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Research Article

Long-term cognitive and affective consequences of mild traumatic brain injury: comparison with older adults

ORCID Icon & ORCID Icon
Received 02 Feb 2024, Accepted 01 Jul 2024, Published online: 12 Jul 2024

References

  • Goldstein M. Traumatic brain injury: a silent epidemic. Ann Neurol. 1990;27(3):327. doi:10.1002/ana.410270315.
  • Veliz P, McCabe SE, Eckner JT, Schulenberg JE. Trends in the prevalence of concussion reported by US adolescents, 2016–2020. JAMA. 2021;325(17):1789. doi:10.1001/jama.2021.1538.
  • Taylor CA, Bell JM, Breiding MJ, Xu L. Traumatic brain injury–related emergency department visits, hospitalizations, and deaths — united states, 2007 and 2013. MMWR Surveill Summ. 2017;66(9):1–16. doi:10.15585/mmwr.ss6609a1.
  • Capizzi A, Woo J, Verduzco-Gutierrez M. Traumatic brain injury: an overview of epidemiology, pathophysiology, and medical management. Med Clinics of North Am. 2020;104(2):213–38. doi:10.1016/j.mcna.2019.11.001.
  • Gordon KE, Kuhle S. Canadians reporting sport-related concussions: increasing and now stabilizing. Clin J Sport Med. 2022;32(3):313–17. doi:10.1097/jsm.0000000000000888.
  • Cassidy JD, Carroll L, Peloso P, Borg J, von Holst H, Holm L, Kraus J, Coronado V. Incidence, risk factors and prevention of mild traumatic brain injury: results of the who collaborating centre task force on mild traumatic brain injury. J Rehabil Med. 2004;36:28–60. doi:10.1080/16501960410023732.
  • Farmer CM, Krull H, Concannon TW, Simmons MM, Pillemer F, Ruder T, Parker A, Purohit MP, Hiatt L, Batorsky BS, et al. Understanding treatment of mild traumatic brain injury in the military health system. Rand Health Q. 2017;6. doi:10.7249/rr844. Cited: in: PMID: 28845349.
  • Feigin VL, Theadom A, Barker-Collo S, Starkey NJ, McPherson K, Kahan M, Dowell A, Brown P, Parag V, Kydd R, et al. Incidence of traumatic brain injury in New Zealand: a population-based study. Lancet Neurol. 2013;12(1):53–64. doi:10.1016/s1474-4422(12)70262-4.
  • Vakil E, Greenstein Y, Weiss I, Shtein S. The effects of moderate-to-severe traumatic brain injury on episodic memory: a meta-analysis. Neuropsychol Rev. 2019;29(3):270–87. doi:10.1007/s11065-019-09413-8.
  • Cantu R. Concussion classification: ongoing controversy. In: Slobounov, S., Sebastianelli, W. editors. Foundations of sport-related brain injuries. Boston, MA: Springer; 2006. p. 87–110. doi:10.1007/0-387-32565-4_5.
  • Isokuortti H, Iverson GL, Silverberg ND, Kataja A, Brander A, Öhman J, Luoto TM. Characterizing the type and location of intracranial abnormalities in mild traumatic brain injury. J Neurosurg. 2018;129(6):1588–97. doi:10.3171/2017.7.JNS17615.
  • Echemendia RJ, Cantu RC. Return to play following sports-related mild traumatic brain injury: the role for neuropsychology. Appl Neuropsychol. 2003;10(1):48–55. doi:10.1207/S15324826AN1001_7.
  • Belanger HG, Curtiss G, Demery JA, Lebowitz BK, Vanderploeg RD. Factors moderating neuropsychological outcomes following mild traumatic brain injury: a meta-analysis. J Int Neuropsychological Soc. 2005;11(3):215–27. doi:10.1017/s1355617705050277.
  • Vanderploeg RD, Curtiss G, Belanger HG. Long-term neuropsychological outcomes following mild traumatic brain injury. J Int Neuropsychological Soc. 2005;11(3):228–36. doi:10.1017/s1355617705050289.
  • Chen J-K, Johnston KM, Frey S, Petrides M, Worsley K, Ptito A. Functional abnormalities in symptomatic concussed athletes: an fMRI study. Neuroimage. 2004;22(1):68–82. doi:10.1016/j.neuroimage.2003.12.032.
  • Frencham KAR, Fox AM, Maybery MT. Neuropsychological studies of mild traumatic brain injury: a meta-analytic review of research since 1995. J Clin Exp Neuropsychol. 2005;27(3):334–51. doi:10.1080/13803390490520328.
  • Rohling ML, Binder LM, Demakis GJ, Larrabee GJ, Ploetz DM, Langhinrichsen-Rohling J. A meta-analysis of neuropsychological outcome after mild traumatic brain injury: re-analyses and reconsiderations of binder et al. (1997), frencham et al. (2005), and Pertab et al. (2009). Clin Neuropsychol. 2011;25(4):608–23. doi:10.1080/13854046.2011.565076.
  • Eierud C, Craddock RC, Fletcher S, Aulakh M, King-Casas B, Kuehl D, LaConte SM. Neuroimaging after mild traumatic brain injury: review and meta-analysis. Neuroimage Clin. 2014;4:283–94. doi:10.1016/j.nicl.2013.12.009.
  • Tellier A, Marshall SC, Wilson KG, Smith A, Perugini M, Stiell IG. The heterogeneity of mild traumatic brain injury: where do we stand? Brain Inj. 2009;23(11):879–87. doi:10.1080/02699050903200555.
  • Dikmen S, Machamer J, Temkin N. Mild traumatic brain injury: longitudinal study of cognition, functional status, and post-traumatic symptoms. J Neurotrauma. 2017;34(8):1524–30. doi:10.1089/neu.2016.4618.
  • Ponsford J, Willmott C, Rothwell A, Cameron P, Kelly A-M, Nelms R, Curran C, Ng K. Factors influencing outcome following mild traumatic brain injury in adults. J Int Neuropsychological Soc. 2000;6(5):568–79. doi:10.1017/s1355617700655066.
  • Ruff RM, Camenzuli L, Mueller J. Miserable minority: emotional risk factors that influence the outcome of a mild traumatic brain injury. Brain Inj. 1996;10(8):551–66. doi:10.1080/026990596124124.
  • Theadom A, Parag V, Dowell T, McPherson K, Starkey N, Barker-Collo S, Jones K, Ameratunga S, Feigin VL. Persistent problems 1 year after mild traumatic brain injury: a longitudinal population study in New Zealand. Br J Gen Pract. 2015;66(642):e16–23. doi:10.3399/bjgp16x683161.
  • Sigurdardottir S, Andelic N, Roe C, Jerstad T, Schanke A-K. Post-concussion symptoms after traumatic brain injury at 3 and 12 months post-injury: a prospective study. Brain Inj. 2009;23(6):489–97. doi:10.1080/02699050902926309.
  • Rutherford WH, Merrett JD, Mcdonald JR. Symptoms at one year following concussion from minor head injuries. Injury. 1979;10(3):225–30. doi:10.1016/0020-1383(79)90015-9.
  • McInnes K, Friesen CL, MacKenzie DE, Westwood DA, Boe SG. Mild traumatic brain injury (mTBI) and chronic cognitive impairment: a scoping review. Kobeissy F, editor. PLOS One. 2017;12(4) 12. doi:10.1371/journal.pone.0174847.
  • Nyberg L, Lövdén M, Riklund K, Lindenberger U, Bäckman L. Memory aging and brain maintenance. Trends Cogn Sci. 2012;16(5):292–305. doi:10.1016/j.tics.2012.04.005.
  • Wager TD, Smith EE. Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci. 2003;3(4):255–74. doi:10.3758/CABN.3.4.255.
  • Squire LR, Zola-Morgan S. The medial temporal lobe memory system. Sci (1979). 1991;253(5026):1380–86. doi:10.1126/science.1896849.
  • Eichenbaum H. Prefrontal–hippocampal interactions in episodic memory. Nat Rev Neurosci. 2017;18(9):547–58. doi:10.1038/nrn.2017.74.
  • Chalfonte BL, Johnson MK. Feature memory and binding in young and older adults. Mem Cognit. 1996;24(4):403–16. doi:10.3758/bf03200930.
  • Mitchell KJ, Johnson MK, Raye CL, Mather M, D’Esposito M. Aging and reflective processes of working memory: binding and test load deficits. Psychol Aging. 2000;15(3):527–41. doi:10.1037/0882-7974.15.3.527.
  • Ranganath C. A unified framework for the functional organization of the medial temporal lobes and the phenomenology of episodic memory. Hippocampus. 2010;20(11):1263–90. doi:10.1002/hipo.20852.
  • Dickerson BC, Eichenbaum H. The episodic memory system: neurocircuitry and disorders. Neuropsychopharmacology. 2010;35(1):86–104. doi:10.1038/npp.2009.126.
  • Moscovitch M, Cabeza R, Winocur G, Nadel L. Episodic memory and beyond: the hippocampus and neocortex in transformation. Annu Rev Psychol. 2016;67(1):105–34. doi:10.1146/annurev-psych-113011-143733.
  • Naveh-Benjamin M. Adult age differences in memory performance: tests of an associative deficit hypothesis. J Exp Psychol Learn Mem Cogn. 2000;26(5):1170–87. doi:10.1037/0278-7393.26.5.1170.
  • Mangels JA, Craik FIM, Levine B, Schwartz ML, Stuss DT. Effects of divided attention on episodic memory in chronic traumatic brain injury: a function of severity and strategy. Neuropsychologia. 2002;40(13):2369–85. doi:10.1016/s0028-3932(02)00084-2.
  • Blanchet S, Paradis-Giroux A-A, Pépin M, Mckerral M. Impact of divided attention during verbal learning in young adults following mild traumatic brain injury. Brain Inj. 2009;23(2):111–22. doi:10.1080/02699050802649688.
  • Bopp KL, Verhaeghen P. Aging and verbal memory span: a meta-analysis. J Gerontol B Psychol Sci Soc Sci. 2005;60(5):P223–33. doi:10.1093/geronb/60.5.p223.
  • Park DC, Lautenschlager G, Hedden T, Davidson NS, Smith AD, Smith PK. Models of visuospatial and verbal memory across the adult life span. Psychol Aging. 2002;17(2):299–320. doi:10.1037/0882-7974.17.2.299.
  • Salthouse TA, Babcock RL. Decomposing adult age differences in working memory. Dev Psychol. 1991;27(5):763–76. doi:10.1037/0012-1649.27.5.763.
  • Diamond A. Executive functions. Annu Rev Psychol. 2013;64(1):135–68. doi:10.1146/annurev-psych-113011-143750.
  • Cabeza R, Dennis NA. Frontal lobes and aging: deterioration and compensation. Princ Frontal Lobe Function. 2012;2:628–52.
  • Moscovitch M, Winocur G. The neuropsychology of memory and aging. In: F. I. M. Craik & T. A. Salthouse editors. The handbook of aging and cognition. Lawrence Erlbaum Associates, Inc.; 1992. p. 315–372.
  • Cabeza R, Dennis NA. Frontal lobes and aging. Oxford University Press eBooks; 2013. 628–52 p. doi:10.1093/med/9780199837755.003.0044.
  • Prull MW, Gabrieli JDE, Bunge SA. Age-related changes in memory: A cognitive neuroscience perspective. In: F. I. M. Craik & T. A. Salthouse editors. The handbook of aging and cognition. 2nd ed. Lawrence Erlbaum Associates Publishers; 2000. p. 91–153.
  • Raz N, Lindenberger U, Rodrigue KM, Kennedy KM, Head D, Williamson A, Dahle C, Gerstorf D, Acker JD. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex. 2005;15(11):1676–89. doi:10.1093/cercor/bhi044.
  • Ozen LJ, Fernandes MA, Clark AJ, Roy EA. Evidence of cognitive decline in older adults after remote traumatic brain injury: an exploratory study. Aging Neuropsychol Cognition. 2015;22(5):517–33. doi:10.1080/13825585.2014.993584.
  • Reuter-Lorenz PA, Festini SB, Jantz TK. Executive functions and neurocognitive aging. In: K. W. Schaie & S. L. Willis. Handbook of the psychology of aging. 8th ed. Academic Press; 2021. p. 67–81.
  • Mattson AJ, Levin HS. Frontal lobe dysfunction following closed head injury. A review of the literature. J Nerv Ment Dis. 1990;178(5):282–91. doi:10.1097/00005053-199005000-00002.
  • Witt ST, Lovejoy DW, Pearlson GD, Stevens MC. Decreased prefrontal cortex activity in mild traumatic brain injury during performance of an auditory oddball task. Brain Imag Behav. 2010;4(3–4):232–47. doi:10.1007/s11682-010-9102-3.
  • Stern Y. Cognitive reserve in ageing and Alzheimer’s disease. Lancet Neurol. 2012;11:1006–12. doi:10.1016/S1474-4422(12)70191-6.
  • Cabeza R, Albert M, Belleville S, Craik FIM, Duarte A, Grady CL, Lindenberger U, Nyberg L, Park DC, Reuter-Lorenz PA, et al. Maintenance, reserve and compensation: the cognitive neuroscience of healthy ageing. Nat Rev Neurosci Nat Publishing Group. 2018;19(11):701–10. doi:10.1038/s41583-018-0068-2.
  • Hellewell SC, Beaton CS, Welton T, Grieve SM. Characterizing the risk of depression following mild traumatic brain injury: a meta-analysis of the literature comparing chronic mTBI to non-mTBI populations. Front Neurol. 2020;11:11. doi:10.3389/fneur.2020.00350.
  • Rao V, Lyketsos C. Neuropsychiatric sequelae of traumatic brain injury. Psychosomatics. 2000;41(2):95–103. doi:10.1176/appi.psy.41.2.95.
  • Musacchio S, Kallenbach MD, Huber DL, Raff H, Johnson BD, Leddy J, McCrea MA, Meier TB, Nelson LD. Salivary cortisol dynamics after mild traumatic brain injury. J Head Trauma Rehabil. 2023;38(4):E318–27. doi:10.1097/HTR.0000000000000855.
  • Sojka P, Stålnacke B-M, Björnstig U, Karlsson K. One-year follow-up of patients with mild traumatic brain injury: occurrence of post-traumatic stress-related symptoms at follow-up and serum levels of cortisol, S-100B and neuron-specific enolase in acute phase. Brain Inj. 2006;20(6):613–20. doi:10.1080/02699050600676982.
  • Spikman JM, van der Horn HJ, Scheenen ME, de Koning ME, Savas M, Langerak T, van Rossum EFC, van der Naalt J. Coping with stress before and after mild traumatic brain injury: a pilot hair cortisol study. Brain Inj. 2021;35(8):871–79. doi:10.1080/02699052.2021.1901143.
  • Anderson JFI, Cockle E. Investigating the effect of fatigue and psychological distress on information processing speed in the postacute period after mild traumatic brain injury in premorbidly healthy adults. Archiv Clin Neuropsychol. 2021;36. doi:10.1093/arclin/acaa123.
  • Möller MC, Nordin LE, Bartfai A, Julin P, Li T-Q. Fatigue and cognitive fatigability in mild traumatic brain injury are correlated with altered neural activity during vigilance test performance. Front Neurol. 2017;8:496. doi:10.3389/fneur.2017.00496.
  • Johansson B, Rönnbäck L. Novel computer tests for identification of mental fatigue after traumatic brain injury. NeuroRehabilitation. 2015;36(2):195–202. doi:10.3233/nre-151207.
  • Berginström N, Nordström P, Ekman U, Eriksson J, Andersson M, Nyberg L, Nordström A. Using functional magnetic resonance imaging to detect chronic fatigue in patients with previous traumatic brain injury: changes linked to altered striato-thalamic-cortical functioning. J Head Trauma Rehabil. 2018;33(4):266–74. doi:10.1097/htr.0000000000000340.
  • Stawski RS, Sliwinski MJ, Almeida DM, Smyth JM. Reported exposure and emotional reactivity to daily stressors: The roles of adult age and global perceived stress. Psychol Aging. 2008;23(1):52–61. doi:10.1037/0882-7974.23.1.52.
  • Cantor JB, Ashman T, Gordon W, Ginsberg A, Engmann C, Egan M, Spielman L, Dijkers M, Flanagan S. Fatigue after traumatic brain injury and its impact on participation and quality of life. J Head Trauma Rehabil. 2008;23(1):41–51. doi:10.1097/01.htr.0000308720.70288.af.
  • Ozen LJ, Itier RJ, Preston FF, Fernandes MA. Long-term working memory deficits after concussion: electrophysiological evidence. Brain Inj. 2013;27(11):1244–55. doi:10.3109/02699052.2013.804207.
  • Raven JC. Guide to using the mill hill vocabulary scale with the progressive matrices scales. London, UK: H. K. Lewis & Co.; 1958.
  • American Congress of Rehabilitation Medicine. Definition of mild traumatic brain injury. J Head Trauma Rehabil. 1993;8(3):86–87. doi:10.1097/00001199-199309000-00010.
  • Ozen LJ, Fernandes MA. Effects of “diagnosis threat” on cognitive and affective functioning long after mild head injury. J Int Neuropsychol Soc. 2010;17(2):219–29. doi:10.1017/s135561771000144x.
  • Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H. The montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53(4):695–99. doi:10.1111/j.1532-5415.2005.53221.x.
  • Carson N, Leach L, Murphy KJ. A re-examination of montreal cognitive assessment (MoCA) cutoff scores. Int J Geriatr Psychiatry. 2018;33(2):379–88. doi:10.1002/gps.4756. Cited: in: PMID: 28731508.
  • Warriner AB, Kuperman V, Brysbaert M. Norms of valence, arousal, and dominance for 13,915 English lemmas. Behav Res Methods. 2013;45(4):1191–207. doi:10.3758/s13428-012-0314-x.
  • Bradley MM, Lang PJ. Affective norms for English words (ANEW): Instruction manual and affective ratings. Technical report C-1. The Center for Research in Psychophysiology, University of Florida; 1999.
  • Van Overschelde JP, Rawson KA, Dunlosky J. Category norms: an updated and expanded version of the battig and montague (1969) norms. J Mem Lang. 2004;50(3):289–335. doi:10.1016/j.jml.2003.10.003.
  • Brysbaert M, New B. Moving beyond kučera and francis: a critical evaluation of current word frequency norms and the introduction of a new and improved word frequency measure for American English. Behav Res Methods. 2009;41(4):977–90. doi:10.3758/brm.41.4.977.
  • Thompson ER. Development and validation of an internationally reliable short-form of the positive and negative affect schedule (PANAS). J Cross Cult Psychol. 2007;38(2):227–42. doi:10.1177/0022022106297301.
  • Blair JR, Spreen O. Predicting premorbid IQ: a revision of the national adult reading test. Clin Neuropsychologist. 1989;3(2):129–36. doi:10.1080/13854048908403285.
  • Wechsler D. Manual for the Wechsler Adult Intelligence Scale-Revised. New York: Psychological Corporation; 1981.
  • Dixon WJ, Yuen KK. Trimming and winsorization: A review. Statistische Hefte. 1974;15(2–3):157–70. doi:10.1007/bf02922904.
  • Rosenbaum SB, Lipton ML. Embracing chaos: the scope and importance of clinical and pathological heterogeneity in mTBI. Brain Imag Behav. 2012;6(2):255–82. doi:10.1007/s11682-012-9162-7.
  • Lennon MJ, Brooker H, Creese B, Thayanandan T, Rigney G, Aarsland D, Hampshire A, Ballard C, Corbett A, Raymont V. Lifetime traumatic brain injury and cognitive domain deficits in late life: the PROTECT-TBI cohort study. J Neurotrauma. 2023;40(13–14):1423–35. doi:10.1089/neu.2022.0360.
  • Karlsen RH, Saksvik SB, Stenberg J, Lundervold AJ, Olsen A, Rautio I, Folvik L, Håberg AK, Vik A, Karr JE, et al. Examining the subacute effects of mild traumatic brain injury using a traditional and computerized neuropsychological test battery. J Neurotrauma. 2021;38(1):74–85. doi:10.1089/neu.2019.6922. Cited: in: PMID: 32948095.
  • van der Horn HJ, Liemburg EJ, Aleman A, Spikman JM, van der Naalt J. Brain networks subserving emotion regulation and adaptation after mild traumatic brain injury. J Neurotrauma. 2016;33(1):1–9. doi:10.1089/neu.2015.3905.
  • van der Horn HJ, Out ML, de Koning ME, Mayer AR, Spikman JM, Sommer IE, van der Naalt J. An integrated perspective linking physiological and psychological consequences of mild traumatic brain injury. J Neurol. 2020;267(9):2497–506. doi:10.1007/s00415-019-09335-8.
  • Brooks J, Fos LA, Greve KW, Hammond JS. Assessment of executive function in patients with mild traumatic brain injury. J Trauma Inj Infect Crit Care. 1999;46(1):159–63. doi:10.1097/00005373-199901000-00027.
  • Kim JJ, Gean AD. Imaging for the diagnosis and management of traumatic brain injury. Neurotherapeutics. 2011;8(1):39–53. doi:10.1007/s13311-010-0003-3.
  • Einarsen CE, Moen KG, Håberg AK, Eikenes L, Kvistad KA, Xu J, Moe HK, Tollefsen MH, Vik A, Skandsen T. Patients with mild traumatic brain injury recruited from both hospital and primary care settings: a controlled longitudinal magnetic resonance imaging study. J Neurotrauma. 2019;36(22):3172–82. doi:10.1089/neu.2018.6360.
  • Løvstad M, Funderud I, Endestad T, Due-Tønnessen P, Meling TR, Lindgren M, Knight RT, Solbakk AK. Executive functions after orbital or lateral prefrontal lesions: neuropsychological profiles and self-reported executive functions in everyday living. Brain Inj. 2012;26(13–14):1586–98. doi:10.3109/02699052.2012.698787.
  • Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc. 2002;8(3):448–60. doi:10.1017/s1355617702813248.
  • Stern Y. Cognitive reserve. Neuropsychologia. 2009;47(10):2015–28. doi:10.1016/j.neuropsychologia.2009.03.004.
  • Jacobs D, Sano M, Marder K, Bell K, Bylsma F, Lafleche G, Albert M, Brandt J, Stern Y. Age at onset of Alzheimer’s disease. Neurology. 1994;44:1215. doi:10.1212/wnl.44.7.1215.
  • Mathias JL, Wheaton P. Contribution of brain or biological reserve and cognitive or neural reserve to outcome after TBI: a meta-analysis (prior to 2015). Neurosci Biobehav Rev. 2015;55:573–93. doi:10.1016/j.neubiorev.2015.06.001.
  • Stenberg J, Håberg AK, Follestad T, Olsen A, Iverson GL, Terry DP, Karlsen RH, Saksvik SB, Karaliute M, Jan E, et al. Cognitive reserve moderates cognitive outcome after mild traumatic brain injury. Arch Phys Med Rehabil. 2020;101(1):72–80. doi:10.1016/j.apmr.2019.08.477.
  • Oldenburg C, Lundin A, Edman G, Nygren-de Boussard C, Bartfai A. Cognitive reserve and persistent post-concussion symptoms—A prospective mild traumatic brain injury (mTBI) cohort study. Brain Inj. 2015;30(2):146–55. doi:10.3109/02699052.2015.1089598.
  • Fay TB, Yeates KO, Taylor HG, Bangert B, Dietrich ANN, Nuss KE, Rusin J, Wright M. Cognitive reserve as a moderator of postconcussive symptoms in children with complicated and uncomplicated mild traumatic brain injury. J Int Neuropsychol Soc. 2009;16(1):94–105. doi:10.1017/s1355617709991007.
  • Anderson JFI, Martin L. The relationship between cognitive reserve and outcome after controlling for psychological status and sex following mild traumatic brain injury. Brain Inj. 2023;37(9):1048–55. doi:10.1080/02699052.2023.2222642.
  • Sorg SF, Delano-Wood L, Luc N, Schiehser DM, Hanson KL, Nation DA, Lanni E, Jak AJ, Lu K, Meloy MJ, et al. White matter integrity in veterans with mild traumatic brain injury. J Head Trauma Rehabil. 2014;29(1):21–32. doi:10.1097/htr.0b013e31828a1aa4.

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