Appetite, 1997, 28, 167–175

Hyperphagia in Dementia: 2. Food Choices and their

Macronutrient Contents in Hyperphagia, Dementia and

Ageing

JANET M. KEENEUniversity of Oxford, Department of Psychiatry

TONY HOPEPractice Skills Project, John Radcliffe Hospital, Oxford

Up to one third of dementia sufferers eat an increased quantity of food comparedwith their premorbid intake, at some stage during the dementia. In addition, overhalf of people with dementia are reported, by their carers, to show a markedchange in food choice, particularly an increased liking for sweet food. Themacronutrient content of foods chosen and the ratio of sweet to savoury foodswere investigated experimentally using a standardized mixed meal. Three subjectgroups were studied: 17 people with dementia who were reported by their carersto overeat and who ate excessively under experimental conditions; 14 people withdementia who ate a normal amount; and, normal, non-demented controls (18under 50 years old and 14 over 50 years old). The results showed that the normalelderly people chose a lower proportion of high-protein food than the young.The proportion of protein eaten was lower in people with dementia than in age-matched controls and was even lower in the hyperphagic dementia group. Theproportion of sweet food eaten was higher in people with dementia and evenhigher in people with dementia who were hyperphagic. Various mechanisms toaccount for the results are discussed. 1997 Academic Press Limited

I

Up to one third of dementia sufferers eat an increased quantity of food comparedwith their premorbid intake, at some stage during the dementia (Morris, Hope &Fairburn, 1989; Teri, Boroson, Kiyak & Yamagishi, 1989; Burns, Jacobs & Levy,1990; Hope, Morris & Fairburn, 1991; Keene et al. in preparation). Furthermore,

Peter Rogers and Nicky Elliman, of the Institute of Food Research at Reading carried out the testmeals on the younger subject group. We were kindly given permission to use of the software programwritten by Andrew Leech, originally developed for use with Automated Food Dispenser (Goodall, Feeney,McGuirk & Silverstone, 1992).

The authors gratefully acknowledge the help of John Blundell, Sandra Cooper, Christopher Fairburn,Kathy Gedling, Paul Griffiths, Robin Jacoby, the Oxford Project to Investigate Memory and Ageing aswell as the subjects and their carers who generously gave their time to help with our research. JanetKeene was a Medical Research Council research student and member of St Cross College, University ofOxford during the period when this research was carried out.

Address correspondence to: Janet M. Keene, University of Oxford, Department of Psychiatry,Warneford Hospital, Oxford OX3 7JX.

0195–6663/97/020167+09 $25.00/0/ap960068 1997 Academic Press Limited

168 J. M. KEENE AND T. HOPE

several researchers have reported distinct changes in food choice in many peoplewith dementia, sweet foods usually being preferred. Mungas, Cooper, Weiler, Gietzen,Franzi and Bernick, (1990) carried out a brief telephone survey on the food consumptionand preference of people with dementia. Carers reported that they needed to restrictsweet foods for 51% of the subjects, and a preference for sweet foods appeared tobe related to an increase in appetite, but not to a change in weight.

Similar results have been found, using semi-structured interviews with carers, byMorris et al. (1989) and Hope et al. (1991). These authors studied the eatingbehaviour of a group of 33 subjects with dementia who were living in the community.They found increased preference for sweet food in 24% of subjects, 15% of subjectsliked more spicy food; non-food pica, including coprophagia, was reported in 15%;and the eating of inappropriate food was reported in 15%.

Of a group of 85 people, who have been followed throughout the course of theirdementing illness until death, 35% had a period of increased eating at some stageduring the illness. Fifty-four per cent ate more sweet food than premorbidly, whensuch food was available. Fifteen per cent of the sample ate inappropriate foods (forexample pet food or potato peelings) and 22% chewed or swallowed non-food items.“Oral behaviour” such as feeling things with the mouth (as seen in the Klu¨ ver-Bucysyndrome), was reported in 15% of the sample.

There are conflicting accounts of energy and macronutrient intake in the normalelderly e.g. Garry, Rhyne, Halioua and Nicholson, (1989) found that in a group ofnormal elderly, protein intake decreased most with age, whereas Wurtman (1988b)found that healthy elderly people ate fewer sweets and starchy food snacks than theyoung but a similar quantity of protein. A Swedish report found that the proportionof energy intake from fat increased with age but the protein intake was sufficientfor individuals who were in good health (Nordstrom, Lundgren, Nilsson, Steen &Osterlind, 1988). In a study which measured food intake over three days, in-patientswith severe dementia ate less protein than normal, elderly controls (Chung-A-On,Thomas, Tidmarsh, Dickerson, Sweeney & Shaw, 1985; Thomas, Chung-A-On,Dickerson, Tidmarsh & Shaw, 1986).

Thus, there is considerable evidence that changes in macronutrient intake andfood choice are common in dementia. However, there are no good data on the exactnature of these changes, nor on their relationship to hyperphagia. The first aim ofthe experiments reported here was to investigate whether the percentage intake ofmacronutrients (protein, fat and carbohydrate) in people with dementia who arehyperphagic, is significantly different from people with dementia who are nothyperphagic, and from normal controls. The second aim was to investigate whetherthe ratio of sweet to savoury food intake is affected by age, by dementia and byhyperphagia.

M

Subject Groups

Four groups of subjects were studied. The subjects over 50 were described inpaper 1 [Keene & Hope, 1997 (17 from Group A—hyperphagic demented; 14 fromGroup B—non-hyperphagic demented and 9 from Group C—normal elderly)]. Eachsubject in groups B and C was matched individually for age and sex to a subject in

169HYPERPHAGIA, DEMENTIA AND AGEING

Group A. In addition, a further group of normal younger people (Group D) wasused to investigate the effect of age on both macronutrient and sweet/savoury foodchoice. This group consisted of 18 subjects under 50 years old.

The Standardized Meal

The standardized meal consisted of a variety of foods with varying macronutrientcontent. After testing during pilot work, eight foods were selected:High Protein—Ham; cheese slices.High Carbohydrate—Bread and a little margarine (non-sweet); digestive biscuits(sweet).High Fat—Pork sausage; thick cheese and butter sandwiches.Low-energy Foods—Pear (sweet); cucumber (non-sweet).

The eight foods were all judged, by a sample of five normal controls, to bepalatable but no one food markedly more attractive than the others. When testedwith demented people, there were no significant problems and some of the foodfrom each category was sampled (Keene & Hope, 1997).

Data on energy value and macronutrient composition (Keene & Hope, 1997Table 1) were taken from manufacturers’ information or, for unprocessed foods,from McCance and Widdowson’s The composition of foods (Paul & Southgate,1991). The macronutrient content and sweet/savoury content of the meal wereanalysed using the “Weight-watcher” program devised by Leech for use with anautomated food dispenser (Goodall et al., 1992). The intake of sweet foods (biscuitsand pear) was measured both as total energy value (kJ) and as mass of sweet foodeaten (g). Both macronutrient and sweet food intake were calculated as a total andalso as a percentage of total intake, to obtain the relative intake of each macronutrientand the ratio of sweet to savoury foods chosen.

Method of Giving Meal

Macronutrient and food choice were measured under standardized conditions(as in Keene & Hope, 1997). For each consecutive subject, the order of foods wasrotated in a fixed sequence to eliminate the possibility that the position of foodstuffswould affect the mean of each group’s results. For every individual, the rotation offood position for subsequent meals, should show whether food choice was random,was by macronutrient type or was chosen by the position of the food on the table.

The main focus of the analysis is to examine macronutrient and sweet/savouryintake but, in addition, the order and types of different foods which were sampledduring meal 1 were noted (e.g. one person might choose four of the eight typesduring the course of the meal and another might eat some of all eight).

A further investigation was made to examine the effect of age on food choice.Data from another experiment (Keene, Hope, Rogers & Elliman, in press) were usedto investigate the effect of age on both macronutrient and sweet/savoury food choice.In this experiment a series of three of the standardized mixed meals were given toa group of 18 normal younger people (aged 23–47) and nine normal elderly (aged56–83). These meals had been preceded an hour earlier by a preload (either 200 mlwater or a milkshake of 660 or 1870 kJ).

Changed food choice may be a side-effect of medication, in particular neuroleptics,tricyclic antidepressants and lithium carbonate (Silverstone, 1985) which are com-

170 J. M. KEENE AND T. HOPE

T 1Intake (kJ) of macronutrient per meal—mixed meal 1

MacronutrientGroup A Group B Group C

(hyperphagic (non-hyperphagic (normaldemented) demented) elderly)

Energy (kJ) % of Energy (kJ) % of Energy (kJ) % ofMean SD energy Mean SD energy Mean SD energy

Protein 680 392 12·3 314 218 15·4 334 122 18·5Fat 2777 1553 49·5 990 600 47·1 878 346 46·8Carbohydrate 2006 985 38·2 684 486 37·5 611 165 34·7

monly prescribed in dementia. Current medication was recorded at the time of eachmeal. All stages of the study were approved by the Psychiatric Sector ResearchEthics Committee.

Test-retest Reliability

Test-retest reliability of both macronutrient intake and sweet/savoury intake wasassessed by repeating the test meals in a sub-group of subjects. Test meals wererepeated with 21 subjects (11 from Group A, 5 from Group B and 5 from GroupC). The second test meal was given from 2 to 15 weeks after the first. The correlationbetween the macronutrient and sweet/savoury intake on the two occasions was usedas a measure of reliability.

R

Results of the first mixed meal were analysed for changes in food choice andresults of the first and second mixed meal provided data for reliability. There wasno significant difference between the two groups with dementia in relevant medication.

Macronutrient Choice

The hyperphagic group ate more of everything, not surprisingly (Table 1).However, when macronutrient intake is expressed as a percentage of the total intake,the hyperphagic group ate significantly less protein than the normal elderly, t(29)=3·5, p=0·002. The non-hyperphagic demented group’s intake of protein was inter-mediate between the other two groups (Fig. 1). No other differences were significantbut a clear pattern suggests that the percentage intake for each of the threemacronutrients can be ranked, with the hyperphagic group and the normal elderlyat the extremes and the non-hyperphagic demented group in the middle.

ReliabilityExpressed as a percentage of the total intake there was a significant correlation

between protein intake at the two meals (Pearson correlation: 0·457, df=20, p=0·037). When energy values (kJ) were compared there was a significant correlation

171HYPERPHAGIA, DEMENTIA AND AGEING

25

0Hyperphagic

demented subjects(N = 17)

Pro

tein

(%

)20

15

10

5

Non-hyperphagicdemented subjects

(N = 14)

Normal elderlycontrols(N = 14)

F 1. Protein intake as a percentage of total meal—(mixed meal 1).

60

0Hyperphagic

demented subjects(N = 17)

Sw

eet

food

(%

) 40

30

20

10

Non-hyperphagicdemented subjects

(N = 14)

Normal elderlycontrols(N = 14)

50

F 2. Sweet food intake as a percentage of total meal (mixed meal 1).

between all three macronutrients eaten at meal 1 and meal 2 (Pearson correlation:protein 0·619, p=0·003; fat 0·849, p<0·0005; carbohydrate 0·821, p<0·0005; df=20).

Sweet/savoury Choice

As a percentage of total intake the hyperphagic demented ate more than twiceas much sweet food as the normal elderly (Fig. 2). Again the non-hyperphagic group

172 J. M. KEENE AND T. HOPE

T 2The effect of age on food choice

Macronutrient Mean intake per meal in each group—Group C (N=9) Group D (N=18)Normal elderly Normal young group

Energy (kJ) % of Energy (kJ) % ofMean SD energy Mean SD energy

Protein 281 116 17·3 959 772 21·7Fat 760 299 46·3 1787 837 48·3Carbohydrate 585 118 34·5 1018 403 29·9

showed a pattern intermediate between the other two groups. Using an independentt-test, the difference in the mean percentage of sweet food eaten by the hyperphagicgroup (34·8%) and the normal elderly (16·0%) was significant, t(27)=3·4, p=0·002).The differences between the non-hyperphagic demented group and either of the othertwo groups were not significant at the p≤0·05 level.

ReliabilityFor the three experimental groups, there was a high correlation in the sweet food

intake (kJ), between the first and second mixed meals (Pearson correlation: 0·579,p=0·005).

Foods Chosen

The normal elderly chose a wider range of food items than either of the dementedgroups. At the first mixed meal the normal elderly ate a mean of 6·6 of the eightdifferent food types whereas the non-hyperphagic, demented group chose a mean of4·9 types. The difference between these groups was significant, t(23)=2·68, p=0·013. The hyperphagic demented were intermediate, eating a mean of 6·2 differenttypes, which was significantly more than the non-hyperphagic group t(24)=2·03,p≤=0·05. The difference between the hyperphagic group and the normal elderlywas not significant. Both demented groups ate a smaller percentage of low-energyfood (pear and cucumber) than the normal elderly (hyperphagic demented 4·4%;non-hyperphagic demented 5·4%; normal elderly 12·6%). The normal elderly groupusually chose foods in a “conventional” order. They ate savoury (or non-sweet) foodfirst, such as ham, cheese, sandwiches and cucumber, then sweet foods (pear and/orbiscuits) at the end of the meal. This was not the case with the two demented groups.

ReliabilityThere was no significant difference in the number of foods eaten between the

first and second mixed meals.

The Effect of Age on Food Choice

Macronutrient choiceFor the three test meals, the means of energy value and percentage of each

macronutrient were calculated (Table 2). The preload was shown to have no significanteffect on subsequent food choice.

173HYPERPHAGIA, DEMENTIA AND AGEING

The normal young group (under 50 years old) ate a higher proportion of proteinthan the normal elderly group (when calculated as the mean of three test means).This difference was significant (p=0·038). The older group chose a greater proportionof carbohydrate (this approached significance—p=0·053) but the difference in fatintake with age was not significant.

Sweet food intake(% of total intake). The difference in sweet food intake by the over-50s and the

under-50s was not significant at the pΖ0·05 level.

ReliabilityTest-retest reliability was calculated by comparing the food intake during the

test meals which followed the water and the low-energy preloads. There was a highcorrelation between the percentage of each macronutrient and of sweet foodseaten during these two test meals (Pearson correlation: protein 0·698; fat 0·837;carbohydrate 0·895; sweet food 0·865; p<0·0005 in each case).

D

In this paper we report the use of a standardized meal to measure the mac-ronutrient intake and sweet food choice made under standardized conditions inhyperphagic people with dementia, non-hyperphagic demented controls, normalelderly controls and adults under 50 years old. The dementia controls were matchedwith the hyperphagia group for age, sex and degree of dementia. The normal elderlycontrols were matched with the hyperphagia group for age and sex. The purposewas to investigate the effect on food choice, of (a) age, (b) dementia and (c) markedhyperphagia with dementia. This is the first study investigating these issues usingprecise measures under standardized conditions.

With increasing age, in normal people, the proportion of protein eaten decreasedand carbohydrate increased. There were also a number of differences between thenormal elderly and those with dementia; in particular people with dementia ate lessprotein and more sweet food. This may be an exaggeration of the changes seen innormal ageing, with the hyperphagic group being at the extreme end of the spectrum.It was not possible to separate differences in palatability for those with dementia asis possible for normal subjects. Therefore, with protein foods for example, itwas not possible to assess whether less protein was chosen because of change inmacronutrient preference or whether the high-protein foods were perceived asrelatively less palatable.

There are two limitations of these experiments. First, the number of subjects ineach group was small. However, in spite of the small numbers in the groups, thereliability studies suggest that these findings are robust. Secondly, the measures weremade using a standardized meal. This enabled us to make precise measures of whatwas eaten. However, it is possible that if food intake over days, rather than withina single meal, were measured, the results would be different.

These studies raise the question of what the mechanism for these findings mightbe. In particular, why is the percentage of protein eaten less in older people, stillless in people with dementia and least (as a percentage) in those with dementia whoare also hyperphagic? And why is the percentage of sweet food chosen progressively

174 J. M. KEENE AND T. HOPE

greater in the above categories? One possible unifying mechanism is that thesedifferences are due to differences in the levels of brain 5-hydroxytryptamine (5-HT).

Brain 5-HT is generally reduced in Alzheimer’s disease (Hardy et al., 1985) butthere is much individual variation. Delayed termination of eating, preference forsweet foods and choice of high-fat and carbohydrate food, together with a severereduction in protein intake are all compatible with a reduction of 5-HT (Leibowitz& Shor-Posner, 1986). Ashley, Coscina and Anderson (1979) found that 5-HTdepletion in rats is followed by a 20–30% reduction in protein intake. Decreasedbrain 5-HT could also account for the hyperphagia (Blundell, 1984). Furthermore,people with bulimia nervosa have been shown to have disturbance of brain 5-HTfunction and were also found to have a relatively low intake of protein (Walsh,Hadigan & Kissileff, 1992).

Reduced brain 5-HT is associated also with increased desire for sweet food andcarbohydrate craving in Alzheimer’s disease (Cooper & Mungas, 1992). The relativeintake of carbohydrate is increased in a number of situations when brain 5-HT islow, for example in carbohydrate-craving obesity (Wurtman, 1988a), seasonal affectivedisorder (Wirz-Justice & Richter, 1979) and premenstrual syndrome (Rogers, Ed-wards, Green & Jas, 1992). Diet in turn can affect 5-HT levels (Fernstrom, Wurtman,Hammarstrom-Wiklund, Rand, Munro & Davidson, 1979; Wurtman, 1978; Teff,Young, Marchand & Botez, 1989). If, in dementia, reduction in 5-HT does influencediet, it might be predicted that the hyperphagic group are a sub-group with stilllower levels of 5-HT. The change in food choice towards less protein and more sweetfoods could hypothetically increase the availability of 5-HT, at least in a highlydysfunctional system (in dementia the blood-brain barrier, hypothalamic neuronesand plasma albumin are known to be abnormal; Ishii, 1966; Hardy et al., 1985).

Reduction in 5-HT may have a direct effect via the central control of food intake,since low 5-HT may lead to hyperphagia. This would account for the link betweenhyperphagia and a lower percentage of protein intake. Alternatively low proteinintake and increased sweet/carbohydrate food intake might increase the productionof brain 5-HT, alleviating the unpleasant symptoms, such as dysphoria and irritability,caused by low brain 5-HT. It is tempting to speculate that such dietary changesmight be a form of self-medication giving a greater feeling of well-being, counteractingthe unpleasant effects of low 5-HT on mood and behaviour. This might lead topositive feedback for eating less protein and more carbohydrate. There could thereforebe some value in the dietary changes, seen in dementia, and particularly in thoseshowing marked dementia, in reversing some negative aspects of low 5-HT.

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Received 12 December 1995, revision 9 September 1996