key: cord-0316740-pr6nlvo3
authors: Picon, E. L.; Todorova, E.; Palombo, D. J.; Perez, D. L.; Howard, A.; Silverberg, N. D.
title: Memory perfectionism is associated with persistent memory complaints after concussion
date: 2021-11-16
journal: nan
DOI: 10.1101/2021.11.15.21266362
sha: ef1c877c0b2c6c9d8eb34083b34474cfc328e012
doc_id: 316740
cord_uid: pr6nlvo3

Objective: The etiology of persistent memory complaints after concussion is poorly understood. Memory perfectionism (highly valuing memory ability and intolerance of minor memory lapses) may help explain why some people report persistent subjective memory problems in the absence of corresponding objective memory impairment. The present study investigated the relationship between memory perfectionism and persistent memory complaints after concussion. Methods: Adults (N=77; 61% women) with persistent symptoms following concussion were recruited from outpatient specialty clinics. Participants completed the National Institutes of Health Toolbox Cognition Battery, Test of Memory Malingering-Trial 1, and questionnaires measuring memory perfectionism (Memory in Adulthood-Achievement subscale), forgetfulness and other post-concussion symptoms (Rivermead Postconcussion Symptoms Questionnaire; RPQ), and depression (Patient Health Questionnaire-2) at M=17.8 weeks post-injury. Patients with vs. without severe memory complaints (based on the RPQ) were compared. Results: Memory perfectionism was associated with severe memory complaint, after controlling for objective memory ability, overall cognitive ability, and depression (95% confidence interval for odds ratio = 1.11 to 1.40). Sensitivity analyses showed that this relationship did not depend on use of specific objective memory tests nor on inclusion of participants who failed performance validity testing. In a control comparison to test the specificity of identified relationships, memory perfectionism was not associated with severe fatigue (95% confidence interval for odds ratio = 0.91 to 1.07). Discussion: Memory perfectionism may predispose people to experience persistent memory symptoms and/or contribute to their perpetuation after concussion, with potential relevance to the spectrum of functional cognitive disorders more broadly.

Discussion: Memory perfectionism may predispose people to experience persistent memory symptoms and/or contribute to their perpetuation after concussion, with potential relevance to the spectrum of functional cognitive disorders more broadly.

. CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 16, 2021. ;  https://doi.org/10.1101/2021.11.15.21266362 doi: medRxiv preprint

Most people who sustain a concussion demonstrate normal cognitive function on neuropsychological testing by three months after injury 1 , however, almost half continue to subjectively experience cognitive problems for a year or longer, with memory complaints being one of the most common [2] [3] [4] . The etiology of these complaints is not clear. The relationship between cognitive complaints and objective cognitive performance on neuropsychological testing, cross-sectionally or longitudinally, is weak or not significant in most studies [5] [6] [7] [8] [9] . The minority of studies that reported an association between subjective and objective cognitive functioning on testing did not control for symptom or performance validity, which could have affected their results 10, 11 . Persistent cognitive complaints after concussion also correlate weakly with indicators of injury severity 8 , trauma-related macrostructural brain lesions 4, 12 and white matter integrity [13] [14] [15] . Stronger correlates of cognitive complaints after concussion include preinjury history of psychiatric conditions 10 , personality traits such as predisposition to interoceptive focus 12 , and current symptoms of depression, anxiety and post-traumatic stress 5, 7, 16 . In summary, underlying cognitive impairment is probably not the primary basis for persistent cognitive symptoms after concussion.

In many individuals with persistent cognitive symptoms after concussion, the clinical presentation is consistent with Functional Cognitive Disorder (FCD), a clinical entity characterized by an internal inconsistency between subjective cognitive symptoms and objective cognitive performance 17, 18 . The FCD literature may help generate hypotheses about why cognitive symptoms (most commonly relating to memory) often persist after concussion in the absence of underlying cognitive impairment. In a recently proposed theoretical model of FCD across various clinical settings 19 , memory perfectionism was positioned as a key predisposing . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 16, 2021. ; https://doi.org/10.1101/2021.11.15.21266362 doi: medRxiv preprint and perpetuating factor. Memory perfectionism refers to the combination of a strongly valued memory ability and an intolerance for minor memory lapses 19 . Memory perfectionism is thought to promote self-monitoring, increase noticing of memory lapses, and incite catastrophic interpretations of benign lapses (e.g., as evidence of permanent brain damage), all of which reinforces attention to and concern for memory problems 19, 20 .

Memory perfectionism correlates with the severity of memory complaints in people who have no objective impairment on memory testing, in both community and clinical samples 21, 22 .

To date, no studies have investigated memory perfectionism in the context of post-concussion symptoms. The objective of the present cohort study was to explore the association between memory perfectionism and persistent memory complaints following concussion. We hypothesized that higher memory perfectionism would be uniquely associated with memory complaint severity, after controlling for potential confounds, including objective episodic memory ability, global cognitive ability, and depression. Furthermore, through sensitivity analyses, we aimed to demonstrate that low effort in a subset of participants could not account for these relationships and that memory perfectionism is not similarly associated with severity of post-concussion symptoms other than memory (e.g., fatigue).

The present study is a secondary analysis of baseline data from a randomized control trial (Clinicaltrials.gov NCT03972579) as well as participants who were ineligible for this trial because they did not score highly on measures of maladaptive coping. Prior to randomization, participants completed an in-person assessment with a research assistant, under the supervision of a board-certified neuropsychologist (NDS). The assessment included self-report measures and neuropsychological testing. The University of British Columbia Behavioural Research Ethics . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint 

Informed consent was obtained from all participants before starting the baseline assessment. Participants recruited after COVID-19 restrictions came into effect (March 14, 2020) were excluded from the present study because they completed a modified online baseline assessment that did not include neuropsychological testing. Seventy-seven participants were Questionnaire (RPQ) 24 , a commonly used cut-off for "symptomatic" status 2 . 24 . The RPQ is a widely used self-report measure of symptom severity in concussion research and is recommended in the National Institute of Neurological Disorders and Stroke Common Data Elements for traumatic brain injury and sport-related concussion. Participants rate a list of 16 symptoms on scale ranging from 0 (not experienced at all) to 4 (severe problem), in comparison to before their . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. Metamemory in Adulthood Questionnaire (MIA) 25 . As in a prior FCD study 21 , we measured memory perfectionism with the Achievement subscale from the MIA 25 . The Achievement subscale consists of 16 items such as "It's important that I am very accurate when remembering names of people" and "It bothers me when others notice my memory failures,"

which are rated on a scale of 1 (agree strongly) to 5 (disagree strongly). After reverse scoring certain items, higher total MIA-Achievement scores reflect higher self-perceived memory perfectionism. In healthy people, intraindividual differences on the MIA-Achievement scale are stable through adulthood, supporting memory perfectionism as a personality trait 26, 27 .

Patient Health Questionnaire-2 (PHQ-2) 28 . We assessed depression with the Patient Health Questionnaire (PHQ-9), a reliable and valid self-report measure of depression symptom severity over the preceding two weeks 29 . The PHQ-9 includes items that overlap with the RPQ (e.g., difficulty concentrating and fatigue). The minimize this overlap, we analyzed the PHQ-2 in this study, which includes only the two cardinal depression symptoms (sadness and anhedonia) and has demonstrated accuracy for detecting depression that rivals the full PHQ-9 28 . 30 . The NIHTB-CB is administered by a trained examiner with the iPad and includes standardized measures of cognitive abilities. The Picture Sequence Memory Test, which requires participants to reproduce the sequence of pictures briefly presented is the core episodic memory test in the NIHTB-CB and for the present study. It has demonstrated good test-retest reliability and expected associations with "gold standard" memory tests and health-related variables (e.g., age) 31 . We used the NIHTB-CB Total Cognition Composite score as an index of global cognitive ability. It is . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 16, 2021. ; https://doi.org/10.1101/2021.11.15.21266362 doi: medRxiv preprint comprised of the Picture Sequence Memory Test and the six other core tests from the NIHTB-CB assessing crystallized intelligence, executive function, processing speed, and attention/working memory. Participants in this study were also administered the abbreviated Rey Auditory Verbal Learning Test (RAVLT), created as a supplementary measure for, and conormed with, the NIHTB-CB. In this task, participants hear a list of fifteen words and then must repeat as many of the words as they can. The NIHTB-CB RAVLT score is the sum of correctly recalled words over three consecutive learning trials. We considered the NIHTB-CB RAVLT as alternative measure of episodic memory in sensitivity analyses.

Test of Memory Malingering 32 . We measured performance validity using Trial 1 of the Test of Memory Malingering (TOMM-1). The TOMM-1 has the appearance of a challenging (visual recognition) memory test but was designed as a test of intention to perform well, i.e., effort or performance validity. In a recent meta-analysis, a cut-off score of below 42 on the TOMM-1 optimally identifies test-takers with known performance invalidity (sensitivity=0.6-0.7 and specificity>0.9) 33 .

Statistical analysis was performed using SPSS version 27 (SPSS, Chicago, IL, USA). Our primary outcome was subjective memory complaints as measured by the "forgetfulness" item on the RPQ. We dichotomized this ordinal scale into a binary variable reflecting the presence (item score=4) or absence (item score=0-3) of severe memory problems, because (1) a high proportion of participants (n=27 out of 77; 35%) endorsed severe memory problems, perhaps not surprising for patients seeking specialty treatment for persistent symptoms, (2) certain cell sizes were insufficient for analysis (only 3 of 77 participants endorsed an item score of 0), and (3) the mean . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this this version posted November 16, 2021. ; https://doi.org/10.1101/2021.11.15.21266362 doi: medRxiv preprint item score for all items on the RPQ was 2.8; in the context of a high overall symptom burden, we wished to identify participants for whom memory was an area of particular clinical concern.

In all logistic regression models, the binary RPQ forgetfulness item was the dependent variable and MIA-Achievement (memory perfectionism) was the main independent variable.

Additional covariates included episodic memory ability (NIHTB-CB Picture Sequence Memory Test), global cognitive ability (NIHTB-CB Total Cognition Composite) and depression (PHQ-2).

We conducted several sensitivity analyses to assess the robustness of our primary findings. First, we substituted the NIHTB-CB RAVLT for the NIHTB-CB Picture Sequence Memory Test in logistic regression modeling to see if a different (auditory-verbal vs. visual) objective measure of episodic memory would alter our findings. Second, to determine if the relationship between memory perfectionism and symptom reporting was specific to memory complaints, we substituted the RPQ fatigue item (a non-memory symptom with a similar frequency distribution) for the forgetfulness item, converting it to binary in the same manner as was done for the forgetfulness item (4=presence of severe complaint, 0-3=absent). Finally, we ran a model excluding the 13 participants who scored below 42 on the TOMM-1 to determine if cases of performance invalidity accounted for the associations between memory perfectionism and memory complaints in the primary analysis. Table 1 .

The primary logistic regression model is presented in Table 2 . Higher memory perfectionism (MIA-Achievement) was associated with severe memory complaint (odds ratio = 1.25, 95% confidence interval = 1.11 to 1.40, p < 0.001), when controlling for depression (PHQ-2), . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. 

It is unclear why subjective memory concerns often persist long after concussion. The present study examined whether memory perfectionism, a core predisposing and/or perpetuating factor in FCD 19, 20 , was associated with persistent memory complaints in a sample of adults . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 16, 2021. ; https://doi.org/10.1101/2021.11.15.21266362 doi: medRxiv preprint seeking treatment post-concussion. Consistent with this hypothesis, we found that higher memory perfectionism was associated with severe memory complaints, after adjusting for objective memory, overall cognitive ability and depression. Sensitivity analyses suggest that this relationship is robust to the modality of objective memory measurement as well as to performance validity concerns. It does not appear that memory perfectionism is a function of higher post-concussion symptom reporting in general, as it did not predict severe fatigue complaint. In other words, memory perfectionism was specific in its relationship to elevated subjective memory concerns. This is the first study to explore memory perfectionism in the context of postconcussion symptoms. Our findings are consistent with studies assessing people with FCD 21, 22 .

As in FCD, perceptions of poor memory following concussion may be fueled by excessive value and standards for one's own memory abilities. Mechanistically, people with high memory perfectionism may have increased vigilance towards cognitive errors and anxiety about the permanence and consequences of brain injury. Heightened attention to minor memory lapses and distress-provoking interpretations of their meaning may further perpetuate memory complaints, and may represent a cognitive parallel of somatic hypervigilance 19, 20 . People may also misremember having fewer memory lapses before their concussion than they actually did, an example of the "good-old-days" bias 34 . Additionally, post-injury stress, sleep problems, psychiatric disorders, and chronic pain may all contribute to both subjective and objective cognitive difficulties misattributed to brain injuy 8,9,12,35-38 . There are several limitations to the current study. Memory perfectionism and memory complaints were assessed concurrently, at an average of four months post-injury. We therefore cannot be sure to what extent memory perfectionism is a premorbid personality trait and . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 16, 2021. ; https://doi.org/10.1101/2021.11.15.21266362 doi: medRxiv preprint predisposing (i.e., vulnerability) factor or becomes (further) elevated after concussion. Relatedly, we cannot rule out reverse causality, that is, the possibility that people place importance on their memory ability and become intolerant of memory lapses because they experience memory problems. Our primary outcome was a single ordinal rating of how much participants' experienced problems with forgetfulness now compared to before their injury. This item has demonstrated test-retest stability 39 and strong discrimination between concussion and orthopedic injury control groups 40 , however, it may not have comparable reliability and validity to longer patient-reported outcomes assessing subjective memory functioning. Still, we believe that the presence vs. absence of severe memory complaints is a clinically relevant outcome. Participant characteristics that limit the generalizability of our findings include the high overall symptom burden (mean RPQ total score = 35.7) and advanced level of education (half had a postsecondary degree), which are not surprising for participants who are seeking treatment and willing to volunteer in research, but may not be representative of the broader concussion population. Our sample size limited us from considering additional covariates that may be important, such as anxiety and medications. Finally, it may be that performance on neuropsychological tests of memory are not sensitive enough to detect subtle real-world deficits that are reflected in people's subjective experiences. Following this logic, relatively severe memory performance decrements (i.e., those detectable on neuropsychological testing) should be associated with more severe subjective memory problems. We and others [5] [6] [7] [8] [9] have not observed this association.

In summary, the present study supports a role for memory perfectionism in persistent memory complaints after concussion. A full mechanistic model for persistent memory complaints awaits further validation and will likely include several other biopsychosocial pre-. CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 16, 2021. ; https://doi.org/10.1101/2021.11.15.21266362 doi: medRxiv preprint and post-injury factors. Subjective concern about memory decline, even in the absence of objective memory impairment, can result in functional impairment. For example, people may self-limit their participation in work or school after concussion due to low self-efficacy and anticipated negative consequences. Assessment of a patient with persistent memory complaints after concussion, especially when their symptoms are incompatible with their demonstrated memory ability on neuropsychological testing, should include exploration of their perceptions of their pre-injury memory ability, fears related to memory loss, reactions to memory lapses, and compensatory behaviors (e.g., reliance on others for help remembering things). Psychological interventions targeted at maladaptive beliefs about memory and counterproductive coping with perceived memory difficulties should be considered.

. CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 16, 2021. ; https://doi.org/10.1101/2021.11.15.21266362 doi: medRxiv preprint

The neuropsychological outcomes of concussion: A systematic review of meta-analyses on the cognitive sequelae of mild traumatic brain injury

Rates of symptom reporting following traumatic brain injury

Persistent problems 1 year after mild traumatic brain injury: A longitudinal population study in New Zealand

Recovery after mild traumatic brain injury in patients presenting to US Level I Trauma Centers: A transforming research and clinical knowledge in traumatic brain injury (TRACK-TBI) Study

The contributions of self-reported injury characteristics and psychiatric symptoms to cognitive functioning in OEF/OIF veterans with mild traumatic brain injury

Cognitive complaint and objective cognition during the post-acute period after mild traumatic brain injury in pre-morbidly healthy adults

Change in self-reported cognitive symptoms after mild traumatic brain injury is associated with changes in emotional and somatic symptoms and not changes in cognitive performance

Subjective cognitive complaints in concussion

Making a difference: Affective distress explains discrepancy between objective and subjective cognitive functioning after mild traumatic brain injury

Concordance of common data elements for assessment of subjective cognitive complaints after mild-traumatic brain injury: a TRACK-TBI Pilot Study

Neuropsychological outcome and its correlates in the first year after adult mild traumatic brain injury: A population-based New Zealand study

Cognitive complaints after mild traumatic brain injury: Things are not always what they seem

Diffusion tensor imaging findings are not strongly associated with postconcussional disorder 2 months following mild traumatic brain injury

A prospective biopsychosocial study of the persistent post-concussion symptoms following mild traumatic brain injury

The evolution of white matter microstructural changes after mild traumatic brain injury: A longitudinal DTI and NODDI study

Cognitive functioning and postconcussive symptoms in trauma patients with and without mild TBI

Functional cognitive disorders: a systematic review

Functional cognitive disorder: Dementia's blind spot

A unifying theory for cognitive abnormalities in functional neurological disorders, fibromyalgia and chronic fatigue syndrome: Systematic review

Functional cognitive disorders (FCD): How is metacognition involved?

How are memory complaints in functional memory disorder related to measures of affect, metamemory and cognition?

Memory complaints in elderly people: The role of memory abilities, metamemory, depression, and personality

Summary of the WHO Collaborating Centre for Neurotrauma Task Force on mild traumatic brain injury

The Rivermead Post Concussion Symptoms Questionnaire: a measure of symptoms commonly experienced after head injury and its reliability

The Metamemory in Adulthood (MIA) questionnaire

Structure and development of Metamemory in Adulthood

Stability and accuracy of metamemory in adulthood and aging: A longitudinal analysis

Accuracy of the PHQ-2 alone and in combination with the PHQ-9 for screening to detect Major Depression: Systematic review and meta-analysis

The PHQ-9: Validity of a brief depression severity measure

Cognition assessment using the NIH Toolbox

Measuring episodic memory across the lifespan: NIH toolbox picture sequence memory test

The Test of Memory Malingering (TOMM): Normative data from cognitively intact and cognitively impaired individuals

A systematic review and meta-analysis of the Test of Memory Malingering in adults: Two decades of deception detection

The nature and clinical significance of preinjury recall bias following mild traumatic brain injury

Psychological factors and subjective cognitive complaints after stroke: Beyond depression and anxiety

Cognitive complaints are associated with depression, fatigue, female sex, and pain catastrophizing in patients with chronic pain

Lifestyle factors are important contributors to subjective memory complaints among patients without objective memory impairment or positive neurochemical biomarkers for alzheimer's disease. Dement Geriatr Cogn Dis Extra2018

Identifying functional cognitive disorder: a proposed diagnostic risk model

Distinguishing between enduring and dynamic concussion symptoms: Applying Generalisability theory to the Rivermead Post Concussion Symptoms Questionnaire (RPQ)

Is the Rivermead Post-Concussion Symptoms Questionnaire a reliable and valid measure to assess long-term symptoms in traumatic brain injury and orthopedic injury patients? A novel investigation using Rasch Analysis

RPQ total score, M (SD) 77 35.74 (13.72) NIHTB-CB Picture Sequence Memory