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Prognostic Value of Artificial Intelligence-Driven, Computed Tomography-Based, Volumetric Assessment of the Volume and Density of Muscle in Patients With Colon Cancer

  • Minsung Kim (Department of Surgery, Hallym University Sacred Heart Hospital, Hallym University College of Medicine) ;
  • Sang Min Lee (Department of Radiology, CHA University Gangnam Medical Center) ;
  • Il Tae Son (Department of Surgery, Hallym University Sacred Heart Hospital, Hallym University College of Medicine) ;
  • Taeyong Park (Medical Artificial Intelligence Center, Hallym University Sacred Heart Hospital, Hallym University College of Medicine) ;
  • Bo Young Oh (Department of Surgery, Hallym University Sacred Heart Hospital, Hallym University College of Medicine)
  • Received : 2022.11.01
  • Accepted : 2023.06.28
  • Published : 2023.09.01

Abstract

Objective: The prognostic value of the volume and density of skeletal muscles in the abdominal waist of patients with colon cancer remains unclear. This study aimed to investigate the association between the automated computed tomography (CT)-based volume and density of the muscle in the abdominal waist and survival outcomes in patients with colon cancer. Materials and Methods: We retrospectively evaluated 474 patients with colon cancer who underwent surgery with curative intent between January 2010 and October 2017. Volumetric skeletal muscle index and muscular density were measured at the abdominal waist using artificial intelligence (AI)-based volumetric segmentation of body composition on preoperative pre-contrast CT images. Patients were grouped based on their skeletal muscle index (sarcopenia vs. not) and muscular density (myosteatosis vs. not) values and combinations (normal, sarcopenia alone, myosteatosis alone, and combined sarcopenia and myosteatosis). Postsurgical disease-free survival (DFS) and overall survival (OS) were analyzed using univariable and multivariable analyses, including multivariable Cox proportional hazard regression. Results: Univariable analysis showed that DFS and OS were significantly worse for the sarcopenia group than for the non-sarcopenia group (P = 0.044 and P = 0.003, respectively, by log-rank test) and for the myosteatosis group than for the non-myosteatosis group (P < 0.001 by log-rank test for all). In the multivariable analysis, the myosteatotic muscle type was associated with worse DFS (adjusted hazard ratio [aHR], 1.89 [95% confidence interval, 1.25-2.86]; P = 0.003) and OS (aHR, 1.90 [95% confidence interval, 1.84-3.04]; P = 0.008) than the normal muscle type. The combined muscle type showed worse OS than the normal muscle type (aHR, 1.95 [95% confidence interval, 1.08-3.54]; P = 0.027). Conclusion: Preoperative volumetric sarcopenia and myosteatosis, automatically assessed from pre-contrast CT scans using AI-based software, adversely affect survival outcomes in patients with colon cancer.

Keywords

Acknowledgement

This research was supported by the Hallym University Research Fund 2020 (HURF-2020-39).

References

  1. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021;71:209-249 
  2. Fleming CA, O'Connell EP, Kavanagh RG, O'Leary DP, Twomey M, Corrigan MA, et al. Body composition, inflammation, and 5-year outcomes in colon cancer. JAMA Netw Open 2021;4:e2115274 
  3. Chai VW, Chia M, Cocco A, Bhamidipaty M, D'Souza B. Sarcopenia is a strong predictive factor of clinical and oncological outcomes following curative colorectal cancer resection. ANZ J Surg 2021;91:E292-E297 
  4. Malietzis G, Currie AC, Athanasiou T, Johns N, Anyamene N, Glynne-Jones R, et al. Influence of body composition profile on outcomes following colorectal cancer surgery. Br J Surg 2016;103:572-580 
  5. Sueda T, Takahasi H, Nishimura J, Hata T, Matsuda C, Mizushima T, et al. Impact of low muscularity and myosteatosis on long-term outcome after curative colorectal cancer surgery: a propensity score-matched analysis. Dis Colon Rectum 2018;61:364-374 
  6. Hopkins JJ, Reif RL, Bigam DL, Baracos VE, Eurich DT, Sawyer MB. The impact of muscle and adipose tissue on long-term survival in patients with stage I to III colorectal cancer. Dis Colon Rectum 2019;62:549-560 
  7. Sonmez O, Tezcanli E, Bas D, Kazanci HB, Altinok A, Demir A, et al. Identifying knowledge and practices regarding cancer patient malnutrition: a survey study among oncologists. Nutr Cancer 2022;74:2392-2399 
  8. Han Q, Kim SI, Yoon SH, Kim TM, Kang HC, Kim HJ, et al. Impact of computed tomography-based, artificial intelligence-driven volumetric sarcopenia on survival outcomes in early cervical cancer. Front Oncol 2021;11:741071 
  9. Kim SI, Chung JY, Paik H, Seol A, Yoon SH, Kim TM, et al. Prognostic role of computed tomography-based, artificial intelligence-driven waist skeletal muscle volume in uterine endometrial carcinoma. Insights Imaging 2021;12:192 
  10. Jones K, Gordon-Weeks A, Coleman C, Silva M. Radiologically determined sarcopenia predicts morbidity and mortality following abdominal surgery: a systematic review and meta-analysis. World J Surg 2017;41:2266-2279 
  11. Su H, Ruan J, Chen T, Lin E, Shi L. CT-assessed sarcopenia is a predictive factor for both long-term and short-term outcomes in gastrointestinal oncology patients: a systematic review and meta-analysis. Cancer Imaging 2019;19:82 
  12. Xiao J, Caan BJ, Cespedes Feliciano EM, Meyerhardt JA, Peng PD, Baracos VE, et al. Association of low muscle mass and low muscle radiodensity with morbidity and mortality for colon cancer surgery. JAMA Surg 2020;155:942-949 
  13. Mizuuchi Y, Tanabe Y, Sada M, Tamura K, Nagayoshi K, Nagai S, et al. Cross-sectional area of psoas muscle as a predictive marker of anastomotic failure in male rectal cancer patients: Japanese single institutional retrospective observational study. Ann Coloproctol 2022;38:353-361 
  14. Thibault R, Pichard C. The evaluation of body composition: a useful tool for clinical practice. Ann Nutr Metab 2012;60:6-16 
  15. Lee YS, Hong N, Witanto JN, Choi YR, Park J, Decazes P, et al. Deep neural network for automatic volumetric segmentation of whole-body CT images for body composition assessment. Clin Nutr 2021;40:5038-5046 
  16. Pickhardt PJ, Summers RM, Garrett JW. Automated CT-based body composition analysis: a golden opportunity. Korean J Radiol 2021;22:1934-1937 
  17. Weston AD, Korfiatis P, Kline TL, Philbrick KA, Kostandy P, Sakinis T, et al. Automated abdominal segmentation of CT scans for body composition analysis using deep learning. Radiology 2019;290:669-679 
  18. Ronneberger O, Fischer P, Brox T. U-Net: Convolutional networks for biomedical image segmentation. In: Navab N, Hornegger J, Wells WM, Frangi AF, eds. 18th International Conference on Medical Image Computing and Computer-Assisted Intervention -MICCAI 2015; 2015 Oct 5-9; Munch, Germany. Cham: Springer International Publishing; 2015;234-241 
  19. Cicek O, Abdulkadir A, Lienkamp SS, Brox T, Ronneberger O. 3D U-Net: learning dense volumetric segmentation from sparse annotation. In: Ourselin S, Joskowicz L, Sabuncu MR, Unal G, Wells W, eds. 19th International Conference on Medical Image Computing and Computer-Assisted Intervention - MICCAI 2016; 2016 Oct 17-21; Athens, Greece. Cham: Springer International Publishing, 2016;424-432 
  20. Ross R, Neeland IJ, Yamashita S, Shai I, Seidell J, Magni P, et al. Waist circumference as a vital sign in clinical practice: a Consensus Statement from the IAS and ICCR Working Group on Visceral Obesity. Nat Rev Endocrinol 2020;16:177-189 
  21. Aubrey J, Esfandiari N, Baracos VE, Buteau FA, Frenette J, Putman CT, et al. Measurement of skeletal muscle radiation attenuation and basis of its biological variation. Acta Physiol (Oxf) 2014;210:489-497 
  22. Miyamoto Y, Baba Y, Sakamoto Y, Ohuchi M, Tokunaga R, Kurashige J, et al. Sarcopenia is a negative prognostic factor after curative resection of colorectal cancer. Ann Surg Oncol 2015;22:2663-2668 
  23. Amini B, Boyle SP, Boutin RD, Lenchik L. Approaches to assessment of muscle mass and myosteatosis on computed tomography: a systematic review. J Gerontol A Biol Sci Med Sci 2019;74:1671-1678 
  24. Wang S, Xie H, Gong Y, Kuang J, Yan L, Ruan G, et al. The value of L3 skeletal muscle index in evaluating preoperative nutritional risk and long-term prognosis in colorectal cancer patients. Sci Rep 2020;10:8153 
  25. Daly LE, Prado CM, Ryan AM. A window beneath the skin: how computed tomography assessment of body composition can assist in the identification of hidden wasting conditions in oncology that profoundly impact outcomes. Proc Nutr Soc 2018;77:135-151 
  26. Akahori T, Sho M, Kinoshita S, Nagai M, Nishiwada S, Tanaka T, et al. Prognostic significance of muscle attenuation in pancreatic cancer patients treated with neoadjuvant chemoradiotherapy. World J Surg 2015;39:2975-2982 
  27. Martin L, Birdsell L, MacDonald N, Reiman T, Clandinin MT, McCargar LJ, et al. Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J Clin Oncol 2013;31:1539-1547 
  28. Kim DW, Ahn H, Kim KW, Lee SS, Kim HJ, Ko Y, et al. Prognostic value of sarcopenia and myosteatosis in patients with resectable pancreatic ductal adenocarcinoma. Korean J Radiol 2022;23:1055-1066 
  29. Kim SI, Yoon S, Kim TM, Cho JY, Chung HH, Song YS. Prognostic implications of body composition change during primary treatment in patients with ovarian cancer: a retrospective study using an artificial intelligence-based volumetric technique. Gynecol Oncol 2021;162:72-79 
  30. Kim HK, Kim KW, Kim EH, Lee MJ, Bae SJ, Ko Y, et al. Age-related changes in muscle quality and development of diagnostic cutoff points for myosteatosis in lumbar skeletal muscles measured by CT scan. Clin Nutr 2021;40:4022-4028 
  31. Aleixo GFP, Shachar SS, Nyrop KA, Muss HB, Malpica L, Williams GR. Myosteatosis and prognosis in cancer: systematic review and meta-analysis. Crit Rev Oncol Hematol 2020;145:102839 
  32. Cruz-Jentoft AJ, Sayer AA. Sarcopenia. Lancet 2019;393:2636-2646 
  33. Ryan AM, Power DG, Daly L, Cushen SJ, Ni Bhuachalla E, Prado CM. Cancer-associated malnutrition, cachexia and sarcopenia: the skeleton in the hospital closet 40 years later. Proc Nutr Soc 2016;75:199-211 
  34. Cheah MT, Chen JY, Sahoo D, Contreras-Trujillo H, Volkmer AK, Scheeren FA, et al. CD14-expressing cancer cells establish the inflammatory and proliferative tumor microenvironment in bladder cancer. Proc Natl Acad Sci U S A 2015;112:4725-4730 
  35. Chen LK, Woo J, Assantachai P, Auyeung TW, Chou MY, Iijima K, et al. Asian Working Group for Sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J Am Med Dir Assoc 2020;21:300-307.e2 
  36. Barberan-Garcia A, Ubre M, Roca J, Lacy AM, Burgos F, Risco R, et al. Personalised prehabilitation in high-risk patients undergoing elective major abdominal surgery: a randomized blinded controlled trial. Ann Surg 2018;267:50-56 
  37. Dent E, Morley JE, Cruz-Jentoft AJ, Arai H, Kritchevsky SB, Guralnik J, et al. International Clinical Practice Guidelines for Sarcopenia (ICFSR): screening, diagnosis and management. J Nutr Health Aging 2018;22:1148-1161 
  38. Redmond HP, Neary PM, Jinih M, O'Connell E, Foley N, Pfirrmann RW, et al. RandomiSed clinical trial assessing use of an anti-inflammatoRy aGent in attenUating peri-operatiVe inflAmmatioN in non-meTastatic colon cancer - the S.U.R.G.U.V.A.N.T. trial. BMC Cancer 2018;18:794 
  39. Kim DW, Kim KW, Ko Y, Park T, Lee J, Lee JB, et al. Effects of contrast phases on automated measurements of muscle quantity and quality using CT. Korean J Radiol 2021;22:1909-1917