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Virtual optical biopsy of human adipocytes with third harmonic generation microscopyCheng-Kun Tsai, Tzung-Dau Wang, Jong-Wei Lin, Ron-Bin Hsu, Lun-Zhang Guo, San-Tai Chen, and Tzu-Ming Liu »View Author Affiliations
Cheng-Kun Tsai,1
Tzung-Dau Wang,2,3,4,6
Jong-Wei Lin,2
Ron-Bin Hsu,5
Lun-Zhang Guo,1
San-Tai Chen,1
and Tzu-Ming Liu1,4,7
1Institute of Biomedical Engineering, National Taiwan University, Taipei 10617, Taiwan 2Division of Cardiology, Department of Internal Medicine, National Taiwan University Hospital and National Taiwan University College of Medicine, Taipei 10617, Taiwan 3Cardiovascular Center and Department of Internal Medicine, National Taiwan University Hospital Yun-Lin Branch, Yun-Lin County 64041, Taiwan 4Molecular Imaging Center, National Taiwan University, Taipei 10617, Taiwan 5Department of Surgery, National Taiwan University Hospital, Taipei 10048, Taiwan 6tdwang@ntu.edu.tw 7tmliu@ntu.edu.tw |
Biomedical Optics Express, Vol. 4, Issue 1, pp. 178-186 (2013)
http://dx.doi.org/10.1364/BOE.4.000178
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Abstract
Using the sectioning capability of third harmonic generation (THG) microscopy, we assessed the morphologic features of human adipocytes directly without fixation and labeling. At the plane of the largest cross-sectional area, both area-equivalent circular diameters (AECD) and perimeters of adipocytes were measured, and their statistical distributions were examined. We found, in patients with no cardiovascular risk factors, the average AECD of epicardial adipocytes were 70–90 μm with 11–17 μm standard deviations. In contrast, for patients with coronary artery disease, amounts of small-sized (AECD <40 µm) epicardial adipocytes were observed and the corresponding standard deviations of AECD were increased to 20–29 μm. Our results indicate that the THG tomography platform can be used to explore the histopathological features of adipocytes in clinical scenarios based on its superior resolution for virtual optical biopsy.
© 2012 OSA
OCIS Codes
(170.6900) Medical optics and biotechnology : Three-dimensional microscopy
(190.1900) Nonlinear optics : Diagnostic applications of nonlinear optics
ToC Category:
Microscopy
History
Original Manuscript: October 8, 2012
Revised Manuscript: November 19, 2012
Manuscript Accepted: November 21, 2012
Published: December 20, 2012
Citation
Cheng-Kun Tsai, Tzung-Dau Wang, Jong-Wei Lin, Ron-Bin Hsu, Lun-Zhang Guo, San-Tai Chen, and Tzu-Ming Liu, "Virtual optical biopsy of human adipocytes with third harmonic generation microscopy," Biomed. Opt. Express 4, 178-186 (2013)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-4-1-178
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References
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- T. McLaughlin, A. Sherman, P. Tsao, O. Gonzalez, G. Yee, C. Lamendola, G. M. Reaven, and S. W. Cushman, “Enhanced proportion of small adipose cells in insulin-resistant vs insulin-sensitive obese individuals implicates impaired adipogenesis,” Diabetologia50(8), 1707–1715 (2007). [CrossRef] [PubMed]
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- M. Dolinková, I. Dostálová, Z. Lacinová, D. Michalský, D. Haluzíková, M. Mráz, M. Kasalický, and M. Haluzík, “The endocrine profile of subcutaneous and visceral adipose tissue of obese patients,” Mol. Cell. Endocrinol.291(1-2), 63–70 (2008). [CrossRef] [PubMed]
- M. Dolinková, I. Dostálová, Z. Lacinová, D. Michalský, D. Haluzíková, M. Mráz, M. Kasalický, and M. Haluzík, “The endocrine profile of subcutaneous and visceral adipose tissue of obese patients,” Mol. Cell. Endocrinol.291(1-2), 63–70 (2008). [CrossRef] [PubMed]
- S. Eroglu, L. E. Sade, A. Yildirir, U. Bal, S. Ozbicer, A. S. Ozgul, H. Bozbas, A. Aydinalp, and H. Muderrisoglu, “Epicardial adipose tissue thickness by echocardiography is a marker for the presence and severity of coronary artery disease,” Nutr. Metab. Cardiovasc. Dis.19(3), 211–217 (2009). [CrossRef] [PubMed]
- C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, C. P. Lin, and X. S. Xie, “Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy,” Proc. Natl. Acad. Sci. U.S.A.102(46), 16807–16812 (2005). [CrossRef] [PubMed]
- J. N. Fain, A. K. Madan, M. L. Hiler, P. Cheema, and S. W. Bahouth, “Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans,” Endocrinology145(5), 2273–2282 (2004). [CrossRef] [PubMed]
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- S. P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante., “Obesity is associated with macrophage accumulation in adipose tissue,” J. Clin. Invest.112(12), 1796–1808 (2003). [PubMed]
- J. P. Bastard, M. Maachi, C. Lagathu, M. J. Kim, M. Caron, H. Vidal, J. Capeau, and B. Feve, “Recent advances in the relationship between obesity, inflammation, and insulin resistance,” Eur. Cytokine Netw.17(1), 4–12 (2006). [PubMed]
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- C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, C. P. Lin, and X. S. Xie, “Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy,” Proc. Natl. Acad. Sci. U.S.A.102(46), 16807–16812 (2005). [CrossRef] [PubMed]
- A. Liu, A. Sonmez, G. Yee, M. Bazuine, M. Arroyo, A. Sherman, T. McLaughlin, G. Reaven, S. Cushman, and P. Tsao, “Differential adipogenic and inflammatory properties of small adipocytes in Zucker Obese and Lean rats,” Diab. Vasc. Dis. Res.7(4), 311–318 (2010). [CrossRef] [PubMed]
- T. McLaughlin, A. Sherman, P. Tsao, O. Gonzalez, G. Yee, C. Lamendola, G. M. Reaven, and S. W. Cushman, “Enhanced proportion of small adipose cells in insulin-resistant vs insulin-sensitive obese individuals implicates impaired adipogenesis,” Diabetologia50(8), 1707–1715 (2007). [CrossRef] [PubMed]
- P. Wang, E. Mariman, J. Keijer, F. Bouwman, J. P. Noben, J. Robben, and J. Renes, “Profiling of the secreted proteins during 3T3-L1 adipocyte differentiation leads to the identification of novel adipokines,” Cell. Mol. Life Sci.61(18), 2405–2417 (2004). [CrossRef] [PubMed]
- P. Wang, E. Mariman, J. Keijer, F. Bouwman, J. P. Noben, J. Robben, and J. Renes, “Profiling of the secreted proteins during 3T3-L1 adipocyte differentiation leads to the identification of novel adipokines,” Cell. Mol. Life Sci.61(18), 2405–2417 (2004). [CrossRef] [PubMed]
- R. A. McLaughlin, L. Scolaro, P. Robbins, S. Hamza, C. Saunders, and D. D. Sampson, “Imaging of human lymph nodes using optical coherence tomography: potential for staging cancer,” Cancer Res.70(7), 2579–2584 (2010). [CrossRef] [PubMed]
- S. P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante., “Obesity is associated with macrophage accumulation in adipose tissue,” J. Clin. Invest.112(12), 1796–1808 (2003). [PubMed]
- A. A. Mahabadi, J. M. Massaro, G. A. Rosito, D. Levy, J. M. Murabito, P. A. Wolf, C. J. O’Donnell, C. S. Fox, and U. Hoffmann, “Association of pericardial fat, intrathoracic fat, and visceral abdominal fat with cardiovascular disease burden: the Framingham Heart Study,” Eur. Heart J.30(7), 850–856 (2009). [CrossRef] [PubMed]
- G. A. Rosito, J. M. Massaro, U. Hoffmann, F. L. Ruberg, A. A. Mahabadi, R. S. Vasan, C. J. O’Donnell, and C. S. Fox, “Pericardial fat, visceral abdominal fat, cardiovascular disease risk factors, and vascular calcification in a community-based sample: the Framingham Heart Study,” Circulation117(5), 605–613 (2008). [CrossRef] [PubMed]
- G. A. Rosito, J. M. Massaro, U. Hoffmann, F. L. Ruberg, A. A. Mahabadi, R. S. Vasan, C. J. O’Donnell, and C. S. Fox, “Pericardial fat, visceral abdominal fat, cardiovascular disease risk factors, and vascular calcification in a community-based sample: the Framingham Heart Study,” Circulation117(5), 605–613 (2008). [CrossRef] [PubMed]
- S. Eroglu, L. E. Sade, A. Yildirir, U. Bal, S. Ozbicer, A. S. Ozgul, H. Bozbas, A. Aydinalp, and H. Muderrisoglu, “Epicardial adipose tissue thickness by echocardiography is a marker for the presence and severity of coronary artery disease,” Nutr. Metab. Cardiovasc. Dis.19(3), 211–217 (2009). [CrossRef] [PubMed]
- R. A. McLaughlin, L. Scolaro, P. Robbins, S. Hamza, C. Saunders, and D. D. Sampson, “Imaging of human lymph nodes using optical coherence tomography: potential for staging cancer,” Cancer Res.70(7), 2579–2584 (2010). [CrossRef] [PubMed]
- D. M. Jaworski, O. Sideleva, H. M. Stradecki, G. D. Langlois, A. Habibovic, B. Satish, W. G. Tharp, J. Lausier, K. Larock, T. L. Jetton, M. Peshavaria, and R. E. Pratley, “Sexually dimorphic diet-induced insulin resistance in obese tissue inhibitor of metalloproteinase-2 (TIMP-2)-deficient mice,” Endocrinology152(4), 1300–1313 (2011). [CrossRef] [PubMed]
- R. A. McLaughlin, L. Scolaro, P. Robbins, S. Hamza, C. Saunders, and D. D. Sampson, “Imaging of human lymph nodes using optical coherence tomography: potential for staging cancer,” Cancer Res.70(7), 2579–2584 (2010). [CrossRef] [PubMed]
- R. A. McLaughlin, L. Scolaro, P. Robbins, S. Hamza, C. Saunders, and D. D. Sampson, “Imaging of human lymph nodes using optical coherence tomography: potential for staging cancer,” Cancer Res.70(7), 2579–2584 (2010). [CrossRef] [PubMed]
- H. Mori, A. D. Borowsky, R. Bhat, C. M. Ghajar, M. Seiki, and M. J. Bissell, “Laser scanning-based tissue autofluorescence/fluorescence imaging (LS-TAFI), a new technique for analysis of microanatomy in whole-mount tissues,” Am. J. Pathol.180(6), 2249–2256 (2012). [CrossRef] [PubMed]
- A. Liu, A. Sonmez, G. Yee, M. Bazuine, M. Arroyo, A. Sherman, T. McLaughlin, G. Reaven, S. Cushman, and P. Tsao, “Differential adipogenic and inflammatory properties of small adipocytes in Zucker Obese and Lean rats,” Diab. Vasc. Dis. Res.7(4), 311–318 (2010). [CrossRef] [PubMed]
- T. McLaughlin, A. Sherman, P. Tsao, O. Gonzalez, G. Yee, C. Lamendola, G. M. Reaven, and S. W. Cushman, “Enhanced proportion of small adipose cells in insulin-resistant vs insulin-sensitive obese individuals implicates impaired adipogenesis,” Diabetologia50(8), 1707–1715 (2007). [CrossRef] [PubMed]
- T.-D. Wang, W.-J. Lee, F.-Y. Shih, C.-H. Huang, W.-J. Chen, Y.-T. Lee, T. T.-F. Shih, and M.-F. Chen, “Association of epicardial adipose tissue with coronary atherosclerosis is region-specific and independent of conventional risk factors and intra-abdominal adiposity,” Atherosclerosis213(1), 279–287 (2010). [CrossRef] [PubMed]
- T.-D. Wang, W.-J. Lee, F.-Y. Shih, C.-H. Huang, W.-J. Chen, Y.-T. Lee, T. T.-F. Shih, and M.-F. Chen, “Association of epicardial adipose tissue with coronary atherosclerosis is region-specific and independent of conventional risk factors and intra-abdominal adiposity,” Atherosclerosis213(1), 279–287 (2010). [CrossRef] [PubMed]
- D. M. Jaworski, O. Sideleva, H. M. Stradecki, G. D. Langlois, A. Habibovic, B. Satish, W. G. Tharp, J. Lausier, K. Larock, T. L. Jetton, M. Peshavaria, and R. E. Pratley, “Sexually dimorphic diet-induced insulin resistance in obese tissue inhibitor of metalloproteinase-2 (TIMP-2)-deficient mice,” Endocrinology152(4), 1300–1313 (2011). [CrossRef] [PubMed]
- S. A. Boppart, W. Luo, D. L. Marks, and K. W. Singletary, “Optical coherence tomography: feasibility for basic research and image-guided surgery of breast cancer,” Breast Cancer Res. Treat.84(2), 85–97 (2004). [CrossRef] [PubMed]
- A. Liu, A. Sonmez, G. Yee, M. Bazuine, M. Arroyo, A. Sherman, T. McLaughlin, G. Reaven, S. Cushman, and P. Tsao, “Differential adipogenic and inflammatory properties of small adipocytes in Zucker Obese and Lean rats,” Diab. Vasc. Dis. Res.7(4), 311–318 (2010). [CrossRef] [PubMed]
- G. S. Hotamisligil, P. Arner, J. F. Caro, R. L. Atkinson, and B. M. Spiegelman, “Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance,” J. Clin. Invest.95(5), 2409–2415 (1995). [CrossRef] [PubMed]
- D. M. Jaworski, O. Sideleva, H. M. Stradecki, G. D. Langlois, A. Habibovic, B. Satish, W. G. Tharp, J. Lausier, K. Larock, T. L. Jetton, M. Peshavaria, and R. E. Pratley, “Sexually dimorphic diet-induced insulin resistance in obese tissue inhibitor of metalloproteinase-2 (TIMP-2)-deficient mice,” Endocrinology152(4), 1300–1313 (2011). [CrossRef] [PubMed]
- M.-R. Tsai, S.-Y. Chen, D.-B. Shieh, P.-J. Lou, and C.-K. Sun, “In vivo optical virtual biopsy of human oral mucosa with harmonic generation microscopy,” Biomed. Opt. Express2(8), 2317–2328 (2011). [CrossRef] [PubMed]
- S.-Y. Chen, S.-U. Chen, H.-Y. Wu, W.-J. Lee, Y.-H. Liao, and C.-K. Sun, “In vivo virtual biopsy of human skin by using noninvasive higher harmonic generation microscopy,” IEEE J. Sel. Top. Quantum Electron.16(3), 478–492 (2010). [CrossRef]
- S.-Y. Chen, H.-Y. Wu, and C.-K. Sun, “In vivo harmonic generation biopsy of human skin,” J. Biomed. Opt.14(6), 060505 (2009). [CrossRef] [PubMed]
- C.-S. Hsieh, C.-Y. Ko, S.-Y. Chen, T.-M. Liu, J.-S. Wu, C.-H. Hu, and C.-K. Sun, “In vivo long-term continuous observation of gene expression in zebrafish embryo nerve systems by using harmonic generation microscopy and morphant technology,” J. Biomed. Opt.13(6), 064041 (2008). [CrossRef] [PubMed]
- S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, H.-J. Tsai, and C.-K. Sun, “In vivo developmental biology study using noninvasive multi-harmonic generation microscopy,” Opt. Express11(23), 3093–3099 (2003). [CrossRef] [PubMed]
- D. M. Jaworski, O. Sideleva, H. M. Stradecki, G. D. Langlois, A. Habibovic, B. Satish, W. G. Tharp, J. Lausier, K. Larock, T. L. Jetton, M. Peshavaria, and R. E. Pratley, “Sexually dimorphic diet-induced insulin resistance in obese tissue inhibitor of metalloproteinase-2 (TIMP-2)-deficient mice,” Endocrinology152(4), 1300–1313 (2011). [CrossRef] [PubMed]
- H.-C. Lee, W.-A. Tseng, F.-Y. Lo, T.-M. Liu, and H.-J. Tsai, “FoxD5 mediates anterior-posterior polarity through upstream modulator Fgf signaling during zebrafish somitogenesis,” Dev. Biol.336(2), 232–245 (2009). [CrossRef] [PubMed]
- S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, H.-J. Tsai, and C.-K. Sun, “In vivo developmental biology study using noninvasive multi-harmonic generation microscopy,” Opt. Express11(23), 3093–3099 (2003). [CrossRef] [PubMed]
- C. Zhou, D. W. Cohen, Y. Wang, H.-C. Lee, A. E. Mondelblatt, T.-H. Tsai, A. D. Aguirre, J. G. Fujimoto, and J. L. Connolly, “Integrated optical coherence tomography and microscopy for ex vivo multiscale evaluation of human breast tissues,” Cancer Res.70(24), 10071–10079 (2010). [CrossRef] [PubMed]
- S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, H.-J. Tsai, and C.-K. Sun, “In vivo developmental biology study using noninvasive multi-harmonic generation microscopy,” Opt. Express11(23), 3093–3099 (2003). [CrossRef] [PubMed]
- A. Liu, A. Sonmez, G. Yee, M. Bazuine, M. Arroyo, A. Sherman, T. McLaughlin, G. Reaven, S. Cushman, and P. Tsao, “Differential adipogenic and inflammatory properties of small adipocytes in Zucker Obese and Lean rats,” Diab. Vasc. Dis. Res.7(4), 311–318 (2010). [CrossRef] [PubMed]
- T. McLaughlin, A. Sherman, P. Tsao, O. Gonzalez, G. Yee, C. Lamendola, G. M. Reaven, and S. W. Cushman, “Enhanced proportion of small adipose cells in insulin-resistant vs insulin-sensitive obese individuals implicates impaired adipogenesis,” Diabetologia50(8), 1707–1715 (2007). [CrossRef] [PubMed]
- H.-C. Lee, W.-A. Tseng, F.-Y. Lo, T.-M. Liu, and H.-J. Tsai, “FoxD5 mediates anterior-posterior polarity through upstream modulator Fgf signaling during zebrafish somitogenesis,” Dev. Biol.336(2), 232–245 (2009). [CrossRef] [PubMed]
- G. A. Rosito, J. M. Massaro, U. Hoffmann, F. L. Ruberg, A. A. Mahabadi, R. S. Vasan, C. J. O’Donnell, and C. S. Fox, “Pericardial fat, visceral abdominal fat, cardiovascular disease risk factors, and vascular calcification in a community-based sample: the Framingham Heart Study,” Circulation117(5), 605–613 (2008). [CrossRef] [PubMed]
- J. P. Bastard, M. Maachi, C. Lagathu, M. J. Kim, M. Caron, H. Vidal, J. Capeau, and B. Feve, “Recent advances in the relationship between obesity, inflammation, and insulin resistance,” Eur. Cytokine Netw.17(1), 4–12 (2006). [PubMed]
- B. L. Wajchenberg, “Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome,” Endocr. Rev.21(6), 697–738 (2000). [CrossRef] [PubMed]
- P. Wang, E. Mariman, J. Keijer, F. Bouwman, J. P. Noben, J. Robben, and J. Renes, “Profiling of the secreted proteins during 3T3-L1 adipocyte differentiation leads to the identification of novel adipokines,” Cell. Mol. Life Sci.61(18), 2405–2417 (2004). [CrossRef] [PubMed]
- T.-D. Wang, W.-J. Lee, F.-Y. Shih, C.-H. Huang, W.-J. Chen, Y.-T. Lee, T. T.-F. Shih, and M.-F. Chen, “Association of epicardial adipose tissue with coronary atherosclerosis is region-specific and independent of conventional risk factors and intra-abdominal adiposity,” Atherosclerosis213(1), 279–287 (2010). [CrossRef] [PubMed]
- C. Zhou, D. W. Cohen, Y. Wang, H.-C. Lee, A. E. Mondelblatt, T.-H. Tsai, A. D. Aguirre, J. G. Fujimoto, and J. L. Connolly, “Integrated optical coherence tomography and microscopy for ex vivo multiscale evaluation of human breast tissues,” Cancer Res.70(24), 10071–10079 (2010). [CrossRef] [PubMed]
- S. P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante., “Obesity is associated with macrophage accumulation in adipose tissue,” J. Clin. Invest.112(12), 1796–1808 (2003). [PubMed]
- K. E. Wellen and G. S. Hotamisligil, “Obesity-induced inflammatory changes in adipose tissue,” J. Clin. Invest.112(12), 1785–1788 (2003). [PubMed]
- A. A. Mahabadi, J. M. Massaro, G. A. Rosito, D. Levy, J. M. Murabito, P. A. Wolf, C. J. O’Donnell, C. S. Fox, and U. Hoffmann, “Association of pericardial fat, intrathoracic fat, and visceral abdominal fat with cardiovascular disease burden: the Framingham Heart Study,” Eur. Heart J.30(7), 850–856 (2009). [CrossRef] [PubMed]
- S.-Y. Chen, S.-U. Chen, H.-Y. Wu, W.-J. Lee, Y.-H. Liao, and C.-K. Sun, “In vivo virtual biopsy of human skin by using noninvasive higher harmonic generation microscopy,” IEEE J. Sel. Top. Quantum Electron.16(3), 478–492 (2010). [CrossRef]
- S.-Y. Chen, H.-Y. Wu, and C.-K. Sun, “In vivo harmonic generation biopsy of human skin,” J. Biomed. Opt.14(6), 060505 (2009). [CrossRef] [PubMed]
- C.-S. Hsieh, C.-Y. Ko, S.-Y. Chen, T.-M. Liu, J.-S. Wu, C.-H. Hu, and C.-K. Sun, “In vivo long-term continuous observation of gene expression in zebrafish embryo nerve systems by using harmonic generation microscopy and morphant technology,” J. Biomed. Opt.13(6), 064041 (2008). [CrossRef] [PubMed]
- C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, C. P. Lin, and X. S. Xie, “Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy,” Proc. Natl. Acad. Sci. U.S.A.102(46), 16807–16812 (2005). [CrossRef] [PubMed]
- A. Liu, A. Sonmez, G. Yee, M. Bazuine, M. Arroyo, A. Sherman, T. McLaughlin, G. Reaven, S. Cushman, and P. Tsao, “Differential adipogenic and inflammatory properties of small adipocytes in Zucker Obese and Lean rats,” Diab. Vasc. Dis. Res.7(4), 311–318 (2010). [CrossRef] [PubMed]
- T. McLaughlin, A. Sherman, P. Tsao, O. Gonzalez, G. Yee, C. Lamendola, G. M. Reaven, and S. W. Cushman, “Enhanced proportion of small adipose cells in insulin-resistant vs insulin-sensitive obese individuals implicates impaired adipogenesis,” Diabetologia50(8), 1707–1715 (2007). [CrossRef] [PubMed]
- S. Eroglu, L. E. Sade, A. Yildirir, U. Bal, S. Ozbicer, A. S. Ozgul, H. Bozbas, A. Aydinalp, and H. Muderrisoglu, “Epicardial adipose tissue thickness by echocardiography is a marker for the presence and severity of coronary artery disease,” Nutr. Metab. Cardiovasc. Dis.19(3), 211–217 (2009). [CrossRef] [PubMed]
- C. Zhou, D. W. Cohen, Y. Wang, H.-C. Lee, A. E. Mondelblatt, T.-H. Tsai, A. D. Aguirre, J. G. Fujimoto, and J. L. Connolly, “Integrated optical coherence tomography and microscopy for ex vivo multiscale evaluation of human breast tissues,” Cancer Res.70(24), 10071–10079 (2010). [CrossRef] [PubMed]
- Z. Huang, S. Zhuo, J. Chen, R. Chen, and X. Jiang, “Multiphoton microscopic imaging of adipose tissue based on second-harmonic generation and two-photon excited fluorescence,” Scanning30(6), 452–456 (2008). [CrossRef] [PubMed]
Am. J. Pathol.
- H. Mori, A. D. Borowsky, R. Bhat, C. M. Ghajar, M. Seiki, and M. J. Bissell, “Laser scanning-based tissue autofluorescence/fluorescence imaging (LS-TAFI), a new technique for analysis of microanatomy in whole-mount tissues,” Am. J. Pathol.180(6), 2249–2256 (2012). [CrossRef] [PubMed]
Arteriosclerosis
- P. Björntorp, ““Portal” adipose tissue as a generator of risk factors for cardiovascular disease and diabetes,” Arteriosclerosis10(4), 493–496 (1990). [CrossRef] [PubMed]
Atherosclerosis
- T.-D. Wang, W.-J. Lee, F.-Y. Shih, C.-H. Huang, W.-J. Chen, Y.-T. Lee, T. T.-F. Shih, and M.-F. Chen, “Association of epicardial adipose tissue with coronary atherosclerosis is region-specific and independent of conventional risk factors and intra-abdominal adiposity,” Atherosclerosis213(1), 279–287 (2010). [CrossRef] [PubMed]
Biomed. Opt. Express
- M.-R. Tsai, S.-Y. Chen, D.-B. Shieh, P.-J. Lou, and C.-K. Sun, “In vivo optical virtual biopsy of human oral mucosa with harmonic generation microscopy,” Biomed. Opt. Express2(8), 2317–2328 (2011). [CrossRef] [PubMed]
- C.-K. Tsai, Y.-S. Chen, P.-C. Wu, T.-Y. Hsieh, H.-W. Liu, C.-Y. Yeh, W.-L. Lin, J.-S. Chia, and T.-M. Liu, “Imaging granularity of leukocytes with third harmonic generation microscopy,” Biomed. Opt. Express3(9), 2234–2243 (2012). [CrossRef] [PubMed]
- C.-K. Chen and T.-M. Liu, “Imaging morphodynamics of human blood cells in vivo with video-rate third harmonic generation microscopy,” Biomed. Opt. Express3(11), 2860–2865 (2012). [CrossRef] [PubMed]
Breast Cancer Res. Treat.
- S. A. Boppart, W. Luo, D. L. Marks, and K. W. Singletary, “Optical coherence tomography: feasibility for basic research and image-guided surgery of breast cancer,” Breast Cancer Res. Treat.84(2), 85–97 (2004). [CrossRef] [PubMed]
Cancer Res.
- C. Zhou, D. W. Cohen, Y. Wang, H.-C. Lee, A. E. Mondelblatt, T.-H. Tsai, A. D. Aguirre, J. G. Fujimoto, and J. L. Connolly, “Integrated optical coherence tomography and microscopy for ex vivo multiscale evaluation of human breast tissues,” Cancer Res.70(24), 10071–10079 (2010). [CrossRef] [PubMed]
- R. A. McLaughlin, L. Scolaro, P. Robbins, S. Hamza, C. Saunders, and D. D. Sampson, “Imaging of human lymph nodes using optical coherence tomography: potential for staging cancer,” Cancer Res.70(7), 2579–2584 (2010). [CrossRef] [PubMed]
Cell. Mol. Life Sci.
- P. Wang, E. Mariman, J. Keijer, F. Bouwman, J. P. Noben, J. Robben, and J. Renes, “Profiling of the secreted proteins during 3T3-L1 adipocyte differentiation leads to the identification of novel adipokines,” Cell. Mol. Life Sci.61(18), 2405–2417 (2004). [CrossRef] [PubMed]
Circulation
- G. A. Rosito, J. M. Massaro, U. Hoffmann, F. L. Ruberg, A. A. Mahabadi, R. S. Vasan, C. J. O’Donnell, and C. S. Fox, “Pericardial fat, visceral abdominal fat, cardiovascular disease risk factors, and vascular calcification in a community-based sample: the Framingham Heart Study,” Circulation117(5), 605–613 (2008). [CrossRef] [PubMed]
Dev. Biol.
- H.-C. Lee, W.-A. Tseng, F.-Y. Lo, T.-M. Liu, and H.-J. Tsai, “FoxD5 mediates anterior-posterior polarity through upstream modulator Fgf signaling during zebrafish somitogenesis,” Dev. Biol.336(2), 232–245 (2009). [CrossRef] [PubMed]
Diab. Vasc. Dis. Res.
- A. Liu, A. Sonmez, G. Yee, M. Bazuine, M. Arroyo, A. Sherman, T. McLaughlin, G. Reaven, S. Cushman, and P. Tsao, “Differential adipogenic and inflammatory properties of small adipocytes in Zucker Obese and Lean rats,” Diab. Vasc. Dis. Res.7(4), 311–318 (2010). [CrossRef] [PubMed]
Diabetologia
- T. McLaughlin, A. Sherman, P. Tsao, O. Gonzalez, G. Yee, C. Lamendola, G. M. Reaven, and S. W. Cushman, “Enhanced proportion of small adipose cells in insulin-resistant vs insulin-sensitive obese individuals implicates impaired adipogenesis,” Diabetologia50(8), 1707–1715 (2007). [CrossRef] [PubMed]
Endocr. Rev.
- B. L. Wajchenberg, “Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome,” Endocr. Rev.21(6), 697–738 (2000). [CrossRef] [PubMed]
Endocrinology
- D. M. Jaworski, O. Sideleva, H. M. Stradecki, G. D. Langlois, A. Habibovic, B. Satish, W. G. Tharp, J. Lausier, K. Larock, T. L. Jetton, M. Peshavaria, and R. E. Pratley, “Sexually dimorphic diet-induced insulin resistance in obese tissue inhibitor of metalloproteinase-2 (TIMP-2)-deficient mice,” Endocrinology152(4), 1300–1313 (2011). [CrossRef] [PubMed]
- J. N. Fain, A. K. Madan, M. L. Hiler, P. Cheema, and S. W. Bahouth, “Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans,” Endocrinology145(5), 2273–2282 (2004). [CrossRef] [PubMed]
Eur. Cytokine Netw.
- J. P. Bastard, M. Maachi, C. Lagathu, M. J. Kim, M. Caron, H. Vidal, J. Capeau, and B. Feve, “Recent advances in the relationship between obesity, inflammation, and insulin resistance,” Eur. Cytokine Netw.17(1), 4–12 (2006). [PubMed]
Eur. Heart J.
- A. A. Mahabadi, J. M. Massaro, G. A. Rosito, D. Levy, J. M. Murabito, P. A. Wolf, C. J. O’Donnell, C. S. Fox, and U. Hoffmann, “Association of pericardial fat, intrathoracic fat, and visceral abdominal fat with cardiovascular disease burden: the Framingham Heart Study,” Eur. Heart J.30(7), 850–856 (2009). [CrossRef] [PubMed]
IEEE J. Sel. Top. Quantum Electron.
- S.-Y. Chen, S.-U. Chen, H.-Y. Wu, W.-J. Lee, Y.-H. Liao, and C.-K. Sun, “In vivo virtual biopsy of human skin by using noninvasive higher harmonic generation microscopy,” IEEE J. Sel. Top. Quantum Electron.16(3), 478–492 (2010). [CrossRef]
Int. J. Biochem. Cell Biol.
- P. Mathieu, P. Pibarot, E. Larose, P. Poirier, A. Marette, and J. P. Després, “Visceral obesity and the heart,” Int. J. Biochem. Cell Biol.40(5), 821–836 (2008). [CrossRef] [PubMed]
J. Allergy Clin. Immunol.
- G. Fantuzzi, “Adipose tissue, adipokines, and inflammation,” J. Allergy Clin. Immunol.115(5), 911–919, quiz 920 (2005). [CrossRef] [PubMed]
J. Biomed. Opt.
- S.-Y. Chen, H.-Y. Wu, and C.-K. Sun, “In vivo harmonic generation biopsy of human skin,” J. Biomed. Opt.14(6), 060505 (2009). [CrossRef] [PubMed]
- C.-S. Hsieh, C.-Y. Ko, S.-Y. Chen, T.-M. Liu, J.-S. Wu, C.-H. Hu, and C.-K. Sun, “In vivo long-term continuous observation of gene expression in zebrafish embryo nerve systems by using harmonic generation microscopy and morphant technology,” J. Biomed. Opt.13(6), 064041 (2008). [CrossRef] [PubMed]
J. Clin. Invest.
- G. S. Hotamisligil, P. Arner, J. F. Caro, R. L. Atkinson, and B. M. Spiegelman, “Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance,” J. Clin. Invest.95(5), 2409–2415 (1995). [CrossRef] [PubMed]
- K. E. Wellen and G. S. Hotamisligil, “Obesity-induced inflammatory changes in adipose tissue,” J. Clin. Invest.112(12), 1785–1788 (2003). [PubMed]
- S. P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante., “Obesity is associated with macrophage accumulation in adipose tissue,” J. Clin. Invest.112(12), 1796–1808 (2003). [PubMed]
Mol. Cell. Endocrinol.
- M. Dolinková, I. Dostálová, Z. Lacinová, D. Michalský, D. Haluzíková, M. Mráz, M. Kasalický, and M. Haluzík, “The endocrine profile of subcutaneous and visceral adipose tissue of obese patients,” Mol. Cell. Endocrinol.291(1-2), 63–70 (2008). [CrossRef] [PubMed]
Nutr. Metab. Cardiovasc. Dis.
- S. Eroglu, L. E. Sade, A. Yildirir, U. Bal, S. Ozbicer, A. S. Ozgul, H. Bozbas, A. Aydinalp, and H. Muderrisoglu, “Epicardial adipose tissue thickness by echocardiography is a marker for the presence and severity of coronary artery disease,” Nutr. Metab. Cardiovasc. Dis.19(3), 211–217 (2009). [CrossRef] [PubMed]
Opt. Express
- S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, H.-J. Tsai, and C.-K. Sun, “In vivo developmental biology study using noninvasive multi-harmonic generation microscopy,” Opt. Express11(23), 3093–3099 (2003). [CrossRef] [PubMed]
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Scanning
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