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Published in: Gastric Cancer 2/2015

01-04-2015 | Original Article

Skeletal muscle loss after total gastrectomy, exacerbated by adjuvant chemotherapy

Authors: Yusuke Yamaoka, Kazumasa Fujitani, Toshimasa Tsujinaka, Kazuyoshi Yamamoto, Motohiro Hirao, Mitsugu Sekimoto

Published in: Gastric Cancer | Issue 2/2015

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Abstract

Background

Skeletal muscle loss is associated with physical disability, nosocomial infections, postoperative complications, and decreased survival. Preventing the loss of skeletal muscle mass after gastrectomy may lead to improved outcomes. The aims of this study were to assess changes in skeletal muscle mass after total gastrectomy (TG) and to clarify the clinical factors affecting significant loss of skeletal muscle after TG.

Patients and methods

One hundred and two patients undergoing TG for primary gastric cancer underwent abdominal computed tomography before and 1 year after TG to precisely quantify postoperative changes in skeletal muscle and adipose tissue. Univariate and multivariate logistic regression analyses identified clinical factors contributing to significant loss of skeletal muscle after TG.

Results

At 1 year after TG, the mass of both skeletal muscle and adipose tissue was reduced by 6.20 ± 6.80 and 65.8 ± 36.1 % of the preoperative values, respectively, and 26 patients (25.5 %) showed a significant loss of skeletal muscle of more than 10 %. Adjuvant chemotherapy with S-1 for ≥6 months (hazard ratio 26.61, 95 % confidence interval, 3.487–203.1) was identified as the single independent risk factor for a significant loss of skeletal muscle.

Conclusions

Skeletal muscle loss was exacerbated by extended adjuvant chemotherapy after TG. Further research should identify appropriate nutritional interventions for maintaining skeletal muscle mass and leading to improved outcomes.
Literature
1.
go back to reference Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147:755–63.CrossRefPubMed Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147:755–63.CrossRefPubMed
2.
go back to reference Lang T, Streeper T, Cawthon P, Baldwin K, Taaffe DR, Harris TB. Sarcopenia: etiology, clinical consequences, intervention, and assessment. Osteoporos Int. 2010;21:543–59.CrossRefPubMedCentralPubMed Lang T, Streeper T, Cawthon P, Baldwin K, Taaffe DR, Harris TB. Sarcopenia: etiology, clinical consequences, intervention, and assessment. Osteoporos Int. 2010;21:543–59.CrossRefPubMedCentralPubMed
3.
go back to reference Cosquéric G, Sebag A, Ducolombier C, Thomas C, Piette F, Weill-Engerer S. Sarcopenia is predictive of nosocomial infection in care of the elderly. Br J Nutr. 2006;96:895–901.CrossRefPubMed Cosquéric G, Sebag A, Ducolombier C, Thomas C, Piette F, Weill-Engerer S. Sarcopenia is predictive of nosocomial infection in care of the elderly. Br J Nutr. 2006;96:895–901.CrossRefPubMed
4.
go back to reference Englesbe MJ, Patel SP, He K, Lynch RJ, Schaubel DE, Harbaugh C, et al. Sarcopenia and mortality after liver transplantation. J Am Coll Surg. 2010;211:271–8.CrossRefPubMedCentralPubMed Englesbe MJ, Patel SP, He K, Lynch RJ, Schaubel DE, Harbaugh C, et al. Sarcopenia and mortality after liver transplantation. J Am Coll Surg. 2010;211:271–8.CrossRefPubMedCentralPubMed
5.
go back to reference Lee JS, He K, Harbaugh CM, Schaubel DE, Sonnenday CJ, Wang SC, et al. Frailty, core muscle size, and mortality in patients undergoing open abdominal aortic aneurysm repair. J Vasc Surg. 2011;53:912–7.CrossRefPubMed Lee JS, He K, Harbaugh CM, Schaubel DE, Sonnenday CJ, Wang SC, et al. Frailty, core muscle size, and mortality in patients undergoing open abdominal aortic aneurysm repair. J Vasc Surg. 2011;53:912–7.CrossRefPubMed
6.
go back to reference Englesbe MJ, Lee JS, He K, Fan L, Schaubel DE, Sheetz KH, et al. Analytic morphomics, core muscle size, and surgical outcomes. Ann Surg. 2012;256:255–61.CrossRefPubMed Englesbe MJ, Lee JS, He K, Fan L, Schaubel DE, Sheetz KH, et al. Analytic morphomics, core muscle size, and surgical outcomes. Ann Surg. 2012;256:255–61.CrossRefPubMed
7.
go back to reference Lieffers JR, Bathe OF, Fassbender K, Winget M, Baracos VE. Sarcopenia is associated with postoperative infection and delayed recovery from colorectal cancer resection surgery. Br J Cancer. 2012;107:931–6.CrossRefPubMedCentralPubMed Lieffers JR, Bathe OF, Fassbender K, Winget M, Baracos VE. Sarcopenia is associated with postoperative infection and delayed recovery from colorectal cancer resection surgery. Br J Cancer. 2012;107:931–6.CrossRefPubMedCentralPubMed
8.
go back to reference Pichard C, Kyle UG, Morabia A, Perrier A, Vermeulen B, Unger P. Nutritional assessment: lean body mass depletion at hospital admission is associated with an increased length of stay. Am J Clin Nutr. 2004;79:613–8.PubMed Pichard C, Kyle UG, Morabia A, Perrier A, Vermeulen B, Unger P. Nutritional assessment: lean body mass depletion at hospital admission is associated with an increased length of stay. Am J Clin Nutr. 2004;79:613–8.PubMed
9.
go back to reference Metter EJ, Talbot LA, Schrager M, Conwit R. Skeletal muscle strength as a predictor of all-cause mortality in healthy men. Am J Clin Nutr. 2004;79:613–8. Metter EJ, Talbot LA, Schrager M, Conwit R. Skeletal muscle strength as a predictor of all-cause mortality in healthy men. Am J Clin Nutr. 2004;79:613–8.
10.
go back to reference Tan BH, Birdsell LA, Martin L, Baracos VE, Fearon KC. Sarcopenia in an overweight or obese patient is an adverse prognostic factor in pancreatic cancer. Clin Cancer Res. 2009;15:6973–9.CrossRefPubMed Tan BH, Birdsell LA, Martin L, Baracos VE, Fearon KC. Sarcopenia in an overweight or obese patient is an adverse prognostic factor in pancreatic cancer. Clin Cancer Res. 2009;15:6973–9.CrossRefPubMed
11.
go back to reference Kimyagarov S, Klid R, Fleissig Y, Kopel B, Arad M, Adunsky A. Skeletal muscle mass abnormalities are associated with survival rates of institutionalized elderly nursing home residents. J Nutr Health Aging. 2012;16:432–6.CrossRefPubMed Kimyagarov S, Klid R, Fleissig Y, Kopel B, Arad M, Adunsky A. Skeletal muscle mass abnormalities are associated with survival rates of institutionalized elderly nursing home residents. J Nutr Health Aging. 2012;16:432–6.CrossRefPubMed
12.
go back to reference Montano-Loza AJ, Meza-Junco J, Prado CM, Lieffers JR, Baracos VE, Bain VG, et al. Muscle wasting is associated with mortality in patients with cirrhosis. Clin Gastroenterol Hepatol. 2012;10:166–73.CrossRefPubMed Montano-Loza AJ, Meza-Junco J, Prado CM, Lieffers JR, Baracos VE, Bain VG, et al. Muscle wasting is associated with mortality in patients with cirrhosis. Clin Gastroenterol Hepatol. 2012;10:166–73.CrossRefPubMed
13.
go back to reference Miholic J, Meyer HJ, Müller MJ, Weimann A, Pichlmayr R. Nutritional consequences of total gastrectomy: the relationship between mode of reconstruction, postprandial symptoms, and body composition. Surgery (St. Louis). 1990;108:488–94. Miholic J, Meyer HJ, Müller MJ, Weimann A, Pichlmayr R. Nutritional consequences of total gastrectomy: the relationship between mode of reconstruction, postprandial symptoms, and body composition. Surgery (St. Louis). 1990;108:488–94.
14.
go back to reference Liedman B, Andersson H, Bosaeus I, Hugosson I, Lundell L. Changes in body composition after gastrectomy: results of a controlled, prospective clinical trial. World J Surg. 1997;21:416–21.CrossRefPubMed Liedman B, Andersson H, Bosaeus I, Hugosson I, Lundell L. Changes in body composition after gastrectomy: results of a controlled, prospective clinical trial. World J Surg. 1997;21:416–21.CrossRefPubMed
15.
go back to reference Kiyama T, Mizutani T, Okuda T, Fujita I, Tokunaga A, Tajiri T, et al. Postoperative changes in body composition after gastrectomy. J Gastrointest Surg. 2005;9:313–9.CrossRefPubMed Kiyama T, Mizutani T, Okuda T, Fujita I, Tokunaga A, Tajiri T, et al. Postoperative changes in body composition after gastrectomy. J Gastrointest Surg. 2005;9:313–9.CrossRefPubMed
16.
go back to reference Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma, 3rd English edition. Gastric Cancer. 2011;14:101–12.CrossRef Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma, 3rd English edition. Gastric Cancer. 2011;14:101–12.CrossRef
17.
go back to reference Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–13.CrossRefPubMedCentralPubMed Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–13.CrossRefPubMedCentralPubMed
18.
go back to reference Mourtzakis M, Prado CM, Lieffers JR, Reiman T, McCargar LJ, Baracos VE. 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. 2008;33(16):997–1006.CrossRefPubMed Mourtzakis M, Prado CM, Lieffers JR, Reiman T, McCargar LJ, Baracos VE. 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. 2008;33(16):997–1006.CrossRefPubMed
19.
go back to reference 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. 1998;85:115–22.PubMed 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. 1998;85:115–22.PubMed
20.
go back to reference Kvist H, Sjöström L, Tylén U. Adipose tissue volume determinations in women by computed tomography: technical considerations. Int J Obes. 1986;10:53–67.PubMed Kvist H, Sjöström L, Tylén U. Adipose tissue volume determinations in women by computed tomography: technical considerations. Int J Obes. 1986;10:53–67.PubMed
21.
go back to reference Vehmas T, Kairemo KJ, Taavitsainen MJ. Measuring visceral adipose tissue content from contrast enhanced computed tomography. Int J Obes Relat Metab Disord. 1996;20:570–3.PubMed Vehmas T, Kairemo KJ, Taavitsainen MJ. Measuring visceral adipose tissue content from contrast enhanced computed tomography. Int J Obes Relat Metab Disord. 1996;20:570–3.PubMed
22.
go back to reference Heymsfield SB. Development of imaging methods to assess adiposity and metabolism. Int J Obes (Lond). 2008;32:76–82.CrossRef Heymsfield SB. Development of imaging methods to assess adiposity and metabolism. Int J Obes (Lond). 2008;32:76–82.CrossRef
23.
go back to reference 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;31:74–7.CrossRefPubMed 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;31:74–7.CrossRefPubMed
24.
go back to reference Tanaka K, Miyashiro I, Yano M, Kishi K, Motoori M, Shingai T, et al. Visceral fat changes after distal gastrectomy according to type of reconstruction procedure for gastric cancer. World J Surg Oncol. 2013;11:146.CrossRefPubMedCentralPubMed Tanaka K, Miyashiro I, Yano M, Kishi K, Motoori M, Shingai T, et al. Visceral fat changes after distal gastrectomy according to type of reconstruction procedure for gastric cancer. World J Surg Oncol. 2013;11:146.CrossRefPubMedCentralPubMed
25.
go back to reference Yoon DY, Kim HK, Kim JA, Choi CS, Yun EJ, Chang SK, et al. Changes in the abdominal fat distribution after gastrectomy: computed tomography assessment. ANZ J Surg. 2007;77:121–5.CrossRefPubMed Yoon DY, Kim HK, Kim JA, Choi CS, Yun EJ, Chang SK, et al. Changes in the abdominal fat distribution after gastrectomy: computed tomography assessment. ANZ J Surg. 2007;77:121–5.CrossRefPubMed
26.
go back to reference Miyato H, Kitayama J, Hidemura A, Ishigami H, Kaisaki S, Nagawa H. Vagus nerve preservation selectively restores visceral fat volume in patients with early gastric cancer who underwent gastrectomy. J Surg Res. 2012;173:60–7.CrossRefPubMed Miyato H, Kitayama J, Hidemura A, Ishigami H, Kaisaki S, Nagawa H. Vagus nerve preservation selectively restores visceral fat volume in patients with early gastric cancer who underwent gastrectomy. J Surg Res. 2012;173:60–7.CrossRefPubMed
27.
go back to reference Puthucheary ZA, Rawal J, McPhail M, Connolly B, Ratnayake G, Chan P, et al. Acute skeletal muscle wasting in critical illness. JAMA. 2013;310:1591–600.CrossRefPubMed Puthucheary ZA, Rawal J, McPhail M, Connolly B, Ratnayake G, Chan P, et al. Acute skeletal muscle wasting in critical illness. JAMA. 2013;310:1591–600.CrossRefPubMed
28.
go back to reference Gilliam LA, St. Clair DK. Chemotherapy-induced weakness and fatigue in skeletal muscle: the role of oxidative stress. Antioxid Redox Signal. 2011;15:2543–63.CrossRefPubMedCentralPubMed Gilliam LA, St. Clair DK. Chemotherapy-induced weakness and fatigue in skeletal muscle: the role of oxidative stress. Antioxid Redox Signal. 2011;15:2543–63.CrossRefPubMedCentralPubMed
29.
go back to reference Scheede-Bergdahl C, Jagoe RT. After the chemotherapy: potential mechanisms for chemotherapy-induced delayed skeletal muscle dysfunction in survivors of acute lymphoblastic leukaemia in childhood. Front Pharmacol. 2013;4:1–7.CrossRef Scheede-Bergdahl C, Jagoe RT. After the chemotherapy: potential mechanisms for chemotherapy-induced delayed skeletal muscle dysfunction in survivors of acute lymphoblastic leukaemia in childhood. Front Pharmacol. 2013;4:1–7.CrossRef
30.
go back to reference Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJ, Nicolson M, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med. 2006;355:11–20.CrossRefPubMed Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJ, Nicolson M, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med. 2006;355:11–20.CrossRefPubMed
31.
go back to reference Ychou M, Boige V, Pignon JP, Conroy T, Bouché O, Lebreton G, et al. Perioperative chemotherapy compared with surgery alone for resectable gastroesophageal adenocarcinoma: an FNCLCC and FFCD multicenter phase III trial. J Clin Oncol. 2011;29(13):1715–21.CrossRefPubMed Ychou M, Boige V, Pignon JP, Conroy T, Bouché O, Lebreton G, et al. Perioperative chemotherapy compared with surgery alone for resectable gastroesophageal adenocarcinoma: an FNCLCC and FFCD multicenter phase III trial. J Clin Oncol. 2011;29(13):1715–21.CrossRefPubMed
32.
go back to reference Fujitani K. Overview of adjuvant and neoadjuvant therapy for resectable gastric cancer in the East. Dig Surg. 2013;30:119–29.CrossRefPubMed Fujitani K. Overview of adjuvant and neoadjuvant therapy for resectable gastric cancer in the East. Dig Surg. 2013;30:119–29.CrossRefPubMed
33.
go back to reference Abdiev S, Kodera Y, Fujiwara M, Koike M, Nakayama G, Ohashi N, et al. Nutritional recovery after open and laparoscopic gastrectomies. Gastric Cancer. 2011;14:144–9.CrossRefPubMed Abdiev S, Kodera Y, Fujiwara M, Koike M, Nakayama G, Ohashi N, et al. Nutritional recovery after open and laparoscopic gastrectomies. Gastric Cancer. 2011;14:144–9.CrossRefPubMed
34.
go back to reference Sakuramoto S, Sasako M, Yamaguchi T, Kinoshita T, Fujii M, Nashimoto A, et al. Adjuvant chemotherapy for gastric cancer with S-1, an oral fluoropyrimidine. N Engl J Med. 2007;357:1810–20.CrossRefPubMed Sakuramoto S, Sasako M, Yamaguchi T, Kinoshita T, Fujii M, Nashimoto A, et al. Adjuvant chemotherapy for gastric cancer with S-1, an oral fluoropyrimidine. N Engl J Med. 2007;357:1810–20.CrossRefPubMed
35.
go back to reference Yoshikawa T, Rino Y, Yukawa N, Oshima T, Tsuburaya A, Masuda M. Neoadjuvant chemotherapy for gastric cancer in Japan: a standing position by comparing with adjuvant chemotherapy. Surg Today. 2014;44:11–21.CrossRefPubMed Yoshikawa T, Rino Y, Yukawa N, Oshima T, Tsuburaya A, Masuda M. Neoadjuvant chemotherapy for gastric cancer in Japan: a standing position by comparing with adjuvant chemotherapy. Surg Today. 2014;44:11–21.CrossRefPubMed
36.
go back to reference 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;9:629–35.CrossRefPubMed 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;9:629–35.CrossRefPubMed
37.
go back to reference Martin L, Birdsell L, Macdonald N, Reiman T, Clandinin MT, McCargar LJ, 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, Reiman T, Clandinin MT, McCargar LJ, 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
38.
go back to reference Ryan AM, Reynolds JV, Healy L, Byrne M, Moore J, Brannelly N, et al. Enteral nutrition enriched with eicosapentaenoic acid (EPA) preserves lean body mass following esophageal cancer surgery: results of a double-blinded randomized controlled trial. Ann Surg. 2009;249:355–63.CrossRefPubMed Ryan AM, Reynolds JV, Healy L, Byrne M, Moore J, Brannelly N, et al. Enteral nutrition enriched with eicosapentaenoic acid (EPA) preserves lean body mass following esophageal cancer surgery: results of a double-blinded randomized controlled trial. Ann Surg. 2009;249:355–63.CrossRefPubMed
39.
go back to reference Yoshikawa T, Hiki N, Taguri M, Sano T, Nunobe S, Taniguchi H, et al. A Phase III trial to evaluate the effect of perioperative nutrition enriched with eicosapentaenoic acid on body weight loss after total gastrectomy for T2–T4a gastric cancer. Jpn J Clin Oncol. 2012;42:459–62.CrossRefPubMed Yoshikawa T, Hiki N, Taguri M, Sano T, Nunobe S, Taniguchi H, et al. A Phase III trial to evaluate the effect of perioperative nutrition enriched with eicosapentaenoic acid on body weight loss after total gastrectomy for T2–T4a gastric cancer. Jpn J Clin Oncol. 2012;42:459–62.CrossRefPubMed
40.
go back to reference Adachi S, Takiguchi S, Okada K, Yamamoto K, Yamasaki M, Miyata H, et al. Effects of ghrelin administration after total gastrectomy: a prospective, randomized, placebo-controlled phase II study. Gastroenterology. 2010;138:1312–20.CrossRefPubMed Adachi S, Takiguchi S, Okada K, Yamamoto K, Yamasaki M, Miyata H, et al. Effects of ghrelin administration after total gastrectomy: a prospective, randomized, placebo-controlled phase II study. Gastroenterology. 2010;138:1312–20.CrossRefPubMed
41.
go back to reference Nass R, Pezzoli SS, Oliveri MC, Patrie JT, Harrell FE Jr, Clasey JL, et al. Effects of an oral ghrelin mimetic on body composition and clinical outcomes in healthy older adults: a randomized trial. Ann Intern Med. 2008;149:601–11.CrossRefPubMedCentralPubMed Nass R, Pezzoli SS, Oliveri MC, Patrie JT, Harrell FE Jr, Clasey JL, et al. Effects of an oral ghrelin mimetic on body composition and clinical outcomes in healthy older adults: a randomized trial. Ann Intern Med. 2008;149:601–11.CrossRefPubMedCentralPubMed
Metadata
Title
Skeletal muscle loss after total gastrectomy, exacerbated by adjuvant chemotherapy
Authors
Yusuke Yamaoka
Kazumasa Fujitani
Toshimasa Tsujinaka
Kazuyoshi Yamamoto
Motohiro Hirao
Mitsugu Sekimoto
Publication date
01-04-2015
Publisher
Springer Japan
Published in
Gastric Cancer / Issue 2/2015
Print ISSN: 1436-3291
Electronic ISSN: 1436-3305
DOI
https://doi.org/10.1007/s10120-014-0365-z

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