Abstract

We have developed dynamic tumor vascular phantoms and utilized them to investigate the biphasic behavior of increases in light absorption, which is directly associated with oxygenated hemoglobin concentration that was observed in vivo from rat breast tumor experiments during carbogen∕oxygen inhalation. The experimental setup for the phantom study included a continuous-wave, multichannel, near-infrared spectroscopy (NIRS) system and syringe pumps to drive the simulated blood through the dynamic vascular phantoms. The results from such phantom experiments clearly show that the two time constants observed in tumor oxygenation dynamics in vivo can result from two different perfusion rates or two different blood flow velocities. We provide experimental support for our previous hypothesis: the biphasic tumor hemodynamic feature stems from a well-perfused and poorly perfused region that could be detected with the two time constants of the NIRS signals. With a multichannel approach, noninvasive NIRS measurements may have useful and prognostic values to quantify the therapeutic effects of cancer treatments.

© 2008 Optical Society of America

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2005 (7)

N. Kawashima, K. Nakazawa, and M. Akai, "Muscle oxygenation of the paralyzed lower limb in spinal cord-injured persons," Med. Sci. Sports Exercise 37, 915-921 (2005).
[CrossRef] [PubMed]

M. J. Herrmann, A. C. Ehlis, A. Wagener, C. P. Jacob, and A. J. Fallgatter, "Near-infrared optical topography to assess activation of the parietal cortex during a visuo-spatial task," Neuropsychologia 43, 1713-1720 (2005).
[CrossRef] [PubMed]

S. Nioka and B. Chance, "NIR spectroscopic detection of breast cancer," Technol. Cancer Res. Treat. 4, 497-512 (2005).
[PubMed]

J. G. Kim and H. Liu, "Investigation of bi-phasic tumor oxygen dynamics induced by hyperoxic gas intervention: A numerical study," Opt. Express. 13, 4465-4475 (2005).
[CrossRef] [PubMed]

J. G. Kim, M. Xia, and H. Liu, "Hemoglobin extinction coefficients: importance of correct value for near-infrared spectroscopy," IEEE Eng. Med. Biol. Mag. 24, 118-121 (2005).
[CrossRef] [PubMed]

Y. Gu, R. Mason, and H. Liu, "Estimated fraction of tumor vascular blood contents sampled by near infrared spectroscopy and 19F magnetic resonance spectroscopy," Opt. Express 13, 1724-1733 (2005).
[CrossRef] [PubMed]

Y. Gu, W. R. Chen, M. Xia, S. W. Jeong, and H. Liu, "Effect of photothermal therapy on breast tumor vascular contents: non-invasive monitoring by near infrared spectroscopy," Photochem. Photobiol. 81, 1002-1009 (2005).
[CrossRef] [PubMed]

2004 (2)

V. S. Kalambur, H. Mahaseth, J. C. Bischof, M. C. Kielbik, T. E. Welch, Å. Vilbäck, D. J. Swanlund, R. P. Hebbel, J. D. Belcher, and G. M. Vercellotti, "Microvascular blood flow and stasis in transgenic sickle mice: utility of a dorsal skin fold chamber for intravital microscopy," Am. J. Hematol. 77, 117-125 (2004).
[CrossRef] [PubMed]

J. H. Kaanders, J. Bussink, and A. J. van der Kogel, "Clinical studies of hypoxia modification in radiotherapy," Semin. Radiat. Oncol. 14, 233-240 (2004).
[CrossRef] [PubMed]

2003 (4)

J. G. Kim, D. Zhao, Y. Song, A. Constantinescu, R. P. Mason, and H. Liu, "Interplay of tumor vascular oxygenation and tumor pO2 observed using NIRS, pO2 needle electrode and 19F MR pO2 mapping," J. Biomed. Opt. 8, 53-62 (2003).
[CrossRef] [PubMed]

Y. Gu, V. A. Bourke, J. G. Kim, A. Constantinescu, R. P. Mason, and H. Liu, "Dynamic response of breast tumor oxygenation to hyperoxic respiratory challenge monitored with three oxygen-sensitive parameters," Appl. Opt. 42, 2960-2967 (2003).
[CrossRef] [PubMed]

D. R. Tailor, H. Poptani, J. D. Glickson, J. S. Leigh, and R. Reddy, "High-resolution assessment of blood flow in murine RIF-1 tumors by monitoring uptake of H217O with proton T1ρ-weighted imaging," Magn. Reson. Med. 49, 1-6 (2003).
[CrossRef] [PubMed]

J. G. Kim, Y. Gu, A. Constantinescu, R. P. Mason, and H. Liu, "Non-uniform tumor vascular oxygen dynamics monitored by three-channel near-infrared spectroscopy," Proc. SPIE 4955, 388-396 (2003).
[CrossRef]

2002 (1)

M. Rijpkema, J. H. Kaanders, F. B. Joosten, A. J. van der Kogel, and A. Heerschap, "Effects of breathing a hyperoxic hypercapnic gas mixture on blood oxygenation and vascularity of head-and-neck tumors as measured by magnetic resonance imaging," Int. J. Radiat. Oncol. , Biol., Phys. 53, 1185-1191 (2002).
[CrossRef] [PubMed]

2001 (3)

D. Zhao, A. Constantinescu, E. W. Hahn, and R. P. Mason, "Tumor oxygenation dynamics with respect to growth and respiratory challenge: investigation of the Dunning prostate R3327-HI tumor," Radiat. Res. 156, 510-520 (2001).
[CrossRef] [PubMed]

S. Hunjan, D. Zhao, A. Constantinescu, E. W. Hahn, P. Antich, and R. P. Mason, "Tumor oximetry: demonstration of an enhanced dynamic mapping procedure using fluorine-19 echo planar magnetic resonance imaging in the dunning prostate R3327-AT1 rat tumor," Int. J. Radiat. Oncol. Biol. Phys. 49, 1097-1108 (2001).
[CrossRef] [PubMed]

M. Höckel and P. Vaupel, "Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects," J. Natl. Cancer Inst. 93, 266-276 (2001).
[CrossRef] [PubMed]

2000 (1)

1999 (2)

R. J. Gillies, P. A. Schornack, T. W. Secomb, and N. Raghunand, "Causes and effects of heterogeneous perfusion in tumors," Neoplasia 1, 197-207 (1999).
[CrossRef] [PubMed]

R. P. Mason, A. Constantinescu, S. Hunjan, D. Le, E. W. Hahn, P. P. Antich, C. Blum, and P. Peschke, "Regional tumor oxygenation and measurement of dynamic changes," Radiat. Res. 152, 239-249 (1999).
[CrossRef] [PubMed]

1998 (2)

B. Chance, E. Anday, S. Nioka, S. Zhou, L. Hong, K. Worden, C. Li, T. Murray, Y. Ovetsky, D. Pidikiti, and R. Thomas, "A novel method for fast imaging of brain function non-invasively with light," Opt. Express 2, 411-423 (1998).
[CrossRef] [PubMed]

A. W. Fyles, M. Milosevic, R. Wng, M. C. Kavanagh, M. Pintile, A. Sun, W. Chapman, W. Levin, L. Manchul, T. J. Keane, and R. P. Hill, "Oxygenation predicts radiation response and survival in patients with cervix cancer," Radiother. Oncol. 48, 149-156 (1998).
[CrossRef] [PubMed]

1997 (1)

J. Griebel, N. A. Mayr, A. de Vries, M. V. Knopp, T. Gneiting, C. Kremser, M. Essig, H. Hawighorst, P. H. Lukas, and W. T. Yuh, "Assessment of tumor microcirculation: a new role of dynamic contrast MR imaging," J. Magn. Reson. Imaging 7, 111-119 (1997).
[CrossRef] [PubMed]

1996 (1)

S. Homma, T. Fukunaga, and A. Kagaya, "Influence of adipose tissue thickness on near infrared spectroscopic signals in the measurement of human muscle," J. Biomed. Opt. 1, 418-424 (1996).
[CrossRef] [PubMed]

1995 (1)

H. Liu, A. H. Hielscher, F. K. Tittel, S. L. Jacques, and B. Chance, "Influence of blood vessels on the measurement of hemoglobin oxygenation as determined by time-resolved reflectance spectroscopy," Med. Phys. 22, 1209-1217 (1995).
[CrossRef] [PubMed]

1994 (2)

R. G. Steen, K. Kitagishi, and K. Morgan, "In vivo measurement of tumor blood oxygenation by near-infrared spectroscopy: immediate effects of pentobarbital overdose or carmustine treatment," J. Neuro-Oncol. 22, 209-220 (1994).
[CrossRef] [PubMed]

R. G. Steen, K. Kitagishi, and K. Morgan, "In vivo measurement of tumor blood oxygenation by near-infrared spectroscopy: immediate effects of pentobarbital overdose or carmustine treatment," J. Neuro-Oncol. 22, 209-220 (1994).
[CrossRef] [PubMed]

1992 (1)

S. R. Arridge, M. Cope, and D. T. Delpy, "The theroretical basis for the determination of optical pathlengths in tissue: temporal and frequency analysis," Phys. Med. Biol. 37, 1531-1560 (1992).
[CrossRef] [PubMed]

1991 (1)

J. D. Chapman, C. C. Stobbe, M. R. Arnfield, R. Santus, J. Lee, and M. S. McPhee, "Oxygen dependency of tumor cell killing in vitro by light activated photofrin II," Radiat. Res. 126, 73-79 (1991).
[CrossRef] [PubMed]

1990 (1)

J. C. Acker, M. W. Dewhirst, G. M. Honore, T. V. Samulski, J. A. Tucker, and J. R. Oleson, "Blood perfusion measurements in human tumors, evaluation of laser Doppler methods," Int. J. Hyperthermia 6, 287-304 (1990).
[CrossRef] [PubMed]

1988 (3)

B. Chance, S. Nioka, J. Kent, K. McCully, M. Fountain, R. Greenfield, and G. Holtom, "Time resolved spectroscopy of hemoglobin and myoglobin in resting and ischemic muscle," Anal. Biochem. 174, 698-707 (1988).
[CrossRef] [PubMed]

M. Cope and D. T. Delpy, "A system for long term measurement of cerebral blood and tissue oxygenation in newborn infants by near infrared transillumination," Med. Biol. Eng. Comput. 26, 289-294 (1988).
[CrossRef] [PubMed]

D. T. Delpy, M. Cope, P. van der Zee, S. Arridge, S. Wray, and J. Wyatt, "Estimation of optical pathlength through tissue from direct time of flight measurement," Phys. Med. Biol. 33, 1433-1442 (1988).
[CrossRef] [PubMed]

1987 (1)

M. W. Dewhirst, C. Gustafson, J. F. Gross, and C. Y. Tso, "Temporal effects of 5.0 Gy radiation in healing subcutaneous microvasculature of a dorsal flap window chamber," Radiat. Res. 112, 581-591 (1987).
[CrossRef] [PubMed]

1981 (1)

B. Teicher, J. Lazo, and A. Sartorelli, "Classification of antineoplastic agents by their selective toxicities toward oxygenated and hypoxic tumor cells," Cancer Res. 41, 73-81 (1981).
[PubMed]

1972 (1)

H. D. Suit, N. Marshall, and D. Woerner, "Oxygen, oxygen plus carbon dioxide, and radiation therapy of a mouse mammary carcinoma. Cancer," Cancer 30, 1154-1158 (1972).
[CrossRef] [PubMed]

1968 (1)

P. Bergsjo and P. Kolstad, "Clinical trial with atmospheric oxygen breathing during radiotherapy of cancer of the cervix," Scand. J. Clin. Lab. Invest. Suppl. 106, 167-171 (1968).
[PubMed]

1955 (1)

R. H. Thomlinson and L. H. Gray, "The histological structure of some human lung cancers and the possible implications for radiotherapy," Br. J. Cancer 9, 539-549 (1955).
[CrossRef] [PubMed]

1951 (1)

S. S. Kety, "The theory and applications of the exchange of inert gas at the lungs and tissue," Pharmacol. Rev. 3, 1-41 (1951).
[PubMed]

Am. J. Hematol. (1)

V. S. Kalambur, H. Mahaseth, J. C. Bischof, M. C. Kielbik, T. E. Welch, Å. Vilbäck, D. J. Swanlund, R. P. Hebbel, J. D. Belcher, and G. M. Vercellotti, "Microvascular blood flow and stasis in transgenic sickle mice: utility of a dorsal skin fold chamber for intravital microscopy," Am. J. Hematol. 77, 117-125 (2004).
[CrossRef] [PubMed]

Anal. Biochem. (1)

B. Chance, S. Nioka, J. Kent, K. McCully, M. Fountain, R. Greenfield, and G. Holtom, "Time resolved spectroscopy of hemoglobin and myoglobin in resting and ischemic muscle," Anal. Biochem. 174, 698-707 (1988).
[CrossRef] [PubMed]

Appl. Opt. (2)

Br. J. Cancer (1)

R. H. Thomlinson and L. H. Gray, "The histological structure of some human lung cancers and the possible implications for radiotherapy," Br. J. Cancer 9, 539-549 (1955).
[CrossRef] [PubMed]

Cancer (1)

H. D. Suit, N. Marshall, and D. Woerner, "Oxygen, oxygen plus carbon dioxide, and radiation therapy of a mouse mammary carcinoma. Cancer," Cancer 30, 1154-1158 (1972).
[CrossRef] [PubMed]

Cancer Res. (1)

B. Teicher, J. Lazo, and A. Sartorelli, "Classification of antineoplastic agents by their selective toxicities toward oxygenated and hypoxic tumor cells," Cancer Res. 41, 73-81 (1981).
[PubMed]

IEEE Eng. Med. Biol. Mag. (1)

J. G. Kim, M. Xia, and H. Liu, "Hemoglobin extinction coefficients: importance of correct value for near-infrared spectroscopy," IEEE Eng. Med. Biol. Mag. 24, 118-121 (2005).
[CrossRef] [PubMed]

Int. J. Hyperthermia (1)

J. C. Acker, M. W. Dewhirst, G. M. Honore, T. V. Samulski, J. A. Tucker, and J. R. Oleson, "Blood perfusion measurements in human tumors, evaluation of laser Doppler methods," Int. J. Hyperthermia 6, 287-304 (1990).
[CrossRef] [PubMed]

Int. J. Radiat. Oncol. (1)

M. Rijpkema, J. H. Kaanders, F. B. Joosten, A. J. van der Kogel, and A. Heerschap, "Effects of breathing a hyperoxic hypercapnic gas mixture on blood oxygenation and vascularity of head-and-neck tumors as measured by magnetic resonance imaging," Int. J. Radiat. Oncol. , Biol., Phys. 53, 1185-1191 (2002).
[CrossRef] [PubMed]

Int. J. Radiat. Oncol. Biol. Phys. (1)

S. Hunjan, D. Zhao, A. Constantinescu, E. W. Hahn, P. Antich, and R. P. Mason, "Tumor oximetry: demonstration of an enhanced dynamic mapping procedure using fluorine-19 echo planar magnetic resonance imaging in the dunning prostate R3327-AT1 rat tumor," Int. J. Radiat. Oncol. Biol. Phys. 49, 1097-1108 (2001).
[CrossRef] [PubMed]

J. Biomed. Opt. (2)

S. Homma, T. Fukunaga, and A. Kagaya, "Influence of adipose tissue thickness on near infrared spectroscopic signals in the measurement of human muscle," J. Biomed. Opt. 1, 418-424 (1996).
[CrossRef] [PubMed]

J. G. Kim, D. Zhao, Y. Song, A. Constantinescu, R. P. Mason, and H. Liu, "Interplay of tumor vascular oxygenation and tumor pO2 observed using NIRS, pO2 needle electrode and 19F MR pO2 mapping," J. Biomed. Opt. 8, 53-62 (2003).
[CrossRef] [PubMed]

J. Magn. Reson. Imaging (1)

J. Griebel, N. A. Mayr, A. de Vries, M. V. Knopp, T. Gneiting, C. Kremser, M. Essig, H. Hawighorst, P. H. Lukas, and W. T. Yuh, "Assessment of tumor microcirculation: a new role of dynamic contrast MR imaging," J. Magn. Reson. Imaging 7, 111-119 (1997).
[CrossRef] [PubMed]

J. Natl. Cancer Inst. (1)

M. Höckel and P. Vaupel, "Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects," J. Natl. Cancer Inst. 93, 266-276 (2001).
[CrossRef] [PubMed]

J. Neuro-Oncol. (2)

R. G. Steen, K. Kitagishi, and K. Morgan, "In vivo measurement of tumor blood oxygenation by near-infrared spectroscopy: immediate effects of pentobarbital overdose or carmustine treatment," J. Neuro-Oncol. 22, 209-220 (1994).
[CrossRef] [PubMed]

R. G. Steen, K. Kitagishi, and K. Morgan, "In vivo measurement of tumor blood oxygenation by near-infrared spectroscopy: immediate effects of pentobarbital overdose or carmustine treatment," J. Neuro-Oncol. 22, 209-220 (1994).
[CrossRef] [PubMed]

Magn. Reson. Med. (1)

D. R. Tailor, H. Poptani, J. D. Glickson, J. S. Leigh, and R. Reddy, "High-resolution assessment of blood flow in murine RIF-1 tumors by monitoring uptake of H217O with proton T1ρ-weighted imaging," Magn. Reson. Med. 49, 1-6 (2003).
[CrossRef] [PubMed]

Med. Biol. Eng. Comput. (1)

M. Cope and D. T. Delpy, "A system for long term measurement of cerebral blood and tissue oxygenation in newborn infants by near infrared transillumination," Med. Biol. Eng. Comput. 26, 289-294 (1988).
[CrossRef] [PubMed]

Med. Phys. (1)

H. Liu, A. H. Hielscher, F. K. Tittel, S. L. Jacques, and B. Chance, "Influence of blood vessels on the measurement of hemoglobin oxygenation as determined by time-resolved reflectance spectroscopy," Med. Phys. 22, 1209-1217 (1995).
[CrossRef] [PubMed]

Med. Sci. Sports Exercise (1)

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Figures (8)

Fig. 1
Fig. 1

(Color online) Normalized hemodynamic changes of tumor blood oxygenation, Δ[HbO2], obtained with the NIRS measurement from a rat breast tumor while the breathing gas was switched from air to carbogen. (Gu et al., Appl. Opt., 2003) [30].

Fig. 2
Fig. 2

Schematic of light transmitting patterns in a tumor when the tumor has two distinct perfusion regions. The center of the tumor represents a poorly perfused region, and the peripheral region of the tumor with the gray color represents a well-perfused region. Since the light transmitting volume is different in each detector, each detector will show the different fitted parameters.

Fig. 3
Fig. 3

Schematic for one VMD. Two different ID sizes of tubing have been used to wind outside of core tubing to simulate different blood vessel diameters within a breast tumor.

Fig. 4
Fig. 4

Experimental setup for the tumor dynamic phantom study. (a) Two syringe pumps were connected to two VMDs in a tumor vascular dynamic phantom individually to have different dye flow rates for each VMD. Light was transmitted from a light source through the tumor vascular dynamic phantom and was collected at three different detectors for dataprocessing in a computer. (b) Enlarged tumor vascular dynamic phantom embedded with two VMDs. Tumor phantom 1 has VMD-1 and VMD-2 as shown here, and tumor phantom 2 has two VMD-1s.

Fig. 5
Fig. 5

(a) Absorption changes measured from the dynamic tumor vascular phantom with increasing a flow rate from (a) 1 to 10 ml∕h and (b) 15 to 60 ml∕h. The symbols and curves are obtained from the phantom experiments and from the one-exponential curve fitting, respectively.

Fig. 6
Fig. 6

(a) Correlation between time constants and flow rates plotted with the linear scale (left and bottom axis) and logarithmic scale (top and right axis). (b) Linear correlation between ink flow velocities and ink flow rates with a fixed diameter of tube.

Fig. 7
Fig. 7

(a) Three temporal profiles of three-channel NIRS measurements result from D1, D2, and D3 on dynamic phantom 1 that has two different sizes of VMDs (VMD-1 and VMD-2). (b) Absorption changes obtained from D1, D2, and D3 during step 3 of (a). Open symbols represent the raw data of absorption changes, and solid curves are obtained with either monoexponential model fitting (D1 and D2) or biexponential model fitting (D3).

Fig. 8
Fig. 8

(a) Three-channel NIRS results measured from tumor dynamic phantom 2 that has two VMD-1s. Three traces represent the readings at D3 (in transmission mode and located between the two VMDs), D2 (near the top VMD-1), and D1 (near the bottom VMD-1). (b) Temporal profiles of the NIRS measurements from D1, D2, and D3 with monoexponential fitting (D1 and D2) and biexponential fitting (D3).

Tables (2)

Tables Icon

Table 1 Summary of Fitted Parameters Obtained at the Three Detectors in Fig. 7(b)

Tables Icon

Table 2 Summary of Fitted Parameters Obtained at Three Detectors Given in Fig. 8(b)

Equations (9)

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Δ [ HbO 2 ] vasculature ( t ) = γ H o [ 1 exp ( f t / γ ) ] = A [ 1 exp ( t / τ ) ] ,
Δ HbO 2 vasculature ( t ) = γ 1 H o [ 1 exp ( f 1 t / γ 1 ) ] + γ 2 H o [ 1 exp ( f 2 t / γ 2 ) ] = A 1 [ 1 exp ( t / τ 1 ) ] + A 2 [ 1 exp ( t / τ 2 ) ] ,
γ 1 γ 2 = A 1 A 2 , f 1 f 2 = A 1 / A 2 τ 1 / τ 2 .
Δ O . D . = O . D . T O . D . B = log ( I B / I T ) / L ,
Δ O . D . = O . D . T O . D . B = log ( I B / I T ) / d .
Q = V / t = S × v = π r 2 × v ,
τ = 419.7 Q 1.13 ,
v V MD - 1 v V MD - 2 = r V MD - 2 2 r V MD -1 2 = 0.43 2 0.255 2 = 2.84 ,
τ 1 τ 2 v VMD-2 v VMD-1 = 1 2.84 .

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