International Journal of Rheumatic Diseases 2013

ORIGINAL ARTICLE

Rheumatoid arthritis disease activity and vitamin D deficiency in an Asian resident population Mohammed K. QURAISHI1 and Humeira BADSHA2 1 Department of Renal Medicine, Heart of England NHS Foundation Trust, Birmingham, UK; and 2Department of Rheumatology, Dr. Humeira Badsha Medical Center, Dubai, UAE

Abstract Aim: We aimed to assess the prevalence of vitamin D deficiency and its association with rheumatoid arthritis (RA) disease activity in a UAE population. Methods: Forty-five consecutive subjects were prospectively recruited during the early summer with their clinical examination and Health Assessment Questionnaire (HAQ) being recorded at a clinic appointment, along with their blood sample being taken for the 25-hydroxyvitamin D (25(OH)D) total test. Results: Thirty-five (76%) patients claimed to be exposed to sunlight for < 30 min daily. The prevalence of vitamin D insufficiency (20–30 ng/mL) and deficiency (< 20 ng/mL) was 36% and 29%, respectively. RA patients who exposed their hands and feet (29 ng/mL) or more (34 ng/mL) to the sunlight had serum vitamin D levels higher than those who exposed their hands alone (18 ng/mL) or less (19 ng/mL) (P < 0.05). The variations in vitamin D levels due to skin color did not reach significance. No significant correlation was seen between serum vitamin D levels and Disease Activity Score (DAS28) or HAQ scores. A direct relationship was observed between HAQ scores and DAS28 scores (P < 0.05). Conclusion: We highlight the importance of skin exposure to sunlight in a conservative dressing culture. No association was observed between vitamin D and disease activity. However, the high prevalence of vitamin D deficiency may negatively impact on bone health of these patients in the future. Key words: association, Emirates, rheumatoid arthritis, United Arab Emirates, vitamin D.

INTRODUCTION Vitamin D plays a vital function in promoting the expression of the genes involved in bone deposition and calcium absorption.1 It also has an important role in regulating autoimmune diseases such as rheumatoid arthritis (RA) by suppressing T cell proliferation and inhibiting gene expression of inflammatory cytokines, including interleukin-2 and interferon-c.2,3

Correspondence: Dr Mohammed K. Quraishi, Department of Renal Medicine, Heartlands Hospital, Heart of England NHS Foundation Trust, Birmingham, West Midlands B9 5SS, UK. Email: [email protected]

Epidemiological studies conducted in the very recent past have attempted to define vitamin D’s role in patients suffering from RA. Increased intake of the vitamin D resulting in significantly lower incidence of RA was reported by a breakthrough cohort study.4 This paved the way for studying the association between serum vitamin D and RA disease activity, which has been controversial, with conflicting results. Studies, including an American cohort study, found high prevalence of low vitamin D in their RA patients, with Vitamin D insufficiency and deficiency prevalences of 84% and 43%, respectively.5 It was the vitamin D deficiency and not the insufficiency that was directly associated with tender joint counts and inflammatory markers (such as C-reactive protein [CRP] levels) in RA

© 2013 Asia Pacific League of Associations for Rheumatology and Wiley Publishing Asia Pty Ltd

M. K. Quraishi and H. Badsha

patients. Vitamin D deficiency prevalence in a largescale multi-centric study on an Italian population was 43%. Rossini et al.6 revealed a statistically significant inverse association between logarithmic serum vitamin D levels and logarithmic Disease Activity Score of 28 joints (DAS28) and Health Assessment Questionnaire (HAQ) scores, only upon exclusion of patients on vitamin supplements. A UK population study exhibited an inverse association between serum vitamin D and tender joint count, DAS28 and HAQ score, upon patients’ initial clinical presentations.7 However, only a significant inverse association was observed between vitamin D and HAQ score after a 1-year follow-up. No significant associations between serum vitamin D and swollen joint count, pain visual analogue scale (VAS) and DAS28 scores was seen in a similar study on an AfricanAmerican population.8 This association has been investigated in a variety of population groups but not in any Middle Eastern or Asian population. This comes of a surprise considering the increased risk of vitamin D insufficiency in nonCaucasians.9 Vitamin D insufficiency may be more prevalent in an Asian RA population, which will enable the study of a more definitive association between vitamin D levels and RA disease activity. If such an association is significant, simple therapeutic measures may be instilled to delay the severely symptomatic stages of RA. If supplementation improves disease activity and severity, low vitamin D may be a causal factor of the symptomatic severity instead of vice versa. Vitamin D insufficiency in the Asian population is a major concern, particularly among females. This may partly be as a consequence of conservative dressing in line with local cultural customs.10 Evidence of male vulnerability was found in a Qatari study of male athletes who were shown to have a 91% prevalence of vitamin D deficiency, despite the bright sunny climate from a low latitude country.11 United Arab Emirates (UAE) is currently at the epicentre of a medical revolution with an influx of highstandard clinicians, academics and health services. Health awareness among the majority of its South Asian expatriate population reflects the increased demand for specialist rheumatology assessment and intervention, which allows for convenient patient recruitment.12 Furthermore, published evidence reveals an astounding prevalence of vitamin D deficiency in this country.13,14 The primary aim of this study was to assess the association of serum vitamin D levels and RA disease activity in an Asian RA patient population. The secondary aim was to document the prevalence of vitamin D deficiency

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and insufficiency along with the relevant risk factors in this population.

METHODS Study population Forty-five patients were prospectively recruited from a specialist stand-alone rheumatology centre. All patients were residents of the UAE and met the American College of Rheumatology (ACR) 2010 criteria for RA. Patient enrolment was undertaken in the early summer and written informed consent was obtained from each participant. Ethical approval was granted from the Dubai Health Authority for this study. The study was conducted in accordance with recommendations from the Declaration of Helsinki.

Questionnaire A standardized questionnaire was filled to collect patient information, including age, gender and ethnicity. Vitamin D deficiency risk factors such as the daily duration of exposure to sunlight, the degree of skin exposure to sunlight and independently assessed skin tone were documented for each patient upon an interview after recruitment. The daily duration of exposure was quantified as < 30 min, 30–60 min, 60–120 min and > 120 min. Skin tone was assessed independently by the interviewer, categorising them as dark, olive or fair.

Blood tests The serum vitamin D levels were measured using a 25-hydroxyvitamin D (25(OH)D) total commercial radioimmunoassay at a single laboratory (HSL, Dubai, UAE). The 25(OH)D metabolite of vitamin D was selected for assessment because its levels are independent of calcium and phosphate status (measurement unavailable for the study) of the patient. To enable comparisons with other populations, vitamin D insufficiency and deficiency was defined as 20–30 ng/mL and < 20 ng/mL, respectively. Baseline laboratory investigations to monitor the RA profile as part of routine follow-up care for the patient were also documented and these included the CRP and erythrocyte sedimentation rate (ESR). Patients’ rheumatoid factor (RF) and anticyclic citrullinated peptide antibody (anti-CCP) status were also documented.

Measures of RA disease activity and severity The questionnaire, blood investigations and clinical examination were all conducted on the same day for

International Journal of Rheumatic Diseases 2013

Vitamin D in rheumatoid arthritis

each patient. The documented clinical findings and blood results were used to calculate the DAS28 for RA. DAS28 was also categorized into disease activity status groups, including remission (< 2.6), low (2.6–3.2), medium (3.2–5.1) and high (> 5.1). Functional ability to undertake daily activities was assessed using the HAQ which enables patients to rate their ability on a 0– 3 scale.

Table 1 Characteristics of rheumatoid arthritis patients in our cohort

Medication

Present medications

Treatments specific for RA management were noted, including non steroidal anti-inflammatory drugs (NSAIDS), corticosteroids, disease-modifying anti-rheumatic drugs (DMARDS) and anti-tumor necrosis factor (TNF) therapies. Previous and current usage of vitamin D and calcium supplements were also noted.

DMARDS Leflunamide Hydroxychloroquine Methotrexate Sulfasalazine None Glucocorticoids Prednisolone Anti-TNF Therapy Medications previously used Anti-TNF therapy Anti-B cell therapy Anti IL-6 therapy

Statistical analysis Data was analyzed using SPSS V20 (IBM Corp., Armonk, NY, USA). Mean values were calculated for all continuous findings of the values, along with their standard deviations. In order to study associations between two continuous variables, a Pearson’s correlation coefficient was calculated. To study differences in mean findings of related continuous interval groups, an unpaired Student’s t-test or a one-way analysis of variance (ANOVA) was performed when relevant. Differences were considered to be of statistical significance at P < 0.05.

RESULTS Patient profiles Forty-five patients were prospectively recruited during the early summer period. Females constituted 37 (84%) patients of the sample, which had a total mean age ( SD) of 45.2 ( 11.4) years. The ethnic distributions, medication usage and antibody status of the patients recruited are listed in Table 1. RF was found to be prevalent in 64% of the patients. Details of anti-CCP and RF status are listed in Table 1.

Prevalence of vitamin D insufficiency and risk factors Table 2 lists the prevalence of the vitamin D level categories in our patient profile. The mean (SD) serum vitamin D level in the entire population was 26.3 (12.9) ng/mL. The overall insufficiency of vitamin D (< 30 ng/ mL) was found in 65% of the population. Only 16% of the sample did not have a past episode of vitamin D insufficiency. Vitamin D therapy in our cohort is listed in Table 3. With regards to over-the-counter (OTC)

International Journal of Rheumatic Diseases 2013

Ethnicity

Frequency

Percentage

28 10 4 2 1

62.2 22.2 8.9 4.4 2.2

Indian subcontinent Arab Caucasian East Asian Hispanic

Anti-CCP status Positive Negative Undocumented anti-CCP status RF status Positive Negative Undocumented RF status

Frequency 5 4 25 8 8 7 5 5 1 1 Frequency

Percentage

20 9 16

44.4 20.0 35.6

29 12 4

64.4 26.7 8.9

DMARDs, disease-modifying anti-rheumatic drugs; TNF, tumor necrosis factor; IL, interleukin; Anti-CCP, anticyclic citrullinated peptide; RF, rheumatoid factor.

Table 2 Prevalence of vitamin D insufficiency and deficiency Status Vitamin D insufficiency (20–30 ng/mL) Vitamin D deficiency (< 20 ng/mL) Vitamin D sufficiency (> 30 ng/mL)

Frequency

Percentage

16

35.6

13 16

28.9 35.6

medication, only nine patients used calcium supplements, one patient used vitamins and two patients used Vitamins and calcium supplements. Supplementation of calcium and/or vitamins was observed with higher serum vitamin D levels (n = 12, 32.7 ng/mL) than those on nil supplements (n = 33, 24.0 ng/mL) (P < 0.05). Seventeen patients (38%) were undertaking

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M. K. Quraishi and H. Badsha

Table 3 Vitamin D therapeutic usage at time of the blood tests

1000 IU once daily 50 000 IU 12-week course 300 000 IU intramuscular Nil

Frequency

Mean serum 25OH-D(SD)

10 4 3 28

34 (10.89) 34.68 (9.55) 23 (14.4) 22.72 (12.68)

prescribed treatment to improve their vitamin D levels at the time of blood sample collection, with the most widely used being the 1000 IU tablets (59%). The difference in serum vitamin D between the vitamin D treatment groups was significant (one-way ANOVA, P < 0.05). Sunscreen usage was observed by only six (13.3%) patients. Table 4 summarizes the prevalence of risk factors for vitamin D deficiency in our cohort. 76% of the patients were exposed to < 30 min of sunlight daily (Fig. 1). A statistically significant difference was observed between the various sunlight exposure duration groups (one-way ANOVA, P < 0.01), but no association trends were observed. Skin exposure was classified as nil (face exposed alone or less), hands alone, hands and feet alone and more than hands and feet alone. The patients exposing more than their hands and feet (33.8 ng/mL) or their hands and feet alone (29.3 ng/mL) had statistically significant higher mean serum Vitamin D levels than their counterparts who exposed their hands alone (19.3 ng/mL) or less (18.1 ng/mL) (P = 0.002). Patient’s skin color was

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Frequency

On vitamin D therapy

40

10

0

4

34 8 1 2

25.2 (12.5) 28.6 (6.1) 65.5 16.9 (11.2)

11 6 18 10

19.3 (9.4) 18.1 (10.6) 29.3 (13.9) 33.8 (10.2)

19 13 11

28.7 (14.1) 23.7 (14.2) 25.8 (8.8)

30–60 mins

60–120 mins

> 120 mins

Figure 1 Sunlight exposure frequency.

independently assessed by the interviewer and categorized as dark, olive or fair. The distribution of mean serum vitamin D levels for each skin exposure category is depicted in Figure 2. The majority of the patients had dark skin (42%). No associations were observed between skin color and serum vitamin D levels. Analysis of serum Vitamin D levels revealed no significant differences between the ethnic groups (Fig. 3).

RA disease activity Table 5 is a summary of our findings of factors assessing disease activity. The negative association between the HAQ score and serum vitamin D did not reach statistical significance. The association of serum vitamin D levels with tender joint counts, swollen joint counts, 40

Mean serum vitamin D level (ng/mL)

Sunlight exposure duration < 30 min 30–60 min > 60 min > 120 min Skin exposure Nil Hands alone Hands and feet alone More than hands and feet Skin color Dark Olive Fair

Mean serum 25OH-D(SD)

< 30 mins

Duration of sunlight exposure

Table 4 Prevalence of certain Vitamin D deficiency risk factors Prevalence

20

30

20

10

0

Nil

Hands alone

Hands & feet alone

More than hands & feet

Skin exposure to sunlight

Figure 2 Mean serum vitamin D in each skin exposure group.

International Journal of Rheumatic Diseases 2013

Vitamin D in rheumatoid arthritis

1.0

0.8 35

Mean HAQ score

Mean serum vitamin D level (ng/mL)

40

30

25

0.6

0.4

0.2

0.0

20 Indian subcontinent

Arab

East asian

Hispanic

Remission

Caucasian

Low

Medium

High

DAS status

Ethnicity

Figure 4 Mean HAQ score against Disease Activity score status.

Figure 3 Mean serum vitamin D among ethnicities. Table 5 Rheumatoid arthritis disease activity and severity features

2.0

Mean

SD

Tender joint count Swollen joint count Pain Visual Analogue Scale (VAS) Health Assessment Questionnaire (HAQ)

2.27 2.7 33

3 3.7 27

0.58

0.46

Disease activity score status Remission Low Medium High

Frequency

Mean serum 25(OH)D (ng/mL) (SD)

11 4 24 6

22.9 (9.3) 34.5 (23.6) 26.4 (13.3) 26.8 (8.8)

pain VAS and DAS28 scores were not statistically significant. The differences in the mean serum vitamin D Levels between the DAS28 statuses (remission, low, medium and high) were not significant. Figure 4 shows the mean HAQ for each DAS28 status. Mean HAQ results strongly correlated with the DAS28 score among patients (r2 = 0.325, P < 0.001) (y = 0.128 + 0.198 9 DAS28 score) (Fig. 5). The difference in the mean HAQ score between DAS28 statuses (remission, low, medium and high) were highly significant (P < 0.001).

DISCUSSION A female prevalence of 84% and RF positivity of 71% (excluding undocumented results) in our cohort was

International Journal of Rheumatic Diseases 2013

1.5

HAQ score

Feature

1.0

0.5

0.0 0

2

4

6

DAS28 score

Figure 5 Correlation of HAQ score against DAS28 score. HAQ, Health Assessment Questionnaire; DAS28, Disease Activity Score of 28 joints.

similar to the findings in the UAE component of the large-scale QUEST-RA study: females (85.8%), RF positivity (75.4%).15 A paucity of evidence exists when documenting levels of vitamin D in residents of the UAE. Mothers of both Arab and South Asian ethnicities in the UAE, having delivered newborns, had a serum vitamin D level of 8.7 ng/mL.16 The high prevalence of vitamin D deficiency in non-Western pregnant and postnatal mothers has been documented, with a possible etiological explanation for the low vitamin D levels in this case.17,18 The finding in these mothers makes it difficult to justify

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M. K. Quraishi and H. Badsha

generalizing them to all women residing in the UAE. However, another Emirati study found no significant difference between baseline serum vitamin D levels in lactating mothers and nulliparous women, yet both groups still had very low levels (10.1 ng/mL and 7.72 ng/mL, respectively).13 Females had statistically higher mean vitamin D levels (10.3 ng/mL) than males (9.68 ng/mL) in a study addressing the prevalence of vitamin D deficiency in young Emiratis.14 The mean serum vitamin D level in our sample was 26.3 ng/mL with no statistically significant difference being observed between the male (25.0 ng/mL) and female (26.6 ng/mL) demographics. The higher mean serum vitamin D levels in our sample than the aforementioned UAE studies may be explained by past vitamin D treatment partially normalizing the insufficiency, with only 14% not having a past vitamin D insufficiency diagnosis. We found the prevalence of vitamin D insufficiency (20–30 ng/mL) and deficiency (< 20 ng/mL) as 36% and 29%, respectively, indicating a 65% suboptimal (< 30 ng/mL) vitamin D level in the cohort. Comparisons of prevalence with similar studies are limited by the differences in definitions of vitamin D insufficiency and deficiency. Vitamin D deficiency prevalence was higher in studies conducted on Italian (43%) and American (45%) RA populations.5,6 A review concluded that vitamin D levels in the range 36–40 ng/mL are most optimal for bone health and other health outcomes.19 Only 11% of our cohort lay in this range. Patients on calcium and/or vitamin supplements had a mean sufficient serum vitamin D level (> 30 ng/mL), which was not seen in those on nil supplements. OTC supplements are inexpensive and indicate an important role in maintaining acceptable vitamin D levels. A mean sufficient vitamin D level was also seen in patients undertaking the 1000 IU or 50 000 IU treatments. The low mean serum vitamin D levels in patients on the 300 000 IU treatment may be explained by intervening for a severely low vitamin D level which only achieved partial normalization at time of the blood collection. The difference in vitamin D was significant between patients who exposed hands and feet or more than those who did not. However, we were unable to elicit a trend of increasing serum vitamin D level with increasing skin exposure, such as that by the Jordanian study.10 Skin color and vitamin D relationship is well recognized, but our failure to exhibit this trend may have been a consequence of the absence of a validated objective skin tone measure.20

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The majority of patients stated they had been exposed to < 30 min of sunlight. No trend between exposure duration and serum vitamin D was seen partly because of the fewer incidences in the longer duration groups and due to the large duration ranges of the groups. Only 22% of the sample exposed more than hands and feet alone, reflecting the conservative nature of the population. Our primary aim was to assess the relationship between DAS28 and serum Vitamin D levels. However, we were unable to observe a significant correlation between the two variables. Similar studies looking at new diagnoses of inflammatory arthritis or RA found associations between DAS28, HAQ, tender joint counts and serum vitamin D only at baseline and not after a year or later of follow-up.7,8 Kerr et al.,5 Rossini et al.6 and Cutolo et al.21 studied this association in patients with active disease (not recently diagnosed patients). Kerr et al. found no difference in DAS28 between RA cohorts having vitamin D insufficiency or sufficiency. Cutolo et al.21 was able to find an association between DAS28 and serum vitamin D in Italian patients in summer and Estonian patients in winter only. Rossini et al. depicted this association in their large-scale Italian resident sample only in patients not supplemented with vitamins. The DAS status of medium or high was also found to have a significantly lower serum vitamin D level. Trends between swollen joint count, DAS status, HAQ and serum vitamin D were unable to be established in our sample despite exclusion of OTC-supplemented patients, which was evident in the Italian cohort. It is difficult to conclude if a similar association between RA disease activity and serum vitamin D exists in an Asian patient population. We would like to acknowledge the various limitations in our study. Studying associations between variables including serum vitamin D against exposure duration may have not reached statistical significance because of the low frequencies in the dependant groups. The relationship between continuous variables, including DAS28 and serum vitamin D, which may have existed, were perhaps not seen due to an inadequate sample size. The documentation of past medications and date of diagnosis was not conducted as initially planned, due to poor patient recall and past medical records.

CONCLUSION Vitamin D insufficiency and deficiency is highly prevalent in an Asian RA population, but it is less than anticipated. The majority of patients avoided sunlight for

International Journal of Rheumatic Diseases 2013

Vitamin D in rheumatoid arthritis

long periods and a lower vitamin D level was observed in patients with more conservative dressing. Our preliminary study does not support the link between disease activity and serum vitamin D levels in an Asian resident RA population as has been suggested by studies addressing other populations. It is possible that these associations were not depicted due to the limited sample size. Further research in this population must be undertaken to disprove the hypothesis with better reliability.

ACKNOWLEDGEMENTS The authors would like to thank the University of Birmingham and the British Medical and Dental Students’ Trust for awarding MKQ with the Onnesley Bursary and the Elective Grant.

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AUTHOR CONTRIBUTIONS Conception and design, reviewing manuscript, Dr Humeira Badsha; data analysis and drafting of manuscript, Dr Mohammed Kamil Quraishi; data acquisition: both authors. Host instituition: Al Biraa Arthritis & Bone Centre, Villa 1029, Al Wasl Road, Um Suqaim, Dubai, UAE.

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levels and disease activity in patients with early inflammatory polyarthritis. Arthritis Rheum 56, 2143–9. Craig SM, Yu F, Curtis JR et al. (2010) Vitamin D status and its associations with disease activity and severity in African Americans with recent-onset rheumatoid arthritis. J Rheumatol 37, 275–81. Grinde AA, Liu MC, Camargo CA Jr (2009) Demographic differences and trends of Vitamin D insufficiency in the US population, 1988–2004. Arch Intern Med 23, 626–32. Mishal A (2001) Effects of different dress styles on vitamin D Levels in healthy young Jordanian women. Osteoporos Int 12, 931–5. Hamilton B, Grantham J, Racinais S, Chalabi H (2010) Vitamin D deficiency is endemic in Middle Eastern sportsmen. Public Health Nutr 13, 1528–34. 1.7 Labour Market In The UAE. (2012) RAK Free Trade Zone.[cited 2013] Available online at http://www.rakftz. com (accessed 5 March 2013). Saadi H, Dawodu A, Afandi A, Zayed R, Benedict S, Nagelkerke N (2007) Efficacy of daily and monthly high-dose calciferol in Vitamin D–eficient nulliparous and lactating women. Am J Clin Nutr 85, 1565–71. Anouti F, Thomas J, Abdel-Wareth L, Rajah J, Grant WB, Haq A (2011) Vitamin D deficiency and sun avoidance among university students at Abu Dhabi. Dermatol Endocrinol 3, 235–9. Sokka T, Toloza S, Cutolo M et al. (2009) Women, men, and rheumatoid arthritis: analyses of disease activity, disease characteristics, and treatments in the QUESTRA study. Arthritis Res Ther 11, R7. Dawodu A, Agarwal M, Hossain M, Kochiyil J, Zayed R (2003) HypoVitaminosis D and Vitamin D deficiency in exclusively breastfeeding infants and their mothers in summer: a justification for Vitamin D supplementation of breast-feeding infants. J Pediatr 142, 169–73. Van der Meer IM, Karamali NS, Boeke AJ et al. (2006) High prevalence of Vitamin D deficiency in pregnant nonWestern women in The Hague, Netherlands. Am J Clin Nutr 84, 350–3. Sachan A, Gupta R, Das V, Agarwal A, Awasthi PK, Bhatia V (2005) High prevalence of Vitamin D deficiency among pregnant women and their new borns in north India. Am J Clin Nutr 81, 1060–64. Bischoff-Ferrari HA, Giovannucci E, Willett WC, Dietrich T, Dawson-Hughes B (2006) Estimation of optimal serum concentrations of 25-hydroxyVitamin D for multiple health outcomes. Am J Clin Nutr 84, 18–28. Glass D, Lens M, Swaminathan R, Spector TD, Bataille V (2009) Pigmentation and Vitamin D metabolism in caucasians: low Vitamin D serum levels in fair skin types in the UK. PLoS ONE 4, e6477. Cutolo M, Otsa K, Laas K et al. (2006) Circannual vitamin D serum levels and disease activity in rheumatoid arthritis: Northern versus Southern Europe. Clin Exp Rheumatol 24, 702–4.

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Rheumatoid arthritis disease activity and vitamin D deficiency in an Asian resident population.

We aimed to assess the prevalence of vitamin D deficiency and its association with rheumatoid arthritis (RA) disease activity in a UAE population...
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