Advertisement

Journal of Gastrointestinal Surgery

, Volume 22, Issue 4, pp 703–712 | Cite as

Anthropometric Changes in Patients with Pancreatic Cancer Undergoing Preoperative Therapy and Pancreatoduodenectomy

  • Jordan M. Cloyd
  • Graciela M. Nogueras-González
  • Laura R. Prakash
  • Maria Q. B. Petzel
  • Nathan H. Parker
  • An T. Ngo-Huang
  • David Fogelman
  • Jason W. Denbo
  • Naveen Garg
  • Michael P. Kim
  • Jeffrey E. Lee
  • Ching-Wei D. Tzeng
  • Jason B. Fleming
  • Matthew H. G. Katz
Original Article

Abstract

Background

The changes in body composition that occur in response to therapy for localized pancreatic ductal adenocarcinoma (PDAC) and during the early survivorship period, as well as their clinical significance, are poorly understood.

Methods

One hundred twenty-seven consecutive patients with PDAC who received preoperative therapy followed by pancreatoduodenectomy (PD) at a single institution between 2009 and 2012 were longitudinally evaluated. Changes in skeletal muscle (SKM), visceral adipose tissue (VAT), and subcutaneous adipose tissue (SAT) were measured on serial computed tomography images obtained upon presentation, prior to pancreatectomy, and approximately 3 and 12 months after surgery.

Results

Prior to therapy, patients’ mean baseline BMI was 26.5 ± 4.7 kg/m2 and 63.0% met radiographic criteria for sarcopenia. During a mean 5.4 ± 2.3 months of preoperative therapy, minimal changes in SKM (− 0.5 ± 7.8%, p > 0.05), VAT (− 1.8 ± 62.6%, p < 0.001), and SAT (− 4.8 ± 27.7%, p < 0.001) were observed. In contrast, clinically significant changes were observed on postoperative CT compared to baseline anthropometry: SKM − 4.1 ± 10.7%, VAT − 38.7 ± 30.2%, and SAT − 24.1 ± 22.6% (all p < 0.001) and these changes persisted at one year following PD. While anthropometric changes during preoperative therapy were not independently associated with survival, SKM gain between the postoperative period and one-year follow-up was associated with improved overall survival (OR 0.50, 95% CI 0.29–0.87).

Conclusions

In contrast to the minor changes that occur during preoperative therapy for PDAC, significant losses in key anthropometric parameters tend to occur over the first year following PD. Ongoing SKM loss in the postoperative period may represent an early marker for worse outcomes.

Keywords

Pancreatic ductal adenocarcinoma Body composition Neoadjuvant therapy Whipple Pancreatoduodenectomy Pancreatectomy 

Notes

Financial Support

This work was supported in part by the National Institutes of Health/National Cancer Institute under award number P30CA016672 (used the Clinical Trials Support Resource and the Biostatistics Resource Group). Additional support provided by the Knox Family fund.

Authors’ Contributions

All authors made substantial contributions to the

- conception or design of the work; or the acquisition, analysis, or interpretation of data for the work

- drafting the work or revising it critically for important intellectual content

- final approval of the version to be published

- agreement 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.

Compliance with Ethical Standards

The University of Texas MD Anderson Cancer Center’s (MDACC) institutional review board approved this retrospective study.

References

  1. 1.
    D. Li, K. Xie, R. Wolff, J.L. Abbruzzese, Pancreatic cancer, The Lancet. 363 (2004) 1049–1057.  https://doi.org/10.1016/S0140-6736(04)15841-8.CrossRefGoogle Scholar
  2. 2.
    L. Martin, L. Birdsell, N. Macdonald, T. Reiman, M.T. Clandinin, L.J. McCargar, R. Murphy, S. Ghosh, M.B. Sawyer, V.E. Baracos, Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index, J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 31 (2013) 1539–1547.  https://doi.org/10.1200/JCO.2012.45.2722.CrossRefGoogle Scholar
  3. 3.
    S. Levolger, J.L.A. van Vugt, R.W.F. de Bruin, J.N.M. IJzermans, Systematic review of sarcopenia in patients operated on for gastrointestinal and hepatopancreatobiliary malignancies, Br. J. Surg. 102 (2015) 1448–1458.  https://doi.org/10.1002/bjs.9893.CrossRefPubMedGoogle Scholar
  4. 4.
    Y. Choi, D.-Y. Oh, T.-Y. Kim, K.-H. Lee, S.-W. Han, S.-A. Im, T.-Y. Kim, Y.-J. Bang, Skeletal Muscle Depletion Predicts the Prognosis of Patients with Advanced Pancreatic Cancer Undergoing Palliative Chemotherapy, Independent of Body Mass Index, PloS One. 10 (2015) e0139749.  https://doi.org/10.1371/journal.pone.0139749.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    K.L. Mei, J.A. Batsis, J.B. Mills, S.D. Holubar, Sarcopenia and sarcopenic obesity: do they predict inferior oncologic outcomes after gastrointestinal cancer surgery?, Perioper. Med. Lond. Engl. 5 (2016) 30.  https://doi.org/10.1186/s13741-016-0052-1.CrossRefGoogle Scholar
  6. 6.
    S. Joglekar, A. Asghar, S.L. Mott, B.E. Johnson, A.M. Button, E. Clark, J.J. Mezhir, Sarcopenia is an independent predictor of complications following pancreatectomy for adenocarcinoma, J. Surg. Oncol. 111 (2015) 771–775.  https://doi.org/10.1002/jso.23862.CrossRefPubMedGoogle Scholar
  7. 7.
    K. Fearon, F. Strasser, S.D. Anker, I. Bosaeus, E. Bruera, R.L. Fainsinger, A. Jatoi, C. Loprinzi, N. MacDonald, G. Mantovani, M. Davis, M. Muscaritoli, F. Ottery, L. Radbruch, P. Ravasco, D. Walsh, A. Wilcock, S. Kaasa, V.E. Baracos, Definition and classification of cancer cachexia: an international consensus, Lancet Oncol. 12 (2011) 489–495.  https://doi.org/10.1016/S1470-2045(10)70218-7.CrossRefPubMedGoogle Scholar
  8. 8.
    A.B. Cooper, R. Slack, D. Fogelman, H.M. Holmes, M. Petzel, N. Parker, A. Balachandran, N. Garg, A. Ngo-Huang, G. Varadhachary, D.B. Evans, J.E. Lee, T. Aloia, C. Conrad, J.-N. Vauthey, J.B. Fleming, M.H.G. Katz, Characterization of Anthropometric Changes that Occur During Neoadjuvant Therapy for Potentially Resectable Pancreatic Cancer, Ann. Surg. Oncol. 22 (2015) 2416–2423.  https://doi.org/10.1245/s10434-014-4285-2.CrossRefPubMedGoogle Scholar
  9. 9.
    C. Yip, V. Goh, A. Davies, J. Gossage, R. Mitchell-Hay, O. Hynes, N. Maisey, P. Ross, A. Gaya, D.B. Landau, G.J. Cook, N. Griffin, R. Mason, Assessment of sarcopenia and changes in body composition after neoadjuvant chemotherapy and associations with clinical outcomes in oesophageal cancer, Eur. Radiol. 24 (2014) 998–1005.  https://doi.org/10.1007/s00330-014-3110-4.CrossRefPubMedGoogle Scholar
  10. 10.
    I.J.G. Rutten, D.P.J. van Dijk, R.F.P.M. Kruitwagen, R.G.H. Beets-Tan, S.W.M. Olde Damink, T. van Gorp, Loss of skeletal muscle during neoadjuvant chemotherapy is related to decreased survival in ovarian cancer patients, J. Cachexia Sarcopenia Muscle. 7 (2016) 458–466.  https://doi.org/10.1002/jcsm.12107.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    T. Akahori, M. Sho, S. Kinoshita, M. Nagai, S. Nishiwada, T. Tanaka, T. Tamamoto, C. Ohbayashi, M. Hasegawa, K. Kichikawa, Y. Nakajima, Prognostic Significance of Muscle Attenuation in Pancreatic Cancer Patients Treated with Neoadjuvant Chemoradiotherapy, World J. Surg. 39 (2015) 2975–2982.  https://doi.org/10.1007/s00268-015-3205-3.CrossRefPubMedGoogle Scholar
  12. 12.
    R.F. Hwang, H. Wang, A. Lara, H. Gomez, T. Chang, N. Sieffert, Y. Moon, S. Ram, S. Zimmerman, J.H. Lee, P.W.T. Pisters, E.P. Tamm, J.B. Fleming, J.L. Abbruzzese, D.B. Evans, Development of an integrated biospecimen bank and multidisciplinary clinical database for pancreatic cancer, Ann. Surg. Oncol. 15 (2008) 1356–1366.  https://doi.org/10.1245/s10434-008-9833-1.CrossRefPubMedGoogle Scholar
  13. 13.
    G.R. Varadhachary, E.P. Tamm, J.L. Abbruzzese, H.Q. Xiong, C.H. Crane, H. Wang, J.E. Lee, P.W.T. Pisters, D.B. Evans, R.A. Wolff, Borderline resectable pancreatic cancer: definitions, management, and role of preoperative therapy, Ann. Surg. Oncol. 13 (2006) 1035–1046.  https://doi.org/10.1245/ASO.2006.08.011.CrossRefPubMedGoogle Scholar
  14. 14.
    J.M. Cloyd, M.H.G. Katz, L. Prakash, G.R. Varadhachary, R.A. Wolff, R.T. Shroff, M. Javle, D. Fogelman, M. Overman, C.H. Crane, E.J. Koay, P. Das, S. Krishnan, B.D. Minsky, J.H. Lee, M.S. Bhutani, B. Weston, W. Ross, P. Bhosale, E.P. Tamm, H. Wang, A. Maitra, M.P. Kim, T.A. Aloia, J.-N. Vauthey, J.B. Fleming, J.L. Abbruzzese, P.W.T. Pisters, D.B. Evans, J.E. Lee, Preoperative Therapy and Pancreatoduodenectomy for Pancreatic Ductal Adenocarcinoma: a 25-Year Single-Institution Experience, J. Gastrointest. Surg. Off. J. Soc. Surg. Aliment. Tract. 21 (2017) 164–174.  https://doi.org/10.1007/s11605-016-3265-1.CrossRefGoogle Scholar
  15. 15.
    J.M. Cloyd, C.H. Crane, E.J. Koay, P. Das, S. Krishnan, L. Prakash, R.A. Snyder, G.R. Varadhachary, R.A. Wolff, M. Javle, R.T. Shroff, D. Fogelman, M. Overman, H. Wang, A. Maitra, J.E. Lee, J.B. Fleming, M.H.G. Katz, Impact of hypofractionated and standard fractionated chemoradiation before pancreatoduodenectomy for pancreatic ductal adenocarcinoma, Cancer. 122 (2016) 2671–2679.  https://doi.org/10.1002/cncr.30117.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    C.-W.D. Tzeng, J.B. Fleming, J.E. Lee, L. Xiao, P.W.T. Pisters, J.-N. Vauthey, E.K. Abdalla, R.A. Wolff, G.R. Varadhachary, D.R. Fogelman, C.H. Crane, A. Balachandran, M.H.G. Katz, Defined clinical classifications are associated with outcome of patients with anatomically resectable pancreatic adenocarcinoma treated with neoadjuvant therapy, Ann. Surg. Oncol. 19 (2012) 2045–2053.  https://doi.org/10.1245/s10434-011-2211-4.CrossRefPubMedGoogle Scholar
  17. 17.
    M.H.G. Katz, J.E. Lee, P.W.T. Pisters, R. Skoracki, E. Tamm, J.B. Fleming, Retroperitoneal Dissection in Patients with Borderline Resectable Pancreatic Cancer: Operative Principles and Techniques, J. Am. Coll. Surg. 215 (2012) e11–e18.  https://doi.org/10.1016/j.jamcollsurg.2012.05.015.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    C.-W.D. Tzeng, J.B. Fleming, J.E. Lee, X. Wang, P.W.T. Pisters, J.-N. Vauthey, G. Varadhachary, R.A. Wolff, M.H.G. Katz, Yield of clinical and radiographic surveillance in patients with resected pancreatic adenocarcinoma following multimodal therapy, HPB. 14 (2012) 365–372.  https://doi.org/10.1111/j.1477-2574.2012.00445.x.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    M. Mourtzakis, C.M.M. Prado, J.R. Lieffers, T. Reiman, L.J. McCargar, V.E. Baracos, 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. Physiol. Appl. Nutr. Metab. 33 (2008) 997–1006.  https://doi.org/10.1139/H08-075.CrossRefGoogle Scholar
  20. 20.
    J.M. Cloyd, H. Wang, M.E. Egger, C.-W.D. Tzeng, L.R. Prakash, A. Maitra, G.R. Varadhachary, R. Shroff, M. Javle, D. Fogelman, R.A. Wolff, M.J. Overman, E.J. Koay, P. Das, J.M. Herman, M.P. Kim, J.-N. Vauthey, T.A. Aloia, J.B. Fleming, J.E. Lee, M.H.G. Katz, Association of Clinical Factors With a Major Pathologic Response Following Preoperative Therapy for Pancreatic Ductal Adenocarcinoma. JAMA Surg. (2017) Nov 1;152(11):1048–1056.Google Scholar
  21. 21.
    J.K. Onesti, G.P. Wright, S.E. Kenning, M.T. Tierney, A.T. Davis, M.G. Doherty, M.H. Chung, Sarcopenia and survival in patients undergoing pancreatic resection, Pancreatol. Off. J. Int. Assoc. Pancreatol. IAP Al. 16 (2016) 284–289.  https://doi.org/10.1016/j.pan.2016.01.009.CrossRefGoogle Scholar
  22. 22.
    N. Pecorelli, G. Carrara, F. De Cobelli, G. Cristel, A. Damascelli, G. Balzano, L. Beretta, M. Braga, Effect of sarcopenia and visceral obesity on mortality and pancreatic fistula following pancreatic cancer surgery, Br. J. Surg. 103 (2016) 434–442.  https://doi.org/10.1002/bjs.10063.CrossRefPubMedGoogle Scholar
  23. 23.
    N. Amini, G. Spolverato, R. Gupta, G.A. Margonis, Y. Kim, D. Wagner, N. Rezaee, M.J. Weiss, C.L. Wolfgang, M.M. Makary, I.R. Kamel, T.M. Pawlik, 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. Off. J. Soc. Surg. Aliment. Tract. 19 (2015) 1593–1602.  https://doi.org/10.1007/s11605-015-2835-y.CrossRefGoogle Scholar
  24. 24.
    A.J. Benjamin, M.M. Buschmann, A. Schneider, B.A. Derstine, J.F. Friedman, S.C. Wang, W. Dale, K.K. Roggin, Can Comprehensive Imaging Analysis with Analytic Morphomics and Geriatric Assessment Predict Serious Complications in Patients Undergoing Pancreatic Surgery?, J. Gastrointest. Surg. Off. J. Soc. Surg. Aliment. Tract. 21 (2017) 1009–1016.  https://doi.org/10.1007/s11605-017-3392-3.CrossRefGoogle Scholar
  25. 25.
    M.D. Sur, J.P. Namm, J.A. Hemmerich, M.M. Buschmann, K.K. Roggin, W. Dale, Radiographic Sarcopenia and Self-reported Exhaustion Independently Predict NSQIP Serious Complications After Pancreaticoduodenectomy in Older Adults, Ann. Surg. Oncol. 22 (2015) 3897–3904.  https://doi.org/10.1245/s10434-015-4763-1.CrossRefPubMedGoogle Scholar
  26. 26.
    S. Buettner, D. Wagner, Y. Kim, G.A. Margonis, M.A. Makary, A. Wilson, K. Sasaki, N. Amini, F. Gani, T.M. Pawlik, Inclusion of Sarcopenia Outperforms the Modified Frailty Index in Predicting 1-Year Mortality among 1,326 Patients Undergoing Gastrointestinal Surgery for a Malignant Indication, J. Am. Coll. Surg. 222 (2016) 397–407.e2.  https://doi.org/10.1016/j.jamcollsurg.2015.12.020.CrossRefPubMedGoogle Scholar
  27. 27.
    P. Peng, O. Hyder, A. Firoozmand, P. Kneuertz, R.D. Schulick, D. Huang, M. Makary, K. Hirose, B. Edil, M.A. Choti, J. Herman, J.L. Cameron, C.L. Wolfgang, T.M. Pawlik, Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma, J. Gastrointest. Surg. Off. J. Soc. Surg. Aliment. Tract. 16 (2012) 1478–1486.  https://doi.org/10.1007/s11605-012-1923-5.CrossRefGoogle Scholar
  28. 28.
    K. Jaap, M. Hunsinger, J. Dove, K. McGinty, E. Stefanowicz, J. Fera, J. Wild, M. Shabahang, J. Blansfield, Morphometric Predictors of Morbidity after Pancreatectomy, Am. Surg. 82 (2016) 1221–1226.PubMedGoogle Scholar
  29. 29.
    A. Aslani, P.J. Roach, R.C. Smith, Long-term changes in body composition after pancreaticoduodenectomy, ANZ J. Surg. 82 (2012) 173–178.  https://doi.org/10.1111/j.1445-2197.2011.05970.x.CrossRefPubMedGoogle Scholar
  30. 30.
    F.T. Curran, M.A. Stokes, G.L. Hill, Long-term changes in body composition after pancreatoduodenectomy, J. R. Coll. Surg. Edinb. 36 (1991) 32–34.PubMedGoogle Scholar
  31. 31.
    D. Royall, K.N. Jeejeebhoy, B. O’Connor, B.R. Taylor, B. Langer, R.S. McLeod, Nutritional status and function in patients following Whipple procedure compared with controls, J. Am. Coll. Nutr. 15 (1996) 73–78.CrossRefPubMedGoogle Scholar
  32. 32.
    J.-Y. Jang, S.-W. Kim, S.-J. Park, Y.-H. Park, Comparison of the functional outcome after pylorus-preserving pancreatoduodenectomy: pancreatogastrostomy and pancreatojejunostomy, World J. Surg. 26 (2002) 366–371.  https://doi.org/10.1007/s00268-001-0234-x.CrossRefPubMedGoogle Scholar
  33. 33.
    D. Hashimoto, A. Chikamoto, M. Ohmuraya, S. Abe, S. Nakagawa, T. Beppu, H. Takamori, M. Hirota, H. Baba, Impact of Postoperative Weight Loss on Survival After Resection for Pancreatic Cancer, JPEN J. Parenter. Enteral Nutr. 39 (2015) 598–603.  https://doi.org/10.1177/0148607114520992.CrossRefPubMedGoogle Scholar
  34. 34.
    H.J. Andreyev, A.R. Norman, J. Oates, D. Cunningham, Why do patients with weight loss have a worse outcome when undergoing chemotherapy for gastrointestinal malignancies?, Eur. J. Cancer Oxf. Engl. 1990. 34 (1998) 503–509.CrossRefGoogle Scholar
  35. 35.
    S.E. Lee, J.H. Lee, K.W. Ryu, B. Nam, C.G. Kim, S.R. Park, M.-C. Kook, Y.-W. Kim, Changing pattern of postoperative body weight and its association with recurrence and survival after curative resection for gastric cancer, Hepatogastroenterology. 59 (2012) 430–435.  https://doi.org/10.5754/hge09218.CrossRefPubMedGoogle Scholar
  36. 36.
    J.L. Davis, L.V. Selby, J.F. Chou, M. Schattner, D.H. Ilson, M. Capanu, M.F. Brennan, D.G. Coit, V.E. Strong, Patterns and Predictors of Weight Loss After Gastrectomy for Cancer, Ann. Surg. Oncol. 23 (2016) 1639–1645.  https://doi.org/10.1245/s10434-015-5065-3.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    X.B. D’Journo, M. Ouattara, A. Loundou, D. Trousse, L. Dahan, T. Nathalie, C. Doddoli, J.F. Seitz, P.-A. Thomas, Prognostic impact of weight loss in 1-year survivors after transthoracic esophagectomy for cancer, Dis. Esophagus Off. J. Int. Soc. Dis. Esophagus. 25 (2012) 527–534.  https://doi.org/10.1111/j.1442-2050.2011.01282.x.CrossRefGoogle Scholar
  38. 38.
    J. Moran, E. Guinan, P. McCormick, J. Larkin, D. Mockler, J. Hussey, J. Moriarty, F. Wilson, The ability of prehabilitation to influence postoperative outcome after intra-abdominal operation: A systematic review and meta-analysis. Surgery. (2016).  https://doi.org/10.1016/j.surg.2016.05.014.
  39. 39.
    D.R. Fogelman, H. Holmes, K. Mohammed, M.H.G. Katz, C.M. Prado, J. Lieffers, N. Garg, G.R. Varadhachary, R. Shroff, M.J. Overman, C. Garrett, R.A. Wolff, M. Javle, Does IGFR1 inhibition result in increased muscle mass loss in patients undergoing treatment for pancreatic cancer?, J. Cachexia Sarcopenia Muscle. 5 (2014) 307–313.  https://doi.org/10.1007/s13539-014-0145-y.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    M. Barret, S. Antoun, C. Dalban, D. Malka, T. Mansourbakht, A. Zaanan, E. Latko, J. Taieb, Sarcopenia is linked to treatment toxicity in patients with metastatic colorectal cancer, Nutr. Cancer. 66 (2014) 583–589.  https://doi.org/10.1080/01635581.2014.894103.CrossRefPubMedGoogle Scholar
  41. 41.
    A. Ngo-Huang, N. Parker, V.A. Martinez, M.Q. Petzel, D. Fogelman, H.M. Holmes, S.S. Dhah, M. Katz, Poster 68 Feasibility of a Prehabilitation Program for Patients with Potentially Resectable Pancreatic Cancer: Pilot Study, PM R. 8 (2016) S183.  https://doi.org/10.1016/j.pmrj.2016.07.111.CrossRefPubMedGoogle Scholar
  42. 42.
    C. Afaneh, D. Gerszberg, E. Slattery, D.S. Seres, J.A. Chabot, M.D. Kluger, Pancreatic cancer surgery and nutrition management: a review of the current literature, Hepatobiliary Surg. Nutr. 4 (2015) 59–71.  https://doi.org/10.3978/j.issn.2304-3881.2014.08.07.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Y. Miyamoto, D.L. Hanna, W. Zhang, H. Baba, H.-J. Lenz, Molecular Pathways: Cachexia Signaling-A Targeted Approach to Cancer Treatment, Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 22 (2016) 3999–4004.  https://doi.org/10.1158/1078-0432.CCR-16-0495.CrossRefGoogle Scholar
  44. 44.
    T.P. Yeo, S.A. Burrell, P.K. Sauter, E.P. Kennedy, H. Lavu, B.E. Leiby, C.J. Yeo, A progressive postresection walking program significantly improves fatigue and health-related quality of life in pancreas and periampullary cancer patients, J. Am. Coll. Surg. 214 (2012) 463–475; discussion 475-477.  https://doi.org/10.1016/j.jamcollsurg.2011.12.017.CrossRefPubMedGoogle Scholar
  45. 45.
    S. Okumura, T. Kaido, Y. Hamaguchi, Y. Fujimoto, T. Masui, M. Mizumoto, A. Hammad, A. Mori, K. Takaori, S. Uemoto, Impact of preoperative quality as well as quantity of skeletal muscle on survival after resection of pancreatic cancer, Surgery. 157 (2015) 1088–1098.  https://doi.org/10.1016/j.surg.2015.02.002.CrossRefPubMedGoogle Scholar
  46. 46.
    S. Taguchi, N. Akamatsu, T. Nakagawa, W. Gonoi, A. Kanatani, H. Miyazaki, T. Fujimura, H. Fukuhara, H. Kume, Y. Homma, Sarcopenia Evaluated Using the Skeletal Muscle Index Is a Significant Prognostic Factor for Metastatic Urothelial Carcinoma, Clin. Genitourin. Cancer. 14 (2016) 237–243.  https://doi.org/10.1016/j.clgc.2015.07.015.CrossRefPubMedGoogle Scholar
  47. 47.
    L. Ebbeling, D.J. Grabo, M. Shashaty, R. Dua, S.S. Sonnad, C.A. Sims, J.L. Pascual, C.W. Schwab, D.N. Holena, Psoas:lumbar vertebra index: central sarcopenia independently predicts morbidity in elderly trauma patients, Eur. J. Trauma Emerg. Surg. Off. Publ. Eur. Trauma Soc. 40 (2014) 57–65.  https://doi.org/10.1007/s00068-013-0313-3.CrossRefGoogle Scholar
  48. 48.
    M.J. Englesbe, J.S. Lee, K. He, L. Fan, D.E. Schaubel, K.H. Sheetz, C.M. Harbaugh, S.A. Holcombe, D.A. Campbell, C.J. Sonnenday, S.C. Wang, Analytic morphomics, core muscle size, and surgical outcomes, Ann. Surg. 256 (2012) 255–261.  https://doi.org/10.1097/SLA.0b013e31826028b1.CrossRefPubMedGoogle Scholar
  49. 49.
    A.J. Cruz-Jentoft, J.P. Baeyens, J.M. Bauer, Y. Boirie, T. Cederholm, F. Landi, F.C. Martin, J.-P. Michel, Y. Rolland, S.M. Schneider, E. Topinková, M. Vandewoude, M. Zamboni, European Working Group on Sarcopenia in Older People, Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People, Age Ageing. 39 (2010) 412–423.  https://doi.org/10.1093/ageing/afq034.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    M. Muscaritoli, S.D. Anker, J. Argilés, Z. Aversa, J.M. Bauer, G. Biolo, Y. Boirie, I. Bosaeus, T. Cederholm, P. Costelli, K.C. Fearon, A. Laviano, M. Maggio, F. Rossi Fanelli, S.M. Schneider, A. Schols, C.C. Sieber, Consensus definition of sarcopenia, cachexia and pre-cachexia: joint document elaborated by Special Interest Groups (SIG) “cachexia-anorexia in chronic wasting diseases” and “nutrition in geriatrics,” Clin. Nutr. Edinb. Scotl. 29 (2010) 154–159.  https://doi.org/10.1016/j.clnu.2009.12.004.CrossRefGoogle Scholar
  51. 51.
    R.A. Fielding, B. Vellas, W.J. Evans, S. Bhasin, J.E. Morley, A.B. Newman, G. Abellan van Kan, S. Andrieu, J. Bauer, D. Breuille, T. Cederholm, J. Chandler, C. De Meynard, L. Donini, T. Harris, A. Kannt, F. Keime Guibert, G. Onder, D. Papanicolaou, Y. Rolland, D. Rooks, C. Sieber, E. Souhami, S. Verlaan, M. Zamboni, Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia, J. Am. Med. Dir. Assoc. 12 (2011) 249–256.  https://doi.org/10.1016/j.jamda.2011.01.003.CrossRefPubMedGoogle Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2017

Authors and Affiliations

  • Jordan M. Cloyd
    • 1
  • Graciela M. Nogueras-González
    • 2
  • Laura R. Prakash
    • 1
  • Maria Q. B. Petzel
    • 1
  • Nathan H. Parker
    • 1
  • An T. Ngo-Huang
    • 3
  • David Fogelman
    • 4
  • Jason W. Denbo
    • 1
  • Naveen Garg
    • 5
  • Michael P. Kim
    • 1
  • Jeffrey E. Lee
    • 1
  • Ching-Wei D. Tzeng
    • 1
  • Jason B. Fleming
    • 1
  • Matthew H. G. Katz
    • 1
  1. 1.Department of Surgical OncologyThe University of Texas MD Anderson Cancer CenterHoustonUSA
  2. 2.Department of BiostatisticsThe University of Texas MD Anderson Cancer CenterHoustonUSA
  3. 3.Department of Palliative, Rehabilitation and Integrative MedicineThe University of Texas MD Anderson Cancer CenterHoustonUSA
  4. 4.Department of Gastrointestinal Medical OncologyThe University of Texas MD Anderson Cancer CenterHoustonUSA
  5. 5.Department of Diagnostic ImagingThe University of Texas MD Anderson Cancer CenterHoustonUSA

Personalised recommendations