Abstract

Iatrogenic nerve damage is a leading cause of morbidity associated with many common surgical procedures. Complications arising from these injuries may result in loss of function and/or sensation, muscle atrophy, and chronic neuropathy. Fluorescence image-guided surgery offers a potential solution for avoiding intraoperative nerve damage by highlighting nerves that are otherwise difficult to visualize. In this work we present the development of a single camera, dual-mode laparoscope that provides near simultaneous display of white-light and fluorescence images of nerves. The capability of the instrumentation is demonstrated through imaging several types of in situ rat nerves via a nerve specific contrast agent. Full color white light and high brightness fluorescence images and video of nerves as small as 100 µm in diameter are presented.

© 2012 OSA

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2012

V. E. Cotero, T. Siclovan, R. Zhang, R. L. Carter, A. Bajaj, N. E. LaPlante, E. Kim, D. Gray, V. P. Staudinger, S. Yazdanfar, and C. A. Tan Hehir, “Intraoperative fluorescence imaging of peripheral and central nerves through a myelin-selective contrast agent,” Mol. Imaging Biol. (2012) (online first).

T. P. Gustafson, Y. Yan, P. Newton, D. A. Hunter, S. Achilefu, W. J. Akers, S. E. Mackinnon, P. J. Johnson, and M. Y. Berezin, “A NIR dye for development of peripheral nerve targeted probes,” MedChemComm.3(6), 685–690 (2012).
[CrossRef]

M. C. Jacobson, R. deVere White, and S. G. Demos, “In vivo testing of a prototype system providing simultaneous white light and near infrared autofluorescence image acquisition for detection of bladder cancer,” J. Biomed. Opt.17(3), 036011 (2012).
[CrossRef] [PubMed]

2011

M. A. Whitney, J. L. Crisp, L. T. Nguyen, B. Friedman, L. A. Gross, P. Steinbach, R. Y. Tsien, and Q. T. Nguyen, “Fluorescent peptides highlight peripheral nerves during surgery in mice,” Nat. Biotechnol.29(4), 352–356 (2011).
[CrossRef] [PubMed]

S. L. Gibbs-Strauss, K. A. Nasr, K. M. Fish, O. Khullar, Y. Ashitate, T. M. Siclovan, B. F. Johnson, N. E. Barnhardt, C. A. Tan Hehir, and J. V. Frangioni, “Nerve-highlighting fluorescent contrast agents for image-guided surgery,” Mol. Imaging10(2), 91–101 (2011).
[PubMed]

H. G. van der Poel, T. Buckle, O. R. Brouwer, R. A. Valdés Olmos, and F. W. B. van Leeuwen, “Intraoperative laparoscopic fluorescence guidance to the sentinel lymph node in prostate cancer patients: clinical proof of concept of an integrated functional imaging approach using a multimodal tracer,” Eur. Urol.60(4), 826–833 (2011).
[CrossRef] [PubMed]

S. Tobis, J. Knopf, C. Silvers, J. Yao, H. Rashid, G. Wu, and D. Golijanin, “Near infrared fluorescence imaging with robotic assisted laparoscopic partial nephrectomy: initial clinical experience for renal cortical tumors,” J. Urol.186(1), 47–52 (2011).
[CrossRef] [PubMed]

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med.17(10), 1315–1319 (2011).
[CrossRef] [PubMed]

S. Keereweer, J. D. F. Kerrebijn, P. B. A. A. van Driel, B. Xie, E. L. Kaijzel, T. J. A. Snoeks, I. Que, M. Hutteman, J. R. van der Vorst, J. S. D. Mieog, A. L. Vahrmeijer, C. J. H. van de Velde, R. J. Baatenburg de Jong, and C. W. G. M. Löwik, “Optical image-guided surgery--where do we stand?” Mol. Imaging Biol.13(2), 199–207 (2011).
[CrossRef] [PubMed]

J. W. Kakareka, T. E. McCann, N. Kosaka, M. Mitsunaga, N. Y. Morgan, T. J. Pohida, P. L. Choyke, and H. Kobayashi, “A portable fluorescence camera for testing surgical specimens in the operating room: description and early evaluation,” Mol. Imaging Biol.13(5), 862–867 (2011).
[CrossRef] [PubMed]

Y. Liu, A. Q. Bauer, W. J. Akers, G. Sudlow, K. Liang, D. Shen, M. Y. Berezin, J. P. Culver, and S. Achilefu, “Hands-free, wireless goggles for near-infrared fluorescence and real-time image-guided surgery,” Surgery149(5), 689–698 (2011).
[CrossRef] [PubMed]

H. S. Tran Cao, S. Kaushal, C. Lee, C. S. Snyder, K. J. Thompson, S. Horgan, M. A. Talamini, R. M. Hoffman, and M. Bouvet, “Fluorescence laparoscopy imaging of pancreatic tumor progression in an orthotopic mouse model,” Surg. Endosc.25(1), 48–54 (2011).
[CrossRef] [PubMed]

2010

J. S. D. Mieog, A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, M. Drijfhout van Hooff, J. Dijkstra, P. J. K. Kuppen, R. Keijzer, E. L. Kaijzel, I. Que, C. J. H. van de Velde, and C. W. G. M. Löwik, “Novel intraoperative near-infrared fluorescence camera system for optical image-guided cancer surgery,” Mol. Imaging9(4), 223–231 (2010).
[PubMed]

N. Tagaya, A. Nakagawa, A. Abe, Y. Iwasaki, and K. Kubota, “Non-invasive identification of sentinel lymph nodes using indocyanine green fluorescence imaging in patients with breast cancer,” Open Surg. Oncol. J.2(2), 71–74 (2010).
[CrossRef]

B. W. Pogue, S. L. Gibbs-Strauss, P. A. Valdés, K. S. Samkoe, D. W. Roberts, and K. D. Paulsen, “Review of neurosurgical fluorescence imaging methodologies,” IEEE J. Sel. Top. Quantum Electron.16(3), 493–505 (2010).
[CrossRef] [PubMed]

S. Gioux, H. S. Choi, and J. V. Frangioni, “Image-guided surgery using invisible near-infrared light: fundamentals of clinical translation,” Mol. Imaging9(5), 237–255 (2010).
[PubMed]

V. Ntziachristos, J. S. Yoo, and G. M. van Dam, “Current concepts and future perspectives on surgical optical imaging in cancer,” J. Biomed. Opt.15(6), 066024 (2010).
[CrossRef] [PubMed]

X. Wang, S. Bhaumik, Q. Li, V. P. Staudinger, and S. Yazdanfar, “Compact instrument for fluorescence image-guided surgery,” J. Biomed. Opt.15(2), 020509 (2010).
[CrossRef] [PubMed]

L. Kong, D. Yi, S. Sprigle, F. Wang, C. Wang, F. Liu, A. Adibi, and R. Tummala, “Single sensor that outputs narrowband multispectral images,” J. Biomed. Opt.15(1), 010502 (2010).
[CrossRef] [PubMed]

R. Sun, M. B. Bouchard, and E. M. C. Hillman, “SPLASSH: Open source software for camera-based high-speed, multispectral in-vivo optical image acquisition,” Biomed. Opt. Express1(2), 385–397 (2010).
[CrossRef] [PubMed]

2009

D. Schellingerhout, L. G. Le Roux, S. Bredow, and J. G. Gelovani, “Fluorescence imaging of fast retrograde axonal transport in living animals,” Mol. Imaging8(6), 319–329 (2009).
[PubMed]

S. L. Troyan, V. Kianzad, S. L. Gibbs-Strauss, S. Gioux, A. Matsui, R. Oketokoun, L. Ngo, A. Khamene, F. Azar, and J. V. Frangioni, “The FLARE intraoperative near-infrared fluorescence imaging system: a first-in-human clinical trial in breast cancer sentinel lymph node mapping,” Ann. Surg. Oncol.16(10), 2943–2952 (2009).
[CrossRef] [PubMed]

R. Yadav, S. Mukherjee, M. Hermen, G. Tan, F. R. Maxfield, W. W. Webb, and A. K. Tewari, “Multiphoton microscopy of prostate and periprostatic neural tissue: a promising imaging technique for improving nerve-sparing prostatectomy,” J. Endourol.23(5), 861–867 (2009).
[CrossRef] [PubMed]

2008

D. S. Cooper, “Thyroxine monotherapy after thyroidectomy: coming full circle,” JAMA299(7), 817–819 (2008).
[CrossRef] [PubMed]

M. D. Michaelson, S. E. Cotter, P. C. Gargollo, A. L. Zietman, D. M. Dahl, and M. R. Smith, “Management of complications of prostate cancer treatment,” CA Cancer J. Clin.58(4), 196–213 (2008).
[CrossRef] [PubMed]

E. M. Sevick-Muraca and J. C. Rasmussen, “Molecular imaging with optics: primer and case for near-infrared fluorescence techniques in personalized medicine,” J. Biomed. Opt.13(4), 041303 (2008).
[CrossRef] [PubMed]

G. Themelis, J. S. Yoo, and V. Ntziachristos, “Multispectral imaging using multiple-bandpass filters,” Opt. Lett.33(9), 1023–1025 (2008).
[CrossRef] [PubMed]

Y. Fu, T. B. Huff, H.-W. Wang, J.-X. Cheng, and H. Wang, “Ex vivo and in vivo imaging of myelin fibers in mouse brain by coherent anti-Stokes Raman scattering microscopy,” Opt. Express16(24), 19396–19409 (2008).
[CrossRef] [PubMed]

2007

S. C. Gebhart, R. C. Thompson, and A. Mahadevan-Jansen, “Liquid-crystal tunable filter spectral imaging for brain tumor demarcation,” Appl. Opt.46(10), 1896–1910 (2007).
[CrossRef] [PubMed]

L. B. Boyette, M. A. Reardon, A. J. Mirelman, T. D. Kirkley, J. J. Lysiak, J. B. Tuttle, and W. D. Steers, “Fiberoptic imaging of cavernous nerves in vivo,” J. Urol.178(6), 2694–2700 (2007).
[CrossRef] [PubMed]

J. Walz, M. Graefen, and H. Huland, “Basic principles of anatomy for optimal surgical treatment of prostate cancer,” World J. Urol.25(1), 31–38 (2007).
[CrossRef] [PubMed]

2006

E. L. Poleshuck, J. Katz, C. H. Andrus, L. A. Hogan, B. F. Jung, D. I. Kulick, and R. H. Dworkin, “Risk factors for chronic pain following breast cancer surgery: a prospective study,” J. Pain7(9), 626–634 (2006).
[CrossRef] [PubMed]

T. M. Peters, “Image-guidance for surgical procedures,” Phys. Med. Biol.51(14), R505–R540 (2006).
[CrossRef] [PubMed]

P. S. Adusumilli, D. P. Eisenberg, B. M. Stiles, S. Chung, M. K. Chan, V. W. Rusch, and Y. Fong, “Intraoperative localization of lymph node metastases with a replication-competent herpes simplex virus,” J. Thorac. Cardiovasc. Surg.132(5), 1179–1188.e1 (2006).
[CrossRef] [PubMed]

2005

A. Katahira, H. Niikura, Y. Kaiho, H. Nakagawa, K. Kurokawa, Y. Arai, and N. Yaegashi, “Intraoperative electrical stimulation of the pelvic splanchnic nerves during nerve-sparing radical hysterectomy,” Gynecol. Oncol.98(3), 462–466 (2005).
[CrossRef] [PubMed]

L. Macdonald, J. Bruce, N. W. Scott, W. C. Smith, and W. A. Chambers, “Long-term follow-up of breast cancer survivors with post-mastectomy pain syndrome,” Br. J. Cancer92(2), 225–230 (2005).
[PubMed]

2003

J. Bruce, N. Drury, A. S. Poobalan, R. R. Jeffrey, W. C. Smith, and W. A. Chambers, “The prevalence of chronic chest and leg pain following cardiac surgery: a historical cohort study,” Pain104(1-2), 265–273 (2003).
[CrossRef] [PubMed]

J. V. Frangioni, “In vivo near-infrared fluorescence imaging,” Curr. Opin. Chem. Biol.7(5), 626–634 (2003).
[CrossRef] [PubMed]

D. P. Taggart, B. Choudhary, K. Anastasiadis, Y. Abu-Omar, L. Balacumaraswami, and D. W. Pigott, “Preliminary experience with a novel intraoperative fluorescence imaging technique to evaluate the patency of bypass grafts in total arterial revascularization,” Ann. Thorac. Surg.75(3), 870–873 (2003).
[CrossRef] [PubMed]

2002

J. Gahlen, R. L. Prosst, M. Pietschmann, T. Haase, M. Rheinwald, G. Skopp, J. Stern, and C. Herfarth, “Laparoscopic fluorescence diagnosis for intraabdominal fluorescence targeting of peritoneal carcinosis experimental studies,” Ann. Surg.235(2), 252–260 (2002).
[CrossRef] [PubMed]

2001

P. Aluffi, M. Policarpo, C. Cherovac, M. Olina, R. Dosdegani, and F. Pia, “Post-thyroidectomy superior laryngeal nerve injury,” Eur. Arch. Otorhinolaryngol.258(9), 451–454 (2001).
[CrossRef] [PubMed]

2000

A. D. Sharma, C. L. Parmley, G. Sreeram, and H. P. Grocott, “Peripheral nerve injuries during cardiac surgery: risk factors, diagnosis, prognosis, and prevention,” Anesth. Analg.91(6), 1358–1369 (2000).
[CrossRef] [PubMed]

1999

J. Rehman, G. J. Christ, A. Kaynan, D. Samadi, and J. Fleischmann, “Intraoperative electrical stimulation of cavernosal nerves with monitoring of intracorporeal pressure in patients undergoing nerve sparing radical prostatectomy,” BJU Int.84(3), 305–310 (1999).
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G. A. Reynolds and K. H. Drexhage, “New coumarin dyes with rigidized structure for flashlamp-pumped dye lasers,” Opt. Commun.13(3), 222–225 (1975).
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J. Bruce, N. Drury, A. S. Poobalan, R. R. Jeffrey, W. C. Smith, and W. A. Chambers, “The prevalence of chronic chest and leg pain following cardiac surgery: a historical cohort study,” Pain104(1-2), 265–273 (2003).
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E. L. Poleshuck, J. Katz, C. H. Andrus, L. A. Hogan, B. F. Jung, D. I. Kulick, and R. H. Dworkin, “Risk factors for chronic pain following breast cancer surgery: a prospective study,” J. Pain7(9), 626–634 (2006).
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P. S. Adusumilli, D. P. Eisenberg, B. M. Stiles, S. Chung, M. K. Chan, V. W. Rusch, and Y. Fong, “Intraoperative localization of lymph node metastases with a replication-competent herpes simplex virus,” J. Thorac. Cardiovasc. Surg.132(5), 1179–1188.e1 (2006).
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S. L. Gibbs-Strauss, K. A. Nasr, K. M. Fish, O. Khullar, Y. Ashitate, T. M. Siclovan, B. F. Johnson, N. E. Barnhardt, C. A. Tan Hehir, and J. V. Frangioni, “Nerve-highlighting fluorescent contrast agents for image-guided surgery,” Mol. Imaging10(2), 91–101 (2011).
[PubMed]

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J. Rehman, G. J. Christ, A. Kaynan, D. Samadi, and J. Fleischmann, “Intraoperative electrical stimulation of cavernosal nerves with monitoring of intracorporeal pressure in patients undergoing nerve sparing radical prostatectomy,” BJU Int.84(3), 305–310 (1999).
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P. S. Adusumilli, D. P. Eisenberg, B. M. Stiles, S. Chung, M. K. Chan, V. W. Rusch, and Y. Fong, “Intraoperative localization of lymph node metastases with a replication-competent herpes simplex virus,” J. Thorac. Cardiovasc. Surg.132(5), 1179–1188.e1 (2006).
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S. L. Gibbs-Strauss, K. A. Nasr, K. M. Fish, O. Khullar, Y. Ashitate, T. M. Siclovan, B. F. Johnson, N. E. Barnhardt, C. A. Tan Hehir, and J. V. Frangioni, “Nerve-highlighting fluorescent contrast agents for image-guided surgery,” Mol. Imaging10(2), 91–101 (2011).
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S. Gioux, H. S. Choi, and J. V. Frangioni, “Image-guided surgery using invisible near-infrared light: fundamentals of clinical translation,” Mol. Imaging9(5), 237–255 (2010).
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D. Schellingerhout, L. G. Le Roux, S. Bredow, and J. G. Gelovani, “Fluorescence imaging of fast retrograde axonal transport in living animals,” Mol. Imaging8(6), 319–329 (2009).
[PubMed]

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S. L. Gibbs-Strauss, K. A. Nasr, K. M. Fish, O. Khullar, Y. Ashitate, T. M. Siclovan, B. F. Johnson, N. E. Barnhardt, C. A. Tan Hehir, and J. V. Frangioni, “Nerve-highlighting fluorescent contrast agents for image-guided surgery,” Mol. Imaging10(2), 91–101 (2011).
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S. Gioux, H. S. Choi, and J. V. Frangioni, “Image-guided surgery using invisible near-infrared light: fundamentals of clinical translation,” Mol. Imaging9(5), 237–255 (2010).
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N. Tagaya, A. Nakagawa, A. Abe, Y. Iwasaki, and K. Kubota, “Non-invasive identification of sentinel lymph nodes using indocyanine green fluorescence imaging in patients with breast cancer,” Open Surg. Oncol. J.2(2), 71–74 (2010).
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E. L. Poleshuck, J. Katz, C. H. Andrus, L. A. Hogan, B. F. Jung, D. I. Kulick, and R. H. Dworkin, “Risk factors for chronic pain following breast cancer surgery: a prospective study,” J. Pain7(9), 626–634 (2006).
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J. S. D. Mieog, A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, M. Drijfhout van Hooff, J. Dijkstra, P. J. K. Kuppen, R. Keijzer, E. L. Kaijzel, I. Que, C. J. H. van de Velde, and C. W. G. M. Löwik, “Novel intraoperative near-infrared fluorescence camera system for optical image-guided cancer surgery,” Mol. Imaging9(4), 223–231 (2010).
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A. Katahira, H. Niikura, Y. Kaiho, H. Nakagawa, K. Kurokawa, Y. Arai, and N. Yaegashi, “Intraoperative electrical stimulation of the pelvic splanchnic nerves during nerve-sparing radical hysterectomy,” Gynecol. Oncol.98(3), 462–466 (2005).
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[PubMed]

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L. B. Boyette, M. A. Reardon, A. J. Mirelman, T. D. Kirkley, J. J. Lysiak, J. B. Tuttle, and W. D. Steers, “Fiberoptic imaging of cavernous nerves in vivo,” J. Urol.178(6), 2694–2700 (2007).
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Matsui, A.

S. L. Troyan, V. Kianzad, S. L. Gibbs-Strauss, S. Gioux, A. Matsui, R. Oketokoun, L. Ngo, A. Khamene, F. Azar, and J. V. Frangioni, “The FLARE intraoperative near-infrared fluorescence imaging system: a first-in-human clinical trial in breast cancer sentinel lymph node mapping,” Ann. Surg. Oncol.16(10), 2943–2952 (2009).
[CrossRef] [PubMed]

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R. Yadav, S. Mukherjee, M. Hermen, G. Tan, F. R. Maxfield, W. W. Webb, and A. K. Tewari, “Multiphoton microscopy of prostate and periprostatic neural tissue: a promising imaging technique for improving nerve-sparing prostatectomy,” J. Endourol.23(5), 861–867 (2009).
[CrossRef] [PubMed]

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J. W. Kakareka, T. E. McCann, N. Kosaka, M. Mitsunaga, N. Y. Morgan, T. J. Pohida, P. L. Choyke, and H. Kobayashi, “A portable fluorescence camera for testing surgical specimens in the operating room: description and early evaluation,” Mol. Imaging Biol.13(5), 862–867 (2011).
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[CrossRef] [PubMed]

J. S. D. Mieog, A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, M. Drijfhout van Hooff, J. Dijkstra, P. J. K. Kuppen, R. Keijzer, E. L. Kaijzel, I. Que, C. J. H. van de Velde, and C. W. G. M. Löwik, “Novel intraoperative near-infrared fluorescence camera system for optical image-guided cancer surgery,” Mol. Imaging9(4), 223–231 (2010).
[PubMed]

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L. B. Boyette, M. A. Reardon, A. J. Mirelman, T. D. Kirkley, J. J. Lysiak, J. B. Tuttle, and W. D. Steers, “Fiberoptic imaging of cavernous nerves in vivo,” J. Urol.178(6), 2694–2700 (2007).
[CrossRef] [PubMed]

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J. W. Kakareka, T. E. McCann, N. Kosaka, M. Mitsunaga, N. Y. Morgan, T. J. Pohida, P. L. Choyke, and H. Kobayashi, “A portable fluorescence camera for testing surgical specimens in the operating room: description and early evaluation,” Mol. Imaging Biol.13(5), 862–867 (2011).
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K. Ponnusamy, J. M. Sorger, and C. Mohr, “Nerve mapping for prostatectomies: novel technologies under development,” J. Endourol. (to be published).
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J. W. Kakareka, T. E. McCann, N. Kosaka, M. Mitsunaga, N. Y. Morgan, T. J. Pohida, P. L. Choyke, and H. Kobayashi, “A portable fluorescence camera for testing surgical specimens in the operating room: description and early evaluation,” Mol. Imaging Biol.13(5), 862–867 (2011).
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R. Yadav, S. Mukherjee, M. Hermen, G. Tan, F. R. Maxfield, W. W. Webb, and A. K. Tewari, “Multiphoton microscopy of prostate and periprostatic neural tissue: a promising imaging technique for improving nerve-sparing prostatectomy,” J. Endourol.23(5), 861–867 (2009).
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N. Tagaya, A. Nakagawa, A. Abe, Y. Iwasaki, and K. Kubota, “Non-invasive identification of sentinel lymph nodes using indocyanine green fluorescence imaging in patients with breast cancer,” Open Surg. Oncol. J.2(2), 71–74 (2010).
[CrossRef]

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A. Katahira, H. Niikura, Y. Kaiho, H. Nakagawa, K. Kurokawa, Y. Arai, and N. Yaegashi, “Intraoperative electrical stimulation of the pelvic splanchnic nerves during nerve-sparing radical hysterectomy,” Gynecol. Oncol.98(3), 462–466 (2005).
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S. L. Gibbs-Strauss, K. A. Nasr, K. M. Fish, O. Khullar, Y. Ashitate, T. M. Siclovan, B. F. Johnson, N. E. Barnhardt, C. A. Tan Hehir, and J. V. Frangioni, “Nerve-highlighting fluorescent contrast agents for image-guided surgery,” Mol. Imaging10(2), 91–101 (2011).
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D. P. Taggart, B. Choudhary, K. Anastasiadis, Y. Abu-Omar, L. Balacumaraswami, and D. W. Pigott, “Preliminary experience with a novel intraoperative fluorescence imaging technique to evaluate the patency of bypass grafts in total arterial revascularization,” Ann. Thorac. Surg.75(3), 870–873 (2003).
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S. Tobis, J. Knopf, C. Silvers, J. Yao, H. Rashid, G. Wu, and D. Golijanin, “Near infrared fluorescence imaging with robotic assisted laparoscopic partial nephrectomy: initial clinical experience for renal cortical tumors,” J. Urol.186(1), 47–52 (2011).
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B. W. Pogue, S. L. Gibbs-Strauss, P. A. Valdés, K. S. Samkoe, D. W. Roberts, and K. D. Paulsen, “Review of neurosurgical fluorescence imaging methodologies,” IEEE J. Sel. Top. Quantum Electron.16(3), 493–505 (2010).
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P. S. Adusumilli, D. P. Eisenberg, B. M. Stiles, S. Chung, M. K. Chan, V. W. Rusch, and Y. Fong, “Intraoperative localization of lymph node metastases with a replication-competent herpes simplex virus,” J. Thorac. Cardiovasc. Surg.132(5), 1179–1188.e1 (2006).
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J. Rehman, G. J. Christ, A. Kaynan, D. Samadi, and J. Fleischmann, “Intraoperative electrical stimulation of cavernosal nerves with monitoring of intracorporeal pressure in patients undergoing nerve sparing radical prostatectomy,” BJU Int.84(3), 305–310 (1999).
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B. W. Pogue, S. L. Gibbs-Strauss, P. A. Valdés, K. S. Samkoe, D. W. Roberts, and K. D. Paulsen, “Review of neurosurgical fluorescence imaging methodologies,” IEEE J. Sel. Top. Quantum Electron.16(3), 493–505 (2010).
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G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med.17(10), 1315–1319 (2011).
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D. Schellingerhout, L. G. Le Roux, S. Bredow, and J. G. Gelovani, “Fluorescence imaging of fast retrograde axonal transport in living animals,” Mol. Imaging8(6), 319–329 (2009).
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E. M. Sevick-Muraca and J. C. Rasmussen, “Molecular imaging with optics: primer and case for near-infrared fluorescence techniques in personalized medicine,” J. Biomed. Opt.13(4), 041303 (2008).
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A. D. Sharma, C. L. Parmley, G. Sreeram, and H. P. Grocott, “Peripheral nerve injuries during cardiac surgery: risk factors, diagnosis, prognosis, and prevention,” Anesth. Analg.91(6), 1358–1369 (2000).
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S. L. Gibbs-Strauss, K. A. Nasr, K. M. Fish, O. Khullar, Y. Ashitate, T. M. Siclovan, B. F. Johnson, N. E. Barnhardt, C. A. Tan Hehir, and J. V. Frangioni, “Nerve-highlighting fluorescent contrast agents for image-guided surgery,” Mol. Imaging10(2), 91–101 (2011).
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S. Tobis, J. Knopf, C. Silvers, J. Yao, H. Rashid, G. Wu, and D. Golijanin, “Near infrared fluorescence imaging with robotic assisted laparoscopic partial nephrectomy: initial clinical experience for renal cortical tumors,” J. Urol.186(1), 47–52 (2011).
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J. Gahlen, R. L. Prosst, M. Pietschmann, T. Haase, M. Rheinwald, G. Skopp, J. Stern, and C. Herfarth, “Laparoscopic fluorescence diagnosis for intraabdominal fluorescence targeting of peritoneal carcinosis experimental studies,” Ann. Surg.235(2), 252–260 (2002).
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S. Keereweer, J. D. F. Kerrebijn, P. B. A. A. van Driel, B. Xie, E. L. Kaijzel, T. J. A. Snoeks, I. Que, M. Hutteman, J. R. van der Vorst, J. S. D. Mieog, A. L. Vahrmeijer, C. J. H. van de Velde, R. J. Baatenburg de Jong, and C. W. G. M. Löwik, “Optical image-guided surgery--where do we stand?” Mol. Imaging Biol.13(2), 199–207 (2011).
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H. S. Tran Cao, S. Kaushal, C. Lee, C. S. Snyder, K. J. Thompson, S. Horgan, M. A. Talamini, R. M. Hoffman, and M. Bouvet, “Fluorescence laparoscopy imaging of pancreatic tumor progression in an orthotopic mouse model,” Surg. Endosc.25(1), 48–54 (2011).
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K. Ponnusamy, J. M. Sorger, and C. Mohr, “Nerve mapping for prostatectomies: novel technologies under development,” J. Endourol. (to be published).
[PubMed]

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L. Kong, D. Yi, S. Sprigle, F. Wang, C. Wang, F. Liu, A. Adibi, and R. Tummala, “Single sensor that outputs narrowband multispectral images,” J. Biomed. Opt.15(1), 010502 (2010).
[CrossRef] [PubMed]

Sreeram, G.

A. D. Sharma, C. L. Parmley, G. Sreeram, and H. P. Grocott, “Peripheral nerve injuries during cardiac surgery: risk factors, diagnosis, prognosis, and prevention,” Anesth. Analg.91(6), 1358–1369 (2000).
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V. E. Cotero, T. Siclovan, R. Zhang, R. L. Carter, A. Bajaj, N. E. LaPlante, E. Kim, D. Gray, V. P. Staudinger, S. Yazdanfar, and C. A. Tan Hehir, “Intraoperative fluorescence imaging of peripheral and central nerves through a myelin-selective contrast agent,” Mol. Imaging Biol. (2012) (online first).

X. Wang, S. Bhaumik, Q. Li, V. P. Staudinger, and S. Yazdanfar, “Compact instrument for fluorescence image-guided surgery,” J. Biomed. Opt.15(2), 020509 (2010).
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L. B. Boyette, M. A. Reardon, A. J. Mirelman, T. D. Kirkley, J. J. Lysiak, J. B. Tuttle, and W. D. Steers, “Fiberoptic imaging of cavernous nerves in vivo,” J. Urol.178(6), 2694–2700 (2007).
[CrossRef] [PubMed]

Steinbach, P.

M. A. Whitney, J. L. Crisp, L. T. Nguyen, B. Friedman, L. A. Gross, P. Steinbach, R. Y. Tsien, and Q. T. Nguyen, “Fluorescent peptides highlight peripheral nerves during surgery in mice,” Nat. Biotechnol.29(4), 352–356 (2011).
[CrossRef] [PubMed]

Stern, J.

J. Gahlen, R. L. Prosst, M. Pietschmann, T. Haase, M. Rheinwald, G. Skopp, J. Stern, and C. Herfarth, “Laparoscopic fluorescence diagnosis for intraabdominal fluorescence targeting of peritoneal carcinosis experimental studies,” Ann. Surg.235(2), 252–260 (2002).
[CrossRef] [PubMed]

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P. S. Adusumilli, D. P. Eisenberg, B. M. Stiles, S. Chung, M. K. Chan, V. W. Rusch, and Y. Fong, “Intraoperative localization of lymph node metastases with a replication-competent herpes simplex virus,” J. Thorac. Cardiovasc. Surg.132(5), 1179–1188.e1 (2006).
[CrossRef] [PubMed]

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Y. Liu, A. Q. Bauer, W. J. Akers, G. Sudlow, K. Liang, D. Shen, M. Y. Berezin, J. P. Culver, and S. Achilefu, “Hands-free, wireless goggles for near-infrared fluorescence and real-time image-guided surgery,” Surgery149(5), 689–698 (2011).
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D. P. Taggart, B. Choudhary, K. Anastasiadis, Y. Abu-Omar, L. Balacumaraswami, and D. W. Pigott, “Preliminary experience with a novel intraoperative fluorescence imaging technique to evaluate the patency of bypass grafts in total arterial revascularization,” Ann. Thorac. Surg.75(3), 870–873 (2003).
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H. S. Tran Cao, S. Kaushal, C. Lee, C. S. Snyder, K. J. Thompson, S. Horgan, M. A. Talamini, R. M. Hoffman, and M. Bouvet, “Fluorescence laparoscopy imaging of pancreatic tumor progression in an orthotopic mouse model,” Surg. Endosc.25(1), 48–54 (2011).
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R. Yadav, S. Mukherjee, M. Hermen, G. Tan, F. R. Maxfield, W. W. Webb, and A. K. Tewari, “Multiphoton microscopy of prostate and periprostatic neural tissue: a promising imaging technique for improving nerve-sparing prostatectomy,” J. Endourol.23(5), 861–867 (2009).
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Tan Hehir, C. A.

V. E. Cotero, T. Siclovan, R. Zhang, R. L. Carter, A. Bajaj, N. E. LaPlante, E. Kim, D. Gray, V. P. Staudinger, S. Yazdanfar, and C. A. Tan Hehir, “Intraoperative fluorescence imaging of peripheral and central nerves through a myelin-selective contrast agent,” Mol. Imaging Biol. (2012) (online first).

S. L. Gibbs-Strauss, K. A. Nasr, K. M. Fish, O. Khullar, Y. Ashitate, T. M. Siclovan, B. F. Johnson, N. E. Barnhardt, C. A. Tan Hehir, and J. V. Frangioni, “Nerve-highlighting fluorescent contrast agents for image-guided surgery,” Mol. Imaging10(2), 91–101 (2011).
[PubMed]

Tewari, A. K.

R. Yadav, S. Mukherjee, M. Hermen, G. Tan, F. R. Maxfield, W. W. Webb, and A. K. Tewari, “Multiphoton microscopy of prostate and periprostatic neural tissue: a promising imaging technique for improving nerve-sparing prostatectomy,” J. Endourol.23(5), 861–867 (2009).
[CrossRef] [PubMed]

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G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med.17(10), 1315–1319 (2011).
[CrossRef] [PubMed]

G. Themelis, J. S. Yoo, and V. Ntziachristos, “Multispectral imaging using multiple-bandpass filters,” Opt. Lett.33(9), 1023–1025 (2008).
[CrossRef] [PubMed]

Thompson, K. J.

H. S. Tran Cao, S. Kaushal, C. Lee, C. S. Snyder, K. J. Thompson, S. Horgan, M. A. Talamini, R. M. Hoffman, and M. Bouvet, “Fluorescence laparoscopy imaging of pancreatic tumor progression in an orthotopic mouse model,” Surg. Endosc.25(1), 48–54 (2011).
[CrossRef] [PubMed]

Thompson, R. C.

Tobis, S.

S. Tobis, J. Knopf, C. Silvers, J. Yao, H. Rashid, G. Wu, and D. Golijanin, “Near infrared fluorescence imaging with robotic assisted laparoscopic partial nephrectomy: initial clinical experience for renal cortical tumors,” J. Urol.186(1), 47–52 (2011).
[CrossRef] [PubMed]

Tran Cao, H. S.

H. S. Tran Cao, S. Kaushal, C. Lee, C. S. Snyder, K. J. Thompson, S. Horgan, M. A. Talamini, R. M. Hoffman, and M. Bouvet, “Fluorescence laparoscopy imaging of pancreatic tumor progression in an orthotopic mouse model,” Surg. Endosc.25(1), 48–54 (2011).
[CrossRef] [PubMed]

Troyan, S. L.

S. L. Troyan, V. Kianzad, S. L. Gibbs-Strauss, S. Gioux, A. Matsui, R. Oketokoun, L. Ngo, A. Khamene, F. Azar, and J. V. Frangioni, “The FLARE intraoperative near-infrared fluorescence imaging system: a first-in-human clinical trial in breast cancer sentinel lymph node mapping,” Ann. Surg. Oncol.16(10), 2943–2952 (2009).
[CrossRef] [PubMed]

Tsien, R. Y.

M. A. Whitney, J. L. Crisp, L. T. Nguyen, B. Friedman, L. A. Gross, P. Steinbach, R. Y. Tsien, and Q. T. Nguyen, “Fluorescent peptides highlight peripheral nerves during surgery in mice,” Nat. Biotechnol.29(4), 352–356 (2011).
[CrossRef] [PubMed]

Tummala, R.

L. Kong, D. Yi, S. Sprigle, F. Wang, C. Wang, F. Liu, A. Adibi, and R. Tummala, “Single sensor that outputs narrowband multispectral images,” J. Biomed. Opt.15(1), 010502 (2010).
[CrossRef] [PubMed]

Tuttle, J. B.

L. B. Boyette, M. A. Reardon, A. J. Mirelman, T. D. Kirkley, J. J. Lysiak, J. B. Tuttle, and W. D. Steers, “Fiberoptic imaging of cavernous nerves in vivo,” J. Urol.178(6), 2694–2700 (2007).
[CrossRef] [PubMed]

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S. Keereweer, J. D. F. Kerrebijn, P. B. A. A. van Driel, B. Xie, E. L. Kaijzel, T. J. A. Snoeks, I. Que, M. Hutteman, J. R. van der Vorst, J. S. D. Mieog, A. L. Vahrmeijer, C. J. H. van de Velde, R. J. Baatenburg de Jong, and C. W. G. M. Löwik, “Optical image-guided surgery--where do we stand?” Mol. Imaging Biol.13(2), 199–207 (2011).
[CrossRef] [PubMed]

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[PubMed]

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[CrossRef] [PubMed]

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G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med.17(10), 1315–1319 (2011).
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Supplementary Material (1)

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Figures (7)

Fig. 1
Fig. 1

Single camera, dual-mode laparoscopic FIGS instrument. (a) Photograph of the laparoscope, coupler, camera with filter, and light guide. (b) Schematic of the illumination path. The LED and 405 nm laser are collimated and coupled into the light guide with aspheric lenses and combined with a dichroic mirror. A longpass filter in the LED path filters the white light spectrum below 450 nm.

Fig. 2
Fig. 2

Timing diagrams indicating synchronization of the camera and light sources. The camera sync output (black) is used to drive the laser (red) and LED (blue) modulation via a digital pulse generator. All waveforms are 5V in amplitude.

Fig. 3
Fig. 3

Fluorescence spectra of the contrast agent GE3082 taken before (blue) and after (red) addition of native myelin basic protein (MBP), its biological target. The agent demonstrates increased fluorescence intensity upon binding to MBP. The average of the enhancement factor (green triangles) across this spectral range is 17.0 ± 0.72 for the specified concentrations of agent (10 μM) and protein (1.6 μM).

Fig. 4
Fig. 4

Image of USAF resolution chart taken on axis at a working distance of 25 mm, demonstrating the spatial resolution of the instrument. Group number 2, element 6 can be easily resolved, corresponding to 7.13 lp/mm, or ~70 μm.

Fig. 5
Fig. 5

Laparoscopic surgery of fluorescently labeled nerves in rodent model, shown under white light (left column) and fluorescence (right column) obtained with the single camera, dual-mode laparoscopic instrument. Both channels are displayed in true color. All scale bars = 1 mm. Red arrows indicate the primary nerves imaged, which include the (a) sciatic, (b) brachial, (c) median, (d) vagus, and (e) phrenic nerves. The yellow arrow (b) shows a branch of the phrenic nerve, with ~100 µm diameter, and branches of the radial, ulnar, and median nerves in close proximity.

Fig. 6
Fig. 6

Single-frame excerpt from video recordings of simultaneous white light (left) and fluorescence (right) imaging of the rat phrenic nerve (Media 1).

Fig. 7
Fig. 7

Results of control experiment, highlighting the sciatic nerve under (a) white light and (b) fluorescence. The inset in (b) is the image intensity histogram, showing no signal in the fluorescence channel, in the absence of injected dye. Scale bar ~1 mm.

Tables (1)

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Table 1 Optical characterization of GE3082

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