Abstract
Background
Hiatal hernia (HH) and gastroesophageal reflux disease (GERD) are risk factors for esophageal adenocarcinoma. High positive margin rates and poor survival were described among HH patients undergoing esophagectomy. We sought to describe incidence and impact of HH on outcomes following esophagectomy.
Methods
Patients who underwent esophagectomy 2012–2019 for esophago-junctional carcinoma were included. CT studies were blindly reviewed by two radiologists. A third radiologist reviewed cases of disagreement. Hernias ≥ 3 cm were included in the HH group.
Results
Overall, 66 patients (33%) had HH ≥ 3 cm. The no hernia group included 12 patients (6%) with < 3 cm HH and 106 (53%) without HH. Preoperative variables were comparable among groups. Location of anastomosis was similar among cohorts and predominantly cervical (n = 97, 82.2% vs 61, 92.4%, p = 0.113). Postoperatively, HH patients had higher incidence of atrial dysrhythmia (n = 11, 16.7% vs n = 6, 5.1% p = 0.015). Rates of R0 resections were similar (n = 62, 93.9%, vs n = 113, 95.8%, p = 0.724). HH patients had higher rates of signet ring cell histology (n = 14, 21.2% vs n = 9, 7.6% p = 0.025); this was confirmed on subgroup analysis including only adenocarcinoma patients (n = 14, 28.6% vs n = 8, 12.3%, p = 0.042). On Cox regression analysis, HH was not associated with disease-free or overall survival (HR 1.308, p = 0.274 and HR .905, p = 0.722).
Conclusions
Patients with preoperative HH had higher rates of postoperative atrial dysrhythmias and signet ring cell features on pathology. In a population with predominant cervical anastomosis, positive margin rates were low and survival comparable among cohorts.
Similar content being viewed by others
Data Availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
H. Pohl, B. Sirovich, H.G. Welch, Esophageal Adenocarcinoma Incidence: Are We Reaching the Peak?, Cancer Epidemiology and Prevention Biomarkers. 19 (2010) 1468–1470. https://doi.org/10.1158/1055-9965.EPI-10-0012.
B. Njei, T.R. Mccarty, J.W. Birk, Trends in esophageal cancer survival in United States adults from 1973 to 2009: A SEER database analysis, Journal of Gastroenterology and Hepatology (Australia). 31 (2016) 1141–1146. https://doi.org/10.1111/jgh.13289.
M. Arnold, I. Soerjomataram, J. Ferlay, D. Forman, Global incidence of oesophageal cancer by histological subtype in 2012, Gut. 64 (2015) 381–387. https://doi.org/10.1136/gutjnl-2014-308124.
Esophageal Cancer — Cancer Stat Facts, (n.d.). https://seer.cancer.gov/statfacts/html/esoph.html (accessed February 17, 2022).
J. Lagergren, R. Bergström, A. Lindgren, O. Nyrén, Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma, N Engl J Med. 340 (1999) 825–831. https://doi.org/10.1056/NEJM199903183401101.
A.H. Wu, C.C. Tseng, L. Bernstein, Hiatal hernia, reflux symptoms, body size, and risk of esophageal and gastric adenocarcinoma, Cancer. 98 (2003) 940–948. https://doi.org/10.1002/cncr.11568.
T. Fukuchi, K. Hirasawa, C. Sato, M. Makazu, H. Kaneko, R. Kobayashi, M. Nishio, R. Ikeda, A. Sawada, Y. Ozeki, M. Sugimori, Y. Inayama, Y. Tateishi, S. Maeda, Potential roles of gastroesophageal reflux in patients with superficial esophageal squamous cell carcinoma without major causative risk factors, J Gastroenterol. 56 (2021) 891–902. https://doi.org/10.1007/S00535-021-01815-X/FIGURES/4.
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.-J.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, 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 (2015) 1090–1098. https://doi.org/10.1016/S1470-2045(15)00040-6.
R.J. Kelly, J.A. Ajani, J. Kuzdzal, T. Zander, E. van Cutsem, G. Piessen, G. Mendez, J. Feliciano, S. Motoyama, A. Lièvre, H. Uronis, E. Elimova, C. Grootscholten, K. Geboes, S. Zafar, S. Snow, A.H. Ko, K. Feeney, M. Schenker, P. Kocon, J. Zhang, L. Zhu, M. Lei, P. Singh, K. Kondo, J.M. Cleary, M. Moehler, Adjuvant Nivolumab in Resected Esophageal or Gastroesophageal Junction Cancer, N Engl J Med. 384 (2021) 1191–1203. https://doi.org/10.1056/NEJMOA2032125.
N. McMillian, M.A. Lenora Pluchino, J.A. Ajani, T.A. D, V. Chair, D.J. Bentrem, J. Chao, D. Cooke, C. Corvera, P. Das, P.C. Enzinger, T. Enzler, P. Fanta, F. Farjah, H. Gerdes, M. Gibson, S. Hochwald, W.L. Hofstetter, D.H. Ilson, R.N. Keswani, S. Kim, L.R. Kleinberg, S. Klempner, J. Lacy, Q.P. Ly, P. Buffett, K.A. Matkowskyj, M. McNamara, D. Outlaw, H. Park, K.A. Perry, J. Pimiento, G.A. Poultsides, S. Reznik, R.E. Roses, V.E. Strong, S. Su, H.L. Wang, G. Wiesner, C.G. Willett, D. Yakoub, S. Jude, H. Yoon, NCCN Guidelines Version 2.2022 Esophageal and Esophagogastric Junction Cancers Continue NCCN, (2022). https://www.nccn.org/home/. Accessed 10 Jun 2023.
A. Gandon, C. Gronnier, F. Renaud, P. Borde, M. Vanderbeken, F. Hec, G. Piessen, A. Adenis, X. Mirabel, C. Mariette, Esophageal adenocarcinoma impact of a large hiatal hernia on outcomes after surgery, Ann Surg. 264 (2016) 862–870. https://doi.org/10.1097/SLA.0000000000001769.
W. Ouyang, C. Dass, H. Zhao, C. Kim, G. Criner, Multiplanar MDCT measurement of esophageal hiatus surface area: association with hiatal hernia and GERD., Surg Endosc. 30 (2015) 2465–2472. https://doi.org/10.1007/S00464-015-4499-9.
M.G. Patti, H.I. Goldberg, M. Arcerito, L. Bortolasi, J. Tong, L.W. Way, Hiatal hernia size affects lower esophageal sphincter function, esophageal acid exposure, and the degree of mucosal injury, Am J Surg. 171 (1996) 182–186. https://doi.org/10.1016/S0002-9610(99)80096-8.
D.E. Low, M.K. Kuppusamy, D. Alderson, I. Cecconello, A.C. Chang, G. Darling, A. Davies, X.B. D’Journo, S.S. Gisbertz, S.M. Griffin, R. Hardwick, A. Hoelscher, W. Hofstetter, B. Jobe, Y. Kitagawa, S. Law, C. Mariette, N. Maynard, C.R. Morse, P. Nafteux, M. Pera, C.S. Pramesh, S. Puig, J. v. Reynolds, W. Schroeder, M. Smithers, B.P.L. Wijnhoven, Benchmarking Complications Associated with Esophagectomy, Ann Surg. 269 (2019) 291–298. https://doi.org/10.1097/SLA.0000000000002611.
D. Dindo, N. Demartines, P.A. Clavien, Classification of surgical complications: A new proposal with evaluation in a cohort of 6336 patients and results of a survey, Ann Surg. 240 (2004) 205–213. https://doi.org/10.1097/01.sla.0000133083.54934.ae.
S.E. Al-Batran, N. Homann, C. Pauligk, T.O. Goetze, J. Meiler, S. Kasper, H.G. Kopp, F. Mayer, G.M. Haag, K. Luley, U. Lindig, W. Schmiegel, M. Pohl, J. Stoehlmacher, G. Folprecht, S. Probst, N. Prasnikar, W. Fischbach, R. Mahlberg, J. Trojan, M. Koenigsmann, U.M. Martens, P. Thuss-Patience, M. Egger, A. Block, V. Heinemann, G. Illerhaus, M. Moehler, M. Schenk, F. Kullmann, D.M. Behringer, M. Heike, D. Pink, C. Teschendorf, C. Löhr, H. Bernhard, G. Schuch, V. Rethwisch, L.F. von Weikersthal, J.T. Hartmann, M. Kneba, S. Daum, K. Schulmann, J. Weniger, S. Belle, T. Gaiser, F.S. Oduncu, M. Güntner, W. Hozaeel, A. Reichart, E. Jäger, T. Kraus, S. Mönig, W.O. Bechstein, M. Schuler, H. Schmalenberg, R.D. Hofheinz, Perioperative chemotherapy with fluorouracil plus leucovorin, oxaliplatin, and docetaxel versus fluorouracil or capecitabine plus cisplatin and epirubicin for locally advanced, resectable gastric or gastro-oesophageal junction adenocarcinoma (FLOT4): a randomised, phase 2/3 trial, The Lancet. 393 (2019) 1948–1957. https://doi.org/10.1016/S0140-6736(18)32557-1.
D. Cunningham, W.H. Allum, S.P. Stenning, J.N. Thompson, C.J.H. van de Velde, M. Nicolson, J.H. Scarffe, F.J. Lofts, S.J. Falk, T.J. Iveson, D.B. Smith, R.E. Langley, M. Verma, S. Weeden, Y.J. Chua, null MAGIC Trial Participants, Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer, N Engl J Med. 355 (2006) 11–20. https://doi.org/10.1056/NEJMoa055531.
T. Rice, D. Patil, E.B.-A. of cardiothoracic surgery, undefined 2017, AJCC/UICC staging of cancers of the esophagus and esophagogastric junction: application to clinical practice, Ncbi.Nlm.Nih.Gov. (n.d.). https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5387145/ (accessed February 26, 2022).
F. Hvid-Jensen, L. Pedersen, A.M. Drewes, H.T. Sørensen, P. Funch-Jensen, Incidence of Adenocarcinoma among Patients with Barrett’s Esophagus, (2011). https://www-nejm-org.beilinson-ez.medlcp.tau.ac.il/doi/10.1056/NEJMoa1103042. Accessed 10 Jun 2023.
S.M. Wang, N.D. Freedman, H.A. Katki, C. Matthews, B.I. Graubard, L.L. Kahle, C.C. Abnet, Gastroesophageal reflux disease: A risk factor for laryngeal squamous cell carcinoma and esophageal squamous cell carcinoma in the NIH-AARP Diet and Health Study cohort, Cancer. 127 (2021) 1871–1879. https://doi.org/10.1002/CNCR.33427.
Å. Åkerlund, I. Hernia diaphragmatica hiatus oesophagei vom anatomischen und rontgenologischen gesichtspunkt, Acta Radiol. 6 (1926) 3–22. https://doi.org/10.3109/00016922609139467.
P.J. Kahrilas, J.E. Pandolfino, Hiatus hernia, GI Motility Online, Published Online: 16 May 2006; |. (2006). https://doi.org/10.1038/GIMO48.
S. WL, S. I, G. GA, G. HC, L. DF, Hiatal hernia and gastroesophageal reflux. A clinicoradiological analysis of more than 1,000 cases, Radiology. 93 (1969) 163–165. https://doi.org/10.1148/93.6.1323.
J. Kim, G.T. Hiura, E.C. Oelsner, X. Yin, R.G. Barr, B.M. Smith, M.R. Prince, Hiatal hernia prevalence and natural history on non-contrast CT in the Multi-Ethnic Study of Atherosclerosis (MESA), BMJ Open Gastroenterol. 8 (2021). https://doi.org/10.1136/BMJGAST-2020-000565.
K. Uno, K. Iijima, W. Hatta, T. Koike, Y. Abe, N. Asano, G. Kusaka, T. Shimosegawa, Direct measurement of gastroesophageal reflux episodes in patients with squamous cell carcinoma by 24-h pH-impedance monitoring, Am J Gastroenterol. 106 (2011) 1923–1929. https://doi.org/10.1038/ajg.2011.282.
M. Kgomo, T.R. Mokoena, J.A. Ker, Non-acid gastro-oesophageal reflux is associated with squamous cell carcinoma of the oesophagus, BMJ Open Gastroenterol. 4 (2017) e000180. https://doi.org/10.1136/bmjgast-2017-000180.
T. Miyashita, K. Miwa, T. Fujimura, I. Ninomiya, S. Fushida, F.A. Shah, J.W. Harmon, T. Hattori, T. Ohta, The severity of duodeno-esophageal reflux influences the development of different histological types of esophageal cancer in a rat model, Int J Cancer. 132 (2013) 1496–1504. https://doi.org/10.1002/ijc.27824.
J.D. Luketich, A. Pennathur, Y. Franchetti, P.J. Catalano, S. Swanson, D.J. Sugarbaker, A. de Hoyos, M.A. Maddaus, N.T. Nguyen, A.B. Benson, H.C. Fernando, Minimally invasive esophagectomy: results of a prospective phase II multicenter trial-the eastern cooperative oncology group (E2202) study, Ann Surg. 261 (2015) 702–707. https://doi.org/10.1097/SLA.0000000000000993.
Y. Nagatsuka, K. Sugimura, H. Miyata, N. Shinnno, K. Asukai, H. Hara, S. Hasegawa, D. Yamada, K. Yamamoto, N. Haraguchi, J. Nishimura, M. Motoori, H. Wada, H. Takahashi, M. Yasui, T. Omori, M. Ohue, M. Yano, Predictive value of preoperative echocardiographic assessment for postoperative atrial fibrillation after esophagectomy for esophageal cancer, Esophagus. 18 (2021) 496–503. https://doi.org/10.1007/S10388-020-00804-Y.
L. te Chen, B. bin Li, C.Y. Jiang, G.S. Fu, Impact of Minimally Invasive Esophagectomy in Post-Operative Atrial Fibrillation and Long-Term Mortality in Patients Among Esophageal Cancer, Cancer Control. 27 (2020). https://doi.org/10.1177/1073274820974013.
M.K. Kuppusamy, D.E. Low, Evaluation of International Contemporary Operative Outcomes and Management Trends Associated With Esophagectomy, Ann Surg. 275 (2022) 515–525. https://doi.org/10.1097/SLA.0000000000004309.
J.E. Tisdale, H.A. Jaynes, M.R. Watson, A.L. Corya, C. Shen, K.A. Kesler, Amiodarone for prevention of atrial fibrillation following esophagectomy, J Thorac Cardiovasc Surg. 158 (2019) 301-310.e1. https://doi.org/10.1016/J.JTCVS.2019.01.095.
L.R. van der Werf, L.A.D. Busweiler, J.W. van Sandick, M.I. van Berge Henegouwen, B.P.L. Wijnhoven, Reporting National Outcomes After Esophagectomy and Gastrectomy According to the Esophageal Complications Consensus Group (ECCG), Ann Surg. 271 (2020) 1095–1101. https://doi.org/10.1097/SLA.0000000000003210.
L. Fei, G. del Genio, L. Brusciano, V. Esposito, D. Cuttitta, F. Pizza, G. Rossetti, V. Trapani, G. Filippone, M. Francesco, A. del Genio, Crura ultrastructural alterations in patients with hiatal hernia: A pilot study, Surgical Endoscopy and Other Interventional Techniques. 21 (2007) 907–911. https://doi.org/10.1007/s00464-006-9043-5.
L. Haverkamp, M.F.J. Seesing, J.P. Ruurda, J. Boone, R. van Hillegersberg, Worldwide trends in surgical techniques in the treatment of esophageal and gastroesophageal junction cancer, Dis Esophagus. 30 (2017) 1–7. https://doi.org/10.1111/DOTE.12480.
K.O. Turner, R.M. Genta, A. Sonnenberg, Oesophageal signet ring cell carcinoma as complication of gastro-oesophageal reflux disease, Aliment Pharmacol Ther. 42 (2015) 1222–1231. https://doi.org/10.1111/APT.13395.
K. Maezato, T. Nishimaki, M. Oshiro, T. Yamashiro, H. Sasaki, Y. Sashida, Signet-ring cell carcinoma of the esophagus associated with Barrett’s epithelium: report of a case, Surg Today. 37 (2007) 1096–1101. https://doi.org/10.1007/S00595-007-3533-5.
S. Szachnowics, I. Cecconello, U. Ribeiro, K. Iriya, R. el Ibrahim, F.R. Takeda, C.E.P. Corbett, A. Vaz Safatle-Ribeiro, Mucin pattern reflects the origin of the adenocarcinoma in Barrett’s esophagus: A retrospective clinical and laboratorial study, World J Surg Oncol. 7 (2009) 1–8. https://doi.org/10.1186/1477-7819-7-27/TABLES/3.
E.M. Corsini, W.C. Foo, K.G. Mitchell, N. Zhou, D.M. Maru, J.A. Ajani, W.L. Hofstetter, A.M. Correa, M.B. Antonoff, S.H. Lin, R.J. Mehran, R. Rajaram, D.C. Rice, J.A. Roth, B. Sepesi, S.G. Swisher, A.A. Vaporciyan, G.L. Walsh, Esophageal adenocarcinoma with any component of signet ring cells portends poor prognosis and response to neoadjuvant therapy, Journal of Thoracic and Cardiovascular Surgery. (2020). https://doi.org/10.1016/j.jtcvs.2020.08.108.
S. Bekkar, C. Gronnier, M. Messager, W.B. Robb, G. Piessen, C. Mariette, A. Dhari, J.M. Regimbeau, J.P. Arnaud, D. Brachet, S. Michalak, G. Luc, D. Collet, F. Peschaud, P. Dechelotte, R. Flamein, B. Gillet, B. Mathieu, D. Pezet, M. Guilbert, E. Leteurtre, A. Poisson, F. Vandois, O. Glehen, J.Y. Mabrut, V. Pichot-Delahaye, J.R. Delpero, X.B. D’Journo, J. Guiramand, P.A. Thomas, A. Glaise, B. Millat, J.M. Balon, S. Fabre, F. Borie, M. Prudhomme, J.H. Lefevre, F. Paye, M. Pocard, B. Meunier, F. Michot, B. Tsilividis, C. Brigand, M. Fernandez, N. Carrere, N. Huten, K. Kraft, D. Goéré, A. Souadka, The impact of preoperative radiochemotherapy on survival in advanced esophagogastric junction signet ring cell adenocarcinoma, Annals of Thoracic Surgery. 97 (2014) 303–310. https://doi.org/10.1016/j.athoracsur.2013.09.010.
F. Scheufele, T. Vogel, M. Gasiorek, A. Novotny, H. Friess, I.E. Demir, S. Schorn, Serum albumin at resection predicts in-hospital death, while serum lactate and aPTT on the first postoperative day anticipate anastomotic leakage after Ivor-Lewis-esophagectomy, Langenbecks Arch Surg. 407 (2022) 2309–2317. https://doi.org/10.1007/S00423-022-02510-Y/FIGURES/2.
S. Matsuda, H. Takeuchi, K. Fukuda, R. Nakamura, T. Takahashi, N. Wada, H. Kawakubo, Y. Saikawa, T. Omori, Y. Kitagawa, Clinical significance of fibrinogen and albumin score for postoperative recurrence in esophageal cancer patients.,. 32 (2014) 14–14. https://doi.org/10.1200/JCO.2014.32.3_SUPPL.14.
S.L. Goh, R.P. De Silva, K. Dhital, R.M. Gett, Is low serum albumin associated with postoperative complications in patients undergoing oesophagectomy for oesophageal malignancies?, Interact Cardiovasc Thorac Surg. 20 (2015) 107–113. https://doi.org/10.1093/ICVTS/IVU324.
Author information
Authors and Affiliations
Contributions
AZ and DS contributed to conception and study design of the research; data acquisition, analysis and interpretation; manuscript drafting. Both approved the final version.
DV, TI, and YA contributed to data acquisition, manuscript revision, and approved the final version.
ST and HK contributed to study conception and design, revised the manuscript, and approved the final version.
Corresponding authors
Ethics declarations
Disclosure
The authors have no interests to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This research work was presented at the 2022 World Congress for Esophageal Diseases on September 26th, 2022.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zaslavsky, A., Solomon, D., Varon, D. et al. Incidence and Impact of Preoperative Hiatal Hernia in Patients with Esophageal Carcinoma Undergoing Curative Surgical Resection. J Gastrointest Surg 27, 2907–2919 (2023). https://doi.org/10.1007/s11605-023-05872-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11605-023-05872-w