Analyze Diet

Krogh’s principle for musculoskeletal physiology and pathology.

Abstract: August Krogh was a comparative physiologist who used frogs, guinea pigs, cats, dogs, and horses in his research that led to his Nobel Prize on muscle physiology. His idea to choose the most relevant organism to study problems in physiology has become known as Krogh's principle. Indeed, many important discoveries in physiology have been made using naturally occurring animal models. However, the majority of research today utilizes laboratory mouse and rat models to study problems in physiology. This paper discusses how Krogh's principle can be invoked in musculoskeletal research as a complementary approach to using standard laboratory rodent models for solving problems in musculoskeletal physiology. This approach may increase our ability to treat musculoskeletal diseases clinically. For example, it has been noted that progress in osteogenesis imperfecta research has been limited by the absence of a naturally occurring animal model. Several examples of naturally occurring animal models are discussed including osteoarthritis and osteosarcoma in dogs, resistance to disuse induced bone and skeletal muscle loss in mammalian hibernators, and bone phenotypic plasticity in fish lacking osteocytes. Many musculoskeletal diseases (e.g., osteoarthritis) occur naturally in companion animals, which may provide clues on etiology and progression of musculoskeletal diseases and accelerate the development of pharmaceutical therapies for humans.
Publication Date: 2018-09-05 PubMed ID: 30179205PubMed Central: PMC6146200
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • U.S. Gov't
  • Non-P.H.S.

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research article explores the application of Krogh’s principle – the choice of the most suitable organism for the study of a particular physiological issue – in the field of musculoskeletal research. The authors discuss how this approach can complement the prevailing use of lab rodents and potentially enhance the process of discovering treatment for musculoskeletal diseases.

Understanding Krogh’s Principle

  • The principle was established by August Krogh, a notable comparative physiologist, known for his work involving a variety of animals including cats, dogs, and horses.
  • The principle suggests that for every physiological problem, there is an organism best suited to its study. The objective is to choose the most relevant organism to study specific problems in physiology.
  • Over the years, Krogh’s principle has facilitated several important discoveries in the realm of physiology, specifically through the use of naturally occurring animal models.

Application in Musculoskeletal Physiology and Pathology

  • The paper propositions how Krogh’s principle can be leveraged in musculoskeletal research, offering a fresh approach to using standardized lab rodent models for solving problems in musculoskeletal physiology.
  • This innovative approach could potentially amplify our capacity for discovering clinical treatments for various musculoskeletal diseases.

Naturally Occurring Animal Models and Disease Study

  • The authors refer to the limited progress in research on Osteogenesis Imperfecta due to the lack of a naturally occurring animal model. This reference demonstrates the importance of using the right organism in understanding specific health conditions.
  • Examples of naturally occurring animal models for musculoskeletal issues include the occurrence of osteoarthritis and osteosarcoma in dogs, mammalian hibernators’ resistance to disuse-induced bone and skeletal muscle loss, and bone phenotypic plasticity in osteocyte-lacking fish.
  • These models emphasize that many musculoskeletal diseases that humans suffer from (such as osteoarthritis) also occur naturally in animals. Studying these cases can provide crucial insights into the origin and progression of musculoskeletal diseases and can fast-track the development of pharmaceutical therapies for human patients.

Cite This Article

APA
Donahue SW. (2018). Krogh’s principle for musculoskeletal physiology and pathology. J Musculoskelet Neuronal Interact, 18(3), 284-291.

Publication

ISSN: 1108-7161
NlmUniqueID: 101084496
Country: Greece
Language: English
Volume: 18
Issue: 3
Pages: 284-291

Researcher Affiliations

Donahue, Seth W
  • Department of Biomedical Engineering, University of Massachusetts, USA.

MeSH Terms

  • Adaptation, Physiological / physiology
  • Animals
  • Bone and Bones / physiology
  • Cartilage, Articular / physiology
  • Muscle, Skeletal / physiology
  • Musculoskeletal Physiological Phenomena

Conflict of Interest Statement

The authors have no conflict of interest.

References

This article includes 96 references
  1. Zimmer HG. August Krogh.. Clin Cardiol 2006 May;29(5):231-3.
    pmc: PMC6653951pubmed: 16739398doi: 10.1002/clc.4960290514google scholar: lookup
  2. Krogh A. THE PROGRESS OF PHYSIOLOGY.. Science 1929 Aug 30;70(1809):200-4.
    pubmed: 17732865doi: 10.1126/science.70.1809.200google scholar: lookup
  3. Krebs HA. The August Krogh Principle: "For many problems there is an animal on which it can be most conveniently studied".. J Exp Zool 1975 Oct;194(1):221-6.
    pubmed: 811756doi: 10.1002/jez.1401940115google scholar: lookup
  4. Shapiro JR, Mcbride DJ Jr, Fedarko NS. OIM and related animal models of osteogenesis imperfecta.. Connect Tissue Res 1995;31(4):265-8.
    pubmed: 15612365doi: 10.3109/03008209509010820google scholar: lookup
  5. Lindert U, Weis MA, Rai J, Seeliger F, Hausser I, Leeb T, Eyre D, Rohrbach M, Giunta C. Molecular Consequences of the SERPINH1/HSP47 Mutation in the Dachshund Natural Model of Osteogenesis Imperfecta.. J Biol Chem 2015 Jul 17;290(29):17679-17689.
    pmc: PMC4505018pubmed: 26004778doi: 10.1074/jbc.m115.661025google scholar: lookup
  6. Doherty AH, Ghalambor CK, Donahue SW. Evolutionary physiology of bone: bone metabolism in changing environments.. Physiology (Bethesda) 2015 Jan;30(1):17-29.
    pubmed: 25559152doi: 10.1152/physiol.00022.2014google scholar: lookup
  7. Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, Shen J, Vinson C, Rueger JM, Karsenty G. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass.. Cell 2000 Jan 21;100(2):197-207.
    pubmed: 10660043doi: 10.1016/s0092-8674(00)81558-5google scholar: lookup
  8. Bendele A. Animal models of rheumatoid arthritis.. J Musculoskelet Neuronal Interact 2001 Jun;1(4):377-85.
    pubmed: 15758488
  9. Jee WS, Yao W. Overview: animal models of osteopenia and osteoporosis.. J Musculoskelet Neuronal Interact 2001 Mar;1(3):193-207.
    pubmed: 15758493
  10. Lelovas PP, Xanthos TT, Thoma SE, Lyritis GP, Dontas IA. The laboratory rat as an animal model for osteoporosis research.. Comp Med 2008 Oct;58(5):424-30.
    pmc: PMC2707131pubmed: 19004367
  11. Martin B, Ji S, Maudsley S, Mattson MP. "Control" laboratory rodents are metabolically morbid: why it matters.. Proc Natl Acad Sci U S A 2010 Apr 6;107(14):6127-33.
    pmc: PMC2852022pubmed: 20194732doi: 10.1073/pnas.0912955107google scholar: lookup
  12. Lagunas-Rangel FA, Chávez-Valencia V. Learning of nature: The curious case of the naked mole rat.. Mech Ageing Dev 2017 Jun;164:76-81.
    pubmed: 28472634doi: 10.1016/j.mad.2017.04.010google scholar: lookup
  13. Frese KK, Tuveson DA. Maximizing mouse cancer models.. Nat Rev Cancer 2007 Sep;7(9):645-58.
    pubmed: 17687385doi: 10.1038/nrc2192google scholar: lookup
  14. van der Kraan PM. Understanding developmental mechanisms in the context of osteoarthritis.. Curr Rheumatol Rep 2013 Jun;15(6):333.
    pubmed: 23591824doi: 10.1007/s11926-013-0333-3google scholar: lookup
  15. Donahue SW, Galley SA, Vaughan MR, Patterson-Buckendahl P, Demers LM, Vance JL, McGee ME. Parathyroid hormone may maintain bone formation in hibernating black bears (Ursus americanus) to prevent disuse osteoporosis.. J Exp Biol 2006 May;209(Pt 9):1630-8.
    pubmed: 16621944doi: 10.1242/jeb.02185google scholar: lookup
  16. Gray SK, McGee-Lawrence ME, Sanders JL, Condon KW, Tsai CJ, Donahue SW. Black bear parathyroid hormone has greater anabolic effects on trabecular bone in dystrophin-deficient mice than in wild type mice.. Bone 2012 Sep;51(3):578-85.
    pmc: PMC3412940pubmed: 22584007doi: 10.1016/j.bone.2012.05.003google scholar: lookup
  17. Innes JF, Clegg P. Comparative rheumatology: what can be learnt from naturally occurring musculoskeletal disorders in domestic animals?. Rheumatology (Oxford) 2010 Jun;49(6):1030-9.
    pubmed: 20176567doi: 10.1093/rheumatology/kep465google scholar: lookup
  18. Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB, Kamal M, Clamp M, Chang JL, Kulbokas EJ 3rd, Zody MC, Mauceli E, Xie X, Breen M, Wayne RK, Ostrander EA, Ponting CP, Galibert F, Smith DR, DeJong PJ, Kirkness E, Alvarez P, Biagi T, Brockman W, Butler J, Chin CW, Cook A, Cuff J, Daly MJ, DeCaprio D, Gnerre S, Grabherr M, Kellis M, Kleber M, Bardeleben C, Goodstadt L, Heger A, Hitte C, Kim L, Koepfli KP, Parker HG, Pollinger JP, Searle SM, Sutter NB, Thomas R, Webber C, Baldwin J, Abebe A, Abouelleil A, Aftuck L, Ait-Zahra M, Aldredge T, Allen N, An P, Anderson S, Antoine C, Arachchi H, Aslam A, Ayotte L, Bachantsang P, Barry A, Bayul T, Benamara M, Berlin A, Bessette D, Blitshteyn B, Bloom T, Blye J, Boguslavskiy L, Bonnet C, Boukhgalter B, Brown A, Cahill P, Calixte N, Camarata J, Cheshatsang Y, Chu J, Citroen M, Collymore A, Cooke P, Dawoe T, Daza R, Decktor K, DeGray S, Dhargay N, Dooley K, Dooley K, Dorje P, Dorjee K, Dorris L, Duffey N, Dupes A, Egbiremolen O, Elong R, Falk J, Farina A, Faro S, Ferguson D, Ferreira P, Fisher S, FitzGerald M, Foley K, Foley C, Franke A, Friedrich D, Gage D, Garber M, Gearin G, Giannoukos G, Goode T, Goyette A, Graham J, Grandbois E, Gyaltsen K, Hafez N, Hagopian D, Hagos B, Hall J, Healy C, Hegarty R, Honan T, Horn A, Houde N, Hughes L, Hunnicutt L, Husby M, Jester B, Jones C, Kamat A, Kanga B, Kells C, Khazanovich D, Kieu AC, Kisner P, Kumar M, Lance K, Landers T, Lara M, Lee W, Leger JP, Lennon N, Leuper L, LeVine S, Liu J, Liu X, Lokyitsang Y, Lokyitsang T, Lui A, Macdonald J, Major J, Marabella R, Maru K, Matthews C, McDonough S, Mehta T, Meldrim J, Melnikov A, Meneus L, Mihalev A, Mihova T, Miller K, Mittelman R, Mlenga V, Mulrain L, Munson G, Navidi A, Naylor J, Nguyen T, Nguyen N, Nguyen C, Nguyen T, Nicol R, Norbu N, Norbu C, Novod N, Nyima T, Olandt P, O'Neill B, O'Neill K, Osman S, Oyono L, Patti C, Perrin D, Phunkhang P, Pierre F, Priest M, Rachupka A, Raghuraman S, Rameau R, Ray V, Raymond C, Rege F, Rise C, Rogers J, Rogov P, Sahalie J, Settipalli S, Sharpe T, Shea T, Sheehan M, Sherpa N, Shi J, Shih D, Sloan J, Smith C, Sparrow T, Stalker J, Stange-Thomann N, Stavropoulos S, Stone C, Stone S, Sykes S, Tchuinga P, Tenzing P, Tesfaye S, Thoulutsang D, Thoulutsang Y, Topham K, Topping I, Tsamla T, Vassiliev H, Venkataraman V, Vo A, Wangchuk T, Wangdi T, Weiand M, Wilkinson J, Wilson A, Yadav S, Yang S, Yang X, Young G, Yu Q, Zainoun J, Zembek L, Zimmer A, Lander ES. Genome sequence, comparative analysis and haplotype structure of the domestic dog.. Nature 2005 Dec 8;438(7069):803-19.
    pubmed: 16341006doi: 10.1038/nature04338google scholar: lookup
  19. Wilke VL, Robinson DA, Evans RB, Rothschild MF, Conzemius MG. Estimate of the annual economic impact of treatment of cranial cruciate ligament injury in dogs in the United States.. J Am Vet Med Assoc 2005 Nov 15;227(10):1604-7.
    pubmed: 16313037doi: 10.2460/javma.2005.227.1604google scholar: lookup
  20. Martig S, Chen W, Lee PV, Whitton RC. Bone fatigue and its implications for injuries in racehorses.. Equine Vet J 2014 Jul;46(4):408-15.
    pubmed: 24528139doi: 10.1111/evj.12241google scholar: lookup
  21. Muir P, Johnson KA, Ruaux-Mason CP. In vivo matrix microdamage in a naturally occurring canine fatigue fracture.. Bone 1999 Nov;25(5):571-6.
    pubmed: 10574577doi: 10.1016/s8756-3282(99)00205-7google scholar: lookup
  22. Martin RB. Is all cortical bone remodeling initiated by microdamage?. Bone 2002 Jan;30(1):8-13.
    pubmed: 11792558doi: 10.1016/s8756-3282(01)00620-2google scholar: lookup
  23. Korhonen MT, Mero AA, Alén M, Sipilä S, Häkkinen K, Liikavainio T, Viitasalo JT, Haverinen MT, Suominen H. Biomechanical and skeletal muscle determinants of maximum running speed with aging.. Med Sci Sports Exerc 2009 Apr;41(4):844-56.
    pubmed: 19276848doi: 10.1249/mss.0b013e3181998366google scholar: lookup
  24. Taylor GM. Maximum force production: why are crabs so strong?. Proc Biol Sci 2000 Jul 22;267(1451):1475-80.
    pmc: PMC1690686pubmed: 10983834doi: 10.1098/rspb.2000.1167google scholar: lookup
  25. Alexander RM. Leg design and jumping technique for humans, other vertebrates and insects.. Philos Trans R Soc Lond B Biol Sci 1995 Feb 28;347(1321):235-48.
    pubmed: 7777591doi: 10.1098/rstb.1995.0024google scholar: lookup
  26. Biewener AA, Blickhan R. Kangaroo rat locomotion: design for elastic energy storage or acceleration?. J Exp Biol 1988 Nov;140:243-55.
    pubmed: 3204333doi: 10.1242/jeb.140.1.243google scholar: lookup
  27. Marsh RL, John-Alder HB. Jumping performance of hylid frogs measured with high-speed cine film.. J Exp Biol 1994 Mar;188:131-41.
    pubmed: 7964379doi: 10.1242/jeb.188.1.131google scholar: lookup
  28. McGowan CP, Skinner J, Biewener AA. Hind limb scaling of kangaroos and wallabies (superfamily Macropodoidea): implications for hopping performance, safety factor and elastic savings.. J Anat 2008 Feb;212(2):153-63.
  29. Krogh A. The rate of diffusion of gases through animal tissues, with some remarks on the coefficient of invasion.. J Physiol 1919 May 20;52(6):391-408.
  30. Krogh A. The number and distribution of capillaries in muscles with calculations of the oxygen pressure head necessary for supplying the tissue.. J Physiol 1919 May 20;52(6):409-15.
  31. Hill AV. First and last experiments in muscle mechanics.. Cambridge Eng: University Press; 1970.
  32. Hill AV. The dimensions of animals and their muscular dynamics.. Science Progress 1950;38(150):209–30.
  33. Alexander RM. Tendon elasticity and muscle function.. Comp Biochem Physiol A Mol Integr Physiol 2002 Dec;133(4):1001-11.
    pubmed: 12485689doi: 10.1016/s1095-6433(02)00143-5google scholar: lookup
  34. Biewener AA, Wakeling JM, Lee SS, Arnold AS. Validation of Hill-type muscle models in relation to neuromuscular recruitment and force-velocity properties: predicting patterns of in vivo muscle force.. Integr Comp Biol 2014 Dec;54(6):1072-83.
    pmc: PMC4296201pubmed: 24928073doi: 10.1093/icb/icu070google scholar: lookup
  35. Kram R, Roberts TJ. A. V. Hill sticks his neck out.. J Exp Biol 2016 Feb;219(Pt 4):468-9.
    pubmed: 26888998doi: 10.1242/jeb.123372google scholar: lookup
  36. Lieber RL, Roberts TJ, Blemker SS, Lee SSM, Herzog W. Skeletal muscle mechanics, energetics and plasticity.. J Neuroeng Rehabil 2017 Oct 23;14(1):108.
    pmc: PMC5651624pubmed: 29058612doi: 10.1186/s12984-017-0318-ygoogle scholar: lookup
  37. Cooper BJ, Winand NJ, Stedman H, Valentine BA, Hoffman EP, Kunkel LM, Scott MO, Fischbeck KH, Kornegay JN, Avery RJ. The homologue of the Duchenne locus is defective in X-linked muscular dystrophy of dogs.. Nature 1988 Jul 14;334(6178):154-6.
    pubmed: 3290691doi: 10.1038/334154a0google scholar: lookup
  38. Vieira NM, Elvers I, Alexander MS, Moreira YB, Eran A, Gomes JP, Marshall JL, Karlsson EK, Verjovski-Almeida S, Lindblad-Toh K, Kunkel LM, Zatz M. Jagged 1 Rescues the Duchenne Muscular Dystrophy Phenotype.. Cell 2015 Nov 19;163(5):1204-1213.
    pmc: PMC4668935pubmed: 26582133doi: 10.1016/j.cell.2015.10.049google scholar: lookup
  39. Dirks ML, Wall BT, van de Valk B, Holloway TM, Holloway GP, Chabowski A, Goossens GH, van Loon LJ. One Week of Bed Rest Leads to Substantial Muscle Atrophy and Induces Whole-Body Insulin Resistance in the Absence of Skeletal Muscle Lipid Accumulation.. Diabetes 2016 Oct;65(10):2862-75.
    pubmed: 27358494doi: 10.2337/db15-1661google scholar: lookup
  40. Moore CD, Craven BC, Thabane L, Laing AC, Frank-Wilson AW, Kontulainen SA, Papaioannou A, Adachi JD, Giangregorio LM. Lower-extremity muscle atrophy and fat infiltration after chronic spinal cord injury.. J Musculoskelet Neuronal Interact 2015 Mar;15(1):32-41.
    pmc: PMC5092153pubmed: 25730650
  41. Cotton CJ. Skeletal muscle mass and composition during mammalian hibernation.. J Exp Biol 2016 Jan;219(Pt 2):226-34.
    pubmed: 26792334doi: 10.1242/jeb.125401google scholar: lookup
  42. Duncan AE, Colman RJ, Kramer PA. Longitudinal study of radiographic spinal osteoarthritis in a macaque model.. J Orthop Res 2011 Aug;29(8):1152-60.
    pmc: PMC3241944pubmed: 21381096doi: 10.1002/jor.21390google scholar: lookup
  43. Lascelles BD, King S, Roe S, Marcellin-Little DJ, Jones S. Expression and activity of COX-1 and 2 and 5-LOX in joint tissues from dogs with naturally occurring coxofemoral joint osteoarthritis.. J Orthop Res 2009 Sep;27(9):1204-8.
    pubmed: 19274754doi: 10.1002/jor.20864google scholar: lookup
  44. Monteiro BP, Klinck MP, Moreau M, Guillot M, Steagall PV, Pelletier JP, Martel-Pelletier J, Gauvin D, Del Castillo JR, Troncy E. Analgesic efficacy of tramadol in cats with naturally occurring osteoarthritis.. PLoS One 2017;12(4):e0175565.
  45. Moreau M, Pelletier JP, Lussier B, d'Anjou MA, Blond L, Pelletier JM, del Castillo JR, Troncy E. A posteriori comparison of natural and surgical destabilization models of canine osteoarthritis.. Biomed Res Int 2013;2013:180453.
    pmc: PMC3833019pubmed: 24288664doi: 10.1155/2013/180453google scholar: lookup
  46. Olive J, d'Anjou MA, Cabassu J, Chailleux N, Blond L. Fast presurgical magnetic resonance imaging of meniscal tears and concurrent subchondral bone marrow lesions. Study of dogs with naturally occurring cranial cruciate ligament rupture.. Vet Comp Orthop Traumatol 2014;27(1):1-7.
    pubmed: 24226972doi: 10.3415/vcot-13-04-0054google scholar: lookup
  47. Reesink HL, Watts AE, Mohammed HO, Jay GD, Nixon AJ. Lubricin/proteoglycan 4 increases in both experimental and naturally occurring equine osteoarthritis.. Osteoarthritis Cartilage 2017 Jan;25(1):128-137.
    pmc: PMC5489058pubmed: 27498214doi: 10.1016/j.joca.2016.07.021google scholar: lookup
  48. Ritzo ME, Ritzo BA, Siddens AD, Summerlott S, Cook JL. Incidence and type of meniscal injury and associated long-term clinical outcomes in dogs treated surgically for cranial cruciate ligament disease.. Vet Surg 2014 Nov;43(8):952-8.
  49. Chen D, Shen J, Zhao W, Wang T, Han L, Hamilton JL, Im HJ. Osteoarthritis: toward a comprehensive understanding of pathological mechanism.. Bone Res 2017;5:16044.
    pmc: PMC5240031pubmed: 28149655doi: 10.1038/boneres.2016.44google scholar: lookup
  50. Bertuglia A, Lacourt M, Girard C, Beauchamp G, Richard H, Laverty S. Osteoclasts are recruited to the subchondral bone in naturally occurring post-traumatic equine carpal osteoarthritis and may contribute to cartilage degradation.. Osteoarthritis Cartilage 2016 Mar;24(3):555-66.
    pubmed: 26505663doi: 10.1016/j.joca.2015.10.008google scholar: lookup
  51. Sanchez-Bustinduy M, de Medeiros MA, Radke H, Langley-Hobbs S, McKinley T, Jeffery N. Comparison of kinematic variables in defining lameness caused by naturally occurring rupture of the cranial cruciate ligament in dogs.. Vet Surg 2010 Jun;39(4):523-30.
  52. Tienen TG, Heijkants RG, Buma P, De Groot JH, Pennings AJ, Veth RP. A porous polymer scaffold for meniscal lesion repair--a study in dogs.. Biomaterials 2003 Jun;24(14):2541-8.
    pubmed: 12695081doi: 10.1016/s0142-9612(03)00053-xgoogle scholar: lookup
  53. Singh K, Masuda K, An HS. Animal models for human disc degeneration.. Spine J 2005 Nov-Dec;5(6 Suppl):267S-279S.
    pubmed: 16291123doi: 10.1016/j.spinee.2005.02.016google scholar: lookup
  54. Donoghue PC, Sansom IJ, Downs JP. Early evolution of vertebrate skeletal tissues and cellular interactions, and the canalization of skeletal development.. J Exp Zool B Mol Dev Evol 2006 May 15;306(3):278-94.
    pubmed: 16555304doi: 10.1002/jez.b.21090google scholar: lookup
  55. Donoghue PC, Sansom IJ. Origin and early evolution of vertebrate skeletonization.. Microsc Res Tech 2002 Dec 1;59(5):352-72.
    pubmed: 12430166doi: 10.1002/jemt.10217google scholar: lookup
  56. Dallas SL, Prideaux M, Bonewald LF. The osteocyte: an endocrine cell ... and more.. Endocr Rev 2013 Oct;34(5):658-90.
    pmc: PMC3785641pubmed: 23612223doi: 10.1210/er.2012-1026google scholar: lookup
  57. Shahar R, Dean MN. The enigmas of bone without osteocytes.. Bonekey Rep 2013 May 1;2:343.
    pmc: PMC3692265pubmed: 24422081doi: 10.1038/bonekey.2013.77google scholar: lookup
  58. Bloomfield SA. Disuse osteopenia.. Curr Osteoporos Rep 2010 Jun;8(2):91-7.
    pubmed: 20425616doi: 10.1007/s11914-010-0013-4google scholar: lookup
  59. Bloomfield SA, Allen MR, Hogan HA, Delp MD. Site- and compartment-specific changes in bone with hindlimb unloading in mature adult rats.. Bone 2002 Jul;31(1):149-57.
    pubmed: 12110428doi: 10.1016/s8756-3282(02)00785-8google scholar: lookup
  60. Vico L, Collet P, Guignandon A, Lafage-Proust MH, Thomas T, Rehaillia M, Alexandre C. Effects of long-term microgravity exposure on cancellous and cortical weight-bearing bones of cosmonauts.. Lancet 2000 May 6;355(9215):1607-11.
    pubmed: 10821365doi: 10.1016/s0140-6736(00)02217-0google scholar: lookup
  61. Harvey KB, Donahue SW. Bending properties, porosity, and ash fraction of black bear (Ursus americanus) cortical bone are not compromised with aging despite annual periods of disuse.. J Biomech 2004 Oct;37(10):1513-20.
  62. Harvey KB, Drummer TD, Donahue SW. The tensile strength of black bear (Ursus americanus) cortical bone is not compromised with aging despite annual periods of hibernation.. J Biomech 2005 Nov;38(11):2143-50.
  63. McGee ME, Magic KW, Miller DL, Maki AJ, Donahue SW. Black bear femoral porosity decreases and mechanical properties increase with age despite annual periods of disuse (hibernation). Eng Fract Mech 2007:741942–52.
  64. McGee ME, Maki AJ, Johnson SE, Nelson OL, Robbins CT, Donahue SW. Decreased bone turnover with balanced resorption and formation prevent cortical bone loss during disuse (hibernation) in grizzly bears (Ursus arctos horribilis).. Bone 2008 Feb;42(2):396-404.
    pmc: PMC2249622pubmed: 18037367doi: 10.1016/j.bone.2007.10.010google scholar: lookup
  65. McGee ME, Miller DL, Auger J, Black HL, Donahue SW. Black bear femoral geometry and cortical porosity are not adversely affected by ageing despite annual periods of disuse (hibernation).. J Anat 2007 Feb;210(2):160-9.
  66. McGee-Lawrence ME, Wojda SJ, Barlow LN, Drummer TD, Bunnell K, Auger J, Black HL, Donahue SW. Six months of disuse during hibernation does not increase intracortical porosity or decrease cortical bone geometry, strength, or mineralization in black bear (Ursus americanus) femurs.. J Biomech 2009 Jul 22;42(10):1378-1383.
  67. Donahue SW, McGee ME, Harvey KB, Vaughan MR, Robbins CT. Hibernating bears as a model for preventing disuse osteoporosis.. J Biomech 2006;39(8):1480-8.
  68. Wojda SJ, Weyland DR, Gray SK, McGee-Lawrence ME, Drummer TD, Donahue SW. Black bears with longer disuse (hibernation) periods have lower femoral osteon population density and greater mineralization and intracortical porosity.. Anat Rec (Hoboken) 2013 Aug;296(8):1148-53.
    pubmed: 23728917doi: 10.1002/ar.22720google scholar: lookup
  69. McCalden RW, McGeough JA, Barker MB, Court-Brown CM. Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity, mineralization, and microstructure.. J Bone Joint Surg Am 1993 Aug;75(8):1193-205.
  70. McGee-Lawrence M, Buckendahl P, Carpenter C, Henriksen K, Vaughan M, Donahue S. Suppressed bone remodeling in black bears conserves energy and bone mass during hibernation.. J Exp Biol 2015 Jul;218(Pt 13):2067-74.
    pmc: PMC4510842pubmed: 26157160doi: 10.1242/jeb.120725google scholar: lookup
  71. McGee-Lawrence ME, Wojda SJ, Barlow LN, Drummer TD, Castillo AB, Kennedy O, Condon KW, Auger J, Black HL, Nelson OL, Robbins CT, Donahue SW. Grizzly bears (Ursus arctos horribilis) and black bears (Ursus americanus) prevent trabecular bone loss during disuse (hibernation).. Bone 2009 Dec;45(6):1186-91.
    pmc: PMC2783552pubmed: 19703606doi: 10.1016/j.bone.2009.08.011google scholar: lookup
  72. Doherty AH, Florant GL, Donahue SW. Endocrine regulation of bone and energy metabolism in hibernating mammals.. Integr Comp Biol 2014 Sep;54(3):463-83.
    pmc: PMC4184349pubmed: 24556365doi: 10.1093/icb/icu001google scholar: lookup
  73. McGee-Lawrence ME, Carey HV, Donahue SW. Mammalian hibernation as a model of disuse osteoporosis: the effects of physical inactivity on bone metabolism, structure, and strength.. Am J Physiol Regul Integr Comp Physiol 2008 Dec;295(6):R1999-2014.
    pmc: PMC2685297pubmed: 18843088doi: 10.1152/ajpregu.90648.2008google scholar: lookup
  74. Reilly BD, Franklin CE. Prevention of muscle wasting and osteoporosis: the value of examining novel animal models.. J Exp Biol 2016 Sep 1;219(Pt 17):2582-95.
    pubmed: 27582559doi: 10.1242/jeb.128348google scholar: lookup
  75. Chow BA, Donahue SW, Vaughan MR, McConkey B, Vijayan MM. Serum immune-related proteins are differentially expressed during hibernation in the American black bear.. PLoS One 2013;8(6):e66119.
  76. Donahue SW, Vaughan MR, Demers LM, Donahue HJ. Bone formation is not impaired by hibernation (disuse) in black bears Ursus americanus.. J Exp Biol 2003 Dec;206(Pt 23):4233-9.
    pubmed: 14581593doi: 10.1242/jeb.00671google scholar: lookup
  77. Fedorov VB, Goropashnaya AV, Tøien Ø, Stewart NC, Chang C, Wang H, Yan J, Showe LC, Showe MK, Donahue SW, Barnes BM. Preservation of bone mass and structure in hibernating black bears (Ursus americanus) through elevated expression of anabolic genes.. Funct Integr Genomics 2012 Jun;12(2):357-65.
    pmc: PMC4480364pubmed: 22351243doi: 10.1007/s10142-012-0266-3google scholar: lookup
  78. Fink T, Rasmussen JG, Emmersen J, Pilgaard L, Fahlman Å, Brunberg S, Josefsson J, Arnemo JM, Zachar V, Swenson JE, Fröbert O. Adipose-derived stem cells from the brown bear (Ursus arctos) spontaneously undergo chondrogenic and osteogenic differentiation in vitro.. Stem Cell Res 2011 Jul;7(1):89-95.
    pubmed: 21497574doi: 10.1016/j.scr.2011.03.003google scholar: lookup
  79. Overstreet M, Floyd T, Polotsky A, Hungerford DS, Frondoza CG. Induction of osteoblast aggregation, detachment, and altered integrin expression by bear serum.. In Vitro Cell Dev Biol Anim 2004 Jan-Feb;40(1-2):4-7.
  80. Seger RL, Cross RA, Rosen CJ, Causey RC, Gundberg CM, Carpenter TO, Chen TC, Halteman WA, Holick MF, Jakubas WJ, Keisler DH, Seger RM, Servello FA. Investigating the mechanism for maintaining eucalcemia despite immobility and anuria in the hibernating American black bear (Ursus americanus).. Bone 2011 Dec;49(6):1205-12.
    pubmed: 21893223doi: 10.1016/j.bone.2011.08.017google scholar: lookup
  81. Vestergaard P, Støen OG, Swenson JE, Mosekilde L, Heickendorff L, Fröbert O. Vitamin D status and bone and connective tissue turnover in brown bears (Ursus arctos) during hibernation and the active state.. PLoS One 2011;6(6):e21483.
  82. Berg von Linde M, Arevström L, Fröbert O. Insights from the Den: How Hibernating Bears May Help Us Understand and Treat Human Disease.. Clin Transl Sci 2015 Oct;8(5):601-5.
    pmc: PMC5351099pubmed: 26083277doi: 10.1111/cts.12279google scholar: lookup
  83. Bogren LK, Johnston EL, Barati Z, Martin PA, Wojda SJ, Van Tets IG, LeBlanc AD, Donahue SW, Drew KL. The effects of hibernation and forced disuse (neurectomy) on bone properties in arctic ground squirrels.. Physiol Rep 2016 May;4(10).
    pmc: PMC4886160pubmed: 27225624doi: 10.14814/phy2.12771google scholar: lookup
  84. Doherty AH, Frampton JD, Vinyard CJ. Hibernation does not reduce cortical bone density, area or second moments of inertia in woodchucks (Marmota monax).. J Morphol 2012 Jun;273(6):604-17.
    pubmed: 22234945doi: 10.1002/jmor.20007google scholar: lookup
  85. Hudson NJ, Bennett MB, Franklin CE. Effect of aestivation on long bone mechanical properties in the green-striped burrowing frog, Cyclorana alboguttata.. J Exp Biol 2004 Jan;207(Pt 3):475-82.
    pubmed: 14691095doi: 10.1242/jeb.00787google scholar: lookup
  86. McGee-Lawrence ME, Stoll DM, Mantila ER, Fahrner BK, Carey HV, Donahue SW. Thirteen-lined ground squirrels (Ictidomys tridecemlineatus) show microstructural bone loss during hibernation but preserve bone macrostructural geometry and strength.. J Exp Biol 2011 Apr 15;214(Pt 8):1240-7.
    pmc: PMC3063110pubmed: 21430199doi: 10.1242/jeb053520google scholar: lookup
  87. Utz JC, Nelson S, O'Toole BJ, van Breukelen F. Bone strength is maintained after 8 months of inactivity in hibernating golden-mantled ground squirrels, Spermophilus lateralis.. J Exp Biol 2009 Sep 1;212(17):2746-52.
    pmc: PMC2727459pubmed: 19684206doi: 10.1242/jeb.032854google scholar: lookup
  88. Wojda SJ, Gridley RA, McGee-Lawrence ME, Drummer TD, Hess A, Kohl F, Barnes BM, Donahue SW. Arctic Ground Squirrels Limit Bone Loss during the Prolonged Physical Inactivity Associated with Hibernation.. Physiol Biochem Zool 2016 Jan-Feb;89(1):72-80.
    pubmed: 27082526doi: 10.1086/684619google scholar: lookup
  89. Wojda SJ, McGee-Lawrence ME, Gridley RA, Auger J, Black HL, Donahue SW. Yellow-bellied marmots (Marmota flaviventris) preserve bone strength and microstructure during hibernation.. Bone 2012 Jan;50(1):182-8.
    pmc: PMC3489026pubmed: 22037004doi: 10.1016/j.bone.2011.10.013google scholar: lookup
  90. Doherty AH, Roteliuk DM, Gookin SE, McGrew AK, Broccardo CJ, Condon KW, Prenni JE, Wojda SJ, Florant GL, Donahue SW. Exploring the Bone Proteome to Help Explain Altered Bone Remodeling and Preservation of Bone Architecture and Strength in Hibernating Marmots.. Physiol Biochem Zool 2016 Sep-Oct;89(5):364-76.
    pubmed: 27617358doi: 10.1086/687413google scholar: lookup
  91. Rauch F. Neuro-musculoskeletal interactions in bed rest, hibernation and stroke.. J Musculoskelet Neuronal Interact 2009 Oct-Dec;9(4):184-5.
    pubmed: 19949276
  92. Withrow SJ, Wilkins RM. Cross talk from pets to people: translational osteosarcoma treatments.. ILAR J 2010;51(3):208-13.
    pubmed: 21131721doi: 10.1093/ilar.51.3.208google scholar: lookup
  93. Ranieri G, Gadaleta CD, Patruno R, Zizzo N, Daidone MG, Hansson MG, Paradiso A, Ribatti D. A model of study for human cancer: Spontaneous occurring tumors in dogs. Biological features and translation for new anticancer therapies.. Crit Rev Oncol Hematol 2013 Oct;88(1):187-97.
  94. Wilkins RM, Cullen JW, Camozzi AB, Jamroz BA, Odom L. Improved survival in primary nonmetastatic pediatric osteosarcoma of the extremity.. Clin Orthop Relat Res 2005 Sep;438:128-36.
  95. Drögemüller C, Becker D, Brunner A, Haase B, Kircher P, Seeliger F, Fehr M, Baumann U, Lindblad-Toh K, Leeb T. A missense mutation in the SERPINH1 gene in Dachshunds with osteogenesis imperfecta.. PLoS Genet 2009 Jul;5(7):e1000579.
  96. Seeliger F, Leeb T, Peters M, Brugmann M, Fehr M, Hewicker-Trautwein M. Osteogenesis imperfecta in two litters of dachshunds.. Vet Pathol 2003 Sep;40(5):530-9.
    pubmed: 12949410doi: 10.1354/vp.40-5-530google scholar: lookup

Citations

This article has been cited 3 times.
  1. Abdel Hamid OI, Attia ME, Hirshon JM, El-Shinawi M, El-Hussaini M, El-Setouhy M. Psychiatric Disorders and Genotoxicity Following Primary Metal on Polyethylene Total Hip Arthroplasty and Their Correlation to Cobalt/Chromium Levels. Drug Healthc Patient Saf 2022;14:97-111.
    doi: 10.2147/DHPS.S360643pubmed: 35880007google scholar: lookup
  2. Shalhoub M, Anaya M, Deek S, Zaben AH, Abdalla MA, Jaber MM, Koni AA, Zyoud SH. The impact of pain on quality of life in patients with osteoarthritis: a cross-sectional study from Palestine. BMC Musculoskelet Disord 2022 Mar 14;23(1):248.
    doi: 10.1186/s12891-022-05207-xpubmed: 35287651google scholar: lookup
  3. Goropashnaya AV, Tøien Ø, Ramaraj T, Sundararajan A, Schilkey FD, Barnes BM, Donahue SW, Fedorov VB. Transcriptional changes and preservation of bone mass in hibernating black bears. Sci Rep 2021 Apr 15;11(1):8281.
    doi: 10.1038/s41598-021-87785-9pubmed: 33859306google scholar: lookup