Advertisement

Robotic Esophagectomy Compared With Open Esophagectomy Reduces Sarcopenia within the First Postoperative Year: A Propensity Score-Matched Analysis

  • Felix Merboth
    Affiliations
    Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany

    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany
    Search for articles by this author
  • Heiner Nebelung
    Affiliations
    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany

    Institute and Polyclinic for Diagnostic and Interventional Radiology, University Hospital Carl Gustav Carus, Technical University Dresden, Dresden, Germany
    Search for articles by this author
  • Natalie Wotschel
    Affiliations
    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany

    Institute and Polyclinic for Diagnostic and Interventional Radiology, University Hospital Carl Gustav Carus, Technical University Dresden, Dresden, Germany
    Search for articles by this author
  • Hendrik Liebscher
    Affiliations
    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany

    Institute and Polyclinic for Diagnostic and Interventional Radiology, University Hospital Carl Gustav Carus, Technical University Dresden, Dresden, Germany
    Search for articles by this author
  • Franziska Eckert
    Affiliations
    Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany

    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany
    Search for articles by this author
  • Janusz von Renesse
    Affiliations
    Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany

    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany
    Search for articles by this author
  • Jasmin Hasanovic
    Affiliations
    Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany

    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany
    Search for articles by this author
  • Thilo Welsch
    Affiliations
    Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany

    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany

    Current Address: Department of General, Visceral, and Thoracic Surgery, St. Elisabethen-Klinikum Ravensburg, Academic Teaching Hospital of the University of Ulm, Ulm, Germany
    Search for articles by this author
  • Johannes Fritzmann
    Affiliations
    Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany

    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany
    Search for articles by this author
  • Daniel E. Stange
    Affiliations
    Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany

    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany
    Search for articles by this author
  • Verena Plodeck
    Affiliations
    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany

    Institute and Polyclinic for Diagnostic and Interventional Radiology, University Hospital Carl Gustav Carus, Technical University Dresden, Dresden, Germany
    Search for articles by this author
  • Ralf-Thorsten Hoffmann
    Affiliations
    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany

    Institute and Polyclinic for Diagnostic and Interventional Radiology, University Hospital Carl Gustav Carus, Technical University Dresden, Dresden, Germany
    Search for articles by this author
  • Marius Distler
    Affiliations
    Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany

    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany
    Search for articles by this author
  • Jürgen Weitz
    Affiliations
    Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany

    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany
    Search for articles by this author
  • Johanna Kirchberg
    Correspondence
    Corresponding author Address for correspondence: Johanna Kirchberg, MD, Department of Visceral, Thoracic and Vascular Surgery, University Hospital and Faculty of Medicine Carl Gustav Carus, Technical University Dresden Fetscherstraße 74, 01307 Dresden, Germany.
    Affiliations
    Department of Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany

    National Center for Tumor Diseases (NCT/UCC), Dresden, Germany: German Cancer Research Center (DKFZ), Heidelberg, Germany; Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany; Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Dresden, Germany
    Search for articles by this author
Published:November 04, 2022DOI:https://doi.org/10.1016/j.jtho.2022.10.018

      Abstract

      Introduction

      Sarcopenia is a known risk factor for adverse outcomes after esophageal cancer (EC) surgery. Robot-assisted minimally invasive esophagectomy (RAMIE) offers numerous advantages, including reduced morbidity and mortality. However, no evidence exists to date comparing the development of sarcopenia after RAMIE and open esophagectomy (OE). The objective was to evaluate whether the development of sarcopenia within the first postoperative year after esophagectomy is associated with the surgical approach: RAMIE versus OE.

      Methods

      A total of 168 patients with EC were analyzed who either underwent total robotic or fully open Ivor Lewis esophagectomy in a propensity score-matched analysis. Sarcopenia was assessed using the skeletal muscle index (cm2/m2) and psoas muscle thickness per height (mm/m) on axial computed tomography scans during the first postoperative year; in total 540 computed tomography scans were evaluated.

      Results

      After 1-to-1 propensity score matching for confounders, 67 patients were allocated to RAMIE and OE groups, respectively. Skeletal muscle index in the OE group was significantly lower compared with the RAMIE group at the third (43.2 ± 7.6 cm2/m2 versus 49.1 ± 6.9 cm2/m2, p = 0.001), sixth (42.7 ± 7.8 cm2/m2 versus 51.5 ± 8.2 cm2/m2, p < 0.001) and ninth (43.0 ± 7.0 cm2/m2 versus 49.9 ± 6.6 cm2/m2, p = 0.015) postoperative month. Similar results were recorded for psoas muscle thickness per height.

      Conclusions

      To our knowledge, this study is the first to suggest a substantial benefit of RAMIE compared with open esophagectomy in terms of postoperative sarcopenia. These results add further evidence to support the implementation of the robotic approach in multimodal therapy of EC.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of Thoracic Oncology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Bray F.
        • Ferlay J.
        • Soerjomataram I.
        • Siegel R.L.
        • Torre L.A.
        • Jemal A.
        Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
        CA Cancer J Clin. 2018; 68: 394-424
        • Anandavadivelan P.
        • Lagergren P.
        Cachexia in patients with oesophageal cancer.
        Nat Rev Clin Oncol. 2016; 13: 185-198
        • Prado C.M.
        • Cushen S.J.
        • Orsso C.E.
        • Ryan A.M.
        Sarcopenia and cachexia in the era of obesity: clinical and nutritional impact.
        Proc Nutr Soc. 2016; 75: 188-198
        • Ryan A.M.
        • Power D.G.
        • Daly L.
        • Cushen S.J.
        • Ní Bhuachalla Ē
        • Prado C.M.
        Cancer-associated malnutrition, cachexia and sarcopenia: the skeleton in the hospital closet 40 years later.
        Proc Nutr Soc. 2016; 75: 199-211
        • von Haehling S.
        • Morley J.E.
        • Anker S.D.
        An overview of sarcopenia: facts and numbers on prevalence and clinical impact.
        J Cachexia Sarcopenia Muscle. 2010; 1: 129-133
        • Boshier P.R.
        • Heneghan R.
        • Markar S.R.
        • Baracos V.E.
        • Low D.E.
        Assessment of body composition and sarcopenia in patients with esophageal cancer: a systematic review and meta-analysis.
        Dis Esophagus. 2018; 31https://doi.org/10.1093/dote/doy047
        • Chen L.K.
        • Woo J.
        • Assantachai P.
        • et al.
        Consensus update on sarcopenia diagnosis and treatment.
        J Am Med Dir Assoc. 2019; 21: 300-307.e302
        • Cruz-Jentoft A.J.
        • Bahat G.
        • Bauer J.
        • et al.
        Sarcopenia: revised European consensus on definition and diagnosis.
        Age Ageing. 2019; 48: 16-31
        • Prado C.M.
        • Lieffers J.R.
        • McCargar L.J.
        • et al.
        Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study.
        Lancet Oncol. 2008; 9: 629-635
        • Durand F.
        • Buyse S.
        • Francoz C.
        • et al.
        Prognostic value of muscle atrophy in cirrhosis using psoas muscle thickness on computed tomography.
        J Hepatol. 2014; 60: 1151-1157
        • Kawakita Y.
        • Motoyama S.
        • Sato Y.
        • et al.
        Decreases in the psoas muscle index correlate more strongly with survival than other prognostic markers in esophageal cancer after neoadjuvant chemoradiotherapy plus esophagectomy.
        World J Surg. 2020; 44: 1559-1568
        • Zhang S.
        • Tan S.
        • Jiang Y.
        • et al.
        Sarcopenia as a predictor of poor surgical and oncologic outcomes after abdominal surgery for digestive tract cancer: a prospective cohort study.
        Clin Nutr. 2019; 38: 2881-2888
        • Tan B.H.
        • Birdsell L.A.
        • Martin L.
        • Baracos V.E.
        • Fearon K.C.
        Sarcopenia in an overweight or obese patient is an adverse prognostic factor in pancreatic cancer.
        Clin Cancer Res. 2009; 15: 6973-6979
        • Cruz-Jentoft A.J.
        • Baeyens J.P.
        • Bauer J.M.
        • et al.
        Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People.
        Age Ageing. 2010; 39: 412-423
        • Gu D.H.
        • Kim M.Y.
        • Seo Y.S.
        • et al.
        Clinical usefulness of psoas muscle thickness for the diagnosis of sarcopenia in patients with liver cirrhosis.
        Clin Mol Hepatol. 2018; 24: 319-330
        • Lordick F.
        • Mariette C.
        • Haustermans K.
        • Obermannová R.
        • Arnold D.
        • ESMO Guidelines Committee
        Oesophageal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up.
        Ann Oncol. 2016; 27: v50-v57
        • Low D.E.
        • Kuppusamy M.K.
        • Alderson D.
        • et al.
        Benchmarking complications associated with esophagectomy.
        Ann Surg. 2019; 269: 291-298
        • Wang P.Y.
        • Xu L.D.
        • Chen X.K.
        • et al.
        Sarcopenia and short-term outcomes after esophagectomy: a meta-analysis.
        Ann Surg Oncol. 2020; 27: 3041-3051
        • Elliott J.A.
        • Doyle S.L.
        • Murphy C.F.
        • et al.
        Sarcopenia: prevalence, and impact on operative and oncologic outcomes in the multimodal management of locally advanced esophageal cancer.
        Ann Surg. 2017; 266: 822-830
        • Boshier P.R.
        • Klevebro F.
        • Jenq W.
        • et al.
        Long-term variation in skeletal muscle and adiposity in patients undergoing esophagectomy.
        Dis Esophagus. 2021; 34: doab016
        • Mariette C.
        • Markar S.R.
        • Dabakuyo-Yonli T.S.
        • et al.
        Hybrid minimally invasive esophagectomy for esophageal cancer.
        N Engl J Med. 2019; 380: 152-162
        • van der Sluis P.C.
        • van der Horst S.
        • May A.M.
        • et al.
        Robot-assisted minimally invasive thoracolaparoscopic esophagectomy versus open transthoracic esophagectomy for resectable esophageal cancer: a randomized controlled trial.
        Ann Surg. 2019; 269: 621-630
        • Merboth F.
        • Hasanovic J.
        • Stange D.
        • et al.
        [Change of strategy to minimally invasive esophagectomy-Results at a certified center].
        Chirurgie (Heidelb). 2022; 93: 694-701
        • Al-Batran S.E.
        • Homann N.
        • Pauligk C.
        • et al.
        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.
        Lancet. 2019; 393: 1948-1957
        • Shapiro J.
        • van Lanschot JJB
        • Hulshof M.
        • et al.
        Neoadjuvant chemoradiotherapy plus surgery versus surgery alone for oesophageal or junctional cancer (CROSS): long-term results of a randomised controlled trial.
        Lancet Oncol. 2015; 16: 1090-1098
        • Kelly R.J.
        • Ajani J.A.
        • Kuzdzal J.
        • et al.
        Adjuvant nivolumab in resected esophageal or gastroesophageal junction cancer.
        N Engl J Med. 2021; 384: 1191-1203
        • Grimminger P.P.
        • Hadzijusufovic E.
        • Ruurda J.P.
        • Lang H.
        • van Hillegersberg R.
        The da VINCI Xi robotic four-arm approach for robotic-assisted minimally invasive esophagectomy.
        Thorac Cardiovasc Surg. 2018; 66: 407-409
        • Yoshida S.
        • Nishigori T.
        • Tsunoda S.
        • et al.
        Chronological changes in skeletal muscle mass two years after minimally invasive esophagectomy: a prospective cohort study.
        Surg Endosc. 2022; 36: 1527-1535
        • Deng H.Y.
        • Zha P.
        • Peng L.
        • Hou L.
        • Huang K.L.
        • Li X.Y.
        Preoperative sarcopenia is a predictor of poor prognosis of esophageal cancer after esophagectomy: a comprehensive systematic review and meta-analysis.
        Dis Esophagus. 2019; 32: doy115
        • Grotenhuis B.A.
        • Shapiro J.
        • van Adrichem S.
        • et al.
        Sarcopenia/muscle mass is not a prognostic factor for short- and long-term outcome after esophagectomy for cancer.
        World J Surg. 2016; 40: 2698-2704
        • van Meerten E.
        • Muller K.
        • Tilanus H.W.
        • et al.
        Neoadjuvant concurrent chemoradiation with weekly paclitaxel and carboplatin for patients with oesophageal cancer: a phase II study.
        Br J Cancer. 2006; 94: 1389-1394
        • van Hagen P.
        • Hulshof M.C.
        • van Lanschot J.J.
        • et al.
        Preoperative chemoradiotherapy for esophageal or junctional cancer.
        N Engl J Med. 2012; 366: 2074-2084
        • Babic B.
        • Tagkalos E.
        • Gockel I.
        • et al.
        C-reactive protein levels after esophagectomy are associated with increased surgical trauma and complications.
        Ann Thorac Surg. 2020; 109: 1574-1583
        • Scarpa M.
        • Cavallin F.
        • Saadeh L.M.
        • et al.
        Hybrid minimally invasive esophagectomy for cancer: impact on postoperative inflammatory and nutritional status.
        Dis Esophagus. 2016; 29: 1064-1070
        • Scheepers J.J.
        • Sietses C.
        • Bos D.G.
        • et al.
        Immunological consequences of laparoscopic versus open transhiatal resection for malignancies of the distal esophagus and gastroesophageal junction.
        Dig Surg. 2008; 25: 140-147
        • Tan J.T.
        • Zhong J.H.
        • Yang Y.
        • et al.
        Comparison of postoperative immune function in patients with thoracic esophageal cancer after video-assisted thoracoscopic surgery or conventional open esophagectomy.
        Int J Surg. 2016; 30: 155-160
        • Tuttle C.S.L.
        • Thang L.A.N.
        • Maier A.B.
        Markers of inflammation and their association with muscle strength and mass: a systematic review and meta-analysis.
        Ageing Res Rev. 2020; 64101185
        • Wolk S.
        • Linke S.
        • Bogner A.
        • et al.
        Use of activity tracking in major visceral surgery-the enhanced perioperative mobilization trial: a randomized controlled trial.
        J Gastrointest Surg. 2019; 23: 1218-1226
        • Dirks M.L.
        • Wall B.T.
        • Snijders T.
        • Ottenbros C.L.
        • Verdijk L.B.
        • van Loon L.J.
        Neuromuscular electrical stimulation prevents muscle disuse atrophy during leg immobilization in humans.
        Acta Physiol (Oxf). 2014; 210: 628-641
        • Chen L.
        • Sun L.
        • Lang Y.
        • et al.
        Fast-track surgery improves postoperative clinical recovery and cellular and humoral immunity after esophagectomy for esophageal cancer.
        BMC Cancer. 2016; 16: 449
        • Triantafyllou T.
        • Olson M.T.
        • Theodorou D.
        • Schizas D.
        • Singhal S.
        Enhanced recovery pathways vs standard care pathways in esophageal cancer surgery: systematic review and meta-analysis.
        Esophagus. 2020; 17: 100-112
        • Paternostro R.
        • Lampichler K.
        • Bardach C.
        • et al.
        The value of different CT-based methods for diagnosing low muscle mass and predicting mortality in patients with cirrhosis.
        Liver Int. 2019; 39: 2374-2385
        • Ryan A.M.
        • Reynolds J.V.
        • Healy L.
        • et al.
        Enteral nutrition enriched with eicosapentaenoic acid (EPA) preserves lean body mass following esophageal cancer surgery: results of a double-blinded randomized controlled trial.
        Ann Surg. 2009; 249: 355-363
        • Baldwin C.
        • Spiro A.
        • Ahern R.
        • Emery P.W.
        Oral nutritional interventions in malnourished patients with cancer: a systematic review and meta-analysis.
        J Natl Cancer Inst. 2012; 104: 371-385
        • Park S.Y.
        • Yoon J.K.
        • Lee S.J.
        • Haam S.
        • Jung J.
        Postoperative change of the psoas muscle area as a predictor of survival in surgically treated esophageal cancer patients.
        J Thorac Dis. 2017; 9: 355-361
        • Nakashima Y.
        • Saeki H.
        • Hu Q.
        • et al.
        Skeletal muscle loss after esophagectomy is an independent risk factor for patients with esophageal cancer.
        Ann Surg Oncol. 2020; 27: 492-498
        • Mayanagi S.
        • Tsubosa Y.
        • Omae K.
        • et al.
        Negative impact of skeletal muscle wasting after neoadjuvant chemotherapy followed by surgery on survival for patients with thoracic esophageal cancer.
        Ann Surg Oncol. 2017; 24: 3741-3747
        • Takahashi K.
        • Watanabe M.
        • Kozuki R.
        • et al.
        Prognostic significance of skeletal muscle loss during early postoperative period in elderly patients with esophageal cancer.
        Ann Surg Oncol. 2019; 26: 3727-3735
        • Matsui K.
        • Kawakubo H.
        • Hirata Y.
        • et al.
        Relationship between early postoperative change in total psoas muscle area and long-term prognosis in esophagectomy for patients with esophageal cancer.
        Ann Surg Oncol. 2021; 28: 6378-6387
        • Nose Y.
        • Yamashita K.
        • Takeoka T.
        • et al.
        Perioperative ghrelin administration attenuates postoperative skeletal muscle loss in patients undergoing esophagectomy for esophageal cancer: secondary analysis of a randomized controlled trial.
        Ann Surg Oncol. 2022; 29: 3604-3612