Impact of Physical Exercises on Bone Activities

A special issue of Life (ISSN 2075-1729). This special issue belongs to the section "Physiology and Pathology".

Deadline for manuscript submissions: closed (1 March 2021) | Viewed by 33434

Special Issue Editors


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Guest Editor
Department of Bioengineering and Osteoarticular Bioimaging (B2OA), Universite d'Orleans, 45100 Orléans, France
Interests: Physical exercise; bone repair; bone quality, bone biology, total knee arthroplasty and rehabilitation

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Co-Guest Editor
Multiscale Multimodal Imaging and Modeling of Bone and Joint Tissue Laboratory, University of Orléans, 45100 Orléans, France
Interests: cell biology; physical activity; cell adhesion

Special Issue Information

Dear Colleagues,

Bone tissue is a dynamic tissue that is modeled and reshaped according to the constraints applied to it (Law of Julius Wolff, 1892(Wolff, 1986)). In particular, the development of bone mass in the absence of exercise is estimated at only 30 to 50% of its potential (Santos et al., 2017). As with muscle, exercise and mechanical strains are therefore necessary for bone strengthening. Physical exercise causes mechanical stresses (impacts on the ground, shocks, traction at muscular insertions) that directly affect bone (Rubin and Lanyon, 1984) and biochemical agents transported by blood (hormones, cytokines) favoring bone anabolism (Bonewald, 2007; Bonewald and Johnson, 2008). Exercise is also recognized to have a positive effect on the human skeleton and to contribute to the prevention and treatment of Bone (Daly et al., 2014; Marques et al., 2012; Musumeci et al., 2013).

Bone quality is associated to bone strength and is dependent on a large variety of interconnected factors. Bone geometry (bone size, cortical thickness, moment of inertia), microarchitecture (trabecular connectivity, trabecular shape, cortical porosity, tissue organization) and tissue properties (cellular density, osteocyte network integrity, mineralization degree, mineral crystallinity, hydration, degree and type of collagen cross-linking) all have an effect on bone quality (Fonseca et al., 2014).

Nowadays, it is generally accepted that without considering the specific effects of the bone cells, whatever the theoretical model, the prediction of bone remodeling remains at best phenomenologically driven. Although at the continuous level (scale of the bone) the continuum mechanics is “manageable”, the integration of continuum biology is highly risky since, for the time being, there are no experimental measurements available in the literature able to link the local cells phenomena to the bone continuum. The full understanding of the bone mechanobiology is still unknown.

For this special issue, studies in human and animal model could be accepted. Original article and/or review will be appreciated.

Dr. Hugues Portier
Dr. Stéphane Pallu
Guest Editors

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Keywords

  • bone
  • mechanical strains
  • physical exercises
  • osteocytes
  • osteoclast activities
  • bone quality
  • Bone microstructure
  • Bone biology

Published Papers (11 papers)

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Research

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12 pages, 2788 KiB  
Article
Impact of Treadmill Interval Running on the Appearance of Zinc Finger Protein FHL2 in Bone Marrow Cells in a Rat Model: A Pilot Study
by Alexandre Germain, Celine Bourzac, Chantal Pichon, Hugues Portier, Stéphane Pallu and Philippe Germain
Life 2022, 12(4), 528; https://doi.org/10.3390/life12040528 - 2 Apr 2022
Cited by 1 | Viewed by 1708
Abstract
Although the benefits of physical exercise to preserve bone quality are now widely recognized, the intimate mechanisms leading to the underlying cell responses still require further investigations. Interval training running, for instance, appears as a generator of impacts on the skeleton, and particularly [...] Read more.
Although the benefits of physical exercise to preserve bone quality are now widely recognized, the intimate mechanisms leading to the underlying cell responses still require further investigations. Interval training running, for instance, appears as a generator of impacts on the skeleton, and particularly on the progenitor cells located in the bone marrow. Therefore, if this kind of stimulus initiates bone cell proliferation and differentiation, the activation of a devoted signaling pathway by mechano-transduction seems likely. This study aimed at investigating the effects of an interval running program on the appearance of the zinc finger protein FHL2 in bone cells and their anatomical location. Twelve 5-week-old male Wistar rats were randomly allocated to one of the following groups (n = 6 per group): sedentary control (SED) or high-intensity interval running (EX, 8 consecutive weeks). FHL2 identification in bone cells was performed by immuno-histochemistry on serial sections of radii. We hypothesized that impacts generated by running could activate, in vivo, a specific signaling pathway, through an integrin-mediated mechano-transductive process, leading to the synthesis of FHL2 in bone marrow cells. Our data demonstrated the systematic appearance of FHL2 (% labeled cells: 7.5%, p < 0.001) in bone marrow obtained from EX rats, whereas no FHL2 was revealed in SED rats. These results suggest that the mechanical impacts generated during high-intensity interval running activate a signaling pathway involving nuclear FHL2, such as that also observed with dexamethasone administration. Consequently, interval running could be proposed as a non-pharmacological strategy to contribute to bone marrow cell osteogenic differentiation. Full article
(This article belongs to the Special Issue Impact of Physical Exercises on Bone Activities)
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25 pages, 7326 KiB  
Article
Prediction of Cortical Bone Thickness Variations in the Tibial Diaphysis of Running Rats
by Daniel George, Stéphane Pallu, Céline Bourzac, Rkia Wazzani, Rachele Allena, Yves Rémond and Hugues Portier
Life 2022, 12(2), 233; https://doi.org/10.3390/life12020233 - 3 Feb 2022
Cited by 5 | Viewed by 1465
Abstract
A cell-mechanobiological model is used for the prediction of bone density variation in rat tibiae under medium and high mechanical loads. The proposed theoretical-numerical model has only four parameters that need to be identified experimentally. It was used on three groups of male [...] Read more.
A cell-mechanobiological model is used for the prediction of bone density variation in rat tibiae under medium and high mechanical loads. The proposed theoretical-numerical model has only four parameters that need to be identified experimentally. It was used on three groups of male Wistar rats under sedentary, moderate intermittent and continuous running scenarios over an eight week period. The theoretical numerical model was able to predict an increase in bone density under intermittent running (medium intensity mechanical load) and a decrease of bone density under continuous running (higher intensity mechanical load). The numerical predictions were well correlated with the experimental observations of cortical bone thickness variations, and the experimental results of cell activity enabled us to validate the numerical results predictions. The proposed model shows a good capacity to predict bone density variation through medium and high mechanical loads. The mechanobiological balance between osteoblast and osteoclast activity seems to be validated and a foreseen prediction of bone density is made available. Full article
(This article belongs to the Special Issue Impact of Physical Exercises on Bone Activities)
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11 pages, 2392 KiB  
Article
Swimming Training Does Not Affect the Recovery of Femoral Midshaft Structural and Mechanical Properties in Growing Diabetic Rats Treated with Insulin
by Gilton de Jesus Gomes, Márcia Ferreira da Silva, Edson da Silva, Ricardo Junqueira Del Carlo, Daise Nunes Queiroz da Cunha, Miguel Araújo Carneiro-Junior, Thales Nicolau Prímola-Gomes and Antônio José Natali
Life 2021, 11(8), 786; https://doi.org/10.3390/life11080786 - 3 Aug 2021
Cited by 1 | Viewed by 1536
Abstract
Background: The effects of swimming training associated with insulin treatment on the cortical bone health in young rats with severe type 1 diabetes remain unclear, although there is evidence of such effects on the cancellous bone. This study examined the effects of swimming [...] Read more.
Background: The effects of swimming training associated with insulin treatment on the cortical bone health in young rats with severe type 1 diabetes remain unclear, although there is evidence of such effects on the cancellous bone. This study examined the effects of swimming training combined with insulin therapy on the femoral midshaft structural and mechanical properties in growing rats with type 1 diabetes. Methods: Male Wistar rats were divided into six groups (n = 10): control sedentary, control exercise, diabetic sedentary, diabetic exercise, diabetic sedentary plus insulin and diabetic exercise plus insulin. Diabetic rats received an injection (60 mg/kg body weight) of streptozotocin (STZ). Exercised animals underwent a swimming program for eight weeks. Results: Diabetes induced by STZ decreased the bone mineral content (BMC) and density (BMD), and cortical thickness and maximum load and tenacity in the femoral midshaft. Insulin treatment partially counteracted the damages induced by diabetes on BMC, BMD and cortical thickness and tenacity. Swimming training did not affect the femoral structural and mechanical properties in diabetic rats. The combination of treatments did not potentiate the insulin effects. In conclusion, swimming training does not affect the benefits of insulin treatment on the femoral midshaft structural and mechanical properties in growing rats with severe type 1 diabetes. Full article
(This article belongs to the Special Issue Impact of Physical Exercises on Bone Activities)
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20 pages, 5657 KiB  
Article
Association between Visceral and Bone Marrow Adipose Tissue and Bone Quality in Sedentary and Physically Active Ovariectomized Wistar Rats
by Hélder Fonseca, Andrea Bezerra, Ana Coelho and José Alberto Duarte
Life 2021, 11(6), 478; https://doi.org/10.3390/life11060478 - 25 May 2021
Cited by 2 | Viewed by 2339
Abstract
Background: Obesity is considered protective for bone mass, but this view has been progressively challenged. Menopause is characterized by low bone mass and increased adiposity. Our aim was to determine how visceral and bone marrow adiposity change following ovariectomy (OVX), how they correlate [...] Read more.
Background: Obesity is considered protective for bone mass, but this view has been progressively challenged. Menopause is characterized by low bone mass and increased adiposity. Our aim was to determine how visceral and bone marrow adiposity change following ovariectomy (OVX), how they correlate with bone quality and if they are influenced by physical activity. Methods: Five-month-old Wistar rats were OVX or sham-operated and maintained in sedentary or physically active conditions for 9 months. Visceral and bone marrow adiposity as well as bone turnover, femur bone quality and biomechanical properties were assessed. Results: OVX resulted in higher weight, visceral and bone marrow adiposity. Visceral adiposity correlated inversely with femur Ct.Th (r = −0.63, p < 0.001), BV/TV (r = −0.67, p < 0.001), Tb.N (r = −0.69, p < 0.001) and positively with Tb.Sp (r = 0.58, p < 0.001). Bone marrow adiposity also correlated with bone resorption (r = 0.47, p < 0.01), bone formation rate (r = −0.63, p < 0.01), BV/TV (r = −0.85, p < 0.001), Ct.Th (r = −0.51, p < 0.0.01), and with higher empty osteocyte lacunae (r = 0.39, p < 0.05), higher percentage of osteocytes with oxidative stress (r = 0.64, p < 0.0.01) and lower femur maximal stress (r = −0.58, p < 0.001). Physical activity correlated inversely with both visceral (r = −0.74, p < 0.01) and bone marrow adiposity (r = −0.92, p < 0.001). Conclusions: OVX increases visceral and bone marrow adiposity which are associated with inferior bone quality and biomechanical properties. Physical activity could contribute to reduce adipose tissue and thereby improve bone quality. Full article
(This article belongs to the Special Issue Impact of Physical Exercises on Bone Activities)
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12 pages, 14297 KiB  
Article
Effect of Various Types of Muscle Contraction with Different Running Conditions on Mouse Humerus Morphology
by Kaichi Ozone, Yuichiro Oka, Yuki Minegishi, Takuma Kano, Takanori Kokubun, Kenji Murata and Naohiko Kanemura
Life 2021, 11(4), 284; https://doi.org/10.3390/life11040284 - 27 Mar 2021
Cited by 3 | Viewed by 2083
Abstract
How various types of muscle contraction during exercises affect bone formation remains unclear. This study aimed to determine how exercises with different muscle contraction types affect bone morphology. In total, 20 mice were used and divided into four groups: Control, Level, Down Slow, [...] Read more.
How various types of muscle contraction during exercises affect bone formation remains unclear. This study aimed to determine how exercises with different muscle contraction types affect bone morphology. In total, 20 mice were used and divided into four groups: Control, Level, Down Slow, and Down. Different types of muscle contraction were induced by changing the running angle of the treadmill. After the intervention, micro-computed tomography (Micro-CT), tartrate-resistant acid phosphatase/alkaline phosphatase (ALP) staining, and immunohistochemical staining were used to analyze the humerus head, tendon-to-bone attachment, and humerus diaphyseal region. Micro-CT found that the volume ratio of the humeral head, the volume of the tendon-to-bone attachment region, and the area of the humeral diaphyseal region increased in the Down group. However, no difference was detected in bone morphology between the Level and Down Slow groups. In addition, histology showed activation of ALP in the subarticular subchondral region in the Down Slow and Down groups and the fibrocartilage region in the tendon-to-bone attachment. Moreover, Osterix increased predominantly in the Down Slow and Down groups.Overall bone morphological changes in the humerus occur only when overuse is added to EC-dominant activity. Furthermore, different type of muscle contractile activities might promote bone formation in a site-specific manner. Full article
(This article belongs to the Special Issue Impact of Physical Exercises on Bone Activities)
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16 pages, 2101 KiB  
Article
Preventive Moderate Continuous Running-Exercise Conditioning Improves the Healing of Non-Critical Size Bone Defects in Male Wistar Rats: A Pilot Study Using µCT
by Céline Bourzac, Morad Bensidhoum, Mathieu Manassero, Christine Chappard, Nicolas Michoux, Stéphane Pallu and Hugues Portier
Life 2020, 10(12), 308; https://doi.org/10.3390/life10120308 - 24 Nov 2020
Cited by 7 | Viewed by 2106
Abstract
Although physical exercise has unquestionable benefits on bone health, its effects on bone healing have been poorly investigated. This study evaluated the effects of preemptive moderate continuous running on the healing of non-critical sized bone defects in rats by µCT. We hypothesized that [...] Read more.
Although physical exercise has unquestionable benefits on bone health, its effects on bone healing have been poorly investigated. This study evaluated the effects of preemptive moderate continuous running on the healing of non-critical sized bone defects in rats by µCT. We hypothesized that a preemptive running exercise would quicken bone healing. Twenty 5-week-old, male, Wistar rats were randomly allocated to one of the following groups (n = 10): sedentary control (SED) or continuous running (EX, 45 min/d, 5 d/week at moderate speed, for 8 consecutive weeks). A 2 mm diameter bone defect was then performed in the right tibia and femur. No exercise was performed during a 4 week-convalescence. Healing-tissue trabecular microarchitectural parameters were assessed once a week for 4 weeks using µCT and plasma bone turnover markers measured at the end of the study protocol (time point T12). At T12, bone volume fraction (BV/TV; BV: bone volume, TV: tissue volume) of the healing tissue in tibiae and femurs from EX rats was higher compared to that in SED rats (p = 0.001). BV/TV in EX rats was also higher in tibiae than in femurs (p < 0.01). The bone mineral density of the healing tissue in femurs from EX rats was higher compared to that in femurs from SED rats (p < 0.03). N-terminal telopeptide of collagen type I in EX rats was decreased compared to SED rats (p < 0.05), while no differences were observed for alkaline phosphatase and parathyroid hormone. The study provides evidence that preemptive moderate continuous running improves the healing of non-critical sized bone defects in male Wistar rats. Full article
(This article belongs to the Special Issue Impact of Physical Exercises on Bone Activities)
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Review

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12 pages, 796 KiB  
Review
Physical Activity and Bone Vascularization: A Way to Explore in Bone Repair Context?
by Rkia Wazzani, Stéphane Pallu, Céline Bourzac, Saïd Ahmaïdi, Hugues Portier and Christelle Jaffré
Life 2021, 11(8), 783; https://doi.org/10.3390/life11080783 - 2 Aug 2021
Cited by 6 | Viewed by 3339
Abstract
Physical activity is widely recognized as a biotherapy by WHO in the fight and prevention of bone diseases such as osteoporosis. It reduces the risk of disabling fractures associated with many comorbidities, and whose repair is a major public health and economic issue. [...] Read more.
Physical activity is widely recognized as a biotherapy by WHO in the fight and prevention of bone diseases such as osteoporosis. It reduces the risk of disabling fractures associated with many comorbidities, and whose repair is a major public health and economic issue. Bone tissue is a dynamic supportive tissue that reshapes itself according to the mechanical stresses to which it is exposed. Physical exercise is recognized as a key factor for bone health. However, the effects of exercise on bone quality depend on exercise protocols, duration, intensity, and frequency. Today, the effects of different exercise modalities on capillary bone vascularization, bone blood flow, and bone angiogenesis remain poorly understood and unclear. As vascularization is an integral part of bone repair process, the analysis of the preventive and/or curative effects of physical exercise is currently very undeveloped. Angiogenesis–osteogenesis coupling may constitute a new way for understanding the role of physical activity, especially in fracturing or in the integration of bone biomaterials. Thus, this review aimed to clarify the link between physical activities, vascularization, and bone repair. Full article
(This article belongs to the Special Issue Impact of Physical Exercises on Bone Activities)
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40 pages, 695 KiB  
Review
The Specificities of Elite Female Athletes: A Multidisciplinary Approach
by Carole Castanier, Valérie Bougault, Caroline Teulier, Christelle Jaffré, Sandrine Schiano-Lomoriello, Nancy Vibarel-Rebot, Aude Villemain, Nathalie Rieth, Christine Le-Scanff, Corinne Buisson and Katia Collomp
Life 2021, 11(7), 622; https://doi.org/10.3390/life11070622 - 26 Jun 2021
Cited by 18 | Viewed by 6433
Abstract
Female athletes have garnered considerable attention in the last few years as more and more women participate in sports events. However, despite the well-known repercussions of female sex hormones, few studies have investigated the specificities of elite female athletes. In this review, we [...] Read more.
Female athletes have garnered considerable attention in the last few years as more and more women participate in sports events. However, despite the well-known repercussions of female sex hormones, few studies have investigated the specificities of elite female athletes. In this review, we present the current but still limited data on how normal menstrual phases, altered menstrual phases, and hormonal contraception affect both physical and cognitive performances in these elite athletes. To examine the implicated mechanisms, as well as the potential performances and health risks in this population, we then take a broader multidisciplinary approach and report on the causal/reciprocal relationships between hormonal status and mental and physical health in young (18–40 years) healthy females, both trained and untrained. We thus cover the research on both physiological and psychological variables, as well as on the Athlete Biological Passport used for anti-doping purposes. We consider the fairly frequent discrepancies and summarize the current knowledge in this new field of interest. Last, we conclude with some practical guidelines for eliciting improvements in physical and cognitive performance while minimizing the health risks for female athletes. Full article
(This article belongs to the Special Issue Impact of Physical Exercises on Bone Activities)
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11 pages, 288 KiB  
Review
Impact of Exercise Intensity on Calprotectin Levels in Healthy Volunteers and Patients with Inflammatory Rheumatic Diseases
by Andy Xavier and Annabelle Cesaro
Life 2021, 11(5), 377; https://doi.org/10.3390/life11050377 - 22 Apr 2021
Viewed by 2263
Abstract
Exercise influences inflammatory response and immune system performance. The regular practice of a moderate activity positively regulates immunity and the inflammatory process, while intensive training depresses it and enhances inflammatory marker secretion. Calprotectin is involved in the inflammatory process, promoting neutrophil recruitment, cell [...] Read more.
Exercise influences inflammatory response and immune system performance. The regular practice of a moderate activity positively regulates immunity and the inflammatory process, while intensive training depresses it and enhances inflammatory marker secretion. Calprotectin is involved in the inflammatory process, promoting neutrophil recruitment, cell degranulation, and inflammatory mediators. Furthermore, calprotectin has been associated with various inflammatory diseases, including inflammatory rheumatic diseases. The present review explores the effect of exercise on calprotectin levels in both healthy and inflammatory rheumatic conditions. Data show that the intensity duration and the type of exercise modulate calprotectin levels and participant inflammatory status. The exact role of calprotectin in the exercise response is yet unknown. Calprotectin could constitute an interesting biomarker for monitoring both the effect of exercise on the inflammatory process in healthy volunteers and the efficiency of exercise treatment programs in a patient with inflammatory rheumatic disease. Full article
(This article belongs to the Special Issue Impact of Physical Exercises on Bone Activities)
34 pages, 1799 KiB  
Review
Does Physical Exercise Always Improve Bone Quality in Rats?
by Hugues Portier, Delphine Benaitreau and Stéphane Pallu
Life 2020, 10(10), 217; https://doi.org/10.3390/life10100217 - 23 Sep 2020
Cited by 20 | Viewed by 3961
Abstract
For decades, the osteogenic effect from different physical activities on bone in rodents remained uncertain. This literature review presents for the first time the effects on five exercise models (treadmill running, wheel running, swimming, resistance training and vibration modes) in three different experimental [...] Read more.
For decades, the osteogenic effect from different physical activities on bone in rodents remained uncertain. This literature review presents for the first time the effects on five exercise models (treadmill running, wheel running, swimming, resistance training and vibration modes) in three different experimental rat groups (males, females, osteopenic) on bone quality. The bone parameters presented are bone mineral density, micro-architectural and mechanical properties, and osteoblast/osteocyte and osteoclast parameters. This review shows that physical activities have a positive effect (65% of the results) on bone status, but we clearly observed a difference amongst the different protocols. Even if treadmill running is the most used protocol, the resistance training constitutes the first exercise model in term of osteogenic effects (87% of the whole results obtained on this model). The less osteogenic model is the vibration mode procedure (31%). It clearly appears that the gender plays a role on the bone response to swimming and wheel running exercises. Besides, we did not observe negative results in the osteopenic population with impact training, wheel running and vibration activities. Moreover, about osteoblast/osteocyte parameters, we conclude that high impact and resistance exercise (such jumps and tower climbing) seems to increase bone formation more than running or aerobic exercise. Among the different protocols, literature has shown that the treadmill running procedure mainly induces osteogenic effects on the viability of the osteocyte lineage in both males and females or ovariectomized rats; running in voluntary wheels contributes to a negative effect on bone metabolism in older male models; whole-body vertical vibration is not an osteogenic exercise in female and ovariectomized rats; whereas swimming provides controversial results in female models. For osteoclast parameters only, running in a voluntary wheel for old males, the treadmill running program at high intensity in ovariectomized rats, and the swimming program in a specific ovariectomy condition have detrimental consequences. Full article
(This article belongs to the Special Issue Impact of Physical Exercises on Bone Activities)
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Other

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20 pages, 552 KiB  
Hypothesis
Does Compression Sensory Axonopathy in the Proximal Tibia Contribute to Noncontact Anterior Cruciate Ligament Injury in a Causative Way?—A New Theory for the Injury Mechanism
by Balázs Sonkodi, Rita Bardoni, László Hangody, Zsolt Radák and István Berkes
Life 2021, 11(5), 443; https://doi.org/10.3390/life11050443 - 14 May 2021
Cited by 16 | Viewed by 4981
Abstract
Anterior cruciate ligament injury occurs when the ligament fibers are stretched, partially torn, or completely torn. The authors propose a new injury mechanism for non-contact anterior cruciate ligament injury of the knee. Accordingly, non-contact anterior cruciate ligament injury could not happen without the [...] Read more.
Anterior cruciate ligament injury occurs when the ligament fibers are stretched, partially torn, or completely torn. The authors propose a new injury mechanism for non-contact anterior cruciate ligament injury of the knee. Accordingly, non-contact anterior cruciate ligament injury could not happen without the acute compression microinjury of the entrapped peripheral proprioceptive sensory axons of the proximal tibia. This would occur under an acute stress response when concomitant microcracks-fractures in the proximal tibia evolve due to the same excessive and repetitive compression forces. The primary damage may occur during eccentric contractions of the acceleration and deceleration moments of strenuous or unaccustomed fatiguing exercise bouts. This primary damage is suggested to be an acute compression/crush axonopathy of the proprioceptive sensory neurons in the proximal tibia. As a result, impaired proprioception could lead to injury of the anterior cruciate ligament as a secondary damage, which is suggested to occur during the deceleration phase. Elevated prostaglandin E2, nitric oxide and glutamate may have a critical neuro-modulatory role in the damage signaling in this dichotomous neuronal injury hypothesis that could lead to mechano-energetic failure, lesion and a cascade of inflammatory events. The presynaptic modulation of the primary sensory axons by the fatigued and microdamaged proprioceptive sensory fibers in the proximal tibia induces the activation of N-methyl-D-aspartate receptors in the dorsal horn of the spinal cord, through a process that could have long term relevance due to its contribution to synaptic plasticity. Luteinizing hormone, through interleukin-1β, stimulates the nerve growth factor-tropomyosin receptor kinase A axis in the ovarian cells and promotes tropomyosin receptor kinase A and nerve growth factor gene expression and prostaglandin E2 release. This luteinizing hormone induced mechanism could further elevate prostaglandin E2 in excess of the levels generated by osteocytes, due to mechanical stress during strenuous athletic moments in the pre-ovulatory phase. This may explain why non-contact anterior cruciate ligament injury is at least three-times more prevalent among female athletes. Full article
(This article belongs to the Special Issue Impact of Physical Exercises on Bone Activities)
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