Mural Endocarditis: The GAMES Registry Series and Review of the Literature

BRIEF REPORT Mural Endocarditis: The GAMES Registry Series and Review of the Literature Andrea Gutie ´rrez-Villanueva .Patricia Mun ˜oz .Antonia Delgado-Montero .Marı ´a Olmedo-Samperio . Arı ´stides de Alarco ´n.Encarnacio ´n Gutie ´rrez-Carretero .Jesu ´s Zarauza .Delia Garcı ´a i Pares . Miguel A ´ngel Goenaga .Guillermo Ojeda-Burgos .Ane Josune Goikoetxea-Agirre . Jose ´M a Reguera-Iglesias .Antonio Ramos .Ana Ferna ´ndez-Cruz on behalf of Spanish Collaboration on Endocarditis—Grupo de Apoyo al Manejo de la Endocarditis infecciosa en Espan ˜a (GAMES) Received: May 7, 2021 / Accepted: June 22, 2021 / Published online: July 26, 2021 ÓThe Author(s) 2021 ABSTRACT Introduction: Mural infective endocarditis (MIE) is a rare type of endovascular infection. We present a comprehensive series of patients with mural endocarditis. Methods: Patients with infectious endocarditis (IE) from 35 Spanish hospitals were prospectively included in the GAMES registry between 2008 and 2017. MIEs were compared to non-MIEs. We also performed a literature search for cases of MIE published between 1979 and 2019 and compared them to the GAMEs series. Results: Twenty-seven MIEs out of 3676 IEs were included. When compared to valvular IE (VIE) or device-associated IE (DIE), patients with MIE were younger (median age 59 years, p\0.01). Transplantation (18.5% versus 1.6% VIE and 2% DIE, p\0.01), hemodialysis (18.5% versus 4.3% VIE and 4.4% DIE, p= 0.006), Supplementary Information The online version contains supplementary material available at https:// doi.org/10.1007/s40121-021-00490-y. A. Gutie ´rrez-Villanueva Internal Medicine Department, Hospital Universitario Puerta de Hierro-Majadahonda, Madrid, Spain P. Mun ˜oz M. Olmedo-Samperio Clinical Microbiology and Infectious Diseases Department, Hospital General Universitario Gregorio Maran ˜o ´n, Madrid, Spain P. Mun ˜oz M. Olmedo-Samperio Instituto de Investigacio ´n Sanitaria Gregorio Maran ˜o ´n, Madrid, Spain P. Mun ˜oz M. Olmedo-Samperio CIBER Enfermedades Respiratorias-CIBERES (CB06/ 06/0058), Madrid, Spain P. Mun ˜oz M. Olmedo-Samperio Facultad de Medicina, Universidad Complutense de Madrid, Madrid, Spain A. Delgado-Montero Echo-Cardiology Unit. Hospital General Universitario Gregorio Maran ˜o ´n, Madrid, Spain A. de Alarco ´n Clinical Unit of Infectious Diseases, Microbiology, and Preventive Medicine, Infectious Diseases Research Group, Institute of Biomedicine of Seville (IBiS), University of Seville/CSIC/University Hospital Virgen del Rocı ´o, Seville, Spain E. Gutie ´rrez-Carretero Cardiac Surgery Department, CIBERCV, Institute of Biomedicine of Seville (IBiS), University of Seville/ CSIC/University Hospital Virgen del Rocı ´o, Seville, Spain J. Zarauza Cardiology Department, Hospital Universitario Marque ´s de Valdecilla, Santander, Spain D. Garcı ´a i Pares Infectious Diseases Service, Hospital Clinic-IDIBAPS, University of Barcelona, Barcelona, Spain D. Garcı ´a i Pares Internal Medicine Service, Clinica Sagrada Familia, Barcelona, Spain Infect Dis Ther (2021) 10:2749–2764 https://doi.org/10.1007/s40121-021-00490-y catheter source (59.3% versus 9.7% VIE and 8.8% DIE, p\0.01) and Candida etiology (22.2% versus 2% DIE and 1.2% VIE, p\0.01) were more common in MIE, whereas the Charlson Index was lower (4 versus 5 in non- MIE, p= 0.006). Mortality was similar.MIE from the literature shared many characteristics with MIE from GAMES, although patients were younger (45 years vs. 56 years, p\0.001), the Charlson Index was lower (1.3 vs. 4.3, p= 0.0001), catheter source was less common (13.9% vs. 59.3%) and there were more IVDUs (25% vs. 3.7%). S. aureus was the most frequent microorganism (50%, p= 0.035). Systemic complications were more common but mortality was similar. Conclusion: MIE is a rare entity. It is often a complication of catheter use, particularly in immunocompromised and hemodialysis patients. Fungal etiology is common. Mortality is similar to other IEs. Keywords: Endocarditis; Mural; Non-valvular endocarditis Key Summary Points Mural endocarditis is a rare but increasingly recognized health careassociated disease that requires a high index of suspicion and a multidisciplinary approach to avoid a relevant morbidity and mortality. It is associated with intravascular catheter use and immunocompromised patients such as transplantation, cancer and hemodialysis patients. Fungal etiology and large vegetations are common in mural endocarditis. INTRODUCTION Mural infective endocarditis (MIE) is a rare type of endovascular infection that involves the nonvalvular endocardium [1–6]. Cases of MIE have been described in Candida and Aspergillus endocarditis [2,7–12] as well as in infective endocarditis (IE) caused by other microorganisms more characteristic of valvular endocarditis (VIE) such as Staphylococcus aureus and Streptococcus. Others have described MIE in intravenous drug users or associated with catheter use [1,5,7,13–17]. Since valves are not involved, diagnosis is often delayed and made only when complications such as systemic or pulmonary embolisms occur, conveying a significant morbidity and mortality. Prognosis of MIE is usually poor according to the literature [3,5,18]. Information about MIE comes from isolated case reports or short series of selected cases. The actual epidemiology, relevance and prognosis are unknown. Data on MIE management and outcome are lacking. We present a series of MIEs from the prospective GAMES registry and a comprehensive review of the literature. M. A ´. Goenaga Infectious Diseases Department, Hospital Universitario Donosti, ISS Biodonostia, San Sebastia ´n, Spain G. Ojeda-Burgos Infectious Diseases Clinical Unit, Hospital Universitario Virgen de La Victoria, Ma ´laga, Spain A. J. Goikoetxea-Agirre Infectious Diseases Department, Hospital Universitario de Cruces, Bilbao, Spain J. M. Reguera-Iglesias Infectious Diseases Department, Hospital Regional Universitario de Ma ´laga, Ma ´laga, Spain A. Ramos A. Ferna ´ndez-Cruz (&) Infectious Diseases Unit, Internal Medicine Department, Hospital Puerta de Hierro- Majadahonda, Madrid, Spain e-mail: [email protected] 2750 Infect Dis Ther (2021) 10:2749–2764 METHODS Study design Between January 2008 and June 2018, consecutive patients with IE according to the Duke criteria were prospectively included in the ‘‘Spanish Collaboration on Endocarditis— Grupo de Apoyo al Manejo de la Endocarditis Infecciosa en Espan ˜a (GAMES)’’ registry, which is maintained by 35 Spanish hospitals. Multidisciplinary teams evaluated every case and completed standardized case report forms for each IE episode, including clinical, microbiologic and echocardiographic sections and follow-up data. Literature search Additionally, we performed a PubMed search that included the search term: ‘‘mural endocarditis.’’ We filtered case reports and case series and omitted cases that included valvular or intracardiac device involvement. Inappropriate and inaccessible posts were excluded. A standardized form adapted from that of the GAMES registry was filled in for each literature MIE with enough available information and included in a database. The list of cases included in the literature review is accessible in Supplementary material. Definitions We considered MIE cases with non-valvular endocardium involvement. Cases with both mural and valvular involvement were excluded from the analysis, as were cases of endovascular infection that could be considered endarteritis (involving great vessels, ductus arteriosus, etc.). We considered as non-mural endocarditis those cases of infective endocarditis that involved valvular endocardial surfaces [valvular endocarditis (VIE) or those with vegetations involving intra-cardiac devices (pacemakers, implantable cardioverter defibrillators) deviceassociated endocarditis (DIE)]. IE was defined according to the modified Duke criteria [19]. Age-adjusted Charlson Comorbidity Index was used to quantify comorbidities [20]. Place of acquisition of IE was defined following ICE recommendations [21]. The catheter was considered as the source of endocarditis when the etiologic microorganism was detected in both the catheter and the blood cultures or surgical samples (vegetation, valve or implantable device), or when, from a clinical standpoint, the treating physician considered the catheter was the source. All patients were evaluated by cardiac surgeons to determine the need for surgery according to international indications [22]. The final decision on surgery was made in agreement with the multidisciplinary endocarditis team at each center. Both in-hospital mortality (overall mortality rate during the hospital stay) and 1-year mortality were analyzed. Data analysis Cases with MIE were compared to cases with non-valvular endocarditis in the GAMES registry (both VIE and DIE). MIEs from the GAMES registry were compared to cases of MIE from the literature. The quantitative variables were expressed as mean and standard deviation or median and interquartile range; qualitative variables were expressed as frequency and percentage. Continuous variables were compared using the ttest, and categorical variables were compared using the v 2 test or Fisher’s exact test when the v 2 test was not appropriate. All statistical analyses were performed with SPSS version 25 software (IBM SPSS Statistics 22.0, Armonk, New York, NY: IBM Corp.). Ethics The study and the common case report form were approved by the local and national institutional review boards and ethics committees (Comite ´e ´tico de Investigacio ´n Clı ´nica Regional de la Comunidad de Madrid CEIC-R; EC 18/07; date 11/01/2008). Infect Dis Ther (2021) 10:2749–2764 2751 RESULTS During the study period 3767 patients were included. Of them, 27 MIE (0.7% of total endocarditis) and 3649 non-mural endocarditis [407 (11.1%) DIE and 3242 (88.2%) VIE] were registered in the GAMES database. Moreover, 36 cases from the literature review that provided enough information to analyze were selected. Differences between mural and non-mural endocarditis in the GAMES registry General characteristics of mural (Fig. 1) and non-mural endocarditis from the GAMES registry are displayed in Table 1. Compared to non-MIE, patients with MIE were significantly younger, and MIE was more prevalent in women. Patients with MIE presented a lower age-adjusted Charlson Comorbidity Index, were receiving hemodialysis more often and transplantation was more frequent as underlying disease. Furthermore, in contrast with VIEs, which were mainly community-acquired (61.7%), the majority of MIEs were hospital-acquired (63%). DIEs were more common in a nosocomial setting and related to medical care. A striking difference was found in the proportion of MIEs originating from the catheter, which was very high (59.3%) compared to non- MIEs with catheter source (8.8% and 9.7% in DIE and VIE, respectively) (p\0.01). The microorganisms most frequently implicated in endocarditis in all groups were Staphylococci, with a prevalence in MIEs of 29.6%, being 14.8% S. aureus and S. coagulase negative each, followed by Streptococci (25.9%). Streptococci were significantly more frequent in MIE and VIE (27.5%) than in DIE (8.1%). Significant differences were found between groups regarding Candida etiology (22.2% among MIE versus 2% in DIE and 1.2% in VIE, p\0.01). Aspergillus was more common in MIE, though without statistical significance (3.7% among MIE vs. 0.2% in DIE and 0.3% in VIE, p= 0.144). Fig. 1 Simultaneous bi-plane imaging by transesophageal echo showing a large sessile heterogeneous mass (3.9 92.8 cm) attached to the lateral and inferior wall of the right atrium, with irregular contour. The tricuspid valve and inferior vena cava were not affected 2752 Infect Dis Ther (2021) 10:2749–2764 Table 1 Infective endocarditis in the GAMES registry: mural compared to valvular and device-associated endocarditis Variables A B C pvalue Mural (MIE) (N= 27) Device (DIE) (N= 407) Valvular (VIE) (N= 3242) Age, median (IQR) 59 (46–67) 71 (62–79) 69 (57–77) \0.01 a.c Sex (male) 11 (40.7) 297 (72.9) 2160 (66.6) 0.001 a Lung disease 8 (29.6) 94 (23.0) 570 (17.5) 0.167 Coronary disease 5 (18.5) 149 (36.6) 809 (24.9) 0.09 Heart failure 10 (37.0) 194 (47.7) 1022 (31.5) 0.001 b Diabetes 3 (11.1) 154 (37.8) 892 (27.5) 0.009 a Trasplantation 5 (18.5) 8 (2.0) 54 (1.6) \0.01 a.c Heart 2 (7.4) 1 (0.2) 3 (0.1) 0.002 a,c Lung 0 0 3 (0.1) 0.761 PM/ICD 2 (7.4) 407 (100.0) 262 (8.0) \0.01 a.b Peripheral arterial disease 2 (7.4) 49 (12.0) 341 (10.5) 0.678 Cerebrovascular disease 3 (11.1) 43 (10.6) 435 (13.4) 0.946 Neoplasm 6 (22.2) 36 (8.8) 528 (16.2) 0.001 b Congenital cardiopathy 3 (11.1) 16 (3.9) 181 (5.5) 0.202 Prior kidney disease 8 (29.6) 127 (31.2) 766 (23.6) 0.001 b Prior hemodialysis 5 (18.5) 18 (4.4) 140 (4.3) 0.006 a.c Liver disease 3 (11.1) 20 (4.9) 352 (10.8) 0.003 b IVDU 1 (3.7) 0 78 (2.4) 0.847 Age-adjusted-Charlson Index 4 (2–6) 5 (3–7) 5 (3–7) 0.006 a.c Place of acquisition Community acquired 7 (25.9) 156 (38.2) 2001 (61.7) 0.007 b.c Hospital acquired 17 (63.0) 184 (45.2) 874 (26.9) \0.01 b.c Health care associated 3 (11.1) 46 (11.3) 250 (7.7) 0.766 Catheter source 16 (59.3) 36 (8.8) 313 (9.7) \0.01 a.c Etiology Staphylococcus aureus 4 (14.8) 125 (30.7) 708 (21.8) \0.01 b CNS 4 (14.8) 123 (30.2) 515 (15.9) \0.01 b Enterococcus 1 (3.7) 20 (4.9) 482 (14.9) \0.01 b Streptococcus 7 (25.9) 33 (8.1) 893 (27.5) \0.01 a.b Candida 6 (22.2) 8 (2.0) 39 (1.2) \0.01 a.c Infect Dis Ther (2021) 10:2749–2764 2753 Table 1 continued Variables A B C pvalue Mural (MIE) (N= 27) Device (DIE) (N= 407) Valvular (VIE) (N= 3242) Unknown etiology 0 35 (8.6) 296 (9.1) 0.795 Enterobacteriaceae 2 (7.4) 10 (2.4) 69 (2.1) 0.225 Neisseria spp. 0 0 2 (0.6) 0.533 Aspergillus spp 1 (3.7) 1 (0.2) 9 (0.3) 0.144 Polymicrobial 2 (7.4) 17 (4.1) 45 (1.4) 0.071 Clinical characteristic Vegetation size (mm), median (IQR) 22 (8–39) 12 (7–18) 10 (7–16) \0.01 a.c Intracardiac complication 1 (3.7) 15 (3.7) 1099 (33.9) \0.01 b.c Perforation/rupture 0 7 (1.7) 495 (15.2) \0.01 b Pseudoaneurysm 0 0 199 (6.1) \0.01 b Abscess 0 6 (1.4) 557 (17.1) \0.01 b Intracardiac fistula 0 1 (0.2) 88 (2.7) 0.004 b Vascular phenomena 3 (11.1) 9 (2.2) 310 (9.5) 0.033 a.b Heart murmur 4 (14.8) 35 (8.6) 1225 (37.7) 0.001 b.c Heart failure 5 (18.5) 76 (18.6) 1383 (42.6) \0.01 b.c Persistent bacteremia 5 (18.5) 51 (12.5) 374 (11.5) 0.408 Central nervous system involvement 1 (3.7) 18 (4.4) 705 (21.7) 0.041 b.c Embolism 6 (22.2) 60 (14.7) 683 (21.0) 0.003 b Kidney failure 5 (18.5) 140 (34.3) 1175 (36.2) 0.087 Septic shock 5 (18.5) 34 (8.3) 416 (12.8) 0.173 Sepsis 3 (11.1) 54 (13.2) 552 (17.0) 0.576 Surgical indication 9 (33.3) 337 (82.8) 2102 (65.3) \0.01 a.b.c Cardiac surgery 5 (18.5) 314 (77.1) 1382 (42.6) \0.01 a.b.c In-hospital mortality 5 (18.5) 58 (14.3) 913 (28.2) \0.01 b 1-year mortality 2 (7.4) 22 (5.4) 206 (6.3) 0.863 a Significant differences between A–B b Significant differences between B–C c Significant differences between A–C 2754 Infect Dis Ther (2021) 10:2749–2764 Table 2 Mural infective endocarditis: GAMES registry versus literature review Variables (%) Games (N= 27) (%) Literature (N= 36) (%) pvalue Total (N= 63) Age, median (IQR) 56 (46–67) 45 (29–57) 0.001 52.5 (35.3–64) Sex (male) 11 (40.7) 22 (61.1) 0.132 33 (52.3) Lung disease 8 (29.7) 2 (5.6) 0.011 10 (16.4) Coronary disease 5 (18.5) 0 (0) 0.010 5 (7.9) Heart failure 10 (37) 0 (0) 0.000 10 (15.8) Diabetes 3 (11.1) 3 (8.3) 1.000 6 (9.5) Trasplantation 5 (18.5) 1 (2.8) 0.076 6 (9.5) Heart 2 (7.4) 0 2 (33.3) Kidney 0 1 (2.8) 1 (16.7) PM/ICD 2 (7.4) 0 (0) 0.180 2 (3.1) Peripheral arterial disease 2 (7.4) 1 (2.8) 0.572 3 (4.8) Cerebrovascular disease 3 (11.1) 1 (2.8) 0.305 4 (6.3) Neoplasm 6 (22.2) 4 (11.1) 0.303 10 (15.9) Congenital cardiopathy 3 (11.1) 4 (11.1) 1.000 7 (11.1) Prior kidney disease 8 (29.6) 2 (5.6) 0.014 10 (15.9) Prior hemodialysis 5 (18.5) 1 (2.8) 0.076 6 (9.5) Liver disease 3 (11.1) 6 (16.7) 0.720 9 (14.3) IVDU 1 (3.7) 9 (25) 0.034 10 (15.9) Age-adjusted Charlson Index 4.3 (DE 2.7) 1.3 (DE 2.2) 0.000 2.7 Place of acquisition 0.0001 Community acquired 7 (25.9) 25 (69.4) 32 (50.8) Hospital acquired 17 (63) 5 (13.9) 22 (34.9) Health care associated 3 (11.1) 6 (16.7) 9 (14.3) Catheter source 16 (59.3) 5 (13.9) 0.000 22 (34.9) Etiology 0.342 Staphylococcus aureus 4 (14.8) 18 (50) 0.035 22 (34.9) CNS 4 (14.8) 0 0.074 3 (4.8) Enterococcus 1 (3.7) 0 0.429 1 (1.6) Streptococcus 7 (25.9) 8 (22.2) 0.772 15 (23.8) Candida 6 (22.2) 3 (8.3) 0.155 9 (14.3) Enterobacteriaceae 2 (7.4) 1 (2.8) 0.572 3 (4.8) Aspergillus spp 1 (3.7) 4 (11.1) 0.381 5 (7.9) Infect Dis Ther (2021) 10:2749–2764 2755 Table 2 continued Variables (%) Games (N= 27) (%) Literature (N= 36) (%) pvalue Total (N= 63) Polymicrobial 2 (7.4) 0 0.180 2 (3.2) Unknown etiology 0 2 (5.6) 0.502 2 (3.2) Clinical characteristics Vegetation size (mm), median (IQR) 22 (8–39) 20 (13–33) 0.910 22 (12–22) Vegetation location 0.0001 Right ventricle 5 (18.5) 9 (25) 14 (22.1) Left ventricle 1 (3.7) 17 (47.2) 18 (28.6) Right auricular 14 (51.9) 4 (11.1) 18 (28.6) Left auricular 2 (7.4) 6 (16.7) 8 (12.7) Septum 1 (3.7) 0 1 (1.6) Superior vena cava 3 (11.1) 0 3 (4.8) Tendinous chords 1 (3.7) 0 1 (1.6) Intracardiac complication 1 (3.7) 5 (13.9) 0.226 6 (9.5) Perforation/rupture 0 2 (5.6) 0.502 2 (3.2) Pseudoaneurysm 0 1 (2.8) 1.000 1 (1.6) Abscess 0 2 (5.6) 0.502 2 (3.2) Intracardiac fistula 0 0 0 (0) Others 1 (3.7) 0 1 (1.6) Vascular phenomena 3 (11.1) 8 (22.2) 0.332 11 (17.5) Heart murmur 4 (14.8) 5 (13.9) 0.207 10 (15.9) Heart failure 5 (18.5) 1 (2.8) 0.076 6 (9.5) Persistent bacteremia 5 (18.5) 3 (8.3) 0.262 8 (12.7) Central nervus system involvement 1 (3.7) 15 (41.7) 0.001 16 (25.4) Embolism 6 (22.2) 24 (66.7) 0.002 31 (49.2) Kidney failiure 5 (18.5) 11 (30.6) 0.383 16 (25.4) Septic shock 5 (18.5) 10 (27.8) 0.552 15 (23.8) Sepsis 3 (11.1) 10 (27.8) 0.128 13 (20.6) Surgical indication 9 (33.3) 21 (58.3) 0.036 30 (47.6) Cardiac surgery 5 (18.5) 14 (38.9) 0.101 19 (30.2) In-hospital mortality 5 (18.5) 9 (25) 0.365 13 (20.6) 1-year mortality 2 (7.4) 1 (2.8) 0.577 3 (4.8) 2756 Infect Dis Ther (2021) 10:2749–2764 Fig. 2 Distribution by calendar year of the cases of mural endocarditis from the literature (blue) and those from the GAMES registry (orange) GAMES LITERATURE 2 1 5 1ª 1c 14 3b 9 17 4 6 Fig. 3 Location of mural endocarditis. a: Septum. b: Vena cava. c: Tendinous chords. 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