Prognostic value of sarcopenia in adults with solid tumours: A meta-analysis and systematic review

European Journal of Cancer

Volumn 57, Issue , 2016, Pages 58-67

  Shachar, Shlomit Strulov ^a,b   Williams, Grant R ^a   Muss, Hyman B ^a   Nishijima, Tomohiro F ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b Division of Oncology   (Israel)

Author keywords

Cancer; Meta analysis; Prognostic factor; Sarcopenia; Skeletal mass index (SMI); Solid tumours; Survival; Systematic review

Indexed keywords

BODY COMPOSITION; CANCER PROGNOSIS; CANCER SPECIFIC SURVIVAL; COLORECTAL CANCER; CROSS-SECTIONAL STUDY; DISEASE FREE SURVIVAL; HUMAN; KIDNEY CARCINOMA; LIVER CELL CARCINOMA; META ANALYSIS; MUSCULOSKELETAL DISEASE ASSESSMENT; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; RECURRENCE FREE SURVIVAL; REVIEW; SARCOPENIA; SKELETAL MUSCLE INDEX; SOLID TUMOR; SYSTEMATIC REVIEW; ADULT; AGED; BODY MASS; FEMALE; KAPLAN MEIER METHOD; MALE; MIDDLE AGED; MORTALITY; NEOPLASM; PROGNOSIS; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; BODY MASS INDEX; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; NEOPLASMS; PROGNOSIS; SARCOPENIA; YOUNG ADULT;

EID: 84957887273     PISSN: 09598049     EISSN: 18790852     Source Type: Journal    
DOI: 10.1016/j.ejca.2015.12.030     Document Type: Review

References (64)

1. R.N. Baumgartner, K.M. Koehler, D. Gallagher, L. Romero, S.B. Heymsfield, R.R. Ross, and et al. Epidemiology of sarcopenia among the elderly in New Mexico Am J Epidemiol 147 8 1998 755 763
2. V. Baracos, and S.M. Kazemi-Bajestani Clinical outcomes related to muscle mass in humans with cancer and catabolic illnesses Int J Biochem Cell Biol 45 10 2013 2302 2308
3. J.J. Tegels, J.L. van Vugt, K.W. Reisinger, K.W. Hulsewe, A.G. Hoofwijk, J.P. Derikx, and et al. Sarcopenia is highly prevalent in patients undergoing surgery for gastric cancer but not associated with worse outcomes J Surg Oncol 112 4 2015 403 407
4. P. Sharma, K. Zargar-Shoshtari, J.T. Caracciolo, M. Fishman, M.A. Poch, J. Pow-Sang, and et al. Sarcopenia as a predictor of overall survival after cytoreductive nephrectomy for metastatic renal cell carcinoma Urol Oncol 33 8 2015 339 e317-323
5. O. Mir, R. Coriat, B. Blanchet, J.P. Durand, P. Boudou-Rouquette, J. Michels, and et al. Sarcopenia predicts early dose-limiting toxicities and pharmacokinetics of sorafenib in patients with hepatocellular carcinoma PLoS One 7 5 2012 e37563
6. S.M. Kazemi-Bajestani, V.C. Mazurak, and V. Baracos Computed tomography-defined muscle and fat wasting are associated with cancer clinical outcomes Semin Cell Dev Biol 2015 10.1016/j.semcdb.2015.09.001
7. D. Moher, A. Liberati, J. Tetzlaff, and D.G. Altman Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement J Clin Epidemiol 62 10 2009 1006 1012
8. M.K. Parmar, V. Torri, and L. Stewart Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints Stat Med 17 24 1998 2815 2834
9. J.P. Higgins, S.G. Thompson, J.J. Deeks, and D.G. Altman Measuring inconsistency in meta-analyses BMJ 327 7414 2003 557 560
10. R. DerSimonian, and N. Laird Meta-analysis in clinical trials Control Clin Trials 7 3 1986 177 188
11. C.B. Begg, and M. Mazumdar Operating characteristics of a rank correlation test for publication bias Biometrics 50 4 1994 1088 1101
12. M. Egger, G. Davey Smith, M. Schneider, and C. Minder Bias in meta-analysis detected by a simple, graphical test BMJ 315 7109 1997 629 634
13. L. Martin, L. Birdsell, N. Macdonald, T. Reiman, M.T. Clandinin, L.J. McCargar, and 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 31 12 2013 1539 1547
14. M. Dhooge, R. Coriat, O. Mir, G. Perkins, C. Brezault, P. Boudou-Rouquette, and et al. Feasibility of gemcitabine plus oxaliplatin in advanced hepatocellular carcinoma patients with Child-Pugh B cirrhosis Oncology 84 1 2013 32 38
15. N. Fujiwara, H. Nakagawa, Y. Kudo, R. Tateishi, M. Taguri, T. Watadani, and et al. Sarcopenia, intramuscular fat deposition, and visceral adiposity independently predict the outcomes of hepatocellular carcinoma J Hepatol 63 1 2015 131 140
16. N. Harimoto, K. Shirabe, Y.I. Yamashita, T. Ikegami, T. Yoshizumi, Y. Soejima, and et al. Sarcopenia as a predictor of prognosis in patients following hepatectomy for hepatocellular carcinoma Br J Surg 100 11 2013 1523 1530
17. S. Iritani, K. Imai, K. Takai, T. Hanai, T. Ideta, T. Miyazaki, and et al. Skeletal muscle depletion is an independent prognostic factor for hepatocellular carcinoma J Gastroenterol 50 3 2015 323 332
18. S. Itoh, K. Shirabe, Y. Matsumoto, S. Yoshiya, J. Muto, N. Harimoto, and et al. Effect of body composition on outcomes after hepatic resection for hepatocellular carcinoma Ann Surg Oncol 21 9 2014 3063 3068
19. S. Kamachi, T. Mizuta, T. Otsuka, S. Nakashita, Y. Ide, A. Miyoshi, and et al. Sarcopenia is a risk factor for the recurrence of hepatocellular carcinoma after curative treatment Hepatol Res 2015 10.1111/hepr.12562
20. S. Levolger, M.G. van Vledder, R. Muslem, M. Koek, W.J. Niessen, R.A. de Man, and et al. Sarcopenia impairs survival in patients with potentially curable hepatocellular carcinoma J Surg Oncol 112 2 2015 208 213
21. J. Meza-Junco, A.J. Montano-Loza, V.E. Baracos, C.M. Prado, V.G. Bain, C. Beaumont, and et al. Sarcopenia as a prognostic index of nutritional status in concurrent cirrhosis and hepatocellular carcinoma J Clin Gastroenterol 47 10 2013 861 870
22. O. Mir, R. Coriat, P. Boudou-Rouquette, S. Ropert, J.P. Durand, A. Cessot, and et al. Gemcitabine and oxaliplatin as second-line treatment in patients with hepatocellular carcinoma pre-treated with sorafenib Med Oncol 29 4 2012 2793 2799
23. T. Voron, L. Tselikas, D. Pietrasz, F. Pigneur, A. Laurent, P. Compagnon, and et al. Sarcopenia impacts on short- and long-term results of hepatectomy for hepatocellular carcinoma Ann Surg 261 6 2015 1173 1183
24. Y. Choi, D.Y. Oh, T.Y. Kim, K.H. Lee, S.W. Han, S.A. Im, and et al. Skeletal muscle depletion predicts the prognosis of patients with advanced pancreatic cancer undergoing palliative chemotherapy, independent of body mass index PLoS One 10 10 2015 e0139749
25. A.B. Cooper, R. Slack, D. Fogelman, H.M. Holmes, M. Petzel, N. Parker, and et al. Characterization of anthropometric changes that occur during neoadjuvant therapy for potentially resectable pancreatic cancer Ann Surg Oncol 22 7 2015 2416 2423
26. S. Dalal, D. Hui, L. Bidaut, K. Lem, E. Del Fabbro, C. Crane, and et al. 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 Manage 44 2 2012 181 191
27. O. Mir, R. Coriat, M. Dhooge, G. Perkins, P. Boudou-Rouquette, C. Brezault, and et al. Feasibility of gemcitabine and oxaliplatin in patients with advanced biliary tract carcinoma and a performance status of 2 Anticancer Drugs 23 7 2012 739 744
28. K.E. Rollins, N. Tewari, A. Ackner, A. Awwad, S. Madhusudan, I.A. Macdonald, and et al. The impact of sarcopenia and myosteatosis on outcomes of unresectable pancreatic cancer or distal cholangiocarcinoma Clin Nutr 2015 10.1016/j.clnu.2015.08.005
29. B.H. Tan, L.A. Birdsell, L. Martin, V.E. Baracos, and K.C. Fearon Sarcopenia in an overweight or obese patient is an adverse prognostic factor in pancreatic cancer Clin Cancer Res 15 22 2009 6973 6979
30. K. Harada, S. Ida, Y. Baba, T. Ishimoto, K. Kosumi, R. Tokunaga, and et al. Prognostic and clinical impact of sarcopenia in esophageal squamous cell carcinoma Dis Esophagus 2015 10.1111/dote.12381
31. D. Tamandl, M. Paireder, R. Asari, P.A. Baltzer, S.F. Schoppmann, and A. Ba-Ssalamah Markers of sarcopenia quantified by computed tomography predict adverse long-term outcome in patients with resected oesophageal or gastro-oesophageal junction cancer Eur Radiol 2015 10.1007/s00330-015-3963-1
32. B.H. Tan, K. Brammer, N. Randhawa, N.T. Welch, S.L. Parsons, E.J. James, and et al. Sarcopenia is associated with toxicity in patients undergoing neo-adjuvant chemotherapy for oesophago-gastric cancer Eur J Surg Oncol 41 3 2015 333 338
33. C. Yip, V. Goh, A. Davies, J. Gossage, R. Mitchell-Hay, O. Hynes, and et al. Assessment of sarcopenia and changes in body composition after neoadjuvant chemotherapy and associations with clinical outcomes in oesophageal cancer Eur Radiol 24 5 2014 998 1005
34. H. Fukushima, M. Yokoyama, Y. Nakanishi, K. Tobisu, and F. Koga Sarcopenia as a prognostic biomarker of advanced urothelial carcinoma PLoS One 10 1 2015 e0115895
35. S.P. Psutka, S.A. Boorjian, M.R. Moynagh, G.D. Schmit, I. Frank, A. Carrasco, and et al. Mortality after radical cystectomy: impact of obesity versus adiposity after adjusting for skeletal muscle wasting J Urol 193 5 2015 1507 1513
36. S.P. Psutka, A. Carrasco, G.D. Schmit, M.R. Moynagh, S.A. Boorjian, I. Frank, and et al. Sarcopenia in patients with bladder cancer undergoing radical cystectomy: impact on cancer-specific and all-cause mortality Cancer 120 18 2014 2910 2918
37. S. Taguchi, N. Akamatsu, T. Nakagawa, W. Gonoi, A. Kanatani, H. Miyazaki, and et al. Sarcopenia evaluated using the skeletal muscle index is a significant prognostic factor for metastatic urothelial carcinoma Clin Genitourin Cancer 2015 10.1016/j.clgc.2015.07.015
38. H. Fukushima, Y. Nakanishi, M. Kataoka, K.I. Tobisu, and F. Koga Prognostic significance of sarcopenia in patients with metastatic renal cell carcinoma J Urol 195 1 2016 26 32
39. S.P. Psutka, S.A. Boorjian, M.R. Moynagh, G.D. Schmit, B.A. Costello, R.H. Thompson, and et al. Decreased skeletal muscle mass is associated with an increased risk of mortality after radical nephrectomy for localized renal cell cancer J Urol 195 2016 270 276
40. Y. Miyamoto, Y. Baba, Y. Sakamoto, M. Ohuchi, R. Tokunaga, J. Kurashige, and et al. Sarcopenia is a negative prognostic factor after curative resection of colorectal cancer Ann Surg Oncol 22 8 2015 2663 2668
41. L. Thoresen, G. Frykholm, S. Lydersen, H. Ulveland, V. Baracos, L. Birdsell, and et al. The association of nutritional assessment criteria with health-related quality of life in patients with advanced colorectal carcinoma Eur J Cancer Care (Engl) 21 4 2012 505 516
42. M.G. van Vledder, S. Levolger, N. Ayez, C. Verhoef, T.C. Tran, and J.N. Ijzermans Body composition and outcome in patients undergoing resection of colorectal liver metastases Br J Surg 99 4 2012 550 557
43. H.A. Parsons, A.M. Tsimberidou, M. Pontikos, S. Fu, D. Hong, S. Wen, and et al. Evaluation of the clinical relevance of body composition parameters in patients with cancer metastatic to the liver treated with hepatic arterial infusion chemotherapy Nutr Cancer 64 2 2012 206 217
44. H.A. Parsons, V.E. Baracos, N. Dhillon, D.S. Hong, and R. Kurzrock Body composition, symptoms, and survival in advanced cancer patients referred to a phase I service PLoS One 7 1 2012 e29330
45. C.M.M. Prado, J.R. Lieffers, L.J. McCargar, T. Reiman, M.B. Sawyer, L. Martin, and 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 9 7 2008 629 635
46. H. Veasey Rodrigues, V.E. Baracos, J.J. Wheler, H.A. Parsons, D.S. Hong, A. Naing, and et al. Body composition and survival in the early clinical trials setting Eur J Cancer 49 15 2013 3068 3075
47. P. Sharma, K. Zargar-Shoshtari, J.T. Caracciolo, G.J. Richard, M.A. Poch, J. Pow-Sang, and et al. Sarcopenia as a predictor of complications in penile cancer patients undergoing inguinal lymph node dissection World J Urol 33 10 2015 1585 1592
48. G.B. Stene, J.L. Helbostad, T. Amundsen, S. Sorhaug, H. Hjelde, S. Kaasa, and et al. Changes in skeletal muscle mass during palliative chemotherapy in patients with advanced lung cancer Acta Oncol 54 3 2015 340 348
49. H.K. Koo, J.H. Park, H.K. Park, H. Jung, and S.S. Lee Conflicting role of sarcopenia and obesity in male patients with chronic obstructive pulmonary disease: Korean National Health and Nutrition Examination Survey PLoS One 9 10 2014 e110448
50. M. Muscaritoli, S. Lucia, and A. Molfino Sarcopenia in critically ill patients: the new pandemia Minerva Anestesiol 79 7 2013 771 777
51. Y. Du, C.J. Karvellas, V. Baracos, D.C. Williams, and R.G. Khadaroo Sarcopenia is a predictor of outcomes in very elderly patients undergoing emergency surgery Surgery 156 3 2014 521 527
52. C.M. Prado, V.E. Baracos, L.J. McCargar, M. Mourtzakis, K.E. Mulder, T. Reiman, and et al. Body composition as an independent determinant of 5-fluorouracil-based chemotherapy toxicity Clin Cancer Res 13 11 2007 3264 3268
53. A.J. Cruz-Jentoft, J.P. Baeyens, J.M. Bauer, Y. Boirie, T. Cederholm, F. Landi, and et al. Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People Age Ageing 39 4 2010 412 423
54. Surveillance E, and end results (SEER) cancer stat fact sheets 2015 http://seer.cancer.gov/statfacts/ [accessed 18.11.15]
55. C.M. Prado, V.E. Baracos, L.J. McCargar, T. Reiman, M. Mourtzakis, K. Tonkin, and et al. Sarcopenia as a determinant of chemotherapy toxicity and time to tumor progression in metastatic breast cancer patients receiving capecitabine treatment Clin Cancer Res 15 8 2009 2920 2926
56. J.M. Argiles, S. Busquets, B. Stemmler, and F.J. Lopez-Soriano Cachexia and sarcopenia: mechanisms and potential targets for intervention Curr Opin Pharmacol 22 2015 100 106
57. A. Pratesi, F. Tarantini, and M. Di Bari Skeletal muscle: an endocrine organ Clin Cases Miner Bone Metab - Off J Italian Soc Osteoporos Mineral Metab Skelet Dis 10 1 2013 11 14
58. M. Maddocks, A.J. Murton, and A. Wilcock Improving muscle mass and function in cachexia: non-drug approaches Curr Opinion Support Palliat Care 5 4 2011 361 364
59. J.M. Argiles, S. Busquets, F.J. Lopez-Soriano, P. Costelli, and F. Penna Are there any benefits of exercise training in cancer cachexia? J Cachexia Sarcopenia Muscle 3 2 2012 73 76
60. F.G. Di Girolamo, R. Situlin, S. Mazzucco, R. Valentini, G. Toigo, and G. Biolo Omega-3 fatty acids and protein metabolism: enhancement of anabolic interventions for sarcopenia Curr Opin Clin Nutr Metab Care 17 2 2014 145 150
61. R. Dallmann, P. Weyermann, C. Anklin, M. Boroff, K. Bray-French, B. Cardel, and et al. The orally active melanocortin-4 receptor antagonist BL-6020/979: a promising candidate for the treatment of cancer cachexia J Cachexia Sarcopenia Muscle 2 3 2011 163 174
62. M. Grossmann Myostatin inhibition: a new treatment for androgen deprivation-induced sarcopenia? J Clin Endocrinol Metab 99 10 2014 3625 3628
63. E. Berardi, D. Annibali, M. Cassano, S. Crippa, and M. Sampaolesi Molecular and cell-based therapies for muscle degenerations: a road under construction Front Physiol 5 2014 119
64. T. Kung, J. Springer, W. Doehner, S.D. Anker, and S. von Haehling Novel treatment approaches to cachexia and sarcopenia: highlights from the 5th Cachexia Conference Expert Opin Investig Drugs 19 4 2010 579 585