Skip to main content

Advertisement

SpringerLink
Log in

Preoperative sarcopenia is a negative predictor for enhanced postoperative recovery after pancreaticoduodenectomy

  • Original Article
  • Published:
Langenbeck's Archives of Surgery Aims and scope Submit manuscript

Abstract  

Purpose

Sarcopenia is common in pancreatic cancer patients. Considering the growing adoption of standardized protocols for enhanced recovery after surgery (ERAS), we examined the clinical impact of sarcopenia in pancreaticoduodenectomy (PD) patients in a 5-day accelerated ERAS program, termed the Whipple Accelerated Recovery Pathway.

Methods

A retrospective review was conducted of patients undergoing PD from 2017 through 2020 on the ERAS pathway. Preoperative computerized tomographic scans taken within 45 days before surgery were analyzed to determine psoas muscle cross-sectional area (PMA) at the third lumbar vertebral body. Sarcopenia was defined as the lowest quartile of PMA respective to gender. Outcome measures were compared between patients with or without sarcopenia.

Results

In this 333-patient cohort, 252 (75.7%) patients had final pathology revealing pancreatic or periampullary cancer. The median age was 66.7 years (16.4–88.4 years) with a 161:172 male to female ratio. Sarcopenia correlated with delayed tolerance of oral intake (OR 2.2; 95%CI 1.1–4.3, P = 0.03), increased complication rates (OR 4.3; 95%CI 2.2–8.5, P < 0.01), and longer hospital length of stay (LOS) (P < 0.05). Preoperative albumin levels, BMI, and history of pancreatitis were also found to correlate with LOS (P < 0.05). Multivariate regression analysis found low PMA, BMI, and male gender to be independent predictors of increased LOS (P < 0.05).

Conclusion

Sarcopenia correlated with increased LOS and postoperative complications in ERAS patients after PD. Sarcopenia can be used to predict poor candidates for ERAS protocols who may require an alternative recovery protocol, promoting a clinical tier-based approach to ERAS for pancreatic surgery.

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

Similar content being viewed by others

References

  1. McGuigan A, Kelly P, Turkington RC, Jones C, Coleman HG, McCain RS (2018) Pancreatic cancer: a review of clinical diagnosis, epidemiology, treatment and outcomes. World J Gastroenterol 24(43):4846–4861

    Article  PubMed  PubMed Central  Google Scholar 

  2. Ansari D, Tingstedt B, Andersson B, Holmquist F, Sturesson C, Williamsson C et al (2016) Pancreatic cancer: yesterday, today and tomorrow. Future Oncol 12(16):1929–1946

    Article  CAS  PubMed  Google Scholar 

  3. Singhi AD, Koay EJ, Chari ST, Maitra A (2019) Early detection of pancreatic cancer: opportunities and challenges. Gastroenterology 156(7):2024–2040

    Article  PubMed  Google Scholar 

  4. Furukawa H, Okada S, Saisho H, Ariyama J, Karasawa E, Nakaizumi A et al (1996) Clinicopathologic features of small pancreatic adenocarcinoma. A collective study Cancer 78(5):986–990

    CAS  PubMed  Google Scholar 

  5. Tran KTC, Smeenk HG, van Eijck CHJ, Kazemier G, Hop WC, Greve JWG et al (2004) Pylorus preserving pancreaticoduodenectomy versus standard Whipple procedure: a prospective, randomized, multicenter analysis of 170 patients with pancreatic and periampullary tumors. Ann Surg 240(5):738–745

    Article  PubMed  PubMed Central  Google Scholar 

  6. D’Cruz JR, Misra S, Shamsudeen S. Pancreaticoduodenectomy. StatPearls. Treasure Island (FL): StatPearls Publishing; 2021.

  7. Srinarmwong C, Luechakiettisak P, Prasitvilai W (2008) Standard Whipple’s operation versus pylorus preserving pancreaticoduodenectomy: a randomized controlled trial study. J Med Assoc Thai 91(5):693–698

    PubMed  Google Scholar 

  8. Lassen K, Coolsen MME, Slim K, Carli F, de Aguilar-Nascimento JE, Schäfer M et al (2012) Guidelines for perioperative care for pancreaticoduodenectomy: Enhanced Recovery After Surgery (ERAS®) Society recommendations. Clin Nutr 31(6):817–830

    Article  PubMed  Google Scholar 

  9. Ji H-B, Zhu W-T, Wei Q, Wang X-X, Wang H-B, Chen Q-P (2018) Impact of enhanced recovery after surgery programs on pancreatic surgery: a meta-analysis. World J Gastroenterol 24(15):1666–1678

    Article  PubMed  PubMed Central  Google Scholar 

  10. Melloul E, Lassen K, Roulin D, Grass F, Perinel J, Adham M et al (2020) Guidelines for perioperative care for pancreatoduodenectomy: enhanced recovery after surgery (ERAS) recommendations 2019. World J Surg 44(7):2056–2084

    Article  PubMed  Google Scholar 

  11. Bongers BC, Dejong CHC, den Dulk M. Enhanced recovery after surgery programmes in older patients undergoing hepatopancreatobiliary surgery: what benefits might prehabilitation have? Eur J Surg Oncol. 2021 Mar;47(3 Pt A):551–9.

  12. Lavu H, McCall NS, Winter JM, Burkhart RA, Pucci M, Leiby BE et al (2019) Enhancing patient outcomes while containing costs after complex abdominal operation: a randomized controlled trial of the Whipple accelerated recovery pathway. J Am Coll Surg 228(4):415–424

    Article  PubMed  PubMed Central  Google Scholar 

  13. Whittle J, Wischmeyer PE, Grocott MPW, Miller TE (2018) Surgical prehabilitation: nutrition and exercise. Anesthesiol Clin 36(4):567–580

    Article  PubMed  Google Scholar 

  14. Thomas G, Tahir MR, Bongers BC, Kallen VL, Slooter GD, van Meeteren NL (2019) Prehabilitation before major intra-abdominal cancer surgery: a systematic review of randomised controlled trials. Eur J Anaesthesiol 36(12):933–945

    Article  PubMed  PubMed Central  Google Scholar 

  15. Wilson RJT, Davies S, Yates D, Redman J, Stone M (2010) Impaired functional capacity is associated with all-cause mortality after major elective intra-abdominal surgery. Br J Anaesth 105(3):297–303

    Article  CAS  PubMed  Google Scholar 

  16. Choi MH, Yoon SB, Lee K, Song M, Lee IS, Lee MA et al (2018) Preoperative sarcopenia and post-operative accelerated muscle loss negatively impact survival after resection of pancreatic cancer. J Cachexia Sarcopenia Muscle 9(2):326–334

    Article  PubMed  PubMed Central  Google Scholar 

  17. Ozola Zalite I, Zykus R, Francisco Gonzalez M, Saygili F, Pukitis A, Gaujoux S et al (2015) Influence of cachexia and sarcopenia on survival in pancreatic ductal adenocarcinoma: a systematic review. Pancreatology 15(1):19–24

    Article  CAS  PubMed  Google Scholar 

  18. Amini N, Spolverato G, Gupta R, Margonis GA, Kim Y, Wagner D et al (2015) Impact total psoas volume on short- and long-term outcomes in patients undergoing curative resection for pancreatic adenocarcinoma: a new tool to assess sarcopenia. J Gastrointest Surg 19(9):1593–1602

    Article  PubMed  PubMed Central  Google Scholar 

  19. Pecorelli N, Carrara G, De Cobelli F, Cristel G, Damascelli A, Balzano G et al (2016) Effect of sarcopenia and visceral obesity on mortality and pancreatic fistula following pancreatic cancer surgery. Br J Surg 103(4):434–442

    Article  CAS  PubMed  Google Scholar 

  20. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T et al (2019) Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 48(1):16–31

    Article  PubMed  Google Scholar 

  21. Chan MY, Chok KSH (2019) Sarcopenia in pancreatic cancer - effects on surgical outcomes and chemotherapy. World J Gastrointest Oncol 11(7):527–537

    Article  PubMed  PubMed Central  Google Scholar 

  22. Simonsen C, de Heer P, Bjerre ED, Suetta C, Hojman P, Pedersen BK et al (2018) Sarcopenia and postoperative complication risk in gastrointestinal surgical oncology: a meta-analysis. Ann Surg 268(1):58–69

    Article  PubMed  Google Scholar 

  23. von Haehling S, Anker SD (2014) Prevalence, incidence and clinical impact of cachexia: facts and numbers-update 2014. J Cachexia Sarcopenia Muscle 5(4):261–263

    Article  Google Scholar 

  24. Amundson JR, Williams JK, Benjamin AJ, Witmer HDD, Roggin KK (2020) The impact of sarcopenia on patients undergoing treatment for pancreatic ductal adenocarcinoma. Journal of Pancreatology 3(2):59–71

    Article  Google Scholar 

  25. Pulvirenti A, Ramera M, Bassi C (2017) Modifications in the International Study Group for Pancreatic Surgery (ISGPS) definition of postoperative pancreatic fistula. Transl Gastroenterol Hepatol 2(12):107

    Article  PubMed  PubMed Central  Google Scholar 

  26. Panwar R, Pal S (2017) The International Study Group of Pancreatic Surgery definition of delayed gastric emptying and the effects of various surgical modifications on the occurrence of delayed gastric emptying after pancreatoduodenectomy. HBPD INT 16(4):353–363

    PubMed  Google Scholar 

  27. Zager Y, Khalilieh S, Ganaiem O, Gorgov E, Horesh N, Anteby R et al (2021) Low psoas muscle area is associated with postoperative complications in Crohn’s disease. Int J Colorectal Dis 36(3):543–550

    Article  PubMed  Google Scholar 

  28. Miyamoto Y, Baba Y, Sakamoto Y, Ohuchi M, Tokunaga R, Kurashige J et al (2015) Sarcopenia is a negative prognostic factor after curative resection of colorectal cancer. Ann Surg Oncol 22(8):2663–2668

    Article  PubMed  Google Scholar 

  29. Shin HE, Walston JD, Kim M, Won CW (2021) Sex-specific differences in the effect of free testosterone on sarcopenia components in older adults. Front Endocrinol (Lausanne) 22:12

    Google Scholar 

  30. Wang S, Xie H, Gong Y, Kuang J, Yan L, Ruan G et al (2020) The value of L3 skeletal muscle index in evaluating preoperative nutritional risk and long-term prognosis in colorectal cancer patients. Sci Rep 10(1):8153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Takagi K, Yagi T, Yoshida R, Umeda Y, Nobuoka D, Kuise T et al (2017) Sarcopenia predicts postoperative infection in patients undergoing hepato-biliary-pancreatic surgery. International Journal of Surgery Open 6:12–18

    Article  Google Scholar 

  32. Makris K, Spanou L (2016) Acute kidney injury: definition, pathophysiology and clinical phenotypes. Clin Biochem Rev 37(2):85–98

    PubMed  PubMed Central  Google Scholar 

  33. 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(2):205–213

    Article  PubMed  PubMed Central  Google Scholar 

  34. Martin L, Birdsell L, Macdonald N, Reiman T, Clandinin MT, McCargar LJ et al (2013) Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J Clin Oncol 31(12):1539–1547

    Article  PubMed  Google Scholar 

  35. Asbun HJ, Stauffer JA (2012) Laparoscopic vs open pancreaticoduodenectomy: overall outcomes and severity of complications using the Accordion Severity Grading System. J Am Coll Surg 215(6):810–819

    Article  PubMed  Google Scholar 

  36. Chua TC, Saxena A (2010) Extended pancreaticoduodenectomy with vascular resection for pancreatic cancer: a systematic review. J Gastrointest Surg 14(9):1442–1452

    Article  PubMed  Google Scholar 

  37. Pugalenthi A, Protic M, Gonen M, Kingham TP, Angelica MID, Dematteo RP et al (2016) Postoperative complications and overall survival after pancreaticoduodenectomy for pancreatic ductal adenocarcinoma. J Surg Oncol 113(2):188–193

    Article  PubMed  Google Scholar 

  38. Weber CE, Bock EA, Hurtuk MG, Abood GJ, Pickleman J, Shoup M et al (2014) Clinical and pathologic features influencing survival in patients undergoing pancreaticoduodenectomy for pancreatic adenocarcinoma. J Gastrointest Surg 18(2):340–347

    Article  PubMed  Google Scholar 

  39. Gouma DJ, van Geenen RC, van Gulik TM, de Haan RJ, de Wit LT, Busch OR et al (2000) Rates of complications and death after pancreaticoduodenectomy: risk factors and the impact of hospital volume. Ann Surg 232(6):786–795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Yu L, Huang Q, Xie F, Lin X, Liu C (2014) Risk factors of postoperative complications of pancreatoduodenectomy. Hepatogastroenterology 61(135):2091–2095

    PubMed  Google Scholar 

  41. Ren S, Liu P, Zhou N, Dong J, Liu R, Ji W (2011) Complications after pancreaticoduodenectomy for pancreatic cancer: a retrospective study. Int Surg 96(3):220–227

    Article  PubMed  Google Scholar 

  42. Chen J-S, Liu G, Li T-R, Chen J-Y, Xu Q-M, Guo Y-Z et al (2019) Pancreatic fistula after pancreaticoduodenectomy: risk factors and preventive strategies. J Cancer Res Ther 15(4):857–863

    Article  PubMed  Google Scholar 

  43. Roberts KJ, Hodson J, Mehrzad H, Marudanayagam R, Sutcliffe RP, Muiesan P et al (2014) A preoperative predictive score of pancreatic fistula following pancreatoduodenectomy. HPB (Oxford) 16(7):620–628

    Article  Google Scholar 

  44. Mogal H, Vermilion SA, Dodson R, Hsu F-C, Howerton R, Shen P et al (2017) Modified frailty index predicts morbidity and mortality after pancreaticoduodenectomy. Ann Surg Oncol 24(6):1714–1721

    Article  PubMed  PubMed Central  Google Scholar 

  45. Benton K, Thomson I, Isenring E, Mark Smithers B, Agarwal E (2018) An investigation into the nutritional status of patients receiving an Enhanced Recovery After Surgery (ERAS) protocol versus standard care following oesophagectomy. Support Care Cancer 26(6):2057–2062

    Article  PubMed  Google Scholar 

  46. Braga M, Pecorelli N, Ariotti R, Capretti G, Greco M, Balzano G et al (2014) Enhanced recovery after surgery pathway in patients undergoing pancreaticoduodenectomy. World J Surg 38(11):2960–2966

    Article  PubMed  Google Scholar 

  47. Shintakuya R, Sasaki M, Nakamitsu A, Kohyama M, Tazaki T, Sugiyama Y et al (2019) Sarcopenia is an independent predictor of delayed gastric emptying following pancreaticoduodenectomy: a retrospective study. ANZ J Surg 89(10):E433–E437

    Article  PubMed  Google Scholar 

  48. Morley JE, Argiles JM, Evans WJ, Bhasin S, Cella D, Deutz NEP et al (2010) Nutritional recommendations for the management of sarcopenia. J Am Med Dir Assoc 11(6):391–396

    Article  PubMed  PubMed Central  Google Scholar 

  49. Horowitz M, Neeman E, Sharon E, Ben-Eliyahu S (2015) Exploiting the critical perioperative period to improve long-term cancer outcomes. Nat Rev Clin Oncol 12(4):213–226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Roschel H, Hayashi AP, Fernandes AL, Jambassi-Filho JC, Hevia-Larraín V, de Capitani M et al (2021) Supplement-based nutritional strategies to tackle frailty: a multifactorial, double-blind, randomized placebo-controlled trial. Clin Nutr 40(8):4849–4858

    Article  CAS  PubMed  Google Scholar 

  51. Berkelmans GHK, Wilts BJW, Kouwenhoven EA, Kumagai K, Nilsson M, Weijs TJ et al (2016) Nutritional route in oesophageal resection trial II (NUTRIENT II): study protocol for a multicentre open-label randomised controlled trial. BMJ Open 6(8):e011979

    Article  PubMed  PubMed Central  Google Scholar 

  52. van Dijk DPJ, van Woerden V, Cakir H, den Dulk M, Olde Damink SWM, Dejong CHC (2017) ERAS: improving outcome in the cachectic HPB patient. J Surg Oncol 116(5):617–622

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Surgery, Biliary and Related Cancer Center, Thomas Jefferson University, Jefferson PancreasPhiladelphia, PA, USA

    David O. Nauheim, Hannah Hackbart, Emily Papai, David Moskal, Charles J. Yeo, Harish Lavu & Avinoam Nevler

  2. Pancreatic Cancer Research Lab, Department of Surgery, Thomas Jefferson University, 1025 Walnut Street, Curtis Building, Suite 618, Philadelphia, PA, 19107, USA

    Avinoam Nevler

Authors
  1. David O. Nauheim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hannah Hackbart
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Emily Papai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David Moskal
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Charles J. Yeo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Harish Lavu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Avinoam Nevler
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

DON, HH, DM, EP, AN: data collection, data analysis, writing (original, review, and editing). AN, HL, CJY: resources, supervision, writing (review and editing).

Corresponding author

Correspondence to Avinoam Nevler.

Ethics declarations

Conflict of interest

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.

This work accepted for presentation to the American College of Surgeons Clinical Congress, 10/23/2021 and Pancreas Club 11/11/2021.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 15 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nauheim, D.O., Hackbart, H., Papai, E. et al. Preoperative sarcopenia is a negative predictor for enhanced postoperative recovery after pancreaticoduodenectomy. Langenbecks Arch Surg 407, 2355–2362 (2022). https://doi.org/10.1007/s00423-022-02558-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00423-022-02558-w

Keywords

Search

Navigation