DOI QR코드

DOI QR Code

Real-Time Fluorescence Imaging in Thoracic Surgery

  • Das, Priyanka (Gordon Center for Medical Imaging, Department of Radiology, Massachusetts General Hospital and Harvard Medical School) ;
  • Santos, Sheena (Gordon Center for Medical Imaging, Department of Radiology, Massachusetts General Hospital and Harvard Medical School) ;
  • Park, G. Kate (Gordon Center for Medical Imaging, Department of Radiology, Massachusetts General Hospital and Harvard Medical School) ;
  • I, Hoseok (Department of Thoracic and Cardiovascular Surgery, Pusan National University Hospital, Pusan National University School of Medicine) ;
  • Choi, Hak Soo (Gordon Center for Medical Imaging, Department of Radiology, Massachusetts General Hospital and Harvard Medical School)
  • Received : 2018.11.27
  • Accepted : 2018.12.24
  • Published : 2019.08.05

Abstract

Near-infrared (NIR) fluorescence imaging provides a safe and cost-efficient method for immediate data acquisition and visualization of tissues, with technical advantages including minimal autofluorescence, reduced photon absorption, and low scattering in tissue. In this review, we introduce recent advances in NIR fluorescence imaging systems for thoracic surgery that improve the identification of vital tissues and facilitate the resection of tumorous tissues. When coupled with appropriate NIR fluorophores, NIR fluorescence imaging may transform current intraoperative thoracic surgery methods by enhancing the precision of surgical procedures and augmenting postoperative outcomes through improvements in diagnostic accuracy and reductions in the remission rate.

Keywords

References

  1. Park GK, Hoseok I, Kim GS, Hwang NS, Choi HS. Optical spectroscopic imaging for cell therapy and tissue engineering. Appl Spectrosc Rev 2018;53:360-75. https://doi.org/10.1080/05704928.2017.1328428
  2. Owens EA, Henary M, El Fakhri G, Choi HS. Tissue-specific near-infrared fluorescence imaging. Acc Chem Res 2016;49:1731-40. https://doi.org/10.1021/acs.accounts.6b00239
  3. Haidekker MA. Computed tomography. In: Haidekker MA, editor. Medical imaging technology. New York (NY): Springer; 2013. p. 37-53.
  4. Osaki Y, Hatazawa J. PET/SPECT. Equil Res 2009;68:54-61. https://doi.org/10.3757/jser.68.54
  5. Haidekker MA. Magnetic resonance imaging. In: Haidekker MA, editor. Medical imaging technology. New York (NY): Springer; 2013. p. 67-96.
  6. Hu S, Kang H, Baek Y, El Fakhri G, Kuang A, Choi HS. Realtime imaging of brain tumor for image-guided surgery. Adv Healthc Mater 2018;7:1800066. https://doi.org/10.1002/adhm.201800066
  7. Haidekker MA. X-ray projection imaging. In: Haidekker MA, editor. Medical imaging technology. New York (NY): Springer; 2013. p. 13-35.
  8. Haidekker MA. Ultrasound imaging. In: Haidekker MA, editor. Medical imaging technology. New York (NY): Springer; 2013. p. 97-110.
  9. Owens EA, Lee S, Choi J, Henary M, Choi HS. NIR fluorescent small molecules for intraoperative imaging. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2015;7:828-38. https://doi.org/10.1002/wnan.1337
  10. Kim T, O'Brien C, Choi HS, Jeong MY. Fluorescence molecular imaging systems for intraoperative image-guided surgery. Appl Spectrosc Rev 2018;53:349-59. https://doi.org/10.1080/05704928.2017.1323311
  11. Son J, Yi G, Yoo J, Park C, Koo H, Choi HS. Light-responsive nanomedicine for biophotonic imaging and targeted therapy. Adv Drug Deliv Rev 2019;138:133-47. https://doi.org/10.1016/j.addr.2018.10.002
  12. DSouza AV, Lin H, Henderson ER, Samkoe KS, Pogue BW. Review of fluorescence guided surgery systems: identification of key performance capabilities beyond indocyanine green imaging. J Biomed Opt 2016;21:80901. https://doi.org/10.1117/1.JBO.21.8.080901
  13. Yang AW, Cho SU, Jeong MY, Choi HS. NIR fluorescence imaging systems with optical packaging technology. J Microelectron Packag Soc 2014;21:25-31.
  14. Troyan SL, Kianzad V, Gibbs-Strauss SL, et al. The FLARE intraoperative near-infrared fluorescence imaging system: a first-in-human clinical trial in breast cancer sentinel lymph node mapping. Ann Surg Oncol 2009;16:2943-52. https://doi.org/10.1245/s10434-009-0594-2
  15. Gioux S, Choi HS, Frangioni JV. Image-guided surgery using invisible near-infrared light: fundamentals of clinical translation. Mol Imaging 2010;9:237-55.
  16. Choi HS, Gibbs SL, Lee JH, et al. Targeted zwitterionic near-infrared fluorophores for improved optical imaging. Nat Biotechnol 2013;31:148-53. https://doi.org/10.1038/nbt.2468
  17. Hyun H, Henary M, Gao T, et al. 700-nm zwitterionic near-infrared fluorophores for dual-channel image-guided surgery. Mol Imaging Biol 2016;18:52-61. https://doi.org/10.1007/s11307-015-0870-4
  18. Ashitate Y, Kim SH, Tanaka E, et al. Two-wavelength near-infrared fluorescence for the quantitation of drug antiplatelet effects in large animal model systems. J Vasc Surg 2012;56:171-80. https://doi.org/10.1016/j.jvs.2011.11.058
  19. Ashitate Y, Levitz A, Park MH, et al. Endocrine-specific NIR fluorophores for adrenal gland targeting. Chem Commun (Camb) 2016;52:10305-8. https://doi.org/10.1039/C6CC03845J
  20. Ashitate Y, Stockdale A, Choi HS, Laurence RG, Frangioni JV. Real-time simultaneous near-infrared fluorescence imaging of bile duct and arterial anatomy. J Surg Res 2012;176:7-13. https://doi.org/10.1016/j.jss.2011.06.027
  21. Ashitate Y, Vooght CS, Hutteman M, Oketokoun R, Choi HS, Frangioni JV. Simultaneous assessment of luminal integrity and vascular perfusion of the gastrointestinal tract using dual-channel near-infrared fluorescence. Mol Imaging 2012;11:301-8.
  22. Hyun H, Owens EA, Wada H, et al. Cartilage-specific near-infrared fluorophores for biomedical imaging. Angew Chem Int Ed Engl 2015;54:8648-52. https://doi.org/10.1002/anie.201502287
  23. Hyun H, Wada H, Bao K, et al. Phosphonated near-infrared fluorophores for biomedical imaging of bone. Angew Chem Int Ed Engl 2014;53:10668-72. https://doi.org/10.1002/anie.201404930
  24. Hyun H, Park MH, Owens EA, et al. Structure-inherent targeting of near-infrared fluorophores for parathyroid and thyroid gland imaging. Nat Med 2015;21:192-7. https://doi.org/10.1038/nm.3728
  25. Kim SH, Lee JH, Hyun H, et al. Near-infrared fluorescence imaging for noninvasive trafficking of scaffold degradation. Sci Rep 2013;3:1198. https://doi.org/10.1038/srep01198
  26. Owens EA, Hyun H, Dost TL, et al. Near-infrared illumination of native tissues for image-guided surgery. J Med Chem 2016;59:5311-23. https://doi.org/10.1021/acs.jmedchem.6b00038
  27. Owens EA, Hyun H, Kim SH, et al. Highly charged cyanine fluorophores for trafficking scaffold degradation. Biomed Mater 2013;8:014109. https://doi.org/10.1088/1748-6041/8/1/014109
  28. Owens EA, Hyun H, Tawney JG, Choi HS, Henary M. Correlating molecular character of NIR imaging agents with tissue-specific uptake. J Med Chem 2015;58:4348-56. https://doi.org/10.1021/acs.jmedchem.5b00475
  29. Wada H, Hyun H, Kang H, et al. Intraoperative near-infrared fluorescence imaging of thymus in preclinical models. Ann Thorac Surg 2017;103:1132-41. https://doi.org/10.1016/j.athoracsur.2016.09.050
  30. Wada H, Hyun H, Vargas C, et al. Sentinel lymph node mapping of liver. Ann Surg Oncol 2015;22 Suppl 3:S1147-55. https://doi.org/10.1245/s10434-015-4601-5
  31. Ashitate Y, Hyun H, Kim SH, et al. Simultaneous mapping of pan and sentinel lymph nodes for real-time image- guided surgery. Theranostics 2014;4:693-700. https://doi.org/10.7150/thno.8721
  32. Wada H, Hyun H, Bao K, et al. Multivalent mannose-decorated NIR nanoprobes for targeting pan lymph nodes. Chem Eng J 2018;340:51-7. https://doi.org/10.1016/j.cej.2018.01.008
  33. Kajiwara N, Maeda J, Yoshida K, et al. Maximizing use of robot-arm no. 3 in daVinci-assisted thoracic surgery. Int Surg 2015;100:930-3. https://doi.org/10.9738/INTSURG-D-14-00259.1
  34. Luo X, Mori K, Peters TM. Advanced endoscopic navigation: surgical big data, methodology, and applications. Annu Rev Biomed Eng 2018;20:221-51. https://doi.org/10.1146/annurev-bioeng-062117-120917
  35. Han KN, Kim HK. Imaging techniques for minimally invasive thoracic surgery-Korea University Guro Hospital experiences. J Thorac Dis 2018;10(Suppl 6):S731-8. https://doi.org/10.21037/jtd.2018.03.114
  36. Kumar A, Asaf BB. Robotic thoracic surgery: the state of the art. J Minim Access Surg 2015;11:60-7. https://doi.org/10.4103/0972-9941.147693
  37. Palep JH. Robotic assisted minimally invasive surgery. J Minim Access Surg 2009;5:1-7. https://doi.org/10.4103/0972-9941.51313
  38. Wagner OJ, Louie BE, Vallieres E, Aye RW, Farivar AS. Near-infrared fluorescence imaging can help identify the contralateral phrenic nerve during robotic thymectomy. Ann Thorac Surg 2012;94:622-5. https://doi.org/10.1016/j.athoracsur.2012.04.119
  39. Latif MJ, Park BJ. Robotics in general thoracic surgery procedures. J Vis Surg 2017;3:44. https://doi.org/10.21037/jovs.2017.03.14
  40. Suda T. Transition from video-assisted thoracic surgery to robotic pulmonary surgery. J Vis Surg 2017;3:55. https://doi.org/10.21037/jovs.2017.03.04
  41. Veronesi G, Novellis P, Voulaz E, Alloisio M. Robot-assisted surgery for lung cancer: state of the art and perspectives. Lung Cancer 2016;101:28-34. https://doi.org/10.1016/j.lungcan.2016.09.004
  42. Drevet G, Conti M, Deslauriers J. Surgical anatomy of the tracheobronchial tree. J Thorac Dis 2016;8(Suppl 2):S121-9.
  43. Miot-Noirault E, Guicheux J, Vidal A, et al. In vivo experimental imaging of osteochondral defects and their healing using (99m)Tc-NTP 15-5 radiotracer. Eur J Nucl Med Mol Imaging 2012;39:1169-72. https://doi.org/10.1007/s00259-012-2081-4
  44. Jo D, Hyun H. Structure-inherent targeting of near-infrared fluorophores for image-guided surgery. Chonnam Med J 2017;53:95-102. https://doi.org/10.4068/cmj.2017.53.2.95
  45. Mailis A, Umana M, Feindel CM. Anterior intercostal nerve damage after coronary artery bypass graft surgery with use of internal thoracic artery graft. Ann Thorac Surg 2000;69:1455-8. https://doi.org/10.1016/S0003-4975(00)01186-3
  46. Kretschmer T, Heinen CW, Antoniadis G, Richter HP, Konig RW. Iatrogenic nerve injuries. Neurosurg Clin N Am 2009;20:73-90. https://doi.org/10.1016/j.nec.2008.07.025
  47. Katahira A, Niikura H, Kaiho Y, et al. Intraoperative electrical stimulation of the pelvic splanchnic nerves during nerve-sparing radical hysterectomy. Gynecol Oncol 2005;98:462-6. https://doi.org/10.1016/j.ygyno.2005.05.004
  48. Cotero VE, Siclovan T, Zhang R, et al. Intraoperative fluorescence imaging of peripheral and central nerves through a myelin-selective contrast agent. Mol Imaging Biol 2012;14:708-17. https://doi.org/10.1007/s11307-012-0555-1
  49. Vinegoni C, Botnaru I, Aikawa E, et al. Indocyanine green enables near-infrared fluorescence imaging of lipid-rich, inflamed atherosclerotic plaques. Sci Transl Med 2011;3:-84ra45. https://doi.org/10.1126/scitranslmed.3001577
  50. Shimada Y, Okumura T, Nagata T, et al. Usefulness of blood supply visualization by indocyanine green fluorescence for reconstruction during esophagectomy. Esophagus 2011;8:259-66. https://doi.org/10.1007/s10388-011-0291-7
  51. Ly HQ, Hoshino K, Pomerantseva I, et al. In vivo myocardial distribution of multipotent progenitor cells following intracoronary delivery in a swine model of myocardial infarction. Eur Heart J 2009;30:2861-8. https://doi.org/10.1093/eurheartj/ehp322
  52. Pajouhesh H, Lenz GR. Medicinal chemical properties of successful central nervous system drugs. NeuroRx 2005;2:541-53. https://doi.org/10.1602/neurorx.2.4.541
  53. He K, Zhou J, Yang F, et al. Near-infrared intraoperative imaging of thoracic sympathetic nerves: from preclinical study to clinical trial. Theranostics 2018;8:304-13. https://doi.org/10.7150/thno.22369
  54. Gibbs-Strauss SL, Nasr KA, Fish KM, et al. Nerve-highlighting fluorescent contrast agents for image-guided surgery. Mol Imaging 2011;10:91-101.
  55. Hingorani DV, Whitney MA, Friedman B, et al. Nerve-targeted probes for fluorescence-guided intraoperative imaging. Theranostics 2018;8:4226-37. https://doi.org/10.7150/thno.23084
  56. Park MH, Hyun H, Ashitate Y, et al. Prototype nerve-specific near-infrared fluorophores. Theranostics 2014;4:823-33. https://doi.org/10.7150/thno.8696
  57. Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J 2008;22:659-61. https://doi.org/10.1096/fj.07-9574LSF
  58. Araki T, Nishino M, Gao W, et al. Normal thymus in adults: appearance on CT and associations with age, sex, BMI and smoking. Eur Radiol 2016;26:15-24. https://doi.org/10.1007/s00330-015-3796-y
  59. Nasseri F, Eftekhari F. Clinical and radiologic review of the normal and abnormal thymus: pearls and pitfalls. Radiographics 2010;30:413-28. https://doi.org/10.1148/rg.302095131
  60. Chung JE, Tan S, Gao SJ, et al. Self-assembled micellar nanocomplexes comprising green tea catechin derivatives and protein drugs for cancer therapy. Nat Nanotechnol 2014;9:907-12. https://doi.org/10.1038/nnano.2014.208
  61. Chang JM, Lee HJ, Goo JM, et al. False positive and false negative FDG-PET scans in various thoracic diseases. Korean J Radiol 2006;7:57-69. https://doi.org/10.3348/kjr.2006.7.1.57
  62. Ofori LO, Withana NP, Prestwood TR, et al. Design of protease activated optical contrast agents that exploit a latent lysosomotropic effect for use in fluorescence-guided surgery. ACS Chem Biol 2015;10:1977-88. https://doi.org/10.1021/acschembio.5b00205
  63. Predina JD, Newton AD, Desphande C, Singhal S. Near-infrared intraoperative imaging during resection of an anterior mediastinal soft tissue sarcoma. Mol Clin Oncol 2018;8:86-8.
  64. Zhou J, Yang F, Jiang G, Wang J. Applications of indocyanine green based near-infrared fluorescence imaging in thoracic surgery. J Thorac Dis 2016;8(Suppl 9):S738-43. https://doi.org/10.21037/jtd.2016.09.49
  65. Wen CT, Liu YY, Fang HY, Hsieh MJ, Chao YK. Image-guided video-assisted thoracoscopic small lung tumor resection using near-infrared marking. Surg Endosc 2018;32:4673-80. https://doi.org/10.1007/s00464-018-6252-7
  66. Okusanya OT, Holt D, Heitjan D, et al. Intraoperative near-infrared imaging can identify pulmonary nodules. Ann Thorac Surg 2014;98:1223-30. https://doi.org/10.1016/j.athoracsur.2014.05.026
  67. Hihara J, Mukaida H, Hirabayashi N. Gastrointestinal stromal tumor of the esophagus: current issues of diagnosis, surgery and drug therapy. Transl Gastroenterol Hepatol 2018;3:6. https://doi.org/10.21037/tgh.2018.01.06
  68. Fujimoto S, Muguruma N, Okamoto K, et al. A novel theranostic combination of near-infrared fluorescence imaging and laser irradiation targeting c-KIT for gastrointestinal stromal tumors. Theranostics 2018;8:2313-28. https://doi.org/10.7150/thno.22027
  69. Kang H, Gravier J, Bao K, et al. Renal clearable organic nanocarriers for bioimaging and drug delivery. Adv Mater 2016;28:8162-8. https://doi.org/10.1002/adma.201601101
  70. Li X, Chen S, Jiang L, et al. Precise intraoperative sentinel lymph node biopsies guided by lymphatic drainage in breast cancer. Oncotarget 2017;8:63064-72. https://doi.org/10.18632/oncotarget.18624
  71. Khullar O, Frangioni JV, Grinstaff M, Colson YL. Imageguided sentinel lymph node mapping and nanotechnologybased nodal treatment in lung cancer using invisible near-infrared fluorescent light. Semin Thorac Cardiovasc Surg 2009;21:309-15. https://doi.org/10.1053/j.semtcvs.2009.11.009
  72. Khullar OV, Gilmore DM, Matsui A, Ashitate Y, Colson YL. Preclinical study of near-infrared-guided sentinel lymph node mapping of the porcine lung. Ann Thorac Surg 2013;95:312-8. https://doi.org/10.1016/j.athoracsur.2012.08.101
  73. Soltesz EG, Kim S, Laurence RG, et al. Intraoperative sentinel lymph node mapping of the lung using near-infrared fluorescent quantum dots. Ann Thorac Surg 2005;79:269-77. https://doi.org/10.1016/j.athoracsur.2004.06.055
  74. Kim S, Lim YT, Soltesz EG, et al. Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping. Nat Biotechnol 2004;22:93-7. https://doi.org/10.1038/nbt920
  75. Frangioni JV, Kim SW, Ohnishi S, Kim S, Bawendi MG. Sentinel lymph node mapping with type-II quantum dots. Methods Mol Biol 2007;374:147-59.
  76. Parungo CP, Ohnishi S, De Grand AM, et al. In vivo optical imaging of pleural space drainage to lymph nodes of prognostic significance. Ann Surg Oncol 2004;11:1085-92. https://doi.org/10.1245/ASO.2004.03.054
  77. Parungo CP, Colson YL, Kim SW, et al. Sentinel lymph node mapping of the pleural space. Chest 2005;127:1799-804. https://doi.org/10.1378/chest.127.5.1799
  78. Chi C, Ye J, Ding H, et al. Use of indocyanine green for detecting the sentinel lymph node in breast cancer patients: from preclinical evaluation to clinical validation. PLoS One 2013;8:e83927. https://doi.org/10.1371/journal.pone.0083927
  79. Sugie T, Kinoshita T, Masuda N, et al. Evaluation of the clinical utility of the ICG fluorescence method compared with the radioisotope method for sentinel lymph node biopsy in breast cancer. Ann Surg Oncol 2016;23:44-50. https://doi.org/10.1245/s10434-015-4809-4
  80. Grischke EM, Rohm C, Hahn M, Helms G, Brucker S, Wallwiener D. ICG fluorescence technique for the detection of sentinel lymph nodes in breast cancer: results of a prospective open-label clinical trial. Geburtshilfe Frauenheilkd 2015;75:935-40. https://doi.org/10.1055/s-0035-1557905
  81. Hirche C, Murawa D, Mohr Z, Kneif S, Hunerbein M. ICG fluorescence-guided sentinel node biopsy for axillary nodal staging in breast cancer. Breast Cancer Res Treat 2010;121:373-8. https://doi.org/10.1007/s10549-010-0760-z
  82. Tagaya N, Yamazaki R, Nakagawa A, et al. Intraoperative identification of sentinel lymph nodes by near-infrared fluorescence imaging in patients with breast cancer. Am J Surg 2008;195:850-3. https://doi.org/10.1016/j.amjsurg.2007.02.032
  83. Guo J, Yang H, Wang S, et al. Comparison of sentinel lymph node biopsy guided by indocyanine green, blue dye, and their combination in breast cancer patients: a prospective cohort study. World J Surg Oncol 2017;15:196. https://doi.org/10.1186/s12957-017-1264-7
  84. Tagaya N, Aoyagi H, Nakagawa A, et al. A novel approach for sentinel lymph node identification using fluorescence imaging and image overlay navigation surgery in patients with breast cancer. World J Surg 2011;35:154-8. https://doi.org/10.1007/s00268-010-0811-y
  85. Van der Vorst JR, Schaafsma BE, Verbeek FP, et al. Randomized comparison of near-infrared fluorescence imaging using indocyanine green and 99(m) technetium with or without patent blue for the sentinel lymph node procedure in breast cancer patients. Ann Surg Oncol 2012;19:4104-11. https://doi.org/10.1245/s10434-012-2466-4
  86. Schaafsma BE, Verbeek FP, Rietbergen DD, et al. Clinical trial of combined radio- and fluorescence-guided sentinel lymph node biopsy in breast cancer. Br J Surg 2013;100:1037-44. https://doi.org/10.1002/bjs.9159
  87. Tong M, Guo W, Gao W. Use of fluorescence imaging in combination with patent blue dye versus patent blue dye alone in sentinel lymph node biopsy in breast cancer. J Breast Cancer 2014;17:250-5. https://doi.org/10.4048/jbc.2014.17.3.250
  88. Toh U, Iwakuma N, Mishima M, Okabe M, Nakagawa S, Akagi Y. Navigation surgery for intraoperative sentinel lymph node detection using Indocyanine green (ICG) fluorescence real-time imaging in breast cancer. Breast Cancer Res Treat 2015;153:337-44. https://doi.org/10.1007/s10549-015-3542-9
  89. Liu J, Huang L, Wang N, Chen P. Indocyanine green detects sentinel lymph nodes in early breast cancer. J Int Med Res 2017;45:514-24. https://doi.org/10.1177/0300060516687149
  90. Papathemelis T, Jablonski E, Scharl A, et al. Sentinel lymph node biopsy in breast cancer patients by means of indocyanine green using the Karl Storz VITOM(R) fluorescence camera. Biomed Res Int 2018;2018:6251468.
  91. Yamamoto M, Sasaguri S, Sato T. Assessing intraoperative blood flow in cardiovascular surgery. Surg Today 2011;41:1467-74. https://doi.org/10.1007/s00595-010-4553-0
  92. Marshall MV, Rasmussen JC, Tan IC, et al. Near-infrared fluorescence imaging in humans with indocyanine green: a review and update. Open Surg Oncol J 2010;2:12-25. https://doi.org/10.2174/1876504101002020012
  93. Lin MW, Chen JS. Image-guided techniques for localizing pulmonary nodules in thoracoscopic surgery. J Thorac Dis 2016;8(Suppl 9):S749-55. https://doi.org/10.21037/jtd.2016.09.71
  94. Owens SL. Indocyanine green angiography. Br J Ophthalmol 1996;80:263-6. https://doi.org/10.1136/bjo.80.3.263
  95. Hackethal A, Hirschburger M, Eicker SO, Mucke T, Lindner C, Buchweitz O. Role of indocyanine green in fluorescence imaging with near-infrared light to identify sentinel lymph nodes, lymphatic vessels and pathways prior to surgery: a critical evaluation of options. Geburtshilfe Frauenheilkd 2018;78:54-62. https://doi.org/10.1055/s-0043-123937
  96. Hong G, Lee JC, Robinson JT, et al. Multifunctional in vivo vascular imaging using near-infrared II fluorescence. Nat Med 2012;18:1841-6. https://doi.org/10.1038/nm.2995
  97. Haque A, Faizi MS, Rather JA, Khan MS. Next generation NIR fluorophores for tumor imaging and fluorescenceguided surgery: a review. Bioorg Med Chem 2017;25:2017-34. https://doi.org/10.1016/j.bmc.2017.02.061
  98. Ujiie H, Effat A, Yasufuku K. Image-guided thoracic surgery in the hybrid operation room. J Vis Surg 2017;3:148. https://doi.org/10.21037/jovs.2017.09.07
  99. Tempany CM, Jayender J, Kapur T, et al. Multimodal imaging for improved diagnosis and treatment of cancers. Cancer 2015;121:817-27. https://doi.org/10.1002/cncr.29012

Cited by

  1. ZW800‐PEG: A Renal Clearable Zwitterionic Near‐Infrared Fluorophore for Potential Clinical Translation vol.133, pp.25, 2019, https://doi.org/10.1002/ange.202102640
  2. ZW800‐PEG: A Renal Clearable Zwitterionic Near‐Infrared Fluorophore for Potential Clinical Translation vol.60, pp.25, 2019, https://doi.org/10.1002/anie.202102640
  3. Evolving from Laboratory Toys towards Life-Savers: Small-Scale Magnetic Robotic Systems with Medical Imaging Modalities vol.12, pp.11, 2019, https://doi.org/10.3390/mi12111310