In addition, the magnitude of preservation and its potential implications for training and rehabilitation of the elderly will be discussed.

2. Evidence for the preservation of eccentric strength in older adults

Numerous cross-sectional comparative studies have provided evidence of the relative maintenance of eccentric torque (Horstmann et al., 1999; Hortobagyi et al., 1995; Klass et al., 2005; Porter et al., 1997; Porter et al., 1995; Poulin et al., 1992; Pousson et al., 2001; Vandervoort et al., 1990) and strength (Phillips et al., 1998) in healthy older adults in spite of overall reductions in muscle contractile capacity. For the purposes of this review, muscle torque is defined as the rotatory effect of a force (force x moment arm) assessed with an isokinetic device, while strength is simply the magnitude of force that a muscle can produce (Enoka, 2002). A detailed description of the studies that support the evidence of the preservation of eccentric strength, including participants’ characteristics, muscle groups tested, methods of normalization and magnitude of strength deficits is outlined in table 1. In short, these studies compare muscle torque (Horstmann et al., 1999; Hortobagyi et al., 1995; Klass et al., 2005; Porter et al., 1997; Porter et al., 1995; Poulin et al., 1992; Pousson et al., 2001; Vandervoort et al., 1990) or strength (Phillips et al., 1998) values between groups of young and older individuals to determine whether age-related deficits in strength are consistent across different types of muscle contractions.

Table 1.

Characteristics of studies that investigated the preservation of eccentric strength in older adults.

Study Subjectsa Muscle and testing velocity Normalized to Magnitude of strength deficitsb
Ecc Con/Iso
Klass 2005 Y=10M/10W (24y)
O=10M/9W (77y)		 Ankle flexors (5/10/50/75/100°s−1) Maximal iso torque at 10°of ankle plantarflexion Ecc torque was 11% (M) and 23% (W) greater in O compared to Y Con torque was 19% (M) and 25% (W) lower in O compared to Y
Pousson 2001 Y=6M/6W (21y)
O=4M/6W (69y)		 Elbow flexors (60/120/180/240°s−1 con) (60/120°s−1 ecc) Ecc torque at 60°s−1 Ecc torque was 27–46% lower in O compared to Y Con torque was 54–77% lower in O compared to Y
Horstmann 1999 Y=19M (24y)
A1=15M (34y)
A2=14M (45y)
O=16M (55y)		 Knee extensors/flexors Ankle extensors/flexors (60/180/240/300°s−1 con) (60/120°s−1 ecc) Not normalized Ecc torque was 4–23% lower in O compared to Y Con torque was 0–29% lower in O compared to Y
Phillips 1998 Y=43W (30y)
O=18W (84y)
H=29W (86y)		 Adductor pollicis Ecc strength normalized to iso strength (normalized to CSA) Ecc strength was 14% (H) and 17% (O) greater compared to Y Iso strength was 14% (H) and 30% (O) lower compared to Y
Lindle 1997 Y=35M/50W (28y)
A1=86M/120W (43y)
A2=103M/88W (55y)
O=122M/50W (75y)		 Knee extensors (30/180°s−1) Not normalized Ecc torque was 31% (M) and 22% (W) lower in O compared to Y Con torque was 33% (M) and 35% (W) lower in O compared to Y
Porter 1997 Y=16W (27y)
O=16W (67y)		 Ankle extensors/flexors (30°s−1) Not normalized Ecc torque was 0–3% lower in O compared to Y Con torque was 11–25% lower in O compared to Y
Hortobagyi 1995 Y=20M/12W (29y)
A=23M/12W (49y)
O=17M/6W (69y)		 Knee extensors (60/90/180°s−1) Not normalized Ecc torque was 20% lower in O (M) and 10% greater in O (W) compared to Y Iso and con torque were 35% and 45% lower in O (M) and 25% and 30% in O (W) compared to Y
Porter 1995 Y=28M/27W (25y)
O=25M/26W (72y)		 Knee extensors (90°s−1) Not normalized Ecc torque was 25–38% lower in O compared to Y Con torque was 42–54% lower in O compared to Y
Poulin 1992 Y=12M (25y)
O=12M (67y)		 Knee extensors Elbow extensors (90/180°s−1) Not normalized Ecc torque was 2–22% lower in O compared to Y Con torque was 31–32% lower in O compared to Y
Vandevoort 1990 Y=26W (25y)
O=26W (73y)		 Knee extensors/flexors (45/90°s−1) Not normalized Ecc torque was 25–38% lower in O compared to Y Con torque was 46–54% lower in O compared to Y
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Y=young; A=adult; O=old; y=years; M=men; W=women; H=hip fracture patients; Con=concentric; Ecc=eccentric; Iso=isometric

a

The age of participants is rounded up.

b

The magnitude of strength deficits was calculated from the mean value using the following equation: (strength of old group/strength young group) × 100

The results of these investigations confirm that, compared to both concentric and isometric strength, differences in eccentric strength between young and older people tend to be smaller. In other words, eccentric strength capacity is preserved in older adults. The relative maintenance of eccentric strength with aging is consistently reported across different muscle groups (table 1), independent of muscle structural characteristics. For example, Hortobagyi et al. (1995) found that eccentric torque of knee extensors was relatively maintained in a group of older adults, although the correlations of either concentric or eccentric torque with muscle mass and fiber type and size were similar. Furthermore, while the majority of studies (Hortobagyi et al., 1995; Poulin et al., 1992) report a greater degree of preservation with higher contraction velocities, consistent with the low influence of velocity of contraction on force production during eccentric contractions (Katz, 1939), the maintenance of eccentric torque is reported across a wide range of velocities (from 30°s−1 to 300°s−1). Thus, it appears that the preservation of eccentric torque in older adults is a well-established phenomenon, occurring indiscriminately across different muscles groups, independent of age-related architectural changes in muscle structure and the velocity of the movement.

3. Evidence contradictory to the preservation of eccentric strength in older adults

There exists only one study reporting no significant preservation of eccentric torque in older adults (Lindle et al., 1997). This study is notable due to its large sample size (n=654) and broad participant age range (20–93 years) (table 1). Despite the fact that no preservation of eccentric torque was found in the oldest group, this study confirms that eccentric strength shows a tendency to be less affected by age (R2~0.19) compared to concentric strength (R2~0.30). The study also yields important information that could help explain these apparently conflicting results. For example, consistent with other reports (Hortobagyi et al., 1995; Klass et al., 2005; Porter et al., 1995), the study reveals that older women tend to show a greater maintenance of eccentric torque compared to men and that this is associated with a gender specific delay in the loss of eccentric torque in women (Lindle et al., 1997). While in men both concentric and eccentric torque losses begin in the 40’s, in women eccentric torque losses appear to start one decade later (50’s). In Lindle et al.’s (1997) study, participants in the oldest and youngest groups had a disproportionate ratio of men to women; 122 men and only 50 women in the oldest group (~75 years), and 35 men and 50 women in the youngest group (~28 years). In fact, pooled together, the two youngest groups had 121 men and 170 women, while the two oldest groups had 225 men and 138 women. Since older women tend to show a more pronounced preservation of eccentric strength than do men, perhaps the larger number of men in the older groups biased the results towards an apparent lack of eccentric torque maintenance in these groups.

4. Evidence for the preservation of eccentric strength in patients with chronic conditions

Numerous studies report the preservation of eccentric torque in people with chronic conditions when compared to age-matched healthy controls (Clark et al., 2006; Damiano et al., 2001; Eng et al., 2009; Griffin et al., 1994; Knutsson et al., 1997; Mathur et al., 2007; Ponichtera et al., 1992). A summary of these studies is shown in table 2. For instance, Mathur et al. (2007) investigated differences in knee flexor and extensor muscle torque between 20 patients with moderate to severe chronic obstructive pulmonary disease (COPD) and 20 healthy controls matched for age, gender and body mass. Although patients with COPD showed marked deficits in torque, patients had greater values of eccentric torque corrected for muscle volume in knee flexors (15.2%; p<0.05) and extensors (17.2%; p<0.05) in comparison to the healthy group. Mathur et al. (2007) hypothesized that this preservation of eccentric strength could be due to an increase in passive muscle stiffness secondary to the accumulation of connective tissue within the muscles of COPD patients (Gosker et al., 2003). However, while intramuscular fat infiltration, as assessed using magnetic resonance imaging, was significantly greater in patients with COPD (~35%; p<0.002), neither the accumulation of connective tissue nor its implication for the preservation of eccentric torque was directly tested.

Table 2.

Characteristics of studies that have investigated preservation of eccentric strength in people with chronic conditions.

Study (Condition) Subjectsa Muscle and testing velocity Normalization method Magnitude of strength deficitsb
Ecc Con
Eng 2009 (Stroke) P=12M/6W (65y)
C=12M/6W (63y)		 Hip extensors/flexors
Knee extensors/flexors
Ankle extensors/flexors (30°s−1)		 Body mass Ecc torque on the paretic leg was 23–52% lower in P compared to C

Ecc torque on the non-paretic leg was 6–21% lower in P compared to C		 Con torque on the paretic side was 40–70% lower in P compared to C

Con torque on the non-paretic leg was 3–35% lower in P compared to C
Mathur 2007 (COPD) P=9M/11W (68y)
C=9M/11W (64y)		 Knee extensors/flexors (30°s−1) Muscle volume Ecc torque was 15–17% greater in P compared to C Con torque was 5–11% greater in P compared to C
Clark 2006 (Stroke) P=11M/6W (57y)
C=6M/7W (63y)		 Knee extensors (30–240°s−1 con) (30–180°s−1 ecc) Maximal iso torque at 55°of knee flexion Ecc torque was 1–16% greater in P compared to C Con torque was 13–24% lower in P compared to C
Damiano 2001 (Cerebral palsy) P=17M/7W (11y)
C=11M/9W (10y)		 Knee extensors/flexors
Ankle extensors/flexors (30/60/120°s−1 con) (30°s−1 ecc)		 Body weight Ecc torque was 42–55% lower in P compared to C Con torque was 43–71% lower in P compared to C
Knutsson 1997 (Spastic paraparesis) P=11M/11W (45y)
C=11M/11W(51y)		 Knee extensors/flexors (30/60/120/180°s−1) Maximal con torque at 30°s−1 Ecc torque was 50–170% greater in P compared to C Con torque was 10–110% greater in C compared to P
Griffin 1994 (Spastic paraparesis) Pp=8M/3W (52y)
Pn=8M/3W (42y)
C= 16M/6W (47y)		 Knee extensors/flexors (30/120°s−1) Not normalized Ecc torque was 34–50% lower in Pp compared to C. Ecc torque was 23–52% lower in Pn compared to C Con torque was 50–77% lower in Pp compared to C. Con torque was 30–55% lower in Pn compared to C
Ponichtera 1992 (Multiple sclerosis) P=6M/3W (41y)
C=6M/3W (37y)		 Knee extensors/flexors (30/60/90°s−1 con) (45/60/75°s−1 ecc) Not normalized Ecc torque was 11–13% lower in P compared to C Con torque was 18–35% lower in P compared to C
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COPD=chronic obstructive pulmonary disease; P=patients; Pp= paretic patients; Pn=non-paretic patients; C=controls; y=years; M=men; W=women; Con=concentric; Ecc=eccentric

a

The age of participants is rounded up.

b

The magnitude of strength deficits was calculated from the mean value using the following equation: (strength of old group/strength young group) × 100

The preserved capacity to produce eccentric torque has also been reported in patients with neurological conditions such as spastic cerebral palsy (Damiano et al., 2001), multiple sclerosis (Ponichtera et al., 1992) and stroke (Clark et al., 2006; Griffin et al., 1994). In addition, two studies have confirmed this preservation in patients with amyotrophic lateral sclerosis, primary lateral sclerosis (Griffin et al., 1994), intramedullary cyst, spastic paresis, myelitis, cerebral palsy, chronic myelopathy, fracture of the thoracic spine and hereditary spastic paraparesis (Knutsson et al., 1997) (table 2). With the exception of the study by Griffin et al. (1994), which included neurological patients with and without signs of spasticity, a uniting theme among all of these studies is that some degree of spasticity was present in all the muscles tested.

The maintained capacity to produce eccentric torque in neurological patients is commonly attributed to the influence of spasticity in voluntary force production (Knutsson et al., 1997). For example, Griffin et al. (1994) found that the preservation of eccentric torque was present only in patients with spasticity, while patients with non-spastic (lower) motor neuron disorders did not show such preservation. However, it is unclear whether the group with spasticity had a greater impairment, which would lead to a preferential reduction of concentric torque and an apparent relative preservation of eccentric torque. Knutsson et al. (1997) suggested that spasticity could increase the stretch reflex of agonist muscles during eccentric contractions, which would add mechanical advantage to the voluntary contraction. In addition, Knutsson et al. (1997) hypothesized that agonist force output could be selectively reduced during concentric contractions via reciprocal inhibition secondary to the strong action of spastic antagonist muscles. Some studies, however, demonstrate that eccentric preservation in patients with stroke (Clark et al., 2006) and spastic cerebral palsy (Damiano et al., 2001) occurs without significant spastic antagonist muscle activity. Moreover, a recent study reports that eccentric torque is not only preserved in the paretic (16%) but also in the non-paretic (14%) lower limb muscles of individuals with stroke compared to controls (Eng et al., 2009), suggesting that spasticity has a negligible effect on the maintenance of eccentric strength and that other neurological mechanisms are also unlikely.

While an exhaustive analysis of these studies is beyond the scope of this paper, these investigations offer an excellent opportunity to explore potential mechanisms for the preservation of eccentric strength in older adults. Firstly, in all of these studies, groups were matched for age, suggesting that age alone does not exclusively mediate the preservation of eccentric strength. This is emphasized, for example, by a study involving children with cerebral palsy in which eccentric torque is preserved in the cerebral palsy group (table 2) (Damiano et al., 2001). Secondly, the preservation of eccentric strength has been observed across a broad range of different clinical populations, suggesting that mediation of this preservation is not restricted to disease specific mechanisms either. The preservation of eccentric torque in both paretic and non-paretic legs of stroke patients (Eng et al., 2009) affirms this hypothesis. It is possible that the lack of physical activity commonly observed in older adults and patients with chronic conditions could contribute to the greater deficits of concentric strength and the preservation of eccentric strength in these individuals. The fact that physical inactivity appears to preferentially affect concentric torque, reinforces this hypothesis (Eng et al., 2009). Evidence in support of potential underlying mechanisms for the preservation of eccentric strength is discussed in the following sections.

5. Potential mechanisms for the preservation of eccentric strength in older adults

5.1 Neurological mechanisms

Decreased agonist activation during concentric contractions

It is possible that the preservation of eccentric strength in older adults is related to specific deficits in the capacity to fully activate muscles under concentric or isometric conditions (fig. 2). Since, compared to concentric and isometric contractions, muscle activation at similar levels of force is significantly lower during eccentric contractions (Bigland and Lippold, 1954), it can be speculated that age-related deficits in muscle activation will have a greater negative impact in concentric and isometric contractions than in eccentric. In view of this, Klass et al. (2005) used both the central activation ratio (CAR) and the ratio between the rectified electromyography (EMG) signal and the evoked action potential (EMG/M-wave) to assess muscle activation of the ankle dorsiflexors during isometric, concentric and eccentric contractions in a group of young (~24 years) and older (~77 years) adults (table 1). In spite of the preservation of eccentric torque in the older group, differences in muscle activation across different types of muscle contractions between groups were not significant, suggesting that differences in agonist neural drive are not responsible for the preservation of eccentric torque observed in the older group (fig. 2).

Fig. 2.

Fig. 2

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Potential neurological mechanisms for the preservation of eccentric strength in older adults

Increased antagonist activation during concentric contractions

The preservation of eccentric strength may also be explained by the disproportionate activation of antagonist muscles with aging reported in some (Macaluso et al., 2002; Hakkinen et al., 1998) but not all (Babault et al., 2001; Ochala et al., 2004; Valour et al., 2003) studies. While it remains to be determined what mechanisms account for this increased coactivation (Hortobagyi and DeVita, 2006), a greater activation of antagonist muscles, specifically during concentric contractions, could contribute to the greater deficits in concentric strength observed in older adults (fig. 2). In line with this, some studies with young adults indicate that antagonist activation of hamstrings and quadriceps is 17% to 91% lower when acting eccentrically compared to concentrically (Kellis and Baltzopoulos, 1999). The reasons for this difference in antagonist coactivation between both eccentric and concentric contractions are unclear and may include differences in the neural pattern between both muscle contractions (Enoka, 1996). However, since the total joint moment can be estimated by way of the difference between agonist and antagonist coactivation, it is likely that a decreased antagonist coactivation during eccentric actions would contribute to the greater agonist force capacity reported during this type of muscle activity. Furthermore, since antagonist coactivation increases with aging, it is possible that the force deficits in concentric and isometric strength would be more accentuated in older adults.

The involvement of an exaggerated antagonist coactivation in the preservation of eccentric strength is unclear, however. For example, a recent study reported no differences in ankle dorsiflexors muscle antagonist coactivation between a group of young (~24 years) and older (~77 years) participants, even though muscle torque normalized to maximal isometric torque at 10° of ankle plantar flexion confirmed that eccentric torque was preserved in the older group (Klass et al., 2005) (table 1). Similarly, Pousson et al. (2001) did not observe differences between a group of young (~21 years) and older (~69 years) participants in elbow flexors antagonist activity, even though muscle torque normalized to concentric torque at 60°s−1 also confirmed that eccentric torque was preserved in the older group (table 1). While the methodological differences of these studies (i.e. disparate muscle groups and EMG protocols) preclude any conclusion regarding the role of neurological mechanisms in the preservation of eccentric strength from being drawn, the evidence is suggestive of the involvement of non-neurological mechanisms (fig. 2).

5.2 Mechanical mechanisms

Increased connective tissue and muscle passive stiffness

A potential mechanical mechanism for the preservation of eccentric strength in older adults is the increase in muscle passive stiffness observed with aging (Ochala et al., 2004; Porter et al., 1997; Valour and Pousson, 2003; Vandervoort et al., 1992) (fig. 3). Muscle passive stiffness is regulated by the action of both parallel (e.g. extracellular connective tissue) and series (e.g. tendon as well as cytoskeletal and contractile proteins) elastic components (Gajdosik, 2001). Studies on animal models suggest that part of the increased muscle passive stiffness observed with aging originates primarily from the accumulation of connective tissue (Alnaqeeb et al., 1984). Several studies confirm that connective tissue and non-contractile material is increased with aging (Kent-Braun et al., 2000). Since skeletal muscle acts as a spring that absorbs elastic strain energy during eccentric contractions (Dickinson et al., 2000), an increased passive stiffness could theoretically enhance the capacity to generate passive mechanical work during this muscle contraction (Lindstedt et al., 2001) (fig. 3).

Fig. 3.

Fig. 3

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Potential mechanical mechanisms for the preservation of eccentric strength in older adults

However, the functional significance of the accumulation of connective tissue in the preservation of eccentric strength is unclear. First, it is uncertain if the age-related connective tissue has the same mechanical properties as the extracellular matrix commonly found in normal muscles. Second, no human studies demonstrate a correlation between increased connective tissue and passive stiffness. More importantly, the preservation of tension during stretch reported in old skinned muscle fibers (Ochala et al. 2006), indicates that the preservation of eccentric strength is present independently of extracellular connective tissue accumulation. Third, the functional relevance of passive stiffness in the preservation of eccentric strength is unclear (fig. 3). For example, Porter et al., (1997) investigated the preservation of eccentric torque of ankle plantar flexors and extensors, as well as the passive resistive torque of ankle plantar flexors in older (~67 years) and younger (~27 years) women, respectively (table 1). Although the older group showed greater passive torque (26.4%; p<0.01), both groups displayed similar torque angle patterns. In addition, the preservation of eccentric torque was observed during ankle plantar flexion, where passive resistance is minimal. Although the role of passive stiffness should not be underestimated, these results suggest that passive stiffness does not entirely account for the preservation of eccentric strength (fig. 3) and that other cellular mechanisms might be involved.

5.3 Cellular mechanisms

Preserved tension in old muscle fibers during stretch

It is possible that the preservation of eccentric strength in older adults is related to age-related adaptations in the contractile behavior of the muscle cell (Hortobagyi et al., 1995) (fig. 4). For instance, Phillips et al. measured specific force, defined as isometric tension (T0) normalized to muscle cross sectional area (CSA), in isolated soleus muscles of young and old mice during eccentric and concentric muscle contractions. The results of this study confirm that age-related deficits in specific force during stretching of the muscle are minimal (Phillips et al., 1991). In other words, muscle weakness due to age is manifested only in concentric contractions, while tension during stretching is preserved in old muscles. Noteworthy, this experiment was specifically designed to eliminate the possible effects of muscle resting tension, which confirms that the preservation of specific force in old muscle fibers during stretch is not exclusively due to increases in passive stiffness from increased extracellular connective tissue.

Fig. 4.

Fig. 4

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Potential cellular mechanisms for the preservation of eccentric strength in older adults

The preservation of tension during stretch in old single muscle fibers has also been confirmed in human subjects. Ochala et al. (2006) conducted an elegant study in which the contractile behavior of a total of 235 single skinned muscle fibers of 6 old (~66 years) and 6 young (~32 years) men were compared after a quick stretch was applied during T0. The use of skinned muscle fibers is relevant because the potential confounding effects of passive stiffness from extracellular connective tissue are eliminated. As expected, the results confirmed that specific force (T0/CSA) was lower in both type I (25%; p=0.005) and type IIa (33.5%; p=0.001) single muscle fibers in the older group. In contrast, when the incremental tensions after the quick stretch were normalized to T0, the resultant tension was greater and lasted longer in the old single muscle fibers. Hence, old human muscle fibers appear to have a preserved capacity to produce tension after a quick stretch, which could explain the maintained capacity to produce eccentric strength in older adults.

A plausible mechanism for the preservation of the tension during stretch in older muscle fibers could be related to an increment of the force produced by each cross-bridge during eccentric contractions. It has been suggested that the stretch produced during eccentric contractions might shift myosin heads into a strongly bound state (Lombardi and Piazzesi, 1990). This, in turn, would reduce during eccentric contractions the age-related force deficits commonly observed during either isometric or concentric contractions (Phillips et al., 1991). It is still unclear though, why this stretch-induced phenomenon does not bring about additional tension in young muscle fibers (Fig. 4). A potential explanation could be that the reduced speed of the cross-bridge cycle (e.g. slower detachment rate of active cross bridges) in older muscle fibers (Larsson et al., 1997) might also be involved in the preservation of eccentric strength (Klass et al., 2005; Ochala et al., 2006). The fact that the study by Ochala et al. (2006) reported that the increment of tension after the stretch lasted longer in older fibers partly supports this hypothesis.

Increased instantaneous stiffness in old muscle fibers

A potential explanation for the preservation of eccentric strength might also include age-related changes in the elastic properties of the muscle cell independent of reductions in the speed of the cross-bridge cycling rate. Ochala et al. (2007) used an experimental setting similar to the one used to study fiber behavior after quick stretch, to investigate differences in the elastic properties of old and young skinned single human fibers. In this case, however, age-related differences in muscle fiber unloaded shortening velocity (V0) and instantaneous stiffness (K) were investigated with the slack test. The slack test involves the quick release of the fiber length during T0. Shortening velocity (V0) was calculated as the ratio of the time required to overcome the applied slack and the change in fiber length. Instantaneous stiffness (K) normalized by specific force (T0/CSA) was calculated as the ratio between the force change during the quick release and the corresponding sarcomere length change. The results of this study show that shortening velocity (V0) and specific force (T0/CSA) are lower in fibers in older men. In contrast, normalized instantaneous stiffness [(K/(T0/CSA)] was greater in type I (31%; p<0.001) and type IIa (20%; p<0.05) fibers in older men. Interestingly, this increased stiffness was unrelated to shortening velocity (V0), which suggests that the greater active stiffness in older fibers is independent of alterations in the velocity of the cross-bridge cycle. Although the greater active stiffness of older muscle fibers could contribute to the preservation of eccentric strength, the exact mechanisms are currently unknown (fig. 4).

6. Magnitude of preservation of eccentric strength

The analysis of the magnitude of preservation of eccentric strength, calculated as the difference between the magnitude of eccentric and concentric strength deficits (table 1), showed inconsistent results. For example, Hortobagyi et al. (1995) estimated that the decline of concentric knee extensors muscle torque per decade was approximately threefold (~30N) compared to eccentric torque (~9N). However, our results show that, compared to concentric strength, the magnitude of eccentric preservation in older adults ranges from 2% to 48% with a mean value from all studies of 21.6% (table 1). This wide range may be related to differential normalization methods and testing velocities as well as to the age and gender of the participants. In general, women tended to show greater levels of preservation (table 1). Due to the numerous factors influencing the magnitude of preservation and the disparity of normalization methods used, the effects of the latter in the magnitude of preservation of eccentric strength are unclear.

7. Implications for training and rehabilitation of the elderly

Since older adults often approach their maximal capabilities when performing activities of daily living (Hortobagyi et al., 2003), any degree of preservation of muscle strength in these individuals could have implications for functional mobility (Ploutz-Snyder et al., 2002; Manini et al., 2007). However, it is unclear whether the relative preservation of eccentric strength offers any advantages to improve muscle function in the elderly. The disparity of results in the magnitude of eccentric preservation (table 1) prevents any conclusions regarding the potential advantages of this phenomenon for training and rehabilitation from being drawn. However, it is possible that the reserve of eccentric strength, albeit variable, could be used, in combination with the greater magnitude of force that can be developed during eccentric contractions (Dudley et al., 1991), to increase the intensity of resistance training protocols thus maximizing gains in muscle function for older adults (Hortobagyi and De Vita, 2000, Lastayo et al., 2000). The preservation of eccentric strength could be particularly important to initiate resistance-training routines in older adults with low levels of strength (Hortobagyi, 2003).

In addition to the potential advantages that the preservation of eccentric strength may have for the initiation of resistance training in older adults it is important to emphasize that resistance training itself with eccentric contractions has shown to be more effective than concentric training in increasing muscle strength and mass (Roig et al., 2008b). This effectiveness appears to be related to both the higher loads and the powerful myogenic stimulus of stretch during eccentric contractions (Golspink et al., 1995). Evidence from studies during the last decade suggest that high-intensity resistance training incorporating eccentric contractions can offer some advantages over more traditional training strategies to increase muscle strength and mass in older adults (Hortobagyi and De Vita., 2000; LaStayo et al., 2003a; Onambele et al., 2008; Reeves et al., 2009). The high metabolic efficiency (LaStayo et al., 2000) and faster adaptations observed with eccentric training (Hortobagyi et al., 1996) make it especially appealing in clinical situations after periods of immobilization or in the most debilitated old individuals (Hortobagyi and De Vita, 2000).

It should be also noted that eccentric muscle contractions are inherent to common daily activities (Dickinson et al., 2000). Muscles contract eccentrically to decelerate movement and store elastic recoil energy in preparation for concentric (or accelerating) contractions (Lastayo et al., 2003b). Although not always obvious, this type of muscle contraction is an integral part of most movements during daily activities. For example, it has been suggested that maximum knee and ankle eccentric strength might be critical in safe stair descent in older individuals (Startzell et al., 2000). Since most falls (~75%) on stairs occur during stair descent (Tinetti et al., 1988) the improvement of eccentric muscle strength could be beneficial to reduce fall risk in older people (Lastayo et al., 2003a). In addition, eccentric contractions appear to be of key importance for the absorption of kinetic forces during the descent phase of a fall impact, which could, theoretically, reduce the risk of hip fracture (Sandler et al., 2001). Thus, maintenance of eccentric strength is likely paramount to maintained mobility and independence.

The current evidence shows that adaptations from eccentric training are highly specific to the velocity and type of muscle contraction (Roig et al., 2008b). Although some studies suggest otherwise (Lastayo et al., 2003: Onambele et al., 2008), it is currently unclear whether this high specificity compromises the transferability of strength gains to more functional movements (Barry and Carson, 2004). Hence, although our results suggest that the preservation of eccentric strength could be used to initiate eccentric training interventions in older adults with low levels of strength, resistance training interventions should incorporate different types of muscle contractions to increase transferability to more complex functional tasks. Moreover, muscle damage from eccentric contractions appears to be exacerbated in older compared with young animals (Brooks and Faulkner, 1996), suggesting that older people may be at risk of exercise induced muscle damage from eccentric exercise if the regiments are not delivered appropriately. Since neither muscle damage nor inflammation are prerequisites for stimulating positive muscle adaptations in older adults (LaStayo et al., 2007), careful and safe progression of the intensity of eccentric training is strongly advised.

8. Conclusions and future directions

Strong evidence demonstrates that eccentric strength is preserved in older adults. The mechanisms for this preservation appear to reside in the muscle itself and might include both passive and active elements regulating muscle stiffness. Since people with chronic conditions show the preservation of eccentric strength when compared to controls matched for age, it appears that age alone does not exclusively mediate the preservation of eccentric strength. We hypothesize that the lack of physical activity commonly observed in older adults and patients with chronic conditions could contribute to the greater deficits of concentric strength and the preservation of eccentric strength. Potential mechanisms induced by a reduction of physical activity include the accumulation of connective tissue, increases in passive stiffness as well as increases in active stiffness due to alterations in muscle fiber phenotype (e.g. shift towards slow myosin heavy chain isoforms) and contractile behavior (e.g. reduced contractile velocity). However, these physiological mechanisms are complex and require further investigations.

Although this review has analyzed the evidence behind the different mechanisms underlying the preservation of eccentric strength in older adults, moving forward the study of these mechanisms requires further experimental investigations in the future. For example, the use of animal models could be of interest to explore of the role that connective tissue may play in the preservation of eccentric strength. To delineate whether the preservation of eccentric strength is produced by the lack of physical activity or the aging process itself, it would be interesting to study older individuals with different training backgrounds to investigate whether highly trained subjects maintain this enhanced capacity to produce eccentric strength. If this were the case, it would indicate that aging, not physical activity, is the main factor regulating the preservation of eccentric strength.

Acknowledgments

During this study, Marc Roig received support through a Strategic Training Fellowship in Rehabilitation Research from the CIHR Musculoskeletal and Arthritis Institute, a Fellowship in Respiratory Rehabilitation from the BC Lung Association, and a Graduate Fellowship from the University of British Columbia, Janice J Eng received a career scientist award from CIHR (MSH-63617).

The authors especially thank Professor Anthony Vandervoort (University of Western Ontario) for providing permission to use one of his figures. We also thank Jennifer Rurak for editing a preliminary version of this manuscript.

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