Abstract
Objective
As anaemia represents a biomarker for increased radiographic damage in rheumatoid arthritis, we aimed to investigate whether it independently predicts spinal radiographic progression in axial spondyloarthritis (axSpA).
Methods
AxSpA patients with available haemoglobin levels from the prospective Swiss Clinical Quality Management Registry were included for comparison of patients with and without anaemia. Spinal radiographic progression was assessed according to the modified Stoke Ankylosing Spondylitis Spinal Score (mSASSS) in patients with ankylosing spondylitis (AS) if ≥ 2 sets of spinal radiographs were available every 2 years. The relationship between anaemia and progression (defined as an increase ≥ 2 mSASSS units in 2 years) was analysed with generalized estimating equation models after adjustment for the Ankylosing Spondylitis Disease Activity Score (ASDAS) and potential confounding, as well as after multiple imputations of missing values.
Results
A total of 212/2522 axSpA patients presented with anaemia (9%). Anaemic patients had higher clinical disease activity, higher acute phase reactants and more severe impairments in physical function, mobility and quality of life. In the subgroup of patients with AS (N = 433), a comparable mSASSS progression was found in anaemic and non-anaemic patients (OR 0.69, 95% CI 0.25 to 1.96, p = 0.49). Age, male sex, baseline radiographic damage and ASDAS were associated with enhanced progression. The results were confirmed in complete case analyses and with progression defined as the formation of ≥ 1 syndesmophyte in 2 years.
Conclusion
Although anaemia was associated with higher disease activity in axSpA, it did not additionally contribute to the prediction of spinal radiographic progression.
Key Points • Anaemia is associated with higher disease activity and more severely impaired physical function, mobility and quality of life in axSpA. • Anaemia does not provide an additional value to ASDAS for prediction of spinal radiographic progression. |
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Spinal structural damage and its progression are major determinants of functional impairment in patients with axial spondyloarthritis (axSpA) and particularly in patients with ankylosing spondylitis (AS) [1, 2]. Structural damage is limited to a selected group of patients, and it is the most conclusive predictor of further progression [3, 4]. Only a few additional predictors of progression have been identified over the last years, including acute phase reactants, fatty post-inflammatory vertebral corner changes on magnetic resonance imaging (MRI), male gender, smoking and manual jobs [5]. The level of disease activity as assessed by the Ankylosing Spondylitis Disease Activity Score (ASDAS) proved to be a better biomarker of progression when compared to some of its components, in particular the Bath Ankylosing Disease Activity Index (BASDAI) and the level of C-reactive protein (CRP) [6, 7]. In contrast, treatment with tumour necrosis factor inhibitors (TNFi) seems to be able to retard radiographic progression [8]. A recent analysis suggested that a genetic factor, the ryanodine receptor 3 gene, might be associated with severe radiographic damage [9]. Other biomarkers proved of modest benefit [10,11,12]. Anaemia predicted radiographic progression independently of common disease activity parameters in rheumatoid arthritis (RA) [13, 14]. As anaemia is known to be associated with disease activity in AS [15], we thought to determine whether it could provide an additional predictive value to ASDAS in AS.
Methods
Study population
We took advantage of the Swiss Clinical Quality Management (SCQM) registry of patients with axSpA, as diagnosed by a board-certified rheumatologist in Switzerland [16]. The registry was initiated in 2005. Clinical assessments were performed according to the recommendations of the Assessment of SpondyloArthritis International Society (ASAS) [17]. Patients were included in the current study if, in addition to diagnosis, they also fulfilled the ASAS classification criteria for axSpA [18] and if an assessment of haemoglobin (Hb) was available (either at inclusion or at the start of a radiographic interval, depending on the analysis performed; see below). For the analysis of spinal radiographic progression, only patients fulfilling the radiographic criterion of the modified New York classification [19] were considered, as patients with nonradiographic disease status have only minimal spinal progression [20]. Written informed consent was obtained from all patients. The study was approved by the Ethics Commission of the Canton of Zurich (KEK-ZH-Nr. 2014–0439). We have chosen the database snapshot of August 1, 2016, for the following reasons: (a) it represented the time-point of radiographic scoring of available spinal radiographs in SCQM; (b) no biological or targeted-synthetic disease-modifying drugs other than TNFi had been approved at this time-point to additionally influence our analyses.
Laboratory assessments
Anaemia was defined according to the definition of the World Health Organization (WHO): Hb level below 12 g/dl in women and below 13 g/dl in men [21]. Hb concentrations, C-reactive protein (CRP) levels and erythrocyte sedimentation rates (ESR) were obtained from certified local laboratories and their levels were entered in the database by the treating rheumatologist.
Radiographic assessments
As data on radiographic progression in axSpA is limited, SCQM rheumatologists were instructed to perform radiographs of the pelvis and of the spine every 2 years if clinically appropriate and in the absence of contraindications. Images were uploaded to the SCQM database. Sacroiliac joint (SIJ) damage was assessed on anteroposterior pelvis radiographs according to the radiographic criterion of the modified New York classification criteria [19] centrally by two calibrated readers of the SCQM scientific committee. Paired reading of lateral radiographs of the cervical and lumbar spine taken every 2 years (up to 5 radiographic intervals, corresponding to 10 years of follow-up) was performed by two calibrated readers according to the modified Stoke Ankylosing Spondylitis Spine Score (mSASSS) [22] as already published (radiographs were not scored again) [7]. Mean scores per vertebral corner (VC) were used. Images were disregarded in the presence of > 3 missing VCs per cervical and lumbar segment [7]. Independent adjudication was performed by a third scorer if the mSASSS status scores varied by ≥ 5 mSASSS units. Radiographic progression was defined either as an increase in mSASSS of at least 2 units in 2 years or as the formation of at least one syndesmophyte in 2 years, with syndesmophytes only counted if both readers agreed on their presence.
Statistical analysis
Comparisons between characteristics of patients with and without anaemia were performed using Fisher’s exact test for nominal variables and the Mann–Whitney test for continuous variables. Generalized estimating equation (GEE) models with an “exchangeable” correlation structure were used to examine the relationship between anaemia and radiographic progression over time [7]. The progression of at least 2 mSASSS units in 2 years was modelled with the use of the binomial family and the logistic link function, and the models were adjusted for the following variables: age, sex, ASDAS, either mSASSS at the start of the interval or the presence of syndesmophytes at the start of the interval, prior treatment with TNFi, current smoking status and the respective length of the radiographic interval. Multiple imputation was used for missing covariate data, with ASDAS derived by passive imputation (missingness: ASDAS 104/617 intervals, smoking status 84/617 intervals, anaemia 70/617 intervals). A Wald test was performed to assess the importance of the addition of anaemia in the prediction model for progression.
Results
Characteristics of axSpA patients with respect to anaemia status
The disposition of patients at inclusion in the SCQM axSpA cohort is depicted in a flow chart in Fig. 1. Out of 3863 with a clinical diagnosis of axSpA, 2522 fulfilled the ASAS axSpA classification criteria. Hb levels were available in 2264 patients (89.8%). Anaemia was observed in 212 of these patients (9.2%). Characteristics of patients with normal Hb levels versus patients with anaemia are shown in Table 1. A higher proportion of patients with anaemia were of female sex (51% vs. 39% in non-anaemic patients). Anaemic patients were slightly older and had a longer disease duration. While the proportion of HLA-B27 positivity was comparable between the two groups, the percentage of patients with definite radiographic SIJ changes was higher in patients with anaemia (80% vs. 72%). Patients with anaemia had significantly higher disease activity as assessed by subjective means (BASDAI) and objective parameters (acute phase reactants, proportion of patients with peripheral arthritis and hip arthritis). In contrast, enthesitis and dactylitis were similarly distributed between the two groups. Paralleling disease activity, physical function, mobility and quality of life (as assessed by the Bath Ankylosing Spondylitis Functional and Mobility Indices and the European Quality of Life Questionnaire 5 domains (EQ-5D), respectively) were more severely impaired in patients with anaemia (Table 1). A higher percentage of non-anaemic patients were already treated with TNFi at inclusion in the SCQM axSpA cohort (23% vs. 16% in anaemic patients), while more patients with anaemia were treated with conventional synthetic disease-modifying anti-rheumatic drugs (19% vs. 12%).
Characteristics of AS patients with respect to anaemia status
Spinal radiographic progression was assessed in patients with radiographic disease, as spinal progression is very limited in patients with nonradiographic axSpA [17]. Hb assessments were available in 445 patients out of 529 patients with at least two sets of spinal radiographs (84.1%) and in 374/433 patients with radiographic intervals at 2-year intervals (86.4%) (Fig. 1). Anaemia was present in 9% of patients in the group with at least 2 sets of radiographs, as well as in the smaller group of patients with sets of radiographs at intervals of 2 years. Comparison of characteristics of non-anaemic vs. anaemic r-axSpA patients is shown for both groups of patients with sequential radiographs in Table 2. The proportion of patients with different numbers of radiographic intervals was comparable in both groups. In line with the results found at inclusion in the SCQM cohort for all axSpA patients, anaemic r-axSpA patients had higher disease activity and more restricted physical function, spinal mobility and quality of life, although numerical differences did not always reach statistical significance given the lower number of patients in the respective comparison groups. The most important differences between anaemic and non-anaemic patients were recorded for acute phase reactants (number of patients with elevated CRP, as well as the height of the CRP and the ESR elevation) (Table 2).
Crude spinal progression analyses
The crude odds of spinal radiographic progression in anaemic versus non-anaemic patients were comparable (OR 1.01, 95% confidence interval (CI) 0.45; 2.23, p = 0.99). This result is also depicted as a cumulative probability plot for mSASSS progression over 2 years for individual radiographic intervals in patients with and without anaemia in Fig. 2.
Adjusted spinal progression analyses
Anaemia was not an independent predictor of spinal progression after adjustment for sex, baseline damage, ASDAS, smoking, TNFi treatment, age and length of the radiographic interval, and multiple imputations of missing covariate data (OR 0.69, 95% CI 0.25 to 1.96, p = 0.49; Table 3, part A). Age, male sex, baseline mSASSS and ASDAS were associated with accelerated progression in this model. We found no evidence that adding anaemia to the progression model significantly improved the model (Chi-squared value of 0.22, p = 0.64). The main results were confirmed in a complete case analysis (Table 3, part B). Moreover, there was no association of anaemia with spinal radiographic progression in the analyses performed with an alternative definition of progression, the formation of at least one syndesmophyte during an X-ray interval (OR 0.61, 95% CI 0.22 to 1.70, p = 0.35; Table 4).
Discussion
Anaemia, as defined by the WHO, was detectable in 9% of patients with axSpA in our cohort. This proportion is two times higher than the one found in patients with recently diagnosed, incident AS in a recent publication [23]. However, our cohort includes patients with longstanding disease with > 10 years of mean symptom duration. The frequency of anaemia is lower than in an Italian analysis (15%) of patients requiring biologic treatment [15]. In that particular study, its pathogenesis was established as anaemia of inflammation, characterized by normal mean corpuscular volume of erythrocytes, low serum iron levels and iron-binding capacity, and elevated serum ferritin, after exclusion of other causes of anaemia. It resolved in 82% of patients following treatment with a TNFi [15], a finding confirmed by other studies in AS [24, 25]. The proportion of patients already treated with TNFi at recruitment in our cohort was 23% in the non-anaemic group, contrasting with a lower percentage in the group of patients with anaemia (16%). Anaemia was still associated with higher BASDAI levels, more peripheral arthritis and particularly with a relevantly higher proportion of patients with elevated CRP and with higher levels of CRP as well as of ESR in both axSpA and AS.
Our group reported that anaemia is associated with a more severe progression of erosive damage in the SCQM cohort of patients with RA [13], a result that was confirmed in another RA population [14]. Follow-up analyses revealed that clinical disease activity was more closely associated with haemoglobin levels than with the effects of treatment with TNFi and interleukin-6 receptor inhibitors [26]. These findings formed the background for the analysis of radiographic progression in AS performed here. Disease activity, particularly when assessed by the ASDAS, is associated with the accelerated progression of osteoproliferative structural changes in AS [6]. The latter can be retarded by treatment with TNFi [7], as confirmed in additional observational analyses (reviewed in [8, 27]).
Our study reveals that, in contrast to RA, anaemia is of no additional benefit to common disease activity assessments for the prediction of radiographic progression in AS. We have used state-of-the-art statistical methods (GEE, multiple imputation of missing covariate data) and have adjusted our analyses for known predictors of progression and for time-varying treatment with TNFi. To simplify the therapeutic context, we have used data from the SCQM cohort at a time, when alternative biologic or targeted-synthetic drugs were not approved for axSpA. Complete case analyses confirmed the robustness of our results. MRI data on inflammatory or post-inflammatory SIJ or spinal changes is currently not available in SCQM, which represents a limitation of our analyses. The relationship between MRI spinal inflammation and new bone formation is quite complex, as reliable detection requires periods of at least 2 years’ duration and involves the intermediate development of fatty degeneration [28, 29]. Besides differences in what constitutes structural damage between RA and axSpA (predominantly erosive changes vs. osteoproliferation), the lower frequency and severity of anaemia in axSpA in comparison to RA [13, 14, 23, 25] might preclude a relevant impact on radiographic progression in axSpA. Indeed, our study may potentially be underpowered to detect small effects on radiographic damage progression associated with anaemia. Our results parallel a series of negative findings in the search for biomarkers for radiographic progression in axSpA [30]. Moreover, the added benefit of several serum markers proved to be very modest [10,11,12]. Applying new technologies to identify biomarkers, therefore, remains warranted [9, 30].
Conclusion
Anaemia was associated with increased disease activity in axSpA, but in contrast to RA, it seemed to not independently predict radiographic structural damage.
Data availability
Restrictions apply to the availability of these data. Data is owned by a third party, the Swiss Clinical Quality Management in Rheumatic Diseases (SCQM) foundation. Data may be obtained after approval and permission from the licence holder (SCQM). Contact information for data request: scqm@hin.ch.
References
Machado P, Landewe R, Braun J, Hermann K-GA, Baraliakos X, Baker D, Hsu B, van der Heijde D (2011) A stratified model for health outcomes in ankylosing spondylitis. Ann Rheum Dis 70:1758–1764
Poddubnyy D, Listing J, Haibel H, Knüppel S, Rudwaleit M, Sieper J (2018) Functional relevance of radiographic spinal progression in axial spondyloarthritis: results from the GErman SPondyloarthritis Inception Cohort. Rheumatology (Oxford) 57:703–711
Baraliakos X, Listing J, von der Recke A, Braun J (2009) The natural course of radiographic progression in ankylosing spondylitis – evidence for major individual variations in a large proportion of patients. J Rheumatol 36:997–1002
Van Tubergen A, Ramiro S, van der Heijde D, Dougados M, Mielants H, Landewé R (2012) Development of new syndesmophytes and bridges in ankylosing spondylitis and their predictors: a longitudinal study. Ann Rheum Dis 71:518–523
van der Heijde D, Braun J, Deodhar A, Baraliakos X, Landewé R, Richards HB, Porter B, Readie A (2019) Modified Stoke ankylosing spondylitis spinal score as an outcome measure to assess the impact of treatment on structural progression in ankylosing spondylitis. Rheumatology (Oxford) 58:388–400
Ramiro S, van der Heijde D, van Tubergen A, Stolwijk C, Dougados M, van den Bosch F, Landewé R (2014) Higher disease activity leads to more structural damage in the spine in ankylosing spondylitis: 12-year longitudinal data from the OASIS cohort. Ann Rheum Dis 73:1455–1461
Molnar C, Scherer A, Baraliakos X, de Hooge M, Micheroli R, Exer P, Kissling RO, Tamborrini G, Wildi LM, Nissen MJ, Zufferey P, Bernhard J, Weber U, Landewé RBM, van der Heijde D, Ciurea A (2018) TNF blockers inhibit spinal radiographic progression in ankylosing spondylitis by reducing disease activity: results from the Swiss Clinical Quality Management cohort. Ann Rheum Dis 77:63–69
Sepriano A, Ramiro S, van der Heijde D, Landewé R (2021) Biological DMARDs and disease modification in axial spondyloarthritis: a review through the lens of causal inference. RMD Open 7:e001654
Nam B, Jo S, Bang S-Y, Park Y, Shin JH, Park Y-S, Lee S, Joo KB, Kim T-H (2022) Clinical and genetic factors associated with radiographic damage in patients with ankylosing spondylitis. Ann Rheum Dis. https://doi.org/10.1136/annrheumdis-2022-222796
Hartl A, Sieper J, Syrbe U, Listing J, Hermann K-G, Rudwaleit M, Poddubnyy D (2017) Serum levels of leptin and high molecular weight adiponectin are inversely associated with radiographic spinal progression in patients with ankylosing spondylitis: results from the ENRADAS trial. Arthritis Res Ther 19:140
Rademacher J, Tietz LM, Le L, Hartl A, Hermann K-GA, Sieper J, Mansmann U, Rudwaleit M, Poddubnyy D (2019) Added value of biomarkers compared with clinical parameters for the prediction of radiographic spinal progression in axial spondyloarthritis. Rheumatology 58:1556–1564
Witte T, Köhler M, Georgi J, Schweikhard E, Matthias T, Baerlecken N, Hermann KG, Sieper J, Rudwaleit M, Poddubnyy D (2020) IgA antibodies against CD74 are associated with structural damage in the axial skeleton in patients with axial spondyloarthritis. Clin Exp Rheumatol 38:1127–1131
Möller B, Scherer A, Förger F, Villiger PM, Finckh A (2014) Anaemia may add information to standardised disease activity assessment to predict radiographic damage in rheumatoid arthritis: a prospective cohort study. Ann Rheum Dis 73:691–696
Möller B, Everts-Graber J, Florentinus S, Ki Y, Kupper H, Finckh A (2018) Low hemoglobin and radiographic damage progression in early rheumatoid arthritis: secondary analysis from a phase III trial. Arthritis Care Res (Hoboken) 70:861–868
Niccoli L, Nannini C, Cassarà E, Kaloudi O, Cantini F (2012) Frequency of anemia of inflammation in patients with ankylosing spondylitis requiring anti-TNFα drugs and therapy-induced changes. Int J Rheum Dis 15:56–61
Ciurea A, Scherer A, Exer P, Bernhard J, Dudler J, Beyeler B, Kissling R, Stekhoven D, Rufibach K, Tamborrini G, Weiss B, Müller R, Nissen MJ, Michel BA, van der Heijde D, Dougados M, Boonen A, Weber U (2013) Tumor necrosis factor α inhibition in radiographic and nonradiographic axial spondyloarthritis. Arthritis Rheum 12:3096–3106
Sieper J, Rudwaleit M, Baraliakos X, Brandt J, Braun J, Burgos-Vargas R, Dougados M, Hermann K-G, Landewé R, Maksymowych W, van der Heijde D (2009) The Assessment of SpondyloArthritis international Society (ASAS) handbook: a guide to assess spondyloarthritis. Ann Rheum Dis 68(Suppl2):ii1-44
Rudwaleit M, van der Heijde D, Landewe R, Listing J, Akkoc N, Brandt J, Braun J, Chou CT, Collantes-Estevez E, Dougados M, Huang F, Gu J, Khan MA, Kiralzi Y, Maksymowych WP, Mielants H, Sorensen IJ, Ozgocmen E, Valle-Onate R, Weber U, Wie J, Sieper J (2009) The development of Assessment of SpondyloArthritis international Society classification criteria for axial spondyloarthritis (part II): validation and final selection. Ann Rheum Dis 68:777–783
van der Linden S, Valkenburg HA, Cats A (1984) Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum 7:361–368
Hebeisen M, Micheroli M, Scherer A, Baraliakos X, de Hooge M, van der Heijde D, Landewé R, Bürki K, Nissen MJ, Möller B, Zufferey P, Exer P, Ciurea A (2020) Spinal radiographic progression in axial spondyloarthritis and the impact of classification as nonradiographic versus radiographic disease: Data from the Swiss Clinical Quality Management cohort. PLoS ONE 15:e0230268
DeMaeyer E, Adiels-Tegman M (1985) The prevalence of anaemia in the world. World Health Stat Q 38:302–316
Creemers MCW, Franssen MJAM, van’t Hof MA, Gribnau FWJ, van de Putte LBA, van Riel PLCM (2005) Assessment of outcome in ankylosing spondylitis: an extended radiographic scoring system. Ann Rheum Dis 64:127–9
Meer E, Thrastardottir T, Wang X, Dubreuil M, Chen Y, Gelfand JM, Love TJ, Ogdie A (2022) Risk factors for diagnosis of psoriatic arthritis, psoriasis, rheumatoid arthritis, and ankylosing spondylitis: a set of parallel case-control studies. J Rheumatol 49:53–59
Braun J, van der Heijde D, Doyle MK, Han C, Deodhar A, Inman R, de Vlam K, Burmester GR, van den Bosch F, Xu S, Visvanathan S, Rahman MU (2009) Improvement in hemoglobin levels in patients with ankylosing spondylitis treated with infliximab. Arthritis Rheum 61:1032–1036
Furst DE, Kay J, Wasko MC, Keystone E, Kavanaugh A, Deodhar A, Murphy FT, Magnus JH, Hsia EC, Hsu B, Xu S, Rahman MU, Doyle MK (2013) The effect of golimumab on haemoglobin levels in patients with rheumatoid arthritis, psoriatic arthritis or ankylosing spondylitis. Rheumatology (Oxford) 52:1845–1855
Scholz GA, Leichtle AB, Scherer A, Arndt U, Fiedler M, Aeberli D, Finckh A, Gabay C, Kyburz D, Villiger PM, Möller B (2019) The links of hepcidin and erythropoietin in the interplay of inflammation and iron deficiency in a large observational study of rheumatoid arthritis. Br J Haematol 186:101–112
Torgutalp M, Rios Rodriguez V, Dilbaryan A, Proft F, Protopopov M, Verba M, Rademacher J, Haibel H, Sieper J, Rudwaleit M, Poddubnyy D (2022) Treatment with tumour necrosis factor inhibitors is associated with a time-shifted retardation of radiographic spinal progression in patients with axial spondyloarthritis. Ann Rheum Dis 81:1252–1259
Baraliakos X, Feldmann F, Callhoff J, Listing J, Appelboom T, Brandt J, Van den Bosch F, Breban M, Burmester G, Dougados M, Emery P, Gaston H, Grunke M, Van der Horst-Bruinsma IE, Landewé R, Leirisalo-Repo M, Sieper J, De Vlam K, Pappas D, Kiltz U, Van der Heijde D, Braun J (2014) Which spinal lesions are associated with new bone formation in patients with ankylosing spondylitis treated with anti-TNF agents? A long-term observational study using MRI and conventional radiography. Ann Rheum Dis 73:1819–1825
Stal R, Baraliakos X, van der Heijde D, van Gaalen F, Ramiro S, van den Berg R, Reijierse M, Braun J, Landewé R, Sepriano A (2022) Role of vertebral corner inflammation and fat deposition on MRI on syndesmophyte development detected on whole spine low-dose CT scan in radiographic axial spondyloarthritis. RMD Open 8:e002250
Maksymowych WP (2019) Biomarkers for diagnosis of axial spondyloarthritis, disease activity, prognosis, and prediction of response to therapy. Front Immunol 10:305
Acknowledgements
We thank all patients and their rheumatologists for participation and the whole SCQM staff for data management. A list of contributing rheumatology private practices and hospitals can be found at www.scqm.ch/institutions.
Funding
Open access funding provided by University of Zurich. The SCQM foundation is supported by the Swiss Society of Rheumatology and by Abbvie, Astra Zeneca, Eli-Lilly, iQone Healthcare, Janssen, Merck Sharp & Dohme, Novartis, Pfizer, Samsung Bioepis and Sandoz.
Author information
Authors and Affiliations
Contributions
Study conception and design: AC, RM, SK. Acquisition of clinical data: AC, AF, ARR, BM, DK, KB, MA, MJN, OD, PE, RB, RM. MdH and XB read the spinal radiographs with adjudication performed by AC. Statistical analysis: SK, AS. All authors contributed to the interpretation of data. AC wrote the manuscript and all authors revised the manuscript and approved the final manuscript to be published. AC and SK accept full responsibility for the finished work, had access to the data, and controlled the decision to publish.
Corresponding author
Ethics declarations
Ethics approval
The study has been approved by the Ethics Commission of the Canton of Zurich (KEK-ZH-Nr. 2014–0439) and has been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. Written informed consent was obtained from all patients.
Conflict of interest
AC received honoraria for lectures from AbbVie and Novartis. AF received research grants to his institution from Abbvie, BMS, Galapagos, Eli Lilly and Pfizer, as well as consulting fees from Abbvie, AstraZeneca, BMS, Galapagos, Eli Lilly, Novartis, Merck Sharp & Dohme, Pfizer, Sandoz and Roche. ARR received honoraria for lectures and consultation from Abbvie, Amgen, BMS, UCB, Pfizer, Gilead, Eli Lilly, Novartis and Janssen. AS received consulting fees from Pfizer and support for attending meetings from Gilead. BM received speaking fees from Janssen, Eli Lilly, Novartis and Pfizer, support for attending meetings from Janssen and Pfizer and a research grant from Celgene. DK received consulting fees from Abbvie, Eli Lilly, Janssen, Novartis, Pfizer, Roche and support for attending meetings from Janssen and Eli Lilly. MdH received grants from FWRO/FRSR and honoraria from UCB for participation in advisory board. MJN received consulting and/or speaking fees from Abbvie, Eli Lilly, Janssen, Novartis and Pfizer, as well as a research grant from Novartis. OD received consulting fees from Abbvie. PE received financial support from UCB for attending a meeting. RM received honoraria for lectures or presentations from Abbvie, Eli Lilly, Janssen, Gilead and Pfizer. KB, MA, RB, SK and XB declare they have no conflicts of interest.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Micheroli, R., Kissling, S., Bürki, K. et al. Anaemia is associated with higher disease activity in axial spondyloarthritis but is not an independent predictor of spinal radiographic progression: data from the Swiss Clinical Quality Management Registry. Clin Rheumatol 42, 2377–2385 (2023). https://doi.org/10.1007/s10067-023-06662-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10067-023-06662-0