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Open Access 01-12-2023 | Ultrasound | Research

Noninvasive prediction of axillary lymph node breast cancer metastasis using morphometric analysis of nodal tumor microvessels in a contrast-free ultrasound approach

Authors: Giulia Ferroni, Soroosh Sabeti, Tasneem Abdus-Shakur, Lorenzo Scalise, Jodi M. Carter, Robert T. Fazzio, Nicholas B. Larson, Mostafa Fatemi, Azra Alizad

Published in: Breast Cancer Research | Issue 1/2023

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Abstract

Purpose

Changes in microcirculation of axillary lymph nodes (ALNs) may indicate metastasis. Reliable noninvasive imaging technique to quantify such variations is lacking. We aim to develop and investigate a contrast-free ultrasound quantitative microvasculature imaging technique for detection of metastatic ALN in vivo.

Experimental design

The proposed ultrasound-based technique, high-definition microvasculature imaging (HDMI) provides superb images of tumor microvasculature at sub-millimeter size scales and enables quantitative analysis of microvessels structures. We evaluated the new HDMI technique on 68 breast cancer patients with ultrasound-identified suspicious ipsilateral axillary lymph nodes recommended for fine needle aspiration biopsy (FNAB). HDMI was conducted before the FNAB and vessel morphological features were extracted, analyzed, and the results were correlated with the histopathology.

Results

Out of 15 evaluated quantitative HDMI biomarkers, 11 were significantly different in metastatic and reactive ALNs (10 with P << 0.01 and one with 0.01 < P < 0.05). We further showed that through analysis of these biomarkers, a predictive model trained on HDMI biomarkers combined with clinical information (i.e., age, node size, cortical thickness, and BI-RADS score) could identify metastatic lymph nodes with an area under the curve of 0.9 (95% CI [0.82,0.98]), sensitivity of 90%, and specificity of 88%.

Conclusions

The promising results of our morphometric analysis of HDMI on ALNs offer a new means of detecting lymph node metastasis when used as a complementary imaging tool to conventional ultrasound. The fact that it does not require injection of contrast agents simplifies its use in routine clinical practice.
Literature
1.
2.
go back to reference Majid S, Tengrup I, Manjer J. Clinical assessment of axillary lymph nodes and tumor size in breast cancer compared with histopathological examination: a population-based analysis of 2537 women. World J Surg. 2013;37(1):67–71.PubMedCrossRef Majid S, Tengrup I, Manjer J. Clinical assessment of axillary lymph nodes and tumor size in breast cancer compared with histopathological examination: a population-based analysis of 2537 women. World J Surg. 2013;37(1):67–71.PubMedCrossRef
3.
go back to reference Chang JM, Leung JW, Moy L, Ha SM, Moon WK. Axillary nodal evaluation in breast cancer: state of the art. Radiology. 2020;295(3):500–15.PubMedCrossRef Chang JM, Leung JW, Moy L, Ha SM, Moon WK. Axillary nodal evaluation in breast cancer: state of the art. Radiology. 2020;295(3):500–15.PubMedCrossRef
4.
go back to reference Kijima Y, Yoshinaka H, Hirata M, Mizoguchi T, Ishigami S, Nakajo A, Arima H, Ueno S, Natsugoe S. Number of axillary lymph node metastases determined by preoperative ultrasound is related to prognosis in patients with breast cancer. Cancers. 2010;2(1):20–31.PubMedPubMedCentralCrossRef Kijima Y, Yoshinaka H, Hirata M, Mizoguchi T, Ishigami S, Nakajo A, Arima H, Ueno S, Natsugoe S. Number of axillary lymph node metastases determined by preoperative ultrasound is related to prognosis in patients with breast cancer. Cancers. 2010;2(1):20–31.PubMedPubMedCentralCrossRef
5.
go back to reference Alvarez S, Añorbe E, Alcorta P, López F, Alonso I, Cortés J. Role of sonography in the diagnosis of axillary lymph node metastases in breast cancer: a systematic review. Am J Roentgenol. 2006;186(5):1342–8.CrossRef Alvarez S, Añorbe E, Alcorta P, López F, Alonso I, Cortés J. Role of sonography in the diagnosis of axillary lymph node metastases in breast cancer: a systematic review. Am J Roentgenol. 2006;186(5):1342–8.CrossRef
6.
go back to reference Marino MA, Avendano D, Zapata P, Riedl CC, Pinker K. Lymph node imaging in patients with primary breast cancer: concurrent diagnostic tools. Oncologist. 2020;25(2):e231–42.PubMedCrossRef Marino MA, Avendano D, Zapata P, Riedl CC, Pinker K. Lymph node imaging in patients with primary breast cancer: concurrent diagnostic tools. Oncologist. 2020;25(2):e231–42.PubMedCrossRef
7.
go back to reference Gu J, Polley EC, Boughey JC, Fazzio RT, Fatemi M, Alizad A. Prediction of invasive breast cancer using mass characteristic frequency and elasticity in correlation with prognostic histologic features and immunohistochemical biomarkers. Ultrasound Med Biol. 2021;47(8):2193–201.PubMedPubMedCentralCrossRef Gu J, Polley EC, Boughey JC, Fazzio RT, Fatemi M, Alizad A. Prediction of invasive breast cancer using mass characteristic frequency and elasticity in correlation with prognostic histologic features and immunohistochemical biomarkers. Ultrasound Med Biol. 2021;47(8):2193–201.PubMedPubMedCentralCrossRef
8.
go back to reference Bayat M, Denis M, Gregory A, Mehrmohammadi M, Kumar V, Meixner D, Fazzio RT, Fatemi M, Alizad A. Diagnostic features of quantitative comb-push shear elastography for breast lesion differentiation. PLoS ONE. 2017;12(3): e0172801.PubMedPubMedCentralCrossRef Bayat M, Denis M, Gregory A, Mehrmohammadi M, Kumar V, Meixner D, Fazzio RT, Fatemi M, Alizad A. Diagnostic features of quantitative comb-push shear elastography for breast lesion differentiation. PLoS ONE. 2017;12(3): e0172801.PubMedPubMedCentralCrossRef
9.
go back to reference Denis M, Gregory A, Bayat M, Fazzio RT, Whaley DH, Ghosh K, Shah S, Fatemi M, Alizad A. Correlating tumor stiffness with immunohistochemical subtypes of breast cancers: prognostic value of comb-push ultrasound shear elastography for differentiating luminal subtypes. PLoS ONE. 2016;11(10): e0165003.PubMedPubMedCentralCrossRef Denis M, Gregory A, Bayat M, Fazzio RT, Whaley DH, Ghosh K, Shah S, Fatemi M, Alizad A. Correlating tumor stiffness with immunohistochemical subtypes of breast cancers: prognostic value of comb-push ultrasound shear elastography for differentiating luminal subtypes. PLoS ONE. 2016;11(10): e0165003.PubMedPubMedCentralCrossRef
10.
go back to reference Ng WL, Omar N, Ab Mumin N, Hamid MTR, Vijayananthan A, Rahmat K. Diagnostic accuracy of shear wave elastography as an adjunct tool in detecting axillary lymph nodes metastasis. Acad Radiol. 2022;29:S69–78.PubMedCrossRef Ng WL, Omar N, Ab Mumin N, Hamid MTR, Vijayananthan A, Rahmat K. Diagnostic accuracy of shear wave elastography as an adjunct tool in detecting axillary lymph nodes metastasis. Acad Radiol. 2022;29:S69–78.PubMedCrossRef
11.
go back to reference Gregory A, Denis M, Bayat M, Kumar V, Kim BH, Webb J, Nayak R, Adabi S, Meixner DD, Polley EC. Predictive value of comb-push ultrasound shear elastography for the differentiation of reactive and metastatic axillary lymph nodes: a preliminary investigation. PLoS ONE. 2020;15(1): e0226994.PubMedPubMedCentralCrossRef Gregory A, Denis M, Bayat M, Kumar V, Kim BH, Webb J, Nayak R, Adabi S, Meixner DD, Polley EC. Predictive value of comb-push ultrasound shear elastography for the differentiation of reactive and metastatic axillary lymph nodes: a preliminary investigation. PLoS ONE. 2020;15(1): e0226994.PubMedPubMedCentralCrossRef
12.
go back to reference Mansel RE, Fallowfield L, Kissin M, Goyal A, Newcombe RG, Dixon JM, Yiangou C, Horgan K, Bundred N, Monypenny I. Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC Trial. J Natl Cancer Inst. 2006;98(9):599–609.PubMedCrossRef Mansel RE, Fallowfield L, Kissin M, Goyal A, Newcombe RG, Dixon JM, Yiangou C, Horgan K, Bundred N, Monypenny I. Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC Trial. J Natl Cancer Inst. 2006;98(9):599–609.PubMedCrossRef
13.
go back to reference Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP, Costantino JP, Ashikaga T, Weaver DL, Mamounas EP, Jalovec LM. Sentinel-lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: overall survival findings from the NSABP B-32 randomised phase 3 trial. Lancet Oncol. 2010;11(10):927–33.PubMedPubMedCentralCrossRef Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP, Costantino JP, Ashikaga T, Weaver DL, Mamounas EP, Jalovec LM. Sentinel-lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: overall survival findings from the NSABP B-32 randomised phase 3 trial. Lancet Oncol. 2010;11(10):927–33.PubMedPubMedCentralCrossRef
14.
go back to reference Alkuwari E, Auger M. Accuracy of fine-needle aspiration cytology of axillary lymph nodes in breast cancer patients: a study of 115 cases with cytologic-histologic correlation. Cancer Cytopathol Interdiscip Int J Am Cancer Soc. 2008;114(2):89–93. Alkuwari E, Auger M. Accuracy of fine-needle aspiration cytology of axillary lymph nodes in breast cancer patients: a study of 115 cases with cytologic-histologic correlation. Cancer Cytopathol Interdiscip Int J Am Cancer Soc. 2008;114(2):89–93.
15.
go back to reference Vijayaraghavan GR, Vedantham S, Kataoka M, DeBenedectis C, Quinlan RM. The relevance of ultrasound imaging of suspicious axillary lymph nodes and fine-needle aspiration biopsy in the post-ACOSOG Z11 era in early breast cancer. Acad Radiol. 2017;24(3):308–15.PubMedCrossRef Vijayaraghavan GR, Vedantham S, Kataoka M, DeBenedectis C, Quinlan RM. The relevance of ultrasound imaging of suspicious axillary lymph nodes and fine-needle aspiration biopsy in the post-ACOSOG Z11 era in early breast cancer. Acad Radiol. 2017;24(3):308–15.PubMedCrossRef
16.
go back to reference Lee E, Koskimaki JE, Pandey NB, Popel AS. Inhibition of lymphangiogenesis and angiogenesis in breast tumor xenografts and lymph nodes by a peptide derived from transmembrane protein 45A. Neoplasia. 2013;15(2):112-IN116.PubMedPubMedCentralCrossRef Lee E, Koskimaki JE, Pandey NB, Popel AS. Inhibition of lymphangiogenesis and angiogenesis in breast tumor xenografts and lymph nodes by a peptide derived from transmembrane protein 45A. Neoplasia. 2013;15(2):112-IN116.PubMedPubMedCentralCrossRef
18.
go back to reference Nakamura Y, Yasuoka H, Tsujimoto M, Yang Q, Imabun S, Nakahara M, Nakao K, Nakamura M, Mori I, Kakudo K. Flt-4-positive vessel density correlates with vascular endothelial growth factor-d expression, nodal status, and prognosis in breast cancer. Clin Cancer Res. 2003;9(14):5313–7.PubMed Nakamura Y, Yasuoka H, Tsujimoto M, Yang Q, Imabun S, Nakahara M, Nakao K, Nakamura M, Mori I, Kakudo K. Flt-4-positive vessel density correlates with vascular endothelial growth factor-d expression, nodal status, and prognosis in breast cancer. Clin Cancer Res. 2003;9(14):5313–7.PubMed
19.
go back to reference Guidi AJ, Berry DA, Broadwater G, Perloff M, Norton L, Barcos MP, Hayes DF. Association of angiogenesis in lymph node metastases with outcome of breast cancer. J Natl Cancer Inst. 2000;92(6):486–92.PubMedCrossRef Guidi AJ, Berry DA, Broadwater G, Perloff M, Norton L, Barcos MP, Hayes DF. Association of angiogenesis in lymph node metastases with outcome of breast cancer. J Natl Cancer Inst. 2000;92(6):486–92.PubMedCrossRef
20.
go back to reference Pyakurel D, Karki S, Agrawal C. A study on microvascular density in breast carcinoma. J Pathol Nepal. 2014;4(7):570–5.CrossRef Pyakurel D, Karki S, Agrawal C. A study on microvascular density in breast carcinoma. J Pathol Nepal. 2014;4(7):570–5.CrossRef
21.
22.
23.
go back to reference Loiselle CR, Eby PR, Peacock S, Kim JN, Lehman CD. Dynamic contrast-enhanced magnetic resonance imaging and invasive breast cancer: primary lesion kinetics correlated with axillary lymph node extracapsular extension. J Magn Reson Imaging. 2011;33(1):96–101.PubMedCrossRef Loiselle CR, Eby PR, Peacock S, Kim JN, Lehman CD. Dynamic contrast-enhanced magnetic resonance imaging and invasive breast cancer: primary lesion kinetics correlated with axillary lymph node extracapsular extension. J Magn Reson Imaging. 2011;33(1):96–101.PubMedCrossRef
24.
go back to reference Yang WT, Chang J, Metreweli C. Patients with breast cancer: differences in color Doppler flow and gray-scale US features of benign and malignant axillary lymph nodes. Radiology. 2000;215(2):568–73.PubMedCrossRef Yang WT, Chang J, Metreweli C. Patients with breast cancer: differences in color Doppler flow and gray-scale US features of benign and malignant axillary lymph nodes. Radiology. 2000;215(2):568–73.PubMedCrossRef
26.
go back to reference Zare A, Shamshiripour P, Lotfi S, Shahin M, Rad VF, Moradi A-R, Hajiahmadi F, Ahmadvand D. Clinical theranostics applications of photo-acoustic imaging as a future prospect for cancer. J Control Release. 2022;351:805–33.PubMedCrossRef Zare A, Shamshiripour P, Lotfi S, Shahin M, Rad VF, Moradi A-R, Hajiahmadi F, Ahmadvand D. Clinical theranostics applications of photo-acoustic imaging as a future prospect for cancer. J Control Release. 2022;351:805–33.PubMedCrossRef
28.
go back to reference de Koekkoek-Doll PK, Roberti S, van den Brekel MW, Maas M, Smit L, Beets-Tan R, Castelijns J. Value of assessing peripheral vascularization with micro-flow imaging, resistive index and absent hilum sign as predictor for malignancy in lymph nodes in head and neck squamous cell carcinoma. Cancers. 2021;13(20):5071.PubMedPubMedCentralCrossRef de Koekkoek-Doll PK, Roberti S, van den Brekel MW, Maas M, Smit L, Beets-Tan R, Castelijns J. Value of assessing peripheral vascularization with micro-flow imaging, resistive index and absent hilum sign as predictor for malignancy in lymph nodes in head and neck squamous cell carcinoma. Cancers. 2021;13(20):5071.PubMedPubMedCentralCrossRef
29.
go back to reference Bayat M, Fatemi M, Alizad A. Background removal and vessel filtering of noncontrast ultrasound images of microvasculature. IEEE Trans Biomed Eng. 2018;66(3):831–42.PubMedPubMedCentralCrossRef Bayat M, Fatemi M, Alizad A. Background removal and vessel filtering of noncontrast ultrasound images of microvasculature. IEEE Trans Biomed Eng. 2018;66(3):831–42.PubMedPubMedCentralCrossRef
31.
go back to reference Ternifi R, Wang Y, Polley EC, Fazzio RT, Fatemi M, Alizad A. Quantitative biomarkers for cancer detection using contrast-free ultrasound high-definition microvessel imaging: fractal dimension, murray’s deviation, bifurcation angle & spatial vascularity pattern. IEEE Trans Med Imaging. 2021;40(12):3891–900.PubMedPubMedCentralCrossRef Ternifi R, Wang Y, Polley EC, Fazzio RT, Fatemi M, Alizad A. Quantitative biomarkers for cancer detection using contrast-free ultrasound high-definition microvessel imaging: fractal dimension, murray’s deviation, bifurcation angle & spatial vascularity pattern. IEEE Trans Med Imaging. 2021;40(12):3891–900.PubMedPubMedCentralCrossRef
32.
go back to reference Ghavami S, Bayat M, Fatemi M, Alizad A. Quantification of morphological features in non-contrast-enhanced ultrasound microvasculature imaging. IEEE Access. 2020;8:18925–37.PubMedPubMedCentralCrossRef Ghavami S, Bayat M, Fatemi M, Alizad A. Quantification of morphological features in non-contrast-enhanced ultrasound microvasculature imaging. IEEE Access. 2020;8:18925–37.PubMedPubMedCentralCrossRef
33.
go back to reference Kurti M, Sabeti S, Robinson KA, Scalise L, Larson NB, Fatemi M, Alizad A. Quantitative biomarkers derived from a novel contrast-free ultrasound high-definition microvessel imaging for distinguishing thyroid nodules. Cancers. 2023;15(6):1888.PubMedPubMedCentralCrossRef Kurti M, Sabeti S, Robinson KA, Scalise L, Larson NB, Fatemi M, Alizad A. Quantitative biomarkers derived from a novel contrast-free ultrasound high-definition microvessel imaging for distinguishing thyroid nodules. Cancers. 2023;15(6):1888.PubMedPubMedCentralCrossRef
35.
go back to reference Adabi S, Ghavami S, Fatemi M, Alizad A. Non-local based denoising framework for in vivo contrast-free ultrasound microvessel imaging. Sensors. 2019;19(2):245.PubMedPubMedCentralCrossRef Adabi S, Ghavami S, Fatemi M, Alizad A. Non-local based denoising framework for in vivo contrast-free ultrasound microvessel imaging. Sensors. 2019;19(2):245.PubMedPubMedCentralCrossRef
36.
go back to reference Nayak R, Kumar V, Webb J, Fatemi M, Alizad A. Non-invasive small vessel imaging of human thyroid using motion-corrected spatiotemporal clutter filtering. Ultrasound Med Biol. 2019;45(4):1010–8.PubMedPubMedCentralCrossRef Nayak R, Kumar V, Webb J, Fatemi M, Alizad A. Non-invasive small vessel imaging of human thyroid using motion-corrected spatiotemporal clutter filtering. Ultrasound Med Biol. 2019;45(4):1010–8.PubMedPubMedCentralCrossRef
37.
go back to reference Nayak R, Kumar V, Webb J, Gregory A, Fatemi M, Alizad A. Non-contrast agent based small vessel imaging of human thyroid using motion corrected power Doppler imaging. Sci Rep. 2018;8(1):1–15.CrossRef Nayak R, Kumar V, Webb J, Gregory A, Fatemi M, Alizad A. Non-contrast agent based small vessel imaging of human thyroid using motion corrected power Doppler imaging. Sci Rep. 2018;8(1):1–15.CrossRef
38.
go back to reference Nayak R, MacNeill J, Flores C, Webb J, Fatemi M, Alizad A. Quantitative assessment of ensemble coherency in contrast-free ultrasound microvasculature imaging. Med Phys. 2021;48(7):3540–58.PubMedCrossRef Nayak R, MacNeill J, Flores C, Webb J, Fatemi M, Alizad A. Quantitative assessment of ensemble coherency in contrast-free ultrasound microvasculature imaging. Med Phys. 2021;48(7):3540–58.PubMedCrossRef
39.
go back to reference Nayak R, Fatemi M, Alizad A. Adaptive background noise bias suppression in contrast-free ultrasound microvascular imaging. Phys Med Biol. 2019;64(24): 245015.PubMedPubMedCentralCrossRef Nayak R, Fatemi M, Alizad A. Adaptive background noise bias suppression in contrast-free ultrasound microvascular imaging. Phys Med Biol. 2019;64(24): 245015.PubMedPubMedCentralCrossRef
40.
go back to reference You QS, Chan JC, Ng AL, Choy BK, Shih KC, Cheung JJ, Wong JK, Shum JW, Ni MY, Lai JS. Macular vessel density measured with optical coherence tomography angiography and its associations in a large population-based study. Invest Ophthalmol Vis Sci. 2019;60(14):4830–7.PubMedCrossRef You QS, Chan JC, Ng AL, Choy BK, Shih KC, Cheung JJ, Wong JK, Shum JW, Ni MY, Lai JS. Macular vessel density measured with optical coherence tomography angiography and its associations in a large population-based study. Invest Ophthalmol Vis Sci. 2019;60(14):4830–7.PubMedCrossRef
41.
go back to reference Edgar LT, Hoying JB, Utzinger U, Underwood CJ, Krishnan L, Baggett BK, Maas SA, Guilkey JE, Weiss JA. Mechanical interaction of angiogenic microvessels with the extracellular matrix. J Biomech Eng. 2014;136(2): 021001.PubMedCrossRef Edgar LT, Hoying JB, Utzinger U, Underwood CJ, Krishnan L, Baggett BK, Maas SA, Guilkey JE, Weiss JA. Mechanical interaction of angiogenic microvessels with the extracellular matrix. J Biomech Eng. 2014;136(2): 021001.PubMedCrossRef
42.
go back to reference Sabo E, Boltenko A, Sova Y, Stein A, Kleinhaus S, Resnick MB. Microscopic analysis and significance of vascular architectural complexity in renal cell carcinoma. Clin Cancer Res. 2001;7(3):533–7.PubMed Sabo E, Boltenko A, Sova Y, Stein A, Kleinhaus S, Resnick MB. Microscopic analysis and significance of vascular architectural complexity in renal cell carcinoma. Clin Cancer Res. 2001;7(3):533–7.PubMed
43.
go back to reference Caresio C, Caballo M, Deandrea M, Garberoglio R, Mormile A, Rossetto R, Limone P, Molinari F. Quantitative analysis of thyroid tumors vascularity: a comparison between 3-D contrast-enhanced ultrasound and 3-D power Doppler on benign and malignant thyroid nodules. Med Phys. 2018;45(7):3173–84.PubMedCrossRef Caresio C, Caballo M, Deandrea M, Garberoglio R, Mormile A, Rossetto R, Limone P, Molinari F. Quantitative analysis of thyroid tumors vascularity: a comparison between 3-D contrast-enhanced ultrasound and 3-D power Doppler on benign and malignant thyroid nodules. Med Phys. 2018;45(7):3173–84.PubMedCrossRef
44.
go back to reference Li L, Mori S, Kodama M, Sakamoto M, Takahashi S, Kodama T. Enhanced sonographic imaging to diagnose lymph node metastasis: importance of blood vessel volume and density. Can Res. 2013;73(7):2082–92.CrossRef Li L, Mori S, Kodama M, Sakamoto M, Takahashi S, Kodama T. Enhanced sonographic imaging to diagnose lymph node metastasis: importance of blood vessel volume and density. Can Res. 2013;73(7):2082–92.CrossRef
45.
go back to reference Zhu J, Rowland EM, Harput S, Riemer K, Leow CH, Clark B, Cox K, Lim A, Christensen-Jeffries K, Zhang G. 3D super-resolution US imaging of rabbit lymph node vasculature in vivo by using microbubbles. Radiology. 2019;291(3):642–50.PubMedCrossRef Zhu J, Rowland EM, Harput S, Riemer K, Leow CH, Clark B, Cox K, Lim A, Christensen-Jeffries K, Zhang G. 3D super-resolution US imaging of rabbit lymph node vasculature in vivo by using microbubbles. Radiology. 2019;291(3):642–50.PubMedCrossRef
46.
go back to reference Kanoulas E, Butler M, Rowley C, Voulgaridou V, Diamantis K, Duncan WC, McNeilly A, Averkiou M, Wijkstra H, Mischi M. Super-resolution contrast-enhanced ultrasound methodology for the identification of in vivo vascular dynamics in 2D. Invest Radiol. 2019;54(8):500.PubMedPubMedCentralCrossRef Kanoulas E, Butler M, Rowley C, Voulgaridou V, Diamantis K, Duncan WC, McNeilly A, Averkiou M, Wijkstra H, Mischi M. Super-resolution contrast-enhanced ultrasound methodology for the identification of in vivo vascular dynamics in 2D. Invest Radiol. 2019;54(8):500.PubMedPubMedCentralCrossRef
47.
go back to reference Chappell JC, Wiley DM, Bautch VL. How blood vessel networks are made and measured. Cells Tissues Organs. 2012;195(1–2):94–107.PubMedCrossRef Chappell JC, Wiley DM, Bautch VL. How blood vessel networks are made and measured. Cells Tissues Organs. 2012;195(1–2):94–107.PubMedCrossRef
48.
go back to reference Gu J, Ternifi R, Larson NB, Carter JM, Boughey JC, Stan DL, Fazzio RT, Fatemi M, Alizad A. Hybrid high-definition microvessel imaging/shear wave elastography improves breast lesion characterization. Breast Cancer Res. 2022;24(1):1–13.PubMedPubMedCentralCrossRef Gu J, Ternifi R, Larson NB, Carter JM, Boughey JC, Stan DL, Fazzio RT, Fatemi M, Alizad A. Hybrid high-definition microvessel imaging/shear wave elastography improves breast lesion characterization. Breast Cancer Res. 2022;24(1):1–13.PubMedPubMedCentralCrossRef
49.
go back to reference Bullitt E, Zeng D, Gerig G, Aylward S, Joshi S, Smith JK, Lin W, Ewend MG. Vessel tortuosity and brain tumor malignancy: a blinded study1. Acad Radiol. 2005;12(10):1232–40.PubMedPubMedCentralCrossRef Bullitt E, Zeng D, Gerig G, Aylward S, Joshi S, Smith JK, Lin W, Ewend MG. Vessel tortuosity and brain tumor malignancy: a blinded study1. Acad Radiol. 2005;12(10):1232–40.PubMedPubMedCentralCrossRef
50.
go back to reference Konerding M, Fait E, Gaumann A. 3D microvascular architecture of pre-cancerous lesions and invasive carcinomas of the colon. Br J Cancer. 2001;84(10):1354–62.PubMedPubMedCentralCrossRef Konerding M, Fait E, Gaumann A. 3D microvascular architecture of pre-cancerous lesions and invasive carcinomas of the colon. Br J Cancer. 2001;84(10):1354–62.PubMedPubMedCentralCrossRef
51.
go back to reference Chen C, He ZC, Shi Y, Zhou W, Zhang X, Xiao HL, Wu HB, Yao XH, Luo WC, Cui YH. Microvascular fractal dimension predicts prognosis and response to chemotherapy in glioblastoma: an automatic image analysis study. Lab Investig. 2018;98(7):924–34.PubMedCrossRef Chen C, He ZC, Shi Y, Zhou W, Zhang X, Xiao HL, Wu HB, Yao XH, Luo WC, Cui YH. Microvascular fractal dimension predicts prognosis and response to chemotherapy in glioblastoma: an automatic image analysis study. Lab Investig. 2018;98(7):924–34.PubMedCrossRef
52.
go back to reference Gu J, Ternifi R, Sabeti S, Larson NB, Carter JM, Fazzio RT, Fatemi M, Alizad A. Volumetric imaging and morphometric analysis of breast tumor angiogenesis using a new contrast-free ultrasound technique: a feasibility study. Breast Cancer Res. 2022;24(1):1–15.PubMedPubMedCentralCrossRef Gu J, Ternifi R, Sabeti S, Larson NB, Carter JM, Fazzio RT, Fatemi M, Alizad A. Volumetric imaging and morphometric analysis of breast tumor angiogenesis using a new contrast-free ultrasound technique: a feasibility study. Breast Cancer Res. 2022;24(1):1–15.PubMedPubMedCentralCrossRef
Metadata
Title
Noninvasive prediction of axillary lymph node breast cancer metastasis using morphometric analysis of nodal tumor microvessels in a contrast-free ultrasound approach
Authors
Giulia Ferroni
Soroosh Sabeti
Tasneem Abdus-Shakur
Lorenzo Scalise
Jodi M. Carter
Robert T. Fazzio
Nicholas B. Larson
Mostafa Fatemi
Azra Alizad
Publication date
01-12-2023
Publisher
BioMed Central
Published in
Breast Cancer Research / Issue 1/2023
Electronic ISSN: 1465-542X
DOI
https://doi.org/10.1186/s13058-023-01670-z

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