Skip to main content
Top

Open Access 19-12-2023 | Central Nervous System Trauma | Review

A Biopsychosocial Framework for Apathy Following Moderate to Severe Traumatic Brain Injury: A Systematic Review and Meta-analysis

Authors: Halle Quang, Travis Wearne, Michaela Filipcikova, Nhi Pham, Nhi Nguyen, Skye McDonald

Published in: Neuropsychology Review

Login to get access

Abstract

Apathy, the deficit of goal-directed behaviour, is well recognised as one of the most debilitating syndromes after moderate-to-severe traumatic brain injury (TBI). However, mechanisms underlying apathy, or at least factors associated with apathy, are sporadically reported. Based on a biopsychosocial framework, this systematic review and meta-analysis synthesised evidence regarding neurobiological, socio-environmental and individual factors associated with apathy. Our searches identified 21 studies satisfying inclusion and exclusion criteria. Results showed that the majority of work has focused on cognitive dysfunction, TBI-related factors, demographic variables and psychological correlates of apathy, while evidence for neural substrates and socio-cultural and premorbid aspects is scant. Overall, the current literature suggests that TBI-related and patient demographic factors did not contribute to apathy after TBI, whereas complex neurocognitive alterations, socio-environmental and cultural factors as well as patients’ self-related factors may be important components. The evidence points to the multifaceted interplay of certain biopsychosocial contributors to apathy and suggests future investigations of more complex behavioural traits, cultural elements and pre-injury levels to better characterise the aetiology of this detrimental impairment after TBI.
Appendix
Available only for authorised users
Literature
go back to reference Anderson, V., Hearps, S. J., Catroppa, C., Beauchamp, M. H., & Ryan, N. P. (2022). What predicts persisting social impairment following pediatric traumatic brain injury: contribution of a biopsychosocial approach. Psychological Medicine, 1–12. Anderson, V., Hearps, S. J., Catroppa, C., Beauchamp, M. H., & Ryan, N. P. (2022). What predicts persisting social impairment following pediatric traumatic brain injury: contribution of a biopsychosocial approach. Psychological Medicine, 1–12.
go back to reference Andersson, S., & Bergedalen, A.-M. (2002). Cognitive correlates of apathy in traumatic brain injury. Cognitive and Behavioral Neurology, 15(3), 184–191. Andersson, S., & Bergedalen, A.-M. (2002). Cognitive correlates of apathy in traumatic brain injury. Cognitive and Behavioral Neurology, 15(3), 184–191.
go back to reference Arafat, S., Chowdhury, H. R., Qusar, M., & Hafez, M. (2016). Cross cultural adaptation & psychometric validation of research instruments: A methodological review. Journal of Behavioral Health, 5(3), 129–136.CrossRef Arafat, S., Chowdhury, H. R., Qusar, M., & Hafez, M. (2016). Cross cultural adaptation & psychometric validation of research instruments: A methodological review. Journal of Behavioral Health, 5(3), 129–136.CrossRef
go back to reference Arnould, A., Rochat, L., Dromer, E., Azouvi, P., & Van Der Linden, M. (2018c). Does multitasking mediate the relationships between episodic memory, attention, executive functions and apathetic manifestations in traumatic brain injury? Journal of Neuropsychology, 12(1), 101–119. https://doi.org/10.1111/jnp.12107CrossRefPubMed Arnould, A., Rochat, L., Dromer, E., Azouvi, P., & Van Der Linden, M. (2018c). Does multitasking mediate the relationships between episodic memory, attention, executive functions and apathetic manifestations in traumatic brain injury? Journal of Neuropsychology, 12(1), 101–119. https://​doi.​org/​10.​1111/​jnp.​12107CrossRefPubMed
go back to reference Bivona, U., Costa, A., Contrada, M., Silvestro, D., Azicnuda, E., Aloisi, M., Catania, G., Ciurli, P., Guariglia, C., Caltagirone, C., Formisano, R., & Prigatano, G. P. (2019). Depression, apathy and impaired self-awareness following severe traumatic brain injury: A preliminary investigation. Brain Injury, 33(9), 1245–1256. https://doi.org/10.1080/02699052.2019.1641225CrossRefPubMed Bivona, U., Costa, A., Contrada, M., Silvestro, D., Azicnuda, E., Aloisi, M., Catania, G., Ciurli, P., Guariglia, C., Caltagirone, C., Formisano, R., & Prigatano, G. P. (2019). Depression, apathy and impaired self-awareness following severe traumatic brain injury: A preliminary investigation. Brain Injury, 33(9), 1245–1256. https://​doi.​org/​10.​1080/​02699052.​2019.​1641225CrossRefPubMed
go back to reference Carroll, L., Cassidy, J., Holm, L., Kraus, J., Coronado, V., & WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. (2004). Methodological issues and research recommendations for mild traumatic brain injury: The WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. Journal of Rehabilitation Medicine, 43(1), 113–125.CrossRef Carroll, L., Cassidy, J., Holm, L., Kraus, J., Coronado, V., & WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. (2004). Methodological issues and research recommendations for mild traumatic brain injury: The WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. Journal of Rehabilitation Medicine, 43(1), 113–125.CrossRef
go back to reference De Simoni, S., Jenkins, P. O., Bourke, N. J., Fleminger, J. J., Hellyer, P. J., Jolly, A. E., Patel, M. C., Cole, J. H., Leech, R., & Sharp, D. J. (2018). Altered caudate connectivity is associated with executive dysfunction after traumatic brain injury. Brain, 141(1), 148–164. https://doi.org/10.1093/brain/awx309CrossRefPubMed De Simoni, S., Jenkins, P. O., Bourke, N. J., Fleminger, J. J., Hellyer, P. J., Jolly, A. E., Patel, M. C., Cole, J. H., Leech, R., & Sharp, D. J. (2018). Altered caudate connectivity is associated with executive dysfunction after traumatic brain injury. Brain, 141(1), 148–164. https://​doi.​org/​10.​1093/​brain/​awx309CrossRefPubMed
go back to reference Dewan, M. C., Rattani, A., Gupta, S., Baticulon, R. E., Hung, Y.-C., Punchak, M., Agrawal, A., Adeleye, A. O., Shrime, M. G., & Rubiano, A. M. (2018). Estimating the global incidence of traumatic brain injury. Journal of Neurosurgery, 130(4), 1080–1097.CrossRefPubMed Dewan, M. C., Rattani, A., Gupta, S., Baticulon, R. E., Hung, Y.-C., Punchak, M., Agrawal, A., Adeleye, A. O., Shrime, M. G., & Rubiano, A. M. (2018). Estimating the global incidence of traumatic brain injury. Journal of Neurosurgery, 130(4), 1080–1097.CrossRefPubMed
go back to reference Diaz, A. P., Schwarzbold, M. L., Thais, M. E., Hohl, A., Bertotti, M. M., Schmoeller, R., Nunes, J. C., Prediger, R., Linhares, M. N., & Guarnieri, R. (2012). Psychiatric disorders and health-related quality of life after severe traumatic brain injury: A prospective study. Journal of Neurotrauma, 29(6), 1029–1037.CrossRefPubMed Diaz, A. P., Schwarzbold, M. L., Thais, M. E., Hohl, A., Bertotti, M. M., Schmoeller, R., Nunes, J. C., Prediger, R., Linhares, M. N., & Guarnieri, R. (2012). Psychiatric disorders and health-related quality of life after severe traumatic brain injury: A prospective study. Journal of Neurotrauma, 29(6), 1029–1037.CrossRefPubMed
go back to reference Filipčíková, M., Quang, H., Cassel, A., Darke, L., Wilson, E., Wearne, T., Rosenberg, H., & McDonald, S. (2022). Exploring neuropsychological underpinnings of poor communication after traumatic brain injury: the role of apathy, disinhibition and social cognition. International Journal of Language & Communication Disorders. Filipčíková, M., Quang, H., Cassel, A., Darke, L., Wilson, E., Wearne, T., Rosenberg, H., & McDonald, S. (2022). Exploring neuropsychological underpinnings of poor communication after traumatic brain injury: the role of apathy, disinhibition and social cognition. International Journal of Language & Communication Disorders.
go back to reference Gray, J. M., Shepherd, M., McKinlay, W. W., Robertson, I., & Pentland, B. (1994). Negative symptoms in the traumatically brain-injured during the first year postdischarge, and their effect on rehabilitation status, work status and family burden. Clinical Rehabilitation, 8(3), 188–197.CrossRef Gray, J. M., Shepherd, M., McKinlay, W. W., Robertson, I., & Pentland, B. (1994). Negative symptoms in the traumatically brain-injured during the first year postdischarge, and their effect on rehabilitation status, work status and family burden. Clinical Rehabilitation, 8(3), 188–197.CrossRef
go back to reference Hogeveen, J., Hauner, K. K., Chau, A., Krueger, F., & Grafman, J. (2017). Impaired valuation leads to increased apathy following ventromedial prefrontal cortex damage. Cerebral Cortex, 27(2), 1401–1408.PubMed Hogeveen, J., Hauner, K. K., Chau, A., Krueger, F., & Grafman, J. (2017). Impaired valuation leads to increased apathy following ventromedial prefrontal cortex damage. Cerebral Cortex, 27(2), 1401–1408.PubMed
go back to reference Hoofien, D., Gilboa, A., Vakil, E., & Donovick, P. J. (2001). Traumatic brain injury (TBI) 10–20 years later: A comprehensive outcome study of psychiatric symptomatology, cognitive abilities and psychosocial functioning. Brain Injury, 15(3), 189–209.CrossRefPubMed Hoofien, D., Gilboa, A., Vakil, E., & Donovick, P. J. (2001). Traumatic brain injury (TBI) 10–20 years later: A comprehensive outcome study of psychiatric symptomatology, cognitive abilities and psychosocial functioning. Brain Injury, 15(3), 189–209.CrossRefPubMed
go back to reference Kales, H. C., Gitlin, L. N., & Lyketsos, C. G. (2015). Assessment and management of behavioral and psychological symptoms of dementia. Bmj, 350. Kales, H. C., Gitlin, L. N., & Lyketsos, C. G. (2015). Assessment and management of behavioral and psychological symptoms of dementia. Bmj, 350.
go back to reference Kilmer, R. P., Demakis, G. J., Hammond, F. M., Grattan, K. E., Cook, J. R., & Kornev, A. A. (2006). Use of the neuropsychiatric inventory in traumatic brain injury: A pilot investigation. Rehabilitation Psychology, 51(3), 232.CrossRef Kilmer, R. P., Demakis, G. J., Hammond, F. M., Grattan, K. E., Cook, J. R., & Kornev, A. A. (2006). Use of the neuropsychiatric inventory in traumatic brain injury: A pilot investigation. Rehabilitation Psychology, 51(3), 232.CrossRef
go back to reference Knutson, K. M., Dal Monte, O., Raymont, V., Wassermann, E. M., Krueger, F., & Grafman, J. (2014). Neural correlates of apathy revealed by lesion mapping in participants with traumatic brain injuries. Human Brain Mapping, 35(3), 943–953.CrossRefPubMed Knutson, K. M., Dal Monte, O., Raymont, V., Wassermann, E. M., Krueger, F., & Grafman, J. (2014). Neural correlates of apathy revealed by lesion mapping in participants with traumatic brain injuries. Human Brain Mapping, 35(3), 943–953.CrossRefPubMed
go back to reference Kumfor, F., Zhen, A., Hodges, J. R., Piguet, O., & Irish, M. (2018). Apathy in Alzheimer’s disease and frontotemporal dementia: Distinct clinical profiles and neural correlates. Cortex, 103, 350–359.CrossRefPubMed Kumfor, F., Zhen, A., Hodges, J. R., Piguet, O., & Irish, M. (2018). Apathy in Alzheimer’s disease and frontotemporal dementia: Distinct clinical profiles and neural correlates. Cortex, 103, 350–359.CrossRefPubMed
go back to reference Lane‐Brown, A., & Tate, R. (2009b). Interventions for apathy after traumatic brain injury. Cochrane Database of Systematic Reviews, (2). Lane‐Brown, A., & Tate, R. (2009b). Interventions for apathy after traumatic brain injury. Cochrane Database of Systematic Reviews, (2).
go back to reference Le Heron, C., Holroyd, C. B., Salamone, J., & Husain, M. (2019). Brain mechanisms underlying apathy. Journal of Neurology, Neurosurgery & Psychiatry, 90(3), 302–312.CrossRef Le Heron, C., Holroyd, C. B., Salamone, J., & Husain, M. (2019). Brain mechanisms underlying apathy. Journal of Neurology, Neurosurgery & Psychiatry, 90(3), 302–312.CrossRef
go back to reference Levy, R., & Dubois, B. (2006). Apathy and the functional anatomy of the prefrontal cortex–basal ganglia circuits. Cerebral Cortex, 16(7), 916–928.CrossRefPubMed Levy, R., & Dubois, B. (2006). Apathy and the functional anatomy of the prefrontal cortex–basal ganglia circuits. Cerebral Cortex, 16(7), 916–928.CrossRefPubMed
go back to reference Marin, R. S. (1991). Apathy: a neuropsychiatric syndrome. The Journal of Neuropsychiatry and Clinical Neurosciences, 3(3), 243–254. Marin, R. S. (1991). Apathy: a neuropsychiatric syndrome. The Journal of Neuropsychiatry and Clinical Neurosciences, 3(3), 243–254.
go back to reference Marin, R. S., & Wilkosz, P. A. (2005). Disorders of diminished motivation. The Journal of Head Trauma Rehabilitation, 20(4), 377–388.CrossRefPubMed Marin, R. S., & Wilkosz, P. A. (2005). Disorders of diminished motivation. The Journal of Head Trauma Rehabilitation, 20(4), 377–388.CrossRefPubMed
go back to reference Mathias, J. L., & Wheaton, P. (2007). Changes in attention and information-processing speed following severe traumatic brain injury: A meta-analytic review. Neuropsychology, 21(2), 212.CrossRefPubMed Mathias, J. L., & Wheaton, P. (2007). Changes in attention and information-processing speed following severe traumatic brain injury: A meta-analytic review. Neuropsychology, 21(2), 212.CrossRefPubMed
go back to reference McDonald, S., Code, C., & Togher, L. (2013). Social and communication disorders following traumatic brain injury. Psychology press. McDonald, S., Code, C., & Togher, L. (2013). Social and communication disorders following traumatic brain injury. Psychology press.
go back to reference Monsalve, B. C., Guitart, M. B., López, R., Vilasar, A. B., & Quemada, J. I. (2012). Psychopathological evaluation of traumatic brain injury patients with the Neuropsychiatric Inventory. Rev Psiquiatr Salud Ment (English Edition), 5(3), 160–166.CrossRef Monsalve, B. C., Guitart, M. B., López, R., Vilasar, A. B., & Quemada, J. I. (2012). Psychopathological evaluation of traumatic brain injury patients with the Neuropsychiatric Inventory. Rev Psiquiatr Salud Ment (English Edition), 5(3), 160–166.CrossRef
go back to reference Morris, L. A., O'Callaghan, C., & Le Heron, C. (2022). Disordered decision making: a cognitive framework for apathy and impulsivity in Huntington’s disease. Movement Disorders. Morris, L. A., O'Callaghan, C., & Le Heron, C. (2022). Disordered decision making: a cognitive framework for apathy and impulsivity in Huntington’s disease. Movement Disorders.
go back to reference Nguyen, T., & Li, X. (2020). Understanding public-stigma and self-stigma in the context of dementia: A systematic review of the global literature. Dementia, 19(2), 148–181.CrossRefPubMed Nguyen, T., & Li, X. (2020). Understanding public-stigma and self-stigma in the context of dementia: A systematic review of the global literature. Dementia, 19(2), 148–181.CrossRefPubMed
go back to reference Niemeier, J. P., Perrin, P. B., Holcomb, M. G., Nersessova, K. S., & Rolston, C. D. (2013). Factor structure, reliability, and validity of the Frontal Systems Behavior Scale (FrSBe) in an acute traumatic brain injury population. Rehabilitation Psychology, 58(1), 51.CrossRefPubMed Niemeier, J. P., Perrin, P. B., Holcomb, M. G., Nersessova, K. S., & Rolston, C. D. (2013). Factor structure, reliability, and validity of the Frontal Systems Behavior Scale (FrSBe) in an acute traumatic brain injury population. Rehabilitation Psychology, 58(1), 51.CrossRefPubMed
go back to reference Peskind, E. R., Brody, D., Cernak, I., McKee, A., & Ruff, R. L. (2013). Military- and sports-related mild traumatic brain injury: Clinical presentation, management, and long-term consequences. The Journal of Clinical Psychiatry, 74(2), 11946.CrossRef Peskind, E. R., Brody, D., Cernak, I., McKee, A., & Ruff, R. L. (2013). Military- and sports-related mild traumatic brain injury: Clinical presentation, management, and long-term consequences. The Journal of Clinical Psychiatry, 74(2), 11946.CrossRef
go back to reference Ponsford, J. (2013). Factors contributing to outcome following traumatic brain injury. NeuroRehabilitation, 32(4), 803–815.CrossRefPubMed Ponsford, J. (2013). Factors contributing to outcome following traumatic brain injury. NeuroRehabilitation, 32(4), 803–815.CrossRefPubMed
go back to reference Quang, H., Kumfor, F., Balleine, B., Nguyen, T.-V., Nguyen, T.-Q., Nguyen, M.-N., & McDonald, S. (2022a). Contributions of intrinsic and extrinsic reward sensitivity to apathy: evidence from traumatic brain injury. Neuropsychology. Quang, H., Kumfor, F., Balleine, B., Nguyen, T.-V., Nguyen, T.-Q., Nguyen, M.-N., & McDonald, S. (2022a). Contributions of intrinsic and extrinsic reward sensitivity to apathy: evidence from traumatic brain injury. Neuropsychology.
go back to reference Quang, H., Le Heron, C., Balleine, B., Nguyen, T.-V., Nguyen, T.-Q., Nguyen, M.-N., Kumfor, F., & McDonald, S. (2023). Reduced sensitivity to background reward underlies apathy after traumatic brain injury: insights from an ecological foraging framework. Neuroscience. Quang, H., Le Heron, C., Balleine, B., Nguyen, T.-V., Nguyen, T.-Q., Nguyen, M.-N., Kumfor, F., & McDonald, S. (2023). Reduced sensitivity to background reward underlies apathy after traumatic brain injury: insights from an ecological foraging framework. Neuroscience.
go back to reference Quang, H., McDonald, S., Huynh-Le, P., Nguyen, T.-V., Le, N.-A., Lam-Nguyen, N.-T., & Kumfor, F. (2021a). Apathy in a high prevalence population of moderate to severe traumatic brain injury: an investigation in Vietnam. Neuropsychology. Quang, H., McDonald, S., Huynh-Le, P., Nguyen, T.-V., Le, N.-A., Lam-Nguyen, N.-T., & Kumfor, F. (2021a). Apathy in a high prevalence population of moderate to severe traumatic brain injury: an investigation in Vietnam. Neuropsychology.
go back to reference Quang, H., Sin, K., Kumfor, F., & McDonald, S. (2022b). Adaptation, validation and preliminary standardisation of the frontal systems behaviour scale–apathy subscale and the dimensional apathy scale in vietnamese healthy samples. Journal of the International Neuropsychological Society, 28(3), 300–310.CrossRefPubMed Quang, H., Sin, K., Kumfor, F., & McDonald, S. (2022b). Adaptation, validation and preliminary standardisation of the frontal systems behaviour scale–apathy subscale and the dimensional apathy scale in vietnamese healthy samples. Journal of the International Neuropsychological Society, 28(3), 300–310.CrossRefPubMed
go back to reference Quang, H., Wong, S., Husain, M., Piguet, O., Hodges, J. R., Irish, M., & Kumfor, F. (2021b). Beyond language impairment: Profiles of apathy in primary progressive aphasia. Cortex, 139, 73–85.CrossRefPubMed Quang, H., Wong, S., Husain, M., Piguet, O., Hodges, J. R., Irish, M., & Kumfor, F. (2021b). Beyond language impairment: Profiles of apathy in primary progressive aphasia. Cortex, 139, 73–85.CrossRefPubMed
go back to reference Radakovic, R., & Abrahams, S. (2018). Multidimensional apathy: Evidence from neurodegenerative disease. Current Opinion in Behavioral Sciences, 22, 42–49.CrossRef Radakovic, R., & Abrahams, S. (2018). Multidimensional apathy: Evidence from neurodegenerative disease. Current Opinion in Behavioral Sciences, 22, 42–49.CrossRef
go back to reference Roy, D., Jayaram, G., Vassila, A., Keach, S., & Rao, V. (2015). Depression after traumatic brain injury: A biopsychosocial cultural perspective. Asian Journal of Psychiatry, 13, 56–61.CrossRefPubMed Roy, D., Jayaram, G., Vassila, A., Keach, S., & Rao, V. (2015). Depression after traumatic brain injury: A biopsychosocial cultural perspective. Asian Journal of Psychiatry, 13, 56–61.CrossRefPubMed
go back to reference Simpson, G., Mohr, R., & Redman, A. (2000). Cultural variations in the understanding of traumatic brain injury and brain injury rehabilitation. Brain Injury, 14(2), 125–140.CrossRefPubMed Simpson, G., Mohr, R., & Redman, A. (2000). Cultural variations in the understanding of traumatic brain injury and brain injury rehabilitation. Brain Injury, 14(2), 125–140.CrossRefPubMed
go back to reference Tay, J., Morris, R. G., & Markus, H. S. (2021). Apathy after stroke: Diagnosis, mechanisms, consequences, and treatment. International Journal of Stroke, 16(5), 510–518.CrossRefPubMedPubMedCentral Tay, J., Morris, R. G., & Markus, H. S. (2021). Apathy after stroke: Diagnosis, mechanisms, consequences, and treatment. International Journal of Stroke, 16(5), 510–518.CrossRefPubMedPubMedCentral
go back to reference Whiteneck, G. G., Gerhart, K. A., & Cusick, C. P. (2004). Identifying environmental factors that influence the outcomes of people with traumatic brain injury. The Journal of Head Trauma Rehabilitation, 19(3), 191–204.CrossRefPubMed Whiteneck, G. G., Gerhart, K. A., & Cusick, C. P. (2004). Identifying environmental factors that influence the outcomes of people with traumatic brain injury. The Journal of Head Trauma Rehabilitation, 19(3), 191–204.CrossRefPubMed
go back to reference Wong, A. W., Ng, S., Dashner, J., Baum, M. C., Hammel, J., Magasi, S., Lai, J.-S., Carlozzi, N. E., Tulsky, D. S., & Miskovic, A. (2017). Relationships between environmental factors and participation in adults with traumatic brain injury, stroke, and spinal cord injury: A cross-sectional multi-center study. Quality of Life Research, 26(10), 2633–2645.CrossRefPubMed Wong, A. W., Ng, S., Dashner, J., Baum, M. C., Hammel, J., Magasi, S., Lai, J.-S., Carlozzi, N. E., Tulsky, D. S., & Miskovic, A. (2017). Relationships between environmental factors and participation in adults with traumatic brain injury, stroke, and spinal cord injury: A cross-sectional multi-center study. Quality of Life Research, 26(10), 2633–2645.CrossRefPubMed
Metadata
Title
A Biopsychosocial Framework for Apathy Following Moderate to Severe Traumatic Brain Injury: A Systematic Review and Meta-analysis
Authors
Halle Quang
Travis Wearne
Michaela Filipcikova
Nhi Pham
Nhi Nguyen
Skye McDonald
Publication date
19-12-2023
Publisher
Springer US
Published in
Neuropsychology Review
Print ISSN: 1040-7308
Electronic ISSN: 1573-6660
DOI
https://doi.org/10.1007/s11065-023-09620-4