Annals of Hepato-Biliary-Pancreatic Surgery (한국간담췌외과학회지)

The Korean Association of Hepato-Biliary-Pancreatic Surgery (한국간담췌외과학회)
권호 표지
DOI QR코드

DOI QR Code

Undifferentiated carcinoma with osteoclast-like giant cells of the pancreas: An individual participant data meta-analysis

  • Adam Mylonakis (First Department of Surgery, National and Kapodistrian University of Athens, Laikon General Hospital) ;
  • Tatiana S. Driva (First Department of Pathology, National and Kapodistrian University of Athens, Medical School) ;
  • Panagis Lykoudis (Third Department of Surgery, National and Kapodistrian University of Athens, Attikon University Hospital) ;
  • Maximos Frountzas (First Propaedeutic Department of Surgery, National and Kapodistrian University of Athens, Hippokration General Hospital) ;
  • Nikolaos Machairas (Second Department of Propaedeutic Surgery, National and Kapodistrian University of Athens, Laikon General Hospital) ;
  • Dimitrios Tsapralis (Department of Surgery, General Hospital of Ierapetra) ;
  • Konstantinos G. Toutouzas (First Propaedeutic Department of Surgery, National and Kapodistrian University of Athens, Hippokration General Hospital) ;
  • Dimitrios Schizas (First Department of Surgery, National and Kapodistrian University of Athens, Laikon General Hospital)
  • Received : 2023.11.30
  • Accepted : 2024.01.25
  • Published : 2024.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

Undifferentiated carcinoma with osteoclast-like giant cells (UC-OGCs) of the pancreas is a rare neoplasm that accounts for less than 1% of all pancreatic malignancies. The aim of this study was to review the literature regarding UC-OGC, and to highlight its biological behavior, clinicopathologic characteristics, prognosis, and therapeutic options. A systematic review of the literature in PubMed/Medline and Scopus databases was performed (last search October 31st, 2023) for articles concerning pancreatic UC-OGC in the adult population. Fifty-seven studies met the inclusion criteria, involving 69 patients with a male-to-female ratio of 1.1:1 and a mean age of 62.96. Main symptoms included abdominal pain (33.3%), jaundice (14.5%), weight loss (8.7%), while fourteen patients (20.3%) were asymptomatic. Surgical resection was performed in 88.4% of cases. Survival rates at one, three, and five years were 58%, 44.7%, and 37.3% respectively. Sex, age, size (cut-off of 4 cm), location, and adjuvant treatment did not significantly affect patient survival. UC-OGC of the pancreas is a rare subtype of undifferentiated pancreatic carcinoma with a better prognosis than conventional pancreatic ductal adenocarcinoma or undifferentiated carcinoma without giant cells. The establishment of a dedicated patient registry is imperative to further delineate the optimal treatment for this uncommon clinical entity.

Keywords

References

  1. Nagtegaal ID, Odze RD, Klimstra D, Paradis V, Rugge M, Schirmacher P, et al. The 2019 WHO classification of tumours of the digestive system. Histopathology 2020;76:1821188.
  2. Demetter P, Marechal R, Puleo F, Delhaye M, Debroux S, Charara F, et al. Undifferentiated pancreatic carcinoma with osteoclast-like giant cells: what do we know so far? Front Oncol 2021;11:630086.
  3. Maksymov V, Khalifa MA, Bussey A, Carter B, Hogan M. Undifferentiated (anaplastic) carcinoma of the pancreas with osteoclast-like giant cells showing various degree of pancreas duct involvement. A case report and literature review. JOP 2011;12:170-176.
  4. Gao HQ, Yang YM, Zhuang Y, Liu P. Locally advanced undifferentiated carcinoma with osteoclast-like giant cells of the pancreas. World J Gastroenterol 2015;21:694-698.
  5. Loya AC, Ratnakar KS, Shastry RA. Combined osteoclastic giant cell and pleomorphic giant cell tumor of the pancreas: a rarity. An immunohistochemical analysis and review of the literature. JOP 2004;5:220-224.
  6. Ashfaq A, Thalambedu N, Atiq MU. A rare case of pancreatic cancer: undifferentiated carcinoma of the pancreas with osteoclast-like giant cells. Cureus 2022;14:e25118.
  7. Guo YL, Ruan LT, Wang QP, Lian J. Undifferentiated carcinoma with osteoclast-like giant cells of pancreas: a case report with review of the computed tomography findings. Medicine (Baltimore) 2018;97:e13516.
  8. Zou XP, Yu ZL, Li ZS, Zhou GZ. Clinicopathological features of giant cell carcinoma of the pancreas. Hepatobiliary Pancreat Dis Int 2004;3:300-302.
  9. Lukas Z, Dvorak K, Kroupova I, Valaskova I, Habanec B. Immunohistochemical and genetic analysis of osteoclastic giant cell tumor of the pancreas. Pancreas 2006;32:325-329.
  10. Paal E, Thompson LD, Frommelt RA, Przygodzki RM, Heffess CS. A clinicopathologic and immunohistochemical study of 35 anaplastic carcinomas of the pancreas with a review of the literature. Ann Diagn Pathol 2001; 5:129-140.
  11. Bergmann F, Esposito I, Michalski CW, Herpel E, Friess H, Schirmacher P. Early undifferentiated pancreatic carcinoma with osteoclastlike giant cells: direct evidence for ductal evolution. Am J Surg Pathol 2007;31:1919-1925.
  12. Wada T, Itano O, Oshima G, Chiba N, Ishikawa H, Koyama Y, et al. A male case of an undifferentiated carcinoma with osteoclast-like giant cells originating in an indeterminate mucin-producing cystic neoplasm of the pancreas. A case report and review of the literature. World J Surg Oncol 2011;9:100.
  13. Hirano H, Morita K, Tachibana S, Okimura A, Fujisawa T, Ouchi S, et al. Undifferentiated carcinoma with osteoclast-like giant cells arising in a mucinous cystic neoplasm of the pancreas. Pathol Int 2008;58:383-389.
  14. Muraki T, Reid MD, Basturk O, Jang KT, Bedolla G, Bagci P, et al. Undifferentiated carcinoma with osteoclastic giant cells of the pancreas: clinicopathologic analysis of 38 cases highlights a more protracted clinical course than currently appreciated. Am J Surg Pathol 2016;40:1203-1216.
  15. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372:n71.
  16. Yazawa T, Watanabe A, Araki K, Segawa A, Hirai K, Kubo N, et al. Complete resection of a huge pancreatic undifferentiated carcinoma with osteoclast-like giant cells. Int Cancer Conf J 2017;6:193-196.
  17. Olayinka O, Kaur G, Gupta G. Undifferentiated pancreatic carcinoma with osteoclast-like giant cells and associated ductal adenocarcinoma with focal signet-ring features. Cureus 2021;13:e14988.
  18. Hur YH, Kim HH, Seoung JS, Seo KW, Kim JW, Jeong YY, et al. Undifferentiated carcinoma of the pancreas with osteoclast-like giant cells. J Korean Surg Soc 2011;81:146-150.
  19. Vnuk K, Pavic I, Brletic D, Zovak M, Kruslin B. Undifferentiated carcinoma of the pancreas with osteoclast-like giant cells: report of two cases. Lib Oncol 2022;50:39-43.
  20. Matsubayashi H, Kaneko J, Sato J, Satoh T, Ishiwatari H, Sugiura T, et al. Osteoclast-like giant cell-type pancreatic anaplastic carcinoma presenting with a duodenal polypoid lesion. Intern Med 2019;58:3545-3550.
  21. Osaka H, Yashiro M, Nishino H, Nakata B, Ohira M, Hirakawa K. A case of osteoclast-type giant cell tumor of the pancreas with high-frequency microsatellite instability. Pancreas 2004;29:239-241.
  22. Igarashi Y, Gocho T, Taniai T, Uwagawa T, Hamura R, Shirai Y, et al. Conversion surgery for undifferentiated carcinoma with osteoclast-like giant cells of the pancreas: a case report. Surg Case Rep 2022;8:42.
  23. Kharkhach A, Bouhout T, Serji B, El Harroudi T. Undifferentiated pancreatic carcinoma with osteoclast-like giant cells: a review and case report analysis. J Gastrointest Cancer 2021;52:1106-1113.
  24. Lahiff C, Swan N, Conlon K, Malone D, Maguire D, Hoti E, et al. Osteoclastic-type giant cell tumours of the pancreas: a homogenous series of rare tumours diagnosed by endoscopic ultrasound. Dig Surg 2016;33:401-405.
  25. Obayashi M, Shibasaki Y, Koakutsu T, Hayashi Y, Shoji T, Hirayama K, et al. Pancreatic undifferentiated carcinoma with osteoclast-like giant cells curatively resected after pembrolizumab therapy for lung metastases: a case report. BMC Gastroenterol 2020;20:220.
  26. Speisky D, Villarroel M, Vigovich F, Iotti A, Garcia TA, Quero LB, et al. Undifferentiated carcinoma with osteoclast-like giant cells of the pancreas diagnosed by endoscopic ultrasound guided biopsy. Ecancermedicalscience 2020;14:1072.
  27. Swaid MB, Vitale E, Alatassi N, Siddiqui H, Yazdani H. Metastatic undifferentiated osteoclast-like giant cell pancreatic carcinoma. Cureus 2022;14:e27586.
  28. Pop RM, Diaconu CI, Rimbas M, Mateescu RB, Rouhani F, Popp C, et al. EUS-guided fine needle biopsy is able to provide diagnosis in rare osteoclast-like giant cells undifferentiated carcinoma of the pancreas: report of two cases. Rom J Intern Med 2023;61:116-124.
  29. Molberg KH, Heffess C, Delgado R, Albores-Saavedra J. Undifferentiated carcinoma with osteoclast-like giant cells of the pancreas and periampullary region. Cancer 1998;82:1279-1287.
  30. Amin MB, Greene FL, Edge SB, Compton CC, Gershenwald JE, Brookland RK, et al. The Eighth Edition AJCC Cancer Staging Manual: continuing to build a bridge from a population-based to a more 'personalized' approach to cancer staging. CA Cancer J Clin 2017;67:93-99.
  31. Mattiolo P, Fiadone G, Paolino G, Chatterjee D, Bernasconi R, Piccoli P, et al. Epithelial-mesenchymal transition in undifferentiated carcinoma of the pancreas with and without osteoclast-like giant cells. Virchows Arch 2021;478:319-326.
  32. Maier HC, Sommers SC. Recurrent and metastatic pulmonary fibrous histiocytoma/plasma cell granuloma in a child. Cancer 1987;60:1073-1076.
  33. Jo S. Huge undifferentiated carcinoma of the pancreas with osteoclast- like giant cells. World J Gastroenterol 2014;20:2725-2730.
  34. Sakhi R, Hamza A, Khurram MS, Ibrar W, Mazzara P. Undifferentiated carcinoma of the pancreas with osteoclast-like giant cells reported in an asymptomatic patient: a rare case and literature review. Autops Case Rep 2017;7:51-57.
  35. Luchini C, Pea A, Lionheart G, Mafficini A, Nottegar A, Veronese N, et al. Pancreatic undifferentiated carcinoma with osteoclast-like giant cells is genetically similar to, but clinically distinct from, conventional ductal adenocarcinoma. J Pathol 2017;243:148-154.
  36. Matissek SJ, Elsawa SF. GLI3: a mediator of genetic diseases, development and cancer. Cell Commun Signal 2020;18:54.
  37. Yonemasu H, Takashima M, Nishiyama KI, Ueki T, Yao T, Tanaka M, et al. Phenotypical characteristics of undifferentiated carcinoma of the pancreas: a comparison with pancreatic ductal adenocarcinoma and relevance of E-cadherin, alpha catenin and beta catenin expression. Oncol Rep 2001;8:745-752.
  38. Sano M, Homma T, Hayashi E, Noda H, Amano Y, Tsujimura R, et al. Clinicopathological characteristics of anaplastic carcinoma of the pancreas with rhabdoid features. Virchows Arch 2014;465:531-538.
  39. Naito Y, Kinoshita H, Okabe Y, Arikawa S, Higaki K, Morimitsu Y, et al. Pathomorphologic study of undifferentiated carcinoma in seven cases: relationship between tumor and pancreatic duct epithelium. J Hepatobiliary Pancreat Surg 2009;16:478-484.
  40. Kubota N, Naito Y, Kawahara A, Taira T, Yamaguchi T, Yoshida T, et al. Granulocyte colony-stimulating factor-producing pancreatic anaplastic carcinoma in ascitic fluid at initial diagnosis: a case report. Diagn Cytopathol 2017;45:463-467.
  41. Togawa Y, Tonouchi A, Chiku T, Sano W, Doki T, Yano K, et al. A case report of undifferentiated carcinoma with osteoclast-like giant cells of the pancreas and literature review. Clin J Gastroenterol 2010;3:195-203.
  42. Fukukura Y, Kumagae Y, Hirahara M, Hakamada H, Nagano H, Nakajo M, et al. CT and MRI features of undifferentiated carcinomas with osteoclast-like giant cells of the pancreas: a case series. Abdom Radiol (NY) 2019;44:1246-1255.
  43. Shindoh N, Ozaki Y, Kyogoku S, Nakanishi A, Sumi Y, Katayama H. Osteoclast-type giant cell tumor of the pancreas: helical CT scans. AJR Am J Roentgenol 1998;170:653-654.
  44. Yang KY, Choi JI, Choi MH, Park MY, Rha SE, Byun JY, et al. Magnetic resonance imaging findings of undifferentiated carcinoma with osteoclast-like giant cells of pancreas. Clinical Imaging 2015;40:148-151.
  45. Brosens LA, Leguit RJ, Vleggaar FP, Veldhuis WB, van Leeuwen MS, Offerhaus GJA. EUS-guided FNA cytology diagnosis of paraduodenal pancreatitis (groove pancreatitis) with numerous giant cells: conservative management allowed by cytological and radiological correlation. Cytopathology 2015;26:122125.
  46. Luchini C. Undifferentiated carcinoma of the pancreas with osteoclast-like giant cells: a challenging cancer with new horizons? Virchows Archiv 2021;478:595-596.
  47. Manduch M, Dexter DF, Jalink DW, Vanner SJ, Hurlbut DJ. Undifferentiated pancreatic carcinoma with osteoclast-like giant cells: report of a case with osteochondroid differentiation. Pathol Res Pract 2009;205:353-359.
  48. Oymaci E, Yakan S, Yildirim M, Argon A, Namdaroglu O. Anaplastic carcinoma of the pancreas: a rare clinical entity. Cureus 2017;9:e1782.
  49. Ren B, Liu X, Suriawinata AA. Pancreatic ductal adenocarcinoma and its precursor lesions: histopathology, cytopathology, and molecular pathology. Am J Pathol 2019;189:9-21.
  50. Jang KT, Park SM, Basturk O, Bagci P, Bandyopadhyay S, Stelow EB, et al. Clinicopathologic characteristics of 29 invasive carcinomas arising in 178 pancreatic mucinous cystic neoplasms with ovarian-type stroma: implications for management and prognosis. Am J Surg Pathol 2015;39:179-187.
  51. Shiozawa M, Imada T, Ishiwa N, Rino Y, Hasuo K, Takanashi Y, et al. Osteoclast-like giant cell tumor of the pancreas. Int J Clin Oncol 2002;7:376-380.
  52. Strobel O, Hartwig W, Bergmann F, Hinz U, Hackert T, Grenacher L, et al. Anaplastic pancreatic cancer: presentation, surgical management, and outcome. Surgery 2011;149:200-208.
  53. Xu M, Chen W, Wang D, Nie M. Clinical characteristics and prognosis of osteoclast-like giant cell tumors of the pancreas compared with pancreatic adenocarcinomas: a population-based study. Med Sci Monit 2020;26:e922585.
  54. Hrudka J, Lawrie K, Waldauf P, Ciprova V, Moravcova J, Matej R. Negative prognostic impact of PD-L1 expression in tumor cells of undifferentiated (anaplastic) carcinoma with osteoclast-like giant cells of the pancreas: study of 13 cases comparing ductal pancreatic carcinoma and review of the literature. Virchows Arch 2020;477:687-696.