Radiographic Texture of the Trabecular Bone in the Proximal Phalanx of Horses
Keywords:
Fractal analysis, fractal dimension, bone area fraction, lacunarity, trabecular bone, horsesAbstract
Trabecular bone is highly dynamic in response to external and internal stimuli, and changes in its structure can be quantified through fractal analysis. However, fractal analysis is still an incipient technique in equine research. This study aimed to evaluate the complexity, heterogeneity, and density of the trabecular bone of the proximal phalanx (P1) of healthy adult horses of different breeds and sexes by measuring the values of fractal dimension (FD), lacunarity, and bone area fraction (BA/TA) in 65 radiographic examinations of the metacarpophalangeal joint and evaluate the agreement between the BoneJ and FracLac plugins for measuring FD. Regions of interest of 50 × 50 pixels were manually selected on the trabecular bone in the proximal epiphysis of the P1. No differences were observed for FD, lacunarity, and BA/TA between horses of different breeds and sexes (p > 0.1). The BoneJ and FracLac plugins showed no agreement when measuring FD (p < 0.01). Therefore, the radiographic texture of the trabecular bone of the P1 in horses had no influence depending on the analyzed breed or sex. The FracLac plugin measured higher FD values, and hence standardization using the BoneJ plugin is recommended. Further studies are required to evaluate other breeds, age groups, and training levels.
References
Podsiadlo P, Dahl L, Englund M, Lohmander LS, Stachowiak GW. Differences in trabecular bone texture between knees with and without radiographic osteoarthritis detected by fractal methods. Osteoarthritis and Cartilage 2008;16:323–9. https://doi.org/10.1016/j.joca.2007.07.010.
Fazzalari NL, Parkinson IH. Fractal properties of subchondral cancellous bone in severe osteoarthritis of the hip. Journal of Bone and Mineral Research 1997;12:632–40. https://doi.org/10.1359/jbmr.1997.12.4.632.
Kivell TL. A review of trabecular bone functional adaptation: what have we learned from trabecular analyses in extant hominoids and what can we apply to fossils? Journal of Anatomy 2016;228:569–94. https://doi.org/10.1111/joa.12446.
Saers JPP, Ryan TM, Stock JT. Trabecular bone functional adaptation and sexual dimorphism in the human foot. American Journal of Physical Anthropology 2019;168:154–69. https://doi.org/10.1002/ajpa.23732.
Jolley L, Majumdar S, Kapila S. Technical factors in fractal analysis of periapical radiographs. Dentomaxillofacial Radiology 2006;35:393–7. https://doi.org/10.1259/dmfr/30969642.
Parkinson, Fazzalari. Methodological principles for fractal analysis of trabecular bone. Journal of Microscopy 2000;198:134–42. https://doi.org/10.1046/j.1365-2818.2000.00684.x.
Alberich‐Bayarri A, Marti‐Bonmati L, Pérez MA, Sanz‐Requena R, Lerma‐Garrido JJ, García‐Martí G, et al. Assessment of 2D and 3D fractal dimension measurements of trabecular bone from high‐spatial resolution magnetic resonance images at 3 T. Medical Physics 2010;37:4930–7. https://doi.org/10.1118/1.3481509.
Rabelo GD, Roux J-P, Portero-Muzy N, Gineyts E, Chapurlat R, Chavassieux P. Cortical Fractal Analysis and Collagen Crosslinks Content in Femoral Neck After Osteoporotic Fracture in Postmenopausal Women: Comparison with Osteoarthritis. Calcified Tissue International 2018;102:644–50. https://doi.org/10.1007/s00223-017-0378-9.
Chirchir H, Ruff CB, Junno J, Potts R. Low trabecular bone density in recent sedentary modern humans. American Journal of Physical Anthropology 2017;162:550–60. https://doi.org/10.1002/ajpa.23138.
Maquer G, Musy SN, Wandel J, Gross T, Zysset PK. Bone volume fraction and fabric anisotropy are better determinants of trabecular bone stiffness than other morphological variables. Journal of Bone and Mineral Research 2015;30:1000–8. https://doi.org/10.1002/jbmr.2437.
Saers JPP, DeMars LJ, Stephens NB, Jashashvili T, Carlson KJ, Gordon AD, et al. Automated resolution independent method for comparing in vivo and dry trabecular bone. American Journal of Physical Anthropology 2020;174:822–31. https://doi.org/10.1002/ajpa.24181.
Kato CN, Barra SG, Tavares NP, Amaral TM, Brasileiro CB, Mesquita RA, et al. Use of fractal analysis in dental images: a systematic review. Dento Maxillo Facial Radiology 2020;49:20180457–20180457. https://doi.org/10.1259/dmfr.20180457.
Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 2012;9:671–5. https://doi.org/10.1038/nmeth.2089.
Yamada ALM, do Prado Vendruscolo C, Marsiglia MF, Sotelo EDP, Agreste FR, Seidel SRT, et al. Effects of oral treatment with chondroitin sulfate and glucosamine in an experimental model of metacarpophalangeal osteoarthritis in horses. BMC Veterinary Research 2022;18:215–215. https://doi.org/10.1186/s12917-022-03323-3.
Yamada ALM, Pinheiro M, Marsiglia MF, Hagen SCF, Baccarin RYA, da Silva LCLC. Ultrasound and clinical findings in the metacarpophalangeal joint assessment of show jumping horses in training. Journal of Veterinary Science 2020;21:e21–e21. https://doi.org/10.4142/jvs.2020.21.e21.
de Souza AF, Pereira CAM, Costa C, Fürst A, Kümmerle JM, De Zoppa ALV. Mechanical properties and failure mode of proximal screw fixation technique using locking compression plate for proximal interphalangeal arthrodesis in horses: an ex vivo study. Veterinary and Comparative Orthopaedics and Traumatology 2024. https://doi.org/10.1055/s-0044-1787680.
Pereira L de O, De Souza AF, Spagnolo JD, Yamada ALM, Salgado DMR de A, De Zoppa AL do V. Radiographic texture of the trabecular bone of the proximal phalanx in horses with metacarpophalangeal osteoarthritis. Journal of Equine Science 2024;35:21–8. https://doi.org/10.1294/jes.35.21.
Santos IG, Ramos de Faria F, da Silva Campos MJ, de Barros BÁC, Rabelo GD, Devito KL. Fractal dimension, lacunarity, and cortical thickness in the mandible: Analyzing differences between healthy men and women with cone-beam computed tomography. Imaging Science in Dentistry 2023;53:153–9. https://doi.org/10.5624/isd.20230042.
Martin Bland J, Altman DouglasG. Statistical methods for assessing agreement between two methods of clinical measurement. The Lancet 1986;327:307–10. https://doi.org/10.1016/s0140-6736(86)90837-8.
Datta D. blandr: Bland-Altman Method Comparison. CRAN: Contributed Packages 2017. https://doi.org/10.32614/cran.package.blandr.
Anne‐Archard N, Martel G, Fogarty U, Richard H, Beauchamp G, Laverty S. Differences in third metacarpal trabecular microarchitecture between the parasagittal groove and condyle at birth and in adult racehorses. Equine Veterinary Journal 2018;51:115–22. https://doi.org/10.1111/evj.12980.
Ayodele BA, Hitchens PL, Wong ASM, Mackie EJ, Whitton RC. Microstructural properties of the proximal sesamoid bones of Thoroughbred racehorses in training. Equine Veterinary Journal 2020;53:1169–77. https://doi.org/10.1111/evj.13394.
Huiskes R, Ruimerman R, van Lenthe GH, Janssen JD. Effects of mechanical forces on maintenance and adaptation of form in trabecular bone. Nature 2000;405:704–6. https://doi.org/10.1038/35015116.
Martig S, Hitchens PL, Lee PVS, Whitton RC. The relationship between microstructure, stiffness and compressive fatigue life of equine subchondral bone. Journal of the Mechanical Behavior of Biomedical Materials 2020;101:103439. https://doi.org/10.1016/j.jmbbm.2019.103439.
Marsiglia MF, Yamada ALM, Agreste FR, de Sá LRM, Nieman RT, da Silva LCLC. Morphological analysis of third metacarpus cartilage and subchondral bone in Thoroughbred racehorses: an ex vivo study. The Anatomical Record 2022;305:3385–97. https://doi.org/10.1002/ar.24918.
Moshage SG, McCoy AM, Polk JD, Kersh ME. Temporal and spatial changes in bone accrual, density, and strain energy density in growing foals. Journal of the Mechanical Behavior of Biomedical Materials 2020;103:103568. https://doi.org/10.1016/j.jmbbm.2019.103568.
Noordwijk KJ, Chen L, Ruspi BD, Schurer S, Papa B, Fasanello DC, 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 (Basel) 2023;13:827. https://doi.org/10.3390/ani13050827.
Rajão MD, Leite CS, Nogueira K, Godoy RF, Lima EMM. The bone response in endurance long distance horse. Open Veterinary Journal 2019;9:58–64. https://doi.org/10.4314/ovj.v9i1.11.
Jackson BF, Dyson PK, Hattersley RD, Kelly HR, Pfeiffer DU, Price JS. Relationship between stages of the estrous cycle and bone cell activity in Thoroughbreds. American Journal of Veterinary Research 2006;67:1527–32. https://doi.org/10.2460/ajvr.67.9.1527.
Chiappe A, Gonzalez G, Fradinger E, Iorio G, Ferretti JL, Zanchetta J. Influence of age and sex in serum osteocalcin levels in Thoroughbred horses. Archives of Physiology and Biochemistry 1999;107:50–4. https://doi.org/10.1076/apab.107.1.50.4357.
Lemazurier E, Pierre Toquet M, Fortier G, Séralini GE. Sex steroids in serum of prepubertal male and female horses and correlation with bone characteristics. Steroids 2002;67:361–9. https://doi.org/10.1016/s0039-128x(01)00190-8.
Prado Filho JRC do, Sterman F de A. [Assessment of bone mineral density in Thoroughbred foals at the beginning of training]. Brazilian Journal of Veterinary Research and Animal Science 2004;41. https://doi.org/10.1590/s1413-95962004000600005.
Jackson BF, Lonnell C, Verheyen K, Wood JLN, Pfeiffer DU, Price JS. Gender differences in bone turnover in 2-year-old thoroughbreds. Equine Veterinary Journal 2003;35:702–6. https://doi.org/10.2746/042516403775696230.
Fazzalari NL, Parkinson IH. Fractal dimension and architecture of trabecular bone. The Journal of Pathology 1996;178:100–5. https://doi.org/10.1002/(sici)1096-9896(199601)178:1<100::aid-path429>3.0.co;2-k.
Yaşar F, Akgünlü F. Fractal dimension and lacunarity analysis of dental radiographs. Dentomaxillofacial Radiology 2005;34:261–7. https://doi.org/10.1259/dmfr/85149245.
White SC, Rudolph DJ. Alterations of the trabecular pattern of the jaws in patients with osteoporosis. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology 1999;88:628–35. https://doi.org/10.1016/s1079-2104(99)70097-1.
Lopes R, Betrouni N. Fractal and multifractal analysis: A review. Medical Image Analysis 2009;13:634–49. https://doi.org/10.1016/j.media.2009.05.003.
Karperien A. Welcome to the User's Guide for FracLac, V. 2.5. FracLac for Imagej n.d. https://imagej.net/ij/plugins/fraclac/FLHelp/Introduction.htm (accessed July 25, 2024).
Doube M, Kłosowski MM, Arganda-Carreras I, Cordelières FP, Dougherty RP, Jackson JS, et al. BoneJ: Free and extensible bone image analysis in ImageJ. Bone 2010;47:1076–9. https://doi.org/10.1016/j.bone.2010.08.023.
Bianchi J, Gonçalves JR, Ruellas AC de O, Vimort J-B, Yatabe M, Paniagua B, et al. Software comparison to analyze bone radiomics from high resolution CBCT scans of mandibular condyles. Dento Maxillo Facial Radiology 2019;48:20190049–20190049. https://doi.org/10.1259/dmfr.20190049.
Malhan D, Muelke M, Rosch S, Schaefer AB, Merboth F, Weisweiler D, et al. An optimized approach to perform bone histomorphometry. Frontiers in Endocrinology 2018;9:666–666. https://doi.org/10.3389/fendo.2018.00666.
Barak MM, Lieberman DE, Hublin J-J. A Wolff in sheep's clothing: Trabecular bone adaptation in response to changes in joint loading orientation. Bone 2011;49:1141–51. https://doi.org/10.1016/j.bone.2011.08.020.
Doershuk LJ, Saers JPP, Shaw CN, Jashashvili T, Carlson KJ, Stock JT, et al. Complex variation of trabecular bone structure in the proximal humerus and femur of five modern human populations. American Journal of Physical Anthropology 2019;168:104–18. https://doi.org/10.1002/ajpa.23725.
Hayward MA, Kharode YP, Becci MM, Kowal D. The effect of conjugated equine estrogens on ovariectomy-induced osteopenia in the rat. Agents and Actions 1990;31:152–6. https://doi.org/10.1007/bf02003236.
Basavarajappa S, Konddajji Ramachandra V, Kumar S. Fractal dimension and lacunarity analysis of mandibular bone on digital panoramic radiographs of tobacco users. Journal of Dental Research, Dental Clinics, Dental Prospects 2021;15:140–6. https://doi.org/10.34172/joddd.2021.024.
Dougherty G, Henebry GM. Lacunarity analysis of spatial pattern in CT images of vertebral trabecular bone for assessing osteoporosis. Medical Engineering & Physics 2002;24:129–38. https://doi.org/10.1016/s1350-4533(01)00106-0.
Sindeaux R, Figueiredo PT de S, de Melo NS, Guimarães ATB, Lazarte L, Pereira FB, et al. Fractal dimension and mandibular cortical width in normal and osteoporotic men and women. Maturitas 2014;77:142–8. https://doi.org/10.1016/j.maturitas.2013.10.011.
Zaia A, Rossi R, Galeazzi R, Sallei M, Maponi P, Scendoni P. Fractal lacunarity of trabecular bone in vertebral MRI to predict osteoporotic fracture risk in over-fifties women. The LOTO study. BMC Musculoskeletal Disorders 2021;22:108–108. https://doi.org/10.1186/s12891-021-03966-7.
Zandieh S, Haller J, Bernt R, Hergan K, Rath E. Fractal analysis of subchondral bone changes of the hand in rheumatoid arthritis. Medicine 2017;96:e6344–e6344. https://doi.org/10.1097/MD.0000000000006344.
He T, Cao C, Xu Z, Li G, Cao H, Liu X, et al. A comparison of micro-CT and histomorphometry for evaluation of osseointegration of PEO-coated titanium implants in a rat model. Scientific Reports 2017;7:16270–16270. https://doi.org/10.1038/s41598-017-16465-4.
de Souza Santos D, dos Santos LCB, de Albuquerque Tavares Carvalho A, Leão JC, Delrieux C, Stosic T, et al. Multifractal spectrum and lacunarity as measures of complexity of osseointegration. Clinical Oral Investigations 2015;20:1271–8. https://doi.org/10.1007/s00784-015-1606-1.
Cordeiro MS, Backes AR, Júnior AFD, Gonçalves EHG, de Oliveira JX. Fibrous dysplasia characterization using lacunarity analysis. Journal of Digital Imaging 2016;29:134–40. https://doi.org/10.1007/s10278-015-9815-3.
Akkari H, Bhouri I, Dubois P, Bedoui MH. On the relations between 2D and 3D fractal dimensions: theoretical approach and clinical application in bone imaging. Mathematical Modelling of Natural Phenomena 2008;3:48–75. https://doi.org/10.1051/mmnp:2008081.
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