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Journal of the American College of Nutrition

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Calf Circumference Is a Good Predictor of Longer


Hospital Stay and Nutritional Risk in Emergency
Patients: A Prospective Cohort Study

Micheli Tarnowski, Elana Stein, Aline Marcadenti, Jaqueline Fink, Estela


Rabito & Flávia Moraes Silva

To cite this article: Micheli Tarnowski, Elana Stein, Aline Marcadenti, Jaqueline Fink, Estela
Rabito & Flávia Moraes Silva (2020): Calf Circumference Is a Good Predictor of Longer Hospital
Stay and Nutritional Risk in Emergency Patients: A Prospective Cohort Study, Journal of the
American College of Nutrition, DOI: 10.1080/07315724.2020.1723452

To link to this article: https://doi.org/10.1080/07315724.2020.1723452

Published online: 21 Feb 2020.

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JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION
https://doi.org/10.1080/07315724.2020.1723452

Calf Circumference Is a Good Predictor of Longer Hospital Stay and Nutritional


Risk in Emergency Patients: A Prospective Cohort Study
Micheli Tarnowskia, Elana Steina, Aline Marcadentib,c,d, Jaqueline Finke, Estela Rabitof, and Flavia Moraes Silvag
a
Department of Nutrition Science, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil; bInstitute of Research
of the Heart Hospital (IP-HCor), S~ao Paulo, Brazil; cPostgraduate Program in Health Sciences: Cardiology, Institute of Cardiology/University
Foundation of Cardiology (IC/FUC), Porto Alegre, Brazil; dPostgraduate Program in Nutrition Sciences, Federal University of Health Sciences
of Porto Alegre (UFCSPA), Porto Alegre, Brazil; eDivision of Nutrition, Dietetics of Nossa Senhora da Conceiç~ao Hospital, Porto Alegre, Brazil;
f
Department of Nutrition, Postgraduate Program in Food and Nutrition, Federal University of Parana, Curitiba, Brazil; gDepartment of
Nutrition, Postgraduate Program in Nutrition, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Brazil

ABSTRACT ARTICLE HISTORY


Objective: This study aimed to evaluate the validity of calf circumference (CC) in identifying mal- Received 24 October 2019
nourished patients and patients at nutritional risk and determine the association between CC and Accepted 23 January 2020
clinical outcomes of hospitalized patients.
KEYWORDS
Methods: A prospective cohort study was conducted involving patients admitted to the emer-
Calf circumference;
gency department of a tertiary hospital in the first 48 hours of admission. Nutritional risk was nutritional assessment;
determined using Nutritional Risk Screening, malnutrition was diagnosed using subjective global mortality; length of
assessment, and CC was manually measured. Brazilian cutoff points for CC were used to identify hospital stay
low muscle mass. The outcomes of interest were length of emergency care and hospital stay,
occurrence of infection, and death, besides nutritional risk and malnutrition.
Results: In total, 528 patients (52.76 ± 16.18 years; 54.6% females) were followed up for 9.0
(3.0–19.0) days; 39.6% of them had reduced CC values. The accuracy of CC in identifying patients
at nutritional risk and malnourished patients was 67.7% and 54.1%, respectively. The cutoff value
of 36.5 cm was highly accurate in identifying nutritional risk [AUC-ROC curve ¼ 0.764 (95% CI:
0.704–0.825) for men, and AUC-ROC curve ¼ 0.716 (95% CI: 0.659–0.774) for women]. Patients
with low CC had a 1.59-fold (95% CI: 1.07–2.36) greater likelihood of a long hospital stay than
patients with normal CC.
Conclusions: Low CC values have satisfactory validity in identifying nutritional risk and are associ-
ated with long hospital stay.

Introduction cutoff point of 33 cm for women and 34 cm for


Malnutrition is prevalent in hospitalized patients, at a rate men (13).
of 20%–50% (1), depending on the patient’s country of resi- Some studies have shown that CC can be an accurate
dence and clinical condition (2). Malnutrition has been asso- predictor of muscle mass loss (14), sarcopenia (15), nutri-
ciated with a long hospital stay, high risk of infection, high tional risk (16), low disability (17), death (18–20), and hos-
rate of hospital readmission, and high hospital costs (3–6). pital readmission (21). A study involving 108 consecutive
Malnutrition is characterized by changes in body compos- patients with esophageal and gastric cancer showed that low
ition, including loss of lean mass (7) due to the release of CC was associated with low skeletal muscle mass index (22).
cytokines and poor immunity (8), with consequent reduc- Most previous studies involved elderly outpatients using dif-
tion in the ability to perform basic functional activities (9). ferent cutoff points to define loss of muscle mass. A pro-
Therefore, in clinical practice, determining muscle mass spective longitudinal study involving the Brazilian
is important to correctly diagnose malnutrition. In this population, using cutoff values, showed that patients with
regard, calf circumference (CC) is a simple, noninvasive, low CC had a 3.89-fold higher risk of hospital readmission
and cheap measurement (10) that reflects body muscle mass in 30 days (21). To the best of our knowledge, there is no
(11). The performance of CC as a predictor of lean mass study on the performance of the Brazilian cutoff point for
loss depends on the cutoff point, which varies among popu- CC in predicting malnutrition, length of hospital stay, and
lations. In a study involving French women aged 70 years or death in hospitalized patients. Therefore, the aim of this
above, the value of 31 cm was defined as a cutoff point for study was to determine the association between low CC and
identification of lean mass loss (12). A study conducted in nutritional risk, malnutrition, and poor clinical outcomes
the South of Brazil involving elderly individuals defined a (long duration of emergency care and hospital stay,

CONTACT Flavia Moraes Silva flaviams@ufcspa.edu.br Departamento de Nutriç~ao, Universidade Federal de Ci^encias da Sa
ude de Porto Alegre, Rua
Sarmento Leite, 245, Centro Hist
orico, Porto Alegre, RS 90050-170, Brazil
ß 2020 American College of Nutrition
2 M. TARNOWSKI ET AL.

occurrence of infection, and death) in patients admitted to performed to evaluate the association between low CC and
the emergency department of a public hospital. length of hospital stay, and Cox regression was performed
to evaluate the association between low CC and death. Age
and metabolic demand of the disease were considered con-
Materials/subjects and methods founders, and the analysis was adjusted for these variables.
This was a prospective cohort study involving patients
admitted to the emergency department of a tertiary public
Results
hospital in Porto Alegre (Rio Grande do Sul, Brazil) that
aimed to compare the predictive and concurrent validity of A total of 752 patients were considered eligible, but 224
different screening nutritional tools. Three trained clinical (29%) of them were not included in the analysis because
dietitians performed data collection between September 2013 they had edema in lower limbs, limiting the measurement of
and January 2015. The Ethics Committee of the hospital the CC. Therefore, the current study included 528 patients
approved the study protocol (approval number 360.639), aged 52.76 ± 16.18 years. Most of them self-reported as white
and all patients granted written informed consent. This (85.4%), and half of the study population comprised women
research was conducted according to the guidelines of the (54.6%). The most common reasons for hospitalization were
Declaration of Helsinki and Brazilian regulations on ethical gastroenterological disorders (21.0%), cancer and related
issues in research involving human subjects. The protocol complications (18.6%), cardiac diseases (11.8%), and neuro-
has been described previously (23). logic diseases (9.0%); 42.9% of the patients had a disease
Briefly, the participants were consecutively selected from resulting in high metabolic demand.
among the patients admitted to the emergency department Those not included in the analysis were significantly
during the study period, namely patients aged >18 years, younger those included (55.88 ± 13.35 versus
who were conscious and able to move. Data were collected 52.76 ± 16.18 years, respectively). Gender, frequency of mal-
within 48 hours of hospitalization. Sociodemographic data nutrition diagnosis, length emergency care and hospital stay,
including gender, age, and ethnicity were collected. Hospital frequency of infection, and death rate did not differ between
admission date, reason for admission, and medical history the groups (p > 0.05 for all analyses [data not shown]).
were obtained from electronic medical records. Nutritional The length of emergency care was 3.0 (2.0–5.0) days and
risk screening was performed with the Nutritional Risk hospital stay was 9.0 (3.0–19.0) days. The death rate was
Screening (NRS-2002) tool and patients were classified as at 3.9%. Occurrence of infection was reported in the medical
nutritional risk or not at nutritional risk (24). The subjective records of 32.5% of the study sample.
global assessment (SGA) was used for nutritional diagnosis, The mean values of current weight and body mass index
and patients were classified as well nourished, moderately (BMI) of the patients were 70.92 ± 16.75 kg and
malnourished, or severely malnourished, as proposed by 27.29 ± 5.93 kg/m2, respectively. The mean CC was
Detsky et al. The metabolic demand of a disease was classi- 36.71 ± 12.85 cm for men and 35.74 ± 5.34 cm for women
fied as mild, moderate, or severe (25). Anthropometric (p ¼ 0.205). About 30.0% of the patients were at nutritional
measurements, i.e., height, weight, and CC, were manually risk according to the NRS-2002. According to the SGA,
recorded, with patients instructed to wear as little clothing 65.9% of the patients were classified as well nourished,
as possible and no shoes. The CC was measured using an 24.8% of patients, as moderately malnourished, and 9.4%, as
inelastic tape at the point of the greatest CC in patients severely malnourished. Considering the cutoff points of CC
without edema. for both genders, 39.6% of the patients had low CC values.
In the current study, only the data of patients whose CC The frequency of low CC values was higher in patients at
measures were available were analyzed. CC values equal to nutritional risk than in those who were not at nutritional
or below the cutoff points of 34 cm for men and 33 cm for risk (64.9% vs. 29.6%, respectively, p < 0.001). The area
women were defined as low CC (13). The clinical outcomes under the ROC curve regarding the performance of CC in
of interest were length of emergency care and hospital stay, identifying patients at nutritional risk was 0.677 (95% CI:
occurrence of infection registered in the medical records, 0.626–0.728; p < 0.001), with 64.9% sensitivity and 70.4%
and death. We also reported as outcomes the presence of specificity. When CC was considered a continuous variable
nutritional risk and malnutrition. in the ROC curve, the area under the ROC curve improved
Data analysis was performed using the SPSS software, for both men (area under the ROC curve ¼ 0.764; 95% CI:
and p values <0.05 were considered significant. Quantitative 0.704–0.825) and women (area under the ROC curve ¼
variables were expressed as mean and standard deviation or 0.716; 95% CI: 0.659–0.774). For a high sensitivity and
median and interquartile range, and categorical variables acceptable specificity (>50%), the cutoff point of CC should
were expressed as absolute and relative frequencies. be 36.5 cm both for men (sensitivity ¼ 79.8%; specificity ¼
Student’s t-test, Mann–Whitney U test, or Chi-square test 52.8%) and for women (sensitivity ¼ 77%; specificity
was performed to compare the outcomes/features of patients ¼ 53.9%).
with low and normal CC. The area under the ROC curve The frequency of low CC values was higher in malnour-
was calculated to evaluate the performance of CC in identi- ished patients than in well-nourished patients, but it did not
fying malnutrition, considering the Brazilian cutoff points, reach statistical significance (45.3% vs. 37.2%, respectively;
with CC as a continuous variable. Logistic regression was p ¼ 0.070). The performance of CC in identifying
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION 3

Table 1. Features of Patients According to Calf Circumference Classification. Table 2. Multivariate Analysis of the Association between Calf Circumference
Low CC Normal CC and Clinical Outcomes.
Feature (n ¼ 209) (n ¼ 319) p value Longer hospital stay (>16 days)
Age (years) 55.37 ± 17.15 50.87 ± 15.28 0.0021 OR (95% CI)1 p value
BMI (kg/m2) 30.96 ± 5.63 22.78 ± 3.87 <0.0011 Low CC (crude) 1.65 (1.11–2.43) 0.012
Nutritional risk (NRS-2002) 48.8% 17.5% <0.0012 Low CC (adjusted) 1.59 (1.07–2.36) 0.023
Malnutrition (SGA) 39.7% 32.3% 0.0612 Mortality
Metabolic demand of disease
Low 11.1% 10.8% HR (95% CI)2 p value
Moderate 37.0% 52.2% 0.0022 Low CC (crude) 2.16 (0.82–5.73) 0.121
High 51.9% 37.0% Low CC (adjusted) 2.02 (0.76–5.36) 0.160
Emergency department LOS 3.0 (2.0–5.0) 3.0 (2.0–4.25) 0.8373 Abbreviations: CC ¼ calf circumference, OR ¼ odds ratio, HR ¼ hazard ratio.
Hospital LOS 10.0 (4.0–21.0) 7.0 (3.0–16.0) 0.0083 1
Logistic regression.
Longest hospital stay (16 days) 34.4% 26.6% 0.0102 2
Cox regression.
Occurrence of infection 34.0% 31.9% 0.6352 Adjusted for age and stress of disease.
Death 6.2% 2.2% 0.0332
Abbreviations: CC ¼ calf circumference, BMI ¼ body mass index, NRS-
2002 ¼ nutritional risk screening, SGA ¼ subjective global assessment, specificity of 71.4% for a CC of <32.5 cm in identifying a
LOS ¼ length of stay. high score of NRS-2002 (16). However, the applicability of
1
Student’s t-test.
2
Chi-square test. CC in clinical practice is questionable since it requires an
3

Mann–Whitney U test. accuracy of at least 75%, which was probably was not
CC < 34 cm for men and < 33 cm for women. reached because CC reflects only the muscle mass (26) and
does not take into account other aspects related to nutri-
malnourished patients was not satisfactory because the area tional status (27). It should be further tested in a representa-
under de ROC curve was 0.541 (95% CI: 0.489–0.593; tive sample of hospitalized adults. The use of CC as a
p ¼ 0.125), which did not improve when CC was considered nutritional screening tool could be interesting. In our other
a continuous variable (data not shown). recent study that developed and validated a new screening
Table 1 describes the general and clinical features of tool for identifying the risk of malnutrition among patients
patients according to CC classification. The frequency of in the emergency department (NRE-2017), muscle mass loss,
occurrence of infection did not differ between patients with determined by physical examination, was a predictor of high
normal and low CC values. The frequency long hospital stay NRE-2017 scores (28). This should also be confirmed in
future studies.
was higher among those with low CC values than among
In the present study, low CC values were not able to effi-
those with normal values as was the frequency of death.
ciently identify malnutrition. A study involving 1164
Table 2 presents the strength of the association between CC,
Japanese elderly patients showed a good accuracy of CC in
long hospital stay, and death. The odds of long hospital stay
predicting malnutrition according to the ESPEN diagnostic
were 1.6-fold greater for patients with low CC than for those
criteria for malnutrition in both women (CC ¼ 26.4 cm;
with normal CC. When CC was considered a continuous
AUC ¼ 0.79; 95% CI: 0.76–0.83) and men (CC ¼ 28.3 cm;
variable in the Cox regression adjusted for age and meta-
AUC ¼ 0.83; 95% CI: 0.80–0.87) (14). However, the cutoff
bolic demand, it was inversely associated with the risk of
point used by the authors was lower than that adopted in
death (HR ¼ 0.864; 95% CI: 0.786–0.949; p ¼ 0.002). The
the current study and the reference diagnostic method pro-
analysis was also performed considering the cutoff point of posed by the ESPEN. A previous study stated that the
36.5 cm, but it was not a significant predictor of long hos- ESPEN criteria might not have satisfactory concurrent valid-
pital stay or death (data not shown). ity when considering the SGA as reference method (29).
Malnutrition is a complex condition that involves changes
Discussion in muscle and fat mass, biochemical parameters, food con-
sumption, functional capacity, and inflammation status (30).
The current study evaluated the performance of CC in iden- Although low CC is notably an important factor in the diag-
tifying patients at nutritional risk and malnourished patients nosis of malnutrition, representing a phenotypic criterion
and in predicting clinical outcomes of patients admitted to according to the Global Leadership Initiative on
the emergency department of a public hospital. CC values of Malnutrition group, it needs to be combined with an etio-
<36.5 cm showed satisfactory validity in identifying patients logic criterion, such as reduced food intake or assimilation,
at nutritional risk, but not malnutrition. On the other hand, disease burden, or inflammation, to result in a confirmed
patients with low CC (considering the Brazilian cutoff diagnosis (31). Furthermore, our study involved adults and
points) had higher odds of long hospital stay than patients elderly patients in whom loss of lean mass is a physiological
with normal CC. finding related to aging, and the elderly are expected to have
The low CC values had an accuracy of 67% in identifying lower CC values than adults, which can impact
patients at nutritional risk in the current study, improving the outcomes.
discretely with the cutoff point of 36.5 cm. This performance Several studies have investigated the performance of CC
was similar to that reported in another Brazilian study as a predictor of mortality and survival (18–20, 32–34). In
involving patients with cancer that reported an area under the present study, low CC was not a predictor of death after
the ROC curve of 0.66, with a sensitivity of 62.7% and adjustment for age and disease-related metabolic demand,
4 M. TARNOWSKI ET AL.

probably due to the small number of individuals who died In addition, repeated measurements of CC during hospital-
(it may lack statistical power). In a cohort study involving ization could help determine muscle mass loss and predict
599 Japanese elderly patients with cardiovascular disease, poor outcomes, albeit warranting further studies.
low CC values were associated with short survival time, but
they did not predict mortality in a multivariate analysis (33).
In another cohort study involving 104 non-hospitalized Conclusions
patients with chronic obstructive pulmonary disease Low CC values showed satisfactory validity in identifying
(COPD), low CC (<30 cm) was positively associated with a nutritional risk and were associated with long hospital stay.
4.5-fold increase in mortality. The small number of deaths Further studies should investigate the validity of CC as a
in our study could be explained by the low cutoff point prognostic marker for patients admitted in the emergency
used, age of patients, and severity of disease (68.2% of the department considering the cutoff points applied in
sample had severe COPD) (32). this study.
In the present study, low CC was a good predictor of
long hospital stay, increasing by 1.59 times, the odds of a
hospital stay longer than 16 days – this cutoff point was con- Author contributions
sidered important because a national multicenter study dem- F.M.S., A.M., J.F., E.R. contributed to conception and design of the
onstrated that this period of hospitalization increased the study. F.M.S. and J.F. contributed to acquisition of the data. F.M.S.
odds of being diagnosed with malnutrition (35). On the analyzed the data. M.T., E.S., and F.M.S. interpreted the results and
other hand, in a prospective cohort study involving 733 draft the manuscript. All authors critically revised the manuscript, gave
final approval and agree to be accountable for all aspects of work
Canadian patients, CC was not a significant predictor of ensuring integrity and accuracy.
long hospital stay (OR 0.98, 95% CI; 0.95–1.00) (34). In our
study (36), hospitalization for seven or more days was con-
sidered long hospital stay, which could explain the contrast- Disclosure statement
ing results. Recently, a Brazilian study showed a 3.89-fold The authors declare no conflict of interest.
increase in the risk of hospital readmission in 30 days
among patients with low CC values, using the same cutoff
points that we used in the present study (21). Individuals References
with low CC in our study seemed to be more unwell than 1. Norman K, Pichard C, Lochs H, Pirlich M. Prognostic impact of
those with high CC, requiring more medications and overall disease-related malnutrition. Clin Nutr. 2008;27(1):5–15. doi:10.
care (contributing to prolonged hospitalization but 1016/j.clnu.2007.10.007.
not death). 2. Correia M, Perman MI, Waitzberg DL. Hospital malnutrition in
CC is a noninvasive measurement that is simple and Latin America: a systematic review. Clin Nutr. 2017;36(4):
958–967. doi:10.1016/j.clnu.2016.06.025.
cheap to perform, and it reflects body muscle mass (10, 13). 3. Allard JP, Keller H, Jeejeebhoy KN, Laporte M, Duerksen DR,
However, it cannot be performed in the presence of edema Gramlich L, et al. Malnutrition at hospital admission-contribu-
since it may lead to overestimated measures. In the current tors and effect on length of stay: a prospective cohort study from
study, 29% of the sample had edema and hence were not the Canadian Malnutrition Task Force. JPEN J Parenter Enteral
included in the study. These patients were older than the Nutr. 2016;40(4):487–497. doi:10.1177/0148607114567902.
4. Mendes J, Alves P, Amaral TF. Comparison of nutritional status
patients studied, so our results should be interpreted with
assessment parameters in predicting length of hospital stay in
caution even though we considered age as a confounder in cancer patients. Clin Nutr. 2014;33(3):466–470. doi:10.1016/j.
the multivariate analysis. Furthermore, it is important to clnu.2013.06.016.
reinforce that the cutoff points of CC used in the current 5. Cereda E, Klersy C, Hiesmayr M, Schindler K, Singer P, Laviano
study were established for older people, which may not be A, Caccialanza R, Nutrition Day Survey Collaborators. Body
sufficiently accurate for adults aged 18 years or older. mass index, age and in-hospital mortality: the NutritionDay
multinational survey. Clin Nutr. 2017;36(3):839–847. doi:10.
Further studies are needed to confirm this speculation. A
1016/j.clnu.2016.05.001.
limitation of the current study is that disease severity was 6. Caccialanza R, Klersy C, Cereda E, Cameletti B, Bonoldi A,
assessed using scoring systems, such as Charlson comorbid- Bonardi C, Marinelli M, Dionigi P. Nutritional parameters asso-
ity index. We considered the metabolic demand of the dis- ciated with prolonged hospital stay among adult patients. CMAJ.
ease as an indirect marker of severity, but we recognize the 2010;182(17):1843–1849. doi:10.1503/cmaj.091977.
7. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T,
drawbacks of this method. Therefore, the results of our
Landi F, et al. Sarcopenia: European consensus on definition and
multivariate analysis should be interpreted with caution. diagnosis: report of the European Working Group on Sarcopenia
According to our results, low CC (34 cm for men and in older people. Age Ageing. 2010;39(4):412–423. doi:10.1093/
33 for women) should be considered a predictor of poor ageing/afq034.
outcomes in patients admitted to the emergency department, 8. Okumura S, Kaido T, Hamaguchi Y, Fujimoto Y, Kobayashi A,
since it was associated with long hospital stay, regardless of Iida T, et al. Impact of the preoperative quantity and quality of
skeletal muscle on outcomes after resection of extrahepatic bil-
the patients’ age and metabolic demand. Also, measuring
iary malignancies. Surgery. 2016;159(3):821–833. doi:10.1016/j.
CC could be an easy and cheap way to identify nutritional surg.2015.08.047.
risk during hospital admission. These results need to be con- 9. Sun Y-S, Kao T-W, Chang Y-W, Fang W-H, Wang C-C, Wu L-
firmed with further studies involving hospitalized patients. W, Yang H-F, Liaw F-Y, Chen W-L. Calf circumference as a
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION 5

novel tool for risk of disability of the elderly population. Sci Rep. 23. Rabito EI, Marcadenti A, Fink JS, Figueira L, Silva FM.
2017;7(1):16359. doi:10.1038/s41598-017-16347-9. Nutritional Risk Screening 2002, Short Nutritional Assessment
10. Kim S, Kim M, Lee Y, Kim BS, Yoon TY, Won CW. Calf cir- Questionnaire, Malnutrition Screening Tool, and Malnutrition
cumference as a simple screening marker for diagnosing sarcope- Universal Screening Tool are good predictors of nutrition risk in
nia in older korean adults: the Korean Frailty and Aging Cohort an emergency service. Nutr Clin Pract. 2017;32(4):526–532. doi:
Study (KFACS). J Korean Med Sci. 2018;33(20):e151. doi:10. 10.1177/0884533617692527.
3346/jkms.2018.33.e151. 24. Kondrup J, Rasmussen HH, Hamberg O, Stanga Z, Espen WG.
11. Chumlea WC, Roche AF, Mukherjee D. Nutritional assessment Nutritional Risk Screening (NRS 2002): a new method based on
of the elderly through anthropometry. Columbus (OH): Ross an analysis of controlled clinical trials. Clin Nutr. 2003;22(3):
Laboratories; 1987. 321–336. doi:10.1016/S0261-5614(02)00214-5.
12. Lauretani F, Russo CR, Bandinelli S, Bartali B, Cavazzini C, Di 25. Detsky AS, McLaughlin JR, Baker JP, Johnston N, Whittaker S,
Iorio A, et al. Age-associated changes in skeletal muscles and Mendelson RA. What is subjective global assessment of nutri-
their effect on mobility: an operational diagnosis of sarcopenia. J tional status? JPEN J Parenter Enteral Nutr. 1987;11:8–13. doi:
Appl Physiol. 2003;95(5):1851–1860. doi:10.1152/japplphysiol.
10.1177/014860718701100108.
00246.2003.
26. Hwang AC, Liu LK, Lee WJ, Peng LN, Chen LK. Calf circumfer-
13. Barbosa-Silva TG, Bielemann RM, Gonzalez MC, Menezes AM.
ence as a screening instrument for appendicular muscle mass
Prevalence of sarcopenia among community-dwelling elderly of
measurement. J Am Med Dir Assoc. 2018;19(2):182–184. doi:10.
a medium-sized South American city: results of the COMO
VAI? study. J Cachexia Sarcopenia Muscle. 2016;7(2):136–143. 1016/j.jamda.2017.11.016.
doi:10.1002/jcsm.12049. 27. Meyer R, Stratton R. Basic concepts in nutrition: epidemiology
14. Maeda K, Koga T, Nasu T, Takaki M, Akagi J. Predictive accur- of malnutrition. e-ESPEN J. 2008;3:167–170.
acy of calf circumference measurements to detect decreased skel- 28. Marcadenti A, Mendes LL, Fink JS, Rabito EI, Silva FM.
etal muscle mass and European Society for Clinical Nutrition Nutritional Risk in Emergency – 2017 (NRE-2017): a new sim-
and Metabolism-defined malnutrition in hospitalized older plified proposal for a nutritional screening tool. JPEN J Parenter
patients. Ann Nutr Metab. 2017;71(1–2):10–15. doi:10.1159/ Enteral Nutr. 2018;42(7):1168–1176. doi:10.1002/jpen.1147.
000478707. 29. Rabito EI, Marcadenti A, Fink JS, Silva FM. The New European
15. Kawakami R, Murakami H, Sanada K, Tanaka N, Sawada SS, Society for Clinical Nutrition and Metabolism definition of mal-
Tabata I, Higuchi M, Miyachi M. Calf circumference as a surro- nutrition. JPEN J Parenter Enteral Nutr. 2018;42(3):550–556. doi:
gate marker of muscle mass for diagnosing sarcopenia in 10.1177/0148607117695248.
Japanese men and women. Geriatr Gerontol Int. 2015;15(8): 30. Cederholm T, Bosaeus I, Barazzoni R, Bauer J, Van Gossum A,
969–976. doi:10.1111/ggi.12377. Klek S, et al. Diagnostic criteria for malnutrition – an ESPEN
16. Leandro-Merhi VA, Aquino JLB, Reis LO. Predictors of nutri- consensus statement. Clin Nutr. 2015;34(3):335–340. doi:10.1016/
tional risk according to nrs-2002 and calf circumference in hos- j.clnu.2015.03.001.
pitalized older adults with neoplasms. Nutr Cancer. 2017;69(8): 31. Cederholm T, Jensen GL, Correia M, Gonzalez MC, Fukushima
1219–1226. doi:10.1080/01635581.2017.1367942. R, Higashiguchi T, et al. GLIM criteria for the diagnosis of mal-
17. Wakabayashi H, Sashika H. Malnutrition is associated with poor nutrition – a consensus report from the global clinical nutrition
rehabilitation outcome in elderly inpatients with hospital-associ- community. JPEN J Parenter Enteral Nutr. 2019;43(1):32–40.
ated deconditioning a prospective cohort study. J Rehabil Med. doi:10.1002/jpen.1440.
2014;46(3):277–282. doi:10.2340/16501977-1258. 32. Ho SC, Wang JY, Kuo HP, Huang CD, Lee KY, Chuang HC,
18. Weng C-H, Tien C-P, Li C-I, L’Heureux A, Liu C-S, Lin C-H, et al. Mid-arm and calf circumferences are stronger mortality
et al. Mid-upper arm circumference, calf circumference and predictors than body mass index for patients with chronic
mortality in Chinese long-term care facility residents: a prospect- obstructive pulmonary disease. Int J Chron Obstruct Pulmon
ive cohort study. BMJ Open. 2018;8(5):e020485. doi:10.1136/ Dis. 2016;11:2075–2080. doi:10.2147/COPD.S107326.
bmjopen-2017-020485. 33. Kamiya K, Masuda T, Matsue Y, Hamazaki N, Matsuzawa R,
19. Wijnhoven HAH, Van Bokhorst-de van der Schueren MAE, Tanaka S, et al. Prognostic usefulness of arm and calf circumfer-
Heymans MW, de Vet HC, Kruizenga HM, Twisk JW, et al.
ence in patients 65 years of age with cardiovascular disease.
Low mid-upper arm circumference, calf circumference, and body
Am J Cardiol. 2017;119(2):186–191. doi:10.1016/j.amjcard.2016.
mass index and mortality in older persons. J Gerontol A Biol Sci
09.040.
Med Sci. 2010;65(10):1107–1114. doi:10.1093/gerona/glq100.
34. Lin SJ, Hwang SJ, Liu CY, Lin HR. The relationship between
20. Tsai AC, Chang TL. The effectiveness of BMI, calf circumference
nutritional status and physical function, admission frequency,
and mid-arm circumference in predicting subsequent mortality
risk in elderly Taiwanese. Br J Nutr. 2011;105(2):275–281. doi:10. length of hospital stay, and mortality in old people living in
1017/S0007114510003429. long-term care facilities. J Nurs Res. 2012;20(2):110–121. doi:10.
21. Real GG, Fr€ uhauf IR, Sedrez JHK, Dall’Aqua EJF, Gonzalez MC. 1097/jnr.0b013e318254eac9.
Calf circumference: a marker of muscle mass as a predictor of 35. Waitzberg DL, Caiaffa WT, Correia MI. Hospital malnutrition:
hospital readmission. JPEN J Parenter Enteral Nutr. 2018;42(8): the Brazilian national survey (IBRANUTRI): a study of 4000
1272–1279. doi:10.1002/jpen.1170. patients. Nutrition. 2001;17(7–8):573–580. doi:10.1016/S0899-
22. Lidoriki I, Schizas D, Mpaili E, Vailas M, Sotiropoulou M, 9007(01)00573-1.
Papalampros A, Misiakos E, Karavokyros I, Pikoulis E, Liakakos 36. Jeejeebhoy KN, Keller H, Gramlich L, Allard JP, Laporte M,
T. Associations between skeletal muscle mass index, nutritional Duerksen DR, et al. Nutritional assessment: comparison of clin-
and functional status of patients with oesophago-gastric cancer. ical assessment and objective variables for the prediction of
Clin Nutr ESPEN. 2019;34:61–67. doi:10.1016/j.clnesp.2019.08. length of hospital stay and readmission. Am J Clin Nutr. 2015;
012. 101(5):956–965. doi:10.3945/ajcn.114.098665.

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