The lumbar paraspinal muscles (PSM) provide postural stability, enabling gait and supporting upper extremity movements.1,2 They are critical to function in a gravitational environment. In particular, these muscles facilitate vertebral motion, and protect articular structures, discs, and ligaments from excessive strain and injury.3 Atrophy of these muscles is evidenced by altered fat content, cross-sectional area (CSA), and higher proportions of type II fast-twitch fibers,4,5 and is strongly associated with low back pain on Earth.6,7 How these muscles function and respond during space flight is, however, not well described.
With microgravity exposure in space, several spine-related issues are observed among crewmembers.8 The torso lengthens 4 to 6 cm, approximately 2 to 3 times the normal diurnal increase (1–2 cm) on Earth.9,10 This reportedly occurs because of spinal unloading, flattening of spinal curvature, loss of paravertebral muscle tone, and vertebral disc degeneration.11,12 Flight medical data indicate that more than half of the US astronauts report spine pain during their mission.13–15 While in space, astronauts report that a lumbar flexed, “fetal tuck” position to stretch is the most effective way of alleviating back pain.14 The back pain is described with a moderate to severe level of intensity for 14% to 28% percent of the US astronauts. Shuttle crewmembers described pain lasting for 15% to 100% of their mission. The location of pain is reported most frequently in the following anatomic regions: 50% low back, 11% midback, 11% neck, and 1% chest. Even after their return to Earth, approximately 40% of crewmembers report spine pain.16 Another indication of lumbar pain is vertebral hypomobility from guarding,17 and preliminary data indicate such spinal stiffness is seen with prolonged space flight.18,19
Even with an exercise protocol in place during prolonged space missions, significantly decreased muscle size is seen at multiple sites in the body, including the lumbar paraspinals.20 The exercise protocols have evolved over time, but traditionally they have not specifically focused on core strengthening.21 LeBlanc and coworkers describe an exponential recovery of preflight muscle size after Mir missions, and the recovery is complete within 30 to 60 days. These measurements were made by manually tracing the outline of muscle cross-sections seen on 1.5 Tesla magnetic resonance images of 16 crew members. It is unknown whether fatty replacement, fluid redistribution, or actual lean muscle mass changes occur, such as that observed in patients or ground-based bed rest simulations of microgravity.22,23
Lastly, a concerning risk of intervertebral disc (IVD) herniation is seen postflight. The incidence of herniated nucleus pulposus is reported as 4.3 times higher in the US Astronaut Corps compared to matched aviator control populations on Earth.11 The highest risk period for disc herniation appears in the first year after return to Earth, with the majority reported within the first month of landing. It is unknown how medical staff surveillance of the astronauts versus control populations, and different behavioral decisions regarding medical care seeking and reporting by crewmembers before versus after a mission might play into the observations. It, however, does strongly suggest that structural changes in the spine associated with space adaptation result in deleterious effects occurring with the reintroduction of the gravity environment. Moreover, the consequence of disc herniation may affect an astronaut's ability to return to work on Earth or conduct work upon arriving at a planetary destination such as Mars after a long space flight.
The immediate purpose of this research is to evaluate lumbar PSM CSA and IVD heights following a 6-month International Space Station (ISS) mission and a 33- to 67-day postflight recovery period. The goals are to understand the factors involved in lumbar spine strength and back pain in crewmembers during a long mission and after increased g-loads of landing and readaptation to Earth. This could provide helpful physiological information to support a manned mission to Mars. On Earth, this information could help our understanding of spinal atrophy and degeneration due to inactivity, and potential issues involved with backpack use of military personnel, and first responders.
MATERIALS AND METHODS
Institutional research board approval was obtained from the National Aeronautics and Space Administration (NASA) and the University of California, San Diego. Six ISS crewmembers volunteered for the study, 1 woman and 5 men. The range of crewmember ages spanned 46 to 55 years, height 168 to 183 cm, and body mass 60 to 93 kg. The mission duration on the ISS ranged from 117 to 213 days. This project represents 4 years of active data collection, through 2016.
Supine lumbar spine magnetic resonance imaging (MRI) scans were conducted preflight, immediate postflight, and at least 30 days postflight recovery after an ISS mission (Figure 1 A, B). Imaging took about 80 minutes, and was performed in the morning, using a Siemens Magnetom Verio 3T system at a University of Texas Medical Branch facility outside Houston, TX. Preflight imaging was performed on average 214 days before launch. While on the ISS, the astronauts engaged in 2 to 3 hours of daily exercise with a treadmill, stationary cycle, and resistive strength training of the large muscle groups.21,24–26 After landing in Kazakhstan, the “immediate” postflight imaging was performed within 1 to 2 days, in Houston. Landing details are described elsewhere.27 The astronauts completed typical post-flight astronaut strength, conditioning, and rehabilitation exercise and activities,26 including a brief trip back to Russia, and return to Houston, TX where they were imaged again. These “Recovery” period images were performed an average of 46 days (range 33–67 days) after landing. The imaging time points are summarized in Table 1.
Functional cross-sectional area (FCSA) measurements of the lumbar PSMs were obtained using the T2-weighted MRI scans. We elected to focus on the L3/4 vertebral level, based on the relative ease of identifying muscle boundaries as compared to lower vertebral levels. The FCSA measurements involved an image-analysis thresholding technique to estimate lean muscle mass. The technical details are reported elsewhere.1,28–31 Briefly, the lumbar PSMs (multifidus, erector spinae, quadratus lumborum, and psoas) were identified and analyzed using Fiji imaging software (National Institutes of Health,32Figure 2A). Total PSM CSA was defined as the sum total of the CSAs obtained from the eight PSMs (combining right and left). Functional PSM CSA was measured using gray-scale thresholding to analyze those regions of the muscle cross-sections corresponding to dark, lean muscle mass. The analysis was conducted by one individual (R.M.H.). Our control studies showed that repeat measurements done by an individual and by several individuals were reliable and reproducible, with an intraclass correlation coefficient of 0.99, consistent with the literature.28,29 Statistical analysis was conducted using one-way, repeated measures analysis of variance (ANOVA) to establish significance, defined as P < 0.05, followed by post-hoc testing with the Newman-Keuls multiple comparison test33 with alpha = 0.05, using GraphPad Prism (version 5.04, GraphPad Software, Inc., La Jolla, CA) software.
Lastly, lumbar IVD heights were measured at the anterior, middle, and posterior sections from the L1-2 to L5-S1 disc levels (Figure 2B). The fast spin echo T2 images were obtained at the midsagittal plane,34 with slice thickness 4 mm, field of view 200, 192 × 320 image matrix, voxel size 1 × 0.6 × 4 mm, and NEX 2. For each subject, the disc height at a given lumbar intervertebral level was defined as the average of measurements made in the anterior, middle, and posterior locations along the disc, modified from the Dabbs method.35 Change in the average disc height was calculated at postflight (post-preflight), recovery (recovery-postflight), and overall change from preflight to recovery (recovery-preflight). This measurement has an uncertainty with inter- and intraobserver standard deviations of 0.2 and 0.3 mm, respectively.36 Our group has used the technique to measure changes in lumbar IVD heights with Earth-bound subjects in unloaded bedrest,34 and loaded backpack studies.36,37
Lumbar paraspinal FCSA decreased by 19% on average from a preflight value of 8737 ± 1758 mm2 (avg ± standard deviation) down to a postflight value of 7049 ± 1822 mm2. Later, there was a change in FCSA up to a recovery value of 8195 ± 1900 mm2. ANOVA testing indicates a significant difference in FCSA measured at the three time points, with F ratio 23.39, R2 0.82, and P = 0.0002. Post-hoc testing indicates the FCSA changed significantly from pre- to postflight, and from postflight to postflight recovery. The FCSA data at the recovery time point were less than the preflight values, representing a 68% recovery of the postflight loss, a difference not significantly different as determined by post-hoc testing. In comparison, the total lumbar paraspinal CSA (that encompass the unthresholded manual outlines, and therefore includes both lean muscle and nonlean muscle components) followed a similar trend at the three time points, but with nonsignificant changes (F ratio 1.44, R2 0.22, P = 0.2832, Table 2).
Expressed as a percentage of the total lumbar CSA, the relative proportion of lumbar lean muscle FCSA decreased from preflight to postflight by 14 percentage points from 86% ± 5% down to 72 ± 7%. The fraction of lumbar muscle FCSA recovered nine percentage points during the next 6 weeks to an average of 81% ± 4%. ANOVA testing indicates a significant difference in percentage FCSA measured at the three time points, with F ratio 22.25, R2 0.82, and P = 0.0002. Post-hoc testing indicates the FCSA changed significantly from pre- to postflight, and from post-flight to postflight recovery. This resulted in a significantly lower lean muscle fractional content at recovery compared with the preflight values (Figure 3).
Among the six crewmembers studied, average disc height did not change in the lumbar spine. There was no consistent pattern before and after the mission (Table 3). There was considerable disc height variability from crewmember to crewmember, over various lumbar spine levels, and along anterior-middle-posterior locations of the disc.
The present study showed reductions in total CSA with long-duration space flight, but even more dramatic reductions in functional CSA, a proxy for lean muscle mass. At 6 weeks postmission, the FCSA and CSA trended toward preflight levels. After the mission, the lumbar paraspinal extensors recovered 68% of the loss after approximately 46 days back on Earth. These ISS data are comparable to previous long-duration Mir data obtained approximately 20 years ago,20 where intrinsic back muscle total CSA decreased to 84% of preflight values, and psoas CSA decreased to 96%. Direct comparisons to that study are, however, difficult to make due to several factors.
We had six crewmembers, whereas LeBlanc and coworkers report on 16 crewmembers. We used one 3 Tesla MRI scanner in Houston operated by a single team of technicians, whereas LeBlanc et al used three 1.5 Tesla scanners at two centers (Moscow, Russia, and Houston, TX). During the missions, different exercise countermeasures were used on board more recent ISS compared with previous Mir flights.38 On Mir specifically, there were no significant resistance exercises for strength. LeBlanc and coworkers report slightly more temporal variability for scan times after landing. For example, five of the six crewmembers were scanned between day 1 and 2 after landing in the present study, whereas their first postflight measurements occurred on landing day itself or up to 4 days after landing. We focused on the L3/4 lumbar level, whereas LeBlanc and coworkers made muscle volume calculations using an unspecified region of the lumbar spine. We elected not to measure the lower lumbar levels due to the greater difficulty in identifying clear muscle boundaries in a region that typically has a greater degree of fatty atrophy/intermuscular fascial connections (e.g., lumbar intermuscular aponeurosis, lumbosacral ligaments) in the multifidi/erector spinae muscles, and a fanning/thinning of the psoas and erector spinae muscles as they traverse normally away from the lumbar spine.39 Lastly, we evaluated both total and functional CSA measurements. This provides insight into lean-muscle mass changes separated from the effects of water retention or fatty replacement.
In contrast to PSM data, individual disc height changes in the lumbar spine were small and demonstrated no consistent changes across time points. Specifically, disc height increases were not seen in a significant or consistent fashion postflight. We continue to review these data in several additional ways, including total lumbar disc height (measured by summing disc heights from every level) and total lumbar length between the L1 and the L5 vertebral bodies,40 and also by making comparisons with lumbar lordosis measurements, MRI T2 water mapping techniques41 in the discs,19 and a separate data set we collected on the subjects using upright standing MRI data.36 So far, our data are compatible to previous lumbar disc height and lumbar length measurements after short-duration space flight,40 and preliminary data from in-flight ultrasound studies of cervical and lumbar disc heights, which also do not indicate significant disc height increases or swelling.42
These measurements run counter to previous hypotheses about the effects of microgravity on disc swelling,11,43 and suggest that the torso lengthening observed in crewmembers 12,44 may be due to factors other than swelling of the IVDs. Specifically, postural straightening (i.e., a flattening of spinal lumbar lordosis and thoracic kyphosis into a “neutral body posture” in microgravity) is an important factor.12,19 Our sample size is, however, presently small for the study of IVD heights, and we have no in-flight images. Further spine analysis with additional crewmembers and in-flight ultrasound imaging will be forthcoming.
Back pain is a part of life. Approximately two-thirds of the adult population will experience low back pain and a specific pathologic anatomical diagnosis is made in only approximately 15% of cases.45 Given that, what are the implications of lowered PSM functional CSA? Back pain patients do demonstrate reduced PSM CSA.7 The positive predictive value of CSA on the development of future low back pain is, however, controversial, and it has not yet been established as a strong independent risk factor.46,47 This may be similar to other reported low back pain risk factors (such as physical demands at work, job satisfaction, bodily vibration, smoking, alcohol consumption, lumbar flexibility, etc.), where reliable predictive conclusions from the literature are difficult to make for any one person due to the many intercorrelated and confounding parameters, and the fact low back pain is common even in people without such risks. Back weakness is one known risk factor for low back pain45,48 and our laboratory is analyzing Biering-Sorensen back extension endurance data to help characterize a structure-function relationship among the crewmembers. Even so, muscle endurance and strength depend not only on CSA, but also on many other factors such as muscle contractility, metabolism, and fiber-type atrophy,49,50 and neuromuscular recruitment, coordination, fatigue mechanisms,51,52 pain, and psychosocial factors.53
Astronaut exercise programs currently emphasize the maintenance of bone mineral density, aerobic/anaerobic capacity, and muscle strength/power (focused on the large muscles of the proximal hips and shoulders) and endurance.21 Preflight, the exercise program involves a mix of cardio aerobic training, functional training for activities performed in daily life, resistive weight-training (e.g., squats and deadlifts), and familiarization of in-flight exercises. In mission there is treadmill training, cycle ergometer, and resistive training (squats, deadlifts, bench/shoulder press, rows). Postflight there are cardio workouts, resistive weight training, and functional exercise, focused on balance, proprioception, agility, coordination, and power.26 These routinized exercise programs are closely monitored by NASA Astronaut Strength, Conditioning and Rehabilitation and medical staff. With such a steady-state, maintenance program in place preflight, we do not believe that significant lumbar deconditioning or strengthening occurs between the preflight images and the flight itself. We are, however, unable to substantiate this belief because mission logistics preclude testing close to the actual launch date.
Our lumbar spine data identify a specific departure from the terrestrial, baseline anatomy of astronauts. It further suggests that an exercise countermeasure is needed to focus on the lumbar PSMs. Low load, lumbar core stabilization exercises are efficacious for back pain patients,54 deconditioned1,55 and healthy56 adults on Earth, specifically improving PSM CSA atrophy and strength,4,57–59 and acute60,61 and chronic57,62,63 low back pain. Such core-strengthening exercises specifically involve isometric exercises or lumbar extensor training. Another promising exercise countermeasure for low back pain is yoga,64 which might be particularly effective in addressing spaceflight-associated lumbar stiffness and hypomobility.15,19,65 Existing exercise interventions in microgravity that target other muscle groups are effective in addressing atrophy.38 Whether new exercise countermeasures can prevent in-flight PSM atrophy, improve spinal pain and function, shorten recovery time, and how such exercise might be performed in a micro-gravity environment with available exercise equipment need further study.
- Lumbar spine MRI data were obtained from six astronauts before, after, and approximately 46 days after a 6-month mission on board the ISS.
- Functional CSA percent of the lumbar PSMs decreased significantly by 14 percentage points during long-duration spaceflight (P = 0.002) and recovered 68% of the loss by postflight day 46.
- Lumbar IVD heights were essentially unchanged after space flight.
- Such results give insight into back pain and IVD risks, suggesting possible countermeasures targeted to the lumbar PSMs while in-flight and during the preflight and postlanding periods.
The authors thank Marilyn Johnson, Stephanie Miller, Laura Sarmiento, and Stephanie Vallarino, and Drs. S. Chiang, D. Hughes, L. Minkoff and R. Riascos-Castaneda for their work toward the success of this project. The authors also thank the International Space Station crew members for their research participation.
1. Holt JA, Macias BR, Schneider SM, et al. WISE 2005: aerobic and resistive countermeasures prevent paraspinal muscle deconditioning during 60-days bed rest in women. J Appl Physiol (1985)
2. Ward SR, Kim CW, Eng CM, et al. Architectural analysis and intraoperative measurements demonstrate the unique design of the multifidus muscle for lumbar spine stability. J Bone Joint Surg Am
3. Barr KP, Griggs M, Cadby T. Lumbar stabilization: core concepts and current literature, part 1. Am J Phys Med Rehabil
4. Mooney V, Gulick J, Perlman M, et al. Relationships between myoelectric activity, strength, and MRI of lumbar extensor muscles in back pain patients and normal subjects. J Spinal Disord
5. Mannion AF, Weber BR, Dvorak J, et al. Fibre type characteristics of the lumbar paraspinal muscles in normal healthy subjects and in patients with low back pain. J Orthop Res
6. Freeman MD, Woodham MA, Woodham AW. The role of the lumbar multifidus in chronic low back pain: a review. PM R
7. Fortin M, Macedo LG. Multifidus and paraspinal muscle group cross-sectional areas of patients with low back pain and control patients: a systematic review with a focus on blinding. Phys Ther
8. Sayson JV, Hargens AR. Pathophysiology of low back pain during exposure to microgravity. Aviat Space Environ Med
9. Brown JW. The Apollo-Soyuz Test Project Medical Report. 1977; Washington, DC: Scientific and Technical Information Office National Aeronautics and Space Administration, 119–121.
10. Young KS, S Rajulu S. The effects of microgravity on seated height (spinal elongation). NASA Human Research Program Investigator's Workshop
. February 14–16, 2011. Houston, TX.
11. Johnston SL, Campbell MR, Scheuring R, et al. Risk of herniated nucleus pulposus among U.S. astronauts. Aviat Space Environ Med
12. Andreoni G, Rigotti C, Baroni G, et al. Quantitative analysis of neutral body posture in prolonged microgravity. Gait Posture
13. Wing PC, Tsang IK, Susak L, et al. Back pain and spinal changes in microgravity. Orthop Clin North Am
14. Kerstman EL, Scheuring RA, Barnes MG, et al. Space adaptation back pain: a retrospective study. Aviat Space Environ Med
15. Pool-Goudzwaard AL, Belavy DL, Hides JA, et al. Low back pain in microgravity and bed rest studies. Aerosp Med Hum Perform
16. Laughlin MS, Murray JD, Wear ML, et al. Post-flight back pain following International Space Station missions: evaluation of spaceflight risk factors. 2016 Human Research Program Investigator's Workshop
. February 8, 2016, Galveston, TX.
17. Dvorak J, Panjabi M, Novotny J, et al. Clinical validation of functional flexion-extension roentgenograms of the lumbar spine. Spine
18. Chang DG, Sayson JV, Chiang S, et al. Risk of intervertebral disc damage after prolonged space flight. International Olympic Committee, World Conference on Prevention of Injury & Illness in Sport
. April 10–12, 2014, Monte-Carlo, Monaco.
19. Bailey JF, Miller SL, Healey RM, et al. Long-Duration Spaceflight Affects Passive and Active Lumbar Stabilization and Health: An Imaging Study on NASA Crew. Orlando, FA: Orthopaedic Research Society; 2016.
20. LeBlanc A, Lin C, Shackelford L, et al. Muscle volume, MRI relaxation times (T2), and body composition after spaceflight. J Appl Physiol (1985)
21. Loehr JA, Guilliams ME, Petersen N, et al. Physical training for long-duration spaceflight. Aerosp Med Hum Perform
22. Elliott J, Pedler A, Jull G, et al. Differential changes in muscle composition exist in traumatic and non-traumatic neck pain. Spine (Phila Pa 1976)
23. Conley MS, Foley JM, Ploutz-Snyder LL, et al. Effect of acute head-down tilt on skeletal muscle cross-sectional area and proton transverse relaxation time. J Appl Physiol (1985)
24. Smith SM, Heer MA, Shackelford LC, et al. Benefits for bone from resistance exercise and nutrition in long-duration spaceflight: evidence from biochemistry and densitometry. J Bone Miner Res
25. Hargens AR, Bhattacharya R, Schneider SM. Space physiology VI: exercise, artificial gravity, and countermeasure development for prolonged space flight. Eur J Appl Physiol
26. Ragusa P. Helping Astronauts Stay Fit in Zero G. Government Recreation and Fitness. Westbury, NY: Ebmpubs; 2011.
28. Ranson CA, Burnett AF, Kerslake R, et al. An investigation into the use of MR imaging to determine the functional cross sectional area of lumbar paraspinal muscles. Eur Spine J
29. Fortin M, Battie MC. Quantitative paraspinal muscle measurements: inter-software reliability and agreement using OsiriX and ImageJ. Phys Ther
30. Snyder AJ, Macias BR, Healey RM, et al. Lumbar paraspinal muscle atrophy during long duration spaceflight. Experimental Biology
. March 28–April 1, 2015, Boston, MA.
31. Chang DG, Healey RM, Holt JA, et al. Cervical Spine Intervertebral Disc and Paraspinal Muscle Morphology in Humans after 6-month Microgravity Exposure and 30-day Terrestrial Recovery. Copenhagen, Denmark: Eurospine; 2015.
32. Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods
33. Hancock GR, Klockars AJ. The quest for α: development in multiple comparison procedures in the quarter century since Games (1971). Rev Educ Res
34. Cao P, Kimura S, Macias BR, et al. Exercise within lower body negative pressure partially counteracts lumbar spine deconditioning associated with 28-day bed rest. J Appl Physiol (1985)
35. Dabbs VM, Dabbs LG. Correlation between disc height narrowing and low-back pain. Spine (Phila Pa 1976)
36. Shymon S, Hargens AR, Minkoff LA, et al. Body posture and backpack loading: an upright magnetic resonance imaging study of the adult lumbar spine. Eur Spine J
37. Neuschwander TB, Cutrone J, Macias BR, et al. The effect of backpacks on the lumbar spine in children: a standing magnetic resonance imaging study. Spine (Phila Pa 1976)
38. Smith SM, Abrams SA, Davis-Street JE, et al. Fifty years of human space travel: implications for bone and calcium research. Annu Rev Nutr
39. Kalimo H, Rantanen J, Viljanen T, et al. Lumbar muscles: structure and function. Ann Med
40. LeBlanc AD, Evans HJ, Schneider VS, et al. Changes in intervertebral disc cross-sectional area with bed rest and space flight. Spine (Phila Pa 1976)
41. Marinelli NL, Haughton VM, Munoz A, et al. T2 relaxation times of intervertebral disc tissue correlated with water content and proteoglycan content. Spine (Phila Pa 1976)
42. Ebert D, Sargsyan AE, Garcia KM, et al. Spinal changes in response to spaceflight. NASA Human Research Program Investigator's Workshop: Integrated Pathways to Mars
. January 13–15, 2015, Galveston, TX.
43. Belavy DL, Adams M, Brisby H, et al. Disc herniations in astronauts: what causes them, and what does it tell us about herniation on earth? Eur Spine J
44. Rajulu S, Young K, Mesloh M. Preliminary results of the effect of microgravity on seated height. International Academy of Astronautics: Humans in Space Symposium
. April 11–15, 2011, Houston, TX.
45. Deyo R, Weinstein J. Low back pain. N Engl J Med
46. Fortin M, Gibbons LE, Videman T, et al. Do variations in paraspinal muscle morphology and composition predict low back pain in men? Scand J Med Sci Sports
47. Suri P, Fry AL, Gellhorn AC. Do muscle characteristics on lumbar spine magnetic resonance imaging or computed tomography predict future low back pain physical function, or performance? a systematic review. PM R
48. Latimer J, Maher CG, Refshauge K, et al. The reliability and validity of the Biering-Sorensen test in asymptomatic subjects and subjects reporting current or previous nonspecific low back pain. Spine (Phila Pa 1976)
49. Fitts RH, Riley DR, Widrick JJ. Functional and structural adaptations of skeletal muscle to microgravity. J Exp Biol
2001; 204 (pt 18):3201–3208.
50. Roy RR, Baldwin KM, Edgerton VR. Response of the neuromuscular unit to spaceflight: what has been learned from the rat model. Exerc Sport Sci Rev
51. Grassi B, Rossiter HB, Zoladz JA. Skeletal muscle fatigue and decreased efficiency: two sides of the same coin? Exerc Sport Sci Rev
52. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev
53. Dedering A, Harms-Ringdahl K, Nemeth G. Back extensor muscle fatigue in patients with lumbar disc herniation. Pre-operative and post-operative analysis of electromyography, endurance time and subjective factors. Eur Spine J
54. Hadala M, Gryckiewicz S. The effectiveness of lumbar extensor training: local stabilization or dynamic strengthening exercises. A review of literature. Ortop Traumatol Rehabil
55. Belavy DL, Armbrecht G, Gast U, et al. Countermeasures against lumbar spine deconditioning in prolonged bed rest: resistive exercise with and without whole body vibration. J Appl Physiol (1985)
56. Steffens D, Maher CG, Pereira LS, et al. Prevention of low back pain: a systematic review and meta-analysis. JAMA Intern Med
57. Kliziene I, Sipaviciene S, Klizas S, et al. Effects of core stability exercises on multifidus muscles in healthy women and women with chronic low-back pain. J Back Musculoskelet Rehabil
58. Danneels LA, Vanderstraeten GG, Cambier DC, et al. Effects of three different training modalities on the cross sectional area of the lumbar multifidus muscle in patients with chronic low back pain. Br J Sports Med
59. Akbari A, Khorashadizadeh S, Abdi G. The effect of motor control exercise versus general exercise on lumbar local stabilizing muscles thickness: Randomized controlled trial of patients with chronic low back pain. J Back Musculoskelet
60. Hides JA, Jull GA, Richardson CA. Long-term effects of specific stabilizing exercises for first-episode low back pain. Spine (Phila Pa 1976)
61. Biering-Sorensen F. Physical measurements as risk indicators for low-back trouble over a one-year period. Spine (Phila Pa 1976)
62. Moon HJ, Choi KH, Kim DH, et al. Effect of lumbar stabilization and dynamic lumbar strengthening exercises in patients with chronic low back pain. Ann Rehabil Med
63. Steele J, Bruce-Low S, Smith D. A review of the clinical value of isolated lumbar extension resistance training for chronic low back pain. PM R
64. Chang DG, Holt JA, Sklar M, et al. Yoga as a treatment for chronic low back pain: a systematic review of the literature. J Orthop Rheumatol
65. Vernikos J, Deepak A, Sarkar DK, et al. Yoga therapy as a complement to astronaut health and emotional fitness-stress reduction and countermeasure effectiveness before, during, and in post-flight rehabilitation: a hypothesis. Gravit Space Biol