OBJECTIVE: to analyze the use of the Adductor Pollicis Muscle Thickness (APMT) as an anthropometric parameter and prognostic indicator in hospitalized or ambulatory patients. METHOD: systematic review carried out the Web of Science, SCOPUS and Lilacs databases. RESULTS: Twenty-three studies were performed on critical, surgical, oncological, nephropathic and hepatopathic patients, collecting data on bibliographic reference, study site, objectives, number of patients, age group, methodology, main results and conclusion. APMT proved to be a good anthropometric parameter for evaluation of nutritional status in critical patients without edema, and surgical, oncological and nephropathic patients, but presented poor performance for diagnosis of malnutrition in hepatopathic patients. It was a good prognostic indicator for mortality in critical, nephropathic and oncological patients, and also a good predictor of hospitalization in nephropathic patients. There was an association with neurological complications in Hepatic Encephalopathy (HE) in the case of hepatophatic patients, but it was not a predictor of postoperative complications in surgical patients. CONCLUSION: APTM was considered a good anthropometric parameter in most clinical conditions, except in patients with liver disease and a good prognostic indicator for mortality in critical, oncological and nephropathic patients, and a predictor of neurological complications in HE. Further prognostic investigation, standardization of cutoff points and evaluation of sensitivity and specificity are required.
OBJECTIVE: to analyze the use of the Adductor Pollicis Muscle Thickness (APMT) as an anthropometric parameter and prognostic indicator in hospitalized or ambulatory patients. METHOD: systematic review carried out the Web of Science, SCOPUS and Lilacs databases. RESULTS: Twenty-three studies were performed on critical, surgical, oncological, nephropathic and hepatopathicpatients, collecting data on bibliographic reference, study site, objectives, number of patients, age group, methodology, main results and conclusion. APMT proved to be a good anthropometric parameter for evaluation of nutritional status in critical patients without edema, and surgical, oncological and nephropathicpatients, but presented poor performance for diagnosis of malnutrition in hepatopathicpatients. It was a good prognostic indicator for mortality in critical, nephropathic and oncological patients, and also a good predictor of hospitalization in nephropathicpatients. There was an association with neurological complications in Hepatic Encephalopathy (HE) in the case of hepatophatic patients, but it was not a predictor of postoperative complications in surgical patients. CONCLUSION: APTM was considered a good anthropometric parameter in most clinical conditions, except in patients with liver disease and a good prognostic indicator for mortality in critical, oncological and nephropathicpatients, and a predictor of neurological complications in HE. Further prognostic investigation, standardization of cutoff points and evaluation of sensitivity and specificity are required.
Due to the limited use of sophisticated equipment for analysis of body composition in
the clinical practice, for the high costs and the experience required in such
procedures, anthropometric and laboratory parameters are still used for the
nutritional assessment of hospitalized patients
. Thus, new assessement methods are needed within the hospital environment,
particularly those that are simple, relatively non-invasive, and that have high
sensitivity and preserved specificity
.In this context, a new assessment technique of the muscle compartment called Adductor
Pollicis Muscle Thickness (APMT) was introduced in 2004 and it has been used to
diagnose muscle loss and consequently, malnutrition
,
. The incidence of malnutrition lies between 20 and 69% in hospitalized
patients, being higher in critical cases and nutritional levels
,
that lead to increased muscle fatigue, loss of contraction force and
relaxation rate of the adductor pollicis muscle (APM)
,
.The opposition of the thumb is present in several activities of the daily life of
humans. Since the APM is also consumed during catabolism and weakened when in
disuse, its trophic condition can reflect the routine of an individual
. This muscle can indicate changes in the muscle composition of the whole
body, including early changes arising from both malnutrition and recovery of
nutritional status
,
.The technique to measure the APM was developed and published in 2004 and described as
follows: the subject should be seated, with the right hand (RH) on the knee and the
elbow flexed at an angle of 90 degrees above the homolateral lower limb. The
adipometer indicated by the researchers is the Lange®, which should be used with a
continuous pressure of 10g/mm². The evaluator pinches the adductor muscle located at
the vertex of the imaginary triangle formed between the extension of the thumb and
the index finger. This should be performed in triplicate to obtain a mean APM value.
The reference values determined by the author serve to classify the degree of
muscle loss in healthy individuals
.The accuracy and reliability of anthropometric measures are influenced by many
variables, such as: equipment, technical ability, cooperation of the individual, and
variety of reference standards
. However, this new technique has many advantages; the APM is a muscle almost
devoid of adipose tissue, flat, with a well-defined anatomic point, being the only
one that allows the direct measurement of its thickness without need for
calculations, and prone to quick, simple, non-invasive, low-cost measurement, easily
reproducible by other researchers in both ambulatory and bedridden patients
,
,
,
. Thus, the objective of this study is to perform a systematic review on the
use of APMT as an anthropometric parameter and prognostic indicator in hospitalized
or ambulatory patients, when compared to other methods of assessment of nutritional
status.
Methods
The following strategy was used for selection of descriptors and formulation of the
guiding question of the systematic review. The group of patients named as “P”
included hospitalized or ambulatory patients; the intervention “I” consisted in the
application of the APMT; the comparison methods “C” were anthropometric and
prognostic; and the expected outcome “O” was a good correlation between the
evaluated variables. The guiding question of the research is: “Is the APMT a good
anthropometric method and prognostic indicator compared to other methods used to
evaluate nutritional status in hospitalized or ambulatory patients?” The following
Health Sciences Descriptors were used (DeCS) to search scientific articles:
“Hospitalização” OR “Avaliação nutricional” OR “Antropometria” OR “Prognóstico” OR
“Desnutrição” OR “Ambulatório Hospitalar” combined with the term “Músculo adutor do
polegar”, which is not indexed in DeCS, and its English and Spanish translations
“Hospitalization”, “Hospitalización”, “Nutritional Assessment”, “Evaluación
nutricional”, “Anthropometry”, “Antropometría”, “Prognosis”, “Pronosis”
“Malnutrition”, “Desnutrición”, “Servicio Ambulatorio en Hospital”; “Hospital
Outpatient Clinics”, “Adductor pollicis muscle” and “Músculo aductor del
pulgar”.The electronic databases used in the search for articles that are part of the
systematic review of the scientific literature were the Web of Science (Thomsons
Reuters), Scopus platform, and Latin American and Caribbean Literature in Health
Sciences (Lilacs). The research and selection of articles were carried out by only
one of the authors. Only articles duplicated in the databases were initially
excluded. Then, eligibility criteria were adopted for the selection process, which
began with the inclusion of studies that had applied the method of assessment of the
APMT in hospitalized or ambulatory patients. After this step, titles and abstracts
were read to select the texts that included the clinical conditions for the study
presented in more than one article (critical, surgical, oncologic, nephropathic and
hepathopatic patients), excluding articles with healthy patients, institutionalized
elderly, hospitalized patients without pathological specifications, and patients
with pathologies presented in only one article.A thorough reading of the selected studies was performed and the following data were
collected: bibliographic reference, study site, objectives, number of evaluated
patients, age range, methodology, main results and conclusion. These data were
organized according to the clinical conditions abovementioned and later discussed
along with the other important considerations reported in the researches. Full texts
of articles of which only the abstract and title available were requested from the
Federal University of Grande Dourados library, and those that were not found were
excluded due to the inaccessibility to the statistical results. The last selection
process excluded complete studies for the following reasons: insufficient results
and lack of comparison with anthropometric variables and prognostic indicators.The anthropometric variables considered for comparison were body mass index (BMI),
arm circumference (AC), arm muscle circumference (AMC), total arm area (TAA), arm
muscle area (AMA), calf circumference (CC), triceps skinfold (TS), percentage weight
loss, hand grip strength (HGS), electrical bioimpedance (EBI) [resistance,
reactance, percentage of cell mass and phase angle (FA)] and Dual Energy X-ray
Absorptiometry (DEXA). The variables considered with prognostic value for comparison
were the Global Subjective Assessment (GSA), Sequential Organ Failure Assessment
(SOFA), Glasgow prognostic score, length of hospital stay, days of mechanical
ventilation, mortality, complications in the postoperative period (PP), risk of
hospitalization, severity of the disease, serum albumin, serum creatinine and
hemoglobin.
Results
Two hundred and twenty nine articles were initially searched, of which 165 were
repeated and 64 were accessed. After the first selection by the criterion described
in the methodology, 36 articles remained. The second selection (reading of the
titles, abstracts and choice of articles of interest for research) resulted in 25
articles and the last step resulted in the final selection of 23 articles, 13 from
the Web of Science, 6 from the Scopus Platform and 4 from the Lilacs. The studies
included in the study were divided into five groups according to the following
clinical conditions: critical (N = four), surgical (N = eight), hepathopatic (N =
five), oncological (N = three) and nephropathic (N = three) patients. Steps for
selection of articles are described in the Figure
1.
Figure 1
Steps for selection of articles
The following are the main results found in the studies conducted with critical
patients and that evaluated APMT in both hands.The first study was conducted in Cuiabá (MS) in 2012 and found that abnormal APMT
(values below those found by other researchers) was associated with higher
mortality (p = 0.03) and significantly correlated with the GSA outcomes for severe
malnutrition (p < 0.001). Only patients without edema had a significant
association between APMT measurement and length of hospital stay [APMT of RH without
edema (β = -0.32, p = 0.03) and left hand without edema (β = -0.36, p = 0.02)]. It
was also observed that patients with abnormal APMT values had stayed in the
intensive care unit (ICU) for approximately five days. There was no correlation
between APMT and the number of days of mechanical ventilation. The values found
were above those found in other studies, being higher in the RH, what the author
considered to be due to the presence of edema in the hands
.In 2015, a study carried out in Porto Alegre (RS) verified the accuracy of APMT by
evaluating the Receiver Operating Characteristics (ROC) with the
GSA (area under the curve regarding the RH of 0.82 and 95% confidence interval of
0.73 to 0.91). The study also related measures of less than 6.5 cm to higher
nutritional risk in the GSA (moderately and severely malnourished). APMT of both
hands was correlated with the BMI (p < 0.05 and r = 0.45) and CC (p < 0.05 r =
0.58); but not with length of hospital stay (p = 0.411) and mortality (p = 0.519).
The study population consisted of 73.5% of elderly participants, which explains the
low values found
.A study carried out in Asia in 2015 observed a significant difference in APMT
measurements between races and genders (p < 0.05). No significant correlation was
found with mortality at 28 days, hospital outcome, and ICU length of stay (p >
0.05). However, there was a significant and moderate correlation with AC and BMI (p
< 0.05), and APMT values were higher when compared to other Brazilian
studies
. A study conducted in Iran found a strong correlation between APMT of both
hands and all anthropometric variables evaluated, namely, TS, AC, AMC, ATB and AMA
(p <0.0001), as well as serum albumin (r = 0.61, p = 0.001). The measures of the
dominant hand (DH) presented positive correlation with ICU length of stay (r = -0.4,
p < 0.001) and the highest correlation with mortality (odds ratio 3.8, 95%
confidence interval, 1.2 to 5.2, p < 0.01). A significant correlation was also
found between the dominant APMT and the SOFA score for organ failure (r = -0.86, p
< 0.001)
.Other studies evaluated surgical patients, three of which were performed with
gastrointestinal (GIT) surgery patients, and the others with patients recovering
from major surgeries and elective procedures.In a research conducted in Rio de Janeiro (RJ) in 2005, APMT showed a significant
correlation with septic complications in the PP in the case of patients with APMT
values lower than 6.5 mm (p = 0.007), as well as correlation with mechanical
ventilation time (p = 0.000), ICU length of stay (p = 0.026), and significant
tendency for hospital admission (p = 0.053). However, there was no significant
association with non-septic PP complications (area under the ROC curve of 0.562
and p = 0.305) and mortality (area under the ROC curve of 0.641 and p =
0.217)
.In the study carried out in Cuiabá (MT) in 2009, APMT was significantly correlated (p
< 0.05) with all the anthropometric variables evaluated (BMI, AMC, AC, TS and
percentage of weight loss) and had a good correlation with GSA values (p <0.05),
considered gold standard. In addition, it presented good sensitivity (72.37% for
APMT of the DH and 77.33% for that of NDH) and 100% of specificity in both hands.
The cutoff point for malnutrition was determined by the ROC curve, with 13.4 mm for
the DH and 13.1 mm for the NDH. In the most recent study in 2011, there was an
association between APMT and HGS (DH p < 0.001; NDH p < 0.001) and mortality
(p < 0.05). However, there was no significant association with length of
hospitalization and complications in the PP (data not shown)
,
.In a more recent study (2014) conducted in the same city, APMT did not show a good
association with the percentage of weight loss (p = 0.113), AMC (p = 0.806) and AMAc
(p = 0.770), but correlated significantly with AC (p = 0.003), TS (p = 0.000) and
BMI (p = 0.000). APMT was also associated with gender and age, as there was a high
prevalence of malnutrition in women and the elderly. The values found in the DH
were higher, suggesting a more rapid atrophy of this musculature in case of
inactivity resulting from malnutrition
.Study conducted in Pelotas (RS) published in 2015 identified an association and a
significant linear trend between APMT values and GSA categories (p < 0.001). It
also found a strong association between APMT results for muscle mass depletion and
GSA for malnutrition (p < 0.001). In this study, APMT showed low sensitivity (DH
34.9% and NDH 37.7%), and high specificity (greater than 90%) for predicting
malnutrition
.In the results of a research carried out in Vitória (ES) in 2016, APMT showed to be
correlated with BMI, AMC, AMAc, CC (p < 0.01) and GSA (p = 0.026), with AMC (p =
0.036) as the variable that most influenced APMT values
. In a study carried out in the city of Salvador (BA) in the year of 2016,
APMT did not present a significant association with the presence of complications in
the PP in either hand (DH p = 0.217 and NDH p = 0.148). However, the APMT of the NDH
was significantly associated with specific infectious complications (p = 0.030)
. In another study conducted in the same year in Recife (PE), APMT was
compared to the gold-standard GSA method, but did not present a significant
association (DH p = 0.513 and NDH p = 0.842)
).Data regarding the objectives, number of patients and age group, objective and
subjective evaluations used for comparison with APMT and conclusion of the studies
performed in surgical patients are described in the Figure 3.
Figure 3
Characteristics of studies performed in surgical patients
Other studies were performed with oncological and nephropathicpatients, being the
first of them performed in 2012 in the city of Porto Alegre (RS), with cancerpatients. The APMT values found in this study were associated with mortality (p
< 0.001), however there was no association with length of hospital stay (DH p =
0.42 and NDH p = 0.43)
. Two studies carried out in Belo Horizonte (MG) in the year 2013 found the
same result for APMT, which presented a significant difference between nourished and
malnourished patients (p < 0.05), but a low agreement with the GSA (ƙ < 0.20);
only one study had no association with the Glasgow prognostic score (p >
0.05)
,
.The next group includes nephropathicpatients with Chronic Kidney Disease (CKD)
undergoing dialysis and is described below. The study carried out in Fortaleza (CE)
in the year 2012 followed patients for 12 months and found a significant difference
and positive correlation between APMT and BMI (r = 0.37; p 0.0001), AC (r = 0.437; p
< 0.0001), AMC (r = 0.494; p < 0.0001), AMA (r = 0.449; p < 0.0001),
percentage of weight adequacy (r = 0.355; p = 0.000), creatinine (r = 0.230; p =
0.006), albumin (r = 0.207; p = 0.013), percentage of body cell mass (r = 0.293;
p=0.000) and FA (r = 0.402; p < 0.0001), and negative correlation with resistance
measured by EBI (r = 20.403; p < 0.0001). However, no significant association was
found with age, dialysis time, TS, hemoglobin, and reactance. Higher risks of
hospitalization within six months and mortality were associated with lower APMT
values
.A study carried out in São Paulo (SP) in the year of 2013 found APMT to be positively
correlated with HGS (p < 0.05), serum albumin (p = 0.07), percentage of body cell
mass (p < 0.05), reactance (p < 0.05) and FA (p < 0.05). However, APMT was
not correlated with serum creatinine (p = 0.08), GSA (p = 0.55) and the
anthropometric measures BMI (p = 0.64), AC (p = 0.62), AMC (p = 0.70) and AMA (p =
0.89)
. In 2014, in a study performed in a reference hospital in Rio Grande do Sul,
APMT was associated with BMI (p = 0.001), where higher values were more prevalent
in overweight individuals and the lowest values in those with low weight
. The objectives, number of patients and age group, objective and subjective
evaluations used for comparison with APMT and completion of the work with
oncological and nephropathicpatients are described in the Figure 4.
Figure 4
Characteristics of the studies performed in oncological and
nephropathic patients.
The last group of studies described was performed in nephropathic, mostly ambulatory,
patients and conducted in the city of Porto Alegre. The first study was published in
2012 with ambulatory cirrhosispatients and found a low percentage of malnutrition
(14.3%) according to APMT measurement when compared to the HGS, TS, AC and AMC
methods. APMT was not associated with disease severity and showed poor agreement
with HGS methods [Kappa index (ƙ) = 0.12] and ASG (ƙ = 0.25)
. Another study found APMT to be significantly associated only with disease
severity (p < 0.05), but also showed a low prevalence of malnutrition, a weak
association with GSA (ƙ = 0.222) and no association with the diagnosis of
malnutrition and inadequate dietary intake
. Two studies conducted in 2015 and 2016 with non-cirrhotic hepatitis Cpatients and patients before and after hepatic transplantation, respectively, did
not identify any individuals with malnutrition and, therefore, APMT presented poor
performance
,
.In the year 2016, a study conducted in the city of Botucatu (SP) in cirrhotic
patients with Hepatic Encephalopathy (HE) related APMT to disease severity, so that
the reduction of 1 mm in the measurement was associated with an increase of 30.7% in
the degree of HE (p = 0.0177). The lower values were related to lower states of
mental acuity, since measures lower than the cutoff point (6.5mm) were associated
with the degrees I and II of HE (p = 0.013)
.Data regarding the objectives, number of patients and age group, objective and
subjective evaluations used for comparison with APMT, as well as the conclusion of
the studies performed in hepatopathic patients are described in the Figure 5.
Figure 5
Characteristics of the studies performed in hepatopathic
patients
Discussion
APMT showed to be a good anthropometric parameter in critically illpatients without
edema
-
, which may be justified by the greater expression of critical and acute
conditions in the ICU, protein depletion and muscle loss caused by both the decrease
in daily activities and the hypercatabolic status of these patients
. APMT was also considered a good prognostic indicator for mortality in this
group
,
, being efficient even in patients with hand edema in one of the studies
, although it was not considered as a good prognosis for ICU length of
stay
-
. Perhaps, this may be explained by the fact that APMT evaluates the lean
mass and whose preservation is an indication of good evolution in such patients,
since malnutrition contributes to increased mortality
. No justification was reported as to the usefulness as a good indicator for
the ICU length of stay, but we believe that other clinical conditions are more
determinant for the hospital stay.The limitations found in the studies included in this review were the interdiction of
the adductor pollicis muscle area, and especially the presence of edema that
diminishes the accuracy of the APMT measurement and, therefore, led to the exclusion
of many patients, compromising the application of this measure in the practice.
Thus, the researchers suggest that this measure must becarefully evaluated and
applied before the onset of edema, ideally on the first day of ICU admission and
analyzed in conjunction with the other anthropometric and GSA methods
,
. The combination of several tools may be more efficient to detect
abnormality in the body composition of these patients
.In the group of individuals submitted to surgeries, APMT also proved to be a good
method for nutritional evaluation and diagnosis of malnutrition, but it was not
considered a good prognostic factor for the prevalence of complications in the PP.
Malnutrition in these patients is associated with surgical stress, as this procedure
promotes the release of catabolic hormones that cause the degradation of muscle
proteins, which is aggravated according to the nutritional deficit of the
patient
. Thus, the potential detection of malnutrition can be justified by the good
specificity of APMT verified in the studies, a characteristic that indicates a low
rate of false positive results
,
. Furthermore, there is a correlation of APMT with anthropometric measures
that happens due to the similar nature of the measures
. As for the non-association with PP complications, it is assumed that this
result comes from the variability of this condition in function of the underlying
disease severity and nutritional status prior to surgery.In the evaluation of cancerpatients, APMT was considered a good parameter for
classification of nutritional status, but had low association with GSA
,
. This finding was indicated by the fact that GSA detected early functional
alterations, while APMT detected malnutrition and changes in body composition only
in later instance
,
. Only one study evaluated APMT as a prognostic indicator and found it to be
a good parameter of mortality, resulting from its high discriminative power
.With regard to nephropathicpatients, APMT was also considered a good method of
nutritional assessment compared to anthropometric parameters
,
and a good predictor of hospitalization and mortality in the only study that
evaluated its prognostic indication
, but the number of studies with this group is still small
,
. This outcome is based on the peculiarities of CKDpatients, namely, reduced
food intake and metabolic acidosis combined with uremia, factors that lead to
protein catabolism
, which along with physical inactivity, further aggravates the disease
. Furthermore, malnutrition is per se a risk factor for death in hemodialysis
patients
.However, studies evaluating hepatopathic patients revealed poor performance of APMT
in the diagnosis of malnutrition, and only one showed an association with
neurological complications in HE. Two studies differed in relation to the severity
of the disease. Non-association of APMT with malnutrition can be explained by fluid
retention
, low sensitivity demonstrated by the method
and anatomical muscle alteration that follows functional changes
.An association of APMT with HE complications and disease severity was observed, most
likely explained by the marked depletion of arm muscle experienced by cirrhotic
patients
. The study in which there was no association with disease severity was
justified by the low number of patients in the severe stage
.GSA is present in almost half of the studies comparing different measures with APMT
results. GSA is set as the gold standard by the American Society of Parenteral and
Enteral Nutrition (ASPEN) for evaluation of hospitalized patients, and it is
frequently used for validation of new methods
,
. GSA evaluates the nutritional status as a whole, including anthropometric,
clinical, physical, metabolic and dietary data, identifying suspected or established
malnutrition before changes in body composition. Thus, GSA presents the best
prediction for arising complications; however, its efficacy depends on the ability
of the evaluator to detect significant nutritional changes. This have led to the
need to study new, simpler and less invasive methods to speed up the nutritional
screening process
,
,
,
.Among the ten studies comparing GSA with APMT, seven found a positive association
between them and only three did not find association. Among the groups where
association was detected are the surgical
,
,
, critical
,
and oncological
,
patients, and those where association was absent were studies with
surgical
, nephropathic
and hepatopathic
patients.Studies with healthy individuals were excluded from this review because they aimed to
establish reference values for this population
,
, and the research with institutionalized elderly people analyzed their
nutritional profile, but not its effectiveness compared to other methods. It is
important to emphasize that in the latter group, all patients presented values
within the normal range for healthy people and more studies are therefore
necessary for the purpose of comparison
.The greatest limitation observed in this review regarding the evaluation of APMT
measurement was the absence of reference standards for the different clinical
conditions, according to gender and age group. The values often referred to in the
studies come from healthy populations or are defined based on a single cutoff point,
and consequently may underestimate malnutrition in adults and in men, and
overestimate it in the elderly and women
. Another limitation found in the researched literature was the use of
different adipometers and the standardization of the technique itself, which may
have led to very different APMT values, besides the variability stemming from
different evaluators
,
.Minimum and maximum mean APMT values (mm) were, respectively, 7.03 ± 2.71 (LH) and
20.4 ± 6 (RH) in critically illpatients
-
; 12.0 ± 3.6 (NDH) and 12.9 ± 3.5 (DH) in cancerpatients
; 10 ± 4.5 (BH) and 11.9 ± 3.07 (BH) in nephropathicpatients
-
; 9.54 ± 2.5 (BH) and 16.98 ± 2.80 (RH) in surgical patients
,
,
,
); and 16.6±3.5 and a median of 7.1 in hepatopathic patients
,
. However, these data refer to only 14 studies that provided such values.
Yet, it is interesting to note that the lowest APMT values were found in a study
with critical patients (7.03 ± 2.71 in the left hand)
and in hepatopathic patients (median of 7.1 mm in both hands)
.Thus, it is necessary to determine specific cutoff points for pathologies or groups
of individuals and carefully interpret the results. It is also necessary to assess
the actual sensitivity and specificity of APMT. In this sense, sensitivity is a
parameter that evaluates the probability of the result to be positive, and
specificity analyzes the probability of that same result to be negative
.
Conclusion
APMT was considered a good anthropometric parameter in the great majority of clinical
conditions evaluated, except in patients with liver disease, and presented low
sensitivity and high specificity. It was also indicated as a good prognostic
indicator for mortality in critical, oncological and renal patients, and as a
predictor of neurological complications in hepatic encephalopathy. However, further
investigation of its prognostic usefulness in other clinical conditions,
standardization of cutoff points for reference in the measurement classification and
assessment of sensitivity and specificity is required.
Authors: Rosalia Bragagnolo; Fernanda Stephan Caporossi; Diana Borges Dock-Nascimento; José Eduardo de Aguilar-Nascimento Journal: Rev Col Bras Cir Date: 2009-10
Authors: Jacqueline Braga da Silva; Sílvia Fernandes Maurício; Tatiana Bering; Maria Isabel T D Correia Journal: Nutr Cancer Date: 2013 Impact factor: 2.900
Authors: Aline Kirjner Poziomyck; Antonio Carlos Weston; Edson Braga Lameu; Ornella Sari Cassol; Luisa Jussara Coelho; Luis Fernando Moreira Journal: Nutr Cancer Date: 2012 Impact factor: 2.900