Abstract
Background
Lymphoadenectomy is a cornerstone of esophageal cancer treatment, and sentinel node (SN) biopsy (SNB) might provide surgeons with an extra tool to limit unnecessarily extended lymphadenectomy and to implement a minimally invasive approach. The aim of our study was to review all the available literature on the use of SNB in esophageal surgery for malignancy.
Methods
The review was conducted according to the PRISMA guidelines. A systematic search was performed in PubMed, EMBASE, and the Cochrane database to identify all original articles on the role of SNB in esophageal cancer. Data on methodologies, tumor stage and localization, and results were summarized and used to address relevant clinical questions related to the application of the SNB technique in esophageal cancer.
Results
Twelve studies were included, with a total of 492 patients. Different methods for SN identification were used (radionuclide, blue dye, computed tomography [CT] lymphography). The pooled values estimated using the random-effects model were, respectively: technetium-99 m overall detection rate (DR) 0.970 (95 % CI 0.814–0.996), accuracy (ACC) 0.902 (95 % CI 0.736–0.968); blue-dye DR 0.971 (95 % CI 0.890–0.993), ACC 0.790 (95 % CI 0.681–0.870); and CT lymphoscintigraphy DR 0.970 (95 % CI 0.814–0.996), ACC 0.902 (95 % CI 0.736–0.968).
Conclusion
Based on these results, the concept of SN in esophageal cancer is technically feasible with an acceptable DR and ACC, and it might be applicable in the event of early-stage adenocarcinoma of the gastroesophageal junction in patients with a high surgical risk or in a patient where an endoscopic resection is taken into consideration. Further studies focused on a single tumor type and localizations are needed in order to predict the correct utilization of this concept in minimally invasive treatment of esophageal cancer.
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References
Cuschieri A, Shimi S, Banting S (1992) Endoscopic oesophagectomy through a right thoracoscopic approach. J R Coll Surg Edinb 37(1):7–11
Briez N, Piessen G, Torres F, Lebuffe G, Triboulet JP, Mariette C (2012) Effects of hybrid minimally invasive oesophagectomy on major postoperative pulmonary complications. Br J Surg 99:1547–1553
Biere SSAY, van Berge Henegouwen MI, Maas KW et al (2012) Minimally invasive oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial. Lancet 379:1887–1892
Hulsher JBF, van Sandick JW, de Boer AGEM, Wijnhoven BP, Tijssen JG, Fockens P et al (2002) Extended transthoracic resection compared with limited transhiatal resection for adenocarcinoma of the esophagus. N Engl J Med 347:1662–1669
Omloo JM, Lagarde SM, Hulscher JB, Reitsma JB, Fockens P, van Dekken H et al (2007) Extended transthoracic resection compared with limited transhiatal resection for adenocarcinoma of the mid/distal esophagus: five-year survival of a randomized clinical trial. Ann Surg 246(6):992–1000
Altorki NK, Zhou XK, Stiles B, Port JL, Paul S, Lee PC et al (2008) Total number of resected lymph nodes predicts survival in esophageal cancer. Ann Surg 248:221–226
Gould EA, Winship T, Philbin PH, Kerr HH (1960) Observations on a ‘‘sentinel node’’ in cancer of the parotid. Cancer 13:77–78
Morton DL, Wen DR, Wong JH, Economou JS, Cagle LA, Storm FK et al (1992) Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg 127:392–399
Giuliano AE, Kirgan DM, Guenther JM, Morton DL (1994) Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 220:391–401
Morton DL, Thompson JF, Essner R, Stern SL, Nieweg OE, Roses DF et al (1999) Validation of the accuracy of intraoperative lymphatic mapping and sentinel lymphadenectomy for early stage melanoma: a multicenter trial. Multicenter Selective Lymphadenectomy Trial Group. Ann Surg 230:453–463
Krag D, Weaver D, Ashikaga T, Moffat F, Klimberg VS, Shriver C et al (1998) The sentinel node in breast cancer: a multicenter validation study. N Engl J Med 339:941–946
Bonenkamp JJ, Hermans J, Sasako M, van de Velde CJ, Welvaart K, Songun I et al (1999) Extended lymph-node dissection for gastric cancer. Dutch Gastric Cancer Group. N Engl J Med 340:908–914
Kitagawa Y, Saha S, Kubo A, Kitajima M (2007) Sentinel node for gastrointestinal malignancies. Surg Oncol Clin N Am 16:71–80
Siewert JR, Sendler A (2000) Potential and futility of sentinel node detection for gastric cancer. Recent Result Cancer Res 157:259–269
Rice TW (1999) Superficial oesophageal carcinoma: is there a need for three-field lymphadenectomy? Lancet 354:792–794
Hosch SB, Stoecklein NH, Pichlmeier U, Rehders A, Scheunemann P, Niendorf A et al (2001) Esophageal cancer: the mode of lymphatic tumor cell spread and its prognostic significance. J Clin Oncol 19:1970–1975
Dresner SM, Lamb PJ, Bennett MK, Hayes N, Griffin SM (2001) The pattern of metastatic lymph node dissemination from adenocarcinoma of the esophagogastric junction. Surgery 129:103–109
Ando N, Ozawa S, Kitagawa Y, Shinozawa Y, Kitajima M (2000) Improvement in the results of surgical treatment of advanced squamous esophageal carcinoma during 15 consecutive years. Ann Surg 232:225–232
Kitagawa Y, Fujii H, Mukai M, Kubota T, Ando N, Watanabe M et al (2000) The role of the sentinel lymph node in gastrointestinal cancer. Surg Clin N Am 80:1799–1809
Albertini JJ, Lyman GH, Cox C (1996) Lymphatic mapping and sentinel node biopsy in the patient with breast cancer. JAMA 276:1818–1822
Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339:b2535
Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283(15):2008–2012
Thompson SK, Bartholomeusz D, Jamieson GG (2011) Sentinel lymph node biopsy in esophageal cancer: should it be standard of care? J Gastrointest Surg 15(10):1762–1768
Uenosono Y, Arigami T, Yanagita S, Kozono T, Arima H, Hirata M et al (2011) Sentinel node navigation surgery is acceptable for clinical T1 and N0 esophageal cancer. Ann Surg Oncol 18(7):2003–2009
Bhat MA, Naikoo ZA, Dass TA, Lone RA, Dar AM (2010) Role of intraoperative sentinel lymph node mapping in the management of carcinoma of the esophagus. Saudi J Gastroenterol 16(3):168–173
Grotenhuis BA, Wijnhoven BP, van Marion R, van Dekken H, Hop WC, Tilanus HW et al (2009) The sentinel node concept in adenocarcinomas of the distal esophagus and gastroesophageal junction. J Thorac Cardiovasc Surg 138(3):608–612
Takeuchi H, Fujii H, Ando N, Ozawa S, Saikawa Y, Suda K et al (2009) Validation study of radio-guided sentinel lymph node navigation in esophageal cancer. Ann Surg 249(5):757–763
Lamb PJ, Griffin SM, Burt AD, Lloyd J, Karat D, Hayes N (2005) Sentinel node biopsy to evaluate the metastatic dissemination of oesophageal adenocarcinoma. Br J Surg 92(1):60–67
Kim HK, Kim S, Park JJ, Jeong JM, Mok YJ, Choi YH (2011) Sentinel node identification using technetium-99 m neomannosyl human serum albumin in esophageal cancer. Ann Thorac Surg 91(5):1517–1522
Hayashi H, Tangoku A, Suga K, Shimizu K, Ueda K, Yoshino S et al (2006) CT lymphography-navigated sentinel lymph node biopsy in patients with superficial esophageal cancer. Surgery 139(2):224–235
Burian M, Stein HJ, Sendler A, Piert M, Nährig J, Feith M et al (2004) Sentinel node detection in Barrett’s and cardia cancer. Ann Surg Oncol 11(3 Suppl):255S–258S
Kato H, Miyazaki T, Nakajima M, Takita J, Sohda M, Fukai Y et al (2003) Sentinel lymph nodes with technetium-99 m colloidal rhenium sulfide in patients with esophageal carcinoma. Cancer 98(5):932–939
Yasuda S, Shimada H, Chino O, Tanaka H, Kenmochi T, Takechi M et al (2003) Sentinel lymph node detection with Tc-99 m tin colloids in patients with esophagogastric cancer. Jpn J Clin Oncol 33(2):68–72
Yuasa Y, Seike J, Yoshida T, Takechi H, Yamai H, Yamamoto Y et al (2012) Sentinel lymph node biopsy using intraoperative indocyanine green fluorescence imaging navigated with preoperative CT lymphography for superficial esophageal cancer. Ann Surg Oncol 19(2):486–493
Aikou T, Kitagawa Y, Kitajima M, Uenosono Y, Bilchik AJ, Martinez SR et al (2006) Sentinel lymph node mapping with GI cancer. Cancer Metastasis Rev 25(2):269–277
Takeuchi H, Kitagawa Y (2011) Sentinel node navigation surgery in upper gastrointestinal cancer: what can it teach us? Ann Surg Oncol 18:1812–1813
van der Pas MH, Meijer S, Hoekstra OS, Riphagen II, de Vet HC, Knol DL et al (2011) Sentinel-lymph-node procedure in colon and rectal cancer:a systematic review and meta-analysis. Lancet Oncol 12:540–550
Wang Z, Dong ZY, Chen JQ, Liu JL (2012) Diagnostic value of sentinel lymph node biopsy in gastric cancer: a meta-analysis. Ann Surg Oncol 19:1541–1550
Kitagawa Y, Kitajima M (2002) Gastrointestinal cancer and sentinel node navigation surgery. J Surg Oncol 79:188–193
Hayashida T, Jinno H, Sakata M, Takayashi M, Onishi T, Seki H, Sato T, Nakahara T et al (2010) Superiority of radioisotope over blue dye for sentinel lymph node detection in breast cancer. Eur Surg Res 44:111–116
Hermansson M, DeMeester SR (2012) Management of stage 1 esophageal cancer. Surg Clin North Am 92(5):1155–1156
Choi J, Kim SG, Kim JS, Jung HC, Song IS (2010) Comparison of endoscopic ultrasonography (EUS), positron emission tomography (PET), and computed tomography (CT) in the preoperative locoregional staging of resectable esophageal cancer. Surg Endosc 24(6):1380–1386
Grotenhuis BA, van Heijl M, Zehetner J, Moons J, Wijnhoven BP, van Berge Henegouwen MI et al (2010) Surgical management of submucosal esophageal cancer: extended or regional lymphadenectomy? Ann Surg 252(5):823–830
Stein HJ, Feith M, Bruecher BL, Naehrig J, Sarbia M, Siewert JR (2005) Early esophageal cancer: pattern of lymphatic spread and prognostic factors for long-term survival after surgical resection. Ann Surg 242(4):566–573
Westerterp M, Koppert LB, Buskens CJ, Tilanus HW, ten Kate FJ, Bergman JJ et al (2005) Outcome of surgical treatment for early adenocarcinoma of the esophagus or gastro-esophageal junction. Virchows Arch 446(5):497–504
Endo M, Yoshino K, Kawano T, Nagai K, Inoue H (2000) Clinicopathologic analysis of lymph node metastasis in surgically resected superficial cancer of the thoracic esophagus. Dis Esophagus 13(2):125–129
Acknowledgments
The authors are very grateful to Dr. M. Apostolico, Clinical Librarian, Veneto Institute of Oncology, Padova, Italy, for his help in retrieving the studies and in defining the search strategy, and to Mrs Christina Drace for her kind help in the final editing of this manuscript.
Disclosure
This study was partially funded by an Italian Ministry of Health grant to Carlo Castoro, and a University of Medicine and Pharmacy Iasi grant (Project POSDRU /107/1.5/S/78702) to Bogdan Filip.
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Bogdan Filip and Marco Scarpa contributed equally to this study
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Filip, B., Scarpa, M., Cavallin, F. et al. Minimally invasive surgery for esophageal cancer: a review on sentinel node concept. Surg Endosc 28, 1238–1249 (2014). https://doi.org/10.1007/s00464-013-3314-8
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DOI: https://doi.org/10.1007/s00464-013-3314-8