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Published in: BMC Cancer 1/2018

Open Access 01-12-2018 | Research article

Inflammation marker ESR is effective in predicting outcome of diffuse large B-cell lymphoma

Authors: Shuang Wu, Ye Zhou, Hai-Ying Hua, Yan Zhang, Wen-Yan Zhu, Zhi-Qing Wang, Jin Li, Hua-Qiang Gao, Xiao-Hong Wu, Ting-Xun Lu, Dong Hua

Published in: BMC Cancer | Issue 1/2018

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Abstract

Background

Systemic inflammation has been implicated in cancer development and progression. This study examined the best cutoff value of erythrocyte sedimentation rate (ESR) in diffuse large B-cell lymphoma (DLBCL) patients.

Methods

The relationship between ESR and clinical characteristics was analyzed in 182 DLBCL patients from 2006 to 2017. The log-rank test, univariate analysis, and Cox regression analysis were applied to evaluate the relationship between ESR and survival. An ESR of more than 37.5 mm/hour was found to be the optimal threshold value for predicting prognosis.

Results

ESR was associated with more frequent advanced Ann Arbor stage, poorer performance status, elevated lactate dehydrogenase level, the presence of B symptoms, high-risk International Prognostic Index (IPI 3–5), more extranodal involvement (ENI ≥2), non-germinal-center B-cell (non-GCB) subtypes, and more frequent Myc protein positivity. Shorter overall survival (OS) and progression-free survival (PFS) were found for patients with higher ESRs. Multivariate analysis demonstrated that ESR level is an independent prognostic factor of both OS and PFS. In addition, dynamic changes in ESR are valuable in assessing curative effect and predicting disease recurrence.

Conclusion

High ESR in DLBCL patients indicated unfavorable prognosis that may require alternative treatment regimens.
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Literature
1.
go back to reference Friedberg JW, Fisher RI. Diffuse large B-cell lymphoma. Hematol Oncol Clin North Am. 2008;22(5):941–52.CrossRef Friedberg JW, Fisher RI. Diffuse large B-cell lymphoma. Hematol Oncol Clin North Am. 2008;22(5):941–52.CrossRef
2.
go back to reference Hans CP, Weisenburger DD, Greiner TC, Gascoyne RD, Delabie J, Ott G, Muller-Hermelink HK, Campo E, Braziel RM, Jaffe ES, et al. Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood. 2004;103(1):275–82.CrossRef Hans CP, Weisenburger DD, Greiner TC, Gascoyne RD, Delabie J, Ott G, Muller-Hermelink HK, Campo E, Braziel RM, Jaffe ES, et al. Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood. 2004;103(1):275–82.CrossRef
3.
go back to reference Ozturk E, Ozbalak M, Berk S, Erdogan I, Avsar E, Dolgun A, Cetiner M, Mandel NM, Yalniz FF, Elverdi T, et al. Comparison of international prognostic index and NCCN-IPI in 324 patients with de novo diffuse large B-cell lymphoma: a multi-center retrospective analysis. Leukemia & lymphoma. 2016;57(5):1211–4.CrossRef Ozturk E, Ozbalak M, Berk S, Erdogan I, Avsar E, Dolgun A, Cetiner M, Mandel NM, Yalniz FF, Elverdi T, et al. Comparison of international prognostic index and NCCN-IPI in 324 patients with de novo diffuse large B-cell lymphoma: a multi-center retrospective analysis. Leukemia & lymphoma. 2016;57(5):1211–4.CrossRef
4.
go back to reference Huang CE, Chen YY, Lu CH, Chen PT, Lee KD, Chen CC. Validation of an enhanced international prognostic index (NCCN-IPI) in an Asian cohort of patients with diffuse large B cell lymphoma. Ann Hematol. 2015;94(6):1063–5.CrossRef Huang CE, Chen YY, Lu CH, Chen PT, Lee KD, Chen CC. Validation of an enhanced international prognostic index (NCCN-IPI) in an Asian cohort of patients with diffuse large B cell lymphoma. Ann Hematol. 2015;94(6):1063–5.CrossRef
5.
go back to reference El-Galaly TC, Villa D, Alzahrani M, Hansen JW, Sehn LH, Wilson D, de Nully Brown P, Loft A, Iyer V, Johnsen HE, et al. Outcome prediction by extranodal involvement, IPI, R-IPI, and NCCN-IPI in the PET/CT and rituximab era: a Danish-Canadian study of 443 patients with diffuse-large B-cell lymphoma. Am J Hematol. 2015;90(11):1041–6.CrossRef El-Galaly TC, Villa D, Alzahrani M, Hansen JW, Sehn LH, Wilson D, de Nully Brown P, Loft A, Iyer V, Johnsen HE, et al. Outcome prediction by extranodal involvement, IPI, R-IPI, and NCCN-IPI in the PET/CT and rituximab era: a Danish-Canadian study of 443 patients with diffuse-large B-cell lymphoma. Am J Hematol. 2015;90(11):1041–6.CrossRef
6.
go back to reference Montalban C, Diaz-Lopez A, Dlouhy I, Rovira J, Lopez-Guillermo A, Alonso S, Martin A, Sancho JM, Garcia O, Sanchez JM, et al. Validation of the NCCN-IPI for diffuse large B-cell lymphoma (DLBCL): the addition of beta2 -microglobulin yields a more accurate GELTAMO-IPI. Br J Haematol. 2017;176(6):918–28.CrossRef Montalban C, Diaz-Lopez A, Dlouhy I, Rovira J, Lopez-Guillermo A, Alonso S, Martin A, Sancho JM, Garcia O, Sanchez JM, et al. Validation of the NCCN-IPI for diffuse large B-cell lymphoma (DLBCL): the addition of beta2 -microglobulin yields a more accurate GELTAMO-IPI. Br J Haematol. 2017;176(6):918–28.CrossRef
7.
go back to reference Eiro N, Vizoso FJ. Inflammation and cancer. World journal of gastrointestinal surgery. 2012;4(3):62–72.CrossRef Eiro N, Vizoso FJ. Inflammation and cancer. World journal of gastrointestinal surgery. 2012;4(3):62–72.CrossRef
8.
go back to reference Rotaru I, Gaman GD, Stanescu C, Gaman AM. Evaluation of parameters with potential prognosis impact in patients with primary gastric diffuse large B-cell lymphoma (PG-DLBCL). Romanian journal of morphology and embryology = Revue roumaine de morphologie et embryologie. 2014;55(1):15–21.PubMed Rotaru I, Gaman GD, Stanescu C, Gaman AM. Evaluation of parameters with potential prognosis impact in patients with primary gastric diffuse large B-cell lymphoma (PG-DLBCL). Romanian journal of morphology and embryology = Revue roumaine de morphologie et embryologie. 2014;55(1):15–21.PubMed
9.
go back to reference Choi ES, Kim HS, Han I. Elevated preoperative systemic inflammatory markers predict poor outcome in localized soft tissue sarcoma. Ann Surg Oncol. 2014;21(3):778–85.CrossRef Choi ES, Kim HS, Han I. Elevated preoperative systemic inflammatory markers predict poor outcome in localized soft tissue sarcoma. Ann Surg Oncol. 2014;21(3):778–85.CrossRef
10.
go back to reference Ma YM, Sun T, Liu YX, Zhao N, Gu Q, Zhang DF, Qie S, Ni CS, Liu Y, Sun BC. A pilot study on acute inflammation and cancer: a new balance between IFN-gamma and TGF-beta in melanoma. Journal of experimental & clinical cancer research : CR. 2009;28:23–36.CrossRef Ma YM, Sun T, Liu YX, Zhao N, Gu Q, Zhang DF, Qie S, Ni CS, Liu Y, Sun BC. A pilot study on acute inflammation and cancer: a new balance between IFN-gamma and TGF-beta in melanoma. Journal of experimental & clinical cancer research : CR. 2009;28:23–36.CrossRef
11.
go back to reference Kantor ED, Udumyan R, Signorello LB, Giovannucci EL, Montgomery S, Fall K. Adolescent body mass index and erythrocyte sedimentation rate in relation to colorectal cancer risk. Gut. 2016;65(8):1289–95.CrossRef Kantor ED, Udumyan R, Signorello LB, Giovannucci EL, Montgomery S, Fall K. Adolescent body mass index and erythrocyte sedimentation rate in relation to colorectal cancer risk. Gut. 2016;65(8):1289–95.CrossRef
12.
go back to reference Go DJ, Lee EY. Elevated Erythrocyte Sedimentation Rate Is Predictive of Interstitial Lung Disease and Mortality in Dermatomyositis. a Korean Retrospective Cohort Study. 2016;31(3):389–96. Go DJ, Lee EY. Elevated Erythrocyte Sedimentation Rate Is Predictive of Interstitial Lung Disease and Mortality in Dermatomyositis. a Korean Retrospective Cohort Study. 2016;31(3):389–96.
13.
go back to reference Sung HH, Jeon HG, Jeong BC, Seo SI, Jeon SS, Choi HY, Lee HM. Clinical significance of prognosis using the neutrophil-lymphocyte ratio and erythrocyte sedimentation rate in patients undergoing radical nephroureterectomy for upper urinary tract urothelial carcinoma. BJU Int. 2015;115(4):587–94.CrossRef Sung HH, Jeon HG, Jeong BC, Seo SI, Jeon SS, Choi HY, Lee HM. Clinical significance of prognosis using the neutrophil-lymphocyte ratio and erythrocyte sedimentation rate in patients undergoing radical nephroureterectomy for upper urinary tract urothelial carcinoma. BJU Int. 2015;115(4):587–94.CrossRef
14.
go back to reference Strojnik T, Smigoc T, Lah TT. Prognostic value of erythrocyte sedimentation rate and C-reactive protein in the blood of patients with glioma. Anticancer Res. 2014;34(1):339–47.PubMed Strojnik T, Smigoc T, Lah TT. Prognostic value of erythrocyte sedimentation rate and C-reactive protein in the blood of patients with glioma. Anticancer Res. 2014;34(1):339–47.PubMed
15.
go back to reference Stojan G, Fang H, Magder L, Petri M. Erythrocyte sedimentation rate is a predictor of renal and overall SLE disease activity. Lupus. 2013;22(8):827–34.CrossRef Stojan G, Fang H, Magder L, Petri M. Erythrocyte sedimentation rate is a predictor of renal and overall SLE disease activity. Lupus. 2013;22(8):827–34.CrossRef
16.
go back to reference Choi Y, Park B, Kim K, Jeong BC, Seo SI, Jeon SS, Choi HY, Lee JE, Lee HM. Erythrocyte sedimentation rate and anaemia are independent predictors of survival in patients with clear cell renal cell carcinoma. Br J Cancer. 2013;108(2):387–94.CrossRef Choi Y, Park B, Kim K, Jeong BC, Seo SI, Jeon SS, Choi HY, Lee JE, Lee HM. Erythrocyte sedimentation rate and anaemia are independent predictors of survival in patients with clear cell renal cell carcinoma. Br J Cancer. 2013;108(2):387–94.CrossRef
17.
go back to reference Hallermann C, Niermann C, Fischer RJ, Schulze HJ. Erythrocyte sedimentation rate as an independent prognostic factor in mycosis fungoides. Br J Dermatol. 2012;166(4):873–4.CrossRef Hallermann C, Niermann C, Fischer RJ, Schulze HJ. Erythrocyte sedimentation rate as an independent prognostic factor in mycosis fungoides. Br J Dermatol. 2012;166(4):873–4.CrossRef
18.
go back to reference Sengupta S, Lohse CM, Cheville JC, Leibovich BC, Thompson RH, Webster WS, Frank I, Zincke H, Blute ML, Kwon ED. The preoperative erythrocyte sedimentation rate is an independent prognostic factor in renal cell carcinoma. Cancer. 2006;106(2):304–12.CrossRef Sengupta S, Lohse CM, Cheville JC, Leibovich BC, Thompson RH, Webster WS, Frank I, Zincke H, Blute ML, Kwon ED. The preoperative erythrocyte sedimentation rate is an independent prognostic factor in renal cell carcinoma. Cancer. 2006;106(2):304–12.CrossRef
19.
go back to reference Johnson NA, Slack GW, Savage KJ, Connors JM, Ben-Neriah S, Rogic S, Scott DW, Tan KL, Steidl C, Sehn LH, et al. Concurrent expression of MYC and BCL2 in diffuse large B-cell lymphoma treated with rituximab plus cyclophosphamide, doxorubicin, vincristine, and prednisone. J Clin Oncol. 2012;30(28):3452–9.CrossRef Johnson NA, Slack GW, Savage KJ, Connors JM, Ben-Neriah S, Rogic S, Scott DW, Tan KL, Steidl C, Sehn LH, et al. Concurrent expression of MYC and BCL2 in diffuse large B-cell lymphoma treated with rituximab plus cyclophosphamide, doxorubicin, vincristine, and prednisone. J Clin Oncol. 2012;30(28):3452–9.CrossRef
20.
go back to reference Cheson BD, Fisher RI, Barrington SF, Cavalli F, Schwartz LH, Lister TA, Alliance AL, Lymphoma G, Eastern Cooperative Oncology G, European Mantle Cell Lymphoma C, et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014;32(27):3059–68.CrossRef Cheson BD, Fisher RI, Barrington SF, Cavalli F, Schwartz LH, Lister TA, Alliance AL, Lymphoma G, Eastern Cooperative Oncology G, European Mantle Cell Lymphoma C, et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014;32(27):3059–68.CrossRef
21.
go back to reference Elinav E, Nowarski R, Thaiss CA, Hu B, Jin C, Flavell RA. Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat Rev Cancer. 2013;13(11):759–71.CrossRef Elinav E, Nowarski R, Thaiss CA, Hu B, Jin C, Flavell RA. Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat Rev Cancer. 2013;13(11):759–71.CrossRef
22.
go back to reference Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74.CrossRef Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74.CrossRef
23.
go back to reference Hagerling C, Casbon AJ, Werb Z. Balancing the innate immune system in tumor development. Trends Cell Biol. 2015;25(4):214–20.CrossRef Hagerling C, Casbon AJ, Werb Z. Balancing the innate immune system in tumor development. Trends Cell Biol. 2015;25(4):214–20.CrossRef
24.
go back to reference Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140(6):883–99.CrossRef Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140(6):883–99.CrossRef
25.
go back to reference Karin M. Nuclear factor-kappaB in cancer development and progression. Nature. 2006;441(7092):431–6.CrossRef Karin M. Nuclear factor-kappaB in cancer development and progression. Nature. 2006;441(7092):431–6.CrossRef
26.
go back to reference Wu S, Rhee KJ, Albesiano E, Rabizadeh S, Wu X, Yen HR, Huso DL, Brancati FL, Wick E, McAllister F, et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med. 2009;15(9):1016–22.CrossRef Wu S, Rhee KJ, Albesiano E, Rabizadeh S, Wu X, Yen HR, Huso DL, Brancati FL, Wick E, McAllister F, et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med. 2009;15(9):1016–22.CrossRef
27.
go back to reference Litao MK, Kamat D. Erythrocyte sedimentation rate and C-reactive protein: how best to use them in clinical practice. Pediatr Ann. 2014;43(10):417–20.CrossRef Litao MK, Kamat D. Erythrocyte sedimentation rate and C-reactive protein: how best to use them in clinical practice. Pediatr Ann. 2014;43(10):417–20.CrossRef
28.
go back to reference Sagaert X, Van Cutsem E, De Hertogh G, Geboes K, Tousseyn T. Gastric MALT lymphoma: a model of chronic inflammation-induced tumor development. Nat Rev Gastroenterol Hepatol. 2010;7(6):336–46.CrossRef Sagaert X, Van Cutsem E, De Hertogh G, Geboes K, Tousseyn T. Gastric MALT lymphoma: a model of chronic inflammation-induced tumor development. Nat Rev Gastroenterol Hepatol. 2010;7(6):336–46.CrossRef
29.
go back to reference Loong F, Chan AC, Ho BC, Chau YP, Lee HY, Cheuk W, Yuen WK, Ng WS, Cheung HL, Chan JK. Diffuse large B-cell lymphoma associated with chronic inflammation as an incidental finding and new clinical scenarios. Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc. 2010;23(4):493–501.CrossRef Loong F, Chan AC, Ho BC, Chau YP, Lee HY, Cheuk W, Yuen WK, Ng WS, Cheung HL, Chan JK. Diffuse large B-cell lymphoma associated with chronic inflammation as an incidental finding and new clinical scenarios. Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc. 2010;23(4):493–501.CrossRef
30.
go back to reference Sun F, Zhu J, Lu S, Zhen Z, Wang J, Huang J, Ding Z, Zeng M, Sun X. An inflammation-based cumulative prognostic score system in patients with diffuse large B cell lymphoma in rituximab era. BMC Cancer. 2018;18(1):5–12.CrossRef Sun F, Zhu J, Lu S, Zhen Z, Wang J, Huang J, Ding Z, Zeng M, Sun X. An inflammation-based cumulative prognostic score system in patients with diffuse large B cell lymphoma in rituximab era. BMC Cancer. 2018;18(1):5–12.CrossRef
31.
go back to reference Hao X, Wei Y, Wei X, Zhou L, Wei Q, Zhang Y, Huang W, Feng R. Glasgow prognostic score is superior to other inflammation-based scores in predicting survival of diffuse large B-cell lymphoma. Oncotarget. 2017;8(44):76740–8.CrossRef Hao X, Wei Y, Wei X, Zhou L, Wei Q, Zhang Y, Huang W, Feng R. Glasgow prognostic score is superior to other inflammation-based scores in predicting survival of diffuse large B-cell lymphoma. Oncotarget. 2017;8(44):76740–8.CrossRef
32.
go back to reference Liu S, Ren J, Xia Q, Wu X, Han G, Ren H, Yan D, Wang G, Gu G, Li J. Preliminary case-control study to evaluate diagnostic values of C-reactive protein and erythrocyte sedimentation rate in differentiating active Crohn's disease from intestinal lymphoma, intestinal tuberculosis and Behcet's syndrome. Am J Med Sci. 2013;346(6):467–72.CrossRef Liu S, Ren J, Xia Q, Wu X, Han G, Ren H, Yan D, Wang G, Gu G, Li J. Preliminary case-control study to evaluate diagnostic values of C-reactive protein and erythrocyte sedimentation rate in differentiating active Crohn's disease from intestinal lymphoma, intestinal tuberculosis and Behcet's syndrome. Am J Med Sci. 2013;346(6):467–72.CrossRef
Metadata
Title
Inflammation marker ESR is effective in predicting outcome of diffuse large B-cell lymphoma
Authors
Shuang Wu
Ye Zhou
Hai-Ying Hua
Yan Zhang
Wen-Yan Zhu
Zhi-Qing Wang
Jin Li
Hua-Qiang Gao
Xiao-Hong Wu
Ting-Xun Lu
Dong Hua
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2018
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-018-4914-4

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