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 Clinical Nutrition ESPEN 54 (2023) 45e51

Contents lists available at ScienceDirect

Clinical Nutrition ESPEN

journal homepage: http://www.clinicalnutritionespen.com

Original article

The association between reduced calf and mid-arm circumferences

and ICU mortality in critically ill COVID-19 patients
Danieli Santer a, 1, Nicole Schneider a, 1, Yasmim Sena Silva de Carvalho b,
Renata Vieira de Souza Bortolini b, Fla
via Moraes Silva c, De

bora Luiza Franken b,
b, *
Jaqueline da Silva Fink
a ~o, Multiprofessional Residency in Health, Porto Alegre, Rio Grande do Sul, Brazil
Grupo Hospitalar Conceiça
b ~o, Division of Nutrition and Dietetics of Hospital Nossa Senhora da Conceiça
Grupo Hospitalar Conceiça ~o, Porto Alegre, Rio Grande do Sul, Brazil
c
Nutrition Department and Graduate Program of Nutrition Science at Universidade Federal de Ci^encias da Saúde de Porto Alegre, Rio Grande do Sul, Brazil

a r t i c l e i n f o s u m m a r y

Article history: Background & aims: Patients with COVID-19 are at a high risk of malnutrition caused by inflammatory
Received 25 August 2022 syndrome and persistent hypermetabolism, which may affect clinical outcomes. This study aimed to
Accepted 6 January 2023 evaluate the changes in nutritional status indicators between two time points of nutritional assessments
of COVID-19 patients during their stay in the intensive care unit (ICU). Moreover, the study also assessed
Keywords: the association of nutritional status with ICU mortality.
COVID-19
Methods: This cohort study included retrospective data of adult patients admitted to a public hospital
Intensive care units
ICU in southern Brazil, between March and September 2020. These participants with confirmed COVID-
Nutritional assessment
Nutritional status
19 diagnosis received nutritional assessment within the first 72 h after ICU admission. The anthropo-
metric measurements collected included mid-arm circumference (MAC) and calf circumference (CC). The
percentage (%) of MAC adequacy was calculated, and values < 50th percentile for sex and age were
considered low. CC values of
33 cm for women and
34 cm for men were indicative of reduced muscle
mass. Data on the date of discharge from the ICU and mortality outcome were collected.
Results: A total of 249 patients were included (53.4% men, 62.2 ± 13.9 years of age, SOFA severity score
9.6 ± 3.5). Of these, 22.7 and 39.1% had reduced MAC and CC at ICU admission, respectively. In these
participants, weight, MAC, CC, and % MAC decreased significantly from the first to second nutritional
assessment (p < 0.05), but there was no significant difference between survivors and non-survivors.
Patients with reduced CC (HR ¼ 2.63; 95% CI 1.65e4.18) or reduced MAC (HR ¼ 2.11; 95% CI 1.37
e3.23) at the first nutritional assessment had approximately twice the risk of death in the ICU than those
with normal CC and normal MAC, regardless of the severity assessed by the SOFA score and age.
Conclusion: Reduced MAC and CC values were identified in approximately 20 and 40% of COVID-19
patients admitted to the ICU, respectively. Additionally, these indicators of nutritional depletion were
associated with an approximately 2-fold increase in the risk of ICU mortality. A significant reduction in
anthropometric indicators during the first weeks of ICU stay confirmed the deterioration of nutritional
status in these patients, although this was not associated with mortality.
© 2023 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights
reserved.

1. Introduction involvement of the lung parenchyma. Approximately 5% of the

cases develop into a critical condition, progressing to acute res-
Although coronavirus disease 2019 (COVID-19) presents piratory failure, pneumonia, shock, multi-organ failure, and death
mostly mild or asymptomatic, a severe course occurs in nearly [1,2]. More than 6.1 million deaths have been caused by COVID-19
10% of cases, with dyspnea, hypoxemia, and extensive worldwide [3].

* Corresponding author. Grupo Hospitalar Conceiça ~o, Division of Nutrition and Dietetics of Hospital Nossa Senhora da Conceiça
~o, Francisco Trein Avenue, 596, Cristo
Redentor, 91350-200, Porto Alegre, Rio Grande do Sul, Brazil.
E-mail address: jaquelinefink@yahoo.com.br (J. da Silva Fink).
1
Danieli Santer and Nicole Schneider are equal contributors to this work and designated as co-first authors.

https://doi.org/10.1016/j.clnesp.2023.01.006
2405-4577/© 2023 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved.
D. Santer, N. Schneider, Y.S.S. de Carvalho et al.
COVID-19 in its critical form induces inflammatory syndrome
and persistent hypermetabolism, with increased energy and pro-
tein expenditure [4e6]. Cytokine storms have also been reported in
severe COVID-19 and are associated with multiple organ failure [7].
In this scenario, energy-protein supply may be impaired by he-
modynamic instability, infection, anorexia, loss of smell and taste,
dyspnea, vomiting, and diarrhea [8]. Thus, COVID-19 patients are at
a high risk of nutritional impairment [9e11], and reduced mobility
due to prolonged hospitalization. Moreover, factors including
advanced age and comorbidities contribute to nutritional defi-
ciency [12e15].
Critically ill patients with acute respiratory distress syndrome
(ARDS) presenting with neuromuscular weakness have been re-
ported to have higher mortality, reduced quality of life, reduced
physical capacity and require more resources after discharge from
the intensive care unit (ICU) due to prolonged hospitalization [16].
Therefore, patients affected by acute lung disease need monitoring
of changes in nutritional status and adequate nutritional support to
diminish the effects of intense catabolism and the consequent loss
of muscle mass.
The nutritional assessment of critically ill patients is chal-
lenging. Frequent edema due to excess fluid and a high degree of
inflammation [17] leads to an overestimation of the patient's
weight. Furthermore, adequate nutritional anamnesis can be diffi-
cult due to intubation and/or sedation. Alternative parameters
including the measurement of the phase angle using bioimpedance
(BIA) have been used in critical patients [18,19], however, owing to
its high cost, BIA is not routinely performed in the ICU. Anthropo-
metric measurements are important for assessing the nutritional
status of hospitalized patients because they are low-cost, quick, and
non-invasive [20]. Calf circumference (CC) is used to detect muscle
depletion in older adults [21] and is a predictor of mortality [20]
and hospital readmission [22] in non-critical patients. In contrast,
mid-arm circumference (MAC) reflects the total body reserves, and
its percentage of adequacy is a predictor of malnutrition in critically
ill patients [23].
No studies have reported the prognostic value of reduced CC and
MAC values in critically ill patients with COVID-19. Therefore, the
objective of this study was to evaluate the change in nutritional
status of critically ill COVID-19 patients through serial anthropo-
metric measurements and the validity of reduced CC and MAC in
predicting ICU mortality. We hypothesized that critically ill COVID-
19 patients with reduced CC and MAC are at an increased risk of
death and that these measures are reduced during ICU stay.
2. Patients & methods
2.1. Study design
This was a retrospective cohort study. The research was con-
ducted in the ICU of the Hospital Nossa Senhora Conceiç~ ao (HNSC),
Grupo Hospitalar Conceiç~ ao (GHC), Porto Alegre, Rio Grande do Sul,
Brazil. This study was approved by the Research Ethics Committee
(protocol number 4164341) from Grupo Hospitalar Conceiç~ ao
(GHC), Porto Alegre, Rio Grande do Sul, Brazil.
2.2. Patients
The study population included all adult patients admitted to the
HNSC ICU with COVID-19, between March 2020 and September
2020. Inclusion criteria were age 18 years, and diagnosis of
COVID-19 confirmed by reverse-transcription polymerase chain
reaction or antigen test [24]. Patients with no data on nutritional
assessment and monitoring during ICU stay were excluded.
46
Clinical Nutrition ESPEN 54 (2023) 45e51
So far, no studies have evaluated the association of CC and MAC
with mortality in critically ill patients. Therefore, we considered the
reported prognostic value of malnutrition in the sample size
calculation. The sample size was calculated based on a previous
report [25]. Using the difference in CC between well-nourished
(34.93 ± 3.19) and malnourished (32.04 ± 4.16) patients based on
the Subjective Global Assessment (SGA), alpha of 5%, power of 80%
and an additional 20% for adjustments in multivariate analysis, the
estimated sample size was 64 patients. Based on the difference in
MAC between patients with and without malnutrition (31.07 ± 3.90
versus 28.90 ± 4.80), the estimated sample size (5% alpha, 80%
power, and an additional 20%) was 154 patients, and the largest
sample size estimate was adopted for the present study.
2.3. Data collection
Between March and April of the study period, anthropometric
measurements were conducted by trained non-dietitian pro-
fessionals from the multidisciplinary team providing care to pa-
tients according to recommendations for the safety of professionals
and patients at the beginning of the pandemic, which advised the
fewest possible number of professionals in direct patient care
[26e28]. As of May, nutritional assessments have been carried out
by dietitians from the assistant team.
According to the institutional protocol, the first nutritional
assessment was expected to be performed within the first 72 h after
ICU admission, and the second nutritional assessment was ex-
pected to occur on the tenth day after the first nutritional assess-
ment. MAC and CC were measured using inelastic tape on the right
or left limb. To measure the CC, the tape was passed around the
greatest circumference area of the calf, with the leg extended or
slightly flexed in critical patients with limited mobility [29]. To
measure the MAC, initially, the arm was flexed at 90 to determine
the midpoint between the acromion and olecranon and, later, the
arm was extended along the body for the measurement [30]. In
addition, weight and height were estimated from knee height and
MAC measurements using predictive equations [31].
Data were retrospectively collected from the electronic medical
records of patients by two previously trained resident dietitians. The
following information was collected: age, sex, clinical and labora-
tory data from the first 24 h of ICU admission to calculate the
Sequential Organ Failure Assessment (SOFA) severity score [32],
start of the diet in the ICU (
48 h or > 48 h), length of stay (in days),
and ICU outcome (discharge or death). Subsequently, for sample
characterization, age and SOFA scores were classified according to
the cut-off points of the Nutrition Risk in Critically ill (NUTRIC) tool
[33]. The following morbidities were also evaluated: type 2 diabetes
mellitus (T2DM), hypertension, other heart diseases, asthma,
chronic obstructive pulmonary disease (COPD), chronic kidney
disease (CKD) and neoplasms. Patients with two or more chronic
conditions among those evaluated were considered multimorbid
[34].
As nutritional status indicators, the collected data included
weight (in kilograms) and height (in centimeters), as well as the
way they were determined (measured, estimated, or informed),
mid-arm circumference (MAC), and calf circumference (CC) in
centimeters, corresponding to the first and second nutritional as-
sessments performed in the ICU. To classify the MAC, its percentage
of adequacy was calculated by dividing the MAC measure by the
MAC value corresponding to the 50th percentile according to sex
and age [35]. A reduced MAC, indicative of malnutrition, was
considered when the adequacy was lower than 90% [36]. For the
classification of reduced CC, indicative of muscle depletion, the cut-
off points proposed by Barbosa-Silva et al. (
33 cm for women and

34 cm for men) were used [21]. The body mass index (BMI) was
D. Santer, N. Schneider, Y.S.S. de Carvalho et al. Clinical Nutrition ESPEN 54 (2023) 45e51

Table 1
Characteristics of the sample of COVID-19 patients admitted to the intensive care unit (ICU) according to the first nutritional assessment.

Reduced MAC (n ¼ 56) Normal MAC (n ¼ 191) p-value Reduced CC (n ¼ 70) Normal CC (n ¼ 109) p-value

Age (years) 0.259 <0.001

<50 3.6 22.5 1.4 29.3
50 e <75 83.9 56.5 61.4 60.5
75 12.5 20.9 37.1 10.1
Sex 0.007 0.269
Male 69.6 49.2 64.3 56.0
Female 30.4 50.8 35.7 44.0
Start of diet in the ICU 0.414 0.072

48 h 98.1 95.8 100.0 95.4
>48 h 1.9 4.2 0.0 4.6
BMI (kg/m2) <0.001 <0.001
<18.5 14.3 0.0 5.7 0.9
18.5e24.9 82.1 11.5 62.8 11.9
25e29.9 1.8 37.7 22.8 37.6
30 1.8 50.8 8.6 49.5
Morbidity
T2DM 41.0 42.4 0.859 48.6 38.5 0.185
Hypertension 51.8 68.0 0.025 64.3 59.6 0.533
Other cardiac diseases 25.0 17.8 0.231 25.7 16.5 0.134
Asthma 7.1 4.7 0.474 7.3 2.9 0.203
COPD 28.6 12.0 0.003 30.0 8.3 <0.001
CKD 7.1 17.3 0.062 14.3 14.7 0.942
Neoplasms 23.2 10.5 0.014 24.3 7.3 <0.001
Multimorbidity (2) 0.850 0.009
No 46.1 44.6 34.3 54.1
Yes 53.9 55.3 65.7 45.9
SOFA score 0.057 0.627
<6 21.4 10.5 17.1 11.0
6 e <10 28.6 29.8 20.0 37.6
10 50.0 59.7 62.9 51.4

Abbreviations: MAC: mid-arm circumference; CC: calf circumference; T2DM ¼ type 2 diabetes mellitus; COPD: chronic obstructive pulmonary disease; CKD: chronic kidney
disease.
Data are presented as relative frequency. Chi-square test. P values < 0.05 are in bold.

calculated by dividing weight (in kilograms) by height (in meters)
squared, which was later classified as underweight (<18.5 kg/m2),
normal weight (18.5e24.9 kg/m2), overweight (25e29.9 kg/m2) or
obesity (30 kg/m2) [29].
The clinical outcome evaluated in this study was ICU mortality.
2.4. Statistical analyses
Descriptive statistics, mean and standard deviation for para-
metric quantitative variables, median and interquartile range for
nonparametric quantitative variables, and numbers and percent-
ages for categorical variables were calculated. The normality of the
quantitative variables was assessed using the Kolmogorove
Smirnov test. The comparison of anthropometric data collected
from the first and second nutritional assessments was performed
using the t-test for paired samples, and the frequency of reduced
MAC and CC was compared using the McNemar test. Comparisons
between survivors and non-survivors with respect to changes in
anthropometric data were performed using the ManneWhitney
test, and the frequency of reduced CC and MAC was compared us-
ing the Chi-square test. The validity of the change in anthropometric
indicators, as well as the reduced MAC and CC of the first nutritional
assessment in predicting death, was tested by Cox regression in an
unadjusted model and a model adjusted for SOFA score and age. The
analysis was performed using SPSS 20.0, and Stata version 12.0.
Statistical significance was set at p < 0.05.
3. Results
A total of 249 patients were included in the study, with a mean
age of 62.2 ± 13.9 years, and 53.8% (n ¼ 134) were male. The mean
SOFA score was 9.6 ± 3.5, the median ICU stay was 14 (8e24) days,
47
and the incidence of ICU death was 48.6% (n ¼ 121). Regarding the
anthropometric indicators of the first nutritional assessment, the
median BMI was 28.7 (24.2e32.1) kg/m2, and obesity was identified
in nearly 40% of the sample (n ¼ 99). The frequency of reduced MAC
(n ¼ 56) was 22.7% (95% CI 17.6e28.4) and the frequency of reduced
CC (n ¼ 70) was 39.1% (95% CI 31.9e46.7).
The most frequent morbidities were hypertension (n ¼ 160,
64.3%) and T2DM (n ¼ 104, 41.8%), and more than half of the sample
(n ¼ 136, 54.6%) was multimorbid. Most patients (n ¼ 236, 96.3%)
started a diet within 48 h of ICU admission. Patients with reduced
MAC and CC at the first nutritional assessment did not differ from
those with normal MAC and CC in terms of the start of diet in the
ICU and SOFA scores (Table 1).
Only 38.1% (n ¼ 95) of the patients underwent nutritional
reassessment during their ICU stay. Among these, 69.9% had the
weight estimated, 18.3% had the weight informed, and 11.8% had
the weight measured in the first evaluation. In the second evalua-
tion, 72.6% of patients had an estimated weight, 9.5% were
informed, and 17.9% were measured. The same weight measure-
ment was used in both assessments in 74.2% of the patients.
Table 2 shows the changes in anthropometric indicators be-
tween the first and second nutritional assessment performed in the
ICU. A mean reduction of 5.5 percentage points in MAC adequacy
and 6 kg in body weight was observed between the two nutritional
assessments. The median time between assessments was 12.5
(9.0e18.3) days. The median change in MAC and CC was 1.7 and
1.5 cm, respectively.
The frequency of patients with reduced CC was significantly
higher in non-survivors than in survivors, whereas the frequency of
patients with reduced MAC did not differ between the groups
(Table 3). According to multivariate analysis adjusted for the SOFA
score and age, reduced MAC increased the risk of death in the ICU
D. Santer, N. Schneider, Y.S.S. de Carvalho et al. Clinical Nutrition ESPEN 54 (2023) 45e51

Table 2
Changes in anthropometric indicators between the first and second nutritional assessments performed in critically ill COVID-19 patients.

First assessment Second assessment Mean difference (CI 95%) p-value

MAC (cm) (n¼92) 33.3 ± 5.0 31.6 ± 4.5 1.7 (1.2e2.2) <0.001a
MAC adequacy (%) (n¼92) 106.4 ± 16.6 100.9 ± 14.5 5.5 (3.9e7.1) <0.001a
CC (cm) (n¼52) 37.1 ± 5.2 35.6 ± 5.5 1.5 (0.9e2.1) <0.001a
Weight (kg) (n¼95) 84.1 ± 20.4 78.1 ± 18.6 6.0 (4.5e7.5) <0.001a
Reduced MAC (n¼92) 18 (19.6%) 20 (21.7%) e 0.791b
Reduced CC (n¼52) 9 (17.3%) 14 (26.9%) e 0.180b

Abbreviations: MAC: mid-arm circumference; CC: calf circumference.

Data presented as mean ± standard deviation or number (%). P values < 0.05 are in bold.
a
T-test for paired samples.
b
McNemar test.

Table 3
Comparison of anthropometric indicators between ICU survivors and non-survivors of COVID-19.

Survivors (n ¼ 126) Non-survivors (n ¼ 121) p-value

Reduced CC and MAC at ICU admission

Reduced CC a 24 (25.3%) 46 (54.8%) <0.001a
Reduced MAC b 24 (19.0%) 32 (26.4%) 0.216a
Anthropometric changes from the first to the second nutritional assessment
D MAC (cm) c 1.5 (0.0e2.5) 2.0 (21.0e3.0) 0.067b
D MAC adequacy (%) c 5.0 (0.0e7.9) 6.4 (3.3e11.2) 0.082b
D CC (cm) d 1.5 (0.0e3.0) 0.5 (0.5e3.3) 0.647b
D Weight (kg) e 4.5 (0.0e9.0) 6.1 (3.0e9.5) 0.122b

CC: calf circumference; MAC: mid-arm circumference.

n ¼ a 95 versus 84; b 126 versus 121; c 55 versus 23; d 35 versus 9; e 58 versus 23.
Data are presented in number (%) or median (P25 e P75). P values < 0.05 are in bold.
a
Chi-square test.
b
ManneWhitney test.

Table 4 4.1. Interpretation of findings and comparison with other studies

Prognostic value of anthropometric indicators for predicting ICU death in patients
with COVID-19. In our study, approximately 20% of the patients had reduced
Unadjusted analysis Adjusted analysis MAC at admission, which presented a 2.11 times greater risk of ICU
death than that of patients with normal or high MAC adequacy. The
HR (CI 95%) p-value HR (CI 95%) p-value
MAC adequacy values below 90% indicate reduced body mass and
Reduced CC 3.25 (2.09e5.05) <0.001 2.63 (1.65e4.18) <0.001
are more frequent in malnourished patients [36]. A study con-
Reduced MAC 1.53 (1.02e2.30) 0.039 2.11 (1.37e3.23) 0.001
D MAC (cm) 0.95 (0.86e1.05) 0.304 0.97 (0.82e1.13) 0.661 ducted with 76 critically ill surgical patients showed lower MAC
D MAC adequacy (%) 1.00 (0.95e1.04) 0.912 0.99 (0.94e1.04) 0.689 values in malnourished patients than in well-nourished patients,
D Weight (kg) 1.03 (0.98e1.09) 0.252 1.03 (0.92e1.20) 0.248 according to the SGA [37]. The prognostic value of malnutrition in
CC: calf circumference; MAC: mid-arm circumference. critically ill patients has already been demonstrated by several
Cox regression. Analysis adjusted for SOFA and age. P values < 0.05 are in bold. studies that applied the SGA [38] or other integrative tools for
malnutrition diagnosis, such as AND-ASPEN [39] and the GLIM
criteria [40,41]. However, the feasibility of malnutrition diagnosis
by 2.11-fold, while reduced CC increased the risk of this outcome in using these tools in the ICU environment is limited because all of
COVID-19 patients by 2.63-fold (Table 4). them require detailed nutritional analysis combined with an ac-
There was no significant difference in the changes in anthro- curate physical examination [42,43]. Simpson et al. also demon-
pometric indicators collected from the first to the second nutri- strated the prognostic value of MAC in a sample of 1363 critically ill
tional assessment between survivors and non-survivors, as shown patients; for each 1 cm increase in MAC, there was a 3% reduction in
in Table 3. The changes in anthropometric measurements were hospital mortality risk [44]. Although reduced MAC should not be
not associated with ICU mortality in the multivariate model used alone to diagnose malnutrition, its assessment in critically ill
(Table 4). patients is relevant due to its low-cost, quick, and easy measure-
ment beyond its prognostic value.
4. Discussion Approximately 40% of critically ill COVID-19 patients admitted
to the ICU had reduced muscle mass according to CC, and this
This study evaluated the prognostic value of quick, easy, and condition was associated with a 2.63-fold increased risk of ICU
low-cost anthropometric measures to monitor the nutritional sta- mortality. No similar studies involving critically ill patients have
tus of critically ill COVID-19 patients. Low measures of CC and MAC been conducted for comparison. However, in a systematic review of
on ICU admission were independently associated with more than non-critical patients, reduced CC was associated with a higher risk
twice the risk of ICU death. Both measures decreased during the ICU of mortality (HR ¼ 2.66, 95% CI 2.06e3.43) [20]. In addition, in a
stay, indicating fat and muscle mass depletion, although it was not study of 329 older Chinese adults admitted to long-term care in-
associated with ICU mortality. stitutions and followed up for seven years, lower MAC and CC

48
D. Santer, N. Schneider, Y.S.S. de Carvalho et al.
values were associated with higher mortality [45]. In COVID-19
patients, only one study evaluated the effect of reduced CC. This
study included 182 hospitalized non-critical older Chinese patients
and demonstrated that reduced CC was an independent risk factor
for malnutrition (OR ¼ 2.42; 95% CI 2.29e3.53), but the cut-off
point used for reduced CC classification was not described by the
authors, which is a considerable limitation [46]. Moreover, a study
of 86 critically ill COVID-19 patients showed that reduced muscle
mass at admission, as assessed by computed tomography (CT), was
associated with prolonged hospital and ICU stay and a higher rate of
tracheostomy [47]. In another study involving 81 critically ill
COVID-19 patients, preserved muscle mass assessed by CT was
associated with successful extubation (OR ¼ 1.02, 95% CI
1.00e1.03), shorter ICU stay (OR ¼ 0.97, 95% CI 0.95e0.99) and
decreased hospital mortality (HR ¼ 0.98, 95% CI 0.96e0.99) [48].
However, CT data is not commonly available due to the high cost.
Monitoring the nutritional status of critically ill patients is a
major challenge, and the international guidelines do not provide
clear recommendations on how this stage of nutritional care should
be conducted. In our study, a reduction of 1.5 and 1.7 cm was
observed in the CC and MAC, respectively from the first to second
nutritional assessment, with a median interval of 12 days between
them. However, these changes were not associated with increased
mortality rate. In Brazil, a study of 60 critically ill patients evaluated
the change in anthropometric measurements, including MAC and
CC, in the first week of ICU admission [49]. Both increase and
decrease in measurements were reported over the days, possibly
due to edema; however, on the 7th day, the measurements were
lower than on the first day, similar to what was observed in our
study. Moreover, loss of muscle mass during the first week in the
ICU (assessed by ultrasound) and nutritional status (assessed by
both SGA and GLIM) were not associated with clinical outcomes,
probably because of the small sample size. This factor could also
play an important role in our study due to the limited sample size in
the second nutritional assessment, which may have contributed to
the lack of association in these analyses.
No other study has evaluated the association between changes
in anthropometric measurements and mortality. One study evalu-
ated the change in body composition across the lumbar cross-
sectional area using abdominal CT, with a small sample of 25 crit-
ically ill patients. Furthermore, the variation in visceral adipose
tissue during the first 7e14 days of ICU stay was significantly
greater in non-survivors than in survivors (22.34 cm2/m2
versus 6.22 cm2/m2, respectively, p ¼ 0.039). No significant as-
sociation was observed between changes in skeletal muscle mass
and mortality [50]. Puthucheary et al. evaluated 63 critically ill
patients and showed that the rectus femoris cross-sectional area
assessed by ultrasound (US) reduced by 12% during the first ICU
week, decreasing by up to 17.7% on day 10 [51]. The muscle thick-
ness of 70 patients with sepsis was measured at mid-arm and mid-
thigh using bedside US at different time points until ICU discharge,
and early decline (from day 1 to day 3) in muscle thickness was
associated with in-hospital mortality [52]. Although the application
of US has been increasing due to its wide availability, relatively low
cost, and no complexity in application, it depends on the evalua-
tor's ability and is influenced by fluid overload [53].
CC is a low-cost, quick, and easy measure for assessing muscle
mass. It is important to highlight that the COMO VAI study estab-
lished the cut-off points used to classify reduced muscle mass in the
current study using a subsample's dual X-ray absorptiometry esti-
mation of the appendicular skeletal muscle mass index (ASMI) as
the gold standard method [21], and other studies also showed an
acceptable concordance between CC and indicators of muscle mass
evaluated using reference methods [54,55]. Similar to MAC, CC can
also be measured at the bedside and is a non-invasive measure.
49
Clinical Nutrition ESPEN 54 (2023) 45e51
However, fluid overload can limit the application of both MAC and
CC in ICU settings [56]. In addition, in obese patients, the CC
adopted cut-off points may not reflect a sarcopenic obesity process
[57].
4.2. Strengths and limitations
Our study has some limitations including the use of different
forms of weight measurement, which is common in the ICU, and
the different time intervals between nutritional assessments. The
schedule of nutritional reassessments had to be modified for pa-
tients with edema or severe hemodynamic instability or trans-
ferred to the operating room, for example. Moreover, the
limitations of retrospective data in a cohort study need to be
emphasized, especially those related to measurement bias, since it
is not possible to exclude the possibility of errors in the anthro-
pometric measurements performed by the assistant team. How-
ever, the clinical relevance of this study needs to be highlighted,
especially in the context of recommendations for remote nutri-
tional care, in the early period of the COVID-19 pandemic [27,28].
Contrary to previous recommendations, indicators that are easily
and quickly measured by dietitians were valuable in predicting the
mortality of critically ill COVID-19 patients.
5. Conclusion
Reduced CC and MAC measures were predictors of an increased
risk of ICU death in critically ill COVID-19 patients by more than
two-fold. The nutritional status indicators analysed in this study
were significantly reduced from the first to the second nutritional
assessment; however, this reduction was not associated with
increased mortality in the studied sample. This study highlights the
clinical importance of easy and quick anthropometric measures to
identify the nutritional status early, in order to direct the best
nutritional care to the critically ill COVID-19 population.
Funding statement
This research did not receive any funding.
Author's contributions
Danieli Santer and Nicole Schneider: Conceptualization,
Methodology, Formal analysis, Investigation, Writing - Original

bora Luiza Franken, Fla
Draft. De
via Moraes Silva, Jaqueline da
Silva Fink: Conceptualization, Methodology, Formal analysis,
Writing - Review & Editing. Yasmim Sena Silva de Carvalho,
Renata Vieira de Souza Bortolini: Conceptualization, Writing -
Review & Editing.
Declaration of competing interest
All authors have declared no conflict of interest.
Acknowledgment
Fl

avia Moraes Silva receives a Productivity Scholarship from
CNPq.
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