Abstract

Colorectal cancer is the second leading cause of cancer death in the United States. Significant limitations in screening and surveillance modalities continue to hamper early detection of primary cancers or recurrences after therapy. In this study, we describe a new registered ultrasound (US) and acoustic-resolution photoacoustic microscopy (AR-PAM) system and report its initial testing in ex vivo human colorectal tissue. A total of 8 colorectal specimens were imaged, which included 2 polyps, 4 malignant colon cancers, and 2 treated colorectal cancers. In each specimen, normal tissue was also imaged for internal control. Initial data have demonstrated the feasibility of identifying colorectal cancer imaging features and the invasion depth using co-registered US and an AR-PAM system. In normal tissue, we found that our system consistently demonstrates the multi-layer structure of normal colonic tissue while differentiating layers with elevated vascularity; these findings highly correlated with histologic findings of each specimen. For malignant colorectal samples, the tissue structure is highly disorganized as seen in US, and photoacoustic imaging revealed distorted vascular distribution inside the tumor. Notably, AR-PAM of tumor beds after complete tumor destruction by radiation and chemotherapy yielded a pattern identical to benign tissue. Quantitative analysis of photoacoustic spectral slope has demonstrated more high-frequency components in malignant tissue as compared to the normal colon tissue, which may be caused by significantly increased microvessel networks. In summary, we demonstrate the successful differentiation of benign and malignant colorectal tissue with our co-registered ultrasound and photoacoustic system.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref]
  7. J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
    [Crossref] [PubMed]
  8. J.-M. Yang, C. Li, R. Chen, B. Rao, J. Yao, C.-H. Yeh, A. Danielli, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Optical-resolution photoacoustic endomicroscopy in vivo,” Biomed. Opt. Express 6(3), 918–932 (2015).
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2017 (1)

R. L. Siegel, K. D. Miller, S. A. Fedewa, D. J. Ahnen, R. G. S. Meester, A. Barzi, and A. Jemal, “Colorectal cancer statistics, 2017,” CA Cancer J. Clin. 67(3), 177–193 (2017).
[Crossref] [PubMed]

2016 (1)

H. S. Salehi, H. Li, A. Merkulov, P. D. Kumavor, H. Vavadi, M. Sanders, A. Kueck, M. A. Brewer, and Q. Zhu, “Coregistered photoacoustic and ultrasound imaging and classification of ovarian cancer: ex vivo and in vivo studies,” J. Biomed. Opt. 21(4), 46006 (2016).
[Crossref] [PubMed]

2015 (2)

H. Li, P. Kumavor, U. Salman Alqasemi, and Q. Zhu, “Utilizing spatial and spectral features of photoacoustic imaging for ovarian cancer detection and diagnosis,” J. Biomed. Opt. 20(1), 016002 (2015).
[Crossref] [PubMed]

J.-M. Yang, C. Li, R. Chen, B. Rao, J. Yao, C.-H. Yeh, A. Danielli, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Optical-resolution photoacoustic endomicroscopy in vivo,” Biomed. Opt. Express 6(3), 918–932 (2015).
[Crossref] [PubMed]

2014 (2)

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

P. V. Chitnis, J. Mamou, and E. J. Feleppa, “Spectrum analysis of photoacoustic signals for characterizing lymph nodes,” J. Acoust. Soc. Am. 135(4), 2372 (2014).
[Crossref]

2013 (2)

J. Yao and L. V. Wang, “Photoacoustic Microscopy,” Laser Photonics Rev. 7(5), 758–778 (2013).
[Crossref] [PubMed]

E. M. Strohm, E .S. L. Berndl, and M. C. Kolios, “Probing red blood cell morphology using high-frequency photoacoustic,” Biophys. J. 105(1), 59 (2013).
[Crossref] [PubMed]

2012 (3)

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

L. V. Wang and S. Hu, “Photoacoustic tomography: in vivo imaging from organelles to organs,” Science 335(6075), 1458–1462 (2012).
[Crossref] [PubMed]

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt. 17(5), 056016 (2012).
[Crossref] [PubMed]

2010 (1)

S. Hu and L. V. Wang, “Photoacoustic imaging and characterization of the microvasculature,” J. Biomed. Opt. 15(1), 011101 (2010).
[Crossref] [PubMed]

2006 (2)

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[Crossref]

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[Crossref]

2002 (1)

S. P. Hiotis, S. M. Weber, A. M. Cohen, B. D. Minsky, P. B. Paty, J. G. Guillem, R. Wagman, L. B. Saltz, and W. D. Wong, “Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients,” J. Am. Coll. Surg. 194(2), 131–135 (2002).
[Crossref] [PubMed]

Ahnen, D. J.

R. L. Siegel, K. D. Miller, S. A. Fedewa, D. J. Ahnen, R. G. S. Meester, A. Barzi, and A. Jemal, “Colorectal cancer statistics, 2017,” CA Cancer J. Clin. 67(3), 177–193 (2017).
[Crossref] [PubMed]

Barzi, A.

R. L. Siegel, K. D. Miller, S. A. Fedewa, D. J. Ahnen, R. G. S. Meester, A. Barzi, and A. Jemal, “Colorectal cancer statistics, 2017,” CA Cancer J. Clin. 67(3), 177–193 (2017).
[Crossref] [PubMed]

Beard, P.

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt. 17(5), 056016 (2012).
[Crossref] [PubMed]

Berndl, E .S. L.

E. M. Strohm, E .S. L. Berndl, and M. C. Kolios, “Probing red blood cell morphology using high-frequency photoacoustic,” Biophys. J. 105(1), 59 (2013).
[Crossref] [PubMed]

Brewer, M. A.

H. S. Salehi, H. Li, A. Merkulov, P. D. Kumavor, H. Vavadi, M. Sanders, A. Kueck, M. A. Brewer, and Q. Zhu, “Coregistered photoacoustic and ultrasound imaging and classification of ovarian cancer: ex vivo and in vivo studies,” J. Biomed. Opt. 21(4), 46006 (2016).
[Crossref] [PubMed]

Cai, X.

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Carson, P. L.

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Chen, R.

J.-M. Yang, C. Li, R. Chen, B. Rao, J. Yao, C.-H. Yeh, A. Danielli, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Optical-resolution photoacoustic endomicroscopy in vivo,” Biomed. Opt. Express 6(3), 918–932 (2015).
[Crossref] [PubMed]

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Chitnis, P. V.

P. V. Chitnis, J. Mamou, and E. J. Feleppa, “Spectrum analysis of photoacoustic signals for characterizing lymph nodes,” J. Acoust. Soc. Am. 135(4), 2372 (2014).
[Crossref]

Cohen, A. M.

S. P. Hiotis, S. M. Weber, A. M. Cohen, B. D. Minsky, P. B. Paty, J. G. Guillem, R. Wagman, L. B. Saltz, and W. D. Wong, “Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients,” J. Am. Coll. Surg. 194(2), 131–135 (2002).
[Crossref] [PubMed]

Cox, B.

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt. 17(5), 056016 (2012).
[Crossref] [PubMed]

Danielli, A.

Favazza, C.

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Fedewa, S. A.

R. L. Siegel, K. D. Miller, S. A. Fedewa, D. J. Ahnen, R. G. S. Meester, A. Barzi, and A. Jemal, “Colorectal cancer statistics, 2017,” CA Cancer J. Clin. 67(3), 177–193 (2017).
[Crossref] [PubMed]

Feleppa, E. J.

P. V. Chitnis, J. Mamou, and E. J. Feleppa, “Spectrum analysis of photoacoustic signals for characterizing lymph nodes,” J. Acoust. Soc. Am. 135(4), 2372 (2014).
[Crossref]

Guillem, J. G.

S. P. Hiotis, S. M. Weber, A. M. Cohen, B. D. Minsky, P. B. Paty, J. G. Guillem, R. Wagman, L. B. Saltz, and W. D. Wong, “Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients,” J. Am. Coll. Surg. 194(2), 131–135 (2002).
[Crossref] [PubMed]

Hiotis, S. P.

S. P. Hiotis, S. M. Weber, A. M. Cohen, B. D. Minsky, P. B. Paty, J. G. Guillem, R. Wagman, L. B. Saltz, and W. D. Wong, “Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients,” J. Am. Coll. Surg. 194(2), 131–135 (2002).
[Crossref] [PubMed]

Hu, S.

L. V. Wang and S. Hu, “Photoacoustic tomography: in vivo imaging from organelles to organs,” Science 335(6075), 1458–1462 (2012).
[Crossref] [PubMed]

S. Hu and L. V. Wang, “Photoacoustic imaging and characterization of the microvasculature,” J. Biomed. Opt. 15(1), 011101 (2010).
[Crossref] [PubMed]

Jemal, A.

R. L. Siegel, K. D. Miller, S. A. Fedewa, D. J. Ahnen, R. G. S. Meester, A. Barzi, and A. Jemal, “Colorectal cancer statistics, 2017,” CA Cancer J. Clin. 67(3), 177–193 (2017).
[Crossref] [PubMed]

Johnson, P.

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt. 17(5), 056016 (2012).
[Crossref] [PubMed]

Joshi, B.

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Kolios, M. C.

E. M. Strohm, E .S. L. Berndl, and M. C. Kolios, “Probing red blood cell morphology using high-frequency photoacoustic,” Biophys. J. 105(1), 59 (2013).
[Crossref] [PubMed]

Kueck, A.

H. S. Salehi, H. Li, A. Merkulov, P. D. Kumavor, H. Vavadi, M. Sanders, A. Kueck, M. A. Brewer, and Q. Zhu, “Coregistered photoacoustic and ultrasound imaging and classification of ovarian cancer: ex vivo and in vivo studies,” J. Biomed. Opt. 21(4), 46006 (2016).
[Crossref] [PubMed]

Kumavor, P.

H. Li, P. Kumavor, U. Salman Alqasemi, and Q. Zhu, “Utilizing spatial and spectral features of photoacoustic imaging for ovarian cancer detection and diagnosis,” J. Biomed. Opt. 20(1), 016002 (2015).
[Crossref] [PubMed]

Kumavor, P. D.

H. S. Salehi, H. Li, A. Merkulov, P. D. Kumavor, H. Vavadi, M. Sanders, A. Kueck, M. A. Brewer, and Q. Zhu, “Coregistered photoacoustic and ultrasound imaging and classification of ovarian cancer: ex vivo and in vivo studies,” J. Biomed. Opt. 21(4), 46006 (2016).
[Crossref] [PubMed]

Laufer, J.

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt. 17(5), 056016 (2012).
[Crossref] [PubMed]

Li, C.

Li, H.

H. S. Salehi, H. Li, A. Merkulov, P. D. Kumavor, H. Vavadi, M. Sanders, A. Kueck, M. A. Brewer, and Q. Zhu, “Coregistered photoacoustic and ultrasound imaging and classification of ovarian cancer: ex vivo and in vivo studies,” J. Biomed. Opt. 21(4), 46006 (2016).
[Crossref] [PubMed]

H. Li, P. Kumavor, U. Salman Alqasemi, and Q. Zhu, “Utilizing spatial and spectral features of photoacoustic imaging for ovarian cancer detection and diagnosis,” J. Biomed. Opt. 20(1), 016002 (2015).
[Crossref] [PubMed]

Lin, J. D.

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Mamou, J.

P. V. Chitnis, J. Mamou, and E. J. Feleppa, “Spectrum analysis of photoacoustic signals for characterizing lymph nodes,” J. Acoust. Soc. Am. 135(4), 2372 (2014).
[Crossref]

Maslov, K.

J.-M. Yang, C. Li, R. Chen, B. Rao, J. Yao, C.-H. Yeh, A. Danielli, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Optical-resolution photoacoustic endomicroscopy in vivo,” Biomed. Opt. Express 6(3), 918–932 (2015).
[Crossref] [PubMed]

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Meester, R. G. S.

R. L. Siegel, K. D. Miller, S. A. Fedewa, D. J. Ahnen, R. G. S. Meester, A. Barzi, and A. Jemal, “Colorectal cancer statistics, 2017,” CA Cancer J. Clin. 67(3), 177–193 (2017).
[Crossref] [PubMed]

Meng, Z.-X.

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Merkulov, A.

H. S. Salehi, H. Li, A. Merkulov, P. D. Kumavor, H. Vavadi, M. Sanders, A. Kueck, M. A. Brewer, and Q. Zhu, “Coregistered photoacoustic and ultrasound imaging and classification of ovarian cancer: ex vivo and in vivo studies,” J. Biomed. Opt. 21(4), 46006 (2016).
[Crossref] [PubMed]

Miller, K. D.

R. L. Siegel, K. D. Miller, S. A. Fedewa, D. J. Ahnen, R. G. S. Meester, A. Barzi, and A. Jemal, “Colorectal cancer statistics, 2017,” CA Cancer J. Clin. 67(3), 177–193 (2017).
[Crossref] [PubMed]

Minsky, B. D.

S. P. Hiotis, S. M. Weber, A. M. Cohen, B. D. Minsky, P. B. Paty, J. G. Guillem, R. Wagman, L. B. Saltz, and W. D. Wong, “Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients,” J. Am. Coll. Surg. 194(2), 131–135 (2002).
[Crossref] [PubMed]

Paty, P. B.

S. P. Hiotis, S. M. Weber, A. M. Cohen, B. D. Minsky, P. B. Paty, J. G. Guillem, R. Wagman, L. B. Saltz, and W. D. Wong, “Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients,” J. Am. Coll. Surg. 194(2), 131–135 (2002).
[Crossref] [PubMed]

Pedley, B.

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt. 17(5), 056016 (2012).
[Crossref] [PubMed]

Rao, B.

Salehi, H. S.

H. S. Salehi, H. Li, A. Merkulov, P. D. Kumavor, H. Vavadi, M. Sanders, A. Kueck, M. A. Brewer, and Q. Zhu, “Coregistered photoacoustic and ultrasound imaging and classification of ovarian cancer: ex vivo and in vivo studies,” J. Biomed. Opt. 21(4), 46006 (2016).
[Crossref] [PubMed]

Salman Alqasemi, U.

H. Li, P. Kumavor, U. Salman Alqasemi, and Q. Zhu, “Utilizing spatial and spectral features of photoacoustic imaging for ovarian cancer detection and diagnosis,” J. Biomed. Opt. 20(1), 016002 (2015).
[Crossref] [PubMed]

Saltz, L. B.

S. P. Hiotis, S. M. Weber, A. M. Cohen, B. D. Minsky, P. B. Paty, J. G. Guillem, R. Wagman, L. B. Saltz, and W. D. Wong, “Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients,” J. Am. Coll. Surg. 194(2), 131–135 (2002).
[Crossref] [PubMed]

Sanders, M.

H. S. Salehi, H. Li, A. Merkulov, P. D. Kumavor, H. Vavadi, M. Sanders, A. Kueck, M. A. Brewer, and Q. Zhu, “Coregistered photoacoustic and ultrasound imaging and classification of ovarian cancer: ex vivo and in vivo studies,” J. Biomed. Opt. 21(4), 46006 (2016).
[Crossref] [PubMed]

Shung, K. K.

J.-M. Yang, C. Li, R. Chen, B. Rao, J. Yao, C.-H. Yeh, A. Danielli, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Optical-resolution photoacoustic endomicroscopy in vivo,” Biomed. Opt. Express 6(3), 918–932 (2015).
[Crossref] [PubMed]

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Siegel, R. L.

R. L. Siegel, K. D. Miller, S. A. Fedewa, D. J. Ahnen, R. G. S. Meester, A. Barzi, and A. Jemal, “Colorectal cancer statistics, 2017,” CA Cancer J. Clin. 67(3), 177–193 (2017).
[Crossref] [PubMed]

Strohm, E. M.

E. M. Strohm, E .S. L. Berndl, and M. C. Kolios, “Probing red blood cell morphology using high-frequency photoacoustic,” Biophys. J. 105(1), 59 (2013).
[Crossref] [PubMed]

Treeby, B.

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt. 17(5), 056016 (2012).
[Crossref] [PubMed]

Vavadi, H.

H. S. Salehi, H. Li, A. Merkulov, P. D. Kumavor, H. Vavadi, M. Sanders, A. Kueck, M. A. Brewer, and Q. Zhu, “Coregistered photoacoustic and ultrasound imaging and classification of ovarian cancer: ex vivo and in vivo studies,” J. Biomed. Opt. 21(4), 46006 (2016).
[Crossref] [PubMed]

Wagman, R.

S. P. Hiotis, S. M. Weber, A. M. Cohen, B. D. Minsky, P. B. Paty, J. G. Guillem, R. Wagman, L. B. Saltz, and W. D. Wong, “Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients,” J. Am. Coll. Surg. 194(2), 131–135 (2002).
[Crossref] [PubMed]

Wang, L. V.

J.-M. Yang, C. Li, R. Chen, B. Rao, J. Yao, C.-H. Yeh, A. Danielli, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Optical-resolution photoacoustic endomicroscopy in vivo,” Biomed. Opt. Express 6(3), 918–932 (2015).
[Crossref] [PubMed]

J. Yao and L. V. Wang, “Photoacoustic Microscopy,” Laser Photonics Rev. 7(5), 758–778 (2013).
[Crossref] [PubMed]

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

L. V. Wang and S. Hu, “Photoacoustic tomography: in vivo imaging from organelles to organs,” Science 335(6075), 1458–1462 (2012).
[Crossref] [PubMed]

S. Hu and L. V. Wang, “Photoacoustic imaging and characterization of the microvasculature,” J. Biomed. Opt. 15(1), 011101 (2010).
[Crossref] [PubMed]

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[Crossref]

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[Crossref]

Wang, X.

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Weber, S. M.

S. P. Hiotis, S. M. Weber, A. M. Cohen, B. D. Minsky, P. B. Paty, J. G. Guillem, R. Wagman, L. B. Saltz, and W. D. Wong, “Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients,” J. Am. Coll. Surg. 194(2), 131–135 (2002).
[Crossref] [PubMed]

Wong, W. D.

S. P. Hiotis, S. M. Weber, A. M. Cohen, B. D. Minsky, P. B. Paty, J. G. Guillem, R. Wagman, L. B. Saltz, and W. D. Wong, “Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients,” J. Am. Coll. Surg. 194(2), 131–135 (2002).
[Crossref] [PubMed]

Xu, G.

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Xu, M.

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[Crossref]

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[Crossref]

Yang, J.-M.

J.-M. Yang, C. Li, R. Chen, B. Rao, J. Yao, C.-H. Yeh, A. Danielli, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Optical-resolution photoacoustic endomicroscopy in vivo,” Biomed. Opt. Express 6(3), 918–932 (2015).
[Crossref] [PubMed]

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Yao, J.

J.-M. Yang, C. Li, R. Chen, B. Rao, J. Yao, C.-H. Yeh, A. Danielli, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Optical-resolution photoacoustic endomicroscopy in vivo,” Biomed. Opt. Express 6(3), 918–932 (2015).
[Crossref] [PubMed]

J. Yao and L. V. Wang, “Photoacoustic Microscopy,” Laser Photonics Rev. 7(5), 758–778 (2013).
[Crossref] [PubMed]

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Yeh, C.-H.

Yuan, J.

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Zhang, E.

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt. 17(5), 056016 (2012).
[Crossref] [PubMed]

Zhou, Q.

J.-M. Yang, C. Li, R. Chen, B. Rao, J. Yao, C.-H. Yeh, A. Danielli, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Optical-resolution photoacoustic endomicroscopy in vivo,” Biomed. Opt. Express 6(3), 918–932 (2015).
[Crossref] [PubMed]

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Zhu, Q.

H. S. Salehi, H. Li, A. Merkulov, P. D. Kumavor, H. Vavadi, M. Sanders, A. Kueck, M. A. Brewer, and Q. Zhu, “Coregistered photoacoustic and ultrasound imaging and classification of ovarian cancer: ex vivo and in vivo studies,” J. Biomed. Opt. 21(4), 46006 (2016).
[Crossref] [PubMed]

H. Li, P. Kumavor, U. Salman Alqasemi, and Q. Zhu, “Utilizing spatial and spectral features of photoacoustic imaging for ovarian cancer detection and diagnosis,” J. Biomed. Opt. 20(1), 016002 (2015).
[Crossref] [PubMed]

Biomed. Opt. Express (1)

Biophys. J. (1)

E. M. Strohm, E .S. L. Berndl, and M. C. Kolios, “Probing red blood cell morphology using high-frequency photoacoustic,” Biophys. J. 105(1), 59 (2013).
[Crossref] [PubMed]

CA Cancer J. Clin. (1)

R. L. Siegel, K. D. Miller, S. A. Fedewa, D. J. Ahnen, R. G. S. Meester, A. Barzi, and A. Jemal, “Colorectal cancer statistics, 2017,” CA Cancer J. Clin. 67(3), 177–193 (2017).
[Crossref] [PubMed]

J. Acoust. Soc. Am. (1)

P. V. Chitnis, J. Mamou, and E. J. Feleppa, “Spectrum analysis of photoacoustic signals for characterizing lymph nodes,” J. Acoust. Soc. Am. 135(4), 2372 (2014).
[Crossref]

J. Am. Coll. Surg. (1)

S. P. Hiotis, S. M. Weber, A. M. Cohen, B. D. Minsky, P. B. Paty, J. G. Guillem, R. Wagman, L. B. Saltz, and W. D. Wong, “Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients,” J. Am. Coll. Surg. 194(2), 131–135 (2002).
[Crossref] [PubMed]

J. Biomed. Opt. (4)

H. Li, P. Kumavor, U. Salman Alqasemi, and Q. Zhu, “Utilizing spatial and spectral features of photoacoustic imaging for ovarian cancer detection and diagnosis,” J. Biomed. Opt. 20(1), 016002 (2015).
[Crossref] [PubMed]

H. S. Salehi, H. Li, A. Merkulov, P. D. Kumavor, H. Vavadi, M. Sanders, A. Kueck, M. A. Brewer, and Q. Zhu, “Coregistered photoacoustic and ultrasound imaging and classification of ovarian cancer: ex vivo and in vivo studies,” J. Biomed. Opt. 21(4), 46006 (2016).
[Crossref] [PubMed]

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt. 17(5), 056016 (2012).
[Crossref] [PubMed]

S. Hu and L. V. Wang, “Photoacoustic imaging and characterization of the microvasculature,” J. Biomed. Opt. 15(1), 011101 (2010).
[Crossref] [PubMed]

Laser Photonics Rev. (1)

J. Yao and L. V. Wang, “Photoacoustic Microscopy,” Laser Photonics Rev. 7(5), 758–778 (2013).
[Crossref] [PubMed]

Nat. Med. (1)

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Radiology (1)

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Rev. Sci. Instrum. (2)

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[Crossref]

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[Crossref]

Science (1)

L. V. Wang and S. Hu, “Photoacoustic tomography: in vivo imaging from organelles to organs,” Science 335(6075), 1458–1462 (2012).
[Crossref] [PubMed]

Other (1)

American National Standards Institute, “American National Standard for the Safe Use of Lasers,” ANSI Standard Z136.1 (American National Standards Institute, New York, 2000).

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Figures (8)

Fig. 1
Fig. 1 (a)AR-PAM imaging head, (b) forward imaging mode, (c) side-view image mode.
Fig. 2
Fig. 2 AR-PAM system.
Fig. 3
Fig. 3 (a) cross-sectional image of 7µm carbon fiber, (b) lateral resolution, (c) axial resolution, (d) depth test in intralipid, (e) SNR versus target depth
Fig. 4
Fig. 4 Photograph of (a) normal colon and (e) adenomatous colon polyp; (b) ultrasound image of the normal tissue; (c) co-registered ultrasound and photoacoustic image of the same cross section of (b), white arrows refer to blood vessel in mucosa and yellow arrows refer to blood vessel in submucosa; (f) ultrasound image of polyp, tissue inside dashed line is polyp; (g) co-registered ultrasound and photoacoustic image of the same cross section of (f); (d) and (h) are H&E images of normal tissue and polyp, yellow arrows identify blood vessels.
Fig. 5
Fig. 5 Gross photographic, ultrasound, coregistered, and CD31-stained histologic images of Specimen 2. (a) Photograph of the normal tissue, (b) ultrasound image of the normal tissue, (c) co-registered ultrasound and photoacoustic image of (b). (e) Photograph of cancer area, (f) and (g) are ultrasound and co-registered image of cancer. (d) and (h) are CD31 images of normal and cancer tissue, respectively, blue arrows point to blood vessels.
Fig. 6
Fig. 6 Images obtained from select areas of Specimen 3 – a colon cancer treated with chemotherapy prior to resection. (a) Photograph of the post treated colon tumor area demonstrating a contracted, scarred ulcer, (b) ultrasound image of the lesion (note that ultrasound gel fills the ulcer cavity (dashed line) but is not within the tissue) (c) co-registered ultrasound and photoacoustic image demonstrating increased photoacoustic signal around the ulcerated area; (d) H&E image of the tumor bed showing residual islands of cancer cells (blue arrows within the dashed box) several millimeters beneath the surface of the specimen.
Fig. 7
Fig. 7 Images of Specimen 4 – a rectal cancer treated with chemotherapy and radiation prior to surgical resection; histologic evaluation revealed no viable tumor in the specimen. (a) Photograph of the post treated rectum tumor area, (b) ultrasound image of the lesion area, (c) co-registered ultrasound and photoacoustic image; (d) H&E image, no residual tumor is found, blood vessels are identified by yellow arrows.
Fig. 8
Fig. 8 (a) Ultrasound echo signal from glass; (b) fast Fourier transform of (a); (c) AR-PAM beam of normal tissue; (d) spectrum of (c); (e) AR-PAM beam of malignant tissue; (f) spectrum of (e); (g) Boxplot and P-value of photoacoustic spectrum slope (absolute value), including 4 malignant cases, 4 normal cases, 2 polyps cases, 1 treated case (rectal cancer with treatment) and 1 residual (colon cancer with treatment)

Tables (2)

Tables Icon

Table 1 Summary of Specimen

Tables Icon

Table 2 Power spectrum slope value

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