Determining Factors of Echocardiographic Changes in Patients With Systemic Lupus Erythematosus: a Cross-sectional Analysis

doi:10.21203/rs.3.rs-5286181/v1

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Determining Factors of Echocardiographic Changes in Patients With Systemic Lupus Erythematosus: a Cross-sectional Analysis

https://doi.org/10.21203/rs.3.rs-5286181/v1

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Introduction:

Systemic Lupus Erythematosus is a chronic autoimmune disease that affects multiple organs. Its pathogenesis involves a dysregulated immune response, but the complete mechanisms are not yet fully understood. Chronic inflammation associated with Lupus increases the risk of premature atherosclerosis, leading to cardiovascular events such as myocardial infarction and stroke, which reinforces the importance of preventive strategies to mitigate these risks.

Objectives

This study aimed to identify echocardiographic changes in patients with Systemic Lupus Erythematosus, considering the duration of the disease, the use of medications and comorbidities .

Method

The cross-sectional study was conducted from September 2023 to June 2024, with 22 volunteer patients from the Pará Rheumatic Patients Group (GARPA). Participants completed questionnaires on socioeconomic data and disease history, including time since diagnosis, comorbidities, and medication use. Subsequently, they underwent echocardiographic examinations performed by a single examiner. Statistical analysis was conducted using Fisher's exact test to associate clinical and socioeconomic variables with the observed cardiac changes, with significance set at p ≤ 0.05.

Result

Of the 22 patients studied, 90.9% were women, with a mean age of 40.82 ± 10.79 years. The majority (63.6%) were married, and 54.5% had completed high school. Regarding access to health care, 63.6% used the SUS. The most frequent comorbidities included systemic arterial hypertension (10.7%) and type 2 diabetes mellitus (7.1%), while 35.7% had no comorbidities. The mean time since diagnosis of the disease was 7.0 ± 4.34 years. In terms of medications, the most commonly used were hydroxychloroquine (25%) and prednisone (16.6%). Echocardiograms revealed pulmonary hypertension, mild mitral and aortic insufficiency, in addition to structural alterations such as left ventricular hypertrophy and interatrial septal aneurysm.

Conclusion

The duration of the disease and autoimmune, cardiovascular, musculoskeletal and neurological comorbidities are the main determinants of echocardiographic changes in patients with SLE. On the other hand, the main lines of treatment (antimalarials, corticosteroids and immunosuppressants) were not related to the outcomes.

Systemic lupus erythematosus (SLE) is a chronic inflammatory autoimmune disease that can affect several organs ¹. Its pathogenesis involves multiple mechanisms, including immunological defects and a dysregulated immune response in both innate and adaptive immunity. However, the pathological process that leads to the development of SLE is still not fully understood ² .

During disease progression, two distinct situations arise in relation to the risks of morbidity and mortality. The first is associated with early complications related to SLE activity or direct damage caused by the disease itself. The second, in turn, refers to chronic complications, such as infections and cardiovascular damage, which arise as the disease progresses ³. It is known that chronic inflammation induced by SLE can cause endothelial damage, predisposing patients to a greater propensity to develop premature atherosclerosis, an important cardiovascular risk factor ⁴ .

Studies have already established a significant correlation between SLE and an increased risk of cardiovascular disease, which raises an alert for the need for strategies to prevent and control cardiovascular risk factors in patients with this condition ⁵. Recently, it has been shown that patients with SLE have almost twice the risk of cardiovascular events, such as stroke, myocardial infarction, cardiovascular disease (CVD) and systemic arterial hypertension (SAH), compared to the general population ⁶. Furthermore, CVD is identified as one of the main causes of death among patients with SLE, being three times more frequent than in the general population and seven times more prevalent among black patients ⁷ .

Valvular, pericardial and myocarditis diseases are also more common in patients with SLE. Valvular lesions, for example, differ from other manifestations of the disease, as they are not necessarily associated with flare-ups of SLE activity and can occur at any stage of the disease. Their presence does not directly correlate with disease activity, unlike other manifestations, such as renal or joint lesions ⁸. Pericardial involvement, in turn, is the most common cardiac lesion among patients with SLE, and is also the most frequent cause of symptomatic cardiac disease. More than half of patients with SLE present with pericardial effusion at some point during their progression, and pericarditis may precede the onset of clinical signs of SLE ⁹ .

Given the high risks of cardiovascular morbidity and mortality, it is essential to integrate preventive measures into the treatment plan for patients with SLE, in addition to performing a routine assessment of cardiovascular risk factors ⁶. Therefore, this study's main objective is to identify the main cardiovascular alterations in patients with SLE.

Objective

The aim of the study was to evaluate the presence of cardiac alterations in patients with Systemic Lupus Erythematosus and the influence of the duration of the disease, medications in use and comorbidities of the patients. In addition, the socioeconomic aspects of the participants were also evaluated and related to the alterations obtained in the Echocardiogram.

Place and period of study

The study was carried out between September 2023 and June 2024 in volunteer patients from a non-profit institution called GARPA (Grupo de Pacientes Reumáticos do Pará) in the state of Pará.

Study design

A cross-sectional epidemiological study was carried out in the population of patients with a confirmed diagnosis of SLE.

Patients and procedures

A total of 22 patients, of both sexes and over 18 years of age, voluntarily participated in this study. Only those who agreed to participate and met the inclusion criteria were included. Inclusion criteria: adults aged 18 years or older, duly informed and who agreed to complete a questionnaire and provide clinical information after reading and signing the Free and Informed Consent Form (FICF). Exclusion criteria: individuals under 18 years of age who refused to sign the FICF or who did not provide their clinical history.

The study followed the ethical principles of the Declaration of Helsinki and complied with local regulations. Ethical approval was granted by the Ethics Committee of the State University of Pará, under protocol no. 6.217.003, on August 3, 2023. All patients gave written informed consent.

Participants completed two objective questionnaires: (1) a socioeconomic questionnaire, which assessed gender, age, education level and type of access to health care; and (2) another on the history of the disease, addressing the time since diagnosis, comorbidities, medications in use, smoking and alcohol consumption. After this, the patients underwent an echocardiogram.

Echocardiographic examinations were performed by a single echocardiogram specialist, who was blinded to the patients' medical history to avoid interference with the results. Patients were instructed not to discuss their medical conditions with the operator. The evaluations took place in a temperature-controlled room (approximately 21°C) with dimmed lighting. Patients were positioned in lateral and dorsal decubitus on a stretcher. The equipment used was a Philips® EPIQ Elite ultrasound system with a 2 to 5 MHz transducer.

Statistical analysis

Given the high error of the Chi -square test for small samples associated with N < 20 and the lowest expected frequency being less than 5, Fisher's exact test was used to calculate the probability of association between two categorical variables and, for this, the Rstudio 2024.09.0 ¹⁰ software was used. The analysis consisted of time of disease, grouped in 5-year intervals, use of corticosteroids, immunosuppressants, use of antimalarials, comorbidities and finally, the comorbidities were separated into metabolic, rheumatic, neurological, musculoskeletal and cardiovascular comorbidities and all of them related to valvular, structural and hemodynamic alterations. The situations were considered true when p < = 0.05.

As shown in Table 1, of the 22 patients, 90.9% (n = 20) were female and 9.1% (n = 2) were male. The mean age was 40.82 ± 10.79 years. Among the participants, 63.6% (n = 14) were married, 22.7% (n = 5) were single, and 13.6% (n = 3) were divorced. Regarding education, 54.5% (n = 12) had completed high school, 40.9% (n = 9) had completed higher education, and 4.5% (n = 1) had completed elementary education.

Most patients (63.6%, n = 14) used the Unified Health System (SUS) for their treatment, while 27.2% (n = 6) had health insurance and 9% (n = 2) depended on private services.

Among the reported comorbidities, the most frequent were hypertension (10.7%, n = 3), type 2 diabetes mellitus (7.1%, n = 2) and other conditions, such as hypothyroidism, rheumatoid arthritis (RA), each with a prevalence of 10.7% (n = 3). Furthermore, 35.7% of patients (n = 10) did not report comorbidities.

Regarding the time since diagnosis, the average was 7.0 ± 4.34 years. Regarding access to health care, 36.3% of patients (n = 8) received the diagnosis of their disease through the SUS, while 63.6% (n = 14) were diagnosed by private services.

The study revealed a series of findings related to the patients' comorbidities, classified into different categories: metabolic, autoimmune, neurological, musculoskeletal and cardiovascular. In the metabolic category, the presence of type 2 diabetes mellitus was identified. Autoimmune findings included rheumatoid arthritis (RA), hypothyroidism and Sjögren 's syndrome (SJ). In the neurological category, epilepsy and fibromyalgia were observed. In addition, musculoskeletal conditions, such as osteoporosis, and cardiovascular conditions, including hypertension, were recorded.

Table 1

– Description of socioeconomic variables in the studied population of patients with SLE (n = 22).
Variables			f (%)
Gender		Feminine	20 (90.9%)
Gender		Masculine	2 (9.1%)
Marital status		Single	5 (22.7%)
		Married	14 (63.6%)
		Widower	0 (0%)
		Divorced	3 (13.6%)
Education		Complete Elementary Education	1 (4.5%)
		High School Diploma	12 (54.5%)
		Incomplete High School	0 (0%)
		Completed higher education	9 (40.9%)
		incomplete higher education	0 (0%)
Access to health		Health plan	6 (27.2%)
		Particular	2 (9%)
		SUS	14 (63.6%)
Comorbidities	Metabolic	Type 2 Diabetes Mellitus	2 (7.1%)
	Autoimmune	Rheumatoid arthritis	3 (10.7%)
		Hypothyroidism	3 (10.7%)
		Sjögren 's syndrome	1 (3.6%)
	Neurological	Epilepsy	1 (3.6%)
	Neurological	Fibromyalgia	1 (3.6%)
	Musculoskeletal	Osteoporosis	1 (3.6%)
	Cardiovascular	HAS	3 (10.7%)
Smoker		Yes	1 (4.5%)
Smoker		No	21 (95.4%)
Drinking alcoholic beverages		Yes	2 (9.1%)
Drinking alcoholic beverages		No	20 (90.9%)
Time of illness		1 to 5 years	7 (31.8%)
		6 to 10	5 (22.7%)
		11 to 15	4 (18.2%)
		16 to 20	1 (4.5%)
Which health service was the diagnosis given?		SUS	8 (36.3%)
Which health service was the diagnosis given?		Particular	14 (63.6%)
The means by which the medicines are supplied		SUS	5 (22.7%)
The means by which the medicines are supplied		Particular	17 (77.2%)
SUS: Unified Health System; HAS: Systemic Arterial Hypertension

As shown in Table 2, among the 22 patients analyzed, the most commonly used medication was hydroxychloroquine, reported by 20% (n = 12) of participants. Prednisone also had a high prevalence, being used by 16.6% (n = 10) of patients. Vitamin D was mentioned by 10% (n = 6) of participants.

Other medications that were reported by a smaller number of patients included azathioprine and chloroquine, both used by 5% (n = 3) of participants. Leflunomide and levothyroxine were each cited by 3.3% (n = 2) of patients.

Additionally, there were a variety of medications that were mentioned by only one person (4.5% of cases), such as ASA, folic acid, contraceptive, carbamazepine, calcium carbonate, etanercept, iron, fluoxetine, levotiracetam, losartan, metformin, metoprolol, methotrexate, mycophenolate mofetil, nifedipine, olmesartan with hydrochlorothiazide, osteoban ( ibandronate ), pantoprazole, paroxetine, quetiapine, warfarin, and vitamin B12.

Table 2

– Distribution of medications used by the patients analyzed (n = 22).
Medicines	f( %)
Aas	1 (1.6%)
Folic Acid	1 (1.6%)
Contraceptive	1 (1.6%)
Azathioprine	3 (5%)
Carbamazepine	1 (1.6%)
Calcium Carbonate	1 (1.6%)
Etanercept	1 (1.6%)
Iron	1 (1.6%)
Fluoxetine	1 (1.6%)
Hydroxychloroquine	15 (25%)
Leflunomide	2 (3.3%)
Levotiractam	1 (1.6%)
Levothyroxine	2 (3.3%)
Losartan	1 (1.6%)
Metformin	1 (1.6%)
Metoprolol	1 (1.6%)
Methotrexate	1 (1.6%)
Mycophenolate Moefetil	1 (1.6%)
Nifedipine	1 (1.6%)
Olmesartan + Hydrochlorothiazide	1 (1.6%)
Osteoban (Ibandronate)	1 (1.6%)
Pantoprazole	1 (1.6%)
Paroxetine	1 (1.6%)
Prednisone	10 (1.6%)
Quetiapine	1 (1.6%)
Warfarin	1 (1.6%)
Vitamin B12	1 (1.6%)
Vitamin D ₃	6 (10%)

Regarding the echocardiogram findings, shown in Table 3, the study performed on the patients revealed several findings that were classified into three categories: hemodynamic, valvular and structural. In the hemodynamic findings, pulmonary hypertension (PH) was observed. Regarding the valvular findings, the following results were found: mild mitral regurgitation and moderate mitral regurgitation, in addition to mild aortic regurgitation, accompanied by mild thickening of the aortic valve leaflets. Moderate tricuspid regurgitation was also identified. In the structural findings, concentric left ventricular (LV) hypertrophy, grade I left ventricular (LV) diastolic dysfunction, interatrial septal aneurysm and 3 mm patent foramen ovale (PFO) without repercussion were observed. In addition, a 5 mm perimembranous interventricular communication (VSD) and mild dilation of the left atrium (LA) were reported. It is worth mentioning that in 15 patients no alterations were found.

Table 3

– Changes found in patients undergoing the examination
Classification	Findings	f
Valve	Mild Mitral Regurgitation	2
	Mild Aortic Insufficiency	3
	Moderate Mitral Regurgitation	2
	Moderate tricuspid insufficiency	1
Structural	Concentric LV Hypertrophy	1
	Mild thickening of the aortic valve leaflets	1
	Atrial septal aneurysm	1
	FOP 3mm without repercussion	1
	Perimembranous VSD (5mm)	1
	Mild LA dilation	2
Hemodynamics	Grade I LV diastolic dysfunction	4
Hemodynamics	Pulmonary Hypertension	1
No changes		12
PFO: Patent Foramen Ovale; VSD: Ventricular Septal Defect; LA: Left Atrium; LV: Left Ventricle.

Fisher's exact test showed that the duration of the disease was related to the development of changes in the echocardiogram (P = 0.023).

Regarding pharmacological treatment, the data demonstrated no correlation between the use of corticosteroids and valvular (p = 0.84), hemodynamic (p = 1) or structural (p = 0.36) alterations. Likewise, the use of antimalarials was not associated with valvular (p = 0.15), structural (p = 1) or hemodynamic (p = 1) involvement. Finally, immunosuppressants did not present valvular (p = 0.30), hemodynamic (p = 0.79) or structural (p = 0.58) repercussions.

Furthermore, the test concluded that there is an association between autoimmune (p = 0.004), neurological (p = 0.043), musculoskeletal (p = 0.042) and cardiovascular (p = 0.042) comorbidities and changes in the echocardiogram.

The results obtained in this study allow us to state that the duration of SLE is directly proportional to cardiac involvement present in the echocardiogram (p = 0.02), especially diastolic dysfunction and valvular heart disease. Several studies have shown this temporal association with various systemic involvements. The study by Sada et al ¹¹ stated that the duration of the disease is an independent risk factor for cardiovascular disease. Therefore, as demonstrated by Gerosa et al ¹², even long-term SLE patients with controlled symptoms require clinical monitoring.

Furthermore, Chang et al ¹³ and Leal et al ¹⁴ identified worse diastolic indices even in children at the time of diagnosis, indicating, along with other authors ^{15 ,} that this may be an early onset in the natural history of the disease. Teixeira et al ¹⁵ and Myhr et al ¹⁶ demonstrated an increase in left ventricular volume and thickness in patients with SLE, which may explain the evolution of the prevalence of diastolic dysfunction in this population over time. The study by Mirfeizi et al ¹⁷ found an association between the duration of the disease and the prevalence of diastolic dysfunction, as well as changes in left ventricular mass and pulmonary artery pressure.

The results of this study did not show any relationship between the use of corticosteroids and valvular (p = 0.84), hemodynamic (p = 1) or structural (p = 0.36) alterations. Despite the importance of glucocorticoids in the adjuvant treatment of SLE, the occurrence of short- and long-term cardiac alterations with their use has not been fully established. Similar and recent data were found by Mohammed et al 18 ^, in which the use of corticosteroids was not associated with the prevalence of structural, valvular or hemodynamic alterations.

The use of antimalarials, namely hydroxychloroquine, had no significant association with valvular (p = 0.15), structural (p = 1) or hemodynamic (p = 1) changes sensitive to echocardiography. Despite its classic involvement with QT interval prolongation and possible predisposition to cardiac arrhythmias, other studies have shown that its long-term use was not associated with echocardiographic changes ¹⁸ .

The use of immunosuppressants, a class represented by azathioprine, methotrexate and mycophenolate moefetil was also not related to valvular (p = 0.30), hemodynamic (p = 0.79) or structural (p = 0.58) repercussions. This is in line with other studies ^20,21 that demonstrated that there were no repercussions sensitive to this test due to the use of these immunosuppressants.

The data collected allow us to state that patients with SLE who have other autoimmune comorbidities (p = 0.028) presented significantly more echocardiographic alterations, especially diastolic dysfunction and valvular heart disease, in addition to left ventricular hypertrophy.

This relationship can be explained by the overlapping mechanisms adjacent to each comorbidity, as evidenced by other studies. RA, in addition to the valve alterations discussed above, has an independent association with LV diastolic dysfunction and possibly with right ventricular dysfunction ^22,23. Furthermore, longitudinal studies ²⁴ indicate progressive worsening over time, as is the case with SLE, strengthening both the hypothesis of concurrence of the injury mechanisms of each disease and the relationship between the duration of the disease and echocardiographic alterations.

Hypothyroidism has been shown to be associated with LV diastolic and systolic dysfunction, as well as impaired left atrial function. However, most studies report significant improvement in these parameters after adequate treatment ^25,26,27. Furthermore, recent studies have associated JS with a higher incidence of subclinical LV systolic and left atrial dysfunction ^29,30 .

Neurological comorbidity, namely epilepsy, demonstrated a significant association with alterations in the examination (p = 0.043). Similarly, other studies concluded that epilepsy alone can worsen systolic and diastolic parameters on echocardiography ^31,32. This suggests that the mechanisms of epilepsy injury may favor the incidence of cardiac damage.

Finally, cardiovascular comorbidity, represented by hypertension, demonstrated a significant influence on the altered parameters of the examination (p = 0.042). This comorbidity is classically associated with direct cardiac disorders, such as LV systolic and diastolic dysfunction and alteration of left atrial function ³³. This relationship is so relevant that the study by Yang et al ³⁴ demonstrates that left ventricular function improves with adequate blood pressure control.

The data from the present study presented some methodological limitations, especially those associated with sample limitation, heterogeneity of treatment among patients and lack of identification of biomarkers potentially associated with the pathophysiology of SLE complications. In addition, another limiting factor is the absence of other complementary tests for classifying the degree of disease activity.

Despite the limitations of the study, it was possible to conclude that the duration of the disease and autoimmune, cardiovascular, musculoskeletal and neurological comorbidities are the main determinants of echocardiographic alterations in patients with SLE. On the other hand, the main lines of treatment (antimalarials, corticosteroids and immunosuppressants) were not related to the outcomes. Thus, the research is an important reflection of the need to screen this population for cardiac alterations through echocardiography, which is an important tool in noninvasive diagnosis and early detection, resulting in better risk stratification and earlier treatment.

AAS	Acetyl Salicylic Acid
AE	Left Atrium
AIR	Rheumatoid arthritis
Stroke	Stroke
CIV	Ventricular septal defect
DCV	Cardiovascular Disease
FOP	Patent foramen ovale
GARPA	Group of Rheumatic Patients of Pará
HAS	Systemic Arterial Hypertension
HP	Pulmonary Hypertension
LES	Systemic Lupus Erythematosus
SJ	Sjogren's syndrome
SUS	Unified Health System
TCLE	Free and Informed Consent Form
VE	Left Ventricle

Consent for Publication

Você está sendo convidado(a) como voluntário(a) a participar da pesquisa: Alterações cardiovasculares de pacientes com Lúpus Eritematoso Sistêmico em Marabá-Pará. Essa pesquisa se propõe a investigar tais alterações, possibilitando uma maior compreensão sobre o assunto e, por conseguinte, melhores cuidados aos pacientes, gerando acréscimos à sociedade e às áreas da cardiologia, dermatologia e reumatologia. Por isso, o objetivo dessa pesquisa é analisar as alterações cardiovasculares em pacientes com lúpus eritematoso sistêmico na cidade de Marabá-PA.

Author Contribution

E.C.: conceived and organized the work, collected data in the field, and wrote the manuscript.G.S.: participated in data collection in the field and wrote parts of the manuscript.M.L.: contributed to data collection in the field and wrote parts of the manuscript.M.J.: participated in data collection in the field and wrote parts of the manuscript.L.S.: assisted in the manuscript writing.O.S.: performed the statistical analysis of the data.D.T.: cardiologist and echocardiographer, conducted examinations on all patients and provided guidance for the work, holding a PhD in the field.All authors reviewed and approved the final version of the manuscript.

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Determining Factors of Echocardiographic Changes in Patients With Systemic Lupus Erythematosus: a Cross-sectional Analysis

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Place and period of study

Study design

Patients and procedures

Statistical analysis

Results

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Conclusions

Abbreviations

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