Assessment of Muscle Contractile Properties at Acute Moderate Altitude Through Tensiomyography

Introduction

The skeletal muscle responses taking place at acute and chronic exposures to hypoxia have been extensively documented in terms of biochemical and physiological adaptive processes (Hoppeler and Vogt 2001; Bartsch and Saltin, 2008; Hoppeler et al., 2014). As regards the neuromuscular system, there is evidence suggesting that hypoxia plays a role in fatigue development and neuromuscular activation (Goodall et al., 2010; 2014). Nevertheless, the effects of hypoxia on the neuromuscular system are not fully understood.

Increased sympathetic nervous activity has been reported at high altitude (Seals et al., 1991; Ashenden et al., 1999; Katayama et al., 2011), although no changes in maximal isometric force generating capacity are generally described (Bowie and Cumming 1971; Orizio et al., 1994; Felici et al., 2001; Esposito et al., 2003; Casale et al., 2004). On the other hand, it has been described that normobaric hypoxia reduces peak power output and oxygen uptake during maximal whole body exercises to fatigue (Duhamel et al., 2004).

Furthermore, there seems to be agreement that hypoxia accelerates fatigue development during voluntary and electrically evoked resistive protocols (Felici et al., 2001; Degens et al., 2006; Katayama et al., 2007), although that is not always the case (Young et al., 1980; Szubski et al., 2007; Perrey and Rupp, 2009). Based on animal models (Ottenheijm et al., 2006; Degens et al., 2010), the mechanisms behind changes in muscular performance have been linked to alterations in muscle contractile properties. Human studies are limited and do not seem to support that hypothesis (Degens et al., 2006).

Inconsistent evidence comes from previous research looking at myoelectric activity (EMG) when examining contractile properties under hypoxic environments (Casale et al., 2004; Degens et al., 2006). For example, no changes in EMG signal were reported after maximum voluntary contractions (Garner et al., 1991), cycling efforts (Kayser et al., 1994; Taylor and Bronks, 1996) or electrically elicited contractions (Casale et al., 2004) when normoxic and hypoxic conditions were compared. On the contrary, other studies have reported changes in EMG variables associated to reduced oxygen availability during voluntary (Moritani et al., 1992; Felici et al., 2001; Goodall et al., 2012; Torres-Peralta et al., 2014) and/or electrically evoked contractions (Garner et al., 1991; Dousset et al., 2001a) and after 5-week low-load hypoxic resistance training (Manimmanakorn et al., 2013). The fact that all these investigations have been conducted at different altitude levels and hypoxic environments (real altitude vs. normobaric hypoxia) may account for these discrepancies.

Tensiomyography (TMG) represents an objective, noninvasive technique capable of measuring changes in muscle contractile properties (Valencic and Knez, 1997). TMG has been proposed as an effective tool at estimating muscle fiber composition and distribution (Dahmane et al., 2000; 2005; Simunic et al., 2011) and at evaluating neuromuscular fatigue (Garcia-Manso et al., 2012), muscle damage (Hunter et al., 2012), and structural muscle adaptations (Dahmane et al., 2006; Loturco et al., 2015). Basic TMG parameters such as muscle displacement (Dm), highly correlated to muscle tone and contractile force (Pisot et al., 2008), and time of contraction (Tc), representative of muscle histochemical properties (Simunic et al., 2011), may be altered under acute hypobaric hypoxia.

Gasparini et al., (2012) reported TMG parameters alterations in individuals with peripheral arterial disease who suffered from intermittent lower-limb claudication. The authors suggested that physiological and structural modifications in muscle function, as result of chronic limited oxygen availability, could be detected by TMG. Nonetheless, to the best of our knowledge, TMG technique has not previously been employed to evaluate the acute effects of hypobaric hypoxia on the muscle contractile properties of healthy trained athletes.

Accordingly, the objective of this study was to investigate the TMG muscle response to increasing percutaneous electrical stimulation intensities during an acute exposure to moderate altitude. It was thus hypothesized that TMG could detect the acute effects of moderate altitude on the muscle contractile characteristics.

Materials and Methods

Procedures

The TMG device detects radial muscle belly displacement through a displacement-measuring sensor (GK40, Panoptik, Ljubljana, Slovenia) whose characteristics have been previously described (Valencic and Knez, 1997; Dahmane et al., 2005). A single twitch electrical stimuli (1 ms duration) elicited muscle contraction through two self-adhesive electrodes (Compex Medical SA, Ecublens, Switzerland) placed symmetrically to the sensor 4 cm apart from midpoint (Dahmane et al., 2005). The measuring point for each muscle was anatomically established as the point of maximal muscle belly displacement detected by palpation during voluntary contraction (Dahmane et al., 2000; Garcia-Manso et al., 2012).

During VL measurements, participants were positioned supinely on a padded bench with a foam pad placed under the knee (knee angle set at 30° knee flexion). Measurements on BF were performed in a prone position on a padded bench with a foam pad placed above the ankle (knee angle set at 5° knee flexion). To avoid potential reproducibility issues (Tous-Fajardo et al., 2010), electrode and sensor positions were outlined on the skin surface with a permanent marker so that the same procedure was accurately reproduced on the following day. The inductive sensor was carefully placed perpendicular (90°) to the muscle belly displacement by using a bubble level and manual goniometer (Fig. 1).

OPEN IN VIEWER

FIG. 1.

Tensiomyography (TMG) set up with displacement sensor and electrodes placed above biceps femoris to deliver electrical stimulation. A bubble level and manual goniometer were employed to ensure perpendicular position of the inductive sensor.

On day one, sea level TMG measurements were recorded at different electrical stimulations (40, 60, 80, and 100 mA). Previous studies using TMG have reported maximal muscle belly response using electrical intensities between 40 and 100 mA (Hunter et al., 2012). There was a 2 min rest period between each measure of the same muscle to avoid potentiation and/or fatigue effects. The muscle responses measured were computer-analyzed to determine the above-described TMG parameters (Dm, Tc, Tr, Td, and Ts).

Force was not measured during testing, as previous research has shown minor force production during TMG assessments (Hunter et al., 2012). Reproducibility of TMG has previously been assessed across consecutive testing days (Simunic 2012). Likewise, long and short-term stability have been previously reported (Ditroilo et al., 2013; Krizaj et al., 2008). TMG reproducibility has also been tested previously at our laboratory (Rodríguez-Matoso et al., 2010).

Results

At altitude, VL showed lower Dm values at 40 mA (4.6 ± 2.01 vs. 5.1 ± 2.1 mm; p = 0.008; ES = −0.237). No significant differences were found at higher electrical stimulations (p ≥ 0.05; ES < 0.019). Biceps femoris showed Dm decrements in all electrical stimulations under hypoxic conditions (p < 0.001, ES > 0.61) (Fig. 2).

OPEN IN VIEWER

FIG. 2.

Mean ± (SE) VL and BF maximal radial displacement values (Dm) at sea level and moderate altitude. **p < 0.0005; *p ≤ 0.01.

In VL, Tc was longer at altitude compared to sea level at 40 (27.93 ± 6.09 vs. 24.72 ± 5.31 ms; z = 2.15, p = 0.031, ES = 0.56) and 100 mA (25.22 ± 3.51 vs. 23.4 ± 3.71ms; p = 0.03, ES = 0.51). No statistical differences were found in Tc of BF between conditions (p > 0.05, ES > −0.19) (Fig. 3).

OPEN IN VIEWER

FIG. 3.

Time of contraction (Tc) behavior under normoxic and hypoxic conditions in vastus lateralis (VL) and biceps femoris (BF) stimulated at different intensities (mA). *p ≤ 0.05.

At altitude, VL showed higher Ts (at 40 and 100 mA) and Tr (at 80 and 100 mA) than under normoxic conditions. No significant differences were observed in BF for Ts and Tr (Table 1).

Vastus lateralis revealed significant increments in Td at all electrical intensities under hypoxic conditions (p ≤ 0.03, ES ≥ 0.33). No significant differences were seen in BF Td (p > 0.05, ES = −0.52 in 40mA, ES ≤ −0.11 in 60, 80 and 100mA) (Table 1).

Discussion

The main outcome of this study is that slight changes in the muscle contractile properties of VM and BF were observed at acute hypobaric hypoxia through TMG. However, those changes do not appear to be consistent across the muscles assessed and electrical intensities employed. To the best of our knowledge, this is the first study to report acute effects of hypobaric hypoxia on muscle contractile properties through TMG technique.

Our results showed lower Dm values in BF at acute moderate altitudes, whereas higher Dm values were observed in VL at 40 mA. TMG appears to be sensitive in the detection of acute muscle damage and fatigue (Garcia-Manso et al., 2011; Hunter et al., 2012). While eccentric exercise-induced muscle damage increases muscle tone (lower Dm values) (Hunter et al., 2012), reductions in muscle stiffness (higher Dm) have been reported after an ultra-endurance event (Garcia-Manso et al., 2011). Given that our participants remained in resting conditions and the exposure to altitude was no longer than ≈5 h, acute changes in muscle tone may have occurred for reasons linked to the effect of altitude exposure on the neuromuscular system (Seals et al., 1991).

The implications of these changes on muscle performance are unknown, as no functional testing was performed. Nevertheless, the evidence supporting changes in muscle function at moderate altitude is limited (Perrey and Rupp, 2009). It should be taken into account that investigations are conducted at different altitude levels and hypoxic conditions (hypobaric vs. normobaric hypoxia), which may account for discrepancies. Our measurements were taken at moderate hypobaric altitude (< 3000 m) and in acute conditions (< 6 h of altitude exposure). At high altitude (> 4000 m), previous research has shown impairments in muscle force generating capacity during endurance force testing (Eiken and Tesch 1984; Degens et al., 2006; Katayama et al., 2007; Katayama et al., 2011). On the contrary, maximal force generating capacity seems to be maintained at high altitude (Garner et al., 1991; Casale et al., 2004; Degens et al., 2006) or even improved at real moderate altitude (Feriche et al., 2014).

Regarding Tr and Ts parameters, opposite responses between muscles were observed under hypoxic conditions. At altitude, lower Tr and Ts values were observed in BF, whereas higher Tr and Ts values were detected in VL (Table 1). These results are consistent with data obtained in animal studies, showing that hypoxia has greater impairment of cellular homeostasis in muscle composed of fibers with low oxidative capacity compared with those of a more oxidative profile (Howlett and Hogan, 2007; Degens et al., 2010). The shorter Ts observed at altitude in BF is also in agreement with previous research showing an improvement of the muscle response when electrically stimulated (Dousset et al., 2001b).

On the other hand, an increment in Ts values has been attributed to muscle fatigue development (Garcia-Manso et al., 2011; 2012), which is in line with previous studies showing faster fatigue development under hypoxia (Perrey and Rupp, 2009). The fact that higher Tc (Fig. 2) and Td (Table 1) values were also observed under hypoxic conditions further supports the idea of muscle fatigue symptoms on VL muscle. Increments in Tc have been attributed to muscle damage (Hunter et al., 2012) and fatigue symptoms after a long distance triathlon competition (Garcia-Manso et al., 2011).

A trend towards shorter Tc values was observed in BF, although it did not reach statistical significance. Previous research has reported shorter Tc values as a result of muscle training adaptations (Dahmane et al., 2006; García-García et al., 2013) and shift in the fiber type composition from type I to type II fibers due to chronic arterial hypoxemia (Gasparini et al., 2012).

These findings may be somewhat limited by several factors that should be taken into account. Hyperventilation during altitude exposure leads to respiratory alkalosis and increased respiratory loss of water (Faiss et al., 2013). Hydration status of participants during altitude exposure was not controlled, which could have affected skin conductivity and therefore electrical impulse propagation during assessments (Tous-Fajardo et al., 2010).

Furthermore, hamstring tightness could have increased during the trip to altitude from sea level (2 hours by bus), altering possibly the TMG response. Assessments were performed between 11.00 and 16.00 h, but comparisons in BF TMG parameters between morning and afternoon testing sessions did not reveal any differences (p > 0.05; data not shown). Nonetheless, sea level assessments were also preceded by a 1.5 h car trip, what may counterbalance this possible confounder factor. Additionally, it is important to bear in mind that arterial oxygen saturation levels were not measured and may differ between participants (Luks and Hopkings, 2014).

These results suggest that the acute exposure to moderate altitude induced little but varying changes on the muscle contractile properties of BF and VL assessed by TMG. In agreement with previous investigations using other neuromuscular assessment techniques (Perrey and Rupp, 2009), a tendency towards muscle fatigue symptoms on VL but the opposite behavior (potentiation) on BF was depicted. More research, along with other neuromuscular assessment techniques, is needed to effectively determine the efficacy of TMG as a valid tool to evaluate altitude-induced changes on muscle function.