Prediction model for severe vesicoureteral reflux in children with urinary tract infection and/or hydronephrosis

doi:10.21203/rs.3.rs-4807449/v1

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Research Article

Prediction model for severe vesicoureteral reflux in children with urinary tract infection and/or hydronephrosis

https://doi.org/10.21203/rs.3.rs-4807449/v1

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Background

As voiding cystourethrography is invasive and carries the risks of radiation and urinary tract infection, identifying only high-grade reflux is important. We aimed to identify risk factors for severe reflux in children presenting with urinary tract infections and/or urinary tract dilatation and to develop a prediction model for severe reflux.

Methods

Data of the children who underwent voiding cystourethrography due to urinary tract infections and/or urinary tract dilatation were retrospectively analyzed for demographic, clinical and imaging findings. Patients with severe (grades 4–5) reflux were compared with the rest for these parameters and a prediction model was developed for severe reflux.

Results

The study included 1044 patients (574 female). Severe reflux was present in 86 (8.2%) patients. Non-E. coli uropathogens, hydronephrosis, UTD-P3 dilatation, multiple renal scar, and decreased renal function on DMSA scintigraphy were associated with severe reflux. The prediction model by using these variables for severe reflux with a score ranging from 0–6 and an accuracy rate of 93.4% was developed. A score of ≥ 4 had a sensitivity 48.8%, specificity 95.8%, PPV 51.2%, and NPV 95.4% for severe reflux. Patients with ≥ 4 score were 21.9 times more likely to have severe reflux.

Conclusion

Non-E. coli uropathogen growth, the presence of hydronephrosis and especially UTD-P3 dilatation on ultrasonography, presence of multiple scars and decreased relative function on DMSA scintigraphy were found to be independent risk factors for severe reflux. Our scoring system based on these variables appears to be effective in predicting the presence of severe VUR.

Severe vesicoureteral reflux

voiding cystourethrography

urinary tract infection

non-E.coli uropathogen

renal scar

prediction model

Vesicoureteral reflux (VUR) is an anatomical and functional disorder characterized by the abnormal backward flow of urine from the bladder into the ureters and renal pelvis. It poses a risk of causing serious complications such as end-stage kidney disease (ESKD) due to recurrent urinary tract infections (UTIs), and the prevention of renal damage forms the basis of treatment [1]. Historically, the detection of all VUR cases was recommended to prevent chronic kidney disease, hypertension, and ESKD caused by UTIs. However, the use of voiding cystourethrography (VCUG) for diagnosing VUR carries risks of radiation exposure, iatrogenic UTIs, and requires urethral catheterization [2]. On the other hand, recent publications report that ESRD caused by reflux nephropathy is extremely rare (< 0.0005%) [3]. Most cases of primary VUR are low grade and have a low likelihood of being associated with acquired renal scarring [1, 2]. Conversely, children diagnosed with high-grade VUR are at the greatest risk for UTIs and renal scarring during infancy [3]. Therefore, identifying high-grade VUR has gained importance, and VCUG should be requested only in selected patients.

In this study, we aimed to identify risk factors for severe VUR (grades 4–5) in children presenting with UTIs and/or urinary tract dilatation and to develop a prediction model for severe VUR.

Patients:

Data from 1044 patients who underwent VCUG due to UTI and/or urinary tract dilatation at Dokuz Eylul University Pediatric Nephrology Clinic between 2010 and 2020 were retrospectively analyzed.

This study was conducted with the approval of the Non-Interventional Ethics Committee of Dokuz Eylul University School of Medicine, under the code 2023/23 − 13.

Methods:

The files of the patients were evaluated for age, gender, presence of UTI, causative microorganism, urinary system ultrasonography (USG), Tc-99m dimercaptosuccinic acid (DMSA) renal scintigraphy and VCUG results retrospectively.

Urinary Tract Infections

UTI was defined as growth of a single microorganism over 100,000 col/mL in association with fever and/or specific symptoms related to UTIs. Recurrent UTI was defined as two or more episodes of UTI. Uropathogens were grouped as E. coli and non-E. coli.

Ultrasonography

All patients underwent urinary system USG. USG results were classified as normal vs abnormal (dilatation, abnormal parenchyma, calculi), presence vs absence of hydronephrosis (HN), and the degree of HN. The degree of HN was determined according to the international urinary tract dilatation system as UTD-P 1–3 [4].

VCUG

VUR was classified according to the criteria of the International Reflux Study Group [5]. In patients with bilateral reflux, the highest degree of VUR was recorded. Grades 4–5 were defined as severe VUR.

Tc-99m DMSA Scintigraphy

Imaging results were evaluated in terms of the presence of scarring, multiple scars, and decreased renal function. Kidneys with cortical renal defects and/or irregular margins were considered to have scarring. Decreased renal function was defined as relative uptake less than 45% [6].

Statistical Analyses:

Risk factors associated with severe VUR were identified using the chi-square test. After that, univariate logistic regression analysis was used to exclude non-significant parameters. We developed a severe VUR prediction model by multivariate logistic regression analysis using a stepwise forward likelihood ratio selection method. We used the coefficients [Exp(B)] from the regression analysis for the severe VUR prediction model. To determine cut-off scores and evaluate the accuracy of the model, ROC (Receiver Operating Characteristic) analysis was performed. Cut-off scores were calculated using sensitivity, specificity values, and Youden's Index. The area under curve (AUC) was provided with 95% confidence intervals (CI). A p-value of less than 0.05 was considered statistically significant. All statistical analyses were conducted using SPSS version 29.

Between 2010 and 2020, a total of 1044 patients who underwent VCUG and met our study criteria were included, comprising 574 (55.0%) females and 470 (45.0%) males. The mean age of the patients at the time of VCUG was 29.0 ± 35.1 months (median 12, range 0-167 months).

Severe VUR was present in only 86 (8.2%) patients in our study population. Patients with severe VUR were compared in terms of demographic and clinical characteristics with the patients with no/mild VUR, as presented in Table 1. Patients with severe VUR were more commonly male and younger than the others. A history of UTIs and the number of UTIs were not associated with the frequency of severe VUR; however, the presence of non-E. coli uropathogens in culture was associated with severe VUR. Pathological USG findings, HN, and particularly UTD-P3 HN were more frequently observed in children with severe VUR. DMSA scintigraphy was performed on 507 patients. The presence of scarring, multiple scars, and decreased renal function on DMSA was also more common in children with severe VUR.

Table 1

Comparison of the children with severe vesicoureteral reflux (VUR) and those with no/mild VUR.
Parameters	Children who underwent VCUG (n = 1044)		p*
Parameters	No/mild VUR (n = 958)	Severe VUR (n = 86)	p*
Age	29.9±35.5	19.1±27.6	< 0.001
Male, n (%)	416 (43.4)	54 (62.8)	< 0.001
UTI, n (%)	559 (58.3)	58 (67.4)	0.100
Recurrent UTIs, n (%)	354 (36.9)	35 (40.7)	0.117
Non-E.Coli, n (%)	206 (21.5)	32 (37.2)	0.006
Abnormal USG, n (%)	650 (67.8)	73 (84.9)	0.001
Hydronephrosis, n (%)	439 (45.8)	68 (79.1)	< 0.001
UTD-P3 hydronephrosis, n (%)	138 (14.4)	43 (50.0)	< 0.001
Scaring, n (%)	242 (25.3)	56 (65.1)	< 0.001
Multiple scaring, n (%)	147 (15.3)	50 (58.1)	< 0.001
Decreased function, n (%)	158 (16.5)	54 (62.8)	< 0.001
USG: Ultrasonography, UTD: Urinary tract dilatation, UTI: Urinary tract infection, VCUG: Voiding cystourethrography, chi square*

Univariate and multivariate regression analyses for factors associated with severe VUR are shown in Table 2. Independent risk factors for severe VUR were found to be the presence of non-E. coli uropathogens in culture, HN and UTD-P3 HN in USG, multiple scars and decreased renal function on DMSA. However, gender, presence of any pathological USG finding and the presence of any scarring on DMSA were not associated with severe VUR.

Table 2

Univariate and multivariate regression analysis for factors independently associated with severe vesicoureteral reflux.
	Severe (grade 4–5) VUR
	No (n = 958) n (%)	Yes (n = 86) n (%)	p4	p5	Exp(B)6	Coefficient
Male gender	416 (43.4)	54 (62.8)	0.060
Non-E.Coli uropathogen	206 (21.5)	32 (37.2)	< 0.001	< 0.001	3.690	1
Abnormal ultrasonography1	650 (67.8)	73 (84.9)	0.470
Hydronephrosis	439 (45.8)	68 (79.1)	< 0.001	< 0.001	2.709	1
UTD-P32 hydronephrosis	138 (14.4)	43 (50.0)	< 0.001	< 0.001	5.635	2
Scar on DMSA3	242 (25.3)	56 (65.1)	0.209
Multiple scar	147 (15.3)	50 (58.1)	< 0.001	< 0.001	2.679	1
Decreased renal function	158 (16.5)	54 (62.8)	< 0.001	< 0.001	2.792	1
Total						6
1 Urinary tract dilatation, parenchymal pathology, urolithiasis; 2 Urinary tract dilatation system; 3 99mTc-dimercaptosuccinic acid scintigraphy; 4 Univariate regression analysis; 5 Multivariate regression analysis; 6 Exp(B): Regression coefficient.

A prediction model for severe VUR was developed using multivariate logistic regression analysis. Each independent risk factor was approximately weighted according to the regression coefficients [Exp(B)] and assigned scores of 1 or 2 (Table 2). Based on these coefficients, the calculated scores ranged from a minimum of 0 to a maximum of 6 with an accuracy rate of 93.4% in predicting severe VUR. The observed rates of severe VUR according to the patients' scores are presented in Table 3. The area under the curve (AUC) from the ROC analysis was found to be 0.898, with a 95% confidence interval (CI) ranging from 0.870 to 0.925 (Fig. 1). Cut-off scores calculated using Youden’s Index were determined as follows: low risk: 0–1; moderate risk: 2–3; high risk: 4–6. In the low risk group, severe VUR was quite rare (0.3%), while in the moderate risk group, this rate was 13.0%, and in the high risk group, the presence of severe VUR was 51.2%. The difference between these groups was significant (Table 4). Among the 862 patients with a score ≤ 3, 44 (5.1%) had severe VUR, whereas among the 82 patients with a score ≥ 4, 42 (51.2%) had severe VUR. According to these parameters, a score ≥ 4 had a sensitivity 48.8%, specificity 95.8%, positive predictive value (PPV) 51.2%, and negative predictive value (NPV) 95.4% for severe VUR. Patients with a score ≥ 4 were 21.9 (95% CI: 12.9–37.2) times more likely to have severe VUR compared to those with a score ≤ 3 (Table 5). Additionally, none of the patients with a score 0 had severe VUR, and the rate of severe VUR among those with a score 1 was 0.5%. In contrast, among patients with a score 5 or 6, 73.3% had severe VUR.

Table 3

Patient’s scores and severe (grade 4–5) vesicoureteral reflux (VUR) rates according to the “severe VUR prediction model”.
Total score	Number of patients		Severe VUR %
	Severe VUR (-)	Severe VUR (+)
6	-	3	100
5	8	19	70.4
4	32	20	38.5
3	132	25	15.9
2	150	17	10.2
1	362	2	0.5
0	274	-	0

Table 4

Comparison of low, moderate and high risk patients for the presence of severe vesicoureteral reflux.
Cut-off scores	Severe (grades 4–5) VUR		p
	Absent n (%)	Present n (%)
Low risk (0–1)	636 (97.7)	2 (0.3)	< 0.001
Medium risk (2–3)	282 (87.0)	42 (13.0)
High risk (4–6)	40 (48.8)	42 (51.2)

Table 5

Predictive power of our model for severe (grades 4–5) vesicoureteral reflux
Cut-off scores	Diagnostic performance
	Sensitivity	Specificity (%)	PPV (%)	NPV (%)	Odds ratio
High risk (4–6)	48.8	95.8	51.2	95.4	21.9 (12.9–37.1)
Moderate risk (2–3)	48.8	70.6	13.0	93.	2.3 (1.5–3.6)
Low risk (0–1)	2.3	33.6	0.3	79.3	1.2 (0.3–0.5)
PPV: Positive predictive value, NPV: Negative predictive value

DMSA scintigraphy was not performed in 537 patients. Thus, prediction model in those patients is based on a maximum score of 4. When we evaluated these patients separately, only 18 (3.3%) had severe VUR and half of them (9 patients) had a score 4. The rate of severe VUR among children with a score 4 was 27.3% (9/33), while it was only 1.8% (9/504) in children with a score ≤ 3 (p < 0.001). Sensitivity, specificity, PPV, NPV and OR of score 4 for predicting severe VUR were 50.0%, 95.4%, 27.3%, 98.3% and 20.0, respectively.

Many guidelines published on the management of UTIs in children have narrowed the indications for VCUG, emphasizing that it should be performed only in selected patients [7–10]. Numerous studies have shown that a history of UTI in children is associated with high-grade VUR [11–14]. Contrary to the literature, our study did not find an association between a history of UTIs or the number of UTIs and the frequency of severe VUR. However, the frequency of severe VUR was higher in patients with non-E. coli uropathogens (Tables 1 and 2). Similarly, a study examining 738 patients aged 0–24 months with a history of UTIs found a higher rate of VUR in those with non-E. coli uropathogens compared to those with E. coli [15]. Another retrospective study reported that the presence of non-E. coli uropathogens in cultures was the only significant predictor of severe VUR [13]. Therefore, it is more important to perform VCUG in patients with non-E. coli UTIs rather than in all patients with a history of UTIs. This approach is consistent with many current guidelines [9, 16, 17].

The selection of imaging tests following UTIs in children remains a contentious issue. Many clinical guidelines recommend performing USG for all patients after a UTI [9, 18, 19]. However, USG results are normal in over 80% of cases, leading to significant time and cost inefficiencies [20–22]. Despite the limited sensitivity of USG in detecting VUR, most clinical guidelines recommend VCUG for abnormalities detected on USG [21, 23]. Nonetheless, numerous studies have shown that USG alone is insufficient for diagnosing VUR [11, 24–29]. In our study, regression analysis revealed that the presence of any abnormality on USG was not associated with the frequency of severe VUR. This indicates that USG has a low predictive ability for severe reflux. However, the presence of HN, particularly UTD-P3 HN, on USG was associated with an increased frequency of severe VUR (Tables 1 and 2).

The approach of performing DMSA imaging first and then VCUG after a febrile UTI is known as the "top-down approach." The top-down approach assumes that clinically significant VUR will have associated changes on DMSA scan and that VUR is clinically insignificant in patients with normal DMSA scans [30]. In a prospective study evaluating the top-down approach, 85% of patients with abnormal DMSA had high-grade VUR [31]. A Cochrane review found that children with negative DMSA scans had less than 1% chance of having high-grade VUR [32]. Similarly, various studies have shown that children with severe VUR are more likely to develop renal scarring [25, 33]. In our study, the presence of multiple scars and decreased function on DMSA was associated with an increased frequency of severe reflux (Tables 1 and 2).

In a study using data from 324 children aged 2–60 months with a history of febrile UTI, a scoring system was developed, and independent risk factors for high-grade VUR were identified as recurrent UTIs, non-E. coli pathogens, and abnormal USG findings [34]. Similarly, in our model, the presence of non-E. coli uropathogens was a risk factor for severe VUR. However, instead of any abnormal USG findings, the presence of HN and specifically UTD-P3 HN were found to be significant. Additionally, multiple scars and decreased function on DMSA were also independent risk factors for severe VUR (Table 2).

In our model, the total score ranges from 0 to 6. The cut-off scores were determined as follows: low risk 0–1, moderate risk 2–3, high risk 4–6. Given that a score ≥ 4 has very high specificity for severe VUR, it may be considered to avoid performing VCUG in patients with lower scores.

Guidelines established by major institutions such as the American Academy of Pediatrics and the National Institute for Healthcare and Excellence have significantly reduced the number of unnecessary VCUGs [7, 35]. However, these guidelines have also led to delays in the diagnosis and treatment of some children with VUR. Various studies reviewing these guidelines have shown that most of the missed cases involve children with low grade VUR. Even if children with low grade VUR are not diagnosed after the first UTI, the impact on patients is minimal because antimicrobial prophylaxis is not routinely recommended for these children [16, 17, 36, 37]. The key is not to diagnose every case of VUR but to identify and treat other risk factors for UTIs, such as bladder and bowel dysfunction [38, 39].

According to our prediction model for severe VUR, patients in the low risk group (score 0–1) constituted 61% of all patients, and the rate of severe VUR in this group was 0.3%. Therefore, VCUG should not be performed in patients within the low risk group. In the moderate-risk group (score 2–3), although the frequency of severe VUR was only 14.9%, half of all severe VUR cases (42/86) were in this group. Thus, the decision to perform VCUG in this group should be carefully evaluated by clinicians. In the high risk group (score 4–6), the rate of severe VUR was 51.2%. Clinicians should not hesitate to request VCUG for patients in this high risk group. Although some cases of VUR might be missed with our model, high grade VUR cases will be detected, and unnecessary VCUGs for patients without VUR or with clinically insignificant VUR will be avoided.

Limitations of our study include retrospective design which might have precluded the fully differentiation between cystitis and pyelonephritis due to incomplete clinical and laboratory data on the patient files. In addition, information on the method of urine culture collection was not available in most patient records, so instances of growth below 100.000 colonies in samples obtained by urinary catheterization may have been missed. Furthermore, approximately half of the patients included in the study underwent DMSA imaging. Patients without a DMSA scan could achieve a maximum score 4. However, evaluation of children without DMSA scintigraphy also showed that probability of severe VUR is 20 times higher in those with a score 4 than the children with a score 0 to 3.

Non-E. coli uropathogen growth, the presence of hydronephrosis and especially UTD-P3 dilatation on USG, presence of multiple scars and decreased relative function on DMSA scintigraphy were found to be independent risk factors for severe VUR. Our predicting model of severe VUR based on these variables appears to be effective.

Conflict of interest:

The authors have declared that no conflict of interest exists.

Funding:

The authors did not receive support from any organization for the submitted work.

Author’s contribution

The study was planned and designed by Pelin Laleoglu, Salih Kavukcu. Data analysis was conducted by Pelin Laleoglu, Gizem Yıldız, Meral Torun Bayram, Alper Soylu, Handan Guleryuz Ucar. The manuscript was written by Pelin Laleoglu, Alper Soylu. All 6 authors contributed to the data and commented on the manuscript.

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Editorial decision: Major Revisions Needed
20 Aug, 2024
Reviewers agreed at journal
29 Jul, 2024
Reviewers invited by journal
26 Jul, 2024
Editor assigned by journal
26 Jul, 2024
First submitted to journal
26 Jul, 2024

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Prediction model for severe vesicoureteral reflux in children with urinary tract infection and/or hydronephrosis

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