Artículo

Garcia-Ovejero, D.; González, S.; Paniagua-Torija, B.; Lima, A.; Molina-Holgado, E.; De Nicola, A.F.; Labombarda, F. "Progesterone reduces secondary damage, preserves white matter, and improves locomotor outcome after spinal cord contusion" (2014) Journal of Neurotrauma. 31(9):857-871
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Abstract:

Progesterone is an anti-inflammatory and promyelinating agent after spinal cord injury, but its effectiveness on functional recovery is still controversial. In the current study, we tested the effects of chronic progesterone administration on tissue preservation and functional recovery in a clinically relevant model of spinal cord lesion (thoracic contusion). Using magnetic resonance imaging, we observed that progesterone reduced both volume and rostrocaudal extension of the lesion at 60 days post-injury. In addition, progesterone increased the number of total mature oligodendrocytes, myelin basic protein immunoreactivity, and the number of axonal profiles at the epicenter of the lesion. Further, progesterone treatment significantly improved motor outcome as assessed using the Basso-Bresnahan-Beattie scale for locomotion and CatWalk gait analysis. These data suggest that progesterone could be considered a promising therapeutical candidate for spinal cord injury. © 2014 Mary Ann Liebert, Inc.

Registro:

Documento: Artículo
Título:Progesterone reduces secondary damage, preserves white matter, and improves locomotor outcome after spinal cord contusion
Autor:Garcia-Ovejero, D.; González, S.; Paniagua-Torija, B.; Lima, A.; Molina-Holgado, E.; De Nicola, A.F.; Labombarda, F.
Filiación:Laboratorio de Neuroinflamación, Hospital Nacional de Parapléjicos, Toledo, Spain
Laboratorio de Nocicepción y Dolor Neuropático, Instituto de Biología y Medicina Experimental, Buenos Aires, Argentina
Laboratorio de Bioquimica Neuroendócrina, Instituto de Biología y Medicina Experimental, Vuelta de Obligado 2490, Buenos Aires 1428, Argentina
Department of Human Biochemistry, School of Medicine, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:CatWalk; oligodendrocytes; progesterone; spare white matter; spinal cord injury; myelin basic protein; progesterone; gestagen; progesterone; adult; animal experiment; animal model; article; catwalk gait analysis test; cell counting; controlled study; drug mechanism; immunoreactivity; locomotion; male; nerve regeneration; nonhuman; nuclear magnetic resonance imaging; oligodendroglia; open field behavior; rat; spinal cord injury; tissue preservation; treatment outcome; white matter; young adult; animal; convalescence; disease model; drug effects; immunohistochemistry; motor activity; pathology; spinal cord injury; white matter; Wistar rat; Animals; Disease Models, Animal; Immunohistochemistry; Magnetic Resonance Imaging; Male; Motor Activity; Progesterone; Progestins; Rats; Rats, Wistar; Recovery of Function; Spinal Cord Injuries; White Matter
Año:2014
Volumen:31
Número:9
Página de inicio:857
Página de fin:871
DOI: http://dx.doi.org/10.1089/neu.2013.3162
Título revista:Journal of Neurotrauma
Título revista abreviado:J. Neurotrauma
ISSN:08977151
CODEN:JNEUE
CAS:progesterone, 57-83-0; Progesterone; Progestins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_08977151_v31_n9_p857_GarciaOvejero

Referencias:

  • Ambrozaitis, K.V., Kontautas, E., Spakauskas, B., Vaitkaitis, D., Pathophysiology of acute spinal cord injury (2006) (Lith Medicina (Kaunas), 42, pp. 255-261
  • Beattie, M.S., Farooqui, A.A., Bresnahan, J.C., Review of current evidence for apoptosis after spinal cord injury (2000) J. Neurotrauma, 17, pp. 915-925
  • Borgens, R.B., Liu-Snyder, P., Understanding secondary injury (2012) Q. Rev. Biol., 87, pp. 89-127
  • Kwon, B.K., Okon, E., Hillyer, J., Mann, C., Baptiste, D., Weaver, L.C., Fehlings, M.G., Tetzlaff, W., A systematic review of non-invasive pharmacologic neuroprotective treatments for acute spinal cord injury (2011) J. Neurotrauma, 28, pp. 1545-1588
  • Lammertse, D.P., Clinical trials in spinal cord injury: Lessons learned on the path to translation (2013) The 2011 International Spinal Cord Society Sir Ludwig Guttmann Lecture. Spinal Cord, 51, pp. 2-9
  • Rabchevsky, A.G., Patel, S.P., Springer, J.E., Pharmacological interventions for spinal cord injury: Where do we stand? How might we step forward? (2011) Pharmacol. Ther., 132, pp. 15-29
  • Bracken, M.B., Methylprednisolone in the management of acute spinal cord injuries (1990) Med. J. Aust., 153, p. 368
  • Bracken, M.B., Shepard, M.J., Holford, T.R., Leo-Summers, L., Aldrich, E.F., Fazl, M., Fehlings, M., Young, W., Administration of methylprednisolone for 24 or 48 hours or tirilazad mesylate for 48 hours in the treatment of acute spinal cord injury (1997) JAMA, 277, pp. 1597-1604
  • Ciriza, I., Carrero, P., Frye, C.A., Garcia-Segura, L.M., Reduced metabolites mediate neuroprotective effects of progesterone in the adult rat hippocampus. The synthetic progestin medroxyprogesterone acetate (Provera) is not neuroprotective (2006) J. Neurobiol., 66, pp. 916-928
  • De Nicola, A.F., Labombarda, F., Deniselle, M.C., Gonzalez, S.L., Garay, L., Meyer, M., Gargiulo, G., Schumacher, M., Progesterone neuroprotection in traumatic CNS injury and motoneuron degeneration (2009) Front. Neuroendocrinol, 30, pp. 173-187
  • Giatti, S., Caruso, D., Boraso, M., Abbiati, F., Ballarini, E., Calabrese, D., Pesaresi, M., Melcangi, R.C., Neuroprotective effects of progesterone in chronic experimental autoimmune encephalomyelitis (2012) J. Neuroendocrinol., 24, pp. 851-861
  • Schumacher, M., Hussain, R., Gago, N., Oudinet, J.P., Mattern, C., Ghoumari, A.M., Progesterone synthesis in the nervous system: Implications for myelination and myelin repair (2012) Front. Neurosci, 6, p. 10
  • Pettus, E.H., Wright, D.W., Stein, D.G., Hoffman, S.W., Progesterone treatment inhibits the inflammatory agents that accompany traumatic brain injury (2005) Brain Res., 1049, pp. 112-119
  • Robertson, C.L., Puskar, A., Hoffman, G.E., Murphy, A.Z., Saraswati, M., Fiskum, G., Physiologic progesterone reduces mitochondrial dysfunction and hippocampal cell loss after traumatic brain injury in female rats (2006) Exp. Neurol., 197, pp. 235-243
  • Stein, D.G., Progesterone exerts neuroprotective effects after brain injury (2008) Brain Res. Rev., 57, pp. 386-397
  • Stein, D.G., Progesterone in the treatment of acute traumatic brain injury: A clinical perspective and update (2011) Neuroscience, 191, pp. 101-106
  • Wright, D.W., Kellermann, A.L., Hertzberg, V.S., Clark, P.L., Frankel, M., Goldstein, F.C., Salomone, J.P., Stein, D.G., ProTECT: A randomized clinical trial of progesterone for acute traumatic brain injury (2007) Ann. Emerg. Med., 49, pp. 391-402. , 402 e1-2
  • Xiao, G., Wei, J., Yan, W., Wang, W., Lu, Z., Improved outcomes from the administration of progesterone for patients with acute severe traumatic brain injury: A randomized controlled trial (2008) Crit. Care, 12, pp. R61
  • Gonzalez, S.L., Labombarda, F., Gonzalez Deniselle, M.C., Guennoun, R., Schumacher, M., De Nicola, A.F., Progesterone up-regulates neuronal brain-derived neurotrophic factor expression in the injured spinal cord (2004) Neuroscience, 125, pp. 605-614
  • Labombarda, F., Gonzalez, S.L., Gonzalez, D.M., Guennoun, R., Schumacher, M., De Nicola, A.F., Cellular basis for progesterone neuroprotection in the injured spinal cord (2002) J. Neurotrauma, 19, pp. 343-355
  • Labombarda, F., Gonzalez, S.L., Lima, A., Roig, P., Guennoun, R., Schumacher, M., De Nicola, A.F., Effects of progesterone on oligodendrocyte progenitors, oligodendrocyte transcription factors, and myelin proteins following spinal cord injury (2009) Glia, 57, pp. 884-897
  • Labombarda, F., Gonzalez, S., Lima, A., Roig, P., Guennoun, R., Schumacher, M., De Nicola, A.F., Progesterone attenuates astro-and microgliosis and enhances oligodendrocyte differentiation following spinal cord injury (2011) Exp. Neurol., 231, pp. 135-146
  • Arevalo-Martin, A., Garcia-Ovejero, D., Sierra-Palomares, Y., Paniagua-Torija, B., Gonzalez-Gil, I., Ortega-Gutierrez, S., Molina-Holgado, E., Early endogenous activation of CB1 and CB2 receptors after spinal cord injury is a protective response involved in spontaneous recovery (2012) PLoS One, 7, pp. e49057
  • Garcia-Ovejero, D., Arevalo-Martin, A., Paniagua-Torija, B., Sierra-Palomares, Y., Molina-Holgado, E., A cell population that strongly expresses the CB1 cannabinoid receptor in the ependyma of the rat spinal cord (2013) J. Comp. Neurol., 521, pp. 233-251
  • Scheff, S.W., Rabchevsky, A.G., Fugaccia, I., Main, J.A., Lumpp Jr., J.E., Experimental modeling of spinal cord injury: Characterization of a force-defined injury device (2003) J. Neurotrauma, 20, pp. 179-193
  • Basso, D.M., Beattie, M.S., Bresnahan, J.C., A sensitive and reliable locomotor rating scale for open field testing in rats (1995) J. Neurotrauma, 12, pp. 1-21
  • Basso, D.M., Beattie, M.S., Bresnahan, J.C., Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection (1996) Exp. Neurol., 139, pp. 244-256
  • Cutler, S.M., Cekic, M., Miller, D.M., Wali, B., Vanlandingham, J.W., Stein, D.G., Progesterone improves acute recovery after traumatic brain injury in the aged rat (2007) J. Neurotrauma, 24, pp. 1475-1486
  • Labombarda, F., Gonzalez, S., Gonzalez Deniselle, M.C., Garay, L., Guennoun, R., Schumacher, M., De Nicola, A.F., Progesterone increases the expression of myelin basic protein and the number of cells showing NG2 immunostaining in the lesioned spinal cord (2006) J. Neurotrauma, 23, pp. 181-192
  • Arevalo-Martin, A., Garcia-Ovejero, D., Molina-Holgado, E., The endocannabinoid 2-arachidonoylglycerol reduces lesion expansion and white matter damage after spinal cord injury (2010) Neurobiol. Dis., 38, pp. 304-312
  • Ma, M., Basso, D.M., Walters, P., Stokes, B.T., Jakeman, L.B., Behavioral and histological outcomes following graded spinal cord contusion injury in the C57Bl/6 mouse (2001) Exp. Neurol., 169, pp. 239-254
  • Schmitz, C., Hof, P.R., Design-based stereology in neuroscience (2005) Neuroscience, 130, pp. 813-831
  • Koopmans, G.C., Brans, M., Gomez-Pinilla, F., Duis, S., Gispen, W.H., Torres-Aleman, I., Joosten, E.A., Hamers, F.P., Circulating insulin-like growth factor i and functional recovery from spinal cord injury under enriched housing conditions (2006) Eur. J. Neurosci., 23, pp. 1035-1046
  • Basso, D.M., Behavioral testing after spinal cord injury: Congruities, complexities, and controversies (2004) J. Neurotrauma, 21, pp. 395-404
  • Hamers, F.P., Koopmans, G.C., Joosten, E.A., CatWalkassisted gait analysis in the assessment of spinal cord injury (2006) J. Neurotrauma, 23, pp. 537-548
  • Hamers, F.P., Lankhorst, A.J., Van Laar, T.J., Veldhuis, W.B., Gispen, W.H., Automated quantitative gait analysis during overground locomotion in the rat: Its application to spinal cord contusion and transection injuries (2001) J. Neurotrauma, 18, pp. 187-201
  • Lankhorst, A.J., Ter Laak, M.P., Van Laar, T.J., Van Meeteren, N.L., De Groot, J.C., Schrama, L.H., Hamers, F.P., Gispen, W.H., Effects of enriched housing on functional recovery after spinal cord contusive injury in the adult rat (2001) J. Neurotrauma, 18, pp. 203-215
  • Singh, A., Murray, M., Houle, J.D., A training paradigm to enhance motor recovery in contused rats: Effects of staircase training (2011) Neurorehabil. Neural Repair, 25, pp. 24-34
  • Vlamings, R., Visser-Vandewalle, V., Koopmans, G., Joosten, E.A., Kozan, R., Kaplan, S., Steinbusch, H.W., Temel, Y., High frequency stimulation of the subthalamic nucleus improves speed of locomotion but impairs forelimb movement in Parkinsonian rats (2007) Neuroscience, 148, pp. 815-823
  • Dolan, S., Nolan, A.M., Blockade of metabotropic glutamate receptor 5 activation inhibits mechanical hypersensitivity following abdominal surgery (2007) Eur. J. Pain, 11, pp. 644-651
  • Obata, K., Yamanaka, H., Kobayashi, K., Dai, Y., Mizushima, T., Katsura, H., Fukuoka, T., Noguchi, K., Role of mitogen-activated protein kinase activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation (2004) J. Neurosci., 24, pp. 10211-10222
  • Hargreaves, K., Dubner, R., Brown, F., Flores, C., Joris, J., A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia (1988) Pain, 32, pp. 77-88
  • Bodley, R., Imaging in chronic spinal cord injury-indications and benefits (2002) Eur. J. Radiol., 42, pp. 135-153
  • Goldberg, A.L., Daffner, R.H., Schapiro, R.L., Imaging of acute spinal trauma: An evolving multi-modality approach (1990) Clin. Imaging, 14, pp. 11-16
  • Parashari, U.C., Khanduri, S., Bhadury, S., Kohli, N., Parihar, A., Singh, R., Srivastava, R.N., Upadhyay, D., Diagnostic and prognostic role of MRI in spinal trauma, its comparison and correlation with clinical profile and neurological outcome, according to ASIA impairment scale (2011) J. Craniovertebr. Junction Spine, 2, pp. 17-26
  • Ballermann, M., Fouad, K., Spontaneous locomotor recovery in spinal cord injured rats is accompanied by anatomical plasticity of reticulospinal fibers (2006) Eur. J. Neurosci., 23, pp. 1988-1996
  • Raineteau, O., Fouad, K., Bareyre, F.M., Schwab, M.E., Reorganization of descending motor tracts in the rat spinal cord (2002) Eur. J. Neurosci., 16, pp. 1761-1771
  • Van Meeteren, N.L., Eggers, R., Lankhorst, A.J., Gispen, W.H., Hamers, F.P., Locomotor recovery after spinal cord contusion injury in rats is improved by spontaneous exercise (2003) J. Neurotrauma, 20, pp. 1029-1037
  • Kloos, A.D., Fisher, L.C., Detloff, M.R., Hassenzahl, D.L., Basso, D.M., Stepwise motor and all-or-none sensory recovery is associated with nonlinear sparing after incremental spinal cord injury in rats (2005) Exp. Neurol., 191, pp. 251-265
  • Deumens, R., Jaken, R.J., Marcus, M.A., Joosten, E.A., The CatWalk gait analysis in assessment of both dynamic and static gait changes after adult rat sciatic nerve resection (2007) J. Neurosci. Methods, 164, pp. 120-130
  • Vrinten, D.H., Hamers, F.F., 'CatWalk' automated quantitative gait analysis as a novel method to assess mechanical allodynia in the rat; A comparison with von Frey testing (2003) Pain, 102, p. 203209
  • Guo, Q., Sayeed, I., Baronne, L.M., Hoffman, S.W., Guennoun, R., Stein, D.G., Progesterone administration modulates AQP4 expression and edema after traumatic brain injury in male rats (2006) Exp. Neurol., 198, pp. 469-478
  • Roof, R.L., Hall, E.D., Gender differences in acute CNS trauma and stroke: Neuroprotective effects of estrogen and progesterone (2000) J. Neurotrauma, 17, pp. 367-388
  • Garay, L.I., Gonzalez Deniselle, M.C., Brocca, M.E., Lima, A., Roig, P., De Nicola, A.F., Progesterone down-regulates spinal cord inflammatory mediators and increases myelination in experimental autoimmune encephalomyelitis (2012) Neuroscience, 226, pp. 40-50
  • Grossman, K.J., Goss, C.W., Stein, D.G., Effects of progesterone on the inflammatory response to brain injury in the rat (2004) Brain Res., 1008, pp. 29-39
  • Lambert, J.J., Belelli, D., Peden, D.R., Vardy, A.W., Peters, J.A., Neurosteroid modulation of GABAA receptors (2003) Prog. Neurobiol., 71, pp. 67-80
  • Labombarda, F., Pianos, A., Liere, P., Eychenne, B., Gonzalez, S., Cambourg, A., De Nicola, A.F., Guennoun, R., Injury elicited increase in spinal cord neurosteroid content analyzed by gas chromatography mass spectrometry (2006) Endocrinology, 147, pp. 1847-1859
  • Ciriza, I., Azcoitia, I., Garcia-Segura, L.M., Reduced progesterone metabolites protect rat hippocampal neurones from kainic acid excitotoxicity in vivo (2004) J. Neuroendocrinol., 16, pp. 58-63
  • Bresnahan, J.C., Beattie, M.S., Todd III, F.D., Noyes, D.H., A behavioral and anatomical analysis of spinal cord injury produced by a feedback-controlled impaction device (1987) Exp. Neurol., 95, pp. 548-570
  • Fehlings, M.G., Tator, C.H., The relationships among the severity of spinal cord injury, residual neurological function, axon counts, and counts of retrogradely labeled neurons after experimental spinal cord injury (1995) Exp. Neurol., 132, pp. 220-228
  • Schucht, P., Raineteau, O., Schwab, M.E., Fouad, K., Anatomical correlates of locomotor recovery following dorsal and ventral lesions of the rat spinal cord (2002) Exp. Neurol., 176, pp. 143-153
  • Basso, D.M., Beattie, M.S., Bresnahan, J.C., Descending systems contributing to locomotor recovery after mild or moderate spinal cord injury in rats: Experimental evidence and a review of literature (2002) Restor. Neurol. Neurosci., 20, pp. 189-218
  • Azcoitia, I., Leonelli, E., Magnaghi, V., Veiga, S., Garcia-Segura, L.M., Melcangi, R.C., Progesterone and its derivatives dihydroprogesterone and tetrahydroprogesterone reduce myelin fiber morphological abnormalities and myelin fiber loss in the sciatic nerve of aged rats (2003) Neurobiol. Aging, 24, pp. 853-860
  • Gago, N., Akwa, Y., Sananes, N., Guennoun, R., Baulieu, E.E., El-Etr, M., Schumacher, M., Progesterone and the oligodendroglial lineage: Stage-dependent biosynthesis and metabolism (2001) Glia, 36, pp. 295-308
  • Garay, L., Tungler, V., Deniselle, M.C., Lima, A., Roig, P., De Nicola, A.F., Progesterone attenuates demyelination and microglial reaction in the lysolecithin-injured spinal cord (2011) Neuroscience, 192, pp. 588-597
  • Ghoumari, A.M., Baulieu, E.E., Schumacher, M., Progesterone increases oligodendroglial cell proliferation in rat cerebellar slice cultures (2005) Neuroscience, 135, pp. 47-58
  • Leonelli, E., Ballabio, M., Consoli, A., Roglio, I., Magnaghi, V., Melcangi, R.C., Neuroactive steroids: A therapeutic approach to maintain peripheral nerve integrity during neurodegenerative events (2006) J. Mol. Neurosci., 28, pp. 65-76
  • Huang, W.L., King, V.R., Curran, O.E., Dyall, S.C., Ward, R.E., Lal, N., Priestley, J.V., Michael-Titus, A.T., A combination of intravenous and dietary docosahexaenoic acid significantly improves outcome after spinal cord injury (2007) Brain, 130, pp. 3004-3019
  • Stirling, D.P., Khodarahmi, K., Liu, J., McPhail, L.T., McBride, C.B., Steeves, J.D., Ramer, M.S., Tetzlaff, W., Minocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury (2004) J. Neurosci., 24, pp. 2182-2190
  • Rabchevsky, A.G., Sullivan, P.G., Scheff, S.W., Temporalspatial dynamics in oligodendrocyte and glial progenitor cell numbers throughout ventrolateral white matter following contusion spinal cord injury (2007) Glia, 55, pp. 831-843
  • Coleman, M.P., Perry, V.H., Axon pathology in neurological disease: A neglected therapeutic target (2002) Trends Neurosci., 25, pp. 532-537
  • Flygt, J., Djupsjo, A., Lenne, F., Marklund, N., Myelin loss and oligodendrocyte pathology in white matter tracts following traumatic brain injury in the rat (2013) Eur. J. Neurosci., 38, pp. 2153-2165
  • Nguyen, T., Mehta, N.R., Conant, K., Kim, K.J., Jones, M., Calabresi, P.A., Melli, G., Griffin, J.W., Axonal protective effects of the myelin-associated glycoprotein (2009) J. Neurosci., 29, pp. 630-637
  • Magnuson, D.S., Trinder, T.C., Zhang, Y.P., Burke, D., Morassutti, D.J., Shields, C.B., Comparing deficits following excitotoxic and contusion injuries in the thoracic and lumbar spinal cord of the adult rat (1999) Exp. Neurol., 156, pp. 191-204
  • Basso, D.M., Neuroanatomical substrates of functional recovery after experimental spinal cord injury: Implications of basic science research for human spinal cord injury (2000) Phys. Ther., 80, pp. 808-817
  • Reier, P.J., Golder, F.J., Bolser, D.C., Hubscher, C., Johnson, R., Schrimsher, G.W., Velardo, M.J., Gray matter repair in the cervical spinal cord (2002) Prog. Brain Res., 137, pp. 49-70
  • Koopmans, G.C., Deumens, R., Honig, W.M., Hamers, F.P., Steinbusch, H.W., Joosten, E.A., The assessment of locomotor function in spinal cord injured rats: The importance of objective analysis of coordination (2005) J. Neurotrauma, 22, pp. 214-225
  • Barriere, G., Leblond, H., Provencher, J., Rossignol, S., Prominent role of the spinal central pattern generator in the recovery of locomotion after partial spinal cord injuries (2008) J. Neurosci., 28, pp. 3976-3987
  • Clarac, F., Some historical reflections on the neural control of locomotion (2008) Brain Res. Rev., 57, pp. 13-21
  • Guertin, P.A., The mammalian central pattern generator for locomotion (2009) Brain Res. Rev., 62, pp. 45-56
  • Pearson, K.G., Rossignol, S., Fictive motor patterns in chronic spinal cats (1991) J. Neurophysiol., 66, pp. 1874-1887
  • Bareyre, F.M., Kerschensteiner, M., Raineteau, O., Mettenleiter, T.C., Weinmann, O., Schwab, M.E., The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats (2004) Nat. Neurosci., 7, pp. 269-277
  • Alsina, B., Vu, T., Cohen-Cory, S., Visualizing synapse formation in arborizing optic axons in vivo: Dynamics and modulation by BDNF (2001) Nat. Neurosci., 4, pp. 1093-1101
  • Hendriks, W.T., Eggers, R., Ruitenberg, M.J., Blits, B., Hamers, F.P., Verhaagen, J., Boer, G.J., Profound differences in spontaneous long-term functional recovery after defined spinal tract lesions in the rat (2006) J. Neurotrauma, 23, pp. 18-35
  • Joosten, E.A., Veldhuis, W.B., Hamers, F.P., Collagen containing neonatal astrocytes stimulates regrowth of injured fibers and promotes modest locomotor recovery after spinal cord injury (2004) J. Neurosci. Res., 77, pp. 127-142
  • Deumens, R., Koopmans, G.C., Honig, W.M., Hamers, F.P., Maquet, V., Jerome, R., Steinbusch, H.W., Joosten, E.A., Olfactory ensheathing cells, olfactory nerve fibroblasts and biomatrices to promote long-distance axon regrowth and functional recovery in the dorsally hemisected adult rat spinal cord (2006) Exp. Neurol., 200, pp. 89-103
  • Thomas, A.J., Nockels, R.P., Pan, H.Q., Shaffrey, C.I., Chopp, M., Progesterone is neuroprotective after acute experimental spinal cord trauma in rats (1999) Spine, 24, pp. 2134-2138
  • Fee, D.B., Swartz, K.R., Joy, K.M., Roberts, K.N., Scheff, N.N., Scheff, S.W., Effects of progesterone on experimental spinal cord injury (2007) Brain Res., 1137, pp. 146-152
  • Cadotte, D.W., Fehlings, M.G., Spinal cord injury: A systematic review of current treatment options (2011) Clin. Orthop. Relat. Res., 469, pp. 732-741

Citas:

---------- APA ----------
Garcia-Ovejero, D., González, S., Paniagua-Torija, B., Lima, A., Molina-Holgado, E., De Nicola, A.F. & Labombarda, F. (2014) . Progesterone reduces secondary damage, preserves white matter, and improves locomotor outcome after spinal cord contusion. Journal of Neurotrauma, 31(9), 857-871.
http://dx.doi.org/10.1089/neu.2013.3162
---------- CHICAGO ----------
Garcia-Ovejero, D., González, S., Paniagua-Torija, B., Lima, A., Molina-Holgado, E., De Nicola, A.F., et al. "Progesterone reduces secondary damage, preserves white matter, and improves locomotor outcome after spinal cord contusion" . Journal of Neurotrauma 31, no. 9 (2014) : 857-871.
http://dx.doi.org/10.1089/neu.2013.3162
---------- MLA ----------
Garcia-Ovejero, D., González, S., Paniagua-Torija, B., Lima, A., Molina-Holgado, E., De Nicola, A.F., et al. "Progesterone reduces secondary damage, preserves white matter, and improves locomotor outcome after spinal cord contusion" . Journal of Neurotrauma, vol. 31, no. 9, 2014, pp. 857-871.
http://dx.doi.org/10.1089/neu.2013.3162
---------- VANCOUVER ----------
Garcia-Ovejero, D., González, S., Paniagua-Torija, B., Lima, A., Molina-Holgado, E., De Nicola, A.F., et al. Progesterone reduces secondary damage, preserves white matter, and improves locomotor outcome after spinal cord contusion. J. Neurotrauma. 2014;31(9):857-871.
http://dx.doi.org/10.1089/neu.2013.3162