Skip to main content

Advertisement

SpringerLink
Log in

Clinical features of atlantoaxial involvement in patients with rheumatoid arthritis using 18F-fluorodeoxyglucose-positron emission tomography with computed tomography

  • Original Article
  • Published:
Clinical Rheumatology Aims and scope Submit manuscript

Abstract

Introduction/objectives

Cervical spine involvement is one of the most serious complications in rheumatoid arthritis (RA). The study aim was to assess the clinical significance of atlantoaxial (AA) joint involvement detected by 18F-fluorodeoxyglucose (FDG)-positron emission tomography (PET) with computed tomography (CT) in patients with RA.

Method

A prospective cross-sectional study was conducted to evaluate AA joint involvement detected by FDG-PET/CT in consecutive RA patients from December 2017 to February 2022. We investigated the relationship between AA joint involvement and clinical data, including disease activity and patients’ cervical symptoms.

Results

Among 48 patients enrolled, abnormal FDG uptake at AA joint was detected in 13 (27%). Rheumatoid factor titre, initial disease activity score 28-erythrocyte sedimentation rate and total standardized uptake value were significantly higher in the 13 patients than in the others (P = 0.004, P < 0.001 and P = 0.001, respectively). All patients with abnormal FDG uptake at AA joint had some cervical symptoms regardless of cervical spine X-ray abnormalities. Neck pain on movement and at rest were more frequent in the 13 patients than in the others (P = 0.001 and P = 0.004, respectively). The most sensitive symptom associated with AA joint involvement was neck pain on movement (sensitivity, 69%), and the most specific symptom was neck pain at rest (specificity, 100%).

Conclusions

AA joint involvement was commonly observed by FDG-PET/CT in patients with active RA, independent of radiographic findings. Specific cervical symptoms can be important surrogate markers for detection of potential AA synovitis associated with active RA.

Key Points

• AA joint involvement was frequently seen in RA with high disease activity independent of radiographic findings.

• Neck pain was a hallmark of AA joint involvement reflecting disease activity, and resting pain was highly specific.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data availability

The data underlying this article will be shared on reasonable request to the corresponding author.

References

  1. McInnes IB, Schett G (2017) Pathogenetic insights from the treatment of rheumatoid arthritis. Lancet 389:2328–2337. https://doi.org/10.1016/S0140-6736(17)31472-1

    Article  CAS  PubMed  Google Scholar 

  2. Gillick JL, Wainwright J, Das K (2015) Rheumatoid arthritis and the cervical spine: a review on the role of surgery. Int J Rheumatol 2015:252456. https://doi.org/10.1155/2015/252456

    Article  PubMed  PubMed Central  Google Scholar 

  3. Kotecki M, Sotniczuk M, Gietka P, Gasik R, Sudol-Szopinska I (2021) Imaging of cervical spine involvement in inflammatory arthropathies: a review. Pol J Radiol 86:e620–e629. https://doi.org/10.5114/pjr.2021.111363

    Article  PubMed  PubMed Central  Google Scholar 

  4. Wasserman BR, Moskovich R, Razi AE (2011) Rheumatoid arthritis of the cervical spine--clinical considerations. Bull NYU Hosp Jt Dis 69:136–148

    PubMed  Google Scholar 

  5. Neva MH, Hakkinen A, Makinen H, Hannonen P, Kauppi M et al (2006) High prevalence of asymptomatic cervical spine subluxation in patients with rheumatoid arthritis waiting for orthopaedic surgery. Ann Rheum Dis 65:884–888. https://doi.org/10.1136/ard.2005.042135

    Article  CAS  PubMed  Google Scholar 

  6. Shlobin NA, Dahdaleh NS (2021) Cervical spine manifestations of rheumatoid arthritis: a review. Neurosurg Rev 44:1957–1965. https://doi.org/10.1007/s10143-020-01412-1

    Article  PubMed  Google Scholar 

  7. Zhang T, Pope J (2015) Cervical spine involvement in rheumatoid arthritis over time: results from a meta-analysis. Arthritis Res Ther 17:148. https://doi.org/10.1186/s13075-015-0643-0

    Article  PubMed  PubMed Central  Google Scholar 

  8. Manczak M, Gasik R (2017) Cervical spine instability in the course of rheumatoid arthritis - imaging methods. Reumatologia 55:201–207. https://doi.org/10.5114/reum.2017.69782

    Article  PubMed  PubMed Central  Google Scholar 

  9. Baker JF, Conaghan PG, Gandjbakhch F (2018) Update on magnetic resonance imaging and ultrasound in rheumatoid arthritis. Clin Exp Rheumatol 36(Suppl 114):16–23

    PubMed  Google Scholar 

  10. Kono M, Kamishima T, Yasuda S, Sakamoto K, Abe S et al (2017) Effectiveness of whole-body magnetic resonance imaging for the efficacy of biologic anti-rheumatic drugs in patients with rheumatoid arthritis: a retrospective pilot study. Mod Rheumatol 27:953–960. https://doi.org/10.1080/14397595.2016.1276425

    Article  CAS  PubMed  Google Scholar 

  11. Magarelli N, Simone F, Amelia R, Leone A, Bosello S et al (2010) MR imaging of atlantoaxial joint in early rheumatoid arthritis. Radiol Med 115:1111–1120. https://doi.org/10.1007/s11547-010-0574-4

    Article  CAS  PubMed  Google Scholar 

  12. Beckers C, Ribbens C, Andre B, Marcelis S, Kaye O et al (2004) Assessment of disease activity in rheumatoid arthritis with (18)F-FDG PET. J Nucl Med 45:956–964

    CAS  PubMed  Google Scholar 

  13. Fosse P, Kaiser MJ, Namur G, de Seny D, Malaise MG et al (2018) (18)F- FDG PET/CT joint assessment of early therapeutic response in rheumatoid arthritis patients treated with rituximab. Eur J Hybrid Imaging 2:6. https://doi.org/10.1186/s41824-017-0022-y

    Article  PubMed  Google Scholar 

  14. Elzinga EH, van der Laken CJ, Comans EF, Boellaard R, Hoekstra OS et al (2011) 18F-FDG PET as a tool to predict the clinical outcome of infliximab treatment of rheumatoid arthritis: an explorative study. J Nucl Med 52:77–80. https://doi.org/10.2967/jnumed.110.076711

    Article  PubMed  Google Scholar 

  15. Kubota K, Ito K, Morooka M, Mitsumoto T, Kurihara K et al (2009) Whole-body FDG-PET/CT on rheumatoid arthritis of large joints. Ann Nucl Med 23:783–791. https://doi.org/10.1007/s12149-009-0305-x

    Article  PubMed  Google Scholar 

  16. Okamura K, Yonemoto Y, Okura C, Higuchi T, Tsushima Y et al (2014) Evaluation of tocilizumab therapy in patients with rheumatoid arthritis based on FDG-PET/CT. BMC Musculoskelet Disord 15:393. https://doi.org/10.1186/1471-2474-15-393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Suto T, Yonemoto Y, Okamura K, Okura C, Kaneko T et al (2017) Predictive factors associated with the progression of large-joint destruction in patients with rheumatoid arthritis after biologic therapy: a post-hoc analysis using FDG-PET/CT and the ARASHI (assessment of rheumatoid arthritis by scoring of large-joint destruction and healing in radiographic imaging) scoring method. Mod Rheumatol 27:820–827. https://doi.org/10.1080/14397595.2016.1266132

    Article  CAS  PubMed  Google Scholar 

  18. Yonemoto Y, Okamura K, Takeuchi K, Kaneko T, Kobayashi T et al (2016) [18F] fluorodeoxyglucose uptake as a predictor of large joint destruction in patients with rheumatoid arthritis. Rheumatol Int 36:109–115. https://doi.org/10.1007/s00296-015-3331-0

    Article  CAS  PubMed  Google Scholar 

  19. Suto T, Okamura K, Yonemoto Y, Okura C, Tsushima Y et al (2016) Prediction of large joint destruction in patients with rheumatoid arthritis using 18F-FDG PET/CT and disease activity score. Medicine (Baltimore) 95:e2841. https://doi.org/10.1097/MD.0000000000002841

    Article  CAS  PubMed  Google Scholar 

  20. Yonemoto Y, Okamura K, Kobayashi T, Kaneko T, Okura C et al (2017) Predictive factors related to shoulder joint destruction in rheumatoid arthritis patients treated with biologics: a prospective study. Mod Rheumatol 27:587–592. https://doi.org/10.1080/14397595.2016.1245125

    Article  CAS  PubMed  Google Scholar 

  21. Kaneta T, Hakamatsuka T, Yamada T, Takase K, Sato A et al (2006) Atlantoaxial osteoarthritis in rheumatoid arthritis: FDG PET/CT findings. Clin Nucl Med 31:209. https://doi.org/10.1097/01.rlu.0000204124.79497.bb

    Article  PubMed  Google Scholar 

  22. Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT et al (2010) 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 62:2569–2581. https://doi.org/10.1002/art.27584

    Article  PubMed  Google Scholar 

  23. Goerres GW, Forster A, Uebelhart D, Seifert B, Treyer V et al (2006) F-18 FDG whole-body PET for the assessment of disease activity in patients with rheumatoid arthritis. Clin Nucl Med 31:386–390. https://doi.org/10.1097/01.rlu.0000222678.95218.42

    Article  PubMed  Google Scholar 

  24. Matsui T, Nakata N, Nagai S, Nakatani A, Takahashi M et al (2009) Inflammatory cytokines and hypoxia contribute to 18F-FDG uptake by cells involved in pannus formation in rheumatoid arthritis. J Nucl Med 50:920–926. https://doi.org/10.2967/jnumed.108.060103

    Article  CAS  PubMed  Google Scholar 

  25. Chaudhari AJ, Ferrero A, Godinez F, Yang K, Shelton DK et al (2016) High-resolution (18)F-FDG PET/CT for assessing disease activity in rheumatoid and psoriatic arthritis: findings of a prospective pilot study. Br J Radiol 89:20160138. https://doi.org/10.1259/bjr.20160138

    Article  PubMed  PubMed Central  Google Scholar 

  26. Lee SJ, Jeong JH, Lee CH, Ahn BC, Eun JS et al (2019) Development and validation of an (18) F-fluorodeoxyglucose-positron emission tomography with computed tomography-based tool for the evaluation of joint counts and disease activity in patients with rheumatoid arthritis. Arthritis Rheumatol 71:1232–1240. https://doi.org/10.1002/art.40860

    Article  CAS  PubMed  Google Scholar 

  27. Zhu S, Xu W, Luo Y, Zhao Y, Liu Y (2017) Cervical spine involvement risk factors in rheumatoid arthritis: a meta-analysis. Int J Rheum Dis 20:541–549. https://doi.org/10.1111/1756-185X.13096

    Article  CAS  PubMed  Google Scholar 

  28. American College of Rheumatology Ad Hoc Committee on Clinical Guidelines (1996) Guidelines for the initial evaluation of the adult patient with acute musculoskeletal symptoms. Arthritis Rheum 39:1–8. https://doi.org/10.1002/art.1780390102

  29. Elzinga EH, van der Laken CJ, Comans EF, Lammertsma AA, Dijkmans BA et al (2007) 2-Deoxy-2-[F-18]fluoro-D-glucose joint uptake on positron emission tomography images: rheumatoid arthritis versus osteoarthritis. Mol Imaging Biol 9:357–360. https://doi.org/10.1007/s11307-007-0113-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Chaudhari AJ, Bowen SL, Burkett GW, Packard NJ, Godinez F et al (2010) High-resolution (18)F-FDG PET with MRI for monitoring response to treatment in rheumatoid arthritis. Eur J Nucl Med Mol Imaging 37:1047. https://doi.org/10.1007/s00259-009-1364-x

    Article  PubMed  PubMed Central  Google Scholar 

  31. Monet A, Massonnat R, Merino B, Riviere A, Richez C (2014) Crowned dens syndrome diagnosed on (1)(8)F-FDG PET/CT. Clin Nucl Med 39:1041–1042. https://doi.org/10.1007/s40336-021-00445-w

    Article  PubMed  Google Scholar 

  32. Casali M, Lauri C, Altini C, Bertagna F, Cassarino G et al (2021) State of the art of (18)F-FDG PET/CT application in inflammation and infection: a guide for image acquisition and interpretation. Clin Transl Imaging 9:299–339. https://doi.org/10.1097/RLU.0000000000000544

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all of the medical staff in the Department of Internal Medicine, Radiology Section, and in the Nuclear Medicine Centre in our hospital for their clinical contributions. The authors would like to thank Enago (www.enago.jp) for the English language review.

Author information

Authors and Affiliations

  1. Department of Internal Medicine, Japanese Red Cross Kitami Hospital, N6E2, Kitami, Hokkaido, 090-8666, Japan

    Atsushi Noguchi & Takashi Kurita

  2. Department of Infectious Diseases, Tokyo Medical and Dental University Hospital, Tokyo, Japan

    Takashi Kurita

  3. Department of Radiology, Japanese Red Cross Kitami Hospital, Kitami, Japan

    Katsura Matsuzawa

Authors
  1. Atsushi Noguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takashi Kurita
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katsura Matsuzawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TK contributed to the study conception and design. AN collected patients’ clinical data and performed the statistical analysis. KM interpreted FDG-PET/CT images including SUV scoring. The first draft of the manuscript was written by AN and TK. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Atsushi Noguchi.

Ethics declarations

Ethical standards

Our study complies with the principles of the Declaration of Helsinki, the locally appointed ethics committee approved the research protocol and written informed consent was obtained from the subjects.

Disclosures

None.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Noguchi, A., Kurita, T. & Matsuzawa, K. Clinical features of atlantoaxial involvement in patients with rheumatoid arthritis using 18F-fluorodeoxyglucose-positron emission tomography with computed tomography. Clin Rheumatol 42, 1875–1884 (2023). https://doi.org/10.1007/s10067-023-06586-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-023-06586-9

Keywords

Search

Navigation