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PloS one2019; 14(7); e0219900; doi: 10.1371/journal.pone.0219900

Growth patterns, metabolic indicators and osteoarticular status in the Lusitano horse: A longitudinal study.

Abstract: Development of a healthy musculoskeletal system is of high concern for horse breeders and users. A longitudinal field study was performed in order to: (i) evaluate growth patterns and long-term changes on bone quality, bone metabolism, growth factors and metabolic variables in the Lusitano horse; and (ii) retrospectively assess whether these changes were related with radiographic findings regarding osteochondrosis-like lesions (OC) at the onset of training. Thirty-four Lusitano foals born and raised at four stud-farms, were periodically weighed (BW), and measured (withers height-WH) from birth to 36 months of age. On the same days, blood samples were collected for determination of osteocalcin, bone alkaline phosphatase, insulin-like growth factor I (IGF-I), leptin, insulin, glucose, parathyroid hormone (PTH), calcium, phosphorus and magnesium plasma concentrations, and quantitative ultrasound measurements were performed on the right third metacarpal bone (McIII). At the end of the study horses underwent radiographic examination of the four fetlocks, hocks and stifles. According to their radiographic status (OC negative vs. OC positive), Richards growth function was adjusted to BW and WH data. Instantaneous BW and WH growth rates (BW IADG and WH IADG) were calculated for each foal, from the resolution of the first derivative of growth models for seven age-classes. The presence of radiographic findings compatible with OC at the onset of training was associated with changes in BW and WH growth rates. Positive horses presented higher BW IADG from six to 18 months of age and lower WH IADG before 45 days of age (P<0.001). Speed of sound measurements (SOS), bone markers, growth factors and other metabolic variables change markedly with age (P<0.01). OC positive horses tended to have lower SOS values at the lateral region of McIII, lower IGF-I, and higher insulin and PTH concentrations (P<0.1). This study provides indirect evidence that monitoring foals' growth during the first year of life may be of assistance in managing the occurrence of OC. Further studies with a higher number of animals and a controlled feed intake should be pursued.
Publication Date: 2019-07-17 PubMed ID: 31314780PubMed Central: PMC6636759DOI: 10.1371/journal.pone.0219900Google Scholar: Lookup
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  • Journal Article
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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.

The research article aims to study the growth patterns, metabolism, and bone health in Lusitano horses and to investigate if these elements are related to the occurrence of bone lesions at the start of their training.

Study Design and Procedure

  • The study was longitudinal, that is, it observed and ideated on a group of 34 Lusitano foals for a period of 36 months (3 years).
  • The foals were weighed and measured regularly, and blood samples were taken at every stage to study various bone metabolism and growth factors such as osteocalcin, bone alkaline phosphatase, insulin-like growth factor I (IGF-I), leptin, insulin, glucose, parathyroid hormone (PTH), calcium, phosphorus and magnesium plasma concentrations.
  • Also, the researchers carried out an ultrasound of each foal’s right third metacarpal bone (McIII) and finally conducted a radiographic examination of their four fetlocks, hocks and stifles at the conclusion of the study.

Findings and Implications

  • The results showed that changes in the weight and height growth rates of the foals were linked to the presence of the bone lesions (osteochondrosis-like lesions or OC).
  • Horses with these lesions showed higher weight growth rates between the ages of six and 18 months, and lower height growth rates before 45 days of age.
  • Additionally, these OC-positive horses showed a potential trend of having lower ultrasound speed-of-sound values at the lateral region of their third metacarpal bone, lower insulin-like growth factor (IGF-I) levels, and higher insulin and parathyroid hormone concentrations.
  • The study implies that regular monitoring of growth during the first year of a Lusitano foal’s life could help in managing the occurrence of osteochondrosis, a condition that can cause pain and joint issues.
  • However, to confirm and understand these findings in greater depth, further studies with a larger group of horses and regulated feeding intake should be carried out by the researchers.

Cite This Article

APA
Fradinho MJ, Mateus L, Bernardes N, Bessa RJB, Caldeira RM, Ferreira-Dias G. (2019). Growth patterns, metabolic indicators and osteoarticular status in the Lusitano horse: A longitudinal study. PLoS One, 14(7), e0219900. https://doi.org/10.1371/journal.pone.0219900

Publication

ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 14
Issue: 7
Pages: e0219900

Researcher Affiliations

Fradinho, Maria J
  • Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, Lisboa, Portugal.
Mateus, Luísa
  • Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, Lisboa, Portugal.
Bernardes, Nuno
  • Faculty of Veterinary Medicine, University of Lisbon, Lisboa, Portugal.
Bessa, Rui J B
  • Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, Lisboa, Portugal.
Caldeira, Rui M
  • Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, Lisboa, Portugal.
Ferreira-Dias, Graça
  • Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, Lisboa, Portugal.

MeSH Terms

  • Animals
  • Biomarkers
  • Body Weights and Measures
  • Bone Development / genetics
  • Cartilage, Articular / growth & development
  • Cartilage, Articular / metabolism
  • Female
  • Horses
  • Longitudinal Studies
  • Male

Conflict of Interest Statement

The authors have declared that no competing interests exist.

References

This article includes 72 references
  1. Martin-Rosset W. Growth and development in the equine. .
  2. Valette J-P, Robert C, Denoix J-M. Use of linear and non-linear functions to describe the growth of young sport- and race-horses born in Normandie. Animal 2008; 2: 560–5.
    doi: 10.1017/S1751731107001462pubmed: 22443570google scholar: lookup
  3. Kocher A, Staniar WB. The pattern of thoroughbred growth is affected by foal’s birth date. Livest Sci 2013; 154: 204–14.
  4. Fradinho MJ, Bessa RJB, Ferreira-Dias G, Caldeira RM. Growth and development of the Lusitano horse managed on grazing systems. Livest Sci 2016; 186: 22–8.
  5. Thompson KN, Baker JP, Jackson SG. The influence of supplemental feed on growth and bone development of nursing foals. J. Anim. Sci. 1988; 66: 1692–6.
    doi: 10.2527/jas1988.6671692xpubmed: 3403399google scholar: lookup
  6. Cymbaluk NF, Christison GI, Leach DH. Longitudinal growth analysis of horses following limited and ad libitum feeding. Equine Vet J 1990; 22: 198–204.
    pubmed: 2361509
  7. Sandgren B, Dalin G, Carlsten J, Lundeheim N. Osteochondrosis in the tarsocrural joint and osteochondral fragments in the fetlock joints in Standardbred trotters. II. Body measurements and clinical findings. Equine Vet J 1993; Suppl: 48–53.
  8. van Weeren PR, Sloet van Oldruitenborgh-Oosterbaan M, 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 1999; Suppl: 26–30.
    pubmed: 10999657
  9. van Weeren PR, Jeffcott LB. Problems and pointers in osteochondrosis: twenty years on. Vet J 2013; 197: 96–102.
    doi: 10.1016/j.tvjl.2013.03.048pubmed: 23639371google scholar: lookup
  10. Dik KJ, Enzerink E, van Weeren PR. Radiographic development of osteochondral abnormalities in the hock and stifle of Dutch Warmblood foals, from age 1 to 11 months. Equine Vet J 1999; 31: 9–15.
    pubmed: 10999655
  11. Denoix J-M, Jeffcott LB, McIlwraith CW, van Weeren PR. A review of terminology for equine juvenile osteochondral conditions (JOCC) based on anatomical and functional considerations. Vet J 2013; 197: 29–35.
    doi: 10.1016/j.tvjl.2013.03.038pubmed: 23683533google scholar: lookup
  12. Barneveld A, van Weeren PR. Conclusions regarding the influence of exercise on the development of the equine musculoskeletal system with special reference to osteochondrosis. Equine Vet J 1999; Suppl. 31: 112–9.
    pubmed: 10999670
  13. Donabédian M, Fleurance G, Perona G, Robert C, Lepage O, Trillaud-Geyl C. Effect of fast vs. moderate growth rate related to nutrient intake on developmental orthopaedic disease in the horse. Animal Res 2006; 55: 471–86.
  14. Ytrehus B, Carlson CS, Ekman S. Etiology and pathogenesis of osteochondrosis. Vet Pathol 2007;44: 429–48.
    doi: 10.1354/vp.44-4-429pubmed: 17606505google scholar: lookup
  15. Distl O. The genetics of equine osteochondrosis. Vet J 2013;197: 13–8.
    doi: 10.1016/j.tvjl.2013.03.036pubmed: 23809989google scholar: lookup
  16. Lepage O, Carstanjen B, Uebelhart D. Non-invasive assessment of equine bone: an update. Vet J 2001;161: 10–23.
    doi: 10.1053/tvjl.2000.0541pubmed: 11145827google scholar: lookup
  17. Carstanjen B, Lepage O, Detilleux J, Duboeuf F, Amory H. Use of multisite quantitative ultrasonography for non-invasive assessment of bone in horses. Am J Vet Res 2002;63: 1464–9.
    pubmed: 12371776
  18. Carstanjen B, Lepage O, Hars O, Langlois P, Duboeuf F, Amory H. Speed of sound measurements of the third metacarpal bone in young exercising Thoroughbred racehorses. Bone 2003;33: 411–8.
    pubmed: 13678783
  19. Fradinho MJ, Vale AC, Bernardes N, Caldeira RM, Vaz MF, Ferreira-Dias G. Biomechanical properties of the equine third metacarpal bone: in vivo quantitative ultrasonography vs ex vivo compression and bending techniques. J Equine Vet Sci 2015;35: 198–205.
  20. Price J, Jackson B, Gray J, Harris P, Wright I, Pfeiffer D. Biochemical markers of bone metabolism in growing thoroughbreds: a longitudinal study. Res Vet Sci 2001;71: 1–9.
    doi: 10.1053/rvsc.2001.0496pubmed: 11666146google scholar: lookup
  21. Reller E, Kivipelto J, Ott E. Age-related changes for serum bone metabolism markers in Thoroughbred and Quarter Horse foals. J Equine Vet Sci 2003;23: 117–20.
  22. Billinghurst RC, Brama PAJ, van Weeren PR, Knowlton MS, McIlwraith CW. Evaluation of serum concentrations of biomarkers of skeletal metabolism and results of radiography as indicators of severity of osteochondrosis in foals. Am J Vet Res 2004;65: 143–50.
    pubmed: 14974569
  23. Donabédian M, van Weeren PR, Perona G, Fleurance G, Robert C, Léger S. Early changes in biomarkers of skeletal metabolism and their association to the occurrence of osteochondrosis (OC) in the horse. Equine Vet J 2008;40: 253–9.
    doi: 10.2746/042516408X273657pubmed: 18267892google scholar: lookup
  24. Trumble TN, Brown MP, Merritt KA, Billinghurst RC. Joint dependent concentrations of bone alkaline phosphatase in serum and synovial fluids of horses with osteochondral injury: an analytical and clinical validation. Osteoarthr Cartilage 2008;16: 779–86.
    pubmed: 18162418
  25. Ducy P. The role of osteocalcin in the endocrine cross-talk between bone remodelling and energy metabolism. Diabetologia 2011;54: 1291–7.
    doi: 10.1007/s00125-011-2155-zpubmed: 21503740google scholar: lookup
  26. Ferron M, Lacombe J. Regulation of energy metabolism by the skeleton: osteocalcin and beyond. Arch Biochem Biophys 2014;561: 137–46.
    doi: 10.1016/j.abb.2014.05.022pubmed: 24893146google scholar: lookup
  27. van der Eerden BCJ, Karperien M, Wit JM. Systemic and local regulation of the growth plate. Endocr Rev 2003;24: 782–801.
    doi: 10.1210/er.2002-0033pubmed: 14671005google scholar: lookup
  28. Fortier LA, Kornatowski MA, Mohammed HO, Jordan MT, O'Cain LC, Stevens WB. Age-related changes in serum insulin-like growth factor-I, insulin-like growth factor-I binding protein-3 and articular cartilage structure in Thoroughbred horses. Equine Vet J 2005;37: 37–42.
    pubmed: 15651732
  29. Mackie EJ, Tatarczuch L, Mirams M. The skeleton: a multi-functional complex organ. The growth plate chondrocyte and endochondral ossification. J Endocrinol 2011;211: 109–21.
    doi: 10.1530/JOE-11-0048pubmed: 21642379google scholar: lookup
  30. Savage CJ, McCarthy RN, Jeffcott LB. Effects of dietary phosphorus and calcium on induction of dyschondroplasia in foals. Equine Vet J 1993;Suppl 16: 80–3.
  31. Sloet van Oldruitenborgh-Oosterban M, Mol J, Barneveld A. Hormones, growth factors and other plasma variables in relation to osteochondrosis. Equine Vet. J. 1999;Suppl 31: 45–54.
    pubmed: 10999660
  32. World Breeding Federation for Sport Horses (WBFSH). Studbook Rankings 2018 [Internet]. .
  33. Peel MC, Finlayson BL, McMahon TA. Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 2007;11: 1633–1644.
  34. Instituto Português do Mar e da Atmosfera, IP. Climate Normals 1981–2010 [Internet]. .
  35. Paço TA, Fradinho MJ. The role of extensive grazing systems in Southern Europe horse prodution. 2011. In: Prochazka NT. Editor. Pastures: Dynamics, Economics and Management. Nova Science Publishers; New York, NY; pp. 131–150.
  36. Hoyt S, Siciliano P. A comparison of ELISA and RIA techniques for the detection of serum osteocalcin in horses. Proceedings 16th Equine Nutr. Phys. Symp. 1999, pp. 351–352.
  37. Jackson BF, Goodship AE, Eastell R, Price JS. Evaluation of serum concentrations of biochemical markers of bone metabolism and insulin-like growth factor I associated with treadmill exercise in young horses. Am. J. Vet. Res. 2003;64: 1549–56.
    pubmed: 14672435
  38. Cosden RS. Insulin-like growth factor-I in growing horses and RNA isolation from small articular cartilage samples. M.Sc. Thesis. Virginia Polytechnic Institute and State University. 2007.
  39. McManus CJ, Fitzgerald BP. Effects of a single day of feed restriction on changes in serum leptin, gonadotropins, prolactin, and metabolites in aged and young mares. Domest Anim Endocrinol 2000;19: 1–13.
    pubmed: 10962194
  40. Cartmill JA, Thompson DL, Gentry LR, Pruett HE, Johnson CA. Effects of dexamethasone, glucose infusion, adrenocorticotropin, and propylthiouracil on plasma leptin concentrations in horses. Domest Anim Endocrinol 2003;24: 1–14.
    pubmed: 12450621
  41. Tinworth KD, Wynn PC, Boston RC, Harris PA, Sillence MN, Thevis M. Evaluation of commercial available assays for the measurement of equine insulin. Domest Anim Endocrinol 2011;41: 81–90.
  42. Brown JE, Fitzhugh A Jr, Cartwright TC. A comparison of nonlinear models for describing weight-age relationship in cattle. J. Anim. Sci. 1976;42: 810–8.
  43. Perotto D, Cue RI, Lee AJ. Comparison of nonlinear functions for describing the growth curve of three genotypes of dairy cattle. Can J Anim Sci 1992;72: 773–82.
  44. Richards FJ. A flexible growth function for empirical use. J Exp Bot 1959;10: 290–300.
  45. Staniar WB, Kronfeld DS, Hoffman RM, Wilson JA, Harris PA. Weight prediction from linear measures of growing Thoroughbreds. Equine Vet J 2004;36: 149–54.
    pubmed: 15038438
  46. Jacquet S, Robert C, Valette J-P, Denoix J-M. Evolution of radiological findings detected in the limbs of 321 young horses, between the age of 6 and 18 months. Vet J 2013;197: 58–64.
    doi: 10.1016/j.tvjl.2013.03.042pubmed: 23660154google scholar: lookup
  47. Baccarin RY, Pereira MA, Roncati NV, Bergamaschi RR, Hagen SC. Development of osteochondrosis in Lusitano foals: a radiographic study. Can Vet J 2012;53: 1079–84.
    pmc: PMC3447310pubmed: 23543926
  48. Bernardes NFG. Estudo da influência do exercício, da idade e da presença de lesões de osteocondrose nos níveis séricos de biomarcadores ósseos no cavalo Lusitano linha Alter Real. M.Sc. Thesis. Faculdade de Medicina Veterinária / Instituto Superior de Agronomia, Universidade Técnica de Lisboa. 2008.
  49. Teixeira JAA. Avaliação radiográfica de osteocondrose como contributo na selecção de reprodutores equinos da raça Puro Sangue Lusitano. M.Sc. Thesis. Faculdade de Medicina Veterinária, Universidade Técnica de Lisboa. 2009.
  50. Vander Heyden L, Lejeune JP, Caudron I, Detilleux J, Sandersen C, Chavatte P. Association of breeding conditions with prevalence of osteochondrosis in foals. Vet Rec 2013;172: 68.
    doi: 10.1136/vr.101034pubmed: 23118049google scholar: lookup
  51. Robert C, Valette J-P, Jacquet S, Lepeule J, Denoix J-M. Study design for the investigation of likely aetiological factors of juvenile osteochondral conditions (JOCC) in foals and yearlings. Vet J 2013;197: 36–43.
    doi: 10.1016/j.tvjl.2013.03.039pubmed: 23642464google scholar: lookup
  52. Lepeule J, Bareille N, Robert C, Ezanno P, Valette J-P, Jacquet S. Association of growth, feeding practices and exercise conditions with the prevalence of developmental orthopaedic disease in limbs of foals. Prev Vet Med 2009;89: 167–77.
  53. Lepeule J, Seegers H, Rondeau V, Robert C, Denoix J-M, Bareille N. Association of growth, feeding practices and exercise conditions with the severity of the osteo-articular status of limbs in French foals. Vet J 2013;197: 65–71.
    doi: 10.1016/j.tvjl.2013.03.043pubmed: 23664071google scholar: lookup
  54. Carroll CL, Huntington PJ. Body condition scoring and weight estimation of horses. Equine Vet J 1988;20: 41–5.
    pubmed: 3366105
  55. Carstanjen B, Duboeuf F, Detilleux J, Lepage O. Equine third metacarpal bone assessment by quantitative ultrasound and dual energy X-Ray absorptiometry: an ex vivo study. J Vet Med A 2003;50: 42–77.
    pubmed: 12650508
  56. Firth EC, van Weeren PR, Pfeiffer DU, Delahunt J, Barneveld A. Effect of age, exercise and growth rate on bone mineral density (BMD) in third carpal bone and distal radius of Dutch Warmblood foals with osteochondrosis. Equine Vet J 1999;Suppl 31: 74–8.
    pubmed: 10999664
  57. Rho J-Y, Kuhn-Spearing L, Zioupos P. Mechanical properties and the hierarchical structure of bone. Med Eng Phys 1998;20: 92–102.
    pubmed: 9679227
  58. Clarke B. Normal Bone Anatomy and Physiology. Clin J Am Soc Nephrol 2008;3: S131–9.
    doi: 10.2215/CJN.04151206pmc: PMC3152283pubmed: 18988698google scholar: lookup
  59. Vervuert I, Winkelsett S, Christmann L, Bruns E, Hoppen H-O, Distl O. Evaluation of the influences of exercise, birth date, and osteochondrosis on plasma bone marker concentrations in Hannoverian Warmblood foals. Am J Vet Res 2007;68; 1319–23.
    doi: 10.2460/ajvr.68.12.1319pubmed: 18052735google scholar: lookup
  60. Baccarin RYA, Pereira MA, Roncati NV, Furtado PV, Oliveira CA, Hagen SCF. Identificação dos níveis séricos do fator de crescimento tipo insulina 1 em potros com osteocondrose. Pesq Vet Bras 2011;31: 677–82.
  61. Verwilghen D, Busoni V, Gangl M, Franck T, Lejeune J-Ph, Vanderheyden L. Relationship between biochemical markers and radiographic scores in the evaluation of the osteoarticular status of Warmblood stallions. Res Vet Sci 2009;87: 319–28.
    doi: 10.1016/j.rvsc.2009.02.002pubmed: 19298987google scholar: lookup
  62. Lejeune J-Ph, Franck T, Gangl M, Schneider N, Michaux C, Deby-Dupont G. Plasma concentration of Insulin-like Growth Factor I (IGF-I) in growing Ardenner horses suffering from Juvenile Digital Degenerative Osteoarthropathy. Vet Res Commun 2007;31: 185–95.
    pubmed: 17216321
  63. Henson FMD, Davenport C, Butler L, Moran I, Shingleton WD, Jeffcott LB. Effects of insulin and insulin-like growth factors I and II on the growth of equine fetal and neonatal chondrocytes. Equine Vet J 1997;29: 441–7.
    pubmed: 9413716
  64. Jeffcott LB, Henson FMD. Studies on growth cartilage in the horse and their application to aetiopathogenesis of dyschondroplasia (osteochondrosis). Vet J 1998;156: 177–92.
    pubmed: 9883086
  65. Fradinho MJ, Mateus L, Bessa RJB, Caldeira RM, Ferreira-Dias G. Age-related changes of bone ultrasound measurements and metabolic indicators in the young horse. Livest Sci 2018;211: 104–10.
  66. Azarpeykan S, Dittmer KE, Gee EK, Marshall JC, Wallace J, Elder P, Acke E, Thompson KG. Influence of blanketing and season on vitamin D and parathyroid hormone, calcium, phosphorus, and magnesium concentrations in horses in New Zealand. Domest Anim Endocrinol 2016;56: 75–84.
  67. Estepa JC, Aguilera-Tejero E, Mayer-Valor R, Almaden Y, Felsenfeld AJ, Rodriguez M. Measurement of parathyroid hormone in horses. Equine Vet J 1998;30: 476–81.
    pubmed: 9844965
  68. Estepa JC, Garfia B, Gao P, Cantor T, Rodriguez M, Aguilera-Tejero E. Validation and clinical utility of a novel immunoradiometric assay exclusively for biologically active whole parathyroid hormone in the horse. Equine Vet J 2003;35: 291–5.
    pubmed: 12755433
  69. Toribio RE, Kohn CW, Sams RA, Capen CC, Rosol TJ. Hysteresis and calcium set-point for the calcium parathyroid hormone relationship in healthy horses. Gen Comp Endocrinol 2003;130: 279–88.
    pubmed: 12606270
  70. Felsenfeld AJ, Rodriguez M, Aguilera-Tejero E. Dynamics of parathyroid hormone secretion in health and secondary hyperparathyroidism. Clin J Am Soc Nephrol 2007; 2: 1283–305.
    doi: 10.2215/CJN.01520407pubmed: 17942777google scholar: lookup
  71. Berlin D, Aroch I. Concentrations of ionized and total magnesium and calcium in healthy horses: Effects of age, pregnancy, lactation, pH and sample type. Vet J 2009; 181, 305–11.
    pubmed: 18467135
  72. Toribio RE. Disorders of calcium and phosphate metabolism in horses. Vet Clin Equine 2011; 27, 129–47.
    pubmed: 21392658

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    doi: 10.3389/fvets.2025.1598038pubmed: 40786980google scholar: lookup
  2. Martinez-Saez L, Marín-García PJ, Llobat ML. Osteochondrosis in horses: An overview of genetic and other factors. Equine Vet J 2026 Jan;58(1):6-19.
    doi: 10.1111/evj.14518pubmed: 40302410google scholar: lookup
  3. Schubert DC, Neustädter LT, Coenen M, Visscher C, Kamphues J. Investigations on the Effects of Different Calcium Supply Exceeding the Requirements on Mineral Serum Concentrations and Bone Metabolism in Young Warmblood Stallions. Animals (Basel) 2021 Aug 19;11(8).
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  4. Veraa S, Scheffer CJW, Smeets DHM, de Bruin RB, Hoogendoorn AC, Vernooij JCM, Nielen M, Back W. Cervical disc width index is a reliable parameter and consistent in young growing Dutch Warmblood horses. Vet Radiol Ultrasound 2020 Oct 13;62(1):11-9.
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