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Effect of low skeletal muscle mass on NK cells in patients with acute myeloid leukemia and its correlation with prognosis

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Abstract

The objective of this study was to analyze the correlation between skeletal muscle mass and the distribution of peripheral blood lymphocytes and natural killer (NK) cells, as well as their impact on prognosis in patients with acute myeloid leukemia (AML). A retrospective analysis was conducted on 211 newly diagnosed AML patients, evaluating skeletal muscle index (SMI), NK cell proportion, and absolute value, along with relevant clinical data. Linear regression and Spearman’s correlation coefficient were used to assess the relationship between various indicators and SMI, followed by multiple linear regression for further modeling. Univariate and multivariate Cox proportional hazards regression models were used to identify independent predictors for overall survival (OS). Among the 211 AML patients, 38 cases (18.0%) were diagnosed with sarcopenia. Multiple linear regression analysis included weight, fat mass, ECOG score, body mass index, and peripheral blood NK cell proportion, constructing a correlation model for SMI (R2 = 0.745). Univariate analysis identified higher NK cell count (> 9.53 × 106/L) as a poor predictor for OS. Multivariate Cox proportional hazards regression model indicated that age ≥ 60 years, PLT < 100 × 109/L, ELN high risk, sarcopenia, and B cell count > 94.6 × 106/L were independent adverse prognostic factors for AML patients. Low skeletal muscle mass may negatively impact the count and function of NK cells, thereby affecting the prognosis of AML. However, further basic and clinical research is needed to explore the specific mechanisms underlying the relationship between NK cells and SMI in AML.

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References

  1. Williams GR, Dunne RF, Giri S, Shachar SS, Caan BJ (2021) Sarcopenia in the older adult with cancer. J Clin Oncol 39:2068–2078. https://doi.org/10.1200/JCO.21.00102

    Article  PubMed  PubMed Central  Google Scholar 

  2. Sun Q, Cui JL, Liu WJ, Li JY, Hong M, Qian SX (2022) The prognostic value of sarcopenia in acute myeloid leukemia patients and the development and validation of a novel nomogram for predicting survival. Front Oncol 12:828939. https://doi.org/10.3389/fonc.2022.828939

    Article  PubMed  PubMed Central  Google Scholar 

  3. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H et al (2017) WHO classification of tumours of haematopoietic and lymphoid tissues. International Agency for Research on Cancer, Lyon

    Google Scholar 

  4. Hong M, Zhu H, Sun Q, Zhu Y, Miao Y, Yang H, Qiu HR, Li JY, Qian SX (2020) Decitabine in combination with low-dose cytarabine, aclarubicin and G-CSF tends to improve prognosis in elderly patients with high-risk AML. Aging (Albany NY) 12:5792–5811. https://doi.org/10.18632/aging.102973

    Article  CAS  PubMed  Google Scholar 

  5. Dohner H, Estey E, Grimwade D, Amadori S, Appelbaum FR, Buchner T et al (2017) Diagnosis and management of AML in adults: 2017 ELN recommendations from an international expert panel. Blood 129:424–447. https://doi.org/10.1182/blood-2016-08-733196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Liu L, Chen X, Jin HM, Zhao SS, Zhu Y, Qian SX, Wu YJ (2022) The expression and function of NK cells in patients with acute myeloid leukemia. Zhongguo Shi Yan Xue Ye Xue Za Zhi 30:49–55. https://doi.org/10.19746/j.cnki.issn.1009-2137.2022.01.009

    Article  PubMed  Google Scholar 

  7. Zeng P, Wu S, Han Y, Liu J, Zhang Y, Zhang E, Zhang Y, Gong H, Pang J, Tang Z, Liu H, Zheng X, Zhang T (2015) Differences in body composition and physical functions associated with sarcopenia in Chinese elderly: reference values and prevalence. Arch Gerontol Geriatr 60:118–123. https://doi.org/10.1016/j.archger.2014.08.010

    Article  PubMed  Google Scholar 

  8. Liu JM, Zheng XY, Zhang YD, Li Z, Fang LD, He WH, Tang QY (2006). Development of a body composition measuring instrument for Chinese individuals. 2006 National Academic Symposium on Sports Equipment and Sports System Simulation, China, pp 122–126

  9. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, Schneider SM, Sieber CC, Topinkova E, Vandewoude M, Visser M, Zamboni M, Writing Group for the European Working Group on Sarcopenia in Older P and the Extended Group for E (2019) Sarcopenia revised European consensus on definition and diagnosis. Age Ageing 48:601. https://doi.org/10.1093/ageing/afz046

    Article  PubMed  PubMed Central  Google Scholar 

  10. Jung J, Lee E, Shim H, Park JH, Eom HS, Lee H (2021) Prediction of clinical outcomes through assessment of sarcopenia and adipopenia using computed tomography in adult patients with acute myeloid leukemia. Int J Hematol 114:44–52. https://doi.org/10.1007/s12185-021-03122-w

    Article  CAS  PubMed  Google Scholar 

  11. Aguilar OA (2023) X chromosome enhances NK cell responses. Trends Genet 39:596–597. https://doi.org/10.1016/j.tig.2023.05.003

    Article  CAS  PubMed  Google Scholar 

  12. Cheng MI, Li JH, Riggan L, Chen B, Tafti RY, Chin S, Ma F, Pellegrini M, Hrncir H, Arnold AP, O’Sullivan TE, Su MA (2023) The X-linked epigenetic regulator UTX controls NK cell-intrinsic sex differences. Nat Immunol 24:780–791. https://doi.org/10.1038/s41590-023-01463-8

    Article  CAS  PubMed  Google Scholar 

  13. Lion E, Willemen Y, Berneman ZN, Van Tendeloo VF, Smits EL (2012) Natural killer cell immune escape in acute myeloid leukemia. Leukemia 26:2019–2026. https://doi.org/10.1038/leu.2012.87

    Article  CAS  PubMed  Google Scholar 

  14. Carlsten M, Jaras M (2019) Natural killer cells in myeloid malignancies: immune surveillance, NK cell dysfunction, and pharmacological opportunities to bolster the endogenous NK cells. Front Immunol 10:2357. https://doi.org/10.3389/fimmu.2019.02357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Yang F, Wang R, Feng W, Chen C, Yang X, Wang L, Hu Y, Ren Q, Zheng G (2018) Characteristics of NK cells from leukemic microenvironment in MLL-AF9 induced acute myeloid leukemia. Mol Immunol 93:68–78. https://doi.org/10.1016/j.molimm.2017.11.003

    Article  CAS  PubMed  Google Scholar 

  16. Aggarwal N, Swerdlow SH, TenEyck SP, Boyiadzis M, Felgar RE (2016) Natural killer cell (NK) subsets and NK-like T-cell populations in acute myeloid leukemias and myelodysplastic syndromes. Cytometry B Clin Cytom 90:349–357. https://doi.org/10.1002/cyto.b.21349

    Article  CAS  PubMed  Google Scholar 

  17. Kiladjian JJ, Bourgeois E, Lobe I, Braun T, Visentin G, Bourhis JH, Fenaux P, Chouaib S, Caignard A (2006) Cytolytic function and survival of natural killer cells are severely altered in myelodysplastic syndromes. Leukemia 20:463–470. https://doi.org/10.1038/sj.leu.2404080

    Article  CAS  PubMed  Google Scholar 

  18. Nakajima H, Zhao R, Lund TC, Ward J, Dolan M, Hirsch B, Miller JS (2002) The BCR/ABL transgene causes abnormal NK cell differentiation and can be found in circulating NK cells of advanced phase chronic myelogenous leukemia patients. J Immunol 168:643–650. https://doi.org/10.4049/jimmunol.168.2.643

    Article  CAS  PubMed  Google Scholar 

  19. Sopper S, Mustjoki S, Gjertsen BT, Giles F, Hochhaus A, Janssen J, Porkka K, Wolf D (2017) NK cell dynamics and association with molecular response in early chronic phase chronic myelogenous leukemia (CML-CP) patients treated with nilotinib. Leukemia 31:2264–2267. https://doi.org/10.1038/leu.2017.235

    Article  CAS  PubMed  Google Scholar 

  20. Kaweme NM, Zhou F (2021) Optimizing NK cell-based immunotherapy in myeloid leukemia: abrogating an immunosuppressive microenvironment. Front Immunol 12:683381. https://doi.org/10.3389/fimmu.2021.683381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. D’Silva SZ, Singh M, Pinto AS (2023) NK cell defects: implication in acute myeloid leukemia. Front Immunol 14:1112059. https://doi.org/10.3389/fimmu.2023.1112059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Jamal E, Azmy E, Ayed M, Aref S, Eisa N (2020) Clinical impact of percentage of natural killer cells and natural killer-like T cell population in acute myeloid leukemia. J Hematol 9:62–70. https://doi.org/10.14740/jh655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Pedersen BK (2011) Muscles and their myokines. J Exp Biol 214:337–346. https://doi.org/10.1242/jeb.048074

    Article  CAS  PubMed  Google Scholar 

  24. Lutz CT, Quinn LS (2012) Sarcopenia, obesity, and natural killer cell immune senescence in aging: altered cytokine levels as a common mechanism. Aging (Albany NY) 4:535–46. https://doi.org/10.18632/aging.100482

    Article  CAS  PubMed  Google Scholar 

  25. Kennedy MK, Glaccum M, Brown SN, Butz EA, Viney JL, Embers M, Matsuki N, Charrier K, Sedger L, Willis CR, Brasel K, Morrissey PJ, Stocking K, Schuh JC, Joyce S, Peschon JJ (2000) Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 191:771–780. https://doi.org/10.1084/jem.191.5.771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Koka R, Burkett PR, Chien M, Chai S, Chan F, Lodolce JP, Boone DL, Ma A (2003) Interleukin (IL)-15R[alpha]-deficient natural killer cells survive in normal but not IL-15R[alpha]-deficient mice. J Exp Med 197:977–984. https://doi.org/10.1084/jem.20021836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Chen XY, Li B, Ma BW, Zhang XZ, Chen WZ, Lu LS, Shen X, Zhuang CL, Yu Z (2019) Sarcopenia is an effective prognostic indicator of postoperative outcomes in laparoscopic-assisted gastrectomy. Eur J Surg Oncol 45:1092–1098. https://doi.org/10.1016/j.ejso.2018.09.030

    Article  PubMed  Google Scholar 

  28. Senpuku H, Miyazaki H, Yoshihara A, Yoneda S, Narisawa N, Kawarai T, Nakagawa N, Miyachi M, Tada A, Yoshida G, Shimada M, Ohashi M, Nishimuta M, Kimura Y, Yoshitake Y (2016) CD56(dim)CD16(high) and CD56(bright)CD16(-) cell percentages associated with maximum knee extensor strength and incidence of death in elderly. Springerplus 5:244. https://doi.org/10.1186/s40064-016-1884-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lv Y, Wang H, Liu Z (2019) The role of regulatory B cells in patients with acute myeloid leukemia. Med Sci Monit 25:3026–3031. https://doi.org/10.12659/MSM.915556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This research was funded by the National Natural Science Foundation of China, grant number 82170153, Young Scholars Fostering Fund of the First Affiliated Hospital of Nanjing Medical University, and Jiangsu Province Capability Improvement Project through Science, Technology, and Education (ZDXK202209).

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Authors and Affiliations

  1. Department of Rehabilitation Medicine, The First Affiliated Hospital of Nanjing Medical University, Jiangsu Province Hospital, Nanjing, China

    Jialin Cui

  2. Department of Hematology, The First Affiliated Hospital of Nanjing Medical University, Jiangsu Province Hospital, Nanjing, China

    Miaomiao Zhao, Wenjie Liu, Ming Hong, Sixuan Qian & Qian Sun

Authors
  1. Jialin Cui
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  2. Miaomiao Zhao
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  3. Wenjie Liu
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  4. Ming Hong
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  5. Sixuan Qian
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  6. Qian Sun
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Contributions

Qian Sun and Sixuan Qian designed the study; all authors collected and analyzed the data; Jialin Cui drafted the manuscript; Qian Sun revised and supervised the manuscript. All authors have read and approved the manuscript.

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Correspondence to Qian Sun.

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The studies involving human participants were reviewed and approved by the ethics committee of the First Affiliated Hospital of Nanjing Medical University, Jiangsu Province Hospital. The patients/participants provided their written informed consent to participate in this study.

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Cui, J., Zhao, M., Liu, W. et al. Effect of low skeletal muscle mass on NK cells in patients with acute myeloid leukemia and its correlation with prognosis. Ann Hematol 103, 771–780 (2024). https://doi.org/10.1007/s00277-024-05645-8

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  • DOI: https://doi.org/10.1007/s00277-024-05645-8

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