ORIGINAL CONTRIBUTION. Continuum of Frontal Lobe Impairment in Amyotrophic Lateral Sclerosis
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1 OIGINA CONTIBUTION Continuum of Frontal obe Impairment in Amyotrophic ateral Sclerosis Jennifer M. Murphy, PhD; oland G. Henry, PhD; Susan angmore, PhD; Joel H. Kramer, PsyD; Bruce. Miller, MD; Catherine omen-hoerth, MD, PhD Objective: To identify the nature and prevalence of cognitive and behavioral abnormalities in patients with amyotrophic lateral sclerosis (AS). Design: Survey of clinical characteristics. Setting: Multidisciplinary clinic within a university medical center. Patients: A volunteer sample of 30 new patients with AS were recruited consecutively. Of those invited, 23 participants (20 with sporadic AS and 3 with familial AS) enrolled. Participants ranged in age from 27 to 80 years (mean age, 56.5 years); the education level ranged from 12 to 21 years (mean education level, 3.5 years of college); and 17 participants (74%) were male. Main Outcome Measures: Neuropsychological tests, neurobehavioral interviews, and structured magnetic resonance imaging. esults: Patients were classified into subtypes of frontotemporal lobar degeneration (n=5), suspected Alzheimer disease (n=1), and subthreshold variants of cognitive impairment (n=2), behavioral impairment (n=4), and cognitively and behaviorally normal (n=11). Five neuropsychological tests, 2 behavioral abnormalities, and right hemisphere gray matter reductions differentiated patients into normal and abnormal groups. Conclusions: In this sample, a sizable proportion of patients with AS possess a range of behavioral and cognitive changes that lie on a spectrum of frontotemporal impairment. ight hemisphere atrophy may be a biomarker for cognitive impairment in patients with AS. Arch Neurol. 2007;64: Author Affiliations: Department of Neurology, AS Center (Drs Murphy, angmore, and omen-hoerth), Department of adiology, Center for Molecular and Functional Imaging (Dr Henry), and Department of Neurology, Memory and Aging Center (Drs Kramer and Miller), University of California, San Francisco. AN ASSOCIATION BETWEEN dementia and amyotrophic lateral sclerosis (AS) was first noted in the late 1800s, and studies dating back to the 1930s document dementia syndromes in AS. 1 In 1994, the und and Manchester groups 2 first used the term frontotemporal dementia (FTD) with motor neuron disease, and a variety of reviews 3-6 document the growing evidence of the link between FTD and motor neuron disease. Incidence rates of AS dementia vary owing to referral bias and differing diagnostic criteria. Historically, rates were documented as 3% in sporadic AS and 15% in familial AS, 7 but recent studies 8-11 using frontal lobe based neuropsychological measures report rates as high as 28% to 48%. ates of AS dementia increase 8,12,13 with the use of frontotemporal lobar degeneration (FTD) based dementia criteria 13,14 and tools measuring behavioral, executive, and language change. Studies that define abnormality as the presence of frontal lobe dysfunction document dementia symptoms in 50% of all cases. 11,15,16 The cerebral, neuropsychological, and pathological deficits associated with AS are increasingly recognized as existing on a spectrum. Many nondemented patients with AS exhibit cognitive deficits Behaviorally, some patients with AS meet full Neary criteria for FTD, 14,23,24 others have milder levels of behavioral changes, and still others appear normal. 25 In this article, we address the following questions: (1) What percentage of patients with AS meets Neary criteria for the 3 subtypes of FTD? (2) How many patients possess cognitive or behavioral deficits that do not meet full criteria for FTD? and (3) Are there neuroimaging differences between these groups? METHODS SUBJECTS New patients were recruited consecutively from the AS Center, University of California, San Francisco. Of approximately
2 patients with AS invited into the study, 23 participants (20 with sporadic AS and 3 with familial AS) gave informed consent and enrolled. easons given for refusal to participate included inability to lie down in the magnetic resonance imaging scanner and lengthy travel distance. No participant had a history of other neurological or psychiatric disease, previous dementia diagnosis, head injury, or central nervous system related medical illness. All of the participants met criteria for probable or definite AS based on World Federation of Neurology criteria. 26 Participants ranged in age from 27 to 80 years (mean age, 56.5 years), the education level ranged from 12 to 21 years (mean education level, 3.5 years of college), and 17 participants (74%) were male. Twenty participants were right-handed, 2 were left-handed, and 1 was ambidextrous. The mean (range) duration of AS symptom onset was 23 (1-36) months. This study was approved by the institutional review board at the University of California, San Francisco. Measured clinical characteristics included age, sex, educational level, disease progression, bulbar vs limb onset, presence of pseudobulbar affect, and secondary effects of depression. A speech pathologist (S..) rated dysarthria levels as absent, mild, moderate, or severe using operational definitions of each level of severity. Pseudobulbar affect was defined by a score higher than 13 on the Center for Neurologic Study ability Scale. 27 Forced vital capacity, a measure of breathing function, was measured by a certified respiratory therapist (Colleen Meier, BS) using standard techniques. DEFINING COGNITIVE ABNOMAITIES IN AS Diagnoses of FTD were based on the Neary criteria. 23 Frontotemporal lobar degeneration includes 3 subtypes of frontotemporal abnormality: the frontal variant (FTD), progressive nonfluent aphasia, and semantic dementia. Core Neary criteria for FTD include early decline in social and personal conduct, emotional blunting, and loss of insight. Core Neary criteria for semantic dementia include fluent speech with loss of word meaning, and Neary criteria for progressive nonfluent aphasia include nonfluent speech with agrammatism, paraphasias, or anomia. We used the NINCDS-ADA (National Institute of Neurological and Communicative Diseases and Stroke/Alzheimer s Disease and elated Disorders Association) criteria for Alzheimer disease (AD) as defined by McKhann et al. 28 Dementia diagnoses were made at a case conference attended by a team including a neurologist specializing in dementia (B..M.), a neurologist specializing in AS (C..-H.), a neuropsychologist (J.M.M. or J.H.K.), and a nurse (Dallas Forshew, BS) known to the patient. The Neary criteria for FTD were reviewed for each patient and diagnoses of the frontal variant of the disease were made when all 5 core criteria were met by identifying clear examples of behavioral abnormalities (eg, decline in social conduct, emotional blunting, or loss of insight). The team gave deliberate consideration to avoid inclusion of social and emotional behaviors resulting from the AS process itself to guard against bias toward overdiagnosing FTD (eg, social isolation due to embarrassment or emotional changes due to pseudobulbar affect). NEUOPSYCHOOGICA MEASUES The neuropsychological battery was weighted toward executive functioning tests and has been detailed elsewhere. 29 Each neuropsychological measure has been shown to be effective in identifying FTD deficits. Neuropsychological evaluations were completed in approximately 2 hours by an experienced neuropsychologist ( J.M.M.). Verbal fluency and motor test scores were not analyzed for participants with moderate to severe dysarthria and upper limb motor impairment. Age- and sexcorrected norms were used to generate standardized scores. NEUOBEHAVIOA MEASUES The Neuropsychiatric Inventory 30 was conducted with a caregiver without the patient present. This scale measures 12 neuropsychiatric behaviors common in dementia: delusions, hallucinations, agitation, dysphoria, anxiety, apathy, irritability, euphoria, disinhibition, aberrant motor behavior, nighttime behavioral disturbances, and appetite and eating abnormalities. NEUOIMAGING Magnetic resonance imaging scans were obtained with wholebrain coverage. The scans included 3-dimensional T1- weighted volumes. We used SIENAX software (Oxford Centre for Functional Magnetic esonance Imaging of the Brain, Oxford, England) to estimate segmented gray and white matter volumes. obar regions were defined from the parcellated Brodmann regions. Magnetic resonance imaging analyses were performed for 20 normal controls and 22 patients with AS. STATISTICS The single AD case was excluded from each analysis. Familial and sporadic cases were not statistically separated owing to small sample size. ESUTS SUBJECT COGNITIVE STATUS Of the 23 patients with AS who consented for the study, 6 met criteria for a dementia syndrome. One patient met criteria for suspected AD and 5 met Neary research criteria for the diagnosis of FTD (2 with FTD, 2 with semantic dementia, and 1 with progressive nonfluent aphasia). IDENTIFYING A CONTINUUM OF FONTA OBE IMPAIMENT The incidence of neurobehavioral or cognitive disorder not meeting criteria for dementia was thus determined for the 17 remaining patients. Of these 17 patients, 11 were cognitively and behaviorally normal and 6 had a spectrum of cognitive or behavioral impairment (Figure 1). The team identified 4 patients who met only partial Neary criteria for FTD or had conflicting informant reports of the severity of the behavioral changes. Our group offers the term AS with behavioral impairment (ASbi) 31 to describe such patients with AS who display frontal lobe based behavioral signs who do not meet full criteria for FTD as defined by a Neuropsychiatric Inventory total domain score (severity frequency) of 3 or more on at least 2 behavioral domains (Table 1). Two patients displayed executive dysfunction deficits on neuropsychological testing but had no behavioral deficits. We suggest the term AS with cognitive impairment 531
3 Cognitively Abnormal (n = 2) Behaviorally Abnormal (n = 4) Alzheimer Disease (n = 1) for those patients with AS who score 1.5 SDs below the mean on at least 2 measures of executive function, semantic dementia, or primary progressive aphasia. Although the subtypes identified here are not completely dissociable and the sample is small, the groups are distinct in interesting ways. The patients with AS with comorbid FTD exhibited their first symptom of cognitive or behavioral decline, on average, 7 years and 7 months prior to their AS diagnosis (range, 2-12 years), and the ASbi group developed cognitive or behavioral symptoms concurrent with or after their AS diagnosis. CINICA COMPAISONS FTD (n = 5) Cognitively and Behaviorally Normal (n = 11) Figure 1. The distribution of dementia status and subthreshold abnormalities in 23 patients with amyotrophic lateral sclerosis in an unselected amyotrophic lateral sclerosis sample. FTD indicates frontotemporal lobar degeneration. The clinical characteristics of the cohort are shown in Table 2. The cognitively or behaviorally impaired AS group includes patients with FTD (n=5), ASbi (n=4), and AS with cognitive impairment (n=2). A 1-way analysis of covariance revealed that the impaired AS group did not differ from the cognitively intact AS group in rates of pseudobulbar affect, level of depression, sex, education level, AS disease state, or handedness. Significant group differences did occur for age. The AS group with cognitive abnormalities was, on average, 16 years older (mean age, 64 years) than the cognitively intact patients with AS (mean age, 48 years). SPECTUM OF NEUOPSYCHOOGICA ABNOMAITIES IN PATIENTS WITH AS WITH BEHAVIOA ABNOMAITIES When the patients with AS without behavioral deficits (n=11) were compared with patients with AS diagnosed with behavioral abnormalities (n=9; 5 patients with FTD and 4 with ASbi), the patients with behavioral abnormalities demonstrated comorbid executive function abnormalities. The 2 patients with cognitive abnormalities were excluded from this analysis to avoid circularity, as the neuropsychological tests are used as a dependent variable. The behaviorally abnormal AS group Table 1. Summary of Cognitive Subtypes Terminology AS AS with cognitive impairment AS with behavioral impairment AS with comorbid FTD Clinical Characteristics Pure motor system disorder as defined by the El Escorial criteria; no clinical evidence of frontotemporal dysfunction Deficits (1.5 SDs below the age-matched mean) on 2 neuropsychological tests of executive functioning or tests measuring semantic or primary progressive aphasia, but insufficient to meet the Neary criteria for FTD NPI total domain score (severity frequency) 3on 2 domains Patient with AS meeting Neary criteria for FTD Abbreviations: AS, amyotrophic lateral sclerosis; FTD, frontotemporal dementia; FTD, frontotemporal lobar degeneration; NPI, Neuropsychiatric Inventory. had significantly more impairment on 5 neuropsychological measures that tap into executive functioning: the Wisconsin Card Sort, the Boston Naming Test, California Designs, the Controlled Oral Word Association Test, and category fluency. On the Controlled Oral Word Association Test fluency test, the group with behavioral abnormalities scored only half the points (mean, 27.8 words) as those who were behaviorally intact (mean, 47.4 words). No group differences emerged for memory or spatial skills. SOCIA DISINHIBITION AND IITABIITY DIFFEENTIATE BETWEEN GOUPS Both the behaviorally and cognitively abnormal patients with AS were grouped into an abnormal group (n=11) and compared with the patients with AS without cognitive and behavioral impairment (n=11) to identify which neurobehavioral traits differentiate between them. The patients with AS with cognitive and behavioral impairment showed more disinhibition (P=.005) and irritability (P=.04) than the cognitively and behaviorally intact AS group. This difference is unlikely owing to depression because group differences in depression did not exist when compared using the Geriatric Depression Scale. STUCTUA MAGNETIC ESONANCE IMAGING esults from the nonparametric Kruskal-Wallis test with Bonferroni adjustment indicate that the AS group with cognitive and behavioral deficits have reduced volumes as compared with the normal controls in all regions of interest (P=.004). The cognitively and behaviorally intact patients with AS have larger right frontal, right parietal, and right limbic volumes as compared with the patients with AS with cognitive and behavioral abnormalities. Cognitively and behaviorally intact patients with AS have decreased right temporal volumes as compared with normal controls (Figure 2). When taking every variable into account and controlling for the statistical effects of age, only right temporal 532
4 Table 2. Participant Clinical Characteristics Clinical Characteristics Patients With Cognitive or Behavioral Dysfunction (n = 11) Cognitively and Behaviorally Normal Patients (n = 11) F Score P Value Pseudobulbar affect, No. (%) affected 7 (64) 7 (64) Bulbar onset, No. 4 2 NA NA Dysarthria scale score, mean* 1.1 (Mild) 0.27 (Absence) GDS score, mean 10 (Mild) 10 (Mild) Age, mean, y Familial cases, No ASFS- score, mean FVC score, mean Female, No. (%) 3 (27) 3 (27) NA NA Education, mean, y MMSE score, mean Abbreviations: ASFS-, Amyotrophic ateral Sclerosis Functional ating Scale; FVC, forced vital capacity; GDS, Geriatric Depression Scale; MMSE, Mini-Mental State examination; NA, not applicable. *The scores were rated as follows: 0 = absent; 1 = mild; 2 = moderate; and 3 = severe. A B C Figure 2. Structural magnetic resonance image comparisons across 3 groups. Coronal, axial, and sagittal views of a 61-year-old neurologically normal control subject (A), a 57-year-old cognitively normal patient with amyotrophic lateral sclerosis (B), and a 54-year-old patient with amyotrophic lateral sclerosis with cognitive abnormalities (C). indicates right;, left. volume is most predictive of group membership. The 2 patients with semantic dementia had right temporal volumes within 1 SD of the mean. One of the 2 patients with semantic dementia was an outlier for left frontal atrophy, and this patient was ambidextrous. COMMENT In an unselected AS cohort, we found a spectrum of frontal lobe dysfunction in half of our patients. The cognitive and behavioral abnormalities varied in severity, with 5 patients(22%) meeting Neary criteria for FTD, 4(17%) demonstrating more subtle behavioral disturbances, and 2 (9%) exhibitingsubtlecognitivedysfunction. Whenthesepatients with AS with abnormalities were grouped together into a broad category, they were found to have reduced volumes in right frontal, right parietal, and right limbic lobes as compared with patients with AS without cognitive or behavioral disturbance. The AS group with moderate or severe behavioral disturbance had comorbid executive dysfunction as compared with the AS group without behavioral impairment, despite the groups similarity in memory, spatial skills, level of depression, and disease progression. The continuumhypothesisissupportedbytheevidencethatboth the ASbi group and the AS-FTD group show the same abnormalities on executive function tests. Although a cutoff of 2 SDs would provide a more conservative criterion when classifying patients with cognitive abnormalities, the 1.5-SD cutoff allows for a more sensitive indicator of the moderate executive function changes typically seen in the AS population. Although our Neuropsychiatric Inventory cutoff for ASbi (domain score 3 on 2 domains) requires validation, to our knowledge, there is no evidence to date that patients with terminal illness possess elevated Neuropsychiatric Inventory scores and it is known that nondemented elderly patients earn scores well below 0.5 on each domain. 30 Advanced age did not account for group differences in cognitive deficits, but it appears to be an indicator of heightened risk for cognitive and behavioral deficits, par- 533
5 ticularly when combined with bulbar-onset AS. 29 Disinhibition and irritability stood out as 2 traits that most distinguished between those patients who met criteria for behavioral disturbance and those who did not, independent of depression rates. The single AD diagnosis may be explained as having a separate cause that is consistent with customary AD, as has been described in other AS samples. 32,33 Among the patients with AS, those with full-blown dementia or subthreshold abnormalities in cognition or behavior had gray matter reductions in right frontal, right parietal, and right limbic lobes as compared with the patients with AS without abnormalities. This anatomical distinction between the 2 AS groups suggests that right hemisphere atrophy among patients with AS may be a type of biomarker linked to behavioral and cognitive abnormalities. Such right hemisphere deficits have been linked to inappropriate range and intensity of affect 34 as well as impaired ability to perceive facial expression. 35 Patients with right-hemisphere deficits exhibit an indifference reaction, tending to deny the extent of their disabilities 36 ; this is a common trait observed in patients with AS with behavioral disturbance. Patients with AS with cognitive abnormalities have poorer compliance and reduced survival rates, suggesting that identification of these traits is clinically important, 29 and the AS field of research may be advanced with a more detailed categorization of AS phenotypes. Accepted for Publication: November 20, Correspondence: Jennifer M. Murphy, PhD, Department of Neurology, AS Center, University of California, San Francisco, 350 Parnassus Ave, Suite 500, San Francisco, CA (jennifer.murphy@ucsf.edu). Author Contributions: Dr Murphy had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Murphy, Henry, Kramer, Miller, and omen-hoerth. Acquisition of data: Murphy, Henry, and angmore. Analysis and interpretation of data: Murphy, Henry, and omen-hoerth. Drafting of the manuscript: Murphy and Henry. Critical revision of the manuscript for important intellectual content: Murphy, Henry, angmore, Kramer, Miller, and omen-hoerth. Statistical analysis: Murphy, Henry, and Kramer. Obtained funding: Kramer, Miller, and omen-hoerth. Administrative, technical, and material support: Murphy, angmore, and Kramer. Study supervision: omen-hoerth. Financial Disclosure: None reported. Funding/Support: This work was supported by the AS Association. EFEENCES 1. Neary D, Snowden JS, Mann DM. Cognitive change in motor neurone disease/ amyotrophic lateral sclerosis (MND/AS). 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