doi:10.1111/pcn.12375 Regular Article Classifying eating-related problems among institutionalized people with dementia Shunichiro Shinagawa, MD, PhD, 1 * Kazuki Honda, MD, PhD, 2 Tetsuo Kashibayashi, MD, PhD, 3 Kazue Shigenobu, MD, PhD, 4 Kazuhiko Nakayama, MD, PhD 1 and Manabu Ikeda, MD, PhD 2 1 Department of Psychiatry, Jikei University School of Medicine, Tokyo, 2 Department of Neuropsychiatry, Graduate School of Medical Science, Kumamoto University, Kumamoto, 3 Department of Rehabilitation, Rehabilitation Nishi-Harima Hospital, Hyogo, and 4 Asakayama General Hospital, Osaka, Japan Aims: Various eating-related problems are commonly observed among people with dementia, and these problems place a huge burden on the caregivers. An appropriate classification of these problems is important in order to understand their underlying mechanisms and to develop a therapeutic approach for managing them. The aim of this study was to develop a possible classification of eating-related problems and to reveal the background factors affecting each of these problems across various conditions causing dementia. Methods: The participants were 208 institutionalized patients with a diagnosis of dementia. Care staff were asked to report all kinds of eating-related problems that they observed. After the nurses responses were analyzed, 24 items relating to eating-related problems were extracted. A factor analysis of these 24 items was conducted, followed by a logistic regression analysis to investigate the independent variables that most affected each of the eating-related factors. Results: Four factors were obtained. Factor 1 was overeating, factor 2 was swallowing problems, factor 3 was decrease in appetite, and factor 4 was obsession with food. Each factor was associated with different background variables, including Mini-Mental State Examination scores, Clinical Dementia Ratings, and neuropsychiatric symptoms. Conclusions: This study suggests that eating-related problems are common across conditions causing dementia and should be separately considered in order to understand their underlying mechanisms. Key words: appetite, dementia, obsession with food, overeating, swallowing. *Correspondence: Shunichiro Shinagawa, MD, PhD, Department of Psychiatry, Jikei University School of Medicine, 3-25-8 Nishi-shimbashi, Minato-ku, Tokyo 105-8461, Japan. Email: shinagawa@jikei.ac.jp Received 4 August 2015; revised 29 September 2015; accepted 7 November 2015. IT IS WELL known that individuals with dementia experience various eating-related problems in association with cognitive dysfunction, psychiatric problems, and a decline in daily activity. 1,2 As these eating problems have to be managed on a daily basis, they become a huge burden on the patients caregivers, which could lead to a diminished quality of life for the patient. 3 These eating problems sometimes disrupt home caring, become a trigger for institutionalization, and can even become a major issue within a nursing care facility. However, until recently, research assessing eating problems in dementia has mainly focused on dietary consequences, nutritional deficiency, and weight loss. 4,5 There are relatively few systematic studies on other eating-related problems, such as overfilling the mouth, deteriorating table manners, and eating non-edible foodstuffs. 6,7 There are several studies on the abnormal eating behaviors of patients with frontotemporal dementia (FTD) as these eating behaviors are common and predominant features among such patients; 8 10 however, only a few studies have been conducted on the eatingrelated problems of patients with Alzheimer s disease (AD) 6,7 and other types of dementia, such as dementia with Lewy bodies (DLB). 11 There is still a lack of 175 1
2176S. S. Shinagawa et et al. al. Psychiatry and Psychiatry Clinical Neurosciences and Clinical 2016; Neurosciences 70: 175 181 2015 clarity regarding the kinds of eating-related problems that are common across individuals with various conditions causing dementia, and the underlying mechanisms of these problems. In addition, there have been no studies wherein the researchers have adopted an empirical approach to separate the eating-related problems of patients with dementia into symptom groups. The appropriate classification of these eatingrelated problems is important for understanding their underlying mechanisms and for developing a therapeutic approach to managing them. The aims of this study were: (i) to reveal the types and frequencies of eating-related problems that are common across patients with various conditions causing dementia; (ii) to develop a possible classification of eatingrelated problems; and (iii) to reveal the relation between eating-related problems and the background factors they are associated with. METHODS Participants All of the patients were recruited from among the inpatients of two psychiatric hospitals, one rehabilitation hospital, and two nursing homes. Patients with a diagnosis of dementia according to DSM- IV-TR criteria during the research period (i.e. October 2011 to March 2012) were included in this research. 12 A total of 208 people with dementia were included in the study, and were classified into diagnostic groups according to the established international consensus clinical criteria. The diagnosis of AD was based on the probable AD criteria of the National Institute of Neurological and Communicative Disorders and Stroke, and the Alzheimer s Disease and Related Disorders Association. 13 The diagnosis of vascular dementia (VaD) was based on the probable VaD criteria of the National Institute of Neurological Disorders and Stroke and the Association Internationale pour la Recherche et l Enseignement en Neurosciences or the Alzheimer s Disease Diagnostic and Treatment Centers. 14,15 The diagnosis of DLB was based on recent clinical diagnostic criteria, 16 and the diagnosis of FTD was based on international diagnostic criteria. 17 For other types of dementia, the diagnosis was based on the consensus criteria. To rule out the presence of major functional psychiatric disorders, such as schizophrenia and mood disorders, all the participants were evaluated by senior neuropsychiatrists and underwent both physical and neurological examinations as well as a standard psychiatric evaluation. In addition, each patient underwent a brain magnetic resonance imaging or computed tomography scan. The patients were assessed using a battery of neuropsychological and neuropsychiatric tests, including the Mini-Mental State Examination (MMSE), Clinical Dementia Rating (CDR), and the Neuropsychiatric Inventory (NPI). 18 20 After a complete description of the study was provided to all the patients or their proxy, informed consent was obtained. The present study was approved by the Ethics Committee of the Jikei University School of Medicine. Assessment of eating-related problems Information about eating-related problems was gathered by expert nurses who cared directly for the patients at their facilities. Geriatric psychiatrists carried out semi-structured systematic interviews with nurses that were based on the Eating and Swallowing questionnaire. 8,9,11 This questionnaire is designed to assess eating problems in patients with FTD, AD and DLB. The mean conducting time is about 30 min. Details of this questionnaire are described elsewhere. 8 In addition, in order to reveal every eating-related symptom, nurses were asked to report any kinds of eating-related problems that they felt caused difficulty in their daily caring and management of the patients. Nurses were asked to report participants usual eating-related problems in order to avoid eating-related problems that may have been caused by acute medical conditions, such as pneumonia. After the nurses responses were analyzed, the participants eating-related problems were summarized into 24 items, as some of the items on the questionnaire were excluded as they were very rare. For all 208 cases, the nurses were asked to rate the frequency of each of the 24 items (0, never; 1, occasionally, less than once per week; 2, often, about once per week; 3, frequently, several times per week but less than every day; 4, very frequently, once or more per day or continuously). Statistical analyses Data analyses were carried out using SPSS Chicago, IL, USA). (SPSS,
Classifying eating eating problems in in dementia 177 3 Table 1. Demographic and clinical characteristics of the patients Sex (male : female) 79:129 Age (mean ± SD) 78.4 ± 9.9 Diagnosis (AD : VaD : DLB : FTD : 96:58:14:17:23 others) MMSE score (mean ± SD) (range) 10.3 ± 8.2 0 26 CDR grade (0.5:1:2:3) 12:47:53:95 BMI (mean ± SD) 19.4 ± 3.78 AD, Alzheimer s disease; BMI, body mass index; CDR, Clinical Dementia Rating; DLB, dementia with Lewy bodies; FTD, frontotemporal dementia; MMSE, Mini-Mental State Examination; VaD, vascular dementia. To develop a classification of eating-related problems, a factor analysis on the 24 items, using the major factor method with promax rotation, was performed. After scree plotting, four factors were obtained. Items with factor loadings equal to or larger than 0.45 were entered. After conducting factor analysis, logistic regression analysis was conducted in order to determine which independent variables most affected each of the four eating-related factors. In the logistic regression analysis, each of the four eating-related factors was considered to be a dependent variable, and age, sex, diagnosis (AD, VaD, DLB, FTD, and others), MMSE score, CDR score, NPI score, body mass index (BMI) score, and the usage of neuroleptic drugs and cholinesterase inhibitors were considered to be independent variables. If one of the items in each factor was positive, we decided that the factor was positive. RESULTS The demographic and clinical characteristics of the patients are shown in Table 1. The most common dementia-causing condition was AD, followed by VaD, FTD, and DLB. The cohort in this study included patients with severe dementia (i.e. those who had low MMSE scores and who were at an advanced stage of dementia as assessed by the CDR). Table 2 shows the frequency of the 24 eatingrelated problems that the expert nurses felt caused difficulties in their daily caring and management of Table 2. Frequency of the 24 eating-related problems Item Frequency Coughs or chokes when swallowing 19.8% Has difficulty swallowing food 18.2% Has difficulty swallowing liquids 16.8% Takes a long time to eat 14.4% Eats without chewing 11.1% Shows deteriorating table manners 9.6% Shows a loss of appetite 7.8% Forgets to eat and asks for food 7.3% Shows fluctuations in appetite 7.2% Eats the same food for every meal 7.2% Eats non-edible foodstuffs 7.2% Refuses to put food into the mouth 5.9% Chews food but does not swallow it 5.8% Tends to overfill mouth 5.8% Tends to grasp any food item 5.8% Has developed food preferences 5.6% Spits out food 5.3% Hoards food 5.3% Looks for food between meals 4.4% Reports hunger 4.4% Adds more seasoning to food 3.9% Drinks too much 3.4% Overeats at mealtimes 3.4% Tends to eat foods in the same order 3.4% the patients. The most common eating-related problem was coughs or chokes when swallowing, followed by has difficulty swallowing food, has difficulty swallowing liquids, takes a long time to eat, and eats without chewing. Table 3 shows the results of the factor analysis for eating-related problems in dementia. A 4-factor solution was obtained. Eigenvalues of factors 1 to 4 were 4.52, 3.12, 2.26, and 2.03, respectively, accounting for 18.8%, 13.0%, 9.4%, and 8.4%, respectively, of the variance. The cumulative contribution ratio was 49.6%. The correlations between the factors were very low (correlation coefficients were between 0.03 and 0.23). Factor 1 was overeating, which included the tendency to drink too much, to overeat at mealtimes, to grasp any food item, to eat foods in the same order, and to report hunger (alpha coefficient = 0.73). Factor 2 was swallowing problems, which included the tendency to have difficulty swallowing liquids, to have difficulty swallowing food, to cough or choke, and to eat without chewing (alpha coefficient = 0.89). Factor 3 was decrease in appetite,
4178S. S. Shinagawa et et al. al. Psychiatry and Psychiatry Clinical Neurosciences and Clinical 2016; Neurosciences 70: 175 181 2015 Table 3. Factor loadings for eating-related problems in dementia Factor 1 Factor 2 Factor 3 Factor 4 Drinks too much 0.88 0.038 0.169 0.225 Overeats at mealtimes 0.88 0.038 0.17 0.212 Tends to grasp any food item 0.835 0.084 0.198 0.217 Eats in the same order 0.53 0.243 0.105 0.127 Reports hunger 0.459 0.012 0.124 0.069 Adds more seasoning to food 0.385 0.214 0.128 0.064 Overfills mouth 0.347 0.34 0.091 0.058 Shows deteriorating table manners 0.273 0.15 0.131 0.101 Eats non-edible foodstuffs 0.165 0.026 0.018 0.035 Has difficulty swallowing liquids 0.104 0.877 0.025 0.014 Has difficulty swallowing food 0.086 0.865 0.105 0.045 Coughs or chokes 0.099 0.804 0.143 0.034 Eats without chewing 0.127 0.722 0.002 0.006 Hoards foods 0.341 0.347 0.206 0.037 Refuses to put foods in the mouth 0.142 0.067 0.953 0.103 Spits out foods 0.149 0.096 0.483 0.151 Shows fluctuations in appetite 0.071 0.018 0.465 0.056 Shows loss of appetite 0.045 0.055 0.45 0.191 Chews food but does not swallow it 0.182 0.063 0.353 0.028 Takes a long time to eat 0.126 0.124 0.35 0.021 Forgets to eat and asks for food 0.223 0.006 0.307 0.024 Looks for food between meals 0.21 0.027 0.046 0.867 Has developed food preferences 0.168 0.049 0.053 0.854 Eats the same food for every meal 0.211 0.028 0.39 0.71 Bold font indicates that factor loadings equal to or larger than 0.45. which included the tendency to refuse to put food into the mouth, to spit out food, to have fluctuations in appetite, and to have loss of appetite (alpha coefficient = 0.65). Factor 4 was obsession with food, which included the tendency to look for food between meals, to develop food preferences, and to eat the same food for every meal (alpha coefficient = 0.82). Based on the results of factor analyses, logistic regression analysis was conducted for each of the four factors. The results of the logistic regression analysis are summarized in Table 4. None of the independent variables significantly affected the overeating factor; BMI, MMSE, and CDR scores significantly affected the swallowing factor; NPI scores significantly affected the appetite factor; and MMSE and NPI scores significantly affected the obsession factor. DISCUSSION The results of the present study provide initial empirical evidence for the classification of eating-related problems across patients with different types of conditions causing dementia. Our cohorts were institutionalized people with dementia, which means that, as a group, their dementia was relatively severe (46% of the participants received a CDR of 3; the mean MMSE score of the participants was 10.3 ± 8.2). The most common condition causing dementia was AD (46% of the patients had it) in this cohort, but dementia was also caused by VaD, FTD, DLB, and other conditions. Among the participants, common eating-related problems were swallowing-related problems, such as the tendency to cough or choke when swallowing, to have difficulty swallowing food, to have difficulty swallowing liquids, to take a long time to eat, and to eat without chewing. These swallowing-related problems among dementia patients have been reported in many studies. 5,21 23 On the other hand, professional caregivers have identified other eatingrelated problems. The factor analysis revealed four eating-related factors, which existed as distinct symptom groups. These factors were overeating, swal-
Classifying eating eating problems in in dementia 179 5 Table 4. Variables affecting each of the four factors Dependent variables Significant independent variables P-value β Overeating factor None Swallowing problems factor BMI 0.027 0.89 (0.82 0.98) MMSE 0.048 0.94 (0. 88 0.99) CDR 0.030 1.56 (1.10 2.12) Decrease in appetite factor NPI 0.001 4.51 (1.87 10.91) Obsession with food factor MMSE 0.030 0.90 (0.86 0.97) NPI 0.020 2.21 (1.57 4.31) BMI, body mass index; CDR, Clinical Dementia Rating; MMSE, Mini-Mental State Examination; NPI, Neuropsychiatric Inventory. lowing problems, decrease in appetite, and obsession with food. The condition causing dementia did not significantly affect any of these four factors, suggesting that these eating-related changes may occur in any type of dementia, at least in the moderate to severe stages of the disorder. The overeating factor was the most distinctive (factor 1) eating-related factor, which included the tendency to drink too much, to overeat at mealtimes, to grasp any food item, to eat in the same order, and to report hunger. These symptoms have been reported to frequently occur in the case of FTD patients; 8,10 however, in the logistic regression analysis, the condition causing dementia did not have a significant effect on the overeating factor. This result suggests that these symptoms can occur even in the case of other conditions causing dementia, at least in the moderate to severe stages of these conditions. In this cohort, overeating may have a similar neural mechanism across conditions causing dementia. No other independent variables were found to significantly affect the presence of the overeating factor. As a whole cohort of relatively severe stage (CDR3 = 46%), cognitive function, neuropsychiatric symptoms, and disease severity may not have a direct effect on the occurrence of overeating symptoms. Factor 2 was the swallowing problems factor, which was related to BMI and MMSE and CDR scores. As we discussed previously, swallowing problems among dementia patients have been reported in many studies. Our results revealed that swallowing problems were associated with cognitive dysfunction (MMSE) and the progression of dementia (CDR), and as a result, may cause loss of body weight (BMI). This result is consistent with that obtained in previous research. 24 Neuropsychiatric symptoms do not directly relate to the occurrence of the swallowing problems factor. In addition, the usage of neuroleptic drugs did not affect the presence of the swallowing problems factor. A possible explanation for this result may be that the question on usage of neuroleptic drugs had to be answered in a yes/no format. In order to get a clearer picture about the effect of neuroleptic drugs, we may need further analysis on the basis of information regarding the dosage of the drugs. The decrease in appetite factor (factor 3) was independent from the other factors. The NPI score significantly affected the presence of this factor. It was noteworthy that cognitive dysfunction and the progression of dementia (CDR) did not significantly affect the decrease in appetite. It is also noteworthy that usage of cholinesterase inhibitors did not significantly affect the decrease in appetite in this cohort. One possibility is that only demented participants who can tolerate enough of these drugs use cholinesterase inhibitors, and those who showed some kind of side-effect to these drugs already stopped taking them before administration. Therefore, when clinicians treat patients with a loss of appetite who do not eat enough, they should investigate the patients neuropsychiatric symptoms. The obsession with food factor (factor 4) was independent from the decrease in appetite and overeating factors, which suggests that decrease in appetite and overeating may have different neural mechanisms from that of the obsession with food. The symptom of obsession with food is also frequently observed among FTD patients, 8,10 although the logistic regression analysis failed to reveal the effect of the condition causing dementia. Obsession with food seems to
6180S. S. Shinagawa et et al. al. Psychiatry and Psychiatry Clinical Neurosciences and Clinical 2016; Neurosciences 70: 175 181 2015 occur in patients with severe cognitive impairments (MMSE) and patients with severe neuropsychiatric symptoms (NPI). When interpreting our results, there are a few methodological issues that should be taken into consideration. First, our cohorts included only institutionalized patients, and excluded patients with relatively mild dementia. Although participants with relatively mild dementia are assumed to have fewer eating-related problems, more studies are needed in order to reveal the types of eating-related problems that occur among people with relatively mild dementia. Next, although we set the condition causing dementia as an independent variable in the logistic regression analysis, patients with FTD, DLB, and other conditions causing dementia were relatively few. This may be why the logistic regression analysis failed to show that the condition causing dementia had a significant effect on eating-related problems. We need to conduct a head-to-head comparison of eating-related problems with regard to each condition causing dementia. Also, 208 patients might not be enough for the analyses in this study as disease severity and the causes of dementia in this cohort were widespread. Next, we did not include other medical conditions and comorbidities that may affect swallowing and appetite problems in the logistic regression analysis, as there are so many medical conditions. However, when gathering information by expert nurses, we avoided patients with acute medical conditions, such as pneumonia. Finally, in the logistic regression analysis, the total NPI score was set as an independent variable. Because numbers of independent variables of logistic regression analysis are limited, we cannot set all NPI subscores as independent variables. However, for a more in-depth picture, further analysis of each NPI subscore, for example, the scores on delusion, agitation, depression, and apathy, is required. In conclusion, in the case of our institutionalized people with dementia, eating-related problems could be classified into four factors: overeating, swallowing problems, decrease in appetite, and obsession with food. Each factor was associated with different background variables, including disease severity and neuropsychiatric symptoms, but not with the condition causing dementia. Our results suggest that these eating-related problems are common across various conditions causing dementia, and the four factors should be separately considered when attempting to understand the underlying mechanisms of eatingrelated problems. It is also important for clinicians to educate caregivers about eating-related problems in dementia. ACKNOWLEDGMENTS This study was conducted with assistance from a Ministry of Health, Labour and Welfare Grant (Dementia Provisions Study Project). DISCLOSURE STATEMENT None of the authors has a conflict of interest regarding this research. REFERENCES 1. Frissoni GB, Franzoni S, Bellelli G, Morris J, Warden V. Overcoming eating difficulties in the severely demented. In: Volicer L, Hurley AC (eds). Hospice Care for Patients with Advanced Progressive Dementia. Springer, New York, 1998; 48 67. 2. Holm B. Factors associated with nutritional status in a group of people in an early stage of dementia. Clin. Nutr. 2003; 22: 385 389. 3. Hsiao H-C, Chao H-C, Wang J-J. Features of problematic eating behaviors among community-dwelling older adults with dementia: Family caregivers experience. Geriatr. Nurs. 2013; 34: 361 365. 4. Pivi GAK, Bertolucci PHF, Schultz RR. Nutrition in severe dementia. Curr. Gerontol. Geriatr. Res. 2012. doi: 10.1155/ 2012/983056 5. van de Rest O, Berendsen AA, Haveman-Nies A, de Groot LC. Dietary patterns, cognitive decline, and dementia: A systematic review. Adv. Nutr. 2015; 6: 154 168. 6. Trinkle DB, Burns A, Levy R. Brief report: Abnormal eating behavior in dementia A descriptive study. Int. J. Geriatr. Psychiatry 1992; 7: 799 803. 7. Cullen P, Abid F, Patel A, Coope B, Ballard CG. Eating disorders in dementia. Int. J. Geriatr. Psychiatry 1997; 12: 559 562. 8. Ikeda M, Brown J, Holland AJ, Fukuhara R, Hodges JR. Changes in appetite, food preference, and eating habits in frontotemporal dementia and Alzheimer s disease. J. Neurol. Neurosurg. Psychiatry 2002; 73: 371 376. 9. Shinagawa S, Ikeda M, Nestor PJ et al. Characteristics of abnormal eating behaviours in frontotemporal lobar degeneration: A cross-cultural survey. J. Neurol. Neurosurg. Psychiatry 2009; 80: 1413 1414. 10. Ahmed RM, Irish M, Kam J et al. Quantifying the eating abnormalities in frontotemporal dementia. JAMA Neurol. 2014; 71: 1540 1546. 11. Shinagawa S, Adachi H, Toyota Y et al. Characteristics of eating and swallowing problems in patients who have
Classifying eating eating problems in in dementia 181 7 dementia with Lewy bodies. Int. Psychogeriatr. 2009; 21: 520 525. 12. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Association, Washington, DC, 2000. 13. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer s disease: Report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer s Disease. Neurology 1984; 34: 939 944. 14. Román GC, Tatemichi TK, Erkinjuntti TJ et al. Vascular dementia: Diagnostic criteria for research studies. Report of the NINDS-AIREN International Workshop. Neurology 1993; 43: 250 260. 15. Chui HC, Victoroff JI, Margolin D, Jagust W, Shankle R, Katzman R. Criteria for the diagnosis of ischemic vascular dementia proposed by the State of California Alzheimer s Disease Diagnostic and Treatment Centers. Neurology 1992; 42: 473 480. 16. McKeith IG, Dickson DW, Lowe J et al. Diagnosis and management of dementia with Lewy bodies: Third report of the DLB consortium. Neurology 2005; 65: 1863 1872. 17. Neary D, Snowden J, Gustafson L et al. Frontotemporal lobar degeneration: A consensus on clinical diagnostic criteria. Neurology 1998; 51: 1546 1554. 18. Folstein MF, Folstein SE, McHugh PR. Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 1975; 12: 189 198. 19. Hughes CP, Berg L, Danziger WL, Coben LA, Martin RL. A new clinical scale for the staging of dementia. Br. J. Psychiatry 1982; 140: 566 572. 20. Cummings JL, Mega MS, Gray KK, Rosenberg-Thompson SS, Carusi DAD, Gornbein JJ. The Neuropsychiatric Inventory: Comprehensive assessment of psychopathology in dementia. Neurology 1994; 44: 2308 2314. 21. Kindell J. Feeding and Swallowing Disorders in Dementia. Speechmark Publishing Ltd, Oxford, 2002. 22. Affoo RH, Foley N, Rosenbek J, Shoemaker JK, Martin RE. Swallowing dysfunction and autonomic nervous system dysfunction in Alzheimer s disease: A scoping review of the evidence. J. Am. Geriatr. Soc. 2013; 61: 2203 2213. 23. Alagiakrishnan K, Bhanji RA, Kurian M. Evaluation and management of oropharyngeal dysphagia in different types of dementia: A systematic review. Arch. Gerontol. Geriatr. 2013; 56: 1 9. 24. Nogueira D, Reis E. Swallowing disorders in nursing home residents: How can the problem be explained? Clin. Interv. Aging 2013; 8: 221 227.