CASE REPORT

Cardiac disease in the Spix Macaw (Cyanopsitta spixii): two cases

MPN de Carvalho,a* MPV Cunha,b T Knöbl,b CS Cirqueira,c RN Dias-Neto,d PP Serafini,e JL Cat~ao-Diasb and J Díaz-Delgadob,f

Cardiovascular disease in avian species, other than poultry, isbeing increasingly reported. In psittacine birds, atherosclerosisand congestive heart failure are the leading cardiovascular dis-eases, often resulting in multiorgan dysfunction and demise. TheSpix’s macaw (Cyanopsitta spixii) is arguably the most endangeredpsittacine species worldwide. We aimed to describe the gross andmicroscopic findings in two adult Spix’s macaws wherein severecardiovascular pathology resulted in sudden death. Bird 1 hadpathologic findings consistent with fibrinoheterophilic vegetativepulmonic valvular endocarditis with luminal obliterative thrombo-sis, myocarditis and epicarditis, myocardial fibrofatty infiltrationand cardiomyocyte loss, as well as generalized septicaemia.Microbiological analysis yielded Pantoea septica from the intes-tines and Acinetobacter baylyi from the cerebrum. Bird 2 hadchanges suggestive of right brachiocephalic coarctation-like oblit-erative arteriopathy. The latter is a novel cardiovascular pathologyin avian species, and its severity and extent likely led to acutedecompensation of pre-existing cardiac disease. These results addto the body of knowledge on avian cardiovascular pathology andmay aid in veterinary medical decisions on caged birds, includingthose part of ex situ conservation efforts.

Keywords avian pathology; cardiovascular disease; coarctation;obliterative arteriopathy

Abbreviations CHD, congenital heart disease; CHF, congestiveheart failure; CoA, coarctation of the aortaAust Vet J 2021 doi: 10.1111/avj.13097

Cardiovascular disease is common in caged birds.1 Athero-sclerosis and congestive heart failure (CHF), which oftenresult in multiorgan dysfunction and death, are the leading

reported cardiovascular diseases in psittacine birds (order Psittaci-formes).1–4 Atherosclerosis is particularly prevalent in aged andfemale birds of genera Psittacus, Amazona and Nymphicus.5 The

brachiocephalic trunks and ascending aorta are typically mostseverely affected.5,6 Primary myocardial, great vessel and coronarydisease are common causes of CHF, whereas secondary myocardialdisease and pericardial disease are less prevalent.1,3 CHF due to car-diomyopathy of unknown aetiology was described in young greyparrots (Psittacus erithacus).7

The Spix’s macaw (Cyanopsitta spixii) is regarded as the mostendangered psittacine species in the world, primarily due to capturefor illegal trade, and is considered to have become extinct in the wildsince 2000.8 Captive breeding and reintroduction to its natural habi-tat is deemed the last hope for the species.9 Therefore, an ambitious,multidisciplinary Action Plan for the Conservation of the Spix’sMacaw with international collaborations and an active involvementof the local community was established and led by The ChicoMendes Institute for the Conservation of Biodiversity (ICMBio)since 2013. Successful captive breeding correlates with medicalknowledge of the species. Nonetheless, there is a paucity of informa-tion in the literature on the causes of morbidity and mortality incaptive Spix’s macaws. Herein, we describe the gross and micro-scopic findings in two adults male Spix’s macaws wherein severe car-diovascular pathology resulted in sudden death.

Medical histories

Bird 1 was a 244 g (normal weight range: 288–318 g), approximately40-year-old (life expectancy in the wild: 20–30 years), male Spix’smacaw in emaciated body condition that was found dead in the cage.The clinical history did not indicate cardiomyopathy. Bird 2 was a330 g, 27-year-old male Spix’s macaw in moderate body conditionthat had been historically diagnosed with cardiomyopathy and wasbeing treated with enalapril (0.16 mg/kg/48 h). The bird was founddead in the cage. The birds were housed in different facilities, anddeath occurred approximately 1 year apart. The diet of both birdsconsisted of extruded feed for parrots, fresh fruits (guava, banana,papaya, orange, apple), vegetables (broccoli, carrot, green peas) andsome nuts. The facilities housed other parrots’ species, but withoutdirect contact with the Spix’s macaws. The birds were not related.Both birds were submitted for postmortem examinations between2 and 5 h after the animals were found dead.

Case report 1A standard necropsy was performed and selected tissues were col-lected (trachea, thyroid, oesophagus, crop, lungs, pro-ventricle, ven-tricle, skin, skeletal muscle, heart, liver, intestines, kidneys, spleenand pancreas) and fixed in 10% neutral buffered formalin. Thetissues were trimmed, routinely processed and embedded inparaffin-wax. Thin tissue sections (5 μm) were cut and stained with

*Corresponding author.aDepartamento de Clínica e Cirurgia Veterin�arias, Escola de Veterin�aria, UniversidadeFederal de Minas Gerais, Av. Pres. Antônio Carlos, 6627 - S~ao Luiz, Belo Horizonte,MG, 31270-901, Brazil; marcelopnc@yahoo.com.brbDepartment of Pathology, School of Veterinary Medicine and Animal Science,University of S~ao Paulo, Av. Prof. Dr. Orlando Marques de Paiva, 87 - Butant~a, S~aoPaulo, SP, 05508-270, BrazilcNúcleo de Anatomia Patol�ogica, Centro de Patologia, Instituto Adolfo Lutz, Av. Dr.Arnaldo, 355 - Pacaembu, Pacaembú, SP, 01246-000, BrazildJardim Zool�ogico do Rio, Parque da Quinta da Boa Vista S/N, Rio de Janeiro, RJ,20940-040, BrazileCentro Nacional de Pesquisa e Conservaç~ao de Aves Silvestres – CEMAVE, InstitutoChico Mendes de Conservaç~ao da Biodiversidade – ICMBio/MMA, Rodovia MaurícioSirotski Sobrinho s/n - Trevo Jurerê, Florian�opolis, SC, 88053-700, BrazilfTexas A&M Veterinary Medical Diagnostic Laboratory, College Station, Texas,77843, USA

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haematoxylin and eosin. Brachiocephalic arteries were additionallystained by Masson’s trichrome (for collagen) and Verhoeff (for elas-tin) techniques. For immunohistochemistry, 3 μm sections of right(rBa) and left (lBa) brachiocephalic arteries were incubated with pri-mary antibodies specific for smooth muscle actin (monoclonal 1A4;1 in 1000 dilution; Thermo Scientific Lab Vision; Rockford, IL, USA),vimentin (monoclonal V9; 1 in 3000 dilution; Dako, Carpinteria, CA,USA) and desmin (monoclonal D33; 1 in 3000 dilution; Dako).Antigen–antibody binding was detected by UltraVisionTM LP Detec-tion System HRP Polymer (Thermo Scientific Lab Vision) and ‘visual-ized’ by use of 3, 30 diaminobenzidine chromogen (Sigma D5637, StLouis, MO, USA). Positive control tissues included Spix’s macawbrachiocephalic artery and human appendix. As negative controls, pri-mary antibodies were replaced by homologous non-immune serum.

Cerebrum, intestines, kidneys and cardiac blood were sampled forbacteriological analysis and cultured for 24 h under aerobic andanaerobic conditions at 37�C. Identification of isolates was per-formed by matrix-assisted laser desorption ionization-time of flightmass spectrometry (MALDI-TOF MS).

On necropsy, this bird had cardiomegaly with multifocal, poorlydemarcated, transmural, pale foci throughout the ventricles, atriaand auricles (Figure 1). Microscopically, there was fibrino-heterophilic vegetative pulmonic valvular endocarditis (Figure 2)with necrosis and luminal obliterative thrombosis, myocarditis andepicarditis. Myocardial fibrofatty infiltration and cardiomyocyte losswere also noted. Additional relevant findings indicated septicaemiaand included: necroheterophilic tubulointerstitial nephritis, ureteritisand polymyositis; hepatic necrosis; pulmonary congestion, oedema

and haemorrhage; and coelomic and abdominal air sac haemorrhage.Microbiological analysis yielded Acinetobacter baylyi (+; puregrowth) in the cerebrum and Pantoea septica (++; polybacterialgrowth) in the intestines. No bacterial growth was observed from thekidneys and cardiac blood samples.

Case report 2A standard necropsy was performed and selected tissues were col-lected as described for bird 1. In bird 2, spanning from the aorticvalve to the right brachiocephalic artery (rBa), there was an 8 mm-long segmental aneurysmal dilatation (up to 3.5 mm in diameter; theunaffected left Ba was up to 2.5 mm in diameter). A 4 � 2 � 2 mmobliterative intraluminal mass was located at 3 mm from the aorticvalve. Distal to this segment, the arterial lumen was markedlyreduced to 1–2 mm in diameter and had transmural haemorrhage(Figure 3). The rBa wall was up to 0.6 mm thick at the coarctation(obliteration, abrupt narrowing of the lumen) point while the left Bawas up to 0.3 mm thick at the same segment level. The intimal andadventitial surfaces at the aneurysmal segment were pale tan to whiteand smooth. The heart was diffusely enlarged with dilated ventriclesand atria. On cut section, the free walls were subjectively thickenedand flaccid (hypertrophic eccentric cardiomyopathy). Diffusely, thecardiac walls were brown with multifocal, poorly demarcated, paletan foci. Additional gross findings consisted of chronic hepatopathyand pulmonary congestion with emphysema.

Microscopically, the rBa had a focal intraluminal mass arising fromthe interface of the subintima and tunica media that led to completearterial stenosis (Figures 4 and 5). The mass was composed of denselypacked 1A4- and vimentin-positive myofibroblasts admixed withabundant dense collagen (blue with Masson’s trichrome stain) bun-dles arranged perpendicular to bloodstream (Figure 5). No elastinfibres were detected. Neither recanalization nor hemosiderophages

Figure 1. The heart of a Spix’s macaw that died of septicaemia. Frontalview of the heart (ex situ). There are multifocal, poorly demarcated, paletan foci in the myocardium of the right and left ventricles. Bar, 1 cm.Inset: Detail of pale tan myocardial foci in the left ventricle. Bar, 0.5 cm.Ao, aorta; Lba, left brachiocephalic artery; lv, left ventricle; Rba, rightbrachiocephalic artery; Rv, right ventricle.

Figure 2. Pulmonary valve of a Spix’s macaw that died of septicaemia.The pulmonary valve is expanded and distorted by inflammatory infil-trates (arrowheads) that extend into the adjacent myocardium and baseof the pulmonary trunk (asterisk). Inset: Detail of mixed, mainlyheterophilic, inflammatory exudate with fibrin, oedema and necroticcellular debris in the pulmonary valve.

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were observed. Distal to this segment, the rBa had transmural necro-sis and haemorrhage; this finding was interpreted as an area of infarc-tion. In the heart, there were scattered foci of myocardial fibrosisassociated with cardiomyocyte atrophy and loss, mild myofiber disar-ray, hypertrophic cardiomyocytes, focal fibrofatty infiltration, lipofus-cinosis, congestion, interstitial oedema and rare haemorrhage.Additional relevant microscopic findings associated with pulmonaryand systemic hypertension were as follows: pulmonary haemorrhageassociated with focal arterial rhexis (Figure 6), oedema and conges-tion; intrapulmonary arterial smooth muscle hypertrophy/hyperpla-sia; chronic glomerulopathy with fibrosis and sclerosis; and renalarterial tunica media hypertrophy/hyperplasia. Based on these find-ings, a diagnosis of rBa coarctation-like obliterative arteriopathy andacute decompensation of pre-existing cardiac disease was determined.

Discussion

We have presented two cases of severe cardiovascular disease withsignificant pathology in two Spix’s macaws. Bacterial infection of theheart can result in endocarditis, including valvular endocarditis,myocarditis or epicarditis, and may be the result of haematogenousspread of infection or direct extension from adjacent tissues. In petand aviary birds, valvular endocarditis is relatively rare, and the leftvalve is chiefly affected.2,8 The most common agents are streptococci,staphylococci, Pasteurella multocida and Escherichia coli.3,10 InBird 1, we found fibrinoheterophilic pulmonic valvular endocarditis,myocarditis and epicarditis together with septicaemia-associatedlesions. Although we did not find an obvious route of entry in thiscase, we propose that vegetative endocarditis and myocarditis mayhave led to cardiac failure, resulting in a clinicopathological picturethat was further aggravated by septicaemia.

In Bird 1, P. septica and A. baylyi were isolated from the intestinesand cerebrum, respectively. The genus Pantoea encompasses adiverse group of widely distributed environmental Gram-negativebacilli (Enterobacteriaceae) that are commonly isolated from plants,insects and nonmammalian and mammalian species, includinghumans.11 Pantoea spp. are typically regarded as environmental con-taminants or are associated with opportunistic or nosocomial infec-tions in humans and animals.12 Currently, there is much debate asto the pathogenicity of this genus in animals. Several Pantoea spe-cies, including P. septica, have been routinely isolated from clinicalsamples of diseased and nondiseased patients who are immunocom-petent or immunocompromised.12 Many disease processes, includingsepticaemia, have been ascribed to various Pantoea spp.; however,direct causation for most of these cases has not been demonstrated.12

Furthermore, P. septica has been isolated from presumably healthysaffron finches (Sicalis flaveola) from S~ao Paulo state, Brazil.13 Tothe best of our knowledge, there are no reports of P. septica isolatedfrom diseased avian species or any healthy or diseased Spix’smacaws. A. baylyi is a nonfermentative environmental Gram-negative bacillus that is frequently isolated from soil. Nonetheless, acase series reported this bacterium as responsible for nosocomialinfection in immunocompromised humans.14 To the best of ourknowledge, A. baylyi has not been reported in animals. Taken theseconsiderations into account, the pathological relevance of P. septicais uncertain and the possibility of environmental contamination or

Figure 3. The heart of a Spix’s macaw that died of heart failure associ-ated with right brachiocephalic coarctation-like (obstructive)arteriopathy. Frontal view of dissected dorsal coelomic (thoracic) cavity(in situ). The right brachiocephalic artery has a focal proximal segmen-tal aneurysm (arrow) and a distal infarcted and haemorrhagic narrowedsegment (circled area). There is also focal chronic epicarditis with fibro-sis at the left ventricle apex (asterisk). Bar, 1 cm. La, left auricle; Lba, leftbrachiocephalic artery; lv, left ventricle; Ra, right auricle; Rba, rightbrachiocephalic artery; Rv, right ventricle.

Figure 4. The heart of a Spix’s macaw that died of heart failure associ-ated with right brachiocephalic (obstructive) arteriopathy. The lumen isoccluded by a mass (arrowheads) composed of myofibroblasts and col-lagen bundles arranged perpendicular to bloodstream that focally mer-ges with the overlying intima, subintima and tunica media. There isadventitial haemorrhage (asterisk).

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opportunistic outgrowth from normal intestinal microbiota cannotbe excluded. Analogously, the pathogenic significance of A. baylyi inthis case remains elusive. Overall, Enterobacteriaceae and non-fermentative Gram-negative bacteria are not part of the microbiotaof free living psittacine birds, they are often a consequence ofcaptivity.15

Congenital heart disease (CHD) in avian species, other than poultry,is rarely described.16 The main CHD conditions reported in psitta-cine birds include ventricular septal defects and congenital aneu-rysms, mainly in cockatoos (Cacatuidae), cockatiels (Nymphicushollandicus) and African grey parrots.2,7 Abnormal narrowing of car-diac chambers, heart valves or blood vessels lead to forms of CHDthat result from obstruction to blood flow. Among them, coarctation

of the aorta (CoA) consists of an abrupt narrowing of the lumen ofthe aorta due to the projection of a shelf-like curtain of aortic medialtissue from the superioposterior wall into the aortic lumen adjacentto the ductus or ligamentum arteriosum.17 Coarctation has been his-torically used interchangeably with hypoplasia and aplasia, however,they are dissimilar. Hypoplasia defines an arrested developmentleading to smaller size or immature state of development of the arte-rial segment. Aplasia, so-called ‘atresia’, denotes absence of the arte-rial segment. Therefore, hypoplasia and aplasia have divergingpathogeneses and/or genetic bases, which primarily involve intracar-diac/aortic blood flow defects, and lack a shelf-like projection of thearterial medial components into the lumen.11,17 In case 2, the rBapresented a focal intraluminal mass composed of myofibroblasts andcollagen bundles, which were perpendicularly oriented to the

Figure 5. The heart of a Spix’s macaw that died of heart failure associated with right brachiocephalic (obstructive) arteriopathy. (A) Close-up viewof squared area in Figure 4 with intraluminal myofibroblastic and collagenous mass (arrowhead). The mass merges with the adjacent subintima/tunica media interface (asterisks). Haemorrhage is indicated with an arrow. (B) The rBa intraluminal mass (arrowhead) is composed of 1A4- (leftinset) and vimentin-positive myofibroblasts (right inset). Immunohistochemistry. (C) The rBa intraluminal mass (arrowhead) is composed of abun-dant dense collagen (blue). Masson’s trichrome. (D) The rBa intraluminal mass (arrowhead) lacks elastin fibres. Verhoeff stain. Inset: Close-up viewof squared area in D. Lu, lumen.

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bloodstream, that merged with the overlying intima, subintima andtunica media and led to complete arterial stenosis. These featuresresembled CoA.18,19 We observed additional findings associated withsystemic hypertension likely as a result of rBa coarctation-likearteriopathy.

Although CoA is well-known in humans, this condition is very rarein animals, being only reported in few dogs.19,20 Its pathogenesis isnot fully understood, but it is known that CoA results from abnormaldevelopment of the embryologic left fourth and sixth aortic arches.18

Often, CoA is associated with other CHD (e.g. bicuspid aortic valve,persistent ductus arteriosus, atrial and ventricular septal defects), aor-tic stenosis and other disease processes (e.g. Turner syndrome andberry aneurisms of the circle of Willis).18 We do not know whetherthis bird was born with such defect and evolved over time or whetherthis represents a secondary phenomenon, as CoA-like reported inhumans subsequent to traumatic events.21,22 The lack of early diag-nostic imaging data and the fact that the animal died at an advancedage render a congenital condition difficult to prove definitively in thiscase, however, the absence of recanalization, hemosiderophages, vary-ing degrees of myofibroblastic disarray or any evident pre-existingpredisposing disease process for chronic thrombotic event, lends sup-port to a diagnosis of rBa coarctation-like arteriopathy.11,18 Further-more, CoA is not invariably fatal and human patients may live for anumber of years after diagnosis. If uncorrected, most human patientswith CoA die before the age of 40 years from heart failure byincreased resistance to the ejection of blood (afterload CHF), rup-tured aorta or cerebral vessel, or infective endocarditis.23

Conclusion

To the authors’ knowledge, this is the first report of spontaneous rBaobliterative arteriopathy in avian species that recapitulates features

of CoA. Neither bird presented gross or microscopic evidence of ath-erosclerosis. In conclusion, these cases add to the body of knowledgeof cardiovascular pathology in avian species and may aid in medicaldecisions on captive avian collections, including those part of ex situconservation efforts, and may prove of value for further comparativepathological analysis.

Acknowledgments

JDD is the recipient of a postdoctoral fellowship by the S~ao PauloResearch Foundation (FAPESP; grant #2017/02223-8). JLCD is therecipient of research fellowship from the CNPq (grant # 304999/2018-0).

Conflicts of interest and sources of funding

The authors declare no conflicts of interest or sources of funding forthe work presented here.

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Figure 6. The lung of a Spix’s macaw that died of heart failure associ-ated with right brachiocephalic (obstructive) arteriopathy. There issevere intrapulmonary haemorrhage due to vascular rhexis. The edgesat multiple vascular rupture sites are indicated by asterisks.

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(Accepted for publication 22 May 2021)

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