Effect of prolonged bed rest on the anterior hip muscles Gait & Posture

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Gait & Posture 30 (2009) 533–537

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Effect of prolonged bed rest on the anterior hip muscles M. Dilani Mendis a,*, Julie A. Hides a, Stephen J. Wilson b, Alison Grimaldi a, Daniel L. Belavy´ c, Warren Stanton d, Dieter Felsenberg c, Joern Rittweger e, Carolyn Richardson a a

The University of Queensland, School of Health and Rehabilitation Sciences, Division of Physiotherapy, St Lucia, Brisbane, Qld 4072, Australia The University of Queensland, School of Information Technology and Electrical Engineering, Qld 4072, Australia c Zentrum fu¨r Muskel-und Knochenforschung, Charite´ Campus Benjamin Franklin, Hindenburgdamm 30, 12200 Berlin, Germany d Mater Health Services Brisbane Limited, South Brisbane, Qld, Australia e Institute for Biomedical Research into Human Movement and Health, Manchester Metropolitan University, Cheshire, United Kingdom b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 24 September 2008 Received in revised form 24 July 2009 Accepted 5 August 2009

Prolonged bed rest and inactivity is known to cause muscular atrophy with previous research indicating that muscles involved in joint stabilisation are more susceptible. The anterior hip muscles are important for hip joint function and stability but little is known about the effects of prolonged inactivity on their function. This study investigated the effect of prolonged bed rest on the size of the anterior hip muscles and their pattern of recovery. The effect of resistive vibration exercise (RVE) as a countermeasure to muscle atrophy was also investigated. 12 male participants, randomly assigned to either a control or an exercise group, underwent 8 weeks of bed rest with 6 months follow-up. Changes in muscle crosssectional area (CSA) of the iliacus, psoas, iliopsoas, sartorius and rectus femoris muscles were measured by magnetic resonance imaging at regular intervals during bed rest and recovery phases. CSAs of iliopsoas and sartorius decreased at the hip joint (p < 0.05) during bed rest but iliacus, psoas, and rectus femoris CSAs were unchanged (p > 0.05). No signiﬁcant difference was found between the two groups for all muscles (all p > 0.1), suggesting inefﬁcacy of the countermeasure in this sample. These ﬁndings suggest that prolonged bed rest can result in the atrophy of speciﬁc muscles across the hip joint which may affect its stability and function. ß 2009 Elsevier B.V. All rights reserved.

Keywords: Bed rest Hip joint Muscle atrophy Iliopsoas Magnetic resonance imaging

1. Introduction The hip joint is designed to support large forces during weight bearing activities. The muscles that cross the hip joint are important for its optimal function as well as for its stabilisation and protection [1]. A recent musculoskeletal modeling study found that simulated weakness in the iliopsoas muscle during hip ﬂexion resulted in increased anterior hip joint forces [2]. Muscular dysfunction in the hip could, therefore, increase the risk of joint injury through excessive or abnormal loading of the joint. Muscle dysfunction can occur as a result of loss of gravitational loading and prolonged inactivity [3]. Bed rest studies simulate microgravity environments and allow investigation of the effects of prolonged inactivity on the human body. So far, these studies have found that prolonged bed rest causes signiﬁcant changes in the musculoskeletal system. Bone loss, altered motor control, decreased muscle size and strength are just some of the changes

* Corresponding author. Tel.: +61 7 3346 7467. E-mail address: [email protected] (M. Dilani Mendis). 0966-6362/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2009.08.002

that occur [4]. These studies have also found that different muscles respond differently to the loss of weight bearing functional activity. In the ﬁrst Berlin Bed Rest Study, atrophy of the deep lumbar multiﬁdus muscles, but not the superﬁcial back muscles, was found after 60 days of bed rest [5]. Deep muscles in close proximity to a joint are thought to provide joint stability and protection while superﬁcial muscles crossing multiple joints generate torque and produce joint movement [6]. It has been proposed that deep muscles, like the multiﬁdus, are more susceptible to atrophy from the loss of weight bearing activity [7]. So far, little is known about the effects of prolonged inactivity on the hip muscles. Only one study investigated the response to 5 weeks of bed rest in the hip extensor muscles using computerized tomography (CT) scans and they found a small decrease in size [8]. The deep anterior hip muscles, in particular the iliacus and psoas muscles, may have a role in joint protection and stability during weight bearing activity in addition to its role as a hip ﬂexor. Andersson et al. [9] highlighted the role of the iliacus and psoas muscles in stabilisation of the lumbopelvic region during single leg stance and sitting. Therefore, these muscles may be more susceptible than the superﬁcial anterior hip muscles to atrophy from prolonged bed rest.

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M. Dilani Mendis et al. / Gait & Posture 30 (2009) 533–537

Various exercise programs have been used in an attempt to counter muscle atrophy in previous bed rest studies. In the Berlin Bed Rest Study resistive vibration exercise (RVE) was used which involved the use of whole body vibration (WBV) with resistive exercises that simulated weight bearing activity. The combination of WBV and closed chain resistance exercise is thought to improve muscle function through the stimulation of the muscle spindle system and improved joint proprioception [10,11]. RVE was effective in minimising soleus, quadriceps and multiﬁdus muscle atrophy during prolonged bed rest [11–13] however its effect on the hip muscles has not been investigated. Therefore the aims of our study were to investigate if prolonged bed rest would result in the atrophy of the deep (iliacus and psoas) but not the superﬁcial (sartorius and rectus femoris) anterior hip muscles; and to investigate their pattern of recovery after bed rest. A further aim of this study was to determine the effectiveness of RVE as a countermeasure to anterior hip muscle atrophy during bed rest. 2. Methods Ethical clearance for this study was obtained from the institutional ethics committee and by the Bundesamt fu¨r Strahlenschutz. Written informed consent was given by the participants. Details of participant recruitment and selection, bed rest protocol, and exercise protocol are published elsewhere [14]. In brief, 20 healthy men aged 20–45 years were recruited and selected to undergo 8 weeks of bed rest with a 6-month follow-up. Participants were randomly allocated to a control (CTRL) group and an exercise (RVE) group. The CTRL group was inactive during bed rest while the RVE group underwent a countermeasure of resistive vibration exercise. One participant (RVE) could not be included in this study as he became claustrophobic during MRI testing and the desired sequences were not performed. A further seven participants’ hip muscle scans (four CTRL, three RVE) had to be excluded from analysis because the initial imaging protocol implemented did not permit adequate resolution of the muscles of interest. Therefore, the analysis for this study was based on six CTRL subjects (mean age: 34.5 5.9 years, height: 181.7 5.9 cm, weight: 75.1 8.3 kg) and six RVE subjects (mean age: 29.8 4.4 years, height: 179.7 7.8 cm, weight: 76.6 4.9 kg).

and knees supported in a neutral position. Transverse images were taken using a 1.5 Tesla Magnetom Vision System (Siemens, Erlangen, Germany). A T2 protocol was used with TR = 7200 ms, TE = 15 ms and resolution = 238 mm 512 mm to obtain 45 contiguous slices (slice thickness = 7 mm) from the top of the iliac crest. Images were saved on to disk and measured on a computer. Measurement of muscle size was performed by manual tracing of the outline of each relevant muscle (Fig. 1) and calculation of its cross-sectional area (CSA) with the use of Image J software (version 1.38x, http://rsb.info.nih.gov/ij/). Only the left side was measured as repeated strength testing was carried out, as part of another project [12], on the right leg of both groups. As the iliacus and psoas muscles fuse to form the iliopsoas muscle, it was decided to take an additional measure of these muscles at the level of the hip joint. Therefore, for each subject, the mean CSA of the iliacus and the psoas muscles was taken from four consecutive slices at the level of the sacrum where these muscles were separate. The mean CSA of the iliopsoas and sartorius muscles was taken from seven consecutive slices from the top of the femoral head and the mean CSA of the rectus femoris muscle was taken from four consecutive slices at the proximal thigh below the greater trochanter (Fig. 2). This method of measurement was based on previously published studies [5,12]. 2.4. Statistical analysis SPSS for Windows (version 15; www.spss.com) was used for data analysis. Due to equipment failure, CSA measurements for three data points were missing (BR14 rectus femoris, R14 iliacus and psoas) in two subjects. Using SPSS, linear interpolation of the data set was used to estimate these missing data points (0.6% of the total data set). A repeated measures ANOVA with a Type I sums of squares model was used to analyse the effect of bed rest on muscle size with ‘time’ as a within-subject factor and ‘group’ (CTRL and RVE) as a between-subject factor. Age, height and weight were used as covariates in the analysis. A Type I sums of squares model was chosen as our research has found a Type III sums of squares model to be problematic for higher-order interactions involving muscle size and

2.1. Bed rest protocol Participants were required to undergo 8 weeks of strict bed rest during which they performed all hygiene activities in the supine position, they were unable to stand or lift their trunk more than 308 and they were transported for MRI testing in the supine position. Subjects were discouraged from doing any excessive or unnecessary movement. Compliance was ensured by video monitoring and force sensors in the bed frames. 2.2. Exercise protocol The RVE group performed a set of resistive vibration exercises twice a day except for Sundays and Wednesday afternoons. The subjects remained in the supine position with both feet on a suspended vibrating platform (Galileo Space, Novotec Medical, Pforzheim, Germany) speciﬁcally designed for the Berlin Bed Rest Study. The apparatus was constructed so that a force of approximately two times the body weight was generated through the subjects’ bodies by elastic springs that were attached to them around their shoulders, pelvis and hands. In the afternoon exercise sessions, the compressive force used was 60–80% of the force used during the morning sessions. The exercise regimen consisted of squats (performed by extending the knees from 908 of hip and knee ﬂexion), heel raises (performed by raising the heels into ankle plantar ﬂexion with the knees kept in near extension and the hips in slight ﬂexion) and toe raises (performed by raising the forefoot into ankle dorsiﬂexion with the knees and hips in a similar position to the heel raises). Each exercise was performed for more than 60 s. During the morning sessions, participants also performed 10 repetitions of ‘kicks’ which involved extending the knees forcefully against the platform from a position of near full hip and knee ﬂexion. Depending on their tolerance, the vibration frequency was gradually increased over time (initial frequency: 19 Hz, maximum frequency: 26 Hz, amplitude: 5–6 mm) in order to progress the training stimulus. 2.3. MRI protocol To examine the effect of bed rest on muscle size, MRI measurements were conducted on the ﬁrst day of bed rest (BR1) and then at 2-week intervals until the end of the bed rest period (BR14, BR28, BR42, BR56). During the recovery phase, scanning was conducted on the 4th day after reambulation (R+4) and then at increasing intervals until 180 days after the bed rest period (R+14, R+28, R+90, R+180). Participants lay in a supine position on the imaging table with their hips

Fig. 1. Measurement of individual muscle cross-sectional area on MRI slices taken from the hip region. PS, psoas muscle; IL, iliacus muscle; ILP, iliopsoas muscle; S, sartorius muscle; RF, rectus femoris muscle.

M. Dilani Mendis et al. / Gait & Posture 30 (2009) 533–537

Fig. 2. Levels at which MRI slices were taken for measurement of individual muscle cross-sectional area. IL, iliacus muscle; PS, psoas muscle; ILP, iliopsoas muscle; S, sartorius muscle; RF, rectus femoris muscle. weight [15]. For the bed rest data, a priori contrasts were used to test changes in muscle size from baseline (BR1) to each time point (BR14, BR28, BR42, BR56). Due to the systematic increase in time for the recovery data, muscle size at baseline (BR1) was compared separately to each recovery time point (R+4, R+14, R+28, R+90, R+180) using repeated measures ANOVA with ‘time’ as a within-subject factor and ‘group’ as a between-subject factor. As multiple analyses were conducted, an a of 0.01 was taken for statistical signiﬁcance for the recovery analysis. In addition, the effect of attrition was examined using ANOVA to compare the cases assessed at R+4 (n = 3) versus cases not assessed at R+4 (n = 3) on their muscle size at all other time points during bed rest and recovery.

3. Results There were signiﬁcant changes in muscle size over time. Table 1 depicts the changes in mean CSA of each muscle during the bed rest Table 1 Mean cross-sectional area (cm2) of each muscle during bed rest and recovery phasesa. Iliacus

Psoas

Iliopsoas

Sartorius

Rectus femoris

19.3 4.1 15.0 1.6 4.1 0.6 18.3 3.1 BR1 13.9 1.4 n = 12 BR14 14.7 2.0 18.9 4.5 14.3 1.6* 3.9 0.6 18.1 3.8 n = 12 * BR28 14.5 2.3 18.7 4.5 14.4 1.8 4.0 0.5 18.2 3.4 n = 12 BR42 13.8 2.4 19.1 4.4 14.4 1.6* 3.9 0.6* 18.3 3.5 n = 12 BR56 13.9 2.2 18.9 3.9 14.7 1.8 3.8 0.5** 18.4 3.2 n = 12 R+4 11.9 3.3 19.6 2.2 14.6 0.2 3.8 0.9 17.1 2.3 n=6 R+14 15.3 2.0 19.8 3.5 15.1 2.9 4.1 0.6 18.2 1.6 n=9 R+28 14.7 2.5 19.0 4.3 14.6 2.1 4.1 0.7 18.5 2.1 n = 11 R+90 14.3 1.5 18.4 4.3 14.5 1.9 3.9 0.5 18.8 2.8 n = 11 ** ** R+180 13.6 1.0 17.0 3.7 14.0 1.8 4.0 0.6 19.0 2.7 n = 10 a Data pooled for CTRL and RVE groups due to lack of group effect. BR: bed rest, R+: recovery. Values are marginal mean standard deviation adjusted for age, height and weight * p < 0.05. ** p < 0.01.

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and recovery phases for both groups combined. Compared to the baseline measurement (BR1), iliopsoas muscle CSA had signiﬁcantly decreased within 14 days of bed rest (F = 8.17, p = 0.02) and continued to be signiﬁcantly less than baseline until day 42 of bed rest (F = 11.48, p = 0.01). By the end of bed rest, the decrease in iliopsoas muscle CSA indicated a trend toward signiﬁcance (p = 0.08). The decrease in sartorius muscle CSA achieved signiﬁcance at day 42 of bed rest (F = 7.96, p = 0.03) and was still signiﬁcantly smaller compared to baseline at BR56 (F = 16.11, p = 0.005). There was no statistically signiﬁcant change in the iliacus, psoas and rectus femoris muscle CSAs during the bed rest period (all p > 0.05). During the recovery period there were no signiﬁcant changes in size, compared to baseline, for all the muscles (p > 0.01) up to 90 days post-bed rest. However, at 180 days after bed rest, there was a signiﬁcant decrease in CSA compared to baseline for the psoas (F = 27.57, p = 0.003) and iliopsoas (F = 41.44, p = 0.001) muscles. Results of the analysis of attrition at R+4 indicated that the cases included in the analysis were representative of the whole group for each muscle (all F < 2.85, all p > 0.14) except for the iliacus muscle (p < 0.05). Effectiveness of the exercise countermeasure to prevent muscle atrophy during bed rest is indicated in the analysis by the interaction effect between the factors of ‘group’ and ‘time’. Results showed that there was no statistically signiﬁcant difference between the CTRL and RVE groups across time for any of the muscles (all F < 2.13, all p > 0.10). Power calculations for the effect sizes found in this study showed that the sample size was sufﬁcient to detect a ‘group’ by ‘time’ effect for the psoas muscle at a power of greater than 0.8, but not the iliacus, iliopsoas, sartorius or rectus femoris muscles. Table 2 shows the changes in mean CSA for each muscle within each group over time. 4. Discussion In this study, we investigated the effect of prolonged bed rest on the deep and superﬁcial muscles of the anterior hip joint. The most important ﬁnding was that the deep iliopsoas muscle signiﬁcantly atrophied at the level of the hip joint in response to a loss of weight bearing activity. Previous studies have proposed that the deep iliacus and psoas muscles are important in joint stabilisation from their activation in motor tasks and gait [9,16] and this may explain the preferential atrophy. Muscle atrophy across the hip joint could be due to the lack of normal proprioceptive input during bed rest. Lack of afferent input can affect muscle recruitment patterns, for example, lack of gravitational load cues have resulted in a tonic to phasic shift in activity of the lumbopelvic muscles while decreased activity was found in the soleus muscles [17,18]. These motor control changes could lead to changes in the muscle ﬁbres resulting in atrophy. Alternatively, the atrophy in different parts of the iliopsoas muscle could be due to the distribution of ﬁbre types within the muscle. Fibre typing of the iliacus muscle in cats found ﬁbres in the deep region of the muscle close to the hip joint to be shorter in length and composed of a higher percentage of slow and oxidative ﬁbres [19]. Postural muscles with a relatively large proportion of slow type I ﬁbres are proposed to be most vulnerable to atrophy from immobilisation [20] and this could explain the response of the iliopsoas muscle at the hip joint. Of the superﬁcial anterior hip muscles, atrophy of the sartorius muscle across the hip joint was signiﬁcant. Considering that the sartorius is a superﬁcial bi-articular muscle, it was expected to be less susceptible to atrophy. Interestingly, Akima et al. [21] also found sartorius muscle atrophy after 20 days of bed rest. This may indicate that this muscle has an accessory role in stabilisation of the pelvis as well as being a hip ﬂexor. Previous EMG studies in gait analysis have reported sartorius activity early in stance phase

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Table 2 Mean cross-sectional area (cm2) of each muscle during bed rest and recovery in the control (CTRL) and exercise (RVE) groupsa. Iliacus

BR1 Ctrl n = 6 Rve n = 6 BR14 Ctrl n = 6 Rve n = 6 BR28 Ctrl n = 6 Rve n = 6 BR42 Ctrl n = 6 Rve n = 6 BR56 Ctrl n = 6 Rve n = 6 R+4 Ctrl n = 3 Rve n = 3 R+14 Ctrl n = 3 Rve n = 6 R+28 Ctrl n = 6 Rve n = 5 R+90 Ctrl n = 5 Rve n = 6 R+180 Ctrl n = 4 Rve n = 6

Psoas

Iliopsoas

Sartorius

Rectus femoris

CTRL

RVE

CTRL

RVE

CTRL

RVE

CTRL

RVE

CTRL

RVE

13.0 2.4

14.9 1.9

19.2 4.4

19.5 3.4

14.4 2.4

15.6 1.8

4.3 0.6

4.0 0.7

18.4 3.8

18.3 3.0

14.1 3.0

15.3 2.6

19.5 4.4

18.2 3.8

14.0 2.0

14.5 1.0

4.2 0.5

3.7 0.7

18.1 4.4

18.2 2.5

14.0 3.1

15.1 3.1

19.2 5.1

18.1 3.1

13.7 2.3

15.0 1.6

4.3 0.5

3.8 0.6

17.7 4.2

18.8 2.8

13.6 2.5

14.0 2.9

19.4 4.4

18.8 3.5

14.0 2.1

14.8 1.2

4.2 0.6

3.8 0.6

17.8 4.0

18.8 2.8

13.0 2.8

15.0 2.6

19.8 4.1

18.1 3.4

14.3 2.4

15.1 1.5

4.0 0.5

3.7 0.6

17.4 4.0

19.3 2.5

11.0 1.7

12.8 2.3

18.8 5.6

20.3 5.2

14.0 2.8

15.3 0.6

3.9 0.4

3.7 0.8

15.6 2.6

18.6 2.4

14.5 2.2

15.7 2.5

21.7 1.6

18.5 3.5

15.2 1.3

15.0 2.4

4.4 0.8

3.8 0.4

16.6 0.8

19.1 2.4

13.6 2.6

16.1 2.7

19.8 4.4

18.3 3.1

14.2 2.5

15.3 2.0

4.3 0.5

3.9 0.8

17.8 3.7

19.9 3.2

13.2 2.0

15.2 2.4

18.5 4.3

18.3 3.6

13.7 2.3

15.2 1.9

4.0 0.3

3.8 0.7

18.7 5.1

18.7 3.1

12.4 2.8

14.4 2.1

17.2 4.4

16.6 2.8

13.6 2.8

14.0 1.6

4.4 0.1

3.6 0.8

19.2 4.0

18.4 3.8

For descriptive purposes, values are mean standard deviation. a BR: bed rest, R+: recovery.

during weight bearing support as well as at the end of stance phase and the beginning of swing phase to assist in hip ﬂexion [22,23]. However, further research into the activation of the sartorius muscle in different postural and motor tasks is required to clarify this role. In contrast, the rectus femoris muscle did not change signiﬁcantly during prolonged bed rest. Lack of atrophy for this muscle was similar to the results found in human and animal studies [24,25]. As Lieber et al. [25] proposed, the rectus femoris muscle may atrophy the least during prolonged immobilisation because it is a phasically activated muscle crossing multiple joints. A further aim of our study was to investigate the pattern of muscle recovery after prolonged bed rest. No signiﬁcant difference to baseline levels was found for all the muscles in the initial recovery period (R+4 to R+90) indicating that the iliopsoas and sartorius muscles recovered to baseline sizes. The signiﬁcant decrease in size in the iliopsoas and psoas muscles at 6 months post-bed rest is an unusual ﬁnding with no plausible explanation and may be an artefact in this small sample. As there have been no other studies investigating the iliopsoas muscle in prolonged bed rest, it is not possible to compare our results to others. However, these ﬁndings will be investigated in the second Berlin Bed Rest Study which is currently in progress. It should be mentioned that due to smaller subject numbers at R+4 a closer examination of the data was conducted. Analysis of attrition indicated that the cases assessed at R+4 were representative of the sample for most of the muscles. Only the results for the iliacus muscle at R+4 should be treated with more caution. Another ﬁnding of this study was the lack of effectiveness of RVE in minimising atrophy or increasing the size of the hip ﬂexor muscles during bed rest. This result differs from previous studies which found RVE to be an effective countermeasure to muscle atrophy in the lower limbs and spine [11–13]. A possible reason for the lack of effect in our study may be that the resistive exercises chosen did not speciﬁcally target or load the hip ﬂexors.

Alternatively, it may be that this sample size was too small to detect an effect for some of the muscles as indicated by power calculations. Detection of a group difference across time, would require sample sizes of 5 for the psoas muscle and 7 for the rectus femoris muscle, indicating that the sample size in this study was sufﬁcient. However, more than 300 in each group would be required for the other muscles. In conclusion, prolonged bed rest resulted in the preferential atrophy of the iliopsoas as well as the sartorius muscle at the hip joint. The ﬁnding of differential atrophy within the anterior muscle complex at the hip joint has implications for joint function. Speciﬁc muscle atrophy around the hip joint may result in muscular imbalances and increase vulnerability to injury through abnormal loading of the joint. Muscle imbalances at the hip joint can have repercussions on the spine and lower limb kinetic chain in many functional weight bearing tasks. These ﬁndings would suggest that targeted rehabilitation programs are required following a prolonged period of inactivity. Acknowledgements The Berlin Bed Rest Study was funded by Grant No. 14431/02/ NL/SH2 from the European Space Agency and by the Charite´ Campus Benjamin Franklin. This study was conducted at the Charite´ Campus Benjamin Franklin hospital in Berlin, Germany. M. Dilani Mendis was supported by a post-graduate scholarship from the NHMRC (Grant ID: 511258). Conﬂict of interest statement We afﬁrm that we have no ﬁnancial afﬁliation or involvement with any commercial party that has a direct ﬁnancial interest in any matter included in this manuscript.

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Influence of prolonged bed-rest on spectral and ...