Blood flow dynamics during local photoreaction in a head and neck tumor model

Frontiers in Physics

Volumn 3, Issue MAR, 2015, Pages

  Rohrbach, Daniel J ^a   Tracy, Erin C ^a   Walker, Jessica ^a   Baumann, Heinz ^a   Sunar, Ulas ^a,b  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b University at Buffalo The State University of New York   (United States)

Author keywords

Biomarker; Blood flow; Diffuse correlation spectroscopy; Head and neck; Photodynamic therapy; STAT3 crosslinking; Vascular response

Indexed keywords

BLOOD; BLOOD VESSELS; DYNAMICS; HEMODYNAMICS; PHOTODYNAMIC THERAPY; PHOTOREACTIVITY;

BLOOD FLOW; BLOOD FLOW DYNAMICS; DIFFUSE CORRELATION SPECTROSCOPY; FLUENCE RATES; HEAD AND NECK; HEAD-AND-NECK TUMOR; PHOTOREACTIONS; STAT3 CROSSLINKING; TUMOR MODELS; VASCULAR RESPONSE;

TUMORS;

EID: 84946399160     PISSN: None     EISSN: 2296424X     Source Type: Journal    
DOI: 10.3389/fphy.2015.00013     Document Type: Article

References (62)

1. Amelink A, Sterenborg HJ, Roodenburg JL, Witjes MJ. Non-invasive measurement of the microvascular properties of non-dysplastic and dysplastic oral leukoplakias by use of optical spectroscopy. Oral Oncol. (2011) 47:1165-70. doi: 10.1016/j.oraloncology.2011.08.014
2. Poh CF, Zhang L, Anderson DW, Durham JS, Williams PM, Priddy RW, et al. Fluorescence visualization detection of field alterations in tumor margins of oral cancer patients. Clin Cancer Res. (2006) 12:6716-22. doi: 10.1158/1078-0432.CCR-06-1317
3. Wilson BC, Patterson MS. The physics, biophysics and technology of photodynamic therapy. Phys Med Biol. (2008) 53:R61-109. doi: 10.1088/0031-9155/53/9/R01
4. Grant WE, Hopper C, Speight PM, Macrobert AJ, Bown SG. Photodynamic therapy of malignant and premalignant lesions in patients with 'field cancerization' of the oral cavity. J Laryngol Otol. (1993) 107:1140-5
5. Karakullukcu B, Kanick SC, Aans JB, Sterenborg HJ, Tan IB, Amelink A, et al. Clinical feasibility of monitoring m-THPC mediated photodynamic therapy by means of fluorescence differential path-length spectroscopy. J Biophotonics (2011) 4:740-51. doi: 10.1002/jbio.201100051
6. Hopper C, Kubler A, Lewis H, Tan IB, Putnam G. mTHPC-mediated photodynamic therapy for early oral squamous cell carcinoma. Int J Cancer. (2004) 111:138-46. doi: 10.1002/ijc.20209
7. Quon H, Grossman CE, Finlay JC, Zhu TC, Clemmens CS, Malloy KM, et al. Photodynamic therapy in the management of pre-malignant head and neck mucosal dysplasia and microinvasive carcinoma. Photodiagnosis Photodyn Ther. (2011) 8:75-85. doi: 10.1016/j.pdpdt.2011.01.001
8. Tan IB, Oppelaar H, Ruevekamp MC, Veenhuizen RB, Timmers A, Stewart FA. The importance of in situ light dosimetry for photodynamic therapy of oral cavity tumors. Head Neck. (1999) 21:434-41
9. Oleinick NL, Morris RL, Belichenko I. The role of apoptosis in response to photodynamic therapy: what, where, why, and how. Photochem Photobiol Sci. (2002) 1:1-21. doi: 10.1039/b108586g
10. Chen B, Pogue BW, Goodwin IA, O'Hara JA, Wilmot CM, Hutchins JE, et al. Blood flow dynamics after photodynamic therapy with verteporfin in the RIF-1 tumor. Radiat Res. (2003) 160:452-9. doi: 10.1667/RR3059
11. van Duijnhoven FH, Aalbers RI, Rovers JP, Terpstra OT, Kuppen PJ. The immunological consequences of photodynamic treatment of cancer, a literature review. Immunobiology (2003) 207:105-13. doi: 10.1078/0171-2985-00221
12. Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res. (1989) 49:6449-65
13. Foster TH, Murant RS, Bryant RG, Knox RS, Gibson SL, Hilf R. Oxygen consumption and diffusion effects in photodynamic therapy. Radiat Res. (1991) 126:296-303. doi: 10.2307/3577919
14. Bargo PR, Prahl SA, Goodell TT, Sleven RA, Koval G, Blair G, et al. In vivo determination of optical properties of normal and tumor tissue with white light reflectance and an empirical light transport model during endoscopy. J Biomed Opt. (2005) 10:034018. doi: 10.1117/1.1921907
15. Jacques SL. Laser-tissue interactions. Photochemical, photothermal, and photomechanical. Surg Clin North Am. (1992) 72:531-58
16. Jacques SL. Light distributions from point, line and plane sources for photochemical reactions and fluorescence in turbid biological tissues. Photochem Photobiol. (1998) 67:23-32. doi: 10.1111/j.1751-1097.1998.tb05161.x
17. Busch TM, Wang HW, Wileyto EP, Yu G, Bunte RM. Increasing damage to tumor blood vessels during motexafin lutetium-PDT through use of low fluence rate. Radiat Res. (2010) 174:331-40. doi: 10.1667/RR2075.1
18. Henderson BW, Busch TM, Snyder JW. Fluence rate as a modulator of PDT mechanisms. Lasers Surg Med. (2006) 38:489-93. doi: 10.1002/lsm.20327
19. Madar-Balakirski N, Tempel-Brami C, Kalchenko V, Brenner O, Varon D, Scherz A, et al. Permanent occlusion of feeding arteries and draining veins in solid mouse tumors by vascular targeted photodynamic therapy (VTP) with Tookad. PLoS ONE (2010) 5:e10282. doi: 10.1371/journal.pone.0010282
20. Busch TM. Local physiological changes during photodynamic therapy. Lasers Surg Med. (2006) 38:494-9. doi: 10.1002/lsm.20355
21. Busch TM, Hahn SM, Evans SM, Koch CJ. Depletion of tumor oxygenation during photodynamic therapy: detection by the hypoxia marker EF3 [2-(2-nitroimidazol-1[H]-yl)-N-(3,3,3-trifluoropropyl)acetamide]. Cancer Res. (2000) 60:2636-42
22. Henderson BW, Daroqui C, Tracy E, Vaughan LA, Loewen GM, Cooper MT, et al. Cross-linking of signal transducer and activator of transcription 3-a molecular marker for the photodynamic reaction in cells and tumors. Clin Cancer Res. (2007) 13:3156-63. doi: 10.1158/1078-0432.CCR-06-2950
23. Mayr NA, Yuh WT, Magnotta VA, Ehrhardt JC, Wheeler JA, Sorosky JI, et al. Tumor perfusion studies using fast magnetic resonance imaging technique in advanced cervical cancer: a new noninvasive predictive assay. Int J Radiat Oncol Biol Phys. (1996) 36:623-33. doi: 10.1016/S0360-3016(97)85090-0
24. DeVries AF, Kremser C, Hein PA, Griebel J, Krezcy A, Ofner D, et al. Tumor microcirculation and diffusion predict therapy outcome for primary rectal carcinoma. Int J Radiat Oncol Biol Phys. (2003) 56:958-65. doi: 10.1016/S0360-3016(03)00208-6
25. Hermans R, Lambin P, Van den Bogaert W, Haustermans K, Van der Goten A, Baert AL. Non-invasive tumour perfusion measurement by dynamic CT: preliminary results. Radiother Oncol. (1997) 44:159-62. doi: 10.1016/S0167-8140(97)01913-0
26. Hermans R, Lambin P, Van der Goten A, Van den Bogaert W, Verbist B, Weltens C, et al. Tumoural perfusion as measured by dynamic computed tomography in head and neck carcinoma. Radiother Oncol. (1999) 53:105-11. doi: 10.1016/S0167-8140(99)00132-2
27. Lapointe D, Brasseur N, Cadorette J, La Madeleine C, Rodrigue S, van Lier JE, et al. High-resolution PET imaging for in vivo monitoring of tumor response after photodynamic therapy in mice. J Nucl Med. (1999) 40:876-82
28. Pirhonen JP, Grenman SA, Bredbacka AB, Bahado-Singh RO, Salmi TA. Effects of external radiotherapy on uterine blood flow in patients with advanced cervical carcinoma assessed by color Doppler ultrasonography. Cancer (1995) 76:67-71
29. Huilgol NG, Khan MM, Puniyani R. Capillary perfusion-a study in two groups of radiated patients for cancer of head and neck. Indian J Cancer (1995) 32:59-62
30. Enejder AM, af Klinteberg C, Wang I, Andersson-Engels S, Bendsoe N, Svanberg S, et al. Blood perfusion studies on basal cell carcinomas in conjunction with photodynamic therapy and cryotherapy employing laser-Doppler perfusion imaging. Acta Derm Venereol. (2000) 80:19-23. doi: 10.1080/000155500750012441
31. Liu DL, Svanberg K, Wang I, Andersson-Engels S, Svanberg S. Laser Doppler perfusion imaging: new technique for determination of perfusion and reperfusion of splanchnic organs and tumor tissue. Lasers Surg Med. (1997) 20:473-9
32. Wang I, Andersson-Engels S, Nilsson GE, Wardell K, Svanberg K. Superficial blood flow following photodynamic therapy of malignant non-melanoma skin tumours measured by laser Doppler perfusion imaging. Br J Dermatol. (1997) 136:184-9. doi: 10.1111/j.1365-2133.1997.tb14893.x
33. Khurana M, Moriyama EH, Mariampillai A, Wilson BC. Intravital high-resolution optical imaging of individual vessel response to photodynamic treatment. J Biomed Opt. (2008) 13:040502. doi: 10.1117/1.2965545
34. Becker TL, Paquette AD, Keymel KR, Henderson BW, Sunar U. Monitoring blood flow responses during topical ALA-PDT. Biomed Opt Express (2010) 2:123-30. doi: 10.1364/BOE.2.000123
35. Rohrbach DJ, Rigual N, Tracy E, Kowalczewski A, Keymel KL, Cooper MT, et al. Interlesion differences in the local photodynamic therapy response of oral cavity lesions assessed by diffuse optical spectroscopies. Biomed Opt Express (2012) 3:2142-53. doi: 10.1364/BOE.3.002142
36. Sunar U, Rohrbach D, Rigual N, Tracy E, Keymel K, Cooper MT, et al. Monitoring photobleaching and hemodynamic responses to HPPH-mediated photodynamic therapy of head and neck cancer: a case report. Opt Express (2010) 18:14969-78. doi: 10.1364/OE.18.014969
37. Yu G, Durduran T, Zhou C, Wang HW, Putt ME, Saunders HM, et al. Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy. Clin Cancer Res. (2005) 11:3543-52. doi: 10.1158/1078-0432.CCR-04-2582
38. Boas DA, Campbell LE, Yodh AG. Scattering and imaging with diffusing temporal field correlations. Phys Rev Lett. (1995) 75:1855-8. doi: 10.1103/PhysRevLett.75.1855
39. Boas DA, Yodh AG. Spatially varying dynamical properties of turbid media probed with diffusing temporal light correlation. J Opt Soc Am A (1997) 14:192-215. doi: 10.1364/JOSAA.14.000192
40. Mesquita RC, Durduran T, Yu G, Buckley EM, Kim MN, Zhou C, et al. Direct measurement of tissue blood flow and metabolism with diffuse optics. Philos. Trans A Math Phys Eng Sci. (2011) 369:4390-406. doi: 10.1098/rsta.2011.0232
41. Cheung C, Culver JP, Takahashi K, Greenberg JH, Yodh AG. In vivo cerebrovascular measurement combining diffuse near-infrared absorption and correlation spectroscopies. Phys Med Biol. (2001) 46:2053-65. doi: 10.1088/0031-9155/46/8/302
42. Culver JP, Durduran T, Furuya D, Cheung C, Greenberg JH, Yodh AG. Diffuse optical tomography of cerebral blood flow, oxygenation, and metabolism in rat during focal ischemia. J Cereb Blood Flow Metab. (2003) 23:911-24. doi: 10.1097/01.WCB.0000076703.71231.BB
43. Zhou C, Yu G, Furuya D, Greenberg J, Yodh A, Durduran T. Diffuse optical correlation tomography of cerebral blood flow during cortical spreading depression in rat brain. Opt Express (2006) 14:1125-44. doi: 10.1364/OE.14.001125
44. Sunar U, Makonnen S, Zhou C, Durduran T, Yu G, Wang HW, et al. Hemodynamic responses to antivascular therapy and ionizing radiation assessed by diffuse optical spectroscopies. Opt Express (2007) 15:15507-16. doi: 10.1364/OE.15.015507
45. Sunar U, Quon H, Durduran T, Zhang J, Du J, Zhou C, et al. Noninvasive diffuse optical measurement of blood flow and blood oxygenation for monitoring radiation therapy in patients with head and neck tumors: a pilot study. J Biomed Opt. (2006) 11:064021. doi: 10.1117/1.2397548
46. Carp SA, Dai GP, Boas DA, Franceschini MA, Kim YR. Validation of diffuse correlation spectroscopy measurements of rodent cerebral blood flow with simultaneous arterial spin labeling MRI; towards MRI-optical continuous cerebral metabolic monitoring. Biomed Opt Express (2010) 1:553-65. doi: 10.1364/BOE.1.000553
47. Li J, Dietsche G, Iftime D, Skipetrov SE, Maret G, Elbert T, et al. Noninvasive detection of functional brain activity with near-infrared diffusing-wave spectroscopy. J Biomed Opt. (2005) 10:44002. doi: 10.1117/1.2007987
48. Becker T. Irradiance: A Parameter Determining Oxygenation during Topical Photodynamic Therapy (PDT). Roswell Park Cancer Institute; State University of New York at Buffalo, Buffalo, NY (2010)
49. Cottrell WJ, Oseroff AR, Foster TH. Portable instrument that integrates irradiation with fluorescence and reflectance spectroscopies during clinical photodynamic therapy of cutaneous disease. Rev Sci Instrum. (2006) 77:064302. doi: 10.1063/1.2204617
50. Patterson MS, Andersson-Engels S, Wilson BC, Osei EK. Absorption spectroscopy in tissue-simulating materials: a theoretical and experimental study of photon paths. Appl Opt. (1995) 34:22-30. doi: 10.1364/AO.34.000022
51. Liu W, Oseroff AR, Baumann H. Photodynamic therapy causes cross-linking of signal transducer and activator of transcription proteins and attenuation of interleukin-6 cytokine responsiveness in epithelial cells. Cancer Res. (2004) 64:6579-87. doi: 10.1158/0008-5472.CAN-04-1580
52. Srivatsan A, Wang Y, Joshi P, Sajjad M, Chen Y, Liu C, et al. In vitro cellular uptake and dimerization of signal transducer and activator of transcription-3 (STAT3) identify the photosensitizing and imaging-potential of isomeric photosensitizers derived from chlorophyll-a and bacteriochlorophyll-a. J Med Chem. (2011) 54:6859-73. doi: 10.1021/jm200805y
53. Choi WW, Lewis MM, Lawson D, Yin-Goen Q, Birdsong GG, Cotsonis GA, et al. Angiogenic and lymphangiogenic microvessel density in breast carcinoma: correlation with clinicopathologic parameters and VEGF-family gene expression. Mod Pathol. (2005) 18:143-52. doi: 10.1038/modpathol.3800253
54. Bhuvaneswari R, Gan YY, Lucky SS, Chin WWL, Ali SM, Soo KC, et al. Molecular profiling of angiogenesis in hypericin mediated photodynamic therapy. Mol Cancer (2008) 7:56. doi: 10.1186/1476-4598-7-56
55. Middelburg TA, de Vijlder HC, de Bruijn HS, van der Ploeg-van den Heuvel A, Neumann HAM, de Haas ERM, et al. Topical photodynamic therapy using different porphyrin precursors leads to differences in vascular photosensitization and vascular damage in normal mouse skin. Photochem Photobiol. (2014) 90:896-902. doi: 10.1111/php.12271
56. Ren J, Li P, Zhao H, Chen D, Zhen J, Wang Y, et al. Assessment of tissue perfusion changes in port wine stains after vascular targeted photodynamic therapy: a short-term follow-up study. Lasers Med Sci. (2014) 29:781-8. doi: 10.1007/s10103-013-1420-4
57. Qiu H, Zhou Y, Gu Y, Ang Q, Zhao S, Wang Y, et al. Monitoring microcirculation changes in port wine stains during vascular targeted photodynamic therapy by laser speckle imaging. Photochem Photobiol. (2012) 88:978-84. doi: 10.1111/j.1751-1097.2012.01153.x
58. Gross S, Gilead A, Scherz A, Neeman M, Salomon Y. Monitoring photodynamic therapy of solid tumors online by BOLD-contrast MRI. Nat Med. (2003) 9:1327-31. doi: 10.1038/nm940
59. Standish BA, Lee KKC, Jin X, Mariampillai A, Munce NR, Wood MFG, et al. Interstitial doppler optical coherence tomography as a local tumor necrosis predictor in photodynamic therapy of prostatic carcinoma: an in vivo study. Cancer Res. (2008) 68:9987-95. doi: 10.1158/0008-5472.CAN-08-1128
60. Li H, Standish BA, Mariampillai A, Munce NR, Mao Y, Chiu S, et al. Feasibility of interstitial Doppler optical coherence tomography for in vivo detection of microvascular changes during photodynamic therapy. Lasers Surg Med. (2006) 38:754-61. doi: 10.1002/lsm.20387
61. Koudinova NV, Pinthus JH, Brandis A, Brenner O, Bendel P, Ramon J, et al. Photodynamic therapy with Pd-Bacteriopheophorbide (TOOKAD): successful in vivo treatment of human prostatic small cell carcinoma xenografts. Int J Cancer (2003) 104:782-9. doi: 10.1002/ijc.11002
62. Zilberstein J, Schreiber S, Bloemers MC, Bendel P, Neeman M, Schechtman E, et al. Antivascular treatment of solid melanoma tumors with bacteriochlorophyll-serine-based photodynamic therapy. Photochem Photobiol. (2001) 73:257-66. doi: 10.1562/0031-8655(2001)073<0257:ATOSMT>2.0.CO;2