Gel wax-based tissue-mimicking phantoms for multispectral photoacoustic imaging

Tissue-mimicking phantoms are widely used for the calibration, evaluation and standardisation of medical imaging systems, and for clinical training. For photoacoustic imaging, tissue-mimicking materials (TMMs) that have tuneable optical and acoustic properties, high stability, and mechanical robustness are highly desired. In this study, gel wax is introduced as a TMM that satisfies these criteria for developing photoacoustic imaging phantoms. The reduced scattering and optical absorption coefficients were independently tuned with the addition of TiO2 and oil-based inks. The frequency-dependent acoustic attenuation obeyed a power law; for native gel wax, it varied from 0.71 dB/cm at 3 MHz to 9.93 dB/cm at 12 MHz. The chosen oil-based inks, which have different optical absorption spectra in the range of 400 to 900 nm, were found to have good photostability under pulsed illumination with photoacoustic excitation light. Optically heterogeneous phantoms that comprised of inclusions with different concentrations of carbon black and coloured inks were fabricated, and multispectral photoacoustic imaging was performed with an optical parametric oscillator and a planar Fabry-Pérot sensor. We conclude that gel wax is well suited as a TMM for multispectral photoacoustic imaging. Published by The Optical Society under the terms of the Creative Commons Attribution 4.0 License. Further distribution of this work must maintain attribution to the author(s) and the published article’s title, journal citation, and DOI. OCIS codes: (170.3880) Medical and biological imaging; (110.5120) Photoacoustic imaging; (170.7170) Ultrasound; (110.3000) Image quality assessment; (160.4760) Optical properties; (120.5820) Scattering measurements. References and links 1. P. Beard, “Biomedical Photoacoustic Imaging,” Interface Focus 1(4), 602–631 (2011). 2. L. V. Wang and S. Hu, “Photoacoustic tomography: in vivo imaging from organelles to organs,” Science 335(6075), 1458–1462 (2012). 3. V. Ntziachristos and D. Razansky, “Molecular imaging by means of multispectral optoacoustic tomography (MSOT),” Chem. Rev. 110(5), 2783–2794 (2010). 4. Y. Cao, A. Kole, L. Lan, P. Wang, J. Hui, M. Sturek, and J.-X. Cheng, “Spectral analysis assisted photoacoustic imaging for lipid composition differentiation,” Photoacoustics 7, 12–19 (2017). 5. M.A.L. Bell, A.K. Ostrowski, K. Li, P. Kazanzides, and E.M. Boctor, “Localization of transcranial targets for photoacoustic-guided endonasal surgeries,” Photoacoustics 3(2), 78–87 (2015). Vol. 9, No. 3 | 1 Mar 2018 | BIOMEDICAL OPTICS EXPRESS 1151 #309069 https://doi.org/10.1364/BOE.9.001151 Journal © 2018 Received 17 Oct 2017; revised 24 Jan 2018; accepted 26 Jan 2018; published 15 Feb 2018 6. J. R. Cook, R. R. Bouchard, and S. Y. Emelianov, “Tissue-mimicking phantoms for photoacoustic and ultrasonic imaging,” Biomed. Opt. Express 2(11), 3193–3206 (2011). 7. E. L. Madsen, M. A. Hobson, H. Shi, T. Varghese, and G. R. Frank, “Tissue-mimicking agar/gelatin materials for use in heterogeneous elastography phantoms,” Phys. Med. Biol. 50(23), 5597–5618 (2005). 8. P. Lai, X. Xu, and L.V. Wang, “Dependence of optical scattering from Intralipid in gelatin-gel based tissue-mimicking phantoms on mixing temperature and time,” J. Biomed. Opt. 19(3), 035002 (2014). 9. J. C. Hebden, D. J. Hall, M. Firbank, and D. T. Delpy, “Time-resolved optical imaging of a solid tissue-equivalent phantom,” Appl. Opt. 34(34), 8038–8047 (1995). 10. M. Firbank, M. Oda, and D. T. Delpy, “An improved design for a stable and reproducible phantom material for use in near-infrared spectroscopy and imaging,” Phys. Med. Biol. 40(5), 955–961 (1995). 11. D. M. de Bruin, R. H. Bremmer, V. M. Kodach, R. de Kinkelder, J. van Marle, T. G. van Leeuwen, and D. J. Faber, “Optical phantoms of varying geometry based on thin building blocks with controlled optical properties,” J. Biomed. Opt. 15(2), 025001 (2010). 12. M. M. Jalili, S. Y. Mousavi, and A. S. Pirayeshfar, “Investigating the acoustical properties of carbon fiber-, glass fiber-, and hemp fiber-reinforced polyester composites,” Polym. Compos. 35(11), 2103–2111 (2014). 13. K. Zell, J. I. Sperl, M. W. Vogel, R. Niessner, and C. Haisch, “Acoustical properties of selected tissue phantom materials for ultrasound imaging,” Phys. Med. Biol. 52(20), N475–N484 (2007). 14. J. E. Browne, K. V. Ramnarine, A. J. Watson, and P. R. Hoskins, “Assessment of the acoustic properties of common tissue-mimicking test phantoms,” Ultrasound Med. Biol. 29(7), 1053–1060 (2003). 15. B. W. Pogue and M. S. Patterson, “Review of tissue simulating phantoms for optical spectroscopy, imaging and dosimetry,” J. Biomed. Opt. 11(4), 041102 (2006). 16. K. J. M. Surry, H. J. B. Austin, A. Fenster, and T. M. Peters, “Poly(vinyl alcohol) cryogel phantoms for use in ultrasound and MR imaging,” Phys. Med. Biol. 49(24), 5529–5546 (2004). 17. A. Kharine, S. Manohar, R. Seeton, R. G. M. Kolkman, R. A. Bolt, W. Steenbergen, and F. F. M. de Mul, “Poly(vinyl alcohol) gels for use as tissue phantoms in photoacoustic mammography,” Phys. Med. Biol.48(3), 357–370 (2003). 18. S. Manohar, A. Kharine, J.C.G. van Hespen, W. Steenbergen, and T. G. van Leeuwen, “Photoacoustic mammography laboratory prototype: imaging of breast tissue phantoms,” J. Biomed. Opt. 9(6), 1172–1181 (2004). 19. W. Xia, D. Piras, M. Heijblom, W. Steenbergen, T. G. van Leeuwen, and S. Manohar, “Poly(vinyl alcohol) gels as photoacoustic breast phantoms revisited,” J. Biomed. Opt. 16(7), 075002 (2011). 20. D. Razansky, J. Baeten, and V. Ntziachristos, “Sensitivity of molecular target detection by multispectral optoacoustic tomography (MSOT),” Med. Phys, 36(3), 939–945 (2009). 21. P.D. Kumavor, C. Xu, A. Aguirre, J. Gamelin, Y. Ardeshirpour, B. Tavakoli, S. Zanganeh, U. Alqasemi, Y. Yang, and Q. Zhu, “Target detection and quantification using a hybrid hand-held diffuse optical tomography and photoacoustic tomography system,” J. Biomed. Opt. 16(4), 046010 (2011). 22. G. M. Spirou, A. A. Oraevsky, I. A. Vitkin, and W. M. Whelan, “Optical and acoustic properties at 1064 nm of polyvinyl chloride-plastisol for use as a tissue phantom in biomedical optoacoustics,” Phys. Med. Biol. 50(14), N141–N153 (2005). 23. S. E. Bohndiek, S. Bodapati, D. Van De Sompel, S. R. Kothapalli, and S. S. Gambhir, “Development and application of stable phantoms for the evaluation of photoacoustic imaging instruments,” PLoS one 8(9), e75533 (2013). 24. W. C. Vogt, C. Jia, K. A. Wear, B. S. Garra, and T. Joshua Pfefer, “Biologically relevant photoacoustic imaging phantoms with tunable optical and acoustic properties,” J. Biomed. Opt. 21(10), 101405 (2016). 25. M. Fonseca, B. Zeqiri, P. C. Beard, and B. T. Cox, “Characterisation of a phantom for multiwavelength quantitative photoacoustic imaging,” Phys. Med. Biol. 61(13), 4950–4973 (2016). 26. T. D. Mast, “Empirical relationships between acoustic parameters in human soft tissues,” Acoust. Res. Lett. Online 1, 37–42 (2000). 27. S. L. Vieira, T. Z. Pavan, J. E. Junior, and A. A. O. Carneiro, “Paraffin-gel tissue-mimicking material for ultrasoundguided needle biopsy phantom,” Ultrasound Med. Biol. 39(12), 2477–2484 (2013). 28. J. Oudry, C. Bastard, V. Miette, R. Willinger, and L. Sandrin, “Copolymer-in-oil phantom materials for elastography,” Ultrasound Med. Biol. 35(7), 1185–1197 (2009). 29. L. C. Cabrelli, P. I. B. G. B. Pelissari, A. M. Deana, A. A. O. Carneiro, and T. Z. Pavan, “Stable phantom materials for ultrasound and optical imaging,” Phys. Med. Biol. 62(2), 432–447 (2017). 30. R. X. Xu, J. Ewing, H. El-Dahdah, B. Wang, and S. P. Povoski, “Design and benchtop validation of a handheld integrated dynamic breast imaging system for noninvasive characterization of suspicious breast lesions,” Technol. Cancer Res. Treat. 7(6), 471–481 (2008). 31. E. Dong, Z. Zhao, M. Wang, Y. Xie, S. Li, P. Shao, L. Cheng, and R. X. Xu, “Three-dimensional fuse deposition modeling of tissue-simulating phantom for biomedical optical imaging,” J. Biomed. Opt. 20(12), 121311 (2015). 32. E. Maneas, W. Xia, D. I. Nikitichev, B. Daher, M. Manimaran, R. Y. J. Wong, B. Rahmani, C. Capelli, S. Schievano, G. Burriesci, S. Ourselin, A. L. David, S. J. West, M. Finlay, T. Vercauteren, and A. E. Desjardins, “Anatomically realistic ultrasound phantoms using gel wax with 3D printed moulds,” Phys. Med. Biol. 63, 015033 (2018). 33. S. A. Prahl, M. J. C. van Gemert, and A. J. Welch, “Determining the optical properties of turbid media by using the adding-doubling method,” Appl. Opt. 32(4), 559 (1993). 34. N. Bilaniuk and G. S. K. Wong, “Speed of sound in pure water as a function of temperature,” J. Acoust. Soc. Am. 93(3), 1609–1612 (1993). Vol. 9, No. 3 | 1 Mar 2018 | BIOMEDICAL OPTICS EXPRESS 1152

[1]  Adrien E Desjardins,et al.  Construction of 3‐Dimensional Printed Ultrasound Phantoms With Wall‐less Vessels , 2016, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[2]  A. Welch,et al.  Determining the optical properties of turbid mediaby using the adding-doubling method. , 1993, Applied optics.

[3]  Minjie Wang,et al.  Three-dimensional fuse deposition modeling of tissue-simulating phantom for biomedical optical imaging , 2015, Journal of biomedical optics.

[4]  George S. K. Wong,et al.  Speed of sound in pure water as a function of temperature , 1993 .

[5]  B T Cox,et al.  k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields. , 2010, Journal of biomedical optics.

[6]  D. Delpy,et al.  An improved design for a stable and reproducible phantom material for use in near-infrared spectroscopy and imaging. , 1995, Physics in medicine and biology.

[7]  Wiendelt Steenbergen,et al.  Poly(vinyl alcohol) gels as photoacoustic breast phantoms revisited. , 2011, Journal of biomedical optics.

[8]  Luciana C. Cabrelli,et al.  Stable phantom materials for ultrasound and optical imaging , 2017, Physics in medicine and biology.

[9]  H. V. van Beusekom,et al.  Intravascular photoacoustic imaging of human coronary atherosclerosis. , 2011, Optics letters.

[10]  T. D. Mast Empirical relationships between acoustic parameters in human soft tissues , 2000 .

[11]  Puxiang Lai,et al.  Dependence of optical scattering from Intralipid in gelatin-gel based tissue-mimicking phantoms on mixing temperature and time , 2014, Journal of biomedical optics.

[12]  R. Xu,et al.  Design and Benchtop Validation of a Handheld Integrated Dynamic Breast Imaging System for Noninvasive Characterization of Suspicious Breast Lesions , 2008, Technology in cancer research & treatment.

[13]  R Willinger,et al.  Copolymer-in-oil phantom materials for elastography. , 2009, Ultrasound in medicine & biology.

[14]  P. Beard Biomedical photoacoustic imaging , 2011, Interface Focus.

[15]  Daniil I. Nikitichev,et al.  Anatomically realistic ultrasound phantoms using gel wax with 3D printed moulds , 2018, Physics in medicine and biology.

[16]  T. Stahl,et al.  Characterization of the thermalisation efficiency and photostability of photoacoustic contrast agents , 2014, Photonics West - Biomedical Optics.

[17]  J. Mari,et al.  Interventional multispectral photoacoustic imaging with a clinical ultrasound probe for discriminating nerves and tendons: an ex vivo pilot study. , 2015, Journal of biomedical optics.

[18]  Jan Laufer,et al.  Evaluation of Absorbing Chromophores Used in Tissue Phantoms for Quantitative Photoacoustic Spectroscopy and Imaging , 2010, IEEE Journal of Selected Topics in Quantum Electronics.

[19]  Alexander A Oraevsky,et al.  Optical and acoustic properties at 1064 nm of polyvinyl chloride-plastisol for use as a tissue phantom in biomedical optoacoustics , 2005, Physics in medicine and biology.

[20]  D. D. de Bruin,et al.  Optical phantoms of varying geometry based on thin building blocks with controlled optical properties. , 2010, Journal of biomedical optics.

[21]  T. Peters,et al.  Poly(vinyl alcohol) cryogel phantoms for use in ultrasound and MR imaging , 2004, Physics in medicine and biology.

[22]  Adrien E Desjardins,et al.  Development of an Ultrasound Phantom for Spinal Injections With 3-Dimensional Printing , 2014, Regional Anesthesia & Pain Medicine.

[23]  A. Kole,et al.  Spectral analysis assisted photoacoustic imaging for lipid composition differentiation , 2017, Photoacoustics.

[24]  S. Jacques Optical properties of biological tissues: a review , 2013, Physics in medicine and biology.

[25]  Jan Laufer,et al.  Backward-mode multiwavelength photoacoustic scanner using a planar Fabry-Perot polymer film ultrasound sensor for high-resolution three-dimensional imaging of biological tissues. , 2008, Applied optics.

[26]  Wiendelt Steenbergen,et al.  Poly(vinyl alcohol) gels for use as tissue phantoms in photoacoustic mammography. , 2003, Physics in medicine and biology.

[27]  B T Cox,et al.  Characterisation of a phantom for multiwavelength quantitative photoacoustic imaging , 2016, Physics in medicine and biology.

[28]  P. Hoskins,et al.  Assessment of the acoustic properties of common tissue-mimicking test phantoms. , 2003, Ultrasound in medicine & biology.

[29]  M. Jalili,et al.  Investigating the acoustical properties of carbon fiber‐, glass fiber‐, and hemp fiber‐reinforced polyester composites , 2014, 1511.04543.

[30]  Sanjiv S. Gambhir,et al.  Development and Application of Stable Phantoms for the Evaluation of Photoacoustic Imaging Instruments , 2013, PloS one.

[31]  Wiendelt Steenbergen,et al.  Photoacoustic mammography laboratory prototype: imaging of breast tissue phantoms. , 2004, Journal of biomedical optics.

[32]  M. B. van der Mark,et al.  Estimation of lipid and water concentrations in scattering media with diffuse optical spectroscopy from 900 to 1,600 nm. , 2010, Journal of biomedical optics.

[33]  D. Delpy,et al.  Time-resolved optical imaging of a solid tissue-equivalent phantom. , 1995, Applied optics.

[34]  B. Pogue,et al.  Review of tissue simulating phantoms for optical spectroscopy, imaging and dosimetry. , 2006, Journal of biomedical optics.

[35]  V. Ntziachristos,et al.  Molecular imaging by means of multispectral optoacoustic tomography (MSOT). , 2010, Chemical reviews.

[36]  Sebastien Ourselin,et al.  Performance characteristics of an interventional multispectral photoacoustic imaging system for guiding minimally invasive procedures , 2015, Journal of biomedical optics.

[37]  Lihong V. Wang,et al.  Photoacoustic Tomography: In Vivo Imaging from Organelles to Organs , 2012, Science.

[38]  R. Niessner,et al.  Acoustical properties of selected tissue phantom materials for ultrasound imaging , 2007, Physics in medicine and biology.

[39]  S. Arridge,et al.  Quantitative spectroscopic photoacoustic imaging: a review. , 2012, Journal of biomedical optics.

[40]  S. Emelianov,et al.  Tissue-mimicking phantoms for photoacoustic and ultrasonic imaging , 2011, Biomedical optics express.

[41]  Congxian Jia,et al.  Biologically relevant photoacoustic imaging phantoms with tunable optical and acoustic properties , 2016, Journal of biomedical optics.

[42]  Vasilis Ntziachristos,et al.  Unmixing Molecular Agents From Absorbing Tissue in Multispectral Optoacoustic Tomography , 2014, IEEE Transactions on Medical Imaging.

[43]  T. Varghese,et al.  Tissue-mimicking agar/gelatin materials for use in heterogeneous elastography phantoms , 2005, Physics in medicine and biology.

[44]  A. Carneiro,et al.  Paraffin-gel tissue-mimicking material for ultrasound-guided needle biopsy phantom. , 2013, Ultrasound in medicine & biology.

[45]  P. Kumavor,et al.  Target detection and quantification using a hybrid hand-held diffuse optical tomography and photoacoustic tomography system. , 2011, Journal of biomedical optics.

[46]  Vasilis Ntziachristos,et al.  Sensitivity of molecular target detection by multispectral optoacoustic tomography (MSOT). , 2009, Medical physics.