Skip to main content
Top
Published in: Annals of Hematology 9/2015

01-09-2015 | Original Article

High numbers of CD68+ tumor-associated macrophages correlate with poor prognosis in extranodal NK/T-cell lymphoma, nasal type

Authors: Hua Wang, Pengfei Li, Liang Wang, Zhongjun Xia, HuiQiang Huang, Yue Lu, ZhiMing Li

Published in: Annals of Hematology | Issue 9/2015

Login to get access

Abstract

Many studies have demonstrated that tumor-associated macrophages (TAMs) were a prognostic indicator in patients with B cell lymphoma. But, we know little about the clinical significance of TAMs in extranodal natural killer/T cell lymphoma(ENKTL), nasal type. CD68 expression was detected using immunohistochemistry to determine the numbers of TAMs in 70 ENKTL patients, and the data were used to evaluate its relationship with clinicopathological features, treatment response, and prognosis. Patients with high number of infiltrated CD68+ TAMs (>60/hpf) at diagnosis tended to have more adverse clinical characteristics. Patients with low CD68+ TAM content (<60/hpf) at diagnosis had better overall survival (P = 0.003) and progression-free survival (P = 0.002) and achieved higher complete remission rates (P = 0.008). Multivariate analysis revealed that CD68 + TAM content, Ki-67 index, and stage III and IV were independent prognostic factors for both OS and PFS. Using the International Prognostic Index or Korean Prognostic Index for extranodal NK/T cell lymphoma, nasal type, the majority of patients were in the low-risk category. CD68 + TAM content was helpful to differentiate the low-risk patients with different survival outcomes. Our data suggest that CD68+ TAM content at diagnosis is a powerful predictor of prognosis for ENKTL, which suggests a role for TAMs in the pathogenesis of this disease and offers new insight into potential therapeutic strategies.
Appendix
Available only for authorised users
Literature
3.
6.
go back to reference Steidl C, Lee T, Shah SP, Farinha P, Han G, Nayar T, Delaney A, Jones SJ, Iqbal J, Weisenburger DD, Bast MA, Rosenwald A, Muller-Hermelink HK, Rimsza LM, Campo E, Delabie J, Braziel RM, Cook JR, Tubbs RR, Jaffe ES, Lenz G, Connors JM, Staudt LM, Chan WC, Gascoyne RD (2010) Tumor-associated macrophages and survival in classic Hodgkin's lymphoma. N Engl J Med 362(10):875–885. doi:10.1056/NEJMoa0905680 PubMedCentralPubMedCrossRef Steidl C, Lee T, Shah SP, Farinha P, Han G, Nayar T, Delaney A, Jones SJ, Iqbal J, Weisenburger DD, Bast MA, Rosenwald A, Muller-Hermelink HK, Rimsza LM, Campo E, Delabie J, Braziel RM, Cook JR, Tubbs RR, Jaffe ES, Lenz G, Connors JM, Staudt LM, Chan WC, Gascoyne RD (2010) Tumor-associated macrophages and survival in classic Hodgkin's lymphoma. N Engl J Med 362(10):875–885. doi:10.​1056/​NEJMoa0905680 PubMedCentralPubMedCrossRef
7.
go back to reference Tan KL, Scott DW, Hong F, Kahl BS, Fisher RI, Bartlett NL, Advani RH, Buckstein R, Rimsza LM, Connors JM, Steidl C, Gordon LI, Horning SJ, Gascoyne RD (2012) Tumor-associated macrophages predict inferior outcomes in classic Hodgkin lymphoma: a correlative study from the E2496 Intergroup trial. Blood 120(16):3280–3287. doi:10.1182/blood-2012-04-421057 PubMedCentralPubMedCrossRef Tan KL, Scott DW, Hong F, Kahl BS, Fisher RI, Bartlett NL, Advani RH, Buckstein R, Rimsza LM, Connors JM, Steidl C, Gordon LI, Horning SJ, Gascoyne RD (2012) Tumor-associated macrophages predict inferior outcomes in classic Hodgkin lymphoma: a correlative study from the E2496 Intergroup trial. Blood 120(16):3280–3287. doi:10.​1182/​blood-2012-04-421057 PubMedCentralPubMedCrossRef
8.
go back to reference Agur A, Amir G, Paltiel O, Klein M, Dann EJ, Goldschmidt H, Goldschmidt N (2014) CD68 staining correlates with the size of residual mass but not with survival in classical Hodgkin lymphoma. Leuk Lymphoma:1–5. doi:10.3109/10428194.2014.963081 Agur A, Amir G, Paltiel O, Klein M, Dann EJ, Goldschmidt H, Goldschmidt N (2014) CD68 staining correlates with the size of residual mass but not with survival in classical Hodgkin lymphoma. Leuk Lymphoma:1–5. doi:10.​3109/​10428194.​2014.​963081
9.
go back to reference Dave SS, Wright G, Tan B, Rosenwald A, Gascoyne RD, Chan WC, Fisher RI, Braziel RM, Rimsza LM, Grogan TM, Miller TP, LeBlanc M, Greiner TC, Weisenburger DD, Lynch JC, Vose J, Armitage JO, Smeland EB, Kvaloy S, Holte H, Delabie J, Connors JM, Lansdorp PM, Ouyang Q, Lister TA, Davies AJ, Norton AJ, Muller-Hermelink HK, Ott G, Campo E, Montserrat E, Wilson WH, Jaffe ES, Simon R, Yang L, Powell J, Zhao H, Goldschmidt N, Chiorazzi M, Staudt LM (2004) Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med 351(21):2159–2169. doi:10.1056/NEJMoa041869 PubMedCrossRef Dave SS, Wright G, Tan B, Rosenwald A, Gascoyne RD, Chan WC, Fisher RI, Braziel RM, Rimsza LM, Grogan TM, Miller TP, LeBlanc M, Greiner TC, Weisenburger DD, Lynch JC, Vose J, Armitage JO, Smeland EB, Kvaloy S, Holte H, Delabie J, Connors JM, Lansdorp PM, Ouyang Q, Lister TA, Davies AJ, Norton AJ, Muller-Hermelink HK, Ott G, Campo E, Montserrat E, Wilson WH, Jaffe ES, Simon R, Yang L, Powell J, Zhao H, Goldschmidt N, Chiorazzi M, Staudt LM (2004) Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med 351(21):2159–2169. doi:10.​1056/​NEJMoa041869 PubMedCrossRef
10.
go back to reference Alvaro T, Lejeune M, Camacho FI, Salvado MT, Sanchez L, Garcia JF, Lopez C, Jaen J, Bosch R, Pons LE, Bellas C, Piris MA (2006) The presence of STAT1-positive tumor-associated macrophages and their relation to outcome in patients with follicular lymphoma. Haematologica 91(12):1605–1612PubMed Alvaro T, Lejeune M, Camacho FI, Salvado MT, Sanchez L, Garcia JF, Lopez C, Jaen J, Bosch R, Pons LE, Bellas C, Piris MA (2006) The presence of STAT1-positive tumor-associated macrophages and their relation to outcome in patients with follicular lymphoma. Haematologica 91(12):1605–1612PubMed
11.
go back to reference Canioni D, Salles G, Mounier N, Brousse N, Keuppens M, Morchhauser F, Lamy T, Sonet A, Rousselet MC, Foussard C, Xerri L (2008) High numbers of tumor-associated macrophages have an adverse prognostic value that can be circumvented by rituximab in patients with follicular lymphoma enrolled onto the GELA-GOELAMS FL-2000 trial. J Clin Oncol : Off J Am Soc Clin Oncol 26(3):440–446. doi:10.1200/jco.2007.12.8298 CrossRef Canioni D, Salles G, Mounier N, Brousse N, Keuppens M, Morchhauser F, Lamy T, Sonet A, Rousselet MC, Foussard C, Xerri L (2008) High numbers of tumor-associated macrophages have an adverse prognostic value that can be circumvented by rituximab in patients with follicular lymphoma enrolled onto the GELA-GOELAMS FL-2000 trial. J Clin Oncol : Off J Am Soc Clin Oncol 26(3):440–446. doi:10.​1200/​jco.​2007.​12.​8298 CrossRef
12.
go back to reference de Jong D, Koster A, Hagenbeek A, Raemaekers J, Veldhuizen D, Heisterkamp S, de Boer JP, van Glabbeke M (2009) Impact of the tumor microenvironment on prognosis in follicular lymphoma is dependent on specific treatment protocols. Haematologica 94(1):70–77. doi:10.3324/haematol.13574 PubMedCentralPubMedCrossRef de Jong D, Koster A, Hagenbeek A, Raemaekers J, Veldhuizen D, Heisterkamp S, de Boer JP, van Glabbeke M (2009) Impact of the tumor microenvironment on prognosis in follicular lymphoma is dependent on specific treatment protocols. Haematologica 94(1):70–77. doi:10.​3324/​haematol.​13574 PubMedCentralPubMedCrossRef
13.
go back to reference Cai QC, Liao H, Lin SX, Xia Y, Wang XX, Gao Y, Lin ZX, Lu JB, Huang HQ (2012) High expression of tumor-infiltrating macrophages correlates with poor prognosis in patients with diffuse large B-cell lymphoma. Med Oncol (Northwood, London, England) 29(4):2317–2322. doi:10.1007/s12032-011-0123-6 CrossRef Cai QC, Liao H, Lin SX, Xia Y, Wang XX, Gao Y, Lin ZX, Lu JB, Huang HQ (2012) High expression of tumor-infiltrating macrophages correlates with poor prognosis in patients with diffuse large B-cell lymphoma. Med Oncol (Northwood, London, England) 29(4):2317–2322. doi:10.​1007/​s12032-011-0123-6 CrossRef
14.
go back to reference Yamamoto W, Nakamura N, Tomita N, Takeuchi K, Ishii Y, Takahashi H, Watanabe R, Takasaki H, Motomura S, Kobayashi S, Yokose T, Ishigatsubo Y, Sakai R (2014) Human leukocyte antigen-DR expression on flow cytometry and tumor-associated macrophages in diffuse large B-cell lymphoma treated by rituximab, cyclophosphamide, doxorubicin, vincristine and prednisone therapy: retrospective cohort study. Leuk Lymphoma 55(12):2721–2727. doi:10.3109/10428194.2014.893311 PubMedCrossRef Yamamoto W, Nakamura N, Tomita N, Takeuchi K, Ishii Y, Takahashi H, Watanabe R, Takasaki H, Motomura S, Kobayashi S, Yokose T, Ishigatsubo Y, Sakai R (2014) Human leukocyte antigen-DR expression on flow cytometry and tumor-associated macrophages in diffuse large B-cell lymphoma treated by rituximab, cyclophosphamide, doxorubicin, vincristine and prednisone therapy: retrospective cohort study. Leuk Lymphoma 55(12):2721–2727. doi:10.​3109/​10428194.​2014.​893311 PubMedCrossRef
16.
go back to reference Au WY, Weisenburger DD, Intragumtornchai T, Nakamura S, Kim WS, Sng I, Vose J, Armitage JO, Liang R (2009) Clinical differences between nasal and extranasal natural killer/T-cell lymphoma: a study of 136 cases from the International Peripheral T-Cell Lymphoma Project. Blood 113(17):3931–3937. doi:10.1182/blood-2008-10-185256 PubMedCrossRef Au WY, Weisenburger DD, Intragumtornchai T, Nakamura S, Kim WS, Sng I, Vose J, Armitage JO, Liang R (2009) Clinical differences between nasal and extranasal natural killer/T-cell lymphoma: a study of 136 cases from the International Peripheral T-Cell Lymphoma Project. Blood 113(17):3931–3937. doi:10.​1182/​blood-2008-10-185256 PubMedCrossRef
17.
go back to reference Lee J, Suh C, Park YH, Ko YH, Bang SM, Lee JH, Lee DH, Huh J, Oh SY, Kwon HC, Kim HJ, Lee SI, Kim JH, Park J, Oh SJ, Kim K, Jung C, Park K, Kim WS (2006) Extranodal natural killer T-cell lymphoma, nasal-type: a prognostic model from a retrospective multicenter study. J Clin Oncol : Off J Am Soc Clin Oncol 24(4):612–618. doi:10.1200/jco.2005.04.1384 CrossRef Lee J, Suh C, Park YH, Ko YH, Bang SM, Lee JH, Lee DH, Huh J, Oh SY, Kwon HC, Kim HJ, Lee SI, Kim JH, Park J, Oh SJ, Kim K, Jung C, Park K, Kim WS (2006) Extranodal natural killer T-cell lymphoma, nasal-type: a prognostic model from a retrospective multicenter study. J Clin Oncol : Off J Am Soc Clin Oncol 24(4):612–618. doi:10.​1200/​jco.​2005.​04.​1384 CrossRef
18.
go back to reference Sun J, Yang Q, Lu Z, He M, Gao L, Zhu M, Sun L, Wei L, Li M, Liu C, Zheng J, Liu W, Li G, Chen J (2012) Distribution of lymphoid neoplasms in China: analysis of 4,638 cases according to the World Health Organization classification. Am J Clin Pathol 138(3):429–434. doi:10.1309/ajcp7yltqpusdq5c PubMedCrossRef Sun J, Yang Q, Lu Z, He M, Gao L, Zhu M, Sun L, Wei L, Li M, Liu C, Zheng J, Liu W, Li G, Chen J (2012) Distribution of lymphoid neoplasms in China: analysis of 4,638 cases according to the World Health Organization classification. Am J Clin Pathol 138(3):429–434. doi:10.​1309/​ajcp7yltqpusdq5c​ PubMedCrossRef
19.
go back to reference Huang JJ, Jiang WQ, Lin TY, Huang Y, Xu RH, Huang HQ, Li ZM (2011) Absolute lymphocyte count is a novel prognostic indicator in extranodal natural killer/T-cell lymphoma, nasal type. Ann Oncol : Off J Eur Soc Med Oncol / ESMO 22(1):149–155. doi:10.1093/annonc/mdq314 CrossRef Huang JJ, Jiang WQ, Lin TY, Huang Y, Xu RH, Huang HQ, Li ZM (2011) Absolute lymphocyte count is a novel prognostic indicator in extranodal natural killer/T-cell lymphoma, nasal type. Ann Oncol : Off J Eur Soc Med Oncol / ESMO 22(1):149–155. doi:10.​1093/​annonc/​mdq314 CrossRef
22.
go back to reference Lee J, Park YH, Kim WS, Lee SS, Ryoo BY, Yang SH, Park KW, Kang JH, Park JO, Lee SH, Kim K, Jung CW, Park YS, Im YH, Kang WK, Lee MH, Ko YH, Ahn YC, Park K (2005) Extranodal nasal type NK/T-cell lymphoma: elucidating clinical prognostic factors for risk-based stratification of therapy. Eur J Cancer (Oxford, England : 1990) 41(10):1402–1408. doi:10.1016/j.ejca.2005.03.010 CrossRef Lee J, Park YH, Kim WS, Lee SS, Ryoo BY, Yang SH, Park KW, Kang JH, Park JO, Lee SH, Kim K, Jung CW, Park YS, Im YH, Kang WK, Lee MH, Ko YH, Ahn YC, Park K (2005) Extranodal nasal type NK/T-cell lymphoma: elucidating clinical prognostic factors for risk-based stratification of therapy. Eur J Cancer (Oxford, England : 1990) 41(10):1402–1408. doi:10.​1016/​j.​ejca.​2005.​03.​010 CrossRef
23.
go back to reference Wang H, Wuxiao ZJ, Zhu J, Wang Z, Wang KF, Li S, Chen X, Lu Y, Xia ZJ (2014) Comparison of gemcitabine, oxaliplatin and L-asparaginase and etoposide, vincristine, doxorubicin, cyclophosphamide and prednisone as first-line chemotherapy in patients with stage IE to IIE extranodal natural killer/T-cell lymphoma: a multicenter retrospective study. Leuk Lymphoma:1–7. doi:10.3109/10428194.2014.939964 Wang H, Wuxiao ZJ, Zhu J, Wang Z, Wang KF, Li S, Chen X, Lu Y, Xia ZJ (2014) Comparison of gemcitabine, oxaliplatin and L-asparaginase and etoposide, vincristine, doxorubicin, cyclophosphamide and prednisone as first-line chemotherapy in patients with stage IE to IIE extranodal natural killer/T-cell lymphoma: a multicenter retrospective study. Leuk Lymphoma:1–7. doi:10.​3109/​10428194.​2014.​939964
24.
go back to reference Cheson BD, Horning SJ, Coiffier B, Shipp MA, Fisher RI, Connors JM, Lister TA, Vose J, Grillo-Lopez A, Hagenbeek A, Cabanillas F, Klippensten D, Hiddemann W, Castellino R, Harris NL, Armitage JO, Carter W, Hoppe R, Canellos GP (1999) Report of an international workshop to standardize response criteria for non-Hodgkin's lymphomas. NCI Sponsored International Working Group. J Clin Oncol : Off J Am Soc Clin Oncol 17(4):1244 Cheson BD, Horning SJ, Coiffier B, Shipp MA, Fisher RI, Connors JM, Lister TA, Vose J, Grillo-Lopez A, Hagenbeek A, Cabanillas F, Klippensten D, Hiddemann W, Castellino R, Harris NL, Armitage JO, Carter W, Hoppe R, Canellos GP (1999) Report of an international workshop to standardize response criteria for non-Hodgkin's lymphomas. NCI Sponsored International Working Group. J Clin Oncol : Off J Am Soc Clin Oncol 17(4):1244
28.
go back to reference Ishii H, Takahara M, Nagato T, Kis LL, Nagy N, Kishibe K, Harabuchi Y, Klein E (2012) Monocytes enhance cell proliferation and LMP1 expression of nasal natural killer/T-cell lymphoma cells by cell contact-dependent interaction through membrane-bound IL-15. Int J Cancer 130(1):48–58. doi:10.1002/ijc.25969 PubMedCrossRef Ishii H, Takahara M, Nagato T, Kis LL, Nagy N, Kishibe K, Harabuchi Y, Klein E (2012) Monocytes enhance cell proliferation and LMP1 expression of nasal natural killer/T-cell lymphoma cells by cell contact-dependent interaction through membrane-bound IL-15. Int J Cancer 130(1):48–58. doi:10.​1002/​ijc.​25969 PubMedCrossRef
29.
go back to reference Wang H, Zhu JY, Liu CC, Zhu MY, Wang JH, Geng QR, Lu Y (2015) Increased serum levels of interleukin-15 correlate with negative prognostic factors in extranodal NK/T cell lymphoma. Med Oncol (Northwood, London, England) 32(1):370. doi:10.1007/s12032-014-0370-4 CrossRef Wang H, Zhu JY, Liu CC, Zhu MY, Wang JH, Geng QR, Lu Y (2015) Increased serum levels of interleukin-15 correlate with negative prognostic factors in extranodal NK/T cell lymphoma. Med Oncol (Northwood, London, England) 32(1):370. doi:10.​1007/​s12032-014-0370-4 CrossRef
30.
go back to reference Lin ZX, Bai B, Cai QC, Cai QQ, Wang XX, Wu XY, Huang HQ (2012) High numbers of tumor-associated macrophages correlate with poor prognosis in patients with mature T- and natural killer cell lymphomas. Med Oncol (Northwood, London, England) 29(5):3522–3528. doi:10.1007/s12032-012-0244-6 CrossRef Lin ZX, Bai B, Cai QC, Cai QQ, Wang XX, Wu XY, Huang HQ (2012) High numbers of tumor-associated macrophages correlate with poor prognosis in patients with mature T- and natural killer cell lymphomas. Med Oncol (Northwood, London, England) 29(5):3522–3528. doi:10.​1007/​s12032-012-0244-6 CrossRef
31.
go back to reference Liu Y, Fan L, Wang Y, Li P, Zhu J, Wang L, Zhang W, Zhang Y, Huang G (2014) Tumor-associated macrophages promote tumor cell proliferation in nasopharyngeal NK/T-cell lymphoma. Int J Clin Exp Pathol 7(9):5429–5435PubMedCentralPubMed Liu Y, Fan L, Wang Y, Li P, Zhu J, Wang L, Zhang W, Zhang Y, Huang G (2014) Tumor-associated macrophages promote tumor cell proliferation in nasopharyngeal NK/T-cell lymphoma. Int J Clin Exp Pathol 7(9):5429–5435PubMedCentralPubMed
32.
go back to reference Jiang L, Li P, Wang H, Liu J, Zhang X, Qiu H, Zhang B (2014) Prognostic significance of Ki-67 antigen expression in extranodal natural killer/T-cell lymphoma, nasal type. Med Oncol (Northwood, London, England) 31(10):218. doi:10.1007/s12032-014-0218-y CrossRef Jiang L, Li P, Wang H, Liu J, Zhang X, Qiu H, Zhang B (2014) Prognostic significance of Ki-67 antigen expression in extranodal natural killer/T-cell lymphoma, nasal type. Med Oncol (Northwood, London, England) 31(10):218. doi:10.​1007/​s12032-014-0218-y CrossRef
34.
go back to reference Alvaro T, Lejeune M, Salvado MT, Lopez C, Jaen J, Bosch R, Pons LE (2006) Immunohistochemical patterns of reactive microenvironment are associated with clinicobiologic behavior in follicular lymphoma patients. J Clin Oncol : Off J Am Soc Clin Oncol 24(34):5350–5357. doi:10.1200/jco.2006.06.4766 CrossRef Alvaro T, Lejeune M, Salvado MT, Lopez C, Jaen J, Bosch R, Pons LE (2006) Immunohistochemical patterns of reactive microenvironment are associated with clinicobiologic behavior in follicular lymphoma patients. J Clin Oncol : Off J Am Soc Clin Oncol 24(34):5350–5357. doi:10.​1200/​jco.​2006.​06.​4766 CrossRef
35.
go back to reference Farinha P, Masoudi H, Skinnider BF, Shumansky K, Spinelli JJ, Gill K, Klasa R, Voss N, Connors JM, Gascoyne RD (2005) Analysis of multiple biomarkers shows that lymphoma-associated macrophage (LAM) content is an independent predictor of survival in follicular lymphoma (FL). Blood 106(6):2169–2174. doi:10.1182/blood-2005-04-1565 PubMedCrossRef Farinha P, Masoudi H, Skinnider BF, Shumansky K, Spinelli JJ, Gill K, Klasa R, Voss N, Connors JM, Gascoyne RD (2005) Analysis of multiple biomarkers shows that lymphoma-associated macrophage (LAM) content is an independent predictor of survival in follicular lymphoma (FL). Blood 106(6):2169–2174. doi:10.​1182/​blood-2005-04-1565 PubMedCrossRef
38.
go back to reference Wada N, Zaki MA, Hori Y, Hashimoto K, Tsukaguchi M, Tatsumi Y, Ishikawa J, Tominaga N, Sakoda H, Take H, Tsudo M, Kuwayama M, Morii E, Aozasa K (2012) Tumour-associated macrophages in diffuse large B-cell lymphoma: a study of the Osaka Lymphoma Study Group. Histopathology 60(2):313–319. doi:10.1111/j.1365-2559.2011.04096.x PubMedCrossRef Wada N, Zaki MA, Hori Y, Hashimoto K, Tsukaguchi M, Tatsumi Y, Ishikawa J, Tominaga N, Sakoda H, Take H, Tsudo M, Kuwayama M, Morii E, Aozasa K (2012) Tumour-associated macrophages in diffuse large B-cell lymphoma: a study of the Osaka Lymphoma Study Group. Histopathology 60(2):313–319. doi:10.​1111/​j.​1365-2559.​2011.​04096.​x PubMedCrossRef
39.
go back to reference Nakagawa J, Saio M, Tamakawa N, Suwa T, Frey AB, Nonaka K, Umemura N, Imai H, Ouyang GF, Ohe N, Yano H, Yoshimura S, Iwama T, Takami T (2007) TNF expressed by tumor-associated macrophages, but not microglia, can eliminate glioma. Int J Oncol 30(4):803–811PubMed Nakagawa J, Saio M, Tamakawa N, Suwa T, Frey AB, Nonaka K, Umemura N, Imai H, Ouyang GF, Ohe N, Yano H, Yoshimura S, Iwama T, Takami T (2007) TNF expressed by tumor-associated macrophages, but not microglia, can eliminate glioma. Int J Oncol 30(4):803–811PubMed
40.
go back to reference Zhang W, Wang L, Zhou D, Cui Q, Zhao D, Wu Y (2011) Expression of tumor-associated macrophages and vascular endothelial growth factor correlates with poor prognosis of peripheral T-cell lymphoma, not otherwise specified. Leuk Lymphoma 52(1):46–52. doi:10.3109/10428194.2010.529204 PubMedCrossRef Zhang W, Wang L, Zhou D, Cui Q, Zhao D, Wu Y (2011) Expression of tumor-associated macrophages and vascular endothelial growth factor correlates with poor prognosis of peripheral T-cell lymphoma, not otherwise specified. Leuk Lymphoma 52(1):46–52. doi:10.​3109/​10428194.​2010.​529204 PubMedCrossRef
Metadata
Title
High numbers of CD68+ tumor-associated macrophages correlate with poor prognosis in extranodal NK/T-cell lymphoma, nasal type
Authors
Hua Wang
Pengfei Li
Liang Wang
Zhongjun Xia
HuiQiang Huang
Yue Lu
ZhiMing Li
Publication date
01-09-2015
Publisher
Springer Berlin Heidelberg
Published in
Annals of Hematology / Issue 9/2015
Print ISSN: 0939-5555
Electronic ISSN: 1432-0584
DOI
https://doi.org/10.1007/s00277-015-2401-4

Other articles of this Issue 9/2015

Annals of Hematology 9/2015 Go to the issue