{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T03:38:45Z","timestamp":1791517125473,"version":"4.3.4"},"reference-count":30,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,10,4]],"date-time":"2019-10-04T00:00:00Z","timestamp":1570147200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2019,10,4]],"date-time":"2019-10-04T00:00:00Z","timestamp":1570147200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Ovarian cancer is the leading cause of death among gynecological cancers, but is poorly amenable to preoperative diagnosis. In this study, we investigate the feasibility of \u201coptical biopsy,\u201d using high-optical-resolution photoacoustic microscopy (OR-PAM) to quantify the microvasculature of ovarian and fallopian tube tissue. The technique is demonstrated using excised human ovary and fallopian tube specimens imaged immediately after surgery. Quantitative parameters are derived using Amira software. The parameters include three-dimensional vascular segment count, total volume and length, which are associated with tumor angiogenesis. Qualitative results of OR-PAM demonstrate that malignant ovarian tissue has larger and more tortuous blood vessels as well as smaller vessels of different sizes, while benign and normal ovarian tissue has smaller vessels of uniform size. Quantitative analysis shows that malignant ovaries have greater tumor vessel volume, length and number of segments, as compared with benign and normal ovaries. The vascular pattern of benign fallopian tube is different than that of benign ovarian tissue. Our initial results demonstrate the potential of OR-PAM as an imaging tool for fast assessment of ovarian tissue and fallopian tube and could avoid unnecessary surgery if the risk of the examined ovary is extremely low.<\/jats:p>","DOI":"10.1038\/s41598-019-50743-7","type":"journal-article","created":{"date-parts":[[2019,10,4]],"date-time":"2019-10-04T10:02:49Z","timestamp":1570183369000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Optical Resolution Photoacoustic Microscopy of Ovary and Fallopian Tube"],"prefix":"10.1038","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6494-3110","authenticated-orcid":false,"given":"Bin","family":"Rao","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiandong","family":"Leng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yifeng","family":"Zeng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yixiao","family":"Lin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5338-359X","authenticated-orcid":false,"given":"Ruimin","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qifa","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrea R.","family":"Hagemann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lindsay M.","family":"Kuroki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carolyn K.","family":"McCourt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David G.","family":"Mutch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matthew A.","family":"Powell","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ian S.","family":"Hagemann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1837-2588","authenticated-orcid":false,"given":"Quing","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2019,10,4]]},"reference":[{"key":"50743_CR1","doi-asserted-by":"publisher","first-page":"284","DOI":"10.3322\/caac.21456","volume":"68","author":"LA Torre","year":"2018","unstructured":"Torre, L. A. et al. Ovarian cancer statistics, 2018. CA: a cancer journal for clinicians 68, 284\u2013296, https:\/\/doi.org\/10.3322\/caac.21456 (2018).","journal-title":"CA: a cancer journal for clinicians"},{"key":"50743_CR2","doi-asserted-by":"publisher","first-page":"7","DOI":"10.3322\/caac.21551","volume":"69","author":"RL Siegel","year":"2019","unstructured":"Siegel, R. L., Miller, K. D. & Jemal, A. Cancer statistics, 2019. CA: a cancer journal for clinicians 69, 7\u201334, https:\/\/doi.org\/10.3322\/caac.21551 (2019).","journal-title":"CA: a cancer journal for clinicians"},{"key":"50743_CR3","doi-asserted-by":"publisher","first-page":"945","DOI":"10.1016\/S0140-6736(15)01224-6","volume":"387","author":"IJ Jacobs","year":"2016","unstructured":"Jacobs, I. J. et al. Ovarian cancer screening and mortality in the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS): a randomised controlled trial. The Lancet 387, 945\u2013956, https:\/\/doi.org\/10.1016\/S0140-6736(15)01224-6 (2016).","journal-title":"The Lancet"},{"key":"50743_CR4","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1016\/j.ajog.2008.04.009","volume":"199","author":"V Nossov","year":"2008","unstructured":"Nossov, V. et al. The early detection of ovarian cancer: from traditional methods to proteomics. Can we really do better than serum CA-125? American journal of obstetrics and gynecology 199, 215\u2013223, https:\/\/doi.org\/10.1016\/j.ajog.2008.04.009 (2008).","journal-title":"American journal of obstetrics and gynecology"},{"key":"50743_CR5","doi-asserted-by":"publisher","first-page":"1445","DOI":"10.1148\/radiographics.20.5.g00se101445","volume":"20","author":"YY Jeong","year":"2000","unstructured":"Jeong, Y. Y., Outwater, E. K. & Kang, H. K. Imaging evaluation of ovarian masses. Radiographics 20, 1445\u20131470, https:\/\/doi.org\/10.1148\/radiographics.20.5.g00se101445 (2000).","journal-title":"Radiographics"},{"key":"50743_CR6","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1016\/S1470-2045(06)70585-X","volume":"7","author":"SM Domchek","year":"2006","unstructured":"Domchek, S. M. et al. Mortality after bilateral salpingo-oophorectomy in BRCA1 and BRCA2 mutation carriers: a prospective cohort study. The lancet oncology 7, 223\u2013229, https:\/\/doi.org\/10.1016\/S1470-2045(06)70585-X (2006).","journal-title":"The lancet oncology"},{"key":"50743_CR7","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1001\/jama.296.2.185","volume":"296","author":"A Finch","year":"2006","unstructured":"Finch, A. et al. Salpingo-oophorectomy and the risk of ovarian, fallopian tube, and peritoneal cancers in women with a BRCA1 or BRCA2 Mutation. Jama 296, 185\u2013192, https:\/\/doi.org\/10.1001\/jama.296.2.185 (2006).","journal-title":"Jama"},{"key":"50743_CR8","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1097\/AOG.0b013e3182783c2f","volume":"121","author":"JS Kwon","year":"2013","unstructured":"Kwon, J. S. et al. Prophylactic salpingectomy and delayed oophorectomy as an alternative for BRCA mutation carriers. Obstetrics & Gynecology 121, 14\u201324, https:\/\/doi.org\/10.1097\/AOG.0b013e3182783c2f (2013).","journal-title":"Obstetrics & Gynecology"},{"key":"50743_CR9","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1016\/j.ygyno.2009.05.014","volume":"114","author":"LP Hariri","year":"2009","unstructured":"Hariri, L. P. et al. Laparoscopic optical coherence tomography imaging of human ovarian cancer. Gynecologic oncology 114, 188\u2013194, https:\/\/doi.org\/10.1016\/j.ygyno.2009.05.014 (2009).","journal-title":"Gynecologic oncology"},{"key":"50743_CR10","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1002\/wnan.1306","volume":"7","author":"T Wang","year":"2015","unstructured":"Wang, T., Brewer, M. & Zhu, Q. An overview of optical coherence tomography for ovarian tissue imaging and characterization. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology 7, 1\u201316, https:\/\/doi.org\/10.1002\/wnan.1306 (2015).","journal-title":"Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology"},{"key":"50743_CR11","doi-asserted-by":"publisher","first-page":"090504","DOI":"10.1117\/1.3625247","volume":"16","author":"Y Yang","year":"2011","unstructured":"Yang, Y. et al. Optical scattering coefficient estimated by optical coherence tomography correlates with collagen content in ovarian tissue. Journal of biomedical optics 16, 090504, https:\/\/doi.org\/10.1117\/1.3625247 (2011).","journal-title":"Journal of biomedical optics"},{"key":"50743_CR12","doi-asserted-by":"publisher","first-page":"025501","DOI":"10.1117\/1.JMI.1.2.025501","volume":"1","author":"WA Welge","year":"2014","unstructured":"Welge, W. A. et al. Diagnostic potential of multimodal imaging of ovarian tissue using optical coherence tomography and second-harmonic generation microscopy. Journal of Medical Imaging 1, 025501, https:\/\/doi.org\/10.1117\/1.JMI.1.2.025501 (2014).","journal-title":"Journal of Medical Imaging"},{"key":"50743_CR13","doi-asserted-by":"publisher","first-page":"438","DOI":"10.4161\/cbt.10.5.12531","volume":"10","author":"LP Hariri","year":"2010","unstructured":"Hariri, L. P. et al. Simultaneous optical coherence tomography and laser induced fluorescence imaging in rat model of ovarian carcinogenesis. Cancer biology & therapy 10, 438\u2013447, https:\/\/doi.org\/10.4161\/cbt.10.5.12531 (2010).","journal-title":"Cancer biology & therapy"},{"key":"50743_CR14","doi-asserted-by":"publisher","first-page":"020501","DOI":"10.1117\/1.JBO.21.2.020501","volume":"21","author":"C Yeh","year":"2016","unstructured":"Yeh, C. et al. Photoacoustic microscopy of arteriovenous shunts and blood diffusion in early-stage tumors. Journal of biomedical optics 21, 020501, https:\/\/doi.org\/10.1117\/1.JBO.21.2.020501 (2016).","journal-title":"Journal of biomedical optics"},{"key":"50743_CR15","doi-asserted-by":"publisher","DOI":"10.1038\/srep11778","volume":"5","author":"M Heijblom","year":"2015","unstructured":"Heijblom, M. et al. Photoacoustic image patterns of breast carcinoma and comparisons with Magnetic Resonance Imaging and vascular stained histopathology. Scientific reports 5, 11778, https:\/\/doi.org\/10.1038\/srep11778 (2015).","journal-title":"Scientific reports"},{"key":"50743_CR16","doi-asserted-by":"publisher","first-page":"208","DOI":"10.1016\/j.neo.2014.12.010","volume":"17","author":"M Omar","year":"2015","unstructured":"Omar, M., Schwarz, M., Soliman, D., Symvoulidis, P. & Ntziachristos, V. Pushing the optical imaging limits of cancer with multi-frequency-band raster-scan optoacoustic mesoscopy (RSOM). Neoplasia 17, 208\u2013214, https:\/\/doi.org\/10.1016\/j.neo.2014.12.010 (2015).","journal-title":"Neoplasia"},{"key":"50743_CR17","doi-asserted-by":"publisher","first-page":"740","DOI":"10.1148\/radiol.2018180666","volume":"289","author":"S Nandy","year":"2018","unstructured":"Nandy, S. et al. Evaluation of ovarian cancer: initial application of coregistered photoacoustic tomography and US. Radiology 289, 740\u2013747, https:\/\/doi.org\/10.1148\/radiol.2018180666 (2018).","journal-title":"Radiology"},{"key":"50743_CR18","doi-asserted-by":"publisher","first-page":"2763","DOI":"10.1364\/BOE.4.002763","volume":"4","author":"T Wang","year":"2013","unstructured":"Wang, T. et al. Characterization of ovarian tissue based on quantitative analysis of photoacoustic microscopy images. Biomedical optics express 4, 2763\u20132768, https:\/\/doi.org\/10.1364\/BOE.4.002763 (2013).","journal-title":"Biomedical optics express"},{"key":"50743_CR19","doi-asserted-by":"publisher","first-page":"4434","DOI":"10.1364\/OL.42.004434","volume":"42","author":"T Jin","year":"2017","unstructured":"Jin, T., Guo, H., Jiang, H., Ke, B. & Xi, L. Portable optical resolution photoacoustic microscopy (pORPAM) for human oral imaging. Optics letters 42, 4434\u20134437, https:\/\/doi.org\/10.1364\/OL.42.004434 (2017).","journal-title":"Optics letters"},{"key":"50743_CR20","doi-asserted-by":"publisher","first-page":"016015","DOI":"10.1117\/1.3528661","volume":"16","author":"CP Favazza","year":"2011","unstructured":"Favazza, C. P., Wang, L. V., Jassim, O. W. & Cornelius, L. A. In vivo photoacoustic microscopy of human cutaneous microvasculature and a nevus. Journal of biomedical optics 16, 016015, https:\/\/doi.org\/10.1117\/1.3528661 (2011).","journal-title":"Journal of biomedical optics"},{"key":"50743_CR21","doi-asserted-by":"publisher","first-page":"e1602168","DOI":"10.1126\/sciadv.1602168","volume":"3","author":"TTW Wong","year":"2017","unstructured":"Wong, T. T. W. et al. Fast label-free multilayered histology-like imaging of human breast cancer by photoacoustic microscopy. Science advances 3, e1602168, https:\/\/doi.org\/10.1126\/sciadv.1602168 (2017).","journal-title":"Science advances"},{"key":"50743_CR22","doi-asserted-by":"publisher","first-page":"409","DOI":"10.1016\/j.ajog.2013.04.019","volume":"209","author":"BK Erickson","year":"2013","unstructured":"Erickson, B. K., Conner, M. G. & Landen, C. N. Jr. The role of the fallopian tube in the origin of ovarian cancer. American Journal of Obstetrics and Gynecology 209, 409\u2013414, https:\/\/doi.org\/10.1016\/j.ajog.2013.04.019 (2013).","journal-title":"American Journal of Obstetrics and Gynecology"},{"key":"50743_CR23","doi-asserted-by":"publisher","first-page":"108","DOI":"10.3389\/fonc.2016.00108","volume":"6","author":"SHL George","year":"2016","unstructured":"George, S. H. L., Garcia, R. & Slomovitz, B. M. Ovarian cancer: the fallopian tube as the site of origin and opportunities for prevention. Frontiers in Oncology 6, 108, https:\/\/doi.org\/10.3389\/fonc.2016.00108 (2016).","journal-title":"Frontiers in Oncology"},{"key":"50743_CR24","doi-asserted-by":"publisher","unstructured":"Zeng, Y. et al. Histogram analysis of en face scattering coefficient map predicts malignancy in human ovarian tissue. Journal of Biophotonics p, e201900115, https:\/\/doi.org\/10.1002\/jbio.201900115 (2019).","DOI":"10.1002\/jbio.201900115"},{"key":"50743_CR25","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1016\/j.ajodo.2006.08.024","volume":"134","author":"MO Lagrav\u00e8re","year":"2008","unstructured":"Lagrav\u00e8re, M. O., Carey, J., Toogood, R. W. & Major, P. W. Three-dimensional accuracy of measurements made with software on cone-beam computed tomography images. American Journal of Orthodontics and Dentofacial Orthopedics 134, 112\u2013116, https:\/\/doi.org\/10.1016\/j.ajodo.2006.08.024 (2008).","journal-title":"American Journal of Orthodontics and Dentofacial Orthopedics"},{"key":"50743_CR26","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1016\/j.tripleo.2006.06.008","volume":"103","author":"T Ogawa","year":"2007","unstructured":"Ogawa, T., Enciso, R., Shintaku, W. H. & Clark, G. T. Evaluation of cross-section airway configuration of obstructive sleep apnea. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology 103, 102\u2013108, https:\/\/doi.org\/10.1016\/j.tripleo.2006.06.008 (2007).","journal-title":"Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology"},{"key":"50743_CR27","doi-asserted-by":"publisher","first-page":"1203","DOI":"10.1016\/j.neuroscience.2005.07.014","volume":"135","author":"Y Ma","year":"2005","unstructured":"Ma, Y. et al. A three-dimensional digital atlas database of the adult C57BL\/6J mouse brain by magnetic resonance microscopy. Neuroscience 135, 1203\u20131215, https:\/\/doi.org\/10.1016\/j.neuroscience.2005.07.014 (2005).","journal-title":"Neuroscience"},{"key":"50743_CR28","doi-asserted-by":"publisher","first-page":"2342","DOI":"10.1364\/OL.42.002342","volume":"42","author":"H Ma","year":"2017","unstructured":"Ma, H., Yang, S., Cheng, Z. & Xing, D. Photoacoustic confocal dermoscope with a waterless coupling and impedance matching optosono probe. Optics Letters 42, 2342\u20132345, https:\/\/doi.org\/10.1364\/OL.42.002342 (2017).","journal-title":"Optics Letters"},{"key":"50743_CR29","doi-asserted-by":"publisher","first-page":"2095","DOI":"10.1364\/BOE.7.002095","volume":"7","author":"D Xu","year":"2016","unstructured":"Xu, D., Yang, S., Wang, Y., Gu, Y. & Xing, D. Noninvasive and high-resolving photoacoustic dermoscopy of human skin. Biomedical Optics Express 7, 2095\u20132102, https:\/\/doi.org\/10.1364\/BOE.7.002095 (2016).","journal-title":"Biomedical Optics Express"},{"key":"50743_CR30","doi-asserted-by":"crossref","unstructured":"Stalling, D., Westerhoff, M. & Hege, H. C. Amira: A highly interactive system for visual data analysis in The visualization handbook (ed. Hansen, C. D. & Johnson, C. R.) 749\u2013767 (Elsevier, 2005).","DOI":"10.1016\/B978-012387582-2\/50040-X"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-50743-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-50743-7","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-50743-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,17]],"date-time":"2022-12-17T14:21:27Z","timestamp":1671286887000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-50743-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,10,4]]},"references-count":30,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2019,12]]}},"alternative-id":["50743"],"URL":"https:\/\/doi.org\/10.1038\/s41598-019-50743-7","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,10,4]]},"assertion":[{"value":"4 June 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 September 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 October 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"14306"}}