Prognostic value of preoperative hematologic biomarkers in urothelial carcinoma of the bladder treated with radical cystectomy: a systematic review and meta-analysis

Antoni S, Ferlay J, Soerjomataram I et al (2017) Bladder cancer incidence and mortality: a global overview and recent trends. Eur Urol 71(1):96–108. https://doi.org/10.1016/j.eururo.2016.06.010 Babjuk M, Burger M, Comperat EM et al (2019) European Association of Urology Guidelines on Non-muscle-invasive Bladder Cancer (TaT1 and Carcinoma In Situ)—2019 Update. Eur Urol 76(5):639–657. https://doi.org/10.1016/j.eururo.2019.08.016 Alfred Witjes J, Lebret T, Comperat EM et al (2017) Updated 2016 EAU guidelines on muscle-invasive and metastatic bladder cancer. Eur Urol 71(3):462–475. https://doi.org/10.1016/j.eururo.2016.06.020 Abdollah F, Gandaglia G, Thuret R et al (2013) Incidence, survival and mortality rates of stage-specific bladder cancer in United States: a trend analysis. Cancer Epidemiol 37(3):219–225. https://doi.org/10.1016/j.canep.2013.02.002 Zargar H, Espiritu PN, Fairey AS et al (2015) Multicenter assessment of neoadjuvant chemotherapy for muscle-invasive bladder cancer. Eur Urol 67(2):241–249. https://doi.org/10.1016/j.eururo.2014.09.007 Kluth LA, Black PC, Bochner BH et al (2015) Prognostic and prediction tools in bladder cancer: a comprehensive review of the literature. Eur Urol 68(2):238–253. https://doi.org/10.1016/j.eururo.2015.01.032 Putluri N, Shojaie A, Vasu VT et al (2011) Metabolomic profiling reveals potential markers and bioprocesses altered in bladder cancer progression. Can Res 71(24):7376–7386. https://doi.org/10.1158/0008-5472.can-11-1154 Karakiewicz PI, Shariat SF, Palapattu GS et al (2006) Nomogram for predicting disease recurrence after radical cystectomy for transitional cell carcinoma of the bladder. J Urol 176(4 Pt 1):1354–1361. https://doi.org/10.1016/j.juro.2006.06.025(discussion 1361-1352) Shariat SF, Palapattu GS, Karakiewicz PI et al (2007) Discrepancy between clinical and pathologic stage: impact on prognosis after radical cystectomy. Eur Urol 51(1):137–149. https://doi.org/10.1016/j.eururo.2006.05.021(discussion 149-151) Lucca I, Jichlinski P, Shariat SF et al (2016) The neutrophil-to-lymphocyte ratio as a prognostic factor for patients with urothelial carcinoma of the bladder following radical cystectomy: validation and meta-analysis. Eur Urol Focus 2(1):79–85. https://doi.org/10.1016/j.euf.2015.03.001 Liberati A, Altman DG, Tetzlaff J et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 6(7):e1000100. https://doi.org/10.1371/journal.pmed.1000100 Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25(9):603–605. https://doi.org/10.1007/s10654-010-9491-z Deeks JJ, Dinnes J, D'Amico R et al (2003) Evaluating non-randomised intervention studies. Health Technol Assess (Winchester, England) 7(27):1–173. https://doi.org/10.3310/hta7270(iii-x) Altman DG, Bland JM (2011) How to obtain the confidence interval from a P value. BMJ (Clin Res Ed) 343:d2090. https://doi.org/10.1136/bmj.d2090 Altman DG, Bland JM (2011) How to obtain the P value from a confidence interval. BMJ (Clin Res Ed) 343:d2304. https://doi.org/10.1136/bmj.d2304 DerSimonian R, Kacker R (2007) Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trials 28(2):105–114. https://doi.org/10.1016/j.cct.2006.04.004 DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188. https://doi.org/10.1016/0197-2456(86)90046-2 Higgins JP, Thompson SG, Deeks JJ et al (2003) Measuring inconsistency in meta-analyses. BMJ (Clin Res Ed) 327(7414):557–560. https://doi.org/10.1136/bmj.327.7414.557 Buisan O, Orsola A, Areal J et al (2017) Low pretreatment neutrophil-to-lymphocyte ratio predicts for good outcomes in patients receiving neoadjuvant chemotherapy before radical cystectomy for muscle invasive bladder cancer. Clin Genitour Cancer 15(1):145–151.e142. https://doi.org/10.1016/j.clgc.2016.05.004 Calvete J, Larrinaga G, Errarte P et al (2019) The coexpression of fibroblast activation protein (FAP) and basal-type markers (CK 5/6 and CD44) predicts prognosis in high-grade invasive urothelial carcinoma of the bladder. Hum Pathol 91:61–68. https://doi.org/10.1016/j.humpath.2019.07.002 Chipollini JJ, Tang DH, Patel SY et al (2017) Perioperative transfusion of leukocyte-depleted blood products in contemporary radical cystectomy cohort does not adversely impact short-term survival. Urology 103:142–148. https://doi.org/10.1016/j.urology.2016.12.015 D'Andrea D, Moschini M, Gust KM et al (2017) Lymphocyte-to-monocyte ratio and neutrophil-to-lymphocyte ratio as biomarkers for predicting lymph node metastasis and survival in patients treated with radical cystectomy. J Surg Oncol 115(4):455–461. https://doi.org/10.1002/jso.24521 Ergani B, Türk H, Ün S et al (2015) Prognostic effect of preoperative anemia in patients who have undergone radical cystectomy for bladder cancer. Cancer Treat Commun 4:196–199. https://doi.org/10.1016/j.ctrc.2015.11.005 Gershman B, Moreira DM, Tollefson MK et al (2016) The association of ABO blood type with disease recurrence and mortality among patients with urothelial carcinoma of the bladder undergoing radical cystectomy. Urol Oncol 34(1):4.e1–9. https://doi.org/10.1016/j.urolonc.2015.07.023 Gierth M, Mayr R, Aziz A et al (2015) Preoperative anemia is associated with adverse outcome in patients with urothelial carcinoma of the bladder following radical cystectomy. J Cancer Res Clin Oncol 141(10):1819–1826. https://doi.org/10.1007/s00432-015-1957-7 Gondo T, Nakashima J, Ohno Y et al (2012) Prognostic value of neutrophil-to-lymphocyte ratio and establishment of novel preoperative risk stratification model in bladder cancer patients treated with radical cystectomy. Urology 79(5):1085–1091. https://doi.org/10.1016/j.urology.2011.11.070 Gorgel SN, Kose O, Koc EM et al (2017) The prognostic significance of preoperatively assessed AST/ALT (De Ritis) ratio on survival in patients underwent radical cystectomy. Int Urol Nephrol 49(9):1577–1583. https://doi.org/10.1007/s11255-017-1648-1 Grimm T, Buchner A, Schneevoigt B et al (2016) Impact of preoperative hemoglobin and CRP levels on cancer-specific survival in patients undergoing radical cystectomy for transitional cell carcinoma of the bladder: results of a single-center study. World J Urol 34(5):703–708. https://doi.org/10.1007/s00345-015-1680-7 Ha YS, Kim SW, Chun SY et al (2019) Association between De Ritis ratio (aspartate aminotransferase/alanine aminotransferase) and oncological outcomes in bladder cancer patients after radical cystectomy. BMC urology 19(1):10. https://doi.org/10.1186/s12894-019-0439-7 Hermanns T, Bhindi B, Wei Y et al (2014) Pre-treatment neutrophil-to-lymphocyte ratio as predictor of adverse outcomes in patients undergoing radical cystectomy for urothelial carcinoma of the bladder. Br J Cancer 111(3):444–451. https://doi.org/10.1038/bjc.2014.305 Jo JK, Jeong SJ, Hong SK, Byun SS, Lee SE, Oh JJ (2016) The impact of preoperative anemia on oncologic outcome in patients undergoing radical cystectomy for urothelial carcinoma of the bladder. Int Urol Nephrol 48(4):489–494. https://doi.org/10.1007/s11255-016-1219-x Jokisch JF, Grimm T, Buchner A et al (2019) Preoperative thrombocytosis in patients undergoing radical cystectomy for urothelial cancer of the bladder: an independent prognostic parameter for an impaired oncological outcome. Urol Int. https://doi.org/10.1159/000500729 Kang M, Balpukov UJ, Jeong CW et al (2017) Can the preoperative neutrophil-to-lymphocyte ratio significantly predict the conditional survival probability in muscle-invasive bladder cancer patients undergoing radical cystectomy? Clin Genitour Cancer 15(3):e411–e420. https://doi.org/10.1016/j.clgc.2016.10.015 Kluth LA, Xylinas E, Rieken M et al (2015) Prognostic model for predicting survival in patients with disease recurrence following radical cystectomy. Eur Urol Focus 1(1):75–81. https://doi.org/10.1016/j.euf.2014.10.003 Ku JH, Kang M, Kim HS et al (2015) The prognostic value of pretreatment of systemic inflammatory responses in patients with urothelial carcinoma undergoing radical cystectomy. Br J Cancer 112(3):461–467. https://doi.org/10.1038/bjc.2014.631 Kwon T, Jeong IG, You D et al (2014) Obesity and prognosis in muscle-invasive bladder cancer: the continuing controversy. Int J Urol 21(11):1106–1112. https://doi.org/10.1111/iju.12530 Lambert JW, Ingham M, Gibbs BB et al (2013) Using preoperative albumin levels as a surrogate marker for outcomes after radical cystectomy for bladder cancer. Urology 81(3):587–592. https://doi.org/10.1016/j.urology.2012.10.055 Liu J, Dai Y, Zhou F et al (2016) The prognostic role of preoperative serum albumin/globulin ratio in patients with bladder urothelial carcinoma undergoing radical cystectomy. Urol Oncol 34(11):484.e481–484.e488. https://doi.org/10.1016/j.urolonc.2016.05.024 Liu Z, Huang H, Li S et al (2017) The prognostic value of preoperative serum albumin-globulin ratio for high-grade bladder urothelial carcinoma treated with radical cystectomy: A propensity score-matched analysis. J Cancer Res Ther 13(5):837–843. https://doi.org/10.4103/jcrt.JCRT_237_17 Matsumoto A, Nakagawa T, Kanatani A et al (2018) Preoperative chronic kidney disease is predictive of oncological outcome of radical cystectomy for bladder cancer. World J Urol 36(2):249–256. https://doi.org/10.1007/s00345-017-2141-2 Miyake M, Morizawa Y, Hori S et al (2017) Integrative assessment of pretreatment inflammation-, nutrition-, and muscle-based prognostic markers in patients with muscle-invasive bladder cancer undergoing radical cystectomy. Oncology 93(4):259–269. https://doi.org/10.1159/000477405 Moschini M, Suardi N, Pellucchi F et al (2014) Impact of preoperative thrombocytosis on pathological outcomes and survival in patients treated with radical cystectomy for bladder carcinoma. Anticancer Res 34(6):3225–3230 Ozcan C, Telli O, Ozturk E et al (2015) The prognostic significance of preoperative leukocytosis and neutrophil-to-lymphocyte ratio in patients who underwent radical cystectomy for bladder cancer. Canad Urological Assoc Journal de l'Association des urologues du Canada 9(11–12):E789–794. https://doi.org/10.5489/cuaj.3061 Rajwa P, Zyczkowski M, Paradysz A et al (2018) Evaluation of the prognostic value of LMR, PLR, NLR, and dNLR in urothelial bladder cancer patients treated with radical cystectomy. Eur Rev Med Pharmacol Sci 22(10):3027–3037. https://doi.org/10.26355/eurrev_201805_15060 Schubert T, Todenhofer T, Mischinger J et al (2016) The prognostic role of pre-cystectomy hemoglobin levels in patients with invasive bladder cancer. World J Urol 34(6):829–834. https://doi.org/10.1007/s00345-015-1693-2 Sejima T, Morizane S, Yao A et al (2014) Prognostic impact of preoperative hematological disorders and a risk stratification model in bladder cancer patients treated with radical cystectomy. Int J Urol 21(1):52–57. https://doi.org/10.1111/iju.12161 Tan YG, Eu E, Lau KamOn W et al (2017) Pretreatment neutrophil-to-lymphocyte ratio predicts worse survival outcomes and advanced tumor staging in patients undergoing radical cystectomy for bladder cancer. Asian J Urol 4(4):239–246. https://doi.org/10.1016/j.ajur.2017.01.004 Todenhofer T, Renninger M, Schwentner C et al (2012) A new prognostic model for cancer-specific survival after radical cystectomy including pretreatment thrombocytosis and standard pathological risk factors. BJU Internat 110(11 Pt B):E533–E540. https://doi.org/10.1111/j.1464-410X.2012.11231.x Un S, Turk H, Dindar AS et al (2018) Does preoperative neutrophil/lymphocyte rate have an effect on survival of the bladder cancer patients who received radical cystectomy? J Cancer Res Ther 14(2):432–436. https://doi.org/10.4103/0973-1482.183555 Viers BR, Boorjian SA, Frank I et al (2014) Pretreatment neutrophil-to-lymphocyte ratio is associated with advanced pathologic tumor stage and increased cancer-specific mortality among patients with urothelial carcinoma of the bladder undergoing radical cystectomy. Eur Urol 66(6):1157–1164. https://doi.org/10.1016/j.eururo.2014.02.042 Yang MH, Yen CC, Chen PM et al (2002) Prognostic-factors-based risk-stratification model for invasive urothelial carcinoma of the urinary bladder in Taiwan. Urology 59(2):232–238. https://doi.org/10.1016/s0090-4295(0101590-4(discussion 238-239) Yoshida T, Kinoshita H, Yoshida K et al (2016) Prognostic impact of perioperative lymphocyte-monocyte ratio in patients with bladder cancer undergoing radical cystectomy. Tumour Biolo 37(8):10067–10074. https://doi.org/10.1007/s13277-016-4874-8 Yuk HD, Jeong CW, Kwak C et al (2019) De Ritis Ratio (Aspartate Transaminase/Alanine Transaminase) as a Significant Prognostic Factor in Patients Undergoing Radical Cystectomy with Bladder Urothelial Carcinoma: a Propensity Score-Matched Study. Dis Markers 2019:6702964. https://doi.org/10.1155/2019/6702964 Botros M, Sikaris KA (2013) The de ritis ratio: the test of time. Clin Biochem Rev 34(3):117–130 Conde VR, Oliveira PF, Nunes AR et al (2015) The progression from a lower to a higher invasive stage of bladder cancer is associated with severe alterations in glucose and pyruvate metabolism. Exp Cell Res 335(1):91–98. https://doi.org/10.1016/j.yexcr.2015.04.007 Warburg O (1956) On the origin of cancer cells. Science (New York, NY) 123(3191):309–314. https://doi.org/10.1126/science.123.3191.309 Dorward A, Sweet S, Moorehead R et al (1997) Mitochondrial contributions to cancer cell physiology: redox balance, cell cycle, and drug resistance. J Bioenerg Biomembr 29(4):385–392. https://doi.org/10.1023/a:1022454932269 Fantin VR, St-Pierre J, Leder P (2006) Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 9(6):425–434. https://doi.org/10.1016/j.ccr.2006.04.023 Greenhouse WV, Lehninger AL (1976) Occurrence of the malate-aspartate shuttle in various tumor types. Can Res 36(4):1392–1396 Tai YS, Chen CH, Huang CY et al (2015) Diabetes mellitus with poor glycemic control increases bladder cancer recurrence risk in patients with upper urinary tract urothelial carcinoma. Diabetes/Metab Res Rev 31(3):307–314. https://doi.org/10.1002/dmrr.2614 Whyard T, Waltzer WC, Waltzer D et al (2016) Metabolic alterations in bladder cancer: applications for cancer imaging. Exp Cell Res 341(1):77–83. https://doi.org/10.1016/j.yexcr.2016.01.005 Kitajima K, Yamamoto S, Fukushima K et al (2016) FDG-PET/CT as a post-treatment restaging tool in urothelial carcinoma: Comparison with contrast-enhanced CT. Eur J Radiol 85(3):593–598. https://doi.org/10.1016/j.ejrad.2015.12.017 Dewys WD, Begg C, Lavin PT et al (1980) Prognostic effect of weight loss prior to chemotherapy in cancer patients Eastern Cooperative Oncology Group. Am J Med 69(4):491–497. https://doi.org/10.1016/s0149-2918(05)80001-3 Chandra RK (1999) Nutrition and immunology: from the clinic to cellular biology and back again. Proc Nutr Soc 58(3):681–683. https://doi.org/10.1017/s0029665199000890 Barbosa-Silva MC (2008) Subjective and objective nutritional assessment methods: what do they really assess? Curr Opin Clin Nutr Metab Care 11(3):248–254. https://doi.org/10.1097/MCO.0b013e3282fba5d7 McMillan DC, Watson WS, O'Gorman P et al (2001) Albumin concentrations are primarily determined by the body cell mass and the systemic inflammatory response in cancer patients with weight loss. Nutr Cancer 39(2):210–213. https://doi.org/10.1207/S15327914nc392_8 Vaupel P, Thews O, Hoeckel M (2001) Treatment resistance of solid tumors: role of hypoxia and anemia. Med Oncol (Northwood, London, England) 18(4):243–259. https://doi.org/10.1385/mo:18:4:243 Vaupel P (2004) The role of hypoxia-induced factors in tumor progression. Oncologist 9(Suppl 5):10–17. https://doi.org/10.1634/theoncologist.9-90005-10 Dachs GU, Tozer GM (2000) Hypoxia modulated gene expression: angiogenesis, metastasis and therapeutic exploitation. Eur J Cancer (Oxford, England: 1990) 36(13 Spec No):1649–1660. https://doi.org/10.1016/s0959-8049(00)00159-3 Semenza GL (2000) Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit Rev Biochem Mol Biol 35(2):71–103. https://doi.org/10.1080/10409230091169186 Wu S, Jiang F, Wu H et al (2018) Prognostic significance of hypoxia inducible factor-1alpha expression in patients with clear cell renal cell carcinoma. Mol Med Rep 17(3):4846–4852. https://doi.org/10.3892/mmr.2018.8409 Coquelle A, Toledo F, Stern S et al (1998) A new role for hypoxia in tumor progression: induction of fragile site triggering genomic rearrangements and formation of complex DMs and HSRs. Mol Cell 2(2):259–265. https://doi.org/10.1016/s1097-2765(00)80137-9 Andrews B, Shariat SF, Kim JH et al (2002) Preoperative plasma levels of interleukin-6 and its soluble receptor predict disease recurrence and survival of patients with bladder cancer. J Urol 167(3):1475–1481 Shariat SF, Semjonow A, Lilja H et al (2011) Tumor markers in prostate cancer I: blood-based markers. Acta Oncol (Stockholm, Sweden) 50(Suppl 1):61–75. https://doi.org/10.3109/0284186x.2010.542174 Lucca I, Hofbauer SL, Leitner CV et al (2016) Development of a preoperative nomogram incorporating biomarkers of systemic inflammatory response to predict nonorgan-confined urothelial carcinoma of the bladder at radical cystectomy. Urology 95:132–138. https://doi.org/10.1016/j.urology.2016.06.007 Raj DS (2009) Role of interleukin-6 in the anemia of chronic disease. Semin Arthritis Rheum 38(5):382–388. https://doi.org/10.1016/j.semarthrit.2008.01.006 Bartrons R, Caro J (2007) Hypoxia, glucose metabolism and the Warburg's effect. J Bioenerg Biomembr 39(3):223–229. https://doi.org/10.1007/s10863-007-9080-3 Ancey PB, Contat C, Meylan E (2018) Glucose transporters in cancer—from tumor cells to the tumor microenvironment. FEBS J 285(16):2926–2943. https://doi.org/10.1111/febs.14577 Chesney J (2006) 6-phosphofructo-2-kinase/fructose-2, 6-bisphosphatase and tumor cell glycolysis. Curr Opin Clin Nutr Metab Care 9(5):535–539. https://doi.org/10.1097/01.mco.0000241661.15514.fb