Twenty-four-hour rhythms of muscle strength with a

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Twenty-four-hour rhythms of muscle
strength with a consideration of some
methodological problems
a
b
b
Leana Gonçalves Araujo , Jim Waterhouse , Ben Edwards ,
c
a
Eduardo Henrique Rosa Santos , Sérgio Tufik & Marco Túlio de
Mello
a
a
Department of Psychobiology, Federal University of São Paulo,
UNIFESP, São Paulo, SP, Brazil
b
Research Institute for Sport and Exercise Sciences, Liverpool
John Moores University, Liverpool, UK
c
Physical Education Faculty, Federal University of Goiás, Goiania,
GO, Brazil
Available online: 24 May 2011
To cite this article: Leana Gonçalves Araujo, Jim Waterhouse, Ben Edwards, Eduardo Henrique Rosa
Santos, Sérgio Tufik & Marco Túlio de Mello (2011): Twenty-four-hour rhythms of muscle strength
with a consideration of some methodological problems, Biological Rhythm Research, 42:6, 473-490
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Biological Rhythm Research
Vol. 42, No. 6, December 2011, 473–490
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Twenty-four-hour rhythms of muscle strength with a consideration of
some methodological problems
Leana Gonçalves Araujoa*, Jim Waterhouseb, Ben Edwardsb, Eduardo Henrique
Rosa Santosc, Sérgio Tufika and Marco Túlio de Melloa
a
Department of Psychobiology, Federal University of São Paulo, UNIFESP, São Paulo, SP,
Brazil; bResearch Institute for Sport and Exercise Sciences, Liverpool John Moores University,
Liverpool, UK; cPhysical Education Faculty, Federal University of Goiás, Goiania, GO, Brazil
(Received 24 September 2010; final version received 26 October 2010)
The aim of the present study was to show the presence of circadian rhythm of
muscle strength under a standardised protocol with controlled parameters to
support suitable observation of variability during the day. Eight male volunteers
were evaluated once a week for 6 weeks at six different times. Rectal temperature,
peak torque (PT), maximum work and the average power of the flexor and
extensor knee muscles in the isokinetic mode, as well as of PT in maximum
voluntary isometric contraction of knee extensors at 608 knee flexion, were
measured. The present study showed rhythms with a period of 24 hours in some
indices of muscle strength performance at both speeds of movement and muscle
groups. To our knowledge, this is the first study that has shown the presence of
circadian rhythm in all speeds of movement and muscle groups tested under strict
standardised protocol.
Keywords: daily rhythm; muscle strength; standardisation; isokinetic movement
1. Introduction
Chronobiological oscillations in human physical performance have implications for
sports training and competition and also for the rehabilitation of individuals.
Twenty-four-hour rhythms have been demonstrated at rest in metabolic variables
(e.g. oxygen consumption and carbon dioxide output), ventilatory and cardiorespiratory responses to exercise (e.g. minute ventilation, heart hate, cardiac output,
and blood pressure), thermoregulatory variables (e.g. core and skin temperatures
and blood flow) and hormonal secretion (e.g. cortisol and catecholamines) (Reilly
et al. 2000).
Studies in humans on the 24-hour rhythm of isokinetic muscle strength (Cabri
et al. 1988, Wyse et al. 1994, Gauthier et al. 1996, 2001, Deschenes et al. 1998,
Martin et al. 1999, Callard et al. 2000) show conflicting results, however. The
controversy might be accounted for at least partly by methodological factors, such as
different experimental conditions, the use of measurements of performance and
rhythm markers that are not accurate and reproducible, lack of familiarisation of
*Corresponding author. Email: [email protected]
ISSN 0929-1016 print/ISSN 1744-4179 online
Ó 2011 Taylor & Francis
http://dx.doi.org/10.1080/09291016.2010.537444
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474
L.G. Araujo et al.
subjects with the test procedure, effects of muscle temperature with warm-up and
inter-investigator reliability. Differences might also result from individual variability
of the subjects regarding chronotype, gender, level of physical conditioning and
training (Reilly and Bambaeichi 2003).
To reduce such differences, it is vital that sufficient control of the volunteers and
protocol be observed. These controls should include monitoring sleep to establish no
sleep deprivation is present; monitoring diet in the hours before the experiment, to
ensure that no stimulants or depressants of the CNS are taken; prohibition of
exercise prior to testing; completion of sufficient sessions to familiarise volunteers
with each exercise; reproducibility and reliability in the use of the isokinetic
dynamometer; assessment of all performance measures by the same evaluator;
sufficient time to recover between sessions and between the different exercises within
each session; a frequency of sampling of at least once per four hours and performance
of the experiment under the same laboratory conditions and season. With these
standardisations, it is possible to minimise the ‘‘noise’’ that is present in any study.
However, none of the studies previously carried out (and cited above) have
observed all these controls, and this lack of detailed comparability between the
studies is likely to have contributed to the lack of agreement between them. The
objective of the present study was to investigate the influence of time of the day on
several measures of muscle strength whilst observing a controlled protocol with all
the controls together used separately in the articles cited above. The precautions
taken in the present study, aimed to standardise this protocol, will be stressed in the
Material and Methods section and further consideration of them will be given in the
Discussion section.
2.
Material and methods
2.1. Volunteers
After explanation of the protocol and requirements to the volunteers, they signed a
formal Consent Form of Participation. The Committee of Ethics in Research
Involving Humans of the university approved the study under process # CEP 0424/
06. The study methods follow the recommendations of the Declaration of Helsinki of
1975 for investigations with humans, and the standards for chronobiology
researchers reported by Touitou et al. (2004 and 2006) and Reilly and Bambaeichi
(2003). The procedures were conducted during the winter time.
Eight male volunteers, moderately active (as defined by the Short Questionnaire
for the Measurement of Habitual Physical Activity; Baecke 1982), aged 27+3.2
years, with body mass 74.6+5.3 kg, height 174.6+6.3 cm, body mass index (BMI)
24.4+1.9 kg/m2, body fat 18%+6.7% and lean mass 82%+6.7% (both assessed by
plexmografia), took part. The exclusion criteria were history of orthopaedic surgery;
osteomyoarticular disease or lesion; neurological disorders; excessive sleepiness, as
defined by the Epworth Sleepiness Scale (Johns 1991) and use of any medication.
Additionally, volunteers were asked to refrain from sleep deprivation during the
period of the experiment, sleeping the time necessary to wake up rested and do not
wake up with the alarm clock, and had not performed shift work and/or taken a
transmeridional trip in the 10 days preceding the beginning of experiment.
Volunteers were not of an extreme chronotype – in other words, they were
‘‘moderate evening types’’, ‘‘moderate morning types’’ or ‘‘indifferent’’, as measured
by the questionnaire of Horne and Östberg (1976). The volunteers went through a
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Biological Rhythm Research
475
clinical examination that included routine blood tests, effort electrocardiogram
(ECG) and ECG at rest to make sure they were fit for undertaking physical
exercise.
The volunteers were informed about the standard recommendations regarding
the length and time of sleep. They slept as much as necessary in the night before a
test session to feel rested. It was at least six hours for all volunteers, which was
confirmed by actigraphy and the Karolinska sleep diary (Akerstedt and Gillberg
1990). They were allowed to sleep before the 06:00 hours test, but had to remain
awake for the 02:00 hours test (Reilly and Down 1986, Atkinson and Reilly 1996).
As regards diet, the last meal before each test session was performed 3 hours in
advance which was confirmed by phone call, to prevent post-prandial thermogenic
effects, and they were recommended not to ingest caffeine or alcohol within the 24
hours preceding the data collection, which was confirmed by a food diary.
Additionally, volunteers were asked to refrain from heavy physical activity during
the experiment (Atkinson and Reilly 1996).
2.2.
Experimental design
2.2.1. Familiarisation sessions
In this phase of the experiment, the volunteers reported to the laboratory at the same
time of the day at weekly intervals on three different occasions (Reilly and
Bambaeichi 2003) in order to become familiar with the procedures and minimise any
learning effects upon the results (Kannus 1994). The volunteer’s position on the
isokinetic dynamometer was recorded and replicated in all subsequent test sessions.
2.2.2. Main investigation
The subjects reported to the laboratory for data collection at six different times
(02:00, 06:00, 10:00, 14:00, 18:00 and 22:00 hours), always on the same day of the
week. There was one test session each day and an interval of 7 days between sessions,
which was sufficient time for a full recovery from previous test sessions (Härmä et al.
1982, Reilly and Down 1986), avoid training effect and also prevented interference
due to changed routines between weekdays and weekends (Folkard and Monk 1980).
The Latin-square cross-sectional design also corrected for any ‘‘order effect’’.
The volunteers reported to the laboratory 1 hour before the test sessions. At the
start of the session, volunteers rested for 30 minutes, awake and in the supine position,
in order to reduce the influence of any previous physical activity. This precaution was
taken since physical activity is an exogenous factor that might mask the endogenous
biological clock (Edwards et al. 2002). During this time, rectal temperature using a
rectal esophageal temperature probe (Steri-Probe/Cincinnati Sub-Zero Products,
Inc.) (Cincinnati, OH; accuracy 0.188C) was measured by a logger (Mini-mitter Co.,
Inc., Bend, OR, USA), with a sampling frequency of one minute. The last five minutes
of the recording were used as a measure of resting core temperature.
The volunteers then carried out 30 seconds of active stretching of the muscle
groups involved in the tests and then warmed up for five minutes on a cycle
ergometer at the low intensity of 85 W. This procedure avoided raising their muscle
and body temperature to an extent that would mask their performance rhythm
(Wyse et al. 1994).
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476
L.G. Araujo et al.
Volunteers were then positioned and stabilised on the isokinetic dynamometer
(Biodex Multi-Joint System 3 Pro; Biodex Medical Systems; Shirley, NY, USA) as
established during the familiarisation studies (see above), aligning their anatomical
axis of articulation with the axis of the equipment. At this time also, the equipment
was calibrated (Keating and Matyas 1996).
During the tests of muscle strength, all measurements were taken from the
dominant limb by means of a computer-controlled isokinetic dynamometer, with
compensation for effects of gravity throughout the whole range of motion.
Mechanical signals were recorded at a sampling frequency of 100 Hz. For each
contraction mode and angular speed, the volunteers performed three sub-maximal
contractions in order to become accustomed to the equipment and exercise
(Kannus 1994). Peak torque (PT), maximum work (MW) and average power (AP)
were measured during three consecutive maximum isokinetic contractions of the
flexor and extensor muscles of the knee muscles at speeds of 1.05 and 4.19 rad s71
over a range of movement of 908. Afterwards, the knee joint was positioned at 608
of flexion, and volunteers were required to exert a maximum voluntary isometric
contraction (MVIC) of the knee extensors for 10 seconds, when the PT was
measured. A visual display of contraction strength was shown on a computer
screen.
Four minutes of rest separated each test. During the contractions, subjects were
asked to cross their arms over their chests. All the measurements were made by the
same researcher to maximise test–retest reliability (Coldwells et al. 1994, Sole et al.
2007). The researcher also gave standardised base instructions (e.g. please give a
maximum effort when I say go) and oral commands to encourage maximum
performance (e.g. come on, come on, push, push) in the controlled temperature of
218C+0.58C (Wilk et al. 1991).
2.3. Data analysis
The software Statistica for Windows was used, and the results are presented as
mean+standard error (SE). Body temperature and muscle strength variables were
investigated by repeated-measures analysis of variance (ANOVA), using one
factor (six times of collection). In cases where there was statistical significance,
Tukey’s post-hoc tests were applied. Single cosinor analysis, setting the value of
tau, the period of the rhythm, to 24 hour, was used to determine rhythm
parameters (Nelson et al. 1979). The method consists of a least-squares regression
analysis to obtain the best estimates of a cosine function of the form:
fðtÞ ¼ Me þ A cos ðwt þ FÞ
where f(t) is the value at time t of the function defined by parameters Me (the
mean level, termed the mesor), A (the amplitude, half the range of oscillation), w
(the angular frequency, degrees per unit time, with 3608 representing a complete
cycle of 24 hours) and F (the time of the maximum of the fitted curve, termed
the acrophase).
The existence of a sinusoidal rhythm with a period of 24 hours was confirmed if
the amplitude of the fitted rhythm was significantly different from zero. In addition,
the mean cosine curve for all subjects (group cosine curve) was estimated. In all
statistical tests, the level of significance was set at 5% (p 0.05).
Biological Rhythm Research
3.
3.1.
477
Results
Rectal temperature
The ANOVA showed a significant effect of time (Table 1). A significant 24-hour
rhythm was observed for Tr (p 50.05) with F at 17:48 hours, Me of 37.08C and A of
0.418C (Table 2 and Figure 1).
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3.2.
Isokinetic muscle strength
The ANOVA showed statistically significant time-of-day effects for all the
variables except average extensor power. Lowest values were nearly always at
06:00 hours and the highest levels generally fell between 14:00 and 18:00 hours
(Table 3). There were significant 24-hour rhythms in maximum concentric
voluntary isokinetic contractions at low speed (1.05 rad s71) for the following
variables: PT of the knee extensors, MW of the knee extensors, MW of the knee
flexors and AP of the knee flexors. The other indices of concentric muscle
performance (extensor AP and flexor PT) at this speed presented highest values in
the afternoon, but the amplitudes of the 24-hour rhythms were not significant
(Table 4 and Figure 2).
With isokinetic knee flexion and extension at 4.19 rad8s71, ANOVA showed a
significant time-of-day effect for all variables except extensor AP and flexor AP of
the knee (Table 5). The post-hoc analyses showed the lowest levels at 06:00 hours
and the highest levels at 18:00 hours. Variables that showed a 24-hour rhythm were
PT of the knee extensors and MW of the knee extensors. The rhythms were not
significant for the other variables measured (extensor AP, flexor PT and flexor AP)
(Table 6 and Figure 3).
3.3. Isometric muscle strength
For the MVIC of the knee extensors until exhaustion, neither ANOVA not cosinor
analysis showed a significant time-of-day effect for PT. However, PT showed a trend
towards significant variability during the 24 hours (p ¼ 0.057), with the highest value
occurring at 18:00 hours (Tables 7 and 8).
4. Discussion
The most important findings from the present study are as follows: (1) 24-hour
rhythmicity was detected at both low and high speeds of movement, but it was more
evident at slow speed; (2) the variable that presented the lowest sensitivity to
variation along the 24 hours was AP and (3) variations with a period of 24 hours
were not observed for all modes of muscle contraction and speeds with concentric
movement.
4.1. Temperature and the sample of volunteers
The results obtained from rectal temperature – chosen because it is considered one of
the main markers of endogenous circadian rhythms – are in line with results
presented in the literature (see Waterhouse et al. 2005, for example). Moreover, the
cosinor parameters observed in our study (F ¼ 17:48 hours, Me ¼ 37.08C and
Tr (8C)
Table 1.
36.78+0.01
02:00 hours
36.58+0.01
06:00 hours
36.79+0.01
10:00 hours
Variation of temperature with time of day (mean+SE).
37.22+0.01
14:00 hours
37.41+0.01
18:00 hours
37.18+0.01
22:00 hours
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1291
F
50.005
p
478
L.G. Araujo et al.
Biological Rhythm Research
Table 2.
479
Parameters of the 24-hour rhythm of rectal temperature (n¼8) (mean+SE or CI).
Variable
Mesor
(SE)
Amplitude
(CI)
Amplitude %
mesor (CI)
Acrophase
hour:
minute (CI)
Significance
(population
cosine curve)
Tr (8C)
37.0 (0.13)
0.41 (0.35–0.77)
1.1 (0.9–2.0)
17:48 (16:07–21:36)
50.05
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Note: Tr¼rectal temperature; CI¼95% confidence interval.
Figure 1. Measured 24-hour rhythm of rectal temperature (Tr) with best-fitting sinusoid
superimposed. Values are mean+SE.
A ¼ 0.418C) were very close to those obtained by Giacomoni et al. (2005) in a male
population (F ¼ 17:29 hours, Me ¼ 37.08C and A ¼ 0.288C).
This result supports the view that our volunteers in the present study exhibited a
typical diurnal pattern of body temperature, as can the conditions under which the
baseline measurements of core temperature were made. This is an important finding
because of our over-riding concern regarding the conditions of measurement and
choice of the volunteers, as well as the controversy that exists in the literature due to
overlooking standardisation procedures that are essential in such studies.
4.2. Rhythms of physical performance: standardisation of volunteers and conditions
Up to the present time, only a few studies have analysed the strength of maximum
contraction under isokinetic conditions, and these have yielded conflicting results.
Wyse et al. (1994) and Atkinson et al. (1994) detected a clear diurnal variation in the
torque produced by extension and flexion of the knees during concentric
contractions, both studies finding maximum values between 18:00 and 20:00 hours.
However, this movement was analysed at only a few times within a period of 24
hours, not enough to establish the details of such a rhythm in any detail. Cabri et al.
(1988) did measure the variable more frequently but did not identify statistically
significant variations in the muscle function over the course of the day; however, they
did observe that the differences of torque and level of fatigue were greater in
concentric than eccentric movements. They also detected more pronounced
199.2+20.7
208.7+20.3
131.9+13.9
109.9+6.0
129.2+10.3
82.1+4.7
06:00 hours
223.3+15.4
233.3+14.0
138.5+9.8
117.7+5.7
149.0+9.1
86.6+4.8
10:00 hours
229.4+17.6
236.7+14.6
143.6+10.6
123.0+7.1
152.4+9.3
91.7+5.0
14:00 hours
Note: Ext¼extensor; Flex¼flexor; PT¼peak torque; Max Work¼maximum work; Av Pow¼average power.
218.7+14.3
222.7+13.6
135.8+10.9
111.0+5.9
137.9+7.7
82.0+3.7
02:00 hours
Variation of isokinetic muscle strength at 1.05 rad 8s71 with time of day (mean+SE).
PT Ext (N8 m)
Max Work Ext (J)
Av Pow Ext (W)
PT Flex (N8 m)
Max Work Flex (J)
Av Pow Flex (W)
Table 3.
229.8+15.0
240.3+13.4
143.9+11.3
116.8+7.0
145.9+8.8
87.6+5.6
18:00 hours
226.6+14.6
234.9+12.0
144.9+11.2
116.7+5.2
147.6+7.6
84.3+4.4
22:00 hours
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5.94
4.72
1.79
4.5
5.5
3.94
F
50.005
50.005
0.13
50.005
50.005
50.005
p
480
L.G. Araujo et al.
Biological Rhythm Research
481
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Table 4. Parameters of the 24-hour rhythm of the variables of isokinetic contraction in knee
flexors and extensors at 1.05 rad s71 (n¼8) (mean+SE or CI).
Amplitude
(CI)
Amplitude %
mesor (CI)
Acrophase
hour:minute
(CI)
Population
cosine curve
Variable
Mesor (SE)
PT Ext
(N8 m)
Max Work
Ext (J)
Max Work
Flex (J)
Av Pow
Flex (W)
221.1 (44.7) 12.0 (8.5–15.5) 5.4 (3.8–7.0)
17:18 (12:18–18:54)
50.01
229.3 (39.8) 12.4 (2.9–21.9) 5.4 (1.2–9.5)
16:54 (11:42–19:30)
50.01
143.9 (23.2)
15:36 (11:48–19:24)
50.05
14:04 (10:8–16:28)
50.01
85.4 (12.2)
8.6 (0.7–16.6)) 5.6 (0.4–11.5)
5.5 (2.1–9.0)
6.4 (2.4–10.5)
Note: Ext¼extensor; Flex¼flexor; PT¼peak torque; Max Work¼maximum work; Av Pow¼mean power;
CI¼95% confidence interval.
differences at high speeds. In more recent studies, Deschenes et al. (1998) observed
that the variables regarding maximum concentric muscle performance of the knee
movement, with the exception of fatigue, only demonstrated a 24-hour rhythm at
high speeds, while Gauthier et al. (2001) reported similar diurnal variations of the
concentric elbow flexion at both low and high speeds and observed the same
variations for isometric contractions.
There are several possible reasons for such disparities, and these are related to
different conditions of measurement. Some of these conditions will now be
considered with regard to the present and previous studies. It is accepted that
some of the precautions that we discuss below might have been taken in the studies
that are cited, even though no mention appears in the published manuscript. It is our
suggestion that, in future, such details be included.
(1) External factors: Even though events that take place regularly are
synchronisers of the endogenous time in living creatures (zeitgebers), they
also have a direct (masking) effect upon the measured rhythm, as a result of
which the timing of the endogenous oscillator is obscured (Minors and
Waterhouse 1981). Therefore, when the possible presence of 24-hour rhythm
in a given variable is sought, these influences must be strictly controlled.
These influences include the environmental conditions as well as ensuring
that the volunteers are in a true ‘‘baseline’’ condition.
(2) Sleep deprivation: Sleep deprivation might temporarily change performance
patterns. Studies have shown that one night of sleep deprivation does not
worsen muscle strength, but that two nights of sleep deprivation do cause
deterioration (Meney et al. 1998, Goh et al. 2001, Bambaeichi et al. 2005).
Therefore, we standardised sleep before the experiments and in the night
before the test sessions and also ensured that the volunteers remained awake
before the test at 02:00 hours, thus preventing sleep inertia (Atkinson and
Reilly 1996). Additionally, excessive sleepiness and trans-meridian travel in
the 10 days prior to the beginning of the experiment were exclusion criteria
(Reilly and Edwards 2007). Among the five previous studies on the effect of
time of day on parameters of muscle strength (Cabri et al. 1988, Wyse et al.
L.G. Araujo et al.
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482
Figure 2. Twenty-four-hour rhythms of isokinetic muscle strength at 1.05 rad s71 with bestfitting sinusoids superimposed. Values are mean+SE.
145.1+9.1
161.8 +13.5
279.7 +30.8
110.3+6.1
106.6+8.5
174.4 +19.6
06:00 hours
153.5+6.7
172.0 +11.0
293.4 +21.3
117.4+6.3
115.9+8.1
183.8 +22.0
10:00 hours
152.1+8.1
171.6+12.1
294.3 +25.0
119.1+5.5
118.2+6.6
189.3 +16.0
14:00 hours
Note: Ext¼extensor; Flex¼flexor; PT¼peak torque; Max Work¼maximum work; Av Pow¼average power.
150.4+8.1
167.8 +11.6
295.6 +24.8
117.9+5.6
114.9+6.8
186.8 +19.3
02:00 hours
Variation of isokinetic muscle strength at 4.19 rad8s71 with time of day (mean+SE).
PT Ext (N8 m)
Max Work Ext (J)
Av Pow Ext (W)
PT Flex (N8 m)
Max Work Flex (J)
Av Pow Flex (W)
Table 5.
156.7+8.0
177.9 +11.0
300.9 +32.8
120.4+4.9
116.4+7.6
179.2 +12.9
18:00 hours
152.3+7.9
172.4 +11.8
308.7 +29.4
114.5+5.9
112.7+6.7
187.7 +17.9
22:00 hours
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3.10
4.7
1.27
3.65
2.53
0.66
F
0.02
50.005
0.29
50.005
0.04
0.65
p
Biological Rhythm Research
483
484
L.G. Araujo et al.
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1994, Deschenes et al. 1998, Gauthier et al. 2001, Giacomoni et al. 2005),
only that of Giacomoni et al. (2005) appeared to adopt sleep alteration as an
exclusion criterion. None of the studies appeared to standardise sleep in the
night before the test.
(3) Warm-up and physical activity: Physical exercise raises core and muscle
temperatures, and so masks the endogenous component of the rhythm in, for
example, muscle strength (Edwards et al. 2002). Also, resistance exercise
Table 6. Parameters of the 24-hour rhythms of isokinetic contraction in knee flexors and
extensors at 4.19 rad s71 (n¼8) (mean+SE or CI).
Variable
Mesor (SE)
Amplitude
(CI)
Amplitude %
mesor (CI)
Acrophase
hour:minute (CI)
Population
cosine curve
PT Ext
(N8 m)
Max Work
Ext (J)
151.6 (22.1)
3.7 (0.5–6.9)
3.0 (0.3–4.5)
17:06 (10:36–19:36)
p 50.05
170.5 (33.3)
5.5 (2.1–9.0)
3.2 (1.2–5.2)
17:30 (12:48–19:24)
p 50.005
Note: Ext¼extensor; PT¼peak torque; Max Work¼maximum work; CI¼95% confidence interval.
Figure 3. Twenty-four-hour rhythms of isokinetic muscle strength at 4.19 rad s71 with bestfitting sinusoids superimposed. Values are mean+SE.
Biological Rhythm Research
485
Table 7. Variable of the maximal isometric contraction in knee extensors depending on time
of day (mean+SE).
MVIC PT
(N8 m)
02:00
hours
06:00
hours
10:00
hours
14:00
hours
18:00
hours
22:00
hours
279.6
(22.3)
268.7
(20.2)
277.5
(20.9)
292.0
(15.8)
294.9
(18.9)
287.4
(18.4)
F
p
2.39
0.057
Downloaded by [Bireme Base de Dados], [Mr Sergio Tufik] at 09:58 21 November 2011
Note: PT¼peak torque.
Table 8. Parameters of the 24-hour rhythm of maximal isometric contraction in knee
extensors (n¼8) (mean).
Variable
Mesor
Amplitude
Acrophase hour:minute
Population cosine curve
Fatigue PT (N m)
283.5
11.7
17:42
p 4 0.05
Note: PT¼peak torque.
increases the levels of circulating catecholamines; this rise affects cardiovascular variables, making it impossible to detect an endogenous rhythm in
cardiac frequency and oxygen uptake after a long period of exercise or after
strenuous exercise (Kraemer et al. 1987). Consequently, the volunteers in the
current study were prohibited from exercise during the experiment and
remained at rest for 30 minutes before the beginning of the data collection.
This minimised the influence of previous physical activity on the rhythm of
core temperature. With regard to physical exercise within the 24 hours before
a test session, Wyse et al. (1994) and Gauthier et al. (2001) appeared not to
impose this condition, whereas Cabri (1988) and Wyse et al. (1994) appear
not to have required rest immediately before the periods of data collection.
The warm-up might also raise muscle and core temperature if it is not
performed at a low intensity; a low-intensity warm-up was incorporated into
our study. Gauthier et al. (2001) and Cabri (1988) do not seem to have
considered this aspect of the protocol.
(4) Dietary intake and ambient conditions: Some researchers believe that digestion
might change thermogenic control through an increase in the metabolism and
that, on the other hand, fasting for a long period before exercise might affect
performance (Douglas 2002, Reilly and Bambaeichi 2003). Room temperature might also affect control of core temperature and mask the endogenous
rhythm (Racinais et al. 2004). Care about a standardised diet was taken by all
researchers except Wyse et al. (1994); the precaution regarding temperature
of the laboratory appears largely to have been ignored by Wyse et al. (1994),
Deschenes et al. (1998) and Giacomoni et al. (2005). The present study was
carried out in the same season, the winter time, as a further guard against
changes in environmental temperature; this precaution appears to have been
observed only in the studies of Gauthier et al. (2001) and Giacomoni et al.
(2005).
(5) Familiarisation and fatigue: Our study was carefully designed to minimise the
effects of learning and fatigue (sessions at weekly intervals and in a Latinsquare design to remove ‘‘order effects’’). In addition, great care was taken to
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486
L.G. Araujo et al.
ensure complete familiarity with the experimental design and apparatus.
Minimising any learning effects maximises the possibility of detecting
rhythmic changes. Gauthier et al. (2001) appear not to have incorporated
this learning phase into their protocols at all; Wyse et al. (1994) had only one
familiarisation session, and Cabri (1988) did not describe the number of
familiarisation sessions. In addition, Cabri (1988), Deschenes et al. (1998)
and Giacomoni et al. (2005) did not report that volunteers performed
contractions before each test in order to become accustomed to the
equipment and exercise (Kannus 1994). The Latin square transverse design
was not present in any previous study reviewed here.
(6) Standardisation and calibration of equipment and advice to volunteers: Studies
have shown inconsistent use of techniques to correct measured torque for
effects of the weight of the limb and gravity. Gravitational forces need to be
added to results for knee flexion and subtracted from those for knee
extension. Failure to use such corrections will decrease the reliability of the
results. Cabri (1988) seems not to have standardised use of the isokinetic
equipment with regard to the exact positioning of the volunteer on the
apparatus. Moreover, in the present study, the volunteers received
standardised oral commands that were given by the same experimenter and
under the same experimental circumstances (Wilk et al. 1991); such
standardisation appears to be new to this field of study.
(7) Frequency of data collection: One of the important aspects in the use of the
cosinor analysis is the frequency of data collection. At least six points are
required to enable reliable results to be obtained from cosinor analysis (Reilly
and Bambaeichi 2003), but this did not occur in the studies of Wyse et al.
(1994) and Deschenes et al. (1998), two studies which used ANOVA to
establish time-of-day effects but were precluded by lack of data points from
cosinor analysis. In the present study, six equi-spaced time points were used.
(8) Choice of subjects: The conflicting results in the studies are also due to interindividual differences between subjects, including chronotype, gender,
familiarisation and level of physical training (Reilly and Bambaeichi 2003).
Chronotype was the criterion not considered in the studies of Cabri (1988),
Wyse et al. (1994) and Deschenes et al. (1998).
Given these sources of possible error, it becomes relevant to evaluate previous
studies of the chronobiology of isokinetic muscle strength and to compare them with
the present study in which all precautions and standardisations have been observed
in an attempt to remove as much variation as possible and thus guarantee the
accuracy and reliability of the results.
4.3.
Muscle strength
4.3.1. Muscle group and speed
The data from the present study show that there were greater 24-hour changes at
slow (rather than rapid) speeds of contraction and in extensor (rather than flexor)
movements. This last aspect is in agreement with the literature, which reports greater
24-hour variations in the knee extensor than flexor muscle group in a sample of
males (Deschenes et al. 1998, Wyse et al. 2004, Giacomoni et al. 2005). However,
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Biological Rhythm Research
487
such variation has been observed more often at a low speed of isokinetic movement
and in the flexors when females have been studied (Giacomoni and Garnet 2002,
Giacomoni et al. 2005). Contributory factors to these differences between knee
flexors and extensors might be that transverse sections of knee extensors comprise
twice the area of knee flexors, and their insertion onto the bone is further from the
knee joint (Smith et al. 1997). Gauthier et al. (1996) proposed that the higher the
muscular mass, the more marked was the measured rhythm; Atkinson et al. (1994)
supported this idea, stating that the higher the muscular mass, the higher the
amplitude of the rhythm. Such views would explain why the rhythm amplitude is
higher in males and why it can be easier to demonstrate rhythms in males than in
females.
Much controversy exists regarding the 24-hour variation of speed of movement.
Some researchers (for example, Deschenes et al. 1998, Bambaeichi et al. 2004,
Giacomoni et al. 2005) suggest that the variation is speed-dependent. The findings of
the present study lead us to disagree with that statement, 24-hour variation having
been found by us at both speeds of movement. Our results corroborate those of
Wyse et al. (1994), who found variation with time of day at both low and high speeds
of movement and in both extension and flexion of the knee during concentric
contractions. Nevertheless, this last group did not evaluate performance at a
sufficient number of times to enable a description of 24-hour rhythmicity.
Giacomoni et al. (2005) found rhythmicity in peak extensor torque of male
volunteers only at the high speed of isokinetic movement. Cabri et al. (1988) did
not find 24-hour rhythmicity, but the differences were more pronounced at the high
speed and in the concentric movement when compared with the eccentric one. In
addition, Deschenes et al. (1998) observed time-of-day oscillations only in knee
extension at a high speed and found no significant rhythms in either extension or
flexion at a low speed. Our data corroborate the findings of Gauthier et al. (2001),
who detected torque rhythmicity during elbow flexion at all speeds analysed, which
suggests that the physical human performance is controlled independently of the
speed of movement.
One explanation of all this variability in results is that many physiological
processes change with time of the day and that these processes all contribute to
maximum muscular performance. These physiological processes include central
factors (command of the central nervous system, alertness, and motivation) and
peripheral factors (contractibility), and these might be influenced by hormonal, ionic
and temperature variations (Birch and Reilly 2002). All these processes are involved
in neuro-motor control during the production of muscle strength, independent of the
speed of movement or the muscle group involved. Therefore, it can be hypothesised
that variations in muscle performance will vary during the day in a manner that
depends upon the type of exercise. However, such a hypothesis requires further
experimental testing.
4.3.2. Warm-up masking effect
The present study did not detect 24-hour rhythms in isometric exercise, and this
absence of rhythmicity is in spite of the fact that rhythms are found in metabolic,
ergogenic and vasomotor functions, all of which contribute to muscle performance.
The performance of two isokinetic tests before the isometric test might have induced
an additional effect of muscle warm-up, increasing muscle temperature and masking
488
L.G. Araujo et al.
any time-of-day effect. This possibility is in agreement with the findings of Reilly
and Down (1992), who failed to detect 24-hour variation in the Wingate test
performed after two anaerobic muscle tests. Giacomoni et al. (2005) found
significant a 24-hour rhythm only when electrical twitches were superimposed due
to the motivation to make the maximum effort. Further work is required to test
these issues.
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4.3.3.
Torque, power and work
Our study assessed whether the rhythmicity of PT was similar for MW and AP, as
well as whether it varied with speed of movement. Muscle torque differs from other
components of physical performance, which are related more closely to speed
(Wilmore and Costill 1994). As far as we are aware, only Deschenes et al. (1998)
analysed changes in isokinetic variables other than PT and muscle fatigue over the
course of the day. PT is believed to be the most precise and reproducible marker of
isokinetic muscle function (Kannus 1994), and this might be the reason why
chronobiology studies are limited to the assessment of PT. However, the reliability,
validation and reproducibility of the variables measured by the isokinetic
dynamometer (power and work, for instance) have been clearly established
(Piencivero et al. 1997, Patterson and Spivey 1992) and should be emphasised in
further studies.
Deschenes et al. (1998), investigating a single repetition (PT), found time-of-day
effects on maximal work by knee extensors solely at higher velocities of movement. A
similar result was found with AP of the extensors at the highest speed. Our results
showed rhythmicity in more variables than in Deschenes et al.’s group – including
MW at both slow and fast speeds of movement as well as with extensor and flexor
muscle groups. The AP showed statistically significant effects of time of day only
with flexion at the slow velocity. From these results, we suggest that it is easier to
detect 24-hour rhythms in maximal performance, as in PT and maximal work, than
in average performance (AP, for example).
5.
Conclusion
In conclusion, the present study showed a significant 24-hour rhythm in slow and
fast speeds of movement of knee extensors and flexors, but the rhythms were most
marked for knee extensors at the slow speed. Comparing these results with those
from the literature stresses the importance of methodological issues to guarantee the
reliability of results in studies of human performance rhythms. If these precautions
are met by using a standardised protocol, then several components muscle strength
show rhythmicity with a period of 24 hours. There is also the implication that more
details of the precautions taken need to be reported.
Understanding rhythmic organisation of the motor system is highly relevant,
since the system is widely involved in the control of simple tasks, such as the
activities of daily living (ADLs), and in more complex movements, as in sports
activities. Knowledge of the time of day when best performance can be obtained
(including components of muscle strength, speed, power and coordination) has
implications for work and daily activities as well as for preparing programmes of
physical training and rehabilitation. Using a sound methodological design is an
important component of studies designed to obtain such knowledge.
Biological Rhythm Research
489
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References
Akerstedt T, Gillberg M. 1990. Subjective and objective sleepiness in the active individual. Int
J Neurosci. 52(1–20):29–37.
Atkinson G, Coldwells A, Reilly T, Waterhouse J. 1994. The influence of age on diurnal
variations in competitive cycling performances. J Sports Sci. 12:127–128.
Atkinson G, Reilly T. 1996. Circadian variation in sports performance [Review]. Sports Med.
21(4):292–312.
Baecke JA, Burema J, Frijters JE. 1982. Short questionnaire for the measurement of habitual
physical activity in epidemiological studies. Am J Clin Nutr. 36(5):936–942.
Bambaeichi E, Reilly T, Cable NT, Giacomoni M. 2004. The isolated and combined effects of
menstrual cycle phase and time-of-day on muscle strength of eumenorrheic females.
Chronobiol Int. 21(4–5):645–660.
Bambaeichi E, Reilly T, Cable NT, Giacomoni M. 2005. Influence of time of day and
partial sleep loss on muscle strength in eumenorrheic females. Ergonomics. 48(11–14):
1499–1511.
Birch K, Reilly T. 2002. The diurnal rhythm in isometric muscular performance differs with
eumenorrheic menstrual cycle phase. Chronobiol Int. 19(4):731–742.
Cabri J, De Witte B, Clarys JP, Reilly T, Strass D. 1988. Circadian variation in blood pressure
responses to muscular exercise. Ergonomics. 31(11):1559–1565.
Callard D, Davenne D, Gauthier A, Lagarde D. 2000. Circadian rhythms in human muscular
efficiency: continuous physical exercise versus continuous rest. A crossover study.
Chronobiol Int. 17(5):693–704.
Coldwells A, Atkinson G, Reilly T. 1994. Sources of variation in back and leg dynamometry.
Ergonomics. 37(1):79–86.
Deschenes MR, Kraemer WJ, Bush JA, Doughty TA, Kim D, Mullen KM, Ramsey K. 1998.
Biorhythmic influences on functional capacity of human muscle and physiological
responses. Med Sci Sports Exerc. 30(9):1399–1407.
Douglas CR. 2002. Tratado de fisiologia aplicada à nutrição. São Paulo: Robe Editorial. p. 76.
Edwards B, Waterhouse J, Reilly T, Atkinson G. 2002. A comparison of the suitabilities of
rectal, gut, and insulated axilla temperatures for measurement of the circadian rhythm of
core temperature in field studies. Chronobiol Int. 19(3):579–597.
Folkard S, Monk TH. 1980. Circadian rhythms in human memory. Br J Psychol. 71:295–307.
Gauthier A, Davenne D, Martin A, Cometti G, Van Hoecke J. 1996. Diurnal rhythm of the
muscular performance of elbow flexors during isometric contractions. Chronobiol Int.
13(2):135–146.
Gauthier A, Davenne D, Martin A, Van Hoecke J. 2001. Time of day effects on isometric and
isokinetic torque developed during elbow flexion in humans. Eur J Appl Physiol. 84(3):
249–252.
Giacomoni M, Edwards B, Bambaeichi E. 2005. Gender differences in the circadian variations
in muscle strength assessed with and without superimposed electrical twitches.
Ergonomics. 48(11–14):1473–1487.
Giacomoni M, Garnet C. 2002. Interaction of time of day and menstrual cycle phase on
muscle function in physically active women. J Sports Sci. 20:36–37.
Goh VH, Tong TY, Lim CL, Low EC, Lee LK. 2001. Effects of one night of sleep deprivation
on hormone profiles and performance efficiency. Mil Med. 166(5):427–431.
Härmä MI, Ilmarinen J, Yletyinen I. 1982. Circadian variation of physiological functions in
physically average and very fit dayworkers. J Hum Ergol (Tokyo). 11(Suppl):33–46.
Horne JA, Östberg O. 1976. A self-assessment questionnaire to determine morningnesseveningness in human circadian rhythms. Int J Chronobiol. 4(2):97–110.
Johns MW. 1991. A new method for measuring daytime sleepiness: the Epworth sleepiness
scale. Sleep. 14(6):540–545.
Kannus P. 1994. Isokinetic evaluation of muscular performance: implications for muscle
testing and rehabilitation. Int J Sports Med. 15(Suppl 11):11–18.
Keating JL, Matyas TA. 1996. The influence of subject and test design on dynamometric
measurements of extremity muscles [Review]. Phys Ther. 76(8):866–889.
Kraemer WJ, Noble BJ, Clark MJ, Culver BW. 1987. Physiologic responses to heavyresistance exercise with very short rest periods. Int J Sports Med. 8(4):247–252.
Downloaded by [Bireme Base de Dados], [Mr Sergio Tufik] at 09:58 21 November 2011
490
L.G. Araujo et al.
Martin A, Carpentier A, Guissard N, Van Hoecke J, Duchateau J. 1999. Effect of time of day
on force variation in a human muscle. Muscle Nerve. 22(10):1380–1387.
Meney I, Waterhouse J, Atkinson G, Reilly T, Davenne D. 1998. The effect of one night’s
sleep deprivation on temperature, mood, and physical performance in subjects with
different amounts of habitual physical activity. Chronobiol Int. 15(4):349–363.
Minors DS, Waterhouse JM. 1981. Circadian rhythms and human. Bristol: Wright PSG.
Nelson W, Tong YL, Lee JK, Halberg F. 1979. Methods for cosinor-rhythmometry.
Chronobiologia. 6(4):305–323.
Patterson LA, Spivey WE. 1992. Validity and reliability of lido active isokinetic system.
J Sports Phys Ther. 15:32–36.
Piencivero DM, Lephard SM, Karunakara RG. 1997. Reliability and precision of isokinetic
strength and muscular endurance for the quadriceps and hamstrings. Int J Sports Med.
18(2):113–117.
Racinais S, Hue O, Blonc S. 2004. Time-of-day effects on anaerobic muscular power in a
moderately warm environment. Chronobiol Int. 21(3):485–495.
Reilly T, Atkinson G, Waterhouse J. 2000. Chronobiology and physical performance. In:
Garret WE, Kirkendall DT, editors. Exercise and sport science. Philadelphia (PA):
Lippincott Williams & Wilkins. p. 351–372.
Reilly T, Bambaeichi E. 2003. Methodological issues in studies of rhythms in human
performance. Biol Rhythm Res. 34(4):321–336.
Reilly T, Down A. 1986. Circadian variation in the standing broad jump. Percept Motor
Skills. 62:830.
Reilly T, Down A. 1992. Investigation of circadian rhythms in anaerobic power and capacity
of the legs. J Sports Med Phys Fitness. 32(4):343–347.
Reilly T, Edwards B. 2007. Altered sleep-wake cycles and physical performance in athletes.
Physiol Behav. 90(2–3):274–284.
Smith LK, Weiss EL, Lehmkuhk LD. 1997. Cinesiologia Clı́nica de Brunnstrom. 5th ed. São
Paulo: Manole.
Sole G, Hamrén J, Milosavljevic S, Nicholson H, Sullivan SJ. 2007. Test-retest reliability of
isokinetic knee extension and flexion. Arch Phys Med Rehabil. 88(5):626–631.
Touitou Y, Portaluppi F, Smolensky MH, Rensing L. 2004. Ethical principles and standards
for the conduct of human and animal biological rhythm research. Chronobiol Int.
21(1):161–170.
Touitou Y, Smolensky MH, Portaluppi F. 2006. Ethics, standards, and procedures of animal
and human chronobiology research. Chronobiol Int. 23(6):1083–1096.
Waterhouse J, Drust B, Weinert D, Edwards B, Gregson W, Atkinson G, Kao S, Aizawa S,
Reilly T. 2005. The circadian rhythm of core temperature: origin and some implications
for exercise performance. Chronobiol Int. 22(2):207–225.
Wilk KE, Arrido CA, Andrews JR. 1991. Standardized isokinetic testing protocol for the
throwing shoulder: the throwers series. Isokinet Exerc Sci. 1:63–71.
Wilmore HJ, Costill DL. 1994. Fisiologia do esporte e do exercı́cio. 2nd ed. Tamboré Barueri:
Manole.
Wyse JP, Mercer TH, Gleeson NP. 1994. Time of day dependence of isokinetic leg strength
and associated interday variability. Br J Sports Med. 28(3):167–170.