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Egyptian Journal of Radiology and Nuclear Medicine
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Ankylosing spondylitis impact on knee cartilage thickness: correlation with demographic data and clinical characteristics

Egyptian Journal of Radiology and Nuclear Medicine volume 54, Article number: 196 (2023) Cite this article

Abstract

Background

Ankylosing spondylitis (AS) is a progressive inflammatory disease involving cartilaginous structures in the spine and peripheral joints. However, the number of the studies assessing knee cartilage thickness in AS and its correlations with parameters of disease activity/severity is even less. We aimed to assess the impact of AS on knee cartilage thickness using musculoskeletal ultrasound (MSUS) and magnetic resonance imaging (MRI).

Methods

Twenty-five AS patients and 25 healthy individuals (15 served for MSUS assessment, and 10 served for MRI assessment) were included. By employing MRI “using a 1.5-T machine” and MSUS “with a 10–18-MHz linear probe,” respectively, the thickness of the femorotibial cartilage and femoral cartilage was assessed.

Results

Compared to healthy controls, AS patients showed statistically significantly thinner cartilage thickness (P < 0.05) at all femorotibial cartilage subdivisions and the medial femoral condyle and intercondylar area on both sides. Femoral cartilage thickness measurements either assessed by MSUS or MRI were negatively correlated with age, measures of disease activity, and Bath Ankylosing Spondylitis Radiology Index for the spine (BASRI-s) (P < 0.05). However, MRI tibial cartilage thickness was negatively correlated with disease duration and measures of spinal mobility, functional limitation, and BASRI-s (P < 0.05). MRI total cartilage thickness measurements at the femoral condyle were negatively correlated with Bath Ankylosing Spondylitis Functional Index (BASFI) and Ankylosing Spondylitis Disease Activity Score-erythrocyte sedimentation rate (ASDAS ESR) (P = 0.04 and P = 0.03, respectively). A positive correlation was found between MSUS and MRI total femoral cartilage thickness (P = 0.02).

Conclusions

The knee cartilage thickness of AS patients was thinner than that of healthy controls. The correlations between cartilage thickness and patient variables demonstrate MSUS and MRI's utility in identifying knee cartilage loss areas in AS patients.

Background

Ankylosing spondylitis (AS) is a persistent, inflammatory condition that influences the axial skeleton over time [1]. Sacroiliitis, enthesitis, and peripheral arthritis are their defining features [2]. AS involved the cartilaginous structures in the spine and peripheral joints [3]. According to a recent study, the immune system's primary target in spondyloarthropathy may be cartilage [4]. Various approaches have been used to directly measure the thickness of articular cartilage in cadavers; however, these techniques are intrusive and do not allow measurements to be taken in vivo [5, 6].

To be fair, magnetic resonance imaging (MRI) is thought to be the most efficient non-invasive technique for evaluating cartilage. However, there are a number of technological and financial restrictions to using MRI regularly to evaluate cartilage [7].

Musculoskeletal ultrasound (MSUS) is a cheap, non-invasive, secure, and convenient technique [8]. It has been shown to be a reliable method for determining the thickness of the distal femoral cartilage, and tests of the femoral cartilage using ultrasound are known to be highly correlated with histological grading [9, 10].

As far as we are aware, this is the first study measuring knee cartilage thicknesses in patients with AS by MRI and determining correlations with US measurements and different disease parameters.

Methods

Study plan and population

Over the course of 7 months, our analytical cross-sectional study was carried out and included 25 patients [17 males and eight females], who fulfilled the modified 1984 New York criteria for ankylosing spondylitis [11] (mean age 28.4 ± 9.4 years; range 20–37 years). All patients were attending Rheumatology and Rehabilitation Outpatient Clinics. Fifteen healthy individuals (who were healthcare workers at the Main Hospital) were served for MSUS assessment of femoral cartilage thickness, and another 10 healthcare workers at the Obstetrics and Gynecology Hospital were served for MRI assessment "as the MSUS and MRI were not in the same hospital." All controls matched for age and body mass index (BMI). All study participants provided their informed permission. The ethics committee of the Faculty of Medicine gave the study their approval.

Patients who had recently undergone joint or soft tissue surgery, those who had received corticosteroid injections into the knee, those who had congenital or traumatic knee problems, and those who had severe neurological, cardiac, pulmonary, renal, or malignant diseases were all excluded from the study.

Clinical and functional assessment

Bath Ankylosing Spondylitis Disease Activity Index (BASDAI) [12] and Ankylosing Spondylitis Disease Activity Score (ASDAS CRP and ASDAS ESR) were used to assess disease activity [13, 14]. The Bath Ankylosing Spondylitis Metrology Index (BASMI) 3-point answer scale [15] and the Bath Ankylosing Spondylitis Functional Index (BASFI) [16] were used to measure the degree of spinal mobility and functional restriction.

Conventional X-rays radiologic scoring methods

All patients had to undergo a recent X-ray procedure that consisted of taking an anteroposterior and lateral views of the spine and an anteroposterior view of the pelvis. Bath Ankylosing Spondylitis Radiology Index for the spine (BASRI-s) [17] was used to analyze the conventional X-ray findings in all patients.

Musculoskeletal ultrasonographic cartilage measurements

All femoral cartilage evaluations were performed by the same physician who was experienced in the musculoskeletal US (EULAR Certified Trainer MSUS) using a linear array probe (10–18 MHz, Siemens Acuson P300, Germany). When the individuals were comfortably seated on the examination table with their knees in maximum flexion, a physician assessed the thickness of the femoral articular cartilage [9, 18]. Each knee's right lateral condyle (RLC), right intercondylar region (RIA), right medial condyle (RMC), left medial condyle (LMC), left intercondylar area (LIA), and left lateral condyle were measured at the midpoint (LLC). The distance between the thin hyperechoic line at the synovial space/cartilage interface and the sharp hyperechoic line at the cartilage bone interface was used to determine the cartilage thickness [19]. The lateral femoral condyle, medial femoral condyle, and intercondylar area were added together, and the means were calculated, to determine the total femoral cartilage thickness.

MRI examination

The physician assessing the MRI scans was unaware of the US data. Both knees of the patients were first scanned by the US, and then, they were taken for MRI. All patients were examined by MRI using a 1.5-T MR machine (Achieva, Philips medical system, the Netherlands). All patients were imaged using the following protocol in sagittal and coronal STIR (TR: 4080 ms; TE: 30 ms; and slice thickness 4 mm), sagittal PD (TR: 2000 ms; TE: 17 ms; and 4-mm slice thickness), axial and sagittal T2 (TR: 3500 ms; TE: 90 ms; and 4-mm slice thickness). Segmentation was done for the cartilage as follows; (1) distal femoral cartilage and (2) tibial cartilage. The segmented cartilage area is then subdivided into medial and lateral compartments. Three functional regions were defined: the anterior region, the middle region, and the posterior region. The overall maximal medial and lateral cartilage width for each condyle included the central and thickest regions of each condyle, and excluded boundary regions were used to calculate the average cartilage thicknesses [20].

Statistical analysis

The data were analyzed with SPSS 21.0. Additionally, to descriptive statistics by number and percent, there were mean and SD calculations. Comparing qualitative variables was done using the Chi-square (χ2) [2] test. The difference between the means of the two groups for interval and ordinal variables was compared using the T-test or Mann–Whitney U-test. There were calculated Pearson correlation coefficients (r). P < 0.05 was used to define the statistical significance level.

Results

Fifty knees from 25 AS patients and 50 knees from 25 healthy people were measured using MRI and US (30 knees were used to test the thickness of the femoral cartilage using the US, and 20 knees were used for MRI).

Clinical characteristics of AS patients

The mean age values of AS patients were 28.4 ± 4.9 years, BMI values were 29.2 ± 2.7 kg/m2, and mean disease duration was 4.7 ± 2.7 years. Knee pain was found in 17 (68%) patients. The mean visual analog scale for pain (VAS) was 13.6 ± 20.9, the mean ASDAS ESR was 2.59 ± 1.04, the mean ASDAS CRP was 2.48 ± 0.74, the BASDI was 4.21 ± 1.27, the mean BASFI was 6.04 ± 1.88, mean BASMI was 3.84 ± 1.55, and mean BASRI was 5.00 ± 1.09. AS patients were currently under nonsteroidal anti-inflammatory drugs (N = 24), sulfasalazine (N = 21), and methotrexate (N = 2) treatment, but none of them used tumor necrosis factor inhibitors.

MRI measurements

Fifty knees of 25 AS patients and 20 knees of the 10 healthy individuals (six males and four females) were examined. The mean age values of healthy individuals were 28.2 ± 3.5 years, and BMI values were 28.8 ± 2.9 kg/m2 (P > 0.05 in comparison with AS patients). Tables 1 and 2 show MRI cartilage thickness values at the subdivisions of femoral and tibial condyles, respectively, for patients and controls. The average cartilage thicknesses for medial and lateral cartilage of femoral and tibials condyle and the total femorotibial cartilage thicknesses were calculated for patients and controls as shown in Table 3. At all measurement sites, AS patients' femoral cartilage was thinner than that of the healthy controls, with statistically significant differences (P < 0.05).

Table 1 Comparison of MRI cartilage thickness measurements at subdivision of femoral condyle in AS patients and controls
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Table 2 Comparison of MRI cartilage thickness measurements at subdivision of tibial condyle in AS patients and controls
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Table 3 Comparison of MRI femorotibial cartilage thickness measurements in AS patients and controls
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MRI images of cartilage thickness measurements at femoral and tibial condyles in AS patients are shown in Figs. 1 and 2.

Fig. 1
figure 1

Sagittal STIR images of male patient aged 30 years show reduced cartilage thickness of the anterior region of the medial compartment of femoral and tibial condyles (a) and middle region of the lateral compartment of femoral condyle (b)

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Fig. 2
figure 2

Sagittal STIR images of male patient aged 34 years show marked reduction in the cartilage thickness of both medial and lateral compartments of femoral (a) and tibial condyles (b)

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MSUS measurements

Fifty knees of 25 AS patients and 30 knees of the 15 healthy individuals (eight males and seven females) were examined. The mean age values of healthy individuals were 26.9 ± 4.7, and BMI values were 29.8 ± 2.6 kg/m2 (P > 0.05 in comparison with AS patients). Table 4 shows the femoral cartilage thickness values for patients and controls. At all measurement sites, femoral cartilage in AS patients was thinner than that in healthy controls; statistically significant differences were found at the medial femoral condyle and intercondylar area in both the right and left knees (P < 0.05). Figure 3 displays musculoskeletal ultrasonographic images of measurements of femoral cartilage thickness in an AS patient.

Table 4 Comparison of musculoskeletal ultrasonographic femoral cartilage thickness measurements in AS patients and controls
Full size table
Fig. 3
figure 3

B-mode ultrasound transverse scan of the anterior knee joint in male patient aged 29 years showing thickness of femoral cartilage at a lateral condyle = 2.4 mm, b intercondylar area = 3.4 mm, and c medial condyle = 1.8 mm

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Correlation between MRI measurements of femoral/tibial cartilage thickness and demographic information and clinical characteristics

Correlations of MRI measurements at subdivisions of femoral and tibial condyles with demographic data and clinical characteristics are shown in Table 5. MRI total cartilage thickness measurements at the femoral condyle were negatively correlated with BASFI and ASDAS ESR (r = − 0.40, P = 0.04 and r = − 0.37, P = 0.03 respectively), but the total MRI cartilage thickness measurements at the tibial condyle and the total femorotibial cartilage thickness were not correlated with any of demographic data or clinical characteristics. Taking into consideration, that there was a very strong positive correlation between the femoral and the tibial cartilage thickness (r = 0.9, P < 0.001).

Table 5 Correlations of MRI cartilage thickness measurements at subdivision of femoral and tibial condyles with demographic data and clinical characteristics
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Correlation of MSUS femoral cartilage thickness values with demographic data and clinical characteristics

Ultrasonographic femoral cartilage thickness at LIA, LLC, and RMC was negatively correlated with age, BASRI, and ASDAS ESR, respectively (r = − 0.37, P = 0.04; r = -0.31, P = 0.04; and r = − 0.38, P = 0.02, respectively). Disease duration or BMI had no correlation with cartilage thickness for all regions.

Correlation between MSUS and MRI total femoral cartilage thickness

Musculoskeletal ultrasonographic total femoral cartilage thickness had a positive correlation with MRI total femoral cartilage thickness (r = 0.49, P = 0.02) as shown in Fig. 4. No other correlation could be detected between the US and MRI knee cartilage thickness in other regions.

Fig. 4
figure 4

Correlation between MRI and MSUS total femoral cartilage thickness in AS patients

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Discussion

Knees, hips, or other joints are involved in 25%–70% of AS patients [21]. In comparison with the other joints, the knee joint has separate cartilage compartments that are easily identified on MRI [22] and US [10].

Our results showed that AS patients had thinner knee cartilage thickness measurements than the healthy controls with statistically significant differences.

The structural damage in AS was predicted using a variety of biomarkers. The various types of biomarkers include genetic markers, markers of inflammation, markers of cartilage and bone turnover, and others. Radiographic damage and AS progression both heavily depend on cartilage degradation [23,24,25]. A study by Kim et al. [3] found elevated C-propeptide of type II collagen (CPII), 846 epitopes, and CPII:C2C ratio in AS patients compared to controls. In individuals with AS, anti-tumor necrosis factor (anti-TNF) medications may affect cartilage metabolism by reducing type II collagen breakdown and boosting aggrecan turnover [26].

For evaluating the size of the knee cartilage in vivo, reliable imaging methods include magnetic resonance imaging and ultrasonography [10, 27]. Most earlier research has looked at the peak and mean cartilage thickness of the entire surface to quantify the cartilage thickness distribution. Other studies have separated the femur's two condyles and trochlea into distinct sections [28,29,30].

Most of our patients have moderate to high activity (according to ASDAS), and 68% of them have knee pain. When compared to healthy controls, AS patients had bilaterally statistically significant (P < 0.05) thinner knee cartilage thickness at all subdivisions of the femoral and tibial condyles. Moreover, total femoral, total tibial, and total femorotibial cartilage thicknesses were significantly reduced (P < 0.05).

The present study reported the correlation of MRI knee cartilage thickness values with patients’ characteristics. Femoral cartilage thickness was negatively correlated with age which was in agreement with Roberts et al. [31]. Moreover, femoral cartilage thickness was negatively correlated with the measure of spinal mobility (BASMI) and of functional limitation (BASFI), measures of disease activity (ASDAS ESR and ASDAS CRP), and measure of radiological changes (BASRI) in AS patients. However, tibial cartilage thickness was negatively correlated with disease duration, BASMI, BASFI, and BASRI. Moreover, we found a very strong positive correlation between the femoral and the tibial cartilage thicknesses, which was in agreement with Cicuttini et al. [32] who reported a strong correlation between the femoral cartilage and the tibial cartilage in both medial and lateral tibiofemoral joints in normal subjects and in those with osteoarthritis.

Due to its high cost, lengthy scanning time, and restricted accessibility, MRI has a limited role in ordinary clinical practice. The US offers a reliable, accessible, affordable, and clinically focused option that could enable more frequent evaluations of the health of the cartilage [33]. Clinicians can measure the thickness at three different sites on the anterior femur to typically establish the size of the anterior femoral cartilage [10].

In the present study, measures of MSUS revealed that AS patients had thinner femoral cartilage than the healthy controls at all measurement sites, with statistically significant differences at both medial femoral condyle (P = 0.02) and at the right and left intercondylar area (P = 0.04 and P = 0.03, respectively).

Contrary to our findings, Batmaz et al. [4] found that individuals with AS had cartilage measures that were considerably thicker at the intercondylar area (P < 0.001) and left medial femoral condyle (P = 0.01). A subgroup study (anti-tumor necrosis factor (TNF) users and anti-TNF naive) revealed that cartilage thickness measurements in the left medial femoral condyle and bilateral intercondylar area were higher in AS patients receiving anti-TNF medication (n = 65) compared to healthy controls. The authors hypothesized that anti-TNF in their patients may have partially protected the cartilage in the knee joint. Sadly, none of our patients with AS are utilizing anti-TNF.

We are the first to describe a relationship between the values obtained from an ultrasonographic examination of the femoral cartilage and patient features in individuals with AS. Femoral cartilage thickness was negatively correlated with age, the measure of disease activity (ASDAS ESR), and radiological changes (BASRI), but it was not correlated with disease duration or laboratory tests. Batmaz et al. [4] failed to find any correlations between clinical and laboratory parameters and ultrasonographic femoral cartilage thickness in AS patients, and similar findings were reported for patients with Behçet’s disease [34]. Moreover, Mesci et al. [35] showed the absence of correlations between ultrasonographic femoral cartilage thickness and age, disease duration, disease activity score-28, health assessment questionnaire scores, ESR, and CRP levels in rheumatoid arthritis patients. Differences within the previous studies may be due to different designs, sample sizes, and ages of the patients.

The present study demonstrated that ultrasonographic total femoral cartilage thickness had a significant positive correlation with MRI total femoral cartilage thickness (r = 0.49, P = 0.02). Very little data are available regarding the comparison between MRI and ultrasound for the assessment of cartilage thickness. Similar results were reported by Tarhan and Unlu [36] and Eckstein et al. [27] who found that there is a high agreement between MRI and ultrasonography in assessing cartilage thickness in patients with knee OA.

Moreover, Pradsgaard et al. [37] used MRI and MSUS to examine the distal femoral cartilage thickness in juvenile idiopathic arthritis patients. They demonstrated the relationship between sonographic and MRI measurements of cartilage thickness and stated that the medial femoral condyle had cartilage that was thinner than the lateral femoral condyle.

Despite advantages of MSUS, there are some limitations associated with the external US of the knee joint. First, it is possible to scan only a part of the femoral condyle cartilage due to the shadow of the patella. Second, external US has no access to the tibial plateau cartilage because of the narrow aquatic window for ultrasound rays at this site which was considered a major limitation [38].

MRI-derived measurements of cartilage thickness and cartilage thickness pattern had high validity [39]. In quantifying cartilage thickness, central and weight-bearing regions of the femoral condyles can provide a more accurate measurement than boundary and non-weight-bearing regions [20]. The thickness of cartilage as determined by MRI appears to be a reliable way to quantify knee cartilage. Cartilage thickness measurement employing a 3.0-T imaging system showed nonsignificant differences from measurements employing a 1.5-T system [40].

Study limitations

The current study had certain limitations. Firstly, it was cross-sectional with a small sample size. Secondly, only the cartilage's thickness and not the volume was measured. Yet, apart from a wide range of studies on MRI imaging of AS patients, we believe that there are no data regarding assessing femoral and tibial cartilage thickness.

Conclusions

Patients with AS had thinner knee cartilage thickness than healthy controls. Correlations of knee cartilage thickness with measures of disease activity, spinal mobility, functional limitation, and radiological changes reflect the useful value of MRI and MSUS in determining areas of knee cartilage loss in AS patients. US may serve as a good alternative to MRI for the assessment of femoral (not tibial) cartilage thickness in AS patients. Further studies including a large number of patients were recommended to evaluate the impact of different therapies (specifically TNF inhibitor) on knee cartilage thickness.

Availability of data and materials

All relevant data are incorporated into the manuscript. Other raw data underlying this article will be provided at a reasonable request to the corresponding author.

Abbreviations

AS:

Ankylosing spondylitis

MSUS:

Musculoskeletal ultrasound

MRI:

Magnetic resonance imaging

BASRI-s:

Bath Ankylosing Spondylitis Radiology Index for the spine

BASFI:

Ankylosing Spondylitis Functional Index

ASDAS ESR:

Ankylosing Spondylitis Disease Activity Score-erythrocyte sedimentation rate

BMI:

Body mass index

BASDAI:

Bath Ankylosing Spondylitis Disease Activity Index

ASDAS CRP:

Ankylosing Spondylitis Disease Activity Score-C-reactive protein

BASMI:

Bath Ankylosing Spondylitis Metrology Index

RLC:

Right lateral condyle

RIA:

Right intercondylar region

RMC:

Right medial condyle

LMC:

Left medial condyle

LIA:

Left intercondylar area

LLC:

Left lateral condyle

χ 2 :

Chi-square

VAS:

Visual analog scale for pain

CPII:

C-propeptide of type II collagen

Anti-TNF:

Anti-tumor necrosis factor

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Acknowledgements

Not applicable.

Funding

No funding was obtained for this study.

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Authors and Affiliations

  1. Rheumatology and Rehabilitation Department, Faculty of Medicine, Minia University, Minya, 61111, Egypt

    Omnia R. Adel, Shereen R. Kamel, Fatma A. Mohamed & Ayman F. Darwish

  2. Radiology Department, Faculty of Medicine, Minia University, Minya, Egypt

    Nadia F. El Ameen

Authors
  1. Omnia R. Adel
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  2. Shereen R. Kamel
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  3. Fatma A. Mohamed
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  4. Nadia F. El Ameen
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  5. Ayman F. Darwish
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Contributions

SRK helped in idea, design of work, manuscript writing, and revision. AFD helped in interpretation of data and revision of the manuscript. FAM helped in MSUS assessment and interpretation of data. NFE helped in MRI assessment and interpretation of data. ORA helped in collection, statistical data analysis, and manuscript revision. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Shereen R. Kamel.

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Ethics approval and consent to participate

The study protocol complies with the Declaration of Helsinki and was approved by the ethics committee of the Faculty of Medicine, Minia University (19-2016).

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Not applicable.

Competing interests

The authors declare that they have no competing interests.

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Adel, O.R., Kamel, S.R., Mohamed, F.A. et al. Ankylosing spondylitis impact on knee cartilage thickness: correlation with demographic data and clinical characteristics. Egypt J Radiol Nucl Med 54, 196 (2023). https://doi.org/10.1186/s43055-023-01142-6

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  • DOI: https://doi.org/10.1186/s43055-023-01142-6

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