Risk Factors for Postoperative Fever and Systemic Inflammatory Response Syndrome After Ureteroscopy for Stone Disease

Abstract

Introduction:

Infectious complications after ureteroscopy (URS) for stone disease lead to emergency department visits, hospitalizations, and other costly health care utilization. The objective of our study was to identify risk factors for postoperative fever (POF) and systemic inflammatory response syndrome (SIRS) after URS for stone disease.

Materials and Methods:

We performed a retrospective cohort study on 2746 patients who underwent 3298 URS for stone disease at Geisinger from 2008 to 2016. A univariate analysis tested the associations between candidate demographic, preoperative, and intraoperative predictors and the primary outcome of POF (temperature >100.4°F) or SIRS. Variables with a p-value of <0.05 on univariate comparisons were entered into a random-effects logistic regression model. The final model used backward elimination random-effects logistic regression to identify predictors most predictive of POF/SIRS.

Results:

Overall, 229 (6.9%) of 3298 URS had POF/SIRS. On univariate analysis, individuals with POF/SIRS were older, had higher mean body mass index, higher Charlson Comorbidity Index (CCI), bilateral and larger stones, stone location in the kidney, positive preoperative urine culture, pre-stented, and longer surgical times. In the final model, female gender (adjusted odds ratio [OR] 1.6, 95% confidence interval [CI] 1.19–2.15), surgical time (adjusted OR 1.01, 95% CI 1.0–1.01), CCI ≥2 (adjusted OR 1.86, 95% CI 1.29–2.67), and positive preoperative urine culture (adjusted OR 1.53, 95% CI 1.06–2.22) were the most significant predictors of POF/SIRS.

Conclusions:

Female gender, longer surgical time, medical complexity, and positive preoperative urine culture are associated with POF/SIRS after URS. These data may be used to identify and counsel high-risk individuals.

Introduction

The burden of kidney stone disease is growing with a lifetime incidence of 7% to 12%.¹ Ureteroscopy (URS) is frequently used for surgical management of upper urinary tract stones less than 1 cm, which has stone-free rates in excess of 80%.^2
–4 Between 2000 and 2010, the use of URS for stone disease increased by 127%.⁵ URS has low overall complication rates of 2.6% to 3.5%; however, a Cochrane review found that extracorporeal shockwave lithotripsy has lower overall complication rates.^4,6,7 As URS is almost exclusively an ambulatory procedure, emergency room (ER) visits and unplanned hospitalizations may result in increased costs to the health system. A review of a statewide database from California of more than 17,000 URS found that in the 7 days following the procedure, 6.6% of patients were seen in the emergency department and 2.2% were admitted.⁸ As a result, it is important to identify the ways to prevent complications that lead to health care utilization after URS to reduce burdens on patients, families, and payers.⁹

One of the most common complications leading to unplanned hospitalizations is postoperative fever (POF) or systemic inflammatory response syndrome (SIRS).^4,6,10,11 Recent estimates suggest that 3.4% to 14.2% of emergency department visits are for POF.^12,13 More than 40% of patients presenting with fever undergo hospital admission.¹⁴ SIRS occurs in up to 8.1% of patients after URS.¹⁵ Early identification and prompt management of POF/SIRS are necessary to prevent progression to sepsis, which carries a mortality rate of 28.3% to 41.1%.¹⁶ A small number of studies have examined a variety of patient and operative characteristics in an attempt to identify high-risk individuals. Due to the smaller sizes of these prior cohorts, the number of potential risk factors that could be assessed was limited.

The objective of this study was to identify predictors of POF/SIRS after URS for stone disease. We examined a comprehensive list of candidate predictors, including demographic, preoperative, and intraoperative factors in a large URS cohort from a community-based health system.

Materials and Methods

Data/cohort

After institutional review board approval, we identified 3598 URS performed at Geisinger, a community-based health system in Pennsylvania, between January 2008 and September 2016. We identified URS by querying the electronic health record (EHR) for the following Current Procedural Terminology (CPT) codes: 52351, 52353, and 52356. Only adults aged 18 years or older at the time of URS were included. URS encounters with incomplete laterality (n = 2), missing preoperative antibiotic data (n = 256), or missing covariates (n = 252) were excluded. URS performed for indications other than stone disease (e.g., upper tract urothelial carcinoma) were also excluded (n = 46). The final analysis cohort included 2746 patients who underwent 3298 URS procedures.

Outcomes

The primary outcome was POF or SIRS identified within 7 days after URS. POF was defined as temperature >100.4°F. SIRS was defined as the presence of at least two of the following: temperature >100.4°F, heart rate >90, respiratory rate >20 or PaCO₂ < 32 mm Hg, or white blood cell count >12,000/mm³, <4000/mm³, or >10% bands.¹⁷ As many postsurgical patients to meet these criteria, we limited the outcome to clinically significant POF/SIRS defined as immediate postoperative admission, hospital readmission within 7 days, or emergency department visit within 7 days.¹⁸ Manual chart review was performed to confirm that patients met criteria for POF or SIRS at the time of the encounter.

Predictors

Demographic, preoperative, and intraoperative predictors were selected a priori based on the literature review and consultation with a fellowship-trained endourologist (B.R.F.). Data were collected through an EHR data pull followed by manual chart review. Demographic characteristics included age at the time of surgery, sex, race/ethnicity, body mass index (BMI), estimated glomerular filtration rate (eGFR), and Charlson Comorbidity Index (CCI). Prior urologic and stone surgeries were identified using a list of CPT codes (Supplementary Table S1; Supplementary Data are available online at www.liebertpub.com/end). Preoperative characteristics included stone laterality (unilateral or bilateral), largest stone size, stone location (renal, ureteral, or both), positive preoperative urine culture (yes/no), pre-stenting (yes/no), and preoperative antibiotics (yes/no). Intraoperative characteristics included total minutes in surgery, type of ureteroscope (flexible, semirigid, or both), access sheath use, and stent placement at the end of URS. Stone type was identified. We examined types of bacteria in preoperative and postoperative urine cultures in patients with POF/SIRS.

Statistical analyses

Unadjusted associations between URS encounters with and without POF/SIRS were assessed. Continuous variables were compared using two-sample t-tests for normally distributed variables and Wilcoxon rank-sum test for nonnormally distributed variables. Pearson's chi-squared tests were used to compare categorical variables. Univariate analyses were conducted without accounting for multiple URS encounters per patient.

Variables with a p-value of <0.05 were entered into a multivariable random-effects logistic regression model (GENMOD procedure using binomial distribution with repeated statement). This type of model was selected to control for individual patients who had multiple URS over the study period. In multivariable analysis, we controlled for demographic, preoperative, and intraoperative characteristics and stone type. To identify the most significant predictors of POF/SIRS, a backward elimination random-effects logistic regression algorithm was conducted on the full multivariable model. The GENMOD procedure only has an automated backward elimination algorithm, and the model was verified by manually adding each individual variable back into the model in a stepwise manner. Analyses were performed using SAS version 9.4 (Cary, NC).

Sensitivity analysis

A sensitivity analysis was performed comparing URS encounters with missing data (n = 252) to complete encounters before excluding encounters with missing data. The data were missing at random, and significant differences between groups were found in eGFR, CCI, access sheath use, stent placement at the end of surgery, and stone type (Supplementary Table S2). As data were missing at random, the URS procedures with missing data were excluded from the main analysis.

We observed significant unadjusted differences between men and women undergoing URS (Supplementary Table S3) and performed analyses using interaction terms between sex and all variables that were significantly different between men and women (age, BMI, preoperative urine culture, stone location, and minutes in surgery).

Results

A total of 2746 patients underwent 3298 URS for stone disease. Of the total cohort, the majority of patients were white (98.4%) and 136 patients (4.9%) underwent 3 or more URS (Fig. 1). POF/SIRS was identified after 229 procedures (6.9%). Of patients with POF/SIRS, 226 had an ER visit within 7 days and 75 were admitted. A total of 1297 URS (39.4%) were performed in pre-stented individuals. Baseline patient demographics, preoperative characteristics, and intraoperative procedures differed between the POF/SIRS and non-POF/SIRS groups. In cases where POF/SIRS occurred, patients were older, had higher mean BMI, lower eGFR, and higher CCI (Table 1). A history of urologic surgery (53.3%) and stone surgery (40.2%) were more frequent in the POF/SIRS group.

FIG. 1.

Distribution of ureteroscopy procedures.

Table 1.

Baseline Characteristics of Ureteroscopy Cases (N = 3298)

	All (N = 3298)	POF/SIRS		p
	All (N = 3298)	No (N = 3069)	Yes (N = 229)	p
Patient characteristics
Age, years, n (%)
<65	2408 (73.0)	2257 (73.5)	151 (65.9)	0.01
≥65	890 (27.0)	812 (26.5)	78 (34.1)
Sex, n (%)
Male	1628 (49.4)	1535 (50)	93 (40.6)	0.006
Female	1670 (50.6)	1534 (50)	136 (59.4)
BMI, mean (SD)	31.8 (8.03)	31.7 (7.91)	33.0 (9.35)	0.05
eGFR, n (%)
<60	799 (24.2)	731 (23.8)	68 (29.7)	0.05
≥60	2499 (75.8)	2338 (76.2)	161 (70.3)
CCI, n (%)
0	1890 (57.5)	1787 (58.3)	103 (45.6)	<0.0001
1	624 (19.0)	584 (19.1)	40 (17.7)
2+	775 (23.6)	692 (22.6)	83 (36.7)
Missing	9	6	3
Prior urologic surgery, n (%)	1418 (43.0)	1294 (42.2)	122 (53.3)	0.001
Prior stone surgery, n (%)	1101 (33.4)	1007 (32.8)	92 (40.2)	0.02
Preoperative characteristics
Stone laterality, n (%)
Bilateral	215 (6.5)	189 (6.2)	26 (11.4)	0.002
Unilateral	3083 (93.5)	2880 (93.9)	203 (88.6)
Stone size on imaging, cm, n (%)
<1.0	2071 (62.8)	1951 (63.6)	120 (52.4)	0.0007
≥1.0 (includes staghorn)	1227 (37.2)	1118 (36.4)	109 (47.6)
Stone location on imaging, n (%)
Both	787 (23.9)	731 (23.8)	56 (24.5)	0.005
Renal	1431 (43.4)	1312 (42.8)	119 (52.0)
Ureteral	1080 (32.7)	1026 (33.4)	54 (23.6)
Preoperative urine culture, n (%)
Positive	481 (14.6)	429 (14.0)	52 (22.7)	0.0003
Negative/not tested	2817 (85.4)	2640 (86.0)	177 (77.3)
Pre-stented, yes, n (%)	1299 (39.4)	1183 (38.5)	116 (50.7)	0.0003
Preoperative antibiotics, yes, n (%)	2965 (89.9)	2759 (89.9)	206 (90)	0.98
Intraoperative characteristics
Total minutes in surgery, median (IQR)	49 (34–75)	49 (33–74)	57 (36–95)	0.0006
Type of ureteroscopy, n (%)
Flexible or semirigid	2934 (89.0)	2737 (89.2)	197 (86.0)	0.14
Both	364 (11.0)	332 (10.8)	32 (14.0)
Access sheath used, n (%)	2183 (66.2)	2021 (65.9)	162 (70.7)	0.13
Stent placed at the end of surgery, n (%)	2748 (83.3)	2547 (82.7)	201 (87.8)	0.06
Stone type, n (%)
Calcium oxalate	1059 (32.1)	994 (32.4)	65 (28.4)	0.22
Calcium oxalate mix	931 (28.2)	876 (28.5)	55 (24)
Calcium phosphate (apatite)/calcium hydrogen phosphate (brushite)	132 (4)	119 (3.9)	13 (5.7)
Struvite mix	75 (2.3)	67 (2.2)	8 (3.5)
Uric acid mix	90 (2.7)	85 (2.8)	5 (2.2)
Cystine	8 (0.2)	7 (0.2)	1 (0.4)
Matrix mix	16 (0.5)	14 (0.5)	2 (0.9)
Missing	987 (29.9)	907 (29.6)	80 (34.9)

POF = postoperative fever; SIRS = systemic inflammatory response syndrome; SD = standard deviation; eGFR = estimated glomerular filtration rate; CCI = Charlson Comorbidity Index; BMI = body mass index; IQR = interquartile range.

POF/SIRS occurred more frequently in procedures with increased stone complexity, including bilateral stones (11.4%), stones ≥1 cm (47.6%), stone location in both the kidney and ureter (24.5%), positive preoperative urine culture (22.7%), and in URS performed in pre-stented individuals (50.7%). Intraoperatively, procedures complicated by POF/SIRS had longer median surgical times (57 minutes vs 49 minutes, p < 0.01).

In a fully adjusted random-effects logistic regression model that included all variables significant on univariate analysis plus stone type, we found that female gender (adjusted odds ratio [OR] 1.55, 95% confidence interval [CI] 1.15–2.10) and CCI ≥2 (adjusted OR 1.59, 95% CI 1.08–2.34) were significantly associated with POF/SIRS (Table 2). The final predictive model developed using a backward elimination algorithm included female gender (adjusted OR 1.60, 95% CI 1.19–2.15), longer surgical time (adjusted OR 1.01, 95% CI 1.00–1.01), CCI ≥2 (adjusted OR 1.86, 95% CI 1.29–2.67), and positive preoperative urine culture (adjusted OR 1.53, 95% CI 1.06–2.22) as the most significant predictors of POF/SIRS (Table 3). In URS procedures with POF/SIRS and positive preoperative urine culture (Table 4), the three most common bacteria types were multiple (6.6%), Enterococcus (4.8%), and Escherichia coli (4.4%). Of the “not tested/negative culture” group with POF/SIRS, 19.8% did not have preoperative urine cultures.

Table 2.

Logistic Regression Model for Postoperative Fever/Systemic Inflammatory Response Syndrome

	OR (95% CI)	p
Age, years (ref: <65)	1.30 (0.92–1.83)	0.14
Sex (ref: male)	1.55 (1.15–2.10)	0.004
BMI (continuous)	1.01 (0.99–1.03)	0.20
Total minutes in surgery (centered, continuous)	1.003 (0.999–1.007)	0.14
eGFR (ref: >60)	1.04 (0.75–1.44)	0.83
Laterality (ref: unilateral)	1.38 (0.83–2.28)	0.21
Stone size on imaging, cm (ref: <1 cm)	1.20 (0.86–1.67)	0.28
Stone location on imaging (ref: renal)
Ureteral	0.79 (0.55–1.14)	0.21
Both	1.01 (0.71–1.43)	0.96
CCI (ref: 0)
1	1.19 (0.81–1.77)	0.38
2+	1.59 (1.08–2.34)	0.02
Prior urologic surgery (ref: no)	1.20 (0.74–1.95)	0.45
Prior stone (ref: no)	1.01 (0.69–1.47)	0.96
Preoperative urine culture (ref: negative/not tested)	1.40 (0.95–2.06)	0.09
Pre-stented (ref: no)	1.08 (0.69–1.68)	0.75

ref = reference value; OR = odds ratio; CI = confidence interval.

Table 3.

Backward Elimination Model for Postoperative Fever/Systemic Inflammatory Response Syndrome

	OR (95% CI)	p
Sex (ref: male)	1.60 (1.19–2.15)	<0.01
Total minutes in surgery (centered, continuous)	1.01 (1.00–1.01)	<0.01
CCI (ref: 0)
1	1.29 (0.88–1.90)	0.19
2+	1.86 (1.29–2.67)	<0.01
Preoperative urine culture (ref: negative/not tested)	1.53 (1.06–2.22)	0.02

Table 4.

Urine Culture Results for Postoperative Fever/Systemic Inflammatory Response Syndrome

	POF/SIRS (N = 229)
	Preoperative, n (%)	Postoperative, n (%)
Urine culture
Positive	52 (22.7)	28 (12.2)
Negative/not tested	177 (77.3)	201 (87.8)
Urine culture bacteria type
Citrobacter	1 (0.4)	0 (0)
Enterobacter	1 (0.4)	1 (0.4)
Enterococcus	11 (4.8)	5 (2.2)
Escherichia coli	10 (4.4)	3 (1.3)
Klebsiella	3 (1.3)	0 (0)
Morganella	0 (0)	0 (0)
Multiple organisms	15 (6.6)	8 (3.5)
Proteus	3 (1.3)	2 (0.9)
Providencia	1 (0.4)	0 (0)
Pseudomonas	0 (0)	5 (2.2)
Staphylococcus	5 (2.2)	4 (1.8)
Streptococcus	1 (0.4)	0 (0)
Missing	1 (0.4)	0 (0)
Negative/not tested	142 (62)	201 (87.8)

In analyses stratified by sex (Supplementary Table S3), women undergoing URS were younger, had higher mean BMI (32.3 vs 31.3), more frequently had stone location in the kidney only (48.7% vs 37.9%), and a higher proportion had positive preoperative urine cultures (17.4% vs 11.7%) and struvite stones (2.8% vs 1.7%). When comparing men and women who developed POF/SIRS after URS, only median total minutes in surgery was significantly different with men having longer surgical time (66 minutes vs 48.5 minutes). Interaction term analysis showed no significant differences between sex and age (p = 0.65), BMI (p = 0.3), preoperative urine culture (p = 0.29), stone location (p = 0.8), and total minutes in surgery (p = 0.16).

Discussion

In this cohort of 3298 URS for stone disease from a community-based health system, our objective was to determine which demographic, preoperative, and intraoperative characteristics were the best predictors of POF/SIRS. We found that female gender, longer surgical times, medical complexity, and positive preoperative urine cultures were the strongest predictors of POF/SIRS after URS for stone disease. This is one of the largest existing studies examining risk factors for infectious complications after URS, and the large sample size allows for a range of candidate predictors.

Stone disease is a growing, costly chronic condition associated with health care utilization.^19,20 URS is one option for treatment of stones <1 cm, and the procedure has expanded exponentially over the past decade.^2,3,5 While complications of URS are infrequent, POF is among the most common and results in high rates of ER visits and unplanned admissions.^6,12
–14 Comparable to reported rates, we found that 6.9% of URS were either seen in the ER or readmitted for POF/SIRS.²¹ Our results expand on prior studies of POF, SIRS, and other infectious complications after URS. Although no standard definition of post-URS infectious complications exists, female gender, medical complexity, longer operative time, and preoperative pyuria or positive urine culture have all been noted as risk factors in studies using a variety of outcome definitions.

We attempted to explain the gender differences in univariate analysis and found significant differences in baseline characteristics, including a higher proportion of women having positive preoperative urine cultures and infection stones. In 1325 procedures from the Clinical Research Office of the Endourological Society (CROES) URS Global Study Database, female gender and medical complexity were predictive of POF or urinary tract infection (UTI), even in the absence of a positive preoperative urine culture.²² Another study corroborated these findings in 927 URS procedures, of which 286 were performed in women. The authors noted a significant difference in the incidence of febrile UTI between men (1%) and women (3%).²³ While it is not clear why women have a higher likelihood of infectious complications after URS, it may be due to short urethral length or ambient bacteria.

Similar to other studies, we found that longer operative times are associated with POF/SIRS. Operative time may be a proxy for surgical complexity due to stone characteristics.²⁴ Kuroda and colleagues developed a model to predict URS operative time based on a cohort of 972 patients.²⁵ Preoperative stenting, stone volume, Hounsfield units, surgeon experience, sex, and small sheaths predicted longer operative times. We believe that the majority of preoperative and intraoperative characteristics in our study were not significant as they contribute collectively to longer surgical time. Other studies found longer operative times to be associated with POF. A study of 550 patients found that URS operative times of greater than 120 minutes were associated with unplanned returns for infection, although the CIs were wide, likely due to the small number of outcomes (adjusted OR 18.51, 95% CI 4.19–82.08, p < 0.001).¹³

Aging and medical complexity are important considerations in discussions regarding the risks and benefits of urologic procedures.²⁶ In 11,719 patients from the CROES URS Global Study Database, the authors found that older medically complex adults on anticoagulation were more likely to have postoperative complications (3.5%), of which 75% were fever, UTI, or other.²⁷ Diabetes and cardiovascular disease posed the greatest risk. In a cohort of 276 URS, patients with ≥2 comorbidities had a higher risk of readmission, and hypertension or asthma/chronic obstructive pulmonary disease was significantly associated with readmission.¹⁴ Similar to the other studies, we found that CCI ≥2 predicted a nearly twofold risk of POF/SIRS.

The most significant modifiable predictor from our cohort was positive preoperative urine culture. Multiple reports have found preoperative pyuria or positive urine cultures to be associated with infectious complications after URS, although they had smaller cohort sizes ranging from 100 to 500 patients. The largest cohort had 532 patients and found that 3.8% had infectious complications, and risk factors included preoperative bacteriuria, hydronephrosis, and urinary tract foreign bodies.²⁸ In another cohort of 153 patients, 18.3% developed febrile UTI, and preoperative pyuria was one of the most significant factors (OR 3.62, 95% CI 1.26–8.11).²⁹ An American Urological Association (AUA) best practice statement recommends perioperative antimicrobial prophylaxis to all patients undergoing URS due to the risk of bacteremia from stone manipulation and endoscopy of the upper tract.³⁰

It is our standard practice to obtain urine cultures and to treat positive cultures regardless of symptoms before undertaking URS. We recognize that this exceeds the current AUA guidelines, which recommend a urinalysis alone for asymptomatic individuals.² The perioperative antibiotic is tailored to the bacterial organism and susceptibilities, as well as the local antibiogram. Our postoperative regimen is 3 days of an antibiotic with genitourinary coverage (e.g., ciprofloxacin or trimethoprim–sulfamethoxazole). However, due to emerging concerns about fluoroquinolones, we now use alternatives such as clindamycin, cephalexin, or 5 to 7 days of nitrofurantoin. Despite this standard practice, some patients still develop infectious complications. Further research is needed to understand the pathophysiology and how to reduce the risk of this complication.

Our study has several strengths. With a large cohort of URS procedures, we were able to examine the relationships between a wide variety of candidate risk factors and the outcome. Due to our robust EHR, it was possible to obtain electronic data and corroborate with chart review. The Geisinger patient population has a low out-migration rate, reducing the possibility that the outcome may be underreported due care outside the system. Our study was conducted in a community-based system allowing for reporting of real-world experience.

Our study must be interpreted within the context of certain limitations. No standard definition of infectious complications exists, and we focused on POF/SIRS, an outcome that results in costly health care utilization. Our study lacked granular data on the length of postoperative stenting, pre- and postoperative antibiotic use, and preoperative urine culture results. Our cohort was predominantly white, which reflects the race/ethnicity of central Pennsylvania but may limit generalizability to diverse populations. The Geisinger catchment area is predominantly rural, which may also limit generalizability. However, rural areas are disproportionately burdened by stone disease, yet urban/rural disparities remain understudied.¹⁹ Our study may provide greater insight into outcomes for stone procedures performed in rural populations.

Conclusions

In this large study of URS, we found that female gender, medical complexity, longer operative times, and positive preoperative urine cultures were the most significant predictors of POF/SIRS. These data will help providers to identify high-risk individuals and counsel them regarding POF/SIRS. Future studies will focus on identifying the ways to prevent infectious complications in at-risk patients.

Footnotes

Acknowledgments

The authors acknowledge Dr. John Walton, Dr. Mahmoud Mohamed, and Dr. Newaj Abdullah for assistance with manual chart review, and Dr. Jacob Baber for initial input on study design. The authors also acknowledge Ayesha Khan for administrative assistance. This study was supported by the Geisinger Clinic Research Fund.

Author Disclosure Statement

No competing financial interests exist.

Abbreviations Used

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