Quantification of PpIX concentration in basal cell carcinoma and squamous cell carcinoma models using spatial frequency domain imaging

Ulas Sunar; Daniel J. Rohrbach; Janet Morgan; Natalie Zeitouni; Barbara W. Henderson

doi:10.1364/BOE.4.000531

Quantification of PpIX concentration in basal cell carcinoma and squamous cell carcinoma models using spatial frequency domain imaging

Ulas Sunar, Daniel J. Rohrbach, Janet Morgan, Natalie Zeitouni, and Barbara W. Henderson

Biomedical Optics Express
Vol. 4,
Issue 4,
pp. 531-537
(2013)
•https://doi.org/10.1364/BOE.4.000531

Get Citation
Copy Citation Text
Ulas Sunar, Daniel J. Rohrbach, Janet Morgan, Natalie Zeitouni, and Barbara W. Henderson, "Quantification of PpIX concentration in basal cell carcinoma and squamous cell carcinoma models using spatial frequency domain imaging," Biomed. Opt. Express 4, 531-537 (2013)

Export Citation
- BibTex
- Endnote (RIS)
- HTML
- Plain Text
Get PDF (1160 KB)
Set citation alerts
Save article

Related Topics
Table of Contents Category
- Optics in Cancer Research
Previously assigned OCIS codes
- Medical optics and biotechnology (170.0170)
- Clinical applications (170.1610)
- Medical and biological imaging (170.3880)
- Photodynamic therapy (170.5180)

About this Article
History
- Original Manuscript: January 15, 2013
- Revised Manuscript: March 5, 2013
- Manuscript Accepted: March 5, 2013
- Published: March 6, 2013

Accessible

Open Access

Abstract

5-aminolaevulinic acid photodynamic therapy (ALA-PDT) is an attractive treatment option for nonmelanoma skin tumors, especially for multiple lesions and large areas. The efficacy of ALA-PDT is highly dependent on the photosensitizer (PS) concentration present in the tumor. Thus it is desirable to quantify PS concentration and distribution, preferably noninvasively to determine potential outcome. Here we quantified protoporphyrin IX (PpIX) distribution induced by topical and intra-tumoral (it) administration of the prodrug ALA in basal and squamous cell carcinoma murine models by using spatial frequency domain imaging (SFDI). The in vivo measurements were validated by analysis of the ex vivo extraction of PpIX. The study demonstrates the feasibility of non-invasive quantification of PpIX distributions in skin tumors.

Full Article | PDF Article

OSA Recommended Articles

Noninvasive mesoscopic imaging of actinic skin damage using spatial frequency domain imaging

Jeffrey B. Travers, Chien Poon, Daniel J. Rohrbach, Nathan M. Weir, Elizabeth Cates, Faye Hager, and Ulas Sunar
Biomed. Opt. Express 8(6) 3045-3052 (2017)

Validity of the semi-infinite tumor model in diffuse reflectance spectroscopy for epithelial cancer diagnosis: a Monte Carlo study

Caigang Zhu and Quan Liu
Opt. Express 19(18) 17799-17812 (2011)

Line scanning, stage scanning confocal microscope (LSSSCM)

Daniel S. Gareau, James G. Krueger, Jason E. Hawkes, Samantha R. Lish, Michael P. Dietz, Alba Guembe Mülberger, Euphemia W. Mu, Mary L. Stevenson, Jesse M. Lewin, Shane A. Meehan, and John A. Carucci
Biomed. Opt. Express 8(8) 3807-3815 (2017)

References

View by:
Article Order
|
Year
|
Author
|
Publication

T. M. Busch, S. M. Hahn, E. P. Wileyto, C. J. Koch, D. L. Fraker, P. Zhang, M. Putt, K. Gleason, D. B. Shin, M. J. Emanuele, K. Jenkins, E. Glatstein, and S. M. Evans, “Hypoxia and Photofrin uptake in the intraperitoneal carcinomatosis and sarcomatosis of photodynamic therapy patients,” Clin. Cancer Res. 10(14), 4630–4638 (2004).
[Crossref] [PubMed]
X. Zhou, B. W. Pogue, B. Chen, E. Demidenko, R. Joshi, J. Hoopes, and T. Hasan, “Pretreatment photosensitizer dosimetry reduces variation in tumor response,” Int. J. Radiat. Oncol. Biol. Phys. 64(4), 1211–1220 (2006).
[Crossref] [PubMed]
A. Bogaards, H. J. Sterenborg, J. Trachtenberg, B. C. Wilson, and L. Lilge, “In vivo quantification of fluorescent molecular markers in real-time by ratio imaging for diagnostic screening and image-guided surgery,” Lasers Surg. Med. 39(7), 605–613 (2007).
[Crossref] [PubMed]
E. H. Moriyama, A. Kim, A. Bogaards, L. Lilge, and B. Wilson, “A ratiometric fluorescence imaging system for surgical guidance,” Adv. Opt. Technol. 2008, 532368 (2008).
[Crossref]
R. B. Saager, D. J. Cuccia, S. Saggese, K. M. Kelly, and A. J. Durkin, “Quantitative fluorescence imaging of protoporphyrin IX through determination of tissue optical properties in the spatial frequency domain,” J. Biomed. Opt. 16(12), 126013 (2011).
[Crossref] [PubMed]
A. E. Oro, K. M. Higgins, Z. Hu, J. M. Bonifas, E. H. Epstein, and M. P. Scott, “Basal cell carcinomas in mice overexpressing sonic hedgehog,” Science 276(5313), 817–821 (1997).
[Crossref] [PubMed]
M. Grachtchouk, R. Mo, S. Yu, X. Zhang, H. Sasaki, C. C. Hui, and A. A. Dlugosz, “Basal cell carcinomas in mice overexpressing Gli2 in skin,” Nat. Genet. 24(3), 216–217 (2000).
[Crossref] [PubMed]
T. L. Becker, “Irradiance: A parameter determining oxygenation during topical photodynamic therapy (PDT)” (University at Buffalo, SUNY, Buffalo, 2010).
C. M. Gardner, S. L. Jacques, and A. J. Welch, “Fluorescence spectroscopy of tissue: recovery of intrinsic fluorescence from measured fluorescence,” Appl. Opt. 35(10), 1780–1792 (1996).
[Crossref] [PubMed]
D. J. Cuccia, F. Bevilacqua, A. J. Durkin, F. R. Ayers, and B. J. Tromberg, “Quantitation and mapping of tissue optical properties using modulated imaging,” J. Biomed. Opt. 14(2), 024012 (2009).
[Crossref] [PubMed]
C. W. Chin, A. J. Foss, A. Stevens, and J. Lowe, “Differences in the vascular patterns of basal and squamous cell skin carcinomas explain their differences in clinical behaviour,” J. Pathol. 200(3), 308–313 (2003).
[Crossref] [PubMed]
R. B. Saager, A. Truong, D. J. Cuccia, and A. J. Durkin, “Method for depth-resolved quantitation of optical properties in layered media using spatially modulated quantitative spectroscopy,” J. Biomed. Opt. 16(7), 077002 (2011).
[Crossref] [PubMed]

2011 (2)

R. B. Saager, D. J. Cuccia, S. Saggese, K. M. Kelly, and A. J. Durkin, “Quantitative fluorescence imaging of protoporphyrin IX through determination of tissue optical properties in the spatial frequency domain,” J. Biomed. Opt. 16(12), 126013 (2011).
[Crossref] [PubMed]

R. B. Saager, A. Truong, D. J. Cuccia, and A. J. Durkin, “Method for depth-resolved quantitation of optical properties in layered media using spatially modulated quantitative spectroscopy,” J. Biomed. Opt. 16(7), 077002 (2011).
[Crossref] [PubMed]

2009 (1)

D. J. Cuccia, F. Bevilacqua, A. J. Durkin, F. R. Ayers, and B. J. Tromberg, “Quantitation and mapping of tissue optical properties using modulated imaging,” J. Biomed. Opt. 14(2), 024012 (2009).
[Crossref] [PubMed]

2008 (1)

E. H. Moriyama, A. Kim, A. Bogaards, L. Lilge, and B. Wilson, “A ratiometric fluorescence imaging system for surgical guidance,” Adv. Opt. Technol. 2008, 532368 (2008).
[Crossref]

2007 (1)

A. Bogaards, H. J. Sterenborg, J. Trachtenberg, B. C. Wilson, and L. Lilge, “In vivo quantification of fluorescent molecular markers in real-time by ratio imaging for diagnostic screening and image-guided surgery,” Lasers Surg. Med. 39(7), 605–613 (2007).
[Crossref] [PubMed]

2006 (1)

X. Zhou, B. W. Pogue, B. Chen, E. Demidenko, R. Joshi, J. Hoopes, and T. Hasan, “Pretreatment photosensitizer dosimetry reduces variation in tumor response,” Int. J. Radiat. Oncol. Biol. Phys. 64(4), 1211–1220 (2006).
[Crossref] [PubMed]

2004 (1)

T. M. Busch, S. M. Hahn, E. P. Wileyto, C. J. Koch, D. L. Fraker, P. Zhang, M. Putt, K. Gleason, D. B. Shin, M. J. Emanuele, K. Jenkins, E. Glatstein, and S. M. Evans, “Hypoxia and Photofrin uptake in the intraperitoneal carcinomatosis and sarcomatosis of photodynamic therapy patients,” Clin. Cancer Res. 10(14), 4630–4638 (2004).
[Crossref] [PubMed]

2003 (1)

C. W. Chin, A. J. Foss, A. Stevens, and J. Lowe, “Differences in the vascular patterns of basal and squamous cell skin carcinomas explain their differences in clinical behaviour,” J. Pathol. 200(3), 308–313 (2003).
[Crossref] [PubMed]

2000 (1)

M. Grachtchouk, R. Mo, S. Yu, X. Zhang, H. Sasaki, C. C. Hui, and A. A. Dlugosz, “Basal cell carcinomas in mice overexpressing Gli2 in skin,” Nat. Genet. 24(3), 216–217 (2000).
[Crossref] [PubMed]

1997 (1)

A. E. Oro, K. M. Higgins, Z. Hu, J. M. Bonifas, E. H. Epstein, and M. P. Scott, “Basal cell carcinomas in mice overexpressing sonic hedgehog,” Science 276(5313), 817–821 (1997).
[Crossref] [PubMed]

1996 (1)

C. M. Gardner, S. L. Jacques, and A. J. Welch, “Fluorescence spectroscopy of tissue: recovery of intrinsic fluorescence from measured fluorescence,” Appl. Opt. 35(10), 1780–1792 (1996).
[Crossref] [PubMed]

Ayers, F. R.

Bevilacqua, F.

Bogaards, A.

E. H. Moriyama, A. Kim, A. Bogaards, L. Lilge, and B. Wilson, “A ratiometric fluorescence imaging system for surgical guidance,” Adv. Opt. Technol. 2008, 532368 (2008).
[Crossref]

Bonifas, J. M.

Busch, T. M.

Chen, B.

Chin, C. W.

Cuccia, D. J.

Demidenko, E.

Dlugosz, A. A.

Durkin, A. J.

Emanuele, M. J.

Epstein, E. H.

Evans, S. M.

Foss, A. J.

Fraker, D. L.

Gardner, C. M.

Glatstein, E.

Gleason, K.

Grachtchouk, M.

Hahn, S. M.

Hasan, T.

Higgins, K. M.

Hoopes, J.

Hu, Z.

Hui, C. C.

Jacques, S. L.

Jenkins, K.

Joshi, R.

Kelly, K. M.

Kim, A.

E. H. Moriyama, A. Kim, A. Bogaards, L. Lilge, and B. Wilson, “A ratiometric fluorescence imaging system for surgical guidance,” Adv. Opt. Technol. 2008, 532368 (2008).
[Crossref]

Koch, C. J.

Lilge, L.

E. H. Moriyama, A. Kim, A. Bogaards, L. Lilge, and B. Wilson, “A ratiometric fluorescence imaging system for surgical guidance,” Adv. Opt. Technol. 2008, 532368 (2008).
[Crossref]

Lowe, J.

Mo, R.

Moriyama, E. H.

E. H. Moriyama, A. Kim, A. Bogaards, L. Lilge, and B. Wilson, “A ratiometric fluorescence imaging system for surgical guidance,” Adv. Opt. Technol. 2008, 532368 (2008).
[Crossref]

Oro, A. E.

Pogue, B. W.

Putt, M.

Saager, R. B.

Saggese, S.

Sasaki, H.

Scott, M. P.

Shin, D. B.

Sterenborg, H. J.

Stevens, A.

Trachtenberg, J.

Tromberg, B. J.

Truong, A.

Welch, A. J.

Wileyto, E. P.

Wilson, B.

E. H. Moriyama, A. Kim, A. Bogaards, L. Lilge, and B. Wilson, “A ratiometric fluorescence imaging system for surgical guidance,” Adv. Opt. Technol. 2008, 532368 (2008).
[Crossref]

Wilson, B. C.

Yu, S.

Zhang, P.

Zhang, X.

Zhou, X.

Adv. Opt. Technol. (1)

E. H. Moriyama, A. Kim, A. Bogaards, L. Lilge, and B. Wilson, “A ratiometric fluorescence imaging system for surgical guidance,” Adv. Opt. Technol. 2008, 532368 (2008).
[Crossref]

Appl. Opt. (1)

Clin. Cancer Res. (1)

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

J. Biomed. Opt. (3)

J. Pathol. (1)

Lasers Surg. Med. (1)

Nat. Genet. (1)

Science (1)

Other (1)

T. L. Becker, “Irradiance: A parameter determining oxygenation during topical photodynamic therapy (PDT)” (University at Buffalo, SUNY, Buffalo, 2010).

Cited By

OSA participates in Crossref's Cited-By Linking service. Citing articles from OSA journals and other participating publishers are listed here.

Alert me when this article is cited.

Click here to see a list of articles that cite this paper

Fig. 1 Diagram and picture of the instrument. The system uses a projector with a built-in red LED, 20 nm band-pass filtered at 635 nm light to project images of varying spatial frequencies onto tissue simulating phantoms or tissue (Target). The reflected light field is captured by an EMCCD camera with adjustable filters to selectively capture emission and excitation light. Crossed linear polarizers reduced specular reflection.

Download Full Size | PPT Slide | PDF

Fig. 2 (a) Uncorrected (raw) PpIX fluorescence (b) Attenuation corrected PpIX fluorescence with respect to concentration using all phantoms at different absorption and scattering parameters. Inset in b) zoom in to the lowest detected PpIX concentration (~4 ng/mL). Error bars represent standard deviation of the fluorescence signal due to differences in optical properties.

Download Full Size | PPT Slide | PDF

Fig. 3 Representative images of a BCC on the tail of a Gli mouse 4h after topical-ALA administration. (a) Whitelight structural image showing the tumor area and topical ALA application site. (b) Uncorrected PpIX fluorescence image showing the tumor and surrounding application area. (c) PpIX fluorescence concentration indicating higher contrast between the tumor and surrounding area compared to the uncorrected image.

Download Full Size | PPT Slide | PDF

Fig. 4 Representative images of a FaDu tumor 1h after it-administration of ALA. (a) Whitelight structural image showing the tumor area and ALA injection site. (b) The uncorrected fluorescence image does not show localized contrast. (c) PpIX fluorescence concentration indicating higher contrast between the tumor and surrounding area compared to the uncorrected image.

Download Full Size | PPT Slide | PDF

Fig. 5 (a) Uncorrected fluorescence signal vs ex vivo PpIX concentration. (b) In vivo PpIX concentration vs ex vivo PpIX concentration. Linearity increased from 0.658 to 0.863.

Download Full Size | PPT Slide | PDF

Tables (1)

Table 1 Optical Parameters (µ_a, µ^’_s) Quantified with SFDI at the Emission (~660 nm) and Excitation (~630 nm) Wavelengths for Tumor and Normal Sites in SCID and Gli Mice^a

View Table

Equations (1)

Equations on this page are rendered with MathJax. Learn more.

\begin{array}{l} X_{1 D} (λ_{e x}, λ_{e m}) = \frac{C_{1} (λ_{e x}) C_{3} (λ_{e m})}{k_{1} (λ_{e x}) / δ (λ_{e x}) + k_{3} (λ_{e m}) / δ (λ_{e m})} \\ - \frac{C_{2} (λ_{e x}) C_{3} (λ_{e m})}{k_{2} (λ_{e x}) / δ (λ_{e x}) + k_{3} (λ_{e m}) / δ (λ_{e m})} \end{array}

		SCID		Gli
Wavelength		FaDu SCC	normal	BCC	normal
Emission	µ_a	0.35 ± 0.06	0.20 ± 0.01	0.21 ± 0.02	0.22 ± 0.02
	µ_s’	9.23 ± 0.99	8.25 ± 0.54	13.21 ± 1.22	14.62 ± 0.70
Excitation	µ_a	0.53 ± 0.07	0.33 ± 0.01	0.33 ± 0.03	0.33 ± 0.02
	µ_s’	9.34 ± 0.97	8.32 ± 0.50	13.41 ± 0.63	14.52 ± 0.37