Eating Difficulties and Relationship With Nutritional Status Among Patients With Dementia

ABSTRACT Background One of the most common behavioral problems in patients with dementia is eating problems, which are known to increase the risk of malnutrition. However, few studies have been conducted in this patient group regarding the relationship between eating difficulties and nutritional status. Purpose This study was designed to determine the eating difficulties faced by patients with dementia and to evaluate the relationship in this population between eating difficulties and malnutrition. Methods This study was carried out in a dementia outpatient clinic of a university hospital in Istanbul, Turkey. This cross-sectional, case-control study included 50 patients and 50 healthy controls as participants. Participants were assessed for eating difficulties and for nutritional, cognitive, and functional statuses. Results The patients with dementia had more difficulties in terms of self-feeding skills. Although problems related to manipulating food on the plate and the use of utensils were not seen in the control group, these problems were found in 30% of the participants in the dementia group (p < .001). Moreover, 30% of the patients in the dementia group were unable to eat without assistance (p < .001). Associations were found between eating difficulties and age, duration of illness, and cognitive and functional (basic and instrumental activities of daily living) statuses. In addition, self-feeding skills were found to be associated with nutritional status. Rate of malnutrition or risk of malnutrition was higher in patients with dementia than in those in the control group. Conclusions In this study, compared with the control group, patients with dementia had more problems in self-feeding skills such as manipulation of food on a plate, use of utensils, need for assistive tools, ability to eat without assistance, and negative eating behaviors (refusal to eat). An association was found between eating difficulties and nutritional status. Evaluating eating difficulties is recommended in patients with dementia to prevent nutritional deterioration.


Introduction
Dementia is a progressive clinical syndrome characterized by the impairment of multiple cognitive functions such as shortand long-term memory loss, thinking, judging, orientation, calculation, and learning ability as well as personality changes, impaired abilities, and motor skills. Patients with dementia experience emotional, social, and behavioral problems as well as cognitive problems. Dementia also negatively affects the activities of daily living (World Health Organization, 2018).
Over 55 million people live with dementia worldwide, and this number is expected to reach 78 million by 2030 (Gauthier et al., 2021). The prevalence of dementia in Turkey has been reported as comparable with that seen in developed countries (Gurvit et al., 2008). In parallel with the world, this number is expected to increase with the aging of the population in Turkey (The World Bank, 2019).
Dementia is a condition that causes many problems for both patients and their relatives/loved ones and caregivers. These patients may experience behavioral problems such as apathy, aberrant motor behavior, sleep deprivation, agitation, and delusions (Küçükgüçlü et al., 2017;Liu et al., 2017). Eating problems are one of the most common behavioral problems in patients with dementia. Factors such as impaired cognitive and motor skills, depression, environmental factors, social interactions, food culture, visual impairment, dental problems, and poor oral hygiene may cause eating difficulties in these patients (Cipriani et al., 2016;K. M. Lee & Song, 2015;Liu et al., 2020). Moreover, eating problems may increase the risk of malnutrition (Chang & Roberts, 2011). It is known that malnutrition adversely affects physical health, reduces quality of life, and increases morbidity and mortality (Saucedo Figueredo et al., 2016). However, few studies exploring the relationship between eating difficulties and nutritional status have been conducted on patients with dementia. Therefore, the aim of this study was to determine eating difficulties experienced by these patients and to evaluate the relationship between eating difficulties and nutritional status.

Design and Sample
An observational, cross-sectional case-control study was conducted in a dementia outpatient clinic of a university hospital in Istanbul between February 2015 and August 2016. Patients with a confirmed diagnosis of dementia were included if they were still living at home and if they were able to stand independently on a scale to be weighed. Patients were excluded if they had any serious illnesses (e.g., cancer, stroke with sequelae, decompensated heart failure). The control group consisted of individuals not affected by dementia and without significant health problems (e.g., cancer, diabetes, myocardial infarction, stroke, heart failure). Most of the control group participants were the relatives of the patients from another clinic (internal medicine), whereas several were personal acquaintances of the authors. The sample size was calculated (α = 5% and power = 80%, Cohen effect size = 0.3) with a minimum of 44 in each group for a total of 88. Fifty participants were recruited for each group to account for possible attrition. Fifty patients who were approached declined to participate because their relatives did not agree (n = 25) or they could not stand on the scale (n = 25). The evaluations were completed with 50 patients. Fifty individuals with a similar mean age, gender ratio, and educational level as the patient group constituted the control group. The compliance of the study with ethical principles was evaluated and approved by the Clinical Research Ethics Committee of Istanbul Faculty of Medicine (15.01.2015/81). In addition, written informed consent was obtained from all of the participants or their relatives.

Data Collection
Patients and their relatives were approached while they were waiting for their appointment. All assessments (except for Mini Mental State Examination [MMSE]) were made by the first author with the individuals who met the inclusion criteria using a face-to-face interview method. Eating difficulties were evaluated using a questionnaire derived from the Minimal Eating Observation Form (MEOF), and nutritional status was evaluated using the Mini Nutritional Assessment (MNA). A patient information form, MMSE, Barthel Index of Activities of Daily Living (BI), Functional Activities Questionnaire (FAQ), and Charlson Comorbidity Index were also used to collect data. The MMSE was performed by the neurologist who examined the patient, and these data were obtained from the patient file at the end of the day.
Eating difficulties questionnaire Eating difficulties were evaluated using a questionnaire based on questions from the MEOF (Westergren, 2019). The questionnaire consisted of problems related to eating activity (i.e., problems in swallowing, chewing, teeth, manipulating food on a plate, and using utensils; the need for assistive tools, inability to eat without help, loss of food awareness in mouth, and refusal of food). This form has a three-factor structure: deglutition, ingestion, and energy/appetite. The Cronbach's alpha value has been reported as .76, and interobserver agreement has been reported to be good (kappa value = .70; Westergren, 2019;Westergren et al., 2009).

Mini nutritional assessment
The MNA is an assessment developed to assess nutritional status that addresses nutritional habits/problems, some anthropometric measurements, and a physical assessment. This assessment is recommended by the European Society for Clinical Nutrition and Metabolism for use with older adults. In terms of scoring, a score of 24-30 indicates normal nutritional status, 17-23.5 indicates risk of malnutrition, and less than 17 indicates malnutrition (Rubenstein et al., 2001;Sarikaya et al., 2015).

Mini mental state examination
The MMSE was developed to evaluate five basic cognitive functions (orientation, memory, attention, calculation, and language). The maximum score that can be obtained from this test is 30, with lower scores indicating impairment in mental functions (Folstein et al., 1975;Gungen et al., 2002). The Turkish version of the MMSE has been validated in the Turkish cultural context and has been shown to have high discriminant validity and interrater reliability in the diagnosis of dementia. A cutoff score of 23-24 was found to have the highest sensitivity (0.91) and specificity (0.95). Interrater reliability analysis has shown high correlation (r = .99) and kappa value (.92; Gungen et al., 2002). A recent study confirmed these psychometric findings and also reported good internal consistency (Cronbach's α of .86; Çebi et al., 2020). The MMSE was assessed by the neurologist who examined the patient, and these data were obtained from the patient file at the end of the day.

Barthel index of activities of daily living
This index, developed to assess dependence in activities of daily living, is widely recommended as a measure for activities of daily living in older populations. Scoring ranges from 0 to 100, with 0 indicating complete dependence and 100 indicating complete independence. The cutoff value for independence is 60, with scores greater than 60 indicating the ability to function independently (Hopman-Rock et al., 2019). This index was validated in Turkish by Küçükdeveci et al. (2000). Internal consistency was good at .93 for stroke and .88 for spinal cord injury. The level of agreement between the two raters was sufficient with kappa levels greater than .5. The intraclass correlation coefficients were .99 and .77 for stroke and spinal cord injury, respectively. This index is widely used to survey older adult populations.

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Functional activities questionnaire
The FAQ is a short questionnaire used to assess the performance of complex daily living activities. This questionnaire is usually conducted on the family caregivers of patients, with higher scores indicating greater dependence with regard to instrumental daily living activities (Pfeffer et al., 1982;Selekler et al., 2004). This scale was developed by Pfeffer et al., and a norm determination study on a Turkish sample in which participants were all 50 years or older was conducted by Selekler et al. (2004). In that study, the average and standard deviations of the participant scores obtained from the FAQ were determined based on age, gender, and educational level.

Statistical Analysis
Frequency and mean were used to describe the characteristics of the participants. The Kolmogorov-Smirnov test was used to evaluate the suitability of the data for normal distribution. Mann-Whitney U and chi-square tests (and the Fisher's exact test) were used to compare patient and control groups. Chi-square was used to evaluate the relationship between eating problems and nutritional status in the dementia group. Eating difficulties were evaluated using an independent samples t test for age, duration of illness, Barthel Index, and FAQ and using the Mann-Whitney U test for the Charlson Comorbidity Index, Clinical Dementia Rating, and MMSE. All of the analyses were conducted using IBM SPSS Statistics Version 21.0 (IBM Inc., Armonk, NY, USA).

Results
One hundred participants were enrolled in this study, including 50 patients and 50 patients in the control group. The sociodemographic characteristics of the participants in the patient and control groups (Table 1) show that the groups were similar in terms of sociodemographic characteristics such as age, gender, education, and income (p > .05).
All of the patients in this study were fed orally. The eating difficulties of the groups are described in Table 3. Although no between-group differences were found in terms of swallowing problems, chewing problems, tooth loss, or food awareness in the mouth, patients with dementia reported greater difficulties in terms of self-feeding skills. Whereas problems related to manipulating food on the plate and utensil use were not seen in the control group, these problems were found in 30% of the dementia group (p < .001). Thirty percent of the patient group could not eat without assistance, whereas no one in the control group required assistance to eat (p < .001). In addition, whereas 56% of the patients reported refusal to eat, this ratio was 2% in the control group (p < .001; Table 3).
Next, eating difficulties in the patient group were evaluated to identify possible relationships with sociodemographic and clinical characteristics. Patients with tooth loss tended to be older and to have longer disease durations (p < .05). Compared with the group with no problem in self-feeding, the poor self-feeding skills group tended to be older, have a longer disease duration, and have poorer MMSE scores, although none of these relationships reached statistical significance. Moreover, patients with poor functional states (BI and FAQ) had problems with all of their eating skills and exhibited a high rate of refusal to eat (Table 4). When the relationships among the scores of the scales used in this study were analyzed, a significantly strong correlation was found between BI and FAQ (r = −.76, p < .001) and moderate correlations between MMSE and BI (r = .51, p < .001) and FAQ (r = −.61, p < .001).
In terms of the relationship in the dementia group between eating difficulties and nutritional status (Table 5), no relationship was found between nutritional status and swallowing or chewing problems, tooth loss, or food awareness in the mouth. However, other eating difficulties (e.g., self-feeding skills) were more commonly found in those with malnutrition or risk of malnutrition. Compared with the nutritionally normal group, patients with malnutrition or risk of malnutrition were found to be worse in terms of their ability to manipulate food on a plate (p = .007), ability to use utensils (p = .007), need for an assistive tool (p = .028), and ability to eat without help (p = .007).

Discussion
In this comparison study of patients with dementia against normal controls, patients with dementia were found to have more problems related to self-feeding skills (e.g., manipulating food on a plate, using utensils, need for assistive tools, ability to eat without help) and eating behaviors (refusal to eat) than the control group. In the related literature, eating difficulties have been reported in around 45% of patients with dementia (Chang et al., 2017). The various methods used in the literature to evaluate eating problems make it difficult to accurately determine the prevalence of these problems. Because of the lack of an eating difficulties questionnaire in the Turkish language, questions from the MEOF were used in this study. Moreover, because of the lack of validity, we did not use the questions as a scale but rather conducted an analysis based on the individual items. Therefore, a prevalence rate for eating difficulties could not be generated in our sample. Rather, we assigned proportions to each difficulty, which makes comparing our results with previous studies difficult. However, we found the frequency of self-feeding problems to be higher (0% vs. 30%) in patients with dementia than in their demographically matched controls. Although the term "eating difficulties" includes problems related to various aspects of eating and drinking, studies have shown that the most common eating difficulty among patients with dementia refers to self-feeding problems, specifically the inability to use utensils (Chang, 2012;Chang et al., 2017;K. M. Lee & Song, 2015). In patients with dementia, impairment in cognitive functions negatively affects eating skills either directly because of buccopharyngeal apraxia (Chandra et al., 2015) or indirectly through the impact on physical functioning. Because of the direct impact of cognitive dysfunction, patients may experience problems related to eating initiation, maintaining attention during the meal,

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In this study, to identify factors associated with eating difficulties that may subsequently be used to identify patients with dementia at a high risk of eating difficulties, eating difficulties were evaluated according to sociodemographic and clinical characteristics. The patients with tooth loss tended to be older. Although the difference between the groups did not reach statistical significance, the patients with problems in self-feeding skills tended to be older and to have a longer disease duration than their peers without these problems (Chang, 2012;Liu et al., 2017). As age and disease duration are generally related parameters, their relations with eating difficulties are parallel. This finding confirms the findings in the literature regarding an association between eating skills and disease duration (Chang, 2012). Eating Difficulties Among Patients With Dementia VOL. 31, NO. 1, FEBRUARY 2023 No difference was found in this study in terms of comorbidities in patients with and without eating difficulties. Liu et al. (2017) reported that having a comorbidity causes eating difficulties in patients with dementia. Slaughter et al. (2011) found a mean Charlson Comorbidity Index score of 5.5 in their patients with dementia and stated that it affected eating abilities independently of all other factors. In both studies, the comorbidity scores of patients with dementia were higher than in this study, possibly because of the higher mean age in those previous studies (86.0 years vs. 71.8 years in this study). Because comorbidity increases with age, the finding in this study showing no association between eating difficulties and comorbidity status may be attributable to lower mean age.
When the patients with dementia in this study were compared with the controls in terms of cognitive and functional states (basic and instrumental activities of daily life), their functions were worse than expected (G. Lee, 2020;Rullier et al., 2013;Tombini et al., 2016).
When the associations of cognitive and functional states with eating difficulties were investigated in the dementia group, both functions revealed a difference between patients with and without difficulties. In this study, the correlations between cognitive function, physical function, and eating difficulties were significant, which echoes the findings of previous studies (Chang, 2012;K. M. Lee & Song, 2015;Lin et al., 2008). Dementia is a disease in which general function is impaired as cognitive function is impaired, whereas eating requires physical functioning such as the manipulation of food, the use of utensils, and the moving of food into the mouth as well as cognitive functions to coordinate these movements. The deterioration of cognitive functions affects the functional status of the patients negatively (as shown by the moderate correlations between these parameters) and increases their dependence levels. This deterioration further complicates food intake (Chang et al., 2017;K. M. Lee & Song, 2015;Mann et al., 2019). In this study, similar associations were found between functional state and eating difficulties. Patients with poor BI and FAQ scores had problems in both self-feeding skills and eating behaviors, with patients with low scores on the function scales more dependent during eating and facing greater difficulties in food intake (Chang, 2012;Chang et al., 2017). Maintaining independence in activities of daily living, especially in eating, ensures adequate food intake. The finding in this study showing a stronger relationship between eating difficulties and functional scales than cognitive functioning may be because of the fact that the eating difficulty assessment tool used mainly focuses on the physical components of eating. Nutritional status was another association of eating difficulties investigated in this study. Although no relationship was identified between nutritional status and swallowing or chewing problems, poor self-feeding skills (i.e., ability to manipulate food on a plate, ability to use utensils, need for assistive tools, and ability to eat without help) were more common in patients with malnutrition or at risk of malnutrition. It has been reported that eating-skill-related problems decrease energy and protein intake and increase the risk of malnutrition in patients with dementia (Keller et al., 2017;Miyamoto et al., 2011;Roque et al., 2013). Some limitations should be taken into consideration when interpreting the results of this study. First, eating difficulties could not be evaluated using a standard questionnaire, as no validated instrument in the Turkish language was available. Thus, our use of individual items from a questionnaire limited the validity of our statistical analysis. Second, although we aimed to include only individuals with no health problems in the control group, this could not be achieved completely because of the difficulty of finding healthy older adult individuals. Although having neurological or psychiatric diseases and having serious health problems such as cancer, myocardial infarction, decompensated heart failure, and complicated diabetes were applied as exclusion criteria, otherwise healthy control candidates with Stage 1 hypertension regulated with a single drug or controlled diabetes were included in the control group. Third, because the assessments made in this study were informant based, scoring may have been affected by subjective recollection and memory biases. Observation of patients by research assistants may help overcome this limitation in future studies.

Conclusions
In this study, the patients with dementia exhibited significantly more eating difficulties than their control group peers. Although the patients were similar with their control peers in terms of swallowing, chewing, and teeth problems, they had more problems in the realm of self-feeding skills such as manipulating food on a plate, using utensils, needing assistive tools, and being able to eat without help as well as in the realm of eating behaviors (i.e., refusal to eat). Moreover, basic and instrumental activities of daily living were found to be associated with eating difficulties. In addition, the rate of malnutrition and risk of malnutrition were both higher in the patients with dementia than in the controls. Finally, an association was found between eating difficulties and nutritional status. Eating difficulties should be regularly evaluated in patients with dementia to prevent nutritional deterioration.

Author Contributions
Study conception and design: ZT, OC Data collection: OC Data analysis and interpretation: ZT, HH, BB Drafting of the article: ZT, OC, HH Critical revision of the article: IHG