History of Urinary Retention Is a Risk Factor for Infection after Prostate Biopsy: A Nationwide,Population-Based Cohort Study

Abstract

Background and Aim:

Infection or bleeding after transrectal prostate biopsy remains a concern of both patients and urologists. We explored the risk of association of certain co-morbidities with both complications.

Patients and Methods:

Using the Taiwan National Health Insurance Research Database, we identified patients undergoing prostate biopsy from 2000 to 2013. We used logistic multivariable regression to search for associations between post-biopsy hospitalization and the two co-morbidities within a year after biopsy.

Results:

Among 3,601 prostate biopsies, 100 infections (3.77%) and 52 (1.44%) bleeding-related emergency room visits and hospitalizations were recorded within 30 days after biopsy. The group having the biopsy as an inpatient exhibited older age (p < 0.0001) and a higher percentage of having diabetes mellitus (p = 0.015) than patients without either complication. The logistic multivariable regression analysis showed that urinary retention, freedom from diabetes, and performance as an outpatient procedure were independent risk factors for infection-related hospitalization (odds ratios 1.81, 1.96, and 1.72; p values 0.031, 0.037, and 0.010, respectively).

Conclusion:

Patients with a recent history of urinary retention have a higher probability of infection-related hospitalization after prostate biopsy.

Prostate cancer has been the most common malignancy and second leading cause of cancer death in men in Western countries for more than 20 years [1]. Although the survival benefit of prostate cancer screening remains controversial [2,3], the majority of cancers can be detected as localized disease owing to screening effects and can be managed with radical prostatectomy, radiotherapy, or active surveillance. Transrectal ultrasound-guided (TRUS) prostate biopsy on an outpatient basis has been the main means of early diagnosis of prostate cancer in Western countries [4,5], although some urologists prefer transperineal prostate biopsy to prevent bacterial contamination posed by the rectal route [6].

Since the late 1990s, the annual detection rate of prostate cancer has risen in Taiwan and other Asian countries [7]. In contrast to Western countries, in Taiwan, many tumors are diagnosed at an advanced stage [8]. Not only the absence of a prostate cancer screening policy in Taiwan, but also lack of concern on the part of patients and urologists, has led to life-threatening infection-related complications of biopsy [9]. The complications and morbidities resulting from biopsy via the rectal route often contribute to emergency department (ED) visits and hospitalization, as well as higher medical costs [10,11]. Thus, it is important to explore the risk factors associated with post-biopsy ED visits and hospitalization.

Several studies focus on how to diminish the complications of prostate needle biopsy, such as empiric antimicrobial drug prophylaxis [12,13], pre-biopsy rectal enema [14 –16], rectal swab culture for drug selection [17], temporary discontinuation of anticoagulants, or attempts to predict the complication using baseline prostate parameters [18] or co-morbidities [19]. Unfortunately, most of these studies were either single institutional or small.

In Taiwan, the patient with an elevated prostate-specific antigen (PSA) concentration should receive prostate biopsy before the prescription of a 5α-reductase inhibitor (i.e., finasteride or dutasteride) for gland shrinkage, and this is mandated by the health insurance system. Many patients receiving prostate biopsy have non-malignant factors that result in elevated serum PSA, including urinary tract infection, acute urinary retention, or sub-clinical prostatitis.

Several urologists in Taiwan offer prostate biopsy as an inpatient procedure. The common reason is to avoid any litigation following the occurrence of life-threatening septic shock, particularly for octogenarian patients [20], because several strategies can be applied strictly before biopsy of inpatients to reduce the infection complications, including an enema and intravenous antimicrobial prophylaxis. Also, some urologists perform saturation biopsy under general or spinal anesthesia. Currently, there is no evidence concerning whether an inpatient biopsy is associated with fewer complications than an outpatient procedure.

The aim of this study was to investigate the effect of co-morbidities on infection- or bleeding related visits or hospitalizations after prostate biopsy using a nationwide, population-based cohort. We also explored the effect of an inpatient biopsy on visits or hospitalizations.

Patients and Methods

Data origin and subjects

The National Health Insurance program has been carried out in Taiwan since 1995. It provides medical coverage for 99% of the population (currently, about 23 million persons). The National Health Insurance Research Database (NHIRD) is a nationwide electronic compilation of data on all the beneficiaries enrolled in the program. The Taiwan National Health Research Institutes (NHRI) deals with NHIRD and provides several kinds of blinded datasets for various research studies. Each dataset contains complete outpatient visits, hospital admissions, prescriptions, disease, and vital status per person of one million beneficiaries randomly sampled from the NHIRD. The patients' personal information has been encrypted to ensure privacy. Anonymous numbers are linked with relevant information, including sex, date of birth, medications prescribed, and medical services received. Patient consent is not necessary to access the NHIRD according to the Institute Ethical Committee's rule of National Cheng Kung University Hospital.

From a one-million-person dataset, we sifted out male patients who were 45 years of age and older, who had been found to have benign prostatic hyperplasia, abnormal serum PSA concentration, or prostate cancer (International Classification of Diseases [ICD] ICD-9-CM codes 600, 6000, 602, 6009, 60090, 79093, and 185), and who received prostate biopsy under ultrasound guidance (19007B, 79401B) between January 1, 2000 and October 31, 2013 on either an outpatient or an inpatient basis.

Outcomes

Because post-biopsy infection and bleeding were encountered most commonly in daily practice, the study outcome was defined as the occurrence of ED visits and hospitalizations for the treatment of urosepsis, urinary tract infection (ICD-9-CM codes 601, 6010, 6011, 6012, 5990, 9985, 7806, 038, 0389, 595, 5959, 5950), or significant bleeding (ICD-9-CM codes 9981, 5997, 59970, 59971, 59972). Some biopsy-related infections or bleeding may occur late and repeatedly within one month [21]. Pinkhasov et al. reported their single-institutional experience of post-biopsy complications using a 30-day hospital readmission and ED visit rate because of an office visit at four weeks and at six months after biopsy as their standardized follow-up protocol [22]. Nam et al. also reported a 30-day post-biopsy hospital readmission rate because of the utility of administrative databases in their population-based study [21]. For the purpose of this study and comparison with other studies [21,22], we calculated the ED visit or hospital readmission rate within 30 days after prostate biopsy.

To make our findings generalizable, we chose co-morbidities that might contribute to post-biopsy infection or bleeding. Data on these co-morbidities the patients exhibited one year before biopsy were collected, including hypertension (ICD-9-CM codes 401, 4010,4011,4019, 402, 4020, 40200, 40201, 40210, 40211, 4029, 40290, 40291), diabetes mellitus (ICD-9-CM codes 249, 2490, 2491 ∼ 2499, 250, 2500, 2501 ∼ 2509), cerebro-vascular accident (CVA) (99702, 430,431, 43401, 43411, 43491, 4320, 4321, 4322, 4323, 4324, 4325, 4326, 4327, 4328, 4329), urinary tract infection (UTI) (ICD-9-CM codes 599, 5990, 595, 5950, 604, 6040, 6049, 601, 6010, 6011, 6012), and retention of urine (ICD-9-CM codes 7882, 78820, 78821, 78829). Both hypertension and CVA may be related to the possibility of post-biopsy bleeding because of anticoagulant administration. Diabetes mellitus, CVA, UTI, and urinary retention may be related to post-biopsy infection.

Statistical analyses

We assessed the distributions of demographic data and co-morbidities in the patients. The risk of visits to the ED and of hospitalization was calculated either with the χ² test or multivariable logistic regression analysis. All statistical analyses were done with SAS (version 9.4) or SPSS (version 17.0). All significance thresholds were set at two-sided p < 0.05.

Results

Altogether, 3,601 prostate biopsies were identified, including 1,714 (47.6%) performed as outpatient procedures and 1,887 (52.4%) as inpatient procedures (Table 1). The mean age of the patients at the time of biopsy was 70.7 years. Patients receiving inpatient biopsy were older than those seen on an outpatient basis (outpatient vs. inpatient, 68.71 ± 9.18 years vs. 72.50 ± 9.72 years; p < 0.0001), particularly those more than 85 years old. There were 1,800 patients (50%) with hypertension, 686 (19.1%) with diabetes mellitus, 131 (3.64%) with a history of CVA, 998 (27.7%) with UTI and 358 (9.94%) with urinary retention among 3,601 selected patients. The inpatient group were significantly more likely to have diabetes mellitus than was the outpatient group (inpatient vs. outpatient, 388 (20.56%) vs. 298 (17.39%); p = 0.015), and there were borderline higher percentages of hypertension (p = 0.074) and CVA history (p = 0.065).

Table 1.

Baseline Demographic and Clinical Characteristic of Patients Undergoing Prostate Needle Biopsy

	Total	Outpatient	Inpatient	p
Total	3,601	1,714	1,887
Mean age (y) (SD) (%)	70.7 (9.49)	68.71 (9.18)	72.50 (9.72)	<0.0001
45–64	1,067 (29.60)	624 (36.41)	443 (23.48)	<0.0001
65–84	2,301 (63.90)	1,033 (60.27)	1,268 (67.19)
≥85	233 (6.47)	57 (3.32)	176 (9.33)
Co-morbidity (%)
Hypertension	1,800 (50.0)	830 (48.42)	970 (51.40)	0.074
Diabetes mellitus	686 (19.10)	298 (17.39)	388 (20.56)	0.015
CVA	131 (3.64)	52 (3.03)	79 (4.19)	0.065
UTI	998 (27.70)	459 (26.78)	539 (28.56)	0.232
Retention	358 (9.94)	163 (9.51)	195 (10.33)	0.409
Adverse event (%)
Infection related	100 (3.77)	60 (3.50)	40 (2.12)	0.012
Bleeding related	52 (1.44)	28 (1.63)	24 (1.27)	0.364

CVA = cerebrovascular accident; SD = standard deviation; UTI = urinary tract infection.

In total, there were 52 (1.44%) bleeding-related and 100 (3.77%) infection-related visits or hospitalizations within 30 days after biopsy. The outpatient group had a significantly higher probability of infection-related complications (outpatient vs. inpatient, 60 (3.50%) vs. 40 (2.12%); p = 0.012).

In addition to performance as an outpatient procedure, univariable analysis demonstrated that being diabetes-free and a recent history of urinary retention were significant risk factors associated with post-biopsy complications (Table 2). Multivariable logistic regression analysis showed that being diabetes-free, having recent history of urinary retention, and biopsy performance as an outpatient procedure were independent risk factors for post-biopsy infection-related visits and hospitalizations (odds ratio [OR] and 95% confidence interval [CI], 1.96 [1.04, 3.57], 1.81 [1.04,3.15], and 1.72 [1.14, 2.63]; p = 0.037, 0.031, and 0.010, respectively) (Table 2). For the bleeding-related adverse events, there was no significant association of these co-morbidities with visits or hospitalizations by either univariable or multivariable analysis (Table 3).

Table 2.

Association of Co-Morbidities and Infection-Related Hospitalization

	Infection related			Univariable		Multivariable
	No (n = 3,501)	Yes (n = 100)	p	OR (95% CI)	p	OR (95% CI)	p
Source (%)
Inpatient	1,847 (52.76)	40 (40.00)	0.012	Ref.		Ref.
Outpatient	1,654 (47.24)	60 (60.00)		1.67 (1.11, 2.50)	0.013	1.72 (1.14, 2.63)	0.012
Age (y) (%)
45–64	1,040 (29.71)	27 (27.00)	0.559	Ref.		Ref.
≥65	2,461 (70.29)	73 (73.00)		1.14 (0.73, 1.79)	0.559	1.19 (0.75, 1.89)	0.460
Hypertension (%)
No	1,756 (50.16)	45 (45.00)	0.309	Ref.		Ref.
Yes	1,745 (49.84)	55 (55.00)		1.23 (0.83, 1.83)	0.310	1.31 (0.87, 1.97)	0.202
Diabetes mellitus (%)
Yes	675 (19.28)	11 (11.00)	0.038	Ref.		Ref.
No	2826 (80.72)	89 (89.00)		1.92 (1.03, 3,57)	0.041	1.96 (1.04, 3.57)	0.037
CVA (%)
No	3,373 (96.34)	97 (97.00)	1.000	Ref.		Ref.
Yes	128 (3.66)	3 (3.00)		0.82 (0.26, 2.61)	0.730	0.75 (0.23, 2.42)	0.630
UTI (%)
No	2,533 (72.35)	70 (70.00)	0.605	Ref.		Ref.
Yes	968 (27.65)	30 (30.00)		1.12 (0.73, 1.73)	0.605	1.03 (0.66, 1.60)	0.914
Retention (%)
No	3,160 (90.26)	83 (83.00)	0.018	Ref.		Ref.
Yes	341 (9.74)	17 (17.00)		1.90 (1.11, 3.24)	0.019	1.81 (1.04, 3.15)	0.035

CI = confidence interval; CVA = cerebrovascular accident; OR = odds ratio; SD = standard deviation; UTI = urinary tract infection.

Logistic = −3.55–0.53 (source) + 0.17 (age) + 0.27 (hypertension) − 0.68 (diabetes mellitus) − 0.29 (CVA) + 0.02 (UTI) + 0.59 (retention).

Table 3.

Association of Co-Morbidities and Subsequent Bleeding-Related Hospitalization

	Bleeding related			Univariable		Multivariable
	No (n = 3,549)	Yes (n = 52)	p	OR (95% CI)	p	OR (95% CI)	p
Procedure site (%)
Outpatient	1,686 (47.51)	28 (53.85)	0.364	Ref.		Ref.
Inpatient	1,863 (52.49)	24 (46.15)		0.78 (0.45, 1.34)	0.365	0.82 (0.47, 1.43)	0.488
Age (y) (%)
45–64	1,047 (29.50)	20 (38.46)	0.160	Ref.		Ref.
≥65	2,502 (70.50)	32 (61.54)		0.67 (0.38, 1.18)	0.163	0.68 (0.38, 1.22)	0.199
Hypertension (%)
No	1,773 (49.96)	28 (53.85)	0.578	Ref.		Ref.
Yes	1,776 (50.04)	24 (46.15)		0.86 (0.49, 1.48)	0.578	0.94 (0.54, 1.66)	0.841
Diabetes mellitus (%)
No	2,870 (80.87)	45 (86.54)	0.301	Ref.		Ref.
Yes	679 (19.13)	7 (13.46)		0.66 (0.30, 1.46)	0.305	0.73 (0.32, 1.65)	0.447
CVA (%)
No	3,419 (96.34)	51 (98.08)	1.000	Ref.		Ref.
Yes	130 (3.66)	1 (1.92)		0.52 (0.07, 3.76)	0.514	0.54 (0.07, 3.95)	0.540
UTI (%)
No	2,568 (72.36)	35 (67.31)	0.419	Ref.		Ref.
Yes	981 (27.64)	17 (32.69)		1.27 (0.71, 2.28)	0.420	1.18 (0.65, 2.16)	0.581
Retention (%)
No	3,200 (90.17)	43 (82.69)	0.074	Ref.		Ref.
Yes	349 (9.83)	9 (17.31)		1.92 (0.93, 3.97)	0.079	1.98 (0.93, 4.20)	0.077

CI = confidence interval; CVA = cerebrovascular accident; OR = odds ratio; SD = standard deviation; UTI = urinary tract infection.

Logistic = −3.92–0.20 (source) − 0.38 (age) − 0.06 (hypertension) − 0.32 (diabetes mellitus) − 0.63 (CVA) + 0.17 (UTI) + 0.68 (retention).

Discussion

In the current study, we explored the risk factors for ED visits and hospitalization after prostate biopsy by utilizing the National Health Insurance Research Database in Taiwan. Our results demonstrated that being diabetes-free, having a recent history of urinary retention, and undergoing an outpatient procedure were independent risk factors for infection-related adverse events, whereas other co-morbidities such as hypertension, CVA, or UTI were not factors. There are many published studies regarding the predictors of post-biopsy infection events, although this can be difficult because the incidence often is low, ranging from 0.5% to 9.3% [11,23 –27]. The risk factors identified include prostate enlargement, diabetes mellitus, recent use of anticoagulant/antiplatelet therapy, an outpatient procedure without a cleansing enema, and a history of CVA. The possible reasons for the inconsistent results include the heterogeneity of patient cohorts, differences in methods, and the low incidence of post-biopsy sepsis.

Lindert et al. reported that once transrectal prostate needle biopsy was done, bacteriuria and bacteremia can be detected in 44% and 16% of the patients, respectively, soon after the procedure [16]. The majority of patients remain asymptomatic, although some developed serious infections requiring hospitalization, with a few cases of rapid progress to fatal sepsis despite utilization of prophylactic antibiotics [28]. In addition to bacterial virulence [29], the innate immune response of the host is one of the pivotal factors contributing to symptomatic UTI while uroepithelial cells become inoculated or already bear uropathogenic bacteria. Co-morbidities (i.e., diabetes mellitus) may diminish the innate immune response by activating or deactivating certain immune cells and molecules (such as chemokines, cytokines, and dendritic, mast, and inflammatory cells) that orchestrate and provide innate host defenses [30]. In contrast, asymptomatic patients with bacteriuria or bacteremia may exhibit no or weak innate immune responses, in which bacteria exist in a commensal-like state [30]. Further studies regarding the microbiome inside the prostate may be required to understand these situations completely.

Generally, prostate needle biopsy a safe, low-complication procedure, and the majority of patients undergo biopsy on an outpatient basis in Western countries. Although there have not been many, there have been some deaths within 30 days after biopsy in Taiwan [9]. Previous studies demonstrated the risk of death increased with age and were higher in patients with known co-morbidity [9,31]. Our previous study demonstrated the importance of scrupulous instructions of each detail before and after an outpatient prostate biopsy [32]. In the current study, we found that from 2000 to 2013, almost half of prostate biopsies were performed on an inpatient basis in Taiwan. Although they were older and were more likely to have diabetes mellitus, the inpatient group exhibited significantly fewer infection-related complications. The reasons included adequate pre-operative enema, proper peri-operative prophylactic antimicrobial drugs, and post-operative monitoring of voiding status, which can be provided routinely during hospitalization. There are some other reasons to do prostate biopsy on an inpatient basis in Taiwan. For example, the patient may receive the biopsy under general or spinal anesthesia because of intolerable pain and scheduled saturation biopsy. Our data showed that there was an absolute difference in the hospital admission rate, namely an approximately 1% reduction of infection-related complication, meaning that for every 100 admitted patients, the procedure can prevent one emergency room visit or hospitalization. Despite this value, cost-effectiveness requires further studies.

The reported association of the risk of post-biopsy infection with diabetes mellitus is not consistent in the current literature. Using a case-control study of 250 patients in Canada, Carignan et al. reported that 6.6% of patients had diabetes and that diabetes is an independent risk factor for post-biopsy infection [33]. Loeb et al. found, in a European screening trial (Rotterdam section), that 6.1% of patients had diabetes and that both prostate enlargement and diabetes were independent risk factors for infectious complications and hospitalization [11]. In contrast, Pinkhasov et al. reported, in their 1,000-case, single-institutional experience in Philadelphia, that there were 133 patients (13.3%) with diabetes, which was not associated with post-biopsy infection [22]. In our study, there were 19.1% patients with diabetes, and the group having inpatient procedures had a significantly higher percentage of patients with diabetes than the group biopsied as outpatients. Our results unexpectedly demonstrated that diabetic patients had significantly fewer infection-related hospitalizations. The probable reason is that inpatient care can reduce post-biopsy infection-related events.

Prostate enlargement has been thought to be an independent risk factor for infectious complication and hospitalization after prostate needle biopsy, a conclusion based on a large-scale European screening trial [11]. Those authors suggested the importance of judicious patient selection for PSA screening-related biopsy because patients with larger prostates may have a lower risk of prostate cancer but a higher risk of biopsy-related infection. Generally, the incidence of urinary retention after transrectal prostate biopsy is 0.8%–1.7% [34], which is lower than in patients having biopsy via the transperineal route (about 6.7%) [35]. However, the incidence of infection after transperineal biopsy is not higher than that after procedures performed via the transrectal route. Our data showed a history of urinary retention to be an independent risk factor for subsequent infection. The possible reason is that prostate biopsy itself can increase the difficulty of voiding in patients with prostate enlargement and contribute to more residual urine, in which uropathogenic bacteria can reproduce easily and rapidly. Moreover, urinary retention may mandate urethral catheterization, which easily inoculates bacteria into the urinary tract or even the prostate gland. Therefore, for patients with an enlarged prostate gland and a history of urinary retention, much attention and scrupulous instructions should be given before and after transrectal biopsy. Although strong evidence for their efficacy is lacking, an alpha-blocking drug should be considered, as well as a prophylactic antibiotic.

There are several limitations to the current study. First, it was not randomized, and there was heterogeneity of the studied subjects. In particular, the inpatient group usually received more attention and instruction before and after the biopsy, as these patients might be assumed to be the more susceptible or fragile ones. Second, only symptomatic patients returned and were hospitalized, which may under-estimate the real incidence of post-biopsy infection. Third, the definition of these co-morbidities might not be strict. Also, this study did not examine the utility of prophylactic antimicrobial drugs or a pre-biopsy enema. Although these strategies may be helpful to reduce the incidence of post-biopsy infection, their effectiveness may be inconsistent and influenced by patient compliance. For example, a pre-biopsy enema may not work well for each patient, particularly elderly patients, treated on an outpatient basis. Fourth, there was a 28% UTI rate and a 10% retention rate in the year prior to the biopsy. Both factors can induce PSA elevation. These numbers are somewhat higher than those in the general population. It may be that patients with any cause of PSA elevation were recommended for prostate biopsy before prescription of a 5α-reductase inhibitor for lower urinary tract symptoms according to the criteria given by the health insurance system in Taiwan. Therefore, our results may not be translated to those in countries without this rule.

Conclusions

In the current nationwide, population-based cohort study, we found that a history of urinary retention and absence of diabetes mellitus were independent factors associated with infection-related visits and hospitalization after transrectal prostate biopsy. We demonstrated that the group treated as inpatients had a significantly lower incidence of infection-related events after biopsy than did the outpatient-biopsy group, although the patients requiring hospital admission were older and exhibited more co-morbidities. These findings can provide important information on how to avoid infection-related visits and hospitalization.

Footnotes

Acknowledgments

This work was supported by a grant from the National Cheng Kung University Hospital Projects (NCKUH-10207022).

Author Disclosure Statement

None of the authors has any financial conflict of interest.

Patient consent is not necessary to access the National Health Insurance Research Database (NHIRD). The NHIRD is a nationwide, electronic database of all the beneficiaries enrolled in the National Health Insurance program. The Taiwan National Health Research Institutes (NHRI) deals with NHIRD and provides several kinds of blinded datasets. Each dataset contains complete outpatient visits, hospital admissions, prescriptions, disease, and vital status per person of one million beneficiaries randomly sampled from the NHIRD. The patients' personal information is encrypted to ensure privacy. The protocol or project can be executed without the necessity of IRB approval.

All authors have made a significant contribution to the methods and findings of the paper and read and approved the final draft. All authors agreed to publication in Surgical Infections.

This work was supported by a grant from the National Cheng Kung University Hospital Projects (NCKUH-10207022) (about US$5,000).

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