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Epidemiological Profile of Patients with Infective Endocarditis at three Tertiary Centers in Brazil from 2003 to 2017

Abstract

Background

Infective endocarditis (IE) is a disease with high morbimortality and an increasing incidence. With improved diagnosis and treatment, a number of epidemiological changes have been reported over time.

Objectives

We sought to describe the epidemiological profile, mortality predictors, and analysis of a possible microbiological transition in patients admitted to three tertiary centers in Brazil.

Methods

In this cross-sectional retrospective study, data from 211 patients with definite or probable IE were analyzed according to the modified Duke criteria between 2003 and 2017. The association between categorical variables was assessed using the chi-square or Fisher's exact test, and binary logistic models were built to investigate mortality. We considered p <0.05 statistically significant.

Results

The median age of the sample was 48 (33-59) years old, 70.6% were men, and the most prevalent pathogen was Staphylococcus spp. (19%). Mortality was 22.3%, with increasing age being the leading risk factor for death (p = 0.028). Regarding the location of the disease, native valves were the most affected site, with the aortic valve being more affected in men than women (p = 0.017). The mean number of cases of Staphylococcus spp. (τ = 0.293, p = 0.148) and Streptococcus spp. (τ = -0.078, p = 0.727) has remained stable over the years.

Conclusion

No trend towards reduced or increased mortality was evident between 2003 and 2017. Although Staphylococcus spp. were the most prevalent pathogen, the expected epidemiological transition could not be observed.

Infective Endocarditis; Epidemiology; Mortality; Streptococci; staphylococci; Hospitalization; Comorbidities

Introduction

With improved resources for the prevention, diagnosis, and treatment of infective endocarditis (IE), significant changes in the characteristics of the disease have been reported over time. If, on the one hand, the prevalence of IE due to rheumatic valve disease has decreased, on the other, there has been an increase in IE related to degenerative valve disease in older adults, valve replacement surgery, the implantation of intracardiac devices, and the use of injectables and hemodialysis. Coincidentally, IE cases due to Staphylococcus spp. have surpassed those of Streptococcus spp., and cases due to atypical microorganisms have also increased.11. Prendergast BD. The changing face of infective endocarditis. Heart. 2006;92(7):879-85. , 22. Cresti A, Chiavarelli M, Scalese M, Nencioni C, Valentini S, Guerrini F, et al. Epidemiological and mortality trends in infective endocarditis, a 17-year population-based prospective study. Cardiovasc Diagn Ther. 2017;7(1):27-35. This microbiological change is attributed to medical progress and the resulting increase in invasive procedures.33. Sunil M, Hieu HQ, Arjan Singh RS, Ponnampalavanar S, Siew KSW, Loch A. Evolving trends in infective endocarditis in a developing country: a consequence of medical progress? Ann Clin Microbiol Antimicrob. 2019;18(1):43. , 44. Fowler VG Jr, Miro JM, Hoen B, Cabell CH, Abrutyn E, Rubinstein E, et al. Staphylococcus aureus Endocarditis: A Consequence of Medical Progress. JAMA. 2005;293(24):3012–3021.

Despite efforts to the contrary, IE is still considered a condition with persistently high morbimortality, and its incidence has increased over time.11. Prendergast BD. The changing face of infective endocarditis. Heart. 2006;92(7):879-85. However, most studies that observed this change were conducted in developed countries, and it is unclear whether developing countries are susceptible to this epidemiological transition to the same extent and magnitude, given the possible difference in access to medical resources.33. Sunil M, Hieu HQ, Arjan Singh RS, Ponnampalavanar S, Siew KSW, Loch A. Evolving trends in infective endocarditis in a developing country: a consequence of medical progress? Ann Clin Microbiol Antimicrob. 2019;18(1):43. Furthermore, it is extremely relevant to understand the risk factors associated with mortality as well as the profile of patients affected by IE.55. Watt G, Pachirat O, Baggett HC, Maloney SA, Lulitanond V, Raoult D, et al. Infective endocarditis in northeastern Thailand. Emerg Infect Dis. 2014;20(3):473-6. , 66. Bin Abdulhak AA, Baddour LM, Erwin PJ, Hoen B, Chu VH, Mensah GA, et al. Global and regional burden of infective endocarditis, 1990–2010: a systematic review of the literature. Glob Heart. 2014;9(1):131–143.

Only 10 epidemiological studies on IE have been published in Brazil, and none of them addressed this possible change, especially since their samples were included over a limited time span. Considering the high regional variability and epidemiological transition in IE, the purpose of this study was to survey the characteristics of a population of patients with IE over 14 years to analyze the behavior of variables over time, determine predictors of mortality, and better understand the profile of affected individuals.

Methods

Sample description and design

This observational, retrospective, cross-sectional study included 211 patients admitted to 3 tertiary health centers in Ipatinga and Belo Horizonte in the state of Minas Gerais, Brazil, between 2003 and 2017. An initial survey of medical records containing International Classification of Diseases related to IE (ICD 10 I33.0) was conducted. These records were analyzed and information on epidemiological, microbiological, valvular, and outcome characteristics were collected in an Excel database.

The inclusion criterion was definite or probable IE according to the modified Duke criteria.77. Li JS, Sexton DJ, Mick N, Nettles R, Fowler VG Jr, Ryan T, et al. Proposed modifications to the Duke criteria for the diagnosis of infective endocarditis. Clin Infect Dis. 2000;30(4):633–8. Patients whose medical records were incomplete, who were transferred during hospitalization, or who were still hospitalized at the time of analysis were excluded. After selection, data from the medical records were collected, including age, sex, blood culture, and prognosis. The microbiology was determined through blood culture results, and the location of the IE was determined through echocardiographic or perioperative findings.

This study was approved by the ethics committee of the Faculty of Medical Sciences of Minas Gerais (CAAE 60893616.7.0000.5134). Informed consent was not required due to the retrospective nature of the study.

Statistical analysis

Categorical variables are presented as absolute and relative frequencies, and quantitative variables are presented as median (1st – 3rd quartile). The normality of quantitative variables was assessed using the Shapiro-Wilk test, while the Wilcoxon-Mann-Whitney test was used to compare quantitative variables among groups. The association between categorical variables was assessed using the chi-square test and Fisher's exact test. Binary logistic models were constructed to verify the association with mortality, and the results are presented as odds ratios (OR) and 95% confidence intervals. The Mann- Kendall test was used to verify the temporal trend. The analysis was performed in R version 3.5.2, with p <0.05 considered significant.

Results

The sample consisted of 211 patients, whose profile has been described in a previous study:88. Bezerra RL, Carvalho TF, Batista RS, Silva YM, Campos BF, Castro JHM, et al. Association between Insulin use and Infective Endocarditis: An Observational Study. Int J Cardiovasc Sci. 2019;33(1):14-21. 110 from Belo Horizonte and 101 from Ipatinga. Their median age was 48.0 (33-59) years and 70.6% were men. Bacteria of the genus Staphylococcus were the most prevalent pathogens, observed in 19% of cases, with Staphylococcus aureus occurring in 10% and Coagulase-negative Staphylococci in 9%. Native valves were the site of IE in 70.6% of the cases, and the greatest prevalence was in the mitral valve (41.7%), ( Table 1 ).

Table 1
Characteristics of 211 patients with infective endocarditis

Mortality

Overall mortality was 22.3%. It was observed that increasing age is a risk factor for death (p = 0.028). However, when the sample was stratified into patients younger and older than 65 years of age, there was no statistical relevance ( Table 2 ). Among patients younger than 65 years who died, the native aortic valve was the most affected site (33.3%) and Staphylococcus spp. was the most frequent pathogen, representing 30.6% of the cases. Regarding the 11 deaths in patients older than 65 years, most were due to Streptococcus spp., and the most prevalent location was the native mitral valve. Sex, blood culture findings, and lesion location had no statistical relevance on mortality. Mortality from IE remained stable between 2003 and 2017 (τ = 0.010). The highest and lowest death rates occurred in 2004 and 2012, respectively.

Table 2
– Mortality risk analysis in 211 patients with infective endocarditis

Differences between the sexes

Of the 211 patients, 149 were men and 62 were women. A total of 82.3% of the men and 81.9% of the women diagnosed with IE were younger than 65 years of age (no significant difference). Native valves were most affected, especially the mitral valve, regardless of the patient's sex, representing 40.3% of the infections in men and 45.2% in women, while the pulmonary valve was the least affected site. Of note, prosthetic valve endocarditis occurred in 22.8% and 27.4% of the men and women, respectively, at a ratio of approximately 1:3 in relation to native valves. The native aortic valve was significantly more affected in men than women (p = 0.017). There was no association between the other findings (blood culture, age group, and other IE sites) and sex.

Microbiological agent

Table 3 shows the relationship between microbiological findings, age, and affected valve. There was no association between a specific microorganism and age, with individuals younger or older than 65 being equally affected. Infection by atypical microorganisms was more common in patients with prosthetic valve endocarditis (p = 0.014). Individuals without mitral lesions were more prone to infection by Coagulase-negative Staphylococci (p = 0.026). Regarding the main pathogens found during the study period ( Figure 1 ), all had a non-significant trend according to the Mann Kendall test: Staphylococcus spp. (τ = 0.293, p = 0.148), Streptococcus spp. (τ = -0.078, p = 0.727) and negative blood culture (τ = -0.332, p = 0.100), which indicates that the occurrence of these microorganisms was stable over the years.

Table 3
– Distribution of microbial agents according to age and location

Figure 1
– Main blood culture findings per year. Figure caption: All findings had a non-significant trend according to the Mann-Kendall test (τ = 0.293, p = 0.148, for Staphylococcus spp.; τ = -0.078, p = 0.727, for Streptococcus spp. and τ = -0.332, p = 0.100 for blood culture negative). Source: The authors

Discussion

IE is a serious infectious disease, and a multidisciplinary approach involving specialists is necessary to treat and monitor these patients. Although the incidence of IE has been increasing over the years,99. Damasco PV, Correal JCD, Cruz-Campos ACD, Wajsbrot BR, Cunha RGD, Fonseca AGD, et al. Epidemiological and clinical profile of infective endocarditis at a Brazilian tertiary care center: an eight-year prospective study. Rev Soc Bras Med Trop. 2019;52:e2018375. few studies have been published on IE in developing countries, which makes a general analysis difficult. The overall mortality in our sample was 22.3%, which is consistent with several other observational studies,1010. Murdoch DR, Corey GR, Hoen B, Miró JM, Fowler VG Jr, Bayer AS, et al. Clinical presentation, etiology, and outcome of infective endocarditis in the 21st century: The International Collaboration on Endocarditis-Prospective Cohort Study. Arch Intern Med. 2009;169(5):463–73. , 1111. Wang A, Athan E, Pappas PA, Fowler VG Jr, Olaison L, Paré C, et al. Contemporary clinical profile and outcome of prosthetic valve endocarditis. JAMA. 2007;297(12):1354–61. including some conducted in developing countries.1212. Ferreiros E, Nacinovich F, Casabé JH, Modenesi JC, Swieszkowski S, Cortes C, et al. Epidemiologic, clinical, and microbiologic profile of infective endocarditis in Argentina: a national survey. The Endocarditis Infecciosa en la República Argentina-2 (EIRA-2) Study. Am Heart J. 2006;151(2):545-52. The logistic regression model ( Table 2 ), showed that patient age was directly related to mortality [p = 0.028; OR 1.020, 95% CI 1.003; 1.039], which agrees with other studies, eg, Khan et al.,1313. Khan A, Aslam A, Satti KN, Ashiq S. Infective endocarditis post-transcatheter aortic valve implantation (TAVI), microbiological profile and clinical outcomes: A systematic review. PLoS One. 2020;15(1):e0225077. who obtained a similar result with a sample of 523,432 patients in the United States. Moreover, this study reported a trend over the years toward reduced mortality in IE patients, which the authors ascribed to improved medical services in the USA. However, such a trend was not observed in our analysis.

No significant differences were found regarding microbiological profile and mortality, which contrasts with the results of Joffre et al.,1414. Joffre J, Dumas G, Aegerter P, Dubée V, Bigé N, Preda G, et al. Epidemiology of infective endocarditis in French intensive care units over the 1997-2014 period-from CUB-Réa Network. Crit Care. 2019;23(1):143.who found an association between Staphylococcus spp., Candida spp. and higher in-hospital mortality, as well as an association between IE due to Streptococcus spp. and a more favorable prognosis. It should also be pointed out that these authors found male sex to be a protective factor against death. Other authors have found a direct relationship between mortality and endocarditis location, with the aortic and mitral valves having the worst outcomes.99. Damasco PV, Correal JCD, Cruz-Campos ACD, Wajsbrot BR, Cunha RGD, Fonseca AGD, et al. Epidemiological and clinical profile of infective endocarditis at a Brazilian tertiary care center: an eight-year prospective study. Rev Soc Bras Med Trop. 2019;52:e2018375. , 1515. Ren Z, Mo X, Chen H, Peng J. A changing profile of infective endocarditis at a tertiary hospital in China: a retrospective study from 2001 to 2018. BMC Infect Dis. 2019;19(1):945. , 1616. Mistiaen WP. What are the main predictors of in-hospital mortality in patients with infective endocarditis: a review. Scand Cardiovasc J. 2018;52(2):58-68. However, we did not observe this in the present study.

It is possible that comorbidities (e.g. hypertension, heart disease, etc.) and events (e.g. septic shock, need for surgical approach) affect prognosis more than the microbiological or valvular characteristics of the IE. Ren et al.1515. Ren Z, Mo X, Chen H, Peng J. A changing profile of infective endocarditis at a tertiary hospital in China: a retrospective study from 2001 to 2018. BMC Infect Dis. 2019;19(1):945. found significant associations between higher mortality and conditions such as hemorrhagic and ischemic stroke, constrictive heart failure, pneumonia, and renal failure. One limitation of our study is the lack of data on these variables.

In general, IE affected men the most (70.6%), at a ratio of 1.7:1. This difference has been found by other authors in Belgium,1717. Yombi JC, Yuma SN, Pasquet A, Astarci P, Robert A, Rodriguez HV. Staphylococcal versus Streptococcal infective endocarditis in a tertiary hospital in Belgium: epidemiology, clinical characteristics and outcome. Acta Clin Belg. 2017;72(6):417–423. Saudi Arabia,1818. Kaki R, Al-Abdullah N. Descriptive epidemiological, clinical and microbiological features of infective endocarditis at a University Hospital in Saudi Arabia. Am J Infect Dis. 2018;14(2):63–68. and Brazil,99. Damasco PV, Correal JCD, Cruz-Campos ACD, Wajsbrot BR, Cunha RGD, Fonseca AGD, et al. Epidemiological and clinical profile of infective endocarditis at a Brazilian tertiary care center: an eight-year prospective study. Rev Soc Bras Med Trop. 2019;52:e2018375. , 1919. Nunes MC, Gelape CL, Ferrari TC. Profile of infective endocarditis at a tertiary care center in Brazil during a seven-year period: prognostic factors and in-hospital outcome. Int J Infect Dis. 2010;14(5):e394–8. and Bakir et al.,2020. Bakir S, Mori T, Durand J, Chen YF, Thompson JA, Oparil S. Estrogen-induced vasoprotection is estrogen receptor dependent: evidence from the balloon-injured rat carotid artery model. Circulation. 2000;101(20):2342–4. ascribed it to the potential protective role of estrogen against endothelial injury. Other authors have reported a lower prevalence of IE in women, including a lesser likelihood of developing sepsis.2121. Wichmann MW, Inthorn D, Andress HJ, Schildberg FW. Incidence and mortality of severe sepsis in surgical intensive care patients: the influence of patient gender on disease process and outcome. Intensive Care Med. 2000;26(2):167–72. , 2222. Oberholzer A, Keel M, Zellweger R, Steckholzer U, Trentz O, Ertel W. Incidence of septic complications and multiple organ failure in severely injured patients is sex specific. J Trauma. 2000;48(5):932–7. Nevertheless, none of these mechanisms are fully understood. It is curious that, although IE affects fewer women, it seems to be related to higher in-hospital mortality.2323. Aksoy O, Meyer LT, Cabell CH, Kourany WM, Pappas PA, Sexton DJ. Gender differences in infective endocarditis: pre- and co-morbid conditions lead to different management and outcomes in female patients. Scand J Infect Dis. 2007;39(2):101-7. , 2424. Castillo JC, Anguita MP, Delgado M, Ruiz M, Mesa D, Romo E, et al. Clinical characteristics and prognosis of infective endocarditis in women. Rev Esp Cardiol. 2008;61(1):36–40. In fact, prognostic scales such as the EuroSCORE and the results of Martínez-Sellés et al.,2525. Martínez-Sellés M, Muñoz P, Arnáiz A, Moreno M, Gálvez J, Rodríguez-Roda J, et al. Valve surgery in active infective endocarditis: a simple score to predict in-hospital prognosis. Int J Cardiol. 2014;175(1):133‐7. indicate a worse outcome among women and a greater likelihood of death.

Furthermore, our analysis showed that native aortic valves are more affected in men than women (p = 0.017), which was also described by Sevilla et al.,2626. Sevilla T, Revilla A, López J, Vilacosta I, Sarriá C, Gómez I, et al. Influence of Sex on Left-Sided Infective Endocarditis. Rev Esp Cardiol. 2010;63(12):1497–500. and Elamragy et al.,2727. Elamragy AA, Meshaal MS, El-Kholy AA, Rizk HH. Gender differences in clinical features and complications of infective endocarditis: 11-year experience of a single institute in Egypt. Egypt Heart J. 2020;72(1):5. who further described that the native mitral valve was more affected in women. Regarding the microbiological profile between the sexes, the most frequent microorganism was Staphylococcus spp. (22.6% men vs 17.4% women, p = 0.501), a result similar to other authors.2727. Elamragy AA, Meshaal MS, El-Kholy AA, Rizk HH. Gender differences in clinical features and complications of infective endocarditis: 11-year experience of a single institute in Egypt. Egypt Heart J. 2020;72(1):5. The equally high negative blood culture rate in men and women is also of note (32.9% and 35.5% respectively, p = 0.838), which may be explained by the indiscriminate use of antibiotics to treat any febrile disease before obtaining cultures, a common practice in Brazil. It should be pointed out that some studies have found a much higher percentage of negative blood cultures than ours, eg, in Egypt (69.5%)2727. Elamragy AA, Meshaal MS, El-Kholy AA, Rizk HH. Gender differences in clinical features and complications of infective endocarditis: 11-year experience of a single institute in Egypt. Egypt Heart J. 2020;72(1):5. and South Africa (55.3%),2828. Koegelenberg CF, Doubell AF, Orth H, Reuter H. Infective endocarditis in the Western Cape Province of South Africa: a three-year prospective study. QJM. 2003;96(3):217-25. while others have found lower percentages, eg, in France (9%)2929. Hoen B, Alla F, Selton-Suty C, Béguinot I, Bouvet A, Briançon S, et al. Changing profile of infective endocarditis: results of a 1-year survey in France. JAMA. 2002;288(1):75–81. and the United Kingdom (12.2%).3030. Lamas CC, Eykyn SJ. Blood culture negative endocarditis: analysis of 63 cases presenting over 25 years. Heart. 2003;89(3):258-62. Thus, it could be cautiously inferred that Brazil is somewhere in the middle of a broad spectrum, which might be associated with improvements to the Brazilian public health system, as well as new and more effective hospital protocols.

The relationship between the affected valve and the blood culture results diverges greatly among studies. What became clear in our study was that a positive blood culture for coagulase-negative staphylococci is less related to mitral valve lesion ( Table 3 ), which was also reported by Barrau et al.,3131. Barrau K, Boulamery A, Imbert G, Casalta JP, Habib G, Messana T, et al. Causative organisms of infective endocarditis according to host status. Clin Microbiol Infect. 2004;10(4):302-8. These authors also found that Staphylococcus aureus affects the aortic valve the least. Another important result of our study was that patients with cardiac prostheses were more likely to be affected by bacteria in the “other” category, which may reflect inadequate laboratory techniques or less strict criteria for diagnosing IE.3232. Cannady PB, Sanford JP. Negative blood cultures in infective endocarditis: a review. South Med J. 1976;69(11):1420-4. , 3333. Tunkell AR, Kaye D. Endocarditis with negative blood cultures. N Engl J Med. 1992;326(18):1215-7.

Finally, we should point out that we found Staphylococcus spp. to be the most prevalent pathogen, which agrees with the literature.11. Prendergast BD. The changing face of infective endocarditis. Heart. 2006;92(7):879-85.

2. Cresti A, Chiavarelli M, Scalese M, Nencioni C, Valentini S, Guerrini F, et al. Epidemiological and mortality trends in infective endocarditis, a 17-year population-based prospective study. Cardiovasc Diagn Ther. 2017;7(1):27-35.

3. Sunil M, Hieu HQ, Arjan Singh RS, Ponnampalavanar S, Siew KSW, Loch A. Evolving trends in infective endocarditis in a developing country: a consequence of medical progress? Ann Clin Microbiol Antimicrob. 2019;18(1):43.
- 44. Fowler VG Jr, Miro JM, Hoen B, Cabell CH, Abrutyn E, Rubinstein E, et al. Staphylococcus aureus Endocarditis: A Consequence of Medical Progress. JAMA. 2005;293(24):3012–3021. , 3434. Wu Z, Chen Y, Xiao T, Niu T, Shi Q, Xiao Y. Epidemiology and risk factors of infective endocarditis in a tertiary hospital in China from 2007 to 2016. BMC Infect Dis. 2020;20(1):428. However, we did not observe the reported epidemiological transition toward more cases due to Staphylococcus spp. and fewer cases due to Streptococcus spp. ( Figure 1 ) over the years as consequence of medical progress. Most studies reporting this trend have been conducted in developed countries,11. Prendergast BD. The changing face of infective endocarditis. Heart. 2006;92(7):879-85. and little evidence for such a trend has been found in low/middle income countries, either due to the precariousness of medical systems or the scarcity of new studies.

Limitations

Our study is not without limitations. First, since we performed a retrospective analysis, associations between variables do not necessarily indicate a causal relationship. Second, the sample can be considered small, since we dealt with cases over 15 years at three different centers, as well as the fact that it included many probable IE cases (93 out of 211). However, few studies have been published on the epidemiological profile of Brazilian patients and, to the best of our knowledge, our study involves the largest such sample. It should also be pointed out that most of the probable IE cases involved a negative blood culture, which is related to the use of antibiotics. Third, no data on comorbidity, heart valve disorder, hemodynamic variables, heart failure, abscess formation, or heart valve surgery were collected. Thus, any discussion of mortality must be extremely limited. Finally, it was not possible to collect blood samples for blood culture in 34 patients, either because they received treatment prior to collection or because they began antibiotic therapy before being transferred to tertiary centers.

Conclusion

In conclusion, among the 211 IE cases included in this study, age had the greatest influence on mortality. However, a trend towards reduced or increased mortality was not evident during the study period. Although more infections occurred in native aortic valves in men than women, no specific bacteria stood out. Additionally, in patients whose IE was due to coagulase-negative staphylococci , the mitral valve was less likely to be affected, whereas patients with heart prostheses were more likely to be infected with bacteria in the “other” category. Even though Staphylococcus spp. were the most prevalent pathogen in the sample, we did not observe the epidemiological transition described in literature. Finally, further research is needed to better understand the risk factors associated with mortality in developing countries, especially comorbidities, symptoms present at admission, and the effects of surgical interventions.

References

  • 1
    Prendergast BD. The changing face of infective endocarditis. Heart. 2006;92(7):879-85.
  • 2
    Cresti A, Chiavarelli M, Scalese M, Nencioni C, Valentini S, Guerrini F, et al. Epidemiological and mortality trends in infective endocarditis, a 17-year population-based prospective study. Cardiovasc Diagn Ther. 2017;7(1):27-35.
  • 3
    Sunil M, Hieu HQ, Arjan Singh RS, Ponnampalavanar S, Siew KSW, Loch A. Evolving trends in infective endocarditis in a developing country: a consequence of medical progress? Ann Clin Microbiol Antimicrob. 2019;18(1):43.
  • 4
    Fowler VG Jr, Miro JM, Hoen B, Cabell CH, Abrutyn E, Rubinstein E, et al. Staphylococcus aureus Endocarditis: A Consequence of Medical Progress. JAMA. 2005;293(24):3012–3021.
  • 5
    Watt G, Pachirat O, Baggett HC, Maloney SA, Lulitanond V, Raoult D, et al. Infective endocarditis in northeastern Thailand. Emerg Infect Dis. 2014;20(3):473-6.
  • 6
    Bin Abdulhak AA, Baddour LM, Erwin PJ, Hoen B, Chu VH, Mensah GA, et al. Global and regional burden of infective endocarditis, 1990–2010: a systematic review of the literature. Glob Heart. 2014;9(1):131–143.
  • 7
    Li JS, Sexton DJ, Mick N, Nettles R, Fowler VG Jr, Ryan T, et al. Proposed modifications to the Duke criteria for the diagnosis of infective endocarditis. Clin Infect Dis. 2000;30(4):633–8.
  • 8
    Bezerra RL, Carvalho TF, Batista RS, Silva YM, Campos BF, Castro JHM, et al. Association between Insulin use and Infective Endocarditis: An Observational Study. Int J Cardiovasc Sci. 2019;33(1):14-21.
  • 9
    Damasco PV, Correal JCD, Cruz-Campos ACD, Wajsbrot BR, Cunha RGD, Fonseca AGD, et al. Epidemiological and clinical profile of infective endocarditis at a Brazilian tertiary care center: an eight-year prospective study. Rev Soc Bras Med Trop. 2019;52:e2018375.
  • 10
    Murdoch DR, Corey GR, Hoen B, Miró JM, Fowler VG Jr, Bayer AS, et al. Clinical presentation, etiology, and outcome of infective endocarditis in the 21st century: The International Collaboration on Endocarditis-Prospective Cohort Study. Arch Intern Med. 2009;169(5):463–73.
  • 11
    Wang A, Athan E, Pappas PA, Fowler VG Jr, Olaison L, Paré C, et al. Contemporary clinical profile and outcome of prosthetic valve endocarditis. JAMA. 2007;297(12):1354–61.
  • 12
    Ferreiros E, Nacinovich F, Casabé JH, Modenesi JC, Swieszkowski S, Cortes C, et al. Epidemiologic, clinical, and microbiologic profile of infective endocarditis in Argentina: a national survey. The Endocarditis Infecciosa en la República Argentina-2 (EIRA-2) Study. Am Heart J. 2006;151(2):545-52.
  • 13
    Khan A, Aslam A, Satti KN, Ashiq S. Infective endocarditis post-transcatheter aortic valve implantation (TAVI), microbiological profile and clinical outcomes: A systematic review. PLoS One. 2020;15(1):e0225077.
  • 14
    Joffre J, Dumas G, Aegerter P, Dubée V, Bigé N, Preda G, et al. Epidemiology of infective endocarditis in French intensive care units over the 1997-2014 period-from CUB-Réa Network. Crit Care. 2019;23(1):143.
  • 15
    Ren Z, Mo X, Chen H, Peng J. A changing profile of infective endocarditis at a tertiary hospital in China: a retrospective study from 2001 to 2018. BMC Infect Dis. 2019;19(1):945.
  • 16
    Mistiaen WP. What are the main predictors of in-hospital mortality in patients with infective endocarditis: a review. Scand Cardiovasc J. 2018;52(2):58-68.
  • 17
    Yombi JC, Yuma SN, Pasquet A, Astarci P, Robert A, Rodriguez HV. Staphylococcal versus Streptococcal infective endocarditis in a tertiary hospital in Belgium: epidemiology, clinical characteristics and outcome. Acta Clin Belg. 2017;72(6):417–423.
  • 18
    Kaki R, Al-Abdullah N. Descriptive epidemiological, clinical and microbiological features of infective endocarditis at a University Hospital in Saudi Arabia. Am J Infect Dis. 2018;14(2):63–68.
  • 19
    Nunes MC, Gelape CL, Ferrari TC. Profile of infective endocarditis at a tertiary care center in Brazil during a seven-year period: prognostic factors and in-hospital outcome. Int J Infect Dis. 2010;14(5):e394–8.
  • 20
    Bakir S, Mori T, Durand J, Chen YF, Thompson JA, Oparil S. Estrogen-induced vasoprotection is estrogen receptor dependent: evidence from the balloon-injured rat carotid artery model. Circulation. 2000;101(20):2342–4.
  • 21
    Wichmann MW, Inthorn D, Andress HJ, Schildberg FW. Incidence and mortality of severe sepsis in surgical intensive care patients: the influence of patient gender on disease process and outcome. Intensive Care Med. 2000;26(2):167–72.
  • 22
    Oberholzer A, Keel M, Zellweger R, Steckholzer U, Trentz O, Ertel W. Incidence of septic complications and multiple organ failure in severely injured patients is sex specific. J Trauma. 2000;48(5):932–7.
  • 23
    Aksoy O, Meyer LT, Cabell CH, Kourany WM, Pappas PA, Sexton DJ. Gender differences in infective endocarditis: pre- and co-morbid conditions lead to different management and outcomes in female patients. Scand J Infect Dis. 2007;39(2):101-7.
  • 24
    Castillo JC, Anguita MP, Delgado M, Ruiz M, Mesa D, Romo E, et al. Clinical characteristics and prognosis of infective endocarditis in women. Rev Esp Cardiol. 2008;61(1):36–40.
  • 25
    Martínez-Sellés M, Muñoz P, Arnáiz A, Moreno M, Gálvez J, Rodríguez-Roda J, et al. Valve surgery in active infective endocarditis: a simple score to predict in-hospital prognosis. Int J Cardiol. 2014;175(1):133‐7.
  • 26
    Sevilla T, Revilla A, López J, Vilacosta I, Sarriá C, Gómez I, et al. Influence of Sex on Left-Sided Infective Endocarditis. Rev Esp Cardiol. 2010;63(12):1497–500.
  • 27
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  • Study Association
    This study is not associated with any thesis or dissertation work.
    Ethics approval and consent to participate
    This article does not contain any studies with human participants or animals performed by any of the authors.
  • Sources of Funding: There were no external funding sources for this study.

Publication Dates

  • Publication in this collection
    07 Jan 2022
  • Date of issue
    2022

History

  • Received
    11 Feb 2021
  • Reviewed
    31 Aug 2021
  • Accepted
    19 Sept 2021
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