Introduction
Systemic lupus erythematosus (SLE) is a systemic autoimmune disease that is associated with multiple organ involvement and leads to significant morbidity and mortality. One of the important environmental factors that influences exacerbations of SLE is ultraviolet (UV) radiation [
1].
UV radiation induces the release of inflammatory chemokines and cytokines, which in turn recruit inflammatory cells. UV radiation also induces necrosis and apoptosis of keratinocytes, which leads to an accumulation of nucleic acids. When the nucleic acids combine with autoantibodies, plasmacytoid dendritic cells are activated. This leads to the production of interferon-alpha and the activation of auto-reactive T-cells. Interferon-alpha subsequently induces the production of more inflammatory chemokines and cytokines, which causes an amplification cycle of inflammation [
2]. Therefore, photoprotection from the sun to reduce UV radiation exposure can effectively prevent a lupus flare, esp. in the cutaneous lupus erythematous, and is an essential component of SLE treatment [
3,
4].
Studies conducted in adults with cutaneous lupus erythematosus (CLE), which is a patient population that is particularly sensitive to UV radiation, reported a significant deficiency in the use of photoprotection [
5], and only a minority of CLE patients reported consistently wearing sunscreen [
6]. A study in adults with SLE found that the majority of patients had good photoprotection awareness. However, they did not translate into better photoprotection practices or better disease activity [
7]. These findings are in contrast to those from a previous study that reported that patients who regularly used sunscreen had a better clinical outcome [
8].
Effective photoprotection in children requires multiple modalities of patient and parent/caregiver cooperation, which may be difficult to achieve in real-life practice [
9]. Children’s behavior is influenced by their age and development. Moreover, children and adolescents have different activities, risk behaviors, and types of recreation compared to adults, and these factors can also increase their exposure to UV radiation [
10,
11]. Another important factor is that the effect of UV radiation is more pronounced in children than in adults as children have a lower concentration of protective melanin and a thinner stratum corneum [
12].
Biologically active vitamin D is formed in the skin after exposure to UV radiation [
13]. Photoprotection can lead to vitamin D deficiency [
14] and may contribute to the progression of active SLE disease due to the importance of vitamin D in regulating the immune response [
15].
The aims of this study were to evaluate the accuracy and adequacy of photoprotection in pediatric SLE patients, and the effect of education on photoprotection. The secondary objectives were to examine the association between photoprotection and SLE disease activity. and to investigate the effect of photoprotection on serum vitamin D level.
Discussion
Although the relationship between UV radiation and SLE is well evidenced [
1], photoprotection could be inadequately practiced. To improve our understanding of the photoprotection of SLE children, we enrolled 100 SLE patients aged ≤ 18 years. The photoprotection questionnaire and status of disease activity were collected and compared from baseline to the ≥ 3-month follow-up time point. Photoprotection education was provided. We found that the majority of patients were practicing photoprotection but not accurately in some areas. Education on photoprotection was effective There were no associations between photoprotection and SLE disease activity or serum vitamin D level.
Compared to the first assessment where 79% of patients used sunscreen, our second assessment showed an improvement of 92% rate of using sunscreen. The rate of sunscreen use is higher compared to the adult studies from Abdul Kadir et. al (52.3%) [
7] and Chanprapaph et al.(63.5%) [
25] but is approximately close to another study in children in Thailand (95.8%) [
26]. This may be because Thai families place value on family connections and close parent–child relationships. Children tend to be more dependent on parents, especially for health and self-care. Thus, our patients were constantly reminded by their parents to use sunscreen or even had their parents apply sunscreen for them.
At the first assessment, the main reason for not applying sunscreen was that our patient thought it was unnecessary. These patients thought that if they stayed indoors or used physical photoprotection then they did not need to apply sunscreen. This underlines the need to counsel patients with SLE that optimal photoprotection requires daily sunscreen application. At the second assessment, the main reason for not using sunscreen switched from thinking it was unnecessary to disliking its texture. This reason is in line with a study from Malaysia, a tropical country with hot climate that makes sunscreen greasier, similar to Thailand [
7]. This is in contrast with a study from the USA in which the inherent features of sunscreens was the third common reason for not using sunscreen [
6]. This reason can be diminished by improving the texture of sunscreen.
The recommended amount of sunscreen use is 2 mg/cm [
2] which is difficult to achieve in real life practice. As a result, a fingertip unit or teaspoon unit has been recommended [
23,
27]. We found that at the first assessment, a majority of the patients applied sunscreen less than the recommended amount, which is in line with previous studies in SLE patients [
7,
26] and in the general population [
28,
29]. An inadequate amount of applied sunscreen significantly decreases its efficacy [
30]. Therefore, the patients need to be instructed as to the correct application and amount of sunscreen.
The facial anatomical sites to which sunscreen was covered least often were the ears, hairline and periorbital areas. These findings are in line with the study of Loesch et al. [
31] In the study, the authors stated that the reasons that the subjects did not apply sunscreen at the hairline and periorbital areas as it would grease their hair and sting their eyes. These reasons could be similar for our patients and such obstacles could be addressed if the sunscreen texture were improved. Interestingly, our study was conducted during the COVID-19 pandemic when wearing a mask was mandatory. However, the majority of patients still applied sunscreen at under the mask areas. The least and second least anatomical body sites to which sunscreen was covered were the dorsum of the feet and dorsum of the hands, respectively. These mentioned areas should be specifically emphasized to apply sunscreen on. Sunscreen application on the dorsum of the feet was not significantly increased at the second assessment. This was likely due to Thai students being required to wear socks as a part of their school uniform. Therefore, patients were unlikely to consider this area to be exposed to the sun.
The least often practiced sun protection behavior was wearing sunglasses which was not improved at the second assessment after education on photoprotection. Although Thailand is a middle-income country, the distribution of poverty is uneven across the regions with the poverty rate in the Northeast almost double the national level, which is where our hospital is based [
32]. Standardized sunglasses can be costly and are not affordable for our patients. As demonstrated in our study, after patients were educated that wearing sunglasses was one aspect of photoprotection, the patients who continued to rarely/never wear sunglasses as shown at the second assessment had significantly lower household income than the rest of the patients. This indicates that education could not improve behaviors around wearing sunglasses if the family could still not afford them. This socioeconomic reason was confirmed by another study from Thailand which found that sunglasses were more frequently used in patients with a higher family income [
26].
During 6:00 am to 10:00 am, the most frequently reported activities engaged in during sun exposure were travelling to school and attending the national flag ceremony. The majority of our patients travelled to school by motorcycles which is the most used vehicle in Thailand as it is less-expensive and more convenient compare to other automobiles. Unfortunately, only 43% of people in Thailand wear helmets—52% of drivers and 20% of passengers [
33]. Moreover, child motorcycle helmets with UV-resistant visors, are simply not affordable, as 43% of our patients had an average household income less than the sustainable living wage [
34]. As a result, our patients are at risk of both head injury and UV exposure. In Thailand, there is a unique activity engaging in sun exposure which is the morning national flag ceremony. The students will line up at the school grounds, which are mostly outdoor and uncovered to sing national anthems. After that, the teachers will inform about important issues. The activity takes about 30 min. The activity starts at 8 am but the UV index can be not low during a sunny day. In the authors’ experiences even though our patients know to avoid this activity, they still would like to attend as they don’t want to be seen as weak students. Therefore, it is important that the physicians should formally inform their patients’ schools regarding the need to avoid sun exposure.
The most often reported activities during 10:01 am to 4:00 pm, which is during the peak UV index, were playing with friends and walking to the cafeterias. Playing with friends is crucial in enhancing development. However, school facilities may not be feasible for indoor recreation activities. In addition, some schools in Thailand have cafeterias in different buildings. Thus, these patients need to use physical photoprotection i.e. hat, umbrella or long-sleeve shirts. In the authors’ experiences, these are difficult to practice especially in our teenage patients as it makes them feel alienated from their peers.
Thailand is an agricultural country in which farming household plays an important role. Some of our patients had to help with outdoor chores such as helping in the farm fields, taking care of cattle, rubber tapping and going to the market/grocery store. Fortunately, most of the outdoor chores are done before or after school when the intensity of UV radiation is lower.
The number of patients exposed to the sun was not significantly decreased in all time periods at the second assessment. This was due to socioeconomic status which could not be changed by education alone i.e. the patients still had to travel by motorcycle and help with outdoor chores.
Education on photoprotection was effective in improving photoprotection practices, including applying an adequate amount of sunscreen and using lip balm with sunscreen, which were behaviors practiced among only a minority of our patients at the first assessment. Moreover, the reason for not using sunscreen was changed from thinking it was unnecessary to disliking its texture at the second assessment. Therefore, these aspects should be vigorously emphasized. Although using water resistant sunscreen, reapplying sunscreen when sweating/doing outdoor activities, applying sunscreen to commonly missed areas, wearing sunglasses, and avoiding sun exposure were not improved by the second assessment, these areas should still be emphasized, esp. in populations with different contexts from our patients, e.g., people who have better access to a pleasant texture of sunscreen or affordable water-resistant sunscreen, people with more flexible break times to reapply sunscreen, those with different or no school uniforms, or those of a higher socioeconomic status. Written and verbal patient education on photoprotection should be given at the diagnosis point and periodically reviewed. As at the first diagnosis point, the seriousness of SLE and information regarding the disease can be overwhelming. Physicians should update their knowledge regarding photoprotection as there are still some knowledge gaps even in subspecialists [
35].
There was no direct association between photoprotection and SLE disease activity which is similar to a previous study [
7] in which good photoprotection practice was not a predictor of disease activity. Our finding is in contrast with Vilá et al. [
8] who found that patients that regularly used sunscreen had significantly lower renal involvement, thrombocytopenia, hospitalizations, and requirement of cyclophosphamide treatment than patients who did not use sunscreen. However, the study was a cross-sectional study and evaluated clinical outcomes by reviewing medical records. One of the main reasons behind this negative finding is that UV has more direct effects on cutaneous lupus than it does on systemic disease [
36]. In addition, only one-third of our patients had cutaneous lupus, and their CLASI scores were low to begin with. Moreover, the other factors could affect the disease activity of SLE and not UV radiation exposure alone. These factors include but are not limited to medications [
37], infection [
38], tobacco smoke and diet [
39].
We found no effect of intensification of photoprotection on serum vitamin D levels, which contradicts previous studies [
14,
40]. The reason could be that we routinely check the serum vitamin D levels at the diagnosis of SLE and every 3 months until levels are normal. Therefore, only a minority of our patients had an abnormal serum vitamin D level. Moreover, the vitamin D pathway requires UV-B exposure in the skin, and SPF30 blocks 97% of it [
41]. Seventy-nine percent of our patients used sunscreen of SPF30 and above on initial assessment. Thus, the change in vitamin D level was too small to reach statistical significance. Considering that photoprotection should be adequately practiced without a risk of vitamin D deficiency, monitoring serum vitamin D levels and vitamin D supplements should be routinely practiced as per recommendations [
42,
43].
This study has some mentionable limitations. Patient responses to the items in the study questionnaire may not accurately reflect the real-life photoprotection since it is known that questionnaire respondents are sometimes inclined toward responding more favorably than is actually true to avoid a loss of credibility and to please their physicians. However, study patients completed the questionnaire privately apart from their subspecialists, and the completed questionnaire was immediately collected by a research assistant. Moreover, the patient questionnaire responses were not evaluated by the research team until the end of the study to reduce the probability of assessment bias. Importantly, the fact that some patients reported inadequate photoprotection on both the baseline and follow-up the photoprotection questionnaires suggests the veracity of the answers to the questionnaire items.
The strengths of this study are the comprehensive evaluation of the practical aspects of photoprotection. The study was also prospectively conducted in a tropical country with a high UV index all year round [
44] and a unique culture and socioeconomic structure. In addition, our study was conducted in the pediatric population in which the data is still scarce. To the best of our knowledge, this is the first study that prospectively conduct to evaluate photoprotection and the effect of education in pediatric SLE patients.
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