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8BIOLOGICAL SCIENCES
NEUROMUSCULAR ELECTRICAL STIMULATION IN CONDITIONS OF GRAVITATIONAL UNLOADING
Koryak Yu.A.
Ph.D., Dr. Sci., Department of Sensory-motor Physiology and Countermeasures, Laboratory of Gravitational Physiology of Sensory-motor system, State Scientific Center of the Russian Federation -Institute of Biomedical Problems of the Russian Academy of Sciences, Moscow
ABSTRACT
Background. The purpose of the present study is to quantitatively describe the relationships between joint angles and muscle architecture of human triceps surae [medial (MG) and lateral (GL) gastrocnemius and soleus (SOL) muscles] after 7 d of «dry» water immersion (DI) with use neuromuscular electrical stimulation (NMES). Methods. Six healthy young men subjects participated in this study. During DI, subjects performed NMES muscle groups of both lower extremities. NMES continued for 6 d, during which daily 5 d on end (from Monday to Friday inclusive) including one day of rest (Saturday). Before and after DI with NMES, a internal architecture (lengths and angles of fascicles, and muscle thickness) of human triceps surae were determined. The triceps surae muscle architecture was measured in vivo by use of B-mode ultrasonography. The ankle was positioned at 15 dorsiflexion (-15 ) and 0, +15, and +30 ° plantar flexion, with the knee set at 90 At each position, longitudinal ultrasonic images of the MG, LG, and SOL were obtained while the subject was relaxed (passive). Result. Before DI in the passive condition, fascicle lengths changed from 36, 47, and 39 mm (ankle, -l5 ) to 27, 3l, and 28 mm (ankle, +30 ); pennation angle changed from 3l, 20, and 23 ° to 49, 29, and 34 ° for MG, LG, and SOL, respectively. After DI with by NMES in the passive condition, fascicle lengths decreased by l6, 37, and 24 %; pennation angle increased by 38, 35, and 34 % for MG, LG, and SOL, respectively. In conclusion, from the present results it was suggested that the architecture of the triceps surae is considerably different, possibly reflecting their functional roles. Changes in pennation angles and fibre length after DI with by NMES, suggesting that muscle architecture does change remarkably by muscle atrophy. Decreases in muscle thicknesses in leg muscles were not prevented by the present exercise protocol, suggesting a need for specific exercise training for these muscles. These findings suggest that rapid muscle architecture remodeling occurs in lower limb in humans, with changes occurring within of unloading of the musculoskeletal system. These adaptations might protect from a larger loss of muscle force.
Keywords: ultrasonography, "dry" water immersion, neuromuscular electrical stimulation, muscle architecture, skeletal muscle, lengths and angles of fascicles
I. Introduction
A number of studies have indicated that sudden exposure to microgravity environment causes a decrease in the tone of the skeletal muscles [Kakurin et al., 1971; Kozlovskaya et al., 1984], reduction of muscle strength [Cherepakhin & Pervushin, 1970; Grigor'yeva & Kozlovskaya, 1985; Koryak, 1998; 2002], perceptual and coordination disorders in the neuromuscular systems [Ross et al., 1984; Grigor'yeva, Kozlovskaya, 1985; Kirenskaya et al., 1985], shift of the spinal reflex mechanisms [Cherepakhin, Pervushin, 1970; Kozlovskaya et al., 1982], and degradation of joint position sense [Bock, 1994]. It is accepted that the major factor responsible for all of these changes is the sudden elimination of the proprioceptive information from the muscle and tendon in response to absence of load-bearing. Gravitational loading appears to be necessary for the maintenance of human lower limb skeletal muscle size and force [Kawakami et al., 2000; Koryak, 2001]. Studies simulating microgravity have shown that exercise countermeasures can attenuate, but not completely prevent the loss of muscle mass and force [Kawakami et al., 2001; Koryak, 2001]. The muscle groups most affected by exposure to microgravity appear to be the an-tigravity extensors of the knee and ankle [Akima et al., 2001]. Among these, the plantarflexors seem to be the
most affected [Akima et al., 2000], likely due to their greater mechanical loading under normal gravitational conditions. Most notable after exposure to microgravity is a disproportionate loss of force as compared to that of muscle size [Akima et al., 2000; Kawakami et al., 2001], indicating that factors other than atrophy contribute to muscle weakness. The internal architecture of a muscle is an important determinant of its functional characteristics (force-velocity relationships, force-length, and maximum isometric force [Gans, Bock, 1965; Lieber, Frieden, 2000].
The purpose of the present study is to quantitatively describe the relationships between joint angles and muscle architecture of human triceps surae [medial (MG) and lateral (GL) gastrocnemius and soleus (SOL) muscles] after 7 d of «dry» water immersion (DI) with use neuromuscular electrical stimulation (NMES).
II. Methods
Participants. Six healthy men aged 20 to 24 years (22.3 ± 0.6) volunteered to participate in the present study. Their average height and mass were 1.78 ± 0.4 m, and 78.3 ± 3.4 kg (means ± SD), respectively.
Six of the subjects had a significant lower limb injury within the previous 5 yr, had inflammatory condi-
tions or hypertension, and had performed weight training. Selection of subjects was based on a screening evaluation that consisted of a detailed medical history, physical examination, complete blood count, urinaly-sis, resting and cycle ergometer electrocardiogram, and a panel of blood chemistry analysis, which included fasting blood glucose, blood urea nitrogen, creatinine, lactic dehydrogenase, bilirubin, uric acid, and cholesterol. All of the subjects were evaluated clinically and considered to be in good physical condition. No subject was taking medication at the time of the study, and all subjects were nonsmokers.
Subjects were fully informed details and possible risks of the protocols and aim of the study before signing a written, informed consent form. All subjects gave written informed consent before the study, which was approved by the Human Research Ethics Committee within the Russian National Committee on Bioethics of the Russian Academy of Sciences and was in compliance with the principles set forth in the Declaration of Helsinki.
«Dry» water immersion. To simulate micrograv-ity the DI model has been used as described by Shul-zhenko and Vil-Villiams (1976). Each subject was positioned horizontally in a special bath on fabric film that t separated him from the water. During DI, the subjects g- remained in a horizontal position (a angle which make the body and horizontal line, e.g. 5 ° head-up position) continuously for all including excretory function and eating (Figure 1). The water temperature was constant (33.4 °C) and maintained automatically at this level throughout the experiment. The duration of the DI was 7 days. A nursing staff was present for subjects' transportation, maintenance of hygiene including toilet and shower, provision of food and medical care, as well as support of subjects' needs within the constraints of the protocol. The subjects were supervised 24 h-d-1.
Functional electrical stimulation "Dry" electrodes (Ltd. "Axelgaard', USA) are placed on the skin above the quadriceps femoris muscles, the hamstrings, the tibialis anterior, the peroneal, and the triceps surae muscles (Figure 1). The synchronous stimulation of antagonistic muscle groups prevents unwanted joint movements. The NMES is performed during 3 hours per day with 1 s « on » and 2 s « off» trains and a frequency of 25 Hz and amplitude of stimulus up to 45 V for training. Used biphasic rectangular by 1 ms pulse width. The electrical stimulus was provided by the "STIMUL LF-1" stimulator (Russia). The NMES of muscles of the examinee was carried out directly in a bath.
Ultrasound scanning
Joint position settings and torque measurement. Each subject's right foot was firmly attached to an iso-^ kinetic dynamometer («Byodex», USA) (Figure 2). The •Jf ankle joint was fixed at 15 ° dorsiflexion (- 15 °) and 0 (neutral anatomic position), + 15 and + 30 ° plantar flexion. The knee joint was positioned at 60 Thus the following measurements were performed in 12 conditions. In each condition, the subject was asked to relax the plantar flexor muscles (passive condition), and pas-
sive plantar flexion torque was recorded from the output of the dynamometer by a computer. We assumed that there was no muscle activity in the passive condition.
Measurement of lengths, and angles of fascicles, and thickness muscle. Fascicular lengths and pennation angles of human the triceps surae were measured in vivo from sonographs taken during rest (passive) (Figure 2). Longitudinal sectional images of human the triceps surae were obtained using a B-mode ultrasound apparatus («SonoSite MicroMaxx», USA) with a linear-array probe (45-mm, 7.5 MHz wave frequency, HFL-38x, SonoSite MicroMaxx, USA).
The probe fixed to the skin using elastic tapes. The probe was coated with, a water-soluble transmission gel to provide acoustic contact without depressing the dermal surface. During scanning, the pressure of the transducer on the skin was minimized to prevent muscle compression. The transducer was aligned in the direction of the muscle fascicles; appropriate orientation was achieved when muscle fascicles could be traced clearly across the ultrasound image. Ultrasound images were stored on computer memory of the apparatus. Longitudinal ultrasonic images of the triceps surae [medial (MG) and lateral (LG) gastrocnemius and soleus (SOL) muscles] were obtained at the proximal levels 30 % (MG and LG) and 50 % (SOL) of the distance between the popliteal crease and the center of the lateral malle-olus. Each level is where the anatomic cross-sectional area of the respective muscle is maximal (Fukunaga et al., 1992). At that level, mediolateral widths of MG and LG were determined over the skin surface, and the position of one-half of the width was used as a measurement site for each muscle. For SOL, the position of the greatest thickness in the lateral half of the muscle was measured at the level mentioned above.
The length of fascicles ( Lf ) across the deep and superficial aponeurosis was measured as a straight line (Figure 1) [Abe, 2000]. The fascicle pennation angle ( ©) was measured from the angles between the echo of the deep aponeurosis of each muscle and interspaces among the fascicles of that muscle (Figure 1) [Fukunaga et al. 1997].
The distance between aponeuroses (muscle thickness) was estimated from the fascicle length and pennation angle using the following equation:
Muscle thickness = Lf x sin a, where
Lf, and a is the pennation angle of each muscle determined by ultrasound.
In the present study, the length and pennation angle of one fascicle were manually measured on each frame using an image processing program («Dr. Real-lyVision» (Ltd. «Alliance - Holding», Russia). The measurements were performed three times for each frame, and the mean values were used for further analyses. The coefficients of variation of the two measurements were less than 3.6 % and 5.5 % for fascicle length and pennation angle, respectively.
Contractile properties and muscle architecture of the triceps surae muscle were tested twice: before and after DI. The test protocol was identical for both pre-and post-DI tests.
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Statistics
Data are presented as the mean values ± standard error of the mean (SE). Differences in pennation angles, fibre lengths and thicknesses between rest and between different ankle angles were tested using two-way analysis of variance tests. Tukey's test was used to determine significant difference between mean values. Oneway analysis of variance was used for comparison of muscle thickness, pennation angles, and fibre lengths. A level of p < 0.05 was selected to indicate statistical significance.
III. Results
After the 7-day DI with application by NMES, in the passive condition, Lf fibres in the MG, and LG, and SOL has decreased for l2 % (from 32 ± 2 to 28 ± l mm), l3 % (from 36 ± 2 to 3l ± 2 mm), and l3 % (from 36 ± 3 to 32 ± 2 mm) but in the active condition by l8 % (from 26 ± 3 to 22 ± 2 mm), 22% (from 36 ± 3 to 28 ± 2 mm), and 2l % (from 32 ± 2 to 26 ± 2 mm), respectively (Figure 3).
The 0 angles, in the passive condition, was decreased by 22, 20 and l6 %; but in the active condition by l7 %, 22 % and l7 %, respectively (Figure 3). Shorter fascicle lengths and steeper fascicle angles in the active compared with the passive condition show internal shortening of fascicles by contraction.
Thicknesses of MG, LG and SOL at rest (~ l8, l6 and l5 mm, respectively) did not change significantly in response to changes in muscle length resulting from changes in ankle joint angle (Figure 4).
The individual data of the maximal torque developed by muscles-extensor foot are shown in Figure 5. Maximal plantar flexion torque increased on the average by l0.5 % (l48.2 ± 6.9 vs l63.8 ± 5.9 N) after DI with application by NMES-training, corresponding by five subjects and one has decreased for 9.6 % (l55 vs l40 N; p > 0.05).
IV. Discussion
This study describes, for the first time, the architecture of the human triceps surae [MG, and LG, and SOL] in vivo. The results obtained in vivo indicate that human MG, LG, and SOL architecture drastically changes both as a function of ankle joint angle at rest. At rest, when changing the ankle joint angle from - l5 to +30 deg, GM pennation angle increased from 3l to 49 deg, LG - from 20 to 28,5 deg, and SOL - from 22.8 to 34 deg; fibre length decreased from 35.5 to 26.8 mm, LG - from 46.8 to 3l.2 mm, and SOL - from 39.2 to 28.2 mm. These results indicate that fibre length and pennation angle of the human triceps surae cannot be assumed to remain constant with changing muscle length [Huijing & Woittiez, l985]. The decrease in fibre length and increase in pennation angle with increasing muscle length may be ascribed the taking up of the slack characterizing these structures [Huijing & Woittiez, l985]. In the present study, the decrease in fibre length occurring from -l5 deg to +30 deg of passive plantar flexion also suggests that muscle fibres became progressively slack with increasing ankle joint angles.
The major findings of this study were that, after 7 day DI with of NMES-training, isometric maximal voluntary torque by the plantar flexor muscles increased
[Koryak et al., 20l0]. Previous studies have documented decrease in MVC more than on 50 % [Gri-gor'eva & Kozlovskaya, 1985; Koryak, 1998a, b; 2002, 2003) and in Po more than on 30 % (Koryak, l998a,b; 200l, 2003].
Efficacy of NMES for increased the contractile properties of skeletal muscles has been suggested in previous studies [Koryak, l995; Mayr et al., 2000; Koryak ^ et al., 2002]. The insignificant increase in force of con- E traction in the present study can be assumed it is defined by slack intensity impulses (Figure 6).
It is well known that the smaller motoneurons innervating muscles are more readily activated than the larger cells innervating units [Henneman et al., l965; Burke & Edgerton, l975], as the strength of the contraction increases progressively. The smaller units consist of slow twitch muscle fibres (type I) and the larger units consist of fast twitch fibres (type II). In submaximal voluntary contractions, type I fibres the motor units are activated by the synaptic current impinging on the motor neuron. The situation is completely different in contractions triggered by NMES, because the muscle fibres of the motor units are activated by an electric current which is applied extracellularly to the nerve endings, and larger cells with lower axonal input resistance are more excitable [Blair & Erlanger, l933; Solomonow, l984]. In fact, when the stimulus is applied from outside the cell, the electric current must first enter through the membrane before it depolarises the cell, but the extracellular medium shunts the current, and the smaller motor units will not be activated during submaximal NMES because of their higher axonal input resistance. Therefore, the smaller motor units do not adapt to training with submaximal NMES. However when use electrical stimulation high training intensity, larger force NMES to be more efficient exercise [Almekinders, l984].
Internal architecture of the GM, LG, and SOL muscle was altered and this was only partially prevented by exercise countermeasures. Both fascicle length and pennation angle were reduced after DI with NMES, this strongly suggests a loss of both in-series and in-parallel sarcomeres, respectively. The functional consequence of the decreased fascicle length was a reduced shortening during contraction. The loss of in-se-ries sarcomeres would mean that this is likely to have implications both on the force-length and force-velocity relationships of the muscle. The observation of a smaller pennation angle during contraction after DI with NMES will partially compensate for the loss of force, because of a more efficient force transmission to the tendon. The reduced initial resting pennation angle probably, grows out reduction decreased tendon stiffness or of the muscle-tendon complex that finds confirmation in substantial growth AL muscle of LG (with 0.9 up to 3.3 mm after DI) during contraction [Koryak et al., 20l0]. This observation is consistent with the findings of Kubo et al. [2000]. In conclusion, NMES-training was partially successful in mitigating the loss of function and architecture induced by prolonged DI. Apparently, by ascending during NMES a flow muscular afferentation [Gazenko et al., l987].
In summary, from the present results, follows, first, that the architecture different lead the triceps su-rae muscle considerably differs, reflecting, probably, their functional roles, second, various changes fibre length and pennation angle between different muscles, probably, are connected to distinctions in ability to develop force and elastic characteristics of sinews or muscle-tendon complex and, at last, in the third, NMES has preventive an effect on stimulated muscles: in part reduces loss of force of reduction of the muscles, the caused long unloading. The received data, allow concluding, that use of NMES renders the expressed preventive action, essentially reduces depth and rate of atrophic processes in muscles.
Acknowledgements
The author are particularly grateful to Mrs. M. Kuz'mina, M.D., Ph.D. (Clinical Hospital N 1 President Medical Center, Moscow, RUSSIA) for the executed ultrasonic researches. Special gratitude the author expresses to Mrs. V. Kovalenko., Head of Moscow Representation «Dalco International» (Moscow, RUSSIA) for providing the ultrasound apparatus «SonoSite MicroMaxx» (USA).
They thank Dr. I. Berezhinski, Ph.D., Head of Moscow Ltd. «Alliance - Holding» for development of the software.
At last, the author express gratitude to all volunteers which participated in this research and without their participation there would be no opportunity to receive an actual material.
Conflict of Interest
The author declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Legends to Figures
Figure 1. Experimental set-up
A. Position of the subject on the dynamometer. Subject performing a muscle function test using isoki-netic dynamometer and ultrasound scanning MG and LG muscles. The ankle and the knee of the tested leg are fixed at 90° (neutral anatomic position) and 60°, respectively. a, dynamometer; b, dynamometer footplate; d, ankle joint and dynamometer footplate axis; c, marker (arrow) was placed between the skin and the ultrasonic probe as the landmark to confirm that the probe did not move during measurements; e, velcro straps for fixating the thigh; f, ultrasonic system. Position of ultrasonic transducer at research of MG (left panel) and LG (right panel) muscle.
B. Ultrasonic images of longitudinal sectional of medial head of the gastrocnemius muscles (MG). Ultrasonic transducer was placed on skin over the muscle at 30 % (MG) distance between the popliteal crease and the center of the lateral malleolus. Fascicle length was determined as length of a line drawn along ultrasonic echo parallel to fascicle. Fascicle angles was determined as angle between echoes obtained from fascicles and deep aponeurosis in ultrasonic image. The superimposed white line at the Ton indicates the path of a fascicle between the superficial and deep aponeuroses. ©f, the angle of pennation; SF, subcutaneous fat; GM, medial head of the gastrocnemius muscle.
Figure 2. Experimental design
All of the enrolled participants were older than 20 years and have never used NMES. Seven days separated the two evaluation sessions. The main objectives of the evaluation sessions were the assessment of some intrinsic muscle and architecture properties during DI as well as the properties during a NMES task. NMES-training of muscles of the examinee was carried out directly in a bath. The intensity level stimulation is determined by a threshold of bearableness of subjects. NMES-training continued for six days, during which daily five days on end (from Monday to Friday inclusive) including one day of rest (Saturday). During DI, subjects executed a NMES-training during 3 hours per day with 1 s « on » and 2 s « off » with a frequency of 25 Hz and amplitude of stimulus from 0 up to 45 V for training.
Figure 3. Changes in the triceps surae complex architecture. Medial (MG), and lateral (LG) gas-trocnemius, and soleus (SOL) muscles fascicle length ( Lf ) and pennation ankle ( © ) as a function of changes joint ankle at rest.
Values presented are means ± SD (n = 5).
Figure 4. Medial (MG), and lateral (LG), and so-leus (SOL) muscles thickness as a function of changes in ankle at rest.
Figure 5
Changes in maximal plantar flexion torque of individual subjects after DI with NMES-training
Figure 6
Dynamics of change of amplitude stimulus pulses during training.
Original population, n = 6 men age = 23+0,2 years
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Evaluation session Day = - 3 Isometric MVC Architecture of a human muscle
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7 weeks 5 sessions/weeks
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Evaluation session Day = R +0 Isometric MVC Architecture of a human muscle
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r o 1 subject • 4 subject
k 2 subject A 5 subject
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3 5 7 9 11 13 15 17 19 21 23 25 27 29 Number of times the amplitude changes during training
Figure 6
References during 20 days of 6° head-down-tilt bed rest prevents
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