Metacarpophalangeal Joint Pathology and Bone Mineral Density Increase with Exercise but Not with Incidence of Proximal Sesamoid Bone Fracture in Thoroughbred Racehorses
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Training and Racing Exercise History
2.3. Imaging Acquisition and Processing
2.3.1. Dual-Energy X-ray Absorptiometry
2.3.2. Computed Tomography Acquisition
2.3.3. Computed Tomography Manual Analysis
2.3.4. Computed Tomography Radiomics Analysis
2.4. Dissection and Gross Examination
2.5. PSB Sectioning and Processing
2.6. Raman Spectroscopy
2.7. Ash Fraction
2.8. Statistical Analysis
3. Results
3.1. Study Population
3.2. Exercise Comparisons between Fracture and Control Groups
3.3. Association between Age and Exercise
3.4. Intra-Class Correlation Coefficients
3.5. Effect of Group: Fracture versus Control
3.5.1. Pathologic Features
3.5.2. Imaging Features
3.5.3. Ash Fraction
3.5.4. Raman Spectroscopy
3.6. Effect of Exercise: Total High-Speed Furlongs
3.6.1. Gross Pathologic Features
3.6.2. Imaging Features
3.6.3. Ash Fraction
3.6.4. Raman Spectroscopy
3.7. Correlation Statistics
4. Discussion
Study Limitations Paragraph
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Johnson, B.J.; Stover, S.M.; Daft, B.M.; Kinde, H.; Read, D.H.; Barr, B.C.; Anderson, M.; Moore, J.; Woods, L.; Stoltz, J.; et al. Causes of death in racehorses over a 2 year period. Equine Vet. J. 1994, 26, 327–330. [Google Scholar] [CrossRef] [PubMed]
- Stover, S.M. and Murray, A. The California Postmortem Program: Leading the Way. Vet. Clin. N. Am. Equine Pract. 2008, 24, 21–36. [Google Scholar] [CrossRef] [PubMed]
- Sarrafian, T.L.; Case, J.T.; Kinde, H.; Daft, B.M.; Read, D.H.; Moore, J.D.; Uzal, F.A.; Stover, S.M. Fatal musculoskeletal injuries of Quarter Horse racehorses: 314 cases (1990–2007). J. Am. Vet. Med. Assoc. 2012, 241, 935–942. [Google Scholar] [CrossRef] [PubMed]
- Sun, T.C.; Riggs, C.M.; Cogger, N.; Wright, J.; Al-Alawneh, J.I. Noncatastrophic and catastrophic fractures in racing Thoroughbreds at the Hong Kong Jockey Club. Equine Vet. J. 2019, 51, 77–82. [Google Scholar] [CrossRef]
- Anthenill, L.A.; Stover, S.M.; Gardner, I.A.; Hill, A.E. Risk factors for proximal sesamoid bone fractures associated with exercise history and horseshoe characteristics in Thoroughbred racehorses. Am. J. Vet. Res. 2007, 68, 760–771. [Google Scholar] [CrossRef]
- Cresswell, E.N.; Ruspi, B.D.; Wollman, C.W.; Peal, B.T.; Deng, S.; Toler, A.B.; McDonough, S.P.; Palmer, S.E.; Reesink, H.L. Determination of correlation of proximal sesamoid bone osteoarthritis with high-speed furlong exercise and catastrophic sesamoid bone fracture in Thoroughbred racehorses. Am. J. Vet. Res. 2021, 82, 467–477. [Google Scholar] [CrossRef]
- Anthenill, L.A.; Gardner, I.A.; Pool, R.R.; Garcia, T.C.; Stover, S.M. Comparison of macrostructural and microstructural bone features in Thoroughbred racehorses with and without midbody fracture of the proximal sesamoid bone. Am. J. Vet. Res. 2010, 71, 755–765. [Google Scholar] [CrossRef]
- Shaffer, S.K.; Shelly, K.; Garcia, T.C.; Samol, M.A.; Hill, A.E.; Fyhrie, D.P.; Stover, S.M. In vitro motions of the medial and lateral proximal sesamoid bones under mid-stance load conditions are consistent with racehorse fracture configurations. J. Biomech. 2022, 130, 110888. [Google Scholar] [CrossRef]
- Shaffer, S.K.; To, C.; Garcia, T.C.; Fyhrie, D.P.; Uzal, F.A.; Stover, S.M. Subchondral focal osteopenia associated with proximal sesamoid bone fracture in Thoroughbred racehorses. Equine Vet. J. 2021, 53, 294–305. [Google Scholar] [CrossRef]
- Beccati, F.; Gialletti, R.; Giontella, A.; Davanzo, S.; Di Meo, A.; Pepe, M. Morphologic Radiographic Study of the Proximal Sesamoid Bones of the Forelimb in Thoroughbred Racehorses in Training. Anat. Histol. Embryol. 2014, 43, 403–407. [Google Scholar] [CrossRef]
- Cresswell, E.N.; McDonough, S.P.; Palmer, S.E.; Hernandez, C.J.; Reesink, H.L. Can quantitative computed tomography detect bone morphological changes associated with catastrophic proximal sesamoid bone fracture in Thoroughbred racehorses? Equine Vet. J. 2019, 51, 123–130. [Google Scholar] [CrossRef]
- Shi, L.; Wang, D.; Riggs, C.M.; Qin, L.; Griffith, J.F. Statistical analysis of bone mineral density using voxel-based morphometry-an application on proximal sesamoid bones in racehorses. J. Orthop. Res. 2011, 29, 1230–1236. [Google Scholar] [CrossRef]
- Wang, D.; Shi, L.; Griffith, J.F.; Qin, L.; Yew, D.T.W.; Riggs, C.M. Comprehensive surface-based morphometry reveals the association of fracture risk and bone geometry. J. Orthop. Res. 2012, 30, 1277–1284. [Google Scholar] [CrossRef]
- Ayodele, B.A.; Hitchens, P.L.; Wong, A.S.M.; Mackie, E.J.; Whitton, R.C. Microstructural properties of the proximal sesamoid bones of Thoroughbred racehorses in training. Equine Vet. J. 2021, 53, 1169–1177. [Google Scholar] [CrossRef]
- Peloso, J.G.; Vogler, J.B.V.; Cohen, N.D.; Marquis, P.; Hilt, L. Association of catastrophic biaxial fracture of the proximal sesamoid bones with bony changes of the metacarpophalangeal joint identified by standing magnetic resonance imaging in cadaveric forelimbs of Thoroughbred racehorses. J. Am. Vet. Med. Assoc. 2015, 246, 661–673. [Google Scholar] [CrossRef]
- Kanis, J.A.; Borgstrom, F.; de Laet, C.; Johansson, H.; Johnell, O.; Jonsson, B.; Oden, A.; Zethraeus, N.; Pfleger, B.; Khaltaev, N. Assessment of fracture risk. Osteoporos. Int. 2005, 16, 581–589. [Google Scholar] [CrossRef]
- Loughridge, A.B.; Hess, A.M.; Parkin, T.D.; Kawcak, C.E. Qualitative assessment of bone density at the distal articulating surface of the third metacarpal in Thoroughbred racehorses with and without condylar fracture. Equine Vet. J. 2017, 49, 172–177. [Google Scholar] [CrossRef]
- Bogers, S.H.; Rogers, C.W.; Bolwell, C.; Roe, W.; Gee, E.; McIlwraith, C.W. Quantitative comparison of bone mineral density characteristics of the distal epiphysis of third metacarpal bones from Thoroughbred racehorses with or without condylar fracture. Am. J. Vet. Res. 2016, 77, 32–38. [Google Scholar] [CrossRef]
- Bogers, S.H.; Rogers, C.W.; Bolwell, C.F.; Roe, W.D.; Gee, E.K.; McIlwraith, C.W. Impact of race training on volumetric bone mineral density and its spatial distribution in the distal epiphysis of the third metatarsal bone of 2-year-old horses. Vet. J. 2014, 201, 353–358. [Google Scholar] [CrossRef]
- Yedavally-Yellayi, S.; Ho, A.M.; Patalinghug, E.M. Update on Osteoporosis. Prim. Care 2019, 46, 175–190. [Google Scholar] [CrossRef]
- Esmaeilzadeh, S.; Cesme, F.; Oral, A.; Yaliman, A.; Sindel, D. The utility of dual-energy X-ray absorptiometry, calcaneal quantitative ultrasound, and fracture risk indices (FRAX® and Osteoporosis Risk Assessment Instrument) for the identification of women with distal forearm or hip fractures: A pilot study. Endocr. Res. 2016, 41, 248–260. [Google Scholar] [CrossRef] [PubMed]
- Carstanjen, B.; Duboeuf, F.; Detilleux, J.; Lepage, O.M. Equine third metacarpal bone assessment by quantitative ultrasound and dual energy X-ray absorptiometry: An ex vivo study. J. Vet. Med. Ser. A 2003, 50, 42–47. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Unal, M.; Akkus, O. Raman spectral classification of mineral- and collagen-bound water’s associations to elastic and post-yield mechanical properties of cortical bone. Bone 2015, 81, 315–326. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Buckley, K.; Kerns, J.G.; Vinton, J.; Gikas, P.D.; Smith, C.; Parker, A.W.; Matousek, P.; Goodship, A.E. Towards the in vivo prediction of fragility fractures with Raman spectroscopy. J. Raman Spectrosc. 2015, 46, 610–618. [Google Scholar] [CrossRef] [Green Version]
- Heales, C.J.; Summers, I.R.; Fulford, J.; Knapp, K.M.; Winlove, C.P. Investigation of changes in bone density and chemical composition associated with bone marrow oedema-type appearances in magnetic resonance images of the equine forelimb. BMC Musculoskelet. Disord. 2019, 20, 330. [Google Scholar] [CrossRef] [Green Version]
- Morris, M.D.; Matousek, P.; Towrie, M.; Parker, A.W.; Goodship, A.E.; Draper, E.R.C. Kerr-gated time-resolved Raman spectroscopy of equine cortical bone tissue. J. Biomed. Opt. 2005, 10, 014014–0140147. [Google Scholar] [CrossRef] [Green Version]
- Davis, A.M.; Fan, X.; Shen, L.; Robinson, P.; Riggs, C.M. Improved radiological diagnosis of palmar osteochondral disease in the Thoroughbred racehorse. Equine Vet. J. 2017, 49, 454–460. [Google Scholar] [CrossRef]
- Anthenill, L.A.; Stover, S.M.; Gardner, I.A.; Hill, A.E.; Lee, C.M.; Anderson, M.L.; Barr, B.C.; Read, D.H.; Johnson, B.J.; Woods, L.W.; et al. Association between Findings on Palmarodorsal Radiographic Images and Detection of a Fracture in the Proximal Sesamoid Bones of Forelimbs Obtained from Cadavers of Racing Thoroughbreds. Am. J. Vet. Res. 2006, 67, 858–868. [Google Scholar] [CrossRef]
- Otsu, N. A Threshold Selection Method from Gray-Level Histograms. IEEE Trans. Syst. Man Cybern. 1979, 9, 62–66. [Google Scholar] [CrossRef] [Green Version]
- McIlwraith, C.W.; Frisbie, D.D.; Kawcak, C.E.; Fuller, C.J.; Hurtig, M.; Cruz, A. The OARSI histopathology initiative—Recommendations for histological assessments of osteoarthritis in the horse. Osteoarthr. Cartil. 2010, 18 (Suppl. 3), S93–S105. [Google Scholar] [CrossRef] [Green Version]
- Gamsjaeger, S.; Klaushofer, K.; Paschalis, E.P. Raman analysis of proteoglycans simultaneously in bone and cartilage. J. Raman Spectrosc. 2014, 45, 794–800. [Google Scholar] [CrossRef]
- Mandair, G.S.; Morris, M.D. Contributions of Raman spectroscopy to the understanding of bone strength. BoneKEy Rep. 2015, 4, 620. [Google Scholar] [CrossRef] [Green Version]
- Penel, G.; Delfosse, C.; Descamps, M.; Leroy, G. Composition of bone and apatitic biomaterials as revealed by intravital Raman microspectroscopy. Bone 2005, 36, 893–901. [Google Scholar] [CrossRef]
- Gamsjaeger, S.; Robins, S.P.; Tatakis, D.N.; Klaushofer, K.; Paschalis, E.P. Identification of Pyridinoline Trivalent Collagen Cross-Links by Raman Microspectroscopy. Calcif. Tissue Int. 2017, 100, 565–574. [Google Scholar] [CrossRef]
- Unal, M.; Uppuganti, S.; Leverant, C.J.; Creecy, A.; Granke, M.; Voziyan, P.; Nyman, J.S. Assessing glycation-mediated changes in human cortical bone with Raman spectroscopy. J. Biophotonics 2018, 11, e201700352. [Google Scholar] [CrossRef] [Green Version]
- Rokidi, S.; Paschalis, E.; Klaushofer, K.; Vennin, S.; Desyatova, A.; Turner, J.A.; Watson, P.; Lappe, J.; Akhter, M.P.; Recker, R.R. Organic matrix quality discriminates between age- and BMD-matched fracturing versus non-fracturing post-menopausal women: A pilot study. Bone 2019, 127, 207–214. [Google Scholar] [CrossRef]
- Gamsjaeger, S.; Srivastava, A.K.; Wergedal, J.E.; Zwerina, J.; Klaushofer, K.; Paschalis, E.P.; Tatakis, D.N. Altered bone material properties in HLA-B27 rats include reduced mineral to matrix ratio and altered collagen cross-links. J. Bone Miner. Res. 2014, 29, 2382–2391. [Google Scholar] [CrossRef]
- Verheyen, K.; Price, J.; Lanyon, L.; Wood, J. Exercise distance and speed affect the risk of fracture in racehorses. Bone 2006, 39, 1322–1330. [Google Scholar] [CrossRef]
- Whitton, R.C.; Trope, G.D.; Ghasem-Zadeh, A.; Anderson, G.A.; Parkin, T.D.H.; Mackie, E.J.; Seeman, E. Third metacarpal condylar fatigue fractures in equine athletes occur within previously modelled subchondral bone. Bone 2010, 47, 826–831. [Google Scholar] [CrossRef]
- Stepnik, M.W.; Radtke, C.L.; Scollay, M.C.; Oshel, P.E.; Albrecht, R.M.; Santschi, E.M.; Markel, M.D.; Muir, P. Scanning electron microscopic examination of third metacarpal/third metatarsal bone failure Surfaces in thoroughbred racehorses with condylar fracture. Vet. Surg. 2004, 33, 2–10. [Google Scholar] [CrossRef] [PubMed]
- Cohen, N.D.; Peloso, J.G.; Mundy, G.D.; Fisher, M.; Holland, R.E.; Little, T.V.; Misheff, M.M.; Watkins, J.P.; Honnas, C.M.; Moyer, W. Racing-related factors and results of prerace physical inspection and their association with musculoskeletal injuries incurred in thoroughbreds during races. J. Am. Vet. Med. Assoc. 1997, 211, 454–463. [Google Scholar] [PubMed]
- Whitton, R.C.; Ayodele, B.A.; Hitchens, P.L.; Mackie, E.J. Subchondral bone microdamage accumulation in distal metacarpus of Thoroughbred racehorses. Equine Vet. J. 2018, 50, 766–773. [Google Scholar] [CrossRef] [PubMed]
- Firth, E.C. The response of bone, articular cartilage and tendon to exercise in the horse. J. Anat. 2006, 208, 513–526. [Google Scholar] [CrossRef]
- Hiney, K.M.; Nielsen, B.D.; Rosenstein, D. Short-duration exercise and confinement alters bone mineral content and shape in weanling horses. J. Anim. Sci. 2004, 82, 2313–2320. [Google Scholar] [CrossRef] [Green Version]
- Noble, P.; Singer, E.R.; Jeffery, N.S. Does subchondral bone of the equine proximal phalanx adapt to race training? J. Anat. 2016, 229, 104–113. [Google Scholar] [CrossRef] [Green Version]
- Kristoffersen, M.; Parkin, T.D.H.; Singer, E.R. Catastrophic biaxial proximal sesamoid bone fractures in UK Thoroughbred races (1999–2004): Horse characteristics and racing history. Equine Vet. J. 2010, 42, 420–424. [Google Scholar] [CrossRef]
- Martig, S.; Hitchens, P.L.; Stevenson, M.A.; Whitton, R.C. Subchondral bone morphology in the metacarpus of racehorses in training changes with distance from the articular surface but not with age. J. Anat. 2018, 232, 919–930. [Google Scholar] [CrossRef]
- Boyde, A.; Firth, E.C. Musculoskeletal responses of 2-year-old Thoroughbred horses to early training. Quantitative back-scattered electron scanning electron microscopy and confocal fluorescence microscopy of the epiphysis of the third metacarpal bone. N. Z. Vet. J. 2005, 53, 123–132. [Google Scholar] [CrossRef]
- Firth, E.C.; Rogers, C.W.; Doube, M.; Jopson, N.B. Musculoskeletal responses of 2-year-old Thoroughbred horses to early training. 6. Bone parameters in the third metacarpal and third metatarsal bones. N. Z. Vet. J. 2005, 53, 101–112. [Google Scholar] [CrossRef]
- Pinchbeck, G.L.; Clegg, P.D.; Boyde, A.; Riggs, C.M. Pathological and clinical features associated with palmar/plantar osteochondral disease of the metacarpo/metatarsophalangeal joint in Thoroughbred racehorses. Equine Vet. J. 2013, 45, 587–592. [Google Scholar] [CrossRef] [Green Version]
- Muir, P.; Peterson, A.L.; Sample, S.J.; Scollay, M.C.; Markel, M.D.; Kalscheur, V.L. Exercise-induced metacarpophalangeal joint adaptation in the Thoroughbred racehorse. J. Anat. 2008, 213, 706–717. [Google Scholar] [CrossRef] [PubMed]
- Pawlak, A.M.; Beattie, J.R.; Glenn, J.V.; Stitt, A.W.; McGarvey, J.J. Raman spectroscopy of advanced glycation end products (AGEs), possible markers for progressive retinal dysfunction. J. Raman Spectrosc. 2008, 39, 1635–1642. [Google Scholar] [CrossRef]
- Ruppel, M.E.; Burr, D.B.; Miller, L.M. Chemical makeup of microdamaged bone differs from undamaged bone. Bone 2006, 39, 318–324. [Google Scholar] [CrossRef]
- Bacchetta, J.; Farlay, D.; Abelin-Genevois, K.; Lebourg, L.; Cochat, P.; Boivin, G. Bone impairment in oxalosis: An ultrastructural bone analysis. Bone 2015, 81, 161–167. [Google Scholar] [CrossRef]
- Paschalis, E.P.; Gamsjaeger, S.; Klaushofer, K. Vibrational spectroscopic techniques to assess bone quality. Osteoporos. Int. 2017, 28, 2275–2291. [Google Scholar] [CrossRef]
- Luedke, L.K.; Ilevbare, P.; Noordwijk, K.J.; Palomino, P.M.; McDonough, S.P.; Palmer, S.E.; Basran, P.S.; Donnelly, E.; Reesink, H.L. Proximal sesamoid bone microdamage is localized to articular subchondral regions in Thoroughbred racehorses, with similar fracture toughness between fracture and controls. Vet. Surg. 2022, 51, 952–962. [Google Scholar] [CrossRef]
- Basran, P.S.; Gao, J.; Palmer, S.; Reesink, H.L. A radiomics platform for computing imaging features from µCT images of Thoroughbred racehorse proximal sesamoid bones: Benchmark performance and evaluation. Equine Vet. J. 2021, 53, 277–286. [Google Scholar] [CrossRef]
- Sowoidnich, K.; Churchwell, J.H.; Buckley, K.; Goodship, A.E.; Parker, A.W.; Matousek, P. Photon migration of Raman signal in bone as measured with spatially offset Raman spectroscopy. J. Raman Spectrosc. 2016, 47, 240–247. [Google Scholar] [CrossRef] [Green Version]
- Hernandez, C.J.; Beaupré, G.S.; Keller, T.S.; Carter, D.R. The influence of bone volume fraction and ash fraction on bone strength and modulus. Bone 2001, 29, 74–78. [Google Scholar] [CrossRef]
- Rubin, M.R.; Paschalis, E.P.; Poundarik, A.; Sroga, G.E.; McMahon, D.J.; Gamsjaeger, S.; Klaushofer, K.; Vashishth, D. Advanced glycation endproducts and bone material properties in type 1 diabetic mice. PLoS ONE 2016, 11, e0154700. [Google Scholar]
- Spriet, M.; Espinosa-Mur, P.; Cissell, D.D.; Phillips, K.L.; Arino-Estrada, G.; Beylin, D.; Stepanov, P.; Katzman, S.A.; Galuppo, L.D.; Garcia-Nolen, T.; et al. 18 F-sodium fluoride positron emission tomography of the racing Thoroughbred fetlock: Validation and comparison with other imaging modalities in nine horses. Equine Vet. J. 2019, 51, 375–383. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kazanci, M.; Roschger, P.; Paschalis, E.P.; Klaushofer, K.; Fratzl, P. Bone osteonal tissues by Raman spectral mapping: Orientation–composition. J. Struct. Biol. 2006, 156, 489–496. [Google Scholar] [CrossRef] [PubMed]
- Roschger, A.; Gamsjaeger, S.; Hofstetter, B.; Masic, A.; Blouin, S.; Messmer, P.; Berzlanovich, A.; Paschalis, E.P.; Roschger, P.; Klaushofer, K.; et al. Relationship between the v2PO4/amide III ratio assessed by Raman spectroscopy and the calcium content measured by quantitative backscattered electron microscopy in healthy human osteonal bone. J. Biomed. Opt. 2014, 19, 065002. [Google Scholar] [CrossRef]
- Taylor, E.A.; Lloyd, A.A.; Salazar-Lara, C.; Donnelly, E. Raman and Fourier Transform Infrared (FT-IR) Mineral to Matrix Ratios Correlate with Physical Chemical Properties of Model Compounds and Native Bone Tissue. Appl. Spectrosc. 2017, 71, 2404–2410. [Google Scholar] [CrossRef]
- Penel, G.; Leroy, G.; Rey, C.; Bres, E. MicroRaman Spectral Study of the PO4 and CO3 Vibrational Modes in Synthetic and Biological Apatites. Calcif. Tissue Int. 1998, 63, 475–481. [Google Scholar] [CrossRef]
- Awonusi, A.; Morris, M.D.; Tecklenburg, M.M.J. Carbonate Assignment and Calibration in the Raman Spectrum of Apatite. Calcif. Tissue Int. 2007, 81, 46–52. [Google Scholar] [CrossRef]
- Kazanci, M.; Fratzl, P.; Klaushofer, K.; Paschalis, E.P. Complementary Information on In Vitro Conversion of Amorphous (Precursor) Calcium Phosphate to Hydroxyapatite from Raman Microspectroscopy and Wide-Angle X-ray Scattering. Calcif. Tissue Int. 2006, 79, 354–359. [Google Scholar] [CrossRef]
- Paschalis, E.; Gamsjaeger, S.; Hassler, N.; Klaushofer, K.; Burr, D. Ovarian hormone depletion affects cortical bone quality differently on different skeletal envelopes. Bone 2017, 95, 55–64. [Google Scholar] [CrossRef] [PubMed]
- Crane, N.J.; Popescu, V.; Morris, M.D.; Steenhuis, P.; Ignelzi, M.A. Raman spectroscopic evidence for octacalcium phosphate and other transient mineral species deposited during intramembranous mineralization. Bone 2006, 39, 434–442. [Google Scholar] [CrossRef]
- Mendes, T.O.; dos Santos, L.; Silva, M.G.; Pereira, L.; Fávero, P.; Singh, P.; Martin, A.A. Combined in vivo confocal Raman spectroscopy and density functional theory to detect carboxymethyl(lysine) in the human stratum corneum. Vib. Spectrosc. 2019, 100, 40–47. [Google Scholar]
- Dehring, K.A.; Crane, N.J.; Smukler, A.R.; McHugh, J.B.; Roessler, B.J.; Morris, M.D. Identifying Chemical Changes in Subchondral Bone Taken from Murine Knee Joints Using Raman Spectroscopy. Appl. Spectrosc. 2006, 60, 1134–1141. [Google Scholar] [CrossRef]
Exercise History Variable | Fracture | Control | p-Value |
---|---|---|---|
Age at first start | 2 years (2 years) | 2 years (2 to 3 years) | 0.16 |
Career duration | 64 (0 to 193) weeks | 69 (12 to 212) weeks | 0.92 |
Race starts | 7.5 (0 to 28) | 5 (0 to 40) | 0.95 |
Cumulative total furlongs | 190 (0 to 384) | 146 (36 to 520) | 0.91 |
Career work weeks | 40.5 (5 to 96) | 32 (8 to 95) | 0.76 |
Career rest weeks | 34 (2 to 112) | 35 (4 to 123) | 0.95 |
Career work:rest ratio | 1.25 (0.59 to 2.35) | 1.07 (0.54 to 2.45) | 0.30 |
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Noordwijk, K.J.; Chen, L.; Ruspi, B.D.; Schurer, S.; Papa, B.; Fasanello, D.C.; McDonough, S.P.; Palmer, S.E.; Porter, I.R.; Basran, P.S.; et al. Metacarpophalangeal Joint Pathology and Bone Mineral Density Increase with Exercise but Not with Incidence of Proximal Sesamoid Bone Fracture in Thoroughbred Racehorses. Animals 2023, 13, 827. https://doi.org/10.3390/ani13050827
Noordwijk KJ, Chen L, Ruspi BD, Schurer S, Papa B, Fasanello DC, McDonough SP, Palmer SE, Porter IR, Basran PS, et al. Metacarpophalangeal Joint Pathology and Bone Mineral Density Increase with Exercise but Not with Incidence of Proximal Sesamoid Bone Fracture in Thoroughbred Racehorses. Animals. 2023; 13(5):827. https://doi.org/10.3390/ani13050827
Chicago/Turabian StyleNoordwijk, Kira J., Leyi Chen, Bianca D. Ruspi, Sydney Schurer, Brittany Papa, Diana C. Fasanello, Sean P. McDonough, Scott E. Palmer, Ian R. Porter, Parminder S. Basran, and et al. 2023. "Metacarpophalangeal Joint Pathology and Bone Mineral Density Increase with Exercise but Not with Incidence of Proximal Sesamoid Bone Fracture in Thoroughbred Racehorses" Animals 13, no. 5: 827. https://doi.org/10.3390/ani13050827
APA StyleNoordwijk, K. J., Chen, L., Ruspi, B. D., Schurer, S., Papa, B., Fasanello, D. C., McDonough, S. P., Palmer, S. E., Porter, I. R., Basran, P. S., Donnelly, E., & Reesink, H. L. (2023). Metacarpophalangeal Joint Pathology and Bone Mineral Density Increase with Exercise but Not with Incidence of Proximal Sesamoid Bone Fracture in Thoroughbred Racehorses. Animals, 13(5), 827. https://doi.org/10.3390/ani13050827