Skip to main content
SpringerLink
Log in

Percutaneous biopsies of skeletal muscle and adipose tissue in individuals older than 70: methods and outcomes in the Study of Muscle, Mobility and Aging (SOMMA)

  • ORIGINAL ARTICLE
  • Published:
GeroScience Aims and scope Submit manuscript

Abstract

Biopsies of muscle and adipose tissue (AT) are useful tools to gain insights into the aging processes in these tissues. However, they are invasive procedures and their risk/benefit profile in older adults can be altered by sarcopenia, frailty, poor healing, and multimorbidity. Their success rates, safety, and tolerability in a geriatric population have not been reported in detail. Investigators in the Study of Muscle, Mobility, and Aging (SOMMA) performed biopsies of muscle and AT in older adults and prospectively collected data on biopsy success rates, safety, and tolerability. We report here the methods and outcomes of these two procedures. In total, 861 participants (aged 70–94) underwent percutaneous biopsies of the Vastus lateralis muscle with a Bergstrom needle. A subset (n = 241) also underwent percutaneous biopsies of the abdominal subcutaneous AT with the tumescent liposuction technique. Success rate was assessed by the percentage of biopsies yielding adequate specimens for analyses; tolerability by pain scores; and safety by frequency of adverse events. All data were prospectively collected. The overall muscle biopsy success rate was 97.1% and was modestly lower in women. The AT biopsy success rate was 95.9% and slightly lower in men. Minimal or no pain was reported in 68% of muscle biopsies and in 83% of AT biopsies. Adverse events occurred in 2.67% of muscle biopsies and 4.15% of AT biopsies. None was serious. In older adults, percutaneous muscle biopsies and abdominal subcutaneous AT biopsies have an excellent safety profile, often achieve adequate tissue yields for analyses, and are well tolerated.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

This manuscript analysis dataset is available on request at https://sommaonline.ucsf.edu/.

References

  1. Ahmed SK, Egginton S, Jakeman PM, Mannion AF, Ross HF. Is human skeletal muscle capillary supply modelled according to fibre size or fibre type? Exp Physiol. 1997;82(1):231–4. https://doi.org/10.1113/expphysiol.1997.sp004012.

    Article  CAS  PubMed  Google Scholar 

  2. Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ, Roubenoff R. Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol (1985). 2000;88(4):1321–6. https://doi.org/10.1152/jappl.2000.88.4.1321.

  3. Larsson L, Sjodin B, Karlsson J. Histochemical and biochemical changes in human skeletal muscle with age in sedentary males, age 22–65 years. Acta Physiol Scand. 1978;103(1):31–9. https://doi.org/10.1111/j.1748-1716.1978.tb06187.x.

    Article  CAS  PubMed  Google Scholar 

  4. Nilwik R, Snijders T, Leenders M, Groen BB, van Kranenburg J, Verdijk LB, van Loon LJ. The decline in skeletal muscle mass with aging is mainly attributed to a reduction in type II muscle fiber size. Exp Gerontol. 2013;48(5):492–8. https://doi.org/10.1016/j.exger.2013.02.012.

    Article  PubMed  Google Scholar 

  5. De Carvalho FG, Justice JN, Freitas EC, Kershaw EE, Sparks LM. Adipose tissue quality in aging: how structural and functional aspects of adipose tissue impact skeletal muscle quality. Nutrients. 2019;11(11). https://doi.org/10.3390/nu11112553.

  6. Wang L, Wang B, Gasek NS, Zhou Y, Cohn RL, Martin DE, et al. Targeting p21(Cip1) highly expressing cells in adipose tissue alleviates insulin resistance in obesity. Cell Metab. 2022;34(1):75-89 e8. https://doi.org/10.1016/j.cmet.2021.11.002.

    Article  CAS  PubMed  Google Scholar 

  7. Palmer AK, Xu M, Zhu Y, Pirtskhalava T, Weivoda MM, Hachfeld CM, et al. Targeting senescent cells alleviates obesity-induced metabolic dysfunction. Aging Cell. 2019;18(3):e12950. https://doi.org/10.1111/acel.12950.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Justice JN, Gregory H, Tchkonia T, LeBrasseur NK, Kirkland JL, Kritchevsky SB, Nicklas BJ. Cellular senescence biomarker p16INK4a+ cell burden in thigh adipose is associated with poor physical function in older women. J Gerontol A Biol Sci Med Sci. 2018;73(7):939–45. https://doi.org/10.1093/gerona/glx134.

    Article  CAS  PubMed  Google Scholar 

  9. Wilson D, Breen L, Lord JM, Sapey E. The challenges of muscle biopsy in a community based geriatric population. BMC Res Notes. 2018;11(1):830. https://doi.org/10.1186/s13104-018-3947-8.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Makary MA, Segev DL, Pronovost PJ, Syin D, Bandeen-Roche K, Patel P, et al. Frailty as a predictor of surgical outcomes in older patients. J Am Coll Surg. 2010;210(6):901–8. https://doi.org/10.1016/j.jamcollsurg.2010.01.028.

    Article  PubMed  Google Scholar 

  11. Joseph B, Pandit V, Zangbar B, Kulvatunyou N, Hashmi A, Green DJ, et al. Superiority of frailty over age in predicting outcomes among geriatric trauma patients: a prospective analysis. JAMA Surg. 2014;149(8):766–72. https://doi.org/10.1001/jamasurg.2014.296.

    Article  PubMed  Google Scholar 

  12. Saxton A, Velanovich V. Preoperative frailty and quality of life as predictors of postoperative complications. Ann Surg. 2011;253(6):1223–9. https://doi.org/10.1097/SLA.0b013e318214bce7.

    Article  PubMed  Google Scholar 

  13. Robinson TN, Wu DS, Pointer L, Dunn CL, Cleveland JC Jr, Moss M. Simple frailty score predicts postoperative complications across surgical specialties. Am J Surg. 2013;206(4):544–50. https://doi.org/10.1016/j.amjsurg.2013.03.012.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Barthelemy F, Woods JD, Nieves-Rodriguez S, Douine ED, Wang R, Wanagat J, et al. A well-tolerated core needle muscle biopsy process suitable for children and adults. Muscle Nerve. 2020;62(6):688–98. https://doi.org/10.1002/mus.27041.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Tarnopolsky MA, Pearce E, Smith K, Lach B. Suction-modified Bergstrom muscle biopsy technique: experience with 13,500 procedures. Muscle Nerve. 2011;43(5):717–25. https://doi.org/10.1002/mus.21945.

    Article  PubMed  Google Scholar 

  16. Derry KL, Nicolle MN, Keith-Rokosh JA, Hammond RR. Percutaneous muscle biopsies: review of 900 consecutive cases at London Health Sciences Centre. Can J Neurol Sci. 2009;36(2):201–6. https://doi.org/10.1017/s0317167100006569.

    Article  PubMed  Google Scholar 

  17. St Sauver JL, Boyd CM, Grossardt BR, Bobo WV, Finney Rutten LJ, Roger VL, et al. Risk of developing multimorbidity across all ages in an historical cohort study: differences by sex and ethnicity. BMJ Open. 2015;5(2):e006413. https://doi.org/10.1136/bmjopen-2014-006413.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Mau T, Barnes HN, Blackwell TL, Kramer PA, Bauer SR, Marcinek DJ, et al. Lower muscle mitochondrial energetics is associated with greater phenotypic frailty in older women and men: the Study of Muscle. Mobility Aging Gerosci. 2023. https://doi.org/10.1007/s11357-023-01002-1.

    Article  Google Scholar 

  19. Irwin M, Artin KH, Oxman MN. Screening for depression in the older adult: criterion validity of the 10-item Center for Epidemiological Studies Depression Scale (CES-D). Arch Intern Med. 1999;159(15):1701–4. https://doi.org/10.1001/archinte.159.15.1701.

    Article  CAS  PubMed  Google Scholar 

  20. Klein JA. Anesthesia for liposuction in dermatologic surgery. J Dermatol Surg Oncol. 1988;14(10):1124–32. https://doi.org/10.1111/j.1524-4725.1988.tb03469.x.

    Article  CAS  PubMed  Google Scholar 

  21. Klein JA. The tumescent technique. Anesthesia and modified liposuction technique. Dermatol Clin. 1990;8(3):425–37.

    Article  CAS  PubMed  Google Scholar 

  22. Boeni R. Safety of tumescent liposuction under local anesthesia in a series of 4,380 patients. Dermatology. 2011;222(3):278–81. https://doi.org/10.1159/000327375.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank all the SOMMA participants who enabled this research. We also thank Jessa Monte, Alyssa Mathews, Erica Kuo, Zana M. Ross, Cody Wolf, and Steve Anthony for their contributions to this research project.

Funding

The Study of Muscle, Mobility, and Aging is supported by funding from the National Institute on Aging, grant number AG059416. Adipose tissue biopsies were supported by grant R01AG066474. Study infrastructure support was funded in part by NIA Claude D. Pepper Older American Independence Centers at University of Pittsburgh (P30AG024827) and Wake Forest University (P30AG021332) and the Clinical and Translational Science Institutes, funded by the National Center for Advancing Translational Science, at Wake Forest University (UL10TR001420).

Author information

Authors and Affiliations

  1. Internal Medicine Section On Gerontology and Geriatrics, Wake Forest School of Medicine, Winston-Salem, NC, USA

    Zeke Zamora, Jamie Justice, Mary Lyles & Stephen Kritchevsky

  2. Sticht Center for Healthy Aging and Alzheimer’s Prevention, Wake Forest School of Medicine, Winston-Salem, NC, USA

    Zeke Zamora, Jamie Justice, Mary Lyles, Landon Gentle, Heather Gregory & Stephen Kritchevsky

  3. Research Institute, California Pacific Medical Center, San Francisco, CA, USA

    Li-Yung Lui

  4. Translational Research Institute, AdventHealth, Orlando, FL, USA

    Lauren M. Sparks & Reichelle X. Yeo

  5. Division of Endocrinology and Metabolism, Dept. of Medicine, School of Medicine, University of Pittsburgh, 200 Lothrop Street BST-W1055, Pittsburgh, PA, 15261, USA

    Erin E. Kershaw, Maja Stefanovic-Racic & Frederico G. S. Toledo

  6. Dept. of Epidemiology, School of Public Health, University of Pittsburgh, Pittsburgh, PA, USA

    Anne B. Newman

Authors
  1. Zeke Zamora
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Li-Yung Lui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lauren M. Sparks
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jamie Justice
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mary Lyles
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Landon Gentle
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Heather Gregory
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Reichelle X. Yeo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Erin E. Kershaw
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Maja Stefanovic-Racic
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Anne B. Newman
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Stephen Kritchevsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Frederico G. S. Toledo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frederico G. S. Toledo.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zamora, Z., Lui, LY., Sparks, L.M. et al. Percutaneous biopsies of skeletal muscle and adipose tissue in individuals older than 70: methods and outcomes in the Study of Muscle, Mobility and Aging (SOMMA). GeroScience 46, 3419–3428 (2024). https://doi.org/10.1007/s11357-024-01087-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11357-024-01087-2

Keywords

Search

Navigation