Myocardial degeneration in Russian rat snake (Elaphe schrenckii)

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Korean J Vet Serv, 2018, 41(3), 217-220 ISSN 1225-6552, eISSN 2287-7630 https://doi.org/10.7853/kjvs.2018.41.3.217

< Case Report >

Korean Journal of

Veterinary Service

Available online at http://kjves.org

*Corresponding author: Yeonsu Oh, Tel. +82-33-250-8792, Fax. +82-33-259-5625, E-mail. [email protected] The first two authors contributed equally to this work.

Myocardial degeneration in Russian rat snake (Elaphe schrenckii)

Shraddha Tiwari¹, Sulhi Aufa¹, Hyung-Hun Park¹, Ho-Seong Cho², Byung-Yong Park³, Yeonsu Oh¹*

1Department of Veterinary Pathology, Collage of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University, Chuncheon 24341, Korea

2College of Veterinary Medicine and Veterinary Diagnostic Center, ³College of Veterinary Medicine and Bio-safety Research Institute, Chonbuk National University, Iksan 54596, Korea

(Received 10 June 2018; revised 13 September 2018; accepted 16 September 2018)

Abstract

A female Russian rat snake, Elaphe schrenckii, was presented for loss of movement. Physical examina- tion showed the swelling in the area of heart. Radiographic examination revealed cardiomegaly, pericardial effusion, and a soft opacity in the area of swelling. Although pericardiocentesis to remove fluid out from the heart as well as vigorous treatments were given to the Russian rat snake, it died during treatments. Postmortem examination confirmed pericardial effusion of pale yellow, translucent ﬂuid with mild dilation of the right atrium and ventricle. Formalin -fixed paraffin embedded tissue sections were stained with routine H&E and the classical von Kossa's method for histopathological demonstration.

Histopathological examination revealed multifocal calcification in myocardium and consists of the displacement of muscular fiber by limy deposits. Congestive heart failure was suspicious for the snake when it was alive. In wild reptiles, muscle degeneration has been reported with nutrition disorders but the present case is the first report of myocardial degeneration in a Russian rat snake and contributes to the rare reports of cardiac disease in snakes.

Key words : Calcification, Myocardial degeneration, Elaphe schrenckii, Radiographic, Russian rat snake

INTRODUCTION

Heart disease in reptiles is a group of pathological entities that remains uncommonly diagnosed, and most available information about cardiovascular disease is based on necropsy examination findings (Kik and Mitchell, 2005). Given that cardiac structure of snakes is quite different from mammals, it is important to be fully aware of the normal anatomy and physiology of reptiles prior to surgery or postmortem examination (Farrell et al, 1998; Girling and Hynes, 2004; Murray, 2006;

Starck, 2009; Wyneken, 2009; Jensen et al, 2010a;

Jensen et al, 2010b). Cardiac disease is only rarely reported in snakes and other reptiles (Schroff et al, 2010) and includes both primary (idiopathic cardiomyopathy, congenital defects, degenerative disease) and secondary (metabolic and nutritional) disorders (Schroff et al, 2010). Clinical signs are often nonspecific and include generalized weakness, anorexia, weight loss, skin dis- coloration, swelling of the cardiac area, edema, ascites, cyanosis, ecchymosis, and sudden death (Murray, 2006).

CASE

A pregnant Russian rat snake (Elaphe schrencki) of unknown age which presented a pronounced enlarge-

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218 Shraddha Tiwari, Sulhi Aufa, Hyung-Hun Park, Ho-Seong Cho, Byung-Yong Park, Yeonsu Oh

Korean J Vet Serv, 2018, Vol. 41, No. 3

A B

Fig. 1.Russian rat snake (Elaphe schrencki). A. Pronounced en- largement of the cardiac region. B.

Cardiomegaly, Radiography.

ment of the cardiac region and inability for physical movement, was rescued to the Kangwon National University Veterinary Teaching Hospital in a winter season. The full radiography confirmed extensive pericardial effusion (Data not shown), and serosanguinous fluid was collected through the ultrasonography-guided pericardiocentesis. Multiple trials of antibiotic treatments and supplemental therapy did not improve the general condition. The mother snake gave birth to six eggs and died during the treatment, and a postmortem examination followed.

The abdominal organs did not seem to be affected by any infection or sepsis, rather shrunken due to malnutrition, but it was not surprising that the animal was in hibernation. However, when it was rescued, it was seen outside with cardiac region enlargement and all of six neonates presented the same symptom with their mother.

The five neonates were dead five hours after being hatched. The one remaining neonate, 65 cm in length and 55 g in weight, was lethargic, thin and weak, and also presented cardiac region enlargement just like its mother (Fig. 1A). Treatments for the young snake were given for suspected trans-shell infective carditis, starting with ceftazidime, 10 mg/kg (Fortum^Ⓡ; GlaxoSmithKline GmbH & Co.KG, Munchen, Germany) intramuscularly every 48 hr, 20 ml/kg of a mixture of Ringer’s solution as a supportive fluid therapy subcutaneously every 24 hr (Delta Select GmbH, Dreidech, Germany), 25% of ami- no acids (Volamin^Ⓡ; Merial GmbH, Hallbergmoos, Germany), 5% of glucose (Baxter Deutschland GmbH, Unterschleißheim, Germany), and 0.5% of calcium gluc- onate (B. Braun Melsungen AG, Melsungen, Germany;

0.5%). For radiographic examination, lateral projection was performed and revealed cardiomegaly, pericardial

effusion, and a soft opacity superimposed over the cardiac silhouette (Fig. 1B). The pericardiocentesis was given to the baby snake as its mother through ultrasonography-guided to remove serosanguinous fluid from the heart. Despite all these treatments, the baby snake did not survive, and an autopsy was performed immediately.

Gross pathological examination on abdominal organs revealed that there was no infection or sepsis, but in- stead it was shrunken in size due to malnutrition as its mother. Moderate amount of pale yellow, translucent fluid was observed in the opened pericardial sac and right atrium and ventricle were observed to be dilated.

When an incision of heart was made, a gritty con- sistency on the cutting surface was noted. The tissue samples from the heart was taken for further histopathological examination.

Tissue specimens were fixed in 10% (w/v) neutral buffered formalin solution and then trimmed and rou- tinely processed, embedded in paraffin, sectioned at ap- proximately 4 to 5 mm using a Leica RM 2235 CWEU microtome. The slides were stained with Hematoxylin and Eosin (H&E) and then subjected to a microscopic examination (Oh and Cho, 2017). Additional heart sections were conducted for the histochemical demonstration of calcium salts. The slides were stained with the classical von Kossa’s method (Chaplin and Grace, 1975). Briefly, the slide was treated with a silver nitrate solution until the silver being deposited by replacing the calcium in the presence of strong light. Then, it was vi- sualized as metallic silver. After counterstaining, the slide was dehydrated and mounted. Histopathologically, heart tissue showed necrosis of cardiomyocytes (Fig.

2A) evidenced by cytoplasmic swelling, vacuolization

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Myocardial degeneration in Russian rat snake 219

A B C

Fig. 2. Russian rat snake (Elaphe schrencki). A. Myocyte necrosis, heart. H&E. Scale bar=200 m. B. Tissue calcification, heart. H&E. Scale bar=50 m; C. Myocardial calcification, heart. Von Kossa’s silver stain. Scale bar=20 m.

and hyalinization which probably preceded gross calcification. Tissue calcification (Fig. 2B), myocardial calcification (Fig. 2C), and displacement of muscular fibers by limy deposits were observed. Area of calcification were scattered throughout the ventricle and it was greater in ventricle being able to be seen by naked eyes.

Based on histopathology findings, this snake has severe myocardial degeneration. The snake had worsening dia- stolic dysfunction before death that was thought to be related to the extensive calcifications, emphasizing the clinical finding.

DISCUSSION

Although a great knowledge regarding the physiology and evolutionary importance of the reptile heart has been assembled, but the clinical implication in veterinary medicine has presented limited attentions (White, 1976). Reptile cardiology may be considered to be its infancy (Kik and Mitchell, 2005). A detail description about the snake cardiology has been described and re- viewed by various authors and can be consulted for bet- ter understanding (Farrell et al, 1998; Girling and Hynes, 2004; Murray, 2006; Wyneken, 2009; Jensen et al, 2010).

Reptile heart diseases have barely known compared to mammals, such as heart enlargement and congenital cardiovascular abnormalities. The myocardial degeneration of a Russian rat snake was reported in this case report.

Most of the cardiovascular disorders reported in reptiles were secondary problems associated with parasitism, infection, nutritional imbalances, and poor husbandry prac-

tices (Madar, 1996).

Classically, cardiac calcification has two main patterns, dystrophic and metastatic, and the latter was the most common in reptiles (Gore and Aron, 1949).

Dystrophic mineralization of arteries was seen in various lizards (Chinnadurai et al, 2008; Borza and Bolfa, 2012) associated most likely with renal failure, tissue trauma, hypervitaminosis D, and other metabolic disturbances, whereas metastatic calcification due to the secondary nutritional hyperparathyroidism (Kik and Mitchell, 2005) was reported in a Chinese water dragon (Physignathus concincinus). Ruptured aorta was induced by mineraliza- tion secondary to hyperparathyroidism and a mandibular abscess. The pathogenesis associated with malnutrition remains to be understood. However, it is thought that vitamin D may play an important role (Allen, 2003). In our case, the snake have calcification in myocardial fibers that was suspicious of nutritional cause. Myocardial degeneration in several reptiles species has been reported due to vitamin E deficiency (Frye, 1991).

The heart of reptiles can be affected by various diseases: pericardial effusion, cardiomyopathy, septic endocarditis, myocarditis, parasitic infestation, infarction, ar- terial calcifications, aneurysms, thrombosis, parasitic infestation, or tumors (Wagner, 1989; Frye,1991; Jacobson et al, 1991; Schilliger et al, 2010). Two cases of cardiomyopathy has been described in snakes (Barten, 1980; Jacobson et al, 1980). A mole king snake (Lampropeltis calligaster rhombomaculata) was presented with lesions characterized by primary collagen pro- liferation and replacement of myocardial fibrils by fi- brocollagen (Barten, 1980) while a Deckert’s rat snake (Elaphe obsoleta deckertii) was presented with degener-

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220 Shraddha Tiwari, Sulhi Aufa, Hyung-Hun Park, Ho-Seong Cho, Byung-Yong Park, Yeonsu Oh

ation and necrosis of myocardial fibers (Jacobson et al, 1980) which is similar to my case study. Both of the cases led to congestive heart failure

Based on the findings, diagnosis of Russian rat snake (Elaphe schrencke), myocardial degeneration was made due to the deposition of calcium within myocardium which is the first report case of snakes on myocardium degeneration and was suspicious congestive heart failure for the snake when it was alive. An additional ex- planation for the formation of myocardium degeneration could be congenital, as the mother of the snake as well as her all neolates have the similar problems of heart and also supposed of nutrition disorders.

There have been few reports of snakes on cardiovascular diseases. The most recently reported case of myocardial degeneration in a Russian rat snake is the first reported case of myocardial degeneration and con- tribution to the rare reports of cardiac disease in snakes.

ACKNOWLEDGEMENTS

This study is supported by 2016 Research Grant from Kangwon National University (No. 520160497).

REFERENCES

Allen ME, Oftedal OT. 2003. Nutrition in captivity. In Biology and husbandry of the green iguana. Malabar (FL):

Krieger Publishing Company 47-74.

Barten SL. 1980. Cardiomyopathy in a king snake (Lampropeltis calligaster rhombomaculata). Vet Med Small Anim Clin 75: 125-9.

Borza G, Bolfa P. 2012. Pathologic mineralization in captive reptiles. Bull UA SMV Vet Med 69: 1-2.

Chaplin AJ, Grace SR. 1975. Calcium oxalate and the von Kossa method with reference to the influence of citric acid.

Histochem J 7: 451-458.

Elliott RJ, John CS, Meliton NN, James PD. 1980. Heart failure associated with unusual hepatic inclusions in a Deckert’s rat snake. J Wildl Dis 15: 75-81.

Frye FL. 1991. Common pathologic lesions & disease processes.

In Biomedical and surgical aspects of captive reptile husbandry. Malabar (FL): Krieger Publishing Co.

Funk RS. 1996. Snakes. In Reptile medicine and surgery.

Philadelphia (US): W.B. Saunders 39-46.

Gore I, Aron SW. 1949. Calcification of myocardium: a pathology study of thirteen cases. Arch Path 48: 1.

Jacobson ER, Homer B, Adams W. 1991. Endocarditis and con- gestive heart failure in a Burmese python (Python molu- rus bivittatus). J Zoo Wildl Med 22: 245-248.

Jensen B, Abe AS, Andrade DV, Nyengaard JR, Wang T. 2010a.

The heart of the South American rattlesnake (Crotalus durissus). J Morphol 271: 1066-1077.

Jensen B, Nyengaard JR, Pedersen M, Wang T. 2010b. Anatomy of the python heart. Anat Sci Int 85(4): 194-203.

Kik MJL, Mitchell M. 2005. Reptile cardiology: a review of anatomy and physiology, diagnostic approaches, and clinical disease. Semin Avian Exot Pet Med 14(1): 52-60.

Meloan SN, Puchtler H. 1985. Chemical mechanisms of staining methods: von Kossa’s technique. What von Kossa really wrote and a modified reaction for selective demonstration of inorganic phosphate. J Histotechol 8:11-13.

Murray MJ. 2006. Cardiopulmonary anatomy and physiology. In Reptile medicine and surgery 2nd editon. Missouri (US):

Saunders Elsevier 124-134.

Oh Y, Cho HS. 2017. Primary pulmonary adenocarcinoma meta- stasized to kidney in a captive nutria (Myocastor coy- pus). Kor J Vet Ser 40(2): 139-142.

Schilliger L, Lemberger K, Chai N, Bourgeois A, Charpentier M.

2010. Atherosclerosis associated with pericardial effu- sion in a central bearded dragon (Pogona vitticeps). J Vet Diagn Invest 22: 789-792.

Schroff S, Schmidt V, Kiefer I, Krautwald-Junghanns ME, Pees M. 2010. Ultrasonographic diagnosis of an endocarditis valvularis in a Burmese python (python molurus bivitta- tus) with pneumonia. J Zoo Wildl Med 41(4): 721-724.

Starck JM. 2009. Functional morphology and patterns of blood ﬂ ow in the heart of Python regius. J Morphol 270:

673-687.

White FN. 1976. Circulation. In Biology of the reptilian. London (UK): Academic Press Inc. 273-334.

Wyneken J. 2009. Normal reptile heart morphology and function.

Vet Clin Exot Anim 12: 51-63.