COPING WITH ANXIETY, DEPRESSION, BURDEN AND QUALITY OF LIFE IN INFORMAL PRIMARY CAREGIVERS OF COMMUNITY-DWELLING INDIVIDUALS WITH DEMENTIA

M. Muscat¹, C. Scerri²

1. Department of Gerontology, Faculty for Social Wellbeing; 2. Department of Pathology, Faculty of Medicine and Surgery, University of Malta, Msida, Malta MSD 2080.

Corresponding Author: Charles Scerri PhD, Department of Pathology, Faculty of Medicine and Surgery, University of Malta, Msida MSD 2080, Malta; Tel.: +356 23402905; Fax: +356 21320281; E-mail: charles.scerri@um.edu.mt

J Aging Res Clin Practice 2018;7:128-135
Published online October 15, 2018, http://dx.doi.org/10.14283/jarcp.2018.22

Abstract

Objective: This study aimed to investigate how informal primary caregivers of individuals with dementia living in the community cope with caring-related measures of anxiety, depression, burden and quality of life. Participants and Design: Participants included 60 informal caregivers (23 males and 37 females) of community-dwelling individuals with dementia who attended a state-run geriatric day hospital in Malta. Caregiver measures included the Hospital Anxiety and Depression Scale, the World Health Organization Quality of Life–BREF and Brief COPE questionnaires, and Zarit Burden Interview. The Mini Mental State Examination and Barthel Index of Activities of Daily Living scores were used to determine the degree of cognitive impairment and performance in activities of daily living of care-recipients. Results: Informal caregivers experienced anxiety and depression with both emotional distress states negatively affecting all quality of life domains. Depression and burden experienced by informal primary caregivers showed a strong association with individuals with dementia-related variables such as age, cognitive impairment and activities of daily living scores. The use of dysfunctional coping strategies was found to be related to caregivers’ emotional distress, low quality of life and burden. Conclusion: The findings indicate that informal primary caregivers experienced anxiety and depression, had a lower quality of life, and feel burdened during their caring role. However, caregivers making use of emotion-focused coping strategies were found to be protected against emotional distress. The results highlight the need of providing support services aimed at promoting the psychological wellbeing of informal carers of community-dwelling individuals with dementia.

Key words: Caregiver, coping, dementia, emotional distress, quality of life.

Introduction

Dementia is a clinical term referring to a group of brain disorders characterized by progressive deterioration of cognitive abilities. In 2015, it was estimated that 1.5% of the population in Malta had dementia, a figure that is projected to more than double in the next 30 years (1). This, in conjunction with a demographic shift favouring a progressive increase in the elderly population, will add to a growing burden on family members who, in the majority of cases, provide informal care for these individuals at home (2).
At present there is no cure for the most common forms of dementia and consequently the main focus lies in promoting the wellbeing and providing optimal quality of life for the individual with dementia and their caregivers (3). Previous research has demonstrated that high levels of neuropsychiatric symptoms in dementia caregivers leads to a reduction in their quality of life (4) and caregiver burden is mostly related to the caregiver ability to cope with the situation (5). A number of coping strategies and styles adopted by dementia caregivers have been proposed with those based on emotional support and problem-focused strategies being associated with caregiver wellbeing and positive outcomes (6-8).
The main objective of this study was to investigate how coping strategies and styles used by informal primary caregivers caring for an individual with dementia living in the community influence their levels of anxiety, depression, burden and quality of life. This category of caregivers was selected as previous research have shown that, in Malta, rather than resorting to institutionalization of the person with dementia, a unique model of care based on reliance on families through a rotation pattern of care by different family members is preferred (2). Therefore, the identification of predictive factors that enhance the wellbeing of caregivers of individuals with dementia living in the community would not only ensure that health and social support programmes are designed to meet the desired needs but would further delay institutionalization of the care-recipient (9).

Methods

The study was conducted in Malta from early January to the end of May 2015. Participants were informal primary caregivers of individuals with dementia attending a state-run geriatric day hospital who had received a formal diagnosis of dementia by a medical specialist. A convenience sample of caregivers (n = 74) was selected with selection criteria being attendance to the day hospital by the individuals with dementia, individuals with dementia living in the community, caregiver residing in the same or separate household and being the primary care provider. Participants were contacted by telephone following which 60 agreed to take part in the study. Sociodemographic data of caregivers included age, gender, occupation, relationship with individuals with dementia, marital status, level of education, whether they were living with the individuals with dementia, duration of caregiving in years, number of contact hours per day and whether they were formally diagnosed with anxiety/depression during their caregiving role. Information on individuals with dementia included age, gender and dementia type. The levels of cognitive impairment and activities of daily living of individuals with dementia were based on the Mini Mental State Examination (MMSE) (10) and Barthel Index of Activities of Daily Living (BI-ADL) (11) scores measured by a geriatric medical specialist prior to study commencement.
The research instruments used in assessing caregivers included the Hospital Anxiety and Depression Scale (HADS), the World Health Organization Quality of Life–BREF (WHOQOL-BREF) and Brief COPE questionnaires, and Zarit Burden Interview (ZBI). The HADS consists of two seven–item subscales, one related to anxiety and the other to depression (12). Each item carries a four-point scale (0-3) with the total possible score for both anxiety and depression ranging from 0-21. Scores are categorized as normal (0-7), mild (8-10), moderate (11-14) and severe (15-21). The WHOQOL-BREF comprises 26 items grouped under domains for physical health, psychological health, social relationships and environmental health (13). Each item is rated on a 5-point Likert scale with higher scores denoting better quality of life. The Zarit Burden Interview consists of 22 items with a 5-point Likert scale ranging from 0 (never) to 4 (nearly always) (14) whereas the Brief COPE measures a number of different coping strategies and consists of 14 subscales with two questions per style with a 4-point Likert scale ranging from 1 (I haven’t been doing this at all) to 4 (I’ve been doing this a lot) (15). The coping strategies are divided into 3 domains: emotion-focus (use of emotional support, positive reframing, acceptance, religion, humour), problem-focus (active coping, planning, use of instrumental support) and dysfunctional coping (venting, denial, substance use, behavioral disengagement, self-distraction, self-blame) (16).
All interviews with informal primary caregivers were carried out face-to-face in English language at the participants’ residence. The study was approved by the Faculty of Social Wellbeing Ethics Committee and the Research Ethics Committee of the University of Malta. Permission was also granted by the management of the day hospital. Participants were guaranteed confidentiality and anonymity and were free to withdraw at any stage of the interview without giving a reason. Written consent was obtained from all participants. Depending on cognitive impairment, consent from individuals with dementia was obtained either directly or by proxy.
Descriptive statistics were used to summarize sociodemographic and clinical data of participants as percentages, means and standard deviation (SD). Relationships between anxiety, depression, quality of life, burden and coping scores with sociodemographic characteristics and clinical data were analysed using Student’s t-test for two groups of data and one factor ANOVA with post hoc comparisons using Tukey for multiple groups. In the event that the data were not normally distributed as determined by the Shapiro-Wilk test, the Mann-Whitney U test was applied.
To study the degree to which anxiety and depression, quality of life and burden experienced by caregivers was related to their coping strategies and styles, the Pearson’s correlation coefficient (r) analysis was conducted. All research instruments used for caregivers’ measures were assessed for internal consistency using the Cronbach’s alpha test. Data analysis was conducted using PASW Statistics (version 20.0) with significance level set at 0.05.

Results

Characteristics of participants

Descriptive characteristics of individuals with dementia and their informal primary caregivers are presented in Table 1. Care-recipients had a mean age of 77.5 years (range: 46 – 92) and showed moderate functional dependency levels. With respect to the severity of cognitive function, 36.7% had mild, 25.0% moderate and 38.3% severe cognitive impairment. A significant positive correlation was observed between MMSE and BI-ADL (r = 0.801, p < 0.001) indicating that individuals with dementia having severe cognitive impairment were the most functionally dependent.
Informal primary caregivers were mostly females, married, had a secondary level of education, unemployed and living in the same household. The duration of caregiving role varied from 1 to 25 years with an average of 4.5 years whereas the average number of contact hours spent in daily caregiving was 16.2 hours. A third of participants indicated that they spend 24 hours per day in their caregiving role.

Table 1
Sociodemographic characteristics and clinical data of individuals with dementia and their informal primary caregivers (AD, Alzheimer’s disease; BI-ADL, Barthel Index of Activities of Daily Living; ipCG, informal primary caregiver; IWD, individual with dementia; LBD, Lewy-body dementia; MMSE, Mini-Mental State Examination; VaD, vascular dementia)

Informal primary caregivers’ anxiety and depression

The mean anxiety score for caregivers was found to be significantly higher than the mean depression score (F = 8.594, p < 0.001) denoting that caregivers experienced more anxiety than depression during their caring role (Table 2). Furthermore, anxiety and depression were found to be significantly correlated (r = 0.777, p < 0.001) indicating that caregivers with high anxiety scores tended to have higher levels of depression. Caregivers who had a lower level of education, cared for individuals with dementia with low cognitive and functional scores, and formally diagnosed with anxiety/depression during the caregiving role experienced higher levels of anxiety and depression.

Table 2
Relationship between anxiety, depression, quality of life and burden scores with sociodemographic characteristics and clinical data of individuals with dementia and their informal primary caregivers (α, Cronbach’s alpha; BI-ADL, Barthel Index of Activities of Daily Living; ipCG, informal primary caregiver; IWD, individual with dementia; MMSE, Mini-Mental State Examination)

Informal primary caregivers’ quality of life

As indicated in Table 2, caregivers who were employed, had a post-secondary level of education and have not been formally diagnosed with anxiety/depression during their caregiving role had higher quality of life scores. Amongst the domains tested, the two highest average standardised scores were reported for the environment and psychological domains with social relationships scoring the lowest. The social relationships domain was found to be significantly correlated with the age of the individual with dementia (r = 0.264, p = 0.042) and caregiver (r = -0.277, p = 0.032) and related to whether the caregiver was living in the same household, relationship with the individual with dementia and the educational status of the caregiver. The latter was also found to similarly affect the environment domain.

Informal primary caregivers’ burden

Approximately half of the caregivers participating in this study (46.7%, n = 28) indicated that they experienced moderate to severe/severe burden whilst caring for an individual with dementia. A significant inverse correlation was found between the age of the individual with dementia and the burden score (r = -0.299, p = 0.020) suggesting that the younger the individual with dementia, the greater the burden on the caregiver. A low BI-ADL score and a formal diagnosis of anxiety/depression in the caregiver were also found to be significantly related to higher caregiver burden (Table 2).

Informal primary caregivers’ coping strategies

The mean rating scores for emotion-focus and problem-focus strategies were similar and significantly higher than dysfunctional coping (p < 0.001) denoting that the latter was the coping strategy that was used the least by the caregivers (Table 3). Moreover, dysfunctional coping was inversely correlated with the age of the care-recipient (r = -0.268, p = 0.038) and significantly related to the increasing number of hours/day spent in caring and the presence of a formal diagnosis of anxiety/depression in the caregiver. Out of the 14 coping styles, the most frequently used were acceptance and active coping with substance abuse scoring the lowest.

Table 3
Relationship between coping strategies and styles with sociodemographic characteristics and clinical data of individuals with dementia and their informal primary caregivers. Cronbach’s α for the Brief COPE = 0.713 (BI-ADL, Barthel Index of Activities of Daily Living; ipCG, informal primary caregiver; IWD, individual with dementia)

Association between informal primary caregivers’ measures of anxiety and depression, quality of life, burden and coping strategies and styles

In informal primary caregivers, higher levels of both anxiety and depression were found to be related to a reduction in the overall quality of life and increased burden (Table 4). Furthermore, caregivers who were using dysfunctional coping strategies experienced higher levels of anxiety and depression. The latter were also found to be positively correlated with the coping styles of planning, behavioral disengagement, denial and self-blame. Conversely, the use of acceptance, positive reframing and self-distraction were related to diminished emotional distress. Caregivers who reported high levels of burden had lower quality of life scores with all domains being affected except physical health. Burden scores were also found to be high in caregivers adopting dysfunctional coping strategies with relationships to coping styles similar to those reported for anxiety and depression.

Table 4
Correlations between anxiety, depression, quality of life, burden and coping strategies and styles of informal primary caregivers of individuals with dementia (WHOQOL-BREF, World Health Organization Quality of Life-BREF; ZBI, Zarit Burden Interview). Only significant Pearson correlation coefficient (r) values reported (* P < 0.05, ** P < 0.01, *** P < 0.001)

Discussion

To the best of our knowledge, this is the first investigation that explored anxiety, depression, burden, quality of life and coping strategies used by informal primary caregivers of community-dwelling individuals with dementia in Malta. Determining the psychological wellbeing and type of coping strategies adopted by this category of caregivers could aid in developing community services that address their needs. This is in agreement with the Call for Action adopted by the First WHO Ministerial Conference on Global Action Against Dementia that emphasised that policy interventions should be sensitive to the specific needs of people living with dementia and their caregivers (17).
The findings reported here showed that more than half of participating caregivers experienced anxiety and with a quarter feeling depressed. Similar to other findings (18, 19), caregivers having higher levels of education scored significantly lower in anxiety and depression possibly indicating that education might act as a protective effect. Of note was the absence of depression in the two-thirds of informal primary caregivers. People caring for individuals with dementia respond to depression in different ways and at different times. They might experience emotional distress soon after diagnosis of dementia in their relative, whereas in others as dementia progresses to its severe stage and the duration of care increases (20). However, the latter was not supported by the present findings in which the levels of anxiety, depression, burden and quality of life in informal primary caregivers were not found to be related to the number of years and number of hours per day spent in caregiving. Even though most caregivers participating in this study appeared to experience lower levels of depression, more research is needed to determine how the changing course of dementia might impact the caregiver emotional response in the local context.
Factors that strongly impacted caregiver burden in this study were the younger age of the individual with dementia, loss of functional status and a formal diagnosis of anxiety and depression in the caregiver. Although caregivers taking care of an individual with dementia with greater functional dependency experienced higher burden levels, no association between burden and patient cognitive scores was found possibly suggesting that deterioration in individuals with dementia abilities to take care of themselves leads to higher caregiver burden compared to cognitive deterioration. Similar trends were observed in other countries in which the direct influence of patients’ cognition on caregiver burden is limited with the patients’ functional abilities being the main predictor for burden (21). Contrasting previous data (22, 23), the age of the caregiver was not found to be related to burden. Rather, the age of the care-recipient showed a significant effect, with a younger age associated to higher caregiver burden. This is not surprising considering that young individuals with dementia pose additional challenges on their primary caregivers such as lack of appropriate access to specialized care as well as work and additional family commitments (24).
In caregivers, dysfunctional coping strategies were found to be significantly related to anxiety and depression, the duration of caregiving and the age of the care-recipient. Emotion-focus coping strategies, with coping styles that included acceptance and positive reframing, were preferred by the majority of caregivers and this may have contributed to a reduction in the anxiety and depression scores. Conversely, dysfunctional coping was mostly related to an increase in caregiver burden. Of note was that positive reframing coping style, in which stressful events are redefined in order to make them manageable (25), showed a significant correlation with emotional distress status, quality of life and caregiver burden. The ability to use this coping style in the present study was possibly related to the cohort cultural context, in which dementia care is a family affair and a shared care arrangement between family members as a form of respite is the norm (2).
The current study has a number of limitations. The WHOQOL-BREF instrument was not specifically developed for caregivers of individuals with dementia, although there are precedents for its use in this population (26). The study made use of individuals with dementia and their informal primary caregivers attending a day hospital which may not be representative of the dementia caregiver population in Malta. Sample selection was not randomised and thus the possibility of selection bias cannot be excluded. The modest sample size may have also limited statistical power.
In conclusion, the results reported here indicate that informal primary caregivers of individuals with dementia living in the community are more likely to suffer from emotional distress, experience burden and have a lower quality of life. However, those caregivers who use emotion-focused strategies were found to be protected against emotional distress. This continues to highlight the need of identifying multi-component interventions that support informal caregivers in maintaining a lifestyle that improves their quality of life. Knowing that in Malta dementia care in the community mostly follows a shared familial arrangement, caregiver support should be tailored to offer caring styles that adjust according to the caregiver circumstances and needs. Furthermore, assessing the psychological wellbeing of informal caregivers of individuals with dementia together with providing the necessary information on coping strategies that would support their caregiving role should form part of the dementia-management process. The present research continues to add to the recommendations of the National Strategy for Dementia in the Malta in which the provision of holistic support services to community-dwelling individuals with dementia and their informal caregivers is one of the main priorities to be addressed (27).

Acknowledgements: The authors would like to thank the caregivers and individuals with dementia who participated in the study.

Conflict of interest: none

Funding: none

Ethical standards: Ethical approval for the study was granted by the Faculty of Social Wellbeing Ethics Committee and the Research Ethics Committee of the University of Malta.

References

1.   Scerri A, Scerri C. Dementia in Malta: New prevalence estimates and projected trends. Malta Med J 2012;24:21-24.
2.   Innes A, Abela S, Scerri C. The organisation of dementia care by families in Malta: The experiences of family caregivers. Dementia 2011;10:165-184.
3.   Ettema TP, Dröes RM, de Lange J, Ooms ME, Mellenbergh GJ, Ribbe MW. The concept of quality of life in dementia in the different stages of the disease. Int Psychogeriatr 2005;17:353-370.
4.   Takai M, Takahashi M, Iwamitsu Y, Oishi S, Miyaoka H. Subjective experiences of family caregivers of patients with dementia as predictive factors of quality of life. Psychogeriatrics 2011;11:98-104.
5.   Campbell P, Oyebode J, Job D et al. Determinants of burden in those who care for someone with dementia. Int J Geriatr Psychiatry 2008;23:1078-1085.
6.   Li R, Cooper C, Bradley J, Shulman A, Livingston G. Coping strategies and psychological morbidity in family carers of people with dementia: a systematic review and meta-analysis. J Affect Disord 2012;139:1-11.
7.   Cooper C, Katona C, Orrell M, Livingston G. Coping strategies, anxiety and depression in caregivers of people with Alzheimer’s disease. Int J Geriatr Psychiatry 2008;23:929-936.
8.   Kneebone II, Martin PR. Coping and caregivers of people with dementia. Br J Health Psychol 2003;8:1-17.
9.   Afram B, Stephan A, Verbeek H et al. Reasons for institutionalization of people with dementia: informal caregiver reports from 8 European countries. J Am Med Dir Assoc 2014;15:108-116.
10.   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.
11.   Collin C, Wade DT, Davies S, Horne V. The Barthel ADL index: a reliability study. Int Disabil Stud 1988;10:61– 63.
12.   Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand 1983;67:361-370.
13.   World Health Organization. WHOQOL-BREF: introduction, administration, scoring and generic version of the assessment – field trial version. 1996. WHO, Geneva.
14.   Zarit SH, Reever KE, Bach-Peterson J. Relatives of the impaired elderly: correlates of feelings of burden. Gerontologist 1980;20:649-655.
15.   Carver CS. You want to measure coping but your protocol’s too long: Consider the Brief COPE. Int J Behav Med 1997;4:92-100.
16.   Cooper C, Katona C, Orrell M, Livingston G. Coping strategies and anxiety in caregivers of people with Alzheimer’s disease: The LASER-AD study. J Affect Disord 2006;90:15–20.
17.   World Health Organization. Call for Action by the participants in the First WHO Ministerial Conference on Global Action Against Dementia (Geneva, 16-17 March 2015). http://www.who.int/mental_health/neurology/dementia/call_for_action_en.pdf?ua=1. Accessed 17 May 2018.
18.   Bjelland I, Krokstad S, Mykletun A, Dahl AA, Tell GS, Tambs K. Does a higher educational level protect against anxiety and depression? The HUNT study. Soc Sci Med 2008;66:1334-1345.
19.   Sansoni J, Vellone E, Piras G. Anxiety and depression in community-dwelling, Italian Alzheimer’s disease caregivers. Int J Nurs Pract 2004;10:93-100.
20.   Covinsky K, Newcomer R, Fox P et al. Patient and caregiver characteristics associated with depression in caregivers of patients with dementia. J Gen Intern Med 2003;18:1006-1014.
21.   Bergvall N, Brinck, P, Eek D et al. Relative importance of patient disease indicators on informal care and caregiver burden in Alzheimer’s disease. Int Psychogeriatr 2011;23:73-85.
22.   Marvardi M, Mattioli P, Spazzafumo L et al. The Caregiver Burden Inventory in evaluating the burden of caregivers of elderly demented patients: results from a multicenter study. Aging Clin Exp Res 2005;17:46-53.
23.   Serrano-Aguilar PG, Lopez-Bastida J, Yanes-Lopez V. Impact on health-related quality of life and perceived burden of informal caregivers of individuals with Alzheimer’s disease. Neuroepidemiology 2006;27:136-142.
24.   Millenaar JK, de Vugt ME, Bakker C et al. The Impact of Young Onset Dementia on Informal Caregivers Compared with Late Onset Dementia: Results from the NeedYD Study. Am J Geriatr Psychiatry 2016;24:467-474.
25.   Kliewer W, Fearnow MD, Miller PA. Coping socialization in middle childhood: tests of maternal and paternal influences. Child Dev 1996;67:2339-2357.
26.   Wang J, Xiao LD, He GP, Ullah S, De Bellis A. Factors contributing to caregiver burden in dementia in a country without formal caregiver support. Aging Ment Health 2014;18:986-996.
27.   Scerri C. Empowering change: a national strategy for dementia in the Maltese Islands. 2015. Parliamentary Secretariat for the Rights of Persons with Disability and Active Ageing, Valletta, Malta.

BASELINE FINDINGS OF CARENUTRITION INTERVENTION (RCT) AMONG OLDER CAREGIVERS – RISK OF MALNUTRITION AND INSUFFICIENT PROTEIN INTAKE

S. Kunvik^1,2, R. Valve², K. Salminen¹, M. Salonoja¹, M.H. Suominen³

1. The Social Services and Healthcare Centre of Pori, Finland; 2. Department of Food and Environmental Sciences, University of Helsinki, Finland; 3. Unit of Primary Health Care, Helsinki University Central Hospital, Finland.

Corresponding Author: Susanna Kunvik, The Social Services and Healthcare Centre of Pori, Finland and Department of Food and Environmental Sciences, University of Helsinki, Finland, susanna.kunvik@gmail.com

J Aging Res Clin Practice 2017;6:117-123
Published online May 18, 2017, http://dx.doi.org/10.14283/jarcp.2017.13

Abstract

Objectives: Older caregivers are vulnerable to nutritional problems, but only a few studies have examined their nutrition. The purpose of this study was to determine the associations between nutritional status and nutrient intake among older caregivers. Design: Cross-sectional analysis of baseline data from the CareNutrition randomized controlled trial (RCT). Setting: Community-dwelling caregivers from the Western part of Finland in two different clusters. Participants: A total of 79 caregivers aged ≥65 with normal cognition were recruited for the study, all of whom had officially approved caregiver status by The Social Insurance Institution of Finland. Measurement: Nutritional status was assessed by the Mini Nutritional Assessment (MNA), nutrient intake by a three-day food diary, nutrition-related blood markers by laboratory tests, cognition by the Mini Mental State Examination (MMSE), and other baseline characteristics were also evaluated using validated methods. Results: The majority of the caregivers (79.7%) had a good nutritional status (MNA points >23.5), 19% were at risk of malnutrition (MNA points 17-23.5) and one person (1.3%) already suffered from malnutrition (MNA points <17). The female caregivers were at a higher risk of malnutrition than the males (26.5% vs. 6.7%, p=0.026). Depressive symptoms and medication were associated with decreased nutritional status, and good health-related quality of life with better nutritional status. Mean protein intake was 1.0 g/kg IBW/d and 79.7% of the caregivers (77.6% female, 83.3% male) did not consume the recommended protein intake of 1.2 g/kg IBW/d. Their intake of dietary fibre, folate and vitamin D was also insufficient. Conclusion: Every fifth caregiver was at risk of malnutrition. The females were at a higher risk than the males. Most of the caregivers had insufficient protein intakes. These findings confirm the importance of investigating the nutritional status of older caregivers and indicate a need for preventive nutritional guidance.

Key words: Caregiver, nutrition, nutrient intake.

Introduction

The world’s population is ageing, and as a consequence, the number of older people with disabilities and chronic diseases who need support and assistance will increase (1). Informal caregivers provide valuable services to people with long-term care needs. Europe has approximately 100–125 million caregivers (2). In Finland, about 350 000 caregivers help their relatives or loved ones, and in 2013, roughly 42 500 caregivers received support for informal care from their municipality. Half of these caregivers are ≥65 years old, and every fourth ≥75 years old. More than half are female and the majority take care of their spouses (3, 4).
Informal care is extremely important in the context of an ageing population, the increasing pressures on public finances, and rising life expectancy at older ages (5). Concern has been mounting about the health and welfare of people who provide informal care for family or friends with chronic illnesses. Older caregivers are often under a heavy burden and suffer from health problems themselves (6). They are at an increased risk of stress, depression and other health complications that can increase the risk of nutritional problems (7-10). Many factors increase this risk among older caregivers because ageing is accompanied by numerous cognitive, psychological and social factors, which may expose older people to inadequate nutrition and poorer well-being (11).
Studies have found the prevalence of malnutrition in community-dwelling older people to be 1%–5%, and one in four to be at risk of malnutrition (12, 13). Among older caregivers, the prevalence of malnutrition is around 5%, and about 16%–32% of caregivers are at risk of malnutrition (14, 15). Intake of protein is also low (<1 g/kg/d) among older caregivers (16). Insufficient protein intake may contribute to age-related loss of lean muscle mass, which can in turn lead to impaired physical function (17). This can weaken caregivers’ ability to cope with everyday tasks and the provision of care. To maintain bone mass, muscle mass, and strength, protein intake should be 1.2–1.5 g protein/kg/d (18).
Relatively few studies have assessed the levels of nutritional risk and nutrient intake among community caregivers. Thus, our study aims to examine older (≥65 y) caregivers’ nutritional status and nutrient intake.

Methods

Setting

This cross-sectional study is part of a randomized controlled intervention trial, CareNutrition, which explores the effectiveness of tailored nutritional counselling on protein intake and wellbeing among older caregivers (≥65 y) and people (≥50 y) receiving care. In this cross-sectional study, we focus on older caregivers. The study was approved by the Ethics Committee of the Hospital District of Southwest Finland. Informed consent was obtained from the participants. The trial was registered and described at the Australian New Zealand Clinical Trials Registry, Trial Id: ACTRN12615001254583.

Participants

Caregivers were recruited for the study during nurses’ appointments, by inviting them to attend a caregivers’ well-being and health screening. These screenings were organized in two clusters; Autumn 2015 and Spring 2016. We invited two groups of caregivers; those who received care allowance from the Services for Disabled People (caregivers ≥65 years) and those who received care allowance from the Services for Older People (caregiver ≥40 years, informal carer ≥3 years). These criteria were decided before this study began, and were based on the recommendations of the Finnish Ministry of Social Affairs and Health. All caregivers had a caregiver status officially approved by The Social Insurance Institution of Finland.
If a caregiver showed an interest in the study during the health screening, a nutritionist made a home visit during which they provided oral and written information about the study. Informed consent was obtained from the caregiver if they fulfilled the inclusion criteria (all criteria had to be fulfilled), which were: age of ≥65 during the study year, informed consent, an officially confirmed caregiver status, living at home, and normal cognition (geriatric assessment MMSE points ≤25, if assessment was needed). If the caregiver participated in the study, the data from the nurse’s appointment were used as baseline measurements.
In autumn 2015 and spring 2016, we sent an invitation to a health screening to 368 caregivers, of whom 169 agreed to attend (Figure 1). During the health screening, 92 participants expressed interest in participating in the study. Ten were too young to participate. During the nutritionist’s first visit, a further 13 caregivers were excluded from the study for not meeting the inclusion criteria or declining to participate after the interview. A total of 79 caregivers aged ≥65 were recruited for the study.

Figure 1
Flow chart of participant enrolment

Measurements

Baseline measurements were taken during two different appointments; the nurse’s health screening and the nutritionist’s home visit. The nurse’s appointment was at the health care centre, with a trained nurse, and included several assessments. Cognition was measured by the MMSE (19), activities of daily living (ADL) by the Katz index (20), instrumental activities of daily living (IADL) by the Lawton-Brody questionnaire (21), lower extremity muscle strength by the Five Times Sit to Stand Test (22), depression by the Geriatric Depression Scale (GDS-15) (23), medication by an open question, and harmful alcohol use (alcohol consumption, drinking behaviours, and alcohol-related problems) by the Alcohol Use Disorders Identification Test (AUDIT) (24). An experienced geriatrician reviewed the health screening papers. After the nurse’s appointment, a nutritionist made a home visit. Nutritional status was assessed by the MNA (25), health-related quality of life (HRQoL) by the 15D measure (26), and both-hand grip strength (27) using a Jamar Hydraulic Hand Dynamometer (Jamar Bolingbrook IL 60440-4989). The hand-grip strength of each hand was measured two or three times and the best result from the dominating hand was taken as the result. Nutrient intake was assessed via the three-day food diaries that caregivers returned by mail after the nutritionist’s home visit. We analysed the food diaries using the Finnish National Food Composition Database, Fineli. Ideal bodyweight (IBW) was used to calculate protein intake/kg IBW/d. If the caregivers’ body mass index (BMI) was between 20 kg/m2 and 30 kg/m2, we used the actual BMI. If BMI was under 20 kg/m2, it was adjusted to 20 and if above 30 kg/m2, it was adjusted to 30. Nutrition-related laboratory tests of plasma 25(OH)D vitamin, complete blood count (haemoglobin reported), plasma albumin, and serum prealbumin were conducted in the Satakunta Central Hospital laboratory (SataDiag, Finnish Accreditation Service, standards SFS-EN ISO/IEC 17025:2005, SFS-EN ISO 15189:2013) after the nutritionist’s visit. Haemoglobin was assessed using a photometric system; serum 25(OH)D vitamin levels using a immunoluminometric system (Advia Centaur) that measures both ergocalciferol and cholecalciferol 25-hydroxylated metabolites; plasma albumin using a photometric (bromocrerol purple method) system; and serum prealbumin using a photometric, immunochemical system. Use of vitamin D supplement was assessed via a questionnaire and the food diaries.

Statistics

The results are presented as means with standard deviation (SD) or as percentages. Statistical differences between groups were determined by T-tests, the Mann Whitney U-test, the Chi Square test or Fisher´s exact test, whichever was appropriate. Associations were analysed by linear regression models (the Enter method) adjusted for age and BMI, and the results are presented as standardized beta coefficients (β). P-values less than 0.05 were considered statistically significant. Statistical analyses were carried out using SPSS version 22.0 (SPSS, Inc., Chicago, IL).

Results

Baseline characteristics

In 2015–2016, 79 older (≥65 y) home-dwelling caregivers – 49 females and 30 males – participated in the study (Table 1). The participation rate was 49.7% of all the 159 caregivers aged ≥65 who attended the health screening. The caregivers’ mean age was 73.7 years, and most of them cared for their spouses. They had good cognition (mean MMSE score 27.4) and had good physical functioning according to their ADL and IADL scores. The mean time in the Five Times Sit to Stand Test was 13.8 seconds. The mean hand-grip strength of the dominating hand was 25.8 kg among the females and 39.0 kg among the males. Most of the caregivers were of normal weight (Mean BMI 28 kg/m2). The mean number of medications was 3.9. Their HRQoL was good (15D score 0.9). According to GDS-15, one in ten (10.1%) suffered from mild or moderate depression. The AUDIT results showed that none of the female caregivers had hazardous alcohol use, but 13.3% (n=4) of the males scored >8 AUDIT points, indicating harmful patterns of alcohol consumption, drinking behaviours or alcohol-related problems.

Table 1
Caregivers’ baseline characteristics and nutritional status (MNA)

Differences between the characteristics of the females and males were tested using the Chi Square test or Fisher´s exact test when appropriate, for categorical variables; the Mann Whitney U-test for non-normally distributed continuous variables and Student’s T-test for normally distributed continuous variables;SD= standard deviation; ICD-10 =International statistical classification of diseases and related health problems (28); MNA= Mini Nutritional Assessment (25); BMI= Body Mass Index: recommended BMI for older people 24–29 kg/m2 (29); MMSE= Minimental State Examination: 24–30 normal cognition, 18.24 mild dementia, 10–18 average dementia, 0-10 severe dementia (19); GDS-15= Geriatric Depression Scale: 0–5 points no depression, 6–10 points mild or moderate depression, 11–15 points severe depression (30); 15D-square= Health-related quality of life square: 0= poor quality of life and 1= good quality of life (26); ADL= Activities of Daily living: 0–6 points, higher score indicating better functioning (20); IADL= Instrumental Activities of Daily Living: 0–8 points, higher score indicating better functioning (21); AUDIT= Alcohol Use Disorders Identification Test: total scores of 8 or more are indicators of hazardous and harmful alcohol use, as well as possible alcohol dependence (24)

Nutritional status

Most of the caregivers (79.7%) had a good nutritional status (MNA points >23.5), 19% were at risk of malnutrition (MNA points 17–23.5) and one person (1.3%) already suffered from malnutrition (MNA points <17). The female caregivers were more likely to be at risk of malnutrition than the males (26.5% vs. 6.7%, p=0.026). The MNA test showed that the females suffered more psychological stress or acute illnesses than the males, but the difference was not quite statistically significant (p=0.056). Among the females, energy intake was associated with nutritional status, but the result was just above statistical significance (p=0.056). Energy intake was higher (1707 kcal/d vs. 1418 kcal/d) among the females who were at risk of malnutrition (MNA <23.5 points).
Nutritional status was negatively associated with depression symptoms (GDS-15, p=0.000, β= -0.487): a higher GDS-15 score indicated a lower MNA score. The number of medications was negatively associated with nutritional status (p=0.000, β= -0.452). The association between good HRQoL and nutritional status (15D score, p=0.026, β=0.336) was positive.

Nutrient intakes

The caregivers’ mean energy intake was 1610 kcal/d (Table 2.). A total of 46.8% had an energy intake of under 1500 kcal/d; 26.7% of the males and 59.2% of the females. The males had a higher energy intake than the females (1798 kcal vs. 1494 kcal, p=0.002). Mean protein intake was 69.2 g/d. Although the males had a higher energy intake, they had less protein calculated as energy (E%) than the females (16.6 E% vs. 18.0 E%, p=0.045). Among the male caregivers, a higher total AUDIT score was associated with lower protein intake g/kg IBW/d (p=0.012, β= -0.454). Greater hand-grip strength was associated with a higher protein intake among the males (p=0.031, β=0.433)

Table 2
Baseline results of caregivers’ nutrient intakes, vitamin D supplement use and nutrition-related laboratory tests

Differences between the characteristics of the females and the males were tested using the Chi Square test or Fisher’s exact test when appropriate for categorical variables, the Mann Whitney U-test for non-normally distributed continuous variables, and Student’s T-test for normally distributed continuous variables. The numbers are presented in means with standard deviation (SD) or percentages. Ideal bodyweight was used to calculate protein intake/ kg/d. If caregivers’ BMI was between 20 and 30 kg/m2, actual BMI was used. If BMI was under 20 kg/m2, it was adjusted to 20, and if above 30 kg/m2, it was adjusted to 30; 1) (31); 2) (32); 3) (33); 4) (34)

For ideal bodyweight (BMI 20–30 kg/m2), the mean protein intake was calculated as 1.0 g/kg IBW/d. A total of 79.7% of the caregivers did not consume the recommended protein intake of 1.2 /kg IBW/d; females 77.6% and male 83.3%.
Dietary fibre (mean 19.8 g), folate (mean 208.1 ug/d) and vitamin D (mean 9.3 ug/d) intake was insufficient. A total of 83.5% did not consume the recommended daily intake of dietary fibre, folate (94.9%) or vitamin D (67.1%).

Laboratory tests

The caregivers’ mean serum 25(OH)D levels were 80.8 nmol/l. A total of 73.4% took a vitamin D supplement. The females were more likely to use supplements than the males (81.6 % vs. 60.0%, p=0.035). The use of a vitamin D supplement was related to serum 25(OH) D levels, as the mean vitamin D status was higher among the caregivers who took a supplement (84.7 nmol/l vs. 69.7 nmol/l, p=0.035). Mean haemoglobin was 138 g/l, plasma albumin 37.6 g/l, and serum prealbumin 0.25 mg/l. The males had higher blood haemoglobin than the females (p=0.002). Haemoglobin levels were positively associated with nutritional status (p=0.031, beta=0.259).

Discussion

In this study, most of the older (≥65 y) caregivers had a good nutritional status, according to the MNA. However, every fifth was at risk of malnutrition, and this risk was more likely among the females. Depressive symptoms and medication were associated with decreased nutritional status, and good HRQoL with better nutritional status. The food diaries showed that most of the caregivers had an insufficient protein intake. Intakes of dietary fibre, folate and vitamin D were also low. Among the males, a higher AUDIT score was associated with a lower protein intake, and greater hand-grip strength with a higher protein intake.
The prevalence of nutritional risk among caregivers in this study is in line with that of previous studies, which have found 16%–30% of older caregivers to be at risk of malnutrition (14, 35). This result is interesting, since although the physical performance of the caregivers in our study was good (IADL, ADL), every fifth caregiver was still at risk of malnutrition. Ageing is also accompanied by many cognitive, psychological, and social factors, which may expose older people to inadequate nutrition (11). In this study, depressive symptoms and medication were associated with decreased nutritional status. This result is expected, as depression is believed to be the most common cause of nutritional problems among older people, and the use of medication can affect nutritional status in many ways (36). Caregivers’ good HRQoL was associated with better nutritional status. Previous studies have also found a relationship between HRQoL and the risk of malnutrition (37). Caregivers are greatly exposed to depression and poor mental health, which can increase the risk of inadequate nutrition (8, 9, 38).
The MNA revealed that the female caregivers were more likely to be at risk of malnutrition than the males, as has been found in other studies examining nutrition among older people (39, 40). In this study, the result is not explained by a lower energy intake among the females, because the energy intake of females who were at risk of malnutrition was higher. The MNA showed that the females had more psychological stress or acute illnesses than the males, but the differences were not quite statistically significant. The results still indicate, however, that these gender differences may be explained by psychological factors. Only a few studies have investigated the nutritional status of older caregivers, which indicates the need for further research and more systematic assessments.
In this study, the caregivers’ protein intake was lower (1.0 g/kg IBW/d) than is recommended in Finland; 1.2–1.4 g/kg/d (31). Approximately 80% of the caregivers did not consume the recommended intake of 1.2 g/kg/d, which is a concern. The male caregivers consumed less protein than the female caregivers when calculated as energy, but their protein E% was still in line with the recommendations in Finland; 15–20 E% (31). Adequate protein intake is known to play an important role in the immune system, bone mass density, muscle function, strength, and the management of sarcopenia (17, 41, 42). It is estimated that an intake of 1,2 to 1.6 g/kg BW/d may be required for older people to preserve muscle mass (18, 43). In this study, greater hand-grip strength was associated with a higher protein intake. Adequate protein intake is important for older caregivers, since they need to stay in relatively good physical shape to be able to take care of another person. Increasing protein intake may help maintain muscle strength and help prevent mobility impairment (44). There is a need for preventive nutritional guidance that specifically focuses on increasing the protein intake of older caregivers.
Among the males, a higher AUDIT score was associated with a lower protein intake. AUDIT is a screening tool for alcohol consumption, drinking behaviour, and alcohol-related problems (24). Our result was analysed using the overall AUDIT score, which may not be the proper way to use this test, as the result is usually classified into different risk categories. Moreover, the moderate alcohol consumption in this population meant that we were unable to obtain the same result when alcohol consumption was categorized as 0–7 and >8 AUDIT points. However, the result is still interesting, because it is known that alcohol consumption is related to eating habits (45). Harmful alcohol consumption among older people may accompany nutritional problems, as it replaces the consumption of foods with superior nutritional value (46).
The caregivers had a poor intake of folate and dietary fibre, as found in previous studies among older caregivers (16). These findings indicate a low intake of fruits, vegetables and whole grain products. Stress can affect eating habits and may be shown in the consumption of vegetables. A study by Shaffer et al. (47) found that cancer-related stress was associated with a low consumption of vegetables among cancer-patients and their caregivers. Nutritional guidance can help increase the use of products rich in fibre and vitamins (48). The average vitamin D intake from food was below the recommended level. Still, the caregivers’ mean plasma 25-OH-vitamin D levels were good (80.8 nmol/l) in comparison to the results from the UK National Diet and Nutrition Survey 2008–2012, in which the year-round mean plasma 25(OH)D concentration was 42.5 nmol/l among >65-year-old females (49). The use of vitamin D supplements was related to higher plasma 25-OH-vitamin D levels, which highlights the clinical value of vitamin D supplements among the older population.
The strength of our study is that it provides information regarding the nutritional status and nutrient intake of older caregivers, information that is generally lacking. We used validated methods to assess their nutritional status. The MNA has been validated for older adults (25, 50) and has been used in large populations (51). We also obtained information on caregivers’ nutrient intakes and 25(OH)D levels, which are not usually reported.
Nevertheless, our study has some potential limitations. Due to its cross-sectional nature, causal relationships cannot be drawn from the results. Because of the specifity of our recruitment, the number of participants was small and the study population was selected. This weakens the generalizability of our results to other older caregivers. Selection bias is also possible because the participants were in good physical shape and were keen to participate. This may indicate that they were more health conscious than the average elderly population, and the study results may be more optimistic than in reality. The study population consisted of both females and males, which improved the sample. Some other limitations are related to the measurements. Nutrient intake was studied using three-day food diaries, which can affect the results through over- or under-reporting. This time may not be long enough to show the actual food intake over a longer period. However, we performed check calls to confirm the amounts and types of foods consumed, and it is still noteworthy that the participants had fairly stable food habits, as older people usually do.
Nutritional well-being is a fundamental component of health, physical functioning and quality of life (52). Older caregivers have shown to be prone to malnutrition (16) so they need special support for their nutritional wellbeing.

Conclusion

Our results showed that most of the older (≥65 y) caregivers had good nutritional status, but that one in five was still at risk of malnutrition, especially among the females. Depressive symptoms and medication were associated with decreased nutritional status, and good HRQoL with better nutritional status. A total of 79.7% of the caregivers had a lower protein intake than that recommended. The intake of dietary fibre, folate and vitamin D were also low. Among the males, a greater AUDIT score was associated with a lower protein intake, and greater hand-grip strength with a higher protein intake. These results highlight the need for systematic nutritional assessment among older caregivers and the importance of preventive nutritional guidance. Further studies are required to obtain more information about older caregivers’ nutritional statuses and nutrient intake.

Funding/Support: This study received funding from the National Institute for Health and Welfare (THL) in Finland. The funders played no role in the design, analysis or interpretation of the data or in writing, reporting or deciding whether to submit this article for publication. The authors are independent researchers and are not associated with the funders.

Conflict of interest: The authors declare that they have no conflicts of interest directly relevant to this report. However, Dr Suominen reports co-operating professionally with Nutricia Medical and Verman.

Ethical standards: The Ethics Committee of the Hospital District of Southwest Finland approved the study and participants provided written informed consent.

References

1.   Torres MJ, Dorigny B, Kuhn M, Berr C, Barberger-Gateau P, Letenneur L Nutritional status in community-dwelling elderly in France in urban and rural areas. PLoS One 2014;9:e105137. doi: 10.1371/journal.pone.0105137.
2.   European Foundation for the Improvement of Living and Working Conditions, 2009. Second European Quality of Life Survey. Overview. Luxembourg: Office for Official Publications of the European Communities. http://www.eurofound.europa.eu/pubdocs/2009/02/en/2/EF0902EN.pdf. Accessed 26 January 2017.
3.   Finnish Ministry of Social Affairs and Health, 2014. National informal care development programme, final report. https://www.julkari.fi/bitstream/handle/10024/116146/URN_ISBN_978-952-00-3483-2.pdf?sequence=1. Accessed 26 January 2017.
4.   The Central Association of Carers in Finland, 2015. Am I a Carer? First-Hand Guide to Informal Care. https://www.omaishoitajat.fi/sites/omaishoitaja.asiakas.fi/files/ensiopas_EN_low_3.pdf. Accessed 26 January 2017.
5.   Robards J, Vlachantoni A, Evandrou M, Falkingham J. Informal caring in England and Wales–Stability and transition between 2001 and 2011. Adv Life Course Res 2015;24:21-33. doi: 10.1016/j.alcr.2015.04.003.
6.   Doran T, Drever F, Whitehead M. Health of young and elderly informal carers. BMJ 2003;327:1388. doi: 10.1136/bmj.327.7428.1388.
7.   Schulz R, Martire LM. Family caregiving of persons with dementia: prevalence, health effects, and support strategies. Am J Geriatr Psychiatry 2004;12:240-249.
8.   Sorensen S, Pinquart M, Duberstein P. How effective are interventions with caregivers? An updated meta-analysis. Gerontologist 2002;42:356-372.
9.   Aggarwal B, Liao M, Christian A, Mosca L. Influence of caregiving on lifestyle and psychosocial risk factors among family members of patients hospitalized with cardiovascular disease. J Gen Intern Med 2009;24:93-98. doi: 10.1007/s11606-008-0852-1.
10.   Alzheimer’s Disease International, 2010. World Alzheimer Report. The global economic impact of dementia. http://www.alz.co.uk/research/files/WorldAlzheimerReport2010.pdf. Accessed 6 January 2017.
11.   Suominen MH et al. Working Group Report, State Nutrition Council, Nutrition Recommendations for Elderly. Edita Prima, Helsinki 2010
12.   Guigoz Y, Lauque S, Vellas BJ. Identifying the elderly at risk for malnutrition. The Mini Nutritional Assessment. Clin Geriatr Med 2002;18:737-757.
13.   Guigoz Y. The Mini Nutritional Assessment (MNA) review of the literature–What does it tell us? J Nutr Health Aging 2006;10:466-85; discussion 485-7.
14.   Suominen MH, Puranen T, Jyväkorpi S. Ravitsemus muistisairaan kodissa. Loppuraportti. Suomen Muistiasiantuntijat ry 2013.
15.   Rullier L, Lagarde A, Bouisson J, Bergua V, Torres M, Barberger-Gateau P. Psychosocial correlates of nutritional status of family caregivers of persons with dementia. Int Psychogeriatr 2014;26:105-113. doi: 10.1017/S1041610213001579.
16.   Puranen T. Intervening nutrition among community-dwelling individuals with Alzheimer’s disease and their spouses. University of Helsinki, Faculty of Medicine, 2015.
17.   Wolfe RR. The role of dietary protein in optimizing muscle mass, function and health outcomes in older individuals. Br J Nutr 2012;108 Suppl 2:S88-93. doi: 10.1017/S0007114512002590.
18.   Pedersen AN, Cederholm T. Health effects of protein intake in healthy elderly populations: a systematic literature review. Food Nutr Res 2014;58:10.3402/fnr.v58.23364. doi: 10.3402/fnr.v58.23364.
19.   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. doi: 0022-3956(75)90026-6.
20.   Katz S, Ford AB, Moskowitz RW, Jackson BA, Jaffe MW. Studies of Illness in the Aged. the Index of Adl: a Standardized Measure of Biological and Psychosocial Function. JAMA 1963;185:914-919
21.   Lawton MP, Brody EM. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist 1969;9:179-186
22.   Bohannon RW. Reference values for the five-repetition sit-to-stand test: a descriptive meta-analysis of data from elders. Percept Mot Skills 2006;103:215-222. doi: 10.2466/pms.103.1.215-222.
23.   Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M, Leirer VO. Development and validation of a geriatric depression screening scale. J Psychiatr Res 1983;17:37-49
24.   Saunders JB, Aasland OG, Babor TF, de la Fuente JR, Grant M. Development of the Alcohol Use Disorders Identification Test (AUDIT): WHO Collaborative Project on Early Detection of Persons with Harmful Alcohol Consumption–II. Addiction 1993;88:791-804
25.   Vellas B, Guigoz Y, Garry PJ, Nourhashemi F, Bennahum D, Lauque S, Albarede JL . The Mini Nutritional Assessment (MNA) and its use in grading the nutritional state of elderly patients. Nutrition 1999;15:116-122. doi: S0899-9007(98)00171-3.
26.   Sintonen H. The 15D instrument of health-related quality of life: properties and applications. Ann Med 2001;33:328-336
27.   Roberts HC, Denison HJ, Martin HJ, Patel HP, Syddall H, Cooper C, Sayer AA. A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardised approach. Age Ageing 2011;40:423-429. doi: 10.1093/ageing/afr051.
28.   World Health Organization, 2016. International statistical classification of diseases and related health problems. Available: http://apps.who.int/classifications/icd10/browse/Content/statichtml/ICD10Volume2_en_2016.pdf?ua=1&ua=1. Accessed 14 February 2017
29.   Beck AM, Ovesen L. At which body mass index and degree of weight loss should hospitalized elderly patients be considered at nutritional risk? Clin Nutr 1998;17:195-198. doi: S0261-5614(98)80058-7.
30.   Friedman B, Heisel MJ, Delavan RL. Psychometric properties of the 15-item geriatric depression scale in functionally impaired, cognitively intact, community-dwelling elderly primary care patients. J Am Geriatr Soc 2005;53:1570-1576. doi: JGS53461.
31.   Finnish Nutrition Recommendations. National Nutrition Council. Health from food – The Finnish Dietary Guidelines, 2014.
32.   Nordic Council of Ministers, Nordic Council of Minister, 2012. Nordic Nutrition Recommendations http://dx.doi.org/10.6027/Nord2014-002.
33.   Satakunta Central Hospital laboratory Satadiag, 2017. Research manual. Satahttp://webohjekirja.mylabservices.fi/SataDiag/?fp=1. Assessed 7.2.2017.
34.   Rustad P, Felding P, Franzson L, Kairisto V, Lahti A, Martensson A, Hyltoft Petersen P, Simonsson P, Steensland H, Uldall A. The Nordic Reference Interval Project 2000: recommended reference intervals for 25 common biochemical properties. Scand J Clin Lab Invest 2004;64:271-284. doi: 10.1080/00365510410006324.
35.   Rullier L, Lagarde A, Bouisson J, Bergua V, Barberger-Gateau P. Nutritional status of community-dwelling older people with dementia: associations with individual and family caregivers’ characteristics. Int J Geriatr Psychiatry 2013;28:580-588. doi: 10.1002/gps.3862.
36.   John BK, Bullock M, Brenner L, McGaw C, Scolapio JS. Nutrition in the elderly. Frequently asked questions. Am J Gastroenterol 2013;108:1252-66; quiz 1267. doi: 10.1038/ajg.2013.125.
37.   Jimenez-Redondo S, Beltran de Miguel B, Gavidia Banegas J, Guzman Mercedes L, Gomez-Pavon J, Cuadrado Vives C. Influence of nutritional status on health-related quality of life of non-institutionalized older people. J Nutr Health Aging 2014;18:359-364. doi: 10.1007/s12603-013-0416-x.
38.   Hiel L, Beenackers MA, Renders CM, Robroek SJ, Burdorf A, Croezen S. Providing personal informal care to older European adults: should we care about the caregivers’ health? Prev Med 2015;70:64-68. doi: 10.1016/j.ypmed.2014.10.028.
39.   Cuervo M, Garcia A, Ansorena D, Sanchez-Villegas A, Martinez-Gonzalez M, Astiasaran I, Martinez J. Nutritional assessment interpretation on 22,007 Spanish community-dwelling elders through the Mini Nutritional Assessment test. Public Health Nutr 2009;12:82-90. doi: 10.1017/S136898000800195X.
40.   Wham CA, McLean C, Teh R, Moyes S, Peri K, Kerse N. The BRIGHT Trial: what are the factors associated with nutrition risk? J Nutr Health Aging 2014;18:692-697. doi: 10.1007/s12603-014-0032-4.
41.   Morley JE, Argiles JM, Evans WJ, Bhasin S, Cella D, Deutz NE, Doehner W, Fearon KC, Ferrucci L, Hellerstein MK et al. Nutritional recommendations for the management of sarcopenia. J Am Med Dir Assoc 2010;11:391-396. doi: 10.1016/j.jamda.2010.04.014.
42.   Bauer J, Biolo G, Cederholm T, Cesari M, Cruz-Jentoft AJ, Morley JE, Phillips S, Sieber C, Stehle P, Teta D et al. Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE Study Group. J Am Med Dir Assoc 2013;14:542-559. doi: 10.1016/j.jamda.2013.05.021.
43.   Lancha AH,Jr, Zanella R,Jr, Tanabe SG, Andriamihaja M, Blachier F. Dietary protein supplementation in the elderly for limiting muscle mass loss. Amino Acids 2017;49:33-47. doi: 10.1007/s00726-016-2355-4.
44.   McLean RR, Mangano KM, Hannan MT, Kiel DP, Sahni S. Dietary Protein Intake Is Protective Against Loss of Grip Strength Among Older Adults in the Framingham Offspring Cohort. J Gerontol A Biol Sci Med Sci 2016;71:356-361. doi: 10.1093/gerona/glv184.
45.   Kesse E, Clavel-Chapelon F, Slimani N, van Liere M, E3N Group. Do eating habits differ according to alcohol consumption? Results of a study of the French cohort of the European Prospective Investigation into Cancer and Nutrition (E3N-EPIC). Am J Clin Nutr 2001;74:322-327.
46.   Satre DD, Sterling SA, Mackin RS, Weisner C. Patterns of alcohol and drug use among depressed older adults seeking outpatient psychiatric services. Am J Geriatr Psychiatry 2011;19:695-703. doi: 10.1097/JGP.0b013e3181f17f0a.
47.   Shaffer KM, Kim Y, Llabre MM, Carver CS. Dyadic associations between cancer-related stress and fruit and vegetable consumption among colorectal cancer patients and their family caregivers. J Behav Med 2016;39:75-84. doi: 10.1007/s10865-015-9665-y.
48.   Jyväkorpi S et al. Nutrition education and cooking classes improve diet quality, nutrient intake, and psychological well-being of home-dwelling older people—a pilot study.” J Aging Res Clin 2014;3:120-124
49.   Bates B, Lennox A, Prentice A, et al, 2014. London: Public Health England, Food Standards Agency National Diet and Nutrition Survey Results from Years 1, 2, 3 and 4 (combined) of the Rolling Programme (2008/2009–2011/2012)
50.   Vellas B, Villars H, Abellan G, Soto ME, Rolland Y, Guigoz Y, Morley JE, Chumlea W, Salva A, Rubenstein LZ et al. Overview of the MNA–Its history and challenges. J Nutr Health Aging 2006;10:456-63; discussion 463-5
51.   Kaiser MJ, Bauer JM, Ramsch C, Uter W, Guigoz Y, Cederholm T, Thomas DR, Anthony PS, Charlton KE, Maggio M et al. Frequency of malnutrition in older adults: a multinational perspective using the mini nutritional assessment. J Am Geriatr Soc 2010;58:1734-1738. doi: 10.1111/j.1532-5415.2010.03016.x.
52.   Phillips MB, Foley AL, Barnard R, Isenring EA, Miller MD. Nutritional screening in community-dwelling older adults: a systematic literature review. Asia Pac J Clin Nutr 2010;19:440-449

NUTRITIONAL CHALLENGES FOR THE FAMILY CAREGIVER AND PERSON WITH DEMENTIA DYAD

E. Beattie^1,2, J. McCrow1,², C. Dyce³, E. Fielding², E. Isenring^3,4

1. Institute of Health and Biomedical Innovation, Brisbane, Queensland, Australia; 2. School of Nursing, Queensland University of Technology, Queensland, Australia; 3. Centre for Dietetics Research, School of Human Movement Studies, University of Queensland, Brisbane, Queensland, 4072, Australia; 4. Department of Nutrition and Dietetics, Princess Alexandra Hospital, Woolloongabba, Queensland

Corresponding Author: Elizabeth Beattie, School of Nursing, 6th floor, N Block, Queensland University of Technology, Kelvin Grove QLD 4059 Australia, elizabeth.beattie@qut.edu.au, Tel: +61 7 3138 3847, Fax: +61 7 3138 5941

Abstract

Background: The majority of people with dementia live at home until quite late in the disease trajectory, supported by family caregivers who typically take increasing responsibility for providing nutrition. Caregiving is highly stressful and thus both dyad partners are at risk of nutritional issues. Objective: This study evaluated the nutritional status of both dyad members and the associations between these. Design: Descriptive, correlational. Setting: Community. Participants: 26 dyads of persons with dementia and caregivers. Measurements: The nutritional status of each dyad member was evaluated at home using a comprehensive battery of measures including the Mini-Nutritional Assessment, Corrected Arm Muscle Area and a 3-day food diary. Stage of dementia and functional eating capacity was measured for the person with dementia. Caregivers completed a brief burden scale. Result: Of those with dementia (n = 26), a large proportion had nutritional issues (one was malnourished and another 16 were at risk). Six of the caregivers were at risk of malnutrition. In addition, fifteen of the people with dementia did not meet their recommended daily energy requirements. A moderate and significant positive correlation between functional eating skills and nutritional status (MNA score) among participants with dementia was found (r = .523, n = 26, p = .006). Conclusion: These findings suggest that a dyadic perspective on nutritional status provides important insights into risk in this vulnerable group. Specifically, monitoring of the functional eating independence skills of the person with dementia is critical, along with assisting caregivers to be aware of their own eating patterns and intake.

Key words: Dementia, nutritional status, caregiver, community, malnutrition.

Introduction

Poor nutritional status in the elderly population is an important predictor of morbidity and mortality (1). For older people living with dementia nutritional status is particularly important, given strong evidence that weight loss is associated with dementia, particularly Alzheimer’s Disease (2). An estimated 35.6 million people worldwide live with dementia, a number expected to double by 2030 and more than triple by 2050 (3). Dementia is considered to be a leading cause of dependency and disability among older people internationally (3).

Weight loss in persons with Alzheimer’s Disease begins up to six years prior to the diagnosis of dementia and accelerates one to two years before the onset of cognitive symptoms (2). This unintentional weight loss contributes to an increased risk of frailty, immobility, illness and premature morbidity (4). For people with dementia in whom adequate nutrition is not maintained, weight loss and malnutrition may occur in excess of that resulting from the disease process alone (5, 6). Protein- energy malnutrition, common among frail elders, is defined as insufficient dietary intake leading to an inadequate nutritional status, weight loss, and muscle wasting (1).

To date nutrition research has predominantly focused on the nutritional status of the person with dementia with more known about those living in residential care than in the community. However, the majority of people with dementia continue to live at home until quite late in the disease trajectory, supported by family caregivers, with caregivers typically taking increasing responsibility over time for food choices for the person with dementia as well as themselves. Typically the level of support required increases as the disease progresses (2).

Recent theoretical work has generated a concept analysis and model of mealtime difficulties in people with dementia, from an examination of 48 literature sources, again primarily from residential care settings (7). Important antecedents and attributes of mealtime difficulties include social and cultural factors, eating abits, mealtime patterns, environment, cognitive status and dyad interaction. As the extent of assistance needed increases, the associated impact on the caregiver as well as the person with dementia is significantly increased.

Given that caring for a person with dementia is highly stressful, and is associated with physical and emotional burden (8) and poor nutrition (9, 10), it is important to understand more about the nutritional status of both the caregiver and the person with dementia within the dyadic relationship. Previous observational research has shown that caregivers eat fewer than two meals per day however little is known about the actual nutritional status of family caregivers (11).

Collectively these findings support the need for further research investigating dyadic nutritional status as potentially there may be some evolving dyadic nutritional profiles. This descriptive, cross-sectional study reports on the nutritional status of community-dwelling people with dementia and their family caregiver, addressing this gap.

Specifically, our research questions were:

What is the nutritional status and dietary intake (and associations between these) of community-dwelling dyads of caregivers and people with dementia?
What associations exist between level of cognitive impairment and nutritional status for the person with dementia?

It was hypothesized that both family caregivers and the person with dementia would be at risk of nutritional issues and there would be a dyadic nutritional relationship.

Methods

Participants

The participants were community-dwelling people with dementia and their adult family caregivers, located in South East Queensland, Australia. Potential participants were initially identified through a variety of mechanisms including: community home care workers, respite centre managers/coordinators and multimedia advertisements. Inclusion criteria were: care recipient and the caregiver relative living in the same household; person with dementia aged 55+ with a diagnosis of dementia and independently ambulating. To be eligible the caregiver must have reported that they prepared at least ten meals per week for their relative. People with dementia were excluded if they had a concurrent disease, such as cancer, causing unintentional weight loss.

Approval for this project was obtained from the Human Research Ethics Committees of all relevant universities, health districts and facilities. Written informed consent for participation was provided by the participants and/or the responsible relative or legal guardian.

Measures/ instruments

All participants completed an assessment battery including a demographic questionnaire.

For both dyad members

Nutritional status was assessed using the Mini Nutritional Assessment [MNA] (12).

Body weight and fat and fat-free mass were assessed using electronic Tanita scales.

Corrected Arm Muscle Area [CAMA], an indicator of nutritional status in terms of body protein and fat stores, was calculated from mid-upper arm circumference and tricep skin fold [TSF]. Triplicate TSF measurements (to the nearest 0.2mm) were made using a standard procedure (Harpenden calipers) (13).

A 3-day food diary was recorded by the caregiver on two week days and one weekend day (14). Due to the cognitive decline issues in this group, it was decided that dietary intake assessment methods relying on recall were not the best choice. In addition 3-day diet diary has been shown to be valid and acceptable for this older age group (15). Participants utilized a simple instruction booklet developed by the study dietician for recording food and fluid type with specified portions. Experienced RAs assisted the caregiver with checking and completing the diaries. When participants did not list all details, some common assumptions were used, such as: generic products were selected when no product brand was recorded; preparation of common meals were assumed when details were not specified (such as sandwiches, stews and curries); and portion sizes were based on previous meals when not recorded in detail.

For the person with dementia

Global cognitive status was quantified using the Mini- mental Status Exam [MMSE] (16). The MMSE yields a global performance score (maximum 30) from eleven, absolute anonymity & fast. items measuring orientation, registration, attention and calculation, recall, language and construction tasks.

Stage of dementia was assessed using the Clinical Dementia Rating Scale [CDR] (17), completed by the caregiver.

Functional self-eating skill of the person with dementia was assessed using the Eating Behavior Scale [EBS] over three meal times. This six item scale measures self-eating in five dimensions, with a total score of 18: attention to meal; ability to locate food; use of utensils; biting, chewing and swallowing, and ending the meal (18).

For the Caregiver only

Pearlin’s four-item scale was used to assess the strain (burden) of caring for someone with dementia (e.g. you are exhausted when you go to bed at night). Caregivers rated each item on a 4-point scale from 1 (not at all) to 4 (completely) (19).

Procedures

Following informed consent, dyads were mailed a package with several of the instruments to be filled out in their own time. Other instruments were collected face-to- face during a 90-minute home visit by two research assistants. At this visit, anthropometrics (height and weight) were taken and household measuring implements (cups, spoons, liter jug, electronic food scale) were left for the caregiver to complete the three-day food and fluid diary. A follow-up phone call was made with each caregiver to answer any emerging questions they may have had about completing the food and fluid diary.

Statistical Analyses

All analyses were performed using the Statistical Package for the Social Sciences (SPSS) version 21. Daily mean protein and energy content was calculated from the three-day record using Australian food composition data (Food Works Professional version 7, Xyris software, Brisbane). Percentages of estimated energy and protein requirements met [EER and EPR] for each participant were calculated using a conservative value of 114kJ/kg (26kcal/kg) and 0.9g/kg of body weight. Global CDR was derived from the scores following the original CDR guidelines (17).

Descriptive statistics were used to summarize characteristics of the sample and frequency calculations were used to summarize the categorical validation response variables. Pearson correlations were used to test the following associations: within person between nutritional status and energy and protein intake; for the person with dementia between nutritional status and cognitive status and functional eating status; and within- dyad between the nutritional status of caregiver and person with dementia. Statistical significance was at the standard P

Results

A total of 32 dyad participants responded to our recruitment requests. Of these, one was excluded because of the advanced state of dementia, two dyads declined to participate, two failed to return consent forms and one dyad withdrew because of a serious medical event. A sample of 26 dyads was included in the final analyses.

The spouse of the person with dementia (n = 21) was the most reported caregiver relationship, with other family members including grandchildren and children making up the rest of the sample. The median time of care-giving was 51 months (range 7-156 months). However, most caregivers (n = 21) had been formally caring for the person with dementia for three years or longer.

The type of dementia for half of the participants was Alzheimer’s (n = 13), with five having vascular, one having Lewy body and one early onset (the remaining six were unsure as to specific type). Results from the CDR indicated that participants were in the following stages of dementia: eleven mild, eight moderate, and three severe, with four having questionable dementia.

In terms of caregiver burden, the mean score was 9 out of a maximum of 16. The most frequently reported strain was that they were “exhausted when they went to bed at night”—half (13 out of 26) answered ‘quite a bit’ or ‘completely.’ In addition, eleven caregivers chose one of those two categories for “did not have time just for themselves.” Other demographic and clinical characteristics of the participants are presented in Table 1.

Table 1: Characteristics of the Participants

MMSE = The Mini Mental State Examination; BMI = Body Mass Index; FFM = Fatfree
Mass; CAMA = Corrected Arm Muscle Area; MNA = Mini-Nutritional Assessment

Question one: Nutritional status and dietary intake

Results from the MNA indicated that one of the people with dementia was malnourished and 16 (out of 26) were at risk of malnutrition. None of the caregivers were identified as malnourished, while six were at risk of malnutrition. Figure 1 displays the distributions of the nutritional profiles of the participants as measured with the MNA. When assessing the dyad nutritional status, again with MNA, results indicated that four of the dyads were both at risk of malnutrition and seven were both well nourished. For the remaining, two dyads had only the caregiver at risk of malnutrition, while only the person with dementia was at risk in half (n = 13) of the sample (see Figure 2).

Figure 1: Nutritional Profiles of Participants. MNA indicator scores: less than 17 points = malnourished; 17 to 23.5 points = at risk of malnutrition; 24 to 30 points = normal nutritional status.

Figure 2: Nutritional Status of Dyad.

Of the total sample, one dyad could not complete the three day food diary due to comprehension difficulties. Of the caregiver participants, the mean reported daily energy and protein intake was 8300 kJ (± 2000) and 80g (±

30) respectively (Table 1). The dementia sample reported a mean daily energy intake of 7700 kJ (± 2700) and a mean protein intake of 80g (± 29). Of the caregiver sample, nine participants did not meet their EER and six participants did not meet their EPR. Fifteen (of 26) of the participants with dementia did not meet their EER and nine did not meet their EPR.

In assessing whether there was a relationship between the nutritional status of the caregiver and the person with dementia within a dyad, bivariate tests were computed for each variable. The only two nutritional variables showing a significant within-dyad association was for the percent of EER (and the percent of EPR) met by the diary food intake of the caregiver and the person with dementia (EER: r = .463, n = 25, p = .020; EPR: r = .514, n = 25, p = .009).

There was a moderate positive relationship between CAMA scores and protein intake in the caregiver sample (r = .41, n = 25, p = .043) and between CAMA and energy (r = .45, n = 25, p = .025) and CAMA and protein (r = .40, n = 25, p = .046) among the people with dementia. There were no statistically significant relationships between MNA scores and protein and energy intake for either group. Similarly, none of the relationships between meeting EER and EPR and CAMA and MNA status were statistically significant. However, among the participants with dementia, the correlation between functional eating skills and nutritional status (MNA score) was positive, moderate in size and significant (r = .523, n = 26, p =.006).

Question two: relationship between cognitiveimpairment and nutritional status

For the people with dementia Pearson’s r was computed to assess the relationship between MNA scores and level of cognition as rated by the MMSE. There was no significant correlation between the two variables (r =.26, n = 26, p = .206).

Discussion

Summary of key findings

This study provides a description of the nutritional status of community-dwelling dyads of people living with dementia and caregivers. In the community, 15% of older people are at risk of malnutrition with an additional 5-30% being malnourished (1, 20). The striking finding in this study was the very high (16 of 26) proportion at risk of malnutrition among the participants with dementia compared to normative rates in the non-caregiver non- dementia diagnosed population with a similar age profile (21). In addition, almost a quarter of family caregivers (n = 6) presented as at risk of malnutrition. These results are in line with the small number of existing studies of community-dwelling people with dementia. In the only other study (n = 56) to look at dyads, Rullier et al (2012) found a similar prevalence (59%) of people with dementia being at risk of malnutrition, but a higher prevalence (23%) being malnourished (22). In Rullier et al’s sample, more of the family caregivers displayed nutritional issues; nearly a third (32%) were at risk of malnutrition while 5% were malnourished. Two other studies examined only people with dementia; a large study (n = 940) resulted in quite similar malnutrition prevalence rates to the current study (5% malnourished and 43% at risk) (23) and a smaller study (n = 49) identified 43% of dementia participants as malnourished or at risk (24).

Our study found an alarmingly high prevalence of suboptimal protein and energy consumption, especially in people with dementia. Because our estimates of energy and protein requirements were conservative (0.9kg/kg) these results are likely to underreport the percentage of subjects meeting actual requirements (i.e. if 1.2g/kg had been used). These results largely support current literature, which infers that poor dietary intake is prevalent among older people with cognitive impairment (25). Energy and protein are vital nutrients and key to the maintenance of health in older adults.

An important association linking eating behavior disturbances and the risk of malnutrition is highlighted by this study. Our results indicate diminished independence of eating behaviors is strongly related to the risk of malnutrition. Those participants whose dementia most affected their eating abilities also tended to be at most risk of malnutrition. Many studies have investigated the role of nutrition on global functioning, showing an important association between malnutrition and functional decline (25). Cognitive disorders commonly influence the individual’s ability to function independently (26).

There are a number of risk factors that have been suggested to contribute to nutritional outcomes of people living with dementia, including severity of cognitive impairment and the timing of the formal dementia diagnosis (25). Conversely, Rullier et al (2012) found no association between malnutrition and cognitive severity (22), as in our results. Rullier et al hypothesized that it is primarily the role of specific activities of daily living affected by the trajectory of the disease and not solely diminished cognitive impairment that impacts nutritional status. Our sample comprised a wide range of cognitive impairment, and the diversity in individual symptoms and characteristics could also explain the results.

Implications for clinical practice

Our results suggest this vulnerable population would benefit from systematic dietary assessment and intervention to prevent further inadequacy in dietary intake and increased nutritional risk, consistent with recommendations by Shatenstein, Kergoat & Reid (2007) (25). Simple nutritional screening can help identify not only people with dementia at nutritional risk but their co- dwelling caregivers with similar risk. A comprehensive appraisal of the level of independence of the person with dementia in the context of eating behaviors is particularly important. Prioritizing eating behavior autonomy, and evaluating when and how to provide eating assistance, may prove to be the most effective intervention to maintain nutritional status of the caregiving dyad. Caregivers and dietetic professionals need to be aware that dyads are at particularly high risk of suboptimal protein and energy intake and that focusing only on the person with dementia or only on the caregiver may provide a limited view of the situation. Keller et al (2007) argues that the interactions among the caregiving dyad during the feeding-related activities, including mealtimes, are central to the nutritional status of both members of the dyad. This underlines the importance of not only assessing eating behavior autonomy, but highlights that for the most effective nutritional interventions a multi-faceted approach that prioritizes eating autonomy may offer the most productive outcome.

Limitations and directions for future research

The relatively small sample size is a primary limitation of this study. However since this is only the second published study of dyads found in the literature, it provides important insights into the challenges of dyad recruitment and measurement in nutrition-focused dementia studies. Future research needs to explore the role of specific symptoms associated with cognitive impairment and caregiver challenges that may contribute to increased risk of poor nutritional outcomes. Increased knowledge of how dyads operate at home at mealtimes and how food is decided upon, prepared and shared is also important in understanding the dynamics of malnutrition in these vulnerable pairs. This, in turn, may allow for the development of more effective interventions to delay or prevent malnutrition.

Not only are persons with dementia at high risk of malnutrition but also their co-dwelling caregivers. It is evident that this population is at risk of suboptimal energy and protein intake and therefore and that those caregivers need to be mindful of their own vulnerability to nutritional issues.

Acknowledgements: The authors would like to acknowledge the 26 caregiver- person with dementia dyads that freely gave their time to participate in this study. Recruitment would not have succeeded without the assistance of the many aged care providers involved. In addition, able research assistance was provided by Joan Connor, Daniel Lee, and Margaret MacAndrew.

Funding: This project was funded the Alzheimer’s Australia Hazel Hawke Research Grant in Dementia Care. The sponsors had no role in the design and conduct of the study; in the collection, analysis, and interpretation of data; in the preparation of the manuscript; or in the review or approval of the manuscript.

References

Watterson C, Fraser A, Banks M, et al. Evidence based practice guidelines for the nutritional management of malnutrition in adult patients across the continuum of care. Nutr Diet 2009; 66:S1-S34.
Johnson DK, Wilkins CH, Morris JC. Accelerated weight loss may precede diagnosis in Alzheimer disease. Arch Neurol 2006; 63:1312- 7.
World Health Organization. Dementia: A public health priority. 2012. Geneva: WHO.
White H, Pieper C, Schmader K. The association of weight change in Alzheimer’s disease with severity of disease and mortality: a longitudinal analysis. J Am Geriatr Soc 1998; 46:1223- 7
Morley JE. Dementia is not necessarily a cause of undernutrition. J Am Geriatr Soc 1996; 44:1403-4.
Franzoni S, Frisoni GB, Boffelli S, Rozzini R, Trabucchi M. Good nutritional oral intake is associated with equal survival in demented and nondemented very old patients. J Am Geriatr Soc 1996; 44:1366-70.
Aselage MB, Amella EJ. An evolutionary analysis of mealtime difficulties in older adults with dementia. J Clin Nurs 2010; 19:33-41.
Vitaliano PP, Young HM, Zhang J. Is caregiving a risk factor for illness? Curr Dir Psychol Sci 2004; 13:13-6.
Mujuru NG. The psychosocial impact of care-giving on the family caregivers of chronically ill AIDS/HIV patients in home based care. 2010. Master’s Thesis: University of the Witwatersrand, Johannesburg.
Branscum A. Stress and coping model for family caregivers of older adults. 2010. Dissertation: University of Iowa.
Rabinowitz YG, Gallagher-Thompson D. Health and health behaviors among female caregivers of elderly relatives with dementia. Clin Gerontologist 2007; 31:1-15.
Guigoz Y, Vellas B, Garry P. Mini Nutritional Assessment: a practical assessment tool for grading the nutritional state of elderly patients. In: Vellas B, Guigoz Y, Garry P, Albarede J (eds) The mini nutritional assessment: MNA. Nutrition in the elderly. 1997. Paris, Serdi, pp 15-60.
Friedman PJ, Campbell JA, Caradoc-Davies TH. Prospective trial of a new diagnostic criterion for severe wasting malnutrition in the elderly. Age Ageing 1985; 14:149-54.
Gibson RS. Principles of nutritional assessment 2nd ed. 2005. Oxford USA, Oxford University Press.
Rothenberg E. Experience of dietary assessment and validation from three Swedish studies in the elderly. Eur J Clin Nutr 2009; 63:S64-8.
Folstein M, Folstein S, McHugh P. “Mini-Mental State”: A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12:189-98.
Morris JC. Clinical dementia rating: a reliable and valid diagnostic and staging measure for dementia of the Alzheimer type. Int Psychogeriatr 1997; 9:173-6.
Tully MW, Matrakas LK, Muir J, Musallam K. The Eating Behavior Scale. A simple method of assessing functional ability in patients with Alzheimer’s disease. J Gerontol Nurs 1997; 23:9-15.
Pearlin LI, Mullan JT, Semple SJ, Skaff MM. Caregiving and the stress process: An overview of concepts and their measures. Gerontologist 1990; 30:583-94.
Leggo M, Banks M, Isenring E, Stewart L, Tweeddale M. A quality improvement nutrition screening and intervention program available to Home and Community Care eligible clients. Nutr Diet 2008; 65:162-7.
Rist G, Miles G, Karimi L. The presence of malnutrition in community-‐living older adults receiving home nursing services. Nutr Diet 2012; 69:46-50.
Rullier L, Lagarde A, Bouisson J, Bergua V, Barberger-‐Gateau P. Nutritional status of community-‐dwelling older people with dementia: Associations with individual and family caregivers’ characteristics. Int J Geriatr Psychiatry 2013; 28: 580-8.
Roqué M, Salva A, Vellas B. Malnutrition in community-dwelling adults with dementia (Nutrialz trial). J Nutr Health Aging 2013; 17:295-9.
Spaccavento S, Del Prete M, Craca A, Fiore P. Influence of nutritional status on cognitive, functional and neuropsychiatric deficits in Alzheimer’s disease. Arch Geront Geriatr 2009; 48:356-60.
Shatenstein B, Kergoat M-J, Reid I. Poor nutrient intakes during 1-year follow-up with community-dwelling older adults with early-stage Alzheimer dementia compared to cognitively intact matched controls. J Am Diet Assoc 2007; 107:2091-9.
Del Parigi A, Panza F, Capurso C, Solfrizzi V. Nutritional factors, cognitive decline, and dementia. Brain Res Bull 2006; 15; 69:1-19.