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Case Reporteve_140 64..68 Idiopathic aseptic pericardial effusion with in a horse F. Malalana*, D. Bardell and S. McKane The Philip Leverhulme Equine Hospital, University of Liverpool, Leahurst, Neston, UK.

Keywords: horse; effusive; ; ; ultrasound

Summary Case details

This report describes the successful treatment of pericardial A 10-year-old Hanoverian gelding was admitted for effusion and cardiac tamponade in a 10-year-old investigation of anorexia and lethargy of 72 h duration. Hanoverian gelding. Pericarditis and pericardial effusion Initial clinical examination revealed a marked are uncommon conditions in horses. Although many with a heart rate of 88 beats/min, muffled potential causes for the effusion have been described most , marked bilateral jugular distension and cases are classified as idiopathic. The most valuable obvious pectoral oedema. Mucous membranes were pink diagnostic procedure for the detection of pericardial and moist and capillary refill time <2 s. Rectal temperature effusion is echocardiography. and was 36.9°C. drainage of the fluid were carried out in this case. At one Haematology revealed leucocytosis (WBC 19.8 ¥ 109/l, year follow-up there were no clinical signs of recurrence reference range [rr] 5–12 ¥ 109/l) with neutrophilia (16.8 ¥ and the horse has returned to his previous level of athletic 109/l, rr 2.5–8.4 ¥ 109/l). performance. Routine serum biochemical examination revealed a mild azotaemia (urea 12 mmol/l, rr 5–9 mmol/l; creatinine 203 mmol/l, rr 53–194 mmol/l). Fibrinogen concentration Introduction was markedly raised (7 g/l, rr 1.5–3.3 g/l). Cardiac troponin was also elevated (0.77 ng/ml, rr 0.05–0.2 ng/ml), Pericarditis and pericardial effusion are reported to be indicating myocardial damage. uncommon in the horse (Freestone et al. 1987; Worth and A base-apex electrocardiogram was performed. Reef 1998). Consistent physical findings in cases of Electric alternans, characterised by an alternate reduction pericardial effusion include tachycardia, pectoral in the amplitude of the QRS complexes, was identified oedema, jugular distension and diminution of audible (Fig 1), but no were detected. heart sounds and/or presence of pericardial friction rubs Cardiac ultrasound (Vivid 7, 3 MHz phased array (Freestone et al. 1987; Worth and Reef 1998; Jesty and Reef probe)1 examination revealed a dorsally displaced heart, 2006). surrounded by a large amount of anechoic pericardial Potential causes of pericardial effusion include fluid. There was no suggestion of fibrin deposits within the immune-mediated processes, bacterial infection, viral parietal pericardial surface. Right atrial and right infection, trauma and neoplasia. However, in most horses, ventricular collapse were also detected (Fig 2). Thoracic the cause of the effusion is not determined (Freestone ultrasonographic examination showed a moderate et al. 1987; Robinson et al. 1992; Worth and Reef 1998). amount of pleural effusion and there was also evidence Aggressive early treatment is essential and should of ascites present on abdominal ultrasound. Cytological include pericardial drainage (Freestone et al. 1987; Vörös examination of pleural fluid collected from both et al. 1991; Robinson et al. 1992; Worth and Reef 1998; Jesty hemithoraxes revealed nonseptic effusion (WBC 2.4 ¥ 109/l, and Reef 2006). and total protein 20 g/l). This report describes the successful treatment of a Following surgical preparation and infiltration of the skin 10-year-old Hanoverian gelding diagnosed with idiopathic and underlying muscle with local anaesthetic, aseptic pericardial effusion and cardiac tamponade. pericardiocentesis was performed. A 24 gauge chest drain catheter was introduced into the pericardial space via *Corresponding author email: [email protected] the left fifth intercostal space, approximately mid-way

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Fig 1: Base-apex electrocardiogram taken at 25 mm/s and 1 mV/mm showing the presence of electric alternans and reduced QRS amplitude.

Ef

Fig 3: Serosanguineous fluid being drained from the pericardial RV sac. RA Ef LV

LA

RV

RA Fig 2: Long axis 4 chamber view of the heart from the right side. LV Note the dorsally displaced heart within the fluid filled pericardial sac, with partial right ventricular collapse. RV: right ventricle; LV: left ventricle; RA: right atrium; LA: left atrium; Ef: effusion. PS LA between the lateral thoracic vein and a line parallel to the ground drawn from the point of the shoulder. Thirteen litres of serosanguineous fluid were drained from the pericardial space (Fig 3). Simultaneously, continuous electrocardiographic and right-sided ultrasonographic valuation of the heart were performed. A catheter placed in the left transverse facial artery allowed continuous Fig 4: Long axis 4 chamber view of the heart from the right side monitoring of arterial . No arrhythmias were following drainage. A small amount of fluid is still visible in the detected and there was progressive disappearance of the pericardial space. RV: right ventricle; LV: left ventricle; RA: right electric alternans during the procedure. The heart rate atrium; LA: left atrium; PS: pericardial space. reduced from 88 to 68 beats/min, and mean arterial blood pressure from 135 to 115 mmHg. The jugular venous murmur audible on the left side. Doppler distension progressively resolved during the procedure. showed regurgitation through the mitral, tricuspid and aortic Once the cardiac tamponade was no longer present and valves. Systemic therapy with a combination of procaine no more fluid could be obtained (Fig 4), 1 litre of saline penicillin (12 mg/kg bwt i.m. q. 12 h) and cefquinome (1 mg/ (0.9% NaCl) containing 1.35 g of cefquinome kg bwt i.v. q. 12 h) was initiated. (Cephaguard)2 was instilled and left in situ for 30 min A sample of the was submitted for before it was drained. analysis. It contained many red blood cells (3.9 ¥ 1012/l). Following drainage of the pericardial sac, a pericardial Among the red blood cells there were scattered small friction rub became apparent on . A grade 4/6 lymphocytes and monocytes. Occasional reactive holosystolic could also be heard from both sides mesothelial cells were also present. No neoplastic cells or of the chest. In addition there was a grade 4/6 diastolic infectious agents were identified and bacterial culture of

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the fluid was negative. The total protein content of the fluid peripheral venous engorgement, excessive jugular , was 40 g/l. These findings were consistent with a nonseptic ventral oedema, ascites and pleural effusion and modified transudate. hepatomegaly) and/or left sided output failure (weakness, Over the next few days the gelding became brighter lethargy, collapse, oliguria and cardiogenic ) and the heart rate reduced gradually to 36 beats/min by develop (Freestone et al. 1987; Worth and Reef 1998; Jesty Day 6. The intensity of the heart murmurs and the and Reef 2006). The clinical signs of pericardial effusion also decreased until they could not with tamponade depend on the volume and rate of be heard 4 days after drainage of the pericardic space. development of the effusion, the compliance of the Repeat echocardiograms confirmed that the effusion had and, in some cases, the aetiology of the not reformed. Five days after pericardiocentesis minor effusion. The horse in the present report presented with mitral, tricuspid and aortic regurgitation were still evident signs of right heart tamponade, and although cardiac on Doppler ultrasound. filling would have been impaired by the increased The horse remained stable and was subsequently pericardial pressure, compensatory mechanisms to discharged on Day 7 on a course of oral enrofloxacin maintain cardiac output, such as an increase in heart rate, (Baytril, 7.5 mg/kg bwt q. 24 h for 3 weeks). The horse was had been established. rested for 3 months after which period he was gradually Concurrent pleural effusion is commonly reported in cases reintroduced to exercise. Twelve months on, the horse of pericarditis (Worth and Reef 1998), usually as a result of remains bright and has returned to his previous level of inflammation and not simple transudation, but may also be athletic performance. related to right sided . Pleuritis could be initially suspected based on thoracic auscultation and percussion; Discussion however, primary pleural effusion without pericardial disease is usually associated with a normal arterial pressure, Pericarditis is an uncommon condition in horses. A search normal jugular veins, and heart sounds that are often audible of veterinary literature since 1987 revealed 77 cases of over a wider area than normal rather than muffled (Freestone pericarditis described in horses (Freestone et al. 1987; et al. 1987). Pericardial effusion can also develop following Bernard et al. 1990; Vörös et al. 1991; Hardy et al. 1992; pleuropneumonia (Bonagura and Reef 2004) so Robinson et al. 1992; Worth and Reef 1998; May et al. 2002; thoracocentesis may be necessary to rule that possibility out. Seahorn et al. 2003; Perkins et al. 2004), although Electrocardiographic abnormalities associated with 38 of these occurred as a single outbreak in Kentucky pericardial effusion and tamponade include diminished in the spring of 2001 (Seahorn et al. 2003; Bolin et al. 2005). QRS voltage and (Freestone et al. Three forms have classically been described in horses 1987; Vörös et al. 1991; Robinson et al. 1992; Worth and (Freestone et al. 1987; Hardy et al. 1992; Worth and Reef Reef 1998). Low voltage QRS complexes may also occur in 1998; Seahorn et al. 2003; Jesty and Reef 2006). 1) Effusive horses with chronic pleuritis, diaphragmatic hernia, other pericarditis is characterised by accumulation of fluid in the chronic medical disorders and even in some apparently pericardial sac. 2) Fibrinous pericarditis is characterised by normal horses. Electrical alternans is attributed to accumulation of fibrin in the pericardial sac, along the movement of the heart within the excess volume of parietal pericardial surface, with or without effusion. 3) pericardial fluid and, although not seen in all cases of Constrictive pericarditis is characterised by fibrosis and pericardial effusion, is uncommon in other conditions. thickening of the pericardial sac, which restricts diastolic Radiographic examination of the thorax in dogs with filling and compromises cardiac function; this is a potential pericardial effusion often demonstrates and sequel of pericardial inflammation or the deposition of rounding of the cardiac silhouette (Thomas 1983). fibrin within the pericardial sac, or a complication of any Radiography, however, is of limited value in establishing the insult to the pericardium. These forms tend to overlap and diagnosis of pericardial effusion in horses (Freestone et al. one can evolve into another; therefore pericardial 1987) and so thoracic radiographs were not taken in this effusions may be better classified by the aetiology or by case. The most valuable noninvasive diagnostic procedure the physical characteristics of the fluid. As with any other for the detection of pericardial effusion is body cavity, the 4 types of potential fluid composition echocardiography. This allows identification of the include transudate, modified transudate, exudates pericardial fluid space and differentiation from pleural (inflammatory, noninflammatory) and haemorrhage effusion (Freestone et al. 1987). The hallmark of pericardial (sanguineous or serosanguineous) (Kienle 1998). effusion is an anechoic space between the epicardial and The most common presenting clinical signs are not parietal pericardial surfaces. Echocardiographic studies specific for pericarditis and include fever (in cases of septic are also valuable in monitoring the reduction and, in some pericarditis), anorexia and lethargy. Horses with pericarditis cases, reaccumulation of fluid following pericardiocentesis, may also present with signs of colic. Specific signs fibrin accumulation and pericardial thickening. associated with pericardial effusion include tachycardia Measuring cardiac troponin I (cTnI) in plasma is the and muffled heart sounds. If cardiac tamponade has gold standard for detecting myocardial injury in horses. developed, signs of right-sided heart failure (jugular and However, an elevation in its serum levels is not specific, as

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it is not uncommon secondary to tachyarrhythmias, or sac had been emptied. Due to the accumulation of fluid in even in association with endurance and short-term the pericardial sac the intrapericardial pressure rises until it strenuous exercise (Cornelisse et al. 2000; Schwarzwald equilibrates with the right atrial and right ventricular et al. 2003; Nostel and Häggström 2008; Divers et al. diastolic pressures. At that point the transmural distending 2009). pressure is zero and cardiac tamponade begins. Further Treatment of effusive pericarditis with tamponade accumulation of fluid causes intrapericardial pressure, right should include pericardial drainage and should be atrial and right ventricular diastolic pressures to rise in performed as soon as possible (Freestone et al. 1987; Vörös concert to the level of the left atrial and left ventricular et al. 1991; Robinson et al. 1992; Worth and Reef 1998; Jesty diastolic pressures, and subsequently all pressures rise and Reef 2006). However, there are other causes of together (Kienle 1998). Although paradoxical, a reduction pericardial effusion, such as haemopericardium, in which in the mean arterial pressure following drainage is actually centesis may not be recommended or necessary. If indicative of decreased intrapericardial pressure and pericardiocentesis is to be performed there should be at improved ventricular filling. least 5 cm of fluid surrounding the heart to justify use of a Following drainage of the fluid in the pericardial space large bore (usually 24 gauge) chest drain (Worth and Reef different murmurs were noted on cardiac auscultation. 1998; Jesty and Reef 2006). Use of an over the needle Jets of regurgitation were also noted through the mitral, intravenous catheter has also been reported (Freestone tricuspid and aortic valves with colour flow Doppler et al. 1987; Vörös et al. 1991; May et al. 2002). Due to echocardiographic studies. It is possible that the the amount of fluid detected in this case on regurgitations developed due to volume overload and echocardiographic examination, we opted for a 24 gauge valve annulus stretching induced by rapid drainage of the chest drain and encountered no complications. The site of pericardial fluid. This would also explain why the murmurs pericardiocentesis is based upon the most superficial extent reduced gradually over the following days. of the pericardium as seen on ultrasonography, and should A pericardial friction rub also became audible after ideally be the location with the greatest depth between the drainage of the pericardial fluid. Pericardial friction rubs pericardium and the epicardium/heart in both systole and are heard when the inflamed epicardial and pericardial diastole, usually the fourth, fifth or sixth intercostal spaces on surfaces rub against one another, as occurs in cases of the left side of the thorax (Freestone et al. 1987; Vörös et al. fibrinous pericarditis (Hardy et al. 1992; Jesty and Reef 1991; May et al. 2002). A right side approach has also been 2006), but are not audible in most cases of effusive described (Freestone et al. 1987; Perkins et al. 2004). In this pericarditis until the pericardial fluid has been drained case, we opted for drainage from the left side, with the (Freestone et al. 1987) as happened in this case. ultrasound transducer placed on the right side to facilitate Classically, pericardial friction rubs are triphasic, occurring right sided echocardiographic monitoring during the during atrial systole, ventricular systole and at the end of procedure. Following drainage, the pericardial space can early ventricular filling, although they can also be biphasic. be lavaged with saline (0.9% NaCl) or other isotonic Treatment by partial using a right polyionic fluid. The volume of lavage fluid recommended thoracotomy approach has been attempted in a case of varies, depending on the nature of the pericardial effusion. constrictive pericarditis in a mare (Hardy et al. 1992). In that More fluid has been recommended for cases where report recurrence of the constrictive pathology was noted significant amounts of fibrin deposits can be seen on 6 weeks after the surgical procedure because of severe ultrasound examination. Antibiotics can be added to the epicardial involvement. However, in selected cases in lavage fluid; sodium penicillin, gentamicin and which the disease is limited to the pericardium or in horses sulphonamides have been instilled in the pericardial space that experience repeat idiopathic effusions, partial safely in previous reports (Vörös et al. 1991; Worth and Reef pericardiectomy may offer a mode of therapy. 1998; Jesty and Reef 2006) but combination of antibiotics Horses with pericardial effusion should be treated with should not be used to avoid formation of precipitates. In this broad-spectrum antibiotics until results of bacterial and case we chose instillation of cefquinome due to its broad cytological evaluation are available. We started antibiotic spectrum activity and fluid form. therapy in case of bacterial involvement until results of Prior to pericardiocentesis, an indwelling jugular bacterial culture were available and to prevent secondary catheter should be placed to facilitate administration bacterial infection following pericardiocentesis. Antibiotic of resuscitative medications if necessary during the treatment was also continued prophylactically following procedure. discharge, although this was probably not necessary since Continual electrocardiographic monitoring is also there was no evidence of a bacterial cause. Horses recommended to monitor for arrhythmias that would be suspected of having immune-mediated or viral induced indicative of irritation of the epicardial surface by the drain pericarditis may be treated with corticosteroids, both (Jesty and Reef 2006). We also placed an intra-arterial systemically or intrapericardially. Reported therapies catheter to monitor arterial pressure during the procedure include 20–50 mg of dexamethasone, i.v. or and found that the mean pressure decreased from intrapericardial (i.p.), every 24 h; 100 mg prednisolone 135 mmHg at the start to 115 mmHg once the pericardial i.p. or 30 mg triamcinolone i.p. (Jesty 2009). Use of

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corticosteroids in these animals is still somewhat References controversial (Freestone et al. 1987; Robinson et al. 1992; Worth and Reef 1998). Most of the opinion suggests that the Bernard, W., Reef, V.B. and Clark, E.S. (1990) Pericarditis in horses: Six benefits of decreasing the immune response to viruses and cases (1982-1986). J. Am. vet. med. Ass. 196, 468-471. possible immune mediated sequelae to viral infections Bolin, D.C., Donahue, J.M., Vickers, M.L., Harrison, L., Sells, S., Giles, R.C., Hong, C.B., Poonacha, K.B., Roberts, J., Sebastion, M.M., Swerczek, outweigh the risk of viral recrudescence; however, the T.W., Tramontin, R. and Williams, N.M. (2005) Microbiologic and therapeutic efficacy of corticosteroids in this condition has pathologic findings in an epidemic of equine pericarditis. J. vet. not been evaluated in horses, and we chose not to diag. Invest. 17, 38-44. administer them in this case. Systemic nonsteroidal Bonagura, J.D. and Reef, V.B. (2004) Disorders of the cardiovascular system. In: Equine Internal Medicine, 2nd edn., Eds: S.M. anti-inflammatories (NSAIDs) can be used to control Reed, W.M. Bayly and D.C. Sellon, Saunders Elsevier, St Louis. pp discomfort regardless of the nature of pericarditis. A 355-459. decision was made in this case not to use NSAIDs due to Cornelisse, C.J., Schott, H.C., II, Olivier, N.B., Mullaney, T.P., Koller, A., the azotaemia. Wilson, D.V. and Derksen, F.J. (2000) Concentration of cardiac Diagnosis of pericardial effusion can be reached troponin I in a horse with a ruptured aortic regurgitation jet lesion and . J. Am. vet. med. Ass. 217, 231- through physical examination and ancillary diagnostic 235. tools; however, determination of the exact cause can be Divers, T.J., Kraus, M.S., Jesty, S.A., Miller, A.D., Mohammed, H.O., Gelzer, more difficult. Pericardial effusion can develop secondary A.R.M., Mitchell, L.M., Soderholm, L.V. and Ducharme, N.G. (2009) to viral or bacterial infection, septicaemia, trauma/vessel Clinical findings and serum cardiac troponin I concentrations in horses after intragastric administration of sodium monensin. J. vet. rupture, neoplasia or in conjunction with primary pleural diag. Invest. 21, 338-343. effusion or pleuropneumonia (Freestone et al. 1987; Freestone, J.F., Thomas, W.P., Carlson, G.P. and Brumbaugh, G.W. (1987) Bernard et al. 1990; Robinson et al. 1992; Worth and Reef Idiopathic effusive pericarditis with tamponade in the horse. Equine 1998; May et al. 2002). It is not unusual for the exact cause vet. J. 19, 38-42. to be undeterminable, therefore many cases are Hardy, J., Robertson, J.T. and Reed, S.M. (1992) Constrictive pericarditis in a mare: Attempted treatment by partial pericardiectomy. Equine considered idiopathic. In horses, septic pericarditis or vet. J. 24, 151-154. idiopathic pericarditis are the most frequent diagnoses Jesty, S.A. (2009) Pericarditis. In: Current Therapy in Equine Medicine, 6th (Freestone et al. 1987; Bernard et al. 1990; Worth and Reef edn., Eds: N.E. Robinson and K.A. Sprayberry, Saunders Elsevier, St 1998). No bacterial agents were identified during analysis Louis. pp 207-211. of the pericardial fluid in this case. Jesty, S.A. and Reef, V.B. (2006) Septicaemia and cardiovascular During the spring of 2001 a larger than usual number of infections in horses. Vet. Clin. Equine 22, 481-495. horses were diagnosed with fibrinous pericarditis in Kienle, R.D. (1998) Pericardial disease and cardiac neoplasia. In: Small Animal Cardiovascular Medicine, 1st edn., Eds: M.D. Kittleson and Kentucky. These cases of pericarditis occurred R.D. Kienle, Mosby, St Louis. pp 413-432. concurrently with components of the mare reproductive May, K.A., Cheramie, H.S., Howard, R.D., Duesterdieck, K., Moll, H.D., loss syndrome (MRLS). Actinobacillus species were the Pleasant, R.S. and Pyle, R.L. (2002) Purulent pericarditis as a sequela principal isolates from affected animals. Actinobacilli are to clostridial myositis in a horse. Equine vet. J. 34, 636-640. commensal bacteria of mucosal surfaces in the horse that Nostel, K. and Häggström, J. (2008) Resting concentrations of cardiac troponin I in fit horses and effect of racing. J. vet. Cardiol. 10, sporadically produce secondary or opportunistic 105-109. infections. It is unlikely that primary infections with Perkins, S.L., Magdesian, K.G., Thomas, W.P. and Spier, S.J. (2004) commensal bacteria could have resulted in the abrupt Pericarditis and pleuritis caused by Corynebacterium onset and disappearance and broad geographic pseudotuberculosis in a horse. J. Am. vet. med. Ass. 224, 1133-1138, distribution of pericarditis cases. It was suggested that 1112. impairment of the immune system by an agent or toxin Robinson, J.A., Marr, C.M., Reef, V.B. and Sweeney, R.W. (1992) Idiopathic, aseptic, effusive, fibrinous, nonconstrictive pericarditis associated with the eastern tent caterpillar contributed to with tamponade in a Standardbred filly. J. Am. vet. med. Ass. 201, a temporary breakdown of mucosal defence mechanisms 1593-1598. (Seahorn et al. 2003; Bolin et al. 2005). Schwarzwald, C.C., Hardy, J. and Buccellato, M. (2003) High cardiac Historically, the prognosis for horses with pericarditis has troponin I serum concentration in a horse with multiform ventricular tachycardia and myocardial necrosis. J. vet. intern. Med. 17, been considered guarded, especially when septic causes 364-368. were suspected. However, successful outcomes have Seahorn, J.L., Slovis, N.M., Reimer, J.M., Carey, V.J., Donahue, J.G. and been reported more recently (Freestone et al. 1987; Cohen, N.D. (2003) Case-control study of factors associated with Bernard et al. 1990; Worth and Reef 1998; May et al. 2002; fibrinous pericarditis among horses in central Kentucky during spring J. Am. vet. med. Ass. Perkins et al. 2004) and, when pericarditis is adequately 2001. 223, 832-838. treated, the prognosis for affected horses is good. Thomas, W.P. (1983) Pericardial disease. In: Textbook of Veterinary Internal Medicine. Diseases of the Dog and Cat, 2nd edn., Vol. 1, Ed: S.J. Ettinger, W. B. Saunders, Philadelphia. pp 1029-1051. Vörös, K., Felkai, C., Szilágyi, Z. and Papp, A. (1991) Two-dimensional Manufacturers’ addresses echocardiographically guided pericardiocentesis in a horse with traumatic pericarditis. J. Am. vet. med. Ass. 198, 1953-1956. 1GE Medical Systems, Chalfont St. Gites, Buckinghamshire, UK. Worth, L.T. and Reef, V.B. (1998) Pericarditis in horses: 18 cases 2Intervet, Walton, Milton Keynes, UK. (1986-1995). J. Am. vet. med. Ass. 212, 248-253.

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