Two distinct pathogenic pathways of digital papillary adenocarcinoma - BRAF mutation or low-risk HPV infection.
digital papillary adenocarcinoma
extensive squamoid differentation
low-grade HPV infection
wild-type BRAF
Journal
Journal of cutaneous pathology
ISSN: 1600-0560
Titre abrégé: J Cutan Pathol
Pays: United States
ID NLM: 0425124
Informations de publication
Date de publication:
Jun 2023
Jun 2023
Historique:
revised:
15
12
2022
received:
17
08
2022
accepted:
03
01
2023
medline:
17
5
2023
pubmed:
10
2
2023
entrez:
9
2
2023
Statut:
ppublish
Résumé
Digital papillary adenocarcinoma (DPA) is a rare neoplasm that can exhibit local recurrence and distant metastasis. We present a series of eight cases of DPA showing two distinct clinical presentations, morphologies, immunophenotypes, and molecular features. Four cases were characterized by painless, slow-growing nodules located on the digits. The lesions were small, well-defined, and confined in the dermis. Histopathologically, these tumors were composed of glandular structures lined by cuboidal epithelium with luminal papillary infoldings. Only rare mitotic figures and minimal squamoid differentiation were present, and cellular necrosis was absent. All four cases were positive for the BRAF V600E immunohistochemistry but negative for p16, low-risk and high-risk HPV in situ hybridization (ISH). In contrast, the remaining four cases were characterized by painful, rapidly growing masses on the digits. These four lesions were located in the deep dermis and consisted of a solid, tightly packed papillary architecture lined by atypical epithelioid cells with inconspicuous nucleoli. Cellular necrosis, numerous mitotic figures, and prominent squamoid differentiation were seen. All cases were negative for the BRAF V600E IHC. However, they showed strong, patchy to diffuse reactivity for p16 and were positive for low-risk HPV ISH and negative for high-risk HPV ISH. Our findings suggest that the current classification of DPA encompasses tumors that show two discrete pathogenic pathways - BRAF mutation or low-risk HPV infection. DPAs with low-risk HPV infection exhibit aggressive clinical features, high-grade morphology, marked squamoid differentiation, and wild-type BRAF. DPAs with BRAF V600E have less aggressive clinical features, low-grade morphologic findings, mild to absent squamoid differentiation, and negative HPV infection.
Substances chimiques
Proto-Oncogene Proteins B-raf
EC 2.7.11.1
BRAF protein, human
EC 2.7.11.1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
568-576Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2023 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Références
Suchak R, Wang WL, Prieto VG, et al. Cutaneous digital papillary adenocarcinoma: a clinicopathologic study of 31 cases of a rare neoplasm with new observations. Am J Surg Pathol. 2012;36(12):1883-1891. doi:10.1097/PAS.0b013e31826320ec
Hsu HC, Ho CY, Chen CH, Yang CH, Hong HS, Chuang YH. Aggressive digital papillary adenocarcinoma: a review. Clin Exp Dermatol. 2010;35(2):113-119. doi:10.1111/j.1365-2230.2009.03490.x
Altmann S, Damert HG, Klausenitz S, Infanger M, Kraus A. Aggressive digital papillary adenocarcinoma - a rare malignant tumor of the sweat glands: two case reports and a review of the literature. Clin Cosmet Investig Dermatol. 2015;8:143-146. doi:10.2147/CCID.S71323
Kao GF, Helwig EB, Graham JH. Aggressive digital papillary adenoma and adenocarcinoma. A clinicopathological study of 57 patients, with histochemical, immunopathological, and ultrastructural observations. J Cutan Pathol. 1987;14(3):129-146.
Gole G, Tati S, Deshpande A, Gole S. Aggressive digital papillary adenocarcinoma in a young female-a rare presentation. J Hand Microsurg. 2016;3(1):31-33. doi:10.1007/s12593-010-0028-1
Frey J, Shimek C, Woodmansee C, et al. Aggressive digital papillary adenocarcinoma: a report of two diseases and review of the literature. J Am Acad Dermatol. 2009;60(2):331-339. doi:10.1016/j.jaad.2008.07.038
Dhillon P, Powell B, Mehdi S. Aggressive digital papillary adenocarcinoma and sentinel node biopsy: a case report and literature review. JPRAS Open. 2020;24:43-46. doi:10.1016/j.jpra.2020.03.001
Yokota K, Kono M, Shimizu K, Sakakibara A, Akiyama M. Highly variable clinical feature and course of aggressive digital papillary adenocarcinoma. J Dermatol. 2018;45(3):357-360. doi:10.1111/1346-8138.14159
Chi CC, Kuo TT, Wang SH. Aggressive digital papillary adenocarcinoma: a silent malignancy masquerading as acquired digital fibrokeratoma. Am J Clin Dermatol. 2007;8(4):243-245. doi:10.2165/00128071-200708040-00007
Duke WH, Sherrod TT, Lupton GP. Aggressive digital papillary adenocarcinoma (aggressive digital papillary adenoma and adenocarcinoma revisited). Am J Surg Pathol. 2000;24(6):775-784. doi:10.1097/00000478-200006000-00002
Laun J, Gopman J, Barnes CW, Segars KA, Elston JB, Stone J. Aggressive digital papillary adenocarcinoma. Eplasty. 2015;15:ic60.
Jones JA, Patel VB, Goldsmith B, Teitelbaum U, Plastaras JP. Diffusely metastatic digital papillary adenocarcinoma 11 years after initial presentation treated with palliative chemotherapy and radiotherapy. J Clin Oncol. 2013;31(22):e386-e389. doi:10.1200/JCO.2012.46.4693
Knackstedt RW, Knackstedt TJ, Findley AB, et al. Aggressive digital papillary adenocarcinoma: treatment with Mohs micrographic surgery and an update of the literature. Int J Dermatol. 2017;56(10):1061-1064. doi:10.1111/ijd.13712
Storino A, Drews RE, Tawa NE. Malignant cutaneous adnexal tumors and role of SLNB. J Am Coll Surg. 2021;232:889-898. doi:10.1016/j.jamcollsurg.2021.01.019
Dias-Santagata D, Lam Q, Bergethon K, et al. A potential role for targeted therapy in a subset of metastasizing adnexal carcinomas. Mod Pathol. 2011;24(7):974-982. doi:10.1038/modpathol.2011.48
Surowy HM, Giesen AK, Otte J, et al. Gene expression profiling in aggressive digital papillary adenocarcinoma sheds light on the architecture of a rare sweat gland carcinoma. Br J Dermatol. 2019;180(5):1150-1160. doi:10.1111/bjd.17446
Bell D, Aung P, Prieto VG, Ivan D. Next-generation sequencing reveals rare genomic alterations in aggressive digital papillary adenocarcinoma. Ann Diagn Pathol. 2015;19(6):381-384. doi:10.1016/j.anndiagpath.2015.08.002
Trager MH, Jurkiewicz M, Khan S, Niedt GW, Geskin LJ, Carvajal RD. A case report of papillary digital adenocarcinoma with BRAFV600E mutation and quantified mutational burden. Am J Dermatopathol. 2021;43(1):57-59. doi:10.1097/DAD.0000000000001694
Vanderbilt C, Brenn T, Moy AP, et al. Association of HPV42 with digital papillary adenocarcinoma and the use of in situ hybridization for its distinction from acral hidradenoma and diagnosis at non-acral sites. Mod Pathol. 2022;35:1405-1410. doi:10.1038/s41379-022-01094-8
Heiwig EB. Eccrine acrospiroma. J Cutan Pathol. 1984;11(5):415-420. doi:10.1111/j.1600-0560.1984.tb00398.x
Rogers MA, Edler L, Winter H, Langbein L, Beckmann I, Schweizer J. Characterization of new members of the human type II keratin gene family and a general evaluation of the keratin gene domain on chromosome 12q13.13. J Invest Dermatol. 2005;124(3):536-544. doi:10.1111/j.0022-202X.2004.23530.x
Langbein L, Reichelt J, Eckhart L, et al. New facets of keratin K77: interspecies variations of expression and different intracellular location in embryonic and adult skin of humans and mice. Cell Tissue Res. 2013;354(3):793-812. doi:10.1007/s00441-013-1716-5
Rütten A, Requena L. Sweat gland carcinomas of the skin. Hautarzt. 2008;59(2):151-160.
Weedon D. Skin pathology: tumor of cutaneous appendages. In: Weedon D, ed. Skin Pathology. 2nd ed. James W. Patterson; 2020:34-1008.
Weingertner N, Gressel A, Battistella M, Cribier B. Aggressive digital papillary adenocarcinoma: a clinicopathological study of 19 cases. J Am Acad Dermatol. 2017;77(3):549-558.e1. doi:10.1016/j.jaad.2017.02.028
Scolyer RA, Karim RZ, Thompson JF, Stretch JR, McCarthy SW, Murali R. Digital papillary adenocarcinoma: a tumour that should be considered in the differential diagnosis of neoplasms involving the digits. Pathology. 2013;45(1):55-61. doi:10.1097/PAT.0b013e32835af778
Hsu PJ, Liu CH, Huang CJ, Printed BM, Denmark I. Mixed tubulopapillary hidradenoma and syringocystadenoma papilliferum occurring as a verrucous tumor case report. J Cutan Pathol. 2003;30:206-210.
Cardoso JC, Calonje E. Malignant sweat gland tumours: an update. Histopathology. 2015;67(5):589-606. doi:10.1111/his.12767
Wiedemeyer K, Gill P, Schneider M, Kind P, Brenn T. Clinicopathologic characterization of hidradenoma on acral sites: a diagnostic pitfall with digital papillary adenocarcinoma. Am J Surg Pathol. 2020;44(5):711-717. doi:10.1097/PAS.0000000000001426
Tingaud C, Costes V, Frouin E, et al. Lymph node location of a clear cell hidradenoma: report of a patient and review of literature. J Cutan Pathol. 2016;43(8):702-706. doi:10.1111/cup.12720
Winnes M, Mölne L, Suurküla M, et al. Frequent fusion of the CRTC1 and MAML2 genes in clear cell variants of cutaneous hidradenomas. Genes Chromosomes Cancer. 2007;46(6):559-563. doi:10.1002/gcc.20440
Kuma Y, Yamada Y, Yamamoto H, et al. A novel fusion gene CRTC3-MAML2 in hidradenoma: histopathological significance. Hum Pathol. 2017;70:55-61. doi:10.1016/j.humpath.2017.10.004
Winnes M, Mölne L, Suurküla M, et al. Frequent fusion of the CRTCI and MAML2 genes in clear cell variants of cutaneous hidradenomas. Genes Chromosomes Cancer. 2007;46(6):559-563. doi:10.1002/gcc.20440
Behboudi A, Winnes M, Gorunova L, et al. Clear cell hidradenoma of the skin-a third tumor type with a t(11;19)-associated TORC1-MAML2 gene fusion. Genes Chromosomes Cancer. 2005;43(2):202-205. doi:10.1002/gcc.20168
Blasini W, Hu S, Gugic D, Vincek V. Papillary eccrine adenoma in association with cutaneous horn. Am J Clin Dermatol. 2007;8(3):179-182. doi:10.2165/00128071-200708030-00005
Płachta I, Kleibert M, Czarnecka AM, Spałek M, Szumera-Ciećkiewicz A, Rutkowski P. Current diagnosis and treatment options for cutaneous adnexal neoplasms with apocrine and eccrine differentiation. Int J Mol Sci. 2021;22(10):5077. doi:10.3390/ijms22105077
Kurtz DH, Finnell JA, Mehler AS. Papillary eccrine adenoma of the heel: a case report. J Foot Ankle Surg. 2000;39(4):249-252. doi:10.1016/S1067-2516(00)80008-3
Liau JY, Tsai JH, Huang WC, Lan J, Hong JB, Yuan CT. BRAF and KRAS mutations in tubular apocrine adenoma and papillary eccrine adenoma of the skin. Hum Pathol. 2018;73:59-65. doi:10.1016/j.humpath.2017.12.002
Galadari E, Mehregan AH, Lee KC. Malignant transformation of eccrine tumors. J Cutan Pathol. 1987;14(1):15-22. doi:10.1111/j.1600-0560.1987.tb00122.x
Chen S, Asgari M. Papillary adenocarcinoma in situ of the skin: report of four cases. Dermatol Pract Concept. 2014;30:23-28. doi:10.5826/dpc.0402a04
Broekaert SMC, Roy R, Okamoto I, et al. Genetic and morphologic features for melanoma classification. Pigment Cell Melanoma Res. 2010;23(6):763-770. doi:10.1111/j.1755-148X.2010.00778.x
Teixido C, Castillo P, Martinez-Vila C, Arance A, Alos L. Molecular markers and targets in melanoma. Cell. 2021;10(9):2320. doi:10.3390/cells10092320
Cohen DN, Lawson SK, Shaver AC, et al. Contribution of beta-HPV infection and UV damage to rapid-onset cutaneous squamous cell carcinoma during BRAF-inhibition therapy. Clin Cancer Res. 2015;21(11):2624-2634. doi:10.1158/1078-0432.CCR-14-2667
Guimerà N, Lloveras B, Lindeman J, et al. The occasional role of low-risk human papillomaviruses 6, 11, 42, 44, and 70 in anogenital carcinoma defined by laser capture microdissection/PCR methodology: results from a global study. Am J Surg Pathol. 2013;37(9):1299-1310. doi:10.1097/PAS.0b013e31828b6be4
Otter S, Whitaker S, Chatterjee J, Stewart A. The human papillomavirus as a common pathogen in oropharyngeal, anal and cervical cancers. Clin Oncol. 2019;31(2):81-90. doi:10.1016/j.clon.2018.10.004
Cacheux W, Rouleau E, Briaux A, et al. Mutational analysis of anal cancers demonstrates frequent PIK3CA mutations associated with poor outcome after salvage abdominoperineal resection. Br J Cancer. 2016;114(12):1387-1394. doi:10.1038/bjc.2016.144
Armstrong SA, Malley R, Wang H, et al. Molecular characterization of squamous cell carcinoma of the anal canal. J Gastrointest Oncol. 2021;12(5):2423-2437. doi:10.21037/jgo-20-610