Top

Arthritis Research & Therapy

Published in:

Open Access 01-12-2018 | Research article

Pannus inflammation in sacroiliitis following immune pathological injury and radiological structural damage: a study of 193 patients with spondyloarthritis

Authors: Dan min Wang, Ling Lin, Jian hua Peng, Yao Gong, Zhi duo Hou, Su biao Chen, Zheng yu Xiao

Published in: Arthritis Research & Therapy | Issue 1/2018

Abstract

Background

The pathogenesis of sacroiliitis is unclear; therefore, we aimed to systematically study the immunopathology of sacroiliitis in patients with axial spondyloarthritis (axSpA), and explore the relationship between pannus formation, inflammation, and the structural damage caused by sacroiliitis.

Methods

Fine needle aspiration biopsy of the sacroiliac joint (SIJ) was performed in 193 patients with axSpA. Clinical, laboratory, and imaging data were collected at baseline and during the follow up. Immunohistochemistry analysis was performed to detect CD34+ microvessels, CD68+ osteoclasts/macrophages, vascular endothelial growth factor (VEGF), metalloproteinase-3 (MMP-3), tumor necrosis factor-α (TNF-α), and caspase-3. Autopsy subjects were used as controls.

Results

In early sacroiliitis (grade 0–1) all pathological features could be observed, with the most common being subchondral pannus formation. Among the 193 patients, 98 were followed up for 1–13 years (mean 3.6 years); 63.3% had radiological progression at the endpoint. Multiple regression analysis showed that cartilage pannus invasion (OR 2.99, P = 0.010) and endochondral ossification (OR 3.97, P = 0.049) at baseline were risk factors for radiological structural damage. Compared to SIJ controls, the subchondral microvessel density, number of CD68+ multinuclear osteoclasts, and the levels of VEGF, caspase-3, MMP-3, and TNF-α expressed at the interface of the bone and cartilage were significantly higher in patients with sacroiliitis.

Conclusions

Subchondral fibrovascular tissue formation is the most important pathological feature in early sacroiliitis. The existence of cartilage pannus invasion or endochondral ossification at baseline can predict radiological structural damage during the follow up.

Available only for authorised users

Shichikawa K. Histopathology of early sacroiliitis and enthesitis in ankylosing spondylitis. In: Advances in inflammation research, vol. 9. New York: Raven Press; 1985. p. 15–24.

Braun J, Bollow M, Neure L, et al. Use of immunohistologic and in situ hybridization techniques in the examination of sacroiliac joint biopsy specimens from patients with ankylosing spondylitis. Arthritis Rheum. 1995;38:499–505.CrossRefPubMed

François RJ, Gardner DL, Degrave EJ, Bywaters EG. Histopathologic evidence that sacroilitiis in ankylosing spondylitis is not merely enthesitis. Arthritis Rheum. 2000;43:2011–24.CrossRefPubMed

Gong Y, Zheng N, Chen S, Xiao Z, Wu M, Liu Y, Zeng QY. Ten years’ experience on needle biopsy in the early diagnosis of sacroiliitis. Arthritis Rheum. 2012;64:1399–406. https://doi.org/10.1002/art.33453.CrossRefPubMed

Peng J, Gong Y, Zhang Y, Wang D, Xiao Z. Immunohistological analysis of active sacroiliitis in patients with axial spondyloarthritis. Medicine (Baltimore). 2017; 96: e6605. https://doi.org/https://doi.org/10.1097/MD.0000000000006605.

Hermann KG, Bollow M. Magnetic resonance imaging of sacroiliitis in patients with spondyloarthritis: correlation with anatomy and histology. Rofo. 2014;186(3):230–7. https://doi.org/10.1055/s-0033-1350411.PubMedCrossRef

Rudwaleit M, Landewé R, van der Heijde D, Listing J, Brandt J, Braun J, et al. The development of Assessment of SpondyloArthritis intemational Society classification criteria for axial spondyloarthritis (part I): classification of paper patients by expert opinion including uncertainty appraisal. Ann Rheum Dis. 2009;68:770–6. https://doi.org/10.1136/ard.2009.108217.CrossRefPubMed

Rudwaleit M, van der Heijde D, Landewé R, Listing J, Akkoc N, Brandt J. et al. The development of Assessment of SpondyloArthritis international Society classification criteria for axial spondyloarthritis (partII): validation and final selection. Ann Rheum Dis. 2009;68:777–83. https://doi.org/10.1136/ard.2009.108233.CrossRefPubMed

Van der Linden S, Valkenburg HA, Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum. 1984;27:361–8.CrossRefPubMed

10.

Sieper J, van der Heijde D. Review: Nonradiographie axial spondyloarthritis: new definition of an old disease? Arthritis Rheum, 2013; 65: 543–551. https://doi.org/https://doi.org/10.1002/art.37803.

11.

Maksymowych WP, Inman RD, Salonen D, Dhillon SS, Williams M, Stone M, et al. Spondyloarthritis research Consortium of Canada magnetic resonance imaging index for assessment of sacroiliac joint inflammation in ankylosing spondylitis. Arthritis Rheum. 2005;53:703–9.CrossRefPubMed

12.

Wang QW, Zeng QY, Xiao ZY, Chen SB, Liu Y, Wu MY. Needle biopsy of spondyloarthropathy: pathological features and clinical significance. Zhonghua Nei Ke Za Zhi. 2004;43:832–6. [Article in Chinese]PubMed

13.

Cruickshank B. Histopathology of diarthrodial joints in ankylosing spondylitis. Ann Rheum Dis. 1951;10:393–404.CrossRefPubMedPubMedCentral

14.

Engfeldt B, Romanus R, Yden S. Histological studies of pelvo-spondylitis ossificans (ankylosing spondylitis) correlated with clinical and radiological findings. Ann Rheum Dis. 1954;13:219–28.CrossRefPubMedPubMedCentral

15.

Ball J. Enthesopathy of rheumatoid and ankylosing spondylitis. Ann Rheum Dis. 1971;30:213–23.CrossRefPubMedPubMedCentral

16.

Poole AR. The histopathology of ankylosing spondylitis: are there unifying hypotheses? Am J Med Sci. 1998;316:228–33.CrossRefPubMed

17.

Fournié B. Pathology and clinico-pathologic correlations in spondyloarthropathies. Joint Bone Spine. 2004;71:525–9.CrossRefPubMed

18.

Benjamin M, McGonagle D. The enthesis organ concept and its relevance to the spondyloarthropathies. Adv Exp Med Biol. 2009;649:57–70.CrossRefPubMed

19.

Maksymowych WP. Ankylosing spondylitis–at the interface of bone and cartilage. J Rheumatol. 2000;27:2295–301.PubMed

20.

Schichikawa K, Tsyimoto M, Nishioka J, et al. Histopathology of early sacroiliitis and enthesitis in ankylosing spondylitis. Advances in inflammation research. In: Ziff M, Cohen SB, editors. The spondyloarthropathies, vol. 9. New York: Raven Press; 1985. p. 15–24.

21.

Francois RJ, Gardner DL, Bywaters EGL. Sacroiliac joint pathology in ankylosing spondylitis. Clin Rheumatol. 1997;16:509.

22.

Blum U, Buitrago-Tellez C, Mundinger A, Krause T, Laubenberger J, Vaith P, et al. Magnetic resonance imaging (MRI) for detection of active sacroiliitis−a prospective study comparing conventional radiography, scintigraphy, and contrast enhanced MRI. J Rheumatol. 1996;23:2107–15.PubMed

23.

Muche B, Bollow M, François RJ, Sieper J, Hamm B, Braun J. Anatomic structures involved in early- and late-stage sacroiliitis in spondylarthritis: a detailed analysis by contrast-enhanced magnetic resonance imaging. Arthritis Rheum. 2003;48:1374–84.CrossRefPubMed

24.

Bollow M, Hermann KG, Biedermann T, Sieper J, Schöntube M, Braun J. Very early spondyloarthritis: where the inflammation in the sacroiliac joints starts. Ann Rheum Dis. 2005;64:1644–6.CrossRefPubMedPubMedCentral

25.

Marzo-Ortega H, McGonagle D, O'Connor P, Hensor EM, Bennett AN, Green MJ, et al. Baseline and 1-year magnetic resonance imaging of the sacroiliac joint and lumbar spine in very early inflammatory back pain. Relationship between symptoms, HLA-B27 and disease extent and persistence. Ann Rheum Dis 2009; 68:1721–1727. https://doi.org/https://doi.org/10.1136/ard.2008.097931.

26.

Marzo-Ortega H, McGonagle D, Bennett AN. Magnetic resonance imaging in spondyloarthritis−how to quantify findings and measure response. Curr Opin Rheumatol 2010; 22:381–387. https://doi.org/https://doi.org/10.1097/BOR.0b013e328339381e.

27.

Baeten D, Demetter P, Cuvelier C, Van Den Bosch F, Kruithof E, Van Damme N, et al. Comparative study of the synovial histology in rheumatoid arthritis, spondyloarthropathy, and osteoarthritis: influence of disease duration and activity. Ann Rheum Dis. 2000;59:945–53.CrossRefPubMedPubMedCentral

28.

Baeten D, De Keyser F. The histopathology of spondyloarthropathy. Curr Mol Med. 2004;4:1–12.CrossRefPubMed

29.

Appel H, Kuhne M, Spiekermann S, Köhler D, Zacher J, Stein H, et al. Immuno-histochemical analysis of hip arthritis in ankylosing spondylitis. Arthritis Rheum. 2006;54:1805–13.CrossRefPubMed

30.

Kruithof E, Baeten D, Van den Bosch F, Mielants H, Veys EM, De Keyser F. Histological evidence that infliximab treatment leads to downregulation of inflammation and tissue remodelling of the synovial membrane in spondyloarthropathy. Ann Rheum Dis. 2005;64:529–36.CrossRefPubMed

31.

Carlevaro MF, Cermelli S, Cancedda R, Descalzi Cancedda F. Vascular endothelial growth factor (VEGF) in cartilage neovascularization and chondrocyte differentiation: auto-paracrine role during endochondral bone formation. J Cell Sci. 2000;113:59–69.PubMed

32.

Babarina AV, Möllers U, Bittner K, Vischer P, Bruckner P. Role of the subchondral vascular system in endochondral ossification: endothelial cell-derived proteinases derepress late cartilage differentiation in vitro. Matrix Biol. 2001;20:205–13.CrossRefPubMed

33.

Suri S, Walsh DA. Osteochondral alterations in osteoarthritis. Bone 2012, 51:204–211. https://doi.org/https://doi.org/10.1016/j.bone.2011.10.010.

Title: Pannus inflammation in sacroiliitis following immune pathological injury and radiological structural damage: a study of 193 patients with spondyloarthritis
Authors: Dan min Wang
Ling Lin
Jian hua Peng
Yao Gong
Zhi duo Hou
Su biao Chen
Zheng yu Xiao
Publication date: 01-12-2018
Publisher: BioMed Central
Published in: Arthritis Research & Therapy / Issue 1/2018
Electronic ISSN: 1478-6362
DOI: https://doi.org/10.1186/s13075-018-1594-z

ACC 2024 Congress Coverage

Cardiology Video

Highlights from the ACC 2024 Congress

Watch now

Watch official videos from the ACC congress summarizing key highlights from the last year in heart failure, cardiomyopathies, valvular disease, pulmonary vascular disease, and pediatric cardiology.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits

ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

ACC 2024 Congress

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2018

Role of the mTOR pathway in minor salivary gland changes in Sjogren’s syndrome and systemic sclerosis

Genome-wide association study meta-analysis identifies five new loci for systemic lupus erythematosus

Recombinant human proteoglycan-4 reduces phagocytosis of urate crystals and downstream nuclear factor kappa B and inflammasome activation and production of cytokines and chemokines in human and murine macrophages

The lack of association between the burden of monosodium urate crystals assessed with dual-energy computed tomography or ultrasonography with cardiovascular risk in the commonly high-risk gout patient