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Validation and comparison of prognostic values of GNRI, PNI, and CONUT in newly diagnosed diffuse large B cell lymphoma

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Abstract

Diffuse large B cell lymphoma (DLBCL) is the most common type of aggressive non-Hodgkin lymphoma. Emerging evidence indicates that poor nutritional status determined with nutritional indices such as geriatric nutritional risk index (GNRI), prognostic nutritional index (PNI), and controlling nutritional status score (CONUT) was associated with poor prognosis of DLBCL. We conducted this multicenter retrospective study to validate and compare prognostic values of the three indices in 615 newly diagnosed DLBCL patients. The overall survival (OS) in patients with poor nutritional status determined with each of these nutritional indices were significantly inferior compared with that in those without nutritional risks (5-year OS in patients with GNRI < 95.7 and GNRI ≥ 95.7 were 56.4% and 83.5%, P < 0.001; PNI < 42.4 and PNI ≥ 42.4 were 56.1% and 81.0%, P < 0.001; CONUT > 4 and CONUT ≤ 4 were 53.1% and 77.1%, P < 0.001). GNRI and CONUT were independent prognostic predictors for OS (GNRI < 95.7, hazard ratio [HR] 1.83, 95% confidence interval [CI] 1.22–2.74, P = 0.0032; CONUT > 4, HR 1.53, 95% CI 1.05–2.23, P = 0.028) after multivariate analyses. Nutritional status determined with GNRI affected OS more strongly in the patients with nongerminal center B cell–like (nonGCB) DLBCL compared with that in those with GCB-type DLBCL. In conclusion, baseline poor nutritional status determined based on GNRI or CONUT was an independent risk factor of newly diagnosed DLBCL, and GNRI was also useful as an independent prognostic factor for patients with nonGCB-type DLBCL.

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References

  1. Swerdlow SHCE, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele JVJ (2008) WHO classification of tumours of haematopoietic and lymphoid tissues, 4th edn. In: WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. France IARC Press, Lyon, France, pp 233–237

    Google Scholar 

  2. Miao Y, Medeiros LJ, Li Y, Li J, Young KH (2019) Genetic alterations and their clinical implications in DLBCL. Nat Rev Clin Oncol 16(10):634–652. https://doi.org/10.1038/s41571-019-0225-1

    Article  CAS  PubMed  Google Scholar 

  3. Coiffier B, Lepage E, Briere J, Herbrecht R, Tilly H, Bouabdallah R, Morel P, Van Den Neste E, Salles G, Gaulard P, Reyes F, Lederlin P, Gisselbrecht C (2002) CHOP chemotherapy plus rituximab compared with CHOP alone in elderly patients with diffuse large-B-cell lymphoma. N Engl J Med 346(4):235–242. https://doi.org/10.1056/NEJMoa011795

    Article  CAS  PubMed  Google Scholar 

  4. Pfreundschuh M, Trumper L, Osterborg A, Pettengell R, Trneny M, Imrie K, Ma D, Gill D, Walewski J, Zinzani PL, Stahel R, Kvaloy S, Shpilberg O, Jaeger U, Hansen M, Lehtinen T, Lopez-Guillermo A, Corrado C, Scheliga A, Milpied N, Mendila M, Rashford M, Kuhnt E, Loeffler M, MabThera International Trial G (2006) CHOP-like chemotherapy plus rituximab versus CHOP-like chemotherapy alone in young patients with good-prognosis diffuse large-B-cell lymphoma: a randomised controlled trial by the MabThera International Trial (MInT) Group. Lancet Oncol 7(5):379–391. https://doi.org/10.1016/S1470-2045(06)70664-7

    Article  CAS  PubMed  Google Scholar 

  5. International Non-Hodgkin’s Lymphoma Prognostic Factors P (1993) A predictive model for aggressive non-Hodgkin’s lymphoma. N Engl J Med 329(14):987–994. https://doi.org/10.1056/NEJM199309303291402

    Article  Google Scholar 

  6. Sonnen R, Schmidt WP, Kuse R, Schmitz N (2002) Treatment results of aggressive B non-Hodgkin’s lymphoma in advanced age considering comorbidity. Br J Haematol 119(3):634–639. https://doi.org/10.1046/j.1365-2141.2002.03896.x

    Article  CAS  PubMed  Google Scholar 

  7. Advani RH, Chen H, Habermann TM, Morrison VA, Weller EA, Fisher RI, Peterson BA, Gascoyne RD, Horning SJ, Eastern Cooperative Oncology G, Cancer, Leukemia Group B, Southwest Oncology G (2010) Comparison of conventional prognostic indices in patients older than 60 years with diffuse large B-cell lymphoma treated with R-CHOP in the US Intergroup Study (ECOG 4494, CALGB 9793): consideration of age greater than 70 years in an elderly prognostic index (E-IPI). Br J Haematol 151(2):143–151. https://doi.org/10.1111/j.1365-2141.2010.08331.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Sehn LH, Berry B, Chhanabhai M, Fitzgerald C, Gill K, Hoskins P, Klasa R, Savage KJ, Shenkier T, Sutherland J, Gascoyne RD, Connors JM (2007) The revised International Prognostic Index (R-IPI) is a better predictor of outcome than the standard IPI for patients with diffuse large B-cell lymphoma treated with R-CHOP. Blood 109(5):1857–1861. https://doi.org/10.1182/blood-2006-08-038257

    Article  CAS  PubMed  Google Scholar 

  9. Zhou Z, Sehn LH, Rademaker AW, Gordon LI, Lacasce AS, Crosby-Thompson A, Vanderplas A, Zelenetz AD, Abel GA, Rodriguez MA, Nademanee A, Kaminski MS, Czuczman MS, Millenson M, Niland J, Gascoyne RD, Connors JM, Friedberg JW, Winter JN (2014) An enhanced International Prognostic Index (NCCN-IPI) for patients with diffuse large B-cell lymphoma treated in the rituximab era. Blood 123(6):837–842. https://doi.org/10.1182/blood-2013-09-524108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Park S, Han B, Cho JW, Woo SY, Kim S, Kim SJ, Kim WS (2014) Effect of nutritional status on survival outcome of diffuse large B-cell lymphoma patients treated with rituximab-CHOP. Nutr Cancer 66(2):225–233. https://doi.org/10.1080/01635581.2014.867065

    Article  CAS  PubMed  Google Scholar 

  11. Bairey O, Shacham-Abulafia A, Shpilberg O, Gurion R (2016) Serum albumin level at diagnosis of diffuse large B-cell lymphoma: an important simple prognostic factor. Hematol Oncol 34(4):184–192. https://doi.org/10.1002/hon.2233

    Article  CAS  PubMed  Google Scholar 

  12. Cox MC, Nofroni I, Ruco L, Amodeo R, Ferrari A, La Verde G, Cardelli P, Montefusco E, Conte E, Monarca B, Aloe-Spiriti MA (2008) Low absolute lymphocyte count is a poor prognostic factor in diffuse-large-B-cell-lymphoma. Leuk Lymphoma 49(9):1745–1751. https://doi.org/10.1080/10428190802226425

    Article  PubMed  Google Scholar 

  13. Cox MC, Nofroni I, Laverde G, Ferrari A, Amodeo R, Tatarelli C, Saltarelli F, Veggia B, Aloe-Spiriti MA, Ruco L, Monarca B (2008) Absolute lymphocyte count is a prognostic factor in diffuse large B-cell lymphoma. Br J Haematol 141(2):265–268. https://doi.org/10.1111/j.1365-2141.2008.07028.x

    Article  PubMed  Google Scholar 

  14. Gao R, Liang JH, Wang L, Zhu HY, Wu W, Cao L, Fan L, Li JY, Yang T, Xu W (2018) Low serum cholesterol levels predict inferior prognosis and improve NCCN-IPI scoring in diffuse large B cell lymphoma. Int J Cancer 143(8):1884–1895. https://doi.org/10.1002/ijc.31590

    Article  CAS  PubMed  Google Scholar 

  15. Kanemasa Y, Shimoyama T, Sasaki Y, Hishima T, Omuro Y (2018) Geriatric nutritional risk index as a prognostic factor in patients with diffuse large B cell lymphoma. Ann Hematol 97(6):999–1007. https://doi.org/10.1007/s00277-018-3273-1

    Article  PubMed  Google Scholar 

  16. Li Z, Guo Q, Wei J, Jin J, Wang J (2018) Geriatric nutritional risk index is not an independent predictor in patients with diffuse large B-cell lymphoma. Cancer Biomark 21(4):813–820. https://doi.org/10.3233/CBM-170754

    Article  CAS  PubMed  Google Scholar 

  17. Go SI, Park S, Kang MH, Kim HG, Kim HR, Lee GW (2019) Clinical impact of prognostic nutritional index in diffuse large B cell lymphoma. Ann Hematol 98(2):401–411. https://doi.org/10.1007/s00277-018-3540-1

    Article  CAS  PubMed  Google Scholar 

  18. Lee S, Fujita K, Morishita T, Negoro E, Oiwa K, Tsukasaki H, Yamamura O, Ueda T, Yamauchi T (2020) Prognostic utility of a geriatric nutritional risk index in combination with a comorbidity index in elderly patients with diffuse large B cell lymphoma. Br J Haematol. https://doi.org/10.1111/bjh.16743

  19. Hamada E, Shinji O, Nishiyama-Fujita Y, Akiimoto M, Tanigawa T, Ito C, Sakurai A, Aisa Y, Nakazato T (2020) The clinical significance of the prognostic nutritional index in very elderly patients over 80 years of age with diffuse large B-cell lymphoma. Ann Hematol 99(5):1153–1155. https://doi.org/10.1007/s00277-020-04012-7

    Article  PubMed  Google Scholar 

  20. Nagata A, Kanemasa Y, Sasaki Y, Nakamura S, Okuya T, Funasaka C, Kageyama A, Shimoyama T, Omuro Y (2020) Clinical impact of Controlling Nutritional Status (CONUT) score on the prognosis of patients with diffuse large B-cell lymphoma. Hematol Oncol 38:309–317. https://doi.org/10.1002/hon.2732

    Article  CAS  PubMed  Google Scholar 

  21. Ignacio de Ulibarri J, Gonzalez-Madrono A, de Villar NG, Gonzalez P, Gonzalez B, Mancha A, Rodriguez F, Fernandez G (2005) CONUT: a tool for controlling nutritional status. First validation in a hospital population. Nutr Hosp 20(1):38–45

    CAS  PubMed  Google Scholar 

  22. Onodera T, Goseki N, Kosaki G (1984) Prognostic nutritional index in gastrointestinal surgery of malnourished cancer patients. Nihon Geka Gakkai Zasshi 85(9):1001–1005

    CAS  PubMed  Google Scholar 

  23. Hans CP, Weisenburger DD, Greiner TC, Gascoyne RD, Delabie J, Ott G, Muller-Hermelink HK, Campo E, Braziel RM, Jaffe ES, Pan Z, Farinha P, Smith LM, Falini B, Banham AH, Rosenwald A, Staudt LM, Connors JM, Armitage JO, Chan WC (2004) Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood 103(1):275–282. https://doi.org/10.1182/blood-2003-05-1545

    Article  CAS  PubMed  Google Scholar 

  24. Bouillanne O, Morineau G, Dupont C, Coulombel I, Vincent JP, Nicolis I, Benazeth S, Cynober L, Aussel C (2005) Geriatric Nutritional Risk Index: a new index for evaluating at-risk elderly medical patients. Am J Clin Nutr 82(4):777–783. https://doi.org/10.1093/ajcn/82.4.777

    Article  CAS  PubMed  Google Scholar 

  25. Kanda Y (2013) Investigation of the freely available easy-to-use software 'EZR' for medical statistics. Bone Marrow Transplant 48(3):452–458. https://doi.org/10.1038/bmt.2012.244

    Article  CAS  PubMed  Google Scholar 

  26. Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A, Boldrick JC, Sabet H, Tran T, Yu X, Powell JI, Yang L, Marti GE, Moore T, Hudson J Jr, Lu L, Lewis DB, Tibshirani R, Sherlock G, Chan WC, Greiner TC, Weisenburger DD, Armitage JO, Warnke R, Levy R, Wilson W, Grever MR, Byrd JC, Botstein D, Brown PO, Staudt LM (2000) Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403(6769):503–511. https://doi.org/10.1038/35000501

    Article  CAS  PubMed  Google Scholar 

  27. Rosenwald A, Wright G, Chan WC, Connors JM, Campo E, Fisher RI, Gascoyne RD, Muller-Hermelink HK, Smeland EB, Giltnane JM, Hurt EM, Zhao H, Averett L, Yang L, Wilson WH, Jaffe ES, Simon R, Klausner RD, Powell J, Duffey PL, Longo DL, Greiner TC, Weisenburger DD, Sanger WG, Dave BJ, Lynch JC, Vose J, Armitage JO, Montserrat E, Lopez-Guillermo A, Grogan TM, Miller TP, LeBlanc M, Ott G, Kvaloy S, Delabie J, Holte H, Krajci P, Stokke T, Staudt LM, Lymphoma/Leukemia Molecular Profiling P (2002) The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N Engl J Med 346 (25):1937-1947. https://doi.org/10.1056/NEJMoa012914

  28. Zhou Q, Wei Y, Huang F, Wei X, Wei Q, Hao X, Zhang Y, Feng R (2016) Low prognostic nutritional index predicts poor outcome in diffuse large B-cell lymphoma treated with R-CHOP. Int J Hematol 104(4):485–490. https://doi.org/10.1007/s12185-016-2052-9

    Article  CAS  PubMed  Google Scholar 

  29. Arroyo V, Garcia-Martinez R, Salvatella X (2014) Human serum albumin, systemic inflammation, and cirrhosis. J Hepatol 61(2):396–407. https://doi.org/10.1016/j.jhep.2014.04.012

    Article  CAS  PubMed  Google Scholar 

  30. Sugino H, Hashimoto I, Tanaka Y, Ishida S, Abe Y, Nakanishi H (2014) Relation between the serum albumin level and nutrition supply in patients with pressure ulcers: retrospective study in an acute care setting. J Med Investig 61(1-2):15–21. https://doi.org/10.2152/jmi.61.15

    Article  Google Scholar 

  31. Karas PL, Goh SL, Dhital K (2015) Is low serum albumin associated with postoperative complications in patients undergoing cardiac surgery? Interact Cardiovasc Thorac Surg 21(6):777–786. https://doi.org/10.1093/icvts/ivv247

    Article  PubMed  Google Scholar 

  32. Gupta D, Lis CG (2010) Pretreatment serum albumin as a predictor of cancer survival: a systematic review of the epidemiological literature. Nutr J 9:69. https://doi.org/10.1186/1475-2891-9-69

    Article  PubMed  PubMed Central  Google Scholar 

  33. Williams JP, Phillips BE, Smith K, Atherton PJ, Rankin D, Selby AL, Liptrot S, Lund J, Larvin M, Rennie MJ (2012) Effect of tumor burden and subsequent surgical resection on skeletal muscle mass and protein turnover in colorectal cancer patients. Am J Clin Nutr 96(5):1064–1070. https://doi.org/10.3945/ajcn.112.045708

    Article  CAS  PubMed  Google Scholar 

  34. Alshadwi A, Nadershah M, Carlson ER, Young LS, Burke PA, Daley BJ (2013) Nutritional considerations for head and neck cancer patients: a review of the literature. J Oral Maxillofac Surg 71(11):1853–1860. https://doi.org/10.1016/j.joms.2013.04.028

    Article  PubMed  Google Scholar 

  35. Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E, Fainsinger RL, Jatoi A, Loprinzi C, MacDonald N, Mantovani G, Davis M, Muscaritoli M, Ottery F, Radbruch L, Ravasco P, Walsh D, Wilcock A, Kaasa S, Baracos VE (2011) Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 12(5):489–495. https://doi.org/10.1016/S1470-2045(10)70218-7

    Article  PubMed  Google Scholar 

  36. Davis RE, Brown KD, Siebenlist U, Staudt LM (2001) Constitutive nuclear factor kappaB activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells. J Exp Med 194(12):1861–1874. https://doi.org/10.1084/jem.194.12.1861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Lam LT, Davis RE, Ngo VN, Lenz G, Wright G, Xu W, Zhao H, Yu X, Dang L, Staudt LM (2008) Compensatory IKKalpha activation of classical NF-kappaB signaling during IKKbeta inhibition identified by an RNA interference sensitization screen. Proc Natl Acad Sci U S A 105(52):20798–20803. https://doi.org/10.1073/pnas.0806491106

    Article  PubMed  PubMed Central  Google Scholar 

  38. Ding BB, Yu JJ, Yu RY, Mendez LM, Shaknovich R, Zhang Y, Cattoretti G, Ye BH (2008) Constitutively activated STAT3 promotes cell proliferation and survival in the activated B-cell subtype of diffuse large B-cell lymphomas. Blood 111(3):1515–1523. https://doi.org/10.1182/blood-2007-04-087734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Fearon KC, Von Meyenfeldt MF, Moses AG, Van Geenen R, Roy A, Gouma DJ, Giacosa A, Van Gossum A, Bauer J, Barber MD, Aaronson NK, Voss AC, Tisdale MJ (2003) Effect of a protein and energy dense N-3 fatty acid enriched oral supplement on loss of weight and lean tissue in cancer cachexia: a randomised double blind trial. Gut 52(10):1479–1486. https://doi.org/10.1136/gut.52.10.1479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgment

The authors would like to thank the nursing and medical staff who looked after the patients.

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T. Matsukawa, K.S., M.K., and K.I. designed this study. T. Matsukawa, K.S., M.K., K.I., K.M., S.Y., H.O, T. Miyagishima, A.M., and S.O. performed recruitment and treatment. T.Matsukawa, K.S., M.K., K.I., and S.Y. collected the data. T. Matsukawa, K.S., and D.H. analyzed and interpreted data. T. Matsukawa and D.H. wrote the manuscript. T.T. supervised this study.

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Correspondence to Toshihiro Matsukawa.

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All procedures involving human participants were in accordance with the ethical standards of institutional and/or national research committees and with the Declaration of Helsinki. This study was approved by institutional review board of each hospital.

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Matsukawa, T., Suto, K., Kanaya, M. et al. Validation and comparison of prognostic values of GNRI, PNI, and CONUT in newly diagnosed diffuse large B cell lymphoma. Ann Hematol 99, 2859–2868 (2020). https://doi.org/10.1007/s00277-020-04262-5

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