Volume Changes After Traumatic Spinal Cord Injury in Animal Studies-A Systematic Review
-
Mahdi Sharif-Alhoseini
,
Fariba Vahedi
,
Mahmoud Omidbeigi
,
Marzieh Sharifi
,
Zahra Hassannejad
,
Shayan Abdollah Zadegan
,
Motahareh Rezvan
,
Mona Mokhatab
,
Kiavash Sajadi
,
Aida Shakouri-Motlagh
,
Farhad Shokraneh
,
Alexander R. Vaccaro
,
Vafa Rahimi Movaghar
Abstract
There are limited data on the lesion volume changes following spinal cord injury (SCI). In this study, a meta-analysis was performed to evaluate the volume size changes of the injured spinal cord over time among animal studies in traumatic SCI. Following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines, we conducted a comprehensive electronic search of English literature of PubMed and EMBASE databases from 1946 to 2015 concerning the time-dependent changes in the volume of the spinal cord following mechanical traumatic SCI. A hand-search was also performed for non-interventional, non-molecular, and non-review studies. Quality appraisal, data extraction, qualitative and quantitative analyses were performed afterward. Of 11,561 articles yielded from electronic search, 49 articles were assessed for eligibility after reviewing of titles, abstracts, and references. Ultimately, 11 articles were eligible for quantitative synthesis. The ratio of lesion volume to spinal cord total volume increased over time. Avascularity appeared in spinal cord 4 hours after injury. During the first week, the spinal subarachnoid space decreased. The hemorrhagic lesion size peaked in 1 week and decreased thereafter. Significant loss of gray and white matter occurred from day 3 with a slower progression of white matter damage. Changes of lesion extent over time is critical in pathophysiologic processes after SCI. Early avascularity, rapid loss of gray matter, slow progression of white matter damage, and late cavitation are the pathophysiologic key points of SCI, which could be helpful in choosing the proper intervention on a timely basis.
1. Ek CJ, Habgood MD, Callaway JK, Dennis R, Dziegielewska KM, Johansson PA, Potter A, Wheaton B, Saunders NR. Spatio-temporal progression of grey and white matter damage following contusion injury in rat spinal cord. PloS one 2010 Aug 9;5(8):e12021.
2. Gensel JC, Tovar CA, Hamers FP, Deibert RJ, Beattie MS, Bresnahan JC. Behavioral and histological characterization of unilateral cervical spinal cord contusion injury in rats. J Neurotrauma 2006 Jan 1;23(1):36-54.
3. Dusart I, Schwab ME. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci 1994 May;6(5):712-24.
4. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 2010 Jan 1;8(5):336-41.
5. Fujiki M, Furukawa Y, Kobayashi H, Abe T, Ishii K, Uchida S, Kamida T. Geranylgeranylacetone limits secondary injury, neuronal death, and progressive necrosis and cavitation after spinal cord injury. Brain Res 2005 Aug 16;1053(1-2):175-84.
6. Kuluz J, Samdani A, Benglis D, Gonzalez-Brito M, Solano JP, Ramirez MA, Luqman A, Santos RD, Hutchinson D, Nares M, Padgett K. Pediatric spinal cord injury in infant piglets: description of a new large animal model and review of the literature. J Spinal Cord Med 2010 Jan 1;33(1):43-57.
7. Noble LJ, Wrathall JR. Spinal cord contusion in the rat: morphometric analyses of alterations in the spinal cord. Exp Neurol 1985 Apr 1;88(1):135-49.
8. Hassannejad Z, Sharif-Alhoseini M, Shakouri-Motlagh A, Vahedi F, Zadegan SA, Mokhatab M, Rezvan M, Saadat S, Shokraneh F, Rahimi-Movaghar V. Potential variables affecting the quality of animal studies regarding pathophysiology of traumatic spinal cord injuries. Spinal Cord 2016 Aug;54(8):579.
9. Andrade MS, Hanania FR, Daci K, Leme RJ, Chadi G. Contuse lesion of the rat spinal cord of moderate intensity leads to a higher time-dependent secondary neurodegeneration than severe one: An open-window for experimental neuroprotective interventions. Tissue and Cell 2008 Apr 1;40(2):143-56.
10. Bose P, Parmer R, Reier PJ, Thompson FJ. Morphological changes of the soleus motoneuron pool in chronic midthoracic contused rats. Exp Neurol 2005 Jan 1;191(1):13-23.
11. Byrnes KR, Fricke ST, Faden AI. Neuropathological differences between rats and mice after spinal cord injury. J Magn Reson Imaging 2010 Oct;32(4):836-46.
12. Ellingson BM, Schmit BD, Kurpad SN. Lesion growth and degeneration patterns measured using diffusion tensor 9.4-T magnetic resonance imaging in rat spinal cord injury. J Neurosurg Spine 2010 Aug;13(2):181-92.
13. Finkelstein SD, Gillespie JA, Markowitz RS, Johnson DD, Black P. Experimental spinal cord injury: qualitative and quantitative histopathologic evaluation. J Neurotrauma 1990;7(1):29-40.
14. Grossman SD, Rosenberg LJ, Wrathall JR. Temporal–spatial pattern of acute neuronal and glial loss after spinal cord contusion. Exp Neurol 2001 Apr 1;168(2):273-82.
15. Hill CE, Beattie MS, Bresnahan JC. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp Neurol 2001 Sep 1;171(1):153-69.
16. Hu R, Zhou J, Luo C, Lin J, Wang X, Li X, Bian X, Li Y, Wan Q, Yu Y, Feng H. Glial scar and neuroregeneration: histological, functional, and magnetic resonance imaging analysis in chronic spinal cord injury. J Neurosurg Spine 2010 Aug;13(2):169-80.
17. Steencken AC, Stelzner DJ. Loss of propriospinal neurons after spinal contusion injury as assessed by retrograde labeling. Neuroscience 2010 Oct 27;170(3):971-80.
18. Zai LJ, Wrathall JR. Cell proliferation and replacement following contusive spinal cord injury. Glia 2005 May;50(3):247-57.
19. Metz GA, Curt A, Van De Meent H, Klusman I, Schwab ME, Dietz V. Validation of the weight-drop contusion model in rats: a comparative study of human spinal cord injury. J Neurotrauma 2000 Jan;17(1):1-7.
20. Liu XZ, Xu XM, Hu R, Du C, Zhang SX, McDonald JW, Dong HX, Wu YJ, Fan GS, Jacquin MF, Hsu CY. Neuronal and glial apoptosis after traumatic spinal cord injury. J Neurosci 1997 Jul 15;17(14):5395-406.
21. Zhang Z, Guth L. Experimental spinal cord injury: Wallerian degeneration in the dorsal column is followed by revascularization, glial proliferation, and nerve regeneration. Exp Neurol 1997 Sep 1;147(1):159-71.
22. Koyanagi I, Tator CH, Lea PJ. Three-dimensional analysis of the vascular system in the rat spinal cord with scanning electron microscopy of vascular corrosion casts. Part 2: Acute spinal cord injury. Neurosurgery 1993 Aug 1;33(2):285-92.
23. Shibuya S, Miyamoto O, Itano T, Mori S, Norimatsu H. Temporal progressive antigen expression in radial glia after contusive spinal cord injury in adult rats. Glia 2003 Apr 15;42(2):172-83.
24. Ek CJ, Habgood MD, Dennis R, Dziegielewska KM, Mallard C, Wheaton B, Saunders NR. Pathological changes in the white matter after spinal contusion injury in the rat. PloS one 2012 Aug 29;7(8):e43484.
25. Pearse DD, Lo Jr TP, Cho KS, Lynch MP, Garg MS, Marcillo AE, Sanchez AR, Cruz Y, Dietrich WD. Histopathological and behavioral characterization of a novel cervical spinal cord displacement contusion injury in the rat. J Neurotrauma 2005 Jun 1;22(6):680-702.
26. Narayana PA, Grill RJ, Chacko T, Vang R. Endogenous recovery of injured spinal cord: longitudinal in vivo magnetic resonance imaging. J Neurosci Res 2004 Dec 1;78(5):749-59.
27. Reyes-Alva HJ, Franco-Bourland RE, Martinez-Cruz A, Grijalva I, Madrazo I, Guizar-Sahagun G. Spatial and temporal morphological changes in the subarachnoid space after graded spinal cord contusion in the rat. J Neurotrauma 2013 Jun 15;30(12):1084-91.
28. Lonjon N, Kouyoumdjian P, Prieto M, Bauchet L, Haton H, Gaviria M, Privat A, Perrin FE. Early functional outcomes and histological analysis after spinal cord compression injury in rats. J Neurosurg Spine 2010 Jan;12(1):106-13.
29. Vaughn CN, Iafrate JL, Henley JB, Stevenson EK, Shlifer IG, Jones TB. Cellular neuroinflammation in a lateral forceps compression model of spinal cord injury. Anat Rec 2013 Aug;296(8):1229-46.
30. Moriarty LJ, Duerstock BS, Bajaj CL, Lin K, Borgens RB. Two-and three-dimensional computer graphic evaluation of the subacute spinal cord injury. J Neurol Sci 1998 Mar 5;155(2):121-37.
31. Guizar-Sahagun G, Grijalva I, Madrazo I, Franco-Bourland R, Salgado H, Ibarra A, Oliva E, Zepeda A. Development of post-traumatic cysts in the spinal cord of rats subjected to severe spinal cord contusion. World Neurosurg 1994 Mar 1;41(3):241-9.
32. Fairholm DJ, Turnbull IM. Microangiographic study of experimental spinal cord injuries. J Neurosurg 1971 Sep;35(3):277-86.
33. Brennan FH, Cowin GJ, Kurniawan ND, Ruitenberg MJ. Longitudinal assessment of white matter pathology in the injured mouse spinal cord through ultra-high field (16.4 T) in vivo diffusion tensor imaging. Neuroimage 2013 Nov 15;82:574-85.
34. Blomster LV, Cowin GJ, Kurniawan ND, Ruitenberg MJ. Detection of endogenous iron deposits in the injured mouse spinal cord through high‐resolution ex vivo and in vivo MRI. NMR Biomed 2013 Feb;26(2):141-50.
35. Kuhn PL, Wrathall JR. A mouse model of graded contusive spinal cord injury. J Neurotrauma 1998 Feb;15(2):125-40.
36. Blight AR. Morphometric analysis of a model of spinal cord injury in guinea pigs, with behavioral evidence of delayed secondary pathology. J Neurol Sci 1991 Jun 1;103(2):156-71.
37. Lane MA, Truettner JS, Brunschwig JP, Gomez A, Bunge MB, Dietrich WD, Dziegielewska KM, Ek CJ, Vandeberg JL, Saunders NR. Age‐related differences in the local cellular and molecular responses to injury in developing spinal cord of the opossum, Monodelphis domestica. Eur J Neurosci 2007 Mar;25(6):1725-42.
38. Vink R, Noble LJ, Knoblach SM, Bendall MR, Faden AI. Metabolic changes in rabbit spinal cord after trauma: magnetic resonance spectroscopy studies. Ann Neurol 1989 Jan;25(1):26-31.
39. Gledhill RF, Harrison BM, McDonald WI. Demyelination and remyelination after acute spinal cord compression. Exp Neurol 1973 Mar 1;38(3):472-87.
40. Bresnahan JC. An electron-microscopic analysis of axonal alterations following blunt contusion of the spinal cord of the rhesus monkey (Macaca mulatta). J Neurological Sci 1978 Jun 1;37(1):59-82.
41. Carlson GD, Gorden CD, Oliff HS, Pillai JJ, Lamanna JC. Sustained spinal cord compression: part I: time-dependent effect on long-term pathophysiology. JBJS 2003 Jan 1;85(1):86-94.
42. Anthes DL, Theriault E, Tator CH. Characterization of axonal ultrastructural pathology following experimental spinal cord compression injury. Brain Res 1995 Dec 8;702(1-2):1-6.
43. Blight AR. Delayed demyelination and macrophage invasion: a candidate for secondary cell damage in spinal cord injury. Cent Nerv Syst Trauma 1985;2(4):299-315.
44. Camand E, Morel MP, Faissner A, Sotelo C, Dusart I. Long‐term changes in the molecular composition of the glial scar and progressive increase of serotoninergic fibre sprouting after hemisection of the mouse spinal cord. Eur J Neurosci 2004 Sep;20(5):1161-76.
45. Ditor DS, John S, Cakiroglu J, Kittmer C, Foster PJ, Weaver LC. Magnetic resonance imaging versus histological assessment for estimation of lesion volume after experimental spinal cord injury. J Neurosurg Spine 2008;9:301–6.
46. Griffiths IR. Vasogenic edema following acute and chronic spinal cord compression in the dog. J Neurosurg 1975 Feb;42(2):155-65.
47. Kostyk SK, Popovich PG, Stokes BT, Wei P, Jakeman LB. Robust axonal growth and a blunted macrophage response are associated with impaired functional recovery after spinal cord injury in the MRL/MpJ mouse. Neuroscience 2008 Oct 15;156(3):498-514.
48. Kouyoumdjian P, Lonjon N, Prieto M, Haton H, Privat A, Asencio G, Perrin FE, Gaviria M. A remotely controlled model of spinal cord compression injury in mice: toward real-time analysis. J Neurosurg Spine 2009 Oct;11(4):461-70.
49. Leskovar AL, Moriarty LJ, Turek JJ, Schoenlein IA, Borgens RB. The macrophage in acute neural injury: changes in cell numbers over time and levels of cytokine production in mammalian central and peripheral nervous systems. J Exp Biol 2000 Jun 15;203(12):1783-95.
50. Li GL, Farooque M, Isaksson J, Olsson YN. Changes in synapses and axons demonstrated by synaptophysin immunohistochemistry following spinal cord compression trauma in the rat and mouse. Biomed Environ Sci 2004 Sep;17(3):281-90.
51. Namiki J, Tator CH. Cell proliferation and nestin expression in the ependyma of the adult rat spinal cord after injury. J Neuropathol Exp Neurol 1999 May 1;58(5):489-98.
52. Nout YS, Mihai G, Tovar CA, Schmalbrock P, Bresnahan JC, Beattie MS. Hypertonic saline attenuates cord swelling and edema in experimental spinal cord injury: a study utilizing magnetic resonance imaging. Crit Care Med 2009 Jul;37(7):2160.
53. Poon PC, Gupta D, Shoichet MS, Tator CH. Clip compression model is useful for thoracic spinal cord injuries: histologic and functional correlates. Spine 2007 Dec 1;32(25):2853-9.
54. Swartz KR, Scheff NN, Roberts KN, Fee DB. Exacerbation of spinal cord injury due to static compression occurring early after onset. J Neurosurg Spine 2009 Nov;11(5):570-4.
55. Vessal M, Aycock A, Garton MT, Ciferri M, Darian‐Smith C. Adult neurogenesis in primate and rodent spinal cord: comparing a cervical dorsal rhizotomy with a dorsal column transection. Eur J Neurosci 2007 Nov;26(10):2777-94.
56. Whetstone WD, Hsu JY, Eisenberg M, Werb Z, Noble‐Haeusslein LJ. Blood‐spinal cord barrier after spinal cord injury: Relation to revascularization and wound healing. J Neurosci Res 2003 Oct 15;74(2):227-39.
2. Gensel JC, Tovar CA, Hamers FP, Deibert RJ, Beattie MS, Bresnahan JC. Behavioral and histological characterization of unilateral cervical spinal cord contusion injury in rats. J Neurotrauma 2006 Jan 1;23(1):36-54.
3. Dusart I, Schwab ME. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci 1994 May;6(5):712-24.
4. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 2010 Jan 1;8(5):336-41.
5. Fujiki M, Furukawa Y, Kobayashi H, Abe T, Ishii K, Uchida S, Kamida T. Geranylgeranylacetone limits secondary injury, neuronal death, and progressive necrosis and cavitation after spinal cord injury. Brain Res 2005 Aug 16;1053(1-2):175-84.
6. Kuluz J, Samdani A, Benglis D, Gonzalez-Brito M, Solano JP, Ramirez MA, Luqman A, Santos RD, Hutchinson D, Nares M, Padgett K. Pediatric spinal cord injury in infant piglets: description of a new large animal model and review of the literature. J Spinal Cord Med 2010 Jan 1;33(1):43-57.
7. Noble LJ, Wrathall JR. Spinal cord contusion in the rat: morphometric analyses of alterations in the spinal cord. Exp Neurol 1985 Apr 1;88(1):135-49.
8. Hassannejad Z, Sharif-Alhoseini M, Shakouri-Motlagh A, Vahedi F, Zadegan SA, Mokhatab M, Rezvan M, Saadat S, Shokraneh F, Rahimi-Movaghar V. Potential variables affecting the quality of animal studies regarding pathophysiology of traumatic spinal cord injuries. Spinal Cord 2016 Aug;54(8):579.
9. Andrade MS, Hanania FR, Daci K, Leme RJ, Chadi G. Contuse lesion of the rat spinal cord of moderate intensity leads to a higher time-dependent secondary neurodegeneration than severe one: An open-window for experimental neuroprotective interventions. Tissue and Cell 2008 Apr 1;40(2):143-56.
10. Bose P, Parmer R, Reier PJ, Thompson FJ. Morphological changes of the soleus motoneuron pool in chronic midthoracic contused rats. Exp Neurol 2005 Jan 1;191(1):13-23.
11. Byrnes KR, Fricke ST, Faden AI. Neuropathological differences between rats and mice after spinal cord injury. J Magn Reson Imaging 2010 Oct;32(4):836-46.
12. Ellingson BM, Schmit BD, Kurpad SN. Lesion growth and degeneration patterns measured using diffusion tensor 9.4-T magnetic resonance imaging in rat spinal cord injury. J Neurosurg Spine 2010 Aug;13(2):181-92.
13. Finkelstein SD, Gillespie JA, Markowitz RS, Johnson DD, Black P. Experimental spinal cord injury: qualitative and quantitative histopathologic evaluation. J Neurotrauma 1990;7(1):29-40.
14. Grossman SD, Rosenberg LJ, Wrathall JR. Temporal–spatial pattern of acute neuronal and glial loss after spinal cord contusion. Exp Neurol 2001 Apr 1;168(2):273-82.
15. Hill CE, Beattie MS, Bresnahan JC. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp Neurol 2001 Sep 1;171(1):153-69.
16. Hu R, Zhou J, Luo C, Lin J, Wang X, Li X, Bian X, Li Y, Wan Q, Yu Y, Feng H. Glial scar and neuroregeneration: histological, functional, and magnetic resonance imaging analysis in chronic spinal cord injury. J Neurosurg Spine 2010 Aug;13(2):169-80.
17. Steencken AC, Stelzner DJ. Loss of propriospinal neurons after spinal contusion injury as assessed by retrograde labeling. Neuroscience 2010 Oct 27;170(3):971-80.
18. Zai LJ, Wrathall JR. Cell proliferation and replacement following contusive spinal cord injury. Glia 2005 May;50(3):247-57.
19. Metz GA, Curt A, Van De Meent H, Klusman I, Schwab ME, Dietz V. Validation of the weight-drop contusion model in rats: a comparative study of human spinal cord injury. J Neurotrauma 2000 Jan;17(1):1-7.
20. Liu XZ, Xu XM, Hu R, Du C, Zhang SX, McDonald JW, Dong HX, Wu YJ, Fan GS, Jacquin MF, Hsu CY. Neuronal and glial apoptosis after traumatic spinal cord injury. J Neurosci 1997 Jul 15;17(14):5395-406.
21. Zhang Z, Guth L. Experimental spinal cord injury: Wallerian degeneration in the dorsal column is followed by revascularization, glial proliferation, and nerve regeneration. Exp Neurol 1997 Sep 1;147(1):159-71.
22. Koyanagi I, Tator CH, Lea PJ. Three-dimensional analysis of the vascular system in the rat spinal cord with scanning electron microscopy of vascular corrosion casts. Part 2: Acute spinal cord injury. Neurosurgery 1993 Aug 1;33(2):285-92.
23. Shibuya S, Miyamoto O, Itano T, Mori S, Norimatsu H. Temporal progressive antigen expression in radial glia after contusive spinal cord injury in adult rats. Glia 2003 Apr 15;42(2):172-83.
24. Ek CJ, Habgood MD, Dennis R, Dziegielewska KM, Mallard C, Wheaton B, Saunders NR. Pathological changes in the white matter after spinal contusion injury in the rat. PloS one 2012 Aug 29;7(8):e43484.
25. Pearse DD, Lo Jr TP, Cho KS, Lynch MP, Garg MS, Marcillo AE, Sanchez AR, Cruz Y, Dietrich WD. Histopathological and behavioral characterization of a novel cervical spinal cord displacement contusion injury in the rat. J Neurotrauma 2005 Jun 1;22(6):680-702.
26. Narayana PA, Grill RJ, Chacko T, Vang R. Endogenous recovery of injured spinal cord: longitudinal in vivo magnetic resonance imaging. J Neurosci Res 2004 Dec 1;78(5):749-59.
27. Reyes-Alva HJ, Franco-Bourland RE, Martinez-Cruz A, Grijalva I, Madrazo I, Guizar-Sahagun G. Spatial and temporal morphological changes in the subarachnoid space after graded spinal cord contusion in the rat. J Neurotrauma 2013 Jun 15;30(12):1084-91.
28. Lonjon N, Kouyoumdjian P, Prieto M, Bauchet L, Haton H, Gaviria M, Privat A, Perrin FE. Early functional outcomes and histological analysis after spinal cord compression injury in rats. J Neurosurg Spine 2010 Jan;12(1):106-13.
29. Vaughn CN, Iafrate JL, Henley JB, Stevenson EK, Shlifer IG, Jones TB. Cellular neuroinflammation in a lateral forceps compression model of spinal cord injury. Anat Rec 2013 Aug;296(8):1229-46.
30. Moriarty LJ, Duerstock BS, Bajaj CL, Lin K, Borgens RB. Two-and three-dimensional computer graphic evaluation of the subacute spinal cord injury. J Neurol Sci 1998 Mar 5;155(2):121-37.
31. Guizar-Sahagun G, Grijalva I, Madrazo I, Franco-Bourland R, Salgado H, Ibarra A, Oliva E, Zepeda A. Development of post-traumatic cysts in the spinal cord of rats subjected to severe spinal cord contusion. World Neurosurg 1994 Mar 1;41(3):241-9.
32. Fairholm DJ, Turnbull IM. Microangiographic study of experimental spinal cord injuries. J Neurosurg 1971 Sep;35(3):277-86.
33. Brennan FH, Cowin GJ, Kurniawan ND, Ruitenberg MJ. Longitudinal assessment of white matter pathology in the injured mouse spinal cord through ultra-high field (16.4 T) in vivo diffusion tensor imaging. Neuroimage 2013 Nov 15;82:574-85.
34. Blomster LV, Cowin GJ, Kurniawan ND, Ruitenberg MJ. Detection of endogenous iron deposits in the injured mouse spinal cord through high‐resolution ex vivo and in vivo MRI. NMR Biomed 2013 Feb;26(2):141-50.
35. Kuhn PL, Wrathall JR. A mouse model of graded contusive spinal cord injury. J Neurotrauma 1998 Feb;15(2):125-40.
36. Blight AR. Morphometric analysis of a model of spinal cord injury in guinea pigs, with behavioral evidence of delayed secondary pathology. J Neurol Sci 1991 Jun 1;103(2):156-71.
37. Lane MA, Truettner JS, Brunschwig JP, Gomez A, Bunge MB, Dietrich WD, Dziegielewska KM, Ek CJ, Vandeberg JL, Saunders NR. Age‐related differences in the local cellular and molecular responses to injury in developing spinal cord of the opossum, Monodelphis domestica. Eur J Neurosci 2007 Mar;25(6):1725-42.
38. Vink R, Noble LJ, Knoblach SM, Bendall MR, Faden AI. Metabolic changes in rabbit spinal cord after trauma: magnetic resonance spectroscopy studies. Ann Neurol 1989 Jan;25(1):26-31.
39. Gledhill RF, Harrison BM, McDonald WI. Demyelination and remyelination after acute spinal cord compression. Exp Neurol 1973 Mar 1;38(3):472-87.
40. Bresnahan JC. An electron-microscopic analysis of axonal alterations following blunt contusion of the spinal cord of the rhesus monkey (Macaca mulatta). J Neurological Sci 1978 Jun 1;37(1):59-82.
41. Carlson GD, Gorden CD, Oliff HS, Pillai JJ, Lamanna JC. Sustained spinal cord compression: part I: time-dependent effect on long-term pathophysiology. JBJS 2003 Jan 1;85(1):86-94.
42. Anthes DL, Theriault E, Tator CH. Characterization of axonal ultrastructural pathology following experimental spinal cord compression injury. Brain Res 1995 Dec 8;702(1-2):1-6.
43. Blight AR. Delayed demyelination and macrophage invasion: a candidate for secondary cell damage in spinal cord injury. Cent Nerv Syst Trauma 1985;2(4):299-315.
44. Camand E, Morel MP, Faissner A, Sotelo C, Dusart I. Long‐term changes in the molecular composition of the glial scar and progressive increase of serotoninergic fibre sprouting after hemisection of the mouse spinal cord. Eur J Neurosci 2004 Sep;20(5):1161-76.
45. Ditor DS, John S, Cakiroglu J, Kittmer C, Foster PJ, Weaver LC. Magnetic resonance imaging versus histological assessment for estimation of lesion volume after experimental spinal cord injury. J Neurosurg Spine 2008;9:301–6.
46. Griffiths IR. Vasogenic edema following acute and chronic spinal cord compression in the dog. J Neurosurg 1975 Feb;42(2):155-65.
47. Kostyk SK, Popovich PG, Stokes BT, Wei P, Jakeman LB. Robust axonal growth and a blunted macrophage response are associated with impaired functional recovery after spinal cord injury in the MRL/MpJ mouse. Neuroscience 2008 Oct 15;156(3):498-514.
48. Kouyoumdjian P, Lonjon N, Prieto M, Haton H, Privat A, Asencio G, Perrin FE, Gaviria M. A remotely controlled model of spinal cord compression injury in mice: toward real-time analysis. J Neurosurg Spine 2009 Oct;11(4):461-70.
49. Leskovar AL, Moriarty LJ, Turek JJ, Schoenlein IA, Borgens RB. The macrophage in acute neural injury: changes in cell numbers over time and levels of cytokine production in mammalian central and peripheral nervous systems. J Exp Biol 2000 Jun 15;203(12):1783-95.
50. Li GL, Farooque M, Isaksson J, Olsson YN. Changes in synapses and axons demonstrated by synaptophysin immunohistochemistry following spinal cord compression trauma in the rat and mouse. Biomed Environ Sci 2004 Sep;17(3):281-90.
51. Namiki J, Tator CH. Cell proliferation and nestin expression in the ependyma of the adult rat spinal cord after injury. J Neuropathol Exp Neurol 1999 May 1;58(5):489-98.
52. Nout YS, Mihai G, Tovar CA, Schmalbrock P, Bresnahan JC, Beattie MS. Hypertonic saline attenuates cord swelling and edema in experimental spinal cord injury: a study utilizing magnetic resonance imaging. Crit Care Med 2009 Jul;37(7):2160.
53. Poon PC, Gupta D, Shoichet MS, Tator CH. Clip compression model is useful for thoracic spinal cord injuries: histologic and functional correlates. Spine 2007 Dec 1;32(25):2853-9.
54. Swartz KR, Scheff NN, Roberts KN, Fee DB. Exacerbation of spinal cord injury due to static compression occurring early after onset. J Neurosurg Spine 2009 Nov;11(5):570-4.
55. Vessal M, Aycock A, Garton MT, Ciferri M, Darian‐Smith C. Adult neurogenesis in primate and rodent spinal cord: comparing a cervical dorsal rhizotomy with a dorsal column transection. Eur J Neurosci 2007 Nov;26(10):2777-94.
56. Whetstone WD, Hsu JY, Eisenberg M, Werb Z, Noble‐Haeusslein LJ. Blood‐spinal cord barrier after spinal cord injury: Relation to revascularization and wound healing. J Neurosci Res 2003 Oct 15;74(2):227-39.
| Files | ||
| Issue | Vol 57, No 6 (2019) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/acta.v57i6.1885 | |
| Keywords | ||
| Spinal Cord Injuries Animal Models Pathophysiology | ||
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How to Cite
1.
Sharif-Alhoseini M, Vahedi F, Omidbeigi M, Sharifi M, Hassannejad Z, Abdollah Zadegan S, Rezvan M, Mokhatab M, Sajadi K, Shakouri-Motlagh A, Shokraneh F, R. Vaccaro A, Rahimi Movaghar V. Volume Changes After Traumatic Spinal Cord Injury in Animal Studies-A Systematic Review. Acta Med Iran. 2019;57(6):385-394.
