Skip to main content
Top
Published in: Supportive Care in Cancer 11/2017

01-11-2017 | Original Article

Factors which modulate the rates of skeletal muscle mass loss in non-small cell lung cancer patients: a pilot study

Authors: Philippe Atlan, Mohamed Amine Bayar, Emilie Lanoy, Benjamin Besse, David Planchard, Jordy Ramon, Bruno Raynard, Sami Antoun

Published in: Supportive Care in Cancer | Issue 11/2017

Login to get access

Abstract

Purpose

Advanced non-small cell lung cancer (NSCLC) is associated with weight loss which may reflect skeletal muscle mass (SMM) and/or total adipose tissue (TAT) depletion. This study aimed to describe changes in body composition (BC) parameters and to identify the factors unrelated to the tumor which modulate them.

Methods

SMM, TAT, and the proportion of SMM to SMM + TAT were assessed with computed tomography. Estimates of each BC parameter at follow-up initiation and across time were derived from a mixed linear model of repeated measurements with a random intercept and a random slope. The same models were used to assess the independent effect of gender, age, body mass index (BMI), and initial values on changes in each BC parameter.

Results

Sixty-four patients with stage III or IV NSCLC were reviewed. The mean ± SD decreases in body weight and SMM were respectively 59 ± 3 g/week (P < 0.03) and 7 mm2/m2/week (P = 0.0003). During follow-up, no changes were identified in TAT nor in muscle density or in the proportion of SMM to SMM + TAT, estimated at 37 ± 2% at baseline. SMM loss was influenced by initial BMI (P < 0.0001) and SMM values (P = 0.0002): the higher the initial BMI or SMM values, the greater the loss observed. Weight loss was greater when the initial weight was heavier (P < 0.0001).

Conclusion

Our results demonstrate that SMM wasting in NSCLC is lower when initial SMM and BMI values are low. These exploratory findings after our attempt to better understand the intrinsic factors associated with muscle mass depletion need to be confirmed in larger studies.
Literature
1.
go back to reference Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136(5):E359–E386. doi:10.1002/ijc.29210 CrossRef Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136(5):E359–E386. doi:10.​1002/​ijc.​29210 CrossRef
2.
go back to reference Brundage MD, Davies D, Mackillop WJ (2002) Prognostic factors in non-small cell lung cancer: a decade of progress. Chest 122(3):1037–1057CrossRef Brundage MD, Davies D, Mackillop WJ (2002) Prognostic factors in non-small cell lung cancer: a decade of progress. Chest 122(3):1037–1057CrossRef
3.
go back to reference Mountain CF (1993) Lung cancer staging classification. Clin Chest Med 14(1):43–53PubMed Mountain CF (1993) Lung cancer staging classification. Clin Chest Med 14(1):43–53PubMed
4.
go back to reference Nourissat A, Bairati I, Fortin A, Gelinas M, Nabid A, Brochet F, Tetu B, Meyer F (2012) Factors associated with weight loss during radiotherapy in patients with stage I or II head and neck cancer. Support Care Cancer: Off J Multinatl Assoc Support Care Cancer 20(3):591–599. doi:10.1007/s00520-011-1132-x CrossRef Nourissat A, Bairati I, Fortin A, Gelinas M, Nabid A, Brochet F, Tetu B, Meyer F (2012) Factors associated with weight loss during radiotherapy in patients with stage I or II head and neck cancer. Support Care Cancer: Off J Multinatl Assoc Support Care Cancer 20(3):591–599. doi:10.​1007/​s00520-011-1132-x CrossRef
5.
go back to reference Scott HR, McMillan DC, Brown DJ, Forrest LM, McArdle CS, Milroy R (2003) A prospective study of the impact of weight loss and the systemic inflammatory response on quality of life in patients with inoperable non-small cell lung cancer. Lung Cancer 40(3):295–299CrossRef Scott HR, McMillan DC, Brown DJ, Forrest LM, McArdle CS, Milroy R (2003) A prospective study of the impact of weight loss and the systemic inflammatory response on quality of life in patients with inoperable non-small cell lung cancer. Lung Cancer 40(3):295–299CrossRef
8.
go back to reference Prado CM, Baracos VE, McCargar LJ, Reiman T, Mourtzakis M, Tonkin K, Mackey JR, Koski S, Pituskin E, Sawyer MB (2009) Sarcopenia as a determinant of chemotherapy toxicity and time to tumor progression in metastatic breast cancer patients receiving Capecitabine treatment. Clin Cancer Res: Off J Am Assoc Cancer Res 15(8):2920–2926. doi:10.1158/1078-0432.CCR-08-2242 CrossRef Prado CM, Baracos VE, McCargar LJ, Reiman T, Mourtzakis M, Tonkin K, Mackey JR, Koski S, Pituskin E, Sawyer MB (2009) Sarcopenia as a determinant of chemotherapy toxicity and time to tumor progression in metastatic breast cancer patients receiving Capecitabine treatment. Clin Cancer Res: Off J Am Assoc Cancer Res 15(8):2920–2926. doi:10.​1158/​1078-0432.​CCR-08-2242 CrossRef
9.
go back to reference Martin L, Birdsell L, Macdonald N, Reiman T, Clandinin MT, McCargar LJ, Murphy R, Ghosh S, Sawyer MB, Baracos VE (2013) 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):1539–1547. doi:10.1200/JCO.2012.45.2722 CrossRefPubMed Martin L, Birdsell L, Macdonald N, Reiman T, Clandinin MT, McCargar LJ, Murphy R, Ghosh S, Sawyer MB, Baracos VE (2013) 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):1539–1547. doi:10.​1200/​JCO.​2012.​45.​2722 CrossRefPubMed
10.
go back to reference Chemama S, Bayar MA, Lanoy E, Ammari S, Stoclin A, Goere D, Elias D, Raynard B, Antoun S (2016) Sarcopenia is associated with chemotherapy toxicity in patients undergoing cytoreductive surgery with hyperthermic intraperitoneal chemotherapy for peritoneal carcinomatosis from colorectal cancer. Ann Surg Oncol. doi:10.1245/s10434-016-5360-7 CrossRef Chemama S, Bayar MA, Lanoy E, Ammari S, Stoclin A, Goere D, Elias D, Raynard B, Antoun S (2016) Sarcopenia is associated with chemotherapy toxicity in patients undergoing cytoreductive surgery with hyperthermic intraperitoneal chemotherapy for peritoneal carcinomatosis from colorectal cancer. Ann Surg Oncol. doi:10.​1245/​s10434-016-5360-7 CrossRef
12.
go back to reference Cousin S, Hollebecque A, Koscielny S, Mir O, Varga A, Baracos VE, Soria JC, Antoun S (2014) Low skeletal muscle is associated with toxicity in patients included in phase I trials. Investig New Drugs 32(2):382–387. doi:10.1007/s10637-013-0053-6 CrossRef Cousin S, Hollebecque A, Koscielny S, Mir O, Varga A, Baracos VE, Soria JC, Antoun S (2014) Low skeletal muscle is associated with toxicity in patients included in phase I trials. Investig New Drugs 32(2):382–387. doi:10.​1007/​s10637-013-0053-6 CrossRef
14.
go back to reference Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E, Fainsinger RL, Jatoi A, Loprinzi C, MacDonald N, Mantovani G, Davis M, Muscaritoli M, Ottery F, Radbruch L, Ravasco P, Walsh D, Wilcock A, Kaasa S, Baracos VE (2011) Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 12(5):489–495. doi:10.1016/S1470-2045(10)70218-7 CrossRefPubMed Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E, Fainsinger RL, Jatoi A, Loprinzi C, MacDonald N, Mantovani G, Davis M, Muscaritoli M, Ottery F, Radbruch L, Ravasco P, Walsh D, Wilcock A, Kaasa S, Baracos VE (2011) Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 12(5):489–495. doi:10.​1016/​S1470-2045(10)70218-7 CrossRefPubMed
15.
go back to reference Baracos VE, Reiman T, Mourtzakis M, Gioulbasanis I, Antoun S (2010) Body composition in patients with non-small cell lung cancer: a contemporary view of cancer cachexia with the use of computed tomography image analysis. Am J Clin Nutr 91(4):1133S–1137S. doi:10.3945/ajcn.2010.28608C CrossRefPubMed Baracos VE, Reiman T, Mourtzakis M, Gioulbasanis I, Antoun S (2010) Body composition in patients with non-small cell lung cancer: a contemporary view of cancer cachexia with the use of computed tomography image analysis. Am J Clin Nutr 91(4):1133S–1137S. doi:10.​3945/​ajcn.​2010.​28608C CrossRefPubMed
16.
go back to reference Barber MD, McMillan DC, Preston T, Ross JA, Fearon KC (2000) Metabolic response to feeding in weight-losing pancreatic cancer patients and its modulation by a fish-oil-enriched nutritional supplement. Clin Sci 98(4):389–399CrossRef Barber MD, McMillan DC, Preston T, Ross JA, Fearon KC (2000) Metabolic response to feeding in weight-losing pancreatic cancer patients and its modulation by a fish-oil-enriched nutritional supplement. Clin Sci 98(4):389–399CrossRef
17.
go back to reference Lieffers JR, Mourtzakis M, Hall KD, McCargar LJ, Prado CM, Baracos VE (2009) A viscerally driven cachexia syndrome in patients with advanced colorectal cancer: contributions of organ and tumor mass to whole-body energy demands. Am J Clin Nutr 89(4):1173–1179. doi:10.3945/ajcn.2008.27273 CrossRefPubMedPubMedCentral Lieffers JR, Mourtzakis M, Hall KD, McCargar LJ, Prado CM, Baracos VE (2009) A viscerally driven cachexia syndrome in patients with advanced colorectal cancer: contributions of organ and tumor mass to whole-body energy demands. Am J Clin Nutr 89(4):1173–1179. doi:10.​3945/​ajcn.​2008.​27273 CrossRefPubMedPubMedCentral
18.
go back to reference Prado CM, Sawyer MB, Ghosh S, Lieffers JR, Esfandiari N, Antoun S, Baracos VE (2013) Central tenet of cancer cachexia therapy: do patients with advanced cancer have exploitable anabolic potential? Am J Clin Nutr 98(4):1012–1019. doi:10.3945/ajcn.113.060228 CrossRefPubMed Prado CM, Sawyer MB, Ghosh S, Lieffers JR, Esfandiari N, Antoun S, Baracos VE (2013) Central tenet of cancer cachexia therapy: do patients with advanced cancer have exploitable anabolic potential? Am J Clin Nutr 98(4):1012–1019. doi:10.​3945/​ajcn.​113.​060228 CrossRefPubMed
19.
go back to reference Prado CM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB, Martin L, Baracos VE (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(7):629–635. doi:10.1016/S1470-2045(08)70153-0 CrossRefPubMed Prado CM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB, Martin L, Baracos VE (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(7):629–635. doi:10.​1016/​S1470-2045(08)70153-0 CrossRefPubMed
21.
go back to reference Baracos VE, Reiman T, Mourtzakis M, Gioulbasanis I, Antoun S (2010) Body composition in patients with non-small cell lung cancer: a contemporary view of cancer cachexia with the use of computed tomography image analysis. Am J Clin Nutr 91(4):1133S–1137S. doi:10.3945/ajcn.2010.28608C CrossRefPubMed Baracos VE, Reiman T, Mourtzakis M, Gioulbasanis I, Antoun S (2010) Body composition in patients with non-small cell lung cancer: a contemporary view of cancer cachexia with the use of computed tomography image analysis. Am J Clin Nutr 91(4):1133S–1137S. doi:10.​3945/​ajcn.​2010.​28608C CrossRefPubMed
22.
go back to reference Palomares MR, Sayre JW, Shekar KC, Lillington LM, Chlebowski RT (1996) Gender influence on weight-loss pattern and survival of nonsmall cell lung carcinoma patients. Cancer 78(10):2119–2126CrossRef Palomares MR, Sayre JW, Shekar KC, Lillington LM, Chlebowski RT (1996) Gender influence on weight-loss pattern and survival of nonsmall cell lung carcinoma patients. Cancer 78(10):2119–2126CrossRef
24.
go back to reference Patel JD, Pereira JR, Chen J, Liu J, Guba SC, John WJ, Orlando M, Scagliotti G, Bonomi PD (2016) Relationship between efficacy outcomes and weight gain during treatment of advanced, non-squamous, non-small-cell lung cancer patients. Ann Oncol: Off J Eur Soc Med Oncol/ ESMO. doi:10.1093/annonc/mdw211 CrossRef Patel JD, Pereira JR, Chen J, Liu J, Guba SC, John WJ, Orlando M, Scagliotti G, Bonomi PD (2016) Relationship between efficacy outcomes and weight gain during treatment of advanced, non-squamous, non-small-cell lung cancer patients. Ann Oncol: Off J Eur Soc Med Oncol/ ESMO. doi:10.​1093/​annonc/​mdw211 CrossRef
25.
go back to reference Di Sebastiano KM, Yang L, Zbuk K, Wong RK, Chow T, Koff D, Moran GR, Mourtzakis M (2013) Accelerated muscle and adipose tissue loss may predict survival in pancreatic cancer patients: the relationship with diabetes and anaemia. Br J Nutr 109(2):302–312. doi:10.1017/S0007114512001067 CrossRefPubMed Di Sebastiano KM, Yang L, Zbuk K, Wong RK, Chow T, Koff D, Moran GR, Mourtzakis M (2013) Accelerated muscle and adipose tissue loss may predict survival in pancreatic cancer patients: the relationship with diabetes and anaemia. Br J Nutr 109(2):302–312. doi:10.​1017/​S000711451200106​7 CrossRefPubMed
28.
go back to reference Goldbohm RA, Voorrips LE (2000) Epidemiology of nutrition and lung cancer. Nestle Nutr Workshop Ser Clin Perform Programme 4:23–35 discussion 35-27CrossRef Goldbohm RA, Voorrips LE (2000) Epidemiology of nutrition and lung cancer. Nestle Nutr Workshop Ser Clin Perform Programme 4:23–35 discussion 35-27CrossRef
31.
go back to reference Antoun S, Lanoy E, Iacovelli R, Albiges-Sauvin L, Loriot Y, Merad-Taoufik M, Fizazi K, di Palma M, Baracos VE, Escudier B (2013) Skeletal muscle density predicts prognosis in patients with metastatic renal cell carcinoma treated with targeted therapies. Cancer 119(18):3377–3384. doi:10.1002/cncr.28218 CrossRefPubMed Antoun S, Lanoy E, Iacovelli R, Albiges-Sauvin L, Loriot Y, Merad-Taoufik M, Fizazi K, di Palma M, Baracos VE, Escudier B (2013) Skeletal muscle density predicts prognosis in patients with metastatic renal cell carcinoma treated with targeted therapies. Cancer 119(18):3377–3384. doi:10.​1002/​cncr.​28218 CrossRefPubMed
32.
go back to reference Shen W, Punyanitya M, Wang Z, Gallagher D, St-Onge MP, Albu J, Heymsfield SB, Heshka S (2004) Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image. J Appl Physiol (Bethesda, Md : 1985) 97(6):2333–2338. doi:10.1152/japplphysiol.00744.2004 CrossRef Shen W, Punyanitya M, Wang Z, Gallagher D, St-Onge MP, Albu J, Heymsfield SB, Heshka S (2004) Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image. J Appl Physiol (Bethesda, Md : 1985) 97(6):2333–2338. doi:10.​1152/​japplphysiol.​00744.​2004 CrossRef
33.
go back to reference Goodpaster BH, Kelley DE, Thaete FL, He J, Ross R (2000) Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J Appl Physiol (Bethesda, Md : 1985) 89(1):104–110CrossRef Goodpaster BH, Kelley DE, Thaete FL, He J, Ross R (2000) Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J Appl Physiol (Bethesda, Md : 1985) 89(1):104–110CrossRef
36.
go back to reference Williams JP, Phillips BE, Smith K, Atherton PJ, Rankin D, Selby AL, Liptrot S, Lund J, Larvin M, Rennie MJ (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(5):1064–1070. doi:10.3945/ajcn.112.045708 CrossRefPubMed Williams JP, Phillips BE, Smith K, Atherton PJ, Rankin D, Selby AL, Liptrot S, Lund J, Larvin M, Rennie MJ (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(5):1064–1070. doi:10.​3945/​ajcn.​112.​045708 CrossRefPubMed
37.
go back to reference Gallagher D, Visser M, De Meersman RE, Sepulveda D, Baumgartner RN, Pierson RN, Harris T, Heymsfield SB (1997) Appendicular skeletal muscle mass: effects of age, gender, and ethnicity. J Appl Physiol (Bethesda, Md : 1985) 83(1):229–239CrossRef Gallagher D, Visser M, De Meersman RE, Sepulveda D, Baumgartner RN, Pierson RN, Harris T, Heymsfield SB (1997) Appendicular skeletal muscle mass: effects of age, gender, and ethnicity. J Appl Physiol (Bethesda, Md : 1985) 83(1):229–239CrossRef
39.
go back to reference Wallengren O, Iresjo BM, Lundholm K, Bosaeus I (2015) Loss of muscle mass in the end of life in patients with advanced cancer. Support Care Cancer: Off J Multinatl Assoc Support Care Cancer 23(1):79–86. doi:10.1007/s00520-014-2332-y CrossRef Wallengren O, Iresjo BM, Lundholm K, Bosaeus I (2015) Loss of muscle mass in the end of life in patients with advanced cancer. Support Care Cancer: Off J Multinatl Assoc Support Care Cancer 23(1):79–86. doi:10.​1007/​s00520-014-2332-y CrossRef
40.
41.
go back to reference Forbes GB (2000) Body fat content influences the body composition response to nutrition and exercise. Ann N Y Acad Sci 904:359–365CrossRef Forbes GB (2000) Body fat content influences the body composition response to nutrition and exercise. Ann N Y Acad Sci 904:359–365CrossRef
43.
go back to reference Casaer MP, Langouche L, Coudyzer W, Vanbeckevoort D, De Dobbelaer B, Guiza FG, Wouters PJ, Mesotten D, Van den Berghe G (2013) Impact of early parenteral nutrition on muscle and adipose tissue compartments during critical illness. Crit Care Med 41(10):2298–2309. doi:10.1097/CCM.0b013e31828cef02 CrossRefPubMed Casaer MP, Langouche L, Coudyzer W, Vanbeckevoort D, De Dobbelaer B, Guiza FG, Wouters PJ, Mesotten D, Van den Berghe G (2013) Impact of early parenteral nutrition on muscle and adipose tissue compartments during critical illness. Crit Care Med 41(10):2298–2309. doi:10.​1097/​CCM.​0b013e31828cef02​ CrossRefPubMed
44.
go back to reference Dietze D, Ramrath S, Ritzeler O, Tennagels N, Hauner H, Eckel J (2004) Inhibitor kappaB kinase is involved in the paracrine crosstalk between human fat and muscle cells. Int J Obes Relat Metab Disord: J Int Assoc Study Obes 28(8):985–992. doi:10.1038/sj.ijo.0802701 CrossRef Dietze D, Ramrath S, Ritzeler O, Tennagels N, Hauner H, Eckel J (2004) Inhibitor kappaB kinase is involved in the paracrine crosstalk between human fat and muscle cells. Int J Obes Relat Metab Disord: J Int Assoc Study Obes 28(8):985–992. doi:10.​1038/​sj.​ijo.​0802701 CrossRef
45.
go back to reference Das SK, Eder S, Schauer S, Diwoky C, Temmel H, Guertl B, Gorkiewicz G, Tamilarasan KP, Kumari P, Trauner M, Zimmermann R, Vesely P, Haemmerle G, Zechner R, Hoefler G (2011) Adipose triglyceride lipase contributes to cancer-associated cachexia. Science 333(6039):233–238. doi:10.1126/science.1198973 CrossRefPubMed Das SK, Eder S, Schauer S, Diwoky C, Temmel H, Guertl B, Gorkiewicz G, Tamilarasan KP, Kumari P, Trauner M, Zimmermann R, Vesely P, Haemmerle G, Zechner R, Hoefler G (2011) Adipose triglyceride lipase contributes to cancer-associated cachexia. Science 333(6039):233–238. doi:10.​1126/​science.​1198973 CrossRefPubMed
46.
go back to reference Akahori T, Sho M, Kinoshita S, Nagai M, Nishiwada S, Tanaka T, Tamamoto T, Ohbayashi C, Hasegawa M, Kichikawa K, Nakajima Y (2015) Prognostic significance of muscle attenuation in pancreatic cancer patients treated with neoadjuvant chemoradiotherapy. World J Surg 39(12):2975–2982. doi:10.1007/s00268-015-3205-3 CrossRefPubMed Akahori T, Sho M, Kinoshita S, Nagai M, Nishiwada S, Tanaka T, Tamamoto T, Ohbayashi C, Hasegawa M, Kichikawa K, Nakajima Y (2015) Prognostic significance of muscle attenuation in pancreatic cancer patients treated with neoadjuvant chemoradiotherapy. World J Surg 39(12):2975–2982. doi:10.​1007/​s00268-015-3205-3 CrossRefPubMed
Metadata
Title
Factors which modulate the rates of skeletal muscle mass loss in non-small cell lung cancer patients: a pilot study
Authors
Philippe Atlan
Mohamed Amine Bayar
Emilie Lanoy
Benjamin Besse
David Planchard
Jordy Ramon
Bruno Raynard
Sami Antoun
Publication date
01-11-2017
Publisher
Springer Berlin Heidelberg
Published in
Supportive Care in Cancer / Issue 11/2017
Print ISSN: 0941-4355
Electronic ISSN: 1433-7339
DOI
https://doi.org/10.1007/s00520-017-3755-z

Other articles of this Issue 11/2017

Supportive Care in Cancer 11/2017 Go to the issue

Letter to the editor

Author’s response

Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine