Acute Spinal Cord Injury—Do Ambulatory Patients Need Urodynamic Investigations? Carlos H. Suzuki Bellucci,* Jens Wöllner,* Flavia Gregorini, Dorothee Birnböck, Marko Kozomara, Ulrich Mehnert, Martin Schubert and Thomas M. Kessler† From Neuro-Urology (CHSB, JW, FG, DB, MK, UM, TMK) and Neurology (MS), Spinal Cord Injury Center & Research, University of Zürich, Balgrist University Hospital, Zürich, Switzerland
Purpose: We compared the urodynamic parameters of ambulatory vs nonambulatory acute spinal cord injured patients. Materials and Methods: A total of 27 women and 33 men (mean age 58 years) with neurogenic lower urinary tract dysfunction due to acute spinal cord injury (duration of injury less than 40 days) were prospectively evaluated. The patients were dichotomized according to the mobility for moderate distances subscale of the SCIM (Spinal Cord Independence Measure) version III into ambulatory (score of 3 or greater) and nonambulatory (score less than 3). Videourodynamic parameters including maximum detrusor pressure during the storage phase, bladder compliance, detrusor overactivity, detrusor external sphincter dyssynergia and vesicoureterorenal reflux were compared between the groups. Results: Of the 60 patients with acute spinal cord injury 17 were ambulatory and 43 were nonambulatory. Mean ⫾ SD duration of injury at urodynamic investigation was 30 ⫾ 8 days. The lesion level was cervical in 14 patients, thoracic in 28 and lumbar/sacral in 18. Comparing unfavorable urodynamic parameters, no significant differences were found between ambulatory vs nonambulatory patients in terms of a high pressure system during the storage phase (29% vs 33%, p ⫽ 0.81), a low compliance bladder (12% vs 7%, p ⫽ 0.54), detrusor overactivity (24% vs 47%, p ⫽ 0.1), detrusor external sphincter dyssynergia (18% vs 21%, p ⫽ 0.77) and vesicoureterorenal reflux (0% vs 5%, p ⫽ 0.36). Conclusions: Ambulatory and nonambulatory patients with acute spinal cord injury have a similar risk of unfavorable urodynamic measures. Thus, we strongly recommend the same neurourological assessment including urodynamic investigations in all acute spinal cord injury patients independent of the ability to walk. Key Words: spinal cord injuries; urodynamics; urinary bladder, neurogenic NEUROGENIC lower urinary tract dysfunction is an important cause of morbidity and mortality among SCI patients.1,2 Neurourological management aims for the preservation or improvement of upper urinary tract function, control of urinary tract infection, and maintenance of a low pressure bladder that is continent and capable of emptying completely. Increased bladder pressure during the storage phase, often due to a low compliance
bladder and/or detrusor overactivity combined with DESD, is the major cause of renal deterioration.3 Consequently, if not recognized or if managed inadequately, NLUTD may result in life threatening complications such as recurrent urinary tract infections, vesicoureterorenal reflux, hydronephrosis and renal failure.4,5 However, in contrast to chronic SCI, little is known about lower urinary tract dysfunction patterns dur-
0022-5347/13/1894-1369/0 THE JOURNAL OF UROLOGY® © 2013 by AMERICAN UROLOGICAL ASSOCIATION EDUCATION
http://dx.doi.org/10.1016/j.juro.2012.10.013 Vol. 189, 1369-1373, April 2013 RESEARCH, INC. Printed in U.S.A.
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Abbreviations and Acronyms DESD ⫽ detrusor external sphincter dyssynergia DO ⫽ detrusor overactivity NLUTD ⫽ neurogenic lower urinary tract dysfunction SCI ⫽ spinal cord injury Accepted for publication October 4, 2012. Study received local ethics committee approval. Supported by the Swiss National Science Foundation (Grant 127477). Nothing to disclose. * Equal study contribution. † Correspondence: Neuro-Urology, Spinal Cord Injury Center & Research, University of Zürich, Balgrist University Hospital, 8008 Zürich, Switzerland (telephone: ⫹41 44 386 38 45; e-mail: tkessler@ gmx.ch).
Editor’s Note: This article is the fifth of 5 published in this issue for which category 1 CME credits can be earned. Instructions for obtaining credits are given with the questions on pages 1608 and 1609.
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ing the acute phase of SCI, probably because urodynamic investigations are postponed to the chronic phase or are not performed at all, especially in patients with less well pronounced neurological impairments. We hypothesized that in the acute phase of SCI, ambulatory patients rarely present unfavorable urodynamic parameters such as high maximum detrusor pressure during the storage phase, low compliance bladder, DO, DESD and vesicoureterorenal reflux, implying that urodynamic investigations would not be necessary in this specific group of patients. Thus, we prospectively compared ambulatory vs nonambulatory SCI patients and assessed urodynamic parameters in the acute phase of the injury.
PATIENTS AND METHODS Patients From January 2010 to May 2012 a consecutive series of 60 acute SCI patients were prospectively evaluated at the Spinal Cord Injury Center, Balgrist University Hospital, Zürich. Study inclusion criteria were NLUTD due to SCI and duration of injury on urodynamic investigation of less than 40 days, ie within the very acute phase or acute phase I of SCI according to the definitions of the European Multicenter Study about Spinal Cord Injury (www.emsci. org). Patients younger than 18 years old were excluded from analysis. The participants gave written informed consent and the study was approved by the local ethics committee. All methods, definitions and units are presented according to the standards recommended by the International Continence Society.6
Neurourological Evaluation Neurourological evaluation consisted of medical history, clinical examination with determination of ASIA (American Spinal Injury Association) impairment scale,7 urinalysis, urine culture, urinary tract ultrasound and videourodynamic investigation including pelvic floor electromyography. The patients were dichotomized according to the mobility for moderate distances subscale of the SCIM version III into ambulatory (score of 3 or greater) and nonambulatory (score less than 3).8 Videourodynamics were performed according to good urodynamic practices recommended by the International Continence Society.9 Patients were urodynamically investigated in a sitting position whenever possible. An 8Fr transurethral reusable microtip dual sensor microtransducer catheter (Unisensor AG, Attikon, Switzerland) was used. The bladder was filled with a 36C mixture of 0.9% sodium chloride solution and contrast medium at a speed of 20 ml per minute. Pelvic floor electromyography was performed with surface electrodes (Ambu®, NF-50-K/W/12, Penang, Malaysia). A Sedia-NT multichannel urodynamic system (Sedia®, Givisiez, Switzerland) was used for all measurements. Blood pressure and heart rate were measured at the beginning and end of the urodynamic investigation, which was interrupted immediately in case of signs of autonomic dysreflexia.
Outcome Measures The outcome measures were the assessment and comparison of urodynamic parameters including maximum detrusor pressure during the storage phase, high pressure system during the storage phase (defined as maximum detrusor pressure during the storage phase greater than 40 cm H2O),3 bladder compliance, low compliance bladder (defined as less than 20 ml/cm H2O),10 DO, DESD and vesicoureterorenal reflux in ambulatory vs nonambulatory patients with acute SCI.
Statistical Analyses Data were approximately normally distributed and presented as means ⫾ SD. Mean values and frequencies were compared between ambulatory and nonambulatory patients using the independent samples t test and the chisquare test, respectively. Multivariate analysis using binary logistic regression was applied to identify predictors of unfavorable urodynamic parameters (ie high maximum detrusor pressure during the storage phase, low compliance bladder, DO, DESD and vesicoureterorenal reflux). Statistical analyses were performed using IBM® SPSS® version 19 with p ⬍0.05 considered statistically significant.
RESULTS Of the 60 patients with acute SCI enrolled in the study 17 (28%) were ambulatory and 43 (72%) were nonambulatory. Overall 27 (45%) patients were female and 33 (55%) male. At urodynamic investigation mean patient age was 58 ⫾ 19 years (range 18 to 87) and mean duration since SCI was 30 ⫾ 8 days (range 14 to 39). Comparing ambulatory and nonambulatory patients, most characteristics were similar between the groups (tables 1 and 2). However, there were significant differences regarding the ASIA impairment scale (most ambulatory patients were classified as ASIA D, whereas ASIA B and C were dominant among nonambulatory patients) and the level of injury (most ambulatory patients had lumbar/ sacral lesions whereas nonambulatory patients had mostly thoracic lesions). The urodynamic parameters investigated were similar in both groups (table 2). Although there was a trend for a lower proportion of unfavorable urodynamic parameters in ambulatory patients, no statistically significant differences were detected. On multivariate analysis no factor predicting unfavorable urodynamic parameters could be identified.
DISCUSSION Main Findings We hypothesized that in the acute phase of SCI, ambulatory patients rarely present with unfavorable urodynamic parameters such as high maximum detrusor pressure during the storage phase, low
ACUTE SPINAL CORD INJURY AND BLADDER DYSFUNCTION
Table 1. Patient characteristics Ambulatory Mean ⫾ SD pt age 52 ⫾ 15 (18–73) No. gender (%): F 8 (47) M 9 (53) No. ASIA impairment scale (%): A 1 (6) B 2 (12) C 2 (12) D 10 (59) E 2 (12) Mean ⫾ SD days of injury on 29 ⫾ 8 (16–39) urodynamics (range) No. level of injury (%): Cervical 2 (12) Thoracic 4 (24) Lumbar/sacral 11 (64) No. bladder emptying method (%): Spontaneous voiding 5 (29) Aseptic intermittent self2 (12) catheterization Indwelling catheter 10 (59) No. bladder medication (%): None 15 (88) Antimuscarinic 2 (12)
Nonambulatory
p Value
60 ⫾ 20 (18–87) 0.17 0.84 19 (44) 24 (56) 0.014 8 (19) 11 (26) 14 (33) 7 (16) 3 (7) 31 ⫾ 8 (14–39) 0.36 0.003 12 (28) 24 (56) 7 (16) 0.17 5 (12) 3 (7) 35 (81) 0.77 39 (91) 4 (9)
compliance bladder, DO, DESD or vesicoureterorenal reflux. Thus, urodynamic investigations might not be necessary in this specific group of patients. However, we found similar unfavorable urodynamic measures in ambulatory and nonambulatory patients with acute SCI, indicating that the same meticulous neurourological assessment including urodynamic investigations should be offered to all patients with acute SCI independent of the ability to walk. Findings in Context of Existing Evidence A large cross-sectional study including 243 SCI patients with a mean injury duration of 18 ⫾ 12 years demonstrated that the correlation between somatic neurological findings and urodynamic findings is not exact.11 In addition, in a series of 64 ambulatory patients with chronic SCI, Patki et al revealed NLUTD in 92% of ASIA D and in 32% of ASIA E patients.12 Both studies included patients in the chronic phase only and, to the best of our knowledge, there is no study comparing the urodynamic parameters of ambulatory and nonambulatory patients in the acute phase of SCI. It is currently recognized that NLUTD due to SCI is not a stable, chronic disease. Variability in lower urinary tract function is usually seen on followup and modifications of bladder management are often necessary.13 Thus, the comprehension of the disease in all stages, including the acute phase, is necessary to better understand the pathomechanisms involved. In this context Wa-
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tanabe et al documented urodynamic abnormalities in acute cases of incomplete SCI (duration of injury 3 to 14 days).14 NLUTD was apparent in 100%, 82% and 41% of ASIA C, D and E patients, respectively. These findings demonstrate the poor accuracy of the ASIA impairment scale in predicting lower urinary tract dysfunction and are in line with those of the present study. Implications for Practice Morbidity and mortality in SCI patients are closely related to bladder function. Since neurourological management evolved from reflex voiding and indwelling catheters to the widespread use of regular urodynamics, intermittent (self-) catheterization and antimuscarinics, optimized bladder management contributed significantly to improved outcomes in SCI patients with a substantial decrease in morbidity and mortality due to urological complications.1,2,13,15–18 Generally accepted risk factors jeopardizing the upper urinary tract are high detrusor pressure during the storage phase due to a low compliance bladder and/or DO combined with DESD. Urodynamic investigations are needed to identify these conditions requiring urological treatment to protect the upper urinary tract.3–5 In patients with DO and DESD, the therapeutic concept is to convert the overactive detrusor into an underactive detrusor with antimuscarinics, and to assist or accomplish bladder emptying by intermittent (self-) catheterization. If this cannot be achieved by antimuscarinics, intradetrusor botulinum neurotoxin type A injections or, rarely, bladder augmentation or urinary diversion are considered. Although the importance of urodynamic investigations in patients with NLUTD is undisputed, the optimal frequency remains unclear.19 The European Association of Urology recommends routine annual or biannual urodynamic investigations as well as on demand when risk factors emerge.20 In contrast, the United Kingdom SCI Table 2. Urodynamic findings Ambulatory Mean ⫾ SD cm H2O max detrusor pressure during storage phase (range) Mean ⫾ SD ml/cm H2O bladder compliance (range) No. unfavorable urodynamic parameters (%): High pressure system during storage phase Low compliance bladder Detrusor overactivity DESD Vesicoureterorenal reflux
Nonambulatory
p Value
31 ⫾ 20 (11–86)
36 ⫾ 23
(4–92)
0.38
59 ⫾ 35 (15–150)
50 ⫾ 25 (12–105)
0.25
8 (47)
28 (65)
0.19
5 (29)
14 (33)
0.81
2 (12) 4 (24) 3 (18) 0
3 (7) 20 (47) 9 (21) 2 (5)*
0.54 0.10 0.77 0.36
* Unilateral vesicoureterorenal reflux on the right side.
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Think Tank consensus paper proposes repeat urodynamic investigations for specific indications only, ie previous unsafe features, new/deteriorating symptoms and/or signs, and changing management objectives.21 In the present study an unexpectedly high incidence of unfavorable urodynamic measures requiring neurourological treatment was found in our ambulatory patients with acute SCI, ie a high pressure system during the storage phase in 29%, low compliance bladder in 12%, DO in 24% and DESD in 18%. Importantly these values were similar in ambulatory vs nonambulatory patients with acute SCI. Considering the findings of the present study, and the fact that early diagnosis and treatment are important in NLUTD,20 we recommend early proactive neurourological management in patients with acute SCI as well, ie before the development of the chronic state of the disease. Indeed, although not proven by randomized, high evidence level studies, it seems reasonable to start an appropriate treatment as early as possible and not wait for the occurrence of complications. Implications for Research Motor function is mediated through the corticospinal tracts immediately dorsal to the sensory nerve fibers in the spinothalamic tracts, which transmit pain impulses. The autonomic system innervating the lower urinary tract is near the most dorsolateral fibers in the spinothalamic tracts.22 Thus, due to the anatomical proximity of the somatic and autonomic systems in the spinal cord, a strong association be-
tween motor and urological impairment might be expected, but this was not the case in our study. The reason for these discordant findings is unclear and needs further investigation. In fact, a holistic approach involving clinical, urodynamic, electrophysiological, structural/biochemical and neuroradiological assessments is highly warranted, and will not only provide new insights into the pathophysiology of the lower urinary tract, but will also improve the neurourological management of the individual patient. Study Limitations Although to our knowledge this is the first comparison of the urodynamic parameters of ambulatory vs nonambulatory patients with acute SCI, our study has limitations. Our unit is part of a highly specialized university spinal cord injury center so that a negative selection bias, ie the inclusion of more severe cases, cannot be completely ruled out. In addition, our study was not randomized, ie we did not compare early vs late (or no) urodynamic investigations. Nevertheless, the present study was prospective and representative of daily clinical practice.
CONCLUSIONS Ambulatory and nonambulatory patients with acute SCI seem to have a similar risk of unfavorable urodynamic measures. Thus, the same neurourological assessment including urodynamic investigations should be offered to all acute SCI patients independent of the ability to walk.
REFERENCES 1. Lidal IB, Snekkevik H, Aamodt G et al: Mortality after spinal cord injury in Norway. J Rehabil Med 2007; 39: 145. 2. Soden RJ, Walsh J, Middleton JW et al: Causes of death after spinal cord injury. Spinal Cord 2000; 38: 604.
6. Abrams P, Cardozo L, Fall M et al: The standardisation of terminology of lower urinary tract function: report from the Standardisation Subcommittee of the International Continence Society. Neurourol Urodyn 2002; 21: 167.
3. McGuire EJ, Woodside JR, Borden TA et al: Prognostic value of urodynamic testing in myelodysplastic patients. J Urol 1981; 126: 205.
7. Ditunno JF Jr, Young W, Donovan WH et al: The international standards booklet for neurological and functional classification of spinal cord injury. American Spinal Injury Association. Paraplegia 1994; 32: 70.
4. Sadananda P, Vahabi B and Drake MJ: Bladder outlet physiology in the context of lower urinary tract dysfunction. Neurourol Urodyn 2011; 30: 708.
8. Itzkovich M, Gelernter I, Biering-Sorensen F et al: The Spinal Cord Independence Measure (SCIM) version III: reliability and validity in a multi-center international study. Disabil Rehabil 2007; 29: 1926.
5. Weld KJ, Graney MJ and Dmochowski RR: Clinical significance of detrusor sphincter dyssynergia type in patients with post-traumatic spinal cord injury. Urology 2000; 56: 565.
9. Schafer W, Abrams P, Liao L et al: Good urodynamic practices: uroflowmetry, filling cystometry, and pressure-flow studies. Neurourol Urodyn 2002; 21: 261.
10. Hackler RH, Hall MK and Zampieri TA: Bladder hypocompliance in the spinal cord injury population. J Urol 1989; 141: 1390. 11. Weld KJ and Dmochowski RR: Association of level of injury and bladder behavior in patients with post-traumatic spinal cord injury. Urology 2000; 55: 490. 12. Patki P, Woodhouse J, Hamid R et al: Lower urinary tract dysfunction in ambulatory patients with incomplete spinal cord injury. J Urol 2006; 175: 1784. 13. Drake MJ, Cortina-Borja M, Savic G et al: Prospective evaluation of urological effects of aging in chronic spinal cord injury by method of bladder management. Neurourol Urodyn 2005; 24: 111. 14. Watanabe T, Vaccaro AR, Kumon H et al: High incidence of occult neurogenic bladder dysfunction in neurologically intact patients with thoracolumbar spinal injuries. J Urol 1998; 159: 965.
ACUTE SPINAL CORD INJURY AND BLADDER DYSFUNCTION
15. Gormley EA: Urologic complications of the neurogenic bladder. Urol Clin North Am 2010; 37: 601. 16. Feifer A and Corcos J: Contemporary role of suprapubic cystostomy in treatment of neuropathic bladder dysfunction in spinal cord injured patients. Neurourol Urodyn 2008; 27: 475. 17. Hansen RB, Biering-Sorensen F and Kristensen JK: Bladder emptying over a period of 10 – 45 years after a traumatic spinal cord injury. Spinal Cord 2004; 42: 631.
18. Pannek J and Kullik B: Does optimizing bladder management equal optimizing quality of life? Correlation between health-related quality of life and urodynamic parameters in patients with spinal cord lesions. Urology 2009; 74: 263. 19. Cameron AP, Rodriguez GM and Schomer KG: Systematic review of urological followup after spinal cord injury. J Urol 2012; 187: 391. 20. Pannek J, Stöhrer M, Blok B et al: Guidelines on Neurogenic Lower Urinary Tract Dysfunction. European Association of Urology Update March
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2011. Available at www.uroweb.org/gls/pdf/ 19_Neurogenic_LR%20II.pdf. Accessed October 1, 2012. 21. Abrams P, Agarwal M, Drake M et al: A proposed guideline for the urological management of patients with spinal cord injury. BJU Int 2008; 101: 989. 22. Brodal A: The autonomic nervous system: the hypothalamus. In: Neurological Anatomy in Relation to Clinical Medicine, 3rd ed. New York: Oxford University Press 1981; pp 698 –787.