Prognostic impact of tumor-associated macrophage infiltration in esophageal cancer: a meta-analysis

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1. Allemani C, Weir HK, Carreira H et al. Global surveillance of cancer survival 1995–2009: analysis of individual data for 25,676,887 patients from 279 population-based registries in 67 countries (CONCORD-2). Lancet 385(9972), 977–1010 (2015).
  MedlineGoogle Scholar
• 2. Napier KJ, Scheerer M, Misra S. Esophageal cancer: a review of epidemiology, pathogenesis, staging workup and treatment modalities. World J. Gastrointest. Oncol. 6(5), 112–120 (2014).
  MedlineGoogle Scholar
• 3. Klemm F, Joyce JA. Microenvironmental regulation of therapeutic response in cancer. Trends Cell Biol. 25(4), 198–213 (2015).
  MedlineGoogle Scholar
• 4. Weitzenfeld P, Meshel T, Ben-Baruch A. Microenvironmental networks promote tumor heterogeneity and enrich for metastatic cancer stem-like cells in Luminal-A breast tumor cells. Oncotarget 7(49), 81123–81143 (2016).
  MedlineGoogle Scholar
• 5. Chanmee T, Ontong P, Konno K, Itano N. Tumor-associated macrophages as major players in the tumor microenvironment. Cancers 6(3), 1670–1690 (2014).
  Medline CASGoogle Scholar
• 6. Wynn TA, Chawla A, Pollard JW. Macrophage biology in development, homeostasis and disease. Nature 496(7446), 445–455 (2013).
  Medline CASGoogle Scholar
• 7. Mantovani A, Locati M. Orchestration of macrophage polarization. Blood 114(15), 3135–3136 (2009).
  Medline CASGoogle Scholar
• 8. Vonderheide RH, Bajor DL, Winograd R, Evans RA, Bayne LJ, Beatty GL. CD40 immunotherapy for pancreatic cancer. Cancer Immunol. Immunother. 62(5), 949–954 (2013).
  Medline CASGoogle Scholar
• 9. Campbell MJ, Tonlaar NY, Garwood ER et al. Proliferating macrophages associated with high grade, hormone receptor negative breast cancer and poor clinical outcome. Breast Cancer Res. Treat. 128(3), 703–711 (2011).
  MedlineGoogle Scholar
• 10. Li J, Zhang BZ, Qin YR et al. CD68 and interleukin 13, prospective immune markers for esophageal squamous cell carcinoma prognosis prediction. Oncotarget 7(13), 15525–15538 (2016). • CD68+ TAMs associated with the prolongation of survival in esophageal cancer patients. This article has a large sample size, but the control of confounding factors is not enough due to specimens from multiple hospitals. Therefore, the results may different from other studies.
  MedlineGoogle Scholar
• 11. Sugimura K, Miyata H, Tanaka K et al. High infiltration of tumor-associated macrophages is associated with a poor response to chemotherapy and poor prognosis of patients undergoing neoadjuvant chemotherapy for esophageal cancer. J. Surg. Oncol. 111(6), 752–759 (2015). • Key study that demonstrates the density of CD68+ TAM was associated with esophageal cancer poor prognosis. This article has a small sample size, but may be different from other studies due to sampling errors.
  MedlineGoogle Scholar
• 12. Shigeoka M, Urakawa N, Nakamura T et al. Tumor associated macrophage expressing CD204 is associated with tumor aggressiveness of esophageal squamous cell carcinoma. Cancer Sci. 104(8), 1112–1119 (2013). •• Key study that suggested CD68+ TAMs were not associated with esophageal cancer prognosis. Both CD204 and CD163 markers were used, and it was concluded that CD204 was helpful to TAM.
  Medline CASGoogle Scholar
• 13. Wells G, Shea B, O'Connell D et al. The Newcastle–Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. www.ohri.ca/programs/clinical_epidemiology/oxford.asp
  Google Scholar
• 14. Tierney JF, Stewart LA, Ghersi D, Burdett S, Sydes MR. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials 8, 16 (2007).
  MedlineGoogle Scholar
• 15. Xu B, Chen L, Li J et al. Prognostic value of tumor infiltrating NK cells and macrophages in stage II+III esophageal cancer patients. Oncotarget 7(46), 74904–74916 (2016).
  MedlineGoogle Scholar
• 16. Xu B, Li J, Feng H et al. Different density of CD57+tumor-inmtrating natural killer cells and CD68+tumor-infiltrating macrophages associated with the prognosis in patients with esophagus cancer. Chinese J. Exp. Surg. 33(4), 1117–1121 (2016).
  Google Scholar
• 17. Hu JM, Liu K, Liu JH et al. CD163 as a marker of M2 macrophage, contribute to predicte aggressiveness and prognosis of Kazakh esophageal squamous cell carcinoma. Oncotarget 8(13), 21526–21538 (2017).
  MedlineGoogle Scholar
• 18. Xue Li, Wang KL, Liu JH et al. High infiltration of CD68-tumor associated macrophages, predict poor prognosis in Kazakh esophageal cancer patients. Int. J. Clin. Exp. Pathol. 10(10), 10282–10292 (2017).
  MedlineGoogle Scholar
• 19. Hosono M, Koma YI, Takase N et al. CXCL8 derived from tumor-associated macrophages and esophageal squamous cell carcinomas contributes to tumor progression by promoting migration and invasion of cancer cells. Oncotarget 8(62), 106071–106088 (2017).
  MedlineGoogle Scholar
• 20. Zhu Y, Li M, Bo C et al. Prognostic significance of the lymphocyte-to-monocyte ratio and the tumor-infiltrating lymphocyte to tumor-associated macrophage ratio in patients with stage T3N0M0 esophageal squamous cell carcinoma. Cancer Immunol. Immunother. 66(3), 343–354 (2017).
  Medline CASGoogle Scholar
• 21. Hatogai K, Kitano S, Fujii S et al. Comprehensive immunohistochemical analysis of tumor microenvironment immune status in esophageal squamous cell carcinoma. Oncotarget 7(30), 47252–47264 (2016).
  MedlineGoogle Scholar
• 22. Cao W, Peters JH, Nieman D, Sharma M, Watson T, Yu J. Macrophage subtype predicts lymph node metastasis in oesophageal adenocarcinoma and promotes cancer cell invasion in vitro. Br. J. Cancer 113(5), 738–746 (2015).
  Medline CASGoogle Scholar
• 23. Zhibing Zhang YZ, Xie J. Influence of CD68 + and CD163 + macrophages on the infiltration of esophageal carcinoma and its prognosis. Modern J. Integr. Tradit. Chinese West. Med. 24(6), 590–592 (2015).
  Google Scholar
• 24. Zhang Y, Ren H, Wang L et al. Clinical impact of tumor-infiltrating inflammatory cells in primary small cell esophageal carcinoma. Int. J. Mol. Sci. 15(6), 9718–9734 (2014).
  Medline CASGoogle Scholar
• 25. Xie R, Dong B, Pang H, Cheng Y, Shang K, Li X. Tumor-associated macrophages in esophageal carcinoma and its impact on prognosis. Chin. J. Clin. Oncol. 38(2), 83–86 (2011).
  CASGoogle Scholar
• 26. Guo SJ, Lin DM, Li J et al. Tumor-associated macrophages and CD3-zeta expression of tumor-infiltrating lymphocytes in human esophageal squamous-cell carcinoma. Dis. Esophagus 20(2), 107–116 (2007). • Suggests that densities of TAM was not associated with esophageal cancer prognosis.
  Medline CASGoogle Scholar
• 27. Koide N, Nishio A, Hiraguri M et al. Differences and relationships of thymidine phosphorylase expression in tumor-associated macrophages and cancer cells in squamous cell carcinoma of the esophagus. Dis. Esophagus 15(1), 67–73 (2002).
  Medline CASGoogle Scholar
• 28. Parisi L, Gini E, Baci D et al. Macrophage polarization in chronic inflammatory diseases: killers or builders? J. Immunol. Res. 2018, 8917804 (2018). •• At present, it is generally believed that TAM subtype is an important factors in the prognosis of tumor patients, with M2-like TAMs related to the malignant biological behavior of tumors.
  MedlineGoogle Scholar
• 29. Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 21(3), 309–322 (2012).
  Medline CASGoogle Scholar
• 30. Coussens LM, Werb Z. Inflammation and cancer. Nature 420(6917), 860–867 (2002).
  Medline CASGoogle Scholar
• 31. Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 11(10), 889–896 (2010).
  Medline CASGoogle Scholar
• 32. Cassetta L, Kitamura T. Targeting tumor-associated macrophages as a potential strategy to enhance the response to immune checkpoint inhibitors. Front. Cell Dev. Biol. 6, 38 (2018). • A comprehensive understanding of macrophages in the tumor microenvironment would assist in the development of new immunotherapy agents.
  MedlineGoogle Scholar
• 33. Mei J, Xiao Z, Guo C et al. Prognostic impact of tumor-associated macrophage infiltration in non-small cell lung cancer: a systemic review and meta-analysis. Oncotarget 7(23), 34217–34228 (2016).
  MedlineGoogle Scholar
• 34. Yuan X, Zhang J, Li D et al. Prognostic significance of tumor-associated macrophages in ovarian cancer: a meta-analysis. Gynecol. Oncol. 147(1), 181–187 (2017).
  Medline CASGoogle Scholar
• 35. Wang XL, Jiang JT, Wu CP. Prognostic significance of tumor-associated macrophage infiltration in gastric cancer: a meta-analysis. Genet. Mol. Res. 15(4), (2016).
  Google Scholar
• 36. Wu SQ, Xu R, Li XF, Zhao XK, Qian BZ. Prognostic roles of tumor associated macrophages in bladder cancer: a system review and meta-analysis. Oncotarget 9(38), 25294–25303 (2018).
  MedlineGoogle Scholar
• 37. Guo B, Cen H, Tan X, Ke Q. Meta-analysis of the prognostic and clinical value of tumor-associated macrophages in adult classical Hodgkin lymphoma. BMC Med. 14(1), 159 (2016).
  MedlineGoogle Scholar
• 38. Zhao X, Qu J, Sun Y et al. Prognostic significance of tumor-associated macrophages in breast cancer: a meta-analysis of the literature. Oncotarget 8(18), 30576–30586 (2017).
  MedlineGoogle Scholar
• 39. Zhang QW, Liu L, Gong CY et al. Prognostic significance of tumor-associated macrophages in solid tumor: a meta-analysis of the literature. PLoS ONE 7(12), e50946 (2012).
  Medline CASGoogle Scholar
• 40. Gottfried E, Kunz-Schughart LA, Weber A et al. Expression of CD68 in non-myeloid cell types. Scand. J. Immunol. 67(5), 453–463 (2008).
  Medline CASGoogle Scholar
• 41. Biswas SK, Allavena P, Mantovani A. Tumor-associated macrophages: functional diversity, clinical significance, and open questions. Semin. Immunopathol. 35(5), 585–600 (2013).
  Medline CASGoogle Scholar
• 42. Komohara Y, Ohnishi K, Kuratsu J, Takeya M. Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas. J. Pathol. 216(1), 15–24 (2008).
  Medline CASGoogle Scholar
• 43. Fujiwara Y, Hizukuri Y, Yamashiro K et al. Guanylate-binding protein 5 is a marker of interferon-γ-induced classically activated macrophages. Clin. Transl. Immunology 5(11), e111 (2016).
  MedlineGoogle Scholar
• 44. Komohara Y, Hasita H, Ohnishi K et al. Macrophage infiltration and its prognostic relevance in clear cell renal cell carcinoma. Cancer Sci. 102(7), 1424–1431 (2011).
  Medline CASGoogle Scholar
• 45. Hirayama S, Ishii G, Nagai K et al. Prognostic impact of CD204-positive macrophages in lung squamous cell carcinoma: possible contribution of cd204-positive macrophages to the tumor-promoting microenvironment. J. Thorac. Oncol. 7(12), 1790–1797 (2012).
  Medline CASGoogle Scholar
• 46. Kawachi A, Yoshida H, Kitano S, Ino Y, Kato T, Hiraoka N. Tumor-associated CD204+ M2 macrophages are unfavorable prognostic indicators in uterine cervical adenocarcinoma. Cancer Sci. 109(3), 863–870 (2018).
  Medline CASGoogle Scholar
• 47. Kim Y, Wen X, Bae JM, Kim JH, Cho NY, Kang GH. The distribution of intratumoral macrophages correlates with molecular phenotypes and impacts prognosis in colorectal carcinoma. Histopathology 73(4), 663–671 (2018). • The difference in tumor and interstitial distribution is also an important factor affecting tumor prognosis.
  MedlineGoogle Scholar
• 48. Caux C, Ramos RN, Prendergast GC, Bendriss-Vermare N, Ménétrier-Caux C. A milestone review on how macrophages affect tumor growth. Cancer Res. 76(22), 6439 (2016).
  Medline CASGoogle Scholar
• 49. Ruffell B, Coussens L. Macrophages and therapeutic resistance in cancer. Cancer Cell 27(4), 462–472 (2015). •• Macrophages play an important role in tumor immunity and progression, and they play different roles in different tumors.
  Medline CASGoogle Scholar
• 50. Biswas SK, Mantovani A. Tumor-associated macrophages: functional diversity, clinical significance, and open questions. Semin. Immunopathol. 35(5), 585–600 (2013).
  Medline CASGoogle Scholar
• 51. Condeelis J, Pollard JW. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124(2), 263–266 (2006).
  Medline CASGoogle Scholar
• 52. Zhang S, Che D, Yang F et al. Tumor-associated macrophages promote tumor metastasis via the TGF-beta/SOX9 axis in non-small cell lung cancer. Oncotarget 8(59), 99801–99815 (2017).
  MedlineGoogle Scholar
• 53. Shiraishi D, Fujiwara Y, Horlad H et al. CD163 is required for protumoral activation of macrophages in human and murine sarcoma. Cancer Res. 78(12), 3255–3266 (2018).
  Medline CASGoogle Scholar
• 54. Alvarado-Vazquez PA, Bernal L, Paige CA et al. Macrophage-specific nanotechnology-driven CD163 overexpression in human macrophages results in an M2 phenotype under inflammatory conditions. Immunobiology 222(8–9), 900–912 (2017).
  Medline CASGoogle Scholar