1932

Abstract

Although higher body mass index (BMI) increases the incidence of many cancers, BMI can also exhibit a null or U-shaped relationship with survival among patients with existing disease; this association of higher BMI with improved survival is termed the obesity paradox. This review discusses possible explanations for the obesity paradox, the prevalence and consequences of low muscle mass in cancer patients, and future research directions. It is unlikely that methodological biases, such as reverse causality or confounding, fully explain the obesity paradox. Rather, up to a point, higher BMI may truly be associated with longer survival in cancer patients. This is due, in part, to the limitations of BMI, which scales weight to height without delineating adipose tissue distribution or distinguishing between adipose and muscle tissue. Thus, cancer patients with higher BMIs often have higher levels of protective muscle. We assert that more precise measures of body composition are required to clarify the relationship of body size to cancer outcomes, inform clinical decision-making, and help tailor lifestyle interventions.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-nutr-082117-051723
2018-08-21
2024-10-16
Loading full text...

Full text loading...

/deliver/fulltext/nutr/38/1/annurev-nutr-082117-051723.html?itemId=/content/journals/10.1146/annurev-nutr-082117-051723&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Adams SC, Segal RJ, McKenzie DC, Vallerand JR, Morielli AR et al. 2016. Impact of resistance and aerobic exercise on sarcopenia and dynapenia in breast cancer patients receiving adjuvant chemotherapy: a multicenter randomized controlled trial. Breast Cancer Res. Treat. 158:497–507
    [Google Scholar]
  2. 2.  Amini N, Spolverato G, Gupta R, Margonis GA, Kim Y 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. 19:1593–602
    [Google Scholar]
  3. 3.  Auclin E, Bourillon C, De Maio E, By MA, Seddik S et al. 2017. Prediction of everolimus toxicity and prognostic value of skeletal muscle index in patients with metastatic renal cell carcinoma. Clin. Genitourin. Cancer 15:350–55
    [Google Scholar]
  4. 4.  Awad S, Tan BH, Cui H, Bhalla A, Fearon KC et al. 2012. Marked changes in body composition following neoadjuvant chemotherapy for oesophagogastric cancer. Clin. Nutr. 31:74–77
    [Google Scholar]
  5. 5.  Banack HR, Kaufman JS 2015. From bad to worse: Collider stratification amplifies confounding bias in the “obesity paradox.”. Eur. J. Epidemiol. 30:1111–14
    [Google Scholar]
  6. 6.  Baracos VE 2000. Regulation of skeletal-muscle–protein turnover in cancer-associated cachexia. Nutrition 16:1015–18
    [Google Scholar]
  7. 7.  Begini P, Gigante E, Antonelli G, Carbonetti F, Iannicelli E et al. 2017. Sarcopenia predicts reduced survival in patients with hepatocellular carcinoma at first diagnosis. Ann. Hepatol. 16:107–14
    [Google Scholar]
  8. 8.  Bekkelund SI, Jorde R 2017. Lean body mass and creatine kinase is associated with reduced inflammation in obesity. Eur. J. Clin. Investig. 47:803–11
    [Google Scholar]
  9. 9.  Biolo G, Cederholm T, Muscaritoli M 2014. Muscle contractile and metabolic dysfunction is a common feature of sarcopenia of aging and chronic diseases: from sarcopenic obesity to cachexia. Clin. Nutr. 33:737–48
    [Google Scholar]
  10. 10.  Blauwhoff-Buskermolen S, Versteeg KS, de van der Schueren MAE, den Braver NR, Berkhof J et al. 2016. Loss of muscle mass during chemotherapy is predictive for poor survival of patients with metastatic colorectal cancer. J. Clin. Oncol. 34:1339–44
    [Google Scholar]
  11. 11.  Boer BC, de Graaff F, Brusse-Keizer M, Bouman DE, Slump CH et al. 2016. Skeletal muscle mass and quality as risk factors for postoperative outcome after open colon resection for cancer. Int. J. Colorectal Dis. 31:1117–24
    [Google Scholar]
  12. 12.  Bowden JCS, Williams LJ, Simms A, Price A, Campbell S et al. 2017. Prediction of 90 day and overall survival after chemoradiotherapy for lung cancer: role of performance status and body composition. Clin. Oncol. 29:576–84
    [Google Scholar]
  13. 13.  Brunner AM, Sadrzadeh H, Feng Y, Drapkin BJ, Ballen KK et al. 2013. Association between baseline body mass index and overall survival among patients over age 60 with acute myeloid leukemia. Am. J. Hematol. 88:642–46
    [Google Scholar]
  14. 14.  Buffart LM, Kalter J, Sweegers MG, Courneya KS, Newton RU et al. 2017. Effects and moderators of exercise on quality of life and physical function in patients with cancer: an individual patient data meta-analysis of 34 RCTs. Cancer Treat. Rev. 52:91–104
    [Google Scholar]
  15. 15.  Caan BJ 2017. Effects of low muscularity and low muscle attenuation on survival in early stage breast and colorectal cancer patients Presented at Int. Conf. Frailty Sarcopenia Res., Apr 27–29 Barcelona:
    [Google Scholar]
  16. 16.  Caan BJ, Meyerhardt JA, Kroenke CH, Alexeeff S, Xiao J et al. 2017. Explaining the obesity paradox: the association between body composition and colorectal cancer survival (C-SCANS Study). Cancer Epidemiol. Biomark. Prev. 26:1008–15
    [Google Scholar]
  17. 17.  Carneiro IP, Mazurak VC, Prado CM 2016. Clinical implications of sarcopenic obesity in cancer. Curr. Oncol. Rep. 18:62
    [Google Scholar]
  18. 18.  Cespedes Feliciano EM, Lee VS, Prado CM, Meyerhardt JA, Alexeeff S et al. 2017. Muscle mass at the time of diagnosis of nonmetastatic colon cancer and early discontinuation of chemotherapy, delays, and dose reductions on adjuvant FOLFOX: the C-SCANS study. Cancer 123:4868–77
    [Google Scholar]
  19. 19.  Cheema BS, Kilbreath SL, Fahey PP, Delaney GP, Atlantis E 2014. Safety and efficacy of progressive resistance training in breast cancer: a systematic review and meta-analysis. Breast Cancer Res. Treat. 148:249–68
    [Google Scholar]
  20. 20.  Chen HN, Chen XZ, Zhang WH, Yang K, Chen XL et al. 2015. The impact of body mass index on the surgical outcomes of patients with gastric cancer: a 10-year, single-institution cohort study. Medicine 94:e1769
    [Google Scholar]
  21. 21.  Cheney CL, Mahloch J, Freeny P 1997. Computerized tomography assessment of women with weight changes associated with adjuvant treatment for breast cancer. Am. J. Clin. Nutr. 66:141–46
    [Google Scholar]
  22. 22.  Cormie P, Zopf EM, Zhang X, Schmitz KH 2017. The impact of exercise on cancer mortality, recurrence, and treatment-related adverse effects. Epidemiol. Rev. 39:71–92
    [Google Scholar]
  23. 23.  Courneya KS, Booth CM, Gill S, O'Brien P, Vardy J et al. 2008. The Colon Health and Life-Long Exercise Change trial: a randomized trial of the National Cancer Institute of Canada Clinical Trials Group. Curr. Oncol. 15:279–85
    [Google Scholar]
  24. 24.  Courneya KS, Segal RJ, McKenzie DC, Dong H, Gelmon K et al. 2014. Effects of exercise during adjuvant chemotherapy on breast cancer outcomes. Med. Sci. Sports Exerc. 46:1744–51
    [Google Scholar]
  25. 25.  Crosbie EJ, Roberts C, Qian W, Swart AM, Kitchener HC, Renehan AG 2012. Body mass index does not influence post-treatment survival in early stage endometrial cancer: results from the MRC ASTEC trial. Eur. J. Cancer 48:853–64
    [Google Scholar]
  26. 26.  Crosby V, D'Souza C, Bristow C, Proffitt A, Hussain A et al. 2017. Can body composition be used to optimize the dose of platinum chemotherapy in lung cancer? A feasibility study. Support. Care Cancer 25:1257–61
    [Google Scholar]
  27. 27.  Dalal S, Hui D, Bidaut L, Lem K, Del Fabbro E et al. 2012. Relationships among body mass index, longitudinal body composition alterations, and survival in patients with locally advanced pancreatic cancer receiving chemoradiation: a pilot study. J. Pain Symptom Manag. 44:181–91
    [Google Scholar]
  28. 28.  Del Fabbro E, Bruera E, Denmark-Wahnfried W, Bowling T, Hopkinson JB, Baracos VE 2010. Nutrition and the Cancer Patient London: Oxford Univ. Press
    [Google Scholar]
  29. 29.  Del Fabbro E, Parsons H, Warneke CL, Pulivarthi K, Litton JK et al. 2012. The relationship between body composition and response to neoadjuvant chemotherapy in women with operable breast cancer. Oncologist 17:1240–45
    [Google Scholar]
  30. 30.  Dhooge M, Coriat R, Mir O, Perkins G, Brezault C et al. 2013. Feasibility of gemcitabine plus oxaliplatin in advanced hepatocellular carcinoma patients with Child-Pugh B cirrhosis. Oncology 84:32–38
    [Google Scholar]
  31. 31.  Di Sebastiano KM, Yang L, Zbuk K, Wong RK, Chow T et al. 2012. Accelerated muscle and adipose tissue loss may predict survival in pancreatic cancer patients: the relationship with diabetes and anaemia. Br. J. Nutr. 109:302–12
    [Google Scholar]
  32. 32.  Dixon JB, Egger GJ 2014. A narrow view of optimal weight for health generates the obesity paradox. Am. J. Clin. Nutr. 99:969–70
    [Google Scholar]
  33. 33.  Ebadi M, Martin L, Ghosh S, Field CJ, Lehner R et al. 2017. Subcutaneous adiposity is an independent predictor of mortality in cancer patients. Br. J. Cancer 117:148–55
    [Google Scholar]
  34. 34.  Fearon K, Arends J, Baracos V 2013. Understanding the mechanisms and treatment options in cancer cachexia. Nat. Rev. Clin. Oncol. 10:90–99
    [Google Scholar]
  35. 35.  Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E et al. 2011. Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 12:489–95
    [Google Scholar]
  36. 36.  Fujiwara N, Nakagawa H, Kudo Y, Tateishi R, Taguri M et al. 2015. Sarcopenia, intramuscular fat deposition, and visceral adiposity independently predict the outcomes of hepatocellular carcinoma. J. Hepatol. 63:131–40
    [Google Scholar]
  37. 37.  Fukushima H, Nakanishi Y, Kataoka M, Tobisu K-I, Koga F 2016.a Prognostic significance of sarcopenia in patients with metastatic renal cell carcinoma. J. Urol. 195:26–32
    [Google Scholar]
  38. 38.  Fukushima H, Nakanishi Y, Kataoka M, Tobisu K-I, Koga F 2016.b Prognostic significance of sarcopenia in upper tract urothelial carcinoma patients treated with radical nephroureterectomy. Cancer Med 5:2213–20
    [Google Scholar]
  39. 39.  Fukushima H, Nakanishi Y, Kataoka M, Tobisu K-I, Koga F 2017. Postoperative changes in skeletal muscle mass predict survival of patients with metastatic renal cell carcinoma undergoing cytoreductive nephrectomy. Clin. Genitourin. Cancer 15:e229–38
    [Google Scholar]
  40. 40.  Fukushima H, Yokoyama M, Nakanishi Y, Tobisu K-I, Koga F 2015. Sarcopenia as a prognostic biomarker of advanced urothelial carcinoma. PLOS ONE 10:e0115895
    [Google Scholar]
  41. 41.  Gérard S, Bréchemier D, Lefort A, Lozano S, Van Kan GA et al. 2016. Body composition and anti-neoplastic treatment in adult and older subjects—a systematic review. J. Nutr. Health Aging 20:878–88
    [Google Scholar]
  42. 42.  Go S-I, Park MJ, Song H-N, Kang MH, Park HJ et al. 2015. Sarcopenia and inflammation are independent predictors of survival in male patients newly diagnosed with small cell lung cancer. Support. Care Cancer 24:2075–84
    [Google Scholar]
  43. 43.  Gonzalez MC, Correia M, Heymsfield SB 2017. A requiem for BMI in the clinical setting. Curr. Opin. Clin. Nutr. Metab. Care 20:314–21
    [Google Scholar]
  44. 44.  Greenlee H, Unger JM, LeBlanc M, Ramsey S, Hershman DL 2017. Association between body mass index and cancer survival in a pooled analysis of 22 clinical trials. Cancer Epidemiol. Biomark. Prev. 26:21–29
    [Google Scholar]
  45. 45.  Grotenhuis BA, Shapiro J, van Adrichem S, de Vries M, Koek M et al. 2016. Sarcopenia/muscle mass is not a prognostic factor for short- and long-term outcome after esophagectomy for cancer. World J. Surg. 40:2698–704
    [Google Scholar]
  46. 46.  Gu W, Zhu Y, Wang H, Zhang H, Shi G et al. 2015. Prognostic value of components of body composition in patients treated with targeted therapy for advanced renal cell carcinoma: a retrospective case series. PLOS ONE 10:e0118022
    [Google Scholar]
  47. 47.  Hakimi AA, Furberg H, Zabor EC, Jacobsen A, Schultz N et al. 2013. An epidemiologic and genomic investigation into the obesity paradox in renal cell carcinoma. J. Natl. Cancer Inst. 105:1862–70
    [Google Scholar]
  48. 48.  Handforth C, Clegg A, Young C, Simpkins S, Seymour MT et al. 2015. The prevalence and outcomes of frailty in older cancer patients: a systematic review. Ann. Oncol. 26:1091–101
    [Google Scholar]
  49. 49.  Harada K, Ida S, Baba Y, Ishimoto T, Kosumi K et al. 2015. Prognostic and clinical impact of sarcopenia in esophageal squamous cell carcinoma. Dis. Esophagus 29:627–33
    [Google Scholar]
  50. 50.  Hardee JP, Porter RR, Sui X, Archer E, Lee IM et al. 2014. The effect of resistance exercise on all-cause mortality in cancer survivors. Mayo Clin. Proc. 89:1108–15
    [Google Scholar]
  51. 51.  Harimoto N, Shirabe K, Yamashita YI, Ikegami T, Yoshizumi T et al. 2013. Sarcopenia as a predictor of prognosis in patients following hepatectomy for hepatocellular carcinoma. Br. J. Surg. 100:1523–30
    [Google Scholar]
  52. 52.  Harimoto N, Yoshizumi T, Shimokawa M, Sakata K, Kimura K et al. 2016. Sarcopenia is a poor prognostic factor following hepatic resection in patients aged 70 years and older with hepatocellular carcinoma. Hepatol. Res. 46:1247–55
    [Google Scholar]
  53. 53.  Haseen F, Murray LJ, Cardwell CR, O'Sullivan JM, Cantwell MM 2010. The effect of androgen deprivation therapy on body composition in men with prostate cancer: systematic review and meta-analysis. J. Cancer Surviv. 4:128–39
    [Google Scholar]
  54. 54.  Hayashi N, Ando Y, Gyawali B, Shimokata T, Maeda O et al. 2016. Low skeletal muscle density is associated with poor survival in patients who receive chemotherapy for metastatic gastric cancer. Oncol. Rep. 35:1727–31
    [Google Scholar]
  55. 55.  Hervochon R, Bobbio A, Guinet C, Mansuet-Lupo A, Rabbat A et al. 2017. Body mass index and total psoas area affect outcomes in patients undergoing pneumonectomy for cancer. Ann. Thorac. Surg. 103:287–95
    [Google Scholar]
  56. 56.  Hiraoka A, Hirooka M, Koizumi Y, Izumoto H, Ueki H et al. 2017. Muscle volume loss as a prognostic marker in hepatocellular carcinoma patients treated with sorafenib. Hepatol. Res. 47:558–65
    [Google Scholar]
  57. 57.  Hirasawa Y, Nakashima J, Yunaiyama D, Sugihara T, Gondo T et al. 2016. Sarcopenia as a novel preoperative prognostic predictor for survival in patients with bladder cancer undergoing radical cystectomy. Ann. Surg. Oncol. 23:1048–54
    [Google Scholar]
  58. 58.  Huang D-D, Chen X-X, Chen X-Y, Wang S-L, Shen X et al. 2016. Sarcopenia predicts 1-year mortality in elderly patients undergoing curative gastrectomy for gastric cancer: a prospective study. J. Cancer Res. Clin. Oncol. 142:2347–56
    [Google Scholar]
  59. 59.  Hubbard JM, Cohen HJ, Muss HB 2014. Incorporating biomarkers into cancer and aging research. J. Clin. Oncol. 32:2611–16
    [Google Scholar]
  60. 60.  Hubbard RE, Lang IA, Llewellyn DJ, Rockwood K 2010. Frailty, body mass index, and abdominal obesity in older people. J. Gerontol. A. 65:377–81
    [Google Scholar]
  61. 61.  Imai K, Takai K, Hanai T, Ideta T, Miyazaki T et al. 2015. Skeletal muscle depletion predicts the prognosis of patients with hepatocellular carcinoma treated with sorafenib. Int. J. Mol. Sci 16:9612–24
    [Google Scholar]
  62. 62.  Iritani S, Imai K, Takai K, Hanai T, Ideta T et al. 2015. Skeletal muscle depletion is an independent prognostic factor for hepatocellular carcinoma. J. Gastroenterol. 50:323–32
    [Google Scholar]
  63. 63.  Ishihara H, Kondo T, Omae K, Takagi T, Iizuka J et al. 2016. Sarcopenia predicts survival outcomes among patients with urothelial carcinoma of the upper urinary tract undergoing radical nephroureterectomy: a retrospective multi-institution study. Int. J. Clin. Oncol. 22:136–44
    [Google Scholar]
  64. 64.  Itoh S, Shirabe K, Matsumoto Y, Yoshiya S, Muto J et al. 2014. Effect of body composition on outcomes after hepatic resection for hepatocellular carcinoma. Ann. Surg. Oncol. 21:3063–68
    [Google Scholar]
  65. 65.  Joglekar S, Nau PN, Mezhir JJ 2015. The impact of sarcopenia on survival and complications in surgical oncology: a review of the current literature. J. Surg. Oncol. 112:503–9
    [Google Scholar]
  66. 66.  Jung HW, Kim JW, Kim JY, Kim SW, Yang HK et al. 2015. Effect of muscle mass on toxicity and survival in patients with colon cancer undergoing adjuvant chemotherapy. Support. Care Cancer 23:687–94
    [Google Scholar]
  67. 67.  Kalinkovich A, Livshits G 2016. Sarcopenic obesity or obese sarcopenia: a cross talk between age-associated adipose tissue and skeletal muscle inflammation as a main mechanism of the pathogenesis. Ageing Res. Rev. 35:200–21
    [Google Scholar]
  68. 68.  Kasahara R, Kawahara T, Ohtake S, Saitoh Y, Tsutsumi S et al. 2017. A low psoas muscle index before treatment can predict a poorer prognosis in advanced bladder cancer patients who receive gemcitabine and nedaplatin therapy. BioMed Res. Int. 2017:7981549
    [Google Scholar]
  69. 69.  Kazemi-Bajestani SM, Mazurak VC, Baracos V 2016. Computed tomography-defined muscle and fat wasting are associated with cancer clinical outcomes. Semin. Cell Dev. Biol. 54:2–10
    [Google Scholar]
  70. 70.  Kim EY, Kim YS, Park I, Ahn HK, Cho EK, Jeong YM 2015. Prognostic significance of CT-determined sarcopenia in patients with small-cell lung cancer. J. Thorac. Oncol. 10:1795–99
    [Google Scholar]
  71. 71.  Kimura M, Naito T, Kenmotsu H, Taira T, Wakuda K et al. 2014. Prognostic impact of cancer cachexia in patients with advanced non-small cell lung cancer. Support. Care Cancer 23:1699–708
    [Google Scholar]
  72. 72.  Kinsey CM, San José Estépar R, van der Velden J, Cole BF, Christiani DC, Washko GR 2016. Lower pectoralis muscle area is associated with a worse overall survival in non–small cell lung cancer. Cancer Epidemiol. Biomark. Prev. 26:38–43
    [Google Scholar]
  73. 73.  Kroenke CH, Neugebauer R, Meyerhardt J, Prado CM, Weltzien E et al. 2016. Analysis of body mass index and mortality in patients with colorectal cancer using causal diagrams. JAMA Oncol 2:1137–45
    [Google Scholar]
  74. 74.  Kubo Y, Naito T, Mori K, Osawa G, Aruga E 2017. Skeletal muscle loss and prognosis of breast cancer patients. Support. Care Cancer 25:2221–27
    [Google Scholar]
  75. 75.  Kudou K, Saeki H, Nakashima Y, Edahiro K, Korehisa S et al. 2017. Prognostic significance of sarcopenia in patients with esophagogastric junction cancer or upper gastric cancer. Ann. Surg. Oncol. 24:1804–10
    [Google Scholar]
  76. 76.  Lauby-Secretan B, Scoccianti C, Loomis D, Grosse Y, Bianchini F et al. 2016. Body fatness and cancer—viewpoint of the IARC Working Group. N. Engl. J. Med. 375:794–98
    [Google Scholar]
  77. 77.  Levolger S, van Vledder MG, Muslem R, Koek M, Niessen WJ et al. 2015. Sarcopenia impairs survival in patients with potentially curable hepatocellular carcinoma. J. Surg. Oncol. 112:208–13
    [Google Scholar]
  78. 78.  Li XT, Tang L, Chen Y, Li YL, Zhang XP, Sun YS 2015. Visceral and subcutaneous fat as new independent predictive factors of survival in locally advanced gastric carcinoma patients treated with neo-adjuvant chemotherapy. J. Cancer Res. Clin. Oncol. 141:1237–47
    [Google Scholar]
  79. 79.  Lindner J, Loibl S, Denkert C, Ataseven B, Fasching PA et al. 2014. Expression of secreted protein acidic and rich in cysteine (SPARC) in breast cancer and response to neoadjuvant chemotherapy. Ann. Oncol. 26:95–100
    [Google Scholar]
  80. 80.  Liu J, Motoyama S, Sato Y, Wakita A, Kawakita Y et al. 2016. Decreased skeletal muscle mass after neoadjuvant therapy correlates with poor prognosis in patients with esophageal cancer. Anticancer Res 36:6677–86
    [Google Scholar]
  81. 81.  Lodewick TM, van Nijnatten TJA, van Dam RM, van Mierlo K, Dello SAWG et al. 2015. Are sarcopenia, obesity and sarcopenic obesity predictive of outcome in patients with colorectal liver metastases?. HPB 17:438–46
    [Google Scholar]
  82. 82.  Malietzis G, Currie AC, Athanasiou T, Johns N, Anyamene N et al. 2016.a Influence of body composition profile on outcomes following colorectal cancer surgery. Br. J. Surg. 103:572–80
    [Google Scholar]
  83. 83.  Malietzis G, Currie AC, Johns N, Fearon KC, Darzi A et al. 2016.b Skeletal muscle changes after elective colorectal cancer resection: a longitudinal study. Ann. Surg. Oncol. 23:2539–47
    [Google Scholar]
  84. 84.  McLeay SC, Morrish GA, Kirkpatrick CM, Green B 2012. The relationship between drug clearance and body size: systematic review and meta-analysis of the literature published from 2000 to 2007. Clin. Pharmacokinet. 51:319–30
    [Google Scholar]
  85. 85.  McSorley ST, Black DH, Horgan PG, McMillan DC 2018. The relationship between tumour stage, systemic inflammation, body composition and survival in patients with colorectal cancer. Clin. Nutr In press. https://doi.org/10.1016/j.clnu.2017.05.017
    [Crossref] [Google Scholar]
  86. 86.  Mei KL, Batsis JA, Mills JB, Holubar SD 2016. Sarcopenia and sarcopenic obesity: Do they predict inferior oncologic outcomes after gastrointestinal cancer surgery?. Perioper. Med. 5:30
    [Google Scholar]
  87. 87.  Meza-Junco J, Montano-Loza AJ, Baracos VE, Prado CM, Bain VG et al. 2013. Sarcopenia as a prognostic index of nutritional status in concurrent cirrhosis and hepatocellular carcinoma. J. Clin. Gastroenterol. 47:861–70
    [Google Scholar]
  88. 88.  Minnella EM, Bousquet-Dion G, Awasthi R, Scheede-Bergdahl C, Carli F 2017. Multimodal prehabilitation improves functional capacity before and after colorectal surgery for cancer: a five-year research experience. Acta Oncol 56:295–300
    [Google Scholar]
  89. 89.  Mir O, Coriat R, Blanchet B, Durand JP, Boudou-Rouquette P et al. 2012.a Sarcopenia predicts early dose-limiting toxicities and pharmacokinetics of sorafenib in patients with hepatocellular carcinoma. PLOS ONE 7:e37563
    [Google Scholar]
  90. 90.  Mir O, Coriat R, Boudou-Rouquette P, Ropert S, Durand JP et al. 2012.b Gemcitabine and oxaliplatin as second-line treatment in patients with hepatocellular carcinoma pre-treated with sorafenib. Med. Oncol. 29:2793–99
    [Google Scholar]
  91. 91.  Mitsiopoulos N, Baumgartner R, Heymsfield S, Lyons W, Gallagher D, Ross R 1998. Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography. J. Appl. Physiol. 85:115–22
    [Google Scholar]
  92. 92.  Miyake M, Morizawa Y, Hori S, Marugami N, Shimada K et al. 2017. Clinical impact of postoperative loss in psoas major muscle and nutrition index after radical cystectomy for patients with urothelial carcinoma of the bladder. BMC Cancer 17: 237. Erratum. 2017 BMC Cancer 17:353
    [Google Scholar]
  93. 93.  Miyamoto Y, Baba Y, Sakamoto Y, Ohuchi M, Tokunaga R et al. 2015.a Negative impact of skeletal muscle loss after systemic chemotherapy in patients with unresectable colorectal cancer. PLOS ONE 10:e0129742
    [Google Scholar]
  94. 94.  Miyamoto Y, Baba Y, Sakamoto Y, Ohuchi M, Tokunaga R et al. 2015.b Sarcopenia is a negative prognostic factor after curative resection of colorectal cancer. Ann. Surg. Oncol. 22:2663–68
    [Google Scholar]
  95. 95.  Nagai MA, Gerhard R, Fregnani JHT, Nonogaki S, Rierger RB et al. 2011. Prognostic value of NDRG1 and SPARC protein expression in breast cancer patients. Breast Cancer Res. Treat. 126:1–14
    [Google Scholar]
  96. 96.  Nagata T, Nakase Y, Nakamura KEI, Sougawa A, Mochiduki S et al. 2016. Prognostic impact of a nutritional index including muscle volume in stage 4 colorectal cancer. In Vivo 30:885–92
    [Google Scholar]
  97. 97.  Nagle C, Dixon S, Jensen A, Kjaer S, Modugno F 2015. Obesity and survival among women with ovarian cancer: results from the Ovarian Cancer Association Consortium. Br. J. Cancer 113:817–26
    [Google Scholar]
  98. 98.  Nakashima Y, Saeki H, Nakanishi R, Sugiyama M, Kurashige J et al. 2018. Assessment of sarcopenia as a predictor of poor outcomes after esophagectomy in elderly patients with esophageal cancer. Ann. Surg. 267:6) 1100–4
    [Google Scholar]
  99. 99.  Natl. Cancer Inst 2017. Resistance Training to Reduce Chemotoxicity in Colon Cancer Bethesda, MD: Natl. Cancer Inst https://maps.cancer.gov/overview/DCCPSGrants/abstract.jsp?applId=9324643&term=CA206196
    [Google Scholar]
  100. 100.  Nattenmüller J, Wochner R, Muley T, Steins M, Hummler S et al. 2017. Prognostic impact of CT-quantified muscle and fat distribution before and after first-line-chemotherapy in lung cancer patients. PLOS ONE 12:e0169136
    [Google Scholar]
  101. 101.  Nault JC, Pigneur F, Nelson AC, Costentin C, Tselikas L et al. 2015. Visceral fat area predicts survival in patients with advanced hepatocellular carcinoma treated with tyrosine kinase inhibitors. Dig. Liver Dis. 47:869–76
    [Google Scholar]
  102. 102.  Navarro WH, Loberiza FR, Bajorunaite R, van Besien K, Vose JM et al. 2006. Effect of body mass index on mortality of patients with lymphoma undergoing autologous hematopoietic cell transplantation. Biol. Blood Marrow Transplant. 12:541–51
    [Google Scholar]
  103. 103.  Ninomiya G, Fujii T, Yamada S, Yabusaki N, Suzuki K et al. 2017. Clinical impact of sarcopenia on prognosis in pancreatic ductal adenocarcinoma: a retrospective cohort study. Int. J. Surg. 39:45–51
    [Google Scholar]
  104. 104.  Okumura S, Kaido T, Hamaguchi Y, Fujimoto Y, Masui T et al. 2015. Impact of preoperative quality as well as quantity of skeletal muscle on survival after resection of pancreatic cancer. Surgery 157:1088–98
    [Google Scholar]
  105. 105.  Padilha CS, Marinello PC, Galvao DA, Newton RU, Borges FH et al. 2017. Evaluation of resistance training to improve muscular strength and body composition in cancer patients undergoing neoadjuvant and adjuvant therapy: a meta-analysis. J. Cancer Surviv. 11:339–49
    [Google Scholar]
  106. 106.  Palmela C, Velho S, Agostinho L, Branco F, Santos M et al. 2017. Body composition as a prognostic factor of neoadjuvant chemotherapy toxicity and outcome in patients with locally advanced gastric cancer. J. Gastric Cancer 17:74–87
    [Google Scholar]
  107. 107.  Park I, Choi SJ, Kim YS, Ahn HK, Hong J et al. 2016. Prognostic factors for risk stratification of patients with recurrent or metastatic pancreatic adenocarcinoma who were treated with gemcitabine-based chemotherapy. Cancer Res. Treat. 48:1264–73
    [Google Scholar]
  108. 108.  Park SY, Yoon J-K, Lee SJ, Haam S, Jung J 2016. Prognostic value of preoperative total psoas muscle area on long-term outcome in surgically treated oesophageal cancer patients. Interact. Cardiovasc. Thorac. Surg. 24:13–19
    [Google Scholar]
  109. 109.  Parkin E, Plumb AA, O'Reilly D, Renehan AG 2012. Body composition and outcome in patients undergoing resection of colorectal liver metastases (Br. J. Surg. 2012; 99:550–557). Br. J. Surg. 99:1021–22
    [Google Scholar]
  110. 110.  Pecorelli N, Carrara G, De Cobelli F Cristel G, Damascelli A et al. 2016. Effect of sarcopenia and visceral obesity on mortality and pancreatic fistula following pancreatic cancer surgery. Br. J. Surg. 103:434–42
    [Google Scholar]
  111. 111.  Pedersen L, Idorn M, Olofsson GH, Lauenborg B, Nookaew I et al. 2016. Voluntary running suppresses tumor growth through epinephrine- and IL-6-dependent NK cell mobilization and redistribution. Cell Metab 23:554–62
    [Google Scholar]
  112. 112.  Peng PD, Hyder O, Firoozmand A, Kneuertz P, Schulick RD et al. 2012. Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma. J. Gastrointest. Surg. 16:1478–86
    [Google Scholar]
  113. 113.  Peng PD, van Vledder MG, Tsai S, de Jong MC, Makary M et al. 2011. Sarcopenia negatively impacts short-term outcomes in patients undergoing hepatic resection for colorectal liver metastasis. HPB 13:439–46
    [Google Scholar]
  114. 114.  Peterson SJ, Braunschweig CA 2016. Prevalence of sarcopenia and associated outcomes in the clinical setting. Nutr. Clin. Pract. 31:40–48
    [Google Scholar]
  115. 115.  Peterson SJ, Mozer M 2017. Differentiating sarcopenia and cachexia among patients with cancer. Nutr. Clin. Pract. 32:30–39
    [Google Scholar]
  116. 116.  Peyton CC, Heavner MG, Rague JT, Krane LS, Hemal AK 2016. Does sarcopenia impact complications and overall survival in patients undergoing radical nephrectomy for stage III and IV kidney cancer?. J. Endourol. 30:229–36
    [Google Scholar]
  117. 117.  Phillips BE, Smith K, Liptrot S, Atherton PJ, Varadhan K et al. 2013. Effect of colon cancer and surgical resection on skeletal muscle mitochondrial enzyme activity in colon cancer patients: a pilot study. J. Cachexia Sarcopenia Muscle 4:71–77
    [Google Scholar]
  118. 118.  Prado CM, Birdsell LA, Baracos VE 2009. The emerging role of computerized tomography in assessing cancer cachexia. Curr. Opin. Support. Palliat. Care 3:269–75
    [Google Scholar]
  119. 119.  Prado CM, Cushen SJ, Orsso CE, Ryan AM 2016. Sarcopenia and cachexia in the era of obesity: clinical and nutritional impact. Proc. Nutr. Soc. 75:188–98
    [Google Scholar]
  120. 120.  Prado CM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB et al. 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 9:629–35
    [Google Scholar]
  121. 121.  Pratesi A, Tarantini F, Bari Di 2013. Skeletal muscle: an endocrine organ. Clin. Cases Miner. Bone Metab. 10:11–14
    [Google Scholar]
  122. 122.  Psutka SP, Boorjian SA, Moynagh MR, Schmit GD, Costello BA et al. 2016. Decreased skeletal muscle mass is associated with an increased risk of mortality after radical nephrectomy for localized renal cell cancer. J. Urol. 195:270–76
    [Google Scholar]
  123. 123.  Psutka SP, Boorjian SA, Moynagh MR, Schmit GD, Frank I et al. 2015. Mortality after radical cystectomy: impact of obesity versus adiposity after adjusting for skeletal muscle wasting. J. Urol. 193:1507–13
    [Google Scholar]
  124. 124.  Psutka SP, Carrasco A, Schmit GD, Moynagh MR, Boorjian SA et al. 2014. Sarcopenia in patients with bladder cancer undergoing radical cystectomy: impact on cancer-specific and all-cause mortality. Cancer 120:2910–18
    [Google Scholar]
  125. 125.  Reisinger KW, Bosmans JW, Uittenbogaart M, Alsoumali A, Poeze M et al. 2015. Loss of skeletal muscle mass during neoadjuvant chemoradiotherapy predicts postoperative mortality in esophageal cancer surgery. Ann. Surg. Oncol. 22:4445–52
    [Google Scholar]
  126. 126.  Reisinger KW, van Vugt JLA, Tegels JJW, Snijders C, Hulsewé KWE et al. 2015. Functional compromise reflected by sarcopenia, frailty, and nutritional depletion predicts adverse postoperative outcome after colorectal cancer surgery. Ann. Surg. 261:345–52
    [Google Scholar]
  127. 127.  Rier HN, Jager A, Sleijfer S, Maier AB, Levin MD 2016. The prevalence and prognostic value of low muscle mass in cancer patients: a review of the literature. Oncologist 21:1396–409
    [Google Scholar]
  128. 128.  Rier HN, Jager A, Sleijfer S, van Rosmalen J, Kock MCJM, Levin M-D 2017. Low muscle attenuation is a prognostic factor for survival in metastatic breast cancer patients treated with first line palliative chemotherapy. Breast 31:9–15
    [Google Scholar]
  129. 129.  Rollins KE, Tewari N, Ackner A, Awwad A, Madhusudan S et al. 2016. The impact of sarcopenia and myosteatosis on outcomes of unresectable pancreatic cancer or distal cholangiocarcinoma. Clin. Nutr. 35:1103–9
    [Google Scholar]
  130. 130.  Sabel MS, Terjimanian M, Conlon ASC, Griffith KA, Morris AM et al. 2013. Analytic morphometric assessment of patients undergoing colectomy for colon cancer. J. Surg. Oncol. 108:169–75
    [Google Scholar]
  131. 131.  Sakurai K, Kubo N, Tamura T, Toyokawa T, Amano R et al. 2017. Adverse effects of low preoperative skeletal muscle mass in patients undergoing gastrectomy for gastric cancer. Ann. Surg. Oncol. 24:2712–19
    [Google Scholar]
  132. 132.  Schlesinger S, Siegert S, Koch M, Walter J, Heits N et al. 2014. Postdiagnosis body mass index and risk of mortality in colorectal cancer survivors: a prospective study and meta-analysis. Cancer Causes Control 25:1407–18
    [Google Scholar]
  133. 133.  Shachar SS, Deal AM, Weinberg M, Nyrop KA, Williams GR et al. 2016.a Skeletal muscle measures as predictors of toxicity, hospitalization, and survival in patients with metastatic breast cancer receiving taxane-based chemotherapy. Clin. Cancer Res. 23:658–65
    [Google Scholar]
  134. 134.  Shachar SS, Williams GR, Muss HB, Nishijima TF 2016.b Prognostic value of sarcopenia in adults with solid tumours: a meta-analysis and systematic review. Eur. J. Cancer 57:58–67
    [Google Scholar]
  135. 135.  Sharma P, Zargar-Shoshtari K, Caracciolo JT, Fishman M, Poch MA et al. 2015. Sarcopenia as a predictor of overall survival after cytoreductive nephrectomy for metastatic renal cell carcinoma. Urol. Oncol. 33:339.e17–23
    [Google Scholar]
  136. 136.  Sheetz KH, Zhao L, Holcombe SA, Wang SC, Reddy RM et al. 2013. Decreased core muscle size is associated with worse patient survival following esophagectomy for cancer. Dis. Esophagus 26:716–22
    [Google Scholar]
  137. 137.  Singal AG, Zhang P, Waljee AK, Ananthakrishnan L, Parikh ND et al. 2016. Body composition features predict overall survival in patients with hepatocellular carcinoma. Clin. Transl. Gastroenterol. 7:e172
    [Google Scholar]
  138. 138.  Sjøblom B, Grønberg BH, Wentzel-Larsen T, Baracos VE, Hjermstad MJ et al. 2016. Skeletal muscle radiodensity is prognostic for survival in patients with advanced non-small cell lung cancer. Clin. Nutr. 35:1386–93
    [Google Scholar]
  139. 139.  Smith AB, Deal AM, Yu H, Boyd B, Matthews J et al. 2014. Sarcopenia as a predictor of complications and survival following radical cystectomy. J. Urol. 191:1714–20
    [Google Scholar]
  140. 140.  Smith AD, Shah SN, Rini BI, Lieber ML, Remer EM 2010. Morphology, Attenuation, Size, and Structure (MASS) criteria: assessing response and predicting clinical outcome in metastatic renal cell carcinoma on antiangiogenic targeted therapy. Am. J. Roentgenol. 194:1470–78
    [Google Scholar]
  141. 141.  Sperrin M, Candlish J, Badrick E, Renehan A, Buchan I 2016. Collider bias is only a partial explanation for the obesity paradox. Epidemiology 27:525–30
    [Google Scholar]
  142. 142.  Srikanthan P, Hevener AL, Karlamangla AS 2010. Sarcopenia exacerbates obesity-associated insulin resistance and dysglycemia: findings from the National Health and Nutrition Examination Survey III. PLOS ONE 5:e10805
    [Google Scholar]
  143. 143.  Stene GB, Helbostad JL, Amundsen T, Sørhaug S, Hjelde H et al. 2014. Changes in skeletal muscle mass during palliative chemotherapy in patients with advanced lung cancer. Acta Oncol 54:340–48
    [Google Scholar]
  144. 144.  Stiles ZE, Rist TM, Dickson PV, Glazer ES, Fleming MD et al. 2017. Impact of body mass index on the short-term outcomes of resected gastrointestinal stromal tumors. J. Surg. Res. 217:123–30
    [Google Scholar]
  145. 145.  Suzuki Y, Okamoto T, Fujishita T, Katsura M, Akamine T et al. 2016. Clinical implications of sarcopenia in patients undergoing complete resection for early non-small cell lung cancer. Lung Cancer 101:92–97
    [Google Scholar]
  146. 146.  Szlejf C, Parra-Rodriguez L, Rosas-Carrasco O 2017. Osteosarcopenic obesity: prevalence and relation with frailty and physical performance in middle-aged and older women. J. Am. Med. Dir. Assoc. 18:733.e1–5
    [Google Scholar]
  147. 147.  Taguchi S, Akamatsu N, Nakagawa T, Gonoi W, Kanatani A et al. 2016. Sarcopenia evaluated using the skeletal muscle index is a significant prognostic factor for metastatic urothelial carcinoma. Clin. Genitourin. Cancer 14:237–43
    [Google Scholar]
  148. 148.  Takagi K, Yagi T, Yoshida R, Shinoura S, Umeda Y et al. 2016. Sarcopenia and American Society of Anesthesiologists physical status in the assessment of outcomes of hepatocellular carcinoma patients undergoing hepatectomy. Acta Med. Okayama 70:363–70
    [Google Scholar]
  149. 149.  Tamandl D, Paireder M, Asari R, Baltzer PA, Schoppmann SF, Ba-Ssalamah A 2016. Markers of sarcopenia quantified by computed tomography predict adverse long-term outcome in patients with resected oesophageal or gastro-oesophageal junction cancer. Eur. Radiol. 26:1359–67
    [Google Scholar]
  150. 150.  Tan BHL, Birdsell LA, Martin L, Baracos VE, Fearon KCH 2009. Sarcopenia in an overweight or obese patient is an adverse prognostic factor in pancreatic cancer. Clin. Cancer Res. 15:6973–79
    [Google Scholar]
  151. 151.  Tegels JJW, van Vugt JLA, Reisinger KW, Hulsewé KWE, Hoofwijk AGM et al. 2015. Sarcopenia is highly prevalent in patients undergoing surgery for gastric cancer but not associated with worse outcomes. J. Surg. Oncol. 112:403–7
    [Google Scholar]
  152. 152.  Thoresen L, Frykholm G, Lydersen S, Ulveland H, Baracos V et al. 2013. Nutritional status, cachexia and survival in patients with advanced colorectal carcinoma: Different assessment criteria for nutritional status provide unequal results. Clin. Nutr. 32:65–72
    [Google Scholar]
  153. 153.  Torres ML, Hartmann LC, Cliby WA, Kalli KR, Young PM et al. 2013. Nutritional status, CT body composition measures and survival in ovarian cancer. Gynecol. Oncol. 129:548–53
    [Google Scholar]
  154. 154.  Tsukioka T, Nishiyama N, Izumi N, Mizuguchi S, Komatsu H et al. 2017. Sarcopenia is a novel poor prognostic factor in male patients with pathological stage I non-small cell lung cancer. Jpn. J. Clin. Oncol. 47:363–68
    [Google Scholar]
  155. 155.  Valero V 3rd, Amini N, Spolverato G, Weiss MJ, Hirose K et al. 2015. Sarcopenia adversely impacts postoperative complications following resection or transplantation in patients with primary liver tumors. J. Gastrointest. Surg. 19:272–81
    [Google Scholar]
  156. 156.  van Dijk DPJ, Bakens MJAM, Coolsen MME, Rensen SS, van Dam RM et al. 2017. Low skeletal muscle radiation attenuation and visceral adiposity are associated with overall survival and surgical site infections in patients with pancreatic cancer. J. Cachexia Sarcopenia Muscle 8:317–26
    [Google Scholar]
  157. 157.  van Londen GJ, Levy ME, Perera S, Nelson JB, Greenspan SL 2008. Body composition changes during androgen deprivation therapy for prostate cancer: a 2-year prospective study. Crit. Rev. Oncol. Hematol. 68:172–77
    [Google Scholar]
  158. 158.  van Vledder MG, Levolger S, Ayez N, Verhoef C, Tran TC, Ijzermans JN 2012. Body composition and outcome in patients undergoing resection of colorectal liver metastases. Br. J. Surg. 99:550–57
    [Google Scholar]
  159. 159.  Vansteelandt S 2017. Asking too much of epidemiologic studies: the problem of collider bias and the obesity paradox. Epidemiology 28:e47–49
    [Google Scholar]
  160. 160.  Vega MC, Laviano A, Pimentel GD 2016. Sarcopenia and chemotherapy-mediated toxicity. Einstein 14:580–84
    [Google Scholar]
  161. 161.  Viallon V, Dufournet M 2017. Re: Collider bias is only a partial explanation for the obesity paradox. Epidemiology 28:e43–45
    [Google Scholar]
  162. 162.  Villaseñor A, Ballard-Barbash R, Baumgartner K, Baumgartner R, Bernstein L et al. 2012. Prevalence and prognostic effect of sarcopenia in breast cancer survivors: the HEAL Study. J. Cancer Surviv. 6:398–406
    [Google Scholar]
  163. 163.  Voron T, Tselikas L, Pietrasz D, Pigneur F, Laurent A et al. 2015. Sarcopenia impacts on short- and long-term results of hepatectomy for hepatocellular carcinoma. Ann. Surg. 261:1173–83
    [Google Scholar]
  164. 164.  Wagner D, DeMarco MM, Amini N, Buttner S, Segev D et al. 2016. Role of frailty and sarcopenia in predicting outcomes among patients undergoing gastrointestinal surgery. World J. Gastrointest. Surg. 8:27–40
    [Google Scholar]
  165. 165.  Williams JP, Phillips BE, Smith K, Atherton PJ, Rankin D et al. 2012. Effect of tumor burden and subsequent surgical resection on skeletal muscle mass and protein turnover in colorectal cancer patients. Am. J. Clin. Nutr. 96:1064–70
    [Google Scholar]
  166. 166.  Wu AH, Gomez SL, Vigen C, Kwan ML, Keegan TH et al. 2013. The California Breast Cancer Survivorship Consortium (CBCSC): prognostic factors associated with racial/ethnic differences in breast cancer survival. Cancer Causes Control 24:1821–36
    [Google Scholar]
  167. 167.  Wysham NG, Nipp RD, LeBlanc TW, Wolf SP, Ekstrom MP, Currow DC 2016. A practical measurement of thoracic sarcopenia: correlation with clinical parameters and outcomes in advanced lung cancer. ERJ Open Res 2:00085–2015
    [Google Scholar]
  168. 168.  Xiao DY, Luo S, O'Brian K, Sanfilippo KM, Ganti A et al. 2016. Longitudinal body composition changes in diffuse large B-cell lymphoma survivors: a retrospective cohort study of United States veterans. J. Natl. Cancer Inst. 108:djw145
    [Google Scholar]
  169. 169.  Xiao Q, Hsing AW, Park Y, Moore SC, Matthews CE et al. 2014. Body mass index and mortality among blacks and whites adults in the Prostate, Lung, Colorectal, and Ovarian (PLCO) Cancer Screening Trial. Obesity 22:260–68
    [Google Scholar]
  170. 170.  Yabusaki N, Fujii T, Yamada S, Suzuki K, Sugimoto H et al. 2016. Adverse impact of low skeletal muscle index on the prognosis of hepatocellular carcinoma after hepatic resection. Int. J. Surg. 30:136–42
    [Google Scholar]
  171. 171.  Yip C, Goh V, Davies A, Gossage J, Mitchell-Hay R et al. 2014. Assessment of sarcopenia and changes in body composition after neoadjuvant chemotherapy and associations with clinical outcomes in oesophageal cancer. Eur. Radiol. 24:998–1005
    [Google Scholar]
  172. 172.  Zhang X, Liu Y, Shao H, Zheng X 2017. Obesity paradox in lung cancer prognosis: evolving biological insights and clinical implications. J. Thorac. Oncol. 12:1478–88
    [Google Scholar]
  173. 173.  Zhou G, Bao H, Zeng Q, Hu W, Zhang Q 2015. Sarcopenia as a prognostic factor in hepatolithiasis-associated intrahepatic cholangiocarcinoma patients following hepatectomy: a retrospective study. Int. J. Clin. Exp. Med. 8:18245–54
    [Google Scholar]
  174. 174.  Zhuang C-L, Huang D-D, Pang W-Y, Zhou C-J, Wang S-L et al. 2016. Sarcopenia is an independent predictor of severe postoperative complications and long-term survival after radical gastrectomy for gastric cancer. Medicine 95:e3164
    [Google Scholar]
/content/journals/10.1146/annurev-nutr-082117-051723
Loading
/content/journals/10.1146/annurev-nutr-082117-051723
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error