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A Novel Frailty Grade Combined with Cachexia Index and Osteopenia in Esophagectomy

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Abstract

Backgrounds

The optimal method for evaluating frailty grade in patients with cancer has not been established in patients undergoing esophagectomy for esophageal cancer. This study aimed to clarify the impact of cachexia index (CXI) and osteopenia on survival in esophagectomized patients for esophageal cancer to develop frailty grade for risk stratification of the prognosis.

Methods

A total of 239 patients who underwent esophagectomy were analyzed. CXI was calculated as follows: skeletal muscle index × serum albumin/neutrophil-to-lymphocyte ratio. Meanwhile, osteopenia was defined as below the cutoff value of bone mineral density (BMD) calculated by the receiver operating characteristic curve. We evaluated the average Hounsfield unit within a circle in the lower midvertebral core of the 11th thoracic vertebra on preoperative computed tomography as BMD.

Results

Multivariate analysis revealed that low CXI (Hazard ratio [HR], 1.95; 95% confidence interval [CI], 1.25–3.04) and osteopenia (HR, 1.86; 95% CI, 1.19–2.93) were independent prognostic factors for overall survival. Meanwhile, low CXI (HR, 1.58; 95% CI, 1.06–2.34) and osteopenia (HR, 1.57; 95% CI, 1.05–2.36) were also significant prognostic factors for relapse-free survival. A frailty grade combined with CXI and osteopenia stratified into four groups by their prognosis.

Conclusions

Low CXI and osteopenia predict poor survival in patients undergoing esophagectomy for esophageal cancer. Furthermore, a novel frailty grade combined with CXI and osteopenia stratified the patients into four groups according to their prognosis.

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References

  1. Sung H, Ferlay J, Siegel RL et al (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA:Cancer J Clin 71(3):209–249

    PubMed  Google Scholar 

  2. Fujita T, Sato K, Ozaki A et al (2022) Propensity-matched analysis of the short-term outcome of robot-assisted minimally invasive esophagectomy versus conventional thoracoscopic esophagectomy in thoracic esophageal cancer. World J Surg 46:1926–1933. https://doi.org/10.1007/s00268-022-06567-0

    Article  PubMed  Google Scholar 

  3. Yoshida N, Yamamoto H, Baba H et al (2020) Can minimally invasive esophagectomy replace open esophagectomy for esophageal cancer? latest analysis of 24,233 esophagectomies from the japanese national clinical database. Ann Surg 272:118–124

    Article  PubMed  Google Scholar 

  4. Argilés JM, Busquets S, Stemmler B et al (2014) Cancer cachexia: understanding the molecular basis. Nat Rev Cancer 14:754–762

    Article  PubMed  Google Scholar 

  5. Sugimura K, Miyata H, Kanemura T et al (2022) Impact of preoperative skeletal muscle mass and physical performance on short-term and long-term postoperative outcomes in patients with esophageal cancer after esophagectomy. Ann Gastroenterol surg 6:623–632

    Article  PubMed  PubMed Central  Google Scholar 

  6. Abe T, Oshikiri T, Goto H et al (2022) Albumin-derived NLR score is a novel prognostic marker for esophageal squamous cell carcinoma. Ann Surg Oncol 29:2663–2671

    Article  PubMed  Google Scholar 

  7. Hamura R, Haruki K, Shirai Y et al (2022) Preoperative cachexia index can predict the prognosis of extrahepatic biliary tract cancer after resection. Surg Oncol 44:101825

    Article  PubMed  Google Scholar 

  8. Verschueren S, Gielen E, O’Neill TW et al (2013) Sarcopenia and its relationship with bone mineral density in middle-aged and elderly European men. Osteoporos Int 24:87–98

    Article  CAS  PubMed  Google Scholar 

  9. Zofková I (2008) Hormonal aspects of the muscle-bone unit. Physiol Res 57(Suppl 1):S159-169

    Article  PubMed  Google Scholar 

  10. Takahashi K, Nishikawa K, Furukawa K et al (2021) Prognostic significance of preoperative osteopenia in patients undergoing esophagectomy for esophageal cancer. World J Surg 45:3119–3128. https://doi.org/10.1007/s00268-021-06199-w

    Article  PubMed  Google Scholar 

  11. Brierley JDGM, Wittekind C (2016) TNM classification of malignant tumours, 8th edn. Wiley, New York

    Google Scholar 

  12. Kitagawa Y, Uno T, Oyama T et al (2019) Esophageal cancer practice guidelines 2017 edited by the Japan Esophageal Society: part 1. Esophagus 16:1–24

    Article  PubMed  Google Scholar 

  13. Sharma P, Parikh ND, Yu J et al (2016) Bone mineral density predicts posttransplant survival among hepatocellular carcinoma liver transplant recipients. Liver Transpl 22:1092–1098

    Article  PubMed  PubMed Central  Google Scholar 

  14. Kanda Y (2013) Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transpl 48:452–458

    Article  CAS  Google Scholar 

  15. Hou YC, Wang CJ, Chao YJ et al (2018) Elevated serum interleukin-8 level correlates with cancer-related cachexia and sarcopenia: an indicator for pancreatic cancer outcomes. J Clin Med 7(12):502

    Article  PubMed  PubMed Central  Google Scholar 

  16. Ábrigo J, Elorza AA, Riedel CA et al (2018) Role of oxidative stress as key regulator of muscle wasting during cachexia. Oxid Med Cell Longev 2018:2063179

    Article  PubMed  PubMed Central  Google Scholar 

  17. Narsale AA, Carson JA (2014) Role of interleukin-6 in cachexia: therapeutic implications. Curr Opin Support Palliat Care 8:321–327

    Article  PubMed  PubMed Central  Google Scholar 

  18. Brenner DA, Buck M, Feitelberg SP et al (1990) Tumor necrosis factor-alpha inhibits albumin gene expression in a murine model of cachexia. J Clin Investig 85:248–255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Grivennikov SI, Greten FR, Karin M (2010) Immunity, inflammation, and cancer. Cell 140:883–899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Zurlo IV, Schino M, Strippoli A et al (2022) Predictive value of NLR, TILs (CD4+/CD8+) and PD-L1 expression for prognosis and response to preoperative chemotherapy in gastric cancer. Cancer Immunol, Immunother: CII 71:45–55

    Article  CAS  PubMed  Google Scholar 

  21. Sun Y, Zhang Y, Huang Z et al (2020) Combination of preoperative plasma fibrinogen and neutrophil-to-lymphocyte ratio (the F-NLR score) as a prognostic marker of locally advanced rectal cancer following preoperative chemoradiotherapy. World J Surg 44:1975–1984. https://doi.org/10.1007/s00268-020-05407-3

    Article  PubMed  Google Scholar 

  22. de Jong MC, Mihai R, Khan S (2021) Neutrophil-to-lymphocyte ratio (NLR) and platelet-to-lymphocyte ratio (PLR) as possible prognostic markers for patients undergoing resection of adrenocortical carcinoma. World J Surg 45:754–764. https://doi.org/10.1007/s00268-020-05868-6

    Article  PubMed  Google Scholar 

  23. Jones DH, Nakashima T, Sanchez OH et al (2006) Regulation of cancer cell migration and bone metastasis by RANKL. Nature 440:692–696

    Article  CAS  PubMed  Google Scholar 

  24. Morony S, Capparelli C, Sarosi I et al (2001) Osteoprotegerin inhibits osteolysis and decreases skeletal tumor burden in syngeneic and nude mouse models of experimental bone metastasis. Cancer Res 61:4432–4436

    CAS  PubMed  Google Scholar 

  25. Roodman GD, Dougall WC (2008) RANK ligand as a therapeutic target for bone metastases and multiple myeloma. Cancer Treat Rev 34:92–101

    Article  CAS  PubMed  Google Scholar 

  26. D’Journo XB, Ouattara M, Loundou A et al (2012) Prognostic impact of weight loss in 1-year survivors after transthoracic esophagectomy for cancer. Dis Esophagus 25:527–534

    Article  CAS  PubMed  Google Scholar 

  27. Zanello SB, Collins ED, Marinissen MJ et al (1997) Vitamin D receptor expression in chicken muscle tissue and cultured myoblasts. Horm Metab Res 29:231–236

    Article  CAS  PubMed  Google Scholar 

  28. Pfeifer M, Begerow B, Minne HW (2002) Vitamin D and muscle function. Osteoporos Int 13:187–194

    Article  CAS  PubMed  Google Scholar 

  29. Lips P, van Schoor NM (2011) The effect of vitamin D on bone and osteoporosis. Best Pract Res Clin Endocrinol Metab 25:585–591

    Article  CAS  PubMed  Google Scholar 

  30. Deeb KK, Trump DL, Johnson CS (2007) Vitamin D signalling pathways in cancer: potential for anticancer therapeutics. Nat Rev Cancer 7:684–700

    Article  CAS  PubMed  Google Scholar 

  31. Müller K, Odum N, Bendtzen K (1993) 1,25-dihydroxyvitamin D3 selectively reduces interleukin-2 levels and proliferation of human T cell lines in vitro. Immunol Lett 35:177–182

    Article  PubMed  Google Scholar 

  32. Gurlek A, Pittelkow MR, Kumar R (2002) Modulation of growth factor/cytokine synthesis and signaling by 1alpha,25-dihydroxyvitamin D(3): implications in cell growth and differentiation. Endocr Rev 23:763–786

    Article  CAS  PubMed  Google Scholar 

  33. Cheng SH, Chen KH, Chen C et al (2021) The optimal strategy of vitamin d for sarcopenia: a network meta-analysis of randomized controlled trials. Nutrients 13(10):3589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

KT designed this research, acquired the data, and drafted this article. All authors read and approved the final manuscript.

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Authors and Affiliations

  1. Department of Gastrointestinal Surgery, Jikei University School of Medicine, 3-25-8 Nishishimbashi, Minato-ku, Tokyo, 105-8461, Japan

    Keita Takahashi, Takahiro Masuda, Yoshitaka Ishikawa, Yuichiro Tanishima, Takanori Kurogochi, Masami Yuda, Yujiro Tanaka, Akira Matsumoto, Fumiaki Yano & Ken Eto

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  1. Keita Takahashi
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  2. Takahiro Masuda
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  3. Yoshitaka Ishikawa
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  4. Yuichiro Tanishima
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  5. Takanori Kurogochi
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  6. Masami Yuda
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  7. Yujiro Tanaka
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Correspondence to Keita Takahashi.

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There is no conflict of interest.

Ethical approval

The Ethics Committee in the Jikei University School of Medicine approved this study (33–303). The need for informed consent was waived because of the retrospective design of the study. All methods were performed in accordance with the ethical standards of the institutional review board of ethical committee with the Helsinki Declaration.

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Takahashi, K., Masuda, T., Ishikawa, Y. et al. A Novel Frailty Grade Combined with Cachexia Index and Osteopenia in Esophagectomy. World J Surg 47, 1503–1511 (2023). https://doi.org/10.1007/s00268-023-06942-5

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