Skip to main content
Top
Published in: BMC Cancer 1/2020

01-12-2020 | Solid Tumor | Research article

The prognostic value of IDO expression in solid tumors: a systematic review and meta-analysis

Authors: Sen Wang, Jia Wu, Han Shen, Junjun Wang

Published in: BMC Cancer | Issue 1/2020

Login to get access

Abstract

Background

Indoleamine 2,3-dioxygenase (IDO) is a rate-limiting enzyme in the metabolism of tryptophan into kynurenine. It is considered to be an immunosuppressive molecule that plays an important role in the development of tumors. However, the association between IDO and solid tumor prognosis remains unclear. Herein, we retrieved relevant published literature and analyzed the association between IDO expression and prognosis in solid tumors.

Methods

Studies related to IDO expression and tumor prognosis were retrieved using PMC, EMbase and web of science database. Overall survival (OS), time to tumor progression (TTP) and other data in each study were extracted. Hazard ratio (HR) was used for analysis and calculation, while heterogeneity and publication bias between studies were also analyzed.

Results

A total of 31 studies were included in this meta-analysis. Overall, high expression of IDO was significantly associated with poor OS (HR 1.92, 95% CI 1.52–2.43, P < 0.001) and TTP (HR 2.25 95% CI 1.58–3.22, P < 0.001). However, there was significant heterogeneity between studies on OS (I2 = 81.1%, P < 0.001) and TTP (I2 = 54.8%, P = 0.007). Subgroup analysis showed lower heterogeneity among prospective studies, studies of the same tumor type, and studies with follow-up periods longer than 45 months.

Conclusions

The high expression of IDO was significantly associated with the poor prognosis of solid tumors, suggesting that it can be used as a biomarker for tumor prognosis and as a potential target for tumor therapy.
Literature
1.
go back to reference Munn DH, Mellor AL. Indoleamine 2,3 dioxygenase and metabolic control of immune responses. Trends Immunol. 2013;34(3):137–43.PubMedCrossRef Munn DH, Mellor AL. Indoleamine 2,3 dioxygenase and metabolic control of immune responses. Trends Immunol. 2013;34(3):137–43.PubMedCrossRef
2.
go back to reference Ball HJ, Yuasa HJ, Austin CJ, Weiser S, Hunt NH. Indoleamine 2,3-dioxygenase-2; a new enzyme in the kynurenine pathway. Int J Biochem Cell Biol. 2009;41(3):467–71.PubMedCrossRef Ball HJ, Yuasa HJ, Austin CJ, Weiser S, Hunt NH. Indoleamine 2,3-dioxygenase-2; a new enzyme in the kynurenine pathway. Int J Biochem Cell Biol. 2009;41(3):467–71.PubMedCrossRef
3.
go back to reference Mbongue J, Nicholas D, Torrez T, Kim N, Firek A, Langridge W. The role of Indoleamine 2, 3-Dioxygenase in immune suppression and autoimmunity. Vaccines. 2015;3(3):703–29.PubMedPubMedCentralCrossRef Mbongue J, Nicholas D, Torrez T, Kim N, Firek A, Langridge W. The role of Indoleamine 2, 3-Dioxygenase in immune suppression and autoimmunity. Vaccines. 2015;3(3):703–29.PubMedPubMedCentralCrossRef
4.
go back to reference Nguyen NT, Nakahama T, Le DH, Van Son L, Chu HH, Kishimoto T. Aryl hydrocarbon receptor and Kynurenine: recent advances in autoimmune disease research. Front Immunol. 2014;5:551.PubMedPubMedCentralCrossRef Nguyen NT, Nakahama T, Le DH, Van Son L, Chu HH, Kishimoto T. Aryl hydrocarbon receptor and Kynurenine: recent advances in autoimmune disease research. Front Immunol. 2014;5:551.PubMedPubMedCentralCrossRef
6.
go back to reference Boasso A, Herbeuval JP, Hardy AW, Anderson SA, Dolan MJ, Fuchs D, Shearer GM. HIV inhibits CD4+ T-cell proliferation by inducing indoleamine 2,3-dioxygenase in plasmacytoid dendritic cells. BLOOD. 2007;109(8):3351–9.PubMedPubMedCentralCrossRef Boasso A, Herbeuval JP, Hardy AW, Anderson SA, Dolan MJ, Fuchs D, Shearer GM. HIV inhibits CD4+ T-cell proliferation by inducing indoleamine 2,3-dioxygenase in plasmacytoid dendritic cells. BLOOD. 2007;109(8):3351–9.PubMedPubMedCentralCrossRef
8.
go back to reference von Bubnoff D, Bieber T. The indoleamine 2,3-dioxygenase (IDO) pathway controls allergy. ALLERGY. 2012;67(6):718–25.CrossRef von Bubnoff D, Bieber T. The indoleamine 2,3-dioxygenase (IDO) pathway controls allergy. ALLERGY. 2012;67(6):718–25.CrossRef
9.
go back to reference Platten M, von Knebel DN, Oezen I, Wick W, Ochs K. Cancer immunotherapy by targeting IDO1/TDO and their downstream effectors. Front Immunol. 2015;5:673.PubMedPubMedCentralCrossRef Platten M, von Knebel DN, Oezen I, Wick W, Ochs K. Cancer immunotherapy by targeting IDO1/TDO and their downstream effectors. Front Immunol. 2015;5:673.PubMedPubMedCentralCrossRef
10.
go back to reference Jiang T, Sun Y, Yin Z, Feng S, Sun L, Li Z. Research progress of indoleamine 2,3-dioxygenase inhibitors. Future Med Chem. 2015;7(2):185–201.PubMedCrossRef Jiang T, Sun Y, Yin Z, Feng S, Sun L, Li Z. Research progress of indoleamine 2,3-dioxygenase inhibitors. Future Med Chem. 2015;7(2):185–201.PubMedCrossRef
11.
go back to reference Liu X, Newton RC, Friedman SM, Scherle PA. Indoleamine 2,3-dioxygenase, an emerging target for anti-cancer therapy. Curr Cancer Drug Targets. 2009;9(8):938–52.PubMedCrossRef Liu X, Newton RC, Friedman SM, Scherle PA. Indoleamine 2,3-dioxygenase, an emerging target for anti-cancer therapy. Curr Cancer Drug Targets. 2009;9(8):938–52.PubMedCrossRef
12.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 2010;8(5):336–41.CrossRefPubMed Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 2010;8(5):336–41.CrossRefPubMed
13.
go back to reference Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–5.CrossRef Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–5.CrossRef
14.
go back to reference Brandacher G. Prognostic value of Indoleamine 2,3-Dioxygenase expression in colorectal Cancer: effect on tumor-infiltrating T cells. Clin Cancer Res. 2006;12(4):1144–51.PubMedCrossRef Brandacher G. Prognostic value of Indoleamine 2,3-Dioxygenase expression in colorectal Cancer: effect on tumor-infiltrating T cells. Clin Cancer Res. 2006;12(4):1144–51.PubMedCrossRef
15.
go back to reference Ino K, Yoshida N, Kajiyama H, Shibata K, Yamamoto E, Kidokoro K, Takahashi N, Terauchi M, Nawa A, Nomura S, et al. Indoleamine 2,3-dioxygenase is a novel prognostic indicator for endometrial cancer. Br J Cancer. 2006;95(11):1555–61.PubMedPubMedCentralCrossRef Ino K, Yoshida N, Kajiyama H, Shibata K, Yamamoto E, Kidokoro K, Takahashi N, Terauchi M, Nawa A, Nomura S, et al. Indoleamine 2,3-dioxygenase is a novel prognostic indicator for endometrial cancer. Br J Cancer. 2006;95(11):1555–61.PubMedPubMedCentralCrossRef
16.
go back to reference Riesenberg R, Weiler C, Spring O, Eder M, Buchner A, Popp T, Castro M, Kammerer R, Takikawa O, Hatz RA, et al. Expression of indoleamine 2,3-dioxygenase in tumor endothelial cells correlates with long-term survival of patients with renal cell carcinoma. Clin Cancer Res. 2007;13(23):6993–7002.PubMedCrossRef Riesenberg R, Weiler C, Spring O, Eder M, Buchner A, Popp T, Castro M, Kammerer R, Takikawa O, Hatz RA, et al. Expression of indoleamine 2,3-dioxygenase in tumor endothelial cells correlates with long-term survival of patients with renal cell carcinoma. Clin Cancer Res. 2007;13(23):6993–7002.PubMedCrossRef
17.
go back to reference Pan K, Wang H, Chen MS, Zhang HK, Weng DS, Zhou J, Huang W, Li JJ, Song HF, Xia JC. Expression and prognosis role of indoleamine 2,3-dioxygenase in hepatocellular carcinoma. J Cancer Res Clin Oncol. 2008;134(11):1247–53.PubMedCrossRef Pan K, Wang H, Chen MS, Zhang HK, Weng DS, Zhou J, Huang W, Li JJ, Song HF, Xia JC. Expression and prognosis role of indoleamine 2,3-dioxygenase in hepatocellular carcinoma. J Cancer Res Clin Oncol. 2008;134(11):1247–53.PubMedCrossRef
18.
go back to reference Ino K, Yamamoto E, Shibata K, Kajiyama H, Yoshida N, Terauchi M, Nawa A, Nagasaka T, Takikawa O, Kikkawa F. Inverse correlation between tumoral indoleamine 2,3-dioxygenase expression and tumor-infiltrating lymphocytes in endometrial cancer: its association with disease progression and survival. Clin Cancer Res. 2008;14(8):2310–7.PubMedCrossRef Ino K, Yamamoto E, Shibata K, Kajiyama H, Yoshida N, Terauchi M, Nawa A, Nagasaka T, Takikawa O, Kikkawa F. Inverse correlation between tumoral indoleamine 2,3-dioxygenase expression and tumor-infiltrating lymphocytes in endometrial cancer: its association with disease progression and survival. Clin Cancer Res. 2008;14(8):2310–7.PubMedCrossRef
19.
go back to reference Urakawa H, Nishida Y, Nakashima H, Shimoyama Y, Nakamura S, Ishiguro N. Prognostic value of indoleamine 2,3-dioxygenase expression in high grade osteosarcoma. CLIN EXP METASTAS. 2009;26(8):1005–12.CrossRef Urakawa H, Nishida Y, Nakashima H, Shimoyama Y, Nakamura S, Ishiguro N. Prognostic value of indoleamine 2,3-dioxygenase expression in high grade osteosarcoma. CLIN EXP METASTAS. 2009;26(8):1005–12.CrossRef
20.
go back to reference Inaba T, Ino K, Kajiyama H, Shibata K, Yamamoto E, Kondo S, Umezu T, Nawa A, Takikawa O, Kikkawa F. Indoleamine 2,3-dioxygenase expression predicts impaired survival of invasive cervical cancer patients treated with radical hysterectomy. Gynecol Oncol. 2010;117(3):423–8.PubMedCrossRef Inaba T, Ino K, Kajiyama H, Shibata K, Yamamoto E, Kondo S, Umezu T, Nawa A, Takikawa O, Kikkawa F. Indoleamine 2,3-dioxygenase expression predicts impaired survival of invasive cervical cancer patients treated with radical hysterectomy. Gynecol Oncol. 2010;117(3):423–8.PubMedCrossRef
21.
go back to reference Sznurkowski JJ, Awrocki A, Emerich J, Sznurkowska K, Biernat W. Expression of indoleamine 2,3-dioxygenase predicts shorter survival in patients with vulvar squamous cell carcinoma (vSCC) not influencing on the recruitment of FOXP3-expressing regulatory T cells in cancer nests. Gynecol Oncol. 2011;122(2):307–12.PubMedCrossRef Sznurkowski JJ, Awrocki A, Emerich J, Sznurkowska K, Biernat W. Expression of indoleamine 2,3-dioxygenase predicts shorter survival in patients with vulvar squamous cell carcinoma (vSCC) not influencing on the recruitment of FOXP3-expressing regulatory T cells in cancer nests. Gynecol Oncol. 2011;122(2):307–12.PubMedCrossRef
22.
go back to reference Speeckaert R, Vermaelen K, van Geel N, Autier P, Lambert J, Haspeslagh M, van Gele M, Thielemans K, Neyns B, Roche N, et al. Indoleamine 2,3-dioxygenase, a new prognostic marker in sentinel lymph nodes of melanoma patients. Eur J Cancer. 2012;48(13):2004–11.PubMedCrossRef Speeckaert R, Vermaelen K, van Geel N, Autier P, Lambert J, Haspeslagh M, van Gele M, Thielemans K, Neyns B, Roche N, et al. Indoleamine 2,3-dioxygenase, a new prognostic marker in sentinel lymph nodes of melanoma patients. Eur J Cancer. 2012;48(13):2004–11.PubMedCrossRef
23.
go back to reference de Jong RA, Kema IP, Boerma A, Boezen HM, van der Want JJ, Gooden MJ, Hollema H, Nijman HW. Prognostic role of indoleamine 2,3-dioxygenase in endometrial carcinoma. Gynecol Oncol. 2012;126(3):474–80.PubMedCrossRef de Jong RA, Kema IP, Boerma A, Boezen HM, van der Want JJ, Gooden MJ, Hollema H, Nijman HW. Prognostic role of indoleamine 2,3-dioxygenase in endometrial carcinoma. Gynecol Oncol. 2012;126(3):474–80.PubMedCrossRef
24.
go back to reference Ye J, Liu H, Hu Y, Li P, Zhang G, Li Y. Tumoral indoleamine 2,3-dioxygenase expression predicts poor outcome in laryngeal squamous cell carcinoma. Virchows Arch. 2013;462(1):73–81.PubMedCrossRef Ye J, Liu H, Hu Y, Li P, Zhang G, Li Y. Tumoral indoleamine 2,3-dioxygenase expression predicts poor outcome in laryngeal squamous cell carcinoma. Virchows Arch. 2013;462(1):73–81.PubMedCrossRef
25.
go back to reference Jia Y, Wang H, Wang Y, Wang T, Wang M, Ma M, Duan Y, Meng X, Liu L. Low expression of Bin1, along with high expression of IDO in tumor tissue and draining lymph nodes, are predictors of poor prognosis for esophageal squamous cell cancer patients. Int J Cancer. 2015;137(5):1095–106.PubMedCrossRef Jia Y, Wang H, Wang Y, Wang T, Wang M, Ma M, Duan Y, Meng X, Liu L. Low expression of Bin1, along with high expression of IDO in tumor tissue and draining lymph nodes, are predictors of poor prognosis for esophageal squamous cell cancer patients. Int J Cancer. 2015;137(5):1095–106.PubMedCrossRef
26.
go back to reference Pelak MJ, Śnietura M, Lange D, Nikiel B, Pecka KM. The prognostic significance of indoleamine-2,3-dioxygenase and the receptors for transforming growth factor β and interferon γ in metastatic lymph nodes in malignant melanoma. Pol J Pathol. 2015;4:376–82.CrossRef Pelak MJ, Śnietura M, Lange D, Nikiel B, Pecka KM. The prognostic significance of indoleamine-2,3-dioxygenase and the receptors for transforming growth factor β and interferon γ in metastatic lymph nodes in malignant melanoma. Pol J Pathol. 2015;4:376–82.CrossRef
27.
go back to reference Ben-Haj-Ayed A, Moussa A, Ghedira R, Gabbouj S, Miled S, Bouzid N, Tebra-Mrad S, Bouaouina N, Chouchane L, Zakhama A, et al. Prognostic value of indoleamine 2,3-dioxygenase activity and expression in nasopharyngeal carcinoma. Immunol Lett. 2016;169:23–32.PubMedCrossRef Ben-Haj-Ayed A, Moussa A, Ghedira R, Gabbouj S, Miled S, Bouzid N, Tebra-Mrad S, Bouaouina N, Chouchane L, Zakhama A, et al. Prognostic value of indoleamine 2,3-dioxygenase activity and expression in nasopharyngeal carcinoma. Immunol Lett. 2016;169:23–32.PubMedCrossRef
28.
go back to reference Liu H, Shen Z, Wang Z, Wang X, Zhang H, Qin J, Qin X, Xu J, Sun Y. Increased expression of IDO associates with poor postoperative clinical outcome of patients with gastric adenocarcinoma. Sci Rep. 2016;6:21319.PubMedPubMedCentralCrossRef Liu H, Shen Z, Wang Z, Wang X, Zhang H, Qin J, Qin X, Xu J, Sun Y. Increased expression of IDO associates with poor postoperative clinical outcome of patients with gastric adenocarcinoma. Sci Rep. 2016;6:21319.PubMedPubMedCentralCrossRef
29.
go back to reference Zhang T, Tan XL, Xu Y, Wang ZZ, Xiao CH, Liu R. Expression and prognostic value of Indoleamine 2,3-dioxygenase in pancreatic Cancer. Chin Med J. 2017;130(6):710–6.PubMedPubMedCentralCrossRef Zhang T, Tan XL, Xu Y, Wang ZZ, Xiao CH, Liu R. Expression and prognostic value of Indoleamine 2,3-dioxygenase in pancreatic Cancer. Chin Med J. 2017;130(6):710–6.PubMedPubMedCentralCrossRef
30.
go back to reference Hudolin T, Mengus C, Coulot J, Kastelan Z, El-Saleh A, Spagnoli GC. Expression of Indoleamine 2,3-Dioxygenase gene is a feature of poorly differentiated non-muscle-invasive Urothelial cell bladder carcinomas. Anticancer Res. 2017;37(3):1375–80.PubMedCrossRef Hudolin T, Mengus C, Coulot J, Kastelan Z, El-Saleh A, Spagnoli GC. Expression of Indoleamine 2,3-Dioxygenase gene is a feature of poorly differentiated non-muscle-invasive Urothelial cell bladder carcinomas. Anticancer Res. 2017;37(3):1375–80.PubMedCrossRef
31.
go back to reference Carvajal-Hausdorf DE, Mani N, Velcheti V, Schalper KA, Rimm DL. Objective measurement and clinical significance of IDO1 protein in hormone receptor-positive breast cancer. J IMMUNOTHER CANCER. 2017;5(1):81.PubMedPubMedCentralCrossRef Carvajal-Hausdorf DE, Mani N, Velcheti V, Schalper KA, Rimm DL. Objective measurement and clinical significance of IDO1 protein in hormone receptor-positive breast cancer. J IMMUNOTHER CANCER. 2017;5(1):81.PubMedPubMedCentralCrossRef
32.
go back to reference Zhai L, Ladomersky E, Lauing KL, Wu M, Genet M, Gritsina G, Gyorffy B, Brastianos PK, Binder DC, Sosman JA, et al. Infiltrating T cells increase IDO1 expression in Glioblastoma and contribute to decreased patient survival. Clin Cancer Res. 2017;23(21):6650–60.PubMedPubMedCentralCrossRef Zhai L, Ladomersky E, Lauing KL, Wu M, Genet M, Gritsina G, Gyorffy B, Brastianos PK, Binder DC, Sosman JA, et al. Infiltrating T cells increase IDO1 expression in Glioblastoma and contribute to decreased patient survival. Clin Cancer Res. 2017;23(21):6650–60.PubMedPubMedCentralCrossRef
33.
go back to reference Ma W, Wang X, Yan W, Zhou Z, Pan Z, Chen G, Zhang R. Indoleamine-2,3-dioxygenase 1/cyclooxygenase 2 expression prediction for adverse prognosis in colorectal cancer. WORLD J GASTROENTERO. 2018;24(20):2181–90.CrossRef Ma W, Wang X, Yan W, Zhou Z, Pan Z, Chen G, Zhang R. Indoleamine-2,3-dioxygenase 1/cyclooxygenase 2 expression prediction for adverse prognosis in colorectal cancer. WORLD J GASTROENTERO. 2018;24(20):2181–90.CrossRef
34.
go back to reference Wei Y, Chu C, Chang C, Lin S, Su W, Tseng Y, Lin C, Yen Y. Different pattern of PD-L1, IDO, and FOXP3 Tregs expression with survival in thymoma and thymic carcinoma. Lung Cancer. 2018;125:35–42.PubMedCrossRef Wei Y, Chu C, Chang C, Lin S, Su W, Tseng Y, Lin C, Yen Y. Different pattern of PD-L1, IDO, and FOXP3 Tregs expression with survival in thymoma and thymic carcinoma. Lung Cancer. 2018;125:35–42.PubMedCrossRef
35.
go back to reference Takeya H, Shiota T, Yagi T, Ohnishi K, Baba Y, Miyasato Y, Kiyozumi Y, Yoshida N, Takeya M, Baba H, et al. High CD169 expression in lymph node macrophages predicts a favorable clinical course in patients with esophageal cancer. Pathol Int. 2018;68(12):685–93.PubMedCrossRef Takeya H, Shiota T, Yagi T, Ohnishi K, Baba Y, Miyasato Y, Kiyozumi Y, Yoshida N, Takeya M, Baba H, et al. High CD169 expression in lymph node macrophages predicts a favorable clinical course in patients with esophageal cancer. Pathol Int. 2018;68(12):685–93.PubMedCrossRef
36.
go back to reference Kiyozumi Y, Baba Y, Okadome K, Yagi T, Ishimoto T, Iwatsuki M, Miyamoto Y, Yoshida N, Watanabe M, Komohara Y, et al. IDO1 expression is associated with immune tolerance and poor prognosis in patients with surgically resected esophageal cancer. Ann Surg. 2019;269(6):1101–8.PubMedCrossRef Kiyozumi Y, Baba Y, Okadome K, Yagi T, Ishimoto T, Iwatsuki M, Miyamoto Y, Yoshida N, Watanabe M, Komohara Y, et al. IDO1 expression is associated with immune tolerance and poor prognosis in patients with surgically resected esophageal cancer. Ann Surg. 2019;269(6):1101–8.PubMedCrossRef
37.
go back to reference Nishi M, Yoshikawa K, Higashijima J, Tokunaga T, Kashihara H, Takasu C, Ishikawa D, Wada Y, Shimada M. The impact of Indoleamine 2,3-dioxygenase (IDO) expression on stage III gastric Cancer. Anticancer Res. 2018;38(6):3387–92.PubMedCrossRef Nishi M, Yoshikawa K, Higashijima J, Tokunaga T, Kashihara H, Takasu C, Ishikawa D, Wada Y, Shimada M. The impact of Indoleamine 2,3-dioxygenase (IDO) expression on stage III gastric Cancer. Anticancer Res. 2018;38(6):3387–92.PubMedCrossRef
38.
go back to reference Ahmadzada T, Lee K, Clarke C, Cooper WA, Linton A, McCaughan B, Asher R, Clarke S, Reid G, Kao S. High BIN1 expression has a favorable prognosis in malignant pleural mesothelioma and is associated with tumor infiltrating lymphocytes. Lung Cancer. 2019;130:35–41.PubMedCrossRef Ahmadzada T, Lee K, Clarke C, Cooper WA, Linton A, McCaughan B, Asher R, Clarke S, Reid G, Kao S. High BIN1 expression has a favorable prognosis in malignant pleural mesothelioma and is associated with tumor infiltrating lymphocytes. Lung Cancer. 2019;130:35–41.PubMedCrossRef
39.
go back to reference Ma W, Duan H, Zhang R, Wang X, Xu H, Zhou Q, Zhang L. High expression of Indoleamine 2, 3-Dioxygenase in Adenosquamous lung carcinoma correlates with favorable patient outcome. J Cancer. 2019;10(1):267–76.PubMedPubMedCentralCrossRef Ma W, Duan H, Zhang R, Wang X, Xu H, Zhou Q, Zhang L. High expression of Indoleamine 2, 3-Dioxygenase in Adenosquamous lung carcinoma correlates with favorable patient outcome. J Cancer. 2019;10(1):267–76.PubMedPubMedCentralCrossRef
40.
go back to reference Mitra D, Horick NK, Brackett DG, Mouw KW, Hornick JL, Ferrone S, Hong TS, Mamon H, Clark JW, Parikh AR, et al. High IDO1 expression is associated with poor outcome in patients with anal cancer treated with definitive chemoradiotherapy. Oncologist. 2019;24(6):e275–e283. Mitra D, Horick NK, Brackett DG, Mouw KW, Hornick JL, Ferrone S, Hong TS, Mamon H, Clark JW, Parikh AR, et al. High IDO1 expression is associated with poor outcome in patients with anal cancer treated with definitive chemoradiotherapy. Oncologist. 2019;24(6):e275–e283.
41.
go back to reference Schollbach J, Kircher S, Wiegering A, Seyfried F, Klein I, Rosenwald A, Germer C, Löb S. Prognostic value of tumour-infiltrating CD8+ lymphocytes in rectal cancer after neoadjuvant chemoradiation: is indoleamine-2,3-dioxygenase (IDO1) a friend or foe? Cancer Immunol Immunother. 2019;68(4):563–75.PubMedCrossRef Schollbach J, Kircher S, Wiegering A, Seyfried F, Klein I, Rosenwald A, Germer C, Löb S. Prognostic value of tumour-infiltrating CD8+ lymphocytes in rectal cancer after neoadjuvant chemoradiation: is indoleamine-2,3-dioxygenase (IDO1) a friend or foe? Cancer Immunol Immunother. 2019;68(4):563–75.PubMedCrossRef
42.
go back to reference Boujelbene N, Ben Yahia H, Babay W, Gadria S, Zemni I, Azaiez H, Dhouioui S, Zidi N, Mchiri R, Mrad K, et al. HLA-G, HLA-E, and IDO overexpression predicts a worse survival of Tunisian patients with vulvar squamous cell carcinoma. HLA. 2019;94(1):11–24.PubMed Boujelbene N, Ben Yahia H, Babay W, Gadria S, Zemni I, Azaiez H, Dhouioui S, Zidi N, Mchiri R, Mrad K, et al. HLA-G, HLA-E, and IDO overexpression predicts a worse survival of Tunisian patients with vulvar squamous cell carcinoma. HLA. 2019;94(1):11–24.PubMed
43.
go back to reference Zhou S, Zhao L, Liang Z, Liu S, Li Y, Liu S, Yang H, Liu M, Xi M. Indoleamine 2,3-dioxygenase 1 and programmed cell death-ligand 1 co-expression predicts poor pathologic response and recurrence in esophageal squamous cell carcinoma after neoadjuvant chemoradiotherapy. Cancers (Basel). 2019;11(2):169.PubMedCentralCrossRef Zhou S, Zhao L, Liang Z, Liu S, Li Y, Liu S, Yang H, Liu M, Xi M. Indoleamine 2,3-dioxygenase 1 and programmed cell death-ligand 1 co-expression predicts poor pathologic response and recurrence in esophageal squamous cell carcinoma after neoadjuvant chemoradiotherapy. Cancers (Basel). 2019;11(2):169.PubMedCentralCrossRef
44.
go back to reference Tsai Y, Jou Y, Tsai H, Cheong I, Tzai T. Indoleamine-2,3-dioxygenase-1 expression predicts poorer survival and up-regulates ZEB2 expression in human early stage bladder cancer. Urol Oncol. 2019;37(11):810.e17–27.CrossRef Tsai Y, Jou Y, Tsai H, Cheong I, Tzai T. Indoleamine-2,3-dioxygenase-1 expression predicts poorer survival and up-regulates ZEB2 expression in human early stage bladder cancer. Urol Oncol. 2019;37(11):810.e17–27.CrossRef
Metadata
Title
The prognostic value of IDO expression in solid tumors: a systematic review and meta-analysis
Authors
Sen Wang
Jia Wu
Han Shen
Junjun Wang
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
Solid Tumor
Published in
BMC Cancer / Issue 1/2020
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-020-06956-5

Other articles of this Issue 1/2020

BMC Cancer 1/2020 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine