Postmortem Diagnostic Imaging to Evaluate Idiopathic Hypertrophic Cardiomyopathy in a Roborovski Hamster

1. Case History
Abreeder brought the cadaver of a 6-month-old male Roborovski dwarf hamster to the Veterinary Clinic of the University of Tehran after its abrupt death and upon the serial death of its brothers and sisters. 

2. Clinical Presentations
The case had clinical symptoms of respiratory disorders and received antibiotic therapy without significant improvement.

3. Diagnostic Testing
Postmortem computed tomography, digital radiography, and echocardiography were performed almost 3 hours after death. The cadaver had a moderate rigor-mortise, and during these 3 hours, it had been kept in a cold and dry bag. In this study, we aimed to uncover the cause of death of this hamster by virtopsy.
Radiography
 Standard whole-body orthogonal left lateral and dorsoventral radiographs were performed on the cadaver. Wet hair artifact was visible around the body. Because of the rigor mortis, the forelimbs were superimposed in the cranial thorax, and the hindlimbs were not extended, resulting in compression in the abdominal cavity. Marked focal soft tissue swelling associated with gas inclusions was detected around the cervical region, possibly resulting from postmortem changes. There are two small tubular structures with mineral opacity in the cranioventral aspect of the abdominal cavity on both sides of the spine, which may be related to gastrointestinal contents. No skeletal abnormalities and the dental arcade were detected. However, the thoracic cardiac silhouette was not well delineated due to increased lung opacity caused by postmortem atelectasis. Postmortem changes comprised gas accumulation within the gastrointestinal tract (Figure 1).

Computed tomography
A native CT scan was performed (using Siemens SOMATOM® 2 detector scanner), and the images were reconstructed in orthogonal views. The heart’s maximum height, width, and length were 7.5, 5.5, and 8.5 mm, respectively (Figure 2).

Two tubular heterogeneous mineral attenuating (HU=1000) structures were visible in the center of the abdomen in the intestinal segments that are dense intestinal contents; otherwise, the skeletal structures, thorax, and abdomen were within the normal range (Figure 3). The ratio of the heart diameter to the thoracic diameter was 8.47 mm/12.7 mm.

Echocardiography
 Echocardiography was performed with a Vivid 7 ultrasonography machine (GE Medical Systems, USA), connected to a multi-frequency (6-13 MHz) phased-array transducer. In the right parasternal long-axis study, the collapsed lumen of the heart could be detected by linear intraluminal hyperechogenicity. The thickness of the left ventricular parietal septum was 2.796 mm, and the thickness of the interventricular septum was 2.748 mm. The left atrium was also dilated, probably due to mitral valve regurgitation, but since we could not use color Doppler or pulse wave, we cannot say it with certainty (Figure 4).

 
All the images were then reviewed and edited by Horos software, version 3.3.6. 
Necropsy was performed. Macroscopically, left ventricular hypertrophy was observed (Figure 5). Lungs and other organs exhibited normal appearance.

4. Assessments
In this research, we studied idiopathic cardiomyopathy in a deceased hamster by postmortem echocardiography. To the best of our knowledge, this is the first report of forensic echocardiography in a veterinary practice and may open a new door into further postmortem echocardiographic investigations.
Virtual autopsy (virtopsy) is a novel approach in the veterinary necropsy procedure that uses different imaging modalities, namely radiography, computed tomography, magnetic resonance imaging, and ultrasonography, to aid postmortem evaluations. Since virtopsy aims to analyze images and add value to forensic medicine, its application can assist with the pre-autopsy diagnosis (Parry & Stoll, 2020; Thali et al., 2009). Although conventional necropsy is extensively employed to determine the cause of death in veterinary practices, minimally invasive postmortem imaging, which is more economical and has more precise results, can be a proper substitution for aggressive methods. In veterinary postmortem examinations, the smaller the animal is, the more we rely on histopathology than necropsy to spot lesions (McDonough & Southard, 2017). 

Even though thoracic radiography and CT scan are helpful in the determination of cardiac diseases in exotic animals‎ (Krautwald et al., 2010), they are inappropriate for postmortem inspection of the heart due to alveolar atelectasis which negatively affects the imaging contrast, compared to echocardiography. Postmortem echocardiography has been performed on the human heart as another diagnostic modality to autopsy to reveal a specific cause of death in infants to increase the diagnostic yield of the autopsy (Ker et al., 2010) and to assess the chamber size and left ventricular wall thickness (Chon et al., 2017). Likewise, echocardiography is the method of choice in dogs and cats for diagnosing cardiac malfunction and cardiac geometry in exotic companion mammals or animal models (Mitchell  & Tully, 2016; Babaei & Razmaraii, 2020). However, considering the advantage of the postmortem echocardiography and based on the normal cardiac size of Syrian hamsters (which is 0.1±0.01 cm for posterior wall thickness [PWT] and 0.1±0.01 cm for interventricular septal thickness [IVST]), we made a diagnosis of idiopathic cardiomyopathy in the deceased hamster (Salemi et al., 2005). Hamsters with heart disease show various clinical signs, including pulmonary manifestations, lethargy, and edema. Some may be very mild and take a long time to be diagnosed (Soroori et al., 2020). Some common heart diseases affecting geriatric hamsters are dilative cardiomyopathy and atherosclerosis, which can contribute to atrial thrombosis (Keeble & Meredith, 2009). Hypertrophic cardiomyopathy is less prevalent (Kubiak, 2020; Dutton, 2020). There is little information about the Roborovski hamster breed, and most of the studies are based on Syrian hamsters because they are more popular as pets and laboratory animals (Keeble & Meredith, 2009). 
Hypertrophic cardiomyopathy is a heart disease associated with an abnormal ventricular wall and interventricular septum thickening with normal or diminished left ventricular dimensions. Hypertrophic cardiomyopathy is prevalent most commonly among feline and affects 10%-15% of them compared to other animal species (Freeman et al., 2017; Simpson et al., 2017). Cardiomyopathy (both dilative and hypertrophic) in Syrian hamsters is an autosomal recessive disease with a phenotypic expression in 100% of the affected line (Factor et al., 1988). Notably, over 90% of hamsters with hypertrophic cardiomyopathy die of premature congestive heart failure (Factor et al., 1988; Strobeck et al., 1979).
The limitation of this report is lacking histopathology and a control postmortem study on a hamster with a normal heart of the same age. However, this unique case report can be a start for using postmortem echocardiography in small animals.
Conclusion
In conclusion, postmortem echocardiography in postmortem hamsters is a non-invasive and quick method to evaluate possible heart diseases like cardiomyopathies.

Ethical Considerations

Compliance with ethical guidelines
There were no ethical considerations to be considered in this research.

Funding
This research did not receive any grant from funding agencies in the public, commercial, or non-profit sectors.

Authors' contributions
All authors equally contributed to preparing this article.

Conflict of interest
The authors declared no conflict of interest.

Acknowledgments
The authors express their appreciation to everyone that assists us in this study.

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