Salivary gland polymorphous adenocarcinoma: Clinicopathological features and gene alterations in 36 Japanese patients
Background Polymorphous adenocarcinoma is a common intraoral minor salivary gland carcinoma in Western countries but is extremely rare in Japan. The current study aimed to characterize the clinicopathological features and status of molecular alterations of polymorphous adenocarcinoma‐associated gene...
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| Veröffentlicht in: | Journal of oral pathology & medicine 2022-09, Vol.51 (8), p.710-720 |
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| creator | Fukumura, Masahiro Ishibashi, Kenichiro Nakaguro, Masato Nagao, Toshitaka Saida, Kosuke Urano, Makoto Tanigawa, Maki Hirai, Hideaki Yagyuu, Takahiro Kikuchi, Kentaro Yada, Naomi Sugita, Yoshihiko Miyabe, Megumi Hasegawa, Shogo Goto, Mitsuo Yamamoto, Hidetaka Ohuchi, Tomoyuki Kusafuka, Kimihide Ogawa, Ikuko Suzuki, Hiroaki Notohara, Kenji Shimoda, Masayuki Tada, Yuichiro Kirita, Tadaaki Takata, Takashi Morinaga, Shojiroh Maeda, Hatsuhiko Warnakulasuriya, Saman Miyabe, Satoru Nagao, Toru |
| description | Background
Polymorphous adenocarcinoma is a common intraoral minor salivary gland carcinoma in Western countries but is extremely rare in Japan. The current study aimed to characterize the clinicopathological features and status of molecular alterations of polymorphous adenocarcinoma‐associated genes, such as PRKD1/2/3, ARID1A, and DDX3X, in a large cohort of Japanese patients with polymorphous adenocarcinoma.
Methods
We examined the cases of 36 Japanese patients with salivary gland polymorphous adenocarcinoma and 26 cases involving histopathological mimics. To detect gene splits, fluorescence in situ hybridization was carried out for polymorphous adenocarcinoma‐associated genes. Additionally, we applied a SNaPshot multiplex assay to identify PRKD1 hotspot mutations.
Results
This study revealed the indolent clinical course of polymorphous adenocarcinoma with a high 10‐year overall survival rate (92.9%), accompanied by occasional local recurrences and cervical lymph node metastasis (23.3%). Twenty cases (55.6%) of polymorphous adenocarcinoma (but none of the mimics) exhibited alterations in at least one polymorphous adenocarcinoma‐associated gene. Rearrangement of polymorphous adenocarcinoma‐associated genes and PRKD1 E710D were identified in 17 (47.2%) and 4 (11.1%) cases, respectively; one case showed coexisting PRKD3 split and PRKD1 E710D. In the multivariate analysis, high clinical stage (p = 0.0005), the presence of prominent nucleoli (p = 0.0003), and ARID1A split positivity (p = 0.004) were independent risk factors for disease‐free survival.
Conclusion
Japanese patients with polymorphous adenocarcinoma showed clinicopathological features similar to those reported in Western countries. This study disclosed that polymorphous adenocarcinoma‐associated genetic alterations were common and specific findings in polymorphous adenocarcinomas. The diagnostic role and possible prognostic significance of polymorphous adenocarcinoma‐associated genetic alterations in polymorphous adenocarcinomas were suggested. |
| doi_str_mv | 10.1111/jop.13336 |
| format | Article |
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Polymorphous adenocarcinoma is a common intraoral minor salivary gland carcinoma in Western countries but is extremely rare in Japan. The current study aimed to characterize the clinicopathological features and status of molecular alterations of polymorphous adenocarcinoma‐associated genes, such as PRKD1/2/3, ARID1A, and DDX3X, in a large cohort of Japanese patients with polymorphous adenocarcinoma.
Methods
We examined the cases of 36 Japanese patients with salivary gland polymorphous adenocarcinoma and 26 cases involving histopathological mimics. To detect gene splits, fluorescence in situ hybridization was carried out for polymorphous adenocarcinoma‐associated genes. Additionally, we applied a SNaPshot multiplex assay to identify PRKD1 hotspot mutations.
Results
This study revealed the indolent clinical course of polymorphous adenocarcinoma with a high 10‐year overall survival rate (92.9%), accompanied by occasional local recurrences and cervical lymph node metastasis (23.3%). Twenty cases (55.6%) of polymorphous adenocarcinoma (but none of the mimics) exhibited alterations in at least one polymorphous adenocarcinoma‐associated gene. Rearrangement of polymorphous adenocarcinoma‐associated genes and PRKD1 E710D were identified in 17 (47.2%) and 4 (11.1%) cases, respectively; one case showed coexisting PRKD3 split and PRKD1 E710D. In the multivariate analysis, high clinical stage (p = 0.0005), the presence of prominent nucleoli (p = 0.0003), and ARID1A split positivity (p = 0.004) were independent risk factors for disease‐free survival.
Conclusion
Japanese patients with polymorphous adenocarcinoma showed clinicopathological features similar to those reported in Western countries. This study disclosed that polymorphous adenocarcinoma‐associated genetic alterations were common and specific findings in polymorphous adenocarcinomas. The diagnostic role and possible prognostic significance of polymorphous adenocarcinoma‐associated genetic alterations in polymorphous adenocarcinomas were suggested.</description><identifier>ISSN: 0904-2512</identifier><identifier>EISSN: 1600-0714</identifier><identifier>DOI: 10.1111/jop.13336</identifier><language>eng</language><publisher>Copenhagen: Wiley Subscription Services, Inc</publisher><subject>Adenocarcinoma ; Cancer ; cribriform adenocarcinoma of salivary gland ; Exocrine glands ; Fluorescence in situ hybridization ; gene fusion ; Gene rearrangement ; Genes ; Lymph nodes ; Metastases ; Multivariate analysis ; Mutation hot spots ; Nucleoli ; Oral cancer ; Patients ; polymorphous adenocarcinoma ; prognosis ; Risk factors ; Salivary gland ; salivary gland neoplasms ; Survival</subject><ispartof>Journal of oral pathology & medicine, 2022-09, Vol.51 (8), p.710-720</ispartof><rights>2022 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd</rights><rights>2022 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3966-ea494fbc1e477c3f9760d39190de967a5f5369eb7eb784098d3235f053eaec9f3</citedby><cites>FETCH-LOGICAL-c3966-ea494fbc1e477c3f9760d39190de967a5f5369eb7eb784098d3235f053eaec9f3</cites><orcidid>0000-0003-3490-2371 ; 0000-0002-0902-6624</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fjop.13336$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fjop.13336$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids></links><search><creatorcontrib>Fukumura, Masahiro</creatorcontrib><creatorcontrib>Ishibashi, Kenichiro</creatorcontrib><creatorcontrib>Nakaguro, Masato</creatorcontrib><creatorcontrib>Nagao, Toshitaka</creatorcontrib><creatorcontrib>Saida, Kosuke</creatorcontrib><creatorcontrib>Urano, Makoto</creatorcontrib><creatorcontrib>Tanigawa, Maki</creatorcontrib><creatorcontrib>Hirai, Hideaki</creatorcontrib><creatorcontrib>Yagyuu, Takahiro</creatorcontrib><creatorcontrib>Kikuchi, Kentaro</creatorcontrib><creatorcontrib>Yada, Naomi</creatorcontrib><creatorcontrib>Sugita, Yoshihiko</creatorcontrib><creatorcontrib>Miyabe, Megumi</creatorcontrib><creatorcontrib>Hasegawa, Shogo</creatorcontrib><creatorcontrib>Goto, Mitsuo</creatorcontrib><creatorcontrib>Yamamoto, Hidetaka</creatorcontrib><creatorcontrib>Ohuchi, Tomoyuki</creatorcontrib><creatorcontrib>Kusafuka, Kimihide</creatorcontrib><creatorcontrib>Ogawa, Ikuko</creatorcontrib><creatorcontrib>Suzuki, Hiroaki</creatorcontrib><creatorcontrib>Notohara, Kenji</creatorcontrib><creatorcontrib>Shimoda, Masayuki</creatorcontrib><creatorcontrib>Tada, Yuichiro</creatorcontrib><creatorcontrib>Kirita, Tadaaki</creatorcontrib><creatorcontrib>Takata, Takashi</creatorcontrib><creatorcontrib>Morinaga, Shojiroh</creatorcontrib><creatorcontrib>Maeda, Hatsuhiko</creatorcontrib><creatorcontrib>Warnakulasuriya, Saman</creatorcontrib><creatorcontrib>Miyabe, Satoru</creatorcontrib><creatorcontrib>Nagao, Toru</creatorcontrib><title>Salivary gland polymorphous adenocarcinoma: Clinicopathological features and gene alterations in 36 Japanese patients</title><title>Journal of oral pathology & medicine</title><description>Background
Polymorphous adenocarcinoma is a common intraoral minor salivary gland carcinoma in Western countries but is extremely rare in Japan. The current study aimed to characterize the clinicopathological features and status of molecular alterations of polymorphous adenocarcinoma‐associated genes, such as PRKD1/2/3, ARID1A, and DDX3X, in a large cohort of Japanese patients with polymorphous adenocarcinoma.
Methods
We examined the cases of 36 Japanese patients with salivary gland polymorphous adenocarcinoma and 26 cases involving histopathological mimics. To detect gene splits, fluorescence in situ hybridization was carried out for polymorphous adenocarcinoma‐associated genes. Additionally, we applied a SNaPshot multiplex assay to identify PRKD1 hotspot mutations.
Results
This study revealed the indolent clinical course of polymorphous adenocarcinoma with a high 10‐year overall survival rate (92.9%), accompanied by occasional local recurrences and cervical lymph node metastasis (23.3%). Twenty cases (55.6%) of polymorphous adenocarcinoma (but none of the mimics) exhibited alterations in at least one polymorphous adenocarcinoma‐associated gene. Rearrangement of polymorphous adenocarcinoma‐associated genes and PRKD1 E710D were identified in 17 (47.2%) and 4 (11.1%) cases, respectively; one case showed coexisting PRKD3 split and PRKD1 E710D. In the multivariate analysis, high clinical stage (p = 0.0005), the presence of prominent nucleoli (p = 0.0003), and ARID1A split positivity (p = 0.004) were independent risk factors for disease‐free survival.
Conclusion
Japanese patients with polymorphous adenocarcinoma showed clinicopathological features similar to those reported in Western countries. This study disclosed that polymorphous adenocarcinoma‐associated genetic alterations were common and specific findings in polymorphous adenocarcinomas. The diagnostic role and possible prognostic significance of polymorphous adenocarcinoma‐associated genetic alterations in polymorphous adenocarcinomas were suggested.</description><subject>Adenocarcinoma</subject><subject>Cancer</subject><subject>cribriform adenocarcinoma of salivary gland</subject><subject>Exocrine glands</subject><subject>Fluorescence in situ hybridization</subject><subject>gene fusion</subject><subject>Gene rearrangement</subject><subject>Genes</subject><subject>Lymph nodes</subject><subject>Metastases</subject><subject>Multivariate analysis</subject><subject>Mutation hot spots</subject><subject>Nucleoli</subject><subject>Oral cancer</subject><subject>Patients</subject><subject>polymorphous adenocarcinoma</subject><subject>prognosis</subject><subject>Risk factors</subject><subject>Salivary gland</subject><subject>salivary gland neoplasms</subject><subject>Survival</subject><issn>0904-2512</issn><issn>1600-0714</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp1kU1LxDAQhoMouH4c_AcBL3qo5qNNN95k8ZMFBfVcxnS6ZskmNWmV_fdG15PgMDCX5x3mnZeQI87OeK7zZejPuJRSbZEJV4wVrOblNpkwzcpCVFzskr2UlozxWpZ8QsYncPYD4pouHPiW9sGtVyH2b2FMFFr0wUA01ocVXNCZs96a0MPwFlxYWAOOdgjDGDHDWb1AjxTcgBEGG3yi1lOp6D304DEhzUqLfkgHZKcDl_Dwd-6Tl-ur59ltMX-4uZtdzgsjtVIFQqnL7tVwLOvayE7XirVSc81a1KqGqquk0vha556WTE9bKWTVsUoioNGd3Ccnm719DO8jpqFZ2WTQZauYDTZC6VIrwafTjB7_QZdhjD5f14iaCyHzCSJTpxvKxJBSxK7po13l9zWcNd8BZFXf_ASQ2fMN-2kdrv8Hm_uHx43iCzBviM8</recordid><startdate>202209</startdate><enddate>202209</enddate><creator>Fukumura, Masahiro</creator><creator>Ishibashi, Kenichiro</creator><creator>Nakaguro, Masato</creator><creator>Nagao, Toshitaka</creator><creator>Saida, Kosuke</creator><creator>Urano, Makoto</creator><creator>Tanigawa, Maki</creator><creator>Hirai, Hideaki</creator><creator>Yagyuu, Takahiro</creator><creator>Kikuchi, Kentaro</creator><creator>Yada, Naomi</creator><creator>Sugita, Yoshihiko</creator><creator>Miyabe, Megumi</creator><creator>Hasegawa, Shogo</creator><creator>Goto, Mitsuo</creator><creator>Yamamoto, Hidetaka</creator><creator>Ohuchi, Tomoyuki</creator><creator>Kusafuka, Kimihide</creator><creator>Ogawa, Ikuko</creator><creator>Suzuki, Hiroaki</creator><creator>Notohara, Kenji</creator><creator>Shimoda, Masayuki</creator><creator>Tada, Yuichiro</creator><creator>Kirita, Tadaaki</creator><creator>Takata, Takashi</creator><creator>Morinaga, Shojiroh</creator><creator>Maeda, Hatsuhiko</creator><creator>Warnakulasuriya, Saman</creator><creator>Miyabe, Satoru</creator><creator>Nagao, Toru</creator><general>Wiley Subscription Services, Inc</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7T5</scope><scope>H94</scope><scope>K9.</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-3490-2371</orcidid><orcidid>https://orcid.org/0000-0002-0902-6624</orcidid></search><sort><creationdate>202209</creationdate><title>Salivary gland polymorphous adenocarcinoma: Clinicopathological features and gene alterations in 36 Japanese patients</title><author>Fukumura, Masahiro ; Ishibashi, Kenichiro ; Nakaguro, Masato ; Nagao, Toshitaka ; Saida, Kosuke ; Urano, Makoto ; Tanigawa, Maki ; Hirai, Hideaki ; Yagyuu, Takahiro ; Kikuchi, Kentaro ; Yada, Naomi ; Sugita, Yoshihiko ; Miyabe, Megumi ; Hasegawa, Shogo ; Goto, Mitsuo ; Yamamoto, Hidetaka ; Ohuchi, Tomoyuki ; Kusafuka, Kimihide ; Ogawa, Ikuko ; Suzuki, Hiroaki ; Notohara, Kenji ; Shimoda, Masayuki ; Tada, Yuichiro ; Kirita, Tadaaki ; Takata, Takashi ; Morinaga, Shojiroh ; Maeda, Hatsuhiko ; Warnakulasuriya, Saman ; Miyabe, Satoru ; Nagao, Toru</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3966-ea494fbc1e477c3f9760d39190de967a5f5369eb7eb784098d3235f053eaec9f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Adenocarcinoma</topic><topic>Cancer</topic><topic>cribriform adenocarcinoma of salivary gland</topic><topic>Exocrine glands</topic><topic>Fluorescence in situ hybridization</topic><topic>gene fusion</topic><topic>Gene rearrangement</topic><topic>Genes</topic><topic>Lymph nodes</topic><topic>Metastases</topic><topic>Multivariate analysis</topic><topic>Mutation hot spots</topic><topic>Nucleoli</topic><topic>Oral cancer</topic><topic>Patients</topic><topic>polymorphous adenocarcinoma</topic><topic>prognosis</topic><topic>Risk factors</topic><topic>Salivary gland</topic><topic>salivary gland neoplasms</topic><topic>Survival</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fukumura, Masahiro</creatorcontrib><creatorcontrib>Ishibashi, Kenichiro</creatorcontrib><creatorcontrib>Nakaguro, Masato</creatorcontrib><creatorcontrib>Nagao, Toshitaka</creatorcontrib><creatorcontrib>Saida, Kosuke</creatorcontrib><creatorcontrib>Urano, Makoto</creatorcontrib><creatorcontrib>Tanigawa, Maki</creatorcontrib><creatorcontrib>Hirai, Hideaki</creatorcontrib><creatorcontrib>Yagyuu, Takahiro</creatorcontrib><creatorcontrib>Kikuchi, Kentaro</creatorcontrib><creatorcontrib>Yada, Naomi</creatorcontrib><creatorcontrib>Sugita, Yoshihiko</creatorcontrib><creatorcontrib>Miyabe, Megumi</creatorcontrib><creatorcontrib>Hasegawa, Shogo</creatorcontrib><creatorcontrib>Goto, Mitsuo</creatorcontrib><creatorcontrib>Yamamoto, Hidetaka</creatorcontrib><creatorcontrib>Ohuchi, Tomoyuki</creatorcontrib><creatorcontrib>Kusafuka, Kimihide</creatorcontrib><creatorcontrib>Ogawa, Ikuko</creatorcontrib><creatorcontrib>Suzuki, Hiroaki</creatorcontrib><creatorcontrib>Notohara, Kenji</creatorcontrib><creatorcontrib>Shimoda, Masayuki</creatorcontrib><creatorcontrib>Tada, Yuichiro</creatorcontrib><creatorcontrib>Kirita, Tadaaki</creatorcontrib><creatorcontrib>Takata, Takashi</creatorcontrib><creatorcontrib>Morinaga, Shojiroh</creatorcontrib><creatorcontrib>Maeda, Hatsuhiko</creatorcontrib><creatorcontrib>Warnakulasuriya, Saman</creatorcontrib><creatorcontrib>Miyabe, Satoru</creatorcontrib><creatorcontrib>Nagao, Toru</creatorcontrib><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Immunology Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of oral pathology & medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fukumura, Masahiro</au><au>Ishibashi, Kenichiro</au><au>Nakaguro, Masato</au><au>Nagao, Toshitaka</au><au>Saida, Kosuke</au><au>Urano, Makoto</au><au>Tanigawa, Maki</au><au>Hirai, Hideaki</au><au>Yagyuu, Takahiro</au><au>Kikuchi, Kentaro</au><au>Yada, Naomi</au><au>Sugita, Yoshihiko</au><au>Miyabe, Megumi</au><au>Hasegawa, Shogo</au><au>Goto, Mitsuo</au><au>Yamamoto, Hidetaka</au><au>Ohuchi, Tomoyuki</au><au>Kusafuka, Kimihide</au><au>Ogawa, Ikuko</au><au>Suzuki, Hiroaki</au><au>Notohara, Kenji</au><au>Shimoda, Masayuki</au><au>Tada, Yuichiro</au><au>Kirita, Tadaaki</au><au>Takata, Takashi</au><au>Morinaga, Shojiroh</au><au>Maeda, Hatsuhiko</au><au>Warnakulasuriya, Saman</au><au>Miyabe, Satoru</au><au>Nagao, Toru</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Salivary gland polymorphous adenocarcinoma: Clinicopathological features and gene alterations in 36 Japanese patients</atitle><jtitle>Journal of oral pathology & medicine</jtitle><date>2022-09</date><risdate>2022</risdate><volume>51</volume><issue>8</issue><spage>710</spage><epage>720</epage><pages>710-720</pages><issn>0904-2512</issn><eissn>1600-0714</eissn><abstract>Background
Polymorphous adenocarcinoma is a common intraoral minor salivary gland carcinoma in Western countries but is extremely rare in Japan. The current study aimed to characterize the clinicopathological features and status of molecular alterations of polymorphous adenocarcinoma‐associated genes, such as PRKD1/2/3, ARID1A, and DDX3X, in a large cohort of Japanese patients with polymorphous adenocarcinoma.
Methods
We examined the cases of 36 Japanese patients with salivary gland polymorphous adenocarcinoma and 26 cases involving histopathological mimics. To detect gene splits, fluorescence in situ hybridization was carried out for polymorphous adenocarcinoma‐associated genes. Additionally, we applied a SNaPshot multiplex assay to identify PRKD1 hotspot mutations.
Results
This study revealed the indolent clinical course of polymorphous adenocarcinoma with a high 10‐year overall survival rate (92.9%), accompanied by occasional local recurrences and cervical lymph node metastasis (23.3%). Twenty cases (55.6%) of polymorphous adenocarcinoma (but none of the mimics) exhibited alterations in at least one polymorphous adenocarcinoma‐associated gene. Rearrangement of polymorphous adenocarcinoma‐associated genes and PRKD1 E710D were identified in 17 (47.2%) and 4 (11.1%) cases, respectively; one case showed coexisting PRKD3 split and PRKD1 E710D. In the multivariate analysis, high clinical stage (p = 0.0005), the presence of prominent nucleoli (p = 0.0003), and ARID1A split positivity (p = 0.004) were independent risk factors for disease‐free survival.
Conclusion
Japanese patients with polymorphous adenocarcinoma showed clinicopathological features similar to those reported in Western countries. This study disclosed that polymorphous adenocarcinoma‐associated genetic alterations were common and specific findings in polymorphous adenocarcinomas. The diagnostic role and possible prognostic significance of polymorphous adenocarcinoma‐associated genetic alterations in polymorphous adenocarcinomas were suggested.</abstract><cop>Copenhagen</cop><pub>Wiley Subscription Services, Inc</pub><doi>10.1111/jop.13336</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0003-3490-2371</orcidid><orcidid>https://orcid.org/0000-0002-0902-6624</orcidid></addata></record> |
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| ispartof | Journal of oral pathology & medicine, 2022-09, Vol.51 (8), p.710-720 |
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| source | Wiley Online Library Journals Frontfile Complete |
| subjects | Adenocarcinoma Cancer cribriform adenocarcinoma of salivary gland Exocrine glands Fluorescence in situ hybridization gene fusion Gene rearrangement Genes Lymph nodes Metastases Multivariate analysis Mutation hot spots Nucleoli Oral cancer Patients polymorphous adenocarcinoma prognosis Risk factors Salivary gland salivary gland neoplasms Survival |
| title | Salivary gland polymorphous adenocarcinoma: Clinicopathological features and gene alterations in 36 Japanese patients |
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