The status of contemporary image-guided modalities in oncologic surgery

Annals of Surgery

Volumn 261, Issue 1, 2015, Pages 46-55

  Rosenthal, Eben L ^a,b   Warram, Jason M ^a   Bland, Kirby I ^a   Zinn, Kurt R ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Cancer; Fluorescence; Image guided surgery; Molecular imaging; Oncologic surgery; Optical imaging

Indexed keywords

CONTRAST MEDIUM; INDOCYANINE GREEN; AMINOLEVULINIC ACID; COLORING AGENT; FLUORESCENT DYE; PHOTOSENSITIZING AGENT;

AUTOFLUORESCENCE GUIDED SURGERY; AUTOFLUORESCENCE IMAGING; BRAIN SURGERY; BRAIN TUMOR; CANCER PATIENT; CANCER SURGERY; CANCER SURVIVAL; CLINICAL TRIAL (TOPIC); ECHOGRAPHY; FLUORESCENCE IMAGING; HUMAN; INDOCYANINE GREEN ANGIOGRAPHY; INTRAOPERATIVE PERIOD; MOLECULAR IMAGING; MORBIDITY; NEAR INFRARED FLUORESCENCE; NUCLEAR MAGNETIC RESONANCE IMAGING; OVERALL SURVIVAL; PRIORITY JOURNAL; REVIEW; SURGEON; SURGICAL TECHNIQUE; TUMOR INVASION; BRAIN NEOPLASMS; COMPUTER ASSISTED SURGERY; DIAGNOSTIC IMAGING; NEOPLASMS; PATHOLOGY;

AMINOLEVULINIC ACID; BRAIN NEOPLASMS; COLORING AGENTS; DIAGNOSTIC IMAGING; FLUORESCENT DYES; HUMANS; INDOCYANINE GREEN; INTRAOPERATIVE PERIOD; NEOPLASMS; OPTICAL IMAGING; PHOTOSENSITIZING AGENTS; SURGERY, COMPUTER-ASSISTED;

EID: 84930397767     PISSN: 00034932     EISSN: 15281140     Source Type: Journal    
DOI: 10.1097/SLA.0000000000000622     Document Type: Review

References (98)

1. Woolgar JA, Triantafyllou A. A histopathological appraisal of surgical margins in oral and oropharyngeal cancer resection specimens. Oral Oncol. 2005; 41: 1034-1043.
2. McMahon J, O'Brien CJ, Pathak I, et al. Influence of condition of surgical margins on local recurrence and disease-specific survival in oral and oropharyngeal cancer. Br J Oral Maxillofac Surg. 2003; 41: 224-231.
3. Ravasz LA, Slootweg PJ, Hordijk GJ, et al. The status of the resection margin as a prognostic factor in the treatment of head and neck carcinoma. J Craniomaxillofac Surg. 1991; 19: 314-318.
4. Atkins J, Al Mushawah F, Appleton CM, et al. Positive margin rates following breast-conserving surgery for stage I-III breast cancer: palpable versus nonpalpable tumors. J Surg Res. 2012; 177: 109-115.
5. Iczkowski KA, Lucia MS. Frequency of positive surgical margin at prostatectomy and its effect on patient outcome. Prostate Cancer. 2011; 2011: 673021.
6. Goto Y, Kodaira T, Furutani K, et al. Clinical outcome and patterns of recurrence of head and neck squamous cell carcinoma with a limited field of postoperative radiotherapy. Jpn J Clin Oncol. 2013; 43: 719-725.
7. Haloua MH, Krekel NM, Winters HA, et al. A systematic review of oncoplastic breast-conserving surgery: current weaknesses and future prospects. Ann Surg. 2013; 257: 609-620.
8. Abraham SC, Fox K, Fraker D, et al. Sampling of grossly benign breast reexcisions: a multidisciplinary approach to assessing adequacy. Am J Surg Pathol. 1999; 23: 316-322.
9. Swindle P, Eastham JA, Ohori M, et al. Do margins matter? The prognostic significance of positive surgical margins in radical prostatectomy specimens. J Urol. 2008; 179: S47-S51.
10. Moliterno JA, Patel TR, Piepmeier JM. Neurosurgical approach. Cancer J. 2012; 18: 20-25.
11. Senft C, Bink A, Franz K, et al. Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol. 2011; 12: 997-1003.
12. Senft C, Schoenes B, Gasser T, et al. Feasibility of intraoperative MRI guidance for craniotomy and tumor resection in the semisitting position. J Neurosurg Anesthesiol. 2011; 23: 241-246.
13. Wong JM, Panchmatia JR, Ziewacz JE, et al. Patterns in neurosurgical adverse events: intracranial neoplasm surgery. Neurosurg Focus. 2012; 33: E16.
14. Claus EB, Horlacher A, Hsu L, et al. Survival rates in patients with lowgrade glioma after intraoperative magnetic resonance image guidance. Cancer. 2005; 103: 1227-1233.
15. Kuhnt D, Becker A, Ganslandt O, et al. Correlation of the extent of tumor volume resection and patient survival in surgery of glioblastoma multiforme with high-field intraoperative MRI guidance. Neuro Oncol. 2011; 13: 1339-1348.
16. Kuhnt D, Ganslandt O, Schlaffer SM, et al. Quantification of glioma removal by intraoperative high-field magnetic resonance imaging: an update. Neurosurgery. 2011; 69: 852-862; discussion 862-863.
17. Kubben PL, ter Meulen KJ, Schijns OE, et al. Intraoperative MRI-guided resection of glioblastoma multiforme: a systematic review. Lancet Oncol. 2011; 12: 1062-1070.
18. Hall WA, Kowalik K, Liu H, et al. Costs and benefits of intraoperative MRguided brain tumor resection. Acta Neurochir Suppl. 2003; 85: 137-142.
19. Lencioni R, Cioni D, Bartolozzi C. Tissue harmonic and contrast-specific imaging: back to gray scale in ultrasound. Eur Radiol. 2002; 12: 151-165.
20. Minami Y, Kudo M. Review of dynamic contrast-enhanced ultrasound guidance in ablation therapy for hepatocellular carcinoma. World J Gastroenterol. 2011; 17: 4952-4959.
21. Solbiati L, TonoliniM, Cova L, et al. The role of contrast-enhanced ultrasound in the detection of focal liver lesions. European Radiol. 2001; 11(suppl 3): E15-E26.
22. Aoki S, Hattori R, Yamamoto T, et al. Contrast-enhanced ultrasound using a time-intensity curve for the diagnosis of renal cell carcinoma. BJU Int. 2011; 108: 349-354.
23. Masuzaki R, Shiina S, Tateishi R, et al. Utility of contrast-enhanced ultrasonography with Sonazoid in radiofrequency ablation for hepatocellular carcinoma. J Gastroenterol Hepatol. 2011; 26: 759-764.
24. Selbekk T, Bang J, Unsgaard G. Strain processing of intraoperative ultrasound images of brain tumours: initial results. Ultrasound Med Biol. 2005; 31: 45-51.
25. Selbekk T, Brekken R, Indergaard M, et al. Comparison of contrast in brightness mode and strain ultrasonography of glial brain tumours. BMC Med Imaging. 2012; 12: 11.
26. Moiyadi A, Shetty P. Objective assessment of utility of intraoperative ultrasound in resection of central nervous system tumors: a cost-effective tool for intraoperative navigation in neurosurgery. J Neurosci Rural Pract. 2011; 2: 4-11.
27. Au GH, Shih WY, Shih WH, et al. Assessing breast cancer margins ex vivo using aqueous quantum-dot-molecular probes. Int J Surg Oncol. 2012; 2012: 861257.
28. RuidiazME, Blair SL, Kummel AC, et al. Computerized decision support system for intraoperative analysis of margin status in breast conservation therapy. ISRN Surg. 2012; 2012: 546721.
29. Jung W, Kang E, Kim SM, et al. Factors associated with re-excision after breast-conserving surgery for early-stage breast cancer. J Breast Cancer. 2012; 15: 412-419.
30. Yu CC, Chiang KC, Kuo WL, et al. Low re-excision rate for positive margins in patients treated with ultrasound-guided breast-conserving surgery. Breast. 2013; 22: 698-702.
31. Dunne C, Burke JP, MorrowM, et al. Effect of margin status on local recurrence after breast conservation and radiation therapy for ductal carcinoma in situ. J Clin Oncol. 2009; 27: 1615-1620.
32. Pleijhuis RG, Graafland M, de Vries J, et al. Obtaining adequate surgical margins in breast-conserving therapy for patients with early-stage breast cancer: currentmodalities and future directions. Ann Surg Oncol. 2009; 16: 2717-2730.
33. Krekel NM, Haloua MH, Lopes Cardozo AM, et al. Intraoperative ultrasound guidance for palpable breast cancer excision (COBALT trial): a multicentre, randomised controlled trial. Lancet Oncol. 2013; 14: 48-54.
34. DaCosta RS, Wilson BC, Marcon NE. Fluorescence and spectral imaging. Scientific World J. 2007; 7: 2046-2071.
35. Herrero LA, Weusten BL, Bergman JJ. Autofluorescence and narrow band imaging in Barrett's esophagus. Gastroenterol Clin North Am. 2010; 39: 747-758.
36. Ohtani K, Lee AM, Lam S. Frontiers in bronchoscopic imaging. Respirology. 2012; 17: 261-269.
37. Poh CF, Durham JS, Brasher PM, et al. Canadian Optically-guided approach for Oral Lesions Surgical (COOLS) trial: study protocol for a randomized controlled trial. BMC Cancer. 2011; 11: 462.
38. Pavlova I, Williams M, El-Naggar A, et al. Understanding the biological basis of autofluorescence imaging for oral cancer detection: high-resolution fluorescence microscopy in viable tissue. Clin Cancer Res. 2008; 14: 2396-2404.
39. Wilke LG, Brown JQ, Bydlon TM, et al. Rapid noninvasive optical imaging of tissue composition in breast tumor margins. Am J Surg. 2009; 198: 566-574.
40. Poh CF, Zhang L, Anderson DW, et al. Fluorescence visualization detection of field alterations in tumor margins of oral cancer patients. Clin Cancer Res. 2006; 12: 6716-6722.
41. Sweeny L, Dean NR, Magnuson JS, et al. Assessment of tissue autofluorescence and reflectance for oral cavity cancer screening. Otolaryngol Head Neck Surg. 2011; 145: 956-960.
42. Widhalm G, Kiesel B, Woehrer A, et al. 5-aminolevulinic acid induced fluorescence is a powerful intraoperative marker for precise histopathological grading of gliomas with non-significant contrast-enhancement. PLoS One. 2013; 8: e76988.
43. Stummer W, Pichlmeier U, Meinel T, et al. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol. 2006; 7: 392-401.
44. Stummer W, Tonn JC, Mehdorn HM, et al. Counterbalancing risks and gains from extended resections in malignant glioma surgery: a supplemental analysis from the randomized 5-aminolevulinic acid glioma resection study. Clinical article. J Neurosurg. 2011; 114: 613-623.
45. Roberts DW, Valdes PA, Harris BT, et al. Glioblastoma multiforme treatment with clinical trials for surgical resection (aminolevulinic acid). Neurosurg Clin N Am. 2012; 23: 371-377.
46. Roberts DW, Valdes PA, Harris BT, et al. Coregistered fluorescenceenhanced tumor resection of malignant glioma: relationships between deltaaminolevulinic acid-induced protoporphyrin IX fluorescence, magnetic resonance imaging enhancement, and neuropathological parameters. Clinical article. J Neurosurg. 2011; 114: 595-603.
47. Valdes PA, Kim A, Brantsch M, et al.Delta-aminolevulinic acid-induced protoporphyrin IX concentration correlates with histopathologic markers of malignancy in human gliomas: the need for quantitative fluorescence-guided resection to identify regions of increasing malignancy. Neuro Oncol. 2011; 13: 846-856.
48. Boudreaux BA, Rosenthal EL, Magnuson JS, et al. Robot-assisted surgery for upper aerodigestive tract neoplasms. Arch Otolaryngol Head Neck Surg. 2009; 135: 397-401.
49. Sohn W, Lee HJ, Ahlering TE. Robotic surgery: review of prostate and bladder cancer. Cancer J. 2013; 19: 133-139.
50. Schaafsma BE, Mieog JS, Hutteman M, et al. The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery. J Surg Oncol. 2011; 104: 323-332.
51. Schaafsma BE, van der Vorst JR, Gaarenstroom KN, et al. Randomized comparison of near-infrared fluorescence lymphatic tracers for sentinel lymph node mapping of cervical cancer. Gynecol Oncology. 2012; 127: 126-130.
52. Garcia-Allende PB, Glatz J, Koch M, et al. Enriching the interventional vision of cancer with fluorescent and optoacoustic imaging.JNuclMed. 2013; 54: 664-667.
53. Harlaar NJ, Kelder W, Sarantopoulos A, et al. Real-time near infrared fluorescence (NIRF) intra-operative imaging in ovarian cancer using an alpha(v)beta(3-)integrin targeted agent. Gynecol Oncol. 2013; 128: 590-595.
54. Speich R, Saesseli B, Hoffmann U, et al. Anaphylactoid reactions after indocyanine-green administration. Ann Intern Med. 1988; 109: 345-346.
55. Sevick-Muraca EM. Translation of near-infrared fluorescence imaging technologies: emerging clinical applications. Annu Rev Med. 2012; 63: 217-231.
56. Xu MH, Wang LHV. Photoacoustic imaging in biomedicine. Rev Sci Instrum. 2006; 77: 041101.
57. Hoelen CG, de Mul FF, Pongers R, et al. Three-dimensional photoacoustic imaging of blood vessels in tissue. Opt Lett. 1998; 23: 648-650.
58. Zhang HF, Maslov K, Stoica G, et al. Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging. Nat Biotechnol. 2006; 24: 848-851.
59. Washington CW, Zipfel GJ, Chicoine MR, et al. Comparing indocyanine green videoangiography to the gold standard of intraoperative digital subtraction angiography used in aneurysm surgery. J Neurosurg. 2013; 118: 420-427.
60. Wang HD, Singh DP. The use of indocyanine green angiography to prevent wound complications in ventral hernia repair with open components separation technique. Hernia. 2013; 17: 397-402.
61. Phillips BT, Lanier ST, Conkling N, et al. Intraoperative perfusion techniques can accurately predict mastectomy skin flap necrosis in breast reconstruction: results of a prospective trial. Plast Reconstr Surg. 2012; 129: 778e-788e.
62. van der Vorst JR, Schaafsma BE, Hutteman M, et al. Near-infrared fluorescence-guided resection of colorectal liver metastases. Cancer. 2013; 119: 3411-3418.
63. Madajewski B, Judy BF, Mouchli A, et al. Intraoperative near-infrared imaging of surgical wounds after tumor resections can detect residual disease. Clin Cancer Res. 2012; 18: 5741-5751.
64. Satou S, Ishizawa T, Masuda K, et al. Indocyanine green fluorescent imaging for detecting extrahepatic metastasis of hepatocellular carcinoma. J Gastroenterol. 2013; 48: 1136-1143.
65. Ishizawa T, Fukushima N, Shibahara J, et al. Real-time identification of liver cancers by using indocyanine green fluorescent imaging. Cancer. 2009; 115: 2491-2504.
66. Ishizawa T, Tamura S, Masuda K, et al. Intraoperative fluorescent cholangiography using indocyanine green: a biliary road map for safe surgery. J Am Coll of Surg. 2009; 208: e1-e4.
67. Peloso A, Franchi E, Canepa MC, et al. Combined use of intraoperative ultrasound and indocyanine green fluorescence imaging to detect liver metastases from colorectal cancer. HPB (Oxford). 2013; 15: 928-934.
68. Angell JE, Khemees TA, Abaza R. Optimization of near-infrared fluorescence tumor localization during robotic partial nephrectomy.JUrol. 2013; 190: 1668-1673.
69. Manny T, Krane LS, Hemal AK. Indocyanine green cannot predictmalignancy in partial nephrectomy: histopathologic correlation with fluorescence pattern in 100 patients. J Endourol. 2013; 27: 918-921.
70. Krane LS, Manny TB, Hemal AK. Is near infrared fluorescence imaging using indocyanine green dye useful in robotic partial nephrectomy: a prospective comparative study of 94 patients. Urology. 2012; 80: 110-116.
71. Intes X, Ripoll J, Chen Y, et al. In vivo continuous-wave optical breast imaging enhanced with indocyanine green. Med Phys. 2003; 30: 1039-1047.
72. Ntziachristos V, Yodh AG, Schnall M, et al. Concurrent MRI and diffuse optical tomography of breast after indocyanine green enhancement. Proc Natl Acad Sci U S A. 2000; 97: 2767-2772.
73. Mataki N, Nagao S, Kawaguchi A, et al. Clinical usefulness of a new infrared videoendoscope system for diagnosis of early stage gastric cancer. Gastrointest Endosc. 2003; 57: 336-342.
74. Iseki K, Tatsuta M, Iishi H, et al. Effectiveness of the near-infrared electronic endoscope for diagnosis of the depth of involvement of gastric cancers. Gastrointest Endosc. 2000; 52: 755-762.
75. Keereweer S, Sterenborg HJ, Kerrebijn JD, et al. Image-guided surgery in head and neck cancer: current practice and future directions of optical imaging. Head Neck. 2012; 34: 120-126.
76. Bailey KM, Wojtkowiak JW, Hashim AI, et al. Targeting the metabolic microenvironment of tumors. Adv Pharmacol. 2012; 65: 63-107.
77. Zhang X, Lin Y, Gillies RJ. Tumor pH and its measurement. J Nucl Med. 2010; 51: 1167-1170.
78. Gindy ME, Prud'homme RK. Multifunctional nanoparticles for imaging, delivery and targeting in cancer therapy. Expert Opin Drug Deliv. 2009; 6: 865-878.
79. Jiang S, Gnanasammandhan MK, Zhang Y. Optical imaging-guided cancer therapy with fluorescent nanoparticles. J R Soc Interface. 2010; 7: 3-18.
80. Adams KE, Ke S, Kwon S, et al. Comparison of visible and near-infrared wavelength-excitable fluorescent dyes for molecular imaging of cancer. J Biomed Opt. 2007; 12: 024017.
81. Kramer-Marek G, Longmire MR, Choyke PL, et al. Recent advances in optical cancer imaging of EGF receptors. Curr Med Chem. 2012; 19: 4759-4766.
82. Andrades P, Bohannon IA, Baranano CF, et al. Indications and outcomes of double free flaps in head and neck reconstruction. Microsurgery. 2009; 29: 171-177.
83. Newman JR, Gleysteen JP, Baranano CF, et al. Stereomicroscopic fluorescence imaging of head and neck cancer xenografts targeting CD147. Cancer Biol Ther. 2008; 7: 1063-1070.
84. Shah N, Zhai G, Knowles JA, et al. F-FDG PET/CT imaging detects therapy efficacy of anti-EMMPRIN antibody and gemcitabine in orthotopic pancreatic tumor xenografts. Mol Imaging Biol. 2012; 14: 237-244.
85. Withrow KP, Newman JR, Skipper JB, et al. Assessment of bevacizumab conjugated to Cy5.5 for detection of head and neck cancer xenografts. Technol Cancer Res Treat. 2008; 7: 61-66.
86. Weissleder R. Molecular imaging in cancer. Science. 2006; 312: 1168-1171.
87. Agdeppa ED, Spilker ME. A review of imaging agent development. AAPS J. 2009; 11: 286-299.
88. van Dam GM, Themelis G, Crane LM, et al. Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-alpha targeting: first in-human results. Nat Med. 2011; 17: 1315-1319.
89. Eward WC, Mito JK, Eward CA, et al. A novel imaging system permits realtime in vivo tumor bed assessment after resection of naturally occurring sarcomas in dogs. Clin Orthop Relat Res. 2013; 471: 834-842.
90. Savariar EN, Felsen CN, Nashi N, et al. Real-time in vivo molecular detection of primary tumors and metastases with ratio metric activatable cell-penetrating peptides. Cancer Res. 2013; 73: 855-864.
91. Day KE, Sweeny L, Kulbersh B, et al. Preclinical comparison of near-infraredlabeled cetuximab and panitumumab for optical imaging of head and neck squamous cell carcinoma. Mol Imaging Biol. 2013; 15: 722-729.
92. Day KE, Beck LN, Deep NL, et al. Fluorescently labeled therapeutic antibodies for detection of microscopic melanoma. Laryngoscope. 2013; 123: 2681-2689.
93. Heath CH, Deep NL, Beck LN, et al. Use of panitumumab-IRDye800 to image cutaneous head and neck cancer in mice. Otolaryngol Head Neck Surg. 2013; 148: 982-990.
94. Day KE, Beck LN, Heath CH, et al. Identification of the optimal therapeutic antibody for fluorescent imaging of cutaneous squamous cell carcinoma. Cancer Biol Ther. 2013; 14: 271-277.
95. Terwisscha van ScheltingaAG, van DamGM, NagengastWB, et al. Intraoperative near-infrared fluorescence tumor imaging with vascular endothelial growth factor and human epidermal growth factor receptor 2 targeting antibodies. J Nucl Med. 2011; 52: 1778-1785.
96. Osborne JR, Akhtar NH, Vallabhajosula S, et al. Prostate-specific membrane antigen-based imaging. Urologic Oncol. 2013; 31: 144-154.
97. Sampath L, Kwon S, Ke S, et al.Dual-labeled trastuzumab-based imaging agent for the detection of human epidermal growth factor receptor 2 overexpression in breast cancer. J Nucl Med. 2007; 48: 1501-1510.
98. Wang W, Ke S, Kwon S, et al. A new optical and nuclear dual-labeled imaging agent targeting interleukin 11 receptor alpha-chain. Bioconjug Chem. 2007; 18: 397-402.