Key Points
-
The tissue of the urinary bladder undergoes constant loading and unloading cycles to fulfil its role in normal physiological conditions
-
Insight into bladder biomechanics is important for restoring its functional properties when bladder augmentation is required
-
Biomechanical clinical assessments include whole-organ urodynamics, whereas preclinical assessments that have been used in animal models also include ex vivo tensile tests of bladder tissue
-
Biomechanical qualification of tissue-engineered bladder scaffolds is crucial; however, the biomechanics of scaffolds have been poorly researched compared with their structural appearance and cellular interactions
-
Mathematical and computational modelling based on biomechanical studies can be used to predict the mechanical performance of a tissue-engineered scaffold
-
A comprehensive algorithm is recommended to study engineered scaffolds in order to validate preclinical experiments before clinical use of these materials
Abstract
The urinary bladder is a complex organ with the primary functions of storing urine under low and stable pressure and micturition. Many clinical conditions can cause poor bladder compliance, reduced capacity, and incontinence, requiring bladder augmentation or use of regenerative techniques and scaffolds. To replicate an organ that is under frequent mechanical loading and unloading, special attention towards fulfilling its biomechanical requirements is necessary. Several biological and synthetic scaffolds are available, with various characteristics that qualify them for use in bladder regeneration in vitro and in vivo, including in the treatment of clinical conditions. The biomechanical properties of the native bladder can be investigated using a range of mechanical tests for standardized assessments, as well as mathematical and computational bladder biomechanics. Despite a large body of research into tissue engineering of the bladder wall, some features of the native bladder and the scaffolds used to mimic it need further elucidation. Collection of comparable reference data from different animal models would be a helpful tool for researchers and will enable comparison of different scaffolds in order to optimize characteristics before entering preclinical and clinical trials.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Drake, M. J. The integrative physiology of the bladder. Ann. R. Coll. Surg. Engl. 89, 580–585 (2007).
Andersson, K.-E. & Arner, A. Urinary bladder contraction and relaxation: physiology and pathophysiology. Physiol. Rev. 84, 935–986 (2004).
Snow, B. W. & Cartwright, P. C. Bladder autoaugmentation. Urol. Clin. North Am. 23, 323–331 (1996).
Cranidis, A. & Nestoridis, G. Bladder augmentation. Int. Urogynecol. J. Pelv. Floor Dysfunct. 11, 33–40 (2000).
Husmann, D. A. Mortality following augmentation cystoplasty: a transitional urologist's viewpoint. J. Pediatr. Urol. 13, 358–364 (2017).
McDougal, W. S. Metabolic complications of urinary intestinal diversion. J. Urol. 147, 1199–1208 (1992).
Atala, A., Bauer, S. B., Hendren, W. H. & Retik, A. B. The effect of gastric augmentation on bladder function. J. Urol. 149, 1099–1102 (1993).
Kaefer, M. et al. Reservoir calculi: a comparison of reservoirs constructed from stomach and other enteric segments. J. Urol. 160, 2187–2190 (1998).
Atala, A. Tissue engineering of human bladder. Br. Med. Bull. 97, 81–104 (2011).
Atala, A., Bauer, S. B., Soker, S., Yoo, J. J. & Retik, A. B. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet 367, 1241–1246 (2006).
Atala, A. Bladder regeneration by tissue engineering. BJU Int. 88, 765–770 (2001).
Langer, R. & Vacanti, J. P. Tissue engineering. Science 260, 920–926 (1993).
Guilak, F., Butler, D. L., Goldstein, S. A. & Baaijens, F. P. T. Biomechanics and mechanobiology in functional tissue engineering. J. Biomech. 47, 1933–1940 (2014).
Tiemessen, D. et al. The effect of a cyclic uniaxial strain on urinary bladder cells. World J. Urol. 35, 1531–1539 (2017).
Birder, L. A. Urinary bladder urothelium: molecular sensors of chemical/thermal/mechanical stimuli. Vascul. Pharmacol. 45, 221–226 (2006).
Farhat, W. A. & Yeger, H. Does mechanical stimulation have any role in urinary bladder tissue engineering? World J. Urol. 26, 301–305 (2008).
Gill, B. C., Damaser, M. S. & Chermansky, C. J. Future perspectives in bladder tissue engineering. Curr. Bl. Dysfunct. Rep. 10, 443–448 (2015).
Osborn, S. L. & Kurzrock, E. A. Bioengineered bladder tissue — close but yet so far! J. Urol. 194, 619–620 (2015).
Gray, H. in Anatomy of the Human Body 1821–1865 (1918).
Nagatomi, J., Toosi, K. K., Grashow, J. S., Chancellor, M. B. & Sacks, M. S. Quantification of bladder smooth muscle orientation in normal and spinal cord injured rats. Ann. Biomed. Eng. 33, 1078–1089 (2005).
Hakenberg, O. W., Linne, C., Manseck, a & Wirth, M. P. Bladder wall thickness in normal adults and men with mild lower urinary tract symptoms and benign prostatic enlargement. Neurourol. Urodyn. 19, 585–593 (2000).
Alison Blatt, H., Titus, J. and Chan, L. Ultrasound measurement of bladder wall thickness in the assessment of voiding dysfunction. J. Urol. 179, 2275–2279 (2008).
Abrams, P. in Urodynamics 7–16 (Springer-Verlag, London, 2006).
DeLancey, J. O. et al. in Incontinence (eds Abrams, P., Cardozo, L., Khoury, S. & Wein, A.) 17–82 (Health Publication, Plymouth, UK, 2002).
Lee, G. Y. H. & Lim, C. T. Biomechanics approaches to studying human diseases. Trends Biotechnol. 25, 111–118 (2006).
Lim, C. T., Zhou, E. H., Li, A., Vedula, S. R. K. & Fu, H. X. Experimental techniques for single cell and single molecule biomechanics. Mater. Sci. Eng. C 26, 1278–1288 (2005).
Woo, S. L., Gomez, M. A. & Akeson, W. H. The time and history-dependent viscoelastic properties of the canine medical collateral ligament. J. Biomech. Eng. 103, 293–298 (1981).
Johnson, G. A., Livesay, G. A., Woo, S. L.-Y. & Rajagopal, K. R. A. Single integral finite strain viscoelastic model of ligaments and tendons. J. Biomech. Eng. 118, 221–226 (1996).
Deveaud, C. M. et al. Molecular analysis of collagens in bladder fibrosis. J. Urol. 160, 1518–1527 (1998).
Nagatomi, J., Gloeckner, D. C., Chancellor, M. B., DeGroat, W. C. & Sacks, M. S. Changes in the biaxial viscoelastic response of the urinary bladder following spinal cord injury. Ann. Biomed. Eng. 32, 1409–1419 (2004).
Cortivo, R., Pagano, F., Passerini, G., Abatangelo, G. & Castellani, I. Elastin and collagen in the normal and obstructed urinary bladder. Br. J. Urol. 53, 134–137 (1981).
Thompoulos, S. & Genin, G. M. in Orthopaedic Biomechanics (ed. Winkelstein, B. A.) 49–74 (CRC Press, 2012).
Nitta, N., Shiina, T. & Ueno, E. in IEEE Symposium on Ultrasonics Vol. 2 1606–1609 (Honolulu, HI, USA 2003).
Zanetti, E. M., Perrini, M., Bignardi, C. & Audenino, A. L. Bladder tissue passive response to monotonic and cyclic loading. Biorheology 49, 49–63 (2012).
Ross, S. E. et al. Hysteretic behavior of bladder afferent neurons in response to changes in bladder pressure. BMC Neurosci. 17, 57 (2016).
Mastrigt, R. & Nagtegaal, J. Dependence of the.viscoelastic response of the urinary bladder wall on strain rate. Med. Biol. Eng. Comput 19, 291–296 (1981).
Natali, A. N. et al. Bladder tissue biomechanical behavior: experimental tests and constitutive formulation. J. Biomech. 48, 3088–3096 (2015).
Nagatomi, J., Toosi, K. K., Chancellor, M. B. & Sacks, M. S. Contribution of the extracellular matrix to the viscoelastic behavior of the urinary bladder wall. Biomech. Model. Mechanobiol. 7, 395–404 (2008).
Levin, R. M., Horan, P. & Liu, S. P. Metabolic aspects of urinary bladder filling. Scand. J. Urol. Nephrol. Suppl. 201, 59–66 (1999).
Blaivas, J., Chancellor, M. B., Weiss, J. & Verhaaren, M. in Atlas of Urodynamics 2nd edn 56–61 (Wiley-Blackwell, Oxford, UK, 2008).
Harris, R. L., Cundiff, G. W., Theofrastous, J. P. & Bump, R. C. Bladder compliance in neurologically intact women. Neurourol. Urodyn. 15, 483–488 (1996).
Cho, S., Yi, J. & Oh, S. The clinical significance of poor bladder compliance. Neurourol. Urodyn. 28, 1010–1014 (2009).
McGuire, E. J., Woodside, J. R., Borden, T. A. & Weiss, R. M. Prognostic value of urodynamic testing in myelodysplastic patients. J. Urol. 167, 1049–1053 (2002).
Weston, P. M., Robinson, L. Q., Williams, S., Thomas, M. & Stephenson, T. P. Poor compliance early in filling in the neuropathic bladder. Br. J. Urol. 63, 28–31 (1989).
Ogawa, T. Bladder deformities in patients with neurogenic bladder dysfunction. Urol. Int. 47 (Suppl. 1), 59–62 (1991).
Gilmour, R. F. et al. A new technique for dynamic analysis of bladder compliance. J. Urol. 150, 1200–1203 (1993).
Weld, K. J., Graney, M. J. & Dmochowski, R. R. Differences in bladder compliance with time and associations of bladder management with compliance in spinal cord injured patients. J. Urol. 163, 1228–1233 (2000).
Alexander, R. S. Mechanical properties of urinary bladder. Am. J. Physiol. 220, 1413–1421 (1971).
Coplen, D. E., Macarak, E. J. & Levin, R. M. Developmental changes in normal fetal bovine whole bladder physiology. J. Urol. 151, 1391–1395 (1994).
Macarak, E. J. & Howard, P. S. The collagens and their urologic significance. Scand. J. Urol. Nephrol. Suppl. 184, 25–33 (1997).
Murakumo, M. et al. Three-dimensional arrangement of collagen and elastin fibers in the human urinary bladder: a scanning electron microscopic study. J. Urol. 154, 251–256 (1995).
Dahms, S. E., Piechota, H. J., Dahiya, R. & Lue, T. F. & Tanagho, E. A. Composition and biomechanical properties of the bladder acellular matrix graft: Comparative analysis in rat, pig and human. Br. J. Urol. 82, 411–419 (1998).
Beach, Z. M., Gittings, D. J. & Soslowsky, L. J. in Muscle and Tendon Injuries: Evaluation and Management (eds Canata, G. L., d'Hooghe, P. & Hunt, K. J.) 15–22 (Springer, Berlin and Heidelberg, 2017).
Martins, P. A. et al. Uniaxial mechanical behavior of the human female bladder. Int. Urogynecol. J. 22, 991–995 (2011).
Korossis, S., Bolland, F., Southgate, J., Ingham, E. & Fisher, J. Regional biomechanical and histological characterisation of the passive porcine urinary bladder: implications for augmentation and tissue engineering strategies. Biomaterials 30, 266–275 (2009).
Chen, J., Drzewiecki, B. A., Merryman, W. D. & Pope, J. C. Murine bladder wall biomechanics following partial bladder obstruction. J. Biomech. 46, 2752–2755 (2013).
Parekh, A. et al. Ex vivo deformations of the urinary bladder wall during whole bladder filling: contributions of extracellular matrix and smooth muscle. J. Biomech. 43, 1708–1716 (2010).
Gloeckner, D. C. et al. Passive biaxial mechanical properties of the rat bladder wall after spinal cord injury. J. Urol. 167, 2247–2252 (2002).
Chen, F., Wang, G., Li, L. & Cheng, H. Mechanical properties of a woven ramie fabric under multidimensional loadings. Text. Res. J. 81, 1226–1233 (2011).
Özdemir, H. & Mert, E. The effects of fabric structural parameters on the tensile, bursting, and impact strengths of cellular woven fabrics. J. Text. Inst. 104, 330–338.
Freytes, D. O., Badylak, S. F., Webster, T. J., Geddes, L. A. & Rundell, A. E. Biaxial strength of multilaminated extracellular matrix scaffolds. Biomaterials 25, 2353–2361 (2004).
Whitson, B. A. et al. Multilaminate resorbable biomedical device under biaxial loading. J. Biomed. Mater. Res. 43, 277–281 (1998).
Freytes, D., Stoner, R. M. & Badylak, S. F. Uniaxial and biaxial properties of terminally sterilized porcine urinary bladder matrix scaffolds. J. Biomed. Mater. Res. B. Appl. Biomater. 84, 408–414 (2008).
Freytes, D. O. et al. Analytically derived material properties of multilaminated extracellular matrix devices using the ball-burst test. Biomaterials 26, 5518–5531 (2005).
Jokandan, M. S. et al. Bladder wall biomechanics: a comprehensive study on fresh porcine urinary bladder. J. Mech. Behav. Biomed. Mater. 79, 92–103 (2018).
Fry, C. H. et al. Modeling the urinary tract — computational, physical, and biological methods. Neurourol. Urodyn. 30, 692–699 (2011).
Bastiaanssen, E. H. C., Leeuwen, Van, J. L., Vanderschoot, J. & Redert, P. A. A. Myocybernetic model of the lower urinary tract. J. Theor. Biol. 178, 113–133 (1996).
Jankowski, R. J. et al. Development of an experimental system for the study of urethral biomechanical function. Am. J. Physiol. Ren. Physiol. 286, F225–F232 (2004).
Damaser, M. S. & Lehman, S. L. The effect of urinary bladder shape on its mechanics during filling. J. Biomech. 28, 725–732 (1995).
Damaser, M., Fraser, M., Li, L., Sullivan, M. & Chermansky, C. in ICS 2013 https://www.ics.org/Workshops/HandoutFiles/000332.pdf (Barcelona, 2013).
Korkmaz, I. & Rogg, B. A simple fluid-mechanical model for the prediction of the stress — strain relation of the male urinary bladder. J. Biomech. 40, 663–668 (2007).
Sun, W., Martin, C. & Pham, T. Computational modeling of cardiac valve function and intervention. Annu. Rev. Biomed. Eng. 16, 53–67 (2014).
Samavati, N. et al. Effect of material property heterogeneity on biomechanical modeling of prostate under deformation. Phys. Med. Biol. 60, 195–209 (2015).
Lu, S. H. et al. Biaxial mechanical properties of muscle-derived cell seeded small intestinal submucosa for bladder wall reconstitution. Biomaterials 26, 443–449 (2005).
Bol, M., Schmitz, A., Nowak, G. & Siebert, T. A three-dimensional chemo-mechanical continuum model for smooth muscle contraction. J. Mech. Behav. Biomed. Mater. 13, 215–229 (2012).
Politi, A. Z. et al. A multiscale, spatially-distributed model of asthmatic airway hyper-responsiveness. J. Theor. Biol. 266, 614–624 (2010).
Avolio, A., Jones, D. & Tafazzoli-Shadpour, M. Quantification of alterations in structure and function of elastin in the arterial media. Hypertension 32, 170–175 (1998).
Martin, C. & Sun, W. Fatigue damage of collagenous tissues: experiment, modeling and simulation studies. J. Long. Term. Eff. Med. Implants 25, 55–73 (2015).
Davis, N. F. et al. Cell-seeded extracellular matrices for bladder reconstruction: An ex vivo comparative study of their biomechanical properties. Int. J. Artif. Organs 36, 251–258 (2013).
Yang, B. et al. Development of a porcine bladder acellular matrix with well-preserved extracellular bioactive factors for tissue engineering. Tissue Eng. Part C. Methods 16, 1201–1211 (2010).
Kazbanov, I. V. et al. Effect of global cardiac ischemia on human ventricular fibrillation: insights from a multi-scale mechanistic model of the human heart. PloS Comput. Biol. 10, e1003891 (2014).
Burrowes, K. S. B., C. Lark, A. R. C., Wilsher, M. L. W., Milne, D. G. M. & Tawhai, M. H. T. Hypoxic pulmonary vasoconstriction as a contributor to response in acute pulmonary embolism. Ann. Biomed. Eng. 42, 1631–1643 (2014).
Sutherland, R. S., Baskin, L. S., Hayward, S. W. & Cunha, G. R. Regeneration of bladder urothelium, smooth muscle, blood vessels and nerves into an acellular tissue matrix. J. Urol. 156, 571–577 (1996).
Piechota, H. J. et al. Bladder acellular matrix graft: in vivo functional properties of the regenerated rat bladder. Urol. Res. 27, 206–213 (1999).
Yoo, J. J., Meng, J., Oberpenning, F. & Atala, A. Bladder augmentation using allogenic bladder submucosa seeded with cells. Urology 51, 221–225 (1998).
Caione, P., Capozza, N., Zavaglia, D., Palombaro, G. & Boldrini, R. In vivo bladder regeneration using small intestinal submucosa: experimental study. Pediatr. Surg. Int. 22, 593–599 (2006).
Kropp, B. P. et al. Experimental assessment of small intestinal submucosa as a bladder wall substitute. Urology 46, 396–400 (1995).
Kropp, B. P. et al. Characterization of small intestinal submucosa regenerated canine detrusor: assessment of reinnervation, in vitro compliance and contractility. J. Urol. 156, 599–607 (1996).
Kropp, B. P. et al. Regenerative urinary bladder augmentation using small intestinal submucosa: urodynamic and histopathologic assessment in long-term canine bladder augmentations. J. Urol. 155, 2098–2104 (1996).
Kropp, B. P., Cheng, E. Y., Lin, H.-K. & Zhang, Y. Reliable and reproducible bladder regeneration using unseeded distal small intestinal submucosa. J. Urol. 172, 1710–1713 (2004).
Caione, P., Boldrinic, R., Salerno, A. & Nappo, S. G. Bladder augmentation using acellular collagen biomatrix: a pilot experience in exstrophic patients. Pediatr. Surg. Int. 28, 421–428 (2012).
Zhang, Y. et al. Coculture of bladder urothelial and smooth muscle cells on small intestinal submucosa: potential applications for tissue engineering technology. J. Urol. 164, 928–935 (2000).
Del Gaudio, C. et al. Evaluation of electrospun bioresorbable scaffolds for tissue-engineered urinary bladder augmentation. Biomed. Mater. 8, 45013 (2013).
Tu, D. D. et al. Bladder tissue regeneration using acellular bi-layer silk scaffolds in a large animal model of augmentation cystoplasty. Biomaterials 34, 8681–8689 (2013).
Oberpenning, F., Meng, J., Yoo, J. J. & Atala, A. De novo reconstitution of a functional mammalian urinary bladder by tissue engineering. Nat. Biotechnol. 17, 149–155 (1999).
Zhang, Y., Lin, H.-K., Frimberger, D., Epstein, R. B. & Kropp, B. P. Growth of bone marrow stromal cells on small intestinal submucosa: an alternative cell source for tissue engineered bladder. BJU Int. 96, 1120–1125 (2005).
Brehmer, B., Rohrmann, D., Rau, G. & Jakse, G. Bladder wall replacement by tissue engineering and autologous keratinocytes in minipigs. BJU Int. 97, 829–836 (2006).
Zhang, Y., Frimberger, D., Cheng, E. Y., Lin, H. K. & Kropp, B. P. Challenges in a larger bladder replacement with cell-seeded and unseeded small intestinal submucosa grafts in a subtotal cystectomy model. BJU Int. 98, 1100–1105 (2006).
Rohman, G., Pettit, J. J., Isaure, F., Cameron, N. R. & Southgate, J. Influence of the physical properties of two-dimensional polyester substrates on the growth of normal human urothelial and urinary smooth muscle cells in vitro. Biomaterials 28, 2264–2274 (2007).
Stankus, J. J., Freytes, D. O., Badylak, S. F. & Wagner, W. R. Hybrid nanofibrous scaffolds from electrospinning of a synthetic biodegradable elastomer and urinary bladder matrix. J. Biomater. Sci. Polym. Ed. 19, 635–652 (2008).
Baker, S. C., Rohman, G., Southgate, J. & Cameron, N. R. The relationship between the mechanical properties and cell behaviour on PLGA and PCL scaffolds for bladder tissue engineering. Biomaterials 30, 1321–1328 (2009).
Jack, G. S. et al. Urinary bladder smooth muscle engineered from adipose stem cells and a three dimensional synthetic composite. Biomaterials 30, 3259–3270 (2009).
Engelhardt, E.-M. et al. A collagen-poly(lactic acid-co-ɛ-caprolactone) hybrid scaffold for bladder tissue regeneration. Biomaterials 32, 3969–3976 (2011).
Sharma, A. K. et al. A nonhuman primate model for urinary bladder regeneration using autologous sources of bone marrow-derived mesenchymal stem cells. Stem Cells 29, 241–250 (2011).
Horst, M. et al. A bilayered hybrid micro fibrous PLGA-A cellular matrix scaffold for hollow organ tissue engineering. Biomaterials 34, 1537–1545 (2013).
Kajbafzadeh, A. M. et al. Bladder muscular wall regeneration with autologous adipose mesenchymal stem cells on three-dimensional collagen-based tissue-engineered prepuce and biocompatible nanofibrillar scaffold. J. Pediatr. Urol. 10, 1051–1058 (2014).
Sivaraman, S., Ostendorff, R., Fleishman, B. & Nagatomi, J. Tetronic®-based composite hydrogel scaffolds seeded with rat-bladder smooth muscle cells for urinary bladder tissue engineering applications. J. Biomater. Sci. Polym. Ed. 26, 196–210 (2015).
Horst, M. et al. Increased porosity of electrospun hybrid scaffolds improved bladder tissue regeneration. J. Biomed. Mater. Res. Part A 102, 2116–2124 (2014).
Coutu, D. L., Mahfouz, W., Loutochin, O., Galipeau, J. & Corcos, J. Tissue engineering of rat bladder using marrow-derived mesenchymal stem cells and bladder acellular matrix. PloS ONE 9, e111966 (2014).
Ajalloueian, F., Zeiai, S., Fossum, M. & Hilborn, J. G. Constructs of electrospun PLGA, compressed collagen and minced urothelium for minimally manipulated autologous bladder tissue expansion. Biomaterials 35, 5741–5748 (2014).
Ajalloueian, F., Zeiai, S., Rojas, R., Fossum, M. & Hilborn, J. One-stage tissue engineering of bladder wall patches for an easy-to-use approach at the surgical table. Tissue Eng. Part C Methods 19, 688–696 (2013).
Engelhardt, E. et al. Compressed collagen gel: a novel scaffold for human bladder cells. J. Tissue Eng. Regen. Med. 4, 123–130 (2010).
Lima, S. V., Araújo, L. A., Vilar, F. O., Mota, D. & Maciel, A. Experience with demucosalized ileum for bladder augmentation. BJU Int. 88, 762–764 (2001).
Kelâmi, A. Lyophilized human dura as a bladder wall substitute: experimental and clinical results. J. Urol. 105, 518–522 (1971).
Kambic, H. et al. Biodegradable pericardial implants for bladder augmentation: a 2.5-year study in dogs. J. Urol. 148, 539–543 (1992).
Fishman, I. J., Flores, F. N., Scott, F. B., Spjut, H. J. & Morrow, B. Use of fresh placental membranes for bladder reconstruction. J. Urol. 138, 1291–1294 (1987).
Merguerian, P., Chavez, D. R. & Hakim, S. Grafting of cultured uroepithelium and bladder mucosa into de-epithelialized segments of colon in rabbits. J. Urol. 152, 671–674 (1994).
Cheng, E. Y. & Kropp, B. P. Urologic tissue engineering with small-intestinal submucosa: potential clinical applications. World J. Urol. 18, 26–30 (2000).
Wang, Y. & Liao, L. Histologic and functional outcomes of small intestine submucosa-regenerated bladder tissue. BMC Urol. 14, 69 (2014).
Sievert, K. D. and Tanagho, E. A. Organ-specific acellular matrix for reconstruction of the urinary tract. World J. Urol. 18, 19–25 (2000).
Ashley, R. A. et al. Regional variations in small intestinal submucosa evoke differences in inflammation with subsequent impact on tissue regeneration in the rat bladder augmentation model. BJU Int. 105, 1462–1468 (2010).
Vaught, J. D. et al. Detrusor regeneration in the rat using porcine small intestinal submucosal Grafts: Functional Innervation and receptor expression. J. Urol. 155, 374–378 (1996).
Brown, a. L. et al. 22 Week assessment of bladder acellular matrix as a bladder augmentation material in a porcine model. Biomaterials 23, 2179–2190 (2002).
Schaefer, M., Kaiser, A., Stehr, M. & Beyer, H. J. Bladder augmentation with small intestinal submucosa leads to unsatisfactory long-term results. J. Pediatr. Urol. 9, 878–883 (2013).
Badylak, S. F. & Lantz, G. C., Coffey, A. and Geddes, L. A. Small intestinal submucosa as a large diameter vascular graft in the dog. J. Surg. Res. 47, 74–80 (1989).
Shell, D. H. et al. Comparison of small-intestinal submucosa and expanded polytetrafluoroethylene as a vascular conduit in the presence of gram-positive contamination. Ann. Surg. 241, 995–1004 (2005).
Robotin-Johnson, M. C., Swanson, P. E., Johnson, D. C., Schuessler, R. B. & Cox, J. L. An experimental model of small intestinal submucosa as a growing vascular graft. J. Thorac. Cardiovasc. Surg. 116, 805–811 (1998).
Ledet, E. H. et al. A pilot study to evaluate the effectiveness of small intestinal submucosa used to repair spinal ligaments in the goat. Spine J. 2, 188–196 (2002).
Musahl, V. et al. The use of porcine small intestinal submucosa to enhance the healing of the medial collateral ligament — a functional tissue engineering study in rabbits. J. Orthop. Res. 22, 214–220 (2004).
Liang, R. et al. Induction of c-myc oncoprotein and of cellular proliferation by radiation in normal human urothelial cultures. J. Orthop. Res. 11, 1609–1612 (2006).
Lindberg, K. & Badylak, S. F. Porcine small intestinal submucosa (SIS): a bioscaffold supporting in vitro primary human epidermal cell differentiation and synthesis of basement membrane proteins. Burns 27, 254–266 (2001).
Zhang, F., Zhu, C., Oswald, T., Lei, M.-P. & Lineaweaver, W. C. Porcine small intestinal submucosa as a carrier for skin flap prefabrication. Ann. Plast. Surg. 51, 488–492 (2003).
Colvert, J. R. et al. The use of small intestinal submucosa as an off-the-shelf urethral sling material for pediatric urinary incontinence. J. Urol. 168, 1872–1876 (2002).
Palminteri, E., Berdondini, E., Colombo, F. & Austoni, E. Small intestinal submucosa (SIS) graft urethroplasty: short-term results. Eur. Urol. 51, 1695–1701 (2007).
Roth, C. C. et al. Bladder regeneration in a canine model using hyaluronic acid-poly(lactic-co-glycolic-acid) nanoparticle modified porcine small intestinal submucosa. BJU Int. 108, 148–155 (2011).
Qin, H. H. & Dunn, J. C. Y. Small intestinal submucosa seeded with intestinal smooth muscle cells in a rodent jejunal interposition model. J. Surg. Res. 171, e21–e26 (2011).
Liatsikos, E. N. et al. Ureteral reconstruction: small intestine submucosa for the management of strictures and defects of the upper third of the ureter. J. Urol. 165, 1719–1723 (2001).
Seth, A. et al. The performance of silk scaffolds in a rat model of augmentation cystoplasty. Biomaterials 34, 4758–4765 (2013).
Lakshmanan, Y., Frimberger, D., Gearhart, J. D. & Gearhart, J. P. Human embryoid body-derived stem cells in tissue engineering-enhanced migration in co-culture with bladder smooth muscle and urothelium. Urology 65, 821–826 (2005).
Chung, Y. G. et al. The use of bi-layer silk fibroin scaffolds and small intestinal submucosa matrices to support bladder tissue regeneration in a rat model of spinal cord injury. Biomaterials 35, 7452–7459 (2014).
Feil, G. et al. Investigations of urothelial cells seeded on commercially available small intestine submucosa. Eur. Urol. 50, 1330–1337 (2006).
Lin, H. et al. Understanding roles of porcine small intestinal submucosa in urinary bladder regeneration: identification of variable regenerative characteristics of small intestinal submucosa. Tissue Eng. Part B. Rev. 20, 73–83 (2014).
Brown, R. A., Wiseman, M., Chuo, C.-B., Cheema, U. & Nazhat, S. N. Ultrarapid engineering of biomimetic materials and tissues: fabrication of nano- and microstructures by plastic compression. Adv. Funct. Mater. 15, 1762–1770 (2005).
Meezan, E., Hjelle, J. T., Brendel, K. & Carlson, E. C. A simple, versatile, nondisruptive method for the isolation of morphologically and chemically pure basement membranes from several tissues. Life Sci. 17, 1721–1732 (1975).
Probst, M., Dahiya, R., Carrier, S. & Tanagho, E. A. Reproduction of functional smooth muscle tissue and partial bladder replacement. Br. J. Urol. 79, 505–515 (1997).
Pokrywczynska, M., Gubanska, I., Drewa, G. & Drewa, T. Application of bladder acellular matrix in urinary bladder regeneration: the state of the art and future directions. Biomed. Res. Int. 2015, 613439 (2015).
Boruch, A. V., Nieponice, A., Qureshi, I. R., Gilbert, T. W. & Badylak, S. F. Constructive remodeling of biologic scaffolds is dependent on early exposure to physiologic bladder filling in a canine partial cystectomy model. J. Surg. Res. 161, 217–225 (2010).
Zhao, Y. et al. Time-dependent bladder tissue regeneration using bilayer bladder acellular matrix graft-silk fibroin scaffolds in a rat bladder augmentation model. Acta Biomater. 23, 91–102 (2015).
Mauney, J. R. et al. Evaluation of gel spun silk-based biomaterials in a murine model of bladder augmentation. Biomaterials 32, 808–818 (2011).
Ashkar, L. & Heller, E. The silastic bladder patch. J. Urol. 98, 679–683 (1967).
Bohne, A. W., Osborn, R. W. & Hettle, P. J. Regeneration of the urinary bladder in the dog, following total cystectomy. Surg. Gynecol. Obstet. 100, 259–264 (1955).
Bohne, A. W. & Urwiller, K. L. Experience with urinary bladder regeneration. J. Urol. 77, 725–732 (1957).
Kudish, H. G. The use of polyvinyl sponge for experimental cystoplasty. J. Urol. 78, 232–235 (1957).
Jack, G. S. et al. Processed lipoaspirate cells for tissue engineering of the lower urinary tract: implications for the treatment of stress urinary incontinence and bladder reconstruction. J. Urol. 174, 2041–2045 (2005).
Usas, A. & Huard, J. Muscle-derived stem cells for tissue engineering and regenerative therapy. Biomaterials 28, 5401–5406 (2007).
Duan, B. et al. Degradation of electrospun PLGA-chitosan/PVA membranes and their cytocompatibility in vitro. J. Biomater. Sci. Polym. Ed. 18, 95–115 (2007).
Shukla, D., Box, G. N., Edwards, R. a. & Tyson, D. R. Bone marrow stem cells for urologic tissue engineering. World J. Urol. 26, 341–349 (2008).
Zhao, J. et al. Transdifferentiation of autologous bone marrow cells on a collagen-poly(1-caprolactone) scaffold for tissue engineering in complete lack of native urothelium. J. R. Soc. Interface 11, 20140233 (2014).
Romagnoli, G. et al. Treatment of posterior hypospadias by the autologous graft of cultured urethral epithelium. N. Engl. J. Med. 323, 527–530 (1990).
Purves, J. T. & Gearhart, J. P. Paraexstrophy skin flaps for the primary closure of exstrophy in boys: outmoded or updated? J. Urol. 180, 1675–1679 (2008).
Kuberka, M., von Heimburg, D., Schoof, H., Heschel, I. & Rau, G. Magnification of the pore size in biodegradable collagen sponges. Int. J. Artif. Organs 25, 67–73 (2002).
Goldstein, R. E. & Westropp, J. L. Urodynamic testing in the diagnosis of small animal micturition disorders. Clin. Tech. Small Anim. Pract. 20, 65–72 (2005).
Chung, S. Y. et al. Bladder reconstitution with bone marrow derived stem cells seeded on small intestinal submucosa improves morphological and molecular composition. J. Urol. 174, 353–359 (2005).
Kropp, B. P. et al. Characterization of cultured bladder smooth muscle cells: assessment of in vitro contractility. J. Urol. 162, 1779–1784 (1999).
Galmiche, M. C., Koteliansky, V. E., Brière, J., Hervé, P. & Charbord, P. Stromal cells from human long-term marrow cultures are mesenchymal cells that differentiate following a vascular smooth muscle differentiation pathway. Blood 82, 66–76 (1993).
Ross, J. J. et al. Cytokine-induced differentiation of multipotent adult progenitor cells into functional smooth muscle cells. J. Clin. Invest. 116, 3139–3149 (2006).
Sharma, A. K. et al. Cotransplantation with specific populations of spina bifida bone marrow stem/progenitor cells enhances urinary bladder regeneration. Proc. Natl Acad. Sci. USA 110, 4003–4008 (2013).
Bury, M. I., Fuller, N. J., Wethekam, L. & Sharma, A. K. Bone marrow derived cells facilitate urinary bladder regeneration by attenuating tissue inflammatory responses. Cent. Eur. J. Urol. 68, 115–120 (2015).
Tian, H. et al. Myogenic differentiation of human bone marrow mesenchymal stem cells on a 3D nano fibrous scaffold for bladder tissue engineering. Biomaterials 31, 870–877 (2010).
Tian, H. et al. Differentiation of human bone marrow mesenchymal stem cells into bladder cells: potential for urological tissue engineering. Tissue Eng. Part A 16, 1769–1779 (2010).
Leite, M. T. C. et al. The use of mesenchymal stem cells in bladder augmentation. Pediatr. Surg. Int. 30, 361–370 (2014).
Flieger, A., Golka, K., Schulze, H. & Follmann, W. Primary cultures of human urothelial cells for genotoxicity testing. J. Toxicol. Environ. Health. A 71, 930–935 (2008).
Chamley-Campbell, J., Campbell, G. R. & Ross, G. The smooth muscle cell in culture. Physiol. Rev. 59, 1–61 (1979).
Bolin, S. R., Matthews, P. J. & Ridpath, J. F. Methods for detection and frequency of contamination of fetal calf serum with bovine viral diarrhea virus and antibodies against bovine viral diarrhea virus. J. Vet. Diagn. Invest. 3, 199–203 (1991).
Lovett, M. L., Cannizzaro, C. M., Vunjak-Novakovic, G. & Kaplan, D. L. Gel spinning of silk tubes for tissue engineering. Biomaterials 29, 4650–4657 (2008).
Wang, Y., Kim, H.-J., Vunjak-Novakovic, G. & Kaplan, D. L. Stem cell-based tissue engineering with silk biomaterials. Biomaterials 27, 6064–6082 (2006).
Altman, G. H. et al. Silk-based biomaterials. Biomaterials 24, 401–416 (2003).
Paterson, R. F. et al. Multilayered small intestinal submucosa is inferior to autologous bowel for laparoscopic bladder augmentation. J. Urol. 168, 2253–2257 (2002).
Bury, M. I. et al. The promotion of functional urinary bladder regeneration using anti-inflammatory nanofibers. Biomaterials 35, 9311–9321 (2014).
Pokrywczynska, M. et al. Is the poly (L-lactide-co-caprolactone) nanofibrous membrane suitable for urinary bladder regeneration? PloS ONE 9, e105295 (2014).
Kanematsu, A. et al. Collagenous matrices as release carriers of exogenous growth factors. Biomaterials 25, 4513–4520 (2004).
Farhat, W. a et al. Porcine bladder acellular matrix (ACM): protein expression, mechanical properties. Biomed. Mater. 3, 25015 (2008).
Huang, J. et al. Tissue performance of bladder following stretched electrospun silk fibroin matrix and bladder acellular matrix implantation in a rabbit model. J. Biomed. Mater. Res. Part A 104, 9–16 (2016).
Jayo, M. J., Jain, D., Wagner, B. J. & Bertram, T. A. Early cellular and stromal responses in regeneration versus repair of a mammalian bladder using autologous cell and biodegradable scaffold technologies. J. Urol. 180, 392–397 (2008).
Gomez, P. et al. The effect of manipulation of silk scaffold fabrication parameters on matrix performance in a murine model of bladder augmentation. Biomaterials 32, 7562–7570 (2011).
Dorsher, P. T. & McIntosh, P. M. Neurogenic bladder. Adv. Urol. 2012, 816274 (2012).
Yao, C. et al. Nanostructured polyurethane-poly-lactic-co-glycolic acid scaffolds increase bladder tissue regeneration: an in vivo study. Int. J. Nanomed. 8, 3285–3296 (2013).
Tiemessen, D. et al. The effect of a cyclic uniaxial strain on urinary bladder cells. World J. Urol. 35, 1531–1539 (2017).
Acknowledgements
This work was supported by grants from the Danish Research Council Foundation (Individual Postdoctoral Grant DFF-4093-00282A and Sapere Aude: DFF-Research Talent 4217-00048A), the Freemason Foundation for Children's Welfare, the Stockholm City Council, and the Swedish Society of Medicine.
Author information
Authors and Affiliations
Contributions
F.A., J.H., I.S.C., and M.F. made substantial contributions to the discussion of content. F.A. and G.L. researched data for the article and wrote the manuscript. All authors reviewed and edited the article before submission.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Glossary
- Load-history-dependent behaviour
-
A characteristic observed in biological soft tissues owing to viscoelasticity. The response of such materials to loading and unloading depends on how quickly the load is applied or removed. This can be considered as time-dependent material behaviour as well.
- Hysteresis
-
The phenomenon in which a body subjected to cyclic loading–unloading exhibits different stress–strain relationships during loading and unloading procedures. The area enclosed by the loading and unloading curve is called the hysteresis loop, which represents the energy dissipated during the deformation and recovery phases.
- Stress relaxation
-
The phenomenon in which a sample is suddenly strained and maintained at a final strain, and its stress gradually decreases with time.
- Creep
-
The phenomenon in which a sample is suddenly stressed, and the load is held for some time. If the sample continues to deform, it is said to be exhibiting creep.
- Viscoelasticity
-
A property of materials that exhibit both viscous and elastic characteristics when experiencing deformation.
- Cystometry
-
The clinical diagnostic procedure that is used to evaluate bladder function and pressure during filling and voiding.
- Cystogram
-
The resulting chart from cystometry. The intravesical volume is plotted against the intravesical pressure, where urinary leakage and patient sensation are also recorded.
- Plastoelasticity
-
A property of materials that exhibit both elastic recovery and plastic (residual) deformation
- Anisotropy
-
A term used in various scientific disciplines to indicate that the material properties vary with the direction from which they are measured.
- Areal strain
-
The 2D change in area caused by deformation.
- Lattice contractility assay164
-
An assay in which different cell types are mixed with the soluble stabilized type I collagen to create a cell-collagen solution. The solution is placed onto a tissue culture plate, maintained for a predefined duration, and mechanically released from the underlying plastic. The relative change in diameter of cell-collagen lattices is calculated by dividing the lattice diameters at 10 min after release by the initial diameters.
Rights and permissions
About this article
Cite this article
Ajalloueian, F., Lemon, G., Hilborn, J. et al. Bladder biomechanics and the use of scaffolds for regenerative medicine in the urinary bladder. Nat Rev Urol 15, 155–174 (2018). https://doi.org/10.1038/nrurol.2018.5
Published:
Issue Date:
DOI: https://doi.org/10.1038/nrurol.2018.5