GEOMETRIC INDICES OF HIP BONE STRENGTH IN MALE PROFESSIONAL SOCCER PLAYERS

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1 ARTICLE ORIGINAL/ ORIGINAL ARTICLE GEOMETRIC INDICES OF HIP BONE STRENGTH IN MALE PROFESSIONAL SOCCER PLAYERS Rawad EL HAGE 1, Eddy ZAKHEM 1, Gautier ZUNQUIN 2, Denis THEUNYNCK 2 El Hage R, Zakhem E, Zunquin G, Theunynck D. Geometric indices of hip bone strength in male professional soccer players. J Med Liban 2014 ; 62 (4) : ABSTRACT Aim of the study : The aim of this study was to compare geometric indices of hip bone strength in male professional soccer players and controls. Methods : Twentythree male professional soccer players and 21 male sedentary subjects whose ages range between 18 and 30 years participated in this study. Weight and height were measured, and body mass index (BMI) was calculated. Daily calcium intake and physical activity were evaluated using validated questionnaires. Hip bone mineral density was measured by dual-energy X-ray absorptiometry (DXA). To evaluate hip bone geometry, DXA scans were analyzed at the narrow-neck (NN), the intertrochanteric (IT) region and the femoral shaft (FS) by the Hip Structure Analysis (HSA) program. Cross sectional area (CSA), an index of axial compression strength, cross sectional moment of inertia (CSMI), an index of structural rigidity, section modulus (Z), an index of bending strength, cortical thickness (CT) and buckling ratio (BR) were measured from bone mass profiles. Results : CSA, CSMI, Z and CT of the three regions (NN, IT and FS) were higher in soccer players compared to controls. After adjustment for either age, body weight, height or physical activity duration (h/week), CSA, CSMI, Z and CT of the three regions remained higher in soccer players compared to controls. Conclusion : This study suggests that, in young adult males, soccer practice is associated with greater axial strength, bending strength and structural rigidity indices at the hip. Keywords : peak bone mass; physical activity; proximal femur INTRODUCTION Osteoporosis is characterized by low bone mineral density (BMD) with microarchitectural deteriorations, which leads to an increased risk of fractures [1]. Although osteoporosis is known to mainly affect postmenopausal women, there is enough evidence to support substantial bone loss with aging in men as well [1]. It has been shown that peak bone mass attained at the third decade may be the single most important factor for the prevention of osteoporosis later in life [2]. Peak bone mass is influenced 1 Département d éducation physique, Faculté des lettres et des sciences humaines, Université de Balamand, Al Koura, Liban. 2 EA 4110, Laboratoire RELACS, Département STAPS, Université du Littoral Côte d Opale, 190 Avenue Schumann, Dunkerque, France. Correspondence: Dr Rawad El Hage. rawadelhage21@hotmail.com El Hage R, Zakhem R, Zunquin G, Theunynck D. Indices géométriques de résistance osseuse de la hanche chez des joueurs professionnels de football. J Med Liban 2014 ; 62 (4) : RÉSUMÉ Objectif de l étude : Le but de cette étude était de comparer les indices géométriques de résistance osseuse chez des footballeurs professionnels et des hommes témoins. Méthodes : Vingt-trois footballeurs professionnels et 21 hommes témoins (sédentaires) âgés de 18 à 30 ans ont participé à cette étude. Le poids, la taille ont été mesurés et l indice de masse corporelle (IMC) a été calculé. La consommation calcique journalière et le volume hebdomadaire d activité physique ont été évalués par des questionnaires validés. La densité minérale osseuse de la hanche a été évaluée par absorptiométrie biphotonique à rayons-x (DXA). La géométrie osseuse au niveau de la hanche a été analysée par le logiciel Hip Structure Analysis (HSA). La surface de la section transversale (CSA), le moment d inertie de la surface transversale (CSMI), le module de section (Z), l épaisseur corticale (CT) et le buckling ratio (BR) au niveau du col fémoral (CF), de la région intertrochantérienne (IT) et de la diaphyse fémorale (DF) ont ainsi été évalués par le logiciel HSA. Résultats : La CSA, le CSMI, le Z et la CT du col fémoral, de la région intertrochantérienne et de la diaphyse fémorale étaient significativement supérieurs chez les footballeurs professionnels par rapport aux témoins. Ces différences entre les deux groupes ont persisté après ajustement pour l âge, le poids, la taille et le volume hebdomadaire d activité physique. Conclusion : Cette étude suggère que chez les hommes jeunes, la pratique du football est associée à une augmentation des indices géométriques de résistance osseuse au niveau de la hanche. by several factors such as genetic factors, endocrine factors, nutritional factors and mechanical factors [1]. Physical activities that include sprints and jumps seem to have a positive effect on BMD [1-5]. For instance, soccer practice has been shown to increase bone mass and BMD in adolescents and adults [3-14]. Although BMD is a predictor of fracture, bone strength and bone geometry are not captured by the measurement. Interestingly, Beck et al. [15] developed a computer program to derive hip geometry from bone mineral data for an estimate of hip strength. Later, many researchers used this program to explore the influence of physical activity and obesity on bone strength and geometry [16-23]. However, little is known concerning the influence of soccer practice on hip geometry in adults. The aim of this study was to compare geometric indices of hip bone strength in male professional soccer players and controls. We hypothesized that professional soccer players should have higher axial and compression strength at the Lebanese Medical Journal 2014 Volume 62 (4) 207

2 hip compared to controls because the hip is a weight-bearing site which is strongly influenced by mechanical factors on one hand, and physical activity is known to influence bone geometry on the other hand [3, 8, 17-18]. METHODS Subjects Twenty-three professional soccer players and twentyone sedentary men (not involved in impact sports) aged between 18 and 30 years participated in this study. The soccer players were regular participants in national or regional competitions. They had been training in their clubs 4 to 6 times per week, for 6-9 h/week for the past 5 years. The participants were nonsmokers and had no history of major orthopaedic problems or other disorders known to affect bone metabolism. Other inclusion criteria included no diagnosis of comorbidities and history of fracture. This study did not include obese (body mass index/bmi > 30 kg/m 2 ) subjects or extremely lean (BMI < 16 kg/m 2 ) subjects. An informed written consent was obtained from the participants. This study was approved by the University of Balamand Ethics Committee. Anthropometric measurements Height (cm) was measured in the upright position to the nearest 1 mm with a Seca standard stadiometer. Body weight (kg) was measured on a Taurus mechanic scale with a sensibility of 100 g. The subjects were weighed wearing only underclothes. BMI was calculated as body weight divided by height squared (kg/m 2 ). Bone mineral density measurements Bone mineral content (BMC, in g) and bone mineral density (BMD, in g/cm 2 ) were determined for each individual by dual-energy X-ray absorptiometry (DXA, Hologic QDR-4500W; Waltham, MA) at the total hip (TH) and the femoral neck (FN). Daily quality control scans were performed with the manufacturer s phantom. The same certified technician performed all analyses using the same technique for all measurements. In our center, the coefficients of variation for hip BMD were < 1% [19-21]. Hip structure analysis The proximal femur densitometry scans were analyzed for geometric properties of bone structure using the Hip Structure Analysis (HSA) software program developed by Beck et al. [15]. The HSA technique calculates dimensions of bone cross-sections at specific locations across the proximal femur using bone mass images generated by absorptiometry scanners [15]. In brief, the HSA program measures bone mineral density and geometry of crosssections using distributions of mineral mass traversing the bone axis, averaged for precision over five parallel lines (5 mm) across the bone axis [15]. The narrow-neck, the intertrochanteric and the femoral shaft regions were analyzed in this study. Bone cross-sectional area (CSA; cm 2 ), cross-sectional moment of inertia (CSMI; (cm 2 ) 2 ), section modulus (Z; cm 3 ), cortical thickness and buckling ratio (BR) were determined directly from the bone profile at the narrow-neck, the intertrochanteric and the femoral shaft regions using algorithms described previously [15]. CSA is equivalent to the amount of bone surface area in the cross-section after excluding soft tissue space and is proportional to conventional bone mineral content in the corresponding cross-section [24]. In mechanical terms, CSA is an indicator of resistance to loads directed along the bone axis [24]. Section modulus is an indicator of TABLE I CLINICAL CHARACTERISTICS and HIP BONE MINERAL DENSITY of the STUDY POPULATION Soccer players Sedentary subjects (n = 23) (n = 21) Age (years) 22.3 ± 4.4* 18.5 ± 1.4 Weight (kg) 74.5 ± 8.2 * 69.2 ± 7.8 Height (cm) ± 5.2 * ± 3.5 BMI (kg/m 2 ) 24.1 ± ± 2.6 DCI (mg/d) 943 ± ± 252 Physical activity (h/week) 12.4 ± 4.28*** 3.4 ± 1.9 TH BMD (g/cm 2 ) ± *** ± FN BMD (g/cm 2 ) ± *** ± BMI: body mass index DCI: daily calcium intake TH: total hip FN: femoral neck BMD: bone mineral density ***p < **p < 0.01 *p < 0.05 TABLE II GEOMETRIC INDICES of HIP BONE STRENGTH of the STUDY POPULATION Soccer players Sedentary subjects (n = 23) (n = 21) NN CSA (cm 2 ) 4.43 ± 0.73 *** 3.54 ± 0.47 NN CSMI (cm 2 ) ± 1.14 *** 3.55 ± 0.59 NN Z (cm 3 ) 2.61 ± 0.49 *** 1.97 ± 0.28 NN CT (cm) ± *** ± NN BR 7.57 ± 1.14 ** 8.86 ± 1.92 IT CSA (cm 2 ) 6.67 ± 1.23 *** 5.47 ± 0.94 IT CSMI (cm 2 ) ± 3.37 ** ± 2.83 IT Z (cm 3 ) 5.35 ± 0.99 *** 4.30 ± 0.86 IT CT (cm) ± ** ± IT BR 5.93 ± 1.20 ** 7.16 ± 1.55 FS CSA (cm 2 ) 4.43 ± 0.73 *** 3.54 ± 0.47 FS CSMI (cm 2 ) ± 1.14 *** 3.55 ± 0.59 FS Z (cm 3 ) 2.61 ± 0.49 *** 1.97 ± 0.28 FS CT (cm) ± *** ± FS BR 7.57 ± 1.14 ** 8.86 ± 1.92 NN: narrow neck IT: intertrochanteric FS: femoral shaft CSA: cross-sectional area CSMI: cross-sectional moment of inertia Z: section modulus CT: cortical thickness BR: buckling ratio ***p < **p < 0.01 *p < Lebanese Medical Journal 2014 Volume 62 (4) R. EL HAGE et al. Physical activity and hip geometry

3 strength of the bone to resist bending and torsion [24]. CSMI (cm 2 ) 2 is the cross-sectional moment of inertia and is derived from the integral of the bone mass weighed by the square of distance from the center of mass. The CSMI is relevant to bending in the plane of the DXA image [24]. Cortical thickness and buckling ratio were also calculated in this study. BR is an index of susceptibility to local cortical buckling under compressive loads [24-25]. All HSA analyses were completed by a single technician at Balamand University. In our laboratory, the coefficients of variation for CSA and Z of the three regions (NN, IT and FS) evaluated by duplicate measurements in 10 subjects were < 3%. Daily calcium intake The estimation of the daily calcium intake (DCI) was based on a frequency questionnaire [26]. Selection of items was based on the food composition diet, frequency of use, and relative importance of food items as a calcium source. The total number of foods was 30 items. The questionnaire included the following [items]: milk and dairy products including calcium-enriched items such as yoghurt, cheese, and chocolate. Items such as eggs, meat, fish, cereals, bread, vegetables, and fruits were also included. Adequacy of calcium in the subjects was assessed using the adequate intake guidelines of 1,300 mg of calcium [27]. Statistical analysis The means and standard deviations or standard errors were calculated for all clinical data and for the bone measurements. Comparisons between the two groups (soccer players and controls) were made after checking for Gaussian distribution. If Gaussian distribution was found, parametric unpaired t-tests were used. In other cases, Mann-Whitney U tests were used. Associations between physical characteristics and bone data were given as Pearson correlation coefficients. Multiple linear regression analysis models were used to test the relationship between bone variables with age, weight and physical activity. Bone variables were compared between the two groups after adjustment for total body weight, height, physical activity and age using a one-way analysis of covariance. Data were analyzed with Number Cruncher Statistical System (NCSS, 2001). A level of significance of p < 0.05 was used. RESULTS Clinical characteristics and bone data of the study population Age, weight, height, BMI, daily calcium intake, physical activity (h/week), and hip BMD are shown in table I. Age, weight, height, physical activity, TH BMD and FN BMD were higher in soccer players compared to controls (p < 0.05). BMI and daily calcium intake were not significantly different between the two groups (Table I). Hip structure analysis variables of the study population CSA, CSMI, Z, CT and BR of the NN, the IT and the FS regions are shown in table II. CSA, CSMI, Z and CT of the three regions were higher in soccer players compared to controls (p < 0.05). BR of the three regions was lower in soccer players compared to controls (p < 0.05). Correlations between clinical characteristics and hip structure analysis variables of the study population Age was positively correlated to Z of the three regions. Weight and physical activity were positively correlated to CSA, Z and CT of the three regions (Tables III-V). Multiple linear regression analysis models Body weight was a stronger determinant of CSA and Z of the three regions (NN, IT and FS) than age and physical activity (Table VI). Physical activity remained positively correlated to CSA and Z of the narrow-neck after controlling for age and body weight. Adjusted hip structure analysis variables After adjusting for either weight, height, physical activity or age, CSA, CSMI, Z and CT of the three regions (NN, IT and FS) remained higher in soccer players compared to controls (p < 0.05) (Table VII). TABLE III CORRELATIONS between CLINICAL CHARACTERISTICS and GEOMETRIC INDICES of NARROW-NECK BONE STRENGTH CSA CSMI Z CT BR (cm 2 ) (cm 2 ) 2 (cm 3 ) (cm) Age (years) ** 0.37 * Weight (kg) 0.51 *** 0.51 *** 0.50 *** 0.43 ** 0.26 Height (cm) 0.45 ** 0.50 *** 0.46 ** 0.33 * 0.10 Body mass index (kg/m 2 ) 0.33 * 0.30 * 0.32 * 0.31 * 0.24 Daily calcium intake (mg/d) Physical activity (h/week) 0.44 ** 0.51 *** 0.50 *** 0.30 * 0.23 CSA: cross sectional area CSMI: cross sectional moment of inertia Z: section modulus CT: cortical thickness BR: buckling ratio ***p < **p < 0.01 *p < 0.05 R. EL HAGE et al. Physical activity and hip geometry Lebanese Medical Journal 2014 Volume 62 (4) 209

4 TABLE IV CORRELATIONS between CLINICAL CHARACTERISTICS and GEOMETRIC INDICES of INTERTROCHANTERIC BONE STRENGTH CSA CSMI Z CT BR (cm 2 ) (cm 2 ) 2 (cm 3 ) (cm) Age (years) 0.29 * 0.35 * 0.31 * Weight (kg) 0.39 * 0.40 ** 0.37 * 0.31 * 0.16 Height (cm) * 0.30 * Body mass index (kg/m 2 ) Daily calcium intake (mg/d) Physical activity (h/week) 0.39 * 0.41 * 0.41 * 0.33 * 0.07 CSA: cross sectional area CSMI: cross sectional moment of inertia Z: section modulus CT: cortical thickness BR: buckling ratio *** p < **p < 0.01 *p < 0.05 TABLE V CORRELATIONS between CLINICAL CHARACTERISTICS and GEOMETRIC INDICES of FEMORAL SHAFT BONE STRENGTH CSA CSMI Z CT BR (cm 2 ) (cm 2 ) 2 (cm 3 ) (cm) Age (years) 0.46 * 0.34 * 0.41 ** 0.42 ** 0.37 * Weight (kg) 0.57 *** 0.68 *** 0.67 *** Height (cm) 0.57 *** 0.57 *** 0.52 *** Body mass index (kg/m 2 ) 0.44 * 0.47 ** 0.48 *** Daily calcium intake (mg/d) Physical activity (h/week) 0.43 * * 0.40 * 0.41 * CSA: cross sectional area CSMI: cross sectional moment of inertia Z: section modulus CT: cortical thickness BR: buckling ratio *** p < **p < 0.01 *p < 0.05 TABLE VII GEOMETRIC INDICES of HIP BONE STRENGTH ADJUSTED for BODY WEIGHT, PHYSICAL ACTIVITY and AGE in the TWO GROUPS ADJUSTED FOR BODY WEIGHT ADJUSTED FOR PHYSICAL ACTIVITY ADJUSTED FOR AGE Soccer players Sedentary subjects Soccer players Sedentary subjects Soccer players Sedentary subjects (n = 23) (n = 21) (n = 23) (n = 21) (n = 23) (n = 21) NN CSA (cm 2 ) 4.35 ± 0.12 *** 3.66 ± ± 0.15 ** 3.47 ± ± 0.13 *** 3.51 ± 0.13 NN CSMI (cm 2 ) ± 0.17 *** 3.71 ± ± 0.21 ** 3.53 ± ± 0.19 *** 3.61 ± 0.20 NN Z (cm 3 ) 2.56 ± 0.07 *** 2.04 ± ± 0.09 ** 1.94 ± ± 0.08 *** 1.99 ± 0.09 NN CT (cm) ± * ± ± ** ± ± ** ± NN BR 7.64 ± 0.32 * 8.71 ± ± ± ± 0.32 * 8.96 ± 0.34 IT CSA (cm 2 ) 6.52 ± 0.21 ** 5.64 ± ± 0.28 * 5.33 ± ± 0.23 ** 5.50 ± 0.24 IT CSMI (cm 2 ) ± 0.59 * ± ± 0.80 * ± ± 0.65 * ± 0.68 IT Z (cm 3 ) 5.23 ± 0.17 ** 4.43 ± ± 0.24 * 4.18 ± ± 0.19 ** 4.34 ± 0.20 IT CT (cm) ± ** ± ± 0.02 * ± ± 0.19 ** 4.34 ± 0.20 IT BR 5.94 ± 0.29 * 7.09 ± ± ± ± 0.29 * 7.19 ± 0.30 FS CSA (cm 2 ) 5.57 ± 0.14 *** 4.68 ± ± 0.19 ** 4.45 ± ± 0.16 ** 4.65 ± 0.17 FS CSMI (cm 2 ) ± 0.08 * 4.24 ± ± 0.27 * 3.80 ± ± 0.22 * 4.10 ± 0.23 FS Z (cm 3 ) 2.99 ± 0.08 ** 2.60 ± ± 0.12 ** 2.41 ± ± 0.10 ** 2.55 ± 0.11 FS CT (cm) ± *** ± ± ** ± ± ** ± FS BR 2.11 ± 0.12 ** 2.75 ± ± ± ± 0.12 * 2.67 ± 0.12 NN: narrow-neck IT: intertrochanteric FS: femoral shaft CSA: cross-sectional area CSMI: cross sectional moment of inertia Z: section modulus CT: cortical thickness BR: buckling ratio ***p < **p < 0.01 *p < Lebanese Medical Journal 2014 Volume 62 (4) R. EL HAGE et al. Physical activity and hip geometry

5 TABLE VI MULTIPLE LINEAR REGRESSION ANALYSIS MODELS COEFFICIENT SE p Dependent variable: NN CSA (r 2 = 0.43) Constant Age (years) Weight (kg) < Physical activity (h/week) Dependent variable: NN Z (r 2 = 0.45) Constant Age (years) Weight (kg) < Physical activity (h/week) Dependent variable: IT CSA (r 2 = 0.30) Constant Age (years) Weight (kg) Physical activity (h/week) Dependent variable: IT Z (r 2 = 0.26) Constant Age (years) Weight (kg) < Physical activity (h/week) Dependent variable: FS CSA (r 2 = 0.51) Constant Age (years) Weight (kg) < Physical activity (h/week) Dependent variable: FS Z (r 2 = 0.55) Constant Age (years) Weight (kg) < Physical activity (h/week) NN: narrow-neck IT: intertrochanteric FS: femoral shaft CSA: cross-sectional area Z: section modulus DISCUSSION The main finding of this study was that axial strength, bending strength and structural rigidity indices at the hip are higher in professional soccer players compared to controls. These differences remained significant after adjustment for body weight. Total hip BMD and femoral neck BMD were higher in soccer players compared to controls. These results are in line with those of several studies and can confirm the positive effect of soccer practice on hip BMD [8, 10, 13]. CSA, CSMI, Z and CT values were higher in soccer players compared to controls. These differences remained significant after adjustment for weight or age. Our results are in line with those of several studies that aimed at exploring the effects of high-impact physical activity on hip geometry [8, 17-18, 22]. After adjustment for physical activity, these differences were reduced highlighting the key influence of physical activity on geometric indices of hip bone strength. Buckling ratio values were lower in soccer players compared to controls. These differences remained significant after adjustment for weight or age. BR is a geometric configuration that describes threshold behavior beyond which strength may be compromised under compressive loads [24, 28]. BR values are elevated in osteoporotic subjects and are positively associated with the incidence of hip fractures [28]. Thus, our results suggest that soccer practice may prevent against hip fractures later in life. In our study, body weight was a strong predictor of hip bone strength. This result is in line with those of several previous studies [19, 22-23]. In fact, low body weight and BMI are associated with an increased risk of hip fracture while obesity is associated with a decreased risk of hip fracture [29]. Furthermore, it has been shown that lean mass is a stronger predictor of geometric indices of hip bone strength than fat mass [23, 30-31]. Physical activity (h/week) was positively correlated to CSA, Z and CT of the three regions. In fact, the hip is a weight-bearing site which is strongly influenced by physical activity [2, 8]. The positive influence of physical activity on hip geometry has been well documented [8, 16-18]. There is some evidence to suggest that the positive effects of exercise on bone strength are not detected by bone mass measurements [9, 16]. For instance, Haapasalo et al. [9] have shown significant increases in the bending strength of the arm of tennis players without any increase in its volumetric BMD. Daily calcium intake was not correlated to HSA variables in our study. The lack of correlation between DCI and bone variables may be due to the cross-sectional nature of the study. Our study had some limitations. The cross-sectional nature of this study is a limitation because it cannot evaluate the confounding variables. The second limitation is the relatively small number of subjects in each group. The third limitation is the two-dimensional nature of DXA [32]. However, up to our knowledge, it s one of few studies that aimed at exploring the influence of soccer practice on geometric indices of hip bone strength in young men. In conclusion, this study suggests that soccer practice is associated with increased axial strength, bending strength and structural rigidity at the hip in young men. Thus, it is suggested that soccer practice during adulthood may prevent osteoporosis at the hip later in life. ACKNOWLEDGMENTS This study was supported by a grant from the research council of the University of Balamand, Lebanon. Moreover, we gratefully acknowledge Lina Rahmé El Hage for her help in improving the quality of this manuscript. CONFLICTS OF INTEREST: None to declare. R. EL HAGE et al. Physical activity and hip geometry Lebanese Medical Journal 2014 Volume 62 (4) 211

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