Abstract
Recent evidence suggests social cognitive deficits may be among the most profound and disabling consequences of childhood traumatic brain injury (TBI); however, it is only over the last decade that this area has received increasing research attention. This study aims to systematically review all studies reporting on the effects of childhood TBI on social cognition. Meta-analytic techniques were employed to determine the magnitude of social cognitive deficits in childhood TBI. Literature searches were conducted in electronic databases (Medline/PubMed, Scopus, Cochrane, EMBASE, PsycINFO and CINAHL) to retrieve relevant articles on social cognitive outcomes of paediatric TBI published from 2007–2019. The systematic review identified fourteen eligible studies, which examined the effect of paediatric TBI on five dimensions of social cognition, including emotion recognition or perception, theory of Mind (ToM), pragmatic language, moral reasoning, and social problem solving. Of these studies, eleven articles were included in subsequent meta-analyses, which included 482 children with TBI. Meta-analysis using a random-effects model revealed non-significant differences between TBI and typically developing (TD) control groups on measures of emotion perception or recognition. In contrast, children and adolescents with TBI performed significantly worse than control groups on ToM and pragmatic language tasks, with small and medium effect sizes, respectively (Hedge’s g = -0.46; -0.73). Meta-regression indicated that post-injury social cognitive deficits were not moderated by child age. While the effect of time since injury was not statistically significant, poorer social cognitive outcomes are documented soon after injury. Despite relatively intact basic social cognitive skills (i.e. emotion perception or recognition) children and adolescents with TBI are vulnerable to deficits in higher-order aspects of social cognition, including ToM and pragmatic language. These findings underscore the importance of further research, using well-validated, standardised outcome instruments, in larger paediatric TBI samples. Furthermore, longitudinal prospective studies are needed to evaluate the respective contribution of injury and non-injury factors to individual variation in outcome and recovery of social cognition after paediatric TBI.
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References
Ackerman, B. P., & Brown, E. D. (2006). Income poverty, poverty co-factors, and the adjustment of children in elementary school. Advances in Child Development and Behavior, 34, 91–129. https://doi.org/10.1016/s0065-2407(06)80005-4
Adolphs, R. (2001). The neurobiology of social cognition. Current Opinion in Neurobiology, 11(2), 231–239. https://doi.org/10.1016/s0959-4388(00)00202-6
Adolphs, R., Damasio, H., & Tranel, D. (2002). Neural systems for recognition of emotional prosody: a 3-D lesion study. Emotion, 2(1), 23–51. https://doi.org/10.1037/1528-3542.2.1.23
Anderson, V., Brown, S., & Newitt, H. (2010). What contributes to quality of life in adult survivors of childhood traumatic brain injury? Journal of Neurotrauma, 27(5), 863–870. https://doi.org/10.1089/neu.2009.1169
Anderson, V., Catroppa, C., Morse, S., Haritou, F., & Rosenfeld, J. (2000). Recovery of intellectual ability following traumatic brain injury in childhood: impact of injury severity and age at injury. Pediatric Neurosurgery, 32(6), 282–290. https://doi.org/10.1159/000028956
Atay, C., Ryan, S. J., & Lewis, F. M. (2016). “Trying to Get a Grip”: Language Competence and Self-Reported Satisfaction With Social Relationships Three Decades Post-Childhood Traumatic Brain Injury. The Journal of Head Trauma Rehabilitation, 31(5), E30-40. https://doi.org/10.1097/htr.0000000000000182
Beauchamp, M. H., & Anderson, V. (2010). SOCIAL: an integrative framework for the development of social skills. Psychological Bulletin, 136(1), 39–64. https://doi.org/10.1037/a0017768
Beauchamp, M. H., Dooley, J. J., & Anderson, V. (2013). A preliminary investigation of moral reasoning and empathy after traumatic brain injury in adolescents. Brain Injury, 27(7–8), 896–902. https://doi.org/10.3109/02699052.2013.775486
Beauchamp, M. H., Vera-Estay, E., Morasse, F., Anderson, V., & Dooley, J. (2019). Moral reasoning and decision-making in adolescents who sustain traumatic brain injury. Brain injury, 33(1), 32–39.
Blakemore, S.-J. (2008). The social brain in adolescence. Nature Reviews Neuroscience, 9(4), 267–277.
Borenstein, M., Hedges, L., Higgins, J., & Rothstein, H. (2005). Comprehensive meta-analysis version 2 (p. 104).
Bornhofen, C., & McDonald, S. (2008). Emotion perception deficits following traumatic brain injury: a review of the evidence and rationale for intervention. Journal of the International Neuropsychological Society, 14(4), 511–525. https://doi.org/10.1017/s1355617708080703
Cacioppo, J. T. (2002). Social neuroscience: understanding the pieces fosters understanding the whole and vice versa. American Psychologist, 57(11), 819–831. https://doi.org/10.1037/0003-066x.57.11.819
Catroppa, C., & Anderson, V. (2004). Recovery and predictors of language skills two years following pediatric traumatic brain injury. Brain and Language, 88(1), 68–78. https://doi.org/10.1016/s0093-934x(03)00159-7
Cattelani, R., Lombardi, F., Brianti, R., & Mazzucchi, A. (1998). Traumatic brain injury in childhood: intellectual, behavioural and social outcome into adulthood. Brain Injury, 12(4), 283–296. https://doi.org/10.1080/026990598122584
Chapman, L. A., Wade, S. L., Walz, N. C., Taylor, H. G., Stancin, T., & Yeates, K. O. (2010). Clinically significant behavior problems during the initial 18 months following early childhood traumatic brain injury. Rehabilitation Psychology, 55(1), 48–57. https://doi.org/10.1037/a0018418
Crowe, L., Babl, F., Anderson, V., & Catroppa, C. (2009). The epidemiology of paediatric head injuries: data from a referral centre in Victoria. Australia. Journal of Paediatrics and Child Health, 45(6), 346–350. https://doi.org/10.1111/j.1440-1754.2009.01499.x
Dennis, M., Barnes, M. A., Donnelly, R. E., Wilkinson, M., & Humphreys, R. P. (1996). Appraising and managing knowledge: Metacognitive skills after childhood head injury. Developmental Neuropsychology, 12(1), 77–103. https://doi.org/10.1080/87565649609540641
Dennis, M., Simic, N., Bigler, E. D., Abildskov, T., Agostino, A., Taylor, H. G., et al. (2013). Cognitive, affective, and conative theory of mind (ToM) in children with traumatic brain injury. Developmental Cognitive Neuroscience, 5, 25–39. https://doi.org/10.1016/j.dcn.2012.11.006
Dennis, M., Spiegler, B. J., Simic, N., Sinopoli, K. J., Wilkinson, A., Yeates, K. O., et al. (2014). Functional plasticity in childhood brain disorders: when, what, how, and whom to assess. Neuropsychology review, 24(4), 389–408.
Donders, J., & Warschausky, S. (2007). Neurobehavioral outcomes after early versus late childhood traumatic brain injury. The Journal of head trauma rehabilitation, 22(5), 296–302.
Edwards, A., Elwyn, G., & Mulley, A. (2002). Explaining risks: turning numerical data into meaningful pictures. BMJ, 324(7341), 827–830. https://doi.org/10.1136/bmj.324.7341.827
Evans, J. S. (2008). Dual-processing accounts of reasoning, judgment, and social cognition. Annual Review of Psychology, 59, 255–278. https://doi.org/10.1146/annurev.psych.59.103006.093629
Faul, M., Xu, L., Wald, M. M., Coronado, V., & Dellinger, A. M. (2010). Traumatic brain injury in the United States: national estimates of prevalence and incidence, 2002–2006. Injury Prevention, 16(Suppl 1), A268–A268. https://doi.org/10.1136/ip.2010.029215.951
Frischen, A., Bayliss, A. P., & Tipper, S. P. (2007). Gaze cueing of attention: visual attention, social cognition, and individual differences. Psychological Bulletin, 133(4), 694–724. https://doi.org/10.1037/0033-2909.133.4.694
Ganesalingam, K., Yeates, K. O., Sanson, A., & Anderson, V. (2007). Social problem-solving skills following childhood traumatic brain injury and its association with self-regulation and social and behavioural functioning. Journal of Neuropsychology, 1(Pt 2), 149–170. https://doi.org/10.1348/174866407x185300
Gates, N. J., & March, E. G. (2016). A Neuropsychologist’s Guide To Undertaking a Systematic Review for Publication: Making the most of PRISMA Guidelines. Neuropsychology Review, 26(2), 109–120. https://doi.org/10.1007/s11065-016-9318-0
Genova, H. M., Haight, A., Natsheh, J. Y., DeLuca, J., & Lengenfelder, J. (2019). The Relationship Between Social Communication and Social Functioning in Pediatric TBI: A Pilot Study [Original Research]. Frontiers in Neurology, 10(850). https://doi.org/10.3389/fneur.2019.00850
Green, M. F., Olivier, B., Crawley, J. N., Penn, D. L., & Silverstein, S. (2005). Social cognition in schizophrenia: recommendations from the measurement and treatment research to improve cognition in schizophrenia new approaches conference. Schizophrenia Bulletin, 31(4), 882–887. https://doi.org/10.1093/schbul/sbi049
Green, R. E., Melo, B., Christensen, B., Ngo, L. A., Monette, G., & Bradbury, C. (2008). Measuring premorbid IQ in traumatic brain injury: an examination of the validity of the Wechsler Test of Adult Reading (WTAR). Journal of Clinical and Experimental Neuropsychology, 30(2), 163–172. https://doi.org/10.1080/13803390701300524
Guastella, A. J., Einfeld, S. L., Gray, K. M., Rinehart, N. J., Tonge, B. J., Lambert, T. J., & Hickie, I. B. (2010). Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biological Psychiatry, 67(7), 692–694. https://doi.org/10.1016/j.biopsych.2009.09.020
Guralnick, M. J., Neville, B., Connor, R. T., & Hammond, M. A. (2003). Family factors associated with the peer social competence of young children with mild delays. American Journal of Mental Retardation, 108(4), 272–287. https://doi.org/10.1352/0895-8017(2003)108%3c272:Ffawtp%3e2.0.Co;2
Haarbauer-Krupa, J., King, T. Z., Wise, J., Gillam, S., Trapani, J., Weissman, B., & DePompei, R. (2019). Early elementary school outcome in children with a history of traumatic brain injury before age 6 years. The Journal of head trauma rehabilitation, 34(2), 111–121.
Hanten, G., Wilde, E. A., Menefee, D. S., Li, X., Lane, S., Vasquez, C., et al. (2008). Correlates of social problem solving during the first year after traumatic brain injury in children. Neuropsychology, 22(3), 357.
Hedges, L. V. (1981). Distribution theory for Glass's estimator of effect size and related estimators. Journal of Educational Statistics, 6(2), 107–128.
Hein, G., & Singer, T. (2010). Neuroscience meets social psychology: An integrative approach to human empathy and prosocial behavior. Prosocial motives, emotions, and behavior: The better angels of our nature, 109–125.
Hermans, K., Achterhof, R., Myin-Germeys, I., Kasanova, Z., Kirtley, O., & Schneider, M. (2019). Improving ecological validity in research on social cognition. In Social Cognition in Psychosis (pp. 249–268). Elsevier.
Hornak, J., Rolls, E. T., & Wade, D. (1996). Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage. Neuropsychologia, 34(4), 247–261. https://doi.org/10.1016/0028-3932(95)00106-9
Levy, N. K., & Milgram, N. (2016). Cognitive contributions to theory of mind ability in children with a traumatic head injury. Child Neuropsychology, 22(2), 177–196. https://doi.org/10.1080/09297049.2014.985642
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gotzsche, P. C., Ioannidis, J. P., et al. (2009). The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Journal of Clinical Epidemiology, 62(10), e1-34. https://doi.org/10.1016/j.jclinepi.2009.06.006
Lipsey, M., & Wilson, D. (2001). Practical meta-analysis Sage Publications.
Masten, A. S., Hubbard, J. J., Gest, S. D., Tellegen, A., Garmezy, N., & Ramirez, M. (1999). Competence in the context of adversity: pathways to resilience and maladaptation from childhood to late adolescence. Development and Psychopathology, 11(1), 143–169. https://doi.org/10.1017/s0954579499001996
Mateer, C. A., & Sira, C. S. (2006). Cognitive and emotional consequences of TBI: intervention strategies for vocational rehabilitation. NeuroRehabilitation, 21(4), 315–326.
McDonald, S., English, T., Randall, R., Longman, T., Togher, L., & Tate, R. L. (2013). Assessing social cognition and pragmatic language in adolescents with traumatic brain injuries. Journal of the International Neuropsychological Society, 19(5), 528–538. https://doi.org/10.1017/s1355617713000039
McDonald, S., Flanagan, S., Rollins, J., & Kinch, J. (2003). TASIT: A new clinical tool for assessing social perception after traumatic brain injury. The Journal of Head Trauma Rehabilitation, 18(3), 219–238. https://doi.org/10.1097/00001199-200305000-00001
McDonald, S., & Pearce, S. (1996). Clinical insights into pragmatic theory: frontal lobe deficits and sarcasm. Brain and Language, 53(1), 81–104. https://doi.org/10.1006/brln.1996.0038
McDonald, S., Rushby, J., Kelly, M., & de Sousa, A. (2014). Disorders of emotion and social cognition following traumatic brain injury.
McGann, W., Werven, G., & Douglas, M. M. (1997). Social competence and head injury: a practical approach. Brain Injury, 11(9), 621–628. https://doi.org/10.1080/026990597123179
Moher, D., Liberati, A., Tetzlaff, J., & Altman, D. G. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Annals of Internal Medicine, 151(4), 264–269, w264. https://doi.org/10.7326/0003-4819-151-4-200908180-00135
Muscara, F., Catroppa, C., & Anderson, V. (2008). The impact of injury severity on executive function 7–10 years following pediatric traumatic brain injury. Developmental Neuropsychology, 33(5), 623–636. https://doi.org/10.1080/87565640802171162
Ownsworth, T., & Fleming, J. (2005). The relative importance of metacognitive skills, emotional status, and executive function in psychosocial adjustment following acquired brain injury. The Journal of Head Trauma Rehabilitation, 20(4), 315–332. https://doi.org/10.1097/00001199-200507000-00004
Peterson, J., Welch, V., Losos, M., & Tugwell, P. (2011). The Newcastle-Ottawa scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa: Ottawa Hospital Research Institute.
Radcliffe, J., Bunin, G. R., Sutton, L. N., Goldwein, J. W., & Phillips, P. C. (1994). Cognitive deficits in long-term survivors of childhood medulloblastoma and other noncortical tumors: age-dependent effects of whole brain radiation. International Journal of Developmental Neuroscience, 12(4), 327–334. https://doi.org/10.1016/0736-5748(94)90081-7
Robinson, K. E., Fountain-Zaragoza, S., Dennis, M., Taylor, H. G., Bigler, E. D., Rubin, K., et al. (2014). Executive functions and theory of mind as predictors of social adjustment in childhood traumatic brain injury. Journal of Neurotrauma, 31(22), 1835–1842. https://doi.org/10.1089/neu.2014.3422
Rosema, S., Crowe, L., & Anderson, V. (2012). Social function in children and adolescents after traumatic brain injury: a systematic review 1989–2011. Journal of Neurotrauma, 29(7), 1277–1291. https://doi.org/10.1089/neu.2011.2144
Ryan, N. P., Anderson, V., Godfrey, C., Beauchamp, M. H., Coleman, L., Eren, S., et al. (2014). Predictors of very-long-term sociocognitive function after pediatric traumatic brain injury: evidence for the vulnerability of the immature “social brain.” Journal of neurotrauma, 31(7), 649–657.
Ryan, N. P., Anderson, V., Godfrey, C., Eren, S., Rosema, S., Taylor, K., & Catroppa, C. (2013). Social communication mediates the relationship between emotion perception and externalizing behaviors in young adult survivors of pediatric traumatic brain injury (TBI). International Journal of Developmental Neuroscience, 31(8), 811–819. https://doi.org/10.1016/j.ijdevneu.2013.10.002
Ryan, N. P., Catroppa, C., Beare, R., Coleman, L., Ditchfield, M., Crossley, L., et al. (2015). Predictors of longitudinal outcome and recovery of pragmatic language and its relation to externalizing behaviour after pediatric traumatic brain injury. Brain and language, 142, 86–95.
Ryan, N. P., Catroppa, C., Cooper, J. M., Beare, R., Ditchfield, M., Coleman, L., et al. (2015). The emergence of age-dependent social cognitive deficits after generalized insult to the developing brain: A longitudinal prospective analysis using susceptibility-weighted imaging. Human brain mapping, 36(5), 1677–1691.
Ryan, N. P., Genc, S., Beauchamp, M. H., Yeates, K. O., Hearps, S., Catroppa, C., et al. (2017). White matter microstructure predicts longitudinal social cognitive outcomes after paediatric traumatic brain injury: a diffusion tensor imaging study. Psychological Medicine, 48(4), 679–691. https://doi.org/10.1017/s0033291717002057
Sanderson, S., Tatt, I. D., & Higgins, J. P. (2007). Tools for assessing quality and susceptibility to bias in observational studies in epidemiology: a systematic review and annotated bibliography. International Journal of Epidemiology, 36(3), 666–676. https://doi.org/10.1093/ije/dym018
Sebastian, C. L., Fontaine, N. M., Bird, G., Blakemore, S.-J., De Brito, S. A., McCrory, E. J., & Viding, E. (2012). Neural processing associated with cognitive and affective Theory of Mind in adolescents and adults. Social cognitive and affective neuroscience, 7(1), 53–63.
Singer, T., Critchley, H. D., & Preuschoff, K. (2009). A common role of insula in feelings, empathy and uncertainty. Trends in cognitive sciences, 13(8), 334–340.
Sirois, K., Tousignant, B., Boucher, N., Achim, A. M., Beauchamp, M. H., Bedell, G., et al. (2017). The contribution of social cognition in predicting social participation following moderate and severe TBI in youth. Neuropsychological Rehabilitation, 29(9), 1383–1398. https://doi.org/10.1080/09602011.2017.1413987
Stang, A. (2010). Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. European Journal of Epidemiology, 25(9), 603–605. https://doi.org/10.1007/s10654-010-9491-z
Sterne, J. A., Sutton, A. J., Ioannidis, J. P., Terrin, N., Jones, D. R., Lau, J., et al. (2011). Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ, 343, d4002. https://doi.org/10.1136/bmj.d4002
Stovold, E., Beecher, D., Foxlee, R., & Noel-Storr, A. (2014). Study flow diagrams in Cochrane systematic review updates: an adapted PRISMA flow diagram. Systematic Reviews, 3, 54. https://doi.org/10.1186/2046-4053-3-54
Turkstra, L. S., Williams, W. H., Tonks, J., & Frampton, I. (2008). Measuring social cognition in adolescents: implications for students with TBI returning to school. NeuroRehabilitation, 23(6), 501–509.
van Tol, E., Gorter, J. W., DeMatteo, C., & Meester-Delver, A. (2011). Participation outcomes for children with acquired brain injury: a narrative review. Brain Injury, 25(13–14), 1279–1287. https://doi.org/10.3109/02699052.2011.613089
Walz, N. C., Yeates, K. O., Taylor, H. G., Stancin, T., & Wade, S. L. (2009). First-order theory of mind skills shortly after traumatic brain injury in 3- to 5-year-old children. Developmental Neuropsychology, 34(4), 507–519. https://doi.org/10.1080/87565640902964490
Yeates, K. O., Bigler, E. D., Dennis, M., Gerhardt, C. A., Rubin, K. H., Stancin, T., et al. (2007). Social outcomes in childhood brain disorder: a heuristic integration of social neuroscience and developmental psychology. Psychological Bulletin, 133(3), 535–556. https://doi.org/10.1037/0033-2909.133.3.535
Yeates, K. O., Swift, E., Taylor, H. G., Wade, S. L., Drotar, D., Stancin, T., & Minich, N. (2004). Short- and long-term social outcomes following pediatric traumatic brain injury. Journal of the International Neuropsychological Society, 10(3), 412–426. https://doi.org/10.1017/s1355617704103093
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We would like to thank Dr Alexia Palvis and Dr Lauren Fitzpatrick for comments on an earlier version of this manuscript, as well as Dr Celia Godfrey and Dr Vicki Anderson for keywords searches and systematic review advice.
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On, Z., Ryan, N.P., Konjarski, M. et al. Social Cognition in Paediatric Traumatic Brain Injury: A Systematic Review and Meta-analysis. Neuropsychol Rev 32, 127–148 (2022). https://doi.org/10.1007/s11065-021-09488-2
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DOI: https://doi.org/10.1007/s11065-021-09488-2