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Neutrophil-lymphocyte ratio as a predictor of recurrence and progression in patients with high-grade pT1 bladder cancer.


At diagnosis, about 75% of bladder cancers are non-muscle-invasive tumours (Ta, T1, and carcinoma in situ). (1) Of these, 20% are pT1 tumours, with 5-year recurrence and progression rates of 30% to 80% and 1% to 50%, respectively. (2-4) Recurrence and progression of these tumours are predicted based on the scores and risk tables of the European Organization for Research and Treatment of Cancer (EORTC); no biochemical indicators are currently used for this purpose. It is particularly difficult to predict the behaviour of high-grade pT1 superficial bladder tumours over time. Such tumours either do not show recurrence or progress to muscle-invasive and metastatic stages. This complicates the clinician's decision-making process regarding follow-up and treatment. (5)

Many studies have shown that inflammation plays a role in tumour response to systemic treatment, tumour metastasis, and angiogenesis in the formation and progression stages of most cancer types. (6) The neutrophil-lymphocyte ratio (NLR) is an indicator of systemic inflammation and is convenient and inexpensive to measure. Recent studies have demonstrated that a high NLR is an important marker of recurrence and poor prognosis in colorectal, gastric, ovarian, and thyroid cancers, as well as in renal and hepatocellular carcinoma and malignant mesothelioma. (7-13)

Our aim in this study was to determine the value of the preoperative NLR in predicting recurrence and progression of high-grade pT1 non-muscle-invasive bladder tumours during a 5-year follow-up period.


Patient selection

We retrospectively evaluated the data of 1100 patients with bladder cancer who underwent transurethral resection and were monitored at 4 medical centres from 2008 to 2013. Approval for this study was obtained from the ethics committee at our university. The tumours were graded according to the World Health Organization-International Society of Urologic Pathology 2004 guidelines and the TNM 2002 staging system. All pertinent laboratory and pathology results (tumour size and number, presence of carcinoma in situ, retransurethral resection [TUR], postoperative immunotherapy and chemotherapy), and medical data were obtained from the hospital databases. The recurrence and progression status was determined for each patient based on these data. Recurrence was defined as the relapse of transitional cell carcinoma of the bladder at any pathological stage after initial surgery. Re-TUR was defined as the TUR which was performed 2 to 6 weeks after the initial transurethral resection. Patients with non-transitional cell bladder cancers, carcinoma in situ, acute inflammatory disease, bleeding disorders, hematological disorders, autoimmune diseases, any malignancies other than bladder tumour, preoperative active infection, or a history of splenectomy as well as patients on maintenance intravesical chemotherapy after transurethral resection were excluded from the study. Of the 1100 examined patients, we consecutively selected 166 patients with pathologically newly diagnosed high-grade pT1 tumours after initial surgery. When we were designing our study, we thought that the systemic inflammatory effects of pTa and low-grade superficial bladder tumors would be very low. Among these tumours, pT1 G3 tumours would be at a greater risk of recurrence and progression; therefore, we included only patients with pT1 G3 tumours. The follow-up period was calculated from the date of surgery, to either the last follow-up or death.

Blood tests

Data obtained from the patients' routine preoperative test results included the neutrophil count, lymphocyte count, red cell distribution width, and mean platelet volume. The NLR was determined by dividing the absolute neutrophil count by the absolute lymphocyte count.

Statistical methods

Statistical analyses were performed using IBM SPSS Statistics for Windows, version 20.0 (IBM Corp., Armonk, NY). Continuous variables were tested for normality by the Kolmogorov-Smirnov test. Normally distributed data were presented as means [+ or -] standard deviation. The rates and proportions of discrete variables were determined using the chi-squared test. The median with data range (minimum to maximum) was used for non-normally distributed data. The independent samples t-test and Mann-Whitney U test were used for parametric and nonparametric groups, respectively. Correlations between tumour size and recurrence were evaluated using Spearman's rank correlation coefficient. Potential predictors of recurrence and progression in individual patients with superficial transitional cell cancer of the bladder were initially compared, and variables that showed a p value of <0.05 were included in a logistic regression model. Results were expressed as odds ratio (OR) and 95% confidence interval (CI). The two-sided p value of <0.05 was considered statistically significant.


In total, 166 patients were enrolled in the study (152 male, 14 female). The patients were evaluated as two separate groups in terms of recurrence and progression. The mean follow-up period was 24.2 months (interquartile range 13.8-36.6 months).

Spearman's correlation test showed a statistically significant positive correlation between tumour size and recurrence (r = 0.368, p < 0.001). In the recurrence group, the tumour size was [less than or equal to]3 cm in 20 patients (31.2%) and >3 cm in 45 patients (69.2%). A statistically significant difference was found between recurrence and tumour size (p < 0.001). A statistically significant positive correlation was also found between tumour size and progression (r = 0.171, p = 0.028). In the progression group, the tumour size was [less than or equal to]3 cm in 6 patients (31.6%) and >3 cm in 13 patients (68.4%). However, there was no statistically significant difference between progression and tumour size (p = 0.097) (Table 1).

After Spearman's correlation analysis there was positive correlation between tumour number and recurrence (r = 0.361, p < 0.001). Recurrence rates were significantly higher in patients with multiple tumours than in patients with a single tumour (59.4% vs. 40.6%, respectively, p < 0.001). There was also a positive correlation between tumour numbers and progression (r = 0.211, p = 0.006). Progression rates were significantly higher in patients with multiple tumours than in patients with a single tumour (66.7% vs. 33.3%, respectively, p = 0.006) (Table 1). Similarly, there was a positive correlation between re-TUR and recurrence (r = 0.25, p = 0.001); recurrence rates were significantly higher in patients with re-TUR than in patients who were treated once (41.3% vs. 18.4%, respectively, p = 0.001). There was no statistically significant relation between progression rates and re-TUR (p = 0.080).

The Spearman's correlation test revealed a statistically significant relation between smoking and reccurence (r = 0.246 p = 0.007). Among the patients in the smoking group, 48 (64%) had reccurence, while 36 (86.7%) did not. Consequently, there was a statistically significant relation between smoking and reccurence (p = 0.007).

The NLR was 2.8 [+ or -] 2.7 (range: 1.4-1 6.8) in the recurrence group and 2.2 [+ or -] 1.2 (range: 0.7-8.2) in the non-recurrence group. A significant correlation was found between recurrence and the NLR. According to receiver operating characteristic (ROC) analysis, the optimum cut-off value for the NLR was [greater than or equal to]2.43 (74% sensitivity, 60% specificity, p < 0.001; area under the curve [AUC] 0.687, 95% CI, 0.607-0.767) (Fig. 1). The NLR was 2.6 [+ or -] 3.4 (range: 1.9-1 6.8) in the progression group and 2.5 [+ or -] 1.7 (range: 0.7-16.3) in the non-progression group. No significant correlation was found between progression and the NLR (p = 0.34) (Table 1).

In univariate analyses, tumour size greater than 3 cm, multiple tumors, and NLR of [greater than or equal to]2.43 were risk factors for recurrence. Multivariate logistic regression analysis determined that the following factors were independent predictors of recurrence in patients with high-grade pT1 non-muscle-invasive bladder cancer: tumour number (OR 5.32, 95% CI 2.10-12.90), NLR of [greater than or equal to]2.43 (OR 2.587; 95% CI 1.156-5.789), and smoking (OR 4.17, 95% CI 1.31-13.21) (Table 2). Since there was a significant correlation between tumour size and number, only tumour number was used in the multivariate analysis.

Multivariate logistic regression analysis determined only tumour number as an independent predictive factor to determine progression in patients with high-grade pT1 non-muscle-invasive bladder cancer (OR 3.29; 95% CI 1.08-10.06) (Table 3).



Many studies have demonstrated a link between systemic inflammation and cancer development and prognosis. (6,14-16) The NLR indicates the presence of systemic inflammation. The correlation between a high NLR and poor prognosis and recurrence in patients with cancer has been confirmed. (9,13,17-22) In the present study, the optimal cut-off value of the NLR as an indicator of recurrence and progression in patients with bladder cancer was [greater than or equal to]2.43. Patients with an NLR above this value exhibited significantly higher recurrence, but no progression, highlighting the potential role of the NLR in pT1 superficial bladder tumours. There is limited information on this topic in the literature. To our knowledge, this is the first clinical study investigating the correlation between the NLR and recurrence in patients with only high-grade pT1 bladder tumours.

The neutrophil and lymphocyte counts play important roles in systemic inflammation. The neutrophil count is increased by anti-apoptotic markers that affect tumour growth and progression (NF-[kappa]B), growth factors, and pro-angiogenic factors (VEGF). (23-25) The lymphocytic response is the main component in the control of cancer progression. Lymphocytopaenia leads to a decrease in the cellular immune response. While some studies have reported that decreased T-cell activity inside the tumour speeds up primary tumour progression, other studies have shown a link between lymphocytes and the cell-mediated response with respect to tumour infiltration;. Additionally, a low level of lymphocytic infiltration at tumour margins indicates a poor prognosis. (17,26,27) The fact that the NLR indicates only part of the inflammatory response somewhat limits its value as a marker. However, the NLR is still a convenient, inexpensive, and reproducible parameter that demonstrates the link between inflammation and tumour development.

Few studies have examined the link between an increased NLR and muscle-invasive bladder cancers. Some of these studies have shown that the risk of invasion significantly increases beyond a certain cut-off NLR value and that a high NLR is significantly correlated with the pathologic stage. (28-30) In a recent study that evaluates the NRL in terms of reccurence and progression in non-invasive bladder cancer, the NLR cut-off point for reccurence and progression was 2.43 and 2.41, respectively. A statistically significant increase in terms of reccurence and progression has been found among individuals with NLR levels over the cut-off limit. A positive correlation between tumour grade and higher levels of NRL has been found as well. (31) In our study, while the cut-off limit for NLR was able to establish a significant difference in reccurence, we could not find a significant difference regarding progression. In the study mentioned above patients with pTa and pT1 tumours were evaluated; (31) in our study, however, we evaluated only high-grade pT1 tumours. Therefore we considered our study more significant regarding case homogenity and number.

Several recent studies also examined the link between the preoperative NLR and recurrence of other types of cancer. Motomura and colleagues determined a NLR cut-off value of [greater than or equal to]4 for recurrence of hepatocellular carcinoma. (19) Mallappa and colleagues found that the stage of colorectal cancer and a preoperative NLR of >5 were important independent risk factors for recurrence. (21) In a study of recurrence of clear-cell renal carcinoma, Ohno and colleagues reported a significant difference in the 10-year survival rate between patients with an NLR of [greater than or equal to]2.7 and those with an NLR of <2.7. (22) All of these findings are consistent with the results obtained in our present study regarding the NLR cut-off value beyond which recurrence significantly increased.

In a study carried out with patients on sunitinib for meta-static renal cell carcinoma, Keizman and colleagues found that NLR values lower than 3 prior to treatment correlated with overall survival and progression-free survival. (32) In a recent meta-analysis evaluating the role of NLR in solid tumours, overall survival, progression-free survival and recurrence-free survival negatively correlated with NRL values over the cut-off point. (33) Contrary to previous studies, in our study, no statistically correlation was found between NLR and progression.


Our results indicate that a high preoperative NLR can play an important role in determining recurrence of superficial transitional cell type high-grade pT1 bladder tumours. However, it did not accurately predict progression in this study, possibly because of the short follow-up period and small sample size. Prospective studies are required to validate the role of NLR as a prognostic marker in high-grade pT1 bladder cancers.

Competing interests: Authors declare no competing financial or personal interests.

This paper has been peer-reviewed.


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Correspondence: Dr. Mehmet Emin Ozyalvacli, Abant izzet Baysal Universitesi Tip Fakultesi, Golkoy 14280 Bolu/Turkey;

Mehmet Emin Ozyalvacli, MD; * Gulzade Ozyalvacli, MD ([dagger]) Ramazan Kocaaslan MD; ([section]) Kursat Cecen, MD; ([section]) Ugur Uyeturk, MD; * Eray Kemahli, MD; * Adnan Gucuk, MD *

* Department of Urology, Faculty of Medicine, Abant izzet Baysal University, Bolu, Turkey; ([dagger]) Department of Pathology, Faculty of Medicine, Abant izzet Baysal University, Bolu, Turkey; ([section]) Department of Urology, Faculty of Medicine, Kafkas University, Kars, Turkey
Table 1. Comparison of patients according to the presence
of recurrence and progression


                                Absent N = 101

Sex (F/M)                            6/95

Age (year) *                   67.3 [+ or -] 11

MPV *                          8.2 [+ or -] 1.2

RDW *                         15.6 [+ or -] 1.6

NLR[yen]                        2.2 (0.7-8.2)

BCG usage                         36 (35.6%)

Single dose                       20 (19.6%)

Tumour         [less than         65 (64.4%)
size (cm)      or equal

               >3                 36 (35.6%)

No. tumours    Single             78 (76.5%)

               Multiple           24 (23.5%)

Smoking                            48 (64%)


                              Present N = 65     p value

Sex (F/M)                          8/57           0.15

Age (year) *                 67.7 [+ or -] 9.4    0.84

MPV *                        8.5 [+ or -] 1.3     0.09

RDW *                        15.5 [+ or -] 1.3    0.67

NLR[yen]                      2.8 (1.4-16.8)     <0.001

BCG usage                       17 (26.2%)         0.2

Single dose                     14 (21.9%)        0.725

Tumour         [less than       20 (30.8%)        0.001
size (cm)      or equal

               >3               45 (69.2%)

No. tumours    Single           26 (40.6%)       <0.001

               Multiple         38 (59.4%)

Smoking                         39 (86.7%)        0.007


                                Absent N = 147

Sex (F/M)                           11/136

Age (year) *                  67.5 [+ or -] 10.5

MPV *                          8.4 [+ or -] 1.3

RDW *                         15.6 [+ or -] 1.5

NLR[yen]                        2.5 (0.7-16.3)

BCG usage                         50 (34.0%)

Single dose                       30 (20.3%)

Tumour         [less than         79 (53.7%)
size (cm)      or equal

               >3                 68 (46.3%)

No. tumours    Single             98 (66.2%)

               Multiple           50 (33.8%)

Smoking                           77 (70.6%)


                               Present N = 19     p value

Sex (F/M)                           3/16           0.22

Age (year) *                 67.5 [+ or -] 10.2      1

MPV *                         8.2 [+ or -] 1.2     0.57

RDW *                        15.4 [+ or -] 1.3     0.46

NLR[yen]                       2.6 (1.9-16.8)      0.34

BCG usage                        3 (15.8%)         0.11

Single dose                      4 (22.2%)         0.846

Tumour         [less than        6 (31.6%)         0.047
size (cm)      or equal

               >3                13 (68.4%)

No. tumours    Single            6 (33.3%)         0.006

               Multiple          12 (66.7%)

Smoking                          10 (90.9%)        0.15

* mean [+ or -] standard deviation; [yen] median(minimum-maximum);
BCG: Bacillus Calmette-Guerin; MPV: mean platelet volume;
NLR: neutrophil-lymphocyte ratio; RDW: red cell distribution.

Table 2. Univariate and multivariate logistic regression
analysis of independent predictive factors for recurrence
in highgrade pT1 bladder cancer

                                       Univariate analysis

                 Reference        OR       95% CI     p value

Age            [greater than     0.95    0.50-1.81      0.87
               or equal to]65

Sex                Female        2.29    0.75-6.93      0.13

BCG Usage                        0.66    0.33-1.32      0.24

No. tumours       Multiple       4.75    2.41-9.35     <0.001

NLR            [greater than     4.29    2.15-8.54     <0.001
              or equal to]2.43

Smoking                          3.66    1.37-9.74     0.007

                                      Multivariate analysis

                 Reference        OR        95% CI      p value

Age            [greater than     1.09     0.42-2.85       0.84
               or equal to]65

Sex                Female        2.58     0.40-16.64      0.31

BCG Usage                        0.75     0.33-2.23       0.75

No. tumours       Multiple       5.32      2.1-12.9      <0001

NLR            [greater than     3.81     1.50-9.67      0.005
              or equal to]2.43

Smoking                          4.17    1.31-13.210     0.015

OR: odds ratio; CI: confidence interval; BCG: Bacillus
Calmette-Guerin; NLR: neutrophil-lymphocyte ratio.

Table 3. Univariate and multivariate logistic regression analysis
of independent predictive factors for progression in highgrade
pT1 bladder cancer

                                        Univariate analysis

                  Reference        OR       95% CI      p value

Age             [greater than      0.9     0.33-2.47     0.842
                or equal to]65

Sex                 Female         2.5     0.62-9.93     0.183

BCG Usage                         0.39     0.11-1.42     0.141

No. tumours        Multiple       3.92     1.4-11.06     0.006

NLR             [greater than     1.79     0.64-5.04     0.262
               or equal to]2.43

Smoking                           1.52     0.57-4.1      0.403

                                       Multivariate analysis

                  Reference        OR       95% CI      p value

Age             [greater than     0.73     0.25-2.15     0.570
                or equal to]65

Sex                 Female        1.97     0.43-9.03     0.383

BCG Usage                         0.47     0.13-1.77     0.265

No. tumours        Multiple       3.29    1.08-10.06     0.036

NLR             [greater than     1.47     0.49-4.38     0.490
               or equal to]2.43

Smoking                           1.08     0.37-3.18     0.891

OR: odds ratio; CI: confidence interval; BCG: Bacillus
Calmette-Guerin; NLR: neutrophil-lymphocyte ratio.
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Author:Ozyalvacli, Mehmet Emin; Ozyalvacli, Gulzade; Kocaaslan, Ramazan; Cecen, Kursat; Uyeturk, Ugur; Kema
Publication:Canadian Urological Association Journal (CUAJ)
Article Type:Report
Date:Mar 1, 2015
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