CC BY-NC-ND
0JAMDA xxx (2017) 1-9
Review Article
High Prevalence of Physical Frailty Among Community-Dwelling Malnourished Older Adults-A Systematic Review and Meta-Analysis
Sjors Verlaan MSc3^*, Gerdien C. Ligthart-Melis PhDb,c, Sander L.J. Wijers PhDb, Tommy Cederholm MD, PhDd, Andrea B. Maier MD, PhDe,f, Marian A.E. de van der Schueren PhDg,h
a Department of Internal Medicine, Section of Gerontology and Geriatrics, VU University Medical Center, Amsterdam, The Netherlands b Nutricia Research, Nutricia Advanced Medical Nutrition, Utrecht, The Netherlands
c Department of Health and Kinesiology, Center for Translational Research in Aging and Longevity, Texas A&M University, College Station, TX d Department of Public Health and Caring Sciences/Clinical Nutrition and Metabolism, Department of Geriatric Medicine, Uppsala University Hospital, Uppsala, Sweden
e Department of Medicine and Aged Care, Royal Melbourne Hospital, University of Melbourne, Melbourne, Australia f Department of Human Movement Sciences, MOVE Research Institute Amsterdam, VU University, Amsterdam, The Netherlands g Department of Internal Medicine, Section Nutrition and Dietetics, VU University Medical Center, Amsterdam, The Netherlands h Department of Nutrition, Sports and Health, Faculty of Health and Social Studies, HAN University of Applied Sciences, Nijmegen, The Netherlands
ABSTRACT
Keywords:
Malnutrition
frailty
community-dwelling
Background: Malnutrition and frailty are two geriatric syndromes that significantly affect independent living and health in community-dwelling older adults. Although the pathophysiology of malnutrition and physical frailty share common pathways, it is unknown to what extent these syndromes overlap and how they relate to each other.
Methods: A systematic review was performed resulting in a selection of 28 studies that assessed both malnutrition and frailty in community-dwelling older adults. Furthermore, a meta-analysis was performed on 10 studies that used Mini- Nutritional Assessment and the Fried frailty phenotype to estimate the prevalence of malnutrition within physical frailty and vice versa.
Results: In the systematic review, 25 of the 28 studies used the Mini-Nutritional Assessment (long or short form) for malnutrition screening. For frailty assessment, 23 of the 28 studies focused on the physical frailty phenotype, of which 19 followed the original Fried phenotype. Fifteen studies analyzed the association between malnutrition and frailty, which was significant in 12 of these. The meta-analysis included 10 studies with a total of 5447 older adults. In this pooled population of community-dwelling older adults [mean (standard deviation) age: 77.2 (6.7) years], 2.3% was characterized as malnourished and 19.1% as physically frail. The prevalence of malnutrition was significantly associated with the prevalence of physical frailty (P < .0001). However, the syndromes were not interchangeable: 68% of the malnourished older adults was physically frail, whereas only 8.4% of the physical frail population was malnourished. Conclusions: The systematic review and meta-analysis revealed that malnutrition and physical frailty in community-dwelling older adults are related, but not interchangeable geriatric syndromes. Two out of 3 malnourished older adults were physically frail, whereas close to 10% of the physically frail older adults was identified as malnourished.
© 2017 AMDA — The Society for Post-Acute and Long-Term Care Medicine. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
S.V. and S.L.J.W. are employees, and G.C.L.-M. is contractor of Nutricia Research, Nutricia Advanced Medical Nutrition. The authors declare no conflicts of interest.
* Address correspondence to Sjors Verlaan, Department of Internal Medicine, Section of Gerontology and Geriatrics, VU University Medical Center, De Boelelaan 1117, Amsterdam 1081 HV, The Netherlands.
E-mail address: G.Verlaan@vumc.nl (S. Verlaan).
As the global population ages, there is increasing attention for geriatric syndromes, which significantly impact independent living, quality of life, and healthcare consumption. Malnutrition and frailty are two important geriatric syndromes in community-dwelling older adults, and both have a clear nutrition-related component.
Malnutrition is defined by the European Society for Clinical Nutrition and Metabolism as "a state resulting from lack of uptake or intake of nutrition causing altered body composition (decreased fat
http://dx.doi.org/10.1016/jjamda.2016.12.074
1525-8610/© 2017 AMDA — The Society for Post-Acute and Long-Term Care Medicine. This is an open access article under the CC BY-NC-ND license (http://creativecommons. org/licenses/by-nc-nd/4.0/).
2 S. Verlaan et al. / JAMDA xxx (2017) 1-9
free mass and body cell mass), leading to diminished physical and mental function and impaired outcome from disease."1,2 In older adults, malnutrition has been shown to contribute to loss of autonomy, lower quality of life, higher frequency of hospital admissions, and mortality.3 Several nutritional screening tools are being used to detect malnutrition. Among the most commonly used tools are the Malnutrition Universal Screening Tool,4 Mini-Nutritional Assessment (MNA),3 Subjective Global Assessment,5 Short Nutritional Assessment Questionnaire,6 and Nutritional Risk Screening-2002.7. Weight loss and nutritional intake are common domains in most tools. For free-living older populations, the MNA is a well-established and widely used tool3 that assesses nutritional intake, involuntary weight loss, mobility, psychological stress or acute disease, neuropsychological problems, and body mass index or calf circumference. Patients are categorized into 1 of 3 categories: normal nutritional status, at risk of malnutrition, or malnourished.
Frailty is the cumulative decline across multiple physiological systems, which increases an individual's vulnerability for developing dependency, morbidity, and/or mortality when exposed to a stressor.8,9 Several domains within the frailty context can be distinguished, among others physical and cognitive impairment, psychological risk factors, and social determinants.10,11 Some of the frailty tools exploit a more holistic approach, including comorbidities and mental characteristics (eg, the Rockwood Frailty Index10 or the Tilburg Frailty Index12). Specifically, physical frailty has been defined as "a medical syndrome with multiple causes and contributors that is characterized by diminished strength, endurance, and reduced physiologic function that increases an individual's vulnerability for developing increased dependency and/or death."9 The most studied physical frailty model is the Physical Frailty Phenotype developed by Fried et al,13 consisting of 5 domains: weight loss, exhaustion, weakness, slowness, and reduced physical activity. This tool classifies patients as either robust (none of the domains below threshold), prefrail (1 or 2 domains below threshold), or frail (3 or more domains below threshold). Several scales have been developed that are derived from this phenotype model, including the Study of Osteoporotic Fractures scale14 and the FRAIL scale.15
Malnutrition and physical frailty share common pathophysiology and screenings tools include overlapping items, such as weight loss and impaired physical function. Furthermore, malnutrition holds an important place within the conceptual physical frailty phenotype developed by Fried et al.13 Weight loss is seen as a modifiable risk factor for physical frailty.16 Therefore, debate exists about how close the link between both syndromes is, and to what extent they coexist or are overlapping phenomena.
Our aim was to assess whether malnutrition and frailty in community-dwelling older adults are associated and/or interchangeable syndromes. Therefore, we systematically reviewed studies that assessed both syndromes. Furthermore, we performed a meta-analysis to estimate the prevalence of malnutrition within physical frailty and vice versa, based on the studies that used MNA and Fried physical frailty phenotype.
Methods
Literature Search
We searched for studies (both full text and abstracts) assessing both malnutrition and frailty in community-dwelling older adults. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) principles were followed in the systematic review and meta-analysis.17 Records were retrieved through PubMed (1900-2016), Medline (1946-2016), Embase (1947-2016), and CAB Abstracts (1910-2016). Records from Medline, Embase, and CAB Abstracts were retrieved using the following search terms: Ti,ab
[(malnutrition OR malnourish* OR "nutritional status" OR undernourish*) AND (frailty OR frail OR physical* p/0 frail* OR "pre-frail" OR "pre-frailty") AND (elderly OR "older people" OR "older adults" OR aged OR aging OR ageing OR "old age" OR retired OR pensioner* OR geriatric*)], whereas records from Pubmed were retrieved using the following search terms: Ti,ab[(malnutrition OR malnourish OR malnourished OR "nutritional status" OR undernourish OR undernourished) AND (frailty OR frail OR "physically frail" OR "physical frailty" OR "pre-frail" OR "pre-frailty") AND (elderly OR "older people" OR "older adults" OR aged OR aging OR ageing OR "old age" OR retired OR pensioner OR pensioners OR geriatric OR geriatrics OR geriatrician)]. The search was limited to titles and abstracts only, without restriction for language or publication date. The last search was run on May 4, 2016 (Medline, Embase and CAB Abstracts) and on May 30, 2016 (PubMed). Duplicate records were removed. The search and selection process is summarized in Figure 1.
Systematic Review
A total of 727 unique records were retrieved using the search strings described above. The first selection was made by 2 investigators (S.L.J.W., D.S.) independently in a standardized manner, by screening titles and abstracts. Inclusion criteria for the first selection were containing both 1) screening for malnutrition and 2) frailty assessment. Based on these criteria, 89 potentially eligible records were identified. Subsequently, full text articles or abstracts, if the results were not published as full articles, were reviewed independently in a standardized manner by 3 authors (S.V., S.L.J.W., and G.C.L.-M.). Disagreements between reviewers were resolved by consensus. Articles were excluded in this second step if they focused on 1) study populations selected for a specific disease, 2) institutionalized study populations, 3) hospitalized study populations, or if 4) no results were available on frailty and/or malnutrition status, and if 5) the same population was described in other articles.
A total of 28 studies were included in the systematic review.18-45 One of the authors (G.C.L.-M.) extracted data regarding study design, country, selection method, sample size and sex, age, malnutrition tool and status, frailty tool and status, and results on association regarding malnutrition and frailty, as presented in Table 1. This was checked independently by S.L.J.W. and S.V.; any disagreement was resolved through discussion.
Meta-Analysis
Selection
Studies were excluded if participants were preselected for malnutrition or frailty (6 studies,22,31,35,40,42,45) because the aim of the current study was to analyze a general "representative" community-dwelling population. Moreover, it was shown that different or adapted screening tools introduce variation, which made it impossible to compare prevalence rates among studies.46 Because most studies applied the MNA (long or short form) and Fried phenotype to classify nutritional status and physical frailty, respectively, we decided that only the 13 studies that applied the MNA, together with the Fried phenotype were eligible for inclusion in the quantitative meta-
analysis 19,20,24,25,28,29,32-34,36,38,39,43
For selected studies, additional data were requested from the authors if not provided in the original article. We asked for absolute numbers of participants in nutritional status categories "normal," "at risk of malnutrition," and "malnourished" and the physical frailty categories "robust," "prefrail," and "frail"19,25,28,32-34,36,38,39,43 and mean age (±standard deviation) of the population.20,24,43 Three authors provided data of more36 or fewer38,43 participants than included in the article. In those cases, the numbers provided by the authors were used for the meta-analysis (Table 2) and explicated in the
S. Verlaan et al. / JAMDA xxx (2017) 1-9 3
Records identified through database searching (n = 931)
Records after du (n = plicates removed 727)
Records excluded that did not apply any screening tools to estimate the prevalence of frailty or malnutrition (n=638)
Studies excluded, with reasons (n = 18):
- Participants pre-selected for frailty or malnutrition (n=6, E1*)
- Fried phenotype or the MNA was not used to detect physical frailty and malnutrition respectively (n=9, E2*)
- No additional information available (n=3, E3*)
Records screened (n = 727)
Full-text articles (n = 55) and abstracts (n = 34) assessed for eligibility
Studies included in qualitative synthesis (systematic review) (n = 28, 24 full-text, 4 abstracts)
Studies included in quantitative synthesis (meta-analysis) (n = 10 full-text, I*)
Full-text and abstracts articles
excluded, with reasons (n = 61):
- Participants selected for a specific disease (n=30)
- Institutionalized study population (n=8)
- Hospitalized study population (n=8)
- No results available on frailty and/or malnutrition status (n=2)
- Same study population described in other article (n=13)
Fig. 1. PRISMA flowchart of study selection for systematic review and meta-analysis. *Codes represent reason for in- and exclusion meta-analysis, detailed in Table 1.
footnotes. For 3 studies, we did not receive the requested data. As a result, 10 studies, which have all been published as full articles (9 in English, 1 in Spanish) were included19'20'24'29'33'34'36'38'39'43 in the meta-analysis.
Statistics
Both malnutrition and physical frailty consisted of 3 ordered categories: normal nutritional status, at risk of malnutrition and malnourished vs robust, prefrail, and frail, respectively. Therefore, we applied the Cochran-Mantel-Haenszel test to analyze the association between physical frailty and nutritional status per study with "no association" as 0-hypothesis and "general association" as alternative hypothesis. The same was tested after pooling the 10 selected studies by using the stratified Cochran-Mantel-Haenszel test with "study" included as stratum. The association between physical frailty and nutritional status was regarded as significant when P values were <.05.
Results
Systematic Review
Characteristics of the 28 studies included in the systematic review are summarized in Table 1. For malnutrition screening, 25 studies used the MNA (long or short form); the other 3 studies used Mini-Nutritional Status, DETERMINE, and Dietary Screening
Tool. In 23 of the studies, the physical frailty phenotype was studied, of which 19 followed the original Fried phenotype; the other studies used modified Fried criteria, Study of Osteoporotic Fractures scale (x2), and FRAIL scale. The remaining 5 studies followed a broad frailty model, using the Tilburg Frailty Index (x2), Edmonton, Rockwood, and Kihon, which included more than only physical characteristics. Fifteen studies addressed the association between malnutrition and frailty.18,20-24,28-3o,32-34,37,41,45 m 12 of these 15 studies, the authors concluded that there was a significant
association between malnutrition and frailty.18,20-24,28,29,32-34,41
Six studies indicated a causal relationship as malnutrition was considered to be a risk factor for the development of
frailty.18,21,24,32,34,41
Meta-Analysis
A total of 5447 older adults from 10 studies19,20,24,29,33,34,36,38,39,43 was included in the meta-analysis. Mean age of the analyzed population was 77.2 (6.7) years. In this pooled population of community-dwelling older adults, 128 (2.3%) were characterized as malnourished and 1036 (19.0%) as at risk for malnutrition; 1041 (19.1%) as physically frail and 2810 (51.6%) as prefrail.
The Cochran-Mantel-Haenszel tests of the individual study data and after pooling of the 10 selected studies showed that the prevalence of malnutrition was significantly associated with the prevalence of physical frailty (P < .0001) (Table 2).
Table 1
Characteristics of the Study Populations, and the Prevalence of Malnutrition and Frailty in the Studies Included in the Systematic Review
Sources Study Design
First Author, Year
Country
Selection
Sample Size
Age, Years (Mean ± SD)
Malnutrition Tool and Status %M, %RM
Frailty Tool and
Status
%F, % PF
Result on Association Regarding (R)M and (P)F
Code in Flowchart (Figure 1)
Akin, 201518
Brandts, 201322 (Abstract only)
Chang, 20162
Eyigor, 20152
Ferrer, 201525
Gillain, 201526 (Abstract only)
Cross-sectional population based
Beaudart, 201519 Prospective
longitudinal
Bollwein, 201320 Cross-sectional
Boulos, 201621 Cross-sectional
Cross-sectional
Cross-sectional
Cross-sectional multi-center
Prospective population-based
Prospective cohort
Turkey
Belgium Germany
Lebanon
Country: not specified
Taiwan
Turkey
Country: not specified
Randomly selected from health centers
Outpatient clinics and general advertisement Day-clinic, rehabilitation center and newspaper advertisement Randomly selected from local authority databases
Older individuals >75 years, selected by general practitioners when considered (possibly) frail Primarily approached using
community posters Outpatients (>65 years) from Physical Medicine and Rehabilitation clinics at 13 centers were recruited All participants were Spanish Caucasians born in 1924, registered in primary healthcare centers Healthy old people
50.6% female
60.5% female
66.0% female
50.8% female
% female: not specified
18.4% female
65.7% female
71.5 (5.6)
73.5 (6.16)
Median (min
-max): 83 (75-96)
75.3 (7.1)
83 (5)
80.9 (7.7)
66, 5% between 65 and 74
60.0% female
57.3% female
MNA-LF 2.8% M 41.4% RM
MNA-LF 1.9% M 85.6% RM MNA-LF 0% M 15.1% RM
MNA-LF 8.0% M 29.1% RM
MNA 33% (R)M
MNA-LF 3.3% M 34.9% RM
MNA-LF 5.3% M 27.5% RM
MNA-LF Mean (SD): 24.88 (3.56)
Mini Nutritional
Status Mean: 12.8
Modified Fried (no physical activity) 27.8% F 34.8% PF Fried 15.5% F, 47.9% PF Fried 15.5% F 39.8% PF
SOF 36.4% F 30.4% PF
56.1% (P)F
SOF 0% F 40.1% PF
Fried 39.2% F 43.3% PF
Fried 16.7% F 55.0% PF
Edmonton 14.5% mild/ moderate F
Increased malnutrition risk in (pre-) frail (P < .001)
Not disclosed in article
Increased malnutrition risk in (pre-) frail (P < .001)
Significant association between frailty and poor nutritional status (P < .001) Significant correlation between frailty and (risk of) malnutrition (MNA) (r2 = 0.35; P = .007) Prefrail had a lower total MNA score than nonfrail (B = -0.36, P < .001) Increased malnutrition (risk) in (pre-) frail (P < .001)
Not disclosed in article
Not disclosed in abstract
Table 1 (continued)
Sources Study Design
First Author, Year
Country
Selection
Sample Size
Age, Years (Mean ± SD)
Malnutrition Tool and Status %M, %RM
Frailty Tool and
Status
%F, % PF
Result on Association Regarding (R)M and (P)F
Code in Flowchart (Figure 1)
Hamza, 201227 Cross-sectional Egypt
Jung, 20162
Jürschik, 201421
Kamo, 201430
Lilamand, 201531
Liu, 20153
Martinez-Reig, 201433
Prospective Korea
cohort (ASPRA)
Prospective cohort (Fralle)
Cross-sectional
Prospective cohort (Toulouse Frailty Clinic)
Community-based aging cohort (ILAS)
France
Taiwan
concurrent cohort (Fradea, second wave)
Older outpatients recruited at geriatric clinic Potentially eligible
residents were identified through the National Healthcare Service Random selection from of older people living independently in community
Patients receiving home care recruited through the Health Care Service
Foundation for Older People.
All outpatients admitted to the Toulouse Frailty Clinic
(prescreened for frailty by general practioner) in 2013
People aged 50 years and older were randomly selected from the database
Adults aged 70 years or more randomly selected from the census of health card holders
60.0% female
56% female
67.6 (6.3) 74.4 (6.5)
62.1% female
90 community-
dwelling 72.2% female
67.0% female
81.2 (5.0)
84.3 (8.2) (community)
81.5 (5.8)
52.5% female
63.9 (9.3)
57.8% female
78.0 (5.7)
DETERMINE 57.5% moderate/ high risk of M MNA-SF 37.9% RM
MNA-LF 2.3% M 19.6% RM
MNA-SF Prevalence not specified for community-dwelling
MNA-SF 1.9% M 22.8% RM
MNA-LF Mean (SD): 27.2 (1.8)
MNA-SF 2.9% M* 23.9% RM*
Fried 25.0% F 45.0% PF Fried (n = 380) 17.4% F 52.6% PF
Fried 9.6% F 47% PF
Rockwood Mean (SD): 4.7 (1.5) (community-dwelling)
Fried 36.8% F 51.9% PF
Fried 6.8% F 40.5% PF
Fried 18.4% F 55.6% PF
Not disclosed in article
Odds ratio (95% CI) for risk of malnutrition for frail vs nonfrail 4.2 (2.0—8.8)
Results show a clear
association between MNA and Fried phenotype
(p < .001)
No significant direct effect of nutritional status on frailty (B = -0.115, NS)
Not disclosed in article
Lower MNA score was
independent risk factor for prefrailty and frailty (PF: OR 0.928 (CI
0.865, 0.997);
F: OR 0.662 (CI 0.582, 0.754)) Significant association between frailty status and MNA (P < .001)
Table 1 (continued )
Sources
First Author, Year
Study Design
Country
Selection
Sample Size
Age, Years (Mean ± SD)
Malnutrition Tool and Status %M, %RM
Frailty Tool and
Status
%F, % PF
Result on Association Regarding (R)M and (P)F
Code in Flowchart (Figure 1)
Maseda, 201634
Nykänen, 20123
Papiol, 20153
Rolf, 201337 (Abstract only)
Ruiz-Arregui. 201338
Satake, 20153!
Longitudinal (Verisaúde) study)
Population based intervention study (GeMS)
Population-based cross-sectional study between January and June 2014 Cross-sectional
Finland
Poland
Longitudinal Mexico
observational study (Coyocan)
Cross-sectional Japan
Serra-Prat, 20 1 340 Intervention
Sewo Sampaio, Cross-sectional Brazil
201541
Baseline data of participants in Verisaude study, recruited from senior centers Baseline data of subpopulation with
malnutrition risk in the GeMS intervention study Random sample from the database, from 3 primary care centers Not specified
Random selection from
government database among community-dwelling elderly Nondependent outpatients >65 years, with chronic
conditions were recruited Recruited at health consortium medical centers, preselected frail and NF groups Recruited at community centers for older adults
60.6% female
79.2% female
47% female
66.2% female
55.9% female
33.5% female
34 older people F: 78.6% female NF: 35.0% Female
100% female
75.8 (7.2)
83.1 (5.1)
80.3 (3.5)
Range: 59-96
79.5 (7.1)
76.4 (6.2)
F: 84.5 (5.0) NF: 80.7 (8.4)
70.8 (6.9)
MNA-SF 0.8% M 13.5% RM
MNA-LF 100% RM
MNA-LF 7.3% (R)M
Dietary Screening Tool
66% at nutritional risk
MNA-LF 3.4% M 23.9% RM
MNA-LF 0.6% M* 24.4% RM*
MNA-LF F: 100% RM NF:15% RM
MNA-SF When frail/NF: 12.5%/2.4% M 45.8%/20% RM
Fried 3.7% F 71.8% PF
Intervention 24.7% F 61.0% PF Control: 25.6% F 61.0% PF Fried 29.4% F 35.7% PF
Fried 88% (P)F
Fried 14.1% F 37.4% PF
Fried 11.6% F 60.4% PF
Fried 41.2% F 58.8% NF
Kihon 22% F
Increased (pre) I
frailty risk with low MNA-SF scores (<11) (P < .001)
Not disclosed in E1
article
Not disclosed in article
No statistically E2
significant relationship between frailty and nutritional risk
Not disclosed in I
article
Not disclosed in I
article
Not disclosed in article
Those who were E2 either at risk of malnutrition or malnourished were more likely to be frail (OR 0.206 (0.079-0.536, P= .001)
S. Verlaan et al. / JAMDA xxx (2017) 1-9
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Table 2
Analysis of the Association Between Malnutrition and Physical Frailty for Individual Studies and Pooled Data in the Meta-Analysis
Cochran-Mantel-Haenszel Test
Articles
First Author, Year
Age, Years Mean (SD)
DF Value
P Value
Beaudart, 201519 534 73.5 (6.2) 4 65.274 <.0001
Bollwein, 201320 206 83 (75-96)* 2 41.552 <.0001
Eyigor, 201524 1126 Not disclosed 4 190.802 <.0001
Jurschik, 201429 512y 81.2 (5.0) 4 94.566 <.0001
Martinez Reig, 201433 678 78.0 (5.7) 4 86.938 <.0001
Maseda, 201634 749 75.8 (7.2) 4 38.510 <.0001
Papiol, 201536 298z 80.3 (3.5) 4 18.046 .0012
Ruiz-Arregui, 201338 583x 79.5 (7.1) 4 93.555 <.0001
Satake, 201539 164 76.4 (6.2) 4 18.740 .0009
Turusheva, 201643 597" 74.5 (5.9) 4 53.887 <.0001
Pooled data 5447 77.2 (6.7)1 4 628.160 <.0001
SD, standard deviation.
*Median (min-max) presented, as mean (SD) was not available.
yCombined data available for 512 older people.
zn = 126 described in article, supplemental data obtained from author.
xn = 1124 described in article, data obtained from author contained less participants.
"n = 611 described in article, data obtained from author contained less participants.
'Based on n = 4115, Bollwein and Eyigor excluded as no mean (SD) was available.
Figure 2 shows the pooled results regarding the classifications of nutritional status vs physical frailty in these community-dwelling older adults. The prevalence of physical frailty was higher when nutritional status was less favorable: 11.9% frail in the well-nourished group (510/4283), 42.9% frail in the group that is at risk of malnutrition (444/1036), and 68.0% frail in the malnourished group (87/128).
The prevalence of malnutrition was higher in more physically frail groups, although with lower rates: 0.5% malnutrition in the robust group (8/1596), 1.2% in the prefrail group (33/2810), and 8.4% in the frail group (87/1041). The prevalence of risk of malnutrition was 7.7% in the robust group (123/1596), 16.7% in the prefrail group (469/2810), and 42.7% in the frail group (444/1041).
Discussion
The results from the systematic review (28 studies) and meta-analysis (10 studies) suggest that malnutrition and physical frailty are related, but not interchangeable syndromes in the community setting. Older malnourished people with an average age of 77 years were likely to be physically frail, but only a small percentage of the physically frail older people in the community was identified as malnourished.
General Prevalence of Malnutrition and Physical Frailty in the Community
The pooled prevalence in the current meta-analysis revealed an overall malnutrition prevalence of 2.3% and risk of malnutrition prevalence of 19.0% in community-dwelling older adults. These findings are comparable to the pooled prevalence of malnutrition of 3.1% and risk of malnutrition of 26.5% found in a recent meta-analysis by Cereda et al.47
Regarding physical frailty, Kane et al48 showed an overall physical frailty prevalence of 14% in pooled data of 123 studies in community-dwelling adults above 65 years of age. A systematic review by Collard et al49 showed a pooled physical frailty prevalence of 9.9% in 44,894 community-dwelling older participants (>65 years of age) and clearly indicated a significant increase in prevalence with age. In our
S. Verlaan et al. / JAMDA xxx (2017) 1-9
Malnourished
'—' At risk of
H malnutrition
3 Normal nutritional status
Robust
Pre-Frail
Physical Frailty status (Fried)
Fig. 2. Pooled prevalence of physical frailty and nutritional status in categories (number and percentage of the total n = 5447 (=100%) is depicted).
systematic review, most of the studies we included report physical frailty percentages above 10%, which resulted in a pooled prevalence of 19.1% in the meta-analysis. The relative old age of the populations studied might explain this higher prevalence. Several of the studies within the systematic review showed a substantially higher prevalence of physical frailty, mainly because of the use of different frailty-tools,21,44 or the preselection of participants for frailty31,42 or malnutrition.35
Prevalence of Physical Frailty in Malnourished Older Adults
The results of the current meta-analysis showed that two-thirds (68%) of the malnourished older adults were also physically frail, and one-quarter (25.8%) prefrail. Thus, malnutrition is a relevant contributor toward increased vulnerability for developing negative health outcomes, loss of independency, and mortality, as suggested previously.20,21 Improving nutritional intake seems to be a prerequisite to manage these malnourished patients and their diseases. Care plans, adequate provision of food, and optimizing stimuli for appetite are essential.50 A protein intake of 1.2 to 1.5 g/kg body weight/day is recommended for a geriatric frail population51 in combination with an adequate amount of energy to maintain energy balance. These recommendations are particularly challenging for already malnourished people.
Prevalence of Malnutrition in Physically Frail Older Adults
On the other hand, the results of the meta-analysis indicated that less than 10% of the physically frail community-dwelling persons aged 75 to 80 years was malnourished. Moreover, one-half of the total community-dwelling older population displayed a normal nutritional status while being pre-frail (42%) or frail (9%). Despite their normal nutritional status overall, these (pre-) frail older adults might still have inadequate intake of certain nutrients, such as protein and vitamin D, so called qualitative malnutrition.50
In addition to malnutrition, another key element of physical frailty is considered to be sarcopenia, which is the age-related decline of muscle mass, strength, and function.52 The muscle is the biological substrate for both physical frailty and sarcopenia. Muscle loss leads to functional decline, such as impaired walking speed and muscle
weakness.52 Therefore, prefrail and frail people may benefit from targeted interventions to maintain or improve muscle mass and function. Resistance exercise is the foremost strategy to offset sarco-penia.53 In addition, there are indications that such interventions would be augmented by a combination with an adequate protein intake of 20 to 40 g of protein after each session to optimize the effectiveness of the training.51,54
Strengths and Limitations
A strength of this systematic review and meta-analysis is the systematic approach following the PRISMA principles. The systematic review revealed that the majority of studies that assessed both malnutrition and frailty in community-dwelling older adults used the Fried phenotype and MNA, respectively. That allowed us to compare the subclasses of malnutrition and physical frailty in a meta-analysis using a 3 x 3 approach, which provided quantitative insights in the at-risk populations as well. On the other hand, the limitation of that approach was that studies that used other screening tools could not be included in the meta-analysis.
The studies that described a preselection of participants based on the presence of either malnutrition or frailty, were not included in the meta-analysis. We cannot exclude, however, that the participants in the included population based studies in the meta-analysis did show some level of preselection because of a recruitment bias, which might provide an explanation for the high overall prevalence of physical frailty in the meta-analysis. Furthermore, we did not include the psychological and social components of frailty in the scope of our search, which may also be associated with an inadequate dietary intake in the community-dwelling elderly.
Conclusions
This systematic review and meta-analysis indicated that malnutrition and physical frailty often coincide in community-dwelling elderly with a potentially detrimental impact on independent living, comorbidities, and, thus, on quality of life. The prevalence of physical frailty, however, is much higher than the prevalence of malnutrition (19% vs 2.3%, respectively), indicating that these syndromes are not interchangeable. Moreover, 2 out of3 malnourished older adults were
S. Verlaan et al. /
physically frail, whereas close to 10% of the physically frail older people in the community was identified as malnourished.
Acknowledgments
We would like to thank all authors who kindly provided additional data for the meta-analysis: Dr. Beaudart,19 Dr. Abizanda Soler,33 Dr. Millán Calenti,34 Dr. Serra Prat,36 Dr. Castrejón Pérez,38 Dr. Satake,39 and Dr. Turusheva.43 From Nutricia Research, we would like to thank Daan Snoeks for performing the literature search and Marion Kaspers for performing the statistical analyses.
References
1. Cederholm T, Barazzoni R, Austin P, et al. ESPEN guidelines on definitions and terminology of clinical nutrition. Clin Nutr 2016 [Epub ahead of print].
2. Sobotka L. Basics in clinical nutrition, 4th ed. Sobotka L, editor: Galen; 2012.
3. Bauer JM, Kaiser MJ, Anthony P, et al. The Mini Nutritional Assessment—Its history, today's practice, and future perspectives. Nutr Clin Pract 2008;23: 388-396.
4. Elia M. The 'MUST' report. Nutritional screening for adults: A multidisciplinary responsibility. Development and use of the Malnutrition Universal Screening Tool (MUST) for adults. A report by the Malnutrition Advisory Group of the British Association for Parenteral and Enteral Nutrition (BaPeN). Redditch, England, 2003.
5. Detsky AS, McLaughlin JR, Baker JP, et al. What is Subjective Global Assessment of nutritional status? JPEN J Parenter Enteral Nutr 1987;11:8-13.
6. Kruizenga HM, Seidell JC, de Vet HC, et al. Development and validation of a hospital screening tool for malnutrition: The Short Nutritional Assessment Questionnaire (SNAQ). Clin Nutr 2005;24:75-82.
7. Kondrup J, Rasmussen HH, Hamberg O, Stanga Z. Ad Hoc EWG. Nutritional Risk Screening (NRS 2002): A new method based on an analysis of controlled clinical trials. Clin Nutr 2003;22:321-336.
8. Abate M, Di lorio A, Di Renzo D, et al. Frailty in the elderly: The physical dimension. Europa Medicophysica 2007;43:407-415.
9. Morley JE, Vellas B, van Kan GA, et al. Frailty consensus: A call to action. J Am Med Dir Assoc 2013;14:392-397.
10. Rockwood K, Stadnyk K, MacKnight C, et al. A brief clinical instrument to classify frailty in elderly people. Lancet 1999;353:205-206.
11. Garre-Olmo J, Calvo-Perxas L, Lopez-Pousa S, et al. Prevalence of frailty phe-notypes and risk of mortality in a community-dwelling elderly cohort. Age Ageing 2013;42:46-51.
12. Gobbens RJ, van Assen MA, Luijkx KG, et al. The Tilburg Frailty Indicator: Psychometric properties. J Am Med Dir Assoc 2010;11:344-355.
13. Fried LP, Tangen CM, Walston J, et al. Frailty in older adults evidence for a phenotype. J Gerontol Ser A Biol Sci Med Sci 2001;56:M146-M157.
14. Cawthon PM, Marshall LM, Michael Y, et al. Frailty in older men: Prevalence, progression, and relationship with mortality. J Am Geriatr Soc 2007;55: 1216-1223.
15. Morley JE, Malmstrom TK, Miller DK. A simple frailty questionnaire (FRAIL) predicts outcomes in middle aged African Americans. J Nutr Health Aging 2012;16:601-608.
16. Martone AM, Onder G, Vetrano DL, et al. Anorexia of aging: A modifiable risk factor for frailty. Nutrients 2013;5:4126-4133.
17. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med 2009;6: e1000097.
18. Akin S, Mazicioglu MM, Mucuk S, et al. The prevalence of frailty and related factors in community-dwelling Turkish elderly according to modified Fried Frailty Index and FRAIL scales. Aging Clin Exp Res 2015;27:703-709.
19. Beaudart C, Reginster JY, Petermans J, et al. Quality of life and physical components linked to sarcopenia: The SarcoPhAge study. Exp Gerontol 2015;69: 103-110.
20. Bollwein J, Volkert D, Diekmann R, et al. Nutritional status according to the mini nutritional assessment (MNA) and frailty in community- dwelling older persons: A close relationship. J Nutr Health Aging 2013;17:351-356.
21. Boulos C, Salameh P, Barberger-Gateau P. Malnutrition and frailty in community- dwelling older adults living in a rural setting. Clin Nutr 2016;35:138-143.
22. Brandts M, Arnold R, Vanneste V. lnventory of frailty and malnutrition within general practice. Eur Geriatr Med 2013;4:S84.
23. Chang SF, Lin PL. Prefrailty in community-dwelling older adults is associated with nutrition status. J Clin Nurs 2016;25:424-433.
24. Eyigor S, Kutsal YG, Duran E, et al. Frailty prevalence and related factors in the older adult—FrailTURK Project. Age 2015;37:1-13.
25. Ferrer A, Formiga F, Cunillera O, et al. Predicting factors of health-related quality of life in octogenarians: A 3-year follow-up longitudinal study. Qual Life Res 2015;24:2701-2711.
26. Gillain S, Wojtasik V, Schwartz C, et al. Baseline characteristics of a two-year prospective study aiming to link clinical components, cognitive and gait performances in healthy old people. Eur Geriatr Med 2015;6:S119-S120.
M xxx (2017) 1-9 9
27. Hamza SA, Mousa SM, Taha SE, et al. Immune response of 23-valent pneu-mococcal polysaccharide vaccinated elderly and its relation to frailty indices, nutritionalstatus, and serum zinc levels. Geriatr Gerontol Int 2012;12: 223-229.
28. Jung HW, Jang IY, Lee YS, et al. Prevalence of frailty and aging-related health conditions in older Koreans in rural communities: A cross-sectional analysis of the Aging Study of Pyeongchang Rural Area. J Korean Med Sci 2016;31: 345-352.
29. Jurschik P, Botigue T, Nuin C, Lavedan A [Association between Mini Nutritional Assessment and the Fried frailty index in older people living in the community]. Med Clin (Barc) 2014;143:191-195.
30. Kamo T, Nishida Y. Direct and indirect effects of nutritional status, physical function and cognitive function on activities of daily living in Japanese older adults requiring long-term care. Geriatri Gerontol Int 2014;14:799-805.
31. Lilamand M, Kelaiditi E, Cesari M, et al. Validation of the Mini-Nutritional Assessment-Short Form in a population of frail elders without disability. Analysis of the Toulouse Frailty Platform Population in 2013. J Nutr Health Aging 2015;19:570-574.
32. Liu L-K, Lee W-J, Chen L-Y, et al. Association between frailty, osteoporosis, falls and hip fractures among community-dwelling people aged 50 years and older in Taiwan: Results from I-Lan Longitudinal Aging Study. PLoS ONE 2015;10: e0136968.
33. Martinez-Reig M, Gomez-Arnedo L, Alfonso-Silguero SA, et al. Nutritional risk, nutritional status and incident disability in older adults. The FRADEA study. J Nutr Health Aging 2014;18:270-276.
34. Maseda A, Gomez-Caamano S, Lorenzo-Lopez L, et al. Health determinants of nutritional status in community-dwelling older population: The VERISAUDE study. Public Health Nutr 2016;19:2220-2228.
35. Nykanen I, Rissanen TH, Sulkava R, Hartikainen S. Effects of individual dietary counseling as part of a comprehensive geriatric assessment (CGA) on frailty status: A population-based intervention study. J Clin Gerontol Geriatr 2012;3: 89-93.
36. Papiol M, Serra-Prat M, Vico J, et al. Poor muscle strength and low physical activity are the most prevalent frailty components in community-dwelling older adults. J Aging Phys Act 2016;24:363-368.
37. Rolf K, Pietruszka B. Influence of selected factors on frailty syndrome among the elderly: A pilot study. Ann Nutr Metab 2013;63:1088-1089.
38. Ruiz-Arregui L, Avila-Funes JA, Amieva H, et al. The Coyoacan Cohort Study: Design, methodology, and participants' characteristics of a Mexican study on nutritional and psychosocial markers of frailty. J Frailty Aging 2013;2:68-76.
39. Satake S, Senda K, Hong YJ, et al. Validity of the Kihon Checklist for assessing frailty status. Geriatr Gerontol Int 2016;16:709-715.
40. Serra-Prat M, Mans E, Palomera E, Clave P. Gastrointestinal peptides, gastrointestinal motility, and anorexia of aging in frail elderly persons. Neuro-gastroenterol Motil 2013;25:291-e245.
41. Sewo Sampaio PY, Sampaio RA, Coelho Junior HJ, et al. Differences in lifestyle, physical performance and quality of life between frail and robust Brazilian community-dwelling elderly women. Geriatr Gerontol Int 2016;16:829-835.
42. Tavassoli N, Guyonnet S, Abellan Van Kan G, et al. Description of 1108 older patients referred by their physician to the "Geriatric Frailty Clinic (G.F.C) for Assessment of Frailty and Prevention of Disability" at the gerontopole. J Nutr Health Aging 2014;18:457-464.
43. Turusheva A, Frolova E, Hegendoerfer E, Degryse JM. Predictors of short-term mortality, cognitive and physical decline in older adults in northwest Russia: A population-based prospective cohort study. Aging Clin Exp Res 2016 [Epub ahead of print].
44. Van Asselt D, Ringnalda Y, Droogsma E, et al. Risk of undernutrition in Dutch community-dwelling elderly receiving home-delivered dinners. Eur Geriatr Med 2013;4:S126.
45. Woo J, Yu R, Wong M, et al. Frailty screening in the community using the FRAIL scale. J Am Med Dir Assoc 2015;16:412-419.
46. Theou O, Cann L, Blodgett J, et al. Modifications to the frailty phenotype criteria: Systematic review of the current literature and investigation of 262 frailty phenotypes in the Survey of Health, Ageing, and Retirement in Europe. Ageing Res Rev 2015;21:78-94.
47. Cereda E, Pedrolli C, Klersy C, et al. Nutritional status in older persons according to healthcare setting: A systematic review and meta-analysis of prevalence data using MNA(R). Clin Nutr 2016;35:1282-1290.
48. Kane RL, Shamliyan T, Talley K, Pacala J. The association between geriatric syndromes and survival. J Am Geriatr Soc 2012;60:896-904.
49. Collard RM, Boter H, Schoevers RA, Oude Voshaar RC. Prevalence of frailty in community-dwelling older persons: A systematic review. J Am Geriatr Soc 2012;60:1487-1492.
50. Landi F, Calvani R, Tosato M, et al. Anorexia of aging: Risk factors, consequences, and potential treatments. Nutrients 2016;8:69.
51. Bauer J, Biolo G, Cederholm T, et al. Evidence-based recommendations for optimal dietary protein intake in older people: A position paper from the PROT-AGE Study Group. J Am Med Dir Assoc 2013;14:542-559.
52. Landi F, Calvani R, Cesari M, et al. Sarcopenia as the biological substrate of physical frailty. Clin Geriatr Med 2015;31:367-374.
53. Phillips SM. Nutritional supplements in support of resistance exercise to counter age-related sarcopenia. Adv Nutr 2015;6:452-460.
54. Wall BT, Cermak NM, van Loon LJ. Dietary protein considerations to support active aging. Sports Med 2014;44:S185-S194.
