Advertisement

Effect of Different Forms of Activity-Based Recovery Training on Bladder, Bowel, and Sexual Function After Spinal Cord Injury

Published:December 02, 2020DOI:https://doi.org/10.1016/j.apmr.2020.11.002

      Abstract

      Objectives

      To investigate whether the urogenital and bowel functional gains previously demonstrated post-locomotor step training after chronic spinal cord injury could have been derived due to weight-bearing alone or from exercise in general.

      Design

      Prospective cohort study; pilot trial with small sample size.

      Setting

      Urogenital and bowel scientific core facility at a rehabilitation institute and spinal cord injury research center in the United States.

      Participants

      Men and women (N=22) with spinal cord injury (American Spinal Injury Association Impairment Scale grades of A-D) participated in this study.

      Interventions

      Approximately 80 daily 1-hour sessions of either stand training or nonweight-bearing arm crank ergometry. Comparisons were made with previously published locomotor training data (step; N=7).

      Main Outcome Measures

      Assessments at both pre- and post-training timepoints included cystometry for bladder function and International Data Set Questionnaires for bowel and sexual functions.

      Results

      Cystometry measurements revealed a significant decrease in bladder pressure and limited improvement in compliance with nonweight-bearing exercise but not with standing. Although International Data Set questionnaires revealed profound bowel dysfunction and marked deficits in sexual function pretraining, no differences were identified poststand or after nonweight-bearing exercise.

      Conclusions

      These pilot trial results suggest that, although stand and weight-bearing alone do not benefit pelvic organ functions after spinal cord injury, exercise in general may contribute at least partially to the lowering of bladder pressure and the increase in compliance that was seen previously with locomotor training, potentially through metabolic, humoral, and/or cardiovascular mechanisms. Thus, to maximize activity-based recovery training benefits for functions related to storage and emptying, an appropriate level of sensory input to the spinal cord neural circuitries controlling bladder and bowel requires task-specific stepping.

      Keywords

      List of abbreviations:

      AD (autonomic dysreflexia), AIS (American Spinal Injury Association Impairment Scale), BWSS (body weight support system), CIC (clean intermittent catheterization), Fr (French), FSFI (female sexual function index), IIEF (International Index of Erectile Function), LT (locomotor training), NBD (neurogenic bowel dysfunction), SCI (spinal cord injury), SP (suprapubic catheter), UDS (urodynamic study), UE (upper extremity)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Archives of Physical Medicine and Rehabilitation
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Anderson K.D.
        Targeting recovery: priorities of the spinal cord-injured population.
        J Neurotrauma. 2004; 21: 1371-1383
        • Anderson K.D.
        • Borisoff J.F.
        • Johnson R.D.
        • Stiens S.A.
        • Elliott S.L.
        The impact of spinal cord injury on sexual function: concerns of the general population.
        Spinal Cord. 2007; 45: 328-337
        • Anderson K.D.
        • Borisoff J.F.
        • Johnson R.D.
        • Stiens S.A.
        • Elliott S.L.
        Long-term effects of spinal cord injury on sexual function in men: implications for neuroplasticity.
        Spinal Cord. 2007; 45: 338-348
        • Ditunno P.L.
        • Patrick M.
        • Stineman M.
        • Ditunno J.F.
        Who wants to walk? Preferences for recovery after SCI: a longitudinal and cross-sectional study.
        Spinal Cord. 2008; 46: 500-506
        • Glickman S.
        • Kamm M.A.
        Bowel dysfunction in spinal-cord-injury patients.
        Lancet. 1996; 347: 1651-1653
        • Wheeler T.L.
        • de Groat W.
        • Eisner K.
        • et al.
        Translating promising strategies for bowel and bladder management in spinal cord injury.
        Exp Neurol. 2018; 306: 169-176
        • Harkema S.J.
        Neural plasticity after human spinal cord injury: application of locomotor training to the rehabilitation of walking.
        Neuroscientist. 2001; 7: 455-468
        • Dietz V.
        • Harkema S.J.
        Locomotor activity in spinal cord-injured persons.
        J Appl Physiol (1985). 2004; 96: 1954-1960
        • Dietz V.
        • Colombo G.
        • Jensen L.
        • Baumgartner L.
        Locomotor capacity of spinal cord in paraplegic patients.
        Ann Neurol. 1995; 37: 574-582
        • Edgerton V.R.
        • Roy R.R.
        • Hodgson J.A.
        • Prober R.J.
        • de Guzman C.P.
        • de Leon R.
        A physiological basis for the development of rehabilitative strategies for spinally injured patients.
        J Am Paraplegia Soc. 1991; 14: 150-157
        • Edgerton V.R.
        • Tillakaratne N.J.
        • Bigbee A.J.
        • de Leon R.D.
        • Roy R.R.
        Plasticity of the spinal neural circuitry after injury.
        Annu Rev Neurosci. 2004; 27: 145-167
        • Harkema S.J.
        • Hillyer J.
        • Schmidt-Read M.
        • Ardolino E.
        • Sisto S.A.
        • Behrman A.L.
        Locomotor training: as a treatment of spinal cord injury and in the progression of neurologic rehabilitation.
        Arch Phys Med Rehabil. 2012; 93: 1588-1597
        • Harkema S.J.
        • Hurley S.L.
        • Patel U.K.
        • Requejo P.S.
        • Dobkin B.H.
        • Edgerton V.R.
        Human lumbosacral spinal cord interprets loading during stepping.
        J Neurophysiol. 1997; 77: 797-811
        • Forssberg H.
        • Grillner S.
        • Halbertsma J.
        The locomotion of the low spinal cat. I. Coordination within a hindlimb.
        Acta physiologica Scandinavica. 1980; 108: 269-281
        • Dietz V.
        • Colombo G.
        • Jensen L.
        Locomotor activity in spinal man.
        Lancet. 1994; 344: 1260-1263
        • Dietz V.
        • Quintern J.
        • Sillem M.
        Stumbling reactions in man: significance of proprioceptive and pre-programmed mechanisms.
        J Physiol. 1987; 386: 149-163
        • Harkema S.J.
        Plasticity of interneuronal networks of the functionally isolated human spinal cord.
        Brain Res Rev. 2008; 57: 255-264
        • Holmes G.M.
        • Hubscher C.H.
        • Krassioukov A.
        • Jakeman L.B.
        • Kleitman N.
        Recommendations for evaluation of bladder and bowel function in pre-clinical spinal cord injury research.
        J Spinal Cord Med. 2020; 43: 165-176
        • Tate D.G.
        • Wheeler T.
        • Lane G.I.
        • et al.
        Recommendations for evaluation of neurogenic bladder and bowel dysfunction after spinal cord injury and/or disease.
        J Spinal Cord Med. 2020; 43: 141-164
        • Hubscher C.H.
        • Herrity A.N.
        • Williams C.S.
        • et al.
        Improvements in bladder, bowel and sexual outcomes following task-specific locomotor training in human spinal cord injury.
        PLoS One. 2018; 13e0190998
        • Hubscher C.H.
        • Montgomery L.R.
        • Fell J.D.
        • et al.
        Effects of exercise training on urinary tract function after spinal cord injury.
        Am J Physiol Renal Physiol. 2016; 310: F1258-F1268
        • Ward P.J.
        • Herrity A.N.
        • Smith R.R.
        • et al.
        Novel multi-system functional gains via task specific training in spinal cord injured male rats.
        J Neurotrauma. 2014; 31: 819-833
        • Galea M.P.
        Spinal cord injury and physical activity: preservation of the body.
        Spinal Cord. 2012; 50: 344-351
        • Marino R.J.
        • Barros T.
        • Biering-Sorensen F.
        • et al.
        International standards for neurological classification of spinal cord injury.
        J Spinal Cord Med. 2003; 26: S50-S56
        • Waring 3rd, W.P.
        • Biering-Sorensen F.
        • Burns S.
        • et al.
        2009 review and revisions of the international standards for the neurological classification of spinal cord injury.
        J Spinal Cord Med. 2010; 33: 346-352
        • Canton S.
        • Momeni K.
        • Ramanujam A.
        • Garbarini E.
        • Forrest G.F.
        Neuromotor response of the leg muscles following a supine, stand retraining with/without neuromuscular electrical stimulation training intervention for individuals with SCI: a case series.
        Annu Int Conf IEEE Eng Med Biol Soc. 2016; 2016: 3143-3146
        • Schäfer W.
        • Abrams P.
        • Liao L.
        • et al.
        Good urodynamic practices: uroflowmetry, filling cystometry, and pressure-flow studies.
        Neurourol Urodyn. 2002; 21: 261-274
        • Blaivas J.G.
        • Awad S.A.
        • Bissada N.
        • et al.
        Urodynamic procedures: recommendations of the Urodynamic Society. I. Procedures that should be available for routine urologic practice.
        Neurourol Urodyn. 1982; 1: 51-55
        • Gammie A.
        • Clarkson B.
        • Constantinou C.
        • et al.
        International Continence Society guidelines on urodynamic equipment performance.
        Neurourol Urodyn. 2014; 33: 370-379
        • Krassioukov A.
        • Warburton D.E.
        • Teasell R.
        • Eng J.J.
        A systematic review of the management of autonomic dysreflexia after spinal cord injury.
        Arch Phys Med Rehabil. 2009; 90: 682-695
        • Biering-Sorensen F.
        • Kennelly M.
        • Kessler T.M.
        • et al.
        International Spinal Cord Injury Lower Urinary Tract Function Basic Data Set (version 2.0).
        Spinal Cord Ser Cases. 2018; 4: 60
        • Krogh K.
        • Emmanuel A.
        • Perrouin-Verbe B.
        • Korsten M.A.
        • Mulcahey M.J.
        • Biering-Sorensen F.
        International spinal cord injury bowel function basic data set (version 2.0).
        Spinal Cord. 2017; 55: 692-698
        • Krogh K.
        • Perkash I.
        • Stiens S.A.
        • Biering-Sorensen F.
        International bowel function basic spinal cord injury data set.
        Spinal Cord. 2009; 47: 230-234
        • Alexander M.S.
        • Biering-Sorensen F.
        • Elliott S.
        • Kreuter M.
        • Sonksen J.
        International spinal cord injury male sexual function basic data set.
        Spinal Cord. 2011; 49: 795-798
        • Rosen R.C.
        • Riley A.
        • Wagner G.
        • Osterloh I.H.
        • Kirkpatrick J.
        • Mishra A.
        The international index of erectile function (IIEF): a multidimensional scale for assessment of erectile dysfunction.
        Urology. 1997; 49: 822-830
        • Alexander M.S.
        • Biering-Sorensen F.
        • Elliott S.
        • Kreuter M.
        • Sonksen J.
        International spinal cord injury female sexual and reproductive function basic data set.
        Spinal Cord. 2011; 49: 787-790
        • Alexander M.S.
        • Brackett N.L.
        • Bodner D.
        • Elliott S.
        • Jackson A.
        • Sonksen J.
        Measurement of sexual functioning after spinal cord injury: preferred instruments.
        J Spinal Cord Med. 2009; 32: 226-236
        • Wiegel M.
        • Meston C.
        • Rosen R.
        The female sexual function index (FSFI): cross-validation and development of clinical cutoff scores.
        J Sex Marital Ther. 2005; 31: 1-20
        • Abrams P.
        • Cardozo L.
        • Fall M.
        • et al.
        The standardisation of terminology of lower urinary tract function: report from the Standardisation Sub-committee of the International Continence Society.
        Neurourol Urodyn. 2002; 21: 167-178
        • Pannek J.
        • Kennelly M.
        • Linsenmeyer T.
        • Wyndaele J.J.
        • Biering-Sorensen F.
        International spinal cord injury urodynamic basic data set (version 2.0).
        Spinal Cord Ser Cases. 2018; 4: 98
        • Monti P.R.
        • Lara R.C.
        • Dutra M.A.
        • de Carvalho J.R.
        New techniques for construction of efferent conduits based on the Mitrofanoff principle.
        Urology. 1997; 49: 112-115
        • Jamil F.
        Towards a catheter free status in neurogenic bladder dysfunction: a review of bladder management options in spinal cord injury (SCI).
        Spinal Cord. 2001; 39: 355-361
        • Hicks A.L.
        • Martin Ginis K.A.
        • Pelletier C.A.
        • Ditor D.S.
        • Foulon B.
        • Wolfe D.L.
        The effects of exercise training on physical capacity, strength, body composition and functional performance among adults with spinal cord injury: a systematic review.
        Spinal Cord. 2011; 49: 1103-1127
        • Adriaansen J.J.
        • van Asbeck F.W.
        • Tepper M.
        • et al.
        Bladder-emptying methods, neurogenic lower urinary tract dysfunction and impact on quality of life in people with long-term spinal cord injury.
        J Spinal Cord Med. 2017; 40: 43-53
        • Lane T.M.
        • Shah P.J.
        Leak-point pressures.
        BJU Int. 2000; 86: 942-949
        • Panicker J.N.
        • de Seze M.
        • Fowler C.J.
        Rehabilitation in practice: neurogenic lower urinary tract dysfunction and its management.
        Clin Rehabil. 2010; 24: 579-589
        • Rosety-Rodriguez M.
        • Camacho A.
        • Rosety I.
        • et al.
        Low-grade systemic inflammation and leptin levels were improved by arm cranking exercise in adults with chronic spinal cord injury.
        Arch Phys Med Rehabil. 2014; 95: 297-302
        • Ordonez F.J.
        • Rosety M.A.
        • Camacho A.
        • et al.
        Arm-cranking exercise reduced oxidative damage in adults with chronic spinal cord injury.
        Arch Phys Med Rehabil. 2013; 94: 2336-2341
        • Horiuchi M.
        • Okita K.
        Arm-cranking exercise training reduces plasminogen activator inhibitor 1 in people with spinal cord injury.
        Arch Phys Med Rehabil. 2017; 98: 2174-2180
        • Behrman A.L.
        • Harkema S.J.
        Locomotor training after human spinal cord injury: a series of case studies.
        Phys Ther. 2000; 80: 688-700
        • Visintin M.
        • Barbeau H.
        The effects of parallel bars, body weight support and speed on the modulation of the locomotor pattern of spastic paretic gait. A preliminary communication.
        Paraplegia. 1994; 32: 540-553
        • Denny-Brown D.
        • Robertson E.
        The state of the bladder and its sphincter in complete transverse lesions of the spinal cord and cauda equina.
        Brain. 1933; 56: 397-469
        • Jolesz F.A.
        • Cheng-Tao X.
        • Ruenzel P.W.
        • Henneman E.
        Flexor reflex control of the external sphincter of the urethra in paraplegia.
        Science. 1982; 216: 1243-1245
        • Mai J.
        • Pedersen E.
        Clonus depression by propranolol.
        Acta Neurol Scand. 1976; 53: 395-398
        • Pedersen E.
        • Petersen T.
        • Schroder H.D.
        Relation between flexor spasms, uninhibited detrusor contractions and anal sphincter activity.
        Journal of neurology, neurosurgery, and Psychiatry. 1986; 49: 273-277
        • Sato A.
        • Sato Y.
        • Sugimoto H.
        • Tervi N.
        Reflex changes in the urinary bladder after mechanical and thermal stimulation of the skin at various segmental levels in cats.
        Neuroscience. 1977; 2: 111-117
        • Tai C.
        • Roppolo J.R.
        • de Groat W.C.
        Spinal reflex control of micturition after spinal cord injury.
        Restor Neurol Neurosci. 2006; 24: 69-78
        • Thor K.B.
        • Roppolo J.R.
        • deGroat W.C.
        Naloxone induced micturition in unanesthetized paraplegic cats.
        J Urol. 1983; 129: 202-205
        • Berkley K.J.
        • Hubscher C.H.
        • Wall P.D.
        Neuronal responses to stimulation of the cervix, uterus, colon, and skin in the rat spinal cord.
        J Neurophysiol. 1993; 69: 545-556
        • MacDonagh R.
        • Sun W.M.
        • Thomas D.G.
        • Smallwood R.
        • Read N.W.
        Anorectal function in patients with complete supraconal spinal cord lesions.
        Gut. 1992; 33: 1532-1538
        • Valles M.
        • Mearin F.
        Pathophysiology of bowel dysfunction in patients with motor incomplete spinal cord injury: comparison with patients with motor complete spinal cord injury.
        Dis Colon Rectum. 2009; 52: 1589-1597
        • Christensen P.
        • Bazzocchi G.
        • Coggrave M.
        • et al.
        Outcome of transanal irrigation for bowel dysfunction in patients with spinal cord injury.
        J Spinal Cord Med. 2008; 31: 560-567
        • Christensen P.
        • Bazzocchi G.
        • Coggrave M.
        • et al.
        A randomized, controlled trial of transanal irrigation versus conservative bowel management in spinal cord-injured patients.
        Gastroenterology. 2006; 131: 738-747
        • Rasmussen M.M.
        • Kutzenberger J.
        • Krogh K.
        • et al.
        Sacral anterior root stimulation improves bowel function in subjects with spinal cord injury.
        Spinal Cord. 2015; 53: 297-301
        • Vardi Y.
        • Dayan L.
        • Apple B.
        • Gruenwald I.
        • Ofer Y.
        • Jacob G.
        Penile and systemic endothelial function in men with and without erectile dysfunction.
        Eur Urol. 2009; 55: 979-985
        • Allers K.A.
        • Richards N.
        • Sultana S.
        • et al.
        I. Slow oscillations in vaginal blood flow: alterations during sexual arousal in rodents and humans.
        J Sex Med. 2010; 7: 1074-1087