Effectiveness of manual bladder expression in paraplegic dogs

Tags: bladder volume, urine volume, expression, ultrasonographic, bladder pressure, intermittent catheterization, residual urine volume, measurement, measurements, strong correlation, estimation, Spinal cord injury, Langford Veterinary Services, detrusor muscle, Nicolas Granger, School of Veterinary Sciences, The bladder, indwelling catheter, urine volumes, Carwardine, Effectiveness, Urinary tract infection, urinary tract infections, urinary bladder, urethral sphincter, urine retention, Barr F. Effect, manual expression, catheterization
Content: Effectiveness of manual bladder expression in paraplegic dogs
Darren R. Carwardine bvsc Jeremy H. Rose ma, vetmb Thomas R. Harcourt-Brown ma, vetmb Nicolas Granger dvm, phd Received February 26, 2016. Accepted April 19, 2016. From the School of Veterinary Sciences (Carwardine, Rose, Granger) and Langford Veterinary Services (Harcourt-Brown), University of Bristol, Langford, Bristol, BS40 5DU, England. Dr. Carwardine's present address is Regenerative Medicine Laboratory, School of Veterinary Sciences, Biomedical Science Building, University Walk, Bristol, BS8 1TD, England. Address correspondence to Dr. Carwardine (darren. [email protected]).
OBJECTIVE To determine the effectiveness of manual bladder expression in paraplegic dogs by comparing urine volumes measured by use of intermittent catheterization and ultrasonography. ANIMALS 36 paraplegic dogs. PROCEDURES 93 measurements of bladder volume were collected for the 36 dogs. Residual urine volume was determined by use of intermittent urethral catheterization and estimated by use of ultrasonography. RESULTS Manual bladder expression voided a mean of 49% of urine from the bladder in this population of dogs. There was no correlation (R2, 0.06) between the effectiveness of manual bladder expression and body weight. Ultrasonographic estimation of bladder volume had good correlation (R2, 0.62) with bladder volume determined by use of intermittent bladder catheterization, but clinically unacceptable variation for predicting actual bladder volume (mean difference, 22 mL; 95% confidence interval, ­96 to 139 mL). CONCLUSIONS AND CLINICAL RELEVANCE Manual bladder expression was ineffective at completely emptying urine from the bladder of paraplegic dogs, but the effectiveness of the procedure was not affected by body weight. Manual bladder expression would likely be a useful procedure to prevent increases in pressure within the bladder. Ultrasonographic estimation of bladder volume could be a useful predictor of actual bladder volume, but it was susceptible to wide variations among dogs, and results should therefore be interpreted with caution. (Am J Vet Res 2017;78:107­112)
Micturition requires a synergistic action between the detrusor muscle of the bladder and the external and internal urethral sphincter muscles.1­4 Their coordinated action requires control of segmental spinal reflexes combined with input from supraspinal centers via the spinal cord. Spinal cord injury in the thoracolumbar region leads to detrusor areflexia and increased urethral sphincter tone (ie, an upper motor neuron bladder) and eventually bladder dyssynergia.5 The lack of afferent information on bladder pressure to the brain initially leads to prolonged urine retention, and preservation of sacral spinal reflexes caudal to the lesion in turn causes persistence of urethral tone. As bladder pressure increases with increasing urine volume, there is often overflow incontinence and vesicoureteral reflux to the kidneys. Prolonged increases in bladder pressure can lead to damage of the detrusor neuromuscular tight junctions and detrusor atony, which can be irreversible. In the acute phase of injury, there is low urethral tone, and reflex incontinence is common.6 By 2 weeks ABBREVIATIONS CI Confidence interval
after spinal cord injury, involuntary detrusor contractions begin during the filling phase, which causes reflex incontinence.7,8 However, these involuntary detrusor contractions, without supraspinal control, are not enough to completely empty the bladder. In addition, detrusor-sphincter dyssynergia develops with simultaneous contraction of the urethral sphincter when the bladder contracts. Short-lived detrusor contraction combined with increased urethral tone leads to incomplete voiding of urine from the bladder.5 The methods for managing bladder dysfunction in patients with spinal cord injury (manual expression, an indwelling catheter, or intermittent catheterization) are intended to frequently remove urine from the bladder to prevent prolonged urine retention.9 Ideally, these techniques should leave the same residual urine volume as in clinically normal dogs (0.2 to 0.4 mL/kg).10 An indwelling catheter allows efficient urine evacuation with minimal intervention once the catheter is placed. Unfortunately, placement of a urinary catheter can result in damage to the bladder or urethra, and the risk of urinary tract infection increases daily with use of an indwelling catheter, both of which can discourage use of indwelling catheters.11­13
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Intermittent catheterization can be time consuming, particularly in female dogs. Manual bladder expression is thought to be quick and easy to perform in small-breed dogs, but it can be difficult in large, obese, or aggressive dogs. Because no apparatus is passed up the urethra during manual expression, the theoretical risk of urinary tract infection may be less than that for catheter-based methods, but this has not yet been determined. Nevertheless, 21% to 38% of dogs with spinal cord injury managed with manual bladder expression develop a urinary tract infection.9,14,15 It is possible that leaving a larger residual urine volume in the bladder may increase the risk of urinary tract infection (by increasing the bladder's exposure to uropathogens that typically are rapidly and efficiently cleared from the bladder) and the risk of detrusor atony. Despite widespread clinical use of manual bladder expression, the effectiveness of this method for emptying the bladder is not known. Accurate data on the effectiveness of current bladder management techniques would allow clinicians and researchers to make objective comparisons with effectiveness of new treatments or techniques. The criterion-referenced standard for accurate measurement of the residual urine volume requires intermittent catheterization.16 Ultrasonographic estimation of the residual urine volume is standard practice at human hospital wards to determine whether bladder management is required, which avoids the invasive and time-consuming procedure of intermittent catheterization.17 Intermittent catheterization has been used in our veterinary clinic by appropriately trained veterinarians and veterinary nurses. The bladder diameter has been used as an approximation of bladder volume to determine whether an intervention (eg, intermittent catheterization, indwelling catheter, or manual bladder expression) is required. Bladder volume in dogs can be accurately estimated with a few simple ultrasonographic measurements by use of a specific equation.18­20 The primary objective of the study reported here was to determine the effectiveness of manual bladder expression for emptying the bladder in paraplegic dogs with an upper motor neuron bladder by measuring residual urine volume after manual bladder expression. Additionally, we examined whether body weight was correlated with the residual urine volume to investigate the commonly held belief that manual bladder expression is less effective in larger dogs. Finally, we compared ultrasonographic bladder volume estimates obtained from conscious paraplegic dogs in a clinically applicable setting to determine whether estimates of bladder volumes correlated and agreed with actual bladder volumes. Materials and Methods Animals The study population consisted of prospectively recruited client-owned dogs with naturally occur-
ring spinal cord injury examined at the veterinary neurology referral service of the University of Bristol between October 2013 and March 2014. Details of the study were explained to owners during the initial consultation. Informed Consent was obtained from owners before dogs were included in the study. The study design was approved by the local ethical committee and assigned a veterinary investigation number (VIN/13/037). Inclusion criteria for the study were acute (within 7 days) paraplegia (with or without pelvic limb pain sensation) secondary to a spinal cord injury between the third thoracic and third lumbar spinal cord segments (T3 through L3), which was confirmed by MRI and surgically decompressed when required; absence of voluntary micturition for 24 hours despite outside access for 10 minutes 3 times/d; and > 48 hours from the time of spinal cord injury (to allow signs of spinal shock to resolve).21 Bladders were not manually expressed if dogs had been sedated within the preceding 8 hours or they had concomitant abdominal or pelvic trauma. Sedation included the use of acepromazine, 2-receptor agonists, or butorphanol but not the use of opioids such as buprenorphine, morphine, methadone, or fentanyl, which were used routinely for postoperative analgesia. Unsuccessful manual bladder expressions were recorded. Experimental procedures Data were collected in the morning between 8 am and 9 am; manual expression of the bladder had not been performed on any dog since midnight. Dogs were taken for a 10-minute assisted walk prior to attempted manual bladder expression. Bladder expression was performed for up to 2 minutes; urine was expressed into a kidney dish, and the volume of urine expressed was recorded. Each dog was then positioned in right lateral recumbency, and ultrasonography of the bladder was performed. Bladder measurements were recorded as described elsewhere.19 Estimates of bladder volume were made by use of the following equation19: bladder volume = L X W X ([DL + DT]/2) X 0.625, where L is longitudinal bladder length, W is transverse bladder width, DL is longitudinal bladder depth, and DT is transverse bladder depth. Intermittent catheterization was then performed. Once urine flow ceased during collection, the catheter was repositioned and collection was attempted for up to another 30 seconds until the operator was confident no more urine could be collected. All procedures (bladder expression, ultrasonography, and bladder catheterization) were performed by a veterinarian or registered veterinary nurse appropriately trained in the procedures. A monitoring form was used to obtain patient demographic data; urine volumes for manual bladder expression and intermittent catheterization and ultrasonographic bladder measurements were also recorded. Manual bladder expression was performed at 4 pm and midnight, but no data were recorded at those times. This process was repeated for 3 consecu-
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tive days for each patient or < 3 days when there was dogs, 2 days for 7 dogs, and 1 day for 4 dogs, with
a return of voluntary micturition.
the latter 11 dogs removed from the study because
statistical analysis
of improvement in neurologic function and ability to urinate). Some dogs had little variation in residual
A Sample Size calculation was performed. Prelimi- urine volume following manual bladder expression
nary data collected for 5 dogs (not included in the study over all 3 days. However, a substantial number of
reported here) were used to estimate sample size. To de- dogs had marked variation in residual urine volume
tect a significant difference in residual urine volume of following manual bladder expression during the
1 mL/kg ( = 0.05; power = 80%), it was calculated that study (Figure 1). Because of this observation, sep-
36 dogs would be required to accurately represent the arate data points were plotted for each attempt at
residual urine volume of the population in 95% of cases. manual bladder expression. Manual bladder expres-
Bladder volumes and body weight were
not normally distributed (Shapiro-Wilk
test); therefore, they were logarithmi-
cally (base 10) transformed to achieve
normality for Linear regression analysis.
descriptive statistics were reported for
demographic data and residual urine
volume. Standard linear regression and
Bland-Altman plots were used to com-
pare estimated bladder volume with
actual bladder volume and to compare
body weight with efficiency of manual
bladder expression. The F statistic was
calculated for linear regression plots to
allow comparison of results with those Figure 1--Residual urine volume of 15 dogs with acute spinal cord injury followof previous studies. The F statistic es- ing manual bladder expression in the morning (between 8 am and 9 am) on each of timated the degree to which variation 3 consecutive days (A) and for each of 74 successful manual bladder expressions in
in estimated bladder volume reflected all 36 dogs in the study (B). Each symbol represents results for a successful bladder
the variation in actual bladder volume. A 2-sample t test was used to compare
expression. Residual urine volume was determined by use of intermittent catheterization. In panel A, notice that the variation in residual urine volume across the 3 days was small for some dogs (eg, Nos. 1, 5, 8, and 12) but large for other
efficiency of manual bladder expres- dogs (eg, Nos. 6, 7, and 11). In panel B, the dashed line represents the upper limit
sion between veterinarians and veteri- of the residual urine volume for clinically normal dogs following micturition (0.4
nary nurses. All statistical analyses were performed and figures created with a
mL/kg), and the solid line represents the mean residual urine volume for all dogs in the present study (8.4 mL/kg).
statistical program.22,a All values were
reported as mean and SD.
Results
Animals A total of 36 dogs (23 males and 13 females) were included in the study. The most common breed represented was Miniature Dachshund (n = 14). Other breeds included Basset Hound (n = 2), Beagle (2), Border Collie (4), Border Terrier (2), Cocker Spaniel (1), French Bulldog (1), Irish Terrier (1), Jack Russell Terrier (3), Labrador Retriever (1), Lurcher (1), Northern Inuit (1), Shih Tzu (2), and Staffordshire Bull Terrier (1). Body weight ranged from 4 to 35 kg (mean, 14 kg). All injuries were between T3 and L3. Causes of injury included Hansen type 1 disc extrusion (n = 32), fibrocartilaginous embolism (3), and myelitis (1). All Hansen type 1 disc extrusions were surgically decompressed. Effectiveness of manual bladder expression Data for 93 attempts at manual bladder expression were recorded for the 36 dogs (3 days for 25
Figure 2--Graph depicting the correlation between ultra-sonographic estimated bladder volume and actual bladder volume in 36 paraplegic dogs. Each symbol represents results for a successful manual bladder expression. The line of best fit (R, 0.79; R2, 0.62; P < 0.001) was determined by use of linear regression. Equation for the line was as follows: log10 actual bladder volume = 0.23 + (0.82 X log10 estimated bladder volume).
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Mean ± SD total bladder volume prior to intervention, as determined by use of intermittent catheterization, was 186 ± 107 mL (range, 34 to 600 mL). This equated to a mean bladder volume of 15.7 ± 9.3 mL/kg.
Actual versus estimated
bladder volume
A linear regression model was
used to determine the correlation be-
tween estimated bladder volume and
Figure3--Bland-Altmanplotsofthemeandifference(A)andthepercentagedifference actual bladder volume (Figure 2). Re-
(B) between ultrasonographically estimated bladder volume and actual bladder volume in 36 paraplegic dogs. Each symbol represents results for a successful manual bladder expression. In panels A and B, the solid line represents the mean difference (21.68 mL
sults indicated a strong positive correlation (R, 0.79 [95% CI, 0.69 to 0.86];
and 23.76%, respectively) and the dotted lines represent the 95% CI (­95.67 to R2, 0.62; P < 0.001) between estimated
139.03 mL and ­79.05% to 126.57%, respectively).
bladder volume and actual bladder vol-
ume and that 62% of the variance in
actual bladder volume could be attributed to variance
in estimated bladder volume. The equation for the re-
gression line was as follows: log10 actual bladder volume = 0.23 (95% CI, ­0.05 to 0.50) + 0.82 (95% CI,
0.68 to 0.96) X log10 estimated bladder volume. A Bland-Altman plot of the same data was used to
quantify the agreement between the 2 methods for
determining bladder volume23 (Figure 3). Typically,
estimated bladder volume underestimated actual blad-
der volume by 21.68 mL (95% CI, ­95.67 to 139.03 mL).
Estimated bladder volume appeared to have greater
variation than actual bladder volume at higher urine
volumes. To investigate this finding further, a second
Bland-Altman plot was constructed with percent-
age differences (mean difference, 23.76%; 95% CI,
­79.05% to 126.57%). This indicated that there was a
similar degree of variation in bladder volumes across
all urine volumes, which had a greater effect on the
estimated volume at higher values.
Figure 4--Graph depicting the correlation between efficiency of manual bladder expression and body weight in 36 paraplegic dogs. Each symbol represents results for a successful manual bladder expression. The line of best fit (R, ­0.23; R2, 0.06; P = 0.04) was determined by use of linear regression. Equation for the line was as follows: efficiency of manual bladder expression = 68.04 ­ (18.05 X body weight).
Manual bladder expression in large dogs To investigate the commonly held belief that manual bladder expression would be more difficult and therefore less effective in large dogs, a linear regression model was constructed that compared body
weight with manual bladder expression efficiency
sion failed in 17 of 93 (18.28%) attempts and catheterization failed in 2 of 93 (2.15%) attempts . For 74 successful attempts, mean ± SD residual urine volume following manual bladder expression was 8.41 ± 6.01 mL/kg (range, 0.50 to 33.02 mL/kg). Thus, none of the dogs in the study achieved a physiologically normal residual urine volume (0.2 to 0.4 mL/ kg) when managed by manual bladder expression.
(Figure 4). Results indicated that there was no correlation (R, ­0.23 [95% CI, ­0.44 to ­0.01]; R2, 0.06; P = 0.04) between these 2 variables and that only 4% of the variation in manual bladder expression efficiency could be attributed to body weight. The equation for the regression line was as follows: manual bladder expression = 68.04 (95% CI, 49.69 to 86.38) ­ 18.05 (95% CI, ­35.05 to ­1.04) X body weight.
Mean efficiency of manual bladder expression, defined as the percentage of total urine volume voided
Discussion
by manual bladder expression, was 49.17 ± 20.07%
Manual bladder expression was ineffective at ful-
(range, 0.56% to 98.18%). Mean efficiency of manual ly emptying the bladder in paraplegic dogs because a
bladder expression was 53.32 ± 24.99% when per- physiologically normal residual urine volume was not
formed by veterinary nurses and 43.63 ± 17.72% achieved for any of the 93 manual bladder expression
when performed by veterinarians; there was no sig- attempts. The 76 successful attempts typically result-
nificant (P = 0.16) difference between these values. ed in 49% of the total urine volume being voided from
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the bladder by use of this technique. This likely would eliminate the risk of detrusor atony attributable to any increase in bladder pressure, but it is not known whether leaving a higher than physiologically normal residual urine volume within the bladder would predispose dogs to urinary tract infection. Investigators of 2 studies9,15 found no increase in the risk of urinary tract infection in dogs managed with manual bladder expression following spinal cord injury, but it appears logical that leaving urine in the bladder may predispose to infection. Difficulties of manual bladder expression in the group of dogs reported here was likely attributable to the lack of supraspinal control that led to an upper motor neuron bladder. Manual bladder expression was completely unsuccessful in 17 of 93 (18.3%) attempts. Most times, manual bladder expression was successful on the subsequent day of the study; however, on the day of a failed attempt, an alternative method for emptying the bladder was required. Manual bladder expression was unsuccessful on all 3 days of the study for 3 of 36 dogs. Body weight of these 3 dogs (17.4, 24.5, and 28.8 kg) was more than the mean weight for the entire study population (14 kg). Despite these findings, there was no correlation between efficiency of manual bladder expression and body weight. A stronger correlation between these variables would have been expected if manual bladder expression was less effective in larger dogs. We concluded that if manual bladder expression was successful, it was equally effective in small and large dogs. Complete failure of manual bladder expression may be more likely in larger dogs, but a larger cohort that includes more dogs in which manual bladder expression failed would be needed to support this hypothesis. Pharmacological treatments may increase the efficiency of manual bladder expression from the 49% for the population of the study reported here. Results of the present study can be used as a benchmark for efficacy of this procedure in paraplegic dogs; thus, improvements afforded by drugs could be investigated to determine whether their use in such patients would be recommended. Although we enrolled dogs with acute spinal cord injury in the present study, the findings would likely be useful for the management of dogs with chronic spinal cord injury, which are often managed at home with manual bladder expression provided by their owners. Parasympathomimetic compounds, such as carbachol and bethanechol, have been used to improve bladder voiding, but there is little information available on clinical efficacy.24 Alternatively, blockade of -adrenergic receptors with sympatholytic compounds (eg, prazosin or phenoxybenzamine) aimed at causing urethral sphincter relaxation and used in combination with parasympathomimetic compounds could be advantageous when dealing with an upper motor neuron bladder.25­27 A sacral nerve root stimulator has provided efficient bladder emptying in dogs with spinal cord inju-
ry and is indicated for use in chronically incontinent dogs.28 At 3 weeks after implantation, 8 of 9 dogs had a voiding efficiency ranging from 92% to 99%, which is a clear improvement on the mean of 49% achieved with manual bladder expression in the study reported here. This neuroprosthesis, which is surgically placed on the extradural sacral nerve root, has been available to stimulate bladder voiding in paraplegic humans since the 1980s.29,30 Ultrasonographic estimation of bladder volume is common practice in human medicine.17 This previously has been performed with conventional 2-D ultrasonography, as was performed in the present study. Results for canine patients have resulted in advocacy for the use of conventional 2-D ultrasonographic bladder measurements for determining urine volume, and a strong correlation was found between estimated and actual bladder volumes in 1 study.18 When comparing the accuracy of 2 procedures, it has been highlighted in the medical literature that agreement between 2 methods is more important than their correlation23 because 2 values can have a perfect correlation, even when one method consistently underestimates or overestimates the value obtained for the second method. In the study reported here, we used the same method described in another study19 to estimate bladder volumes by use of ultrasonography and, similar to results of that study,19 found a strong correlation with actual bladder volumes. However, in that study,19 investigators used the same collection method on healthy dogs. Furthermore, in the study reported here, we also assessed the agreement between estimated bladder volume and actual bladder volume by use of Bland-Altman plots and found that the estimated bladder volume consistently underestimated the actual bladder volume by a mean of 21.68 mL. We decided this was a clinically acceptable estimation, but values for the 95% CI were unacceptably wide (­95.67 to 139.03 mL), although similar to those determined for humans by use of the same technique.31,32 Considering that the bladder of an 11kg dog is thought to be able to hold approximately 100 to 120 mL of urine without overt bladder distension,33 narrower CI values would be needed for ultrasonographic bladder estimates to be useful. Larger sample sizes yield a more precise sample statistic and therefore typically result in smaller values for the CI; however, if there is a high degree of variability in the measurement, these values for the CI may still be too wide for clinical use. Most of the variability in bladder volume estimates in the present study could have been attributable to the patients, ultrasound machine (although the same machine was used for all dogs), or operator. Repeated measurements of the same dog at the same time point by multiple operators would have allowed assessment of interobserver reliability. Ultrasonographic estimates determined by diagnostic imaging specialists may limit variability for the procedure; however, this would not be practical for day-to-day management of these patients. Thus, measurements in the present study were obtained by attending veteri-
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narians or veterinary nurses to ensure the results were clinically applicable and represented the real-life situation of a busy neurology service. In human medicine, estimates of bladder volume have been determined by use of planimetric 3-D volumetric measurements obtained with a portable ultrasonographic bladder-scanning device,b which has been used for > 20 years.16 This method provides a much more accurate estimate of bladder volume, with a mean difference of 41 mL (95% CI, 26 to 55 mL).34 To the authors' knowledge, this or a similar device has not yet been tested in canine patients and warrants further investigation. In the present study, manual bladder expression performed by a trained veterinarian or veterinary nurse voided approximately half of the total bladder volume. There was a strong correlation between estimated bladder volume (determined on the basis of 4 ultrasonographic measurements) and actual bladder volume, with good agreement (mean difference, ­22 mL). However, the CI for this estimation (­95.67 to 139.03 mL) was unacceptably wide, which indicated that estimates must be interpreted with caution. Increasing body weight did not influence the effectiveness of manual bladder expression. Footnotes a. The R, version 3.1.3, R Foundation for Statistical Computing, Vienna, Austria. Available at: www.R-project.org. Accessed Feb 1, 2016. b. BladderScan, Diagnostic Ultrasound, Bothell, Wash. References 1. Tai C, Roppolo JR, de Groat WC. Spinal reflex control of micturition after spinal cord injury. Restor Neurol Neurosci 2006;24:69­78. 2. de Groat WC, Booth AM, Yoshimura N. Neurophysiology of micturition and its modification in animal models of human disease. In: Maggi CA, ed. Nervous control of the urogenital system: the autonomic nervous system. Vol. 3. London: Harwood Academic Publishers, 1993;227­290. 3. de Groat WC, Fraser MO, Yoshiyama M, et al. Neural control of the urethra. Scand J Urol Nephrol Suppl 2001;207:35­43. 4. Shefchyk SJ. Spinal cord neural organization controlling the urinary bladder and striated sphincter. Prog Brain Res 2002;137:71­82. 5. Barsanti JA, Coates JR, Bartges JW, et al. Detrusor-sphincter dyssynergia. Vet Clin North Am Small Anim Pract 1996;26:327­338. 6. Denny-Brown D, Robertson EG. The state of the bladder and its sphincter in complete transverse lesions of the spinal cord and cauda equina. Brain 1933;56:397­469. 7. Handa Y, Naito A, Watanabe S, et al. Functional recovery of locomotive behavior in the adult spinal dog. Tohoku J Exp Med 1986;148:373­384. 8. Jonas U, Jones LW, Tanagha EA. Recovery of bladder function after spinal cord transection. J Urol 1975;113:626­628. 9. Bubenik L, Hosgood G. Urinary tract infection in dogs with thoracolumbar intervertebral disc herniation and urinary bladder dysfunction managed by manual expression, indwelling catheterization or intermittent catheterization. Vet Surg 2008;37:791­800. 10. Oliver JE, Hoerlein BF, Mayhew IG. Disorders of micturition. In: Hoerlein BF, Mayhew IG, eds. Veterinary neurology. Philadelphia: WB Saunders Co, 1987;342­352. 11. Biertuempfel PH, Ling GV, Ling GA. Urinary tract infection resulting from catheterization in healthy adult dogs. J Am Vet Med Assoc 1981;178:989­991.
12. Bubenik LJ, Hosgood GL, Waldron DR, et al. Frequency of urinary tract infection in catheterized dogs and comparison of bacterial culture and susceptibility testing results for catheterized and noncatheterized dogs with urinary tract infections. J Am Vet Med Assoc 2007;231:893­899. 13. Barsanti JA, Blue J, Edmunds J. Urinary tract infection due to indwelling bladder catheters in dogs and cats. J Am Vet Med Assoc 1985;187:384­388. 14. Olby NJ, MacKillop E, Cerda-Gonzalez S, et al. Prevalence of urinary tract infection in dogs after surgery for thoracolumbar intervertebral disc extrusion. J Vet Intern Med 2010;24:1106­1111. 15. Stiffler KS, Stevenson M, Sanchez S, et al. Prevalence and characterization of urinary tract infections in dogs with surgically treated type 1 thoracolumbar intervertebral disc extrusion. Vet Surg 2006;35:330­336. 16. Kelly CE. Evaluation of voiding dysfunction and measurement of bladder volume. Rev Urol 2004;6(suppl 1):S32­S37. 17. National Institute for Health and Clinical Excellence. Urinary incontinence in neurological disease: assessment and management; 2012. Available at: www.nice.org.uk. Accessed Feb 1, 2016. 18. Atalan G, Barr F, Holt PE. Assessment of urinary bladder volume in dogs by use of linear ultrasonographic measurements. Am J Vet Res 1998;59:10­15. 19. Atalan G, Holt PE, Barr F. Effect of body position on ultrasonographic estimations of bladder volume. J Small Anim Pract 1999;40:177­179. 20. Atalan G, Barr F, Holt PE. Frequency of urination and ultrasonographic estimation of residual urine in normal and dysuric dogs. Res Vet Sci 1999;67:295­299. 21. Blauch B. Spinal reflex walking in the dog. Vet Med Small Anim Clin 1977;72:169­173. 22. R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, 2013. Available at: www.R-project. org/. Accessed Feb 1, 2016. 23. Bland JM, Altman D. statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986;1:307­310. 24. Noлl S, Claeys S, Hamaide A. Acquired urinary incontinence in the bitch: update and perspectives from human medicine. Part 1: the bladder component, pathophysiology and medical treatment. Vet J 2010;186:10­17. 25. Holt PE, Hotson-Moore A. Urinary incontinence. In: Holt PE, Hotson-Moore A, eds. Urological disorders of the dog and cat: investigation, diagnosis, treatment. London: Manson Publishing, 2008;142­144. 26. Haagsman AN, Kummeling A, Moes M, et al. Comparison of terazosin and prazosin for treatment of vesico-urethral reflex dyssynergia in dogs. Vet Rec 2013;173:41. 27. Byron JK. Micturition disorders. Vet Clin North Am Small Anim Pract 2015;45:769­782. 28. Granger N, Chew D, Fairhurst P, et al. Use of an implanted sacral nerve stimulator to restore urine voiding in chronically paraplegic dogs. J Vet Intern Med 2013;27:99­105. 29. Brindley GS, Polkey CE, Rushton DN, et al. Sacral anterior root stimulators for bladder control in paraplegia: the first 50 cases. J Neurol Neurosurg Psychiatry 1986;49:1104­ 1114. 30. Martens FM, Heesakkers JP. Clinical results of a Brindley procedure: sacral anterior root stimulation in combination with a rhizotomy of the dorsal roots. Adv Urol 2011;2011:709708. 31. Hakenberg OW, Ryall RL, Langlois SL, et al. The estimation of bladder volume by sonocystography. J Urol 1983;130:249­251. 32. Harrison NW, Parks C, Sherwood T. Ultrasound assessment of residual urine in children. Br J Urol 1975;47:805­814. 33. Evans HE, De Lahunta A. The urogenital system. In: Evans HE, De Lahunta A, eds. Miller's anatomy of the dog. 4th ed. St Louis: Elsevier Health Sciences, 2013;361­401. 34. Coombes GM, Millard RJ. The accuracy of portable ultrasound scanning in the measurement of residual urine volume. J Urol 1994;152:2083­2085.
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