Spinal radiographic progression is correlated with preclinical atherosclerosis in spondyloarthritis

Abstract

BACKGROUND:

A higher prevalence of cardiovascular risk was observed in spondyloarthritis (SpA). The relationship between disease-related factors structural damage and subclinical atherosclerosis is still unknown.

OBJECTIVE:

The aim of our study was to evaluate the association of subclinical atherosclerosis with radiographic structural damage in patients with SpA.

METHODS:

Forty-seven SpA patients who fulfilled the ASAS criteria were enrolled in a case-control study conducted over 12 months and compared with 47 age and sex-matched healthy controls. None of the subjects had a previous history of cardiovascular diseases or cardiovascular risk factors. Demographic and disease characteristics were recorded. Structural lesions were evaluated using plain radiography, and two scoring tools were used to spine (BASRI and mSASSS). Subclinical atherosclerosis was assessed using ultrasound measurements of flow-mediated dilation (FMD) and carotid intima-media thickness (cIMT).

RESULTS:

The median age of patients was 36 years. The sex ratio was 2.35. The median BASRI total score was 3 (IQR 2–4), median mSASSS score was 10 (IQR 415). cIMT was significantly increased in SpA patients compared to controls ( $p<$ 0.0001), and FMD was significantly lower in patients than in healthy subjects ( $p=$ 0.008). cIMT was significantly associated with ankylosis of the facet joints ( $p=$ 0.035) and Romanus spondylitis ( $p=$ 005). FMD was negatively associated with vertebral squaring ( $p=$ 0049), bridging syndesmophytes ( $p=$ 0031) and mSASSS score ( $p=$ 0.047).

CONCLUSION:

Our result supports the association of radiographic structural damage and subclinical atherosclerosis assessed using cIMT and FMD. This finding highlights the importance of earlier treatment in order to prevent radiographic damage progression and atherosclerotic events.

Keywords

Spondyloarthritis atherosclerosis carotid intima-media thickness radiography

1. Introduction

Spondyloarthritis (SpA) is an inflammatory rheu-matic disease characterized by enthesitis involving the spine, sacroiliac, and peripheral joints. According to the predominant manifestations, SpA can be classified as axial SpA (axSpA) or peripheral SpA [1, 2]. Compelling evidence during the last decades suggests that patients with SpA carry an increased risk for cardiovascular (CV) disease and CV death compared to the general population [3, 4, 5]. This risk appears to be mediated by systemic inflammation over and above classical CV risk factors, suggesting that different mechanisms are implicated in the genesis and acceleration of the atherosclerotic process [6]. The structural evolution of SpA is defined by the formation of syndesmophytes, which corresponds to a healing process leading to new bone formation at entheses sites after an initial inflammatory phase [7]. Radiographic progression in SpA patients is variable, and has been described in early, as well as in very advanced older patients. Therefore, considering the key role that the marked inflammation on magnetic resonance imaging (MRI) plays in the radiographic progression in axSpA and the development of syndesmophytes, it may be hypothesized that radiographic structural damage may increase estimated CV risk in SpA.

To better stratify the CV risk in these patients, it would be better to establish a patient SpA profile with high CV risk. The associations of disease-related factors, mainly radiographic structural damage, with accelerated subclinical atherosclerosis are still unknown. Given the relative lack of data on the contribution of structural damage to the increased CV burden and subclinical atherosclerosis in SpA patients, we conducted this study whose main objective was to assess the association between subclinical atherosclerosis with radiographic structural damage in SpA patients.

2. Methods

2.1 Study design and population

We have conducted a case-control study over 12 months from September 2020 to September 2021. Patients diagnosed with SpA according to the Assessment in SpondyloArthritis international Society (ASAS) criteria were included [1, 2]. Healthy volunteers matched for age and sex represented the control group. Non-inclusion criteria for patients and controls were: age $>$ 50 years, history of CV disease, CV risk factor among the following (hypertension, diabetes mellitus, dyslipidemia, chronic renal failure, smoking, hyperuricemia, gout, obesity). Patients suffering from SpA associated with psoriasis, inflammatory bowel diseases, juvenile SpA, or reactive arthritis were also not included. The local ethics committee of the University Charles Nicolle Hospital approved the study (CHRH04/2022) and each participant provided informed consent.

2.2 Data collection

Demographic factors (patients’ age and sex) were recorded. Anthropometric measurements (weight, height, waist circumference, hip circumference, body mass index [BMI]) were obtained by a trained examiner. Waist circumference was measured midway between the lowest rib margin and the iliac crest after normal exhalation. Hip circumference was measured at the site of the largest convexity of the buttocks below the hip plates. The following disease characteristics were listed: age at onset of SpA, disease duration, type of SpA, BASMI, BASFI, and disease activity scores: Bath AS Disease Activity Index (BASDAI) and AS Disease Activity Score (ASDAS). At the time of study enrollment, biochemical parameters (lipid profile, fasting blood glucose, C-reactive protein [CRP]) were measured, and therapeutic data were detailed.

Radiographic data comprised conventional plain X-ray images of the cervical spine, thoracic spine, and lumbar spine. Pelvic radiography with an anterior-posterior view of the sacroiliac joints was performed. Conventional radiography interpretation was performed by a trained rheumatologist and a radiologist. Right and left sacroiliitis were recorded according to the modified New York criteria [8]. Structural lesions recorded in the spinal conventional radiography were: vertebral corner erosions or Romanus spondylitis, vertebral squaring, sclerosis and erosions of the vertebral endplate, disk calcifications, syndesmophytes, bony bridging, and ankylosis of facet joints. The modified Stoke AS Spine Score (mSASSS) and the Bath AS Radiological Index (BASRI) were the two spine radiography scoring methods used to assess the spine [9, 10].

2.3 Ultrasound measurements

Carotid intima media thickness (cIMT) measurement and flow-mediated dilation (FMD) are two tools for the assessment of atherosclerosis at two different stages: endothelial dysfunction and arterial wall infiltration [11].

2.3.1 Carotid intima-media thickness

Common carotid arteries (CCA) were assessed using continuous-wave Doppler and color flow B-mode Doppler ultrasound (US) using a high-resolution 11 MHz linear probe (MindrayResona 7 ZST $+$ ). A longitudinal image of the distal CCA, 2 cm upstream from the bifurcation was acquired during diastole, with subjects lying in the supine position and the head turned 45 ${}^{\circ}$ to the opposite side of the CCA examined. cIMT was measured on the posterior far wall of the CCA from the media-adventitia interface to the intima-lumen interface using a specifically designed automatic software program. Three measurements were obtained for the far wall of both the right and left CCA. These measurements were then averaged. Finally, the mean cIMT values from both sides (right and left CCA) were again averaged, and a single value was selected as the cIMT value. Carotid plaque was defined as cIMT $>$ 1.5 mm and increased cIMT corresponded to cIMT $>$ 0.7 mm [12].

2.3.2 Flow-mediated dilation

Subject preparation recommendations before FMD were fulfilled [13]. Longitudinal images of the right brachial artery were taken using high-resolution B-mode US (the same US probe of 11 MHz). The occlusion cuff was placed around the forearm, distal to the US probe. Brachial artery diameter was continuously measured. After a 1-minute baseline diameter recording, a cuff pressure was inflated $>$ 50 mmHg above systolic blood pressure for 5 minutes. After deflation, hyperemia occurred. The percent peak dilatation related to the baseline diameter was calculated as % $\Delta$ FMD $=$ (Peak diameter $-$ Baseline diameter/Baseline diameter) $\times$ 100.

Where peak diameter is the diameter of the largest brachial artery after deflation; and baseline diameter is the diameter of the pre-occlusion brachial artery.

Intra and inter-observer reproducibility of the two US measurements (IMT, FMD) was assessed. For cIMT, there was excellent interobserver ( $k=$ 0.824; $p=$ 0.015) and intra-observer ( $k=$ 0.851; $p=$ 0.011) agreement. FMD obtained good interobserver ( $k=$ 0.696; $p=$ 0.048) and good intraobserver ( $k=$ 0.752; $p=$ 0.038) agreement.

2.4 Statistical analysis

The sample size was calculated: $n=(Z_{\alpha})^{2}\times\delta^{2}/i^{2}$ ( $Z=$ normal distribution of the corresponding alpha value; $Z_{\alpha}=$ 1.96 for 95% confidence level; $i=$ type 1 error of 0.05; $\delta=$ standard deviation). The minimum sample size was 31 patients.

The results were presented as medians and interquartile ranges between the 25 ${}^{\text{th}}$ and 75 ${}^{\text{th}}$ percentiles (IQR 25–75). Comparisons between two groups were made using the Mann-Whitney test (quantitative data), and the Pearson’s chi-square test (qualitative data). Comparisons between more than three quantitative data were performed using the Kruskal-Wallis test. The significance of association was determined using the Cramer’s Phi and V test. $P$ values less than 0.05 were considered significant.

3. Results

3.1 Demographic and clinical data

The study included 47 SpA patients and 47 healthy controls, without gender difference (sex ratio was 2.35 in two groups, $p=$ 0.589). The median age of SpA patients was 36 (28–46) years versus 32 (26–43) years in control subjects ( $p=$ 0.267). SpA patients have a significantly lower weight 69 kg (56–80) versus 80 kg (65–83) ( $p=$ 0.021), and higher waist circumference 88 cm (82–97) versus 79 cm (72–88) ( $p<$ 0.0001). There was no difference between patients and controls in terms of median height ( $p=$ 0.054), median hip circumference ( $p=$ 0.396), and median BMI ( $p=$ 0.238).

Table 1 shows the main disease features of the SpA patients. The median age at onset of SpA was 20 years (18–32), median disease duration was 11 years (5–16). Regarding the distribution of SpA patterns, 25 patients (53%) presented r-ax SpA, 2 (4%) nr-ax SpA, 19 (41%) peripheral involvement and 1 (2%) mixed forms. Median BASDAI score was 2.6 (1.8–3.8), while median ASDAS-CRP was 2.18 (1.62–2.91). Median CRP level was 6.45 mg/l (1.5–19.9). At the study visit, 91% of patients were receiving non-steroidal anti-inflammatory drugs (NSAIDs), 51% were treated using Conventional synthetic disease modifying antirheumatic drugs [csDMARDS] (47% sulfasalazine, 4% methotrexate), and 38% were on tumor necrosis factor inhibitors (TNFi). The median duration of TNFi treatment was 36 months (24–72).

Table 1
Characteristics of the SpA population ( $n=$ 47)

	Median (IQR 25–75%)
Age (years)	36 (28–46)
BMI (kg/m ${}^{2}$ )	24.5 (20.7–26.87)
Age at onset of SpA (years)	20 (18–32)
Disease duration (years)	11 (5–16)
BASDAI	2.6 (1.8–3.8)
ASDAS-CRP	2.18 (1.62–2.9)
BASFI	3 (1.5–5.1)
BASMI	1.5 (0–4)
Spinal mobility measures
Occiput-wall distance (cm)	3 (2–5)
Chin-sternum distance (cm)	0 (0–2)
Right tragus acromion distance (cm)	10 (9–14)
Left tragus acromion distance (cm)	11 (9–14)
Right chin-acromion distance (cm)	10 (9–14)
Left chin-acromion distance (cm)	10 (9–15)
C7 to wall distance (cm)	4 (3–6)
Finger to floor distance (cm)	25 (0–70)
Chest expansion (cm)	4 (3–5)
Schober test (cm)	3 (2–5)
Biochemical parameters
Fasting blood sugar (mmo/l)	4.9 (4.55–5.1)
Total Cholesterol	3.66 (3.18–4.28)
Triglycerides	0.84 (0.79–1.15)
C-LDL	2.17 (0.93–3.9)
C-HDL	1.08 (0.63–1.49)
CRP (mg/l)	6.45 (1.5–19.9)
Total BASRI	3 (2–4)
mSASSS	10 (4–15)
cIMT (mm)	0.55 (0.48–0.62)
FMD (%)	14.6 (9–24)

ASDAS-CRP: Ankylosing Spondylitis Disease Activity Score C Reactive Protein; BASDAI: Bath Ankylosing Spondylitis Disease Activity index; BASFI: Bath Ankylosing Spondylitis Functional Index; BASMI: Bath Ankylosing Spondylitis metrology index; BASRI: Bath Ankylosing Spondylitis Radiologic Index; BMI: Body mass index; CRP: C Reactive Protein; FMD: Flow-mediated dilation; cIMT: carotid Intima media thickness; IQR: Interquartile range,mm:millimeter; mSASSS: modified Stoke Ankylosing Spondylitis Spine Score; SpA: spondyloarthritis; cm: centimeter.

3.2 Imaging data

Radiographic structural lesions of the spine were distributed as follows: Romanus spondylitis ( $n=$ 6), vertebral squaring ( $n=$ 39), syndesmophytes ( $n=$ 21), bony bridging ( $n=$ 7), dagger spine ( $n=$ 3) and ankylosis of facet joints ( $n=$ 16) (Fig. 1). Median BASRI total score was 3 (2–4), while median mSASSS score was 10 (4–15). Radiographic sacroiliitis was seen in 96% of patients; this was bilateral in 91% of cases. Distribution of sacroiliitis was for the right side: stage 1 ( $n=$ 1), stage 2 ( $n=$ 8), stage 3 ( $n=$ 24), stage 4 ( $n=$ 10); and for left sacroiliitis: stage 1 ( $n=$ 2), stage 2 ( $n=$ 7), stage 3 ( $n=$ 24), stage 4 ( $n=$ 10).

Figure 1.

Legend: Distribution of spinal radiographic lesions in our patients.

As regards ultrasound assessment, cIMT was significantly increased in SpA patients than controls (0.55 mm [0.48–0.62] versus 0.46 mm [0.43–0.5]; $p<$ 0.0001). FMD was significantly lower in SpA patients versus healthy subjects (14.6% (9–24) versus 18.2% (12.8–23.1); $p=$ 0.008).

3.3 Association between cIMT, FMD, and structural damage

cIMT was significantly increased in SpA patients with Romanus spondylitis ( $p=$ 0.05) and ankylosis of the facet joints ( $p=$ 0.035), while FMD was significantly decreased in patients presenting vertebral squaring ( $p=$ 0.049) and bridging syndesmophytes ( $p=$ 0.031) (Table 2). There was no significant correlation between US measurements and sacroiliitis. There was no significant difference between the stages of sacroiliitis on the right side, as well as on the left side (Table 3).

Table 2
Association between cIMT, FMD and spinal radiographic lesions

		cIMT				FM
		Median	P2	P7	$p$	Median	P2	P7	$p$
Romanus spondylitis	No	0.54	0.48	0.59	0.05	15.00	10.00	24.00	0.138
	Yes	0.65	0.60	0.70		11.90	7.80	13.90
Vertebral squaring	No	0.54	0.48	0.58	0.6	17.80	15.30	24.50	0.049
	Yes	0.55	0.48	0.64		13.80	8.00	21.00
Syndesmophytes	No	0.53	0.47	0.59	0.202	16.00	10.00	24.00	0.116
	Yes	0.57	0.50	0.64		13.80	6.12	18.00
Bridging syndesomphytes	No	0.54	0.48	0.59	0.138	15.45	10.00	24.00	0.031
	Yes	0.60	0.52	0.70		7.80	5.00	13.90
Dagger spine	No	0.55	0.49	0.61	0.727	14.80	10.00	24.00	0.061
	Yes	0.52	0.45	0.64		6.00	5.00	12.50
Ankylosis of the facet joints	No	0.52	0.47	0.59	0.035	14.60	10.00	24.00	0.500
	Yes	0.57	0.53	0.69		13.95	7.25	19.50

cIMT: carotid Intima media thickness; FMD: Flow mediated dilation; $p$ : Significance coefficient; P25: Percentile 25; P75: Percentile 75.

Table 3

Comparison of IMT and FMD in patients according to sacroiliitis

		IMT				FMD
		Median	P25	P75	$p$	Median	P25	P75	$p$
Sacroiliitis	No	0.55	0.45	0.64	0.874	17.70	11.40	24.00	0.673
	Yes	0.55	0.49	0.60		14.60	9.00	21.00
Right sacroiliitis	Grade I	0.55	0.55	0.55	0.420	26.00	26.00	26.00	0.301
	Grade II	0.49	0.45	0.55		10.50	7.30	24.00
	Grade III	0.57	0.52	0.63		14.80	9.50	18.65
	Grade IV	0.53	0.50	0.64		13.90	6.00	16.00
Left sacroiliitis	Grade I	0.54	0.52	0.55	0.595	21.75	17.50	26.00	0.260
	Grade II	0.49	0.44	0.58		10.00	6.60	24.00
	Grade III	0.57	0.51	0.63		14.60	9.50	18.65
	Grade IV	0.53	0.47	0.64		13.90	6.00	16.00

IMT: Intima media thickness; FMD: Flow mediated dilation; $p$ : Significance coefficient; P25: Percentile 25; P75: Percentile 75.

FMD was negatively correlated to mSASSS ( $p=$ 0.047; $r=-$ 0.298). We did not find any significant correlation between cIMT and mSASSS ( $p=$ 0.126; $r=$ 0.232). On the other hand, BASRI total score showed no significant correlation with cIMT ( $p=$ 0.305; $r=$ 0.156) and FMD ( $p=$ 0.197; $r=-$ 0.196).

Table 4

Association of structural spinal damage in SpA and ultrasound markers of atherosclerosis in the literature

Study	Radiographic lesion	Ultrasound measure	$p$
Ladehesa-Pineda et al. [14]	• mSASSS • Syndesmophytes • Bridging syndesmophytes	cIMT	$<$ 0.0001. $<$ 0.001. $<$ 0.0001.
Giollo et al. [15]	Syndesmophytes	cIMT	0.01
Gonzalez-Juanatey et al. [16]	• Romanus spondylitis • Zygapophyseal Joint ankylosis • Syndesmophytes	cIMT	0.05 NS
Hamdi et al. [17]	• mSASSS • BASRI	cIMT	0.035 0.699
Mathieu et al. [18]	• mSASSS	cIMT	NS

cIMT: carotid intima media thickness; $p$ : Significance coefficient; mSASSS: modified Stoke Ankylosing Spondylitis Spine Score; NS: not significant.

4. Discussion

The present study supports the hypothesis that structural damage is an important piece of the puzzle in the increased CV burden in SpA patients. In this study, we confirmed the increased CV risk in SpA patients compared to the general population. We also found that structural damage was significantly associated with markers of subclinical atherosclerosis. Previous researchers have demonstrated that radiographic progression was closely associated with increased cIMT (Table 4) [14, 15, 16, 17, 18]. As shown in Table 4, available literature to date shows that structural damage in SpA was significantly associated with estimated CV risk in SpA measured using the same US parameter (cIMT). To our knowledge, this is the first study to find a correlation between radiographic progression and endothelial dysfunction. FMD was significantly lower in our SpA patients having vertebral squaring and bone bridges; and negatively correlated with total mSASSS score.

The structural lesions reported to be associated with a significant increase in atherosclerotic plaques in SpA patients compared to healthy controls and cIMT progression were syndesmophytes [14, 15, 19] and bone bridges [14]. In our patients, cIMT was significantly increased, with the presence of erosive Romanus spondylitis and ankylosis of the facet joints. However, a recent large population-based study reported that the atherosclerosis burden was similar in non-radiographic axSpA and AS [20]. Gonzalez-Juanatey et al. did not find a significant association between syndesmophytosis and disease [16].

In line with literature data, we did not find any significant associations between US parameters and total BASRI score (Table 4). The BASRI score appears to be less sensitive to radiographic progression than the mSASSS score. In fact, the mSASSS is considered the most sensitive and valid spine radiography scoring method in axSpA, including in the early phases of the disease [21]. mSASSS was independently associated with higher SCORE levels, predicting a 10-year risk of fatal CV disease in axSpA patients [14], the Framingham risk score, the predictive factor of the 10-year coronary heart disease (CHD) risk [19], and increased cIMT [17].

In our study, no correlation was found between sacroiliitis and US measurements. Only one study conducted by Kang et al. showed a significant correlation between the Framingham risk score and the grade of sacroiliitis on X-ray [19].

The impact of structural damage on the progression of cIMT and endothelial dysfunction remains unknown. Confounding factors that affect the relationship between radiographic progression in SpA and accelerated subclinical atherosclerosis include age, male sex, smoking, and chronic inflammation [22]. Smoking, a traditional CV risk, is now well recognized as being associated with early disease onset, high disease activity and increased axial structural damage on X-ray [23].

To note, the positive association between structural damage and subclinical atherosclerosis was independent of smoking, since this was a non-inclusion criterion. Another common factor: adipokines produced by the adipose tissue and a known mediator of the immune system and the inflammatory response. Adipokines are involved in cardiometabolic complications in patients with rheumatic diseases [19, 24]. Visfatin and omentin were also correlated with an enhanced CV risk in SpA [25, 26]. In parallel, the adipokines level was associated with spinal progression [27, 28, 29, 30]. A recent study highlights the fact that changes in adipokine (visfatin and leptin) levels in the first 2 years showed significant association with new syndesmophyte formation and mSASSS progression after 4 years in SpA [31]. Thus, adipokines with special emphasis on the more widely studied molecules (leptin, visfatin) contribute dually to the radiographic progression and increased CV risk.

Chronic subclinical inflammation is a key process in the initiation and progression of atherosclerotic CV disease. Immune cells, pro-inflammatory molecules such as interleukins (IL-1 $\beta$ , IL-6), TNF- $\alpha$ , and circulating microparticles, contribute to the inflammatory mechanism in atherosclerosis [32, 33]. Therefore, modulation of inflammation by adding anti-inflammatory agents, such as IL-1 inhibitor (canakinumab) and tocilizumab to conventional CV treatment has becomes a subject of current debates in atherosclerotic CV disease management [34]. Over the past decades, the therapeutic objective in the prevention and treatment of atherosclerosis has focused on the role of lipid-lowering medications, given the lipid deposition in the arterial wall and role in the pathological process of atherosclerosis and plaque formation [33]. The synergistic effect of IL-17 and TNF are linked to radiographic progression in axSpA, with a potentially strong determinant role of IL-17 in bone remodeling [7].

Spinal radiographic progression reflects rather the effects of long-term and cumulative inflammation [35, 36]. Syndesmophytes arise at sites with present active inflammation, as well as at sites without detectable inflammation using conventional imaging methods; this is underlined by histological studies showing inflammation at sites without signs of inflammation in MRI [37]. The most important factor predictive of radiographic progression is the pre-existence of radiographic changes before initiation of treatment, indicating a higher potential for protective effect in early, than in later, stages of the disease [38, 39]. Our study supports this fact, as we did not find any correlation between activity scores and US measurements in our patients. Inflammatory parameters (BASDAI, ASDAS, CRP) do not appear to be the determinant factor of subclinical atherosclerosis in the literature, since they indicated acute inflammatory status at the time of assessment [40, 41].

Published data support the evidence that TNFi is effective in preventing or even reversing the progression of cIMT in SpA patients responding to treatment [6]. However, the disease-modifying effect of TNFi on spinal radiographic progression (inhibition or slowing syndesmophyte formation and progression) remains controversial [7]. On the other hand, the experience with IL-17 inhibitors (IL-17i) in axSpA is shorter compared to the use of TNFi, which precludes any conclusion on radiographic progression, and there are no specific study that examines CV risk [6].

Among the limitations of this study, the analysis of the association between structural damage and subclinical atherosclerosis markers did not take into account two confounding factors: NSAID intake and disease duration. However, the strength of our study consists in study selection criteria (patients without history of traditional CV risk factors).

The association between structural damage and subclinical atherosclerosis could be due to their connection with the chronic inflammatory burden of the disease or possibly due to an indirect relationship through dysregulation of these confounding factors (age, adipokines). Once again, strict control of inflammation and slowing radiographic progression would be the best way to minimize the high CV risk in SpA.

5. Conclusion

SpA patients present accelerated subclinical atherosclerosis compared to healthy controls. Radiographic progression is correlated to higher CV risk in this population. To our knowledge, this is the first study to establish a correlation between FMD and spinal structural damage. We therefore believe that SpA patients with initial radiographic lesions will benefit from screening for atherosclerosis at an early and pre-clinical stage using non-invasive techniques such as cIMT and FMD. This monitoring should be done at diagnosis, and then routinely. Deeper knowledge about the association between structural damage and increased CV risk in SpA patients is needed to identify patients at higher CV risk. Management of these patients should focus on suppressing inflammation to prevent radiographic progression and atherosclerosis.

Key message:

•

Radiographic progression is associated withhigher cardiovascular risk in SpA populations.

•

cIMT and FMD are useful tools for screening higher CV risk in SPA patients.

Funding

No specific funding was received from any bodies in the public, commercial or not-for-profit sectors to carry out the work described in this article.

Ethics statement

The Charles Nicolle Hospital local committee approved the research protocol. The study was carried out according to the principles of the Declaration of Helsinki. Informed consent was provided by all participants.

Availability of data and materials

The data and supporting information are included in the article.

Footnotes

Acknowledgments

None to report.

Conflict of interest

The authors declare no conflicts of interest.

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Spinal radiographic progression is correlated with preclinical atherosclerosis in spondyloarthritis

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2. Methods

2.1 Study design and population

2.2 Data collection

2.3 Ultrasound measurements

2.3.1 Carotid intima-media thickness

2.3.2 Flow-mediated dilation

2.4 Statistical analysis

3. Results

3.1 Demographic and clinical data

Table 1 Characteristics of the SpA population ( n = 47)

Table 2 Association between cIMT, FMD and spinal radiographic lesions

5. Conclusion

Funding

Ethics statement

Availability of data and materials

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Characteristics of the SpA population ( $n=$ 47)

Table 2
Association between cIMT, FMD and spinal radiographic lesions