Left Atrial Mural Thrombosis and Hemopericardium in a Dog with Myxomatous Mitral Valve Disease

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Case Report Left Atrial Mural Thrombosis and Hemopericardium in a Dog with Myxomatous Mitral Valve Disease

Domenico Caivano * , Maria Chiara Marchesi, Francesco Birettoni * , Elvio Lepri † and Francesco Porciello †

Department of Veterinary Medicine, University of Perugia, Via San Costanzo 4, 06126 Perugia, Italy; [email protected] (M.C.M.); [email protected] (E.L.); [email protected] (F.P.) * Correspondence: [email protected] (D.C.); [email protected] (F.B.); Tel.: +39-075-5857613 (D.C.); +39-075-5857608 (F.B.) † These authors contributed equally to this work.

Abstract: A 14-year-old mixed-breed dog with a 2-year history of myxomatous mitral valve disease was examined for collapse and lethargy. At the presentation, pale oral mucous membranes, rapid and weak femoral pulses, and mufﬂed heart sounds with a moderate left apical systolic murmur were revealed. Echocardiographic examination showed pericardial effusion with organized echogenic material originating from the left atrial wall. Tamponade of the right atrium and severe left atrial enlargement were also observed. Multiple views of the left atrium and left auricle allowed to visualize a hyperechoic mass adherent to the endocardium of the left atrial wall. Contrast-enhanced ultrasonography study allowed to rule out active intrapericardial hemorrhages, and echo-guided pericardiocentesis was performed. No recurrence of pericardial effusion was observed, but the dog suddenly died after 10 days. The postmortem examination conﬁrmed multifocal left atrial thrombosis attached to the endomyocardial tears.

Citation: Caivano, D.; Marchesi, Keywords: echocardiography; left atrial rupture; mitral valve disease; mural thrombosis; pericar- M.C.; Birettoni, F.; Lepri, E.; Porciello, dial effusion F. Left Atrial Mural Thrombosis and Hemopericardium in a Dog with Myxomatous Mitral Valve Disease. Vet. Sci. 2021, 8, 112. https:// 1. Introduction doi.org/10.3390/vetsci8060112 Left atrial rupture has been previously reported as an uncommon complication of severe myxomatous mitral valve disease (MMVD) in dogs [1–7]. The etiology of left atrial Academic Editor: Bartosz Kempisty rupture in dogs affected by MMVD can be multifactorial, however, endocardial splitting represents a predisposing factor in the development of this clinical condition [1,5–7]. Received: 30 April 2021 Endocardial splitting can variably extend in depth into the myocardium with spontaneous Accepted: 15 June 2021 tear of the endomyocardium [1,5–7]. Therefore, dogs with endocardial splitting can develop Published: 17 June 2021 complete endomyocardial rupture with hemopericardium [1–7]. Conversely, an incomplete endocardial tear can result in intracardiac bleeding and thrombus formation, as previously Publisher’s Note: MDPI stays neutral reported in a dog [8]. with regard to jurisdictional claims in Rupture of the left atrial wall results in a rapid accumulation of blood within the published maps and institutional afﬁl- iations. pericardium with clinical signs of cardiac tamponade and cardiogenic shock [1]. Pericar- diocentesis may be performed to resolve cardiac tamponade, but in the case of ongoing hemorrhage, this can worsen the bleeding as a consequence of relieving the pericardial pressure during the ﬂuid removal. Contrast-enhanced ultrasonography (CEUS) has been used for improving the detection of active pericardial hemorrhages during cardiac rupture Copyright: © 2021 by the authors. in humans [9,10]. Licensee MDPI, Basel, Switzerland. The present report describes a rare case of atrial mural thrombosis and hemoperi- This article is an open access article cardium in a dog affected by MMVD. Additionally, we describe the use of CEUS to rule distributed under the terms and conditions of the Creative Commons out active intrapericardial hemorrhages from left atrial tears. Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

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2. Case Presentation 2. Case Presentation A 14-year-old, 5.5 kg, mixed-breed dog with a 2-year history of MMVD was pre- A 14-year-old, 5.5 kg, mixed-breed dog with a 2-year history of MMVD was presented sented to our hospital for collapse and lethargy. Conventional heart failure therapy (furo- to our hospital for collapse and lethargy. Conventional heart failure therapy (furosemide semide 2 mg/kg twice a day, orally; benazepril 0.5 mg/kg once a day, orally; pimobendan 2 mg/kg twice a day, orally; benazepril 0.5 mg/kg once a day, orally; pimobendan 0.25 mg/kg twice a day orally) had been initiated 10 months prior. Physical examination 0.25 mg/kg twice a day orally) had been initiated 10 months prior. Physical examina- revealedtion revealed pale oral pale mucous oral mucous membranes, membranes, rapid rapid and weak and weakfemoral femoral pulses, pulses, and muffled and muffled heart soundsheart sounds with a with moderate a moderate left apical left apical systolic systolic murmur. murmur. Mild regenerative Mild regenerative anemia anemia (Hct 35%, (Hct 3 reference35%, reference limits limits 37–55%) 37–55%) with withthrombocytopenia thrombocytopenia (PLT (PLT 180 180× 10×/µL,103/ referenceµL, reference intervals inter- 3 200–500vals 200–500 × 10 ×/µL)10 3were/µL) detected were detected on CBC. on Serum CBC. Serum biochemical biochemical analysis analysis revealed revealed high BUN high (90BUN mg/dL, (90 mg/dL, reference reference limits limits 20–40 20–40 mg/dL) mg/dL) and creatinine and creatinine (2.2 mg/dL, (2.2 mg/dL, reference reference limits limits 1–2 mg/dL)1–2 mg/dL) concentrations. concentrations. Electrocardiographic Electrocardiographic examination examination showed showed sinus sinus tachycardia tachycardia (170 bpm)(170 bpm) with withsporadic sporadic atrial atrial premature premature beats. beats. Two-dimensional Two-dimensional echocardiography echocardiography identi- iden- fiedtified severe severe left left atrial atrial enlargement enlargement (left-atrial-to-aortic (left-atrial-to-aortic ratios ratios = = 3), 3), left left ventricular ventricular dilation (diastolic and systolic left left ventricular ventricular internal internal diameter diameter were were 3.82 3.82 cm cm and and 1.61 1.61 cm, cm, respec- respec- tively),tively), marked marked thickening, thickening, and and prolapse prolapse of of the the leaflets leaflets of of both atrioventricular valves. valves. Moderate pericardial effusion with right atrium collapse was also observed. An organized echogenic material originating from from the wall of the left atrium was evident within the pericardial space (Figure 11).). MultipleMultiple viewsviews ofof thethe leftleft atriumatrium andand leftleft auricleauricle revealedrevealed aa hyperechoic mass adherent to the atrial wall (Figure1 1).). SevereSevere mitralmitral andand mildmild tricuspidtricuspid valve regurgitation was demonstrated by color Doppler echocardiography. Velocity of tricuspidtricuspid valve valve regurgitation regurgitation was was 2.76 2.76 m/sec m/sec (pressure (pressure gradient gradient = 30.5 = 30.5 mmHg). mmHg). Mild Mild ab- dominalabdominal effusion effusion with with caudal caudal vena vena cava cava dist distentionention and and hepatic hepatic venous venous congestion congestion were also identified identified on ultrasonography.

(a) (b)

Figure 1. Conventional echocardiography at the presentation: ( a) Right parasternalparasternal long-axis view showingshowing pericardialpericardial effusion (PE)(PE) withwith hyperechoic hyperechoic density density suggestive suggestive of of a thrombus a thrombus (Th). (Th). (b) ( Modiﬁedb) Modified left parasternalleft parasternal long-axis long-axis view view optimized opti- tomized visualize to visualize the left the atrium left atri (LA)um and (LA) auricle and auricle (LAu). (LAu). A hyperechoic A hyperechoic structure struct (arrow),ure (arrow), adherent adherent to the to left the atrial left atrial wall wall and consistentand consistent with with a thrombus, a thrombus, is evident. is evident. LV, left LV, ventricle; left ventricle; PV, pulmonary PV, pulmonary vein. vein.

A diagnosis of severe MMVD, hemoperica hemopericardiumrdium with cardiac tamponade secondary toto left atrial rupture, and left atrial thrombusthrombus was made. To enhance the visualization of active intrapericardialintrapericardial bleeding,bleeding, CEUS CEUS was wa performeds performed using using an ultrasoundan ultrasound machine machine (My- (MyLabLab Class Class C, Esaote, C, Esaote, Florence, Florence, Italy) Italy) equipped equipped with with a contrast-tuned a contrast-tuned imaging imaging technology technol- ogymodule module (CnTI (CnTITM,TM Esaote,, Esaote, Florence, Florence, Italy). Italy). A A bolus bolus (0.05 (0.05 mL/kg) mL/kg) ofof sulfursulfur hexafluoridehexafluoride microbubbles stabilized by a phospholipid shell (SonoVue ®,, Bracco, Milano, Italy) waswas intravenouslyintravenously infusedinfused by by hand hand as as previously previous describedly described [11]. [11]. The CEUSThe CEUS study study demonstrated demon- stratedno evidence no evidence of microbubbles of microbubbles in the pericardialin the pericardial space afterspace the after complete the complete opacification opacifica- of tionthe left of the atrium left (Figureatrium 2(Figure). This finding2). This wasfindi suggestiveng was suggestive of the absence of the of absence active intrapericar-of active in- trapericardialdial hemorrhages, hemorrhages, thus echo-guided thus echo-guided pericardiocentesis pericardiocentesis was performed, was performed, yielding 35yielding mL of

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35 mL of hemorrhagic fluid. No recurrence of hemopericardium was noted over the hos- hemorrhagicpitalization ﬂuid. period No recurrence(3 days) ofand hemopericardium the dog was discharged was noted over with the hospitalizationfurosemide (2 mg/kg twice perioda day, (3 orally), days) and benazepril the dog was (0.5 discharged mg/kg with once furosemide a day, orally), (2 mg/kg pimobendan twice a day, orally), (0.25 mg/kg twice a benazeprilday, orally), (0.5 mg/kgand clavulanate-amoxycillin once a day, orally), pimobendan (12.5 (0.25 mg/kg mg/kg twice twice a a day, orally), orally). In addition, and clavulanate-amoxycillin (12.5 mg/kg twice a day, orally). In addition, clopidogrel (2clopidogrel mg/kg once (2 a day,mg/kg orally) once was a prescribedday, orally) to further was prescribed inhibit the enhancement to further inhibit of the left the enhancement atrialof the thrombus. left atrial thrombus.

FigureFigure 2. 2.Contrast-enhanced Contrast-enhanced echocardiographic echocardiographic image (left image apical (left 4-chamber apical 4-chamber view) showing view) no showing no evidenceevidence of of microbubbles microbubbles in the in pericardial the pericardial space after spac thee after complete the opacificationcomplete opacification of the cardiac of the cardiac chambers.chambers. PE, PE, pericardial pericardial effusion; effusion; LV, left ventricle;LV, left ventricle; LA, left atrium. LA, left atrium. Seven days after the discharge, the dog suddenly died, and a complete necroscopy was performed.Seven days At theafter opening the discharge, of the thoracic the cavity, dog suddenly the pericardial died, sac and was thickeneda complete necroscopy andwas edematous; performed. the pericardialAt the opening cavity contained of the thoracic only a small cavity, amount the of pericardial serosanguineous sac was thickened fluid;and edematous; in the left atrial the lumen,pericardial multiple cavity pedunculated contained 1–2 only cm, a red-pink, small amount smooth, of soft serosanguineous massesfluid; in were the present,left atrial adherent lumen, to multiple interatrial pedunculated septum, atrial, and1–2 auricularcm, red-pink, wall; atsmooth, the soft masses base of some masses a red discoloration was present (Figure3). In the myocardium, multifocalwere present, poorly adherent defined whitish to interatrial areas were septum, present. atrial, Mitral and and, auricular to a lesser wall; extent, at the base of some tricuspidalmasses a red leaflets discoloration were thickened was and present distorted. (Figure All the 3). other In the examined myocardium, tissues had multifocal poorly nodefined gross lesions, whitish including areas were brain. present. Histologically Mitral the and, main to findings a lesser were extent, hepatic tricuspidal diffuse leaflets were centrolobularthickened and hemorrhagic distorted. necrosis, All the multifocal other examin tubular renaled tissues necrosis. had In the no heart, gross apart lesions, including from severe myxoid degeneration of atrioventricular valves, multifocal to coalescing severe acutebrain. myocardial Histologically necrosis the with main calcifications findings was were present, hepatic involving diffuse about centrolobular 30–40% of hemorrhagic myocardium,necrosis, multifocal both in the tubular left and rightrenal ventricular necrosis. free In the wall heart, and interventricular apart from severe septum; myxoid degen- theeration left atrium of atrioventricular contained multifocal valves, mural multifocal thrombosis to (Figure coalescing3). severe acute myocardial necrosis with calcifications was present, involving about 30–40% of myocardium, both in the left and right ventricular free wall and interventricular septum; the left atrium contained multifocal mural thrombosis (Figure 3).

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FigureFigure 3. 3.Necroscopy Necroscopy imaging. imaging. Several, Several, up to 1 cm, up pink, to 1 pedunculated cm, pink, pedunculated masses (thrombi) masses adherent (thrombi) to adherent theto the mural mural endocardium endocardium of the interatrial of the interatrial septum and septum left auricle. and Note left the auricle. hemorrhages Note aroundthe hemorrhages the around basethe base in the in upper the thrombusupper thrombus (white arrow). (white Mitral arrow). septal (anterior)Mitral septal leaflet is(anterior) thickened leaflet and distorted, is thickened and dis- andtorted, in the and myocardium in the myocardium multifocal to coalescingmultifocal whitish to coalescing areas (necrosis whitish with areas calcifications). (necrosis Insert: with calcifications). pedunculatedInsert: pedunculated thrombus (dashedthrombus arrow) (dashed attached arrow) to the atta endocardialched to surface the endocardial of the auricle surface (black of the auricle arrow);(black Hematoxylinarrow); Hematoxylin and eosin, low and magnification. eosin, lowTh, magnification. thrombus. Th, thrombus. 3. Discussion 3. DiscussionThe case described in this report represents the first description of antemortem diagnosis ofThe atrial case mural described thrombosis in this associated report with represents hemopericardium the first description in a dog affected of antemortem by diag- MMVD. Mural thrombosis and hemopericardium due to left atrial rupture can occur in dogsnosis with of atrial severe mural MMVD, thrombosis but these have associated not been previously with hemopericardium reported as concomitant in a dog affected by complications.MMVD. Mural Thrombus thrombosis formation and is anhemopericardium uncommon complication due to of cardiacleft atrial diseases rupture in can occur in dogs.dogs Intracardiacwith severe thrombus MMVD, in the but left these atrium have has been not reported been inpreviously dogs with atrialreported fibrilla- as concomitant tioncomplications. [12], secondary Thrombus to blunt cardiac formation injury [is13 ],an or un ascommon a consequence complication of myocarditis of cardiac [14]. diseases in Recently, thrombi attached to partial left atrial endocardial tears have been described in adogs. dog with Intracardiac MMVD and thrombus myocardial in infarct the left [8]. atrium Pericardial has effusion been reported is usually in associated dogs with atrial fibril- withlation tumors [12], orsecondary idiopathic pericardialto blunt cardiac effusion injury in dogs; [13], less or commonly, as a consequence it is secondary of tomyocarditis [14]. coagulopathy,Recently, thrombi local infections, attached congestive to partial heart left failure,atrial endocardial or left atrial rupture tears [have1–7,15 been–20]. described in a Leftdog atrial with tears MMVD can occur and in myocardial the lateral wall infarct of the left[8]. atrium Pericardial secondary effusion to MMVD is andusually associated causewith pericardialtumors or effusion, idiopathic cardiac pericardial tamponade, andeffusion sudden in death dogs; in dogs less [1commonly,–3,5]. Buchanan it is secondary to and Kelly described left atrial tears in a first report of 22 dogs and 7 of these showed peri- cardialcoagulopathy, effusion [1 ].local Rarely, infections, acquired atrial congestive septal defects heart secondary failure, toor MMVDleft atrial have rupture been [1–7,15–20]. reportedLeft atrial in dogs: tears fossa can ovalis occur can in be the a site lateral of tear wall as a consequenceof the left atrium of mechanical secondary trauma to MMVD and orcause increased pericardial atrial pressure effusion, [21,22 ].cardiac The etiology tamponad of the lefte, atrialand tearssudden in dogs death affected in dogs by [1–3,5]. Bu- MMVDchanan is and unclear: Kelly Increased described left atrial left volume/pressure atrial tears in and a mechanicalfirst report trauma of 22 from dogs high and 7 of these velocity mitral regurgitation jet represent predisposing factors for spontaneous tears [1,5–7]. Theshowed dog described pericardial in this effusion report presented [1]. Rarely, atrial acquir thrombosised atrial and septal hemopericardium defects secondary sec- to MMVD ondaryhave been to left reported atrial rupture: in dogs: Multiple fossa left ovalis atrial tearscan be with a site variable of tear depths as a were consequence able to of mechan- causeical trauma both intracardiac or increased and intrapericardial atrial pressure hemorrhages. [21,22]. The No etiology acquired atrialof the defect left wasatrial tears in dogs visualizedaffected inby the MMVD interatrial is septumunclear: on echocardiographyIncreased left andatrial necroscopy. volume/pressure In the present and mechanical trauma from high velocity mitral regurgitation jet represent predisposing factors for spontaneous tears [1,5–7]. The dog described in this report presented atrial thrombosis and hemopericardium secondary to left atrial rupture: Multiple left atrial tears with variable depths were able to cause both intracardiac and intrapericardial hemorrhages. No acquired atrial defect was visualized in the interatrial septum on echocardiography and necroscopy. In the present case, the death of the dog was attributed to severe myocardial necrosis, inducing severe hypotension and tissue hypoxia that led to centrilobular hepatic necrosis and renal tubular necrosis, both presumed to be hypoxic. Causes of severe myo-

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case, the death of the dog was attributed to severe myocardial necrosis, inducing severe hypotension and tissue hypoxia that led to centrilobular hepatic necrosis and renal tubular necrosis, both presumed to be hypoxic. Causes of severe myocardial necrosis in dogs include thromboembolic events, which is unlikely to cause extensive multifocal necrosis, as well as toxic or nutritional. None of these causes were identified in this case, and the exact cause of myocardial necrosis remains unexplained. Transthoracic echocardiography is a noninvasive, reliable, and fast-imaging technique that can be useful for diagnosis of pericardial diseases, cardiac masses, myocardial and valvular diseases. In our report, transthoracic echocardiography allowed to demonstrate pericardial effusion and cardiac tamponade secondary to left atrial rupture. Moreover, echocardiographic images of the pericardial effusion were characterized by an organized echogenic material, originating from the wall of the left atrium, suggestive of a thrombus. This echocardiographic feature associated to left ventricular and atrial enlargement, and mitral valve thickening and regurgitation, have been reported as specific echocardiographic criteria for antemortem diagnosis of left atrial rupture secondary to MMVD [4,5,7]. In the dog of this report, transthoracic echocardiography also allowed to visualize a hyperechoic mass adherent to the left atrial wall. Differential diagnosis of the left atrial masses included neoplasia and thrombus. Cardiac tumors are extremely rare (0.19%) in dogs, and sporadically, tumors involve the left-sided heart chambers [23]. Based on the echocardiographic appearance of the intracardiac mass in the reported dog, a presumptive diagnosis of left atrial thrombus was made. Postmortem examination confirmed multifocal left atrial thrombosis attached to the endomyocardial tears. Our findings are similar to the previous case report of Sleeper et al. [8]. Indeed, these authors reported an antemortem diagnosis of myocardial infarct presumed secondary to left atrial thrombi, which were confirmed with necropsy [8]. Diagnosis of presumptive left atrial thrombosis was made on the ultrasonographic appearance and anatomic position of the intracardiac masses [8]. Moreover, these masses appeared to adhere to the LA wall on echocardiography [8], as observed on echocardiography and necroscopy in our dog. Left atrial rupture can lead to cardiovascular instability involving pericardial effusion, cardiac tamponade, reduced preload, and low cardiac output. If cardiac tamponade and clinical signs of hemodynamic compromise are present, the drainage of the effusion from the pericardial space is necessary, but pericardial effusion can recur because of relieving the pericardial pressure during the fluid removal. In humans, CEUS have been used for improving the detection of active intrapericardial hemorrhages due to cardiac rupture [9,10]. Evidence of microbubbles in the pericardial space was considered suggestive of a myocardium tear in patients with pericardial effusion [9,10]. Contrast-enhanced ultrasonography is an imaging modality that improves the diagnostic accuracy of conventional ultrasonography by increasing the intensity of blood-pool echo signals in vessels and heart through intravenous injection of stabilized gas-filled microbubbles as a contrast agent [11,24]. In our case, CEUS study demonstrated no evidence of microbubbles in the pericardial space after the complete opacification of the left atrium. This feature was suggestive of no active intrapericardial hemorrhages and pericardiocentesis was performed without recurrence of hemopericardium. However, CEUS can be useful for improving the detection of active intrapericardial hemorrhages, but cannot exclude a recurrence of hemopericardium because of relieving the pericardial pressure during the fluid removal. Further studies are needed to discern the value of the CEUS in dogs with left atrial rupture. Additionally, the use of CEUS could open up new perspectives for assessing other cardiac diseases characterized by bleeding (e.g., tumors or pericarditis), using this advanced ultrasonographic technique. A recent consensus statement regarding rational use of antithrombotic drugs in dogs and cats recommended the administration of anticoagulants in venous thrombosis and antiplatelet drugs in arterial thrombosis, although no recommendation for using these drugs in combination was stated because of low clinical evidence [25]. A previous study reported no anticoagulant treatment in dogs with left atrial rupture secondary to MMVD because no Vet. Sci. 2021, 8, 112 6 of 7

clinical suspicion of thromboembolic disease could be advanced in these dogs [7]. In the dog described in this report, left atrial thrombosis was suspected and an antiplatelet drug (clopidogrel) was used to limit further enhancement of the left atrial thrombus. Although no recurrence of hemopericardium was observed in our dog, antiplatelet therapy could increase the bleeding risk in dogs with left atrial rupture. Therefore, clinicians should carefully consider the use of antithrombotic drugs in dogs with left atrial rupture and thrombosis, assessing the risk of bleeding and possible recurrences of the hemopericardium.

4. Conclusions Left atrial tears can occur in dogs with severe MMVD, and clinical presentation can be characterized by hemopericardium, intracardiac thrombosis, or both, as described in the present case report. Moreover, CEUS could be a useful diagnostic tool in dogs with left atrial rupture to rule out active intrapericardial hemorrhages.

Author Contributions: Investigation, D.C., M.C.M. and E.L.; Project supervision, F.B. and F.P.; Writing—original draft, D.C., M.C.M. and E.L.; Writing—review & editing, D.C., M.C.M., F.B., E.L. and F.P. All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Institutional Review Board Statement: Ethical review and approval were waived for this study because, being a case report derived from clinical practice, all medical procedures and post-mortem examination were performed after obtaining written consent from the owner. Informed Consent Statement: Informed consent was obtained from the owner of the dog involved in the study. Conﬂicts of Interest: The authors declare no conﬂict of interest.

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