Browse > Article
http://dx.doi.org/10.3807/COPP.2019.3.6.555

Changes in Breast-tumor Blood Flow in Response to Hypercapnia during Chemotherapy with Laser Speckle Flowmetry  

Kim, Hoonsup (Department of Biomedical Science & Engineering, Institute of Integrated Technology, Gwangju Institute of Science and Technology)
Lee, Youngjoo (Department of Biomedical Science & Engineering, Institute of Integrated Technology, Gwangju Institute of Science and Technology)
Lee, Songhyun (Center for BioMicrosystems, Brain Science Institute, Korea Institute of Science and Technology (KIST))
Kim, Jae Gwan (Department of Biomedical Science & Engineering, Institute of Integrated Technology, Gwangju Institute of Science and Technology)
Publication Information
Current Optics and Photonics / v.3, no.6, 2019 , pp. 555-565 More about this Journal
Abstract
Development of a biomarker for predicting tumor-treatment efficacy is a matter of great concern, to reduce time, medical expense, and effort in oncology therapy. In a preclinical study, we hypothesized that the blood-flow parameter based on laser speckle flowmetry (LSF) could be a potential indicator to estimate the efficacy of breast-cancer treatment. To verify this hypothesis, a 13762-MAT-B-III rat breast tumor was grown in a dorsal skinfold window chamber applied to a nude mouse, and the change in blood flow rate (BFR) - or the speckle flow index (SFI) is used together as the same meaning in this manuscript - was longitudinally monitored during tumor growth and metronomic cyclophosphamide treatment. Based on the daily LSF angiogram, several BFR parameters (baseline SFI, normalized SFI, and △rBFR) were compared to tumor size in the normal, treated, and untreated tumor groups. Despite the incomplete tumor treatment, we found that the daily changes in all BFR parameters tended to have partially positive correlation with tumor size. Moreover, we observed that the changes in baseline SFI and normalized SFI responded one day earlier than the tumor shrinkage during chemotherapy. However, daily variations in the hypercapnia-induced △rBFR lagged tumor shrinkage by one day. This study would contribute not only to evaluating tumor vascular response to treatment, but also to monitoring blood-flow-mediated diseases (in brain, skin, and retina) by using LSF in preclinical settings.
Keywords
Laser speckle imaging; Blood flow; Tumor growth assessment; Early prediction; Respiratory challenges;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 C. Cappelli, I. Pirola, E. Gandossi, F. Marini, A. Cristiano, C. Casella, D. Lombardi, B. Agosti, A. Ferlin, and M. Castellano, "Ultrasound microvascular blood flow evaluation: a new tool for the management of thyroid nodule?," Int. J. Endocrinol. 2019, 7874890 (2019).   DOI
2 D. Mustafi, A. Leinroth, X. Fan, E. Markiewicz, M. Zamora, J. Mueller, S. D. Conzen, and G. S. Karczmar, "Magnetic resonance angiography shows increased arterial blood supply associated with murine mammary cancer," Int. J. Biomed. Imaging 2019, 5987425 (2019).   DOI
3 M. R. Jochumsen, L. P. Tolbod, B. G. Pedersen, M. M. Nielsen, S. Hoyer, J. Frokiær, M. Borre, K. Bouchelouche, and J. Sorensen, "Quantitative tumor perfusion imaging with 82Rubidium-PET/CT in prostate cancer - analytical and clinical validation," J. Nucl. Med. 118, 219188 (2019).
4 T. Pedanekar, R. Kedare, and A. Sengupta, "Monitoring tumor progression by mapping skin microcirculation with laser Doppler flowmetry," Lasers Med. Sci. 34, 61-77 (2019).   DOI
5 G. Ramirez, A. R. Proctor, K. W. Jung, T. T. Wu, S. Han, R. R. Adams, J. Ren, D. K. Byun, K. S. Madden, E. B. Brown, T. H. Foster, P. Farzam, T. Durduran, and R. Choe, "Chemotherapeutic drug-specific alteration of microvascular blood flow in murine breast cancer as measured by diffuse correlation spectroscopy," Biomed. Opt. Express 7, 3610-3630 (2016).   DOI
6 C. Chen, K. H. Y. Cheng, R. Jakubovic, J. Jivraj, J. Ramjist, R. Deorajh, W. Gao, E. Barnes, L. Chin, and V. X. D. Yang, "High speed, wide velocity dynamic range Doppler optical coherence tomography (Part V): optimal utilization of multi-beam scanning for Doppler and speckle variance microvascular imaging," Opt. Express 25, 7761-7777 (2017).   DOI
7 O. Yang, D. J. Cuccia, and B. Choi, "Real-time blood flow visualization using the graphics processing unit," J. Biomed. Opt. 16, 016009 (2011).   DOI
8 S. C. Gnyawali, K. Blum, D. Pal, S. Ghatak, S. Khanna, S. Roy, and C. K. Sen, "Retooling laser speckle contrast analysis algorithm to enhance non-invasive high resolution laser speckle functional imaging of cutaneous microcirculation," Sci. Rep. 7, 41048 (2017).   DOI
9 S. J. Kirkpatrick, D. D. Duncan, and E. M. Wells-Gray, "Detrimental effects of speckle-pixel size matching in laser speckle contrast imaging," Opt. Lett. 33, 2886-2888 (2008).   DOI
10 A. Nadort, K. Kalkman, T. G. V. Leeuwen, and D. J. Faber, "Quantitative blood flow velocity imaging using laser speckle flowmetry," Sci. Rep. 6, 25258 (2016).   DOI
11 A. Edelstein, N. Amodaj, K. Hoover, R. Vale, and N. Stuurman, "Computer control of microscopes using ${\mu}Manager$," Curr. Protoc. Mol. Biol. 92, 14.20.1-14.20.17 (2010).
12 B. Choi, J. C. Ramirez-San-Juan, J. Lotfi, and J. S. Nelson, "Linear response range characterization and in vivo application of laser speckle imaging of blood flow dynamics," J. Biomed. Opt. 11, 041129 (2006).   DOI
13 H. Cheng and T. Q. Duong, "Simplified laser-speckle-imaging analysis method and its application to retinal blood flow imaging," Opt. Lett. 32, 2188-2190 (2007).   DOI
14 J. Pan, L. Cheng, X. Bi, X. Zhang, S. Liu, X. Bai, F. Li, and A. Z. Zhao, "Elevation of ${\omega}$-3 polyunsaturated fatty acids attenuates PTEN-deficiency induced endometrial cancer development through regulation of COX-2 and PGE2 production," Sci. Rep. 5, 14958 (2015).   DOI
15 T. J. Dunn, R. D. Braun, W. E. Rhemus, G. L. Rosner, T. W. Secomb, G. M. Tozer, D. J. Chaplin, and M. W. Dewhirst, "The effects of hyperoxic and hypercarbic gases on tumour blood flow," Br. J. Cancer 80, 117-126 (1999).   DOI
16 J. C. Ramirez-San-Juan, R. Ramos-Garcia, I. Guizar-Iturbide, G. Martinez-Niconoff, and B. Choi, "Impact of velocity distribution assumption on simplified laser speckle imaging equation," Opt. Express 16, 3197-3203 (2008).   DOI
17 A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, "Dynamic imaging of cerebral blood flow using laser speckle," J. Cereb. Blood Flow Metab. 21, 195-201 (2001).   DOI
18 R. Bonner and R. Nossal, "Model for laser Doppler measurements of blood flow in tissue," Appl. Opt. 20, 2097-2107 (1981).   DOI
19 J. K. Meisner, S. Sumer, K. P. Murrell, T. J. Higgins, and R. J. Price, "Laser speckle flowmetry method for measuring spatial and temporal hemodynamic alterations throughout large microvascular networks," Microcirculation 19, 619-631 (2012).   DOI
20 S. Lee, H. Jeong, M. Seong, and J. G. Kim, "Change of tumor vascular reactivity during tumor growth and postchemotherapy observed by near-infrared spectroscopy," J. Biomed. Opt. 22, 121603 (2017).   DOI
21 M. Neeman, H. Dafni, O. Bukhari, R. D. Braun, and M. W. Dewhirst, "In vivo BOLD contrast MRI mapping of subcutaneous vascular function and maturation: validation by intravital microscopy," Magn. Reson. Med. 45, 887-898 (2001).   DOI
22 J. W. Goodman, Statistical Optics (Wiley-Interscience, New York, 1985).
23 R. Abramovitch, H. Dafni, E. Smouha, L. E. Benjamin, and M. Neeman, "In vivo prediction of vascular susceptibility to vascular endothelial growth factor withdrawal: magnetic resonance imaging of C6 rat glioma in nude mice," Cancer Res. 59, 5012-5016 (1999).
24 R. K. Jain, "Determinants of tumor blood flow: a review," Cancer Res. 48, 2641-2658 (1988).
25 D. D. Duncan and S. J. Kirkpatrick, "Can laser speckle flowmetry be made a quantitative tool?," J. Opt. Soc. Am. A 25, 2088-2094 (2008).   DOI
26 M. N. Chonghaile, B. Higgins, and J. G. Laffey, "Permissive hypercapnia: role in protective lung ventilatory strategies," Curr. Opin. Crit. Care 11, 56-62 (2005).   DOI
27 W. Heeman, W. Steenbergen, G. M. van Dam, and E. C. Boerma, "Clinical applications of laser speckle contrast imaging: a review," J. Biomed. Opt. 24, 080901 (2019).
28 W. J. Aston, D. E. Hope, A. K. Nowak, B. W. Robinson, R. A. Lake, and W. J. Lesterhuis, "A systematic investigation of the maximum tolerated dose of cytotoxic chemotherapy with and without supportive care in mice," BMC Cancer 17, 684 (2017).   DOI
29 M. A. Davis, L. Gagnon, D. A. Boas, and A. K. Dunn, "Sensitivity of laser speckle contrast imaging to flow perturbations in the cortex," Biomed. Opt. Express 7, 759-775 (2016).   DOI
30 A. B. Parthasarathy, W. J. Tom, A. Gopal, X. Zhang, and A. K. Dunn, "Robust flow measurement with multi-exposure speckle imaging," Opt. Express 16, 1975-1989 (2008).   DOI
31 D. Shemesh, N. Bokobza, K. Rozenberg, T. Rosenzweig, and D. Abookasis, "Decreased cerebral blood flow and hemodynamic parameters during acute hyperglycemia in mice model observed by dual-wavelength speckle imaging," J. Biophotonics 12, e201900002 (2019).
32 A. Rauh, D. Henn, S. Nagel, A. Bigdeli, U. Kneser, and C. Hirche, "Continuous video-rate laser speckle imaging for intra- and postoperative cutaneous perfusion imaging of free flaps," J. Reconstr. Microsurg. 35, 489-498 (2019).   DOI
33 M. Chen, D. Wen, S. Huang, S. Gui, Z. Zhang, J. Lu, and P. Li, "Laser speckle contrast imaging of blood flow in the deep brain using microendoscopy," Opt. Lett. 43, 5627-5630 (2018).   DOI
34 C.-W. Chen, T. R. Blackwell, R. Naphas, P. T. Winnard JR, V. Raman, K. Glunde, and Y. Chen, "Development of needle-based microendoscopy for fluorescence molecular imaging of breast tumor models," J. Innov. Opt. Health Sci. 2, 343-352 (2009).   DOI
35 S. Ueda and T. Saeki, "Early therapeutic prediction based on tumor hemodynamic response imaging: clinical studies in breast cancer with time-resolved diffuse optical spectroscopy," Appl. Sci. 9, 3 (2019).   DOI
36 A. J. Moy, S. M. White, E. S. Indrawan, J. Lotfi, M. J. Nudelman, S. J. Costantini, N. Agarwal, W. Jia, K. M. Kelly, B. S. Sorg, and B. Choi, "Wide-field functional imaging of blood flow and hemoglobin oxygen saturation in the rodent dorsal window chamber," Microvasc. Res. 82, 199-209 (2011).   DOI
37 J. Tang, S. E. Erdener, B. Li, B. Fu, S. Sakadzic, S. A. Carp, J. Lee, and D. A. Boas, "Shear-induced diffusion of red blood cells measured with dynamic light scattering-optical coherence tomography," J. Biophotonics 11, e201700070 (2018).   DOI
38 S. Dziennis, J. Qin, L. Shi, and R. K. Wang, "Macro-tomicro cortical vascular imaging underlies regional differences in ischemic brain," Sci. Rep. 5, 10051 (2015).   DOI
39 R. L. Siegel, K. D. Miller, and A. Jemal, "Cancer statistics, 2019," Ca-Cancer J. Clin. 69, 7-34 (2019).   DOI
40 C. Zhou, R. Choe, N. Shah, T. Durduran, G. Yu, A. Durkin, D. Hsiang, R. Mehta, J. Butler, A. Cerussi, B. J. Tromberg, and A. G. Yodh, "Diffuse optical monitoring of blood flow and oxygenation in human breast cancer during early stages of neoadjuvant chemotherapy," J. Biomed. Opt. 12, 051903 (2007).   DOI
41 S. Lee and J. G. Kim, "Breast tumor hemodynamic response during a breath-hold as a biomarker to predict chemotherapeutic efficacy: preclinical study," J. Biomed. Opt. 23, 048001 (2018).
42 H. S. Yazdi, T. D. O'Sullivan, A. Leproux, B. Hill, A. Durkin, S. Telep, J. Lam, S. S. Yazdi, A. M. Police, R. M. Carroll, F. J. Combs, T. Stromberg, A. G. Yodh, and B. J. Tromberg, "Mapping breast cancer blood flow index, composition, and metabolism in a human subject using combined diffuse optical spectroscopic imaging and diffuse correlation spectroscopy," J. Biomed. Opt. 22, 045003 (2017).   DOI
43 H. Kim, T. J. Eom, and J. G. Kim, "Vascular morphometric changes during tumor growth and chemotherapy in a murine mammary tumor model using OCT angiography: a preliminary study," Curr. Opt. Photon. 3, 54-65 (2019).   DOI
44 X. Zhang, Y. Lin, and R. J. Gillies, "Tumor pH and Its Measurement," J. Nucl. Med. 51, 1167-1170 (2010).   DOI
45 A. Cerussi, N. Shah, D. Hsiang, A. Durkin, J. Butler, and B. J. Tromberg, "In vivo absorption, scattering, and physiologic properties of 58 malignant breast tumors determined by broadband diffuse optical spectroscopy," J. Biomed. Opt. 11, 044005 (2006).   DOI
46 J. Cochran, "Diffuse optical biomarkers of breast cancer," Ph. D. Dissertation, University of Pennsylvania, Pennsylvania (2018).