Introduction

Rheumatic autoimmune diseases are associated with a myriad of comorbidities [1]. Ischemic heart disease, heart failure, cerebrovascular disease, and peripheral arterial disease are important due to their morbimortality [2]. Rheumatoid arthritis (RA) entails an increased prevalence of cardiovascular traditional risk factors, including hypertension, diabetes, smoking, obesity, and dyslipidemia [3]. Additionally, the risk of ischemic heart disease is 5- to eightfold higher in patients with systemic lupus erythematosus (SLE) and 2- to threefold higher in RA than in the general population [4, 5].

The coronavirus disease 2019 (COVID-19) pandemic greatly impacted the world population in many aspects, including personal relationships, work, education, and health. Isolation, quarantine, and the home office impacted lifestyle, becoming a public health challenge [6] with these strategies increasing sitting and screen time [7]. Mental health disorders, such as major depression and anxiety, also increased. The most affected populations were women and young people [8]. The greater increase among females was anticipated because women were more likely affected by the social and economic consequences of the pandemic [9].

Patients with rheumatic autoimmune diseases, such as rheumatoid arthritis and systemic lupus erythematosus, had to face several additional challenges besides COVID-19 infection. These people suffered changes in their medical care, from the availability of qualified rheumatologists to a telemedicine implementation. Unemployment, decreased physical activity, social isolation, and a lack of access to certain medications, including hydroxychloroquine, were other issues they faced [10].

Social isolation measurements applied in many countries have influenced rheumatic patients’ health. A decrease in physical activity predisposes an increase in disease activity and flares [11, 12]. Isolation from family and friends could mean denying patient’s emotional support, increasing the risk of depression and anxiety [13], and unhealthy eating behaviors, such as increased snacking and consumption of comfort foods [14,15,16]. At the same time, these actions could lead to an increase in their body weight, and therefore, overweight and obesity. This review summarizes the impact of the COVID-19 pandemic on cardiovascular risk factors and comorbidities in patients with rheumatic autoimmune diseases (Table 1). Since there is a lack of data about changes in comorbidities during the lockdown, we focused on the most relevant of these, for which there is more information, RA and SLE.

Table 1 Summary of information available on cardiovascular risk factors and comorbidities in patients with RA and SLE

Methods

A review of the literature was conducted analyzing the published data about cardiovascular health and its changes in patients with autoimmune rheumatological diseases (particularly RA and SLE) during the COVID-19 pandemic.

Eligibility criteria

It was included articles that contained information on risk factors and comorbidities in general population and patients with rheumatologic diseases before and during the COVID-19 pandemic, in addition to articles that report definitions. It was excluded those did not have information on risk factors and comorbidities of our interest.

Search strategies

Searches on the impact of comorbidities in patients with rheumatoid arthritis and systemic lupus erythematosus were carried out in MEDLINE/PubMed and Scopus from August to December 2022. The keywords used for the search were “rheumatoid arthritis” and “systemic lupus erythematosus” in combination with other keywords such as “COVID-19,” “lockdown,” “comorbidities,” “cardiovascular risk factors,” “pandemic,” “diabetes,” “hypertension,” “dyslipidemia,” “alcohol intake,” “obesity,” “sedentarism,” “diet,” “depression,” “anxiety,” and “smoking.”

Study selection

Four reviewers screened the title and abstract of retrieved records. Potentially eligible reports were then reviewed in full text. Differences were reconciled by either consensus or discussion with an external reviewer.

Risk factors and unhealthy behavior during the COVID-19 pandemic

Sedentarism

Physical activity (PA) is defined as any bodily movement produced by the skeletal muscles that result in energy expenditure above resting (basal) levels [26]. An increase in PA is an intervention that can significantly improve many different disease-related symptoms such as fatigue, functional disability, inflammation, and systemic outcomes (cardiovascular disease risk and body composition) [27]. PA has health benefits for people with rheumatic diseases, and the European Alliance of Associations for Rheumatology (EULAR) recommends exercises in the four domains (cardiorespiratory fitness, muscle strength, flexibility, and neuromotor performance) [28]. In one study, it was shown that after 24 weeks of exercise, subjects had better total cholesterol and triglyceride levels, decreased fat tissue and blood pressure, lower serum levels of proinflammatory C reactive protein (CRP), and higher levels of high-density lipoprotein (HDL) [29]. The COVID-19 pandemic caused many lifestyle changes in the population with chronic health conditions [30], including rheumatic diseases. In addition, the reduction in PA led patients to increased sarcopenia and the deterioration of muscle strength and function more frequently in older populations [31]. During the pandemic, PA was reduced by as much as 56.8%, mostly due to fear of infection, as reported by Saxena et al., and thus, quality of life and disease activity were affected [32].

Researchers around the world have reported sedentary behavior findings during the quarantine. In France, Deschasaux-Tanguy et al. reported that 63.2% of the participants increased sedentary time with an average of 7 h per day spent sitting [33] similar to a study in Europe, North Africa, Western Asia, and the Americas, where the most notable change in the population was a 28.6% increase in the hours per day sitting [34], mostly increased screen time [35], especially TV-viewing. In a comparison of pre-COVID-19 and during the COVID-19 pandemic, people spending more than 5 h per day in front of a screen increased from 14.6 to 37.5%, respectively [36]. PA in patients with RA and SLE is less frequent due to the discomfort caused at the beginning of exercise, even considering the previously described benefits.

Alcohol

A systematic review showed that alcohol drinking remained stable in most of the population examined. However, an important part of the sample increased consumption during the early stages of the pandemic, with a decreasing trend at the end of the lockdown [37]. Those motivated to drink alcohol to cope had a greater increase in consumption [38]. In the same way, a cross-sectional study conducted in seven European countries with 1800 patients with rheumatic diseases (REUMAVID study) showed that most drank the same amount of alcohol. Still, a significant percentage (18.2%) increased their consumption [17].

Consequences of alcohol abuse include increased cardiovascular risk (CVR) and liver disease. It also influences the innate and adaptative immune system. In RA, it is important to consider that alcohol consumption increases the risk of developing a liver injury induced by treatment with methotrexate (MTX). Alcohol added to folate deficiency, the administration of other hepatotoxic drugs and lipid disorders predispose to MTX-induced steatohepatitis and hepatic fibrosis [39]. Several observational studies have investigated the potential relationship between alcohol intake and the risk of rheumatic diseases. One suggested that ethanol and antioxidants in alcohol could suppress the immune response and trigger proinflammatory cytokines, which may play an important role in the risk of RA or SLE [40]. Other emerging studies associate moderate alcohol consumption with protection against both diseases [41, 42]. Nevertheless, the beneficial effects of alcohol have been questioned due to the difficulties in establishing a safe drinking threshold [43].

Smoking

It is well known that smoking negatively affects several disease outcomes of rheumatic and musculoskeletal diseases (RMDs), such as the response to treatment, disease activity, and comorbidities. Tobacco consumption in patients with RA causes a lower response to a first-line disease-modifying antirheumatic drug (DMARD), a greater probability of interstitial lung disease before or after DMARDs, a 2.6-higher risk of EULAR non-remission, higher disease activity, and higher CRP levels compared to non-smokers. SLE patients who smoke have worse 36-Item Short form survey scores and a more severe rash [44]. The REUMAVID study showed that smoking declined in patients with RMDs as 28.2% of the population quit smoking during the pandemic; however, a significant proportion of patients (24.6%) smoked more than before COVID-19 pandemic [17]. Also, in a study made from the COVID-19 Global Rheumatology Alliance database, patients with RMDs who smoked were more likely to be admitted to hospital, and ever smoking was more common in those who died [18].

Dietary changes

There is evidence of the association between diet, both micro- and macronutrients, and immunity regulation and how disturbances in the nutritional status of people can lead to autoimmunity [45]. The COVID-19 pandemic had many, mainly, negative consequences on feeding and dietary habits and could have an important impact on health, including mental health. Most studies reported negative dietary changes, especially an increase in meals and snacks. A possible explanation could be increased intake and consumption of high-caloric foods to cope with anxiety, sadness, and boredom during lockdown [14, 15, 46,47,48,49].

Some specific dietary behavior could be associated with gender. Boaz et al. reported women consumed sweet baked goods, vegetables, and olive oil more than men. On the other hand, men consumed red meat and sweetened/carbonated beverages more than women [46]. Most of the information about dietary changes was obtained from studies on the general population. Caton et al. found similar outcomes in patients with rheumatic diseases. Most of these patients declared a worsening in their diet during the lockdown. This finding was explained by an increase in the number of meals and caloric intake, as well as adopting this behavior for emotional coping [16].

Comorbidities during the COVID-19 pandemic

Diabetes mellitus

Diabetes is a very important comorbidity to consider in patients with SLE or RA, increasing by itself the cardiovascular risk in this population, being the cardiovascular disease the main cause of death in people with diabetes mellitus [50].

Various studies carried out before the pandemic documented a prevalence of 15% in patients with RMD, which was reflected in studies carried out during the pandemic, where the prevalence of diabetes mellitus in patients with RA was 14.9% [19, 51], although in another study carried out in 2021, a prevalence of 25.02% was found in patients with rheumatological diseases, mainly RA and SLE [52]. These data could point to a slight increase in this comorbidity in patients with RA and SLE, although more studies are needed to clarify this potential increase.

Obesity

Obesity is prevalent in patients with rheumatic diseases, such as RA [53] and SLE [54]. Observational studies have shown that obesity predisposes to negative outcomes [55]. The negative influence of an excessively high body mass index (BMI) on the risk of developing the disease, on activity indexes, quality of life, and response to treatment is suggested to be strong in inflammatory joint diseases (IJD), such as RA and SLE [56, 57], because of increased cytokine production in visceral adipose tissue [55].

During the COVID-19 outbreak, some studies used weight modifications as an indicator of habit changes [35, 57,58,59,60,61] that could lead to an increase in obesity [35]. Patients that are overweight or obese, in addition to having longstanding and moderate disease activity, have a high risk of cardiovascular disease [53]. Thus, this risk may increase in patients with rheumatic diseases because of the COVID-19 pandemic.

Hypertension

One of the most common comorbidities in severe COVID-19 patients is hypertension, which is also a risk factor for pneumonia and severe disease in the general population and patients with multiple comorbidities, including rheumatic diseases [20, 62,63,64]. Therefore, blood pressure follow-up during the lockdown was an important point for public health services. In a sample of 72 hypertensive patients, Fucile et al. demonstrated a decrease in blood pressure levels, approximately 7 mmHg in systolic blood pressure and 3 mmHg in diastolic blood pressure [65]. Almost the same results were found in the study by Pengo et al., in which they reported a decrease in blood pressure in 126 patients with a reduction of 6 mmHg in systolic blood pressure in most patients during the first lockdown period [66]. Similar results were found in a French population, with a reduction of about 1.5 mmHg in diastolic blood pressure and 3 mmHg in systolic pressure after 4 weeks of lockdown [67]. However, these changes in blood pressure did not last beyond the first period of lockdown, according to the blood pressure values recorded between January and March 2021, where there was a slight increase in diastolic and systolic blood pressure values [68]. Although there is insufficient evidence of this behavior in rheumatic patients, the worsening lifestyle in the general population might be similar in rheumatic patients, with a tendency for increased blood pressure.

Hypertension among rheumatic patients hospitalized for COVID-19 was around 50%, and this finding correlated with a higher probability of being admitted than rheumatic patients who do not have hypertension [69,70,71,72]. Also, hypertension in this population is an independent determinant of disease severity, increasing mortality risk [64].

In the rheumatic population, an interesting finding was observed by Fouad et al., where most patients with rheumatic diseases and comorbidities such as hypertension dropped their medication or did not adhere to treatment because of the fear generated by COVID-19. They also reported that close to 50% of the rheumatologic patients (mainly RA and SLE) experienced limitations in access to specialized care including DMARDs during this period. Besides, they found a negative impact in mental health in 92% of their patients with 60% of high levels of psychological distress and an increase in patients with uncontrolled disease from 8.3% prior to the pandemic to 20% during it [62].

Pham et al. found that patients with higher values of the 4-item Perceived Stress Scale (PSS-4) have higher values of Routine Assessment of Patient Index Data 3 (RAPID3) score. During the pandemic, most of the patients included in the study presented higher PSS-4 values [73]. Considering the negative impact of the COVID-19 pandemic on mental health mentioned before, the increase in uncontrolled disease, and the correlation found by Pham et al., there is clearly a negative impact on disease activity caused by the COVID-19 pandemic, and derived actions. These findings take importance mainly because of the high prevalence of hypertension among patients with RA. This drop in medication and the high prevalence in psychological distress worsen their cardiovascular risk, increase disease activity, and eventually lead to a major risk of being admitted when infected with SARS-CoV-2 [64, 74].

Dyslipidemia

Dyslipidemia is an important comorbidity among patients with rheumatic diseases mainly because of its role in subclinical atherosclerosis development, increasing the cardiovascular risk and the prevalence of carotid plaque [75, 76]. Although there is a lack of evidence about the behavior of blood lipid levels during the pandemic, some studies showed a trend of increased blood lipid levels when comparing before and after the lockdown in asymptomatic patients [77]. Even patients with an optimal lipid profile before the pandemic were affected by the lockdown. Perrone et al. found that stopping physical activity correlated with an increase of 15.8% in low-density lipoprotein (LDL) and total cholesterol [78, 79]. This behavior in the lipid profile might have also affected patients with RA and SLE due to the stopping of physical activity because of the pandemic, COVID-19, and the dropping of medication mentioned before. This finding is relevant because most people with rheumatic diseases and severe COVID-19 are older than 65 and have a high rate of comorbidities such as hypertension, diabetes, and dyslipidemia [64]. In addition, higher blood lipid levels correlate with a worse prognosis in rheumatic patients hospitalized with COVID-19 and with a higher risk of hospitalization than rheumatic patients who do not have dyslipidemia [63, 64, 71, 80, 81].

Due to the prothrombotic state caused by COVID-19 and accelerated atherosclerosis in patients with rheumatoid arthritis or systemic erythematosus lupus, dyslipidemia needs special attention from physicians, and further investigation about the interactions of SARS-CoV-2, rheumatic diseases, and dyslipidemia in this population might be necessary [82].

Depression and anxiety

Lockdown caused an increase in the prevalence of rheumatic patients with psychopathologies, especially depression and anxiety [12, 13, 21,22,23,24, 83, 84]. In the REUMAVID study, of the 534 RA patients included, 53.2% were at risk of anxiety and 43.2% of depression. Meanwhile, of 97 SLE patients included, 57.7% were at risk of anxiety and 51.5% of depression [17]. Fear of infection by SARS-CoV-2 and possible outcomes, familial health concerns, and baseline mental health have been described as possible risk factors for depression and anxiety [25, 83]. Scherlinger et al. reported that difficulties accessing medical care were significantly associated to anxiety (OR 1.94, p = 0.012); for depression, financial difficulties (OR 2.59, p = 0.006) and difficulties accessing medical care (OR 2.57, p < 0.0001) were associated [21]. On the other hand, emotional support and resilience have been mentioned as possible protective factors [13]. The study realized by Tee et al. found that satisfaction with the available health information COVID-19 was associated with depression subscales (p = 0.005) and wearing of face masks was associated with lower levels of depression (p = 0.044) [23].

The COVID-19 outbreak reduced activities and social interaction, which impacted mental health [11]. Depression and anxiety are highly prevalent in patients with rheumatic diseases [11, 85]. There are many reports about an increase in the frequency of flares in rheumatic patients associated with a decrease in physical activity levels, which predisposed to depression and anxiety. Inversely, patients suffering from these mental disorders are susceptible to increased disease activity scores [11, 12, 21, 25]. Ammitzbøll et al. found an increase of disease activity in 23.5% of patients, which contrasts with 18.9% of patients who showed symptoms of moderate depression in their study [12].

Depression and anxiety are twice as common in women, which is relevant since they represent a large proportion of rheumatic patients [86, 87]. Although depression and anxiety are not considered traditional cardiovascular risk factors, they have been related to increased cardiovascular events and worse outcomes [87, 88]. Possible mechanisms for this increase in cardiovascular risk are increased inflammatory cytokines, platelet aggregation, oxidative stress, endothelial dysfunction, atherosclerosis progression, and an increase in unhealthy behaviors such as smoking, decreased physical activity, and a higher intake of high-calorie foods associated with these mental disorders [87, 88].

Patients with cognitive impairment have a high prevalence of depression and anxiety, which increased during the lockdown [89, 90]. This data is relevant since the development of cognitive disturbances is common in patients with RA and SLE [91, 92]. Bartolini et al. observed a cognitive dysfunction prevalence of 38 to 71% in RA patients [93]. These findings, and the increased risk of depression and anxiety in RA and SLE, suggest that cognitive impairment could lead to worse cardiovascular outcomes.

Discussion

In this review, we found that during the COVID-19 pandemic, there was an increase in the prevalence of some of the most important cardiovascular comorbidities and risk factors in patients with rheumatic diseases. There was an increase in obesity and sedentarism, which can potentiate immune dysregulation and is linked with increased disease activity and symptoms in patients with RA [94]. When analyzing the impact of the pandemic on mental health, there was an increased prevalence of psychiatric disorders. Several studies associate RMDs, especially RA and SLE, with depression and anxiety. This finding is generally attributed to inflammation and the adverse impact of these diseases on quality of life, functioning, and productivity. Inversely, depression is linked to an increased risk of developing RA and a deteriorating disease course reflected in poor treatment adherence [95]. The effect of the pandemic on alcohol and tobacco consumption is difficult to determine. In general, a positive impact was seen by decreasing smoking prevalence and increasing the intention to quit smoking. As for alcoholism, an increase was reported, especially at the beginning of the pandemic, but it decreased and remained stable in the final phases. An increase in consumption was seen in both risk behaviors in those who used it as a coping mechanism. We must emphasize the importance of reducing these comorbidities, as smoking is considered the most important modifiable risk factor for RA. Alcohol consumption indirectly affects rheumatoid patients by interacting with some drugs used for the disease [39, 96].

It is important to know the behavior of these comorbidities during the pandemic in rheumatic and non-rheumatic patients due to the lack of access to healthcare services that were more available before the lockdown. There were also limited healthcare services for patients with hypertension and dyslipidemia, which also play an important role in rheumatic diseases due to the accelerated development of subclinical atherosclerosis and cardiovascular events [97]. These findings are interesting because most rheumatic patients with hypertension, dyslipidemia, and/or obesity hospitalized for COVID-19 had worse outcomes, such as severe disease or death [81, 98]. It is also important to mention that we need further investigation into the prevalence of these comorbidities in patients with rheumatic diseases due to a lack of information.

Analyzing all these consequences that the pandemic had on patients with rheumatic inflammatory autoimmune diseases, we also researched strategies to reduce comorbidities. The EULAR 2021 recommendations mention the importance of quitting tobacco use due to impaired function, increased symptoms, disease activity, disease progress, and comorbidities. In addition, this habit could affect DMARD treatment in patients with rheumatoid arthritis. Although a low level of alcohol consumption is unlikely to impact rheumatic disease outcomes negatively, people with rheumatoid arthritis and health professionals should be aware because moderate alcohol consumption is associated with an increased risk of rheumatoid arthritis flare and comorbidities. Sometimes, the line between low and moderate alcohol consumption is not well delimited due to misunderstanding or misinformation [99].

Physical activity benefits several aspects of physical and mental health and should be promoted for all. It has a protective effect on the development of depression or can be used to manage symptoms acutely [100]. In the long term, continuous exercise will modulate the immune system and decrease chronic inflammation, offering protection against infections and chronic diseases [29]. Physical activity, specifically aerobic exercise in moderate intensity for at least 150 min per week and strengthening exercise twice a week, has an anti-inflammatory effect that is beneficial in RA and SLE patients by reducing inflammatory markers and joint pain, as well as improving function and quality of life and reducing all-cause mortality in patients with rheumatic autoimmune diseases [99].

This study has limitations worth noting. Information on the behavior of cardiovascular risk factors and comorbidities in patients with rheumatological diseases is limited. Additionally, disease activity data during and after the pandemic, which may impact cardiovascular risk, are also scarce. Studies that compare these factors longitudinally before, during, and after the COVID-19 pandemic are necessary.

Conclusion

The pandemic and lockdown by COVID-19 affected rheumatic patients, not only in disease-related characteristics but in the prevalence of their comorbidities, predisposing them to the development of new complications and, therefore, an increase in their cardiovascular risk. Lifestyle changes, such as healthy eating, and physical activity, besides optimal management of their rheumatic diseases and comorbidities, are essential to manage the consequences of the COVID-19 outbreak.