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Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis
Journal of Veterinary Cardiology (2017)
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www.elsevier.com/locate/jvc
Case Report
Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis E.H. Chapel, DVM , B.A. Scansen, DVM, MS* Department of Clinical Sciences, The Ohio State University College of Veterinary Medicine, 601 Vernon L Tharp St., Columbus, OH 43210, USA Received 23 August 2016; received in revised form 5 December 2016; accepted 12 December 2016
KEYWORDS Vascular anomaly; Truncular aplasia; Catheterization; Interventional radiology; Canine
Abstract Two English bulldogs referred for interventional palliation of severe pulmonary valve stenosis were incidentally diagnosed with unilateral absence of an external jugular vein (left in one case, right in the other) by computed tomography and Doppler ultrasound. The right internal jugular vein also could not be visualized in the dog with absence of the left external jugular vein. Cervical venous anomalies can impact diagnostic or interventional venous catheterization procedures such as balloon pulmonary valvuloplasty. Additionally, absence of an external jugular vein may impact central venous catheter placement. Absence of an external jugular vein should be considered in dogs when the external jugular vein cannot be easily palpated. Ultrasound or computed tomography may help identify jugular venous anatomy and confirm anomalies. ª 2017 Elsevier B.V. All rights reserved.
Case 1 A 2eyear-old castrated, male English bulldog weighing 26.3 kg was presented to The Ohio State University Veterinary Medical Center for a second opinion of severe pulmonary valve stenosis (PS). * Corresponding author. E-mail address: [email protected] (B.A. Scansen).
Pertinent diagnostic tests performed three weeks prior to referral included an echocardiogram performed by a board-certified cardiologist, electrocardiography, thoracic radiographs, complete blood count, and serum biochemistry profile including a total thyroxine level. The echocardiographic report described thickened and immobile pulmonary valve leaflets with secondary severe right ventricular hypertrophy (RVH), moderate tricuspid regurgitation (TR), and right atrial enlargement
http://dx.doi.org/10.1016/j.jvc.2016.12.002 1760-2734/ª 2017 Elsevier B.V. All rights reserved.
Please cite this article in press as: Chapel EH, Scansen BA, Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis, Journal of Veterinary Cardiology (2017), http://dx.doi.org/10.1016/j.jvc.2016.12.002
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E.H. Chapel, B.A. Scansen Abbreviations BPV CTA EJV IJV PLCVC PS RAE RVH TR
balloon pulmonary valvuloplasty computed tomographic angiography external jugular vein internal jugular vein persistent left cranial vena cava pulmonary valve stenosis right atrial enlargement right ventricular hypertrophy tricuspid regurgitation
(RAE). Single lead electrocardiogram showed a supraventricular tachycardia with a rate of 260 beats per minute and prominent S waves in lead II. A single lateral thoracic radiograph, which was not available for review, was interpreted by the referring veterinarian as having a cranial mediastinal opacity obscuring the cranial margin of the heart
and unremarkable pulmonary parenchyma. All laboratory test results were within reference intervals. The dog was diagnosed with severe PS with right heart failure and subsequently prescribed enalapril (0.36mg/kg/day) and furosemide (2.8mg/kg/day). On presentation to The Ohio State University, the dog was overweight (body condition score of 4/5) with severe facial and ventral cervical swelling (Fig. 1). A grade III/VI systolic murmur was ausculted with the point of maximum intensity over the left heart base. The heart rhythm was irregular on auscultation with a rate of 90 per minute and the femoral pulse was also irregular and bilaterally synchronous. The remainder of the physical exam was unremarkable. A six-lead electrocardiogram was performed, documenting atrial fibrillation and a right axis deviation. Three-view thoracic radiographs again showed increased soft tissue opacity within the cranial mediastinum as well as RAE and right ventricular enlargement. The cranial mediastinum
Figure 1 Images from an English bulldog (case 1) with absence of the left EJV and pulmonary valve stenosis. Panel A: A volume-rendered 3-D reformatted image from a thoracic CT angiogram viewed from a ventral perspective showing a right EJV (arrows) with absence of the left EJV and a prominent left IJV (arrowheads) draining into the left brachiocephalic vein (*) and the cranial vena cava (#). The right auricular appendage (RAA) is markedly dilated and there is post-stenotic dilation of the pulmonary trunk (PT). R ¼ right side of dog; L ¼ left side of dog. Panel B: A volumerendered 3-D reformatted image from the same thoracic CT angiogram viewed from a left lateral perspective highlighting the ventral course of the right EJV (arrows) compared to the more dorsal course of the left IJV (arrowheads). Cranial is to the left of the image. Panel C: A photograph of case 1 showing severe cranioventral edema and facial swelling.
Please cite this article in press as: Chapel EH, Scansen BA, Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis, Journal of Veterinary Cardiology (2017), http://dx.doi.org/10.1016/j.jvc.2016.12.002
Absent external jugular vein in two dogs
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Figure 2 Cervical CT images from English bulldogs. Panel A: An axial CT angiographic image of the neck from a normal bulldog shows a right EJV (large black arrow), left EJV (large white arrow), right IJV (small black arrow), left IJV (small white arrow), right common carotid artery (black arrowhead), and left common carotid artery (white arrowhead). Panel B: An axial CT angiographic image from case 1 showing the same structures as in panel A, but with absence of the left EJV, dilation of the left IJV, and apparent absence of the right IJV. Panel C: An axial CT image from case 2 showing the same structures as in panel A, but with absence of the right EJV. R ¼ right side of each dog; L ¼ left side of each dog.
was widened on the dorsoventral images causing caudal displacement of the cranial lung lobes. Serosal detail of the cranial abdominal organs was normal as was liver size and shape. Two-dimensional echocardiography with Doppler studiesa were comparable to the prior report with severe PS (peak systolic pressure gradient of 112 mmHg) characterized by annular hypoplasia, severe RVH, moderate to severe TR, severe RAE with spontaneous echogenic contrast, and a single left coronary ostium. Due to the possibility of a cranial mediastinal mass and coronary anomaly, a computed tomographic angiography (CTA)b scan was performed prior to balloon pulmonary valvuloplasty (BPV). Axial images of the cervical region revealed edematous soft tissue with congestion of the deep and superficial lymph nodes; no discrete mass was present. The left external jugular vein (EJV) was absent (Figs. 1 and 2B). The left linguofacial and maxillary veins connected to a dilated left internal jugular vein (IJV), which had a normal position and directional course. The right EJV was present and normal in caliber, while the right IJV was unable to be visualized and presumed to be absent. Spatial resolution of the coronary arterial system was suboptimal; therefore, right ventriculography was planned for balloon sizing and to further assess the coronary circulation. Due to severe cervical swelling, the right femoral vein was utilized for right heart catheterization. During the levophase of the right ventriculogram, a single left coronary ostium with a prepulmonic right coronary artery circulation was
suspected. This coronary anatomy has been previously reported [1]. Due to the risk for coronary trauma, BPV was not performed and the dog recovered uneventfully from general anesthesia.
a Vivid 7 Dimension with EchoPAC software package, GE Healthcare, Waukesha, WI, USA. b GE Light Speed Ultra 8-slice CT, GE Healthcare, Waukesha, WI, USA.
c Vivid 9 with EchoPAC software package, GE Healthcare, Waukesha, WI, USA. d Definition Flash 128-slice dual-source CT, Siemens Healthcare, Forchheim, Germany.
Case 2 A 6-month-old intact, male English bulldog was presented to The Ohio State University Veterinary Medical Center for enrollment in a clinical trial for PS in the breed. The dog had been diagnosed with severe PS by a board-certified cardiologist three weeks prior to presentation. The dog was asymptomatic, was not receiving any medical therapy, and had no history of trauma. On presentation, a grade V/VI systolic murmur was ausculted with the point of maximum intensity over the left heart base. Echocardiographicc findings included severe PS (peak systolic pressure gradient of 170 mmHg) characterized by annular hypoplasia and leaflet tethering, severe RVH, mild TR, and mild RAE. A patent foramen ovale was detected on color Doppler imaging of the interatrial septum. As part of the clinical trial the dog underwent a CTA,d which confirmed the echocardiographic findings and demonstrated normal coronary artery origin and course. Evaluation of the cervical venous anatomy on a non-contrast helical scan revealed absence of the right EJV. As the neck was not scanned after contrast, determination of the IJV anatomy was challenging; however, both right and left IJVs appeared to be present (Fig. 2C). The dog recovered from general anesthesia uneventfully, was
Please cite this article in press as: Chapel EH, Scansen BA, Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis, Journal of Veterinary Cardiology (2017), http://dx.doi.org/10.1016/j.jvc.2016.12.002
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Figure 3 Ultrasonographic images of the right (A) and left (B) jugular furrows from case 2. In the right jugular furrow, no EJV could be visualized and the right IJV was prominent and nearly of equal diameter to the left EJV. Note the depth from the skin surface to the IJV as compared to the EJV. Measurements shown reflect the diameter of the right IJV in panel A and the left EJV in panel B.
prescribed atenolol (1.5mg/kg PO q12), and returned 1 month later for BPV. A cervical ultrasounde was performed using a 12 MHz linear transducer prior to the interventional procedure. Two-dimensional ultrasound with color flow and pulsed wave Doppler were used to scan the cervical region of the right and left jugular furrows from the thoracic inlet to the mandible to identify the carotid arteries, IJVs, and EJVs. In the left jugular furrow, the left EJV was visible as an easily compressible vessel ventral/ superficial and remote from the uncompressible carotid artery (Fig. 3). A small caliber and compressible left IJV was apparent adjacent to the left carotid artery. In the right jugular furrow, the right EJV could not be located with extensive scanning in both sagittal and transverse planes. The right IJV was visualized as a smaller caliber, easily compressible vessel adjacent to the right carotid artery. Unfortunately, the images showing the relationship of the IJV and EJV to each carotid artery were not archived appropriately; therefore, Figure 3 only demonstrates the relative position of each vein to the skin surface. The BPV procedure was successfully performed through percutaneous access of the left EJV without complication.
Discussion We describe two cases of congenital unilateral absence of an EJV, one with apparent absence of the contralateral IJV, in English bulldogs referred for transvenous intervention. The absence of an EJV impacts clinical decision making for venous access and this anomaly, to the authors’ e
Vivid q, GE Healthcare, Waukesha, WI, USA.
knowledge, has not previously been reported in a clinical canine patient. The EJVs are the primary vessels draining deoxygenated blood from the head in the dog. In this species, the EJV forms as the union of the linguofacial and maxillary veins. As the EJV courses caudally, it crosses the ventral surface of the sternocephalicus muscle just beneath the skin of the ventrolateral neck. At the point of the shoulder, the EJV receives the omobrachial, superficial cervical, and cephalic veins laterally and the much smaller IJV, medially [2]. The EJV terminates as it joins the subclavian vein to form the brachiocephalic vein. The IJVs arise in the tympanoocccipital fissure from the confluence of the petrosal and sigmoid sinuses and continue caudoventrally in close association with the internal and common carotid arteries, much deeper (dorsal and medial) than the ipsilateral EJVs [2]. The bilateral brachiocephalic, or innominate, veins then merge to form the rightward cranial vena cava [2]. This vascular pattern is conserved among most mammals with the notable exception of rodents and lagomorphs (rats, mice, hamsters, gerbils, rabbits), which have paired cranial vena cava [3]. In man, the EJV arises at the union of the posterior branch of the retromandibular vein (a union of the maxillary and superficial temporal veins) and the posterior auricular vein [4]. The IJV of humans is the dominant pathway for venous return from the head, with the size of the human IJV much larger than the ipsilateral EJV, while the opposite is true for most veterinary species. The embryologic formation and maturation of the venous system involves multiple stages of evolution and involution throughout embryogenesis. A complete description of cranial venous development is beyond the depth of this case report. In brief, the
Please cite this article in press as: Chapel EH, Scansen BA, Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis, Journal of Veterinary Cardiology (2017), http://dx.doi.org/10.1016/j.jvc.2016.12.002
Absent external jugular vein in two dogs EJVs arise independently from blood islands in the mandibular region. These irregular clusters of mesoderm expand, become fluid filled and eventually anastomose with bordering blood islands to form a plexus of communicating vessels which ultimately then fuse with the brachiocephalic veins. Conversely, the IJVs and brachiocephalic veins arise directly from the early-established anterior cardinal veins and their anastomoses [5]. The complex process of venous development is believed to be why venous malformations comprise two thirds of all vascular malformations in people [6]. A congenital vascular malformation is defined as an embryologically-developed, in-born error of vascular morphogenesis leading to structural anomalies [7]. Classification of vascular malformations in veterinary medicine currently relies on naming the absent, aberrant, or otherwise affected vessels and describing the changes in detail. There are several vascular malformation classification schemes in the human literature. One of the most frequently cited is the Hamburg classification [7], which was created to replace the many eponymous syndromes used in other classification schemes. This system accounts for the underlying anatomical, histological, and pathophysiological features of congenital vascular malformations and introduces embryological aspects, further subdividing malformations into either an extratruncular or truncular form, based upon the time of developmental arrest during embryonic life. Extratruncular refers to the web-like plexus of vessels that appear during early development, and truncular refers to an anomaly of a tubular, formed vessel. The two cases presented are examples of truncular venous aplasia of the EJV. Truncular venous aplasia can result in compensatory dilation of collateral veins, which can lead to chronic venous insufficiency and edema formation [8]. This, along with right heart failure, may account for the cranial edema formation in case 1 of this report. Truncular venous aplasia of the cervical venous system has been reported in humans and the cat [9e14]. In the feline case report, absence of the left EJV and both IJVs was incidentally diagnosed on a musculoskeletal computed tomography scan [9]. The majority of case reports in people come from anatomy departments at academic institutions reporting on anomalies found during cadaveric dissection [10e12]. There are, however, reports of antemortem diagnosis of absent IJV in people [13e15]. Since the IJV in people is larger in caliber than the EJV, it is often the site for central venous catheter placement or interventional venous catheterization and is therefore more clinically relevant to the human population.
5 Another cranial venous system anomaly that has been reported in dogs is a persistent left cranial vena cava [16]. This hemodynamically insignificant malformation becomes clinically relevant during cardiac interventional procedures as reported in dogs for pacemaker implantation, heartworm extraction, and atrial septal defect closure [17e19]. Utilizing the left EJV in the presence of a persistent left cranial vena cava (PLCVC), or the right EJV in cases with an absent right cranial vena cava, causes catheters, wires, or pacemaker leads to enter the heart via the coronary sinus located on the caudomedial aspect of the right atrium. With this approach, instrumentation entering through the coronary sinus courses cranial toward the right auricular appendage and an acute bend in instrumentation is necessary to cross the tricuspid valve for access to the right ventricle. The right cranial vena cava is present in approximately 90% of dogs and humans with a PLCVC [16]. A bridging vein between the right and left cranial vena cava is present in 60% of humans with PLCVC [20]. However, absence of the right cranial vena cava in the setting of PLCVC does occur, limiting transcatheter procedures [17,19]. Coronary sinus dilation detected on pre-procedural echocardiography is suggestive of PLCVC but not specific for this condition [21]. The definitive diagnosis of a PLCVC requires advanced diagnostics and the right cranial vena cava is rarely absent; as such, veterinary interventionalists typically catheterize the right EJV when central venous access is required. As shown in case 2 of this report, absence of this vein limits this approach and those that perform central venous catheterization through the right EJV should be aware of this anomaly. To the authors’ knowledge, the presented cases are the first reports of EJV aplasia in the dog. In Buchannan’s case series of dogs with a PLCVC [16], there is a brief mention of a Boston Terrier in which catheterization of the left EJV was performed because the operator failed to locate the right EJV after ‘extensive dissection’. The authors are aware of other anecdotal cases in which the desired EJV could not be identified after prolonged dissection. Whether unsuccessful isolation of the EJV in these instances represented truncular venous aplasia of the vessel remains unknown. The diagnosis of cervical venous anomalies can be made with a variety of imaging modalities including CTA, MRI, ultrasound, and both selective and non-selective fluoroscopic angiography. While CTA or MRI remain the gold standard diagnostic tests for characterization of vascular anomalies, their limited availability, cost, and need for general anesthesia are excessive for the detection of an absent EJV. Ultrasound, while providing
Please cite this article in press as: Chapel EH, Scansen BA, Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis, Journal of Veterinary Cardiology (2017), http://dx.doi.org/10.1016/j.jvc.2016.12.002
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significantly less detailed information regarding vascular branching patterns and vessel course, can provide a simple ‘yes or no’ answer to the presence of a superficial cervical vessel such as the EJV. In pediatric medicine, it has been recommended to perform cervical ultrasound prior to IJV catheterization to limit undue patient stress, procedural time, and complications [14]. In veterinary medicine, the EJV is typically located with simple palpation and digital venous occlusion. Identifying the EJV in this manner can be challenging in overweight animals, those with excessive cervical skin folds, or with cervical edema and swelling. In these patients, cervical ultrasound may aid in identification of this vessel. In addition to truncal venous aplasia, causes of absence of the EJV include previous trauma and thrombosis of the vessel or previous ligation of the vessel. Previous thrombosis is often accompanied by recruitment of collateral circulation [21], which was not a finding in the presented cases. Neither of the two cases had a history of jugular venous instrumentation. Inability to locate the EJV on palpation or ultrasound should prompt the clinician to review the patient’s medical history to determine if a previous surgical or interventional procedure or trauma has occurred. If not, truncal aplasia of the EJV should be considered. Interventionalists should be aware of both the normal anatomy and variations of venous drainage when accessing the vasculature for any reason. With the growing prevalence of interventional venous procedures and central venous catheter placement, absence of the EJV should be a consideration when it is not readily palpated. We now routinely perform cervical ultrasounds prior to central venous catheterization in dogs and have identified one more dog (a Jack Russell Terrier) with absence of an EJV.
Conflicts of Interest Statement The authors do not have any conflicts of interest to disclose.
References [1] Visser LC, Scansen BA, Schober KE. Single left coronary ostium and an anomalous prepulmonic right coronary artery in 2 dogs with congenital pulmonic valve stenosis. J Vet Cardiol 2013;15:161e9.
[2] Bezuidenhout AJ. Veins. In: Evans HE, de Lahunta A, editors. Miller’s Anatomy of the Dog. St. Louis: Elsevier Saunders; 2013. p. 505e34. [3] O’Farrell L, Griffith J. Comparative anatomy of the cranial vena cava in laboratory animals. Lab Anim Sci 1996;46:448e9. [4] Standring S. Grey’s anatomy, the anatomical basis of clinical practice. 40th ed. St. Louis: Elsevier; 2009. [5] Avery LB. Developmental anatomy. revised 7th ed. Philadelphia: WB Saunders; 1974. [6] Eifert S, Villacicencio J, Kao T, Taute B, Rich N. Prevalence of deep venous anomalies in congenital vascular malformations of venous predominance. J Vasc Surg 2000;31:462e71. [7] Mulliken J, Glowacki J. Hemangiomas and vascular malformations in infants and children: a classification based on endothelial characteristics. Plast Reconstr Surg 1982;69:412e20. [8] Lee BB, Bergan J, Gloviczki P, Laredo J, Loose DA, Mattassi R, Parsi K, Villavicencio JL, Zamboni P. Diagnosis and treatment of venous malformations. Consensus document of the International Union of Phlebology (IUP)-2009. Int Angiol 2009;28:434e51. [9] Giovanna B, Zotti A. Imaging diagnosis: absence of the left external and both internal jugular veins in a cat. Vet Radiol Ultrasound 2006;47:468e9. [10] Patil RA, Rajgopal L, Iyer P. Absent external jugular vein e ontogeny and clinical implications. Int J Anat Var 2013;6: 103e5. [11] Abhinitha P, Rao MKG, Kumar N, Nayak SB, Ravindra SS, Aithal PA. Absence of the external jugular vein and an abnormal drainage pattern in the veins of the neck. OA Anat 2013;1:15. [12] Chauhan NK, Rani A, Chopra J, Rani A, Srivastava AK, Kumar V. Anomalous formation of external jugular vein and its clinical implication. Natl J Maxillofac Surg 2011;2:51e3. [13] Kayiran O, Calli C, Emre A, Soy FK. Congenital agenesis of the internal jugular vein: an extremely rare anomaly. Case Rep Surg 2015;2015:637067. [14] Miller BR. Absence of a right internal jugular vein detected by ultrasound imaging. Paediatr Anaesth 2011;21:91. [15] Alago ¸ M, Sazak H, Pehlivanoglu P, Go ¸ek A, Ulus F. ¨z A, Tunc ¨kc Absence of the right internal jugular vein during ultrasound guided cannulation. Truk J Anesthesiol Reanim 2015;43:212e4. [16] Buchanan J. Persistent left cranial vena cava in dogs: angiography, significance, and coexisting anomalies. Am J Vet Radiol Soc 1963;4:1e8. [17] Venco L, Kramer L, Genchi C. Heartworm disease in dogs: unusual clinical cases. Vet Parasitol 2005;133:207e18. [18] Cunningham S, Rush J. Transvenous pacemaker placement in a dog with atrioventricular block and persistent left cranial vena cava. J Vet Cardiol 2007;9:129e34. [19] Gordon SG, Miller MW, Roland RM, Saunders AB, Achen SE, Drourr LT, Nelson DA. Transcatheter atrial septal defect closure with Amplatzer atrial septal occluder in 13 dogs: shortand mid-term outcome. J Vet Intern Med 2009;23:995e1002. [20] Waikar HD, Lahie YKM, Zoysa LD, Chand P, Kamalanesan RPP. Systemic venous anomalies: absent right superior vena cava with persistent left superior vena cava. J Cardiothorac Vasc Anesth 2004;18:332. [21] Lawler LP, Corl FM, Fishman EK. Multi-detector row and volume-rendered CT of the normal and accessory flow pathways of the thoracic systemic and pulmonary veins. Radiographics 2002;22:S45e60.
Available online at www.sciencedirect.com
ScienceDirect Please cite this article in press as: Chapel EH, Scansen BA, Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis, Journal of Veterinary Cardiology (2017), http://dx.doi.org/10.1016/j.jvc.2016.12.002
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www.elsevier.com/locate/jvc
Case Report
Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis E.H. Chapel, DVM , B.A. Scansen, DVM, MS* Department of Clinical Sciences, The Ohio State University College of Veterinary Medicine, 601 Vernon L Tharp St., Columbus, OH 43210, USA Received 23 August 2016; received in revised form 5 December 2016; accepted 12 December 2016
KEYWORDS Vascular anomaly; Truncular aplasia; Catheterization; Interventional radiology; Canine
Abstract Two English bulldogs referred for interventional palliation of severe pulmonary valve stenosis were incidentally diagnosed with unilateral absence of an external jugular vein (left in one case, right in the other) by computed tomography and Doppler ultrasound. The right internal jugular vein also could not be visualized in the dog with absence of the left external jugular vein. Cervical venous anomalies can impact diagnostic or interventional venous catheterization procedures such as balloon pulmonary valvuloplasty. Additionally, absence of an external jugular vein may impact central venous catheter placement. Absence of an external jugular vein should be considered in dogs when the external jugular vein cannot be easily palpated. Ultrasound or computed tomography may help identify jugular venous anatomy and confirm anomalies. ª 2017 Elsevier B.V. All rights reserved.
Case 1 A 2eyear-old castrated, male English bulldog weighing 26.3 kg was presented to The Ohio State University Veterinary Medical Center for a second opinion of severe pulmonary valve stenosis (PS). * Corresponding author. E-mail address: [email protected] (B.A. Scansen).
Pertinent diagnostic tests performed three weeks prior to referral included an echocardiogram performed by a board-certified cardiologist, electrocardiography, thoracic radiographs, complete blood count, and serum biochemistry profile including a total thyroxine level. The echocardiographic report described thickened and immobile pulmonary valve leaflets with secondary severe right ventricular hypertrophy (RVH), moderate tricuspid regurgitation (TR), and right atrial enlargement
http://dx.doi.org/10.1016/j.jvc.2016.12.002 1760-2734/ª 2017 Elsevier B.V. All rights reserved.
Please cite this article in press as: Chapel EH, Scansen BA, Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis, Journal of Veterinary Cardiology (2017), http://dx.doi.org/10.1016/j.jvc.2016.12.002
2
E.H. Chapel, B.A. Scansen Abbreviations BPV CTA EJV IJV PLCVC PS RAE RVH TR
balloon pulmonary valvuloplasty computed tomographic angiography external jugular vein internal jugular vein persistent left cranial vena cava pulmonary valve stenosis right atrial enlargement right ventricular hypertrophy tricuspid regurgitation
(RAE). Single lead electrocardiogram showed a supraventricular tachycardia with a rate of 260 beats per minute and prominent S waves in lead II. A single lateral thoracic radiograph, which was not available for review, was interpreted by the referring veterinarian as having a cranial mediastinal opacity obscuring the cranial margin of the heart
and unremarkable pulmonary parenchyma. All laboratory test results were within reference intervals. The dog was diagnosed with severe PS with right heart failure and subsequently prescribed enalapril (0.36mg/kg/day) and furosemide (2.8mg/kg/day). On presentation to The Ohio State University, the dog was overweight (body condition score of 4/5) with severe facial and ventral cervical swelling (Fig. 1). A grade III/VI systolic murmur was ausculted with the point of maximum intensity over the left heart base. The heart rhythm was irregular on auscultation with a rate of 90 per minute and the femoral pulse was also irregular and bilaterally synchronous. The remainder of the physical exam was unremarkable. A six-lead electrocardiogram was performed, documenting atrial fibrillation and a right axis deviation. Three-view thoracic radiographs again showed increased soft tissue opacity within the cranial mediastinum as well as RAE and right ventricular enlargement. The cranial mediastinum
Figure 1 Images from an English bulldog (case 1) with absence of the left EJV and pulmonary valve stenosis. Panel A: A volume-rendered 3-D reformatted image from a thoracic CT angiogram viewed from a ventral perspective showing a right EJV (arrows) with absence of the left EJV and a prominent left IJV (arrowheads) draining into the left brachiocephalic vein (*) and the cranial vena cava (#). The right auricular appendage (RAA) is markedly dilated and there is post-stenotic dilation of the pulmonary trunk (PT). R ¼ right side of dog; L ¼ left side of dog. Panel B: A volumerendered 3-D reformatted image from the same thoracic CT angiogram viewed from a left lateral perspective highlighting the ventral course of the right EJV (arrows) compared to the more dorsal course of the left IJV (arrowheads). Cranial is to the left of the image. Panel C: A photograph of case 1 showing severe cranioventral edema and facial swelling.
Please cite this article in press as: Chapel EH, Scansen BA, Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis, Journal of Veterinary Cardiology (2017), http://dx.doi.org/10.1016/j.jvc.2016.12.002
Absent external jugular vein in two dogs
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Figure 2 Cervical CT images from English bulldogs. Panel A: An axial CT angiographic image of the neck from a normal bulldog shows a right EJV (large black arrow), left EJV (large white arrow), right IJV (small black arrow), left IJV (small white arrow), right common carotid artery (black arrowhead), and left common carotid artery (white arrowhead). Panel B: An axial CT angiographic image from case 1 showing the same structures as in panel A, but with absence of the left EJV, dilation of the left IJV, and apparent absence of the right IJV. Panel C: An axial CT image from case 2 showing the same structures as in panel A, but with absence of the right EJV. R ¼ right side of each dog; L ¼ left side of each dog.
was widened on the dorsoventral images causing caudal displacement of the cranial lung lobes. Serosal detail of the cranial abdominal organs was normal as was liver size and shape. Two-dimensional echocardiography with Doppler studiesa were comparable to the prior report with severe PS (peak systolic pressure gradient of 112 mmHg) characterized by annular hypoplasia, severe RVH, moderate to severe TR, severe RAE with spontaneous echogenic contrast, and a single left coronary ostium. Due to the possibility of a cranial mediastinal mass and coronary anomaly, a computed tomographic angiography (CTA)b scan was performed prior to balloon pulmonary valvuloplasty (BPV). Axial images of the cervical region revealed edematous soft tissue with congestion of the deep and superficial lymph nodes; no discrete mass was present. The left external jugular vein (EJV) was absent (Figs. 1 and 2B). The left linguofacial and maxillary veins connected to a dilated left internal jugular vein (IJV), which had a normal position and directional course. The right EJV was present and normal in caliber, while the right IJV was unable to be visualized and presumed to be absent. Spatial resolution of the coronary arterial system was suboptimal; therefore, right ventriculography was planned for balloon sizing and to further assess the coronary circulation. Due to severe cervical swelling, the right femoral vein was utilized for right heart catheterization. During the levophase of the right ventriculogram, a single left coronary ostium with a prepulmonic right coronary artery circulation was
suspected. This coronary anatomy has been previously reported [1]. Due to the risk for coronary trauma, BPV was not performed and the dog recovered uneventfully from general anesthesia.
a Vivid 7 Dimension with EchoPAC software package, GE Healthcare, Waukesha, WI, USA. b GE Light Speed Ultra 8-slice CT, GE Healthcare, Waukesha, WI, USA.
c Vivid 9 with EchoPAC software package, GE Healthcare, Waukesha, WI, USA. d Definition Flash 128-slice dual-source CT, Siemens Healthcare, Forchheim, Germany.
Case 2 A 6-month-old intact, male English bulldog was presented to The Ohio State University Veterinary Medical Center for enrollment in a clinical trial for PS in the breed. The dog had been diagnosed with severe PS by a board-certified cardiologist three weeks prior to presentation. The dog was asymptomatic, was not receiving any medical therapy, and had no history of trauma. On presentation, a grade V/VI systolic murmur was ausculted with the point of maximum intensity over the left heart base. Echocardiographicc findings included severe PS (peak systolic pressure gradient of 170 mmHg) characterized by annular hypoplasia and leaflet tethering, severe RVH, mild TR, and mild RAE. A patent foramen ovale was detected on color Doppler imaging of the interatrial septum. As part of the clinical trial the dog underwent a CTA,d which confirmed the echocardiographic findings and demonstrated normal coronary artery origin and course. Evaluation of the cervical venous anatomy on a non-contrast helical scan revealed absence of the right EJV. As the neck was not scanned after contrast, determination of the IJV anatomy was challenging; however, both right and left IJVs appeared to be present (Fig. 2C). The dog recovered from general anesthesia uneventfully, was
Please cite this article in press as: Chapel EH, Scansen BA, Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis, Journal of Veterinary Cardiology (2017), http://dx.doi.org/10.1016/j.jvc.2016.12.002
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E.H. Chapel, B.A. Scansen
Figure 3 Ultrasonographic images of the right (A) and left (B) jugular furrows from case 2. In the right jugular furrow, no EJV could be visualized and the right IJV was prominent and nearly of equal diameter to the left EJV. Note the depth from the skin surface to the IJV as compared to the EJV. Measurements shown reflect the diameter of the right IJV in panel A and the left EJV in panel B.
prescribed atenolol (1.5mg/kg PO q12), and returned 1 month later for BPV. A cervical ultrasounde was performed using a 12 MHz linear transducer prior to the interventional procedure. Two-dimensional ultrasound with color flow and pulsed wave Doppler were used to scan the cervical region of the right and left jugular furrows from the thoracic inlet to the mandible to identify the carotid arteries, IJVs, and EJVs. In the left jugular furrow, the left EJV was visible as an easily compressible vessel ventral/ superficial and remote from the uncompressible carotid artery (Fig. 3). A small caliber and compressible left IJV was apparent adjacent to the left carotid artery. In the right jugular furrow, the right EJV could not be located with extensive scanning in both sagittal and transverse planes. The right IJV was visualized as a smaller caliber, easily compressible vessel adjacent to the right carotid artery. Unfortunately, the images showing the relationship of the IJV and EJV to each carotid artery were not archived appropriately; therefore, Figure 3 only demonstrates the relative position of each vein to the skin surface. The BPV procedure was successfully performed through percutaneous access of the left EJV without complication.
Discussion We describe two cases of congenital unilateral absence of an EJV, one with apparent absence of the contralateral IJV, in English bulldogs referred for transvenous intervention. The absence of an EJV impacts clinical decision making for venous access and this anomaly, to the authors’ e
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knowledge, has not previously been reported in a clinical canine patient. The EJVs are the primary vessels draining deoxygenated blood from the head in the dog. In this species, the EJV forms as the union of the linguofacial and maxillary veins. As the EJV courses caudally, it crosses the ventral surface of the sternocephalicus muscle just beneath the skin of the ventrolateral neck. At the point of the shoulder, the EJV receives the omobrachial, superficial cervical, and cephalic veins laterally and the much smaller IJV, medially [2]. The EJV terminates as it joins the subclavian vein to form the brachiocephalic vein. The IJVs arise in the tympanoocccipital fissure from the confluence of the petrosal and sigmoid sinuses and continue caudoventrally in close association with the internal and common carotid arteries, much deeper (dorsal and medial) than the ipsilateral EJVs [2]. The bilateral brachiocephalic, or innominate, veins then merge to form the rightward cranial vena cava [2]. This vascular pattern is conserved among most mammals with the notable exception of rodents and lagomorphs (rats, mice, hamsters, gerbils, rabbits), which have paired cranial vena cava [3]. In man, the EJV arises at the union of the posterior branch of the retromandibular vein (a union of the maxillary and superficial temporal veins) and the posterior auricular vein [4]. The IJV of humans is the dominant pathway for venous return from the head, with the size of the human IJV much larger than the ipsilateral EJV, while the opposite is true for most veterinary species. The embryologic formation and maturation of the venous system involves multiple stages of evolution and involution throughout embryogenesis. A complete description of cranial venous development is beyond the depth of this case report. In brief, the
Please cite this article in press as: Chapel EH, Scansen BA, Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis, Journal of Veterinary Cardiology (2017), http://dx.doi.org/10.1016/j.jvc.2016.12.002
Absent external jugular vein in two dogs EJVs arise independently from blood islands in the mandibular region. These irregular clusters of mesoderm expand, become fluid filled and eventually anastomose with bordering blood islands to form a plexus of communicating vessels which ultimately then fuse with the brachiocephalic veins. Conversely, the IJVs and brachiocephalic veins arise directly from the early-established anterior cardinal veins and their anastomoses [5]. The complex process of venous development is believed to be why venous malformations comprise two thirds of all vascular malformations in people [6]. A congenital vascular malformation is defined as an embryologically-developed, in-born error of vascular morphogenesis leading to structural anomalies [7]. Classification of vascular malformations in veterinary medicine currently relies on naming the absent, aberrant, or otherwise affected vessels and describing the changes in detail. There are several vascular malformation classification schemes in the human literature. One of the most frequently cited is the Hamburg classification [7], which was created to replace the many eponymous syndromes used in other classification schemes. This system accounts for the underlying anatomical, histological, and pathophysiological features of congenital vascular malformations and introduces embryological aspects, further subdividing malformations into either an extratruncular or truncular form, based upon the time of developmental arrest during embryonic life. Extratruncular refers to the web-like plexus of vessels that appear during early development, and truncular refers to an anomaly of a tubular, formed vessel. The two cases presented are examples of truncular venous aplasia of the EJV. Truncular venous aplasia can result in compensatory dilation of collateral veins, which can lead to chronic venous insufficiency and edema formation [8]. This, along with right heart failure, may account for the cranial edema formation in case 1 of this report. Truncular venous aplasia of the cervical venous system has been reported in humans and the cat [9e14]. In the feline case report, absence of the left EJV and both IJVs was incidentally diagnosed on a musculoskeletal computed tomography scan [9]. The majority of case reports in people come from anatomy departments at academic institutions reporting on anomalies found during cadaveric dissection [10e12]. There are, however, reports of antemortem diagnosis of absent IJV in people [13e15]. Since the IJV in people is larger in caliber than the EJV, it is often the site for central venous catheter placement or interventional venous catheterization and is therefore more clinically relevant to the human population.
5 Another cranial venous system anomaly that has been reported in dogs is a persistent left cranial vena cava [16]. This hemodynamically insignificant malformation becomes clinically relevant during cardiac interventional procedures as reported in dogs for pacemaker implantation, heartworm extraction, and atrial septal defect closure [17e19]. Utilizing the left EJV in the presence of a persistent left cranial vena cava (PLCVC), or the right EJV in cases with an absent right cranial vena cava, causes catheters, wires, or pacemaker leads to enter the heart via the coronary sinus located on the caudomedial aspect of the right atrium. With this approach, instrumentation entering through the coronary sinus courses cranial toward the right auricular appendage and an acute bend in instrumentation is necessary to cross the tricuspid valve for access to the right ventricle. The right cranial vena cava is present in approximately 90% of dogs and humans with a PLCVC [16]. A bridging vein between the right and left cranial vena cava is present in 60% of humans with PLCVC [20]. However, absence of the right cranial vena cava in the setting of PLCVC does occur, limiting transcatheter procedures [17,19]. Coronary sinus dilation detected on pre-procedural echocardiography is suggestive of PLCVC but not specific for this condition [21]. The definitive diagnosis of a PLCVC requires advanced diagnostics and the right cranial vena cava is rarely absent; as such, veterinary interventionalists typically catheterize the right EJV when central venous access is required. As shown in case 2 of this report, absence of this vein limits this approach and those that perform central venous catheterization through the right EJV should be aware of this anomaly. To the authors’ knowledge, the presented cases are the first reports of EJV aplasia in the dog. In Buchannan’s case series of dogs with a PLCVC [16], there is a brief mention of a Boston Terrier in which catheterization of the left EJV was performed because the operator failed to locate the right EJV after ‘extensive dissection’. The authors are aware of other anecdotal cases in which the desired EJV could not be identified after prolonged dissection. Whether unsuccessful isolation of the EJV in these instances represented truncular venous aplasia of the vessel remains unknown. The diagnosis of cervical venous anomalies can be made with a variety of imaging modalities including CTA, MRI, ultrasound, and both selective and non-selective fluoroscopic angiography. While CTA or MRI remain the gold standard diagnostic tests for characterization of vascular anomalies, their limited availability, cost, and need for general anesthesia are excessive for the detection of an absent EJV. Ultrasound, while providing
Please cite this article in press as: Chapel EH, Scansen BA, Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis, Journal of Veterinary Cardiology (2017), http://dx.doi.org/10.1016/j.jvc.2016.12.002
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significantly less detailed information regarding vascular branching patterns and vessel course, can provide a simple ‘yes or no’ answer to the presence of a superficial cervical vessel such as the EJV. In pediatric medicine, it has been recommended to perform cervical ultrasound prior to IJV catheterization to limit undue patient stress, procedural time, and complications [14]. In veterinary medicine, the EJV is typically located with simple palpation and digital venous occlusion. Identifying the EJV in this manner can be challenging in overweight animals, those with excessive cervical skin folds, or with cervical edema and swelling. In these patients, cervical ultrasound may aid in identification of this vessel. In addition to truncal venous aplasia, causes of absence of the EJV include previous trauma and thrombosis of the vessel or previous ligation of the vessel. Previous thrombosis is often accompanied by recruitment of collateral circulation [21], which was not a finding in the presented cases. Neither of the two cases had a history of jugular venous instrumentation. Inability to locate the EJV on palpation or ultrasound should prompt the clinician to review the patient’s medical history to determine if a previous surgical or interventional procedure or trauma has occurred. If not, truncal aplasia of the EJV should be considered. Interventionalists should be aware of both the normal anatomy and variations of venous drainage when accessing the vasculature for any reason. With the growing prevalence of interventional venous procedures and central venous catheter placement, absence of the EJV should be a consideration when it is not readily palpated. We now routinely perform cervical ultrasounds prior to central venous catheterization in dogs and have identified one more dog (a Jack Russell Terrier) with absence of an EJV.
Conflicts of Interest Statement The authors do not have any conflicts of interest to disclose.
References [1] Visser LC, Scansen BA, Schober KE. Single left coronary ostium and an anomalous prepulmonic right coronary artery in 2 dogs with congenital pulmonic valve stenosis. J Vet Cardiol 2013;15:161e9.
[2] Bezuidenhout AJ. Veins. In: Evans HE, de Lahunta A, editors. Miller’s Anatomy of the Dog. St. Louis: Elsevier Saunders; 2013. p. 505e34. [3] O’Farrell L, Griffith J. Comparative anatomy of the cranial vena cava in laboratory animals. Lab Anim Sci 1996;46:448e9. [4] Standring S. Grey’s anatomy, the anatomical basis of clinical practice. 40th ed. St. Louis: Elsevier; 2009. [5] Avery LB. Developmental anatomy. revised 7th ed. Philadelphia: WB Saunders; 1974. [6] Eifert S, Villacicencio J, Kao T, Taute B, Rich N. Prevalence of deep venous anomalies in congenital vascular malformations of venous predominance. J Vasc Surg 2000;31:462e71. [7] Mulliken J, Glowacki J. Hemangiomas and vascular malformations in infants and children: a classification based on endothelial characteristics. Plast Reconstr Surg 1982;69:412e20. [8] Lee BB, Bergan J, Gloviczki P, Laredo J, Loose DA, Mattassi R, Parsi K, Villavicencio JL, Zamboni P. Diagnosis and treatment of venous malformations. Consensus document of the International Union of Phlebology (IUP)-2009. Int Angiol 2009;28:434e51. [9] Giovanna B, Zotti A. Imaging diagnosis: absence of the left external and both internal jugular veins in a cat. Vet Radiol Ultrasound 2006;47:468e9. [10] Patil RA, Rajgopal L, Iyer P. Absent external jugular vein e ontogeny and clinical implications. Int J Anat Var 2013;6: 103e5. [11] Abhinitha P, Rao MKG, Kumar N, Nayak SB, Ravindra SS, Aithal PA. Absence of the external jugular vein and an abnormal drainage pattern in the veins of the neck. OA Anat 2013;1:15. [12] Chauhan NK, Rani A, Chopra J, Rani A, Srivastava AK, Kumar V. Anomalous formation of external jugular vein and its clinical implication. Natl J Maxillofac Surg 2011;2:51e3. [13] Kayiran O, Calli C, Emre A, Soy FK. Congenital agenesis of the internal jugular vein: an extremely rare anomaly. Case Rep Surg 2015;2015:637067. [14] Miller BR. Absence of a right internal jugular vein detected by ultrasound imaging. Paediatr Anaesth 2011;21:91. [15] Alago ¸ M, Sazak H, Pehlivanoglu P, Go ¸ek A, Ulus F. ¨z A, Tunc ¨kc Absence of the right internal jugular vein during ultrasound guided cannulation. Truk J Anesthesiol Reanim 2015;43:212e4. [16] Buchanan J. Persistent left cranial vena cava in dogs: angiography, significance, and coexisting anomalies. Am J Vet Radiol Soc 1963;4:1e8. [17] Venco L, Kramer L, Genchi C. Heartworm disease in dogs: unusual clinical cases. Vet Parasitol 2005;133:207e18. [18] Cunningham S, Rush J. Transvenous pacemaker placement in a dog with atrioventricular block and persistent left cranial vena cava. J Vet Cardiol 2007;9:129e34. [19] Gordon SG, Miller MW, Roland RM, Saunders AB, Achen SE, Drourr LT, Nelson DA. Transcatheter atrial septal defect closure with Amplatzer atrial septal occluder in 13 dogs: shortand mid-term outcome. J Vet Intern Med 2009;23:995e1002. [20] Waikar HD, Lahie YKM, Zoysa LD, Chand P, Kamalanesan RPP. Systemic venous anomalies: absent right superior vena cava with persistent left superior vena cava. J Cardiothorac Vasc Anesth 2004;18:332. [21] Lawler LP, Corl FM, Fishman EK. Multi-detector row and volume-rendered CT of the normal and accessory flow pathways of the thoracic systemic and pulmonary veins. Radiographics 2002;22:S45e60.
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ScienceDirect Please cite this article in press as: Chapel EH, Scansen BA, Unilateral absence of an external jugular vein in two English bulldogs with pulmonary valve stenosis, Journal of Veterinary Cardiology (2017), http://dx.doi.org/10.1016/j.jvc.2016.12.002