Skip to main content
SpringerLink
Log in

Muscular Echo-Intensity of the Quadriceps by Ultrasound Is More Related to Improvement of Gait Independence than Muscle Thickness in Older Inpatients

  • Original Research
  • Published:
The journal of nutrition, health & aging

Abstract

Objectives

This study aimed to examine whether the decrease in muscular echo-intensity of the quadriceps by ultrasound in older inpatients is related to the improvement of gait independence than the increase of muscle thickness.

Design

Longitudinal study

Setting

Hospital-based study

Participants

This study included 171 inpatients aged ≥ 65 years (median age: 84.0 [77.0–88.0], 56.1% female). Patients who were able to walk independently at hospital admission were excluded from the study.

Measurements

Improvement of gait independence during hospital stay was assessed using the change in Functional Independence Measure (FIM) gait score (i.e., FIM gait score at hospital discharge minus FIM gait score at hospital admission) and FIM gait score at hospital discharge. Muscular echo-intensity and muscle thickness of the quadriceps were assessed at hospital admission and discharge using ultrasound images, respectively. Muscular echo-intensity has been shown to be mainly related to intramuscular adipose tissue. Multiple linear regression analysis was performed to identify the factors independently associated with the change in FIM gait score and FIM gait score at discharge.

Results

Change in quadriceps echo-intensity was independently and significantly associated with the change in FIM gait score (β = −0.22, p = 0.017) and FIM gait score at hospital discharge (β = −0.21, p = 0.017). In contrast, change in quadriceps thickness was not independently and significantly associated with the change in FIM gait score (β = 0.16, p = 0.050) and FIM gait score at hospital discharge (β = 0.15, p = 0.050).

Conclusions

Our study indicates that a decrease in muscular echo-intensity of the quadriceps by ultrasound is more related to the improvement of gait independence than an increase of muscle thickness in older inpatients. Intervention for intramuscular adipose tissue of the quadriceps may be important for improving gait independence in older inpatients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ADL:

activities of daily living

FIM:

Functional Independence Measure

References

  1. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2), and the Extended Group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019; 48: 16–31. doi: https://doi.org/10.1093/ageing/afz046.

    Article  PubMed  Google Scholar 

  2. Akazawa N, Kishi M, Hino T, Tsuji R, Tamura K, Hioka A, et al. Relationship between aging and intramuscular adipose tissue in older inpatients. J Am Med Dir Assoc. 2021; 22: 1287–1291. doi: https://doi.org/10.1016/j.jamda.2020.09.017.

    Article  PubMed  Google Scholar 

  3. Bhasin S, Travison TG, Manini TM, Patel S, Pencina KM, Fielding RA, et al. Sarcopenia definition: The position statements of the Sarcopenia Definition and Outcomes Consortium. J Am Geriatr Soc. 2020; 68: 1410–1418. doi: https://doi.org/10.1111/jgs.16372.

    Article  PubMed  Google Scholar 

  4. Young HJ, Jenkins NT, Zhao Q, Mccully KK. Measurement of intramuscular fat by muscle echo intensity. Muscle Nerve. 2015; 52: 963–971. doi: https://doi.org/10.1002/mus.24656.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Akima H, Hioki M, Yoshiko A, Koike T, Sakakibara H, Takahashi H, et al. Intramuscular adipose tissue determined by T1-weighted MRI at 3T primarily reflects extramyocellular lipids. Magn Reson Imaging. 2016; 34: 397–403. doi: https://doi.org/10.1016/j.mri.2015.12.038.

    Article  CAS  PubMed  Google Scholar 

  6. Fukumoto Y, Taniguchi M, Hirono T, Yagi M, Yamagata M, Nakai R, et al. Influence of ultrasound focus depth on the association between echo intensity and intramuscular adipose tissue. Muscle Nerve. 2022; 66: 568–575. doi: https://doi.org/10.1002/mus.27677.

    Article  PubMed  Google Scholar 

  7. Wilhelm EN, Rech A, Minozzo F, Radaelli R, Botton CE, Pinto RS. Relationship between quadriceps femoris echo intensity, muscle power, and functional capacity of older men. Age. 2014; 36: 9625. doi: https://doi.org/10.1007/s11357-014-9625-4.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Akazawa N, Okawa N, Tamura K, Moriyama H. Relationships between intramuscular fat, muscle strength, and gait independence in older women: a cross-sectional study. Geriatr Gerontol Int. 2017; 17: 1683–1688. doi: https://doi.org/10.1111/ggi.12869.

    Article  PubMed  Google Scholar 

  9. Mayer KP, Thompson Bastin ML, Montgomery-Yates AA, Pastva AM, Dupont-Versteegden EE, Parry SM, et al. Acute skeletal muscle wasting and dysfunction predict physical disability at hospital discharge in patients with critical illness. Crit Care. 2020; 24: 637. doi: https://doi.org/10.1186/s13054-020-03355-x.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Osawa Y, Arai Y, Oguma Y, Hirata T, Abe Y, Azuma K, et al. Relationships of muscle echo intensity with walking ability and physical activity in the very old population. J Aging Phys Act. 2017; 25: 189–195. doi: https://doi.org/10.1123/japa.2015-0203.

    Article  PubMed  Google Scholar 

  11. Akazawa N, Okawa N, Kishi M, Hino T, Tsuji R, Tamura K, et al. Quantitative features of intramuscular adipose tissue of the quadriceps and their association with gait independence in older inpatients: A cross-sectional study. Nutrition. 2020; 71: 110600. doi: https://doi.org/10.1016/j.nut.2019.110600.

    Article  PubMed  Google Scholar 

  12. Akazawa N, Kishi M, Hino T, Tsuji R, Tamura K, Hioka A, et al. Intramuscular adipose tissue in the quadriceps is more strongly related to recovery of activities of daily living than muscle mass in older inpatients. J Cachexia Sarcopenia Muscle. 2021; 12: 891–899. doi: https://doi.org/10.1002/jcsm.12713.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Akazawa N, Kishi M, Hino T, Tsuji R, Tamura K, Hioka A, et al., Longitudinal relationship between intramuscular adipose tissue of the quadriceps and activities of daily living in older inpatients. J Cachexia Sarcopenia Muscle. 2021; 12: 2231–2237. doi: https://doi.org/10.1002/jcsm.12842.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Akazawa N, Kishi M, Hino T, Tsuji R, Tamura K, Hioka A et al., Intramuscular adipose tissue of the quadriceps is more strongly related to recovery of swallowing ability than muscle mass in older inpatients: A prospective study. Nutrition. 2021; 91–92: 111364. doi: https://doi.org/10.1016/j.nut.2021.111364.

    Article  PubMed  Google Scholar 

  15. Akazawa N, Okawa N, Hino T, Tsuji R, Tamura K, Moriyama H. Higher malnutrition risk is related to increased intramuscular adipose tissue of the quadriceps in older inpatients: A cross-sectional study. Clin Nutr. 2020; 39: 2586–2592. doi: https://doi.org/10.1016/j.clnu.2019.11.028.

    Article  PubMed  Google Scholar 

  16. Akazawa N, Kishi M, Hino T, Tsuji R, Tamura K, Hioka A, et al. Higher malnutrition risk in older inpatients who are referred to the department of rehabilitation is related to increase of intramuscular adipose tissue: A prospective study. Clin Nutr. 2022; 41: 2087–2093. doi: https://doi.org/10.1016/j.clnu.2022.08.010.

    Article  PubMed  Google Scholar 

  17. Maranesi E, Riccardi GR, Di Donna V, Di Rosa M, Fabbietti P, Luzi R, et al. Effectiveness of Intervention Based on End-effector Gait Trainer in Older Patients With Stroke: A Systematic Review. J Am Med Dir Assoc. 2020; 21: 1036–1044. doi: https://doi.org/10.1016/j.jamda.2019.10.010.

    Article  PubMed  Google Scholar 

  18. van Ooijen MW, Roerdink M, Trekop M, Janssen TW, Beek PJ. The efficacy of treadmill training with and without projected visual context for improving walking ability and reducing fall incidence and fear of falling in older adults with fall-related hip fracture: a randomized controlled trial. BMC Geriatr. 2016; 16: 215. doi: https://doi.org/10.1186/s12877-016-0388-x.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Ottenbacher KJ, Hsu Y, Granger CV, Fiedler RC. The reliability of the functional independence measure: a quantitative review. Arch Phys Med Rehabil. 1996; 77: 1226–1232. doi: https://doi.org/10.1016/s0003-9993(96)90184-7.

    Article  CAS  PubMed  Google Scholar 

  20. Akazawa N, Harada K, Okawa N, Tamura K, Hayase A, Moriyama H. Relationships between muscle mass, intramuscular adipose and fibrous tissues of the quadriceps, and gait independence in chronic stroke survivors: a cross-sectional study. Physiotherapy. 2018; 104: 438–445. doi: https://doi.org/10.1016/j.physio.2017.08.009.

    Article  PubMed  Google Scholar 

  21. Kunieda K, Ohno T, Fujishima I, Hojo K, Morita T. Reliability and validity of a tool to measure the severity of dysphagia: the Food Intake LEVEL Scale. J Pain Symptom Manage. 2013; 46: 201–206. doi: https://doi.org/10.1016/j.jpainsymman.2012.07.020.

    Article  PubMed  Google Scholar 

  22. Bouillanne O, Morineau G, Dupont C, Coulombel I, Vincent JP, Nicolis I, et al. Geriatric Nutritional Risk Index: a new index for evaluating at-risk elderly medical patients. Am J Clin Nutr. 2005; 82: 777–783. doi: https://doi.org/10.1093/ajcn/82.4.777.

    Article  CAS  PubMed  Google Scholar 

  23. Quan H, Li B, Couris CM, Fushimi K, Graham P, Hider P, et al. Updating and validating the Charlson comorbidity index and score for risk adjustment in hospital discharge abstracts using data from 6 countries. Am J Epidemiol. 2011; 173: 676–682. doi: https://doi.org/10.1093/aje/kwq433.

    Article  PubMed  Google Scholar 

  24. Ryan ED, Shea NW, Gerstner GR, Barnette TJ, Tweedell AJ, Kleinberg CR, et al. The influence of subcutaneous fat on the relationship between body composition and ultrasound-derived muscle quality. Appl Physiol Nutr Metab. 2016; 27: 1–4. doi: https://doi.org/10.1139/apnm-2016-0238.

    Google Scholar 

  25. Selya AS, Rose JS, Dierker LC, Hedeker D, Mermelstein RJ. A practical guide to calculating Cohen’s f(2), a measure of local effect size, from PROC MIXED. Front Psychol. 2012; 3: 111. doi: https://doi.org/10.3389/fpsyg.2012.00111.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Hamaguchi Y, Kaido T, Okumura S, Ito T, Fujimoto Y, Ogawa K, et al. Preoperative intramuscular adipose tissue content is a novel prognostic predictor after hepatectomy for hepatocellular carcinoma. J Hepatobiliary Pancreat Sci. 2015; 22: 475–485. doi: https://doi.org/10.1002/jhbp.236.

    Article  PubMed  Google Scholar 

  27. Fukumoto Y, Ikezoe T, Yamada Y, Tsukagoshi R, Nakamura M, Takagi Y, et al. Age-related ultrasound changes in muscle quantity and quality in women. Ultrasound Med Biol. 2015; 41: 3013–3017. doi: https://doi.org/10.1016/j.ultrasmedbio.2015.06.017.

    Article  PubMed  Google Scholar 

  28. Conte M, Vasuri F, Trisolino G, Bellavista E, Santoro A, Degiovanni A, et al. Increased Plin2 expression in human skeletal muscle is associated with sarcopenia and muscle weakness. PLoS One. 2013; 8: e73709. doi: https://doi.org/10.1371/journal.pone.0073709.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Conte M, Vasuri F, Bertaggia E, Armani A, Santoro A, Bellavista E, Degiovanni A, D’Enico-Grigioni A, Trisolino G, Capri M, Franchi MV, Narici MV, Sandri M, Franceschi C, Salvioli S. Differential expression of perilipin 2 and 5 in human skeletal muscle during aging and their association with atrophy-related genes. Biogerontology. 2015; 16: 329–40. doi: https://doi.org/10.1007/s10522-014-9549-5.

    Article  CAS  PubMed  Google Scholar 

  30. Wang X, Huang G, Mei S, Qian J, Ji J, Zhang J. Over-expression of C/EBP-alpha induces apoptosis in cultured rat hepatic stellate cells depending on p53 and peroxisome proliferator-activated receptor-gamma. Biochem Biophys Res Commun. 2009; 380: 286–291. doi: https://doi.org/10.1016/j.bbrc.2009.01.060.

    Article  CAS  PubMed  Google Scholar 

  31. Hussain MA, Schmitz O, Mengel A, Keller A, Christiansen JS, Zapf J, et al. Insulinlike growth factor I stimulates lipid oxidation, reduces protein oxidation, and enhances insulin sensitivity in humans. J Clin Invest. 1993; 92: 2249–2256. doi: https://doi.org/10.1172/JCI116828.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Reimers K, Reimers CD, Wagner S, Paetzke I, Pongratz DE. Skeletal muscle sonography: a correlative study of echogenicity and morphology. J Ultrasound Med. 1993; 12: 73–77. doi: https://doi.org/10.7863/jum.1993.12.2.73.

    Article  CAS  PubMed  Google Scholar 

  33. Englund DA, Kirn DR, Koochek A, Zhu H, Travison TG, Reid KF, et al. Nutritional supplementation with physical activity improves muscle composition in mobility-limited older adults, The VIVE2 Study: A randomized, double-blind, placebo-controlled trial. J Gerontol A Biol Sci Med Sci. 2017; 73: 95–101. doi: https://doi.org/10.1093/gerona/glx141.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Silva PE, de Cássia Marqueti R, Iivino-de-Carvalho K, de Araujo AET, Castro J, da Silva VM, et al., Neuromuscular electrical stimulation in critically ill traumatic brain injury patients attenuates muscle atrophy, neurophysiological disorders, and weakness: a randomized controlled trial. J Intensive Care. 2019; 12; 7: 59. doi: https://doi.org/10.1186/s40560-019-0417-x.

    Article  Google Scholar 

  35. Yamada M, Kimura Y, Ishiyama D, Nishio N, Abe Y, Kakehi T, et al., Differential Characteristics of Skeletal Muscle in Community-Dwelling Older Adults. J Am Med Dir Assoc. 2017; 18: 807.e9–807.e16. doi: https://doi.org/10.1016/j.jamda.2017.05.011.

    Article  PubMed  Google Scholar 

  36. Mirón Mombiela R, Facal de Castro F, Moreno P, Borras C. Ultrasonic Echo Intensity as a New Noninvasive In Vivo Biomarker of Frailty. J Am Geriatr Soc. 2017; 65: 2685–2690. doi: https://doi.org/10.1111/jgs.15002.

    Article  PubMed  Google Scholar 

  37. Donoghue OA, Savva GM, Cronin H, Kenny RA, Horgan NF. Using timed up and go and usual gait speed to predict incident disability in daily activities among community-dwelling adults aged 65 and older. Arch Phys Med Rehabil. 2014; 95: 1954–1961. doi: https://doi.org/10.1016/j.apmr.2014.06.008.

    Article  PubMed  Google Scholar 

  38. Wang DXM, Yao J, Zirek Y, Reijnierse EM, Maier AB. Muscle mass, strength, and physical performance predicting activities of daily living: a meta-analysis. J Cachexia Sarcopenia Muscle. 2020; 11: 3–25. doi: https://doi.org/10.1002/jcsm.12502.

    Article  CAS  PubMed  Google Scholar 

  39. Kara M, Kaymak B, Frontera W, Ata AM, Ricci V, Ekiz T, et al. Diagnosing sarcopenia: Functional perspectives and a new algorithm from the ISarcoPRM. J Rehabil Med. 2021; 53: jrm00209. doi: https://doi.org/10.2340/16501977-2851.

    Article  Google Scholar 

  40. Ikezoe T, Mori N, Nakamura M, Ichihashi N. Atrophy of the lower limbs in elderly women: is it related to walking ability? Eur J Appl Physiol. 2011; 111: 989–995. doi: https://doi.org/10.1007/s00421-010-1728-8.

    Article  PubMed  Google Scholar 

  41. Abe T, Sakamaki M, Yasuda T, Bemben MG, Kondo M, Kawakami Y, et al. Age-related, site-specific muscle loss in 1507 Japanese men and women aged 20 to 95 years. J Sports Sci Med. 2011; 10: 145–150.

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank the participants and staff members who helped with this study.

Funding

This work was supported by JSPS KAKENHI Grant Number JP17K18294 and JP20K19661.

Author information

Authors and Affiliations

  1. Department of Physical Therapy, Faculty of Health and Welfare, Tokushima Bunri University, Hoji 180, Nishihama, Yamashiro-cho, Tokushima-city, Tokushima, 770-8514, Japan

    Naoki Akazawa & A. Hioka

  2. Department of Rehabilitation, Kasei Tamura Hospital, Wakayama, Wakayama, Japan

    M. Kishi, T. Hino, R. Tsuji & K. Tamura

  3. Life and Medical Sciences Area, Health Sciences Discipline, Kobe University, Kobe, Hyogo, Japan

    H. Moriyama

Authors
  1. Naoki Akazawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Kishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. Hino
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. Tsuji
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. K. Tamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. Hioka
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. H. Moriyama
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Naoki Akazawa.

Ethics declarations

All participants or their guardians provided informed consent prior to the study, and the study was approved by the ethics committee of Tokushima Bunri University.

Additional information

Statement of Authorship

(1) The conception and design of the study, or acquisition of data, or analysis and interpretation of data; NA, MK, TH, RT, KT, AH, and HM. (2) Drafting the article; NA, MK, TH, RT, KT, AH, and HM. (3) Final approval of the version to be submitted; NA, MK, TH, RT, KT, AH, and HM.

Disclosure of interest

The authors declare that there is no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akazawa, N., Kishi, M., Hino, T. et al. Muscular Echo-Intensity of the Quadriceps by Ultrasound Is More Related to Improvement of Gait Independence than Muscle Thickness in Older Inpatients. J Nutr Health Aging 27, 103–110 (2023). https://doi.org/10.1007/s12603-023-1880-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12603-023-1880-6

Key words

Search

Navigation