effects of recreational football on women’s fitness and...
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European Journal of Applied Physiology https://doi.org/10.1007/s00421-017-3733-7
INVITED REVIEW
Effects of recreational football on women’s fitness and health: adaptations and mechanisms
Peter Krustrup1,2 · Eva Wulff Helge3 · Peter R. Hansen4 · Per Aagaard1 · Marie Hagman1 · Morten B. Randers1 · Maysa de Sousa5 · Magni Mohr1,6,7
Received: 29 June 2017 / Accepted: 28 September 2017 © Springer-Verlag GmbH Germany 2017
AbstractThe review describes the fitness and health effects of recreational football in women aged 18–65 years. The review docu-ments that 2 × 1 h of recreational football training for 12–16 weeks causes marked improvements in maximal oxygen uptake (5–15%) and myocardial function in women. Moreover, mean arterial blood pressure was shown to decrease by 2–5 mmHg in normotensive women and 6–8 mmHg in hypertensive women. This review also show that short-term (< 4 months) and medium-term (4–16 months) recreational football training has major beneficial impact on metabolic health profile in women, with fat losses of 1–3 kg and improvements in blood lipid profile. Lastly, 2 × 1 h per week of recreational football training for women elevates lower extremity bone mineralisation by 1–5% and whole-body bone mineralization by 1–2% within 4–12-month interventions. These training adaptations are related to the high heart rates, high number of fast runs, and multiple changes of direction and speed occurring during recreational football training for untrained women. In conclusion, regular small-sided football training for women is an intense and versatile type of training that combines elements of high-intensity interval training (HIIT), endurance training and strength training, thereby providing optimal stimuli for cardiovascular, metabolic and musculoskeletal fitness. Recreational football, therefore, seems to be an effective tool for prevention and treatment of lifestyle diseases in young and middle-aged women, including hypertension, type 2 diabetes and osteopenia. Future research should elucidate effects of football training for elderly women, and as treatment and rehabilitation of breast cancer patients and other women patient groups.
Keywords Cardiovascular · Metabolic · Musculoskeletal · Training · Body composition · Blood pressure
Introduction
It is now well documented that physical inactivity increases the risk of several adverse health conditions, including major non-communicable diseases such as coronary heart disease,
type 2 diabetes, and different types of cancers, as well as shortening of life expectancy (Lee et al. 2011). By way of example, a recent scientific report by Lee et al. (2011) sug-gests that on a worldwide basis physical inactivity causes 6% of the burden of disease from coronary heart disease, 7% from type 2 diabetes, and 10% from breast and colon cancer.
Communicated by Michael Lindinger.
* Peter Krustrup [email protected]
1 Department of Sports Science and Clinical Biomechanics, SDU Sport and Health Sciences Cluster (SHSC), Faculty of Health Sciences, University of Southern Denmark, Campusvej 55, 3450 Odense, Denmark
2 Sport and Health Sciences, College of Life and Environmental Sciences, St Luke’s Campus, University of Exeter, Exeter, UK
3 Department of Nutrition, Exercise and Sports, University of Copenhagen, Copenhagen, Denmark
4 Department of Cardiology, Herlev-Gentofte University Hospital, Gentofte, Denmark
5 Laboratory of Medical Investigation, LIM-18, Endocrinology Division, School of Medicine, University of São Paulo, São Paulo, Brazil
6 Centre of Health Science, Faculty of Health Sciences, University of the Faroe Islands, Tórshavn, Faroe Islands
7 Center of Health and Human Performance, Department of Food and Nutrition, and Sport Science, University of Gothenburg, Gothenburg, Sweden
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Moreover, inactivity causes 9% of premature mortality, e.g., corresponding to 5.3 million of the 57 million deaths that occurred worldwide in 2008. In addition, if the prevalence of physical inactivity was lowered by 10 or 25%, more than 533,000 or more than 1.3 million premature deaths, respectively, could be averted yearly (Lee et al. 2011). Thus, research initiatives elucidating optimal exercise training modes for the general population are highly warranted.
The fitness and health effects of recreational football have been studied extensively over the last 10 years with at least 120 scientific articles published in more than 30 interna-tional peer-reviewed journals. About a third of these articles have dealt with the cardiovascular, metabolic and musculo-skeletal effects of recreational football for untrained women. In addition, two narrative reviews have covered the physi-ological response and health effects of recreational football for untrained men (Krustrup et al. 2010a, b; Bangsbo et al. 2015). Finally, three meta-analyses have been published (Oja et al. 2015; Milanović et al. 2015, 2017), which primarily focus on statistical evidence of recreational football train-ing for selected health parameters in both sexes. However, a narrative review on fitness and health effects of recreational football in untrained women is currently not available.
Women experience a decline in fitness and health status in the years of menopause (Appelman et al. 2015), including a higher prevalence of physical inactivity, cardiovascular diseases, type 2 diabetes, and impaired muscle and skel-etal health (Rizzoli et al. 2014; Shufelt et al. 2015). Thus, middle-aged women appear to be at risk in relation to several lifestyle diseases, which calls for broad-spectrum focused health research in sedentary women and female patient populations. Since exercise exerts a preventive effect on the development of lifestyle-related deficiencies (Chedraui and Pérez-López 2013), exercise interventions targeting a broad health response are highly relevant for women of all ages. Given that much of the world’s population is inactive, the association with non-communicable diseases presents a major public health issue. Thus, it is a worldwide challenge to provide initiatives that will get inactive people to become active and increase life expectancy.
The current timing for a review of the physiological demands and training adaptations of recreational football for women seems appropriate, as several recent papers have covered the short-term (< 4 months) and medium-term (4–16 months) effects of recreational football for untrained healthy women aged 20–65 (av Fløtum et al. 2016; Barene et al. 2014a, b, 2016; Bowtell et al. 2016). Moreover, three recent investigations described the use of recreational foot-ball for women with hypertension and type 2 diabetes (Mohr et al. 2015; De Sousa et al. 2016; Krustrup et al. 2017). Last but not least, the last 5 years of investigations have included interesting studies of movement pattern (GPS, video foot-age, etc.), muscle metabolite response, acute bone markers,
plasma creatine kinase (CK) response, heart rate responses, etc., to short- and medium-duration football training that can be used to describe the link between the type of training, the cardiovascular, metabolic and musculoskeletal fitness training effects and the modifications in the risk of lifestyle diseases (see Fig. 1 below). Interestingly, there are many similarities but also several differences when comparing the women’s game with the men’s game. For example, the time in the highest heart rate zone above 90% HRmax and muscle lactate values are lower for untrained women during recrea-tional football training than for untrained men (Randers et al. 2010; Mohr et al. 2014a, b) and the number of jumps and headers are also lower (Pedersen et al. 2009). On the other hand, the rating of perceived exertion during recreational football training is similar to or even higher for untrained women compared to untrained men (Elbe et al. 2010, 2016; Nielsen et al. 2014). On that basis, it is of interest to compare the physical demands and physiological adaptations to rec-reational football training for women and men, with specific emphasis on skeletal, metabolic and cardiac effects.
The objectives of the present review are, therefore, to describe the fitness and health effects of recreational foot-ball in women as well as to describe the type and inten-sity of small-sided football training for women and the link between physical loading and training-induced adaptations. Comprehensive electronic database searches for reports of football studies for adult women were performed in PubMed, MEDLINE, Web of Science and Google Scholar using all available records up to 31 December 2016. No publication status restrictions were imposed.
Cardiovascular demands and training effects for untrained women
Effects on the cardiovascular system and circulating lipids
While underrepresentation of women in clinical studies must be recognized, it is well established that gender-dependent differences exist in cardiovascular disease epidemiology, pathophysiology, manifestations, treatments, and outcomes (Uhl et al. 2007; EUGenMed Cardiovascular Clinical Study Group et al. 2016). Women are generally protected from cardiovascular disease up to the menopause, presumably because of the effects of female sex hormones, mainly oes-trogen. Postmenopause adversely affects the cardiometabolic risk profile and life-time risk of cardiovascular mortality is, in fact, higher in women than in men. Even in the healthy state, however, there are sex-dependent differences in cardio-vascular function, e.g., women have higher left ventricular (LV) ejection fraction and better arterial function than men (Chung et al. 2006; Schnabel et al. 2013). Echocardiography
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has long been favored for clinical studies of myocardial structure and function in health and disease, and while origi-nally focused on global systolic LV function, newer echocar-diographic techniques including tissue Doppler, strain, strain rate, and speckle tracking analyses, and current interest in left ventricular diastolic function and right ventricular func-tion, respectively, have revealed the existence of more subtle alterations of myocardial function that carry independent prognostic weight in both women and men (Mogelvang et al. 2009; Halley et al. 2011; Mohammed et al. 2014).
Cardiac structure and function
In premenopausal healthy women, 16 weeks of recreational football (1 h two to three times per week) induced consider-able changes in cardiac structure and function, e.g., increases in LV end diastolic volume, LV posterior wall thickness and right ventricle diameter, improved LV systolic and diastolic performances, and improved right ventricular function, respectively, compared to a matched sedentary control group and these changes were comparable to those observed in women randomized to running sessions with the same aver-age intensity (Table 1) (Andersen et al. 2010). Similar car-diac adaptations to recreational football were observed in a
long-term study of premenopausal women, where 16 months of recreational football significantly increased myocardial chamber dimensions and LV and RV performances, respec-tively (Krustrup al. 2010b). Not surprisingly, greater car-diac dimensions and LV diastolic function were also dem-onstrated in a cross-sectional study of elite female football players compared to untrained women (Randers et al. 2013).
Given the global type 2 diabetes epidemic, cardiac effects of recreational football in patients with diabetes warrant spe-cial emphasis. However, while physical exercise improves diabetes control and a range of cardiovascular risk factors in both women and men with type 2 diabetes, reports of cardio-vascular effects of exercise interventions aimed more selec-tively at women with diabetes are scarce. Subjects with dia-betes frequently display LV dysfunction even in the absence of hypertension or coronary artery diseases and such ‘dia-betic cardiomyopathy’ is associated with increased myocar-dial lipid content (Rijzewijk et al. 2008; Aneja et al. 2008). LV diastolic function has long been considered as the earli-est marker of diabetic cardiomyopathy, but more recent tis-sue Doppler echocardiographic imaging and strain analyses have indicated that LV systolic function, e.g., longitudinal systolic strain, can be diminished in patients with diabetes even in the absence of diastolic dysfunction (Ernande et al.
Aerobic low-intensity
Metabolicfitness
Training categories Areas of fitness Measures Lifestyle diseases
Footballtraining Cardio-
vascularfitness
Musculo-skeletal fitness
Aerobic mode-rate intensity
Aerobic high intensity
Speed endurance
Bone impact
Musclemass
Glucosetolerance
Fat per-centage
Blood pressure
VO2max
Posturalbalance
Bone mass
Type 2 diabetes
Cardiovasculardiseases
Osteoporosis
Risk of fallsand fracturesSpeed, strength
Training types
Endurancetraining
HIIT training
Strengthtraining
Fig. 1 A holistic model of the mechanistic link between football as an intense and versatile training form and its broad-spectrum fitness and health effects. The model describes football training as a combina-tion HIIT training, endurance training and strength training, together eliciting five training categories and providing an optimal stimuli to all three areas of fitness, metabolic fitness, cardiovascular fitness
and musculoskeletal fitness, and also describes how improvements in these fitness components affects the risk of lifestyle diseases such as type 2 diabetes, cardiovascular diseases and osteopenia/osteoporosis (modified from Krustrup et al. 2010a, SJMSS, and Krustrup 2017, Science and football)
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Tabl
e 1
Cha
nges
in c
ardi
ovas
cula
r var
iabl
es in
unt
rain
ed w
omen
as
a re
sult
of a
per
iod
of re
crea
tiona
l foo
tbal
l tra
inin
g (F
) com
pare
d to
runn
ing
(R),
zum
ba (Z
), vi
brat
ion
train
ing
(V),
swim
-m
ing
(MS,
HS)
or i
nact
ive
cont
rols
(C)
Stud
yA
ctiv
ity,
targ
et g
roup
, ge
nder
Age
(yea
rs)
Trai
ning
inte
rven
tion:
dur
a-tio
n (w
eeks
), in
tens
ity (%
), fr
eque
ncy
(per
wee
k), s
essi
on
dura
tion
(min
)
VO2m
ax (%
)H
R su
b-m
ax
(bpm
or
%H
Rm
ax)
HR
rest
(bpm
)B
Psys
rest
(mm
Hg)
BPd
ia re
st (m
mH
g)M
AP
rest
(mm
Hg)
RV sy
stolic
fu
nctio
n,
TAPS
E (%
)
LV d
iasto
lic
func
tion,
E/A
ra
tio (%
)
Arte
rial s
tiff-
ness
(AI)
(%)
Kru
strup
et
al.
(201
0a)
And
erse
n et
al.
(201
0)
F, U
T, W
19–4
716
; 83%
HR
max
; 1.8
0; 6
015
%↑*
$13↓*
5↓*$
7↓*
4↓*
5↓*
16%↑*
$57
%↑*
$5%↓*
$#
R, U
T, W
19–4
716
; 82%
HR
max
; 1.8
5; 6
017↓*
5↓*$
6↓*
3↓N
S3↓
*10
%↑*
$44
%↑*
$N
SC
, UT,
W19
–47
No
inte
rven
tion
10%↑*
$
3%↑N
S6↓
NS
0↔N
S2↓
NS
2↓N
S2↓
NS
5%↓*
6%↑N
SN
S
Bar
ene
et a
l. (2
013)
F, U
T, W
25–6
512
; 78.
3%H
Rm
ax; 2
.4; 6
05%↑$
7↓$
–2↑
NS
1↑N
S–
––
–Z,
UT,
W25
–65
12; 7
5.3%
HR
max
; 2.3
; 60
5%↑$
3↓N
S–
0.1↑
NS
0.4↓
NS
––
––
C, U
T, W
25–6
5N
o in
terv
entio
nN
SN
S–
NS
NS
––
––
Con
nolly
et
al.
(201
4)
F, U
T, W
20–4
516
; 155
bpm
; 2; 1
5–
12↓*
4↓N
S2↑
NS
1↑N
S–
––
–V,
UT,
W20
–45
16; 9
0 bp
m; 2
; 15
––
2↓N
S3↓
NS
1↓N
S–
––
–C
, UT,
W20
–45
No
inte
rven
tion
––
3↓N
S1↑
NS
0↔N
S–
––
–D
e So
usa
et a
l. (2
014)
F, U
T, W
t +
Mt
48–6
812
; 83%
HR
max
; 3; 4
0; F
+ D
10%↑*
$–
––
––
––
–
C, U
T, W
t +
Mt
48–6
8D
iet g
roup
3%↓N
S–
––
––
––
–
av F
løtu
m
et a
l. (2
016)
F, U
T,
W +
M20
–72
18; 7
6.6%
HR
max
; 1.6
; 60
–2–
6↓*
6↓*
3.5↓
*2.
3↓*
2.7↓
*–
––
Moh
r et a
l. (2
014a
)M
ohr e
t al.
(201
4b)
Moh
r et a
l. (2
015)
F, U
T, W
mh
35–5
015
; 80.
5%H
Rm
ax; 3
.0; 6
0–
7%↓*
$7↓
*12↓*
$6↓
*$8↓
*$–
––
MS,
UT,
W
mh
35–5
015
; 72.
5%H
Rm
ax; 2
.9; 6
0–
4%↓*
$5↓
*4↓
*$N
S1↓
NS
––
–
HS,
UT,
Wm
h35
–50
15; 8
5.5%
HR
max
; 2.9
; 15–
25–
5%↓*
$5↓
*6↓
*$N
S3↓
NS
––
–C
, UT,
Wm
h35
–50
No
inte
rven
tion
–1%↑N
S3↓
NS
1↑N
S1↑
NS
0↔N
S–
––
Kru
strup
et
al.
(201
7)
F, U
T, W
mh
35–5
052
; 81%
HR
max
; 2.5
; 60
–7%↓$
6↓N
S7↓
$4↓
$5↓
$–
––
C, U
T, W
mh
35–5
0N
o in
terv
entio
n–
1%↑N
S3↓
NS
3↑N
S4↑
NS
4↑N
S–
––
Cha
nges
bet
wee
n pr
e- a
nd p
ost-t
rain
ing
inte
rven
tion
(unl
ess o
ther
wis
e st
ated
)AI
aug
men
tatio
n in
dex,
BPd
ia d
iasto
lic b
lood
pre
ssur
e, b
pm b
eats
per
min
ute,
BPs
ys s
ysto
lic b
lood
pre
ssur
e, C
con
trols
, E/A
ratio
, rat
io o
f ear
ly (E
) to
late
(A) v
entri
cula
r filli
ng v
eloc
ities
, F
foot
ball,
F +
D fo
otba
ll +
diet
gro
up, H
Rmax
max
imal
hea
rt ra
te, H
S hi
gh-in
tens
ity sw
imm
ing,
LV
left
vent
ricul
ar, M
men
, MAP
mea
n ar
teria
l pre
ssur
e, m
h m
ild h
yper
tens
ive
subj
ects
, MS
mod
-er
ate-
inte
nsity
sw
imm
ing,
NS
not s
igni
fican
t, R
runn
ing,
RV
right
ven
tricu
lar,
t typ
e 2
diab
etic
s, TA
PSE
tricu
spid
ann
ular
pla
ne s
ysto
lic e
xcur
sion
, UT
untra
ined
, V v
ibra
tion
train
ing,
VO
2max
m
axim
al o
xyge
n co
nsum
ptio
n, W
wom
en, Z
zum
ba*S
igni
fican
t diff
eren
ce fr
om 0
wee
ks$ Si
gnifi
cant
gro
up d
iffer
ence
com
pare
d to
con
trol
# Sign
ifica
nt g
roup
diff
eren
ce c
ompa
red
to o
ther
trai
ning
inte
rven
tion
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2011). As yet limited studies of aerobic exercise interven-tions in men and women with type 2 diabetes and obesity have had conflicting results (Brassard et al. 2007; Loimaala et al. 2007; Hordern et al. 2009; Millen et al. 2014). How-ever, one study showed that 12 weeks of home-based high-intensity interval training (HIIT) improved LV diastolic and systolic function more in patients of both sexes with type 2 diabetes than moderate-intensity exercise (Hollekim-Strand et al. 2014). The activity profile of recreational football is similar to that of HIIT (see Fig. 1), and it is notable that, in middle-aged men with type 2 diabetes, recreational football has been found to elicit significant cardiac adaptations, e.g., increased longitudinal systolic displacement and increased LV diastolic dysfunction (Schmidt et al. 2013).
Maximal oxygen uptake, resting heart rate, blood pressure, arterial function, and circulating lipids
Several studies have examined the effects of women’s foot-ball on maximal oxygen uptake. These studies show that recreational football training 2 × 1 h per week for 3–4 months causes marked improvements in maximal oxygen uptake, both for pre-menopausal women (5–15%, Krustrup et al. 2010a; Barene et al. 2013) and post-menopausal women (7–12%, Barene 2014a, b; De Sousa et al. 2014) (Table 1). Premenopausal women randomized to 16 weeks of recrea-tional football showed significant decreases in resting heart rate and arterial blood pressure that were comparable to a running group (Table 1). However, decreased arterial stiff-ness measured by the augmentation index and increased skeletal muscle capillarisation, respectively, were exclu-sively observed in the football group (Krustrup et al. 2010a). In that study, plasma cholesterol and triglyceride levels showed discrete changes, but a significant decrease in the low-density lipoprotein/high-density lipoprotein cholesterol ratio was only found in the football group. In a study of premenopausal women with mild hypertension, 15 weeks of recreational football significantly reduced total choles-terol and triglyceride levels compared to sedentary controls (Mohr et al. 2014a). Moreover, in pre- and postmenopausal women with T2DM, randomisation to 12 weeks of com-bined recreational football training and calorie-restricted diet decreased total cholesterol, triglyceride, LDL choles-terol and very low-density lipoprotein levels compared to controls (de Sousa et al. 2014).
Areas of uncertainty and new avenues of research
Cardiovascular adaptations to recreational football in women as described above appear to mirror findings in middle-aged and older untrained men as well as men with cardiometabolic
disease, including hypertension and type 2 diabetes, respec-tively (Krustrup et al. 2009a, 2013; Andersen et al. 2010, 2014; Schmidt et al. 2013, 2014; Bangsbo et al. 2015). These findings also mimic those reported in the vast number of studies (mainly performed in men) of cardiovascular adapta-tions to other physical training modalities, and many of the underlying molecular mechanisms are, of course, likely to be sex independent (Wilson et al. 2016). Along this line, long-term maintenance of football-induced cardiovascular effects so far reported in women (in addition to the well-documented increase in exercise capacity), including improvements in myocardial function, reductions in resting heart rate, blood pressure, and arterial stiffness, and amelioration of plasma lipid profile, respectively, are likely to translate into reduced risk of cardiovascular disease. However, many mechanisms for cardiovascular disease are unique to women, especially those pertaining to effects of failing oestrogen levels during and after menopause and the importance of these mecha-nisms for the effects of exercise has not been defined in detail (Ren and Kelley 2009; Abramson and Melvin 2014; La Favor et al. 2014; EUGenMed Cardiovascular Clinical Study Group et al. 2016). Furthermore, differences between women and men in basic determinants of exercise-induced cardiovas-cular adaptations, e.g., capacity for long-term maintenance of the intensity and volume of different training modalities, including recreational football, are unclear. Interestingly, limited acute response data for recreational football have suggested that although untrained premenopausal women display a reduced activity profile, compared to that of men e.g., shorter sprints and more time standing still, their heart rate distribution expressed as percentages of recreational football playing time in different heart rate zones is remark-ably similar to the distribution in untrained men (Randers et al. 2010). It is also notable that the physical training load in football training resembles HIIT which may be more effec-tive at eliciting favorable cardiovascular adaptations than moderate-intensity continuous training (Nybo et al. 2010; Mohr et al. 2014b; Weston et al. 2014; Ramos et al. 2015; see Fig. 1). Adequately powered studies in women (pre and post menopause) and men are also needed to examine the effects of recreational football on other indices of cardiovas-cular health including, for example, coronary flow reserve, cardiac variables at stress echocardiography, and surrogates of atherosclerotic disease (e.g., carotid intima-media thick-ness and coronary artery calcification). In addition, future studies in this area should focus on the efficacy and safety of recreational football in patients with heart diseases (e.g., ischaemic heart disease and heart failure), and, ultimately, on determining the effects of recreational football on cardiovas-cular morbidity and mortality.
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Skeletal muscle impacts and training effects in untrained women
Aging and human skeletal muscle properties: inflammation and oxidative stress
Aging is associated with a decline in skeletal muscle mass, muscle strength, and functional capacity (Buch et al. 2016). The muscle strength of obese individuals is inferior to that of non-obese individuals and could lead to major functional limitations for daily living, higher frequency of hospitalization and reduced quality of life (Mendham et al. 2014; Malafarina et al. 2013). Furthermore, adipos-ity plays a critical role in the functional decline of elderly whereas higher levels of inflammatory cytokines [tumor necrosis factor (TNF)-α and interleukin (IL)-6] are asso-ciated with lower muscle mass, strength and sarcopenia (Erskine et al. 2017; Mendham et al. 2014). For example, Fisher et al. (2014) have shown a higher concentration of circulating TNF-α in postmenopausal women older than 60 years who do not increase fat-free mass following resistance training or aerobic training programs.
Fat infiltration into the skeletal muscle reduces the con-tractile component of the total muscle volume, thereby lowering the intrinsic strength of the whole muscle, which may be suggested as a major cause of chronically elevated levels of pro-inflammatory circulating cytokines in older vs younger adults (Rivas et al. 2016). The elevation of these cytokines in the blood results in chronic low-grade systemic inflammation (Farinha et al. 2015). Intramuscular lipids act as a chemoattractant for macrophages, which produce pro-inflammatory cytokines, such as TNF-α and adipo-cyte-derived IL-6. In muscle, these cytokines are directly involved in the breakdown of muscle protein, reducing mus-cle force, as well as several metabolic health impairments, such as insulin resistance. Furthermore, increases in pro-inflammatory cytokines in the hypothalamus may provoke neuroinflammation (Waise et al. 2015; Okuda et al. 2014).
In the study by Erskine et al. (2017) serum IL-6 concen-trations were higher in older than young untrained women performing isometric and isokinetic voluntary contractions. Furthermore, IL-6 correlated with adiposity in young and old subjects. Moreover, the study found an inverse rela-tionship between basal IL-6 levels and voluntary muscle activation. This inverse relationship strongly suggests that adipocyte-derived IL-6 has a negative effect on ability to voluntarily activate skeletal muscle which may be influenced by central inflammation. Thus, the chronically elevated lev-els of IL-6 and lower voluntary muscle activation levels in older adults suggest that IL-6-induced neuroinflammation plays a role in reducing voluntary muscle strength.
In this sense, a synergistic relationship between low-grade inflammation and oxidative stress has also been postulated as
cytokines and immune cells are able to trigger the produc-tion of reactive oxygen (ROS) as a defense activity. Accord-ing to the study by Farinha et al. (2015), 12 weeks of aerobic training of moderate-intensity in postmenopausal women with metabolic syndrome reduced IL-1β, IL-6, TNF-α, and interferon (INF)-γ and increased IL-10 serum levels, induc-ing positive effects on oxidative stress and inflammatory modulation in this population. Working skeletal muscle is a potential source of cytokines as well as the adipose tissue. However, the IL-6 produced by myocytes during aerobic exercise presents anti-inflammatory effects as opposed to IL-6 secreted by adipose tissue, promoting the release of IL-10 and IL-1 receptor antagonist, with a concomitant inhi-bition of TNF-α production during and after exercise ses-sions, decreasing proinflammatory status (Nunes et al. 2016; Imayama et al. 2012). The reduction in pro-inflammatory interleukins in postmenopausal women undergoing aerobic training was also reported by Reed et al. (2010) and Steck-ling et al. (2016). However, there are still few studies evalu-ating the impact of aerobic training on circulating biomark-ers of inflammation in mature women. Likewise, there is a lack of studies involving menopausal women in team sports. A recent study also demonstrated an upregulation of skeletal muscle antioxidative capacity after 15 weeks of recreational football training (Mohr et al., unpublished results). Thus, small-sided football training may also reduce inflammatory markers in postmenopausal women, preventing sarcopenia, being effective as treatment against chronic inflammation in this age group.
Senescence has been linked both to loss of muscle mass and muscle strength, varying according to gender and muscle activity status. It is known that women, in general, have inferior muscle strength than men. Indeed the type IIA fibers have been shown to have a larger cross-sectional area in men, whereas the type I fibers tended to be the largest in women (Staron et al. 2000). This type of comparison is, however, difficult due to the effect of training status. However, whereas the relative proportion of the number of type I vs II fibers appears to remain unaltered with increasing age in both women and men (Kosek et al. 2006), postmortem muscle biopsy samples obtained in females of mixed ages (24–82 years) have indicated that the diameter of type II fibers may decline with increase in age (Bougea et al. 2016). Further sup-porting a relationship between type II fiber size and age, reduced type II fiber cross-sectional area was observed in old (60–70 yrs) vs young (~ 30 years) community-living healthy women (Kosek et al. 2006; Callahan et al. 2014). Perhaps more importantly, prolonged heavy-resistance strength training intervention seems effective in increas-ing type II muscle fiber size in aging women (Häkkinen et al. 2001; Kosek et al. 2006; Taaffe et al. 1996), thus helping to both prevent and treat the age-related loss in
European Journal of Applied Physiology
1 3
skeletal muscle mass (Aagaard et al. 2010). As discussed below small-sided football training may also provide a significant myogenic stimulus to the trained muscles, causing gains in skeletal muscle mass in middle-aged and elderly women.
In a recent study by Nordsborg et al. (2015), it was tested whether the oxidative adaptive potential of the upper body muscle is higher than that of the leg mus-culature in sedentary premenopausal women comparing high- and moderate-intensity training including recrea-tional football. It was reported that arm muscle has a lower oxidative capacity than leg muscle, despite similar fiber type composition and capillarization. However, a higher protein expression and glycogen content were observed in arm vs leg muscle after high vs low-intensity exercise training compared to inactive controls (Nordsborg et al. 2015). Moreover, football training, which is a combina-tion of high- and low-intensity training, improved skeletal muscle oxidative capacity in premenopausal women (Nor-dsborg et al. 2015; see Table 2).
Skeletal muscle function and size
Strength and resistance training are both known to result in marked improvements in neuromuscular function, mani-fested by gains in contractile rate of rapid force develop-ment (RFD), eccentric muscle strength, and maximal muscle power, respectively, as a result of adaptive changes in spinal circuitry function and descending supraspinal motor drive (for review, see Aagaard 2003, Aagaard et al. 2010). At the same time, strength/resistance training can evoke substantial gains in muscle mass, indicated by elevated myofiber areas and increased anatomical muscle cross-sectional area (CSA) and volume accompanied by changes in muscle architec-ture (increased muscle fascicle angles) (cf. Aagaard et al. 2001). Both classes (neural and muscular) of adaptive physi-ological changes are considered to be important for athletic performance (Aagaard 2003) as well as for ensuring sus-tained functional capacity in old adults (Aagaard et al. 2010) including frail elderly patients (Suetta et al. 2007). However, only a few studies have investigated the effect of recreational football exercise on neuromuscular function (including RFD
Table 2 Changes in muscle enzymatic activity, capillarisation, glycogen content and oxidative capacity in untrained women as a result of a period of recreational football training (F) compared to running (R) or inactive controls (C)
Changes between pre and post training intervention (unless otherwise stated)C controls, CS citrate synthase, F football, HAD 3-hydroxyacyl-CoA dehydrogenase, HRmax maximal heart rate, HS high-intensity swimming, mh mild hypertensive subjects, MS moderate-intensity swimming, NS not significant, R running, UT untrained, W women*Significant difference from 0 weeks$ Significant group difference compared to control# Significant group difference compared to other training intervention¥ Significant group difference compared to football
Study Activ-ity, target group, gender
Age (years) Training inter-vention: dura-tion (weeks), intensity (%), frequency (per week), session duration (min)
Capillarisa-tion, cap per fiber (%)
CS activity (%)
CS protein expression (%)
HAD activ-ity (%)
Glycogen content (mmol/kg dw or %)
Mito-chondrial complex expression (%)
Krustrup et al. (2010a)
Bangsbo et al. (2010)
F, UT, W 19–47 16; 83%HRmax; 1.80; 60
18%↑*# 11%↑* – 9%↑* 39↑NS –
R, UT, W 19–47 16; 82%HRmax; 1.85; 60
12%↑NS 13%↑* – 5%↑NS 55↑NS –
C, UT, W 19–47 No intervention – – – – – –
Nordsborg et al. (2015)
F, UT, Wmh 35–50 15; 80.5%HRmax; 3.0; 60
– 27–37%↑* 31–49%↑*$ 3–25↑*12–20↑*
2–20%↑NS 27–230%↑*
MS, UT, Wmh
35–50 15; 72.5%HRmax; 2.9; 60
– 29–35%↑* 33–48%↑*$ 16–24%↑NS
30–218%↑*
HS, UT, Wmh
35–50 15; 85.5%HRmax; 2.9; 15–25
– 52–95%↑*#¥ 44–100%↑*$#¥
18–35↑*¥ 11–63%↑*#¥
28–213%↑*
C, UT, Wmh 35–50 No intervention NS 0–22%↑NS NS 11–20%↑NS
2–132%↑NS
European Journal of Applied Physiology
1 3
and power) and skeletal muscle health (muscle mass/size, myocellular morphology and metabolism, contractile func-tion) in women (see Tables 2, 3, 4).
As an indication that acute football training may impose substantial adaptive stress on the skeletal muscle involved in the exercise, plasma CK was 55–119% elevated at 48 h following an acute single bout of short- (15 min) or long-duration (60 min) small-sided football exercise in premeno-pausal women (38 ± 5 years) (Bowtell et al. 2016). Similarly, markers of bone and/or tendon collagen turnover (procol-lagen type 1 amino-terminal propeptide, osteocalcin) were elevated in response to football exercise of both short and long duration, as discussed in greater detail below (Bow-tell et al. 2016). In combination, it was suggested that acute changes contribute to favorable effects of prolonged football training on musculoskeletal health (Bowtell et al. 2016).
Potentially stimulating adaptations in RFD and accelera-tion capacity, young women (37 ± 2 years) demonstrated a high number of activity changes during 1-hour small-sided game play (4v4 and 2v2: 1158–1221 activity changes), which was higher than that observed with more players on the pitch (7v7: 951 activity changes) (Randers et al. 2010). Although the number of high-intensity runs performed did not differ with a higher (7v7: 100 high-intensity runs) versus lower number of players (4v4 and 2v2: 91–104 high-inten-sity runs), a longer mean duration of high-intensity runs was noted in 4v4 (1.7 s) than in 7v7 (1.4 s) or 2v2 (1.4 s) (Rand-ers et al. 2010). These observations suggest that small-sided football training sessions with 4v4 game-play may ensure an optimal stimulus for acceleration capacity and RFD adapta-tion in previously untrained women.
In support of this notion, medium-term (16 months) football training in young previously untrained premeno-pausal women (40 ± 3 years) resulted in substantial gains in mechanical muscle function, reflected by elevated levels of fast (27 and 16%) and slow (16% and 17%) eccentric quadri-ceps muscle strength accompanied by marked increases in rapid force capacity (contractile impulse at 0–30 ms relative to contraction onset 66 and 65%) compared with 4 and 0 months (Krustrup et al. 2010a, b, c). Importantly, compara-ble changes were noted for the hamstring muscles (Krustrup et al. 2010a, b, c), which may reduce the risk of non-contact ACL injury in this population (Zebis et al. 2011). Nota-bly, postural balance ability was also improved following 16 months of football training (Krustrup et al. 2010a, b, c; see Table 4). Comparable changes were observed in age-matched women who were randomized to endurance running for 16 months (Krustrup et al. 2010a, b, c).
A further demonstration that football training can elicit positive changes in neuromuscular function was that trunk stabilization capacity, measured as stopping time in response to random anterior trunk perturbations, was improved (decreased by 15%) accompanied by a reduced
distance moved (24% decreased) following 16 weeks of football training in young untrained women (19–45 years) (Pedersen et al. 2009). In contrast, no changes were detected in females exposed to 16 weeks of endurance run-ning exercise or in non-exercising controls (Pedersen et al. 2009). Probably representing a strong stimulatory effect on the changes observed with football training, 1 h of soccer training was characterized by a high number of sudden movements (192 ± 63) including sudden loading impacts on the upper body (e.g., turns, stops, throw-ins, headers, shoulder tackles) (Pedersen et al. 2009). The authors con-cluded that football training performed in young women includes a high number of sudden loadings of the upper body, which appears to improve the reflex response to sud-den trunk loading impacts. Furthermore, it was suggested, based on the enhanced trunk reflex response that football training may reduce the risk of lower back injury (Pedersen et al. 2009).
Notably, football training may also exert positive effects on total skeletal muscle mass in women. Thus, lean whole body mass measured by DXA scanning increased nearly 3 kg (+ 7%) concurrently with a drop in total body mass following 1 year of small-sided football training (128 × 1-h sessions) in physically inactive and mildly hypertensive middle-aged women (45 ± 6 years; Krustrup et al. 2017). In addition, mean arterial pressure decreased more in study participants randomized to football training compared to non-exercising controls (− 5 vs + 4 mmHg) along with sim-ilar trends for total body fat mass (− 2.5 vs + 0.6 kg) and total body mass (− 2.5 vs + 0.6 kg) (Krustrup et al. 2017). As a proxy measure of maximal muscle strength and RFD, 20-m sprint performance was also found to improve (+ 6%) following 1 year of football training (Krustrup et al. 2017). In terms of positive changes in lean body mass, similar data were reported by Andersen and co-workers (2010a) who found that twice-weekly 1-hour sessions of small-sided recreational soccer (or outdoor continuous running) for 16 weeks produced significant gains in lean body mass accom-panied by reductions in fat mass (Andersen et al. 2010b). In contrast, no changes in lean body mass were observed in elderly (48–68 years) female patients with type 2 diabetes following 12 weeks (3 × 40 min/week) of football training based on small-sided game activities (3v3 up to 7v7) (Sousa et al. 2014), indicating that improvements in lean body mass are not a uniform observation following recreational football training in women. It is probable that differences in train-ing protocols and/or intervention duration, as well as differ-ences in health status, are responsible for these diverging observations.
Overall, recreational football training appears to be effec-tive of evoking positive changes in neuromuscular func-tion and skeletal muscle mass and function in adult women. These changes include improvements in mechanical muscle
European Journal of Applied Physiology
1 3
Tabl
e 3
Cha
nges
in b
ody
com
posi
tion
in u
ntra
ined
wom
en a
s a
resu
lt of
a p
erio
d of
recr
eatio
nal f
ootb
all t
rain
ing
(F) c
ompa
red
to r
unni
ng (R
), zu
mba
(Z),
vibr
atio
n tra
inin
g (V
), sw
imm
ing
(MS,
HS)
or i
nact
ive
cont
rols
(C)
Stud
yA
ctiv
ity,
targ
et g
roup
, ge
nder
Age
(yea
rs)
Trai
ning
inte
r-ve
ntio
n: d
ura-
tion
(wee
ks),
inte
nsity
(%),
freq
uenc
y (p
er
wee
k), s
essi
on
dura
tion
(min
)
Tota
l fat
m
ass (
kg)
Tota
l fat
pe
rcen
tage
(%
)
Lean
bod
y m
ass,
who
le
body
(kg)
Lean
bod
y m
ass,
legs
(k
g or
%)
Bon
e m
iner
al d
ensi
ty, s
pe-
cific
site
s (%
); tib
ia, f
emo-
ral s
haft
and
troch
ante
r
Bon
e m
in-
eral
den
sity
, w
hole
bod
y (g
/cm
2 or %
)
Bon
e m
in-
eral
den
sity
, le
gs (g
/cm
2 or
%)
Bon
e m
arke
r, os
teoc
alci
n (%
)
Kru
strup
et
al.
(201
0a, b
)
F, U
T, W
19–4
716
; 83%
HR
max
; 1.
80; 6
01.
4↓*$
2.1↓
*1.
4↑*$
1.5↑
*–
1.3%↑*
#2.
6%↑N
S–
R, U
T, W
19–4
716
; 82%
HR
max
; 1.
85; 6
01.
1↓*
1.7↓
*1.
3↑*$
1.2↑
*–
0.3%↑N
S2.
4%↑*
–
C, U
T, W
19–4
7N
o in
terv
entio
n0.
5↓N
S0.
8↓N
S0.
1↑N
S0.
3↑N
S–
1.7%↑N
S1.
4%↑N
S–
Bar
ene
et a
l. (2
013)
F, U
T, W
25–6
512
; 78.3
%H
Rm
ax;
2.4;
60
1.0↓
$1.
1↓$
––
–0.
0↔N
S0.
0↔N
S21
%↑$
Z, U
T, W
25–6
512
; 75.3
%H
Rm
ax;
2.3;
60
0.6↓
$0.
7↓N
S–
––
0.0↔
NS
0.0↔
NS
10%↑$
C, U
T, W
25–6
5N
o in
terv
entio
nN
SN
S–
––
NS
NS
NS
De
Sous
a et
al.
(201
4)
F, U
T,
Wt +
Mt
48–6
812
; 83%
HR
max
; 3;
40;
F +
D3.
4↓*
2.4↓
NS
0.2↓
NS
––
0.1↑
*–
–
C, U
T,
Wt +
Mt
48–6
8D
iet g
roup
3.7↓
*2.
4↓N
S1.
0↓N
S–
–0.
0↑*
––
Hel
ge e
t al.
(201
0)F,
UT,
W36
14; 8
3%H
Rm
ax;
1.8;
60
––
–1.
4↑*
Tib:
LL
2.6%↑*
#$
RL:
2.1
%↑*
$0.
2%↓N
S1.
5%↑N
S
R, U
T, W
3614
; 82%
HR
max
; 1.
9; 6
0–
––
1.0↑
*LL
: 0.7
%↑*
RL:
1.1
%↑*
0.3%↓N
S1.
5%↓N
S
C, U
T, W
36N
o in
terv
entio
n–
––
0.6↑
NS
LL: 0
.0%
↔N
SR
L: 0
.4%↑N
S0.
1%↓N
S0.
2%↓N
S–
Con
nolly
et
al.
(201
4)B
owte
ll et
al.
(201
6)
F, U
T, W
20–4
516
; 155
bpm
; 2;
15
1.4↓
NS
1.7↓
*#0.
8↑N
S0.
4↑N
S–
––
10%↑*
(48
h po
st ex
er-
cise
)V,
UT,
W20
–45
16; 9
0 bp
m;
2; 1
50.
4↑N
S0.
4↑N
S0.
1↓N
S0.
0↔N
S–
––
11%↑*
(48
h po
st ex
er-
cise
)C
, UT,
W20
–45
No
inte
rven
tion
0.2↓
NS
0.2↓
NS
0.2↑
NS
0.1↑
NS
––
––
Jack
man
et
al.
(201
3)
F, U
T, W
2716
; 83%
HR
max
; 1.
8; 6
01.
5↓*
–1.
4↑*
––
0.0↔
NS
0.0↔
NS
37%↑*
European Journal of Applied Physiology
1 3
Cha
nges
bet
wee
n pr
e- a
nd p
ost-t
rain
ing
inte
rven
tion
(unl
ess o
ther
wis
e st
ated
)Bp
m b
eats
per
min
ute,
C c
ontro
ls, F
foot
ball,
F +
D fo
otba
ll +
diet
gro
up, H
Rmax
max
imal
hea
rt ra
te, H
S hi
gh-in
tens
ity sw
imm
ing,
LL
left
leg,
M m
en, m
h m
ild h
yper
tens
ive
subj
ects
, MS
mod
-er
ate-
inte
nsity
swim
min
g, N
S no
t sig
nific
ant,
R ru
nnin
g, R
L rig
ht le
g, S
shaf
t, t t
ype
2 di
abet
ics,
T Tr
ocha
nter
, Tib
tibi
a, U
T un
train
ed, V
vib
ratio
n tra
inin
g, W
wom
en, Z
zum
ba*S
igni
fican
t diff
eren
ce fr
om 0
wee
ks$ Si
gnifi
cant
gro
up d
iffer
ence
com
pare
d to
con
trol
# Sign
ifica
nt g
roup
diff
eren
ce c
ompa
red
to o
ther
trai
ning
inte
rven
tion
Tabl
e 3
(con
tinue
d)
Stud
yA
ctiv
ity,
targ
et g
roup
, ge
nder
Age
(yea
rs)
Trai
ning
inte
r-ve
ntio
n: d
ura-
tion
(wee
ks),
inte
nsity
(%),
freq
uenc
y (p
er
wee
k), s
essi
on
dura
tion
(min
)
Tota
l fat
m
ass (
kg)
Tota
l fat
pe
rcen
tage
(%
)
Lean
bod
y m
ass,
who
le
body
(kg)
Lean
bod
y m
ass,
legs
(k
g or
%)
Bon
e m
iner
al d
ensi
ty, s
pe-
cific
site
s (%
); tib
ia, f
emo-
ral s
haft
and
troch
ante
r
Bon
e m
in-
eral
den
sity
, w
hole
bod
y (g
/cm
2 or %
)
Bon
e m
in-
eral
den
sity
, le
gs (g
/cm
2 or
%)
Bon
e m
arke
r, os
teoc
alci
n (%
)
Moh
r et a
l. (2
014a
)F,
UT,
Wm
h35
–50
15; 80
.5%
HR
max
; 3.
0; 6
0
2.3↓
*$2.
1↓$
1.2↑
*7%↑*
$S:
1.7
%↑*
#$1%↓N
S0%
↔N
S37
%↑*
#$
Moh
r et a
l. (2
014b
)M
S, U
T,
Wm
h35
–50
5; 7
2.5%
HR
max
; 2.
9; 6
02.
2↓*$
2.0↓
*$1.
3↑*$
3%↑N
ST:
2.4
%↑*
#$0%
↔N
S1%↓N
SN
S
Moh
r et a
l. (2
015)
HS,
UT,
W
mh
35–5
015
; 85.5
%H
Rm
ax;
2.9;
15–
25
1.1↓
*$1.
7↓*$
1.7↑
*$6%↑*
$T:
NS
2%↓N
S0%
↔N
SN
S
Nor
dsbo
rg
et a
l. (2
015)
C, U
T, W
mh
35–5
0N
o in
terv
entio
n0.
4↑N
S0.
5↑N
S0.
4↑N
S1%↑N
ST:
NS
2%↓N
S2%↓N
SN
S
Kru
strup
et
al.
(201
7)
F, U
T, W
mh
35–5
052
; 81%
HR
max
; 2.
5; 6
03.
2↓$
3↓*
2.6↑
*–
–0.
0↑$
––
C, U
T, W
mh
35–5
0N
o in
terv
entio
n0.
2↑N
SN
S1.
1↑N
S–
–0.
0↓N
S–
–
European Journal of Applied Physiology
1 3
function, reflected by substantial gains in rapid force capac-ity (RFD) and maximal concentric/eccentric/isometric mus-cle strength for the leg extensors and flexors, respectively.
These changes are accompanied by gains in functional performance, including improvements in postural control, sprint/acceleration capacity and rapid trunk stabilization.
Table 4 Changes in performance of untrained women as a result of a period of recreational football training (F) compared to running (R), zumba (Z), swimming (MS, HS) or inactive controls (C)
Changes are between pre- and post-training intervention (unless otherwise stated)C controls, F football, H hamstring contraction, HRmax maximal heart rate, HS high-intensity swimming, LL left leg, mh mild hypertensive sub-jects, MS moderate-intensity swimming, NS not significant, RL right leg, R running, UT untrained, Yo–Yo IE1/IE2 Yo–Yo intermittent endurance test level 1/level 2, W women, Z zumba, Q quadriceps contraction*Significant difference from 0 weeks$ Significant group difference compared to control
Study Activ-ity, target group, gender
Age (years) Training inter-vention: dura-tion (weeks), intensity (%), frequency (per week), session (min)
Time to exhaustion, max. work (s or %)
Counter-movement jump (%)
Sprint, 30 m (s)
Max. leg strength (%)
Yo-Yo IE1/IE2 (%)
Postural balance, Flamingo test (%)
Bangsbo et al. (2010)
Krustrup et al. (2010b)
F, UT, WR, UT, WC, UT, W
19–4719–4719–47
16; 83%HRmax; 1.80; 60
16; 82%HRmax; 1.85; 60
No intervention
21%↑*$
17%↑*$
4%↑*
–––
0.39↑*0.19↑NS–
Q:12%↑*H:23%↑*Q:7%↑NSH:10%↑NSNS
37%↑*26%↑*15%↓NS
47%↑*$
40%↑*$
9%↑NS
Barene et al. (2013)
F, UT, WZ, UT, WC, UT, W
25–6525–6525–65
12; 78.3%HRmax; 2.4; 60
12; 75.3%HRmax; 2.3; 60
No intervention
11.0↑$
12.7↑$
NS
–––
–––
–––
–––
–––
av Fløtum et al. (2016)
F, UT, W + M
20–72 18; 76.6%HRmax; 1.6; 60
– – 6%↑* (agil-ity)
–––
41%↑* 45%↑*
Helge et al. (2010)
F, UT, WR, UT, WC, UT, W
363636
14; 83%HRmax; 1.8; 60
14; 82%HRmax; 1.9; 60
No intervention
–––
6%↑*$
7%↑*$
5%↓NS
–––
11%↑*3%↑NS0.5%↑NS
–––
29%↑*$
33%↑*$
17%↑*
Jackman et al. (2013)
F, UT, W 27 16; 83%HRmax; 1.8; 60
– – 0.22↑NS – – LL:29%↑*RL:15%↑NS
Mohr et al. (2014a)
F, UT, Wmh 35–50 15; 80.5%HRmax; 3.0; 60
– – – – 111%↑$ –
Mohr et al. (2014b)
MS, UT, Wmh
35–50 15; 72.5%HRmax; 2.9; 60
– – – – 45%↑*$ –
Mohr et al. (2015)
HS, UT, Wmh
35–50 15; 85.5%HRmax; 2.9; 15–25
– – – – 58%↑*$ –
C, UT, Wmh 35–50 No intervention – – – – 1%↓NS –Krustrup
et al. (2017)
F, UT, Wmh
C, UT, Wmh35–5035–50
52; 81%HRmax; 2.5; 60
No intervention
––
––
0.26↓$ (20 m)
0.06↑NS (20 m)
––
122%↑$
2%↑NS––
European Journal of Applied Physiology
1 3
Osteogenic impact and training effects in untrained women
As the populations of western societies have grown older and lifestyles have become more sedentary during the later decades, the prevalence of osteoporosis has increased con-siderably, especially for women. Thus, in 2010, 22 million women and 5.5 million men in the EU were estimated to suf-fer from osteoporosis (Hernlund et al. 2013; Svedbom et al. 2013), and it seems incontestable that these numbers will increase in the coming years. For both genders, peak bone mass is attained during the third decade of life followed by a decrease of approximately 1% annually from the late forties onwards (Bonjour et al. 2009). However, due to the post-menopausal oestrogen withdrawal, women are subjected to an additional bone loss, which results in a reported annual decrease in bone mineral density (BMD) and content (BMC) of, respectively, 1.9 and 1.3% from the onset of menopause to 67 years of age (Ahlborg et al. 2003). Thus, the increased risk of osteoporosis, therefore, makes it highly relevant to focus on the osteogenic stimulus from bone-loading exercise to promote bone health and decrease fracture risk in women. A meta-analysis (Howe et al. 2011) concluded that there seems to be “a relatively small significant, but possibly important, osteogenic effect of exercise on bone density in postmeno-pausal women”, but that the quality of the included studies was generally low due to, e.g., inadequate training intensities.
A high musculoskeletal training intensity is associated with large forces applied to bone with a high rate of force production (Bennell et al. 1997; von Stengel et al. 2007), and the key stimuli are the resulting strain magnitude and strain rate (Lanyon 1996; Turner 1998; Turner and Robling 2003). Thus, high-impact training as well as heavy-resist-ance training with large power outputs (Vincent and Braith 2002; von Stengel et al. 2007) are preferable to training with lower musculoskeletal intensity. In addition, it has been argued that multimodal training regimens (Beck et al. 2017; Gianoudis et al. 2014) and odd-impact activities like, e.g., ball games (Nikander et al. 2005, 2009) increase the osteogenic stimuli due to the diverse and intermittent forces applied to the skeleton, which may diminish the desensitiza-tion of bone that is seen with repetitive stimuli (Turner 1998; Turner and Robling 2003). In agreement with this notion, randomized controlled trials (RCTs) have demonstrated that recreational football can improve areal BMD and biochemi-cal bone turnover marker (BTM) profile in untrained men (Uth et al. 2016; Helge et al. 2014a, b). Moreover, from a recent cross-sectional study showing that female elite foot-ball players exhibit significantly higher total BMD (13%) and BMC (23%) as well as resting plasma osteocalcin (45%) than untrained controls (Jackman et al. 2013) it can be hypothesized to hold for women as well. This is sup-ported by RCTs reporting that for untrained premenopausal
women football training for 4 months (Krustrup et al. 2010b) and for 16 months (Krustrup et al. 2010c) resulted in sig-nificant musculoskeletal benefits compared to controls, and that 14 weeks of football training assessed with quantitative computed tomography was superior to running as well as to a sedentary control group (Helge et al. 2010). Thus, for the football group volumetric BMD increased significantly by 2.1% in right tibia and 2.6% in left tibia. In the left tibia the increase was significantly higher than for the running group and controls whereas the increase in the right tibia was significantly higher than for controls (Helge et al. 2010).
In accordance with the above findings, BMD in the femo-ral shaft and trochanter increased (P < 0.05) by 1.7 and 2.4%, respectively, in premenopausal women after 15 weeks of football training, which was significantly higher than after moderate-intensity continuous swimming, but not higher than after high-intensity interval swimming (Mohr et al. 2015). The resting plasma concentrations of BTMs seemed to support the football-induced increases in BMD with con-comitant increases (P < 0.05) in the plasma markers of bone formation, procollagen type 1 N propeptide (P1NP; 52%) and osteocalcin (37%), but also in the resorption marker C-terminal telopeptide (CTX-1); 42% (Mohr et al. 2015). Overall these changes may indicate an increased bone turno-ver rate in premenopausal women after recreational football training without any changes after swimming training. A similar significant increase in resting osteocalcin was seen for premenopausal women after 16 weeks of small-volume small-sided football training (37%) (Jackman et al. 2013) and for female hospital employees after 12 weeks of recrea-tional football training (21%) or zumba (10%) (Barene et al. 2013) but without any changes in BMD or BMC. As the bone turnover rate is relatively low with a remodeling cycle of approximately 4 months it takes several months to evalu-ate the osteogenic impact of exercise training on BMD and BMC, and from the present BTM data it seems promising that the osteogenic impact from exercise could be predicted from assessment of BTM even after a relatively short period of training.
In a comparison of the acute BTM response due to foot-ball training (Bowtell et al. 2016) it is reported that P1NP was significantly increased during 15 min of football training as well as during 60 min of football training. It is remarkable that CTX-1 did not change and that osteocalcin was still sig-nificantly elevated in all groups after 48 h of recovery. It may be hypothesized that the overall changes in BTM induced by football training reflect a true anabolic response character-ized by an uncoupling of resorption (CTX-1) and formation processes (osteocalcin, P1NP) in bone remodeling.
In summary, both BMD and BTM results show that for premenopausal women football exerts an important osteo-genic impact that is greater than with repetitive training such as running and swimming. When evaluating musculoskeletal
European Journal of Applied Physiology
1 3
adaptations to recreational football, it appears that football training may be associated with higher BMD, stronger bones and a decreased risk of osteoporosis and falls. Despite the increased risk of low bone strength, fractures and osteopo-rosis for postmenopausal women, the osteogenic effects of football are yet to be evaluated in depth for that group.
Implications for female patient groups with hypertension, type 2 diabetes and hormonal disturbances
A recent systematic review by Pedersen and Saltin (2015) provides strong evidence that exercise training can by implemented as treatment for various non-communicable diseases such as hypertension and T2DM. Also, two special issues published in Scandinavian Journal of Medicine and Science in Sports in 2010 and 2014 highlighted the exten-sive research carried out into the health effects of small-sided football training including football as treatment for different patient groups. A number of the RCTs presented in these issues are linked to the “exercise as medicine” con-cept of applying football training as an exercise protocol to treat non-communicable diseases (“football training as medicine”).
Football as treatment for female patients with hypertension
Arterial hypertension is a major risk factor for cardiovascular mortality and morbidity, including stroke, coronary artery dis-ease, atrial fibrillation, renal insufficiency, and heart failure with or without reduced left ventricular (LV) ejection fraction (Lewington et al. 2002). Thus, a number of studies have tested the hypothesis that recreational football training provides an efficient treatment for hypertensive individuals (Mohr et al. 2014a; Andersen et al. 2014; av Fløtum et al. 2016). In a study by Mohr et al. (2014a), for example, mean arterial pressure (MAP) was lowered by 8 mmHg after 15 weeks of small-sided football training compared to an inactive control group in mid-dle-aged sedentary hypertensive women. The clinical impor-tance of this finding is underlined by the fact that for both sexes at ages 40–69 years, each 10 mmHg reduction of sys-tolic or diastolic blood pressure is associated with an approxi-mately 30% decrease in risk of death from stroke or ischae-mic heart disease (Lewington et al. 2002). Thus, both systolic and diastolic blood pressure were nearly normalized after the football intervention. Moreover, several other cardiovascular disease risk factors such as fat mass, resting heart rate and physical capacity as well as total plasma cholesterol and tri-glyceride levels were improved in the football training group. Similar findings, including structural and functional cardiac adaptations, have been reported in middle-aged hypertensive
men after 6 months of football training (Andersen et al. 2014). The above-mentioned study by Mohr et al. (2014a) was part of a larger study that also tested the effects of 15 weeks of high-volume low-intensity vs low-volume high-intensity swimming training on cardiovascular health in hypertensive sedentary women (see Mohr et al. 2014b). In contrast to football training (Mohr et al. 2014a), the two swimming training interventions did not significantly lower either MAP or diastolic blood pres-sure (Mohr et al. 2014b). These findings thus suggest that football training may be a more efficient treatment protocol than swimming training for women with moderate hyperten-sion. Moreover, it has been demonstrated that twice-weekly football training over 20 weeks induces a greater blood pres-sure reduction in hypertensive women (MAP > 100 mmHg) than in normotensive women (av Fløtum et al. 2016). The impact of football training on blood pressure is also evident in young girls. Recently, it was demonstrated that 11 wks of football training (2 × 45 min/week) lowered mean arterial pressure by 2 mmHg in 10–12-year-old children (Ørntoft et al. 2016a, b). Finally, a recent meta-analysis and system-atic review by Milanović et al. (2015) demonstrated multiple broad-spectrum positive effects of recreational football on health-related physical fitness in both sexes in comparison to no-exercise controls, including beneficial effects on several parameters affecting cardiovascular health such as maximal oxygen uptake, blood pressure, resting heart rate and fat mass. For hypertensive individuals the observed effects were con-sidered ‘most likely beneficial’ [effect size (ES) 0.64; 95% confidence interval (CI) 0.37, 0.90] and ‘likely beneficial’ (ES 0.39; 95% CI 0.00, 0.77) for the diastolic and systolic blood pressure (Milanović et al. 2017). For some cardiovas-cular health parameters including maximal oxygen uptake, football training appears to elicit superior effects compared to other training methods (Milanović et al. 2017). Several cardio-vascular adaptations of importance for arterial hypertension have been demonstrated to be improved by football training in women (Table 1). Thus, football training appears to have an efficient broad-spectrum treatment potential for hyperten-sion in women.
Football as treatment for type 2 diabetes in women
T2DM is a major worldwide health challenge that is asso-ciated with considerable morbidity and mortality (Asso-ciation 2014). For example, in the US alone, the incidence of T2DM increased 117% from 1980 to 2011 (Al Tunaiji et al. 2014) and as many as one in three adults are projected to develop T2DM by 2050 if the current trends continue (Boyle et al. 2010). T2DM is thus imposing a significant economic burden on the healthcare system. Since T2DM is partly associated with an inactive lifestyle, the most recent diabetes care recommendations conclude that education on self-management is essential (Standards of medical care in
European Journal of Applied Physiology
1 3
diabetes 2015). In relation to exercise, patients with diabetes are instructed to perform at least 150 min/week of moder-ate-intensity aerobic physical activity combined with resist-ance training (Lanhers et al. 2017). Recent findings indicate that high-intensity intermittent training may be beneficial for improving metabolic health and blood glucose control in women (Nordsborg et al. 2015; Connolly et al. 2014) and individuals with, or at risk of T2DM (Little and Francois 2014). Since football training is a complex training method encompassing endurance, high-intensity exercise and resist-ance training in the same training session (Krustrup et al. 2010a, b, c; Krustrup 2017) (see Fig. 1), it may be a suitable exercise training therapy for women with T2DM.
It has been shown that 12 weeks of football train-ing (40 min 3 times/week) combined with diet advice in 48–68-year-old patients with T2DM improves insulin sen-sitivity (de Sousa et al. 2014, 2016). In this study two-thirds of the patients were women, and in addition to improving blood glucose regulation, the football and diet therapy also increased maximal oxygen uptake and reduced blood cho-lesterol and triglycerides. The adaptations in the football and diet group were greater than for diet alone (de Sousa et al. 2014). These findings are in accordance with several other football training studies in women (Table 5), as well as in men (Andersen et al. 2014). Moreover, football training has been shown to markedly improve skeletal muscle oxida-tive capacity, such as maximal activity of citrate synthase and 3-hydroxyacyl-CoA dehydrogenase, as well as mito-chondrial complex protein expression (Bangsbo et al. 2010; Krustrup et al. 2010a; Nordsborg et al. 2015; Table 2), which is essential in T2DM patients (Pedersen and Saltin 2015). Additionally, T2DM has been closely linked with obesity and low muscle mass (Pedersen and Saltin et al. 2015). A consistent finding in football training studies in women across the lifespan is a decrease in body fat con-tent and an increase in muscle mass (Ørntoft et al. 2016, b; Table 3). It has been shown that T2DM patients face several other health challenges, such as a much higher prevalence of cardiovascular deficiencies compared to health individuals (Rijzewijk et al. 2008; Aneja et al. 2008). Thus, the broad-spectrum adaptations of football training may be the optimal treatment for this specific patient group.
In conclusion, there is evidence that football training has a high potential as treatment protocol for patients with arte-rial hypertension and T2DM.
Aging process and hormonal disturbances in women: additional potential health benefits of football training
The aging process in women is linked to changes in blood hormone level and several behavioral and physiological disturbances, including a progressive decrease in physical
activity contributing to changes in metabolism and some lev-els of overweight leading to an increased inflammatory sta-tus. In this context postmenopausal women warrant special attention (Stehr and Lengerke 2012), since lifestyle changes may further modulate these disturbances in these women. For example, de Sousa et al. (data not published) investi-gated metabolic and hormonal modulation after 12 weeks of football training and a calorie-restricted diet in previously untrained postmenopausal women. Luteinising hormone (LH) levels decreased significantly in the football group after 12 weeks of intervention (pre 25.0 vs post 20.3 IU/L), whereas the diet group alone had no alterations. These find-ings are supported by Scheid et al. (2013), who have shown that elevations in ghrelin following a 12-week exercise and diet programme leading to weight loss are associated with a decrease in LH pulsatility. Importantly, as reported by Hagner-Derengowska et al. (2015), a higher LH level may be associated with the prevalence of breast cancer in pre-menopausal and postmenopausal women, suggesting that the decrease in LH levels after football training may be a poten-tial mechanism for the favorable effect of regular training and weight reduction on cancer development (Brown et al. 2012; Bhaskaran et al. 2014).
Locomotor activity and physiological demands of recreational football for women vs men
Distance covered during a 1-h session of 7v7 for women in total, high-intensity running and sprinting has been reported to be 3.8, 0.5 and 0.1 km, respectively, which was less than observed in men (5.0, 0.9, and 0.2 km, respectively; Krus-trup et al. 2010c). Recent studies using GPS technology have found similar values for total (3.7 km) and high-intensity (0.6 km) distances for women (Bowtell et al. 2016), but lower (3.6 and 0.4 km, respectively) values for men than previously reported albeit that in these studies only 54 and 48 min of active playing time were analyzed (Randers et al. 2014). Moreover, it should be noted that different speed categories are used for men and women, which may affect values for high-intensity running and sprinting.
A study by Randers et al. (2010) found a similar number of total activities (951 vs 886 activities), high-intensity runs (100 vs 98 runs) and sprints (15 vs 16 sprints) in women and men, respectively. The duration of high-intensity runs (1.5 vs 1.9 s) and sprints (1.5 vs 2.3 s) was lower in women than men (Randers 2011), so differences between women and men are found in the distance of each intense run rather than in the number of intense runs performed. A minor difference is also found in many of the intense football-specific actions, as more shots and tackles are found in women, whereas more jumps, headers as and sideways/backward running bouts
European Journal of Applied Physiology
1 3
Tabl
e 5
Cha
nges
in b
lood
lipi
ds a
nd m
arke
rs o
f glu
cose
han
dlin
g in
unt
rain
ed w
omen
as a
resu
lt of
a p
erio
d of
recr
eatio
nal f
ootb
all t
rain
ing
(F) c
ompa
red
to ru
nnin
g (R
), zu
mba
(Z),
swim
min
g (M
S, H
S) o
r ina
ctiv
e co
ntro
ls (C
)
Cha
nges
bet
wee
n pr
e an
d po
st tra
inin
g in
terv
entio
n (u
nles
s oth
erw
ise
stat
ed)
C c
ontro
ls, C
hol c
hole
stero
l, F
foot
ball,
HbA
1c g
lyca
ted
hem
oglo
bin,
HD
L hi
gh-d
ensi
ty li
popr
otei
n, H
OM
A-IR
hom
eost
atic
mod
el a
sses
smen
t for
insu
lin re
sist
ance
, HRm
ax m
axim
al h
eart
rate
, H
S hi
gh-in
tens
ity sw
imm
ing,
LD
L lo
w-d
ensi
ty li
popr
otei
n, M
men
, mh
mild
hyp
erte
nsiv
e su
bjec
ts, M
S m
oder
ate-
inte
nsity
swim
min
g, N
S no
t sig
nific
ant,
R ru
nnin
g, t
type
2 d
iabe
tics,
Tota
l-cho
l to
tal p
lasm
a ch
oles
tero
l, U
T un
train
ed, W
wom
en, Z
zum
ba*S
igni
fican
t diff
eren
ce fr
om 0
wee
ks$ Si
gnifi
cant
gro
up d
iffer
ence
com
pare
d to
con
trol
Stud
yA
ctiv
ity,
targ
et g
roup
, ge
nder
Age
(yea
rs)
Trai
ning
inte
rven
tion:
du
ratio
n (w
eeks
), in
tens
ity (%
), fr
e-qu
ency
(per
wee
k),
sess
ion
dura
tion
(min
)
Tota
l-cho
l re
st (m
mol
/l)H
DL-
chol
re
st (m
mol
/l)LD
L-ch
ol re
st (m
mol
/l)Tr
igly
cerid
es
rest
(mm
ol/l)
Fasti
ng
gluc
ose
rest
(mm
ol/L
)
HbA
1c re
st (%
)H
OM
A-I
RG
luca
gon
(ρg/
mL)
Bar
ene
et a
l. (2
014a
)F,
UT,
WZ,
UT,
WC
, UT,
W
25–6
525
–65
25–6
5
40; 7
8.6%
HR
max
; 1.
5; 6
040
; 74.
9%H
Rm
ax;
1.2;
60
No
inte
rven
tion
0.0↔
NS
0.2↓
NS
NS
0.0↔
NS
0.0↔
NS
NS
0.1↓
NS
0.2↓
NS
NS
0.0↔
NS
0.1↑
NS
NS
0.1↑
NS
0.2↓
NS
NS
– – –
– – –
– – –
De
Sous
a et
al.
(201
4)F,
UT,
W
t + M
t
C, U
T,
Wt +
Mt
48–6
848
–68
12; 8
3%H
Rm
ax; 3
; 40;
F
+ D
Die
t gro
up
0.6↓
*$
0.4↑
NS
0↔N
S0↔
NS
0.4↓
*$
0.3↑
NS
0.4↓
*$
0.1↑
NS
1.1↓
*1.
1↓*
1.0%↓*
0.8%↓*
1.7↓
*1.
2↓N
S17
.9↓*
10.8↓N
S
Kru
strup
et
al.
(201
0a)
F, U
T, W
R, U
T,W
C, U
T, W
19–4
719
–47
19–4
7
16; 8
3%H
Rm
ax; 1
.8;
6016
; 82%
HR
max
; 1.8
5;
60N
o in
terv
entio
n
0.1↓
NS
0.1↓
NS
0.2↑
NS
0.1↑
NS
0.1↑
NS
0.1↑
NS
0.2↓
NS
0.0↔
NS
0.1↑
NS
0.1↓
NS
0.1↑
NS
0.1↑
NS
0.0↔
NS
0.4↓
NS
0.1↑
NS
– – –
– – –
– – –
Moh
r et a
l. (2
014a
)F,
UT,
Wm
h35
–50
15; 8
0.5%
HR
max
; 3.
0; 6
00.
4↓*$
NS
NS
0.2↓
*$–
––
–
Moh
r et a
l. (2
014b
)M
S, U
T, W
mh
35–5
015
; 72.
5%H
Rm
ax;
2.9;
60
0.2↓
NS
0.1↑
NS
0.1↓
NS
0.1↓
NS
––
––
Moh
r et a
l. (2
015)
HS,
UT,
Wm
h35
–50
15; 8
5.5%
HR
max
; 2.9
; 15
–25
0.1↓
NS
0.0↔
NS
0.1↓
NS
0.1↓
NS
––
––
C, U
T, W
mh
35–5
0N
o in
terv
entio
n0.
1↑N
S0.
1↓N
S0.
1↓N
S0.
3↑N
S–
––
–K
rustr
up
et a
l. (2
017)
F, U
T, W
mh
C, U
T, W
mh
35–5
035
–50
52; 8
1%H
Rm
ax; 2
.5;
60N
o in
terv
entio
n
0.0↔
NS
0.5↑
*0.
2↑*$
0.2↓
*0.
1↓N
S0.
3↑*
0.1↓
$
0.2↑
*0.
3↑N
S0.
2↑N
S– –
– –– –
European Journal of Applied Physiology
1 3
are seen in men (Krustrup et al. 2010a, b, c; Pedersen et al. 2009; Randers et al. 2010).
Heart rate measurements during recreational small-sided games for women have shown mean relative heart rates rang-ing from 76 to 84% of individual HRmax with peak heart rates reaching 94–99% HRmax (av Fløtum et al. 2016; Bow-tell et al. 2016; Connolly et al. 2014; Randers et al. 2010; Mohr et al. 2014a). Time spent with HR above 90%HRmax varies from 11 to 21% of total playing time in women (Rand-ers et al. 2010; Mohr et al. 2014a, b; av Fløtum et al. 2016). Thus, mean and peak heart rates for women are similar to, or slightly lower than, those observed for men (80–89 and 95–99% HRmax, respectively). Moreover, time spent with HR above 90% HRmax has been shown to be 20–41% in men (Randers et al. 2010, 2012, 2014; Krustrup et al. 2009, 2010a, b, c). In the study by Randers et al. (2010), heart rate response in women and men was compared directly and mean and peak heart rate as well as time spent with heart rate > 90% HRmax was lower in women than in men.
Blood metabolites during training have been reported in one study where blood glucose increased from 4.1 to 5.6 mmol/L, whereas blood lactate increased from 0.6 to between 2.6 and 3.4 mmol/L (Bowtell et al. 2016). The blood glucose values were similar to those reported in untrained men (Randers et al. 2010), whereas the blood lactate values were lower than typically reported in men with peak values of 5.2–7.4 mmol/L (Krustrup et al. 2010a, b, c; Randers et al. 2010, 2014). In women, plasma FFA increased from ~ 500 to 1267 mg/L after training (Bow-tell et al. 2016), whereas increases up to 600–900 µmol/L have been reported in men (Randers et al. 2010, 2014). Plasma ammonia was also increased in women reaching 57 µmol/L but dropped to 40 µmol/L at the end of the ses-sion (Bowtell et al. 2016). As observed for lactate, markedly higher values have been reported in men with increases up to 140–170 µmol/L (Randers 2011; Randers et al. 2014), which, combined with the lactate values, indicates differ-ences between the genders in anaerobic performance dur-ing recreational small-sided games. In the study by Bowtell and colleagues (2016) increases in plasma osteocalcin and plasma CK were reported, indicating significant impact on the musculoskeletal system. Gender differences have also been found in muscle metabolites, although not all statisti-cally different. Resting muscle lactate was 6.0 mmol/kg d.w. and increased during 7v7 recreational football almost three-fold to 17 mmol/kg d.w. A similar roughly threefold increase was seen in men during 7v7 recreational football, but values at rest were higher and increased to a higher level in men (12–30 mmol/kg d.w.) (Randers et al. 2010). Muscle CP decreased by 15% (82–64 mmol/kg d.w.) in women and 31% (81–50 mmol/kg d.w.) in men. Muscle glycogen decreased by 11% during a 1-hour session of recreational football training in women (424–372 mmol/kg d.w.), which was less
than the 28% decrement observed in men (422–304 mmol/kg d.w.) (Randers et al. 2010). Thus, gender differences are also apparent in utilization of muscle metabolites during recreational football training. Interestingly, although the physiological response to small-sided recreational football games seems slightly lower in untrained women compared to untrained men, a higher rating of perceived exertion was reported by untrained women than untrained men (5.8 vs 3.9; Elbe et al. 2010, 2016).
In summary, small-sided recreational football for untrained women is an activity with a high number of activ-ity changes encompassing several short high-intensity bouts, which lead to a marked increase in markers of cardiovascu-lar, metabolic and musculoskeletal fitness.
Conclusions and future research
The present review emphasizes that regular recreational football training (i.e., 2 × 1 h per week) for untrained women results in marked improvements of myocardial function and a 7–15% increase in maximal oxygen uptake over 12–16 weeks, with similar improvements to those in young, middle-aged or elderly untrained men. Moreover, MAP is shown to decline by 2–6 mmHg in normotensive untrained women and 6–8 mmHg in hypertensive untrained women, slightly less than their male counterparts. It is also concluded that short-term (< 4 months) and medium-term (4–16 months) recreational football training has a major ben-eficial impact on metabolic health profile in women, with fat losses of 1–3 kg and improvements in blood lipid profile after football training alone as well as football combined with a calorie-restricted diet. Lastly, 2 × 1 h per week of rec-reational football training for women was shown to elevate lower extremity bone mineralization within 4 months and whole-body bone mineralization in medium-term interven-tions, with superior effects for football compared to running and swimming. These training adaptations are related to the high heart rates, high number of fast runs, and the multiple speed, direction and movement changes occurring during recreational football training for untrained women, albeit that heart rates and occurrence of intense runs and decel-erations are slightly lower than for untrained men. Nonethe-less, we conclude that regular small-sided football training for women is an intense and versatile type of training that combines elements of high-intensity interval training (HIIT), endurance training and strength training, thereby providing optimal stimuli for cardiovascular, metabolic and musculo-skeletal fitness. Recreational football is, therefore, an effec-tive tool for the prevention and treatment of lifestyle diseases in young and middle-aged women, including hypertension, T2DM and osteopenia.
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Future research is warranted in relation to the use of recreational football and walking football for women aged 60–80 years. Considerable training and health effects of small-sided football in elderly men have been demonstrated (Helge et al. 2014a, b; Uth et al. 2016) and pilot studies involving elderly women suggest the feasibility of the walking football and Football Fitness concept for women (av Fløtum et al. 2016; Reddy et al. 2017). Football training may also be of particular relevance in relation to musculoskeletal disorders such as osteoarthritis and rheumatoid arthritis due to the anti-inflammatory effects of high-intensity training (Pedersen and Saltin 2015). Since old age is the main predictor of neurode-generative diseases such as Alzheimer’s disease, which covers over 50% of all dementia causes (Pedersen and Saltin 2015), walking football could also be tested as a treatment of elderly suffering from dementia. Exercise training may also prevent dementia, possibly via increases in hippocampal volume stimulated by exercise-induced upregulation of brain-derived neurotrophic factor concentrations in the brain (Pedersen et al. 2009). Thus, effects of recreational or walking football may be examined in elderly women aimed at delaying or preventing impairment of cognitive function. Another neurological dis-ease to be investigated in future recreational football studies may be Parkinson disease, since exercise may attenuate the degree of injury to midbrain dopaminergic neurons, and may restore basal ganglia function through adaptive mechanisms of dopamine and glutamate neurotransmission (Speelman et al. 2011). Along this line, it is relevant to conduct further studies of injury prevention and injury reduction for elderly women and female patient groups participating in walking football and Football Fitness. Indeed, it is well known that the number of injuries is reduced with proper warm-up including strength and balance exercises, and by conducting small-sided football training rather than 11v11 match-play, but large-scale controlled studies are warranted to provide optimal recom-mendations for the introduction of safe concepts for partici-pants with reduced physical capacity. Last but not the least, it would be of interest to investigate whether interventions with small-sided football training can be used to reduce the nega-tive side effects of hormone treatment for women after breast cancer, as Football Fitness has been shown to counteract the negative side effects of antiandrogen treatment against pros-tate cancer, including increases in fat mass and loss of muscle and bone strength (Uth et al. 2016).
Perspectives: implementation of the club‑based Football Fitness for women
Football is the most popular sport in the world, with more than 275 million registered club football players and an esti-mated 400–500 million people regularly playing football
(FIFA 2015; Krustrup and Bangsbo 2015). Girls’ and wom-en’s football constitutes about 10% of these players, but the number and fraction of female football players is expanding markedly worldwide and football is the most rapidly increas-ing female sport over the last decade. Traditionally the play-ers are playing grassroot club-based tournament football, club-based elite football, commercial tournament-based football or unorganized recreational football (Bennike et al. 2014). However, the studies on the fitness and health effects of recreational football presented in the present review have led to creation of a concept that can be considered a fifth type of football participation, i.e., the so-called “Football Fitness” concept. This concept that is founded on an evi-dence-based program created by the Danish FA and profes-sor Peter Krustrup in 2010 was implemented nationwide in the Danish football clubs from 2011 and is now supported by nationwide courses for coachess run by the Danish FA and the University of Southern Denmark. In brief, the pro-gram consists of 1-hour training sessions with a 10–15 min injury preventing warm-up followed by 20–25 min of small-sided drills and pair-based technical exercises and ended by 20–30 min of small-sided football training 4v4, 5v5 or 6v6 with one ball and two goals, but with rule adjustment according to the participant group. In Denmark, the Football Fitness concept is being offered for all adult women by local football clubs with a low membership fee, as these teams are not participating in tournaments. Usually these teams train two times 1-h per week year-round, as recommended based on the available scientific results, or 1 h once per week year-round.
The Football Fitness programme is now running in more than 300 Danish football clubs and the ambitions goal for the Danish FA is to reach 600 clubs within the next two years, corresponding to 40% of all Danish football clubs. The implementation of the Football Fitness concept has been evaluated scientifically and one interesting finding was that more than three-fourths of the participants were women (Bennike et al. 2014). Apart from the physiological ben-efits of regular Football Fitness training, research has dem-onstrated that Football Fitness is a motivating and socially engaging activity and works well for women in all age groups, irrespective of social background, physical fitness and skill level (Ottesen et al. 2010; Elbe et al. 2010; Bennike et al. 2014). Those factors seem to be important for the pop-ularity of Football Fitness among women and are of obvious relevance for continued adherence with training (Ottesen et al. 2010; Nielsen et al. 2014; Elbe et al. 2016). Recently, we evaluated the implementation of Football Fitness on a national scale in the Faroe Islands, which is a small country with 19 football clubs and a total for 50,000 habitants (av Fløtum et al. 2016). The Faroese FA and the University of Faroe Islands launched the program in collaboration with the Danish FA. All football clubs offered Football Fitness for all
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adult men and women starting in the spring 2015. Within a few weeks, more than 800 participants turned up in the clubs to take part in the Football Fitness training, corresponding to more than 2% of the entire adult population. Surprisingly, as many as 95% of the participants were women, and in the age groups 20–40 and 40–60 years as many as 4 and 5% of the entire female population participated. A majority of these women had not played football before and, interestingly, the recruitment covered two or three generations of women that started playing together. After 18 weeks of training approxi-mately 45% of original participants remained active, and large health effects were observed (av Fløtum et al. 2016). Thus, Football Fitness appears to be a feasible concept with considerable potential to recruit inactive women for physical training in the Scandinavian countries. Considering that this type of training is an intense and effective type of physical exercise to promote health and that at the same time foot-ball training enhances motivational and social aspects that promote adherence, Football Fitness is considered to be a very promising component of the “Exercise is medicine” platform. It will be interesting to follow the outreach and effects of this concept in other Northern European countries, but certainly also in different ethnic and cultural settings.
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