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Gold nanorods for intravital vascular imaging of preneoplastic oral mucosaSaam Motamedi, Tuya Shilagard, Kert Edward, Luke Koong, Suimin Qui, and Gracie Vargas »View Author Affiliations
Saam Motamedi,1
Tuya Shilagard,1
Kert Edward,1
Luke Koong,1,2
Suimin Qui,3,4
and Gracie Vargas1,4,5,*
1Center for Biomedical Engineering, The University of Texas Medical Branch, Galveston, TX 77555-0456 2Present address, Department of Biochemistry and Molecular Biology, The University of Texas Medical Branch, Galveston, TX 77555 3Department of Pathology, The University of Texas Medical Branch, Galveston, TX 77555-0456 4Center for Cancers of the Head and Neck, The University of Texas Medical Branch, Galveston, TX 77555-04565 5Department of Neuroscience & Cell Biology, The University of Texas Medical Branch, Galveston, TX 77555-0456 *Corresponding author: grvargas@utmb.edu |
Biomedical Optics Express, Vol. 2, Issue 5, pp. 1194-1203 (2011)
http://dx.doi.org/10.1364/BOE.2.001194
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Abstract
We explore the feasibility of using gold nanorods with efficient two-photon luminescence properties as contrast agents for intravital imaging of neoplasia. This investigation spanned ex vivo characterization in cells/tissue to in vivo implementation in an oral carcinogenesis model. GNRs were >40 times brighter than surrounding tissue. Intravital imaging revealed 3D microvasculature, and in dysplasia, abnormal vessels (dense and tortuous) compared to normal. GNRs were diffusely distributed in lesions after 24 hours. No known previous study has revealed abnormal vessel structure in dysplasia by imaging. Results suggest GNRs can function as high-contrast agents for in vivo visualization of carcinogenesis features.
© 2011 OSA
OCIS Codes
(170.3880) Medical optics and biotechnology : Medical and biological imaging
(160.4236) Materials : Nanomaterials
(180.4315) Microscopy : Nonlinear microscopy
ToC Category:
Nanotechnology and Plasmonics
History
Original Manuscript: January 4, 2011
Revised Manuscript: April 8, 2011
Manuscript Accepted: April 11, 2011
Published: April 13, 2011
Citation
Saam Motamedi, Tuya Shilagard, Kert Edward, Luke Koong, Suimin Qui, and Gracie Vargas, "Gold nanorods for intravital vascular imaging of preneoplastic oral mucosa," Biomed. Opt. Express 2, 1194-1203 (2011)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-2-5-1194
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References
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- P. Wilder-Smith, K. Osann, N. Hanna, N. El Abbadi, M. Brenner, D. Messadi, and T. Krasieva, “In vivo multiphoton fluorescence imaging: a novel approach to oral malignancy,” Lasers Surg. Med. 35(2), 96–103 (2004). [CrossRef] [PubMed]
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- X. Huang, I. H. El-Sayed, and M. A. El-Sayed, “Applications of gold nanorods for cancer imaging and photothermal therapy,” Methods Mol. Biol. 624, 343–357 (2010). [CrossRef] [PubMed]
- I. H. El-Sayed, X. H. Huang, and M. A. El-Sayed, “Selective laser photo-thermal therapy of epithelial carcinoma using anti-EGFR antibody conjugated gold nanoparticles,” Cancer Lett. 239(1), 129–135 (2006). [CrossRef] [PubMed]
- J. Paoli, M. Smedh, and M. B. Ericson, “Multiphoton laser scanning microscopy--a novel diagnostic method for superficial skin cancers,” Semin. Cutan. Med. Surg. 28(3), 190–195 (2009). [CrossRef] [PubMed]
- A. Ebihara, T. B. Krasieva, L.-H. Liaw, S. Fago, D. Messadi, K. Osann, and P. Wilder-Smith, “Detection and diagnosis of oral cancer by light-induced fluorescence,” Lasers Surg. Med. 32(1), 17–24 (2003). [CrossRef] [PubMed]
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- N. Mohtasham, S. Babakoohi, J. Salehinejad, L. Montaser-Kouhsari, M. T. Shakeri, S. Shojaee, N. S. Sistani, and A. Firooz, “Mast cell density and angiogenesis in oral dysplastic epithelium and low- and high-grade oral squamous cell carcinoma,” Acta Odontol. Scand. 68(5), 300–304 (2010). [CrossRef] [PubMed]
- M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007). [CrossRef] [PubMed]
- M. C. Skala, J. M. Squirrell, K. M. Vrotsos, J. C. Eickhoff, A. Gendron-Fitzpatrick, K. W. Eliceiri, and N. Ramanujam, “Multiphoton microscopy of endogenous fluorescence differentiates normal, precancerous, and cancerous squamous epithelial tissues,” Cancer Res. 65(4), 1180–1186 (2005). [CrossRef] [PubMed]
- S. E. Gratton, P. A. Ropp, P. D. Pohlhaus, J. C. Luft, V. J. Madden, M. E. Napier, and J. M. DeSimone, “The effect of particle design on cellular internalization pathways,” Proc. Natl. Acad. Sci. U.S.A. 105(33), 11613–11618 (2008). [CrossRef] [PubMed]
- P. Wilder-Smith, K. Osann, N. Hanna, N. El Abbadi, M. Brenner, D. Messadi, and T. Krasieva, “In vivo multiphoton fluorescence imaging: a novel approach to oral malignancy,” Lasers Surg. Med. 35(2), 96–103 (2004). [CrossRef] [PubMed]
- L. Tong, W. He, Y. Zhang, W. Zheng, and J. X. Cheng, “Visualizing systemic clearance and cellular level biodistribution of gold nanorods by intrinsic two-photon luminescence,” Langmuir 25(21), 12454–12459 (2009). [CrossRef] [PubMed]
- H. Wang, T. B. Huff, D. A. Zweifel, W. He, P. S. Low, A. Wei, and J. X. Cheng, “In vitro and in vivo two-photon luminescence imaging of single gold nanorods,” Proc. Natl. Acad. Sci. U.S.A. 102(44), 15752–15756 (2005). [CrossRef] [PubMed]
- F. Nussenbaum and I. M. Herman, “Tumor angigoenesis: insights and inovations,” J. Oncolog. 2010, 132641 (2010).
- G. Vargas, T. Shilagard, K. H. Ho, and S. McCammon, “Multiphoton autofluorescence microscopy and second harmonic generation microscopy of oral epithelial neoplasms,” Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 6311–6313 (2009). [PubMed]
- X. Huang, I. H. El-Sayed, and M. A. El-Sayed, “Applications of gold nanorods for cancer imaging and photothermal therapy,” Methods Mol. Biol. 624, 343–357 (2010). [CrossRef] [PubMed]
- I. H. El-Sayed, X. H. Huang, and M. A. El-Sayed, “Selective laser photo-thermal therapy of epithelial carcinoma using anti-EGFR antibody conjugated gold nanoparticles,” Cancer Lett. 239(1), 129–135 (2006). [CrossRef] [PubMed]
- H. Wang, T. B. Huff, D. A. Zweifel, W. He, P. S. Low, A. Wei, and J. X. Cheng, “In vitro and in vivo two-photon luminescence imaging of single gold nanorods,” Proc. Natl. Acad. Sci. U.S.A. 102(44), 15752–15756 (2005). [CrossRef] [PubMed]
- A. M. Kluftinger, N. L. Davis, N. F. Quenville, S. Lam, J. Hung, and B. Palcic, “Detection of squamous cell cancer and pre-cancerous lesions by imaging of tissue autofluorescence in the hamster cheek pouch model,” Surg. Oncol. 1(2), 183–188 (1992). [CrossRef] [PubMed]
- X. Qu, J. Wang, Z. Zhang, N. Koop, R. Rahmanzadeh, and G. Hüttmann, “Imaging of cancer cells by multiphoton microscopy using gold nanoparticles and fluorescent dyes,” J. Biomed. Opt. 13(3), 031217 (2008). [CrossRef] [PubMed]
- V. L. Noonan and S. Kabani, “Diagnosis and management of suspicious lesions of the oral cavity,” Otolaryngol. Clin. North Am. 38(1), 21–35, vii (2005) (vii.). [CrossRef] [PubMed]
- A. M. Kluftinger, N. L. Davis, N. F. Quenville, S. Lam, J. Hung, and B. Palcic, “Detection of squamous cell cancer and pre-cancerous lesions by imaging of tissue autofluorescence in the hamster cheek pouch model,” Surg. Oncol. 1(2), 183–188 (1992). [CrossRef] [PubMed]
- X. Qu, J. Wang, Z. Zhang, N. Koop, R. Rahmanzadeh, and G. Hüttmann, “Imaging of cancer cells by multiphoton microscopy using gold nanoparticles and fluorescent dyes,” J. Biomed. Opt. 13(3), 031217 (2008). [CrossRef] [PubMed]
- J. Park, A. Estrada, K. Sharp, K. Sang, J. A. Schwartz, D. K. Smith, C. Coleman, J. D. Payne, B. A. Korgel, A. K. Dunn, and J. W. Tunnell, “Two-photon-induced photoluminescence imaging of tumors using near-infrared excited gold nanoshells,” Opt. Express 16(3), 1590–1599 (2008). [CrossRef] [PubMed]
- N. J. Durr, T. Larson, D. K. Smith, B. A. Korgel, K. Sokolov, and A. Ben-Yakar, “Two-photon luminescence imaging of cancer cells using molecularly targeted gold nanorods,” Nano Lett. 7(4), 941–945 (2007). [CrossRef] [PubMed]
- P. Wilder-Smith, K. Osann, N. Hanna, N. El Abbadi, M. Brenner, D. Messadi, and T. Krasieva, “In vivo multiphoton fluorescence imaging: a novel approach to oral malignancy,” Lasers Surg. Med. 35(2), 96–103 (2004). [CrossRef] [PubMed]
- A. Ebihara, T. B. Krasieva, L.-H. Liaw, S. Fago, D. Messadi, K. Osann, and P. Wilder-Smith, “Detection and diagnosis of oral cancer by light-induced fluorescence,” Lasers Surg. Med. 32(1), 17–24 (2003). [CrossRef] [PubMed]
- A. M. Kluftinger, N. L. Davis, N. F. Quenville, S. Lam, J. Hung, and B. Palcic, “Detection of squamous cell cancer and pre-cancerous lesions by imaging of tissue autofluorescence in the hamster cheek pouch model,” Surg. Oncol. 1(2), 183–188 (1992). [CrossRef] [PubMed]
- N. J. Durr, T. Larson, D. K. Smith, B. A. Korgel, K. Sokolov, and A. Ben-Yakar, “Two-photon luminescence imaging of cancer cells using molecularly targeted gold nanorods,” Nano Lett. 7(4), 941–945 (2007). [CrossRef] [PubMed]
- A. Ebihara, T. B. Krasieva, L.-H. Liaw, S. Fago, D. Messadi, K. Osann, and P. Wilder-Smith, “Detection and diagnosis of oral cancer by light-induced fluorescence,” Lasers Surg. Med. 32(1), 17–24 (2003). [CrossRef] [PubMed]
- S. A. Liu, Y. K. Wong, J. C. Lin, C. K. Poon, K. C. Tung, and W. C. Tsai, “Impact of recurrence interval on survival of oral cavity squamous cell carcinoma patients after local relapse,” Otolaryngol. Head Neck Surg. 136(1), 112–118 (2007). [CrossRef] [PubMed]
- M. Eghtedari, A. V. Liopo, J. A. Copland, A. A. Oraevsky, and M. Motamedi, “Engineering of hetero-functional gold nanorods for the in vivo molecular targeting of breast cancer cells,” Nano Lett. 9(1), 287–291 (2009). [CrossRef] [PubMed]
- S. A. Liu, Y. K. Wong, J. C. Lin, C. K. Poon, K. C. Tung, and W. C. Tsai, “Impact of recurrence interval on survival of oral cavity squamous cell carcinoma patients after local relapse,” Otolaryngol. Head Neck Surg. 136(1), 112–118 (2007). [CrossRef] [PubMed]
- H. Wang, T. B. Huff, D. A. Zweifel, W. He, P. S. Low, A. Wei, and J. X. Cheng, “In vitro and in vivo two-photon luminescence imaging of single gold nanorods,” Proc. Natl. Acad. Sci. U.S.A. 102(44), 15752–15756 (2005). [CrossRef] [PubMed]
- S. E. Gratton, P. A. Ropp, P. D. Pohlhaus, J. C. Luft, V. J. Madden, M. E. Napier, and J. M. DeSimone, “The effect of particle design on cellular internalization pathways,” Proc. Natl. Acad. Sci. U.S.A. 105(33), 11613–11618 (2008). [CrossRef] [PubMed]
- S. E. Gratton, P. A. Ropp, P. D. Pohlhaus, J. C. Luft, V. J. Madden, M. E. Napier, and J. M. DeSimone, “The effect of particle design on cellular internalization pathways,” Proc. Natl. Acad. Sci. U.S.A. 105(33), 11613–11618 (2008). [CrossRef] [PubMed]
- E. Z. Michailidou, A. K. Markopoulos, and D. Z. Antoniades, “Mast cells and angiogenesis in oral malignant and premalignant lesions,” Open Dent. J. 2(1), 126–132 (2008). [CrossRef] [PubMed]
- G. Vargas, T. Shilagard, K. H. Ho, and S. McCammon, “Multiphoton autofluorescence microscopy and second harmonic generation microscopy of oral epithelial neoplasms,” Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 6311–6313 (2009). [PubMed]
- V. A. Resto, M. M. Burdick, N. M. Dagia, S. D. McCammon, S. M. Fennewald, and R. Sackstein, “L-selectin-mediated lymphocyte-cancer cell interactions under low fluid shear conditions,” J. Biol. Chem. 283(23), 15816–15824 (2008). [CrossRef] [PubMed]
- P. Wilder-Smith, K. Osann, N. Hanna, N. El Abbadi, M. Brenner, D. Messadi, and T. Krasieva, “In vivo multiphoton fluorescence imaging: a novel approach to oral malignancy,” Lasers Surg. Med. 35(2), 96–103 (2004). [CrossRef] [PubMed]
- A. Ebihara, T. B. Krasieva, L.-H. Liaw, S. Fago, D. Messadi, K. Osann, and P. Wilder-Smith, “Detection and diagnosis of oral cancer by light-induced fluorescence,” Lasers Surg. Med. 32(1), 17–24 (2003). [CrossRef] [PubMed]
- E. Z. Michailidou, A. K. Markopoulos, and D. Z. Antoniades, “Mast cells and angiogenesis in oral malignant and premalignant lesions,” Open Dent. J. 2(1), 126–132 (2008). [CrossRef] [PubMed]
- N. Mohtasham, S. Babakoohi, J. Salehinejad, L. Montaser-Kouhsari, M. T. Shakeri, S. Shojaee, N. S. Sistani, and A. Firooz, “Mast cell density and angiogenesis in oral dysplastic epithelium and low- and high-grade oral squamous cell carcinoma,” Acta Odontol. Scand. 68(5), 300–304 (2010). [CrossRef] [PubMed]
- N. Mohtasham, S. Babakoohi, J. Salehinejad, L. Montaser-Kouhsari, M. T. Shakeri, S. Shojaee, N. S. Sistani, and A. Firooz, “Mast cell density and angiogenesis in oral dysplastic epithelium and low- and high-grade oral squamous cell carcinoma,” Acta Odontol. Scand. 68(5), 300–304 (2010). [CrossRef] [PubMed]
- M. Eghtedari, A. V. Liopo, J. A. Copland, A. A. Oraevsky, and M. Motamedi, “Engineering of hetero-functional gold nanorods for the in vivo molecular targeting of breast cancer cells,” Nano Lett. 9(1), 287–291 (2009). [CrossRef] [PubMed]
- J. Sun, T. Shilagard, B. Bell, M. Motamedi, and G. Vargas, “In vivo multimodal nonlinear optical imaging of mucosal tissue,” Opt. Express 12(11), 2478–2486 (2004). [CrossRef] [PubMed]
- S. E. Gratton, P. A. Ropp, P. D. Pohlhaus, J. C. Luft, V. J. Madden, M. E. Napier, and J. M. DeSimone, “The effect of particle design on cellular internalization pathways,” Proc. Natl. Acad. Sci. U.S.A. 105(33), 11613–11618 (2008). [CrossRef] [PubMed]
- V. L. Noonan and S. Kabani, “Diagnosis and management of suspicious lesions of the oral cavity,” Otolaryngol. Clin. North Am. 38(1), 21–35, vii (2005) (vii.). [CrossRef] [PubMed]
- F. Nussenbaum and I. M. Herman, “Tumor angigoenesis: insights and inovations,” J. Oncolog. 2010, 132641 (2010).
- M. Eghtedari, A. V. Liopo, J. A. Copland, A. A. Oraevsky, and M. Motamedi, “Engineering of hetero-functional gold nanorods for the in vivo molecular targeting of breast cancer cells,” Nano Lett. 9(1), 287–291 (2009). [CrossRef] [PubMed]
- P. Wilder-Smith, K. Osann, N. Hanna, N. El Abbadi, M. Brenner, D. Messadi, and T. Krasieva, “In vivo multiphoton fluorescence imaging: a novel approach to oral malignancy,” Lasers Surg. Med. 35(2), 96–103 (2004). [CrossRef] [PubMed]
- A. Ebihara, T. B. Krasieva, L.-H. Liaw, S. Fago, D. Messadi, K. Osann, and P. Wilder-Smith, “Detection and diagnosis of oral cancer by light-induced fluorescence,” Lasers Surg. Med. 32(1), 17–24 (2003). [CrossRef] [PubMed]
- A. M. Kluftinger, N. L. Davis, N. F. Quenville, S. Lam, J. Hung, and B. Palcic, “Detection of squamous cell cancer and pre-cancerous lesions by imaging of tissue autofluorescence in the hamster cheek pouch model,” Surg. Oncol. 1(2), 183–188 (1992). [CrossRef] [PubMed]
- J. Paoli, M. Smedh, and M. B. Ericson, “Multiphoton laser scanning microscopy--a novel diagnostic method for superficial skin cancers,” Semin. Cutan. Med. Surg. 28(3), 190–195 (2009). [CrossRef] [PubMed]
- R. Weissleder and M. J. Pittet, “Imaging in the era of molecular oncology,” Nature 452(7187), 580–589 (2008). [CrossRef] [PubMed]
- S. E. Gratton, P. A. Ropp, P. D. Pohlhaus, J. C. Luft, V. J. Madden, M. E. Napier, and J. M. DeSimone, “The effect of particle design on cellular internalization pathways,” Proc. Natl. Acad. Sci. U.S.A. 105(33), 11613–11618 (2008). [CrossRef] [PubMed]
- S. A. Liu, Y. K. Wong, J. C. Lin, C. K. Poon, K. C. Tung, and W. C. Tsai, “Impact of recurrence interval on survival of oral cavity squamous cell carcinoma patients after local relapse,” Otolaryngol. Head Neck Surg. 136(1), 112–118 (2007). [CrossRef] [PubMed]
- X. Qu, J. Wang, Z. Zhang, N. Koop, R. Rahmanzadeh, and G. Hüttmann, “Imaging of cancer cells by multiphoton microscopy using gold nanoparticles and fluorescent dyes,” J. Biomed. Opt. 13(3), 031217 (2008). [CrossRef] [PubMed]
- A. M. Kluftinger, N. L. Davis, N. F. Quenville, S. Lam, J. Hung, and B. Palcic, “Detection of squamous cell cancer and pre-cancerous lesions by imaging of tissue autofluorescence in the hamster cheek pouch model,” Surg. Oncol. 1(2), 183–188 (1992). [CrossRef] [PubMed]
- X. Qu, J. Wang, Z. Zhang, N. Koop, R. Rahmanzadeh, and G. Hüttmann, “Imaging of cancer cells by multiphoton microscopy using gold nanoparticles and fluorescent dyes,” J. Biomed. Opt. 13(3), 031217 (2008). [CrossRef] [PubMed]
- M. Raica, A. M. Cimpean, and D. Ribatti, “Angiogenesis in pre-malignant conditions,” Eur. J. Cancer 45(11), 1924–1934 (2009). [CrossRef]
- M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007). [CrossRef] [PubMed]
- M. C. Skala, J. M. Squirrell, K. M. Vrotsos, J. C. Eickhoff, A. Gendron-Fitzpatrick, K. W. Eliceiri, and N. Ramanujam, “Multiphoton microscopy of endogenous fluorescence differentiates normal, precancerous, and cancerous squamous epithelial tissues,” Cancer Res. 65(4), 1180–1186 (2005). [CrossRef] [PubMed]
- V. A. Resto, M. M. Burdick, N. M. Dagia, S. D. McCammon, S. M. Fennewald, and R. Sackstein, “L-selectin-mediated lymphocyte-cancer cell interactions under low fluid shear conditions,” J. Biol. Chem. 283(23), 15816–15824 (2008). [CrossRef] [PubMed]
- M. Raica, A. M. Cimpean, and D. Ribatti, “Angiogenesis in pre-malignant conditions,” Eur. J. Cancer 45(11), 1924–1934 (2009). [CrossRef]
- M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007). [CrossRef] [PubMed]
- S. E. Gratton, P. A. Ropp, P. D. Pohlhaus, J. C. Luft, V. J. Madden, M. E. Napier, and J. M. DeSimone, “The effect of particle design on cellular internalization pathways,” Proc. Natl. Acad. Sci. U.S.A. 105(33), 11613–11618 (2008). [CrossRef] [PubMed]
- V. A. Resto, M. M. Burdick, N. M. Dagia, S. D. McCammon, S. M. Fennewald, and R. Sackstein, “L-selectin-mediated lymphocyte-cancer cell interactions under low fluid shear conditions,” J. Biol. Chem. 283(23), 15816–15824 (2008). [CrossRef] [PubMed]
- N. Mohtasham, S. Babakoohi, J. Salehinejad, L. Montaser-Kouhsari, M. T. Shakeri, S. Shojaee, N. S. Sistani, and A. Firooz, “Mast cell density and angiogenesis in oral dysplastic epithelium and low- and high-grade oral squamous cell carcinoma,” Acta Odontol. Scand. 68(5), 300–304 (2010). [CrossRef] [PubMed]
- N. Mohtasham, S. Babakoohi, J. Salehinejad, L. Montaser-Kouhsari, M. T. Shakeri, S. Shojaee, N. S. Sistani, and A. Firooz, “Mast cell density and angiogenesis in oral dysplastic epithelium and low- and high-grade oral squamous cell carcinoma,” Acta Odontol. Scand. 68(5), 300–304 (2010). [CrossRef] [PubMed]
- G. Vargas, T. Shilagard, K. H. Ho, and S. McCammon, “Multiphoton autofluorescence microscopy and second harmonic generation microscopy of oral epithelial neoplasms,” Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 6311–6313 (2009). [PubMed]
- J. Sun, T. Shilagard, B. Bell, M. Motamedi, and G. Vargas, “In vivo multimodal nonlinear optical imaging of mucosal tissue,” Opt. Express 12(11), 2478–2486 (2004). [CrossRef] [PubMed]
- N. Mohtasham, S. Babakoohi, J. Salehinejad, L. Montaser-Kouhsari, M. T. Shakeri, S. Shojaee, N. S. Sistani, and A. Firooz, “Mast cell density and angiogenesis in oral dysplastic epithelium and low- and high-grade oral squamous cell carcinoma,” Acta Odontol. Scand. 68(5), 300–304 (2010). [CrossRef] [PubMed]
- N. Mohtasham, S. Babakoohi, J. Salehinejad, L. Montaser-Kouhsari, M. T. Shakeri, S. Shojaee, N. S. Sistani, and A. Firooz, “Mast cell density and angiogenesis in oral dysplastic epithelium and low- and high-grade oral squamous cell carcinoma,” Acta Odontol. Scand. 68(5), 300–304 (2010). [CrossRef] [PubMed]
- M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007). [CrossRef] [PubMed]
- M. C. Skala, J. M. Squirrell, K. M. Vrotsos, J. C. Eickhoff, A. Gendron-Fitzpatrick, K. W. Eliceiri, and N. Ramanujam, “Multiphoton microscopy of endogenous fluorescence differentiates normal, precancerous, and cancerous squamous epithelial tissues,” Cancer Res. 65(4), 1180–1186 (2005). [CrossRef] [PubMed]
- J. Paoli, M. Smedh, and M. B. Ericson, “Multiphoton laser scanning microscopy--a novel diagnostic method for superficial skin cancers,” Semin. Cutan. Med. Surg. 28(3), 190–195 (2009). [CrossRef] [PubMed]
- J. Park, A. Estrada, K. Sharp, K. Sang, J. A. Schwartz, D. K. Smith, C. Coleman, J. D. Payne, B. A. Korgel, A. K. Dunn, and J. W. Tunnell, “Two-photon-induced photoluminescence imaging of tumors using near-infrared excited gold nanoshells,” Opt. Express 16(3), 1590–1599 (2008). [CrossRef] [PubMed]
- N. J. Durr, T. Larson, D. K. Smith, B. A. Korgel, K. Sokolov, and A. Ben-Yakar, “Two-photon luminescence imaging of cancer cells using molecularly targeted gold nanorods,” Nano Lett. 7(4), 941–945 (2007). [CrossRef] [PubMed]
- N. J. Durr, T. Larson, D. K. Smith, B. A. Korgel, K. Sokolov, and A. Ben-Yakar, “Two-photon luminescence imaging of cancer cells using molecularly targeted gold nanorods,” Nano Lett. 7(4), 941–945 (2007). [CrossRef] [PubMed]
- M. C. Skala, J. M. Squirrell, K. M. Vrotsos, J. C. Eickhoff, A. Gendron-Fitzpatrick, K. W. Eliceiri, and N. Ramanujam, “Multiphoton microscopy of endogenous fluorescence differentiates normal, precancerous, and cancerous squamous epithelial tissues,” Cancer Res. 65(4), 1180–1186 (2005). [CrossRef] [PubMed]
- L. Tong, W. He, Y. Zhang, W. Zheng, and J. X. Cheng, “Visualizing systemic clearance and cellular level biodistribution of gold nanorods by intrinsic two-photon luminescence,” Langmuir 25(21), 12454–12459 (2009). [CrossRef] [PubMed]
- S. A. Liu, Y. K. Wong, J. C. Lin, C. K. Poon, K. C. Tung, and W. C. Tsai, “Impact of recurrence interval on survival of oral cavity squamous cell carcinoma patients after local relapse,” Otolaryngol. Head Neck Surg. 136(1), 112–118 (2007). [CrossRef] [PubMed]
- S. A. Liu, Y. K. Wong, J. C. Lin, C. K. Poon, K. C. Tung, and W. C. Tsai, “Impact of recurrence interval on survival of oral cavity squamous cell carcinoma patients after local relapse,” Otolaryngol. Head Neck Surg. 136(1), 112–118 (2007). [CrossRef] [PubMed]
- G. Vargas, T. Shilagard, K. H. Ho, and S. McCammon, “Multiphoton autofluorescence microscopy and second harmonic generation microscopy of oral epithelial neoplasms,” Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 6311–6313 (2009). [PubMed]
- J. Sun, T. Shilagard, B. Bell, M. Motamedi, and G. Vargas, “In vivo multimodal nonlinear optical imaging of mucosal tissue,” Opt. Express 12(11), 2478–2486 (2004). [CrossRef] [PubMed]
- M. C. Skala, J. M. Squirrell, K. M. Vrotsos, J. C. Eickhoff, A. Gendron-Fitzpatrick, K. W. Eliceiri, and N. Ramanujam, “Multiphoton microscopy of endogenous fluorescence differentiates normal, precancerous, and cancerous squamous epithelial tissues,” Cancer Res. 65(4), 1180–1186 (2005). [CrossRef] [PubMed]
- H. Wang, T. B. Huff, D. A. Zweifel, W. He, P. S. Low, A. Wei, and J. X. Cheng, “In vitro and in vivo two-photon luminescence imaging of single gold nanorods,” Proc. Natl. Acad. Sci. U.S.A. 102(44), 15752–15756 (2005). [CrossRef] [PubMed]
- X. Qu, J. Wang, Z. Zhang, N. Koop, R. Rahmanzadeh, and G. Hüttmann, “Imaging of cancer cells by multiphoton microscopy using gold nanoparticles and fluorescent dyes,” J. Biomed. Opt. 13(3), 031217 (2008). [CrossRef] [PubMed]
- H. Wang, T. B. Huff, D. A. Zweifel, W. He, P. S. Low, A. Wei, and J. X. Cheng, “In vitro and in vivo two-photon luminescence imaging of single gold nanorods,” Proc. Natl. Acad. Sci. U.S.A. 102(44), 15752–15756 (2005). [CrossRef] [PubMed]
- R. Weissleder and M. J. Pittet, “Imaging in the era of molecular oncology,” Nature 452(7187), 580–589 (2008). [CrossRef] [PubMed]
- M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007). [CrossRef] [PubMed]
- P. Wilder-Smith, K. Osann, N. Hanna, N. El Abbadi, M. Brenner, D. Messadi, and T. Krasieva, “In vivo multiphoton fluorescence imaging: a novel approach to oral malignancy,” Lasers Surg. Med. 35(2), 96–103 (2004). [CrossRef] [PubMed]
- A. Ebihara, T. B. Krasieva, L.-H. Liaw, S. Fago, D. Messadi, K. Osann, and P. Wilder-Smith, “Detection and diagnosis of oral cancer by light-induced fluorescence,” Lasers Surg. Med. 32(1), 17–24 (2003). [CrossRef] [PubMed]
- S. A. Liu, Y. K. Wong, J. C. Lin, C. K. Poon, K. C. Tung, and W. C. Tsai, “Impact of recurrence interval on survival of oral cavity squamous cell carcinoma patients after local relapse,” Otolaryngol. Head Neck Surg. 136(1), 112–118 (2007). [CrossRef] [PubMed]
- L. Tong, W. He, Y. Zhang, W. Zheng, and J. X. Cheng, “Visualizing systemic clearance and cellular level biodistribution of gold nanorods by intrinsic two-photon luminescence,” Langmuir 25(21), 12454–12459 (2009). [CrossRef] [PubMed]
- X. Qu, J. Wang, Z. Zhang, N. Koop, R. Rahmanzadeh, and G. Hüttmann, “Imaging of cancer cells by multiphoton microscopy using gold nanoparticles and fluorescent dyes,” J. Biomed. Opt. 13(3), 031217 (2008). [CrossRef] [PubMed]
- L. Tong, W. He, Y. Zhang, W. Zheng, and J. X. Cheng, “Visualizing systemic clearance and cellular level biodistribution of gold nanorods by intrinsic two-photon luminescence,” Langmuir 25(21), 12454–12459 (2009). [CrossRef] [PubMed]
- H. Wang, T. B. Huff, D. A. Zweifel, W. He, P. S. Low, A. Wei, and J. X. Cheng, “In vitro and in vivo two-photon luminescence imaging of single gold nanorods,” Proc. Natl. Acad. Sci. U.S.A. 102(44), 15752–15756 (2005). [CrossRef] [PubMed]
Acta Odontol. Scand.
- N. Mohtasham, S. Babakoohi, J. Salehinejad, L. Montaser-Kouhsari, M. T. Shakeri, S. Shojaee, N. S. Sistani, and A. Firooz, “Mast cell density and angiogenesis in oral dysplastic epithelium and low- and high-grade oral squamous cell carcinoma,” Acta Odontol. Scand. 68(5), 300–304 (2010). [CrossRef] [PubMed]
Cancer Lett.
- I. H. El-Sayed, X. H. Huang, and M. A. El-Sayed, “Selective laser photo-thermal therapy of epithelial carcinoma using anti-EGFR antibody conjugated gold nanoparticles,” Cancer Lett. 239(1), 129–135 (2006). [CrossRef] [PubMed]
Cancer Res.
- M. C. Skala, J. M. Squirrell, K. M. Vrotsos, J. C. Eickhoff, A. Gendron-Fitzpatrick, K. W. Eliceiri, and N. Ramanujam, “Multiphoton microscopy of endogenous fluorescence differentiates normal, precancerous, and cancerous squamous epithelial tissues,” Cancer Res. 65(4), 1180–1186 (2005). [CrossRef] [PubMed]
Conf. Proc. IEEE Eng. Med. Biol. Soc.
- G. Vargas, T. Shilagard, K. H. Ho, and S. McCammon, “Multiphoton autofluorescence microscopy and second harmonic generation microscopy of oral epithelial neoplasms,” Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 6311–6313 (2009). [PubMed]
Eur. J. Cancer
- M. Raica, A. M. Cimpean, and D. Ribatti, “Angiogenesis in pre-malignant conditions,” Eur. J. Cancer 45(11), 1924–1934 (2009). [CrossRef]
J. Biol. Chem.
- V. A. Resto, M. M. Burdick, N. M. Dagia, S. D. McCammon, S. M. Fennewald, and R. Sackstein, “L-selectin-mediated lymphocyte-cancer cell interactions under low fluid shear conditions,” J. Biol. Chem. 283(23), 15816–15824 (2008). [CrossRef] [PubMed]
J. Biomed. Opt.
- X. Qu, J. Wang, Z. Zhang, N. Koop, R. Rahmanzadeh, and G. Hüttmann, “Imaging of cancer cells by multiphoton microscopy using gold nanoparticles and fluorescent dyes,” J. Biomed. Opt. 13(3), 031217 (2008). [CrossRef] [PubMed]
J. Oncolog.
- F. Nussenbaum and I. M. Herman, “Tumor angigoenesis: insights and inovations,” J. Oncolog. 2010, 132641 (2010).
Langmuir
- L. Tong, W. He, Y. Zhang, W. Zheng, and J. X. Cheng, “Visualizing systemic clearance and cellular level biodistribution of gold nanorods by intrinsic two-photon luminescence,” Langmuir 25(21), 12454–12459 (2009). [CrossRef] [PubMed]
Lasers Surg. Med.
- P. Wilder-Smith, K. Osann, N. Hanna, N. El Abbadi, M. Brenner, D. Messadi, and T. Krasieva, “In vivo multiphoton fluorescence imaging: a novel approach to oral malignancy,” Lasers Surg. Med. 35(2), 96–103 (2004). [CrossRef] [PubMed]
- A. Ebihara, T. B. Krasieva, L.-H. Liaw, S. Fago, D. Messadi, K. Osann, and P. Wilder-Smith, “Detection and diagnosis of oral cancer by light-induced fluorescence,” Lasers Surg. Med. 32(1), 17–24 (2003). [CrossRef] [PubMed]
Methods Mol. Biol.
- X. Huang, I. H. El-Sayed, and M. A. El-Sayed, “Applications of gold nanorods for cancer imaging and photothermal therapy,” Methods Mol. Biol. 624, 343–357 (2010). [CrossRef] [PubMed]
Nano Lett.
- M. Eghtedari, A. V. Liopo, J. A. Copland, A. A. Oraevsky, and M. Motamedi, “Engineering of hetero-functional gold nanorods for the in vivo molecular targeting of breast cancer cells,” Nano Lett. 9(1), 287–291 (2009). [CrossRef] [PubMed]
- N. J. Durr, T. Larson, D. K. Smith, B. A. Korgel, K. Sokolov, and A. Ben-Yakar, “Two-photon luminescence imaging of cancer cells using molecularly targeted gold nanorods,” Nano Lett. 7(4), 941–945 (2007). [CrossRef] [PubMed]
Nature
- R. Weissleder and M. J. Pittet, “Imaging in the era of molecular oncology,” Nature 452(7187), 580–589 (2008). [CrossRef] [PubMed]
Open Dent. J.
- E. Z. Michailidou, A. K. Markopoulos, and D. Z. Antoniades, “Mast cells and angiogenesis in oral malignant and premalignant lesions,” Open Dent. J. 2(1), 126–132 (2008). [CrossRef] [PubMed]
Opt. Express
- J. Sun, T. Shilagard, B. Bell, M. Motamedi, and G. Vargas, “In vivo multimodal nonlinear optical imaging of mucosal tissue,” Opt. Express 12(11), 2478–2486 (2004). [CrossRef] [PubMed]
- J. Park, A. Estrada, K. Sharp, K. Sang, J. A. Schwartz, D. K. Smith, C. Coleman, J. D. Payne, B. A. Korgel, A. K. Dunn, and J. W. Tunnell, “Two-photon-induced photoluminescence imaging of tumors using near-infrared excited gold nanoshells,” Opt. Express 16(3), 1590–1599 (2008). [CrossRef] [PubMed]
Otolaryngol. Clin. North Am.
- V. L. Noonan and S. Kabani, “Diagnosis and management of suspicious lesions of the oral cavity,” Otolaryngol. Clin. North Am. 38(1), 21–35, vii (2005) (vii.). [CrossRef] [PubMed]
Otolaryngol. Head Neck Surg.
- S. A. Liu, Y. K. Wong, J. C. Lin, C. K. Poon, K. C. Tung, and W. C. Tsai, “Impact of recurrence interval on survival of oral cavity squamous cell carcinoma patients after local relapse,” Otolaryngol. Head Neck Surg. 136(1), 112–118 (2007). [CrossRef] [PubMed]
Proc. Natl. Acad. Sci. U.S.A.
- M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007). [CrossRef] [PubMed]
- H. Wang, T. B. Huff, D. A. Zweifel, W. He, P. S. Low, A. Wei, and J. X. Cheng, “In vitro and in vivo two-photon luminescence imaging of single gold nanorods,” Proc. Natl. Acad. Sci. U.S.A. 102(44), 15752–15756 (2005). [CrossRef] [PubMed]
- S. E. Gratton, P. A. Ropp, P. D. Pohlhaus, J. C. Luft, V. J. Madden, M. E. Napier, and J. M. DeSimone, “The effect of particle design on cellular internalization pathways,” Proc. Natl. Acad. Sci. U.S.A. 105(33), 11613–11618 (2008). [CrossRef] [PubMed]
Semin. Cutan. Med. Surg.
- J. Paoli, M. Smedh, and M. B. Ericson, “Multiphoton laser scanning microscopy--a novel diagnostic method for superficial skin cancers,” Semin. Cutan. Med. Surg. 28(3), 190–195 (2009). [CrossRef] [PubMed]
Surg. Oncol.
- A. M. Kluftinger, N. L. Davis, N. F. Quenville, S. Lam, J. Hung, and B. Palcic, “Detection of squamous cell cancer and pre-cancerous lesions by imaging of tissue autofluorescence in the hamster cheek pouch model,” Surg. Oncol. 1(2), 183–188 (1992). [CrossRef] [PubMed]
Other
- G. Shklar, “Experimental pathology of oral cancer,” in Oral Cancer, G. Shklar, ed. (W.B. Sanders, 1984), pp. 41–54.
- G. Vargas, T. Shilagard, J. Sun, and M. Motamedi, “In vivo multiphoton and second harmonic generation microscopy of epithelial carcinogenesis,” Proc. SPIE 6091, 000–000 (2006).
- American Cancer Society, Cancer Facts & Figures 2002 (American Cancer Society, New York, 2002).
- S. Silverman, Oral Cancer, 3rd ed. (The American Cancer Society, Atlanta, 1990).
2010, Huang, Methods Mol. Biol.
- X. Huang, I. H. El-Sayed, and M. A. El-Sayed, “Applications of gold nanorods for cancer imaging and photothermal therapy,” Methods Mol. Biol. 624, 343–357 (2010). [CrossRef] [PubMed]
- F. Nussenbaum and I. M. Herman, “Tumor angigoenesis: insights and inovations,” J. Oncolog. 2010, 132641 (2010).
- N. Mohtasham, S. Babakoohi, J. Salehinejad, L. Montaser-Kouhsari, M. T. Shakeri, S. Shojaee, N. S. Sistani, and A. Firooz, “Mast cell density and angiogenesis in oral dysplastic epithelium and low- and high-grade oral squamous cell carcinoma,” Acta Odontol. Scand. 68(5), 300–304 (2010). [CrossRef] [PubMed]
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