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1 Department of Physiology and
Pharmacology, The effects of eccentric exercise on changes in
numbers of circulating leukocytes, cell activation, cell adhesion, and
cellular memory function were investigated in 12 men, aged 22-35
yr. The immunologic effects of postexercise epidermal treatment with
monochromatic, infrared light were also evaluated. Blood was drawn
before and 6, 24, and 48 h after exercise for phenotyping and analysis
of creatine kinase activity. There was an increase in leukocyte, monocyte, and neutrophil number, no change in the number of basophils, eosinophils, B cells, and T cells, and a decrease in natural killer cell number postexercise. Some markers of lymphocyte and monocyte activation remained unchanged or decreased, whereas the expression of
adhesion molecules 62L and 11b increased on monocytes. It is concluded
that eccentric exercise induced decreased activation, and increased
cell adhesion capacity, of monocytes. Altered trafficking of cells
between lymphoid tissue and blood, selective apoptosis, or
attachment/detachment from the endothelial wall can explain the
observed phenotypic changes. Treatment with monochromatic, infrared
light did not significantly affect any of the investigated variables.
Correlations between immunologic and physiological parameters indicate
a role of the immune system in adaptation to physical exercise.
leukocytes; muscle damage; cell adhesion; cell activation; flow
cytometry
PHYSICAL ACTIVITY and strenuous physical exercise have
been shown to cause significant changes in several immunologic
parameters (23). The causes of these changes have usually been
attributed to changes in hormone (e.g., cortisol and catecholamines)
and cytokine [e.g., interleukin (IL)-1, IL-6] (1, 5) levels in blood and skeletal muscle. It has also been suggested that leakage
or release of muscle cell proteins from human skeletal muscle damaged
by physical exercise can affect the immune system (10), one possible
outcome being increased expression of cell adhesion molecules on
circulating leukocytes (11, 18, 26). Even though there are presently no
data available, the involvement of the immune system in adaptation to
physical training is most likely of vital importance and has also been
previously suggested (26, 28, 33). To investigate the role of the
immune system in (muscular) adaptation to physical stress, it is
necessary to first determine which classes of leukocytes are influenced
by the type of stress under investigation.
The present study investigated a large number of leukocyte subclasses
and the expression of cluster of differentiation (CD) antigens on
leukocytes before and 6, 24, and 48 h after one bout of eccentric-type
walking exercise. Anaerobic exercise performance, postexercise delayed
onset of muscle soreness (DOMS), and plasma creatine kinase (CK)
activity were also determined. The purpose was
1) to investigate which subclasses
of circulating leukocytes are affected by eccentric exercise,
2) to correlate immunologic and
physiological parameters before and after eccentric exercise, and
3) to investigate the effects of
postexercise treatment with 950-nm pulsed, monochromatic light
(Biolight) on circulating leukocytes, DOMS, and exercise performance.
To stress the immune system in vivo, an eccentric exercise model was
used because this type of exercise is known to cause muscle
inflammation (8, 33), increased cell adhesion capacity (11, 26), and
DOMS (6). The effects of eccentric exercise on changes in different
subsets of blood leukocyte numbers, activation, and cell adhesion
capacity have previously been studied in humans (8, 26, 27). However,
these studies and others have focused on only a few cell surface
antigens. To understand the complex changes in the immune system, it is
necessary to analyze a large number of different cell surface
receptors, as well as in vitro cell activity. With respect to the
immune system, the present study was limited to the investigation
of CD receptors on circulating leukocytes. A wide range of CD receptors
was chosen (Tables 1 and
2) to describe changes in cell numbers,
subset distribution, cell activation, and cell adhesion capacity. The
physiological relevance of the observed immunologic changes in blood
after exercise is largely unknown. It has been suggested that the
inflammation-like immune response, such as seen after eccentric
exercise, is necessary for muscular regeneration and adaptation to
physical exercise (26, 33) but also that strenuous physical exercise
can increase the risk for upper respiratory tract infections (20).
Correlations between immunologic and physiological parameters are of
interest both to athletes, possibly as a marker of muscle damage (10), overuse and overtraining, and in the treatment of immunologic disorders
such as myopathies.
ABSTRACT
Top
Abstract
Introduction
Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Methods
Results
Discussion
References
Table 1.
Main phenotypes on leukocytes
Table 2.
Antigens investigated on lymphocytes and monocytes
It is of interest for athletes to reduce recovery time after strenuous exercise, and new methods for this purpose are constantly being developed and evaluated. Findings by Karu et al. (9) indicate that some types of light can affect cellular protein structures. On the basis of these findings, it was hypothesized that postexercise treatment with monochromatic, infrared light (Biolight) could affect the immune system, with one possible outcome being decreased recovery time and reduced DOMS after eccentric exercise. Support for this hypothesis can also be found in a very recent study, which demonstrates that humans in fact possess extraocular photoreceptors (2).
Thus the present study investigated some aspects of the immune system's response to eccentric exercise-induced muscle damage, as well as the correlation between physiological and immunologic variables.
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METHODS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Subjects
Twelve healthy male subjects, mean age 26 yr (range 22-35 yr) and mean body mass 77.4 kg (range 65-92 kg), participated in the study. All subjects exercised on a regular basis, and two subjects were accustomed to eccentric leg exercise (squash and fencing). Omitting these two subjects does not affect the results; thus all subjects are included in the statistical analysis. After receiving oral and written information about the study, subjects signed an informed consent document. The Ethics Committee of the Karolinska Institute approved the study (Dnr 96-263).Testing
At least 2 days before, and 48 h after, eccentric exercise, all subjects performed an anaerobic cycling test as a measurement of anaerobic exercise performance. The test consisted of a light 10-min warm-up, 30-s all-out cycling, 5-min recovery, and 10 × 10-s all-out cycling interspersed with 50-s rest periods (work rate at 7% of total body weight). This anaerobic test does not cause muscle cell damage, measured as increased plasma CK activity (16). The anaerobic tests were performed on an electrically controlled, modified Cardionics Wingate ergometer (Cardionics, Bandhagen, Sweden). The rpm were recorded by computer and later converted to watts. Blood from a fingertip capillary was collected 3 min posttesting on both testing occasions for determination of blood lactate concentration. To evaluate the effects of a new treatment method (Biolight) on recovery and muscle soreness, subjects were pairwise matched (on the basis of their performance in the anaerobic cycling test) and randomly assigned to group A or group B. Subjects were asked not to perform any strenuous or unaccustomed exercise for a period of 2 days before the first cycling test until the second cycling test was completed, which was 48 h after eccentric exercise.Eccentric Exercise
On the morning of the exercise day, the subjects performed a 10-min warm-up on a stationary cycle ergometer; thereafter, they performed 5 × 30 eccentric-type walking steps (15 steps/leg) with a 1-min rest between each set. The type of eccentric exercise used (Borsov steps) will induce severe muscle soreness. The steps are executed by kneeling down with the leading leg at a 90° angle, touching the ground with the knee of the lagging leg, and returning to an upright, standing position.Treatment
The Biolight equipment emits a 400- to 1,200-nm monochromatic, infrared light with the energy of 4 J/cm2. It has been tested by the Swedish National Testing and Research Institute (ref. 95F42266a) and was determined not to have any harmful effects on living tissue. A treatment on the quadriceps and gluteus muscles of 29-min duration was given with either Biolight (950 nm) or an identical placebo machine in a double-blind fashion immediately, 1 h, and 24 h postexercise. The collaborators at Biolight International (Danderyd, Sweden) set treatment mode and time.Venous Blood Samples
Blood samples for analysis of leukocyte numbers and CK activity were drawn from a forearm vein before and 6, 24, and 48 h postexercise. Five milliliters of blood were collected into Vacutainer tubes containing EDTA (Becton-Dickinson) for leukocyte analysis, and 5 ml were collected in untreated Vacutainer tubes for analysis of soluble CD8. CK activity was measured by using a standard laboratory kit (CK MPR2, Boehringer Mannheim). White blood cell count and differentials were estimated with a Coulter STKS hemocytometer (Coulter Electronics). Because cell numbers were determined in whole blood, corrections for changes in plasma volume were not made.Immunophenotyping
Determination of different subsets of leukocytes (Tables 1 and 2) was accomplished by flow cytometry with three-color analyses. The method for three-color flow cytometry has been described in detail (13) and is based on a high degree of standardization. Briefly, the staining was performed on whole blood for 30 min, on ice, followed by erythrocyte lysing with Ortho-mune Lysing Reagent (Johnson & Johnson, Raritan, NJ). The staining panel (Table 3) comprised 10 combinations of monoclonal antibodies conjugated with FITC, phycoerythrin (PE), or peridinin chlorophyll protein (PerCP) all from Becton-Dickinson (Mountain View, CA), with the exception of monoclonal antibody CD45RO-PE (Dakopatts). The samples were analyzed with a daily calibrated FACScan flow cytometer (Becton-Dickinson) by using different microbeads [QC Windows and Quantum 1000 (Flow Cytometry Standards) and CaliBRITE (Becton-Dickinson)], as usually done for quantification of cellular antigens with flow cytometry. Because the fluorescence intensity of the calibration beads was constant and no adjustments were done to compensation circuits, the mean fluorescence intensity can be considered a relevant indicator of the expression of surface CD antigen molecules.
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Correlated data of 12,000 events were acquired with live gate applied on lymphocytes and monocytes. Analysis was performed by using Paint-A-GatePlus software that reports the mean fluorescence intensity of a certain antigen on whole cell populations, or on subsets of these populations identified by three-color analysis (Table 3). Lymphocytes and monocytes were separately gated electronically on a sideward scatter vs. a forward scatter cytogram.
Muscle Soreness
DOMS at rest was estimated before and 24 and 48 h after eccentric exercise by the subjects and was rated by subjects on a 1-10 subject rating scale, similar to the Borg scale, whereby a score of 1 was "no soreness" and 9 was "very, very sore."Statistical Analysis
StatView software (Abacus Concepts, Berkeley, CA) was used for all statistical analysis. Because of the non-Gaussian fluorescence distribution of most CD antigens on lymphocytes of healthy subjects (13), as well as in the sample group (skewness >1.0), nonparametric methods were used. The Friedman test was used for changes over time, the Mann-Whitney test for within-group changes, and the Wilcoxon signed rank test for comparison between groups. Nonparametric methods were also used for analysis of CK and DOMS. Correlations were investigated by Fisher's r-to-z method. To compensate for multiple time points of blood sampling and to minimize the risk for a type 1 error, P < 0.01 was used for between- and within-group comparisons. To compensate for the large number of variables, P < 0.01 was used for the Friedman test.| |
RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Treatment
There was no statistically significant difference between the placebo- and Biolight-treated group regarding any of the analyzed variables at any time. Thus the results from the two groups are combined (Tables 4 and 5).
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Physiological Variables
There was no statistically significant change in exercise performance (in W/kg body mass) in the 30-s cycling test before compared with 48 h after eccentric exercise, but there was an increase in performance in the 10 × 10-s test during the same period (Table 6). DOMS increased significantly from before to 24 and 48 h after eccentric exercise (Table 6). Plasma CK activity did not increase significantly over time, but large interindividual differences were observed (Table 6).
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Immunologic Parameters
Cell number.
After eccentric exercise, and compared with resting values, there was a
statistically significant increase in the total number of circulating
leukocytes, mainly because of increased numbers of neutrophils (73% at
6 h postexercise) and monocytes (39% at 6 h). Even though the number
of lymphocytes did not change compared with resting values, there was a
significant decrease (28% at 6 h) in the percentage of
lymphocytes. There was also a decrease in the number of CD20+CD5+ B
cells (40% at 48 h), memory T-helper cells (CD4+CD45RO+,
change over time, Friedman), and NK cells (CD56+CD16+CD57
CD3; 30% at 6 h) (Fig.
1, Table 4). There were no statistically
significant changes in any other cell populations (Tables 1 and 2)
analyzed in the present study.
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Antigen expression.
The density of some surface CD-antigen molecules also changed (Fig. 1,
Table 5), with a significant increase in expression of CD62L on
CD4CD8 lymphocytes (22% at 24 h), CD62L on monocytes (26% at 24 h), and CD11b on monocytes (change over time). There was a
decreased expression of CD14 on CD45+DR+ (38% at 24 h) and of CD4 on
monocytes (24% at 6 h).
Correlation.
The numbers and percent difference of leukocyte subsets after eccentric
exercise, correlated with anaerobic exercise performance, muscle
soreness, and plasma CK activity are given in Table
7.
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The main findings of this investigation were that brief, eccentric exercise 1) increased the numbers of circulating monocytes and neutrophils; 2) decreased the activation of monocytes; 3) increased the cell adhesion capacity of monocytes; 4) decreased the numbers of NK cells and of CD20+CD5+ B cells in circulation; and 5) did not affect the T-cell population, except for a minor change in T-helper cells with memory function. In addition, correlations between some immunologic and physiological variables were found.
The increase on the 10 × 10-s cycling test from before to after the eccentric exercise was, even though small (+8.3%), still surprising. A previous study that used the same cycling test also showed an increase performance with repeated testing (16). The muscle soreness experienced by the subjects after the eccentric exercise (Table 6) apparently affected their performance less because of the experience and adaptation having performed the test once before. Although the within-group changes were different between the two groups (Tables 4 and 5), statistical analyses could not demonstrate that treatment with Biolight significantly affected the postexercise changes in the immunologic and physiological variables investigated in the present study. Because it is unknown exactly which receptors could be affected by extraoccular treatment with monochromatic light, and because of the large deviation in the measured CD-receptor number and expression, subtle changes due to the Biolight may not be detected.
It has been suggested that one consequence of eccentric exercise is muscle inflammation (8, 28, 30, 33) and that the immune system is involved in the muscle-repair process after exercise-induced muscle injury (4, 28, 33). Because the inflammatory response is a complex series of events, involving cell signaling, activation, adhesion, migration, and so on, a wide spectrum of variables needs to be considered to describe these events. Unfortunately, most studies to date dealing with exercise immunology have focused on only one or a few of these variables at one time, and during a short follow-up period, often limited to a few hours postexercise. Comparisons between studies are, therefore, not always possible, and the physiological relevance of the observed changes are difficult to determine. In the present study, several aspects of immunologic parameters in blood have been investigated after exercise-induced muscle damage, and observed alterations have been compared with physiological parameters.
It is well documented that physical exercise induces changes in both the numbers of circulating leukocytes and leukocyte populations, as well as modifications of the expression of different cell surface antigens (23). These changes can depend on several factors. Among them, one can cite altered trafficking of cells between lymphoid tissue and blood and apoptosis of certain cell subsets.
Leukocytes and Monocytes
The postexercise leukocytosis in the present study was mostly due to neutrophilia and monocytosis (Fig. 1, Table 4) and agrees with previous studies using eccentric or resistance exercise (21, 26). Leukocytosis has been suggested to be a marker of liver and muscle damage, at least after strenuous endurance exercise (10). The correlation between circulating leukocyte number and plasma CK demonstrated by Kayashima et al. (10) was not seen in the present study, but the number of neutrophils at 6 h correlated with CK at 48 h (Table 7). Postexercise neutrophilia is thought to depend on the release of neutrophils from the bone marrow because of either cortisol or some unknown signal from exercise-damaged tissue (28). Positive correlation between neutrophil infiltration in human muscle 45 min after eccentric exercise and intracellular Z-band damage was in fact demonstrated by Fielding et al. (5). They suggested that neutrophils might be involved in the repair process of muscle tissue after eccentric exercise. Our results (Table 5) show an increase in the expression of adhesion molecules CD11b and CD62L on monocytes. It has previously been shown that CD11b on neutrophils and C3bi (the CD11b ligand) on human skeletal muscle cells increase after eccentric (8, 26) and resistance (18) exercise. In general, CD62L mediates leukocyte rolling and adhesion to endothelium at the site of inflammation in nonlymphoid organs (31), whereas CD11b is necessary for transepithelial migration, at least of neutrophils (7). However, others have reported that the migration of monocytes and/or macrophages from blood to tissue (kidney) is complement independent (12). Taken together, these findings indicate that changes in the population of circulating neutrophils and monocytes may be regulated, at least partially, through the CD11b and CD62L adhesion molecules and are related to immunologic events in some (muscle) but not all tissue. The twofold increase in CD11b expression on monocytes in the present study is relatively small compared with the six- to eightfold increase on maximally activated monocytes (17). Thus further investigations with postexercise muscle biopsies must be conducted to outline the mechanisms behind leukocyte adhesion and migration in human skeletal muscle and the clinical relevance of these observations. Because there was no change in the number of cells expressing CD11b and CD62L, it can be concluded that the observed increase in expression of CD11b and CD62L is due to an upregulation of membrane expression of these antigens. This is in agreement with previous findings by Kurokawa et al. (11).Lymphocytes
No postexercise lymphocytosis was noted in the present study, but, because of increases in other leukocyte populations (mostly neutrophils and monocytes), the percentage of lymphocytes in the total leukocyte number decreased 6 h after exercise (Fig. 1 and Table 4). Previous studies have shown that the activation and the proliferative response of lymphocytes is usually depressed during exercise but returns to resting levels within a few hours afterward (21, 34). Thus it was surprising to find that the number of CD20+CD5+ B cells decreased significantly 48 h after exercise (Table 4). Because the total number of CD20+ cells remained unchanged (Table 4), it can be concluded that the decreased number of CD20+CD5+ B cells in circulation was probably due to a modulation of CD5 antigen on circulating B cells, or to an altered trafficking of B-cell subsets. This may indicate that there is one immediate postexercise effect on lymphocyte number, activation, and proliferation (11, 21, 26, 32) and a second, delayed effect on CD20+CD5+ B cells. One reason for the delayed effect could be that B cells are influenced by intracellular antigens (other than CK) released from damaged muscle cells 24-48 h after eccentric exercise. It can be speculated that the purpose for decreased CD20+CD5+ B-cell numbers at this late time point is to avoid autoimmunity (24). The T-cell population was not affected by the exercise protocol used in the present study, as indicated by the constant number of lymphocytes in main T-cell subsets as well as in various T-cell subsets associated with cellular activation (except CD4+CD45RO+ memory cells discussed in Memory Cells). Pizza et al. (27) found increased numbers of activated T cells (CD8+CD25+) immediately after one bout of downhill running and a suppression during 48 h of recovery. As indicated by the unchanged CD4-to-CD8 ratio, the present protocol was either not strenuous enough to induce changes in the T-cell population, or all changes had returned to baseline before the first, 6-h postexercise sample.NK Cells
The present study shows that short-duration eccentric exercise can decrease the number of NK cells for at least 6 h postexercise (Fig. 1, Table 4). These findings are similar to reports by Nieman et al. (21) and Bruunsgaard et al. (1). NK cells are thought to be the cell population most respondent to physical exercise, but a postexercise reduction in the number of NK cells has previously been associated only with intense exercise of long duration (23). The postexercise depression in NK cell number and activity has been attributed to changes in cell distribution and related to cortisol levels and the release of prostaglandins from monocytes and neutrophils that have infiltrated damaged muscle (29). It should be noted that the observed change in NK cell number in the present study, and other studies, falls within the range for normal, healthy adults (14). Thus the clinical relevance of these observations is uncertain.Memory Cells
In the present study we showed that, during the 48 h after one bout of eccentric exercise, dynamic changes in the number of T-helper cells with memory function (CD4+CD45RO+) could be observed (Table 4). The numbers of naive T cells (CD45RA+) remained unchanged during the same time period. Because there was no change in the membrane expression of either CD45RA or CD45RO on lymphocytes, it can be concluded that there was a redistribution of memory T-helper cells to and from circulation. It is well documented that, compared with CD45RA+ T cells (naive), CD45RO+ T cells (memory) have increased interaction capacity with activated endothelium (15). It has also been shown that there is selective recruitment of CD45RO+ lymphocytes into inflammatory sites (19, 25). These data, together with the report by van Kooten et al. (35) that CD45RO+ cells are producers of IL-1 and IL-6, suggest that T-memory cells may be involved in both acute and chronic inflammation and, potentially, also in the inflammatory response after eccentric exercise. One possible explanation for the finding in the present study could be that the increase (13%) in memory T-helper cell number 6 h postexercise serves to enhance protection against infection during the proposed postexercise "open window" (23). The decreased number 48 h postexercise (10%) either could serve to decrease the risk
for autoimmunity or indicates an adhesion and/or migration to
and/or through activated endothelium.
Eosinophils and Basophils
Eosinophils and basophils are important cells in allergic diseases and inflammation (3, 22) but have received little attention in exercise immunology. Nieman et al. (21) reported an increased number of basophils immediately and 2 h after exhaustive resistance exercise and a decreased eosinophil number 2 h postexercise. The unchanged number of circulating eosinophils and basophils postexercise in the present study (Table 4) may indicate that, to respond, these cells need a more severe stress than the stress induced in the present study.Correlations
Because the immune system can be modified by physical training, it was not surprising to find correlations between immunologic and physiological parameters. Presently, we can only hypothesize about the physiological relevance of these correlations, with further investigations being necessary. Monocyte number at rest correlated positively with DOMS 48 h postexercise and negatively with the exercise performance on the 10 × 10-s anaerobic cycling test (Table 7). However, the increase in monocyte number from rest to 24 h postexercise correlated positively with anaerobic exercise performance, measured before the bout of eccentric exercise. Basophil number at rest also correlated positively with anaerobic exercise performance. One possible interpretation of the observed correlations is that the number of monocytes is low in anaerobically well-trained subjects and that the degree of postexercise increase in monocyte number is positively related to anaerobic exercise performance. A consequence of the low resting numbers of monocytes is less muscle soreness. These observations could depend on the subject's adaptation to previous physical training.Conclusion
In summary, significant changes were found in 12 of 69 analyzed phenotypes (all investigated phenotypes are not presented), some of which have not previously been analyzed in relation to physical exercise. Despite the short duration of the exercise, several immunologic variables remained altered for at least 48 h, and a longer follow-up is recommended for future studies. Because of the low increase in heart rate and oxygen consumption during the type of exercise performed, the observed alterations are probably due to hormonal changes, or factors released from the affected muscles. Treatment with monochromatic, infrared light did not significantly affect any of the investigated variables. To understand the mechanisms behind the observed phenotypic changes, future studies should probably also include immunohistochemical analyses of muscle biopsies. This is also desirable to determine the physiological and clinical relevance of measured blood variables. Consequently, further investigations of the immune system's role in muscular adaptation to physical exercise are needed.| |
ACKNOWLEDGEMENTS |
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The authors are grateful to laboratory technicians Berit Sjöberg of the Karolinska Institute for analysis of creatine kinase, and Pia Karlsson of Centrala Automations Laboratoriet (now known as Nova Medical) for flow cytometry analyses.
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FOOTNOTES |
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This study was supported in part by Biolight International.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests: C. Malm, Dept. of Physiology and Pharmacology, Karolinska Institute, Box 5626, S-114 86 Stockholm, Sweden (E-mail: christer.malm{at}fyfa.ki.se).
Received 9 February 1998; accepted in final form 30 September 1998.
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Top
Abstract
Introduction
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Discussion
References
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.
* P < 0.01 compared with rest
(Wilcoxon signed rank test).