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Oligometastatic Adenocarcinoma of the Esophagus: Current Understanding, Diagnosis, and Therapeutic Strategies

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Oligometastatic Adenocarcinoma of the Esophagus: Current Understanding, Diagnosis, and Therapeutic Strategies cancers Review Oligometastatic Adenocarcinoma of the Esophagus: Current Understanding, Diagnosis, and Therapeutic Strategies Michael P. Rogers 1 , Anthony J. DeSantis 1 and Christopher G. DuCoin 2,* 1 Department of Surgery, Morsani College of Medicine, University of South Florida, Tampa, FL 33606, USA; [email protected] (M.P.R.); [email protected] (A.J.D.) 2 Department of Surgery, Division of Gastrointestinal Surgery, Morsani College of Medicine, University of South Florida, Tampa, FL 33606, USA * Correspondence: [email protected] Simple Summary: The diagnosis and management of oligometastatic esophageal adenocarcinoma remains nuanced. Early diagnosis may allow for prompt intervention and, ideally, prolonged patient survival. As recent and emerging trials shed new light on this topic, we sought to identify the current understanding and treatment recommendations for oligometastatic disease by performing a thorough review of the available literature. Abstract: Esophageal adenocarcinoma is an aggressive cancer of increasing incidence and is associ- ated with poor prognosis. The early recognition of synchronous and metachronous oligometastasis in esophageal adenocarcinoma may allow for prompt intervention and potentially improved survival. However, curative approaches to oligometastatic esophageal disease remain unproven and may represent an area of emerging divergence of opinion for surgical and medical oncologists. We sought to identify the current understanding and evidence for management of oligometastatic esophageal Citation: Rogers, M.P.; DeSantis, A.J.; adenocarcinoma by performing a thorough review of the available literature. DuCoin, C.G. Oligometastatic Adenocarcinoma of the Esophagus: Keywords: esophageal adenocarcinoma; esophageal cancer; oligometastasis Current Understanding, Diagnosis, and Therapeutic Strategies. Cancers 2021, 13, 4352. https://doi.org/ 10.3390/cancers13174352 1. Introduction Esophageal adenocarcinoma (EA) comprises up to 80% of esophageal cancer in the Academic Editor: Alexander Quaas United States and is a major cause of cancer morbidity and mortality worldwide [1]. While esophageal squamous cell carcinoma has been declining in the United States and Received: 2 July 2021 in other parts of the western world, EA incidence has experienced a five-fold increase Accepted: 22 August 2021 Published: 28 August 2021 over the last four decades [2]. The five-year overall survival rate from 2009–2015 was 19.9%, with patients without lymph node involvement experiencing significantly better Publisher’s Note: MDPI stays neutral prognosis than those with involved lymph nodes [3]. Although surgical resection remains with regard to jurisdictional claims in the mainstay treatment, survival is poor due to the high incidence of locoregional or distant published maps and institutional affil- metastasis [4–6]. Accordingly, a multimodal approach of neoadjuvant chemoradiotherapy iations. (i.e., cT1b-T4a, N0-N+ staged patients) or perioperative chemotherapy alone (i.e., cT4b staged patients) has become the standard of care [7,8]. While oncologic outcomes have improved with multimodal therapy, five-year survival rates continue to give cancer spe- cialists pause. This poor prognosis has highlighted the need for refinements in current treatment practices and pursuits of novel understandings in tumor biology, microenviron- Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. ment, invasion tactics, and metastatic potential. The early identification and treatment of This article is an open access article oligometastatic esophageal adenocarcinoma represents one such strategy. distributed under the terms and Though no exact definition exists, oligometastatic disease is generally characterized conditions of the Creative Commons by a state of limited metastatic burden of less than five metastases, and can be detected at Attribution (CC BY) license (https:// the time of primary cancer diagnosis, so-called synchronous oligometastasis, or detected creativecommons.org/licenses/by/ following treatment of the primary tumor, known as metachronous oligometastasis [9,10]. 4.0/). Whether this state represents an intermediate step in widespread metastasis or is a distinct Cancers 2021, 13, 4352. https://doi.org/10.3390/cancers13174352 https://www.mdpi.com/journal/cancers Cancers 2021, 13, x FOR PEER REVIEW 2 of 11 Cancers 2021, 13, 4352 2 of 11 Whether this state represents an intermediate step in widespread metastasis or is a distinct molecular metastatic pattern remains debatable [11]. Regardless, the potential for im- provedmolecular survival metastatic outcomes pattern with remains early detection, debatable and [11 thus]. Regardless,earlier treatment, the potential is of significant for im- interest.proved survivalMetastatic outcomes esophag witheal disease early detection, is largely and regarded thus earlier as an end treatment,-stage condition is of significant, with manyinterest. patients Metastatic offered esophageal palliative diseasetherapy. is Consequently, largely regarded the as ability an end-stage to detect condition, and intervene with priormany to patients widespread offered metastatic palliative burden therapy. remains Consequently, a topic of the significant ability to detectresearch. and Currently, intervene noprior consens to widespreadus treatment metastatic guidelines burden exist remains for oligometastatic a topic of significant esophageal research. cancer, Currently, mainly dueno consensusto the paucity treatment of large guidelines randomized exist control for oligometastatic trial data in this esophagealcohort. We sought cancer, to mainly iden- tifydue the to current the paucity understanding, of large randomized diagnostic controltools, and trial treatment data in thismodalities cohort. available We sought in o tol- identify the current understanding, diagnostic tools, and treatment modalities available igometastatic esophageal adenocarcinoma by performing a thorough review of the avail- in oligometastatic esophageal adenocarcinoma by performing a thorough review of the able literature. available literature. 2.2. Methods Methods AA comprehensive comprehensive review review of of the the available available literature literature was was performed performed on on 30 30 May May 2021, 2021, usingusing PubMed, PubMed, Cochrane Cochrane Library, Library, MEDLINE MEDLINE,, and and EMBASE EMBASE databases. databases. Search Search terms terms in- cludedincluded the the following: following: “oligometastatic “oligometastatic esophageal esophageal adenocarcinoma”, adenocarcinoma”, “oligometastasis”, “oligometasta- “esophagealsis”, “esophageal cancer cancer oligometastasis”, oligometastasis”, “esophageal “esophageal adenocarcinoma adenocarcinoma oligometastasis”, oligometastasis”, “ol- igometastatic“oligometastatic gastroesophageal gastroesophageal adenocarcinoma” adenocarcinoma”,, and and “oligometastatic “oligometastatic esophageal esophageal can- can- cer”.cer”. Articles Articles were were limited limited to to those those published published in in English and German. Given Given the the relative scarcityscarcity of of available available literature, literature, search search results’ results’ references references were were thoroughly reviewed for possiblepossible inclusion inclusion to to ensure ensure the the maximal maximal amount amount of of available available information information was was captured. captured. AvailableAvailable results were manually reviewed reviewed thoroughly thoroughly for for relevance relevance and and included included retro- retro- spectivespective observational observational studies, studies, prospective prospective multicenter multicenter trials, trials, an ongoing an ongoing prospective prospective ran- domizedrandomized trial, trial, and and a systematic a systematic revi reviewew of ofthe the available available literature. literature. Duplicate Duplicate results results and and thosethose unrelated unrelated to to the the subject subject matter matter were were eliminated eliminated from from further further review. review. Though Though not not a systematica systematic review, review, screening screening and and eligibility eligibility for for inclusion inclusion of of relevant relevant studies followed standardstandard PRISMA PRISMA guidelines guidelines (Figure (Figure 11).). FigureFigure 1. 1. FlowFlow chart chart of selection of selection strategy strategy for included for included reviewed reviewed manuscripts manuscripts following followingPRISMA guidelines.PRISMA guidelines. 3. Discussion Cancers 2021, 13, 4352 3 of 11 3. Discussion 3.1. Diagnostic Approaches General diagnostic approaches to esophageal carcinoma with suspected oligometas- tases follow the traditional work-up strategy when staging esophageal cancer. Depth of tumor invasion and nodal involvement are the best predictors of long-term survival and an important determinant of therapeutic approach, making thorough initial staging essential to optimize patient outcome. Endoscopy and tissue biopsy remain the initial steps, with careful documentation of tumor location, length, extent of circumferential involvement, and presence of associated Barrett’s esophagus of vital importance [12]. Additionally, en- doscopic ultrasound (EUS) is generally recommended to aid in assessing tumor depth and nodal staging. The diagnostic yield is increased when EUS is combined with fine-needle aspiration (FNA) when evaluating lymph node metastasis [13]. The potential presence of synchronous or metachronous double primary malignancies
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