TELEMETERING ELECTROMYOGRAPHY OF MUSCLES USED

TELEMETERING ELECTROMYOGRAPHY OF MUSCLES USED IN WALKING UP AND DOWN STAIRS J. JOSEPH and RICHARD WATSON, LONDON, ENGLAND From the Departmeizt of Analomi, Gui s Hospital Medical School, Loizdon The interactions during walking of some of the muscles of the lower limb and back have been investigated by means of electromyography and a pattern of gait has been established ( Report on Fundamental Studies of Human Locomotion Relating to the Design of Artificial Limbs, University ofcalifornia 1947; Battye and Joseph 1966). However, the actions of muscles involved during walking up and down stairs have not been investigated. This paper attempts to ascertain if there is a consistent pattern of muscle activity among individuals and to determine what is the sequence and extent ofactivity ofthe muscle involved. Electromyography is a recognised and well established method of investigating the action of muscles, and by using a telemetering device it is possible to dispense with long trailing wires so that interference with recorded activity by artefacts is reduced to a minimum. METHODS The apparatus used for picking up the muscle potentials comprised a small transistorised amplifier and transmitter carried on the subject s back (Fig. I) and a radio receiver which was connected to two double beam oscilloscopes, one of which was used for monitoring and one for recording on moving photographic paper the potentials from the muscles investigated. Figure 4 shows a typical recording of muscle activity. All the electronic apparatus used was fully described in the paper on walking (Battye and Joseph 1966). Initially, six men aged from eighteen to fifty-two years were investigated. They had no history of any significant locomotor disturbance or injury. Their heights varied from 175 to 186 centimetres and their weights from 60 to 84 kilograms. The muscles investigated were the tibialis anterior, soleus, quadriceps femoris, hamstring group, flexors of the hip, gluteus medius, gluteus maximus and erector spinae. Because of difficulty in determining the pattern of activity of the contraction of the tibialis anterior, this muscle was investigated in six further subjects. All recordings were made from the right side of the body. Surface electrodes were used. The electrode site over each muscle was prepared in a standard manner: the skin was shaved, scraped gently twenty times with fine glass paper to remove the keratinised layer, and cleansed with alcohol. The sites chosen have been described previously (Battye and Joseph 1966). Only one change was made: the hamstrings were investigated as a group with one electrode over the lateral and one over the medial hamstrings, I 5 centimetres above the knee joint. The. three electrodes consisted of shallow silver cups 00l 5 centimetre. J thick and 15 centimetres in diameter. The cups were filled with ----- FIG. I commercial electrode jelly and held in position with adhesive The subject wearing the tape. If care was taken to avoid the spread of jelly between amplifier and transmitter. adjacent electrodes the records were free from artefacts. The electrodes are over the.. hamstring muscles. The stairs were made to the standard dimensions used by 774 THE JOURNAL OF BONE AND JOINT SURGERY

TELEMETERING ELECTROMYOGRAPHY OF MUSCLES USED IN WALKING UP AND DOWN STAIRS 775 builders with a rise of I65 centimetres and a tread of 28 centimetres. The subject wore his ordinary shoes and socks and wore a pair of shorts and a shirt. Before recording, the subject walked up and down the stairs several times so that he walked naturally. After a regular pattern of activity was seen on the monitoring oscilloscope, at least two recordings were made from each muscle while the subject ascended and descended the stairs. When the subject was about halfway up or down the stairs, a flash photograph was taken of his hips and lower limbs. By means of a light sensitive cell, the photographic flash was recorded on the time scale of the recording so that the exact time when the photograph was taken was known. Previously cinematograph films had been made of one subject walking up and down the stairs. A complete step during the ascent could be divided into twenty-one stages (Fig. 2) 1 2 3 4/v 5 : I tij!! 8 ( 9 10 11 12 13, L),1 n i i FIG. 2 The cinematograph film of a subject walking up stairs. It shows a step divided into twenty-one stages. The photograph below is the flash photograph taken at a random point during the recording. This photograph is matched with the appropriate stage of the divided step, in this case stage 18. and during the descent into nineteen stages (Fig. 3). A complete step on the recording was recognised by the repetition of a similar pattern of muscle activity (Fig. 4). The length on the record occupied by one step was divided into either twenty-one stages for going up the stairs or nineteen for going down. The flash photograph was matched with the appropriate stage of the divided step (Fig. 2) and the notch on the time scale (Fig. 4) marked at what stage of the recording this photograph was taken. Thus it was possible to relate the contraction of the muscle with the appropriate stages ofthe step. A muscle was considered to show significant activity if potentials which could not be attributed to artefact or to activity from a nearby muscle had an amplitude exceeding I 5 per cent of its peak value. At the beginning and end of each session a calibration signal was recorded to ensure that there was no variation in the amplifier throughout the experiment. VOL. 49 B, NO. 4, NOVEMBER 1967

776 J. JOSEPH AND R. WATSON RESULTS The periods of activity for each of the muscles in each of the subjects were tabulated and the results for each muscle in each subject compared. It was possible to detect a pattern of activity for all the muscles investigated. Figures 5 and 6 summarise the results obtained for going up and down the stairs. The beginning and end ofthe phases ofactivity were determined by calculating the means of the observations made on the six subjects. r6_i_r M V FIG. 3 The cinematograph film of a subject walking down stairs. It shows a complete step divided into nineteen stages.,, - -- - -- - - --..,..- [sso,.v A.#{149} #{149},8 A, JvVW v Wf FIG. 4 A recording from quadriceps femoris during walking up stairs. A complete step, A1 to A2, can be recognised in the upper tracing by the pattern of muscle activity beginning at A, being repeated at A2. The lower tracing is a time scale of 50 c/s. The notch B indicates when the photo flash was taken. As in walking on a flat surface, each limb while the subject is going up or down stairs has a supporting and a swinging phase. There is a period when both limbs are supporting at the same time. WALKING UP STAIRS The beginning of the step of the right limb (stage 0) is taken at the stage when the foot is flat on the stair and the left foot is beginning to leave the ground. The supporting phase of the right limb lasts for fifteen stages (0 to 14) and the swinging phase for six stages (15 to 20): thus for about two-thirds ofthe step the limb is supporting and for about one-third it is swinging. There are two periods lasting about six stages (10 to 15 and 0 to 5) when both limbs are supporting simultaneously. Tibia/is anterior is active during the swinging phase from stage 14 to stage 19. Soleus is active from stage 0 to stage 1 1, from the beginning of the supporting phase until the opposite limb is firmly placed on the step above. Quadricepsfernoris is active from stage 0 to stage 10 during the supporting phase. Its activity begins to decrease at about stage 7. THE JOURNAL OF BONE AND JOINT SURGERY

TELEMETERING ELECTROMYOGRAPHY OF MUSCLES USED IN WALKING UP AND DOWN STAIRS 777 Hamstring group shows two phases of activity: 1) between stage 12 and stage 14 during the swinging phase; and 2) between stage 18 and stage 7 during the supporting phase. In the second of these phases the beginning of the contraction is weak but after stage I the muscles are contracting strongly. Hipflexors begin to contract at stage 12 and end their contraction at stage 2. They are active during the swinging phase. Soleus - 0.. Tibialis anterior..-- -------. Quadriceps.- femoris Hamstrings Hamstrings Hamstrings #{149}Iip flexors -0- ----,_. -#{248}.: - Stuteus medius Gtuteus medws 0 Hip flexors - Gluteus maximus Erector_spinae Erector_spinae Erector spinae --- - -------0.. - L i I! I!! I I I 0 3 6 9 12 15 18 0 FRAME NUMBER FIG. 5 A summary of the results obtained from the muscles investigated during walking up stairs. The arrows indicate the beginning and end of the phase of activity. The dotted line indicates a marked decrease in activity found in only half the subjects. Gluteus medius begins to contract at stage 1 and ends its contraction at stage 10. It is contracted during the supporting phase. In three subjects there was a weak contraction between stages 13 and 16 during the swinging phase. Gluteus maximus is active from stage 1 to stage 9. The end of its contraction is more variable than that of other muscles (between stage 5 and stage 12). Erector spinae is active in two phases: 1) from stage 11 to stage 13; and 2) from stage 16 to stage 8. The contraction in the second phase is weaker from stage 3 to the end ofthe contraction and was seen in only half the subjects. It may be added that the left erector spinae was investigated in four subjects and showed a corresponding pattern of activity. WALKING DOWN STAIRS As in walking on the flat and up stairs each limb has a supporting and a swinging phase. The beginning of the step (stage 0) is when the right limb is placed flat on the stair below and the opposite limb is beginning to be raised from the stair above. The supporting phase lasts from stage 1 8 to stage 10-that is, for twelve of the nineteen stages-and the swinging phase lasts from stage I 1 to stage 1 7-that is, for seven of the nineteen stages. Both limbs VOL. 49 B, NO. 4, NOVEMBER 1967

778.i. JOSEPH AND R. WATSON are supporting from stage 7 to stage 10 and from stage 18 to stage 2. The supporting phase thus lasts about three-fifths of the complete step and the swinging phase about two-fifths. There is support by both limbs for about one-fifth of the step, and this occurs twice. Tibia/is anterior is active in two phases : 1 ) from stage 9 to stage 1 1 during the swinging phase (in all twelve subjects); and 2) from stage 17 to stage 2 (in eleven out oftwelve subjects) during the end of the swinging phase and the beginning of the supporting phase. Tibialis anterior Tibialis anterior Tibialis anterior 0. 0 Soteus 0 Soleus Ouadriceps femoris Quadriceps lemons Hamstrings Hip flexors 0. Gluteus medius Gluteus medius..- 0. Gluteus maximus Gluteus maximus Erector spinae Erector spinae Erector spinae L I I I I I I I I 1 I I I I 0 3 6 9 12 15 18 0 FRAME NUMBER FIG. 6 A summary of the results from muscles investigated during walking down stairs. Soleus is active from stage 18 to stage 7 throughout most of the supporting phase. Quadricepsfemoris shows activity from stage 16 to stage 8. This activity is decreased between stage 0 and stage 3. It really contracts strongly in two phases-at the end of the swinging phase and after the beginning of the supporting phase. Hamstring group are active from stage 1 1 to stage 1 5 during the swinging phase. Hipfiexors are active from stage 8 to stage 12. It should be added that in one subject it was impossible to obtain a recording which could be satisfactorily analysed. Gluteus medius shows activity from stage 16 to stage 6. This activity occurs during the late part of the swinging phase and most of the supporting phase. There is a decrease in activity between stages 1 8 and 0. Gluteus maximus apparently contracts in only a proportion of the subjects studied-four out of six. In spite of repeated attempts no evidence of contraction of the gluteus maximus was found in two of the subjects. The others showed a small amount of contraction from stage 18 to stage 1 at the beginning of the supporting phase. THE JOURNAL OF BONE AND JOINT SURGERY

TELEMETERING ELECTROMYOGRAPHY OF MUSCLES USED IN WALKING UP AND DOWN STAIRS 779 Erector spinae is active in two phases: 1) from stage 7 to stage 10 during the later part of the support phase; and 2) from stage 17 to stage 1 during the later part of the swinging phase. It should be added that there was considerable difficulty in determining the phases of activity of this muscle. The left erector spinae was investigated in four subjects and showed a corresponding pattern of activity. DISCUSSION Walking up stairs involves, during the supporting phase, an elevation of the body on to the stair above. This is achieved by the concerted, powerful contraction of the soleus, quadriceps femoris, hamstrings (acting as extensors of the thigh at the hip) and gluteus maximus. At the same time the body is balanced over the limb by the gluteus medius. For a short time the supporting, elevating limb remains on the stair while the opposite limb is placed firmly on the stair above and then becomes the supporting, elevating limb. It is of interest that the elevation on to the stair above is achieved by the straightening of the limb placed there and not by a lifting upwards by the calf muscles of the limb on the stair below. The contraction of the quadriceps femoris is considerably reduced after stage 7 as compared with the continued strong contraction of the soleus. The hamstrings apparently begin to contract before they act as extensors of the hip and it is suggested that in this phase of their activity they control the final extension of the leg at the knee (stages 1 8 to 20). The hamstring activity during the swinging phase causes flexion of the leg at the knee. It should be noted that this movement is to some extent inertial and not due to muscle contraction since the contraction of the hamstrings is short compared with the period of flexion. During the swinging phase the limb is dorsiflexed at the ankle, flexed at the knee and flexed at the hip. During this stage it is carried from the step below to the step above and it is important that the toe clears the step on which the opposite limb is placed. The tibialis anterior is an important muscle in achieving this. The contraction of the gluteus medius seen in some of the subjects during the swinging phase may be for the purpose of abducting the lower limb slightly as it clears the stair. Both erectores spinae contract strikingly in the early supporting phase when the trunk flexes forwards as the body is lifted upwards. The flexion ofthe trunk assists forward movement of the body. The opposite erector spinae contracts markedly during the later part of the supporting phase. This is a somewhat unexpected finding and is difficult to explain. There is considerable difficulty in picking up potentials from the flexors of the hip but apparently they contract during the swinging phase while the thigh is being flexed at the hip. Walking down stairs involves lowering the body during the supporting phase and this is achieved by the controlled lengthening of the soleus and the quadriceps femoris. The gluteus maximus contracts in only a proportion of the subjects and in these for only a short time and not much at the beginning of this activity. This prevents the trunk from flexing at the hips when the lower limb becomes supporting. The quadriceps femoris has two phases of activity which run into each other. The earlier phase is responsible for the final stage of extension of the leg at the knee at the end of the swinging phase. The later phase, together with the contraction of the soleus, is responsible for the lowering of the body. The gluteus medius also shows two peaks of activity with an intervening phase of less activity. The first peak is at the end of the swinging phase and may be a contraction to prevent the swinging limb from adducting across the midline as the pelvis pivots horizontally around the supporting limb. The second peak is the expected activity during the supporting phase and prevents the unsupported side of the body from falling. The hamstrings are responsible for flexing the leg at the knee during the swinging phase. The tibialis anterior shows two periods ofactivity. The first takes place during the swinging phase and prevents the foot from dropping as it passes the stair. The second inverts the foot as it is placed on the step below. Contrary to what happens when walking on a flat surface, the foot, while a subject walks down stairs, is placed toe to heel not heel to toe, while the weight VOL. 49 B, NO. 4, NOVEMBER 1967

780 J. JOSEPH AND R. WATSON is transferred along the outer border of the foot. Inversion of the foot by the tibialis anterior just before the supporting phase ensures that this takes place. Contraction of the soleus at this stage overcomes the dorsiflexing action of the contracting tibialis anterior. It is more difficult to explain the continued contraction of the latter muscle during the early part of the supporting phase, although it is interesting that the tibialis anterior continues to contract in the early supporting phase in walking on a flat surface. Wright, Desai and Henderson (1962) described a movement of inversion of the foot at the beginning of the supporting phase of normal walking and this may be the explanation. Again few assertions can be made about the muscles that are referred to as flexors of the hip. So far as can be determined, they actively flex the thigh on the pelvis during the early part of the swinging phase. The erector spinae contracts twice and the muscles on both sides contract at the same time. They prevent flexing of the trunk. It should be added that in many of the subjects, in repeated attempts to determine the phases of activity of the back muscles, the results varied from one session to another. It is suggested that individuals at different times walk up and down stairs with a variable degree of flexion of the trunk, thus producing variable recordings of the potentials from the back muscles. SUMMARY I. Telemetering electromyography has been used to investigate the pattern of activity of certain muscles of the lower limb and back while the subjects walked up and down stairs. 2. During walking up and down stairs each limb has a supporting and swinging phase in each complete step. 3. Walking up stairs revealed the following facts. Firstly, raising the body on to the stair above is brought about by the contraction of the soleus, quadriceps femoris, hamstrings and gluteus maximus; the gluteus medius at the same time prevents the body falling on to the unsupported side. Secondly, the tibialis anterior dorsiflexes the foot during the swinging phase and helps the limb to clear the stair on which the supporting limb is placed. Thirdly, the hamstrings flex the leg at the knee in the early part of the swinging phase and control the terminal part of extension at the knee at the end of this phase. Fourthly, both erectores spinae contract twice in each step and control the forward bending of the body at the vertebral column. 4. Walking down stairs revealed the following. Firstly, the body is lowered on to the stair below by the controlled lengthening of the soleus and quadriceps femoris ; the gluteus medius at the same time prevents the body from falling on to the unsupported side. Secondly, the tibialis anterior inverts the foot at the beginning of the supporting phase as the toe is placed on the stair below and dorsiflexes the foot in the middle of the swinging phase. Thirdly, the hamstrings control the extension of the leg at the knee during the middle of the swinging phase. Fourthly, both erectores spinae contract twice in each step and prevent forward bending of the trunk at the vertebral column. We wish to thank Mr R. George for his technical help with the apparatus, the Departments of Medical Photography and Medical Illustration for their assistance in preparing the figures, and the subjects who so willingly cooperated in the investigation. REFERENCES BATTYE, C. K., and JOSEPH, J. (1966): An Investigation by Telemetering of the Activity of Some Muscles in Walking. Medical and Biological Engineering, 4, 125. CALIFORNIA UNIVERSITY. COLLEGE OF ENGINEERING. PROSTHETIC DEVICES RESEARCH PROJECT (1 947) : Subcontractor s Report on Fundamental Studies of Human Locomotion and Other information Relating to Design ofartificiallimbs. Covering the Period from September 1945 through June 1947. 2 v. [Berkeley.] WRIGHT, D. G., DESAI, S. M., and HENDERSON, W. H. (1962): Action ofthe Subtalar and Ankle Joint Complex during the Stance Phase of Walking. Report No. 48. San Francisco: University ofcalifornia, Biomechanics Laboratory. THE JOURNAL OF BONE AND JOINT SURGERY