Introduction
Rheumatic fever is an autoimmune disease that occurs as a result of group A β-hemolytic streptococcal infection in genetically susceptible individuals, Reference Bisno1 and in which carditis, arthritis, chorea, subcutaneous nodules, and erythema marginatum develop. Reference Gewitz, Baltimore and Tani2 In 2015, changes were introduced in the Jones criteria in the intermediate- and high-risk population, including clinical and/or subclinical rheumatic heart disease, polyarthritis, monoarthritis, and polyarthralgia in the major criteria. Reference Gewitz, Baltimore and Tani2,Reference Zühlke, Beaton and Engel3 Echocardiography examination is currently the main diagnostic tool used to confirm, diagnose, and monitor valvular lesions in the course of rheumatic fever, especially in cases of subclinical rheumatic heart disease. Subclinical rheumatic heart disease is considered to be a condition in which no auscultatory murmur is heard on cardiac examination or recognised by the diagnosing clinician, but where echocardiography reveals mitral or aortic valve pathology. The prevalence of subclinical rheumatic heart disease varies between 0% and 53%. Reference Gewitz, Baltimore and Tani2–Reference Reményi, Wilson and Steer6 The aim of early diagnosis may be considered to stop or reverse the progression of the disease to a more severe form with secondary benzathine penicillin G prophylaxis. Reference Gerber, Baltimore and Eaton7
However, recent studies have shown that globalisation, migration, and refugee crises have led to the development of rheumatic heart disease in developed countries, making rheumatic heart disease a global health problem. Reference Iung, Vahanian, Iung and Vahanian8,Reference Murphy, Woodman, Roberts and McKee9 In this study, we aimed to retrospectively evaluate the results of our mild, moderate, and severe rheumatic heart disease patients who presented to our centre for different reasons, who were diagnosed by echocardiography and followed up for a mean of 4.92 years (1–8 years).
Materials and methods
Between 1 March 2015 and 31 December 2023, 180 patients diagnosed with rheumatic heart disease with a mean follow-up of 4.92 ± 2.0 (3.5–6.5 years) years were included in the study. The rate of rheumatic heart disease among all acute rheumatic fever/rheumatic heart disease diagnosed during this period was 55.2% (n = 180) (total 326 patients). These patients were diagnosed according to American Heart Association and World Health Organization. The 8-year follow-up, treatment, and echocardiography of the patients were performed by the same paediatric cardiologist. Patients diagnosed with rheumatic heart disease were asymptomatic patients who were referred to our paediatric cardiology outpatient clinic for other reasons such as pre-sports evaluation, chest pain, dizziness, Sydenham chorea, and syncope. Patients were evaluated with echocardiography at 6–12-month intervals. The study was conducted in accordance with the Declaration of Helsinki and ratified by the educational planning board of our hospital (approval no. 13.05.2024/09).
Populations at moderate and high risk for acute rheumatic fever: Populations where the incidence of acute rheumatic fever is >2 per 100,000 school-age children (usually 5–14 years) per year, or where the all-age prevalence of rheumatic heart disease is >1 per 1000 population, are moderate- to high-risk populations. Reference Reményi, Wilson and Steer6 Subclinical rheumatic heart disease: Rheumatic valvular heart disease was detected on echocardiography scan in an asymptomatic population. Subclinical rheumatic heart disease refers exclusively to the circumstance in which classic auscultatory findings of valvar dysfunction either are not present or are not recognised by the diagnosing clinician, but echocardiography studies reveal mitral or aortic valvulitis. Reference Gewitz, Baltimore and Tani2,Reference Lawrence, Carapetis, Griffiths, Edwards and Condon4,Reference Reményi, Wilson and Steer6 Rheumatic mitral regurgitation and aortic regurgitation: Pathologic mitral regurgitation and aortic regurgitation were diagnosed according to the echocardiography criteria developed by The American Society of Echocardiography in 2023. Reference Pandian, Kim and Arias-Godinez10 Pathologic mitral regurgitation on colour Doppler echocardiography was considered to be a pathologic mitral regurgitation when regurgitation was demonstrated on at least two different images, systolic jet length was ≥2 cm on at least one image, and peak velocity was >3 m/s. Pathologic aortic regurgitation on colour Doppler echocardiography was considered pathologic aortic regurgitation if aortic regurgitation was demonstrated on at least two different images, diastolic jet length was ≥1 cm on at least one image, and peak velocity was >3 m/s. Chronic mitral valve involvement on echocardiography was evaluated as thickening of the leaflets, fusions and thickening of the chorda tendinea, limited mobility of the leaflets, and calcifications. Patients diagnosed with valvulitis and cardiomegaly on echocardiography were evaluated as moderate carditis and severe carditis in the presence of heart failure, and mild/moderate/severe valve insufficiency was classified according to the severity of the valve insufficiency. Reference Gerber, Baltimore and Eaton7,Reference Pandian, Kim and Arias-Godinez10 Benzathine penicillin G 600 thousand U for patients with a body weight <27 kg, 1.2 million U for those with a body weight between 27 and 65 kg, and 2.4 million U for those with a body weight >65 kg were administered by intramuscular injection every 21 days. In all patients, information about secondary prophylaxis was given by the parents and/or the patient. Although the statements of the patients and parents were essential, the written prescription was also checked. Those who complied with this rule were considered to have received regular benzathine penicillin G prophylaxis.
Results
Of the 326 patients we followed for acute rheumatic fever and acute rheumatic heart disease, 180 (55.21%) were evaluated as subclinical rheumatic heart disease. Among patients with rheumatic heart disease, 50.6% were male, 49.4% were female, mean age at diagnosis was 11.74 ± 3.18 years, mean follow-up was 4.92 ± 2.0 years, and 22.2% had a positive history of acute rheumatic fever. Rheumatic heart disease was mild in 90%, moderate in 7.8%, and severe in 2.2% of the patients. The rates of mitral regurgitation and aortic regurgitation were 87.2% and 38.3%, respectively. In addition, mitral regurgitation and aortic regurgitation coexisted in 27.2% patients. Mitral regurgitation regressed in 20.6% of patients, completely resolved in 7.8%, and in aortic regurgitation these rates were 12.8% and 3.4%, respectively. Mitral regurgitation increased in 8.3% patients. In addition, Sydenham chorea was diagnosed in 7.8% of the patients. Further, 23.3% patients were on irregular benzathine penicillin G prophylaxis. Patients with mitral valve stenosis and valve surgery were the patients with severe rheumatic heart disease clinically. Benzathine penicillin G allergy was present in only three female patients, and two of them used irregular secondary antibiotherapy prophylaxis. As allergic reactions, itching and widespread maculopapular rash developed in two patients, and syncope (anaphylaxis?) developed in one. Subsequently, the skin test performed by Pediatric Allergy showed positive penicillin allergy in all three patients. In benzathine penicillin G allergy, patients were started on macrolide group antibiotic prophylaxis (Table 1). The majority of patients with moderate and severe rheumatic heart disease were female, while in mild rheumatic heart disease cases, the number of males was found to be higher (P = 0.057). The prevalence of mitral regurgitation was 85.8% in mild rheumatic heart disease and 100% in moderate and severe rheumatic heart disease cases (P = 0.231). However, the prevalence of aortic regurgitation was 38.9% in mild rheumatic heart disease, 42.9% in moderate rheumatic heart disease, and aortic regurgitation was absent in severe rheumatic heart disease cases (P = 0.269). Heart failure was present in cases with moderate and severe rheumatic heart disease, and among three patients who underwent surgical intervention and mitral stenosis, all had severe rheumatic heart disease. It was observed that patients with increased mitral regurgitation significantly had irregular secondary antibiotic prophylaxis (P < 0.001) (Table 2).
AR = aortic regurgitation; SBPGP = secondary benzathine penicillin G prophylaxis; MR = mitral regurgitation; *Pearson chi-square, **Fisher’s exact test.
Of the patients, 130 with mild rheumatic heart disease (n = 130) were found to have regular while 32 patients had irregular benzathine penicillin G prophylaxis. In moderate rheumatic heart disease, this ratio was seven patients each, and in severe rheumatic heart disease, three out of four patients were found to have irregular benzathine penicillin G prophylaxis. It was observed that patients with decreased mitral regurgitation significantly adhered to regular benzathine penicillin G prophylaxis (P = 0.043). Men showed a significant adherence to regular benzathine penicillin G prophylaxis (P = 0.004). Although not statistically significant, patients with Sydenham chorea tended to have a higher rate of adherence to regular benzathine penicillin G prophylaxis. Additionally, although not statistically significant, adherence to secondary prophylaxis was found to be lower in patients with a follow-up period of more than 5 years (Table 3).
*Pearson chi-square, **Fisher’s exact test.
Statistical evaluation
After encoding the data obtained from the study, they were transferred to the computer and analysed using the SPSS (Version 22 for Windows, SPSS Inc., Chicago, IL, USA) package programme. Continuous variables were expressed as mean ± standard deviation (1.quartile–3. quartile). Frequency data were expressed as numbers and percentages (%). For comparison of frequency data, the Pearson chi-square test or Fisher’s exact test was used. A significance level of p < 0.05 was considered for all tests.
Discussion
In this study, we observed a decrease, improvement, or delay in the progression of rheumatic aortic regurgitation and mitral regurgitation in rheumatic heart disease patients who regularly underwent benzathine penicillin G prophylaxis. Conversely, we found a significant increase in valve insufficiencies in those who underwent benzathine penicillin G prophylaxis irregularly. It is known that without regular benzathine penicillin G prophylaxis application to rheumatic heart disease patients, deterioration in carditis may occur over time. Reference Araújo, Goulart and Meira11–Reference Tubridy-Clark and Carapetis13 The purpose of early diagnosis can be considered to halt or regress the disease to a less severe form with secondary benzathine penicillin G prophylaxis. The main cause of morbidity and mortality resulting from acute rheumatic fever is recurrent acute rheumatic fever attacks and rheumatic heart disease with its associated complications (heart failure, arrhythmia, stroke, thromboembolic events, death). Reference Araújo, Goulart and Meira11,Reference Karthikeyan12
Although some studies suggest that rheumatic heart disease lesions may persist or worsen despite secondary antibiotic prophylaxis, the existing data are insufficient and of low quality, so reliable conclusions about the prognosis of rheumatic heart disease cannot be made. Until better studies are conducted, we don’t have good evidence, but also we have to make evidence-based decisions. These decisions will have important practical implications, such as the use of echocardiography during the acute phase and follow-up, and the duration of secondary prophylaxis for acute rheumatic fever (ARF) diagnosis and rheumatic heart disease patients. Reference Tubridy-Clark and Carapetis13 While reliable conclusions about the prognosis of rheumatic heart disease were not provided in some retrospective studies, we believe that the long-term follow-up of patients in our study by the same paediatric cardiologist for an average of 4.92 years (1–8 years) enhances the quality and reliability of the study. Meanwhile, the fact that some of our rheumatic heart disease patients with increased valve insufficiencies (although the number of cases is small) were in the group that applied irregular secondary antibiotic prophylaxis highlights the importance of antibiotic prophylaxis. Some rheumatic heart disease progressions can be prevented with regular benzathine penicillin G prophylaxis. Reference Karthikeyan12,Reference Beaton, Okello and Rwebembera14 The prevalence of rheumatic heart disease in the population is five to ten times higher than clinical rheumatic heart disease. Reference Marijon, Ou and Celermajer15,Reference Lamichhane, Patel and Al Mefleh16
Incomplete adherence to secondary prevention measures increases the risk of recurrent acute rheumatic fever and worsening of rheumatic heart disease after each acute rheumatic fever recurrence. Optimising adherence and ensuring safe and adequate drug supply are key to the success of secondary prevention, and a distribution model involving special services, case management, and family support can enhance adherence to secondary prevention in the acute rheumatic fever/ rheumatic heart disease population. Reference Kevat, Gunnarsson, Reeves and Ruben17–Reference Beaton, Okello and Aliku19 In fact, penicillin has been the cornerstone of acute rheumatic fever treatment for decades, and there is no other proven treatment that alters the likelihood or severity of rheumatic heart disease after an acute rheumatic fever attack. Reference Beaton, Okello and Aliku19
Approximately 55% (180/326) of our acute rheumatic fever/ rheumatic heart disease patients, who were followed up for an average of 4.92 years, were diagnosed with rheumatic heart disease. The patients diagnosed with rheumatic heart disease were typically referred to our clinic with other complaints (pre-sports assessment, chest pain, Syn. chorea, dizziness, syncope, etc.) and were asymptomatic. Results from studies conducted over the past 20 years, using echocardiography effectively in the diagnosis of acute rheumatic fever, have reported rheumatic heart disease rates up to 53%. Despite the absence of auscultation findings in most studies related to rheumatic heart disease, echocardiography has demonstrated mitral or aortic valve insufficiency in acute rheumatic fever patients. Reference Zühlke, Beaton and Engel3,Reference Reményi, Wilson and Steer6,Reference Gerber, Baltimore and Eaton7,Reference Pandian, Kim and Arias-Godinez10,Reference Hunter, Monaghan, Lloyd, Pecoraro, Doubell and Herbst20 The high rate of rheumatic heart disease in our study suggests that the effectiveness and reliability of echocardiography in diagnosing rheumatic heart disease are higher than clinical examination. Both the World Health Organization and the World Heart Federation support rheumatic heart disease screening for rheumatic heart disease in moderate- and high-risk areas. Reference Wyber, Grainger Gasser and Thompson21–Reference Bottomley, Jones and Claassens23
Recent studies have strongly supported the use of portable echocardiography for rheumatic heart disease screening in developing countries. The detection rate of rheumatic heart disease patients by echocardiography has been shown to be 10 times higher compared to auscultation. Reference Marijon, Ou and Celermajer15 In some school screenings, this rate was found to be 2.3%, and in some studies using echocardiography for screening, the prevalence was detected to be 2.3 per 1000. Reference Chillo, Mutagaywa and Nkya25–Reference Beaton, Okello, Lwabi, Mondo, McCarter and Sable28 Optimising case detection in this way maximises the chance of preventing advanced rheumatic heart disease. Reference Marijon, Celermajer and Tafflet29 Adding echocardiography to rheumatic heart disease screening protocols leads to a much higher estimated prevalence, which is 10 times higher than that detected by clinical screening alone. However, in many echocardiographic screening studies, rheumatic heart disease prevalence has been found to range from 8 to 57 per 1000 children. Globally, it is estimated that there could be rheumatic heart disease in 62–78 million individuals, resulting in nearly 1.4 million deaths annually. Reference Dougherty, Khorsandi and Herbst30 When the child population rates of the 27 European Union member states were examined, it was found that while the child population rate was 18.1% on average in the European Union in 2022, it was higher in Turkey at 26.5%. According to the Address-Based Population Registration System, as of the end of 2022, there were 22,578,378 children aged 0–17 in Turkey. Among these children, 16,911,205 (74.9%) are aged between 5 and 17. Reference Dougherty, Khorsandi and Herbst30 Although there are many differences between countries (such as socio-economic status, genetic predisposition, possible pathogenicity of group A β-haemolytic streptococcal), when we adapt the rheumatic heart disease prevalence found in echocardiographic screening studies in medium- and high-risk countries like ours to Turkey, it is between 135,000 and 963,000 in the 5–17 age group. However, we think that more screening programmes and special studies should be conducted to investigate the incidence of rheumatic heart disease in Turkey.
In clinical practice, the use of echocardiography and Doppler technology has increased the detection rate of rheumatic heart disease, allowing for early diagnosis and intervention even in asymptomatic, latent rheumatic heart disease cases. This has contributed to the reduction of morbidity and mortality associated with rheumatic heart disease. Reference Reményi, Wilson and Steer6
Recent technological advancements in echocardiography and other diagnostic methods, along with the development of new and modified diagnostic criteria, have achieved significant progress in the diagnosis and monitoring of rheumatic heart disease. The use of echocardiography in rheumatic heart disease and acute phases of rheumatic carditis has proven beneficial, surpassing clinical examination alone. This is because the rate of detecting carditis on echocardiography is higher, even in cases of acute rheumatic fever without clinical symptoms. Reference Araújo, Goulart and Meira11,Reference Karthikeyan12
Although 7.8% of our patients had moderate rheumatic heart disease, these patients lacked symptoms and auscultatory findings. In studies reporting rheumatic heart disease, despite the absence of auscultatory findings, echocardiography has shown mitral regurgitation and aortic regurgitation in acute rheumatic fever patients. Reference Pandian, Kim and Arias-Godinez10,Reference Hunter, Monaghan, Lloyd, Pecoraro, Doubell and Herbst20 Sydenham chorea is a hyperkinetic disorder characterised by irregular, jerky movements affecting the face, extremities, and trunk, associated with emotional variability and hypotonia. Sydenham chorea is a widely recognised post-streptococcal autoimmune disorder of the central nervous system. Reference Marques-Dias, Mercadante, Tucker and Lombroso32 Studies have reported the co-occurrence of rheumatic carditis with Sydenham chorea to range between 60% and 87.8% (34–36.)
Our patients had a clinical presentation of Sydenham chorea in 7.8% of cases, with no auscultatory findings or murmurs detected during cardiac examination. However, all patients referred due to Sydenham chorea were found to have subclinical rheumatic heart disease on echocardiography. The incidence of acute rheumatic fever varies greatly depending on socio-economic development, remaining a public health issue in low- and middle-income countries. The adherence to secondary antibiotic prophylaxis was found to be higher in patients with Sydenham chorea. This could be attributed to the physical and psychological impact of Sydenham chorea, which may affect patients more significantly than other clinical manifestations.
Preventing recurrent Group A streptococcal pharyngitis attacks is the most effective method to prevent the development of serious rheumatic heart disease. In populations where the incidence of rheumatic fever is particularly high, it is recommended to administer benzathine penicillin G every 3 weeks, as serum drug levels can fall below a protective level before the fourth week following the administration of this penicillin dose (Class I, Level of Evidence A). Reference Lue, Wu, Wang, Wu and Wu36 In our patients, the frequency of irregular secondary benzathine penicillin G prophylaxis was 22.2%, and it was found that mitral valve insufficiency increased in these patients. Possible reasons for irregular secondary benzathine penicillin G prophylaxis in acute rheumatic fever include difficulties in accessing healthcare centres, painful intramuscular administration, lack of awareness about the importance of prophylaxis, freezing of the preparation in the syringe, concerns about allergic reactions to the medication, and the long duration of secondary penicillin prophylaxis.
Secondary prevention is a strategy aimed at preventing the recurrence of acute rheumatic fever and the progression of rheumatic heart disease to a severe form by continuing antibiotics in individuals who have previously experienced acute rheumatic fever or already have rheumatic heart disease. Regular administration of secondary benzathine penicillin G prophylaxis reduces the rates of streptococcal pharynx/tonsil infections and recurrence of acute rheumatic fever. Reference Carapetis, Beaton and Cunningham37,Reference Katzenellenbogen, Ralph, Wyber and Carapetis38 Early detection of acute rheumatic fever and antibiotic use for secondary prevention are essential in combating rheumatic heart disease. However, a treatment strategy involving intramuscular benzathine penicillin G prophylaxis injections every 4 weeks for at least 5–10 years becomes the key determinant of success in preventing acute rheumatic fever and rheumatic heart disease recurrence. Lack of funding, distance to facilities, shortage of medical resources, fear of side effects, painful injections, and lack of awareness about the importance of treatment have been reported as the main reasons for poor adherence to secondary prevention. Reference Kevat, Gunnarsson, Reeves and Ruben17,Reference Lue, Wu, Wang, Wu and Wu36
The early detection of subclinical rheumatic heart disease can contribute to the reversal of mild lesions, delay the progression of the disease, reduce morbidity and mortality, and improve the quality of life for patients. Echocardiography is the gold standard method for screening and confirming latent rheumatic heart disease cases. Although there are doubts about the effectiveness of secondary antibiotic prophylaxis in randomised controlled trials, Reference Zühlke, Engel and Lemmer39 we believe that adherence to secondary antibiotic prophylaxis following the diagnosis of subclinical rheumatic heart disease with echocardiography in children from regions with moderate to high risk for rheumatic heart disease, such as Turkey, demonstrates the effectiveness and safety profile of reducing the risk of rheumatic heart disease. Nevertheless, it is important to confirm these results with large-scale randomised controlled trials.
Further research is needed before implementing population level screening. Secondary benzathine penicillin G prophylaxis alone may not be sufficient to prevent rheumatic heart disease; therefore, there is a need for improvements in health literacy, access to adequate healthcare services, increasing community awareness about the disease through technology and internet tools, improving overcrowded conditions and housing, and addressing socio-economic conditions, along with advancements in group A streptococcus vaccination.
Limitations of the study may include its retrospective nature and the small number of cases.
Author’s contributions
A.İ. designed the study. S.O.E., A.İ., and F.E.D. collected and analysed the data. A.İ. wrote the manuscript. All authors read and approved the final manuscript.
Financial support
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sector.
Competing interests
The authors declare no conflict of interest.