INTRODUCTION:

Systemic Lupus Erythematosus (SLE) stands as an autoimmune disease marked by a multifactorial etiology, involving an intricate interplay between genetic factors and environmental influences. Numerous studies emphasize the significance of environmental factors in the pathogenesis of autoimmune diseases, with vitamin D emerging as a notable example.

While deficiencies in vitamin D have been widely documented in various autoimmune conditions,^1-4 there is currently no concrete data about this condition in SLE patients, especially those treated at Dr. Soetomo Regional Public Hospital, Surabaya, Indonesia.

Vitamin D is chiefly derived from de novo synthesis in the skin, triggered by exposure to Ultraviolet B radiation. Despite the intake of vitamin D through food, reliance on dietary sources alone is often inadequate.⁵SLE patients exhibit several risk factors for hypovitaminosis D, characterized by nonspecific symptoms such as musculoskeletal pain, paresthesias, and cramps. These symptoms commonly overlap with those experienced by SLE patients, leading to potential oversight. Recognizing the importance of hypovitaminosis D treatment in individuals with SLE, given the potential immunomodulatory effects of vitamin D, becomes crucial.⁶Therefore, it is imperative to consider the likelihood of vitamin D hypovitaminosis in SLE patients, ensuring that appropriate management beyond conventional therapy is administered.

The role of Vitamin D is presumably exhibited through various mechanisms, including maintaining tolerance of antigen-presenting cells (APC) by inhibiting dendritic cell maturation,^7.8 as an antimicrobial,as well as anti-apoptosis by increasing self-antigen. A recent study found that vitamin D has the potential to downregulate the expression of Fasl and Bax. It also increases the expression of Bcl-2, a molecule with an antiapoptotic function. The antiapoptotic and antiproliferative effects are partly due to the termination of the cell cycle in G1. Immune cells can receive stimuli or signals because they have receptors, namely Vitamin D receptors (VDR). Furthermore, macrophages, dendritic cells, and B lymphocytes also have enzymes that can produce active Vitamin D. Activation of VDR initiates the impact on immune cells,⁸which will have a positive influence on SLE patients.

The afore mentioned report suggests a link between SLE activity and Vitamin D deficiency. The findings indicate heightened disease activity in SLE patients experiencing Vitamin D deficiency. Consequently, the objective of this study is to examine the levels of 25(OH)D in the serum of SLE patients receiving treatment at Dr. Soetomo Regional Public Hospital. The hypothesis posited in this study proposes an inverse association between the levels of 25(OH)D in the serum and disease activity in SLE patients visiting Dr. Soetomo Regional Public Hospital's Outpatient and Inpatient Installation, evaluated through the SLAM score. The primary objective is to facilitate the administration of appropriate additional therapy, with the overarching goal of mitigating the morbidity and mortality rates associated with SLE.

MATERIALS AND METHODS:

Employing an analytical method with a cross-sectional design, this research considered individuals between the ages of 16 and 50, encompassing both men and women, diagnosed with SLE according to the American College of Rheumatology (ACR) 1997 criteria.The study focused on new SLE patients, including those yet to undergo immunosuppressant therapy or those with a withdrawal period from SLE treatment exceeding four weeks.Inpatients and individuals undergoing routine control with methylprednisolone therapy of ≤4mg (Kasjmir et al., 2011), along with immunosuppressants, were considered. Participants were required to express a willingness to provide informed consent.⁹Exclusion criteria comprised SLE patients with overlapping conditions such as other connective tissue diseases (e.g., dermatomyositis, rheumatoid arthritis, scleroderma), diabetes mellitus, tuberculosis, a history of malignancy, and those using Vitamin D supplements. It was established that a minimum of 38.8 individuals, rounded up to 40, was required for this study according to the formula for determining sample sizes in correlation studies.

All participants underwent uniform clinical and laboratory assessments. Furthermore, clinical and laboratory data were evaluated and calculated using Systemic Lupus Activity Measure (SLAM) scores, which include constitutional, skin, eye, reticuloendothelial, pulmonary, cardiovascular, gastrointestinal, and neuromotor, as well as joint symptoms. Laboratory tests included hematological examination, as well as LED and renal involvement namely serum creatinine and urine sediment. Each parameter in the SLAM scores was assigned a value of 0-3, contributing to a total score ranging from 0 to 86.^10,11The completion of SLAM scores was conducted and approved by the attending Rheumatologist.

The researchers conducted the examination of 25(OH)D serum in Prodia Surabaya laboratory, utilizing chemiluminescent microparticle immunoassay (CMIA) technology with Architect 25(OH)D to measure the peripheral blood levels in the study subjects. Variable levels in serum are expressed in units of ng/mL.

The assessment of data distribution normality was conducted using the Shapiro-Wilk test. Spearman's statistical test was utilized to determine the correlation between two variables that did not follow a normal distribution. The data obtained were subjected to statistical analysis using SPSS for Windows version 23.0. Ethical approval for this study was obtained from the Health Research Ethics Committee of Dr. Soetomo Regional Public Hospital, Surabaya, under reference number 1197/KEPK/V/2019.

RESULT:

A cohort of 40 SLE participants, inclusive of both outpatients and inpatients at Dr. Soetomo Regional Public Hospital’s Department of Internal Medicine, meeting the stipulated inclusion and exclusion criteria, were enrolled. The general characteristics and laboratory examination details are presented in Table 1. The majority of the subjects had hematological disorders in the form of anemia, as well as increased LED.

25(OH)D Serum Levels in the Study Subjects:

All subjects were examined for their 25(OH)D serum levels, which had a mean of 21.69±2.72ng/mL. The Normality test with Saphiro-Wilk showed that the data obtained were normally distributed.

SLE activity in study subjects:

The activity of SLE was measured using the SLAM scores, and the results showed a median of 17.5, with the lowest score of 1 and the highest of 39. The normality test with Saphiro-Wilk showed that the levels of data were abnormally distributed. See Tables 2 and 3.

Table 2. Characteristics of the subjects based on the SLAM Scores

Indicator	n (%)
Constitutional	28 (70%)
Integument	24 (60%)
Reticuloendothelial	9 (22.5%)
Pulmonary	16 (40%)
Cardiovascular	8 (20%)
Gastrointestinal	4 (10%)
Neuromotor	23 (57.5%)
Joints	25 (62.5%)
Laboratory:
Hematology + LED	35 (87.5%)
Renal	25 (62.5%)

Table 3. Characteristics of ANA Profile

Indicator	n (%)
RNP/Sm	12 (30%)
Sm	6 (15%)
SS-A native	16 (40%)
Ro-52 recombinant	12 (30%)
SS-B	5 (12.5%)
Scl-70	2 (5%)
PM-Scl100	1 (2.5%)
Jo-1	1 (2.5%)
dsDNA	12 (30%)
Nucleosomes	13 (32.5)
Histones	18 (45%)
Ribosomal Protein	14 (35%)
AMA-M2	7 (17.5%)

Interrelation of 25(OH)D Serum Level with the Activity of SLE in Study Subjects:

Through the utilization of the Spearman correlation test, an exploration into the connection between SLAM scores and 25(OH)D serum levels was conducted, revealing a substantial positive correlation (r = -0.665, p < 0.01), as depicted in Figure 1. Consequently, an examination of the associations between CRP, C3, C4, anti-dsDNA, and LED with 25(OH)D serum levels was conducted, revealing noteworthy correlations exclusively with C3 (r = 0.538; p < 0.01), C4 (r = 0.356; p = 0.024), and CRP (r = -0.414; p = 0.008).

Figure 1. Scatter Diagram of the Interrelation of 25(OH)D Serum Level with the Activity of SLE.

DISCUSSION:

Hypovitaminosis D is common in Southeast Asian countries, with a prevalence of 6-70%. Some of the factors that influence this include skin pigmentation, aging, sun protection behavior such as sunscreen application, religion, lifestyle, and nutritional differences.¹²

In this study, the participants comprised productive young women exhibiting mild to high Systemic Lupus Erythematosus (SLE) activity. Consequently, it was anticipated that these individuals would manifest adecline in 25(OH)D serum levels. The results reaffirm the hypothesis, showcasing a strong inverse relationship between disease activity, as measured by the SLAM scores, and 25(OH)D serum levels.

Gender distribution found that all subjects were female. In several epidemiological studies of SLE patients, it was found that women had a higher incidence than men.^13,14 These findings are also consistent with similar studies conducted in Denmark and Korea.^15,16 The average age of study subjects at diagnosis is 27.43 years, with a range of 17-49 years. The most dominant age groups in this study sample were 21-30 years old (35%) and 31-40 years old (32.5%). This result is consistent with other studies conducted in Korea, Malaysia, and the Philippines.^16,17 These studies support the theory that SLE is a dominant disease in women of childbearing age, and this is related to the estrogen and prolactin hormones.^18-20

SLAM Score is a tool for scoring systems to assess the activity of SLE, and it has been validated internationally.²¹ It was obtained in the subjects with a median of 17.5, a minimum score of 1, and a maximum score of 39. This is the same as the study conducted by Paramaiswari et al. (2014) in Jogyakarta, which showed that the average SLAM score of SLE inpatients was16.7.²² Furthermore, Yuliasih et al. (2019) in a study performed in Surabaya reported that the average SLAM score of SLE inpatients was 29.3±3.9. The mean was higher, probably because the study involved only active SLE patients as subjects.²³

It is noteworthy that the interrelation of the activity of SLE with 25(OH)D serum levels has not demonstrated uniformity across all observations. Several studies reported negative correlations,^24-26 while others found no correlation.^27,28

In this study, the interrelation between the activity of SLE with 25(OH)D serum levels was evaluated using the SLAM scores, with a strong correlation strength of (p <0.05; r = -0.661). The results are in line with Amital et al. (2010) and Mok et al. (2012). Based on the SLEDAI scores (p <0.05), Amital et al.reported an inverse correlation between interrelation of the activity of SLE with 25(OH)D serum levels. Meanwhile, Mok et al. (2012) indicated a significant inverse interrelation of the activity of SLE with 25(OH)D serum levels (p <0.05).^29-30

Mok et al. (2012) highlighted the role of low 25(OH)D serum levels in assessing both renal and extra-renal activity in Systemic Lupus Erythematosus (SLE). Their discovery revealed that in detecting renal SLE activity, low 25(OH)D serum levels demonstrate greater specificity while showing reduced sensitivity when compared to anti-dsDNA. In particular, the sensitivity and specificity reported for detecting renal SLE activity with 25(OH)D serum levels below 15 ng/mL were 0.44 and 0.78, respectively.^30-35

In this study, laboratory tests were carried out as mentioned in the 1997 ACR criteria and SLAM score, and some of the parameters examined correlated with SLE activity. The analysis results indicated that LED and anti-ds-DNA were not correlated to the SLAM score, CRP was correlated, while C3 and C4 were negatively correlated to SLAM scores. Contrary to findings in Australia and Egypt, this study did not establish aninterrelationof LED with25(OH)Dserum levels (r = -0.115; p = 0.481) or SLE activity (r = 0.149; p = 0.357). These results differ from studies reporting a significant inverse interrelation of 25(OH)D serum levels with LED.^36,37 Other studies describe different conditions where there is a significant relationship between increased LED and high SLE activity based on the BILAG score.^38-41

Additionally, 25(OH)D serum levels interrelated with CRP results in this study (r = -0.414; p = 0.008). This finding aligns with a study by Emam et al. (2014) in Egypt, revealing a significant inverse correlation between 25(OH)D serum levels and CRP (r = -0.55, P = 0.013).^34,42

In this study, the results of C3 and C4 significantly and negatively interrelated with the activity of SLE. These results are consistent with Nasiri et al. (2009), Narayanan et al. (2011), and Bahlas and Damiati (2014), which obtained a value of p <0.05.^33,35,36Furthermore, C3 and C4 levels significantlyinterrelated with 25(OH)D serum levels, supporting the findings of Alnaggar et al. (2019).^43-45

The results indicate that anti-ds-DNA did not exhibit a significant interrelation of the activity of SLE with 25(OH)D serum levels. Prior studies have shown inconsistent outcomes, with some reporting a significant negative interrelationof anti-dsDNA with 25(OH)D serum levels (r= -0.13; p= 0.02).^46-48A a study conducted in Egypt by Emam et al. (2014) revealed a significant inverse interrelation between 25(OH)D serum levels and anti-dsDNA (r= −0.64, P= 0.04).^34,49,50Similarly, Narayanan et al. (2011) found a significant and positive correlation between SLEDAI scores and anti-dsDNA levels in India.^35,51-53

CONCLUSION:

This study identifies hypovitaminosis D in SLE patients, with results indicating that the activity of SLE significantly and negatively correlates with 25(OH)D serum levels assessed by SLAM scores. Further research needs to be carried out using appropriate research methods, for example, a cohort study to determine the interrelation of the activity of SLE with 25(OH)D serum levels to assess changes and compare remission, active, and inactive states.

CONFLICT OF INTEREST:

The authors declare that there is no conflict of interest.

FUNDING SOURCE:

This study was funded by the Faculty Excellence Research Program– Airlangga University 2019.

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Received on 20.08.2023 Revised on 15.04.2024

Accepted on 24.09.2024 Published on 24.12.2024

Available online from December 27, 2024

Research J. Pharmacy and Technology. 2024;17(12):5773-5778.

DOI: 10.52711/0974-360X.2024.00878

Indicator		Total (n = 40)
Indicator	n (%)	Mean ± SD	Median	Min	Maks
Gender
Male Female	0 (0) 40 (100)
Age (years)		27.43 ± 8.65
BMI (kg/m²)		21.69 ± 2.71
Hemoglobin (gr/dl)			10.05	2.3	14.1
Leukocytes (cell/mm3)			8030	2,420	21,990
Lymphocytes (cell/mm3)			1490	240	6,400
Platelets (cell/mm3)		22,46.25 ± 11,65.83
ESR (mm/hour)		36.75 ± 20.44
CRP (mg/dl)			0.50	0.01	14.00
C3 (mg/dl)			54.80	16.40	144.00
C4 (mg/dl)			22.45	3.00	90.6
Anti-dsDNA (IU/ml)			95.10	10.00	2,779.70