Risk factors and nomogram for predicting urinary tract infection in patients with ureterolithiasis complicated with hydronephrosis
Original Article

Risk factors and nomogram for predicting urinary tract infection in patients with ureterolithiasis complicated with hydronephrosis

Qiao Qi1,2,3#, Yongtao Hu1,2,3#, Bingbing Hou1,2,3#, Kaiguo Xia1,2,3, Yuexian Xu1,2,3, Chaozhao Liang1,2,3, Zongyao Hao1,2,3

1Department of Urology, The First Affiliated Hospital of Anhui Medical University, Hefei, China; 2Institute of Urology, Anhui Medical University, Hefei, China; 3Anhui Province Key Laboratory of Urological and Andrological Diseases Research and Medical Transformation, Anhui Medical University, Hefei, China

Contributions: (I) Conception and design: Q Qi, Z Hao; (II) Administrative support: Q Qi, Y Hu; (III) Provision of study materials or patients: B Hou; (IV) Collection and assembly of data: Q Qi, K Xia; (V) Data analysis and interpretation: Y Xu; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

#These authors contributed equally to this work.

Correspondence to: Zongyao Hao, MD. Department of Urology, The First Affiliated Hospital of Anhui Medical University, 218th Jixi Road, Hefei 230022, China; Institute of Urology, Anhui Medical University, Hefei, China; Anhui Province Key Laboratory of Urological and Andrological Diseases Research and Medical Transformation, Anhui Medical University, Hefei, China. Email: haozongyao@163.com.

Background: Urinary tract infection (UTI) is a common disease in urology and often occurs in patients with urolithiasis. This study aimed to identify the risk factors for UTI in patients with ureterolithiasis complicated with hydronephrosis, and to construct a simple and practical nomogram to predict the incidence of UTI for patients.

Methods: A total of 383 patients were enrolled from September 2019 to June 2022. The results from univariate and multivariate logistic regression showed the risk factors for predicting UTI and a prediction model was constructed. Subsequently, the differentiation, calibration, and clinical applicability of the model were estimated by receiver operating characteristic (ROC) curve analysis, calibration curve, and decision curve analysis (DCA), respectively.

Results: The study included 72 (18.80%) patients with UTI. Multivariate logistic regression showed that tissue rim sign (P=0.04), positive urinary nitrite (P<0.001), and positive urinary leukocyte esterase (P=0.005) were independent predictive indexes of UTI for patients with ureterolithiasis complicated with hydronephrosis, and a nomogram was constructed in accordance with these indicators. The area under the ROC curve was 0.773, which indicated good prediction ability. The Hosmer-Lemeshow test (P=0.97) indicated that the model fitted well. The calibration curve and DCA showed good consistency and clinical applicability, respectively.

Conclusions: The prediction model constructed with the risk factors including tissue rim sign, positive urinary nitrite, and positive urinary leukocyte esterase can better detect patients with UTI early and take timely intervention measures.

Keywords: Urolithiasis; urine culture; nomogram; urinary tract infection (UTI)

Submitted May 05, 2024. Accepted for publication Sep 08, 2024. Published online Sep 26, 2024.

doi: 10.21037/tau-24-217

Highlight box

Key findings

• This study constructed a simple and practical nomogram to predict the incidence of urinary tract infection (UTI) early in patients with ureterolithiasis complicated with hydronephrosis.

What is known and what is new?

• There are few studies predicting the risk of preoperative UTI. Current prediction tools cannot meet clinical needs and have certain limitations.

• The study constructed a nomogram with the risk factors including tissue rim sign, positive urinary nitrite, and positive urinary leukocyte esterase, which has superior discrimination, excellent calibration abilities, and great clinical benefit.

What is the implication, and what should change now?

• The establishment of the new nomogram was helpful for clinicians to predict the risk of UTI in patients with ureteral calculi complicated with hydronephrosis, and to prevent the disease from further progressing to urosepsis.

Introduction

Urolithiasis is a widespread disease in urology, accounting for more than 1.2 million emergency department visits each year (1). Patients with ureteral calculi often have upper urinary tract obstruction, which is characterized by rapid onset, rapid progression, and severe symptoms (2,3). If not treated in time, these patients’ conditions can deteriorate further, which may progress to urosepsis, disseminated intravascular coagulation (DIC) and so on, and may even lead to death in severe cases (4,5). Based on available epidemiological surveys, severe sepsis or septic shock can lead to a mortality rate of 22–76% (6). Considering that hydronephrosis is an important manifestation of upper urinary tract obstruction, early recognition of urinary tract infection (UTI) in patients with ureteral calculi complicated with hydronephrosis would facilitate clinical decision-making and reduce mortality. In addition, given the overuse and drug resistance of antibiotics in clinical practice, timely identification of UTIs in these patients is particularly necessary.

Given that it takes at least 48 hours for the results of urine culture to be available, the diagnosis of UTI remains challenging. Currently, clinicians mainly make preliminary judgments based on their own subjective judgment and laboratory examination. Although many studies have found that several indicators can be used for the diagnosis of UTI (7-11), most of them focus on the analysis of UTI after ureteroscopic lithotripsy, and in patients with ureterolithiasis complicated with hydronephrosis, there are relatively few articles predicting the risk of preoperative UTI. Meanwhile, studies have shown that the start time of antibiotic use is closely related to the prognosis of patients (12-14). The mortality rate continues to increase with delayed use of antibiotics. Therefore, the purpose of this research is to develop a nomogram of UTI in patients with ureteral calculi complicated with hydronephrosis to optimize the early diagnosis and clinical decision-making of clinicians. We present this article in accordance with the TRIPOD reporting checklist (available at https://tau.amegroups.com/article/view/10.21037/tau-24-217/rc).

Methods

Study population

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This study was approved by the Ethics Committee of The First Affiliated Hospital of Anhui Medical University (No. PJ-2023-12-40). Individual consent for this retrospective analysis was waived. From September 2019 to June 2022, a total of 383 participants were enrolled in our retrospective research, including 72 participants with positive urine culture and 311 participants with negative urine culture. The inclusion criteria were composed of the following conditions: (I) at least 18 years old; (II) complete clinical data; and (III) ureteral calculi with hydronephrosis. The exclusion criteria were composed of the following conditions: (I) immunosuppressive diseases; (II) patients with abnormal kidney such as horseshoe kidney and transplanted kidney; (III) abnormal ureteral anatomy (such as duplication of ureter and congenital ureteral strictures); and (IV) infection with other systems.

Data collection

The collection of clinical data on patients included the following indicators: (I) demographic data, involving gender, age, body mass index (BMI), diabetes, hypertension, and history of urolithiasis surgery. (II) laboratory tests: (i) serological tests, involving neutrophil-lymphocyte ratio (NLR), lymphocyte-monocyte ratio (LMR), platelet-lymphocyte ratio (PLR), serum creatinine, etc. (ii) urine tests, including urinary leukocytes, urinary leukocyte esterase, urinary nitrite, urine culture, etc. (III) imaging examination, including the side, number (single/multiple) and maximum diameter of stones, the mean computed tomography (CT) value of hydronephrosis, perinephric fat stranding, periureteric fat stranding, and positive tissue rim sign.

We used the picture archiving and communication system (PACS) system of our hospital to measure the size of stones and the mean CT value of hydronephrosis. Urine came mainly from the bladder and was collected directly with self-urination. UTI was defined as a positive culture of middle clean urine samples (the count of isolated bacteria or fungi ≥105 colony forming unit/mL) excluding the bacteria that are not clinically relevant or indicate contamination (e.g., Lactobacillus crispatus and Gardnerella vaginalis) and at least one of the following symptoms should be included: dysuria, frequency, urgency, suprapubic pain, or fever (temperature >38 ℃). Perirenal and ureteral fat stranding were represented by increased fat density in the perirenal and periureteral spaces, respectively (15). Positive tissue rim sign referred to a decrease in annular soft tissue density [20–40 Hounsfield unit (HU)] due to edema in the ureteral wall around the stone (15).

Statistical analysis

Continuous variables were represented as mean ± standard deviation and compared by t-test or Mann-Whitney U test. Categorical variables were represented by count (percentage) and compared by Chi-squared test or Fisher’s exact test. Independent predictive indicators were screened out by multivariate logical regression analyses, and then the included factors were used by fitting the logistic regression model to predict UTI. The area under the curve (AUC) value was used to evaluate the accuracy of the prediction model. The higher the AUC value, the better the discrimination ability of the nomogram. An AUC value of 0.5–0.7 means that the accuracy of the model is low; an AUC value of 0.7–0.9 is acceptable; and an AUC value higher than 0.9 is excellent.

The differences between the predicted probabilities and the observed metrics were evaluated by calibration curves, while the Hosmer-Lemeshow test was utilized to verify the goodness of fit of the model. The bootstrap sample was repeated 1,000 times for internal verification. The clinical applicability of the model was evaluated by decision curve analysis (DCA).

Statistical analysis of the data was performed using SPSS (26.0) and R (4.3.1) software. P<0.05 for the two tails was considered statistically significant.

Results

Clinical characteristics of patients

In the research, 383 participants were involved, including 269 males and 114 females. The baseline data are presented in Table 1. The participants in this research were divided into UTI group and non-UTI group, including 72 (18.80%) participants with UTI. For the two groups, there were statistically significant differences in age, sex, BMI, diabetes, periureteric fat stranding, tissue rim sign, NLR, LMR, PLR, hemoglobin, blood albumin/globulin ratio, positive urinary white blood count (WBC), positive urinary protein, positive urinary nitrite, and positive urinary leucocyte esterase, and no significant differences in other indicators.

Table 1

Demographic and clinical data of the patients

Variables Total (n=383) UTI (n=72) Non-UTI (n=311) P value
Age (years) 49.00±14.19 55.04±14.97 47.60±13.65 <0.001*
Gender (male) 269 (70.23) 37 (51.39) 232 (74.60) <0.001*
BMI (kg/m2) 24.54±3.27 23.46±2.76 24.79±3.34 0.002*
Hypertension 121 (31.59) 26 (36.11) 95 (30.55) 0.36
Diabetes 46 (12.01) 14 (19.44) 32 (10.29) 0.03*
History of urolithiasis surgery 181 (47.26) 38 (52.78) 143 (45.98) 0.30
Preoperative stent 82 (21.41) 21 (29.17) 61 (19.61) 0.08
Affected side 0.46
   Left 142 (37.08) 23 (31.94) 119 (38.26)
   Right 163 (42.56) 31 (43.06) 132 (42.44)
   Both 78 (20.37) 18 (25.00) 60 (19.29)
Stone number 0.70
   Single 173 (45.17) 34 (47.22) 139 (44.69)
   Multiple 210 (54.83) 38 (52.78) 172 (55.31)
Stone location 0.75
   Ureteral 185 (48.30) 36 (50.00) 149 (47.91)
   Ureteral + renal 198 (51.70) 36 (50.00) 162 (52.09)
Stone diameter (mm) 9.25±4.11 8.96±4.36 9.31±4.06 0.52
Hydronephrosis 0.49
   Mild 277 (72.32) 48 (66.67) 229 (73.63)
   Moderate 79 (20.63) 18 (25.00) 61 (19.61)
   Severe 27 (7.05) 6 (8.33) 21 (6.75)
Mean HU of hydronephrosis 5.90±6.65 6.81±6.00 5.68±6.78 0.25
Perinephric fat stranding 64 (16.71) 17 (23.61) 47 (15.11) 0.08
Periureteral fat stranding 37 (9.66) 14 (19.44) 23 (7.40) 0.002
Tissue rim sign 62 (16.19) 24 (33.33) 38 (12.22) <0.001*
Blood WBC (109/L) 6.94±2.28 6.74±1.93 6.99±2.35 0.40
NLR 2.88±2.46 3.17±2.48 2.81±2.46 0.01*
LMR 4.71±1.91 4.17±1.89 4.84±1.90 0.007*
PLR 139.09±57.14 157.98±74.79 134.72±51.38 0.002*
Platelets (109/L) 232.86±65.21 235.43±70.70 232.27±63.97 0.72
Hb (g/L) 138.80±20.36 127.06±22.49 141.52±18.86 <0.001*
BUN (mmol/L) 5.81±2.51 6.06±2.61 5.76±2.49 0.36
Serum creatinine (μmol/L) 94.25±59.82 90.98±49.64 95.01±61.99 0.31
Blood albumin/globulin ratio 1.78±0.36 1.62±0.39 1.81±0.35 <0.001*
Positive urine WBC 243 (63.45) 62 (86.11) 181 (58.20) <0.001*
Positive urine protein 119 (31.07) 30 (41.67) 89 (28.62) 0.03*
Positive urine nitrite 35 (9.14) 25 (34.72) 10 (3.22) <0.001*
Positive urine leukocyte esterase 140 (36.55) 51 (70.83) 89 (28.62) <0.001*

Continuous variables were compared using mean ± standard deviation, and categorical variables using median (percentage). *, statistically significant. BMI, body mass index; HU, Hounsfield unit; WBC, white blood cell; NLR, neutrophil-lymphocyte ratio; LMR, lymphocyte-monocyte ratio; PLR, platelet-lymphocyte ratio; Hb, hemoglobin; BUN, blood urea nitrogen; UTI, urinary tract infection.

Logistic regression analysis and risk factors

For potential predictive indicators, meaningful variables from univariate logistic regression analysis were brought into the multivariate logistic regression. Ultimately, as shown in Table 2, multivariate logistic regression analysis identified tissue rim sign, positive urinary nitrite, and positive urinary leukocyte esterase as independent risk factors for UTI in patients with ureterolithiasis complicated with hydronephrosis.

Table 2

Univariate and multivariate logistic regression analysis of factors associated with UTI

Variables Univariate analysis Multivariate analysis
OR (95% CI) P value OR (95% CI) P value
Age (years) 1.04 (1.02–1.06) <0.001* 1.01 (0.99–1.03) 0.43
Gender (ref: female) 0.36 (0.21–0.61) <0.001* 1.22 (0.57–2.68) 0.61
BMI (kg/m2) 0.88 (0.81–0.95) 0.002* 0.91 (0.82–1.01) 0.08
Hypertension (ref: no) 1.29 (0.74–2.19) 0.36 – –
Diabetes (ref: no) 2.10 (1.03–4.13) 0.03* 1.50 (0.58–3.69) 0.39
History of urolithiasis surgery (ref: no) 1.31 (0.79–2.20) 0.30 – –
Preoperative stent (ref: no) 1.69 (0.93–2.99) 0.08 – –
Affected side (ref: left)
   Right 1.22 (0.67–2.22) 0.52 – –
   Both 1.55 (0.77–3.09) 0.21 – –
Stone number (ref: single) 0.90 (0.54–1.51) 0.70 – –
Stone location (ref: ureteral) 0.92 (0.55–1.54) 0.75 – –
Stone diameter (mm) 0.98 (0.92–1.04) 0.52 – –
Hydronephrosis (ref: mild)
   Moderate 1.41 (0.75–2.56) 0.27 – –
   Severe 1.36 (0.48–3.37) 0.53 – –
Mean HU of hydronephrosis 1.03 (0.99–1.07) 0.19 – –
Perinephric fat stranding (ref: no) 1.74 (0.91–3.20) 0.08 – –
Periureteral fat stranding (ref: no) 3.02 (1.44–6.17) 0.003* 2.43 (0.91–6.28) 0.07
Tissue rim sign (ref: no) 3.59 (1.97–6.50) <0.001* 2.25 (1.04–4.74) 0.04*
Blood WBC (109/L) 0.95 (0.84–1.07) 0.40 – –
NLR 1.05 (0.95–1.15) 0.27 – –
LMR 0.82 (0.71–0.95) 0.008* 0.98 (0.80–1.19) 0.83
PLR 1.01 (1.00–1.01) 0.003* 1.00 (1.00–1.01) 0.40
Hb (g/L) 0.97 (0.95–0.98) <0.001* 0.98 (0.97–1.00) 0.053
BUN (mmol/L) 1.04 (0.95–1.14) 0.36 – –
Serum creatinine (μmol/L) 1.00 (0.99–1.00) 0.61 – –
Blood albumin/globulin ratio 0.21 (0.09–0.45) <0.001* 0.98 (0.35–2.69) 0.98
Positive urine WBC 4.45 (2.29–9.53) <0.001* 1.87 (0.75–4.83) 0.19
Positive urine protein 1.78 (1.04–3.02) 0.03* 0.61 (0.29–1.24) 0.18
Positive urine nitrite 16.01 (7.43–36.99) <0.001* 5.98 (2.36–15.99) <0.001*
Positive urine leukocyte esterase 6.06 (3.49–10.84) <0.001* 3.18 (1.44–7.34) 0.005*

*, statistically significant. UTI, urinary tract infection; BMI, body mass index; HU, Hounsfield unit; WBC, white blood cell; NLR, neutrophil-lymphocyte ratio; LMR, lymphocyte-monocyte ratio; PLR, platelet-lymphocyte ratio; Hb, hemoglobin; BUN, blood urea nitrogen; OR, odds ratio; CI, confidence interval.

Construction and validation of the nomogram

In light of the consequences of multivariate logistic regression analysis, we established a predictive model that included all independent risk factors (Figure 1). As shown in Figure 2, we plotted the receiver operating characteristic (ROC) curves for the predicted probability to validate this nomogram. The area under the ROC curve of the prediction model was 0.773, which was superior to the application of individual risk factors, indicating better identification of the nomogram. The Hosmer-Lemeshow test did not show statistical significance (P>0.05), indicating a good fit for the nomogram. To prevent overfitting, the model was verified internally by bootstrapping with 1,000 repeated samples, and the value of the corrected C-index was 0.770, implying that this model had excellent repeatability. As shown in Figure 3, the calibration curve represented a good consistency between the observed and predicted values in this model.

Figure 1 Nomogram for predicting the probability of UTI in patients with ureterolithiasis complicated with hydronephrosis. UTI, urinary tract infection.
Figure 2 ROC curves of the prediction model compared with individual indicators. ROC, receiver operating characteristic.
Figure 3 The calibration curve of the prediction model. The red line represents the original performance and the blue line represents the performance during internal validation by bootstrapping (B =1,000).

Clinical usefulness of the model

DCA was established to evaluate the clinical applicability of the nomogram (Figure 4). The clinical practicality of combined indicators was significantly better than that of individual indicators. If the threshold is set to 0.08–0.84, using this model to predict the probability of UTI would increase the net benefit more than the “no intervention” or “all intervention” strategies.

Figure 4 Decision curve analysis for the nomogram and individual indicators. The y-axis measures the net benefit. The black line (None) represents the assumption of intervention-none. The gray line (All) represents the assumption of intervention-all-patients.

Discussion

Urolithiasis is a common disease in urology (16,17). Due to the presence of obstructive factors, UTI has become a common complication in patients with urinary stones (18). Considering the obvious urinary obstruction in patients with ureterolithiasis complicated with hydronephrosis, the main objective of this research was to construct a nomogram for the occurrence of UTI in the patients, aiming to assess the risk of developing UTI earlier and more accurately. This is also the first clinical retrospective study of patients with ureterolithiasis complicated with hydronephrosis. The results indicated that the model built with three indexes of tissue positive sign, positive urine nitrite, and positive urine leukocyte esterase had good predictive ability, which was conducive to early detection and decision-making by clinicians.

Since noncontrast helical CT was applied in patients with ureterolithiasis, secondary signs related to ureterolithiasis, such as perinephric fat stranding, periureteral fat stranding, and hydronephrosis, have shown relevant clinical significance (19-21). Positive tissue rim sign is defined as the attenuation of annular soft tissue (20–40 HU) due to edema of the ureteral wall around the stone (15). Tissue rim sign occurs frequently in patients with ureteral stones and is of great significance in distinguishing ureterolithiasis from phlebolith (22). Ahmed et al. found that perinephric fat stranding and tissue rim sign played important roles in the natural elimination of stones during conservative treatment (23). In addition, in retrospective research of 237 participants, Kim et al. identified that tissue rim sign was a predictor of stone clearance rate after ureteroscopic lithotripsy (24). In this study, we found that tissue rim sign [odd ratio (OR): 2.25, 95% confidence interval (CI): 1.04–4.74] was an independent predictive index of UTI for patients with ureterolithiasis complicated with hydronephrosis. Tissue rim sign is an imaging manifestation of inflammation and edema in the ureter. For the participants included in this research, with ureteral obstruction and significantly elevated renal pelvis pressure, the ureter was more prone to inflammation so that tissue rim sign could reflect the changes in peripheral inflammation caused by stone obstruction.

Positive urinary nitrite was another independent predictive index of UTI for patients with ureterolithiasis complicated with hydronephrosis. Since the relationship between positive urinary nitrite and UTI was first identified in 1914, plenty of studies have found the role of urinary nitrite in UTI (25-27). By propensity score matching, Ma et al. found that preoperative positive urinary nitrite may be significant in predicting fever after flexible ureteroscopy (28). In addition, an artificial neural network analysis involving 1,716 patients showed that urine nitrite positive was a crucial factor in the development of urosepsis for patients with upper urolithiasis (29). Although nitrite is generally absent in the urine, parts of the bacteria in urine, such as Escherichia coli, have the ability to convert nitrate to nitrite. This may explain to some extent that positive urine nitrite can be one of the predictors of UTI.

In this study, urinary leukocyte esterase was an important predictive indicator for the occurrence of UTI. Urinary leukocyte esterase, which is mainly found in neutrophils, has been extensively studied as a biological marker of UTI (30-32). For example, in a retrospective cross-sectional study involving 20,000 children, Nadeem et al. revealed that positive urinary leukocyte esterase was an important risk factor for UTI, regardless of urinary concentration (33). This was consistent with our findings. Other biomarkers, such as xanthine oxidase and myeloperoxidase, which can enhance their own activity after the occurrence of UTI, seem to be good indicators for the diagnosis of UTI (34). However, due to the cost and feasibility, they have not been implemented in clinical practice. Therefore, in terms of predictive ability and clinical practicability, positive leukocyte esterase is currently a better indicator for predicting UTI.

This research had several shortcomings. First, this was a retrospective clinic research, which inevitably led to selection bias. Second, this was only a single-center study, and the sample size collected was relatively small, which might have influenced the efficiency of the nomogram to some extent. Third, this model has not yet been widely used in clinical practice. In the future, we will use this model in clinical practice and conduct subsequent reports. In addition, we will collect data to establish a nomogram for predicting urosepsis. Eventually, this research was verified internally without external verification. Therefore, a larger sample size and multicenter data are needed for validation.

Conclusions

In summary, tissue rim sign, positive urinary nitrite, and positive urine leukocyte esterase were independent risk factors for UTI in patients with ureterolithiasis complicated with hydronephrosis. We developed a model to predict the occurrence of UTI and avoid further progression of the disease through early intervention.

Acknowledgments

Funding: This work was supported by the National Natural Science Foundation of China (Nos. 82070724 and 82370768).

Footnote

Reporting Checklist: The authors have completed the TRIPOD reporting checklist. Available at https://tau.amegroups.com/article/view/10.21037/tau-24-217/rc

Data Sharing Statement: Available at https://tau.amegroups.com/article/view/10.21037/tau-24-217/dss

Peer Review File: Available at https://tau.amegroups.com/article/view/10.21037/tau-24-217/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tau.amegroups.com/article/view/10.21037/tau-24-217/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Ethics Committee of The First Affiliated Hospital of Anhui Medical University (No. PJ-2023-12-40). Individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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Cite this article as: Qi Q, Hu Y, Hou B, Xia K, Xu Y, Liang C, Hao Z. Risk factors and nomogram for predicting urinary tract infection in patients with ureterolithiasis complicated with hydronephrosis. Transl Androl Urol 2024;13(9):1946-1954. doi: 10.21037/tau-24-217

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