DOI QR코드

DOI QR Code

Impact of Skeletal Muscle Loss and Visceral Obesity Measured Using Serial CT on the Prognosis of Operable Breast Cancers in Asian Patients

  • Mi-ri Kwon (Department of Radiology, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine) ;
  • Eun Sook Ko (Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Min Su Park (Department of Information and Statistics, Chungnam National University) ;
  • Woo Kyoung Jeong (Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Na Young Hwang (Statistics and Data Center, Research Institute for Future Medicine, Samsung Medical Center) ;
  • Jae-Hun Kim (Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Jeong Eon Lee (Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Seok Won Kim (Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Jong Han Yu (Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Boo-Kyung Han (Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Eun Young Ko (Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Ji Soo Choi (Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Ko Woon Park (Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine)
  • Received : 2020.12.19
  • Accepted : 2021.10.16
  • Published : 2022.02.01

Abstract

Objective: This study aimed to investigate the impact of baseline values and temporal changes in body composition parameters, including skeletal muscle index (SMI) and visceral adipose tissue area (VAT), measured using serial computed tomography (CT) imaging on the prognosis of operable breast cancers in Asian patients. Materials and Methods: This study retrospectively included 627 Asian female (mean age ± standard deviation [SD], 53.6 ± 8.3 years) who underwent surgery for stage I-III breast cancer between January 2011 and September 2012. Body composition parameters, including SMI and VAT, were semi-automatically calculated on baseline abdominal CT at the time of diagnosis and follow-up CT for post-treatment surveillance. Serial changes in SMI and VAT were calculated as the delta values. Multivariable Cox regression analysis was used to evaluate the association of baseline and delta SMI and VAT values with disease-free survival. Results: Among 627 patients, 56 patients (9.2%) had breast cancer recurrence after a median of 40.5 months. The mean value ± SD of the baseline SMI and baseline VAT were 43.7 ± 5.8 cm2/m2 and 72.0 ± 46.0 cm2, respectively. The mean value of the delta SMI was -0.9 cm2/m2 and the delta VAT was 0.5 cm2. The baseline SMI and VAT were not significantly associated with disease-free survival (adjusted hazard ratio [HR], 0.983; 95% confidence interval [CI], 0.937-1.031; p = 0.475 and adjusted HR, 1.001; 95% CI, 0.995-1.006; p = 0.751, respectively). The delta SMI and VAT were also not significantly associated with disease-free survival (adjusted HR, 0.894; 95% CI, 0.766-1.043; p = 0.155 and adjusted HR, 1.001; 95% CI, 0.989-1.014; p = 0.848, respectively). Conclusion: Our study revealed that baseline and early temporal changes in SMI and VAT were not independent prognostic factors regarding disease-free survival in Asian patients undergoing surgery for breast cancer.

Keywords

References

  1. Doherty TJ. Invited review: aging and sarcopenia. J Appl Physiol (1985) 2003;95:1717-1727 https://doi.org/10.1152/japplphysiol.00347.2003
  2. Baracos V, Kazemi-Bajestani SM. Clinical outcomes related to muscle mass in humans with cancer and catabolic illnesses. Int J Biochem Cell Biol 2013;45:2302-2308 https://doi.org/10.1016/j.biocel.2013.06.016
  3. Kazemi-Bajestani SM, Mazurak VC, Baracos V. Computed tomography-defined muscle and fat wasting are associated with cancer clinical outcomes. Semin Cell Dev Biol 2016;54:2-10 https://doi.org/10.1016/j.semcdb.2015.09.001
  4. Shachar SS, Williams GR, Muss HB, Nishijima TF. Prognostic value of sarcopenia in adults with solid tumours: a meta-analysis and systematic review. Eur J Cancer 2016;57:58-67 https://doi.org/10.1016/j.ejca.2015.12.030
  5. Williams GR, Rier HN, McDonald A, Shachar SS. Sarcopenia & aging in cancer. J Geriatr Oncol 2019;10:374-377 https://doi.org/10.1016/j.jgo.2018.10.009
  6. Tsai S. Importance of lean body mass in the oncologic patient. Nutr Clin Pract 2012;27:593-598 https://doi.org/10.1177/0884533612457949
  7. Aleixo GFP, Williams GR, Nyrop KA, Muss HB, Shachar SS. Muscle composition and outcomes in patients with breast cancer: meta-analysis and systematic review. Breast Cancer Res Treat 2019;177:569-579 https://doi.org/10.1007/s10549-019-05352-3
  8. Kwan ML, Chen WY, Kroenke CH, Weltzien EK, Beasley JM, Nechuta SJ, et al. Pre-diagnosis body mass index and survival after breast cancer in the after breast cancer pooling project. Breast Cancer Res Treat 2012;132:729-739 https://doi.org/10.1007/s10549-011-1914-3
  9. Protani M, Coory M, Martin JH. Effect of obesity on survival of women with breast cancer: systematic review and meta-analysis. Breast Cancer Res Treat 2010;123:627-635 https://doi.org/10.1007/s10549-010-0990-0
  10. Litton JK, Gonzalez-Angulo AM, Warneke CL, Buzdar AU, Kau SW, Bondy M, et al. Relationship between obesity and pathologic response to neoadjuvant chemotherapy among women with operable breast cancer. J Clin Oncol 2008;26:4072-4077 https://doi.org/10.1200/JCO.2007.14.4527
  11. Del Fabbro E, Parsons H, Warneke CL, Pulivarthi K, Litton JK, Dev R, et al. The relationship between body composition and response to neoadjuvant chemotherapy in women with operable breast cancer. Oncologist 2012;17:1240-1245 https://doi.org/10.1634/theoncologist.2012-0169
  12. Fang Q, Huang J, Gan L, Shen K, Chen X, Wu B. Weight gain during neoadjuvant chemotherapy is associated with worse outcome among the patients with operable breast cancer. J Breast Cancer 2019;22:399-411 https://doi.org/10.4048/jbc.2019.22.e37
  13. 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;33:997-1006 https://doi.org/10.1139/H08-075
  14. Shen W, Punyanitya M, Wang Z, Gallagher D, St-Onge MP, Albu J, et al. Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image. J Appl Physiol (1985) 2004;97:2333-2338 https://doi.org/10.1152/japplphysiol.00744.2004
  15. Rossi F, Valdora F, Bignotti B, Torri L, Succio G, Tagliafico AS. Evaluation of body computed tomography-determined sarcopenia in breast cancer patients and clinical outcomes: a systematic review. Cancer Treat Res Commun 2019;21:100154
  16. Kim MS, Choi YJ, Lee YH. Visceral fat measured by computed tomography and the risk of breast cancer. Transl Cancer Res 2019;8:1939-1949 https://doi.org/10.21037/tcr.2019.09.16
  17. Iwase T, Sangai T, Nagashima T, Sakakibara M, Sakakibara J, Hayama S, et al. Impact of body fat distribution on neoadjuvant chemotherapy outcomes in advanced breast cancer patients. Cancer Med 2016;5:41-48 https://doi.org/10.1002/cam4.571
  18. Schapira DV, Clark RA, Wolff PA, Jarrett AR, Kumar NB, Aziz NM. Visceral obesity and breast cancer risk. Cancer 1994;74:632-639
  19. Caan BJ, Cespedes Feliciano EM, Prado CM, Alexeeff S, Kroenke CH, Bradshaw P, et al. Association of muscle and adiposity measured by computed tomography with survival in patients with nonmetastatic breast cancer. JAMA Oncol 2018;4:798-804 https://doi.org/10.1001/jamaoncol.2018.0137
  20. Kim SS, Kim JH, Jeong WK, Lee J, Kim YK, Choi D, et al. Semiautomatic software for measurement of abdominal muscle and adipose areas using computed tomography: a STROBE-compliant article. Medicine (Baltimore) 2019;98:e15867
  21. Rier HN, Jager A, Sleijfer S, van Rosmalen J, Kock MCJM, Levin MD. Low muscle attenuation is a prognostic factor for survival in metastatic breast cancer patients treated with first line palliative chemotherapy. Breast 2017;31:9-15 https://doi.org/10.1016/j.breast.2016.10.014
  22. Voduc KD, Cheang MC, Tyldesley S, Gelmon K, Nielsen TO, Kennecke H. Breast cancer subtypes and the risk of local and regional relapse. J Clin Oncol 2010;28:1684-1691 https://doi.org/10.1200/JCO.2009.24.9284
  23. Bustreo S, Osella-Abate S, Cassoni P, Donadio M, Airoldi M, Pedani F, et al. Optimal Ki67 cut-off for luminal breast cancer prognostic evaluation: a large case series study with a long-term follow-up. Breast Cancer Res Treat 2016;157:363-371 https://doi.org/10.1007/s10549-016-3817-9
  24. Guiu S, Michiels S, Andre F, Cortes J, Denkert C, Di Leo A, et al. Molecular subclasses of breast cancer: how do we define them? The IMPAKT 2012 working group statement. Ann Oncol 2012;23:2997-3006 https://doi.org/10.1093/annonc/mds586
  25. Zhou ZR, Wang WW, Li Y, Jin KR, Wang XY, Wang ZW, et al. In-depth mining of clinical data: the construction of clinical prediction model with R. Ann Transl Med 2019;7:796
  26. Caan BJ, Emond JA, Natarajan L, Castillo A, Gunderson EP, Habel L, et al. Post-diagnosis weight gain and breast cancer recurrence in women with early stage breast cancer. Breast Cancer Res Treat 2006;99:47-57 https://doi.org/10.1007/s10549-006-9179-y
  27. Mazzuca F, Onesti CE, Roberto M, Di Girolamo M, Botticelli A, Begini P, et al. Lean body mass wasting and toxicity in early breast cancer patients receiving anthracyclines. Oncotarget 2018;9:25714-25722 https://doi.org/10.18632/oncotarget.25394
  28. Rier HN, Jager A, Sleijfer S, van Rosmalen J, Kock MCJM, Levin MD. Changes in body composition and muscle attenuation during taxane-based chemotherapy in patients with metastatic breast cancer. Breast Cancer Res Treat 2018;168:95-105 https://doi.org/10.1007/s10549-017-4574-0
  29. Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, et al. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc 2014;15:95-101 https://doi.org/10.1016/j.jamda.2013.11.025
  30. Wu YH, Hwang AC, Liu LK, Peng LN, Chen LK. Sex differences of sarcopenia in Asian populations: the implications in diagnosis and management. J Clin Gerontol Geriatr 2016;7:37-43 https://doi.org/10.1016/j.jcgg.2016.04.001
  31. WHO Expert Consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 2004;363:157-163 https://doi.org/10.1016/S0140-6736(03)15268-3
  32. Park J, Euhus DM, Scherer PE. Paracrine and endocrine effects of adipose tissue on cancer development and progression. Endocr Rev 2011;32:550-570 https://doi.org/10.1210/er.2010-0030
  33. Park J, Morley TS, Kim M, Clegg DJ, Scherer PE. Obesity and cancer--mechanisms underlying tumour progression and recurrence. Nat Rev Endocrinol 2014;10:455-465 https://doi.org/10.1038/nrendo.2014.94
  34. Dirat B, Bochet L, Dabek M, Daviaud D, Dauvillier S, Majed B, et al. Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res 2011;71:2455-2465 https://doi.org/10.1158/0008-5472.CAN-10-3323
  35. Ibrahim MM. Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev 2010;11:11-18 https://doi.org/10.1111/j.1467-789X.2009.00623.x
  36. Chen GC, Chen SJ, Zhang R, Hidayat K, Qin JB, Zhang YS, et al. Central obesity and risks of pre- and postmenopausal breast cancer: a dose-response meta-analysis of prospective studies. Obes Rev 2016;17:1167-1177 https://doi.org/10.1111/obr.12443
  37. Griner SE, Wang KJ, Joshi JP, Nahta R. Mechanisms of adipocytokine-mediated trastuzumab resistance in HER2-positive breast cancer cell lines. Curr Pharmacogenomics Person Med 2013;11:31-41 https://doi.org/10.2174/1875692111311010006
  38. Joshi JP, Brown NE, Griner SE, Nahta R. Growth differentiation factor 15 (GDF15)-mediated HER2 phosphorylation reduces trastuzumab sensitivity of HER2-overexpressing breast cancer cells. Biochem Pharmacol 2011;82:1090-1099 https://doi.org/10.1016/j.bcp.2011.07.082
  39. Soma D, Kitayama J, Yamashita H, Miyato H, Ishikawa M, Nagawa H. Leptin augments proliferation of breast cancer cells via transactivation of HER2. J Surg Res 2008;149:9-14 https://doi.org/10.1016/j.jss.2007.10.012
  40. Crozier JA, Moreno-Aspitia A, Ballman KV, Dueck AC, Pockaj BA, Perez EA. Effect of body mass index on tumor characteristics and disease-free survival in patients from the HER2-positive adjuvant trastuzumab trial N9831. Cancer 2013;119:2447-2454