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Nutrition in Older Adults Topic 36

Module 36.1

Epidemiology, Aetiology and Consequences


of Malnutrition in Older Adults

Tommy Cederholm
Department of Public Health and Caring Sciences,
Clinical Nutrition and Metabolism
Department of Geriatrics, Uppsala University Hospital
Uppsala University, Uppsala, Sweden

Learning Objectives

To know the prevalence of malnutrition according to the subjects life setting;


To know the major reasons for malnutrition in the older adult;
To know the main medical consequences of malnutrition.

Contents

1. Introduction
2. What is the prevalence of malnutrition in older adults living in the community, in
nursing homes, and when they are hospitalised?
3. Aetiology of malnutrition in older adult
4. What are the consequences of malnutrition in older adults?
5. What about micronutrients?
6. Summary
7. References

Key Messages

The prevalence of proteinenergy malnutrition (PEM) varies according to residency


and the clinical setting. Up to 5% of community-dwelling older adults, 20-40% of
nursing home residents and 20-50% of hospitalised older patients are reported to be
undernourished;
The reason for malnutrition is a mix of age-related, medical and socio-psychological
factors. Inflammation induces anorexia, muscle wasting and energy depletion. Poor
dental status and medication, as well as cognitive impairment, depression and
bereavement contribute;
PEM is associated with increased morbidity, mortality and longer hospital stays.
Malnutrition also increases the risk for hip fractures, infections and pressure ulcers;
Older subjects are at risk of micronutrient deficiency (eg vitamin D and vitamin B12).
Vitamin D deficiency increases the risk for osteoporosis and fractures.

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1. Introduction

There is a physiological decline in food intake from the ages of 20 to 80 years (1).
This has been termed the "anorexia of ageing" and may be an appropriate response to
the decreases in lean body mass, energy expenditure and physical activity that occur
over the lifespan (2). Ageing is a degenerative process driven by diseases, oxidative
damage, anabolic resistance and increased catabolism, which places older men and
women at high risk of developing pathological weight loss and eventually malnutrition.

2. What is the Prevalence of Malnutrition in Older Adults Living in


the Community, in Nursing Homes, and When They are
Hospitalised?

The estimation of the prevalence of malnutrition in older subjects depends on the


tools used to evaluate the nutritional status, and on the setting of the studied population.
Assessment tools are usually combinations of anthropometry (body mass index), reports
of recent weight loss, eating difficulties, and sometimes biochemical markers. The Mini
Nutritional Assessment (MNA) is an example of a composite nutritional evaluation tool
that is often used in older populations (3). Studies have been performed in older subjects
living at home, in nursing homes and in hospitalised older patients. From several
prevalence studies it can be deduced that about 5% of community-living older adults,
20-40% of nursing home residents and 20-50% of hospitalized older adults are
malnourished (4,5). The population-based Euronut-SENECA study in 2600 subjects aged
70-75 years from 12 countries in Europe showed that 10% of the subjects had a body
mass index (BMI) <20 kg/m2 (6). Malnutrition becomes more frequent in populations
with higher morbidity and care burden. About 8% of home-living older adults who
needed help from domiciliary care services displayed malnutrition (7). Unintentional
weight loss is reported in about 10% of free-living older subjects (8), and in up to 25%
of functionally dependent home-living older persons (9).
Nursing home residents are usually frail, and show concurrent co-morbidities and
cognitive decline. The care burden in such settings varies with social and cultural context,
which is reflected in large variations in prevalence figures for malnutrition. Thus, ranges
from 20% to 40% are reported (4, 10, 11). The National Diet and Nutrition Survey,
based on 1368 subjects aged 65 and over, showed that 21% of institutionalised persons
were undernourished, based on a composite measure of low BMI and recent weight loss
(12). The NutritionDay initiative was recently extended to nursing homes and the first
report from >2000 residents in Austrian and German settings disclosed staff-assessed
malnutrition in 10%, and BMI <20 kg/m2 in 17% (13). High age, immobility, dementia
and dysphagia were independent risk factors for malnutrition. When close to all of the
institutionalized older adults of Helsinki were assessed by MNA only 10% came out as
well-nourished (14). In a comparison of nutritional status of nursing home residents in
the same Swedish community in 1996 and 2010 the prevalence of malnutrition had
fallen, residents were older and heavier, but still only 7% were assessed as well-
nourished (15).
In the hospital, the prevalence of malnutrition is reported to be even higher; i.e.
20-50% depending on the type of ward or assessment tools that are used (4, 16, 17).
One third of patients hospitalised in a geriatric unit had a BMI <20 kg/m 2 (18). Among
sub-acute-care older patients, 18% had a BMI <19 kg/m2, and 53% of the subjects had
albuminaemia <35 g/L (19). Albuminaemia as an indicator of malnutrition has been
questioned as it is mainly affected by ongoing inflammatory activity, but as such it
reflects catabolic activity.
Although the relative occurrence of malnutrition is lowest among the community-
living older adults, this group of adults make up the largest group of malnourished
individuals. For example it is estimated that in Europe 4 million community-dwelling older
people are malnourished compared to about 2.5 million malnourished in hospitals and
nursing homes.

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3. Aetiology of Malnutrition in Older Adult

Malnutrition/protein-energy malnutrition is an umbrella concept for various


conditions with somewhat different phenotypes and underlying mechanisms. For
example, cachexia is the disease-related inflammatory-driven catabolism (20), whereas
sarcopenia is the muscle loss and weakness partly following cachexia but also a separate
age-related condition (21). Frailty which is often observed in very old adults is loss of
organ reserves, weight loss and age-related weakness (22). Pure starvation due to
poverty or to natural catastrophes still occurs, mainly in the less developed part of the
world.
There are somatic as well as social and psychological reasons for reduced food
intake and increased catabolism. Disease-related malnutrition, i.e. cachexia, is driven by
the inflammatory response to the underlying disease. Ageing in itself is a low-grade
inflammatory condition, sometimes called inflamm-ageing (23). In combination with a
chronic disease this inflammation starts a number of catabolic actions, e.g. increased
expression of anorexic molecules in the brain as well as of proteolytic enzymes and
pathways like the ubiquitin-proteasome system. Proteolysis combined with insulin
resistance has strong muscle wasting effects. The combined inflammatory effect on the
bodys lipase systems results in overall lipolysis. Added to the inflammatory activities of
ageing and disease there are age-specific reductions in anabolic hormone secretion (e.g.
testosterone, estrogen, GH/IGF-1, DHEA). Free radicals (reactive oxidative species (ROS)
coming from energy production in the mitochondria causes oxidative damage for
example to mitochondrial DNA which is supposed then to trigger exaggerated cellular
apoptosis (24).
Cognitive impairment, dementia and depression are neurodegenerative and
neurological mechanisms behind malnutrition. Bereavement and reduced social networks
are also common causes for depression in the old.

4. What are the Consequences of Malnutrition in Older Adults?

Interestingly, health economic calculations performed by the British BAPEN


indicate that the societal costs from malnutrition are double that of obesity (25), half
emanating from direct hospital care and the other from increased needs for community
care.
Studies have consistently reported an association between morbidity and
mortality, and nutritional status in older subjects, as assessed by BMI, weight loss or
food intake (26). Recent large-scale prospective observational studies point to being
underweight as a stronger risk factor for death than obesity in older adults. In ~9200 70-
75 year-old Americans the highest 10-year survival was observed in those with a BMI
between 25 and 30 kg/m2. Mortality was higher among those with BMI <20 as compared
to those with BMI >35 kg/m2 (27). A similar 7-year follow-up study in ~13000 subjects
>65 years of age indicated that the least risk of disability was found if the BMI was ~25
kg/m2 at the start, whereas survival was highest if BMI was around 30 (28). In a
prospective community-based study including 247 men aged 65 and over, the annual
incidence of a weight loss of 4% or more was 13%. Although the weight-losing subjects
were similar to the non-weight losers for age, BMI, health status, albumin and
cholesterol measurements, they had a significantly greater 2-year mortality rate
(RR=2.43; 95% CI=1.344.41) (8). In 288 older patients receiving home help services,
weight loss was a significant predictor of mortality in a multivariate analysis including
age, sex, BMI, weight loss and functional status (RR=1.76; 95%CI 1.152.71) (29).
Mortality was studied as a function of BMI in 8428 hospitalised patients. In patients aged
20-40 years mortality doubled in the most underweight (BMI <18) compared to BMI
groups 20-40; however, in patients aged 70-79 years, there was a tripling in mortality
for BMI <18 compared to the BMI groups 32-40 (30) (Fig. 1).

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Fig. 1. Association between BMI and mortality as a function of age in 8428 hospitalised
patients. Reproduced from (30).

In 109 patients admitted to a geriatric rehabilitation unit, the best predictor of


mortality in the 1 year after admission and the 1 year after discharge from hospital was
the percentage of usual body weight lost in the year prior to admission (31). Pre-
admission weight loss was still predictive for mortality up to 4.5 years after discharge
(32). In 400 consecutive geriatric patients BMI was the strongest independent predictor
of 1-year mortality, a marker even stronger than diagnosis and age (33). Similarly, data
from the NutritionDay programme show that among the oldest hospitalized patients a
reduced food intake increased the 40-day mortality from <2% in those who ate all that
was served, to 16% among those who did not eat at all. The results remained significant
after adjustment for illness severity (34).
The immune system is sensitive to nutrient deprivation as it has a high cellular
turnover. Thus, immune suppression with an increased risk of infections is a hallmark of
malnutrition. This state is sometimes called MAIDS (Malnutrition Associated Immune
Deficiency Syndrome), and is in several aspects similar to the HIV-induced immune
deficiency syndrome (35). Episodes of sepsis occurred significantly more often in
severely undernourished hospitalised older patients as assessed by BMI and corrected
muscle area (36).
One prominent feature of malnutrition is loss of muscle mass, i.e. sarcopenia (21,
37). Weight loss in combination with muscle weakness makes up the diagnosis of frailty
(38). Sarcopenia combined with osteoporosis, another condition related to malnutrition,
paves the way to musculo-skeletal related incidents like gait disorders, falls and
fractures. The fracture incidence is further promoted by:
the effect of low protein and calcium intake and vitamin D depletion on bone mass;
the decrease in fat mass that would otherwise protect the bone in the case of a fall.
In the Study of Osteoporotic Fractures, 6700 women were weighed at baseline and after
a mean of 6 years. After adjustment for age, cigarette smoking, physical activity,
oestrogen use, medical conditions, health status, body weight, femoral neck bone mass,
and rate of change in calcaneal bone mass, the women who had lost weight had a
significantly increased risk of fracture of the proximal femur, pelvis and proximal
humerus (age adjusted RR per 10% decrease in weight: 1.68; 95% CI 1.172.41) (39).
Among 255 old hip-fracture patients >50% were malnourished or at risk according to
MNA, and the mortality rate was higher among the malnourished (40).

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Fig. 2. Hip fracture in an older undernourished patient

Malnutrition increases the risk of pressure sores (Fig. 3). Low protein and
energy intake, BMI and hypoalbuminaemia are risk factors for the development of
pressure sores in older patients (41, 42). Importantly, a meta-analysis of 4 clinical
studies showed that oral nutritional supplements could significantly reduce the incidence
of pressure ulcer development in at-risk patients (odds ratio 0.75, 95% CI 0.62-0.89)
(43).

Fig. 3. Stage 3 pressure sore in an undernourished older patient

Depression is a common cause of malnutrition. Depression is also an underrated


complication of malnutrition. An unexpected finding during the Minnesota Starvation
Study when 34 young men voluntarily starved for 6 months and lost 25% of their body
weight, was the observed changes in mood; i.e. depression, apathy and irritability (44).
These effects disappeared after nutritional repletion. It is most likely that this
observation is also valid in the older person.
All these negative consequences of malnutrition may partly account for the association
between malnutrition and poor quality of life in older persons (10, 45, 46).

5. What about Micronutrients?

Older persons are at risk of micronutrient deficiency. This may be due to low food
intake, chronic diseases or drugs. The Euronut-SENECA study reported in a population of
1005 subjects (aged 7479 years) that about 1/4 of the men and half of the women had
low dietary intakes or low plasma levels for at least one of the following micronutrients:

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calcium, iron, retinol, -carotene, thiamine, pyridoxine, vitamin C, cobalamin and vitamin
D (47). In institutionalised and in hospitalised older persons, the prevalence of
micronutrient deficiency appears to be higher, especially for thiamine, pyridoxine,
cobalamin, folate, vitamin C, vitamin E and selenium (48). Low calcium intake and low
vitamin D levels increase the risk of osteoporosis. Several intervention studies have
shown that the combination of calcium and vitamin D (at least 700 IU/d)
supplementation reduces the incidence of hip fractures in older populations (49, 50).
Almost all cells in the body express vitamin D receptors, indicating a wide spectrum of
potential effects from this vitamin. A meta-analysis indicates that vitamin D
supplementation reduces the incidence of falls in older adults (51). Although it is
suggested that vitamin D deficiency may play crucial roles in the development of
immunological, neurological and psychiatric disorders, a recent evidence-based expert
consensus from The American Institute of Medicine could not find sufficient data to
recommend vitamin D supplementation for purposes other than fracture prevention in
the older adult (52).
As in younger adults, severe micronutrient depletion leads to specific well-known
clinical symptoms and must be treated. However, in the older person, the micronutrient
deficiencies described are mostly mild, the consequences of which are difficult to assess.
Micronutrient intervention studies have shown conflicting results. Still, for older small-
eaters in care homes or in hospital, the risk of malnutrition readily justifies the use of
multivitamin supplementation.

6. Summary

Malnutrition is frequent (20-50%) in the hospitalized and institutionalized older


persons. Most malnourished old adults live in the community, although the prevalence of
malnutrition is less there (~5%). Age-related degenerative phenomena, as well as
medical catabolic processes like inflammation, interact with socio-psychological factors
like cognitive impairment and bereavement to make malnutrition a common condition in
the older adult. Malnutrition has adverse effects on morbidity (e.g. infections, fractures),
mortality, function (e.g. sarcopenia and frailty) and quality of life. Macronutrient and
micronutrient deficiencies both play important roles.

7. References

1. Wakimoto P, Block G. Dietary intake, dietary patterns, and changes with age: an
epidemiological perspective. J Gerontol A Biol Sci Med Sci 2001;56 Spec No 2:65-80.
2. Wilson MMG, Morley JE. Invited Review: Aging and energy balance. J Appl Physiol
2003;95:1728-1736.
3. Kondrup J, Allison SP, Elia M, Vellas B, Plauth M. Educational and Clinical Practice
Committee, European Society of Parenteral and Enteral Nutrition (ESPEN). ESPEN
guidelines for nutrition screening 2002. Clin Nutr 2003;22:415-21.
4. Kaiser MJ, Bauer JM, Rmsch C, Uter W, Guigoz Y, Cederholm T, Thomas DR,
Anthony P, Charlton KE, Maggio M, Tsai AC, Vellas B, Sieber CC for the MNA
International Group. Frequency of malnutrition in the elderly: A multinational
perspective using the Mini Nutritional Assessment (MNA ). J Am Ger Soc
2010;58:1734-8.
5. Tsai AC, Chang TL, Yang TW, Chang-Lee SN, Tsay SF. A modified mini nutritional
assessment without BMI predicts nutritional status of community-living elderly in
Taiwan. J Nutr Health Aging 2010;14:183-9.
6. Euronut-SENECA, a concerted action on nutrition and health in the European
community. Eur J Clin Nutr 1991;45 (suppl 3).
7. Saletti A, Johansson L, Yifter-Lindgren E, Wissing U, sterberg K, Cederholm T.
Nutritional status and a three-year follow-up in elderly receiving support at home.
Gerontology 2005;51:192-198.

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8. Wallace JI, Schwartz RS, LaCroix AZ, Uhlmann RF, Pearlman RA. Involuntary weight
loss in older outpatients: incidence and clinical sigificance. J Am Geriatr Soc
1995;43:329-37.
9. Payette H, Coulombe C, Boutier V, Gray-Donald K. Nutrition factors for
institutionalisation in a free-living functionally-dependent elderly population. J Clin
Epidemiol 2000;53:579-87.
10. Crogan NL, Pasvogel A. The influence of protein-calorie malnutrition on quality of life
in nursing homes. J Gerontol A Biol Sci Med Sci 2003;58:159-64.
11. Saletti A, Yifter-Lindgren E, Johansson L, Cederholm T. Nutritional status according
to Mini Nutritional Assessment in an institutionalized elderly population in Sweden.
Gerontology 2000:46:139-45.
12. Margetts BM, Thompson RL, Elia M, Jackson AA. Prevalence of risk of undernutrition
is associated with poor health status in older people in the UK. Eur J Clin Nutr
2003;57:69-74.
13. Valentini L, Schindler K, Schlaffer R, Bucher H, Mouhieddine M, Steininger K,
Tripamer J, Handschuh M, Schuh C, Volkert D, Lochs H, Sieber CC, Hiesmayr M. The
first nutriionDay in nursing homes: participation may improve malnutrition
awareness. Clin Nutr 2009;28:109-16.
14. Soini H, Muurinen S, Routasalo P, Sandelin E, Savikko N, Suominen M, Ainamo A,
Pitkala KH. Oral and nutritional status--Is the MNA a useful tool for dental clinics. J
Nutr Health Aging 2006;10:495-499.
15. Torma J, Winblad U, Cederholm T, Saletti A. Does undernutrition still prevail among
nursing home residents? Clin Nutr 2013;32:562-8.
16. Persson M, Brismar K, Katzarski K, Nordenstrm J, Cederholm T. Nutritional status
by Subjective global assessment and Mini nutritional assessment predict mortality in
geriatric patients. J Am Ger Soc 2002;50:1996-2002.
17. Pablo AM, Izaga MA, Alday LA. Assessment of nutritional status on hospital
admission: nutritional scores. Eur J Clin Nutr 2003;57:824-31.
18. Paillaud E, Merlier I, Dupeyron C, Scherman E, Poupon J, Bories Phuong-Nhi. Oral
candidiasis and nutritional deficiencies in elderly hospitalised patients. Br J Nutr
2004;92:861-7.
19. Thomas DR, Zdrowski CD, Wilson MM et al. Malnutrition in subacute care. Am J Clin
Nutr 2002;75:308-13.
20. Evans WJ, Morley JE, Argils J, Bales C, Baracos V, Guttridge D, Jatoi A, Kalantar-
Zadeh K, Lochs H, Mantovani G, Marks D, Mitch WE, Muscaritoli M, Najand A,
Ponikowski P, Rossi Fanelli F, Schambelan M, Schols A, Schuster M, Thomas D, Wolfe
R, Anker SD. Cachexia: a new definition. Clin Nutr 2008;27:793-9.
21. Cruz-Jentoft A, Baeyens JP, Bauer J, Boirie Y, Cederholm T, Landi F, Martin F, Michel
JP, Rolland Y, Schneider S, Topinkova E, Vandewoude M, Zamboni M. Sarcopenia:
European Consensus on Definition and Diagnosis. Age Ageing 2010;39:412-23.
22. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T,
Tracy R, Kop WJ, Burke G, McBurnie MA; Cardiovascular Health Study Collaborative
Research Group. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol
Sci Med Sci 2001;56:M146-56.
23. Cevenini E, Monti D, Franceschi C. Inflamm-ageing. Curr Opin Clin Nutr Metab Care.
2013;16:14-20.
24. Schttker B, Saum KU, Jansen EH, Boffetta P, Trichopoulou A, Holleczek B,
Dieffenbach AK, Brenner H. Oxidative stress markers and all-cause mortality at older
age: a population-based cohort study. J Gerontol A Biol Sci Med Sci 2015;70:518-24.
25. Elia M. The cost of disease-related malnutrition in the UK and economic
considerations for the use of oral nutritional supplements (ONS) in adults. Health
Economic Report on Malnutrition in the UK. BAPEN Reports 2012.
26. Akner G, Cederholm T. Nutritional treatment of protein-energy malnutrition in
chronic non-malignant disorders. Am J Clin Nutr 2001;74:6-24.
27. Al Snih S, Ottenbacher KJ, Markides KS, Kuo YF, Eschbach K, Goodwin JS. The effect
of obesity on disability vs mortality in older Americans. Arch Intern Med
2007;167:774-80.

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8

28. Flicker L, McCaul KA, Hankey GJ, Jamrozik K, Brown WJ, Byles JE, Almeida OP. Body
mass index and survival in men and women aged 70 to 75. J Am Geriatr Soc
2010;58:234-41.
29. Payette H, Coulombe C, Boutier V, Gray-Donald K. Weight loss and mortality among
free-living frail elders: a prospective study.J Gerontol A Biol Sci Med Sci
1999;54:M440-5.
30. Potter JF, Schafer DF, Bohi RL. In-hospital mortality as a function of body mass
index: an age-dependent variable. J Gerontol 1988;43:M59-63.
31. Sullivan DH, Walls RC, Lipschitz DA. Protein-energy undernutrition and the risk of
mortality within 1 y of hospital discharge in a select population of geriatric
rehabilitation patients. Am J Clin Nutr 1991;53:599-605.
32. Sullivan DH, Walls RC. Protein-energy undernutrition and the risk of mortality within
six years of hospital discharge. J Am Coll Nutr 1998;17:571-8.
33. Flodin L, Svensson S, Cederholm T. Body mass index as a predictor of one-year
mortality in geriatric patients. Clin Nutr 2000;19:121-25.
34. Hiesmayr M, Schindler K, Pernicka E, Schuh C, Schoeniger-Hekele A, Bauer P,
Laviano A, Lovell AD, Mouhieddine M, Schuetz T, Schneider SM, Singer P, Pichard C,
Howard P, Jonkers C, Grecu I, Ljungqvist O; NutritionDay Audit Team. Decreased
food intake is a risk factor for mortality in hospitalised patients: the NutritionDay
survey 2006 Clin Nutr 2009;28:484-91.
35. Palmblad J, Cederholm T. Host defence mechanisms and ageing. Bailliere's Clinical
Infectious Diseases.Infections in the elderly 1998;5:1-15.
36. Potter J, Klipstein K, Reilly JJ, Roberts M. The nutritional status and clinical course of
acute admissions to a geriatric unit. Age Ageing 1995;24:131-6.
37. Muscaritoli M, Anker SD, Argiles J, Aversa Z, bauer J, Biolo G, Boirie Y, Bosaeus I,
Cederholm T, Costelli P, Fearon K, Laviano A, Maggio M, Rossi Fanelli F, Schneider
SM, Schols A, Sieber C, Consensus definition of sarcopenia, cachexia and pre-
cachexia: Joint document elaborated by Special Interest Groups (SIG) cachexia-
anorexia in chronic wasting diseases and nutrition in geriatrics. Clin Nutr
2010;29;154-59.
38. Strandberg T, Pitkl K, Tilvis R. Frailty in older people. Eur Ger Med 2011;2:344-55.
39. Ensrud KE, Cauley J, Lipschutz R, Cummings SR. Weight change and fractures in
older women. Study of Osteoporotic Fractures Research Group. Arch Intern Med
1997;157:857-63.
40. Koren-Hakim T, Weiss A, Hershkovitz A, Otzrateni I, Anbar R, Gross Nevo RF,
Schlesinger A, Frishman S, Salai M, Beloosesky Y. Comparing the adequacy of the
MNA-SF, NRS-2002 and MUST nutritional tools in assessing malnutrition in hip
fracture operated elderly patients. Clin Nutr 2015pii:S0261-5614(15)00193-4.
doi:10.1016/j.clnu.2015.07.014.
41. Litchford MD, Dorner B, Posthauer ME. Malnutrition as a Precursor of Pressure Ulcers.
Adv Wound Care 2014;3:54-63.
42. EPUAP (European Pressure Ulcer Advisory Panel). www.epuap.org.
43. Stratton RJ, Ek AC, Engfer M et al. Enteral nutritional support in prevention and
treatment of pressure ulcers: a systematic review and meta-analysis. Ageing Res
Rev 2005;4:422-50.
44. Brozek J. Bibliographical note on behavioral aspects: on the margin of the 50th
anniversary of the Minnesota Starvation-Nutritional Rehabilitation experiment.
Percept Mot Skills 1995;81:395-400.
45. Amarantos E, Martinez A, and Dwyer J. Nutrition and quality of life in older adults. J
Gerontol A Biol Sci Med Sci 2001;56: 54-64.
46. Brantervik AM, Jacobsson IE, Grimby A, Wallen TC, Bosaeus IG. Older hospitalised
patients at risk of malnutrition: correlation with quality of life, aid from the social
welfare system and length of stay? Age Ageing 2005;34:444-9.
47. de Groot CP, van den Broek T, van Staveren W. Energy intake and micronutrient
intake in elderly Europeans: seeking the minimum requirement in the SENECA study.
Age Ageing 1999;28:469-74.
48. Biesalski HK, Brummer RJ, Konig J et al. Micronutrient deficiencies. Hohenheim

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Consensus Conference. Eur J Nutr 2003;42:353-63.


49. Jackson RD, LaCroix AZ, Gass M et al. Calcium plus vitamin D supplementation and
the risk of fractures. N Engl J Med 2006;354:669-83.
50. Grant AM, Avenell A, Campbell MK et al. RECORD Trial Group. Oral vitamin D3 and
calcium for secondary prevention of low-trauma fractures in elderly people
(Randomised Evaluation of Calcium Or vitamin D, RECORD): a randomised placebo-
controlled trial. Lancet 2005;365:1621-8.
51. Bischoff-Ferrari HA, Dawson-Hughes B, Staehelin HB, Orav JE, Stuck AE, Theiler R,
Wong JB, Egli A, Kiel DP, Henschkowski J. Fall prevention with supplemental and
active forms of vitamin D: a meta-analysis of randomised controlled trials. Br Med J
2009;339:b3692.doi: 10.1136/bmj.b3692.
52. Institute of Medicine. Dietary Reference Intakes for Calcium and Vitamin D. 2010
www.iom.edu/vitamind.

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