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Z Gastroenterol 2023; 61(05): 526-535
DOI: 10.1055/a-1890-5818
Übersicht

Prevalence of benign focal liver lesions and non-hepatocellular carcinoma malignant lesions in liver cirrhosis

Prävalenz von benignen fokalen Leberläsionen und nicht-hepatozellulären malignen Läsionen in der Leberzirrhose
Kathleen Möller
1   Sana-Klinikum Lichtenberg, Berlin, Germany
,
Ehsan Safai Zadeh 
2   Interdisciplinary Centre of Ultrasound Diagnostics, Gastroenterology, Endocrinology, Metabolism and Clinical Infectiology, Philipps University Marburg, Marburg, Germany
,
Christian Görg
2   Interdisciplinary Centre of Ultrasound Diagnostics, Gastroenterology, Endocrinology, Metabolism and Clinical Infectiology, Philipps University Marburg, Marburg, Germany
,
Yi Dong
3   Zhongshan Hospital Fudan University, Shanghai, China (Ringgold ID: RIN92323)
,
Xin-Wu Cui
4   Department of Medical Ultrasound, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
,
Siegbert Faiss
1   Sana-Klinikum Lichtenberg, Berlin, Germany
,
Christoph F. Dietrich 
5   Allgemeine Innere Medizin (DAIM) Kliniken Beau Site, Salem und Permanence, Kliniken Hirslanden Beau Site, Salem und Permanence, Bern, Switzerland
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Abstract

Liver cirrhosis is associated with an increased risk of developing hepatocellular carcinoma (HCC). However, other benign and malignant liver lesions may co-exist or may be the only focal liver lesion (FLL) detected. Compared to HCC, comparatively little is known about the frequency and natural history of benign FLL in patients with established liver cirrhosis.

This review analyses the prevalence and frequency of benign and malignant FLL others than hepatocellular carcinoma (HCC) in liver cirrhosis including imaging and autopsy studies. Understanding these data should be helpful in avoiding misdiagnoses.

Zusammenfassung

Die Leberzirrhose ist mit einem erhöhten Risiko verbunden, ein hepatozelluläres Karzinom (HCC) zu entwickeln. Es können jedoch auch andere benigne und maligne Leberläsionen koexistieren oder die einzige nachgewiesene fokale Leberläsion (FLL) sein. Im Vergleich zum HCC ist über die Häufigkeit und den Verlauf benigner FLL bei Patienten mit bestehender Leberzirrhose vergleichsweise wenig bekannt.

Dieser Review analysiert die Prävalenz und Häufigkeit von benignen und malignen FLL außer dem hepatozellulären Karzinom (HCC) bei Leberzirrhose, einschließlich Bildgebungs- und Autopsiestudien. Das Verständnis dieser Daten sollte hilfreich sein, um Fehldiagnosen zu vermeiden.

Schlüsselwörter

Hämangiom - Fokal Noduläre Hyperplasie - Adenom - Leberzirrhose - HCC

Keywords

hemangioma - focal nodular hyperplasia - adenoma - Liver cirrhosis - HCC


Publication History

Received: 15 December 2021

Accepted after revision: 13 June 2022

Article published online:
22 November 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Yu MW, Hsu FC, Sheen IS. et al. Prospective study of hepatocellular carcinoma and liver cirrhosis in asymptomatic chronic hepatitis B virus carriers. Am J Epidemiol 1997; 145: 1039-1047
    CrossrefPubMedSearch in Google Scholar
  • 2 Pocha C, Xie C. Hepatocellular carcinoma in alcoholic and non-alcoholic fatty liver disease-one of a kind or two different enemies?. Transl Gastroenterol Hepatol 2019; 4: 72
    CrossrefPubMedSearch in Google Scholar
  • 3 Caraiani C, Boca B, Bura V. et al. CT/MRI LI-RADS v2018 vs. CEUS LI-RADS v2017-Can Things Be Put Together?. Biology (Basel) 2021; 10
    CrossrefPubMedSearch in Google Scholar
  • 4 Dietrich CF, Dong Y, Kono Y. et al. LI-RADS ancillary features on contrast-enhanced ultrasonography. Ultrasonography 2020; 39: 221-228
    CrossrefPubMedSearch in Google Scholar
  • 5 Dietrich CF, Potthoff A, Helmberger T. et al. Group CL-RW. [Contrast-enhanced ultrasound: Liver Imaging Reporting and Data System (CEUS LI-RADS)]. Z Gastroenterol 2018; 56: 499-506
    Thieme ConnectPubMedSearch in Google Scholar
  • 6 Lyshchik A, Kono Y, Dietrich CF. et al. Contrast-enhanced ultrasound of the liver: technical and lexicon recommendations from the ACR CEUS LI-RADS working group. NY: Abdom Radiol; 2017
    Search in Google Scholar
  • 7 Piscaglia F, Wilson SR, Lyshchik A. et al. American College of Radiology Contrast Enhanced Ultrasound Liver Imaging Reporting and Data System (CEUS LI-RADS) for the diagnosis of Hepatocellular Carcinoma: a pictorial essay. Ultraschall Med 2017; 38: 320-324
    Thieme ConnectPubMedSearch in Google Scholar
  • 8 Renzulli M, Brocchi S, Ierardi AM. et al. Imaging-based diagnosis of benign lesions and pseudolesions in the cirrhotic liver. Magn Reson Imaging 2021; 75: 9-20
    CrossrefPubMedSearch in Google Scholar
  • 9 Ignee A, Weiper D, Schuessler G. et al. Sonographic characterisation of hepatocellular carcinoma at time of diagnosis. Z. Gastroenterol 2005; 43: 289-294
    Thieme ConnectPubMedSearch in Google Scholar
  • 10 Dodd GD, Baron RL, Oliver JH. et al. Spectrum of imaging findings of the liver in end-stage cirrhosis: Part II, focal abnormalities. AJR Am J Roentgenol 1999; 173: 1185-1192
    CrossrefPubMedSearch in Google Scholar
  • 11 Ruiz Guinaldo A, Martin Herrera L, Roldan Cuadra R. Hepatic tumors in patients with cirrhosis: an autopsy study. Rev Esp Enferm Dig 1997; 89: 771-780
    PubMedSearch in Google Scholar
  • 12 Galvao B, Torres LR, Cardia PP. et al. Prevalence of simple liver cysts and hemangiomas in cirrhotic and non-cirrhotic patients submitted to magnetic resonance imaging. J Radiologia Brasileira 2013; 46: 203-208
    CrossrefPubMedSearch in Google Scholar
  • 13 Karhunen PJ. Benign hepatic tumours and tumour like conditions in men. J Clin Pathol 1986; 39: 183-188
    CrossrefPubMedSearch in Google Scholar
  • 14 Karhunen PJ, Penttila A, Liesto K. et al. Benign bile duct tumours, non-parasitic liver cysts and liver damage in males. J Hepatol 1986; 2: 89-99
    CrossrefPubMedSearch in Google Scholar
  • 15 Brancatelli G, Federle MP, Blachar A. et al. Hemangioma in the cirrhotic liver: diagnosis and natural history. Radiology 2001; 219: 69-74
    CrossrefPubMedSearch in Google Scholar
  • 16 Duran R, Ronot M, Di Renzo S. et al. Is magnetic resonance imaging of hepatic hemangioma any different in liver fibrosis and cirrhosis compared to normal liver?. Eur J Radiol 2015; 84: 816-822
    CrossrefPubMedSearch in Google Scholar
  • 17 Mastropasqua M, Kanematsu M, Leonardou P. et al. Cavernous hemangiomas in patients with chronic liver disease: MR imaging findings. Magn Reson Imaging 2004; 22: 15-18
    CrossrefPubMedSearch in Google Scholar
  • 18 Dietrich CF, Mertens JC, Braden B. et al. Contrast-enhanced ultrasound of histologically proven liver hemangiomas. Hepatology 2007; 45: 1139-1145
    CrossrefPubMedSearch in Google Scholar
  • 19 Dietrich CF, Ignee A, Trojan J. et al. Improved characterisation of histologically proven liver tumours by contrast enhanced ultrasonography during the portal venous and specific late phase of SHU 508A. Gut 2004; 53: 401-405
    CrossrefPubMedSearch in Google Scholar
  • 20 Vernuccio F, Cannella R, Porrello G. et al. Uncommon imaging evolutions of focal liver lesions in cirrhosis. Abdom Radiol (NY) 2019; 44: 3069-3077
    CrossrefPubMedSearch in Google Scholar
  • 21 Ren Y, Yuan G, Zhou Y. et al. Incidence and characteristics of benign liver space-occupying mass in 17 721 patients with chronic hepatitis B: a color Doppler ultrasound-based case-control study. Nan Fang Yi Ke Da Xue Xue Bao 2019; 39: 1149-1154
    CrossrefPubMedSearch in Google Scholar
  • 22 Libbrecht L, Cassiman D, Verslype C. et al. Clinicopathological features of focal nodular hyperplasia-like nodules in 130 cirrhotic explant livers. Am J Gastroenterol 2006; 101: 2341-2346
    CrossrefPubMedSearch in Google Scholar
  • 23 Seitz K, Greis C, Schuler A. et al. Frequency of tumor entities among liver tumors of unclear etiology initially detected by sonography in the noncirrhotic or cirrhotic livers of 1349 patients. Results of the DEGUM multicenter study. Ultraschall Med 2011; 32: 598-603
    Thieme ConnectPubMedSearch in Google Scholar
  • 24 Dietrich CF, Shi L, Lowe A. et al. Conventional ultrasound for diagnosis of hepatic steatosis is better than believed. Z Gastroenterol 2021;
    Thieme ConnectPubMedSearch in Google Scholar
  • 25 Chiorean L, Caraiani C, Radzina M. et al. Vascular phases in imaging and their role in focal liver lesions assessment. Clin Hemorheol Microcirc 2015; 62: 299-326
    CrossrefPubMedSearch in Google Scholar
  • 26 Hirche TO, Ignee A, Hirche H. et al. Evaluation of hepatic steatosis by ultrasound in patients with chronic hepatitis C virus infection. Liver Int 2007; 27: 748-757
    CrossrefPubMedSearch in Google Scholar
  • 27 Dietrich CF, Schall H, Kirchner J. et al. Sonographic detection of focal changes in the liver hilus in patients receiving corticosteroid therapy. Z. Gastroenterol 1997; 35: 1051-1057
    PubMedSearch in Google Scholar
  • 28 Kaltenbach TE, Engler P, Kratzer W. et al. Prevalence of benign focal liver lesions: ultrasound investigation of 45,319 hospital patients. Abdom Radiol (NY) 2016; 41: 25-32
    CrossrefPubMedSearch in Google Scholar
  • 29 Seguchi T, Akiyama Y, Itoh H. et al. Multiple hepatic peribiliary cysts with cirrhosis. J Gastroenterol 2004; 39: 384-390
    CrossrefPubMedSearch in Google Scholar
  • 30 Nakanuma Y, Kurumaya H, Ohta G. Multiple cysts in the hepatic hilum and their pathogenesis. A suggestion of periductal gland origin. Virchows Arch A Pathol Anat Histopathol 1984; 404: 341-350
    CrossrefPubMedSearch in Google Scholar
  • 31 Bazerbachi F, Haffar S, Sugihara T. et al. Peribiliary cysts: a systematic review and proposal of a classification framework. BMJ Open Gastroenterol 2018; 5: e000204
    CrossrefPubMedSearch in Google Scholar
  • 32 Ronot M, Dioguardi Burgio M, Purcell Y. et al. Focal lesions in cirrhosis: Not always HCC. Eur J Radiol 2017; 93: 157-168
    CrossrefPubMedSearch in Google Scholar
  • 33 Pedica F, Heaton N, Quaglia A. Peribiliary glands pathology in a large series of end-stage alcohol-related liver disease. Virchows Arch 2020; 477: 817-823
    CrossrefPubMedSearch in Google Scholar
  • 34 Nakanuma Y, Uesaka K, Kakuda Y. et al. Intraductal Papillary Neoplasm of Bile Duct: Updated Clinicopathological Characteristics and Molecular and Genetic Alterations. J Clin Med 2020; 9
    CrossrefPubMedSearch in Google Scholar
  • 35 Goldstein MJ. Metastases in the cirrhotic liver. N Engl J Med 1969; 281: 221
    CrossrefPubMedSearch in Google Scholar
  • 36 Hamaya K, Hashimoto H, Maeda Y. Metastatic carcinoma in cirrhotic liver--Statistical survey of autopsies in Japan. Acta Pathol Jpn 1975; 25: 153-159
    CrossrefPubMedSearch in Google Scholar
  • 37 Pereira-Lima JE, Lichtenfels E, Barbosa FS. et al. Prevalence study of metastases in cirrhotic livers. Hepatogastroenterology 2003; 50: 1490-1495
    PubMedSearch in Google Scholar
  • 38 Vanbockrijck M, Kloppel G. Incidence and morphology of liver metastasis from extrahepatic malignancies to cirrhotic livers. Zentralbl Pathol 1992; 138: 91-96
    PubMedSearch in Google Scholar
  • 39 Melato M, Laurino L, Mucli E. et al. Relationship between cirrhosis, liver cancer, and hepatic metastases. An autopsy study. Cancer 1989; 64: 455-459
    CrossrefPubMedSearch in Google Scholar
  • 40 Seymour K, Charnley RM. Evidence that metastasis is less common in cirrhotic than normal liver: a systematic review of post-mortem case-control studies. Br J Surg 1999; 86: 1237-1242
    CrossrefPubMedSearch in Google Scholar
  • 41 Mahdi Z, Ettel MG, Gonzalez RS. et al. Metastases can occur in cirrhotic livers with patent portal veins. Diagn Pathol 2021; 16: 18
    CrossrefPubMedSearch in Google Scholar
  • 42 Seitz G. Why are metastases in cirrhotic livers so rare?. Ultraschall Med 1989; 10: 123-126
    Thieme ConnectPubMedSearch in Google Scholar
  • 43 Ramia JM, Lopez-Andujar R, Torras J. et al. Multicentre study of liver metastases from colorectal cancer in pathological livers. HPB (Oxford) 2011; 13: 320-323
    CrossrefPubMedSearch in Google Scholar
  • 44 Liu Q, Zhang H, Jiang X. et al. Factors involved in cancer metastasis: a better understanding to “seed and soil” hypothesis. Mol Cancer 2017; 16: 176
    CrossrefPubMedSearch in Google Scholar
  • 45 Iwakiri Y, Shah V, Rockey DC. Vascular pathobiology in chronic liver disease and cirrhosis – current status and future directions. J Hepatol 2014; 61: 912-924
    CrossrefPubMedSearch in Google Scholar
  • 46 Cai B, Liao K, Song XQ. et al. Patients with chronically diseased livers have lower incidence of colorectal liver metastases: a meta-analysis. PLoS One 2014; 9: e108618
    CrossrefPubMedSearch in Google Scholar
  • 47 Song E, Chen J, Ouyang N. et al. Kupffer cells of cirrhotic rat livers sensitize colon cancer cells to Fas-mediated apoptosis. Br J Cancer 2001; 84: 1265-1271
    CrossrefPubMedSearch in Google Scholar
  • 48 Cheng L, Geng L, Dai B. et al. Repression of let-7a cluster prevents adhesion of colorectal cancer cells by enforcing a mesenchymal phenotype in presence of liver inflammation. Cell Death Dis 2018; 9: 489
    CrossrefPubMedSearch in Google Scholar
  • 49 Beuth J, Ko HL, Pulverer G. et al. Importance of lectins for the prevention of bacterial infections and cancer metastases. Glycoconj J 1995; 12: 1-6
    CrossrefPubMedSearch in Google Scholar
  • 50 Uhlenbruck G, Beuth J, Weidtman V. Liver lectins: mediators for metastases?. Experientia 1983; 39: 1314-1315
    CrossrefPubMedSearch in Google Scholar
  • 51 Lieber MM. The rare occurrence of metastatic carcinoma in the cirrhotic liver. Am J Med Sci 1957; 233: 145-152
    CrossrefPubMedSearch in Google Scholar
  • 52 Ruebner BH, Green R, Miyai K. et al. The rarity of intrahepatic metastasis in cirrhosis of the liver. A statistical explanation with some comments on the interpretation of necropsy data. Am J Pathol 1961; 39: 739-746
    PubMedSearch in Google Scholar
  • 53 Han EC, Ryoo SB, Park JW. et al. Oncologic and surgical outcomes in colorectal cancer patients with liver cirrhosis: A propensity-matched study. PLoS One 2017; 12: e0178920
    CrossrefPubMedSearch in Google Scholar
  • 54 Chiou WY, Chang CM, Tseng KC. et al. Effect of liver cirrhosis on metastasis in colorectal cancer patients: a nationwide population-based cohort study. Jpn J Clin Oncol 2015; 45: 160-168
    CrossrefPubMedSearch in Google Scholar
  • 55 Kondo T, Okabayashi K, Hasegawa H. et al. The impact of hepatic fibrosis on the incidence of liver metastasis from colorectal cancer. Br J Cancer 2016; 115: 34-39
    CrossrefPubMedSearch in Google Scholar
  • 56 Terzi E, Iavarone M, Pompili M. et al. Contrast ultrasound LI-RADS LR-5 identifies hepatocellular carcinoma in cirrhosis in a multicenter restropective study of 1,006 nodules. J Hepatol 2018; 68: 485-492
    CrossrefPubMedSearch in Google Scholar
  • 57 Mork H, Ignee A, Schuessler G. et al. Analysis of neuroendocrine tumour metastases in the liver using contrast enhanced ultrasonography. Scand.J. Gastroenterol 2007; 42: 652-662
    CrossrefPubMedSearch in Google Scholar
  • 58 Dong Y, Teufel A, Trojan J. et al. Contrast enhanced ultrasound in mixed hepatocellular cholangiocarcinoma: Case series and review of the literature. Dig Liver Dis 2018; 50: 401-407
    CrossrefPubMedSearch in Google Scholar
  • 59 Dantas E, Santos J, Coelho M. et al. Primary hepatic lymphoma in a patient with cirrhosis: a case report. J Med Case Rep 2020; 14: 168
    CrossrefPubMedSearch in Google Scholar
  • 60 Imrani K, Znati K, Amouri W. et al. Primary hepatic lymphoma in liver cirrhosis: A rare case report. Radiol Case Rep 2021; 16: 2179-2183
    CrossrefPubMedSearch in Google Scholar
  • 61 European Association for the Study of the Liver. Electronic address: easloffice@easloffice.eu, European Association for the Study of the L. EASL Clinical Practice Guidelines: Management of hepatocellular carcinoma. J Hepatol 2018; 69: 182-236
    CrossrefPubMedSearch in Google Scholar
  • 62 Heimbach JK, Kulik LM, Finn RS. et al. AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology 2018; 67: 358-380
    CrossrefPubMedSearch in Google Scholar
  • 63 Forner A, Vilana R, Ayuso C. et al. Diagnosis of hepatic nodules 20 mm or smaller in cirrhosis: Prospective validation of the noninvasive diagnostic criteria for hepatocellular carcinoma. Hepatology 2008; 47: 97-104
    CrossrefPubMedSearch in Google Scholar
  • 64 Mullhaupt B, Durand F, Roskams T. et al. Is tumor biopsy necessary?. Liver Transpl 2011; 17: S14-25
    CrossrefPubMedSearch in Google Scholar
  • 65 Khalili K, Kim TK, Jang HJ. et al. Indeterminate 1–2-cm nodules found on hepatocellular carcinoma surveillance: biopsy for all, some, or none?. Hepatology 2011; 54: 2048-2054
    CrossrefPubMedSearch in Google Scholar
  • 66 Bru C, Maroto A, Bruix J. et al. Diagnostic accuracy of fine-needle aspiration biopsy in patients with hepatocellular carcinoma. Dig Dis Sci 1989; 34: 1765-1769
    CrossrefPubMedSearch in Google Scholar
  • 67 Choi JY, Lee HC, Yim JH. et al. Focal nodular hyperplasia or focal nodular hyperplasia-like lesions of the liver: a special emphasis on diagnosis. J Gastroenterol Hepatol 2011; 26: 1004-1009
    CrossrefPubMedSearch in Google Scholar
  • 68 Lee H, Yoon JH, Kim H. et al. False Positive Diagnosis of Hepatocellular Carcinoma in Liver Resection Patients. J Korean Med Sci 2017; 32: 315-320
    CrossrefPubMedSearch in Google Scholar
  • 69 Kim MJ, Lee S, An C. Problematic lesions in cirrhotic liver mimicking hepatocellular carcinoma. Eur Radiol 2019; 29: 5101-5110
    CrossrefPubMedSearch in Google Scholar
  • 70 Lee YH, Kim SH, Cho MY. et al. Focal nodular hyperplasia-like nodules in alcoholic liver cirrhosis: radiologic-pathologic correlation. AJR Am J Roentgenol 2007; 188: W459-463
    CrossrefPubMedSearch in Google Scholar
  • 71 Marin D, Galluzzo A, Plessier A. et al. Focal nodular hyperplasia-like lesions in patients with cavernous transformation of the portal vein: prevalence, MR findings and natural history. Eur Radiol 2011; 21: 2074-2082
    CrossrefPubMedSearch in Google Scholar
  • 72 Seo JM, Lee SJ, Kim SH. et al. Hepatocellular carcinoma arising from hepatocellular adenoma in a hepatitis B virus-associated cirrhotic liver. Clin Radiol 2012; 67: 329-333
    CrossrefPubMedSearch in Google Scholar
  • 73 Alshak NS, Cocjin J, Podesta L. et al. Hepatocellular adenoma in glycogen storage disease type IV. Arch Pathol Lab Med 1994; 118: 88-91
    PubMedSearch in Google Scholar