Laparoscopic colorectal cancer surgery reduces the adverse impacts of sarcopenia on postoperative outcomes: a propensity score-matched analysis

  • Feng-Min Zhang
  • Bing-Wei Ma
  • Yang-Yang Huang
  • Wei-Zhe Chen
  • Jing-Juan Chen
  • Qian-Tong Dong
  • Wei-Sheng Chen
  • Xiao-Lei Chen
  • Xian Shen
  • Zhen Yu
  • Cheng-Le ZhuangEmail author



Sarcopenia is a negative predictor for postoperative recovery. This study was performed to evaluate the short-term outcomes of laparoscopic surgery in colorectal cancer patients with sarcopenia.


We conducted a study of patients who underwent curative surgeries for colorectal cancer in two centers from July 2014 to July 2018. In order to reduce selection bias, we conducted a propensity score matching analysis. Preoperative characteristics including age, gender, anemia, body mass index, hypoalbuminemia, America society of anesthesiology scores, epidural anesthesia, operative procedure, stoma, tumor location, and combined resection were incorporated in the model, and produced 58 matched pairs. The third lumbar skeletal muscle mass, handgrip strength, and 6 m usual gait speed were measured to define sarcopenia. Short-term outcomes were compared between the two groups.


In a total of 1136 patients, 272 had sarcopenia diagnosed, and 227 were further analyzed in this study. Among them, 108 patients underwent laparoscopic colorectal surgery and 119 underwent open colorectal surgery. In the matched cohort, the clinical characteristics of the two groups were well matched. The laparoscopic group had significantly reduced overall complications (15.5% vs. 36.2%, P = 0.016) and shorter postoperative hospital stays (10.5 vs. 14, P = 0.027). Subgroup analysis of postoperative complications showed that the incidence of surgical complications (P = 0.032) was lower in the laparoscopic group. Hospitalization costs (P = 0.071) and 30-day readmissions (P = 0.215) were similar between the two groups.


Laparoscopic surgery for colorectal cancer is a safe and feasible option with better short-term outcomes in patients with sarcopenia.


Sarcopenia Laparoscopy Colorectal cancer Short-term outcome Propensity score 



This work was funded by the National Natural Science Foundation of China (Nos. 81800795, 81770884), Shanghai Municipal Commission of Health and Family Planning (No. 20184Y0301), Shanghai Science and Technology Committee (No. 16411954200), the Fundamental Research Funds for the Central Universities and the foundation of the Health Department of Zhejiang province (2016DTA006).

Compliance with ethical standards


Feng-Min Zhang, Bing-Wei Ma, Yang-Yang Huang, Wei-Zhe Chen, Jing-Juan Chen, Qian-Tong Dong, Wei-Sheng Chen, Xiao-Lei Chen, Xian Shen, Zhen Yu, and Cheng-Le Zhuang have no conflicts of interest or financial ties to disclose.


  1. 1.
    Narici MV, Maffulli N (2010) Sarcopenia: characteristics, mechanisms and functional significance. Br Med Bull 95:139–159PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Cruzjentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM (2010) Sarcopenia: European consensus on definition and diagnosis report of the European working group on sarcopenia in older people. Age Ageing 39:412–423CrossRefGoogle Scholar
  3. 3.
    Cheng Q, Zhu X, Zhang X, Li H, Du Y, Hong W, Xue S, Zhu H (2014) A cross-sectional study of loss of muscle mass corresponding to sarcopenia in healthy Chinese men and women: reference values, prevalence, and association with bone mass. J Bone Miner Metab 32:78–88PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Phillips SM (2015) Nutritional supplements in support of resistance exercise to counter age-related sarcopenia. Adv Nutr Res 6:452–460CrossRefGoogle Scholar
  5. 5.
    Dodson S, Baracos VE, Jatoi A, Evans WJ, Cella D, Dalton JT, Steiner MS (2011) Muscle wasting in cancer cachexia: clinical implications, diagnosis, and emerging treatment strategies. Annu Rev Med 62:265–279PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Feliciano EMC, Kroenke CH, Meyerhardt JA, Prado CM, Bradshaw PT, Kwan ML, Xiao J, Alexeeff S, Corley D, Weltzien E, Castillo AL, Caan BJ (2017) Association of systemic inflammation and sarcopenia with survival in nonmetastatic colorectal cancer: results from the C SCANS Study. JAMA Oncol 3:e172319PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Janssen I, Heymsfield SB, Ross R (2002) Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 50:889–896CrossRefGoogle Scholar
  8. 8.
    Yamada M, Shu N, Fukutani N, Tanigawa T, Yukutake T, Kayama H, Aoyama T, Arai H (2013) Prevalence of sarcopenia in community-dwelling Japanese older adults. J Am Med Dir Assoc 14:911–915PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Kim TN, Park MS, Lim KI, Choi HY, Yang SJ, Yoo HJ, Kang HJ, Song W, Choi H, Baik SH (2013) Relationships between sarcopenic obesity and insulin resistance, inflammation, and vitamin D status: the Korean Sarcopenic Obesity Study. Clin Endocrinol 78:525–532CrossRefGoogle Scholar
  10. 10.
    Peterson SJ, Braunschweig CA (2015) Prevalence of sarcopenia and associated outcomes in the clinical setting. Nutr Clin Pract 31:40–48PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Lieffers JR, Bathe OF, Fassbender K, Winget M, Baracos VE (2012) Sarcopenia is associated with postoperative infection and delayed recovery from colorectal cancer resection surgery. Br J Cancer 107:931–936PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    National Comprehensive Cancer Network. Colon Cancer (Version 4.2018). Accessed 11 Sep 2018
  13. 13.
    National Comprehensive Cancer Network. Rectal Cancer (Version 3.2018). Accessed 11 Sep 2018
  14. 14.
    Yeo H, Niland J, Milne D, ter Veer A, Bekaii-Saab T, Farma JM, Lai L, Skibber JM, Small W Jr, Wilkinson N, Schrag D, Weiser MR (2015) Incidence of minimally invasive colorectal cancer surgery at National Comprehensive Cancer Network Centers. J Natl Cancer Inst 107:362PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Nelson H, Sargent DJ, Wieand HS, Fleshman J, Anvari M, Stryker SJ, Beart RW Jr, Hellinger M, Flanagan R Jr, Peters W, Ota D (2004) A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med 350:2050–2059PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Veldkamp R, Kuhry E, Hop WC, Jeekel J, Kazemier G, Bonjer HJ, Haglind E, Påhlman L, Cuesta MA, Msika S (2005) Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol 6:477–484CrossRefGoogle Scholar
  17. 17.
    Hewett PJ, Allardyce RA, Bagshaw PF, Frampton CM, Frizelle FA, Rieger NA, Smith JS, Solomon MJ, Stephens JH, Stevenson AR (2008) Short-term outcomes of the Australasian randomized clinical study comparing laparoscopic and conventional open surgical treatments for colon cancer: the ALCCaS trial. Ann Surg 248:728–738PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Abdiev S, Kodera Y, Fujiwara M, Koike M, Nakayama G, Ohashi N, Tanaka C, Sakamoto J, Nakao A (2011) Nutritional recovery after open and laparoscopic gastrectomies. Gastric Cancer 14:144–149PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Aoyama T, Sato T, Hayashi T, Yamada T, Cho H, Ogata T, Oba K, Yoshikawa T (2017) Does a laparoscopic approach attenuate the body weight loss and lean body mass loss observed in open distal gastrectomy for gastric cancer? A single-institution exploratory analysis of the JCOG 0912 phase III trial. Gastric Cancer 21:345–352PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Kondrup J, Allison SP, Elia M, Vellas B, Plauth M (2003) ESPEN guidelines for nutrition screening 2002. Clin Nutr (Edinburgh, Scotland) 22:415–421CrossRefGoogle Scholar
  21. 21.
    Charlson ME, Pompei P, Ales KL, Mackenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chron Dis 40:373–383PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Mourtzakis M, Prado CM, Lieffers JR, Reiman T, McCargar LJ, Baracos VE (2008) A practical and precise approach to quantification of body composition in cancer patients using computed tomography images acquired during routine care. Appl Physiol Nutr Metab 33:997–1006PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Mitsiopoulos N, Baumgartner RN, Heymsfield SB, Lyons W, Gallagher D, Ross R (1998) Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography. J Appl Physiol (Bethesda, MD: 1985) 85:115–122CrossRefGoogle Scholar
  25. 25.
    Fess EE (1992) Grip strength. In: dCasanova JS (ed) Clinical assessment recommendations, 2nd edn. American Society of Hand Therapists, Chicago, pp 41–45Google Scholar
  26. 26.
    Watanabe T, Owashi K, Kanauchi Y, Mura N, Takahara M, Ogino T (2005) The short-term reliability of grip strength measurement and the effects of posture and grip span. J Hand Surg 30:603–609CrossRefGoogle Scholar
  27. 27.
    Cesari M, Kritchevsky SB, Newman AB, Simonsick EM, Harris TB, Penninx BW, Brach JS, Tylavsky FA, Satterfield S, Bauer DC, Rubin SM, Visser M, Pahor M (2009) Added value of physical performance measures in predicting adverse health-related events: results from the Health, Aging and Body Composition Study. J Am Geriatr Soc 57:251–259PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, Chou MY, Chen LY, Hsu PS, Krairit O (2014) Sarcopenia in Asia: consensus report of the Asian working group for sarcopenia. J Am Med Dir Assoc 15:95–101CrossRefGoogle Scholar
  29. 29.
    Zhuang CL, Huang DD, Pang WY, Zhou CJ, Wang SL, Lou N, Ma LL, Yu Z, Shen X (2016) Sarcopenia is an independent predictor of severe postoperative complications and long-term survival after radical gastrectomy for gastric cancer: analysis from a large-scale cohort. Medicine 95:e3164PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Prado CM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB, Martin L, Baracos VE (2008) Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol 9:629–635CrossRefGoogle Scholar
  31. 31.
    Austin PC (2009) Some methods of propensity-score matching had superior performance to others: results of an empirical investigation and Monte Carlo simulations. Biometrical J 51:171–184CrossRefGoogle Scholar
  32. 32.
    Wilson D, Jackson T, Sapey E, Lord JM (2017) Frailty and sarcopenia: the potential role of an aged immune system. Ageing Res Rev 36:1–10PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Simonsen C, De HP, Bjerre ED, Suetta C, Hojman P, Pedersen BK, Svendsen LB, Christensen JF (2018) Sarcopenia and postoperative complication risk in gastrointestinal surgical oncology: a meta-analysis. Ann Surg 268:58–69PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Bahat G, Tufan A, Ozkaya H, Tufan F, Akpinar TS, Akin S, Bahat Z, Kaya Z, Kiyan E, Erten N (2014) Relation between hand grip strength, respiratory muscle strength and spirometric measures in male nursing home residents. Aging Male 17:136–140PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Wakabayashi H (2014) Presbyphagia and sarcopenic dysphagia: association between aging, sarcopenia, and deglutition disorders. J Frailty Aging 3:97–103PubMedPubMedCentralGoogle Scholar
  36. 36.
    Ida S, Watanabe M, Yoshida N, Baba Y, Umezaki N, Harada K, Karashima R, Yu I, Iwagami S, Baba H (2015) Sarcopenia is a predictor of postoperative respiratory complications in patients with esophageal cancer. Ann Surg Oncol 22:4432–4437PubMedCrossRefGoogle Scholar
  37. 37.
    Nishigori T, Okabe H, Tanaka E, Tsunoda S, Hisamori S, Sakai Y (2016) Sarcopenia as a predictor of pulmonary complications after esophagectomy for thoracic esophageal cancer. J Surg Oncol 113:678–684PubMedCrossRefGoogle Scholar
  38. 38.
    Wakefield CH, Carey PD, Foulds S, Monson JR, Guillou PJ (1993) Changes in major histocompatibility complex class II expression in monocytes and T cells of patients developing infection after surgery. Br J Surg 80:205–209PubMedCrossRefGoogle Scholar
  39. 39.
    Styliani K, Theodoros K, Theodoropoulos GE (2013) Immune response after laparoscopic colectomy for cancer: a review. Gastroenterol Rep 1:85–94CrossRefGoogle Scholar
  40. 40.
    Mh VDP, Haglind E, Cuesta MA, Fürst A, Lacy AM, Hop WC, Bonjer HJ (2013) Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomised, phase 3 trial. Lancet Oncol 14:210–218CrossRefGoogle Scholar
  41. 41.
    Abraham NS, Young JM, Solomon MJ (2004) Meta-analysis of short-term outcomes after laparoscopic resection for colorectal cancer. Br J Surg 91:1111–1124PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Zheng HL, Lu J, Zheng CH, Li P, Xie JW, Wang JB, Lin JX, Chen QY, Lin M, Tu RH (2017) Short- and long-term outcomes in malnourished patients after laparoscopic or open radical gastrectomy. World J Surg 42:1–9Google Scholar
  43. 43.
    Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G, McBurnie MA (2001) Frailty in older adults: evidence for a phenotype. Med Sci 56:M146–M156Google Scholar
  44. 44.
    Gietelink L, Wouters MW, Bemelman WA, Dekker JW, Tollenaar RA, Tanis PJ (2016) Reduced 30-day mortality after laparoscopic colorectal cancer Surgery: a population based study from the dutch surgical colorectal audit (DSCA). Ann Surg 264:135–140PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Cerdan Santacruz C, Frasson M, Flor-Lorente B, Ramos Rodriguez JL, Trallero Anoro M, Millan Scheiding M, Maseda Diaz O, Dujovne Lindenbaum P, Monzon Abad A, Garcia-Granero Ximenez E (2017) Laparoscopy may decrease morbidity and length of stay after elective colon cancer resection, especially in frail patients: results from an observational real-life study. Surg Endosc 31:5032–5042PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Frasson M, Braga M, Vignali A, Zuliani W, Di Carlo V (2008) Benefits of laparoscopic colorectal resection are more pronounced in elderly patients. Dis Colon Rectum 51:296–300PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Grailey K, Markar SR, Karthikesalingam A, Aboud R, Ziprin P, Faiz O (2013) Laparoscopic versus open colorectal resection in the elderly population. Surg Endosc 27:19–30PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Pędziwiatr M, Pisarska M, Major P, Grochowska A, Matłok M, Przęczek K, Stefura T, Budzyński A, Kłęk S (2016) Laparoscopic colorectal cancer surgery combined with enhanced recovery after surgery protocol (ERAS) reduces the negative impact of sarcopenia on short-term outcomes. Eur J Surg Oncol 42:779–787PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Binay SV, Safer U, Kaplan M, Terekeci H, Top C (2015) Limitations of the definition of sarcopenia in cancer surgery. J Surg Oncol 112:116–116CrossRefGoogle Scholar
  50. 50.
    Reisinger KW, Vugt JLA, Van Tegels JJW, Claire S, Hulsewé KWE, Hoofwijk AGM, Stoot JH, Meyenfeldt MF, Von Beets GL, Derikx JPM (2015) Functional compromise reflected by sarcopenia, frailty, and nutritional depletion predicts adverse postoperative outcome after colorectal cancer surgery. Ann Surg 261:345–352PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Tegels JJW, Vugt JLA, Van Reisinger KW, Hulsewé KWE, Hoofwijk AGM, Derikx JPM, Stoot JHMB (2015) Sarcopenia is highly prevalent in patients undergoing surgery for gastric cancer but not associated with worse outcomes. J Surg Oncol 112:403–407PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Burden ST, Hill J, Shaffer JL, Todd C (2010) Nutritional status of preoperative colorectal cancer patients. J Hum Nutr Diet 23:402–407PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Lidder P, Thomas S, Fleming S, Hosie K, Shaw S, Lewis S (2013) A randomized placebo controlled trial of preoperative carbohydrate drinks and early postoperative nutritional supplement drinks in colorectal surgery. Colorectal Dis 15:737–745PubMedCrossRefPubMedCentralGoogle Scholar
  54. 54.
    Dronkers JJ, Lamberts H, Reutelingsperger IM, Naber RH, Dronkers-Landman CM, Veldman A, van Meeteren NL (2010) Preoperative therapeutic programme for elderly patients scheduled for elective abdominal oncological surgery: a randomized controlled pilot study. Clin Rehabil 24:614–622PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    Varadhan KK, Neal KR, Dejong CHC, Fearon KCH, Olle L, Lobo DN (2010) The enhanced recovery after surgery (ERAS) pathway for patients undergoing major elective open colorectal surgery: a meta-analysis of randomized controlled trials. Clin Nutr 29:434–440PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Feng-Min Zhang
    • 1
    • 3
  • Bing-Wei Ma
    • 2
  • Yang-Yang Huang
    • 5
  • Wei-Zhe Chen
    • 1
  • Jing-Juan Chen
    • 2
  • Qian-Tong Dong
    • 1
  • Wei-Sheng Chen
    • 1
  • Xiao-Lei Chen
    • 1
  • Xian Shen
    • 4
  • Zhen Yu
    • 2
  • Cheng-Le Zhuang
    • 1
    • 2
    Email author
  1. 1.Department of Gastrointestinal SurgeryThe First Affiliated Hospital of Wenzhou Medical UniversityWenzhouChina
  2. 2.Department of Gastrointestinal SurgeryShanghai Tenth People’s Hospital Affiliated to TongJi UniversityShanghaiChina
  3. 3.The First Clinical Medical InstituteWenzhou Medical UniversityWenzhouChina
  4. 4.Department of Gastrointestinal SurgeryThe Second Affiliated Hospital of Wenzhou Medical UniversityWenzhouChina
  5. 5.Department of NeurologyShanghai Fourth People’s HospitalShanghaiChina

Personalised recommendations