Management of urinary and bowel dysfunction in rabbit model of spinal cord injury using Schwann cells and muscle progenitors: functional study and evidence for novel mechanism of action.


Journal

International urology and nephrology
ISSN: 1573-2584
Titre abrégé: Int Urol Nephrol
Pays: Netherlands
ID NLM: 0262521

Informations de publication

Date de publication:
May 2021
Historique:
received: 08 09 2020
accepted: 13 11 2020
pubmed: 28 11 2020
medline: 1 10 2021
entrez: 27 11 2020
Statut: ppublish

Résumé

We tried to investigate the role of Schwann and satellite cells in the treatment of neurogenic bladder and bowel dysfunction; following spinal cord injury in the rabbit model. Twelve male New Zealand rabbits underwent induction of neurogenic bladder by spinal cord injury. Rabbits underwent the fiber tractography analysis to confirm the induction of spinal cord injury. Then, animals were randomly divided into two groups. In group I (n = 4), Schwann cells were obtained from autologous peroneal nerve. In group II (n = 4), the co-culture of nerve-muscle cells was obtained from autologous peroneal nerve and quadriceps muscle. Animals in the control group (n = 4) did not undergo any rehabilitation therapy. One and 4 months after injection of cells into the external anal sphincter, electromyography, urethral pressure profiles, urodynamic studies, voiding cystourethrogram, and manometry was performed to confirm the efficacy of treatment in short- (1 month) and long-term (4 months) follow-ups. The investigations validated that no statistically significant difference was detected between the two experimental groups in a short-term follow-up (p-value > 0.05). However, the functional features were improved in group II in long-term follow-up. In both groups, the external anal sphincter contracted in response to electrical signals delivered to the muscle. However, more signals were detected in group II in electromyography evaluation. The immunohistochemical staining demonstrated that the histological features of the bladder and spinal cord were more satisfactory in group II in all follow-ups compared to group I, in terms of less edema, inflammation, presence of progenitor cells, and expression of muscle and nerve markes. Our results suggested that the injection of nerve-muscle co-culture cells into the external anal sphincter may be a helpful tactic for ameliorating the urological complications; following spinal cord injury induction in the rabbit model.

Identifiants

pubmed: 33245534
doi: 10.1007/s11255-020-02722-5
pii: 10.1007/s11255-020-02722-5
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

893-906

Subventions

Organisme : Tehran University of Medical Sciences and Health Services
ID : 977295

Références

Esclarín De Ruz A, García Leoni E, Herruzo Cabrera R (2000) Epidemiology and risk factors for urinary tract infection in patients with spinal cord injury. J Urol 164(4):1285–1289
doi: 10.1016/S0022-5347(05)67157-1
Krassioukov A, Eng JJ, Claxton G, Sakakibara BM, Shum S (2010) Neurogenic bowel management after spinal cord injury: a systematic review of the evidence. Spinal Cord 48(10):718
doi: 10.1038/sc.2010.14
Simpson LA, Eng JJ, Hsieh JT, Wolfe DL, the Spinal Cord Injury Rehabilitation Evidence Research Team (2012) The health and life priorities of individuals with spinal cord injury: a systematic review. J Neurotrauma 29(8):1548–1555
doi: 10.1089/neu.2011.2226
Anderson KD (2004) Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma 21(10):1371–1383
doi: 10.1089/neu.2004.21.1371
Hamid R, Averbeck MA, Chiang H, Garcia A, Al Mousa RT, Oh S-J, Patel A, Plata M, Del Popolo G (2018) Epidemiology and pathophysiology of neurogenic bladder after spinal cord injury. World J Urol 36(10):1517–1527
doi: 10.1007/s00345-018-2301-z
Manack A, Motsko SP, Haag-Molkenteller C, Dmochowski RR, Goehring EL Jr, Nguyen-Khoa BA, Jones JK (2011) Epidemiology and healthcare utilization of neurogenic bladder patients in a US claims database. Neurourol Urodyn 30(3):395–401
doi: 10.1002/nau.21003
Hubscher CH, Herrity AN, Williams CS, Montgomery LR, Willhite AM, Angeli CA, Harkema SJ (2018) Improvements in bladder, bowel and sexual outcomes following task-specific locomotor training in human spinal cord injury. PLoS ONE 13(1):e0190998
doi: 10.1371/journal.pone.0190998
Al Taweel W, Seyam R (2015) Neurogenic bladder in spinal cord injury patients. Res Rep Urol 7:85
Wöllner J, Pannek J (2016) Initial experience with the treatment of neurogenic detrusor overactivity with a new β-3 agonist (mirabegron) in patients with spinal cord injury. Spinal Cord 54(1):78
doi: 10.1038/sc.2015.195
Zhu Y, Uezono N, Yasui T, Nakashima K (2018) Neural stem cell therapy aiming at better functional recovery after spinal cord injury. Dev Dyn 247(1):75–84
doi: 10.1002/dvdy.24558
Doumit ME, Merkel RA (1992) Conditions for isolation and culture of porcine myogenic satellite cells. Tissue Cell 24(2):253–262
doi: 10.1016/0040-8166(92)90098-R
Kajbafzadeh A-M, Elmi A, Talab SS, Esfahani SA, Tourchi A (2010) Functional external anal sphincter reconstruction for treatment of anal incontinence using muscle progenitor cell auto grafting. Dis Colon Rectum 53(10):1415–1421
doi: 10.1007/DCR.0b013e3181e53088
Welk B, Schneider MP, Thavaseelan J, Traini LR, Curt A, Kessler TM (2018) Early urological care of patients with spinal cord injury. World J Urol 36(10):1537–1544
doi: 10.1007/s00345-018-2367-7
Gao Y, Danforth T, Ginsberg DA (2017) Urologic management and complications in spinal cord injury patients: a 40-to 50-year follow-up study. Urology 104:52–58
doi: 10.1016/j.urology.2017.03.006
Wheeler TL, de Groat W, Eisner K, Emmanuel A, French J, Grill W, Kennelly MJ, Krassioukov A, Santacruz BG, Biering-Sørensen F (2018) Translating promising strategies for bowel and bladder management in spinal cord injury. Exp Neurol 306:169–176
doi: 10.1016/j.expneurol.2018.05.006
Cameron AP, Rodriguez GM, Gursky A, He C, Clemens JQ, Stoffel JT (2015) The severity of bowel dysfunction in patients with neurogenic bladder. J Urol 194(5):1336–1341
doi: 10.1016/j.juro.2015.04.100
Panicker JN, Marcelissen T, von Gontard A, Vrijens D, Abrams P, Wyndaele M (2019) Bladder-bowel interactions: do we understand pelvic organ cross-sensitization? International Consultation on Incontinence Research Society (ICI-RS) 2018. Neurourol Urodyn 38:S25–S34
doi: 10.1002/nau.24111
Pavese C, Schneider MP, Schubert M, Curt A, Scivoletto G, Finazzi-Agrò E, Mehnert U, Maier D, Abel R, Röhrich F (2016) Prediction of bladder outcomes after traumatic spinal cord injury: a longitudinal cohort study. PLoS Med 13(6):e1002041
doi: 10.1371/journal.pmed.1002041
Ronaghi M, Erceg S, Moreno-Manzano V, Stojkovic M (2010) Challenges of stem cell therapy for spinal cord injury: human embryonic stem cells, endogenous neural stem cells, or induced pluripotent stem cells? Stem Cell 28(1):93–99
Kajbafzadeh A-M, Ahmadi H, Montaser-Kouhsari L, Sabetkish S, Ladi-Seyedian S, Sotoudeh M (2019) Intravesical electromotive administration of botulinum toxin type A in improving the bladder and bowel functions: evidence for novel mechanism of action. J Spinal Cord Med 1–7
Gazdic M, Volarevic V, Harrell CR, Fellabaum C, Jovicic N, Arsenijevic N, Stojkovic M (2018) Stem cells therapy for spinal cord injury. Int J Mol Sci 19(4):1039
doi: 10.3390/ijms19041039
Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM, Fike JR, Lee HO, Pfeffer K, Lois C, Morrison SJ, Alvarez-Buylla A (2003) Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nat 425(6961):968
doi: 10.1038/nature02069
Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, Meyer EM, Morel L, Petersen BE, Scott EW (2002) Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nat 416(6880):542
doi: 10.1038/nature730
Ying Q-L, Nichols J, Evans EP, Smith AG (2002) Changing potency by spontaneous fusion. Nature 416(6880):545
doi: 10.1038/nature729
Chen A, Xu XM, Kleitman N, Bunge MB (1996) Methylprednisolone administration improves axonal regeneration into Schwann cell grafts in transected adult rat thoracic spinal cord. Exp Neurol 138(2):261–276
doi: 10.1006/exnr.1996.0065
Paino CL, Bunge MB (1991) Induction of axon growth into Schwann cell implants grafted into lesioned adult rat spinal cord. Exp Neurol 114(2):254–257
doi: 10.1016/0014-4886(91)90043-C
Yazdani SO, Hafizi M, Zali A-R, Atashi A, Ashrafi F, Seddighi A-S, Soleimani M (2013) Safety and possible outcome assessment of autologous Schwann cell and bone marrow mesenchymal stromal cell co-transplantation for treatment of patients with chronic spinal cord injury. Cytotherapy 15(7):782–791
doi: 10.1016/j.jcyt.2013.03.012
Cao Q-L, Howard RM, Dennison JB, Whittemore SR (2002) Differentiation of engrafted neuronal-restricted precursor cells is inhibited in the traumatically injured spinal cord. Exp Neurol 177(2):349–359
doi: 10.1006/exnr.2002.7981
Cao Q-l, Zhang YP, Howard RM, Walters WM, Tsoulfas P, Whittemore SR (2001) Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp Neurol 167(1):48–58
doi: 10.1006/exnr.2000.7536
Geffner L, Santacruz P, Izurieta M, Flor L, Maldonado B, Auad A, Montenegro X, Gonzalez R, Silva F (2008) Administration of autologous bone marrow stem cells into spinal cord injury patients via multiple routes is safe and improves their quality of life: comprehensive case studies. Cell Transplant 17(12):1277–1293
doi: 10.3727/096368908787648074
Čížková D, Rosocha J, Vanický I, Jergová S, Čížek M (2006) Transplants of human mesenchymal stem cells improve functional recovery after spinal cord injury in the rat. Cell Mol Neurobiol 26(7–8):1165–1178
doi: 10.1007/s10571-006-9093-1
Khan S, Mafi P, Mafi R, Khan W (2018) A systematic review of mesenchymal stem cells in spinal cord injury, intervertebral disc repair and spinal fusion. Curr Stem Cell Res Ther 13(4):316–323
doi: 10.2174/1574888X11666170907120030
Fandel TM, Trivedi A, Nicholas CR, Zhang H, Chen J, Martinez AF, Noble-Haeusslein LJ, Kriegstein AR (2016) Transplanted human stem cell-derived interneuron precursors mitigate mouse bladder dysfunction and central neuropathic pain after spinal cord injury. Cell Stem Cell 19(4):544–557
doi: 10.1016/j.stem.2016.08.020
Kajbafzadeh A-M, Kajbafzadeh M, Sabetkish S, Sabetkish N, Tavangar SM (2016) Tissue-engineered external anal sphincter using autologous myogenic satellite cells and extracellular matrix: functional and histological studies. Ann Biomed Eng 44(5):1773–1784
doi: 10.1007/s10439-015-1468-3

Auteurs

Shabnam Sabetkish (S)

Pediatric Urology and Regenerative Medicine Research Center, Section of Tissue Engineering and Stem Cells Therapy, Children's Hospital Medical Center, Tehran University of Medical Sciences, No. 62, Dr. Gharib's Street, Keshavarz Boulevard, Tehran, Iran.

Reza Nejad Gashti (RN)

Pediatric Urology and Regenerative Medicine Research Center, Section of Tissue Engineering and Stem Cells Therapy, Children's Hospital Medical Center, Tehran University of Medical Sciences, No. 62, Dr. Gharib's Street, Keshavarz Boulevard, Tehran, Iran.

Bahareh Mohammadi Jobani (BM)

Pediatric Urology and Regenerative Medicine Research Center, Section of Tissue Engineering and Stem Cells Therapy, Children's Hospital Medical Center, Tehran University of Medical Sciences, No. 62, Dr. Gharib's Street, Keshavarz Boulevard, Tehran, Iran.

Maryam Alijani (M)

Pediatric Urology and Regenerative Medicine Research Center, Section of Tissue Engineering and Stem Cells Therapy, Children's Hospital Medical Center, Tehran University of Medical Sciences, No. 62, Dr. Gharib's Street, Keshavarz Boulevard, Tehran, Iran.

Maryam Farsi (M)

Pediatric Urology and Regenerative Medicine Research Center, Section of Tissue Engineering and Stem Cells Therapy, Children's Hospital Medical Center, Tehran University of Medical Sciences, No. 62, Dr. Gharib's Street, Keshavarz Boulevard, Tehran, Iran.

Shaghayegh Mousavi (S)

Pediatric Urology and Regenerative Medicine Research Center, Section of Tissue Engineering and Stem Cells Therapy, Children's Hospital Medical Center, Tehran University of Medical Sciences, No. 62, Dr. Gharib's Street, Keshavarz Boulevard, Tehran, Iran.

Alireza Moradzadeh (A)

Pediatric Urology and Regenerative Medicine Research Center, Section of Tissue Engineering and Stem Cells Therapy, Children's Hospital Medical Center, Tehran University of Medical Sciences, No. 62, Dr. Gharib's Street, Keshavarz Boulevard, Tehran, Iran.

Jaleh Parizad (J)

Pediatric Urology and Regenerative Medicine Research Center, Section of Tissue Engineering and Stem Cells Therapy, Children's Hospital Medical Center, Tehran University of Medical Sciences, No. 62, Dr. Gharib's Street, Keshavarz Boulevard, Tehran, Iran.

Masoumeh Majidi Zolbin (MM)

Pediatric Urology and Regenerative Medicine Research Center, Section of Tissue Engineering and Stem Cells Therapy, Children's Hospital Medical Center, Tehran University of Medical Sciences, No. 62, Dr. Gharib's Street, Keshavarz Boulevard, Tehran, Iran.

Abdol-Mohammad Kajbafzadeh (AM)

Pediatric Urology and Regenerative Medicine Research Center, Section of Tissue Engineering and Stem Cells Therapy, Children's Hospital Medical Center, Tehran University of Medical Sciences, No. 62, Dr. Gharib's Street, Keshavarz Boulevard, Tehran, Iran. kajbafzd@sina.tums.ac.ir.

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