International Journal of

Environmental Research
and Public Health

Article
Changes in Lipoinflammation Markers in People
with Obesity after a Concurrent Training Program:
A Comparison between Men and Women
José Antonio González-Jurado 1 , Walter Suárez-Carmona 2 , Sergio López 3,4 and
Antonio Jesús Sánchez-Oliver 5, *
1 Facultad de Ciencias del Deporte; Universidad Pablo de Olavide de Sevilla, 41013 Sevilla, Spain;
[email protected]
2 Investigador Sistema de Información Científica de Andalucía, Universidad Pablo Olavide de Sevilla,
41013 Sevilla, Spain; [email protected]
3 Laboratory of Cellular and Molecular Nutrition, Inst. de la Grasa, CSIC, 41013 Seville, Spain; [email protected]
4 Department of Cell Biology, University of Seville, 41012 Seville, Spain
5 Departamento de Motricidad Humana y Rendimiento Deportivo, Universidad de Sevilla,
41013 Sevilla, Spain
* Correspondence: [email protected]




Received: 31 July 2020; Accepted: 24 August 2020; Published: 25 August 2020


Abstract: Obesity is related to low-grade systemic inflammation. This state of inflammation is

characterized by the alteration in adipokine regulation, which may lead to a situation of cardiometabolic
risk. The aim of this study was to evaluate the effects of a concurrent training program on markers of
lipoinflammation in adult people with obesity, comparing the response to the training between men
and women. A quasi-experimental, quantitative, and longitudinal study with a pre–post intervention
was conducted. An 8-week concurrent training program was carried out, in which 26 individuals
with obesity participated (mean ± SD; age = 46.38 ± 4.66) (BMI = 36.05 ± 4.99) (12 men and
14 women). Before and after the intervention period, blood samples were taken by percutaneous
puncture. The blood levels of adiponectin and leptin were evaluated. Significant differences were
obtained in the adiponectin–leptin ratio (A/L ratio) of the entire sample (p = 0.009, ES = 0.53), which
indicates a decrease in the risk of cardiovascular diseases and lipoinflammation. There were no
significant differences in the improvements observed after the training in A/L ratio between women
(A/L change = +63.5%) and men (A/L change= +59.2%). It can be concluded that the combination of
aerobic exercise and resistance training induced an improvement in markers of lipoinflammation and
cardiometabolic risk in the individuals with obesity evaluated in this study.

Keywords: overweight; sedentary lifestyle; physical exercise; adiponectin; leptin; adiponectin-leptin ratio

1. Introduction
The worldwide expansion of obesity is a reason to consider it a pandemic nowadays. The World
Health Organization (WHO) defines overweight and obesity as an abnormal or excessive accumulation
of fat that poses a health risk [1]. Despite this relatively simplistic definition, obesity is a chronic,
multifactorial, and multicausal disease, which corresponds to an alteration of the correct function of
the adipose tissue in its capacity to store fat, both quantitatively and qualitatively [2]. In addition,
it leads to an inflammatory condition of the aforementioned tissue (lipoinflammation), closely linked
to metabolic disorders, which in turn are strongly associated with the metabolic syndrome [2].
Although an increase of the total body fat is associated with an increase of health risk, the amount
of abdominal fat, particularly when it is found within the abdominal cavity, has been associated with

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Int. J. Environ. Res. Public Health 2020, 17, 6168 2 of 12

an increase of the risk of comorbidity and mortality for different reasons. Thus, we observe a higher
prevalence of type 2 diabetes, heart disease, stroke, sleep apnea, hypertension, dyslipidemia, insulin
resistance, inflammation, and some types of cancer [2]. All these diseases have negative effects on the
quality of life, work productivity, and the costs of medical assistance [3,4].
Lifestyle changes are a critical part of obesity prevention and intervention and are being pursued
by public health organizations to promote health [5]. Physical inactivity and sedentary behavior are
two powerful drivers of the obesity pandemic [6] and have been linked to an increased prevalence of
disease and an increased risk of all-cause mortality [7].
Obesity has been recognized as a systemic low-grade inflammatory state, characterized by an
increase of inflammatory factors and infiltration of immune cells, with no lesions or alterations in tissue
structure or function [2]. It has been reported that obesity is associated with an atypical activation
of proinflammatory signaling in the hypothalamus [8]. Although there are no alterations in cell
morphology at the histological level, at the plasmatic level there is an increase of proinflammatory
cytokines, such as TNF-α, IL-1b, IL-6, and C-reactive protein, as well as infiltration of macrophages and
T lymphocytes in insulin-dependent tissues, among others, which triggers factors such as oxidative
stress and insulin resistance [9].
Adipose tissue (AT) is a primordial connective tissue in the energy storage of every organism,
and it mainly consists of adipocytes. It carries out autocrine, endocrine, and paracrine functions
on the rest of the organs, participating in the regulation of energetic homeostasis, glucose and lipid
metabolism, and hormone modulation, and it also plays a relevant role in the inflammatory process [10].
When a hypertrophic adipocyte exceeds its threshold capacity, its normal activity stops, showing a
decrease in insulin sensitivity, hypoxia, an increase in cell stress, and consequently cell apoptosis, thus
activating the inflammatory process [11]. AT secretes a series of proinflammatory and anti-inflammatory
adipokines, of which the most popular are leptin and adiponectin. Leptin is a protein that performs
its physiological activity through its receptor LEP-R (leptin receptor). The binding of leptin to its
receptor in the hypothalamus triggers a series of chemical signals that affects the feeling of hunger and
help to produce the feeling of satiety. An excess of leptin in the adipocyte promotes the inflammatory
effect and decreases insulin sensitivity [12]. Adiponectin is the most abundant adipokine in human
blood, with physiological levels of 5–30 ug/mL. It is secreted by the AT, mainly by white adipose tissue
(WAT) [13]. Adiponectin is a protein hormone that plays an anti-inflammatory role within the adipose
tissue. Previous studies have shown insulin-sensitizing, anti-atherogenic, and anti-inflammatory
effects [2]. This role of adiponectin in the inflammatory process is particularly positive in patients
with metabolic diseases such as type 2 diabetes mellitus and obesity, who have shown low-grade
chronic inflammation and low serum adiponectin concentrations [4]. Therefore, leptin and adiponectin
play an important role in the health of the individual and his adipose tissue. Leptin regulates innate
and adaptive responses through the modulation of the activity and proliferation of immune cells;
thus, it can regulate the polarization toward a proinflammatory phenotype. On the other hand,
adiponectin shows anti-inflammatory properties, stimulates lipid oxidation, and improves glucose
metabolism by increasing insulin sensitivity. Adipocyte hypertrophy produces an imbalance in these
hormones, promoting the production of leptin and reducing that of adiponectin; participating in
adverse signals from adipose tissue that can lead to secondary tissue damage that increases concomitant
lipotoxicity [2,14]. Therefore, the adiponectin/leptin ratio (A/L ratio) is identified as a marker of adipose
tissue failure. It has been demonstrated that this index is strongly associated with insulin resistance,
showing a stronger relationship with the risk of developing type 2 diabetes compared to the analysis
of leptin or adiponectin separately [15].
The A/L ratio is a good indicator of a malfunctioning adipose tissue and it is negatively
associated with markers of low-grade chronic inflammation; thus, it can be a useful stimulator
of the cardiometabolic risk associated with obesity [16]. Although the measurement method used
must be taken into account, it is considered that a normal A/L ratio should have values above 1.0
(adiponectin levels expressed in µg/mL and leptin levels in ng/mL), whereas an A/L ratio between 0.5
Int. J. Environ. Res. Public Health 2020, 17, 6168 3 of 12

and 1.0 represents a moderate/medium cardiometabolic risk, and a proportion below 0.5 is a serious
indicator of cardiometabolic risk [17].
Numerous authors agree in the effects of physical exercise on the AT [18–21], such as changes
in the AT phenotype that lead to a significant decrease of M1 macrophages and an increase of M2
macrophages, as well as the secretion of more anti-inflammatory cytokines, such as IL-6 and TNF-α [22].
Other researchers have studied the possible changes in the signaling pathways after implementing
exercise programs, reporting a decrease of postprandial lipemia, a reduction in NF-kB signaling, and an
increase in AMPK signaling (showing anti-inflammatory properties) [23–25]. The interest of these
studies is increasingly focused on determining the most adequate training to reduce the inflammatory
state and its effects on metabolic syndrome in people with obesity. There is scientific evidence that
aerobic training improves the levels of proinflammatory cytokines (TNF-α, IL-6, and IL-8) in people
with obesity and type 2 diabetes [26]. In fact, aerobic or cardiorespiratory exercise programs are the
most frequently implemented [27]. However, other studies have analyzed the impact of resistance
training or a combination of resistance and aerobic training on low-grade chronic inflammation in
people with obesity and overweight [28–31]. Even methodologies of highly specialized training
with high-intensity interval training (HIIT) have been implemented to compare their effect on the
inflammatory state of people with obesity and normal weight [32].
The aim of this study was to evaluate the effects of an 8-week concurrent training program on
markers of lipoinflammation (adiponectin, leptin, and adiponectin-leptin ratio) in 26 adult people with
obesity, comparing the response to the training between men and women.

2. Materials and Methods

This is a quasi-experimental, quantitative, and longitudinal study with a pre–post intervention.
A total of 26 individuals participated in the study (12 men and 14 women), with an age range of 38 to
54 years (46.38 ± 4.66) and obesity (BMI = 36.05 ± 4.99). Table 1 shows baseline and Figure 1 shows a
flowchart of the participant selection process followed in the study.

Table 1. Participants’ baselines.

Male Female All

Mean ± SD Range Mean ± SD Range Mean ± SD Range
Age (yr) 46.42 ± 5 38–54 46.36 ± 4.53 40–53 46.38 ± 4.66 38–54
Height (m) 1.75 ± 0.07 1.6–1.9 1.61 ± 0.08 1.44–1.73 1.67 ± 0.10 1.44–1.9
Weight (kg) 109.9 ± 16.35 87–140 94.67 ± 21.95 70.7–147 101.73 ± 20.7 70.7–147
BMI 35.98 ± 3.98 30.1–42.2 36.12 ± 5.87 30.05–49.69 36.05 ± 4.99 30–49.7
BFM (kg) 43.86 ± 11.08 24–58.4 45.11 ± 14.70 30.8–79.3 44.53 ± 12.92 24–79.3
BFMP (%) 39.53 ± 5.94 28–48.8 47.59 ± 4.63 39–53.9 43.87 ± 6.59 28–53.9
BMI: Body Mass Index. BFM: Body Fat Mass; BFMP: Body Fat Mass Percent.
Int. J. Environ. Res. Public Health 2020, 17, 6168 4 of 12
Int. J. Environ. Res. Public Health 2020, 17, x FOR PEER REVIEW 13 of 12

Figure 1. Recruitment
Figure flowchart.
1. Recruitment flowchart.

TheThe
following
following inclusion
inclusioncriteria were
criteria applied;
were (i) 35–55
applied; years
(i) 35–55 of age;
years (ii) BMI:
of age; > 30;
(ii) BMI: (iii)(iii)
> 30; abdominal
abdominal
perimeter: >90 >100 in men; (iv) fat%: >40
perimeter: > 90 cm in women and> 100 cm in men; (iv) fat %: > 40 in women and > 30 insigned
cm in women and cm in women and >30 in men; (v) men; (v)
informed
signed consent;
informedand (vi) official
consent; and (vi)medical
officialauthorization that allowed
medical authorization thattheallowed
participant to carry outtothe
the participant carry
program
out theofprogram
planned exercises.
of plannedSimilarly,
exercises.the following
Similarly, theexclusion
following criteria were criteria
exclusion applied;were (i) diagnosis
applied; (i)
of adiagnosis
pathology ofinvolving
a pathology aninvolving
inflammatory process (e.g.,process
an inflammatory myocardial (e.g., infarction
myocardial ininfarction
the last 12inmonths,
the last 12
rheumatoid arthritis, fibromyalgia, and arthrosis), and (ii) failing
months, rheumatoid arthritis, fibromyalgia, and arthrosis), and (ii) failing to complete to complete 75% of the training
75% of the
sessions.
trainingThe study meets
sessions. The studythe requirements of the Declaration
meets the requirements of Helsinki of
of the Declaration of Helsinki
the World of Medical
the World
Association
Medical Association (2013) about the ethical principles for research with human beings, and itbywas
(2013) about the ethical principles for research with human beings, and it was approved
theapproved
Ethics Committee of theCommittee
by the Ethics Universityof ofthe
Pablo de Olavide
University (Seville,
of Pablo Spain). (Seville, Spain).
de Olavide
TheThe
independent
independent variable was a concurrent training program out
variable was a concurrent training program carried for 8 out
carried weeks,for with
8 weeks,3 weekly
with 3
sessions of ~60 min each in alternate days (Monday, Wednesday, and
weekly sessions of ~60 min each in alternate days (Monday, Wednesday, and Friday). The trainings Friday). The trainings were
conducted in the time
were conducted frame
in the time of frame
5:30 p.m. to 8:30
of 5:30 p.m.p.m. to accommodate
to 8:30 p.m. to accommodate the individual needs ofneeds
the individual each of
participant (work, family, personal, etc.) (Figure
each participant (work, family, personal, etc.) (Figure 2). 2).
Each
Eachtraining
trainingsession
sessionbegan
began with a general
with a general joint mobility
joint mobility (5 min)
(5 min)andand cardiovascular
cardiovascular activation
activation
(5 min), followed
(5 min), followed by abycardiorespiratory
a cardiorespiratory resistance
resistanceexercise
exercise(three possible
(three possibleoptions:
options: treadmill,
treadmill, cycle
cycle
ergometer, or elliptical bike). This task was carried out for 12 min
ergometer, or elliptical bike). This task was carried out for 12 min at a medium–low intensity. The at a medium–low intensity.
Theintensity
intensitywas wasdetermined
determined using
using Borg’s
Borg’s rate
rate of of perceived
perceived exertion
exertion (RPE),
(RPE), aiming
aiming to reach
to reach a RPEa RPE
value
value
of of
4–54–5
out outofof1010[33].
[33].Then,
Then,aaresistance
resistance training
training was wasconducted,
conducted,with witha 10-station
a 10-station circuit.
circuit. Figure 2 2
Figure
shows the ten exercises proposed, which involve the main muscle groups
shows the ten exercises proposed, which involve the main muscle groups used in the most habitual used in the most habitual
basic motor
basic motor skills andand
skills global motor
global motoractions
actions of daily
of dailyliving (walking,
living (walking, running,
running, throwing,
throwing, carrying
carrying
weight, etc.).
weight, etc.).
Int. J. Environ. Res. Public Health 2020, 17, 6168 5 of 12
6 of 12

Figure 2. Summary of the training program and training session.

Figure 2. Summary of the training program and training session.

The working time in each station was 45 s in the first two weeks, and it was increased to 60 s from
The working time in each station was 45 s in the first two weeks, and it was increased to 60 s
the third week. The resting time between exercises was 45 s in the first two week and 30 s from the
from the third week. The resting time between exercises was 45 s in the first two week and 30 s from
second week. In the first two weeks, two circuits were completed in each session, with a passive rest of
the second week. In the first two weeks, two circuits were completed in each session, with a passive
2 min.
rest After the third
of 2 min. After week, the week,
the third circuitthe
wascircuit
completed 3 times in 3each
was completed timessession,
in eachkeeping
session,the restingthe
keeping time
to 2resting
min. time
The intensity
to 2 min. The intensity of the exertion was measured through the RPE scale OMNI-RES, to
of the exertion was measured through the RPE scale OMNI-RES, aiming
reach and to
aiming maintain
reach and values of 6–7
maintain out ofof10
values 6–7[34].
out Every session
of 10 [34]. Everyended with
session cooling
ended withexercises (Figure 2).
cooling exercises
The planned
(Figure 2). training (temporalization, organization, methodology, training load levels,
characteristics of the exercises, etc.) allowed each participant to undergo
The planned training (temporalization, organization, methodology, training load levels,an individualized training
stimulus. In thisofstudy,
characteristics it was never
the exercises, intended
etc.) allowed to participant
each standardizetoaundergo
closed and rigid trainingtraining
an individualized program.
In this sense,Ineach
stimulus. this participant,
study, it wasdepending
never intended on their physical capacity,
to standardize underwent
a closed and a training
rigid training stimulus
program. In
this sense, each participant, depending on their physical capacity, underwent a training
that posed a relative subjective intensity similar to that of the rest of the sample. Therefore, simple stimulus that
posed were
exercises a relative subjective
selected, in termsintensity similarand
of execution to that of the to
adaptation restthe
ofindividual
the sample. Therefore, simple
capacities.
exercises weremarkers
The blood selected,analyzed
in terms ofwereexecution
leptinandandadaptation to theEndovenous
adiponectin. individual capacities.
puncture equipment
and tubes Thewere
bloodused
markers analyzed
for the were leptin
collection and adiponectin.
of biological samples. Endovenous
Endovenous puncture
blood wasequipment andby
extracted
tubes were used for the collection of biological samples. Endovenous
percutaneous puncture using appropriate needles and syringes. These techniques are minimally blood was extracted by
percutaneous puncture using appropriate needles and syringes.
invasive, practically harmless, and pose no serious threat to the participants. These techniques are minimally
invasive, practically harmless, and pose no serious threat to the participants.
For the statistical analyses, the IBM SPSS Statistics 23 software (SPSS Inc., Chicago, IL, USA)
For the statistical analyses, the IBM SPSS Statistics 23 software (SPSS Inc., Chicago, IL, USA) was
was used. Regarding the descriptive statistics, the mean and standard deviation were calculated.
used. Regarding the descriptive statistics, the mean and standard deviation were calculated. The
The reliability of the measurements was estimated at a 95% confidence interval for the mean. Regarding
reliability of the measurements was estimated at a 95% confidence interval for the mean. Regarding
the inferential statistics, a paired-sample t or Wilcoxon test was conducted for intragroup comparisons,
the inferential statistics, a paired-sample t or Wilcoxon test was conducted for intragroup
depending on the normality (assessed through the Shapiro–Wilk test), and an independent-samples t
comparisons, depending on the normality (assessed through the Shapiro–Wilk test), and an
or Mann–Whitney
independent-samples U test, depending
t or Mann–Whitneyon the U normality and theon
test, depending Levene test. Cohen’s
the normality and the d effect
Levene size was
test.
also calculated [35], considering values of d < 0.3 as small, d = 0.3–0.5 as moderate,
Cohen’s d effect size was also calculated [35], considering values of d < 0.3 as small, d = 0.3–0.5 as d = 0.5–0.7 as large,
d =moderate,
0.7–0.9 asdvery large,
= 0.5–0.7 asand d>
large, d 0.9 as extremely
= 0.7–0.9 large and
as very large, [36].d > 0.9 as extremely large [36].

3. Results
3. Results
Table 2 shows
Table 2 showsthethepre–post
pre–postcomparison
comparison for
for the
the entire
entire sample.
sample. AsAscan
canbebeseen,
seen,there
therewas
wasa a
significant
significant increase in the adiponectin/leptin ratio at the end of the intervention period with respect to
increase in the adiponectin/leptin ratio at the end of the intervention period with respect
the baseline situation, with a moderate effect size. There were no significant differences in the results
obtained in the variables “adiponectin” and “leptin”.
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Int. J. Environ. Res. Public Health 2020, 17, 6168 6 of 12

Table 2. Intragroup comparisons. Whole sample (n = 26).

Pre-Test Post-Test Change p§

E.S ¥
Mean ± SD CI (95%) Mean ± SD CI (95%) Mean ± SD CI (95%) Value
Adiponecti
16.94 ± 4.89 (14.9–18.6) 17.3 ± 5.1 (15.2–19.3) 0.32 ± 3.04 (−0.91–1.55) 0.20 0.06
(ug/mL)
Leptin
44.09 ± 24.3 (34.3–53.9) 41.6 ± 30.5 (29.3–53.9) −2.5 ± 20.1 (−10.6–5.59) 0.47 −0.09
(ng/mL)
A/L ratio * 0.5 ± 0.32 (0.37–0.63) 0.82 ± 0.79 (0.5–1.14) 0.32 ± 0.57 (0.09–0.55) 0.009 * 0.53
§Student t-test or Wilcoxon depending on the normality; ¥ Cohen’s effect size (d < 0.3 small; d = 0.3–0.5 moderate;
d = 0.5–0.7 large; d = 0.7–0.9 very large and d > 0.9 extremely large). * Adiponectin/leptin ratio.

Table 3 shows the results obtained when comparing the variables “adiponectin” and “leptin”
before and after the intervention in the women’s group. There were no significant differences in the
levels of adipokines. However, the A/L ratio did show a statistically significant improvement (p = 0.05)
with a large effect size (d = 0.55).

Table 3. Intragroup comparisons. Women (N = 14).

Pre-Test Post-Test Change p§ E.S ¥

Mean ± SD CI (95%) Mean ± SD CI (95%) Mean ± SD Mean ± SD Value CI (95%)
Adiponectin
18.24 ± 3.8 (16.04–20.43) 18.17 ± 1.16 (15.67–20.67) −0.06 ± 3.63 (−2.16–2.03) 0.55 −0.02
(ug/mL)
Leptin
46.5 ± 23.8 (32.7–60.2) 46.1 ± 37.6 (2.44–6.78) −0.4 ± 21.52 (−12.8–12.0) 0.82 −0.01
(ng/mL)
A/L ratio * 0.51 ± 0.28 (0.35–0.67) 0.85 ± 0.8 (0.39–1.31) 0.34 ± 0.62 (−0.01–0.7) 0.05* 0.55
§Student t-test or Wilcoxon depending on the normality. ¥ Cohen’s effect size (d < 0.3 small; d = 0.3–0.5 moderate;
d = 0.5–0.7 large; d = 0.7–0.9 very large and d > 0.9 extremely large). * Adiponectin/leptin ratio.

Table 4 shows the values obtained in the men’s group, which were similar to those observed
in the women’s group, i.e., there were no significant differences in the levels of adipokines between
the pre-test and the post-test. In this case, although the A/L ratio improved, this increase was not
statistically significant (p = 0.08); however, the effect size of this increase can be considered as moderate
(d = 0.46).

Table 4. Intragroup comparisons. Men (N = 12).

Pre-Test Post-Test Change p

Value § E.S ¥
Mean ± SD CI (95%) Mean ± SD CI (95%) Mean ± SD CI (95%)
Adiponectin
15.43 ± 5.71 (11.8–19.1) 16.2 ± 5.71 (12.57–19.83) 0.76 ± 2.25 (−0.67–2.2) 0.26 0.12
(ug/mL)
Leptin
41.32 ± 25.6 (25.1–57.6) 36.36 ± 19.86 (23.7–48.9) −4.96 ± 18.82 (−16.9–6.9) 0.38 −0.22
(ng/mL)
A/L ratio * 0.49 ± 0.37 (0.25–0.73) 0.78 ± 0.81 (0.27–1.29) 0.29 ± 0.53 (−0.05–0.63) 0.08 0.46
§ Student t-test or Wilcoxon according to normality. Cohen’s effect size (d < 0.3 small; d = 0.3–0.5 moderate;
¥

d = 0.5–0.7 large; d = 0.7–0.9 very large and d > 0.9 extremely large). * Adiponectin/Leptin ratio.

The results of the intergroup comparisons (women vs. men) are represented in Figure 3.
The pre–post differences are compared, expressed in percentages. As can be observed, the differences
between men and women are very small; in fact, there were no statistically significant differences in
any of the three variables. It is worth highlighting that the A/L ratio increased considerably in the two
groups and in a similar manner, suggesting that both improved this index to the same extent.
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Int. J. Environ. Res. Public Health 2020, 17, x FOR PEER REVIEW 13 of 12

Female vs. Male comparisons differences posttest—pretest

75%
Female Male All 63% 64%
59%
60%
Change Percent

45%

30%

15%
5%
1.89%
0%
-0.38% -0.86%
-12% -5.67%
-15%
Adiponectin Leptin A/L Ratio

Figure Changesafter
3. Changes
Figure 3. afterintervention
interventioncomparisons.
comparisons.NoNo significant
significant differences
differences were
were found
found between
between sex
sex groups. Student t-test or Mann–Whitney U were carried out depending on the normality
groups. Student t-test or Mann–Whitney U were carried out depending on the normality and Levene and
Levene
test. test.

4. Discussion
4. Discussion
The aim of this study was to analyze the effects of a physical exercise program based on concurrent
The aim of this study was to analyze the effects of a physical exercise program based on
training on lipoinflammation marker adipokines in adults with obesity, comparing the responses
concurrent training on lipoinflammation marker adipokines in adults with obesity, comparing the
between men and women.
responses between men and women.
Table 2 compares the results of the entire sample (n = 26), showing that the initial average leptin
Table 2 compares the results of the entire sample (n = 26), showing that the initial average leptin
levels were 44.09 ng/mL. These levels are associated with greater insulin resistance, and they are
levels were 44.09 ng/mL. These levels are associated with greater insulin resistance, and they are
usually found in people with a BMI above 30. The results show an improvement of these values after
usually found in people with a BMI above 30. The results show an improvement of these values after
the intervention, from 44.09 down to 41.59 ng/mL, although this decrease was small (−2.5 ng/mL) and
the intervention, from 44.09 down to 41.59 ng/mL, although this decrease was small (−2.5 ng/mL) and
not statistically significant. The changes in adiponectin were also positive, that is, there was an increase
notitsstatistically
in blood levelssignificant. The although
(+0.32 ug/mL), changes in thisadiponectin
increase was were also positive,
not statistically that is, there
significant either.was an
increase
The results are presented separately by sex in Tables 3 and 4. These results are similar toeither.
in its blood levels (+0.32 ug/mL), although this increase was not statistically significant those
The results are presented separately by sex in Tables 3 and 4. These
obtained considering the entire sample. There were signs of improvement in adiponectin and leptin,results are similar to those
obtained considering the entire sample. There were signs of improvement
although such changes were very small. On the other hand, there were more considerable differences in adiponectin and leptin,
although
in such changes
the increases wereratio,
in the A/L very small.
which On werethesignificant
other hand,inthere were more
the women’s considerable
group (p = 0.5)differences
and close
in the increases in the A/L ratio, which were significant in the women’s group
to statistical significance in the men’s group (p = 0.08), with a large effect size in women (0.55) (p = 0.5) and close to
and
statistical significance
moderate in men (0.46). in the men’s group (p = 0.08), with a large effect size in women (0.55) and
moderate in men (0.46).
In numerous studies, people with obesity have conducted different training programs, reporting
In numerous
improvements in the studies, peoplelevels
plasmatic with of
obesity
leptinhave conducted
[37–40], different training
with significant decreases. programs,
Likewise, reporting
a large
improvements in the plasmatic levels of leptin [37–40], with significant decreases.
number of studies have analyzed the effects of different physical exercise programs on the concentrations Likewise, a large
number
of of studies
adiponectin [41–44]. have analyzed the effects of different physical exercise programs on the
concentrations of adiponectin
In the present study, the changes[41–44]. in adiponectin and leptin were lower, probably due to the fact
In the present study, the changes
that the intervention period was considerably in adiponectin
shorter and leptin were
compared to thatlower,
of theprobably due to
cited studies the fact
[37,42,45],
that
or the intervention
because period was
their interventions considerably
evaluated the acuteshorter
effectcompared
of exercisetoprograms
that of theof cited
higher studies [37,42,45],
intensity [43,44].
or because their interventions evaluated the acute effect of exercise
Other studies combined the training with the administration of ergogenic or anti-inflammatory programs of higher intensity
[43,44]. Other
supplements studies combined the training with the administration of ergogenic or anti-
[41].
inflammatory supplements
The improvements [41].levels of adiponectin and leptin, analyzed independently, were not
in the
The improvements in
significant; however, the A/L ratio the levels of adiponectin
did obtain andincrease
a significant leptin, analyzed independently,
after the training period (pwere not
= 0.009),
significant; however, the A/L ratio did obtain a significant increase after the training period (p = 0.009),
with a large effect size (0.53).The A/L ratio is a biomarker that has been well studied in its relationship
Int. J. Environ. Res. Public Health 2020, 17, 6168 8 of 12

with a large effect size (0.53). The A/L ratio is a biomarker that has been well studied in its relationship
with lipoinflammation [16], and as an indicator of obesity and metabolic risk [46–48]. However, only
few studies have analyzed the effect of planned and controlled physical exercise programs on this
marker (A/L ratio) in people with obesity, and most of these studies evaluated these two adipocytokines
independently [27,30,49,50]. All of them report significant improvements after exercise, both an
increase in adiponectin and a decrease in leptin, which is in line with the results of the present study.
A novelty of our study is that it analyses the effect of a concurrent or combined training program on
a specific lipoinflammation marker (A/L ratio), obtaining significant improvements after 8 weeks of
intervention. One of the factors in controversy or disagreement with the scientific literature is related to
the characteristics of the training programs implemented. In this sense, most of the studies that report
positive results in the levels of both adipokines (adiponectin and leptin) after the exercise program,
carried out aerobic or cardiorespiratory trainings [49,51–53]. Few studies have included resistance
training [30,31], although concurrent or combined training programs are being applied increasingly
frequently, as they seem to be more effective, as was demonstrated in the current study.
Another finding among the obtained results is related to the response of the lipoinflammation
markers analyzed based on sex. Most studies have been conducted with samples of a single gender.
In a meta-analysis published in 2017, in which 28 RCTs were included, only two of these recruited both
men and women in their samples [27]. One of these studies only evaluated the effects of exercise on
leptin and the participants were adolescents [54], and in another study the participants were children
and the authors only evaluated adiponectin [55]. Another meta-analysis published in 2018 included
22 trials with 2996 individuals. These authors concluded aerobic exercise increased adiponectin and
reduced leptin levels in prediabetic and diabetic adults. Most trials included both sexes, but there
were not compared men versus women. In addition, the studies, the population analyzed, and the
design of physical exercise interventions heterogeneity was found [56]. Figure 3 compares the change
percentages in the three variables analyzed between men and women, clearly showing that sex was not
a determining factor in the response of these adipokines to exercise, obtaining no significant differences
between men and women in the response to the training program implemented.
A current narrative review about the effects of physical activity (PA) on adipokine levels in
individuals with overweight and obesity has analyzed approximately 90 different investigations on
adipokine levels in individuals with overweight/obesity were reviewed. The results support the
benefits of exercise regardless of the mode (resistance vs. aerobic), intensity, and cohort (healthy
vs. diabetes) on adipokines levels. However, several confounding factors (frequency, intensity, time,
and type of exercise) can alter the magnitude of these effects [57].
A low number of experimental subjects and the lack of a control group are the two major
limitations of this study. Despite this, the present study has been able to demonstrate that a simple and
a short program of physical exercise improves the markers of lipoinflammation studied and, therefore,
the inflammatory health of the participants. However, cautious interpretation of current findings
is warranted.
There is a large number of studies about the effect of exercise on low-grade chronic inflammation;
however, there is also a wide methodological variety, diversity in the characteristics of the participants,
and multiple physical exercise programs implemented with important differences in the characteristics
of the training loads. Therefore, it seems obvious that further research is still required in this field.

5. Conclusions
The participants of this study started with a low A/L ratio, with risk of low-grade chronic
inflammation. Both women and men improved in the three indicators analyzed, although statistically
significant improvements with a large effect size in women and moderate in men were obtained in A/L
ratio, with these improvements being more evident when considering the entire sample without sex
differentiation. In fact, when comparing women and men, no difference was found in the response of
the adipokines to the exercise program based on sex.
Int. J. Environ. Res. Public Health 2020, 17, 6168 9 of 12

Author Contributions: Conceptualization, J.A.G.-J., W.S.-C., and A.J.S.-O.; methodology, J.A.G.-J., W.S.-C.,
and A.J.S.-O.; formal analysis, J.A.G.-J.,; investigation, W.S.-C. and S.L.; resources, J.A.G.-J. and S.L.; data
curation, J.A.G.-J.; writing—original draft preparation, J.A.G.-J.; writing—review and editing, J.A.G.-J., W.S.-C.,
and A.J.S.-O.; visualization, J.A.G.-J., W.S.-C., and A.J.S.-O.; project administration, J.A.G.-J.; funding acquisition,
J.A.G.-J. All authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Acknowledgments: The authors would like to thank to the participants. Additionally, Sergio Lopez acknowledges
the “V Own Research Plan” of the University of Seville (VPPI-US) contract (cofounded by the European Social Fund).
Conflicts of Interest: The authors declare no conflict of interest.

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