doi:10.1016/j.expneurol.2005.01.027 
Copyright © 2005 Elsevier Inc. All rights reserved.
A noninvasive ultrasonographic method to evaluate bladder function recovery in spinal cord injured rats
Hans S. Keirstead
, 
, Vadim Fedulov, Frank Cloutier, Oswald Steward and Barry P. Duel
Reeve-Irvine Research Center, Department of Anatomy and Neurobiology, 2111 Gillespie Neuroscience Research Facility, College of Medicine, University of California Irvine, Irvine, CA 92697-4292, USA
Received 6 October 2004;
revised 8 December 2004;
accepted 4 January 2005.
Available online 23 March 2005.
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Abstract
Suprasacral spinal cord injury induces changes in the mechanical and neuronal properties of the bladder resulting in bladder areflexia followed by bladder–sphincter dyssynergia and detrusor muscle hypertrophy, which lead to urinary retention and increased bladder size. These changes are most often quantified using highly skilled urodynamic techniques that involve catheterization. We investigated whether a hand-held digital ultrasound imaging system could monitor urinary retention in the bladder following spinal cord injury in adult rats. Our findings indicate that contusive spinal cord injury resulted in high residual bladder volumes that decreased and stabilized by 2 weeks post-injury but remained significantly higher than control bladder volumes up to 46 days post-injury (the longest time point examined). Post hoc analysis indicated that the degree of bladder function recovery recorded at the end of the study correlated with the degree of bladder function recovery recorded at 6 days post-injury, indicating that bladder function recovery can be predicted by analyzing bladder volume as early as 6 days post-injury. Bladder function recovery correlated with locomotor recovery as assessed using the BBB locomotor rating scale. While providing a noninvasive assessment of bladder function with no detrimental impact on locomotor function or assessment, this protocol provides researchers with a clinically relevant outcome measure for quantifying bladder function recovery after spinal cord injury or after experimental treatments for spinal cord injury.
Keywords: Spinal cord injury; Neurogenic bladder; Residual volume; Ultrasound; Manual crede; Severe lower urinary tract dysfunction
Fig. 1. Experimental set-up. A SonoSite 180 Plus ultrasound with a 10–5 MHz 38-mm linear array transducer was used to measure bladder volumes of spinal cord injured and control animals under isoflurane anesthesia, following depilation of the belly. A digital balance was used to weigh the urine after the ultrasound measurements were taken.
Fig. 2. High-resolution 2-dimensional images of bladders from uninjured (A–D) and injured (E–H) animals acquired using ultrasound. Bladders appear as a dark hypo-echoic oval structure with hyper-echoic surrounding tissue. Measurements were performed by orientating the transducer longitudinally to measure the bladder length (A, E) and depth (B, F) and then rotating the transducer 90° to measure the bladder width (C, G). Volumetric calculations were subsequently performed by the onboard SonoSite software (D, H). Note the increased size of the bladder 6 days following injury (E–H) relative to that from an uninjured animal (A–D).
Fig. 3. Spinal cord injured animals had significantly (P < 0.05) larger bladder volumes as compared to uninjured control animals throughout the study. Bladder volumes in spinal cord injured animals decreased markedly by 8 days post-injury, continued to decrease until approximately 14 days post-injury and remained relatively constant thereafter. At all time points, the mean bladder volume of spinal cord injured rats remained significantly (P < 0.05) elevated as compared to uninjured control rats. Error bars illustrate the standard error.
Fig. 4. Bladder volumes calculated using ultrasonography did not differ significantly (P < 0.05) from the weight of urine expressed via manual crede under anesthesia in both spinal cord injured (A) and control (B) animals. Linear regression analysis indicated a highly significant correlation coefficient for the two sampling methods (C).
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Fig. 5. Post hoc analysis of bladder volume and weight measurements indicated that spinal cord injured animals varied with respect to recovery of bladder function. (A) Segregation of spinal cord injured animals into those with the greatest bladder volume at day 46 post-injury and those with the least bladder volume at day 46 post-injury revealed that significant differences in bladder volume between the two groups were detectable as early as day 6 post-injury. This finding indicates that bladder function recovery can be predicted by analyzing bladder volume as early as 6 days post-injury. (B) Spinal cord injured animals with the greatest bladder weight were the same animals with the greatest bladder volume at days 6 and 46 post-injury. Spinal cord injured animals with the least bladder weight were the same animals with the least bladder volume at days 6 and 46 post-injury; although this animal group did recover bladder volumes to a degree that was not significantly different than uninjured control animals (A), the mean bladder weight at the end of the study was significantly higher (P < 0.05) than the mean bladder weight of uninjured control animals.
Fig. 6. The degree of bladder function recovery correlated with locomotor recovery as assessed with the BBB locomotor rating scale. (A) Spinal cord injured animals progressively recovered locomotor skills until approximately 3 weeks post-injury when their locomotor skills reached a plateau. The low BBB scores indicate that the animals did not recover weight supported stepping during the duration of the study. (B) When animals were segregated into those with the greatest bladder volume at day 46 post-injury and those with the least bladder volume at day 46 post-injury, there was a significant (P < 0.05) correlation between the degree of bladder function recovery and locomotor skills.
Abstract
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