Clinical Review & Education
The Rational Clinical Examination
Does This Man With Lower Urinary Tract Symptoms Have Bladder Outlet Obstruction? The Rational Clinical Examination: A Systematic Review Karen A. D’Silva, MD, MS; Philipp Dahm, MD, MHSc; Camilla L. Wong, MD, MHSc
IMPORTANCE Early, accurate diagnosis of bladder outlet obstruction in men with lower urinary
Author Audio Interview at jama.com
tract symptoms may reduce the need for invasive testing (ie, catheter placement, urodynamics), and prompt early treatment to provide symptomatic relief and avoid complications.
Supplemental content at jama.com
OBJECTIVES To systematically review the evidence on (1) the diagnostic accuracy of
CME Quiz at jamanetworkcme.com and CME Questions page 549
office-based tests for bladder outlet obstruction in men with lower urinary tract symptoms; and (2) the accuracy of the bladder scan as a measure of urine volume because management decisions rely on measuring postvoid bladder residual volumes. DATA SOURCES AND STUDY SELECTION MEDLINE, EMBASE, and the Cochrane Central Register of Controlled Trials (1950-March 2014), along with reference lists from retrieved articles were searched to identify studies of diagnostic test accuracy among males with lower urinary tract symptoms due to bladder outlet obstruction. MEDLINE, EMBASE, CINAHL, and the Cochrane Library (1950-March 2014) were searched to identify studies of urine volumes measured with a bladder scanner vs those measured with bladder catheterization. Prospective studies were selected if they compared 1 or more office-based, noninvasive diagnostic test with the reference test or were invasive urodynamic studies, and if urine volumes were measured with a bladder scanner and bladder catheterization. DATA EXTRACTION AND SYNTHESIS For the bladder outlet obstruction objective, 8628 unique citations were identified. Ten studies (1262 patients among 9 unique cohorts) met inclusion criteria. For the bladder scan objective, 2254 unique citations were identified. Twenty studies (n = 1397 patients) met inclusion criteria. MAIN OUTCOMES AND MEASURES The first main outcome and measure was the diagnostic accuracy of individual symptoms and questionnaires compared with the reference standard (urodynamic studies) for the diagnosis of bladder outlet obstruction in males with lower urinary tract symptoms. The second was the correlation between urine volumes measured with a bladder scanner and those measured with bladder catheterization. RESULTS Among males with lower urinary tract symptoms, the likelihood ratios (LRs) of individual symptoms and questionnaires for diagnosing bladder outlet obstruction from the highest quality studies had 95% CIs that included 1.0, suggesting they are not significantly associated with one another. An International Prostate Symptom Score cutoff of 20 or greater increased the likelihood of bladder outlet obstruction (positive LR, 1.5; 95% CI, 1.1-2.0), whereas scores of less than 20 had an LR that included 1.0 in the 95% CI (negative LR, 0.82; 95% CI, 0.67-1.00). We found no data on the accuracy of physical examination findings to predict bladder outlet obstruction. Urine volumes measured by a bladder scanner correlated highly with urine volumes measured by bladder catheterization (summary correlation coefficient, 0.93; 95% CI, 0.91-0.95). CONCLUSIONS AND RELEVANCE In patients with lower urinary tract symptoms, the symptoms alone are not enough to adequately diagnose bladder outlet obstruction. A bladder scan for urine volume should be performed to assess patients with suspected large postvoid residual volumes.
JAMA. 2014;312(5):535-542. doi:10.1001/jama.2014.5555
Author Affiliations: Department of Medicine, University of Toronto, Toronto, Ontario, Canada (D’Silva, Wong); Division of Geriatrics, St Michael’s Hospital, Toronto, Ontario, Canada (D’Silva, Wong); Department of Urology, University of Florida College of Medicine, Gainesville (Dahm); Malcom Randall Veterans Affairs Medical Center, Gainesville, Florida (Dahm); Li Ka Shing Knowledge Institute, St Michael’s Hospital, Toronto, Ontario, Canada (Wong). Corresponding Author: Karen A. D’Silva, MD, MS, St Michael’s Hospital, 30 Bond St, Toronto, ON M5B 1W8, Canada (karen.dsilva@medportal.ca). Section Editors: David L. Simel, MD, MHS, Durham Veterans Affairs Medical Center and Duke University Medical Center, Durham, NC; Edward H. Livingston, MD, Deputy Editor.
535
Copyright 2014 American Medical Association. All rights reserved.
Downloaded From: http://jama.jamanetwork.com/ by a University of St. Andrews Library User on 05/11/2015
Clinical Review & Education The Rational Clinical Examination
Urinary Tract Symptoms and Bladder Obstruction
Figure. Anatomy and Spatial Relationship of the Prostate Gland to the Lower Urinary Tract
Clinical Scenario A 72-year-old man has to get up 3 times per night to urinate. Frequent, nocturnal urination has been a problem for the past several years, but has recently worsened. Despite the sensation that his bladder is full, initiating urination has become more difficult during the last few months and he often has a very weak urine stream. Several episodes of urinary incontinence occurred the week he was evaluated by his physician. He does not have hematuria, dysuria, prior urinary tract infection (UTI), or other history of prostate or urinary tract problems. When evaluating this patient, which lower urinary tract symptoms are most suggestive of bladder outlet obstruction?
VIEW
Prostate gland
Vas deferens BLADDER
Detrusor muscle scle
Seminal vesicle
Bladder neck
RECTUM
Prostatic urethra
Background Bladder outlet obstruction causes several clinical symptoms including a weak urine stream, a sensation of incomplete urination, and urinary frequency. These symptoms are referred to as lower urinary tract symptoms. Lower urinary tract symptoms include voiding or obstructive symptoms such as hesitancy; poor or intermittent stream, or both; straining; prolonged micturition; dribbling; and storage or irritative symptoms such as frequency, urgency, urge incontinence, and nocturia.1 The most commonly reported lower urinary tract symptoms include urinary hesitancy, weak urine stream, and nocturia.2 Benign prostatic hyperplasia (BPH) frequently causes lower urinary tract symptoms and is very common in men older than 60 years. Among individuals aged 81 to 90 years, the prevalence of BPH approaches 90%.3,4 Benignprostatichyperplasiaisassociatedwithbenignsmooth muscle and epithelial cell proliferation within the prostate’s transition zone.5 The transition zone has 2 lobes and surrounds the proximal urethra (Figure). The prostate is located at the base of the bladder and contains the prostatic urethra. Cellular hyperplasia expands the transition zone volume, compressing the urethra and resulting in bladder outlet obstruction and subsequent lower urinary tract symptoms. Benign prostatic hyperplasia does not always result in bladder outlet obstruction and patients with BPH may be asymptomatic. In older men, lower urinary tract symptoms may be caused by many clinical conditions (Box 1). Causes of lower urinary tract symptoms other than BPH can be important6 and include structural or functional abnormalities of the lower urinary tract7 (Box 1). Prescription drugs such as antidepressants, antihistamines, bronchodilators, anticholinergics, and sympathomimetics can cause or exacerbate lower urinary tract symptoms because of their effects on detrusor muscle and urinary sphincter function. Diuretics increase urine volume and can cause lower urinary tract symptoms.8 An overactive bladder associated with impaired detrusor muscle contractility may by itself or in combination with other diseases cause lower urinary tract symptoms. Bladder overactivity often causes lower urinary tract symptoms in men who were unresponsive to therapy and initially thought to have bladder outlet obstruction.6 Several complications may result if bladder outlet obstruction is untreated, highlighting the need to establish its underlying cause.6,9 These complications include recurrent UTI, bladder stones, overflow incontinence, gross hematuria, hydronephrosis, acute urinary retention, and renal disease.2 Symptoms related to bladder outlet obstruction are detrimental to a patient’s quality of life and re536
Ejaculatory duct
Membranous urethra
External urethral sphincter
Bulbous urethra
Prostatic urethra
Periurethral tissue Ejaculatory ducts
CROSS SECTION
Prostatic urethra
LEVEL OF CROSS SECTION
ANTERIOR
Transition zone Prostate gland
Periurethral tissue ANTERIOR
This diagram illustrates the normal spatial relationship of the prostate gland to the bladder, urethra, and rectum. From the bladder neck, the prostatic urethra runs through the entire length of the prostate gland before becoming the membranous urethra where it traverses the external urethral sphincter. These close relationships help to illustrate how enlargement of the transition zone, which surrounds the prostatic urethra, may result in bladder outlet obstruction.
sult in a large number of outpatient visits.2,4,5 In the United States, almost 8 million visits were made in 2000 by patients with a primary or secondary diagnosis of BPH.10 Population-based assessments show that outpatient office visits for bladder outlet obstruction in Canada increased by more than 50% between 2000 and 2004. These increases in outpatient visits place a significant burden on the health care system at large. In the United States, the direct cost of medical services for treatment of BPH provided at hospital inpatient and outpatient settings, emergency departments, and physician offices was estimated to be $1.1 billion in 2000.10 Most patients with lower urinary tract symptoms will first present to their primary care practitioner.2,11 Recognition of risk factors associated with bladder outlet obstruction at initial presentation identifies patients at risk for complications who might benefit from medical treatment (α-blockers, 5-α reductase inhibitors, or both) or specialist referral to avoid complications. The reference standard tests for diagnosing bladder outlet obstruction are invasive pressure-flow studies, which are referred to as urodynamic studies and are performed by urologists. Urodynamic studies are performed in 2 phases to provide an assessment of the main functions of the bladder, which are urine storage at low pressure (filling phase) and effective voluntary empty-
JAMA August 6, 2014 Volume 312, Number 5
Copyright 2014 American Medical Association. All rights reserved.
Downloaded From: http://jama.jamanetwork.com/ by a University of St. Andrews Library User on 05/11/2015
jama.com
Urinary Tract Symptoms and Bladder Obstruction
ing (voiding phase). It involves placement of a small catheter to slowly fill the bladder with normal saline as well as to measure the pressure in the bladder. An intrarectal probe is also placed to measure the intraabdominal pressure. During the voiding phase, external measurement of urinary flow as well as the detrusor pressure (calculated by subtracting the intraabdominal pressure from the intravesical pressure) allows the generation of various indices of bladder outlet resistance (eg, the Abrams-Griffiths nomogram) to make a diagnosis of bladder outlet obstruction. The underlying principle is that detrusor pressure during micturition reflects outlet resistance with the hallmark of bladder outlet obstruction being a high-pressure, lowflow system.12 In the Abrams-Griffiths nomogram, maximal urinary flow while voiding is plotted against the corresponding voiding detrusor pressure to make a determination whether the bladder outlet is obstructed, unobstructed, or equivocally obstructed. Quantifying the extent of lower urinary tract symptoms provides valuable information on severity of disease, response to therapy, and symptom progression.5,13-15 Although there are many surveys, the most commonly used questionnaire is the American Urological Association Symptom Index, also known as the International Prostate Symptom Score (IPSS).5 The questionnaire was originally designed in 1992 to quantify the intensity of symptoms from BPH.16 It was then adapted by the World Health Organization in 1993 to create the IPSS based on the 7 original questions of the American Urological Association Symptom Index plus 1 question to assess the degree to which patients find their symptoms bothersome, now known as the bother score.17 The IPSS and the American Urological Association Symptom Index are often used interchangeably. In this article, the index will be referred to as the IPSS. Because the initial presentation of symptoms will probably occur in the office of the nonspecialist or primary care practitioner, it is important to evaluate the diagnostic accuracy of the commonly used screening methods for bladder outlet obstruction. The objective of this systematic review was to determine the diagnostic accuracy of individual symptoms and questionnaires compared with urodynamic studies (the reference standard) for the diagnosis of bladder outlet obstruction in males with lower urinary tract symptoms. A secondary objective was to determine the correlation of retained urine volumes measured by bladder scanners and those measured by bladder catheterization. Normal bladder function results in emptying to completion with no retained urine volume, or a postvoid residual volume of zero. Therefore, increasing postvoid residual volumes reflect deterioration of emptying function. Although there is currently no standardized definition of a normal postvoid residual urine volume, the widely accepted value is less than 200 mL.18 Large postvoid residual volumes of 200 mL or greater indicate substantially diminished bladder emptying, which is a risk factor for the development of UTIs. Potential long-term complications of worsening bladder emptying include acute renal failure and urinary retention.
Methods Literature Search Strategy Searches of MEDLINE, EMBASE, and the Cochrane Central Register of Controlled Trials (from 1950-March 2014) were completed to iden-
The Rational Clinical Examination Clinical Review & Education
Box 1. Causes of Lower Urinary Tract Symptoms Other Than Bladder Outlet Obstruction Secondary to Benign Prostatic Hyperplasia Urethral stricture Primary bladder neck obstruction Bladder neck contracture Meatal stenosis Bladder dysfunction (ie, overactive bladder) Urinary tract infections Malignancies (ie, bladder cancer, prostate cancer) Chronic pelvic pain conditions (ie, prostatitis, interstitial cystitis) Medications (ie, diuretics) General medical conditions (ie, congestive heart failure) Nervous system dysfunction Stroke Parkinson disease Adapted from Abrams et al,6 2013, and Abrams et al,7 2002.
tify diagnostic studies of patients with lower urinary tract symptoms due to bladder outlet obstruction. The search strategy used terms, including benign prostatic hyperplasia, lower urinary tract symptoms, and prostatitis, combined with validated search filters for retrievingarticles19,20 onthediagnosisofhealthdisorders(eAppendix in the Supplement). Additional articles were hand searched by reviewing the reference lists of the included original research studies as well as those of review articles and editorials on this topic. In addition, we contacted experts in the field to identify unpublished studies relevant to this topic. A second literature search was conducted to identify studies using a bladder scanner, which is a portable bedside tool, as a measure of urine volume. This second search included MEDLINE, EMBASE, CINAHL, and the Cochrane Library (from 1950-March 2014). The search terms bladder scanner, portable ultrasound, and bladder ultrasound were used (eAppendix in the Supplement). Appropriate wild cards were used in the search strategy to account for plurals and variations in spelling.
Study Selection and Data Extraction To identify diagnostic studies for patients with lower urinary tract symptoms due to bladder outlet obstruction, inclusion criteria were chosen to select prospective studies of findings (history, physical examination, simple bedside tests) in adult men conducted in a primary care or other clinical setting. The study populations included inpatients or outpatients with at least 1 type of lower urinary tract symptom. The studies must have included at least 1 diagnostic (or index) test compared with urodynamic studies (the reference standard test). The diagnostic test used in each study had to be readily available to nonspecialist clinicians to be eligible for inclusion. The study must have applied the same diagnostic test to most patients (>90%), applied the same reference tests to all patients, and included participants with and without bladder outlet obstruction. Additionally, primary data or appropriate summary statistics had to be available. When necessary, additional data were obtained by contacting individual study authors. The reference standard was bladder outlet obstruction identified by urodynamic studies. Studies of
jama.com
JAMA August 6, 2014 Volume 312, Number 5
Copyright 2014 American Medical Association. All rights reserved.
Downloaded From: http://jama.jamanetwork.com/ by a University of St. Andrews Library User on 05/11/2015
537
Urinary Tract Symptoms and Bladder Obstruction
The Rational Clinical Examination Clinical Review & Education
Scenario Resolution Lower urinary tract symptoms are very common and nonspecific in aging men. In this 72-year-old patient, the pretest probability of bladder outlet obstruction is 64% based on the studies in this review. His IPSS was 21 (bladder emptying = 4, frequency = 2, intermittency = 2, urgency = 2, weak stream = 5, strain = 3, nocturia = 3) and was obtained to quantify the intensity of his symptoms. A complete medical history, a physical examination with digital rectal examination, and a focused examination to assess for other causes of voiding dysfunction including infection, medication use, other systemic disease, or underlying malignancy did not reveal any positive findings. Using an IPSS of 20 or greater, a positive LR of 1.5 could be applied, resulting in a 73% posttest probability of bladder outlet obstruction. The IPSS quantifies the symptom intensity and the amount of bother experienced by the patient. A bladder scan performed postvoid revealed 350 mL of urine indicated inefficient bladder emptying as a risk factor for UTIs, which indicates the development of hydronephrosis, acute renal disease, and urinary retention. Catheterization was unnecessary because of the known high correlation with bladder scan results. The patient was referred to a urologist who initiated a trial of an α-blocker and a 5-α reductase inhibitor. Only mild improvement in symptoms resulted. Recent clinical practice guidelines recommend that urodynamic studies
ARTICLE INFORMATION Author Contributions: Dr D’Silva had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Dahm, Wong. Acquisition, analysis, or interpretation of data: All authors. Drafting of the manuscript: D’Silva, Dahm. Critical revision of the manuscript for important intellectual content: D’Silva, Wong. Statistical analysis: D’Silva, Wong. Administrative, technical, or material support: D’Silva. Study supervision: Dahm, Wong. Conflict of Interest Disclosures: The authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Dr Wong reported receiving other from Li Ka Shing Knowledge Institute during the conduct of the study and outside the submitted work. No other disclosures were reported. Additional Contributions: We thank Laure Perrier, MEd, MLIS (Faculty of Medicine, Continuing Education, and Professional Development, University of Toronto, Toronto, Ontario, Canada), for her assistance in the literature search, and Bessie Audet, HCPNS (St Michael’s Hospital, Toronto, Ontario, Canada), for retrieval of relevant articles. We also appreciate the suggestions on earlier versions of the manuscript from Daniella Zipkin, MD (Duke University, Durham, North Carolina), S. Nicole Hastings, MD, MHS (Durham Veterans Affairs Medical Center and Duke University, Durham, North Carolina), and Sheri A. Keitz, MD, PhD (University of Miami Miller School of Medicine, Miami, Florida). We also thank Molly
confirm bladder outlet obstruction prior to proceeding with invasive ablative therapies such as transurethral resection of the prostate.60 Therefore, urodynamic studies were performed to confirm bladder outlet obstruction. After a thorough discussion about the expected benefits, risks, complications, and alternative approaches such as laser ablation, the patient underwent an uncomplicated transurethral resection of the prostate. A follow-up visit 3 months later revealed a subjectively much improved urinary stream and sensation of bladder emptying. The IPSS was 8.
The Bottom Line Among men with lower urinary tract symptoms, the IPSS quantifies the symptoms experienced by the patient along with a measure for the bother caused by the symptoms. However, each lower urinary tract symptom and the IPSS have poor diagnostic accuracy for bladder outlet obstruction. Given that the prevalence of bladder outlet obstruction is high among older men with lower urinary tract symptoms, a bladder scan provides a noninvasive and reliable approach to determine whether the patient has substantial postvoid residual volumes, thereby making it unnecessary for bladder catheterization in the patient as well as providing a useful tool for serial examinations to assess changes in urine volume suggestive of worsening disease.
Neuberger (Department of Urology, University of Florida, Gainesville) for her assistance in proofreading the manuscript. Financial compensation was not provided for any of these contributions. REFERENCES 1. Chapple CR, Wein AJ, Abrams P, et al. Lower urinary tract symptoms revisited: a broader clinical perspective. Eur Urol. 2008;54(3):563-569. 2. Tanguay S, Awde M, Brock G, et al. Diagnosis and management of benign prostatic hyperplasia in primary care. Can Urol Assoc J. 2009;3(3)(suppl 2): S92-S100. 3. Berry SJ, Coffey DS, Walsh PC, Ewing LL. The development of human benign prostatic hyperplasia with age. J Urol. 1984;132(3):474-479. 4. Carballido J, Fourcade R, Pagliarulo A, et al. Can benign prostatic hyperplasia be identified in the primary care setting using only simple tests? results of the Diagnosis IMprovement in PrimAry Care Trial. Int J Clin Pract. 2011;65(9):989-996. 5. McVary KT, Roehrborn CG, Avins AL, et al. Update on AUA guideline on the management of benign prostatic hyperplasia. J Urol. 2011;185(5): 1793-1803. 6. Abrams P, Chapple C, Khoury S, et al; International Consultation on New Developments in Prostate Cancer and Prostate Diseases. Evaluation and treatment of lower urinary tract symptoms in older men. J Urol. 2013;189(1)(suppl): S93-S101. 7. Abrams P, Cardozo L, Fall M, et al; Standardisation Sub-committee of the International Continence Society. The standardisation of
jama.com
terminology of lower urinary tract function. Neurourol Urodyn. 2002;21(2):167-178. 8. Wuerstle MC, Van Den Eeden SK, Poon KT, et al; Urologic Diseases in America Project. Contribution of common medications to lower urinary tract symptoms in men. Arch Intern Med. 2011;171(18): 1680-1682. 9. Madersbacher S, Klingler HC, Djavan B, et al. Is obstruction predictable by clinical evaluation in patients with lower urinary tract symptoms? Br J Urol. 1997;80(1):72-77. 10. Wei JT, Calhoun E, Jacobsen SJ. Urologic diseases in America project: benign prostatic hyperplasia. J Urol. 2008;179(5)(suppl):S75-S80. 11. AUA Practice Guidelines Committee. AUA guideline on management of benign prostatic hyperplasia (2003), chapter 1: diagnosis and treatment recommendations. J Urol. 2003;170(2 pt 1):530-547. 12. Nitti VW. Pressure flow urodynamic studies: the gold standard for diagnosing bladder outlet obstruction. Rev Urol. 2005;7(suppl 6):S14-S21. 13. Barry MJ, Fowler FJ Jr, O’Leary MP, et al; Measurement Committee of the American Urological Association. Measuring disease-specific health status in men with benign prostatic hyperplasia. Med Care. 1995;33(4)(suppl):AS145AS155. 14. Donovan JL, Kay HE, Peters TJ, et al. Using the ICSOoL to measure the impact of lower urinary tract symptoms on quality of life: evidence from the ICS-‘BPH’ Study: International Continence Society—Benign Prostatic Hyperplasia. Br J Urol. 1997;80(5):712-721. 15. Hald T, Nordling J, Andersen JT, et al. A patient weighted symptom score system in the evaluation JAMA August 6, 2014 Volume 312, Number 5
Copyright 2014 American Medical Association. All rights reserved.
Downloaded From: http://jama.jamanetwork.com/ by a University of St. Andrews Library User on 05/11/2015
541
Urinary Tract Symptoms and Bladder Obstruction
The Rational Clinical Examination Clinical Review & Education
Table. Summary Data for Diagnostic Accuracy of Questionnaires and Symptoms for Diagnosing Bladder Outlet Obstruction From Level 3 Studiesa
Diagnostic Test by Threshold
Sample Size
Bladder Outlet Obstruction Prevalence, No./Total (%)
Age, y
Sensitivity (95% CI), %
Specificity (95% CI), %
Positive LR (95% CI)b
Negative LR (95% CI)b
Diagnostic OR (95% CI)
IPSS/AUA Symptom Index ≥20 Steele et al,32 2000
204
Mean, 67
152/204 (74)
46 (38-54)
67 (53-80)
1.40 (0.92-2.20)
0.80 (0.63-1.00)
1.80 (0.91-3.40)
van Venrooij et al,33 2008
160
Mean, 65
87/160 (54)
44 (33-55)
75 (64-85)
1.8 (1.1-2.8)
0.75 (0.60-0.94)
2.4 (1.2-4.7)
78
Mean, 68
62/78 (79)
29 (18-42)
69 (41-89)
0.93 (0.41-2.10)
1.00 (0.72-1.50)
0.90 (0.27-3.00)
41 (30-52)
71 (63-78)
1.5 (1.1-2.0); I2 = 75%
0.82 (0.67-1.00); I2 = 6.4%
1.8 (1.2-2.8)
75/160 (47)
69 (58-79)
41 (31-52)
1.20 (0.93-1.50)
0.75 (0.49-1.10)
1.60 (0.82-3.00)
152/204 (74)
Yalla et al,34 1995 Summary IPSS ≥14 Oelke et al,35 2007
160
Median, 62
Steele et al,32 2000
204
Mean, 67
91 (86-95)
14 (6-26)
1.10 (0.94-1.20)
0.64 (0.27-1.50)
1.70 (0.63-4.43)
van Venrooij et al,33 2008
160
Mean, 65
54 (87/160)
97 (90-99)
12 (6-22)
1.1 (1.0-1.2)
0.28 (0.08-1.00)
3.9 (1.0-15.1)
78
Mean, 68
62/78 (79)
86 (74-93)
0 (0-21)
0.88 (0.77-1.00)
5.10 (0.31-84.00)
0.17 (0.01-3.09)
91 (85-95)
12 (8-19)
1.00 (0.89-1.10); I2 = 75%
0.58 (0.28-1.20); I2 = 44%
1.60 (0.49-5.40)
IPSS/AUA Symptom Index ≥8
Yalla et al,34 1995 Summary Intermittent stream29
157
Median, 68
95/157 (60)
23 (15-33)
82 (71-91)
1.30 (0.68-2.50)
0.93 (0.80-1.10)
1.40 (0.62-3.10)
Terminal dribbling29
155
Median, 68
94/155 (61)
50 (40-61)
57 (44-70)
1.20 (0.82-1.70)
0.87 (0.65-1.20)
1.30 (0.79-2.60)
Abbreviations: AUA, American Urological Association; IPSS, International Prostate Symptom Score; LR, likelihood ratio; OR, odds ratio. a
The results from studies with a quality level of 4 or 5 appear in the Supplement.
population examined in 2 reports,29,30 93% to 95% of the participants received the diagnostic tests.
Prevalence of Bladder Outlet Obstruction From the quality level 3 studies, bladder outlet obstruction occurred in more than half the patients with lower urinary tract symptoms (summary prevalence, 64%; 95% CI, 52%-74%).29,30,32-35 Considering studies of all quality levels, the highest prevalence, 79%, was in a study (quality level 3) of patients referred to a US Veteran Affairs urology clinic34 and the lowest, 38%, was in a study (quality level 4) of patients referred to a continence clinic in Singapore (eTable 1 in the Supplement).28
Accuracy of Symptoms in the Diagnosis of Bladder Outlet Obstruction The Table displays the summary data for diagnostic accuracy of questionnaires and symptoms for diagnosing bladder outlet obstruction from the highest quality studies (all quality level 3). The studies examined a variety of lower urinary tract symptoms, including the presence of poor urine stream, nocturia, frequency, intermittent stream, urge incontinence, manual compression, straining, terminal dribbling, urgency, hesitancy, and sensation of incomplete emptying (eTable 2 in the Supplement) with respect to diagnosing bladder outlet obstruction. Among these, only the presence of an intermittent stream or terminal dribbling were evaluated in level 3 studies and both had LRs with 95% CIs that included 1.0. In the studies of lesser quality among patients referred for evaluation of incontinence, the complaint of a poor stream increased the likelihood of bladder outlet obstruction (positive LR, 1.7; 95% CI, 1.1-2.5), whereas
b
Heterogeneity was explored using I2, which describes the percentage of total variation across studies that is due to heterogeneity rather than chance (I2 value of 25% categorized as low; 50%, moderate; and 75%, high).
the absence of nocturia (negative LR, 0.19; 95% CI, 0.05-0.79) made bladder outlet obstruction less likely (Table).28 The IPSS was studied most frequently in the highest quality studies at thresholds of 20 or greater (severe symptoms) and 8 or greater (moderate symptoms) to determine if the results predict bladder outlet obstruction (Table). The positive LR for bladder outlet obstruction might have increased slightly from lower to higher thresholds, but even at a greater severity with an IPSS of 20 or greater, the positive LR was only 1.5 (95% CI, 1.1-2.0). Likewise, the ability of the IPSS to rule out bladder outlet obstruction improved as the symptoms decreased. However, even at the lowest threshold (IPSS <8), the negative LR was only 0.58 (95% CI, 0.28-1.20). Thus, the IPSS results did not have much effect on the probability of bladder outlet obstruction beyond the baseline prevalence among patients with lower urinary tract symptoms and therefore were of limited clinical utility.
Accuracy of Physical Examination for the Diagnosis of Bladder Outlet Obstruction Many studies included the use of the digital rectal examination but none had data on its diagnostic accuracy. There were no studies that met our inclusion criteria in which the rectal examination for prostate enlargement or bladder percussion was compared with a reference standard for bladder outlet obstruction.
Accuracy of Bladder Scanner for Assessment of Urine Volume We identified 2254 citations that compared assessment of urine volume by bladder scan with bladder catheterization, of which 57 unique studies were retrieved for full-text review and 20 studies37-56 met
jama.com
JAMA August 6, 2014 Volume 312, Number 5
Copyright 2014 American Medical Association. All rights reserved.
Downloaded From: http://jama.jamanetwork.com/ by a University of St. Andrews Library User on 05/11/2015
539
Clinical Review & Education The Rational Clinical Examination
the inclusion criteria (eFigure 2 in the Supplement). The included studies varied in sample size from 15 to 186 (eTable 3 in the Supplement). In the 14 studies* that specified the range of urine volumes measured with bladder catheterization, the range was 0 to 1269 mL. Fourteen studies† examined the correlation between urine volumes measured with a bladder scanner and postvoid residual volumes, and 8 studies38,41,47-50,53,55 examined the correlation between urine volumes measured with a bladder scanner and prevoid urine volumes. The patient populations were varied, containing both men and women, and being conducted in inpatient and outpatient, and acute care and rehabilitation settings (eTable 3 in the Supplement). The summary correlation coefficient was r = 0.93 (95% CI, 0.91-0.95). This suggests that the urine volumes measured with a bladder scanner and those measured with bladder catheterization were highly correlated. There was heterogeneity (I2 = 88%), but no evidence of publication bias (Begg and Mazumdar rank correlation, P = .36).
Limitations Diagnostic accuracy studies frequently had a high risk of bias related to patient selection.21 The level 4 studies27,28,36 lacked an independent comparison of signs and symptoms with a reference standard for patient selection and had narrowly defined patient populations (eTable 4 in the Supplement). In 4 of the 5 level 3 studies, consecutive sampling was used but these studies did not clearly define the spectrum of disease, range, and relative frequency of alternative conditions in the patient populations without bladder obstruction (eTable 4 in the Supplement). This review was further limited by the small number of studies fitting the selection criteria and the small sample sizes of the studies. Most of the reviewed studies lacked a blinded, independent assessment of urodynamic studies (eTable 1 in the Supplement). The main limitation of the bladder scanner assessment was reliance on the correlation coefficient between bladder scanning and catheterization, although only 5 of 22 studies reported differences between urine volumes measured with bladder catheterization and those measured with a bladder scanner. Those that did are summarized in eTable 3 in the Supplement. All of these studies used the means, rather than the medians, as the measure to express the central tendency for measured differences. Means are susceptible to outlying values and can overstate discrepancy. In the study by Schott-Baer and Reaume,53 the mean difference score (ie, actual urine volume minus scan volume) was 79 mL. Fifty percent of the urine volumes were underestimated by the bladder scanner. In the group of patients that had lower actual urine volumes (range, 200-800 mL), 25% (or 12 patients) had difference scores of 20 mL or less. In the group of patients with larger actual urine volumes (range, 375-900 mL), 10% of patients had difference scores greater than 100 mL. Cardenas et al40 found that the mean of the differences between urine volumes was 56 mL. When actual urine volumes of greater than 500 mL were excluded, the mean difference was reduced to 37 mL. Considering only small actual urine volumes of 200 mL or less, the mean difference was 25 mL. The bladder scanner was found to underestimate the actual urine volumes. In the study by Massagli et al,48 actual urine vol*References 38-42, 44, 45, 47-50, 53, 54, 56 †References 37, 39, 40, 42-46, 49, 51-54, 56 540
Urinary Tract Symptoms and Bladder Obstruction
umes ranged from 2 mL to 500 mL and mean differences were about 14 mL for “experienced” personnel. Coombes and Millard43 looked at 2 different types of scanners in their study. The mean difference in urine volume for the 2-step BVI 2500 unit was 41 mL. Over- and underestimations of bladder volume were found in 50% of patients. For the 1-step BVI 2500+, the mean difference in urine volume was 24 mL. In this group, the bladder scanner tended to slightly underestimate actual urine volumes. Choe et al42 also examined 2 different scanning devices. The mean difference in bladder urine volume for the BME-150A unit was 7.8 mL and with the BVI 3000 it was 3.6 mL. Notably, in plotting the mean differences according to range of actual urine volume, the greatest mean difference was seen in the group with the largest actual volumes (>400 mL). In this study, there were 6 cases in which postvoid residual volume measurements had overestimated actual urine volumes. These patients were later diagnosed with various pelvic pathologies, including ovarian hemorrhagic cyst and uterine myoma. The results from these studies indicate that larger urine volumes are more vulnerable to discrepancies in measurement. However, discrepancies are usually not clinically relevant because the purpose of measuring residual volumes is simply to recognize whether there is significant urine retention. The techniques of both bladder scanning and catheterization for measuring residual urine volume can be limited in the presence of structural pathology. When there is a high index of suspicion that actual urine volumes are nearing diagnostic thresholds, it would be prudent to do serial bladder scanning to avoid misclassification from the measurement itself but also from daily variations in urinary events.
Discussion The low positive LR associated with questionnaires and symptoms implies that these are not useful for diagnosing bladder outlet obstruction. Lower urinary tract symptoms in men are usually attributed to benign prostatic hypertrophy causing bladder outlet obstruction. Questionnaires may fail to identify the correct diagnosis for bladder outlet obstruction because they may lack specificity for identifying other causes for lower urinary tract symptoms, including drugs,8 nervous system, renal, cardiovascular, and respiratory disease or dysfunction.6 The precision of the IPSS as a tool is limited by potentially inaccurate patient recall of symptoms and willingness to report urinary symptoms, which may depend on education, cognitive abilities, and cross-cultural differences in perception.57,58 A patient’s symptoms may fluctuate because of comorbid illness, medication use, and hydration status. These may influence the accurate categorization of disease severity depending on the timing of questionnaire administration.59 The IPSS as a tool may reliably measure treatment response once a diagnosis has been established. Even though guidelines from urological associations recommend the initial evaluation of males with lower urinary tract symptoms to include a digital rectal examination and prostate-specific antigen measurement,5 based on the present review, evidence is lacking for both of these tests as markers for bladder outlet obstruction. The utility of these diagnostic tests for other conditions was beyond the scope of this study.
JAMA August 6, 2014 Volume 312, Number 5
Copyright 2014 American Medical Association. All rights reserved.
Downloaded From: http://jama.jamanetwork.com/ by a University of St. Andrews Library User on 05/11/2015
jama.com
Urinary Tract Symptoms and Bladder Obstruction
The Rational Clinical Examination Clinical Review & Education
Scenario Resolution Lower urinary tract symptoms are very common and nonspecific in aging men. In this 72-year-old patient, the pretest probability of bladder outlet obstruction is 64% based on the studies in this review. His IPSS was 21 (bladder emptying = 4, frequency = 2, intermittency = 2, urgency = 2, weak stream = 5, strain = 3, nocturia = 3) and was obtained to quantify the intensity of his symptoms. A complete medical history, a physical examination with digital rectal examination, and a focused examination to assess for other causes of voiding dysfunction including infection, medication use, other systemic disease, or underlying malignancy did not reveal any positive findings. Using an IPSS of 20 or greater, a positive LR of 1.5 could be applied, resulting in a 73% posttest probability of bladder outlet obstruction. The IPSS quantifies the symptom intensity and the amount of bother experienced by the patient. A bladder scan performed postvoid revealed 350 mL of urine indicated inefficient bladder emptying as a risk factor for UTIs, which indicates the development of hydronephrosis, acute renal disease, and urinary retention. Catheterization was unnecessary because of the known high correlation with bladder scan results. The patient was referred to a urologist who initiated a trial of an α-blocker and a 5-α reductase inhibitor. Only mild improvement in symptoms resulted. Recent clinical practice guidelines recommend that urodynamic studies
ARTICLE INFORMATION Author Contributions: Dr D’Silva had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Dahm, Wong. Acquisition, analysis, or interpretation of data: All authors. Drafting of the manuscript: D’Silva, Dahm. Critical revision of the manuscript for important intellectual content: D’Silva, Wong. Statistical analysis: D’Silva, Wong. Administrative, technical, or material support: D’Silva. Study supervision: Dahm, Wong. Conflict of Interest Disclosures: The authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Dr Wong reported receiving other from Li Ka Shing Knowledge Institute during the conduct of the study and outside the submitted work. No other disclosures were reported. Additional Contributions: We thank Laure Perrier, MEd, MLIS (Faculty of Medicine, Continuing Education, and Professional Development, University of Toronto, Toronto, Ontario, Canada), for her assistance in the literature search, and Bessie Audet, HCPNS (St Michael’s Hospital, Toronto, Ontario, Canada), for retrieval of relevant articles. We also appreciate the suggestions on earlier versions of the manuscript from Daniella Zipkin, MD (Duke University, Durham, North Carolina), S. Nicole Hastings, MD, MHS (Durham Veterans Affairs Medical Center and Duke University, Durham, North Carolina), and Sheri A. Keitz, MD, PhD (University of Miami Miller School of Medicine, Miami, Florida). We also thank Molly
confirm bladder outlet obstruction prior to proceeding with invasive ablative therapies such as transurethral resection of the prostate.60 Therefore, urodynamic studies were performed to confirm bladder outlet obstruction. After a thorough discussion about the expected benefits, risks, complications, and alternative approaches such as laser ablation, the patient underwent an uncomplicated transurethral resection of the prostate. A follow-up visit 3 months later revealed a subjectively much improved urinary stream and sensation of bladder emptying. The IPSS was 8.
The Bottom Line Among men with lower urinary tract symptoms, the IPSS quantifies the symptoms experienced by the patient along with a measure for the bother caused by the symptoms. However, each lower urinary tract symptom and the IPSS have poor diagnostic accuracy for bladder outlet obstruction. Given that the prevalence of bladder outlet obstruction is high among older men with lower urinary tract symptoms, a bladder scan provides a noninvasive and reliable approach to determine whether the patient has substantial postvoid residual volumes, thereby making it unnecessary for bladder catheterization in the patient as well as providing a useful tool for serial examinations to assess changes in urine volume suggestive of worsening disease.
Neuberger (Department of Urology, University of Florida, Gainesville) for her assistance in proofreading the manuscript. Financial compensation was not provided for any of these contributions. REFERENCES 1. Chapple CR, Wein AJ, Abrams P, et al. Lower urinary tract symptoms revisited: a broader clinical perspective. Eur Urol. 2008;54(3):563-569. 2. Tanguay S, Awde M, Brock G, et al. Diagnosis and management of benign prostatic hyperplasia in primary care. Can Urol Assoc J. 2009;3(3)(suppl 2): S92-S100. 3. Berry SJ, Coffey DS, Walsh PC, Ewing LL. The development of human benign prostatic hyperplasia with age. J Urol. 1984;132(3):474-479. 4. Carballido J, Fourcade R, Pagliarulo A, et al. Can benign prostatic hyperplasia be identified in the primary care setting using only simple tests? results of the Diagnosis IMprovement in PrimAry Care Trial. Int J Clin Pract. 2011;65(9):989-996. 5. McVary KT, Roehrborn CG, Avins AL, et al. Update on AUA guideline on the management of benign prostatic hyperplasia. J Urol. 2011;185(5): 1793-1803. 6. Abrams P, Chapple C, Khoury S, et al; International Consultation on New Developments in Prostate Cancer and Prostate Diseases. Evaluation and treatment of lower urinary tract symptoms in older men. J Urol. 2013;189(1)(suppl): S93-S101. 7. Abrams P, Cardozo L, Fall M, et al; Standardisation Sub-committee of the International Continence Society. The standardisation of
jama.com
terminology of lower urinary tract function. Neurourol Urodyn. 2002;21(2):167-178. 8. Wuerstle MC, Van Den Eeden SK, Poon KT, et al; Urologic Diseases in America Project. Contribution of common medications to lower urinary tract symptoms in men. Arch Intern Med. 2011;171(18): 1680-1682. 9. Madersbacher S, Klingler HC, Djavan B, et al. Is obstruction predictable by clinical evaluation in patients with lower urinary tract symptoms? Br J Urol. 1997;80(1):72-77. 10. Wei JT, Calhoun E, Jacobsen SJ. Urologic diseases in America project: benign prostatic hyperplasia. J Urol. 2008;179(5)(suppl):S75-S80. 11. AUA Practice Guidelines Committee. AUA guideline on management of benign prostatic hyperplasia (2003), chapter 1: diagnosis and treatment recommendations. J Urol. 2003;170(2 pt 1):530-547. 12. Nitti VW. Pressure flow urodynamic studies: the gold standard for diagnosing bladder outlet obstruction. Rev Urol. 2005;7(suppl 6):S14-S21. 13. Barry MJ, Fowler FJ Jr, O’Leary MP, et al; Measurement Committee of the American Urological Association. Measuring disease-specific health status in men with benign prostatic hyperplasia. Med Care. 1995;33(4)(suppl):AS145AS155. 14. Donovan JL, Kay HE, Peters TJ, et al. Using the ICSOoL to measure the impact of lower urinary tract symptoms on quality of life: evidence from the ICS-‘BPH’ Study: International Continence Society—Benign Prostatic Hyperplasia. Br J Urol. 1997;80(5):712-721. 15. Hald T, Nordling J, Andersen JT, et al. A patient weighted symptom score system in the evaluation JAMA August 6, 2014 Volume 312, Number 5
Copyright 2014 American Medical Association. All rights reserved.
Downloaded From: http://jama.jamanetwork.com/ by a University of St. Andrews Library User on 05/11/2015
541
Clinical Review & Education The Rational Clinical Examination
of uncomplicated benign prostatic hyperplasia. Scand J Urol Nephrol Suppl. 1991;138:59-62. 16. Barry MJ, Fowler FJ Jr, O’Leary MP, et al; The Measurement Committee of the American Urological Association. The American Urological Association Symptom Index for benign prostatic hyperplasia. J Urol. 1992;148(5):1549-1557. 17. Rhodes PR, Krogh RH, Bruskewitz RC. Impact of drug therapy on benign prostatic hyperplasia-specific quality of life. Urology. 1999;53 (6):1090-1098. 18. Thüroff JW, Abrams P, Andersson KE, et al. EAU guidelines on urinary incontinence. Eur Urol. 2011; 59(3):387-400. 19. Wilczynski NL, Haynes RB; Hedges Team. EMBASE search strategies for identifying methodologically sound diagnostic studies for use by clinicians and researchers. BMC Med. 2005;3:7. 20. Haynes RB, Wilczynski NL. Optimal search strategies for retrieving scientifically strong studies of diagnosis from Medline: analytical survey. BMJ. 2004;328(7447):1040. 21. Bossuyt PM, Reitsma JB, Bruns DE, et al; STARD group. Towards complete and accurate reporting of studies of diagnostic accuracy: the STARD initiative. Ann Clin Biochem. 2003;40(pt 4):357-363. 22. Whiting PF, Rutjes AW, Westwood ME, et al; QUADAS-2 Group. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155(8):529-536. 23. Sackett D. Update: primer on precision and accuracy. In: Simel D, Rennie D, eds. Rational Clinical Examination: The Evidence-Based Clinical Diagnosis. New York, NY: McGraw-Hill; 2008:9-16. 24. Simel DL, Samsa GP, Matchar DB. Likelihood ratios with confidence: sample size estimation for diagnostic test studies. J Clin Epidemiol. 1991;44(8): 763-770. 25. Hatala R, Keitz S, Wyer P, Guyatt G; Evidence-Based Medicine Teaching Tips Working Group. Tips for learners of evidence-based medicine, 4: assessing heterogeneity of primary studies in systematic reviews and whether to combine their results. CMAJ. 2005;172(5):661-665. 26. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088-1101. 27. Aganovic D. The role of uroflowmetry in diagnosis of infravesical obstruction in the patients with benign prostatic enlargement. Med Arh. 2004; 58(1)(suppl 2):109-111. 28. Ding YY, Lieu PK, Choo PW. Is the bladder “an unreliable witness” in elderly males with persistent lower urinary tract symptoms? Geriatr Nephrol Urol. 1997;7(1):17-21.
prostate volume for predicting bladder outflow obstruction in men with lower urinary tract symptoms. J Urol. 2000;164(2):344-348. 33. van Venrooij GE, van Melick HH, Eckhardt MD, Boon TA. Diagnostic and predictive value of voiding diary data versus prostate volume, maximal free urinary flow rate, and Abrams-Griffiths number in men with lower urinary tract symptoms suggestive of benign prostatic hyperplasia. Urology. 2008;71 (3):469-474. 34. Yalla SV, Sullivan MP, Lecamwasam HS, et al. Correlation of American Urological Association Symptom Index with obstructive and nonobstructive prostatism. J Urol. 1995;153(3 pt 1): 674-680. 35. Oelke M, Höfner K, Jonas U, et al. Diagnostic accuracy of noninvasive tests to evaluate bladder outlet obstruction in men: detrusor wall thickness, uroflowmetry, postvoid residual urine, and prostate volume. Eur Urol. 2007;52(3):827-834. 36. Aganovic D, Spahovic H, Prcic A, Hadziosmanovic O. Bladder outlet obstruction number: a good indicator of infravesical obstruction in patients with benign prostatic enlargement? Bosn J Basic Med Sci. 2012;12(3):144-150. 37. Araki Y, Ishibashi N, Sasatomi T, et al. Effectiveness of the portable ultrasound bladder scanner in the measurement of residual urine volume after total mesorectal extirpation. Minim Invasive Ther Allied Technol. 2003;12(5):245-248. 38. Barrington JW, Jones A, Robinson J, Stephenson TP. Estimation of bladder volume using portable ultrasound in clam enterocystoplasty patients. J Urol. 1996;155(1):82-83. 39. Borrie MJ, Campbell K, Arcese ZA, et al. Urinary retention in patients in a geriatric rehabilitation unit: prevalence, risk factors, and validity of bladder scan evaluation. Rehabil Nurs. 2001;26(5):187-191. 40. Cardenas DD, Kelly E, Krieger JN, Chapman WH. Residual urine volumes in patients with spinal cord injury: measurement with a portable ultrasound instrument. Arch Phys Med Rehabil. 1988;69(7):514-516. 41. Chan H. Noninvasive bladder volume measurement. J Neurosci Nurs. 1993;25(5):309-312. 42. Choe JH, Lee JY, Lee KS. Accuracy and precision of a new portable ultrasound scanner, the BME-150A, in residual urine volume measurement: a comparison with the BladderScan BVI 3000. Int Urogynecol J Pelvic Floor Dysfunct. 2007;18(6):641644. 43. Coombes GM, Millard RJ. The accuracy of portable ultrasound scanning in the measurement of residual urine volume. J Urol. 1994;152(6 pt 1): 2083-2085.
29. Reynard J, Lim C, Abrams P. Significance of intermittency in men with lower urinary tract symptoms. Urology. 1996;47(4):491-496.
44. Ding YY, Sahadevan S, Pang WS, Choo PW. Clinical utility of a portable ultrasound scanner in the measurement of residual urine volume. Singapore Med J. 1996;37(4):365-368.
30. Reynard JM, Lim C, Peters TJ, Abrams P. The significance of terminal dribbling in men with lower urinary tract symptoms. Br J Urol. 1996;77(5):705710.
45. Fuse H, Yokoyama T, Muraishi Y, Katayama T. Measurement of residual urine volume using a portable ultrasound instrument. Int Urol Nephrol. 1996;28(5):633-637.
31. Sirls LT, Kirkemo AK, Jay J. Lack of correlation of the American Urological Association Symptom 7 Index with urodynamic bladder outlet obstruction. Neurourol Urodyn. 1996;15(5):447-457.
46. Ireton RC, Krieger JN, Cardenas DD, et al. Bladder volume determination using a dedicated, portable ultrasound scanner. J Urol. 1990;143(5): 909-911.
Urinary Tract Symptoms and Bladder Obstruction
47. Marks LS, Dorey FJ, Macairan ML, et al. Three-dimensional ultrasound device for rapid determination of bladder volume. Urology. 1997;50 (3):341-348. 48. Massagli TL, Cardenas DD, Kelly EW. Experience with portable ultrasound equipment and measurement of urine volumes: inter-user reliability and factors of patient position. J Urol. 1989;142(4):969-971. 49. O’Farrell B, Vandervoort MK, Bisnaire D, et al. Evaluation of portable bladder ultrasound: accuracy and effect on nursing practice in an acute care neuroscience unit. J Neurosci Nurs. 2001;33(6):301309. 50. Oh-Oka H, Fujisawa M. Study of low bladder volume measurement using 3-dimensional ultrasound scanning device: improvement in measurement accuracy through training when bladder volume is 150 ml or less. J Urol. 2007;177 (2):595-599. 51. Ouslander JG, Simmons S, Tuico E, et al. Use of a portable ultrasound device to measure post-void residual volume among incontinent nursing home residents. J Am Geriatr Soc. 1994;42(11):1189-1192. 52. Revord JP, Opitz JL, Murtaugh P, Harrison J. Determining residual urine volumes using a portable ultrasonographic device. Arch Phys Med Rehabil. 1993;74(5):457-462. 53. Schott-Baer FD, Reaume L. Accuracy of ultrasound estimates of urine volume. Urol Nurs. 2001;21(3):193-195. 54. Teng CH, Huang YH, Kuo BJ, Bih LI. Application of portable ultrasound scanners in the measurement of post-void residual urine. J Nurs Res. 2005;13(3):216-224. 55. Topper AK, Holliday PJ, Fernie GR. Bladder volume estimation in the elderly using a portable ultrasound-based measurement device. J Med Eng Technol. 1993;17(3):99-103. 56. Yucel S, Kocak H, Sanli A, et al. How accurate is measuring postvoid residual volume by portable abdominal ultrasound equipment in peritoneal dialysis patient? Neurourol Urodyn. 2005;24(4): 358-361. 57. Master VA, Johnson TV, Abbasi A, et al. Poorly numerate patients in an inner city hospital misunderstand the American Urological Association symptom score. Urology. 2010;75(1):148-152. 58. Cam K, Senel F, Akman Y, Erol A. The efficacy of an abbreviated model of the International Prostate Symptom Score in evaluating benign prostatic hyperplasia. BJU Int. 2003;91(3):186-189. 59. Yap TL, Cromwell DA, Brown C, et al. The relationship between objective frequency-volume chart data and the I-PSS in men with lower urinary tract symptoms. Eur Urol. 2007;52(3):811-818. 60. Winters JC, Dmochowski RR, Goldman HB, et al; American Urological Association; Society of Urodynamics, Female Pelvic Medicine and Urogenital Reconstruction. Urodynamic studies in adults: AUA/SUFU guideline. J Urol. 2012;188(6) (suppl):2464-2472.
32. Steele GS, Sullivan MP, Sleep DJ, Yalla SV. Combination of symptom score, flow rate and
542
JAMA August 6, 2014 Volume 312, Number 5
Copyright 2014 American Medical Association. All rights reserved.
Downloaded From: http://jama.jamanetwork.com/ by a University of St. Andrews Library User on 05/11/2015
jama.com