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Optics Express

Optics Express

  • Editor: Michael Duncan
  • Vol. 10, Iss. 23 — Nov. 18, 2002
  • pp: 1347–1353
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Myocardial tissue characterization based on the time-resolved Stokes-Mueller formalism

Chia-Wei Sun, Long-Sheng Lu, C. C. Yang, Yean-Woei Kiang, and Ming-Jai Su  »View Author Affiliations


Optics Express, Vol. 10, Issue 23, pp. 1347-1353 (2002)
http://dx.doi.org/10.1364/OE.10.001347


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Abstract

Time-resolved Stokes vectors of transmitted optical signals were measured to differentiate normal and stunned myocardium tissues. The corresponding Mueller matrices were calculated based on the Stokes-Mueller formalism. Our experimental results indicated that the time-resolved Mueller matrices could provide information about myocardial architectural alteration in stunned myocardium. Thus, the Stokes-Mueller measurement can be a useful method in cardiovascular research.

© 2002 Optical Society of America

1. Introduction

Recently, the quasi-coherent photon imaging method becomes attractive as a promising noninvasive technique for biological tissue characterization [5–7

5. S. K. Gayen and R. R. Alfano, “Sensing lesions in tissues with light,” Opt. Express 4, 475–480 (1999). http://www.opticsexpress.org/abstract.cfm?URI=OPEX-4-11-475. [CrossRef] [PubMed]

]. In such an ultra-fast optics technique, short optical pulses are applied to biological tissues. The photons travel with nearly straight line trajectories with fewer random scattering events are collected as quasi-coherent photons or snake photons. Because the snake photons pass through biological tissues with weaker scattering, they carry direct information about histological characteristics of tissues. Because of the quasi-regular arrangement in myocardial muscle fibers, deterministic optical birefringence effect is expected [8

8. R. E. Weiss and M. Morad, “Birefringence signals in mammalian and frog myocardium,” J. Gen. Physiol. 82, 79–117 (1983). [CrossRef] [PubMed]

,9

9. C. -W. Sun, C. -Y. Wang, C. C. Yang, Y. -W Kiang, C. -W. Lu, I -J. Hsu, and C. -W. Lin, “Polarization dependent characteristics and polarization gating in time-resolved optical imaging of skeletal muscle tissues,” IEEE J. Select. Topics Quantum Electron. 7, 924–930 (2001). [CrossRef]

]. In this situation, all the elements of polarization state must be considered for observing the polarization evolution and hence providing information of histological structure in myocardium. To observe the polarization properties in myocardial tissues, the Stokes-Mueller formalism was adopted to provide a complete representation of the polarization states [10–12

10. T. T. Tower and R. T. Tranquillo, “Alignment maps of tissues: II. Fast harmonic analysis for imaging,” Biophys. J. 81, 2964–2971 (2001). [CrossRef] [PubMed]

]. In this paper, we measured the time-resolved Stokes vectors of normal and stunned myocardium from rats and compared their differences. Structural alterations in these specimens were also evaluated with the standard H&E staining process. The 4×4 full Mueller matrices of samples were evaluated from the measured Stokes vectors with time-gating processes. In section 2 of this paper, we describe the experimental procedures. The time-resolved Stokes-Mueller formalism is briefly introduced in section 3. The measurement results and discussions are given in section 4. Finally, conclusions are drawn in section 5.

2. Experimental Procedures

The work was conducted in accordance with the R.O.C. Animal Protection Law (Scientific Application of Animals), 1998. In this research, we adopted stunned myocardium of rats and cardiomyopathic myocardium of hamsters for optical measurements. Normal myocardial tissues in each case were also prepared for comparison.

In the case of stunned myocardium study, six adult male WKY rats were randomly assigned into either control (C) or stunned (S) group. Left thoracotomy after generalized anaethesia (sodium pentobarbital, 30 mg/kg i.p.) was performed. For rats in the S group (stunned myocardium), we ligated left anterior descending artery at its proximal part under adequate ventilation support. Ischemia was monitored with electrocardiography tracing as depression of ST segment in lead II. After 30 minutes, the ligature was released. The animals were then allowed reperfusion for another 180 minutes. For rats in the C group (normal myocardium), a sham operation was performed. To harvest myocardial tissues, lethal dose of sodium pentobarbital was administered. Animals were retrogradely perfused with heparinized PBS (10 units/ml) for 15 minutes followed by 2 % paraformaldehyde (pH 7.4) for another 15 minutes. Then, hearts were removed quickly and stored in 10 % formaldehyde till the optical experiments.

Bio14.6 hamster is another widely used animal model for autosomal recessive cardiomyopathy [13

13. V. Nigro, Y. Okazaki, A. Belsito, G. Piluso, Y. Matsuda, L. Politano, G. Nigro, C. Ventura, C. Abbondanza, A. M. Molinari, D. Acampora, M. Nishimura, Y. Hayashizaki, and G. A. Puca, “Identification of the Syrian hamstercardiomyopathy gene”, Human Molecular Genetics , 6, 601–607 (1997). [CrossRef] [PubMed]

]. Such an animal dies prematurely from progressive myocardial necrosis and heart failure due to a genetic defect leading to total absence of delta-sarcoglycan, which contributes significantly to stablizing cell membrane in striated muscle cells. The myocardium of the Bio14.6 cardiomyopathic hamster was obtained from Biobreeders Inc., Watertown, MA, USA. The heart was extracted and fixated in 10% formaldehyde after retrograde perfusion from ascending aorta. All other procedures of sample preparation are the same as those for the rat experiment.

The optical experiment setup is shown in Fig. 1. A Verdi-laser-pumped mode-locked Ti:sapphire laser was used to provide 76 MHz, around 100 fs laser pulses at 800 nm. The laser beam was split into two branches, one for triggering the used streak camera and another for propagating through tissue sample. About 100-mW average power of laser pulses was applied to the samples. The diameter of the sample beam was slightly smaller than 1 mm. The samples were submerged in water to avoid thermal damage. In positioning the samples, care was taken to ensure that laser pulses traveled through the middle segment of the left ventricle free wall. We positioned the heart as described to minimize the possibility that laser pulses past through valves, papillary muscles or intraventricular septum. Complex fiber orientation in these intracardiac structures adds uncertainties in output polarization state and may introduce errors.

Fig. 1. Experimental setup. BP: beam splitter; P: polarizer; HW: half-wave plate; QW: quarter-wave plate; D: trigger detector.

According to the Stokes-Mueller formalism, we need to prepare four different polarization states of incident photons, including the horizontal polarization component, the vertical polarization component, the 45° linear polarization component, and the right-hand circular polarization component. In experiments, such polarization control was accomplished through adjusting the used polarizers, half-wave plates and quarter-wave plates. Here, the horizontal and vertical polarization directions are referred to the coordinate of the laboratory. The transmitted signals of samples were directed to the streak camera with a fiber bundle for each of the 16 combinations of the polarization states. The temporal resolution of the operation mode of the streak camera was about 20 ps due to the temporal limitation of the streak camera and the group-velocity dispersion effect in the fiber bundle. The quasi-coherent photon data were obtained through the integration of the time-resolved intensity profiles with the duration of 50 ps from the leading edges of the profiles. After the measurements, specimens were processed for standard H&E staining.

3. Stokes-Mueller Formalism

The Stokes components, generally denoted by S0, S1, S2 and S3, form a sufficient set for describing the amplitude, phase and polarization of a light wave. To express the Stokes vector S in terms of our experimental data, the following relation is needed:

S=[S0S1S2S3]=[H+VHV2PHV2RHV].
(1)

Here, H, V, P, and R are the measured quantities of the polarization components, vertical polarization component, 45° linear polarization component, and right-hand circular polarization component, respectively. In experiments, the Stokes vectors of transmitted photons corresponding to the four incident polarization states H, V, P, and R are denoted, respectively, by S H, S V, S P, and S R. According to the Stokes-Mueller formalism, the Mueller matrix M can be evaluated from the output Stokes vectors as

M=12[SH+SVSHSV2SP(SH+SV)2SR(SH+SV)].
(2)

4. Experimental Results

Figure 2 shows the time-resolved intensity profiles of the four polarization components of normal cardiac muscle tissue with horizontal polarization inputs. The middle segment of left ventricle free wall of a myocardium sample was used for obtaining the data. The narrow width (~70 ps) of the co-polarized component H and the weak intensity of the cross-polarized component V indicate the weak random scattering in the myocardial tissue. However, the small difference between the components P and R in the quasi-coherent part implies the polarization coupling effect due to the anisotropic structure of myocardial muscle fibers.

Fig. 2. Measured time-resolved polarization components of normal myocardium.

Figure 3 shows the histological images of normal and stunned myocardium. The wall thicknesses in both samples were about 3 mm with a left ventricle dimension of 4 mm. Under microscopic examination, hearts from the C group (as shown in Fig. 3 (a)) show a regular arrangement of muscle fibers. On the contrary, hearts from the S group show pronounced contraction band necrosis, myocyte contracture (arrowheads) and muscle fiber derangement (arrows) in putative regions through which the laser beam passed (Fig. 3 (b)). We believe that the loss of regularly arranged contractile proteins, degradation of bundle structures and disarrayed muscle fibers all contribute to the changes of birefringence effect in myocardium.

Fig. 3. Microphotographs (under 400X magnification) of (a) normal and (b) stunned myocardium.

Based on the measured polarization components, the time-resolved Stokes elements of normal and stunned myocardium with horizontally polarized incident pulses can be obtained and shown in Figs. 4 (a) and (b), respectively. The measurement results of myocardial samples in each group (S or C) have similar patterns. The S0 profile represents the total intensity of measured signal through the myocardium samples. The S1 profile indicates the portion of transmitted quasi-coherent photons. The information of coupled polarization components was furnished with the quasi-coherent parts of S2 and S3. In Fig. 4 (a), the depression features of S2 and S3 near the leading edges of the time-resolved profiles should result from optical birefringence with the regular fiber architecture of normal myocardium. After ischemia-reperfusion, the altered tissue structure led to the changes of S2 and S3 (as shown in Fig. 4 (b)).

Fig. 4. Time-resolved Stokes vectors of (a) normal and (b) stunned myocardium.

For further understanding of polarization evolution in myocardial tissues, the complete polarization elements of Mueller matrices are needed. Based on the Stokes-Mueller formalism with our experimental data, the Mueller matrices of normal and stunned myocardium are shown in Figs. 5 (a) and (b), respectively. The time-gated data was obtained by the integration of the time-resolved intensity profiles with duration of about 50 ps from the leading edges (~ 220 ps in Fig. 2) of the profiles. The 3-D mapping image represents a 4 × 4 full Mueller matrix with a linear interpolation surface. The quantities of diagonal elements in the Mueller matrices stand for the intensities of preserved original polarization states from various polarization inputs. The quantities of diagonal elements (the red region) in Fig. 5 (b) are lower than those of Fig. 5 (a) that reveals the larger polarization changes in the damaged fiber architecture. Meanwhile, the pattern in Fig. 5 (b) manifests the difference of polarization evolution with compare to Fig. 5 (a). The strength of circular polarization coupling (the violet region at the right corner) in Fig. 5 (b) is higher than (a) that again is attributed to the histological alterations of the fibrous structure in stunned myocardium. The clear difference in experimental results between normal and stunned myocardium implies different polarization evolution due to the altered structures.

Fig. 5. Time-resolved Mueller matrices of (a) normal and (b) stunned myocardium.

The histological features of hearts from Bio14.6 hamsters include central nucleation, wide variation in muscle fiber diameter, and necrosis (see Fig. 6). Besides, in Fig. 6 we can see that muscle fibers are no longer regularly arranged and infiltration of scar tissue is evident. All these features contribute to the enhanced photon scattering and reduced degree of polarization of transmitted light. Fig. 7 (a) shows the Mueller matrix of hamster’s normal myocardium. The result of cardiomyopathic myocardium is shown in Fig. 7 (b). The significant difference between the two samples can be clearly seen. Because the cardiomyopathic myocardium tissue (about 5 mm in wall thickness) is thicker than normal myocardium tissue, the average level of matrix element values is relatively lower due to stronger scattering.

Fig. 6. Microphotograph (under 400X magnification) of cardiomyopathic myocardium.
Fig. 7. Time-resolved Mueller matrices of (a) normal and (b) cardiomyopathic myocardium.

5. Discussions and Conclusions

The results of time-resolved Stokes-Mueller experiments have demonstrated that optical measurements using the time gating of transmitted light was a promising method for characterizing myocardial tissues. Altered birefringence signals could be utilized to differentiate stunned or cardiomyopathic from normal myocardium. The underlying mechanism was assumed to be the loss of optical anisotropy, both in the subcellular and tissue levels. Optical characterization based on time-resolved Stokes-Mueller measurements is a diagnostic tool of great potential, which can be a great assistance to the management of cardiovascular diseases. The full 4×4 time-gated Mueller matrix can reflect altered structures in myocardial tissues. Time-gated signals will be helpful in reducing the depolarization effect of random scattering in biological tissues. The transmission measurements were used for the first-step characterization of such tissues because they are supposed to provide more information than the reflection measurements. Since it is difficult to conductor the optical transmission measurements in in vivo experiments, the reflection type of measurement based on the technique of optical coherence tomography is currently under development.

Acknowledgement:

This research was supported by National Health Research Institute, The Republic of China, under the grant of NHRI-GT-EX89E819L. L.S.L. is a recipient of NHRI MDPhD/DDSPhD Predoctoral Fellowship from the National Health Research Institute.

References and links

1.

O. M. Hess, J. Schneider, H. Nonogi, J. D. Carroll, K. Schneider, M. Turina, and H. P. Krayenbuehl, “Myocardial structure in patients with exercise-induced ischemia,” Circulation 77, 967–977 (1988). [CrossRef] [PubMed]

2.

S. A. Rubin, M. C. Fishbein, and H. J. Swan, “Compensatory hypertrophy in the heart after myocardial infarction in the rat,” J. Am. Coll. Cardiol. 1, 1435–1441 (1983). [CrossRef] [PubMed]

3.

R. A. Kloner and R. B. Jennings, “Consequences of brief ischemia: stunning, preconditioning, and their clinical implications,” Circulation 104, 2981–2989 (2001). [CrossRef] [PubMed]

4.

A. Lochner, I. S. Harper, R. Salie, S. Genade, and A. R. Coetzee, “Halothane protects the isolated rat myocardium against excessive total intracellular calcium and structural damage during ischemia and reperfusion,” Anesth. Analg. 79, 226–233 (1994). [CrossRef] [PubMed]

5.

S. K. Gayen and R. R. Alfano, “Sensing lesions in tissues with light,” Opt. Express 4, 475–480 (1999). http://www.opticsexpress.org/abstract.cfm?URI=OPEX-4-11-475. [CrossRef] [PubMed]

6.

D. Grosenick, H. Wabnitz, H. H. Rinneberg, K. T. Moesta, and P. M. Schlag, “Development of a time-domain optical mammography and first in vivo applications,” Appl. Opt. 38, 2927–2943 (1999). [CrossRef]

7.

C. -W. Sun, C. -Y. Wang, C. C. Yang, Y. -W Kiang, I -J. Hsu, and C. -W. Lin, “Polarization gating in ultrafast-optics imaging of skeletal muscle tissues,” Opt. Lett. 26, 432–434 (2001). [CrossRef]

8.

R. E. Weiss and M. Morad, “Birefringence signals in mammalian and frog myocardium,” J. Gen. Physiol. 82, 79–117 (1983). [CrossRef] [PubMed]

9.

C. -W. Sun, C. -Y. Wang, C. C. Yang, Y. -W Kiang, C. -W. Lu, I -J. Hsu, and C. -W. Lin, “Polarization dependent characteristics and polarization gating in time-resolved optical imaging of skeletal muscle tissues,” IEEE J. Select. Topics Quantum Electron. 7, 924–930 (2001). [CrossRef]

10.

T. T. Tower and R. T. Tranquillo, “Alignment maps of tissues: II. Fast harmonic analysis for imaging,” Biophys. J. 81, 2964–2971 (2001). [CrossRef] [PubMed]

11.

S. Jiao, G. Yao, and L. V. Wang, “Depth-resolved two-dimensional Stokes vectors of backscattered light and Mueller matrices of biological tissue measured with optical coherent tomography,” Appl. Opt. 39, 6318–6324 (2000). [CrossRef]

12.

A. H. Hielscher, A. A. Eick, J. R. Mourant, D. Shen, James. P. Freyer, and I. J. Bigio, “Diffuse backscattering Mueller matrices of highly scattering media,” Opt. Express 1, 441–453 (1997). http://www.opticsexpress.org/abstract.cfm?URI=OPEX-1-13-441. [CrossRef] [PubMed]

13.

V. Nigro, Y. Okazaki, A. Belsito, G. Piluso, Y. Matsuda, L. Politano, G. Nigro, C. Ventura, C. Abbondanza, A. M. Molinari, D. Acampora, M. Nishimura, Y. Hayashizaki, and G. A. Puca, “Identification of the Syrian hamstercardiomyopathy gene”, Human Molecular Genetics , 6, 601–607 (1997). [CrossRef] [PubMed]

OCIS Codes
(170.0170) Medical optics and biotechnology : Medical optics and biotechnology
(170.3660) Medical optics and biotechnology : Light propagation in tissues

ToC Category:
Research Papers

History
Original Manuscript: August 1, 2002
Revised Manuscript: November 6, 2002
Published: November 18, 2002

Citation
Chia-Wei Sun, Long-Sheng Lu, C. C. Yang, Yean-Woei Kiang, and Ming-Jai Su, "Myocardial tissue characterization based on the time-resolved Stokes-Mueller formalism," Opt. Express 10, 1347-1353 (2002)
http://www.opticsinfobase.org/oe/abstract.cfm?URI=oe-10-23-1347


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References

  1. O. M. Hess, J. Schneider, H. Nonogi, J. D. Carroll, K. Schneider, M. Turina and H. P. Krayenbuehl, �??Myocardial structure in patients with exercise-induced ischemia,�?? Circulation 77, 967-977 (1988). [CrossRef] [PubMed]
  2. S. A. Rubin, M. C. Fishbein, H. J. Swan, �??Compensatory hypertrophy in the heart after myocardial infarction in the rat,�?? J. Am. Coll. Cardiol. 1, 1435-1441 (1983). [CrossRef] [PubMed]
  3. R. A. Kloner and R. B. Jennings, �??Consequences of brief ischemia: stunning, preconditioning, and their clinical implications,�?? Circulation 104, 2981-2989 (2001). [CrossRef] [PubMed]
  4. A. Lochner, I. S. Harper, R. Salie, S. Genade, A. R. Coetzee, �??Halothane protects the isolated rat myocardium against excessive total intracellular calcium and structural damage during ischemia and reperfusion,�?? Anesth. Analg. 79, 226-233 (1994). [CrossRef] [PubMed]
  5. S. K. Gayen and R. R. Alfano, �??Sensing lesions in tissues with light,�?? Opt. Express 4, 475-480 (1999). <a href="http://www.opticsexpress.org/abstract.cfm?URI=OPEX-4-11-475">http://www.opticsexpress.org/abstract.cfm?URI=OPEX-4-11-475</a>. [CrossRef] [PubMed]
  6. D. Grosenick, H. Wabnitz, H. H. Rinneberg, K. T. Moesta, and P. M. Schlag, �??Development of a timedomain optical mammography and first in vivo applications,�?? Appl. Opt. 38, 2927-2943 (1999). [CrossRef]
  7. C. -W. Sun, C. -Y. Wang, C. C. Yang, Y. -W Kiang, I -J. Hsu, and C. -W. Lin, �??Polarization gating in ultrafast-optics imaging of skeletal muscle tissues,�?? Opt. Lett. 26, 432-434 (2001). [CrossRef]
  8. R. E. Weiss and M. Morad, �??Birefringence signals in mammalian and frog myocardium,�?? J. Gen. Physiol. 82, 79-117 (1983). [CrossRef] [PubMed]
  9. C. -W. Sun, C. -Y. Wang, C. C. Yang, Y. -W Kiang, C. -W. Lu, I -J. Hsu, and C. -W. Lin, �??Polarization dependent characteristics and polarization gating in time-resolved optical imaging of skeletal muscle tissues,�?? IEEE J. Sel. Top. Quantum Electron. 7, 924-930 (2001). [CrossRef]
  10. T. T. Tower and R. T. Tranquillo, �??Alignment maps of tissues: II. Fast harmonic analysis for imaging,�?? Biophys. J. 81, 2964-2971 (2001). [CrossRef] [PubMed]
  11. S. Jiao, G. Yao, and L. V. Wang, �??Depth-resolved two-dimensional Stokes vectors of backscattered light and Mueller matrices of biological tissue measured with optical coherent tomography,�?? Appl. Opt. 39, 6318-6324 (2000). [CrossRef]
  12. A. H. Hielscher, A. A. Eick, J. R. Mourant, D. Shen, James. P. Freyer, and I. J. Bigio, �??Diffuse backscattering Mueller matrices of highly scattering media,�?? Opt. Express 1, 441-453 (1997). <a href="http://www.opticsexpress.org/abstract.cfm?URI=OPEX-1-13-441">http://www.opticsexpress.org/abstract.cfm?URI=OPEX-1-13-441</a>. [CrossRef] [PubMed]
  13. V. Nigro, Y. Okazaki, A. Belsito, G. Piluso, Y. Matsuda, L. Politano, G. Nigro, C. Ventura, C. Abbondanza, A. M. Molinari, D. Acampora, M. Nishimura, Y. Hayashizaki and G. A. Puca, "Identification of the Syrian hamstercardiomyopathy gene," Human Molecular Genetics 6, 601-607 (1997). [CrossRef] [PubMed]

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