Left coronary artery to main pulmonary artery fistula in a dog

Left coronary artery to main pulmonary artery fistula in a dog | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Case Report Left coronary artery to main pulmonary artery fistula in a dog CF Agudelo, B Lukac, A Bockay, N Vargova, G Kackova, M Figurova, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3972957/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 04 Aug, 2025 Read the published version in BMC Veterinary Research → Version 1 posted 10 You are reading this latest preprint version Abstract A vascular communication between the left coronary artery and the main pulmonary artery (coronary fistula) was diagnosed as an incidental finding in a 3-year-old female Tatran hound by echocardiography as part of preanesthetic evaluation. The history, clinical examination, and diagnostic imaging did not reveal evidence of trauma or endocarditis which could have led to this condition. Transthoracic echocardiography revealed dilation of the left coronary sinus secondary to an abnormal vessel shunting blood into the main pulmonary artery. Computed tomography confirmed this diagnosis. Coronary artery fistula is a very rare finding in human and animals. According to the authors, this is the first clinical case of a congenital fistula between the left coronary artery and the main pulmonary artery in a dog. Figures Figure 1 Figure 2 Figure 3 Figure 4 Background Coronary artery fistula (CAF) is a very rare condition in which the left or right coronary artery terminates directly into a heart chamber or great vessel without passing through the capillaries [1,2]. They may develop as congenital anomalies, as a complications of trauma or surgery, or as a result of a ruptured aneurysm of the sinus of Valsalva [3,4]. In animals, CAFs are occasionally observed as isolated coronary and pulmonary arterial junctions or as part of a larger thoracic arteriovenous malformation [5,6]. The incidence of CAF has been determined to be 0.9% of all heart diseases in dogs [2]. Fistulae originate from the right coronary artery (RCA) in approximately 52% of patients, the paraconal interventricular branch in 30%, and the circumflex branch in 18% of cases [5,7,8,9]. More than 90% of fistulae from a single coronary artery drain to the right side of the heart, and the remainder drain to the left side of the heart [7]. Additionally, human studies have revealed that CAFs extending into the main pulmonary artery (MPA) originate in 28% of the left coronary artery (LCA), 14% from the RCA and 57% from both coronary arteries [10]. The blood vessels that form the fistula are histologically of arterial origin because of their similarity to the pulmonary artery [2]. In this article, we report a case of an LCA fistula communicating with the MPA and demonstrate the use of echocardiography to visualize lesions, fistular blood flow and its drainage site. Case presentation A 3-year-old, 14-kg, female-neutered Tatra hound dog was examined at the University Veterinary Hospital at the University of Veterinary Medicine and Pharmacy in Košice, Slovakia for anesthetic purposes. She was asymptomatic for heart disease. Clinical examination was unremarkable. A six-lead electrocardiogram (EKG Praktik Veterinary®, SEIVA, Czech Republic) showed normal sinus arrhythmia (100 bpm) (Figure 1). Transthoracic echocardiography (TTE) (Esaote Mylab X5 Vet with 3.5 and 5.0 MHz transducers, Genova, Italy) was performed in accordance with recommended standards for dogs. There were a subjectively normal left ventricular dimensions in diastole (left ventricular internal diameter = 29.4 mm), and systole (left ventricular internal diameter = 18.7 mm). The left atrial diameter, as measured in the short axis was considered subjectively enlarged (left atrial diameter = 26.2 mm) but normal according to the left atrial-to-aorta-ratio (1.43). Additionally, the aortic annulus had an irregular shape at the left coronary cusp (Figure 2A). The left coronary ostium and LCA appeared dilated on the short and long axis right parasternal views. On assessment of the MPA, a jet of continuous blood flow, entering from the abnormal coronary cusp just distal to the pulmonic valve, was identified traveling in an antegrade and retrograde direction within the lumen of the MPA (Figure 2B,C). Visible mild pulmonary regurgitation was also observed (Figure 2D). The jet had a velocity of approximately 0.8 m/s both in systole and diastole. Despite these results it was suggested that anesthesia would be safe. Thoracic radiography was performed during anesthesia and revealed a normal vertebral heart score of 10.2 units (reference interval 8.5-10.5) with bulging the region of the ascending aorta ventrodorsal and lateral projections (Figure 3). The anatomy of coronary vessels was further evaluated via computed tomography (Philips Access CT, Philips Medical Systems, The Netherlands). Nongated CT scanning was conducted under general anesthesia. Two intravenous catheters were placed before premedication in the cephalic veins following aseptic preparation. The dog was premedicated with butorphanol 0.2 mg/kg (Butomidor; Richter Pharma AG, Austria) plus medetomidine 15 μg/kg (Cepetor; CP-Pharma Handelsges, Germany) intravenously (IV). General anesthesia was induced with intravenous (IV) propofol (Propofol; Fresenius Kabi GmbH, Austria) until endotracheal intubation was achieved and anesthesia was maintained with isoflurane (Isoflutek, 1000 mg/g, Laboratorois Karizoo, Spain) in 100% oxygen. Lactated Ringer´s solution (Compound Sodium Lactate Ringer-Lactat; B. Braun Melsungen AG, Germany) was started at a constant rate of 10 ml/kg/ hour. The CT scanning parameters were 100 kVp, 57 mA, a 512 × 512 matrix, a 207 mm FOV, a 2 mm collimation thickness, and a pitch of 1.0625. Precontrast and postcontrast CT images were acquired. Six hundred milligrams of iodine/kg iohexol contrast medium (Omnipaque 300 mg/ml, GE Healthcare, Norway) was intravenously injected at the injection rate of 2 mL/s with a power injector and a postcontrast scan was performed 60 s after the first injection. CT images revealed a short course of the LCA that divided into the left circumflex and left paraconal arteries (Figure 4A). The latter in oblique views courses tortuously and slightly cranioventrally and toward the left (Figure 4B,C), and then shortly after its origin inserts into the MPA. Routine blood work including heart marker troponin I (0.05, range < 0,1 ng/ml) and NT-proBNP (< 500, range < 900 pmol/l) was unremarkable. The patient recovered from anesthesia uneventfully and until now remains without signs of cardiac disease. Discussion This article describes a very rare vascular condition in a dog. To the authors’ knowledge, this is the first report of a coronary arterial shunt from the LCA to the MPA in a dog. The diagnosis of this congenital abnormality was achieved through a multimodal imaging approach including TTE and CT imaging. Cases of CAF in veterinary medicine have been described for canine, feline, bovine, and camelid patients [1,2,3,4,5,8,9,11,12,13]. Fistulous connections between the coronary arterial system can communicate directly to the cardiac chambers (coronary cameral fistula), to a great vessel (coronary arteriovenous shunt) [8] such as the MPA or the cava vein or can finish inside the cardiac myocardium (aortocardiac fistula) [5,11,13]. The last type seems to be very serious in horses [11,13], where the CAF may finish into the interventricular septum, which results in ventricular arrhythmias, left-sided congestive heart failure (CHF) or wall rupture [11,13]. Further classification of CAFs may include the size and number of fistulae present, with solitary macro fistulas being more common than multiple micro fistulas [14]. We presume that its origin may be congenital because there was no evidence of trauma or surgery of the thorax, neither local nor systemic infection nor neoplastic process from the history and other examinations including radiographs, CT scan, abdominal ultrasound or blood tests. In general, congenital CAFs arise secondary to embryonic developmental disturbances resulting in the persistence of the vascular network which nourishes embryonic ventricular walls. These remnants are known as Thebesian vessels, which provide direct connections between the coronary vasculature and the heart chambers, bypassing the coronary sinus [12]. In humans, most CAFs (90%) drain into the right side of the heart, with the other 10% terminating into left-sided chambers [1,8]. In asymptomatic human patients, CAFs typically originate from the LCA and often drain into the MPA [8]; however, this type of connection has not been described in the veterinary literature until now. The presence or absence of clinical signs is thought to be determined by the size, location, and configuration of the fistula itself [1]. In our patient, a murmur was not detected during clinical examination. This was probably due to the small size and flow velocity through the shunt. These anatomic facts can also explain, -at least partially-, why our patient remains without clinical signs and even underwent anesthesia without complications. Most of CAF cases in humans have a continuous or more commonly diastolic murmur [1]. Medium to large CAFs can result in volume overload and chamber remodeling, which can lead to CHF, exercise intolerance, endocarditis, myocardial ischemia [1], fistula rupture [4,9,12] and arrhythmias, particularly atrial fibrillation, if there is atrial enlargement [9]. Furthermore, the dog described in this report had no obvious evidence of coronary steal syndrome (when blood is preferentially shunted through the fistula rather than perfused through the myocardium, which leads to myocardial ischemia), as there were no clinical signs, no arrhythmias, normal left ventricular function [1,12,15] and no elevation of cardiac markers [1]. A final diagnosis was achieved through echocardiography and CT imaging, which are helpful complementary diagnostic tools for obtaining more precise information about coronary vessel anatomy and confirming the lesions. Standard two-dimensional and Doppler echocardiography initially proved useful for evaluating the CAF and providing information on intraluminal fistular flow and its site of drainage. However, spectral Doppler failed to show a more realistic value of systolic and diastolic velocities, although it was able to define flow direction during systole and diastole. On the other hand, color Doppler echocardiography demonstrated intraluminal fistular blood flow and its communication with the MPA. The continuous mosaic color signal observed within the fistula indicated flow signal aliasing as a result of turbulent blood flow. Other turbulent jets between the proximal aorta and MPA can be observed in cases of aortopulmonary window; however, the lesion in our patient was located at the level of the aortic valve, where there is a dilated and interrupted Valsalva sinus. A supracristal ventricular septal defect and coronary cameral fistula were also ruled out because the flow finished directly in the MPA. However, echocardiography may not be sufficient for the assessment of extracardiac structures and due to the size of our patient, we chose to perform CT imaging in lieu of cardiac catheterization with angiography [1]. Two-dimensional reformation and three-dimensional reconstruction provided an accurate depiction of the morphologic structures of the aortic root, coronary arteries and CAF; thus the presence of more distal fistulae or an aortic tunnel (abnormal tubular extracardiac communication between the aortic root and other heart structures) were also ruled out [5,6,16]. Coronary angiography may help in further characterization of this lesion and is considered the gold standard for the diagnosis of CAFs in humans. Transesophageal, and 3D echocardiography, and magnetic resonance imaging have also proven useful [15]; however, these modalities were unavailable at the time of diagnosis. No therapy was necessary. There was no evident dilation of the aorta or MPA, volume overload, or other changes compatible with ongoing pulmonary hypertension based on her hemodynamics (the Qp:Qs was estimated to be 1.19). Treatment options include surgical ligation of the fistula under cardiopulmonary bypass, percutaneous transcatheter closure, and medical management of the resulting volume overload and myocardial ischemia. Long-term medical management with antiplatelet drugs is indicated when aneurysmal dilation of the CAF causes blood stagnation and thrombosis [1,2]. None of the anterior splints were necessary for our patient who was free of clinical signs. Conclusions We classified this rare type of LCA-to-MPA shunt as a congenital, solitary, macrofistula based on the signalment, history, clinical examination and diagnostic imaging findings. This is a very rare condition, though as in other reported cases, it seldom causes clinical signs and is mostly an incidental finding during echocardiography or CT scan. Abbreviations PDA, patent ductus arteriosus CHF, chronic heart failure HR, heart rate f, respiratory rate ºC, Celsius LVDd, left ventricular diastolic diameter Vmax, maximum velocity PG, pressure gradient Declarations Ethics approval and consent to participate Consent for performing clinical procedures was obtained from the owner. The present case report does not include experimental data, and all data collected in this study were generated as part of the diagnostic work-up of the patient. Written informed consent from the dog’s owner was obtained for medical data to be used for educational and research purposes. Consent for publication Written informed consent from the dog’s owner was obtained for the publication. Availability of data and materials The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request. Competing interests The authors declare that they have no competing interests. Funding This study was supported by grant VEGA 1/0392/17 funded by the Scientific Grant Agency of Ministry of Education if the Slovakian Republic and Slovak Academy of Sciences. Authors' contributions C.F.A. echocardiography and revision of CT scans, and drafted the manuscript. B.L. ECG analysis, concept and critical review. A.B. hemodynamics, interpretation of data and critical review. M.F. radiographs, design and drafted the manuscript. N.V., G.K. and S.H. design, interpretation of data and critical review. All authors read and approved the final manuscript version. Acknowledgements Not applicable References Bowden S, Winter RL, Hostnik ET, Habing A, Green E. Right coronary artery to left ventricle coronary cameral fistula in a cat. J Vet Cardiol. 2022;44:57-62. doi: 10.1016/j.jvc.2022.10.001. Sato T, Takao K, Takao T, Fujioka T. A case of a dog with right coronary to pulmonary artery fistula [title in Japanese]. Adv Anim Cardiol, 2015;48:73-79. Jacobs GJ, Calvert CA, Hall DG, Kraus M. Diagnosis of right coronary artery to right atrial fistula in a dog using two-dimensional echocardiography. J Small Anim Pract. 1996;37:387-90. doi: 10.1111/j.1748-5827.1996.tb02422.x. Abbott JA, Porzio P. Rupture of the left aortic sinus into the pulmonary artery in a Dalmation dog. Vet Radiol Ultrasound. 1998;39:544-50. doi: 10.1111/j.1740-8261.1998.tb01649.x. Scansen BA. Coronary Artery Anomalies in Animals. In: Fonfara S, O’Sullivan L, editors. Special Issue Comparison of Cardiovascular Systems and Diseases Across Species. Vet Sci. 2017;4:20. doi: 10.3390/vetsci4020020 Scollan K, Salinardi B, Bulmer BJ, Sisson DD. Anomalous left-to-right shunting communication between the ascending aorta and right pulmonary artery in a dog, J Vet Cardiol. 2011;13:147-52. doi: 10.1016/j.jvc.2011.01.003. Qureshi SA. Coronary arterial fistulas. Orphanet J. Rare Dis. 2006;1:51. doi: 10.1186/1750-1172-1-51. Pelosi A, Côté E, Eyster GE. Congenital coronary-pulmonary arterial shunt in a German shepherd dog: Diagnosis and surgical correction. J Vet Cardiol. 2011;13:153-8. doi: 10.1016/j.jvc.2011.03.001. Tursi M, Poser H, Janus I, Guglielmini C. Pathology in Practice. J Am Vet Med Assoc. 2018;253:1551-1553. doi: 10.2460/javma.253.12.1551. Gobel LF, Anderson FC, Baltaxe AH, Amplatz K, Wang Y. (1970): Shunts between the coronary and pulmonary arteries with normal origin of the coronary arteries. Am. J. Cardiol. 1970;25:655-61. doi: 10.1016/0002-9149(70)90615-6. Baker RE, Schlipf JW, Scollan KF, LeBlanc NL, Russell DS, In-hospital development of an aorto-cardiac fistula in a Warmblood gelding with chronic renal disease. Equine Vet Educ. 2021;33:e86-e91. Bildfell RJ, Pringle JK, Miller LM. Coronary Arterioventricular Anomaly in a Calf. J Vet Diagn Invest. 1996;8:500-2. doi: 10.1177/104063879600800421. Marr CM, Reef VB, Brazil TJ, Thomas WP, Knottenbelt DC, Kelly DF, Baker JR, Reimer JM, Maxson AD, Crowhurst JS. Aorto-cardiac fistulas in seven horses. Vet. Radiol. Ultrasound. 1998;39:22–31. Said SA, Lam J, van der Werf T. Solitary coronary artery fistulas: a congenital anomaly in children and adults. A contemporary review. Congenit Heart Dis. 2006;1:63-76. Blake RR, Longo M, Santarelli G, Liuti T, Martinez-Pereira Y. Coronary arteriovenous malformation in a dog with a complex arrhythmia and hypothyroidism. J Vet Cardiol. 2019;23:38-44. doi: 10.1016/j.jvc.2019.01.005. Geunha K, Yewon J, Ho-Gyun J, Taekwon L, Kichang L, Hakyoung Y. Case report: Imaging features of aorta-right atrial tunnel in a dog using two-dimensional echocardiography and computed tomography. Front Vet Sci. 2023;10:1160390. doi: 10.3389/fvets.2023.1160390. Additional Declarations No competing interests reported. Cite Share Download PDF Status: Published Journal Publication published 04 Aug, 2025 Read the published version in BMC Veterinary Research → Version 1 posted Editorial decision: Revision requested 11 Sep, 2024 Reviews received at journal 03 May, 2024 Reviewers agreed at journal 29 Apr, 2024 Reviews received at journal 16 Apr, 2024 Reviewers agreed at journal 15 Apr, 2024 Reviewers invited by journal 05 Apr, 2024 Editor invited by journal 06 Mar, 2024 Editor assigned by journal 22 Feb, 2024 Submission checks completed at journal 22 Feb, 2024 First submitted to journal 20 Feb, 2024 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3972957","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Case Report","associatedPublications":[],"authors":[{"id":274349119,"identity":"bdfdd7e2-f4ff-4176-b41e-14c60e3f0695","order_by":0,"name":"CF Agudelo","email":"","orcid":"","institution":"Veterinary Teaching Hospital, University of Veterinary Medicine and Pharmacy in Košice","correspondingAuthor":false,"prefix":"","firstName":"CF","middleName":"","lastName":"Agudelo","suffix":""},{"id":274349121,"identity":"6df262fc-14b1-455a-b2e9-05840abb8266","order_by":1,"name":"B Lukac","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABAklEQVRIiWNgGAWjYBACexCRwGABJHkYGBsYGOQYGJgbPoDEcAHDBrAWCbgWYwYGxsYZ+LQYHABTCC2JDYS0GM4+/OzBgz8S8gYHeNgkZ9TYpW+4kdjYwPAnDbdf+NLMDRLbJAw3gLRsOJacC9bC2JaD25YeBjOJxAYJxpkNQC0P2A7kbjhzsP0BY0MFbr+cYf8mkfBHwh6i5d+BdIMzB0EOw6eFx0wigU0isZ8BqGVj24EEg+ONQC1s+BzGUyYB9EtyPzMPs+XMvmTDmSAtiW14vM/Dvk3yxx8b2zb2/oc3e77ZyfMdZj7Y8OFPMk4tCMCMzEkgQsMoGAWjYBSMAtwAAJxDVilXHikbAAAAAElFTkSuQmCC","orcid":"","institution":"Veterinary Teaching Hospital, University of Veterinary Medicine and Pharmacy in Košice","correspondingAuthor":true,"prefix":"","firstName":"B","middleName":"","lastName":"Lukac","suffix":""},{"id":274349123,"identity":"22ee531c-5363-4eca-92ad-27563a6f2c04","order_by":2,"name":"A Bockay","email":"","orcid":"","institution":"Veterinary Teaching Hospital, University of Veterinary Medicine and Pharmacy in Košice","correspondingAuthor":false,"prefix":"","firstName":"A","middleName":"","lastName":"Bockay","suffix":""},{"id":274349124,"identity":"ade9f923-9261-48f0-9ee4-8ec512817842","order_by":3,"name":"N Vargova","email":"","orcid":"","institution":"Veterinary Teaching Hospital, University of Veterinary Medicine and Pharmacy in Košice","correspondingAuthor":false,"prefix":"","firstName":"N","middleName":"","lastName":"Vargova","suffix":""},{"id":274349125,"identity":"846cf765-d4a5-41bc-b8d7-6d2ffe2a3a9c","order_by":4,"name":"G Kackova","email":"","orcid":"","institution":"Veterinary Teaching Hospital, University of Veterinary Medicine and Pharmacy in Košice","correspondingAuthor":false,"prefix":"","firstName":"G","middleName":"","lastName":"Kackova","suffix":""},{"id":274349126,"identity":"24b62ef5-4bdf-4eee-93d1-2c7c90476b2c","order_by":5,"name":"M Figurova","email":"","orcid":"","institution":"Veterinary Teaching Hospital, University of Veterinary Medicine and Pharmacy in Košice","correspondingAuthor":false,"prefix":"","firstName":"M","middleName":"","lastName":"Figurova","suffix":""},{"id":274349127,"identity":"07d2c42c-0369-40d5-8446-29ce39875eb3","order_by":6,"name":"S Hornak","email":"","orcid":"","institution":"Veterinary Teaching Hospital, University of Veterinary Medicine and Pharmacy in Košice","correspondingAuthor":false,"prefix":"","firstName":"S","middleName":"","lastName":"Hornak","suffix":""}],"badges":[],"createdAt":"2024-02-20 14:07:15","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3972957/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3972957/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1186/s12917-025-04730-y","type":"published","date":"2025-08-04T15:57:00+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":51565907,"identity":"a2f96c09-cb98-4541-ae4f-26b05bad358d","added_by":"auto","created_at":"2024-02-23 19:09:46","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":57124,"visible":true,"origin":"","legend":"\u003cp\u003e6-lead ECG. Sinus arrhythmia. The average heart rate is 100 bpm. Mean electrical axis 60 degrees. Speed 50 mm/s, amplitude 0.5 cm = 1 mV\u003c/p\u003e","description":"","filename":"1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-3972957/v1/27cd654b383c17f6133b5d88.jpg"},{"id":51565910,"identity":"83b74b93-35f1-4eab-aa18-808896c66cf5","added_by":"auto","created_at":"2024-02-23 19:09:46","extension":"jpg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":146150,"visible":true,"origin":"","legend":"\u003cp\u003eTTE images from right parasternal short axis 2D and color Doppler echocardiographic images at the heart base demonstrating an abnormal left-to-right fistula with a course that circumscribes the left coronary cusp and empties into the MPA during system and diastole. Right parasternal short axis view: An abnormal aortic cusp and a defect (arrow) are observed between the proximal walls of the great arteries (A), through which a low-velocity bidirectional turbulent blood flow (backward and forward) into the MPA is demonstrated (B,C). The left cranial parasternal short axis view (D) shows a flow from the CAF that prolonged up to pulmonary artery bifurcation. Mild pulmonary regurgitation was also observed. AV = aortic valve, MPA = pulmonary artery, PV = pulmonary valve, RV = right ventricle, LA = left atrium.\u003c/p\u003e","description":"","filename":"2.jpg","url":"https://assets-eu.researchsquare.com/files/rs-3972957/v1/ec55c9f0891ea5a938e43694.jpg"},{"id":51565908,"identity":"03a25172-7554-4637-ba78-1932b5c0c39b","added_by":"auto","created_at":"2024-02-23 19:09:46","extension":"jpg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":46351,"visible":true,"origin":"","legend":"\u003cp\u003eDorsoventral and right lateral views taken under anesthesia. There was a mild bulging at the level of ascending aorta (arrows).\u003c/p\u003e","description":"","filename":"3.jpg","url":"https://assets-eu.researchsquare.com/files/rs-3972957/v1/f42b79cf46a51461e8caa46c.jpg"},{"id":51565906,"identity":"bbba6254-b929-4d91-9a32-50defb16170c","added_by":"auto","created_at":"2024-02-23 19:09:46","extension":"jpg","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":35787,"visible":true,"origin":"","legend":"\u003cp\u003eA. Multiplanar reconstruction at the level of the aortic valve in the axial view displaying a short LCA dividing in the LCx and LPc arteries (arrows). B. Oblique view of Figure 4A demonstrating a tortuous coronary fistula terminating at the MPA. C Multiplanar reconstruction at the level of the heart base in a sagittal view, demonstrating a CAF from the aortic root to the MPA (arrow}.\u003c/p\u003e","description":"","filename":"4.jpg","url":"https://assets-eu.researchsquare.com/files/rs-3972957/v1/961f27cbf33653eac5994b1f.jpg"},{"id":88814237,"identity":"673183a9-2a07-4483-9668-4017fa1ed6d7","added_by":"auto","created_at":"2025-08-11 16:08:56","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":641602,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3972957/v1/565e14fd-6496-4c28-8dd3-0424ed7d1a2a.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Left coronary artery to main pulmonary artery fistula in a dog","fulltext":[{"header":"Background","content":"\u003cp\u003eCoronary artery fistula (CAF) is a very rare condition in which the left or right coronary artery terminates directly into a heart chamber or great vessel without passing through the capillaries [1,2]. They may develop as congenital anomalies, as a complications of trauma or surgery, or as a result of a ruptured aneurysm of the sinus of Valsalva [3,4]. In animals, CAFs are occasionally observed as isolated coronary and pulmonary arterial junctions or as part of a larger thoracic arteriovenous malformation [5,6]. The incidence of CAF has been determined to be 0.9% of all heart diseases in dogs [2]. Fistulae originate from the right coronary artery (RCA) in approximately 52% of patients, the paraconal interventricular branch in 30%, and the circumflex branch in 18% of cases [5,7,8,9]. More than 90% of fistulae from a single coronary artery drain to the right side of the heart, and the remainder drain to the left side of the heart [7]. Additionally, human studies have revealed that CAFs extending into the main pulmonary artery (MPA) originate in 28% of the left coronary artery (LCA), 14% from the RCA and 57% from both coronary arteries [10]. The blood vessels that form the fistula are histologically of arterial origin because of their similarity to the pulmonary artery [2]. In this article, we report a case of an LCA fistula communicating with the MPA and demonstrate the use of echocardiography to visualize lesions, fistular blood flow and its drainage site.\u003c/p\u003e"},{"header":"Case presentation","content":"\u003cp\u003eA 3-year-old, 14-kg, female-neutered Tatra hound dog was examined at the University Veterinary Hospital at the University of Veterinary Medicine and Pharmacy in Ko\u0026scaron;ice, Slovakia for anesthetic purposes. She was asymptomatic for heart disease. Clinical examination was unremarkable. A six-lead electrocardiogram (EKG Praktik Veterinary\u0026reg;,\u003c/p\u003e\n\u003cp\u003eSEIVA, Czech Republic) showed normal sinus arrhythmia (100 bpm) (Figure 1). Transthoracic echocardiography (TTE) (Esaote Mylab X5 Vet with 3.5 and 5.0 MHz transducers, Genova, Italy) was performed in accordance with recommended standards for dogs. There were a subjectively normal left ventricular dimensions in diastole (left ventricular internal diameter = 29.4 mm), and systole (left ventricular internal diameter = 18.7 mm). The left atrial diameter, as measured in the short axis was considered subjectively enlarged (left atrial diameter = 26.2 mm) but normal according to the left atrial-to-aorta-ratio (1.43). Additionally, the aortic annulus had an irregular shape at the left coronary cusp (Figure 2A). The left coronary ostium and LCA appeared dilated on the short and long axis right parasternal views. On assessment of the MPA, a jet of continuous blood flow, entering from the abnormal coronary cusp just distal to the pulmonic valve, was identified traveling in an antegrade and retrograde direction within the lumen of the MPA (Figure 2B,C). Visible mild pulmonary regurgitation was also observed (Figure 2D). The jet had a velocity of approximately 0.8 m/s both in systole and diastole. Despite these results it was suggested that anesthesia would be safe. Thoracic radiography was performed during anesthesia and revealed a normal vertebral heart score of 10.2 units (reference interval 8.5-10.5) with bulging the region of the ascending aorta ventrodorsal and lateral projections (Figure 3). The anatomy of coronary vessels was further evaluated via computed tomography (Philips Access CT, Philips Medical Systems, The Netherlands). Nongated CT scanning was conducted under general anesthesia. Two intravenous catheters were placed before premedication in the cephalic veins following aseptic preparation. The dog was premedicated with butorphanol 0.2 mg/kg (Butomidor; Richter Pharma AG, Austria) plus medetomidine 15 \u0026mu;g/kg (Cepetor; CP-Pharma Handelsges, Germany) intravenously (IV). General anesthesia was induced with intravenous (IV) propofol (Propofol; Fresenius Kabi GmbH, Austria) until endotracheal intubation was achieved and anesthesia was maintained with isoflurane (Isoflutek, 1000 mg/g, Laboratorois Karizoo, Spain) in 100% oxygen. Lactated Ringer\u0026acute;s solution (Compound Sodium Lactate Ringer-Lactat; B. Braun Melsungen AG, Germany) was started at a constant rate of 10 ml/kg/ hour. The CT scanning parameters were 100 kVp, 57\u0026thinsp;mA, a 512\u0026thinsp;\u0026times;\u0026thinsp;512 matrix, a 207\u0026thinsp;mm FOV, a 2\u0026thinsp;mm collimation thickness, and a pitch of 1.0625. Precontrast and postcontrast CT images were acquired. Six hundred milligrams of iodine/kg iohexol contrast medium (Omnipaque 300 mg/ml, GE Healthcare, Norway) was intravenously injected at the injection rate of 2\u0026thinsp;mL/s with a power injector and a postcontrast scan was performed 60\u0026thinsp;s after the first injection. CT images revealed a short course of the LCA that divided into the left circumflex and left paraconal arteries (Figure 4A). The latter in oblique views courses tortuously and slightly cranioventrally and toward the left (Figure 4B,C), and then shortly after its origin inserts into the MPA.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eRoutine blood work including heart marker troponin I (0.05, range \u0026lt; 0,1 ng/ml) and NT-proBNP (\u0026lt; 500, range \u0026lt; 900 pmol/l) was unremarkable. The patient recovered from anesthesia uneventfully and until now remains without signs of cardiac disease.\u0026nbsp;\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eThis article describes a very rare vascular condition in a dog. To the authors\u0026rsquo; knowledge, this is the first report of a coronary arterial shunt from the LCA to the MPA in a dog. The diagnosis of this congenital abnormality was achieved through a multimodal imaging approach including TTE and CT imaging. Cases of CAF in veterinary medicine have been described for canine, feline, bovine, and camelid patients [1,2,3,4,5,8,9,11,12,13]. Fistulous connections between the coronary arterial system can communicate directly to the cardiac chambers (coronary cameral fistula), to a great vessel (coronary arteriovenous shunt) [8] such as the MPA or the cava vein or can finish inside the cardiac myocardium (aortocardiac fistula) [5,11,13]. The last type seems to be very serious in horses [11,13], where the CAF may finish into the interventricular septum, which results in ventricular arrhythmias, left-sided congestive heart failure (CHF) or wall rupture [11,13]. Further classification of CAFs may include the size and number of fistulae present, with solitary macro fistulas being more common than multiple micro fistulas [14]. We presume that its origin may be congenital because there was no evidence of trauma or surgery of the thorax, neither local nor systemic infection nor neoplastic process from the history and other examinations including radiographs, CT scan, abdominal ultrasound or blood tests. In general, congenital CAFs arise secondary to embryonic developmental disturbances resulting in the persistence of the vascular network which nourishes embryonic ventricular walls. These remnants are known as Thebesian vessels, which provide direct connections between the coronary vasculature and the heart chambers, bypassing the coronary sinus [12].\u003c/p\u003e\n\u003cp\u003eIn humans, most CAFs (90%) drain into the right side of the heart, with the other 10% terminating into left-sided chambers [1,8]. In asymptomatic human patients, CAFs typically originate from the LCA and often drain into the MPA [8]; however, this type of connection has not been described in the veterinary literature until now. The presence or absence of clinical signs is thought to be determined by the size, location, and configuration of the fistula itself [1]. In our patient, a murmur was not detected during clinical examination. This was probably due to the small size and flow velocity through the shunt. These anatomic facts can also explain, -at least partially-, why our patient remains without clinical signs and even underwent anesthesia without complications. Most of CAF cases in humans have a continuous or more commonly diastolic murmur [1]. Medium to large CAFs can result in volume overload and chamber remodeling, which can lead to CHF, exercise intolerance, endocarditis, myocardial ischemia [1], fistula rupture [4,9,12] and arrhythmias, particularly atrial fibrillation, if there is atrial enlargement [9]. Furthermore, the dog described in this report had no obvious evidence of coronary steal syndrome (when blood is preferentially shunted through the fistula rather than perfused through the myocardium, which leads to myocardial ischemia), as there were no clinical signs, no arrhythmias, normal left ventricular function [1,12,15] and no elevation of cardiac markers [1].\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eA final diagnosis was achieved through echocardiography and CT imaging, which are helpful complementary diagnostic tools for obtaining more precise information about coronary vessel anatomy and confirming the lesions. Standard two-dimensional and Doppler echocardiography initially proved useful for evaluating the CAF and providing information on intraluminal fistular flow and its site of drainage. However, spectral Doppler failed to show a more realistic value of systolic and diastolic velocities, although it was able to define flow direction during systole and diastole. On the other hand, color Doppler echocardiography demonstrated intraluminal fistular blood flow and its communication with the MPA. The continuous mosaic color signal observed within the fistula indicated flow signal aliasing as a result of turbulent blood flow. Other turbulent jets between the proximal aorta and MPA can be observed in cases of aortopulmonary window; however, the lesion in our patient was located at the level of the aortic valve, where there is a dilated and interrupted Valsalva sinus. A supracristal ventricular septal defect and coronary cameral fistula were also ruled out because the flow finished directly in the MPA. However, echocardiography may not be sufficient for the assessment of extracardiac structures and due to the size of our patient, we chose to perform CT imaging in lieu of cardiac catheterization with angiography [1]. Two-dimensional reformation and three-dimensional reconstruction provided an accurate depiction of the morphologic structures of the aortic root, coronary arteries and CAF; thus the presence of more distal fistulae or an aortic tunnel (abnormal tubular extracardiac communication between the aortic root and other heart structures) were also ruled out [5,6,16].\u003c/p\u003e\n\u003cp\u003eCoronary angiography may help in further characterization of this lesion and is considered the gold standard for the diagnosis of CAFs in humans. Transesophageal, and 3D echocardiography, and magnetic resonance imaging have also proven useful [15]; however, these modalities were unavailable at the time of diagnosis.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eNo therapy was necessary. There was no evident dilation of the aorta or MPA, volume overload, or other changes compatible with ongoing pulmonary hypertension based on her hemodynamics (the Qp:Qs was estimated to be 1.19). Treatment options include surgical ligation of the fistula under cardiopulmonary bypass, percutaneous transcatheter closure, and medical management of the resulting volume overload and myocardial ischemia. Long-term medical management with antiplatelet drugs is indicated when aneurysmal dilation of the CAF causes blood stagnation and thrombosis [1,2]. None of the anterior splints were necessary for our patient who was free of clinical signs.\u0026nbsp;\u003c/p\u003e"},{"header":"Conclusions","content":"\u003cp\u003eWe classified this rare type of LCA-to-MPA shunt as a congenital, solitary, macrofistula based on the signalment, history, clinical examination and diagnostic imaging findings. This is a very rare condition, though as in other reported cases, it seldom causes clinical signs and is mostly an incidental finding during echocardiography or CT scan.\u003c/p\u003e"},{"header":"Abbreviations","content":"\u003cp\u003ePDA, patent ductus arteriosus\u003c/p\u003e\n\u003cp\u003eCHF, chronic heart failure\u003c/p\u003e\n\u003cp\u003eHR, heart rate\u003c/p\u003e\n\u003cp\u003ef, respiratory rate\u003c/p\u003e\n\u003cp\u003e\u0026ordm;C, Celsius\u003c/p\u003e\n\u003cp\u003eLVDd, left ventricular diastolic diameter\u003c/p\u003e\n\u003cp\u003eVmax, maximum velocity\u003c/p\u003e\n\u003cp\u003ePG, pressure gradient\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eEthics approval and consent to participate\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eConsent for performing clinical procedures was obtained from the owner. The present case report does not include experimental data, and all data collected in this study were generated as part of the diagnostic work-up of the patient. Written informed consent from the dog\u0026rsquo;s owner was obtained for medical data to be used for educational and research purposes.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent for publication\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWritten informed consent from the dog\u0026rsquo;s owner was obtained for the publication.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAvailability of data and materials\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting interests\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare that they have no competing interests.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis study was supported by grant VEGA 1/0392/17 funded by the Scientific Grant Agency of Ministry of Education if the Slovakian Republic and Slovak Academy of Sciences. \u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthors\u0026apos; contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eC.F.A. echocardiography and revision of CT scans, and drafted the manuscript. B.L. ECG analysis, concept and critical review. A.B. hemodynamics, interpretation of data and critical review. M.F. radiographs, design and drafted the manuscript. N.V., G.K. and S.H. \u0026nbsp;design, interpretation of data and critical review. All authors read and approved the final manuscript version.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgements\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable\u0026nbsp;\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eBowden S, Winter RL, Hostnik ET, Habing A, Green E. Right coronary artery to left ventricle coronary cameral fistula in a cat. J Vet Cardiol. 2022;44:57-62. doi: 10.1016/j.jvc.2022.10.001. \u003c/li\u003e\n\u003cli\u003eSato T, Takao K, Takao T, Fujioka T. A case of a dog with right coronary to pulmonary artery fistula [title in Japanese]. Adv Anim Cardiol, 2015;48:73-79.\u003c/li\u003e\n\u003cli\u003eJacobs GJ, Calvert CA, Hall DG, Kraus M. Diagnosis of right coronary artery to right atrial fistula in a dog using two-dimensional echocardiography. J Small Anim Pract. 1996;37:387-90. doi: 10.1111/j.1748-5827.1996.tb02422.x.\u003c/li\u003e\n\u003cli\u003eAbbott JA, Porzio P. Rupture of the left aortic sinus into the pulmonary artery in a Dalmation dog. Vet Radiol Ultrasound. 1998;39:544-50. doi: 10.1111/j.1740-8261.1998.tb01649.x.\u003c/li\u003e\n\u003cli\u003eScansen BA. Coronary Artery Anomalies in Animals. In: Fonfara S, O\u0026rsquo;Sullivan L, editors. Special Issue Comparison of Cardiovascular Systems and Diseases Across Species. Vet Sci. 2017;4:20. doi: 10.3390/vetsci4020020\u003c/li\u003e\n\u003cli\u003eScollan K, Salinardi B, Bulmer BJ, Sisson DD. Anomalous left-to-right shunting communication between the ascending aorta and right pulmonary artery in a dog, J Vet Cardiol. 2011;13:147-52. doi: 10.1016/j.jvc.2011.01.003. \u003c/li\u003e\n\u003cli\u003eQureshi SA. Coronary arterial fistulas. Orphanet J. Rare Dis. 2006;1:51. doi: 10.1186/1750-1172-1-51.\u003c/li\u003e\n\u003cli\u003ePelosi A, C\u0026ocirc;t\u0026eacute; E, Eyster GE. Congenital coronary-pulmonary arterial shunt in a German shepherd dog: Diagnosis and surgical correction. J Vet Cardiol. 2011;13:153-8. doi: 10.1016/j.jvc.2011.03.001. \u003c/li\u003e\n\u003cli\u003eTursi M, Poser H, Janus I, Guglielmini C. Pathology in Practice. J Am Vet Med Assoc. 2018;253:1551-1553. doi: 10.2460/javma.253.12.1551. \u003c/li\u003e\n\u003cli\u003eGobel LF, Anderson FC, Baltaxe AH, Amplatz K, Wang Y. (1970): Shunts between the coronary and pulmonary arteries with normal origin of the coronary arteries. Am. J. Cardiol. 1970;25:655-61. doi: 10.1016/0002-9149(70)90615-6.\u003c/li\u003e\n\u003cli\u003eBaker RE, Schlipf JW, Scollan KF, LeBlanc NL, Russell DS, In-hospital development of an aorto-cardiac fistula in a Warmblood gelding with chronic renal disease. Equine Vet Educ. 2021;33:e86-e91.\u003c/li\u003e\n\u003cli\u003eBildfell RJ, Pringle JK, Miller LM. Coronary Arterioventricular Anomaly in a Calf. J Vet Diagn Invest. 1996;8:500-2. doi: 10.1177/104063879600800421. \u003c/li\u003e\n\u003cli\u003eMarr CM, Reef VB, Brazil TJ, Thomas WP, Knottenbelt DC, Kelly DF, Baker JR, Reimer JM, Maxson AD, Crowhurst JS. Aorto-cardiac fistulas in seven horses. Vet. Radiol. Ultrasound. 1998;39:22\u0026ndash;31.\u003c/li\u003e\n\u003cli\u003eSaid SA, Lam J, van der Werf T. Solitary coronary artery fistulas: a congenital anomaly in children and adults. A contemporary review. Congenit Heart Dis. 2006;1:63-76.\u003c/li\u003e\n\u003cli\u003eBlake RR, Longo M, Santarelli G, Liuti T, Martinez-Pereira Y. Coronary arteriovenous malformation in a dog with a complex arrhythmia and hypothyroidism. J Vet Cardiol. 2019;23:38-44. doi: 10.1016/j.jvc.2019.01.005. \u003c/li\u003e\n\u003cli\u003eGeunha K, Yewon J, Ho-Gyun J, Taekwon L, Kichang L, Hakyoung Y. Case report: Imaging features of aorta-right atrial tunnel in a dog using two-dimensional echocardiography and computed tomography. Front Vet Sci. 2023;10:1160390. doi: 10.3389/fvets.2023.1160390.\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"bmc-veterinary-research","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"","sideBox":"Learn more about [BMC Veterinary Research](http://bmcvetres.biomedcentral.com/)","snPcode":"12917","submissionUrl":"https://submission.nature.com/new-submission/12917/3?","title":"BMC Veterinary Research","twitterHandle":"@BMC_series","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"","lastPublishedDoi":"10.21203/rs.3.rs-3972957/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3972957/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"A vascular communication between the left coronary artery and the main pulmonary artery (coronary fistula) was diagnosed as an incidental finding in a 3-year-old female Tatran hound by echocardiography as part of preanesthetic evaluation. The history, clinical examination, and diagnostic imaging did not reveal evidence of trauma or endocarditis which could have led to this condition. Transthoracic echocardiography revealed dilation of the left coronary sinus secondary to an abnormal vessel shunting blood into the main pulmonary artery. Computed tomography confirmed this diagnosis. Coronary artery fistula is a very rare finding in human and animals. According to the authors, this is the first clinical case of a congenital fistula between the left coronary artery and the main pulmonary artery in a dog.","manuscriptTitle":"Left coronary artery to main pulmonary artery fistula in a dog","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-02-23 19:09:41","doi":"10.21203/rs.3.rs-3972957/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2024-09-11T14:58:23+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2024-05-03T20:32:03+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"136600708012725725161612600240094898757","date":"2024-04-30T03:21:08+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2024-04-17T02:48:23+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"d76a59e9-87fe-4ee2-9372-3b538f143dee","date":"2024-04-16T02:41:10+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2024-04-05T09:01:16+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"","date":"2024-03-06T06:03:24+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2024-02-22T06:18:01+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2024-02-22T06:18:00+00:00","index":"","fulltext":""},{"type":"submitted","content":"BMC Veterinary Research","date":"2024-02-20T14:04:57+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"bmc-veterinary-research","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"","sideBox":"Learn more about [BMC Veterinary Research](http://bmcvetres.biomedcentral.com/)","snPcode":"12917","submissionUrl":"https://submission.nature.com/new-submission/12917/3?","title":"BMC Veterinary Research","twitterHandle":"@BMC_series","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"aada6128-55bc-4e05-a629-d8ebadccc8b2","owner":[],"postedDate":"February 23rd, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2025-08-11T16:05:25+00:00","versionOfRecord":{"articleIdentity":"rs-3972957","link":"https://doi.org/10.1186/s12917-025-04730-y","journal":{"identity":"bmc-veterinary-research","isVorOnly":false,"title":"BMC Veterinary Research"},"publishedOn":"2025-08-04 15:57:00","publishedOnDateReadable":"August 4th, 2025"},"versionCreatedAt":"2024-02-23 19:09:41","video":"","vorDoi":"10.1186/s12917-025-04730-y","vorDoiUrl":"https://doi.org/10.1186/s12917-025-04730-y","workflowStages":[]},"version":"v1","identity":"rs-3972957","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3972957","identity":"rs-3972957","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}