Top

Published in:

Open Access 11-01-2022 | Original Paper

Reappraisal of Grading in Intestinal-Type Sinonasal Adenocarcinoma: Tumor Budding as an Independent Prognostic Parameter

Authors: Christian M. Meerwein, Muriel D. Brada, Michael B. Soyka, David Holzmann, Niels J. Rupp

Published in: Head and Neck Pathology | Issue 3/2022

Abstract

Since sinonasal intestinal-type adenocarcinomas (ITAC) show resemblance to colorectal adenocarcinomas, we aimed to investigate novel prognostic factors of outcome, with particular focus on the role of tumor budding (TB). Retrospective clinico-pathological single-institution study on consecutive ITAC patients between 1996 and 2020. Histopathological parameters including conventional subtypes and TB features (low, intermediate, high) were evaluated with the aid of pancytokeratin (AE1/AE3) immunohistochemical staining. Parameters were correlated to clinical data and outcome. A total of 31 ITAC patients were included. Overall, 19/31 patients (61.3%) presented with stage III/IV disease. Presence of lymph node or distant metastases was rare (1/31 patient, 3.2%). Treatment protocols consisted of tumor resection in 30/31 patients (96.8%) and primary radiochemotherapy in 1/31 patient (3.2%). Adjuvant radiation therapy was conducted in 20/30 surgically treated patients (66.7%). The 3- and 5-year overall survival (OS) was 83.9% and 78.3% and the 3- and 5-years disease-specific survival (DSS) 83.7% % and 78.5%, respectively. The presence of intermediate/high TB (defined as ≥ 5 buds) was associated with both, worse DSS (log rank p = 0.03) and OS (log rank p = 0.006). No patient with low TB revealed progressive disease or died of the disease. No association between TB and tumor stage or conventional tumor subtype was found. Tumor budding seems to be an independent prognostic factor of worse outcome in ITAC.

Hoeben A, van de Winkel L, Hoebers F, Kross K, Driessen C, Slootweg P, et al. Intestinal-type sinonasal adenocarcinomas: the road to molecular diagnosis and personalized treatment. Head Neck. 2016;38(10):1564–70.PubMedCrossRef

Tripodi D, Quéméner S, Renaudin K, Ferron C, Malard O, Guisle-Marsollier I, et al. Gene expression profiling in sinonasal adenocarcinoma. BMC Med Genomics. 2009;2(1):1–12.CrossRef

Kılıç S, Samarrai R, Kılıç SS, Mikhael M, Baredes S, Eloy JA. Incidence and survival of sinonasal adenocarcinoma by site and histologic subtype*. Acta Otolaryngol. 2018;138(4):415–21.PubMedCrossRef

Binazzi A, Ferrante P, Marinaccio A. Occupational exposure and sinonasal cancer: a systematic review and meta-analysis. BMC Cancer. 2015;15(1):1–7.CrossRef

Binazzi A, Corfiati M, Di Marzio D, Cacciatore AM, Zajacovà J, Mensi C, et al. Sinonasal cancer in the Italian national surveillance system: epidemiology, occupation, and public health implications. Am J Ind Med. 2018;61(3):239–50.PubMedCrossRef

Cantu G, Solero CL, Mariani L, Lo Vullo S, Riccio S, Colombo S, et al. Intestinal type adenocarcinoma of the ethmoid sinus in wood and leather workers: a retrospective study of 153 cases. Head Neck. 2011;33(4):535–42.PubMedCrossRef

Rampinelli V, Ferrari M, Nicolai P. Intestinal-type adenocarcinoma of the sinonasal tract: an update. Curr Opin Otolaryngol Head Neck Surg. 2018;26(2):115–21.PubMedCrossRef

Andersson M, Selin F, Järvholm B. Asbestos exposure and the risk of sinonasal cancer. Occup Med (Chic Ill). 2016;66(4):326–31.CrossRef

Van Gerven L, Jorissen M, Nuyts S, Hermans R, Vander PV. Long-term follow-up of 44 patients with adenocarcinoma of the nasal cavity and sinuses primarily treated with endoscopic resection followed by radiotherapy. Head Neck. 2011;33(6):898–904.PubMedCrossRef

10.

Jankowski R, Georgel T, Vignaud JM, Hemmaoui B, Toussaint B, Graff P, et al. Endoscopic surgery reveals that woodworkers’ adenocarcinomas originate in the olfactory cleft. Rhinology. 2007;45(4):308.PubMed

11.

Camp S, Van Gerven L, Poorten Vander V, Nuyts S, Hermans R, Hauben E, et al. Long-term follow-up of 123 patients with adenocarcinoma of the sinonasal tract treated with endoscopic resection and postoperative radiation therapy. Head Neck. 2016;38(S1):E996–1003.

12.

Nicolai P, Schreiber A, Bolzoni Villaret A, Lombardi D, Morassi L, Raffetti E, et al. Intestinal type adenocarcinoma of the ethmoid: outcomes of a treatment regimen based on endoscopic surgery with or without radiotherapy. Head Neck. 2016;38:E996–1003.PubMedCrossRef

13.

Grigore A, Jolly M, Jia D, Farach-Carson M, Levine H. Tumor budding: the name is EMT. Partial EMT J Clin Med. 2016;5(5):51.CrossRef

14.

Choussy O, Ferron C, Védrine PO, Toussaint B, Liétin B, Marandas P, et al. Role of radiotherapy in the treatment of nasoethmoidal adenocarcinoma. Arch Otolaryngol Head Neck Surg. 2010;136(2):143–6.PubMedCrossRef

15.

Almangush A, Pirinen M, Heikkinen I, Mäkitie AA, Salo T, Leivo I. Tumour budding in oral squamous cell carcinoma: a meta-analysis. Br J Cancer. 2018;118(4):577–86.PubMedCrossRef

16.

Karamitopoulou E, Zlobec I, Born D, Kondi-Pafiti A, Lykoudis P, Mellou A, et al. Tumour budding is a strong and independent prognostic factor in pancreatic cancer. Eur J Cancer. 2013;49(5):1032–9.PubMedCrossRef

17.

Mäkitie AA, Almangush A, Rodrigo JP, Ferlito A, Leivo I. Hallmarks of cancer: Tumor budding as a sign of invasion and metastasis in head and neck cancer. Head Neck. 2019;41(10):3712–8.PubMedCrossRef

18.

Cappellesso R, Luchini C, Veronese N, Lo Mele M, Rosa-Rizzotto E, Guido E, et al. Tumor budding as a risk factor for nodal metastasis in pT1 colorectal cancers: a meta-analysis. Hum Pathol. 2017;65:62–70.PubMedCrossRef

19.

Petrelli F, Pezzica E, Cabiddu M, Coinu A, Borgonovo K, Ghilardi M, et al. Tumour budding and survival in Stage II colorectal cancer: a systematic review and pooled analysis. J Gastrointest Cancer. 2015;46(3):212–8.PubMedCrossRef

20.

Maffeis V, Nicolè L, Cappellesso R. RAS, Cellular plasticity, and tumor budding in colorectal cancer. Front Oncol. 2019;49(1):183–200.

21.

Maffeis V, Cappellesso R, Galuppini F, Guzzardo V, Zanon A, Cazzador D, et al. Tumor budding is an adverse prognostic marker in intestinal-type sinonasal adenocarcinoma and seems to be unrelated to epithelial-mesenchymal transition. Virchows Arch. 2020;477(2):241–8.PubMedCrossRef

22.

Franchi A, Innocenti DRD, Palomba A, Miligi L, Paiar F, Franzese C, et al. Low prevalence of K-RAS, EGF-R and BRAF mutations in sinonasal adenocarcinomas. Implications for anti-EGFR treatments. Pathol Oncol Res. 2014;20(3):571–9.PubMedCrossRef

23.

Franchi A, Massi D, Palomba A, Biancalani M, Santucci M. CDX-2, cytokeratin 7 and cytokeratin 20 immunohistochemical expression in the differential diagnosis of primary adenocarcinomas of the sinonasal tract. Virchows Arch. 2004;445(1):63–7.PubMed

24.

Meerwein CM, Pazahr S, Soyka MB, Hüllner MW, Holzmann D. Diagnostic accuracy of computed tomography and magnetic resonance imaging compared to surgical exploration for anterior skull base and medial orbital wall infiltration in advanced sinonasal tumors. Head Neck. 2020;42(8):2002–12.PubMedCrossRef

25.

Castelnuovo P, Turri-Zanoni M, Battaglia P, Antognoni P, Bossi P, Locatelli D. Sinonasal malignancies of anterior skull base: histology-driven treatment strategies. Otolaryngol Clin N Am. 2016;49(1):183–200.CrossRef

26.

Meerwein CM, Pangalu A, Pazahr S, Epprecht L, Soyka MB, Holzmann D. The Zurich magnetic resonance imaging protocol for standardized staging and restaging of sinonasal tumours*. Rhinol Online. 2021;4:161–4.CrossRef

27.

Barnes L. Intestinal-type adenocarcinoma of the nasal cavity and paranasal sinuses. Am J Surg Pathol. 1986;10(3):192–202.PubMedCrossRef

28.

Lugli A, Kirsch R, Ajioka Y, Bosman F, Cathomas G, Dawson H, et al. Recommendations for reporting tumor budding in colorectal cancer based on the International Tumor Budding Consensus Conference (ITBCC) 2016. Mod Pathol. 2017;30(9):1299–311.PubMedCrossRef

29.

Kennedy MT, Jordan RCK, Berean KW, Perez-Ordoñez B. Expression pattern of CK7, CK20, CDX-2, and villin in intestinal-type sinonasal adenocarcinoma. J Clin Pathol. 2004;57(9):932–7.PubMedPubMedCentralCrossRef

30.

Cathro HP, Mills SE. Immunophenotypic differences between intestinal-type and low-grade papillary sinonasal adenocarcinomas: an immunohistochemical study of 22 cases utilizing CDX2 and MUC2. Am J Surg Pathol. 2004;28(8):1026–32.PubMedCrossRef

31.

D’Aguillo CM, Kanumuri VV, Khan MN, Sanghvi S, Patel NR, Baredes S, et al. Demographics and survival trends of sinonasal adenocarcinoma from 1973 to 2009. Int Forum Allergy Rhinol. 2014;4(9):771–6.PubMedCrossRef

32.

Vergez S, Du Mayne MD, Coste A, Gallet P, Jankowski R, Dufour X, et al. Multicenter study to assess endoscopic resection of 159 sinonasal adenocarcinomas. Ann Surg Oncol. 2014;21(4):1384–90.PubMedCrossRef

33.

Bogaerts S, Poorten Vander V, Nuyts S, Van Den Bogaert W, Jorisser M. Results of endoscopic resection followed by radiotherapy for primarily diagnosed adenocarcinomas of the paranasal sinuses. Head Neck. 2008;30(6):728–36.PubMedCrossRef

34.

Parasher AK, Kuan EC, John MAS, Tajudeen BA, Adappa ND. What is the appropriate timing for endoscopic and radiographic surveillance following treatment for sinonasal malignancies? Laryngoscope. 2018;12(8):1511–2.CrossRef

35.

Donhuijsen K, Kollecker I, Petersen P, Gaßler N, Schulze J, Schroeder HG. Metastatic behaviour of sinonasal adenocarcinomas of the intestinal type (ITAC). Eur Arch Oto-Rhino-Laryngology. 2016;273(3):649–54.CrossRef

36.

Meerwein CM, Balermpas P, Vital DG, Broglie MA, Soyka MB, Holzmann D. The role of regional disease and patterns of treatment failure in primary sinonasal malignancies. Am J Rhinol Allergy. 2021;36(1):157–66.PubMedCrossRef

37.

Meccariello G, Deganello A, Choussy O, Gallo O, Vitali D, De Raucourt D, et al. Endoscopic nasal versus open approach for the management of sinonasal adenocarcinoma: a pooled-analysis of 1826 patients. Head Neck. 2016;38(S1):E2267–74.PubMedCrossRef

38.

Turri-Zanoni M, Battaglia P, Lambertoni A, Giovannardi M, Schreiber A, Volpi L, et al. Treatment strategies for primary early-stage sinonasal adenocarcinoma: a retrospective bi-institutional case-control study. J Surg Oncol. 2015;112(5):561–7.PubMedCrossRef

39.

Gallet P, Nguyen DT, Russel A, Jankowski R, Vigouroux C, Rumeau C. Intestinal and non-intestinal nasal cavity adenocarcinoma: Impact of wood dust exposure. Eur Ann Otorhinolaryngol Head Neck Dis. 2018;135(6):383–7.PubMedCrossRef

40.

Skalova A, Sar A, Laco J, Metelkova A, Miesbauerova M, Steiner P, et al. The role of SATB2 as a diagnostic marker of sinonasal intestinal-type adenocarcinoma. Appl Immunohistochem Mol Morphol. 2018;26(2):140–6.PubMedCrossRef

41.

Berg KB, Schaeffer DF. SATB2 as an immunohistochemical marker for colorectal adenocarcinoma a concise review of benefits and pitfalls. Arch Pathol Lab Med. 2017;141(10):1428–33.PubMedCrossRef

42.

WHO Classification of Tumours Editorial Board. Digestive System Tumours (WHO classification of tumours series, 5th edition, vol. 1). Lyon (France): International Agency for Research on Cancer. 2019.

43.

Dawson H, Galuppini F, Träger P, Berger MD, Studer P, Brügger L, et al. Validation of the International Tumor Budding Consensus Conference 2016 recommendations on tumor budding in stage I-IV colorectal cancer. Hum Pathol. 2019;85:145–51.PubMedCrossRef

44.

Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest. 2009;120(5):1786.CrossRef

45.

Koelzer VH, Assarzadegan N, Dawson H, Mitrovic B, Grin A, Messenger DE, et al. Cytokeratin-based assessment of tumour budding in colorectal cancer: analysis in stage II patients and prospective diagnostic experience. J Pathol Clin Res. 2017;3(3):171–8.PubMedPubMedCentralCrossRef

46.

Perez-Ordonez B, Huynh NN, Berean KW, Jordan RCK. Expression of mismatch repair proteins, β catenin, and E cadherin in intestinal-type sinonasal adenocarcinoma. J Clin Pathol. 2004;57(10):1080–3.PubMedPubMedCentralCrossRef

Title: Reappraisal of Grading in Intestinal-Type Sinonasal Adenocarcinoma: Tumor Budding as an Independent Prognostic Parameter
Authors: Christian M. Meerwein
Muriel D. Brada
Michael B. Soyka
David Holzmann
Niels J. Rupp
Publication date: 11-01-2022
Publisher: Springer US
Published in: Head and Neck Pathology / Issue 3/2022
Electronic ISSN: 1936-0568
DOI: https://doi.org/10.1007/s12105-022-01410-3

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Reappraisal of Grading in Intestinal-Type Sinonasal Adenocarcinoma: Tumor Budding as an Independent Prognostic Parameter

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3/2022

A Rare Case of Peripheral Compound Odontoma and Review of the Literature

Clear Cell Odontogenic Carcinoma a Systematic Review

Unclassified Neuroendocrine Tumor with a Novel CHD4::AFF2 Fusion: Expanding the Family of AFF2-Rearranged Head and Neck Malignancies

NUT Carcinoma of the Submandibular Gland: A Case at This Uncommon Site with Review of the Literature

Oncocytoid Variant of High-Grade Salivary Duct Carcinoma: A Potential Diagnostic Pitfall. A Report on Two Patients

Squamoglandular Variant of Acinic Cell Carcinoma: A Case Report of a Novel Variant