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Acquired Pulmonic Stenosis Due to a Compressing Intrathoracic Abscess in a Thoroughbred Yearling
Journal of Equine Veterinary Science 35 (2015) 692–696
Contents lists available at ScienceDirect
Journal of Equine Veterinary Science journal homepage: www.j-evs.com
Case Report
Acquired Pulmonic Stenosis Due to a Compressing Intrathoracic Abscess in a Thoroughbred Yearling Sigrid Hyldahl Laursen a, *, Gaby van Galen a, Godelind A. Wolf-Jäckel b, Rikke Buhl a a b
Department of Large Animal Sciences, University of Copenhagen, Taastrup, Denmark Department of Veterinary Disease Biology, University of Copenhagen, Frederiksberg, Denmark
a r t i c l e i n f o
a b s t r a c t
Article history: Received 10 December 2014 Received in revised form 23 March 2015 Accepted 11 June 2015 Available online 18 June 2015
A 12-month-old Thoroughbred filly was admitted for poor weight gain, intermittent fever, and distal limb edema. Initial clinical examination revealed tachycardia, tachypnea, and pyrexia. A loud holosystolic murmur was identified by cardiac auscultation, and thoracic auscultation identified bilateral diffuse crackles. Echocardiography demonstrated severe extrinsic pulmonic stenosis, enlargement of the right ventricle and compression of the left ventricle. Mediastinal ultrasound revealed a large, encapsulated, cavernous mass in the cranial thorax, compressing the heart. Bacterial culture of tracheal aspirates and aspirations of the intrathoracic mass yielded a pure culture of Streptococcus equi spp. zooepidemicus. Acquired pulmonic stenosis has not previously been reported in horses, whereas congenital pulmonic stenosis has. This case report demonstrates that in line with human medicine, pulmonic stenosis can be acquired because of thoracic masses compressing the pulmonic artery. Ó 2015 Elsevier Inc. All rights reserved.
Keywords: Pulmonic stenosis Pneumonia Streptococcus equi spp. zooepidemicus Intrathoracic abscess
1. Introduction Pulmonic stenosis is a rare finding in the horse, characterized by an increased resistance emptying the right ventricle that is caused by either intrinsic obstruction or extrinsic compression of the right ventricular outflow tract. This in turn causes hypertrophy of and increased pressure within the right ventricle and atrium. Severe stenosis will decrease the stroke volume of the heart and cause compensatory increased heart rates [1]. The condition in turn will thus lead to systemic circulatory changes causing exercise intolerance, weight loss, peripheral edema, and pulmonary edema [2]. Pulmonic stenosis has been described as a congenital disorder causing severe hypoxia in affected foals [3,4]. These congenital abnormalities are usually diagnosed early
* Corresponding author at: Sigrid Hyldahl Laursen, Department of Large Animal Sciences, University of Copenhagen, Højbakkegaard Alle 5, 2630 Taastrup, Denmark. E-mail address: [email protected] (S. Hyldahl Laursen). 0737-0806/$ – see front matter Ó 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jevs.2015.06.009
in life because of their severe clinical impact [4]. Only a single report describes an assumed congenital malformation of the pulmonic valves causing pulmonic stenosis in an adult horse [1]. Theoretically, pulmonic stenosis can also be acquired in the horse because of external compression. Extrinsic pulmonic stenosis due to cranial thoracic neoplasia has been described in the human literature [5–9]. Cranial thoracic abscesses may arise as a sequel to infections such as pneumonia, pulmonary abscesses, pericarditis, or pleuropneumonia and can result in cardiac compression depending on localization [10,11]. Multiple reports describe cranial thoracic masses including neoplasia and abscess formation in the horse, but to the authors’ knowledge, there are no reports of masses causing acquired pulmonic stenosis in the horse [12,13]. 2. Case History A 12-month-old Thoroughbred filly was referred to the Large Animal Teaching Hospital at the University of
S. Hyldahl Laursen et al. / Journal of Equine Veterinary Science 35 (2015) 692–696
Copenhagen for evaluation of ill thrift and intermittent fever of 3- to 4-week duration. Before referral, a loud holosystolic murmur was noted as well as distal limb edema of the front limbs. Four weeks before admission, several yearlings in the same herd were noted to have respiratory symptoms including nasal discharge, fever, and cough. No prior diagnostic tests were performed on the facility to determine the cause of the infection. The horse never showed overt symptoms of airway disease and had not received antibiotic treatment before referral. 2.1. Initial Clinical Findings At the time of admission, the filly was bright and alert with a good appetite. The horse appeared unthrifty, with matted hair coat and a body condition score of 2/9. The initial clinical examination revealed an elevated heart rate (60 bpm) and rectal temperature (38.7 C). The filly presented with moderately elevated respiratory rate (20 rpm), a mild abdominal respiratory pattern, and bilateral mucopurulent nasal discharge. An intermittent productive cough was also noted, and coughing was easily provoked by compression of the larynx and trachea. The submandibular lymph nodes were normal on palpation. Thoracic auscultation identified diffuse crackles bilaterally. No rattling sounds were evident on tracheal auscultation. Moderate, pitting distal limb edema was noted on both front limbs. The filly appeared well hydrated, mucous membranes were pink and moist, and capillary refill time was within 2 seconds. Normal stasis and emptying of the jugular veins was noted, and on palpation of the facial artery, a strong pulse with normal rhythm was identified. Cardiac auscultation revealed a holosystolic murmur, grade 4/6 with point of maximal intensity over the pulmonic ostium. Persistent tachycardia was noted, but no arrhythmias could be identified on auscultation or subsequent base-apex electrocardiogram examination. 2.2. Initial Diagnostics Blood samples at the time of admission revealed mild anemia (packed cell volume: 27% [20%–41%]), severe neutrophilic leukocytosis (white blood cells: 20,980 cells/ mL [5,450–12,650 cells/mL], neutrophils: 14,920 cells/mL [2,260–7,220 cells/mL], lymphocytes: 4,240 cells/mL [1,260–5,740 cells/mL], monocytes: 1,280 cells/mL [0–1,000 cells/mL], eosinophils: 100 cells/mL [0–1,000 cells/mL], basophils: 120 cells/mL [0–290 cells/mL], hyperfibrinogenemia [fibrinogen: 7.76 g/L; 1–4 g/L]), and increased serum amyloid A (3265.4 mg/L [0–30 mg/L]), and decreased iron levels (5.99 mmol/L [13.1–25.1 mmol/L]). All these blood parameters indicate severe inflammation. Cranial thoracic ultrasound, through the triceps muscle, revealed a large, oval-shaped, cavernous, multiloculated mass measuring approximately 15 by 20 cm. The mass was surrounded by a hyperechoic capsule approximately 3 cm in thickness and was filled with slightly hyperechoic fluid material. The mass appeared to occupy the majority of the cranial thoracic space, exerting significant compression of the heart and in particular the
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pulmonary artery (Fig. 1). Thoracic ultrasound was suggestive of mild bilateral pleural inflammation (comet tails) and mild pneumonia. Echocardiography revealed severe enlargement of the right ventricle (luminal diameter) and compression of the left ventricle, with marked bulging of the interventricular septum into the left ventricle. Echocardiographic measurements are presented in Table 1. The right ventricular internal diameter at end diastole was increased, and the left ventricular internal diameter at end diastole demonstrated severe extrinsic volume restriction (Fig. 2). The pulmonary artery was severely compressed by the external mass. The diameter of the pulmonary artery obtained from the right parasternal angled view was severely reduced to 3.53 cm in systole and 1.74 cm in diastole (Fig. 3). Color Doppler examination identified no valvular regurgitation at the pulmonic, tricuspid, mitral, or aortic valves. Maximum pulmonary velocity was 2.3 m/s (reference values, 0.78–1.04 m/s [15]; Fig. 3). Minimal pericardial fluid was observed (Fig. 2). Endoscopy of the upper airways demonstrated moderate pharyngeal lymphoid hyperplasia (grade III/IV) and mucopurulent exudate in the trachea (grade III/IV) [16]. A subsequent transendoscopic tracheal aspirate through a nonguarded catheter using 30 mL of sterile saline demonstrated macroscopically visible mucopurulent secretions and contained 82% neutrophils, 7.5% macrophages, 1.5% lymphocytes, 0.5% eosinophils, and 8.5% epithelial cells, suggestive of pulmonary inflammation. Bacterial culture of tracheal aspirates and a direct ultrasound-guided aspirate of the intrathoracic mass yielded a pure culture of Streptococcus equi spp. zooepidemicus sensitive to penicillin. Thoracic radiographs demonstrated increased cranioventral radio density and diffusely increased bronchointerstitial pattern, suggestive of chronic bronchopneumonia. On radiographs, no mass could be visualized and they were not diagnostic in terms of distribution of the cranial thoracic mass. A blood culture obtained by strict aseptic technique via venipuncture of the left jugular vein yielded no bacterial growth.
Fig. 1. Cranial thoracic ultrasound: Left parasternal ultrasound view obtained at the third intercostal space, showing a large cavernous fluid-filled structure with a thick capsule occupying almost the entire cranial thorax.
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Table 1 Echocardiographic measurements of the case and reference ranges. Variable
Size (cm)
Reference Ranges (Thoroughbred Yearlings) [14]
IVSs IVSd LVIDs LVIDd LVFWs LVFWd RVIDd FS% Ao PADs PADd LA Ao/PADs
3.8 2.8 6.4 8.0 2.6 2.8 7.0 20% 4.8 3.5 1.74 9.0 1.4
3.01 1.93 7.12 10.40 2.94 2.22 d 21.1 4.34 d d 3.82 d
0.85 0.46 0.74 0.85 0.45 0.21
1.4 0.32
0.60
Abbreviations: Ao, aortic diameter at peak systole (cm); Ao/PADs, aortic diameter at peak systole (cm)/pulmonic artery diameter at peak systole (cm); FS%, fractional shortening (%); IVSd, interventricular septal thickness at end diastole (cm); IVSs, interventricular septal thickness at peak systole (cm); LA, left atrial diameter at end diastole (cm); LVFWd, left ventricular free wall at end diastole (cm); LVFWs, left ventricular free wall at peak systole (cm); LVIDd, left ventricular internal diameter at end diastole (cm); LVIDs, left ventricular internal diameter at peak systole (cm); PADd, pulmonic artery diameter at end diastole (cm); PADs, pulmonic arterial diameter at peak systole; RVIDd, right ventricular internal diameter at end diastole (cm).
3. Case Progression The filly was initially treated with 1.1 mg/kg of flunixin meglumine oral administration. Because of financial implications and guarded prognosis for recovery and future racing performance, the owner declined further treatment and the horse was euthanized. After euthanasia, a full necropsy was performed.
Fig. 3. Pulse-wave Doppler examination: Right parasternal angled long-axis view (right ventricular outflow view) with color pulse-wave Doppler. This view shows a maximum pulmonary velocity of 2.3 m/s due to severe compression of the pulmonary artery.
pericardium, which contained approximately 50-mL cloudy fluid. The epicardium showed multifocal hyperemia. Fibrous attachments were found between the abscess and the pleura overlying the sternum and the left cranial lung lobe (Fig. 5). This lung lobe was affected by chronic purulent bronchopneumonia. The myocardium and cardiac valves were macroscopically unremarkable and without lesions suggesting congenital pulmonary artery stenosis. Additional findings were related to parasitic infestation unrelated to the cardiopulmonary pathology: chronic, fibrinous, thrombosing endarteritis in the ileocolic artery and cyathostominosis affecting the cecum and colon. The remainder of the postmortem examination was unremarkable.
4. Postmortem Findings External inspection revealed bilateral mucopurulent nasal discharge. In the thoracic cavity, a mediastinal abscess was situated cranially to the heart. The abscess had an almost globose shape, measured 15 cm in diameter, and was encapsulated by approximately 3-cm-thick fibrous tissue (Fig. 4). The abscess was adherent to the cranial
Fig. 2. Echocardiography: Right parasternal long-axis view (four-chamber view) showing an enlargement of the right ventricle and bulging of the interventricular septum into the left ventricle. Left side of the image is ventral. LA, left atrium; LV, left ventricle; RV, right ventricle.
Fig. 4. Postmortem view of the incised cranial thoracic abscess: The abscess was located in the cranial thorax compressing the heart and pulmonary artery. The abscess contained large amounts of purulent material, and it was enclosed by an approximately 3-cm-thick fibrous capsule and was adhered to the pericardium. A, abscess; C, capsule; P, pericardium.
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Fig. 5. Cranial thoracic abscess in situ after dissection of the fibrous capsule from the pericardium: Dissection resulted in drainage of purulent material suggesting adherence of the abscess in part of the pericardium. The abscess was adherent to the pleura overlying the sternum and the left cranial lung lobe. A, abscess; LL, left lung; P, pericardium.
5. Discussion Murmurs associated with the right ventricular outflow tract are rare findings because of the physiologically low pressure within the pulmonary circulation. Systolic murmurs with point of maximal intensity over the pulmonic or aortic ostium may be physiological flow murmurs; however, echocardiographic examination is warranted to establish the exact cause of the murmur and severity of disease [17,18]. The loud systolic murmur associated with the right ventricular outflow tract in this case, in the absence of pulmonic valve abnormality, is most likely related to the stenosis of the pulmonary artery. Few reports in the literature describe pulmonic stenosis in horses. An exaggerated form of the tetralogy of Fallot with a congenital pulmonic stenosis has been described in conjunction with a ventricular septum defect and overriding of the aorta and right ventricular hypertrophy in three Arabian foals but may also occur in solitude [1,3,4,19]. These foals present early in life in cardiac failure and with loud murmurs [3]. These conditions usually carry a poor prognosis and are thus unexpected in older horses [3,4]. In addition, a single case report describes valvular pulmonic stenosis as an incidental finding in an adult Arabian horse with a grade 4/5 systolic murmur. In contrast to the congenital disorders in foals, the adult Arabian horse was clinically unaffected [1]. Echocardiography of the present case demonstrated severe extrinsic pulmonic compression, secondary enlargement of the right ventricular internal diameter, and compression of the left ventricle with marked bulging of the interventricular septum into the left ventricle. Pulse-wave Doppler examination demonstrated increased velocity of blood flow over the pulmonic valve, but as there was no tricuspid regurgitation, a pressure gradient was not calculated. Cardiac catheterization can be used for direct
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measurement of right ventricular pressure, and pulmonary artery catheterization can be used in cases where the origin of pulmonary hypertension is unclear. In cases of secondary pulmonic hypertension due to reduced left ventricular function, pulmonary artery wedge pressure will often equal left ventricular pressure. When pulmonary hypertension is caused by increased pulmonary vascular resistance, such as recurrent airway obstruction, pulmonary wedge pressure will be close to normal values [20,21]. In this case, we did not have the opportunity to perform cardiac catheterization, but pulse-wave Doppler demonstrated high pulmonary velocity with a characteristic dagger-shaped curve, suggestive of increased pressure due to pulmonic stenosis (Fig. 3). Furthermore, thoracic ultrasound showed an extrinsic pulmonic stenosis compressing the pulmonary valve area caused by a large abscess, and therefore, no further diagnostics were pursued. Although cranial thoracic masses have been described to compress the heart in horses [10], no previous reports discuss pulmonic stenosis as a result of extrinsic compression in the horse. Acquired (extrinsic) pulmonic stenosis caused by mediastinal neoplasia has been described in the human literature, and indeed, this case demonstrates that acquired pulmonary stenosis due to an extrinsic mass can also occur in the horse. The condition can be detected by thoracic ultrasonography along with Doppler echocardiography and in humans also by computerized tomography [5,6,10,11]. Computed tomography of the thorax is unfortunately of less use for horses because of size limitations, but it could potentially be performed in foals, small ponies, or donkeys. The present case demonstrates the value of the ultrasonographic view through the triceps muscle in visualizing masses in the cranial thorax. Mediastinal neoplasia in young horses, such as lymphosarcoma, may also present as cavernous encapsulated masses [22]. To differentiate abscess formation from neoplasia, ultrasound-guided aspiration for cytologic examination is essential [13,22]. In this case, the aspiration demonstrated a purulent material, and cytologic examination and bacterial culture confirmed the diagnosis of a mediastinal abscess due to streptococcal infection. Necropsy of the present case demonstrated chronic bronchopneumonia. Thoracic abscessation may arise secondary to trauma, pneumonia, pericarditis, or pleuropneumonia, and most likely, this filly developed a cranial thoracic abscess secondarily to pneumonia. Despite no prior history of respiratory disease, the clinical and necropsy findings were significant, and clinical signs possibly overlooked at the farm. Pathogens most frequently associated with intrathoracic masses in adult horses are Streptococcus spp., Actinobacillus spp., and Escherichia coli. [10,23,24], whereas Rhodococcus equi frequently may cause intrathoracic masses in foals and weanlings [11]. The S. equi spp. zooepidemicus isolated from this case was a Lancefield group C beta hemolytic streptococcus that is commonly isolated from the airways of horses. The organism is often described as an opportunistic pyogenic pathogen causing disease of the respiratory system and reproductive tract [25,26]. Although S. equi spp. zooepidemicus is a part of the normal flora of the respiratory tract in horses and may be considered less pathogenic and not contagious, a recent
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report has found pathogenic strains causing outbreaks of strangles-like symptoms [27]. Indeed, the present case indicates that numerous horses in the herd were infected and showing signs of respiratory disease and, in this case, severe complications, although no diagnostic tests were performed at the farm to identify the pathogen. It is thus possible that the initial outbreak of respiratory disease could have been caused by a viral agent such as Equine Herpes Virus or Equine Influenza and a secondary infection with S. equi spp. zooepidemicus in this particular case. The yearling was euthanized because of financial implications and guarded prognosis. However, medical treatment including prolonged broad-spectrum antimicrobial treatment has been proven effective in a number of reports of intrathoracic abscesses [10,11,24]. In this case, penicillin would be the drug of choice, although issues with regard to penetration of the thick fibrous capsule and large amount of purulent material within the abscess will affect treatment efficacy [28]. One report demonstrated a fair prognosis for racing after successful treatment of pulmonary abscesses although none of these cases presented with pulmonic stenosis [24]. Because of the severity of pulmonic compression and related cardiovascular compromise, surgical drainage followed by prolonged antimicrobial therapy could have been attempted to alleviate the pulmonary artery compression and resolve the infection [10,23]. Byars et al [10] described improvement after surgical drainage and lavage in three horses with cranial thoracic abscesses that were nonresponsive to medical treatment. Furthermore, a more recent study, including 16 horses, has also described standing thoracotomy for persistent thoracic abscesses related to pleuropneumonia with 88% survival and 46% return to previous level of performance [23]. Although these recent studies suggest that prognosis can be reasonably good after surgical drainage, the cranial localization of the abscess and adherences to the left lung and pericardium in the current case would most likely have complicated such an aggressive surgical approach. Moreover, there are no reports in the veterinary literature describing cardiac function after relieving right ventricular outflow tract compression. However, reports from human literature describe good outcomes with normalized cardiac parameters after medical or surgical removal of mediastinal neoplasms causing extrinsic pulmonic stenosis [7–9]. 6. Conclusions This case report shows that acquired pulmonic artery stenosis may arise secondary to thoracic abscessation. It can result in loud murmurs and cardiac compromise in the horse. Furthermore, it illustrates the possible severity of complications of S. equi spp. zooepidemicus infection. References [1] Gehlen H, Bubeck K, Stadler P. Valvular pulmonic stenosis with normal aortic root and intact ventricular and atrial septa in an Arabian horse. Equine Vet Educ 2001;13:286–8. [2] Davis JL, Gardner SY, Schwabenton B, Breuhaus BA. Congestive heart failure in horses: 14 cases (1984-2001). J Am Vet Med Assoc 2002; 220:1512–5.
[3] Hinchcliff KW, Adams WM. Critical pulmonary stenosis in a newborn foal. Equine Vet J 1991;23:318–20. [4] Vitums A, Bayly WM. Pulmonary atresia with dextroposition of the aorta and ventricular septal defect in three Arabian foals. Vet Pathol 1982;19:160–8. [5] Robinson T, Lynch J, Grech E. Non-Hodgkin’s lymphoma causing extrinsic pulmonary artery compression. Eur J Echocardiogr 2008;9: 577–8. [6] Agarwala BN, Thomas LE, Waldman JD. Acquired pulmonary stenosis: ultrasonographic diagnosis. Pediatr Cardiol 1995;16:179–81. [7] Ozer N, Deveci OS, Kaya EB, Demircin M. Mediastinal lymphoma causing extrinsic pulmonary stenosis. Turk Kardiyol Dern Ars 2009; 37:421–4. [8] Pugliatti P, Donato R, Grimaldi P, Nunnari F, de Gregorio C, Zito C, et al. Extrinsic pulmonary stenosis in primary mediastinal B-cellular lymphoma. J Clin Ultrasound 2014;43:68–70. [9] Chaudhry I, Bojal S, Poovathumkadavil A, Amr SS. Role of surgery after chemotherapy in B-cell lymphoma of thymus causing airway compression and right ventricle outflow tract obstruction. Ann Thorac Surg 2011;92:1120–2. [10] Byars TD, Dainis CM, Seltzer KL, Rantanen NW. Cranial thoracic masses in the horse: a sequel to pleuropneumonia. Equine Vet J 1991;23:22–4. [11] Wion L, Perkins G, Ainsworth DM, Dykes NL, Divers TJ. Use of computerised tomography to diagnose a Rhodococcus equi mediastinal abscess causing severe respiratory distress in a foal. Equine Vet J 2001;33:523–6. [12] Kondo H, Wickins SC, Conway JA, Mallicote MF, Sanchez LC, Agnew DW, et al. Cranial mediastinal liposarcoma in a horse. Vet Pathol 2012;49:1040–2. [13] De Clercq D, Van Loon G, Lefére L, Deprez P. Ultrasound-guided biopsy as a diagnostic aid in three horses with a cranial mediastinal lymphosarcoma. Vet Rec 2004;154:722–6. [14] Ohmura H, Hiraga A, Matsui H, Aida Y, Inoue A, Asai A, et al. Physiological responses of young Thoroughbreds during their first year of race training. Equine Vet J Suppl 2002;34:140–6. [15] Blissitt KJ, Bonagura JD. Pulsed wave Doppler echocardiography in normal horses. Equine Vet J Suppl 1995:38–46. [16] Gerber V, Straub R, Marti E, Hauptman J, Herholz C, King M, et al. Endoscopic scoring of mucus quantity and quality: observer and horse variance and relationship to inflammation, mucus viscoelasticity and volume. Equine Vet J 2004;36:576–82. [17] Marr CM, Reef VB. Physiological valvular regurgitation in clinically normal young racehorses: prevalence and two-dimensional colour flow Doppler echocardiographic characteristics. Equine Vet J Suppl 1995:56–62. [18] Blissitt KJ, Bonagura JD. Colour flow Doppler echocardiography in horses with cardiac murmurs. Equine Vet J Suppl 1995:82–5. [19] Young LB, Blunden AS, Bartram DH, Edgar A. Pulmonary atresia with an intact ventricular septum in a Thoroughbred foal. Equine Vet Educ 1997;9:123–7. [20] Gehlen H, Bubeck K, Stadler P. Pulmonary artery wedge pressure measurement in healthy warmblood horses and in warmblood horses with mitral valve insufficiencies of various degrees during standardised treadmill exercise. Res Vet Sci 2004;77:257–64. [21] Lightowler C, Guglielmini C, Pidal G, Chiaramonte P. Dopplerderived evidence of severe pulmonary arterial hypertension in a pony with recurrent airway obstruction. Vet Rec 2009;164:340–1. [22] Garber JL, Reef VB, Reimer JM. Sonographic findings in horses with mediastinal lymphosarcoma: 13 cases (1985-1992). J Am Vet Med Assoc 1994;205:1432–6. [23] Hilton H, Aleman M, Madigan J, Nieto J. Standing lateral thoracotomy in horses: indications, complications, and outcomes. Vet Surg 2010;39:847–55. [24] Ainsworth DM, Hollis N, Eicker SW, Yeagar AE, Viel L, Sweeney CR, et al. Effects of pulmonary abscesses on racing performance of horses treated at referral veterinary medical teaching hospitals: 45 cases (1985–1997). J Am Vet Med Assoc 2000;216:1282–6. [25] Timoney JF. The pathogenic equine streptococci. Vet Res 2004;35: 397–409. [26] Anzai T, Timoney JE, Kuwamoto Y, Wada R, Oikawa M, Higuchi T. Polymerase chain reaction-restriction fragment length polymorphism analysis of the SzP gene of Streptococcus zooepidemicus isolated from the respiratory tract of horses. Am J Vet Res 2002;63:1298–301. [27] Lindahl SB, Aspan A, Baverud V, Paillot R, Pringle J, Rash NL, et al. Outbreak of upper respiratory disease in horses caused by Streptococcus equi subsp. zooepidemicus ST-24. Vet Microbiol 2013;166:281–5. [28] Giuére S, Prescott JF, Dowling PM. In: Antimicrobial therapy in veterinary medicine. 5th ed. Ames, Iowa, USA: Wiley Blackwell; 2013.
Contents lists available at ScienceDirect
Journal of Equine Veterinary Science journal homepage: www.j-evs.com
Case Report
Acquired Pulmonic Stenosis Due to a Compressing Intrathoracic Abscess in a Thoroughbred Yearling Sigrid Hyldahl Laursen a, *, Gaby van Galen a, Godelind A. Wolf-Jäckel b, Rikke Buhl a a b
Department of Large Animal Sciences, University of Copenhagen, Taastrup, Denmark Department of Veterinary Disease Biology, University of Copenhagen, Frederiksberg, Denmark
a r t i c l e i n f o
a b s t r a c t
Article history: Received 10 December 2014 Received in revised form 23 March 2015 Accepted 11 June 2015 Available online 18 June 2015
A 12-month-old Thoroughbred filly was admitted for poor weight gain, intermittent fever, and distal limb edema. Initial clinical examination revealed tachycardia, tachypnea, and pyrexia. A loud holosystolic murmur was identified by cardiac auscultation, and thoracic auscultation identified bilateral diffuse crackles. Echocardiography demonstrated severe extrinsic pulmonic stenosis, enlargement of the right ventricle and compression of the left ventricle. Mediastinal ultrasound revealed a large, encapsulated, cavernous mass in the cranial thorax, compressing the heart. Bacterial culture of tracheal aspirates and aspirations of the intrathoracic mass yielded a pure culture of Streptococcus equi spp. zooepidemicus. Acquired pulmonic stenosis has not previously been reported in horses, whereas congenital pulmonic stenosis has. This case report demonstrates that in line with human medicine, pulmonic stenosis can be acquired because of thoracic masses compressing the pulmonic artery. Ó 2015 Elsevier Inc. All rights reserved.
Keywords: Pulmonic stenosis Pneumonia Streptococcus equi spp. zooepidemicus Intrathoracic abscess
1. Introduction Pulmonic stenosis is a rare finding in the horse, characterized by an increased resistance emptying the right ventricle that is caused by either intrinsic obstruction or extrinsic compression of the right ventricular outflow tract. This in turn causes hypertrophy of and increased pressure within the right ventricle and atrium. Severe stenosis will decrease the stroke volume of the heart and cause compensatory increased heart rates [1]. The condition in turn will thus lead to systemic circulatory changes causing exercise intolerance, weight loss, peripheral edema, and pulmonary edema [2]. Pulmonic stenosis has been described as a congenital disorder causing severe hypoxia in affected foals [3,4]. These congenital abnormalities are usually diagnosed early
* Corresponding author at: Sigrid Hyldahl Laursen, Department of Large Animal Sciences, University of Copenhagen, Højbakkegaard Alle 5, 2630 Taastrup, Denmark. E-mail address: [email protected] (S. Hyldahl Laursen). 0737-0806/$ – see front matter Ó 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jevs.2015.06.009
in life because of their severe clinical impact [4]. Only a single report describes an assumed congenital malformation of the pulmonic valves causing pulmonic stenosis in an adult horse [1]. Theoretically, pulmonic stenosis can also be acquired in the horse because of external compression. Extrinsic pulmonic stenosis due to cranial thoracic neoplasia has been described in the human literature [5–9]. Cranial thoracic abscesses may arise as a sequel to infections such as pneumonia, pulmonary abscesses, pericarditis, or pleuropneumonia and can result in cardiac compression depending on localization [10,11]. Multiple reports describe cranial thoracic masses including neoplasia and abscess formation in the horse, but to the authors’ knowledge, there are no reports of masses causing acquired pulmonic stenosis in the horse [12,13]. 2. Case History A 12-month-old Thoroughbred filly was referred to the Large Animal Teaching Hospital at the University of
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Copenhagen for evaluation of ill thrift and intermittent fever of 3- to 4-week duration. Before referral, a loud holosystolic murmur was noted as well as distal limb edema of the front limbs. Four weeks before admission, several yearlings in the same herd were noted to have respiratory symptoms including nasal discharge, fever, and cough. No prior diagnostic tests were performed on the facility to determine the cause of the infection. The horse never showed overt symptoms of airway disease and had not received antibiotic treatment before referral. 2.1. Initial Clinical Findings At the time of admission, the filly was bright and alert with a good appetite. The horse appeared unthrifty, with matted hair coat and a body condition score of 2/9. The initial clinical examination revealed an elevated heart rate (60 bpm) and rectal temperature (38.7 C). The filly presented with moderately elevated respiratory rate (20 rpm), a mild abdominal respiratory pattern, and bilateral mucopurulent nasal discharge. An intermittent productive cough was also noted, and coughing was easily provoked by compression of the larynx and trachea. The submandibular lymph nodes were normal on palpation. Thoracic auscultation identified diffuse crackles bilaterally. No rattling sounds were evident on tracheal auscultation. Moderate, pitting distal limb edema was noted on both front limbs. The filly appeared well hydrated, mucous membranes were pink and moist, and capillary refill time was within 2 seconds. Normal stasis and emptying of the jugular veins was noted, and on palpation of the facial artery, a strong pulse with normal rhythm was identified. Cardiac auscultation revealed a holosystolic murmur, grade 4/6 with point of maximal intensity over the pulmonic ostium. Persistent tachycardia was noted, but no arrhythmias could be identified on auscultation or subsequent base-apex electrocardiogram examination. 2.2. Initial Diagnostics Blood samples at the time of admission revealed mild anemia (packed cell volume: 27% [20%–41%]), severe neutrophilic leukocytosis (white blood cells: 20,980 cells/ mL [5,450–12,650 cells/mL], neutrophils: 14,920 cells/mL [2,260–7,220 cells/mL], lymphocytes: 4,240 cells/mL [1,260–5,740 cells/mL], monocytes: 1,280 cells/mL [0–1,000 cells/mL], eosinophils: 100 cells/mL [0–1,000 cells/mL], basophils: 120 cells/mL [0–290 cells/mL], hyperfibrinogenemia [fibrinogen: 7.76 g/L; 1–4 g/L]), and increased serum amyloid A (3265.4 mg/L [0–30 mg/L]), and decreased iron levels (5.99 mmol/L [13.1–25.1 mmol/L]). All these blood parameters indicate severe inflammation. Cranial thoracic ultrasound, through the triceps muscle, revealed a large, oval-shaped, cavernous, multiloculated mass measuring approximately 15 by 20 cm. The mass was surrounded by a hyperechoic capsule approximately 3 cm in thickness and was filled with slightly hyperechoic fluid material. The mass appeared to occupy the majority of the cranial thoracic space, exerting significant compression of the heart and in particular the
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pulmonary artery (Fig. 1). Thoracic ultrasound was suggestive of mild bilateral pleural inflammation (comet tails) and mild pneumonia. Echocardiography revealed severe enlargement of the right ventricle (luminal diameter) and compression of the left ventricle, with marked bulging of the interventricular septum into the left ventricle. Echocardiographic measurements are presented in Table 1. The right ventricular internal diameter at end diastole was increased, and the left ventricular internal diameter at end diastole demonstrated severe extrinsic volume restriction (Fig. 2). The pulmonary artery was severely compressed by the external mass. The diameter of the pulmonary artery obtained from the right parasternal angled view was severely reduced to 3.53 cm in systole and 1.74 cm in diastole (Fig. 3). Color Doppler examination identified no valvular regurgitation at the pulmonic, tricuspid, mitral, or aortic valves. Maximum pulmonary velocity was 2.3 m/s (reference values, 0.78–1.04 m/s [15]; Fig. 3). Minimal pericardial fluid was observed (Fig. 2). Endoscopy of the upper airways demonstrated moderate pharyngeal lymphoid hyperplasia (grade III/IV) and mucopurulent exudate in the trachea (grade III/IV) [16]. A subsequent transendoscopic tracheal aspirate through a nonguarded catheter using 30 mL of sterile saline demonstrated macroscopically visible mucopurulent secretions and contained 82% neutrophils, 7.5% macrophages, 1.5% lymphocytes, 0.5% eosinophils, and 8.5% epithelial cells, suggestive of pulmonary inflammation. Bacterial culture of tracheal aspirates and a direct ultrasound-guided aspirate of the intrathoracic mass yielded a pure culture of Streptococcus equi spp. zooepidemicus sensitive to penicillin. Thoracic radiographs demonstrated increased cranioventral radio density and diffusely increased bronchointerstitial pattern, suggestive of chronic bronchopneumonia. On radiographs, no mass could be visualized and they were not diagnostic in terms of distribution of the cranial thoracic mass. A blood culture obtained by strict aseptic technique via venipuncture of the left jugular vein yielded no bacterial growth.
Fig. 1. Cranial thoracic ultrasound: Left parasternal ultrasound view obtained at the third intercostal space, showing a large cavernous fluid-filled structure with a thick capsule occupying almost the entire cranial thorax.
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Table 1 Echocardiographic measurements of the case and reference ranges. Variable
Size (cm)
Reference Ranges (Thoroughbred Yearlings) [14]
IVSs IVSd LVIDs LVIDd LVFWs LVFWd RVIDd FS% Ao PADs PADd LA Ao/PADs
3.8 2.8 6.4 8.0 2.6 2.8 7.0 20% 4.8 3.5 1.74 9.0 1.4
3.01 1.93 7.12 10.40 2.94 2.22 d 21.1 4.34 d d 3.82 d
0.85 0.46 0.74 0.85 0.45 0.21
1.4 0.32
0.60
Abbreviations: Ao, aortic diameter at peak systole (cm); Ao/PADs, aortic diameter at peak systole (cm)/pulmonic artery diameter at peak systole (cm); FS%, fractional shortening (%); IVSd, interventricular septal thickness at end diastole (cm); IVSs, interventricular septal thickness at peak systole (cm); LA, left atrial diameter at end diastole (cm); LVFWd, left ventricular free wall at end diastole (cm); LVFWs, left ventricular free wall at peak systole (cm); LVIDd, left ventricular internal diameter at end diastole (cm); LVIDs, left ventricular internal diameter at peak systole (cm); PADd, pulmonic artery diameter at end diastole (cm); PADs, pulmonic arterial diameter at peak systole; RVIDd, right ventricular internal diameter at end diastole (cm).
3. Case Progression The filly was initially treated with 1.1 mg/kg of flunixin meglumine oral administration. Because of financial implications and guarded prognosis for recovery and future racing performance, the owner declined further treatment and the horse was euthanized. After euthanasia, a full necropsy was performed.
Fig. 3. Pulse-wave Doppler examination: Right parasternal angled long-axis view (right ventricular outflow view) with color pulse-wave Doppler. This view shows a maximum pulmonary velocity of 2.3 m/s due to severe compression of the pulmonary artery.
pericardium, which contained approximately 50-mL cloudy fluid. The epicardium showed multifocal hyperemia. Fibrous attachments were found between the abscess and the pleura overlying the sternum and the left cranial lung lobe (Fig. 5). This lung lobe was affected by chronic purulent bronchopneumonia. The myocardium and cardiac valves were macroscopically unremarkable and without lesions suggesting congenital pulmonary artery stenosis. Additional findings were related to parasitic infestation unrelated to the cardiopulmonary pathology: chronic, fibrinous, thrombosing endarteritis in the ileocolic artery and cyathostominosis affecting the cecum and colon. The remainder of the postmortem examination was unremarkable.
4. Postmortem Findings External inspection revealed bilateral mucopurulent nasal discharge. In the thoracic cavity, a mediastinal abscess was situated cranially to the heart. The abscess had an almost globose shape, measured 15 cm in diameter, and was encapsulated by approximately 3-cm-thick fibrous tissue (Fig. 4). The abscess was adherent to the cranial
Fig. 2. Echocardiography: Right parasternal long-axis view (four-chamber view) showing an enlargement of the right ventricle and bulging of the interventricular septum into the left ventricle. Left side of the image is ventral. LA, left atrium; LV, left ventricle; RV, right ventricle.
Fig. 4. Postmortem view of the incised cranial thoracic abscess: The abscess was located in the cranial thorax compressing the heart and pulmonary artery. The abscess contained large amounts of purulent material, and it was enclosed by an approximately 3-cm-thick fibrous capsule and was adhered to the pericardium. A, abscess; C, capsule; P, pericardium.
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Fig. 5. Cranial thoracic abscess in situ after dissection of the fibrous capsule from the pericardium: Dissection resulted in drainage of purulent material suggesting adherence of the abscess in part of the pericardium. The abscess was adherent to the pleura overlying the sternum and the left cranial lung lobe. A, abscess; LL, left lung; P, pericardium.
5. Discussion Murmurs associated with the right ventricular outflow tract are rare findings because of the physiologically low pressure within the pulmonary circulation. Systolic murmurs with point of maximal intensity over the pulmonic or aortic ostium may be physiological flow murmurs; however, echocardiographic examination is warranted to establish the exact cause of the murmur and severity of disease [17,18]. The loud systolic murmur associated with the right ventricular outflow tract in this case, in the absence of pulmonic valve abnormality, is most likely related to the stenosis of the pulmonary artery. Few reports in the literature describe pulmonic stenosis in horses. An exaggerated form of the tetralogy of Fallot with a congenital pulmonic stenosis has been described in conjunction with a ventricular septum defect and overriding of the aorta and right ventricular hypertrophy in three Arabian foals but may also occur in solitude [1,3,4,19]. These foals present early in life in cardiac failure and with loud murmurs [3]. These conditions usually carry a poor prognosis and are thus unexpected in older horses [3,4]. In addition, a single case report describes valvular pulmonic stenosis as an incidental finding in an adult Arabian horse with a grade 4/5 systolic murmur. In contrast to the congenital disorders in foals, the adult Arabian horse was clinically unaffected [1]. Echocardiography of the present case demonstrated severe extrinsic pulmonic compression, secondary enlargement of the right ventricular internal diameter, and compression of the left ventricle with marked bulging of the interventricular septum into the left ventricle. Pulse-wave Doppler examination demonstrated increased velocity of blood flow over the pulmonic valve, but as there was no tricuspid regurgitation, a pressure gradient was not calculated. Cardiac catheterization can be used for direct
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measurement of right ventricular pressure, and pulmonary artery catheterization can be used in cases where the origin of pulmonary hypertension is unclear. In cases of secondary pulmonic hypertension due to reduced left ventricular function, pulmonary artery wedge pressure will often equal left ventricular pressure. When pulmonary hypertension is caused by increased pulmonary vascular resistance, such as recurrent airway obstruction, pulmonary wedge pressure will be close to normal values [20,21]. In this case, we did not have the opportunity to perform cardiac catheterization, but pulse-wave Doppler demonstrated high pulmonary velocity with a characteristic dagger-shaped curve, suggestive of increased pressure due to pulmonic stenosis (Fig. 3). Furthermore, thoracic ultrasound showed an extrinsic pulmonic stenosis compressing the pulmonary valve area caused by a large abscess, and therefore, no further diagnostics were pursued. Although cranial thoracic masses have been described to compress the heart in horses [10], no previous reports discuss pulmonic stenosis as a result of extrinsic compression in the horse. Acquired (extrinsic) pulmonic stenosis caused by mediastinal neoplasia has been described in the human literature, and indeed, this case demonstrates that acquired pulmonary stenosis due to an extrinsic mass can also occur in the horse. The condition can be detected by thoracic ultrasonography along with Doppler echocardiography and in humans also by computerized tomography [5,6,10,11]. Computed tomography of the thorax is unfortunately of less use for horses because of size limitations, but it could potentially be performed in foals, small ponies, or donkeys. The present case demonstrates the value of the ultrasonographic view through the triceps muscle in visualizing masses in the cranial thorax. Mediastinal neoplasia in young horses, such as lymphosarcoma, may also present as cavernous encapsulated masses [22]. To differentiate abscess formation from neoplasia, ultrasound-guided aspiration for cytologic examination is essential [13,22]. In this case, the aspiration demonstrated a purulent material, and cytologic examination and bacterial culture confirmed the diagnosis of a mediastinal abscess due to streptococcal infection. Necropsy of the present case demonstrated chronic bronchopneumonia. Thoracic abscessation may arise secondary to trauma, pneumonia, pericarditis, or pleuropneumonia, and most likely, this filly developed a cranial thoracic abscess secondarily to pneumonia. Despite no prior history of respiratory disease, the clinical and necropsy findings were significant, and clinical signs possibly overlooked at the farm. Pathogens most frequently associated with intrathoracic masses in adult horses are Streptococcus spp., Actinobacillus spp., and Escherichia coli. [10,23,24], whereas Rhodococcus equi frequently may cause intrathoracic masses in foals and weanlings [11]. The S. equi spp. zooepidemicus isolated from this case was a Lancefield group C beta hemolytic streptococcus that is commonly isolated from the airways of horses. The organism is often described as an opportunistic pyogenic pathogen causing disease of the respiratory system and reproductive tract [25,26]. Although S. equi spp. zooepidemicus is a part of the normal flora of the respiratory tract in horses and may be considered less pathogenic and not contagious, a recent
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report has found pathogenic strains causing outbreaks of strangles-like symptoms [27]. Indeed, the present case indicates that numerous horses in the herd were infected and showing signs of respiratory disease and, in this case, severe complications, although no diagnostic tests were performed at the farm to identify the pathogen. It is thus possible that the initial outbreak of respiratory disease could have been caused by a viral agent such as Equine Herpes Virus or Equine Influenza and a secondary infection with S. equi spp. zooepidemicus in this particular case. The yearling was euthanized because of financial implications and guarded prognosis. However, medical treatment including prolonged broad-spectrum antimicrobial treatment has been proven effective in a number of reports of intrathoracic abscesses [10,11,24]. In this case, penicillin would be the drug of choice, although issues with regard to penetration of the thick fibrous capsule and large amount of purulent material within the abscess will affect treatment efficacy [28]. One report demonstrated a fair prognosis for racing after successful treatment of pulmonary abscesses although none of these cases presented with pulmonic stenosis [24]. Because of the severity of pulmonic compression and related cardiovascular compromise, surgical drainage followed by prolonged antimicrobial therapy could have been attempted to alleviate the pulmonary artery compression and resolve the infection [10,23]. Byars et al [10] described improvement after surgical drainage and lavage in three horses with cranial thoracic abscesses that were nonresponsive to medical treatment. Furthermore, a more recent study, including 16 horses, has also described standing thoracotomy for persistent thoracic abscesses related to pleuropneumonia with 88% survival and 46% return to previous level of performance [23]. Although these recent studies suggest that prognosis can be reasonably good after surgical drainage, the cranial localization of the abscess and adherences to the left lung and pericardium in the current case would most likely have complicated such an aggressive surgical approach. Moreover, there are no reports in the veterinary literature describing cardiac function after relieving right ventricular outflow tract compression. However, reports from human literature describe good outcomes with normalized cardiac parameters after medical or surgical removal of mediastinal neoplasms causing extrinsic pulmonic stenosis [7–9]. 6. Conclusions This case report shows that acquired pulmonic artery stenosis may arise secondary to thoracic abscessation. It can result in loud murmurs and cardiac compromise in the horse. Furthermore, it illustrates the possible severity of complications of S. equi spp. zooepidemicus infection. References [1] Gehlen H, Bubeck K, Stadler P. Valvular pulmonic stenosis with normal aortic root and intact ventricular and atrial septa in an Arabian horse. Equine Vet Educ 2001;13:286–8. [2] Davis JL, Gardner SY, Schwabenton B, Breuhaus BA. Congestive heart failure in horses: 14 cases (1984-2001). J Am Vet Med Assoc 2002; 220:1512–5.
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