You are on page 1of 8

Clinical Research

Nutrition in Clinical Practice


Volume 33 Number 6
Risk of Malnutrition Evaluated by Mini Nutritional December 2018 879–886

C 2018 American Society for

Assessment and Sarcopenia in Noninstitutionalized Parenteral and Enteral Nutrition


DOI: 10.1002/ncp.10022
Elderly People wileyonlinelibrary.com

Ilaria Liguori, MD1 ; Francesco Curcio, MD1 ; Gennaro Russo, MD1 ;


Michele Cellurale, MD1 ; Luisa Aran, MD1 ; Giulia Bulli, MD1 ;
David Della-Morte, MD, PhD2,3 ; Gaetano Gargiulo, MD4 ; Gianluca Testa, MD,
PhD1,5 ; Francesco Cacciatore, MD, PhD1,6 ; Domenico Bonaduce, MD1 ;
and Pasquale Abete, MD, PhD1

Abstract
Background: Malnutrition indices and muscle mass and strength in the elderly are poorly investigated. Moreover, malnutrition seems
to be 1 of the more important factors in the cause of sarcopenia. The presence of sarcopenia and its relationship with malnutrition
indices were studied in noninstitutionalized elderly people who underwent Comprehensive Geriatric Assessment (CGA). Methods:
A total of 473 elderly subjects (mean age, 80.9 ± 6.6 years) admitted to CGA were studied. Malnutrition risk was evaluated with
Mini Nutritional Assessment (MNA) score, whereas muscle mass and muscle strength were evaluated by bioimpedentiometry and
hand grip, respectively. Sarcopenia was assessed as indicated in the European Working Group on Sarcopenia in Older People
(EWGSOP) consensus. Results: Overall prevalence of sarcopenia was 13.1%, and it increased from 6.1% to 31.4% as MNA
decreased (P < .001). MNA score was lower in elderly subjects with sarcopenia (15.4 ± 4.2) than without sarcopenia (22.0 ±
4.0) (P = .024). Linear regression analysis showed that MNA score is linearly related both with muscle mass (r = 0.72; P < .001)
and strength (r = 0.42; P < .001). Multivariate analysis, adjusted for several confounding variables including comorbidity and
disability, confirmed these results. Conclusions: MNA score is low in noninstitutionalized elderly subjects with sarcopenia, and it
is linearly related to muscle mass and muscle strength. These data indicate that MNA score, when evaluated with muscle mass and
strength, may recognize elderly subjects with sarcopenia. (Nutr Clin Pract. 2018;33:879–886)

Keywords
aged; elderly; malnutrition; muscle strength; nutrition assessment; nutritional status; sarcopenia

Sarcopenia has been defined as a phenomenon character- elderly patients, and 22%–28% in this setting are at nutrition
ized by an age-related loss of muscle mass and strength risk.12 However, data on the prevalence of malnutrition in
particularly evident in older people aged >75 years.1-3
Sarcopenia is related to an increased risk for morbidity
and mortality in elderly people,4-6 especially in institution- From the 1 Department of Translational Medical Sciences, University
alized elderly nursing home residents.7 This pathological of Naples “Federico II”, Naples, Italy; 2 Department of Systems
condition is defined as a geriatric syndrome characterized Medicine, University of Rome Tor Vergata, Rome, Italy; 3 IRCCS San
by a loss of independence, a higher risk for falls, a reduc- Raffaele Pisana, Rome, Italy; 4 Division of Internal Medicine, AOU
San Giovanni di Dio e Ruggi di Aragona, Salerno, Italy; 5 Department
tion of the quality of life, and an increase in healthcare of Medicine and Health Sciences, University of Molise, Campobasso,
cost.1-3 From the pathophysiological point of view, several Italy; and 6 Azienda Ospedaliera dei Colli, Monaldi Hospital, Heart
factors may be involved in the pathogenesis of sarcope- Transplantation Unit, Naples, Italy.
nia including hormonal, metabolic, inflammatory state, Financial disclosure: None declared.
physical inactivity, and more importantly, malnutrition
Conflicts of interest: None declared.
state.8
[This article was modified on 2018-06-05 after initial online
Muscle protein loss at advancing age depends on a publication to correct reference 17.]
discrepancy between muscle protein synthesis and muscle
This article originally appeared online on February 13, 2018.
protein breakdown; in fact, muscle protein synthesis rates
are reduced in the older population with age-related decline Corresponding Author:
Pasquale Abete, MD, PhD, Associate Professor of Geriatrics,
at a rate of 3.5% per decade from age 20–90 years.9-11 It
Dipartimento di Scienze Mediche Traslazionali, Università di Napoli
is well known that protein-energy-malnutrition prevalence Federico II, Via S. Pansini, 80131 Naples, Italy.
in the acute care setting ranges between 23% and 60% of Email: p.abete@unina.it
880 Nutrition in Clinical Practice 33(6)

community-dwelling older adults are poor, although some Frailty status was assessed by the Italian Frailty Index
reports indicate a range of 5%–30%.12 derived by Rockwood’s frailty methods, recently validated
Moreover, malnutrition and sarcopenia often coexist in in an Italian cohort of elderly subjects.24 Fried’s frailty
a clinical syndrome characterized by a combination of methods were also assessed according to the Cardiovascular
decreased nutrient intake and decreased body weight, along Health Study Collaborative Research Group.25
with a decrease in muscle mass, strength, and/or physical
function (ie, malnutrition-sarcopenia syndrome [MSS]).13
Malnutrition and sarcopenia, taken together, are associated
Assessment of Nutrition Status
with negative health outcomes. Thus, it is extremely impor- Nutrition status was assessed by MNA. The MNA test
tant to assess malnutrition status, and more importantly, is composed of simple measurements and brief questions
nutrition assessment should be integrated with sarcopenia that can be completed in <10 minutes: (1) anthropometric
screening.13 measurements (weight, height, and weight loss); (2) global
Several malnutrition tools have been used with different assessment (6 questions related to lifestyle, medication, and
results.14 Mini Nutritional Assessment (MNA) represents mobility); (3) dietary questionnaire (8 questions, related to
1 of the more specific tool to assess malnutrition state in number of meals, food and fluid intake, and autonomy of
geriatric settings.15 However, this approach, together with feeding); and (4) subjective assessment (self-perception of
sarcopenia screening, is not well investigated in outpatient health and nutrition). The sum of the MNA score distin-
older adults. guishes between elderly patients: (1) with adequate nutrition
Thus, in this study, we aimed to investigate the rela- status (MNA ࣙ 24), (2) with protein-calorie malnutrition
tionship between muscle mass and strength and malnutri- (MNA >17), and (3) at risk for malnutrition (MNA between
tion evaluated by MNA in outpatients older adults who 17 and 23.5). With this scoring, sensitivity was found to be
underwent Comprehensive Geriatric Assessment (CGA), 96%, specificity 98%, and predictive value 97%.26
including several clinical and biochemical parameters.
Assessment of Muscle Mass and Strength
Methods
Muscle mass was measured by bioelectrical impedance
Study Population analysis (BIA) using a Quantum/S Bioelectrical Body Com-
The study enrolled 473 consecutive elderly outpatients (ࣙ65 position Analyzer (Akern Srl, Florence, Italy). Whole-body
years) admitted to a CGA center. The study received BIA measurements were taken between the right wrist and
full ethical approval from research ethics committees in ankle with the subject in a supine position. Muscle mass
accordance with the ethical standards laid down in the was calculated using the following BIA equation of Janssen
1964 Declaration of Helsinki and its later amendments. All and colleagues.27 Skeletal muscle mass (kg) = ([height2 /BIA
participants signed an informed consent form, and the insti- resistance × 0.401] + [gender × 3.825] + [age × −0.71])
tutional review boards approved the study. Anthropometric + 5.102, where height is measured in centimeters; BIA
measurements including age, sex, body mass index (BMI), resistance is measured in ohms; for gender, men = 1 and
and waist circumference (WC) were performed.16,17 women = 0; and age is measured in years. Absolute skeletal
muscle mass (kg) was converted to skeletal muscle index
standardizing by meters squared (kg/m2 ). Muscle strength
Comprehensive Geriatric Assessment was assessed by grip strength, measured using a hand-grip
Elderly participants underwent a comprehensive geri- dynamometer (Mecmesin Advanced Force Gauge 500N;
atric multidimensional evaluation that included cognitive GDM, Corsico (MI), Italy). The participant squeezed the
function evaluation with Mini-Mental State Examination dynamometer with maximum effort for at least 5 seconds.
(MMSE)18 ; depressive symptoms with Geriatric Depression Hand-grip strength was tested 3 times with a minimum of
Scale (GDS)19 ; comorbidity and comorbidity severity with 60 seconds rest provided for recovery between each attempt.
a Cumulative Illness Rating Scale (CIRS-Comorbidity and Maximum grip strength was recorded as the highest value of
CIRS-Severity)20 and drug number; disability with basic 3 trials. The maximum value was used rather than the mean
and instrumental activities of daily living (BADLs and of 3 trials allowing for a measure that was independent
IADLs, respectively); physical performance with 4-m gait of fatigue, which may have been possible in some of the
speed (cutoff < 0.8 m/s)21 ; physical activity with Physical participants. BMI-adjusted values were used as a cutoff
Activity Scale for the Elderly (PASE)22 ; social support eval- point to classify low muscle strength (BMI ࣘ24, 24.1–28,
uation with Social Support Assessment (SSA) scored from <28 was 29, ࣘ30, and ࣘ32 kg for men; BMI ࣘ23, 23.1–
17 (participants with the lowest support) to 0 (participants 26, 26.1–29, and <29 was 17, ࣘ17.3, ࣘ18, and ࣘ21 kg for
with the highest support)23 and Tinetti Mobility Test or women, respectively).25 Using the cutoff points indicated
Performance-Oriented Mobility Assessment (TMT). in the European Working Group on Sarcopenia in Older
Liguori et al 881

People (EWGSOP) consensus, subjects with a low grip 4-m gait speed decreased as MNA score decreased. GDS
strength presenting low muscle mass (skeletal muscle index score, BADLs and IADLs lost, and low social support
<8.87 and 6.42 kg/m2 in men and women, respectively) were increase as MNA score decreased. Similarly, both frailty
classified as “sarcopenia.”28 by Fried’s score and Rockwood’s score increased as MNA
score decreased. Among biomarkers, lymphocytes and b-
Biochemical Parameters CHE decreased, whereas CRP increased as MNA score
decreased.
Hemoglobin (normal values: 12.0–17.5 g/dL in men and Figure 1 shows the relationship among skeletal muscle
12.0–16.0 g/dL in women), lymphocytes (normal values: mass and strength stratified by MNA score in nonin-
1.0–4.8 × 103 ), serum albumin level (normal values: 3.6– stitutionalized elderly people. Muscle mass progressively
5.2 g/dL), total iron binding capacity (normal values: 218– decreased (from 17.6 ± 3.0 to 10.0 ± 2.9 kg/m2 ), as well as
411 μg/dL), C-reactive protein (CRP; normal values: <5 muscle strength (from 41.2 ± 10.2 to 27.7 ± 8.3 kg), as MNA
mg/dL), and butyryl-cholinesterase (b-CHE; normal values: score decreased.
5.400–13.200 U/L) were routinely obtained. At univariate analysis, age, CIRS-severity score, number
of drugs, BADLs lost, and CRP were negatively correlated
Statistical Analysis with skeletal muscle mass, whereas Tinetti score, 4-m gait
Baseline characteristics of the sample are expressed as speed, PASE score, serum albumin level, hemoglobin, b-
mean ± standard deviation. Participants were stratified CHE, and, more importantly, MNA score were positively
by the presence or absence of sarcopenia and stratified correlated with skeletal muscle mass. Multivariate analysis
by categories of MNA (<17, 17–23.5, ࣙ24). Categorical confirms this correlation except for serum albumin level and
variables were analyzed using χ 2 testing, continuous vari- CRP (Table 3). The positive linear relation between skeletal
ables using a 1-way analysis of variance, and nonparametric muscle mass and MNA score is shown in Figure 2A (y =
variables (ie, PASE score and lymphocyte number) using 0.65x + 2.2; r = 0.72; P < .001).
Wilcoxon-Mann-Whitney. Univariate regression analysis Univariate and multivariate linear regression analysis on
was used to test a correlation among muscle mass and muscle strength is shown in Table 3. Age, CIRS comorbidity
strength, and MNA score with other variables such as and severity, number of drugs, BADLs lost, and CRP were
age, BMI, WC, MMSE, GDS, CIRS-Comorbidity, CIRS- negatively correlated with muscle strength, whereas Tinetti
Severity, drug number, BADLs, IADLs, PASE, 4-m walking score, 4-m gait speed, PASE score, hemoglobin, b-CHE, and
speed, TMT, and social support score. Statistically signifi- MNA score were positively correlated with muscle strength.
cant variables were included into a multivariate regression Except for CRP, all linear relationships were confirmed at
model as potential confounders. All statistical analyses multivariate analysis. The positive linear relation between
were performed with SPSS software (version 15.0; SPSS, muscle strength and MNA score is shown in Figure 2B
Chicago, IL). A P value <.05 was considered statistically (y = 1.1x + 14.2; r = 0.46; P < .001).
significant.
Discussion
Results Our data show that MNA score, 1 of the most specific
tools for the assessment of malnutrition, is lower in non-
A total of 473 elderly subjects with a mean age of 80.9
institutionalized older adults with sarcopenia than in those
± 6.6 years was studied. Table 1 lists the anthropometric
without sarcopenia. Interestingly, MNA score is strongly
measurements, CGA, and biochemical assessment stratified
related to muscle mass and strength both at univariate and
in sarcopenia and nonsarcopenia according to EWGSOP
multivariate analyses. This evidence suggests that malnutri-
definition and diagnostic algorithm. The prevalence rate
tion state is frequently associated with a reduction of muscle
of sarcopenia was 13.1%. CIRS comorbidity and severity
mass and strength; therefore, it should be investigated,
score, drug number, and CRP were higher, whereas 4-minute
especially in the presence of sarcopenia in noninstitution-
gait speed, Tinetti score, and b-CHE were lower in elderly
alized older adults.
subjects with sarcopenia. In addition, MNA score together
with muscle mass and grip strength were lower in elderly
Sarcopenia
subjects with sarcopenia with respect to elderly subjects
without sarcopenia (Table 1). Age-related muscle mass decline is defined “sarcopenia,”
Table 2 lists the same parameters stratified for different and it is primarily due to the progressive atrophy and
levels of MNA score (ࣙ24, 17–23.5, and <17). Prevalence loss of type II muscle fibers and motor neurons.29 This
of sarcopenia progressively increased as MNA decreased phenomenon tends to be reduced at a rate of 1%–2% per
(from 6.1% to 31.4%; P < .001). Elderly subjects were year after the age of 50 years.1-3 Sarcopenia is characterized
progressively older, and MMSE and Tinetti score and by fibrosis and infiltration of adipose tissue determining a
882 Nutrition in Clinical Practice 33(6)

Table 1. Baseline Characteristics of the 473 Elderly Patients Enrolled in the Study Stratified for the Presence and Absence of
Sarcopenia.

Sarcopeniaa

All No (86.9%) Yes (13.1%)


Characteristics (N = 473) (n = 411) (n = 62) Pb

Anthropometric data
Age ± SD, y 80.9 ± 6.6 74.3 ± 8.1 80.5 ± 7.6 .145
Female sex, % 60.9 64.5 37.1 .057
BMI ± SD, kg/m2 27.4 ± 5.6 27.2 ± 3.1 24.2 ± 4.0 .064
Waist circumference ± SD, cm 99.7 ± 13.5 99.0 ± 10.8 96.4 ± 11.4 .007
Geriatric evaluation ± SD
Mini-Mental State Examination score 21.5 ± 6.3 23.2 ± 6.4 21.6 ± 4.4 .059
Geriatric Depression Scale score 7.6 ± 4.4 6.7 ± 4.6 8.6 ± 5.4 .187
CIRS-Comorbidity score 3.9 ± 2.2 3.40 ± 1.79 5.12 ± 2.05 .024
CIRS-Severity score 1.9 ± 0.5 1.60 ± 0.22 2.34 ± 0.55 .030
No. of drugs 6.1 ± 3.2 2.0 ± 1.0 4.0 ± 1.0 .020
BADLs lost, n 2.0 ± 1.8 1.4 ± 1.6 2.6 ± 1.8 .212
IADLs lost, n 4.2 ± 2.8 2.8 ± 1.4 4.0 ± 3.2 .321
Tinetti score 17.3 ± 7.8 22.4 ± 4.0 18.2 ± 2.2 .020
MNA score 20.9 ± 4.3 22.0 ± 4.0 15.4 ± 4.2 .024
4-m gait speed, m/s 0.46 ± 0.4 0.91 ± 0.20 0.60 ± 0.30 <.05
PASE score 37.6 ± 51.1 102.0 ± 40.8 38.4 ± 80.2 <.001
Social support score 8.3 ± 4.9 7.0 ± 2.0 9.5 ± 2.0 <.05
Fried’s frailty score 3.5 ± 1.5 2.2 ± 1.2 3.6 ± 1.2 <.05
Rockwood’s frailty score 21.2 ± 8.7 14.6 ± 9.4 28.2 ± 6.2 <.05
Muscle measurements
Grip strength, kg 26.2 ± 7.6 30.4 ± 8.6 21.8 ± 8.4 <.05
Skeletal muscle mass, kg/m2 8.0 ± 1.6 9.0 ± 1.6 6.6 ± 1.4 <.05
Biochemical measurements ± SD
Serum albumin level, g/dL 4.1 ± 0.7 4.0 ± 0.4 3.4 ± 0.8 .560
Total iron binding capacity, μg/dL 325.6 ± 54.6 296.4 ± 68.2 222.8 ± 74.2 .266
Hemoglobin, g/dL 12.9 ± 1.8 13.2 ± 1.4 12.4 ± 2.0 .059
Lymphocytes, n × 103 4.1 ± 8.2 2.2 ± 1.0 1.7 ± 1.7 .112
C-reactive protein, mg/dL 0.8 ± 0.4 0.40 ± 0.28 0.90 ± 0.44 <.05
Butyryl-cholinesterase, U/L 7480 ± 2320 8600 ± 1450 3400 ± 2850 <.05

BADLs, basic activities of daily living; BMI, body mass index; CIRS, Cumulative Index Rating Scale; IADLs, instrumental activities of daily
living; MNA, Mini Nutritional Assessment; PASE, Physical Activity Scale for the Elderly.
a Sarcopenia was defined in subjects with a low muscle strength presenting low muscle mass (skeletal muscle index <8.87 and <6.42 kg/m2 in men

and women, respectively). BMI-adjusted values were used as a cutoff point to classify low muscle strength (BMI ࣘ24, 24.1–28, and <28 was 29,
ࣘ30, and ࣘ32 kg for men; BMI ࣘ23, 23.1–26, 26.1–29, and <29 was 17, ࣘ17.3, ࣘ18, and ࣘ21 kg for women, respectively).
b P = statistical difference between the presence and the absence of sarcopenia.

reduction of functional capacity, an increase of disability Therefore, elderly adults may lose muscle mass and
and mortality, and therefore an increase of healthcare strength.33 Accordingly, older adults usually eat less protein
costs.3-5,30 Many mechanisms have been hypothesized to than younger adults.31 In fact, community-dwelling older
explain the origin of age-related decline in muscle strength adults (ࣈ10%) and those living in care homes (ࣈ30%) do not
and mass, including inflammation, physical inactivity, and consume the estimated average requirement for daily protein
malnutrition.31,32 intake (0.7 g/kg body weight/day),34,35 which represents the
minimum intake level to maintain muscle integrity for older
Malnutrition and Sarcopenia adults.36,37

The relationship between malnutrition and sarcopenia is Mini Nutritional Assessment as Tool
not well established, especially in elderly outpatients.29 A
disproportion between protein intake and protein needs may
for Malnutrition Detection
determine a loss of skeletal muscle mass because of im- Because malnutrition in the elderly is multifactorial, several
balance between muscle protein synthesis and degradation. measures of malnutrition in geriatric people have been
Liguori et al 883

Table 2. Baseline Characteristics of the 473 Older Adult Participants Enrolled in the Study stratified for Mini Nutritional
Assessment.

Mini Nutritional Assessment score

ࣙ24 (51.0%) 17-23.5 (34.2%) <17 (14.8%) P


Characteristics (n = 241) (n = 162) (n = 70) for Trend

Anthropometric data
Age ± SD, y 79.7 ± 6.5a 81.3 ± 6.7 81.8 ± 6.3 .001
Female sex, % 27.4 46.3 26.3 .432
Body mass index, kg/m2 28.1 ± 5.0a 27.6 ± 6.2 26.1 ± 5.0 <.05
Waist circumference, cm 100.3 ± 9.4a 98.5 ± 11.2 98.2 ± 10.1 <.05
Geriatric evaluation ± SD
Mini-Mental State Examination score 24.3 ± 4.9a 21.0 ± 6.3 18.5 ± 6.8 <.001
Geriatric Depression Scale score 4.8 ± 3.6a 8.3 ± 4.0 10.1 ± 4.1 <.001
CIRS-Comorbidity score 3.1 ± 2.1 4.1 ± 2.2 4.4 ± 2.0 .456
CIRS-Severity score 1.7 ± 0.4 1.9 ± 0.5 2.0 ± 0.4 .455
No. of drugs 5.2 ± 3.3 6.5 ± 3.0 6.6 ± 3.2 .184
BADLs lost, n 1.0 ± 1.5 2.1 ± 1.8 3.2 ± 1.8 <.05
IADLs lost, n 2.5 ± 2.6 4.5 ± 2.6 5.9 ± 2.2 <.05
Tinetti score 21.9 ± 6.0 16.2 ± 7.5 12.8 ± 7.1 <.05
MNA score 25.8 ± 1.5a 20.6 ± 1.8 14.5 ± 2.2 <.001
4-m gait speed, m/s 0.66 ± 0.47 0.46 ± 0.5 0.33 ± 0.5 <.05
PASE score 65.4 ± 60.8a 28.9 ± 43.8 16.1 ± 28.7 <.05
Social support score 5.4 ± 3.9 8.9 ± 4.6 11.4 ± 4.2 <.05
Fried’s frailty score 2.6 ± 1.5 3.6 ± 1.4 4.5 ± 1.3 <.001
Rockwood’s frailty score 15.7 ± 8.0 22.2 ± 7.4 27.2 ± 7.1 <.001
Sarcopenia, n (%) 15 (6.2) 25 (15.4) 22 (31.4) <.001
Muscle measurements ± SD
Grip strength, kg 41.2 ± 10.2 38.1 ± 9.3 27.7 ± 10.3 <.001
Skeletal muscle mass, kg/m2 17.6 ± 1.5 16.8 ± 2.1 10.0 ± 2.9 <.001
Biochemical measurements ± SD
Serum albumin level, g/dL 4.2 ± 0.5 4.2 ± 0.9 3.9 ± 0.4 .052
Total iron binding capacity, μg/dL 350.4 ± 50.4 341.0 ± 60.2 265.0 ± 80.2 .163
Hemoglobin, g/dL 13.2 ± 1.8 13.0 ± 1.7 12.0 ± 1.9 .420
Lymphocytes, n × 103 5.0 ± 9.8 4.9 ± 9.3 1.2 ± 0.6 <.05
C-reactive protein, mg/dL 0.50 ± 0.42a 0.64 ± 0.50 0.95 ± 0.30 .048
Butyryl-cholinesterase, U/L 7950 ± 2150 7650 ± 2300 7000 ± 2100 .042

BADLs, basic activities of daily living; CIRS, Cumulative Index Rating Scale; IADLs, instrumental activities of daily living; MNA, Mini
Nutritional Assessment; PASE, Physical Activity Scale for the Elderly.
a P < .01 vs MNA score <17.

developed. Biochemical and clinical indices are investi- Sarcopenia and Mini Nutritional Assessment
gated by Nutritional Risk Index38 and Geriatric Nutri- Score
tional Risk Index39 ; anthropometry, mobility, cognitive
state, self-perceived health, and nutrition by Short Form In our noninstitutionalized older adults, MNA score pro-
MNA,40 by Malnutrition Universal Screening Tool,41 and gressively decreases as muscle mass and strength are
by unintentional weight loss and poor intake (MST)42 ; and reducing in both univariate (r = 0.72 and r = 0.46, respec-
medical history and clinical and subjective evaluation by tively) and multivariate (r = 0.62 and r = 0.40, respectively)
Nutrition Risk Screening 2002 (NRS-2002).43 In contrast analyses. Interestingly, MNA score is significantly lower in
with nutrition screening tools, nutrition assessment methods subjects with sarcopenia vs without sarcopenia (15.4 ± 4.2
are more comprehensive and are frequently used by geria- vs 22.0 ± 4.0; P < .024). Some reports have investigated the
tricians. In particular, the Subjective Global Assessment44 relationship between MNA and sarcopenia. However, this
and MNA45 are largely used to perform a nutrition di- relationship in noninstitutionalized older adults is poorly
agnosis and begin nutrition management in older adult investigated. In contrast, among acute geriatric patients,
patients.46 malnutrition evaluated with MNA was associated to 30%
884 Nutrition in Clinical Practice 33(6)

Figure 1. Muscle mass and strength stratified by Mini


Nutritional Assessment score (ࣙ24, 17–23.5, <17) in
noninstitutionalized elderly people; P for trend = .001 for
both muscle mass (*P < .05 for <17 vs 17–23.5 and ࣙ24) and
strength (*P < .05 for <17 vs 17–23.5 and ࣙ24).

of the patients with sarcopenia.47 In addition, among male


residents in a nursing home, MNA scores were significantly
lower in residents having low compared with having normal
skeletal muscle mass (17.1 ± 3.4 vs 19.6 ± 2.5; P = .005).48
More importantly, in a prospective study, subjects with
malnutrition risk and sarcopenia have a risk for mortality 4
times higher than subjects without sarcopenia with normal
nutrition.49 Therefore, Vandewoude et al13 recently indi-
cated the MSS to depict the clinical scenario characterized
by both malnutrition and sarcopenia. Finally, it should
be emphasized that malnutrition plays a key role in the
pathogenesis of both frailty and sarcopenia.8 Malnutrition Figure 2. Regression linear relationship among muscle mass
and sarcopenia are frequently present in older adults with (A) and muscle strength (B) and Mini Nutritional Assessment
diabetes and chronic obstructive pulmonary disease that are score for noninstitutionalized elderly people.
characterized by a high degree of frailty.50,51 Interestingly,
the “frailty score” identified by Fried’s and Rockwood’s
methods was 2.6 ± 1.5 and 15.7 ± 8.0 at the highest status should be always evaluated to address therapeutical
MNA and 4.5 ± 1.3 and 27.2 ± 7.1 at the lowest MNA, interventions and lifestyle modifications (ie, increase of
respectively. protein intake and physical activity).3 Thus, it is mandatory
for clinician researchers to develop a reliable and valid
Evaluation of Nutrition Status in Patients With diagnostic algorithm to identify elderly subjects with both
Sarcopenia: Clinical Implications malnutrition and sarcopenia.

As discussed earlier, malnutrition and sarcopenia are con-


Conclusions
ditions frequently found in older adults that lead to nega-
tive outcomes including increased morbidity and mortality MNA score, 1 of the most accepted instruments for the
and increased healthcare costs and rehospitalizations.8,13,49 assessment of malnutrition, is lower in noninstitutionalized
Usually, these conditions have been separately screened, older adults with sarcopenia. Thus, the presence of mal-
but rarely are both conditions simultaneously assessed.8,13 nutrition is strongly related to muscle mass and strength.
Moreover, many patients concurrently show malnutrition These findings support that low MNA score is frequently
and sarcopenia; therefore, patient’s nutrition and functional associated to elderly outpatients with sarcopenia.
Liguori et al 885

Table 3. Univariate and Multivariate Linear Regression Analyses on Skeletal Muscle Mass and Muscle Strength.

Muscle Mass Muscle Strength

Univariate Multivariate Univariate Multivariate

Variables r P r P r P r P

Age −0.14 <.05 −0.15 <.05 −0.18 <.05 −0.16 <.05


Body mass index 0.06 .204 0.04 .220
Waist circumference 0.12 .340 0.06 .320
Mini-Mental State Examination 0.08 .120 0.08 .102
Geriatric Depression Scale −0.14 .347 −0.10 .300
CIRS-Comorbidity −0.10 .340 −0.10 <.05 −0.08 <.05
CIRS-Severity −0.07 .032 −0.06 <.05 −0.10 <.01 −0.09 <.01
No. of drugs −0.08 .030 −0.07 <.01 −0.04 .042 −0.04 <.05
BADLs −0.14 <.05 −0.12 <.05 −0.14 <.05 −0.12 <.05
IADLs −0.08 .342 −0.04 .442
Mini Nutritional Assessment 0.72 <.01 0.62 <.05 0.46 <.01 0.40 <.05
Tinetti score 0.65 <.01 0.051 .03 0.44 <.01 0.39 <.05
4-m gait speed 0.30 <.05 0.29 <.05 0.32 .05 0.28 <.05
PASE 0.57 <.05 0.30 .04 0.41 .001 0.29 <.05
Social support −0.04 .282 −0.07 .541
Serum albumin level 0.18 .022 0.14 .084 0.12 .064
Total iron binding capacity 0.14 .112 0.14 .122
Hemoglobin 0.24 <.04 0.20 <.05 0.30 <.05 0.26 .020
Lymphocytes 0.14 .114 0.15 .75
C-reactive protein −0.24 <.05 −0.08 .421 −0.20 <.05 −0.18 .325
Butyryl-cholinesterase 0.35 <.01 0.30 <.01 0.44 <.01 0.40 .036

BADLs, basic activities of daily living; CIRS, Cumulative Index Rating Scale; IADLs, instrumental activities of daily living; PASE, Physical
Activity Scale for the Elderly.

Acknowledgments 5. Iannuzzi-Sucich M, Prestwood KM, Kenny AM. Prevalence of sar-


copenia and predictors of skeletal muscle mass in healthy, older men
Funding source: Fondazione Roma NCDS-2013-00000331 –
and women. J Gerontol A Biol Sci Med Sci. 2002;57:M772-M777.
Sarcopenia and Insulin Resistance in the Elderly; Age- 6. Metter EJ, Talbot LA, Schrager M, Conwit R. Skeletal muscle strength
Associated Inflammation as a Shared Pathogenic Mechanism as a predictor of all-cause mortality in healthy men. J Gerontol A Biol
and Potential Therapeutic Target (DDM), Rome, ITALY. Sci Med Sci. 2002;57:B359-B365.
7. Landi F, Liperoti R, Fusco D, Mastropaolo S, Quattrociocchi D, Proia
Statement of Authorship A. Sarcopenia and mortality among older nursing home residents. J Am
Med Dir Assoc. 2012;13:121-126.
I. Liguori, F. Cacciatore, D. Bonaduce and P. Abete contributed 8. Cruz-Jentoft AJ, Kiesswetter E, Drey M, Sieber CC. Nutrition, frailty,
to conception and design; D. Della-Morte, G. Gargiulo and and sarcopenia. Aging Clin Exp Res. 2017;29:43-48.
G. Testa contributed to analysis and interpretation of data; 9. Walrand S, Guillet C, Salles J, Cano N, Boirie Y. Physiopathological
F. Curcio, G. Russo, M. Cellurale L. Aran and G. Bulli mechanism of sarcopenia. Clin Geriatr Med. 2011;27:365-385.
contributed to acquisition of data. 10. Cooper C, Fielding R, Visser M, et al. Tools in the assessment of
sarcopenia. Calcif Tissue Int. 2013;93:201-210.
11. Mithal A, Bonjour JP, Boonen S, et al; IOF CSA Nutrition Working
References Group. Impact of nutrition on muscle mass, strength, and performance
1. Baumgartner RN, Koehler KM, Gallagher D, et al. Epidemiology in older adults. Osteoporos Int. 2013;24:1555-1566.
of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 12. Agarwal E, Miller M, Yaxley A, Isenring E. Malnutrition in the elderly:
1998;147:755-763. a narrative review. Maturitas. 2013;76:296-302.
2. Marcell TJ. Sarcopenia: causes, consequences, and preventions. J 13. Vandewoude MF, Alish CJ, Sauer AC, Hegazi RA. Malnutrition-
Gerontol A Biol Sci Med Sci. 2003;58:M911-M916. sarcopenia syndrome: is this the future of nutrition screening and
3. Rolland Y, Czerwinski S, Abellan Van Kan G, et al. Sarcopenia: its as- assessment for older adults? J Aging Res. 2012;2012:651570.
sessment, etiology, pathogenesis, consequences and future perspectives. 14. van Bokhorst-de van der Schueren MA, Guaitoli PR, Jansma EP, et al.
J Nutr Health Aging. 2008;12:433-450. Nutrition screening tools: does one size fit all? A systematic review of
4. Rantanen T, Guralnik JM, Sakari-Rantala R, et al. Disability, physical screening tools for the hospital setting. Clin Nutr. 2014;33:39-58.
activity, and muscle strength in older women: the Women’s Health and 15. Guigoz Y. The Mini Nutritional Assessment (MNA) review of the
Aging Study. Arch Phys Med Rehabil. 1999;80:130-135. literature: what does it tell us? J Nutr Health Aging. 2006;10:466-485.
886 Nutrition in Clinical Practice 33(6)

16. Testa G, Cacciatore F, Galizia G, et al. Waist circumference but not 35. Tieland M, Borgonjen-Van Den Berg K, van Loon LJ, de Groot LC.
body mass index predicts long-term mortality in elderly subjects with Dietary protein intake in community-dwelling, frail, and institutional-
chronic heart failure. J Am Geriatr Soc. 2010;58:1433-1440. ized elderly people: scope for improvement. Eur J Nutr. 2012;51:173-
17. Cacciatore F, Testa G, Langellotto A, et al. Role of ventricular rate 179.
response on dementia in cognitively impaired elderly subjects with atrial 36. Bauer J, Biolo G, Cederholm T, et al. Evidence-based recommenda-
fibrillation: a 10-year study. Dement Geriatr Cogn Disord. 2012;34:143- tions for optimal dietary protein intake in older people: a position paper
148. from the PROT-AGE study group. J Am Med Dir Assoc. 2013;14:542-
18. Testa G, Cacciatore F, Galizia G, et al. Depressive symptoms predict 559.
mortality in elderly subjects with chronic heart failure. Eur J Clin Invest. 37. Deutz NE, Bauer JM, Barazzoni R, et al. Protein intake and exercise
2011;41:1310-1317. for optimal muscle function with aging: recommendations from the
19. Testa G, Cacciatore F, Galizia G, et al. Charlson Comorbidity Index ESPEN Expert Group. Clin Nutr 2014;33:929-936.
does not predict long-term mortality in elderly subjects with chronic 38. Wolinsky F, Coe RM, McIntosh WA, et al. Progress in the development
heart failure. Age Ageing. 2009;38:734-740. of a nutritional risk index. J Nutr. 1990;120:1549-1553.
20. Washburn RA, Smith KW, Jette AM, Janney CA. The Physical Activity 39. Cereda E, Pedrolli C. The geriatric nutritional risk index. Curr Opin
Scale for the Elderly (PASE): development and evaluation. J Clin Clin Nutr Metab Care. 2009;12:1-7.
Epidemiol. 1993;46:153e62. 40. Rubenstein L, Harker J, Salva A, Guigoz Y, Vellas B. Screening
21. Peel NM, Kuys SS, Klein K. Gait speed as a measure in geriatric for undernutritionin geriatric practice: developing the short-form
assessment in clinical settings: a systematic review. J Gerontol A Biol mini nutritional assessment (MNA-SF). J Gerontol. 2001;56A:M366-
Sci Med Sci. 2013;68:39-46. M372.
22. Abete P, Cacciatore F, Ferrara N, et al. Body mass index and preinfarc- 41. Malnutrition Advisory Group (MAG). The ‘MUST’ Explanatory
tion angina in elderly patients with acute myocardial infarction. Am J Booklet. A Guide to the ‘Malnutrition Universal Screening Tool’
Clin Nutr. 2003;78:796-801. (‘MUST’) for Adults: A Standing Committee of the British Association
23. Mazzella F, Cacciatore F, Galizia G, et al. Social support and long- for Parenteral and Enteral Nutrition (BAPEN). Worcestershire (UK):
term mortality in the elderly: role of comorbidity. Arch Gerontol Redditch; 2003.
Geriatr. 2010;51:323-328. 42. Ferguson M, Capra S, Bauer J, Banks M. Development of a valid and
24. Abete P, Basile C, Bulli G, et al. The Italian version of the “frailty reliable malnutrition screening tool for adult acute hospital patients.
index” based on deficits in health: a validation study. Aging Clin Exp Nutrition. 1999;15:458-464.
Res. 2017;29(5):913-926. 43. Kondrup J, Rasmussen H, Hamberg O, et al. An ad hoc ESPEN Work-
25. Fried LP, Tangen CM, Walston J, et al; Cardiovascular Health Study ing Group. Nutritional Risk Screening (NRS 2002): a new method
Collaborative Research Group. Frailty in older adults: evidence for a based on analysis of controlled clinical trials. Clin. Nutr. 2003;22:321-
phenotype. J Gerontol A Biol Sci Med Sci. 2001;56:M146-M156. 336.
26. Vellas B, Guigoz Y, Garry PJ, et al. The Mini Nutritional Assessment 44. Detsky A, McLaughlin J, Baker J. What is subjective global assess-
(MNA) and its use in grading the nutritional state of elderly patients. ment of nutritional status. JPEN J Parenter Enteral Nutr. 1987;11:
Nutrition. 1999;15:116-122. 8-13.
27. Janssen I, Heymsfield SB, Baumgartner RN, Ross R. Estimation 45. Guigoz Y, Vellas B, Garry P. Assessing the nutritional status of
of skeletal muscle mass by bioelectrical impedance analysis. J Appl the elderly: the mini nutritional assessment as part of the geriatric
Physiol. 2000;89:465-471. evaluation. Nutr Rev. 1996;54:S59-S65.
28. Volpato S, Bianchi L, Cherubini A, et al. Prevalence and clinical cor- 46. Young AM, Kidston S, Banks MD, et al. Malnutrition screening tools:
relates of sarcopenia in community-dwelling older people: application comparison against two validated nutrition assessment methods in
of the EWGSOP definition and diagnostic algorithm. J Gerontol A Biol older medical inpatients. Nutrition. 2013;29:101-106.
Sci Med Sci. 2014;69:438-446. 47. Jacobsen EL, Brovold T, Bergland A, et al. Prevalence of factors
29. Cruz-Jentoft AJ, Landi F, Topinkova E, et al. Understanding sarcope- associated with malnutrition among acute geriatric patients in Norway:
nia as a geriatric syndrome. Curr Opin Clin Nutr Metab Care. 2010;13: a cross-sectional study. BMJ Open. 2016;6:e011512.
1-7. 48. Tufan A, Bahat G, Ozkaya H, et al. Low skeletal muscle mass index is
30. Goodpaster BH, Chomentowski P, Ward BK, et al. Effects of physical associated with function and nutritional status in residents in a Turkish
activity on strength and skeletal muscle fat infiltration in older adults: nursing home. Aging Male. 2016;19:182-186.
a randomized controlled trial. J Appl Physiol. 2008;105:1498-1503. 49. Hu X, Zhang L, Wang H, et al. Malnutrition-sarcopenia syndrome
31. Morley JE, Baumgartner RN. Cytokine-related aging process. J Geron- predicts mortality in hospitalized older patients. Sci Rep. 2017;7:
tol A Biol Sci Med Sci. 2004;59:924-929. 3171.
32. Soeters PB, Schols AM. Advances in understanding and assessing 50. Galizia G, Cacciatore F, Testa G, et al. Role of clinical frailty on
malnutrition. Curr Opin Clin Nutr Metab Care. 2009;12:487-494. long-term mortality of elderly subjects with and without chronic
33. Meng X, Zhu K, Devine A, Kerr DA, Binns CW, Prince RL. A 5-year obstructive pulmonary disease. Aging Clin Exp Res. 2011;23:
cohort study of the effects of high protein intake on lean mass and 118-125.
BMC in elderly postmenopausal women. J Bone Miner Res. 2009;24: 51. Abete P, Della-Morte D, Gargiulo G, Basile C, Langellotto A, Galizia
1827-1834. G, Testa G, Canonico V, Bonaduce D, Cacciatore F. Cognitive
34. Volpi E, Campbell WW, Dwyer JT, et al. Is the optimal level of impairment and cardiovascular diseases in the elderly. A heart-brain
protein intake for older adults greater than the recommended dietary continuum hypothesis. Ageing Res Rev. 2014;18:41-52.
allowance. J Gerontol A Biol Sci Med Sci. 2013;68:677-681.

You might also like