Abstract
The geriatric nutritional risk index (GNRI) is a simple and well-established nutritional assessment tool that is a significant prognostic factor for various cancers. However, the role of the GNRI in predicting clinical outcomes of diffuse large B cell lymphoma (DLBCL) patients has not been investigated. To address this issue, we retrospectively analyzed a total of 476 patients with newly diagnosed de novo DLBCL. We defined the best cutoff value of the GNRI as 96.8 using a receiver operating characteristic curve. Patients with a GNRI < 96.8 had significantly lower overall survival (OS) and progression-free survival (PFS) than those with a GNRI ≥ 96.8 (5-year OS, 61.2 vs. 84.4%, P < 0.001; 5-year PFS, 53.7 vs. 75.8%, P < 0.001). Multivariate analysis showed that performance status, Ann Arbor stage, serum lactate dehydrogenase, and GNRI were independent prognostic factors for OS. Among patients with high-intermediate and high-risk by National Comprehensive Cancer Network-International Prognostic Index (NCCN-IPI), the 5-year OS was significantly lower in patients with a GNRI < 96.8 than in those with a GNRI ≥ 96.8 (high-intermediate risk, 59.5 vs. 75.2%, P = 0.006; high risk, 37.4 vs. 64.9%, P = 0.033). In the present study, we demonstrated that the GNRI was an independent prognostic factor in DLBCL patients. The GNRI could identify a population of poor-risk patients among those with high-intermediate and high-risk by NCCN-IPI.
Similar content being viewed by others
References
Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (2008) World Health Organization classification of tumours of haematopoietic and lymphoid tissues, 4th edn. France IARC Press, Lyon, pp 233–237
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
Habermann TM, Weller EA, Morrison VA, Gascoyne RD, Cassileth PA, Cohn JB, Dakhil SR, Woda B, Fisher RI, Peterson BA, Horning SJ (2006) Rituximab-CHOP versus CHOP alone or with maintenance rituximab in older patients with diffuse large B-cell lymphoma. J Clin Oncol Off J Am Soc Clin Oncol 24(19):3121–3127. https://doi.org/10.1200/jco.2005.05.1003
Pfreundschuh M, Kuhnt E, Trumper L, Osterborg A, Trneny M, Shepherd L, Gill DS, Walewski J, Pettengell R, Jaeger U, Zinzani PL, Shpilberg O, Kvaloy S, de Nully Brown P, Stahel R, Milpied N, Lopez-Guillermo A, Poeschel V, Grass S, Loeffler M, Murawski N (2011) CHOP-like chemotherapy with or without rituximab in young patients with good-prognosis diffuse large-B-cell lymphoma: 6-year results of an open-label randomised study of the MabThera International Trial (MInT) Group. Lancet Oncol 12(11):1013–1022. https://doi.org/10.1016/s1470-2045(11)70235-2
Pfreundschuh M, Schubert J, Ziepert M, Schmits R, Mohren M, Lengfelder E, Reiser M, Nickenig C, Clemens M, Peter N, Bokemeyer C, Eimermacher H, Ho A, Hoffmann M, Mertelsmann R, Trumper L, Balleisen L, Liersch R, Metzner B, Hartmann F, Glass B, Poeschel V, Schmitz N, Ruebe C, Feller AC, Loeffler M (2008) Six versus eight cycles of bi-weekly CHOP-14 with or without rituximab in elderly patients with aggressive CD20+ B-cell lymphomas: a randomised controlled trial (RICOVER-60). Lancet Oncol 9(2):105–116. https://doi.org/10.1016/s1470-2045(08)70002-0
Cortelazzo S, Tarella C, Gianni AM, Ladetto M, Barbui AM, Rossi A, Gritti G, Corradini P, Di Nicola M, Patti C, Mule A, Zanni M, Zoli V, Billio A, Piccin A, Negri G, Castellino C, Di Raimondo F, Ferreri AJ, Benedetti F, La Nasa G, Gini G, Trentin L, Frezzato M, Flenghi L, Falorio S, Chilosi M, Bruna R, Tabanelli V, Pileri S, Masciulli A, Delaini F, Boschini C, Rambaldi A (2016) Randomized trial comparing R-CHOP versus high-dose sequential chemotherapy in high-risk patients with diffuse large B-cell lymphomas. J Clin Oncol 34(33):4015–4022. https://doi.org/10.1200/jco.2016.67.2980
Friedberg JW (2011) Relapsed/refractory diffuse large B-cell lymphoma. Hematol Am Soc Hematol Educ Program 2011(1):498–505. https://doi.org/10.1182/asheducation-2011.1.498
The International Non-Hodgkin's Lymphoma Prognostic Factors Project (1993) A predictive model for aggressive non-Hodgkin’s lymphoma. N Engl J Med 329(14):987–994. https://doi.org/10.1056/nejm199309303291402
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
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
Hao X, Wei Y, Wei X, Zhou L, Wei Q, Zhang Y, Huang W, Feng R (2017) Glasgow prognostic score is superior to other inflammation-based scores in predicting survival of diffuse large B-cell lymphoma. Oncotarget 8(44):76740–76748. https://doi.org/10.18632/oncotarget.20832
Kim Y, Kim SJ, Hwang D, Jang J, Hyun SY, Kim YR, Kim JS, Min YH, Cheong JW (2014) The modified Glasgow Prognostic Scores as a predictor in diffuse large B cell lymphoma treated with R-CHOP regimen. Yonsei Med J 55(6):1568–1575. https://doi.org/10.3349/ymj.2014.55.6.1568
Li X, Zhang Y, Zhao W, Liu Z, Shen Y, Li J, Shen Z (2015) The Glasgow Prognostic Score as a significant predictor of diffuse large B cell lymphoma treated with R-CHOP in China. Ann Hematol 94(1):57–63. https://doi.org/10.1007/s00277-014-2167-0
Perisa V, Zibar L, Knezovic A, Perisa I, Sincic-Petricevic J, Aurer I (2017) Prognostic nutritional index as a predictor of prognosis in patients with diffuse large B cell lymphoma. Wien Klin Wochenschr 129(11–12):411–419. https://doi.org/10.1007/s00508-016-1077-7
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
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
Buzby GP, Knox LS, Crosby LO, Eisenberg JM, Haakenson CM, McNeal GE, Page CP, Peterson OL, Reinhardt GF, Williford WO (1988) Study protocol: a randomized clinical trial of total parenteral nutrition in malnourished surgical patients. Am J Clin Nutr 47(2 Suppl):366–381. https://doi.org/10.1093/ajcn/47.2.366
Buzby GP, Williford WO, Peterson OL, Crosby LO, Page CP, Reinhardt GF, Mullen JL (1988) A randomized clinical trial of total parenteral nutrition in malnourished surgical patients: the rationale and impact of previous clinical trials and pilot study on protocol design. Am J Clin Nutr 47(2 Suppl):357–365. https://doi.org/10.1093/ajcn/47.2.357
Naber TH, de Bree A, Schermer TR, Bakkeren J, Bar B, de Wild G, Katan MB (1997) Specificity of indexes of malnutrition when applied to apparently healthy people: the effect of age. Am J Clin Nutr 65(6):1721–1725. https://doi.org/10.1093/ajcn/65.6.1721
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
Bo Y, Wang K, Liu Y, You J, Cui H, Zhu Y, Lu Q, Yuan L (2016) The geriatric nutritional risk index predicts survival in elderly esophageal squamous cell carcinoma patients with radiotherapy. PLoS One 11(5):e0155903. https://doi.org/10.1371/journal.pone.0155903
Gu W, Zhang G, Sun L, Ma Q, Cheng Y, Zhang H, Shi G, Zhu Y, Ye D (2015) Nutritional screening is strongly associated with overall survival in patients treated with targeted agents for metastatic renal cell carcinoma. J Cachexia Sarcopenia Muscle 6(3):222–230. https://doi.org/10.1002/jcsm.12025
Miyake H, Tei H, Fujisawa M (2017) Geriatric nutrition risk index is an important predictor of cancer-specific survival, but not recurrence-free survival, in patients undergoing surgical resection for non-metastatic renal cell carcinoma. Curr Urol 10(1):26–31. https://doi.org/10.1159/000447147
Shoji F, Matsubara T, Kozuma Y, Haratake N, Akamine T, Takamori S, Katsura M, Toyokawa G, Okamoto T, Maehara Y (2017) Preoperative geriatric nutritional risk index: a predictive and prognostic factor in patients with pathological stage I non-small cell lung cancer. Surg Oncol 26(4):483–488. https://doi.org/10.1016/j.suronc.2017.09.006
Shoji F, Miura N, Matsubara T, Akamine T, Kozuma Y, Haratake N, Takamori S, Katsura M, Takada K, Toyokawa G, Takenaka T, Yamazaki K, Okamoto T, Takeo S, Maehara Y (2017) Prognostic significance of immune-nutritional parameters for surgically resected elderly lung cancer patients: a multicentre retrospective study. Interact Cardiovasc Thorac Surg. https://doi.org/10.1093/icvts/ivx337
Mori M, Niitsu N, Takagi T, Tomiyama J, Matsue T, Nakagawa Y, Okamoto R (2001) Reduced-dose chop therapy for elderly patients with non-Hodgkin’s lymphoma. Leuk Lymphoma 41(3–4):359–366. https://doi.org/10.3109/10428190109057991
Shah B, Sucher K, Hollenbeck CB (2006) Comparison of ideal body weight equations and published height-weight tables with body mass index tables for healthy adults in the United States. Nutr Clin Pract 21(3):312–319. https://doi.org/10.1177/0115426506021003312
Yamada K, Furuya R, Takita T, Maruyama Y, Yamaguchi Y, Ohkawa S, Kumagai H (2008) Simplified nutritional screening tools for patients on maintenance hemodialysis. Am J Clin Nutr 87(1):106–113
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
Bozzetti F, Mariani L, Lo Vullo S, Amerio ML, Biffi R, Caccialanza G, Capuano G, Correja I, Cozzaglio L, Di Leo A, Di Cosmo L, Finocchiaro C, Gavazzi C, Giannoni A, Magnanini P, Mantovani G, Pellegrini M, Rovera L, Sandri G, Tinivella M, Vigevani E (2012) The nutritional risk in oncology: a study of 1,453 cancer outpatients. Support Care Cancer 20(8):1919–1928. https://doi.org/10.1007/s00520-012-1387-x
Hebuterne X, Lemarie E, Michallet M, de Montreuil CB, Schneider SM, Goldwasser F (2014) Prevalence of malnutrition and current use of nutrition support in patients with cancer. JPEN J Parenter Enteral Nutr 38(2):196–204. https://doi.org/10.1177/0148607113502674
Carson KR, Bartlett NL, McDonald JR, Luo S, Zeringue A, Liu J, Fu Q, Chang SH, Colditz GA (2012) Increased body mass index is associated with improved survival in United States veterans with diffuse large B-cell lymphoma. J Clin Oncol Off J Am Soc Clin Oncol 30(26):3217–3222. https://doi.org/10.1200/jco.2011.39.2100
Jones JA, Fayad LE, Elting LS, Rodriguez MA (2010) Body mass index and outcomes in patients receiving chemotherapy for intermediate-grade B-cell non-Hodgkin lymphoma. Leuk Lymphoma 51(9):1649–1657. https://doi.org/10.3109/10428194.2010.494315
Li T, Liu ZG, Liang PQ, Wang HT (2016) Can body mass index predict the outcome of diffuse large B-cell lymphoma? A single-center retrospective study in China. Leuk Lymphoma 58(7):1–6. https://doi.org/10.1080/10428194.2016.1257793
Weiss L, Melchardt T, Habringer S, Boekstegers A, Hufnagl C, Neureiter D, Hopfinger G, Greil R, Egle A (2014) Increased body mass index is associated with improved overall survival in diffuse large B-cell lymphoma. Ann Oncol 25(1):171–176. https://doi.org/10.1093/annonc/mdt481
Boyle T, Connors JM, Gascoyne RD, Berry BR, Sehn LH, Bashash M, Spinelli JJ (2017) Physical activity, obesity and survival in diffuse large B-cell and follicular lymphoma cases. Br J Haematol 178(3):442–447. https://doi.org/10.1111/bjh.14702
Hong F, Habermann TM, Gordon LI, Hochster H, Gascoyne RD, Morrison VA, Fisher RI, Bartlett NL, Stiff PJ, Cheson BD, Crump M, Horning SJ, Kahl BS (2014) The role of body mass index in survival outcome for lymphoma patients: US intergroup experience. Ann Oncol 25(3):669–674. https://doi.org/10.1093/annonc/mdt594
Hwang HS, Yoon DH, Suh C, Huh J (2015) Body mass index as a prognostic factor in Asian patients treated with chemoimmunotherapy for diffuse large B cell lymphoma, not otherwise specified. Ann Hematol 94(10):1655–1665. https://doi.org/10.1007/s00277-015-2438-4
Kanemasa Y, Shimoyama T, Sasaki Y, Tamura M, Sawada T, Omuro Y, Hishima T, Maeda Y (2017) Analysis of the prognostic value of BMI and the difference in its impact according to age and sex in DLBCL patients. Hematol Oncol. https://doi.org/10.1002/hon.2426
Camus V, Lanic H, Kraut J, Modzelewski R, Clatot F, Picquenot JM, Contentin N, Lenain P, Groza L, Lemasle E, Fronville C, Cardinael N, Fontoura ML, Chamseddine A, Brehar O, Stamatoullas A, Lepretre S, Tilly H, Jardin F (2014) Prognostic impact of fat tissue loss and cachexia assessed by computed tomography scan in elderly patients with diffuse large B-cell lymphoma treated with immunochemotherapy. Eur J Haematol 93(1):9–18. https://doi.org/10.1111/ejh.12285
Lanic H, Kraut-Tauzia J, Modzelewski R, Clatot F, Mareschal S, Picquenot JM, Stamatoullas A, Lepretre S, Tilly H, Jardin F (2014) Sarcopenia is an independent prognostic factor in elderly patients with diffuse large B-cell lymphoma treated with immunochemotherapy. Leuk Lymphoma 55(4):817–823. https://doi.org/10.3109/10428194.2013.816421
de van der Schueren M, Elia M, Gramlich L, Johnson MP, Lim SL, Philipson T, Jaferi A, Prado CM (2014) Clinical and economic outcomes of nutrition interventions across the continuum of care. Ann N Y Acad Sci 1321(1):20–40. https://doi.org/10.1111/nyas.12498
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
Dalia S, Chavez J, Little B, Bello C, Fisher K, Lee JH, Chervenick P, Sokol L, Sotomayor E, Shah B (2014) Serum albumin retains independent prognostic significance in diffuse large B-cell lymphoma in the post-rituximab era. Ann Hematol 93(8):1305–1312. https://doi.org/10.1007/s00277-014-2031-2
Ngo L, Hee SW, Lim LC, Tao M, Quek R, Yap SP, Loong EL, Sng I, Hwan-Cheong TL, Ang MK, Ngeow J, Tham CK, Tan MH, Lim ST (2008) Prognostic factors in patients with diffuse large B cell lymphoma: before and after the introduction of rituximab. Leuk Lymphoma 49(3):462–469. https://doi.org/10.1080/10428190701809156
Marian M, August DA (2014) Prevalence of malnutrition and current use of nutrition support in cancer patient study. JPEN J Parenter Enteral Nutr 38(2):163–165. https://doi.org/10.1177/0148607113506940
Forrest LM, McMillan DC, McArdle CS, Angerson WJ, Dunlop DJ (2003) Evaluation of cumulative prognostic scores based on the systemic inflammatory response in patients with inoperable non-small-cell lung cancer. Br J Cancer 89(6):1028–1030. https://doi.org/10.1038/sj.bjc.6601242
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
McMillan DC, Crozier JE, Canna K, Angerson WJ, McArdle CS (2007) Evaluation of an inflammation-based prognostic score (GPS) in patients undergoing resection for colon and rectal cancer. Int J Color Dis 22(8):881–886. https://doi.org/10.1007/s00384-006-0259-6
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
Iseki Y, Shibutani M, Maeda K, Nagahara H, Ohtani H, Sugano K, Ikeya T, Muguruma K, Tanaka H, Toyokawa T, Sakurai K, Hirakawa K (2015) Impact of the preoperative Controlling Nutritional Status (CONUT) score on the survival after curative surgery for colorectal cancer. PLoS One 10(7):e0132488. https://doi.org/10.1371/journal.pone.0132488
Toyokawa T, Kubo N, Tamura T, Sakurai K, Amano R, Tanaka H, Muguruma K, Yashiro M, Hirakawa K, Ohira M (2016) The pretreatment Controlling Nutritional Status (CONUT) score is an independent prognostic factor in patients with resectable thoracic esophageal squamous cell carcinoma: results from a retrospective study. BMC Cancer 16(1):722. https://doi.org/10.1186/s12885-016-2696-0
Thieblemont C, Coiffier B (2007) Lymphoma in older patients. J Clin Oncol Off J Am Soc Clin Oncol 25(14):1916–1923. https://doi.org/10.1200/jco.2006.10.5957
Klapper W, Kreuz M, Kohler CW, Burkhardt B, Szczepanowski M, Salaverria I, Hummel M, Loeffler M, Pellissery S, Woessmann W, Schwanen C, Trumper L, Wessendorf S, Spang R, Hasenclever D, Siebert R (2012) Patient age at diagnosis is associated with the molecular characteristics of diffuse large B-cell lymphoma. Blood 119(8):1882–1887. https://doi.org/10.1182/blood-2011-10-388470
Duran Alert P, Mila Villarroel R, Formiga F, Virgili Casas N, Vilarasau Farre C (2012) Assessing risk screening methods of malnutrition in geriatric patients: Mini Nutritional Assessment (MNA) versus Geriatric Nutritional Risk Index (GNRI). Nutr Hosp 27(2):590–598. https://doi.org/10.1590/s0212-16112012000200036
Kinugasa Y, Kato M, Sugihara S, Hirai M, Yamada K, Yanagihara K, Yamamoto K (2013) Geriatric nutritional risk index predicts functional dependency and mortality in patients with heart failure with preserved ejection fraction. Circ J 77(3):705–711
Matsumura T, Mitani Y, Oki Y, Fujimoto Y, Ohira M, Kaneko H, Kawashima T, Nishio M, Ishikawa A (2015) Comparison of Geriatric Nutritional Risk Index scores on physical performance among elderly patients with chronic obstructive pulmonary disease. Heart Lung 44(6):534–538. https://doi.org/10.1016/j.hrtlng.2015.08.004
Acknowledgments
We would like to thank all the patients who took part in this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The protocol for this study was approved by the institutional ethics review board of our hospital, and informed consent for retrospective analysis was obtained from all patients.
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Kanemasa, Y., Shimoyama, T., Sasaki, Y. et al. Geriatric nutritional risk index as a prognostic factor in patients with diffuse large B cell lymphoma. Ann Hematol 97, 999–1007 (2018). https://doi.org/10.1007/s00277-018-3273-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00277-018-3273-1