Nutrition 125 (2024) 112505

Contents lists available at ScienceDirect

Nutrition
journal homepage: www.nutritionjrnl.com

Applied nutritional investigation

Body mass index-adjusted calf circumference is associated with

mortality in hospitalized older patients with excess weight
Jarson Pedro da Costa Pereira MSc a, Maria Cristina Gonzalez PhD, MD b, Carla M. Prado PhD, RD c,
Poliana Coelho Cabral PhD a, Tais Galdencio do Nascimento MSc a, Maria Karolainy do Nascimento RD g,
Alcides da Silva Diniz PhD, MD a, Claudia Porto Sabino Pinho Ramiro PhD, RD d,e,f,
Ana Paula Trussardi Fayh PhD, RD g,h,*
a
Postgraduate Program in Nutrition and Public Health, Department of Nutrition, Federal University of Pernambuco, Recife, Pernambuco, Brazil
b
Postgraduate Program in Nutrition and Food, Federal University of Pelotas, Pelotas, Rio Grande do Sul, Brazil
c
Human Nutrition Research Unit, Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada
d
Hospital of Clinics, Federal University of Pernambuco, Recife, Pernambuco, Brazil
e
Brazilian Company of Hospital Services, EBSERH, Recife, Pernambuco, Brazil
f
Emergency Cardiology Unit of the University of Pernambuco, Recife, Pernambuco, Brazil
g
Postgraduate Program in Health Science, Health Science Center, Federal University of Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil
h
PesqClin Lab, Onofre Lopes University Hospital, Brazilian Company of Hospital Services (EBSERH), Federal University of Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil

A R T I C L E I N F O A B S T R A C T

Article History: Objectives: Given the innovative nature of the method, our study aimed to assess the prognostic significance
Received 7 March 2024 of body mass index (BMI)-adjusted calf circumference (CC) in older patients who are hospitalized.
Received in revised form 28 May 2024 Methods: This was a unique analysis as part of other cohorts comprising general hospitalized patients aged
Accepted 29 May 2024
60 years or older of both sexes. Only patients with excess weight (BMI
25 kg/m2) were included. CC was
adjusted by reducing 3, 7, or 12 cm for BMI (in kg/m2) within 25-29.9, 30
39.9, and
40 kg/m2, respectively.
Keywords:
CC was considered low if  34 cm for males and  33 cm for females. Clinical outcomes included prolonged
Calf circumference
length of hospital stay (LOS) and mortality.
Body mass index
Body composition
Results: A total of 222 patients were included. After BMI adjustments, 72.1% of the patients were reclassified
Muscle mass from a normal CC category to a low CC category. The frequency of low CC increased from 33.8% to 81.9% fol-
Prognosis lowing BMI adjustments. Among those reclassified to the low CC, 11 died, compared to only 2 patients in the
Obesity group that maintained a normal CC classification. BMI-adjusted CC was inversely associated with mortality
(HR adjusted 0.84, 95% CI 0.73 to 0.95), but not with prolonged LOS.
Conclusions: Our novel study highlights the prognostic value of BMI-adjusted CC. As an anthropometric
marker of muscle mass, it proved to be a predictor of mortality in older patients with high BMI. This adjust-
ment is further important because it may help to better detect low muscle mass in these patients where such
conditions might be masked.
© 2024 Elsevier Inc. All rights are reserved, including those for text and data mining, AI training, and similar
technologies.

Introduction

Aging is a natural process that results in changes in body com-

This study was partially funded by the Coordenaç a~o de Aperfeiçoamento de Pes- position, marked by the mobilization of fat mass and a simulta-
soal de Nível Superior (CAPES), Brazil (Finance Code 001) and the Brazilian National neous decline in fat-free mass, particularly in skeletal muscle [1,2].
Council for Scientific and Technological Development (CNPq). APTF and MCG Older adults are more susceptible to both chronic and acute dis-
received a productivity scholarship from CNPq. The supporting sources had no
eases, which can significantly impact overall nutritional status [3].
involvement or restrictions on this publication.
*Corresponding author: Ana Paula Trussardi Fayh, R.D., Ph.D. Graduate Program in
This susceptibility may lead to conditions such as sarcopenia and
Nutrition, Health Sciences Center, Universidade Federal do Rio Grande do Norte, malnutrition, even in individuals with excess weight [4,5]. A com-
Avenida Senador Salgado Filho, n° 3000, Natal, RN 59078-970, Brazil. mon characteristic of these nutritional conditions is low muscle
E-mail address: ana.fayh@ufrn.br (A.P.T. Fayh).

https://doi.org/10.1016/j.nut.2024.112505
0899-9007/© 2024 Elsevier Inc. All rights are reserved, including those for text and data mining, AI training, and similar technologies.

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2 J.P.d. Costa Pereira et al. / Nutrition 125 (2024) 112505

mass [5], underscoring the importance of assessing muscle mass in the non-edematous calf was measured instead. The measuring tape was wrapped
clinical settings. In this context, anthropometry emerges as a prac- firmly around the largest part of the calf, pulled taut to lie closely against the skin,
without compression. The evaluator knelt beside the participant, gently sliding
tical, cost-effective, and feasible method for estimating muscle
the tape up and down to pinpoint the maximum circumference. Measurements
mass when more precise and robust techniques are not readily were conducted twice and the mean value was recorded for analytical purposes.
available [6]. CC was considered low if 34 cm for men and 33 cm for women [23]. CC was
Calf circumference (CC) is widely utilized as a marker of muscle adjusted for BMI by subtracting 3, 7, or 12 cm (for BMI categories of 25
29,
30
39, and
40 kg/m2, respectively), according to Gonzalez et al [19].
mass in both clinical and research settings [6-8]. CC serves as a
practical parameter that can aid in the diagnosis of conditions such
Statistical analyses
as malnutrition and sarcopenia [9
12]. Furthermore, additional
evidence has demonstrated the prognostic value of CC as a signifi- Data were analyzed using the MedCalc version 22.0.0.9 software (MedCalc,
cant predictor of adverse outcomes, such as falls, frailty, prolonged Mariakerke, Belgium), and Statistical Package for the Social Sciences (SPSS), ver-
length of hospital stay (LOS), and mortality [13
18]. However, the sion 20.0 (SPSS IBM Inc., Chicago, IL, USA). Normality of continuous variables was
assessed using the Shapiro-Wilk test. Data with normal distribution was described
use of CC in patients with excess weight (body mass index, BMI,
as mean § standard deviation (SD) and compared using an independent Student’s

25 kg/m2) can be compromised due to the potential impact of “t” test or 1-way ANOVA. Non-normally distributed data was described as median
body size and adiposity [6,19]. Excess adiposity may lead to falsely and interquartile (IQ) ranges, and compared using the Mann-Whitney U test or
normal CC values, masking low muscle mass levels, potentially Kruskal-Wallis, as appropriate. Categorical variables were presented as frequen-
affecting CC’s prognostic value. cies (N) and relative percentages (%), and the respective tests were applied (Pear-
son’s x2, Fisher’s exact, or likelihood ratio x2 tests).
Considering the challenges of assessing CC in patients with Cramer’s V was used to measure the effect size (ES) of the univariate associa-
excess body weight, a group of experts developed a method to tion between CC categories and mortality (low CC prior adjustment, low BMI-
adjust CC measurements based on BMI [19]. They recommended adjusted CC, and normal BMI-adjusted CC). Values  0.2 indicate a weak effect, 0.2
reducing CC by 3 cm for those with a BMI of 25
29.9 kg/m2, 7 cm to 0.6 a moderate effect, and > 0.6 a strong effect. A Cox proportional hazards anal-
ysis was conducted in both crude and adjusted forms to assess the independent
for a BMI of 30
39.9 kg/m2, and 12 cm for a BMI over 40 kg/m2 association between BMI-adjusted CC and clinical outcomes. To estimate the risk
[19]. As a novel method, the prognostic value of BMI-adjusted CC associated with a decrease in BMI-adjusted CC (continuous variable), the recipro-
in relation to adverse health outcomes is still largely unexplored. cal of the hazard ratio (1/HR) was calculated. Data on age, sex, clinical diagnoses,
Consequently, there is a clear need for further research into this and comorbidities were included as adjustment factors due to their clinical rela-
tionship with outcomes. Statistical significance was set at P < 0.05 for all analyses.
crucial area. Therefore, our study aimed to evaluate the prognostic
Although this is a debatable approach, a post hoc sample size calculation to
value of BMI-adjusted CC in relation to clinical outcomes among assess the study’s power was estimated, centered on the main outcome: overall
older hospitalized patients with excess weight. mortality found in our own sample. Statcalc program of the EPI-INFO software,
version 6.04 (CDC, Atlanta, GE, USA) was utilized for this purpose. The Fleiss
Material and methods method with continuity correction was employed. Parameters used included a sig-
nificance level of 95% (1-a), a study power of 80% (1-b), and a ratio of 0.72. Expo-
Study design and participants sure was defined as the phenotype of low CC. Mortality incidence in the exposure
group was 58.1%, compared to 41.9% in the unexposed group, with an odds
This study presents a unique analysis of other cohorts with prospective data ratio of 3.26 used for calculation. Based on these criteria, a minimum sample size
collection [20,21], assessing the nutritional status of older patients hospitalized in of 112 participants was estimated.
two Northeast Brazilian hospitals (Hospital das Clínicas de Pernambuco and Pronto
Socorro Cardiolo  gico Universitario de Pernambuco Prof. Luiz Tavares). Studies
were conducted between May 2021 and June 2023, and patients were conve- Results
niently sampled. Consecutive patients aged 60 years or older of both sexes, who
were hospitalized in clinical and surgical wards for multiple causes, were opportu- This study initially screened for 558 eligible patients; however,
nistically included in this analysis.
47 were excluded due to inconsistent or missing CC data. Among
Patients with excess weight by BMI criteria (
25 kg/m2) were selected for this
analysis [22]. Trained registered dietitians screened for eligibility using electronic the 511 patients, 299 had excess weight by BMI (
25 kg/m2). Of
medical records. Data collection was conducted within 72 hours of hospital admis- those, 77 patients were excluded due to the absence of clinical out-
sion. For our analyses, patients without CC measurements and those without clini- comes or those aged under 60 y, resulting in a final sample of 222
cal outcomes were excluded. At the first evaluation, patients who were unable to patients (Fig. 1). Most of the patients were males (51.4%), 34.2%
complete the questionnaires or had conditions that could interfere with anthropo-
metric assessments, such as severe edema (also in both legs), ascites, severe ill-
had a heart disease diagnoses, and 25.2% had cancer. Regarding
nesses, or postoperative trauma, were also excluded. The study was approved by comorbidities, 82.2% had SAH and 50% DM2.
the Institutional Ethics Committees, in compliance with the Declaration of Helsinki Patients were monitored during their hospitalization and after
(1964), its subsequent revisions, and Resolution no. 466/2012 of the National discharge, with an average follow-up of 8.5 months and a maxi-
Health Council. All patients provided their written informed consent.
mum period of 28 months. During the follow-up, mortality inci-
Clinical assessment and covariates
dence was observed in 14% (n = 31) of the patients. Low
unadjusted CC was found in 33.8% of the patients (n = 75). This
Sociodemographic and clinical data were assessed through electronic medical number increased to 81.9% (n = 181) after BMI-adjustments.
records, and it included sex, age, the presence of comorbidities such as systemic Females exhibited significantly lower values of BMI-adjusted CC
arterial hypertension (SAH), type 2 diabetes mellitus (DM2), and clinical diagnoses.
For analytical purposes, the clinical diagnosis was categorized into malignancies,
values. Table 1 provides more descriptive details of our population.
cardiological, and other health conditions. Study participants were monitored Excluding patients who had prior (non-adjusted) low CC
throughout their hospitalization and after discharge, using clinical records to (n = 75), a total of 72.1% (n = 106) were reclassified from a normal
assess prolonged LOS and mortality, our outcome measures. Prolonged LOS was CC category to a low CC category following BMI adjustment. Only
defined as greater than 7 days according to the median of population distribution.
27.9% (n = 41) maintained a normal CC classification. Figure 2 dis-
Anthropometric assessment
plays a flowchart following BMI-CC adjustments.
When comparing patients following BMI adjustments, those
Weight (kg) and height (m) were measured to calculate the BMI (kg/m2), clas- who presented with low CC prior to adjustment were older and
sified according to World Health Organization (WHO - 1995) criteria [22]. CC was had lower BMI values (P < 0.001). In contrast, patients with low CC
measured using an inelastic measuring tape at the largest part of the calf (i.e., max-
after adjustment exhibited higher BMI values but still had lower
imum circumference). Patients were positioned in a standardized manner, seated
with both knees and ankles bent at a 90-degree angle to the floor. Measurements CC and BMI-adjusted CC compared to those who maintained nor-
were consistently taken on the right side. In cases where mild edema was present, mal values (P < 0.001). Significant differences in mortality were

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Fig. 1. Study flowchart. BMI: body mass index; CC: calf circumference.

observed between the groups (P = 0.006), with a moderate ES asso- older hospitalized patients with excess weight. Our main results
ciation (Cramer’s V of 0.22). Patients with low CC prior to adjust- demonstrated that BMI-adjusted CC was independently associated
ment had significantly higher mortality rates (24%). Among those with mortality, but not with prolonged LOS. These findings high-
with low CC after BMI adjustment, the mortality rate was more light the importance of CC as a simple and significant prognostic
than twice as high compared to patients who maintained a normal marker. Additionally, BMI-adjusted CC can be used as an adequate
CC (10.4% vs. 4.9%) (Table 2). proxy in older patients with excess weight without compromising
Cox regression analysis did not reveal an association between its prognostic significance.
CC and prolonged LOS, even after BMI adjustments, neither in Our findings are different from those by Souza et al [24]. While
crude nor adjusted models. However, BMI-adjusted CC was they did not find a link between BMI-adjusted CC and mortality,
inversely associated with mortality. Each centimeter increase in and showed such association with LOS, it is important to highlight
BMI-adjusted CC, corresponded to a decrease in the hazard for the differences between our studies. Souza et al [24] investigated a
mortality. In contrast, each centimeter decrease in BMI-adjusted diverse hospital population, including individuals across various
CC was associated with an  19% increase in the relative hazard for body mass ranges and age groups. Moreover, their evaluation con-
mortality (1/HR: 1.19). This association remained significant even sidered outcomes up to 6 months, which was shorter than ours.
after adjusting for potential confounders such as age, sex, clinical Additionally, our research was solely focused on older patients
diagnoses, and comorbidities (HR adjusted 0.84, 95% CI 0.73 to 0.95) with excess weight, and we were particularly interested in assess-
(Table 3). ing the relevance of the BMI-adjustment for predicting clinical out-
comes.
Discussion Notably, patients reclassified as having low CC after BMI adjust-
ment had higher BMI values compared to those who did not
To the best of our knowledge, this is the first study to assess the change categories. This finding is particularly interesting, suggest-
association between BMI-adjusted CC and clinical outcomes among ing that patients with more excess weight might have a lower

Table 1
Characteristics of hospitalized older patients (N = 222)

Variables Total Males Females P

N, % 222 114 (51.4) 108 (48.6)

Age (years) 67 (63;72) 67 (63;72) 68 (63.3;72.8) 0.64*
BMI (kg/m2) 28.6 (26.8;31.6) 28.4 (26.7;31.2) 28.8 (26.9;32.5) 0.36*
Systemic arterial hypertension 183 (82.4) 88 (77.2) 95 (88.0) 0.035y
Type 2 diabetes mellitus 111 (50.0) 53 (46.5) 58 (53.7) 0.28y
Diagnoses 0.92y
Oncological 56 (25.2) 30 (26.3) 26 (24.1)
Cardiological 76 (34.2) 39 (34.2) 37 (34.3)
Othersz 90 (40.6) 45 (39.5) 45 (41.7)
CC (cm) 36 (33;38) 36 (34;39) 34 (32;37) <0.001*
BMI-adjusted CC (cm) 31 (29;33) 32 (30;34) 30 (28;32) <0.001*
Low CC 75 (33.8) 33 (28.9) 42 (38.9) 0.13y
Low BMI-adjusted CC 181 (81.5) 87 (76.3) 94 (87.0) 0.040y
Length of stay 7 (3;14) 7 (3.8;13) 8 (3;16) 0.40a
Mortality 31 (14.0) 18 (15.8) 13 (12.0) 0.42y
BMI, body mass index; CC, calf circumference.
*Mann-U-Whitney test (median and interquartile ranges).
y
Pearson’s x2 (Frequencies, N %).
z
Diagnoses for elective surgeries (hernia, cholelithiasis), as well as infectious, parasitic, neurological, and rheumatological diseases.

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4 J.P.d. Costa Pereira et al. / Nutrition 125 (2024) 112505

Fig. 2. Frequency of low calf circumference following BMI-adjustments. BMI: body mass index; CC: calf circumference.

muscle mass. Furthermore, patients with low CC prior to adjust- Prior research contributes to the discussion on the impact of
ment had significantly higher mortality rates. This suggests that different weight phenotypes on CC. For instance, individuals carry-
these patients may have had severely compromised muscle mass, ing excess body weight may present with higher intramuscular fat
which was not masked by excess weight and could be a marker of infiltration, reducing CC’s ability to accurately estimate muscle
severity. In fact, they had lower CC/BMI values compared to those mass [27
29]. Considering CC’s use in various assessment tools
reclassified as having low CC after BMI adjustments. When exam- like sarcopenia screening (SARC-CalF) [30] and the mini-nutritional
ining absolute values, the proportion of patients who were reclas- assessment [31], we advocate for the adoption of BMI adjustment
sified as having a low CC exhibited a mortality rate more than [32]. This is crucial because these tools are instrumental in diag-
5 times higher than that of the group with a normal CC after BMI nosing nutritional issues and predicting adverse outcomes in
adjustment. However, it is also important to note that unadjusted diverse clinical populations [33
38], and without adjustments,
CC is commonly used as a marker of muscle mass [11,25,26]. This nearly no subjects who have overweight or obesity would be clas-
underscores the importance of BMI adjustment to attain a more sified as at risk based on CC measures.
accurate estimation of muscle status using CC, facilitating early Our study has some limitations that warrant acknowledgment.
detection of catabolic states, especially in older patients. The relatively small sample size, convenience sampling, and broad

Table 2
Comparative analysis between hospitalized older patients with low calf circumference following BMI adjustments (N = 222).

Variables Low CC prior BMI adjustment Low CC after BMI adjustment Normal CC after BMI adjustment P

N, % 75 (33.8) 106 (47.7) 41 (18.5)

Age (years) 69 (66;76) 66 (63;71) 66 (62;68) <0.001*
Sex 0.08y
Males 33 (44.0) 54 (50.9) 27 (65.9)
Females 42 (56.0) 52 (49.1) 14 (34.1)
BMI (kg/m2) 27.5 (26.4;28.7) 30.6 (27.8;33.7) 28.6 (26.9;29.8) <0.001*
Systemic arterial hypertension 61 (81.3) 90 (84.9) 32 (78.0) 0.59y
Type 2 diabetes mellitus 39 (52.0) 56 (52.8) 16 (39.0) 0.29y
Diagnoses 0.31y
Oncological 23 (30.7) 24 (22.6) 9 (22.0)
Cardiological 22 (29.3) 35 (33.0) 19 (46.3)
Othersx 30 (40.0) 47 (44.3) 13 (31.7)
CC (cm) 32 (31;33) 36 (35;38) 40 (38;41) <0.001*
BMI-adjusted CC (cm) 29 (27;30) 32 (30;33) 36 (35;37) <0.001*
Prolonged length of stay 38 (50.7) 38 (35.8) 19 (46.3) 0.12y
Mortality 18 (24.0) 11 (10.4) 2 (4.9) 0.006z
*Kruskal-Wallis (median and interquartile ranges).
y
Pearson’s x2 test (Frequencies, N %).
z
Likelihood ratio x2 (Frequencies, N %).
BMI, body mass index; CC, calf circumference.
x
Diagnoses for elective surgeries (hernia, cholelithiasis), as well as infectious, parasitic, neurological, and rheumatological diseases.

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 J.P.d. Costa Pereira et al. / Nutrition 125 (2024) 112505 5

Table 3 with Prodiet Clinical Nutrition that includes: funding grants. Carla
Cox regression analyses: Associations between BMI-adjusted calf circumference and M Prado reports a relationship with Abbott Nutrition that includes:
clinical outcomes of hospitalized older patients. consulting or advisory. Carla M Prado reports a relationship with
Variables HR (95% CI) P Danone Nutricia Research that includes: consulting or advisory.
Carla M Prado reports a relationship with Nestle Health Science
Prolonged LOS
that includes: consulting or advisory. Carla M Prado reports a rela-
Unadjusted CC 1.02 (0.97-1.08) 0.40 tionship with Pfizer that includes: consulting or advisory. Carla M
BMI-adjusted CC 1.04 (0.98-1.10) 0.13
Prado reports a relationship with AMRA Medical that includes:
Adjusted model* 1.02 (0.95-1.10) 0.55
consulting or advisory. Maria Cristina Gonzalez reports a relation-
Overall mortality ship with Abbott Nutrition that includes: consulting or advisory.
Unadjusted CC 0.85 (0.76-0.94) 0.002 Maria Cristina Gonzalez reports a relationship with Danone Nutri-
BMI-adjusted CC 0.88 (0.78-0.98) 0.031 cia Research that includes: consulting or advisory. Maria Cristina
Adjusted model* 0.84 (0.73-0.95) 0.010 Gonzalez reports a relationship with Nestle Health Science that
95% CI, 95% confidence interval; BMI, body mass index; CC:, calf circumference; HR, includes: consulting or advisory. If there are other authors, they
hazard ratio; LOS, length of hospital stay (prolonged if > 7 days). declare that they have no known competing financial interests or
*Models with BMI-adjusted CC were adjusted for age, sex, clinical diagnoses, and
personal relationships that could have appeared to influence the
comorbidities.
work reported in this paper.
range of diagnoses might not represent the entire spectrum and
may limit the generalizability of our findings. Nevertheless, we CRediT authorship contribution statement
acknowledge that this reflects the reality in hospitals for older
patients who require hospitalization. Despite being somewhat Jarson Pedro da Costa Pereira: Writing
original draft, Meth-
informed by our post hoc sample size calculation, this approach odology, Investigation, Formal analysis, Conceptualization. Maria
presents additional limitations that could potentially skew our find- Cristina Gonzalez: Writing
review & editing, Formal analysis.
ings. However, this study constitutes a secondary analysis, thereby Carla M. Prado: Writing
review & editing, Methodology. Poliana
precluding prior sample size calculations. Relying solely on elec- Coelho Cabral: Writing
review & editing, Supervision. Tais Gal-
tronic medical records to assess outcomes is also a significant limita- dencio do Nascimento: Investigation, Conceptualization. Maria
tion, as it may lead to underestimation of the outcome of interest. Karolainy do Nascimento: Methodology, Investigation. Alcides da
Due to sample size constraints, conducting more stratified Silva Diniz: Writing
review & editing, Formal analysis. Claudia
time-event analyses for survival was not feasible. Additionally, our Porto Sabino Pinho Ramiro: Writing
review & editing, Supervi-
regression models may not have accounted for all potential con- sion, Resources, Project administration. Ana Paula Trussardi Fayh:
founding factors that could influence these outcomes such as die- Writing
review & editing, Methodology, Formal analysis,
tary consumption and treatments. Future research should focus on Conceptualization.
securing larger, more representative samples, particular among
patients with excess weight, to enhance our understand of BMI- Availability of data and materials
adjusted CC’s prognostic value in hospitalized patients. These stud-
ies should also consider exploring the relationship between BMI- The data described in the manuscript will be made available by
adjusted CC and other clinically relevant secondary outcomes, the corresponding author upon reasonable request.
such as infections, sepsis, and surgical complications.
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