Aging with a traumatic brain injury: Could behavioral morbidities and endocrine symptoms be influenced by microglial priming?

Brain, Behavior, and Immunity

Volumn 59, Issue , 2017, Pages 1-7

  Ziebell, Jenna M ^a,b,c   Rowe, Rachel K ^b,c,e   Muccigrosso, Megan M ^g   Reddaway, Jack T ^b,c,d   Adelson, P David ^b,c,d   Godbout, Jonathan P ^g   Lifshitz, Jonathan ^b,c,e,f  

^a UNIVERSITY OF TASMANIA   (Australia)

^b PHOENIX CHILDREN'S HOSPITAL   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^d University of Bath   (United Kingdom)

^e ARIZONA STATE UNIVERSITY   (United States)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

^g OHIO STATE UNIVERSITY   (United States)

Author keywords

Aging; Cognition; Endocrine dysfunction; Inflammation; Microglia; Traumatic brain injury

Indexed keywords

AGE; AGING; DISEASE SEVERITY; ENDOCRINE DISEASE; GENETICS; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; INFLAMMATION; LIFESPAN; MENTAL HEALTH; MICROGLIA; MORBIDITY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PUBERTY; REVIEW; SENESCENCE; SOCIAL BEHAVIOR; TRAUMATIC BRAIN INJURY; AGED; ANIMAL; PATHOLOGY; PSYCHOLOGY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; AGING; ANIMALS; BRAIN INJURIES, TRAUMATIC; ENDOCRINE SYSTEM DISEASES; HUMANS; INFLAMMATION; MICROGLIA;

EID: 84961773396     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2016.03.008     Document Type: Review

References (108)

1. Acerini, C.L., et al. Hypopituitarism in childhood and adolescence following traumatic brain injury: the case for prospective endocrine investigation. Eur. J. Endocrinol. 155:5 (2006), 663–669.
2. Age limits and adolescents. Paediatr. Child Health 8:9 (2003), 577–578.
3. Anderson, V., Moore, C., Age at injury as a predictor of outcome following pediatric head injury: a longitudinal perspective. Child Neuropsychol. 1:3 (1995), 187–202.
4. Anderson, V., Spencer-Smith, M., Wood, A., Do children really recover better? Neurobehavioural plasticity after early brain insult. Brain 134:Pt 8 (2011), 2197–2221.
5. Anderson, V., et al. 10 years outcome from childhood traumatic brain injury. Int. J. Dev. Neurosci. 30:3 (2012), 217–224.
6. Andrews, T.K., Rose, F.D., Johnson, D.A., Social and behavioural effects of traumatic brain injury in children. Brain Inj. 12:2 (1998), 133–138.
7. Auble, B.A., et al. Hypopituitarism in pediatric survivors of inflicted traumatic brain injury. J. Neurotrauma 31:4 (2014), 321–326.
8. Aungst, S.L., et al. Repeated mild traumatic brain injury causes chronic neuroinflammation, changes in hippocampal synaptic plasticity, and associated cognitive deficits. J. Cereb. Blood Flow Metab. 34:7 (2014), 1223–1232.
9. Barrientos, R.M., et al. Greater glucocorticoid receptor activation in hippocampus of aged rats sensitizes microglia. Neurobiol. Aging 36:3 (2015), 1483–1495.
10. Barrientos, R.M., et al. Neuroinflammation in the normal aging hippocampus. Neuroscience 309 (2015), 84–99.
11. Belanger, H.G., Vanderploeg, R.D., The neuropsychological impact of sports-related concussion: a meta-analysis. J. Int. Neuropsychol. Soc. 11:4 (2005), 345–357.
12. Blakemore, S.J., Burnett, S., Dahl, R.E., The role of puberty in the developing adolescent brain. Hum. Brain Mapp. 31:6 (2010), 926–933.
13. Boake, C., et al. Diagnostic criteria for postconcussional syndrome after mild to moderate traumatic brain injury. J. Neuropsychiatry Clin. Neurosci. 17:3 (2005), 350–356.
14. Boutzios, G, Kaltsas, G., Immune System Effects on the Endocrine System. De Groot, L.J., et al. (eds.) Endotext, South Dartmouth (MA), 2000.
15. Brooks, D.N., Memory and head injury. J. Nerv. Ment. Dis. 155:5 (1972), 350–355.
16. Chapman, S.B., Neurocognitive stall, a paradox in long term recovery from pediatric brain injury. Brain Inj. Prof. 3 (2006), 10–13.
17. Chensue, S.W., et al. In vivo biologic and immunohistochemical analysis of interleukin-1 alpha, beta and tumor necrosis factor during experimental endotoxemia. Kinetics, Kupffer cell expression, and glucocorticoid effects. Am. J. Pathol. 138:2 (1991), 395–402.
18. Clark, B.D., et al. Detection of interleukin 1 alpha and 1 beta in rabbit tissues during endotoxemia using sensitive radioimmunoassays. J. Appl. Physiol. (1985) 71:6 (1991), 2412–2418.
19. Dennis, M., Barnes, M.A., Knowing the meaning, getting the point, bridging the gap, and carrying the message: aspects of discourse following closed head injury in childhood and adolescence. Brain Lang. 39:3 (1990), 428–446.
20. Fenn, A.M., et al. Immune activation promotes depression 1 month after diffuse brain injury: a role for primed microglia. Biol. Psychiatry 76:7 (2014), 575–584.
21. Fernandez-Rodriguez, E., et al. Hypopituitarism following traumatic brain injury: determining factors for diagnosis. Front. Endocrinol. (Lausanne), 2, 2011, 25.
22. Fernandez-Rodriguez, E., et al. Hypopituitarism after traumatic brain injury. Endocrinol. Metab. Clin. North Am. 44:1 (2015), 151–159.
23. Frank, M.G., et al. Prior exposure to glucocorticoids sensitizes the neuroinflammatory and peripheral inflammatory responses to E. coli lipopolysaccharide. Brain Behav. Immun. 24:1 (2010), 19–30.
24. Frank, M.G., Watkins, L.R., Maier, S.F., Stress-induced glucocorticoids as a neuroendocrine alarm signal of danger. Brain Behav. Immun. 33 (2013), 1–6.
25. Gaidolfi, E., Vignolo, L.A., Closed head injuries of school-age children: neuropsychological sequelae in early adulthood. Ital. J. Neurol. Sci. 1:2 (1980), 65–73.
26. Gandhi, R., et al. Influence of poly I: C on sickness behaviors, plasma cytokines, corticosterone and central monoamine activity: moderation by social stressors. Brain Behav. Immun. 21:4 (2007), 477–489.
27. Garcia-Segura, L.M., McCarthy, M.M., Minireview: role of glia in neuroendocrine function. Endocrinology 145:3 (2004), 1082–1086.
28. Gentleman, S.M., et al. Long-term intracerebral inflammatory response after traumatic brain injury. Forensic Sci. Int. 146:2–3 (2004), 97–104.
29. Giedd, J.N., et al. Puberty-related influences on brain development. Mol. Cell. Endocrinol. 254–255 (2006), 154–162.
30. Giza, C.C., Prins, M.L., Is being plastic fantastic? Mechanisms of altered plasticity after developmental traumatic brain injury. Dev. Neurosci. 28:4–5 (2006), 364–379.
31. Golub, M.S., et al. Public health implications of altered puberty timing. Pediatrics 121:Suppl. 3 (2008), S218–S230.
32. Hannon, M.J., et al. Acute glucocorticoid deficiency and diabetes insipidus are common after acute traumatic brain injury and predict mortality. J. Clin. Endocrinol. Metab. 98:8 (2013), 3229–3237.
33. Hart, A.D., et al. Age related changes in microglial phenotype vary between CNS regions: grey versus white matter differences. Brain Behav. Immun. 26:5 (2012), 754–765.
34. Henry, C.J., et al. Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both pro-inflammatory IL-1beta and anti-inflammatory IL-10 cytokines. Brain Behav. Immun. 23:3 (2009), 309–317.
35. Himanen, L., et al. Longitudinal cognitive changes in traumatic brain injury: a 30-year follow-up study. Neurology 66:2 (2006), 187–192.
36. Holland, A.L., When is aphasia aphasia? The problem of closed head injury. Brookshire, R.H., (eds.) Clinical Aphasiology: Conference Proceedings, 1982, BRK Publishers, Minneapolis, MN.
37. Hosseini, A.H., Lifshitz, J., Brain injury forces of moderate magnitude elicit the fencing response. Med. Sci. Sports Exerc. 41:9 (2009), 1687–1697.
38. Hukkelhoven, C.W., et al. Patient age and outcome following severe traumatic brain injury: an analysis of 5600 patients. J. Neurosurg. 99:4 (2003), 666–673.
39. Ibanez, L., et al. Premature adrenarche–normal variant or forerunner of adult disease?. Endocr. Rev. 21:6 (2000), 671–696.
40. Johansson, B.B., Brain plasticity and stroke rehabilitation. The Willis lecture. Stroke 31:1 (2000), 223–230.
41. Johnson, V.E., et al. Inflammation and white matter degeneration persist for years after a single traumatic brain injury. Brain 136:Pt 1 (2013), 28–42.
42. Kaulfers, A.M., et al. Endocrine dysfunction following traumatic brain injury in children. J. Pediatr. 157:6 (2010), 894–899.
43. Klein, M., Houx, P.J., Jolles, J., Long-term persisting cognitive sequelae of traumatic brain injury and the effect of age. J. Nerv. Ment. Dis. 184:8 (1996), 459–467.
44. Klose, M., Feldt-Rasmussen, U., Hypopituitarism in traumatic brain injury – a critical note. J. Clin. Med. 4:7 (2015), 1480–1497.
45. Klose, M., et al. Acute and long-term pituitary insufficiency in traumatic brain injury: a prospective single-centre study. Clin. Endocrinol. (Oxf.) 67:4 (2007), 598–606.
46. Kogan, N., et al. Understanding visual metaphor: developmental and individual differences. Monogr. Soc. Res. Child Dev. 45:1 (1980), 1–78.
47. Kolb, B., Brain Plasticity and Behavior. 1995, Erlbaum, Mahwah, NJ.
48. Kozlowski Moreau, O., et al. Lasting pituitary hormone deficiency after traumatic brain injury. J. Neurotrauma 29:1 (2012), 81–89.
49. Kumar, A., et al. Traumatic brain injury in aged animals increases lesion size and chronically alters microglial/macrophage classical and alternative activation states. Neurobiol. Aging 34:5 (2013), 1397–1411.
50. Learoyd, A.E., Lifshitz, J., Comparison of rat sensory behavioral tasks to detect somatosensory morbidity after diffuse brain-injury. Behav. Brain Res. 226:1 (2012), 197–204.
51. Levin, H.S., et al. Neurobehavioral outcome 1 year after severe head injury. Experience of the Traumatic Coma Data Bank. J. Neurosurg. 73:5 (1990), 699–709.
52. Levin, H.S., et al. Psychosocial outcome of TBI in children with unilateral frontal lesions. J. Int. Neuropsychol. Soc. 10:3 (2004), 305–316.
53. Lifshitz, J., Lisembee, A.M., Neurodegeneration in the somatosensory cortex after experimental diffuse brain injury. Brain Struct. Funct. 217:1 (2012), 49–61.
54. Loane, D.J., et al. Progressive neurodegeneration after experimental brain trauma: association with chronic microglial activation. J. Neuropathol. Exp. Neurol. 73:1 (2014), 14–29.
55. McAllister, T.W., Neuropsychiatric sequelae of head injuries. Psychiatr. Clin. North Am. 15:2 (1992), 395–413.
56. McLean, J.P., Broadbent, D.E., Broadbent, M.H., Combining attributes in rapid serial visual presentation tasks. Q. J. Exp. Psychol. A 35:Pt 1 (1983), 171–186.
57. McNamara, K.C., Lisembee, A.M., Lifshitz, J., The whisker nuisance task identifies a late-onset, persistent sensory sensitivity in diffuse brain-injured rats. J. Neurotrauma 27:4 (2010), 695–706.
58. Meffre, D., et al. Distribution of membrane progesterone receptor alpha in the male mouse and rat brain and its regulation after traumatic brain injury. Neuroscience 231 (2013), 111–124.
59. Milton, S.B., Prutting, C.A., Binder, G.M., Appraisal of communicative competence in head injured adults. Brooshire, R.H., (eds.) Slinical Aphasiology: Conference Proceedings, 1984, BRK Publishers, Minneapolis, MN.
60. Moon, R.J., et al. Pituitary function at long-term follow-up of childhood traumatic brain injury. J. Neurotrauma 27:10 (2010), 1827–1835.
61. Moss, A.R., et al. Hormonal risk factors in testicular cancer. A case-control study. Am. J. Epidemiol. 124:1 (1986), 39–52.
62. Mouzon, B.C., et al. Chronic neuropathological and neurobehavioral changes in a repetitive mild traumatic brain injury model. Ann. Neurol. 75:2 (2014), 241–254.
63. Muccigrosso, M.M., et al. Cognitive deficits develop 1 month after diffuse brain injury and are exaggerated by microglia-associated reactivity to peripheral immune challenge. Brain Behav. Immun., 2016.
64. Norden, D.M., Muccigrosso, M.M., Godbout, J.P., Microglial priming and enhanced reactivity to secondary insult in aging, and traumatic CNS injury, and neurodegenerative disease.Neuropharmacology., 96(Pt A), 2015, 29–41.
65. Norwood, K.W., et al. Traumatic brain injury in children and adolescents: surveillance for pituitary dysfunction. Clin. Pediatr. (Phila) 49:11 (2010), 1044–1049.
66. Oddy, M., Humphrey, M., Social recovery during the year following severe head injury. J. Neurol. Neurosurg. Psychiatry 43:9 (1980), 798–802.
67. Palin, K., et al. Systemic inflammation switches the inflammatory cytokine profile in CNS Wallerian degeneration. Neurobiol. Dis. 30:1 (2008), 19–29.
68. Paolicelli, R.C., et al. Synaptic pruning by microglia is necessary for normal brain development. Science 333:6048 (2011), 1456–1458.
69. Perry, V.H., Teeling, J., Microglia and macrophages of the central nervous system: the contribution of microglia priming and systemic inflammation to chronic neurodegeneration. Semin. Immunopathol. 35:5 (2013), 601–612.
70. Peters, R., Ageing and the brain. Postgrad. Med. J. 82:964 (2006), 84–88.
71. Popovic, V., et al. Hypopituitarism as a consequence of traumatic brain injury (TBI) and its possible relation with cognitive disabilities and mental distress. J. Endocrinol. Invest. 27:11 (2004), 1048–1054.
72. Ramlackhansingh, A.F., et al. Inflammation after trauma: microglial activation and traumatic brain injury. Ann. Neurol. 70:3 (2011), 374–383.
73. Richmond, E., Rogol, A.D., Traumatic brain injury: endocrine consequences in children and adults. Endocrine 45:1 (2014), 3–8.
74. Ritchie, P.D., et al. A study of the functional outcome and mortality in elderly patients with head injuries. J. Clin. Neurosci. 7:4 (2000), 301–304.
75. Roe, C., et al. Post-concussion symptoms after mild traumatic brain injury: influence of demographic factors and injury severity in a 1-year cohort study. Disabil. Rehabil. 31:15 (2009), 1235–1243.
76. Rosema, S., Crowe, L., Anderson, V., Social function in children and adolescents after traumatic brain injury: a systematic review 1989–2011. J. Neurotrauma 29:7 (2012), 1277–1291.
77. Rothweiler, B., Temkin, N.R., Dikmen, S.S., Aging effect on psychosocial outcome in traumatic brain injury. Arch. Phys. Med. Rehabil. 79:8 (1998), 881–887.
78. Salehi, F., et al. Histologic study of the human pituitary gland in acute traumatic brain injury. Brain Inj. 21:6 (2007), 651–656.
79. Sandhir, R., Onyszchuk, G., Berman, N.E., Exacerbated glial response in the aged mouse hippocampus following controlled cortical impact injury. Exp. Neurol. 213:2 (2008), 372–380.
80. Schwarzbold, M., et al. Psychiatric disorders and traumatic brain injury. Neuropsychiatr. Dis. Treat. 4:4 (2008), 797–816.
81. Semple, B.D., Canchola, S.A., Noble-Haeusslein, L.J., Deficits in social behavior emerge during development after pediatric traumatic brain injury in mice. J. Neurotrauma 29:17 (2012), 2672–2683.
82. Semple, B.D., et al. Sociosexual and communication deficits after traumatic injury to the developing murine brain. PLoS ONE, 9(8), 2014, e103386.
83. Senathi-Raja, D., Ponsford, J., Schonberger, M., Impact of age on long-term cognitive function after traumatic brain injury. Neuropsychology 24:3 (2010), 336–344.
84. Sierra, A., et al. Steroid hormone receptor expression and function in microglia. Glia 56:6 (2008), 659–674.
85. Soliman, A., et al. Pituitary deficiency following traumatic brain injury in early childhood: a review of the literature. Georgian Med. News 244–245 (2015), 62–71.
86. Stein, D.G., Hoffman, S.W., Concepts of CNS plasticity in the context of brain damage and repair. J. Head Trauma Rehabil. 18:4 (2003), 317–341.
87. Stern, Y., Cognitive reserve. Neuropsychologia 47:10 (2009), 2015–2028.
88. Sternberg, E.M., Neuroendocrine regulation of autoimmune/inflammatory disease. J. Endocrinol. 169:3 (2001), 429–435.
89. Stuss, D.T., et al. Traumatic brain injury, aging and reaction time. Can. J. Neurol. Sci. 16:2 (1989), 161–167.
90. Sundaram, N.K., Geer, E.B., Greenwald, B.D., The impact of traumatic brain injury on pituitary function. Endocrinol. Metab. Clin. North Am. 42:3 (2013), 565–583.
91. Swerdlow, A.J., Huttly, S.R., Smith, P.G., Testis cancer: post-natal hormonal factors, sexual behaviour and fertility. Int. J. Cancer 43:4 (1989), 549–553.
92. Tanriverdi, F., Kelestimur, F., Neuroendocrine disturbances after brain damage: an important and often undiagnosed disorder. J. Clin. Med. 4:5 (2015), 847–857.
93. Taylor, S.E., et al. Rod microglia: a morphological definition. PLoS ONE, 9(5), 2014, e97096.
94. Tremblay, M.E., Lowery, R.L., Majewska, A.K., Microglial interactions with synapses are modulated by visual experience. PLoS Biol., 8(11), 2010, e1000527.
95. Tyerman, A., Humphrey, M., Changes in self-concept following severe head injury. Int. J. Rehabil. Res. 7:1 (1984), 11–23.
96. VanGuilder, H.D., et al. Concurrent hippocampal induction of MHC II pathway components and glial activation with advanced aging is not correlated with cognitive impairment. J. Neuroinflammation, 8, 2011, 138.
97. Wagner, A.K., et al. Persistent hypogonadism influences estradiol synthesis, cognition and outcome in males after severe TBI. Brain Inj. 26:10 (2012), 1226–1242.
98. Wake, H., et al. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 29:13 (2009), 3974–3980.
99. Wamstad, J.B., et al. Neuropsychological recovery and quality-of-life in children and adolescents with growth hormone deficiency following TBI: a preliminary study. Brain Inj. 27:2 (2013), 200–208.
100. Weil, Z.M., Gaier, K.R., Karelina, K., Injury timing alters metabolic, inflammatory and functional outcomes following repeated mild traumatic brain injury. Neurobiol. Dis. 70 (2014), 108–116.
101. Whiteneck, G.G., Gerhart, K.A., Cusick, C.P., Identifying environmental factors that influence the outcomes of people with traumatic brain injury. J. Head Trauma Rehabil. 19:3 (2004), 191–204.
102. Wiig, E.H., Alexander, E.W., Secord, W., Linguistic competence and level of cognitive functioning in adults with traumatic head injury. Whitaker, H.A., (eds.) Neuropsychological Studies of Non-Focal Brain Damage: Dementia and Trauma, 1988, Springer-Verlag, New York, 186–201.
103. Witcher, K.G., Eiferman, D.S., Godbout, J.P., Priming the inflammatory pump of the CNS after traumatic brain injury. Trends Neurosci. 38:10 (2015), 609–620.
104. Wyrwoll, C.S., Holmes, M.C., Seckl, J.R., 11beta-hydroxysteroid dehydrogenases and the brain: from zero to hero, a decade of progress. Front. Neuroendocrinol. 32:3 (2011), 265–286.
105. Yeates, K.O., Traumatic brain injury. Yeates, K.O., et al. (eds.) Pediatric Neuropsychology: Research, Theory, and Practice, 2000, The Guilford Press, New York, NY.
106. Ziebell, J.M., Morganti-Kossmann, M.C., Involvement of pro- and anti-inflammatory cytokines and chemokines in the pathophysiology of traumatic brain injury. Neurotherapeutics 7:1 (2010), 22–30.
107. Ziebell, J.M., et al. Attenuated neurological deficit, cell death and lesion volume in Fas-mutant mice is associated with altered neuroinflammation following traumatic brain injury. Brain Res. 1414 (2011), 94–105.
108. Ziebell, J.M., et al. Rod microglia: elongation, alignment, and coupling to form trains across the somatosensory cortex after experimental diffuse brain injury. J. Neuroinflammation, 9, 2012, 247.