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The Craniovertebral Junction in Rheumatoid Arthritis: State of the Art

  • Angelo Ferrante
  • Francesco Ciccia
  • Giuseppe Roberto Giammalva
  • Domenico Gerardo Iacopino
  • Massimiliano Visocchi
  • Federica Macaluso
  • Rosario Maugeri
Chapter
Part of the Acta Neurochirurgica Supplement book series (NEUROCHIRURGICA, volume 125)

Abstract

Rheumatoid arthritis (RA) is a chronic inflammatory disorder, characterized by polyarticular inflammation causing progressive joint damage and disability. The mechanisms underlying its pathogenesis involve activation of innate and adaptive immunity, microvascular endothelial cell activation, and inflammatory infiltration of lymphocytes and monocytes into the synovium. Spinal involvement in RA is not typical; when it occurs, the main radiological features are (1) atlantoaxial subluxation (AAS), which is the most typical form of cervical spine involvement; (2) cranial settling—also known as basilar impression, atlantoaxial impaction or superior migration of the odontoid—which is the most severe form of associated spinal instability; and (3) subaxial subluxation. A combination of these alterations may occur. Synovitis is characterized by infiltration of innate and adaptive immune cells; joint destruction is a consequence of activation of synovial fibroblasts, which acquire aggressive, inflammatory, invasive features, associated with increased chondrocyte catabolism and synovial osteoclastogenesis.

Neck pain is the most frequent symptom of spinal involvement in RA; it occurs in 40–80% of patients and is mostly localized at the craniocervical junction. Other symptoms—caused by compression of neural structures such as the greater occipital nerve (at C2), the nucleus of the spinal trigeminal tract and the greater auricular nerve—are occipital neuralgia, facial pain and ear pain, respectively. Irritation of the lesser occipital nerve (at C1) can cause pain in the suboccipital region. Sometimes patients may complain of a sensation of their head falling down with flexion, weakness, reduced endurance, loss of ability, gait alterations, paraesthesias or other symptoms due to cord and medullary compression, and upper or lower motor neuron signs, or both. Surgical management of RA remains a challenging field.

Keywords

Craniovertebral junction Rheumatoid arthritis Cervical spine Inflammation Transnasal decompression Transoral decompression Instrumentation and fusion procedures Atlantoaxial dislocation Atlantoaxial instability Atlantoaxial synovitis Basilar invagination 

References

  1. 1.
    Smolen JS, Aletaha D, McInnes IB. Rheumatoid arthritis. Lancet. 2016;388:2023–38.CrossRefGoogle Scholar
  2. 2.
    Garrod AE. A treatise on rheumatism and rheumatoid arthritis. London: Griffin’s Medical Series; 1890.Google Scholar
  3. 3.
    Cha TD, An HS. Cervical spine manifestations in patients with inflammatory arthritis. Nat Rev Rheumatol. 2013;9:423–32.CrossRefGoogle Scholar
  4. 4.
    Agarwal AK, Peppelman WC Jr, Kraus DR, Eisenbeis CH Jr. The cervical spine in rheumatoid arthritis. BMJ. 1993;306:79–80.CrossRefGoogle Scholar
  5. 5.
    Halla JT, Hardin JG, Vitek J, Alarcon GS. Involvement of the cervical spine in rheumatoid arthritis. Arthritis Rheum. 1989;32:652–9.CrossRefGoogle Scholar
  6. 6.
    Reiter MF, Boden SD. Inflammatory disorders of the cervical spine. Spine. 1998;23:2755–66.CrossRefGoogle Scholar
  7. 7.
    Kauppi MJ, Neva MH, Laiho K, Kautiainen H, Luukkainen R, Karjalainen A, et al. Rheumatoid atlantoaxial subluxation can be prevented by intensive use of traditional disease modifying antirheumatic drugs. J Rheumatol. 2009;36(2):273–8.CrossRefGoogle Scholar
  8. 8.
    Del Grande M, Del Grande F, Carrino J, Bingham CO III, Louie GH. Cervical spine involvement early in the course of rheumatoid arthritis. Semin Arthritis Rheum. 2014;43:738–44.CrossRefGoogle Scholar
  9. 9.
    Bland J, Boushey D. Anatomy and physiology of the cervical spine. Semin Arthritis Rheum. 1990;20:1–20.CrossRefGoogle Scholar
  10. 10.
    La Caffinière JY, Seringe R, Roy-Camille R. Étude physiopathologique des lésions ligamentaires graves dans les traumatismes de la charnière occipito-rachidienne. Rev Chir Orthop. 1972;58:11–9.PubMedGoogle Scholar
  11. 11.
    Krauss WE, Bledsoe JM, Clarke MJ, Nottmeier EW, Pichelmann MA. Rheumatoid arthritis of the craniovertebral junction. Neurosurgery. 2010;66:83–95.CrossRefGoogle Scholar
  12. 12.
    Wasserman BR, Moskovich R, Razi AE. Rheumatoid arthritis of the cervical spine—clinical considerations. Bull NYU Hosp Jt Dis. 2011;69:136–48.PubMedGoogle Scholar
  13. 13.
    Winfield J, Young A, Williams P, Corbett M. Prospective study of the radiologic changes in hands, feet, and cervical spine in adult rheumatoid disease. Ann Rheum Dis. 1983;42:613–8.CrossRefGoogle Scholar
  14. 14.
    Bouchaud-Chabot A, Lioté F. Cervical spine involvement in rheumatoid arthritis. A review. Joint Bone Spine. 2002;69:141–54.CrossRefGoogle Scholar
  15. 15.
    Lipson S. Rheumatoid arthritis of the cervical spine. Clin Orthop. 1984;182:143–9.Google Scholar
  16. 16.
    Lipson S. Cervical myelopathy and posterior atlanto-axial subluxations in patients with rheumatoid arthritis. J Bone Joint Surg. 1985;67A:593–7.CrossRefGoogle Scholar
  17. 17.
    Menezes AH, VanGilder JC, Clark CR, El-Khoury G. Odontoid upward migration in rheumatoid arthritis. An analysis of 45 patients with “cranial settling”. J Neurosurg. 1985;63(1):500–9.CrossRefGoogle Scholar
  18. 18.
    Cabot A, Becker A. The cervical spine in rheumatoid arthritis. Clin Orthop. 1978;131:130–40.Google Scholar
  19. 19.
    Seignon B, Tellart-Chaudeur MO, Gougeon J. Les lesions destructrices du rachis cervical moyen et inférieur au cours de la polyarthrite rhumatoïde. Sem Hôp Paris. 1975;51:1157–66.PubMedGoogle Scholar
  20. 20.
    Gonzalez A, Icen M, Kremers HM, et al. Mortality trends in rheumatoid arthritis: the role of rheumatoid factor. J Rheumatol. 2008;35:1009–14.CrossRefGoogle Scholar
  21. 21.
    van Gaalen FA, van Aken J, Huizinga TW, et al. Association between HLA class II genes and autoantibodies to cyclic citrullinated peptides (CCPs) influences the severity of rheumatoid arthritis. Arthritis Rheum. 2004;50:2113–21.CrossRefGoogle Scholar
  22. 22.
    Anquetil F, Clavel C, Offer G, Serre G, Sebbag M. IgM and IgA rheumatoid factors purified from rheumatoid arthritis sera boost the Fc receptor– and complement-dependent effector functions of the disease-specific anti-citrullinated protein autoantibodies. J Immunol. 2015;194:3664–74.CrossRefGoogle Scholar
  23. 23.
    Reynisdottir G, Olsen H, Joshua V, et al. Signs of immune activation and local inflammation are present in the bronchial tissue of patients with untreated early rheumatoid arthritis. Ann Rheum Dis. 2016;75(9):1722–7.CrossRefGoogle Scholar
  24. 24.
    Harre U, Georgess D, Bang H, et al. Induction of osteoclastogenesis and bone loss by human autoantibodies against citrullinated vimentin. J Clin Investig. 2012;122:1791–802.CrossRefGoogle Scholar
  25. 25.
    Smolen JS, Aletaha D, Koeller M, Weisman M, Emery P. New therapies for the treatment of rheumatoid arthritis. Lancet. 2007;370:1861–74.CrossRefGoogle Scholar
  26. 26.
    McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med. 2011;365:2205–19.CrossRefGoogle Scholar
  27. 27.
    Humby F, Kelly S, Hands R, et al. Use of ultrasound-guided small joint biopsy to evaluate the histopathologic response to rheumatoid arthritis therapy: recommendations for application to clinical trials. Arthritis Rheumatol. 2015;67:2601–10.CrossRefGoogle Scholar
  28. 28.
    Feldmann M, Maini SR. Role of cytokines in rheumatoid arthritis: an education in pathophysiology and therapeutics. Immunol Rev. 2008;223:7–19.CrossRefGoogle Scholar
  29. 29.
    Pettit AR, Ji H, von Stechow D, et al. TRANCE/RANKL knockout mice are protected from bone erosion in a serum transfer model of arthritis. Am J Pathol. 2001;159:1689–99.CrossRefGoogle Scholar
  30. 30.
    Redlich K, Hayer S, Ricci R, et al. Osteoclasts are essential for TNF-α-mediated joint destruction. J Clin Investig. 2002;110:1419–27.CrossRefGoogle Scholar
  31. 31.
    Rawlins BA, Girardi FP, Boachie-Adjei O. Rheumatoid arthritis of the cervical spine. Rheum Dis Clin North Am. 1998;24:55–65.CrossRefGoogle Scholar
  32. 32.
    Dreyer SJ, Boden SD. Natural history of rheumatoid arthritis of the cervical spine. Clin Orthop Relat Res. 1999;366:98–106.CrossRefGoogle Scholar
  33. 33.
    Bohlman HH, Emery SE, Goodfellow DB, Jones PK. Robinson anterior cervical discectomy and arthrodesis for cervical radiculopathy. Long-term follow-up of one hundred and twenty-two patients. J Bone Joint Surg Am. 1993;75:1298–307.CrossRefGoogle Scholar
  34. 34.
    Blom M, Creemers MC, Kievit W, Lemmens JA, van Riel PL. Long-term follow-up of the cervical spine with conventional radiographs in patients with rheumatoid arthritis. Scand J Rheumatol. 2013;42:281–8.CrossRefGoogle Scholar
  35. 35.
    Kim HJ, Nemani VM, Riew KD, Brasington R. Cervical spine disease in rheumatoid arthritis: incidence, manifestations, and therapy. Curr Rheumatol Rep. 2015;17(2):9.CrossRefGoogle Scholar
  36. 36.
    Yurube T, Sumi M, Nishida K, et al. Accelerated development of cervical spine instabilities in rheumatoid arthritis: a prospective minimum 5-year cohort study. PLoS One. 2014;18:e88970.CrossRefGoogle Scholar
  37. 37.
    Zikou AK, Alamanos Y, Argyropoulou MI, Tsifetaki N, Tsampoulas C, Voulgari PV, et al. Radiological cervical spine involvement in patients with rheumatoid arthritis: a cross sectional study. J Rheumatol. 2005;32:801–6.PubMedGoogle Scholar
  38. 38.
    Kwek TK, Lew TW, Thoo FL. The role of preoperative cervical spine X-rays in rheumatoid arthritis. Anaesth Intensive Care. 1998;26(6):636–41.PubMedGoogle Scholar
  39. 39.
    Boden SD, Dodge LD, Bohlman HH, Rechtine GR. Rheumatoid arthritis of the cervical spine. A long-term analysis with predictors of paralysis and recovery. J Bone Joint Surg Am. 1993;75(9):1282–97.CrossRefGoogle Scholar
  40. 40.
    Ahn JK, Hwang JW, Oh JM, Lee J, Lee YS, Jeon CH, et al. Risk factors for development and progression of atlantoaxial subluxation in Korean patients with rheumatoid arthritis. Rheumatol Int. 2011;31:1363–8.CrossRefGoogle Scholar
  41. 41.
    Sugita S, Chikuda H, Kadono Y, Ohtsu H, Takeshita K, Nishino J, et al. Clinical characteristics of rheumatoid arthritis patients undergoing cervical spine surgery: an analysis of National Database of Rheumatic Diseases in Japan. BMC Musculoskelet Disord. 2014;15:203.CrossRefGoogle Scholar
  42. 42.
    Zoli A, Priolo F, Galossi A, Altomonte L, Di Gregorio F, Cerase A, et al. Craniocervical junction involvement in rheumatoid arthritis: a clinical and radiological study. J Rheumatol. 2000;27:1178–82.PubMedGoogle Scholar
  43. 43.
    Joaquim AF, Ghizoni E, Tedeschi H, Appenzeller S, Riew KD. Radiological evaluation of cervical spine involvement in rheumatoid arthritis. Neurosurg Focus. 2015;38:1–7.Google Scholar
  44. 44.
    Aggarwal A, Kulshreshtha A, Chaturvedi V, Misra R. Cervical spine involvement in rheumatoid arthritis: prevalence and relationship with overall disease severity. J Assoc Physicians India. 1996;44:468–71.PubMedGoogle Scholar
  45. 45.
    Ranawat CS, O’Leary P, Pellicci P, et al. Cervical spine fusion in rheumatoid arthritis. J Bone Joint Surg Am. 1979;61:1003–10.CrossRefGoogle Scholar
  46. 46.
    Redlund-Johnell I, Pettersson H. Radiographic measurements of the cranio-vertebral region. Designed for evaluation of abnormalities in rheumatoid arthritis. Acta Radiol Diagn (Stockh). 1984;25(1):23–8.CrossRefGoogle Scholar
  47. 47.
    Clark CR, Goetz DD, Menezes AH. Arthrodesis of the cervical spine in rheumatoid arthritis. J Bone Joint Surg Am. 1989;71:381–92.CrossRefGoogle Scholar
  48. 48.
    Riew KD, Hilibrand AS, Palumbo MA, Sethi N, Bohlman HH. Diagnosing basilar invagination in the rheumatoid patient. The reliability of radiographic criteria. J Bone Joint Surg Am. 2001;83-A:194–200.CrossRefGoogle Scholar
  49. 49.
    Tehranzadeh J, Ashikyan O, Dascalos J. Magnetic resonance imaging in early detection of rheumatoid arthritis. Semin Musculoskelet Radiol. 2003;7:79–94.CrossRefGoogle Scholar
  50. 50.
    Stiskal MA, Neuhold A, Szolar DH, Saeed M, Czerny C, Leeb B, et al. Rheumatoid arthritis of the craniocervical region by MR imaging: detection and characterization. Am J Roentgenol. 1995;165:585–92.CrossRefGoogle Scholar
  51. 51.
    Bundschuh C, Modic MT, Kearney F, Morris R, Deal C. Rheumatoid arthritis of the cervical spine: surface-coil MR imaging. AJR Am J Roentgenol. 1988;151:181–7.CrossRefGoogle Scholar
  52. 52.
    Reijnierse M, Breedveld FC, Kroon HM, Hansen B, Pope TL, Bloem JL. Are magnetic resonance flexion views useful in evaluating the cervical spine of patients with rheumatoid arthritis? Skeletal Radiol. 2000;29:85–9.CrossRefGoogle Scholar
  53. 53.
    Kroft LJ, Reijnierse M, Kloppenburg M, Verbist BM, Bloem JL, van Buchem MA. Rheumatoid arthritis: epidural enhancement as an underestimated cause of subaxial cervical spinal stenosis. Radiology. 2004;231:57–63.CrossRefGoogle Scholar
  54. 54.
    Roca A, Bernreuter WK, Alarcon GS. Functional magnetic resonance imaging should be included in the evaluation the cervical spine in patients with rheumatoid arthritis. J Rheumatol. 1993;20(9):1485–8.PubMedGoogle Scholar
  55. 55.
    Weissman BN, Aliabadi P, Weinfeld MS, et al. Prognostic features of atlantoaxial subluxation in rheumatoid arthritis patients. Radiology. 1982;144(4):745–51.CrossRefGoogle Scholar
  56. 56.
    Lourie H, Stewart WA. Spontaneous atlantoaxial dislocation. A complication of rheumatoid disease. N Engl J Med. 1961;265:677–81.CrossRefGoogle Scholar
  57. 57.
    Mathews JA. Atlanto-axial subluxation in rheumatoid arthritis. A 5-year follow-up study. Ann Rheum Dis. 1974;33:526–31.CrossRefGoogle Scholar
  58. 58.
    Rasker JJ, Cosh JA. Radiological study of cervical spine and hand in patients with rheumatoid arthritis of 15 years’ duration: an assessment of the effects of corticosteroid treatment. Ann Rheum Dis. 1978;37:529–35.CrossRefGoogle Scholar
  59. 59.
    Yonezawa T, Tsuji H, Matsui H, Hirano N. Subaxial lesions in rheumatoid arthritis. Radiographic factors suggestive of lower cervical myelopathy. Spine (Phila Pa 1976). 1995;20:208–15.CrossRefGoogle Scholar
  60. 60.
    Paimela L, Laasonen L, Kankaanpaa E, Leirisalo-Repo M. Progression of cervical spine changes in patients with early rheumatoid arthritis. J Rheumatol. 1997;24:1280–4.PubMedGoogle Scholar
  61. 61.
    Neva MH, et al. Combination drug therapy retards the development of rheumatoid atlantoaxial subluxations. Arthritis Rheum. 2000;43:2397–401.CrossRefGoogle Scholar
  62. 62.
    Kaito T, et al. Effect of biological agents on cervical spine lesions in rheumatoid arthritis. Spine. 2012;37:1742–6.CrossRefGoogle Scholar
  63. 63.
    Graziano F, Maugeri R, Basile L, Meccio F, Iacopino DG. Aulogous fibrin sealant (Vivostat®) in the neurosurgical practice: part II: vertebro-spinal procedure. Surg Neurol Int. 2016;7(Suppl 3):S77–82.PubMedPubMedCentralGoogle Scholar
  64. 64.
    Maugeri R, Giammalva GR, Graziano F, Iacopino DG. May autologue fibrin glue alone enhance ossification? An unexpected spinal fusion. World Neurosurg. 2016;95:611–2.CrossRefGoogle Scholar
  65. 65.
    Visocchi M, Doglietto F, Della Pepa GM, et al. Endoscope-assisted microsurgical transoral approach to the anterior craniovertebral junction compressive pathologies. Eur Spine J. 2011;20:1518–25.CrossRefGoogle Scholar
  66. 66.
    Visocchi M, Signorelli F, Liao C, Rigante M, Paludetti G, Barbagallo G, et al. Endoscopic endonasal approach for craniovertebral junction pathologies: myth and truth in clinical series and personal experience. World Neurosurg. 2017;101:122–9.  https://doi.org/10.1016/j.wneu.2017.01.099.CrossRefPubMedGoogle Scholar
  67. 67.
    Visocchi M, Pietrini D, Tufo T, Fernandez E, Di Rocco C. Preoperative irreducible C1–C2 dislocations: intraoperative reduction and posterior fixation. The always posterior strategy. Acta Neurochir. 2009;151(5):551–9.CrossRefGoogle Scholar
  68. 68.
    Visocchi M, Iacopino DG, Signorelli F, Olivi A, Maugeri R. Walk the line. The surgical highways to the craniovertebral junction in endoscopic approaches: a historical perspective. World Neurosurg. 2018;110:544–57.  https://doi.org/10.1016/j.wneu.2017.06.125.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2019

Authors and Affiliations

  • Angelo Ferrante
    • 1
  • Francesco Ciccia
    • 1
  • Giuseppe Roberto Giammalva
    • 2
  • Domenico Gerardo Iacopino
    • 2
  • Massimiliano Visocchi
    • 3
  • Federica Macaluso
    • 1
  • Rosario Maugeri
    • 2
  1. 1.Di.Bi.M.I.S., Section of Rheumatology, University of PalermoPalermoItaly
  2. 2.Department of Experimental Biomedicine and Clinical Neurosciences, School of Medicine, Neurosurgical ClinicUniversity of PalermoPalermoItaly
  3. 3.Institute of NeurosurgeryCatholic University of RomeRomeItaly

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