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ORIGINAL ARTICLE
Year : 2021  |  Volume : 34  |  Issue : 1  |  Page : 347-353

Study of musculoskeletal manifestations in patients with inflammatory bowel diseases


1 Department of Physical Medicine, Rheumatology and Rehabilitation, Faculty of Medicine, Menoufia University, Shebeen El-Kom, Egypt
2 Department of Radiodiagnosis, Faculty of Medicine, Menoufia University, Shebeen El-Kom, Egypt
3 Department of Internal Medicine and Gastroenterology, Faculty of Medicine, Menoufia University, Shebeen El-Kom, Egypt

Date of Submission25-May-2019
Date of Decision11-Jun-2019
Date of Acceptance19-Jun-2019
Date of Web Publication27-Mar-2021

Correspondence Address:
Maha M. A. Salman
Melig, Shebin El Kom, Menoufia
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_183_19

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  Abstract 


Objective
The aim was to study the involvement of sacroiliac joints, lower limb joints, and enthesis and to detect osteoporosis in patients with inflammatory bowel disease (IBD), and then to correlate them with disease activity in patients with ulcerative colitis (UC).
Background
IBDs are systemic diseases that commonly display extraintestinal manifestations. Musculoskeletal involvement is one of the most common extraintestinal manifestations.
Patients and methods
This cross-sectional study included 50 patients with IBD who were evaluated for rheumatologic manifestations by clinical examination, laboratory, and radiologic studies such as musculoskeletal ultrasonography of lower limb entheses, digital radiographs of both sacroiliac and hip joints, and dual-energy X-ray absorptiometry scan for evaluation of osteoporosis.
Results
In this study, we found that most patients had tenderness rather than swelling of joints (knee tenderness in 66% and swelling in 34%). Bilateral sacroiliitis was present in 78% of patients. The proximal patellar entheses were the most inflamed site followed by Achilles tendon entheses. UC disease activity was significantly related to knee, ankle, and entheseal swelling and sacroiliac tenderness. There was a highly significant positive correlation between UC disease activity and fecal calprotectin level and a nonsignificant negative correlation with dual-energy X-ray absorptiometry scan T-score.
Conclusion
Musculoskeletal manifestations are common in patients with IBD and should be studied clinically and radiologically by expert rheumatologist for early detection and management.

Keywords: disease activity, entheses, inflammatory bowel disease, musculoskeletal, osteoporosis


How to cite this article:
Soliman SG, Labeeb AA, Mousa WA, Badr MH, Salman MM. Study of musculoskeletal manifestations in patients with inflammatory bowel diseases. Menoufia Med J 2021;34:347-53

How to cite this URL:
Soliman SG, Labeeb AA, Mousa WA, Badr MH, Salman MM. Study of musculoskeletal manifestations in patients with inflammatory bowel diseases. Menoufia Med J [serial online] 2021 [cited 2021 Jun 21];34:347-53. Available from: http://www.mmj.eg.net/text.asp?2021/34/1/347/312010




  Introduction Top


Inflammatory bowel diseases (IBD) are chronic inflammatory diseases affecting primarily the gastrointestinal tract, which include mainly ulcerative colitis (UC) and Crohn's disease (CD) [1]. Extraintestinal manifestations are commonly seen in patients with IBD with incidence ranging from 25 to 40% [2].

Musculoskeletal involvement is a major concern in patients with IBD with frequency of ∼20–50% [3]. IBD-related arthropathy is one of seronegative spondyloarthropathies, which are characterized by axial involvement (inflammatory low back pain and sacroiliitis) and peripheral symptoms (peripheral arthritis, dactylitis, and enthesitis) [4]. Patients with IBD also have many risk factors that lead to reduction in bone mineral density, which leads to osteopenia and osteoporosis [5].

The aim of this work was to study the involvement of sacroiliac joints, lower limbs joints, and entheses both clinically and radiologically and to detect osteoporosis in patients with IBD, and then to correlate these musculoskeletal manifestations with disease activity and fecal calprotectin level in patients with UC.


  Patients and methods Top


This cross-sectional study included 50 patients with IBD recruited from the outpatient clinic and gastrointestinal tract Endoscopy Unit of Internal Medicine Department and the Outpatient Clinic of Rheumatology, Physical Medicine and Rehabilitation Department in Menoufia University Hospitals during the period from October 2017 to October 2018. Exclusion criteria were age less than 18 years; history of any inflammatory, microcrystalline, degenerative, or infectious musculoskeletal disease; history of lower limb peripheral neuropathy; history of severe trauma; knee or ankle surgery; or corticosteroid injections in the examined structures. The study was approved by Menoufia Faculty of Medicine Ethics Committee, and all patients gave a written informed consent.

All patients were subjected to sociodemographic data (name, age, and sex) and clinical and radiological assessment of both IBD and rheumatologic manifestations.

  1. Inflammatory bowel disease assessment included history of type of IBD, disease duration, and number of flares and evaluation of disease activity using the CD Activity Index and the UC Mayo Index [6],[7]
  2. Rheumatologic evaluation included physical examination for tenderness or swelling in sacroiliac, hip, knee, and ankle joints, lower limbs enthesis, and dactylitis. Fecal calprotectin level was measured by ELISA (sandwich Hitachi EU 7000 manufacturer is :Hitachi High-Technologies Corporation (TSE: 8036, Hitachi High-Tech), in Tokyo, Japan. -Osteo Prima manufacturer is : Medonica Co., Ltd, in Seoul, South Korea) test according to kit's instructions; the kit suggested a cut-off level of less than 50 μg/g. Radiological studies included musculoskeletal ultrasonography using Hitachi EU 7000 (Japan), to detect either enthesitis or enthesopathy of lower limbs entheases. Digital radiographs (anteroposterior view) of both sacroiliac and hip joints was done. Dual-energy X-ray absorptiometry (DEXA) scan was done (using Osteo Prima DEXA bone densitometer/pencil beam; Korea) for detection of osteoporosis.


Statistical analysis

Data were collected, tabulated, and statistically analyzed using an IBM personal computer with statistical package of the social science (SPSS) version 22 (SPSS Inc., Chicago, Illinois, USA) where the following statistics were applied:

Descriptive statistics: quantitative data were presented in the form of mean, SD, and range, and qualitative data were presented in the form numbers and percentages (%).

Analytical statistics: Mann–Whitney test (U), Kruskal–Wallis test (K). and Spearman correlation coefficient test (r-test).

  1. P value of up to 0.05 was considered statistically significant
  2. P value of up to 0.001 was considered statistically highly significant.



  Results Top


This cross-sectional study included 50 patients with IBD. Five patients had CD and 45 had UC. Their age ranged between 23 and 52 years, with a mean of 35 years. Overall, 54% of patients were females and 46% were males. IBD duration range was 1–18 years, with a mean of 6 years. Tenderness of lower limbs joints was detected in most patients (sacroiliac 64%, hip 60%, knee 66%, ankle 58% and entheseal tenderness in 86% of patients), whereas swelling was detected in lesser number of patients (knee 34%, ankle 28%, and entheses 50% of patients) [Figure 1]. Sacroiliitis was mainly bilateral, affecting 78% of the patients, with grade 2 sacroiliitis being the most common, affecting 38% of the patients bilaterally. Hip arthritis was present in 62% of the patients [Figure 2]. Ultrasonographic study revealed that the proximal patellar entheses were the most affected (enthesitis in 38–46%, whereas enthesopathy in 20–26%) followed by Achilles tendon enthesis (enthesitis in 20–26%, whereas enthesopathy in 16–42%) [Figure 3], [Figure 4], [Figure 5].
Figure 1: Musculoskeletal signs in patients with inflammatory bowel disease.

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Figure 2: Frequency of sacroiliitis and hip arthritis in patients with inflammatory bowel disease.

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Figure 3: Ultrasonographic study of lower limb entheses in patients with inflammatory bowel disease.

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Figure 4: ultrasonography (US) image of proximal patellar enthesophyte (white arrow).

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Figure 5: ultrasonography (US) image of an abnormal tendo-Achilles insertion. Swollen, hypoechoic tendo-Achilles insertion, and irregular, blurred cortical outline denoting enthesitis.

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There was a significant relation between UC disease activity and sacroiliac tenderness and knee and ankle joints swelling [Table 1]. There was a highly significant relation between disease activity and entheseal involvement of proximal patellar tendons, and a significant relation with involvement of distal patellar tendons and right Achilles tendon [Table 2]. There was a highly significant positive correlation between UC disease activity and fecal calprotectin level and a nonsignificant negative correlation between UC disease activity and DEXA scan T-score at all levels [Figure 6] and [Figure 7] [Table 3].
Table 1: Relation between ulcerative colitis disease activity and musculoskeletal signs in this group

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Table 2: Relation between ulcerative colitis disease activity and ultrasonographic findings in lower limb entheses in this group

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Figure 6: Values of dual-energy X-ray absorptiometry (DEXA) scan scores in a patient with ulcerative colitis showing osteoporosis in spine and hips.

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Figure 7: Anteroposterior spine bone density of the same patient compared with reference values.

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Table 3: Correlation between ulcerative colitis disease activity and fecal calprotectin level and dual-energy X-ray absorptiometry scan T-score

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  Discussion Top


This study revealed that 60, 66, and 58% of the patients had hip, knee, and ankle tenderness, respectively; moreover, 34% had knee synovitis and 28% had ankle synovitis. This is consistent with Hammoudeh et al. [8] who found that peripheral manifestations were present in 43.3%. Perez-Alamino et al. [1] also found a prevalence of lower limb arthritis in 51% of the patients, and Fatemi et al. [9] found that 12 (57%) of 20 patients with IBD had arthritis. Moreover, Orchard [10] reported that ∼60–70% of the arthritis seen in patients with IBD is peripheral arthritis, and the most commonly affected joints are the knees, ankles, wrists, elbows, and hips. This result was higher than that reported by Malaty et al. [11] who studied 626 patients with IBD and found that 43% had inflammatory peripheral arthritis. However, Al-Jarallah et al. [12] found that peripheral arthritis was seen in 31.5% patients with IBD. Moreover, Bandyopadhyay et al. [13] reported peripheral arthritis in 23% of 120 patients with IBD. Ossum et al. [14] reported a much lower result, with the prevalence of IBD-related peripheral arthritis in 17.2%. This study revealed that 86% of patients had tenderness of lower limb entheses, whereas only 50% had swollen entheses. This result was close to that reported by van Erp et al. [15] who found that 48 (31.0%) patients had at least one tender pressure point for enthesitis, whereas only one (0.7%) patient with enthesitis. On the contrary, Ossum et al. [14] reported the prevalence of peripheral spondyloarthritis to be 27.9% of 441 patients with IBD. The Assessment of Spondyloarthritis International Society criteria were used to define peripheral spondyloarthritis, including patients with peripheral arthritis, enthesitis, and/or dactylitis.

In this study, 88% of patients had right sacroiliitis and 78% had left sacroiliitis. Bilateral sacroiliitis was found in 78% of patients. This result is consistent with Kelly et al. [16] who studied 49 patients with IBD and found that 64% of them fulfilled the imaging component of Modified New York criteria for AS. However, this result is much higher than that obtained by Chan et al. [17] who studied 233 patients with CD and 83 patients with UC by computed tomography scan and found that the prevalence of sacroiliitis was 15.5%. Moreover, Karreman et al. [18] found that the pooled prevalence calculated for sacroiliitis was 10%. Perez-Alamino et al. [1] reported that the prevalence of sacroiliitis was between 12 and 24%, and Bandinelli et al. [3] found occult Sacroiliac joint (SIJ) abnormalities at radiograph in 27% of patients with IBD. Al-Jarallah et al. [12] found that axial skeletal involvement presenting as a combination of spondyloarthritis with sacroiliitis was seen in 8.5% of 130 patients with IBD. Isolated sacroiliitis was seen in 3.1% of patients with IBD. In this study, most patients (38%) had grade 2 sacroiliitis. The second most common was grade 1 sacroiliitis. This is consistent with the results reported by Peeters et al. [19] who found radiological sacroiliitis in 23% of patients: 8% had unilateral sacroiliitis grade 2, 14% had bilateral sacroiliitis grade 2, and one had unilateral sacroiliitis grade 3.

In this study, the most commonly involved enthesis was the proximal patellar tendon. Enthesitis was found in 38–46% and enthesopathy in 20–26%.The second most affected site was Achilles tendon entheses, with enthesitis affecting 20–24% and enthesopathy in 16–42%. This result is consistent with Rovisco et al. [20] who found that the quadriceps tendon was affected in 40.8% of 76 patients with IBD, but on the contrary, the distal patellar tendon was affected in higher percent 67.1%. Moreover, they found that Achilles tendon was affected in 43.4% of patients and plantar fascia enthesitis in 25%, which is higher than our result. Moreover, Hsiao et al. [21] found that the most common abnormal enthesopathy in 14 patients with IBD were entheseal thickness of the proximal patellar ligament and quadriceps tendon.

In this study, there was a significant relation between UC disease activity and sacroiliac joints tenderness and knee and ankle swelling. This result is in agreement with Fatemi et al. [9] who found that 15% of the patients with current arthritis had active IBD. Moreover, this is in agreement with Ditisheim et al. [22] who found that inflammatory articular disease (defined as persistent or recurrent joint pain with an inflammatory pattern or the presence of arthritis) was associated with more active intestinal disease. On the contrary, Ossum et al. [14] found that IBD severity and activity were not different between those with IBD-related peripheral arthritis or peripheral spondyloarthritis and those without. In this study, we found a highly significant relation between UC disease activity score and entheseal involvement at proximal patellar tendons, and a significant relation at distal patellar tendons and right Achilles tendon. This is in contrast with Cuomo et al. [23] who concluded that the entity of entheseal alteration (as assessed by MASEI) did not correlate with activity of IBD. Moreover, Vicente et al. [24] concluded that subclinical entheseal Power Doppler ultrasonography (PDUS) abnormalities and enthesopathy in patients with IBD are independent of activity, duration, and type of gut disease.

In this study, we found a highly significant positive correlation between UC disease activity and fecal calprotectin level. This is consistent with Zittan et al. [25] who found that in UC, Fecal calprotectin (FC) was correlated with the Mayo clinical score and was highly correlated with the total Mayo score. In this study, we found a nonsignificant negative correlation between UC disease activity and DEXA scan T-score at all levels. This is in contrast with Piodi et al. [26] who reported that low bone mass in UC is related to the severity of the disease.


  Conclusion Top


This study showed that musculoskeletal manifestations are common in patients with IBD especially involvement of lower limbs joints and entheses. Most patients with IBD had different grades of radiographic sacroiliitis, hip arthritis. and osteoporosis. Most musculoskeletal manifestations are related to disease activity in patients with UC. The main limitations to this study were small sample size and we studied only patients with UC, so further studies should be performed on a large sample size and should include CD group for confirmation and better interpretation of the results.

Conflicts of interest

There are no conflicts of interest.



 
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