Issue 23-4, 2024

DISSERTATION ORBIT

https://doi.org/10.38025/2078-1962-2024-23-4-92-100

Secondary Sarcopenia in Patients with Locomotor Disorders: Prevalence, Diagnosis and Medical Rehabilitation. А Review

View article (Download PDF file)



Download XML file

1 ORCIDKirill D. Kuznetsov,1 ORCIDLarisa A. Marchenkova

1 National Medical Research Center for Rehabilitation and Balneology, Moscow, Russia


ABSTRACT

INTRODUCTION. The development of rehabilitation methods for patients with sarcopenia, a generalized age-associated loss of skeletal muscle mass and strength, is important, since sarcopenia leads to pronounced weakness, functional and motor disorders and an increased risk of death in the elderly.

AIM. To analyze the prevalence, features of pathogenesis, diagnosis of secondary sarcopenia, including against the background of motor disorders due to stroke, as well as methods of treatment and medical rehabilitation of such patients.

MAIN CONTENT. Among the secondary forms, sarcopenia is of the greatest clinical importance against the background of the consequences of acute cerebrovascular accident (ACA), due to muscular atrophy associated with paralysis and immobility, spasticity, inflammation and denervation of muscles, malnutrition and intestinal absorption of protein and vitamin D. Recent studies show that the prevalence of sarcopenia in stroke patients in emergency hospitals is 8.5–33.8 %, according to other data — more than 42 %. Muscle weakness after a stroke contributes to a decrease in physical functions and the development of disability, and sarcopenia leads to adverse outcomes 90 days after a stroke. According to the meta-analysis, which included 7 cohort studies with a total sample of 1,774 patients who underwent ACA, 27.1 % of them had sarcopenia. Moreover, the presence of sarcopenia negatively affected the clinical and functional outcomes of ACA, as well as the results of medical rehabilitation (odds ratio: 2.42, 95 % confidence interval: 1.76–3.33, p < 0.001).

CONCLUSION. Despite the prevalence and relevance of this pathology, rehabilitation programs for patients with sarcopenia against the background of the consequences of ACA have not been developed. Isolated foreign publications demonstrate the effectiveness of certain methods of physical therapy and electrical stimulation, but the evidence base for their effectiveness is low.


KEYWORDS: sarcopenia, acute cerebrovascular accident, medical rehabilitation, mechanotherapy, electrical stimulation

FUNDING: The authors declare no external funding in the conduct of the study.

CONFLICT OF INTEREST: The authors declare no apparent or potential conflicts of interest related to the publication of this article.

FOR CITATION:

Kuznetsov K.D., Marchenkova L.A. Secondary Sarcopenia in Patients with Locomotor Disorders: Prevalence, Diagnosis and Medical Rehabilitation. A Review. Bulletin of Rehabilitation Medicine. 2024; 23(4):92-100. https://doi.org/10.38025/2078-1962-2024-23-4-92-100

FOR CORRESPONDENCE:

Kirill D. Kuznetsov, E-mail: kuznetsovkd@nmicrk.ru


References:

  1. Rosenberg I.H. Sarcopenia: origins and clinical relevance. The Journal of nutrition. 1997; 127(5): 990S–991S. https://doi.org/10.1093/jn/127.5.990S
  2. Roubenoff R. Origins and clinical relevance of sarcopenia. Canadian journal of applied physiology. 2001;26(1): 78–89. https://doi.org/10.1139/h01-006
  3. Kilgour R.D., Vigano A., Trutschnigg B., et al. Cancer-related fatigue: the impact of skeletal muscle mass and strength in patients with advanced cancer. J Cachexia Sarcopenia Muscle. 2010; 1(2): 177–185. https://doi.org/10.1007/s13539-010-0016-0
  4. Schefold J.C., Bierbrauer J., Weber-Carstens S. Intensive care unit - acquired weakness (ICUAW) and muscle wasting in critically ill patients with severe sepsis and septic shock J. Cachexia Sarcopenia Muscle. 2010; 1(2): 147–157. https://doi.org/10.1007/s13539-010-0010-6
  5. Martone A.M., Bianchi L., Abete P., et al. The incidence of sarcopenia among hospitalized elderly patients: the results of the study Glisten. J. Cachexia. Muscle sarcopenia. 2017; 8: 907–914. https://doi.org/10.1002/jcsm.12224
  6. Sato Y., Yoshimura Y., Abe T. Phase Angle as an Indicator of Baseline Nutritional Status and Sarcopenia in Acute Stroke. J Stroke Cerebrovasc Dis. 2022; 31(1): 106220. https://doi.org/10.1016/j.jstrokecerebrovasdis.2021.106220
  7. Nozoe M., Kubo H., Kanai M., et al. Reliability and validity of measuring temporal muscle thickness as the evaluation of sarcopenia risk and the relationship with functional outcome in older patients with acute stroke. Clinical Neurology and Neurosurgery. 2021; 201: 106444. https://doi.org/10.1016/j.clineuro.2020.106444
  8. Abe T., Yoshimua Y., Imai R., et al. A Combined Assessment Method of Phase Angle and Skeletal Muscle Index to Better Predict Functional Recovery after Acute Stroke. J Nutr Health Aging. 2022; 26(5): 445–451. https://doi.org/10.1007/s12603-022-1777-9
  9. Lee H., Lee I.H., Heo J., et al. Impact of Sarcopenia on Functional Outcomes Among Patients with Mild Acute Ischemic Stroke and Transient Ischemic Attack: A Retrospective Study. Front Neurol. 2022; 13: 841945. https://doi.org/10.3389/fneur.2022.841945
  10. Bellelli G., Zambon A., Volpato S., et al. The association between delirium and sarcopenia in older adult patients admitted to acute geriatrics units: Results from the GLISTEN multicenter observational study. Clin Nutr. 2018; 37(5): 1498–1504. https://doi.org/10.1016/j.clnu.2017.08.027
  11. Scherbakov N., Sandek A., Doehner W. Stroke-related sarcopenia: specific characteristics. J Am Med Dir Assoc. 2015; 16(4): 272–276. https://doi.org/10.1016/j.jamda.2014.12.007
  12. Scherbakov N., von Haehling S., Anker S.D., et al. Stroke induced Sarcopenia: muscle wasting and disability after stroke. Int J Cardiol. 2013; 170(2): 89–94. https://doi.org/10.1016/j.ijcard.2013.10.031
  13. Nishioka S., Yamanuchi A., Matsushita T., et al. Validity of the circumference of the tibia for assessing skeletal muscle mass in patients after stroke. Nutrition. 2021; 82: 111028. https://doi.org/10.1016/j.nut.2020.111028
  14. Patel H.P., Syddall H.E., Jameson K., et al. Prevalence of sarcopenia in community-dwelling older people in the UK using the European Working Group on Sarcopenia in Older People (EWGSOP) definition: findings from the Hertfordshire Cohort Study (HCS). Age and ageing. 2013; 42(3): 378–384. https://doi.org/10.1093/ageing/afs197
  15. Brown, J.C., Harhay, M.O., Harhay, M.N. Sarcopenia and mortality among a population-based sample of community-dwelling older adults. Journal of Cachexia, Sarcopenia and Muscle. 2016; 7(3): 290–298. https://doi.org/10.1002/jcsm.12073
  16. Fielding R., Vellas B., Evans W., et al. Sarcopenia: An Undiagnosed Condition in Older Adults. Current Consensus Definition: Prevalence, Etiology, and Consequences. International Working Group on Sarcopenia. J Am Med Dir Assoc. 2011; 12 (4): 249–256. https://doi.org/10.1016/j.jamda.2011.01.003
  17. Dam T., Peters K., Fragala M., et al. An Evidence-Based Comparison of Operational Criteria for the Presence of Sarcopenia. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences. 2014; 69 (5): 584–590. https://doi.org/10.1093/gerona/glu013
  18. Cruz-Jentoft A., Bahat G., Bauer J., et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019; 48 (1): 16–31. https://doi.org/10.1093/ageing/afy169
  19. Bhasin S., Travison T., Manini T., et al. Sarcopenia Definition: The Position Statements of the Sarcopenia Definition and Outcomes Consortium. J Am Geriatr Soc. 2020; 68(7): 1410–1418. https://doi.org/10.1111/jgs.16372
  20. Sergi G., De Rui M., Veronese N., et al. Assessing appendicular skeletal muscle mass with bioelectrical impedance analysis in free-living Caucasian older adults. Clinical Nutrition. 2015; 34 (4): 667–673. https://doi.org/10.1016/j.clnu.2014.07.010
  21. Mentiplay B.F., Perraton L.G., Bower K.J., et al. Assessment of Lower Limb Muscle Strength and Power Using Hand-Held and Fixed Dynamometry: A Reliability and Validity Study. PLoS One. 2015; 10(10): e0140822. https://doi.org/10.1371/journal.pone.0140822
  22. Steiber N. Strong or Weak Handgrip? Normative Reference Values for theGerman Population across the Life Course Stratified by Sex, Age, and BodyHeight. PLoS ONE. 2016; 11 (10): e0163917. https://doi.org/10.1371/journal.pone.0163917
  23. Leong D., Teo K., Rangarajan S., et al. Prognostic value of grip strength: findings from the Prospective Urban Rural Epidemiology (PURE) study. The Lancet. 2015; 386 (9990): 266–273. https://doi.org/10.1016/S0140-6736(14)62000-6
  24. Ibrahim K., May C., Patel H., et al. A feasibility study of implementing grip strength measurement into routine hospital practice (GRImP): study protocol. Pilot Feasibility Study. 2016; 2 (1): 27. https://doi.org/10.1186/s40814-016-0067-x
  25. Roberts H., Denison H., Martin H., et al. A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardized approach. AgeAgeing. 2011; 40 (4): 423–429. https://doi.org/10.1093/ageing/afr051
  26. Beaudart C., McCloskey E., Bruyère O., et al. Sarcopenia in daily practice: assessment and management. BMC Geriatr. 2016; 16(1): 170. https://doi.org/10.1186/s12877-016-0349-4
  27. Beaudart C., Rolland Y., Cruz-Jentoft A.J., et al. Assessment of Muscle Function and Physical Performance in Daily Clinical Practice: A position paper endorsed by the European Society for Clinical and Economic Aspects of Osteoporosis, Osteoarthritis and Musculoskeletal Diseases (ESCEO). Calcif Tissue Int. 2019; 105(1): 1–14. https://doi.org/10.1007/s00223-019-00545-w
  28. Osuka Y., Kim H., Kawai H., et al. Sarcoscore: A Novel Approach for Assessing Sarcopenia and Functional Disability in Older Adults. J Clin Med. 2020; 9(3):692. https://doi.org/10.3390/jcm9030692
  29. Beaudart C., Biver E., Reginster J.Y., et al. Validation of the SarQoL®, a specific health-related quality of life questionnaire for Sarcopenia. J Cachexia Sarcopenia Muscle. 2017; 8(2): 238–244. https://doi.org/10.1002/jcsm.12149
  30. Malmstrom T.K., Miller D.K., Simonsick E.M., et al. SARC-F: a symptom score to predict persons with sarcopenia at risk for poor functional outcomes. J Cachexia Sarcopenia Muscle. 2016; 7(1): 28–36. https://doi.org/10.1002/jcsm.12048
  31. Shiraishi A., Yoshimura Y., Wakabayashi H., et al. Prevalence of stroke-related sarcopenia and its association with poor oral status in post-acute stroke patients: Implications for oral sarcopenia. Clin Nutr. 2018; 37(1): 204–207. https://doi.org/10.1016/j.clnu.2016.12.002
  32. Piotrowicz K., Głuszewska A., Czesak J., et al. SARC-F as a case-finding tool for sarcopenia according to the EWGSOP2. National validation and comparison with other diagnostic standards. Aging Clin. Exp. Res. 2021; 33: 1821–1829. https://doi.org/10.1007/s40520-020-01782-y
  33. Inoue T., Maeda K., Shimizu A., et al. Calf circumference value for sarcopenia screening among older adults with stroke. Arch Gerontol Geriatr. 2021; 93: 104290. https://doi.org/10.1016/j.archger.2020.104290
  34. Yao R., Yao L., Yuan C., et al. Accuracy of Calf Circumference Measurement, SARC-F Questionnaire, and Ishii’s Score for Screening Stroke-Related Sarcopenia. Front Neurol. 2022; 13: 880907. https://doi.org/10.3389/fneur.2022.880907
  35. Hsieh C.L., Hsueh I.P., Mao H.F. Validity and responsiveness of the rivermead mobility index in stroke patients.Scand J Rehabil Med. 2000; 32(3): 140–142.
  36. Kasner S.E. Clinical interpretation and use of stroke scales. Lancet Neurol. 2006; 5(7): 603–612. https://doi.org/10.1016/S1474-4422(06)70495-1
  37. Gong G., Wan W., Zhang X., et al. Correlation between the Charlson comorbidity index and skeletal muscle mass/physical performance in hospitalized older people potentially suffering from sarcopenia. BMC Geriatr. 2019; 19(1): 367. https://doi.org/10.1186/s12877-019-1395-5
  38. O’Connell M.D., Roberts S.A., Srinivas-Shankar U., et al. Do the effects of testosterone on muscle strength, physical function, body composition, and quality of life persist six months after treatment in intermediate-frail and frail elderly men? J Clin Endocrinol Metab. 2011; 96(2): 454–458. https://doi.org/10.1210/jc.2010-1167
  39. Dubois V., Simitsidellis I., Laurent M.R., et al. Enobosarm (GTx-024) Modulates Adult Skeletal Muscle Mass Independently of the Androgen Receptor in the Satellite Cell Lineage. Endocrinology. 2015; 156(12): 4522–4533. https://doi.org/10.1210/en.2015-1479
  40. Morley J.E. Pharmacologic Options for the Treatment of Sarcopenia. Calcif Tissue Int. 2016; 98(4): 319–333. https://doi.org/10.1007/s00223-015-0022-5
  41. Blackman M.R., Sorkin J.D., Münzer T., et al. Growth hormone and sex steroid administration in healthy aged women and men: a randomized controlled trial. JAMA. 2002; 288(18): 2282–2292. https://doi.org/10.1001/jama.288.18.2282
  42. Liu H., Bravata D.M., Olkin I., et al. Systematic review: the safety and efficacy of growth hormone in the healthy elderly. Ann Intern Med. 2007; 146(2): 104–115. https://doi.org/10.7326/0003-4819-146-2-200701160-00005
  43. Adunsky A., Chandler J., Heyden N., et al. MK-0677 (ibutamoren mesylate) for the treatment of patients recovering from hip fracture: a multicenter, randomized, placebo-controlled phase IIb study. Arch Gerontol Geriatr. 2011; 53(2): 183–189. https://doi.org/10.1016/j.archger.2010.10.004
  44. Schellenbaum G.D., Smith N.L., Heckbert S.R., et al. Weight loss, muscle strength, and angiotensin-converting enzyme inhibitors in older adults with congestive heart failure or hypertension. J Am Geriatr Soc. 2005; 53(11): 1996–2000. https://doi.org/10.1111/j.1532-5415.2005.53568.x
  45. Peters R., Beckett N., Burch L., et al. The effect of treatment based on a diuretic (indapamide) +/- ACE inhibitor (perindopril) on fractures in the Hypertension in the Very Elderly Trial (HYVET). Age Ageing. 2010; 39(5): 609–616. https://doi.org/10.1093/ageing/afq071
  46. Writing Group; Edaravone (MCI-186) ALS 19 Study Group. Safety and efficacy of edaravone in well defined patients with amyotrophic lateral sclerosis: a randomised, double-blind, placebo-controlled trial. Lancet Neurol. 2017; 16(7): 505–512. https://doi.org/10.1016/S1474-4422(17)30115-1
  47. Gaskin F.S., Farr S.A., Banks W.A., et al. Ghrelin-induced feeding is dependent on nitric oxide. Peptides. 2003; 24(6): 913–918. https://doi.org/10.1016/s0196-9781(03)00160-8
  48. Uwamahoro R., Sundaraj K., Subramaniam I.D. Assessment of muscle activity using electrical stimulation and mechanomyography: a systematic review. Biomed Eng Online. 2021; 20(1): 1. https://doi.org/10.1186/s12938-020-00840-w
  49. Phu S., Boersma D., Duque G. Exercise and Sarcopenia. J Clin Densitom. 2015; 18(4): 488–492. https://doi.org/10.1016/j.jocd.2015.04.011
  50. Nascimento C.M., Ingles M., Salvador-Pascual A., et al. Sarcopenia, frailty and their prevention by exercise. Free Radic Biol Med. 2019; 132: 42–49. https://doi.org/10.1016/j.freeradbiomed.2018.08.035
  51. Carda S., Cisari C., Invernizzi M. Sarcopenia or muscle modifications in neurologic diseases: a lexical or patophysiological difference? Eur J Phys Rehabil Med. 2013; 49(1): 119–130.
  52. Hunnicutt J.L., Gregory C.M. Skeletal muscle changes following stroke: a systematic review and comparison to healthy individuals. Top Stroke Rehabil. 2017; 24(6): 463–471. https://doi.org/10.1080/10749357.2017.1292720
  53. Huang J., Ji J.R., Liang C., et al. Effects of physical therapy-based rehabilitation on recovery of upper limb motor function after stroke in adults: a systematic review and meta-analysis of randomized controlled trials. Ann Palliat Med. 2022; 11(2): 521–531. https://doi.org/10.21037/apm-21-3710
  54. Pires Peixoto R., Trombert V., Poncet A., et al. Feasibility and safety of high-intensity interval training for the rehabilitation of geriatric inpatients (HIITERGY) a pilot randomized study. BMC Geriatr. 2020; 20(1): 197. https://doi.org/10.1186/s12877-020-01596-7
  55. Gomes-Neto M., Durães A.R., Reis H.F.C.D., et al. High-intensity interval training versus moderate-intensity continuous training on exercise capacity and quality of life in patients with coronary artery disease: A systematic review and meta-analysis. Eur J Prev Cardiol. 2017; 24(16): 1696–1707. https://doi.org/10.1177/2047487317728370
  56. Porter M.M. The effects of strength training on sarcopenia. Can J Appl Physiol. 2001; 26(1): 123–141. https://doi.org/10.1139/h01-009
  57. American College of Sports Medicine Position Stand. The recommended quantity and quality of exercise for developing and maintaining cardiorespiratory and muscular fitness, and flexibility in healthy adults. Medicine and Science in Sports and Exercise. 1998; 30(6): 975–991. https://doi.org/10.1097/00005768-199806000-00032
  58. Lu L., Mao L., Feng Y., et al. Effects of different exercise training modes on muscle strength and physical performance in older people with sarcopenia: a systematic review and meta-analysis. BMC Geriatr. 2021; 21(1): 708. https://doi.org/10.1186/s12877-021-02642-8
  59. Barbat-Artigas S., Garnier S., Joffroy S., et al. Caloric restriction and aerobic exercise in sarcopenic and non-sarcopenic obese women: an observational and retrospective study. J Cachexia Sarcopenia Muscle. 2016; 7(3): 284–289. https://doi.org/10.1002/jcsm.12075
  60. Кузнецов К.Д., Марченкова Л.А., Стяжкина Е.М. и др. Способ медицинской реабилитации пациентов с саркопенией на фоне последствий острого нарушения мозгового кровообращения. Патент RU 2024113417, 17.05.2024. [Kuznecov K.D., Marchenkova L.A., Styazhkina E.M. et al. Sposob medicinskoj reabilitacii pacientov s sarkopeniej na fone posledstvij ostrogo narusheniya mozgovogo krovoobrashcheniya. Patent RU 2024113417, 17.05.2024. (In Russ.).]
  61. Kokura Y., Wakabayashi H., Nishioka S., et al. Nutritional intake is associated with activities of daily living and complications in older inpatients with stroke. Geriatr Gerontol Int. 2018; 18(9): 1334–1339. https://doi.org/10.1111/ggi.13467
  62. Sions J.M., Tyrell C.M., Knarr B.A., et al. Age- and stroke-related skeletal muscle changes: a review for the geriatric clinician. J Geriatr Phys Ther. 2012; 35(3): 155–161. https://doi.org/10.1519/JPT.0b013e318236db92
  63. Scherbakov N., Knops M., Ebner N., et al. Evaluation of C-terminal Agrin Fragment as a marker of muscle wasting in patients after acute stroke during early rehabilitation. J Cachexia Sarcopenia Muscle. 2016; 7(1): 60–67. https://doi.org/10.1002/jcsm.12068
  64. Dennis M.S., Lewis S.C., Warlow C. FOOD Trial Collaboration. Routine oral nutritional supplementation for stroke patients in hospital (FOOD): a multicentre randomised controlled trial. Lancet. 2005; 365(9461): 755–763. https://doi.org/10.1016/S0140-6736(05)17982-3
  65. Somanchi M., Tao X., Mullin G.E. The facilitated early enteral and dietary management effectiveness trial in hospitalized patients with malnutrition. JPEN J Parenter Enteral Nutr. 2011; 35(2): 209–216. https://doi.org/10.1177/0148607110392234
  66. Verhoeven S., Vanschoonbeek K., Verdijk L.B., et al. Long-term leucine supplementation does not increase muscle mass or strength in healthy elderly men. Am J Clin Nutr. 2009; 89(5): 1468–1475. https://doi.org/10.3945/ajcn.2008.26668
  67. Jiang X., Pu H., Hu X., et al. A Post-stroke Therapeutic Regimen with Omega-3 Polyunsaturated Fatty Acids that Promotes White Matter Integrity and Beneficial Microglial Responses after Cerebral Ischemia. Transl Stroke Res. 2016; 7(6): 548–561. https://doi.org/10.1007/s12975-016-0502-6
  68. Zhao W., Tang H., Yang X., et al. Fish Consumption and Stroke Risk: A Meta-Analysis of Prospective Cohort Studies. J Stroke Cerebrovasc Dis. 2019; 28(3): 604–611. https://doi.org/10.1016/j.jstrokecerebrovasdis.2018.10.036
  69. Chen Y., Liang Y., Guo H., et al. Muscle-Related Effect of Whey Protein and Vitamin D3 Supplementation Provided before or after Bedtime in Males Undergoing Resistance Training. Nutrients. 2022; 14(11): 2289. https://doi.org/10.3390/nu14112289
  70. Garbagnati F., Cairella G., De Martino A., et al. Is antioxidant and n-3 supplementation able to improve functional status in poststroke patients? Results from the Nutristroke Trial. Cerebrovasc Dis. 2009; 27(4): 375–383. https://doi.org/10.1159/000207441
  71. Ferrara-Romeo I., Martinez P., Saraswati S., et al. The mTOR pathway is necessary for survival of mice with short telomeres. Nat Commun. 2020; 11(1): 1168. https://doi.org/10.1038/s41467-020-14962-1



Creative Commons License
The content is available under the Creative Commons Attribution 4.0 License.

©


This is an open article under the CC BY 4.0 license. Published by the National Medical Research Center for Rehabilitation and Balneology.