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Biomedical Optics Express

Biomedical Optics Express

  • Editor: Joseph A. Izatt
  • Vol. 3, Iss. 5 — May. 1, 2012
  • pp: 1110–1115
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Quantitative analysis of water distribution in human articular cartilage using terahertz time-domain spectroscopy

Euna Jung, Hyuck Jae Choi, Meehyun Lim, Hyeona Kang, Hongkyu Park, Haewook Han, Byung-hyun Min, Sangin Kim, Ikmo Park, and Hanjo Lim  »View Author Affiliations


Biomedical Optics Express, Vol. 3, Issue 5, pp. 1110-1115 (2012)
http://dx.doi.org/10.1364/BOE.3.001110


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Abstract

The water distribution in human osteoarthritic articular cartilage has been quantitatively characterized using terahertz time-domain spectroscopy (THz TDS). We measured the refractive index and absorption coefficient of cartilage tissue in the THz frequency range. Based on our measurements, the estimated water content was observed to decrease with increasing depth cartilage tissue, showing good agreement with a previous report based on destructive biochemical methods.

© 2012 OSA

1. Introduction

Osteoarthritis (OA), one of the most prevalent chronic diseases in the elderly, is characterized by progressive degeneration of cartilage. Cartilage degeneration is affected by biochemical alterations, including an increase in water content and the loss of proteoglycans [1

1. A. R. Poole, T. Kojima, T. Yasuda, F. Mwale, M. Kobayashi, and S. Laverty, “Composition and structure of articular cartilage: a template for tissue repair,” Clin. Orthop. Relat. Res. 391(391Suppl), S26–S33 (2001). [CrossRef] [PubMed]

3

3. C.-B. James and T. L. Uhl, “A review of articular cartilage pathology and the use of glucosamine sulfate,” J. Athl. Train. 36(4), 413–419 (2001). [PubMed]

]. Several studies have shown that the water content in osteoarthritic cartilage may increase by about 10% [4

4. H. J. Mankin and A. Z. Thrasher, “Water content and binding in normal and osteoarthritic human cartilage,” J. Bone Joint Surg. Am. 57(1), 76–80 (1975). [PubMed]

]. Therefore, a precise measurement of the water content in cartilage can aid in the diagnosis of early-stage OA. However, changes in the water content in the early stages of OA cannot be detected using current clinical techniques such as radiography and arthroscopy. Only magnetic resonance imaging (MRI) has been used for the detection of water content in the early stages of OA [5

5. C. Liess, S. Lüsse, N. Karger, M. Heller, and C.-C. Glüer, “Detection of changes in cartilage water content using MRI T2-mapping in vivo,” Osteoarthritis Cartilage 10(12), 907–913 (2002). [CrossRef] [PubMed]

,6

6. S. Lüssea, H. Claassen, T. Gehrke, J. Hassenpflug, M. Schünke, M. Heller, and C.-C. Glüer, “Evaluation of water content by spatially resolved transverse relaxation times of human articular cartilage,” Magn. Reson. Imaging 18(4), 423–430 (2000). [CrossRef] [PubMed]

].

Terahertz time-domain spectroscopy (THz TDS) has recently been developed because of recent advances in THz technology. THz TDS is a coherent and non-ionizing method that can quantify the complex refractive index from both the phase and amplitude information of a medium [7

7. B. B. Hu and M. C. Nuss, “Imaging with terahertz waves,” Opt. Lett. 20(16), 1716–1718 (1995). [CrossRef] [PubMed]

9

9. M. Tonouchi, “Cutting-edge terahertz technology,” Nat. Photonics 1(2), 97–105 (2007). [CrossRef]

]. Moreover, this method can also probe low frequency vibrational modes of biomolecules, thus providing structural and functional information about biological tissue [10

10. P. H. Siegel, “Terahertz technology in biology and medicine,” IEEE Trans. Microw. Theory Tech. 52(10), 2438–2447 (2004). [CrossRef]

]. Because water has strong absorptions across the entire THz frequency range, THz images will likely show a good image contrast dependent on the changes in medium water content. This enables THz TDS to be used for spectroscopic investigation of a biological medium.

To date, several biological tissues have been examined using this technique. For instance, characterization of human dental tissues [11

11. D. Crawley, C. Longbottom, V. P. Wallace, B. Cole, D. Arnone, and M. Pepper, “Three-dimensional terahertz pulse imaging of dental tissue,” J. Biomed. Opt. 8(2), 303–307 (2003). [CrossRef] [PubMed]

], basal cell carcinoma from both ex vivo and in vivo samples [12

12. R. M. Woodward, V. P. Wallace, R. J. Pye, B. E. Cole, D. D. Arnone, E. H. Linfield, and M. Pepper, “Terahertz pulse imaging of ex vivo basal cell carcinoma,” J. Invest. Dermatol. 120(1), 72–78 (2003). [CrossRef] [PubMed]

,13

13. V. P. Wallace, A. J. Fitzgerald, S. Shankar, N. Flanagan, R. Pye, J. Cluff, and D. D. Arnone, “Terahertz pulsed imaging of basal cell carcinoma ex vivo and in vivo,” Br. J. Dermatol. 151(2), 424–432 (2004). [CrossRef] [PubMed]

], and human cortical bone [14

14. M. R. Stringer, D. N. Lund, A. P. Foulds, A. Uddin, E. Berry, R. E. Miles, and A. G. Davies, “The analysis of human cortical bone by terahertz time-domain spectroscopy,” Phys. Med. Biol. 50(14), 3211–3219 (2005). [CrossRef] [PubMed]

] has been reported. More recently, human breast tumors [15

15. A. J. Fitzgerald, V. P. Wallace, M. Jimenez-Linan, L. Bobrow, R. J. Pye, A. D. Purushotham, and D. D. Arnone, “Terahertz pulsed imaging of human breast tumors,” Radiology 239(2), 533–540 (2006). [CrossRef] [PubMed]

] and micro-metastic lymph nodes [16

16. E.-A. Jung, M.-H. Lim, K.-W. Moon, Y.-W. Do, S.-S. Lee, H.-W. Han, H.-J. Choi, K.-S. Cho, and K.-R. Kim, “Terahertz pulse imaging of micro-metastatic lymph nodes in early-stage cervical cancer patients,” J. Opt. Soc. Korea 15(2), 155–160 (2011). [CrossRef]

] have been successfully investigated using THz TDS although the clinical application of THz TDS has not been demonstrated due to the high water absorption. However, no literature is available on the quantitative analysis of human articular cartilage in the THz region. Only THz reflection images of rabbit cartilage have been reported [17

17. W.-C. Kan, W.-S. Lee, W.-H. Cheung, V. P. Wallace, and E. Pickwell-Macpherson, “Terahertz pulsed imaging of knee cartilage,” Biomed. Opt. Express 1(3), 967–974 (2010). [CrossRef] [PubMed]

]. Here we report on the THz characterization of water distribution in human articular cartilage.

2. Materials and methods

The experimental setup was based on a conventional TDS system with transmission geometry. The THz pulse was generated by an InAs wafer pumped by a Ti:sapphire laser with a center wavelength of 790 nm, a pulse width of 100 fs, and a repetition rate of 80 MHz. The generated THz pulse was collimated and focused by off-axis parabolic mirrors. The cartilage sample was placed at the THz beam waist and moved on a motorized stage between two off-axis parabolic mirrors. The focal length of a set of off-axis parabolic mirrors was 5 cm. The scanned area was 3.5 × 2 mm2, and the scanning steps of the horizontal (x) and vertical (y) directions were 0.3 and 1 mm, respectively. The transmitted THz signal was detected by a photoconductive antenna fabricated on a low-temperature grown GaAs using standard optical gating and phase-sensitive detection techniques.

3. Results and discussion

Figure 2
Fig. 2 THz signals and transmitted amplitudes of reference and cartilage tissue.
shows the THz pulse signals and amplitude spectra with and without cartilage tissue with the transmitted THz pulses recorded at the center of cartilage sample (x = 1.0 and y = 1.0 mm). The transmitted THz pulse for the cartilage sample was significantly attenuated by absorption and Fresnel loss, and was ~10 times smaller than that of the reference signal. As a THz pulse propagates through an absorptive medium, such as a biological medium, the pulse width broadens due to the dispersion. The spectral amplitude transmitted through the cartilage tissue was found to be reduced over the entire THz frequency range (Fig. 2(b)).

Figure 4
Fig. 4 Refractive index images and absorption coefficient images of articular cartilage at 0.4 and 0.8 THz. The dashed lines indicate the cartilage surface.
shows the refractive index images and absorption coefficient images of cartilage tissue at 0.4 and 0.8 THz. The refractive index was relatively constant along the depth of cartilage at both 0.4 and 0.8 THz with the exception of the surface of the cartilage because of the diffraction. In the absorption coefficient image of the cartilage, the absorption was high at the articular surface and gradually decreased along the depth of the cartilage. The refractive indices and absorption coefficients along the depth of cartilage at specific frequencies are shown in Fig. 5
Fig. 5 (a) Refractive index profile and (b) absorption coefficient profile along the depth of cartilage tissue at 0.4 and 0.8 THz.
. At each frequency, the difference between the maximum and minimum values of the refractive index was less than 5% along the depth. In contrast, the absorption coefficient at each frequency significantly decreased from the articular surface to the subchondral bone. It has been known that the cartilage tissue is spatially heterogeneous and molecular composition of cartilage varies significantly in going from the articular surface to subchondral bone [1

1. A. R. Poole, T. Kojima, T. Yasuda, F. Mwale, M. Kobayashi, and S. Laverty, “Composition and structure of articular cartilage: a template for tissue repair,” Clin. Orthop. Relat. Res. 391(391Suppl), S26–S33 (2001). [CrossRef] [PubMed]

6

6. S. Lüssea, H. Claassen, T. Gehrke, J. Hassenpflug, M. Schünke, M. Heller, and C.-C. Glüer, “Evaluation of water content by spatially resolved transverse relaxation times of human articular cartilage,” Magn. Reson. Imaging 18(4), 423–430 (2000). [CrossRef] [PubMed]

]. Therefore we speculate that the alteration of absorption coefficient along the depth of the cartilage matrix may result primarily from changes in water content because water has a strong absorption in the THz frequency range.

4. Conclusion

Acknowledgments

This work was supported by the Basic Science Research Program (2009-0083512); the Priority Research Centers Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education, Science and Technology (2010-0029711); the Brain Korea 21 Project; and the IT Consilience Creative Program of MKE and NIPA (C1515-1121-0003).

References and links

1.

A. R. Poole, T. Kojima, T. Yasuda, F. Mwale, M. Kobayashi, and S. Laverty, “Composition and structure of articular cartilage: a template for tissue repair,” Clin. Orthop. Relat. Res. 391(391Suppl), S26–S33 (2001). [CrossRef] [PubMed]

2.

Y. Xia, T. Farquhar, N. Burton-Wurster, E. Ray, and L. W. Jelinski, “Diffusion and relaxation mapping of cartilage-bone plugs and excised disks using microscopic magnetic resonance imaging,” Magn. Reson. Med. 31(3), 273–282 (1994). [CrossRef] [PubMed]

3.

C.-B. James and T. L. Uhl, “A review of articular cartilage pathology and the use of glucosamine sulfate,” J. Athl. Train. 36(4), 413–419 (2001). [PubMed]

4.

H. J. Mankin and A. Z. Thrasher, “Water content and binding in normal and osteoarthritic human cartilage,” J. Bone Joint Surg. Am. 57(1), 76–80 (1975). [PubMed]

5.

C. Liess, S. Lüsse, N. Karger, M. Heller, and C.-C. Glüer, “Detection of changes in cartilage water content using MRI T2-mapping in vivo,” Osteoarthritis Cartilage 10(12), 907–913 (2002). [CrossRef] [PubMed]

6.

S. Lüssea, H. Claassen, T. Gehrke, J. Hassenpflug, M. Schünke, M. Heller, and C.-C. Glüer, “Evaluation of water content by spatially resolved transverse relaxation times of human articular cartilage,” Magn. Reson. Imaging 18(4), 423–430 (2000). [CrossRef] [PubMed]

7.

B. B. Hu and M. C. Nuss, “Imaging with terahertz waves,” Opt. Lett. 20(16), 1716–1718 (1995). [CrossRef] [PubMed]

8.

B. Ferguson and X.-C. Zhang, “Materials for terahertz science and technology,” Nat. Mater. 1(1), 26–33 (2002). [CrossRef] [PubMed]

9.

M. Tonouchi, “Cutting-edge terahertz technology,” Nat. Photonics 1(2), 97–105 (2007). [CrossRef]

10.

P. H. Siegel, “Terahertz technology in biology and medicine,” IEEE Trans. Microw. Theory Tech. 52(10), 2438–2447 (2004). [CrossRef]

11.

D. Crawley, C. Longbottom, V. P. Wallace, B. Cole, D. Arnone, and M. Pepper, “Three-dimensional terahertz pulse imaging of dental tissue,” J. Biomed. Opt. 8(2), 303–307 (2003). [CrossRef] [PubMed]

12.

R. M. Woodward, V. P. Wallace, R. J. Pye, B. E. Cole, D. D. Arnone, E. H. Linfield, and M. Pepper, “Terahertz pulse imaging of ex vivo basal cell carcinoma,” J. Invest. Dermatol. 120(1), 72–78 (2003). [CrossRef] [PubMed]

13.

V. P. Wallace, A. J. Fitzgerald, S. Shankar, N. Flanagan, R. Pye, J. Cluff, and D. D. Arnone, “Terahertz pulsed imaging of basal cell carcinoma ex vivo and in vivo,” Br. J. Dermatol. 151(2), 424–432 (2004). [CrossRef] [PubMed]

14.

M. R. Stringer, D. N. Lund, A. P. Foulds, A. Uddin, E. Berry, R. E. Miles, and A. G. Davies, “The analysis of human cortical bone by terahertz time-domain spectroscopy,” Phys. Med. Biol. 50(14), 3211–3219 (2005). [CrossRef] [PubMed]

15.

A. J. Fitzgerald, V. P. Wallace, M. Jimenez-Linan, L. Bobrow, R. J. Pye, A. D. Purushotham, and D. D. Arnone, “Terahertz pulsed imaging of human breast tumors,” Radiology 239(2), 533–540 (2006). [CrossRef] [PubMed]

16.

E.-A. Jung, M.-H. Lim, K.-W. Moon, Y.-W. Do, S.-S. Lee, H.-W. Han, H.-J. Choi, K.-S. Cho, and K.-R. Kim, “Terahertz pulse imaging of micro-metastatic lymph nodes in early-stage cervical cancer patients,” J. Opt. Soc. Korea 15(2), 155–160 (2011). [CrossRef]

17.

W.-C. Kan, W.-S. Lee, W.-H. Cheung, V. P. Wallace, and E. Pickwell-Macpherson, “Terahertz pulsed imaging of knee cartilage,” Biomed. Opt. Express 1(3), 967–974 (2010). [CrossRef] [PubMed]

18.

L. Ro̸nne, P.-O. Thrane, A. Åstrand, K. V. Wallqvist, Mikkelsen, and S. R. Keiding, “Investigation of the temperature dependence of dielectric relaxation in liquid water by THz reflection spectroscopy and molecular dynamics simulation,” J. Chem. Phys. 107(14), 5319–5331 (1997). [CrossRef]

19.

S. L. Chuang, Physics of Optoelectronic Devices (Wiley Interscience, New York, 1995), p. 209.

20.

R. Brocklehurst, M. T. Bayliss, A. Maroudas, H. L. Coysh, M. A. Freeman, P. A. Revell, and S. Y. Ali, “The composition of normal and osteoarthritic articular cartilage from human knee joints. With special reference to unicompartmental replacement and osteotomy of the knee,” J. Bone Joint Surg. Am. 66(1), 95–106 (1984). [PubMed]

21.

E. M. Shapiro, A. Borthakur, J. H. Kaufman, J. S. Leigh, and R. Reddy, “Water distribution patterns inside bovine articular cartilage as visualized by 1H magnetic resonance imaging,” Osteoarthritis Cartilage 9(6), 533–538 (2001). [CrossRef] [PubMed]

OCIS Codes
(000.1430) General : Biology and medicine
(110.6795) Imaging systems : Terahertz imaging

ToC Category:
Spectroscopic Diagnostics

History
Original Manuscript: January 31, 2012
Revised Manuscript: March 14, 2012
Manuscript Accepted: March 14, 2012
Published: April 25, 2012

Citation
Euna Jung, Hyuck Jae Choi, Meehyun Lim, Hyeona Kang, Hongkyu Park, Haewook Han, Byung-hyun Min, Sangin Kim, Ikmo Park, and Hanjo Lim, "Quantitative analysis of water distribution in human articular cartilage using terahertz time-domain spectroscopy," Biomed. Opt. Express 3, 1110-1115 (2012)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-3-5-1110


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References

  1. A. R. Poole, T. Kojima, T. Yasuda, F. Mwale, M. Kobayashi, and S. Laverty, “Composition and structure of articular cartilage: a template for tissue repair,” Clin. Orthop. Relat. Res. 391(391Suppl), S26–S33 (2001). [CrossRef] [PubMed]
  2. Y. Xia, T. Farquhar, N. Burton-Wurster, E. Ray, and L. W. Jelinski, “Diffusion and relaxation mapping of cartilage-bone plugs and excised disks using microscopic magnetic resonance imaging,” Magn. Reson. Med. 31(3), 273–282 (1994). [CrossRef] [PubMed]
  3. C.-B. James and T. L. Uhl, “A review of articular cartilage pathology and the use of glucosamine sulfate,” J. Athl. Train. 36(4), 413–419 (2001). [PubMed]
  4. H. J. Mankin and A. Z. Thrasher, “Water content and binding in normal and osteoarthritic human cartilage,” J. Bone Joint Surg. Am. 57(1), 76–80 (1975). [PubMed]
  5. C. Liess, S. Lüsse, N. Karger, M. Heller, and C.-C. Glüer, “Detection of changes in cartilage water content using MRI T2-mapping in vivo,” Osteoarthritis Cartilage 10(12), 907–913 (2002). [CrossRef] [PubMed]
  6. S. Lüssea, H. Claassen, T. Gehrke, J. Hassenpflug, M. Schünke, M. Heller, and C.-C. Glüer, “Evaluation of water content by spatially resolved transverse relaxation times of human articular cartilage,” Magn. Reson. Imaging 18(4), 423–430 (2000). [CrossRef] [PubMed]
  7. B. B. Hu and M. C. Nuss, “Imaging with terahertz waves,” Opt. Lett. 20(16), 1716–1718 (1995). [CrossRef] [PubMed]
  8. B. Ferguson and X.-C. Zhang, “Materials for terahertz science and technology,” Nat. Mater. 1(1), 26–33 (2002). [CrossRef] [PubMed]
  9. M. Tonouchi, “Cutting-edge terahertz technology,” Nat. Photonics 1(2), 97–105 (2007). [CrossRef]
  10. P. H. Siegel, “Terahertz technology in biology and medicine,” IEEE Trans. Microw. Theory Tech. 52(10), 2438–2447 (2004). [CrossRef]
  11. D. Crawley, C. Longbottom, V. P. Wallace, B. Cole, D. Arnone, and M. Pepper, “Three-dimensional terahertz pulse imaging of dental tissue,” J. Biomed. Opt. 8(2), 303–307 (2003). [CrossRef] [PubMed]
  12. R. M. Woodward, V. P. Wallace, R. J. Pye, B. E. Cole, D. D. Arnone, E. H. Linfield, and M. Pepper, “Terahertz pulse imaging of ex vivo basal cell carcinoma,” J. Invest. Dermatol. 120(1), 72–78 (2003). [CrossRef] [PubMed]
  13. V. P. Wallace, A. J. Fitzgerald, S. Shankar, N. Flanagan, R. Pye, J. Cluff, and D. D. Arnone, “Terahertz pulsed imaging of basal cell carcinoma ex vivo and in vivo,” Br. J. Dermatol. 151(2), 424–432 (2004). [CrossRef] [PubMed]
  14. M. R. Stringer, D. N. Lund, A. P. Foulds, A. Uddin, E. Berry, R. E. Miles, and A. G. Davies, “The analysis of human cortical bone by terahertz time-domain spectroscopy,” Phys. Med. Biol. 50(14), 3211–3219 (2005). [CrossRef] [PubMed]
  15. A. J. Fitzgerald, V. P. Wallace, M. Jimenez-Linan, L. Bobrow, R. J. Pye, A. D. Purushotham, and D. D. Arnone, “Terahertz pulsed imaging of human breast tumors,” Radiology 239(2), 533–540 (2006). [CrossRef] [PubMed]
  16. E.-A. Jung, M.-H. Lim, K.-W. Moon, Y.-W. Do, S.-S. Lee, H.-W. Han, H.-J. Choi, K.-S. Cho, and K.-R. Kim, “Terahertz pulse imaging of micro-metastatic lymph nodes in early-stage cervical cancer patients,” J. Opt. Soc. Korea 15(2), 155–160 (2011). [CrossRef]
  17. W.-C. Kan, W.-S. Lee, W.-H. Cheung, V. P. Wallace, and E. Pickwell-Macpherson, “Terahertz pulsed imaging of knee cartilage,” Biomed. Opt. Express 1(3), 967–974 (2010). [CrossRef] [PubMed]
  18. L. Ro̸nne, P.-O. Thrane, A. Åstrand, K. V. Wallqvist, Mikkelsen, and S. R. Keiding, “Investigation of the temperature dependence of dielectric relaxation in liquid water by THz reflection spectroscopy and molecular dynamics simulation,” J. Chem. Phys. 107(14), 5319–5331 (1997). [CrossRef]
  19. S. L. Chuang, Physics of Optoelectronic Devices (Wiley Interscience, New York, 1995), p. 209.
  20. R. Brocklehurst, M. T. Bayliss, A. Maroudas, H. L. Coysh, M. A. Freeman, P. A. Revell, and S. Y. Ali, “The composition of normal and osteoarthritic articular cartilage from human knee joints. With special reference to unicompartmental replacement and osteotomy of the knee,” J. Bone Joint Surg. Am. 66(1), 95–106 (1984). [PubMed]
  21. E. M. Shapiro, A. Borthakur, J. H. Kaufman, J. S. Leigh, and R. Reddy, “Water distribution patterns inside bovine articular cartilage as visualized by 1H magnetic resonance imaging,” Osteoarthritis Cartilage 9(6), 533–538 (2001). [CrossRef] [PubMed]

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