INTRAHEPATIC BILIARY STRICTURES WITH UNDERLYING PRE-MALIGNANT BILIARY LESIONS: IS IT TIME TO BUILD GUIDELINES ON DIAGNOSIS AND MANAGEMENT?

Giuliano LA BARBA Carlo Alberto PACILIO Cecilia BINDA Francesca FAPPIANO Carlo FABBRI Giorgio ERCOLANI About the authors

HEADINGS:
Intrahepatic bile ducts; Intrahepatic cholestasis; Carcinoma in situ; Cholangiocarcinoma; Minimally invasive surgical procedures

INTRODUCTION AND LITERATURE REVIEW

Biliary intraepithelial neoplasia (BilIN) is defined as a precursor lesion of invasive adenocarcinoma and it can develop both in intrahepatic and extrahepatic bile ducts. BilIN grossly presents as flat lesions but is usually macroscopically and radiologically unidentifiable1010 Nagtegaal ID, Odze RD, Klimstra D, Paradis V, Rugge M, Schirmacher P, Washington KM, Carneiro F, Cree IA; WHO Classification of Tumours Editorial Board. The 2019 WHO classification of tumours of the digestive system. Histopathology. 2020;76(2):182-188. doi: 10.1111/his.13975.
https://doi.org/10.1111/his.13975...
,2121 Zen Y, Adsay NV, Bardadin K, Colombari R, Ferrell L, Haga H, Hong SM, Hytiroglou P, Klöppel G, Lauwers GY, et al. Biliary intraepithelial neoplasia: an international interobserver agreement study and proposal for diagnostic criteria. Mod Pathol. 2007;20(6):701-9. doi: 10.1038/modpathol.3800788.
https://doi.org/10.1038/modpathol.380078...
. Interestingly, in the last decades due to the spread of imaging techniques, focal intrahepatic biliary strictures (FIHS) are more commonly incidentally founded in clinical practice. It is currently unknown which is their correct management and in what percentage they can harbor pre-neoplastic alterations (as BilIN) or malignancy2020 Yeo D, Perini MV, Muralidharan V, Christophi C. Focal intrahepatic strictures: a review of diagnosis and management. HPB (Oxford). 2012;14(7):425-34. doi: 10.1111/j.1477-2574.2012.00481.x.
https://doi.org/10.1111/j.1477-2574.2012...
. Due to the concomitant increase in western countries of intrahepatic cholangiocarcinoma, it would be useful to understand the natural history of FIHS, as they can represent a radiological manifestation of underlying pre-malignant disease: in that perspective, the ideal treatment could be an early surgery to prevent cholangiocarcinoma33 Blechacz B. Cholangiocarcinoma: Current Knowledge and New Developments. Gut Liver. 2017;11(1):13-26. doi: 10.5009/gnl15568.
https://doi.org/10.5009/gnl15568...
,1818 Witjes CD, Karim-Kos HE, Visser O, de Vries E, IJzermans JN, de Man RA, Coebergh JW, Verhoef C. Intrahepatic cholangiocarcinoma in a low endemic area: rising incidence and improved survival. HPB (Oxford). 2012;14(11):777-81. doi: 10.1111/j.1477-2574.2012.00536.x.
https://doi.org/10.1111/j.1477-2574.2012...
.

Cholangiocarcinoma is the most common biliary tract malignancy, with a well known unfavorable prognosis. Currently, surgery is the only potential curative treatment but, unfortunately, the majority of patients are diagnosed at late stage or are found to be unresectable during explorative laparotomy33 Blechacz B. Cholangiocarcinoma: Current Knowledge and New Developments. Gut Liver. 2017;11(1):13-26. doi: 10.5009/gnl15568.
https://doi.org/10.5009/gnl15568...
. Interestingly, during the last three decades, the incidence of the intrahepatic subtype of cholangiocarcinoma has increased in Western Europe1818 Witjes CD, Karim-Kos HE, Visser O, de Vries E, IJzermans JN, de Man RA, Coebergh JW, Verhoef C. Intrahepatic cholangiocarcinoma in a low endemic area: rising incidence and improved survival. HPB (Oxford). 2012;14(11):777-81. doi: 10.1111/j.1477-2574.2012.00536.x.
https://doi.org/10.1111/j.1477-2574.2012...
.

Cholangiocarcinoma of intrahepatic and extrahepatic bile ducts is known to develop through a multistep carcinogenesis sequence, including biliary intraepithelial neoplasia. BilIN is characterized by a flat or micropapillary growth of atypical biliary epithelium. In 2007 Zen et al1010 Nagtegaal ID, Odze RD, Klimstra D, Paradis V, Rugge M, Schirmacher P, Washington KM, Carneiro F, Cree IA; WHO Classification of Tumours Editorial Board. The 2019 WHO classification of tumours of the digestive system. Histopathology. 2020;76(2):182-188. doi: 10.1111/his.13975.
https://doi.org/10.1111/his.13975...
. reported the results of the international consensus on its diagnostic criteria and grading.

In the last 20 years, pathologists have identified two main precursors of invasive cholangiocarcinoma, namely BilIN and intraductal papillary neoplasm of bile duct, both currently included in the WHO classification of tumors of digestive system1010 Nagtegaal ID, Odze RD, Klimstra D, Paradis V, Rugge M, Schirmacher P, Washington KM, Carneiro F, Cree IA; WHO Classification of Tumours Editorial Board. The 2019 WHO classification of tumours of the digestive system. Histopathology. 2020;76(2):182-188. doi: 10.1111/his.13975.
https://doi.org/10.1111/his.13975...
. As expected, BilIN and intraductal papillary neoplasm have been identified in the bile ducts of patients suffering of primary sclerosing cholangitis, choledochal cyst and hepatolithiasis, all well known risk factors for cholangiocarcinoma. In 2006, Zen et al.2222 Zen Y, Sasaki M, Fujii T, Chen TC, Chen MF, Yeh TS, Jan YY, Huang SF, Nimura Y, Nakanuma Y. Different expression patterns of mucin core proteins and cytokeratins during intrahepatic cholangiocarcinogenesis from biliary intraepithelial neoplasia and intraductal papillary neoplasm of the bile duct--an immunohistochemical study of 110 cases of hepatolithiasis. J Hepatol. 2006;44(2):350-8. doi: 10.1016/j.jhep.2005.09.025.
https://doi.org/10.1016/j.jhep.2005.09.0...
reported a series of 110 patients with biliary neoplasm associated to hepatolithiasis, differentiating cases of BilIN and intraductal papillary neoplasm by cytokeratin and mucin immunoistochemical staining; in that series, cholangiocarcinomas arising from BilIN developed tubular adenocarcinoma, while those arising from intraductal papillary neoplasm developed either tubular or colloid carcinomas; moreover, those latter seemed to have a better survival1616 Tajima Y, Kuroki T, Fukuda K, Tsuneoka N, Furui J, Kanematsu T. An intraductal papillary component is associated with prolonged survival after hepatic resection for intrahepatic cholangiocarcinoma. Br J Surg. 2004;91(1):99-104. doi: 10.1002/bjs.4366.
https://doi.org/10.1002/bjs.4366...
. Regarding the difference in tumorigenic pathways, BilIN lesions seem to have higher expression of the mucin core protein MUC 1, probably favoring a more invasive phenotype with respect to cholangiocarcinomas harboring form IPNB11 Abu Hilal M, Aldrighetti L, Dagher I, Edwin B, Troisi RI, Alikhanov R, et al. The Southampton Consensus Guidelines for Laparoscopic Liver Surgery: From Indication to Implementation. Ann Surg. 2018;268(1):11-18. doi: 10.1097/SLA.0000000000002524.
https://doi.org/10.1097/SLA.000000000000...
. Moreover, many studies have supposed BilIN and IPNB to be biliary counterparts of pancreatic intraepithelial neoplasia intraductal papillary neoplasm and intraductal papillary mucinous neoplasm of the pancreas intraductal papillary neoplasm 8,11,13.

Strictly related to the topic of cholangiocarcinoma’s pre-neoplastic lesions, nowadays in clinical practice another issue is emerging, regarding focal undetermined intrahepatic biliary duct strictures.

An appropriate diagnostic evaluation is of paramount importance, because it is currently unknown FIHS’ natural history and if they can harbor malignancy or pre-neoplastic lesions1919 Woo YS, Lee JK, Oh SH, Kim MJ, Jung JG, Lee KH, Lee KT. Role of SpyGlass peroral cholangioscopy in the evaluation of indeterminate biliary lesions. Dig Dis Sci. 2014;59(10):2565-70. doi: 10.1007/s10620-014-3171-x.
https://doi.org/10.1007/s10620-014-3171-...
. Based on the accessibility of the biliary tree and the site of the lesion, biliary strictures can be evaluated by endoscopic retrograde cholangiopancreatography or percutaneous transhepatic cholangiography. Both techniques allow sampling of the strictures and therapeutic biliary stent placing. However, biliary brushing cytology, as reported by Trikudanathan et al.1717 Trikudanathan G, Navaneethan U, Njei B, Vargo JJ, Parsi MA. Diagnostic yield of bile duct brushings for cholangiocarcinoma in primary sclerosing cholangitis: a systematic review and meta-analysis. Gastrointest Endosc. 2014;79(5):783-9. doi: 10.1016/j.gie.2013.09.015.
https://doi.org/10.1016/j.gie.2013.09.01...
in a recent meta-analysis, has a low sensitivity (not exceeding 43%) in detection of cholangiocarcinoma in primary sclerosing cholangitis patients. The same authors, in another meta-analysis, reported that fluorescence in situ hybridization (FISH) was able to increase the sensitivity up to 68%1212 Navaneethan U, Njei B, Venkatesh PG, Vargo JJ, Parsi MA. Fluorescence in situ hybridization for diagnosis of cholangiocarcinoma in primary sclerosing cholangitis: a systematic review and meta-analysis. Gastrointest Endosc. 2014;79(6):943-950.e3. doi: 10.1016/j.gie.2013.11.001.
https://doi.org/10.1016/j.gie.2013.11.00...
.

Another reported technique in the evaluation of indeterminate biliary lesions is the SpyGlass single-operator peroral cholangioscopy44 Brunaldi VO, Brunaldi JE, Vollet-Filho JD, Brunaldi MO, Ardengh JC, Bagnato VS, Dos-Santos JS, Kemp R. Photodynamic therapy of extrahepatic cholangiocarcinoma using digital cholangioscopy. Arq Bras Cir Dig. 2020;33(1):e1490. doi: 10.1590/0102-672020190001e1490
https://doi.org/10.1590/0102-67202019000...
,99 Kurihara T, Yasuda I, Isayama H, Tsuyuguchi T, Yamaguchi T, Kawabe K, Okabe Y, Hanada K, Hayashi T, Ohtsuka T, et al. Diagnostic and therapeutic single-operator cholangiopancreatoscopy in biliopancreatic diseases: Prospective multicenter study in Japan. World J Gastroenterol. 2016;22(5):1891-901. doi: 10.3748/wjg.v22.i5.1891.
https://doi.org/10.3748/wjg.v22.i5.1891...
. Woo et al.1919 Woo YS, Lee JK, Oh SH, Kim MJ, Jung JG, Lee KH, Lee KT. Role of SpyGlass peroral cholangioscopy in the evaluation of indeterminate biliary lesions. Dig Dis Sci. 2014;59(10):2565-70. doi: 10.1007/s10620-014-3171-x.
https://doi.org/10.1007/s10620-014-3171-...
reported that overall accuracy of SpyGlass visual assessment and SpyBite biopsy for the diagnosis of malignancy were 96.7% and 73.6%, respectively. Similar results were obtained in a Japanese large prospective multicenter study (95.5% and 70.7%)99 Kurihara T, Yasuda I, Isayama H, Tsuyuguchi T, Yamaguchi T, Kawabe K, Okabe Y, Hanada K, Hayashi T, Ohtsuka T, et al. Diagnostic and therapeutic single-operator cholangiopancreatoscopy in biliopancreatic diseases: Prospective multicenter study in Japan. World J Gastroenterol. 2016;22(5):1891-901. doi: 10.3748/wjg.v22.i5.1891.
https://doi.org/10.3748/wjg.v22.i5.1891...
. Interestingly, this study reported 10 cases of intrahepatic indeterminate biliary lesions, in which accuracy values decreased (80% and 83.3%). A recent meta-analysis by Sun et al.1515 Sun X, Zhou Z, Tian J, Wang Z, Huang Q, Fan K, Mao Y, Sun G, Yang Y. Is single-operator peroral cholangioscopy a useful tool for the diagnosis of indeterminate biliary lesion? A systematic review and meta-analysis. Gastrointest Endosc. 2015;82(1):79-87. doi: 10.1016/j.gie.2014.12.021.
https://doi.org/10.1016/j.gie.2014.12.02...
, considering the usefulness of this diagnostic tool in determining malignancy in biliary lesions, reported sensitivity and specificity of visual assessment and visual guided biopsy of 90-87% and 69-98%, respectively. Currently, no study has demonstrated the ability of CT scan or MRCP, as well as endoscopic or intraductal ultrasound, to differentiate benign from malignant intrahepatic strictures.

Regarding treatment, due to the undefined possibility of FIHS to harbor malignancy, it has been advocated that stricture should be resected whenever, during the diagnostic work-up, a malignant diagnosis is suspected or of course ascertained. Yeo et al.2020 Yeo D, Perini MV, Muralidharan V, Christophi C. Focal intrahepatic strictures: a review of diagnosis and management. HPB (Oxford). 2012;14(7):425-34. doi: 10.1111/j.1477-2574.2012.00481.x.
https://doi.org/10.1111/j.1477-2574.2012...
, in their review, proposed an interesting algorithm treatment for FIHS: after a two level diagnostic work-up, based on non-invasive and invasive diagnostic tools, in case of supposed benign stricture, cholangioscopy with or without biopsy should be performed. If a benign stricture is confirmed, treatment should be reserved only to symptomatic patients and could be surgical or non-surgical (endoscopic, percutaneous). Regarding the surgical technique, in the last decade, we have assisted to the spreading of laparoscopic liver resection worldwide11 Abu Hilal M, Aldrighetti L, Dagher I, Edwin B, Troisi RI, Alikhanov R, et al. The Southampton Consensus Guidelines for Laparoscopic Liver Surgery: From Indication to Implementation. Ann Surg. 2018;268(1):11-18. doi: 10.1097/SLA.0000000000002524.
https://doi.org/10.1097/SLA.000000000000...
and several cases of laparoscopic liver resection for intrahepatic bile duct dilatation with associated hepatolithiasis, a condition quite similar to FIHS, have been described55 Cai X, Wang Y, Yu H, Liang X, Peng S. Laparoscopic hepatectomy for hepatolithiasis: a feasibility and safety study in 29 patients. Surg Endosc. 2007;21(7):1074-8. doi: 10.1007/s00464-007-9306-9.
https://doi.org/10.1007/s00464-007-9306-...
,66 Dagher I, Diop PS, Lainas P, Carloni A, Franco D. Laparoscopic liver resection for localized primary intrahepatic bile duct dilatation. Am J Surg. 2010;199(1):131-5. doi: 10.1016/j.amjsurg.2008.12.027.
https://doi.org/10.1016/j.amjsurg.2008.1...
,1515 Sun X, Zhou Z, Tian J, Wang Z, Huang Q, Fan K, Mao Y, Sun G, Yang Y. Is single-operator peroral cholangioscopy a useful tool for the diagnosis of indeterminate biliary lesion? A systematic review and meta-analysis. Gastrointest Endosc. 2015;82(1):79-87. doi: 10.1016/j.gie.2014.12.021.
https://doi.org/10.1016/j.gie.2014.12.02...
. In our centre, we performed in 2019 two cases of left biliary duct stricture who underwent laparoscopic left hepatectomy with final diagnosis of BilIN1010 Nagtegaal ID, Odze RD, Klimstra D, Paradis V, Rugge M, Schirmacher P, Washington KM, Carneiro F, Cree IA; WHO Classification of Tumours Editorial Board. The 2019 WHO classification of tumours of the digestive system. Histopathology. 2020;76(2):182-188. doi: 10.1111/his.13975.
https://doi.org/10.1111/his.13975...
,2020 Yeo D, Perini MV, Muralidharan V, Christophi C. Focal intrahepatic strictures: a review of diagnosis and management. HPB (Oxford). 2012;14(7):425-34. doi: 10.1111/j.1477-2574.2012.00481.x.
https://doi.org/10.1111/j.1477-2574.2012...
. In a retrospective Korean series involving 24 patients who underwent surgical resection for bile duct dilatation without demonstrable mass on pre-operative imaging, Kim et al.77 Kim HJ, Lee KT, Kim SH, Lee JK, Lim JH, Paik SW, Rhee JC. Differential diagnosis of intrahepatic bile duct dilatation without demonstrable mass on ultrasonography or CT: benign versus malignancy. J Gastroenterol Hepatol. 2003;18(11):1287-92. doi: 10.1046/j.1440-1746.2003.03169.x.
https://doi.org/10.1046/j.1440-1746.2003...
found in half of patients (n=12) malignancy at the final pathology. From a morphological point of view these patients, compared to those with benign bile duct stricture, showed thickening of bile duct wall ≥5 mm and regional lymph node enlargement on CT scan, abrupt cut-off and bile duct separation on cholangiogram. The prospective series by Seo et al.1414 Seo DW, Kim MH, Lee SK, Myung SJ, Kang GH, Ha HK, Suh DJ, Min YI. Usefulness of cholangioscopy in patients with focal stricture of the intrahepatic duct unrelated to intrahepatic stones. Gastrointest Endosc. 1999;49(2):204-9. doi: 10.1016/s0016-5107(99)70487-6.
https://doi.org/10.1016/s0016-5107(99)70...
on percutaneous transhepatic cholangioscopy included 17 patients with FIHS without stones: a histopathologic diagnosis was obtained in all patients (9 adenocarcinomas, 1 squamous cell carcinoma, 2 hepatocellular carcinomas, 2 adenomas and 3 benign strictures). Of the nine with bile duct adenocarcinoma, eight underwent surgery and a curative resection was possible in seven patients. Interestingly, five patients had early-stage bile duct cancer in which cancer invasion was limited to the mucosa or fibromuscular layer and there was no evidence of lymph node metastasis.

CONCLUSION

It is raising the fact that FIHS can harbor pre-neoplastic lesions (BilIN). The diagnostic work-up is often inconclusive in order to rule out malignancy, but in literature cholangioscopy with biopsy is emerging as a promising technique to overcome this issue, even if it is not widespread and available in every center as it deserves a specific training and equipment. Whenever the suspicion of malignancy is moderate to high, we believe that surgery is fully justified, as it can represent a kind of preventive treatment of cholangiocarcinoma. Minimally invasive liver resection in this setting could represent the optimal choice. As high level evidence in this topic is still lacking in literature, we call for national and international registers to address the issue of diagnosis and management of focal intrahepatic undetermined strictures.

REFERENCES

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    » https://doi.org/10.1016/s0016-5107(99)70487-6
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    » https://doi.org/10.1002/bjs.4366
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    » https://doi.org/10.1016/j.gie.2013.09.015
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    Witjes CD, Karim-Kos HE, Visser O, de Vries E, IJzermans JN, de Man RA, Coebergh JW, Verhoef C. Intrahepatic cholangiocarcinoma in a low endemic area: rising incidence and improved survival. HPB (Oxford). 2012;14(11):777-81. doi: 10.1111/j.1477-2574.2012.00536.x.
    » https://doi.org/10.1111/j.1477-2574.2012.00536.x
  • 19
    Woo YS, Lee JK, Oh SH, Kim MJ, Jung JG, Lee KH, Lee KT. Role of SpyGlass peroral cholangioscopy in the evaluation of indeterminate biliary lesions. Dig Dis Sci. 2014;59(10):2565-70. doi: 10.1007/s10620-014-3171-x.
    » https://doi.org/10.1007/s10620-014-3171-x
  • 20
    Yeo D, Perini MV, Muralidharan V, Christophi C. Focal intrahepatic strictures: a review of diagnosis and management. HPB (Oxford). 2012;14(7):425-34. doi: 10.1111/j.1477-2574.2012.00481.x.
    » https://doi.org/10.1111/j.1477-2574.2012.00481.x
  • 21
    Zen Y, Adsay NV, Bardadin K, Colombari R, Ferrell L, Haga H, Hong SM, Hytiroglou P, Klöppel G, Lauwers GY, et al. Biliary intraepithelial neoplasia: an international interobserver agreement study and proposal for diagnostic criteria. Mod Pathol. 2007;20(6):701-9. doi: 10.1038/modpathol.3800788.
    » https://doi.org/10.1038/modpathol.3800788
  • 22
    Zen Y, Sasaki M, Fujii T, Chen TC, Chen MF, Yeh TS, Jan YY, Huang SF, Nimura Y, Nakanuma Y. Different expression patterns of mucin core proteins and cytokeratins during intrahepatic cholangiocarcinogenesis from biliary intraepithelial neoplasia and intraductal papillary neoplasm of the bile duct--an immunohistochemical study of 110 cases of hepatolithiasis. J Hepatol. 2006;44(2):350-8. doi: 10.1016/j.jhep.2005.09.025.
    » https://doi.org/10.1016/j.jhep.2005.09.025

  • Fundings:

    None

Publication Dates

  • Publication in this collection
    05 Jan 2022
  • Date of issue
    2021

History

  • Received
    20 Feb 2020
  • Accepted
    27 Apr 2021
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