Bilateral atrial thrombosis in an African hedgehog (Atelerix albiventris) with cardiomyopathy, endometrial hyperplasia, and left cystic ovary

Bilateral atrial thrombosis in an African hedgehog (Atelerix albiventris) with cardiomyopathy, endometrial hyperplasia, and left cystic ovary

ARTICLE IN PRESS Journal of Exotic Pet Medicine 000 (2019) 1 4 Contents lists available at ScienceDirect Journal of Exotic Pet Medicine journal home...

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Journal of Exotic Pet Medicine journal homepage: www.elsevier.com/locate/jepm

Diagnostic Challenge

Bilateral atrial thrombosis in an African hedgehog (Atelerix albiventris) with cardiomyopathy, endometrial hyperplasia, and left cystic ovary Enrique Yarto, MVZ, MSc a,*, Jorge Fajardo, MVZ. Esp a, Marycarmen Morales, MVZ a, Anneke Moresco, DVM, PhD b, Ixchel Arriaga, MVZ a, Alonso Reyes-Matute, MVZ, MMVZ c a b c

Centro Veterinario Mexico, Ciudad de Mexico, Mexico Denver Zoo, Denver, CO, USA Departamento de Patología Veterinaria, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autonoma de M exico, Ciudad de Mexico, Mexico

A R T I C L E

I N F O

Keywords: Hedgehog Atelerix albiventris Atrial thrombi Endometrial hyperplasia Ovarian cysts Dilated cardiomyopathy

A B S T R A C T

A 2-year-old female African pygmy hedgehog (Atelerix albiventris) presented to emergency for anorexia, lethargy and vulvar discharge. Tranquilization with midazolam, administration of oxygen therapy and facemask anesthesia with isoflurane were used for radiography study which showed increased radio-opacity and silhouette sign in the thoracic cavity. The patient underwent cardio-respiratory arrest during the performance of TFAST echocardiography. TFAST confirmed pleural effusion, a nodule in the chamber of the right atrium. Abdominal ultrasound revealed two fluid filled structures compatible with left ovarian cysts. Necropsy confirmed dilated cardiomyopathy, bilateral atrial thrombi, endometrial hyperplasia and two left ovarian cysts.

History A 2-year-old, 0.333 kg female African pygmy hedgehog (Atelerix albiventris) presented to the emergency service of Centro Veterinario Mexico (Mexico City, Mexico) with a 2-day history of anorexia, lethargy, and hemorrhagic vulvar discharge. The patient was fed an insectivore pelleted diet (Mazuri Insectivore Diet; Land OLakes Inc; Richmond, IN) and ad-libitum fresh water. The initial and prompt feasible physical examination revealed weakness, low body condition (2/5), hemorrhagic vulvar discharge. A firm, slightly bigger than 1 cm in diameter, rounded, smooth-surfaced structure was palpated mid-abdomen. Midazolam (Stern Pharma, JM Teresa 65, San Angel, 0100, Ciudad de Mexico; 0.25 mg/kg i.m.) was administered to reduce stress of handling and was followed by oxygen therapy via facemask for 10 minutes, which * Corresponding author. E-mail addresses: [email protected] (E. Yarto), [email protected] (J. Fajardo), [email protected] (M. Morales), [email protected] (A. Moresco), [email protected] (I. Arriaga), [email protected] (A. Reyes-Matute). Enrique Yarto: Clinical case attention; literature review; overall description of the case. Jorge Fajardo: Interpretation of imagenology (radiology and ultrasound). Marycarmen Morales: Performance of imagenology, literature review. Anneke Moresco: Literature review, edition, updates in reproductive diseases. Ixchel Arriaga: Clinical attention of the case and literature review on cardiology of hedgehogs. Alonso Reyes-Matute: Pathologist, pathology review and description of the case. https://doi.org/10.1053/j.jepm.2019.09.012 1557-5063/© 2019 Elsevier Inc. All rights reserved.

the patient tolerated well. Radiographs were taken under supplemental isoflurane anesthesia (2.5%, via facemask) and revealed a midabdominal radiolucent structure, displacing the stomach and colon cranially, consistent with a cyst on the reproductive system. Radiographs also showed an increase in radio-opacity and silhouette sign compatible with free fluid in the thoracic cavity. Therefore, it was decided to perform a TFAST (Thoracic Focused Assessment with Sonography for Trauma) echography. TFAST echocardiography confirmed pleural effusion; cardiac window images were obtained as part of the same study revealing a mixed-echogenicity, well-defined circular nodule in the chamber of the right atrium at the level of the atrioventricular junction, which was attached to the right atriums endocardial wall as well, compatible with a thrombus or neoplasia (Fig. 1A). This irregular structure occupying the whole right atrioventricular region was obstructing blood flow between the two chambers (Fig. 1B). Abdominal ultrasonography revealed two fluid-filled structures caudal to the stomach and left kidney, compatible with left ovarian cysts. Approximately 10 minutes after the starting of the ultrasound examination, the patient collapsed and went into cardiorespiratory arrest. Resuscitation efforts were immediately started but were unsuccessful and the patient died. Due to the collapse of the patient, it was not possible to perform a more detailed echocardiogram such as Doppler flux measurement, fractional shortening or other views, except for the fourchambered longitudinal view at the level of the base of the heart on the right parasternal window. Diagnosis Presumptive diagnosis based on ultrasound images were a cystic left ovary and dilated cardiomyopathy, with right atrial thrombus or

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Dissection of the heart revealed a marked biventricular dilation with apparent thickening of the ventricular walls, and both atria were completely occupied by thrombi. The thrombus in the right atrium laying on the tricuspid valve and being of considerable diameter and size enters the right ventricle as well (Fig. 2A). Lungs were congested and edematous. Histologically, both ventricular walls contained haphazardly arranged myocardial bundles, with multifocal fascicles of fibrous connective tissue. The cytoplasm of cardiomyocytes was multifocally fragmented and occasionally remarkably pale to slightly hyalinized, interpreted as degeneration of the cytoplasm. Enlargement of myocardial cells with coarse, clear cytoplasmic vacuoles and slightly enlarged, bizarrely shaped nuclei or multinucleated cells were present. Both atria were occluded by a laminated meshwork of pale eosinophilic fibrillar material adherent to the endothelium, occasionally characterized by ingrowth of endothelial cells, fibroblasts, and small capillary channels intermixed with numerous neutrophils; the latter is consistent with thrombus organization and recanalization (Fig. 3A to D). Lungs were moderately congested, and the alveoli were occupied by a moderate amount of proteinaceous fluid consistent with edema. On the reproductive tract, the left ovary showed two cysts (0.5 cm and 1.2 cm diam.). The cysts were lined by flattened epithelium and surrounded by smooth muscle and filled with copious amounts of yellowish translucent fluid (Fig. 2B). No other findings were identified in the rest of the parenchyma. No significant lesions were found on the right ovary. The endometrium was moderately thickened with an increase in the number of glands (endometrial hyperplasia). In the liver, random foci of bridging fibrosis were observed, with a notable hyperplasia of bile ducts, and a lympho-plasmacytic infiltrate. Differential diagnoses for the reproductive tract included: Ovarian cysts, ovarian tumors, endometrial hyperplasia, endometrial adenocarcinoma, endometritis, and pyometra. Discussion

Fig. 1. (A) Four-chambered longitudinal cut in the right parasternal window (Fig. 1) where a mixed-echogenicity structure in the right atrioventricular intrachamber region is seen. Point a well-defined hyperechoic circular nodule attached to the endocardial wall of the right atrium. (B) The arrow points to an irregular structure that occupies the whole atrioventricular region and obstructs blood flow between the right atrium and ventricle and is compatible with a thrombus. RV = right ventricle; M = mass; RA = right atrium; AVR = atrioventricular region; LA = left atrium; Mi = mitral valve; LV = left ventricle.

Although cardiovascular disease and endometrial hyperplasia are common findings in hedgehogs, this case is noteworthy because the patient presented at 2 years of age with both, in addition to presenting with bilateral atrial thrombi; the thrombus in the right atrium enters the ventricle as well. Even though atrial thrombi have been reported to occur spontaneously in other small mammals such as hamsters, this condition has not been explicitly described in the literature or studied in hedgehogs.1 Acquired cardiovascular disease in small exotic mammals is a common finding at necropsy, but antemortem diagnosis is infrequent since assessing the cardiovascular system can be a challenge in smallsized patients, and normal ranges are not available.1,2 Prevalence of dilated cardiomyopathy in African pygmy hedgehogs diagnosed during postmortem examination is almost 40%.3 African hedgehogs with

neoplasia. An atrial thrombus was confirmed at necropsy. Additionally, a second thrombus was found in the left atrium. Gross postmortem examination revealed ∼16 mL of serosanguinous fluid in the thoracic cavity. The heart was markedly enlarged and rounded; both left and right atria were severely increased in size and firm.

Fig. 2. (A) The heart shows marked cardiomegaly and a rounded shape, both atria are engorged. On cut surface (inset), severe biventricular dilation with complete obliteration of atria by thrombi can be seen. (B) Genital tract with two cysts arising from the left ovary filled with copious amounts of yellowish translucent fluid.

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Fig. 3. (A) Atrial thrombi, a laminated thrombus can be seen adhered to the atrial wall (arrows), H&E, 4×. (B) Laminations of the thrombi are prominent, H&E, 4×. (C) Different- sized blood vessels (arrows), were identified arising from the thrombi (recanalization), H&E, 40×. (D) Degeneration of cardiomyocytes, H&E, 40×.

disease, regular clinical re-checks under anesthesia that include radiographs, cardiac ultrasound, ECG, and abdominal ultrasound are recommended in hedgehogs starting at 2-year-old to facilitate early diagnosis. In hedgehogs of unknown cardiovascular status, careful clinical handling and anesthesia protocols for critical patients are suggested. Preventive medicine in hedgehogs in our private practice includes routine ovariohysterectomy at 6 months of age to prevent reproductive disease, and whenever possible cardiac evaluation. To the authors’ knowledge, this is the first published report of bilateral atrial thrombosis in a hedgehog with cardiomyopathy. This case was submitted by Enrique Yarto, MVZ, MC, Jorge Fajardo, MVZ. Esp, Marycarmen Morales, Anneke Moresco, DVM, PhD, Ixchel Arriaga MVZ, and Alonso Reyes-Matute, MVZ, MMVZ, from Centro Veterinario Mexico, Mexico City, Denver Zoo, and the Department of Pathology, Faculty of Veterinary Medicine, National Autonomous University of Mexico.

cardiovascular disease are reported to be 3 years of age or older, but occasionally as young as 1-year-old with higher prevalence in geriatric males than in females. Clinical signs may include dyspnea, lethargy, weight loss, dehydration, heart murmurs, moist rales, ascites, hydrothorax, pleural effusion, or acute death.1,2 This patient did not fit the typical signalment, as it was female and towards the younger side, and did not display the distinctive clinical signs, instead, the only presenting complaint was vulvar discharge. Literature on co-occurrence of cardiac and reproductive disease such as this case is sparse.4 Spontaneous atrial thrombosis has not been previously reported in African hedgehogs, but similar lesions occur in some colonies of aged Syrian hamsters (Mesocricetus auratus) along with consumption coagulopathy5 at present known as Disseminated Intravascular Coagulopathy (DIC). Thrombi are usually located in the left atrium, but some hamsters can present bilateral thrombi with bilateral ventricular hypertrophy with blood stasis secondary to cardiac failure as the primary hypothesis.5 According to the Virchows triad, blood stasis, endothelial injury and hypercoagulability are the main drivers to the formation of a thrombus. Endothelial injury is most frequently associated with left atrial dilation and endocardial changes. A dilated left atrium from underlying cardiac disease and complications with congestive heart failure are common drivers of blood stasis in humans and other animal species.6 Mortality due to the thromboembolism is very high in cats, and even with treatment most feline patients show low survival rates.7 Causes of hemorrhagic vaginal discharge and/or hematuria in hedgehogs include endometrial cysts and polyps,4 endometrial hyperplasia, uterine neoplasia, pregnancy loss, pyometra, and has even been reported in a case with granulosa cell tumor.8 Ovarian cysts are not uncommon in hedgehogs (Agnew D, pers. comm.) although not as frequently reported as in other species of small mammals, such as guinea pigs in which they are space-occupying masses leading to discomfort, gastrointestinal disturbances, hormonal alterations, chronic stress and abdominal pain.9 Early treatment of acquired cardiac disease in hedgehogs requires timely diagnosis of the cause/origin and extrapolations from small animal cardiology.1,2,10,11 Given the high prevalence of cardiac and reproductive

Supplementary materials Supplementary material associated with this article can be found in the online version at doi:10.1053/j.jepm.2019.09.012. References 1. Heatley JJ: Small exotic mammal cardiovascular disease. In: Proceedings of the 28th Association of Avian Veterinarians and the Association of Exotic Mammal Veterinarians Conference, pp 69–79, 2007 2. Schnellbacher R, Olson EE, Mayer J: Emergency presentations associated with cardiovascular disease in exotic herbivores. J Exot Pet Med 21:316–327, 2012 3. Raymond JT, Garner MM: Cardiomyopathy in captive African hedgehogs (Atelerix albiventris). J Vet Diagn Investig 12:468–472, 2000 4. Allison N: Clinical exposures-a hyperplastic endometrial polyp and vascular thrombosis in a hedgehog. Vet Med 98:298–303, 2003 5. McMartin DN: Spontaneous atrial thrombosis in aged Syrian hamsters. Thromb Haemost 38:0447–0456, 1977 6. Hogan DF: Treatment and Prevention of Feline Arterial Thromboembolism, in Little S (ed): August’s Consultations in Feline Internal Medicine. Vol. 7, Elsevier, pp 369–378, 2016 7. Borgeat K, Wright J, Garrod O, et al: Arterial thromboembolism in 250 cats in general practice: 2004 2012. J Vet Intern Med 28:102–108, 2014 3

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8. Wellehan JF, Southorn E, Smith DA, Taylor WM: Surgical removal of a mammary adenocarcinoma and a granulosa cell tumor in an African pygmy hedgehog. Can Vet J 44:235–237, 2003 9. Hocker SE, Eshar D, Wouda RM: Rodent oncology: diseases, diagnostics, and therapeutics. Vet Clin North Am Exotic Anim Pract 20:111–134, 2017

10. Powers LV, Brown SA: Basic Anatomy, Physiology and Husbandry, in Queensberry KE, Carpenter JW (eds): Ferrets, Rabbits and Rodents. Elsevier/Saunders, pp 411–427, 2012 11. Anderson RK, Gilmore CE, Schnelle GB: Utero-ovarian disorders associated with use of medroxyprogesterone in dogs. J Am Vet Med Assoc 146:1311–1316, 1965

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