Foxtail-associated endocarditis in a cat

Abstract

An adult female neutered domestic shorthair cat developed right heart failure 1 week after having surgical drainage of a neck abscess of unknown etiology established at our hospital. Echocardiography revealed a large vegetative mass adhered to the tricuspid valve. Post-mortem examination revealed fibrinous endocarditis and myocarditis associated with the presence of a grass awn (Hordeum species) foreign body. Foxtail migration with subsequent thrombus and endocarditis formation on the tricuspid valve is considered a very unusual sequel to foxtail migration.

Infectious (bacterial) and non-infectious endocarditis are rare in cats, with an estimated incidence of 6–18 cases per 100,000 cats presented for evaluation. ^1–3 The most common bacterial cause of endocarditis in the dog is Streptococci species. ⁴ In cats, reported causes of bacterial endocarditis include Bartonella species, Escherichia coli, Streptococcus species, and Staphylococcus species. ⁵ Although intrathoracic grass awns are not uncommon, an intracardiac grass awn with secondary endocarditis has not been reported in a feline patient. The majority of cardiac foreign body cases reported have been in dogs and include coils or surgical implants; foreign bodies of the myocardium and pericardium such as wood, bullets, and metal have also been described, but none have been associated with endocarditis. ^6–11 These cases are usually associated with thoracic and cardiac disease including pneumothorax, pericardial effusion, arrhythmias, pyothorax, respiratory distress, and/or death; however, systemic manifestations from the resultant inflammation, infection, and/or hypercoagulability may also occur such as systemic inflammatory response syndrome (SIRS), sepsis, and/or disseminated intravascular coagulation (DIC).

Reported causes of right heart failure (RHF) in cats include tricuspid valve dysplasia, heartworm disease, arrhythmogenic right ventricular (RV) cardiomyopathy, pulmonic stenosis, restrictive cardiomyopathy, thyrotoxic cardiac disease, and hypertrophic cardiomyopathy. ¹² RHF is diagnosed clinically in cats when there are cavitary effusions (abdominal, pleural, and/or pericardial) in combination with right heart enlargement and central venous distension evident via physical examination (jugular distention), echocardiography or radiography. ¹ Definitive diagnosis is made by confirming an elevated central venous pressure in the presence of right heart disease. ¹²

Foxtails, which are awns of Hordeum species of grasses, are found throughout a majority of the United States. These grass awns are a frequent cause of tissue foreign bodies in dogs and cats, and have been reported in the eye and orbit, cranium, spinal canal, and organs within the peritoneal and thoracic cavities. ^13–19 They are most commonly located in the external ear canal, interdigital webs, thoracic cavity, third eyelid, and nasal cavity. ^13–19 A sharply pointed tip and retrograde barbs make the grass awn ideal for penetration and unidirectional movement. ¹⁶ Like most plant foreign material, grass awns act as a fomite for bacterial inoculation. Actinomyces, Staphylococcus, and Streptococcus species are the most common bacteria isolated from wounds associated with grass awns, although Pasteurella multocida and Nocardia species are also commonly reported. ^14,16,20 This report describes a cat in which aberrant migration of a grass awn and attachment to the tricuspid valve resulted in fibrinous endocarditis and myocarditis with subsequent RHF.

An adult female neutered 3.3 kg domestic shorthair cat of unknown age presented for evaluation of a ventral neck abscess that was treated by surgical drain placement. At the time of original presentation the physical examination, hematology (including feline leukemia virus/feline immunodeficiency virus serology), and chemistry were within normal limits. Three days postoperatively the cat presented with anorexia, lethargy, a dry cough and a persistent bloody discharge from the drain site. Pyrexia (105.2F (40.6°C); reference interval (RI), 101–102.5F (38.3–39.16°C)), tachycardia (240 bpm; RI, 140–220 bpm), a grade II/VI systolic heart murmur with point of maximal intensity localized to the left parasternal cardiac apex, a gallop rhythm (a short recording of this can be found on Science Direct at doi:10.1016/j.jfms.2010.08.009), and a persistent firm swelling were noted at the abscess site when the physical examination was performed. Complete blood count (CBC) revealed a mild mature neutrophilia (12.66×10³/μl; RI 2.5–12.5×10³/μl) and a normocytic, normochromic non-regenerative anemia (packed cell volume (PCV) 26%, RI 30–45%). Blood chemistry revealed hypoalbuminemia (1.9 g/dl; RI 2.2–4.0 g/dl) and hyperbilirubinemia (5.5 mg/dl; RI 0–0.9 mg/dl). Thoracic and neck radiographs showed an increased soft tissue opacity and subcutaneous emphysema of the ventral neck, with no evident thoracic abnormalities.

The patient was treated with 140 ml/kg/day intravenous (IV) Normasol-R, IV enrofloxacin (5 mg/kg q24 h) and IV ampicillin (22 mg/kg q8 h). Persistent hypothermia developed (95.9F–99.2F (35.5–37.3°C); RI 101–102.5F (38.3–39.16°C)). Hypotension was noted using a Doppler ultrasonic flow meter (systolic pressure of 75 mmHg; RI 118–162 mmHg). PCV and total protein decreased to 18% and 4.6 g/dl, respectively, and continued to decline at which point the patient was blood typed (type A) and a unit of packed red blood cells (pRBC, 60 ml) was transfused. Recheck CBC documented a leukocytosis (29.6×10³/μl; RI 4.2–15.6×10³/μl) with a mature neutrophilia (26,048/μl; RI 2500–12,500/μl), persistence of the non-regenerative anemia, and development of thrombocytopenia (40,000×10³/μl; RI 170–600×10³/μl). Prothrombin time was 16.3 s (RI 7–12.7 s) and partial thromboplastin time was 26.4 s (RI 10–28 s). D-Dimer concentration was elevated (500–1000 ng/ml; RI<250 ng/ml). Prednisone (1 mg/kg subcutaneous (SC) q12 h) and doxycycline (5 mg/kg orally q12 h) were added due to suspicion of immune-mediated hemolytic anemia. Following the development of acute inspiratory dyspnea, echocardiography revealed pleural effusion, severe right atrial dilatation, as well as a 1.5×0.6×0.8 cm vegetative mass attached to the ventricular surface of the valve leaflets (Fig 1). The mass was of mixed echogenicity and extended through the right ventricular outflow tract (RVOT). The vegetation was associated with moderate tricuspid regurgitation as well as turbulent flow through the RVOT. About 80 ml of yellow pleural effusion (transudate, protein <2.0, and low numbers of nucleated cells) was removed via thoracocentesis. No evidence of inflammation or malignancy was identified. Abdominal ultrasound revealed mild mesenteric lymphadenopathy, a moderate amount of ascites (transudate), and congested hepatic vessels. A diagnosis of RHF was made due to the presence of cavitary effusion in combination with central venous congestion and right heart enlargement. Euthanasia was elected. Bradycardia (112 bpm; RI 140–220 bpm) was noted just prior to euthanasia.

Fig 1

Modified right parasternal long-axis echocardiographic image. RV=right ventricle; LV=left ventricle; TV=tricuspid valve; RA=right atrium; TR=tricuspid regurgitation.

Post-mortem examination was performed and revealed a large, dark red, friable mass adhered to the tricuspid valve. The mass was attached to the ventricular wall and extended throughout the right ventricle to the level of the pulmonic valve. Dissection revealed a foxtail within the mass (Fig 2). Bilateral petechiation of the renal cortices and medulla was suggestive of acute renal infarction. Histopathologic evaluation of the right ventricle and vegetative mass documented fibrinous endocarditis and myocarditis.

Fig 2

Image of thrombus with foxtail removed.

This case represents a rare complication of grass awn migration causing tricuspid valvular endocarditis. The tricuspid valve is an uncommon site of endocarditis in small animals. In this case, it is possible that the foxtail migrated from the ventral neck wound entering the jugular vein and traveled hematogenously to the tricuspid valve. Alternatively, it may have been swallowed and migrated through the esophagus, or traveled through the thoracic inlet, mediastinum and right atrial wall. These routes are less likely due to the proximity of the jugular vein to the external abscess and direct communication of the jugular vein with the tricuspid valve. Once attached, the grass awn would serve as a nidus for thrombus formation that would ultimately allow for the formation of systemic thromboembolic disease through induction of a severe inflammatory response. Suspected systemic embolization in the kidneys of this patient, may have been due to associated complications of endocarditis (such as SIRS and/or DIC), or may have been due to an undiscovered right to left intracardiac shunt associated with the vegetative lesion. The latter is unlikely given the lack of RV hypertrophy that occurs with chronic pulmonary hypertension or RVOT obstruction from a right to left shunt. It is, however, possible that acute tricuspid regurgitation and RVOT obstruction causing right atrial pressures in excess of left atrial pressures could cause right to left shunting of blood across a patent foramen ovale, which under normal atrial pressures would have been functionally closed.

The vegetative mass and associated thrombus occupied approximately 75% of the RV lumen and outflow tract. RHF may have occurred secondary to obstruction of both RV inflow and outflow by the mass. Obstruction of inflow (acquired tricuspid stenosis) would be expected to elevate right atrial pressure. Additionally, elevations in RV systolic pressure due to RVOT obstruction would exacerbate tricuspid regurgitant volume, as well as increase systolic RV wall stress and promote RV systolic dysfunction. Myocarditis alone can cause severe impairment of myocardial function, and may have further elevated RV filling pressure and depressed RV inotropy. While the proximate cause of the RHF remains speculative, these hemodynamic perturbations are the most likely cause of congestive heart failure in the cat of this report.

SIRS is a common sequel of a number of severe diseases, including endocarditis. Patients with SIRS are in a hypercoagulable state due to inflammatory mediator activation of the coagulation cascade resulting in microvascular thrombosis, ischemia, and ultimately end organ damage. ²¹ In systemically ill cats, SIRS is diagnosed if three of four of the following criteria are met: rectal temperature >103.5F (39.7°C) or <101F (38.3°C), heart rate >225 bpm or <140 bpm, respiratory rate >40 breaths/min, and a white cell count of >19,500/ml or <5000/ml or band neutrophil fraction >5%. ²² Tachypnea, bradycardia, hypothermia, anemia, hypoalbuminemia, and icterus are common abnormalities in cats with SIRS and/or sepsis and were all abnormalities found in this case, therefore, SIRS was diagnosed. ^2,22

Disseminated intravascular coagulopathy (DIC) is a clinical syndrome that results from intravascular activation of coagulation combined with insufficient anti-coagulant pathway activity. DIC is the consequence of severe underlying, usually inflammatory, pathology. The end result of DIC is microvascular thrombosis followed by fibrinolysis. Platelets and clotting factors are exhausted during the process of microvascular thrombus formation causing a consumptive coagulopathy. ²³

Hemolysis remains a possible cause of the observed anemia. Hemolysis can be a consequence of sepsis/SIRS, but it is feasible that turbulence within the right ventricle associated with the presence of a foreign body and thrombus also played a role in accelerated erythrocyte destruction.

In the dog, endocarditis lesions of the left heart greater than 1 cm in size pose the greatest risk of causing thromboembolic events, which most commonly infarct the spleen and kidney. ² In this case we hypothesize that the diffuse renal petechiations may have been a consequence of massive thromboembolic disease secondary to SIRS or DIC, both end results of the large vegetative lesion, rather than from distant embolization of fragments of the valvular lesion itself. Although bacterial sepsis was highly likely in this patient, it is not possible to further characterize the etiology due to failure to culture the blood pre- or post-mortem. The size of the thrombus in the ventricle, the endocarditis and the presence of SIRS, and RHF contributed to shock, and likely would have resulted in death if euthanasia had not been performed.

This case is unique, in that RHF was caused by a grass awn that migrated to the heart and attached to the tricuspid valve leaflets. Reports of foxtail migration can be found in the veterinary literature. ^13–19 Foxtail migration with subsequent thrombus and endocarditis formation on the tricuspid valve has not been reported in a veterinary patient.