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DEMENTIA AND GERIATRIC COGNITIVE DISORDERS
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ORIGINAL RESEARCH ARTICLE
Free Access
NEUROPSYCHIATRIC SYMPTOMS IN PRIMARY PROGRESSIVE APHASIA AND APRAXIA OF SPEECH
Singh T.D.a · Duffy J.R.a · Strand E.A.a · Machulda M.M.b · Whitwell J.L.c ·
Josephs K.A.a
Author affiliations
Departments of aNeurology, bPsychiatry and Psychology and cNeuroradiology, Mayo
Clinic, Rochester, Minn., USA
Corresponding Author
Keith A. Josephs, MD, MST, MSc
Department of Neurology, Mayo Clinic
200 First St. SW - Mayo W8B
Rochester, MN 55905 (USA)
E-Mail josephs.keith@mayo.edu
Keywords: Neuropsychiatric symptomsPrimary progressive aphasiaProgressive
apraxia of speech
RELATED ARTICLES FOR ""
Dement Geriatr Cogn Disord 2015;39:228-238
https://doi.org/10.1159/000369062
* Abstract
* FullText
* PDF
* References
* Extras : 7
ABSTRACT
Aim: To conduct a prospective analysis of the neuropsychiatric symptoms (NPS)
across the three categories of primary progressive aphasia (PPA) and progressive
apraxia of speech (PAOS), compare the prevalence and nature of the symptoms, and
look at which symptoms could be helpful to better differentiate these PPA and
PAOS categories. Methods: A total of 106 consecutive patients with a diagnosis
of semantic variant (n = 13), logopenic variant (n = 37), agrammatic variant (n
= 15) or PAOS (n = 41) were included in this prospective study. The NPS were
measured by the Neuropsychiatric Inventory Questionnaire. Results: There were 65
patients with PPA and 41 with PAOS diagnosis. The most distinguishing features
between the two groups were anxiety, apathy, aberrant motor behavior and
appetite, while among the subtypes of PPA they were disinhibition and appetite
changes. PPA and PAOS patients initially exhibited depression, but with
increased disease duration, PAOS patients showed apathy (55.5%) while PPA
patients showed disinhibition (28.6%) and aberrant motor behavior (14.3%).
Conclusion: Mood symptoms like anxiety and appetite changes are more likely to
be present at initial stages of PPA, whereas behavioral symptoms like aberrant
motor behavior and apathy are likely to occur early in PAOS. The NPS seem to
evolve with the progression of the disease in both PPA and PAOS.
© 2015 S. Karger AG, Basel
--------------------------------------------------------------------------------
INTRODUCTION
Primary progressive aphasia (PPA) is a group of neurodegenerative disorders,
which present with language impairment as the most characteristic feature [1].
The diagnosis of PPA requires that an insidiously progressive language
impairment should be the primary cognitive deficit for approximately 2 years
after the symptom onset with no or minimal change in other cognitive functions
including memory, visuospatial skills and executive abilities [2]. However, as
the disease progresses, other cognitive domains may become impaired leading to
PPA-plus, although the language impairment remains the most prominent anomaly
[3]. A new classification was proposed in 2011, segregating the PPA patients
into three categories based on their type of speech impairment [4]. The first
category is known as the semantic variant (svPPA) and is characterized by anomia
and impaired single word comprehension. The second is the logopenic variant
(lvPPA), which is characterized by impaired single word retrieval and impaired
repetition of phrases. The third is the agrammatic variant (agPPA), which
includes patients with grammatical errors in written and verbal language. More
recently, another category of patients with neurodegenerative speech disorders
has been identified known as progressive apraxia of speech (PAOS). These
patients present with a motor speech neurodegenerative disorder with speech
impairment being the sole or dominant sign or symptom [5,6].
Since PPA and PAOS are primarily neurodegenerative speech disorders, there has
been a lot of research looking into the neuropathology and clinical features.
However, little has been reported about the neuropsychiatric aspects. These
aspects may be helpful as clinical markers for different stages and may help in
categorizing patients between PPA and PAOS. There have been some studies looking
at the neuropsychiatric symptoms (NPS) of PPA [7,8,9,10] but only one analyzed
the symptoms according to PPA subtypes [10], and that study used an older PPA
classification. Most of the previous studies also had relatively smaller
cohorts. There have not been any studies looking into the neuropsychiatric
aspects of PAOS patients.
In this study, we conducted a prospective analysis of the NPS across the three
categories of PPA and PAOS to compare the prevalence and nature of the symptoms
and look at the factors that may help us to better differentiate these
categories.
METHODS
STANDARD PROTOCOL APPROVALS AND PATIENT CONSENTS
The study was approved by the Mayo Clinic Institutional Review Board, and all
subjects signed consent forms for enrollment into the study.
PATIENT SELECTION
All patients who presented to the Mayo Clinic in Rochester, Minn., USA between
July 2010 and March 2014 with a suspected speech and language disorder secondary
to a neurodegenerative process were recruited prospectively. Subjects with
concurrent illnesses that could account for language deficits or meeting
criteria for other neurodegenerative syndrome were excluded. Only patients over
the age of 18, with an informant to provide independent evaluation of
functioning and who spoke English as their primary language were included. All
patients underwent detailed speech and language examination, neurological
evaluation, neuropsychological testing and neuroimaging analysis over a span of
48-72 h.
CLINICAL DIAGNOSTIC CLASSIFICATION
To be included in the study, patients must have had svPPA, lvPPA, agPPA or PAOS.
Patients with PPA as a primary diagnosis and who were not able to be classified
among any of the three categories (svPPA, lvPPA and agPPA) were not included in
this study. Quantitative scores and video recordings of all the crucial aspects
of the speech and language assessments were reviewed for all the study
participants by 2 speech-language pathologists separately (J.R.D. and E.A.S.)
for consensus agreement about the diagnosis.
Study participants who, by consensus agreement, demonstrated apraxia of speech
(AOS) without, or with less prominent, aphasia, were classified as PAOS, based
on the published criteria [5,6]. Any participant who, by mutual agreement among
the speech pathologists, demonstrated features of PPA was analyzed for the
diagnostic features of each PPA subtype [4]. All participants had disrupted
normal activities of daily living (talking on the phone, writing a letter) due
to speech or language dysfunction. None complained of early deficits in other
cognitive domains.
In accordance with the consensus guidelines for the classification of PPA, tasks
for the evaluation of speech and language functions were qualitatively utilized
for the assessment of the presence or absence of each diagnostic feature of the
individual variants.
NEUROPSYCHIATRIC EXAMINATION
All patients underwent detailed neurological examination by a behavioral and
movement disorder specialist (K.A.J.) as well as standardized testing of
cognitive, behavioral, functional and motor performance.
The NPS of all cases across different categories were measured by the
Neuropsychiatric Inventory Questionnaire (NPI-Q) [11]. The NPI-Q measures and
grades 12 behavioral domains according to the severity of the symptoms and the
distress that is experienced by the caregiver due to those symptoms in the last
30 days. The distress index was not analyzed for this study. The severity of the
symptoms was graded as 1-3, with 1 being mild and 3 being severe. The 12
behavioral domains that are measured can be subcategorized as
behavioral/compartmental (aberrant motor behavior, disinhibition,
apathy/indifference), appetite/eating disorder, mood symptoms (anxiety,
euphoria/elation, irritability/lability, depression) and disruptive/psychotic
symptoms (delusions, hallucinations, agitation/aggression, nighttime behavior).
Adding the total score of the 12 behavioral domains yielded the total NPI score.
In our study population, the NPI-Q testing was done by a behavioral neurologist
(K.A.J.). The NPI-Q has been shown to be a reliable and valid scale for testing
NPS [11,12].
STATISTICAL ANALYSIS
Statistical analysis was performed using JMP 9.0.1 (SAS Institute Inc., Cary,
N.C., USA). The analysis was done at the conventional two-tailed α level of
0.05. Group differences for categorical variables were assessed with the χ2 test
and Fisher's exact test for small numbers. Differences in the continuous
variables were assessed using the Kruskal-Wallis one-way analysis of variance.
Mann-Whitney U post hoc testing was performed if Kruskal-Wallis testing was
significant. Multivariate regression analysis was used to compare the two groups
of PPA and PAOS, and the odds ratio (OR) and 95% confidence interval (CI) were
computed. Demographics and neuropsychological profiles were summarized as
percentages and means ± SD.
RESULTS
We included 106 patients [56 (52.8%) males and 50 (47.2%) females] with a mean
age at onset of 63.9 ± 8.1 years who fulfilled the above criteria for the
diagnosis of either PPA or PAOS during the study period. The mean age at testing
was 66.8 ± 8 years, and their Mini-Mental State Examination (MMSE) score was
27.3 ± 2.5. After the final segregation, there were 65 patients with PPA and 41
with PAOS diagnosis. When the PPA patients were further categorized in
accordance with the latest guidelines [4], it yielded 15 (23.1%) with agPPA, 37
(56.9%) with lvPPA and 13 (20.0%) with svPPA diagnosis. The only significant
difference between PPA and PAOS was observed on MMSE, with patients with PAOS
presenting with a significantly higher mean MMSE. However, MMSE and illness
duration were different among the various subtypes of PPA. The breakdown of the
demographic variables, education, MMSE, age at onset and testing according to
the patients' final diagnosis is presented in table 1. The demographics
according to the subtypes of PPA are presented in table 2.
TABLE 1
Demographics according to diagnosis
TABLE 2
Demographics according to PPA subtypes
There were no significant differences in the NPS between the PPA and PAOS
patient groups when compared according to the severity of the NPI score. The
frequency of distribution of NPS across PPA and PAOS according to the NPI
breakdown is shown in table 3 and figure 1. However, significant differences
became more apparent when the two groups were compared according to the presence
or absence of the NPI-Q symptoms. The most distinguishing features between the
two groups were anxiety (p = 0.0282), apathy (p = 0.0217), aberrant motor
behavior (p = 0.0344) and appetite (p = 0.0068). The patients with PPA were 3.5
times more likely to have anxiety and 12.2 times more likely to have appetite
abnormalities. However, apathy was 3.2 times and aberrant motor behavior 9.1
times more likely to be present in patients with PAOS. Delusions and euphoria
were present only in the PPA patients, and hallucinations and nighttime behavior
abnormalities were present in only 3 (2.8%) and 6 (5.7%) patients across both
groups. Further details of the multivariate analysis comparing PPA and PAOS are
shown in table 4.
TABLE 3
NPS in PPA and PAOS
TABLE 4
Multivariate logistic regression analysis for NPI symptoms present or absent in
PPA and PAOS
FIG. 1
Distribution of NPS across PPA and PAOS according to the NPI breakdown.
When comparing the three subtypes of PPA (agPPA, lvPPA and svPPA), the most
significant differentiating symptoms among them were disinhibition and appetite.
Delusion and hallucination were present only in lvPPA, whereas aberrant motor
behavior abnormalities were not present in this group. The details of NPS
according to their severity among the three groups of PPA patients are presented
in table 5.
TABLE 5
NPS among different PPA subtypes
DISCUSSION
Our study with a large series of patients with PPA and PAOS - the largest
collection of PAOS cases to date - highlights the behavioral differences between
PPA and PAOS and among the three categories of PPAs. Mood symptoms like anxiety
and appetite changes are more likely to be present in PPA, whereas PAOS patients
are more likely to have behavioral symptoms like aberrant motor behavior and
apathy. Among the three categories of PPA, svPPA patients are more likely to
show disinhibition, while appetite changes are more likely to be present in
svPPA and agPPA patients.
AOS is a disorder of speech motor planning or programming that affects the
production of speech [13]. More recently, AOS has been demonstrated in the
context of neurodegenerative disorders [6,13,14]. In fact, a syndrome with motor
speech impairment as the presenting sign in the absence of any aphasia is
referred to as primary progressive apraxia of speech [6], which is subsumed
under PAOS [5]. In our study, caregivers of PAOS most commonly endorsed apathy
(48.8%), irritability (46.3%), depression (31.7%), anxiety (22%) and agitation
(19.5%). The less common symptoms were aberrant motor behavior (12.2%),
nighttime behavior abnormalities (4.9%), appetite changes (4.9%) and
disinhibition (4.9%). Delusion and euphoria were not present in any of our
patients. PAOS patients are therefore more likely to demonstrate behavioral
abnormalities like apathy and aberrant motor behavior abnormalities when
compared to PPA patients. These findings are not unexpected as PAOS has often
been linked to progressive supranuclear palsy (PSP) pathology [15], and profound
apathy is often a common and supportive feature of PSP [16,17]. PAOS patients
also demonstrate midbrain atrophy, which is a feature of pathologically
confirmed PSP [5,18]. This association has been further quantified in a recent
study showing the evolution of primary progressive apraxia of speech, which
demonstrated that such patients may progress to a PSP-like syndrome referred to
as PSP-AOS [19].
There have been some studies looking at the NPS of PPA patients [7,8,9,10].
However, none of them compared the various subtypes of PPA according to the
latest classification. In our cohort of PPA patients, the most common
presentation was lvPPA (56.9%). The earliest age at onset of PPA was 61.7 ± 6.5
years in svPPA patients, whereas agPPA patients presented the earliest to the
hospital (2.3 ±1.4 years). Differentiating symptoms among the three subtypes of
PPA were disinhibition (p = 0.0245) and appetite changes (p = 0.006).
Disinhibition was more likely to be present in svPPA compared to the other two
subtypes. Interestingly, although disinhibition is the most common in svPPA
compared to the other PPA variants and PAOS, it has been shown to be less common
in semantic dementia compared to the behavioral variant of frontotemporal
dementia [20]. The appetite changes were highly significant among the three
groups, with svPPA and agPPA patients more likely to present with these changes.
Depression was present in 43% of PPA patients, with the lvPPA diagnosis
encompassing the majority of patients (60.7%). Depression has also been observed
in PPA patients [1,21,22]. Interestingly, depression was present in 4 of the 6
PPA patients that were first reported by Mesulam [1] in 1982.
In our study, delusion and hallucinations were present in only lvPPA among the
PPA patients. This is a novel finding and could be due to the fact that lvPPA
has been linked to the Alzheimer's disease pathology which can co-occur with
Lewy body disease [23]. Lewy body disease is strongly associated with
hallucinations. In fact, in a recent clinicopathological series, mixed
Alzheimer's and Lewy body disease was reported in 8% of lvPPA cases [24].
Some researchers have suggested that PAOS should not be considered different
from patients with nonfluent/agPPA, although we have clearly demarcated that
PAOS is anatomically different from agPPA with involvement of the bilateral
superior and mid-premotor cortex [5], in contrast to agPPA, which affects the
left posterior frontoinsular cortex [2]. The findings of this study further
strengthen the argument of segregating them as the patients with PPA were more
likely to have mood symptoms like anxiety and appetite changes, while PAOS
patients are more likely to have behavioral symptoms like aberrant motor
behavior and apathy.
The type of behavioral symptoms changed over time with longer disease durations.
Patients with both PPA and PAOS showed symptoms initially inclined towards mood
disorders like depression. This may be related to an emotional response towards
the disease affecting their daily communication capabilities. However, with the
increase in disease duration, PAOS patients more likely showed apathy (55.5%),
while PPA patients more likely showed disinhibition (28.6%) and aberrant motor
behavior (14.3%). The PPA symptoms present in the initial 5 years, and those
that develop afterwards, are consistent with previous reports [7]. These
findings suggest that, as PPA progresses, the neurodegenerative process expands
and eventually involves the brain regions affecting behavior, such as the
frontal lobe [2,18,25]. Another interesting finding that has not previously been
reported was the fact that some of the behavioral symptoms present early in the
disease (<5 years) appeared to resolve over time. For example, aberrant motor
behaviors, while present in 15.6% of the PAOS subjects <5 years after onset,
were no longer present after 5 years of illness duration. The details of the NPS
present before and after 5 years for both PAOS and PPA are shown in table 6.
TABLE 6
NPS according to disease duration
The NPS associated with both PPA and PAOS may have treatment implications for
physicians as well as for patients and their caregivers. With better knowledge
of the NPS associated with these neurodegenerative disorders, appropriate
psychosocial education and support can be outlined for both patients and their
caregivers and may help them in handling the behaviors. Patients with PPA might
also have emotion recognition disturbances that are mediated by attentional
deficits [26]. Hence, with a better knowledge of the relationship between
illness duration and the appearance of a specific NPS, physicians are better
able to discuss long-term outcomes and treatment options.
This study has some limitations. Although there have been studies showing the
reliability and validity of the NPI-Q [11,12], the NPI-Q is a brief measure of
symptom assessment asking just one question per symptom domain. The simple and
brief nature of the NPI-Q may not necessarily capture the nuances of some
particularly complex symptoms, particularly during the earlier stages of the
illness. For example, it is difficult to know whether patients present with mild
depression/anxiety due to an emotional response secondary to language
impairment, or due to a noncognitive manifestation of the neurodegenerative
process. Another limitation is that the estimation of disease duration is
subjective, and we could not follow the progression of behavioral symptoms.
Hence, further studies are needed to access the potential mechanisms linking NPS
with these disorders, and long-term follow-up of subtypes of PPA and PAOS
patients may help in understanding the natural history and evolution of their
NPS.
In conclusion, the result of this study highlights the differences in the NPS
between the two categories of neurodegenerative speech disorders, PAOS and PPA
as well as among the different subtypes of PPA patients. Mood symptoms like
anxiety and appetite changes are more likely to be present at initial stages of
PPA, whereas behavioral symptoms like aberrant motor behavior and apathy are
likely to occur in PAOS. Additionally, it appears that NPS evolve with the
progression of the disease and may not always be present. A better understanding
of the NPS among these groups of patients helps to better outline a treatment
strategy for both the patient and the caregiver.
ACKNOWLEDGMENT
This study was supported by NIH R01-DC010367.
DISCLOSURE STATEMENT
T.D. Singh reports no disclosures. J.R. Duffy is a coinvestigator for
R01-DC012519 and R01-DC010367. E.A. Strand is a coinvestigator for R01-DC012519
and R01-DC010367. M.M. Machulda is funded by R01-AG037491 (Co-I), R01-DC012519
(Co-I) and the Alzheimer's Association (Co-I). J.L. Whitwell is funded by
R01-DC012519 (PI), R01-DC010367 (Co-I), R01-AG037491 (Co-I) and the Alzheimer's
Association (PI). K.A. Josephs is funded by NIH R01-DC010367 (PI), R01-AG037491
(PI), R01-DC012519 (Co-I) and the Alzheimer's Association (Co-I).
--------------------------------------------------------------------------------
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REFERENCES
1. Mesulam MM: Slowly progressive aphasia without generalized dementia. Ann
Neurol 1982;11:592-598.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
2. Bonner MF, Ash S, Grossman M: The new classification of primary progressive
aphasia into semantic, logopenic, or nonfluent/agrammatic variants. Curr
Neurol Neurosci Rep 2010;10:484-490.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
3. Mesulam MM: Primary progressive aphasia: a 25-year retrospective. Alzheimer
Dis Assoc Disord 2007;21:S8-S11.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
4. Gorno-Tempini ML, Hillis AE, Weintraub S, Kertesz A, Mendez M, Cappa SF,
Ogar JM, Rohrer JD, Black S, Boeve BF, Manes F, Dronkers NF, Vandenberghe
R, Rascovsky K, Patterson K, Miller BL, Knopman DS, Hodges JR, Mesulam MM,
Grossman M: Classification of primary progressive aphasia and its variants.
Neurology 2011;76:1006-1014.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
5. Josephs KA, Duffy JR, Strand EA, Machulda MM, Senjem ML, Lowe VJ, Jack CR
Jr, Whitwell JL: Syndromes dominated by apraxia of speech show distinct
characteristics from agrammatic PPA. Neurology 2013;81:337-345.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
6. Josephs KA, Duffy JR, Strand EA, Machulda MM, Senjem ML, Master AV, Lowe
VJ, Jack CR Jr, Whitwell JL: Characterizing a neurodegenerative syndrome:
primary progressive apraxia of speech. Brain 2012;135:1522-1536.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
7. Banks SJ, Weintraub S: Neuropsychiatric symptoms in behavioral variant
frontotemporal dementia and primary progressive aphasia. J Geriatr
Psychiatry Neurol 2008;21:133-141.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
8. Fatemi Y, Boeve BF, Duffy J, Petersen RC, Knopman DS, Cejka V, Smith GE,
Geda YE: Neuropsychiatric aspects of primary progressive aphasia. J
Neuropsychiatry Clin Neurosci 2011;23:168-172.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
9. Marczinski CA, Davidson W, Kertesz A: A longitudinal study of behavior in
frontotemporal dementia and primary progressive aphasia. Cogn Behav Neurol
2004;17:185-190.
External Resources
* Pubmed/Medline (NLM)
10. Rohrer JD, Warren JD: Phenomenology and anatomy of abnormal behaviours in
primary progressive aphasia. J Neurol Sci 2010;293:35-38.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
11. Cummings JL, Mega M, Gray K, Rosenberg-Thompson S, Carusi DA, Gornbein J:
The neuropsychiatric inventory: comprehensive assessment of psychopathology
in dementia. Neurology 1994;44:2308-2314.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
12. Kaufer DI, Cummings JL, Ketchel P, Smith V, MacMillan A, Shelley T, Lopez
OL, DeKosky ST: Validation of the NPI-Q, a brief clinical form of the
neuropsychiatric inventory. J Neuropsychiatry Clin Neurosci
2000;12:233-239.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
13. Duffy J: Apraxia of speech in degenerative neurologic disease. Aphasiology
2006;20:511-527.
External Resources
* Crossref (DOI)
14. Josephs KA, Duffy JR, Strand EA, Whitwell JL, Layton KF, Parisi JE, Hauser
MF, Witte RJ, Boeve BF, Knopman DS, Dickson DW, Jack CR Jr, Petersen RC:
Clinicopathological and imaging correlates of progressive aphasia and
apraxia of speech. Brain 2006;129:1385-1398.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
15. Josephs KA, Boeve BF, Duffy JR, Smith GE, Knopman DS, Parisi JE, Petersen
RC, Dickson DW: Atypical progressive supranuclear palsy underlying
progressive apraxia of speech and nonfluent aphasia. Neurocase
2005;11:283-296.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
16. Burrell JR, Hodges JR, Rowe JB: Cognition in corticobasal syndrome and
progressive supranuclear palsy: a review. Mov Disord 2014;29:684-693.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
17. Josephs KA, Whitwell JL, Eggers SD, Senjem ML, Jack CR Jr: Gray matter
correlates of behavioral severity in progressive supranuclear palsy. Mov
Disord 2011;26:493-498.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
18. Josephs KA, Duffy JR, Strand EA, Machulda MM, Senjem ML, Lowe VJ, Jack CR
Jr, Whitwell JL: Syndromes dominated by apraxia of speech show distinct
characteristics from agrammatic PPA. Neurology 2013;81:337-345.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
19. Josephs KA, Xia R, Mandrekar J, Gunter JL, Senjem ML, Jack CR Jr, Whitwell
JL: Modeling trajectories of regional volume loss in progressive
supranuclear palsy. Mov Disord 2013;28:1117-1124.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
20. Josephs KA, Duffy JR, Strand EA, Machulda MM, Senjem ML, Gunter JL, Schwarz
CG, Reid RI, Spychalla AJ, Lowe VJ, Jack CR Jr, Whitwell JL: The evolution
of primary progressive apraxia of speech. Brain 2014;137:2783-2795.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
21. Snowden JS, Bathgate D, Varma A, Blackshaw A, Gibbons ZC, Neary D: Distinct
behavioural profiles in frontotemporal dementia and semantic dementia. J
Neurol Neurosurg Psychiatry 2001;70:323-332.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
22. Starkstein SE, Robinson RG: Mood disorders in neurodegenerative diseases.
Semin Clin Neuropsychiatry 1996;1:272-281.
External Resources
* Pubmed/Medline (NLM)
23. Medina J, Weintraub S: Depression in primary progressive aphasia. J Geriatr
Psychiatry Neurol 2007;20:153-160.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
24. Gorno-Tempini ML, Dronkers NF, Rankin KP, Ogar JM, Phengrasamy L, Rosen HJ,
Johnson JK, Weiner MW, Miller BL: Cognition and anatomy in three variants
of primary progressive aphasia. Ann Neurol 2004;55:335-346.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
25. Harris JM, Gall C, Thompson JC, Richardson AM, Neary D, du Plessis D, Pal
P, Mann DM, Snowden JS, Jones M: Classification and pathology of primary
progressive aphasia. Neurology 2013;81:1832-1839.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
26. Chow TW, Fridhandler JD, Binns MA, Lee A, Merrilees J, Rosen HJ, Ketelle R,
Miller BL: Trajectories of behavioral disturbance in dementia. J Alzheimers
Dis 2012;31:143-149.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
27. Kumfor F, Miller L, Lah S, Hsieh S, Savage S, Hodges JR, Piguet O: Are you
really angry? The effect of intensity on facial emotion recognition in
frontotemporal dementia. Soc Neurosci 2011;6:502-514.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
--------------------------------------------------------------------------------
AUTHOR CONTACTS
Keith A. Josephs, MD, MST, MSc
Department of Neurology, Mayo Clinic
200 First St. SW - Mayo W8B
Rochester, MN 55905 (USA)
E-Mail josephs.keith@mayo.edu
--------------------------------------------------------------------------------
ARTICLE / PUBLICATION DETAILS
First-Page Preview
Accepted: October 10, 2014
Published online: January 21, 2015
Issue release date: February 2015
Number of Print Pages: 11
Number of Figures: 1
Number of Tables: 6
ISSN: 1420-8008 (Print)
eISSN: 1421-9824 (Online)
For additional information: https://www.karger.com/DEM
--------------------------------------------------------------------------------
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REFERENCES
1. Mesulam MM: Slowly progressive aphasia without generalized dementia. Ann
Neurol 1982;11:592-598.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
2. Bonner MF, Ash S, Grossman M: The new classification of primary progressive
aphasia into semantic, logopenic, or nonfluent/agrammatic variants. Curr
Neurol Neurosci Rep 2010;10:484-490.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
3. Mesulam MM: Primary progressive aphasia: a 25-year retrospective. Alzheimer
Dis Assoc Disord 2007;21:S8-S11.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
4. Gorno-Tempini ML, Hillis AE, Weintraub S, Kertesz A, Mendez M, Cappa SF,
Ogar JM, Rohrer JD, Black S, Boeve BF, Manes F, Dronkers NF, Vandenberghe
R, Rascovsky K, Patterson K, Miller BL, Knopman DS, Hodges JR, Mesulam MM,
Grossman M: Classification of primary progressive aphasia and its variants.
Neurology 2011;76:1006-1014.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
5. Josephs KA, Duffy JR, Strand EA, Machulda MM, Senjem ML, Lowe VJ, Jack CR
Jr, Whitwell JL: Syndromes dominated by apraxia of speech show distinct
characteristics from agrammatic PPA. Neurology 2013;81:337-345.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
6. Josephs KA, Duffy JR, Strand EA, Machulda MM, Senjem ML, Master AV, Lowe
VJ, Jack CR Jr, Whitwell JL: Characterizing a neurodegenerative syndrome:
primary progressive apraxia of speech. Brain 2012;135:1522-1536.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
7. Banks SJ, Weintraub S: Neuropsychiatric symptoms in behavioral variant
frontotemporal dementia and primary progressive aphasia. J Geriatr
Psychiatry Neurol 2008;21:133-141.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
8. Fatemi Y, Boeve BF, Duffy J, Petersen RC, Knopman DS, Cejka V, Smith GE,
Geda YE: Neuropsychiatric aspects of primary progressive aphasia. J
Neuropsychiatry Clin Neurosci 2011;23:168-172.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
9. Marczinski CA, Davidson W, Kertesz A: A longitudinal study of behavior in
frontotemporal dementia and primary progressive aphasia. Cogn Behav Neurol
2004;17:185-190.
External Resources
* Pubmed/Medline (NLM)
10. Rohrer JD, Warren JD: Phenomenology and anatomy of abnormal behaviours in
primary progressive aphasia. J Neurol Sci 2010;293:35-38.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
11. Cummings JL, Mega M, Gray K, Rosenberg-Thompson S, Carusi DA, Gornbein J:
The neuropsychiatric inventory: comprehensive assessment of psychopathology
in dementia. Neurology 1994;44:2308-2314.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
12. Kaufer DI, Cummings JL, Ketchel P, Smith V, MacMillan A, Shelley T, Lopez
OL, DeKosky ST: Validation of the NPI-Q, a brief clinical form of the
neuropsychiatric inventory. J Neuropsychiatry Clin Neurosci
2000;12:233-239.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
13. Duffy J: Apraxia of speech in degenerative neurologic disease. Aphasiology
2006;20:511-527.
External Resources
* Crossref (DOI)
14. Josephs KA, Duffy JR, Strand EA, Whitwell JL, Layton KF, Parisi JE, Hauser
MF, Witte RJ, Boeve BF, Knopman DS, Dickson DW, Jack CR Jr, Petersen RC:
Clinicopathological and imaging correlates of progressive aphasia and
apraxia of speech. Brain 2006;129:1385-1398.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
15. Josephs KA, Boeve BF, Duffy JR, Smith GE, Knopman DS, Parisi JE, Petersen
RC, Dickson DW: Atypical progressive supranuclear palsy underlying
progressive apraxia of speech and nonfluent aphasia. Neurocase
2005;11:283-296.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
16. Burrell JR, Hodges JR, Rowe JB: Cognition in corticobasal syndrome and
progressive supranuclear palsy: a review. Mov Disord 2014;29:684-693.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
17. Josephs KA, Whitwell JL, Eggers SD, Senjem ML, Jack CR Jr: Gray matter
correlates of behavioral severity in progressive supranuclear palsy. Mov
Disord 2011;26:493-498.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
18. Josephs KA, Duffy JR, Strand EA, Machulda MM, Senjem ML, Lowe VJ, Jack CR
Jr, Whitwell JL: Syndromes dominated by apraxia of speech show distinct
characteristics from agrammatic PPA. Neurology 2013;81:337-345.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
19. Josephs KA, Xia R, Mandrekar J, Gunter JL, Senjem ML, Jack CR Jr, Whitwell
JL: Modeling trajectories of regional volume loss in progressive
supranuclear palsy. Mov Disord 2013;28:1117-1124.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
20. Josephs KA, Duffy JR, Strand EA, Machulda MM, Senjem ML, Gunter JL, Schwarz
CG, Reid RI, Spychalla AJ, Lowe VJ, Jack CR Jr, Whitwell JL: The evolution
of primary progressive apraxia of speech. Brain 2014;137:2783-2795.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
21. Snowden JS, Bathgate D, Varma A, Blackshaw A, Gibbons ZC, Neary D: Distinct
behavioural profiles in frontotemporal dementia and semantic dementia. J
Neurol Neurosurg Psychiatry 2001;70:323-332.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
22. Starkstein SE, Robinson RG: Mood disorders in neurodegenerative diseases.
Semin Clin Neuropsychiatry 1996;1:272-281.
External Resources
* Pubmed/Medline (NLM)
23. Medina J, Weintraub S: Depression in primary progressive aphasia. J Geriatr
Psychiatry Neurol 2007;20:153-160.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
24. Gorno-Tempini ML, Dronkers NF, Rankin KP, Ogar JM, Phengrasamy L, Rosen HJ,
Johnson JK, Weiner MW, Miller BL: Cognition and anatomy in three variants
of primary progressive aphasia. Ann Neurol 2004;55:335-346.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
25. Harris JM, Gall C, Thompson JC, Richardson AM, Neary D, du Plessis D, Pal
P, Mann DM, Snowden JS, Jones M: Classification and pathology of primary
progressive aphasia. Neurology 2013;81:1832-1839.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
26. Chow TW, Fridhandler JD, Binns MA, Lee A, Merrilees J, Rosen HJ, Ketelle R,
Miller BL: Trajectories of behavioral disturbance in dementia. J Alzheimers
Dis 2012;31:143-149.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
27. Kumfor F, Miller L, Lah S, Hsieh S, Savage S, Hodges JR, Piguet O: Are you
really angry? The effect of intensity on facial emotion recognition in
frontotemporal dementia. Soc Neurosci 2011;6:502-514.
External Resources
* Pubmed/Medline (NLM)
* Crossref (DOI)
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1. Abstract
2. Introduction
3. Methods
1. Standard Protocol Approvals and Patient Consents
2. Patient Selection
3. Clinical Diagnostic Classification
4. Neuropsychiatric Examination
5. Statistical Analysis
4. Results
5. Discussion
6. Acknowledgment
7. Disclosure Statement
8. References
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