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Scand J Med Sci Sports. 2018;1–10. wileyonlinelibrary.com/journal/sms
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© 2018 John Wiley & Sons A/S.
Published by John Wiley & Sons Ltd
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INTRODUCTION
Type 2 diabetes mellitus (T2DM) is a major worldwide
health challenge associated with considerable morbidity and
mortality, and additionally, it is imposing a significant eco-
nomic burden on the healthcare system.1 Globally, it is esti-
mated that the number of patients with T2DM will increase
to around 370 million by 2030.1,2 For example, in the United
States alone, the incidence of T2DM increased 117% from
1980 to 2011 and as many as one in three adults are projected
to develop T2DM by 2050 if current trends continue.3
T2DM is a pathological condition partly related to life-
styles such as physical inactivity and poor nutritional hab-
its. Moreover, the latest recommendations on diabetes care
concluded that education on self- management is essen-
tial.4 Within these recommendations, patients with diabetes
Accepted: 6 March 2018
DOI: 10.1111/sms.13081
ORIGINAL ARTICLE
Football training improves metabolic and cardiovascular health
status in 55- to 70- year- old women and men with prediabetes
M.-B. Skoradal1
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P. Weihe1,2
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P. Patursson1,3
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J. Mortensen3,4
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L. Connolly5
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P. Krustrup5,6
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M. Mohr1,6,7
1Faculty of Health Sciences,Centre of
Health Science,University of the Faroe
Islands, Tórshavn, Faroe Islands
2Department of Occupational Medicine
and Public Health,The Faroese Hospital
System, Tórshavn, Faroe Islands
3Department of Medicine,The Faroese
National Hospital, Tórshavn, Faroe Islands
4Department of Clinical
Physiology,Nuclear Medicine &
PET,Rigshospitalet,Copenhagen
University Hospital, Copenhagen, Denmark
5Sport and Health Sciences,University of
Exeter, Exeter, UK
6Department of Sports Science and Clinical
Biomechanics,SDU Sport and Health
Sciences Cluster (SHSC),Faculty of Health
Sciences,University of Southern Denmark,
Odense, Denmark
7Department of Food and Nutrition,
and Sport Science,Center for Health
and Human Performance,University of
Gothenburg, Gothenburg, Sweden
Correspondence
Magni Mohr, Faculty Health Sciences,
Centre of Health Science, University of the
Faroe Islands, Tórshavn, Faroe Islands.
Email: magnim@setur.fo
Funding information
Faroese Research Council; Faroese Football
Association; Faroese Diabetes Organisation
We examined the effects of 16 weeks of football training and dietary advice on blood
glucose control and health status in 55- to 70- year- old women and men with predia-
betes. Fifty participants with prediabetes (age; 61 ± 6 years, BMI; 29.6 ± 4.7;
VO2max 22.3 ± 5.7 mL·min−1·kg−1) were randomized into a football and dietary ad-
vice group (F+D; n = 27) and a dietary advice group (D; n = 23). F+D performed
football training (twice weekly 30- to 60- minutes sessions) and received dietary ad-
vice, while D only received dietary advice. An oral glucose tolerance test (OGTT)
was completed pre and post the 16- week period. Body composition, blood pressure,
and maximal oxygen uptake (VO2max) were additionally measured. Both groups
demonstrated a decrement (P < .05) in fasting blood glucose (−0.4 ± 0.5 mmol·L−1)
and lowered blood glucose throughout OGTT. F+D displayed lower values than D
(P < .05) after 60 minutes (9.0 ± 2.7 vs 10.6 ± 2.9 mmol·L−1) and 120 minutes
(5.7 ± 1.6 vs 7.5 ± 2.4 mmol·L−1). VO2max increased by 14% in F+D, with a higher
(P < .05) change score than in D (2%). Mean arterial pressure declined more
(P < .05) in F+D than in D (−8 ± 9 vs −4 ± 11 mm Hg). Fat loss was greater
(P < .05) in F+D than in D (−3.4 ± 2.8 vs −1.2 ± 2.0 kg), and the increase in lean
body mass was also greater (P < .05) in F+D than in D (0.7 ± 1.5 vs −0.3 ± 1.6 kg).
In conclusion, football training combined with dietary advice has broad- spectrum
effects on metabolic and cardiovascular health profile with greater overall effects
than professional dietary advice per se for 55- to 70- year- old women and men with
prediabetes.
KEYWORDS
blood pressure, cardiometabolic fitness, cholesterol, fat percentage, soccer, VO2max
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SKORADAL etAL.
are instructed to perform at least 150 minutes per week of
moderate- intensity aerobic physical activity combined with
resistance training at least twice per week.5 Moreover, nu-
trition therapy is included as an integral part of the self-
management education in individuals with T2DM.4
T2DM is preceded by a progressive impairment in glu-
cose regulation or prediabetes defined by impaired fasting
glycemia (IFG) or impaired glucose tolerance (IGT).5 In ad-
dition to a deterioration in blood glucose control, patients
with T2DM often suffer from other serious health compli-
cations, such as poor physical fitness, obesity, low muscle
mass, and cardiovascular deficiencies.6 Exercise training
has been shown to improve blood glucose regulation and
is proposed for inclusion in the treatment of patients with
prediabetes and T2DM.7 Thus, development of efficient ex-
ercise training protocols for these patient groups is highly
warranted.
Football training has been extensively studied during
the last decade and proves to be a complex exercise train-
ing method that results in broad- spectrum health effects.8 For
example, football training two to three times per week has
been shown to improve metabolic and cardiovascular health
in sedentary hypertensive women.9 Moreover, improved
blood glucose control and general health profile have been
demonstrated in both male and female patients with T2DM
after recreational football training interventions.9,10 Indeed,
a recent study by de Sousa et al11 showed that a combination
of 12 weeks of football training and a caloric- restricted diet
markedly improved glucose regulation and reduced markers
of muscle catabolism, with greater changes than diet approach
alone. Thus, it is interesting and appears plausible to suggest
that football training may facilitate blood glucose control
in patients with prediabetes. Football training is especially
likely to have major potential as a treatment protocol for pa-
tients with prediabetes and may prevent or delay the onset of
the disease, due to the broad- spectrum effects encompassing
both major metabolic and cardiovascular benefits.
It is well- known that aging results in marked deteriorations
in health profile. For example, meta- analysis has demonstrated
that mortality can be reduced by physical activity in elderly
people up to the age of eighty.12 The prevalence of T2DM also
accelerates markedly with increasing age,13 and low physical
capacity has been substantiated to be an independent marker
of mortality in patients with T2DM14 Thus, it is highly rele-
vant to develop treatment protocols for patients with prediabe-
tes prior to old age. Recently, a T2DM prevalence screening
study was conducted in the Faroe Islands based on glycated
hemoglobin (HbA1c levels) and an oral glucose tolerance
test (OGTT; Veyhe et al personal communication). The study
demonstrated a high prevalence, with ~10% of the population
between 40 and 74 years being diagnosed with T2DM and
another ~15% having glycemic disturbances. This national
cohort was used to recruit participants with prediabetes aged
55- 70 years of age to take part in this study.
Thus, the aim of this study was to test the hypothesis that
football training combined with dietary advice is more ef-
ficient as a treatment protocol for patients with prediabetes
aged 55- 70 years than dietary advice alone.
Please click on this video link to hear more about the
study.
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MATERIALS AND METHODS
2.1
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Participants
The participants in this study were recruited from a
population- based cross- sectional survey which aimed to de-
termine the prevalence of T2DM and prediabetes among the
population aged 40- 74 years in the Faroe Islands. The study
included 1772 individuals (corresponding to ~10% of the
entire population aged 40- 74 years) (Veyhe et al, personal
communication).
A total of 117 individuals aged 55- 70 years living on the
Faroe Islands at the recruiting time diagnosed with predia-
betes (HbA1c ≥ 5.8% (40 mmol·mol−1)) received a letter of
invitation to participate in the study. The letter contained in-
formation about the study and the various tests that the par-
ticipants would undergo. Thereafter, the letter was followed
up by a phone call to clarify any questions and to invite the
patients to an informational group meeting near their resi-
dence. Participants that took part in regular physical activity
were excluded. Participants using beta- blockers were also ex-
cluded, while participants using other antihypertensive drugs
such as thiazides and angiotensin receptor blockers (n = 25)
were included. In addition, participants taking medication for
high plasma cholesterol levels such as statins (n = 16) were
included. Finally, three participants included in the study
were taking anti- asthmatic drugs. None of the participants
changed their drug usage during the intervention period.
After being informed in writing and verbally of the experi-
mental procedures and associated risks, 55 persons (28 men
and 27 women; see Table 1) accepted to participate in the
study and gave their written consent. The study was approved
by the ethical committee of the Faroe Islands and conducted
in accordance with the Declaration of Helsinki (1964).
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SKORADAL etAL.
2.2
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Experimental design
The study was designed as a randomized controlled trial.
The participants reported to the laboratory on four sepa-
rate occasions over a 12- day period. On visit 1, the par-
ticipants had a fasting blood sample taken and completed
an oral glucose tolerance test (OGTT), as described by
Connolly et al15 In addition, blood pressure and resting
heart rate were recorded. On visit 2, body composition was
assessed with a DXA scan, scaling body mass, and measur-
ing waist and hip circumference, as previously.16 On visit
3, the participants performed an incremental cycling test to
exhaustion with measurements of maximal oxygen uptake
(VO2max), pulmonary ventilation (VE), and maximal heart
rate (HRmax). The primary endpoint was blood glucose ki-
netics during the OGTT, whereas the secondary endpoints
were blood lipid profile, body composition, blood pressure,
resting heart rate, and VO2max. On visit 4, dietary advice
was given by a registered dietitian in a 3- hours group- based
session. Subsequently, the participants were randomized to
a football and dietary advice group (F+D; n = 32) and a
dietary advice group (D; n = 23). Males and females were
randomized separately to ensure an equal gender distribu-
tion in the two groups. There were five dropouts from the
F+D group (due to low training attendance; <1 session per
week, which was the minimum criteria for training comple-
tion), of which two were men and three were women, re-
sulting in 27 participants completing the F+D intervention.
There were no dropouts from D (n = 23). Thus, the final
sample consisted of 50 participants. There were examples
of severe muscle soreness as result of the football training
in the initial phase of the intervention period, but no serious
injuries occurred.
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Resting blood sampling and
OGTT testing
On the day of testing, the participants reported to the lab-
oratory after transport by car or bus. No training was per-
formed 48- 72 hours prior to testing, and the participants were
instructed to avoid physical activity on the day prior to the
OGTT tests. Using a venipuncture technique, a resting blood
sample was taken under standardized conditions from an
antecubital vein between 7 am and 8 am after an overnight
fast. The blood was rapidly centrifuged for 30 seconds and
the plasma collected and analyzed by an automatic analyzer
(Cobas Fara, Roche, France) using enzymatic kits (Roche
Diagnostics, Germany) to determine plasma total cholesterol,
HDL, LDL, triglycerides, C- reactive protein, and vitamin D.
Additionally, an OGTT test was performed as previously
described,17 with blood samples taken after 0, 30, 60, and
120 minutes and analyzed for plasma [glucose] using enzy-
matic kits (Roche Diagnostics, Germany). Changes in plasma
[glucose] during the OGTT were also quantified using total
area under the curve (tAUC) analyses employing the trape-
zium rule (GraphPad Prism, San Diego, CA). The intra- assay
coefficient of variations for glucose is 3.0 ± 3.5%.
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Maximal oxygen uptake, pulmonary
ventilation, and performance
On a separate day, the participants reported to the laboratory
in a postabsorptive state (at least 4 hours), having refrained
from vigorous exercise, alcohol, tobacco, and caffeine dur-
ing the previous 24 hours. To ensure standardization of nu-
tritional and hydration status, the participants recorded their
food and fluid intakes for the 48- hours period prior to the
first trial so that the diet could be repeated for the remainder
of the trial. The participants did not consume any fluid dur-
ing the experimental trials. Maximal oxygen consumption
(VO2max) was determined for each individual by means of an
incremental cycling test to volitional exhaustion on an elec-
tronically braked cycle ergometer (Excalibur Sport, Lode,
Groningen, Netherlands). The test was performed under
standard laboratory conditions (20°C; 40% relative humid-
ity). VO2max was determined as the highest value achieved
over a 20- seconds period. A plateau in VO2, despite an in-
creased speed, and a respiratory exchange ratio (RER) >1.15
were used as criteria for VO2max achievement. The test was
initiated at 0 W and increased by 20 W every minute until
Age (y) Height (cm) Weight (kg) BMI (kg·m−2) VO2max (mL·min−1·kg−1)
All participants (n = 50)
61 ± 6 171 ± 9 86.9 ± 17.1 29.6 ± 4.7 22.3 ± 5.7
Football+Diet (F+D; n = 27)
60 ± 6 172 ± 8 85.0 ± 15.1 28.6 ± 4.1 24.9 ± 5.3
Diet (D; n = 23)
62 ± 6 170 ± 9 89.9 ± 18.4 30.9 ± 4.9 20.2 ± 4.8*
Data are mean±SD.
Significance level P < .05.
*Denotes a significant difference from D.
TABLE 1 Participant characteristics,
including age and baseline body
composition and maximal oxygen uptake of
the total participant sample recruited for the
study
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SKORADAL etAL.
the participants could no longer handle the given load. The
participants maintained a cadence of 60, 65, or 70 rep·min−1
based on individual preference. Pulmonary VO2 and VE were
measured throughout the protocol by a breath- by- breath gas
analyzing system (model Cosmed, Quark b2, Milan, Italy).
The analyzer was calibrated before each test with two gases
of known oxygen and carbon dioxide concentrations as well
as by the use of a 3- liter syringe for the tube flowmeter cali-
bration. The end- power output (cycling load at the point of
volitional exhaustion) was noted as the exercise performance
marker.
2.5
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Blood pressure measurements
The participants reported at the hospital at 8.00 am after an
overnight fast and rested in a supine position for 2 hours.
Systolic blood pressure (SBP) and diastolic blood pressure
(DBP) were measured according to standard procedures18
using an automatic BP monitor (HEM- 709; OMRON, IL,
US) once every 30 minutes over the 2- hours resting period.
The average of the four measurements was used as the test re-
sult. Mean arterial pressure (MAP) was calculated as 1/3 SBP
+ 2/3 DBP. Resting heart rate (RHR) was measured during
the same time intervals as for BP.
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Body composition
Whole- body fat and lean body mass (LBM) were evaluated
by total- body DXA scanning (Norland XR- 800, Norland
Corporation, Oslo, Norway). The body was segmented in ac-
cordance with standard procedures to evaluate regional tissue
distribution, and all analyses were performed using Illuminatus
DXA software (Norland Corporation, Oslo, Norway). The ef-
fective radiation dose was <0.2 mSv per scan.
2.7
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Training intervention
The F+D participants completed a total of 32 ± 2 (19- 46)
football training sessions over the 16- week intervention pe-
riod, corresponding to 2.0 ± 0.1 (1.2- 2.9) sessions per week.
Four training sessions were organized by week, and the par-
ticipants were encouraged to take part in 2- 3 sessions per
week. Each session lasted 30- 60 minutes (30 minutes during
weeks 0- 2, 40 minutes during weeks 3- 4, 50 minutes during
weeks 5- 6, and 60 minutes during weeks 7- 16). The sessions
were organized with two halves separated by 2- 3 minutes
of recovery). All sessions were organized as small- sided
games (4v4- 6v6), as previously described.19 All sessions
were preceded by a 10- minutes warm- up period.16 Heart rate
was measured during one training session in week 4 and one
session in week 12 of the intervention, and mean and peak
heart rate were 127 ± 5 and 153 ± 4 bpm, respectively, cor-
responding to 79 ± 1 and 96 ± 1%HRmax, respectively.
2.8
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Dietary intervention
All participants were given group- based dietary advice by
a registered dietitian and provided with a standardized meal
plan. The meal plan aimed to improve glycemic control, to
reduce the risk of worsening the cardiometabolic profile, and
to maintain a healthy body weight. Weight loss in diabetic
subjects may provide clinical benefits such as improved gly-
cemia, blood pressure and lipids.4 Thus, the meal plan was
semilow caloric providing 1800 and 2300 kilocalories per
day for women and men, respectively. Studies of group-
based diabetes education have reported HbA1C decreases of
0.5%- 2.0% for patients with T2DM.4 The main principles of
the meal plan were substituting high- starch and high- sucrose
foods with low- glycemic natural fiber- rich plant foods.20 In
accordance with the official Danish dietary recommenda-
tions, the recommended vegetable intake was 300 g per day
and fruit consumption was limited to two to three pieces per
day in order to limit fructose intake.20,21 The participants were
instructed to minimize the consumption of sucrose- containing
foods, especially sugar- sweetened beverages, and to substi-
tute starchy foods with wholemeal foods such as wholemeal
bread, pasta, and rice.22 The recommended intake of saturated
fat, dietary cholesterol, and trans fat is the same for diabetic
subjects as for the healthy population.4,22 However, based on
Danish dietary surveys, the participants were advised to in-
crease the consumption of foods containing long- chain n- 3
fatty acids (EPA and DHA) from fatty fish. 23
2.9
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Statistical analysis
Data are presented as means ± SD. Statistical analyses were
performed using SPSS v.22. A two- factor mixed ANOVA
design with the between- factor “group” (F+D vs D) and
FIGURE 1 Whole- body fat percentage (%) preintervention
(black bars) and postintervention (white bars) in F+D and D. # denotes
a significant difference in change score compared to D. * denotes
a significant difference from preintervention. Significance level is
P < .05
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SKORADAL etAL.
repeated factor “condition” (pre- vs postintervention) was
used. When significant main effects were detected, data were
subsequently analyzed using Bonferroni post- hoc t tests. The
significance level was P < .05.
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RESULTS
3.1
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Body composition
Body mass was 85.0 ± 15.1 and 89.9 ± 18.4 kg at base-
line in F+D and D, respectively. Body mass was lowered
(P < .05) by 2.4 ± 2.9 kg postintervention in F+D with a
greater (P < .05) change score than D (1.5 ± 3.4 kg). Total
body fat percentage was 35.3 ± 8.7 and 39.1 ± 9.9% at base-
line in F+D and D, but declined (P < .05) more in F+D
than in D, being 32.1 ± 9.0 and 38.3 ± 9.8%, respectively,
postintervention. The intervention- induced fat loss in F+D
was −3.4 ± 2.8 kg, which was greater (P < .05) than in D
(−1.2 ± 2.0 kg; Figure 1). LBM was similar in F+D and D
(53.3 ± 11.9 and 53.6 ± 14.2 kg, respectively) and increased
(P < .05) from pre- to postintervention by 0.7 ± 1.5 kg in
F+D, which was more (P < .05) than in D (−0.3 ± 1.6 kg;
Figure 1). Hip and waist circumference were 102 ± 8 and
98 ± 7 cm in F+D and 105 ± 11 and 103 ± 10 cm in D pre-
intervention, and waist circumference was lowered (P < .05)
by 5 ± 4 cm in F+D and 2 ± 5 cm in D postintervention,
with a greater (P < .05) change score in F+D than in D.
3.2
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Blood pressure
SBP and DBP were 138 ± 16 and 84 ± 11 mm Hg in F+D
and 142 ± 18 and 87 ± 11 mm Hg in D at baseline, but
FIGURE 2 Systolic blood pressure (SBP), diastolic blood
pressure (DBP), and mean arterial pressure (MAP; mm Hg)
preintervention (black bars) and postintervention (white bars) in F+D
and D. #denotes a significant difference in change score compared to
D. *denotes a significant difference from preintervention. Significance
level is P < .05
FIGURE 3 Maximal oxygen uptake (VO2max) preintervention
(black bars) and postintervention (white bars) in F+D and D. #denotes
a significant difference in change score from D. *denotes a significant
difference from preintervention. Significance level is P < .05
FIGURE 4 Blood glucose during an OGTT in F+D (A) and D
(B) pre- and postintervention. *denotes a significant difference from
preintervention. Significance level is P < .05
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SKORADAL etAL.
decreased (P < .05) to 127 ± 15 and 77 ± 10 mm Hg in
F+D, which was a greater (P < .05) change score than in D
(Figure 2). MAP was reduced (P < .05) by −8 ± 9 mm Hg
in F+D and showed a greater (P < .05) change score than D
(−4 ± 11 mm Hg; Figure 2).
3.3
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Maximal oxygen uptake, pulmonary
ventilation, and resting heart rate
F+D had an intervention- induced increase (P < .05) in
VO2max of 3.4 ± 3.0 mL·min−1·kg−1, corresponding to 14%,
which was greater (P < .05) than a nonsignificant change of
0.5 ± 5.9 mL·min−1·kg−1 in D (Figure 3). VE was 74.2 ± 14.2
and 67.5 ± 15.5 L·min−1 in F+D and D, respectively, at base-
line with higher (P < .05) values in F+D. Postintervention,
VE was increased (P < .05) by 5.0 ± 10.0 L·min−1 in F+D
with a greater change score than in D (0.3 ± 11 L·min−1).
End- power output was 183 ± 36 and 173 ± 43 W at base-
line in F+D and D, respectively. Postintervention, F+D had
increased (P < .05) end- power output by 10%, which was a
greater change than in the D group. RHR was 73 ± 10 and
72 ± 12 b·min−1 in F+D and D at baseline, but was lowered
postintervention in F+D only (−5 ± 5 vs −2 ± 4 b·min−1).
3.4
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Plasma glucose
The fasting plasma glucose concentration was 6.2 ± 0.7 and
6.2 ± 0.8 mmol·L−1 in F+D and D at baseline and was low-
ered (P < .05) postintervention by 0.4 ± 0.7 mmol·L−1 in
both groups (Figure 4). Plasma glucose during the OGTT was
lower (P < .05) at all- time points postintervention compared to
preintervention in F+D and D (Figure 4). At 60 and 120 min-
utes, the postintervention plasma glucose concentration was
9.0 ± 2.7 and 5.7 ± 1.6 mmol·L−1 in F+D, which was lower
(P < .05) than in D (10.6 ± 2.9 and 7.5 ± 2.4 mmol·L−1).
Plasma glucose values were back at baseline after 120 min-
utes in F+D, but not in D (Figure 4). Preintervention tAUC
was 1092 ± 281 and 1240 ± 230 mmol·min−1·L−1 in F+D
and D, respectively, and was lowered (P < .05) to 957 ± 203
and 1095 ± 221 mmol·min−1·L−1 postintervention with no
difference in change score. However, postintervention tAUC
was lower (P < .05) in F+D than in D.
3.5
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Blood lipid profile, C- reactive
protein, and vitamin D
F+D showed a greater (P < .05) intervention- induced de-
crease (−0.5 ± 0.5 mmol·L−1) in total plasma cholesterol in
comparison with D (0.0 ± 0.5 mmol·L−1; Table 2). Plasma
LDL cholesterol was also lowered (−0.3 ± 0.5 mmol·L−1)
in F+D only with a greater change score than D
(+0.1 ± 0.4 mmol·L−1), while HDL was unchanged in both
groups (Table 2). Plasma triglyceride concentrations were
reduced (P < .05) in F+D (−0.2 ± 0.5 mmol·L−1) only with
no between- group differences (Table 2). Plasma CRP and vi-
tamin D were unaltered during the intervention period in both
groups (Table 2). Plasma CRP tended to decrease (P = .06)
in D only (Table 2), while plasma vitamin D was unchanged
in both groups during the intervention period (Table 2).
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DISCUSSION
The present study is the first to examine the impact of foot-
ball training on 55- to 70- year- old patients with prediabetes.
The results demonstrate that 16 weeks of football training
combined with dietary advice causes broad- spectrum posi-
tive effects on metabolic and cardiovascular health profile in
individuals with prediabetes and that the effects are greater
than professional dietary advice alone.
Patients with T2DM, prediabetes, or metabolic syndrome
are more likely to have cardiovascular deficiencies than
healthy individuals.6,9 In the present study, the participants
were moderately hypertensive prior to the intervention, but
F+D D
Pre Post Pre Post
Total cholesterol (mmol·L−1) 5.5 ± 0.9 5.0 ± 1.0*# 5.0 ± 1.3 5.0 ± 1.2
HDL cholesterol (mmol·L−1) 1.4 ± 0.3 1.4 ± 0.3 1.4 ± 0.4 1.4 ± 0.3
LDL cholesterol (mmol·L−1) 3.5 ± 0.8 3.2 ± 0.9*# 3.0 ± 1.1 3.1 ± 1.0
Triglycerides (mmol·L−1) 1.4 ± 0.6 1.2 ± 0.3*1.4 ± 1.0 1.3 ± 0.7
CRP (mg·L−1) 3.8 ± 4.5 3.6 ± 4.3 3.8 ± 3.8 3.2 ± 4.3
Vitamin D (nmol·L−1) 62.1 ± 27.7 63.1 ± 28.0 55.7 ± 24.8 54.1 ± 22.6
Plasma lipid profile, C- reactive protein (CRP), and vitamin D in F+D (n = 27) and D (n = 23).
Data are mean±SD.
Significance level P < .05.
*Denotes a significant difference from preintervention.
#Denotes a significant difference in change score compared to D.
TABLE 2 Plasma parameters pre- and
postintervention
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SKORADAL etAL.
both groups showed a decrease in systolic and diastolic blood
pressure postintervention (Figure 2). However, the football
group showed a drop in mean arterial pressure of 8 mm Hg,
which was higher than the diet group, and which is on a com-
parable magnitude as conventional pharmacological agents
used for blood pressure management. Indeed, the football
training group was actually able to normalize systolic and di-
astolic blood pressure (127 and 77 mm Hg) in just 16 weeks.
These findings are supported by other football training stud-
ies in hypertensive women.10 Small- sided football games
have been shown to induce high cardiovascular loading,19
which is confirmed by mean and peak heart rates of 80 and
95% HRmax, respectively, in the present study. Moreover, the
F+D group showed a markedly improved blood lipid pro-
file postintervention, with a decrease in total cholesterol of
0.5 mmol·L−1 as well as a drop in plasma triglyceride con-
centration. These findings are confirmed by numerous other
football training interventions in various women subject
groups.9 Thus, football training in combination with dietary
advice markedly improves cardiovascular health in 55- to
70- year- olds with prediabetes.
The F+D intervention induced an increase of
~3.5 mL·min−1·kg−1 in maximal oxygen uptake, which is
clinically significant.23 Low cardiorespiratory fitness is a
common characteristic in patients with T2DM,10,24 and the
baseline values of the participants with prediabetes in the
present study confirm these findings. These participants
were 55- to 70- year- olds, and it is evident that physiological
aging causes a decline in VO2max of 5%- 10% per decade.25
Thus, patients with prediabetes in this age group are likely
to display low aerobic fitness values, which has an impact
on their cardiorespiratory health. Consequently, the observed
improvement in VO2max is highly important for this patient
group, as patients with T2DM who increase their level of
cardiorespiratory fitness of approximately 5 mL·kg−1·min−1
have a significant reduction in overall cardiovascular mortal-
ity of 39%- 70%.23,26 The 14% increase in VO2max is approxi-
mately at the same level or even higher than shown previously
after football interventions lasting 12- 52 weeks.8 In addition,
a recent meta- analysis confirmed that football training is
most likely largely beneficial (effect size=1.14) for increas-
ing VO2max and may be more efficient than other training
methods such as running and strength training.27 Moreover,
football training interventions demonstrate the same magni-
tude effects on VO2max as reported in meta- analysis of high-
intensity interval training.28 Thus, football training appears
to be a highly efficient training method for increasing the
cardiorespiratory health status of patients with prediabetes.
In addition to the improved aerobic capacity, the football
training intervention also increased cycling performance
and lowered resting heart rate, despite that the latter change
was not significantly different from the diet group. Physical
performance and resting heart rate are both independent
health markers.29 For example, a high resting heart rate is
statistically related to increased risk of hypertension, vascular
oxidative stress, endothelial dysfunction, and accelerated ath-
erosclerosis,30 which further highlights the broad- spectrum
health benefits of football training.
Another principal finding of the present study was that
fasting plasma glucose concentrations declined from 6.2
to 5.8 mmol·L−1 in both intervention groups, which means
that the average values decline below the clinical thresh-
old of impaired blood glucose control. Moreover, tAUC in
the OGTT was lowered postintervention, and collectively
these results demonstrate clear improvements in blood glu-
cose regulation and an attenuation of the risk of develop-
ing T2DM with both interventions being beneficial for the
respective patient group. Interestingly, the F+D interven-
tion group displayed lower postintervention plasma glu-
cose concentrations at 60 and 120 minutes of the OGTT
and had a lower absolute tAUC compared to the D group,
despite a similar change score in both groups. Hence,
football training performed twice weekly as small- sided
games for 16 weeks in conjunction with dietary advice
may be slightly more effective than dietary advice alone.
Indeed, postintervention the football group, in contrast to
the diet group, was able to normalize the plasma glucose
concentration to baseline values at the end of the OGTT
(see Figure 4), which indicates a decreased risk of progres-
sion of diabetes.31 These findings are in accordance with a
recent study applying a combined football and diet inter-
vention to patients with T2DM, which also demonstrated
greater adaptations in glucose regulation than a calorie-
restricted diet alone.10 However, it should be noted that it
is a limitation in the present study that the intervention-
induced effects on HbA1c and insulin were not measured,
that the absolute tAUG values were nonsignificantly higher
preintervention in D than F+D, and that no between- group
effects were present.
An independent risk factor for insulin resistance and
T2DM is obesity, and especially abdominal fat accumulation,
which is also detrimental to cardiovascular homeostasis.32 In
the present study, the football intervention induced a markedly
greater fat loss (~3.5 kg) compared to dietary advice alone. In
addition, waist circumference F+D was reduced more than
twice as much in comparison with D. The large decrease in
body fat content after 4 months of football training is in line
with findings in sedentary men33 and women,8 as well as
various female patient groups.9 In addition, cross- sectional
studies in elderly football players show markedly lower body
fat content than age- matched sedentary controls.34 Recently,
we demonstrated that 15 weeks of football training in middle-
aged sedentary hypertensive women upregulated skeletal
muscle mitochondrial function and β- oxidative capacity,9
which is also supported by increased whole- body fat oxida-
tion during exercise after a football training intervention.8
8
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SKORADAL etAL.
Thus, it is plausible to suggest that increased muscle fat ox-
idative capacity contributed to the decrease in body fat con-
tent in the football group. Part of the pathology in T2DM is
low skeletal muscle mitochondrial function.35
Type 2 diabetes is closely linked not only with obesity
but also with low muscle mass,7 and a consistent finding in
football training studies across the lifespan is an increase in
muscle mass.8,16,36 Additionally, in the present study the F+D
group had a ~1 kg increase in lean body mass compared to
the D group. The higher muscle mass provides a larger po-
tential total muscle glycogen storage capacity, which is likely
to improve clearance of glucose from the bloodstream.37 This
adaptation may have added to the effect on postintervention
glucose control in F+D.
The current exercise recommendation for patients with di-
abetes is at least 150 minutes per week of moderate- intensity
aerobic physical activity combined with resistance training.5
However, the present findings and other recent investigations
indicate that high- intensity intermittent training may be essen-
tial for improving metabolic and cardiovascular health profile
in sedentary populations15 as well as in individuals with10 or
at risk of32 T2DM. As football represents a complex training
method encompassing simultaneous endurance, high- intensity
exercise and resistance training,8 this type of training modality
may be well suited as an exercise training therapy for patients
with prediabetes. In the study by de Sousa et al,10 the authors
prescribed 12 weeks of football training (40 minutes 3 times
per week) combined with a calorie- restricted diet for 48- to
68- year- old patients with T2DM. The combined intervention
augmented insulin sensitivity more efficiently than dietary
advice alone with concomitant increases in maximal oxygen
uptake and improvement in blood lipid profile, as found in the
current study of patients with prediabetes. The participants in
the present study trained on average 60- 120 minutes per week,
which questions the above- mentioned 150 minutes per week
recommendation for patients with prediabetes. Prevalence of
T2DM increases with age,13 and a sedentary lifestyle is proven
to be a valid predictor of mortality in patients with T2DM.14
However, mortality risk can be attenuated by physical train-
ing in the aging population.7 The patient group in the present
study was recruited from a cohort in the Faroe Islands where
~10 and ~15% of the population between 40 and 79 years had
T2DM and prediabetes, respectively (Veyhe et al, personal
communication) Type 2 diabetes is a major worldwide health
challenge, causing considerable morbidity and mortality,1,2
and is imposing a significant economic burden on the health-
care system. Thus, treating patients with prediabetes with
lifestyle changes, such as the combination of football training
and diet alterations, may offer excellent prospects and may be
integrated into the “Exercise as Medicine” concept.7 The fact
that no serious injuries occurred as result of the football train-
ing in a fragile group with low physical capacity supports this
notion.
A limitation in the present study is that we did not monitor
the impact of the diet advice on the eating habits during the
intervention period. Therefore, it is not possible to evaluate
to what degree the participants followed the recommenda-
tions. However, both groups received the diet advice, which
may limit potential bias of the applied approach. In addition,
we did not perform any assessment of the daily activity level
of the participants, which may have affected the results.
However, none of the participants took part in regular physi-
cal training prior or during the intervention period.
In conclusion, 16 weeks of football training combined
with dietary advice have broad- spectrum effects on meta-
bolic and cardiovascular health profile for 55- to 70- year- old
men and women with prediabetes, with greater overall effects
than professional dietary advice per se.
5
|
PERSPECTIVES
Individuals suffering from prediabetes usually have broad-
spectrum pathophysiological challenges such as poor
cardiovascular health, obesity, low muscle mass, and cardi-
orespiratory fitness, and the observed broad- spectrum health
effects of football training are therefore highly relevant for
this patient group. The results of the present study are with
line with other recent studies using small- sided football train-
ing, emphasizing that just 2 hours of training per week in
combination with dietary advice seems to be a feasible and
efficient approach to improve the overall fitness level and
health profile of untrained female and male patients across
the lifespan. In the present study, elderly women and men
trained together, and the positive fitness and health adapta-
tions occurred independently of skill level and gender, dem-
onstrating that mixed- gender football training can be applied
as treatment for patients with prediabetes, which may have
some socio- psychological benefits.
ACKNOWLEDGEMENTS
The authors would like to express their appreciation for the
outstanding efforts and positive attitude of the participants.
In addition, we are extremely grateful for the technical as-
sistance provided by Sólfríð Skoradal, Jan Poulsen, Annika
Gleðisheygg, Hjalti Gleðisheygg, Charlotta Nielsen, Brandur
Jacobsen, Súsanna Holm, Noomi Holm, Johild Dulavík,
Liljan av Fløtum, Kristianna Dam, Jens Andreassen,
Ivy Hansen, Gunnrið Jóannesarson, Ann Østerø, Nina
Djurhuus, Ebba Andreassen, Maud av Fløtum, Janus Vang,
Ronnie Midjord, and Jens Jung Nielsen. The study was
supported by a grant from the Faroese Research Council
(Sjúkakassagrunnurin), as well as by the Faroese Football
Association (Fótbóltssamband Føroya; FSF) and the Faroese
Diabetes Organisation (Diabetesfelag Føroya).
|
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SKORADAL etAL.
ORCID
P. Krustrup http://orcid.org/0000-0002-1461-9838
REFERENCES
1. Yang W, Dall TM, Halder P, Gallo P, Kowal SL, Hogan PF.
Economic Costs of Diabetes in the U.S. in 2012. Diabetes Care.
2013;36:1033‐1046.
2. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prev-
alence of diabetes for 2010 and 2030. Diabetes Res Clin Pract.
2010;87:4‐14.
3. Boyle JP, Thompson TJ, Gregg EW, Barker LE, Williamson DF.
Projection of the year 2050 burden of diabetes in the US adult
population: dynamic modeling of incidence, mortality, and predi-
abetes prevalence. Popul Health Metr. 2010;8:29‐40.
4. American Diabetes Association. Lifestyle management Sec. 4.
In standards of medical care in diabetesd 2017. Diabetes Care
2017;40(Suppl 1):S33‐S43.
5. Jagannathan R, Bergman M. Use of 1- h post- load plasma glucose
concentration to identify individuals at high risk of developing
Type 2 diabetes. Diabet Med. 2017;34:877‐878.
6. Flores-Le Roux JA, Comin J, Pedro-Botet J, et al. Seven- year
mortality in heart failure patients with undiagnosed diabetes: an
observational study. Cardiovasc Diabetol. 2011;10:39.
7. Pedersen BK, Saltin B. Exercise as medicine - evidence for pre-
scribing exercise as therapy in 26 different chronic diseases.
Scand J Med Sci Sports. 2015;3:25.
8. Krustrup P, Aagaard P, Nybo L, Petersen J, Mohr M, Bangsbo
J. Recreational football as a health promoting activity: a topical
review. Scand J Med Sci Sports. 2010;20:1‐13.
9. Krustrup P, Helge EW, Hansen PR, etal. Effects of recreational
football on women’s fitness and health: adaptations and mecha-
nisms. Eur J Appl Physiol. 2018;118:11‐32.
10. De Sousa MV, Fukui R, Krustrup P, et al. Positive effects
of football on fitness, lipid profile, and insulin resistance in
Brazilian patients with type 2 diabetes. Scand J Med Sci Sports.
2014;24:57‐65.
11. De Sousa MV, Fukui R, Krustrup P, Dagogo-Jack S, Rossi da
Silva ME. Combination of recreational soccer and caloric re-
stricted diet reduces markers of protein catabolism and cardiovas-
cular risk in patients with Type 2 diabetes. J Nutr Health Aging.
2017;21:180‐186.
12. Pedersen BK, Saltin B. Evidence for prescribing exercise
as therapy in chronic disease. Scand J Med Sci Sports.
2006;16:3‐63.
13. Ringborg A, Lindgren P, Martinell M, Yin DD, Schön S,
Stålhammar J. Prevalence and incidence of Type 2 diabetes and its
complications 1996- 2003–estimates from a Swedish population-
based study. Diabet Med. 2008;25:1178‐1186.
14. Kohl HW, Gordon NF, Villegas JA, Blair SN. Cardiorespiratory
fitness, glycemic status, and mortality risk in men. Diabetes Care.
1992;15:184‐192.
15. Connolly LJ, Nordsborg NB, Nyberg M, Weihe P, Krustrup P,
Mohr M. Low- volume high- intensity swim training is superior
to high- volume low- intensity training in relation to insulin sensi-
tivity and glucose control in inactive middle- aged women. Eur J
Appl Physiol. 2016;116:1889‐1897.
16. Mohr M, Lindenskov A, Holm PM, etal. Football training im-
proves cardiovascular health profile in sedentary, premenopausal
hypertensive women. Scand J Med Sci Sports. 2014;24:36‐42.
17. Durrer C, Robinson E, Wan Z, etal. Differential impact of acute
high- intensity exercise on circulating endothelial microparticles
and insulin resistance between overweight/obese males and fe-
males. PLoS ONE. 2015;24:10.
18. Krustrup P, Randers MB, Andersen LJ, Jackman SR, Bangsbo
J, Hansen PR. Soccer improves fitness and attenuates cardiovas-
cular risk factors in hypertensive men. Med Sci Sports Exerc.
2013;45:553‐560.
19. Randers MB, Nielsen JJ, Krustrup BR, etal. Positive performance
and health effects of a football training program over 12weeks
can be maintained over a 1- year period with reduced training fre-
quency. Scand J Med Sci Sports. 2010;20:80‐89.
20. Wheeler ML, Dunbar SA, Jaacks LM, Karmally W, Mayer-
Davis EJ, Wylie-Rosett J. Yancy WS Jr. Macronutrients, food
groups, and eating patterns in the management of diabetes:
a systematic review of the literature, 2010. Diabetes Care.
2012;35:434‐445.
21. Danish Veterinary and Food Administration. De officielle kostråd
[The official dietary advice]. 2013:1–28. http://altomkost.dk/en-
glish/#c41067. Accessed June, 15, 2017
22. Nordic Council of Ministers. Nordic Nutrition Recommendations.
Integrating Nutrition and Physical Activity. 5th ed. Nordic
Council of Ministers, ed. Copenhagen, Denmark: Norden; 2012.
https://www.norden.org/en/publications/publikationer/2014-002\
nhttp://urn.kb.se/resolve?urn=urn:nbn:se:norden:org:diva-2561.
Accessed June 15, 2017.
23. Milanović Z, Pantelić S, Čović N, Sporiš G, Krustrup P. Is rec-
reational soccer effective for improving VO2max A systematic
review and meta- analysis. Sports Med. 2015;45:1339‐1353.
24. Regensteiner JG, Sippel J, McFarling ET, Wolfel EE, Hiat
WR. Effects on non- insulin- dependent diabetes on oxygen
consumption during treadmill exercise. Med Sci Sports Exerc.
1995;27:875‐881.
25. Hawkins SA, Wiswell RA. Rate and mechanism of maxi-
mal oxygen consumption decline with aging. Sports Med.
2003;33:877‐888.
26. Church TS, LaMonte MJ, Barlow CE, Blair SN. Cardiorespiratory
fitness and body mass index as predictors of cardiovascular dis-
ease mortality among men with diabetes. Arch Intern Med.
2005;165:2114‐2120.
27. Kostić R, Uzunović S, Purenović-Ivanović T, etal. The effects of
dance training program on the postural stability of middle aged
women. Cent Eur J Public Health. 2015;23:67‐73.
28. Weston M, Taylor KL, Batterham AM, Hopkins WG. Effects of
low- volume high- intensity interval training (HIT) on fitness in
adults: a meta- analysis of controlled and non- controlled trials.
Sports Med. 2014;44:1005‐1017.
29. Lee IM, Shiroma EJ, Lobelo F, Puska P, Blair SN, Katzmarzyk
PT. Effect of physical inactivity on major non- communicable dis-
eases worldwide: an analysis of burden of disease and life expec-
tancy. Lancet. 2012;380:219‐229.
30. Custodis F, Schirmer SH, Baumhäkel M, Heusch G, Böhm M,
Laufs U. Vascular pathophysiology in response to increased heart
rate. J Am Coll Cardiol. 2010;7:1973‐1983.
31. Abdul-Ghani MA, Williams K, DeFronzo R, Stern M. Risk of
progression to type 2 diabetes based on relationship between
10
|
SKORADAL etAL.
postload plasma glucose and fasting plasma glucose. Diabetes
Care. 2006;29:1613‐1618.
32. Little JP, Francois ME. High- intensity interval training for
improving postprandial hyperglycemia. Res Q Exerc Sport.
2014;85:451‐456.
33. Bangsbo J, Hansen PR, Dvorak J, Krustrup P. Recreational foot-
ball for disease prevention and treatment in untrained men: a nar-
rative review examining cardiovascular health, lipid profile, body
composition, muscle strength and functional capacity. Br J Sports
Med. 2015;49:568‐576.
34. Randers MB, Andersen JL, Petersen J, etal. Exercise performance
and cardiovascular health variables in 70- year- old male soccer
players compared to endurance- trained, strength- trained and un-
trained age- matched men. J Sports Sci. 2014;32:1300‐1308.
35. Wojtaszewski JF. AMP- activated protein kinase in sickness and
health–from molecule to man. Acta Physiol (Oxf). 2009;196:1.
36. Barene S, Krustrup P, Jackman SR, Brekke OL, Holtermann A.
Do soccer and Zumba exercise improve fitness and indicators of
health among female hospital employees? A 12- week RCT. Scand
J Med Sci Sports. 2014;24:990‐999.
37. Krustrup P, Söderlund K, Mohr M, Bangsbo J. Slow- twitch fiber
glycogen depletion elevates moderate- exercise fast- twitch fiber
activity and O2 uptake. Med Sci Sports Exerc. 2004;36:973‐982.
How to cite this article: Skoradal M-B, Weihe P,
Patursson P, etal. Football training improves
metabolic and cardiovascular health status in 55- to
70- year- old women and men with prediabetes. Scand
J Med Sci Sports. 2018;00:1–10.
https://doi.org/10.1111/sms.13081