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The Effects of Long-Term Spinal Cord Injury on Mechanical Properties of the Rat Urinary Bladder

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Abstract

We have demonstrated that bladder wall tissue in spinal cord injury (SCI) rats at 10 days post-injury is more compliant and accompanied by changes in material class from orthotropic to isotropic as compared to normal tissue. The present study examined the long-term effects (3-, 6-, and 10-weeks) post-SCI on the mechanical properties of bladder wall tissues, along with quantitative changes in smooth muscle orientation and collagen and elastin content. Bladder wall compliance (defined as det(F) − 1 under an equi-biaxial stress state of 100 kPa, where F is the deformation gradient tensor) was found to be significantly greater at 3- and 6-weeks (0.873 ± 0.092 and 0.864 ± 0.112, respectively) when compared to the normal bladders (0.260 ± 0.028), but at 10 weeks the compliance reduced (0.389 ± 0.061) to near that of normal bladders. This trend in mechanical compliance closely paralleled the collagen/elastin ratio. Moreover, changes in material class, assessed using a graphical technique, correlated closely with quantitative changes in smooth muscle fiber orientation. The results of the present study provide the first evidence that, while similarities exist between acute and chronic responses of the urinary bladder wall tissue to SCI, the overall alterations are distinct, result in profound and complex time dependent changes in bladder wall structure, and will lay the basis for simulations of the bladder wall disease process.

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References

  1. Cortivo R., F. Pagano, G. Passerini, G. Abatangelo, I. Castellani (1981). Elastin and collagen in the normal and obstructed urinary bladder. Br. J. Urol. 53(2): 134–137

    Article  PubMed  CAS  Google Scholar 

  2. Criscione J. C., M. S. Sacks, W. C. Hunter (2003). Experimentally tractable, pseudo-elastic constitutive law for biomembranes: I. Theory. J. Biomech. Eng. 125(1): 94–99. doi:10.1115/1.1530770

    Article  PubMed  Google Scholar 

  3. de Groat W. C. (1997). A neurologic basis for the overactive bladder. Urology 50(6A Suppl): 36–52; discussion 53–56

    PubMed  Google Scholar 

  4. de Groat, W. C., A. M. Booth, and N. Yoshimura. Neurophysiology of micturition and its modification in animal models of human disease. In: Nervous Control of the Urogenital System, Vol. 3, edited by C. A. Maggi. Chur: Harwood Academic Publishers, 1993, pp. 227–290

  5. Deveaud C. M., E. J. Macarak, U. Kucich, D. H. Ewalt, W. R. Abrams, P. S. Howard (1998). Molecular analysis of collagens in bladder fibrosis. J. Urol. 160(4): 1518–1527. doi:10.1016/S0022-5347(01)62606-5

    Article  PubMed  CAS  Google Scholar 

  6. Drake M. J., P. Hedlund, I. W. Mills, R. McCoy, G. McMurray, B. P. Gardner, K. E. Andersson, A. F. Brading (2000). Structural and functional denervation of human detrusor after spinal cord injury. Lab. Invest. 80(10): 1491–1499

    PubMed  CAS  Google Scholar 

  7. Fung Y. C. (1993). Biomechanics: Mechanical Properties of Living Tissues. New York, Springer Verlag

    Google Scholar 

  8. Gloeckner, D. C. Tissue Biomechanics of the Urinary Bladder Wall. Pittsburgh: Department of Bioengineering, University of Pittsburgh, 258 p, 2003

  9. Gloeckner D. C., M. S. Sacks, M. O. Fraser, G. T. Somogyi, W. C. de Groat, M. B. Chancellor (2002). Passive biaxial mechanical properties of the rat bladder wall after spinal cord injury. J. Urol. 167(5): 2247–2252. doi:10.1016/S0022-5347(05)65137-3

    Article  PubMed  Google Scholar 

  10. Hackler R. H., M. K. Hall, T. A. Zampieri (1989). Bladder hypocompliance in the spinal cord injury population. J. Urol. 141(6): 1390–1393

    PubMed  CAS  Google Scholar 

  11. Humphrey J. D. (2002). Cardiovascular Solid Mechanics: Cells, Tissues, and Organs. New York, Springer

    Google Scholar 

  12. Kim J. C., J. Y. Yoon, S. I. Seo, T. K. Hwang, Y. H. Park (2000). Effects of partial bladder outlet obstruction and its relief on types I and III collagen and detrusor contractility in the rat. Neurourol. Urodyn. 19(1): 29–42. doi:10.1002/(SICI)1520-6777(2000)19:1<29::AID-NAU5>3.0.CO;2-#

    Article  PubMed  CAS  Google Scholar 

  13. Kim K. M., B. A. Kogan, C. A. Massad, Y. C. Huang (1991). Collagen and elastin in the obstructed fetal bladder. J. Urol. 146(2 (Pt 2)): 528–531

    PubMed  CAS  Google Scholar 

  14. Kondo A., J. G. Susset (1974). Viscoelastic properties of bladder. Investigat. Urol. 11(6):459–465

    CAS  Google Scholar 

  15. Kruse M. N., L. A. Bray, W. C. de Groat (1995). Influence of spinal cord injury on the morphology of bladder afferent and efferent neurons. J. Auton. Nerv. Syst. 54(3): 215–224. doi:10.1016/0165-1838(95)00011-L

    Article  PubMed  CAS  Google Scholar 

  16. Macarak E. J., D. Ewalt, L. Baskin, D. Coplen, H. Koo, R. Levin, J. W. Duckett, H. Snyder, J. Rosenbloom, P. S. Howard (1995). The collagens and their urologic implications. Adv. Exp. Med. Biol. 385: 173–177

    PubMed  CAS  Google Scholar 

  17. Mimata H., F. Satoh, T. Tanigawa, Y. Nomura, J. Ogata (1993). Changes of rat urinary bladder during acute phase of spinal cord injury. Urol. Int. 51(2): 89–93

    PubMed  CAS  Google Scholar 

  18. Nagatomi J., D. C. Gloeckner, M. B. Chancellor, W. C. DeGroat, M. S. Sacks (2004). Changes in the biaxial viscoelastic response of the urinary bladder following spinal cord injury. Ann. Biomed. Eng. 32(10): 1409–1419. doi:10.1114/B:ABME.0000042228.89106.48

    Article  PubMed  Google Scholar 

  19. Nagatomi, J., K. Toosi, M. Chancellor, and M. Sacks. Contribution of the extracellular matrix to the viscoelastic behavior: A new modeling approach for rat bladder wall tissue. Biomech. Model. Mechanobiol., 2007. [Epub ahead of print]

  20. Nagatomi J., K. K. Toosi, J. S. Grashow, M. B. Chancellor, M. S. Sacks (2005). Quantification of bladder smooth muscle orientation in normal and spinal cord injured rats. Ann. Biomed. Eng. 33(8): 1078–1089. doi:10.1007/s10439-005-5776-x

    Article  PubMed  Google Scholar 

  21. Ogawa T. (1991). Bladder deformities in patients with neurogenic bladder dysfunction. Urol. Int. 47(Suppl 1): 59–62

    Article  PubMed  Google Scholar 

  22. Sacks M. S. (2000). Biaxial mechanical evaluation of planar biological materials. J. Elast. 61: 199–246. doi:10.1023/A:1010917028671

    Article  Google Scholar 

  23. Sandberg L. B., N. T. Soskel, J. G. Leslie (1981). Elastin structure, biosynthesis, and relation to disease states. N Engl J. Med. 304(10): 566–579

    PubMed  CAS  Google Scholar 

  24. Shin J. C., C. I. Park, H. J. Kim, I. Y. Lee (2002). Significance of low compliance bladder in cauda equina injury. Spinal Cord 40(12): 650–655. doi:10.1038/sj.sc.3101380

    Article  PubMed  CAS  Google Scholar 

  25. Sun W., M. S. Sacks, M. J. Scott (2005). Effects of boundary conditions on the estimation of the planar biaxial mechanical properties of soft tissues. J. Biomech. Eng. 127(4): 709–715. doi:10.1115/1.1933931

    Article  PubMed  Google Scholar 

  26. Sun W., M. S. Sacks, T. L. Sellaro, W. S. Slaughter, M. J. Scott (2003). Biaxial mechanical response of bioprosthetic heart valve biomaterials to high in-plane shear. J. Biomech. Eng. 125: 372–380. doi:10.1115/1.1572518

    Article  PubMed  Google Scholar 

  27. Uvelius B., A. Mattiasson (1984). Collagen content in the rat urinary bladder subjected to infravesical outflow obstruction. J. Urol. 132(3): 587–590

    PubMed  CAS  Google Scholar 

  28. Vande Geest J. P., M. S. Sacks, D. A. Vorp (2006). The effects of aneurysm on the biaxial mechanical behavior of human abdominal aorta. J. Biomech. 39(7): 1324–1334. doi:10.1016/j.jbiomech.2005.03.003

    Article  PubMed  Google Scholar 

  29. Watanabe T., D. A. Rivas, M. B. Chancellor (1996). Urodynamics of spinal cord injury. Urol. Clin. North Am. 23(3): 459–473. doi:10.1016/S0094-0143(05)70325-6

    Article  PubMed  CAS  Google Scholar 

  30. Weld K. J., M. J. Graney, R. R. Dmochowski (2000). Differences in bladder compliance with time and associations of bladder management with compliance in spinal cord injured patients. J. Urol. 163(4): 1228–1233. doi:10.1016/S0022-5347(05)67730-0

    Article  PubMed  CAS  Google Scholar 

  31. Yoshimura N., C. P. Smith, M. B. Chancellor, W. C. de Groat (2000). Pharmacologic and potential biologic interventions to restore bladder function after spinal cord injury. Curr. Opin. Neurol. 13(6): 677–681. doi:10.1097/00019052-200012000-00011

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors wish to acknowledge funding by NICDH P01-HD39768 and the Paralyzed Veterans of America Spinal Cord Research Foundation (#2289-01). KKT was supported by an NIH T32 training grant (DK7774). The authors wish to also thank Drs. Kazumasa Torimoto and Teruyuki Ogawa for providing the rat bladders used in this study, and Ms. Silvia Wognum for technical assistance.

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Authors and Affiliations

  1. Engineered Tissue Mechanics and Mechanobiology Laboratory, Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, 15219, USA

    Kevin K. Toosi, Jiro Nagatomi & Michael S. Sacks

  2. McGowan Institute for Regenerative Medicine, University of Pittsburgh, 100 Technology Drive, Room 234, Pittsburgh, PA, 15219, USA

    Kevin K. Toosi, Jiro Nagatomi & Michael S. Sacks

  3. Department of Urology, University of Pittsburgh, Pittsburgh, PA, 15219, USA

    Michael B. Chancellor

Authors
  1. Kevin K. Toosi
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  2. Jiro Nagatomi
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  3. Michael B. Chancellor
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  4. Michael S. Sacks
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Correspondence to Michael S. Sacks.

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Toosi, K.K., Nagatomi, J., Chancellor, M.B. et al. The Effects of Long-Term Spinal Cord Injury on Mechanical Properties of the Rat Urinary Bladder. Ann Biomed Eng 36, 1470–1480 (2008). https://doi.org/10.1007/s10439-008-9525-9

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  • DOI: https://doi.org/10.1007/s10439-008-9525-9

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