Skip to main content
SpringerLink
Log in

Liver surface nodularity: a novel predictor of post-hepatectomy liver failure in patients with colorectal liver metastases following chemotherapy

  • Hepatobiliary-Pancreas
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

The goal of this study was to assess the relationship between liver surface nodularity (LSN), chemotherapy-associated liver injury (CALI), and clinically relevant post-hepatectomy liver failure (CR-PHLF) (i.e., ≥ grade B) in patients undergoing hepatectomy for colorectal liver metastases (CLM).

Methods

Preoperative CT scans of patients who underwent chemotherapy followed by hepatectomy for CLM between 2010 and 2017 were retrospectively analyzed. LSN was measured using semi-automated CT software CT images in patients who had available preoperative CT scans within 6 weeks before hepatectomy, and was computed based on the means of one to 10 measurements by two abdominal radiologists consensually. The association of LSN, CALI, and CR-PHLF was analyzed.

Results

Two hundred fifty-six patients were analyzed (149 men and 107 women; overall median age, 61 [range, 29–88 years]). A total of 26 patients (10.2%) developed CR-PHLF. The optimal LSN cut-off value for detecting CR-PHLF was 2.5, as determined by receiver operative characteristic analysis (p < 0.001). LSN ≥ 2.5 was associated with prolonged chemotherapy (> 6 cycles, p = 0.018), but not with CALIs. After propensity score matching, LSN remained significantly associated with CR-PHLF (p = 0.031). Furthermore, multivariate analysis identified LSN ≥ 2.50 and future liver remnant (FLR) < 30% as significant preoperative predictors of CR-PHLF in 102 patients undergoing major hepatectomy. LSN ≥ 2.50 was more frequent in patients undergoing major hepatectomy despite FLR ≥ 30% (p = 0.008).

Conclusion

LSN quantified on CT is an independent surrogate of CR-PHLF in patients who undergo chemotherapy followed by hepatectomy for CLM and may provide a valuable additional tool in the preoperative assessment of these patients.

Key Points

• LSN was not associated with chemotherapy- associated liver injury but high LSN (defined ≥ 2.5) was associated with prolonged chemotherapy (> 6 cycles).

• High LSN was an independent predictor of clinically relevant postoperative liver failure in patients undergoing hepatectomy for CRLM.

• LSN ≥ 2.50 was more frequent in patients with PHLF after major hepatectomy despite a future liver remnant ≥ 30%.

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
Fig. 3

Similar content being viewed by others

Abbreviations

(CR)-PHLF:

(Clinically relevant) post-hepatectomy liver failure

ALPPS:

Associating liver partition and portal vein ligation for staged hepatectomy

APRI:

Aspartate amino transferase-to-platelet ratio index

CALI:

Chemotherapy-associated liver injury

CASH:

Chemotherapy-associated steatohepatitis

CLM:

Colorectal liver metastases

FIB-4:

Fibrosis-4

FLR:

Future liver remnant

LSN:

Liver surface nodularity

NRH:

Nodular regenerative hyperplasia

SOS:

Sinusoidal obstruction syndrome

References

  1. Vigano L, De Rosa G, Toso C et al (2017) Reversibility of chemotherapy-related liver injury. J Hepatol 67:84–91

    Article  CAS  Google Scholar 

  2. Adam R, De Gramont A, Figueras J et al (2012) The oncosurgery approach to managing liver metastases from colorectal cancer: a multidisciplinary international consensus. Oncologist 17:1225–1239

    Article  CAS  Google Scholar 

  3. Soubrane O, Brouquet A, Zalinski S et al (2010) Predicting high grade lesions of sinusoidal obstruction syndrome related to oxaliplatin-based chemotherapy for colorectal liver metastases: correlation with post-hepatectomy outcome. Ann Surg 251:454–460

    Article  Google Scholar 

  4. Dorcaratto D, Mazzinari G, Fernandez M et al (2019) Impact of postoperative complications on survival and recurrence after resection of colorectal liver metastases: systematic review and meta-analysis. Ann Surg 270(6):1018–1027

    Article  Google Scholar 

  5. Farid SG, Aldouri A, Morris-Stiff G et al (2010) Correlation between postoperative infective complications and long-term outcomes after hepatic resection for colorectal liver metastasis. Ann Surg 251:91–100

    Article  Google Scholar 

  6. Araujo RL, Gönen M, Herman P (2015) Chemotherapy for patients with colorectal liver metastases who underwent curative resection improves long-term outcomes: systematic review and meta-analysis. Ann Surg Oncol 22:3070–3078

    Article  Google Scholar 

  7. Rahbari NN, Reissfelder C, Koch M et al (2011) The predictive value of postoperative clinical risk scores for outcome after hepatic resection: a validation analysis in 807 patients. Ann Surg Oncol 18:3640–3649

    Article  Google Scholar 

  8. Rubbia-Brandt L, Audard V, Sartoretti P et al (2004) Severe hepatic sinusoidal obstruction associated with oxaliplatin-based chemotherapy in patients with metastatic colorectal cancer. Ann Oncol 15:460–466

    Article  CAS  Google Scholar 

  9. Kneuertz PJ, Maithel SK, Staley CA, Kooby DA (2011) Chemotherapy-associated liver injury: impact on surgical management of colorectal cancer liver metastases. Ann Surg Oncol 18:181–190

    Article  Google Scholar 

  10. Smith AD, Branch CR, Zand K et al (2016) Liver surface nodularity quantification from routine ct images as a biomarker for detection and evaluation of cirrhosis. Radiology 280:771–781

    Article  Google Scholar 

  11. Sartoris R, Rautou PE, Elkrief L et al (2018) Quantification of liver surface nodularity at ct: utility for detection of portal hypertension. Radiology 289:698–707

    Article  Google Scholar 

  12. Catania R, Furlan A, Smith AD, Behari J, Tublin M, Borhani A (2020) Diagnostic value of MRI-derived liver surface nodularity score for the non-invasive quantification of hepatic fibrosis in non-alcoholic fatty liver disease. Eur Radiol. https://doi.org/10.1007/s00330-020-07114-y

  13. Rahbari NN, Garden OJ, Padbury R et al (2011) Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery 149:713–724

    Article  Google Scholar 

  14. Sartoris R, Lazareth M, Nivolli A, Dioguardi Burgio M, Vilgrain V, Ronot M (2020) CT-based liver surface nodularity for the detection of clinically significant portal hypertension: defining measurement quality criteria. Abdom Radiol (NY). https://doi.org/10.1007/s00261-020-02519-1

  15. Bedossa P, Poitou C, Veyrie N et al (2012) Histopathological algorithm and scoring system for evaluation of liver lesions in morbidly obese patients. Hepatology 56:1751–1759

    Article  Google Scholar 

  16. Wanless IR (1990) Micronodular transformation (nodular regenerative hyperplasia) of the liver: a report of 64 cases among 2,500 autopsies and a new classification of benign hepatocellular nodules. Hepatology 11:787–797

    Article  CAS  Google Scholar 

  17. Strasberg SM (2005) Nomenclature of hepatic anatomy and resections: A review of the Brisbane 2000 system. J Hepatobiliary PancreatSurg 12:351–355

    Article  Google Scholar 

  18. Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 40:205–213

    Article  Google Scholar 

  19. Friedman SF, Martin P, Munoz JS (2003) Laboratory evaluation of the patient with liver disease. Hepatology, a textbook of liver disease. Philedelphia; Saunders publication 1:661–709

    Google Scholar 

  20. Pesce A, Scilletta R, Branca A et al (2012) Does transient elastography (FibroScan®) have a role in decision making in hepatocellularcarcinoma? HPB (Oxford) 14:403–408

    Article  Google Scholar 

  21. Overman MJ, Maru DM, Charnsangavej C et al (2010) Oxaliplatin-mediated increase in spleen size as a biomarker for the development of hepatic sinusoidal injury. J Clin Oncol 28:2549–2555

    Article  CAS  Google Scholar 

  22. Rubbia-Brandt L, Lauwers GY, Wang H et al (2010) Sinusoidal obstruction syndrome and nodular regenerative hyperplasia are frequent oxaliplatin-associated liver lesions and partially prevented by bevacizumab in patients with hepatic colorectal metastasis. Histopathology 56:430–439

    Article  Google Scholar 

  23. Hobeika C, Cauchy F, Sartoris R et al (2020) Relevance of liver surface nodularity for preoperative risk assessment in patients with resectable hepatocellular carcinoma. Br J Surg. https://doi.org/10.1002/bjs.11511

  24. Nakano H, Oussoultzoglou E, Rosso E et al (2008) Sinusoidal injury increases morbidity after major hepatectomy in patients with colorectal liver metastases receiving preoperative chemotherapy. Ann Surg 247:118–124

    Article  Google Scholar 

  25. Vauthey JN, Mizuno T, Overman MJ, Soubrane O (2017) Can we navigate chemotherapy-induced hepatic injuries from pathology to bedside? J Hepatol 67:10–11

    Article  Google Scholar 

  26. Yamashita S, Shindoh J, Mizuno T et al (2017) Hepatic atrophy following preoperative chemotherapy predicts hepatic insufficiency after resection of colorectal liver metastases. J Hepatol 67:56–64

    Article  Google Scholar 

  27. Niekamp AS, Huang SY, Mahvash A et al (2020) Hepatic vein embolization after portal vein embolization to induce additional liver hypertrophy in patients with metastatic colorectal carcinoma. Eur Radiol 30:3862–3868

    Article  Google Scholar 

  28. Shindoh J, Tzeng CW, Aloia TA et al (2013) Optimal future liver remnant in patients treated with extensive preoperative chemotherapy for colorectal liver metastases. Ann Surg Oncol 20:2493–2500

    Article  Google Scholar 

  29. Narita M, Oussoultzoglou E, Fuchshuber P et al (2012) What is a safe future liver remnant size in patients undergoing major hepatectomy for colorectal liver metastases and treated by intensive preoperative chemotherapy? Ann Surg Oncol 19(8):2526–2538

    Article  Google Scholar 

  30. De Vos N, Sartoris R, Cauchy F, Rautou PE, Vilgrain V, Ronot M (2020) Performance of liver surface nodularity quantification for the diagnosis of portal hypertension in patients with cirrhosis: comparison between MRI with hepatobiliary phase sequences and CT. Abdom Radiol (NY) 45(2):365–372

Download references

Funding

The authors state that this work has not received any funding.

Author information

Authors and Affiliations

  1. Department of HPB Surgery and Liver Transplantation, Beaujon Hospital, 100 Boulevard du Général Leclerc, 92110, Clichy, France

    Tomoaki Yoh, Christian Hobeika, Olivier Soubrane & François Cauchy

  2. Assistance Publique Hôpitaux de Paris, Paris, France

    Tomoaki Yoh, Antoine Perrot, Aurélie Beaufrère, Christian Hobeika, Riccardo Sartoris, Valérie Paradis, Valérie Vilgrain, Olivier Soubrane, François Cauchy & Maxime Ronot

  3. Université Paris VII Paris-Diderot, Paris, France

    Tomoaki Yoh, Antoine Perrot, Aurélie Beaufrère, Christian Hobeika, Riccardo Sartoris, Valérie Paradis, Valérie Vilgrain, Olivier Soubrane, François Cauchy & Maxime Ronot

  4. Department of Radiology, Beaujon Hospital, 100 Boulevard du Général Leclerc, 92110, Clichy, France

    Antoine Perrot, Riccardo Sartoris, Valérie Vilgrain & Maxime Ronot

  5. Department of Pathology, Beaujon Hospital, 100 Boulevard du Général Leclerc, 92110, Clichy, France

    Aurélie Beaufrère & Valérie Paradis

Authors
  1. Tomoaki Yoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Antoine Perrot
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aurélie Beaufrère
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christian Hobeika
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Riccardo Sartoris
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Valérie Paradis
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Valérie Vilgrain
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Olivier Soubrane
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. François Cauchy
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Maxime Ronot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maxime Ronot.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Maxime Ronot.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• retrospective

• diagnostic or prognostic study

• performed at one institution

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 2769 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yoh, T., Perrot, A., Beaufrère, A. et al. Liver surface nodularity: a novel predictor of post-hepatectomy liver failure in patients with colorectal liver metastases following chemotherapy. Eur Radiol 31, 5830–5839 (2021). https://doi.org/10.1007/s00330-020-07683-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-020-07683-y

Keywords

Search

Navigation