Impact of coronavirus disease 2019 (COVID-19) pandemic on attitude, behavior, and mental health of patients with rheumatic diseases

Background The coronavirus disease 2019 (COVID-19) pandemic has become a global health, social, and economic crisis. Healthcare professionals, patients, healthy individuals, and the whole community are under inevitable psychological pressure which may cause different psychological problems as fear, anxiety, depression, and insomnia. The aim was to assess the impact of the COVID19 pandemic on the attitude, behavior, and mental health of rheumatic patients and to compare them with healthy individuals. This is a case-control study, 360 participants were included and divided into a patient group composed of 180 patients with rheumatic diseases, and a control group composed of 180 healthy people. Data were collected via a self-administered structured questionnaire designed on Google forms. It was sent to participants via social networks and emails to different rheumatic patients and healthy individuals. Mental health was measured by the 5-item Brief Symptom Rating Scale (BSRS-5). Results The mean age of cases and control were (35.05 ± 8.79 vs 34.56 ± 9.06) years. In comparing attitudes and behavior toward COVID 19, there was a statistically significant difference (p ≤ 0.05) between both groups regarding washing hands, going outdoors, wearing masks and gloves outdoors, and staying in their rooms. Patients depended mainly on telehealth more than usual where about 50% used either phone calls, internet or sent their relatives to their physicians; moreover, 20% did not contact their physicians at all the past few months. There was a statistically significant difference (p ≤ 0.05) between both groups regarding feeling angry/irritated, inferior and insomniac. The BSRS-5 total score and being defined as a psychiatric case (according to the BSRS-5 scale) also differed significantly between patients and controls. Systemic lupus erythematosus (SLE) patients showed more adherence to their medications and stayed mostly at home and they have higher BSRS scores. Conclusion Patients with rheumatic diseases show comparable degrees of anxiety and depression to healthy individuals, but higher distress symptoms and panic in the form of anger, irritability, and insomnia. They have a significantly higher sense of inferiority and a higher total BSRS compared to controls. SLE patients show more adherence to their medications and stay mostly at home as a reflection of feeling more vulnerable. Moreover, they have higher degrees of psychological affection in the form of higher BSRS scores. Abandoning drug purchasing without medical prescription is necessary in Egypt to protect our patients from unnecessary drug shortages adding to their fear and anxiety. Mental health should be addressed in the same manner we deal with the infectious disease itself, being of no less importance. Mental health professionals, social workers, and support groups need to provide psychological support to vulnerable populations, including patients with rheumatic diseases. Rheumatologists should be aware of the need for psychiatric consultation for their patients whenever necessary.


Background
The corona virus disease 2019 (COVID- 19) is an infectious disease caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which originated in Wuhan, China, in early December 2019 and declared a pandemic by the World Health Organization (WHO) on 11 March 2020 [1,2]. Previous data from similar outbreaks, such as the Severe Acute Respiratory Syndrome [SARS], showed that the community suffered considerable anxiety, depression, and panic, resulting in a significant psychological impact [3][4][5].
The mortality of COVID-19 is even higher than previous epidemics inducing profound fear [6,7]; mental health reflections can last longer and even have a higher frequency than the epidemic itself [8,9]. Shortages of masks and health equipment, quarantine, lack of effective treatment, closure of schools and public places, boredom, fear of infection, or death could increase panic. Moreover, it can lead to a feeling of insecurity due to economic and social losses [10][11][12][13][14].
Patients with rheumatic diseases-those suffering from rheumatoid arthritis, systemic lupus, scleroderma, ankylosing spondylitis, Sjogren's disease, inflammatory myositis, fibromyalgia, or others-are considered at greater risk both due to their chronic illnesses and use of immunosuppressive drugs [15]. They are also facing many issues-drug shortages, difficulties reaching clinics or hospitals, and hazards of physical inactivity staying at home. It is expected that these individuals with chronic diseases will be prone to higher levels of impaired psychology [16] since the COVID-19 tends to hit hardest those with multiple comorbidities [17]. The American College of Rheumatology [ACR] Issues COVID-19 Treatment Guidance for Rheumatic Disease Patients recommended the reduction of the number of health care encounters; laboratory monitoring less frequently, using telehealth, and increasing intervals between intravenous doses and they set the basis for when to start, stop, or reduce medications [18].
A recent public survey conducted in China about the psychological impact of the COVID-19 outbreak showed that about a third of participants experienced moderate to severe anxiety and about half experienced moderate to severe psychological impairment [19]. No previous researches studied the psychological impact of COVID-19 on patients with rheumatic diseases in Egypt. This present study represents the first mental health survey conducted in Egypt addressing this vulnerable population. From this point we aimed to assess the impact of  pandemic on the attitude, behavior, and mental health of patients with rheumatic disease and to compare them with healthy individuals.

The study design
This is an Egyptian case-control study, sample size was calculated based on findings from the pilot study prevalence among cases 17% and prevalence among control 40% case to control 1:1. A total of 360 participants were included consecutively in this study and divided into two groups: a patient group composed of 180 patients with rheumatic diseases and a control group composed of 180 healthy individuals. Rheumatic patients and healthy individuals had been recruited from 14 to 29 April 2020. Data were collected via a self-administered structured questionnaire that were delivered as a Google form in Arabic, which were sent to participants via social networks targeting rheumatic patients and healthy individuals, or via emails. The survey was translated into Arabic [mother tongue of Egyptians] and validated by the authors. It took about 5-10 min to be completed. The participants' information is kept anonymous. The translated form is available in the supplemental files. All control subjects were age, sex, socio-economically, and geographically matched with the patients [living allover Egypt those educated enough to use social media and internet]. The study complied with the Declaration of Helsinki, and informed online consent has been obtained graded as a Likert-type scale "never," "a bit of the time/few times," "most of the time", and "always" based on the question. 6. Eight questions for rheumatic patients only about: contact with the physician, the means and causes of contact and their feeling afterward, their attitude towards immunosuppressive drugs. 7. Six questions for mental health assessment for patients and controls: Mental health was measured by the 5-item Brief Symptom Rating Scale  which was derived from the 50-item BSRS [20]. This effective screening instrument has satisfactory reliability and validity and is widely used to identify psychiatric impairment in medical settings and community samples [20][21][22]. The scale was translated and back-translated to Arabic language and a pilot study was conducted to test the applicability and the clarity of the scale then changes were made accordingly. The score for each item ranges from 0 to 4 [0, not at all; 1, a little bit; 2, moderately; 3, quite a bit; and 4, extremely], based on a 5-point Likert-type scale, participants were asked to indicate how much discomfort they experienced that was caused by a particular symptom in the past week [including the current day]. The sum of the scores across the five items represented the total score of the BSRS-5 and ranged from 0 to 20. A total score on the BSRS-5 above 14 may indicate a severe mood disorder. Scores between 10 and 14 may indicate moderate mood disorders, and those between 6 and 9 could indicate mild mood disorders. A cut-off score of ≥ 6 was considered as a BRSR-5 defined psychiatric case [20].

Statistical analysis
The collected data were statistically analyzed using the Statistical Package for Social Science software [SPSS] [Version 20.0. Armonk, NY: IBM Corp.]. Continuous variables with a normal distribution were reported as mean and standard deviation [SD]. Categorical variables were summarized as frequencies and percentages. Quantitative data were evaluated using Independent t test or one-way ANOVA, which were suitable for normally distributed data, while qualitative data were evaluated by chi-square test [χ2] or Fisher's exact test. p values ≤ 0.05* and ≤ 0.001** were considered statistically significant and highly statistically significant, respectively.

Results
Socio-demographic and personal characteristics of the studied groups showed that there was no statistically significant difference [p > 0.05] between both groups; ensuring their comparability.  (Table 1).
On comparing attitude and behavior toward COVID-19 pandemic among the studied groups, no statistically significant difference [p > 0.05] was found between patients and the control group regarding their belief that staying at home protects them from infection, healthy diet and exercises help, and frequent washing hands, while there was a statistically significant difference [p ≤ 0.05] between both groups regarding their behavior regarding washing hands, going outdoors, wearing masks and gloves outdoors, and staying in their room (Table  2).
Mental health comparison among the studied groups showed that no statistically significant difference [p > 0.05] was found between the patients and control groups regarding anxiety and depression, while there was a statistically significant difference [p ≤ 0.05] between both groups regarding feeling angry/irritated, inferior, and insomniac. BSRS-5 total score and being defined as a psychiatric case according to BSRS-5 scale was significantly higher in patients (Table 3).
Regarding patients, attitude, and behavior towards their illness, medications, and medical advice, the highest proportion of them answered that they felt at higher risk and they felt no change in their disease activity; however, they believed that fear may increase disease activity. They contacted their physicians less than usual, mainly using the internet. They mainly asked for medication advice and most of them still felt non-assured after communication. Most of them had no fears about drugs, did not reduce doses/stop drugs, and many experienced drug shortages (Table 4).
On assessing the relationship between different parameters and patients' mental health degree, there was no statistically significant association [p > 0.05] between the degree of impaired mental health and all studied parameters except for "feeling at risk more than other" where there was a statistically significant association [p ≤ 0.05] where their feeling of "being at risk" was associated with a higher degree of impaired mental health [BSRS-5 ≥ 6] (Tables 5 and 6).
Comparison between patients with rheumatoid arthritis (RA), systemic lupus erythematosus (SLE), and other rheumatic diseases regarding different parameters showed that there was a statistically significant difference [p ≤ 0.05] between them as regards age, sex, their belief that a healthy diet and exercises may help, frequency of going outdoors, BSRS-5 total score, being at risk, their feeling after communication, stopping drugs and experiencing drug shortages. RA patients had higher mean age and a higher percent of the male sex, they believe that a healthy diet and exercises can help, they go out only for necessities, they feel "maybe/not at risk", they feel less/the same anxiety and fear after communicating with their physicians, they are less adherent to some drugs and experience more drug shortages. SLE patients had a higher percentage of the female sex, they believe a healthy diet and exercises "maybe/not help," mostly "never go outdoors," they feel "yes at risk," feel more/the same anxiety, and fear after communication, and most do not stop drugs. Patients with other rheumatic diseases had higher mean BSRS-5 a total score and mostly "go outdoors freely any time," feel "not at risk," and experienced no drug shortage.     Also, comparing between patients with RA and SLE only, a statistically significant difference [p ≤ 0.05] was found among them as regards some parameters. RA patients had higher mean age, lower mean BSRS-5 total score, and a higher percentage of the male sex, "yes healthy diet and exercises help," feel "not at all/quite a bit inferiority," feel "maybe/not at risk," feel less anxiety and fear after communication, and stopped drugs more often.

Discussion
COVID-19 pandemic has affected people's lives in many different aspects. The fact that neither vaccine nor confirmed effective treatment has been developed has made the Coronavirus a huge stressor and a fearful threat to many individuals [23]. With COVID-19, the social isolation, quarantine, and loneliness in addition to fear of infection or death were the main factors impacting not only those infected with COVID but also the general population. The resulting fears, although considered a usual response to this major threatening event, when chronic and profound becomes harmful and may lead to psychiatric illness [24,25].
Health professionals, including doctors and nurses, being the most at risk, suffered impaired mental health [26,27]. Special population groups who are considered more vulnerable to infection-old age, immunecompromised, and patients with chronic illnesses-frequently complained of considerable psychological problems [7]. The "double crush" of having a chronic illness and receiving immunosuppressive drugs makes patients with rheumatic diseases among these groups more vulnerable to infection and thus impaired mental health.
Most patients were non-smokers and the majority had no previous lung affection. However, smokers and those with lung affection did not seem to have a different attitude or behavior regarding being at a greater risk, most probably due to the fact that most patients with chronic diseases had comparable degrees of anxiety. When comparing the attitude and behavior towards COVID among the studied groups, no statistically significant difference was found between cases and control group regarding their attitude towards staying at home, the value of a healthy diet and exercises and washing hands; while there was a statistically significant difference between both groups regarding going outdoors, also, wearing masks and gloves outdoors, where patients seemed to be more selfprotecting. Self-isolation in their room most of the time was mostly practiced by patients more than controls.
Previous studies have shown that mental health disorders can last longer than the epidemic itself [8,9]. Individuals with chronic illnesses are even more exposed to psychological impairment [16,17]. Mental health comparison among the studied groups using the BSRS showed that there was a statistically significant difference between both groups regarding "feeling angry/irritated," "feeling inferior to others," insomnia, and regarding the BSRS total score. Out of all patients, 85.6% were defined as a psychiatric case. Their belief of "being at risk" was associated with a higher degree of impaired mental health [BSRS-5 ≥ 6]. These distress reactions [feeling angry, irritable, and disturbed sleep] being more  prominent in cases denote fear and panic. About 20% were "extremely" angry and agitated. Moreover, cases were feeling more inferior, which is most probably related to their chronic illness. Ironically, no significant difference was found regarding anxiety and depression between cases and controls denoting that the general population during the pandemic felt similar degrees of anxiety and depression. Fear of infection or death raises anxiety levels in healthy individuals as well, quarantine and social isolation increased depression in both groups similarly. Both patients and healthy feared mostly losing their families and beloved ones.
Regarding the attitude and behavior of the cases towards medications; the highest proportion of them answered that they have no fear of drugs, they did not reduce doses, nor did they stop any of their drugs. Those who stopped drugs may have had financial issues or difficulty finding medications. This is a good positive attitude consistent with the EULAR guidelines regarding medications, representing their awareness of the necessity of continuing their medications to avoid flares [28]. Moreover, many of them did not experience any increase in their disease activity, although many believed that fear itself may cause a flare. The most frequent cause to contact their physician was medication advice rather than consultation due to pain and disease activity. The increased usage of antimalarial drugs to treat COVID-19 patients caused a decline in their availability in pharmacies, highlighting the harm to patients caused by medications being purchased in Egypt without medical prescription [29]. For some patients, this might be an essential treatment especially for those with SLE, and many had to communicate with their physicians for substitutes. During the pandemic, most of the patients visited their physicians less than usual to minimize going outdoors to healthcare facilities; they mostly contacted them using telehealth.
Regarding the comparison between patients with RA, SLE, and other rheumatic diseases, RA patients had higher mean age and a higher percent of the male sex, while SLE patients were mostly younger females. Most RA patients believe that a healthy diet and exercise can help combat infection while SLE patients are less confident about that. RA patients only go out for necessities while most SLE patients never go outdoors as they felt that they are at risk more than other patients. They even feel more/the-same anxiety and fear after communicating with their physicians. Most of SLE patients are adherent to their drugs more than other patients. We conclude that although rheumatologists succeeded to convince their patients to stick to their medications, they failed to relieve their anxiety and fear which may be augmented by media, following numbers of those COVIDinfected and dead. About 48% depended on social media as a source of information about COVID-19. Both RA patients and SLE patients experienced drug shortages. Most patients with other rheumatic diseases go outdoors more freely, they do not feel great that they are at a higher risk like SLE patients nor do they significantly complain of drug shortages as they are less dependent on anti-malarials unlike SLE patients.
Regarding their mental status RA patients had significantly lower mean BSRS-5 total score and felt less inferiority than SLE patients. No significant difference was found in patients with different diseases regarding anxiety and depression. Although cases were significantly different regarding anger and insomnia compared to controls, there were no differences comparing patients with different disease categories.
The limitations of our study were the inability to assess the same patients' psychological status just before the hit of coronavirus, an unexpected event, which would have been more informative about the direct impact of COVID-19 pandemic isolated from the effect of their chronic illnesses which had been also accused to affect mental health [30,31]. The finding that mental health status was more affected by their belief of "being at risk" of infection was a clear indicator of the impact of COVID-19 pandemic. The presented data are preliminary data that could be obtained during the quarantine period and we are planning for future studies to test behavioral changes on rheumatic patients that had suffered from COVID-19 infection. Another limitation is recruiting patients who use social media with no inclusion of patients not using it as illiterate patients and patients from

Conclusion
Patients with rheumatic diseases show comparable degrees of anxiety and depression to healthy individuals, but higher distress symptoms and panic in the form of anger, irritability, and insomnia. They have a significantly higher sense of inferiority and a higher total BSRS compared to controls. SLE patients show more adherence to their medications and stay mostly at home as a reflection of feeling more vulnerable. Moreover, they have higher degrees of psychological affection in the form of higher BSRS scores. Abandoning drug purchasing without medical prescription is necessary in Egypt to protect our patients from unnecessary drug shortages adding to their fear and anxiety. Mental health should be addressed in the same manner we deal with the infectious disease itself, being of no less importance. Mental health professionals, social workers, and support groups need to provide psychological support to vulnerable populations, including patients with rheumatic diseases.
Rheumatologists should be aware of the need for psychiatric consultation for their patients whenever necessary.