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Acute ischemic stroke treated with mechanical thrombectomy and fungal endocarditis: A case report and systematic review of the literature
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Acute ischemic stroke treated with mechanical thrombectomy and fungal endocarditis: A case report and systematic review of the literature Alessandro Sgreccia a,∗ , Giuseppe Carità b , Oguzhan Coskun c , Federico Di Maria c , Hakim Benamer d , Marie Tisserand c , Anthony Scemama d , Georges Rodesch c , Bertrand Lapergue e , Arturo Consoli c a
Department of Radiology, Ospedali Riuniti, Ancona, Italy Department of Radiology, Azienda Ospedaliero Universitaria Ferrara, Ospedale Sant’ Anna Cona, Ferrara, Italy c Department of Diagnostic and Interventional Neuroradiology, Foch Hospital, Suresnes, France d Department of Cardiology, Foch Hospital, Suresnes, France e Division of Neurology, Stroke Center, Foch Hospital, University Versailles Saint-Quentin en Yvelines, Suresnes, France b
a r t i c l e Article history: Available online xxx Keywords: Stroke Candida Endocarditis Clot Histopathology Stent
i n f o
a b s t r a c t Fungal endocarditis is a rare clinical form of infective endocarditis. The main etiology of FE is Candida albicans but also Candida parapsilosis and the overall mortality is high. We report a case of an acute ischemic stroke treated by mechanical thrombectomy, with the histopathological analysis of the retrieved clot followed by the confirmation of fungal endocarditis. An extensive review of the literature has been proposed and three key points concerning the fungal endocarditis predisposing factors, the relation between thrombolysis and hemorrhagic risk and, finally, the importance of clot analysis have been discussed. © 2019 Elsevier Masson SAS. All rights reserved.
Introduction
Case report
The incidence of infectious endocarditis in stroke patients lies between 8% and 11% according to some studies analyzing the impact of transesophageal echocardiography (TEE) [1,2]. Fungal endocarditis (FE) is a rare clinical form of infective endocarditis accounting for 1.3% to 6% of cases [3,4]. Among this population, males seem to be more frequently affected, associated with a mean age of about 44–48 years [3,5]. The main etiology of FE, reported in the literature in different proportions, is Candida spp, detected in 53–67.8% of cases, and the most frequent pathogens are C. albicans (26–48%) and C. parapsilosis (19–33%) [3,4,5,6]. FE is associated with a high overall mortality (63.6%), with a rate of 54% and 79% related to the aortic andmitral valves, respectively. We report here a case of acute ischemic stroke treated by mechanical thrombectomy (MT) followed by histopathological analysis of the clot and a diagnosis of fungal endocarditis.
Admission and acute treatment
∗ Corresponding author at: Department of Radiology, Ospedali Riuniti, via Conca, 71, 60126 Torrette, Ancona AN, Italy. E-mail address: [email protected] (A. Sgreccia).
A 31-year-old male patient was referred to our institution one hour after the onset of a sudden left hemiplegia, homonymous lateral hemianopia, hemispacial neglect, dysarthria and hypoesthesia with an initial NIHSS of 18 (baseline mRS0). The patient suffered from hemorrhagic recto-colitis and was under treatment with azathioprine, 50 mg/day since 2015. A mild fever (37.5 ◦ C), treated by antibiotics 10 days before, was reported. An aortic murmur was detected without any sign of heart failure. White blood cell count was normal. Red blood cell count was 3.64 × 1012 /L (normal values: 4.60–6.20 × 1012 /L) and hemoglobin was 8.7 gr/dL. C-reactive protein level was 52.2 mg/L (normal values: < 3 mg/L). Magnetic resonance imaging (MRI) showed an acute right superficial temporo-fronto-insular ischemia (DWI-ASPECTS 5) without hyperintensity in the FLAIR sequence. MR-angiography showed a T-type occlusion of the right internal carotid bifurcation. Intravenous r-tPA was administered 96 minutes after the onset of symptoms and the patient was immediately transferred to the angio-suite for MT. Onset-to-groin puncture was 125 minutes. MT was performed by a 6 × 24 mm solitaire platinum stent-like
https://doi.org/10.1016/j.neurad.2019.03.003 0150-9861/© 2019 Elsevier Masson SAS. All rights reserved.
Please cite this article in press as: Sgreccia A, et al. Acute ischemic stroke treated with mechanical thrombectomy and fungal endocarditis: A case report and systematic review of the literature. J Neuroradiol (2019), https://doi.org/10.1016/j.neurad.2019.03.003
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Fig. 1. Baseline MRI at the admission. A. DWI sequence showing the ischemic lesion in the fronto-temporo-insular area, without FLAIR hyper-intensity (B); C. 3D-TOF sequence reconstruction showing the right ICA occlusion; Pre- (D) and Post-treatment (E) DSA, anteroposterior view: complete recanalization of the MCA occlusion after 1 maneuver of Mechanical Thrombectomy. F. Retrieved clot after washing out with saline, white-colored aspect.
retriever (Medtronic, Irvine, California) and a balloon guiding catheter (Cello 9F; Medtronic, Irvine, California). A complete recanalization (mTICI 3) was achieved after the first maneuver (time-to-reperfusion: 140 minutes) and the clot (Fig. 1) was sent for histopathological examination, according to our systeatic protocol.
Clinical evolution Two days after the procedure the patient completely recovered (NIHSS: 0). The MRI performed 24 hours after MT showed a regression of the insular superficial lesions (DWI-ASPECTS 8) and no hemorrhagic infarction. During the first hours of hospitalization in the stroke unit after the MT, fever (40.1 ◦ C) associated with hypotension and tachycardia was observed, requiring hydration and antibiotics. Anamnestic and clinical data gave rise to the suspicion of endocarditis and therefore TEE, blood cultures and microbiological analysis on the clot were performed. A type 0 bicuspid aortic valve with a 5 × 7 mm vegetation on both cusps was observed. Polymerase-chain-reaction (PCR) analysis performed on the clot revealed the presence of Candida parapsilosis, which was confirmed also by blood cultures. Furthermore, a thoraco-abdominal computed tomography (CT) scan showed a deep venous popliteal thrombosis associated with multiple renal and splenic ischemic lesions. The diagnosis was an ischemic stroke secondary to fungal endocarditis (FE) with systemic involvement. Anamnesis and lab tests excluded any immunodeficiency disorders or drug abuse. Medical therapy was set up with low molecular weight heparin (tinzaparin sodium 12 000 IU/day), i.v. cloxacillin 200 mg/kg/day, amoxicillin 200 mg/kg/day, gentamicin 3 mg/kg/day and i.v. amphotericin B 300 mg/day plus i.v. flucitosyn (Ancotil) 1800 mg every 6 hours.
Sub-acute management Eight days after the initial treatment, Candida persisted in blood cultures, a thickening of the vegetation was observed and a retinal embolus was detected. This suggested an indication for a biological aortic valve replacement. Sixteen days after the ischemic event the patient was still complaining of persistent headaches. MRI was performed and showed a small (1 cm) right temporo-occipital hematoma associated with some enhanced vascular structures within the hematoma. Digital subtraction angiography showed two small mycotic aneurysms (MAs) located at the level of two branches of the right posterior temporal artery, associated with local vasospasm. After multidisciplinary discussion, the indication for a super-selective embolization of the two MAs was advanced in order to prevent re-bleeding and to ensure a safe valve replacement. The embolization was performed by placing a microcatheter Magic 1.2F (Balt Extrusion, Montmorency, France) close to the origin of the two small branches and by injecting a mixture of 0.2 mL of glue (Glubran2, GEM, Viareggio, Italy) and lipiodol (Guerbet France, Villepinte) at a 50% dilution (Fig. 2). During the follow-up the patient experienced a progressive improvement of his clinical condition and a reduction in the vegetation thickness was observed. At this stage, after a multidisciplinary discussion we decided not to perform the valve replacement and to continue the follow-up. The patient was finally discharged in a good and stable clinical condition with continuation of the anti-fungal therapy.His mRS was 0 at three months. Materials and methods The collection of clinical data was approved by the institutional review board. An extensive review of the literature regarding MT performed in patients with FE was performed. We searched
Please cite this article in press as: Sgreccia A, et al. Acute ischemic stroke treated with mechanical thrombectomy and fungal endocarditis: A case report and systematic review of the literature. J Neuroradiol (2019), https://doi.org/10.1016/j.neurad.2019.03.003
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Fig. 2. MRI performed 16 h after the ischemic event. A. SWI sequence, axial plane, showing the right occipital hematoma; B. DSA, anteroposterior view showing the two mycotic aneurysms (black arrow) with an associated local vasospasm; C. MR-XperCT fusion confirming the anatomical correlation of the mycotic aneurysms in the context of the hematoma (white arrow); D. DSA, super-selective embolization of the two aneurysms by glue. E. Post-treatment angiogram.
in the PubMed database using keywords such as “infective endocarditis” AND “stroke” AND “thrombectomy” OR “fungal thrombus retrieval”. For the purpose of our review, we considered any case report or case series of FE and related ischemic stroke treated by thrombectomy with associated clot analysis. Sixteen articles matched our research filters. Three further papers were excluded because clot retrieval occurred in other organs (Fig. 3). Results Including our patient, 27 cases of MT of ischemic stroke related to infective endocarditis were found. Age and sex were not available for three patients; in the remaining 24 cases the mean age was 57 years (range 24–80 years) with a total of 12 male patients. The occlusion site was mainly MCA-M1: 14/27 cases (51.8%), with MCA-M2 in 6/27 cases (22.2%), ICA in 5 cases (18.5%) and basilar occlusion in 2 cases (7.5%). Except for 4 cases with missing data regarding the microorganism, all stroke cases were related to a bacterial pathogen that was identified through blood cultures and in 10 cases there was histological confirmation of the septic embolus. All patients underwent thrombectomy but 8/27 cases (29.6%) received i.v. thrombolysis and another 2 (7.4%) received combined i.a. thrombolysis. The recanalization rate was 79% (19/24 cases with TICI 2b-3 scores, including our patient). In three cases reported by Sveinsson et al. [7] it was not possible to extrapolate the exact grade of recanalization. Favorable clinical outcome was variably reported in 20 patients (74%) and 3 patients died (3/27, 11%) (Table 1). All patients received antibiotic or anti-fungal therapy. Discussion Predisposing factors In our review, the main predisposing factor was of cardiac valvular origin such as a prosthetic implant or other valvulopathies (15/27, 55.5%). One case reported intravenous drug abuse with immunodeficiency (1/27, 3.7%). Eleven patients had no apparent
predisposing factor for endocarditis (11/27, 40.8%). Although our patient had no history of immunodeficiency disorders or drug abuse, the bicuspid aortic valve and the immunosuppressive therapy with azathioprine for hemorrhagic rectocolitis were probably related to the FE. Intravenous Thrombolysis and Hemorrhagic risk The hemorrhagic risk in the infective endocarditis (bacterial and fungal) population lies between 3-7%, generally related to the hemorrhagic conversion of an ischemic stroke due to a septic embolus. Thus the conversion seems to be secondary to the development and subsequent rupture of a mycotic aneurysm or of a very fragile vessel caused by immune complex arteritis [7,9]. The mortality in this condition could reach rates close to 80% [9]. Intravenous thrombolysis is contraindicated by 2018 AHA Guidelines [10] in patients with symptoms consistent with infective endocarditis because of an expected increased risk of hemorrhagic transformation. However, the data supporting this recommendation (Grade III) are weak. In our review, i.v. thrombolysis was administered in 8 patients, while intra-parenchymal hemorrhage was reported only in our case 16 days after the initial event. A limited subarachnoid hemorrhage was described in another case [11] but no mycotic aneurysms were identified with MRI. Despite the small sample size, these observations could suggest that rapidly delivered MT [26,27], associated with i.v. thrombolysis when possible, might be safe and effective in cases of very acute infective endocarditis. Clot analysis Another issue that should be considered is the composition of the clot. In our review only 10 cases reported the results of clot analysis and examination of the type of clot. In 4 cases, standalone Gram staining was performed and was associated with blood cultures except for 1 case. Hematoxylin-eosin staining was performed in 3 cases and in two of these Gomori’s trichrome staining was also associated. Molecular biological examination of the clot was reported in 2/10 cases but no description of the technique used was provided.
Please cite this article in press as: Sgreccia A, et al. Acute ischemic stroke treated with mechanical thrombectomy and fungal endocarditis: A case report and systematic review of the literature. J Neuroradiol (2019), https://doi.org/10.1016/j.neurad.2019.03.003
Localization of occlusion
Pathogen
Type of analysis on the clot
Onset NIHSS Score
Thrombectomy
Recanalization Clinical Outcome
ICH
Mycotic AneurysmTreatment
Bain, et al. [12] 2011
24/F
ICA
Methicillinresistant Staphylococcus Epidermidis
No-Blood Cultures
18
yes + i.v. thrombolysis
TICI 2b
NIHSS 2 at 2 months
No
No
Dababneh, et al. [13] 2012
67/F
post-pregnancy non-ischemic dilated cardiomyopathyBacteremia Bovine prosthetic valve already implanted
MCA - M1
Gram negative Vancomycin resistant rods
No-Blood Cultures
NA
yes
TICI 2b
No
No
Liang, et al. [14] 2012
70/F
No
MCA - M2
No-Blood Cultures
24
yes
TICI 3
No
No
Sukumaran, et al. [15] 2012
33/M
Rheumatic Mitral Stenosis
MCA - M1
group B Streptococcus agalactiae Alpha Hemolytic Streptococci
14
yes
TICI 2b
No
No
Kan, et al. [16] 2012
78/F
(Mitral Valve Prolapse)
MCA - M2
Streptococci Viridans
16
yes
TICI 3
No
No
Kang, et al. [17] 2013
39/F
No
MCA - M1
Streptococcus Gordonii
Blood Cultures-Gram’s stain Blood CulturesCultures of the embolus No-Blood Cultures
NA poor outcome for causes not related to brain infarction Completely recovered to the baseline NIHSS 0 at 4 days
16
TICI 2b
No
No
Kim, et al. [18] 2014
40/F
No
MCA - M1
Streptococcus Mitis
15
yes + i.a. thrombolysis (urokinase + tirofiban) yes
No
No
Ladner, et al. [19] 2014 Toeg, et al. [20] 2014 Scharf, et al. [21] 2016
40/NA
i.v. opiate use
yes
TICI 3
No
No
No
20
No
No
Mitral Valve already implanted No Aortic Valve already implanted Prosthetic Mitral Valve already implanted Prosthetic Mitral Valve already implanted No
yes + i.v. thrombolysis yes
TICI 2b
NA
Enterococcus Faecalis Gram positive cocci dead gram coccal forms
3
73/M
Partial Occlusion M1 ICA
No
No
NA NA
Sveinsson, et al. [8] 2016
33/M
67/M
39/F
MCA - M1
Blood Cultures-Gram’s stain No-Blood Cultures No-Blood Cultures Gram’s stain
12
TICI 3
TICI 3
NIHSS 12 at 24 hrs poor outcome NIHSS 3 at 4 weeks of medical therapy NIHSS 3 at 3 days mRs 2 at 3 months NIHSS 0 and mRs 0 at 13 days NIHSS 0 at 8 months NIHSS 1
MCA - M2 MCA - M1
NA NA
NA NA
18 19
yes yes + i.v. thrombolysis
TICI 3 TICI 2a
NIHSS 5 NIHSS 17 poor outcome
No No
No No
MCA - M1
Serratia Marcescens
No-Blood Cultures
14
yes
NA
NIHSS 1 at discharge
No
No
MCA - M1
Enterococcus Faecalis
No-Blood Cultures
13
yes
NA
NIHSS 3 at discharge
No
No
MCA - M2
Staphylococcal sepsis
No-Blood Cultures
15
yes
NA
NIHSS 4 at discharge
No
No
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Please cite this article in press as: Sgreccia A, et al. Acute ischemic stroke treated with mechanical thrombectomy and fungal endocarditis: A case report and systematic review of the literature. J Neuroradiol (2019), https://doi.org/10.1016/j.neurad.2019.03.003
Table 1 Review of mechanical thrombectomy cases related to infective endocarditis.
Predisposing factors
Localization of occlusion
Pathogen
Type of analysis on the clot
Onset NIHSS Score
Thrombectomy
Recanalization Clinical Outcome
ICH
Mycotic AneurysmTreatment
Ambrosioni, et al. [22] 2017
79/M
Prosthetic Valve already implanted Prosthetic Mitral Valve already implanted
Tandem (Carotid - M1)
Staphylococcus Aureus
No-Blood Cultures
9
yes
TICI 0
mRs 6
No
No
Basilar
Staphylococcus Oralis
10
yes
TICI 3
NIHSS 2 at 24 hrs
No
No
56/F 72/M
No No
MCA - M1 Basilar
NA Streptococcus Dysgalactiae
19 35
yes yes
TICI 3 TICI 3
NIHSS 2 at 24 hrs mRs 6
No No
No No
79/F
Prosthetic Valve already implanted Prosthetic Valve already implanted Prosthetic Valve already implanted
MCA - M1
NA
Blood CulturesMolecular Biology of the thrombus NA Blood CulturesMolecular Biology of the thrombus NA
5
yes
TICI 2b
NIHSS 2 at 24 hrs
No
No
MCA - M1
Staphylococcus Epidermidis
No-Blood Cultures
8
yes
TICI 3
mRs 6
No
No
MCA - M1
Staphylococcus Epidermidis
Gram’s stain Hematoxylin and Eosin stain -Blood Cultures Hematoxylin & Eosin stain Gram and Gomori trichrome - Blood Culture Hematoxylin and Eosin stain Gram and Gomori trichrome - Blood Culture Gram’s stain
16
yes + i.v. thrombolysis
TICI 3
NIHSS 2 at 24 hrs, mRs 1 at 5 days after procedure
No
No
13
yes + i.v. thrombolysis
TICI 2b
mRs1 at 3 months
No
No
15
yes + i.v. thrombolysis
TICI 2b
mRs 2 at 3 months
No
No
18
yes + i.v. thrombolysis
TICI 0
NIHSS 12 at 18 months, poor outcome
micro-sub aracnoid Hemorrhage
yes + i.a. thrombolysis (rt-PA 5 mg) yes + i.v. thrombolysis
TICI 2b
NIHSS 0 at 4 weeks
No
TICI 3
NIHSS 0 at 2 days
yes
Suspect but no evidence at MRA No endovascular treatment No – Cerebral Abscesses in MCA Territory yes – glue embolization
69/F
85/M
Bhaskar, et al. [23] 2017
36/M
HernandezFernandez, et al. [24] 2017
57/M
Prosthetic Valve already implanted
ICA
S.Sanguinis
66/M
No
ICA
S.Bovis
Nakanishi, et al. [11] 2017
80/F
No
MCA - M2
Gram positive cocci
Bolognese, et al. [25] 2018
42/M
No
MCA - M2
Streptococcus Viridans
Blood Cultures
3
Sgreccia, et al. 2018
31/M
Medical therapy with AZT for hemorrhagic rectocolitis Bicuspid Aortic Valve
ICA
Candida Parapsilosis
Blood CulturesMolecular Biology of the thrombus
18
i.v: intravenous; i.a.: intra-arterial; AZT: azathioprine; hrs: hours.
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Please cite this article in press as: Sgreccia A, et al. Acute ischemic stroke treated with mechanical thrombectomy and fungal endocarditis: A case report and systematic review of the literature. J Neuroradiol (2019), https://doi.org/10.1016/j.neurad.2019.03.003
Table 1 (Continued)
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Fig. 3. Prisma flow-diagram.
In one case the clot specifically underwent microbiological cultures. In our case a PCR was performed, which revealed the presence of a consistent amount of Candida parapsilosis DNA via the amplification of the ITS-1 (internal transcribed spacer) gene inside the clot (threshold cycle: 12). The major causative pathogens reported in the review are Streptococcus spp. in 9/26 cases, 6 Staphylococcus spp. in 6 cases, Enterococcus faecalis in 2 cases and Serratia marcescens in 1 case. The other results were not pathogen-specific and authors reported only “Cocci Gram positive” or “negative” [11,13,20,21]. Our report is, to our knowledge, the only one reporting the presence of Candida parapsilosis inside the clot and associated with FE.
Conclusion Systematic microbiological analysis of the removed clot should be considered in patients with acute ischemic stroke caused by infective endocarditis.
Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Disclosure of interest The authors declare that they have no competing interest.
Acknowledgments We thank Mary Osborne-Pellegrin for help in editing the final draft of the manuscript.
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[17] Kang G, Yang TK, Choi JH, Heo ST. Effectiveness of mechanical embolectomy for septic embolus in the cerebral artery complicatedwith infective endocarditis. J Korean Med Sci 2013;28(8):1244–7, http://dx.doi.org/10.3346/jkms.2013.28.8.1244. [18] Kim JM, Jeon JS, Kim YW, Kang DH, Hwang YH, Kim YS. Forced arterial suction thrombectomy of septic embolic middle cerebral artery occlusion due to infective endocarditis: an illustrative case and review of the literature. Neurointervention 2014;9(2):101–5, http://dx.doi.org/10.5469/neuroint.2014.9.2.101. [19] Ladner TR, Davis BJ, He L, Kirshner HS, Froehler MT, Mocco J. Complex decision-making in stroke: preoperative mechanical thrombectomy of septic embolusfor emergency cardiac valve surgery. BMJ Case Rep 2014;2014, http://dx.doi.org/10.1136/bcr-2014-011488 [pii: bcr2014011488]. [20] Toeg HD, Al-Atassi T, Kalidindi N, Iancu D, Zamani D, GiacR, cone et al. Endovascular treatment for cerebral septic stroke. J Stroke Cerebrovasc Dis 2014;23(5):e375–7, embolic http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2013.12.014. [21] Scharf EL, Chakraborty T, Rabinstein A, Miranpuri AS. Endovascular management of cerebral septic embolism: three recent cases and review of the literature. J Neurointerv Surg 2017;9(5):463–5, http://dx.doi.org/10.1136/neurintsurg-2016-012792. [22] Ambrosioni J, Urra X, Hernández-Meneses M, Almela M, Falces C, Tellez A, et al. Hospital clínic infective endocarditis study group. mechanical thrombectomy for acute ischemic stroke secondary to infective endocarditis. Clin Infect Dis 2018;66(8):1286–9, http://dx.doi.org/10.1093/cid/cix1000. [23] Bhaskar S, Cordato D, Cappelen-Smith C, Cheung A, Ledingham D, Celermajer D, Levi C. Clarion call for histopathological clot analysis in c¨ ryptogenic¨ischemic stroke: implications for diagnosis and treatment. Ann Clin Transl Neurol 2017;4(12):926–30, http://dx.doi.org/10.1002/acn3.500. [24] Hernández-Fernández F, Rojas-Bartolomé L, García-García J, Ayo-Martín Ó, Molina-Nuevo JD, Barbella-Aponte RA, et al. Histopathological and Bacteriological analysis of thrombus material extracted during mechanical thrombectomy in acute stroke patients. Cardiovasc Intervent Radiol 2017;40(12):1851–60, http://dx.doi.org/10.1007/s00270-017-1718-x. [25] Bolognese M, von Hessling A, Müller M. Successful thrombectomy in endocarditis-related stroke: case report and review of the literature. Interv Neuroradiol 2018, http://dx.doi.org/10.1177/1591019918774761 [1591019918774761]. [26] Hofmeister J, Kulcsar Z, Bernava G, Pellaton A, Yilmaz H, Erceg G, et al. The Catch Mini stent retriever for mechanical thrombectomy in distal intracranial occlusions. J Neuroradiol 2018;45(5):305–9, http://dx.doi.org/10.1016/j.neurad.2018.01.051. [27] Bourcier R, Abed D, Piotin M, Redjem H, Ferré JC, Eugène F, et al. Multicenter initial experience with the EmboTrap device in acute anterior ischemic stroke. J Neuroradiol 2018;45(4):230–5, http://dx.doi.org/10.1016/j.neurad.2018.01.052.
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Acute ischemic stroke treated with mechanical thrombectomy and fungal endocarditis: A case report and systematic review of the literature Alessandro Sgreccia a,∗ , Giuseppe Carità b , Oguzhan Coskun c , Federico Di Maria c , Hakim Benamer d , Marie Tisserand c , Anthony Scemama d , Georges Rodesch c , Bertrand Lapergue e , Arturo Consoli c a
Department of Radiology, Ospedali Riuniti, Ancona, Italy Department of Radiology, Azienda Ospedaliero Universitaria Ferrara, Ospedale Sant’ Anna Cona, Ferrara, Italy c Department of Diagnostic and Interventional Neuroradiology, Foch Hospital, Suresnes, France d Department of Cardiology, Foch Hospital, Suresnes, France e Division of Neurology, Stroke Center, Foch Hospital, University Versailles Saint-Quentin en Yvelines, Suresnes, France b
a r t i c l e Article history: Available online xxx Keywords: Stroke Candida Endocarditis Clot Histopathology Stent
i n f o
a b s t r a c t Fungal endocarditis is a rare clinical form of infective endocarditis. The main etiology of FE is Candida albicans but also Candida parapsilosis and the overall mortality is high. We report a case of an acute ischemic stroke treated by mechanical thrombectomy, with the histopathological analysis of the retrieved clot followed by the confirmation of fungal endocarditis. An extensive review of the literature has been proposed and three key points concerning the fungal endocarditis predisposing factors, the relation between thrombolysis and hemorrhagic risk and, finally, the importance of clot analysis have been discussed. © 2019 Elsevier Masson SAS. All rights reserved.
Introduction
Case report
The incidence of infectious endocarditis in stroke patients lies between 8% and 11% according to some studies analyzing the impact of transesophageal echocardiography (TEE) [1,2]. Fungal endocarditis (FE) is a rare clinical form of infective endocarditis accounting for 1.3% to 6% of cases [3,4]. Among this population, males seem to be more frequently affected, associated with a mean age of about 44–48 years [3,5]. The main etiology of FE, reported in the literature in different proportions, is Candida spp, detected in 53–67.8% of cases, and the most frequent pathogens are C. albicans (26–48%) and C. parapsilosis (19–33%) [3,4,5,6]. FE is associated with a high overall mortality (63.6%), with a rate of 54% and 79% related to the aortic andmitral valves, respectively. We report here a case of acute ischemic stroke treated by mechanical thrombectomy (MT) followed by histopathological analysis of the clot and a diagnosis of fungal endocarditis.
Admission and acute treatment
∗ Corresponding author at: Department of Radiology, Ospedali Riuniti, via Conca, 71, 60126 Torrette, Ancona AN, Italy. E-mail address: [email protected] (A. Sgreccia).
A 31-year-old male patient was referred to our institution one hour after the onset of a sudden left hemiplegia, homonymous lateral hemianopia, hemispacial neglect, dysarthria and hypoesthesia with an initial NIHSS of 18 (baseline mRS0). The patient suffered from hemorrhagic recto-colitis and was under treatment with azathioprine, 50 mg/day since 2015. A mild fever (37.5 ◦ C), treated by antibiotics 10 days before, was reported. An aortic murmur was detected without any sign of heart failure. White blood cell count was normal. Red blood cell count was 3.64 × 1012 /L (normal values: 4.60–6.20 × 1012 /L) and hemoglobin was 8.7 gr/dL. C-reactive protein level was 52.2 mg/L (normal values: < 3 mg/L). Magnetic resonance imaging (MRI) showed an acute right superficial temporo-fronto-insular ischemia (DWI-ASPECTS 5) without hyperintensity in the FLAIR sequence. MR-angiography showed a T-type occlusion of the right internal carotid bifurcation. Intravenous r-tPA was administered 96 minutes after the onset of symptoms and the patient was immediately transferred to the angio-suite for MT. Onset-to-groin puncture was 125 minutes. MT was performed by a 6 × 24 mm solitaire platinum stent-like
https://doi.org/10.1016/j.neurad.2019.03.003 0150-9861/© 2019 Elsevier Masson SAS. All rights reserved.
Please cite this article in press as: Sgreccia A, et al. Acute ischemic stroke treated with mechanical thrombectomy and fungal endocarditis: A case report and systematic review of the literature. J Neuroradiol (2019), https://doi.org/10.1016/j.neurad.2019.03.003
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Fig. 1. Baseline MRI at the admission. A. DWI sequence showing the ischemic lesion in the fronto-temporo-insular area, without FLAIR hyper-intensity (B); C. 3D-TOF sequence reconstruction showing the right ICA occlusion; Pre- (D) and Post-treatment (E) DSA, anteroposterior view: complete recanalization of the MCA occlusion after 1 maneuver of Mechanical Thrombectomy. F. Retrieved clot after washing out with saline, white-colored aspect.
retriever (Medtronic, Irvine, California) and a balloon guiding catheter (Cello 9F; Medtronic, Irvine, California). A complete recanalization (mTICI 3) was achieved after the first maneuver (time-to-reperfusion: 140 minutes) and the clot (Fig. 1) was sent for histopathological examination, according to our systeatic protocol.
Clinical evolution Two days after the procedure the patient completely recovered (NIHSS: 0). The MRI performed 24 hours after MT showed a regression of the insular superficial lesions (DWI-ASPECTS 8) and no hemorrhagic infarction. During the first hours of hospitalization in the stroke unit after the MT, fever (40.1 ◦ C) associated with hypotension and tachycardia was observed, requiring hydration and antibiotics. Anamnestic and clinical data gave rise to the suspicion of endocarditis and therefore TEE, blood cultures and microbiological analysis on the clot were performed. A type 0 bicuspid aortic valve with a 5 × 7 mm vegetation on both cusps was observed. Polymerase-chain-reaction (PCR) analysis performed on the clot revealed the presence of Candida parapsilosis, which was confirmed also by blood cultures. Furthermore, a thoraco-abdominal computed tomography (CT) scan showed a deep venous popliteal thrombosis associated with multiple renal and splenic ischemic lesions. The diagnosis was an ischemic stroke secondary to fungal endocarditis (FE) with systemic involvement. Anamnesis and lab tests excluded any immunodeficiency disorders or drug abuse. Medical therapy was set up with low molecular weight heparin (tinzaparin sodium 12 000 IU/day), i.v. cloxacillin 200 mg/kg/day, amoxicillin 200 mg/kg/day, gentamicin 3 mg/kg/day and i.v. amphotericin B 300 mg/day plus i.v. flucitosyn (Ancotil) 1800 mg every 6 hours.
Sub-acute management Eight days after the initial treatment, Candida persisted in blood cultures, a thickening of the vegetation was observed and a retinal embolus was detected. This suggested an indication for a biological aortic valve replacement. Sixteen days after the ischemic event the patient was still complaining of persistent headaches. MRI was performed and showed a small (1 cm) right temporo-occipital hematoma associated with some enhanced vascular structures within the hematoma. Digital subtraction angiography showed two small mycotic aneurysms (MAs) located at the level of two branches of the right posterior temporal artery, associated with local vasospasm. After multidisciplinary discussion, the indication for a super-selective embolization of the two MAs was advanced in order to prevent re-bleeding and to ensure a safe valve replacement. The embolization was performed by placing a microcatheter Magic 1.2F (Balt Extrusion, Montmorency, France) close to the origin of the two small branches and by injecting a mixture of 0.2 mL of glue (Glubran2, GEM, Viareggio, Italy) and lipiodol (Guerbet France, Villepinte) at a 50% dilution (Fig. 2). During the follow-up the patient experienced a progressive improvement of his clinical condition and a reduction in the vegetation thickness was observed. At this stage, after a multidisciplinary discussion we decided not to perform the valve replacement and to continue the follow-up. The patient was finally discharged in a good and stable clinical condition with continuation of the anti-fungal therapy.His mRS was 0 at three months. Materials and methods The collection of clinical data was approved by the institutional review board. An extensive review of the literature regarding MT performed in patients with FE was performed. We searched
Please cite this article in press as: Sgreccia A, et al. Acute ischemic stroke treated with mechanical thrombectomy and fungal endocarditis: A case report and systematic review of the literature. J Neuroradiol (2019), https://doi.org/10.1016/j.neurad.2019.03.003
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Fig. 2. MRI performed 16 h after the ischemic event. A. SWI sequence, axial plane, showing the right occipital hematoma; B. DSA, anteroposterior view showing the two mycotic aneurysms (black arrow) with an associated local vasospasm; C. MR-XperCT fusion confirming the anatomical correlation of the mycotic aneurysms in the context of the hematoma (white arrow); D. DSA, super-selective embolization of the two aneurysms by glue. E. Post-treatment angiogram.
in the PubMed database using keywords such as “infective endocarditis” AND “stroke” AND “thrombectomy” OR “fungal thrombus retrieval”. For the purpose of our review, we considered any case report or case series of FE and related ischemic stroke treated by thrombectomy with associated clot analysis. Sixteen articles matched our research filters. Three further papers were excluded because clot retrieval occurred in other organs (Fig. 3). Results Including our patient, 27 cases of MT of ischemic stroke related to infective endocarditis were found. Age and sex were not available for three patients; in the remaining 24 cases the mean age was 57 years (range 24–80 years) with a total of 12 male patients. The occlusion site was mainly MCA-M1: 14/27 cases (51.8%), with MCA-M2 in 6/27 cases (22.2%), ICA in 5 cases (18.5%) and basilar occlusion in 2 cases (7.5%). Except for 4 cases with missing data regarding the microorganism, all stroke cases were related to a bacterial pathogen that was identified through blood cultures and in 10 cases there was histological confirmation of the septic embolus. All patients underwent thrombectomy but 8/27 cases (29.6%) received i.v. thrombolysis and another 2 (7.4%) received combined i.a. thrombolysis. The recanalization rate was 79% (19/24 cases with TICI 2b-3 scores, including our patient). In three cases reported by Sveinsson et al. [7] it was not possible to extrapolate the exact grade of recanalization. Favorable clinical outcome was variably reported in 20 patients (74%) and 3 patients died (3/27, 11%) (Table 1). All patients received antibiotic or anti-fungal therapy. Discussion Predisposing factors In our review, the main predisposing factor was of cardiac valvular origin such as a prosthetic implant or other valvulopathies (15/27, 55.5%). One case reported intravenous drug abuse with immunodeficiency (1/27, 3.7%). Eleven patients had no apparent
predisposing factor for endocarditis (11/27, 40.8%). Although our patient had no history of immunodeficiency disorders or drug abuse, the bicuspid aortic valve and the immunosuppressive therapy with azathioprine for hemorrhagic rectocolitis were probably related to the FE. Intravenous Thrombolysis and Hemorrhagic risk The hemorrhagic risk in the infective endocarditis (bacterial and fungal) population lies between 3-7%, generally related to the hemorrhagic conversion of an ischemic stroke due to a septic embolus. Thus the conversion seems to be secondary to the development and subsequent rupture of a mycotic aneurysm or of a very fragile vessel caused by immune complex arteritis [7,9]. The mortality in this condition could reach rates close to 80% [9]. Intravenous thrombolysis is contraindicated by 2018 AHA Guidelines [10] in patients with symptoms consistent with infective endocarditis because of an expected increased risk of hemorrhagic transformation. However, the data supporting this recommendation (Grade III) are weak. In our review, i.v. thrombolysis was administered in 8 patients, while intra-parenchymal hemorrhage was reported only in our case 16 days after the initial event. A limited subarachnoid hemorrhage was described in another case [11] but no mycotic aneurysms were identified with MRI. Despite the small sample size, these observations could suggest that rapidly delivered MT [26,27], associated with i.v. thrombolysis when possible, might be safe and effective in cases of very acute infective endocarditis. Clot analysis Another issue that should be considered is the composition of the clot. In our review only 10 cases reported the results of clot analysis and examination of the type of clot. In 4 cases, standalone Gram staining was performed and was associated with blood cultures except for 1 case. Hematoxylin-eosin staining was performed in 3 cases and in two of these Gomori’s trichrome staining was also associated. Molecular biological examination of the clot was reported in 2/10 cases but no description of the technique used was provided.
Please cite this article in press as: Sgreccia A, et al. Acute ischemic stroke treated with mechanical thrombectomy and fungal endocarditis: A case report and systematic review of the literature. J Neuroradiol (2019), https://doi.org/10.1016/j.neurad.2019.03.003
Localization of occlusion
Pathogen
Type of analysis on the clot
Onset NIHSS Score
Thrombectomy
Recanalization Clinical Outcome
ICH
Mycotic AneurysmTreatment
Bain, et al. [12] 2011
24/F
ICA
Methicillinresistant Staphylococcus Epidermidis
No-Blood Cultures
18
yes + i.v. thrombolysis
TICI 2b
NIHSS 2 at 2 months
No
No
Dababneh, et al. [13] 2012
67/F
post-pregnancy non-ischemic dilated cardiomyopathyBacteremia Bovine prosthetic valve already implanted
MCA - M1
Gram negative Vancomycin resistant rods
No-Blood Cultures
NA
yes
TICI 2b
No
No
Liang, et al. [14] 2012
70/F
No
MCA - M2
No-Blood Cultures
24
yes
TICI 3
No
No
Sukumaran, et al. [15] 2012
33/M
Rheumatic Mitral Stenosis
MCA - M1
group B Streptococcus agalactiae Alpha Hemolytic Streptococci
14
yes
TICI 2b
No
No
Kan, et al. [16] 2012
78/F
(Mitral Valve Prolapse)
MCA - M2
Streptococci Viridans
16
yes
TICI 3
No
No
Kang, et al. [17] 2013
39/F
No
MCA - M1
Streptococcus Gordonii
Blood Cultures-Gram’s stain Blood CulturesCultures of the embolus No-Blood Cultures
NA poor outcome for causes not related to brain infarction Completely recovered to the baseline NIHSS 0 at 4 days
16
TICI 2b
No
No
Kim, et al. [18] 2014
40/F
No
MCA - M1
Streptococcus Mitis
15
yes + i.a. thrombolysis (urokinase + tirofiban) yes
No
No
Ladner, et al. [19] 2014 Toeg, et al. [20] 2014 Scharf, et al. [21] 2016
40/NA
i.v. opiate use
yes
TICI 3
No
No
No
20
No
No
Mitral Valve already implanted No Aortic Valve already implanted Prosthetic Mitral Valve already implanted Prosthetic Mitral Valve already implanted No
yes + i.v. thrombolysis yes
TICI 2b
NA
Enterococcus Faecalis Gram positive cocci dead gram coccal forms
3
73/M
Partial Occlusion M1 ICA
No
No
NA NA
Sveinsson, et al. [8] 2016
33/M
67/M
39/F
MCA - M1
Blood Cultures-Gram’s stain No-Blood Cultures No-Blood Cultures Gram’s stain
12
TICI 3
TICI 3
NIHSS 12 at 24 hrs poor outcome NIHSS 3 at 4 weeks of medical therapy NIHSS 3 at 3 days mRs 2 at 3 months NIHSS 0 and mRs 0 at 13 days NIHSS 0 at 8 months NIHSS 1
MCA - M2 MCA - M1
NA NA
NA NA
18 19
yes yes + i.v. thrombolysis
TICI 3 TICI 2a
NIHSS 5 NIHSS 17 poor outcome
No No
No No
MCA - M1
Serratia Marcescens
No-Blood Cultures
14
yes
NA
NIHSS 1 at discharge
No
No
MCA - M1
Enterococcus Faecalis
No-Blood Cultures
13
yes
NA
NIHSS 3 at discharge
No
No
MCA - M2
Staphylococcal sepsis
No-Blood Cultures
15
yes
NA
NIHSS 4 at discharge
No
No
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Please cite this article in press as: Sgreccia A, et al. Acute ischemic stroke treated with mechanical thrombectomy and fungal endocarditis: A case report and systematic review of the literature. J Neuroradiol (2019), https://doi.org/10.1016/j.neurad.2019.03.003
Table 1 Review of mechanical thrombectomy cases related to infective endocarditis.
Predisposing factors
Localization of occlusion
Pathogen
Type of analysis on the clot
Onset NIHSS Score
Thrombectomy
Recanalization Clinical Outcome
ICH
Mycotic AneurysmTreatment
Ambrosioni, et al. [22] 2017
79/M
Prosthetic Valve already implanted Prosthetic Mitral Valve already implanted
Tandem (Carotid - M1)
Staphylococcus Aureus
No-Blood Cultures
9
yes
TICI 0
mRs 6
No
No
Basilar
Staphylococcus Oralis
10
yes
TICI 3
NIHSS 2 at 24 hrs
No
No
56/F 72/M
No No
MCA - M1 Basilar
NA Streptococcus Dysgalactiae
19 35
yes yes
TICI 3 TICI 3
NIHSS 2 at 24 hrs mRs 6
No No
No No
79/F
Prosthetic Valve already implanted Prosthetic Valve already implanted Prosthetic Valve already implanted
MCA - M1
NA
Blood CulturesMolecular Biology of the thrombus NA Blood CulturesMolecular Biology of the thrombus NA
5
yes
TICI 2b
NIHSS 2 at 24 hrs
No
No
MCA - M1
Staphylococcus Epidermidis
No-Blood Cultures
8
yes
TICI 3
mRs 6
No
No
MCA - M1
Staphylococcus Epidermidis
Gram’s stain Hematoxylin and Eosin stain -Blood Cultures Hematoxylin & Eosin stain Gram and Gomori trichrome - Blood Culture Hematoxylin and Eosin stain Gram and Gomori trichrome - Blood Culture Gram’s stain
16
yes + i.v. thrombolysis
TICI 3
NIHSS 2 at 24 hrs, mRs 1 at 5 days after procedure
No
No
13
yes + i.v. thrombolysis
TICI 2b
mRs1 at 3 months
No
No
15
yes + i.v. thrombolysis
TICI 2b
mRs 2 at 3 months
No
No
18
yes + i.v. thrombolysis
TICI 0
NIHSS 12 at 18 months, poor outcome
micro-sub aracnoid Hemorrhage
yes + i.a. thrombolysis (rt-PA 5 mg) yes + i.v. thrombolysis
TICI 2b
NIHSS 0 at 4 weeks
No
TICI 3
NIHSS 0 at 2 days
yes
Suspect but no evidence at MRA No endovascular treatment No – Cerebral Abscesses in MCA Territory yes – glue embolization
69/F
85/M
Bhaskar, et al. [23] 2017
36/M
HernandezFernandez, et al. [24] 2017
57/M
Prosthetic Valve already implanted
ICA
S.Sanguinis
66/M
No
ICA
S.Bovis
Nakanishi, et al. [11] 2017
80/F
No
MCA - M2
Gram positive cocci
Bolognese, et al. [25] 2018
42/M
No
MCA - M2
Streptococcus Viridans
Blood Cultures
3
Sgreccia, et al. 2018
31/M
Medical therapy with AZT for hemorrhagic rectocolitis Bicuspid Aortic Valve
ICA
Candida Parapsilosis
Blood CulturesMolecular Biology of the thrombus
18
i.v: intravenous; i.a.: intra-arterial; AZT: azathioprine; hrs: hours.
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Table 1 (Continued)
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Fig. 3. Prisma flow-diagram.
In one case the clot specifically underwent microbiological cultures. In our case a PCR was performed, which revealed the presence of a consistent amount of Candida parapsilosis DNA via the amplification of the ITS-1 (internal transcribed spacer) gene inside the clot (threshold cycle: 12). The major causative pathogens reported in the review are Streptococcus spp. in 9/26 cases, 6 Staphylococcus spp. in 6 cases, Enterococcus faecalis in 2 cases and Serratia marcescens in 1 case. The other results were not pathogen-specific and authors reported only “Cocci Gram positive” or “negative” [11,13,20,21]. Our report is, to our knowledge, the only one reporting the presence of Candida parapsilosis inside the clot and associated with FE.
Conclusion Systematic microbiological analysis of the removed clot should be considered in patients with acute ischemic stroke caused by infective endocarditis.
Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Disclosure of interest The authors declare that they have no competing interest.
Acknowledgments We thank Mary Osborne-Pellegrin for help in editing the final draft of the manuscript.
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Please cite this article in press as: Sgreccia A, et al. Acute ischemic stroke treated with mechanical thrombectomy and fungal endocarditis: A case report and systematic review of the literature. J Neuroradiol (2019), https://doi.org/10.1016/j.neurad.2019.03.003