Pathologie Biologie 52 (2004) 43–49

www.elsevier.com/locate/patbio

Actualité biologique

Biological markers for the follow-up of athletes

throughout the training season
Les marqueurs biologiques pour
la surveillance des athlètes à l’entraînement
G. Lac *, F. Maso
Laboratoire de Physiologie de la Performance Motrice, Univ. B. Pascal, Bat Biologie B, Les cézeaux, 63177 Aubiere, France
Received 12 December 2002; accepted 20 December 2002

Abstract

During the training season, a state of fatigue known as overtraining may occur, resulting from an excessive load of training, both in volume
and intensity. Even now, difficult to predict the risk of overtraining, although this syndrome has been the subject of numerous studies. A lot of
biological markers have been propounded. Taken alone, none of them have an absolute significance. This paper aims to review these markers,
considering their biological interest, the ease with which they can be measured and the cost, from the simplest (body weight daily recording)
to the most up to date markers (e.g. anti-oxidant status). They are grouped into three categories: non-invasive behavioural and biological
markers, biochemical markers, and hormonal and immunological markers.
© 2003 Elsevier SAS. All rights reserved.

Résumé

Au cours de la saison d’entraînement et de compétition chez le sportif, un état de fatigue nommé surentraînement peut survenir. Il est le
résultat d’une charge excessive d’entraînement, à la fois en volume et en intensité. Malgré que ce syndrome ait fait l’objet de nombreuses
études, il est encore difficile à ce jour de prédire le risque de survenue. Un grand nombre de marqueurs biologiques ont été proposés, mais
aucun d’entre eux pris isolément n’a de signification absolue. Cet article a pour objet de recenser ces principaux marqueurs, en prenant en
compte leur intérêt biologique, la facilité et le coût de la détermination, en allant du plus simple (pesée quotidienne) au plus élaboré (statut
anti-oxydant par exemple). Ces marqueurs sont regroupés en trois catégories : marqueurs comportementaux et biologiques non invasifs,
marqueurs biochimiques et marqueurs hormonaux et immunolmogiques.
© 2003 Elsevier SAS. All rights reserved.

Keywords: Training; Overtraining; Biological markers

Mots clés : Entraînement ; Surentraînement ; Marqueurs biologiques

1. Introduction Overtraining corresponds to a loss of adaptability result-

Training conditions an improvement in performance, but
there is a very narrow line between pre-competitive tapering
off and the syndrome of overtraining.
* Corresponding author.
E-mail address: Gerard.Lac@univ-bpclermont.fr (G. Lac).
© 2003 Elsevier SAS. All rights reserved.
doi:10.1016/S0369-8114(03)00049-X
ing in a well-known symptomatology: a deterioration in
performance, difficulty to train and an absence of motivation,
behavioural disorders (irritability, melancholy), sleeping dis-
orders, difficult recovery, an increased occurrence of muscu-
lar accidents and higher sensitivity to infections. These
symptoms are generally felt by the subject and make it
possible to characterise a case of overtraining by using ques-
44 G. Lac, F. Maso / Pathologie Biologie 52 (2004) 43–49
tionnaires including the above-mentioned symptoms. In ad-
dition to this, the blood constants of a subject suffering from
overtraining will be abnormal. Reviews on this topic are
available [1–6].
The state of optimal form or pre-competitive tapering off
for an athlete corresponds to his maximum performance
capacities, to a state of well-being or even of euphoria, with
an optimal attention. It is a state of maximum adaptation and
is obviously underlain by excellent health. It has now been
admitted that some changes in the biological constants can
also be associated with pre-competitive tapering off. In par-
ticular, the need for the athlete to attain the limits of his
physical capacities can chronically modify some regulation
factors such as the glucocorticoid and sexual hormones [7,8].
It has long been a challenge for sports medicine to propose
reliable markers which would allow the form, or conversely
the tiredness, of an athlete to be detected. This means of
ensuring that the athlete is at the top of his form and that he
does not present a risk of overtraining is fundamental. It must
allow quick adjustment of the training load and, if necessary,
respect of a period of rest if the risk of overtraining occurs.
The need for a regular control of selected variables has
actually been propounded. In addition, this method, which is
currently called the “longitudinal follow-up” of the athlete, is
the best if not the only way of making sure that progresses in
recorded performance are of a “physiological” and not “phar-
macological” nature.
We will try to summarise the tools available for this
follow-up which exist at the present time in this field. We will
specify those for which there are consensus and those which
remain more in the field of research, and to give a possible
hierarchy of the tests to be applied, taking into account the
ease with which they can be done, their cost and reliability.
Table 1
Physiological and behavioural markers (non-invasive)
Biological
interest
Weight control +++
Sleep quality
% Body fat +++
% Lean body mass
Follow-up of fitness and performance +++
Coupled with lactates and blood gas control ++
Nutritional follow-up +++
Autoquestionnaire for well-being, e.g. POMS* +++
Resting heart rate +++
Exercising HR +++
Electrocardiography
Electromyography +++
ECG, EMG spectrum
Blood pressure (at rest and during exercise) ++
Echography, DEXA* (skeleton, body composition) ++
MRI*, MNR* ++
* Profile of mood state (POMS), double X-ray absorption (DEXA), magnetic resonance imagery (MRI), magnetic nuclear resonance (MNR).
2. Biological markers
These are of a physiological, biochemical, hormonal and
immunological nature. The physician may of course request
some microbiological analyses to be sure that the observed
symptoms are not the result of infectious illness. We will not
cover this last case.
All these parameters are summarised in Tables 1–3.
3. Comments of Table 1
The first three items of this table constitute the minimal
base for the follow-up of an athlete. These controls are
generally carried out by the trainers and often by the athletes
themselves. For measurements of body composition, the
skinfold thickness measurement is the simplest and most
reliable. Impedencemetry gives more random results, but
makes it possible to provide an indication about the hydration
state of the subject. The physical tests should be adapted
according to the sporting specialty.
The nutritional follow-up using a 7-d table should be
carried out systematically. These measurements are often
criticised by purists who consider them to be insufficiently
precise for quantitative assessment. In our opinion, the essen-
tial interest of this method is not quantitative (any imbalance
of the energy is easily controllable by regular weighing), but
qualitative. It allows any imbalance of the ration between the
large food groups, minerals and vitamins to be objectified. It
also measures the distribution of food consumption over the
day. So it enables the detection of food skews resulting from
bad habits (overconsumption of fat, underconsumption of
fruit and vegetables, insufficient breakfast, excessive nib-
Practicability (non-invasive methods) References
+++ Daily [9–11]
Autocontrol
+++ Skinfold thickness
Impedencemetry
++ VO2max, VMA, vertical jump (Bosco), short sprints, etc. [12–14]
++
++ During a week using adapted software. Quality assessment of
the diet
+++ At various periods of the sporting season [15–23]
++ Daily, use of cardiofrequencemeter [10,24,25]
++
[26–28]
++ Using adapted software
+ [28,29]
++ Cardiac control (medical care). Already used for high-level [30]
athletes
+/– For research only
 G. Lac, F. Maso / Pathologie Biologie 52 (2004) 43–49 45

Table 2
Biochemical markers (invasive)
Biological Practicability (on blood or urine samples) References
interest
NF – SS* haemoglobin, haematocrit Red blood cells (RBC) volume ++ ++ Blood [1,31,32]
Rheological measures of blood + + [33,34]
Fe, Ferritin, % of transferrine saturation ++ ++ Especially in females [5,35–37]
CK – LDH* + ++ Very great variability if micro-traumatisms
(from 1 to 1000 fold)
Myosin chains (for muscle damages) ++ +–
3-Methylhistidine (muscle damages) – ++ Possible interference with food proteins [5,38]
OH proline (tendon) ++ +–
Pyridinoline (bone) – + Urine
Propeptide C
Myoglobin (muscle)
Albumin, hématie + +
Ionnogram ++ ++ Blood [5,34,39–42]
Glycaemia + ++
Lipidic status ++ ++
NH3, urea, uric acid – ++ [43,44]
Branched chain amino acids (BCAA) ++ +
Glutamine +++ +–
Ca, Mg, P (Zn, Cu, Se) ++ +– Blood [45–50]
Anti-oxidant status
Vitamin status Blood [51]
Numeration formula (NF), sedimentation speed (SS), creatine kinase (CK), lactico-dehydrogenase (LDH).

bling, etc.). It seems to us to be particularly recommended for 4. Comments of Table 2

young athletes to help them set up their own dietary disci-
pline on an objective basis.
The autoquestionnaires (psychological profiling, over-
training questionnaires, etc.) used to determine the states of
form are valuable and probably precious aids for the evalua-
tion of the state of tapering off or overtraining. They consti-
tute an alarm system. Additional biological examinations are
necessary to confirm that there is a risk of overtraining.
Cardiac control is used very widely in athletes to adjust
the intensity of training. It is the “ad minima” examination of
aptitude to sport and has the advantage of being non-invasive;
the existence of reliable on-field heart rate recorders allows a
continuous recording over long periods (24 h) with computer
analysis of the profile facilitating the exploitation of this tool.
In an overtrained athlete, resting heart rate and blood pres-
sure are elevated, the adaptation of the heart rate to exercise
(e.g. Ruffier-Dickson test) is altered, and there are some
anomalies on the ECG. These modifications constitute good
indicators of fatigue.
More sophisticated tests carried out in the laboratory by
experts in cardiac examination of sportsmen can be useful,
like ECG spectral analysis [26,29], echocardiography and
Doppler [27].
The analysis of the whole body composition, including the
skeleton (bone mineral density (BMD) and bone mineral
content (BMC)), with an up to date non-invasive method
(double X-ray absorpsiometry or DEXA, magnetic reso-
nance imagery (MRI) and magnetic nuclear resonance
(MNR)) is possible [30], but these very expensive tools are
primarily reserved for hospitalised patients. In sports medi-
cine, they are mainly reserved for the research field.
These examinations are made on the biological liquids;
generally on blood, urine, and even in saliva. The muscular
biopsies are reserved for research or for pathology. In this
category, we find the markers of blood constants, muscular
damage and the various metabolisms. The sedimentation test
and leukocytic formula provide information about the pos-
sible existence of an infectious state. The haematocrit and
blood cell count tell us about the transport capacity of gases
by blood (and about possible illicit practices). These prelimi-
nary blood examinations are relatively cheap and valuable
for an initial appreciation of the general level of health. In the
event of real asthenia and of suspicion of anaemia, the mea-
surement of the haemoglobin level and globular volume, plus
the levels of iron, ferritin and percentage of saturation of the
transferrine will complete the examination [32]. The iron
level alone is not a sufficient indicator [5]. The occurrence of
anaemia is higher in women, but can also occur in men as a
result of a restrictive and/or poorly balanced diet. Although
there is no real consensus on the occurrence of hyposider-
emia (almost systematic in the sportsman) and its effect on
performance, one should compensate by adopting the prin-
ciple of precaution.
Muscular damage is a systematic consequence of physical
exercise, but is amplified in the case of overtraining. Mea-
surements of the levels of creatine kinase (CK) and lactico-
dehydrogenase (LDH) are simple to carry out and not very
expensive. The validity of this indicator is limited by the fact
that traumatisms may multiply the CK values by a factor of a
hundred [37]. The urinary myoglobin reflects severe muscu-
lar constraints. It can reveal the existence of a rhabdomyoly-
46 G. Lac, F. Maso / Pathologie Biologie 52 (2004) 43–49
sis, particularly in veterans. For 3-methylhistidine (marker of
muscle catabolism) and hydroxy proline (marker for the
tendon), the problem is even more complicated because pro-
teins contained in meat consumed may interfere with these
levels [5]. Finally, the measurement of the release of myosin
chains in plasma is expensive and complicated and thus
remains reserved for research [33]. Taking into account these
complications, one can easily understand that by default, the
best indicator remains the CK, but that high values of this
must be interpreted with prudence and that this indicator
must be associated with others to give a valid interpretation.
Urinary DPD (dihydroxy pyridinoline) is an indicator of
osseous resorption whereas osteocalcine and the collagen
propeptides C and N are markers of accretion [38]. The
measurement of these compounds provides an indication of
osseous remodelling and can provide a supplement to infor-
mation obtained on the BMD by imagery (see above). These
measurements are still reserved for the field of research.
Albuminurie and haematurie can occur after tests of ultra
endurance and are the result of a renal inflammation. Control
is simple, and recovery to the normal state must be checked.
The following items are related to general metabolism.
Ionnogram and glycaemia measurements are simple to per-
form and analysis is currently automated. An imbalance in
the K/Na ratio may appear after physical effort, but generally
returns quickly to normal. The overtrained subject presents a
tendency towards hypoglycaemia.
The lipid assessment must be carried out in order to detect a
possible family dyslipidemia, whose occurrence in sportsmen
is identical to that seen in people in general. The lipid assess-
ments practised in sportsmen have systematically made it
possible to highlight an improvement in lipid status (or a
reduction in cardiovascular risk) with, in particular, a rise in
the high density lipoprotein (HDL) fraction (with a correlative
rise in its apoprotein A1) and a reduction in the low density
lipoprotein (LDL) cholesterol [39,41,42]. These modifica-
tions are thus representative of a good level of “fitness”.
Ammonia (NH3), urea and uric acid [5] are compounds
resulting from nitrogen metabolism, but they do not have the
same significance. Ammonia and urea are representative of
the metabolism of proteins, mainly of food origin (thus in
relation to diet composition), and also of muscular origin.
Basal levels are amplified by long exercise when neogluco-
genesis starts. Ammonia dosage is difficult to do and is
mainly used in research. Uric acid levels are increased by
short intense exercise (xanthine pathway). Urea and uric acid
are both toxic compounds (uric acid role is implicit in ten-
dinitis) and their urinary elimination is directly correlated
with diuresis. Weak diuresis is thus the first cause of high
levels. The sportsman must rehydrate himself sufficiently,
not only to compensate for losses due to sweating, but also to
ensure sufficient diuresis, which is especially important since
an athlete produces more urea than a sedentary person. High
urea levels of a chronic nature constitute an indication of
overtraining, but we think that it must be associated with
other markers before being used to signal this condition.
Physical exercise increases the catabolism of proteins and
thus the release of amino acids. They are consumed for
energy production, in particular the branched amino acids
(valin, leucine and isoleucine) which lower their concentra-
tion in blood and muscle. A supplement [40] in these compo-
nents appeared to be beneficial for tests of endurance.
Glutamine is a particular amino acid that is used as a donor
of ammonium ions for urea renal excretion (ammonia amino
acid-givers). So the catabolic phenomena that accompany
muscle exercise increase the production of ammonia and
cause a reduction in glutamine levels, with a cumulative effect.
Overtraining indicates a significant chronic fall in the levels of
this compound and constitutes an interesting marker of this
syndrome. In addition, glutamine is essential for the immune
system functionality, which explains immune deficiencies
(with increased occurrence of infectious episodes) during
overtraining. A supplement of glutamine in the diet makes it
possible to limit this risk. It would appear that this compound
is a good marker of overtraining but unfortunately it is difficult
to assess (for review see [43]). Recently, Rowbottom et al.
[44] have shown that elevated glutamine levels might be
associated with well-trained states in male triathletes.
Calcium, magnesium and phosphorus are implicated in
various metabolisms related to performance. Ca and P are the
elements of the bone capital, but along with Mg, are also
implicit in cellular excitability; in situations of tiredness and
stress, the calci-magnesic deficit can lead to bouts of spasmo-
philia. Some data associate Mg with force; in the same
manner, P would improve the aerobic performance [46].
Systemic dosages are not very indicative (although these
values can be easily obtained with the ionnogram) since the
bone content is huge and is in balance with the plasmatic pool
under hormonal control. What is fundamental for these three
elements is to make sure that the daily ration is sufficient.
The oligo-elements, Zn, Cu and Se, have also been the
subject of investigations in sportsmen. These metals are co-
factors of anti-oxidant enzymes which playa fundamental
role in sportsmen on account of an increased production of
free radicals [48,49]. Generally, the anti-oxidant potential is
increased by training, so, the best way to evaluate the oxida-
tive stress is to determine the balance between the free radical
levels and the anti-oxidant potential [48,49]. A drop of this
ratio will correspond to a possible state of overtraining. With
respect to the vitamins [51], A, C and E have anti-oxidant
properties and are thus concerned with sporting activity, but
theydo not present a particular risk of deficit. Vitamin D3 is
involved in the phospho-calcic metabolism and its rate must
be supervised in athletes, especially those little exposed to
the sun (indoor sportsmen). Deficits in B1 and B6 can occur
in sportsmen. Athletes concerned by weight control and low
diet consumption need to be checked for their vitamin as well
as mineral levels. Thus, branched amino acids, glutamine,
minerals and vitamins can be supplemented, on the condition
that this is done reasonably under medical control in order to
avoid the risk of overdosing.
 G. Lac, F. Maso / Pathologie Biologie 52 (2004) 43–49
Table 3
Hormonal and immunological markers
Biological interest
Cortisol (reflection of stress) +++
Testosterone +++
DHEA* (female) +++
Osteocalcine ++
GH* + +
IGF1* ++
IGF1 BP1 and BP3* ++
Epinephrine ++
Norepinephrine
Ig total* ++
Salivary sIgA* (upper respiratory tract) ++
Glutamine
C reactive protein
* Dehydroepiandrosterone (DHEA), growth hormone (GH), insulin like growth factor I (IGFI) = somatomedine, IGFI binding protein 1 and 3 (IGFI BP1 and
3), immunoglobulin (Ig), secretory immunoglobulin A (sIgA).
5. Comments of Table 3
Hormones are metabolic regulators and are in this way
concerned with sport. It is traditional to find in the literature
the concepts of sympathetic tiredness (the Basedowoid syn-
drome, with increased resting heart rate and basal metabolic
rate, insomnia, etc.) or of parasympathetic tiredness (the
Addisonoid syndrome, with a fall in resting heart rate and
blood pressure, digestive troubles, etc.) in relation to the
increase or conversely, a reduction in the catecholamine
levels [4,62]. It means that overtraining may lead to two
opposite physiological reactions, but some authors consider
that sympathetic reactions are less alarming and even corre-
spond to training improvements. Catecholamines are diffi-
cult to assess and can be used only as additive interpretative
factors in research. Their levels are correlated to the heart
rate, so that continuous recording of the heart rate provides
an indication of which type of tiredness is observed.
With respect to hormonal levels, lot of work during this
last decade has focused on the cortisol responses to exercise
[8,52–54,70–72]. This compound is qualified as the hormone
of “stress” and induces a positive adaptation of the organism:
stimulatory effects of the nervous system, even euphoric
effects, analgesic effects, anti-inflammatory, ergogenic and
also a hyper glycaemic role by neoglucogenesis. The neo-
glucogenesis being carried out from amino acids of the pro-
teic capital explains that this hormone is said to be catabolic.
Due to the constraint resulting from physical exercise, this
hormone presents temporary increased rates following inten-
sive exercises [52,53]. It may also be chronically elevated in
athletes submitted to heavy training loads [2,3,8,54] which
corresponds to a positive adaptation. Beyond a certain
threshold, the negative effects will be able to override the
positive effects with, in particular, asthenia and protein ca-
tabolism. In the situations of chronic tiredness which can
occur in the athlete and which represents the most serious
47
Practicability (blood, urine, saliva) References
+++ Saliva [2,8,31,52–55]
+ Blood
+++ [31,55–58]
+
+++ [59]
+
+ Blood [60]
Blood [2]
+ Blood [33,61]
+
+ Blood
Urine [1,4,10,55,62,63]
+ Control of infectious disease [64–67]
++
Blood [5,68,69]
stage of overtraining, the cortisol levels will drop. It is there-
fore difficult to make an interpretation starting from only one
cortisol assay, since the levels of this hormone vary during
the day (circadian rhythm). On the other hand, it is interest-
ing to follow long-term variations in the same athlete accord-
ing to time and circumstances (training session, competition,
advance of the training season with cumulated tiredness).
This long-term follow-up is now possible thanks in particular
to the possibility of assaying this hormone in saliva, which is
a non-invasive process and which allows the repetition of a
great number of samplings [8,72].
The testosterone levels (male sex hormone) may also be
affected by the practice of high-level sport. This hormone,
apart from its specific effects on the genital apparatus, exerts
a positive effect on the reconstitution of the glycogen stock
and on muscle protein synthesis after long exercise, which
makes this compound an anabolic hormone. However, it has
been shown for a long time that high-level endurance training
in the female athlete causes a blocking of the sexual function
with amenorrhoea. In the same way, more recently, it has
been observed that, in man, intensive endurance training
caused a fall in the testosterone level [56,57]. Conversely, for
athletes practicing strength training, this phenomenon does
not occur and would even be reversed [58]. Recently, we
proposed substituting the adrenal androgen DHEA for test-
osterone in the female for whom testosterone is not a specific
marker [59].
In conclusion, in a large number of sports practise, cortisol
levels are normally elevated and testosterone levels may be
lowered. As a result of this, Adlercreutz et al. [70] proposed
considering the testosterone/cortisol (T/C) ratio as an index,
denoting tapering off when it was slightly lowered, and
overtraining when this ratio fell by more than 30%. Of
course, this rule may be applied only in the long-term
follow-up of an athlete, and not by comparing the level of a
given athlete to a reference value. This index is considered as
48 G. Lac, F. Maso / Pathologie Biologie 52 (2004) 43–49
highly valuable by a number of authors [52,71,73]. However,
one has to consider that such a regular control is rather
expensive and, due to this fact, rarely performed in the
follow-up of sportsmen. It is worth noting that recently, the
International Cyclists Union decided to systematise the long-
term control of cortisol and testosterone, with the aim of
avoiding drug abuse. We think that this control will probably
reward the athletes for managing well both their health and
their sporting season.
The growth hormone (GH) and its relay, the somatome-
dine (IGF1) play a proteosynthetic role at the muscular level.
GH is also associated with a rise in muscular strength. IGF1
is associated with bone growth and calcium accretion in the
adolescent. At present, on account of the pulsatile secretion
of GH which makes its assay not very meaningful, the IGF1
assay is considered as more reliable. Physical exercise en-
hances its production and thus plays a positive role in mus-
cular mass and bone density gain. Recently, it was shown that
the carrier proteins of IGF1 (BP1 and BP3) were also modi-
fied with training: increased in the well-trained and de-
creased in the overtrained [61]. For these compounds, the
only data that exist are in the research field.
One of the well-known consequences of overtraining is an
immunological weakness which becomes evident through an
increased frequency in the occurrence of colds and even
more serious infections. Such infectious episodes result in a
consequential enhancement of staleness. The blood formula
is altered (low leucocytes and rise in lymphocytes). Immuno-
globulins (which the immunological defences depend on) are
lowered during states of fatigue. The general profile of the
whole blood immunoglobulin is affected [66]. To date, im-
munoglobulins are not easy to assay for the follow-up of
training. The possibility of assaying saliva secretory IgA
constitutes a non-invasive possibility [65]. Moreover, the
greater part of infections in athletes concerns the upper res-
piratory tract, which is mainly protected by IgAs, a fact
which reinforces the interest in determining their levels.
It is rather difficult to strengthen the immune defences of a
subject. Ig injections induce a supplementary fatigue which
is undesirable for performance [5]. As quoted above,
glutamine intake may have positive effects. Another strategy
consists of correct vaccination (at least against influenza) and
also by the use of auto vaccination (oral treatment) in autumn
in order to reinforce the immune system.
6. Conclusion
A very large panel of biological tests exists, that has been
propounded for the follow-up of the athlete during the train-
ing season. Taken alone, none of them has absolute signifi-
cance. The physician mayask routinely for tests to confirm
his clinical examination, considering the best compromise
between biological interest, ease and coast. Some of the tests
listed above are still in the research field. Maybe, with tech-
nical progresses, some of them (for instance, anti-oxidant
markers) will become easier to realise and less costly and
will be candidates for overtraining markers.
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