Chiadi U. Onyike Johns Hopkins University Division of Geriatric Psychiatry and Neuropsychiatry
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1 Chiadi U. Onyike Johns Hopkins University Division of Geriatric Psychiatry and Neuropsychiatry
2 Disclosure: PI of the Baltimore site of the NAM-53 Multicenter trial of memantine for frontotemporal dementia Discussion of medicines pertains to off-label use Objectives: Examine phenotype(s), epidemiology and pathobiology Review evaluation and diagnosis Discuss treatments and rehabilitative interventions
3 Is it memory loss? Is it old age? How is it different from Alzheimer disease?
4 Alzheimer disease, AD Types of dementia Most common cause between ages 50-65; 33% of dementia below age 65 Cerebrovascular disease, CVD Genetic varieties particularly Frontotemporal dementias, FTD 1:1 or greater ratio FTD:AD below age 50 Dementia with Lewy bodies Uncommon before age 65 Traumatic brain injury, TBI HIV/AIDS dementia Alcohol-related dementia Follows head trauma Prevalence has decreased since HAART Mostly associated with nutritional deficienceis Huntington disease, HD Among the commonest below age 35 Prion dementias Generally rare beyond age 65 Multiple sclerosis, MS Normal Pressure Hydrocephalus McMurtay et al, 2006
5 Generally non-amnestic Disorders of temperament and conduct Motor features: parkinsonism, apraxia, ataxia, tremor, gait disorder Mid-life onset common
6 Insidious deterioration Behavioral disinhibition and asocial behavior Inertia and apathy Loss of empathy/sympathy Perseveration, stereotypies and compulsions Hyperorality and altered eating habits Executive dysfunction Focal abnormalities on brain imaging Tau, progranulin or FUS mutations Sources: Rascovsky et al., 2011
7 A technician of 55 had difficulty findings words, which in a few years evolved to dysfluency, repetitiousness, stereotypies and echolalia. In the 2 nd year, his work efficiency deteriorated due to his poor comprehension and reasoning, so he was placed on disability leave. He was childlike, impulsive and unfeeling. He insisted on the same TV shows. His manners coarsened examples include indiscrimmately approaching strangers, eating out of a serving bowl, jumping queues, abruptness in conversations. He was restless - biking, swimming laps and running 6.5 miles each day. His wife arranged his volunteering at a local nursing home, where he made rounds with maintenance crews all day long. She noted that his awareness of tiredness seemed impaired. On examination 30 months ago, he was pleasant and proper. Depression was not evident, and he did not have euphoria, psychosis or paranoia. Speech was mildly nonfluent. Verbal fluency was impaired. MMSE 29 (3MS 96). Brain MRI showed right temporal atrophy. A year later he developed marked preference for sweets, along with foraging and overeating. Two years later he was admitted to residential care. At the last visit 6 months ago, MMSE score was 27.
8 Progressive coarsening of conduct Literalness and rigidity Indifference Impulsions and compulsions Sweet tooth and hyperphagia Impaired perception of body states/functions Verbal and motor stereotypies Hyperkinesis Motor phenomena Focal atrophy on MRI MMSE 29!
9 Agrammatism Effortful, halting speech with sound errors and distortions Impaired comprehension of syntactically complex sentences Impaired confrontation naming Impaired word comprehension Impaired object knowledge Surface dyslexia and/or dysgraphia Impaired word retrieval Impaired repetition of sentences and phrases Phonological errors in spontaneous speech Sources: Gorno-Tempini et al., 2011
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11 Localization to Broca s area Compilation of words into statements with appropriate syntax L R L Sources: Gorno-Tempini et al., 1998
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13 L Localization to the left anterior pole Transformation of words from generic to specific meanings Typically bilateral, left preponderant, anterior temporal atrophy R L Sources: Gorno-Tempini et al., 1998
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15 Localization to Wernicke s area Linkage of word forms to their distributed associations L R L Sources: Gorno-Tempini et al., 1998
16 Frontotemporal dementia with amyotrophic lateral sclerosis, FTD-ALS: muscle atrophy, weakness, spasticity Corticobasal degeneration, CBD: asymmetric rigidity and apraxia with alien limb phenomenon, cortical sensory loss, dystonia, and myoclonus Progressive supranuclear palsy, PSP: apathy, dyexecutive state, vertical gaze palsy, parkinsonism, pseudobulbar palsy, retropulsion and falls, dementia Primary prosopagnosia with visual agnosia: loss of face and object knowledge
17 Progressive loss of mental faculties Irreversible decline in 2 domains Orientation Memory Language Object recognition Executive functions Praxis
18 Left: The Prague Asylum, with a view of the tower of St. Catharine Monastery. Right: Arnold Pick ( ); Professor of Psychiatry and Neuropathology and Chair of Neuropsychiatry in Prague ( ). His work includes ~280 papers devoted to topics in neuropsychiatric states. He described the presenile focal dementias and the progressive aphasias that would became known as Pick s disease. Sources: Kertesz and Kavlach, 1996
19 First known case of primary aphasia Paul Serieux, Clinical features and lobar atrophy Arnold Pick, Cortical gliosis with rounded eosinophilic, argyrophilic cytoplasmic Pick bodies Alois Alzheimer, Pick s disease Gans, 1923; Onari and Spatz, Frontal lobe dementia, Types A, B and C Tissot, Constantinidis and Richards, 1974 and Semantic aphasia Elizabeth Warrington, Primary progressive aphasia M.-Marcel Mesulam, First international conference Lund, Sweden, Lund-Manchester consensus 1994; Manchester consensus First genetic mutations (MAPT) Michael Hutton and colleagues, Sources: ; Hutton et al., 1998; Bergeron, Morris and Rossor, 2003; Brun, 2007; Mesulam; 2007
20 Pathological appearance of the brain in a case of Pick s Disease: knife s edge atrophy of the frontal lobe; thinning of the cortical ribbon, white matter pallor and atrophy of the caudate head Sources: Graff-Radford and Woodruff, 2007
21 Pick disease is characterized by argyrophilic (silver staining) spherical inclusions called Pick bodies and globose neurons. The Pick body is composed of numerous tau fibrils arranged in a disorderly array. Tau protein is a major component of the Pick body, but other antibodies also stain Pick bodies, including those to ubiquitin, alpha-synuclein, and apolipoprotein E. Sources:
22 Sources: Cairns et al., 2007 Frontotemporal dementia with MAPT G389R mutation. A) Numerous tau-immunoreactive Pick body-like inclusions in the granule neurons of the dentate fascia. B) Swollen achromatic neuron in the superior temporal gyrus. C) Swollen neuron showing anti-tau immunoreactivity. D) intraneuronal inclusion resembling a Pick body in the superior frontal gyrus. E) Neurofibrillary tangle-like inclusion in layer V of the superior frontal gyrus. F) Globose neurofibrillary tangle-like inclusion in the dorsal raphe. G) Astrocytic fibrillary inclusion and oligodendrocytic coiled body in the frontal white matter.
23 Sources: Cairns et al., 2007 Frontotemporal dementia showing spectrum of TDP-43 pathology. Adjacent sections of superficial frontal cortex showing neuronal cytoplasmic inclusions (NCI), dystrophic neurites (DN), and isolated intranuclear inclusions (NII) stain for ubiquitin [A] and TDP-43 [B]. NCI in the dentate granule cells stain for ubiquitin [C] and TDP-43 [D]. Neuronal and glial inclusions include NCI [E], round and lentiform NIIs [F, G]. Skein-like [H], and compact round [I] NCI in the lower motor neurons. Glial cytoplasmic inclusions (GCI) [J]. TDP-43 immunohistochemistryin E-J.
24 Sources: Neumann et al., 2009 FUS immunohistochemistry on sections of post-mortem brain from normal control (A) and FTD subjects (B-I). Normal staining pattern, consisting of strong staining neuronal nuclei and weaker staining of neuronal cytoplasm and glial nuclei is evident in normal controls (A). In FTD subjects neurons with inclusions retain some of the normal staining (B). NCI are most numerous in the middle and deeper layers of the neocortex (C-E) and the dentate granule cells of the hippocampus (F), and range in morphology from round or oval (D and F) to crescentic (E). Dentate granule cells with vermiform NII also frequently show NCI (G). Globular NCI are present in lower motor neurons (H). Flame-shaped cytoplasmic inclusions are seen in white matter (I).
25 FTD-tau FTD- TDP43 FTD-FUS FTD-UPS FTD-tau FTD Atypical FTD-u FTD3 Pick disease FTD-ALS BIBD CBD/PSP ALS? NIFID MST-D IBMPFD AGD NFT WMT- GGI Sources: Cairns et al., 2007; MacKenzie et al., 2009
26 MAPT PGRN TARDP (TDP) CHMP2B VCP FUS C9orf72 FTD-tau FTD ALS FTD3 IBMPFD ALS ALS Pick disease FTD-ALS FTD- ALS* FTD-ALS CBD/PSP MST-D Sources: Hutton et al., 1998; Watts et al., 2004; Skibinski et al., 2005; Baker et al., 2006; Cruts et al., 2006; Vance et al., 2009; DeJesus-Hernandez et al., 2011; Renton et al., 2011
27 Peak age of onset 53 58, range for behavioral FTD and semantic PPA; peaks onset a decade later (mid late 60s) for agrammatic and logopenic PPA Prevalence: 9 17% in autopsy series ~5 10% of all dementias M>>F in most reports AD:FTD ratio <2 below age 65 Familial in >40% of cases of FTD and semantic PPA, much lower for agrammatic PPA, rare for logopenic PPA; other risk factors unknown Higher prevalence of learning disability (personal 7 15%, familial 14 30%) Life expectancy: 7 13 years (mirrors AD); shorter (3-5 years) for FTD-ALS Sources: Bird et. Al, 2003; Ratnavalli et al., 2002; Rosso et al., 2003; Pasquier et al., 1999; Hodges et al., 2002; Pasquier et al., 2004; Le Rhun et al., 2005; Rogalski et al., 2008; Xie et al., 2008; Borroni et al., 2009; Garcin et al., 2009; Chiu et al., 2010; Hodges et al., 2010; Kang et al, 2010; Nunnemann et al., 2011; Onyike, 2011
28 Gender Onset Clinic Death Features FamHx Tau Ubiq TDP4 3 Diagnosis Case 1 F DEP, COGIMP None + - N FTD17 Case 2 M SCHIZ None FTD-MND Case 3 M? APATH/DISIN? - -? DLDH Case 4 M BIPOLAR None - + N FTD-U Case 5 M SCHIZ None FTD-MND Case 6 M DEP/APATH YOD FTD-U (PGRN) Case 7 M SCHIZ FTD-MND - +? FTD-ID Case 8 M APATH FTD FTD17 Case 9 M COGIMP None FTD-ID Case 10 F? COGIMP YOD + - N FTD17 Case 11 M COGIMP/APATH MND* - +? FTD-U Case 12 M? COGIMP FTD N FTD17 Case 13 F COGIMP LOD - +? FTD-U Case 14 F COGIMP None FTD-ID Case 15 M COGIMP/PSP AD + - N PSP Case 16 M DISIN/COGIMP None FTD-ID Case 17 F COGIMP None FTD-MND Sources: Velakoulis et al., 2009
29 Sources: Momeni et al., 2009
30 Case Gender Age at onset Age at death Phenotype Clinical diagnosis Pathology diagnosis AO M Apathy, poor self-care AD FTD-tau ME F Apathy, distractibility, hyperorality JE M Disinhibition, asocial behavior, apathy Dementia NOS DLB FTD-ni FTD-U EU M Amnestic AD FTD-ni GW M Disinhibition, perseveration, executive dysfunction AD FTD-ni RC M Apathy, apraxia, Parkinsonism CBD FTD-tau PH F Amnesia, disorientation, apathy, poor self-care, food fads AD FTD-U/AD AW F Amnestic AD FTD-tau Sources: C. Onyike, Data from the JH Brain Resource Center
31 30 Mild dementia Cognitive symptoms Severe dementia MMSE score Decline in ADLs Behavioral problems 0 Nursing-home care Death Years
32 Natural history Sources: Kertesz et al., 2005, 2007
33 Natural history Sources: Kertesz et al., 2005, 2007
34 Natural history Sources: Kertesz et al., 2005, 2007
35 Sources: Libon et al., 2009
36 Sources: Seelaar et al., 2010
37 Syndrome to disease (phenotype:pathology) correlation is imperfect Sources: Boeve, 2007
38 Syndrome : proteinopathy Syndrome : gene Sources: Boeve, 2007
39 Disease Phenotype Age at onset DIagnosis FTD Asocial, dysexecutive dementia <60 Focal frontal or temporal atrophy Alzheimer disease Amnestic dementia >65 Global atrophy Major depression Intermittent depression <30 Normal cognition; no atrophy OCD Bipolar disorder Schizophrenia Obsessions, compulsions and anxiety Intermittent mania and depression Intermittent or chronic psychosis <30 Normal insight and cognition; no atrophy <35 Normal cognition; no atrophy <30 No compulsions; stable cognition; no atrophy
40 History - proxy interview is essential! Bedside cognitive measures: MMSE, mmmse (3MS), MOCA, verbal fluency tasks, CDR, clock drawing, digit span, Trail Making Test (parts A and B), picture naming tasks, picture matching Formal neuropsychological testing Brain imaging EEG CSF analysis
41 Sources: C. Onyike, unpublished data from the Maryland Assisted Living Study O n y i k
42 Date MMSE 3MS CDR Jun Oct Jan Mar Jun Sep 2009: Poor CVLT Category-cued fluency = 5 Digit span (reverse) = 4 BNT (15-item) = 10 CGIC: Mild decline Sep Sources: C. Onyike, data from JH FTD-YOD Clinic
43 Impairments of emotion recognition (face, voice and language) Impairments of Theory of Mind Poor social reasoning Loss of autonomy (environment-dependence, stimulus bound, utilization behavior) Environment agnosia (i.e., inability to perceive contexts) Indifference Loss of social attachments
44 Which of the three children at the bottom of the page feels the same as the one above?
45 Sources: Baron-Cohen, 2001 Reflective, impatient or irritated?
46 Jill had just moved into a new apartment. Jill went shopping and bought some new curtains for her bedroom. When she had just finished decorating the apartment her best friend Lisa came over. Jill gave her a tour of the apartment: How do you like my bedroom? Those curtains are horrible Lisa said, I hope you re going to get some new ones Questions: Did someone said something they shouldn t have? What did they say that they should not have said? Why do you think they said it? Control question Courtesy of Eleni Aretouli, JH Neuropsychology
47 First-order false belief question: Where is Sally going to look for her ball? Second-order false belief question: Where does Anne think Sally is going to look for her ball? Wimmer and Perner, 1983
48 Marjoram et al., 2005
49 Task b-ftd a-ppa s-ppa l-ppa Fluency +hesitations Production Speech apraxia Errors phonemic semantic (mixed) Naming / Repetition Reading (literal) surface dyslexia* Writing telegraphic Spelling omissions surface dysgraphia Comprehension for sentences for words Verbal fluency Letters < categories Letters > categories *Difficulty reading irregularly spelled words, along with regularization errors Regularization errors in spelling, for example colonel spelled as curnal and soldiers solgers
50 Listening: Word searching, fluency, grammar, articulatory struggle, production, content, comprehension, (words and sentences) Probing: Narrative, naming, recognition/knowledge), repetition, spelling, writing
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53 Phenotype Mean Score SD Semantic PPA Agrammatic PPA Logopenic PPA Normal subjects Sources: A. Hillis
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57 Imaging of frontotemporal dementia (FTD) subtypes. (A) Frontal atrophy on axial fluid attenuated inversion recovery MRI. (B) Axial T1-weighted image of left temporal lobe atrophy. (C) Coronal T1-weighted MR image of left inferior frontal and superior temporal atrophy. (D) Axial T1- weighted MR image of predominant right temporal lobe atrophy. Sources: Seelaar et al., 2010
58 Sources: Sampson et al., 2003
59 Sources: C. Onyike, images from the JH FTD-YOD Clinic archives
60 Sources: C. Onyike, images from the JH FTD-YOD Clinic archives
61 Sources: C. Onyike, images from the JH FTD-YOD Clinic archives
62 Sources: A. Hillis, images from the JH Cognitive Neurology Clinic archives
63 Plasma GRN Levels (ng/ml) Var N Median IQR Range p Loss of function PGRN mutation Yes <0.001 No Gender M F Family history* (excludes cases with GRN mutation) Yes No Clinical FTD subtypes bvftd PNFA SD FA CBS Sources: Finch et al., 2009
64 Cut-point Senstivity 95% CI Specificity 95% CI Sources: Finch et al., 2009
65 Delayed diagnosis Limited availability of treatment Limited access to treatment Limited age-appropriate supportive care structures Heritability of the dementia Loss of employment Dependent children Children s adjustment Lack of natural peer group Financial pressures
66 Class Amantadine SSRI & SNRI* Neuroleptics Benzodiazepines Methylphenidate Mirtazapine Zolpidem Topiramate Agent/daily dosage Start mg BID; Max. 400 mg total Sertraline ( mg QAM); fluoxetine (10 40 mg QAM); paroxetine (20 60 mg QAM); citalopram (20 mg daily); venlafaxine ( mg daily) Quetiapine ( mg daily); aripiprazole (2.5 5 mg daily), olanzapine mg daily) Clonazepam ODT mg daily; lorazepam 0.5 1mg, PRN 5 20 mg daily mg at bedtime mg at bedtime; Zolpidem CR 12.5 mg at bedtime Start mg daily, target mg total
67 Class Amantadine Benzodiazepines Methylphenidate SDRI Agent/daily dosage Start mg BID; Max. 400 mg total Clonazepam ODT mg daily 5 20 mg daily Bupropion ( mg daily) Failed trials: Cholinesterase inhibitors, memantine, steroids, bromocriptine, lithium (adverse effects), intraspinal ethanercept, omental transplant, transcranial magnetic stimulation (TMS) Antidepressants and psychosocial interventions limit depression and risk for suicide
68 Support groups & psychotherapy Problem Solving Therapy, PST Behavior/environment modifications Speech therapy (especially early in the illness) Augmentative/Alternative Communication (AAC) interventions Occupational therapy interventions Physical therapy Swallowing/dietary interventions
69 Stage Intervention Partner participation No noticeable disability in selfexpression Lapses in self-expression, with dysfluencies Noticeably disabled language use (agrammatism, circumlocutions, telegraphing, paraphasias) Severely disabled language use No functional speech/language Sources: Fried-Oken, 2008 Education Behavioral strategies to support conversation Low tech AAC and training on downshifting for most effective communication strategy Introduction of additional tools and techniques for multimodal communication system, including speech generating devices Reduce tool choice if options are overwhelming; family/carer education and environmental support for established multi modal communication system. Education Learn how to ask questions, reduce conversation demands, provide choices, and alter verbal and physical environment to support communication Learn strategies and message selection techniques to identify visual forms of mental dictionary Learn strategies and operations of each tool. Message selection techniques to identify visual forms of mental dictionary. Partners become pivotal in successful interaction. They may carry the content of conversation while supporting participation with multi-modal techniques.
70 tdcs: weak electrical current passed to target areas of the cortex, via electrodes placed on the head.
71 % Correct Written Naming of Objects Sources: Lacey et al., 2011
72 NORMAL IMPAIRMENT None (0) Slight (1) Mild (2) Moderate (3) Severe (4) Awareness & Orientation Fully oriented to self, time, space, location, navigation and/or context Modest/occasional disorientation. Occasional need for cues Significant disorientation. Regularly relies on cues Marked disorientation. Generally needs guidance Complete disorientation; may be self aware; constant need for direction Speech & communication Normal speech fluency, and no impairment in comprehension or pragmatics (exchange) Detectable abnormality of fluency, comprehension, or pragmatics, but has no difficulty conversing Obvious impairment, but with effort or assistance is able to converse Marked impairments, cannot converse, usually provides responses, can makes some requests and comments Little or no communication; generally not able to provide responses, or to make requests or comments Self care & home maintenance Normal, does not need any help with home maintenance and selfcare tasks Slight difficulty; may need occasional reminders Often needs reminders and prompting; needs supervision with complex or multistep tasks Needs supervision and practical assistancewith most tasks Complete dependence on others for self-care Life skills & problem-solving No difficulty with home or work skills, routines, or transactions, or in solving everyday problems Modest/occasional difficulty, performance is generally adequate Significant difficulty; frequent judgment errors; performance is impaired, needs supervision Marked difficulty; judgment very impaired; can make only simple decisions, can do simple tasks like folding laundry Basic skills essentially lost. Cannot make any judgments or do any tasks; generally requires assistance with basic tasks Comportment & socialization Normal attitudes, habits and conduct. Normal involvement in family, professional and community activities. Detectable changes in behavior, social judgment and conduct. May be apparent to intimates only. Has little or no impact on life activities Obvious changes in behavior, social judgment and conduct, May require supervision and cues for participation in life activities Everyday conduct is dominated by abnormal behaviors. Shows modest or no participation in life activities. Needs supervision and direction Profound disruption of behavior, showing loss of purpose/coherence. Little or no meaningful interaction with others. Generally needs to be steered
73 Appropriately individualized Close involvement of the family Respect for advanced directives Mindful of the dementia quandry
74 Davunetide for PSP Memantine for FTD?? Clinical trials
75 Memantine group Placebo group Outcomes: 1. NPI total score 2. CDR-SOB (FTD vers.), CGI-C, MMSE, FBI, FAQ, TFLS, EXIT25, mupdrs, UCSF battery, and time to antipsychotic Rx 3. Adverse effects Duration 26 weeks Visit schedule: -5, 0, 3, 6, 9, 12, 18, 26 N = 140 cases from 11 centers in North America Sponsored by Forest Lab. Inc.
76 Formulary compounds Novel compounds Pluripotent stem cells Drosophila C. Elegans Zebra fish Mouse Clinical trials Stratified by phenotype Tauopathies TDP-43 FUS
77 The Alzheimer Association at or for the local chapter Association for Frontotemporal dementias at The CJD Foundation at Websites at JHH, UCSF, the Mayo Clinics several other universities, and the NIH SOME EXCELLENT BOOKS: What if it is not Alzheimer s: A Caregiver s Guide to Dementia - Lisa and Gary Radin, editors The Banana Lady and Other Stories of Curious Behavior - Andrew Kertesz The Family That Couldn t Sleep: A Medical Mystery - D.T. Max The 36 Hour Day - Nancy Mace and Peter Rabins
78 FTD/ YOD Clinic: Peter Rabins, MD Brian Appleby, MD Greg Pontone, MD Shawn Smyth, MD Mary Anne Wylie, RN Rebecca Rye, RN Kate Hicks, MPH Neuropsychiatry: Kostas Lyketsos, MD Cognitive Neurology: Marilyn Albert, PhD Argye Hillis, MD FTD Research Group Kelly Sloane Sandeepa Sur Neuropsychology Jason Brandt, PhD Eleni Aretouli, PhD Rehabilitation Psychology Kathleen Kortte, PhD Neuropathology Juan Troncoso, MD Olga Pletnikova Packard Center for ALS Jeff Rothstein, MD, PhD Nick Maragakis, MD Lora Clawson, RN Myositis Center Andrew Mammen, MD Lisa Christopher-Stine, MD Thomas Lloyd, MD
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