Structure and mechanical characteristics of spinal dura mater in different segments of sheep’s spine_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

YANG Chengwei ¹ , YANG Xinle ¹ ,  LAN Xu ¹ , ZHANG Hong ² , WANG Ming ³ , ZHANG Yaqiang ¹ , XU Yajie ⁴ , ZHEN Ping ¹

1. Department of Spine Surgery, the 940th Hospital of Joint Logistics Support Force of Chinese PLA, Lanzhou Gansu, 730050, P.R.China;
2. Department of Orthopedics, Hubei Maternal and Child Health Hospital, Wuhan Hubei, 430070, P.R.China;
3. Department of Orthopedics, the Second Hospital of Lanzhou University, Lanzhou Gansu, 730000, P.R.China;
4. Department of Respiratory Medicine, Henan Rong Jun Hospital, Xinxiang Henan, 453000, P.R.China;

Corresponding author：

LAN Xu, Email: lzzyjw@sina.com

Keywords：

Dura mater; structure; mechanical characteristics; sheep

DOI：

10.7507/1002-1892.201807085

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Objective To clarify the structure and biomechanical characteristics of the dura mater of the cervical, thoracic, and lumbar segments of sheep, in order to provide a theoretical reference for the study of artificial dura mater.Methods Five adult male white sheep were sacrificed. The dura mater of C₅, T₁₀, and L₃ planes were obtained. The histological HE staining was used to observe the internal structure and the thickness of dura mater; the inner and outer surfaces morphology of the dura was observed by scanning electron microscopy (SEM); transmission electron microscopy (TEM) was used to observe the internal structure of dura mater and to measure the diameter of collagen fibers in each part of dura mater. The dura mater of C₆, C₇, T₁₁, T₁₂, L₄, and L₅ planes were taken for uniaxial biomechanical test, and modulus of elasticity, tensile strength, and elongation at break were measured.Results HE staining showed that the thickness of the cervical, thoracic, and lumbar dura mater gradually decreased, and the thickness of the dura mater was (268.19±15.91), (198.16±27.25), (103.74±21.54) μm, respectively, and the differences were significant (P<0.05). SEM observation showed that there were more collagen fibers and fewer cells on the inner surface of the dura mater, while more cells were distributed on the outer surface, and the cells on the inner and outer surface were stretched along the longitudinal axis. TEM observation showed that the collagen fibers in the dura mater were interlaced and arranged in layers. The collagen fibers in the lamina were arranged in the same direction, and the collagen fibers between the lamina were arranged vertically. The diameters of collagen fibers in the cervical, thoracic, and lumbar dura mater were (68.04±21.00), (64.54±20.64), (60.36±19.65) nm, respectively, and the differences were not significant (P>0.05). Uniaxial biomechanical tests results showed that there was no significant difference in modulus of elasticity, tensile strength, and elongation at break between the axial and transverse dura mater of the cervical dura mater (P>0.05); the axial data of thoracic and lumbar segments were significantly larger than the transverse data (P<0.05). The axial modulus of elasticity, tensile strength, and elongation at break of the dura mater of the cervical, thoracic, and lumbar dura mater were significantly different (P<0.05) from the transverse ones, and showing a decreasing trend. Among them, the ratio of axial and transverse modulus of elasticity of cervical and thoracic dura were significantly smaller than that of lumbar segment (P<0.05), and there was no significant difference between cervical segments and thoracic segments (P>0.05).Conclusion The thickness of dura mater in sheep decreased gradually from head to tail. There are more collagen fibers and fewer cells on the inner surface of dura mater, while the outer surface of dura mater is covered by cells. The collagen fiberboard layers in the dura mater are arranged alternately, and have obvious anisotropic biomechanical characteristics, and the anisotropic biomechanical characteristics get more significant from the head to the tail.

Citation： YANG Chengwei, YANG Xinle, LAN Xu, ZHANG Hong, WANG Ming, ZHANG Yaqiang, XU Yajie, ZHEN Ping. Structure and mechanical characteristics of spinal dura mater in different segments of sheep’s spine. Chinese Journal of Reparative and Reconstructive Surgery, 2019, 33(2): 232-238. doi: 10.7507/1002-1892.201807085 Copy

1.	Bokka S, Trivedi A. Histopathological study of the outer membrane of the dura mater in chronic sub dural hematoma: Its clinical and radiological correlation. Asian J Neurosurg, 2016, 11(1): 34-38.
2.	Kurpinski K, Patel S. Dura mater regeneration with a novel synthetic, bilayered nanofibrous dural substitute: an experimental study. Nanomedicine (Lond), 2011, 6(2): 325-337.
3.	O’Rahilly R, Müller F. The meninges in human development. J Neuropathol Exp Neurol, 1986, 45(5): 588-608.
4.	Bhimani AD, Denyer S, Esfahani DR, et al. Surgical complications in intradural extramedullary spinal cord tumors-an ACS-NSQIP analysis of spinal cord level and malignancy. World Neurosurg, 2018, 117: e290-e299.
5.	Scantland JT, Gondim MJ, Koivuniemi AS, et al. Primary spinal intradural extraosseous Ewing sarcoma in a pediatric patient: case report and review of the literature. Pediatr Neurosurg, 2018, 53(4): 222-228.
6.	Mortazavi MM, Verma K, Harmon OA, et al. The microanatomy of spinal cord injury: a review. Clin Anat, 2015, 28(1): 27-36.
7.	Runza M, Pietrabissa R, Mantero S, et al. Lumbar dura mater biomechanics: experimental characterization and scanning electron microscopy observations. Anesth Analg, 1999, 88(6): 1317-1321.
8.	Persson C, Evans S, Marsh R, et al. Poisson’s ratio and strain rate dependency of the constitutive behavior of spinal dura mater. Ann Biomed Eng, 2010, 38(3): 975-983.
9.	Patin DJ, Eckstein EC, Harum K, et al. Anatomic and biomechanical properties of human lumbar dura mater. Anesth Analg, 1993, 76(3): 535-540.
10.	Maikos JT, Elias RA, Shreiber DI. Mechanical properties of dura mater from the rat brain and spinal cord. J Neurotrauma, 2008, 25(1): 38-51.
11.	Wilcox RK, Bilston LE, Barton DC, et al. Mathematical model for the viscoelastic properties of dura mater. J Orthop Sci, 2003, 8(3): 432-434.
12.	Mazgajczyk E, Ścigała K, Czyż M, et al. Mechanical properties of cervical dura mater. Acta Bio Biomech, 2012, 14(1): 51-58.
13.	Shetye SS, Deault MM, Puttlitz CM. Biaxial response of ovine spinal cord dura mater. J Mech Behav Biomed Mater, 2014, 34(6): 146-153.
14.	Fink BR, Walker S. Orientation of fibers in human dorsal lumbar dura mater in relation to lumbar puncture. Anesth Analg, 1989, 69(6): 768-772.
15.	Reina MA, Dittmann M, López GA, et al. New perspectives in the microscopic structure of human dura mater in the dorsolumbar region. Reg Anesth, 1997, 22(2): 161-166.
16.	郭兴锋, 侯春林, 窦源东, 等. 几丁糖电纺膜预防脑脊液漏远期效果的实验研究. 中国修复重建外科杂志, 2014, 28(8): 993-997.
17.	Centonze R, Agostini E, Massaccesi S, et al. A novel equine-derived pericardium membrane for dural repair: a preliminary, short-term investigation. Asian J Neurosurg, 2016, 11(3): 201-205.
18.	Arnautovic KI, Kovacevic M. CSF-related complications after intradural spinal tumor surgery: utility of an autologous fat graft. Med Arch, 2016, 70(6): 460-465.
19.	Ma J, Meng J, Simonet M, et al. Biodegradable fibre scaffolds incorporating water-soluble drugs and proteins. J Mater Sci Mater Med, 2015, 26(7): 205.
20.	Sae-Jung S, Apiwatanakul P. Chitosan pad, cellulose membrane, or gelatin sponge for peridural bleeding: an efficacy study on a lumbar laminectomized rat model. Asian Spine J, 2018, 12(2): 195-201.
21.	Sun H, Wang H, Diao Y, et al. Large retrospective study of artificial dura substitute in patients with traumatic brain injury undergo decompressive craniectomy. Brain Behav, 2018, 8(5): e00907.
22.	Marton E, Giordan E, Gioffrè G, et al. Homologous cryopreserved amniotic membrane in the repair of myelomeningocele: preliminary experience. Acta Neurochir (Wien), 2018, 160(8): 1625-1631.
23.	Dafford EE, Anderson PA. Comparison of dural repair techniques. Spine J, 2015, 15(5): 1099-1105.
24.	胡家正, 席孝庄, 陈鲁芹, 等. 颞筋膜修补硬脑膜缺损 48 例. 中国修复重建外科杂志, 1997, 11(1): 45.
25.	LeHuec JC, Sadikki R, Cogniet A, et al. Role of a collagen membrane in adhesion prevention strategy for complex spinal surgeries. Int Orthop, 2015, 39(7): 1383-1390.
26.	张念武, 郭常芬, 牟善宇, 等. 颈侧皮下蒂皮瓣修补多发性脑脊液耳漏一例. 中国修复重建外科杂志, 1998, 12(4): 235.
27.	Gürer B, Kertmen H, Akturk UD, et al. Use of the bovine pericardial patch and fibrin sealant in meningomyelocele closure. Acta Neurochir (Wien), 2014, 156(7): 1345-1350.
28.	Nakano T, Yoshikawa K, Kunieda T, et al. Treatment for infection of artificial dura mater using free fascia lata. J Craniofac Surg, 2014, 25(4): 1252-1255.
29.	Vandenabeele F, Creemers J, Lambrichts I. Ultrastructure of the human spinal arachnoid mater and dura mater. J Anat, 1996, 189(Pt 2): 471-430.
30.	杨成伟, 邓国英, 杨洋, 等. 单层组织工程纤维环取向纳米纤维支架的构建和初步验证. 脊柱外科杂志, 2014, 12(2): 87-91.
31.	Hasler C, Sprecher CM, Milz S. Comparison of the immature sheep spine and the growing human spine: a spondylometric database for growth modulating research. Spine (Phila Pa 1976), 2010, 35(23): E1262-1272.
32.	Sheng SR, Wang XY, Xu HZ, et al. Anatomy of large animal spines and its comparison to the human spine: a systematic review. Eur Spine J, 2010, 19(1): 46-56.

1. Bokka S, Trivedi A. Histopathological study of the outer membrane of the dura mater in chronic sub dural hematoma: Its clinical and radiological correlation. Asian J Neurosurg, 2016, 11(1): 34-38.
2. Kurpinski K, Patel S. Dura mater regeneration with a novel synthetic, bilayered nanofibrous dural substitute: an experimental study. Nanomedicine (Lond), 2011, 6(2): 325-337.
3. O’Rahilly R, Müller F. The meninges in human development. J Neuropathol Exp Neurol, 1986, 45(5): 588-608.
4. Bhimani AD, Denyer S, Esfahani DR, et al. Surgical complications in intradural extramedullary spinal cord tumors-an ACS-NSQIP analysis of spinal cord level and malignancy. World Neurosurg, 2018, 117: e290-e299.
5. Scantland JT, Gondim MJ, Koivuniemi AS, et al. Primary spinal intradural extraosseous Ewing sarcoma in a pediatric patient: case report and review of the literature. Pediatr Neurosurg, 2018, 53(4): 222-228.
6. Mortazavi MM, Verma K, Harmon OA, et al. The microanatomy of spinal cord injury: a review. Clin Anat, 2015, 28(1): 27-36.
7. Runza M, Pietrabissa R, Mantero S, et al. Lumbar dura mater biomechanics: experimental characterization and scanning electron microscopy observations. Anesth Analg, 1999, 88(6): 1317-1321.
8. Persson C, Evans S, Marsh R, et al. Poisson’s ratio and strain rate dependency of the constitutive behavior of spinal dura mater. Ann Biomed Eng, 2010, 38(3): 975-983.
9. Patin DJ, Eckstein EC, Harum K, et al. Anatomic and biomechanical properties of human lumbar dura mater. Anesth Analg, 1993, 76(3): 535-540.
10. Maikos JT, Elias RA, Shreiber DI. Mechanical properties of dura mater from the rat brain and spinal cord. J Neurotrauma, 2008, 25(1): 38-51.
11. Wilcox RK, Bilston LE, Barton DC, et al. Mathematical model for the viscoelastic properties of dura mater. J Orthop Sci, 2003, 8(3): 432-434.
12. Mazgajczyk E, Ścigała K, Czyż M, et al. Mechanical properties of cervical dura mater. Acta Bio Biomech, 2012, 14(1): 51-58.
13. Shetye SS, Deault MM, Puttlitz CM. Biaxial response of ovine spinal cord dura mater. J Mech Behav Biomed Mater, 2014, 34(6): 146-153.
14. Fink BR, Walker S. Orientation of fibers in human dorsal lumbar dura mater in relation to lumbar puncture. Anesth Analg, 1989, 69(6): 768-772.
15. Reina MA, Dittmann M, López GA, et al. New perspectives in the microscopic structure of human dura mater in the dorsolumbar region. Reg Anesth, 1997, 22(2): 161-166.
16. 郭兴锋, 侯春林, 窦源东, 等. 几丁糖电纺膜预防脑脊液漏远期效果的实验研究. 中国修复重建外科杂志, 2014, 28(8): 993-997.
17. Centonze R, Agostini E, Massaccesi S, et al. A novel equine-derived pericardium membrane for dural repair: a preliminary, short-term investigation. Asian J Neurosurg, 2016, 11(3): 201-205.
18. Arnautovic KI, Kovacevic M. CSF-related complications after intradural spinal tumor surgery: utility of an autologous fat graft. Med Arch, 2016, 70(6): 460-465.
19. Ma J, Meng J, Simonet M, et al. Biodegradable fibre scaffolds incorporating water-soluble drugs and proteins. J Mater Sci Mater Med, 2015, 26(7): 205.
20. Sae-Jung S, Apiwatanakul P. Chitosan pad, cellulose membrane, or gelatin sponge for peridural bleeding: an efficacy study on a lumbar laminectomized rat model. Asian Spine J, 2018, 12(2): 195-201.
21. Sun H, Wang H, Diao Y, et al. Large retrospective study of artificial dura substitute in patients with traumatic brain injury undergo decompressive craniectomy. Brain Behav, 2018, 8(5): e00907.
22. Marton E, Giordan E, Gioffrè G, et al. Homologous cryopreserved amniotic membrane in the repair of myelomeningocele: preliminary experience. Acta Neurochir (Wien), 2018, 160(8): 1625-1631.
23. Dafford EE, Anderson PA. Comparison of dural repair techniques. Spine J, 2015, 15(5): 1099-1105.
24. 胡家正, 席孝庄, 陈鲁芹, 等. 颞筋膜修补硬脑膜缺损 48 例. 中国修复重建外科杂志, 1997, 11(1): 45.
25. LeHuec JC, Sadikki R, Cogniet A, et al. Role of a collagen membrane in adhesion prevention strategy for complex spinal surgeries. Int Orthop, 2015, 39(7): 1383-1390.
26. 张念武, 郭常芬, 牟善宇, 等. 颈侧皮下蒂皮瓣修补多发性脑脊液耳漏一例. 中国修复重建外科杂志, 1998, 12(4): 235.
27. Gürer B, Kertmen H, Akturk UD, et al. Use of the bovine pericardial patch and fibrin sealant in meningomyelocele closure. Acta Neurochir (Wien), 2014, 156(7): 1345-1350.
28. Nakano T, Yoshikawa K, Kunieda T, et al. Treatment for infection of artificial dura mater using free fascia lata. J Craniofac Surg, 2014, 25(4): 1252-1255.
29. Vandenabeele F, Creemers J, Lambrichts I. Ultrastructure of the human spinal arachnoid mater and dura mater. J Anat, 1996, 189(Pt 2): 471-430.
30. 杨成伟, 邓国英, 杨洋, 等. 单层组织工程纤维环取向纳米纤维支架的构建和初步验证. 脊柱外科杂志, 2014, 12(2): 87-91.
31. Hasler C, Sprecher CM, Milz S. Comparison of the immature sheep spine and the growing human spine: a spondylometric database for growth modulating research. Spine (Phila Pa 1976), 2010, 35(23): E1262-1272.
32. Sheng SR, Wang XY, Xu HZ, et al. Anatomy of large animal spines and its comparison to the human spine: a systematic review. Eur Spine J, 2010, 19(1): 46-56.

Chinese Journal of Reparative and Reconstructive Surgery

Structure and mechanical characteristics of spinal dura mater in different segments of sheep’s spine

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