Clinical Nutrition 29 (2010) 160–169
Contents lists available at ScienceDirect
Clinical Nutrition
journal homepage: http://www.elsevier.com/locate/clnu
Review
Older adults and patients in need of nutritional support: Review of current
treatment options and factors influencing nutritional intake
Willem F. Nieuwenhuizen a, *, Hugo Weenen a, Paul Rigby b, Marion M. Hetherington c
a
Danone Research, Center for Specialised Nutrition, Bosrandweg 20, 6700 CA Wageningen, The Netherlands
Danone Medical Nutrition Division, WTC Schiphol Airport, Tower E, Schiphol Boulevard 105, 118 BG Schiphol Airport, The Netherlands
c
Marion M. Hetherington, Institute of Psychological Sciences, University of Leeds, Leeds, LS2 9JT England, UK
b
a r t i c l e i n f o
s u m m a r y
Article history:
Received 11 February 2009
Accepted 11 September 2009
Background & aims: Many older adults and patients do not achieve sufficient nutritional intake to support
their minimal needs and are at risk of, or are suffering from, (protein-energy) malnutrition. Better
understanding of current treatment options and factors determining nutritional intake, may help design
new strategies to solve this multifactorial problem.
Methods: Medline, Science Citation Index, ScienceDirect and Google databases (until December 2008)
were searched with the keywords malnutrition, elderly, older adults, food intake, energy density, variety,
taste, satiety, and appetite.
Results: 37 Factors affecting nutritional intake were identified and divided in three categories; those
related to the environment, the person, and the food. For older adults in nursing homes, encouragement
by carers and an appropriate ambiance seem particularly important. Meal fortification, offering variety,
providing frequent small meals, snacks and particularly Oral Nutritional Supplements (ONS) between
meals are other possibilities for this group. Product factors that stimulate intake include palatability, high
energy density, low volume, and liquid format.
Conclusion: The current review gives a comprehensive overview of factors affecting nutritional intake and
may help carers to improve nutritional intake in their patients. The product factors identified here suggest
that especially small volume, energy and nutrient dense ONS can be effective to improve nutritional intake.
Ó 2009 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
Keywords:
Oral Nutritional Supplement
Elderly
Volume
Energy density
Malnutrition
Nutrition support
1. Introduction
Much attention is given to the obesity problem i.e. people who
consume more energy than they need, and less attention is given to
the many, often older people who do not consume enough nutrients and/or energy to support their minimum requirements.
Malnutrition is very common in this group, even in Western
society.1 Up to 12.5% of patients residing in the community with
chronic disease are underweight. The prevalence of undernutrition
and risk of undernutrition in community dwelling older adults
(>65 years) have been reported to be 4.3% and 25.4%, respectively.2
Two recent studies showed that 49.5% of residents (average age
84.2 years) in residential care facilities were moderately to severely
malnourished,3 and that 6% of frail older adults (78–86 years)
undergoing rehabilitation were malnourished and 13% mildly
malnourished.4 The prevalence of malnutrition in long-term care
home residents has been estimated to be as high as 85%.5 It has
* Corresponding author. Tel.: þ31 317 467992.
E-mail address: [email protected] (W.F. Nieuwenhuizen).
been estimated that the mean prevalence of being underweight in
patients admitted to hospital is approximately 18% (range
5%-37.5%).6 On average nutritionally at risk patients incurred 19%
higher hospital costs than the average of those not at risk with
a similar diagnosis.7 Other studies have reported figures of up to
75% and even 300% greater treatment costs associated with the
presence of malnutrition.8–10
Malnutrition has been defined as ‘‘.a state of nutrition in which
a deficiency or excess (or imbalance) of energy, protein and other
nutrients causes measurable adverse effects on tissue/body form
(body shape, size and composition) and function, and clinical
outcome’’.11
Malnutrition is one of the greatest threats to the health, wellbeing and autonomy of older adults.12 The National Health and
Nutrition Survey (NHANES) II in the USA, has shown that involuntary weight loss is disproportionately high in older adults and is
associated with increased mortality.12 In older patients unintentional weight loss is associated with higher risk of infection,
depression and death. Unintentional weight loss can lead to muscle
wasting, decreased immunocompetence and increased rate of
complications.7
0261-5614/$ – see front matter Ó 2009 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
doi:10.1016/j.clnu.2009.09.003
W.F. Nieuwenhuizen et al. / Clinical Nutrition 29 (2010) 160–169
A BMI below 20 kg/m2 and/or recent unintentional weight loss
can be used to detect protein-energy malnutrition, which has been
defined as undernutrition due to an inadequate intake of protein,
fat, and carbohydrate.6 A loss of approximately 5–10% of body
weight in the previous 12 months may indicate a problem in the
older patient. The leading causes of involuntary weight loss are
depression, cancer, cardiac disorders, lower socioeconomic status,
functional disabilities and benign gastrointestinal diseases. Overall,
psychiatric disorders, including depression, account for 58% of the
cases of involuntary weight loss in nursing home patients.13
The aim of this review is to give an overview of malnutrition
factors that influence nutritional intake in older adults and current
ways to treat protein-energy malnutrition status.
161
Table 1
Factors affecting nutritional intake in older adults.
Reduces intake
Promotes intake
Product
Ingredients
Ingredients
- High protein
- High fat
- High fibre
- Slow-digestible
carbohydrates
Food attributes
Food attributes
- High palatability
- High viscosity
- Appetizing appearance
- Large volume
- High energy density
- Monotonous diets
- Low volume/Small
Culturally inappropriate food
portion size
Presentation of too large
- Liquids (between meals)
portion size
- Variety in the diet
Personal
Social changes
Physiological changes
Psychological changes
Eating process
2. Methods
Medline, Science Citation Index, ScienceDirect and Google databases were searched (until December 2008) with the keywords
malnutrition, elderly, older adults, food intake, energy density,
variety, taste, satiety, and appetite. The first author prepared the initial
list of publications based on the search results. Based on this initial list,
all authors (WFN, HW, PR and MMH) made the selection of the papers
together and analyzed the scientific studies used in this review.
Publications were selected as follows: 1. Initially all relevant publications from English peer-reviewed journals were selected that gave
theoretical or practical information on factors affecting nutritional
intake in patients and older adults and current treatment options. 2.
From this long list, publications were selected for the review that most
convincingly described the importance of a factor or underlying
mechanism. If there were too many papers on a specific topic and no
clear difference in the quality of the evidence, then the first published
paper(s) on a particular topic were selected. There were no prior
hypotheses on the relevant importance of factors.
3. Results
Based on our search and subsequent selection of papers, 123
papers have been reviewed. These were reviewed for their topic
content and then sub-divided into the topics of factors influencing
nutritional intake i.e. personal, food and environmental factors.
Current practices to improve nutritional intake in malnourished
older adults i.e. dietary advice, meal fortification, variety, betweenmeal snacks and frequent small meals, and Oral Nutritional
Supplements were also reviewed.
3.1. Factors influencing nutritional intake
Nutritional intake is influenced by multiple factors that will be
discussed below. In Table 1 these factors are summarized.
3.1.1. Personal factors
3.1.1.1. Satiety. Voluntary nutritional intake is governed by
a complex system of interactions of the senses, the digestive tract,
the central nervous system and gut hormones that are known to be
involved in the ‘‘satiety cascade’’.14 According to the ideas underlying the satiety cascade, nutritional intake is regulated by two main
physiological processes: satiation (that leads the subject to stop
eating) and satiety (which controls the interval between two
successive meals). The balance between these two processes
determines energy intake and therefore affects energy balance.
Foods produce their satiation and satiety affects as a result of a series
of anticipatory sensory (i.e. palatability), cognitive (i.e. expectations
with regard to food consumed), pre-absorptive (i.e. gastric filling
and distension) and post-absorptive (i.e. nutrients and hormones in
circulation) processes.14
Environmental Living alone
Social isolation
Meal interrupting
procedures
Lack of help with eating
Inappropriate mealtimes
Good health
Motivation
Distraction (e.g. TV watching)
Convenience/easy access to food
Encouragement by care givers
Sharing a meal with other
people/ambiance
Eating at the same
time every day
One hormone especially associated with the satiety cascade is
the appetite suppressing cholecystokinin (CCK). CCK is released
from the endocrine cells in the intestine, and older adults seem to
be more sensitive to this satiety-associated hormone than younger
people.15 This may partially explain the rapid satiation and reduced
food intake in older adults.
3.1.1.2. Anorexia of aging. The average food intake drops by about
25% from 40 to 70 years of age. The reduction of energy intake
between 20 and 80 years of age can be as high as 1300 kCal/day for
men and 600 kCal/day for women, respectively. This phenomenon
is sometimes called the ‘‘anorexia of ageing’’.12 Because reduction in
nutritional intake is only partly balanced by reductions in energy
expenditure,16 older individuals generally lose weight,17 and
specifically lose muscle weight (sarcopenia).18 On average older
adults eat more slowly, are less hungry, less thirsty, have lower
sensory acuity, consume smaller meals, snack less between
meals14,19,20 and have lower energy intakes than younger adults.12,21
With aging people increasingly suffer from functional disabilities like poor dentition, impaired vision, Alzheimer’s disease,
dementia, psychological problems such as depression, and social
changes (e.g. isolation and living alone).17 Dementia and amnesia
greatly influence feeding behaviour. People with dementia may
experience depression and lack of appetite, they may forget ‘‘how’’
to eat and/or eat inappropriate substances or amounts of foods.22
Loss of taste and olfaction are common as a result of aging because
of functional changes in taste bud number and structure, dry mouth
and throat, disease states associated with aging, medications, surgical
interventions and environmental exposure.23–26 Over 60% of adults
between 60 and 80 years have major olfactory deficits and above 80
years this increases to over 80%.25 Intact senses of taste and smell are
necessary for the cephalic phase of digestion, which is the initial
increase in salivary, gastric, pancreatic, and intestinal secretions, that
all contribute to the initiation of digestion.17,27,28 Older adults, often
have a lower salivary response,26 and dissatisfaction with the ability
to taste food is associated with dry mouth during chewing.29
Age-related changes in gut function, including dyspepsia,
hypochlorhydria (reduced secretion of hydrochloric acid in the
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W.F. Nieuwenhuizen et al. / Clinical Nutrition 29 (2010) 160–169
stomach), smaller and thicker villi, a decrease of mucosal surface,
quicker filling of the distal gastric antrum, and slower gastric
emptying17,19,22,26,28,30,31 also influence nutritional intake, digestion and nutrient absorption. In addition CCK levels are higher and
satiety lasts longer in older adults.28
A good example for the age-related impairment in the regulation of food intake is shown in Fig. 1. A preload is a food item or
drink that is consumed before a main meal. Older men consumed
significantly less energy at lunch than the younger men after
yoghurt preloads varying in energy and macronutrient content.
Lower intake was associated with subjective sensations of satiety;
visual analog scale ratings indicated that the older men were less
hungry and more full at the start of lunch, compared to younger
men. Strikingly, although older men felt fuller, compensation for
energy in the preloads was less precise in the older than in the
younger men, therefore older men consistently overate at the selfselected lunch. Younger men consumed about 10% more total
energy (lunch þ yogurt) in the yogurt preload conditions compared
with their baseline intake; older men overate between 10% and 30%
in relation to their baseline intake.32
Intragastric mechanisms rather than nutrient-mediated small
intestinal feedback may play a key role in the anorexia of aging
since the infusion of glucose and lipids in the small intestine of
healthy elders (65–75 years old) did not evoke satiety.31 The role of
gastric feedback is corroborated by the observation that older
adults (60–84 years old) were more satiated after a meal or water
preload than younger adults (21–50 years old), and by the observation that postprandial hunger was inversely related to the rate of
gastric emptying.33–35
Older adults are less able to recover after a period of undernutrition. This was shown in a 6-month study with healthy older
(mean age 68 years) and younger (mean age 26 years) adults,
who voluntarily reduced their daily energy intake by approximately 1000 kCal/day during 6 weeks. The older adults were less
able to increase their nutritional intake over at least 6 months
following this underfeeding period compared to the young, and
regained only 64% of the weight they lost during the experimental period.36
In Fig. 2 the personal factors causing malnutrition are
summarized.
3.1.2. Food factors
3.1.2.1. Macronutrients and fibres
3.1.2.1.1. Protein. It is well established that the degree of satiety
per calorie caused by isolated macronutrients is in the order protein > carbohydrate > fat.37,38 The satiating effect of proteins may
be weaker in liquid products, even with substantial loads, in
healthy younger adults,39 but these data are not univocal.40
3.1.2.1.2. Carbohydrate. An important factor affecting appetite
and nutritional intake appears to be the rate of glucose release into
the blood stream in response to a food i.e. its glycaemic index (GI).
The GI of a food depends on the amount and type of carbohydrate,
the macronutrient composition, and the presence of dietary fibre.41
The majority of studies (not looking at older adults) support an
increased short-term satiety by low GI foods.41 Energy intake can
be increased by 29–53% by high GI foods or liquid preloads
compared with low GI ones.42
3.1.2.1.3. Fat. Fat is the least satiating macronutrient. Monounsaturated fatty acids (MUFAs, e.g. oleic acid) have a lower satiating effect than saturated and long-chain polyunsaturated fatty
acids (LCPUFAs, e.g. linoleic acid). Medium chain triglycerides
(MCTs) are more satiating than long-chain triglycerides (LCTs). In
contrast to LCTs, MCTs are not easily stored in the body but are
oxidized and ketone bodies are formed, which can induce satiety.
LCPUFAs have been reported to induce the production of the
satiety-inducing peptides PYY and CCK.37,43,44 The PYY stimulation
by LCPUFAs has, however, been questioned.45
3.1.2.1.4. Fibre. Water-binding viscous gelling fibres (e.g. guar
gum, pectin) and insoluble fibres are more satiating than soluble
fibres. Water-binding fibres slow down gastric emptying and/or
intestinal absorption of nutrients and thus influence the secretion
of satiety hormones, increase the volume of the alimentary bolus
and stimulate the receptors sensitive to gastric distension.14 The
water-holding capacity of a food in the gut may thus greatly
influence nutritional intake.37
3.1.2.2. Taste, variety, palatability and sensory-specific satiety.
Flavour perception has been identified as one of the main drivers of
nutritional intake.38,46 Older adults rate flavour as the strongest
determinant of their food choices.47 Taste perception decreases
with age and thresholds for sweet (e.g. sucrose, aspartame) and
umami (e.g. inosine 50 -monophosphate, sodium glutamate) have
been reported to be approximately 1.3 and 5.7 times higher for
healthy elderly (60–75 years) than for healthy younger adults
(19–33 years).48 It has been shown that for community dwelling
older women (65–93 years) loss of smell (i.e. diminished flavour
perception) resulted in a lower interest in food-related activities
(e.g. cooking, eating a varied diet) and in higher intakes of sweets
and fat.49 Flavour enhanced foods seem to be liked better by older
adults,17,50 and can increase nutritional intake in institutionalized
elderly (84.6 0.8 years).51 In a 3-day study with 14 older hospitalized patients, food intake was improved by 13–26% by using
regular foods with added natural flavours.52 Therefore, to counter
the loss of taste perception in older adults, foods with richer tastes
and relatively strong but appetizing smells may need to be
developed.
Fig. 1. Mean (SEM) total energy intake at lunch 30 min after: no preload, after a 500 g (229 kcal) yoghurt preload, after a 500 g (508 kcal) high fat yoghurt preload, and after
a 500 g (508 kcal) high carbohydrate preload in younger adults (n ¼ 16, 18–35 years) and older adults (n ¼ 16, 60–84 years). (Figure was adapted from32).
W.F. Nieuwenhuizen et al. / Clinical Nutrition 29 (2010) 160–169
163
Social changes
• social isolation
– living alone
– eating alone
• poverty
• reliance on others
Physiological changes
• functional disabilities
– impaired vision
– dementia incl. Alzheimer;
amnesia; forgetting to eat
– general functional difficulties
(shopping etc.)
• oronasal
– poor dentition, hence poor
mastication
– dry mouth
– impaired taste and olfactory
sensitivities
Eating process
• slower eating
• less snacking
• less dietary variety
Decreased food intake
• calories
• nutrients
• foods & drinks
Malnutrition
• GI
– slower gastric emptying
– impaired gut function
• satiety
–
–
–
–
more sensitive to CCK
more rapid and longer satiation
less hungry
less thirsty
Psychological problems
• depression
• foods are less liked
• less motivation to eat
Fig. 2. Personal factors causing malnutrition in older adults.
Also the appearance and palatability of foods determine the
magnitude of voluntary nutritional intake.53 The palatability of
a food i.e. how pleasant and desirable the food is considered to be,
is determined by prior experience with that food coupled with
sensory properties such as temperature, appearance, smell, taste,
texture, the physical state, aftertaste and afterfeel. Palatability can
also be influenced by the sensory capacities and metabolic state of
the individual and the environment in which the food is
consumed. The subjective palatability of a food tends to decline as
it is eaten. This phenomenon is called ‘‘sensory-specific satiety’’,53
or more accurately sensory-specific satiation (SSS), and refers to
the decrease in liking of a food eaten within a meal in comparison
to other foods that are tasted but not eaten. SSS is primarily
related to the sensory stimulation caused by a food, and not to the
post-absorptive effects of the food. Interestingly, older adults
(65–82 years) are less sensitive to SSS than younger adults,54
which may partly explain the reduction in dietary variety in
older adults.55,56
Energy intake can be raised by offering more variety, even for
foods with the same macronutrient composition.53,57,58 Hollis et al.
have shown that older adults (mean age 70 years), like young adults
consumed more from a varied four course sandwich meal than
from a similar four course monotonous sandwich meal.59 One study
has shown that community dwelling older men and women (60–75
years) consumed more varied diets than younger individuals
(20–30 years). Most studies show the opposite i.e. less variety with
aging. Dietary variety tends to decline with increasing age,60 and it
has been shown that over two thirds of institutionalized people
over 65 years had changed their diets, restricted their food choices
and reduced food intake.61,62
A palatable food can lead to a more rapid return of appetite and
can increase nutritional and energy intake in the short-to-medium
term. Up to 44% higher nutritional intake has been reported using
palatable foods in comparison to less palatable foods.46 Highly
palatable foods override satiation signals and stimulate the reward
system.63
Sensory stimuli act as ‘‘a gatekeeper of acceptability’’ for foods.53
Until recently, the sensory attributes of food were the most
important signals of the probable nutrient contents of the food.53
There is evidence that sensory factors can increase the intake of fat
and carbohydrate in the short-to-medium term.53
3.1.2.3. Energy density. It has been shown that perception of fullness and satiety are linearly associated with postprandial gastric
volumes.64 Under well-controlled laboratory conditions individuals
appear to eat a constant volume and not constant energy. Rolls and
colleagues have demonstrated that liquids with identical energy
and macronutrient content have a greater satiating effect when
their volume and weight are increased by the addition of water.
Even increasing volume by incorporating air (>150 mL) transiently
reduced subjective appetite and nutritional intake at a meal served
30 min later.65
The energy density (ED) of a food depends on the concentration
and nature of its nutrients. The ED of a food is largely determined by
its water and fat content, as protein and digestible carbohydrates
each contribute 4 kCal/g and lipids 9 kCal/g to the energy content of
a food. High fat diets are least satiating and can lead to ‘‘passive
overconsumption’’.53 Energy intake is stimulated by energy dense
sweet and high fat foods, most likely as a result of the combination
of palatability and high energy density.53
A study which analyzed the 7-day dietary reports of 669 freeliving normal adults using a computer model of stomach emptying
of solids and fluid movements, indicated that short-term intake is
controlled by the food’s weight and volume as opposed to the
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energy density i.e. short-term nutritional intake regulation may
occur on the basis of stomach filling.66 Other studies have also
shown that nutritional intake is influenced by cues related to the
weight and volume, i.e. high ED leads to higher energy intake in the
short-term.67–70 In a study with healthy individuals the gastric
emptying rate after the ingestion of liquids differing in ED, but of
similar volumes and osmolarities, is mainly a function of ED i.e.
gastric emptying is slower for foods with higher EDs.71
High energy dense foods tend to be more palatable, but people
may learn to consume them in smaller portion sizes as in the
longer-term the perceived palatability of a food is strongly influenced by its post-ingestive consequences72 (e.g. gastric distension
and emptying rates). The effects of ED on energy intake of a single
meal cannot be extrapolated directly to longer effects on energy
intake and long-term effects of dietary ED can only be estimated.73
The fullness after a meal may predict long-term energy intake,
and fullness in response to a fixed load may be useful to predict
subsequent and total energy intake.74 It is reasonable to assume
that smaller volume preloads result in reduced feelings of fullness,
and hence subsequent, voluntary energy intake will increase.
3.1.2.4. Portion size and volume. Increased portion sizes lead to
increased nutritional intake in healthy young adults.14 A study with
healthy volunteers indicated that individuals mainly monitor the
weight of the food ingested i.e. foods with higher energy density
increased nutrient intake in the short-term.70 Therefore small
volumes in combination with high energy densities are likely to
help improve intake.
Eating preferences and habits are learned, and as a consequence
the weight and volume of a product become associated with energy
value and nutrient content. Novel diets result in little compensatory response in the short-to-medium term, if the time is too short
to learn to associate the sensory attributes to the post-ingestive
consequences. In other words people anticipate the post-ingestive
effects of a new food to be the same as that of a similar known
food.37
Another important mechanism that affects food intake is the
decrease in the liking of a food during a meal. This decrease in liking
is affected more by the volume of a food than by the energy density
of a food.75 Therefore high ED can lead to higher nutritional and
energy intakes than low ED foods.
Large portions, or indeed a perceived large portion size may be
overwhelming and may actually discourage intake in people who
have problems to reach sufficient nutritional intake.13 Package size
can also influence the amount of food that is consumed. People may
believe that smaller quantities of a product are ‘‘acceptable’’ as their
consumption may be perceived as easier to self regulate. Small, and
even small-looking, packages can thus contribute to increase
consumption.76 The latter has been shown in a study with teenagers with different designs of drinking glasses with the same
volume.58 We therefore hypothesize that people who are required
to increase nutritional intake because they suffer from malnutrition, may benefit from simply being offered frequent small servings
of foods they like.
The ED and portion size of foods can also influence nutritional
intake simultaneously. With energy dense foods satiation (i.e. meal
termination) is reached after the intake of more energy. The
opposite is true for water-rich low energy dense foods where
satiation is reached after the intake of less energy. Water has to be
incorporated into the meal (and not merely included by drinking
a glass of water alongside the meal) to have the greatest effect on
nutritional intake. The mechanisms by which these factors influence nutritional intake are not clear, but may very well include
cognitive and orosensory factors as well as physiological controls
related to gastric distension and gastric emptying.77 This may also
apply to malnourished older adults: consuming energy dense foods
(i.e. smaller volumes) from a small packaging or from a serving aid
(e.g. glass) that looks small may help to increase intake.
3.1.2.5. Liquid vs. solid foods. Epidemiological data indicate that
caloric (clear) beverage consumption is positively associated with
energy intake and body mass index. There is now compelling
evidence that the liquid state, rather than energy form or nutrient
composition, is responsible for this phenomenon.78,79
Although soups are basically liquids, they are more satiating
than other liquids. The explanation given for this is that consumers
expect soups to be filling, in part because they are warm.80
However this is not in agreement with the observation that hot or
warm vegetable juice preloads did not affect food intake by healthy
young individuals.81
Postprandial hunger was lower in older adults (overweight and
underweight) following a solid meal replacement (i.e. meal replacement bars) than after a liquid meal replacement (i.e. shakes). In spite
of the higher protein and fibre content and the lower fat content of
the liquid, less reduction in hunger and desire to eat was observed.82
In another study with healthy older adults (50–80 years) the
consumption of a single liquid meal replacement blunted the
postprandial decline in hunger and a higher (þ13.4%) nutritional
intake was observed in the subsequent meal compared to a solid
meal replacement.83
Meal replacement beverages aimed at promoting weight loss
have been developed to promote satiation and satiety, but their
satiety value is still lower than that of solid foods. Hence, it is
unlikely that liquid meals will replace another eating occasion and
may even increase energy intake.84
The absence of mastication prior to swallowing has been
proposed as an explanation for the lower satiety of liquids. This
may be due to a decrease in pancreatic exocrine and endocrine
responses in the absence of chewing. In addition liquids empty
from the stomach more quickly than solid foods and may induce
weaker signals in the gastrointestinal tract that would otherwise
lead to inhibition of further nutritional intake.85 There are also
studies that show the opposite i.e. liquids are more satiating than
solids, or liquid preloads have no effect on subsequent nutritional
intake. An explanation for this apparent discrepancy may be the
difference in the delay between preload and meal for studies with
solid preloads (2–4 h) vs. liquid preloads (0–30 min). It has been
suggested that the use of high volume liquids consumed close to
a meal may promote energy compensation, whereas liquids
consumed between meals do not.85,86
The physical state of a food (solid vs. liquid) has an effect on
voluntary nutritional intake, but the effect may vary depending on
the subject and food. One of the factors contributing to this variability may be related to the mouth-wetting characteristics, and
may be reflected in a shift in the acceptability of a food when the
mouth becomes dry. Mouth wetting is stimulated by cold and
acidity and can be regarded as ‘‘thirst-quenching’’. Changes in saliva
glands and mouth feel in older adults may explain why they report
feeling less thirsty than young adults. Drinks that elicit saliva
production (e.g. acidic and cold) are likely to quench thirst and be
more sensitive to hedonic shifts caused by increases in mouth
dryness, and could therefore very well be consumed in greater
quantities.87
3.1.2.6. Viscosity. The viscosity of a liquid also influences satiety i.e.
viscous liquids are more satiating. For example, with milkshakes
matched in volume, weight, temperature, energy, taste and
macronutrients, but with different viscosities, the most viscous
liquids were most satiating. They did, however, not affect 24 h food
intake in healthy volunteers. The enhanced satiety may be explained
W.F. Nieuwenhuizen et al. / Clinical Nutrition 29 (2010) 160–169
by orosensory effects of viscous liquids and not by their postingestive effects since subsequent food intake was not affected.88,89
3.1.3. Environmental factors
Nutritional intake is also influenced by environmental factors,
i.e. factors that are not directly related to the food composition or
subject. These factors include time, social environment, eating
environment (e.g. atmosphere, eating effort, eating with others),
culture, presentation (e.g. shape of plates, glasses and bowls), staff
and carers.58,90 Also, the effort needed to eat i.e. the ease, access or
convenience with which a food can be consumed has a strong
influence on consumption. Packaging also influences food intake
since it provides discrete stopping points during a meal and may
influence whether or not to continue eating.58
3.1.3.1. Timing. Although ‘‘hunger’’ is the physiological signal that
motivates people to start eating, most people do not wait until they
feel hungry to initiate a meal. Most meal episodes take place in
anticipation of hunger and energy deficit. Environmental factors,
such as usual meal time, account for 80% of nutritional intakes, and
hunger for only 20%.14
3.1.3.2. Social isolation. Humans are social beings that normally eat
in groups. An increased frequency of eating alone may be one of the
factors contributing to low energy intake in older adults.91 Living
and eating alone diminish food consumption and dietary quality in
older adults, with older men living alone seeming to be particularly
vulnerable to poorer dietary intake.92
3.1.3.3. Encouragement, help with eating and interruptions. Many
patients need encouragement to eat and simple things like
encouraging family members to visit at mealtimes, making sure
eating is not interrupted by procedures, sufficient staff, assisting
with eating if needed and meeting a patient’s food preferences have
been proposed to ensure sufficient nutritional intake. In practice,
however, mealtimes are often regarded as another task to be
completed and so receive inadequate attention.22 We think that this
may be attributed to the low priority of nutrition within medical
contexts or lack of understanding of the importance of good nutrition for immunocompetence and a better response to treatment.
3.1.3.4. Ambiance. Ambiance characteristics like temperature,
lighting, odour and noise influence the immediate eating environment. For example low temperatures and soft lighting may
increase nutritional intake. Eating with familiar people or watching
other people eat can lead to an extended meal. The meal size can
increase by up to 96% if meals are eaten with several people.58
Two studies in nursing homes have shown that by simply
improving the eating environment and atmosphere of the dining
room (e.g. decoration with flowers, soft music, table cloths, removal
of trays, full cutlery, eating together and staff sitting and eating at
the same table, undisturbed eating, medications provided before
meals to separate medication from nutrition), nutritional intake
was improved (þ236 kCal/day), the percentage malnourished
(MNA score) patients decreased (17%), quality of life improved
(þ6.1 units) and body mass improved significantly (1.5–3.3 kg).93,94
3.2. Current practices to improve nutritional intake in
malnourished older adults
The success of nutritional support depends in part on the efficacy of the nutrients, but also on the compliance to the prescription
or recommended intake. Current practices to increase nutritional
intake by older adults are discussed below (see also Table 2).
165
3.2.1. Dietary advice
Dietary advice is frequently recommended as the first means
of nutritional intervention. Although such an approach may
increase energy (and potentially protein) intakes, other nutrients
such as fibres and micronutrients may be compromised. There is
a lack of clinical data supporting dietary advice to treat
malnutrition.95
3.2.2. Meal fortification
Meal fortification can improve energy (þ26%) and protein
(þ23%) intake in hospitalized older adults.96 The use of a sauce with
a meal can increase energy intake of protein and fat in older adults
without affecting pre-meal hunger, desire to eat, or post-meal
pleasantness.97 Other examples include studies that provided
hospitalized older patients with smaller, protein and fat fortified,
more palatable menus. Total energy intake was improved by 14–
25%, but protein intake was not always improved and energy
intakes remained below recommended levels.5,98 In other meal
fortification studies the improved nutritional intake was also
shown to be mainly due to a higher intake of (saturated) fat.99,100
Another study with institutionalized older adults showed that meal
fortification was not sufficient to alleviate malnutrion.101
3.2.3. Variety
It is well established that variety can stimulate food intake in
healthy younger individuals whereas that monotonous diets tend
to decrease intake.102,103
Older adults on a monotonous liquid diet for 5 days had
significantly less cravings (intense desire or longing to eat
a particular food)55 for foods with different sensory qualities than
young subjects.55 Also people with a better sense of smell had more
cravings during the monotonous liquid diet than those with poor
smell.55 Older adults often fail to respond to dietary monotony (for
example eating more plain sandwiches than younger adults59) and
this may partly explain their higher risk to consume nutritionally
inadequate diets. Older adults therefore need to be encouraged to
have adequate variety in their diets,55 as this may help to maintain
an optimal nutritional balance.
3.2.4. Between-meal snacks and frequent small meals
Small meals or between-meal snacks have been used to improve
nutritional intake. For example, frail malnourished hospital patients
who received two between-meal snacks per day, increased intake
by 600 kCal/day and 12 g protein/day compared to routine care, and
had a shorter length of stay.104 Older adults do not compensate as
much as younger adults for between meal supplementation and
a feeding regime that offers small snacks or between-meal snacks
may promote extra nutritional intake.32
3.2.5. Oral Nutritional Supplements
Oral Nutritional Supplements (ONS) are liquid foods that are
used to improve nutritional intake in older adults and patients with
Table 2
Current practices to improve nutritional intake by older adults and their efficacy.
Practice to improve intake
Effectiveness on energy and nutritional intake
Dietary advice
Meal fortification
Lack of sufficient supporting clinical data.
Nutrient and energy intake often below
recommended levels. Can result in
elevated saturated fat intake.
No strong data available, but it may
stimulate energy intake and help to
maintain nutritional balance.
Increases overall nutritional intake.
Significantly increases nutritional and
energy intake and improves clinical outcomes.
Variety of diets
Between-meal snacks
Oral Nutritional Supplements
(ONS)
166
W.F. Nieuwenhuizen et al. / Clinical Nutrition 29 (2010) 160–169
a variety of health and eating problems. The importance of enteral
nutrition (tube and ONS) as a means of artificial nutritional support
has been elaborated.105,106 In a wide variety of hospital and
community patients, the use of ONS has been shown to improve
energy and nutrient intake (see Fig. 3), increase body weight and
functional outcomes, reduce mortality and complications, and
reduce length of stay in hospitalized patients when compared with
routine clinical care.6
A meta analysis of 24 trials (2387 patients) on oral protein and
energy supplementation in older adults, showed that ONS reduced
mortality and that this was consistently significant in undernourished older adults (>75 years) who were offered 400 kCal/day in
the supplement for 35 days, and when patients were hospitalized.
Also the length of stay was approximately 6 days shorter, although
this did not reach statistical significance. Body weight increased
significantly (þ2.4%) when ONS was used.107
In malnourished older adults ONS have been shown to be
consistently beneficial and to be superior to dietary counselling for
malnourished patients with digestive diseases.108 Studies in older
adults have shown that ONS in-between meals reduced feelings of
hunger between meals, but that voluntary energy intake was
improved, thus offering a solution to treat malnourished older
adults.109
In line with these analyses, the authors of a recent Cochrane
meta analysis concluded that dietary advice plus ONS may be more
effective than dietary advice alone, since evidence is lacking to treat
illness-related malnutrition with dietary advice only. Positive
effects of ONS were found on body weight, but not on mortality.95
ONS were found to provide significantly greater energy and
protein than isocaloric food snacks throughout a 7-day period
(P < 0.02),110 suggesting they are a more effective method of
supplying energy and protein to patients. This was further
confirmed when total intake (including food and ONS/snack intake)
was measured, with the ONS group having significantly greater
energy (mean difference of 314 kCal/day; P < 0.03) and protein
(mean difference 14.1 g protein/day; P < 0.01) intakes over the
same period of time.111 Mean hunger, desire to eat, pleasantness
and satisfaction ratings did not significantly differ between the
groups.111 This indicated that not only did ONS supply more energy
and protein than isocaloric snacks, but that the total overall energy,
protein and other nutrient intake (including ONS/snacks) had
significantly increased.111
Liquid supplements are preferred to solids as with liquids gastric
emptying time is quicker and total caloric intake is more likely to be
improved.13 Liquid supplements given between meals should
prevent compensation at the next meal.
When smaller volume ONS were given to older hospitalized
patients (3 120 mL at 8.00 AM, 2.00 PM, and 6.00 PM) and intake
was monitored by the nurses, overall compliance was good and
dietary intake increased with up to 540 kCal per day, but the
amount of supplement prescribed did not ensure minimum energy
requirements were met in all patients.42,112 This can be explained
by the low energy and nutrient density of the ONS used in this
study.
The importance of the prescribed volume was shown in a study
where patients receiving 200 mL sip-feeds per day consumed 64%
of the prescribed amount (mean 129 mL), whereas patients
receiving 400 mL sip-feeds per day consumed 53% of the total
prescribed volume (mean 211 mL/day).113
Compliance was found to increase (95%) when small volumes
(4 60 mL daily) of energy and protein dense ONS were offered
between the main meals to older adults (83.3–84.5 years) at
nutritional risk and admitted to hospital for acute care.114 Normal
practice with less nutritionally dense ONS resulted in lower
compliance (estimated 35–60%).114 In the small volume energy
dense ONS group, a higher number of meals were consumed,
protein intake and weight increased, duration of stay in the hospital
decreased and there was small but insignificant increase in
appetite.114
A randomized controlled parallel study has shown that total
daily energy intake can be significantly increased (þ415 kCal) by
daily supplementation of a small volume high energy dense high fat
supplement (400 kCal in 3 30 mL) to 84 7 year old community
based patients (BMI 20.9 3.9 kg/m2), whereas in the dietary
advice control group an increase of þ 264 kCal was achieved.115 In
elders at risk of malnutrition, the use of energy dense supplements
can improve total energy intake without suppressing voluntary
food intake.115
Milne et al. reported that ONS are routinely given to hospitalized elderly, and that ONS are effective in increasing both energy
and protein intake. However, frail older adults have low intakes and
can find it difficult to consume ONS, to the extent that even with
extra feeding by trained staff their nutritional status is not
improved.107
Fig. 3. Summary of results for total energy intake from hospital and community trials of ONS (Figure was adapted from6).
W.F. Nieuwenhuizen et al. / Clinical Nutrition 29 (2010) 160–169
Also limited staffing in long-term care and nursing homes may
result in inappropriate dispensing of the supplements and/or little
assistance to encourage consumption to frail and dependent
residents. It has been reported that staff spend less than 1 min per
person to encourage consumption of a nutritional supplement or
meal. In one study only 75% of oral liquid supplements were
dispensed and only 55% of the residents consumed the supplement.116 ONS provided in nursing homes are often not supplied
according to the treatment scheme,117 and wastage of nutritional
supplements may be considerable.113,118,119 The encouragement,
food intake control, and support from health care professionals112,120 all influence compliance. In addition, a structured
approach e.g. distribution of the supplements by the nursing staff
at medication rounds (i.e. regular timing), may improve
compliance.42
No studies investigating the effect of variety on intake of ONS
have yet been reported, however as discussed above, increasing
sensory variety (form, flavour, texture etc) of foods has been shown
to increase consumption, energy and protein intake and desire to
eat in healthy adults.102,103,121,122
It is therefore generally accepted that offering a variety of
supplements with different sensory characteristics (appearance,
flavour, texture, consistency and composition) are likely to improve
compliance and intake more than when only one type of supplement is used, especially for longer-term use when ‘taste fatigue’ can
develop. Recently ESPEN supported this theory and stated that
variety and alteration of taste (different flavours, temperature and
consistency) are important to achieve increased energy and
nutrient intake with ONS in older patients.123
4. Conclusion
From the evidence reviewed here, it is clear that improving
nutritional intake in older adults in need of nutritional support is
a multifactorial problem. We have identified 37 factors affecting
nutritional intake that can be divided in three categories:
(1) Personal factors
Older adults undergo a series of social, physiological and
psychological changes that affect their eating process and ultimately their energy intake (Fig. 2). Older adults are more quickly
satiated, often suffer from olfactory dysfunction and are less
sensitive to sensory-specific satiation. As a result they are at risk of
insufficient or inadequate nutrient and energy intake. Older adults
do not fully compensate for in-between meal supplementation and
a feeding regime that offers small snacks in-between meals
therefore promotes extra nutritional intake in this age group. Oral
Nutritional Supplements are particularly suitable for this purpose,
as they are liquid and contain all necessary nutrients.
(2) Food factors
Food intake is limited by satiation and satiety, which are
affected, amongst others, by gastric distension and gastric
emptying. Although gastric emptying is somewhat slower for
energy dense foods, energy intake is higher for energy dense foods.
Proteins are the most satiating macronutrient, followed by
carbohydrates and fat. High glycaemic index (GI) carbohydrates
have a lower satiating effect than low GI ones. Fat has the highest
ED, and leads to highest energy intake. MUFAs have a smaller
satiating effect than PUFAs and MCT. Water-binding fibres increase
satiety and may thus reduce nutritional intake.
Studies have shown that palatability and variety increase intake
in the general population, and one publication suggest that this is
167
also true for older adults,59 although older adults may accept
monotonous diets more easily.55 Stimulating intake in older adults
can be achieved by in-between-meal snacks with high energy
density. Liquids are generally less satiating than solid foods,
therefore small volume liquid energy dense meals and/or supplements are most suitable to increase nutrient and energy intake by
patients and older adults.
(3) Environmental factors
By creating an ambiance that stimulates nutritional intake, the
nutritional status and quality of life of institutionalized older adults
can be significantly improved. This includes eating with familiar
others, encouragement by carers, and a pleasant eating environment.
The evidence summarized in this review also shows that
nutritional intake in older adults can be increased by various
methods including (1) improving the eating environment, (2)
motivation and help by carers, (3) dietary advice, (4) by using
fortified meals, and (5) by offering a variety of energy dense small
nutritious items (e.g. ONS) between the main meals.
Administering extra energy to older adults may be achieved by
food fortification in combination with between-meal snacks.
However, the dietary composition of fortified meals is often
unsatisfactory, with additional energy coming from high fat
intakes.
The largest body of evidence exists for the efficacy of ONS. Meta
analyses have clearly shown the positive effects of ONS on the
nutritional status of malnourished older adults. The use of ONS
increases nutritional intake and improves clinical outcomes as long
as compliance is sufficiently high. Compliance may be optimized by
offering variety, eating in groups and with small volume nutritionally dense ONS. Because the volume of ONS that needs to be
consumed to alleviate malnutrition may be too large for some
individuals, small volume, energy and nutrient dense ONS may
offer a solution.
The ideal ONS would be concentrated (i.e. small volume), have
a low satiation capacity and have only a short-term satiety effect,
hence would not lead to less intake during meals or across the day.
To help malnourished individuals improve their nutritional intake,
smaller volume, more energy and nutrient dense ONS than
currently available, in-between meals may offer a solution.
Conflict of interest statement
Willem F. Nieuwenhuizen, Hugo Weenen, Paul Rigby are
employees of Danone, a supplier of ONS. This work was funded by
Danone Research, Center for Specialised Nutrition, Wageningen The
Netherlands.
Statement of authorship and author agreement
WFN, HW, PR and MMH analyzed scientific studies used in this
review and wrote the manuscript together. All authors read and
approved the final manuscript.
Acknowledgements
We gratefully acknowledge Willemijn van Schuppen and Jennifer Hall for literature searches used in this review.
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