Infective Endocarditis in Childhood: a Single- Center Experience of 26 Years

doi:10.21203/rs.3.rs-1645159/v1

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Infective Endocarditis in Childhood: a Single- Center Experience of 26 Years

https://doi.org/10.21203/rs.3.rs-1645159/v1

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Background: Despite developments in diagnosis and treatment, infective endocarditis (IE) continues to be a disease with high rates of morbidity and mortality. The aim of this study was to present the clinical and microbiological characteristics of patients with IE.

Methods: A retrospective evaluation was made of patients diagnosed with IE in our clinic between 1995 and 2021. The clinical and laboratory characteristics of the patients were recorded together with conditions constituting a risk for the development of IE, treatment, and surgical outcomes.

Results: Evaluation was made of 68 patients with a mean age of 7.3 years (range, 3 months-17 years), diagnosed with IE. An underlying cause of congenital heart disease was determined in 47 (69%) patients, and rheumatic valve disease in 3 (4.4%). There was no structural heart disease in 18 (26%) patients. A causative organism was found in 41 (60%) cases, and the micro-organism most often determined was viridans group streptococcus. No difference was determined between the patients diagnosed before and after 2007 in respect of the frequency of viridans streptococcus (p>0.05). Septic emboli were seen in 18 (26%) patients, of which 17 required surgical treatment. In 5 of 11 (16.6%) patients with mortality, the agent was S. aureus. Of the total IE patients, 28 (41%) were evaluated as hospital-acquired IE. The most frequently determined agents in this group were staphylococcus epidermidis (n:6) and S. aureus (n:5).

Conclusion: Although congenital heart diseases continue to be the greatest risk factor for IE, there is an increasing frequency of IE in patients with no structural heart disease. Mortality rates are still high in IE, especially in S. aureus endocarditis.

congenital heart disease

infective endocarditis

pediatric

normal heart structure

Infective endocarditis (IE) is defined as infection of the endocardial surface of the heart, native or prosthetic valves, or of various devices placed in the heart (1). Despite advances in diagnosis and treatment, IE continues to be a disease with high morbidity and mortality rates. The incidence of IE in the paediatric age group has been reported to be 0.34-0.64/100,000 per year (2). As the survival rates of children with congenital heart disease (CHD) have increased in recent years with repair or palliation, there has been an increase in IE cases associated with CHD. In children with IE, CHD is the most common underlying risk factor. Rheumatic heart diseases, which were the most common underlying cause in the past, are now the least frequent in developed societies (3-5). IE is seen in 8-10% of structurally normal hearts. The current increase in invasive cardiac procedures and the use of central venous catheters has caused an increase in the risk of IE in individuals with no underlying heart disease (6).

The aim of this study was to present the clinical, diagnostic, treatment and follow-up, and microbiological characteristics of patients with IE followed up in our clinic between 1995 and 2021.

Patients

This retrospective study was conducted using the patient database of the Department of Pediatric Cardiology, Çukurova University Hospital, a tertiary referral hospital. The study included all children aged <18 years who were diagnosed with definite or possible IE following the modified Duke Criteria between 1995 and 2021. Approval for the study was granted by the Local Ethics Committe. Informed consent was provided by the parents or legal guardians of the children in the study.

Clinical Data

A record was made for each patient of date of birth, gender, underlying CHD and surgical and interventional treatments. The recorded data of the IE episode included the date of IE diagnosis, patient history, clinical presentation, echocardiographic findings, biochemical and microbiological data, medical and surgical treatment, complications, and outcome. Patients who met the pathological criteria according to the modified Duke criteria and those who met two major criteria, one major and three minor criteria, or five minor criteria according to the clinical criteria were considered to have definite IE, and those who met one major and one minor criteria or three minor criteria were considered to have possible IE. Community-acquired (CA) IE was defined as episodes occurring more than 6 months after cardiac surgery in non-hospitalized patients or within the first 72 hours of hospitalization.

Statistical Analysis

Statistical analysis of the data was performed using SPSS for Windows, version 15.0 software (SPSS Inc.; Chicago, IL, USA). Categorical variables were presented as absolute and percentage frequencies, and quantitative variables were summarized as mean and standard deviation values.

Patient characteristics

From an examination of patient records, a total of 68 patients diagnosed with IE between 1995 and 2021 were identified. According to the modified Duke criteria, 55 (81%) of these patients had definite IE and 13 (19%) had possible IE. The patients comprised 34 (50%) females and 34 (50%) males, with a mean age at the time of diagnosis of 7.3 years (range, 3 months- 17 years). The age groups were determined as 11 (16%) patients aged <1 year, 15 (22%) aged 1- 5 years, 20 (29%) in the 6-10 years age group, and 12 (25.5%) in the 11-18 years age group.

Diagnosis was made in the period 1995-2007 in 29 patients, and in 2007-2021 in 39 cases. During the treatment for IE, 17 (25%) patients required surgery and 11 patients died. All the patients received 4-6 weeks antibiotic treatment in accordance with the European Society of Cardiology (ESC) guidelines. The patient characteristics are shown in Table 1.

Underlying risk factors for infective endocarditis

Of the 68 patients, the underlying risk factor was determined to be CHD in 47 (69%), and rheumatic valve disease in 3 (4.4%) patients. Ventricular septal defect was most often underlying CHD (n:12). The detailed diagnoses of congenital/acquired heart disease and surgical procedures before IE episodes are shown in Table 2. Surgery because of CHD was performed on a total of 27 patients (57% of all CHD patients) as palliative in 4 cases and corrective in 23 cases before the IE diagnosis. Of the 3 patients with rheumatic valve disease, mitral valve replacement was applied to 2. A total of 5 patients had a prosthetic valve (3 MVR, 2 AVR).

There was residual defect in 5 patients applied with corrective surgery. There was a history of dental treatment in 2 patients and untreated dental caries in 6 patients before IE. In 18 (26%) of the patients with IE there was no underlying structural heart disease. Of these patients, there was use of broad spectrum antibiotics in 7, a port catheter in 2, a permanent dialysis catheter in 2, and immune deficiency in 2. Of this group of patients, no risk factor for IE could be determined in 5. Hospital-acquired IE was determined in 28 (41%) of the total patients with IE.

Clinical Features at IE Diagnosis

The most frequently determined symptom of the IE patients was fever (≥38°C) in 84% of the patients. Pallor was determined in 77% of cases, murmur in 72%, fatigue in 62%, loss of appetite in 55%, splenomegaly in 38%, and skin findings in 20%. During diagnosis, there was seen to be congestive heart failure in 10 (15%) patients, and neurological findings in 6 (8%) (changes in consciousness in 2, stroke in 1, meningismus in 1, focal neurological findings in 1). At the time of presentation, 2 patients had symptoms of pulmonary emboli. Elevated CRP was determined in 97% of patients, anemia in 77%, leukocytosis in 78%, and hematuria in 23%.

Echocardiography and Lesion Location

Vegetation was observed with echocardiography in a total of 59 (86.7%) patients, on transthoracic echocardiography (TTE) in 54, and on transoesophageal echocardiography (TEE) in 5. In 9 patients with no vegetation observed on TTE or TEE, IE was diagnosed and treated based on micro-organism production in blood culture and/or minor criteria. From the analysis of echocardiography records, 35 (51%) patients were evaluated as right-side endocarditis, 25 (37%) as left-side endocarditis, 7 (10%) as bilateral endocarditis, and 1 as aorto-pulmonary shunt endocarditis.

Mitral valve involvement was most common (n.16, 24%), and the other cardiac structures where vegatation was determined were tricuspid valve (n:14, 21%), ventricular septum (n:9, 13%), pulmonary valve (n:8, 12%; 2 with native pulmonary valve, 6 with pulmonary homograft), aortic valve (n:5, 7%), both mitral and aortic valve (n:3, 4.4%), over coarctation patch (n:1, 1.5%) and aorto-pulmonary shunt (n:1, 1.5%).

Microbiology

Micro-organisms were isolated as the cause of IE in 41 (60%) patients. Throughout the whole study period of 1995-2021, the most frequently isolated micro-organisms in patients with culture production were viridans group streptococci (11 episodes, 27%), S. aureus (9 episodes, 22%), and coagulase-negative staphylococci (7 episodes, 17%). Other micro-organisms determined less frequently were candida, enterococci, pseudomonas species and HACEK group micro-organisms.

The patients were separated into two subgroups according to the time of diagnosis, as Group 1 diagnosed between 1995 and 2007, and Group 2 diagnosed between 2008 and 2021. Micro-organism production in culture was determined in 18 of the 29 Group 1 patients and in 23 of the 39 Group 2 patients. No significant difference was determined between the two groups in respect of the frequency of production in blood culture (p>0.05). No significant difference was determined between the groups in respect of viridans group streptococci (p>0.05).

There was also no prominent causal agent in left, right or bilateral heart IE. The majority of culture-negative endocarditis patients received antibiotic treatment before the blood culture test (22/27, 81%). In children with HA IE (n:28), the most common causative organisms were coagulase-negative staphylococci (6 episodes) and S aureus (5 episodes). Other organisms included Candida and pseudomonas. Ten patients with HA IE were culture-negative. The micro-organisms isolated in the IE episodes are shown in Table 3.

Outcomes

With antibiotic treatment of median 42 days, 42 (68%) patients recovered. Septic emboli were determined in 18 (26%) patients; systemic in 14, and pulmonary in 4. Of the 14 patients with systemic embolisation, there was central nervous system embolisation in 8. Focal neurological findings were determined in 6 patients, seizure in 2, and intracranial abscess in 3 . Aortic root abscess was observed in 1 patient, perivalvular abscess in 1, and purulent pericarditis in 1. Of the 6 patients with peripheral emboli observed, the emboli were in multiple regions in 3 (spleen, mesenteric, renal), renal in 2 and mesenteric in 1. Necrotising pneumonia developed in 2 patients with pulmonary embolism. All complications are shown in Table 4.

Early surgery was required in 17 (25%) patients. The mean period of preoperative antibiotic use in these patients was 7.5 days (range, 4-13 days). The reason for early surgery was severe valve failure in 9 patients, large mobile vegetation and removal of infected prosthetic material in 4, multiple emboli in 3, and mycotic aneurysm in 1. Congenital heart disease repair was performed together with the removal of vegetation in 6 of these patients, valve replacement was performed in 8 cases, valve repair and vegetation removal in 1, and repair of mycotic aneurysm in 1.

Elective surgery was performed after finishing antibiotic treatment in 9 patients. The general mortality rate was 16.6% (11/68). The patients with mortality left-side endocarditis in 6 cases, bilateral endocarditis in 3 cases, right-side endocarditis in 1 case, and shunt endocarditis in 1 case. In the cultures of these patients, S. aureus was determined in 5 cases, coagulase negative staphylococcus in 3, candida albicans in 1, strep. viridans in 1, and in 1 case the culture was negative. The cause of death was recorded as septic shock and multiple organ failure in 5 patients, systemic and intracranial embolism in 4, pulmonary emboli in 2, and diffuse intracerebral abscess in 2. The other 2 patients were exitus during postoperative intensive care follow up. In 1 of these patients prosthetic mitral valve replacement (MVR) had been performed because of previous rheumatic valve disease. During IE, perivalvular abscess developed in this patient and abscess drainage and vegetation clearance were performed together with MVR during the surgery. However, the patient required re-operation for prosthesis failure. The other exitus patient who had fungal endocarditis developed multiple organ failure after the surgery. In 1 VSD-pulmonary atresia patient with total correction made using a conduit, there was vegetation in the conduit. Transcatheter pulmonary melody valve replacement was performed in that patient after antibiotic treatment.

Despite advances in diagostic methods and treatment, paediatric IE continues to be a significant cause of mortality at the rate of 5–11% (7–9). According to the results reflected in this study, IE continues to be a significant and complex clinical problem. Of the IE cases in this study, 25% required early surgical intervention and 16% developed mortality. Several studies have shown similar high rates of IE morbidity and mortality (5, 7, 10).

The mean age of the current study patients was 7.3 years and 16% were aged < 1 year. There is known to be a high risk of IE in infants with congenital heart disease, one of the main reasons for which is the high rate of surgical interventions for CHD in this age group (5, 7, 11). This is supported by the finding of this study that the majority of patients in this age group (10/11) underwent palliative or corrective surgery because of CHD.

Having experienced endocarditis, the presence of an artificial heart valve, cyanotic CHD, or the presence of residue after CHD surgery are the most high-risk conditons for IE in the first 6 months after CHD surgery (12). In 74% of the current study patients, there was structural heart disease (47 CHD, 3 rheumatismal heart disease). These rates are similar to the data reported in other studies. CHD is seen more frequently in patients who have undergone surgery as they have got older and have been implanted with different devices and materials. These implanted materials constitute a risk for IE in both paediatric and adult patients. Almost half of IE patients with CHD have undergone surgery (5, 12, 13). In the current study, 57% of the patients with CHD were patients who had undergone surgery for CHD. Of these patients, endocarditis was determined in 10 within the first 6 months postoperatively. Moreover, these patients included patients implanted with artifical materials; 5 patients with mechanical heart valve, 6 with different valved conduits and 2 with Gore-tex shunt.

Morris et al. reported that there was a high risk of IE in patients with cyanotic CHD who had undergone corrective or palliative surgery. Of the 27 patients who underwent surgery in the current study, 16 had cyanotic CHD. The CHDs most often reported together with IE are ventricular septal defect (VSD), patent ductus arteriosus, aortic valve anomalies, and Fallot tetralogy. In the current study, VSD was the most commonly determined cardiac defect. Similarly, Niwa et al. reported the combination of VSD-IE to be most common (14).

Although rheumatic valve diseases were one of the most significant causes of IE in the past, they have now reduced dramatically in developed countries (15). However, in developing countries, rheumatic valve diseases are still a frequent cause of IE, especially in adult patients (5). In the current study, rheumatic valve disease was determined as the cause of IE in 4.4% of the cases. The incidence of acute rheumatic fever has been reported as 1/100,000 in developed countries (16) and as 50–100/100,000 in Turkey (17). The rate of rheumatic valve disease in IE patients in Turkey was reported as 64% in the 1990s, and as 18–36% in the 2000s (18, 19). According to these data, IE associated with rheumatic heart disease has decreased in Turkey, but this rate is still high compared to developed countries.

It has been reported that 8–10% of paediatric IE cases have structurally normal hearts (20). In the current study, 26% of the cases had a structurally normal heart, and recent publications have reported similarly high rates (21, 22). That there was chronic disease and/or immune deficiency in the majority of the IE cases with a structurally normal heart in the current study suggests that the IE was related to a invasive devices such as a tunneled central venous catheter. In 13 of the 18 IE cases with a structurally normal heart, there was at least one of these or similar risk factors creating a predisposition to IE.

In the current study cases with culture positivity, the most frequently isolated micro-organism was viridans group streptococcus. This was followed by S. aureus and coagulase-negative staphylococci. In different studies, some have reported S. aureus as the most common agent and some, streptococcus viridans (23, 25). Culture positivity rates have been reported to be approximately 90% in developed countries and 60% in Turkey. The reason for this difference is that some important microbiological tests cannot be performed in some centres (26). Another reason for the low culture positivity rate in the current stuy could be the use of antibiotics before diagnosis in these cases. In a previous meta-analysis which evaluated paediatric and adult patients, no micro-organisms were seen in 26.6% of IE cases (23). There are also studies that have reported much higher rates of culture negative IE (10).

The importance of invasive dental and medical interventions triggering IE in CHD is not very clear (27). Discussions are ongoing in literature on the subject of prophylactic prevention of IE. In the current ESC and AHA guidelines, IE prophylaxis is recommended for groups at high risk in respect of IE development and complications (28, 29). Since the IE prophylaxis regimen was changed in 2007, conflicting results have been reported in studies related to IE epidemiology. In a study that evaluated the effects of the change in prophylaxis regimen on IE incidence, clinical course, length of stay in hospital, and mortality, it was reported that in a 5-year period there was no significant change in incidence and disease severity, but there was an increase in the frequency of viridans group streptococcus in children aged > 10 years. It was emphasised that attention must be paid to the fact that dental treatments and related procedures are performed more often in this age group (30). In the current study, no change was observed in the rates of viridans group streptococcus infection between the periods before and after 2007 when the prophylaxis regimen changed. Moreover, the low rates of culture-positive IE in the current study prevented a strong conclusion in this respect. These findings were similar to those of Kelchtermans et al., who also reported no change in viridans group streptococcus rates before and after 2007 (9).

It has been reported that almost half of IE cases require surgery (31). Heart failure that cannot be controlled, severe valve failure, and the presence of local or systemic infection that cannot be brought under control constitute indications for surgery. The surgical mortality rate in active IE is 6–25% (32–35). In the current study, the mortality rate was determined to be 18% (2/11) in patients who required surgery due to the presence of active infection. There are no guidelines related to the surgical recommendations and indications for paediatric IE patients. More aggressive surgical approaches have been shown in some clinical conditions, especially in left-side and S.aureus endocarditis (36). The high mortality rates in S.aureus endocarditis in this and some previous studies support this view. However, there is a need for more comprehensive studies on this subject.

Clinical suspicion is very important in the diagnosis of children with risk factors for IE. The classic clinical symptoms of IE such as fever and sepsis, continue to be the primary clinical symptoms seen at the time of presentation. This highlights the importance of clinical suspicion, especially in patients with a history of CHD and implanted prosthetic material. The use of the modified Duke criteria provides an objective evaluation and early identification of suspicious endocarditis cases. The Duke criteria have mean sensitivity and specificity of 80% in IE diagnosis. Although these criteria support the IE diagnosis with objective findings in clinical practice, as sensitivity is low in cases with negative blood culture or low numbers obtained in blood culture, or with artifical valve IE or right heart IE, they should not supercede clinical evaluation (37).

Systemic embolisation is seen in 22–50% of IE cases, mostly in the cntral nervous system. The majority of embolic events are seen before diagnosis or in the first 2 weeks of treatment. Al-Bassri et al. reported neurological complications at a frequency of 23% in children with IE, the majority of which were stroke. In the same study, mortality was determined to be 2-fold higher in patients with neurological complications than in those without (38). The frequency of neurological complications was determined to be 16% in the current study. Of the 11 patients with neurological complications (8 emboli, 3 abscess), 6 were lost to mortality. There is a higher rate of neurological complications in patients with left-side endocarditis. In the current study, 9 of the 11 patients with neurological complications had left-side endocarditis.

Limitations

The major limitation of this study was the low number of patients. Another limitation was the retrospective design, resulting in incomplete documentation and data. Collection of weight-based standardized volumes of blood could not be confirmed from the records, as this was a retrospective study.

IE continues to be a significant problem because of high morbidity and mortality rates. Although CHD is the most important risk factor, the frequency of IE is increasing in individuals with a structurally normal heart. The identification of IE in children with risk factors is based on a high level of clinical suspicion. A high awareness by paediatricians and rapid treatment are important because of the complicated course. To reduce mortality and prevent complications in endocarditis with a high probability of a complicated course such as S. aureus, early diagnosis and early surgery may be useful. Further studies will serve an important purpose in more definitively predicting the symptoms of neurological complications which are an important cause of morbidity and mortality.

Acknowledgements:

None.

Financial Support:

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Conflict of Interest:

None

Ethical Approval:

The study was conducted in compliance with the Declaration of Helsinki with ethics approval provided by our hospital’s ethics committees.

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Table 1

Characteristics of IE patients.

Gender

34 (50%) female

34 (50%) male

Mean age at IE

7.3 years (3 months-17 years)

Underlying heart disease

CHD

Rheumatic heart disease

47 (69%)

3 (4.4%)

IE between 2000 and 2007

29 (42.6%)

IE between 2008 and 2021

39 (57.3%)

Localisation of IE

Right-sided

Left-sided IE

Bilateral

35 (51%)

25 (37%)

7 (10%)

28(41%)

Surgery for IE

During treatment

After completed treatment

17/(25%)

9/(13%)

Death due to IE

11(16%)

IE, infective endocarditis; HA, hospital acquired

Table 2

Detailed diagnoses of congenital/acquaired heart disease and surgical procedures before infective endocarditis episodes.

Underlying heart disease	Presurgery (n)	After surgery (n)
VSD	9	3 VSD repair
VSD+Coarctation		2 VSD repair+end to end anastomosis of COA
MVP	1
Bicuspid aortic valve+AS+AR	2	2 AVR
Shone complex	1	1 MVR
Rheumatic heart disease	1	2 MVR
VSD+Pulmonary stenosis	2
COA		1 Dacron patch repair
Pulmonary stenosis	2
PDA	1
Tetralogy of Fallot	1	6 TOF repair,
VSD+Pulmonary atresia		1 Central shunt 2 RVOT reconstruction with conduits+VSD repair
TGA+VSD+PS (Rastelli)		3 Rastelli surgery
DORV+VSD+PS	1	1 Rastelli surgery, 1 central shunt
Univentricular heart	2	1 BDG, 1 Pulmonary banding

VSD, ventricular septal defect; MVP, mitral valve prolapse; AS, aortic stenosis; MVR, mitral valve replacment; AVR, aortic valve replacment; PDA, patent ductus arteriosus; AI, aortic insufficiency; DORV, double outlet right ventricle; PS, pulmonary stenosis; TOF, tetralogy of Fallot; TGA, transposition of the great arteries; BDG, bidirectional Glenn; RVOT, right ventricular outflow tract

Table 3

Micro-organisms isolated in infective endocarditis episode.

Micro-organisms	Endocarditis episode (n=41)*
Streptococcus viridans	11(26.8%)
Staphylococcus aureus	9(21.9%)
Coagulase negative staphylococci	7(17.0%)
Candida albicans	3 (7.3%)
Pseudomonas aeroginosa	3 (7.3%)
Klebsiella oxytoca	2 (4.8%)
HACEK	2 (4.8%)
Streptococcus pyogenes	2 (4.8%)
Pseudomonas-like	1 (2.4%)
Enterobacter cloacae	1 (2.4%)
Total	41 (100%)

*Culture negative 27 patients

Table 4

Complications in patients with infective endocarditis

Complication	n
Systemic embolism Cerebral Peripheral embolism	8 6
Heart failure	10
Cerebral abscess	3
Sepsis	7
Pulmonary embolism	4
Mycotic aneurysm	4
Necrotic pneumonia	2
Cardiac abscess	2
Seizure	2
Renal failure (required renal replacment treatment)	2
Pulmonary edema	2
Purulant pericarditis	1

No competing interests reported.

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Infective Endocarditis in Childhood: a Single- Center Experience of 26 Years

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