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Research Papers

Effects of Elastase Digestion on the Murine Vaginal Wall Biaxial Mechanical Response

[+] Author and Article Information
Akinjide R. Akintunde

Department of Biomedical Engineering,
Lindy Boggs Center Suite 500,
Tulane University,
New Orleans, LA 70118
e-mail: aakintun@tulane.edu

Kathryn M. Robison

Mem. ASME
Department of Biomedical Engineering,
Lindy Boggs Center Suite 500,
Tulane University,
New Orleans, LA 70118
e-mail: krobison@tulane.edu

Daniel J. Capone

Department of Biomedical Engineering,
Lindy Boggs Center Suite 500,
Tulane University,
New Orleans, LA 70118
e-mail: dcapone@tulane.edu

Laurephile Desrosiers

Department of Female Pelvic Medicine
and Reconstructive Surgery,
UQ Ochsner Clinical School,
1514 Jefferson Highway,
New Orleans, LA 70121
e-mail: laurephile.desrosiers@ochsner.org

Leise R. Knoepp

Department of Female Pelvic Medicine
and Reconstructive Surgery,
UQ Ochsner Clinical School,
1514 Jefferson Highway,
New Orleans, LA 70121
e-mail: lknoepp@ochsner.org

Kristin S. Miller

Mem. ASME
Department of Biomedical Engineering,
Lindy Boggs Center Suite 500,
Tulane University,
New Orleans, LA 70118
e-mail: kmille11@tulane.edu

1Corresponding author.

Manuscript received April 10, 2018; final manuscript received October 31, 2018; published online December 12, 2018. Assoc. Editor: Thao (Vicky) Nguyen.

J Biomech Eng 141(2), 021011 (Dec 12, 2018) (11 pages) Paper No: BIO-18-1172; doi: 10.1115/1.4042014 History: Received April 10, 2018; Revised October 31, 2018

Although the underlying mechanisms of pelvic organ prolapse (POP) remain unknown, disruption of elastic fiber metabolism within the vaginal wall extracellular matrix (ECM) has been highly implicated. It has been hypothesized that elastic fiber fragmentation correlates to decreased structural integrity and increased risk of prolapse; however, the mechanisms by which elastic fiber damage may contribute to prolapse are poorly understood. Furthermore, the role of elastic fibers in normal vaginal wall mechanics has not been fully ascertained. Therefore, the objective of this study is to investigate the contribution of elastic fibers to murine vaginal wall mechanics. Vaginal tissue from C57BL/6 female mice was mechanically tested using biaxial extension–inflation protocols before and after intraluminal exposure to elastase. Elastase digestion induced marked changes in the vaginal geometry, and biaxial mechanical properties, suggesting that elastic fibers may play an important role in vaginal wall mechanical function. Additionally, a constitutive model that considered two diagonal families of collagen fibers with a slight preference toward the circumferential direction described the data reasonably well before and after digestion. The present findings may be important to determine the underlying structural and mechanical mechanisms of POP, and aid in the development of growth and remodeling models for improved assessment and prediction of changes in structure–function relationships with prolapse development.

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References

DeLancey, J. O. , 2005, “ The Hidden Epidemic of Pelvic Floor Dysfunction: Achievable Goals for Improved Prevention and Treatment,” Am. J. Obstet. Gynecol., 192(5), pp. 1488–1495. [CrossRef] [PubMed]
Subak, L. L. , Waetjen, L. E. , van den Eeden, S. , Thom, D. H. , Vittinghoff, E. , and Brown, J. S. , 2001, “ Cost of Pelvic Organ Prolapse Surgery in the United States,” Obstet. Gynecol., 98(4), pp. 646–651. [PubMed]
Pizarro-Berdichevsky, J. , Clifton, M. M. , and Goldman, H. B. , 2015, “ Evaluation and Management of Pelvic Organ Prolapse in Elderly Women,” Clin. Geriatr. Med., 31(4), pp. 507–521. [CrossRef] [PubMed]
Baah-Dwomoh, A. , McGuire, J. , Tan, T. , and De Vita, R. , 2016, “ Mechanical Properties of Female Reproductive Organs and Supporting Connective Tissues: A Review of the Current State of Knowledge,” ASME Appl. Mech. Rev., 68(6), p. 060801. [CrossRef]
Abramowitch, S. D. , Feola, A. , Jallah, Z. , and Moalli, P. A. , 2009, “ Tissue Mechanics, Animal Models, and Pelvic Organ Prolapse: A Review,” Eur. J. Obstetr. Gynecol., 144, pp. S146–S158. [CrossRef]
Alperin, A. M. , and Moalli, A. P. , 2006, “ Remodeling of Vaginal Connective Tissue in Patients With Prolapse,” Curr. Opin. Obstetr. Gynecol., 18(5), pp. 544–550. [CrossRef]
Kerkhof, M. H. , Hendriks, L. , and Brölmann, H. A. , 2009, “ Changes in Connective Tissue in Patients With Pelvic Organ Prolapse—A Review of the Current Literature,” Int. Urogynecol. J. Pelvic. Floor Dysfunct., 20(4), pp. 461–474. [CrossRef] [PubMed]
Skoczylas, L. C. , Jallah, Z. , Sugino, Y. , Stein, S. E. , Feola, A. , Yoshimura, N. , and Moalli, P. , 2013, “ Regional Differences in Rat Vaginal Smooth Muscle Contractility and Morphology,” Reprod. Sci., 20(4), pp. 382–390. [CrossRef] [PubMed]
Ferruzzi, J. , Collins, M. J. , Yeh, A. T. , and Humphrey, J. D. , 2011, “ Mechanical Assessment of Elastin Integrity in Fibrillin-1-Deficient Carotid Arteries: Implications for Marfan Syndrome,” Cardiovasc. Res., 92(2), pp. 287–295. [CrossRef] [PubMed]
Fonck, E. , Prod'hom, G. , Roy, S. , Augsburger, L. , Rüfenacht, D. A. , and Stergiopulos, N. , 2007, “ Effect of Elastin Degradation on Carotid Wall Mechanics as Assessed by a Constituent-Based Biomechanical Model,” Am. J. Physiol. Heart Circ. Physiol., 292(6), pp. H2754–H2763. [CrossRef] [PubMed]
Henninger, H. B. , Underwood, C. J. , Romney, S. J. , Davis, G. L. , and Weiss, J. A. , 2013, “ Effect of Elastin Digestion on the Quasi‐Static Tensile Response of Medial Collateral Ligament,” J. Orthop. Res., 31(8), pp. 1226–1233. [CrossRef] [PubMed]
DeLancey, J. O. , and Starr, R. A. , 1990, “ Histology of the Connection Between the Vagina and Levator Ani Muscles. Implications for Urinary Tract Function,” J. Reprod. Med., 35(8), pp. 765–771. https://www.ncbi.nlm.nih.gov/pubmed/2213737 [PubMed]
Tracy, P. V. , DeLancey, J. O. , and Ashton-Miller, J. A. , 2016, “ A Geometric Capacity-Demand Analysis of Maternal Levator Muscle Stretch Required for Vaginal Delivery,” ASME J. Biomech. Eng., 138(2), p. 021001. [CrossRef]
DeLancey, J. O. , Morgan, D. M. , Fenner, D. E. , Kearney, R. , Guire, K. , Miller, J. M. , Hussain, H. , Umek, W. , Hsu, Y. , and Ashton-Miller, J. A. , 2007, “ Comparison of Levator Ani Muscle Defects and Function in Women With and Without Pelvic Organ Prolapse,” Obstet. Gynecol., 109(2), pp. 295–302. [CrossRef] [PubMed]
Miklos, J. R. , Moore, R. D. , and Kohli, N. , 2002, “ Laparoscopic Surgery for Pelvic Support Defects,” Curr. Opin. Obstetr. Gynecol., 14(4), pp. 387–395. [CrossRef]
DeLancey, J. , 1992, “ Anatomic Aspects of Vaginal Eversion After Hysterectomy,” Am. J. Obstetr. Gynecol., 166(6), pp. 1717–1724. [CrossRef]
Becker, W. R. , and De Vita, R. , 2015, “ Biaxial Mechanical Properties of Swine Uterosacral and Cardinal Ligaments,” Biomech. Model. Mechanobiol., 14(3), pp. 549–560. [CrossRef] [PubMed]
Tan, T. , Cholewa, N. , Case, S. , and De Vita, R. , 2016, “ Micro-Structural and Biaxial Creep Properties of the Swine Uterosacral–Cardinal Ligament Complex,” J. Biomed. Eng. Soc., 44(11), pp. 3225–3237. https://link.springer.com/article/10.1007%2Fs10439-016-1661-z
Baah-Dwomoh, A. , and De Vita, R. , 2017, “ Effects of Repeated Biaxial Loads on the Creep Properties of Cardinal Ligaments,” J. Mech. Behav. Biomed. Mater., 74, pp. 128–141. [CrossRef] [PubMed]
Rivaux, G. , Rubod, C. , Dedet, B. , Brieu, M. , Gabriel, B. , De Landscheere, L. , Devos, P. , Delmas, V. , and Cosson, M. , 2011, “ Biomechanical Characterisation of Uterine Ligaments. Implications for the Pelvic Floor,” Pelvi-Perineologie, 6(2), pp. 67–74. [CrossRef]
Rivaux, G. , Rubod, C. , Dedet, B. , Brieu, M. , Gabriel, B. , and Cosson, M. , 2013, “ Comparative Analysis of Pelvic Ligaments: A Biomechanics Study,” Int. Urogynecol. J., 24(1), pp. 135–139. [CrossRef] [PubMed]
Rubod, C. , Brieu, M. , Cosson, M. , Rivaux, G. , Clay, J.-C. , de Landsheere, L. , and Gabriel, B. , 2012, “ Biomechanical Properties of Human Pelvic Organs,” Urology, 79(4), pp. 968.e917–968.e922. [CrossRef]
Kerkhof, M. H. , Ruiz-Zapata, A. M. , Bril, H. , Bleeker, M. C. , Belien, J. A. , Stoop, R. , and Helder, M. N. , 2014, “ Changes in Tissue Composition of the Vaginal Wall of Premenopausal Women With Prolapse,” Am. J. Obstet. Gynecol., 210(2), pp. 168.e161–168.e169. [CrossRef]
Drewes, P. G. , Yanagisawa, H. , Starcher, B. , Hornstra, I. , Csiszar, K. , Marinis, S. I. , Keller, P. , and Word, R. A. , 2007, “ Pelvic Organ Prolapse in Fibulin-5 Knockout Mice—Pregnancy-Induced Changes in Elastic Fiber Homeostasis in Mouse Vagina,” Am. J. Pathol., 170(2), pp. 578–589. [CrossRef] [PubMed]
Rahn, D. D. , Ruff, M. D. , Brown, S. A. , Tibbals, H. F. , and Word, R. A. , 2008, “ Biomechanical Properties of the Vaginal Wall: Effect of Pregnancy, Elastic Fiber Deficiency, and Pelvic Organ Prolapse,” Am. J. Obstet. Gynecol., 198(5), pp. 590.e591–590.e596. [CrossRef]
Rahn, D. D. , Acevedo, J. F. , and Word, R. A. , 2008, “ Effect of Vaginal Distention on Elastic Fiber Synthesis and Matrix Degradation in the Vaginal Wall: Potential Role in the Pathogenesis of Pelvic Organ Prolapse,” Am. J. Physiol. Regul. Integr. Comp. Physiol., 295(4), pp. R1351–R1358. [CrossRef] [PubMed]
Downing, K. T. , Billah, M. , Raparia, E. , Shah, A. , Silverstein, M. C. , Ahmad, A. , and Boutis, G. S. , 2014, “ The Role of Mode of Delivery on Elastic Fiber Architecture and Vaginal Vault Elasticity: A Rodent Model Study,” J. Mech. Behav. Biomed. Mater., 29, pp. 190–198. [CrossRef] [PubMed]
Chen, B. , Wen, Y. , and Polan, M. L. , 2004, “ Elastolytic Activity in Women With Stress Urinary Incontinence and Pelvic Organ Prolapse,” Neurourol. Urodynam., 23(2), pp. 119–126. [CrossRef]
Liu, X. , Zhao, Y. , Pawlyk, B. , Damaser, M. , and Li, T. , 2006, “ Failure of Elastic Fiber Homeostasis Leads to Pelvic Floor Disorders,” Am. J. Pathol., 168(2), pp. 519–528. [CrossRef] [PubMed]
Wieslander, C. K. , Marinis, S. I. , Drewes, P. G. , Keller, P. W. , Acevedo, J. F. , and Word, R. A. , 2008, “ Regulation of Elastolytic Proteases in the Mouse Vagina During Pregnancy, Parturition, and Puerperium,” Biol. Reprod., 78(3), pp. 521–528. [CrossRef] [PubMed]
Rahn, D. , Acevedo, J. , Roshanravan, S. , Keller, P. , Davis, E. , Marmorstein, L. , and Word, R. , 2009, “ Failure of Pelvic Organ Support in Mice Deficient in Fibulin-3,” Am. J. Pathol., 174(1), pp. 206–215. [CrossRef] [PubMed]
Moalli, P. A. , Shand, S. H. , Zyczynski, H. M. , Gordy, S. C. , and Meyn, L. A. , 2005, “ Remodeling of Vaginal Connective Tissue in Patients With Prolapse,” Obstet. Gynecol., 106(5), pp. 953–963. [CrossRef] [PubMed]
Budatha, M. , Roshanravan, S. , Zheng, Q. , Weislander, C. , Chapman, S. L. , Davis, E. C. , Starcher, B. , Word, R. A. , and Yanagisawa, H. , 2011, “ Extracellular Matrix Proteases Contribute to Progression of Pelvic Organ Prolapse in Mice and Humans,” J. Clin. Invest., 121(5), pp. 2048–2059. [CrossRef] [PubMed]
Gosline, J. , Lillie, M. , Carrington, E. , Guerette, P. , Ortlepp, C. , and Savage, K. , 2002, “ Elastic Proteins: Biological Roles and Mechanical Properties,” Philos. Trans.: Biol. Sci., 357(1418), pp. 121–132. [CrossRef]
De Landsheere, L. , Munaut, C. , Nusgens, B. , Maillard, C. , Rubod, C. , Nisolle, M. , Cosson, M. , and Foidart, J. , 2013, “ Histology of the Vaginal Wall in Women With Pelvic Organ Prolapse: A Literature Review,” Int. Urogynecol. J., (12), pp. 2011–2020.
Oxlund, H. , Manschot, J. , and Viidik, A. , 1988, “ The Role of Elastin in the Mechanical Properties of Skin,” J. Biomech., 21(3), pp. 213–218. [CrossRef] [PubMed]
Wagenseil, J. , and Mecham, R. , 2012, “ Elastin in Large Artery Stiffness and Hypertension,” J. Cardiovasc. Transl. Res., 5(3), pp. 264–273. [CrossRef] [PubMed]
Starcher, B. C. , 1986, “ Elastin and the Lung,” Thorax, 41(8), pp. 577–585. [CrossRef] [PubMed]
Peter, D. Y. , Robert, P. M. , and David, E. B. , 1994, Extracellular Matrix Assembly and Structure, Elsevier Science, Cambridge, MA.
Mecham, R. P. , 2018, “ Elastin in Lung Development and Disease Pathogenesis,” Matrix Biol., 73, pp. 6–20. [CrossRef] [PubMed]
Frances, C. , and Robert, L. , 1984, “ Elastin and Elastic Fibers in Normal and Pathologic Skin,” Int. J. Dermatol., 23(3), pp. 166–179. [CrossRef] [PubMed]
Echenne, P. B. , Barneon, G. G. , Pages, G. M. , Caillens, G. J. , Guibal, G. C. , Jarrousse, G. Y. , Dimeglio, G. A. , and Pous, G. J. , 1988, “ Skin Elastic Fiber Pathology and Idiopathic Scoliosis,” J. Pediatr. Orthop., 8(5), pp. 522–528. [CrossRef] [PubMed]
Leppert, P. C. , Yu, S. Y. , Keller, S. , Cerreta, J. , and Mandl, I. , 1987, “ Decreased Elastic Fibers and Desmosine Content in Incompetent Cervix,” Am. J. Obstetr. Gynecol., 157(5), pp. 1134–1139. [CrossRef]
Jayyosi, C. , Lee, N. , Willcockson, A. , Nallasamy, S. , Mahendroo, M. , and Myers, K. , 2018, “ The Mechanical Response of the Mouse Cervix to Tensile Cyclic Loading in Term and Preterm Pregnancy,” Acta Biomater., 78, pp. 308–319. [CrossRef] [PubMed]
Nallasamy, S. , Yoshida, K. , Akins, M. , Myers, K. , Iozzo, R. , and Mahendroo, M. , 2017, “ Steroid Hormones are Key Modulators of Tissue Mechanical Function Via Regulation of Collagen and Elastic Fibers,” Endocrinology, 158(4), pp. 950–962. [CrossRef] [PubMed]
Grant, T. M. , Yapp, C. , Chen, Q. , Czernuszka, J. T. , and Thompson, M. S. , 2015, “ The Mechanical, Structural, and Compositional Changes of Tendon Exposed to Elastase,” Ann. Biomed. Eng., 43(10), pp. 2477–2486. [CrossRef] [PubMed]
Henninger, H. B. , Valdez, W. R. , Scott, S. A. , and Weiss, J. A. , 2015, “ Elastin Governs the Mechanical Response of Medial Collateral Ligament Under Shear and Transverse Tensile Loading,” Acta Biomater., 25, pp. 304–312. [CrossRef] [PubMed]
Yuan, H. , Kononov, S. , Cavalcante, F. , and Lutchen, K. , 2000, “ Effects of Collagenase and Elastase on the Mechanical Properties of Lung Tissue Strips,” J. Appl. Physiol., 89(1), pp. 3–14. [CrossRef] [PubMed]
Jesudason, R. , Black, L. , Majumdar, A. , Stone, P. , and Suki, B. , 2007, “ Differential Effects of Static and Cyclic Stretching During Elastase Digestion on the Mechanical Properties of Extracellular Matrices,” J. Appl. Physiol., 103(3), pp. 803–811. [CrossRef] [PubMed]
López-Aguilar, J. , and Romero, P. V. , 1998, “ Effect of Elastase Pretreatment on Rat Lung Strip Induced Constriction,” Respir. Physiol., 113(3), pp. 239–246. [CrossRef] [PubMed]
Moretto, A. , Dallaire, M. , Romero, P. , and Ludwig, M. , 1994, “ Effect of Elastase on Oscillation Mechanics of Lung Parenchymal Strips,” J. Appl. Physiol., 77(4), pp. 1623–1629. [CrossRef] [PubMed]
Barbir, A. , Michalek, A. J. , Abbott, R. D. , and Iatridis, J. C. , 2010, “ Effects of Enzymatic Digestion on Compressive Properties of Rat Intervertebral Discs,” J. Biomech., 43(6), pp. 1067–1073. [CrossRef] [PubMed]
Fan, Y. , Zhao, J. , Liao, D. , and Gregersen, H. , 2005, “ The Effect of Digestion of Collagen and Elastin on Histomorphometry and the Zero-Stress State in Rat Esophagus,” Dig. Dis. Sci., 50(8), pp. 1497–1505. [CrossRef] [PubMed]
Collins, M. , Eberth, J. , Wilson, E. , and Humphrey, J. , 2012, “ Acute Mechanical Effects of Elastase on the Infrarenal Mouse Aorta: Implications for Models of Aneurysms,” J. Biomech., 45(4), pp. 660–665. [CrossRef] [PubMed]
Gundiah, N. , Babu, A. R. , and Pruitt, L. A. , 2013, “ Effects of Elastase and Collagenase on the Nonlinearity and Anisotropy of Porcine Aorta,” Physiol. Meas., 34(12), pp. 1657–1673. [CrossRef] [PubMed]
Bloksgaard, M. , Leurgans, T. M. , Spronek, B. , Heusinkveld, M. H. G. , Thorsted, B. , Rosenstand, K. , Nissen, I. , Hansen, U. M. , Brewer, J. R. , Bagatolli, L. A. , Rasniussen, L. M. , Irmukhamedov, A. , Reesink, K. D. , and De Mey, J. G. R. , 2017, “ Imaging and Modeling of Acute Pressure-Induced Changes of Collagen and Elastin Microarchitectures in Pig and Human Resistance Arteries,” Am. J. Physiol., 313(1), pp. H164–H178.
Zeinali-Davarani, S. , Chow, M.-J. , Turcotte, R. , and Zhang, Y. , 2013, “ Characterization of Biaxial Mechanical Behavior of Porcine Aorta Under Gradual Elastin Degradation,” J. Biomed. Eng. Soc., 41(7), pp. 1528–1538.
Humphrey, J. , Kang, T. , Sakarda, P. , and Anjanappa, M. , 1993, “ Computer-Aided Vascular Experimentation: A New Electromechanical Test System,” Ann. Biomed. Eng., 21(1), pp. 33–43. [CrossRef] [PubMed]
Macrae, R. A. , Miller, K. , and Doyle, B. J. , 2016, “ Methods in Mechanical Testing of Arterial Tissue: A Review,” Strain, 52(5), pp. 380–399. [CrossRef]
Rubod, C. , Boukerrou, M. , Brieu, M. , Dubois, P. , and Cosson, M. , 2007, “ Biomechanical Properties of Vaginal Tissue. Part 1: New Experimental Protocol,” J. Urol., 178(1), pp. 320–325. [CrossRef] [PubMed]
Amin, M. , Le, V. P. , and Wagenseil, J. E. , 2012, “ Mechanical Testing of Mouse Carotid Arteries: From Newborn to Adult,” J. Vis. Exp., (60), p. 3733.
Robison, K. M. , Conway, C. K. , Desrosiers, L. , Knoepp, L. R. , and Miller, K. S. , 2017, “ Biaxial Mechanical Assessment of the Murine Vaginal Wall Using Extension-Inflation Testing,” ASME J. Biomech. Eng., 139(10), p. 104504. [CrossRef]
Ferruzzi, J. , Bersi, M. , and Humphrey, J. , 2013, “ Biomechanical Phenotyping of Central Arteries in Health and Disease: Advantages of and Methods for Murine Models,” Ann. Biomed. Eng., 41(7), pp. 1311–1330. [CrossRef] [PubMed]
Cox, R. H. , 1974, “ Three-Dimensional Mechanics of Arterial Segments In Vitro: Methods,” J. Appl. Physiol., 36(3), pp. 381–384. [CrossRef] [PubMed]
Van Loon, P. , 1977, “ Length-Force and Volume-Pressure Relationships of Arteries,” Biorheology, 14(4), pp. 181–201. [CrossRef] [PubMed]
Humphrey, J. D. , 2002, Cardiovascular Solid Mechanics: Cells, Tissues, and Organs, Springer Science & Business Media, New York.
Le, V. , Yamashiro, Y. , Yanagisawa, H. , and Wagenseil, J. , 2014, “ Measuring, Reversing, and Modeling the Mechanical Changes Due to the Absence of Fibulin-4 in Mouse Arteries,” Biomech. Model. Mechanobiol., 13(5), pp. 1081–1095. [CrossRef] [PubMed]
Bersi, M. R. , Collins, M. J. , Wilson, E. , and Humphrey, J. D. , 2013, “ Disparate Changes in the Mechanical Properties of Murine Carotid Arteries and Aorta in Response to Chronic Infusion of Angiotensin-II,” Int. J. Adv. Eng. Sci. Appl. Math., 4(4), pp. 228–240. [CrossRef] [PubMed]
Holzapfel, G. A. , Gasser, T. C. , and Ogden, R. W. , 2000, “ A New Constitutive Framework for Arterial Wall Mechanics and a Comparative Study of Material Models,” J. Elasticity Phys. Sci. Solids, 61(1/3), pp. 1–48. [CrossRef]
Holzapfel, G. A. , and Ogden, R. W. , 2010, “ Constitutive Modelling of Arteries,” Proc. R. Soc. A: Math., Phys. Eng. Sci., 466(2118), pp. 1551–1597. [CrossRef]
Ni Annaidh, A. , Bruyere, K. , Destrade, M. , Gilchrist, M. D. , Maurini, C. , Ottenio, M. , and Saccomandi, G. , 2012, “ Automated Estimation of Collagen Fibre Dispersion in the Dermis and Its Contribution to the Anisotropic Behaviour of Skin,” Ann. Biomed. Eng., 40(8), pp. 1666–1678. [CrossRef] [PubMed]
Ogden, R. W. , 2003, “ Nonlinear Elasticity, Anisotropy, Material Stability and Residual Stresses in Soft Tissue,” Biomechanics of Soft Tissue in Cardiovascular Systems, G. A. Holzapfel and R. W. Ogden , eds., Springer, Vienna, Austria, pp. 65–108.
Gleason, R. L. , Dye, W. W. , Wilson, E. , and Humphrey, J. D. , 2008, “ Quantification of the Mechanical Behavior of Carotid Arteries From Wild-Type, Dystrophin-Deficient, and Sarcoglycan-Delta Knockout Mice,” J. Biomech., 41(15), pp. 3213–3218. [CrossRef] [PubMed]
Rynkevic, R. , Martins, P. , Hympanova, L. , Almeida, H. , Fernandes, A. A. , and Deprest, J. , 2017, “ Biomechanical and Morphological Properties of the Multiparous Ovine Vagina and Effect of Subsequent Pregnancy,” J. Biomech., 57, pp. 94–102. [CrossRef] [PubMed]
Storn, R. , and Price, K. , 1997, “ Differential Evolution—A Simple and Efficient Heuristic for Global Optimization Over Continuous Spaces,” J. Global Optim., 11(4), pp. 341–359. [CrossRef]
Price, K. V. , 2005, “ Differential Evolution a Practical Approach to Global Optimization,” Global Optimization, R. M. Storn and J. A. Lampinen , eds., Springer, Berlin.
Akintunde, A. , and Miller, K. , 2018, “ Evaluation of Microstructurally Motivated Constitutive Models to Describe Age-Dependent Tendon Healing,” Biomech. Model. Mechanobiol., 17(3), pp. 793–814. [CrossRef] [PubMed]
Schneider, C. A. , Rasband, W. S. , and Eliceiri, K. W. , 2012, “ NIH Image to ImageJ: 25 Years of Image Analysis,” Nat. Methods, 9(7), pp. 671–675. [CrossRef] [PubMed]
Udelsman, B. V. , Khosravi, R. , Miller, K. S. , Dean, E. W. , Bersi, M. R. , Rocco, K. , Yi, T. , Humphrey, J. D. , and Breuer, C. K. , 2014, “ Characterization of Evolving Biomechanical Properties of Tissue Engineered Vascular Grafts in the Arterial Circulation,” J. Biomech., 47(9), pp. 2070–2079. [CrossRef] [PubMed]
Ruifrok, A. C. , and Johnston, D. A. , 2001, “ Quantification of Histochemical Staining by Color Deconvolution,” Anal. Quant. Cytol. Histol., 23(4), pp. 291–299. https://www.ncbi.nlm.nih.gov/pubmed/11531144 [PubMed]
Team, R. C. , 2016, R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria.
Dobrin, P. B. , Baker, W. H. , and Gley, W. C. , 1984, “ Elastolytic and Collagenolytic Studies of Arteries. Implications for the Mechanical Properties of Aneurysms,” Arch. Surg., 119(4), pp. 405–409. [CrossRef] [PubMed]
Karlinsky, J. B. , Catanese, A. , Honeychurch, C. , Sherter, C. B. , Hoppin, F. G. , and Snider, G. L. , 1976, “ In Vitro Effects of Elastase and Collagenase on Mechanical Properties of Hamster Lungs,” Chest, 69(2 Suppl.), pp. 275–276. [CrossRef] [PubMed]
Cardamone, L. , Valentin, A. , Eberth, J. , and Humphrey, J. , 2009, “ Origin of Axial Prestretch and Residual Stress in Arteries,” Biomech. Model. Mechanobiol., 8(6), pp. 431–446. [CrossRef] [PubMed]
Lee, T. C. , Midura, R. J. , Hascall, V. C. , and Vesely, I. , 2001, “ The Effect of Elastin Damage on the Mechanics of the Aortic Valve,” J. Biomech., 34(2), pp. 203–210. [CrossRef] [PubMed]
Miskolczi, L. , Guterman, L. R. , Flaherty, J. D. , Szikora, I. , and Hopkins, L. N. , 1997, “ Rapid Saccular Aneurysm Induction by Elastase Application In Vitro,” Neurosurgery, 41(1), pp. 220–228. [CrossRef] [PubMed]
Greenwald, S. E. , Moore , J. E., Jr., Rachev , A. , Kane, T. P. C. , and Meister, J. J. , 1997, “ Experimental Investigation of the Distribution of Residual Strains in the Artery Wall,” ASME J. Biomech. Eng., 119(4), pp. 438–444. [CrossRef]
Smith, L. , Byers, S. , Costi, J. , and Fazzalari, N. , 2008, “ Elastic Fibers Enhance the Mechanical Integrity of the Human Lumbar Anulus Fibrosus in the Radial Direction,” J. Biomed. Eng. Soc., 36(2), pp. 214–223.
Fang, F. , and Lake, S. P. , 2016, “ Multiscale Mechanical Integrity of Human Supraspinatus Tendon in Shear After Elastin Depletion,” J. Mech. Behav. Biomed. Mater., 63, pp. 443–455. [CrossRef] [PubMed]
Woessner, J. , 1963, “ Formation and Breakdown of Collagen and Elastin in the Human Uterus During Pregnancy and Post-Partum Involution,” Biochem. J., 89(1), pp. 75–82. [CrossRef] [PubMed]
Liang, R. , Abramowitch, S. , Knight, K. , Palcsey, S. , Nolfi, A. , Feola, A. , Stein, S. , and Moalli, P. A. , 2013, “ Vaginal Degeneration Following Implantation of Synthetic Mesh With Increased Stiffness,” BJOG, 120(2), pp. 233–243. [CrossRef] [PubMed]
Jallah, Z. , Liang, R. , Feola, A. , Barone, W. , Palcsey, S. , Abramowitch, S. D. , Yoshimura, N. , and Moalli, P. , 2015, “ The Impact of Prolapse Mesh on Vaginal Smooth Muscle Structure and Function,” BJOG, 123(7), pp. 1076–1085. [CrossRef] [PubMed]
Alford, P. , Humphrey, J. , and Taber, L. , 2008, “ Growth and Remodeling in a Thick-Walled Artery Model: Effects of Spatial Variations in Wall Constituents,” Biomech. Model. Mechanobiol., 7(4), pp. 245–262. [CrossRef] [PubMed]

Figures

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Fig. 1

Estimation of the physiologic, in vivo axial stretch ratio for representative sample #4 in Table 1: (a) the nearly constant transducer-measured axial force occurs at the estimated physiologic (in vivo) axial stretch ratio and (b) the point of intersection of force–length (extension) tests performed at constant, multiple luminal pressures further confirms the estimated in vivo axial stretch ratio. The dashed vertical line represents the estimated in vivo axial stretch.

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Fig. 2

Fits of the HGO model to experimental (pre- and post-treatment with elastase) data (mean±SEM, n = 8, paired): (a) intraluminal pressure versus outer diameter: a rightward shift was observed post-treatment, indicating dilatation of the vagina, (b) wall-averaged circumferential Cauchy stress versus circumferential stretch ratio: a rise was observed post-treatment, indicating increased structural stiffness circumferentially, (c) wall-averaged axial Cauchy stress versus circumferential stretch ratio, (d) wall-averaged axial Cauchy stress versus axial stretch ratio, (e) the transducer-measured axial force versus pressure, which remained nearly constant with increasing pressure, and (f) the sum of transducer-measured force and force due to increasing intraluminal pressure versus pressure: the increased separation at higher pressures is attributable to dilated lumen (increased inner radius) of the elastase-treated vagina

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Fig. 3

Holzapfel–Gasser–Ogden model sensitivity in the (a) circumferential and (b) axial directions, pre-elastase (solid lines) and postelastase (dashed lines) treatment. Pre- and post-treatment, the model was most sensitive to the collagen-associated nondimensional parameter—c2 and the alignment angle-α. Relative to control, post-treatment, the influence of the two parameters increased the most in both directions. Sensitivity indices were computed using optimized model parameters for averaged data (n = 8/group, for control and elastase).

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Fig. 4

Vaginal tissue average compliance as a function of intraluminal pressure, data = mean±SEM. Statistically significant (*p < 0.05) decrease was observed at 5 and 10 mmHg.

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Fig. 5

Histological section samples stained with: (a)–(d) PSR,(e)–(h) MTC, and (i)–(l) Hart's elastin stain. Elastic fiber area fraction exhibited statistically significant decrease post-treatment. For all stains, area fraction analysis was performed using images acquired at 4× objective. In the 20× and 40× (Supplemental Fig. 3, which is available under the “Supplemental Data” tab for this paper on the ASME Digital Collection) objective images of Hart's stained section, a decrease in population and organization of elastic fibers is observable.

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