Vascular density of histologically benign breast tissue from women with breast cancer: associations with tissue composition and tumor characteristics
In breast tumors, it is well established that intratumoral angiogenesis is crucial for malignant progression, but little is known about the vascular characteristics of extratumoral, cancer-adjacent breast. Genome-wide transcriptional data suggest that extratumoral microenvironments may influence bre...
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| Veröffentlicht in: | Human pathology 2019-09, Vol.91, p.43-51 |
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| creator | Fuller, Ashley M. Olsson, Linnea T. Midkiff, Bentley R. Kirk, Erin L. McNaughton, Kirk K. Calhoun, Benjamin C. Troester, Melissa A. |
| description | In breast tumors, it is well established that intratumoral angiogenesis is crucial for malignant progression, but little is known about the vascular characteristics of extratumoral, cancer-adjacent breast. Genome-wide transcriptional data suggest that extratumoral microenvironments may influence breast cancer phenotypes; thus, histologic features of cancer-adjacent tissue may also have clinical implications. To this end, we developed a digital algorithm to quantitate vascular density in approximately 300 histologically benign tissue specimens from breast cancer patients enrolled in the UNC Normal Breast Study (NBS). Specimens were stained for CD31, and vascular content was compared to demographic variables, tissue composition metrics, and tumor molecular features. We observed that the vascular density of cancer-adjacent breast was significantly higher in older and obese women, and was strongly associated with breast adipose tissue content. Consistent with observations that older and heavier women experience higher frequencies of ER+ disease, higher extratumoral vessel density was also significantly associated with positive prognostic tumor features such as lower stage, negative nodal status, and smaller size ( |
| doi_str_mv | 10.1016/j.humpath.2019.06.003 |
| format | Article |
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•Cancer-adjacent breast vessel density is positively associated with age and obesity.•Cancer-adjacent breast vessel density strongly varies with tissue composition.•Breast vessel density is associated with positive prognostic tumor features.•Tissue composition influences breast vessel density-tumor phenotype associations.</description><identifier>ISSN: 0046-8177</identifier><identifier>EISSN: 1532-8392</identifier><identifier>DOI: 10.1016/j.humpath.2019.06.003</identifier><identifier>PMID: 31271812</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adult ; Age Factors ; Aged ; Breast - blood supply ; Breast - pathology ; Breast cancer ; Breast Neoplasms - blood supply ; Breast Neoplasms - pathology ; CD31 ; Demography ; Digital histology ; Family medical history ; Female ; Gene expression ; Humans ; Immunoglobulins ; Medical records ; Microenvironment ; Middle Aged ; Neovascularization, Pathologic - pathology ; Normal breast ; Obesity - pathology ; Population ; Vasculature ; Womens health</subject><ispartof>Human pathology, 2019-09, Vol.91, p.43-51</ispartof><rights>2019</rights><rights>Copyright © 2019. Published by Elsevier Inc.</rights><rights>Copyright Elsevier Limited Sep 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c495t-887a9bb386db7cb1cc2cf13af466e9ed91dac73d78a658d2f5c2d0fc5985bde63</citedby><cites>FETCH-LOGICAL-c495t-887a9bb386db7cb1cc2cf13af466e9ed91dac73d78a658d2f5c2d0fc5985bde63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.humpath.2019.06.003$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31271812$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Fuller, Ashley M.</creatorcontrib><creatorcontrib>Olsson, Linnea T.</creatorcontrib><creatorcontrib>Midkiff, Bentley R.</creatorcontrib><creatorcontrib>Kirk, Erin L.</creatorcontrib><creatorcontrib>McNaughton, Kirk K.</creatorcontrib><creatorcontrib>Calhoun, Benjamin C.</creatorcontrib><creatorcontrib>Troester, Melissa A.</creatorcontrib><title>Vascular density of histologically benign breast tissue from women with breast cancer: associations with tissue composition and tumor characteristics</title><title>Human pathology</title><addtitle>Hum Pathol</addtitle><description>In breast tumors, it is well established that intratumoral angiogenesis is crucial for malignant progression, but little is known about the vascular characteristics of extratumoral, cancer-adjacent breast. Genome-wide transcriptional data suggest that extratumoral microenvironments may influence breast cancer phenotypes; thus, histologic features of cancer-adjacent tissue may also have clinical implications. To this end, we developed a digital algorithm to quantitate vascular density in approximately 300 histologically benign tissue specimens from breast cancer patients enrolled in the UNC Normal Breast Study (NBS). Specimens were stained for CD31, and vascular content was compared to demographic variables, tissue composition metrics, and tumor molecular features. We observed that the vascular density of cancer-adjacent breast was significantly higher in older and obese women, and was strongly associated with breast adipose tissue content. Consistent with observations that older and heavier women experience higher frequencies of ER+ disease, higher extratumoral vessel density was also significantly associated with positive prognostic tumor features such as lower stage, negative nodal status, and smaller size (<2 cm). These results reveal biological relationships between extratumoral vascular content and body size, breast tissue composition, and tumor characteristics, and suggest biological plausibility for the relationship between weight gain (and corresponding breast tissue changes) and breast cancer progression.
•Cancer-adjacent breast vessel density is positively associated with age and obesity.•Cancer-adjacent breast vessel density strongly varies with tissue composition.•Breast vessel density is associated with positive prognostic tumor features.•Tissue composition influences breast vessel density-tumor phenotype associations.</description><subject>Adult</subject><subject>Age Factors</subject><subject>Aged</subject><subject>Breast - blood supply</subject><subject>Breast - pathology</subject><subject>Breast cancer</subject><subject>Breast Neoplasms - blood supply</subject><subject>Breast Neoplasms - pathology</subject><subject>CD31</subject><subject>Demography</subject><subject>Digital histology</subject><subject>Family medical history</subject><subject>Female</subject><subject>Gene expression</subject><subject>Humans</subject><subject>Immunoglobulins</subject><subject>Medical records</subject><subject>Microenvironment</subject><subject>Middle Aged</subject><subject>Neovascularization, Pathologic - pathology</subject><subject>Normal breast</subject><subject>Obesity - pathology</subject><subject>Population</subject><subject>Vasculature</subject><subject>Womens health</subject><issn>0046-8177</issn><issn>1532-8392</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUFv1DAQhSMEotvCTwBZ4sIli-2sHYcDCFUUkCpxAa6WM55svErsxXZa7Q_h_-JqtxVw4eTDfO89z7yqesHomlEm3-zW4zLvTR7XnLJuTeWa0uZRtWKi4bVqOv64WlG6kbVibXtWnae0o5QxsRFPq7OG8ZYpxlfVrx8mwTKZSCz65PKBhIGMLuUwha0DM00H0qN3W0_6iCZlkl1KC5Ihhpnchhk9uXV5vJ-C8YDxLTEpBXAmu-DTETjpIMz7UILKgBhvSV7mEAmMJhrIGEuyg_SsejKYKeHz03tRfb_6-O3yc3399dOXyw_XNWw6kWulWtP1faOk7VvoGQCHgTVm2EiJHdqOWQNtY1tlpFCWDwK4pQOIToneomwuqndH3_3Sz2gBfY5m0vvoZhMPOhin_554N-ptuNEt5Z3kohi8PhnE8HPBlPXsEuA0GY9hSZoXpqGdUG1BX_2D7sISfVmvUKrdUNkoVihxpCCGlCIOD59hVN8Vr3f6VLy-K15TqUvxRffyz00eVPdNF-D9EcByzxuHUSdwWMqyLiJkbYP7T8RvCKTIag</recordid><startdate>20190901</startdate><enddate>20190901</enddate><creator>Fuller, Ashley M.</creator><creator>Olsson, Linnea T.</creator><creator>Midkiff, Bentley R.</creator><creator>Kirk, Erin L.</creator><creator>McNaughton, Kirk K.</creator><creator>Calhoun, Benjamin C.</creator><creator>Troester, Melissa A.</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>K9.</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20190901</creationdate><title>Vascular density of histologically benign breast tissue from women with breast cancer: associations with tissue composition and tumor characteristics</title><author>Fuller, Ashley M. ; Olsson, Linnea T. ; Midkiff, Bentley R. ; Kirk, Erin L. ; McNaughton, Kirk K. ; Calhoun, Benjamin C. ; Troester, Melissa A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c495t-887a9bb386db7cb1cc2cf13af466e9ed91dac73d78a658d2f5c2d0fc5985bde63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Adult</topic><topic>Age Factors</topic><topic>Aged</topic><topic>Breast - blood supply</topic><topic>Breast - pathology</topic><topic>Breast cancer</topic><topic>Breast Neoplasms - blood supply</topic><topic>Breast Neoplasms - pathology</topic><topic>CD31</topic><topic>Demography</topic><topic>Digital histology</topic><topic>Family medical history</topic><topic>Female</topic><topic>Gene expression</topic><topic>Humans</topic><topic>Immunoglobulins</topic><topic>Medical records</topic><topic>Microenvironment</topic><topic>Middle Aged</topic><topic>Neovascularization, Pathologic - pathology</topic><topic>Normal breast</topic><topic>Obesity - pathology</topic><topic>Population</topic><topic>Vasculature</topic><topic>Womens health</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fuller, Ashley M.</creatorcontrib><creatorcontrib>Olsson, Linnea T.</creatorcontrib><creatorcontrib>Midkiff, Bentley R.</creatorcontrib><creatorcontrib>Kirk, Erin L.</creatorcontrib><creatorcontrib>McNaughton, Kirk K.</creatorcontrib><creatorcontrib>Calhoun, Benjamin C.</creatorcontrib><creatorcontrib>Troester, Melissa A.</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 & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Human pathology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fuller, Ashley M.</au><au>Olsson, Linnea T.</au><au>Midkiff, Bentley R.</au><au>Kirk, Erin L.</au><au>McNaughton, Kirk K.</au><au>Calhoun, Benjamin C.</au><au>Troester, Melissa A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Vascular density of histologically benign breast tissue from women with breast cancer: associations with tissue composition and tumor characteristics</atitle><jtitle>Human pathology</jtitle><addtitle>Hum Pathol</addtitle><date>2019-09-01</date><risdate>2019</risdate><volume>91</volume><spage>43</spage><epage>51</epage><pages>43-51</pages><issn>0046-8177</issn><eissn>1532-8392</eissn><abstract>In breast tumors, it is well established that intratumoral angiogenesis is crucial for malignant progression, but little is known about the vascular characteristics of extratumoral, cancer-adjacent breast. Genome-wide transcriptional data suggest that extratumoral microenvironments may influence breast cancer phenotypes; thus, histologic features of cancer-adjacent tissue may also have clinical implications. To this end, we developed a digital algorithm to quantitate vascular density in approximately 300 histologically benign tissue specimens from breast cancer patients enrolled in the UNC Normal Breast Study (NBS). Specimens were stained for CD31, and vascular content was compared to demographic variables, tissue composition metrics, and tumor molecular features. We observed that the vascular density of cancer-adjacent breast was significantly higher in older and obese women, and was strongly associated with breast adipose tissue content. Consistent with observations that older and heavier women experience higher frequencies of ER+ disease, higher extratumoral vessel density was also significantly associated with positive prognostic tumor features such as lower stage, negative nodal status, and smaller size (<2 cm). These results reveal biological relationships between extratumoral vascular content and body size, breast tissue composition, and tumor characteristics, and suggest biological plausibility for the relationship between weight gain (and corresponding breast tissue changes) and breast cancer progression.
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| ispartof | Human pathology, 2019-09, Vol.91, p.43-51 |
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| source | MEDLINE; Elsevier ScienceDirect Journals Complete |
| subjects | Adult Age Factors Aged Breast - blood supply Breast - pathology Breast cancer Breast Neoplasms - blood supply Breast Neoplasms - pathology CD31 Demography Digital histology Family medical history Female Gene expression Humans Immunoglobulins Medical records Microenvironment Middle Aged Neovascularization, Pathologic - pathology Normal breast Obesity - pathology Population Vasculature Womens health |
| title | Vascular density of histologically benign breast tissue from women with breast cancer: associations with tissue composition and tumor characteristics |
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