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Research Papers

Design Requirements for Annulus Fibrosus Repair: Review of Forces, Displacements, and Material Properties of the Intervertebral Disk and a Summary of Candidate Hydrogels for Repair

[+] Author and Article Information
Rose G. Long

Icahn School of Medicine at Mount Sinai,
Leni and Peter W. May Department of
Orthopaedics,
New York, NY 10029;
Collaborative Research Partner Annulus Fibrosus
Rupture Program of AO Foundation,
Davos 7270, Switzerland
e-mail: rose.long@mssm.edu

Olivia M. Torre

Icahn School of Medicine at Mount Sinai,
Leni and Peter W. May Department of
Orthopaedics,
One Gustave Levy Place, Box 1188,
New York, NY 10029
e-mail: olivia.torre@icahn.mssm.edu

Warren W. Hom

Icahn School of Medicine at Mount Sinai,
Leni and Peter W. May Department of
Orthopaedics,
One Gustave Levy Place, Box 1188,
New York, NY 10029
e-mail: warren.hom@mssm.edu

Dylan J. Assael

Icahn School of Medicine at Mount Sinai,
Leni and Peter W. May Department of
Orthopaedics,
One Gustave Levy Place, Box 1188,
New York, NY 10029
e-mail: dylan.assael@icahn.mssm.edu

James C. Iatridis

Icahn School of Medicine at Mount Sinai,
Leni and Peter W. May Department of
Orthopaedics,
One Gustave Levy Place, Box 1188,
New York, NY 10029;
Collaborative Research Partner Annulus Fibrosus
Rupture Program of AO Foundation,
Davos 7270, Switzerland
e-mail: james.iatridis@mssm.edu

1Corresponding author.

Manuscript received August 26, 2015; final manuscript received December 8, 2015; published online January 27, 2016. Editor: Beth A. Winkelstein.

J Biomech Eng 138(2), 021007 (Jan 27, 2016) (14 pages) Paper No: BIO-15-1421; doi: 10.1115/1.4032353 History: Received August 26, 2015; Revised December 08, 2015

There is currently a lack of clinically available solutions to restore functionality to the intervertebral disk (IVD) following herniation injury to the annulus fibrosus (AF). Microdiscectomy is a commonly performed surgical procedure to alleviate pain caused by herniation; however, AF defects remain and can lead to accelerated degeneration and painful conditions. Currently available AF closure techniques do not restore mechanical functionality or promote tissue regeneration, and have risk of reherniation. This review determined quantitative design requirements for AF repair materials and summarized currently available hydrogels capable of meeting these design requirements by using a series of systematic PubMed database searches to yield 1500+ papers that were screened and analyzed for relevance to human lumbar in vivo measurements, motion segment behaviors, and tissue level properties. We propose a testing paradigm involving screening tests as well as more involved in situ and in vivo validation tests to efficiently identify promising biomaterials for AF repair. We suggest that successful materials must have high adhesion strength (∼0.2 MPa), match as many AF material properties as possible (e.g., approximately 1 MPa, 0. 3 MPa, and 30 MPa for compressive, shear, and tensile moduli, respectively), and have high tensile failure strain (∼65%) to advance to in situ and in vivo validation tests. While many biomaterials exist for AF repair, few undergo extensive mechanical characterization. A few hydrogels show promise for AF repair since they can match at least one material property of the AF while also adhering to AF tissue and are capable of easy implantation during surgical procedures to warrant additional optimization and validation.

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References

Vos, T. , Flaxman, A. D. , Naghavi, M. , Lozano, R. , Michaud, C. , Ezzati, M. , Shibuya, K. , Salomon, J. A. , Abdalla, S. , Aboyans, V. , Abraham, J. , Ackerman, I. , Aggarwal, R. , Ahn, S. Y. , Ali, M. K. , AlMazroa, M. A. , Alvarado, M. , Anderson, H. R. , Anderson, L. M. , Andrews, K. G. , Atkinson, C. , Baddour, L. M. , Bahalim, A. N. , Barker-Collo, S. , Barrero, L. H. , Bartels, D. H. , Basáñez, M.-G. , Baxter, A. , Bell, M. L. , Benjamin, E. J. , Bennett, D. , Bernabé, E. , Bhalla, K. , Bhandari, B. , Bikbov, B. , Abdulhak, A. B. , Birbeck, G. , Black, J. A. , Blencowe, H. , Blore, J. D. , Blyth, F. , Bolliger, I. , Bonaventure, A. , Boufous, S. , Bourne, R. , Boussinesq, M. , Braithwaite, T. , Brayne, C. , Bridgett, L. , Brooker, S. , Brooks, P. , Brugha, T. S. , Bryan-Hancock, C. , Bucello, C. , Buchbinder, R. , Buckle, G. , Budke, C. M. , Burch, M. , Burney, P. , Burstein, R. , Calabria, B. , Campbell, B. , Canter, C. E. , Carabin, H. , Carapetis, J. , Carmona, L. , Cella, C. , Charlson, F. , Chen, H. , Cheng, A. T.-A. , Chou, D. , Chugh, S. S. , Coffeng, L. E. , Colan, S. D. , Colquhoun, S. , Colson, K. E. , Condon, J. , Connor, M. D. , Cooper, L. T. , Corriere, M. , Cortinovis, M. , Courville de Vaccaro, K. , Couser, W. , Cowie, B. C. , Criqui, M. H. , Cross, M. , Dabhadkar, K. C. , Dahiya, M. , Dahodwala, N. , Damsere-Derry, J. , Danaei, G. , Davis, A. , De Leo, D. , Degenhardt, L. , Dellavalle, R. , Delossantos, A. , Denenberg, J. , Derrett, S. , Des Jarlais, D. C. , Dharmaratne, S. D. , Dherani, M. , Diaz-Torne, C. , Dolk, H. , Dorsey, E. R. , Driscoll, T. , Duber, H. , Ebel, B. , Edmond, K. , Elbaz, A. , Eltahir Ali, S. , Erskine, H. , Erwin, P. J. , Espindola, P. , Ewoigbokhan, S. E. , Farzadfar, F. , Feigin, V. , Felson, D. T. , Ferrari, A. , Ferri, C. P. , Fèvre, E. M. , Finucane, M. M. , Flaxman, S. , Flood, L. , Foreman, K. , Forouzanfar, M. H. , Fowkes, F. G. R. , Franklin, R. , Fransen, M. , Freeman, M. K. , Gabbe, B. J. , Gabriel, S. E. , Gakidou, E. , Ganatra, H. A. , Garcia, B. , Gaspari, F. , Gillum, R. F. , Gmel, G. , Gosselin, R. , Grainger, R. , Groeger, J. , Guillemin, F. , Gunnell, D. , Gupta, R. , Haagsma, J. , Hagan, H. , Halasa, Y. A. , Hall, W. , Haring, D. , Haro, J. M. , Harrison, J. E. , Havmoeller, R. , Hay, R. J. , Higashi, H. , Hill, C. , Hoen, B. , Hoffman, H. , Hotez, P. J. , Hoy, D. , Huang, J. J. , Ibeanusi, S. E. , Jacobsen, K. H. , James, S. L. , Jarvis, D. , Jasrasaria, R. , Jayaraman, S. , Johns, N. , Jonas, J. B. , Karthikeyan, G. , Kassebaum, N. , Kawakami, N. , Keren, A. , Khoo, J.-P. , King, C. H. , Knowlton, L. M. , Kobusingye, O. , Koranteng, A. , Krishnamurthi, R. , Lalloo, R. , Laslett, L. L. , Lathlean, T. , Leasher, J. L. , Lee, Y. Y. , Leigh, J. , Lim, S. S. , Limb, E. , Lin, J. K. , Lipnick, M. , Lipshultz, S. E. , Liu, W. , Loane, M. , Lockett Ohno, S. , Lyons, R. , Ma, J. , Mabweijano, J. , MacIntyre, M. F. , Malekzadeh, R. , Mallinger, L. , Manivannan, S. , Marcenes, W. , March, L. , Margolis, D. J. , Marks, G. B. , Marks, R. , Matsumori, A. , Matzopoulos, R. , Mayosi, B. M. , McAnulty, J. H. , McDermott, M. M. , McGill, N. , McGrath, J. , Medina-Mora, M. E. , Meltzer, M. , Memish, Z. A. , Mensah, G. A. , Merriman, T. R. , Meyer, A.-C. , Miglioli, V. , Miller, M. , Miller, T. R. , Mitchell, P. B. , Mocumbi, A. O. , Moffitt, T. E. , Mokdad, A. A. , Monasta, L. , Montico, M. , Moradi-Lakeh, M. , Moran, A. , Morawska, L. , Mori, R. , Murdoch, M. E. , Mwaniki, M. K. , Naidoo, K. , Nair, M. N. , Naldi, L. , Narayan, K. M. V. , Nelson, P. K. , Nelson, R. G. , Nevitt, M. C. , Newton, C. R. , Nolte, S. , Norman, P. , Norman, R. , O' Donnell, M. , O' Hanlon, S. , Olives, C. , Omer, S. B. , Ortblad, K. , Osborne, R. , Ozgediz, D. , Page, A. , Pahari, B. , Pandian, J. D. , Panozo Rivero, A. , Patten, S. B. , Pearce, N. , Perez Padilla, R. , Perez-Ruiz, F. , Perico, N. , Pesudovs, K. , Phillips, D. , Phillips, M. R. , Pierce, K. , Pion, S. , Polanczyk, G. V. , Polinder, S. , Pope III, C. A. , Popova, S. , Porrini, E. , Pourmalek, F. , Prince, M. , Pullan, R. L. , Ramaiah, K. D. , Ranganathan, D. , Razavi, H. , Regan, M. , Rehm, J. T. , Rein, D. B. , Remuzzi, G. , Richardson, K. , Rivara, F. P. , Roberts, T. , Robinson, C. , Rodriguez De Leòn, F. , Ronfani, L. , Room, R. , Rosenfeld, L. C. , Rushton, L. , Sacco, R. L. , Saha, S. , Sampson, U. , Sanchez-Riera, L. , Sanman, E. , Schwebel, D. C. , Scott, J. G. , Segui-Gomez, M. , Shahraz, S. , Shepard, D. S. , Shin, H. , Shivakoti, R. , Silberberg, D. , Singh, D. , Singh, G. M. , Singh, J. A. , Singleton, J. , Sleet, D. A. , Sliwa, K. , Smith, E. , Smith, J. L. , Stapelberg, N. J. C. , Steer, A. , Steiner, T. , Stolk, W. A. , Stovner, L. J. , Sudfeld, C. , Syed, S. , Tamburlini, G. , Tavakkoli, M. , Taylor, H. R. , Taylor, J. A. , Taylor, W. J. , Thomas, B. , Thomson, W. M. , Thurston, G. D. , Tleyjeh, I. M. , Tonelli, M. , Towbin, J. A. , Truelsen, T. , Tsilimbaris, M. K. , Ubeda, C. , Undurraga, E. A. , van der Werf, M. J. , van Os, J. , Vavilala, M. S. , Venketasubramanian, N. , Wang, M. , Wang, W. , Watt, K. , Weatherall, D. J. , Weinstock, M. A. , Weintraub, R. , Weisskopf, M. G. , Weissman, M. M. , White, R. A. , Whiteford, H. , Wiersma, S. T. , Wilkinson, J. D. , Williams, H. C. , Williams, S. R. M. , Witt, E. , Wolfe, F. , Woolf, A. D. , Wulf, S. , Yeh, P.-H. , Zaidi, A. K. M. , Zheng, Z.-J. , Zonies, D. , Lopez, A. D. , and Murray, C. J. L. , 2012, “ Years Lived With Disability (YLDs) for 1160 Sequelae of 289 Diseases and Injuries 1990–2010: A Systematic Analysis for the Global Burden of Disease Study 2010,” Lancet, 380(9859), pp. 2163–2196. [CrossRef] [PubMed]
March, L. , Smith, E. U. R. , Hoy, D. G. , Cross, M. J. , Sanchez-Riera, L. , Blyth, F. , Buchbinder, R. , Vos, T. , and Woolf, A. D. , 2014, “ Burden of Disability Due to Musculoskeletal (MSK) Disorders,” Best Pract. Res. Clin. Rheumatol., 28(3), pp. 353–366. [CrossRef] [PubMed]
Weinstein, J. N. , Lurie, J. D. , Tosteson, T. D. , Skinner, J. S. , Hanscom, B. , Tosteson, A. N. A. , Herkowitz, H. , Fischgrund, J. , Cammisa, F. P. , Albert, T. , and Deyo, R. A. , 2006, “ Surgical versus Nonoperative Treatment for Lumbar Disk Herniation: The Spine Patient Outcomes Research Trial (SPORT) Observational Cohort,” JAMA, 296(20), pp. 2451–2459. [CrossRef] [PubMed]
Weinstein, J. N. , Lurie, J. D. , Tosteson, T. D. , Tosteson, A. N. A. , Blood, E. A. , Abdu, W. A. , Herkowitz, H. , Hilibrand, A. , Albert, T. , and Fischgrund, J. , 2008, “ Surgical Versus Nonoperative Treatment for Lumbar Disc Herniation: Four-Year Results for the Spine Patient Outcomes Research Trial (SPORT),” Spine, 33(25), pp. 2789–2800. [CrossRef] [PubMed]
Asch, H. L. , Lewis, P. J. , Moreland, D. B. , Egnatchik, J. G. , Yu, Y. J. , Clabeaux, D. E. , and Hyland, A. H. , 2002, “ Prospective Multiple Outcomes Study of Outpatient Lumbar Microdiscectomy: Should 75 to 80% Success Rates be the Norm?,” J. Neurosurg., 96(1 Suppl.), pp. 34–44. [PubMed]
Gray, D. T. , Deyo, R. A. , Kreuter, W. , Mirza, S. K. , Heagerty, P. J. , Comstock, B. A. , and Chan, L. , 2006, “ Population-Based Trends in Volumes and Rates of Ambulatory Lumbar Spine Surgery,” Spine, 31(17), pp. 1957–1964. [CrossRef] [PubMed]
McGirt, M. J. , Eustacchio, S. , Varga, P. , Vilendecic, M. , Trummer, M. , Gorensek, M. , Ledic, D. , and Carragee, E. J. , 2009, “ A Prospective Cohort Study of Close Interval Computed Tomography and Magnetic Resonance Imaging After Primary Lumbar Discectomy: Factors Associated With Recurrent Disc Herniation and Disc Height Loss,” Spine, 34(19), pp. 2044–2051. [CrossRef] [PubMed]
Watters, W. C. , and McGirt, M. J. , 2009, “ An Evidence-Based Review of the Literature on the Consequences of Conservative Versus Aggressive Discectomy for the Treatment of Primary Disc Herniation With Radiculopathy,” Spine J., 9(3), pp. 240–257. [CrossRef] [PubMed]
Ambrossi, G. L. G. , McGirt, M. J. , Sciubba, D. M. , Witham, T. F. , Wolinsky, J.-P. , Gokaslan, Z. L. , and Long, D. M. , 2009, “ Recurrent Lumbar Disc Herniation After Single-Level Lumbar Discectomy,” Neurosurgery, 65(3), pp. 574–578. [CrossRef] [PubMed]
Iatridis, J. C. , MacLean, J. J. , Roughley, P. J. , and Alini, M. , 2006, “ Effects of Mechanical Loading on Intervertebral Disc Metabolism In Vivo,” J. Bone Joint Surg. Am., 88(Suppl. 2), pp. 41–46. [CrossRef] [PubMed]
Elliott, D. M. , Yerramalli, C. S. , Beckstein, J. C. , Boxberger, J. I. , Johannessen, W. , and Vresilovic, E. J. , 2008, “ The Effect of Relative Needle Diameter in Puncture and Sham Injection Animal Models of Degeneration,” Spine, 33(6), pp. 588–596. [CrossRef] [PubMed]
Iatridis, J. C. , Nicoll, S. B. , Michalek, A. J. , Walter, B. A. , and Gupta, M. S. , 2013, “ Role of Biomechanics in Intervertebral Disc Degeneration and Regenerative Therapies: What Needs Repairing in the Disc and What are Promising Biomaterials for its Repair?,” Spine J., 13(3), pp. 243–262. [CrossRef] [PubMed]
Michalek, A. J. , and Iatridis, J. C. , 2012, “ Height and Torsional Stiffness are Most Sensitive to Annular Injury in Large Animal Intervertebral Discs,” Spine J., 12(5), pp. 425–432. [CrossRef] [PubMed]
Masuda, K. , Aota, Y. , Muehleman, C. , Imai, Y. , Okuma, M. , Thonar, E. J. , Andersson, G. B. , and An, H. S. , 2005, “ A Novel Rabbit Model of Mild, Reproducible Disc Degeneration by an Anulus Needle Puncture: Correlation Between the Degree of Disc Injury and Radiological and Histological Appearances of Disc Degeneration,” Spine, 30(1), pp. 5–14. [PubMed]
Melrose, J. , Roberts, S. , Smith, S. , Menage, J. , and Ghosh, P. , 2002, “ Increased Nerve and Blood Vessel Ingrowth Associated With Proteoglycan Depletion in an Ovine Anular Lesion Model of Experimental Disc Degeneration,” Spine, 27(12), pp. 1278–1285. [CrossRef] [PubMed]
Freemont, A. J. , Peacock, T. E. , Goupille, P. , Hoyland, J. A. , O'Brien, J. , and Jayson, M. I. , 1997, “ Nerve Ingrowth Into Diseased Intervertebral Disc in Chronic Back Pain,” Lancet, 350(9072), pp. 178–181. [CrossRef] [PubMed]
Ahlgren, B. D. , Lui, W. , Herkowitz, H. N. , Panjabi, M. M. , and Guiboux, J. P. , 2000, “ Effect of Anular Repair on the Healing Strength of the Intervertebral Disc: A Sheep Model,” Spine, 25(17), pp. 2165–2170. [CrossRef] [PubMed]
Bailey, A. , Araghi, A. , Blumenthal, S. , and Huffmon, G. V. , 2013, “ Prospective, Multicenter, Randomized, Controlled Study of Anular Repair in Lumbar Discectomy,” Spine, 38(14), pp. 1161–1169. [CrossRef] [PubMed]
Lequin, M. B. , Barth, M. , Thomé, C. , and Bouma, G. J. , 2012, “ Primary Limited Lumbar Discectomy With an Annulus Closure Device: One-Year Clinical and Radiographic Results From a Prospective, Multi-Center Study,” Korean J. Spine, 9(4), pp. 340–347. [CrossRef] [PubMed]
Wilke, H.-J. , Ressel, L. , Heuer, F. , Graf, N. , and Rath, S. , 2013, “ Can Prevention of a Reherniation be Investigated? Establishment of a Herniation Model and Experiments With an Anular Closure Device,” Spine, 38(10), pp. E587–E593. [CrossRef] [PubMed]
Trummer, M. , Eustacchio, S. , Barth, M. , Klassen, P. D. , and Stein, S. , 2013, “ Protecting Facet Joints Post-Lumbar Discectomy: Barricaid Annular Closure Device Reduces Risk of Facet Degeneration,” Clin. Neurol. Neurosurg., 115(8), pp. 1440–1445. [CrossRef] [PubMed]
Masuda, K. , and Lotz, J. C. , 2010, “ New Challenges for Intervertebral Disc Treatment Using Regenerative Medicine,” Tissue Eng. Part B: Rev., 16(1), pp. 147–158. [CrossRef] [PubMed]
Sakai, D. , and Andersson, G. B. J. , 2015, “ Stem Cell Therapy for Intervertebral Disc Regeneration: Obstacles and Solutions,” Nat. Rev. Rheumatol., 11(4), pp. 243–256. [CrossRef] [PubMed]
Guterl, C. C. , See, E. Y. , Blanquer, S. B. G. , Pandit, A. , Ferguson, S. J. , Benneker, L. M. , Grijpma, D. W. , Sakai, D. , Eglin, D. , Alini, M. , Iatridis, J. C. , and Grad, S. , 2013, “ Challenges and Strategies in the Repair of Ruptured Annulus Fibrosus,” Eur. Cell Mater., 25, pp. 1–21. [PubMed]
Kandel, R. , Roberts, S. , and Urban, J. P. G. , 2008, “ Tissue Engineering and the Intervertebral Disc: The Challenges,” Eur. Spine J., 17(S4), pp. 480–491. [CrossRef] [PubMed]
Nerurkar, N. L. , Elliott, D. M. , and Mauck, R. L. , 2010, “ Mechanical Design Criteria for Intervertebral Disc Tissue Engineering,” J. Biomech., 43(6), pp. 1017–1030. [CrossRef] [PubMed]
Likhitpanichkul, M. , Dreischarf, M. , Illien-Junger, S. , Walter, B. A. , Nukaga, T. , Long, R. G. , Sakai, D. , Hecht, A. C. , and Iatridis, J. C. , 2014, “ Fibrin-Genipin Adhesive Hydrogel for Annulus Fibrosus Repair: Performance Evaluation With Large Animal Organ Culture, In Situ Biomechanics, and In Vivo Degradation Tests,” Eur. Cell Mater., 28, pp. 25–38. [PubMed]
Quinnell, R. C. , Stockdale, H. R. , and Willis, D. S. , 1983, “ Observations of Pressures Within Normal Discs in the Lumbar Spine,” Spine, 8(2), pp. 166–169. [CrossRef] [PubMed]
Nachemson, A. , and Elfstrom, G. , 1970, “ Intravital Dynamic Pressure Measurements in Lumbar Discs. A Study of Common Movements, Maneuvers and Exercises,” Scand. J. Rehabil. Med. Suppl., 1, pp. 1–40. [PubMed]
Wilke, H. J. , Neef, P. , Caimi, M. , Hoogland, T. , and Claes, L. E. , 1999, “ New In Vivo Measurements of Pressures in the Intervertebral Disc in Daily Life,” Spine, 24(8), pp. 755–762. [CrossRef] [PubMed]
Sato, K. , Kikuchi, S. , and Yonezawa, T. , 1999, “ In Vivo Intradiscal Pressure Measurement in Healthy Individuals and in Patients With Ongoing Back Problems,” Spine, 24(23), pp. 2468–2474. [CrossRef] [PubMed]
Schultz, A. , Andersson, G. , Ortengren, R. , Haderspeck, K. , and Nachemson, A. , 1982, “ Loads on the Lumbar Spine. Validation of a Biomechanical Analysis by Measurements of Intradiscal Pressures and Myoelectric Signals,” J. Bone Joint Surg. Am., 64(5), pp. 713–720. [PubMed]
Okushima, H. , 1970, “ Study on Hydrodynamic Pressure of Lumbar Intervertebral Disc,” Nihon Geka Hokan, 39(1), pp. 45–57. [PubMed]
Nachemson, A. , and Morris, J. M. , 1964, “ In Vivo Measurements of Intradiscal Pressure. Discometry, A Method for the Determination of the Pressure in the Lower Lumbar Discs,” J. Bone Joint Surg. Am., 46, pp. 1077–1092. [PubMed]
Nachemson, A. , 1965, “ The Effect of Forward Leaning on Lumbar Intradiscal Pressure,” Acta Orthop. Scand., 35, pp. 314–328. [CrossRef] [PubMed]
Nachemson, A. , 1966, “ The Load on Lumbar Disks in Different Positions of the Body,” Clin. Orthop. Relat. Res., 45, pp. 107–122. [PubMed]
Andersson, B. J. , and Ortengren, R. , 1974, “ Lumbar Disc Pressure and Myoelectric Back Muscle Activity During Sitting. 3. Studies on a Wheelchair,” Scand. J. Rehabil. Med., 6(3), pp. 122–127. [PubMed]
Andersson, B. J. , and Ortengren, R. , 1974, “ Lumbar Disc Pressure and Myoelectric Back Muscle Activity During Sitting. II. Studies on an Office Chair,” Scand. J. Rehabil. Med., 6(3), pp. 115–121. [PubMed]
Andersson, G. B. , Ortengren, R. , and Nachemson, A. , 1977, “ Intradiskal Pressure, Intra-Abdominal Pressure and Myoelectric Back Muscle Activity Related to Posture and Loading,” Clin. Orthop. Relat. Res., 129, pp. 156–164. [CrossRef] [PubMed]
Adams, M. A. , and Hutton, W. C. , 1980, “ The Effect of Posture on the Role of the Apophysial Joints in Resisting Intervertebral Compressive Forces,” J. Bone Joint Surg. Br., 62(3), pp. 358–362. [PubMed]
Claus, A. , Hides, J. , Moseley, G. L. , and Hodges, P. , 2008, “ Sitting Versus Standing: Does the Intradiscal Pressure Cause Disc Degeneration or Low Back Pain?,” J. Electromyogr. Kinesiol., 18(4), pp. 550–558. [CrossRef] [PubMed]
Nachemson, A. , 1960, “ Lumbar Intradiscal Pressure. Experimental Studies on Post-Mortem Material,” Acta Orthop. Scand. Suppl., 43, pp. 1–104. [CrossRef] [PubMed]
Merriam, W. F. , Quinnell, R. C. , Stockdale, H. R. , and Willis, D. S. , 1984, “ The Effect of Postural Changes on the Inferred Pressures Within the Nucleus Pulposus During Lumbar Discography,” Spine, 9(4), pp. 405–408. [CrossRef] [PubMed]
Pearcy, M. , Portek, I. , and Shepherd, J. , 1984, “ Three-Dimensional X-Ray Analysis of Normal Movement in the Lumbar Spine,” Spine, 9(3), pp. 294–297. [CrossRef] [PubMed]
Pearcy, M. J. , and Tibrewal, S. B. , 1984, “ Axial Rotation and Lateral Bending in the Normal Lumbar Spine Measured by Three-Dimensional Radiography,” Spine, 9(6), pp. 582–587. [CrossRef] [PubMed]
Lee, S.-H. , Daffner, S. D. , and Wang, J. C. , 2014, “ Does Lumbar Disk Degeneration Increase Segmental Mobility In Vivo? Segmental Motion Analysis of the Whole Lumbar Spine Using Kinetic MRI,” J. Spinal Disord. Tech., 27(2), pp. 111–116. [CrossRef] [PubMed]
Nagel, T. M. , Zitnay, J. L. , Barocas, V. H. , and Nuckley, D. J. , 2014, “ Quantification of Continuous In Vivo Flexion–Extension Kinematics and Intervertebral Strains,” Eur. Spine J., 23(4), pp. 754–761. [CrossRef] [PubMed]
Nagel, T. M. , Hadi, M. F. , Claeson, A. A. , Nuckley, D. J. , and Barocas, V. H. , 2014, “ Combining Displacement Field and Grip Force Information to Determine Mechanical Properties of Planar Tissue With Complicated Geometry,” ASME J. Biomech. Eng., 136(11), p. 114501. [CrossRef]
Kanayama, M. , Tadano, S. , Kaneda, K. , Ukai, T. , Abumi, K. , and Ito, M. , 1995, “ A Cineradiographic Study on the Lumbar Disc Deformation During Flexion and Extension of the Trunk,” Clin. Biomech. (Bristol, Avon), 10(4), pp. 193–199. [CrossRef] [PubMed]
Zhong, W. , Driscoll, S. J. , Wu, M. , Wang, S. , Liu, Z. , Cha, T. D. , Wood, K. B. , and Li, G. , 2014, “ In Vivo Morphological Features of Human Lumbar Discs,” Medicine, 93(28), p. e333. [CrossRef] [PubMed]
Pearcy, M. J. , and Tibrewal, S. B. , 1984, “ Lumbar Intervertebral Disc and Ligament Deformations Measured In Vivo,” Clin. Orthop. Relat. Res., 191, pp. 281–286. [PubMed]
Aiyangar, A. K. , Zheng, L. , Tashman, S. , Anderst, W. J. , and Zhang, X. , 2014, “ Capturing Three-Dimensional In Vivo Lumbar Intervertebral Joint Kinematics Using Dynamic Stereo-X-Ray Imaging,” ASME J. Biomech. Eng., 136(1), p. 011004. [CrossRef]
Miao, J. , Wang, S. , Wan, Z. , Park, W. M. , Xia, Q. , Wood, K. , and Li, G. , 2013, “ Motion Characteristics of the Vertebral Segments With Lumbar Degenerative Spondylolisthesis in Elderly Patients,” Eur. Spine J., 22(2), pp. 425–431. [CrossRef] [PubMed]
Stokes, I. A. , and Frymoyer, J. W. , 1987, “ Segmental Motion and Instability,” Lumbar Intradiscal Pressure: Experimental Studies on Post-Mortem Material, 12(7), pp. 688–691.
Li, G. , Wang, S. , Passias, P. , Xia, Q. , Li, G. , and Wood, K. , 2009, “ Segmental In Vivo Vertebral Motion During Functional Human Lumbar Spine Activities,” Eur. Spine J., 18(7), pp. 1013–1021. [CrossRef] [PubMed]
Xia, Q. , Wang, S. , Kozanek, M. , Passias, P. , Wood, K. , and Li, G. , 2010, “ In-Vivo Motion Characteristics of Lumbar Vertebrae in Sagittal and Transverse Planes,” J. Biomech., 43(10), pp. 1905–1909. [CrossRef] [PubMed]
Wang, S. , Xia, Q. , Passias, P. , Li, W. , Wood, K. , and Li, G. , 2011, “ How Does Lumbar Degenerative Disc Disease Affect the Disc Deformation at the Cephalic Levels In Vivo?,” Spine, 36(9), pp. E574–E581. [CrossRef] [PubMed]
Yoder, J. H. , Peloquin, J. M. , Song, G. , Tustison, N. J. , Moon, S. M. , Wright, A. C. , Vresilovic, E. J. , Gee, J. C. , and Elliott, D. M. , 2014, “ Internal Three-Dimensional Strains in Human Intervertebral Discs Under Axial Compression Quantified Noninvasively by Magnetic Resonance Imaging and Image Registration,” ASME J. Biomech. Eng., 136(11), p. 111008. [CrossRef]
Stokes, I. A. , 1987, “ Surface Strain on Human Intervertebral Discs,” J. Orthop. Res., 5(3), pp. 348–355. [CrossRef] [PubMed]
Nachemson, A. L. , Schultz, A. B. , and Berkson, M. H. , 1979, “ Mechanical Properties of Human Lumbar Spine Motion Segments. Influence of Age, Sex, Disc Level, and Degeneration,” Spine, 4(1), pp. 1–8. [CrossRef] [PubMed]
Shea, M. , Takeuchi, T. Y. , Wittenberg, R. H. , White, A. A. , and Hayes, W. C. , 1994, “ A Comparison of the Effects of Automated Percutaneous Diskectomy and Conventional Diskectomy on Intradiscal Pressure, Disk Geometry, and Stiffness,” J. Spinal Disord., 7(4), pp. 317–325. [CrossRef] [PubMed]
Beckstein, J. C. , Sen, S. , Schaer, T. P. , Vresilovic, E. J. , and Elliott, D. M. , 2008, “ Comparison of Animal Discs Used in Disc Research to Human Lumbar Disc: Axial Compression Mechanics and Glycosaminoglycan Content,” Spine, 33(6), pp. E166–E173. [CrossRef] [PubMed]
Gardner-Morse, M. G. , and Stokes, I. A. F. , 2004, “ Structural Behavior of Human Lumbar Spinal Motion Segments,” J. Biomech., 37(2), pp. 205–212. [CrossRef] [PubMed]
Lu, W. W. , Luk, K. D. K. , Holmes, A. D. , Cheung, K. M. C. , and Leong, J. C. Y. , 2005, “ Pure Shear Properties of Lumbar Spinal Joints and the Effect of Tissue Sectioning on Load Sharing,” Spine, 30(8), pp. E204–E209. [CrossRef] [PubMed]
Showalter, B. L. , Beckstein, J. C. , Martin, J. T. , Beattie, E. E. , Espinoza Orías, A. A. , Schaer, T. P. , Vresilovic, E. J. , and Elliott, D. M. , 2012, “ Comparison of Animal Discs Used in Disc Research to Human Lumbar Disc: Torsion Mechanics and Collagen Content,” Spine, 37(15), pp. E900–E907. [CrossRef] [PubMed]
Thompson, R. E. , Pearcy, M. J. , Downing, K. J. , Manthey, B. A. , Parkinson, I. H. , and Fazzalari, N. L. , 2000, “ Disc Lesions and the Mechanics of the Intervertebral Joint Complex,” Spine, 25(23), pp. 3026–3035. [CrossRef] [PubMed]
Marini, G. , Huber, G. , Püschel, K. , and Ferguson, S. J. , 2015, “ Nonlinear Dynamics of the Human Lumbar Intervertebral Disc,” J. Biomech., 48(3), pp. 479–488. [CrossRef] [PubMed]
O'Connell, G. D. , Jacobs, N. T. , Sen, S. , Vresilovic, E. J. , and Elliott, D. M. , 2011, “ Axial Creep Loading and Unloaded Recovery of the Human Intervertebral Disc and the Effect of Degeneration,” J. Mech. Behav. Biomed. Mater., 4(7), pp. 933–942. [CrossRef] [PubMed]
Landham, P. R. , Baker-Rand, H. L. A. , Gilbert, S. J. , Pollintine, P. , Annesley-Williams, D. J. , Adams, M. A. , and Dolan, P. , 2015, “ Is kyphoplasty Better Than Vertebroplasty at Restoring Form and Function After Severe Vertebral Wedge Fractures?,” Spine J., 15(4), pp. 721–732. [CrossRef] [PubMed]
Frei, H. , Oxland, T. R. , and Nolte, L. P. , 2002, “ Thoracolumbar Spine Mechanics Contrasted Under Compression and Shear Loading,” J. Orthop. Res., 20(6), pp. 1333–1338. [CrossRef] [PubMed]
Okawa, A. , Shinomiya, K. , Takakuda, K. , and Nakai, O. , 1996, “ A Cadaveric Study on the Stability of Lumbar Segment After Partial Laminotomy and Facetectomy With Intact Posterior Ligaments,” J. Spinal Disord., 9(6), pp. 518–526. [CrossRef] [PubMed]
McGlashen, K. M. , Miller, J. A. , Schultz, A. B. , and Andersson, G. B. , 1987, “ Load Displacement Behavior of the Human Lumbo-Sacral Joint,” J. Orthop. Res., 5(4), pp. 488–496. [CrossRef] [PubMed]
Kiehl, K. L. , Curry, W. H. , Stemper, B. D. , Eckardt, G. , Basiden, J. L. , Maiman, D. J. , Yoganandan, N. , and Shender, B. S. , 2014, “ A Method for Inducing and Determining Biomechanics Associated With Endplate Fractures in the Lumbar Spine,” Biomed. Sci. Instrum., 50, pp. 119–124. [PubMed]
Gardner-Morse, M. G. , and Stokes, I. A. , 2003, “ Physiological Axial Compressive Preloads Increase Motion Segment Stiffness, Linearity and Hysteresis in all Six Degrees of Freedom for Small Displacements About the Neutral Posture,” J. Orthop. Res., 21(3), pp. 547–552. [CrossRef] [PubMed]
Izambert, O. , Mitton, D. , Thourot, M. , and Lavaste, F. , 2003, “ Dynamic Stiffness and Damping of Human Intervertebral Disc Using Axial Oscillatory Displacement Under a Free Mass System,” Eur. Spine J., 12(6), pp. 562–566. [CrossRef] [PubMed]
Costi, J. J. , Stokes, I. A. , Gardner-Morse, M. G. , and Iatridis, J. C. , 2008, “ Frequency-Dependent Behavior of the Intervertebral Disc in Response to Each of Six Degree of Freedom Dynamic Loading: Solid Phase and Fluid Phase Contributions,” Spine, 33(16), pp. 1731–1738. [CrossRef] [PubMed]
Smeathers, J. E. , and Joanes, D. N. , 1988, “ Dynamic Compressive Properties of Human Lumbar Intervertebral Joints: A Comparison Between Fresh and Thawed Specimens,” J. Biomech., 21(5), pp. 425–433. [CrossRef] [PubMed]
Alkalay, R. N. , Vader, D. , and Hackney, D. , 2015, “ The Degenerative State of the Intervertebral Disk Independently Predicts the Failure of Human Lumbar Spine to High Rate Loading: An Experimental Study,” Clin. Biomech. (Bristol, Avon)., 30(2), pp. 211–218. [CrossRef] [PubMed]
Keller, T. S. , Spengler, D. M. , and Hansson, T. H. , 1987, “ Mechanical Behavior of the Human Lumbar Spine. I. Creep Analysis During Static Compressive Loading,” J. Orthop. Res., 5(4), pp. 467–478. [CrossRef] [PubMed]
Amin, D. B. , Lawless, I. M. , Sommerfeld, D. , Stanley, R. M. , Ding, B. , and Costi, J. J. , 2015, “ Effect of Potting Technique on the Measurement of Six Degree-of-Freedom Viscoelastic Properties of Human Lumbar Spine Segments,” ASME J. Biomech. Eng., 137(5), p. 054501. [CrossRef]
Zirbel, S. A. , Stolworthy, D. K. , Howell, L. L. , and Bowden, A. E. , 2013, “ Intervertebral Disc Degeneration Alters Lumbar Spine Segmental Stiffness in all Modes of Loading Under a Compressive Follower Load,” Spine J., 13(9), pp. 1134–1147. [CrossRef] [PubMed]
Schmidt, T. A. , An, H. S. , Lim, T. H. , Nowicki, B. H. , and Haughton, V. M. , 1998, “ The Stiffness of Lumbar Spinal Motion Segments With a High-Intensity Zone in the Anulus Fibrosus,” Spine, 23(20), pp. 2167–2173. [CrossRef] [PubMed]
Haughton, V. M. , Lim, T. H. , and An, H. , 1999, “ Intervertebral Disk Appearance Correlated With Stiffness of Lumbar Spinal Motion Segments,” AJNR Am. J. Neuroradiol., 20(6), pp. 1161–1165. [PubMed]
Garges, K. J. , Nourbakhsh, A. , Morris, R. , Yang, J. , Mody, M. , and Patterson, R. , 2008, “ A Comparison of the Torsional Stiffness of the Lumbar Spine in Flexion and Extension,” J. Manipulat. Physiol. Ther., 31(8), pp. 1–7. [CrossRef]
Brown, M. D. , Holmes, D. C. , and Heiner, A. D. , 2002, “ Measurement of Cadaver Lumbar Spine Motion Segment Stiffness,” Spine, 27(9), pp. 918–922. [CrossRef] [PubMed]
Miller, J. A. , Schultz, A. B. , Warwick, D. N. , and Spencer, D. L. , 1986, “ Mechanical Properties of Lumbar Spine Motion Segments Under Large Loads,” J. Biomech., 19(1), pp. 79–84. [CrossRef] [PubMed]
Bisschop, A. , Mullender, M. G. , Kingma, I. , Jiya, T. U. , van der Veen, A. J. , Roos, J. C. , van Dieën, J. H. , and van Royen, B. J. , 2011, “ The Impact of Bone Mineral Density and Disc Degeneration on Shear Strength and Stiffness of the Lumbar Spine Following Laminectomy,” Eur. Spine J., 21(3), pp. 530–536. [CrossRef] [PubMed]
Bisschop, A. , van Royen, B. J. , Mullender, M. G. , Paul, C. P. L. , Kingma, I. , Jiya, T. U. , van der Veen, A. J. , and van Dieën, J. H. , 2012, “ Which Factors Prognosticate Spinal Instability Following Lumbar Laminectomy?,” Eur. Spine J., 21(12), pp. 2640–2648. [CrossRef] [PubMed]
Cassidy, J. J. , Hiltner, A. , and Baer, E. , 1989, “ Hierarchical Structure of the Intervertebral Disc,” Connect. Tissue Res., 23(1), pp. 75–88. [CrossRef] [PubMed]
Ebara, S. , Iatridis, J. C. , Setton, L. A. , Foster, R. J. , Mow, V. C. , and Weidenbaum, M. , 1996, “ Tensile Properties of Nondegenerate Human Lumbar Anulus Fibrosus,” Spine, 21(4), pp. 452–461. [CrossRef] [PubMed]
Isaacs, J. L. , Vresilovic, E. , Sarkar, S. , and Marcolongo, M. , 2014, “ Role of Biomolecules on Annulus Fibrosus Micromechanics_ Effect of Enzymatic Digestion on Elastic and Failure Properties,” J. Mech. Behav. Biomed. Mater., 40(C), pp. 75–84. [CrossRef] [PubMed]
O'Connell, G. D. , Guerin, H. L. , and Elliott, D. M. , 2009, “ Theoretical and Uniaxial Experimental Evaluation of Human Annulus Fibrosus Degeneration,” ASME J. Biomech. Eng., 131(11), p. 111007. [CrossRef]
Elliott, D. M. , and Setton, L. A. , 2001, “ Anisotropic and Inhomogeneous Tensile Behavior of the Human Anulus Fibrosus: Experimental Measurement and Material Model Predictions,” ASME J. Biomech. Eng., 123(3), p. 256. [CrossRef]
Shan, Z. , Li, S. , Liu, J. , Mamuti, M. , Wang, C. , and Zhao, F. , 2015, “ Correlation Between Biomechanical Properties of the Annulus Fibrosus and Magnetic Resonance Imaging (MRI) Findings,” Eur. Spine J., 24(9), pp. 1909–1916. [CrossRef] [PubMed]
O'Connell, G. D. , Sen, S. , and Elliott, D. M. , 2012, “ Human Annulus Fibrosus Material Properties From Biaxial Testing and Constitutive Modeling are Altered With Degeneration,” Biomech. Model. Mechanobiol., 11(3–4), pp. 493–503. [CrossRef] [PubMed]
Bass, E. C. , Ashford, F. A. , Segal, M. R. , and Lotz, J. C. , 2004, “ Biaxial Testing of Human Annulus Fibrosus and its Implications for a Constitutive Formulation,” Ann. Biomed. Eng., 32(9), pp. 1231–1242. [CrossRef] [PubMed]
Skaggs, D. L. , Weidenbaum, M. , Iatridis, J. C. , Ratcliffe, A. , and Mow, V. C. , 1994, “ Regional Variation in Tensile Properties and Biochemical Composition of the Human Lumbar Anulus Fibrosus,” Spine, 19(12), pp. 1310–1319. [CrossRef] [PubMed]
Holzapfel, G. A. , Schulze-Bauer, C. A. J. , Feigl, G. , and Regitnig, P. , 2004, “ Single Lamellar Mechanics of the Human Lumbar Anulus Fibrosus,” Biomech. Model. Mechanobiol., 3(3), pp. 125–140. [CrossRef] [PubMed]
Stemper, B. D. , Baisden, J. L. , Yoganandan, N. , Shender, B. S. , and Maiman, D. J. , 2014, “ Mechanical Yield of the Lumbar Annulus: A Possible Contributor to Instability,” J. Neurosurg.: Spine, 21(4), pp. 608–613. [CrossRef] [PubMed]
Acaroglu, E. R. , Iatridis, J. C. , Setton, L. A. , Foster, R. J. , Mow, V. C. , and Weidenbaum, M. , 1995, “ Degeneration and Aging Affect the Tensile Behavior of Human Lumbar Anulus Fibrosus,” Spine, 20(24), pp. 2690–2701. [CrossRef] [PubMed]
Best, B. A. , Guilak, F. , Setton, L. A. , Zhu, W. , Saed-Nejad, F. , Ratcliffe, A. , Weidenbaum, M. , and Mow, V. C. , 1994, “ Compressive Mechanical Properties of the Human Anulus Fibrosus and Their Relationship to Biochemical Composition,” Spine, 19(2), pp. 212–221. [CrossRef] [PubMed]
Iatridis, J. C. , Setton, L. A. , Foster, R. J. , Rawlins, B. A. , Weidenbaum, M. , and Mow, V. C. , 1998, “ Degeneration Affects the Anisotropic and Nonlinear Behaviors of Human Anulus Fibrosus in Compression,” J. Biomech., 31(6), pp. 535–544. [CrossRef] [PubMed]
Antoniou, J. , Epure, L. M. , Michalek, A. J. , Grant, M. P. , Iatridis, J. C. , and Mwale, F. , 2013, “ Analysis of Quantitative Magnetic Resonance Imaging and Biomechanical Parameters on Human Discs With Different Grades of Degeneration,” J. Magn. Reson. Imaging, 38(6), pp. 1402–1414. [CrossRef] [PubMed]
Freeman, A. L. , Buttermann, G. R. , Beaubien, B. P. , and Rochefort, W. E. , 2013, “ Compressive Properties of Fibrous Repair Tissue Compared to Nucleus and Annulus,” J. Biomech., 46(10), pp. 1714–1721. [CrossRef] [PubMed]
Iatridis, J. C. , Kumar, S. , Foster, R. J. , Weidenbaum, M. , and Mow, V. C. , 1999, “ Shear Mechanical Properties of Human Lumbar Annulus Fibrosus,” J. Orthop. Res., 17(5), pp. 732–737. [CrossRef] [PubMed]
Guerin, H. A. L. , and Elliott, D. M. , 2006, “ Degeneration Affects the Fiber Reorientation of Human Annulus Fibrosus Under Tensile Load,” J. Biomech., 39(8), pp. 1410–1418. [CrossRef] [PubMed]
Fujita, Y. , Wagner, D. R. , Biviji, A. A. , Duncan, N. A. , and Lotz, J. C. , 2000, “ Anisotropic Shear Behavior of the Annulus Fibrosus: Effect of Harvest Site and Tissue Prestrain,” Med. Eng. Phys., 22(5), pp. 349–357. [CrossRef] [PubMed]
Wagner, D. R. , and Lotz, J. C. , 2004, “ Theoretical Model and Experimental Results for the Nonlinear Elastic Behavior of Human Annulus Fibrosus,” J. Orthop. Res., 22(4), pp. 901–909. [CrossRef] [PubMed]
Green, T. P. , Adams, M. A. , and Dolan, P. , 1993, “ Tensile Properties of the Annulus Fibrosus II. Ultimate Tensile Strength and Fatigue Life,” Eur. Spine J., 2(4), pp. 209–214. [CrossRef] [PubMed]
Fujita, Y. , Duncan, N. A. , and Lotz, J. C. , 1997, “ Radial Tensile Properties of the Lumbar Annulus Fibrosus are Site and Degeneration Dependent,” J. Orthop. Res., 15(6), pp. 814–819. [CrossRef] [PubMed]
Sen, S. , Jacobs, N. T. , Boxberger, J. I. , and Elliott, D. M. , 2012, “ Human Annulus Fibrosus Dynamic Tensile Modulus Increases With Degeneration,” Mech. Mater., 44, pp. 93–98. [CrossRef] [PubMed]
Cortes, D. H. , Jacobs, N. T. , DeLucca, J. F. , and Elliott, D. M. , 2014, “ Elastic, Permeability and Swelling Properties of Human Intervertebral Disc Tissues: A Benchmark for Tissue Engineering,” J. Biomech., 47(9), pp. 2088–2094. [CrossRef] [PubMed]
Bron, J. L. , van der Veen, A. J. , Helder, M. N. , van Royen, B. J. , and Smit, T. H. , 2010, “ Biomechanical and In Vivo Evaluation of Experimental Closure Devices of the Annulus Fibrosus Designed for a Goat Nucleus Replacement Model,” Eur. Spine J, 19(8), pp. 1347–1355. [CrossRef] [PubMed]
Nerurkar, N. L. , Elliott, D. M. , and Mauck, R. L. , 2007, “ Mechanics of Oriented Electrospun Nanofibrous Scaffolds for Annulus Fibrosus Tissue Engineering,” J. Orthop. Res., 25(8), pp. 1018–1028. [CrossRef] [PubMed]
Nerurkar, N. L. , Baker, B. M. , Sen, S. , Wible, E. E. , Elliott, D. M. , and Mauck, R. L. , 2009, “ Nanofibrous Biologic Laminates Replicate the Form and Function of the Annulus Fibrosus,” Nat. Mater., 8(12), pp. 986–992. [CrossRef] [PubMed]
Nerurkar, N. L. , Han, W. , Mauck, R. L. , and Elliott, D. M. , 2011, “ Homologous Structure–Function Relationships Between Native Fibrocartilage and Tissue Engineered From MSC-Seeded Nanofibrous Scaffolds,” Biomaterials, 32(2), pp. 461–468. [CrossRef] [PubMed]
Nerurkar, N. L. , Sen, S. , Baker, B. M. , Elliott, D. M. , and Mauck, R. L. , 2011, “ Dynamic Culture Enhances Stem Cell Infiltration and Modulates Extracellular Matrix Production on Aligned Electrospun Nanofibrous Scaffolds,” Acta Biomater., 7(2), pp. 485–491. [CrossRef] [PubMed]
Koepsell, L. , Remund, T. , Bao, J. , Neufeld, D. , Fong, H. , and Deng, Y. , 2011, “ Tissue Engineering of Annulus Fibrosus Using Electrospun Fibrous Scaffolds With Aligned Polycaprolactone Fibers,” J. Biomed. Mater. Res., 99A(4), pp. 564–575. [CrossRef]
Yeganegi, M. , Kandel, R. A. , and Santerre, J. P. , 2010, “ Characterization of a Biodegradable Electrospun Polyurethane Nanofiber Scaffold: Mechanical Properties and Cytotoxicity,” Acta Biomater., 6(10), pp. 3847–3855. [CrossRef] [PubMed]
Wismer, N. , Grad, S. , Fortunato, G. , Ferguson, S. J. , Alini, M. , and Eglin, D. , 2014, “ Biodegradable Electrospun Scaffolds for Annulus Fibrosus Tissue Engineering: Effect of Scaffold Structure and Composition on Annulus Fibrosus Cells In Vitro,” Tissue Eng., Part A, p. 140123085256009.
Turner, K. G. , Ahmed, N. , Santerre, J. P. , and Kandel, R. A. , 2014, “ Modulation of Annulus Fibrosus Cell Alignment and Function on Oriented Nanofibrous Polyurethane Scaffolds Under Tension,” Spine J., 14(3), pp. 424–434. [CrossRef] [PubMed]
Sharifi, S. , van Kooten, T. G. , Kranenburg, H.-J. C. , Meij, B. P. , Behl, M. , Lendlein, A. , and Grijpma, D. W. , 2013, “ An Annulus Fibrosus Closure Device Based on a Biodegradable Shape-Memory Polymer Network,” Biomaterials, 34(33), pp. 8105–8113. [CrossRef] [PubMed]
Vernengo, J. , Fussell, G. W. , Smith, N. G. , and Lowman, A. M. , 2010, “ Synthesis and Characterization of Injectable Bioadhesive Hydrogels for Nucleus Pulposus Replacement and Repair of the Damaged Intervertebral Disc,” J. Biomed. Mater. Res., 93B(2), pp. 309–317. [CrossRef]
Cho, H. , Park, S.-H. , Park, K. , Shim, J. W. , Huang, J. , Smith, R. , Elder, S. , Min, B.-H. , and Hasty, K. A. , 2013, “ Construction of a Tissue-Engineered Annulus Fibrosus,” Artif. Organs, 37(7), pp. E131–E138. [CrossRef] [PubMed]
Martin, J. T. , Milby, A. H. , Chiaro, J. A. , Kim, D. H. , Hebela, N. M. , Smith, L. J. , Elliott, D. M. , and Mauck, R. L. , 2014, “ Translation of an EngineeredNanofibrous Disc-Like Angle-Ply Structure for Intervertebral Disc Replacement in a Small Animal Model,” Acta Biomater., 10(6), pp. 2473–2481. [CrossRef] [PubMed]
Driscoll, T. P. , Nerurkar, N. L. , Jacobs, N. T. , Elliott, D. M. , and Mauck, R. L. , 2011, “ Fiber Angle and Aspect Ratio Influence the Shear Mechanics of Oriented Electrospun Nanofibrous Scaffolds,” J. Mech. Behav. Biomed. Mater., 4(8), pp. 1627–1636. [CrossRef] [PubMed]
Schek, R. M. , Michalek, A. J. , and Iatridis, J. C. , 2011, “ Genipin-Crosslinked Fibrin Hydrogels as a Potential Adhesive to Augment Intervertebral Disc Annulus Repair,” Eur. Cell Mater., 21, pp. 373–383. [PubMed]
Guterl, C. C. , Torre, O. M. , Purmessur, D. , Khyati, D. , Likhitpanichkul, M. , Hecht, A. C. , Nicoll, S. B. , and Iatridis, J. C. , 2014, “ Characterization of Mechanics and Cytocompatibility of Fibrin-Genipin Annulus Fibrosus Sealant With the Addition of Cell Adhesion Molecules,” Tissue Eng. Part A, 20(17–18), p. 140506130038007.
Jeong, C. G. , Francisco, A. T. , Niu, Z. , Mancino, R. L. , Craig, S. L. , and Setton, L. A. , 2014, “ Screening of Hyaluronic Acid–Poly(Ethylene Glycol) Composite Hydrogels to Support Intervertebral Disc Cell Biosynthesis Using Artificial Neural Network Analysis,” Acta Biomater., 10(8), pp. 3421–3430. [CrossRef] [PubMed]
Nerurkar, N. L. , Mauck, R. L. , and Elliott, D. M. , 2008, “ ISSLS Prize Winner: Integrating Theoretical and Experimental Methods for Functional Tissue Engineering of the Annulus Fibrosus,” Spine, 33(25), pp. 2691–2701. [CrossRef] [PubMed]
Wan, Y. , Feng, G. , Shen, F. H. , Balian, G. , Laurencin, C. T. , and Li, X. , 2007, “ Novel Biodegradable Poly(1,8-octanediol malate) for Annulus Fibrosus Regeneration,” Macromol. Biosci., 7(11), pp. 1217–1224. [CrossRef] [PubMed]
Wiltsey, C. , Christiani, T. , Williams, J. , Scaramazza, J. , Van Sciver, C. , Toomer, K. , Sheehan, J. , Branda, A. , Nitzl, A. , England, E. , Kadlowec, J. , Iftode, C. , and Vernengo, J. , 2015, “ Thermogelling Bioadhesive Scaffolds for Intervertebral Disk Tissue Engineering: Preliminary In Vitro Comparison of Aldehyde-Based Versus Alginate Microparticle-Mediated Adhesion,” Acta Biomater., 16, pp. 71–80. [CrossRef] [PubMed]
Jiao, Y. , Gyawali, D. , Stark, J. M. , Akcora, P. , Nair, P. , Tran, R. T. , and Yang, J. , 2012, “ A Rheological Study of Biodegradable Injectable PEGMC/HA Composite Scaffolds,” Soft Matter, 8(5), pp. 1499–1507. [CrossRef] [PubMed]
Sitterle, V. B. , Sun, W. , and Levenston, M. E. , 2008, “ A Modified Lap Test to More Accurately Estimate Interfacial Shear Strength for Bonded Tissues,” J. Biomech., 41(15), pp. 3260–3264. [CrossRef] [PubMed]
Maher, S. A. , Mauck, R. L. , Rackwitz, L. , and Tuan, R. S. , 2010, “ A Nano-Fibrous Cell Seeded Hydrogel Promotes Integration in a Cartilage Gap Model,” J. Anat., 4(1), pp. 25–29.
Iatridis, J. C. , and ap Gwynn, I. , 2004, “ Mechanisms for Mechanical Damage in the Intervertebral Disc Annulus Fibrosus,” J. Biomech., 37(8), pp. 1165–1175. [CrossRef] [PubMed]
Vergroesen, P.-P. A. , Bochyn ska, A. I. , Emanuel, K. S. , Sharifi, S. , Kingma, I. , Grijpma, D. W. , and Smit, T. H. , 2015, “ A Biodegradable Glue for Annulus Closure,” Spine, 40(9), pp. 622–628. [CrossRef] [PubMed]
Long, R. G. , Buerki, A. , Zysset, P. , Eglin, D. , Grijpma, D. W. , Blanquer, S. B. G. , Hecht, A. C. , and Iatridis, J. C. , 2015, “ Mechanical Restoration and Failure Analyses of Composite Repair Strategy for Annulus Fibrosus,” Acta Biomater., 30, pp. 116–125. [CrossRef] [PubMed]
Gantenbein, B. , Illien-Jünger, S. , Chan, S. , Walser, J. , Haglund, L. , Ferguson, S. J. , Iatridis, J. C. , and Grad, S. , 2015, “ Organ Culture Bioreactors-Platforms to Study Human Intervertebral Disc Degeneration and Regenerative Therapy,” Curr. Stem Cell Res. Ther., 31(23), pp. 339–352. [CrossRef]
Gawri, R. , Mwale, F. , Ouellet, J. , Roughley, P. J. , Steffen, T. , Antoniou, J. , and Haglund, L. , 2011, “ Development of an Organ Culture System for Long-Term Survival of the Intact Human Intervertebral Disc,” Spine, 36(22), pp. 1835–1842. [CrossRef] [PubMed]
Walter, B. A. , Illien-Junger, S. , Nasser, P. R. , Hecht, A. C. , and Iatridis, J. C. , 2014, “ Development and Validation of a Bioreactor System for Dynamic Loading and Mechanical Characterization of Whole Human Intervertebral Discs in Organ Culture,” J. Biomech., 47(9), pp. 2095–2101. [CrossRef] [PubMed]
Haglund, L. , Moir, J. , Beckman, L. , Mulligan, K. R. , Jim, B. , Ouellet, J. A. , Roughley, P. , and Steffen, T. , 2011, “ Development of a Bioreactor for Axially Loaded Intervertebral Disc Organ Culture,” Tissue Eng. Part C, 17(10), pp. 1011–1019. [CrossRef]
O'Connell, G. D. , Vresilovic, E. J. , and Elliott, D. M. , 2007, “ Comparison of Animals Used in Disc Research to Human Lumbar Disc Geometry,” Spine, 32(3), pp. 328–333. [CrossRef] [PubMed]
Wang, S. , Park, W. M. , Kim, Y. H. , Cha, T. , Wood, K. , and Li, G. , 2014, “ In Vivo Loads in the Lumbar L3–4 Disc During a Weight Lifting Extension,” Clin. Biomech. (Bristol, Avon)., 29(2), pp. 155–160. [CrossRef] [PubMed]
Michalek, A. J. , Funabashi, K. L. , and Iatridis, J. C. , 2010, “ Needle Puncture Injury of the Rat Intervertebral Disc Affects Torsional and Compressive Biomechanics Differently,” Eur. Spine J., 19(12), pp. 2110–2116. [CrossRef] [PubMed]

Figures

Grahic Jump Location
Fig. 1

Intradiscal pressure increases on average 3.4 and 2.7 times in sitting and standing postures from lying prone (0.223 MPa), respectively. Marker size indicates number of samples in each study with Wilke having one and Quinnell having forty. Label indicates first author and publication year of study. Error bars indicate the total range of values found in the study. Range data not available for studies indicated by markers without error bars. Values from Refs. [29] and [3336] were multiplied by 0.0981 to convert from kg/cm2 to MPa. [2839].

Grahic Jump Location
Fig. 2

Tensile moduli values reported for human AF with different orientation (C = cirumferential; R = radial; and A = axial) and for single lamella and multiple lamellae samples. Tensile moduli are reported as the linear Young's moduli values from Refs. [9094], [97100], [106], and [107].

Grahic Jump Location
Fig. 3

Testing paradigm for evaluating IVD repair strategies. Screening tests involve high through-put evaluations that can rapidly assess materials. Testing process progresses to in vivo validation.

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