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Published in: Surgical Endoscopy 2/2017

Open Access 01-02-2017

Endoscopic tattooing of early colon carcinoma enhances detection of lymph nodes most prone to harbor tumor burden

Authors: Iban Aldecoa, Carla Montironi, Nuria Planell, Maria Pellise, Gloria Fernandez-Esparrach, Angels Gines, Salvadora Delgado, Dulce Momblan, Leticia Moreira, Maria Lopez-Ceron, Natalia Rakislova, Graciela Martinez-Palli, Jaume Balust, Josep Antoni Bombi, Antonio de Lacy, Antoni Castells, Francesc Balaguer, Miriam Cuatrecasas

Published in: Surgical Endoscopy | Issue 2/2017

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Abstract

Background

Colorectal cancer (CRC) screening programs result in the detection of early-stage asymptomatic carcinomas suitable to be surgically cured. Lymph nodes (LN) from early CRC are usually small and may be difficult to collect. Still, at least 12 LNs should be analyzed from colectomies, to ensure a reliable pN0 stage. Presurgical endoscopic tattooing improves LN procurement. In addition, molecular detection of occult LN tumor burden in histologically pN0 CRC patients is associated with a decreased survival rate. We aimed to study the impact of presurgical endoscopic tattooing on the molecular detection of LN tumor burden in early colon neoplasms.

Methods

A prospective cohort study from a CRC screening-based population was performed at a tertiary academic hospital. LNs from colectomies with and without preoperative endoscopic tattooing were assessed by two methods, hematoxylin and eosin (HE), and RT-LAMP, to detect tumor cytokeratin 19 (CK19) mRNA. We compared the amount of tumor burden and LN yields from tattooed and non-tattooed specimens.

Results

HE and RT-LAMP analyses of 936 LNs were performed from 71 colectomies containing early carcinomas and endoscopically unresectable adenomas (8 pT0, 17 pTis, 27 pT1, 19 pT2); 47 out of 71 (66.2 %) were tattooed. Molecular positivity correlated with the presence of tattoo in LN [p < 0.001; OR 3.1 (95 % CI 1.7–5.5)]. A significantly higher number of LNs were obtained in tattooed specimens (median 17 LN vs. 14.5 LN; p = 0.019).

Conclusions

Endoscopic tattooing enables the analysis of those LNs most prone to harbor tumor cells and improves the number of LN harvested.
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Literature
1.
go back to reference Ellis KK, Fennerty MB (1997) Marking and identifying colon lesions. Tattoos, clips, and radiology in imaging the colon. Gastrointest Endosc Clin N Am 7:401–411PubMed Ellis KK, Fennerty MB (1997) Marking and identifying colon lesions. Tattoos, clips, and radiology in imaging the colon. Gastrointest Endosc Clin N Am 7:401–411PubMed
4.
go back to reference Lacy AM, García-Valdecasas JC, Delgado S, Castells A, Taurá P, Piqué JM, Visa J (2002) Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet 359:2224–2229. doi:10.1016/S0140-6736(02)09290-5 CrossRefPubMed Lacy AM, García-Valdecasas JC, Delgado S, Castells A, Taurá P, Piqué JM, Visa J (2002) Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet 359:2224–2229. doi:10.​1016/​S0140-6736(02)09290-5 CrossRefPubMed
5.
go back to reference Quintero E, Castells A, Bujanda L, Cubiella J, Salas D, Lanas Á, Andreu M, Carballo F, Morillas JD, Hernández C, Jover R, Montalvo I, Arenas J, Laredo E, Hernández V, Iglesias F, Cid E, Zubizarreta R, Sala T, Ponce M, Andrés M, Teruel G, Peris A, Roncales M-P, Polo-Tomás M, Bessa X, Ferrer-Armengou O, Grau J, Serradesanferm A, Ono A, Cruzado J, Pérez-Riquelme F, Alonso-Abreu I, de la Vega-Prieto M, Reyes-Melian JM, Cacho G, Díaz-Tasende J, Herreros-de-Tejada A, Poves C, Santander C, González-Navarro A (2012) Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening. N Engl J Med 366:697–706. doi:10.1056/NEJMoa1108895 CrossRefPubMed Quintero E, Castells A, Bujanda L, Cubiella J, Salas D, Lanas Á, Andreu M, Carballo F, Morillas JD, Hernández C, Jover R, Montalvo I, Arenas J, Laredo E, Hernández V, Iglesias F, Cid E, Zubizarreta R, Sala T, Ponce M, Andrés M, Teruel G, Peris A, Roncales M-P, Polo-Tomás M, Bessa X, Ferrer-Armengou O, Grau J, Serradesanferm A, Ono A, Cruzado J, Pérez-Riquelme F, Alonso-Abreu I, de la Vega-Prieto M, Reyes-Melian JM, Cacho G, Díaz-Tasende J, Herreros-de-Tejada A, Poves C, Santander C, González-Navarro A (2012) Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening. N Engl J Med 366:697–706. doi:10.​1056/​NEJMoa1108895 CrossRefPubMed
6.
go back to reference Williams JG, Pullan RD, Hill J, Horgan PG, Salmo E, Buchanan GN, Rasheed S, McGee SG, Haboubi N (2013) Management of the malignant colorectal polyp: ACPGBI position statement. Colorectal Dis 15:1–38. doi:10.1111/codi.12262 CrossRefPubMed Williams JG, Pullan RD, Hill J, Horgan PG, Salmo E, Buchanan GN, Rasheed S, McGee SG, Haboubi N (2013) Management of the malignant colorectal polyp: ACPGBI position statement. Colorectal Dis 15:1–38. doi:10.​1111/​codi.​12262 CrossRefPubMed
8.
go back to reference Kelder W, Inberg B, Schaapveld M, Karrenbeld A, Grond J, Wiggers T, Plukker JT (2009) Impact of the number of histologically examined lymph nodes on prognosis in colon cancer: a population-based study in the Netherlands. Dis Colon Rectum 52:260–267. doi:10.1007/DCR.0b013e3181979164 CrossRefPubMed Kelder W, Inberg B, Schaapveld M, Karrenbeld A, Grond J, Wiggers T, Plukker JT (2009) Impact of the number of histologically examined lymph nodes on prognosis in colon cancer: a population-based study in the Netherlands. Dis Colon Rectum 52:260–267. doi:10.​1007/​DCR.​0b013e3181979164​ CrossRefPubMed
11.
go back to reference Rosenberg R, Friederichs J, Schuster T, Gertler R, Maak M, Becker K, Grebner A, Ulm K, Höfler H, Nekarda H, Siewert J-R (2008) Prognosis of patients with colorectal cancer is associated with lymph node ratio: a single-center analysis of 3,026 patients over a 25-year time period. Ann Surg 248:968–978. doi:10.1097/SLA.0b013e318190eddc CrossRefPubMed Rosenberg R, Friederichs J, Schuster T, Gertler R, Maak M, Becker K, Grebner A, Ulm K, Höfler H, Nekarda H, Siewert J-R (2008) Prognosis of patients with colorectal cancer is associated with lymph node ratio: a single-center analysis of 3,026 patients over a 25-year time period. Ann Surg 248:968–978. doi:10.​1097/​SLA.​0b013e318190eddc​ CrossRefPubMed
12.
go back to reference Rahbari NN, Bork U, Motschall E, Thorlund K, Büchler MW, Koch M, Weitz J (2012) Molecular detection of tumor cells in regional lymph nodes is associated with disease recurrence and poor survival in node-negative colorectal cancer: a systematic review and meta-analysis. J Clin Oncol 30:60–70. doi:10.1200/JCO.2011.36.9504 CrossRefPubMed Rahbari NN, Bork U, Motschall E, Thorlund K, Büchler MW, Koch M, Weitz J (2012) Molecular detection of tumor cells in regional lymph nodes is associated with disease recurrence and poor survival in node-negative colorectal cancer: a systematic review and meta-analysis. J Clin Oncol 30:60–70. doi:10.​1200/​JCO.​2011.​36.​9504 CrossRefPubMed
14.
go back to reference Sloothaak DAM, Sahami S, van der Zaag-Loonen HJ, van der Zaag ES, Tanis PJ, Bemelman WA, Buskens CJ (2014) The prognostic value of micrometastases and isolated tumour cells in histologically negative lymph nodes of patients with colorectal cancer: a systematic review and meta-analysis. Eur J Surg Oncol 40:263–269. doi:10.1016/j.ejso.2013.12.002 CrossRefPubMed Sloothaak DAM, Sahami S, van der Zaag-Loonen HJ, van der Zaag ES, Tanis PJ, Bemelman WA, Buskens CJ (2014) The prognostic value of micrometastases and isolated tumour cells in histologically negative lymph nodes of patients with colorectal cancer: a systematic review and meta-analysis. Eur J Surg Oncol 40:263–269. doi:10.​1016/​j.​ejso.​2013.​12.​002 CrossRefPubMed
15.
go back to reference Sirop S, Kanaan M, Korant A, Wiese D, Eilender D, Nagpal S, Arora M, Singh T, Saha S (2011) Detection and prognostic impact of micrometastasis in colorectal cancer. J Surg Oncol 103:534–537. doi:10.1002/jso.21793 CrossRefPubMed Sirop S, Kanaan M, Korant A, Wiese D, Eilender D, Nagpal S, Arora M, Singh T, Saha S (2011) Detection and prognostic impact of micrometastasis in colorectal cancer. J Surg Oncol 103:534–537. doi:10.​1002/​jso.​21793 CrossRefPubMed
17.
go back to reference Croner RS, Geppert C-I, Bader FG, Nitsche U, Späth C, Rosenberg R, Zettl A, Matias-Guiu X, Tarragona J, Güller U, Stürzl M, Zuber M (2014) Molecular staging of lymph node-negative colon carcinomas by one-step nucleic acid amplification (OSNA) results in upstaging of a quarter of patients in a prospective, European, multicentre study. Br J Cancer 110:2544–2550. doi:10.1038/bjc.2014.170 CrossRefPubMedPubMedCentral Croner RS, Geppert C-I, Bader FG, Nitsche U, Späth C, Rosenberg R, Zettl A, Matias-Guiu X, Tarragona J, Güller U, Stürzl M, Zuber M (2014) Molecular staging of lymph node-negative colon carcinomas by one-step nucleic acid amplification (OSNA) results in upstaging of a quarter of patients in a prospective, European, multicentre study. Br J Cancer 110:2544–2550. doi:10.​1038/​bjc.​2014.​170 CrossRefPubMedPubMedCentral
18.
go back to reference Güller U, Zettl A, Worni M, Langer I, Cabalzar-Wondberg D, Viehl CT, Demartines N, Zuber M (2012) Molecular investigation of lymph nodes in colon cancer patients using one-step nucleic acid amplification (OSNA): a new road to better staging? Cancer 118:6039–6045. doi:10.1002/cncr.27667 CrossRefPubMedPubMedCentral Güller U, Zettl A, Worni M, Langer I, Cabalzar-Wondberg D, Viehl CT, Demartines N, Zuber M (2012) Molecular investigation of lymph nodes in colon cancer patients using one-step nucleic acid amplification (OSNA): a new road to better staging? Cancer 118:6039–6045. doi:10.​1002/​cncr.​27667 CrossRefPubMedPubMedCentral
19.
go back to reference Iddings D, Ahmad A, Elashoff D, Bilchik A (2006) The prognostic effect of micrometastases in previously staged lymph node negative (N0) colorectal carcinoma: a meta-analysis. Ann Surg Oncol 13:1386–1392. doi:10.1245/s10434-006-9120-y CrossRefPubMed Iddings D, Ahmad A, Elashoff D, Bilchik A (2006) The prognostic effect of micrometastases in previously staged lymph node negative (N0) colorectal carcinoma: a meta-analysis. Ann Surg Oncol 13:1386–1392. doi:10.​1245/​s10434-006-9120-y CrossRefPubMed
21.
22.
go back to reference Feo CV, Portinari M, Zuolo M, Targa S, Matarese VG, Gafà R, Forini E, Lanza G (2015) Preoperative endoscopic tattooing to mark the tumour site does not improve lymph node retrieval in colorectal cancer: a retrospective cohort study. J Negat Results Biomed 14:9. doi:10.1186/s12952-015-0027-7 CrossRefPubMedPubMedCentral Feo CV, Portinari M, Zuolo M, Targa S, Matarese VG, Gafà R, Forini E, Lanza G (2015) Preoperative endoscopic tattooing to mark the tumour site does not improve lymph node retrieval in colorectal cancer: a retrospective cohort study. J Negat Results Biomed 14:9. doi:10.​1186/​s12952-015-0027-7 CrossRefPubMedPubMedCentral
24.
go back to reference Viehl CT, Guller U, Hamel CT, Riehle HM, Plaass C, Marti WR, Oertli D, Zuber M (2006) Carbon dye staining of sentinel lymph nodes facilitates microstaging of colon cancer patients. World J Surg 30:453–456. doi:10.1007/s00268-005-0336-y CrossRefPubMed Viehl CT, Guller U, Hamel CT, Riehle HM, Plaass C, Marti WR, Oertli D, Zuber M (2006) Carbon dye staining of sentinel lymph nodes facilitates microstaging of colon cancer patients. World J Surg 30:453–456. doi:10.​1007/​s00268-005-0336-y CrossRefPubMed
26.
go back to reference Peg V, Espinosa-Bravo M, Vieites B, Vilardell F, Antúnez JR, de Salas MS, Delgado-Sánchez JJ, Pinto W, Gozalbo F, Petit A, Sansano I, Del Mar Téllez M, Rubio IT (2013) Intraoperative molecular analysis of total tumor load in sentinel lymph node: a new predictor of axillary status in early breast cancer patients. Breast Cancer Res Treat 139:87–93. doi:10.1007/s10549-013-2524-z CrossRefPubMed Peg V, Espinosa-Bravo M, Vieites B, Vilardell F, Antúnez JR, de Salas MS, Delgado-Sánchez JJ, Pinto W, Gozalbo F, Petit A, Sansano I, Del Mar Téllez M, Rubio IT (2013) Intraoperative molecular analysis of total tumor load in sentinel lymph node: a new predictor of axillary status in early breast cancer patients. Breast Cancer Res Treat 139:87–93. doi:10.​1007/​s10549-013-2524-z CrossRefPubMed
27.
go back to reference Yamamoto H, Tomita N, Inomata M, Furuhata T, Miyake Y, Noura S, Kato T, Murata K, Hayashi S, Igarashi S, Itabashi M, Kameoka S, Matsuura N (2015) OSNA-assisted molecular staging in colorectal cancer: a prospective multicenter trial in Japan. Ann Surg Oncol. doi:10.1245/s10434-015-4880-x Yamamoto H, Tomita N, Inomata M, Furuhata T, Miyake Y, Noura S, Kato T, Murata K, Hayashi S, Igarashi S, Itabashi M, Kameoka S, Matsuura N (2015) OSNA-assisted molecular staging in colorectal cancer: a prospective multicenter trial in Japan. Ann Surg Oncol. doi:10.​1245/​s10434-015-4880-x
28.
go back to reference Yamamoto H, Sekimoto M, Oya M, Yamamoto N, Konishi F, Sasaki J, Yamada S, Taniyama K, Tominaga H, Tsujimoto M, Akamatsu H, Yanagisawa A, Sakakura C, Kato Y, Matsuura N (2011) OSNA-based novel molecular testing for lymph node metastases in colorectal cancer patients: results from a multicenter clinical performance study in Japan. Ann Surg Oncol 18:1891–1898. doi:10.1245/s10434-010-1539-5 CrossRefPubMed Yamamoto H, Sekimoto M, Oya M, Yamamoto N, Konishi F, Sasaki J, Yamada S, Taniyama K, Tominaga H, Tsujimoto M, Akamatsu H, Yanagisawa A, Sakakura C, Kato Y, Matsuura N (2011) OSNA-based novel molecular testing for lymph node metastases in colorectal cancer patients: results from a multicenter clinical performance study in Japan. Ann Surg Oncol 18:1891–1898. doi:10.​1245/​s10434-010-1539-5 CrossRefPubMed
29.
go back to reference Oezkan F, Khan AM, Hager T, Freitag L, Christoph D, Darwiche K (2015) OSNA: a fast molecular test based on CK19 mRNA concentration for assessment of EBUS–TBNA samples in lung cancer patients. Clin Lung Cancer. doi:10.1016/j.cllc.2015.09.001 PubMed Oezkan F, Khan AM, Hager T, Freitag L, Christoph D, Darwiche K (2015) OSNA: a fast molecular test based on CK19 mRNA concentration for assessment of EBUS–TBNA samples in lung cancer patients. Clin Lung Cancer. doi:10.​1016/​j.​cllc.​2015.​09.​001 PubMed
30.
go back to reference Nagai T, Niikura H, Okamoto S, Nakabayashi K, Matoda M, Utsunomiya H, Nagase S, Watanabe M, Takeshima N, Yaegashi N (2015) A new diagnostic method for rapid detection of lymph node metastases using a one-step nucleic acid amplification (OSNA) assay in endometrial cancer. Ann Surg Oncol 22:980–986. doi:10.1245/s10434-014-4038-2 CrossRefPubMed Nagai T, Niikura H, Okamoto S, Nakabayashi K, Matoda M, Utsunomiya H, Nagase S, Watanabe M, Takeshima N, Yaegashi N (2015) A new diagnostic method for rapid detection of lymph node metastases using a one-step nucleic acid amplification (OSNA) assay in endometrial cancer. Ann Surg Oncol 22:980–986. doi:10.​1245/​s10434-014-4038-2 CrossRefPubMed
31.
go back to reference Del Carmen S, Gatius S, Franch-Arcas G, Baena JA, Gonzalez O, Zafon C, Cuevas D, Valls J, Pérez A, Martinez M, Ros S, Macías CG, Iglesias C, Matías-Guiu X, de Álava E (2015) Concordance study between one-step nucleic acid amplification and morphologic techniques to detect lymph node metastasis in papillary carcinoma of the thyroid. Hum Pathol 48:132–141. doi:10.1016/j.humpath.2015.09.020 CrossRefPubMed Del Carmen S, Gatius S, Franch-Arcas G, Baena JA, Gonzalez O, Zafon C, Cuevas D, Valls J, Pérez A, Martinez M, Ros S, Macías CG, Iglesias C, Matías-Guiu X, de Álava E (2015) Concordance study between one-step nucleic acid amplification and morphologic techniques to detect lymph node metastasis in papillary carcinoma of the thyroid. Hum Pathol 48:132–141. doi:10.​1016/​j.​humpath.​2015.​09.​020 CrossRefPubMed
32.
go back to reference Rembacken B, Hassan C, Riemann JF, Chilton A, Rutter M, Dumonceau J-M, Omar M, Ponchon T (2012) Quality in screening colonoscopy: position statement of the European Society of Gastrointestinal Endoscopy (ESGE). Endoscopy 44:957–968. doi:10.1055/s-0032-1325686 CrossRefPubMed Rembacken B, Hassan C, Riemann JF, Chilton A, Rutter M, Dumonceau J-M, Omar M, Ponchon T (2012) Quality in screening colonoscopy: position statement of the European Society of Gastrointestinal Endoscopy (ESGE). Endoscopy 44:957–968. doi:10.​1055/​s-0032-1325686 CrossRefPubMed
33.
go back to reference Washington MK, Berlin J, Branton P, Burgart LJ, Carter DK, Fitzgibbons PL, Halling K, Frankel W, Jessup J, Kakar S, Minsky B, Nakhleh R, Compton CC (2009) Protocol for the examination of specimens from patients with primary carcinoma of the colon and rectum. Arch Pathol Lab Med 133:1539–1551. doi:10.1043/1543-2165-133.10.1539 PubMedPubMedCentral Washington MK, Berlin J, Branton P, Burgart LJ, Carter DK, Fitzgibbons PL, Halling K, Frankel W, Jessup J, Kakar S, Minsky B, Nakhleh R, Compton CC (2009) Protocol for the examination of specimens from patients with primary carcinoma of the colon and rectum. Arch Pathol Lab Med 133:1539–1551. doi:10.​1043/​1543-2165-133.​10.​1539 PubMedPubMedCentral
34.
go back to reference Tsujimoto M, Nakabayashi K, Yoshidome K, Kaneko T, Iwase T, Akiyama F, Kato Y, Tsuda H, Ueda S, Sato K, Tamaki Y, Noguchi S, Kataoka TR, Nakajima H, Komoike Y, Inaji H, Tsugawa K, Suzuki K, Nakamura S, Daitoh M, Otomo Y, Matsuura N (2007) One-step nucleic acid amplification for intraoperative detection of lymph node metastasis in breast cancer patients. Clin Cancer Res 13:4807–4816. doi:10.1158/1078-0432.CCR-06-2512 CrossRefPubMed Tsujimoto M, Nakabayashi K, Yoshidome K, Kaneko T, Iwase T, Akiyama F, Kato Y, Tsuda H, Ueda S, Sato K, Tamaki Y, Noguchi S, Kataoka TR, Nakajima H, Komoike Y, Inaji H, Tsugawa K, Suzuki K, Nakamura S, Daitoh M, Otomo Y, Matsuura N (2007) One-step nucleic acid amplification for intraoperative detection of lymph node metastasis in breast cancer patients. Clin Cancer Res 13:4807–4816. doi:10.​1158/​1078-0432.​CCR-06-2512 CrossRefPubMed
35.
go back to reference Visser M, Jiwa M, Horstman A, Brink AATP, Pol RP, van Diest P, Snijders PJF, Meijer CJLM (2008) Intra-operative rapid diagnostic method based on CK19 mRNA expression for the detection of lymph node metastases in breast cancer. Int J Cancer 122:2562–2567. doi:10.1002/ijc.23451 CrossRefPubMedPubMedCentral Visser M, Jiwa M, Horstman A, Brink AATP, Pol RP, van Diest P, Snijders PJF, Meijer CJLM (2008) Intra-operative rapid diagnostic method based on CK19 mRNA expression for the detection of lymph node metastases in breast cancer. Int J Cancer 122:2562–2567. doi:10.​1002/​ijc.​23451 CrossRefPubMedPubMedCentral
37.
go back to reference Goldstein NS (2002) Lymph node recoveries from 2427 pT3 colorectal resection specimens spanning 45 years: recommendations for a minimum number of recovered lymph nodes based on predictive probabilities. Am J Surg Pathol 26:179–189CrossRefPubMed Goldstein NS (2002) Lymph node recoveries from 2427 pT3 colorectal resection specimens spanning 45 years: recommendations for a minimum number of recovered lymph nodes based on predictive probabilities. Am J Surg Pathol 26:179–189CrossRefPubMed
38.
go back to reference Johnson PM, Malatjalian D, Porter GA (2002) Adequacy of nodal harvest in colorectal cancer: a consecutive cohort study. J Gastrointest Surg 6:883–888 (discussion 889–890) CrossRefPubMed Johnson PM, Malatjalian D, Porter GA (2002) Adequacy of nodal harvest in colorectal cancer: a consecutive cohort study. J Gastrointest Surg 6:883–888 (discussion 889–890) CrossRefPubMed
39.
go back to reference Espinosa-Bravo M, Sansano I, Pérez-Hoyos S, Ramos M, Sancho M, Xercavins J, Rubio IT, Peg V (2013) Prediction of non-sentinel lymph node metastasis in early breast cancer by assessing total tumoral load in the sentinel lymph node by molecular assay. Eur J Surg Oncol 39:766–773. doi:10.1016/j.ejso.2013.03.011 CrossRefPubMed Espinosa-Bravo M, Sansano I, Pérez-Hoyos S, Ramos M, Sancho M, Xercavins J, Rubio IT, Peg V (2013) Prediction of non-sentinel lymph node metastasis in early breast cancer by assessing total tumoral load in the sentinel lymph node by molecular assay. Eur J Surg Oncol 39:766–773. doi:10.​1016/​j.​ejso.​2013.​03.​011 CrossRefPubMed
42.
go back to reference Bettegowda C, Sausen M, Leary RJ, Kinde I, Wang Y, Agrawal N, Bartlett BR, Wang H, Luber B, Alani RM, Antonarakis ES, Azad NS, Bardelli A, Brem H, Cameron JL, Lee CC, Fecher LA, Gallia GL, Gibbs P, Le D, Giuntoli RL, Goggins M, Hogarty MD, Holdhoff M, Hong S-M, Jiao Y, Juhl HH, Kim JJ, Siravegna G, Laheru DA, Lauricella C, Lim M, Lipson EJ, Marie SKN, Netto GJ, Oliner KS, Olivi A, Olsson L, Riggins GJ, Sartore-Bianchi A, Schmidt K, Shih le-M, Oba-Shinjo SM, Siena S, Theodorescu D, Tie J, Harkins TT, Veronese S, Wang T-L, Weingart JD, Wolfgang CL, Wood LD, Xing D, Hruban RH, Wu J, Allen PJ, Schmidt CM, Choti MA, Velculescu VE, Kinzler KW, Vogelstein B, Papadopoulos N, Diaz LA (2014) Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med 6:224ra24. doi:10.1126/scitranslmed.3007094 CrossRefPubMedPubMedCentral Bettegowda C, Sausen M, Leary RJ, Kinde I, Wang Y, Agrawal N, Bartlett BR, Wang H, Luber B, Alani RM, Antonarakis ES, Azad NS, Bardelli A, Brem H, Cameron JL, Lee CC, Fecher LA, Gallia GL, Gibbs P, Le D, Giuntoli RL, Goggins M, Hogarty MD, Holdhoff M, Hong S-M, Jiao Y, Juhl HH, Kim JJ, Siravegna G, Laheru DA, Lauricella C, Lim M, Lipson EJ, Marie SKN, Netto GJ, Oliner KS, Olivi A, Olsson L, Riggins GJ, Sartore-Bianchi A, Schmidt K, Shih le-M, Oba-Shinjo SM, Siena S, Theodorescu D, Tie J, Harkins TT, Veronese S, Wang T-L, Weingart JD, Wolfgang CL, Wood LD, Xing D, Hruban RH, Wu J, Allen PJ, Schmidt CM, Choti MA, Velculescu VE, Kinzler KW, Vogelstein B, Papadopoulos N, Diaz LA (2014) Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med 6:224ra24. doi:10.​1126/​scitranslmed.​3007094 CrossRefPubMedPubMedCentral
Metadata
Title
Endoscopic tattooing of early colon carcinoma enhances detection of lymph nodes most prone to harbor tumor burden
Authors
Iban Aldecoa
Carla Montironi
Nuria Planell
Maria Pellise
Gloria Fernandez-Esparrach
Angels Gines
Salvadora Delgado
Dulce Momblan
Leticia Moreira
Maria Lopez-Ceron
Natalia Rakislova
Graciela Martinez-Palli
Jaume Balust
Josep Antoni Bombi
Antonio de Lacy
Antoni Castells
Francesc Balaguer
Miriam Cuatrecasas
Publication date
01-02-2017
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 2/2017
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-016-5026-3

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