Skip to main content
Top
Published in: Annals of Surgical Oncology 1/2017

Open Access 01-01-2017 | Pancreatic Tumors

Skeletal Muscle Quality is Associated with Worse Survival After Pancreatoduodenectomy for Periampullary, Nonpancreatic Cancer

Authors: L. B. Van Rijssen, MD, N. C. M. van Huijgevoort, MD, R. J. S. Coelen, MD, J. A. Tol, MD, PhD, E. B. Haverkort, MSc, PhD, C. Y. Nio, MD, O. R. Busch, MD, PhD, M. G. Besselink, MD, MSc, PhD

Published in: Annals of Surgical Oncology | Issue 1/2017

Login to get access

Abstract

Background

Body composition measures may predict outcomes of cancer surgery. Whereas low muscle mass shown on preoperative computed tomography (CT) scans has been associated with worse outcomes after surgery for pancreatic cancer, less consideration has been given to low muscle attenuation, reflecting poor muscle quality. Studies relating muscle mass and muscle attenuation with outcomes for patients with periampullary, nonpancreatic cancer are lacking.

Methods

Skeletal muscle mass and attenuation were assessed in 166 consecutive patients undergoing pancreatoduodenectomy (PD) for periampullary, nonpancreatic cancer at a single center between 2000 and 2012. The skeletal muscle index (SMI) was calculated from cross-sectional muscle area on preoperative CT imaging at the third lumbar vertebra level (L3) and normalized for height. The skeletal muscle attenuation index (MAI) was calculated by measuring the average Hounsfield units of the total muscle area at the L3 level. Overall survival (OS) and the rate of major postoperative complications (Clavien-Dindo ≥3) were extracted from prospectively maintained databases.

Results

Low SMI was present in 78.3 % and low MAI in 48.8 % of the patients. The multivariate analysis showed lymph node metastasis [hazard ratio (HR) 1.8; 95 % confidence interval (CI) 1.1–2.9], microscopic radicality (HR 2.0; 95 % CI 1.2–3.4), and low MAI (HR 2.0; 95 % CI 1.2–3.3), but not low SMI to be significantly associated with decreased OS. Low MAI (HR 1.9; 95 % CI 1.0–3.8) was the only independent risk factor for major postoperative complications.

Conclusion

Skeletal muscle quality, but not muscle mass, predicted survival and major complications after PD for periampullary, nonpancreatic cancer. Preoperative CT-derived body composition measures may stratify patients into risk categories and support shared decision making.
Appendix
Available only for authorised users
Literature
1.
go back to reference Prado CM, Lieffers JR, McCargar LJ, 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;9:629–35.CrossRefPubMed Prado CM, Lieffers JR, McCargar LJ, 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;9:629–35.CrossRefPubMed
2.
go back to reference Levolger S, van Vugt JL, de Bruin RW, JN IJ. Systematic review of sarcopenia in patients operated on for gastrointestinal and hepatopancreatobiliary malignancies. Br J Surg. 2015;102:1448–58.CrossRefPubMed Levolger S, van Vugt JL, de Bruin RW, JN IJ. Systematic review of sarcopenia in patients operated on for gastrointestinal and hepatopancreatobiliary malignancies. Br J Surg. 2015;102:1448–58.CrossRefPubMed
3.
go back to reference Peng P, Hyder O, Firoozmand A, et al. Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma. J Gastrointest Surg. 2012;16:1478–86.CrossRefPubMedPubMedCentral Peng P, Hyder O, Firoozmand A, et al. Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma. J Gastrointest Surg. 2012;16:1478–86.CrossRefPubMedPubMedCentral
4.
go back to reference Okumura S, Kaido T, Hamaguchi Y, et al. Impact of preoperative quality as well as quantity of skeletal muscle on survival after resection of pancreatic cancer. Surgery. 2015;157:1088–98.CrossRefPubMed Okumura S, Kaido T, Hamaguchi Y, et al. Impact of preoperative quality as well as quantity of skeletal muscle on survival after resection of pancreatic cancer. Surgery. 2015;157:1088–98.CrossRefPubMed
5.
go back to reference Sur MD, Namm JP, Hemmerich JA, Buschmann MM, Roggin KK, Dale W. Radiographic sarcopenia and self-reported exhaustion independently predict NSQIP serious complications after pancreaticoduodenectomy in older adults. Ann Surg Oncol. 2015;22:3897–904.CrossRefPubMed Sur MD, Namm JP, Hemmerich JA, Buschmann MM, Roggin KK, Dale W. Radiographic sarcopenia and self-reported exhaustion independently predict NSQIP serious complications after pancreaticoduodenectomy in older adults. Ann Surg Oncol. 2015;22:3897–904.CrossRefPubMed
6.
go back to reference Amini N, Spolverato G, Gupta R, et al. 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. 2015;19:1593–602.CrossRefPubMedPubMedCentral Amini N, Spolverato G, Gupta R, et al. 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. 2015;19:1593–602.CrossRefPubMedPubMedCentral
7.
go back to reference Martin L, Birdsell L, Macdonald N, et al. Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J Clin Oncol. 2013;31:1539–47.CrossRefPubMed Martin L, Birdsell L, Macdonald N, et al. Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J Clin Oncol. 2013;31:1539–47.CrossRefPubMed
8.
go back to reference Sabel MS, Lee J, Cai S, Englesbe MJ, Holcombe S, Wang S. Sarcopenia as a prognostic factor among patients with stage III melanoma. Ann Surg Oncol. 2011;18:3579–85.CrossRefPubMed Sabel MS, Lee J, Cai S, Englesbe MJ, Holcombe S, Wang S. Sarcopenia as a prognostic factor among patients with stage III melanoma. Ann Surg Oncol. 2011;18:3579–85.CrossRefPubMed
9.
go back to reference Antoun S, Lanoy E, Iacovelli R, et al. Skeletal muscle density predicts prognosis in patients with metastatic renal cell carcinoma treated with targeted therapies. Cancer. 2013;119:3377–84.CrossRefPubMed Antoun S, Lanoy E, Iacovelli R, et al. Skeletal muscle density predicts prognosis in patients with metastatic renal cell carcinoma treated with targeted therapies. Cancer. 2013;119:3377–84.CrossRefPubMed
10.
go back to reference Wagner D, Buttner S, Kim Y, et al. Clinical and morphometric parameters of frailty for prediction of mortality following hepatopancreaticobiliary surgery in the elderly. Br J Surg. 2016;103:e83–92.CrossRefPubMed Wagner D, Buttner S, Kim Y, et al. Clinical and morphometric parameters of frailty for prediction of mortality following hepatopancreaticobiliary surgery in the elderly. Br J Surg. 2016;103:e83–92.CrossRefPubMed
11.
go back to reference Goodpaster BH, Park SW, Harris TB, et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging, and body composition study. J Gerontol A Biol Sci Med Sci. 2006;61:1059–64.CrossRefPubMed Goodpaster BH, Park SW, Harris TB, et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging, and body composition study. J Gerontol A Biol Sci Med Sci. 2006;61:1059–64.CrossRefPubMed
12.
go back to reference Newman AB, Kupelian V, Visser M, et al. Strength, but not muscle mass, is associated with mortality in the health, aging, and body composition study cohort. J Gerontol A Biol Sci Med Sci. 2006;61:72–7.CrossRefPubMed Newman AB, Kupelian V, Visser M, et al. Strength, but not muscle mass, is associated with mortality in the health, aging, and body composition study cohort. J Gerontol A Biol Sci Med Sci. 2006;61:72–7.CrossRefPubMed
13.
go back to reference Aubrey J, Esfandiari N, Baracos VE, et al. Measurement of skeletal muscle radiation attenuation and basis of its biological variation. Acta Physiol Oxford. 2014;210:489–97.CrossRefPubMedPubMedCentral Aubrey J, Esfandiari N, Baracos VE, et al. Measurement of skeletal muscle radiation attenuation and basis of its biological variation. Acta Physiol Oxford. 2014;210:489–97.CrossRefPubMedPubMedCentral
14.
go back to reference Marcus RL, Addison O, Kidde JP, Dibble LE, Lastayo PC. Skeletal muscle fat infiltration: impact of age, inactivity, and exercise. J Nutr Health Aging. 2010;14:362–6.CrossRefPubMedPubMedCentral Marcus RL, Addison O, Kidde JP, Dibble LE, Lastayo PC. Skeletal muscle fat infiltration: impact of age, inactivity, and exercise. J Nutr Health Aging. 2010;14:362–6.CrossRefPubMedPubMedCentral
15.
go back to reference Cameron JL, He J. Two thousand consecutive pancreaticoduodenectomies. J Am Coll Surg. 2015;220:530–6.CrossRefPubMed Cameron JL, He J. Two thousand consecutive pancreaticoduodenectomies. J Am Coll Surg. 2015;220:530–6.CrossRefPubMed
16.
go back to reference Tol JA, Brosens LA, van Dieren S, et al. Impact of lymph node ratio on survival in patients with pancreatic and periampullary cancer. Br J Surg. 2015;102:237–45.CrossRefPubMed Tol JA, Brosens LA, van Dieren S, et al. Impact of lymph node ratio on survival in patients with pancreatic and periampullary cancer. Br J Surg. 2015;102:237–45.CrossRefPubMed
17.
go back to reference Bassi C, Dervenis C, Butturini G, et al. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery. 2005;138:8–13.CrossRefPubMed Bassi C, Dervenis C, Butturini G, et al. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery. 2005;138:8–13.CrossRefPubMed
18.
go back to reference Clavien PA, Barkun J, de Oliveira ML, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250:187–96.CrossRefPubMed Clavien PA, Barkun J, de Oliveira ML, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250:187–96.CrossRefPubMed
19.
go back to reference Wente MN, Bassi C, Dervenis C, et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery. 2007;142:761–8.CrossRefPubMed Wente MN, Bassi C, Dervenis C, et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery. 2007;142:761–8.CrossRefPubMed
20.
go back to reference Wente MN, Veit JA, Bassi C, et al. Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery. 2007;142:20–5.CrossRefPubMed Wente MN, Veit JA, Bassi C, et al. Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery. 2007;142:20–5.CrossRefPubMed
21.
go back to reference van Vledder MG, Levolger S, Ayez N, Verhoef C, Tran TC, Ijzermans JN. Body composition and outcome in patients undergoing resection of colorectal liver metastases. Br J Surg. 2012;99:550–7.CrossRefPubMed van Vledder MG, Levolger S, Ayez N, Verhoef C, Tran TC, Ijzermans JN. Body composition and outcome in patients undergoing resection of colorectal liver metastases. Br J Surg. 2012;99:550–7.CrossRefPubMed
22.
go back to reference Coelen RJ, Wiggers JK, Nio CY, et al. Preoperative computed tomography assessment of skeletal muscle mass is valuable in predicting outcomes following hepatectomy for perihilar cholangiocarcinoma. HPB Oxford. 2015;17:520–8.CrossRefPubMedPubMedCentral Coelen RJ, Wiggers JK, Nio CY, et al. Preoperative computed tomography assessment of skeletal muscle mass is valuable in predicting outcomes following hepatectomy for perihilar cholangiocarcinoma. HPB Oxford. 2015;17:520–8.CrossRefPubMedPubMedCentral
23.
go back to reference Paniccia A, Hosokawa P, Henderson W, et al. Characteristics of 10-year survivors of pancreatic ductal adenocarcinoma. JAMA Surg. 2015;150:701–10.CrossRefPubMed Paniccia A, Hosokawa P, Henderson W, et al. Characteristics of 10-year survivors of pancreatic ductal adenocarcinoma. JAMA Surg. 2015;150:701–10.CrossRefPubMed
24.
go back to reference Bouvet M, Gamagami RA, Gilpin EA, et al. Factors influencing survival after resection for periampullary neoplasms. Am J Surg. 2000;180:13–7.CrossRefPubMed Bouvet M, Gamagami RA, Gilpin EA, et al. Factors influencing survival after resection for periampullary neoplasms. Am J Surg. 2000;180:13–7.CrossRefPubMed
25.
26.
go back to reference Nitecki SS, Sarr MG, Colby TV, van Heerden JA. Long-term survival after resection for ductal adenocarcinoma of the pancreas: is it really improving? Ann Surg. 1995;221:59–66.CrossRefPubMedPubMedCentral Nitecki SS, Sarr MG, Colby TV, van Heerden JA. Long-term survival after resection for ductal adenocarcinoma of the pancreas: is it really improving? Ann Surg. 1995;221:59–66.CrossRefPubMedPubMedCentral
27.
go back to reference Hatzaras I, George N, Muscarella P, Melvin WS, Ellison EC, Bloomston M. Predictors of survival in periampullary cancers following pancreaticoduodenectomy. Ann Surg Oncol. 2010;17:991–7.CrossRefPubMedPubMedCentral Hatzaras I, George N, Muscarella P, Melvin WS, Ellison EC, Bloomston M. Predictors of survival in periampullary cancers following pancreaticoduodenectomy. Ann Surg Oncol. 2010;17:991–7.CrossRefPubMedPubMedCentral
28.
go back to reference Roberts KJ, Sutcliffe RP, Marudanayagam R, et al. Scoring system to predict pancreatic fistula after pancreaticoduodenectomy: a UK multicenter study. Ann Surg. 2015;261:1191–7.CrossRefPubMed Roberts KJ, Sutcliffe RP, Marudanayagam R, et al. Scoring system to predict pancreatic fistula after pancreaticoduodenectomy: a UK multicenter study. Ann Surg. 2015;261:1191–7.CrossRefPubMed
29.
go back to reference Goodpaster BH, Chomentowski P, Ward BK, et al. Effects of physical activity on strength and skeletal muscle fat infiltration in older adults: a randomized controlled trial. J Appl Physiol. (1985) 2008;105:1498–503. Goodpaster BH, Chomentowski P, Ward BK, et al. Effects of physical activity on strength and skeletal muscle fat infiltration in older adults: a randomized controlled trial. J Appl Physiol. (1985) 2008;105:1498–503.
30.
go back to reference Santa Mina D, Clarke H, Ritvo P, et al. Effect of total-body prehabilitation on postoperative outcomes: a systematic review and meta-analysis. Physiotherapy. 2014;100:196–207.CrossRefPubMed Santa Mina D, Clarke H, Ritvo P, et al. Effect of total-body prehabilitation on postoperative outcomes: a systematic review and meta-analysis. Physiotherapy. 2014;100:196–207.CrossRefPubMed
31.
go back to reference Callery MP, Pratt WB, Kent TS, Chaikof EL, Vollmer CM Jr. A prospectively validated clinical risk score accurately predicts pancreatic fistula after pancreatoduodenectomy. J Am Coll Surg. 2013;216:1–14.CrossRefPubMed Callery MP, Pratt WB, Kent TS, Chaikof EL, Vollmer CM Jr. A prospectively validated clinical risk score accurately predicts pancreatic fistula after pancreatoduodenectomy. J Am Coll Surg. 2013;216:1–14.CrossRefPubMed
32.
go back to reference Miller BC, Christein JD, Behrman SW, et al. A multi-institutional external validation of the fistula risk score for pancreatoduodenectomy. J Gastrointest Surg. 2014;18:172–79.CrossRefPubMed Miller BC, Christein JD, Behrman SW, et al. A multi-institutional external validation of the fistula risk score for pancreatoduodenectomy. J Gastrointest Surg. 2014;18:172–79.CrossRefPubMed
33.
go back to reference Glant JA, Waters JA, House MG, et al. Does the interval from imaging to operation affect the rate of unanticipated metastasis encountered during operation for pancreatic adenocarcinoma? Surgery. 2011;150:607–16.CrossRefPubMed Glant JA, Waters JA, House MG, et al. Does the interval from imaging to operation affect the rate of unanticipated metastasis encountered during operation for pancreatic adenocarcinoma? Surgery. 2011;150:607–16.CrossRefPubMed
Metadata
Title
Skeletal Muscle Quality is Associated with Worse Survival After Pancreatoduodenectomy for Periampullary, Nonpancreatic Cancer
Authors
L. B. Van Rijssen, MD
N. C. M. van Huijgevoort, MD
R. J. S. Coelen, MD
J. A. Tol, MD, PhD
E. B. Haverkort, MSc, PhD
C. Y. Nio, MD
O. R. Busch, MD, PhD
M. G. Besselink, MD, MSc, PhD
Publication date
01-01-2017
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 1/2017
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-016-5495-6

Other articles of this Issue 1/2017

Annals of Surgical Oncology 1/2017 Go to the issue