Keywords:
Frontotemporal Dementia - Deglutition Disorders - Feeding Behavior - International
Classification of Functioning, Disability and Health - Cognition Disorders
Palavras-chave:
Demência Frontotemporal - Transtornos da Deglutição - Comportamento Alimentar - Classificação
Internacional de Funcionalidade, Incapacidade e Saúde - Transtornos Cognitivos
INTRODUCTION
Swallowing is a complex and synchronized neuromuscular process during feeding that
includes sensory and motor aspects. It starts with voluntary mechanisms that are highly
dependent upon cognition, language, behavior and funcionality; therefore, swallowing
consists on the following five phases[1]: the first phase (anticipatory) precedes the food in the oral cavity; the second
phase (oral preparatory) is related to the preparation of the bolus with oral motor
acts; the third phase (oral phase) is characterized by the backward movement of the
tongue for oral ejection of food; the fourth (pharyngeal) and the fifth phases (esophageal)
are involuntary. The voluntary phases of swallowing (anticipatory, oral preparatory,
and oral) are also influenced by functional, cognitive and behavioral aspects that
can result in dysphagia and malnutrition[2],[3].
Behavioral variant frontotemporal dementia (bvFTD) is a clinical syndrome characterized
by progressive changes in behavior and personality, whereas at least three of the
following clinical features must be present: early disinhibition, early apathy, loss
of empathy for others, overeating, compulsions, and frontal executive loss; these
features may occur in isolation or in addition to executive dysfunction[4],[5],[6],[7]. Dysphagia is common in neurodegenerative diseases[2],[3]. Feeding problems previously described in bvFTD include loss of social graces when
eating, eating quickly, increased appreciation of sweet foods, hyperphagia, and hyperorality[8],[9]. Several studies have assessed feeding behavior in bvFTD, but there is little information
regarding swallowing problems[8],[9],[10], and no description of the feeding situation of these patients with their caregivers.
In view of the well-known clinical features of patients with bvFTD, particularly regarding
the pattern of neuropsychiatric symptoms, we hypothesized that swallowing and feeding
would have peculiar characteristics in this dementia syndrome in comparison with other
neurodegenerative diseases. Herein, our aims were to characterize feeding and swallowing
features in patients with bvFTD in mild, moderate and severe dementia stages, and
to correlate ensuing swallowing problems with functionality, executive dysfunction,
and cognitive and behavioral features.
METHODS
In this uncontrolled cohort, outpatients with bvFTD[4] were consecutively recruited from the Behavioral Neurology Section of Hospital São
Paulo, Universidade Federal de São Paulo (UNIFESP), and from the Neurology Service
of Hospital das Clínicas, Universidade de São Paulo (USP), from March 2012 to September
2013 (19 months). Diagnosis of bvFTD was based on the international consensus research
criteria for behavioral variant frontotemporal dementia[4]. All patients and their caregivers were evaluated by neurologists with expertise
in neurocognition and dementia, and by a speech therapist. Patients with previous
history of stroke, Parkinson’s disease, Parkinson-plus syndromes, and neuromuscular
diseases would be excluded from the study. All patients had a magnetic resonance exam
to evaluate mostly the presence of orbitofrontal and/or anterior temporal atrophy[4].
Neuropsychiatric assessment
We employed the Mini Mental State Examination (MMSE)[11] for global cognitive assessment, along with the Severe Mini Mental State Examination
(SMMSE)[12] for moderately and severely impaired patients.
The Index of Independence in Activities of Daily Living (ADL)[13] was used for caregiver assessment of the following sociobiological functions: bathing,
dressing, toileting, transfer, continence and feeding, with index total scores ranging
from 0 (severe functional impairment) to 6 (preserved functionality).
The Frontal Assessment Battery (FAB)[14] was employed for screening of executive dysfunction, consisting on six subtests
that evaluate the following aspects: similarities, lexical fluency, motor series,
conflicting instructions, go/no-go and prehension behavior. The maximum score for
each subtest is 3 points, which a maximum total score of 18.
The 12-item Neuropsychiatric Inventory (NPI)[15] was employed for caregiver assessment of behavioral features, including frequency,
severity and caregiver distress for each item.
Assessment of dementia severity
Dementia stages were assessed by way of a structured interview with the caregiver
using the FTLD-modified Clinical Dementia Rating[16] (CDR) - scores were CDR=1 (mild stage), CDR=2 (moderate stage), or CDR=3 (severe
stage), based on observation of the following cognitive-behavioral aspects: memory,
orientation, judgment, problem solving, community affairs, home and hobbies, personal
care and language, language and behavior, and comportment and personality.
Assessment of swallowing and feeding situation
A face to face interview with all patients and their caregivers was conducted by a
speech therapist. To characterize feeding and swallowing, the questionnaire Assessment
of Feeding and Swallowing Difficulties in Dementia (AFSDD)[2],[17] was used, consisting on five sections. Three sections (sensory impairment and dentition;
mental state and behavior; and issues related to food, drink and swallowing) were
answered by caregivers. Two sections (feeding situation and skills; severe swallowing
problems) were answered by the speech therapist. Caregivers were asked to rate the
frequency for each symptom (0=never; 1=rarely; 2=sometimes; 3=frequently; 4=always).
In the section entitled "sensory impairment and dentition", the caregiver was asked
about vision problems, hearing loss and dentition problems. In the section entitled
“mental state and behavior”, the anticipatory phase of swallowing was investigated,
which is affected by behavioral aspects such as agitation, passivity, appetite abnormalities
and sleep disturbances. Caregivers answered questions about eating behaviors, such
as inappropriate feeding speed, passivity, agitation and distraction in feeding situations.
Aspects of the oral preparatory phase and the oral phase of swallowing, such as difficulty
with food consistency and drooling saliva or food by mouth, were investigated in the
section “issues related to food, drink and swallowing”. In the section “feeding situation
and skills”, the speech therapist observed how patients were fed along with their
caregivers. In the section “severe problems of swallowing”, the evaluator concluded
whether the patient had severe swallowing problems and whether there was any need
of additional examinations.
Assessment of swallowing functionality
Functional swallowing was graded according to the Swallowing Rating Scale of the American
Speech-Language-Hearing Association (SRS)[18] with scores from 1 to 7, with score=1 corresponding to severe dysphagia and score=7
corresponding to normal swallowing.
DATA ANALYSIS
Continuous data for each variable were first compared with the normal curve by distance
test using the Kolmogorov-Smirnov test and categorized as non-parametric. The non-parametric
data were represented by median, lower quartile (25th percentile) and upper quartile (75th percentile), while independent groups were compared by way of the Mann-Whitney test.
Spearman rank-order correlation coefficients were employed to assess correlations
between variables. The threshold of significance was set at p<0.05.
Ethical considerations
This study was approved by the Ethics Committee of Hospital das Clínicas, USP, according
to the registration number 51762. All invited patients and their legal representatives
agreed to participate on the research and signed the Informed Consent Form before
the evaluation.
RESULTS
A total of 30 patients and their 30 caregivers participated in the study.
Of 30 patients (10 men and 20 women), 14 (46%) were classified as mild stage, 8 (27%)
as moderate stage, and 8 (27%) as severe stage of dementia. The description of characteristics
of patients and caregivers may be found in [Table 1].
Table 1
Characteristics of patients and caregivers.
|
bvFTD
|
Median
|
25%
|
75%
|
|
Time since onset of symptoms (years)
|
4.5
|
3
|
7
|
|
Time since diagnosis (years)
|
2
|
2
|
4
|
|
Time of untreated disease (years)
|
1
|
1
|
3
|
|
Patient age (years-old)
|
66
|
60
|
70
|
|
Education of the patient (years)
|
5
|
4
|
9
|
|
Caregiver age (years-old)
|
56
|
42
|
64
|
|
Education of the caregiver (years)
|
10
|
4
|
14
|
|
Care time in personal daily life activities (hours per day)
|
2
|
0
|
4
|
|
Care time in instrumental daily life activities (hours per day)
|
4
|
1
|
6
|
|
Caregiver residing with the patient
|
1
|
1
|
1
|
|
Number of caregivers
|
1
|
1
|
3
|
|
Percentage of contribution in the care
|
5
|
3
|
5
|
|
MMSE
|
16
|
9
|
21
|
|
CDR
|
2
|
1
|
3
|
|
FAB similarities
|
1
|
0
|
1
|
|
FAB lexical fluency
|
1
|
0
|
3
|
|
FAB motor series
|
0
|
0
|
2
|
|
FAB conflicting instructions
|
0
|
0
|
2
|
|
FAB go/no-go
|
1
|
0
|
2
|
|
FAB prehension behavior
|
3
|
3
|
3
|
|
ADL
|
6
|
2
|
6
|
|
SRS
|
6
|
6
|
7
|
bvFTD: behavioral variant frontotemporal dementia; MMSE: Mini Mental State Examination;
CDR: FTLD-modified Clinical Dementia Rating; FAB: Frontal Assessment Battery; ADL:
Index of Independence in Activities of Daily Living; SRS: Swallowing Rating Scale
of the American Speech-Language-Hearing Association.
The median value of MMSE was 16 (9-21) and of CDR was 2 (1-3) ([Table 2]). According to [Table 2] and to [Figure 1], the most frequent behavioral features of all patients were: apathy (range of frequency:
2-4), appetite and eating disorders (range of frequency: 0-4), abnormal sleep (range
of frequency: 0-3), and agitation (range of frequency: 0-4). Regarding the SRS, we
observed score=7 (normal swallowing) in seven (23%) patients with bvFTD.
Table 2
Descriptive results for neuropsychiatric symptoms.
|
bvFTD
|
Median
|
25%
|
75%
|
|
Delusions
|
|
S
|
0
|
0
|
2
|
|
F
|
0
|
0
|
3
|
|
CD
|
0
|
0
|
3
|
|
Hallucinations
|
|
S
|
0
|
0
|
1
|
|
F
|
0
|
0
|
2
|
|
CD
|
0
|
0
|
0
|
|
Agitation
|
|
S
|
2
|
0
|
3
|
|
F
|
2
|
0
|
4
|
|
CD
|
0
|
0
|
3
|
|
Dysphoria
|
|
S
|
1
|
0
|
2
|
|
F
|
1
|
0
|
3
|
|
CD
|
0
|
0
|
2
|
|
Anxiety
|
|
S
|
0
|
0
|
3
|
|
F
|
0
|
0
|
4
|
|
CD
|
0
|
0
|
2
|
|
Euphoria
|
|
S
|
0
|
0
|
1
|
|
F
|
0
|
0
|
2
|
|
CD
|
0
|
0
|
1
|
|
Apathy
|
|
S
|
3
|
1
|
3
|
|
F
|
4
|
2
|
4
|
|
CD
|
0
|
0
|
2
|
|
Disinhibition
|
|
S
|
0
|
0
|
1
|
|
F
|
0
|
0
|
1
|
|
CD
|
0
|
0
|
0
|
|
Irritability
|
|
S
|
1
|
0
|
3
|
|
F
|
1
|
0
|
3
|
|
CD
|
0
|
0
|
2
|
|
Aberrant motor behavior
|
|
S
|
1
|
0
|
3
|
|
F
|
1
|
0
|
4
|
|
CD
|
0
|
0
|
2
|
|
Abnormal sleep
|
|
S
|
2
|
0
|
3
|
|
F
|
3
|
0
|
4
|
|
CD
|
0
|
0
|
2
|
|
Eating disorders
|
|
S
|
2
|
0
|
3
|
|
F
|
4
|
0
|
4
|
|
CS
|
0
|
0
|
2
|
bvFTD: behavioral variant frontotemporal dementia; S: severity; F: frequency; CD:
caregiver distress.
Figure 1 Graphic representation of scores for each behavioral domain of the Neuropsychiatric
Inventory (frequency times severity).DEL-delusions; HAL-hallucinations; AGI-agitation;
DYS-dysphoria; ANX-anxiety; EUP-euphoria; APA-apathy; DIS-disinhibition; IRR-irritability;
AMB-aberrant motor behavior; ABS-abnormal sleep; EAD-eating disorders; bv-FTD-behavioral
variant frontotemporal dementia; S-severity; F-frequency.
[Table 3] showed that several aspects influenced the anticipatory and oral preparatory phases
of swallowing (according to the sections of the questionnaire AFSDD) such as drowsiness,
restlessness, distractibility, passivity, improper speed during feeding, delayed triggering
of swallowing, and accumulation of food in the mouth, resulting in coughing and choking.
Swallowing and feeding problems most often observed were: passivity (range: 0-4) in
“mental state and behavior”, messy to eat (range: 0-3) in “feeding situation and skills”,
problems with certain foods (range: 0-4) and problems of food consistency (range:
0-4) in “issues related to food, drink and swallowing”. Only one patient in the severe
dementia stage had severe swallowing problems.
Table 3
Descriptive results for Assessment of Feeding and Swallowing Difficulties in Dementia
scores.
|
bvFTD
|
Median
|
25%
|
75%
|
|
Mental state and behavior
|
|
Sleepiness
|
0
|
0
|
0
|
|
Agitation
|
0
|
0
|
4
|
|
Distraction
|
2
|
0
|
4
|
|
Passivity
|
4
|
0
|
4
|
|
Refusal of food
|
0
|
0
|
2
|
|
Inappropriate speed eating- too fast
|
2
|
0
|
4
|
|
Inappropriate speed eating- too slow
|
0
|
0
|
0
|
|
Oral exploration of objects
|
0
|
0
|
1
|
|
Feeding situation and skills
|
|
Inappropriate supervision
|
0
|
0
|
2
|
|
Inappropriate position
|
0
|
0
|
0
|
|
Dependent to eat
|
0
|
0
|
2
|
|
Eat from caregiver plate
|
0
|
0
|
0
|
|
Distraction with utensils
|
0
|
0
|
3
|
|
Messy to eat
|
1
|
0
|
3
|
|
Mixing courses
|
0
|
0
|
0
|
|
Severe caregiver
|
0
|
0
|
0
|
|
Caregiver not use gentle tone of voice
|
0
|
0
|
0
|
|
Caregiver not encouraging
|
0
|
0
|
4
|
|
Stress situation
|
0
|
0
|
0
|
|
Feeder does not approach
|
0
|
0
|
2
|
|
Issues related to food, drink, and swallowing
|
|
Drooling saliva or food
|
0
|
0
|
2
|
|
Tongue weakness
|
0
|
0
|
0
|
|
Difficulty with consistencies
|
3
|
0
|
4
|
|
Delayed swallow
|
0
|
0
|
3
|
|
Coughing and choking
|
2
|
0
|
4
|
|
Wet voice quality after swallowing
|
0
|
0
|
0
|
|
Multiple swallows
|
0
|
0
|
1
|
|
Difficulty with specific food
|
4
|
0
|
4
|
|
Difficulty with correctly opening the mouth
|
0
|
0
|
3
|
|
Does not recognize temperature
|
0
|
0
|
0
|
|
Left greater portion of food in the plate
|
0
|
0
|
3
|
|
Does not recognize tastes
|
0
|
0
|
4
|
|
Left food in the mouth
|
0
|
0
|
2
|
bvFTD: behavioral variant frontotemporal dementia; AFSDD: Assessment of Feeding and
Swallowing Difficulties in Dementia.
Visual impairment was reported in 90% of patients, and dental problems were reported
in 77% of patients. Caregivers reported hyperphagia in 28% and hyperorality in 20%
of patients.
There was significant association (r>0.5) and good correlation (p<0.05) of MMSE, SMMSE,
ADL, CDR and FAB with AFSDD ([Table 4]), and significant association (r>0.5) and good correlation (p<0.01) between sum
of NPI items and the section “mental state and behavior” of AFSDD ([Table 5]).
Table 4
Correlations of Mini Mental State Examination, Severe Mini Mental State Examination,
Index of Independence in Activities of Daily Living, FTLD-modified Clinical Dementia
Rating and Frontal Assessment Battery with Assessment of Feeding and Swallowing Difficulties
in Dementia.
|
bvFTD
|
|
AFSDD-FSS*
|
AFSDD-IFS*
|
|
MMSE*
|
Correlation coefficient
|
-0.626
|
|
|
Significance (2-tailed)
|
<0.001
|
|
|
n
|
30
|
|
|
SMMSE*
|
Correlation coefficient
|
-0.689
|
|
|
Significance (2-tailed)
|
0.040
|
|
|
n
|
9
|
|
|
ADL*
|
Correlation coefficient
|
-0.768
|
-0.593
|
|
Significance (2-tailed)
|
<0.001
|
0.001
|
|
n
|
30
|
30
|
|
CDR
|
Correlation coefficient
|
0.524
|
0.402
|
|
Significance (2-tailed)
|
0.003
|
0.028
|
|
n
|
30
|
30
|
|
FAB*
|
Correlation coefficient
|
-0.642
|
|
|
Significance (2-tailed)
|
<0.001
|
|
|
n
|
30
|
|
bvFTD: behavioral variant frontotemporal dementia; AFSDD: Assessment of Feeding and
Swallowing Difficulties in Dementia; FSS: feeding situation and skills; IFS:Issues
related to food, drink, and swallowing; MMSE: Mini Mental State Examination; SMMSE:
Severe Mini Mental State Examination; CDR: FTLD-modified Clinical Dementia Rating;
FAB: Frontal Assessment Battery; ADL: Index of Independence in Activities of Daily
Living; SRS: Swallowing Rating Scale of the American Speech-Language-Hearing Association.
*Total test score.
Table 5
Correlations of neuropsychiatric symptoms of Neuropsychiatric Inventory with domains
of Assessment of Feeding and Swallowing Difficulties in Dementia.
|
bvFTD test parameters (n=30)
|
|
•AFSDD-FSS
•total score
|
•AFSDD-IFS
•total score
|
|
Euphoria (F X S)
|
Correlation coefficient
|
|
0.374
|
|
Significance (2-tailed)
|
|
0.042
|
|
Euphoria - CD
|
Correlation coefficient
|
|
0.408
|
|
Significance (2-tailed)
|
|
0.025
|
|
Aberrant motor behavior (F X S)
|
Correlation coefficient
|
0.387
|
0.444
|
|
Significance (2-tailed)
|
0.034
|
0.014
|
|
Abnormal sleep - CD
|
Correlation coefficient
|
0.374
|
|
|
Significance (2-tailed)
|
0.042
|
|
|
Eating disorders - CD
|
Correlation coefficient
|
|
0.589
|
|
Significance (2-tailed)
|
|
0.016
|
|
NPI total scores
|
Correlation coefficient
|
|
0.423
|
|
Significance (2-tailed)
|
|
0.020
|
bvFTD: behavioral variant frontotemporal dementia; AFSDD: Assessment of Feeding and
Swallowing Difficulties in Dementia; FSS: feeding situation and skills; IFS: Issues
related to food, drink, and swallowing; NPI: Neuropsychiatric Inventory; S: severity;
F: frequency; CD: caregiver distress.
DISCUSSION
In the current study, we reported the feeding situation between caregivers and patients
with bvFTD, and correlated the swallowing abnormalities with behavioral, cognitive
and functional aspects within and among different stages of this dementia syndrome.
Most of the caregivers who accepted to participate were spouses, sons or daughters
of our patients, and lived with them ([Table 1]). Even though most caregivers contributed to almost 100% of the care of our patients,
we noticed frequent caregiver difficulties when managing feeding, an aspect that may
increase the risk of choking, the time of food in the mouth, and the risk of aspiration.
We believe that this is due to cognitive and behavioral impairments, as well as the
pattern of dependence for activities of daily living.
According to caregiver reports, 90% of our patients had visual impairment. In the
feeding situation, visual impairment may affect the information about what type of
food is being offered or eaten, lead to inappropriate use of cutlery and impair hand-to-mouth
movements; thus, the amount of food may be too much for chewing at once, and result
in coughing and choking.
Apathy and lack of initiative may interfere with swallowing, considering that more
than half of all patients who presented passivity during feeding also presented chewing
problems, coughing and choking. Lack of initiative and low engagement during feeding
may affect the anticipatory phase of swallowing, while patients eating too slow when
apathetic may have increased oral transit time, thus affecting the preparatory oral
and oral phases as well, possibly resulting in choking episodes. Furthermore, disorganized
initiation or maintenance of the feeding situation were more prevalent when more cutlery
was available to patients.
Patients with bvFTD had different swallowing feature profiles in different dementia
stages. Passivity and inappropriate speed (“eating too slow”) predominated in the
severe dementia stage. Half of all patients with passivity in the feeding situation
had dysphagia (chewing problems and choking), probably because passivity influenced
the anticipatory and oral preparatory phases. Instead, inappropriate speed (“eating
too fast”) and agitation predominated in the moderate stage of bvFTD causing cough
and choking. Aspects such as passivity and eating too slow may also happen in the
mild dementia stage, though less frequently than in the severe dementia stage.
Our study is consistent with published data showing that patients with bvFTD have
feeding problems, but we found that these patients have more swallowing difficulties
than what is clinically reported in usual situations. Previous studies reported problems
such as hyperphagia, hyperorality, changes in feeding preferences and appetite, whereas
swallowing changes would be rare[8],[9],[10]. Our study reported hyperphagia, hyperorality, altered mental status during feeding,
and swallowing difficulties starting from the mild dementia stage. Our former studies[2],[3] regarding swallowing in Alzheimer’s disease and primary progressive aphasia also
showed the importance of investigating swallowing difficulties with caregivers. In
moderate and severe stages of Alzheimer’s disease[2], Correia et al. observed difficulties such as passivity, forgetting or distraction,
and eating too slow, besides difficulties when swallowing specific food and delays
in the early phases of swallowing. However, in the present study, we observed that
caregivers of patients with bvFTD were distressed when dealing with swallowing difficulties
in all dementia stages. The burden of neuropsychiatric symptoms starting from the
mild stage of bvFTD may lead to more hardness for caregivers to deal with feeding
and swallowing difficulties. Nevertheless, in patients with primary progressive aphasia[3], Marin et al. reported multiple swallows and drooling of saliva, particularly in
the semantic variant, but these features were not frequently observed in our patients
with bvFTD.
Ikeda et al.[8] investigated swallowing in 91 patients who were allocated into three groups: bvFTD
(n=23), semantic variant primary progressive aphasia (n=25) and Alzheimer's disease
(n=43). The mean age of these groups was, respectively: 61, 65 and 68 years. Six participants
with bvFTD were institutionalized. A questionnaire comprising 36 questions to be answered
by caregivers was used to assess swallowing problems. The questionnaire presented
five domains: swallowing problems, change in appetite, food preference, eating habits,
and other oral behaviors. The authors found rare swallowing problems in the bvFTD
group, and suggested that dysphagia in bvFTD tends to develop in later dementia stages.
Our results were different from those, and one possible reason for this discrepancy
is that we employed a more detailed evaluation that included the observation of feeding
behaviors, suggesting the need for a thorough assessment of swallowing in patients
with bvFTD.
In the literature, the main behavioral aspects reported in bvFTD are: apathy, anxiety,
psychomotor agitation and feeding disorders[19],[20],[21]. In our study, the most evident ones were apathy, feeding disorders and sleep disorders.
The fact that most of our patients were in the mild dementia stage might have affected
such results
The correlations observed between the section “feeding situation and abilities” of
AFSDD and the instruments MMSE, SMMSE, ADL, CDR and FAB (p<0.05) showed that cognitive
aspects, functional abilities, severity of disease and executive dysfunction can influence
the feeding situation. These aspects led to the conclusion that swallowing difficulties
tend to follow cognitive and behavioral decline in patients with bvFTD.
Limitations of this study include its cross-sectional nature with a relatively small
sample and no randomization. In future studies, the use of a thorough battery of neuropsychological
tests for memory and visuospatial skills along with objective exams for assessment
of swallowing (such as fluoroscopy with barium) could provide more information to
objectively assess these features of patients with bvFTD. Nevertheless, it should
be noted that patients with dementia might not collaborate with exams such as videofluoroscopy
and videoendoscopy, which is why we suggest that proper indication should be individualized
so as not to mask the actual patterns of swallowing of each patient. In spite of these
caveats, clinical assessment of dysphagia was well documented, and added important
information to the relatively scarce literature on the subject, particularly by considering
the feeding situation between caregivers and patients with bvFTD.
In summary, swallowing and feeding problems were present in different stages of bvFTD,
with different characteristics in each stage. This study should alert healthcare professionals
not only about the prevalence of swallowing difficulties starting in the mild stage
of bvFTD but also on the need for orientation programs for caregivers, so that therapy
can be established for improvement and to prevent complications.
