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1 Department of Health and Exercise Science, Gustavus Adolphus College, St. Peter, MN, USA 2 College of Health, University of Utah, Salt Lake City, UT, USA
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(Received 7 January 2005;
accepted after revision 28 February 2005; first published online 8 March 2005)
Corresponding author J. P. Mattson: 212C Lund Center, 800 West College Avenue, Gustavus Adolphus College, St. Peter, MN 56082, USA. Email: jmattson{at}gac.edu
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Introduction |
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Indeed, previous investigations have demonstrated elevated exercising inorganic phosphate/phosphocreatine (Pi/PCr) ratios (Tada et al. 1992; Wuyam et al. 1992), reductions in maximal force (Bernard et al. 1998; Engelen et al. 1994; Zattara-Hartmann et al. 1995; Clark et al. 2000; Gosselink et al. 2000) and impaired endurance (Zattara-Hartmann et al. 1995; Gosselink et al. 1996; Serres et al. 1998a; Haccoun et al. 2002) in non-ventilatory skeletal muscle of COPD patients. Unfortunately, it has not been possible to fully determine whether these alterations result from the disease per se or dyspnoea, muscle deconditioning, pharmacological intervention and/or malnutrition. However, several investigations (Dillard et al. 1989; Killian et al. 1992; Gosselink et al. 1996; Somfay et al. 2002) have demonstrated that aspects other than a decrease in lung function may contribute to exercise intolerance in these patients. Serres et al. (1998) reported that reductions in endurance time to fatigue of the quadriceps muscle in COPD patients were associated with physical inactivity. Bernard et al. (1998) and Clark et al. (2000) concluded that reductions in isokinetic and isotonic peripheral muscle function in COPD patients were due, at least in part, to chronic inactivity and muscle deconditioning. Furthermore, myopathy is an established side effect of corticosteroid treatment (Dekhuijzen & Decramer, 1992). Thus, it is not surprising that Decramer et al. (1996) demonstrated reductions in quadriceps muscle force in COPD patients with steroid-induced myopathy compared to COPD controls. Moreover, reductions in handgrip-strength were determined to be related to nutritional depletion in patients with COPD (Engelen et al. 1994). Therefore, characteristics other than lung dysfunction appear to underlie problems in locomotory skeletal muscle of patients with COPD.
What is uncertain is whether EMP per se induces deficits in locomotory skeletal muscle contractile function. Knowledge of this could provide the basis for targeting specific therapeutic interventions aimed at reversing these alterations. Therefore, the purpose of this investigation was to determine whether EMP: (1) induces a reduction in force production; (2) induces increased fatigability; and (3) impairs the speed of recovery in locomotory skeletal muscle. We hypothesized that EMP would diminish muscle contractile function in an accepted animal model (Mattson & Poole, 1998) where the entire muscle of similar human skeletal muscle fibre composition and locomotory movement could be studied. Specifically, functional measures of the force–velocity relationship, fatigability and recovery were measured in situ in the gastrocnemius muscle to determine whether locomotory skeletal muscle contractile function was altered in this disease state.
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Methods |
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Emphysema model
Male Syrian Golden hamsters (9 weeks old; weight, 100–120 g) were housed in 7.5 inch x 8.5 inch cages, maintained on a 12 h light–12 h dark cycle, and supplied rodent chow and water ad libitum. Following a 1-week habituation period, animals were randomly divided into control (CON) (n = 5) and EMP groups (n = 10). Under deep ketamine/xylazine anaesthesia (150/7.5 mg kg–1 I.M.), either saline (0.3 ml (100 g body wt)–1; 0% mortality) or porcine elastase (25 IU (100 g body wt)–1; Sigma Chemical, St Louis, MO, USA) in 0.3 ml of normal saline (30% mortality) was instilled intratracheally as previously described (Mattson & Poole, 1998).
Determination of contractile properties
Hamsters were weighed and anaesthetized (ketamine/xylazine, 150/7.5 mg kg–1
I.M.) 8 months after instillation. In situ mechanical properties of gastrocnemius muscle were determined as described by Caiozzo et al. (1991, 1994, 1996). Briefly, an incision was made through the skin in the posterior aspect of the lower right leg. The gastrocnemius muscle was exposed, dissected free from surrounding tissue, and its distal tendon insertion was cut. The leg was secured with the muscle in a near-horizontal plane and a mineral oil bath (
30°C) was formed around the muscle by using the skin and Parafilm. The distal tendon was attached to a dual-control servo motor (305B-LR Aurora Scientific Inc., Aurora, ON, Canada) for measurement and control of force and displacement (sampled at 2 kHz). Muscles were excited with a computer-activated stimulator (F300-HP2 Aurora Scientific Inc.) via bipolar stainless steel electrodes placed on the distal stump of the transected sciatic nerve. All contractions were elicited at supramaximal voltages (i.e. 2.5 times the threshold for maximal activation), and muscles were allowed to rest for 1 min between subsequent contractions. Optimal muscle length (Lo) was determined by measuring force during a series of tetanic contractions (250 ms pulse train at 100 Hz). The muscle was initially held at a relatively slack length and then increased by 0.64 mm for each subsequent contraction. All subsequent isometric contractions were performed at Lo. Force–velocity measurements were determined from 9 to 10 afterloaded contractions ranging from 10 to 100% of isometric tension. Force–velocity data were fitted to a Hill-type curve (Hill, 1938) with velocity expressed in muscle length s–1 and force expressed relative to isometric force. Muscle fatigue was evaluated with a Burke (Burke et al. 1973) protocol (40 Hz pulse trains for 330 ms every second for 240 s) (initial force: EMP, 630 ± 44 g; CON, 642 ± 24 g). Recovery was evaluated (muscles had recovered from the Burke fatigue protocol after 15 min) (initial force: EMP, 574 ± 62 g; CON, 623 ± 27 g) by using repeated maximal tetanic contractions following a 40-s maximal isometric contraction. It was necessary to fully fatigue, reduce maximal tetanic force to 0 g (not complete with Burke protocol), the muscles with this sustained maximal contraction to adequately examine recovery. After mechanical measurements, Lo was measured in situ and the muscle was dissected and weighed. In addition, a saline displacement technique was used to measure excised lung volume (FRC) at 0 cmH2O airway pressure (Scherle, 1970).
Statistical analysis
Maximal force, individual fatigue and recovery time points, and half-times of recovery were compared using a t test. Force–velocity characteristics, fatigue and recovery measurements were compared using a repeated measures two-way ANOVA: treatment by time (post hoc:Tukey's least significant difference). Values are presented as means ±
S.D. and significance was accepted at P
0.05.
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Results |
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Neither final body mass nor gastrocnemius mass were different between EMP and CON animals (Table 1). The presence of lung pathology and air trapping was supported by the large increase (80%; P < 0.01) in lung volume weight in EMP group versus CON group (Table 1).
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Peak tetanic force was similar between groups (Table 2). These similarities where preserved when peak force was normalized for body mass and muscle mass (Table 2). There were no differences in force–velocity characteristics (Fig. 1) (Hill-coefficients: EMP, a = 0.043 ± 0.03, b = 1.67 ± 0.12; CON, a = 0.045 ± 0.08, b = 1.48 ± 0.25)].
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EMP gastrocnemius muscle force was reduced (P = 0.05) compared to CON at all time points following the initial contraction during the Burke fatigue protocol (Fig. 2). Force decreased by 24% in CON animals and 55% in EMP (P = 0.05) during this protocol. Differences in fatigue were demonstrated by a repeated measures two-way ANOVA (P = 0.03).
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EMP gastrocnemius muscle force was reduced (P = 0.05) compared to CON at 6, 12 and 156 s following a 40 s maximal isometric contraction (Fig. 3). It is interesting to note that only gastrocnemius muscle in two EMP animals had fully recovered at the end of this protocol, which demonstrates the severity of impairment displayed by these animals. Half-times to recovery were greater in EMP (92 ± 92 s) than in CON (7 ± 7 s) gastrocnemius muscle (P = 0.05). Slower recovery characteristics were demonstrated by a repeated measures two-way ANOVA (P = 0.05).
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Discussion |
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Locomotory skeletal muscle contractile function
The increased fatigability and slowed recovery of locomotory skeletal muscle found with this investigation extend those found in COPD patients (Serres et al. 1998; Clark et al. 2000; Haccoun et al. 2002). Using a dynamic extension test, Serres et al. (1998) reported a 33% reduction in time to fatigue of the quadriceps in COPD patients receiving treatment with inhaled bronchodilators and corticoids. Furthermore, they found skeletal muscle endurance to be correlated with the level of daily physical activity. Gosselink et al. (1996) demonstrated that isometric quadriceps and hand-grip force was significantly related to a 6-min walking distance test in COPD patients. These latter results support the notion that locomotory skeletal muscle weakness, caused by loss of endurance or strength or both, contributes to the exercise limitation in these patients. However, neither physical activity level nor pharmacological treatment was reported. Clark et al. 2000) reported that those COPD patients free from long-term oral steroid therapy, demonstrated a significant reduction in lower but not upper body sustained performance compared with healthy sedentary subjects. Furthermore, these patients were able to ameliorate this deficit with a 6-week weight-training programme leading the authors to conclude that the original reduction in lower body sustained performance was due to muscle deconditioning. Haccoun et al. (2002) concluded that leg muscle dysfunction, assessed by a 30-s isokinetic cycle test, contributes to the exercise limitation in COPD patients. However, data on dose and duration of steroid use was not reported.
Previous investigations (Engelen et al. 1994; Zattara-Hartmann et al. 1995; Bernard et al. 1998; Clark et al. 2000; Gosselink et al. 2000) have demonstrated reductions of maximal force in non-ventilatory skeletal muscle of COPD patients. However, neither we (current investigation) nor Serres et al. (1998) were able to substantiate these findings. The apparent divergence in response between our investigation and those of others may be important for understanding the mechanisms underlying impaired force production in EMP. Controlling physical activity by housing hamsters individually in a cage (previously demonstrated in this model; Mattson & Poole, 1998), use of pharmacological agents (absent in this model), and nutritional status (no differences in body or muscle mass), allows us to support the conclusion that previously reported reductions in maximal force generation of locomotory skeletal muscle in COPD patients may have been the result of one or more of these confounding factors rather than the disease per se. Furthermore, this conclusion is supported by the work of Bernard et al. (1998) who demonstrated that reductions in maximal force of quadriceps in COPD patients could be explained by an atrophy of muscle mass. Moreover, it has been demonstrated that COPD patients with steroid-induced myopathy can only produce a quadriceps peak torque of 28% compared with normal COPD patients (Decramer et al. 1996) and that nutritionally depleted patients exhibited a 40% reduction in hand-grip strength compared to non-nutritionally depleted patients (Engelen et al. 1994).
Further demonstration of contractile impairment may be indicated by an absence of staircase potentiation during the first few contractions of the Burke fatigue protocol in EMP animals (Fig. 2). Such an absence has previously been demonstrated in atrophied muscle (St-Pierre & Gardiner, 1985) accompanied by a lack of phosphorylation of the regulatory light chains of myosin (Tubman et al. 1996). Although potentiation effects were not the focus of our current investigation, this is an intriguing finding and deserves further examination.
Potential mechanisms for reductions in the endurance of peripheral skeletal muscle
As presented in the introduction, reductions in skeletal muscle oxidative enzyme activities are expected to reduce skeletal muscle fatigue resistance and impair exercise tolerance. We (Mattson & Poole, 1998) and others (Gosker et al. 2002; Jakobsson et al. 1995; Maltais et al. 1996) have demonstrated alterations in oxidative enzyme activities of non-ventilatory skeletal muscle in animals with emphysema and/or COPD patients. Thus, it is likely that reductions in locomotory skeletal muscle fatigue resistance may be the result of a fall in oxidative capacity. Alternatively, skeletal muscle dysfunction may result from fibre-type conversion and/or atrophy. COPD patients present with alterations in non-ventilatory skeletal muscle composition and structure, including altered fibre composition (Jobin et al. 1998; Whittom et al. 1998; Gosker et al. 2002) and myosin heavy chain expression (Satta et al. 1997; Maltais et al. 1999), and atrophy of type I and II fibres (Hughes et al. 1983; Sato et al. 1997; Whittom et al. 1998). Furthermore, we (Mattson et al. 2004) demonstrated fibre atrophy of fast-twitch types IIA, IIX, and/or IIB in a variety of locomotory skeletal muscles of hamsters with EMP. Specifically, there is IIX fibre atrophy and a shift in fibre composition (decrease in type IIA and appearance of type IIB) in gastrocnemius muscles of EMP animals. The reduction in highly oxidative type IIA fibres (Mattson et al. 2002a) may contribute to the impaired endurance function, while the appearance of type IIB fibres may account for the preservation of maximal force production and absence of overall muscle atrophy found herein. Therefore, fibre transformation and atrophy may underlie problems of locomotory skeletal muscle function in patients with COPD. Moreover, type IIB fibres are only recruited during high-intensity exercise (Armstrong & Laughlin, 1985; Delp & Duan, 1996). Thus, if EMP-associated locomotory muscle changes are the sole result of physical inactivity related to caged-housing, then fibre atrophy would not have been expected to occur in type IIB fibres. Therefore, physical inactivity does not fully account for EMP-induced locomotory skeletal muscle alterations.
Reactive oxygen species (ROS) may be contributing to the skeletal muscle dysfunction. We (Mattson et al. 2002b) and others (Barnes, 1990; Allaire et al. 2002) have demonstrated that EMP animals and COPD patients, respectively, have increased markers of oxidative stress. ROS have been implicated in oxidative enzyme dysfunction (Corretti et al. 1991; Andersson et al. 1998), H2O2 has been demonstrated to reduce Ca2+ release from the sarcoplasmic reticulum (Brotto & Nosek, 1996) and its sensitivity in skeletal muscle, and nitric oxide may reduce myosin ATPase activity (Allaire et al. 2002). Therefore, ROS may impair locomotory skeletal muscle contractile function by disturbing cellular homeostasis or directly interfering with cellular energetics. Alternatively, impaired locomotory skeletal muscle contractile function may result from reduced oxygen delivery. Indeed, this animal model can result in average arterial PO2 (PaO2) values of 59 Torr at rest and 69 Torr during exercise (Sexton & Poole, 1998). Jakobsson et al. (1990) reported significant correlations between metabolite concentrations and PaO2 of the quadriceps muscles, and Mannix et al. (1995) demonstrated that ATP flux is dependent on the severity of hypoxaemia in the gastrocnemius/soleus group in COPD patients. If hypoxaemia contributes to impaired locomotory skeletal muscle contractile function in COPD patients, then oxygen therapy should ameliorate this effect by restoring normal oxygen delivery to the working muscle(s). However, Somfay et al. (2002) suggested that modest improvements in the exercise performance of non-hypoxaemic COPD patients supplemented with oxygen was the result of ventilatory alterations from chemoreceptor inhibition and not the result of improved oxygen delivery to the working muscle. Moreover, Maltais et al. (1998) concluded that COPD patients suffer from an intrinsic skeletal muscle abnormality given that peripheral O2 delivery did not account for early lactate release during lower-limb exercise in their patient population.
In conclusion, the results of this investigation provide evidence that EMP induces increased fatigability and slowed recovery of locomotory skeletal muscle. Moreover, the responses reported here have significant implications related to the functional contractile characteristics of locomotory skeletal muscle in COPD patients. Even though an array of factors may provoke locomotory skeletal muscle dysfunction in EMP hamsters, physical inactivity, drug therapy and/or nutritional status do not appear to be compulsory stimuli for this response. Therefore, future investigations should focus on determining whether cachectic factors directly stemming from the disease per se underlie the changes found herein.
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