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Prognostic implication of types of tumor-associated macrophages in Hodgkin lymphoma

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Abstract

To evaluate roles of tumor-associated macrophages (TAMs) for prognosis of classical Hodgkin lymphoma (CHL). Expression of markers for TAMs, CD68, HLA-DR, CD163, HLA-DR/CD68 (M1), and CD163/CD68 (M2) was immunohistochemically examined in 82 cases with CHL. Positively stained cells were counted and correlation of number of TAMs and patients’ survival time was analyzed. Number of CD163+ cells and M2 cells was significantly correlated with shorter overall survival (P < 0.05), while it was marginally significant for CD68+ cells (P = 0.0827). HLA-DR + cells and M1 cells showed no significant correlation with overall survival. When confined to mixed cellularity subtype, number of M1 cells was correlated with favorable prognosis (P < 0.05), while M2 did not (P = 0.7). Older age and male sex were unfavorable factors for prognosis. At multivariate analysis, number of CD163+ cells, M2+ cells, and age were independent factors for poor overall survival (P = 0.03, 0.02, and 0.01, respectively). CD163+ cells and M2 cells might work to be tumor promotive in CHL. M1 cells might be tumor suppressive in mixed cellularity type.

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References

  1. Fermé C, Eghbali H, Meerwaldt JH, Rieux C, Bosq J, Berger F, Girinsky T, Brice P, van’t Veer MB, Walewski JA, Lederlin P, Tirelli U, Carde P, Van den Neste E, Gyan E, Monconduit M, Diviné M, Raemaekers JM, Salles G, Noordijk EM, Creemers GJ, Gabarre J, Hagenbeek A, Reman O, Blanc M, Thomas J, Vié B, Kluin-Nelemans JC, Viseu F, Baars JW, Poortmans P, Lugtenburg PJ, Carrie C, Jaubert J, Henry-Amar M (2007) Chemotherapy plus involved-field radiation in early-stage Hodgkin’s disease. N Engl J Med 357:1916–1927

    Article  PubMed  Google Scholar 

  2. Ansell SM, Armitage JO (2006) Management of Hodgkin lymphoma. Mayo Clin Proc 81:419–426

    Article  PubMed  Google Scholar 

  3. Lewis CE, Pollard JW (2006) Distinct role of macrophages in different tumor microenvironments. Cancer Res 66:605–612

    Article  PubMed  CAS  Google Scholar 

  4. 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 362:875–885

    Article  PubMed  CAS  Google Scholar 

  5. Buddingh EP, Kuijjer ML, Duim RA, Bürger H, Agelopoulos K, Myklebost O, Serra M, Mertens F, Hogendoorn PC, Lankester AC, Cleton-Jansen AM (2011) Tumor-infiltrating macrophages are associated with metastasis suppression in high-grade osteosarcoma: a rationale for treatment with macrophage activating agents. Clin Cancer Res 17:2110–2119

    Article  PubMed  CAS  Google Scholar 

  6. Dai F, Liu L, Che G, Yu N, Pu Q, Zhang S, Ma J, Ma L, You Z (2010) The number and microlocalization of tumor-associated immune cells are associated with patient’s survival time in non-small cell lung Cancer. BMC Cancer. 10: 220. Available at: http://www.biomedcentral.com/1471-2407/10/220

    Article  PubMed  Google Scholar 

  7. Jensen TO, Schmidt H, Møller HJ, Høyer M, Maniecki MB, Sjoegren P, Christensen IJ, Steiniche T (2009) Macrophage markers in serum and tumor have prognostic impact in American Joint Committee on Cancer stage I/II melanoma. J Clin Oncol 7:3330–3337

    Article  Google Scholar 

  8. Ma J, Liu L, Che G, Yu N, Dai F, You Z. (2010) The M1 form of tumor-associated macrophages in non-small cell lung cancer is positively associated with survival time. BMC Cancer. 10:112. Available at: http://www.biomedcentral.com/1471-2407/10/112

    Article  PubMed  Google Scholar 

  9. Glaser SL, Hsu JL (2002) Hodgkin’s disease in Asians: incidence patterns and risk factors in population-based data. Leuk Res 26:261–269

    Article  PubMed  Google Scholar 

  10. Aozasa K, Ueda T, Tamai M, Tsujimura T (1986) Hodgkin’s disease in Osaka, Japan (1964–1985). Eur J Cancer Clin Oncol 22:1117–1119

    Article  PubMed  CAS  Google Scholar 

  11. Tjiu JW, Chen JS, Shun CT, Lin SJ, Liao YH, Chu CY, Tsai TF, Chiu HC, Dai YS, Inoue H, Yang PC, Kuo ML, Jee SH (2009) Tumor-associated macrophage-induced invasion and angiogenesis of human basal cell carcinoma cells by cyclooxygenase-2 induction. J Invest Dermatol 129:1016–1025

    Article  PubMed  CAS  Google Scholar 

  12. Lamagna C, Aurrand-Lions M, Imhof BA (2006) Dual role of macrophages in tumor growth and angiogenesis. J Leuk Biol 80:705–713

    Article  CAS  Google Scholar 

  13. Al-Sarireh B, Eremin O (2004) Tumor-associated macrophages (TAMS): disordered function, immune suppression and progressive tumour growth. J R Coll Surg Edinb 5:1–16

    Google Scholar 

  14. Caux C, Vanbervliet B, Massacrier C, Dezutter-Dambuyant C, de Saint-Vis B, Jacquet C, Yoneda K, Imamura S, Schmitt D, Banchereau J (1996) CD34+ hematopoietic progenitors from human cord blood differentiate along two independent dendritic cell pathways in response to GM-CSF + TNF alpha. J Exp Med 184:695–706

    Article  PubMed  CAS  Google Scholar 

  15. Nakamura H, Saji H, Aute I, Kawasaki N, Hosaka M, Ogata A, Saijo T, Kato H (2003) Peripheral leukocytes with HLA-DR+/CD8-phenotype are associated with prognosis in patients with lung cancer. Anticancer Res 23:4149–4152

    PubMed  Google Scholar 

  16. Maniecki MB, Møller HJ, Moestrup SK, Møller BK (2006) CD163 positive subsets of blood dendritic cells: the scavenging macrophage receptors CD163 and CD91 are coexpressed on human dendritic cells and monocytes. Immunobiology 211:407–417

    Article  PubMed  CAS  Google Scholar 

  17. Kamper P, Bendix K, Hamilton-Dutoit S, Honoré B, Nyengaard JR, d’Amore F (2011) Tumor-infiltrating macrophages correlate with adverse prognosis and Epstein–Barr virus status in classical Hodgkin’s lymphoma. Haematologica 96:269–276

    Article  PubMed  Google Scholar 

  18. Lee CH, Espinosa I, Vrijaldenhoven S, Subramanian S, Montgomery KD, Zhu S et al (2008) Prognostic significance of macrophage infiltration in leiomyosarcomas. Clin Cancer Res 14:1423–1430

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors thank Ms. M. Tone, T. Sawamura, M. Sugano, and E. Maeno for their technical assistance.

This work was supported by grants from the Ministry of Education, Culture, Sports, Science and Technology, Japan (#20590364, #20014010).

Author information

Authors and Affiliations

  1. Department of Pathology (C3), Osaka University Graduate School of Medicine, 2-2 Yamadaoka, Suita, Osaka, 565-0871, Japan

    Mona A. A. Zaki, Naoki Wada, Junichiro Ikeda, Eiichi Morii & Katsuyuki Aozasa

  2. Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Osaka, Japan

    Hirohiko Shibayama

  3. Department of Internal Medicine, Kansai Rosai Hospital, Amagasaki, Hyogo, Japan

    Koji Hashimoto

  4. Department of Hematology, NTT West Osaka Hospital, Osaka, Japan

    Tamotsu Yamagami

  5. Department of Hematology, Kinki University School of Medicine, Osakasayama, Osaka, Japan

    Yoichi Tatsumi

  6. Department of Hematology, Sakai Municipal Hospital, Sakai, Osaka, Japan

    Machiko Tsukaguchi

  7. Department of Internal Medicine, Toyonaka Municipal Hospital, Toyonaka, Osaka, Japan

    Hironori Take

  8. Department of Hematology, Osaka Red Cross Hospital, Osaka, Japan

    Mitsuru Tsudo

Authors
  1. Mona A. A. Zaki
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  2. Naoki Wada
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  3. Junichiro Ikeda
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  5. Koji Hashimoto
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  6. Tamotsu Yamagami
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  7. Yoichi Tatsumi
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  8. Machiko Tsukaguchi
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  9. Hironori Take
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  10. Mitsuru Tsudo
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  11. Eiichi Morii
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  12. Katsuyuki Aozasa
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Corresponding author

Correspondence to Katsuyuki Aozasa.

Additional information

Mona A.A. Zaki and Naoki Wada equally contributed to this study.

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Zaki, M.A.A., Wada, N., Ikeda, J. et al. Prognostic implication of types of tumor-associated macrophages in Hodgkin lymphoma. Virchows Arch 459, 361–366 (2011). https://doi.org/10.1007/s00428-011-1140-8

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  • DOI: https://doi.org/10.1007/s00428-011-1140-8

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