Comparison of two threshold detection criteria methodologies for determination of probe positivity for intraoperative in situ identification of presumed abnormal 18F-FDG-avid tissue sites during radioguided oncologic surgery

BMC Cancer

Edward W Martin Jr³  Robert Lee¹  Douglas A Murrey²  Nathan C Hall²  Stephen P Povoski³  Gregg J Chapman¹ 

[1]Department of Electrical and Computer Engineering, The Ohio State University, Columbus, OH 43210, USA

[2]Division of Molecular Imaging and Nuclear Medicine, Department of Radiology, The Ohio State University Wexner Medical Center, Columbus, OH 43210, USA

[3]Division of Surgical Oncology, Department of Surgery, Arthur G. James Cancer Hospital and Richard J. Solove Research Institute and Comprehensive Cancer Center, The Ohio State University Wexner Medical Center, Columbus, OH 43210, USA

关键词: Oncologic;    Neoplasms;    Count rate;    in situ;    Gamma detection probes;    Intraoperative detection;    Radioguided surgery;    ¹⁸F-FDG-directed surgery;    Threshold;    Ratiometric;    Three-sigma;    Tumor-to-background ratio;    Target-to-background ratio;    ¹⁸F-FDG;    ¹⁸F-fluorodeoxyglucose;   

Others  :  1121086
DOI  :  10.1186/1471-2407-14-667

 received in 2014-07-07, accepted in 2014-09-10,  发布年份 2014

【 摘 要 】

Background

Intraoperative in situ identification of ¹⁸F-FDG-avid tissue sites during radioguided oncologic surgery remains a significant challenge for surgeons. The purpose of our study was to evaluate the 1.5-to-1 ratiometric threshold criteria method versus the three-sigma statistical threshold criteria method for determination of gamma detection probe positivity for intraoperative in situ identification of presumed abnormal ¹⁸F-FDG-avid tissue sites in a manner that was independent of the specific type of gamma detection probe used.

Methods

From among 52 patients undergoing appropriate in situ evaluation of presumed abnormal ¹⁸F-FDG-avid tissue sites during ¹⁸F-FDG-directed surgery using 6 available gamma detection probe systems, a total of 401 intraoperative gamma detection probe measurement sets of in situ counts per second measurements were cumulatively taken.

Results

For the 401 intraoperative gamma detection probe measurement sets, probe positivity was successfully met by the 1.5-to-1 ratiometric threshold criteria method in 150/401 instances (37.4%) and by the three-sigma statistical threshold criteria method in 259/401 instances (64.6%) (P < 0.001). Likewise, the three-sigma statistical threshold criteria method detected true positive results at target-to-background ratios much lower than the 1.5-to-1 target-to-background ratio of the 1.5-to-1 ratiometric threshold criteria method.

Conclusions

The three-sigma statistical threshold criteria method was significantly better than the 1.5-to-1 ratiometric threshold criteria method for determination of gamma detection probe positivity for intraoperative in situ detection of presumed abnormal ¹⁸F-FDG-avid tissue sites during radioguided oncologic surgery. This finding may be extremely important for reshaping the ongoing and future research and development of gamma detection probe systems that are necessary for optimizing the in situ detection of radioisotopes of higher-energy gamma photon emissions used during radioguided oncologic surgery.

【 授权许可】

   
2014 Chapman et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Povoski SP, Neff RL, Mojzisik CM, O’Malley DM, Hinkle GH, Hall NC, Murrey DA Jr, Knopp MV, Martin EW Jr: A comprehensive overview of radioguided surgery using gamma detection probe technology. World J Surg Oncol 2009, 7:11. BioMed Central Full Text
• [2]Povoski SP, Chapman GJ, Murrey DA Jr, Lee R, Martin EW Jr, Hall NC: Intraoperative detection of 18F-FDG-avid tissue sites using the increased probe counting efficiency of the K-alpha probe design and variance-based statistical analysis with the three-sigma criteria. BMC Cancer 2013, 13:98. BioMed Central Full Text
• [3]Desai D, Arnold M, Saha S, Hinkle G, Soble D, Frye J, DePalatis L, Mantil J, Satter M, Martin E: Intraoperative gamma detection of FDG distribution in colorectal cancer. Clin Positron Imaging 1999, 2:325.
• [4]Desai DC, Arnold M, Saha S, Hinkle G, Soble D, Fry J, DePalatis LR, Mantil J, Satter M, Martin EW: Correlative whole-body FDG-PET and intraoperative gamma detection of FDG distribution in colorectal cancer. Clin Positron Imaging 2000, 3:189-196.
• [5]Zervos EE, Desai DC, DePalatis LR, Soble D, Martin EW: 18F-labeled fluorodeoxyglucose positron emission tomography-guided surgery for recurrent colorectal cancer: a feasibility study. J Surg Res 2001, 97:9-13.
• [6]Essner R, Hsueh EC, Haigh PI, Glass EC, Huynh Y, Daghighian F: Application of an [(18)F]fluorodeoxyglucose-sensitive probe for the intraoperative detection of malignancy. J Surg Res 2001, 96:120-126.
• [7]Essner R, Daghighian F, Giuliano AE: Advances in FDG PET probes in surgical oncology. Cancer J 2002, 8:100-108.
• [8]Higashi T, Saga T, Ishimori T, Mamede M, Ishizu K, Fujita T, Mukai T, Sato S, Kato H, Yamaoka Y, Matsumoto K, Senda M, Konishi J: What is the most appropriate scan timing for intraoperative detection of malignancy using 18F-FDG-sensitive gamma probe? Preliminary phantom and preoperative patient study. Ann Nucl Med 2004, 18:105-114.
• [9]Yap JT, Carney JP, Hall NC, Townsend DW: Image-guided cancer therapy using PET/CT. Cancer J 2004, 10:221-233.
• [10]Barranger E, Kerrou K, Petegnief Y, David-Montefiore E, Cortez A, Daraï E: Laparoscopic resection of occult metastasis using the combination of FDG-positron emission tomography/computed tomography image fusion with intraoperative probe guidance in a woman with recurrent ovarian cancer. Gynecol Oncol 2005, 96:241-244.
• [11]Carrera D, Fernandez A, Estrada J, Martin-Comin J, Gamez C: Detection of occult malignant melanoma by 18F-FDG PET-CT and gamma probe. Rev Esp Med Nucl 2005, 24:410-413. Spanish
• [12]Franc BL, Mari C, Johnson D, Leong SP: The role of a positron- and high-energy gamma photon probe in intraoperative localization of recurrent melanoma. Clin Nucl Med 2005, 30:787-791.
• [13]Kraeber-Bodéré F, Cariou B, Curtet C, Bridji B, Rousseau C, Dravet F, Charbonnel B, Carnaille B, Le Néel JC, Mirallié E: Feasibility and benefit of fluorine 18-fluoro-2-deoxyglucose-guided surgery in the management of radioiodine-negative differentiated thyroid carcinoma metastases. Surgery 2005, 138:1176-1182.
• [14]Gulec SA, Daghighian F, Essner R: PET-probe. Evaluation of technical performance and clinical utility of a handheld high-energy gamma probe in oncologic surgery. Ann Surg Oncol 2006. Epub ahead of print
• [15]Meller B, Sommer K, Gerl J, von Hof K, Surowiec A, Richter E, Wollenberg B, Baehre M: High energy probe for detecting lymph node metastases with 18F-FDG in patients with head and neck cancer. Nuklearmedizin 2006, 45:153-159.
• [16]Nwogu C, Fischer G, Tan D, Glinianski M, Lamonica D, Demmy T: Radioguided detection of lymph node metastasis in non-small cell lung cancer. Ann Thorac Surg 2006, 82:1815-1820. discussion 1820
• [17]Curtet C, Carlier T, Mirallié E, Bodet-Milin C, Rousseau C, Barbet J, Kraeber-Bodéré F: Prospective comparison of two gamma probes for intraoperative detection of 18F-FDG: in vitro assessment and clinical evaluation in differentiated thyroid cancer patients with iodine-negative recurrence. Eur J Nucl Med Mol Imaging 2007, 34:1556-1562.
• [18]Gulec SA, Hoenie E, Hostetter R, Schwartzentruber D: PET probe-guided surgery: applications and clinical protocol. World J Surg Oncol 2007, 5:65. BioMed Central Full Text
• [19]Gulec SA: PET probe-guided surgery. J Surg Oncol 2007, 96:353-357.
• [20]Hall NC, Povoski SP, Murrey DA, Knopp MV, Martin EW: Combined approach of perioperative 18F-FDG PET/CT imaging and intraoperative 18F-FDG handheld gamma probe detection for tumor localization and verification of complete tumor resection in breast cancer. World J Surg Oncol 2007, 5:143. BioMed Central Full Text
• [21]Piert M, Burian M, Meisetschlager G, Stein HJ, Ziegler S, Nahrig J, Picchio M, Buck A, Siewert JR, Schwaiger M: Positron detection for the intraoperative localisation of cancer deposits. Eur J Nucl Med Mol Imaging 2007, 34:1534-1544.
• [22]Sarikaya I, Povoski SP, Al-Saif OH, Kocak E, Bloomston M, Marsh S, Cao Z, Murrey DA, Zhang J, Hall NC, Knopp MV, Martin EW: Combined use of preoperative 18F FDG-PET imaging and intraoperative gamma probe detection for accurate assessment of tumor recurrence in patients with colorectal cancer. World J Surg Oncol 2007, 5:80. BioMed Central Full Text
• [23]Sun D, Bloomston M, Hinkle G, Al-Saif OH, Hall NC, Povoski SP, Arnold MW, Martin EW: Radioimmunoguided surgery (RIGS), PET/CT image-guided surgery, and fluorescence image-guided surgery: past, present, and future. J Surg Oncol 2007, 96:297-308.
• [24]Agrawal A, Hall NC, Ringel MD, Povoski SP, Martin EW Jr: Combined use of perioperative TSH-stimulated 18F-FDG PET/CT imaging and gamma probe radioguided surgery to localize and verify resection of iodine scan-negative recurrent thyroid carcinoma. Laryngoscope 2008, 118:2190-2194.
• [25]Cohn DE, Hall NC, Povoski SP, Seamon LG, Farrar WB, Martin EW Jr: Novel perioperative imaging with 18F-FDG PET/CT and intraoperative 18F-FDG detection using a handheld gamma probe in recurrent ovarian cancer. Gynecol Oncol 2008, 110:152-157.
• [26]Hall NC, Povoski SP, Murrey DA, Knopp MV, Martin EW: Bringing advanced medical imaging into the operative arena could revolutionize the surgical care of cancer patients. Expert Rev Med Devices 2008, 5:663-667.
• [27]Moffatt-Bruce SD, Povoski SP, Sharif S, Hall NC, Ross P Jr, Johnson MA, Martin EW Jr: A novel approach to positron emission tomography in lung cancer. Ann Thorac Surg 2008, 86:1355-1357.
• [28]Piert M, Carey J, Clinthorne N: Probe-guided localization of cancer deposits using [(18)F]fluorodeoxyglucose. Q J Nucl Med Mol Imaging 2008, 52:37-49.
• [29]Povoski SP, Hall NC, Martin EW, Walker MJ: Multimodality approach of perioperative 18F-FDG PET/CT imaging, intraoperative 18F-FDG handheld gamma probe detection, and intraoperative ultrasound for tumor localization and verification of resection of all sites of hypermetabolic activity in a case of occult recurrent metastatic melanoma. World J Surg Oncol 2008, 6:1. BioMed Central Full Text
• [30]Povoski SP, Sarikaya I, White WC, Marsh SG, Hall NC, Hinkle GH, Martin EW Jr, Knopp MV: Comprehensive evaluation of occupational radiation exposure to intraoperative and perioperative personnel from 18F-FDG radioguided surgical procedures. Eur J Nucl Med Mol Imaging 2008, 35:2026-2034.
• [31]Murrey DA Jr, Bahnson EE, Hall NC, Povoski SP, Mojzisik CM, Young DC, Sharif S, Johnson MA, Abdel-Misih S, Martin EW Jr, Knopp MV: Perioperative (18)F-fluorodeoxyglucose-guided imaging using the becquerel as a quantitative measure for optimizing surgical resection in patients with advanced malignancy. Am J Surg 2009, 198:834-840.
• [32]Gollub MJ, Akhurst TJ, Williamson MJ, Shia J, Humm JL, Wong WD, Paty PB, Guillem JG, Weiser MR, Temple LK, Dauer LT, Jhanwar SC, Kronman RE, Montalvo CV, Miller AR, Larson SM, Margulis AR: Feasibility of ex vivo FDG PET of the colon. Radiology 2009, 252:232-239.
• [33]Molina MA, Goodwin WJ, Moffat FL, Serafini AN, Sfakianakis GN, Avisar E: Intra-operative use of PET probe for localization of FDG avid lesions. Cancer Imaging 2009, 9:59-62.
• [34]Hall NC, Povoski SP, Murrey DA, Martin EW Jr, Knopp MV: Ex vivo specimen FDG PET/CT imaging for oncology. Radiology 2010, 255:663-664.
• [35]Nalley C, Wiebeck K, Bartel TB, Bodenner D, Stack BC Jr: Intraoperative radiation exposure with the use of (18)F-FDG-guided thyroid cancer surgery. Otolaryngol Head Neck Surg 2010, 142:281-283.
• [36]de Jong JS, van Ginkel RJ, Slart RH, Lemstra CL, Paans AM, Mulder NH, Hoekstra HJ: FDG-PET probe-guided surgery for recurrent retroperitoneal testicular tumor recurrences. Eur J Surg Oncol 2010, 36:1092-1095.
• [37]Lee GO, Costouro NG, Groome T, Kashani-Sabet M, Leong SPL: The use of intraoperative PET probe to resect metastatic melanoma. BMJ Case Reports 2010. doi:10.1136/bcr.12.2009.2593
• [38]García JR, Fraile M, Soler M, Bechini J, Ayuso JR, Lomeña F: PET/CT-guided salvage surgery protocol. Results with ROLL technique and PET probe. Rev Esp Med Nucl 2011, 30:217-222. Spanish
• [39]Kim WW, Kim JS, Hur SM, Kim SH, Lee SK, Choi JH, Kim S, Choi JY, Lee JE, Kim JH, Nam SJ, Yang JH, Choe JH: Radioguided surgery using an intraoperative PET probe for tumor localization and verification of complete resection in differentiated thyroid cancer: a pilot study. Surgery 2011, 149:416-424.
• [40]Manca G, Biggi E, Lorenzoni A, Boni G, Roncella M, Ghilli M, Volterrani D, Mariani G: Simultaneous detection of breast tumor resection margins and radioguided sentinel node biopsy using an intraoperative electronically collimated probe with variable energy window: a case report. Clin Nucl Med 2011, 36:e196-e198.
• [41]Povoski SP, Hall NC, Murrey DA Jr, Chow AZ, Gaglani JR, Bahnson EE, Mojzisik CM, Kuhrt MP, Hitchcock CL, Knopp MV, Martin EW Jr: Multimodal imaging and detection approach to 18F-FDG-directed surgery for patients with known or suspected malignancies: a comprehensive description of the specific methodology utilized in a single-institution cumulative retrospective experience. World J Surg Oncol 2011, 9:152. BioMed Central Full Text
• [42]Francis CL, Nalley C, Fan C, Bodenner D, Stack BC Jr: 18F-fluorodeoxyglucose and 131I radioguided surgical management of thyroid cancer. Otolaryngol Head Neck Surg 2012, 146:26-32.
• [43]Bains S, Reimert M, Win AZ, Khan S, Aparici CM: A patient with psoriatic arthritis imaged with FDG-PET/CT demonstrated an unusual imaging pattern with muscle and fascia involvement: a case report. Nucl Med Mol Imaging 2012, 46:138-143.
• [44]Vos CG, Hartemink KJ, Muller S, Oosterhuis JW, Meijer S, van den Tol MP, Comans EF: Clinical applications of FDG-probe guided surgery. Acta Chir Belg 2012, 112:414-418.
• [45]Hall NC, Povoski SP, Zhang J, Knopp MV, Martin EW Jr: Use of intraoperative nuclear medicine imaging technology: strategy for improved patient management. Expert Rev Med Devices 2013, 10:149-152.
• [46]Yasuda S, Makuuchi H, Fujii H, Nakasaki H, Mukai M, Sadahiro S, Tajima T, Ide M, Shohtsu A, Suzuki Y: Evaluation of a surgical gamma probe for detection of 18F-FDG. Tokai J Exp Clin Med 2000, 25:93-99.
• [47]Yamamoto S, Matsumoto K, Senda M: Optimum threshold setting for a positron-sensitive probe with background rejection capability. Ann Nucl Med 2004, 18:251-256.
• [48]Yamamoto S, Matsumoto K, Sakamoto S, Tarutani K, Minato K, Senda M: An intra-operative positron probe with background rejection capability for FDG-guided surgery. Ann Nucl Med 2005, 19:23-28.
• [49]Yamamoto S, Higashi T, Matsumoto K, Senda M: Development of a positron-imaging detector with background rejection capability. Ann Nucl Med 2006, 20:655-662.
• [50]Thurston MO: Development of the gamma-detecting probe for radioimmunoguided surgery. In Radioimmunoguided Surgery (RIGS) in the Detection and Treatment of Colorectal Cancer. 1st edition. Edited by Martin EW. Austin: R.G. Landes Company; 1994:41-65.
• [51]Martin EW Jr, Thurston MO: The use of monoclonal antibodies (MAbs) and the development of an intraoperative hand-held probe for cancer detection. Cancer Invest 1996, 14:560-571.
• [52]Martin EW Jr, Thurston MO: Method for locating, differentiating, and removing neoplasms. Publication number: US 4782840 A. Filing date September 10, 1986. Publication date: November 8, 1988. http://www.google.com/patents/US4782840 webcite
• [53]Ramsey RC, Thurston MO: Gamma radiation detector with enhanced signal treatment. Publication number: US 4889991 A. Filing date: September 23, 1988. Publication date: December 26, 1989. http://www.google.com/patents/US4889991 webcite
• [54]Arnold MW, Young DC, Hitchcock CL, Schneebaum S, Martin EW Jr: Radioimmunoguided surgery in primary colorectal carcinoma: an intraoperative prognostic tool and adjuvant to traditional staging. Am J Surg 1995, 170:315-318.
• [55]Bertsch DJ, Burak WE Jr, Young DC, Arnold MW, Martin EW Jr: Radioimmunoguided Surgery system improves survival for patients with recurrent colorectal cancer. Surgery 1995, 118:634-638. discussion 638–639
• [56]Bertsch DJ, Burak WE Jr, Young DC, Arnold MW, Martin EW Jr: Radioimmunoguided surgery for colorectal cancer. Ann Surg Oncol 1996, 3:310-316.
• [57]Arnold MW, Hitchcock CL, Young DC, Burak WE Jr, Bertsch DJ, Martin EW Jr: Intra-abdominal patterns of disease dissemination in colorectal cancer identified using radioimmunoguided surgery. Dis Colon Rectum 1996, 39:509-513.
• [58]Barbera-Guillem E, Arnold MW, Nelson MB, Martin EW Jr: First results for resetting the antitumor immune response by immune corrective surgery in colon cancer. Am J Surg 1998, 176:339-343.
• [59]Martin EW, Chapman GJ, Subramaniam VV, Povoski SP: Intraoperative detection of gamma emissions using K-alpha X-ray fluorescence. Expert Rev Med Devices 2010, 7:431-434.
• [60]Currie LA: Limits for qualitative detection and quantitative determination. Application to radiochemistry. Anal Chem 1968, 40:586-593.
• [61]Knoll GF: Radiation Detection and Measurement. 4th edition. New York, New York: John Wiley & Sons, Inc; 2010.
• [62]Miller I, Freund JE: Probability and Statistics for Engineers. 2nd edition. Englewood Cliffs, New Jersey: Prentice-Hall, Inc; 1977.
• [63]Povoski SP, Hatzaras IS, Mojzisik CM, Arnold MW, Hinkle GH, Hitchcock CL, Young DC, Martin EW Jr: Antigen-directed cancer surgery for primary colorectal cancer: 15-year survival analysis. Ann Surg Oncol 2012, 19:131-138.
• [64]Povoski SP, Hatzaras IS, Mojzisik CM, Martin EW Jr: Oncologic theranostics: recognition of this concept in antigen-directed cancer therapy for colorectal cancer with anti-TAG-72 monoclonal antibodies. Expert Rev Mol Diagn 2011, 11:667-670.
• [65]Green DM, Swets JA: Signal Detection Theory and Psychophysics. 1st edition. New York, New York: John Wiley & Sons, Inc; 1966.
• [66]Zweig MH, Campbell G: Receiver-operating characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine. Clin Chem 1993, 39:561-577.
• [67]Akobeng AK: Understanding diagnostic tests 3: receiver operating characteristic curves. Acta Paediatr 2007, 96:644-647.
• [68]Benneyan JC: Performance of number-between g-type statistical control charts for monitoring adverse events. Health Care Manag Sci 2001, 4:319-336.
• [69]Phillips GW, Nagel DJ, Coffey T: A Primer on the Detection of Nuclear and Radiological Weapons. 1st edition. Washington, DC: National Defense University Center for Technology and National Security Policy; 2005.
• [70]Jendzurski J, Paulter NG: Calibration of speed enforcement down-the-road radars. J Res Natl Inst Stand Technol 2009, 114:137-148.