Abstract
Purpose:
To assess the impact of implementing the recommendations included in the 2014 American Urological Association (AUA) white paper on complications of transrectal prostate needle biopsy (PNB).
Methods:
In the outpatient setting of a single tertiary-care institution, prophylactic antibiotic use and rate of infectious complications were compared before and after implementation by nursing of a standardized algorithm to select antibiotic prophylaxis (derived from the recommendations of the AUA white paper). The 584 patients in cohort A (January 2011–January 2012) received antimicrobial prophylaxis at the discretion of the treating physician; 654 patients in cohort B (January 2014–January 2015) received standardized risk-adapted antibiotic prophylaxis. Data on antibiotics administered and infectious complications were analyzed.
Results:
Fluoroquinolone was the most common prophylactic regimen in both cohorts. In cohort A, 73% of men received a single-drug regimen, although 19 different regimens were utilized with duration of 72 hours. In cohort B, 97% received 1 of 4 standardized single-drug antibiotic regimens for duration of 24 hours. Infectious complications occurred in 19 men (3.3%) in cohort A, and in 18 men (2.8%) in cohort B (difference − 0.5%; one-sided 95% CI: 1.1%). No clinically relevant increase in infectious complication rates was found after implementing this quality improvement initiative.
Conclusions:
Use of a standardized risk-adapted approach to select antibiotic prophylaxis for PNB by nursing staff reduced the duration of antimicrobial prophylaxis and number of antibiotic regimens used, without increasing the rate of infectious complications. Our findings validate the current AUA recommendations for antibiotic prophylaxis.
Keywords: prostatic neoplasm, biopsy, infection, prophylaxis, treatment outcome, stewardship
INTRODUCTION
Over one million transrectal ultrasound-guided prostate needle biopsies (PNB) are performed annually in the United States among Medicare beneficiaries alone. Among the complications reported, infections are the most worrisome. These range from minor to life-threatening and include bacteriuria, urinary tract infection (UTI), prostatitis, epididymitis, orchitis, and sepsis. Overall rates of reported infectious complications after PNB range from 0.1 to 7% [1].
Two recent meta-analyses of randomized controlled trials confirmed the benefits of antimicrobial prophylaxis to reduce the morbidity of infectious complications after PNB. Longer courses of antibiotics were not associated with reduced rates of serious infections [2–3].
Fluoroquinolones are the most commonly used antibiotics to prevent infectious complications after PNB, due to their good oral bioavailability, extended half-life, high concentration in urine and prostatic tissue, and broad spectrum of antimicrobial activity [4]. However, their widespread use has resulted in an increase in fluoroquinolone-resistant bacteria [5] and recent epidemiologic studies have shown increased rates of infectious complications following PNB [6–7]. The most common etiologic agent is fluoroquinolone-resistant Escherichia coli, which has been found in up to 22% of men undergoing PNB [8]. To address this problem, several strategies have been developed, including targeted prophylaxis, augmented prophylaxis, and risk-adapted prophylaxis according to a preventive risk assessment [9]. However, the optimal strategy to prevent or reduce post-PNB infectious complications has not yet been defined.
In 2014, the American Urological Association (AUA) published a white paper on the incidence, prevention, and treatment of complications related to PNB, including evidence-based recommendations to reduce infection rates following PNB [10]. Soon afterward, our institution implemented a new standardized algorithm to select antibiotic prophylaxis prior to PNB, using the recommendations proposed in the white paper. The aim of this initiative was to increase value in healthcare by reducing unnecessary exposure to antibiotics, which has medical, economic, and patient satisfaction implications. In this study, we sought to evaluate the impact of implementing these recommendations on the rate of infectious complications after PNB.
PATIENTS AND METHODS
Following institutional review board approval (IRB WA0601–11), we performed an observational cohort study analyzing data in our prospectively collected database to identify all men who underwent PNB for any indication at our tertiary care institution during 2 pre-specified 13-month periods. Cohort A included men who underwent PNB between January 1, 2011, and January 31, 2012 [11], and cohort B included those between January 1, 2014, and January 31, 2015. To assess whether there were differences between the two cohorts other than antibiotic regimen used, patient characteristics and comorbidities were compared between cohorts using Wilcoxon rank sum and Fisher’s exact tests.
All patients with symptoms of UTI, including new onset dysuria, frequency, or urgency, had a urine culture and urinalysis obtained within 2 weeks prior to the procedure; infections were treated with culture-specific antibiotics. A rectal enema was administered the morning of the procedure. TRUS-guided infiltration using 10mL of 1% lidocaine was performed near the neurovascular bundles and seminal vesicles in all patients. Our standard PNB template samples a total of 14 cores—including the apical, mid, basal, and transitional zone—using an 18-gauge needle. Additional targeted cores were sampled in the case of suspicious findings on multi-parametric magnetic resonance imaging (MRI) of the prostate. No rectal swabs were used in either cohort.
In cohort A, the choice of antimicrobial prophylaxis for PNB was at the discretion of the treating physician, and typically consisted of a 72-h course of antibiotics. Most commonly, an oral fluoroquinolone was given the evening before the procedure and continued for 3 days. Following the AUA Quality Improvement Summit on infectious complications of PNB, antimicrobial prophylaxis for PNB was standardized at our institution, and adhered to the recommendations of the Quality Improvement Summit (Online Resource 1) [10]. To effectively implement the antibiotic prophylaxis, nurses conducted a risk assessment based on a screening questionnaire (Table 1) and selected 1 of 4 single-antibiotic regimens using a standardized algorithm (Online Resource 2). The local antibiogram guided identification of fluoroquinolones as the first-line regimen. Therefore, patients in cohort B received a 24-hour course of risk-adapted, single-agent antibiotic prophylaxis.
Table 1.
Screening questionnaire for preventive risk assessment in cohort B.
| Question | Answer | Action |
|---|---|---|
| Do you have allergies to any antibiotics? | ||
| Yes, fluoroquinolones | Exclude ciprofloxacin | |
| Yes, penicillins or cephalosporins | Exclude cefuroxime and ceftriaxone | |
| Other | Exclude the listed antibiotic(s) | |
| Do you have a history of Achilles tendon injury or tendonitis? | ||
| Yes | Exclude ciprofloxacin | |
| Do you have any difficulty hearing? | ||
| Yes | Exclude gentamicin | |
| Have you been exposed to any antibiotics in the past 3 months? | ||
| Yes | Exclude the listed antibiotic(s) | |
| Did you have an infection requiring IV antibiotics or hospitalization after your last prostate biopsy? | ||
| Yes | Exclude the listed antibiotic(s) | |
| Are the blood or urine culture sensitivity results available? | ||
| Yes | Exclude the listed “resistant to” antibiotic(s) | |
| Yes, resistant to cefpodoxime, ceftazidime, aztreonam, cefotaxime, or ceftriaxone (ESBL) | Use imipenem | |
| Are you a hospital/nursing home employee or have you been hospitalized in the past 3 months? | ||
| Yes | Exclude ciprofloxacin | |
The primary objective was to determine whether the overall incidence of infectious complications after PNB was higher after standardizing antibiotic prophylaxis, in other words, whether the change to the shorter, risk-adapted regimen was associated with an increased infection rate. An infectious complication was defined as hospitalization for infection; bacteremia; symptomatic bacteriuria; or fever greater than 100.3 °F (37.9 °C) (considered infectious regardless of urine culture results). To identify and characterize infectious complications, each patient was contacted by a nurse within 14 days of the procedure and data on symptoms at presentation, urine and blood culture results, and antibiotic treatments were collected. For patients evaluated for symptoms of infection or hospitalized at outside institutions within 30 days, the medical records were obtained as part of usual care. Secondary objectives included reporting the total number of prophylactic antibiotic regimens used and the duration of antibiotics, which were extracted from the electronic medical record.
The difference in the rate of infectious complications between cohorts was calculated, using a 1-sided confidence interval (95% CI) to estimate the highest reasonable increase in infections associated with shorter antibiotic duration. Significance testing was 1-sided because the study was not adequately powered to detect a decrease in infection rates. An increase in post-biopsy infection rate of up to 1.5% was deemed clinically acceptable a priori based on the number needed to treat (67 patients would need to be treated with 72-hour course rather than 24-hour course antibiotics to prevent 1 infection). A permutation test was used to calculate the probability of this difference in rates based on the null hypothesis that the true rate of infectious complications was 1.5% higher in cohort B. The distribution of the difference in event rates across 10,000 simulations was used to calculate the probability of seeing the observed difference under the null.
The alpha level for statistical significance was 0.05. All statistical analyses were conducted using Stata 13 (StataCorp, College Station, TX).
RESULTS
Cohorts A and B included 584 and 654 men, respectively. Clinical and demographic characteristics of each cohort are summarized in Table 2. Men in cohort B showed higher detection rate of prostate cancer, frequency of Gleason 7 disease, and number of prior biopsies.
Table 2.
Baseline patient characteristics. Data are presented as median (quartiles) or frequency (%).
| Cohort A | Cohort B | p-value | |
|---|---|---|---|
| No. pts | 584 | 654 | |
| Median age at biopsy, years (IQR) | 64 (58, 69) | 64 (58, 69) | 0.5 |
| No. biopsy positive for prostate cancer (%) | 332 (57) | 431 (66) | 0.001 |
| No. biopsy Gleason score (n = 1237) | 0.001 | ||
| Negative | 252 (43) | 223 (34) | |
| ≤6 (%) | 174 (30) | 199 (30) | |
| 7 (%) | 124 (21) | 196 (30) | |
| 8–10 (%) | 34 (5.8) | 35 (5.4) | |
| No. prior biopsies | <0.0001 | ||
| 0 (%) | 92 (16) | 145 (22) | |
| 1 (%) | 279 (48) | 52 (8) | |
| 2 (%) | 117 (20) | 251 (38) | |
| 3 (%) | 96 (16) | 206 (31) | |
| Comorbid conditions (%) | |||
| Conditions related to infections | |||
| Urinary tract infection | 3 (0.5) | 10 (1.5) | 0.10 |
| Pyelonephritis | 0 (0) | 1 (0.2) | >0.9 |
| Prostatitis | 9 (1.5) | 7 (1.1) | 0.6 |
| Epididymitis | 4 (0.7) | 0 (0) | 0.049 |
| Sepsis | 1 (0.2) | 2 (0.3) | >0.9 |
| Lower urinary tract symptoms | 107 (18) | 239 (37) | <0.0001 |
| Diabetes | 49 (8.4) | 57 (8.7) | 0.9 |
| HIV/AIDS | 0 (0) | 2 (0.3) | 0.5 |
| Conditions unrelated to infections | |||
| Cardiovascular disease | 67 (11) | 105 (16) | 0.021 |
| Chronic obstructive pulmonary disease | 17 (2.9) | 9 (1.4) | 0.074 |
| Hypertension | 208 (36) | 253 (39) | 0.3 |
| High cholesterol | 220 (38) | 271 (41) | 0.2 |
| Cancer (excluding prostate) | 61 (10) | 75 (11) | 0.6 |
In cohort A, 19 different regimens were used for antibiotic prophylaxis. The most common regimen was single-agent fluoroquinolone (71%), followed by an augmented regimen of fluoroquinolone and aminoglycoside (20%) (Table 3). Overall, 93% of patients received a fluoroquinolone and 26% received an aminoglycoside as part of their antibiotic prophylaxis regimen. Although the majority of men (73%) received a single antibiotic, a significant proportion received an augmented regimen: 144 (25%) received a 2-drug regimen and 14 (2%) received a 3-drug regimen. Usual duration was 72 hours.
Table 3.
Prophylactic antibiotic regimens used in each cohort, by drug class. Data are presented as frequency (%).
| Prophylactic antibiotic regimen | No. in Cohort A | No. in Cohort B |
|---|---|---|
| Fluoroquinolone | 412 (71) | 484 (74) |
| Fluoroquinolone, aminoglycoside | 117 (20) | -- |
| Aminoglycoside | -- | 105 (16) |
| Cephalosporin | 3 (0.5) | 35 (5.4) |
| Culture-specific regimen | -- | 17 (2.6) |
| Carbapenem | -- | 13 (2.0) |
| Penicillin, aminoglycoside | 12 (2.1) | -- |
| Sulfamethoxazole | 6 (1.0) | -- |
| Sulfamethoxazole, aminoglycoside | 6 (1.0) | -- |
| Penicillin, aminoglycoside, fluoroquinolone | 4 (0.7) | -- |
| Clindamycin | 3 (0.5) | -- |
| Penicillin/clavulanic acid, aminoglycoside | 2 (0.3) | -- |
| Penicillin, aminoglycoside, Sulfamethoxazole | 2 (0.3) | -- |
| Metronidazole, aminoglycoside | 1 (0.2) | -- |
| Metronidazole, fluoroquinolone | 1 (0.2) | -- |
| Penicillin/clavulanic acid | 1 (0.2) | -- |
| Penicillin, cephalosporin | 1 (0.2) | -- |
| Penicillin/clavulanic acid, fluoroquinolone | 1 (0.2) | -- |
| Vancomycin, fluoroquinolone, aminoglycoside | 1 (0.2) | -- |
| Cephalosporin, fluoroquinolone | 1 (0.2) | -- |
| Cephalosporin, aminoglycoside | 1 (0.2) | -- |
| Unknown | 8 (1.4) | -- |
In cohort B, 97% of men received 1 of the 4 standardized antibiotic regimens for a duration of 24 hours. The majority (74%) received first-line fluoroquinolone in the form of ciprofloxacin (Table 3). Of 17 men (2.6%) who received a non-standardized, culture-specific regimen, 12 received an augmented regimen consisting of 2 antibiotics and 5 received a single agent. Overall, 97% of men adhered to the standardized prophylaxis and received a single-agent antibiotic. There was a significant reduction in the number of patients receiving two or more antibiotics following standardization (26% in cohort A vs 1.8% in cohort B, p<0.0001).
Infectious complications were observed in 3.3% (19 of 584 patients) in cohort A and 2.8% (18 of 654 patients) in cohort B. The difference in infectious complication rates was −0.5% (upper bound of one-sided 95% CI: 1.1%). Using a permutation approach, the p-value for the null hypothesis that the true difference in rates is a 1.5% higher infection rate in cohort B was calculated to be 0.037. Although more men in cohort B reported having higher incidence of baseline lower urinary tract symptoms compared to those in cohort A (18% in cohort A vs 37% in cohort B, p<0.0001), this did not translate to a higher infectious complication rate following the biopsy procedures.
Among the 19 patients who developed infections in cohort A, 7 were found to have E. coli infections (5 with ciprofloxacin-resistant E. coli and 2 with pan-resistant extended-spectrum beta lactamase (ESBL)-producing E. coli) and 1 patient was found to have gentamicin-resistant enterococcus. Blood or urine culture results were negative in the remaining 11 patients.
Blood or urine culture results were available for 15 of 18 patients who developed an infection in cohort B. Twelve patients developed an E. coli infection, including 8 with pan-resistant E. coli, 1 with ampicillin-resistant E. coli, and 3 with pan-sensitive E. coli. One patient was found to have a pan-resistant coagulase-negative Staphylococcus infection. One patient developed a fever but had a negative culture. Five of these patients received prophylactic ciprofloxacin but were later found to have ciprofloxacin- and gentamicin-resistant E. coli infections.
DISCUSSION
In this validation study, we confirmed that implementing the 2014 AUA recommendations for antibiotic prophylaxis for PNB at our institution was associated with a reduction in the number and duration of antibiotic regimens used as well as a reduction in the use of multidrug regimens. We rejected the null hypothesis that the new approach was associated with a 1.5% or greater increase in infection rate; the infection rate was in fact non-significantly lower after antibiotic standardization. The cohorts showed difference in prostate cancer detection rate, Gleason score, and the number of prior biopsies. A possible explanation for this finding is that Cohort B contained more patients on active surveillance protocol compared to Cohort A. Despite the shorter duration of therapy, reduced number of antimicrobial agents used, and higher number of prior biopsies, patients in Cohort B did not experience a higher rate of infectious complications following PNB. Our results confirm findings from several randomized controlled trials [12–15], thus providing further evidence supporting the adoption of such recommendations. Importantly, antibiotic regimen choice was directed by a preventive risk assessment conducted by nursing, and it did not require rectal swabs or fecal culture to direct prophylaxis.
Although we consider these results to be sufficient evidence to support the continued implementation of the recommendations included in the 2014 AUA white paper on infectious complications of PNB, there is room for improvement, as the rate of infectious complications is non-negligible. Several proposed strategies include rectal cleansing and disinfection, detersion of biopsy needles with povidone-iodine or formalin, augmented antimicrobial prophylaxis using broad-spectrum antimicrobials or a combination of antibiotics of different classes instead of a standardized single-drug regimen, rectal swabs followed by culture-specific antibiotic therapy, and changing the approach from transrectal to transperineal PNB. Rectal cleansing and disinfectant enemas or suppositories are controversial. The majority of studies have failed to demonstrate a significant decrease in the rate of infectious complications [16–17]. Inclusion of rectal enemas in our pre-biopsy routine is primarily aimed at improving prostate visualization during transrectal ultrasound rather than infection control. Evidence to support disinfecting the needle before using it again in the same patient has been inconclusive. Using a broad-spectrum antibiotic for prophylaxis may not necessarily reduce the rate of infections [18] and may ultimately lead to increased resistance to broad-spectrum antibiotics. Additionally, although the transperineal PNB approach and targeted prophylaxis after rectal swab have been associated with a decrease in the rate of infectious complications, they could result in a significant increase in healthcare costs if implemented universally. Two recent studies—a systematic review of retrospective and prospective cohort studies and a multi-institutional observational study [19–20]— showed that targeted antimicrobial prophylaxis determined by rectal swab culture susceptibilities resulted in a decreased use of broad-spectrum empirical antibiotics without increasing the rate of sepsis. However, the applicability and cost-effectiveness of such a strategy should also be evaluated locally based on the costs associated with rectal swabs and cultures and the number of infectious complications avoided when compared to empirical antibiotic prophylaxis [21].
Recent refinements to PNB technique, including the use of MRI-targeted biopsies, resulted in longer procedures and an increased number of cores collected in cohort B compared to cohort A, which may have represented unmeasured confounders of our study. We also acknowledge that, since our objective was to estimate the impact of implementing the recommendations from the AUA white paper in an outpatient clinical setting rather than investigating risk factors for infection after PNB, no adjustment was made in our retrospective validation study for known risk factors for infection following PNB. While we did not perform an a priori sample size calculation, we used biopsy data from all patients undergoing PNB during each time period, and the confidence interval was narrow enough to exclude our pre-defined benchmark for a clinically relevant increase in infection rates (1.5%).
The findings of our study validate the recommendations of the 2014 AUA white paper on infectious complications of transrectal PNB. Implementation of the recommendations at our institution did not result in an increased rate of infectious complications, despite a reduction in the number of prophylactic antibiotic regimens from 19 to 4, and a reduction of their duration from 72 hours to less than 24 hours.
CONCLUSION
A risk-adapted approach to antimicrobial prophylaxis is an effective strategy to minimize the development of antibiotic resistance, while preventing infectious complications following PNB. The relatively low overall rate of these complications mandates a multi-institutional approach for adequate power. The integration of additional strategies aimed at the reduction of infectious complications after PNB should be the focus of continued research.
Supplementary Material
Acknowledgments
FUNDING
This research was supported by funds from the Sidney Kimmel Center for Prostate and Urologic Diseases and NIH Cancer Center Support Grant P30 CA008748.
Footnotes
CONFLICT OF INTEREST: The authors declare that they have no conflict of interest.
ETHICAL APPROVAL: All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
INFORMED CONSENT: Informed consent was obtained from all individual participants included in the study.
Publisher's Disclaimer: This Author Accepted Manuscript is a PDF file of an unedited peer-reviewed manuscript that has been accepted for publication but has not been copyedited or corrected. The official version of record that is published in the journal is kept up to date and so may therefore differ from this version.
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