Abstract
BACKGROUND:
Few studies have described characteristics of swallowing in primary progressive aphasia (PPA) and its variants.
OBJECTIVE:
To describe and characterize swallowing and eating behaviors of patients with PPA, as well as their correlates with neuropsychiatric symptoms and patterns of communication.
METHODS:
We studied 16 patients with PPA and 16 their caregivers. PPA was subdivided in agrammatic variant (PPA-G), semantic variant (PPA-S) and logopenic variant (PPA-L). All patients and their caregivers were screened with the following scales: “Assessment of Feeding and Swallowing Difficulties in Dementia”, “Neuropsychiatric Inventory”, and “Functional Outcome Questionnaire for Aphasia”.
RESULTS:
Patients with PPA-S had diverse swallowing problems such as drooling of saliva or food, multiple swallows, delayed swallow and choking, all of which correlated with anxiety, apathy and aberrant motor behavior. Patients with PPA-G and PPA-L had choking and delayed swallow, respectively. Disturbances in eating behaviors were more frequent in the group with PPA-L, and they correlated with difficulties in patterns of communication.
CONCLUSIONS:
All variants showed swallowing difficulties and they were more frequent in PPA-S. Further studies with larger samples of patients are needed to better characterize swallowing problems and their consequences in the different variants of PPA.
Keywords
Introduction
Primary progressive aphasia (PPA) is a clinical syndrome characterized by a prominent and isolated language deficit, without salient impairments in cognitive domains, at least in the early stages of the disease (Gorno-Tempini, Hillis, Weintraub, Kertesz, Mendez, Cappa, Ogar, Rohrer, Black, Boeve, Manes, Dronkers, Vandenberghe, Rascovsky, Patterson, Miller, Knopman, Hodges, Mesulam, & Grossman, 2011). In PPA usually occurs progressive difficulties in word finding, word usage, word comprehension and sentence construction, interfering with independence for activities of daily living (Mesulam, 2013). It can be divided in three variants: agrammatic primary progressive aphasia (PPA-G), semantic progressive aphasia (PPA-S) and logopenic primary progressive aphasia (PPA-L). In PPA-G, syntactic impairments and motor speech deficits are common. Patients with PPA-S usually have loss of semantic knowledge and loss of ability to understand words and sentences, whereas in PPA-L, they have phonological deficits with normal semantic processing.
There are few reports on swallowing and feedingbehaviors in the different variants of PPA (Fuh, Liao, Wang, & Lin, 1994; Ikeda, Brown, Holland,Fukuhara, & Hodges, 2002; Langmore, Olney, Lomen-Hoerth, & Miller, 2007). Herein, our objective is to characterize swallowing and eating behaviors in the three variants of PPA, and to correlate these findings with neuropsychiatric aspects and communication.
Methods
Patients
Sixteen patients with diagnosis of PPA and their 16 caregivers were evaluated at the Behavioral Neurology Section of the Federal University of Sao Paulo, and in the Neurology Service of the Hospital das Clinicas at the University of Sao Paulo. Patients were evaluated for cognitive abilities, functionality, language, behavior, and swallowing and eating behaviors.
The Mini-mental State Examination (MMSE) (Bertolucci, Brucki, Campacci, & Juliano, 1994) was used for cognitive impairment screening. Disease severity was measured by the Clinical Dementia Rating scale (CDR) (Chaves, Camozzato, Godinho, Kochhann, Schuh, Almeida, & Kaye, 2007) Patients were classified as CDR = 1 (mild stage), CDR = 2 (moderate stage), or CDR = 3 (severe stage).
All subjects underwent a magnetic resonance of the brain which was compatible with PPA. The diagnosis of each variant was confirmed by: fluency test (phonologic and semantic); repetition of single words, sentences and phrases; confrontation naming; object knowledge; reading words, sentences and phrases; syntax comprehension; semantic knowledge; and analyses of conversational discourse (spontaneous speech) with analyses of fluency, grammar, motor speech and sound errors. We used the clinical criteria based on Gorno-Tempini, Hillis, Weintraub, Kertesz, Mendez, Cappa, Ogar, Rohrer, Black, Boeve, Manes, Dronkers, Vandenberghe, Rascovsky, Patterson, Miller, Knopman, Hodges, Mesulam & Grossman, 2011 and Mesulam, 2013 for conformation for each of the PPA variants.
Procedures
Swallowing and eating behaviors were evaluated by the “Assessment of Feeding and Swallowing Difficulties in Dementia” (AFSDD) (Correia, Morillo, Filho, & Mansur, 2010; Kindell, 2002) which has five sections. Three sections (sensory impairment and dentition; mental state and behavior; and issues related to food, drinking and swallowing) were answered by caregivers. Two sections (feeding situation and skills; severe swallowing problems) were answered by a speech-language pathologist. Caregivers were asked to rate the frequency for each symptom. In the section “sensory impairment and dentition”, the caregiver was asked about vision problems, hearing loss and dentition problems. In the section “mental state and behavior”, the anticipatory phase of swallowing influenced by behavioral aspects was investigated. Caregivers answered questions about eating behaviors, such as inappropriate feeding speed, passivity, agitation and distraction in feeding situations. Aspects of the oral preparatory 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, drinking and swallowing”. In the section “feeding situation and skills”, the speech-language pathologist 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.
We used the Neuropsychiatric Inventory (NPI) (Camozzatto, Kochhann, Simeoni, Konrath, Franz, Carvalho, & Chaves, 2008) to assess frequency and severity of neuropsychiatric symptoms. It consists on the following 12 items: delusions, hallucinations, agitation, dysphoria, anxiety, apathy, irritability, euphoria, disinhibition, aberrant motor behavior, sleep disorders and eating disorders and appetite. Caregivers were asked to rate frequency, severity and caregiver distress for each scored item regarding behavioral symptoms of patients.
The Functional Outcome Questionnaire for Aphasia (FOQ-A) (Ketterson, Glueckauf, Blonder, Gustafson, Donovan, Rodriquez, Pekich, Ley, & Gonzalez-Rothi, 2008) was answered by caregivers to evaluate functional communication. Caregivers were asked to rate the frequency for each characteristic of communication. This questionnaire consists of 32 items that evaluate communication of basic needs (7 questions), making routine requests (7 questions), communication of new information (8 questions), and attention/other communication skills (10 questions).
A speech pathologist evaluated patients and their caregivers in a face-to-face interview in a single evaluation session.
This study was approved by the local Research Ethics Committee (registration number: 51.762).
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 the Mann-Whitney test.
Spearman correlation coefficient were employed to assess correlations between variables. The threshold of significance was set at p < 0.05.
Results
Of 16 patients with PPA, 5 (31%) were in the mild stage, 5 (31%) in the moderate stage, and 6 (38%) in the severe stage. Seven patients (44%) presented PPA-G, 4 (31%) PPA-S and 4 (25%) PPA-L. The description of characteristics of patients and caregivers are in Table 1.
Sections of AFSDD were described and compared among subgroups of PPA (Table 2).
All patients with PPA-S had dental problems, as well as most patients with PPA-G (86%). All patients with PPA-L had some visual impairment. The section “mental state and behavior” had the highest scores for PPA-L and PPA-S. The most frequent problems in this section were passivity in PPA-S with the median value of 4 (2–4) and the inappropriate speed eating – too slow in PPA-L with the median value of 2 (0–4).
The item “caregiver not encouraging” of section “feeding situation and skills” showed higher median value for PPA-L with the value of 3 (2–4). The frequent problems in the section “issues related to food, drinking, and swallowing” were regarding “difficulty with food consistency” with the median value of 2 (0–4), and “delay in swallowing” with the median value of 2 (0–4) in PPA-L. Complaints of “drooling saliva or food” and “cough and choking” were reported only in PPA-S.
Hyperphagia was reported in 31% of patients, and hyperorality was reported in 20% of patients.
There were no statistically significant differences in the comparisons among subgroups of PPA in NPI (Table 3).
FOQ-A results were described and compared among subgroups of PPA (Table 4), and no statistically significant differences was observed.
The sections of AFSDD showed correlations with the domains of FOQ-A (r > 0.5) (Table 5). The section “mental state and behavior” of AFSDD had correlations with domains “euphoria” and “aberrant motor behavior” of the NPI (r > 0.5) (Table 5).
Discussion
Our study is the first to characterize the swallowing problems and eating behaviors in the three variants of PPA, and to correlate them with neuropsychiatric aspects and communication.
The application of specific questionnaires to assess aspects of swallowing showed different profiles in the 3 subgroups of the PPA.
Unlike other studies (Ikeda, Brown, Holland, Fukuhara, & Hodges, 2002; Langmore, Olney, Lomen-Hoerth, & Miller, 2007), we observed various swallowing problems in patients with PPA-S. The problem “drooling mouth saliva or food”, for example, was observed only in patients with PPA-S in our study. We believe that this swallowing problem is influenced by the presence of apathy, a common behavioral symptom most often present in our PPA-S patients (Snowden, Bathgate, Varma, Blackshaw, Gibbons, & Neary, 2001). Apathy can interfere in the feeding situation because it is a behavioral symptom of voluntary action caused by dysfunctions that occur at the level of preparation, execution and control of behavior (Brown & Pluck, 2000). Thus, apathy may contribute to the slowness of the anticipatory phase and oral preparation, which may facilitate the drooling of food from themouth.
Difficulty in the correct mouth opening was observed only in patients with PPA-G. This finding may be related to the oral apraxia which is specifically observed in this variant of PPA. Oral apraxia reflects an impaired performance of voluntary actions such as opening the mouth to feed, preparation of food in the oral cavity and chewing (Daniels, 2000). Swallowing problems were reported by caregivers in the mild and severe stages of PPA-G.
PPA-L was the variant with more frequent problems in eating behaviors, and these problems were present from the mild stage of the disease. Among them were more frequent the passivity and refusal of food. Most of these patients also had inappropriate speed eating- too slow, which may have contributed to the swallowing problems such as delayed swallow and difficulty with food consistency. Previously, there are no references in the literature about feeding behavior and swallowing problems in PPA-L.
The section “mental state and behavior” of AFSDD was the most representative for the PPA-L and PPA-S variants. This finding is expected because PPA-L was the variant with more behavioral problems in the feeding situation, and PPA-S was the variant with more neuropsychiatric problems that impacted swallowing.
Correlations were observed between the section “sensory impairment and dentition” of AFSDD in the domain “communication of basic needs” of FOQ-A. The section “sensory impairment and dentition” has questions about sensory aspects such as hearing and vision, as well as motor aspects related to the presence of teeth. The auditory and visual changes interfere with reception of expressive language, which results in impaired communication. Similarly, problems of teeth may also affect speech and consequently the communication. The behavioral symptom “aberrant motor behavior” had correlations with the section “mental state and behavior”. The individual with “aberrant motor behavior” has changes in posture and disorganization for oral ingestion that can interfere in the anticipatory phase of swallowing. “Eating disorders” reported by caregivers in the NPI had correlations with the section “issues related to food drink and swallowing”, drawing our attention to the associations of feeding difficulties with swallowing disorders.
Reports of hyperorality and hyperphagia in the PPA are rare (Ikeda, Brown, Holland, Fukuhara, & Hodges, 2002; Langmore, Olney, Lomen-Hoerth, & Miller, 2007). There is survey that showed tendency to eat non-edible things in PPA-S and other study that reported patients with PPA- S with more compulsive eating behaviors than patients with PPA- G (Ikeda, Brown, Holland, Fukuhara, & Hodges, 2002; Langmore, Olney, Lomen-Hoerth, & Miller, 2007). Hyperorality was present in PPA-S and PPA-L in our study, and was reported in patients with 5 years or more of disease duration. Hyperphagia was present in all variants of PPA, and was reported in patients with 3 or more years of illness duration.
In our study, only one patient with PPA had no sensory impairment and dentition, and this patient had PPA-G in the mild dementia stage. Fourteen patients had dental problems. Of the 14 patients, 4 had chewing problems. Three patients with chewing problems were using dentures or dental implants, which may suggest that the chewing problem could be associated with to oral apraxia. Five patients with PPA-G variant in moderate stage had hearing impairment, according caregivers. Our data further demonstrate that all these patients had a problem in feeding situation and most of them had swallowing problems. There are no studies correlating the hearing impairment with swallowing and feeding in PPA, but there is a recent study that demonstrated the effects of delayed auditory feedback in speech of individuals with PPA-G (Maruta, Makhmood, Downey, Golden, Fletcher, Witoonpanich, Rohrer, & Warren, 2014). Caregivers also reported visual disturbances such as astigmatism, myopia and hyperopia; such visual disturbances started prior to the onset of symptoms of PPA in their patients.
A shortcoming of our study was the small sample of patients with PPA, which may limit the accuracy of analysis of swallowing problems in each variant of the disease.
In conclusion, swallowing problems were present in all variants of PPA. Further studies with larger samples of patients are needed to better characterize swallowing problems and their consequences in the different variants of PPA.
Conflict of interest
The authors report no conflicts of interest related to this work.