Public Health 189 (2020) 110e114

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Original Research

Association between type 2 diabetes and non-exercise estimated

cardiorespiratory fitness among adults: evidences from a middle-
income country
Geraldo A. Maranhao Neto a, d, *, Iberico Alves a, Eduardo Lattari a, Aldair Jose Oliveira b,
Sergio Machado a, Silvio Marques Neto a, Xuemei Sui c
a
Salgado de Oliveira University, Postgraduate Program in Physical Activity Sciences (PGCAF), Nitero
i, RJ, Brazil
b
Rural Federal University of Rio de Janeiro, Laboratory of Social Dimensions Applied to Physical Activity and Sport (LABSAFE), Department of Physical
Education and Sports, Serop
edica, Brazil
c
University of South Carolina, Department of Exercise Science, Division of Health Aspects of Physical Activity, Columbia, USA
d
Kardiovize Brno 2030, St. Anne's University Hospital Brno, International Clinical Research Center, Brno, Czech Republic

a r t i c l e i n f o a b s t r a c t

Article history: Objective: The objective of this study is to assess the association between type 2 diabetes (T2D) and
Received 21 April 2020 cardiorespiratory fitness (CRF) estimated through a non-exercise model in a large representative group of
Received in revised form Brazilian adults.
16 July 2020
Study design: The study design of this study is a cross-sectional population-based study.
Accepted 24 September 2020
Available online 16 November 2020
Methods: The presence of T2D was assessed through self-report in 42,631 individuals aged 20e59 years.
The CRF was predicted from a non-exercise equation containing the following data: sex, age, body mass
index, and physical activity level. The corresponding metabolic equivalent (MET) value was used to
Keywords:
Exercise capacity
classify participants into the following four groups based on the cutpoints: <6, 6e9, 10e11, and
12
Fitness METs. Crude and multivariable-adjusted logistic regressions were carried out to determine the associ-
Diabetes ation between CRF and the presence of diabetes.
Regression Results: Significant linear trends were observed in diabetes across different categories of CRF in men. In
Epidemiology women, however, linear trends were not observed in T2D across ‘10e11’ and ‘
12’ categories. A 1-MET
increase in estimated CRF was associated with 29% lower odds of diabetes in men and 14% in women
after adjusting all the potential confounders (P < 0.001).
Conclusions: The presence of T2D was inversely associated with every CRF level in men and with 6e9
METs when comparing with <6 METs in women, through a non-exercise model in Brazilian adults. This
finding suggests that a practical, viable, and low-cost measurement of CRF could be applied in lower
income countries to assess the relationship between CRF and T2D. However, new non-exercise models
are needed to better detect T2D in women.
© 2020 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.

Introduction 629 million by 2045.3 The literature identifies a number of

Diabetes is a chronic health condition which is associated with
disability, mortality, and higher healthcare costs.1 About 422
million people worldwide have diabetes, especially in low- and
middle-income countries.2 This number is projected to increase to
* Corresponding author. Salgado de Oliveira University, Postgraduate Program in
Physical Activity Sciences (PGCAF), 22061-021, Nitero
i, Rio de Janeiro, Brazil.
Tel.: þ55 21 2138 4942.
E-mail address: maranhaoneto@gmail.com (G.A. Maranhao Neto).
diabetes-related risk factors such as obesity, hypertension, hyper-
lipidemia, age, sex, race, and cardiorespiratory fitness (CRF).4,5
CRF is an important marker of cardiovascular health that pro-
vides a measure of the body's ability to deliver and use oxygen to
energy transfer to the muscles during physical activity and exer-
cise.6 Higher CRF seems to be associated with lower risk of devel-
oping type 2 diabetes (T2D).7,8 This relationship is mediated by
changes in body's tissue, such as reduced adiposity and increased
skeletal muscle.8 In addition, it directly increases insulin sensitivity
and glucose disposal.9 As an objective marker of people's habitual

https://doi.org/10.1016/j.puhe.2020.09.020
0033-3506/© 2020 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.

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G.A. Maranhao Neto, I. Alves, E. Lattari et al. Public Health 189 (2020) 110e114

physical activity, population data with CRF measurement are A continuous value in ml/kg/min was calculated based on the
limited due to the high costs for implementation and time spent on aforementioned equation. The MET values were calculated using
tests, especially in low- and middle-income countries. This omis- the standardized MET formula: MET ¼ VO2 (ml/kg/min)/3.5 (ml/kg/
sion characterizes a loss of relevant information on health status.10 min). The corresponding MET value was used to classify partici-
An important alternative to assess CRF would be through a pants into the following four groups based on the cutpoints from
prediction model without performing exercises. The method was Juraschek et al.5: <6, 6e9, 10e11, and
12 METs.
developed with the application of multiple regression equations
containing information related to CRF and shows good accuracy
and predictive ability.11 Although the association between CRF and
Data analysis
T2D is recognized, no report exists on this relationship in
population-based studies in a middle-income country such as
The statistical package Stata, version 12.1 (Stata Corp, College
Brazil. In the year 2045, the projected estimate for diabetes in Brazil
Station, USA), was used. Population characteristics are described by
is 26 million, ranking the country in the fifth place among countries
diabetes status and CRF groups. Sampling weights and complex
with the highest prevalence of diabetes.12 Application of non-
samples were considered using the ‘svy’ command and were applied
exercise CRF has been limited only to predict all-cause and car-
to all the following analyses. Continuous variables and categorical
diovascular mortality,13e16 non-fatal cardiovascular events,16 and
variables are expressed as mean standard deviation (SD) and num-
cognitive function.17 More application of non-exercise models to
ber (percentage), respectively. The Chi-squared, t-tests, and one-
predict other health outcomes such as diabetes is needed.
way analysis of variance (ANOVA) test, were used to test the differ-
The aim of this study is therefore to assess the association be-
ences between variables across diabetes status and CRF categories.
tween T2D and CRF estimated through a non-exercise model in a
Next, crude and multivariable-adjusted logistic regressions were
large representative group of Brazilian adults.
carried out to determine the association between CRF and the
presence of diabetes. Models were separated by sex. Model 1 was the
unadjusted model. Model 2 was adjusted for age, race, marital status,
Methods
educational level, current alcohol use, and body weight. These
confounders were significantly different between the two diabetes
Study design, setting, and population

This is a population-based, cross-sectional study, using 2013 Table 1

National Health Survey data from Brazil, a household survey that Population characteristics by diabetes status (n ¼ 42,631).
used sampling consisting of three-stage conglomerate, with strat- Diabetes* No diabetes P
ification of the primary sampling units. The primary units were (n ¼ 1935) (n ¼ 40,696)
census tracts or set of tracts, the second-stage units were the
Sex
households, and the third-stage units were the residents aged Men 653 (33.75%) 16,798 (41.3%)
18e59 years old.18 Women 1282 (66.25%) 23,898 (58.7%) <0.001
Age categories (years)
Individual data 18e29 134 (6.9%) 11,474 (28.2%)
30e39 337 (17.4%) 12,148 (29.8%)
40e49 538 (27.8%) 9688 (23.8%)
Individual questionnaires were completed by interviewers 50e59 926 (47.9%) 7386 (18.2%) <0.001
trained by the Brazilian Institute of Geography and Statistics (IBGE) Race (self-determined)
and Ministry of Health. The results are available for download on White 728 (37.6%) 16,247 (39.9%)
Non-white 1207 (62.4%) 24,449 (60.1%) 0.04
the IBGE website (http://www.ibge.gov.br/home/estatistica/
Place of residence
populacao/pns/2013_vol3/default_microdados.shtm). Urban 1634 (84.4%) 34,329 (84.35%)
The presence of diabetes was assessed in according to the pos- Rural 301 (15.6%) 6367 (15.65%) 0.915
itive answer to the question ‘Has a doctor ever told you that you Marital status
have diabetes’?.19 The following sociodemographic variables were Married 933 (48.2%) 16,263 (40.0%)
Non-married 1002 (51.8%) 24,433 (60.0%) <0.001
included in the present study: age, weight, and height to calculate Educational level (years)
the body mass index (BMI), place of residence (urban or rural), 0e8 1206 (62.3%) 19,006 (46.7%)
marital status (married or not married), educational level, race 9e11 507 (26.2%) 15,474 (38.0%)
(white or not white), current alcohol use, and current smoker.
12 222 (11.5%) 6216 (15.3%) <0.001
Body mass index (kg/m2) 29.1 (5.9%) 26.4 (5.0%) <0.001
The CRF was predicted from the non-exercise equation of Wier
Body weight status
et al.,20 which contains the following data: sex, age, BMI, and Normal 454 (23.5%) 17,153 (42.15%)
physical activity level. The physical activity level was extracted Excess body weight 1481 (76.5%) 23,543 (57.85%) <0.001
from a valid and reliable questionnaire consisting of questions Current alcohol use
about the frequency and duration of physical activity in different Yes 573 (29.6%) 16,942 (41.6%)
No 1362 (70.4%) 23,754 (58.4%) <0.001
domains: leisure, transportation, occupational, and household.21 Current smoker
Physical activity scores were developed applying the physical Yes 275 (14.2%) 5635 (13.8%)
activity rating (PA-R) scale by attributing a value that ranged No 1660 (85.8%) 35,061 (86.2%) 0.65
from 0 to 10, which corresponded to the type, volume, and intensity Physical activity level (0e10)
Inactive/low level (0e2) 1019 (52.8%) 18,757 (46.1%)
of the physical activity reported.10
Moderate activity (3) 809 (41.8%) 16,637 (40.9%)
The prediction equation was as follows: High activity (
4) 105 (5.4%) 5302 (13.0%) <0.001

*p for difference between subject with and without diabetes; the table presents
VO2 max ¼ 57:402 þ ½1:396 * ðPA  RÞ  ½0:372 * ðage in yearsÞ
mean (standard deviation) or N (%); normal body weight: <25 kg/m2; excess body
 ½0:683 * ðBMIÞ þ ½8:596 * ðsex; 0 ¼ female; 1 ¼ maleÞ: weight:
25 kg/m2.

111

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G.A. Maranhao Neto, I. Alves, E. Lattari et al. Public Health 189 (2020) 110e114

Table 2
Population characteristics by CRF level (n ¼ 42,631).

<6 METs 6e9 METs 10e11 METs
12 METs P

(n ¼ 4285) (n ¼ 17,090) (n ¼ 11,785) (n ¼ 9471)

Sex
Men 83 (1.9%) 3862 (22.6%) 6022 (51.1%) 7484 (79.0%)
Women 4202 (98.1%) 13,228 (77.4%) 5763 (48.9%) 1987 (21.0%) <0.001
Age categories (years)
18e29 57 (1.3%) 1831 (10.7%) 4069 (34.5%) 5651 (59.7%)
30e39 389 (9.1%) 5218 (30.5%) 3948 (33.5%) 2930 (30.9%)
40e49 1171 (27.3%) 5723 (33.5%) 2555 (21.7%) 777 (8.2%)
50e59 2668 (62.3%) 4318 (25.3%) 1213 (10.3%) 113 (1.2%) <0.001
Race (self-determined)
White 1816 (42.4%) 6856 (40.1%) 4666 (39.6%) 3637 (38.4%)
Non-white 2469 (57.6%) 10,234 (59.9%) 7119 (60.4%) 5834 (61.6%) <0.001
Place of residence
Urban 3609 (84.2%) 14,389 (84.2%) 9917 (84.1%) 8048 (85.0%)
Rural 676 (15.8%) 2701 (15.8%) 1868 (15.9%) 1423 (15.0%) 0.318
Marital status
Married 2074 (48.4%) 7788 (45.6%) 4688 (39.8%) 2646 (27.9%)
Non-married 2211 (51,6%) 9302 (54.4%) 7097 (60.1%) 6825 (70.1%) <0.001
Educational level (years)
0e8 2726 (63.6%) 8531 (49.9%) 5155 (43.7%) 3808 (40.2%)
9e11 1090 (25.4%) 5882 (34.4%) 4701 (39.9%) 4308 (45.5%)

12 477 (11.0%) 2677 (15.7%) 1929 (16.4%) 1355 (14.3%) <0.001
Body mass index (kg/m2) 33.3 (5.8) 27.5 (4.5) 24.8 (3.9) 23.6 (3.5) <0.001
Body weight status
Normal 207 (4.8%) 5164 (30.2%) 6512 (55.3%) 5724 (60.4%)
Excess body weight 4078 (95.2%) 11,926 (69.8%) 5273 (44.7%) 3747 (39.6%) <0.001
Current alcohol use
Yes 899 (21.0%) 6044 (35.4%) 5477 (46.5%) 5095 (53.8%)
No 3386 (79.0%) 11,046 (64.6%) 6308 (53.5%) 4376 (46.2%) <0.001
Current smoker
Yes 533 (12.4%) 2376 (13.9%) 1656 (14.0%) 1345 (14.2%)
No 3752 (87.6%) 14,714 (86.1%) 10,129 (86.0%) 8126 (85.8%) 0.036
Physical activity level (0e10)
Inactive/low level (0e2) 3275 (76.4%) 9902 (57.9%) 4850 (41.1%) 1751 (18.5%)
Moderate activity (3) 994 (23.2%) 6883 (40.3%) 5875 (49.8%) 8370 (39.0%)
High activity (
4) 16 (0.4%) 305 (1.8%) 1060 (9.1%) 5072 (42.5%) <0.001
2
*p for difference between subject with and without diabetes; the table presents mean (standard deviation) or N (%); normal body weight: <25 kg/m ; excess body weight:

25 kg/m2. CRF, cardiorespiratory fitness.

Table 3
Association between CRF in METs and presence of T2D in men (n ¼ 17,451).

Categories of fitness (METs) Diabetes** Model 1a 95% CI Model 2b 95% CI

n (%) OR OR

<6 19 (22.9) 1.0 (reference) 1.0 (reference)

6e9 370 (9.6) 0.33* 0.14e0.80 0.36* 0.14e0.88
10e11 197 (3.3) 0.08** 0.03e0.20 0.15** 0.06e0.39

12 67 (0.9) 0.03** 0.01e0.08 0.13** 0.04e0.39
METs per unit 0.58** 0.64e0.63 0.71** 0.75e0.86

CI, confidence interval; OR, odds ratio; CRF, cardiorespiratory fitness; T2D, type 2 diabetes. *P < 0.05 trend across categories. **P < 0.001.
a
Unadjusted.
b
Adjusted by age categories, sex, race, marital status, educational level, excess body weight, current alcohol use, current smoker.

Table 4
Association between CRF in METs and presence of T2D in women (n ¼ 25,180).

Categories of fitness (METs) Diabetes** Model 1a 95% CI Model 2b 95% CI

n (%) OR OR

<6 512 (12.2) 1.0 (reference) 1.0 (reference)

6e9 631 (4.8) 0.35** 0.28e0.42 0.67** 0.53e0.85
10e11 103 (1.8) 0.14** 0.09e0.21 0.77 0.41e1.44

12 36 (1.8) 0.08** 0.03e0.24 0.74 0.21e2,57
METs per unit 0.68** 0.69e0.74 0.86** 0.78e0.94

CI, confidence interval; OR, odds ratio; CRF, cardiorespiratory fitness; T2D, type 2 diabetes. *P < 0.05. **P < 0.001.
a
Unadjusted.
b
Adjusted by age categories, sex, race, marital status, educational level, excess body weight, current alcohol use, current smoker.

112

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G.A. Maranhao Neto, I. Alves, E. Lattari et al.
groups. Statistical significance was set at P < 0.05 based on 2-sided
probability.
Ethical aspects
The study was approved by the National Research Ethics Com-
mittee Comissa

~o Nacional de Etica em Pesquisa, in portuguese
(CONEP) under approval number 328.159, on 26 June 2013 and was
conducted in accordance with Resolution 466 of the National
Health Council from 12 December 2012. All subjects received
detailed information about the study and agreed to participate by
signing the informed consent form.
Results
The characteristics of sample are summarized in Tables 1 and 2.
The overall average age was 37.2 years (SD: 11.4), and the BMI was
26.4 kg/m2 (SD: 5.1). Most of them were either overweight or obese
(excess body weight). Diabetes was reported by 4.5% of the sample
(3.7% in men and 5.1% in women). The average estimated MET was
9.29 (SD: 2.51). The difference between the presence and absence
of diabetes was significant for ‘sex’, ‘age categories’, ‘physical ac-
tivity level’ (by the 0e10 score), ‘BMI’, ‘body weight status’, ‘marital
status’, ‘educational level’, ‘race’ (self-determined), and ‘current
alcohol use’. The difference was not observed for ‘place of resi-
dence’ and ‘current smoker’.
In Table 2, when comparing physical activity levels by CRF cat-
egories, a curious proportion (18.5%) of the 'fittest' individuals are
reporting low levels of physical activity. In fact, the level of physical
activity is one of the information inserted in the model that cal-
culates CRF; however, it is possible that other factors inserted in the
equation also have significant influence. For instance, the correla-
tion between physical activity level and CRF (r ¼ 0.56) is very
similar to that obtained by other studies (from 0.58 to 0.32).22
Significant linear trends were observed in T2D across different
categories of CRF in both unadjusted and adjusted models in men
(Table 3). The association was sizeable; subjects with better CRF
had lower odds of diabetes than individuals with lower levels of
CRF (<6 METs) in unadjusted and adjusted models. A 1-MET in-
crease in estimated CRF was associated with 29% lower odds of
diabetes after adjusting all the potential confounders (P < 0.001).
In women, however, linear trends were not observed in T2D
across ‘10e11’ and ‘
12’ categories of CRF in the adjusted model
(Table 4). A 1-MET increase in estimated CRF was associated with
14% lower odds of diabetes after adjusting all the potential con-
founders (P < 0.001).
Discussion
The objective of the present study was to assess the association
between diabetes and CRF estimated through a non-exercise model
in Brazilian adults. To our understanding, this is the first research to
apply a non-exercise model in a representative population-based
sample of adults. Findings can be summarized as follows: the
presence of T2D was inversely associated with estimated CRF in
every category higher than ''<6 METs'' in men, even when adjusted
for con founders such as age, body weight, race, marital status,
educational level and alcohol intake. In women, the presence of
T2D was not associated with CRF levels higher than 10METs. Some
results of the present study are consistent with previous literature.
A lower CRF has been associated with increased risk of the devel-
opment of metabolic abnormalities associated with the metabolic
syndrome. In fact, low CRF has been observed as the most prevalent
abnormality in populations at risk of diabetes and would be an
early marker of insulin sensitivity.23
113
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Public Health 189 (2020) 110e114
For instance, Gray et al.,24 in a sample of 330 female subjects,
examined the potential relationship(s) between CRF when calcu-
lated using a non-exercise method and the risk of T2D as predicted
by five risk assessments: Leicester Diabetes Risk Score, Q Diabetes,
Cambridge Risk Score, Finnish Diabetes Risk Score, and American
Diabetes Association Diabetes Risk Test. The proportion of women
in quintile 1 predicted at ‘high risk’ (low CRF) was between 20.9%
and 81.4%, depending on diabetes risk assessment used, compared
with none of the women in quintile 5 (high CRF). The authors
consider that the identification of a low CRF value could aid in the
identification of female individual models who can prevent their
development of T2D through lifestyle or pharmacological inter-
vention without the need for consulting diabetes risk prediction
models. However, the results would not likely be applicable to men
and to non-Caucasians populations.
A non-exercise CRF has been inversely associated with diag-
nosed diabetes (7.0% with low CRF versus 0.9% with high CRF in
men and 5.8% versus 0.4% in women) in 32,319 adults (14,650 men)
aged 35e70 years.13 Artero et al.16 in a sample of 43,356 adults (21%
women) from the Aerobics Center Longitudinal Study found that
participants with higher levels of non-exercise estimated CRF were
less likely to have diabetes when compared with subjects with low
CRF levels (7.6% versus 2.2% in men; 5.5% versus 2.8% in women).
Zhang et al.25 with a total of 12,834 participants, aged 20e86 years,
have observed, in a sample of low and high non-exercise CRF, a
presence of diabetes of 19.2% versus 12.4% in men and 25.4% versus
11.3% in women, respectively. The studies aforementioned focused
mainly on studying the associations between non-exercise esti-
mated CRF and mortality, and their results suggest that non-
exercise CRF significantly predicted the risk for non-fatal Cardio-
vascular disease (CVD) events16 and the risk of all-cause and car-
diovascular mortality,13,16,25 which reinforce the feasibility and
cost-effectiveness of the non-exercise method.
One of the main criticisms of non-exercise models is the low
evidence in heterogeneous samples. The sample populations used
to develop the equations are often homogeneous in ethnic distri-
bution, health, and educational level (most subjects are white,
healthy, and well educated).11 In the present study, we show evi-
dence of the generalizability of a non-exercise model in a hetero-
geneous sample. However, regarding the inclusion of variable ‘sex’
in only 38.3% of non-exercise models,11 more analysis should be
performed separately by sex. In the present study, the model
applied was more appropriate to men.
Although CRF may be better estimated when resting heart rate,
body fat percentage, and waist circumference are accounted for,
accurate measurements of these variables as part of epidemiolog-
ical studies may not be logistically feasible, especially in low- and
middle-income countries. Moreover, Peterman et al.26,27 have not
shown much difference when comparing models with and without
these variables to assess longitudinal changes in CRF.
Some limitations of the present study must be addressed. Re-
spondents answered about the existence of a diabetes diagnosis
regardless of type of disease. However, considering that about
90%e95% of all cases are type 2 especially in the adult population,3
the results presented here predominantly refer to T2D. The use of
self-reported data depends on the access to health services; thus,
users who more often use these services have a higher opportunity
for medical diagnosis.28 In addition, the cross-sectional nature of
this study limits the inference of a causal relationship between CRF
and diabetes.
Conclusion
In conclusion, the presence of T2D was inversely associated with
every CRF level in men and with 6e9 METs when comparing with
G.A. Maranhao Neto, I. Alves, E. Lattari et al.
<6 METs in women, through a non-exercise model in Brazilian
adults. This finding suggests that a practical, viable, and low-cost
measurement of CRF could be applied in lower income countries
to assess the relationship between CRF and T2D and, therefore,
enhance diabetes risk stratification beyond conventional office-
based methods. However, new non-exercise models are needed
to better detect T2D in women.
Author statements
Ethical approval
The study was approved by the National Research Ethics Com-
mittee (CONEP) under approval number 328.159. All subjects
received detailed information about the study and agreed to
participate by signing the informed consent form.
Funding
This study was supported by the Carlos Chagas Filho Foundation
for Research Support of the State of Rio de Janeiro (FAPERJ) for the
‘Young Scientist of Our State’ grant (E-26/203.237/2016) for
G.A.M.N.
Competing interests
The authors declare they have no competing interests.
Authors' contributions
G.A.M.N. conceived the study, carried out data collection, per-
formed data analysis, and drafted the manuscript; I.A., S.M., and
S.M.N. drafted the manuscript; E.L. conceived the study and drafted
the manuscript; A.J.O. performed data analysis; X.S. reviewed the
manuscript and the data analysis. All authors have read and
approved the final version of the manuscript and agree with the
order of presentation of the authors.
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