Skip to main content

Advertisement

SpringerLink
Log in

Reappraisal of T1b gallbladder cancer (GBC): clinicopathologic analysis of 473 in situ and invasive GBCs and critical review of the literature highlights its rarity, and that it has a very good prognosis

  • ORIGINAL ARTICLE
  • Published:
Virchows Archiv Aims and scope Submit manuscript

Abstract

There are highly conflicting data on relative frequency (2–32%), prognosis, and management of pT1b-gallbladder carcinoma (GBC), with 5-year survival ranging from > 90% in East/Chile where cholecystectomy is regarded as curative, versus < 50% in the West, with radical operations post-cholecystectomy being recommended by guidelines. A total of 473 in situ and invasive extensively sampled GBCs from the USA (n = 225) and Chile (n = 248) were re-evaluated histopathologically per Western invasiveness criteria. 349 had invasive carcinoma, and only 24 were pT1. Seven cases previously staged as pT1b were re-classified as pT2. There were 19 cases (5% of all invasive GBCs) qualified as pT1b and most pT1b carcinomas were minute (< 1mm). One patient with extensive pTis at margins (but pT1b focus away from the margins) died of GBC at 27 months, two died of other causes, and the remainder were alive without disease (median follow-up 69.9 months; 5-year disease-specific survival, 92%). In conclusion, careful pathologic analysis of well-sampled cases reveals that only 5% of invasive GBCs are pT1b, with a 5-year disease-specific survival of > 90%, similar to findings in the East. This supports the inclusion of pT1b in the “early GBC” category, as is typically done in high-incidence regions. Pathologic mis-staging of pT2 as pT1 is not uncommon. Cases should not be classified as pT1b unless extensive, preferably total, sampling of the gallbladder to rule out a subtle pT2 is performed. Critical appraisal of the literature reveals that the Western guidelines are based on either SEER or mis-interpretation of stage IB cases as “pT1b.” Although the prognosis of pT1b-GBC is very good, additional surgery (radical cholecystectomy) may be indicated, and long-term surveillance of the biliary tract is warranted.

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
Fig. 4

Similar content being viewed by others

Data availability

The data reported in this manuscript are available from the corresponding author upon reasonable request.

References

  1. Duffy A, Capanu M, Abou-Alfa GK, Huitzil D, Jarnagin W, Fong Y, D’Angelica M, Dematteo RP, Blumgart LH, O’Reilly EM (2008) Gallbladder cancer (GBC): 10-year experience at Memorial Sloan-Kettering Cancer Centre (MSKCC). J Surg Oncol 98:485–489. https://doi.org/10.1002/jso.21141

    Article  CAS  PubMed  Google Scholar 

  2. Wagholikar GD, Behari A, Krishnani N, Kumar A, Sikora SS, Saxena R, Kapoor VK (2002) Early gallbladder cancer. J Am Coll Surg 194:137–141. https://doi.org/10.1016/s1072-7515(01)01136-x

    Article  PubMed  Google Scholar 

  3. Wakai T, Shirai Y, Yokoyama N, Nagakura S, Watanabe H, Hatakeyama K (2001) Early gallbladder carcinoma does not warrant radical resection. Br J Surg 88:675–678. https://doi.org/10.1046/j.1365-2168.2001.01749.x

    Article  CAS  PubMed  Google Scholar 

  4. Yuza K, Sakata J, Prasoon P, Hirose Y, Ohashi T, Toge K, Miura K, Nagahashi M, Kobayashi T, Wakai T (2020) Long-term outcomes of surgical resection for T1b gallbladder cancer: an institutional evaluation. BMC Cancer 20:20. https://doi.org/10.1186/s12885-019-6507-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Butte JM, Matsuo K, Gonen M, D’Angelica MI, Waugh E, Allen PJ, Fong Y, DeMatteo RP, Blumgart L, Endo I, De La Fuente H, Jarnagin WR (2011) Gallbladder cancer: differences in presentation, surgical treatment, and survival in patients treated at centers in three countries. J Am Coll Surg 212:50–61. https://doi.org/10.1016/j.jamcollsurg.2010.09.009

    Article  PubMed  Google Scholar 

  6. Cangemi V, Fiori E, Picchi C, De Cesare A, Cangemi R, Galati G, Volpino P (2006) Early gallbladder carcinoma: a single-center experience. Tumori 92:487–490

    Article  PubMed  Google Scholar 

  7. Ethun CG, Le N, Lopez-Aguiar AG, Pawlik TM, Poultsides G, Tran T, Idrees K, Isom CA, Fields RC, Krasnick BA, Weber SM, Salem A, Martin RCG, Scoggins CR, Shen P, Mogal HD, Schmidt C, Beal E, Hatzaras I, Shenoy R, Russell MC, Maithel SK (2017) Pathologic and prognostic ımplications of ıncidental versus nonincidental gallbladder cancer: a 10-ınstitution study from the United States extrahepatic biliary malignancy consortium. Am Surg 83:679–686

    Article  PubMed  PubMed Central  Google Scholar 

  8. Fuks D, Regimbeau JM, Pessaux P, Bachellier P, Raventos A, Mantion G, Gigot JF, Chiche L, Pascal G, Azoulay D, Laurent A, Letoublon C, Boleslawski E, Rivoire M, Mabrut JY, Adham M, Le Treut YP, Delpero JR, Navarro F, Ayav A, Boudjema K, Nuzzo G, Scotte M, Farges O (2013) Is port-site resection necessary in the surgical management of gallbladder cancer? J Visc Surg 150:277–284. https://doi.org/10.1016/j.jviscsurg.2013.03.006

    Article  CAS  PubMed  Google Scholar 

  9. Maker AV, Butte JM, Oxenberg J, Kuk D, Gonen M, Fong Y, Dematteo RP, D’Angelica MI, Allen PJ, Jarnagin WR (2012) Is port site resection necessary in the surgical management of gallbladder cancer? Ann Surg Oncol 19:409–417. https://doi.org/10.1245/s10434-011-1850-9

    Article  PubMed  Google Scholar 

  10. Ito H, Ito K, D’Angelica M, Gonen M, Klimstra D, Allen P, DeMatteo RP, Fong Y, Blumgart LH, Jarnagin WR (2011) Accurate staging for gallbladder cancer: implications for surgical therapy and pathological assessment. Ann Surg 254:320–325. https://doi.org/10.1097/SLA.0b013e31822238d8

    Article  PubMed  Google Scholar 

  11. Puhalla H, Wild T, Bareck E, Pokorny H, Ploner M, Soliman T, Stremitzer S, Depisch D, Laengle F, Gruenberger T (2002) Long-term follow-up of surgically treated gallbladder cancer patients. Eur J Surg Oncol 28:857–863. https://doi.org/10.1053/ejso.2002.1301

    Article  CAS  PubMed  Google Scholar 

  12. Yoon JH, Lee YJ, Kim SC, Lee JH, Song KB, Hwang JW, Lee JW, Lee DJ, Park KM (2014) What is the better choice for T1b gallbladder cancer: simple versus extended cholecystectomy. World J Surg 38:3222–3227. https://doi.org/10.1007/s00268-014-2713-x

    Article  PubMed  Google Scholar 

  13. Kang CM, Lee WJ, Choi GH, Kim JY, Kim KS, Choi JS, Kim BR (2007) Does “clinical” R0 have validity in the choice of simple cholecystectomy for gallbladder carcinoma? J Gastrointest Surg 11:1309–1316. https://doi.org/10.1007/s11605-007-0225-9

    Article  PubMed  Google Scholar 

  14. Butte JM, Kingham TP, Gonen M, D’Angelica MI, Allen PJ, Fong Y, DeMatteo RP, Jarnagin WR (2014) Residual disease predicts outcomes after definitive resection for incidental gallbladder cancer. J Am Coll Surg 219:416–429. https://doi.org/10.1016/j.jamcollsurg.2014.01.069

    Article  PubMed  PubMed Central  Google Scholar 

  15. de Savornin Lohman EAJ, van der Geest LG, de Bitter TJJ, Nagtegaal ID, van Laarhoven C, van den Boezem P, van der Post CS, de Reuver PR (2020) Re-resection in ıncidental gallbladder cancer: survival and the ıncidence of residual disease. Ann Surg Oncol 27:1132–1142. https://doi.org/10.1245/s10434-019-08074-4

    Article  PubMed  Google Scholar 

  16. Leigh NL, Solomon D, Feingold D, Hiotis SP, Labow DM, Magge DR, Sarpel U, Golas BJ (2019) Staging gallbladder cancer with lymphadenectomy: the practical application of new AHPBA and AJCC guidelines. HPB (Oxford) 21:1563–1569. https://doi.org/10.1016/j.hpb.2019.03.372

    Article  PubMed  Google Scholar 

  17. Goetze TO, Paolucci V (2014) Immediate radical re-resection of incidental T1b gallbladder cancer and the problem of an adequate extent of resection (results of the German Registry “Incidental Gallbladder Cancer”). Zentralbl Chir 139(Suppl 2):e43-48. https://doi.org/10.1055/s-0030-1262698

    Article  PubMed  Google Scholar 

  18. Kim BH, Kim SH, Song IS, Chun GS (2019) The appropriate surgical strategy for T1b gallbladder cancer incidentally diagnosed after a simple cholecystectomy. Ann Hepatobiliary Pancreat Surg 23:327–333. https://doi.org/10.14701/ahbps.2019.23.4.327

    Article  PubMed  PubMed Central  Google Scholar 

  19. Mayo SC, Shore AD, Nathan H, Edil B, Wolfgang CL, Hirose K, Herman J, Schulick RD, Choti MA, Pawlik TM (2010) National trends in the management and survival of surgically managed gallbladder adenocarcinoma over 15 years: a population-based analysis. J Gastrointest Surg 14:1578–1591. https://doi.org/10.1007/s11605-010-1335-3

    Article  PubMed  Google Scholar 

  20. Goetze TO, Paolucci V (2008) Immediate re-resection of T1 incidental gallbladder carcinomas: a survival analysis of the German Registry. Surg Endosc 22:2462–2465. https://doi.org/10.1007/s00464-008-9747-9

    Article  CAS  PubMed  Google Scholar 

  21. Sung YN, Song M, Lee JH, Song KB, Hwang DW, Ahn CS, Hwang S, Hong SM (2019) Validation of the 8th edition of the American joint committee on cancer staging system for gallbladder cancer and implications for the follow-up of patients without node dissection. Cancer Res Treat. https://doi.org/10.4143/crt.2019.271

    Article  PubMed  PubMed Central  Google Scholar 

  22. Ouchi K, Mikuni J, Kakugawa Y (2002) Laparoscopic cholecystectomy for gallbladder carcinoma: results of a Japanese survey of 498 patients. J Hepatobiliary Pancreat Surg 9:256–260. https://doi.org/10.1007/s005340200028

    Article  PubMed  Google Scholar 

  23. Zhang LF, Hou CS, Xu Z, Guo LM, Ling XF, Wang LX, Xiu DR (2019) [Laparoscopic treatment for incidental gallbladder cancer: a retrospective 10 years study from a single institution] Zhonghua Wai Ke Za Zhi 57:277–281. https://doi.org/10.3760/cma.j.issn.0529-5815.2019.04.007

  24. Glauser PM, Strub D, Käser SA, Mattiello D, Rieben F, Maurer CA (2010) Incidence, management, and outcome of incidental gallbladder carcinoma: analysis of the database of the Swiss association of laparoscopic and thoracoscopic surgery. Surg Endosc 24:2281–2286. https://doi.org/10.1007/s00464-010-0952-y

    Article  PubMed  Google Scholar 

  25. Yamaguchi J, Kaneoka Y, Maeda A, Takayama Y, Onoe S, Isogai M (2016) Benefit of extended radical surgery for incidental gallbladder carcinoma. Surg Today 46:453–459. https://doi.org/10.1007/s00595-015-1198-z

    Article  PubMed  Google Scholar 

  26. Yoon YS, Han HS, Cho JY, Choi Y, Lee W, Jang JY, Choi H (2015) Is laparoscopy contraindicated for gallbladder cancer? A 10-year prospective cohort study. J Am Coll Surg 221:847–853. https://doi.org/10.1016/j.jamcollsurg.2015.07.010

    Article  PubMed  Google Scholar 

  27. Steffen T, Ebinger SM, Tarantino I, Widmann B (2020) Prognostic impact of lymph node excision in T1 and T2 gallbladder cancer: a population-based and propensity score-matched SEER analysis. J Gastrointest Surg 24:633–642. https://doi.org/10.1007/s11605-019-04175-3

    Article  PubMed  Google Scholar 

  28. Hari DM, Howard JH, Leung AM, Chui CG, Sim MS, Bilchik AJ (2013) A 21-year analysis of stage I gallbladder carcinoma: is cholecystectomy alone adequate? HPB (Oxford) 15:40–48. https://doi.org/10.1111/j.1477-2574.2012.00559.x

    Article  PubMed  Google Scholar 

  29. Tian YH, Ji X, Liu B, Yang GY, Meng XF, Xia HT, Wang J, Huang ZQ, Dong JH (2015) Surgical treatment of incidental gallbladder cancer discovered during or following laparoscopic cholecystectomy. World J Surg 39:746–752. https://doi.org/10.1007/s00268-014-2864-9

    Article  PubMed  Google Scholar 

  30. Chong JU, Lee WJ (2019) Oncologic outcomes of extended lymphadenectomy without liver resection for T1/T2 gallbladder cancer. Yonsei Med J 60:1138–1145. https://doi.org/10.3349/ymj.2019.60.12.1138

    Article  PubMed  PubMed Central  Google Scholar 

  31. Benoist S, Panis Y, Fagniez PL (1998) Long-term results after curative resection for carcinoma of the gallbladder. French University Association for Surgical Research. Am J Surg 175:118–122. https://doi.org/10.1016/s0002-9610(97)00269-9

    Article  CAS  PubMed  Google Scholar 

  32. Kim EK, Lee SK, Kim WW (2002) Does laparoscopic surgery have a role in the treatment of gallbladder cancer? J Hepatobiliary Pancreat Surg 9:559–563. https://doi.org/10.1007/s005340200074

    Article  PubMed  Google Scholar 

  33. Shukla PJ, Barreto G, Kakade A, Shrikhande SV (2008) Revision surgery for incidental gallbladder cancer: factors influencing operability and further evidence for T1b tumours. HPB (Oxford) 10:43–47. https://doi.org/10.1080/13651820701867794

    Article  CAS  PubMed  Google Scholar 

  34. Jang JY, Heo JS, Han Y, Chang J, Kim JR, Kim H, Kwon W, Kim SW, Choi SH, Choi DW, Lee K, Jang KT, Han SS, Park SJ (2016) Impact of type of surgery on survival outcome in patients with early gallbladder cancer in the era of minimally invasive surgery: oncologic safety of laparoscopic surgery medicine (Baltimore) 95:e3675. https://doi.org/10.1097/md.0000000000003675

  35. Kim HS, Park JW, Kim H, Han Y, Kwon W, Kim SW, Hwang YJ, Kim SG, Kwon HJ, Vinuela E, Jarufe N, Roa JC, Han IW, Heo JS, Choi SH, Choi DW, Ahn KS, Kang KJ, Lee W, Jeong CY, Hong SC, Troncoso A, Losada H, Han SS, Park SJ, Yanagimoto H, Endo I, Kubota K, Wakai T, Ajiki T, Adsay NV, Jang JY (2018) Optimal surgical treatment in patients with T1b gallbladder cancer: an international multicenter study. J Hepatobiliary Pancreat Sci 25:533–543. https://doi.org/10.1002/jhbp.593

    Article  PubMed  Google Scholar 

  36. Sun CD, Zhang BY, Wu LQ, Lee WJ (2005) Laparoscopic cholecystectomy for treatment of unexpected early-stage gallbladder cancer. J Surg Oncol 91:253–257. https://doi.org/10.1002/jso.20318

    Article  PubMed  Google Scholar 

  37. Roa JC, Tapia O, Manterola C, Villaseca M, Guzman P, Araya JC, Bagci P, Saka B, Adsay V (2013) Early gallbladder carcinoma has a favorable outcome but Rokitansky-Aschoff sinus involvement is an adverse prognostic factor. Virchows Arch 463:651–661. https://doi.org/10.1007/s00428-013-1478-1

    Article  PubMed  Google Scholar 

  38. Roa I, Ibacache G, Munoz S, de Aretxabala X (2014) Gallbladder cancer in Chile: pathologic characteristics of survival and prognostic factors: analysis of 1,366 cases. Am J Clin Pathol 141:675–682. https://doi.org/10.1309/ajcpqt3eln2bbcka

    Article  PubMed  Google Scholar 

  39. Goetze T, Paolucci V (2006) Does laparoscopy worsen the prognosis for incidental gallbladder cancer? Surg Endosc 20:286–293. https://doi.org/10.1007/s00464-005-0121-x

    Article  CAS  PubMed  Google Scholar 

  40. Vo E, Curley SA, Chai CY, Massarweh NN, Tran Cao HS (2019) National failure of surgical staging for T1b gallbladder cancer. Ann Surg Oncol 26:604–610. https://doi.org/10.1245/s10434-018-7064-7

    Article  PubMed  Google Scholar 

  41. Cucinotta E, Lorenzini C, Melita G, Iapichino G, Currò G (2005) Incidental gall bladder carcinoma: does the surgical approach influence the outcome? ANZ J Surg 75:795–798. https://doi.org/10.1111/j.1445-2197.2005.03528.x

    Article  PubMed  Google Scholar 

  42. Miller G, Jarnagin WR (2008) Gallbladder carcinoma Eur J Surg Oncol 34:306–312. https://doi.org/10.1016/j.ejso.2007.07.206

    Article  CAS  PubMed  Google Scholar 

  43. Jayaraman S, Jarnagin WR (2010) Management of gallbladder cancer. Gastroenterol Clin North Am 39(331–342):x. https://doi.org/10.1016/j.gtc.2010.02.006

    Article  PubMed  Google Scholar 

  44. Aloia TA, Jarufe N, Javle M, Maithel SK, Roa JC, Adsay V, Coimbra FJ, Jarnagin WR (2015) Gallbladder cancer: expert consensus statement HPB (Oxford) 17:681-690https://doi.org/10.1111/hpb.12444

  45. Watson H, Dasari B, Wyatt J, Hidalgo E, Prasad R, Lodge P, Toogood G (2017) Does a second resection provide a survival benefit in patients diagnosed with incidental T1b/T2 gallbladder cancer following cholecystectomy? HPB (Oxford) 19:104–107. https://doi.org/10.1016/j.hpb.2016.11.006

    Article  PubMed  Google Scholar 

  46. Regmi P, Hu HJ, Chang-Hao Y, Liu F, Ma WJ, Ran CD, Wang JK, Paudyal A, Cheng NS, Li FY (2020) Laparoscopic surgery for oncologic extended resection of T1b and T2 incidental gallbladder carcinoma at a high-volume center: a single-center experience in China. Surg Endosc. https://doi.org/10.1007/s00464-020-08146-7

    Article  PubMed  Google Scholar 

  47. Huang XT, Huang CS, Li JH, Chen W, Gan TT, Wang XY, Liang LJ, Yin XY (2020) Evaluating the adequacy of nodal status in node-negative gallbladder cancer with T1b-T2 stages: use of nodal staging score HPB (Oxford). https://doi.org/10.1016/j.hpb.2020.09.018

  48. Shirobe T, Maruyama S (2015) Laparoscopic radical cholecystectomy with lymph node dissection for gallbladder carcinoma. Surg Endosc 29:2244–2250. https://doi.org/10.1007/s00464-014-3932-9

    Article  PubMed  Google Scholar 

  49. Adsay NV, Basturk O, Roa JC, Memis B, Pehlivanoglu B, Jang KT, Araya JC, Jang JY, Lee K, Reid MD, Das P, Koshiol J, Balakrishnan A, Palepu J, Shrikhande SV, B. S, Lendoire J, de Aretxabala X, Endo I, Losada H, de Reuver PR, Maithel S, Jarnagin W (2022) Standardization of pathologic sampling and evaluation of gallbladder specimens: recommendations of the International Study Group on Gallbladder Cancer (ISG-GBC) of International Hepato-Pancreato-Biliary Association (IHPBA) (USCAP 2022 Abstracts: Pancreas, Gallbladder, Ampulla, and Extra-Hepatic Biliary Tree). Mod Pathol 35:1206https://doi.org/10.1038/s41379-022-01046-2

  50. DeSimone MS, Goodman M, Pehlivanoglu B, Memis B, Balci S, Roa JC, Jang KT, Jang JY, Hong SM, Lee K, Kim H, Choi HJ, Muraki T, Araya JC, Bellolio E, Sarmiento JM, Maithel SK, Losada HF, Basturk O, Reid MD, Koshiol J, Adsay V (2021) T2 gallbladder cancer shows substantial survival variation between continents and this is not due to histopathologic criteria or pathologic sampling differences. Virchows Arch 478:875–884. https://doi.org/10.1007/s00428-020-02968-5

    Article  CAS  PubMed  Google Scholar 

  51. Amin MB, Edge SB, Greene FL et al (eds) (2017) AJCC cancer staging manual, 8th edn. Springer, New York, NY

    Google Scholar 

  52. Roa I, Araya JC, Wistuba I, Villaseca M, de Aretxabala X, Busel D, Burgos L (1993) Epithelial lesions associated with gallbladder carcinoma. A methodical study of 32 cases. Rev Med Chil 121:21–29

    CAS  PubMed  Google Scholar 

  53. Roa I, de Aretxabala X, Araya JC, Villaseca M, Roa J, Guzmán P (2001) Incipient gallbladder carcinoma. Clinical and pathological study and prognosis in 196 cases. Rev Med Chil 129:1113–1120

    CAS  PubMed  Google Scholar 

  54. Memis B, Reid MD, Bedolla G, Roa JC, Araya JC, Bellolio E, Villaseca M, Van Dyke AL, Xue Y, Quigley B, Krasinskas A, Polito H, Ghosh A, Koshiol J, Adsay NV (2017) Pathologic findings in gallbladders: an analysis of the true frequency and distribution in 203 totally sampled and mapped gallbladders from a North American population (abstract, pancreas and biliary tree). Mod Pathol 30:447A. https://doi.org/10.1038/modpathol.2016.259

    Article  Google Scholar 

  55. Mazer LM, Losada HF, Chaudhry RM, Velazquez-Ramirez GA, Donohue JH, Kooby DA, Nagorney DM, Adsay NV, Sarmiento JM (2012) Tumor characteristics and survival analysis of incidental versus suspected gallbladder carcinoma. J Gastrointest Surg 16:1311–1317. https://doi.org/10.1007/s11605-012-1901-y

    Article  PubMed  PubMed Central  Google Scholar 

  56. Memis B, Roa JC, Muraki T, Hacihasanoglu E, Dursun N, Saka B, Bellolio E, Araya JC, Sarmiento J, Losada H, Kooby DA, Maithel S, Reid MD, Quigley B, Krasinskas A, Adsay NV (2016) Not All T2 Gallbladder Carcinomas (GBC) Are equal: proposal for sub-staging of T2 GBC with significant prognostic value (abstract). Mod Pathol 29:445. https://doi.org/10.1038/modpathol.2016.19

    Article  Google Scholar 

  57. Roa JC, Basturk O, Torres J, Mucientes F, del Pozo M, Villaseca M, Aguayo G, Bellolio E, Araya JC, Endo I, Jang KT, Lee KB, Jang JY, Ohike N, Schimizu M, Hirabayashi K, Terris B, Zamboni G, Reid MD, Xue Y, Bedolla G, Quigley B, Krasinskas A, Akkas G, Memis B, Klimstra D, Hruban R, Zhu B, Van Dyke AL, Koshiol J, Adsay NV (2016) Marked geographic differences in the pathologic diagnosis of non-invasive (Tis) vs minimally invasive (T1) gallbladder cancer: Santiago consensus conference highlights the need for the unifying category “early gallbladder cancer” (EGBC) (Abstract). Mod Pathol 29:447

    Google Scholar 

  58. Adsay V, Jang KT, Roa JC, Dursun N, Ohike N, Bagci P, Basturk O, Bandyopadhyay S, Cheng JD, Sarmiento JM, Escalona OT, Goodman M, Kong SY, Terry P (2012) Intracholecystic papillary-tubular neoplasms (ICPN) of the gallbladder (neoplastic polyps, adenomas, and papillary neoplasms that are ≥1.0 cm): clinicopathologic and immunohistochemical analysis of 123 cases. Am J Surg Pathol 36:1279–1301. https://doi.org/10.1097/PAS.0b013e318262787c

    Article  PubMed  Google Scholar 

  59. Principe A, Del Gaudio M, Ercolani G, Golfieri R, Cucchetti A, Pinna AD (2006) Radical surgery for gallbladder carcinoma: possibilities of survival. Hepatogastroenterology 53:660–664

    PubMed  Google Scholar 

  60. Foster JM, Hoshi H, Gibbs JF, Iyer R, Javle M, Chu Q, Kuvshinoff B (2007) Gallbladder cancer: defining the indications for primary radical resection and radical re-resection. Ann Surg Oncol 14:833–840. https://doi.org/10.1245/s10434-006-9097-6

    Article  PubMed  Google Scholar 

  61. Ouchi K, Sugawara T, Ono H, Fujiya T, Kamiyama Y, Kakugawa Y, Mikuni J, Endo K (1999) Diagnostic capability and rational resectional surgery for early gallbladder cancer. Hepatogastroenterology 46:1557–1560

    CAS  PubMed  Google Scholar 

  62. Wang Z, Li Y, Jiang W, Yan J, Dai J, Jiao B, Yin Z, Zhang Y (2019) Simple cholecystectomy is adequate for patients with T1b gallbladder adenocarcinoma < 1 cm in diameter. Front Oncol 9:409. https://doi.org/10.3389/fonc.2019.00409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Schauer RJ, Meyer G, Baretton G, Schildberg FW, Rau HG (2001) Prognostic factors and long-term results after surgery for gallbladder carcinoma: a retrospective study of 127 patients. Langenbecks Arch Surg 386:110–117. https://doi.org/10.1007/s004230000189

    Article  CAS  PubMed  Google Scholar 

  64. Muraki T, Pehlivanoglu B, Memis B, Reid MD, Uehara T, Basturk O, Pernicka JG, Klimstra DS, Jarnagin WR, Ito T, Hasebe O, Okaniwa S, Horigome N, Hisa T, Mittal P, Sarmiento JM, Maithel SK, Koshiol J, Tsai S, Evans D, Erkan M, Adsay V (2020) Pancreatobiliary maljunction-associated gallbladder cancer is as common in the west, shows distinct clinicopathologic characteristics and offers an invaluable model for anatomy-induced reflux-associated physio-chemical carcinogenesis. Ann Surg. https://doi.org/10.1097/sla.0000000000004482

    Article  PubMed  Google Scholar 

  65. Reid MD, Losada H, Muraki T, Pehlivanoglu B, Memis B, Koshiol J, Bagci P, Seven Erbarut I, Balci S, Saka B, Dursun N, Jang KT, Ohike N, Tajiri T, Goodman M, Roa JC, Araya JC, Bellolio E, Sarmiento J, Xue Y, Basturk O, Adsay V (2019) Field risk (“field-effect”/“field-defect”) in the gallbladder and biliary tree: an under-recognized phenomenon with major implications for management and carcinogenesis (abstract). Mod Pathol 32:43

    Google Scholar 

  66. Hasumi A, Matsui H, Sugioka A, Uyama I, Komori Y, Fujita J, Aoki H (2000) Precancerous conditions of biliary tract cancer in patients with pancreaticobiliary maljunction: reappraisal of nationwide survey in Japan. J Hepatobiliary Pancreat Surg 7:551–555. https://doi.org/10.1007/s005340070003

    Article  CAS  PubMed  Google Scholar 

  67. Downing SR, Cadogan KA, Ortega G, Oyetunji TA, Siram SM, Chang DC, Ahuja N, Leffall LD Jr, Frederick WA (2011) Early-stage gallbladder cancer in the surveillance, epidemiology, and end results database: effect of extended surgical resection. Arch Surg 146:734–738. https://doi.org/10.1001/archsurg.2011.128

    Article  PubMed  Google Scholar 

  68. Cubertafond P, Gainant A, Cucchiaro G (1994) Surgical treatment of 724 carcinomas of the gallbladder. Results of the French Surgical Association Survey Ann Surg 219:275–280. https://doi.org/10.1097/00000658-199403000-00007

    Article  CAS  PubMed  Google Scholar 

  69. Bertran E, Heise K, Andia ME, Ferreccio C (2010) Gallbladder cancer: incidence and survival in a high-risk area of Chile. Int J Cancer 127:2446–2454. https://doi.org/10.1002/ijc.25421

    Article  CAS  PubMed  Google Scholar 

  70. de Aretxabala X, Roa I, Hepp J, Maluenda F, Mordojovich G, Leon J, Roa JC (2009) Early gallbladder cancer: is further treatment necessary? J Surg Oncol 100:589–593. https://doi.org/10.1002/jso.21389

    Article  PubMed  Google Scholar 

  71. Chan SY, Poon RT, Lo CM, Ng KK, Fan ST (2008) Management of carcinoma of the gallbladder: a single-institution experience in 16 years. J Surg Oncol 97:156–164. https://doi.org/10.1002/jso.20885

    Article  PubMed  Google Scholar 

  72. Lee SE, Jang JY, Kim SW, Han HS, Kim HJ, Yun SS, Cho BH, Yu HC, Lee WJ, Yoon DS, Choi DW, Choi SH, Hong SC, Lee SM, Kim HJ, Choi IS, Song IS, Park SJ, Jo S (2014) Surgical strategy for T1 gallbladder cancer: a nationwide multicenter survey in South Korea. Ann Surg Oncol 21:3654–3660. https://doi.org/10.1245/s10434-014-3527-7

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pathology, Emory University School of Medicine, Atlanta, GA, USA

    Burcin Pehlivanoglu, Gizem Akkas, Bahar Memis, Michelle D. Reid, Burcu Saka & Serdar Balci

  2. Current affiliation: Department of Pathology, Dokuz Eylul University, Izmir, Turkey

    Burcin Pehlivanoglu

  3. Current affiliation: Department of Pathology, Faculty of Medicine, Kutahya University of Health Sciences, Kutahya, Turkey

    Gizem Akkas

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

    Olca Basturk

  5. Department of Pathology, University of Health Sciences, Istanbul Education and Research Hospital, Istanbul, Turkey

    Nevra Dursun

  6. Department of Pathology, Marmara University School of Medicine, Istanbul, Turkey

    Pelin Bagci

  7. Department of Surgery, Emory University School of Medicine, Atlanta, GA, USA

    Juan Sarmiento & Shishir K. Maithel

  8. Department of Pathology, Wayne State University School of Medicine, Detroit, MI, USA

    Sudeshna Bandyopadhyay

  9. Department of Pathology, Universidad de La Frontera, Temuco, Chile

    Oscar Tapia Escalona

  10. Department of Pathology, Hospital Dr. Hernan Henriquez Aravena, Temuco, Chile

    Juan Carlos Araya

  11. Department of Surgery and Traumatology, Universidad de La Frontera, Temuco, Chile

    Hector Losada

  12. Department of Epidemiology, Emory University Rollins School of Public Health, Atlanta, GA, USA

    Michael Goodman & Jessica Holley Knight

  13. Department of Pathology, Pontificia Universidad Catolica de Chile, Santiago, Chile

    Juan Carlos Roa

  14. Department of Pathology, Koç University Hospital, Davutpaşa Caddesi No:4, Topkapi, 34010, Istanbul, Turkey

    Volkan Adsay

  15. Koç University Research Center for Translational Medicine (KUTTAM), Istanbul, Turkey

    Volkan Adsay

Authors
  1. Burcin Pehlivanoglu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gizem Akkas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bahar Memis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Olca Basturk
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michelle D. Reid
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Burcu Saka
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nevra Dursun
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Pelin Bagci
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Serdar Balci
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Juan Sarmiento
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Shishir K. Maithel
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Sudeshna Bandyopadhyay
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Oscar Tapia Escalona
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Juan Carlos Araya
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Hector Losada
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Michael Goodman
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Jessica Holley Knight
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Juan Carlos Roa
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Volkan Adsay
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors agreed with the content and gave explicit consent to submit this work. All authors made substantial contributions to the conception, design, case acquisition, analysis, and interpretation of data, and assisted with drafting and revising the work, and approving the version to be published. The authors agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. Each investigator contributed significantly in multiple ways as outlined below:

VA, JCR, MDR, and OB conceived the study and designed the approach and analytic methods along with MG and JHK. Case procurement for study, case organization, and collection of clinical information including survival data were performed by JS, SKM, and SB from the USA, JCR, HL, JCA, and OTE from Chile. The initial histopathologic review was conducted by VA, GA, BM, MDR, SB, and OB for cases from the USA, and JCA, and JCR for Chilean cases. The second histopathologic review was performed by VA, BP, GA, BM, and MDR. BP, GA, BM, BS, PB, SB, OB, and VA conducted the literature analysis and organization of the manuscript. Statistical analysis was performed by MG, JHK, and BP. BP, GA, OB, MDR, JCR, and VA prepared the manuscript draft. All authors of this paper have critically reviewed the intellectual content and approved the final version submitted.

Corresponding author

Correspondence to Volkan Adsay.

Ethics declarations

Ethics approval

The study was conducted in accordance with the Institutional Review Board requirements.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

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

Drs. Pehlivanoglu and Akkas are co-contributing first authors.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pehlivanoglu, B., Akkas, G., Memis, B. et al. Reappraisal of T1b gallbladder cancer (GBC): clinicopathologic analysis of 473 in situ and invasive GBCs and critical review of the literature highlights its rarity, and that it has a very good prognosis. Virchows Arch 482, 311–323 (2023). https://doi.org/10.1007/s00428-022-03482-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00428-022-03482-6

Keywords

Search

Navigation