Risk Factors of Urinary Tract Infection After Ureteral Stenting in Patients with Renal Colic During Pregnancy

Abstract

Introduction:

To investigate risk factors associated with urinary tract infection (UTI), following ureteral stenting, for patients with renal colic during pregnancy.

Patients and Methods:

Patients with renal colic during pregnancy who underwent ureteral stenting in The First Affiliated Hospital of Guangzhou Medical University between 2009 and 2019 were examined retrospectively. Ureteral stenting patients who had UTIs after hospital discharge and before delivery were classified as the infected group. Multivariate logistic regression analysis was used to assess the risk factors associated with UTI after ureteral stenting.

Results:

A total of 102 patients were enrolled into the study. Mean age was 30 years (interquartile range [IQR]: 26–33 years) and mean gestation age was 22 weeks (IQR: 18–28 weeks). UTI occurred in 21 patients (20.6%). Compared with noninfected patients, infected patients had a higher rate of positive urine culture (52.4% vs 13.6%, p = 0.000), kidney stones ≥10 mm (81% vs 35.8%, p = 0.000), residual stones after ureteral stenting (71.4% vs 43.2%, p = 0.021), and different surgical indications and gestational ages (18 vs 23 weeks, p = 0.00). Multifactor analysis showed that gestational age, positive urine culture (odds ratio [OR] = 6.233, 95% confidence interval [CI]: 1.830–21.227), and stones ≥10 mm (OR = 0.124, 95% CI: 0.031–0.495) were independent risk factors for UTI after ureteral stenting in patients with renal colic. In the infection group, Escherichia coli was the most commonly found organism (47.4%).

Conclusions:

Gestational age, positive urine culture before surgery, and stone ≥10 mm were risk factors for UTI after ureteral stenting in pregnant patients with renal colic. E. coli was the main pathogen of UTI after this procedure. Preoperative anti-infection treatment needs to be based on drugs that are sensitive to E. coli.

Introduction

Pregnancy with renal colic is one of the most common nonobstetric complications for which pregnant women can be hospitalized. Approximately, 1:200–1:1500 pregnant women experience a symptomatic stone event that might be renal colic or complications related to it.¹ Renal colic may cause adverse outcomes for mothers and fetuses, such as premature delivery, premature rupture of membranes, urinary tract infections (UTIs) and urosepsis, even pregnancy loss, and the occurrence of preeclampsia.^2,3

Conservative treatment of renal colic during pregnancy is effective in 70%–90% of patients.^4,5 However, when conservative treatment is ineffective, persistent renal colic or obstetric-related complications can occur; under these circumstances, active surgical intervention is necessary.⁶ As a safe and effective treatment, ureteral stenting has been used for patients with renal colic who did not respond to conservative treatment.^1,7

Ureteral stenting can serve as a drainage and supportive device to prevent obstruction, ureteral stenosis, colic, and renal failure caused by ureteral edema or kidney stone fragments; however, ureteral stenting is associated with complications such as pain, UTI, sepsis, readmission, and long-term hospitalization.⁸ UTI not only reduces a patient's quality of life and increases the cost of treatment but also affects the patient's recovery and, in some cases, can lead to pyelonephritis and systemic inflammatory response syndrome.

The aims of the present study were to analyze the risk factors for UTIs after ureteral stenting in patients with renal colic during pregnancy and to provide a theoretical basis for prevention and treatment of such infections.

Patients and Methods

We retrospectively reviewed the medical records of patients referred to the emergency department with a complaint of renal colic with pregnancy. The study period was between January 2009 and December 2019. In the past 10 years, a total of 418 patients were admitted to the hospital due to renal colic. Among them, 316 patients underwent effective conservative treatment; however, 102 patients required surgical treatment after conservative treatment failed.

In all cases, the diagnosis was based on clinical manifestations and confirmed by urinary color Doppler. Patients after ureteral stenting were hospitalized due to UTI before delivery and were evaluated.

The study evaluated demographic data, including patient age, gestational age, body mass index (BMI), fever, previous history of urolithiasis, infection indicators (such as White blood cell count, C-reactive protein [CRP], and procalcitonin [PCT]), urine culture, causes of renal colic, stone size, stone location, stone number, hydronephrosis, surgery indications (such as persistent renal colic, double kidney obstruction, purulent kidney, and isolated kidney), and residual stones after surgery. All patients undergo urine culture examination after admission. Before the urine culture results were available, patients with fever and elevated infection indicators were needed to be treated with antibiotics and we used second- or third-generation cephalosporins empirically. When the urine culture results are obtained, the medicine should be used according to the drug sensitivity test. The duration of antibiotic use should be based on two consecutive negative urine cultures. Under general or local anesthesia and antibiotic prophylaxis, cystoscopy was performed and a guidewire was advanced to the kidney through the ureter under fluoroscopic control, with the patient in the lithotomy position. Surgeons experienced in endourological methods performed the ureteral stenting procedures in all cases. A Double-J ureteral catheter was applied at the end of the procedure according to the surgeon's preference, and depending on the gestational week, we have chosen to place a stent for 3 months or 6 months or even 1 year. Double-J stents were removed at 4–6 weeks after delivery in all patients.

The definition of a UTI was that the patient had symptoms of urinary tract irritation such as frequent urination, urgency, and dysuria; tenderness in the lower abdomen; or percussion in the kidney area with or without fever. Laboratory examination showed urine test leukocytes of ≥10/high-magnification field of view and urine cultured with bacteria. The infected group was defined as patients who had a UTI after hospital discharge and before delivery. All patients were categorized into groups according to postoperative UTI.

Data were analyzed using SPSS 25. Numerical data are expressed as interquartile range (IQR) (Q1, Q3), while categorical data are given as numbers and percentages. To compare patient groups, the chi-square and Mann–Whitney U tests were used. Factors affecting the rates of UTIs after ureteral stenting were revealed using multiple binary logistic regression analysis. The level of significance was p < 0.05.

Results

A total of 102 patients were enrolled in this study. The mean patient age was 30 years (IQR = 26–33 years); mean patient BMI was 23 (IQR = 21–25) kg/m²; and mean gestational age was 22 weeks (IQR = 18–28). The early gestational age is 11 weeks. The latest gestational age is 32 weeks. Postoperative UTI after ureteral stenting occurred in 20.6% of patients between hospital discharge and delivery. To assess factors for UTI after ureteral stenting, UTI patients (n = 21) were compared with patients without UTI (n = 81). There was no statistically significant difference in age, BMI, white blood cells, neutrophils, CRP, PCT, causes of renal colic, hydronephrosis, calculus site, or surgical site between the UTI group and the control group. Univariate analysis results showed that gestational age (p = 0.00), stones ≥10 mm (p = 0.00), residual stones after surgery (p = 0.021), positive preoperative urine culture (p = 0.00), and surgery indication (p = 0.04) were risk factors for UTI in patients with renal colic after ureteral stenting. Baseline characteristics of the study population are shown in Table 1.

Table 1.

Comparison of Clinical Factors Between Patients With and Without Urinary Tract Infection After Ureteral Stenting

	Total cases (n = 102)	UTI group (n = 21)	Non-UTI group (n = 81)	p
Age (years), median (IQR)	30 (26–33)	29 (27–34)	30 (26–32)	0.284
Body mass index, (kg/m²), median (IQR)	23 (21–25)	21 (20.6–23)	23 (21–25)	0.451
Gestational age (weeks), median (IQR)	22 (18–28)	18 (14–22)	23 (21–25)	0.000
History of previous stone treatment, n (%)	26 (25.5)	8 (38.1)	18 (22.2)	0.137
Fever, n (%)	22 (21.6)	8 (38.1)	14 (17.3)	0.077
White blood cell count (10⁹/L), median (IQR)	13.25 (10.38–15.3)	12.64 (10.4–16.69)	12.1 (10.38–15)	0.477
Neutrophils (10⁹/L), median (IQR)	11.26 (8.0–13.72)	9.86 (8–13.19)	10.26 (8–13.72)	0.987
CRP (mg/dL), median (IQR)	3.32 (0.73–3.81)	2.62 (1.07–6.32)	1.84 (0.72–3.25)	0.147
PCT, n (%)	22 (21.6)	4 (19)	18 (22.2)	0.986
Preoperative urine culture, n (%)	22 (21.6)	11 (52.4)	11 (13.6)	0.000
Causes of renal colic, n (%)				1.000
Stones combined with hydronephrosis	82 (80.4)	17 (81)	65 (80.2)
Hydronephrosis	20 (19.6)	4 (19)	16 (19.8)
Stone location, n (%)				0.654
Kidney	30 (29.4)	4 (19)	26 (32.1)
Ureter	16 (15.9)	4 (19)	12 (14.8)
Both	36 (15.7)	9 (42.9)	27 (33.3)
None	24 (23.5)	4 (19)	20 (19.6)
Stone size, n (%)				0.000
<10 mm	56 (54.9)	4 (19)	52 (64.2)
≥10 mm	38 (37.3)	17 (81)	21 (35.8)
Stone number, n (%)				1.000
Single	22 (21.6)	4 (19)	18 (22.2)
Multiple	60 (58.8)	13 (61.9)	47 (58)
None	20 (19.6)	4 (19)	16 (19.8)
Hydronephrosis laterality, n (%)				0.178
Left	24 (23.5)	2 (9.5)	22 (27.2)
Right	40 (39.2)	11 (52.4)	29 (35.8)
Bilateral	38 (37.3)	8 (38.1)	30 (37)
Surgery indication, n (%)				0.040
Persistent renal colic	55 (53.9)	8 (38.1)	47 (58)
Double kidney obstruction	17 (16.7)	5 (23.8)	12 (14.8)
Pus kidney	28 (27.5)	6 (28.6)	22 (27.2)
Solitary kidney	2 (2)	2 (9.5)	0
Surgery laterality, n (%)				0.370
Left	48 (47)	13 (61.9)	35 (43.2)
Right	30 (29.4)	6 (28.6)	24 (42)
Bilateral	4 (4)	2 (9.5)	2 (14.8)
Residual stone after DJ placement, n (%)	50 (49)	15 (71.4)	35 (43.2)	0.028
Residual stone size after DJ placement, n (%)				0.355
<1 cm	76 (74.5)	14 (66.7)	62 (76.5)
≥1 cm	26 (25.5)	7 (33.3)	19 (23.5)

CRP = C-reactive protein; DJ = Double-J tube; IQR = interquartile range; PCT = procalcitonin; UTI = urinary tract infection.

On multivariate analysis, positive preoperative urine culture (odds ratio [OR] = 6.233, 95% confidence interval [CI]: 1.830–21.227), gestational age (OR = 1.147, 95% CI: 1.034–1.271), and stones ≥10 mm (OR = 0.124, 95% CI: 0.031–0.495) increased the risk of UTI after ureteral stenting. For the UTI group, the average gestational age is 18 weeks, early gestational age is 11 weeks, and latest gestational age is 24 weeks, and for the non-UTI group, the average gestational age is 23 weeks, early gestational age is 6 weeks, and latest gestational age is 32 weeks. Among 21 patients with postoperative UTI, 11 cases (52.4%) had a positive preoperative urine culture; among 81 cases of nonpostoperative UTI, 11 cases (13.6%) had a positive preoperative urine culture. The positive rate of preoperative urine culture in patients with UTI was 52.4% (11/21), and the positive rate of preoperative urine culture in patients with non-UTI was 13.6% (11/81), the difference was statistically significant (χ ² = 12.64, p < 0.01).

Compared with those who had a negative urine culture before surgery, the risk of postoperative UTI was increased (OR = 6.233, 95% CI: 1.830–21.227). In 21 patients with postoperative UTIs, 17 patients (81%) had stones ≥10 mm; among 81 cases of nonpostoperative UTIs, 21 patients (35.8%) had stones ≥10 mm. The difference was statistically significant (χ ² = 13.73, p < 0.01). Patients with stones ≥10 mm were at higher risk of UTI after surgery (OR = 0.124, 95% CI: 0.031–0.495; Table 2).

Table 2.

Multivariate Analysis for Urinary Tract Infection After Ureteral Stenting

Variables	OR	95% CI	p
Gestational age	1.147	1.034–1.271	0.009
Urine culture	6.233	1.830–21.227	0.003
Stone size	0.124	0.031–0.495	0.003

CI = confidence interval; OR = odds ratio.

The positive rate of urine culture in patients with postoperative UTI was 52.4%; however, in the non-UTI group, the positive rate of urine culture was 13.6%. The pathogenic bacteria in patients preoperatively were mainly Escherichia coli (Table 3).

Table 3.

Analysis of Pathogenic Bacteria in Patients with Renal Colic During Pregnancy Before Ureteral Stenting

Pathogenic bacteria	UTI group (n = 21)	Non-UTI group (n = 81)	p
Escherichia coli, n (%)	7 (33.3)	9 (11.1)	0.000
Pseudomonas aeruginosa, n (%)	2 (9.5)	0 (0)
Kepley pneumonia, n (%)	2 (9.5)	2 (2.5)

All the UTI patients had single-pathogen infections; 19 pathogenic bacteria were isolated and 2 patients were admitted to hospital due to fever, empirical use of antibiotics, and urine culture that failed to cultivate clear bacteria. Analysis of urine culture results after ureteral stent placement in 21 UTI patients showed that 52.3% of the patients were still infected with E. coli and the rest with Pseudomonas aeruginosa, Kepley pneumonia, Staphylococcus epidermidis, Acinetobacter baumannii, and Proteus mirabilis (Table 4). In patients with E. coli infection before surgery, 63.6% still had an E. coli urine culture after ureteral stenting.

Table 4.

Analysis of Urine Culture Pathogens in Patients with Urinary Tract Infection After Ureteral Stent Placement

Pathogenic bacteria	n (%)
Escherichia Coli	11 (52.3)
Pseudomonas aeruginosa	2 (9.5)
Kepley pneumonia	2 (9.5)
Staphylococcus epidermidis	2 (9.5)
Acinetobacter baumannii	2 (9.5)
Not clear	2 (9.5)

After analyzing drug resistance of the E. coli pathogen, the following Class B antibiotics were effective during pregnancy: piperacillin/tazobactam, cefoxitin, ceftriaxone, amoxicillin/clavulanate potassium, cefoperazone/sulbactam, cefazolin, cefotaxime, and cefuroxime sodium. Antibiotics which are sensitive to Pseudomonas aeruginosa and Klebsiella pneumoniae include piperacillin/tazobactam, cefoxitin and cefoperazone/sulbactam.

Discussion

In this retrospective study, we explored the risk factors associated with UTIs after ureteral stenting in pregnant patients with renal colic and analyzed the pathogenic bacteria. We report that the incidence of UTI after ureteral stenting in these patients was 20.6%. Multivariate analysis showed that gestational age, a positive preoperative urine culture, and stones ≥10 mm were independent risk factors for UTI after ureteral stenting in patients with renal colic during pregnancy.

Postoperative UTI is a common complication after ureteral stenting in nonpregnant patients. The incidence of UTI after ureteral stent placement has been reported in the literature, ranging from 6% to 45%,⁹ including a recent prospectively performed study reporting an 11% incidence of UTIs in stented patients.¹⁰ Reports of the incidence of UTI after ureteral stenting in pregnancy are relatively few. While pregnant women with a stone managed conservatively had a UTI rate of 3.7%, those managed with ureteral stents and/or ureteroscopy had an increased UTI rate of 8.7%. Urologic intervention with a ureteral stent independently increased the risk of UTI at delivery.¹¹ Our research showed that the incidence of postoperative UTI was 20.6% and that gestational age was a high risk factor for postoperative UTI. In the infected group, the average gestational age was 18 weeks, and in the noninfected group, the average gestational age was 22 weeks. The average gestational age of the infected group was 4 weeks longer than that of the noninfected group, which increased the time for ureteral stent placement. A stent residence time >30 days is associated with a 5-fold increase in postoperative urinary tract sepsis risk.¹² In our study, the infection group had a 1.1-fold increased risk of UTI compared with the noninfection group (OR = 1.147, 95% CI: 1.034–1.271). The increase in the use of the stent is related to stent-linked infections, and bacterial stent colonization plays an important role in infections linked to the stent.^13,14 Bacterial colonization at the stent began 2 weeks after indwelling stent placement and that stent colonization preceded urine colonization.¹⁵ The majority of stents placed are removed within 2 weeks, but a subset of stented patients require chronic indwelling stents over longer periods, sometimes indefinitely, such as pregnancy.¹⁶ The bacteriuria rate was 4.2% for stents removed within 30 days and 34% for stents removed after 90 days.¹⁷ A sharp rise in bacteriuria is observed when the dwell time is greater than 6 weeks.¹⁸ Stent colonization at the time of removal is generally reported at rates over 40%¹⁹ and rates of 90% or more have been reported.²⁰ To reduce UTIs caused by long ureter retention times, first, we should reduce the time of indwelling (as much as possible) and replace the ureteral stent in time, and second, we need to consider the material of the ureteral stent.¹⁶ For patients who needed surgical treatment for renal colic during pregnancy, we used the same type of stent. Stent encrustation is common in pregnancy, which was an important factor of UTI after ureteral stent placement. An indwelling stent presents multiple challenges with regard to infection, specifically, fouling and deposition of biomaterials on the stent and the continual transient entry of bacteria into the urinary tract.²¹ Bioresorbable stents and a plethora of stent coatings have been developed to address stent-associated complications, including infection, pain, and encrustation. However, these innovations continue to be preclinical and, in several cases, have proven ineffective in clinical studies. Work continues on evolving stent designs.²²

In our study, the rate of positive preoperative urine culture was 21.6% among 102 patients; 52.4% of preoperative urine cultures were positive in the UTI group, therefore a positive preoperative urine culture was a risk factor for postoperative UTIs. A positive urine culture before surgery is the most powerful predictor of postoperative infection and an important risk factor for emergency admission after surgery. Sohn et al. revealed that bacteriuria and catheterization were the strongest risk factors for febrile complications.²³ The degree of pyuria was likely to be associated with severity of postoperative febrile UTI.²⁴ The incidence of postoperative infectious complications is still high even if antibacterial treatment has been administered before surgery and a sterile urine culture has been obtained before ureteral stenting.²⁵ Although we provided reasonable antibiotic treatment to patients with positive urine cultures, there were still 11 cases of UTI after surgery, consistent with previous studies. A positive urine culture before surgery increased infectious complications (4.75-fold) after laser lithotripsy in patients with calculi.²⁶ Patel and colleagues report that a positive percutaneous nephrolithotomy urine culture before surgery can increase the incidence of postoperative infectious complications (4.89-fold).²⁷ Our study showed that a positive preoperative urine culture increased the incidence of UTIs after ureteral stenting (6.3-fold); the use of sensitive antibiotics in patients having a positive urinary culture before surgery is important. Therefore, prevention of infection is a high priority for any doctor. For now, the basic principles of prophylactic antibiotics at time of insertion, minimizing stent dwell time, and avoiding contamination remain the best practices to avoid stent-related urinary infections.¹⁶ At the time of ureteral stent removal, the most common organisms isolated from stents are common urinary pathogens, such as E. coli, P. aeruginosa, Staphylococcus spp, and Enterococcus spp, although these probably vary with local infection patterns.¹⁹ By analyzing the pathogens in preoperative urine cultures, we found that E. coli commonly caused UTI after surgery. As many antibiotics are banned during pregnancy, empirical therapy is essential before urine culture results become available. E. coli is sensitive to drugs such as piperacillin/tazobactam, cefoxitin, and ceftriaxone; this has a strong clinical significance and deserves special attention from obstetricians and urologists. These related findings are particularly important because infections caused by urine culture pathogens require timely and appropriate treatment, including empirical and definitive antibiotic treatment, to reduce postoperative morbidity and cost.

UTIs are common in patients with urinary stones, and stone size is the main factor affecting the passage of ureteral stones. Compared with patients who did not experience an antepartum stone admission, stone patients had a higher rate of UTI before delivery (40.0% vs 0.7%).¹¹ Stone diameter was considered to predict complications in previous studies²⁸ because a median stone of 15 mm may be much larger than that in previous reports that studied complications of ureteroscopy or endourological procedures.²⁹ However, stone size was not significantly different between patients with and without UTI in some studies.²⁴ Our research showed that stones ≥10 mm increased the risk of postoperative UTI. The risk of infection with stones <10 mm was 19%, and the risk of UTI with stones >10 mm was 81%. Therefore, we suggest that it is necessary to use antibiotics before surgery, especially for patients with larger stones.

Our research provides useful information for obstetricians and urologists. Determining the risk factors for the postoperative urinary tract can improve the patient–clinician relationship and allows the clinician to identify patients who need to be readmitted again after discharge. Appropriate guidance should be given for preoperative prevention and postoperative care.

Limitations

Our research had some limitations. First, this was a single-center retrospective study, which may have led to selective bias. However, urology is a key discipline at The First Affiliated Hospital of Guangzhou Medical University in China, where patients from all over the country seek their medical services. Second, no information was collected regarding operation time. Finally, the incidence of renal colic during pregnancy is relatively low, 70%–90% conservative treatments of renal colic during pregnancy were effective, and our success rate of conservative treatment was about 75.6% (316/418), therefore there were relatively few patients undergoing surgery and the sample size was relatively small. Further evaluation of this subject requires large-scale, multicenter prospective research.

Conclusions

Our study showed that a positive urine culture before surgery, gestational age, and stones ≥10 mm were important risk factors for UTI after ureteral stenting in pregnant women with renal colic. However, due to the limitations of this single-center retrospective study, it is necessary to conduct a well-designed, multicenter prospective study to discover the postoperative risk factors for UTI. Nevertheless, we suggest that it is important to use antibiotics rationally in patients with a positive urine culture and stones ≥10 mm before surgery. For patients with no obvious symptoms after ureteral stent placement, B-ultrasound stones <10 mm, and negative urine culture, can we try to remove the stent earlier to reduce UTIs? This is worth discussing and merits further research.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

Funding Information

Research Fund Project of Guangzhou Medical University (2013A03).

Abbreviations Used

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