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Clinical Hemorheology and Microcirculation 49 (2011) 207–214 DOI 10.3233/CH-2011-1470 IOS Press

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Blood rheology and body composition as determinants of exercise performance in female rugby players

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Jean-Frédéric Bruna,∗ , Emmanuelle Varlet-Marieb,c , Delphine Cassana and Eric Raynaud de Mauvergera a

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U1046, INSERM, Université de Montpellier 1, Université de Montpellier 2, Montpellier, France; CHRU Montpellier, Département de Physiologie Clinique, Montpellier, France b Laboratoire Performance Santé Altitude, Université de Perpignan Via Domitia, Département Sciences et Techniques des Activités Physiques et Sportives, Font-Romeu, France c Laboratoire de Biophysique and Bio-Analyses, Faculté de Pharmacie, Université Montpellier I, Montpellier, France

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Abstract. Athletes involved in rugby are characterized by a very specific pattern of body composition with an unusually important muscle mass. In a preceding study about rugbymen we evidenced that they exhibit a correlation between red blood cell aggregability and the amount of body fat although it remains within a normal range, and that red cell rigidity was correlated to isometric adductor strength. We had the opportunity of studying the relationships among exercise performance, body composition and hemorheology in 19 female rugby players (age 19–26, mean: 24.47 ± 0.67 yr) practising 4 – 10 hr/wk (mean 7.15 ± 0.3) since 1–12 yr (mean 4,05 ± 0,694). VO2max was not related by its own to blood rheology, either hematocrit (r = −0.0717 p = 0.7706) or plasma viscosity (r = 0.0144; p = 0.9533), but other markers of performance exhivited a correlation with red cell rheology. Relationships between fitness and body composition were evidenced. Isometric handgrip strength was negatively correlated to red blood cell aggregability (Myrenne M, r = −0.57839; p = 0.00948 M1 r = −0.58910; p = 0.00795). Adductor isometric strength was negatively correlated to red blood cell aggregability Myrenne M (r = −0.5033; p = 0.0280) but not to M1 (r = −0.4227; p = 0.0714). Fat mass is a major determinant of the maximal oxygen consumption VO2max either measured by a field test (r = −0.766; p = 0.00013) or exercise test (r = −0.575; p = 0.00994) and was also negatively correlated to both handgrip (r = −0.4918; p = 0.0325) and RBC aggregability M (r = −0.57839; p = 0.00948 and M1 r = −0.5891; p = 0.00795). Independently of fat mass, FFM appears to be a determinant of blood viscosity (r = 0.4622; p = 0.0463) due to its correlation with RBC rigidity (r = 0.4781; p = 0.0384). Thus, trained young women exercising 4–10 hr/wk and thus exhibiting a low percentage of body fat exhibit clear relationships between body composition and hemorheology, but fat mass being low, the parameter correlated with blood rheology is in this case fat-free mass, consistent with recent findings indicating that high fat mass in women is sometimes correlated with parameters of the metabolic syndrome such as insulin resistance or inflammation. In addition, parameters quantifying fatness even within such a physiological range are in this sample negatively related with exercise performance. Keywords: Rugby, exercise, fat mass, hematocrit, blood viscosity, plasma viscosity, hemorheology, erythrocyte aggregation

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Corresponding author: Dr. Jean-Frédéric Brun, U1046, INSERM, Université de Montpellier 1, Université de Montpellier 2, Montpellier, France; CHRU Montpellier, Département de Physiologie Clinique, Montpellier, France. E-mail: [email protected]. 1386-0291/11/$27.50 © 2011 – IOS Press and the authors. All rights reserved

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1. Introduction

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Exercise modifies blood viscosity [11, 16, 18, 27]. In a recent review we tried to summarize all these effects [6]. On the whole regular exercise training results in increased blood fluidity [5, 6]. On the other hand, exercise-induced alterations in body composition were likely to result in further modifications of blood viscosity [8], but this issue remains poorly known. Recently, emphasis has been given on the complexity ot the relationships between body composition and metabolism. While on the whole excess fat is associated with hyperlipidemia, insulin resistance, and increated cardiovascular risk [1, 26, 28–29], gluteofemoral fat is on the opposite protective against these pathogenic, due to its specific storage properties [22]. Moreover, fat-free mass, which is generally assumed to be beneficial for metabolism, is associated with insulin resistance in obese women [4]. Rugby is an interesting sport for studying these relationships since athletes practising it exhibit a high fat-free mass [3, 12]. These data prompted us to investigate in female rugby players the relationships between these specific aspects of body composition and blood rheology.

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2. Methods 2.1. Study subjects

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We had the opportunity of studying the relationships among exercise performance, body composition and hemorheology in 19 female rugby players (age 19–26, mean: 24.47 ± 0.67 yr) practising 4–10 hr/wk (mean 7.15 ± 0.3) since 1–12 yr (mean 4,05 ± 0,694). Subjects were assessed in our laboratory with bioimpedance analysis (Dietosystem) for measuring body composition with published equations [19, 21] and a maximal exercise test on cycloergometer in order to measure their maximal oxygen consumption VO2max according to the guidelines of the French Society of Sports Medicine. 2.2. Hemorheological in vitro measurements Blood samples for hemorheological measurements (7 ml) were drawn with potassium EDTA as the anticoagulant in a vacuum tube (Vacutainer). Viscometric measurements were done at very high shear rate (1000 s−1 ) with a falling ball viscometer (MT 90 Medicatest, F-86280 Saint Benoit) [14, 17]. The coefficient of variation of this method ranges between 0.6 and 0.8%. We measured with this device apparent viscosity of whole blood at native hematocrit, plasma viscosity, and blood viscosity at corrected hematocrit (45%) according to the equation of Quemada [23]. η = ηp (1 − 1/2kφ)−2

(1)

– where φ is hematocrit, ηp is plasma viscosity, and k(␥) is a shear-dependent parameter quantifying the contribution of erythrocyte rheological properties to whole blood viscosity. – At the high shear rate used here k(␥) is representative of red cell rigidity (ie, the lower k(␥), the higher is erythrocyte deformability). With this equation it is possible to standardize η for hematocrit 45% after calculating k: k = 2.(1 − ηr −0.5 ) · h−1 This value of k is reintroduced in Equation (1) with φ set at 0.45.

(2)


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RBC aggregation was assessed with the Myrenne aggregometer [25] which gives two indices of RBC aggregation: ‘M’ (aggregation during stasis after shearing at 600 s−1 ) and ‘M1’ (facilitated aggregation at low shear rate after shearing at 600 s−1 ). It was also measured with laser backscattering (erythroagregometer SEFAM-AFFIBIO [13, 15]. Hematocrit was measured with microcentrifuge. The recently released new guidelines for hemorheological laboratory techniques [2] were carefully taken into account.

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2.3. Statistics

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Values are presented as mean ± the standard error of the mean (SEM). Linear correlations and stepwise correlation analyses were performed with the software “Sigmastat” from Jandel Scientific, San Jose, California, USA. A value of p < 0.05 was considered as significant. 3. Results

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As shown on Figs. 1 and 2, isometric handgrip strength was negatively correlated to red blood cell aggregability (Myrenne M, r = −0.57839; p = 0.00948; M1 r = −0.58910; p = 0.00795). As shown on Fig. 3, adductor isometric strength was negatively correlated to red blood cell aggregability Myrenne M (r = −0.5033; p = 0.0280). However, the correlation of adductor isometric strength with M1 did not reach significance (r = −0.4227; p = 0.0714). As shown on Table 3 fat mass is a major determinant of VO2max either measured by a field test (r =−0.766; p = 0.00013) or exercise test (r = −0.575; p = 0.00994) and was also negatively correlated with handgrip (r = −0.4918; p = 0.0325). By contrast as shown on table 4, VO2 max was not related by its own to blood rheology, either hematocrit (r = −0.0717; p = 0.7706) or plasma viscosity (r = 0.0144; p = 0.9533). The most original finding of this study is shown on Figs. 4 and 5 which show that that FFM appears to be a determinant of blood viscosity (r = 0.4622; p = 0.0463) due to its correlation with RBC rigidity (r = 0.4781; p = 0.0384). A multivariate analysis shows that this correlation is not explained by a correlation of these 450

Handgrip strength (N)

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y = -17,887x + 415,86 R2 = 0,3345

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Fig. 1. Negative correlation between isometric handgrip strength and red blood cell aggregability index Myrenne M (r = −0.57839 p = 0.00948).

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J.-F. Brun et al. / Hemorheology in rugby women 450

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y = -14,282x + 459,74 R2 = 0,347

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Handgrip strength (N)

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Fig. 2. Negative correlation between isometric handgrip strength and red blood cell aggregability M1 (r = −0.58910; p = 0.00795).

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Adductor strength (N)

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y = -14,282x + 459,74 R2 = 0,347

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Fig. 3. Negative correlation between adductor isometric strength and red blood cell aggregability Myrenne M (r = −0.5033; p = 0.0280). The correlation with M1does not reach significance (r = −0.4227; p = 0.0714).

viscosity factors with FM, which is actually well correlated with FFM (0.678; p = 0.00143) but neither with blood viscosity (r = 0.259; p = 0.284) nor RBC rigidity index ‘Tk’ (r = 0.295; p = 0.220). Table 3 also shows that neither FM nor FFM are correlated with plasma viscosity (respectively r = 0.309 and r = 0.153, both nonsignificant). Table 3 also shows that total body water, which is strongly correlated with FFM (r = 0.759503; p = 0.000162) does not exhibit any significant correlation with hemorheological parameters. 4. Discussion This study in female rugby players confirms some of our previous findings in male rugby players and shows also that fat free mass is positively correlated with red cell rigidity. Therefore in young, healthy

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r = 0,462 p = 0,046

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Whole blood viscosity (mPa,s)


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Fig. 4. Correlation between fat-free mass and blood viscosity (r = 0.4622; p = 0.0463). This correlation is not explained by a correlation between fat mass and blood viscosity, since this one is not significant.

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Tk (RBC rigidity index)

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Fig. 5. Correlation between fat-free mass and the RBC rigidity index ‘Tk’ (r = 0.4781; p = 0.0384). Since fat free mass is not correlated with plasma viscosity, this correlation explains all the correlation shown on Fig 4.

Table 1 Anthropometry, body composition, hemorheologic parameters and ergometric data of study subjects (n=19, all female) Age (years)

BMI (kg/m²)

%Fat

24,47 ± 0,67 24,56 ± 0,67 15,47 ± 0,65

VO2max exercise test (mlmin−1 kg−1 ) Handgrip strength (N) Adductor strength (N) 32,60 ± 1,09

328,42 ± 8,25

335,8 ± 14,98

women used to regularly exercise, we evidence the same relationships as we previously reported in patients suffering from the metabolic syndrome. Fat mass in overweight patients is associated with higher red cell aggregability [8, 10]. However, in male rugby players [3] such an association is also found, although the percentage of fat is within a physiological range. Interestingly, this relationship is found again in our sample of rugbywomen, confirming that the proportionality between body fat mass and erythrocyte aggregability is a physiological relationship, even

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J.-F. Brun et al. / Hemorheology in rugby women Table 2 Correlations between body composition and ergometric data of study subjects VO2max exercise test

Handgrip strength

Adductor strength

r = −0.766 p = 0.000130 r = −0.190 NS r = −0.190 NS

r = −0.575 p = 0.00994 r = −0.105 NS r = −0.105 NS

r = −0.4918 p = 0.0325 r = −0.118 NS r = −0.118 NS

r = −0.128 NS r = 0.0993 NS r = 0.0993 NS

Fat-free mass (kg) Total body water (l)

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Fat mass (kg)

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VO2max field test

Table 3 Correlations between body composition and hemorheological parameters RBC RBC aggregation aggregation “M” “M1”

r = −0.128 r = 0.139 NS NS Fat mass r = −0.233 r = 0.267 NS NS Total body water r = −0.0504 r = −0.0278 NS NS Body mass index r = −0.335 r = 0.193 NS NS

r = 0.3912 p = 0.0977 r = 0.382 NS r = 0.189 NS r = 0.314 NS

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Fat-free mass

Blood viscosity

Plasma viscosity

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Hematocrit

r = 0.4622 r = 0.153 p = 0.0463 NS r = 0.259 r = 0.309 NS NS r = 0.296 r = −0.0508 NS NS r = 0.295 r = 0.129 NS NS

Blood viscosity at Hct corrected 45%

RBC rigidity “Tk”

RBC rigidity “k”

r = 0.4981 p = 0.0300 r = 0.331 NS r = 0.327 NS r = 0.4128 p = 0.0790

r = 0.4781 p = 0.0384 r = 0.295 NS r = 0.327 NS r = 0.4198 p = 0.0735

r = 0.4799 p = 0.0376 r = 0.293 NS r = 0.332 NS r = 0.4196 p = 0.0737

Table 4 Correlations between ergometry and hemorheological parameters Hematocrit

VO2max exercise r = −0.0717 test NS Pmax exercise r = −0.0342 test NS

RBC RBC aggregation aggregation “M” “M1” r = 0.282 NS r = 0.345 NS

r = 0.113 NS r = 0.236 NS

Blood viscosity

Plasma viscosity

r = −0.195 r = 0.0144 NS NS r = 0.0108 r = 0.207 NS NS

Blood viscosity at Hct corrected 45% r = −0.113 NS r = 0.0560 NS

RBC rigidity “Tk”

RBC rigidity “k”

r = −0.178 r = −0.178 NS NS r = −0.0294 r = −0.0324 NS NS

if it is exaggerated when fat mass reaches pathologic levels. The mechanism of this relationship is not yet defined. Actually, adipocytes release free-fatty acids, PAI1 that leads to an increase in fibrinogen, and a host of biologically active substances refered as adipokines. Among adipokines, leptin has been reported to be associated to higher blood viscosity [7], but the hemorheological effects of other substances secreted by adipocytes remains largely unknown. What is newer concerning fat mass and hemorheology


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Acknowledgments

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is the finding that gluteofemoral fat is associated with a decrease in plasma viscosity [9]. It was logic to look for such a correlation, since there is growing evidence that lower body fat exerts a protective role, by decreasing circulating levels of pro-atherogenetic lipoprotein [22]. Lower body fat is the opposite picture compared to abdominal obesity, and is associated with high values of insulin sensitivity [24]. I represents a phenotype of “metabolically healthy obesity” [20] in which weight loss does not improve insulin sensitivity but, on the other way about, decreases it, resulting in a worsening of the metabolic profile. In patients exhibiting the metabolic syndrome, we reported that hip circumference is negatively correlated to plasma viscosity [9]. A third relationship that needs to be pointed out is the positive correlation between fat-free mass and blood viscosity. We looked for this correlation after the report by Brochu et al of an unexpected insulin resistance in post menopausal obese women exhibiting high fat free mass (FFM) [4]. In patients suffering from the metabolic syndrome, FFM is associated with higher blood viscosity and hematocrit [9]. Our current findings show that even in healthy subjects, a high FFM is associated with hyperviscosity, and more precisely with higher red cell rigidity and plasma viscosity. This fact is interesting because both are likely to impair blood flow at the microcirculation level. Therefore the physiological meaning of these results require more investigations. On the whole, results presented here support the concept that body composition, not only in pathology but also in physiology, is closely related to hemorheology and is thus likely to be and important modifier of blood viscosity factors. Even more, this relationship is complex, since beside the well known impairment of blood fluidity that occurs when overall fat mass increases, and the more pronounced hyperviscosity observed in abdominal obesity, there are specific effects of gluteofemoral fat (that seems to improve blood rheology) and of FFM (that seems to surprisingly impair it). All these relationships need to be more thoroughly described, and their mechanisms and physiological meaning remain to elucidated.

References

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The authors comply with the Ethical Guidelines for Publication in Clinical Hemorheology and Microcirculation as published on the IOS Press website and in Volume 44, 2010, pp. 1-2 of this journal.

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