Skip to main content
Top
Published in: World Journal of Surgical Oncology 1/2016

Open Access 01-12-2016 | Research

Sentinel node biopsy during thoracolaparoscopic esophagectomy for advanced esophageal cancer

Authors: Judith Boone, Monique G. G. Hobbelink, Marguerite E. I. Schipper, Frank P. Vleggaar, Inne H. M. Borel Rinkes, Robbert J. de Haas, Jelle P. Ruurda, Richard van Hillegersberg

Published in: World Journal of Surgical Oncology | Issue 1/2016

Login to get access

Abstract

Background

Omitting extensive lymph node dissection could reduce esophagectomy morbidity in patients without lymph node metastases. Sentinel node biopsy may identify abdominal or thoracic lymph node metastases, thereby differentiating treatment. Feasibility of this approach was investigated in Western European esophageal cancer patients with advanced disease, without lymph node metastases at diagnostic work-up.

Methods

The sentinel node biopsy was performed in eight esophageal cancer patients with cT1-3N0 disease. One day pre-operatively, Tc-99m-labeled nanocolloid was endoscopically injected around the tumor. Lymphoscintigraphy was performed 1 and 3 h after injection. All patients underwent robotic thoracolaparoscopic esophagectomy with two-field lymph node dissection. Intraoperatively, sentinel nodes were detected by gamma probe. The resection specimen was analyzed for remaining activity by scintigraphy and gamma probe.

Results

Visualization rates of lymphoscintigraphy 1 and 3 h after tracer injection were 88 and 100 %, respectively. Intraoperative identification rate was 38 %. Postoperative identification was possible in all patients using the gamma probe to analyze the resection specimen. In 5/8 patients, lymph node metastases were found at histopathology, none of which was detected by the sentinel node biopsy. No adverse events related to the sentinel node biopsy were observed.

Conclusions

In our advanced esophageal cancer patients who underwent thoracolaparoscopic esophagectomy, the sentinel node biopsy did not predict lymph node status. Probably the real sentinel node could not be identified due to localization adjacent to the primary tumor or bypassing due to metastatic tumor involvement. Therefore, we consider the sentinel node biopsy not feasible in advanced esophageal cancer.
Literature
2.
go back to reference Hulscher JB, van Sandick JW, de Boer AG, Wijnhoven BP, Tijssen JG, Fockens P, et al. Extended transthoracic resection compared with limited transhiatal resection for adenocarcinoma of the esophagus. N Engl J Med. 2002;347:1662–9.CrossRefPubMed Hulscher JB, van Sandick JW, de Boer AG, Wijnhoven BP, Tijssen JG, Fockens P, et al. Extended transthoracic resection compared with limited transhiatal resection for adenocarcinoma of the esophagus. N Engl J Med. 2002;347:1662–9.CrossRefPubMed
3.
go back to reference Zuidema GD, Orringer MB, Ritchie Jr WP, Turcotte JG, Condon RE, Nyhus LM. Shackelford’s surgery of the alimentary tract. Philadelphia: WB Saunders; 1996. Zuidema GD, Orringer MB, Ritchie Jr WP, Turcotte JG, Condon RE, Nyhus LM. Shackelford’s surgery of the alimentary tract. Philadelphia: WB Saunders; 1996.
4.
go back to reference Lerut T, Nafteux P, Moons J, Coosemans W, Decker G, De Leyn P, et al. Three-field lymphadenectomy for carcinoma of the esophagus and gastroesophageal junction in 174 R0 resections: impact on staging, disease-free survival, and outcome: a plea for adaptation of TNM classification in upper-half esophageal carcinoma. Ann Surg. 2004;240:962–72.CrossRefPubMedPubMedCentral Lerut T, Nafteux P, Moons J, Coosemans W, Decker G, De Leyn P, et al. Three-field lymphadenectomy for carcinoma of the esophagus and gastroesophageal junction in 174 R0 resections: impact on staging, disease-free survival, and outcome: a plea for adaptation of TNM classification in upper-half esophageal carcinoma. Ann Surg. 2004;240:962–72.CrossRefPubMedPubMedCentral
5.
go back to reference van Rossum PS, van Hillegersberg R, Lever FM, Lips IM, van Lier AL, Meijer GJ, et al. Imaging strategies in the management of oesophageal cancer: what’s the role of MRI? Eur Radiol. 2013;23:1753–65.CrossRefPubMed van Rossum PS, van Hillegersberg R, Lever FM, Lips IM, van Lier AL, Meijer GJ, et al. Imaging strategies in the management of oesophageal cancer: what’s the role of MRI? Eur Radiol. 2013;23:1753–65.CrossRefPubMed
6.
go back to reference Isono K, Sato H, Nakayama K. Results of a nationwide study on the three-field lymph node dissection of esophageal cancer. Oncology. 1991;48:411–20.CrossRefPubMed Isono K, Sato H, Nakayama K. Results of a nationwide study on the three-field lymph node dissection of esophageal cancer. Oncology. 1991;48:411–20.CrossRefPubMed
7.
go back to reference Baba M, Aikou T, Yoshinaka H, Natsugoe S, Fukumoto T, Shimazu H, et al. Long-term results of subtotal esophagectomy with three-field lymphadenectomy for carcinoma of the thoracic esophagus. Ann Surg. 1994;219:310–6.CrossRefPubMedPubMedCentral Baba M, Aikou T, Yoshinaka H, Natsugoe S, Fukumoto T, Shimazu H, et al. Long-term results of subtotal esophagectomy with three-field lymphadenectomy for carcinoma of the thoracic esophagus. Ann Surg. 1994;219:310–6.CrossRefPubMedPubMedCentral
8.
go back to reference Orringer MB, Marshall B, Chang AC, Lee J, Pickens A, Lau CL. Two thousand transhiatal esophagectomies: changing trends, lessons learned. Ann Surg. 2007;246:363–72.CrossRefPubMedPubMedCentral Orringer MB, Marshall B, Chang AC, Lee J, Pickens A, Lau CL. Two thousand transhiatal esophagectomies: changing trends, lessons learned. Ann Surg. 2007;246:363–72.CrossRefPubMedPubMedCentral
9.
go back to reference Luketich JD, Alvelo-Rivera M, Buenaventura PO, Christie NA, McCaughan JS, Litle VR, et al. Minimally invasive esophagectomy: outcomes in 222 patients. Ann Surg. 2003;238:486–94.PubMedPubMedCentral Luketich JD, Alvelo-Rivera M, Buenaventura PO, Christie NA, McCaughan JS, Litle VR, et al. Minimally invasive esophagectomy: outcomes in 222 patients. Ann Surg. 2003;238:486–94.PubMedPubMedCentral
10.
12.
go back to reference Sato K, Shigenaga R, Ueda S, Shigekawa T, Krag DN. Sentinel lymph node biopsy for breast cancer. J Surg Oncol. 2007;96:322–9.CrossRefPubMed Sato K, Shigenaga R, Ueda S, Shigekawa T, Krag DN. Sentinel lymph node biopsy for breast cancer. J Surg Oncol. 2007;96:322–9.CrossRefPubMed
13.
go back to reference Kim T, Giuliano AE, Lyman GH. Lymphatic mapping and sentinel lymph node biopsy in early-stage breast carcinoma: a metaanalysis. Cancer. 2006;106:4–16.CrossRefPubMed Kim T, Giuliano AE, Lyman GH. Lymphatic mapping and sentinel lymph node biopsy in early-stage breast carcinoma: a metaanalysis. Cancer. 2006;106:4–16.CrossRefPubMed
14.
go back to reference Kitagawa Y, Fujii H, Mukai M, Kubota T, Ando N, Watanabe M, et al. The role of the sentinel lymph node in gastrointestinal cancer. Surg Clin North Am. 2000;80:1799–809.CrossRefPubMed Kitagawa Y, Fujii H, Mukai M, Kubota T, Ando N, Watanabe M, et al. The role of the sentinel lymph node in gastrointestinal cancer. Surg Clin North Am. 2000;80:1799–809.CrossRefPubMed
15.
go back to reference Arima H, Natsugoe S, Uenosono Y, Arigami T, Ehi K, Yanagita S, et al. Area of nodal metastasis and radioisotope uptake in sentinel nodes of upper gastrointestinal cancer. J Surg Res. 2006;135:250–4.CrossRefPubMed Arima H, Natsugoe S, Uenosono Y, Arigami T, Ehi K, Yanagita S, et al. Area of nodal metastasis and radioisotope uptake in sentinel nodes of upper gastrointestinal cancer. J Surg Res. 2006;135:250–4.CrossRefPubMed
16.
go back to reference Kato H, Miyazaki T, Nakajima M, Takita J, Sohda M, Fukai Y, et al. Sentinel lymph nodes with technetium-99m colloidal rhenium sulfide in patients with esophageal carcinoma. Cancer. 2003;98:932–9.CrossRefPubMed Kato H, Miyazaki T, Nakajima M, Takita J, Sohda M, Fukai Y, et al. Sentinel lymph nodes with technetium-99m colloidal rhenium sulfide in patients with esophageal carcinoma. Cancer. 2003;98:932–9.CrossRefPubMed
17.
go back to reference Kosugi S, Nakagawa S, Kanda T, Odano I, Yajima K, Kaneko K, et al. Radio-guided sentinel node mapping in patients with superficial esophageal carcinoma: feasibility study. Minim Invasive Ther Allied Technol. 2007;16:181–6.CrossRefPubMed Kosugi S, Nakagawa S, Kanda T, Odano I, Yajima K, Kaneko K, et al. Radio-guided sentinel node mapping in patients with superficial esophageal carcinoma: feasibility study. Minim Invasive Ther Allied Technol. 2007;16:181–6.CrossRefPubMed
18.
go back to reference Tanaka C, Fujii H, Kitagawa Y, Nakahara T, Suzuki T, Tanami Y, et al. Oblique view of preoperative lymphoscintigraphy improves detection of sentinel lymph nodes in esophageal cancer. Ann Nucl Med. 2005;19:719–23.CrossRefPubMed Tanaka C, Fujii H, Kitagawa Y, Nakahara T, Suzuki T, Tanami Y, et al. Oblique view of preoperative lymphoscintigraphy improves detection of sentinel lymph nodes in esophageal cancer. Ann Nucl Med. 2005;19:719–23.CrossRefPubMed
19.
go back to reference Yasuda S, Shimada H, Chino O, Tanaka H, Kenmochi T, Takechi M, et al. Sentinel lymph node detection with Tc-99m Tin colloids in patients with esophagogastric cancer. Jpn J Clin Oncol. 2003;33:68–72.CrossRefPubMed Yasuda S, Shimada H, Chino O, Tanaka H, Kenmochi T, Takechi M, et al. Sentinel lymph node detection with Tc-99m Tin colloids in patients with esophagogastric cancer. Jpn J Clin Oncol. 2003;33:68–72.CrossRefPubMed
20.
go back to reference van Hillegersberg R, Boone J, Draaisma WA, Broeders IA, Giezeman MJ, Borel Rinkes IH. First experience with robot-assisted thoracoscopic esophagolymphadenectomy for esophageal cancer. Surg Endosc. 2006;20:1435–9.CrossRefPubMed van Hillegersberg R, Boone J, Draaisma WA, Broeders IA, Giezeman MJ, Borel Rinkes IH. First experience with robot-assisted thoracoscopic esophagolymphadenectomy for esophageal cancer. Surg Endosc. 2006;20:1435–9.CrossRefPubMed
21.
go back to reference Boone J, Schipper ME, Moojen WA, Borel Rinkes IH, Cromheecke GJ, van Hillegersberg R. Robot-assisted thoracoscopic oesophagectomy for cancer. Br J Surg. 2009;96:878–86.CrossRefPubMed Boone J, Schipper ME, Moojen WA, Borel Rinkes IH, Cromheecke GJ, van Hillegersberg R. Robot-assisted thoracoscopic oesophagectomy for cancer. Br J Surg. 2009;96:878–86.CrossRefPubMed
22.
go back to reference Ovrebo KK, Lie SA, Laerum OD, Svanes K, Viste A. Long-term survival from adenocarcinoma of the esophagus after transthoracic and transhiatal esophagectomy. World J Surg Oncol. 2012;10:130.CrossRefPubMedPubMedCentral Ovrebo KK, Lie SA, Laerum OD, Svanes K, Viste A. Long-term survival from adenocarcinoma of the esophagus after transthoracic and transhiatal esophagectomy. World J Surg Oncol. 2012;10:130.CrossRefPubMedPubMedCentral
23.
go back to reference Fujii H, Kitagawa Y, Kitajima M, Kubo A. Sentinel nodes of malignancies originating in the alimentary tract. Ann Nucl Med. 2004;18:1–12.CrossRefPubMed Fujii H, Kitagawa Y, Kitajima M, Kubo A. Sentinel nodes of malignancies originating in the alimentary tract. Ann Nucl Med. 2004;18:1–12.CrossRefPubMed
24.
go back to reference Kitagawa Y, Ohgami M, Fujii H, Mukai M, Kubota T, Ando N, et al. Laparoscopic detection of sentinel lymph nodes in gastrointestinal cancer: a novel and minimally invasive approach. Ann Surg Oncol. 2001;8:86S–9S.PubMed Kitagawa Y, Ohgami M, Fujii H, Mukai M, Kubota T, Ando N, et al. Laparoscopic detection of sentinel lymph nodes in gastrointestinal cancer: a novel and minimally invasive approach. Ann Surg Oncol. 2001;8:86S–9S.PubMed
25.
go back to reference Bohanes T, Neoral C, Aujesky R, Vrba R, Klein J, Koranda P. Sentinel lymph node in esophageal cancer before neoadjuvant therapy. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2005;149:145–7.CrossRefPubMed Bohanes T, Neoral C, Aujesky R, Vrba R, Klein J, Koranda P. Sentinel lymph node in esophageal cancer before neoadjuvant therapy. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2005;149:145–7.CrossRefPubMed
26.
go back to reference Burian M, Stein HJ, Sendler A, Piert M, Nahrig J, Feith M, et al. Sentinel node detection in Barrett’s and cardia cancer. Ann Surg Oncol. 2004;11:255S–8S.CrossRefPubMed Burian M, Stein HJ, Sendler A, Piert M, Nahrig J, Feith M, et al. Sentinel node detection in Barrett’s and cardia cancer. Ann Surg Oncol. 2004;11:255S–8S.CrossRefPubMed
27.
go back to reference Lamb PJ, Griffin SM, Burt AD, Lloyd J, Karat D, Hayes N. Sentinel node biopsy to evaluate the metastatic dissemination of oesophageal adenocarcinoma. Br J Surg. 2005;92:60–7.CrossRefPubMed Lamb PJ, Griffin SM, Burt AD, Lloyd J, Karat D, Hayes N. Sentinel node biopsy to evaluate the metastatic dissemination of oesophageal adenocarcinoma. Br J Surg. 2005;92:60–7.CrossRefPubMed
28.
go back to reference Filip B, Scarpa M, Cavallin F, Alfieri R, Cagol M, Castoro C. Minimally invasive surgery for esophageal cancer: a review on sentinel node concept. Surg Endosc. 2014;28:1238–49.CrossRefPubMed Filip B, Scarpa M, Cavallin F, Alfieri R, Cagol M, Castoro C. Minimally invasive surgery for esophageal cancer: a review on sentinel node concept. Surg Endosc. 2014;28:1238–49.CrossRefPubMed
29.
go back to reference Kitagawa Y, Kitajima M. Gastrointestinal cancer and sentinel node navigation surgery. J Surg Oncol. 2002;79:188–93.CrossRefPubMed Kitagawa Y, Kitajima M. Gastrointestinal cancer and sentinel node navigation surgery. J Surg Oncol. 2002;79:188–93.CrossRefPubMed
30.
go back to reference Kitagawa Y, Fujii H, Mukai M, Kubota T, Ando N, Ozawa S, et al. Intraoperative lymphatic mapping and sentinel lymph node sampling in esophageal and gastric cancer. Surg Oncol Clin N Am. 2002;11:293–304.CrossRefPubMed Kitagawa Y, Fujii H, Mukai M, Kubota T, Ando N, Ozawa S, et al. Intraoperative lymphatic mapping and sentinel lymph node sampling in esophageal and gastric cancer. Surg Oncol Clin N Am. 2002;11:293–304.CrossRefPubMed
31.
go back to reference Aikou T, Kitagawa Y, Kitajima M, Uenosono Y, Bilchik AJ, Martinez SR, et al. Sentinel lymph node mapping with GI cancer. Cancer Metastasis Rev. 2006;25:269–77.CrossRefPubMed Aikou T, Kitagawa Y, Kitajima M, Uenosono Y, Bilchik AJ, Martinez SR, et al. Sentinel lymph node mapping with GI cancer. Cancer Metastasis Rev. 2006;25:269–77.CrossRefPubMed
32.
go back to reference Suga K, Shimizu K, Kawakami Y, Tangoku A, Zaki M, Matsunaga N, et al. Lymphatic drainage from esophagogastric tract: feasibility of endoscopic CT lymphography for direct visualization of pathways. Radiology. 2005;237:952–60.CrossRefPubMed Suga K, Shimizu K, Kawakami Y, Tangoku A, Zaki M, Matsunaga N, et al. Lymphatic drainage from esophagogastric tract: feasibility of endoscopic CT lymphography for direct visualization of pathways. Radiology. 2005;237:952–60.CrossRefPubMed
33.
go back to reference Hayashi H, Tangoku A, Suga K, Shimizu K, Ueda K, Yoshino S, et al. CT lymphography-navigated sentinel lymph node biopsy in patients with superficial esophageal cancer. Surgery. 2006;139:224–35.CrossRefPubMed Hayashi H, Tangoku A, Suga K, Shimizu K, Ueda K, Yoshino S, et al. CT lymphography-navigated sentinel lymph node biopsy in patients with superficial esophageal cancer. Surgery. 2006;139:224–35.CrossRefPubMed
34.
go back to reference Suga K, Yuan Y, Okada M, Matsunaga N, Tangoku A, Yamamoto S, et al. Breast sentinel lymph node mapping at CT lymphography with iopamidol: preliminary experience. Radiology. 2004;230:543–52.CrossRefPubMed Suga K, Yuan Y, Okada M, Matsunaga N, Tangoku A, Yamamoto S, et al. Breast sentinel lymph node mapping at CT lymphography with iopamidol: preliminary experience. Radiology. 2004;230:543–52.CrossRefPubMed
35.
go back to reference Suga K, Yuan Y, Ueda K, Kaneda Y, Kawakami Y, Zaki M, et al. Computed tomography lymphography with intrapulmonary injection of iopamidol for sentinel lymph node localization. Invest Radiol. 2004;39:313–24.CrossRefPubMed Suga K, Yuan Y, Ueda K, Kaneda Y, Kawakami Y, Zaki M, et al. Computed tomography lymphography with intrapulmonary injection of iopamidol for sentinel lymph node localization. Invest Radiol. 2004;39:313–24.CrossRefPubMed
36.
go back to reference Tangoku A, Yamamoto S, Suga K, Ueda K, Nagashima Y, Hida M, et al. Sentinel lymph node biopsy using computed tomography-lymphography in patients with breast cancer. Surgery. 2004;135:258–65.CrossRefPubMed Tangoku A, Yamamoto S, Suga K, Ueda K, Nagashima Y, Hida M, et al. Sentinel lymph node biopsy using computed tomography-lymphography in patients with breast cancer. Surgery. 2004;135:258–65.CrossRefPubMed
37.
go back to reference Imano H, Motoyama S, Saito R, Minamiya Y, Katayose Y, Okuyama M, et al. Superior mediastinal and neck lymphatic mapping in mid- and lower-thoracic esophageal cancer as defined by ferumoxides-enhanced magnetic resonance imaging. Jpn J Thorac Cardiovasc Surg. 2004;52:445–50.CrossRefPubMed Imano H, Motoyama S, Saito R, Minamiya Y, Katayose Y, Okuyama M, et al. Superior mediastinal and neck lymphatic mapping in mid- and lower-thoracic esophageal cancer as defined by ferumoxides-enhanced magnetic resonance imaging. Jpn J Thorac Cardiovasc Surg. 2004;52:445–50.CrossRefPubMed
38.
go back to reference Motoyama S, Ishiyama K, Maruyama K, Okuyama M, Sato Y, Hayashi K, et al. Preoperative mapping of lymphatic drainage from the tumor using ferumoxide-enhanced magnetic resonance imaging in clinical submucosal thoracic squamous cell esophageal cancer. Surgery. 2007;141:736–47.CrossRefPubMed Motoyama S, Ishiyama K, Maruyama K, Okuyama M, Sato Y, Hayashi K, et al. Preoperative mapping of lymphatic drainage from the tumor using ferumoxide-enhanced magnetic resonance imaging in clinical submucosal thoracic squamous cell esophageal cancer. Surgery. 2007;141:736–47.CrossRefPubMed
39.
go back to reference Ishiyama K, Motoyama S, Tomura N, Sashi R, Imano H, Ogawa J, et al. Visualization of lymphatic basin from the tumor using magnetic resonance lymphography with superparamagnetic iron oxide in patients with thoracic esophageal cancer. J Comput Assist Tomogr. 2006;30:270–5.CrossRefPubMed Ishiyama K, Motoyama S, Tomura N, Sashi R, Imano H, Ogawa J, et al. Visualization of lymphatic basin from the tumor using magnetic resonance lymphography with superparamagnetic iron oxide in patients with thoracic esophageal cancer. J Comput Assist Tomogr. 2006;30:270–5.CrossRefPubMed
40.
go back to reference Nishimura H, Tanigawa N, Hiramatsu M, Tatsumi Y, Matsuki M, Narabayashi I. Preoperative esophageal cancer staging: magnetic resonance imaging of lymph node with ferumoxtran-10, an ultrasmall superparamagnetic iron oxide. J Am Coll Surg. 2006;202:604–11.CrossRefPubMed Nishimura H, Tanigawa N, Hiramatsu M, Tatsumi Y, Matsuki M, Narabayashi I. Preoperative esophageal cancer staging: magnetic resonance imaging of lymph node with ferumoxtran-10, an ultrasmall superparamagnetic iron oxide. J Am Coll Surg. 2006;202:604–11.CrossRefPubMed
Metadata
Title
Sentinel node biopsy during thoracolaparoscopic esophagectomy for advanced esophageal cancer
Authors
Judith Boone
Monique G. G. Hobbelink
Marguerite E. I. Schipper
Frank P. Vleggaar
Inne H. M. Borel Rinkes
Robbert J. de Haas
Jelle P. Ruurda
Richard van Hillegersberg
Publication date
01-12-2016
Publisher
BioMed Central
Published in
World Journal of Surgical Oncology / Issue 1/2016
Electronic ISSN: 1477-7819
DOI
https://doi.org/10.1186/s12957-016-0866-9

Other articles of this Issue 1/2016

World Journal of Surgical Oncology 1/2016 Go to the issue