Image-guided tumor resection using real-time near-infrared fluorescence in a syngeneic rat model of primary breast cancer

Breast Cancer Research and Treatment

Volumn 128, Issue 3, 2011, Pages 679-689

  Mieog, J Sven D ^a   Hutteman, Merlijn ^a   Van Der Vorst, Joost R ^a   Kuppen, Peter J K ^a   Que, Ivo ^a   Dijkstra, Jouke ^a   Kaijzel, Eric L ^a   Prins, Frans ^a   Löwik, Clemens W G M ^a   Smit, Vincent T H B M ^a   Van De Velde, Cornelis J H ^a   Vahrmeijer, Alexander L ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Breast conserving surgery; Cathepsin; Image guided surgery; Incomplete tumor resection; Near infrared fluorescence imaging

Indexed keywords

ACCURACY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST SURGERY; CAMERA; CANCER CELL; CANCER SIZE; CANCER SURGERY; CELL COUNT; CELL DENSITY; COMPUTER ASSISTED SURGERY; CONTROLLED STUDY; FLUORESCENCE IMAGING; HISTOPATHOLOGY; IMAGE GUIDED TUMOR RESECTION; MINIMAL RESIDUAL DISEASE; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; RAT; REAL TIME NEAR INFRARED FLUORESCENCE; STROMA; SURGICAL TECHNIQUE;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FEMALE; MICROSCOPY, FLUORESCENCE; RATS; SURGERY, COMPUTER-ASSISTED; TRANSPLANTATION, ISOGENEIC; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79960848143     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-010-1130-6     Document Type: Article

References (47)

1. KT Mai HM Yazdi PA Isotalo 2000 Resection margin status in lumpectomy specimens of infiltrating lobular carcinoma Breast Cancer Res Treat 60 29 33 10845806 10.1023/A:1006359308505 1:STN:280:DC%2BD3cvpt1GqtQ%3D%3D (Pubitemid 30307462)
2. AB Chagpar RC Martin LJ Hagendoorn C Chao KM McMasters 2004 Lumpectomy margins are affected by tumor size and histologic subtype but not by biopsy technique Am J Surg 188 399 402 15474434 10.1016/j.amjsurg.2004.06.020 (Pubitemid 39330544)
3. MC Smitt K Horst 2007 Association of clinical and pathologic variables with lumpectomy surgical margin status after preoperative diagnosis or excisional biopsy of invasive breast cancer Ann Surg Oncol 14 1040 1044 17203329 10.1245/s10434-006-9308-1
4. M Rizzo R Iyengar SG Gabram, et al. 2010 The effects of additional tumor cavity sampling at the time of breast-conserving surgery on final margin status, volume of resection, and pathologist workload Ann Surg Oncol 17 228 234 19636625 10.1245/s10434-009-0643-x
5. JC Hewes A Imkampe A Haji T Bates 2009 Importance of routine cavity sampling in breast conservation surgery Br J Surg 96 47 53 19108003 10.1002/bjs.6435 1:STN:280:DC%2BD1M%2FlslWisw%3D%3D
6. M Clarke R Collins S Darby, et al. 2005 Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: an overview of the randomised trials Lancet 366 2087 2106 16360786 1:STN:280:DC%2BD2MnnsVSitA%3D%3D (Pubitemid 41797643)
7. Nyirenda N, Farkas DL, Ramanujan VK. (2010) Preclinical evaluation of nuclear morphometry and tissue topology for breast carcinoma detection and margin assessment. Breast Cancer Res Treat
8. H Stepp T Beck T Pongratz, et al. 2007 ALA and malignant glioma: fluorescence-guided resection and photodynamic treatment J Environ Pathol Toxicol Oncol 26 157 164 17725542 1:CAS:528:DC%2BD2sXhtVWhsb3J (Pubitemid 47295558)
9. T Ishizawa N Fukushima J Shibahara, et al. 2009 Real-time identification of liver cancers by using indocyanine green fluorescent imaging Cancer 115 2491 2504 19326450 10.1002/cncr.24291
10. NQ Nguyen AV Biankin RW Leong, et al. 2009 Real time intraoperative confocal laser microscopy-guided surgery Ann Surg 249 735 737 19387332 10.1097/SLA.0b013e3181a38f11
11. JV Frangioni 2008 New technologies for human cancer imaging J Clin Oncol 26 4012 4021 18711192 10.1200/JCO.2007.14.3065
12. MM Mohamed BF Sloane 2006 Cysteine cathepsins: multifunctional enzymes in cancer Nat Rev Cancer 6 764 775 16990854 10.1038/nrc1949 1:CAS:528: DC%2BD28XpvVCmu7Y%3D (Pubitemid 44450465)
13. V Gocheva W Zeng D Ke, et al. 2006 Distinct roles for cysteine cathepsin genes in multistage tumorigenesis Genes Dev 20 543 556 16481467 10.1101/gad.1407406 1:CAS:528:DC%2BD28Xit1Kmtbw%3D (Pubitemid 43345321)
14. BS Parker DR Ciocca BN Bidwell, et al. 2008 Primary tumour expression of the cysteine cathepsin inhibitor Stefin A inhibits distant metastasis in breast cancer J Pathol 214 337 346 17985332 10.1002/path.2265 1:CAS:528: DC%2BD1cXivVSgt7k%3D (Pubitemid 351212389)
15. N Harbeck U Alt U Berger, et al. 2001 Prognostic impact of proteolytic factors (urokinase-type plasminogen activator, plasminogen activator inhibitor 1, and cathepsins B, D, and L) in primary breast cancer reflects effects of adjuvant systemic therapy Clin Cancer Res 7 2757 2764 11555589 1:CAS:528:DC%2BD3MXnsFSit7k%3D (Pubitemid 32911381)
16. TT Lah M Kokalj-Kunovar B Strukelj, et al. 1992 Stefins and lysosomal cathepsins B, L, and D in human breast carcinoma Int J Cancer 50 36 44 1728611 10.1002/ijc.2910500109 1:STN:280:DyaK38%2FpvVajtQ%3D%3D
17. TT Lah J Kos A Blejec, et al. 1997 The expression of lysosomal proteinases and their inhibitors in breast cancer: possible relationship to prognosis of the disease Pathol Oncol Res 3 89 99 11173633 10.1007/BF02907801
18. JA Foekens J Kos HA Peters, et al. 1998 Prognostic significance of cathepsins B and L in primary human breast cancer J Clin Oncol 16 1013 1021 9508185 1:CAS:528:DyaK1cXitVKisbk%3D (Pubitemid 28108735)
19. R Weissleder CH Tung U Mahmood A Bogdanov Jr 1999 In vivo imaging of tumors with protease-activated near-infrared fluorescent probes Nat Biotechnol 17 375 378 10207887 10.1038/7933 1:CAS:528:DyaK1MXitl2htb0%3D (Pubitemid 29166041)
20. DG Kirsch DM Dinulescu JB Miller, et al. 2007 A spatially and temporally restricted mouse model of soft tissue sarcoma Nat Med 13 992 997 17676052 10.1038/nm1602 1:CAS:528:DC%2BD2sXos1CjsLc%3D (Pubitemid 47222037)
21. C Bremer CH Tung A Bogdanov Jr R Weissleder 2002 Imaging of differential protease expression in breast cancers for detection of aggressive tumor phenotypes Radiology 222 814 818 11867806 10.1148/radiol.2223010812 (Pubitemid 34218157)
22. J von Burstin S Eser B Seidler, et al. 2008 Highly sensitive detection of early-stage pancreatic cancer by multimodal near-infrared molecular imaging in living mice Int J Cancer 123 2138 2147 10.1002/ijc.23780
23. RA Sheth R Upadhyay L Stangenberg R Sheth R Weissleder U Mahmood 2009 Improved detection of ovarian cancer metastases by intraoperative quantitative fluorescence protease imaging in a pre-clinical model Gynecol Oncol 112 616 622 19135233 10.1016/j.ygyno.2008.11.018 1:CAS:528:DC%2BD1MXisVOhsrs%3D
24. H Alencar MA Funovics J Figueiredo H Sawaya R Weissleder U Mahmood 2007 Colonic adenocarcinomas: near-infrared microcatheter imaging of smart probes for early detection-study in mice Radiology 244 232 238 17507718 10.1148/radiol.2441052114 (Pubitemid 46981978)
25. AA Bogdanov Jr CP Lin M Simonova L Matuszewski R Weissleder 2002 Cellular activation of the self-quenched fluorescent reporter probe in tumor microenvironment Neoplasia 4 228 236 11988842 10.1038/sj.neo.7900238 1:CAS:528:DC%2BD38XksFGnu7o%3D (Pubitemid 34525254)
26. MJ Niedre RH de Kleine E Aikawa DG Kirsch R Weissleder V Ntziachristos 2008 Early photon tomography allows fluorescence detection of lung carcinomas and disease progression in mice in vivo Proc Natl Acad Sci USA 105 19126 19131 19015534 10.1073/pnas.0804798105 1:CAS:528:DC%2BD1cXhsFamu77J
27. V Ntziachristos CH Tung C Bremer R Weissleder 2002 Fluorescence molecular tomography resolves protease activity in vivo Nat Med 8 757 760 12091907 10.1038/nm729 1:CAS:528:DC%2BD38XkvFeht7w%3D (Pubitemid 34778731)
28. C Bremer V Ntziachristos B Weitkamp G Theilmeier W Heindel R Weissleder 2005 Optical imaging of spontaneous breast tumors using protease sensing 'smart' optical probes Invest Radiol 40 321 327 15905717 10.1097/01.rli.0000163797. 23172.90 1:CAS:528:DC%2BD2MXktlKlurc%3D (Pubitemid 40734559)
29. E Gounaris CH Tung C Restaino, et al. 2008 Live imaging of cysteine-cathepsin activity reveals dynamics of focal inflammation, angiogenesis, and polyp growth PLoS One 3 e2916 18698347 10.1371/journal.pone. 0002916
30. J Grimm DG Kirsch SD Windsor, et al. 2005 Use of gene expression profiling to direct in vivo molecular imaging of lung cancer Proc Natl Acad Sci USA 102 14404 14409 16183744 10.1073/pnas.0503920102 1:CAS:528: DC%2BD2MXhtFCgsr%2FE (Pubitemid 41429710)
31. QT Nguyen ES Olson TA Aguilera, et al. 2010 Surgery with molecular fluorescence imaging using activatable cell-penetrating peptides decreases residual cancer and improves survival Proc Natl Acad Sci USA 107 4317 4322 20160097 10.1073/pnas.0910261107 1:CAS:528:DC%2BC3cXjsFWiur0%3D
32. JH van Dierendonck R Keijzer CJ Cornelisse CJ van de Velde 1991 Surgically induced cytokinetic responses in experimental rat mammary tumor models Cancer 68 759 767 1855176 10.1002/1097-0142(19910815)68:4<759::AID- CNCR2820680417>3.0.CO;2-2
33. JH Wijsman CJ Cornelisse R Keijzer CJ van de Velde JH van Dierendonck 1991 A prolactin-dependent, metastasising rat mammary carcinoma as a model for endocrine-related tumour dormancy Br J Cancer 64 463 468 1911185 10.1038/bjc.1991.332 1:CAS:528:DyaK3MXmslKku78%3D
34. T Sorlie R Tibshirani J Parker, et al. 2003 Repeated observation of breast tumor subtypes in independent gene expression data sets Proc Natl Acad Sci USA 100 8418 8423 12829800 10.1073/pnas.0932692100 1:CAS:528: DC%2BD3sXlsFGntLk%3D (Pubitemid 36842560)
35. H Sihto J Lundin T Lehtimaki, et al. 2008 Molecular subtypes of breast cancers detected in mammography screening and outside of screening Clin Cancer Res 14 4103 4110 18593987 10.1158/1078-0432.CCR-07-5003 1:CAS:528: DC%2BD1cXnvFylu74%3D
36. JS Mieog AL Vahrmeijer M Hutteman, et al. 2010 Novel intraoperative near-infrared fluorescence camera system for optical image-guided cancer surgery Mol Imaging 9 223 231 20643025
37. M Keramidas V Josserand CA Righini C Wenk C Faure JL Coll 2010 Intraoperative near-infrared image-guided surgery for peritoneal carcinomatosis in a preclinical experimental model Br J Surg 97 737 743 20309948 10.1002/bjs.6986 1:STN:280:DC%2BC3c3mt1KltA%3D%3D
38. Mansfield JR, Hoyt C, Levenson RM (2008) Visualization of microscopy-based spectral imaging data from multi-label tissue sections. Curr Protoc Mol Biol, Chapter 14:Unit
39. Rasband WS, Image J (2009) US National Institutes of Health, Bethesda. http://rsb.info.nih.gov/ij/
40. P Juni DG Altman M Egger 2001 Systematic reviews in health care: assessing the quality of controlled clinical trials BMJ 323 42 46 11440947 10.1136/bmj.323.7303.42 1:STN:280:DC%2BD3Mzos1OltQ%3D%3D (Pubitemid 32682008)
41. D Kuester H Lippert A Roessner S Krueger 2008 The cathepsin family and their role in colorectal cancer Pathol Res Pract 204 491 500 18573619 10.1016/j.prp.2008.04.010
42. V Gocheva JA Joyce 2007 Cysteine cathepsins and the cutting edge of cancer invasion Cell Cycle 6 60 64 17245112 10.4161/cc.6.1.3669 1:CAS:528:DC%2BD2sXnvFygsbc%3D (Pubitemid 46173882)
43. SL Troyan V Kianzad SL Gibbs-Strauss, et al. 2009 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 2943 2952 19582506 10.1245/s10434-009-0594-2
44. C Hirche D Murawa Z Mohr S Kneif M Hunerbein 2010 ICG fluorescence-guided sentinel node biopsy for axillary nodal staging in breast cancer Breast Cancer Res Treat 121 373 378 20140704 10.1007/s10549-010-0760-z
45. T Kitai T Inomoto M Miwa T Shikayama 2005 Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer Breast Cancer 12 211 215 16110291 10.2325/jbcs.12.211
46. S Bloom M Morrow 2010 A clinical oncologic perspective on breast magnetic resonance imaging Magn Reson Imaging Clin N Am 18 277 294 20494312 10.1016/j.mric.2010.02.007 ix
47. AM De Grand SJ Lomnes DS Lee, et al. 2006 Tissue-like phantoms for near-infrared fluorescence imaging system assessment and the training of surgeons J Biomed Opt 11 014007 16526884 10.1117/1.2170579 (Pubitemid 44355106)