Attention,Praxis,and Reasoning Are Associated with Risk of Undernutrition in Older People with Cognitive Impairment

Abstract

Background:

Dementia is a risk factor for undernutrition. However, it is not clear if specific cognitive deficits have a higher risk of undernutrition and how much appetite/nutritional problems and caregiver stress mediate this association.

Objective:

To evaluate the relationship between nutritional status and severity of global and function-specific scores of cognitive dysfunctions, and to which extent this association is mediated by appetite/nutritional problems and caregiver stress.

Methods:

Cross-sectional analysis of the ReGAl study data, including 761 older adults attending a Memory Clinic. Nutritional status was evaluated with Mini Nutritional Assessment (MNA). The relationship between scores at neuro-cognitive tests and risk of undernutrition was evaluated using logistic regression models adjusted for potential confounders. To allow comparison between different tests, all scores were standardized. Mediation analysis was used to evaluate how much appetite/nutritional problems and caregiver stress mediate this association.

Results:

Mean age was 77 years (SD: 9), 37.3% were women. Exploring different cognitive domains, a stronger association was documented for attentive matrices (OR:0.49, 95% CI: 0.34–0.72), the figure copy test (OR:0.63, 95% CI: 0.45–0.88), and the verbal judgement test (OR:0.61, 95% CI: 0.42–0.91). The proportion of the effect of cognition (MMSE) on nutritional status mediated by caregiver distress was 9.5% (95% CI: 0.002–0.27), the proportion mediated by appetite/nutritional problems was 11% (95% CI: –4.8–3.18).

Conclusion:

Risk of undernutrition is associated to cognitive decline; a stronger association was observed for attention, praxis, and reasoning. Caregiver distress is a mediator of this association. This information should be considered in the management plans of this population.

Keywords

Appetite alteration caregiver burden dementia malnutrition Mini Nutritional Assessment

INTRODUCTION

The number of people currently living with dementia in Europe is almost 9.8 million and almost one in every 20 people over the age of 65 has Alzheimer’s disease (AD), the most common form of dementia [1, 2].

Dementia is a risk factor for undernutrition [3], and unintentional weight loss may be considered a hallmark of AD even at its early stages, leading to severe complications such as muscular atrophy and loss of independence [4, 5].

It is unknown whether the nutritional risk in AD is due to higher energy expenditure, reduced dietary intake, or a combination of both, and what is the influence of other factors (e.g., interaction with caregivers). Dietary intake is partly driven by olfactory and gustatory functioning and food preferences [6], and subjects with mild cognitive impairment or AD have difficulties in discriminating and identifying odors. It has been reported that this sensory impairment is directly associated to dementia severity [7 –9]. Nonetheless, current available literature shows no differences between AD and cognitively healthy subjects with respect to energy intake or energy expenditure [10]; actually, food choice and dietary pattern of people with and without dementia seem comparable [11].

Other factors may play a key role in the nutritional status among people with dementia. Feeding difficulties and changes in eating and dietary habits may be secondary to apraxia, as cortical function decline decreases patient’s ability to obtain adequate nutrition, and malnutrition risk seems to be different according to different types of dementia [12], suggesting that specific cognitive domains impairment, implicated in feeding, might be associated with a higher risk of undernutrition. Very few studies are available on this topic, documenting that executive disfunction is associated with an impairment of oral intake [13], and that attention, language and visuospatial ability are associated with a higher risk of undernutrition in patients with dementia [14].

Among nursing home residents, the importance of staff-resident (dyadic) interactions during mealtime is acknowledged [15 –18] and is considered an important modifiable factor to manage mealtime difficulties and promote intake; in particular, food intake seems to be promoted by dyadic verbal interactions [17]. Also, in the community setting, poor nutritional status may be the result of insufficient care due to a heavy burden for family caregivers who may be stressed, depressed, and socially isolated [19]. Actually, the risk of undernutrition of people with dementia, evaluated using the Mini-Nutritional Assessment (MNA), is associated with the MNA of their caregiver [20]; furthermore, the nutritional status of older people with dementia is associated with burden of family caregivers and can be worsened by physical and psychological difficulties experienced by the caregivers themselves [21, 22]. However, these studies evaluated the association between nutrition and caregiver burden among older adults with dementia, but there are no studies that analyze the role of caregiver distress as a mediator of the relationship between cognitive impairment and nutritional status.

Given this body of evidence, the risk of undernutrition may be associated with specific cognitive deficits; in particular, we hypothesized that an impairment of memory, attention, visual attention, executive and praxic abilities may affect the ability of the patient conceive and realize the idea of eating. Furthermore, we also hypothesized that this relationship may be affected by appetite/nutritional problems and caregiver stress. The aim of this study was to evaluate the relationship between nutritional status and severity of global and function-specific scores of cognitive dysfunctions, and to evaluate to which extent the effect of cognitive dysfunction on nutritional status is mediated by appetite/nutritional problems and caregiver stress.

METHODS

Study population

We used data from the Italian Geriatric Network on Alzheimer’s disease (Rete Geriatrica Alzheimer - ReGAl) project, a longitudinal multicentric study promoted by the Italian Society of Gerontology and Geriatrics (Società Italiana di Gerontologia e Geriatria, SIGG). The project has been described extensively elsewhere [23]. Briefly, it included all the older adults attending Memory Clinics in multiple centers in Italy, and recorded data routinely collected during the clinical workup, including demographic characteristics, medical history, pharmacological treatments, and clinical and neurological examination and a neuropsychological evaluation. Subjects with clinically severe psychiatric or systemic disease, intellectual disability, and severe sensory impairment (blindness, deafness) were excluded. The diagnosis of dementia was based on DSM-IV [24] and on Petersen’s criteria [25] for mild cognitive impairment. AD was diagnosed according to the NINDS-ADRDA criteria [26], vascular dementia on the NINDS-AIREN criteria [27], frontotemporal dementia on those described by Neary et al. [28], dementia with Lewy bodies on those by McKeith et al. [29], and Parkinson’s disease dementia according to Emre et al. [30]. The severity of dementia was rated by the Clinical Dementia Rating scale (CDR) [31]. For the present study, we included only patients attending the Memory Clinic of University of Perugia due to several missing of variables of interest in the other centers, and we only used baseline data. All the patients signed a written informed consent to participate to the study. The study was approved by the Ethic Committee of the University of Perugia (n. 2773/16).

Cognitive status

From the tests included in the database, for the present study we took into account the Mini-Mental State Examination (MMSE) [32], as test of general cognition, the immediate and delayed recall of the Rey’s Auditory Verbal Learning Test, as a test for episodic memory, the backward digit-span test and attentive matrices for attention, the Clock Drawing Test for executive abilities, the figure copy test for praxis, the Corsi block-tapping test for visuo-spatial working memory, the Token test for language, and the verbal judgment test for reasoning. For each test, details on administration procedures and Italian normative data for score adjustment for age and education as well as normality cut-off scores (95% of the lower tolerance limit of the normal population distribution) are available [33 –35].

Current depressive symptoms were assessed by the 15-item version of the Geriatric Depression Scale [36]. Appetite and nutritional problems were definite on the basis of the relevant item of the Neuro-psychiatric Inventory (NPI) Questionnaire. Also caregiver stress was evaluated using the NPI [37].

Nutritional status

Nutritional status was assessed using the Mini Nutritional Assessment (MNA), that has been extensively validated in older people, including those with cognitive impairment [38]. The maximum score of the MNA is 30, scores between 17 and 23.5 points indicate nutritional risk and scores below 17 indicate overt undernutrition.

Statistical analysis

The sample was divided in four groups based on their CDR score: no dementia (0 points), very mild impairment (0.5 points), mild impairment (1 point) and moderate/severe impairment (≥2 points) [31]. The distribution of all continuous variables was visually inspected using histograms and quantile-quantile plots to check for substantial deviation from the normal distribution. Given the small number of patients with overt undernutrition, we analyzed them in the group of patients at risk of undernutrition. Group characteristics were compared using descriptive statistics (mean and standard deviations for numerical variables, proportion for categorical variables). We explored the distribution of MNA by dementia subtype and by severity of dementia using bar plots. Comparison between groups was performed using the chi-square test.

To study the association between cognitive performance test scores and risk of undernutrition, we excluded patients without dementia at the CDR. This association was evaluated using logistic regression models, both unadjusted and adjusted for age, sex, education, presence of caregiver, reported changes in appetite/eating, and caregiver stress. To allow comparison between different tests, all scores were standardized by centering (subtracting the mean) and rescaling (dividing by SD), thus the ORs express the changes in the dependent variable for a 1 SD change in the independent variable. To evaluate to which extent the effect of cognitive function on nutrition is mediated by appetite and nutritional problems or caregiver stress we used mediation analysis, that allows to break down the effect of an independent variable on a dependent variable into a “average direct effect” and an “average causal mediation effect”, that is the amount of effect that is mediated by a third variable considered in the model [39].

Analyses were performed using R version 3.5.0 (R Foundation for Statistical Computing, Vienna, Austria).

RESULTS

We included 761 participants with a mean age of 77 years (SD: 9); 37.3% were women and 95.3% have a study partner. Twenty-two percent of the participants was affected by mild cognitive impairment, 18% by AD dementia, 14% by mixed dementia, 12% by depression with cognitive impairment (Fig. 1). CDR classified as without dementia 244 patients, 210 as very mild impaired, 199 as mild impaired, and 92 as moderate or severe impaired. The mean MNA score in the four groups was 25.7 (SD: 2.0), 24.2 (SD: 2.5), 23.6 (SD: 2.2), and 21.9 (SD: 2.9), respectively (Table 1). Other characteristics of the groups are reported in Table 1.

Fig. 1

Distribution of dementia subtypes.

Table 1

General characteristics of the sample according to cognitive function

	No dementia N: 244 Mean (SD) or N (%)	Very mild impairment N: 210 Mean (SD) or N (%)	Mild impairment N: 199 Mean (SD) or N (%)	Moderate/Severe impairment N: 92 Mean (SD) or N (%)
Age	71.9 (11.3)	77.9 (6.2)	81.1 (6.5)	81.4 (6.3)
Gender (woman)	149 (61.1%)	117 (55.7%)	133 (66.8%)	69 (75.0%)
ADL score	5.4 (0.9)	5.3 (0.9)	4.7 (1.3)	3.0 (1.6)
IADL score	6.6 (1.8)	5.1 (2.3)	3.0 (2.0)	0.9 (1.1)
GDS score	4.4 (3.3)	5.3 (3.4)	5.5 (3.1)	6.1 (3.7)
Lives with family member	113 (71.5%)	108 (77.1%)	86 (69.4%)	43 (74.1%)
Lives alone	36 (22.8%)	28 (20.0%)	33 (26.6%)	5 (8.6%)
Lives with another person	9 (5.7%)	4 (2.9%)	5 (4.0%)	10 (17.2%)
Education: 5th grade	30 (19.0%)	76 (54.3%)	81 (65.3%)	49 (84.5%)
Education: 8th grade	83 (52.5%)	47 (33.6%)	31 (25.0%)	8 (13.8%)
Education: higher	45 (28.5%)	17 (12.1%)	12 (9.7%)	1 (1.7%)
Hospital admission in the last year	57 (24.3%)	16 (7.8%)	16 (8.2%)	8 (8.8%)
Distress score	3.5 (3.8)	5.4 (4.7)	6.7 (5.8)	8.8 (6.8)
Nutritional/appetite problems	9 (9.2%)	18 (11.0%)	32 (17.6%)	20 (24.4%)
Mini Nutritional Assessment	25.7 (2.0)	24.2 (2.5)	23.6 (2.2)	21.9 (2.9)

ADL, activities of daily living; GDS, Geriatric Depression Scale; IADL, instrumental activities of daily living.

Less than 10% of participants without cognitive impairment were at risk of undernutrition, while it arises up to 24% for mild cognitive impairment, to 44% for AD dementia, and 50% for mixed dementia (p < 0.001) (Fig. 2). Considering dementia severity, the proportion of patients with undernutrition increases with the severity of dementia, from <20% in participants without dementia to >60% in those with moderate-severe dementia (Fig. 3).

Fig. 2

Distribution of risk of malnutrition according to dementia subtypes.

Fig. 3

Distribution of risk of malnutrition according to dementia severity.

MMSE score was inversely associated with risk of undernutrition (standardized OR 0.64, 95% CI 0.53–0.77), as also Clock Drawing Test (standardized OR 0.68, 95% CI 0.56–0.82), backward digit span (standardized OR 0.74, 95% CI 0.6–0.91), Auditory verbal learning test (AVLT) delayed (standardized OR 0.76, 95% CI 0.6–0.96), attentive matrices (standardized OR 0.54, 95% CI 0.43–0.68), figure copy test (standardized OR 0.64, 95% CI 0.52–0.79), Token test (standardized OR 0.94, 95% CI 0.91–0.98), and verbal judgement test (standardized OR 0.98, 95% CI 0.96–0.99). Adjustment for potential confounders, however, reduced the estimated effect of cognitive function on nutritional status, except for attentive matrices (standardized OR 0.49, 95% CI 0.34–0.72), figure copy test (standardized OR 0.63, 95% CI 0.45–0.88), and verbal judgement test (standardized OR 0.61, 95% CI 0.42–0.91) (Table 3).

Mediation analysis showed that the proportion of the effect of cognition (expressed by the MMSE) on nutritional status mediated by caregiver distress was 9.5% (95% CI: 0.002, 0.27), independently of appetite/nutritional problems. On the other hand, the proportion of the effect mediated by appetite/nutritional problems, independently of caregiver distress, was 11% (95% CI: –4.8, 3.18).

DISCUSSION

Our data confirm an association between cognitive impairment and nutritional risk that is independent of age, sex, and other potential confounders. Among specific cognitive domains considered, attention, praxis, and reasoning seem to have the greatest potential impact on nutritional status, and their effect is partly mediated by caregiver distress. Among the very few available studies evaluating the association between nutritional status and cognitive performance in different domains, Doorduijn et al. showed that a poor performance in the domains of attention, language and visuospatial ability and executive functioning was associated with lower modified MNA scores [14].

These partially discording results may be explained by different sample characteristics. Indeed, Doorduijn et al enrolled patients from no cognitive impairment to dementia, younger, dosed AD biomarkers, and used a different set of neuro-psychological tests. To the best of our knowledge, no other studies are available on this topic on patients with dementia.

It is conceivable that nutritional problems arise in different disease stages as a consequence of pathophysiological changes, dementia-specific nutritional problems, and the continuous decline of competences contributes to the reduced dietary intake and progression of the disease itself as a vicious circle [40].

Table 2

Association between cognitive tests score and risk of undernutrition

	Natural scale		Standardized⁺
	Crude OR (95% CI)	Adjusted* OR (95% CI)	Crude OR (95% CI)	Adjusted* OR (95% CI)
Mini-Mental State Examination	0.93 (0.9–0.96)	0.95 (0.9–1)	0.64 (0.53–0.77)	0.72 (0.52–1.01)
Clock-drawing test	0.8 (0.71–0.89)	0.9 (0.75–1.08)	0.68 (0.56–0.82)	0.84 (0.62–1.13)
Backward digit span	0.75 (0.62–0.91)	0.82 (0.61–1.09)	0.74 (0.6–0.91)	0.8 (0.59–1.1)
AVLT immediate	0.98 (0.95–1)	0.96 (0.92–1.01)	0.83 (0.67–1.03)	0.74 (0.51–1.07)
AVLT delayed	0.9 (0.82–0.98)	0.93 (0.79–1.09)	0.76 (0.6–0.96)	0.82 (0.54–1.25)
Attentive matrices	0.95 (0.93–0.97)	0.94 (0.92–0.97)	0.54 (0.43–0.68)	0.49 (0.34–0.72)
Corsi test	0.88 (0.75–1.03)	0.88 (0.72–1.08)	0.84 (0.68–1.03)	0.85 (0.64–1.11)
Figure copy test	0.87 (0.82–0.93)	0.87 (0.78–0.96)	0.64 (0.52–0.79)	0.63 (0.45–0.88)
Token test	0.94 (0.91–0.98)	0.97 (0.92–1.02)	0.71 (0.57–0.89)	0.83 (0.63–1.1)
Verbal judgement test	0.98 (0.96–0.99)	0.97 (0.94–0.99)	0.7 (0.56–0.88)	0.61 (0.42–0.91)

⁺Variables are scaled so that coefficients express changes in MNA by changes in cognitive function tests using SD as unit. ^*Adjusted for age, sex, education, caregiver, nutritional/appetite problems, caregiver distress score.

While the proportion of undernutrition risk was high in our sample of people with cognitive impairment, we found few patients with overt undernutrition. This is in contrast to some studies available in the recent literature [3 , 42], probably because we took in consideration only ambulatory patients, and with a relatively young age (mean age 77 years): there is strong evidence that the prevalence of undernutrition varies across settings [43, 44], being more prevalent among nursing home residents and in acute care hospital or rehabilitation settings [45 –48].

We have found that a sizable part (about 10%) of the effect of cognitive impairment on nutritional status is mediated by caregiver distress. To our knowledge, this is the first study reporting such a relationship through a mediation analysis rather than as a pure association [21, 22]. Within the dementia literature several studies examined the experience of being a caregiver of people with dementia, but less research explored the effect of caregiver burden on nutritional status. There is growing evidence that stress increases the vulnerability of chronic dementia caregiver to disease and diminishes their ability to provide optimal care [49]. Indeed, caregiver burnout is associated with poor outcomes for the care recipient, including early institutionalization, depression, poor quality of life, and mortality [50, 51]. The importance of this finding lies in the fact that caregiver distress is potentially modifiable, and this is relevant for intervention aimed at the prevention and care of undernutrition in people with dementia, that should include the evaluation and management of caregiver distress.

This study has some limitations. First, it is a mono-centric study and therefore our results may not be generalizable to other population, although the general characteristics of our sample are similar to that of most samples of older people. Second, our results are relevant only with respect to undernutrition risk, as we found only a few patients with overt undernutrition: further studies are needed to confirm our findings also with respect to this outcome. Third, the mediation analysis could be affected by the cross-sectional design of the study. Finally, given the design and setting of the study, a power analysis was not conducted.

In conclusion, we showed that the risk of undernutrition is clearly associated to cognitive decline and caregiver distress is one of the mediators of undernutrition in people with dementia. This information should be considered in the management plans of people with dementia, especially those with more severe impairment.

DISCLOSURE STATEMENT

Authors’ disclosures available online (https://www.j-alz.com/manuscript-disclosures/21-5732r2).

References

Alzheimer Europe (2019) Dementia in Europe Yearbook 2019: Estimating the prevalence of dementia in Europe. https://www.alzheimer-europe.org/sites/default/files/alzheimereuropedementiaineuropeyearbook2019.pdf. Accessed on December 27, 2021.

Waldemar

, Phung

KTT

, Burns

, Georges

, Hansen

, Iliffe

, Marking

, Rikkert

, Selmes

, Stoppe

, Sartorius

(2007) Access to diagnostic evaluation and treatment for dementia in Europe. Int J Geriatr Psychiatry 22, 47–54.

Suominen

, Muurinen

, Routasalo

, Soini

, Suur-Uski

, Peiponen

, Finne-Soveri

, Pitkala

(2005) Malnutrition and associated factors among aged residents in all nursing homes in Helsinki. Eur J Clin Nutr 59, 578–583.

Gillette Guyonnet

, Abellan Van Kan

, Alix

, Andrieu

, Belmin

, Berrut

, Bonnefoy

, Brocker

, Constans

, Ferry

, Ghisolfi-Marque

, Girard

, Gonthier

, Guerin

, Hervy

M-P

, Jouanny

, Laurain

M-C

, Lechowski

, Nourhashemi

, Raynaud-Simon

, Ritz

, Roche

, Rolland

, Salva

, Vellas

, International Academy on Nutrition and Aging Expert Group (2007) IANA (International Academy on Nutrition and Aging) Expert Group: Weight loss and Alzheimer’s disease. J Nutr Health Aging 11, 38–48.

Minaglia

, Giannotti

, Boccardi

, Mecocci

, Serafini

, Odetti

, Monacelli

(2019) Cachexia and advanced dementia. J Cachexia Sarcopenia Muscle 10, 263–277.

McCrickerd

, Forde

(2016) Sensory influences on food intake control: Moving beyond palatability. Obes Rev 17, 18–29.

Contri-Degiovanni

, Degiovanni

, Ferriolli

, da Costa Lima

, Moriguti

(2020) Impact of the severity of dementia due to Alzheimer’s disease on the gustatory sensitivity of older persons. Aging Clin Exp Res 32, 2303–2309.

Peters

, Hummel

, Kratzsch

, Lötsch

, Skarke

, Frölich

(2003) Olfactory function in mild cognitive impairment and Alzheimer’s disease: An investigation using psychophysical and electrophysiological techniques. Am J Psychiatry 160, 1995–2002.

Steinbach

, Hundt

, Vaitl

, Heinrich

, Förster

, Bürger

, Zahnert

(2010) Taste in mild cognitive impairment and Alzheimer’s disease. J Neurol 257, 238–246.

10.

Tjahyo

, Gandy

, Porter

, Henry

(2021) Is weight loss more severe in older people with dementia? . J Alzheimers Dis 81, 57–73.

11.

Doorduijn

, van de Rest

, van der Flier

, Visser

, de van der Schueren

MAE

(2019) Energy and protein intake of Alzheimer’s disease patients compared to cognitively normal controls: Systematic review. J Am Med Dir Assoc 20, 14–21.

12.

Soysal

, Dokuzlar

, Erken

, Dost Günay

, Isik

(2020) The relationship between dementia subtypes and nutritional parameters in older adults. J Am Med Dir Assoc 21, 1430–1435.

13.

Mourão

, Vicente

LCC

, Abreu

MNS

, Chaves

, Sant’Anna

, Braga

MAF

, de Meira

FCA

, de Souza

, de Miranda

, Rachid

, Teixeira

(2018) Association between executive and food functions in the acute phase after stroke. Arq Neuropsiquiatr 76, 158–162.

14.

Doorduijn

, Visser

, van de Rest

, Kester

, de Leeuw

, Boesveldt

, Fieldhouse

JLP

, van den Heuvel

EGHM

, Teunissen

, Scheltens

, van der Flier

, de van der Schueren

MAE

(2019) Associations of AD biomarkers and cognitive performance with nutritional status: The NUDAD Project. Nutrients 11, E1161.

15.

Liu

, Williams

, Batchelor-Murphy

, Perkhounkova

, Hein

(2019) Eating performance in relation to intake of solid and liquid food in nursing home residents with dementia: A secondary behavioral analysis of mealtime videos. Int J Nurs Stud 96, 18–26.

16.

Keller

, Carrier

, Slaughter

, Lengyel

, Steele

, Duizer

, Morrison

, Brown

, Chaudhury

, Yoon

, Duncan

, Boscart

, Heckman

, Villalon

(2017) Prevalence and determinants of poor food intake of residents living in long-term care. J Am Med Dir Assoc 18, 941–947.

17.

Liu

, Perkhounkova

, Williams

, Batchelor

, Hein

(2020) Food intake is associated with verbal interactions between nursing home staff and residents with dementia: A secondary analysis of videotaped observations. Int J Nurs Stud 109, 103654.

18.

Liu

, Jao

Y-L

, Williams

(2017) The association of eating performance and environmental stimulation among older adults with dementia in nursing homes: A secondary analysis. Int J Nurs Stud 71, 70–79.

19.

Cipriani

, Carlesi

, Lucetti

, Danti

, Nuti

(2016) Eating behaviors and dietary changes in patients with dementia. Am J Alzheimers Dis Other Demen 31, 706–716.

20.

Rullier

, Lagarde

, Bouisson

, Bergua

, Barberger-Gateau

(2013) Nutritional status of community-dwelling older people with dementia: Associations with individual and family caregivers’ characteristics. Int J Geriatr Psychiatry 28, 580–588.

21.

Andrieu

, Balardy

, Gillette-Guyonnet

, Bocquet

, Cantet

, Albarède

, Vellas

, Grand

(2003) [Burden experienced by informal caregivers assisting Alzheimer’s patients in the REAL.FR study]. Rev Med Interne 24(Suppl 3), 351s–359s.

22.

Brocker

, Benhamidat

, Benoit

, Staccini

, Bertogliati

, Guérin

, Lechowski

, Robert

(2003) [Nutritional status andAlzheimer’s disease: Preliminary results of the REAL.FR study]. Rev Med Interne 24(Suppl 3), 314s–318s.

23.

Mariani

, Monastero

, Ercolani

, Rinaldi

, Mangialasche

, Costanzi

, Vitale

, Senin

, Mecocci

, ReGAl Study Group (2008) Influence of comorbidity and cognitive status on instrumental activities of daily living in amnestic mild cognitive impairment: Results from the ReGAl project. Int J Geriatr Psychiatry 23, 523–530.

24.

American Psychiatric Association (1994) Diagnostic and Statistical Manual, 4th ed, APA Press, Washington, DC..

25.

Petersen

(2004) Mild cognitive impairment as a diagnostic entity. J Intern Med 256, 183–194.

26.

McKhann

, Drachman

, Folstein

, Katzman

, Price

, Stadlan

(1984) 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 34, 939–944.

27.

Román

, Tatemichi

, Erkinjuntti

, Cummings

, Masdeu

, Garcia

, Amaducci

, Orgogozo

, Brun

, Hofman

(1993) Vasculardementia: Diagnostic criteria for research studies. Report of theNINDS-AIREN International Workshop. Neurology 43, 250–260.

28.

Neary

, Snowden

, Gustafson

, Passant

, Stuss

, Black

, Freedman

, Kertesz

, Robert

, Albert

, Boone

, Miller

, Cummings

, Benson

(1998) Frontotemporal lobar degeneration: A consensus on clinical diagnostic criteria. Neurology 51, 1546–1554.

29.

McKeith

, Ballard

, Perry

, Ince

, O’Brien

, Neill

, Lowery

, Jaros

, Barber

, Thompson

, Swann

, Fairbairn

, Perry

(2000) Prospective validation of consensus criteria for the diagnosis of dementia with Lewy bodies. Neurology 54, 1050–1058.

30.

Emre

, Aarsland

, Brown

, Burn

, Duyckaerts

, Mizuno

, Broe

, Cummings

, Dickson

, Gauthier

, Goldman

, Goetz

, Korczyn

, Lees

, Levy

, Litvan

, McKeith

, Olanow

, Poewe

, Quinn

, Sampaio

, Tolosa

, Dubois

(2007) Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 22, 1689–1707;quiz1837.

31.

Hughes

, Berg

, Danziger

, Coben

, Martin

(1982) A new clinical scale for the staging of dementia. Br J Psychiatry 140, 566–572.

32.

Folstein

, Folstein

, McHugh

(1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12, 189–198.

33.

Spinnler

, Tognoni

(1987) Standardizzazione e taratura italiana di test neuropsicologici: Gruppo italiano per lo tudio neuropsicologico dell’ivecchiamento,Masson Italia Periodici, Milano.

34.

Carlesimo

, Caltagirone

, Gainotti

(1996) The Mental Deterioration Battery: Normative data, diagnostic reliability and qualitative analyses of cognitive impairment. The Group for the Standardization of the Mental Deterioration Battery. Eur Neurol 36, 378–384.

35.

Palmiero

, Di Vita

, Teghil

, Piccardi

(2022) The Verbal Judgement Task: Normative data of verbal abstract reasoning in a sample of 18- to 40-years old. Appl Neuropsychol Adult 29, 562–569.

36.

Yesavage

(1988) Geriatric Depression Scale. Psychopharmacol Bull 24, 709–711.

37.

Cummings

, Mega

, Gray

, Rosenberg-Thompson

, Carusi

, Gornbein

(1994) The Neuropsychiatric Inventory: Comprehensive assessment of psychopathology in dementia. Neurology 44, 2308–2314.

38.

Guigoz

, Lauque

, Vellas

(2002) Identifying the elderly at risk for malnutrition The Mini Nutritional Assessment. Clin Geriatr Med 18, 737–757.

39.

Fairchild

, McDaniel

(2017) Best (but oft-forgotten) practices: Mediation analysis. Am J Clin Nutr 105, 1259–1271.

40.

Volkert

, Chourdakis

, Faxen-Irving

, Frühwald

, Landi

, Suominen

, Vandewoude

, Wirth

, Schneider

(2015) ESPEN guidelines on nutrition in dementia. Clin Nutr 34, 1052–1073.

41.

, Yu

, Liu

, Wan

, Chen

, Xiong

, Zhang

, Lü

(2021) Associations between malnutrition and cognitive impairment in an elderly Chinese population: An analysis based on a 7-year database. Psychogeriatrics 21, 80–88.

42.

Roqué

, Salvà

, Vellas

(2013) Malnutrition incommunity-dwelling adults with dementia (NutriAlz Trial). JNutr Health Aging 17, 295–299.

43.

Visser

, Deeg

, Puts

, Seidell

, Lips

(2006) Low serum concentrations of 25-hydroxyvitamin D in older persons and the risk of nursing home admission. Am J Clin Nutr 84, 616–622.

44.

Maseda

, Gómez-Caamaño

, Lorenzo-López

, López-López

, Diego-Diez

, Sanluís-Martínez

, Valdiglesias

, Millán-Calenti

(2016) Health determinants ofnutritional status in community-dwelling older population: TheVERISAÚDE study. Public Health Nutr 19, 2220–2228.

45.

van Zwienen-Pot

, Visser

, Kuijpers

, Grimmerink

MFA

, Kruizenga

(2017) Undernutrition in nursing home rehabilitation patients. Clin Nutr 36, 755–759.

46.

Rojer

AGM

, Kruizenga

, Trappenburg

, Reijnierse

, Sipilä

, Narici

, Hogrel

, Butler-Browne

, McPhee

, Pääsuke

, Meskers

CGM

, Maier

, de van der Schueren

MAE

(2016) The prevalence of malnutrition according to the new ESPEN definition in four diverse populations. Clin Nutr 35, 758–762.

47.

Kaiser

, Bauer

, Rämsch

, Uter

, Guigoz

, Cederholm

, Thomas

, Anthony

, Charlton

, Maggio

, Tsai

, Vellas

, Sieber

, Mini Nutritional Assessment International Group (2010) Frequency of malnutrition in older adults: A multinational perspective using the mini nutritional assessment. J Am Geriatr Soc 58, 1734–1738.

48.

Kruizenga

, van Keeken

, Weijs

, Bastiaanse

, Beijer

, Huisman-de Waal

, Jager-Wittenaar

, Jonkers-Schuitema

, Klos

, Remijnse-Meester

, Witteman

, Thijs

(2016) Undernutrition screening survey in 564,063 patients: Patients with a positive undernutrition screening score stay in hospital 1.4 d longer. Am J Clin Nutr 103, 1026–1032.

49.

Fonareva

, Oken

(2014) Physiological and functional consequences of caregiving for relatives with dementia. Int Psychogeriatr 26, 725–747.

50.

Gaugler

, Kane

, Clay

, Newcomer

(2005) The effects of duration of caregiving on institutionalization. Gerontologist 45, 78–89.

51.

Torti

, Gwyther

, Reed

, Friedman

, Schulman

(2004) A multinational review of recent trends and reports in dementia caregiver burden. Alzheimer Dis Assoc Disord 18, 99–109.