Skip to main content

Advertisement

SpringerLink
Log in

Computed Tomography Image Texture: A Noninvasive Prognostic Marker of Hepatic Recurrence After Hepatectomy for Metastatic Colorectal Cancer

  • Colorectal Cancer
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Recurrence after resection of colorectal liver metastases (CRLMs) occurs in up to 75% of patients. Preoperative prediction of hepatic recurrence may inform therapeutic strategies at the time of initial resection. Texture analysis (TA) is an established technique that quantifies pixel intensity variations (heterogeneity) on cross-sectional imaging. We hypothesized that tumoral and parenchymal changes that are predictive of overall survival (OS) and recurrence in the future liver remnant (FLR) can be detected using TA on preoperative computed tomography (CT) images.

Methods

Patients who underwent resection for CRLM between 2003 and 2007 with appropriate preoperative CT scans were included (n = 198) in this retrospective study. Texture features extracted from the tumor and FLR, and clinicopathologic variables, were incorporated into a multivariable survival model.

Results

Quantitative imaging features of the FLR were an independent predictor of both OS and hepatic disease–free survival (HDFS). Tumor texture showed significant association with OS. TA of the FLR allowed patient stratification into two groups, with significantly different risks of hepatic recurrence (hazard ratio 2.09, 95% confidence interval 1.33–3.28; p = 0.001). Patients with homogeneous parenchyma had approximately twice the risk of hepatic recurrence (41 vs. 20%).

Conclusion

TA of the tumor and FLR are independently associated with OS, and TA of the FLR is independently associated with HDFS. Patients with homogeneous parenchyma had a significantly higher risk of hepatic recurrence. Preoperative TA of the liver represents a potential biomarker to identify patients at risk of liver recurrence after resection for CRLM.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Siegel R, DeSantis C, Virgo K, Stein K, Mariotto A, Smith T, et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin. 2012;62(4):220–41.

    Article  PubMed  Google Scholar 

  2. Mella J, Biffin A, Radcliffe AG, Stamataki JD, Steele RJ. Population-based audit of colorectal cancer management in two UK health regions. Colorectal cancer working group, Royal College of surgeons of England Clinical Epidemiology and Audit Unit. Br J Surg. 1997;84(12):1731–36.

    Article  CAS  PubMed  Google Scholar 

  3. Tomlinson JS, Jarnagin WR, DeMatteo RP, Fong Y, Kornprat P, Gonen M, et al. Actual 10-year survival after resection of colorectal liver metastases defines cure. J Clin Oncol. 2007; 25(29):4575–80.

    Article  PubMed  Google Scholar 

  4. Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999;230(3):309–18; discussion 318–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. House MG, Ito H, Gonen M, Fong Y, Allen PJ, DeMatteo RP, et al. Survival after hepatic resection for metastatic colorectal cancer: trends in outcomes for 1,600 patients during two decades at a single institution. J Am Coll Surg 2010;210(5):744–52.

    Article  PubMed  Google Scholar 

  6. D’Angelica M, Kornprat P, Gonen M, DeMatteo RP, Fong Y, Blumgart LH, et al. Effect on outcome of recurrence patterns after hepatectomy for colorectal metastases. Ann Surg Oncol. 2011;18(4):1096–03.

    Article  PubMed  Google Scholar 

  7. Kemeny N, Huang Y, Cohen AM, Shi W, Conti JA, Brennan MF, et al. Hepatic arterial infusion of chemotherapy after resection of hepatic metastases from colorectal cancer. N Engl J Med. 1999;341(27):2039–48.

    Article  CAS  PubMed  Google Scholar 

  8. Goere D, Benhaim L, Bonnet S, Malka D, Faron M, Elias D, et al. Adjuvant chemotherapy after resection of colorectal liver metastases in patients at high risk of hepatic recurrence: a comparative study between hepatic arterial infusion of oxaliplatin and modern systemic chemotherapy. Ann Surg. 2013;257(1):114–20.

    Article  PubMed  Google Scholar 

  9. Nordlinger B, Guiguet M, Vaillant JC, Balladur P, Boudjema K, Bachellier P, et al. Surgical resection of colorectal carcinoma metastases to the liver. A prognostic scoring system to improve case selection, based on 1568 patients. Association Francaise de Chirurgie. Cancer. 1996;77(7):1254–62.

    Article  CAS  PubMed  Google Scholar 

  10. Rees M, Tekkis PP, Welsh FK, O’rourke T, John TG. Evaluation of long-term survival after hepatic resection for metastatic colorectal cancer: a multifactorial model of 929 patients. Ann Surg. 2008;247(1):125–35.

    Article  PubMed  Google Scholar 

  11. Zakaria S, Donohue JH, Que FG, Farnell MB, Schleck CD, Ilstrup DM, et al. Hepatic resection for colorectal metastases: value for risk scoring systems? Ann Surg. 2007;246(2):183–91.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Leen E. The detection of occult liver metastases of colorectal carcinoma. J Hepatobiliary Pancreat Surg. 1999;6(1):7–15.

    Article  CAS  PubMed  Google Scholar 

  13. Conzelmann M, Linnemann U, Berger MR. Detection of disseminated tumour cells in the liver of colorectal cancer patients. Eur J Surg Oncol. 2005;31(1):38–44.

    Article  CAS  PubMed  Google Scholar 

  14. Rao SX, Lambregts DM, Schnerr RS, van Ommen W, van Nijnatten TJ, Martens MH, et al. Whole-liver CT texture analysis in colorectal cancer: Does the presence of liver metastases affect the texture of the remaining liver? United European Gastroenterol J. 2014;2(6):530–38.

    Article  Google Scholar 

  15. Ganeshan B, Miles KA, Young RC, Chatwin CR. Hepatic entropy and uniformity: additional parameters that can potentially increase the effectiveness of contrast enhancement during abdominal CT. Clin Radiol. 2007;62(8):761–68.

    Article  CAS  PubMed  Google Scholar 

  16. Miles KA, Ganeshan B, Griffiths MR, Young RC, Chatwin CR. Colorectal cancer: texture analysis of portal phase hepatic CT images as a potential marker of survival. Radiology. 2009;250(2):444–52.

    Article  PubMed  Google Scholar 

  17. Simpson AL, Adams LB, Allen PJ, D’Angelica MI, DeMatteo RP, Fong Y, et al. Texture analysis of preoperative CT images for prediction of postoperative hepatic insufficiency: a preliminary study. J Am Coll Surg. 2015;220(3):339–46.

    Article  PubMed  Google Scholar 

  18. Wu Z, Matsui O, Kitao A, Kozaka K, Koda W, Kobayashi S, et al. Hepatitis C related chronic liver cirrhosis: feasibility of texture analysis of MR images for classification of fibrosis stage and necroinflammatory activity grade. PLoS ONE. 2015;10(3):e0118297.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Ba-Ssalamah A, Muin D, Schernthaner R, Kulinna-Cosentini C, Bastati N, Stift J, et al. Texture-based classification of different gastric tumors at contrast-enhanced CT. Eur J Radiol. 2013;82(10):e537–43.

    Article  PubMed  Google Scholar 

  20. Ng F, Ganeshan B, Kozarski R, Miles KA, Goh V. Assessment of primary colorectal cancer heterogeneity by using whole-tumor texture analysis: contrast-enhanced CT texture as a biomarker of 5-year survival. Radiology. 2013;266(1):177–84.

    Article  PubMed  Google Scholar 

  21. Hayano K, Yoshida H, Zhu AX, Sahani DV. Fractal analysis of contrast-enhanced CT images to predict survival of patients with hepatocellular carcinoma treated with sunitinib. Dig Dis Sci. 2014;59(8):1996–03.

    Article  CAS  PubMed  Google Scholar 

  22. Lubner MG, Stabo N, Lubner SJ, Del Rio AM, Song C, Halberg RB, et al. CT textural analysis of hepatic metastatic colorectal cancer: pre-treatment tumor heterogeneity correlates with pathology and clinical outcomes. Abdom Imaging. 2015;40(7):2331–37.

    Article  PubMed  Google Scholar 

  23. Chun YS, Vauthey JN, Boonsirikamchai P, Maru DM, Kopetz S, Palavecino M, et al. Association of computed tomography morphologic criteria with pathologic response and survival in patients treated with bevacizumab for colorectal liver metastases. JAMA. 2009;302(21):2338–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Wolf PS, Park JO, Bao F, Allen PJ, DeMatteo RP, Fong Y, et al. Preoperative chemotherapy and the risk of hepatotoxicity and morbidity after liver resection for metastatic colorectal cancer: a single institution experience. J Am Coll Surg. 2013;216(1):41–9.

    Article  PubMed  Google Scholar 

  25. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41(6):1313–21.

    Article  PubMed  Google Scholar 

  26. Rubbia-Brandt L, Audard V, Sartoretti P, Roth AD, Brezault C, Le Charpentier M, et al. Severe hepatic sinusoidal obstruction associated with oxaliplatin-based chemotherapy in patients with metastatic colorectal cancer. Ann Oncol. 2004;15(3):460–66.

    Article  CAS  PubMed  Google Scholar 

  27. Poultsides GA, Bao F, Servais EL, Hernandez-Boussard T, DeMatteo RP, Allen PJ, et al. Pathologic response to preoperative chemotherapy in colorectal liver metastases: fibrosis, not necrosis, predicts outcome. Ann Surg Oncol. 2012;19(9):2797–04.

    Article  PubMed  Google Scholar 

  28. Haralick RM, Shanmuga.K, Dinstein I. Textural features for image classification. IEEE Trans Syst Man Cybern. 1973;3(6):610–21.

    Article  Google Scholar 

  29. Haralick RM. Statistical and structural approaches to texture. Proc IEEE. 1979;67(5):786–04.

    Article  Google Scholar 

  30. Soh LK, Tsatsoulis C. Texture analysis of SAR sea ice imagery using gray level co-occurrence matrices. IEEE Trans Geosci Remote Sens. 1999;37(2):780–795.

    Article  Google Scholar 

  31. van der Wal GE, Gouw AS, Kamps JA, Moorlag HE, Bulthuis ML, Molema G, et al. Angiogenesis in synchronous and metachronous colorectal liver metastases: the liver as a permissive soil. Ann Surg. 2012;255(1):86–94.

    Article  PubMed  Google Scholar 

  32. van der Wal GE, Gouw AS, Kamps JA, Moorlag HE, Bulthuis ML, Molema G, et al. Reply to letter: “Markers of angiogenesis in synchronous and in metachronous colorectal hepatic metastases”. Ann Surg. 2015;261(1):e20–e21.

    PubMed  Google Scholar 

  33. Eveno C, Hainaud P, Rampanou A, Bonnin P, Bakhouche S, Dupuy E, et al. Proof of prometastatic niche induction by hepatic stellate cells. J Surg Res. 2015;194(2):496–04.

    Article  PubMed  Google Scholar 

  34. Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 2015;17(6):816–26.

    Article  CAS  PubMed  Google Scholar 

  35. Lorenz M, Muller HH, Schramm H, Gassel HJ, Rau HG, Ridwelski K, et al. Randomized trial of surgery versus surgery followed by adjuvant hepatic arterial infusion with 5-fluorouracil and folinic acid for liver metastases of colorectal cancer. German Cooperative on Liver Metastases (Arbeitsgruppe Lebermetastasen). Ann Surg. 1998;228(6):756–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Yamaguchi T, Mori T, Takahashi K, Matsumoto H, Miyamoto H, Kato T, et al. A new classification system for liver metastases from colorectal cancer in Japanese multicenter analysis. Hepatogastroenterology. 2008;55(81):173–78.

    PubMed  Google Scholar 

  37. Iwatsuki S, Dvorchik I, Madariaga JR, Marsh JW, Dodson F, Bonham AC, et al. Hepatic resection for metastatic colorectal adenocarcinoma: a proposal of a prognostic scoring system. J Am Coll Surg. 1999;189(3):291–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Kanemitsu Y, Kato T. Prognostic models for predicting death after hepatectomy in individuals with hepatic metastases from colorectal cancer. World J Surg. 2008;32(6):1097–07.

    Article  PubMed  Google Scholar 

  39. Allen PJ, Kemeny N, Jarnagin W, DeMatteo R, Blumgart L, Fong Y. Importance of response to neoadjuvant chemotherapy in patients undergoing resection of synchronous colorectal liver metastases. J Gastrointest Surg. 2003;7(1):109–15.

    Article  PubMed  Google Scholar 

Download references

Acknowledgement

Funding

This study was supported in part by National Institutes of Health/National Cancer Institute (NIH/NCI) Cancer Center Support Grant P30 CA008748. Alexandre Doussot received research fellowship grants from the French Association of Hepatobiliary Surgery and Transplantation, and the Université de Bourgogne.

Author information

Authors and Affiliations

  1. Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA

    Amber L. Simpson PhD, Alexandre Doussot MD, John M. Creasy MD, Lauryn B. Adams BS, Peter J. Allen MD, Ronald P. DeMatteo MD, T. Peter Kingham MD, William R. Jarnagin MD & Michael I. D’Angelica MD

  2. Department of Radiology, Memorial Sloan Kettering Cancer Center, New York, NY, USA

    Richard K. G. Do MD, PhD

  3. Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, USA

    Mithat Gönen PhD

  4. Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA

    Nancy E. Kemeny MD

  5. Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, USA

    Jinru Shia MD

Authors
  1. Amber L. Simpson PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexandre Doussot MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John M. Creasy MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lauryn B. Adams BS
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peter J. Allen MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ronald P. DeMatteo MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mithat Gönen PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Nancy E. Kemeny MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. T. Peter Kingham MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jinru Shia MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. William R. Jarnagin MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Richard K. G. Do MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Michael I. D’Angelica MD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amber L. Simpson PhD.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 15 kb)

Supplementary material 2 (DOCX 310 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Simpson, A.L., Doussot, A., Creasy, J.M. et al. Computed Tomography Image Texture: A Noninvasive Prognostic Marker of Hepatic Recurrence After Hepatectomy for Metastatic Colorectal Cancer. Ann Surg Oncol 24, 2482–2490 (2017). https://doi.org/10.1245/s10434-017-5896-1

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-017-5896-1

Keywords

Search

Navigation