The Utah paradigm of skeletal physiology: what is it?

Summary

An elegant design stratagem for an organ intended to carry loads for life without fracturing, rupturing or wearing out would make those loads determine the organ's strength. It seems load-bearing mammalian bones, joints, fascia, ligaments and tendons do exactly that. Physiologists begin to understand how they do it, and that led to the Utah paradigm of skeletal physiology. Those adaptations occur in two major steps. The first step creates the genetically predetermined newborn skeleton with its anatomical relationships and biologic machinery. The second step adds to the first one all postnatal adaptations to mechanical and other challenges that would affect an organ's strength, size, architecture and composition. During postnatal growth, increasing loads make tissue-level biologic mechanisms correspondingly increase the strength of such organs. Mechanical strain-dependent signals help to control that process, which muscle strength, muscle anatomy and neuromuscular physiology strongly influence. Its problems seem to cause or help to cause numerous skeletal and some extraskeletal disorders. A Table in the article lists examples of them.

This article summarizes salient features of the Utah paradigm, which includes both facts and some meanings inferred from them. Other times and people must resolve any questions about those meanings and about the devils that can lie in the details. Parenthetically, instead of the accuracy of the facts on which that paradigm stands, the above questions usually concern the different meanings people can infer from facts, and whether particular facts and ideas would be relevant to a particular issue.

Keywords

Biomechanics - bone - joints - tendons - ligaments - physiology

• REFERENCES

• 1 Adams ME, Billingham MEJ. Animal models of degenerative joint disease. In: Bone and Joint Disease. Berry CL. ed. Springer-Verlag; Berlin: 1982: 265-98.
• 2 Aegerter E, Kirkpatrick JA. Orthopaedic Diseases. WB Saunders Co; Philadelphia: 1958
• 3 Alexander McNR. Optimum strength for bones liable to fatigue and accidental failure. J Theor Biol 1984; 109: 621-36.
• 4 Bilezikian JP, Raisz LG, Rodan GA. Principles of Bone Biology. Academic Press; Orlando, FL: 1996
• 5 Burr DB, Martin RB. Mechanisms of bone adaptation to the mechanical environment. Triangle (Sandoz) 1992; 31: 59-76.
• 6 Burr DB. Remodeling and the repair of fatigue damage. Calc Tiss Int 1993; 53 (Suppl. 01) 75-81.
• 7 Burr DB. Muscle strength, bone mass, and age-related bone loss. J Bone Miner Res 1997; 12: 1547-51.
• 8 Burr DB. Microdamage in bone. Curr Opin Orthoped 1997; 08: 8-14.
• 9 Dietz FR, Mathews KD. Update on the genetic bases of disorders with orthopaedic manifestations. J Bone Jt Surg 1996; 78A: 1583-98.
• 10 Evans RA. Is there a need for whole body physiology?. Bone and Min 1987; 02: 243-4.
• 11 Eyre DR. Collagen structure and function in articular cartilage. In: Osteoarthritic Disorders. Kuettner KE, Goldberg VM. (Eds). Amer Acad Orthop Surg; 1995: 219-28.
• 12 Ferretti JL. Peripheral, quantitative computed tomography (pQCT) for evaluating structural and mechanical properties of small bone. In: Practical Guide for Mechanical Testing of Bone. YH An, Draughn RA. (Eds). CRC Press; Boca Raton, FL: 1999: 1-25.
• 13 Frost HM. The origin and nature of transients in human bone remodeling dynamics. In: Clinical Aspects of Metabolic Bone Disease. Duncan H, Frame B, Parfitt AM. (Eds). Excerpta Medica; Amsterdam: 1973: 124-37.
• 14 Frost HM. The biology of fracture healing. Clin Orthop Rel Res 1989; Part I: 248: 283-93. Part II: 248: 294-309.
• 15 Frost HM. Pathogenesis of congenital hip dysplasia (CDH). A proposal. Vet Comp Orthop Trauma 1989; 01: 1-10.
• 16 Frost HM. Structural adaptations to mechanical usage (SATMU): 1. Redefining Wolff’s Law: The bone modeling problem. Anat Rec 1990; 226: 403-13.
• 17 Frost HM. Structural adaptations to mechanical usage (SATMU): 2. Redefining Wolff’s Law: The bone remodeling problem. Anat Rec 1990; 226: 414-22.
• 18 Frost HM. Structural adaptations to mechanical usage (SATMU): 3. The hyaline cartilage modeling problem. Anat Rec 1990; 226: 423-32.
• 19 Frost HM. Structural adaptations to mechanical usage (SATMU): 4. Mechanical influences on fibrous tissues. Anat Rec 1990; 226: 433-9.
• 20 Frost HM. Perspectives: A proposed general model for the mechanostat (suggestions from a new paradigm). Anat Rec 1996; 244: 139-47.
• 21 Frost HM. On rho, a marrow mediator and estrogen: Their roles in bone strength and “mass” in human females, osteopenias and osteoporoses (insights from a new paradigm). J Bone Miner Metab 1998; 16: 113-23.
• 22 Frost HM. Osteoporoses: New Concepts and Some Implications for Future Diagnosis, Treatment and Research (based on insights from the Utah paradigm). Ernst Schering Research Foundation AG; 1998: 7-57.
• 24 Frost HM. The Utah paradigm of skeletal physiology: An overview of its insights for bone, cartilage and collagenous tissue organs. J Bone Miner Metab 2000; 18: 305-16.
• 25 Frost HM. Does bone design intend to minimize fatigue failures? A case for the affirmative. J Bone Miner Metab 2000; 18: 278-62.
• 26 Frost HM. The Frozen shoulder syndrome plus clinical-pathologic evidence and insights of the Utah paradigm suggest new targets for collagenous tissue research, as well as that syndrome’s pathogenesis. J Neuromusc and Neuronal Interactions 2001; 01: 113-9.
• 27 Frost HM. From Wolff’s Law to the Utah paradigm. Anat Rec 2001; 262: 398-419.
• 28 Gingrich N. An opportunities-based science budget. Science 2000; 290: 1303.
• 29 Gorski J. Do we need new paradigms?. Endocrine News 1997; 22: 4 12.
• 30 Heaney RP. The bone-remodeling transient: Implications for the interpretation of clinical studies of bone mass change. J Bone and Min Res 1994; 09: 1515-23.
• 31 Jee WSS. Hard Tissue Workshops organized annually since 1965 by Prof. Jee provided a uniquely seminal, multidisciplinary forum for presenting and discussing new methods, evidence and ideas about human skeletal disorders. The University of Utah sponsored them and hundreds of international authorities and fellows in many disciplines attended them. They probably affected how people think about and study skeletal physiology and disorders more than any other meetings in this century. The Utah paradigm had its genesis at these Workshops; hence its name.
• 32 Jee WSS. Proceedings of the International Conference on Animal Models in the Prevention and Treatment of Osteopenia). Bone 1995; 17 (Suppl): 1-466.
• 33 Jee WSS. The interactions of muscles and skeletal tissue. In: Musculoskeletal Interactions. Vol II. Lyritis GP. (Ed). Hylonome Editions; Athens: 1999: 35-46.
• 34 Jee WS. Principles in bone physiology. J Musculoskeletal Interactions 2000; 01: 9-11.
• 35 Jensen OT. The Sinus Bone Graft). Quintessence Publishing Co, Carol Stream; IL: 1998
• 36 Jiang Y, Zhao J, Rosen C, Gensens P, Genant H. Perspectives on bone mechanical properties and adaptive response to mechanical loading. J Clin Densitom 1999; 02: 422-33.
• 37 Kippel JH, Dieppe PA. Rheumatology). Mosby-Year Book. Inc; 1994
• 38 Kuhlencordt F, Bartelheimer H. Hand-buch der Inneren Medizin. Vol VI). Springer-Verlag; Heidelberg: 1981
• 39 Lewis FT. Stohr’s Histology). (6th U.S. ed). P Blakiston’s Son and Co; Philadelphia: 1906
• 40 Martin RB, Burr DB, Sharkey NA. Skeletal Tissue Mechanics. Springer-Verlag; New York: 1998
• 41 Martin RB. Towards a unifying theory of bone remodeling. Bone 2000; 26: 1-6.
• 42 Mayr E. Cause and effect in biology. Science 1961; 134: 1501-6.
• 43 McLean FC, Urist MR. Bone (2nd ed). University of Chicago Press; Chicago: 1961
• 44 Muir H. A molecular approach to the understanding of osteoarthritis. Ann Rheum Dis 1985; 36: 199-208.
• 45 Nimni ME. Collagen. Biochemistry, Biomechanics, Biotechnology). CRC Press; Boca Raton: 1988
• 46 Ogden JA, Grogan DP. Postnatal development and growth of the musculoskeletal system. In: The Scientific Basis of Orthopaedics. 2nd Ed. Albright JA, Brand RA. (eds). Appleton and Lange; Norwalk: 1987: 91-160.
• 47 Parfitt AM. Osteoporosis: 50 years of change, mostly in the right direction. In: Osteoporosis and Bone Biology. Compston J, Ralston S. (Eds). International Medical Press; 2000: 1-13.
• 48 Polanyi M. Life’s irreducible structure. Science 1968; 160: 1308-12.
• 49 Putschar WGJ. General pathology of the musculoskeletal system. In: Handbuch der Allgemeinen Pathologie. Buchner F, Letterer E, Roulet F. eds. Springer-Verlag; Berlin: 1960: 361-488.
• 50 Schonau E. Paediatric Osteology. New Trends and Diagnostic Possibilities). Elsevier Science; Amsterdam: 1996
• 51 Schönau E, Westermann F, Mokow E, Scheidhauer K, Werhahn E, Stabrey A, Müller-Berghaus J. The functional muscle-bone-unit in health and disease. In: Paediatric Osteology. Prevention of Osteoporosis - a Paediatric Task?. Schonau E, Matkovic V. (Eds). Excerpta Medica; Amsterdam: 1998: 191-202.
• 52 Snapper I. Bone Disease in Medical Practice. Grune and Stratton; New York: 1957
• 53 Takahashi HE. Spinal Disorders in Growth and Aging). Springer-Verlag; Tokyo: 1995
• 54 Takahashi HE. Mechanical Loading of Bones and Joints). Springer-Verlag; Tokyo: 1999
• 55 Wiener N. Cybernetics. MIT Press; Cambridge: 1964
• 56 Weinmann JP, Sicher H. Bone and Bones. 2nd Ed. CV Mosby Co; St Louis: 1955
• 57 Woodard JC. Morphology of fracture nonunion and osteomyelitis. Vet Clin N Amer 1991; 21: 813-44.