Skip to main content

Advertisement

SpringerLink
Log in

High numbers of tumor-associated macrophages correlate with poor prognosis in patients with mature T- and natural killer cell lymphomas

  • Original Paper
  • Published:
Medical Oncology Aims and scope Submit manuscript

Abstract

Various studies on lymphoma microenvironment have demonstrated the prognostic impact of tumor-associated macrophages (TAMs) in patients with B-cell lymphoma. Little is known about the correlation between TAMs and treatment outcome in mature T- and natural killer (NK) cell lymphomas. We analyzed the prognostic relevance of CD68+ TAMs by immunohistochemical analysis in 64 Chinese patients with mature T- and NK-cell lymphomas. Higher number of infiltrated TAMs was significantly related to B symptoms and extranodal involvement (p < 0.05). The TAMs content did not differ significantly between pathological subtypes. Using the mean value of TAMs per high-power field (hpf) as the cutoff point (87/hpf), 36 cases (56.2 %) were categorized as low level of TAMs content and 28 cases (43.8%) as high level. Patients with high level of TAMs content had a worse 5-year overall survival compared to those with low level (28.1 vs. 44.3 %, p = 0.039). In multivariate analysis, TAMs content remained an independent biological variable for survival distinct from the International Prognostic Index (Cox multivariate model, p = 0.009). High TAMs content indicated an adverse overall outcome in mature T- and NK-cell lymphomas. Our results show that expression of stromal TAMs may become a useful marker for prognosis of mature T- and NK-cell lymphomas.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Gonda TA, Tu S, Wang TC. Chronic inflammation, the tumor microenvironment and carcinogenesis. Cell Cycle. 2009;8:2005–13.

    Article  PubMed  CAS  Google Scholar 

  2. Mbeunkui F, Johann DJ Jr. Cancer and the tumor microenvironment: a review of an essential relationship. Cancer Chemother Pharmacol. 2009;63:571–82.

    Article  PubMed  Google Scholar 

  3. Siveen KS, Kuttan G. Role of macrophages in tumour progression. Immunol Lett. 2009;123:97–102.

    Article  PubMed  CAS  Google Scholar 

  4. Allavena P, Sica A, Solinas G, et al. The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages. Crit Rev Oncol Hematol. 2008;66:1–9.

    Article  PubMed  Google Scholar 

  5. Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006;66:605–12.

    Article  PubMed  CAS  Google Scholar 

  6. Dave SS, Wright G, Tan B, et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med. 2004;351:2159–69.

    Article  PubMed  CAS  Google Scholar 

  7. Farinha P, Masoudi H, Brian F, et al. Analysis of multiple biomarkers shows that lymphoma-associated macrophage (LAM) content is an independent predictor of survival in follicular lymphoma (FL). Blood. 2005;106:2169–74.

    Article  PubMed  CAS  Google Scholar 

  8. Alvaro T, Lejeune M, Salvadó MT, et al. Immunohistochemical patterns of reactive microenvironment are associated with clinicobiologic behavior in follicular lymphoma patients. J Clin Oncol. 2006;24:5350–7.

    Article  PubMed  Google Scholar 

  9. Kelley T, Beck R, Absi A, et al. Biologic predictors in follicular lymphoma: importance of markers of immune response. Leuk Lymphoma. 2007;48:2403–11.

    Article  PubMed  Google Scholar 

  10. Canioni D, Salles G, Mounier N, et al. 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. 2008;26:440–6.

    Article  PubMed  CAS  Google Scholar 

  11. de Jong D, Koster A, Hagenbeek A, et al. Impact of the tumor microenvironment on prognosis in follicular lymphoma is dependent on specific treatment protocols. Haematologica. 2009;94:70–7.

    Article  PubMed  Google Scholar 

  12. Hasselblom S, Hansson U, Sigurdardottir M, et al. Expression of CD68+ tumor-associated macrophages in patients with diffuse large B-cell lymphoma and its relation to prognosis. Pathol Int. 2008;58:529–32.

    Article  PubMed  Google Scholar 

  13. Cai QC, Liao H, Lin SX et al. High expression of tumor-infiltrating macrophages correlates with poor prognosis in patients with diffuse large B-cell lymphoma. Med Oncol. 2011; doi:10.1007/s12032-011-0123-6.

  14. Wada N, Zaki MA, Hori Y, et al. Tumour-associated macrophages in diffuse large B-cell lymphoma: a study of the Osaka Lymphoma Study Group. Histopathology. 2012;60:313–9.

    Article  PubMed  Google Scholar 

  15. Rüdiger T, Weisenburger DD, Anderson JR, et al. Peripheral T-cell lymphoma (excluding anaplastic large-cell lymphoma): results from the Non-Hodgkin’s Lymphoma Classification Project. Ann Oncol. 2002;13:140–9.

    Article  PubMed  Google Scholar 

  16. Au WY, Ma SY, Chim CS, et al. Clinicopathologic features and treatment outcome of mature T-cell and natural killer-cell lymphomas diagnosed according to the World Health Organization classification scheme: a single center experience of 10 years. Ann Oncol. 2005;16(2):206–14.

    Article  PubMed  Google Scholar 

  17. Iqbal J, Weisenburger DD, Greiner TC, et al. Molecular signatures to improve diagnosis in peripheral T-cell lymphoma and prognostication in angioimmunoblastic T-cell lymphoma. Blood. 2010;115:1026–36.

    Article  PubMed  CAS  Google Scholar 

  18. Armitage J, Vose J, Weisenburger D. International peripheral T-cell and natural killer/T-cell lymphoma study: pathology findings and clinical outcomes. J Clin Oncol. 2008;26:4124–30.

    Article  PubMed  Google Scholar 

  19. Delsol G (2008) WHO lymphoma classification. Ann Pathol. 2008;28 Spec No 1:S20–S24.

  20. Wilcox RA, Wada DA, Ziesmer SC, et al. Monocytes promote tumor cell survival in T-cell lymphoproliferative disorders and are impaired in their ability to differentiate into mature dendritic cells. Blood. 2009;114:2936–44.

    Article  PubMed  CAS  Google Scholar 

  21. Zhang W, Wang L, Zhou D, et al. Expression of tumor-associated macrophages and vascular endothelial growth factor correlates with poor prognosis of peripheral T-cell lymphoma, not otherwise specified. Leuk Lymphoma. 2011;52:46–52.

    Article  PubMed  CAS  Google Scholar 

  22. Niino D, Komohara Y, Murayama T, et al. Ratio of M2 macrophage expression is closely associated with poor prognosis for angioimmunoblastic T-cell lymphoma (AITL). Pathol Int. 2010;60:278–83.

    Article  PubMed  Google Scholar 

  23. Kawamura K, Komohara Y, Takaishi K, et al. Detection of M2 macrophages and colony-stimulating factor 1 expression in serous and mucinous ovarian epithelial tumors. Pathol Int. 2009;59:300–5.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank all the treating physicians in the Department of Medical Oncology, Cancer Center of Sun Yat-Sen University, for their assistance.

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Medical Oncology, The Third Affiliated Hospital of Sun Yat-Sen University, 600 Tian He Road, Guangzhou, Guangdong, People’s Republic of China

    Ze-Xiao Lin & Xiang-Yuan Wu

  2. State Key Laboratory of Oncology in Southern China, Department of Medical Oncology, Lymphoma Centre, Cancer Center of Sun Yat-Sen University, 651 Dong Feng Road East, Guangzhou, 510060, Guangdong, People’s Republic of China

    Bing Bai, Qi-Chun Cai, Qing-Qing Cai, Xiao-Xiao Wang & Hui-Qiang Huang

Authors
  1. Ze-Xiao Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bing Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qi-Chun Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qing-Qing Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiao-Xiao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiang-Yuan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hui-Qiang Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hui-Qiang Huang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lin, ZX., Bai, B., Cai, QC. et al. High numbers of tumor-associated macrophages correlate with poor prognosis in patients with mature T- and natural killer cell lymphomas. Med Oncol 29, 3522–3528 (2012). https://doi.org/10.1007/s12032-012-0244-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12032-012-0244-6

Keywords

Search

Navigation