Sie sind auf Seite 1von 11

DOI: 10.1111/eci.

12637

ORIGINAL ARTICLE

Nutritional predictors of mortality after discharge in


elderly patients on a medical ward
Silvio Buscemi*, John A. Batsis†, Gaspare Parrinello*, Fatima M. Massenti‡, Giuseppe Rosafio*,
Vittoria Sciascia*, Flavia Costa§, Sebastiano Pollina Addario¶, Serena Mendola*, Anna M. Barile*,
Vincenza Maniaci*, Nadia Rini* and Gregorio Caimi*
*Dipartimento Biomedico di Medicina Interna e Specialistica (DIBIMIS), Laboratorio di Metabolismo e Nutrizione Clinica,
Policlinico P. Giaccone, University of Palermo, Palermo, Italy, †Section of General Internal Medicine at Dartmouth, The
Dartmouth Institute for Health Policy & Clinical Practice, Geisel School of Medicine at Dartmouth, Lebanon, NH, USA,

Dipartimento di Scienze per la Promozione della Salute e Materno Infantile, Policlinico P. Giaccone, University of Palermo,
Palermo, Italy, §Servizio di Ingegneria Clinica, Policlinico ‘P. Giaccone’, Palermo, Italy, ¶Dipartimento Attivita
 Sanitarie ed
Osservatorio Epidemiologico, Regione Siciliana, Palermo, Italy

ABSTRACT
Background Malnutrition in elderly inpatients hospitalized on medical wards is a significant public health con-
cern. The aim of this study was to investigate nutritional markers as mortality predictors following discharge in
hospitalized medical elderly patients.
Materials and methods This is a prospective observational cohort study with follow-up of 48 months. Two
hundred and twenty-five individuals aged 60 and older admitted from the hospital emergency room in the past
48 h were investigated at the medical ward in the University hospital in Palermo (Italy). Anthropometric and
clinical measurements, Mini-nutritional Assessment (MNA) questionnaire, bioelectrical (BIA) phase angle (PA),
grip strength were obtained all within 48 h of admission. Mortality data were verified by means of mortality
registry and analysed using Cox-proportional hazard models.
Results Ninety (40%) participants died at the end of follow-up. There were significant relationships between
PA, MNA score, age and gender on mortality. Patients in the lowest tertile of PA (< 46°) had higher mortality
estimates [I vs II tertile: hazard ratio (HR) = 340; 95% confidence interval (CI): 201–577; II vs III tertile:
HR = 383; 95% CI: 221–664; log-rank test: v2 = 436; P < 0001]. Similarly, the survival curves demonstrated
low MNA scores (< 22) were associated with higher mortality estimates (HR = 185; 95% CI: 122–281
v2 = 82; P = 0004).
Conclusions The MNA and BIA-derived phase angle are reasonable tools to identify malnourished patients at
high mortality risk and may represent useful markers in intervention trials in this high-risk subgroup.
Keywords Bioimpedance, hospitalization, malnutrition, mini-nutritional assessment, mortality, phase angle.
Eur J Clin Invest 2016; 46 (7): 609–618

malnutrition in this subset of patients and selecting biomarkers


Introduction
may be useful in predicting clinical events, allowing clinicians
Malnutrition in elderly inpatients hospitalized on medical to target specific nutritional interventions [9–11].
wards is a significant public health concern [1] affecting up to Simple and reproducible methods that are clinically practical
60–70% of this subpopulation [2,3]. Malnutrition is a well- and easily available have not been fully validated in longitu-
established predictor of mortality in hospitalized patients [4,5]. dinal studies. Among commonly available instruments for
As a recognized independent risk factor for morbidity and malnutrition screening is the Mini-nutritional Assessment
mortality [6,7], malnutrition likely contributes to the posthos- (MNA) [12], a practical, well known questionnaire with excel-
pital syndrome [8], leading to high rates of 30-day readmissions lent external validity [13]. Alternatively, bioelectrical impe-
following hospital discharge. The cause of readmission often dance analysis (BIA) [14] has also been proposed to define a
differs from the original admitting diagnosis [8]. Studies have nutritional state [15,16] based on predictive equations to cal-
found clinical and biochemical indicators that identify culate body composition. However, the applicability of BIA

European Journal of Clinical Investigation Vol 46 609


SILVIO BUSCEMI ET AL. www.ejci-online.com

often is questioned in multimorbid patients, [15,17] particularly performed twice using standardized procedures (Omron M6;
in those with disturbed hydration due to medical illness. Omron Healthcare Co., Matsusaka, Mie, Japan). Height, body
Recently, the use of crude BIA measures such as phase angle weight (SECA; Hamburg, Germany) and body circumferences
(PA) or the vectorial representation of resistance and reactance (nondominant arm and calf circumference) were measured
has received increasing attention as a plausible indicator of with participants lightly dressed and without shoes. Body mass
intra/extracellular hydration and nutritional status [15]. index (BMI) was calculated as body weight (kg)/height2 (m2).
Despite the MNA and PA being possible screening tools for In the case of patients unable to maintain the upright position,
malnutrition, to our knowledge, there are no data available height was obtained using a predictive equation [19] based on
about whether they predict postdischarge mortality in hospi- the leg length measured using a calliper as the distance
talized older adults. We investigated whether these emerging between the heel and the kneecap. Grip strength was measured
nutritional markers predict mortality following discharge in a using a hydraulic hand dynamometer (JAMAR SH5001, Sae-
cohort of hospitalized medical elderly patients. han, Republic of Korea). Patients performed the test while sit-
ting with their shoulder adducted and forearm neutrally
Materials and methods rotated, elbow flexed to 90°, and forearm and wrist in a neutral
position. Patients were instructed to perform a maximal iso-
Participants of this prospective observational cohort study were
metric contraction. The test was repeated within 15–20 s, with
recruited each Monday and Wednesday from June 2010 to May
each hand and the average value (kg) of the three tests was
2011, among patients admitted to the Department of Internal
used for the analysis [20].
Medicine, Cardiovascular and Kidney Diseases of the University
of Palermo, in Italy. Inclusion criteria consisted of subjects aged
Bioimpedance analysis
≥ 60 years and admitted to the hospital from the hospital emer-
Bioelectrical impedance analysis was performed (GR, SM, VM,
gency room in the past 48 h. Exclusion criteria consisted of sub-
AB, NR) as previously described [21,22] using an 800 mA,
jects hospitalized within preceding 30 days; resident of a nursing
50 kHz, tetrapolar impedance plethysmograph (BIA; BIA-103,
home facility; the lack of a unique contact person to allow for
RJL, Detroit, USA/Akern Florence, Italy) to obtain body resis-
future telephone follow-up requests in case a participant expired
tance (R, Ohm), reactance (Xc, Ohm) and PA (PA
or was unable to provide data; lack of a telephone number; low
degrees = arctan (Xc/R)∙(180/p).). Patients were assessed in
levels of patient or caregiver education (illiterate or below pri-
the morning after an overnight fast, in the supine position with
mary school level); or the inability to perform BIA due to con-
arms and legs abducted from the body. Source and sensor
traindications such as pacemaker, metal implants, or amputation
electrodes were placed on the dorsum of both the hand and foot
of limbs. The study was conducted according to the guidelines
of the dominant side of the body.
laid down in the Declaration of Helsinki, and the protocol was
approved by the Institutional Review Boards at the Biomedical
Laboratory analysis
Department of Internal and Specialist Medicine (DIBIMIS) of the
Blood test results were abstracted from the medical record at
University of Palermo and at Dartmouth College. Each partici-
the time of admission. We recorded the following tests: fasting
pant approved and signed an informed consent form.
plasma glucose, cholesterol, triglycerides, high-density
A physician not involved in patient care (GP) abstracted the
lipoprotein (HDL) cholesterol, white blood cells (WBC), hae-
medical record of all participants. All information was obtained
moglobin, albumin. Low-density lipoprotein (LDL) cholesterol
through patient interview directly or, in the event they were
concentration was calculated using the Friedewald’s formula.
unable due to a health condition, a collateral history from a
family member or caregiver was obtained. The MNA was
Follow-up information
administered by GR, SM, VM, AB, NR as described elsewhere
Patients were contacted by telephone at 4-month intervals
[9,18]. A MNA total score of < 17 was indicative of malnutrition
( 1 month) following discharge. A 10- to 15-min telephone
and a score of 17–235 indicative of risk of malnutrition [18].
interview was conducted using a standardized template of
Discharge diagnoses were classified using International Clas-
questions by SM and VM. The interview determined changes in
sification of Diseases-9 codes and classified by the discharging
health status, new episodes of hospitalization, changes in
physician [http://www.who.int/classifications/icd/en
medications, socio-environmental and nutritional conditions.
accessed on 12 October 2013].
Patients or their caregivers were interviewed face to face in the
clinic or assessments performed by telephone. Mortality was
Clinical measurements ascertained by telephone interview by the study assistant who
Systolic blood pressure and diastolic arterial blood pressure obtained information from the family. Mortality data were
were assessed at 5-min intervals in the seated position and additionally verified by linking participants to the Sicilian

610 ª 2016 Stichting European Society for Clinical Investigation Journal Foundation
MORTALITY AND NUTRITIONAL PREDICTORS

regional mortality registry at the Epidemiologic Observatory of Table 1 International Classification of Diseases-9 discharge
the Regional Department of Health (Palermo, Italy); this pro- diagnoses
cedure allowed also to obtain mortality data of participants that ICD-9 codes n %
were lost at telephone contact.
1–139 Infectious and parasitic diseases 2 09

Data analysis 140–239 Neoplasms 19 84


Results are presented as mean  standard deviation or counts 240–279 Endocrine, nutritional and metabolic 28 124
(prevalence). Variables of interest were divided into tertiles of diseases, and immunity
PA (lowest (I) tertile < 46°, middle (II) tertile 46–61° and
280–289 Diseases of the blood and 4 18
highest (III) tertile > 61°) and according to the median value blood-forming organs
(< 22 and ≥ 22) for MNA score. A one-way ANOVA was applied
390–459 Diseases of the circulatory system 72 320
to investigate differences between tertiles and Tukey’s test for
comparison between each couple of tertiles. Student’s unpaired 460–519 Diseases of the respiratory system 42 187
t-test or Pearson chi-square test was applied to evaluate dif- 520–579 Diseases of the digestive system 13 58
ferences between participants who survived and those who
580–629 Diseases of the genitourinary system 38 169
died. The primary outcome was all-cause mortality. We created
Cox-proportional hazard models, general and time modelled 680–709 Diseases of the skin and 2 09
(censoring at 4, 8, 12, 24, 36, 48 months), including the follow- subcutaneous tissue
ing covariates: age, gender, BMI, muscle strength, number of 710–739 Diseases of the musculoskeletal 3 13
comorbidities and total MNA score to identify the impact of PA system and connective tissue
(primary predictor) on death. Laboratory variables were 780–799 Symptoms, signs and 2 09
included in the general model if they were significantly dif- ill-defined conditions
ferent between participants who survived and those who died.
Total 225 1000
There was no collinearity between our two main predictors, PA
and MNA (variance inflation factor = 100). Kaplan–Meier
survival curves were constructed, and outcome differences
100
were evaluated using the log-rank test. Hazard ratios with 95%
confidence intervals were presented. The referent category was 90
Survival probability (%)

lowest tertile of PA and lowest MNA score, respectively. A


80
P-value of < 005 was considered statistically significant. All
statistical analyses were performed using MEDCALC Statistical 70

Software version 1333 (MedCalc Software bvba, Ostend, Bel- 60


HR (CI 95%) for death:

gium; http://www.medcalc.org; 2014). I vs II tertile 3·40 (2·01-5·77);


50 I vs III tertile 3·83 (2·21-6·64)
Reporting of the study conforms to STROBE statement along
with references to STROBE statement and the broader 40
EQUATOR guidelines.
30
0 10 20 30 40
Results Time (months)

Two hundred and twenty-five patients survived to hospital Time (months) 4 12 24 36 48

discharge. We present the cohort’s discharge diagnoses in Deaths (n) 18 35 62 73 88


Table 1. BIA measurements were performed in 192 patients
Phase Angle tertiles - blue: I tertile <4·6°; green: II tertile 4·6°-6·1°; orange: III tertile >6·1°
(853%). Telephone interviews were obtained at 4 months in
Log-rank test: χ2 = 43·6; P< 0·001
225 (100%) patients, in 200 (889%) patients at 12 months, in 162
(720%) patients at 24 months, in 89 (396%) patients at Figure 1 Kaplan–Maier survival probability curves according to
36 months and in 48 (188%) patients at 48 months. Complete the tertile of bioelectrical phase angle in 192 patients aged
mortality data at each time point, as obtained from mortality ≥ 65 years after discharge from Internal Medicine hospital wards.
public registry, are reflected in Figs 1 and 2. Mean survival was
31  15 months (range 1–48), and 90 participants of 225 died in Table 2, including those who died and survived at
(400%) at the end of follow-up (Figs 1 and 2). Demographic 48 months. The prevalence of malnutrition at time of hospital
and clinical characteristics of our included cohort are presented admission using the MNA was 173% (n = 39), while 564%

European Journal of Clinical Investigation Vol 46 611


SILVIO BUSCEMI ET AL. www.ejci-online.com

100 discharge (no = 0; yes = 1). These individuals were examined


HR (CI 95%) for death:
using logistic regression analysis, and we demonstrated that
Low vs. High MNA score
90 PA (P = 002) and MNA scores (P = 0006) were independently
Survival probability (%)

1·85 (1·22-2·81) associated with readmission within 4 months. The OR (95%


80 confidence interval) for readmission was 069 (051–095) for PA
and 086 (078–096) for MNA score.
70

60
Discussion
50 Our data are the first to identify the importance of considering
PA as a mortality predictor following discharge in elderly
40
inpatients. This important finding in a population at risk of
0 10 20 30 40 50 malnutrition provides additional evidence that tools other than
Time (months)
MNA should be considered to identify patients at risk of death
Time (months) 4 12 24 36 48 posthospitalization.
Our data are consistent with other studies demonstrating that
Deaths (n) 18 35 63 74 90 PA is predictive of in-hospital mortality in geriatric patients
[23] or in conditions with persons with multimorbidity,
MNA total score (< median value = blue; ≥ median value = green; median value = 22) including cancer [24–26], haemodialysis [27], human immun-
Log-rank test: χ2 = 8·2; P = 0·004 odeficiency virus infection [28], and amyotrophic lateral scle-
rosis [29]. Our study suggests that PA independently is
Figure 2 Kaplan–Maier survival probability curves according
to the median value of Mini-nutritional Assessment score in associated with mortality after discharge from hospital in
225 patients aged ≥ 65 years after discharge from Internal patients with different clinical conditions suggesting that even
Medicine hospital wards. in complex patients, there may be utility in using this measure
for predictive modelling.
Considering the three groups based on the tertiles of PA
(n = 127) of participants were at risk of malnutrition. Partici- groups (Appendix 1), we did not observe any significant dif-
pants who died were older, had a higher number of offspring, a ference in terms of age, gender and associated comorbidities;
lower hypertension rates and similar rates of coronary heart however, the low PA group exhibited characteristics suggestive
disease, type 2 diabetes and chronic renal failure. Patients who of malnutrition and frailty. In this group, we demonstrated
died had no different discharge diagnoses as compared to those lower body weight, muscle strength and MNA score, lower
alive at follow-up (data not shown). The clinical characteristics blood concentrations of albumin and haemoglobin and higher
of the participants classified according to the tertile of bioelec- WBC concentrations than higher PA groups. Notably, we did
tric phase angle are presented in Appendix 1. The MNA score not measure specific parameters of inflammation (i.e. hs-C-
was significantly correlated with BMI (r = 026; P < 0001). reactive protein, interleukin-6, tumour necrosis factor-a). The
Cox-proportional hazard model demonstrated significant finding of higher WBC concentrations in patients with poorer
relationships for PA, MNA score, age and gender on mortality, PA value may likely reflect a general tendency towards
while BMI, number of comorbidities, muscle strength, serum inflammation that has been associated with both increased risk
concentrations of haemoglobin and albumin had no significant of mortality [30,31] and malnutrition/frailty condition in the
effect (Table 3). Censoring participants at each time of follow- elderly hospitalized patient [32,33]. The value of using PA in
up resulted in different time models for death (Table 4). Age highlighting both individual clinical and nutritional conditions
and sex-specific interactions were tested in each model and may be explained using the BIA theory [34]. PA is inversely
were not significant (data not shown). In particular, only PA related with the extracellular/intracellular water ratio (ECW/
resulted significantly in associations with death at each study ICW); therefore, a low PA value is in consequence of high
time point. Figure 1 demonstrates Kaplan–Meier survival ECW/ICW value, a condition that occurs when the absolute or
curves suggesting that patients with the lowest tertile of PA relative amount of ECW is increased [15,35]. An increased
had higher adjusted mortality estimates. Similarly, the survival ECW/ICW value may result from compromised general clini-
curves demonstrated that the median MNA score discrimi- cal conditions due to altered cellular (i.e. membrane sodium/
nated survival probability (Fig. 2). potassium pumps) functioning as well as from altered nutri-
Of participants with both PA and MNA scores available tional states characterized by loss of body cell mass and the
(n = 192), 25 (13%) had a readmission within 4 months after consequent loss of ICW. Impaired clinical or nutritional

612 ª 2016 Stichting European Society for Clinical Investigation Journal Foundation
MORTALITY AND NUTRITIONAL PREDICTORS

Table 2 Baseline characteristics of patients aged ≥ 65 years after discharge from hospital
Participants
All (N = 225) Alive (N = 135) Dead (N = 90) P*

Age (years) 74  8 72  8 77  8 < 0001


Gender, male sex (n, %) 165 (733) 95 (704) 70 (778) < 005
Follow-up (months) 31  15 39  10 18  12 < 0001
Offspring (n) 29  18 26  16 35  23 0002
Smoking
Current smoker (n, %) 22 (98) 14 (104) 8 (89) 089
Cigarettes (n/day) 14  47 14  48 14  48 096
Never smoker (n, %) 81 (360) 46 (341) 35 (389) 054
Comorbidity
Hypertension (%) 147 (653) 105 (778) 42 (467) < 0001
Type 2 diabetes (%) 89 (396) 57 (422) 32 (356) 070
Coronary heart disease (%) 102 (453) 62 (459) 40 (444) 060
Chronic renal failure (%) 69 (307) 41 (304) 28 (311) 051
Body weight (kg) 748  177 768  186 711  153 002
Body mass index (kg/m ) 2
278  57 287  62 263  45 < 0001
Body circumferences
Arm (cm) 260  50 267  47 248  52 0008
Calf (cm) 325  42 333  43 312  37 < 0001
Bioelectrical characteristics (n = 192)
Resistance (Ohm) 539  106 539  95 539  123 099
Reactance (Ohm) 54  26 56  23 51  30 029
Phase angle 55  19 59  18 48  20 003
Handgrip test (kg) 222  86 236  84 198  85 002
MNA (total score) 21  4 22  4 20  4 < 0001
Laboratory parameters
Glucose (mg/dL) 121  61 119  61 124  62 063
Total cholesterol (mg/dL) 160  46 163  44 155  50 033
HDL cholesterol (mg/dL) 43  17 43  16 42  19 071
Triglycerides (mg/dL) 124  63 129  66 116  58 017
LDL cholesterol (mg/dL) 91  33 94  35 85  28 012
Haemoglobin (g/dL) 120  23 123  22 109  21 < 0001
White blood cells (cells/mm 10 )
3 3
8589  4941 8302  5005 9547  4643 011
Albumin (g/dL) 35  07 36  07 32  07 < 0001
HDL, high-density lipoprotein; LDL, low-density lipoprotein; MNA, Mini-nutritional Assessment (score: < 17 = malnutrition; 17–235 = risk of malnutrition).
Data are: mean  SD or prevalence.
Participants alive and dead at follow-up assessment.
Handgrip test represents mean value of both hands.
*Unpaired Student’s t-test or Pearson chi-square test when appropriate.

European Journal of Clinical Investigation Vol 46 613


SILVIO BUSCEMI ET AL. www.ejci-online.com

Table 3 General-modelled Cox-proportional hazard for likely is a nonspecific measure suggestive of impaired home-
mortality in 192 patients aged ≥ 65 years after discharge from ostasis, a characteristic observed in frailty. Future study
Internal Medicine hospital wards should determine whether PA impacts shorter-term function
HR 95% CI and recovery from the negative effects of hospitalizations, but
also investigate the impact on serological inflammatory
Phase angle 078 064–095
biomarkers such as C-reactive protein, interleukin-6 and
MNA 095 090–099 tumour necrosis factor-a.
Age 104 101–107 Our results also paralleled those observed by others noting
that low MNA scores predict poor outcomes in geriatric hos-
Gender* 042 024–074
pitalized patients [37]. While this was not surprising, the fact
BMI 098 094–103 that the relationship was not modified by PA at 48 months
Muscle strength †
098 094–102 suggests that both could potentially be biomarkers for death in
‡ this at-risk population, at least in the long run. Surprisingly, we
Comorbidities 099 083–117
did not observe any impact of grip strength on mortality. One
Serum concentrations of possible explanation is there may be an interplay between
Haemoglobin 090 082–103 nutritional status and grip strength and that MNA score or PA
led to its nonsignificance. This is purely hypothetical, and we
Albumin 082 058–115
suggest further studies to reproduce these results.
HR, hazard ratio; CI, confidence interval; BMI, body mass index; MNA, Adequate data concerning the general prevalence of hospital
Mini-nutritional Assessment. malnutrition in Italy are lacking. As in other reports [38,39],
*Male = 1, female = 2.

Handgrip test.
we found a high prevalence of malnutrition and risk of mal-

Total number of comorbidities: type 2 diabetes, hypertension, coronary nutrition among the nonsurgical elderly patients included in
heart disease, congestive heart failure, chronic obstructive pulmonary dis- this study. Our results are in agreement with a study
ease, chronic renal failure, liver cirrhosis, malignant cancer, dementia.
demonstrating poor outcomes in terms of in-hospital and long-
term mortality in geriatric hospitalized patients with low
conditions may be associated with low PA values and can MNA score [37]. The group of patients who died during fol-
possibly explain our findings that PA may predict mortality low-up exhibited poorer clinical and nutritional characteristics
and that PA is a measure of cell mass, nutritional risk and (Table 2). However, PA was uniquely associated with survival
general health [34]. In fact, BIA is not a direct method for the length probability. In fact, individuals with a PA < 46° at
assessment of body composition and its accuracy as an indi- admission had less chance of survival following discharge.
cator of body composition relies largely on the use of appro- These values closely approximate PA values that other studies
priate regression equations that may not be applicable in [16,23] demonstrated to be critical for survival in similar group
patients with disturbed hydration or altered distribution of of patients.
ECW/ICW. Our results suggest that we can bypass standard Our study also demonstrates that rate of rehospitalization
mathematical equations and use raw parameters to elicit 4 months after discharge was predicted by a low PA. This
hydration and body cell status [15]. Our study is based upon result may be analysed in view of the recently described
posthospitalization mortality that differs from those previously ‘posthospital syndrome’ a condition concerning patients dis-
published that describe in-hospital mortality [6, 7]. Future charged from hospital that have an acute medical problem
studies measuring the PA likely could permit to identify the within the subsequent 30 days necessitating another hospital-
subgroup of malnourished patients with high mortality risk to ization often for conditions different from the initial diagnosis
be included in nutritional intervention trials in order to [8,40–42]. The sample size of the cohort considered in this study
demonstrate the efficacy of treatment of illness-related malnu- was too small to analyse data relative to 30-day rehospitaliza-
trition, a field that is still lacking of adequate evidence [36]. tion rate; however, the results concerning 4-month rehospital-
Our mortality estimates are not trivial and potentially may ization are in agreement with the possibility that PA may also
provide a new line of research. Clinicians currently have be a good candidate to predict 30-day posthospital syndrome.
limited modalities in assessing malnutrition in hospitalized This is a hypothesis that remains to be investigated by specifi-
adults. These results suggest that BIA has improved predictive cally designed trials.
validity over MNA. This is important clinically in that BIA Our analysis has some important limitations that should be
can easily be performed in hospitalized patients, and is less acknowledged. First, BIA was not performed at discharge and
labour-intensive than the MNA. MNA requires trained staff this information would have greatly increased the quality of
spending at least 15 min with patients or caregivers. Low PA information. We relied on BIA measurement during the

614 ª 2016 Stichting European Society for Clinical Investigation Journal Foundation
MORTALITY AND NUTRITIONAL PREDICTORS

109 (079–150) hospital stay and hence factors that could impact body com-
123 (093–161)
116 (091–146)
096 (079–116)
096 (079–116)
096 (081–114)
Comorbidities‡
Table 4 Time-modelled Cox-proportional hazard for mortality in 192 patients aged ≥ 65 years after discharge from Internal Medicine hospital wards

Total number of comorbidities: type 2 diabetes, hypertension, coronary heart disease, congestive heart failure, chronic obstructive pulmonary disease, chronic renal failure, liver
position and fluid shifts could conceivably impact our results. It
remains unclear whether mortality rate was lower in those
patients whose PA improved at discharge. A limitation is the
heterogeneity of the patient population; however, this may be a
result of our real-life study design and likely reflects reliability.
Another limitation of the present study is that the role of
Muscle strength†

101 (093–111)
099 (092–107)
099 (092–107)
097 (093–101)
097 (093–101)
096 (092–100)
comorbidities could not be investigated as the number of cases
included was rather limited to allow an adequate analysis of
the effect of comorbidity. We attempted to overcome this lim-
itation by including the number of comorbidities in the
regression analysis which was not significant. While we had
complete mortality ascertainment, future study with adequate
099 (088–112)
101 (093–112)
099 (092–107)
098 (093–103)
098 (093–103)
099 (095–104)

deaths can allow for such an examination.


In conclusion, both malnutrition and risk of malnutrition are
important clinical aspects in hospitalized elderly patients that
should be promptly recognized. MNA and BIA-derived phase
BMI

angle are reasonable tools to identify patients at high mortality


risk and may represent useful markers in intervention trials in
this high-risk subgroup.
086 (027–278)
049 (016–147)
067 (029–156)
054 (029–101)
054 (029–101)
041 (024–068)

Acknowledgments
Gender*

We are gratefully indebted with Professor Antonio Craxi


HR, hazard ratio; CI, confidence interval; BMI, body mass index; MNA, Mini-nutritional Assessment.

(University of Palermo, Italy) for logistic support and very


stimulating comments during manuscript preparation.
105 (098–113)
104 (099–110)
105 (101–111)
106 (103–110)
106 (103–110)
102 (100–105)

Funding sources
This research was supported in part by the no profit Associ-
azione Onlus Nutrizione e Salute, Palermo, Italy.
Age

Conflict of interest statement


None to disclose.
089 (078–103)
092 (082–103)
095 (087–104)
096 (090–102)
096 (090–102)
092 (087–097)

Address
Dipartimento Biomedico di Medicina Interna e Specialistica
MNA

(DIBIMIS), Laboratorio di Metabolismo e Nutrizione Clinica,


Policlinico P. Giaccone, University of Palermo, Via del vespro
129, 90127 Palermo, Italy (S. Buscemi, G. Parrinello, G. Rosafio,
034 (022–062)
046 (030–069)
049 (035–069)
077 (062–097)
077 (062–097)
084 (069–099)

V. Sciascia, S. Mendola, A. M. Barile, V. Maniaci, N. Rini, G.


Phase angle
HR (95% CI)

Caimi); Section of General Internal Medicine at Dartmouth,


cirrhosis, malignant cancer, dementia.

Geisel School of Medicine at Dartmouth, The Dartmouth


Institute for Health Policy & Clinical Practice, Lebanon, NH
03756, USA (J. A. Batsis); Dipartimento di Scienze per la Pro-
mozione della Salute e Materno Infantile, Policlinico P. Giac-
Model 3 (12 months)
Model 4 (24 months)
Model 5 (36 months)
Model 6 (48 months)

cone, University of Palermo, Via del vespro 129, 90127 Palermo,


Model 1 (4 months)
Model 2 (8 months)

*Male = 1, female = 2.

Italy (F. M. Massenti); Servizio di Ingegneria Clinica, Policlinico


‘P. Giaccone’, Via del vespro 129, 90127 Palermo, Italy (F.
Handgrip test.

Costa); Dipartimento Attivit a Sanitarie ed Osservatorio Epi-


demiologico, Regione Siciliana, Via del vespro 129, 90127
Palermo, Italy (S. Pollina Addario).

European Journal of Clinical Investigation Vol 46 615


SILVIO BUSCEMI ET AL. www.ejci-online.com

Correspondence to: Silvio Buscemi, Dipartimento Biomedico di 17 Montagnani M, Montomoli M, Mulinari M, Guzzo G, Scopetani N,
Medicina Interna e Specialistica (DIBIMIS), Laboratorio di Gennari C. Relevance of hydration state of the fat free mass in
estimating fat mass by body impedance analysis. Appl Radiat Isot
Metabolismo e Nutrizione Clinica, Policlinico P. Giaccone, Via
1998;49:499–500.
del Vespro 129, 90127 Palermo, Italy. Tel.:+39-91-6554580; fax: 18 Vellas B, Guigoz Y, Garry PJ, Nourhashemi F, Bennahum D, Lauque
+39-91-6554580; e-mail: silbus@tin.it S et al. The Mini Nutritional Assessment (MNA) and its use in
grading the nutritional state of elderly patients. Nutrition
Received 16 December 2015; accepted 22 April 2016 1999;15:116–22.
19 Chumlea WC, Roche AF, Steinbaugh ML. Estimating stature from
knee height for persons 60 to 90 years of age. J Am Geriatr Soc
References 1985;33:116–20.
1 Council of Europe, Committee of Ministers. Resolution ReAP (2003) 3 20 Gill D, Reddon J, Renny C, Stefanyk W. Hand dynamometer: effects
on Food and Nutritional Care in Hospitals. Strasbourg, France: Council of trials and session. Percept Mot Skills 1985;61:195–8.
of Europe, 2003. 21 Buscemi S, Blunda G, Maneri R, Verga S. Bioelectrical characteristics
2 Pablo AM, Izaga MA, Alday LA. Assessment of nutritional status on of type 1 and type 2 diabetic subjects with reference to body water
hospital admission: nutritional scores. Eur J Clin Nutr 2003;57:824– compartments. Acta Diabetol 1998;35:220–3.
31. 22 Piccoli A, Nigrelli S, Caberlotto A, Bottazzo S, Rossi B, Pillon L et al.
3 Lucchin L, D’Amicis A, Gentile MG, Battistini NC, Fusco MA, Palmo Bivariate normal values of the bioelectrical impedance vector in
A et al. A nationally representative survey of hospital malnutrition: adult and elderly populations. Am J Clin Nutr 1995;61:269–70.
the Italian PIMAI (Project: Iatrogenic MAlnutrition in Italy) study. 23 Wirth R, Volkert D, R€ osler A, Sieber CC, Bauer JM. Bioelectric
Med J Nutrition Metab 2009;2:171–9. impedance phase angle is associated with hospital mortality of
4 Lainscak M, Farkas J, Frantal S, Singer P, Bauer P, Hiesmayr M et al. geriatric patients. Arch Gerontol Geriatr 2010;51:290–4.
Self-rated health, nutritional intake and mortality in adult 24 Gupta D, Lammersfeld CA, Vashi PG, King J, Dahlk SL, Grutsch JF
hospitalized patients. Eur J Clin Invest 2014;44:813–24. et al. Bioelectrical impedance phase angle as a prognostic indicator
5 Asiimwe SB, Muzoora C, Wilson LA, Moore CC. Bedside measures in breast cancer. BMC Cancer 2008;8:249.
of malnutrition and association with mortality in hospitalized 25 Gupta D, Lis CG, Dahlk SL, King J, Vashi PG, Grutsch JF et al. The
adults. Clin Nutr 2015;34:252–6. relationship between bioelectrical impedance phase angle and
6 Bouillanne O, Morineau G, Dupont C, Coulombel I, Vincent JP, subjective global assessment in advanced colorectal cancer. Nutr J
Nicolis I et al. Geriatric Nutritional Risk Index: a new index for 2008;7:19.
evaluating at-risk elderly medical patients. Am J Clin Nutr 26 Gupta D, Lammersfeld CA, Vashi PG, King J, Dahlk SL, Grutsch JF
2005;82:777–83. et al. Bioelectrical impedance phase angle in clinical practice:
7 Correia MI, Waitzberg DL. The impact of malnutrition on morbidity, implications for prognosis in stage III B and IV non-small cell lung
mortality, length of hospital stay and costs evaluated through a cancer. BMC Cancer 2009;9:37.
multivariate model analysis. Clin Nutr 2003;22:235–9. 27 Maggiore Q, Nigrelli S, Ciccarelli C, Grimaldi C, Rossi GA,
8 Krumholz HM. Post-hospital syndrome - An acquired, transient Michelassi C. Nutritional and prognostic correlates of bioimpedance
condition of generalized risk. N Engl J Med 2013;368:100–2. indexes in hemodialysis patients. Kidney Int 1996;50:2103–8.
9 Kondrup J, Allison SP, Elia M, Vella B, Plauth M. ESPEN guidelines 28 Ott M, Fischer H, Polat H, Helm EB, Frenz M, Caspary WF et al.
for nutrition screening 2002. Clin Nutr 2003;22:415–21. Bioelectrical impedance analysis as a predictor of survival in
10 Nivet-Antoine V, Golmard JL, Coussieu C, Piette F, Cynober L, patients with human immunodeficiency virus infection. J Acquir
Bouillanne O. Leptin is better than any other biological parameter Immune Defic Syndr Hum Retrovirol 1995;9:20–5.
for monitoring the efficacy of renutrition in hospitalized 29 Desport JC, Marin B, Funalot B, Preux PM, Couratier P. Phase angle
malnourished elderly patients. Clin Endocrinol 2011;75:315–20. is a prognostic factor for survival in amyotrophic lateral sclerosis.
11 Mueller C, Compher C, Ellen DM, ASPEN Board of Directors. Amyotroph Lateral Scler Frontotemporal Degener 2008;9:273–8.
ASPEN clinical guidelines. Nutrition screening, assessment and 30 Weijenberg MP, Feskens EJ, Kromhout D. White blood cell count
intervention in adults. J Parenter Enteral Nutr 2011;35:16–24. and the risk of coronary heart disease and all-cause mortality in
12 Guigoz Y, Vellas B, Garry PJ. Assessing the nutritional status of the elderly men. Arterioscler Thromb Vasc Biol 1996;16:499–503.
elderly: the Mini Nutritional Assessment as part of the geriatric 31 Larsson S, Nordenson A, Glader P, Yoshihara S, Linden A, Slinde
evaluation. Nutr Rev 1996;54(1 Pt 2):S59–65. F. A gender difference in circulating neutrophils in malnourished
13 Bauer JM. The MNA in 2013 – still going stronger after almost patients with COPD. Int J Chron Obstruct Pulmon Dis 2011;6:
twenty years. J Nutr Health Aging 2013;17:288–9. 83–8.
14 Piccoli A. Identification of operational clues to dry weight 32 Fernandez-Garrido J, Navarro-Martınez R, Buigues-Gonzalez C,
prescription in hemodialysis using bioimpedance vector analysis. Martınez-Martınez M, Ruiz-Ros V, Cauli O. The value of neutrophil
Kidney Int 1998;53:1036–43. and lymphocyte count in frail older women. Exp Gerontol
15 Norman K, Stob€ aus N, Pirlich M, Bosy-Westphal A. Bioelectrical 2014;54:35–41.
phase angle and impedance vector analysis – clinical relevance 33 Fontana L, Addante F, Copetti M, Paroni G, Fontana A, Sancarlo D
and applicability of impedance parameters. Clin Nutr 2012;31: et al. Identification of a metabolic signature for multidimensional
854–61. impairment and mortality risk in hospitalized older patients. Aging
16 Oliveira CM, Kubrusly M, Mota RS, Silva CA, Choukroun G, Cell 2013;12:459–66.
Oliveira VN. The phase angle and mass body cell as markers of 34 Baumgartner RN, Chumlea WC, Roche AF. Bioelectric
nutritional status in hemodialysis patients. J Ren Nutr 2010;20:314– impedance phase angle and body composition. Am J Clin Nutr
20. 1988;48:16–23.

616 ª 2016 Stichting European Society for Clinical Investigation Journal Foundation
MORTALITY AND NUTRITIONAL PREDICTORS

35 Barbosa-Silva MC, Barros AJ. Bioelectrical impedance analysis in 39 Kagansky N, Berner Y, Koren-Morag N, Perelman L, Knobler
clinical practice: a new perspective on its use beyond body H, Levy S. Poor nutritional habits are predictors of poor
composition equations. Curr Opin Clin Nutr Metab Care 2005;8: outcome in very old hospitalized patients. Am J Clin Nutr
311–7. 2005;82:784–91.
36 Baldwin C, Weekes CE. Dietary advice for illness-related 40 Krumholz HM. Reducing the trauma of hospitalization. JAMA
malnutrition in adults. Cochrane Database Syst Rev 2008;1: CD002008. 2014;311:2169–70.
37 Cereda E, Lucchin L, Pedrolli C, D’Amicis A, Gentile MG, Battistini 41 Sadatsafavi M, Lynd LD, FitzGerald JM. Post-hospital syndrome in
NC et al. Nutritional care routines in Italy: results from the PIMAI adults with asthma: a case-crossover study. Allergy Asthma Clin
(Project: Iatrogenic MAlnutrition in Italy) study. Eur J Clin Nutr Immunol 2013;9:49.
2010;64:894–8. 42 Muscaritoli M, Molfino A. Malnutrition: the hidden killer in
38 Norman K, Pichard C, Lochs H, Pirlich M. Prognostic impact of healthcare systems. BMJ 2013;346:f1547.
disease-related malnutrition. Clin Nutr 2008;27:5–15.

Appendix 1 Anthropometric, demographic and clinical characteristics of the participants classified according to the tertile of bioelectric phase angle

Phase angle tertile


I (N = 61) II (N = 68) III (N = 63) P†

Age (year) 75  9 75  7 73  8 0.14


Gender, male sex (n, %) 37 (60.6) 45 (66.2) 48 (76.2) 0.18
Offspring (n) 3.3  2.0 2.9  1.8 3.1  1.9 0.72
Smoking
Current smoker (n, %) 1 (0.02) 7 (10.3) 6 (9.5) 0.20
Cigarettes (n/day) 0.2  1.3 1.3  4.8 1.6  5.3 0.19
Never smoker (n, %) 30 (49.2) 27 (39.7) 24 (38.1) 0.32
Prevalence of
Hypertension (%) 37 (60.7) 48 (70.6) 37 (58.7) 0.44
Duration of hypertension (year) 9.6  15.6 8.3  11.9 7.0  10.0 0.81
Type 2 diabetes (%) 22 (36.1) 22 (32.4) 22 (34.9) 0.90
Duration of type 2 diabetes (year) 2.6  6.6 3.8  7.6 4.1  8.5 0.81
Coronary heart disease (%) 24 (39.3) 29 (42.6) 19 (30.2) 0.59
Duration of coronary heart disease (year) 0.0  0.0 0.8  4.0 0.1  0.4 0.46
Chronic renal failure (%) 21 (34.4) 16 (23.5) 16 (25.4) 0.51
Duration of chronic renal failure (year) 0.2  0.5 1.2  4.4 0.9  2.5 0.56
Body weight (kg) 70.7  15.4 75.2  15.5 79.7  21.2 0.05
BMI (kg/m )2
27.1  5.1 28.3  5.5 29.4  6.1 0.14
Laboratory parameters
Glucose (mg/dL) 129  53 112  42 111  52 0.17
Total cholesterol (mg/dL) 155  48 162  51 162  42 0.72
HDL cholesterol (mg/dL) 43  18 42  17 47  16 0.36
Triglycerides (mg/dL) 132  73 125  69 112  54 0.43
LDL cholesterol (mg/dL) 81  32 94  35 95  37 0.26
Bioelectrical characteristics

European Journal of Clinical Investigation Vol 46 617


SILVIO BUSCEMI ET AL. www.ejci-online.com

Appendix 1 Continued
Phase angle tertile
I (N = 61) II (N = 68) III (N = 63) P†

Resistance (Ohm) 541  116 534  97 542  93 0.92


Reactance (Ohm) 35  10 50  10* 77  29* ** ,
< 0.001
Phase angle 3.6  0.7 5.3  0.5* 8.1  2.4* ** ,
< 0.001
Handgrip test
Average (kg) 15  8 23  10*** 21  7 0.01
Mini-nutritional Assessment (score)
Total valuation 20  4 22  4* 23  4 0.002
BMI, body mass index; MNA, Mini-nutritional Assessment.
Data are: mean  SD or prevalence.

ANOVA or Pearson chi-square test when appropriate.
Tukey’s test:
*P < 0.001 vs. phase angle tertile I; **P < 0.001 vs. phase angle tertile II; ***P < 0.001 vs. phase angle tertile I.

618 ª 2016 Stichting European Society for Clinical Investigation Journal Foundation
Copyright of European Journal of Clinical Investigation is the property of Wiley-Blackwell
and its content may not be copied or emailed to multiple sites or posted to a listserv without
the copyright holder's express written permission. However, users may print, download, or
email articles for individual use.

Das könnte Ihnen auch gefallen