Skip to main content
SpringerLink
Log in

Preoperative Muscle Strength Is a Predictor of Outcomes After Esophagectomy

  • Original Article
  • Published:
Journal of Gastrointestinal Surgery

Abstract

Background

Sarcopenia, loss of muscle mass and strength, has been associated with more frequent complications after esophagectomy. This study compared hand-grip strength, muscle mass, and intramuscular adipose tissue as predictors of postoperative outcomes and mortality after esophagectomy.

Methods

Minimally invasive esophagectomy was performed on 175 patients with esophageal cancer. Skeletal muscle index and skeletal muscle density were derived from preoperative CTs. Hand-grip strength was measured using dynamometer. Univariate and multivariable analyses were performed.

Results

Preoperative hand-grip strength was normal in 91 (52%), intermediate in 43 (25%), and weak in 41 (23%) patients. Hand-grip strength was significantly correlated with both skeletal muscle index and skeletal muscle density. Postoperative pneumonia occurred in 8/41 (20%) patients with weak strength compared to 4/91 (4%) with normal strength (p = 0.006; Cochran-Armitage Test). Prolonged postoperative ventilation occurred in 11/41 (27%) patients with weak strength compared to 11/91 (12%) with normal strength (p = 0.036). Median length of stay was 9 days in patients with weak strength compared to 7 days for those with normal strength (p = 0.005; Kruskal–Wallis Test). Discharge to non-home location occurred in 15/41 (37%) with weak strength compared to 8/91 (9%) with normal strength (p < 0.001). Postoperative mortality at 90 days was 4/41 (10%) with weak strength compared with no mortalities (0/91) in the normal strength group (p = 0.004). Mortality at 1 year was 18/39 (46%) in patients with weak strength compared to 6/81 (7%) with normal strength, among 158 patients with 1-year follow-up (p < 0.001).

Conclusions

Preoperative hand-grip strength was found to be a powerful predictor of postoperative pneumonia, length of stay, discharge to non-home location, and mortality after esophagectomy.

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

Similar content being viewed by others

Abbreviations

HGS:

Hand-grip strength

LOS:

Length of stay

SMA:

Skeletal muscle area

SMD:

Skeletal muscle density

SMI:

Skeletal muscle index

References

  1. Reisinger KW, Bosmans JW, Uittenbogaart M, Alsoumali A, Poeze M, Sosef MN et al. Loss of Skeletal Muscle Mass During Neoadjuvant Chemoradiotherapy Predicts Postoperative Mortality in Esophageal Cancer Surgery. Ann Surg Oncol. 2015;22(13):4445-52. https://doi.org/10.1245/s10434-015-4558-4.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Awad S, Tan BH, Cui H, Bhalla A, Fearon KC, Parsons SL et al. Marked changes in body composition following neoadjuvant chemotherapy for oesophagogastric cancer. Clin Nutr. 2012;31(1):74-7. https://doi.org/10.1016/j.clnu.2011.08.008.

    Article  PubMed  Google Scholar 

  3. Fearon KC, Jenkins JT, Carli F, Lassen K. Patient optimization for gastrointestinal cancer surgery. Br J Surg. 2013;100(1):15-27. https://doi.org/10.1002/bjs.8988.

    Article  CAS  PubMed  Google Scholar 

  4. Santilli V, Bernetti A, Mangone M, Paoloni M. Clinical definition of sarcopenia. Clin Cases Miner Bone Metab. 2014;11(3):177-80.

    PubMed  PubMed Central  Google Scholar 

  5. Simonsen C, de Heer P, Bjerre ED, Suetta C, Hojman P, Pedersen BK et al. Sarcopenia and Postoperative Complication Risk in Gastrointestinal Surgical Oncology: A Meta-analysis. Ann Surg. 2018;268(1):58-69. https://doi.org/10.1097/SLA.0000000000002679.

    Article  PubMed  Google Scholar 

  6. Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90(6):1579-85. https://doi.org/10.3945/ajcn.2009.28047.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Martin L, Hopkins J, Malietzis G, Jenkins JT, Sawyer MB, Brisebois R et al. Assessment of Computed Tomography (CT)-Defined Muscle and Adipose Tissue Features in Relation to Short-Term Outcomes After Elective Surgery for Colorectal Cancer: A Multicenter Approach. Ann Surg Oncol. 2018;25(9):2669-80. https://doi.org/10.1245/s10434-018-6652-x.

    Article  PubMed  Google Scholar 

  8. Amini B, Boyle SP, Boutin RD, Lenchik L. Approaches to Assessment of Muscle Mass and Myosteatosis on Computed Tomography: A Systematic Review. J Gerontol A Biol Sci Med Sci. 2019;74(10):1671-8. https://doi.org/10.1093/gerona/glz034.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Kilgour RD, Vigano A, Trutschnigg B, Lucar E, Borod M, Morais JA. Handgrip strength predicts survival and is associated with markers of clinical and functional outcomes in advanced cancer patients. Support Care Cancer. 2013;21(12):3261-70. https://doi.org/10.1007/s00520-013-1894-4.

    Article  CAS  PubMed  Google Scholar 

  10. Gomez-Perez SL, Haus JM, Sheean P, Patel B, Mar W, Chaudhry V et al. Measuring Abdominal Circumference and Skeletal Muscle From a Single Cross-Sectional Computed Tomography Image: A Step-by-Step Guide for Clinicians Using National Institutes of Health ImageJ. JPEN J Parenter Enteral Nutr. 2016;40(3):308-18. https://doi.org/10.1177/0148607115604149.

    Article  PubMed  Google Scholar 

  11. Prado CM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB, Martin L et al. Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol. 2008;9(7):629-35. https://doi.org/10.1016/S1470-2045(08)70153-0.

    Article  PubMed  Google Scholar 

  12. Mitsiopoulos N, Baumgartner RN, Heymsfield SB, Lyons W, Gallagher D, Ross R. Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography. J Appl Physiol (1985). 1998;85(1):115-22. https://doi.org/10.1152/jappl.1998.85.1.115.

    Article  CAS  Google Scholar 

  13. Motz BM, Lorimer PD, Boselli D, Symanowski JT, Reames MK, Hill JS et al. Minimally Invasive Ivor Lewis Esophagectomy Without Patient Repositioning. J Gastrointest Surg. 2019. https://doi.org/10.1007/s11605-018-4063-8

  14. Lorimer PD, Motz BM, Boselli DM, Reames MK, Hill JS, Salo JC. Quality Improvement in Minimally Invasive Esophagectomy: Outcome Improvement Through Data Review. Ann Surg Oncol. 2019;26(1):177-87. https://doi.org/10.1245/s10434-018-6938-z.

    Article  PubMed  Google Scholar 

  15. Alley DE, Shardell MD, Peters KW, McLean RR, Dam TT, Kenny AM et al. Grip strength cutpoints for the identification of clinically relevant weakness. J Gerontol A Biol Sci Med Sci. 2014;69(5):559-66. https://doi.org/10.1093/gerona/glu011.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Martin L, Senesse P, Gioulbasanis I, Antoun S, Bozzetti F, Deans C et al. Diagnostic criteria for the classification of cancer-associated weight loss. J Clin Oncol. 2015;33(1):90-9. https://doi.org/10.1200/JCO.2014.56.1894.

    Article  PubMed  Google Scholar 

  17. Boshier PR, Heneghan R, Markar SR, Baracos VE, Low DE. Assessment of body composition and sarcopenia in patients with esophageal cancer: a systematic review and meta-analysis. Dis Esophagus. 2018;31(8). https://doi.org/10.1093/dote/doy047

  18. Deng HY, Zha P, Peng L, Hou L, Huang KL, Li XY. Preoperative sarcopenia is a predictor of poor prognosis of esophageal cancer after esophagectomy: a comprehensive systematic review and meta-analysis. Dis Esophagus. 2019;32(3). https://doi.org/10.1093/dote/doy115

  19. Ryan AM, Power DG, Daly L, Cushen SJ, Ni Bhuachalla E, Prado CM. Cancer-associated malnutrition, cachexia and sarcopenia: the skeleton in the hospital closet 40 years later. Proc Nutr Soc. 2016;75(2):199-211. https://doi.org/10.1017/S002966511500419X.

    Article  PubMed  Google Scholar 

  20. Wolfe RR. The underappreciated role of muscle in health and disease. Am J Clin Nutr. 2006;84(3):475-82. https://doi.org/10.1093/ajcn/84.3.475.

    Article  CAS  PubMed  Google Scholar 

  21. Zhuang CL, Shen X, Huang YY, Zhang FM, Chen XY, Ma LL et al. Myosteatosis predicts prognosis after radical gastrectomy for gastric cancer: A propensity score-matched analysis from a large-scale cohort. Surgery. 2019;166(3):297-304. https://doi.org/10.1016/j.surg.2019.03.020.

    Article  PubMed  Google Scholar 

  22. Stephens NA, Skipworth RJ, Macdonald AJ, Greig CA, Ross JA, Fearon KC. Intramyocellular lipid droplets increase with progression of cachexia in cancer patients. J Cachexia Sarcopenia Muscle. 2011;2(2):111-7. https://doi.org/10.1007/s13539-011-0030-x.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Zampieri S, Doria A, Adami N, Biral D, Vecchiato M, Savastano S et al. Subclinical myopathy in patients affected with newly diagnosed colorectal cancer at clinical onset of disease: evidence from skeletal muscle biopsies. Neurol Res. 2010;32(1):20-5. https://doi.org/10.1179/016164110X12556180205997.

    Article  CAS  PubMed  Google Scholar 

  24. Clark BC, Manini TM. Sarcopenia =/= dynapenia. J Gerontol A Biol Sci Med Sci. 2008;63(8):829-34. https://doi.org/10.1093/gerona/63.8.829.

    Article  PubMed  Google Scholar 

  25. Mitchell WK, Williams J, Atherton P, Larvin M, Lund J, Narici M. Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol. 2012;3:260. https://doi.org/10.3389/fphys.2012.00260.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Kurita D, Oguma J, Ishiyama K, Hirano Y, Kanamori J, Daiko H. Handgrip Strength Predicts Postoperative Pneumonia After Thoracoscopic-Laparoscopic Esophagectomy for Patients with Esophageal Cancer. Ann Surg Oncol. 2020;27(9):3173-81. https://doi.org/10.1245/s10434-020-08520-8.

    Article  PubMed  Google Scholar 

  27. Chen CH, Ho C, Huang YZ, Hung TT. Hand-grip strength is a simple and effective outcome predictor in esophageal cancer following esophagectomy with reconstruction: a prospective study. J Cardiothorac Surg. 2011;6:98. https://doi.org/10.1186/1749-8090-6-98.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Prado CM, Baracos VE, McCargar LJ, Reiman T, Mourtzakis M, Tonkin K et al. Sarcopenia as a determinant of chemotherapy toxicity and time to tumor progression in metastatic breast cancer patients receiving capecitabine treatment. Clin Cancer Res. 2009;15(8):2920-6. https://doi.org/10.1158/1078-0432.CCR-08-2242.

    Article  CAS  PubMed  Google Scholar 

  29. Lorimer PD, Motz BM, Watson M, Trufan SJ, Prabhu RS, Hill JS et al. Enteral Feeding Access Has an Impact on Outcomes for Patients with Esophageal Cancer Undergoing Esophagectomy: An Analysis of SEER-Medicare. Ann Surg Oncol. 2019;26(5):1311-9. https://doi.org/10.1245/s10434-019-07230-0.

    Article  PubMed  Google Scholar 

  30. Huddy JR, Huddy FMS, Markar SR, Tucker O. Nutritional optimization during neoadjuvant therapy prior to surgical resection of esophageal cancer-a narrative review. Dis Esophagus. 2018;31(1):1-11. https://doi.org/10.1093/dote/dox110.

    Article  CAS  PubMed  Google Scholar 

  31. Kight CE. Nutrition considerations in esophagectomy patients. Nutr Clin Pract. 2008;23(5):521-8. https://doi.org/10.1177/0884533608323427.

    Article  PubMed  Google Scholar 

  32. McKendry J, Thomas ACQ, Phillips SM. Muscle Mass Loss in the Older Critically Ill Population: Potential Therapeutic Strategies. Nutr Clin Pract. 2020;35(4):607-16. https://doi.org/10.1002/ncp.10540.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. LCI Research Support, Clinical Trials Office, Levine Cancer Institute, Carolinas Medical Center, Atrium Health, Charlotte, NC, USA

    Madison E. Colcord, Jennifer H. Benbow, Nicole L. Gower & Reilly E. Shea

  2. Department of Biostatistics, Levine Cancer Institute, Carolinas Medical Center, Atrium Health, Charlotte, NC, USA

    Sally Trufan

  3. Department of Clinical Nutrition, Carolinas Medical Center, Atrium Health, Charlotte, NC, USA

    Meredith E. Byrne

  4. Division of Surgical Oncology, Department of Surgery, Levine Cancer Institute, Carolinas Medical Center, Atrium Health, 1021 Morehead Medical Drive, Charlotte, NC, 28204, USA

    Michael D. Watson, Joshua S. Hill, M. Hart Squires & Jonathan C. Salo

Authors
  1. Madison E. Colcord
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jennifer H. Benbow
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sally Trufan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicole L. Gower
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Meredith E. Byrne
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Reilly E. Shea
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michael D. Watson
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Joshua S. Hill
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. M. Hart Squires
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jonathan C. Salo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MEC, JHB, NLG, MDW, JSH, MHS, and JCS contributed to the conception/design of the work; MEC, MEB, JHB, NLG, RES, and JCS contributed to the acquisition of data; SJT and JCS contributed to the analysis/interpretation of the data; MEC, SJT, JHB, and JCS drafted the manuscript; all authors critically revised the manuscript for intellectual content; all authors approved the final version submitted and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author

Correspondence to Jonathan C. Salo.

Ethics declarations

Conflict of Interest

The authors have no financial or conflict of interest disclosures.

Additional information

Publisher's Note

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

This paper was presented at American Society of Clinical Oncology Gastrointestinal Cancer Symposium in San Francisco in January 2020 and Society of Surgical Oncology Virtual Meeting in August 2020.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Colcord, M.E., Benbow, J.H., Trufan, S. et al. Preoperative Muscle Strength Is a Predictor of Outcomes After Esophagectomy. J Gastrointest Surg 25, 3040–3048 (2021). https://doi.org/10.1007/s11605-021-05183-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11605-021-05183-y

Keywords

Search

Navigation