Introduction

Spinal cord injury (SCI) causes a significant impact on the affected individual. In addition to a loss of motor function and sensation, the injury causes profound disruption of the person’s control of bodily functions. Loss of bladder and bowel control are two of the most significant problems for persons with SCIs [1]. These deficits result in significant personal distress related to intimacy issues, strained partner relationships, and role changes for family members and friends [2]. Moreover, the lack of the ability to naturally control voiding and defecation results in the need for costly appliances and medications to maintain continence.

As compared to studies pertaining to ambulation, few reports have addressed the recovery of bladder [3,4,5] and bowel function, based upon injury pattern. With regard to the lower urinary tract, continence and bladder emptying 1 year after SCI were predicted by the sensation in S3 for light touch, Spinal Cord Indepence Measure subscales for sphincter management and respiration, and lower extremity motor score [4]. Additionally, persons with greater perianal pinprick, which correlates with S4–5 sensation, had greater ability to void volitionally [4]. We were unable to find any studies predicting recovery of bowel control.

In contrast, many reports have addressed recovery of ambulation after SCI [6, 7]. The majority have utilized the International Standards for the Neurologic Classification of SCI (ISNCSCI) as the standard to document remaining neurologic function after SCI. Moreover, studies have shown that the amount of remaining supraspinal control of motoric function is the best predictor for regaining ambulation [6]. One aspect of neurologic function that has been studied to see if it is predictive of recovery of motor function is that of the lower sacral spinal cord: voluntary anal sphincter control, deep anal sensation and sensation at S4–5. These are the components of the ISNCSCI that comprise sacral sparing; and retention of sensation defines an AIS B injury, whereas, concomitant retention of voluntary anal contraction would signify an AIS C injury. Despite use in clinical trials [8], retrospective and prospective research has documented retention of deep anal sensation is not predictive of motor function [9].

In 2009, a system of classification for remaining autonomic function after SCI, the International Standards for Autonomic Function after SCI (ISAFSCI) was developed through consensus of an international team of experts [10]. The standards were simplified in 2012 [11] and have been assessed for clinical adherence [12], utility of educational workshops [13], and inter-rater reliability [14]. These standards include sections where the clinician can describe the impact of specific injuries on respiratory, cardiovascular, sudomotor, thermoregulatory, bladder, bowel, and sexual functions. Most recently the sacral components of the autonomic standards (assessing bladder, bowel and sexual function) have been utilized in a clinical trial [15]; however, to date we were unable to find any attempts to determine a relationship between these components and the AIS.

This retrospective cross-sectional pilot study was performed to determine whether persons with AIS B injuries would show differential bladder or bowel function as compared to persons with absent sacral sensation (AIS A) or greater retention of sacral responses (AIS C-E).

Methods

The urodynamic and examination methods have been previously described in a prospective study assessing specific patterns of sensory retention and bladder control [3]. Institutional review board approval was obtained for the study. As part of this study, participants underwent an ISNCSCI examination along with queries of their bladder and bowel function based upon the ISAFSCI [10]. Subsequently, participants underwent urodynamic testing to determine whether there was sensation of bladder filling and results were previously described and published.

In this study, a retrospective review of the data regarding the participant’s AIS and their control of bladder and bowel function based upon investigator recorded determination and self-reported data was performed. We hypothesized that there would be a greater retention of sensation and control in participants with more neurologic function as determined by the AIS. Moreover, we believed that both the investigator-determined and self-reported data would show statistically significant differences.

Subjects

Out of an original 79 participants, there were 72 individuals with SCIs who had adequate data to participate in this secondary analysis. Levels of injury ranged from C2 to L4. Participants were a mean of 35 ± 13.0 years of age. There were 41 males and 31 females. Mean years of education was 13.1 ± 2.5. There were 38 participants with AIS A injury, 5 with AIS B and 29 with C-E injuries. All participants had a rectal examination performed and documentation of anal sensation and voluntary contraction were used to document the neurologic status, e.g., those participants with AIS A injury had no sensation and no contraction, whereas AIS B only had sensation and other groups had sensation plus voluntary contraction.

Statistics

SPSS version 23 was used to analyze results. Cross tabs of investigator-determined bladder and bowel function are in Table 1, while self-reported bladder function is in Table 2, and self-reported bowel function is in Table 3. Statistical analysis of various AIS impairment scores versus degree of function is shown in Table 4. Between group comparisons were performed based upon AIS A versus B versus CDE for bowel and bladder control and sensation as determined by the physician and based upon self-report. Pair-by-pair Jonckheere–Herpstra Test was performed to analyze between group differences based upon investigator’s determination of participants bladder and bowel control and participants self-report of historical control of these functions. The Jonckheere–Herpstra test was chosen because it is a non-parametric test which best allows for statistical analysis comparing the two ordered categorical variables: the AIS and the categorized degree to which the patients had bladder and bowel sensation or control (i.e., present, partially present, absent).

Table 1 Crosstabulation of Bladder and Bowel Control Data as deemed by investigator based upon AIS
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Table 2 Self-reported history of bladder sensation and voiding control in persons with SCI based upon AIS
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Table 3 Self-reported sensation and control of bowel movements based upon AIS
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Table 4 Investigator determined and self-reported sensation and control of bladder and bowel
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Results

Statistically significant differences were found in history of bladder control and bowel control per investigator and bladder sensation via self-report between participants categorized as an “A” on the AIS versus participants categorized as a “B” on the AIS. As would be expected by the classification, sample groups of participants categorized as “B” had a tendency towards greater bladder control; however, no statistically significant differences were obtained for the differences between “A” and “B” participant groups for the other variables surveyed: history of voiding control, history of bowel sensation, and history of bowel control. Proportionally, “B” participants did have fewer cases of “absent” responses for all three variables than “A” participants, but there were not enough individuals measured to have any significant results.

Similarly, in comparing AIS “B” groups with combined AIS “C”, “D”, and “E” groups, some variables showed significant differences while others did not. Self-reported bowel sensation and voiding control were more likely in subjects with C, D, or E injuries than with B injuries. Moreover, there was a strong trend in investigator-determined bowel control in participants with B versus C, D, and E injuries (p = 0.05). No significant differences were found between the groups for the other variables surveyed.

All variables had measured significant differences between AIS “A” and combined AIS “C”, “D”, and “E” with p < 0.02. As expected, the “C”, “D”, and “E” groups had much greater proportions of combined present and partially present conditions in each of the measured variables than the “A” groups.

Discussion

Our data are important because they provide an initial overview of how the sacral components of bladder and bowel function of the ISAFSCI are related to the AIS. As expected, there was greater awareness of the sensation of the need to void, have a bowel movement and a greater history of voiding control in persons with AIS B lesions versus AIS A. This is expected because of the incompleteness of sacral function in the B group versus the A group. Similarly, history of voiding control and bowel sensation were more likely in subjects with C, D, or E than with B injuries. Finally, AIS A participants were statistically less likely to have control over all the functions than participants with C-E injuries.

Despite these findings, not all variables were statistically significant between groups. We attribute this to weaknesses of our study, which are the small number of participants and the retrospective nature of this analysis. We believe that further expansion of this study such as can be achieved in a large prospective study monitoring the bladder and bowel recovery patterns of participants with specific AIS groups based upon the ISAFSCI would provide statistically significant results amongst each category of AIS scale.

Clinical trials have targeted recovery of recovery of function using the AIS; however, the meaning of the conversion from AIS A status to AIS B status has not been fully assessed. One study showed there were statistically greater hospitalization costs when comparing thoracic SCI participants across AIS grades [16]. Another showed that people with AIS A injuries and complete lower motor neuron injuries are less likely to have orgasms as compared to participants with all other levels and degrees of injuries [17]. Previous data showed that AIS B participants were more likely to be more independent in bladder management [18], and it was hypothesized that increased bladder sensation could be the reason. On the other hand, sparse research has assessed these responses and a recent study by the same group looking at AIS A versus B conversions focused on the lack of improvement in ambulatory capacity in association with conversion to AIS B rather than sacral function after injury [19].

More attention needs to be paid to the recovery of sacral autonomic function in clinical trials pertaining to neurologic recovery after SCI. However, review of relevant outcome measures [20,21,22] reveals a lack of information regarding retention of bladder sensation and control of voiding in commonly used outcome measures that focus on quality of life issues.

The autonomic standards are currently in a process of revision [23]. One goal of the autonomic standards is to communicate the degree of remaining sacral autonomic function. Thus, they provide a foundation for the study of recovery of sacral autonomic responses through consistent documentation of the degree of remaining bladder and bowel control and sensation and the degree of preservation of specific sexual responses. To our knowledge, the sacral component of the ISAFSCI represents the only available measure where all three functions are grouped. Our study provides a first comparison of the AIS with specific components of sacral autonomic responses assessed via the standards. Our results are retrospective and preliminary with the number of subjects insufficient to obtain statistical significance in all areas assessed. However, these findings should be considered in association with a previous report that documented strong agreement in lower urinary tract, bowel and sexual function with kappa values from 0.41–0.6 [14]. Based upon these data, we believe that further assessment and development of the sacral autonomic components of the ISAFSCI is warranted. We believe that the sacral components of the ISAFSCI should be added to the ISNCSCI. Additionally, we believe that further development of the sacral components of the autonomic standards may be appropriate as an outcome measure specifically tailored to predict recovery of sacral function after SCI.

Conclusion

Regardless of which next steps are taken, bladder, bowel, and sexual function are important aspects of quality of life for persons with SCI, and more attention needs to be paid to determining the anticipated impact of degrees of AIS impairment on the preservation of these functions. Although we have substantial information regarding the impact of specific degrees of SCI on sexual responses such as orgasm and arousal [17, 24, 25], it is important to have greater knowledge of the natural history of specific injury patterns on bladder and bowel function. With this information, researchers will have better data to develop and document therapies to improve bladder and bowel function after SCI.