Characterization of bony changes localized to the cervical articular processes in a mixed population of horses


Autoři: Kevin K. Haussler aff001;  Roy R. Pool aff002;  Hilary M. Clayton aff003
Působiště autorů: Gail Holmes Equine Orthopaedic Research Center, Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colorado, United States of America aff001;  Texas A&M University, Department of Veterinary Pathobiology, Veterinary Medicine and Biomedical Sciences, College Station, Texas, United States of America aff002;  Department of Large Animal Clinical Sciences, Michigan State University, East Lansing, Michigan, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222989

Souhrn

The objectives of this observational, cross-sectional study were to characterize and establish the prevalence of osseous proliferation of articular surfaces, joint margins and adjacent soft tissue attachments (i.e., joint capsule and deep spinal muscles) in a mixed population of horses of variable ages, sizes, and breeds to better capture the full spectrum of disease affecting the cervical articular processes. Cranial and caudal articular processes of the cervical and first three thoracic vertebrae (C2-T3) from 55 horses without a primary complaint of neck pain were evaluated for the presence and severity of abnormal bony changes. Data were analyzed to compare alterations in joint margin quadrants, paired articular surfaces within a synovial articulation, left-right laterality, and vertebral level distributions and to determine associations with age, wither height and sex. Seventy-two percent of articular processes had bony changes that were considered abnormal. Osteophyte formation was the most common bony change noted. Overall grades of severity included: normal (28%), mild (45%), moderate (22%), and severe (5%). The highest prevalence of mild changes was localized to the C3-C6 vertebral levels; moderate changes to C6-T2; and severe changes to C2-C3 and C6-T2. Most paired articular surfaces and left-right grades of severity were not significantly different. The grade of osseous pathology was positively associated with both age and wither height. A high prevalence and wide variety of abnormal bony changes of varying severity were found in articular processes across all vertebral levels. The clinical significance of the described lesions is unknown, but the findings are expected to enhance the reporting of articular process and periarticular changes noted on advanced diagnostic imaging of the equine cervical and cranial thoracic vertebral regions.

Klíčová slova:

Cranium – Horses – Neck – Osteoarthritis – Skeletal joints – Vertebrae – Animal husbandry


Zdroje

1. Janes JG, Garrett KS, McQuerry KJ, Pease AP, Williams NM, Reed SM, et al. Comparison of magnetic resonance imaging with standing cervical radiographs for evaluation of vertebral canal stenosis in equine cervical stenotic myelopathy. Equine Vet J 2014;46(6):681–6. doi: 10.1111/evj.12221 24329734

2. Sleutjens J, Cooley AJ, Sampson SN, Wijnberg ID, Back W, van der Kolk JH, et al. The equine cervical spine: comparing MRI and contrast-enhanced CT images with anatomic slices in the sagittal, dorsal, and transverse plane. Vet Q 2014;34(2):74–84. doi: 10.1080/01652176.2014.951129 25174534

3. Moore BR, Holbrook TC, Stefanacci JD, Reed SM, Tate LP, Menard MC. Contrast-enhanced computed tomography and myelography in six horses with cervical stenotic myelopathy. Equine Vet J 1992;24(3):197–202. doi: 10.1111/j.2042-3306.1992.tb02814.x 1606933

4. Powers BE, Stashak TS, Nixon AJ, Yovich JV, Norrdin RW. Pathology of the vertebral column of horses with cervical static stenosis. Vet Pathol 1986;23(4):392–9. doi: 10.1177/030098588602300408 3750733

5. Papageorges M, Gavin PR, Sande RD, Barbee DD, Grant BD. Radiographic and myelographic examination of the cervical vertebral column in 306 ataxic horses. Vet Radiol Ultrasound 1987;28(2):53–59.

6. Levine JM, Adam E, MacKay RJ, Walker MA, Frederick JD, Cohen ND. Confirmed and presumptive cervical vertebral compressive myelopathy in older horses: a retrospective study (1992–2004). J Vet Internal Medicine 2007;21(4):812–9.

7. Tomizawa N, Nishimura R, Sasaki N, Hayashi Y, Senba H, Hara S, et al. Morphological analysis of cervical vertebrae in ataxic foals. J Vet Med Sci 1994;56(6):1081–5. doi: 10.1292/jvms.56.1081 7696396

8. Dyson SJ. Lesions of the equine neck resulting in lameness or poor performance. Vet Clin North Am Equine Pract 2011;27(3):417–37. doi: 10.1016/j.cveq.2011.08.005 22100038

9. Lautenschläger I, Baumann I, Schulze M, Martens I, Rohn K, Stadler P. Radiological evaluations of the caudal cervical synovial articulations in the warmblooded horse. / Die röntgenologische Darstellung der caudalen Facettengelenke der Halswirbelsäule beim Warmblutpferd. Pferdeheilkunde 2009;25(6):544–553.

10. Janes JG, Garrett KS, McQuerry KJ, Waddell S, Voor MJ, Reed SM, et al. Cervical vertebral lesions in equine stenotic myelopathy. Vet Pathol 2015;52(5):919–27. doi: 10.1177/0300985815593127 26169385

11. DeRouen A, Spriet M, Aleman M. Prevalence of anatomical variation of the sixth cervical vertebra and association with vertebral canal stenosis and articular process osteoarthritis in the horse. Vet Radiol Ultrasound 2016;57(3):253–258. doi: 10.1111/vru.12350 26915973

12. Birmingham SSW, Reed SM, Mattoon JS, Saville WJ. Qualitative assessment of corticosteroid cervical articular facet injection in symptomatic horses. Equine Vet Educ. 2010;22(2):77–82.

13. Pepe M, Angelone M, Gialletti R, Nannarone S, Beccati F. Arthroscopic anatomy of the equine cervical articular process joints. Equine Vet J 2014;46(3):345–51. doi: 10.1111/evj.12112 23742017

14. Gellhorn AC, Katz JN, Suri P. Osteoarthritis of the spine: the facet joints. Nat Rev Rheumatol 2012;9(4):216–224. doi: 10.1038/nrrheum.2012.199 23147891

15. Jaumard NV, Welch WC, Winkelstein BA. Spinal facet joint biomechanics and mechanotransduction in normal, injury and degenerative conditions. J Biomech Eng 2011;133(7):071010. doi: 10.1115/1.4004493 21823749

16. Martinelli M, Rantanen NW, Grant B. Cervical arthropathy, myelopathy or just a pain in the neck? Equine Vet Educ 2010;22:88–89.

17. Nowak N, Huskamp B. Special findings in diseases of the cervical spine in the horse. / Über einige spezielle Befunde bei Erkrankungen der Halswirbelsäule des Pferdes. Pferdeheilkunde 1989;5(2):95–107.

18. Ricardi G, Dyson SJ. Forelimb lameness associated with radiographic abnormalities of the cervical vertebrae. Equine Vet J 1993;25(5):422–6. doi: 10.1111/j.2042-3306.1993.tb02984.x 8223374

19. Hett AR, Busato A, Ueltschi G. Radiographic measurements of the equine cervical spine with arthrotic alterations—a retrospective statistical study. [Radiologische Messungen an der arthrotisch veränderten Halswirbelsäule des Pferdes—eine retrospektive, statistische Studie]. Pferdeheilkunde 2006;22(3):241–249.

20. Claridge HA, Piercy RJ, Parry A, Weller R. The 3D anatomy of the cervical articular process joints in the horse and their topographical relationship to the spinal cord. Equine Vet J 2010;42(8):726–31. doi: 10.1111/j.2042-3306.2010.00114.x 21039803

21. Moore BR, Reed SM, Biller DS, Kohn CW, Weisbrode SE. Assessment of vertebral canal diameter and bony malformations of the cervical part of the spine in horses with cervical stenotic myelopathy. Amer J Vet Res 1994;55(1):5–13. 8141496

22. Stewart RH, Rush BR. Cervical vertebral stenotic myelopathy. In: Reed SM, Bayly WM, Sellon DC, editors. Equine internal medicine. St. Louis, MO: Elsevier; 2004. p. 594–599.

23. Dimock AN, Puchalski SM. Cervical radiology. Equine Vet Educ 2010;22:83–87.

24. Down SS, Henson FM. Radiographic retrospective study of the caudal cervical articular process joints in the horse. Equine Vet J 2009;41(6):518–24. doi: 10.2746/042516409x391015 19803045

25. Whitwell KE, Dyson S. Interpreting radiographs. 8: Equine cervical vertebrae. Equine Vet J 1987;19(1):8–14. doi: 10.1111/j.2042-3306.1987.tb02568.x 3319578

26. Johnson JP, Stack JD, Rowan CI. H, O”Leary JM. Ultrasound-guided approach to the cervical articular process joints in horses: a validation of the technique in cadavers. Vet Comp Orthop Traumatol 2017;30:165–171. doi: 10.3415/VCOT-16-09-0139 28094412

27. Veraa S, Bergmann W, van den Belt AJ, Wijnberg I, Back W. Ex vivo computed tomographic evaluation of morphology variations in equine cervical vertebrae. Vet Radiol Ultrasound 2016;57(5):482–8. doi: 10.1111/vru.12393 27438135

28. Chope K. How to Perform Sonographic Examination and Ultrasound-Guided Injection of the Cervical Vertebral Facet Joints in Horses. Proc Amer Assoc Equine Practitioners 2008;54:186–189.

29. Trostle SS, Dubielzig RR, Beck KA. Examination of frozen cross sections of cervical spinal intersegments in nine horses with cervical vertebral malformation: lesions associated with spinal cord compression. J Vet Diagnostic Investigation 1993;5(3):423–31.

30. Fürst A. Cervical vertebral arthrosis in horses: an overview [Halswirbelsäulenarthrose beim Pferd: Eine Übersicht]. Prakt Tierarzt 2006;87:956–964.

31. Tomizawa N, Nishimura R, Sasaki N, Nakayama H, Kadosawa T, Senba H, et al. Relationships between radiography of cervical vertebrae and histopathology of the cervical cord in wobbling 19 foals. J Vet Med Sci 1994;56(2):227–233. doi: 10.1292/jvms.56.227 8075209

32. VanderBroek A, Stubbs NC, Clayton HM. Osseous pathology of the synovial intervertebral articulations in the equine thoracolumbar spine. J Equine Vet Sci 2016;44:67–73.

33. Clayton HM, Buchholz R, Nauwelaerts S. Relationship between morphological and stabilographic variables in standing horses. Vet J 2013;198 Suppl 1:e65–9.

34. Binks DA, Gravallese EM, Bergin D, Hodgson RJ, Tan AL, Matzelle MM, et al. Role of vascular channels as a novel mechanism for subchondral bone damage at cruciate ligament entheses in osteoarthritis and inflammatory arthritis. Ann Rheum Dis 2015;74(1):196–203. doi: 10.1136/annrheumdis-2013-203972 24095939

35. Rijkenhuizen AB, Nemeth F, Dik KJ, Goedegebuure SA. The arterial supply of the navicular bone in adult horses with navicular disease. Equine Vet J 1989;21(6):418–24. doi: 10.1111/j.2042-3306.1989.tb02187.x 2591356

36. Rombach N, Stubbs NC, Clayton HM. Gross anatomy of the deep perivertebral musculature in horses. Amer J Vet Res 2014;75(5):433–40. doi: 10.2460/ajvr.75.5.433 24762014

37. Lee MJ, Riew KD. The prevalence cervical facet arthrosis: an osseous study in a cadveric population. Spine J 2009;9(9):711–4. doi: 10.1016/j.spinee.2009.04.016 19477691

38. Zsoldos RR, Kruger B, Licka TF. From maturity to old age: tasks of daily life require a different muscle use in horses. Comp Exerc Physiol 2014;10(2):75–88. doi: 10.3920/CEP140001 28680481

39. Singh S, Kumar D, Kumar S. Risk factors in cervical spondylosis. J Clin Orthop Trauma 2014;5(4):221–6. doi: 10.1016/j.jcot.2014.07.007 25983502

40. Zsoldos RR, Groesel M, Kotschwar A, Kotschwar AB, Licka T, Peham C. A preliminary modelling study on the equine cervical spine with inverse kinematics at walk. Equine Vet J Suppl 2010(38):516–22. doi: 10.1111/j.2042-3306.2010.00265.x 21059054

41. Listi GA, Manhein MH. The use of vertebral osteoarthritis and osteophytosis in age estimation. J Forensic Sci 2012;57(6):1537–40. doi: 10.1111/j.1556-4029.2012.02152.x 22486633

42. Tischer T, Aktas T, Milz S, Putz RV. Detailed pathological changes of human lumbar facet joints L1-L5 in elderly individuals. Eur Spine J 2006;15(3):308–15. doi: 10.1007/s00586-005-0958-7 16021481

43. Sleutjens J, Voorhout G, Kolk JHvd, Wijnberg ID, Back W. The effect of ex vivo flexion and extension on intervertebral foramina dimensions in the equine cervical spine. Equine Vet J 2010;42(s38):425–430.

44. Pagger H, Schmidburg I, Peham C, Licka T. Determination of the stiffness of the equine cervical spine. Vet J 2010;186(3):338–41. doi: 10.1016/j.tvjl.2009.09.015 19850500

45. Pool RR. Pathologic manifestions of joint disease in the athletic horse. In: McIlwraith CW, Trotter GW, editors. Joint disease in the horse. Philadelphia, PA: W.B. Saunders Company; 1996. p. 87–104.

46. van der Kraan PM, van den Berg WB. Osteophytes: relevance and biology. Osteoarthritis Cartilage 2007;15(3):237–244. doi: 10.1016/j.joca.2006.11.006 17204437

47. Erben RG. Trabecular and endocortical bone surfaces in the rat: modeling or remodeling? Anat Rec 1996;246(1):39–46. doi: 10.1002/(SICI)1097-0185(199609)246:1<39::AID-AR5>3.0.CO;2-A 8876822

48. Langdahl B, Ferrari S, Dempster DW. Bone modeling and remodeling: potential as therapeutic targets for the treatment of osteoporosis. Ther Adv Musculoskelet Dis 2016;8(6):225–235. doi: 10.1177/1759720X16670154 28255336

49. Neogi T. Clinical significance of bone changes in osteoarthritis. Ther Adv Musculoskelet Dis 2012;4(4):259–267. doi: 10.1177/1759720X12437354 22859925

50. Reichenbach S, Guermazi A, Niu J, Neogi T, Hunter DJ, Roemer FW, et al. Prevalence of bone attrition on knee radiographs and MRI in a community-based cohort. Osteoarthritis Cartilage 2008;16(9):1005–10. doi: 10.1016/j.joca.2008.02.001 18367415

51. Burr DB. Anatomy and physiology of the mineralized tissues: role in the pathogenesis of osteoarthrosis. Osteoarthritis Cartilage 2004;12 Suppl A:S20–30.

52. Wang M, Nasiri A, VanHouten JN, Tommasini SM, Broadus AE. The remarkable migration of the medial collateral ligament. J Anat 2014;224(4):490–8. doi: 10.1111/joa.12145 24266550

53. Dorfl J. Migration of tendinous insertions. I. Cause and mechanism. J Anat 1980;131(Pt 1):179–95. 7440401

54. Sojka JH, Everhart JS, Kirven JC, Beal MD, Flanigan DC. Variation in tibial tuberosity lateralization and distance from the tibiofemoral joint line: An anatomic study. Knee 2018;25(3):367–373. doi: 10.1016/j.knee.2018.03.006 29681529

55. Benjamin M, Toumi H, Ralphs JR, Bydder G, Best TM, Milz S. Where tendons and ligaments meet bone: attachment sites ('entheses') in relation to exercise and/or mechanical load. J Anat 2006;208(4):471–90. doi: 10.1111/j.1469-7580.2006.00540.x 16637873

56. McCarty WJ, Masuda K, Sah RL. Fluid movement and joint capsule strains due to flexion in rabbit knees. J Biomech 2011;44(16):2761–7. doi: 10.1016/j.jbiomech.2011.09.005 21945567

57. Haynes DR. Bone lysis and inflammation. Inflamm Res 2004;53(11):596–600. 15693607

58. Ramasamy SK. Structure and functions of blood vessels and vascular niches in bone. Stem Cells Int 2017;2017:5046953. doi: 10.1155/2017/5046953 29104595

59. Pool RR, Meagher DM, Stover SM. Pathophysiology of navicular syndrome. Vet Clin North Am Equine Pract 1989;5(1):109–29. 2650826

60. Benjamin M, Rufai A, Ralphs JR. The mechanism of formation of bony spurs (enthesophytes) in the achilles tendon. Arthritis Rheum 2000;43(3):576–83. doi: 10.1002/1529-0131(200003)43:3<576::AID-ANR14>3.0.CO;2-A 10728751

61. Slobodin G, Rozenbaum M, Boulman N, Rosner I. Varied presentations of enthesopathy. Semin Arthritis Rheum 2007;37(2):119–26. doi: 10.1016/j.semarthrit.2007.01.004 17350676

62. Girodroux M, Dyson S, Murray R. Osteoarthritis of the thoracolumbar synovial intervertebral articulations: clinical and radiographic features in 77 horses with poor performance and back pain. Equine Vet J 2009;41(2):130–138. doi: 10.2746/042516408x345099 19418740

63. Dippel M, Zsoldos RR, Licka TF. An equine cadaver study investigating the relationship between cervical flexion, nuchal ligament elongation and pressure at the first and second cervical vertebra. Vet J 2019;252:105353.


Článek vyšel v časopise

PLOS One


2019 Číslo 9
Nejčtenější tento týden