Stesura Seveso


Archivio Italiano di Urologia e Andrologia 2021; 93, 4436

ORIGINAL PAPER

No conflict of interest declared.

ation of renal fibrosis (4). The infiltrating lymphocytes,
monocytes/macrophages and mast cells activate and pro-
duce reactive oxygen species (ROS) after infection and
release fibrogenic cytokines and growth factors (5, 6). The
resulting damage causes interstitial inflammation, collagen
deposition and disruption of the normal tubular arrange-
ment. As a result, permanent parenchymal damage and
scar formation occur, which are accompanied by tubular
atrophy and interstitial fibrosis (7). Even if the infection is
treated and VUR is corrected, the inflammatory process
continues and scars may, therefore, develop (1).
It is known that the complete blood count parameters
vary qualitatively and quantitatively in inflammatory
processes (8) and that the neutrophil-to-lymphocyte ratio
(NLR) is effective in predicting inflammation (9). Platelets
also contribute to increased inflammation by enhancing
the secretion of cytokines at the beginning of inflamma-
tion (10). Mean thrombocyte volume (MPV) level can be
used as an indicator of platelet functions (11).
Tc-99m dimercaptosuccinic acid (DMSA) scintigraphy is
the gold standard in detecting the development of renal
scars after pyelonephritis (12). Pyelonephritic inflamma-
tory changes in the kidney occur immediately and can be
detected with DMSA. While some of these acute changes
resolve within 6 months, some lead to renal scarring (13).
Currently, the development of scars in patients cannot be
predicted as there is no easily accessible predictive mark-
er for renal scar development. If such a marker is identi-
fied, improvements can be made in the follow-up and
treatment algorithm of patients with VUR. 
The present study aims to compare the NLR and MPV
values in patients having VUR with and without renal
scarring. To the best of our knowledge, this is the first
study on the topic.

MATERIALS AND METHODS
The hospital records of patients diagnosed with VUR
using voiding cystourethrography (VCUG) between January
2008 and August 2020 were retrospectively reviewed.
Ethics committee approval was granted by our Faculty
Ethics Committee (HRU/16.06.27). Patients' age, frequen-
cy of past UTI episodes, use of prophylactic antibiotics,
physical examination findings, blood urea nitrogen and
creatinine, complete blood count, complete urinalysis,

Objectives: Vesicoureteral reflux (VUR)
exacerbates the risk of renal scarring by

establishing a ground for pyelonephritis. It is known that the
inflammatory process is more influential than the direct damage
caused by bacterial infection in the development of renal scars
after pyelonephritis. Therefore, the present study aims to inves-
tigate the relationship between renal scarring and systemic
inflammatory markers in patients with VUR.
Material and methods: Hundred and ninety-two patients (116
females, 76 males) diagnosed with VUR were divided into two
groups based on the presence or absence of renal scarring and
into three groups according to the grade of VUR (low, moderate
and high). Neutrophil count, lymphocyte count, mean platelet
volume (MPV) and neutrophil-to-lymphocyte ratio (NLR) were
compared among the groups.
Results: Of the 192 patients, 102 had renal scarring. The age
and gender distribution did not differ significantly between the
groups with and without renal scarring (p > 0.05). However, the
grade of reflux and lymphocyte count were significantly higher
in the group with renal scarring (p < 0.05), and the NLR was
significantly lower in the group with renal scarring (p < 0.05).
The lymphocyte count was significantly higher (p < 0.05) and
NLR was significantly lower in the high-grade VUR group
(p < 0.05). However, MPV values did not differ significantly
(p > 0.05) between the groups.
Conclusions: NLR can be used to predict renal scarring in
patients with VUR, especially in the period of 3-6 months after
the first attack of infection, and may even serve as a candidate
marker for treatment selection. However, larger series and
prospective studies are needed.

KEY WORDS: Vesicoureteral reflux; Neutrophil-to-lymphocyte
ratio; Pyelonephritis; Renal scarring.

Submitted 15 October 2021; Accepted 28 October 2021   

INTRODUCTION
Vesicoureteral reflux (VUR) is a functional and anatomical
disorder that can result in renal scarring, hypertension and
end-stage renal failure (1). VUR predisposes the patients to
urinary tract infection (UTI) and pyelonephritis and increas-
es the risk of scarring in the kidney (2). Renal scarring is an
important cause of hypertension and chronic renal failure
(CRF) in children and young adults (3). The etiopathogen-
esis of renal scarring has not been clearly understood.
However, lymphocytes play an important role in the initi-

Is there a relationship between renal scarring 
and neutrophil-to-lymphocyte ratio in patients 
with vesicoureteral reflux?

Mehmet Demir, İsmail Yağmur, Eyyup Sabri Pelit, Bülent Katı, Eser Ördek, Halil Çiftçi

Department of Urology, Harran University, Sanliurfa, Turkey.

DOI: 10.4081/aiua.2021.4.436

Summary



437Archivio Italiano di Urologia e Andrologia 2021; 93, 4

Renal scarring and neutrophil-to-lymphocyte ratio

urine culture, ultrasound (USG), VCUG and DMSA find-
ings were examined. The VCUG findings of the patients
were evaluated according to the standards of the
International Reflux Study in Children (14). Most of the
patients were admitted to our clinic with the pre-diagno-
sis of VUR after acute infection, for further investigation,
some of them were diagnosed with VUR after acute infec-
tion and for follow-up and treatment, and some of them
were directly admitted to our clinic because of recurrent
UTI. No new VCUG was performed in patients diagnosed
with VUR and referred to our clinic. Imaging was per-
formed in our hospital for patients who were referred
with a pre-diagnosis of VUR and did not have VCUG.
DMSA scintigraphs, provided that they were performed
3-6 months after the occurrence of UTI, were examined.
DMSA scintigraphies taken during the acute infection
period were not included in the study. 
The renal parenchymal scar was defined as cortical thin-
ning, volume loss, decreased DMSA uptake and renal
contour irregularities. Neutrophil count, lymphocyte
count and MPV values were recorded by examining the
results of complete blood count at the time of DMSA
acquisition, and it was established that the patients had
no active infection by demonstrating a sterile urine cul-
ture. Patients with malignant diseases and those on
chronic anti-inflammatory drug therapy were excluded
from the study. Patients with secondary VUR caused by
other factors, such as neurogenic bladder and posterior
urethral valve, and those with voiding dysfunction were
excluded from the study. Hundred and ninety-two
patients with accessible data were included in the study. 
The patients were divided into two groups based on the
presence or absence of renal scarring and into three
groups according to the grade of VUR (mild: grades I-II,
moderate: grade III; high: grades IV-V). Neutrophil
count, lymphocyte count, MPV values and NLR were
compared among the groups.

Statistical methods
Mean, standard deviation, median, minimum, maximum
value frequency and percentage were used for descriptive
statistics. Kolmogorov-Smirnov test was employed to
check the distribution of the variables. Mann-Whitney U
test was used for the comparison of the quantitative data.
Chi-square test was used for the comparison of the quali-
tative data. SPSS 26.0 was used for the statistical analysis.

RESULTS
Of the 192 patients with VUR, 116 were females, and 76
were males. The mean age of the patients was 5.4 ± 5
years. Of the patients, 124 had unilateral and 68 had
bilateral VUR (Table 1).
The age and gender distribution did not differ signifi-
cantly between patients with and without renal scarring
(p > 0.05). The rates of renal scarring were 9%, 32.5%,
57.1%, 67.3% and 65.6% in patients with grade I, II, III,
IV and V VUR, respectively. The VUR grade and lympho-
cyte counts were significantly higher (p < 0.05) and the
neutrophil count and NLR were significantly lower (p <
0.05) in the group with renal scarring than in the group
without renal scarring. The MPV values did not differ sig-

nificantly (p > 0.05) between the groups with and with-
out renal scarring (Table 2).
According to the grade of reflux, the patients were divid-
ed into three groups, that is, low (grades I-II), intermedi-
ate (grade III) and high (grades IV-V) VUR groups.
Lymphocyte count was significantly higher in the high-
grade VUR group than in the low- and moderate-VUR
groups (p < 0.05). NLR was significantly lower in the
high-grade VUR group than in the low- and moderate-
VUR groups (p < 0.05). However, neutrophil count and
MPV values did not differ significantly according to the
grade of VUR (p > 0.05) (Table 3).
In the sub-data analysis, the patients who were divided
into three groups (low, moderate and high) according to
the degree of reflux were further divided into two groups
based on the presence or absence of renal scarring. The
neutrophil count was significantly lower in scar-positive
patients with low-grade (grades I-II) VUR (p < 0.05) than
in scar-negative patients. However, lymphocyte count
and NLR did not differ significantly (p > 0.05) (Table 4).

Table 1. 
Demographic data of the patients.

Min-max Median  Mean ± sd/n-%
Age 0.10 - 36.00 4.00 5.40 ± 5.00
Gender Girl 116 60.4%

Boy 76 39.6%
Side Right 43 22.4%

Left 81 42.2%
Bilateral 68 35.4%

Grade I 11 5.7%
II 40 20.8%
III 63 32.8%
IV 46 24.0%
V 32 16.7%

Neutrophil 1.10 - 10.80 4.70 4.78 ± 1.89
Lymphocyte 1.30 - 9.90 3.70 4.07 ± 1.55
NLR 0.20 - 4.06 1.22 1.37 ± 0.79
MPV 4.20 - 10.70 6.20 6.36 ± 0.99

NLR: Neutrophil Lymphocyte Ratio; MPV: Mean Platelet Volume.

Table 2. 
Comparison of patients with and without renal scarring.

Scar (-) Scar (+) P
Mean ± sd/n-% Median  Mean ± sd/n-% Median 

Age 5.80 ± 6.36 4.00 5.04 ± 3.37 4.00 0.620 m

Gender Girl 54 60.0% 62 60.8% 0.912 X2

Boy 36 40.0% 40 39.2%
Side Right 19 21.1% 24 23.5% 0.492 X2

Left 42 46.7% 39 38.2%
Bilateral 29 32.2% 39 38.2%

Grade I 10 11.1% 1 1.0% 0.000 X2

II 27 30.0% 13 12.7%
III 27 30.0% 36 35.3%
IV 15 16.7% 31 30.4%
V 11 12.2% 21 20.6%

Neutrophil 5.19 ± 1.70 4.90 4.42 ± 1.98 4.40 0.002 m

Lymphocyte 3.71 ± 1.25 3.60 4.39 ± 1.71 3.80 0.020 m

NLR 1.59 ± 0.83 1.38 1.16 ± 0.70 0.99 0.000 m

MPV 6.28 ± 0.92 6.10 6.43 ± 1.04 6.30 0.395 m

m: Mann-whitney u test;  X2: Chi-square test; Statistically significant results are in bold italics (p < 0.05).
NLR: Neutrophil Lymphocyte Ratio; MPV: Mean Platelet Volume. 



Archivio Italiano di Urologia e Andrologia 2021; 93, 4

M. Demir, İ. Yağmur, E. Sabri Pelit, B. Katı, E. Ördek, H. Çiftçi

438

Neutrophil count, lymphocyte count and NLR did not dif-
fer significantly (p > 0.05) between scar-positive and scar-
negative patients with moderate (grade III) VUR (Table 4).
The lymphocyte count was significantly higher (p < 0.05)
and the neutrophil count and NLR were significantly lower
(p < 0.05) in scar-positive patients with high-grade (grades
IV-V) VUR than in scar-negative patients (Table 4).

DISCUSSION
VUR increases the risk of renal scarring by establishing a
ground for UTI and pyelonephritis. If the necessary pre-
cautions are not taken and the condition is not treated in a
timely manner, VUR causes reflux nephropathy and CRF
develops in 25%-60% of these patients (15). The reflux of
the infected urine back to the kidney does not always cause
parenchymal damage and renal scar in VUR (16). It has
been shown that the inflammatory process is more influ-
ential than the direct damage caused by bacterial infection
in renal scar development after pyelonephritis (17, 18). It
has been suggested that even if the infection is treated and
VUR is corrected, the inflammatory process that has
already started continues and therefore scar may develop
(1, 15). Partial benefits of the use of corticosteroids com-

bined with antibiotic therapy have been
observed in animal studies based on the
hypothesis that the development of renal
scarring can be reduced by preventing the
inflammatory process (19). In a recent dou-
ble-blind, placebo-controlled study con-
ducted by Shaikh et al., patients who were
treated for UTI were divided into two
groups. One group received antibiotics and
placebo, while the other group received
antibiotics and corticosteroids. The devel-
opment of the renal scar was found to be
lower in the group in which corticosteroids
were added to the treatment although the
difference was not statistically significant
(20). Based on the results of the study, it
was argued that better results could be
achieved by adding corticosteroids to the

treatment of patients predicted to develop pyelonephritis
and renal scarring. Urinary inflammatory biomarkers such
as TGF-b1, VEGF, and MCP-1 (15), Interleukin-18 (IL-18)
are known to play a role in renal ischemia-reperfusion and
acute kidney injury, and procalcitonin (PCT) and CRP
serum inflammation markers have proven to be reliable in
VUR patients (21). However, an easy-to-reach biomarker
predicting renal scar is still not available.
The NLR is a simple, useful parameter that is used as a
systemic inflammation marker. It has been widely
employed to predict the outcomes of oncological, cardio-
vascular, gastrointestinal and hematogenous infections
(22). It has been proposed as a marker of infection in
patients with sepsis and has been reported to be associat-
ed with the severity of the disease (23). In the study per-
formed by Terradas et al., increased mortality was demon-
strated in patients with bacteraemia who had an NLR of
> 7 (24). In another study, it has been reported that the
risk of sepsis increased after percutaneous nephrolithoto-
my in patients with an NLR of ≥ 2.5 (25).
Based on the data from literature, we hypothesised that
there might be a relationship between renal scarring and
complete blood count parameters. Hence, we analysed
the complete blood count parameters of patients diag-
nosed with VUR. The NLR was 0.99 (1.16 ± 0.7) in the
group with renal scarring and 1.38 (1.59 ± 0.83) in the

Figure 1. 
The relationship between NLR and renal scarring.

Table 4. 
Comparison of patients with and without renal scarring
according to the grade of reflux.

Scar (-) Scar (+) P
Mean ± sd/n-% Median  Mean ± sd/n-% Median 

Grade I-II Neutrophil 4.95 ± 1.55 4.80 4.38 ± 2.73 3.30 0.038 m

Lymphocyte 3.59 ± 1.25 3.30 3.28 ± 0.71 3.10 0.619 m

NLR 1.53 ± 0.66 1.41 1.45 ± 1.05 0.97 0.202 m

MPV 6.19 ± 0.89 6.10 6.36 ± 0.94 6.40 0.398 m

Grade III Neutrophil 5.39 ± 1.49 5.20 4.79 ± 1.91 4.75 0.173 m

Lymphocyte 3.78 ± 1.35 3.90 4.08 ± 1.61 3.50 0.835 m

NLR 1.71 ± 0.98 1.45 1.36 ± 0.71 1.45 0.285 m

MPV 6.42 ± 1.04 6.40 6.40 ± 0.96 6.30 0.867 m

Grade IV-V Neutrophil 5.32 ± 2.08 4.90 4.18 ± 1.79 3.95 0.020 m

Lymphocyte 3.82 ± 1.18 3.60 4.91 ± 1.79 4.50 0.016 m

NLR 1.57 ± 0.89 1.31 0.96 ± 0.52 0.83 0.001 m

MPV 6.26 ± 0.84 6.10 6.48 ± 1.13 6.25 0.652 m

m: Mann-whitney u test; Statistically significant results are in bold italics (p < 0.05).
NLR: Neutrophil Lymphocyte Ratio; MPV: Mean Platelet Volume. 

Table 3. 
Comparison of patients according to the grade of reflux.

Grade I-II Grade III Grade IV-V P
Mean ± sd/n-% Median  Mean ± sd/n-% Median Mean ± sd/n-% Median

Age 7.50 ± 7.14 7.00 5.14 ± 3.71 5.00 4.23 ± 3.67 4.00 0.005 K

Gender Girl 40 78.4% 39 61.9% 37 47.4% 0.002 X2

Boy 11 21.6% 24 38.1% 41 52.6%
Side Right 12 23.5% 15 23.8% 16 20.5% 0.124 X2

Left 28 54.9% 25 39.7% 28 35.9%
Bilateral 11 21.6% 23 36.5% 34 43.6%

Neutrophil 4.79 ± 1.93 4.50 5.05 ± 1.75 5.10 4.56 ± 1.95 4.45 0.146 K

Lymphocyte 3.51 ± 1.13 3.10 3.95 ± 1.50 3.60 4.55 ± 1.69 4.20 0.001 K

NLR 1.51 ± 0.78 1.28 1.51 ± 0.84 1.45 1.16 ± 0.72 1.01 0.004 K

MPV 6.23 ± 0.90 6.10 6.41 ± 0.99 6.30 6.40 ± 1.04 6.15 0.540 K

K: Kruskal-wallis (Mann-whitney u test);  X2: Chi-square test; Statistically significant results are in bold italics (p < 0.05).
NLR: Neutrophil Lymphocyte Ratio; MPV: Mean Platelet Volume. 



439Archivio Italiano di Urologia e Andrologia 2021; 93, 4

Renal scarring and neutrophil-to-lymphocyte ratio

group without renal scarring. We found that NLR was
low in patients with renal scars (Figure 1), and a rela-
tionship was discerned between the grade of reflux and
NLR (Figure 2). Therefore, we considered that NLR can
be used to predict renal scarring.
Risk factors precipitating the development of renal scar-
ring have been identified in patients with VUR (26). One
of these factors is the severity of the reflux. The risk of
renal scar developing after pyelonephritis increases with
the severity of VUR (27, 28). In a study involving 303
children with UTI who were under 2 years of age,
Stokland et al. showed that the risk of renal scarring was
elevated in Tc-99m DMSA scintigraphy in cases with
high-grade VUR (29). In the carried out by Bandari et al.,
the rates of renal scarring were 33%, 33%, 40%, 50% and
80% in patients with grade I, II, III, IV and V VUR,
respectively (30). Similarly, Jaukovic et al. found renal
scars in 26% of the children with low-grade VUR and in
56% of the children with high-grade VUR (31). 
In our study, the renal scar rates were 9%, 32.5%, 57.1%,
67.3% and 65.6% in patients with grade I, II, III, IV and V
VUR, respectively. As seen in VUR studies in the literature
and in the present study, the rate of scarring increased as
the grade of reflux increased (Figure 3). However, not all
patients with high-grade reflux develop renal scarring and
those with low-grade reflux can also develop renal scars

since the inflammatory process and immune response
progress differently in each patient (17, 32). In the sub-
data analysis of our study, the lymphocyte count was sig-
nificantly higher (p < 0.05) and the neutrophil count and
NLR were significantly lower (p < 0.05) in patients with
renal scarring who had high-grade (grades IV-V) reflux
than in those without renal scarring. We identified a rela-
tionship between renal scarring and NLR in patients with
high-grade (grades IV-V) VUR. Although our study did not
establish this relationship in the low and moderate (grades
I, II and III) reflux groups, we think that NLR could be the
reason why some patients develop renal scarring while oth-
ers with a similar grade of VUR do not.
Currently, requesting DMSA scintigraphy and performing
VCUG for those with DMSA uptake are recommended as a
Top-Down approach in the first-line workup after febrile
UTI (13). VUR occurs in 24%-39% of patients with acute
pyelonephritis detected by DMSA scintigraphy (33). 
In a systematic review by Shaikh et al., DMSA changes were
found in the acute phase in 57% of the patients after the
first UTI episode and these changes were observed in 15%
of the patients during follow-up (32). Therefore, repeat
DMSA imaging 6-12 months later is recommended to
determine the long-term outcomes in patients with signs of
acute pyelonephritis (34). However, DMSA screening in
children is impractical and expensive (20). In addition,
DMSA between the ages of 1-3 has disadvantages such as
the need for sedation during scintigraphy (35) and irradia-
tion (36). Therefore, we think that NLR can be used as a
parameter in predicting renal scarring and that DMSA
scintigraphy can reduce the number of shots.

Limitations
Our study has some limitations. The first limitation is the
retrospective study design. Since the number of febrile
UTI episodes in the study patients and whether they
received an effective therapy are unknown, these data
were not included in the study. Similarly, because we are
a tertiary health centre, patients are referred from exter-
nal centres. Therefore, most of the patients do not have
complete blood count data for the acute period. 
Therefore, infection parameters pertaining to the acute
infection period were not included in the study. We think
that the relationship between the complete blood param-
eters at the time of acute infection and renal scar forma-
tion should be examined with prospective studies.

CONCLUSIONS
We opine that NLR can be used as a parameter to predict
renal scarring in patients with VUR and may even be a
guiding marker candidate for treatment selection. In
addition, we anticipate that the number of DMSA scans,
which are costly and relatively difficult to implement, can
be reduced in this manner. However, these findings need
to be confirmed by well-designed prospective studies.

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Figure 3. 
The relationship between the grade of reflux and renal scarring.

Figure 2. 
Relationship between the grade of VUR and NLR.



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Correspondence
Mehmet Demir, MD (Corresponding Author)
drdemir02@gmail.com
Ismail Yagmur, MD 
dr_iyagmur@hotmail.com
Eyyup Sabri Pelit, MD 
dreyyupsabri@hotmail.com
Bülent Katı, MD 
bulentkati@yahoo.com
Eser Ördek, MD 
dr_eseser@hotmail.com
Halil Çiftçi, MD 
halilciftci63@hotmail.com
Harran University. Faculty of Medicine Urology Department 
Sanliurfa (Turkey)