Abstract

Fiducial markers placed in the prostate prior to treatment planning are often used in image guided radiation therapy to optimize beam alignment. A potential serious complication following fiducial marker placement or prostate biopsy is a bacterial urinary tract infection, particularly urosepsis, which requires hospitalization and aggressive antibiotic therapy. Patients usually undergo either procedure transrectally under ultrasound guidance and routinely receive antibiotic prophylaxis before and after the procedure, usually with fluoroquinolones (FQ), to reduce the risk of infection. There are few data pertaining to the risk of post fiducial marker placement infection so that most data pertain to post-biopsy bacterial urinary tract infection which has been increasing in recent years, primarily due to FQ-resistant gram-negative bacilli, usually Escherichia coli (E. coli). Strategies to reduce the risk of infection include empirically changing the prophylactic antibiotic regimen to include agents to which FQ-resistant bacteria are likely sensitive, obtaining a rectal swab culture prior to the procedure and tailoring the regimen based on the results of the sensitivity profile, and performing the procedure via the transperineal rather than the transrectal route. The transperineal route often requires more anesthesia and time and is thus more impractical to implement. Additionally, the data do not convincingly demonstrate an advantage associated with the transperineal route. A caveat is that most of the relevant data are from a time period when the risk of a bacterial urinary tract infection was probably lower. Thus the rectal swab cultures and targeted prophylaxis is likely the optimal strategy.

Introduction

Fiducial markers are often placed in the prostate prior to image guided radiation therapy (RT) to optimize beam alignment [16]. A potentially serious complication following transrectal ultrasound-guided fiducial marker placement is a bacterial urinary tract infection (UTI). A subset of these infections result in urosepsis, which requires hospitalization and may be life-threatening. There are few data pertaining to the risk of this complication so that most data relate to patients who undergo a transrectal ultrasound guided prostate biopsy (TRUSPB) [726]. Although the transperineal route is an option, the transrectal route is usually preferred because it requires less anesthesia and is more convenient [1, 27, 28]. Patients almost always undergo a course of antibiotic prophylaxis prior to, and following, the procedure to reduce the risk of a bacterial UTI. The antibiotics of choice are fluoroquinolones (FQ). The incidence of urosepsis due to FQ-resistant bacteria, primarily Escherichia coli (E. coli) has been increasing over the last few years likely due to antimicrobial resistance rather than virulence genotype [24, 25].

The aim of this paper is to review the incidence of bacterial UTIs after fiducial marker placement or TRUSPB, the factors associated with an increased likelihood of this complication, and to discuss how to reduce the risk of this adverse event. Because there are few data pertaining to fiducial marker placement, most of the discussion will focus on post prostate biopsy bacterial infections.

Incidence of Bacterial Urinary Tract Infection following Transrectal Fiducial Marker Placement or Prostate Biopsy

Sanders and Buchan reported on 1421 patients who underwent TRUSPB in Christchurch Hospital (New Zealand) between 2010 and 2011 [29]. All patients received prophylactic antibiotics with ciprofloxacin (cipro) 250 mg orally (PO) twice daily (BID) for 4 days starting 2 hours before the procedure unless there was a history of a prior adverse reaction. Forty patients (2.8%) required hospitalization to Christchurch Hospital at the median of 2 days after biopsy for a bacterial infection; the median hospital stay was 3 days. Midstream urine culture was positive in 26 patients (65%), primarily for E. coli (23 patients). Thirty-eight patients had blood cultures and 20 (53%) were positive, the majority (16 patients) for E. coli. A urine and/or blood culture, positive for E. coli, was obtained in 27 patients which was resistant to amoxicillin in 82% and to FQ in 52%. A combination of gentamicin and ceftriaxone was the most effects regime for the E. coli cultured.

Carignan et al [30] reported on 5798 patients who underwent TRUSPB at the Université de Sherbrooke (Quebec, Canada) between 2002 and 2011. All patients underwent routine antibiotic prophylaxis with cipro in conjunction with biopsy. Forty-eight patients (0.83%) developed urinary sepsis. The rate of urinary infections increased from 0.52 per 100 biopsies during 2002 to 2009 to 2.15 per 100 biopsies in 2010 to 2011 (p<0.001). E. coli was the predominant pathogen and was identified in 75% of patients with UTIs. Independent risk factors for post-biopsy infection included diabetes, hospitalization during the preceding month, chronic obstructive pulmonary disease, and biopsy during 2010 to 2011.

Campeggi et al [31] reported on 3000 patients who underwent a 21-core TRUSPB between 2006 and 2009 at the Henri Mondor Hospital (Créteil, France). All patients received a 7 day course of FQ prophylaxis. Twenty patients (0.67%) developed a bacterial prostatitis requiring hospitalization within roughly 2.9 days (range, 1 to 7 days). E. coli was isolated in all 20 patients; 95% were resistant to FQ and amoxicillin. Resistance was also detected as follows: amoxiclav (70%), trimethoprim sulfamethoxazole (70%), 3rd generation cephalosporins (25%), and amikacin (5%). None were resistant to imipenem.

Ehdaie et al [32] reported on 403 patients on active surveillance for prostate cancer who underwent a 14-core TRUSPB between January 2011 and January 2012 at the Memorial Sloan-Kettering Cancer Center (New York, NY, USA). Prophylactic FQ antibiotics were given to 92% of patients and intramuscular (IM) gentamicin was administered to 28%. Fourteen patients (3.5%) developed a bacterial infection; 13 patients required hospitalization. Five patients had positive urine cultures, 4 of the 5 had FQ-resistant bacteria. Factors potentially impacting the probability of developing a bacterial UTI were analyzed and included diabetes mellitus, benign prostatic hypertrophy, antibiotic regimen, and the number of prior prostate biopsies. Only the number of prior TRUSPBs significantly increased the risk of infection which was 1.3 times higher for every prior biopsy.

Patel et al [33] reported on 316 patients who underwent a TRUSPB at The Prostate Centre (London, UK) between June 2008 and June 2010. Antibiotic prophylaxis consisted of cipro 500 mg BID for 5 days starting 24 hours before the biopsy and gentamicin 120 mg to 160 mg intravenously (IV) and metronidazole suppository 1 g immediately before the biopsy. Sixteen patients (5%) developed a bacterial infection necessitating hospitalization. Cultures were positive in 10 of 16 patients (63%), all with E. coli that was resistant to cipro and amoxicillin and variably to gentamicin and co-amoxiclav. Nearly all were sensitive to meropenem. Both recent travel (p=0.04) and antibiotic use within 4 weeks (p=0.025) were associated with an increased risk of infection unrelated to the country visited or the type of antibiotic used.

Williamson et al [34] evaluated all male patients (N=258) admitted to the Auckland City Hospital (New Zealand) between 2006 and 2010 with community onset E. coli bacterium and compared those having undergone a recent TRUSPB with the remaining patients. Forty-seven of 258 patients (18%) were admitted after a recent TRUSPB and were twice as likely to require admission to the intensive care unit (25% vs 12%) and to have a higher rate of resistance to gentamicin (43%), trimethoprim sulfamethoxazole (60%) and cipro (62%), as well as all 3 agents in combination (19%).

The incidence of bacterial UTI after TRUSPB is summarized in Table 1.

Table 1.

Incidence of bacterial UTI after prostate biopsy.

Incidence of bacterial UTI after prostate biopsy.
Incidence of bacterial UTI after prostate biopsy.

Berglund et al [35] reported on 50 consecutive patients who underwent Calypso® transducer placement (Varian Medical Systems, Palo Alto, CA) prior to RT at the Cleveland Clinic (Cleveland, OH, USA) between February 2008 and October 2010. Patients received a 3-day course of cipro 500 mg PO BID starting the night before the procedure. Five of 50 patients (10%) developed a bacterial infection including grade 2 UTI (3 patients), grade 3 epidural abscess and osteomyelitis requiring open debridement and lumbar fusion (1 patient), and a methicillin-resistant Staphylococcus aureus (S. aureus) prostate abscess (1 patient). Culture identified the responsible bacteria in 4 of 5 patients; 3 of 4 had FQ-resistant E. coli.

Langenhuijsen et al [36] reported on 209 patients who underwent transrectal ultrasound (US) guided placement of 4 gold fiducial markers prior to image guided RT (IGRT) at Radboud University Nijmegen Medical Centre (Nijmegen, The Netherlands) between 2001 and 2005. Patients received cipro 500 mg BID for 3 days beginning the day prior to the procedure. Four patients (1.9%) developed a fever that responded to additional antibiotics. Igdem et al [37] reported on 135 patients who underwent transrectal US guided placement of 3 gold fiducial markers prior to intensity modulated RT (IMRT) at Istanbul Bilim University (Istanbul, Turkey) between 2005 and 2008. Patients received cipro 500 mg BID for 3 days beginning the day of the procedure. Three patients (2.2%) developed a bacterial UTI documented by urine culture and were successfully treated with additional antibiotics. No patient required hospitalization. Linden et al [38] reported on 98 patients who US guided transrectal placement of 3 gold fiducial markers prior to IMRT at the Thomas Jefferson University (Philadelphia, PA) between 2003 and 2006. Patients received prophylactic oral antibiotics, usually with quinolones, for 2 days beginning the day before the procedure. No patient experienced a bacterial UTI. Brown et al [39] reported on 20 patients who underwent transrectal US guided placement of 3 gold fiducial markers prior to image IGRT beginning in 2007 at the Princess Alexandra Hospital (Brisbane, Australia). Patients received prophylactic trimethoprim antibiotics. One patient (5%) developed a bacterial UTI. Thompson et al [40] reported on 28 patients who underwent transrectal US guided placement of 2 to 5 gold fiducial markers prior to IGRT at the Peter MacCallum Cancer Center (Melbourne, Australia) in 2007. Patients received prophylactic cipro. No patient developed sepsis or required hospitalization. Yang et al [41] reported on 16 patients who underwent transrectal US guided placement of a minimum of 3 gold fiducial markers prior to IMRT at the University of Miami between 2007 and 2008. Patients received IV cipro the day of the procedure and then orally for 5 days thereafter. No patient experienced a bacterial UTI. Kably et al [42] subsequently reported on 75 patients who underwent transrectal US guided gold fiducial marker placement prior to IGRT at the University of Miami between 2010 and 2013. Seventy-two patients were previously untreated, 2 had a local recurrence after prostatectomy, and 1 had a local recurrence after cryotherapy. Patients received a 3 day course of oral cipro beginning the day before the procedure. Two patients (2.7%) developed a bacterial UTI; 1 of 2 required hospitalization due to E. coli sepsis that was resistant to cipro, levaquin, and ampicillin.

The incidence of bacterial UTIs after transrectal placement of fiducials is summarized in Table 2.

Table 2.

Incidence of bacterial UTI after transrectal fiducials.

Incidence of bacterial UTI after transrectal fiducials.
Incidence of bacterial UTI after transrectal fiducials.

Thus the incidence of post TRUSPB appears to be increasing primarily due to an increasing incidence of multidrug resistant E. coli which may be more virulent than other community onset E. coli infections [4348]. Some patients may be at an increased risk for developing a post-biopsy bacterial UTI, such as those having undergone a recent prostate biopsy and/or a history of recent antibiotic use. Limited data suggest that the risk of post transrectal fiducial marker placement may be similar to that observed after TRUSPB, which is not surprising given that essentially all of these patients have undergone a recent prostate biopsy with antibiotic prophylaxis.

Strategies to Reduce the Risk of Post-Procedure Bacterial Urinary Tract Infection

Strategies to reduce the risk of post-procedure bacterial UTI can be broadly stratified into empiric changes in the prophylactic regimen, directed changes in the prophylactic regimen based on rectal swab cultures, and changing the procedure route from transrectal to transperineal [28, 44, 45, 4869]. Essentially all of these data pertain to patients who have undergone a TRUSPB so that the results must be extrapolated to those undergoing fiducial marker placement prior to IGRT.

Empiric Changes in the Prophylactic Regimen

AbuGhosh et al [49] reported on 865 patients who underwent TRUSPB at the University of British Columbia (Vancouver, Canada) between 2009 and 2011. All patients received cipro prophylaxis and had a prebiopsy rectal swab culture. Patients were randomized to rectal cleansing with povidone-iodine (421 patients) or no cleansing (444 patients). Infections were defined as fever >38.0°C, UTI, or sepsis. Infections were observed in 31 patients (3.5%), including 11 (2.6%) who received rectal cleansing versus 20 (4.5%) controls (p=0.15). Sepsis was observed in 4 patients (1.0%) who received povidone-iodine versus 7 controls (1.6%; p=0.55). Multivariate analysis revealed that cipro-resistant bacteria detected on rectal swab cultures (p=0.002) and a history of taking cipro within 3 months of biopsy (p=0.009) predicted infection. Although rectal cleansing with povidone-iodine reduced the risk of bacterial infection by 42%, the risk reduction was not statistically significant.

Adibi et al [50] reported on 600 patients who underwent a TRUSPB at the University of Texas Southwestern (Dallas, TX, USA) between January 2010 and December 2011. Between January 2010 and December 2010, 290 patients received a standard prophylactic regimen of cipro for 3 days unless allergic in which a 3-day course of Bactrim DS was employed. From January 2011 to December 2011, gentamicin 80 mg IM was added to the standard prophylactic antibiotic regimen. Eleven of 290 patients (3.8%) required hospitalization for a bacterial UTI after standard prophylaxis compared with 2 of 310 patients (0.6%) who underwent the augmented prophylactic regimen (p<0.001). Of the 11 patients admitted after standard prophylaxis, 73% had a FQ-resistant E. coli UTI and only 9% had bacteria resistant to gentamicin.

Chan et al [51] reported on 367 patients who underwent a TRUSPB at the Chinese University of Hong Kong between November 2007 and July 2009 and were randomized into 2 prophylactic antibiotic regimens: (1) Group A (179 patients), amoxicillin-clavulanate 1 g 2 hours before biopsy and then every 12 hours times 2 and (2) Group B (188 patients), amoxicillin as above plus cipro 250 mg 2 hours before biopsy and then every 12 hours times 2 after the biopsy. In Group A, 7 of 179 patients (3.91%) developed a bacterial UTI compared with 1 of 188 patients (0.53%) in Group B (p=0.008). Five of 8 patients who developed a bacterial UTI required hospitalization.

Manecksha et al [52] reported on 1183 patients who underwent TRUSPB at the Adelaide and Meath Hospital (Dublin, Ireland) between January 2008 and December 2009. Patients biopsied in 2008 (Group A, 558 patients) received ofloxacin 400 mg immediately before biopsy followed by 200 mg every 12 hours for 3 days whereas those biopsied in 2009 (Group B, 625 patients) received ofloxacin 200 mg every 12 hours for 3 days starting 24 hours before the biopsy. In Group A, 20 of 558 patients (3.6%) developed a bacterial UTI compared with 10 of 625 patients (1.6%) in Group B (p=0.03). E. coli was the most frequently isolated organism. Overall, 7 of 13 positive urine cultures (54%) were FQ resistant and 5 of 13 (40%) were multidrug resistant. All patients with positive cultures had organisms sensitive to meropenem.

Madden et al [55] reported on 709 patients who underwent a TRUSPB between 2008 and 2009 at Cambridge University Hospitals (UK). Cipro prophylaxis was initially employed in 454 patients and 11 (2.4%) developed a bacterial UTI. The prophylactic regimen was changed to co-amoxiclav and gentamicin and 33 of 255 patients (12.9%) developed a bacterial UTI. The prophylactic regimen was switched back to cipro with a subsequent decrease in the likelihood of bacterial UTI.

Batura et al [58] reported on 871 patients who underwent TRUSPB at Northwick Park Hospital (London, UK) between 2006 and 2008; antibiotic prophylaxis varied over the study period. Prior to 2007, the regimen consisted of cipro 500 mg PO BID for 5 days starting 2 days before biopsy, co-amoxiclav 1.2 g IV immediately before biopsy and 625 mg PO three times daily after biopsy, and metronidazole suppository 500 mg after biopsy. Fourteen of 281 patients (4.9%) developed a bacterial UTI, 7 patients (2.5%) became septic, and 13 of 14 were cipro resistant. After 2006, the prophylactic regimen was switched to cipro 500 mg PO BID for 5 days beginning 2 days before biopsy, co-amoxiclav 625 mg PO 3 times daily for 5 days beginning 2 days before biopsy, and amikacin 1 g IV immediately before biopsy. The PO co-amoxiclav was discontinued after August 2008. After 2006, 8 of 590 patients (1.4%) developed a bacterial UTI (p=0.02) and 2 patients (0.3%) became septic (p=0.002).

Lorber et al [62] reported on 4655 patients who underwent TRUSPB at Hadassah-Hebrew University between 2001 and 2012. All patients received a 3-day course of cipro or oxfloxacin; after 2007 an increasing dose of gentamicin IM was included in the prophylactic regimen. One hundred ten patients (2.4%) required hospitalization for urosepsis; 90 of 110 (82%) had positive blood and/or urine cultures. Of these, 86% were positive for E. coli which was FQ resistant. The following rates of urosepsis were observed: oxfloxacin, 3.6%; oxfloxacin plus gentamicin 80 mg, 3.5% (p=1.0); oxfloxacin plus gentamicin 160 mg, 2.7% (p=0.27); and oxfloxacin plus gentamicin 240 mg, 0.6% (p=0.04).

Issa et al [68] reported on 1642 patients who underwent a TRUSPB at Emory University (Atlanta, GA, USA) between 2008 and 2012. All had a negative urine culture, a bisacodyl enema, and a 3-day course of FQ antibiotics. Prior to each core, the needle was placed in 10% formalin. Five patients (0.3%) had a mild uncomplicated UTI and 2 patients were hospitalized for sepsis with blood and urine cultures positive for FQ-resistant E. coli. Compared with historical controls, the use of 10% formalin resulted in reduction of bacterial UTIs from 0.8% to 0.3% (p=0.13).

Rectal Swab and Culture

Series where rectal swab cultures were obtained prior to the procedure can be stratified into those where the antibiotic prophylactic regimen was not altered based on the results and those where it was tailored based on the culture and sensitivity profile.

Steensels et al [44] reported on 342 patients who underwent rectal swab/cultures prior to TRUSPB between 2009 and 2010. Patients were excluded if the cultures were negative, had no antibiotic prophylaxis, or antibiotics other than FQ. Of the remaining 236 patients, 52 (22%) had cipro resistant E. coli. Seven of 236 patients (3.0%) developed bacterial UTIs, all with cipro resistant E. coli. By comparison, no patient with a rectal swab culture revealing cipro sensitive organisms developed a bacterial UTI (p<0.01).

Minamida et al [45] reported on 100 patients who had a rectal swab culture prior to TRUSPB between April and December 2010 at the Kitasato University Hospital (Kanagawa, Japan). Antibiotic prophylaxis consisted of levofloxacin (levaquin) 500 mg PO QD for 3 days beginning 2 hours before biopsy. Thirteen patients (13%) had cultures positive for FQ-resistant E. coli; 4 of 13 (31%) had a bacterial UTI compared with 0 of 87 patients with cultures revealing FQ sensitive organisms (p<0.01).

Liss et al [57] reported on 136 patients who underwent rectal swab cultures prior to TRUSPB at the University of California, Irvine, (Irvine, CA, USA) between January 2009 and March 2010. Thirty patients (22%) had cultures positive for FQ-resistant E. coli. Cultures of 29 patients with FQ-resistant E. coli revealed them to be susceptible to the following antibiotics: amikacin, 100%; cefazolin, 79%; ceftazidime, 93%; cefepime, 93%; impenem, 100%; nitrofuratoin, 100%; piperacillin-tazobactam, 90%; gentamicin, 66%; and trimethoprim-sulfamethoxazole, 62%.

Qi et al [66] reported on 991 patients who underwent a rectal swab culture followed by TRUSPB at Northwestern University (Chicago, IL, USA) between July 2010 and September 2011. Cipro resistant organisms were detected in 193 patients (19.4%); 167 of 193 (87%) were E. coli. Taylor et al [69] reported on 865 patients who underwent TRUSPB at the University of British Columbia between 2009 and 2011. All had prebiopsy urine and rectal swab cultures and a post-biopsy urine culture. Cipro resistant gram-negative coliforms were detected in 19% of rectal cultures; E. coli was the most prevalent gram-negative rectal isolate (80.9%) and accounted for 90.6% of cipro resistance.

Liss et al [64] reported on 58 patients who underwent TRUSPB at the University of California, Irvine (Irvine, CA, USA); rectal cultures were obtained a median of 2 weeks before biopsy and again just prior to biopsy to detect FQ-resistant organisms. Fifty-four of 58 pairs (93%) of rectal cultures were concordant. Overall, sensitivity was 95.9%, specificity was 77.8%, negative predictive value was 95.9%, and positive predictive value was 77.8%.

Taylor et al [54] reported on 457 patients who underwent TRUSPB at Northwestern University between July 2010 and March 2011. Standard cipro prophylaxis without a rectal swab culture was employed in 345 patients (76%); rectal swab cultures to detect FQ-resistant bacteria were obtained prior to biopsy in 112 patients and those with FQ-resistant bacteria received targeted prophylaxis. Twenty-two of 112 patients (19.6%) had FQ-resistant organisms; none developed a bacterial UTI. Nine of 345 patients (2.6%) who received standard prophylaxis developed a bacterial UTI including 1 patient who developed sepsis (p=0.12). Seven of 9 had FQ-resistant bacteria. The authors estimated that it would be necessary for 38 patients to undergo rectal swab cultures prior to TRUSPB to avoid 1 bacterial UTI.

Duplessis et al [53] reported on 235 patients who underwent rectal swab cultures prior to TRUSPB between March 2010 and March 2011 and had their antibiotic prophylaxis customized based on the results. Thirty-two patients (14%) had FQ-resistant E. coli. No patient developed a post-biopsy infection. In contrast, 3 of 103 patient (2.9%) biopsies in the 4 months prior to routinely obtaining a rectal swab culture developed a post-biopsy bacterial UTI.

Transperineal versus Transrectal Route

Pinkstaff et al [59] reported on 210 patients who underwent transperineal prostate biopsy at the Mayo Clinic Jacksonville between 1999 and 2003. All patients had 1 or more prior biopsies; the mean number of cores obtained was 21.2 (range, 12 to 41). All patients had a 3 day peri-operative course of antibiotics, usually with FQ. Twenty-four patients (11%) developed post-biopsy urinary retention; no patient experienced a bacterial UTI.

Miller et al [28] reported on 197 prostate biopsies in 178 patients at the Nambour General Hospital (Nambour, Australia) between 1996 and 2001. Eighty-one transperineal biopsies were obtained in 75 patients and 116 transrectal biopsies in 103 patients. Patients who received transperineal biopsies did not receive antibiotic prophylaxis whereas those who underwent transrectal biopsies usually had IV gentamicin prior to the procedure and 3 to 5 days of trimethoprim post-biopsy. Overall, complications were observed in 22.2% after transperineal biopsy versus 19.8% after transrectal biopsy (p=0.773). Sepsis was observed in 1.2% after transperineal biopsy compared with 0% after transrectal biopsy (p=0.411).

Hara et al [27] reported on 246 patients who underwent a 12-core prostate biopsy at the Kawasaki Medical School (Kawasaki, Japan) between May 2003 and October 2005. Patients were randomized to receive either a transperineal biopsy (126 patients) or a transrectal biopsy (120 patients). All patients received levaquin 200 mg on the day of the biopsy. The rate of prostate cancer detection was 42.1% after transperineal biopsy compared with 48.3% after transrectal biopsy (p=0.323). Bacterial UTI did not occur in any patient after a transperineal biopsy versus 2 of 120 patients (1.7%) after transrectal biopsy.

Takenaka et al [63] reported on 200 patients who underwent a prostate biopsy at Kobe University and the Kawasaki Medical School between May 2003 and September 2004. Patients were randomized to transperineal biopsy (100 patients) or transrectal biopsy (100 patients). No patient had undergone a previous prostate biopsy. All patients received antibiotic prophylaxis for 1 day with 300 mg of levaquin. The prostate cancer detection rate was 47% after transperineal biopsy and 53% after transrectal biopsy (p=0.48). There was no difference in the overall rate of complications or the risk of bacterial UTI after transperineal biopsy (19% and 1%) compared with transrectal (20% and 2%) biopsy.

Pepe and Aragona [67] reported on 4000 patients who underwent transperineal prostate biopsy at Cannizzaro Hospital (Catania, Italy) between 1991 and 2012. Six cores were obtained in 612 patients, 12 cores in 1428 patients, 18 cores in 1330 patients, and >24 cores in the remainder. All patients received antibiotic prophylaxis with levaquin 500 mg QD for 3 days beginning the day before the procedure. Infectious complications included UTI, 2.5%; prostatitis, 0.7%; and sepsis, 0%.

Vyas et al [70] reported on 634 patients who underwent a transperineal prostate biopsy at Guy's Hospital (London, United Kingdom) between 2007 and 2011. The procedure was usually performed under general anesthesia; 24 to 38 cores were obtained. Antibiotic prophylaxis consisted of Amikacin 500 mg IV at induction followed by cipro 500 mg twice daily for 3 days. Postoperative urinary retention was observed in 11 patients (1.7%); 2 patients required hospitalization for peri-urethral bleeding. No patients developed urosepsis.

Conclusions

The risk of a bacterial UTI following TRUSPB is rising due to an increasing incidence of antibiotic resistant organisms, particularly FQ-resistant E. coli. Similar risks likely exist after transrectal placement of fiducial markers for target localization prior to RT. Patients who have had fiducial markers placed are all probably at high risk because all have had at least one prostate biopsy that was likely performed with antibiotic prophylaxis. Three general strategies exist to reduce this risk: (1) empirically changing the antibiotic prophylaxis, (2) rectal swab culture and targeted antibiotic prophylaxis, and (3) using the transperineal rather than the transrectal route. One of the problems with assessing the efficacy of these strategies is that series including patients who have undergone these procedures as recently as the early 2000s likely had a lower risk of resistant bacteria compared with patients undergoing the procedure today. This is particularly pertinent when comparing the transperineal route to the transrectal route. While there is understandable resistance to change, continuing routine FQ prophylaxis will likely result in an increasing risk of potentially severe urosepsis. The disadvantage of rectal swab culture is that it must be obtained far enough in advance of the procedure to obtain the results to change the prophylactic regimen if necessary. However, if obtained in advance, the antibiotic prophylaxis can be targeted based on the culture and sensitivity results. The disadvantage with the transperineal route is that it may require additional anesthesia and time and is thus more difficult to implement. The advantage of the transperineal approach is that the rectal bacterial flora are avoided and routine antibiotic prophylaxis, which would further increase the development of resistant organisms, might be avoided as well. However, the available data do not convincingly demonstrate an advantage associated with the transperineal route. Thus, rectal swab culture and targeted antibiotic prophylaxis is probably the best alternative.

ADDITIONAL INFORMATION AND DECLARATIONS

Conflicts of Interest Disclosure: The authors have no conflicts to disclose.

Acknowledgments: The authors thank Dr. Roger O'Bryan for his contributions and the Editorial Staff at the University of Florida, Department of Radiation Oncology.

References

References
1
Shen
PF
,
Zhu
YC
,
Wei
WR
,
Li
YZ
,
Yang
J
,
Li
YT
,
Li
DM
,
Wang
J
,
Zeng
H
.
The results of transperineal versus transrectal prostate biopsy: a systematic review and meta-analysis
.
Asian J Androl
.
2012
;
14
:
310
5
.
2
Skarsgard
D
,
Cadman
P
,
El-Gayed
A
,
Pearcey
R
,
Tai
P
,
Pervez
N
,
Wu
J
.
Planning target volume margins for prostate radiotherapy using daily electronic portal imaging and implanted fiducial markers
.
Radiat Oncol
.
2010
;
5
:
52
.
3
Susil
RC
,
Menard
C
,
Krieger
A
,
Coleman
JA
,
Camphausen
K
,
Choyke
P
,
Fichtinger
G
,
Whitcomb
LL
,
Coleman
CN
,
Atalar
E
.
Transrectal prostate biopsy and fiducial marker placement in a standard 1.5T magnetic resonance imaging scanner
.
J Urol
.
2006
;
175
:
113
20
.
4
Mendenhall
NP
,
Hoppe
BS
,
Nichols
RC
,
Mendenhall
WM
,
Morris
CG
,
Li
Z
,
Su
Z
,
Williams
CR
,
Costa
J
,
Henderson
RH
.
Five-year outcomes from 3 prospective trials of image-guided proton therapy for prostate cancer
.
Int J Radiat Oncol Biol Phys
.
2014
;
88
:
596
602
.
5
Huisman
HJ
,
Futterer
JJ
,
van Lin
EN
,
Welmers
A
,
Scheenen
TW
,
van Dalen
JA
,
Visser
AG
,
Witjes
JA
,
Barentsz
JO
.
Prostate cancer: precision of integrating functional MR imaging with radiation therapy treatment by using fiducial gold markers
.
Radiology
.
2005
;
236
:
311
7
.
6
Wu
J
,
Haycocks
T
,
Alasti
H
,
Ottewell
G
,
Middlemiss
N
,
Abdolell
M
,
Warde
P
,
Toi
A
,
Catton
C
.
Positioning errors and prostate motion during conformal prostate radiotherapy using on-line isocentre set-up verification and implanted prostate markers
.
Radiother Oncol
.
2001
;
61
:
127
33
.
7
Abdollah
F
,
Novara
G
,
Briganti
A
,
Scattoni
V
,
Raber
M
,
Roscigno
M
,
Suardi
N
,
Gallina
A
,
Artibani
W
,
Ficarra
V
,
Cestari
A
,
Guazzoni
G
,
Rigatti
P
,
Montorsi
F
.
Trans-rectal versus trans-perineal saturation rebiopsy of the prostate: is there a difference in cancer detection rate?
Urology
.
2011
;
77
:
921
5
.
8
Akduman
B
,
Akduman
D
,
Tokgoz
H
,
Erol
B
,
Turker
T
,
Ayoglu
F
,
Mungan
NA
.
Long-term fluoroquinolone use before the prostate biopsy may increase the risk of sepsis caused by resistant microorganisms
.
Urology
.
2011
;
78
:
250
5
.
9
Chang
DT
,
Challacombe
B
,
Lawrentschuk
N
.
Transperineal biopsy of the prostate–is this the future?
Nat Rev Urol
.
2013
;
10
:
690
702
.
10
Dumford
D
, 3rd,
Suwantarat
N
,
Bhasker
V
,
Kundrapu
S
,
Zabarsky
TF
,
Drawz
P
,
Zhu
H
,
Donskey
CJ
.
Outbreak of fluoroquinolone-resistant Escherichia coli infections after transrectal ultrasound-guided biopsy of the prostate
.
Infect Control Hosp Epidemiol
.
2013
;
34
:
269
73
.
11
Ekici
S
,
Cengiz
M
,
Turan
G
,
Alis
EE
.
Fluoroquinolone-resistant acute prostatitis requiring hospitalization after transrectal prostate biopsy: effect of previous fluoroquinolone use as prophylaxis or long-term treatment
.
Int Urol Nephrol
.
2012
;
44
:
19
27
.
12
Emiliozzi
P
,
Corsetti
A
,
Tassi
B
,
Federico
G
,
Martini
M
,
Pansadoro
V
.
Best approach for prostate cancer detection: a prospective study on transperineal versus transrectal six-core prostate biopsy
.
Urology
.
2003
;
61
:
961
6
.
13
Gill
S
,
Li
J
,
Thomas
J
,
Bressel
M
,
Thursky
K
,
Styles
C
,
Tai
KH
,
Duchesne
GM
,
Foroudi
F
.
Patient-reported complications from fiducial marker implantation for prostate image-guided radiotherapy
.
Br J Radiol
.
2012
;
85
:
1011
7
.
14
Kawakami
S
,
Yamamoto
S
,
Numao
N
,
Ishikawa
Y
,
Kihara
K
,
Fukui
I
.
Direct comparison between transrectal and transperineal extended prostate biopsy for the detection of cancer
.
Int J Urol
.
2007
;
14
:
719
24
.
15
Loeb
S
,
van den Heuvel
S
,
Zhu
X
,
Bangma
CH
,
Schroder
FH
,
Roobol
MJ
.
Infectious complications and hospital admissions after prostate biopsy in a European randomized trial
.
Eur Urol
.
2012
;
61
:
1110
4
.
16
Mosharafa
AA
,
Torky
MH
,
El Said
WM
,
Meshref
A
.
Rising incidence of acute prostatitis following prostate biopsy: fluoroquinolone resistance and exposure is a significant risk factor
.
Urology
.
2011
;
78
:
511
4
.
17
Oh
MM
,
Chae
JY
,
Kim
JW
,
Yoon
CY
,
Park
MG
,
Moon du G. Positive culture for extended-spectrum beta-lactamase during acute prostatitis after prostate biopsy is a risk factor for progression to chronic prostatitis
.
Urology
.
2013
;
81
:
1209
12
.
18
Ongun
S
,
Aslan
G
,
Avkan-Oguz
V
.
The effectiveness of single-dose fosfomycin as antimicrobial prophylaxis for patients undergoing transrectal ultrasound-guided biopsy of the prostate
.
Urol Int
.
2012
;
89
:
439
44
.
19
Pinkhasov
GI
,
Lin
YK
,
Palmerola
R
,
Smith
P
,
Mahon
F
,
Kaag
MG
,
Dagen
JE
,
Harpster
LE
,
Reese
CT
,
Raman
JD
.
Complications following prostate needle biopsy requiring hospital admission or emergency department visits - experience from 1000 consecutive cases
.
BJU Int
.
2012
;
110
:
369
74
.
20
Satyanarayana
R
,
Parekh
D
.
Prevention and treatment of biopsy-related complications
.
Curr Urol Rep
.
2014
;
15
:
381
.
21
Suzuki
M
,
Kawakami
S
,
Asano
T
,
Masuda
H
,
Saito
K
,
Koga
F
,
Fujii
Y
,
Kihara
K
.
Safety of transperineal 14-core systematic prostate biopsy in diabetic men
.
Int J Urol
.
2009
;
16
:
930
5
.
22
Wagenlehner
FM
,
van Oostrum
E
,
Tenke
P
,
Tandogdu
Z
,
Cek
M
,
Grabe
M
,
Wullt
B
,
Pickard
R
,
Naber
KG
,
Pilatz
A
,
Weidner
W
,
Bjerklund-Johansen
TE
.
Infective complications after prostate biopsy: outcome of the Global Prevalence Study of Infections in Urology (GPIU) 2010 and 2011, a prospective multinational multicentre prostate biopsy study
.
Eur Urol
.
2013
;
63
:
521
7
.
23
Watanabe
M
,
Hayashi
T
,
Tsushima
T
,
Irie
S
,
Kaneshige
T
,
Kumon
H
.
Extensive biopsy using a combined transperineal and transrectal approach to improve prostate cancer detection
.
Int J Urol
.
2005
;
12
:
959
63
.
24
Williamson
DA
,
Barrett
LK
,
Rogers
BA
,
Freeman
JT
,
Hadway
P
,
Paterson
DL
.
Infectious complications following transrectal ultrasound-guided prostate biopsy: new challenges in the era of multidrug-resistant Escherichia coli
.
Clin Infect Dis
.
2013
;
57
:
267
74
.
25
Williamson
DA
,
Freeman
JT
,
Porter
S
,
Roberts
S
,
Wiles
S
,
Paterson
DL
,
Johnson
JR
.
Clinical and molecular correlates of virulence in Escherichia coli causing bloodstream infection following transrectal ultrasound-guided (TRUS) prostate biopsy
.
J Antimicrob Chemother
.
2013
;
68
:
2898
906
.
26
Eggener
SE
,
Large
MC
,
Gerber
GS
,
Pettus
J
,
Yossepowitch
O
,
Smith
ND
,
Kundu
S
,
Kunnavakkam
R
,
Zorn
K
,
Raman
JD
.
Empiric antibiotics for an elevated prostate-specific antigen (PSA) level: a randomised, prospective, controlled multi-institutional trial
.
BJU Int
.
2013
;
112
:
925
9
.
27
Hara
R
,
Jo
Y
,
Fujii
T
,
Kondo
N
,
Yokoyoma
T
,
Miyaji
Y
,
Nagai
A
.
Optimal approach for prostate cancer detection as initial biopsy: prospective randomized study comparing transperineal versus transrectal systematic 12-core biopsy
.
Urology
.
2008
;
71
:
191
5
.
28
Miller
J
,
Perumalla
C
,
Heap
G
.
Complications of transrectal versus transperineal prostate biopsy
.
ANZ J Surg
.
2005
;
75
:
48
50
.
29
Sanders
A
,
Buchan
N
.
Infection-related hospital admissions after transrectal biopsy of the prostate
.
ANZ J Surg
.
2013
;
83
:
246
8
.
30
Carignan
A
,
Roussy
JF
,
Lapointe
V
,
Valiquette
L
,
Sabbagh
R
,
Pepin
J
.
Increasing risk of infectious complications after transrectal ultrasound-guided prostate biopsies: time to reassess antimicrobial prophylaxis?
Eur Urol
.
2012
;
62
:
453
9
.
31
Campeggi
A
,
Ouzaid
I
,
Xylinas
E
,
Lesprit
P
,
Hoznek
A
,
Vordos
D
,
Abbou
CC
,
Salomon
L
,
de la Taille
A
.
Acute bacterial prostatitis after transrectal ultrasound-guided prostate biopsy: epidemiological, bacteria and treatment patterns from a 4-year prospective study
.
Int J Urol
.
2014
;
21
:
152
5
.
32
Ehdaie
B
,
Vertosick
E
,
Spaliviero
M
,
Giallo-Uvino
A
,
Taur
Y
,
O'Sullivan
M
,
Livingston
J
,
Sogani
P
,
Eastham
J
,
Scardino
P
,
Touijer
K
.
The impact of repeat biopsies on infectious complications in men with prostate cancer on active surveillance
.
J Urol
.
2014
;
191
:
660
4
.
33
Patel
U
,
Dasgupta
P
,
Amoroso
P
,
Challacombe
B
,
Pilcher
J
,
Kirby
R
.
Infection after transrectal ultrasonography-guided prostate biopsy: increased relative risks after recent international travel or antibiotic use
.
BJU Int
.
2012
;
109
:
1781
5
.
34
Williamson
DA
,
Roberts
SA
,
Paterson
DL
,
Sidjabat
H
,
Silvey
A
,
Masters
J
,
Rice
M
,
Freeman
JT
.
Escherichia coli bloodstream infection after transrectal ultrasound-guided prostate biopsy: implications of fluoroquinolone-resistant sequence type 131 as a major causative pathogen
.
Clin Infect Dis
.
2012
;
54
:
1406
12
.
35
Berglund
RK
,
Zaytoun
O
,
Thousand
R
,
Stephans
K
,
Tendulkar
R
,
Klein
EA
,
Jones
JS
.
Early infectious complications with transponder placement for external beam radiation therapy for prostate cancer
.
BJU Int
.
2012
;
110
:
834
9
.
36
Langenhuijsen
JF
,
van Lin
EN
,
Kiemeney
LA
,
van der Vight
LP
,
McColl
GM
,
Visser
AG
,
Witjes
JA
.
Ultrasound-guided transrectal implantation of gold markers for prostate localization during external beam radiotherapy: complication rate and risk factors
.
Int J Radiat Oncol Biol Phys
.
2007
;
69
:
671
6
.
37
Igdem
S
,
Akpinar
H
,
Alco
G
,
Agacayak
F
,
Turkan
S
,
Okkan
S
.
Implantation of fiducial markers for image guidance in prostate radiotherapy: patient-reported toxicity
.
Br J Radiol
.
2009
;
82
:
941
5
.
38
Linden
RA
,
Weiner
PR
,
Gomella
LG
,
Dicker
AP
,
Suh
DB
,
Trabulsi
EJ
,
Valicenti
RK
.
Technique of outpatient placement of intraprostatic fiducial markers before external beam radiotherapy
.
Urology
.
2009
;
73
:
881
6
.
39
Brown
S
,
Lehman
M
,
Ferrari-Anderson
J
,
Glyde
A
,
Burmeister
E
,
Nicol
D
.
Assessment of prostatic fiducial marker introduction: patient morbidity, staff satisfaction and improved treatment field placement
.
J Med Imaging Radiat Oncol
.
2011
;
55
:
417
24
.
40
Thompson
A
,
Fox
C
,
Foroudi
F
,
Styles
C
,
Tai
KH
,
Owen
R
,
Laferlita
M
.
Planning and implementing an implanted fiducial programme for prostate cancer radiation therapy
.
J Med Imaging Radiat Oncol
.
2008
;
52
:
419
24
.
41
Yang
J
,
Abdel-Wahab
M
,
Ribeiro
A
.
EUS-guided fiducial placement before targeted radiation therapy for prostate cancer
.
Gastrointest Endosc
.
2009
;
70
:
579
83
.
42
Kably
I
,
Bordegaray
M
,
Shah
K
,
Salsamendi
J
,
Narayanan
G
.
Single-Center Experience in Prostate Fiducial Marker Placement: Technique and Midterm Follow-up
.
J Vasc Interv Radiol
.
2014
;
25
:
1125
32
.
43
Carmignani
L
,
Picozzi
S
,
Spinelli
M
,
Di Pierro
S
,
Mombelli
G
,
Negri
E
,
Tejada
M
,
Gaia
P
,
Costa
E
,
Maggioni
A
.
Bacterial sepsis following prostatic biopsy
.
Int Urol Nephrol
.
2012
;
44
:
1055
63
.
44
Steensels
D
,
Slabbaert
K
,
De Wever
L
,
Vermeersch
P
,
Van Poppel
H
,
Verhaegen
J
.
Fluoroquinolone-resistant E. coli in intestinal flora of patients undergoing transrectal ultrasound-guided prostate biopsy–should we reassess our practices for antibiotic prophylaxis?
Clin Microbiol Infect
.
2012
;
18
:
575
81
.
45
Minamida
S
,
Satoh
T
,
Tabata
K
,
Kimura
M
,
Tsumura
H
,
Kurosaka
S
,
Matsumoto
K
,
Fujita
T
,
Iwamura
M
,
Baba
S
.
Prevalence of fluoroquinolone-resistant Escherichia coli before and incidence of acute bacterial prostatitis after prostate biopsy
.
Urology
.
2011
;
78
:
1235
9
.
46
Zaytoun
OM
,
Vargo
EH
,
Rajan
R
,
Berglund
R
,
Gordon
S
,
Jones
JS
.
Emergence of fluoroquinolone-resistant Escherichia coli as cause of postprostate biopsy infection: implications for prophylaxis and treatment
.
Urology
.
2011
;
77
:
1035
41
.
47
Ubee
SS
,
Marri
RR
,
Srirangam
SJ
.
Pain related and overall morbidity with TRUS guided prostate biopsy–a prospective study
.
Int Braz J Urol
.
2013
;
39
:
671
4
.
48
Liss
MA
,
Nakamura
KK
,
Peterson
EM
.
Comparison of broth enhancement to direct plating for screening of rectal cultures for ciprofloxacin-resistant Escherichia coli
.
J Clin Microbiol
.
2013
;
51
:
249
52
.
49
Abughosh
Z
,
Margolick
J
,
Goldenberg
SL
,
Taylor
SA
,
Afshar
K
,
Bell
R
,
Lange
D
,
Bowie
WR
,
Roscoe
D
,
Machan
L
,
Black
PC
.
A prospective randomized trial of povidone-iodine prophylactic cleansing of the rectum before transrectal ultrasound guided prostate biopsy
.
J Urol
.
2013
;
189
:
1326
31
.
50
Adibi
M
,
Hornberger
B
,
Bhat
D
,
Raj
G
,
Roehrborn
CG
,
Lotan
Y
.
Reduction in hospital admission rates due to post-prostate biopsy infections after augmenting standard antibiotic prophylaxis
.
J Urol
.
2013
;
189
:
535
40
.
51
Chan
ES
,
Lo
KL
,
Ng
CF
,
Hou
SM
,
Yip
SK
.
Randomized controlled trial of antibiotic prophylaxis regimens for transrectal ultrasound-guided prostate biopsy
.
Chin Med J (Engl)
.
2012
;
125
:
2432
5
.
52
Manecksha
RP
,
Nason
GJ
,
Cullen
IM
,
Fennell
JP
,
McEvoy
E
,
McDermott
T
,
Flynn
RJ
,
Grainger
R
,
Thornhill
JA
.
Prospective study of antibiotic prophylaxis for prostate biopsy involving >1100 men
.
ScientificWorld Journal
.
2012
;
2012
:
650858
.
53
Duplessis
CA
,
Bavaro
M
,
Simons
MP
,
Marguet
C
,
Santomauro
M
,
Auge
B
,
Collard
DA
,
Fierer
J
,
Lesperance
J
.
Rectal cultures before transrectal ultrasound-guided prostate biopsy reduce post-prostatic biopsy infection rates
.
Urology
.
2012
;
79
:
556
61
.
54
Taylor
AK
,
Zembower
TR
,
Nadler
RB
,
Scheetz
MH
,
Cashy
JP
,
Bowen
D
,
Murphy
AB
,
Dielubanza
E
,
Schaeffer
AJ
.
Targeted antimicrobial prophylaxis using rectal swab cultures in men undergoing transrectal ultrasound guided prostate biopsy is associated with reduced incidence of postoperative infectious complications and cost of care
.
J Urol
.
2012
;
187
:
1275
9
.
55
Madden
T
,
Doble
A
,
Aliyu
SH
,
Neal
DE
.
Infective complications after transrectal ultrasound-guided prostate biopsy following a new protocol for antibiotic prophylaxis aimed at reducing hospital-acquired infections
.
BJU Int
.
2011
;
108
:
1597
602
.
56
Remynse
LC
, 3rd,
Sweeney
PJ
,
Brewton
KA
,
Lonsway
JM
.
Intravenous piperacillin/tazobactam plus fluoroquinolone prophylaxis prior to prostate ultrasound biopsy reduces serious infectious complications and is cost effective
.
Open Access J Urol
.
2011
;
3
:
139
43
.
57
Liss
MA
,
Peeples
AN
,
Peterson
EM
.
Detection of fluoroquinolone-resistant organisms from rectal swabs by use of selective media prior to a transrectal prostate biopsy
.
J Clin Microbiol
.
2011
;
49
:
1116
8
.
58
Batura
D
,
Rao
GG
,
Bo Nielsen P, Charlett A. Adding amikacin to fluoroquinolone-based antimicrobial prophylaxis reduces prostate biopsy infection rates
.
BJU Int
.
2011
;
107
:
760
4
.
59
Pinkstaff
DM
,
Igel
TC
,
Petrou
SP
,
Broderick
GA
,
Wehle
MJ
,
Young
PR
.
Systematic transperineal ultrasound-guided template biopsy of the prostate: three-year experience
.
Urology
.
2005
;
65
:
735
9
.
60
Gardiner
BJ
,
Mahony
AA
,
Ellis
AG
,
Lawrentschuk
N
,
Bolton
DM
,
Zeglinski
PT
,
Frauman
AG
,
Grayson
ML
.
Is fosfomycin a potential treatment alternative for multidrug-resistant gram-negative prostatitis?
Clin Infect Dis
.
2014
;
58
:
e101
5
.
61
Vyas
L
,
Acher
P
,
Kinsella
J
,
Challacombe
B
,
Chang
RT
,
Sturch
P
,
Cahill
D
,
Chandra
A
,
Popert
R
.
Indications, results and safety profile of transperineal sector biopsies (TPSB) of the prostate: a single centre experience of 634 cases
.
BJU Int
.
2013
.
62
Lorber
G
,
Benenson
S
,
Rosenberg
S
,
Gofrit
ON
,
Pode
D
.
A single dose of 240 mg gentamicin during transrectal prostate biopsy significantly reduces septic complications
.
Urology
.
2013
;
82
:
998
1002
.
63
Takenaka
A
,
Hara
R
,
Ishimura
T
,
Fujii
T
,
Jo
Y
,
Nagai
A
,
Fujisawa
M
.
A prospective randomized comparison of diagnostic efficacy between transperineal and transrectal 12-core prostate biopsy
.
Prostate Cancer Prostatic Dis
.
2008
;
11
:
134
8
.
64
Liss
MA
,
Nakamura
KK
,
Meuleners
R
,
Kolla
SB
,
Dash
A
,
Peterson
EM
.
Screening rectal culture to identify fluoroquinolone-resistant organisms before transrectal prostate biopsy: do the culture results between office visit and biopsy correlate?
Urology
.
2013
;
82
:
67
71
.
65
Pepe
P
,
Aragona
F
.
Morbidity after transperineal prostate biopsy in 3000 patients undergoing 12 vs 18 vs more than 24 needle cores
.
Urology
.
2013
;
81
:
1142
6
.
66
Qi
C
,
Malczynski
M
,
Schaeffer
AJ
,
Barajas
G
,
Nadler
RB
,
Scheetz
MH
,
Zembower
TR
.
Characterization of ciprofloxacin resistant Escherichia coli isolates among men undergoing evaluation for transrectal ultrasound guided prostate biopsy
.
J Urol
.
2013
;
190
:
2026
32
.
67
Pepe
P
,
Aragona
F
.
Prostate biopsy: results and advantages of the transperineal approach-twenty-year experience of a single center
.
World J Urol
.
2014
;
32
:
373
7
.
68
Issa
MM
,
Al-Qassab
UA
,
Hall
J
,
Ritenour
CW
,
Petros
JA
,
Sullivan
JW
.
Formalin disinfection of biopsy needle minimizes the risk of sepsis following prostate biopsy
.
J Urol
.
2013
;
190
:
1769
75
.
69
Taylor
S
,
Margolick
J
,
Abughosh
Z
,
Goldenberg
SL
,
Lange
D
,
Bowie
WR
,
Bell
R
,
Roscoe
D
,
Machan
L
,
Black
P
.
Ciprofloxacin resistance in the faecal carriage of patients undergoing transrectal ultrasound guided prostate biopsy
.
BJU Int
.
2013
;
111
:
946
53
.
70
Vyas
L
,
Acher
P
,
Kinsella
J
,
Challacombe
B
,
Chang
RT
,
Sturch
P
,
Cahill
D
,
Chandra
A
,
Popert
R
.
Indications, results and safety profile of transperineal sector biopsies (TPSB) of the prostate: a single centre experience of 634 cases
.
BJU Int
.
2014
;
114
:
32
7
.