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Papillary lesions of the breast: A systematic evaluation of cytologic parameters

Background The cytologic diagnosis of papillary lesions of the breast is challenging because of the diverse morphology, including epithelial hyperplasia, atypia, low‐grade malignancy, and neuroendocrine differentiation; also, traditional malignant features such as necrosis and myoepithelial cell los...

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Published in:Cancer cytopathology 2021-08, Vol.129 (8), p.649-661
Main Authors: Jamidi, Shirley Kristina, Li, Joshua J. X., Aphivatanasiri, Chaiwat, Chow, Maria B. C. Y., Chan, Ronald C. K., Ng, Joanna K. M., Tsang, Julia Y., Tse, Gary M.
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container_title Cancer cytopathology
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creator Jamidi, Shirley Kristina
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Tse, Gary M.
description Background The cytologic diagnosis of papillary lesions of the breast is challenging because of the diverse morphology, including epithelial hyperplasia, atypia, low‐grade malignancy, and neuroendocrine differentiation; also, traditional malignant features such as necrosis and myoepithelial cell loss can be lacking. Thus, the diagnostic criteria for papillary lesions may differ from those for other breast lesions. This study evaluated various cytologic parameters in a large cohort to identify useful diagnostic features. Methods Cytologic preparations of papillary lesions with histologic follow‐up were reviewed for features related to cellularity, epithelial cohesiveness, cellular and stromal architecture, cytomorphology, and background. Corresponding histologic slides were also reviewed. Results In all, 153 cases were included. Epithelial discohesion, solid and cribriform patterns, atypical nuclear features, and mitoses (P ≤ .001 to P = .017) were associated with malignancy. Cell balls, monolayer sheets, and features of cystic change (P < .001 to P = .016) were associated with benign lesions. Complex (P = .031) and slender (P = .026) papillae and neuroendocrine features (P < .001) were associated with malignancy. Hemorrhage, background, and infiltrating neutrophils (P < .001 to P = .025) were associated with malignancy; fibrotic broad papillary stromal fragments (naked papillary fronds [NPFs]; P = .043) were associated with benignity. The presence of any single parameter, including the absence of myoepithelial cells within epithelial structure, the presence of cytoplasmic granules, an increased amount of cytoplasm, and a nuclear to cytoplasmic (N/C) ratio greater than 0.7, which were identified by principal component analysis, yielded a sensitivity of 95.1% and a specificity of 100.0% in predicting malignancy. Conclusions Methodological assessment of multiple features is recommended. Myoepithelial cells, cytoplasmic granules, the amount of cytoplasm, and the N/C ratio are key features for diagnosis. Papillary breast aspirates are challenging and require methodological assessment of multiple features. Myoepithelial cells, cytoplasmic granules, the amount of cytoplasm, and the nuclear to cytoplasmic ratio are key features for diagnosis.
doi_str_mv 10.1002/cncy.22412
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X. ; Aphivatanasiri, Chaiwat ; Chow, Maria B. C. Y. ; Chan, Ronald C. K. ; Ng, Joanna K. M. ; Tsang, Julia Y. ; Tse, Gary M.</creator><creatorcontrib>Jamidi, Shirley Kristina ; Li, Joshua J. X. ; Aphivatanasiri, Chaiwat ; Chow, Maria B. C. Y. ; Chan, Ronald C. K. ; Ng, Joanna K. M. ; Tsang, Julia Y. ; Tse, Gary M.</creatorcontrib><description>Background The cytologic diagnosis of papillary lesions of the breast is challenging because of the diverse morphology, including epithelial hyperplasia, atypia, low‐grade malignancy, and neuroendocrine differentiation; also, traditional malignant features such as necrosis and myoepithelial cell loss can be lacking. Thus, the diagnostic criteria for papillary lesions may differ from those for other breast lesions. This study evaluated various cytologic parameters in a large cohort to identify useful diagnostic features. Methods Cytologic preparations of papillary lesions with histologic follow‐up were reviewed for features related to cellularity, epithelial cohesiveness, cellular and stromal architecture, cytomorphology, and background. Corresponding histologic slides were also reviewed. Results In all, 153 cases were included. Epithelial discohesion, solid and cribriform patterns, atypical nuclear features, and mitoses (P ≤ .001 to P = .017) were associated with malignancy. Cell balls, monolayer sheets, and features of cystic change (P &lt; .001 to P = .016) were associated with benign lesions. Complex (P = .031) and slender (P = .026) papillae and neuroendocrine features (P &lt; .001) were associated with malignancy. Hemorrhage, background, and infiltrating neutrophils (P &lt; .001 to P = .025) were associated with malignancy; fibrotic broad papillary stromal fragments (naked papillary fronds [NPFs]; P = .043) were associated with benignity. The presence of any single parameter, including the absence of myoepithelial cells within epithelial structure, the presence of cytoplasmic granules, an increased amount of cytoplasm, and a nuclear to cytoplasmic (N/C) ratio greater than 0.7, which were identified by principal component analysis, yielded a sensitivity of 95.1% and a specificity of 100.0% in predicting malignancy. Conclusions Methodological assessment of multiple features is recommended. Myoepithelial cells, cytoplasmic granules, the amount of cytoplasm, and the N/C ratio are key features for diagnosis. Papillary breast aspirates are challenging and require methodological assessment of multiple features. Myoepithelial cells, cytoplasmic granules, the amount of cytoplasm, and the nuclear to cytoplasmic ratio are key features for diagnosis.</description><identifier>ISSN: 1934-662X</identifier><identifier>EISSN: 1934-6638</identifier><identifier>DOI: 10.1002/cncy.22412</identifier><identifier>PMID: 33561323</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Breast ; Carcinoma, Papillary ; Diagnosis, Differential ; Epithelial Cells ; Fibroadenoma ; fine‐needle aspirate cytology ; Humans ; intraductal papilloma ; papillary ; papillary carcinoma ; Principal components analysis ; Tumors</subject><ispartof>Cancer cytopathology, 2021-08, Vol.129 (8), p.649-661</ispartof><rights>2021 American Cancer Society</rights><rights>2021 American Cancer Society.</rights><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3932-86f7e5324800b60a8751588f6c9f1d622ddfdde3828d58c68e6a82776a7b57d93</citedby><cites>FETCH-LOGICAL-c3932-86f7e5324800b60a8751588f6c9f1d622ddfdde3828d58c68e6a82776a7b57d93</cites><orcidid>0000-0003-2425-0314 ; 0000-0001-9267-0076</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fcncy.22412$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fcncy.22412$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,786,790,27957,27958,50923,51032</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33561323$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jamidi, Shirley Kristina</creatorcontrib><creatorcontrib>Li, Joshua J. X.</creatorcontrib><creatorcontrib>Aphivatanasiri, Chaiwat</creatorcontrib><creatorcontrib>Chow, Maria B. C. Y.</creatorcontrib><creatorcontrib>Chan, Ronald C. K.</creatorcontrib><creatorcontrib>Ng, Joanna K. M.</creatorcontrib><creatorcontrib>Tsang, Julia Y.</creatorcontrib><creatorcontrib>Tse, Gary M.</creatorcontrib><title>Papillary lesions of the breast: A systematic evaluation of cytologic parameters</title><title>Cancer cytopathology</title><addtitle>Cancer Cytopathol</addtitle><description>Background The cytologic diagnosis of papillary lesions of the breast is challenging because of the diverse morphology, including epithelial hyperplasia, atypia, low‐grade malignancy, and neuroendocrine differentiation; also, traditional malignant features such as necrosis and myoepithelial cell loss can be lacking. Thus, the diagnostic criteria for papillary lesions may differ from those for other breast lesions. This study evaluated various cytologic parameters in a large cohort to identify useful diagnostic features. Methods Cytologic preparations of papillary lesions with histologic follow‐up were reviewed for features related to cellularity, epithelial cohesiveness, cellular and stromal architecture, cytomorphology, and background. Corresponding histologic slides were also reviewed. Results In all, 153 cases were included. Epithelial discohesion, solid and cribriform patterns, atypical nuclear features, and mitoses (P ≤ .001 to P = .017) were associated with malignancy. Cell balls, monolayer sheets, and features of cystic change (P &lt; .001 to P = .016) were associated with benign lesions. Complex (P = .031) and slender (P = .026) papillae and neuroendocrine features (P &lt; .001) were associated with malignancy. Hemorrhage, background, and infiltrating neutrophils (P &lt; .001 to P = .025) were associated with malignancy; fibrotic broad papillary stromal fragments (naked papillary fronds [NPFs]; P = .043) were associated with benignity. The presence of any single parameter, including the absence of myoepithelial cells within epithelial structure, the presence of cytoplasmic granules, an increased amount of cytoplasm, and a nuclear to cytoplasmic (N/C) ratio greater than 0.7, which were identified by principal component analysis, yielded a sensitivity of 95.1% and a specificity of 100.0% in predicting malignancy. Conclusions Methodological assessment of multiple features is recommended. Myoepithelial cells, cytoplasmic granules, the amount of cytoplasm, and the N/C ratio are key features for diagnosis. Papillary breast aspirates are challenging and require methodological assessment of multiple features. Myoepithelial cells, cytoplasmic granules, the amount of cytoplasm, and the nuclear to cytoplasmic ratio are key features for diagnosis.</description><subject>Breast</subject><subject>Carcinoma, Papillary</subject><subject>Diagnosis, Differential</subject><subject>Epithelial Cells</subject><subject>Fibroadenoma</subject><subject>fine‐needle aspirate cytology</subject><subject>Humans</subject><subject>intraductal papilloma</subject><subject>papillary</subject><subject>papillary carcinoma</subject><subject>Principal components analysis</subject><subject>Tumors</subject><issn>1934-662X</issn><issn>1934-6638</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp9kE1LwzAYgIMobk4v_gApeBGhMx9Lmnobwy8Q3UFBTyFL32pH28ykVfrvzezcwYOnvISHh_d9EDomeEwwphemNt2Y0gmhO2hIUjaJhWBydzvTlwE68H6JMZEJJftowBgXhFE2RPO5XhVlqV0XleALW_vI5lHzDtHCgfbNZTSNfOcbqHRTmAg-ddmGydZrzHSNLe1b-F9ppytowPlDtJfr0sPR5h2h5-urp9ltfP94czeb3seGpYzGUuQJcEYnEuOFwFomnHApc2HSnGSC0izLswyYpDLj0ggJQkuaJEInC55kKRuhs967cvajBd-oqvAGwik12NarYJZEcpKKgJ7-QZe2dXXYTlHOJRaMJGvqvKeMs947yNXKFVUIowhW685q3Vn9dA7wyUbZLirItuhv2ACQHvgqSuj-UanZw-y1l34DIaiHKw</recordid><startdate>202108</startdate><enddate>202108</enddate><creator>Jamidi, Shirley Kristina</creator><creator>Li, Joshua J. 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M. ; Tsang, Julia Y. ; Tse, Gary M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3932-86f7e5324800b60a8751588f6c9f1d622ddfdde3828d58c68e6a82776a7b57d93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Breast</topic><topic>Carcinoma, Papillary</topic><topic>Diagnosis, Differential</topic><topic>Epithelial Cells</topic><topic>Fibroadenoma</topic><topic>fine‐needle aspirate cytology</topic><topic>Humans</topic><topic>intraductal papilloma</topic><topic>papillary</topic><topic>papillary carcinoma</topic><topic>Principal components analysis</topic><topic>Tumors</topic><toplevel>online_resources</toplevel><creatorcontrib>Jamidi, Shirley Kristina</creatorcontrib><creatorcontrib>Li, Joshua J. X.</creatorcontrib><creatorcontrib>Aphivatanasiri, Chaiwat</creatorcontrib><creatorcontrib>Chow, Maria B. C. Y.</creatorcontrib><creatorcontrib>Chan, Ronald C. K.</creatorcontrib><creatorcontrib>Ng, Joanna K. M.</creatorcontrib><creatorcontrib>Tsang, Julia Y.</creatorcontrib><creatorcontrib>Tse, Gary M.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Cancer cytopathology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jamidi, Shirley Kristina</au><au>Li, Joshua J. X.</au><au>Aphivatanasiri, Chaiwat</au><au>Chow, Maria B. C. Y.</au><au>Chan, Ronald C. K.</au><au>Ng, Joanna K. M.</au><au>Tsang, Julia Y.</au><au>Tse, Gary M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Papillary lesions of the breast: A systematic evaluation of cytologic parameters</atitle><jtitle>Cancer cytopathology</jtitle><addtitle>Cancer Cytopathol</addtitle><date>2021-08</date><risdate>2021</risdate><volume>129</volume><issue>8</issue><spage>649</spage><epage>661</epage><pages>649-661</pages><issn>1934-662X</issn><eissn>1934-6638</eissn><notes>577‐578</notes><notes>this issue.</notes><notes>See editorial on pages</notes><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Background The cytologic diagnosis of papillary lesions of the breast is challenging because of the diverse morphology, including epithelial hyperplasia, atypia, low‐grade malignancy, and neuroendocrine differentiation; also, traditional malignant features such as necrosis and myoepithelial cell loss can be lacking. Thus, the diagnostic criteria for papillary lesions may differ from those for other breast lesions. This study evaluated various cytologic parameters in a large cohort to identify useful diagnostic features. Methods Cytologic preparations of papillary lesions with histologic follow‐up were reviewed for features related to cellularity, epithelial cohesiveness, cellular and stromal architecture, cytomorphology, and background. Corresponding histologic slides were also reviewed. Results In all, 153 cases were included. Epithelial discohesion, solid and cribriform patterns, atypical nuclear features, and mitoses (P ≤ .001 to P = .017) were associated with malignancy. Cell balls, monolayer sheets, and features of cystic change (P &lt; .001 to P = .016) were associated with benign lesions. Complex (P = .031) and slender (P = .026) papillae and neuroendocrine features (P &lt; .001) were associated with malignancy. Hemorrhage, background, and infiltrating neutrophils (P &lt; .001 to P = .025) were associated with malignancy; fibrotic broad papillary stromal fragments (naked papillary fronds [NPFs]; P = .043) were associated with benignity. The presence of any single parameter, including the absence of myoepithelial cells within epithelial structure, the presence of cytoplasmic granules, an increased amount of cytoplasm, and a nuclear to cytoplasmic (N/C) ratio greater than 0.7, which were identified by principal component analysis, yielded a sensitivity of 95.1% and a specificity of 100.0% in predicting malignancy. Conclusions Methodological assessment of multiple features is recommended. Myoepithelial cells, cytoplasmic granules, the amount of cytoplasm, and the N/C ratio are key features for diagnosis. Papillary breast aspirates are challenging and require methodological assessment of multiple features. Myoepithelial cells, cytoplasmic granules, the amount of cytoplasm, and the nuclear to cytoplasmic ratio are key features for diagnosis.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>33561323</pmid><doi>10.1002/cncy.22412</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-2425-0314</orcidid><orcidid>https://orcid.org/0000-0001-9267-0076</orcidid><oa>free_for_read</oa></addata></record>
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subjects Breast
Carcinoma, Papillary
Diagnosis, Differential
Epithelial Cells
Fibroadenoma
fine‐needle aspirate cytology
Humans
intraductal papilloma
papillary
papillary carcinoma
Principal components analysis
Tumors
title Papillary lesions of the breast: A systematic evaluation of cytologic parameters
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