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

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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)

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Related Topics
Table of Contents Category
- Optics in Cancer Research
Optics & Photonics Topics
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The topics in this list come from the OSA Optics and Photonics Topics applied to this article.
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

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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.

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References

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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]
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[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]
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[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).

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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.

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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.

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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.

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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.

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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.

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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

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Equations (1)

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\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