Abstract

Treatment of resectable esophageal cancer includes neoadjuvant chemo-radiation therapy (nCRT) followed by esophagectomy in operable patients. High-risk surgery may have been avoided in patients with a pathological complete response (pCR). We investigated the feasibility of optical coherence tomography (OCT) to detect residual cancer and radiation-induced fibrosis in 10 esophageal cancer patients that underwent nCRT followed by esophagectomy. We compared our OCT findings with histopathology. Overall, OCT was able to differentiate between healthy tissue, fibrotic tissue, and residual cancer with a sensitivity and specificity of 79% and 67%, respectively. Hence, OCT has the potential to add to the assessment of a pCR.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2018 (2)

R. Langer and K. Becker, “Tumor regression grading of gastrointestinal cancers after neoadjuvant therapy,” Virchows Arch. 472(2), 175–186 (2018).
[PubMed]

P. Jelvehgaran, D. M. de Bruin, F. J. Salguero, G. R. Borst, J.-Y. Song, T. G. van Leeuwen, J. F. de Boer, T. Alderliesten, and M. van Herk, “Feasibility of using optical coherence tomography to detect acute radiation-induced esophageal damage in small animal models,” J. Biomed. Opt. 23(4), 1–12 (2018).
[Crossref] [PubMed]

2017 (3)

P. Jelvehgaran, T. Alderliesten, J. J. A. Weda, M. de Bruin, D. J. Faber, M. C. C. M. Hulshof, T. G. van Leeuwen, M. van Herk, and J. F. de Boer, “Visibility of fiducial markers used for image-guided radiation therapy on optical coherence tomography for registration with CT: an esophageal phantom study,” Med. Phys. 44(12), 6570–6582 (2017).
[Crossref] [PubMed]

A. M. Brown, M. J. Pucci, A. C. Berger, T. Tatarian, N. R. Evans, I. I. I. Ernest, and L. R. Francesco, “A standardized comparison of peri-operative complications after minimally invasive esophagectomy : Ivor Lewis versus McKeown,” Surg. Endosc. 32, 204–211 (2017).
[PubMed]

D. Pfirrmann, S. Tug, O. Brosteanu, M. Mehdorn, M. Busse, P. P. Grimminger, F. Lordick, T. Glatz, J. Hoeppner, H. Lang, P. Simon, and I. Gockel, “Internet-based perioperative exercise program in patients with Barrett ’ s carcinoma scheduled for esophagectomy [iPEP - study] a prospective randomized- controlled trial,” BMC Cancer 17, 413 (2017)

2016 (1)

A. Swager, D. F. Boerwinkel, D. M. de Bruin, B. L. Weusten, D. J. Faber, S. L. Meijer, T. G. van Leeuwen, W. L. Curvers, and J. J. Bergman, “Volumetric laser endomicroscopy in Barrett’s esophagus: a feasibility study on histological correlation,” Dis. Esophagus 29(6), 505–512 (2016).
[Crossref] [PubMed]

2015 (6)

H. C. Wolfsen, P. Sharma, M. B. Wallace, C. Leggett, G. Tearney, and K. K. Wang, “Safety and feasibility of volumetric laser endomicroscopy in patients with Barrett’s esophagus (with videos),” Gastrointest. Endosc. 82(4), 631–640 (2015).
[Crossref] [PubMed]

J. Guo, C. Q. Li, M. Li, X. L. Zuo, T. Yu, J. W. Liu, J. Liu, G. J. Kou, and Y. Q. Li, “Diagnostic value of probe-based confocal laser endomicroscopy and high-definition virtual chromoendoscopy in early esophageal squamous neoplasia,” Gastrointest. Endosc. 81(6), 1346–1354 (2015).
[Crossref] [PubMed]

P. Pimentel-Nunes, M. Dinis-Ribeiro, T. Ponchon, A. Repici, M. Vieth, A. De Ceglie, A. Amato, F. Berr, P. Bhandari, A. Bialek, M. Conio, J. Haringsma, C. Langner, S. Meisner, H. Messmann, M. Morino, H. Neuhaus, H. Piessevaux, M. Rugge, B. P. Saunders, M. Robaszkiewicz, S. Seewald, S. Kashin, J. M. Dumonceau, C. Hassan, and P. H. Deprez, “Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) Guideline,” Endoscopy 47(9), 829–854 (2015).
[Crossref] [PubMed]

B. J. Noordman, J. Shapiro, M. C. Spaander, K. K. Krishnadath, H. W. van Laarhoven, M. I. van Berge Henegouwen, G. A. Nieuwenhuijzen, R. van Hillegersberg, M. N. Sosef, E. W. Steyerberg, B. P. Wijnhoven, and J. J. B. van Lanschot, “Accuracy of detecting residual disease after cross neoadjuvant chemoradiotherapy for esophageal cancer (preSANO Trial): rationale and protocol,” JMIR Res. Protoc. 4(2), e79 (2015).
[Crossref] [PubMed]

J. Shapiro, J. J. B. van Lanschot, M. C. C. M. Hulshof, P. van Hagen, M. I. van Berge Henegouwen, B. P. L. Wijnhoven, H. W. M. van Laarhoven, G. A. P. Nieuwenhuijzen, G. A. P. Hospers, J. J. Bonenkamp, M. A. Cuesta, R. J. B. Blaisse, O. R. C. Busch, F. J. W. Ten Kate, G. M. Creemers, C. J. A. Punt, J. T. M. Plukker, H. M. W. Verheul, E. J. S. Bilgen, H. van Dekken, M. J. C. van der Sangen, T. Rozema, K. Biermann, J. C. Beukema, A. H. M. Piet, C. M. van Rij, J. G. Reinders, H. W. Tilanus, E. W. Steyerberg, and A. van der Gaast, “Neoadjuvant chemoradiotherapy plus surgery versus surgery alone for oesophageal or junctional cancer (CROSS): long-term results of a randomised controlled trial,” Lancet Oncol. 16(9), 1090–1098 (2015).
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M. C. J. Anderegg, E. J. de Groof, S. S. Gisbertz, R. J. Bennink, S. M. Lagarde, J. H. G. Klinkenbijl, M. G. W. Dijkgraaf, J. J. G. H. M. Bergman, M. C. C. M. Hulshof, H. W. M. van Laarhoven, and M. I. van Berge Henegouwen, “18F-FDG PET-CT after neoadjuvant chemoradiotherapy in esophageal cancer patients to optimize surgical decision making,” PLoS One 10(11), e0133690 (2015).
[Crossref] [PubMed]

2014 (2)

F. Roeder, N. H. Nicolay, T. Nguyen, L. Saleh-Ebrahimi, V. Askoxylakis, T. Bostel, F. Zwicker, J. Debus, C. Timke, and P. E. Huber, “Intensity modulated radiotherapy (IMRT) with concurrent chemotherapy as definitive treatment of locally advanced esophageal cancer,” Radiat. Oncol. 9(9), 191 (2014).
[Crossref] [PubMed]

M. J. Suter, M. J. Gora, G. Y. Lauwers, T. Arnason, J. Sauk, K. A. Gallagher, L. Kava, K. M. Tan, A. R. Soomro, T. P. Gallagher, J. A. Gardecki, B. E. Bouma, M. Rosenberg, N. S. Nishioka, and G. J. Tearney, “Esophageal-guided biopsy with volumetric laser endomicroscopy and laser cautery marking: a pilot clinical study,” Gastrointest. Endosc. 79(6), 886–896 (2014).
[Crossref] [PubMed]

2013 (1)

M. T. J. Bus, B. G. Muller, D. M. de Bruin, D. J. Faber, G. M. Kamphuis, T. G. van Leeuwen, T. M. de Reijke, and J. J. M. C. H. de la Rosette, “Volumetric in Vivo Visualization of Upper Urinary Tract Tumors Using Optical Coherence Tomography: A Pilot Study,” J. Urol. 190(6), 2236–2242 (2013).
[Crossref] [PubMed]

2012 (5)

P. Cernohorsky, D. M. de Bruin, M. van Herk, J. Bras, D. J. Faber, S. D. Strackee, and T. G. van Leeuwen, “In-situ imaging of articular cartilage of the first carpometacarpal joint using co-registered optical coherence tomography and computed tomography,” J. Biomed. Opt. 17(6), 060501 (2012).
[Crossref] [PubMed]

R. Wong, C. Walker-Dilks, and A. Raifu, “Evidence-based guideline recommendations on the use of positron emission tomography imaging in oesophageal cancer,” Clin. Oncol. 24(2), 86–104 (2012).
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P. van Hagen, M. C. C. M. Hulshof, J. J. B. van Lanschot, E. W. Steyerberg, M. I. van Berge Henegouwen, B. P. Wijnhoven, D. J. Richel, G. A. Nieuwenhuijzen, G. A. Hospers, J. J. Bonenkamp, M. A. Cuesta, R. J. Blaisse, O. R. Busch, F. J. ten Kate, G. J. Creemers, C. J. Punt, J. T. Plukker, H. M. Verheul, E. J. Spillenaar Bilgen, H. van Dekken, M. J. van der Sangen, T. Rozema, K. Biermann, J. C. Beukema, A. H. Piet, C. M. van Rij, J. G. Reinders, H. W. Tilanus, A. van der Gaast, and A. Van Der Gaast, “Preoperative Chemoradiotherapy for Esophageal or Junctional Cancer,” N. Engl. J. Med. 366(22), 2074–2084 (2012).
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W. Hatta, K. Uno, T. Koike, K. Iijima, N. Asano, A. Imatani, and T. Shimosegawa, “A prospective comparative study of optical coherence tomography and EUS for tumor staging of superficial esophageal squamous cell carcinoma,” Gastrointest. Endosc. 76(3), 548–555 (2012).
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C. Sun, F. Nolte, K. H. Y. Cheng, B. Vuong, K. K. C. Lee, B. A. Standish, B. Courtney, T. R. Marotta, A. Mariampillai, and V. X. D. Yang, “In vivo feasibility of endovascular Doppler optical coherence tomography,” Biomed. Opt. Express 3(10), 2600–2610 (2012).
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2011 (3)

C. L. Donohoe, E. McGillycuddy, and J. V. Reynolds, “Long-term health-related quality of life for disease-free esophageal cancer patients,” World J. Surg. 35(8), 1853–1860 (2011).
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R. L. G. M. Blom, W. M. J. Schreurs, H. J. Belgers, L. E. Oostenbrug, R. F. A. Vliegen, and M. N. Sosef, “The value of post-neoadjuvant therapy PET-CT in the detection of interval metastases in esophageal carcinoma,” Eur. J. Surg. Oncol. 37(9), 774–778 (2011).
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K. Thurau, D. Palmes, C. Franzius, E. Minin, N. Senninger, K. U. Juergens, and M. Bruewer, “Impact of PET-CT on primary staging and response control on multimodal treatment of esophageal cancer,” World J. Surg. 35(3), 608–616 (2011).
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2010 (3)

A. J. E. Seely, J. Ivanovic, J. Threader, A. Al-Hussaini, D. Al-Shehab, T. Ramsay, S. Gilbert, D. E. Maziak, F. M. Shamji, and R. S. Sundaresan, “Systematic classification of morbidity and mortality after thoracic surgery,” Ann. Thorac. Surg. 90(3), 936–942, discussion 942 (2010).
[Crossref] [PubMed]

A. M. Monjazeb, G. Riedlinger, M. Aklilu, K. R. Geisinger, G. Mishra, S. Isom, P. Clark, E. A. Levine, and A. W. Blackstock, “Outcomes of patients with esophageal cancer staged with [18F]fluorodeoxyglucose positron emission tomography (FDG-PET): can postchemoradiotherapy FDG-PET predict the utility of resection?” J. Clin. Oncol. 28(31), 4714–4721 (2010).
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W. Hatta, K. Uno, T. Koike, S. Yokosawa, K. Iijima, A. Imatani, and T. Shimosegawa, “Optical coherence tomography for the staging of tumor infiltration in superficial esophageal squamous cell carcinoma,” Gastrointest. Endosc. 71(6), 899–906 (2010).
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2008 (3)

Y. Chen, A. D. Aguirre, P.-L. Hsiung, S.-W. Huang, H. Mashimo, J. M. Schmitt, and J. G. Fujimoto, “Effects of axial resolution improvement on optical coherence tomography (OCT) imaging of gastrointestinal tissues,” Opt. Express 16(4), 2469–2485 (2008).
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A. Pennathur and J. D. Luketich, “Resection for esophageal cancer: strategies for optimal management,” Ann. Thorac. Surg. 85(2), S751–S756 (2008).
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H. M. Salahudeen, A. Balan, K. Naik, S. Mirsadraee, and A. F. Scarsbrook, “Impact of the introduction of integrated PET-CT into the preoperative staging pathway of patients with potentially operable oesophageal carcinoma,” Clin. Radiol. 63(7), 765–773 (2008).
[Crossref] [PubMed]

2007 (2)

H. L. van Westreenen, M. Westerterp, G. W. Sloof, H. Groen, P. M. M. Bossuyt, P. L. Jager, E. F. Comans, H. M. van Dullemen, P. Fockens, J. Stoker, E. J. van der Jagt, J. J. B. van Lanschot, and J. T. M. Plukker, “Limited additional value of positron emission tomography in staging oesophageal cancer,” Br. J. Surg. 94(12), 1515–1520 (2007).
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L. Bedenne, P. Michel, O. Bouché, C. Milan, C. Mariette, T. Conroy, D. Pezet, B. Roullet, J. F. Seitz, J. P. Herr, B. Paillot, P. Arveux, F. Bonnetain, and C. Binquet, “Chemoradiation followed by surgery compared with chemoradiation alone in squamous cancer of the esophagus: FFCD 9102,” J. Clin. Oncol. 25(10), 1160–1168 (2007).
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2006 (3)

S. H. Yun, G. J. Tearney, B. J. Vakoc, M. Shishkov, W. Y. Oh, A. E. Desjardins, M. J. Suter, R. C. Chan, J. A. Evans, I.-K. Jang, N. S. Nishioka, J. F. de Boer, and B. E. Bouma, “Comprehensive volumetric optical microscopy in vivo,” Nat. Med. 12(12), 1429–1433 (2006).
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E. P. M. van Vliet, M. J. C. Eijkemans, J. W. Poley, E. W. Steyerberg, E. J. Kuipers, and P. D. Siersema, “Staging of esophageal carcinoma in a low-volume EUS center compared with reported results from high-volume centers,” Gastrointest. Endosc. 63(7), 938–947 (2006).
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J. A. Evans, J. M. Poneros, B. E. Bouma, J. Bressner, E. F. Halpern, M. Shishkov, G. Y. Lauwers, M. M. Kenudson, N. S. Nishioka, and G. J. Tearney, “Optical coherence tomography to identify intramucosal carcinoma and high-grade dysplasia in Barrett’s esophagus,” Clin. Gastroenterol. Hepatol.  4(1), 38–43 (2006).

2005 (2)

J. W. Wolthaus, M. van Herk, S. H. Muller, J. S. Belderbos, J. V. Lebesque, J. A. de Bois, M. M. Rossi, and E. M. Damen, “Fusion of respiration-correlated PET and CT scans: correlated lung tumour motion in anatomical and functional scans,” Phys. Med. Biol. 50(7), 1569–1583 (2005).
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M. Stahl, M. Stuschke, N. Lehmann, H.-J. Meyer, M. K. Walz, S. Seeber, B. Klump, W. Budach, R. Teichmann, M. Schmitt, G. Schmitt, C. Franke, and H. Wilke, “Chemoradiation with and without surgery in patients with locally advanced squamous cell carcinoma of the esophagus,” J. Clin. Oncol. 23(10), 2310–2317 (2005).
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2004 (1)

F. Fiorica, D. Di Bona, F. Schepis, A. Licata, L. Shahied, A. Venturi, A. M. Falchi, A. Craxì, and C. Cammà, “Preoperative chemoradiotherapy for oesophageal cancer: a systematic review and meta-analysis,” Gut 53(7), 925–930 (2004).
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2003 (2)

J. D. Urschel and H. Vasan, “A meta-analysis of randomized controlled trials that compared neoadjuvant chemoradiation and surgery to surgery alone for resectable esophageal cancer,” Am. J. Surg. 185(6), 538–543 (2003).
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S. H. Bailey, D. A. Bull, D. H. Harpole, J. J. Rentz, L. A. Neumayer, T. N. Pappas, J. Daley, W. G. Henderson, B. Krasnicka, S. F. Khuri, and D. E. Wood, “Outcomes after esophagectomy: A ten-year prospective cohort,” Ann. Thorac. Surg. 75(1), 217–222 (2003).
[Crossref] [PubMed]

2002 (1)

J. D. Birkmeyer, A. E. Siewers, E. V. Finlayson, T. A. Stukel, F. L. Lucas, I. Batista, H. G. Welch, and D. E. Wennberg, “Hospital volume and surgical mortality in the United States,” N. Engl. J. Med. 346(15), 1128–1137 (2002).
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2001 (1)

A. Das, M. V. Sivak, A. Chak, R. C. Wong, V. Westphal, A. M. Rollins, J. Willis, G. Isenberg, and J. A. Izatt, “High-resolution endoscopic imaging of the GI tract: a comparative study of optical coherence tomography versus high-frequency catheter probe EUS,” Gastrointest. Endosc. 54(2), 219–224 (2001).
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2000 (1)

B. E. Bouma, G. J. Tearney, C. C. Compton, and N. S. Nishioka, “High-resolution imaging of the human esophagus and stomach in vivo using optical coherence tomography,” Gastrointest. Endosc. 51(4), 467–474 (2000).
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1998 (1)

K. Kobayashi, J. A. Izatt, M. D. Kulkarni, J. Willis, and M. V. Sivak., “High-resolution cross-sectional imaging of the gastrointestinal tract using optical coherence tomography: preliminary results,” Gastrointest. Endosc. 47(6), 515–523 (1998).
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1997 (4)

A. Sergeev, V. Gelikonov, G. Gelikonov, F. Feldchtein, R. Kuranov, N. Gladkova, N. Shakhova, L. Snopova, A. Shakhov, I. Kuznetzova, A. Denisenko, V. Pochinko, Y. Chumakov, and O. Streltzova, “In vivo endoscopic OCT imaging of precancer and cancer states of human mucosa,” Opt. Express 1(13), 432–440 (1997).
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A. Sergeev, V. Gelikonov, G. Gelikonov, F. Feldchtein, R. Kuranov, N. Gladkova, N. Shakhova, L. Snopova, A. Shakhov, I. Kuznetzova, A. Denisenko, V. Pochinko, Y. Chumakov, and O. Streltzova, “In vivo endoscopic OCT imaging of precancer and cancer states of human mucosa,” Opt. Express 1(13), 432–440 (1997).
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G. J. Tearney, M. E. Brezinski, B. E. Bouma, S. A. Boppart, C. Pitris, J. F. Southern, and J. G. Fujimoto, “In vivo endoscopic optical biopsy with optical coherence tomography,” Science 276(5321), 2037–2039 (1997).
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J.-F. Bosset, M. Gignoux, J.-P. Triboulet, E. Tiret, G. Mantion, D. Elias, P. Lozach, J.-C. Ollier, J. J. Pavy, M. Mercier, T. Sahmoud, and M. B. Tarek, “Chemoradiotherapy followed by surgery compared with surgery alone in squamous-cell cancer of the esophagus,” N. Engl. J. Med. 337(3), 161–167 (1997).
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1994 (1)

A.-M. Mandard, F. Dalibard, J.-C. Mandard, J. Marnay, M. Henry-Amar, J.-F. Petiot, A. Roussel, J.-H. Jacob, P. Segol, G. Samama, J.-M. Ollivier, S. Bonvalot, and M. Gignoux, “Pathologic assessment of tumor regression after preoperative chemoradiotherapy of esophageal carcinoma: clinicopathologic correlations,” Cancer 73(11), 2680–2686 (1994).
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1991 (1)

D. Huang, E. Swanson, C. Lin, J. Schuman, W. Stinson, W. Chang, M. Hee, T. Flotte, K. Gregory, C. Puliafito, and A. Et, “Optical coherence tomography,” Science 254, 1178–1181 (1991)

1986 (1)

K. F. Siu, H. C. Cheung, and J. Wong, “Shrinkage of the esophagus after resection for carcinoma,” Ann. Surg. 203(2), 173–176 (1986).
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Aguirre, A. D.

Aklilu, M.

A. M. Monjazeb, G. Riedlinger, M. Aklilu, K. R. Geisinger, G. Mishra, S. Isom, P. Clark, E. A. Levine, and A. W. Blackstock, “Outcomes of patients with esophageal cancer staged with [18F]fluorodeoxyglucose positron emission tomography (FDG-PET): can postchemoradiotherapy FDG-PET predict the utility of resection?” J. Clin. Oncol. 28(31), 4714–4721 (2010).
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Alderliesten, T.

P. Jelvehgaran, D. M. de Bruin, F. J. Salguero, G. R. Borst, J.-Y. Song, T. G. van Leeuwen, J. F. de Boer, T. Alderliesten, and M. van Herk, “Feasibility of using optical coherence tomography to detect acute radiation-induced esophageal damage in small animal models,” J. Biomed. Opt. 23(4), 1–12 (2018).
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P. Jelvehgaran, T. Alderliesten, J. J. A. Weda, M. de Bruin, D. J. Faber, M. C. C. M. Hulshof, T. G. van Leeuwen, M. van Herk, and J. F. de Boer, “Visibility of fiducial markers used for image-guided radiation therapy on optical coherence tomography for registration with CT: an esophageal phantom study,” Med. Phys. 44(12), 6570–6582 (2017).
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Al-Hussaini, A.

A. J. E. Seely, J. Ivanovic, J. Threader, A. Al-Hussaini, D. Al-Shehab, T. Ramsay, S. Gilbert, D. E. Maziak, F. M. Shamji, and R. S. Sundaresan, “Systematic classification of morbidity and mortality after thoracic surgery,” Ann. Thorac. Surg. 90(3), 936–942, discussion 942 (2010).
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Al-Shehab, D.

A. J. E. Seely, J. Ivanovic, J. Threader, A. Al-Hussaini, D. Al-Shehab, T. Ramsay, S. Gilbert, D. E. Maziak, F. M. Shamji, and R. S. Sundaresan, “Systematic classification of morbidity and mortality after thoracic surgery,” Ann. Thorac. Surg. 90(3), 936–942, discussion 942 (2010).
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Amato, A.

P. Pimentel-Nunes, M. Dinis-Ribeiro, T. Ponchon, A. Repici, M. Vieth, A. De Ceglie, A. Amato, F. Berr, P. Bhandari, A. Bialek, M. Conio, J. Haringsma, C. Langner, S. Meisner, H. Messmann, M. Morino, H. Neuhaus, H. Piessevaux, M. Rugge, B. P. Saunders, M. Robaszkiewicz, S. Seewald, S. Kashin, J. M. Dumonceau, C. Hassan, and P. H. Deprez, “Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) Guideline,” Endoscopy 47(9), 829–854 (2015).
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Anderegg, M. C. J.

M. C. J. Anderegg, E. J. de Groof, S. S. Gisbertz, R. J. Bennink, S. M. Lagarde, J. H. G. Klinkenbijl, M. G. W. Dijkgraaf, J. J. G. H. M. Bergman, M. C. C. M. Hulshof, H. W. M. van Laarhoven, and M. I. van Berge Henegouwen, “18F-FDG PET-CT after neoadjuvant chemoradiotherapy in esophageal cancer patients to optimize surgical decision making,” PLoS One 10(11), e0133690 (2015).
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Arnason, T.

M. J. Suter, M. J. Gora, G. Y. Lauwers, T. Arnason, J. Sauk, K. A. Gallagher, L. Kava, K. M. Tan, A. R. Soomro, T. P. Gallagher, J. A. Gardecki, B. E. Bouma, M. Rosenberg, N. S. Nishioka, and G. J. Tearney, “Esophageal-guided biopsy with volumetric laser endomicroscopy and laser cautery marking: a pilot clinical study,” Gastrointest. Endosc. 79(6), 886–896 (2014).
[Crossref] [PubMed]

Arveux, P.

L. Bedenne, P. Michel, O. Bouché, C. Milan, C. Mariette, T. Conroy, D. Pezet, B. Roullet, J. F. Seitz, J. P. Herr, B. Paillot, P. Arveux, F. Bonnetain, and C. Binquet, “Chemoradiation followed by surgery compared with chemoradiation alone in squamous cancer of the esophagus: FFCD 9102,” J. Clin. Oncol. 25(10), 1160–1168 (2007).
[Crossref] [PubMed]

Asano, N.

W. Hatta, K. Uno, T. Koike, K. Iijima, N. Asano, A. Imatani, and T. Shimosegawa, “A prospective comparative study of optical coherence tomography and EUS for tumor staging of superficial esophageal squamous cell carcinoma,” Gastrointest. Endosc. 76(3), 548–555 (2012).
[Crossref] [PubMed]

Askoxylakis, V.

F. Roeder, N. H. Nicolay, T. Nguyen, L. Saleh-Ebrahimi, V. Askoxylakis, T. Bostel, F. Zwicker, J. Debus, C. Timke, and P. E. Huber, “Intensity modulated radiotherapy (IMRT) with concurrent chemotherapy as definitive treatment of locally advanced esophageal cancer,” Radiat. Oncol. 9(9), 191 (2014).
[Crossref] [PubMed]

Bailey, S. H.

S. H. Bailey, D. A. Bull, D. H. Harpole, J. J. Rentz, L. A. Neumayer, T. N. Pappas, J. Daley, W. G. Henderson, B. Krasnicka, S. F. Khuri, and D. E. Wood, “Outcomes after esophagectomy: A ten-year prospective cohort,” Ann. Thorac. Surg. 75(1), 217–222 (2003).
[Crossref] [PubMed]

Balan, A.

H. M. Salahudeen, A. Balan, K. Naik, S. Mirsadraee, and A. F. Scarsbrook, “Impact of the introduction of integrated PET-CT into the preoperative staging pathway of patients with potentially operable oesophageal carcinoma,” Clin. Radiol. 63(7), 765–773 (2008).
[Crossref] [PubMed]

Batista, I.

J. D. Birkmeyer, A. E. Siewers, E. V. Finlayson, T. A. Stukel, F. L. Lucas, I. Batista, H. G. Welch, and D. E. Wennberg, “Hospital volume and surgical mortality in the United States,” N. Engl. J. Med. 346(15), 1128–1137 (2002).
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Becker, K.

R. Langer and K. Becker, “Tumor regression grading of gastrointestinal cancers after neoadjuvant therapy,” Virchows Arch. 472(2), 175–186 (2018).
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Bedenne, L.

L. Bedenne, P. Michel, O. Bouché, C. Milan, C. Mariette, T. Conroy, D. Pezet, B. Roullet, J. F. Seitz, J. P. Herr, B. Paillot, P. Arveux, F. Bonnetain, and C. Binquet, “Chemoradiation followed by surgery compared with chemoradiation alone in squamous cancer of the esophagus: FFCD 9102,” J. Clin. Oncol. 25(10), 1160–1168 (2007).
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Belderbos, J. S.

J. W. Wolthaus, M. van Herk, S. H. Muller, J. S. Belderbos, J. V. Lebesque, J. A. de Bois, M. M. Rossi, and E. M. Damen, “Fusion of respiration-correlated PET and CT scans: correlated lung tumour motion in anatomical and functional scans,” Phys. Med. Biol. 50(7), 1569–1583 (2005).
[Crossref] [PubMed]

Belgers, H. J.

R. L. G. M. Blom, W. M. J. Schreurs, H. J. Belgers, L. E. Oostenbrug, R. F. A. Vliegen, and M. N. Sosef, “The value of post-neoadjuvant therapy PET-CT in the detection of interval metastases in esophageal carcinoma,” Eur. J. Surg. Oncol. 37(9), 774–778 (2011).
[Crossref] [PubMed]

Bennink, R. J.

M. C. J. Anderegg, E. J. de Groof, S. S. Gisbertz, R. J. Bennink, S. M. Lagarde, J. H. G. Klinkenbijl, M. G. W. Dijkgraaf, J. J. G. H. M. Bergman, M. C. C. M. Hulshof, H. W. M. van Laarhoven, and M. I. van Berge Henegouwen, “18F-FDG PET-CT after neoadjuvant chemoradiotherapy in esophageal cancer patients to optimize surgical decision making,” PLoS One 10(11), e0133690 (2015).
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Berger, A. C.

A. M. Brown, M. J. Pucci, A. C. Berger, T. Tatarian, N. R. Evans, I. I. I. Ernest, and L. R. Francesco, “A standardized comparison of peri-operative complications after minimally invasive esophagectomy : Ivor Lewis versus McKeown,” Surg. Endosc. 32, 204–211 (2017).
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Bergman, J. J.

A. Swager, D. F. Boerwinkel, D. M. de Bruin, B. L. Weusten, D. J. Faber, S. L. Meijer, T. G. van Leeuwen, W. L. Curvers, and J. J. Bergman, “Volumetric laser endomicroscopy in Barrett’s esophagus: a feasibility study on histological correlation,” Dis. Esophagus 29(6), 505–512 (2016).
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Bergman, J. J. G. H. M.

M. C. J. Anderegg, E. J. de Groof, S. S. Gisbertz, R. J. Bennink, S. M. Lagarde, J. H. G. Klinkenbijl, M. G. W. Dijkgraaf, J. J. G. H. M. Bergman, M. C. C. M. Hulshof, H. W. M. van Laarhoven, and M. I. van Berge Henegouwen, “18F-FDG PET-CT after neoadjuvant chemoradiotherapy in esophageal cancer patients to optimize surgical decision making,” PLoS One 10(11), e0133690 (2015).
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Berr, F.

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D. Huang, E. Swanson, C. Lin, J. Schuman, W. Stinson, W. Chang, M. Hee, T. Flotte, K. Gregory, C. Puliafito, and A. Et, “Optical coherence tomography,” Science 254, 1178–1181 (1991)

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H. L. van Westreenen, M. Westerterp, G. W. Sloof, H. Groen, P. M. M. Bossuyt, P. L. Jager, E. F. Comans, H. M. van Dullemen, P. Fockens, J. Stoker, E. J. van der Jagt, J. J. B. van Lanschot, and J. T. M. Plukker, “Limited additional value of positron emission tomography in staging oesophageal cancer,” Br. J. Surg. 94(12), 1515–1520 (2007).
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G. J. Tearney, M. E. Brezinski, B. E. Bouma, S. A. Boppart, C. Pitris, J. F. Southern, and J. G. Fujimoto, “In vivo endoscopic optical biopsy with optical coherence tomography,” Science 276(5321), 2037–2039 (1997).
[Crossref] [PubMed]

Surg. Endosc. (1)

A. M. Brown, M. J. Pucci, A. C. Berger, T. Tatarian, N. R. Evans, I. I. I. Ernest, and L. R. Francesco, “A standardized comparison of peri-operative complications after minimally invasive esophagectomy : Ivor Lewis versus McKeown,” Surg. Endosc. 32, 204–211 (2017).
[PubMed]

Virchows Arch. (1)

R. Langer and K. Becker, “Tumor regression grading of gastrointestinal cancers after neoadjuvant therapy,” Virchows Arch. 472(2), 175–186 (2018).
[PubMed]

World J. Surg. (2)

K. Thurau, D. Palmes, C. Franzius, E. Minin, N. Senninger, K. U. Juergens, and M. Bruewer, “Impact of PET-CT on primary staging and response control on multimodal treatment of esophageal cancer,” World J. Surg. 35(3), 608–616 (2011).
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[Crossref] [PubMed]

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Figures (13)

Fig. 1
Fig. 1 A) The schematic demonstrates a gross tumor inside an intact esophagus prior to nCRT treatment. B) The schematic shows residual cancer and radiation-induced fibrosis as results of nCRT treatment in a cut open esophageal specimen after esophagectomy. C) The figure shows a resected esophageal specimen from patient 7 pinned to a styrene foam board. The white arrow points to the location of the primary tumor area.
Fig. 2
Fig. 2 A) This schematic diagram and image show the needle fiducial markers inserted prior to OCT imaging (patient 7). The third fiducial marker was larger in diameter for better identification on OCT. B) The schematic diagram and image demonstrate the Indian ink and suturing thread markings made after OCT imaging and prior to tissue fixation.
Fig. 3
Fig. 3 Our dedicated scanning setup with moving stage to precisely position the hand-held probe in sagittal, coronal, and axial planes.
Fig. 4
Fig. 4 A) The schematic shows a stack of six times four 20.0 X 20.0 x 8.8 mm3 OCT images with 2.0 mm overlaps between neighboring scans. Note that the usable depth of OCT imaging is limited to 2-3 mm. B) The schematic illustrates the resulting combined OCT image made from the 24 small images.
Fig. 5
Fig. 5 A) The combined OCT image covers the whole ROI in sagittal view. B) En face view of figure A. Although there are some artifacts at the interface between the OCT images in sagittal view, the resulting image quality is good. Fiducial markers are indicated by arrows.
Fig. 6
Fig. 6 A) This CT image shows GTV (yellow), CTV (blue), and PTV (red) in a sagittal view. The dashed line represents the stomach level. B) Illustration of PTV length measurement. C) Illustration of GTV length measurement.
Fig. 7
Fig. 7 A) OCT image and plot showing esophageal wall layers of a healthy part of the esophagus (epithelium (ep), lamina propria (ep), muscularis mucosa (mm), submucosa (sm), and muscle layers (ml)). B) OCT image and plot illustrating radiation-induced fibrosis with partial loss of esophageal wall layers. C) OCT image and plot illustrating residual cancer. . Note that tails of the OCT signals (beyond 1.2-1.5 mm) in A and B were very noisy have been set to 0 for visual representation.
Fig. 8
Fig. 8 A) and B) show the corresponding esophageal wall layers of a healthy part of the esophagus (epithelium (ep), lamina propria (ep), muscularis mucosa (mm), submucosa (sm), and muscle layers (ml)) on OCT and histopathology, respectively (patient 7). C) and D) represent the corresponding radiation-induced fibrosis on OCT and histopathology (patient 7). E) and F) show the corresponding residual cancer on OCT and histopathology (patient 10).
Fig. 9
Fig. 9 A) and B) show the correlation of histopathology and OCT defined borders between radiation-induced fibrosis and healthy tissue for two patients (patient 6 and 7, respectively) in the proximal and distal esophagus.
Fig. 10
Fig. 10 Distance between reference marker and radiation-induced fibrosis and healthy tissue border in OCT and histopathology.
Fig. 11
Fig. 11 A) and B) show the location of residual cancer in a patient’s esophagus (patient 7) in histopathology (in yellow) and OCT (in blue), respectively. The maximum longitudinal lengths of the residual cancer regions healthy are shown by “D”. Similarly, C) and D), E) and F), and G) and H) demonstrate the residual cancer regions of patients 6, 8, and 10 in histopathology (in yellow) and OCT (in blue).
Fig. 12
Fig. 12 A, B) Distance measurements in OCT and histopathology. The graphs demonstrate the distance between residual cancer and healthy tissue/radiation-induced fibrosis border to the reference fiducial marker in proximal and distal esophagus. C, D) Also show these distances while reducing the data points using the medians between neighboring measurements to eliminate outliers. E, F) The graphs show the maximum distance from the reference fiducial markers to the identified borders in proximal and distal esophagus.
Fig. 13
Fig. 13 A) Length of the esophagus on CT and after esophagectomy. B) The absolute value of the length ratios of the PTV and radiation-induced fibrosis regions. C) The graph shows the absolute value of the length ratios of the GTV and residual cancer regions.

Tables (3)

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Table 1 Overview of patients, their tumor regression grading (TRG) score, histopathology and OCT analysis to identify the border between 1) healthy tissue and radiation-induced fibrosis, and between 2) healthy tissue and/or fibrosis and residual cancer. “Positive” means that we identified the border in OCT or histopathology. TRG 1: fibrosis without detectable residual tumor cells; TRG 2: fibrosis with rare residual tumor cells; TRG 3: fibrosis and residual tumor cells with preponderance of fibrosis; TRG 4: fibrosis and residual tumor cells with preponderance of tumor cells, TRG 5: no tumor regression.

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Table 2 Overview of the histopathology and OCT analysis of the border between radiation-induced fibrosis and healthy tissue in three lateral levels in the proximal and distal esophagus. The numbers represent the distances between these borders and the reference fiducial markers for each specimen at the different lateral levels used for pathology. Patients that showed fibrosis with no healthy tissue in both histopathology and OCT were excluded from this table. “–” indicates that we could not identify the borders. Patients that did not show any radiation-induced fibrosis in histopathology were excluded from this table. Only patients that showed at least one correspondent measurements for both histopathology and OCT were presented.

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Table 3 Overview of the histopathology and OCT analysis of identification of residual cancer borders in several lateral levels in proximal and distal esophagus. The numbers represent the distances between the borders and the reference fiducial markers for each specimen. Patients that did not show any residual cancer in either histopathology or OCT were excluded from this table.

Equations (3)

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S 1 =  D inked   D needle  .
S 2 =  D fixated   D inked  .
M pathology  =  M OCT  .   S 1  .   S 2  .

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