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SCIENCE FRIDAY: BONE STRENGTH FOR ATHLETES BASICS; MUSCLE AS INFLUENCER

9/21/2018

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Weather on my mind in September. Taken by PKSenagore 2018. All rights reserrved.
BECAUSE THE EARNED RUNS PAGE “BONE STRENGTH FOR ATHLETES” will attempt to post scientific information about maintaining and possibly improving bone health in athletes, it seemed like a good idea to start building it on a foundation of basic information. The Science Friday blog is a perfect “venue” on which to post science-heavy articles.
 
An article, “Bone Biomechanical Properties and Changes with Osteoporosis” may be one such basic learning resource.  It describes the nature of normal bone and begins to discuss what is known to change with bone loss, as occurs with osteoporosis.   It is summarized below in Part I. Be aware that, to not misrepresent what was written in the article, a good portion of the summary is lifted word for word by Earned Runs. You are encouraged to read the entire paper.
 
However, this one piece doesn’t fully explain how bone strength is determined or measured. Another basic article “Mechanical basis of bone strength: influence of bone material, bone structure and muscle action” reviews other fundamentals.  It is quite lengthy and detailed. 

Earned Runs is hoping to acquire knowledge of the science of bone health so as to better understand additional literature that applies specifically to athletes, thus, much of the summary quotes the article directly but arranges it in outline form.
 
Exact wording is maintained to avoid inadvertent change in meaning. These articles may be frequently referenced as other materials are discussed or posted on the BONE STRENGTH FOR ATHLETES  page.  Earned Runs tried its best to present the information in the articles to this post,but understanding will be greatly improved by reading the original source articles too.
 
Because of the length of the discussion, the remainder of this post can be read (click "Read More") below, or the PDFs of Part I and Part II can be downloaded by clicking on the titles. 
 
Discussion: Part I: “BONE BIOMECHANICAL PROPERTIES AND CHANGES WITH OSTEOPOROSIS”
By Georg Osterhoff, Elise F. Morgan, Sandra J. Shefelbine, Lamya Karim, Laoise M. McNamara, and Peter Augatg
Article: Injury. 2016 June; 47(Suppl 2): S11–S20. doi:10.1016/S0020-1383(16)47003-8. 
 
Discussion Part II: “MECHANICAL BASIS OF BONE STRENGTH: INFLUENCE OF BONE MATERIAL, BONE STRUCTURE AND MUSCLE ACTION”
by N.H. Hart, S. Nimphius, T. Rantalainen, A. Ireland, A. Siafarikas R.U. Newton
Article: J Musculoskelet Neuronal Interact 2017; 17(3):114-139

I. “BONE BIOMECHANICAL PROPERTIES AND CHANGES WITH OSTEOPOROSIS” “BONE BIOMECHANICAL PROPERTIES AND CHANGES WITH OSTEOPOROSIS”
By Georg Osterhoff, Elise F. Morgan, Sandra J. Shefelbine, Lamya Karim, Laoise M. McNamara, and Peter Augatg
Article: Injury. 2016 June; 47(Suppl 2): S11–S20. doi:10.1016/S0020-1383(16)47003-8. 
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4955555/pdf/nihms803093.pdf

Mature bone tissue is classified as two types: trabecular [also known as spongy] and cortical [also known as compact].  Cortical type bone forms the dense, outer shell that surrounds the inner core of honeycomb-like, trabecular type bone.  Blood vessels deliver nourishment to cortical bone; trabecular bone receives nutrients by diffusion from the inner bone marrow. While all trabecular bone is surrounded by cortical bone, the thickness of the cortex differs by location.  The ratio of cortical: trabecular bone is higher in long bones like the shaft of the femur, and is lower in vertebral body bones.
 
Bone micro-structure and composition are determined by location in the body and the forces acting on it.  Biomechanical strength is related to density and to the connectivity between trabecular network structures, which are influenced by loading pressures, both compressive and tensile.
 
 “For example, vertebral bodies must resist high and repetitive axial compression loads but experience much less shear or tension loads.” If the trabecular component of these bones is removed, their ability to withstand compressive forces is disproportionately reduced.
 
“The femoral neck [of the hip] or the proximal humerus [of the arm], on the other hand, is mainly subjected to shear forces and bending moments, the latter of which create a combination of compression, tension, and shear”. Any reduction in cortical thickness or shape, increases the risk of hip or arm fracture, whereas removal of the trabecular component in these locations has little effect on biomechanical strength.
 
Bone loss in early osteoporosis is mainly a trabecular bone loss. With increasing age [later stages of bone loss] the cortical bone becomes more and more porous.
 
“The transition from early trabecular to later cortical bone loss is consistent with the epidemiological [population] data on osteoporotic fractures. Vertebral compression fractures, being “trabecular fractures”, are more common in individuals aged less than 65 years. With increasing cortical bone loss after the age of 65 years, hip fractures, being rather “cortical fractures”, become more frequent.
 
The heterogeneity [the opposite of being homogeneous; a material that is homogeneous is uniform in composition or character (i.e. shape, size, weight, height, distribution, texture, architectural design, etc.); one that is heterogeneous is distinctly non-uniform in one of these qualities]  in density and architecture throughout bones such as the femur and vertebra have been proposed as a major reason why the average BMD [bone mineral density] of a bone explains only ~60% of the variation in whole-bone strength. 
 
Biomechanical studies show that bone heterogeneity is important for mechanical strength.
  • Femur: an increase in bone density in a fairly small region at the “neck” could produce a relatively greater increase in bone strength as compared to a uniform increase throughout the entire bone.
  • Vertebrae: compressive failure of the vertebra was predicted better by measures of density from one or several sub-regions of the center of the body as compared to average density of the entire central area.
    • Bones with a high prevalence of osteoporotic fracture tend to contain large amounts of heterogeneity in density and microstructure throughout the trabecular compartment.

THE MATRIX [substance] OF BONE is composed of both inorganic (i.e. mineral) and organic (i.e. water, collagen protein, and non-collagenous proteins) components
  • INORGANIC mineral content: known to provide strength and stiffness
  • ORGANIC collagen and non-collagen protein content: changes in protein (content and structure) play important roles in age- and disease-related alteration in bone. The organic matrix is thought to be responsible for bone’s ductility (ability to undergo significant “plastic” deformation before rupture) and its ability to absorb energy prior to fracturing.
 
ORGANIC MATRIX: COLLAGEN AND NON-COLLAGEN PROTEIN
 
There is increasing evidence that the bone’s organic matrix plays a role in age- and disease-related changes in its mechanical properties.
 
Collagen protein:
  • enzymatic crosslinking of collagen is generally considered to be healthy and have a positive effect on bone’s mechanical properties
  • non-enzymatic crosslinking occurs as a result of aging and with some diseases;  it can lead to deteriorated bone mechanical properties.
 
Non-collagenous proteins play a role in preventing harmful micro-damage.
 
Though osteoporosis is generally defined as a loss of bone mass (a type of quantity), there are considerable matrix changes, particularly in collagen crosslinks, which cause a loss of bone quality. 
 
[COLLAGEN PROTEIN MATRIX details]

Collagen undergoes numerous modifications with aging and disease, including both enzymatic and non-enzymatic crosslinking. 

  • Enzymatic crosslinking: links the ends of the collagen molecules; considered to be a normal process for healthy collagen and has a beneficial effect on its mechanical properties,
  • Non-enzymatic crosslinking: links are found at any position along the collagen, within and across collagen fibers; results in a brittle collagen network that leads to deteriorated bone mechanical properties if its accumulation exceeds normal repair.
    • Products of non-enzymatic cross-linking are known as advanced glycation end-products (AGEs)
    • AGEs accumulate with age and disease in numerous body tissues including skin, cartilage, tendons, and bone. 
    • Increased AGEs levels can result in brittleness of tissues; accumulated AGEs stiffen bone’s collagen matrix
    • Osteoporotic bone has significantly more AGEs than normal healthy bone  
    • Research study findings don’t all tell the same story though, possibly because of differences in methods used to study bone. Thus, the exact contribution of AGEs to age-related skeletal fragility remains undefined.
    • Receptors on the surface of many cell types interact with AGEs, and are referred to as RAGEs.  RAGEs are activated when AGEs bind to them, which can lead to inflammation, abnormal cell function, and localized tissue destruction.
    • In bone, the interaction of AGEs with RAGEs receptors (activation) inhibits the proliferation and differentiation (a type of maturation) of osteoblasts (bone building cells), reduces matrix production, reduces bone formation, and increases osteoblast apoptosis (programmed “cell suicide”)
 
[NON-COLLAGEN MATRIX details]
Non-collagen proteins comprise 10% of bone’s organic matrix; 2 of these proteins are:
  • Osteocalcin stimulates mineral maturation, inhibits bone formation, recruits precursor osteoclasts (bone destroying cells) to bone resorption sites and helps with their differentiation into mature osteoclasts
  • Osteopontin plays a role in mineralization and assists in bone resorption (destruction) by anchoring osteoclasts to the mineral matrix of the bone surface
 
ORGANIC MATRIX SUMMARY:
The ‘normal’ type of collagen crosslinking helps maintain healthy bone. The abnormal type of collagen crosslinking that is associated with aging and some diseases likely causes bone brittleness, interferes with normal maintenance and repair processes, and leads to the decreased bone formation of osteoporosis.
 
Non-collagen matrix proteins act as the glue that holds mineralized collagen fibers together. When a force is applied, these components stretch, help dissipate energy by breaking sacrificial bonds between adjacent collagen fibrils, and prevent harmful crack formation and propagation
  • Increased serum osteocalcin and osteopontin has been reported in postmenopausal women with osteoporosis compared to healthy controls 
 
Article Summary:
 
“The bone’s inorganic and organic composition, its trabecular and cortical nano-, micro-, and macroscopic architecture, and the heterogeneity of these structural features all have impact on age- and disease-related changes in bone’s mechanical properties. Though osteoporosis is generally defined as a loss of bone mass, there are considerable changes of the structure and matrix itself, which can cause a loss of bone quality...."
 
[Read the remainder of this section in the original article].
 
II. “MECHANICAL BASIS OF BONE STRENGTH: INFLUENCE OF BONE MATERIAL, BONE STRUCTURE AND MUSCLE ACTION”
by N.H. Hart, S. Nimphius, T. Rantalainen, A. Ireland, A. Siafarikas R.U. Newton
J Musculoskelet Neuronal Interact 2017; 17(3):114-139
 
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5601257/
 
SOME KEY POINTS [material in brackets has been modified or added by Earned Runs]:
 
“Accrual of bone takes place most rapidly in the teenage years, culminating in the third decade of life to achieve peak bone mass.”
 
“Bone strength …. Is modulated by neighboring muscle as a key osteogenic [bone building] stimulant and modifier of mechanical behavior”
 
 “…bone cells are responsive to local strains expressed in their precise vicinity by routine stresses supplied by activities of daily living…”
 
“… therefore, the determinants of bone adaptation in response to mechanical load involve all aspects of the strain environment” [including strain magnitude, rate, frequency, and distribution, and the number of loading cycles and rest-recovery periods]
 
“… all components of the strain environment are interlinked and interdependent, such that they collectively contribute to the osteogenic effect and potency of mechanical loading”
 
MECHANICAL BEHAVIOR [OF BONE]
“… Bone is structurally complex and hierarchically designed, with diverse arrangements and various layers of biomaterial working co-operatively to meet numerous paradoxical requirements.”
 
“… bones behave and respond uniquely to various loading modalities of differing magnitudes, directions, rates and frequencies. While this relationship between mechanical load and mechanical behaviour is multifactorial; bone strength and stiffness are greatest in the direction where loads are most commonly expressed”
 
 “…bone widens under compression and narrows under tension…”
 
MINERAL CONTRIBUTION [TO BONE STRENGTH]
“Bones are bi-phasic composite materials, with organic and inorganic components. The interplay between these materials and their relative composition considerably influences
mechanical behaviour and bone strength. Specifically, the degree of mineralisation and porosity (i.e.: apparent density) ultimately determines the quality of bone material, and … [its] ultimate strength.

  • “Mineralisation refers to the deposition [primary phase] and maturation [secondary phase] of mineral content within bone…”
 
  • “Sequentially, newly deposited bone begins to rapidly mineralise within ~5 to 10 days of creation, generating ~60% of its total mineral content… gradually advancing toward complete maturation and calcification… within ~30 months of initial deposition.”
 
  • “...If mineralisation and crystallinity are too high, bone may become excessively stiff and brittle”
 
  • “...If mineralisation and crystallinity are too low, bone may become fragile and weak”
 
  • “…thus, a presently undefined, yet evidently optimal ratio of organic-to-inorganic material [is associated] with bone strength and mechanical competence.”
 
  • “Porosity represents the prevalence, magnitude and distribution of pores within the bone matrix, which characteristically differs between macroscopic tissues” [cortical versus trabecular bone types].
    • [Trabecular bone ~50 to 90% porous]: “porosity is a prominent and purposeful architectural feature”
    • [Cortical bone ~5 to 10% porous]: porosity is “minimal in quantity and size under normal circumstances”
 
  • “The functional merit of porosity in trabecular and cortical bone is provided at the expense of strength, with small increases in porosity equating to disproportionately large decreases in bone mass and density,  the major clinical feature of bone degeneration from ageing, disuse or disease.”
  •  “Trabecular bone is rapidly affected by increased porosity; resulting in progressively thinner, disconnected and separated trabeculae”
  •  [Cortical bone weakening] “is also predominated by increased porosity, resulting in loss of stiffness and reduced load tolerability”
  • “... [increased porosity] of trabecular and cortical bone rapidly compromises mechanical integrity, accounting for ~90% and ~75% of strength loss during ageing respectively.
 
“Density is the product of mineralisation and porosity, expressed as mass per unit of volume. Specifically, the amount of mineral content per volume of bone [mineralization], and its ratio of void volume to total volume [porosity] respectively combine to establish apparent bone mineral density.
 
“Bone mineral density (BMD) [traditionally areal BMD] is a frequently used surrogate measure of mechanical competence and bone strength [bone quality] …”
-           to establish fracture risk;
-           to diagnose osteopenia and osteoporosis
-           to quantify interventional efficacy of preventative and remedial programs.
 
[However] “all measures of bone mineral density [BMD] inherently neglect structural properties of bone [architecture, morphology, geometry], which substantially influences mechanical behaviour, and greatly contributes to bone strength and fatigue resistance.”
…”it is only one of several determinants of bone and should therefore form part of a wider investigative framework which includes structural quantities”.
 
STRUCTURAL CONTRIBUTION [TO BONE STRENGTH]
 “Bone has unique …properties which specifically and functionally adapt to routine mechanical loads in order to enhance bone strength and stiffness in the absence of increased bone mass.”
  • [bone] modifies its structure by adjusting its size (thickness and diameter), shape (contour and dimensions) and architecture (alignment and distribution) …”
 
 MUSCULAR CONTRIBUTION [TO BONE STRENGTH] [Note: important to athletes!!!]
“Muscle and bone are inextricably linked by anatomical, mechanical, metabolic, and pleiotropic [more than one effect of a gene] functions. 
  • Anatomically, muscle transforms and mobilises skeletal segments into an interlinked system of levers via tendinous junctions.
  • “Mechanically, muscle exerts contractile forces onto the skeleton in order to effectuate movement,”; [muscle supplants gravity as a being a more important stimulant of bone].
  • “Metabolically”, [hormone signaling between muscle and bone allows] “release of secretory factors capable of modulating each other (muscle to bone; bone to muscle), nearby tissues, and distant organs.”  
  • “Pleiotropically, muscle and bone share several “[genetically determined] “traits, responsive to the same genetic influences and pathways, which if altered, cooperatively contribute to the development of sarcopenia [muscle loss] and osteopenia [bone loss] simultaneously, and may explain co-adaptive anabolic [tissue building] and catabolic [tissue breakdown] responses to [the presence or absence of a] mechanical stimulus.”
 
  • “Adaptation of muscle and bone are interdependent; such that alterations in muscle size, density and strength are linked [in a timely manner] and positively correlated with alterations in bone size, density and strength.”
  • “…when immobilised; muscle cross-sectional area, volume and strength significantly reduces after ~5 to 7 days; whereas bone thickness, volume and strength significantly reduces after ~14 to 21 days.
  • “…when mechanically loaded, muscle cross-sectional area, length and strength significantly increases after ~20 days; whereas bone diameter, thickness and volume significantly increases after ~40 to 80 days”  
    • “The time-course of adaptation is such that genomic and metabolic alterations occur rapidly”, [before tissue changes are observed]  
    • Muscle changes precede bone changes (~3:1 to 4:1)
    • Losses of muscle/bone occur more rapidly than accrual (~3:1 to 4:1)
      • exercise-induced long-term gains are rapidly reversed and gradually recovered [!!!]
Muscle is a potent osteogenic stimulant
  • Muscle asserts synergistic dominance over bone, such that bone growth     or loss is subservient to muscle hypertrophy or atrophy            
  • Muscle and bone [co-adapt] together in response to anabolic or catabolic stimuli; highlighting the importance of muscle size and strength as trainable features to enhance and protect bone size and strength.
 
“Beyond its osteogenic capabilities, muscle...
  • “acts to mechanically alter the distribution of stress applied to bone
  • [secretes substances (myokines) that allow muscle and bone to "cross-talk"]

[The section below seems to be indicating that, because muscle interacts with and influences bone in so many different ways, when muscle fatigue sets in the quality and efficiency of body movement is diminished.  This inferior form of movement makes the skeleton (bone) vulnerable to injury. Either leading to trauma (fracture) or tissue alterations associated with overuse.  Recovery periods are therefore important with strenuous weight training designed to build or strengthen muscle]

"Bone mass, material and structure interact with muscle to determine the resultant mechanical behavior and load tolerability of bone to a given loading environment.
  • “… the interplay between loading magnitude and repetition generates a level of musculoskeletal fatigue and structural vulnerability which, in the absence of suitable rest and recovery, will eventuate in traumatic or overuse injury."
  •  “… movement quality and efficiency becomes compromised as muscle fatigues, resulting in an altered gait; reduced shock absorption; irregular loading; and abnormal stress distribution, such that higher rates and magnitudes of force undesirably transmit direct to the skeleton”
  • "In the absence of recovery following strenuous activity, accumulative bone fatigue; micro-damage; and eventual bone failure eventuates, highlighting the importance of inserting rest periods within mechanical loading programs designed to promote growth or prevent Injury

[The remainder of the article  future directions in research; please read the original article to enjoy the prespective provided by the authors]

If there is ONE message that athletes might take from this post, its that bone health is remarkable influenced by muscle, and that changes in muscle will effect it. On the favorable side as well as the favorable side.  There's more to bone than just it's mineral content, as currently measured by bone mineral content (BMD).

RUN & MOVE HAPPY!

PS: after this whopper of a post you might be yearning for the lighter  "summer" version of Science Friday!
 
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4955555/pdf/nihms803093.pdf
 
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4955555/
 
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5601257/
 
https://www.ncbi.nlm.nih.gov/pubmedhealth/PMHT0022808/ (bone types)
 
https://www.livescience.com/12949-cell-suicide-apoptosis-nih.html
 

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