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Journal of morphology2016; 277(7); 948-956; doi: 10.1002/jmor.20548

Trabecular bone of precocials at birth; Are they prepared to run for the wolf(f)?

Abstract: Bone is a dynamic tissue adapting to loading according to "Wolff's law of bone adaptation." During very early life, however, such a mechanism may not be adequate enough to adapt to the dramatic change in environmental challenges in precocial species. Their neonates are required to stand and walk within hours after birth, in contrast to altricial animals that have much more time to adapt from the intrauterine environment to the outside world. In this study, trabecular bone parameters of the talus and sagittal ridge of the tibia from stillborn but full-term precocials (calves and foals) were analyzed by micro-CT imaging in order to identify possible anticipatory mechanisms to loading. Calculated average bone volume fraction in the Shetland pony (49-74%) was significantly higher compared to Warmblood foals (28-51%). Bovine trabecular bone was characterized by a low average bone volume fraction (22-28%), however, more directional anisotropy was found. It is concluded that anticipatory strategies in skeletal development exist in precocial species, which differ per species and are most likely related to anatomical differences in joint geometry and related loading patterns. The underlying regulatory mechanisms are still unknown, but they may be based on a genetic blueprint for the development of bone. More knowledge, both about a possible blueprint and its regulation, will be helpful in understanding developmental bone and joint diseases. J. Morphol. 277:948-956, 2016. © 2016 Wiley Periodicals, Inc.
Publication Date: 2016-04-20 PubMed ID: 27098190PubMed Central: PMC5111789DOI: 10.1002/jmor.20548Google Scholar: Lookup
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  • Journal Article

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 study investigates how the bones of newborn animals, which are required to stand and walk shortly after birth, adapt to their new environment in order to determine if there are any anticipatory mechanisms for dealing with load-bearing activities. Findings suggest that these animals employ species-specific anticipatory strategies in skeletal development, although the underlying mechanisms remain unidentified.

Objective of the Research

  • The main objective of this study was to determine how the bones of precocial animals (those that can stand and walk at birth) adapt to their dramatic environmental changes. The research aimed to identify any anticipatory mechanisms for load-bearing activities, which these animals need to undertake almost immediately after they are born. This was done by analyzing the trabecular bone parameters (the spongy interior of bones) of full-term but stillborn calves and foals.

Methodology

  • Micro-CT imaging was used to analyse the trabecular bone parameters of the talus (ankle bone) and sagittal ridge of the tibia (lower leg bone) in these precocial animals.
  • The researchers also calculated the average bone volume fraction to compare between Shetland pony foals, Warmblood foals, and bovines (cattle).

Findings

  • The study found that the average bone volume fraction in Shetland pony foals is significantly higher compared to that in Warmblood foals.
  • The bovine trabecular bone had a low average bone volume fraction but exhibited more directional anisotropy, which means their bones had more variation in structural properties depending on direction.
  • The research concluded that anticipatory strategies in skeletal development do exist in precocial species, but these strategies differ per species and are most likely related to the anatomical differences in joint geometry and specific loading patterns.

Implications

  • While the study identified that these developmental strategies exist, it also acknowledged that the underlying regulatory mechanisms that govern these adaptations are still unknown.
  • The researchers suggested these may be based on a genomic blueprint for the development of bone.
  • The research highlights the need for further understanding about this possible blueprint and its regulation, which could be useful in further understanding developmental bone and joint diseases.

Cite This Article

APA
Gorissen BM, Wolschrijn CF, van Vilsteren AA, van Rietbergen B, van Weeren PR. (2016). Trabecular bone of precocials at birth; Are they prepared to run for the wolf(f)? J Morphol, 277(7), 948-956. https://doi.org/10.1002/jmor.20548

Publication

ISSN: 1097-4687
NlmUniqueID: 0406125
Country: United States
Language: English
Volume: 277
Issue: 7
Pages: 948-956

Researcher Affiliations

Gorissen, Ben M C
  • Department of Pathobiology, Anatomy and Physiology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.
Wolschrijn, Claudia F
  • Department of Pathobiology, Anatomy and Physiology Division, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.
van Vilsteren, Anouk A M
  • Department of Animal Sciences, Human and Animal Physiology Division, Wageningen University, Wageningen, The Netherlands.
van Rietbergen, Bert
  • Department of Biomedical Engineering, Orthopedic Biomechanics Division, Eindhoven University of Technology, Eindhoven, The Netherlands.
van Weeren, P René
  • Department of Equine Sciences, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.

MeSH Terms

  • Adaptation, Physiological
  • Animals
  • Animals, Newborn
  • Cancellous Bone / anatomy & histology
  • Cancellous Bone / embryology
  • Cattle / anatomy & histology
  • Cattle / embryology
  • Horses / anatomy & histology
  • Horses / embryology
  • Models, Biological
  • Running

References

This article includes 55 references
  1. Abdunnabi AH, Ahmed YA, Philip CJ, Davies HM. Morphometrical variations of the carpal bones in thoroughbreds and ponies.. Anat Histol Embryol 2012 Apr;41(2):139-48.
  2. Badoux DM. Some biomechanical aspects of the structure of the equine tarsus.. Anat Anz 1987;164(1):53-61.
    pubmed: 3662028
  3. Barak MM, Lieberman DE, Hublin JJ. Of mice, rats and men: trabecular bone architecture in mammals scales to body mass with negative allometry.. J Struct Biol 2013 Aug;183(2):123-31.
    pubmed: 23639903doi: 10.1016/j.jsb.2013.04.009google scholar: lookup
  4. Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing.. J R Stat Soc Ser B Stat Methodol 57:289–300.
  5. Borah B, Dufresne TE, Cockman MD, Gross GJ, Sod EW, Myers WR, Combs KS, Higgins RE, Pierce SA, Stevens ML. Evaluation of changes in trabecular bone architecture and mechanical properties of minipig vertebrae by three-dimensional magnetic resonance microimaging and finite element modeling.. J Bone Miner Res 2000 Sep;15(9):1786-97.
    pubmed: 10976998doi: 10.1359/jbmr.2000.15.9.1786google scholar: lookup
  6. Branch MV, Murray RC, Dyson SJ, Goodship AE. Is there a characteristic distal tarsal subchondral bone plate thickness pattern in horses with no history of hindlimb lameness?. Equine Vet J 2005 Sep;37(5):450-5.
    pubmed: 16163948doi: 10.2746/042516405774479951google scholar: lookup
  7. Christen P, Ito K, Ellouz R, Boutroy S, Sornay-Rendu E, Chapurlat RD, van Rietbergen B. Bone remodelling in humans is load-driven but not lazy.. Nat Commun 2014 Sep 11;5:4855.
    pubmed: 25209333doi: 10.1038/ncomms5855google scholar: lookup
  8. Christen P, Ito K, van Rietbergen B. A potential mechanism for allometric trabecular bone scaling in terrestrial mammals.. J Anat 2015 Mar;226(3):236-43.
    pmc: PMC4337663pubmed: 25655770doi: 10.1111/joa.12278google scholar: lookup
  9. Cunningham CA, Black SM. Anticipating bipedalism: trabecular organization in the newborn ilium.. J Anat 2009 Jun;214(6):817-29.
  10. Doube M, Klosowski MM, Wiktorowicz-Conroy AM, Hutchinson JR, Shefelbine SJ. Trabecular bone scales allometrically in mammals and birds.. Proc Biol Sci 2011 Oct 22;278(1721):3067-73.
    pmc: PMC3158937pubmed: 21389033doi: 10.1098/rspb.2011.0069google scholar: lookup
  11. Dowthwaite JN, Rosenbaum PF, Sames CA, Scerpella TA. Muscle function, dynamic loading, and femoral neck structure in pediatric females.. Med Sci Sports Exerc 2014;46(5):911-9.
  12. Ducro BJ, Bovenhuis H, Back W. Heritability of foot conformation and its relationship to sports performance in a Dutch Warmblood horse population.. Equine Vet J 2009 Feb;41(2):139-43.
    pubmed: 19418741doi: 10.2746/042516409x366130google scholar: lookup
  13. Evans HE. 1993. Miller's Anatomy of the Dog, 3rd ed. Philadelphia, PA: W.B. Saunders Company; pp 32–97.
  14. Fajardo RJ, Müller R. Three-dimensional analysis of nonhuman primate trabecular architecture using micro-computed tomography.. Am J Phys Anthropol 2001 Aug;115(4):327-36.
    pubmed: 11471131doi: 10.1002/ajpa.1089google scholar: lookup
  15. Fontaine P, Blond L, Alexander K, Beauchamp G, Richard H, Laverty S. Computed tomography and magnetic resonance imaging in the study of joint development in the equine pelvic limb.. Vet J 2013 Jul;197(1):103-11.
    pubmed: 23688440doi: 10.1016/j.tvjl.2013.03.049google scholar: lookup
  16. Frost HM. From Wolff's law to the Utah paradigm: insights about bone physiology and its clinical applications.. Anat Rec 2001 Apr 1;262(4):398-419.
    pubmed: 11275971doi: 10.1002/ar.1049google scholar: lookup
  17. Frost HM, Jee WS. Perspectives: a vital biomechanical model of the endochondral ossification mechanism.. Anat Rec 1994 Dec;240(4):435-46.
    pubmed: 7879896doi: 10.1002/ar.1092400402google scholar: lookup
  18. Gosman JH, Ketcham RA. Patterns in ontogeny of human trabecular bone from SunWatch Village in the Prehistoric Ohio Valley: general features of microarchitectural change.. Am J Phys Anthropol 2009 Mar;138(3):318-32.
    pubmed: 18785633doi: 10.1002/ajpa.20931google scholar: lookup
  19. Hendriks WK, Colenbrander B, van der Weijden GC, Stout TA. Maternal age and parity influence ultrasonographic measurements of fetal growth in Dutch Warmblood mares.. Anim Reprod Sci 2009 Oct;115(1-4):110-23.
  20. Huiskes R, Weinans H, Grootenboer HJ, Dalstra M, Fudala B, Slooff TJ. Adaptive bone-remodeling theory applied to prosthetic-design analysis.. J Biomech 1987;20(11-12):1135-50.
    pubmed: 3429459doi: 10.1016/0021-9290(87)90030-3google scholar: lookup
  21. Kabel J, Odgaard A, van Rietbergen B, Huiskes R. Connectivity and the elastic properties of cancellous bone.. Bone 1999 Feb;24(2):115-20.
    pubmed: 9951779doi: 10.1016/s8756-3282(98)00164-1google scholar: lookup
  22. Küpfer M, Schinz HR. Beiträge zur Kenntnis der Skelettbildung bei domestizierten Säugern auf Grund röntgenlogischer Untersuchungen.. Denkschriftender Schweiz Naturforsc Gesellsc 49.
  23. Lai LP, Mitchell J. Indian hedgehog: its roles and regulation in endochondral bone development.. J Cell Biochem 2005 Dec 15;96(6):1163-73.
    pubmed: 16187314doi: 10.1002/jcb.20635google scholar: lookup
  24. Lazenby RA, Skinner MM, Kivell TL, Hublin JJ. Scaling VOI size in 3D μCT studies of trabecular bone: a test of the over-sampling hypothesis.. Am J Phys Anthropol 2011 Feb;144(2):196-203.
    pubmed: 20979207doi: 10.1002/ajpa.21385google scholar: lookup
  25. Leterrier C, Nys Y. Composition, cortical structure and mechanical properties of chicken tibiotarsi: effect of growth rate.. Br Poult Sci 1992 Dec;33(5):925-39.
    pubmed: 1493559doi: 10.1080/00071669208417536google scholar: lookup
  26. Linden TC, Bicalho RC, Nydam DV. Calf birth weight and its association with calf and cow survivability, disease incidence, reproductive performance, and milk production.. J Dairy Sci 2009 Jun;92(6):2580-8.
    pubmed: 19447990doi: 10.3168/jds.2008-1603google scholar: lookup
  27. MacLatchy L, Müller R. A comparison of the femoral head and neck trabecular architecture of Galago and Perodicticus using micro-computed tomography (microCT).. J Hum Evol 2002 Jul;43(1):89-105.
    pubmed: 12098212doi: 10.1006/jhev.2002.0559google scholar: lookup
  28. Martin RB, Burr DB. Structure, Function and Adaptation of Compact Bone.. .
  29. 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
  30. 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
  31. Mittra E, Rubin C, Qin YX. Interrelationship of trabecular mechanical and microstructural properties in sheep trabecular bone.. J Biomech 2005 Jun;38(6):1229-37.
  32. Murray RC, Dyson SJ, Weekes JS, Branch MV, Hladick S. Nuclear scintigraphic evaluation of the distal tarsal region in normal horses.. Vet Radiol Ultrasound 2004 Jul-Aug;45(4):345-51.
  33. Nickel R, Schummer A, Seiferle E. Lehrbuch der Anatomie des Haustiere Band I, Bewegungsapparat.. pp 110–128.
  34. Pitsillides AA. Early effects of embryonic movement: 'a shot out of the dark'.. J Anat 2006 Apr;208(4):417-31.
  35. Prisby R, Menezes T, Campbell J, Benson T, Samraj E, Pevzner I, Wideman RF Jr. Kinetic examination of femoral bone modeling in broilers.. Poult Sci 2014 May;93(5):1122-9.
    pubmed: 24795304doi: 10.3382/ps.2013-03778google scholar: lookup
  36. Rot I, Mardesic-Brakus S, Costain WJ, Saraga-Babic M, Kablar B. Role of skeletal muscle in mandible development.. Histol Histopathol 2014 Nov;29(11):1377-94.
    pubmed: 24867377doi: 10.14670/hh-29.1377google scholar: lookup
  37. Ryan TM, Krovitz GE. Trabecular bone ontogeny in the human proximal femur.. J Hum Evol 2006 Dec;51(6):591-602.
    pubmed: 16963108doi: 10.1016/j.jhevol.2006.06.004google scholar: lookup
  38. Ryan TM, Shaw CN. Trabecular bone microstructure scales allometrically in the primate humerus and femur.. Proc Biol Sci 2013 May 7;280(1758):20130172.
    pmc: PMC3619467pubmed: 23486443doi: 10.1098/rspb.2013.0172google scholar: lookup
  39. Ryan WF, Lynch PB, O'Doherty JV. Survey of cull sow bone and joint integrity in the Moorepark Research Farm herd.. Vet Rec 2010 Feb 27;166(9):268-71.
    pubmed: 20190217doi: 10.1136/vr.b4773google scholar: lookup
  40. Schamhardt HC, Hartman W, Lammertink JL. Forces loading the tarsal joint in the hind limb of the horse, determined from in vivo strain measurements of the third metatarsal bone.. Am J Vet Res 1989 May;50(5):728-33.
    pubmed: 2729717
  41. Schneider RK, Milne DW, Gabel AA, Groom JJ, Bramlage LR. Multidirectional in vivo strain analysis of the equine radius and tibia during dynamic loading with and without a cast.. Am J Vet Res 1982 Sep;43(9):1541-50.
    pubmed: 7149401
  42. Schryver HF, Foose TJ, Williams J, Hintz HF. Calcium excretion in feces of ungulates.. Comp Biochem Physiol A Comp Physiol 1983;74(2):375-9.
    pubmed: 6131781doi: 10.1016/0300-9629(83)90618-7google scholar: lookup
  43. Skedros JG, Hunt KJ, Bloebaum RD. Relationships of loading history and structural and material characteristics of bone: development of the mule deer calcaneus.. J Morphol 2004 Mar;259(3):281-307.
    pubmed: 14994328doi: 10.1002/jmor.10167google scholar: lookup
  44. Skedros JG, Sorenson SM, Hunt KJ, Holyoak JD. Ontogenetic structural and material variations in ovine calcanei: a model for interpreting bone adaptation.. Anat Rec (Hoboken) 2007 Mar;290(3):284-300.
    pubmed: 17525944doi: 10.1002/ar.20423google scholar: lookup
  45. Staines KA, Pollard AS, McGonnell IM, Farquharson C, Pitsillides AA. Cartilage to bone transitions in health and disease.. J Endocrinol 2013 Oct;219(1):R1-R12.
    pmc: PMC3769078pubmed: 23959079doi: 10.1530/joe-13-0276google scholar: lookup
  46. Tanck E, Homminga J, van Lenthe GH, Huiskes R. Increase in bone volume fraction precedes architectural adaptation in growing bone.. Bone 2001 Jun;28(6):650-4.
    pubmed: 11425654doi: 10.1016/s8756-3282(01)00464-1google scholar: lookup
  47. Torcasio A, Jähn K, Van Guyse M, Spaepen P, Tami AE, Vander Sloten J, Stoddart MJ, van Lenthe GH. Trabecular bone adaptation to low-magnitude high-frequency loading in microgravity.. PLoS One 2014;9(5):e93527.
  48. Ulrich D, Hildebrand T, Van Rietbergen B, Müller R, Rüegsegger P. The quality of trabecular bone evaluated with micro-computed tomography, FEA and mechanical testing.. Stud Health Technol Inform 1997;40:97-112.
    pubmed: 10168885
  49. van der Tol PP, Metz JH, Noordhuizen-Stassen EN, Back W, Braam CR, Weijs WA. The pressure distribution under the bovine claw during square standing on a flat substrate.. J Dairy Sci 2002 Jun;85(6):1476-81.
  50. van Weeren PR, Sloet van Oldruitenborgh-Ooste, Barneveld A. The influence of birth weight, rate of weight gain and final achieved height and sex on the development of osteochondrotic lesions in a population of genetically predisposed Warmblood foals.. Equine Vet J Suppl 1999 Nov;(31):26-30.
  51. Walton A, Hammond J. The maternal effects on growth and conformation in Shire horse‐Shetland Pony crosses.. Proc R Soc Lond Biol 125:311–335.
  52. Williams B, Waddington D, Murray DH, Farquharson C. Bone strength during growth: influence of growth rate on cortical porosity and mineralization.. Calcif Tissue Int 2004 Mar;74(3):236-45.
    pubmed: 14517713doi: 10.1007/s00223-002-2124-0google scholar: lookup
  53. Wolff J. Das Gesetz der Transformation der Knochen.. .
  54. Wolschrijn CF, Weijs WA. Development of the trabecular structure within the ulnar medial coronoid process of young dogs.. Anat Rec A Discov Mol Cell Evol Biol 2004 Jun;278(2):514-9.
    pubmed: 15164338doi: 10.1002/ar.a.20039google scholar: lookup
  55. Yokota H, Leong DJ, Sun HB. Mechanical loading: bone remodeling and cartilage maintenance.. Curr Osteoporos Rep 2011 Dec;9(4):237-42.
    pubmed: 21858507doi: 10.1007/s11914-011-0067-ygoogle scholar: lookup

Citations

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  1. Bala MM, Bala KA. Association Among Complete Blood Count Parameters, Bone Mineral Density, and Cobb Angle in Cases of Adolescent Idiopathic Scoliosis.. Med Sci Monit 2023 May 20;29:e940355.
    doi: 10.12659/MSM.940355pubmed: 37208892google scholar: lookup
  2. Magrini SH, Mossor AM, German RZ, Young JW. Developmental factors influencing bone strength in precocial mammals: An infant pig model.. J Anat 2023 Jul;243(1):174-181.
    doi: 10.1111/joa.13848pubmed: 36815568google scholar: lookup
  3. Saers JPP, Gordon AD, Ryan TM, Stock JT. Trabecular bone ontogeny tracks neural development and life history among humans and non-human primates.. Proc Natl Acad Sci U S A 2022 Dec 6;119(49):e2208772119.
    doi: 10.1073/pnas.2208772119pubmed: 36459637google scholar: lookup
  4. Cheng Y, Yang H, Hai Y, Pan A, Zhang Y, Zhou L. Hounsfield unit for assessing asymmetrical loss of vertebral bone mineral density and its correlation with curve severity in adolescent idiopathic scoliosis.. Front Surg 2022;9:1000031.
    doi: 10.3389/fsurg.2022.1000031pubmed: 36211282google scholar: lookup
  5. Saers JPP, Gordon AD, Ryan TM, Stock JT. Growth and development of trabecular structure in the calcaneus of Japanese macaques (Macaca fuscata) reflects locomotor behavior, life history, and neuromuscular development.. J Anat 2022 Jul;241(1):67-81.
    doi: 10.1111/joa.13641pubmed: 35178713google scholar: lookup
  6. Deckers K, Tsegai ZJ, Skinner MM, Zeininger A, Kivell TL. Ontogenetic changes to metacarpal trabecular bone structure in mountain and western lowland gorillas.. J Anat 2022 Jul;241(1):82-100.
    doi: 10.1111/joa.13630pubmed: 35122239google scholar: lookup
  7. Wang H, Sun Z, Wang L, Zou D, Li W. Proximal Fusion Level Above First Coronal Reverse Vertebrae: An Essential Factor Decreasing the Risk of Adjacent Segment Degeneration in Degenerative Lumbar Scoliosis.. Global Spine J 2023 Jan;13(1):149-155.
    doi: 10.1177/2192568221994082pubmed: 33648368google scholar: lookup
  8. Saers JPP, Ryan TM, Stock JT. Baby steps towards linking calcaneal trabecular bone ontogeny and the development of bipedal human gait.. J Anat 2020 Mar;236(3):474-492.
    doi: 10.1111/joa.13120pubmed: 31725189google scholar: lookup
  9. Bishop PJ, Hocknull SA, Clemente CJ, Hutchinson JR, Farke AA, Beck BR, Barrett RS, Lloyd DG. Cancellous bone and theropod dinosaur locomotion. Part I-an examination of cancellous bone architecture in the hindlimb bones of theropods.. PeerJ 2018;6:e5778.
    doi: 10.7717/peerj.5778pubmed: 30402347google scholar: lookup
  10. Oinas J, Ronkainen AP, Rieppo L, Finnilä MAJ, Iivarinen JT, van Weeren PR, Helminen HJ, Brama PAJ, Korhonen RK, Saarakkala S. Composition, structure and tensile biomechanical properties of equine articular cartilage during growth and maturation.. Sci Rep 2018 Jul 27;8(1):11357.
    doi: 10.1038/s41598-018-29655-5pubmed: 30054498google scholar: lookup
  11. Amson E, Arnold P, van Heteren AH, Canoville A, Nyakatura JA. Trabecular architecture in the forelimb epiphyses of extant xenarthrans (Mammalia).. Front Zool 2017;14:52.
    doi: 10.1186/s12983-017-0241-xpubmed: 29213295google scholar: lookup