Cancer and Prostatic Diseases (2010) 13, 52–57 & 2010 Nature Publishing Group All rights reserved 1365-7852/10 $32.00 www.nature.com/pcan ORIGINAL ARTICLE

Can residents perform transrectal ultrasound-guided prostate with patient comfort comparable to biopsy performed by attending staff urologists?

CT Nguyen1, T Gao2, AV Hernandez2 and JS Jones1 1Department of Regional , Glickman Urological & Kidney Institute, Cleveland Clinic Foundation, Cleveland, OH, USA and 2Department of Quantitative Health Sciences, Cleveland Clinic Foundation, Cleveland, OH, USA

Transrectal ultrasound (TRUS)-guided prostate biopsy is a critical diagnostic tool in urology. Residents require adequate training but resident education could have a deleterious effect on patient comfort and morbidity. We compared pain associated with prostate biopsy when performed by staff versus resident urologists in order to determine the impact of resident training. Male patients scheduled to undergo prostate biopsy were assigned to either a staff urologist or a resident as the primary surgeon. All residents were directly assisted by the staff surgeon. The patients were given a visual analogue scale (VAS; 0–100 mm) and were asked to assess the pain associated with each component of prostate biopsy, including probe insertion, anesthetic injection and the themselves. The mean VAS scores for probe insertion, anesthetic injection and biopsies were 31.0, 30.4 and 30.1, respectively, for patients in the staff cohort and 37.1, 28.9 and 33.6, respectively, for those in the resident cohort. There was a statistically significant difference between staff and resident VAS scores, marked by a higher odds of greater pain with ultrasound probe placement (odds ratio (OR) ¼ 1.48, P ¼ 0.012) and the biopsies themselves (OR ¼ 1.52, P ¼ 0.01) in the resident cohort. TRUS biopsy can be performed by adequately trained and supervised resident urologists of all levels, but there is the potential for increased patient pain, particularly with ultrasonic probe insertion and obtaining core biopsies. However, the absolute magnitude of the differences in pain scores between residents and staff was small and may not be clinically meaningful. Such data indicate that urological resident training can be accomplished without compromising patient care and comfort. and Prostatic Diseases (2010) 13, 52–57; doi:10.1038/pcan.2009.36; published online 22 September 2009

Keywords: prostate biopsy; pain score; morbidity; resident training

Introduction patient discomfort and morbidity as well as to optimize diagnostic accuracy. Despite advances in tumor markers and the develop- Instruction in the technique of TRUS biopsy is ment of screening tests (for example, PSA test), the gold typically provided in residency, and until recently, standard for detection of prostate cancer continues to be there has been a distinct paucity of data regarding the transrectal ultrasound (TRUS)-guided prostate biopsy. impact of surgical experience and resident training TRUS biopsy is an invasive, complex and highly on patient morbidity from urological procedures. We sensitive procedure with the potential for inducing have recently published studies showing that there significant pain for the patient.1 Proper technique in are no clinically significant differences in patient pain prostate biopsy requires the mastering of several intricate with cystoscopy or , whether performed by steps, including inserting the probe, injecting peripro- staff or resident urologists.2,3 However, among ambu- static block (PPB) and performing multiple, appropri- latory urological operations, prostate biopsy is arguably ately placed core biopsies. Adequate training of the most complex and invasive, and may have a steeper urologists in TRUS biopsy has the potential to minimize learning curve and a higher potential for adverse effects on patients who have biopsies performed by a resident. Correspondence: Dr JS Jones, Department of Regional Urology, In this study we analyze whether resident urologists, Glickman Urological & Kidney Institute, Cleveland Clinic with proper instruction and supervision, are able to Foundation, 9500 Euclid Avenue, A100, Cleveland, OH 44195, USA. E-mail: [email protected] perform TRUS biopsy with comparable proficiency to Received 30 June 2009; accepted 21 July 2009; published online 22 staff surgeons. On the basis of our previous work in this September 2009 field, we hypothesized that there would be no significant TRUS-guided prostate biopsy by staff vs resident urologists CT Nguyen et al differences in patient pain between biopsies performed levels, and the proportional odds assumption was tested. 53 by resident and those performed by staff urologists. The effect of resident versus staff performance of TRUS biopsy on patient pain was adjusted for other possible confounders, including patient age, block site, probe type and anesthesia usage. A P-value o0.05 indicated Patients and methods statistical significance. All statistical analyses were carried out using SAS 9.1 (SAS Institute Inc., Cary, NC, A total of 865 men scheduled for elective office-based USA). TRUS prostate biopsy were included in our prospective institutional review board-approved protocol between January 2006 and December 2008. Indications for TRUS biopsy included elevated or rising PSA level, abnormal findings on digital , active surveillance Results for patients with low-risk prostate cancer and rising PSA The mean pain scores for each component of TRUS level after previous non-extirpative therapy for prostate biopsy for both resident and staff patient groups are cancer. Fourteen staff urologists and residents in their summarized in Table 1. Patients in the resident group second, third or fifth year of training participated in the showed slightly higher mean VAS scores for probe study. Fourth-year residents in our program were insertion (37.1 versus 31.0, P ¼ 0.0004) and the core assigned entirely to research and did not participate in biopsies (33.6 versus 30.1, P ¼ 0.03) compared with those the study. Patients were assigned to either the staff in the staff group. In contrast, there were no significant urologist or a resident as the primary surgeon, based differences in the pain associated with the PPB between primarily on whether the resident was in the clinic at the resident and staff patient groups. time (the default is for the resident to perform the Table 1 also delineates the relative distribution of procedure if present in the clinic). In addition, the staff potential confounders between the two patient groups, demonstrated the first of any given procedure each including age, block site, probe type and use of a topical month when a new resident rotated on service. anesthetic. Previous work from Cleveland Clinic has The residents assigned to a given patient’s TRUS shown that apical periprostatic injection of an anesthetic biopsy performed all components of the procedure results in reduced biopsy pain compared with basilar themselves. Operations were performed by residents injection, but it does not increase the pain of the PPB under the direct supervision of the staff urologist. In itself.5 In addition, preliminary data from our group have brief, a lubricated ultrasound probe was inserted into the suggested that pain associated with probe insertion may rectum and correct positioning was confirmed by depend, in part, on the specific design and make of the ultrasonic image. To perform the PPB, a 7-inch 22-gauge ultrasound probe, potentially introducing a confounding spinal needle was inserted though the biopsy needle 3 effect (JS Jones, unpublished data/personal communi- guide, and 5 cm of 1% lidocaine was then injected cation). Hurricaine, a topical anesthetic gel commonly bilaterally at either the apex or the base of the prostate. used to facilitate gastroenterological endoscopic proce- Prostatic biopsy was then performed using a disposable 4 dures, has been used by some of the staff urologists at spring-loaded biopsy needle as described earlier. our institution, given its potential utility in reducing the Immediately after completion of the procedure, patients discomfort of probe insertion. As such, the distribution were given an unmarked 100-mm visual analogue scale and frequency of these variables between the two patient (VAS) and were asked to assign a separate pain score for groups were examined. each component of the procedure, including probe The average age of patients in either the staff or the insertion, the PPB and the core biopsies. resident cohorts was similar (63.8 versus 64.1, P ¼ 0.62). Patients in the resident group had a higher rate of apical PPB compared with those in the staff group (60 versus Statistical analysis 43%, Po0.0001), on the basis of their working more Sample size calculations, which assumed that pain scores closely with a staff urologist (JSJ) who recommends had a coefficient of variation of 0.95, indicated that a apical injection based on the above data. Regarding sample size of at least 200 patients per group was needed probe type distribution, most residents used a Siemens to detect a 5-point difference in pain scores, with 80% Prima ultrasound probe with a long plastic guide, power and a two-sided significance level of 0.05. whereasthe majority of the staff used the Sonoline G50 The pain scores in the scale of 0–100 were not normally (Malvern, PA, USA) probe. The staff urologists showed a distributed (Figure 1). Transformation of the scores could wider distribution regarding usage of different probe not completely overcome the problem of non-normality, types when compared with the residents. The choice of and therefore continuous regression techniques with a probe type was determined mainly by the clinic site as normality assumption were not applicable. Instead, pain different facilities have different equipments. There was scores were placed into five ordered categories, and the no difference in the rate of usage of Hurricaine between association between the factors of interest and the the resident and staff patient groups, and it was used in ordered pain categories was modeled through ordinal only a small number of patients. logistic regression, in which no assumption of the After performing logistic regression on the data and normality of pain scores was made. adjusting for all the aforementioned potential confoun- A proportional odds model was used to fit the ordinal ders, patients in the resident group were found to have a categorical data. The odds ratio (OR) of higher pain 1.48-fold greater odds (95% confidence interval 1.1–2.0) levels between patients in the resident and staff groups of experiencing greater pain with probe insertion than was assumed to be consistent across the ordered pain those in the staff group, regardless of the actual

Prostate Cancer and Prostatic Diseases TRUS-guided prostate biopsy by staff vs resident urologists CT Nguyen et al

54 Probe pain score distributions for patients treated by staff and residents

17.5 Lower Quartile 20 15.0 Mean 37.06 12.5 Median 33 10.0 Upper Quartile 53

Percent 7.5 resident 5.0 2.5 0 17.5 Lower Quartile 13 15.0 Mean 31.01 12.5 Median 27 10.0 Upper Quartile 45 staff

Percent 7.5 5.0 2.5 0 0510 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 100 probe_pain

Block pain score distributions for patients treated by staff and residents

15.0 Lower Quartile 10 12.5 Mean 28.92 Median 24 10.0 Upper Quartile 42 7.5 Percent resident 5.0 2.5 0 15.0 Lower Quartile 12 12.5 Mean 30.39 10.0 Median 30 Upper Quartile 44

staff 7.5 Percent 5.0 2.5 0 0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 100 block_pain

Biopsy pain score distributions for patients treated by staff and residents

17.5 Lower Quartile 16 15.0 Mean 33.63 12.5 Median 30 10.0 Upper Quartile 48 Percent

resident 7.5 5.0 2.5 0 17.5 Lower Quartile 14 15.0 Mean 30.12 12.5 Median 26.5 10.0 Upper Quartile 43 staff

Percent 7.5 5.0 2.5 0 0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 100 biopsy_pain Figure 1 Distributions of pain scores for each component of transrectal ultrasound-guided (TRUS) biopsy for patients in the resident and staff groups.

magnitude of the VAS score (P ¼ 0.012) (Table 2). interval 1.1–2.1) of higher pain than the staff group Similarly, for biopsy pain, patients in the resident group (P ¼ 0.01). Analysis of the pain data associated with the showed a 1.523-fold greater odds (95% confidence PPB revealed no increase in the OR (0.993, 95%

Prostate Cancer and Prostatic Diseases TRUS-guided prostate biopsy by staff vs resident urologists CT Nguyen et al 55 Table 1 Descriptive statistics Variable Staff Resident P-value

N Mean (s.d.) N Mean (s.d.) Median (quartiles) Median (quartiles) Odds ratio Odds ratio Frequency (percentage) Frequency (percentage)

Probe pain 615 31.0 (22.3) 250 37.1 (23.7) 0.0004 27 (13, 45) 33 (20, 53) Block pain 615 30.4 (21.1) 250 28.9 (22.6) 0.36 30 (12, 44) 24 (10, 42) Biopsy pain 610 30.1 (20.8) 249 33.6 (22.5) 0.03 26.5 (14, 43) 30 (16, 48) Age 613 63.8 (8.2) 250 64.1 (8.6) 0.62 63 (58, 69) 65 (58, 70)

Block o0.0001 a 592 256 (43%) 250 151 (60%) b 285 (48%) 98 (40%) a+b 51 (9%) 1 (0.5%)

Probe type o0.0001 bk 608 157 (26%) 250 2 (1%) g50 215 (35%) 63 (25%) Long plastic guide 110 (18%) 141 (57%) Prima 113 (19%) 26 (10%) Short plastic guide 13 (2%) 18 (7%)

Anesthesia 0.1 Hurricane 616 30 (5%) 250 6 (2%) None 586 (95%) 244 (98%)

Table 2 Comparison of pain scores for transrectal ultrasound Table 3 Comparison of pain scores for transrectal ultrasound biopsy between staff and resident urologists biopsy between different resident levels Odds ratio 95% Confidence intervals P-value Resident-level Odds ratio 95% Confidence intervals P-value comparison Probe insertion 1.48 1.091 2.008 0.012 Periprostatic block 0.993 0.729 1.351 0.96 Probe insertion Biopsy 1.523 1.119 2.074 0.01 3 vs 2 1.328 0.762 2.313 5 vs 2 1.478 0.845 2.586 0.36 Odds ratio is the odds of greater pain for resident versus staff. 5 vs 3 1.114 0.618 2.004

Block confidence interval 0.7–1.4, P ¼ 0.96) between resident 3 vs 2 1.619 0.919 2.852 and staff groups. 5 vs 2 1.663 0.941 2.939 0.13 The effect of resident training level was also studied by 5 vs 3 1.027 0.568 1.859 ordinal logistic regression, after pain scores for each Biopsy component of TRUS biopsy were grouped by resident 3 vs 2 0.912 0.521 1.596 postgraduate year (Table 3). Higher-level residents 5 vs 2 1.115 0.635 1.955 0.8 consistently showed higher odds of inducing greater 5 vs 3 1.222 0.675 2.212 pain among patients when compared with junior residents for any component of TRUS biopsy. However, none of the observed differences reached statistical importance. Although limited in magnitude, surgeon skill significance. It should be noted that our study was and experience influence pain levels in patients under- powered for examination of the resident versus staff going TRUS biopsy, raising the question of whether having effect, whereas the substudy between different resident a biopsy performed by a resident urologist adversely year groups was not adequately powered. impacts patient comfort. Indeed, a study from the United Kingdom assessing the comfort level of residents with TRUS biopsy indicated that most residents felt they had received insufficient training and were not comfortable Discussion with independent performance of prostate biopsy.6 The effect of a urological surgeon’s training level on TRUS-guided biopsy of the prostate is a critical tool in the pain experienced by patients undergoing ambulatory the diagnosis and management of prostate cancer. As it procedures has been largely unexplored in the current is an invasive and intricate procedure often performed literature. Cleveland Clinic recently published the first in the office on awake and unsedated patients, improv- studies detailing the impact of urological resident ing the tolerance of TRUS biopsy is of paramount training on patient care.2,3 Comparing staff versus

Prostate Cancer and Prostatic Diseases TRUS-guided prostate biopsy by staff vs resident urologists CT Nguyen et al

56 resident performance of cystoscopy and vasectomy, the urological residency. Interestingly, we did observe that investigators found minimal differences in pain scores higher-level residents showed higher pain scores when between the two groups, suggesting that resident compared with junior residents. Although not statisti- training in these procedures can be accomplished with- cally significant, these differences may reflect a tendency out compromising on the high standards of patient care. by senior residents to perform procedures more aggres- Furthermore, these studies showed no significant differ- sively because of greater comfort and/or confidence in ences in pain scores between residents of different their skills. training levels for either cystoscopy or vasectomy, The results in this study do not completely support suggesting that these urological procedures do not have our initial hypothesis that resident and staff urologists a steep learning curve and can be performed early in the are able to perform TRUS biopsy with similar profi- training experience with proper instruction and over- ciency, and indicate that greater efforts may be required sight. to ensure that urological residents receive adequate In contrast with those studies, the data contained in training in this procedure (for example, increased this report show that patients whose biopsies are familiarity with anorectal anatomy and greater case performed by resident urologists have statistically sig- numbers). However, despite a higher risk of slightly nificant higher odds of greater pain with probe insertion increased pain with probe insertion and biopsy, we still and obtaining core biopsies, whereas the pain of the PPB believe that resident performance of TRUS biopsy does was comparable between the two patient groups. not pose significant harm to patients or adversely impact Although it is presumably the simplest component of their tolerance of the procedure based on the small TRUS biopsy, insertion of the ultrasonic probe can be magnitude of these differences, which we believe have complicated by insufficient knowledge of anorectal limited clinical significance. anatomy and physiology, or inadequate recognition of The lack of randomization and blinding are the how hard to push with the probe as it is inserted. Lack of limitations of this study. Nevertheless, our practice is familiarity with the direction of the anal canal (which for the resident to perform the procedure in the clinic to angulates anteriorly toward the umbilicus rather than maximize the learning opportunity. Furthermore, both coursing directly cephalad) and its rich innervation with age distribution and rates of Hurricaine usage were somatic sensory nerves may lead to a poorly directed comparable between the two patient groups, but the probe and account for the higher pain scores observed frequencies of other potential confounders, including with residents, suggesting that repeated reinforcement of type of probe used, were different. these points may be valuable. Although it is reasonable to attribute the difference in pain scores to the variable usage of specific probe types between residents and staff, we should reiterate that the data were adjusted for this Conclusions potential confounder in the final statistical multivariate Prostate biopsy is a vital diagnostic tool for urologists, analysis. but can cause significant pain and morbidity if per- The finding of greater pain with the core biopsies in formed by poorly trained hands. This study shows that, the resident group is interesting, given the lack of with proper instruction and supervision, resident uro- difference in PPB pain scores between the staff and logists of all training levels can perform this procedure resident groups, and may suggest that resident applica- with only slightly higher discomfort during certain tion of lidocaine is slightly less effective in inducing components. The data indicate that urological resident anesthesia. Although not associated with greater pain of 5 training can be accomplished successfully without the PPB itself, apical injection of anesthetic (which was significant detriment to patients whose biopsies are performed more frequently in the resident group) is performed by properly supervised residents. However, technically more difficult and, if not performed correctly, there are some measures that can be instituted to may have failed to achieve adequate anesthesia in a potentially improve resident proficiency in TRUS biopsy, number of resident cases. It is also possible that the probe including reiteration of the basic anatomy involved, was causing the pain during the actual biopsy, and usage of basilar PPB and/or greater case numbers. patients may reflect this experience in the scores recorded for the biopsy portion of the procedure. Despite the increased odds of greater pain with probe insertion and biopsy in the resident group, the overall Conflict of interest pain scores associated with TRUS biopsy tended to be The authors declare no conflict of interest. low (that is, o40). Furthermore, the absolute magnitude of the differences in pain scores between staff and resident urologists was limited, with the greatest spread being only 6 points (37.1 versus 31.0 for probe insertion Acknowledgements for residents and staff, respectively). Therefore, it is reasonable to suggest that the observed differences in This study was funded by the Glickman Urological and pain scores, although statistically significant, may not Kidney Institute. represent a major clinical detriment to patients. Moreover, there were no statistically significant differ- ences in pain scores for any component of TRUS biopsy References when the data were stratified by year of residency training, suggesting that the technical maneuvers of 1 Zisman A, Leibovici D, Kleinmann J, Siegel YI, Lindner A. The prostate biopsy can be taught and performed early in impact of prostate biopsy on patient well-being: a prospective

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