The functional vascular anatomy of the swine for research

Abstract

Objectives

Swine (Sus Scrofa) are utilized broadly in research settings, given similarities to human vessel size and function; however, there are some important differences for clinicians to understand in order to interpret and perform translational research. This review article uses angiograms acquired in the course of a translational research program to present a description of the functional anatomy of the swine.

Methods

Digital subtraction angiography and computed tomography angiography were obtained throughout the course of multiple studies utilizing power injection with iodinated contrast. Subtracted two-dimensional images and three-dimensional multiplanar reformations were utilized post image acquisition to create maximal intensity projections and three-dimensional renderings of using open-source software (OsiriX). These imaging data are presented along with vessel measurements for reference.

Results

An atlas highlighting swine vascular anatomy, with an emphasis on inter-species differences that may influence how studies are conducted and interpreted, was compiled.

Conclusions

Swine are utilized in broad-reaching fields for preclinical research. While many similarities between human and swine vasculature exist, there are important differences to consider when conducting and interpreting research. This review article highlights these differences and presents accompanying images to inform clinicians gaining experience in swine research.

Keywords

Vascular anatomy swine anatomy porcine anatomy vascular atlas pig vasculature pig anatomy

Introduction

Endovascular therapy has gained acceptance as a critical tool in a number of disease processes, spanning surgical and interventional radiological fields.^1–3 In the current climate of rapid medical device development, it is imperative to have appropriate in vivo animal models to subject potentially harmful therapies to rigorous scientific testing. Development and understanding of the appropriate animal models require a basic understanding of the anatomical and functional differences between the species. The objective of this paper is to present the anatomical differences between swine and humans from an endovascular perspective using digital subtraction angiography (DSA) and computed tomographic angiography (CTA), and to explore the influence of these anatomical differences on research using endovascular therapies.

The first aim of this work is to inform researchers in the field on important features of porcine vascular anatomy that may provide advantages and/or challenges to proposed research. The second aim is to educate clinicians with limited large-animal research experience on swine anatomy so that data derived from preclinical porcine studies can be appropriately interpreted. The collection of the included figures also represents a concise, but broad anatomical atlas of swine vascular anatomy.

Porcine overview

Sus scrofa domestica, otherwise known as domestic swine, are utilized commonly in a variety of research settings, given similarities in gross anatomy and size.^4,5 From a functional standpoint, swine cardiovascular, digestive, dermal, and urinary processes are comparable to humans.⁶ In particular, the swine cardiovascular system has been used frequently in preclinical research given the similar ratio of heart to body weight (5 g/kg in ∼30 kg pigs), structure of chambers and valves, and lack of preexisting collateral epicardial circulation seen in other species such as dogs.⁷ Thus, porcine models exhibit remarkable potential for a broad range of medical and surgical research.

Despite the similarities, there are important differences, as swine represent a quadruped species, while humans exhibit a biped stance⁷ (see Figure 1(a)). One significant difference is the orientation of the front of the face, as the snout of a pig represents the apex of the axial plane, whereas the face in humans is oriented 90° with respect to axial plane. In addition, swine have a cone-shaped chest cavity which is laterally compressed with a central and anteriorly located heart, whereas humans have a dorso-ventrally compressed chest cavity (see Figure 1(b)). An additional aspect of the swine vasculature is the preferential perfusion of soft tissue given the muscular build of the pig, most notably demonstrated by the relative size of the vessels of the common carotid bifurcation, which will be described in detail below. Finally, although swine can develop atherosclerotic lesions, this occurs at a more advanced age than what is typically used in laboratory settings.⁸

Figure 1.

(a) Anatomical planes of a quadruped animal such as the swine. Note how the front of the face in CT scans is sliced in the axial plane, whereas the front of the face in humans is sliced in a coronal plane.⁹ (b) Three-dimensional rendering of the chest cavity of swine with prominent lateral compression and anterior/central location of heart. Abbrebviations: CeA = celiac artery; dAo = descending aorta; SMA = superior mesenteric artery.

While domestic farm breeds, such as the Yorkshire, are commonly utilized, miniature swine, such as the Hanford and Gottingen are being increasingly used in longer term studies,⁶ as they exhibit physiological maturity at smaller sizes compared to common farm pigs. Minipigs have also been shown to be more resilient to experimental protocol.¹⁰ The upkeep of minipigs is more cost-effective than that of standard farm breeds. This is primarily due to the tremendous ability of the traditional farm pig to gain weight over time, between 0.5 and 1 kg per day.¹¹

Vascular imaging overview

Although the knowledge of image acquisition in human clinical practice is of value, there are important differences to consider when performing vascular imaging procedures with swine. In the laboratory setting, imaging is carried out while the animal is under general anesthesia. In our experience, swine are quite hyperdynamic under inhalant anesthesia and thus, when performing DSA studies of central vessels, an increased frame rate, a longer duration of contrast bolus administration, or pharmacologic therapy to alter hemodynamics may be necessary to acquire a quality image with sufficient contrast. An additional challenge with DSA is the relatively long porcine torso (see Figure 1(b)) which limits the length of vasculature visible, especially when magnification is needed. The relatively long torso may also affect CTA acquisition, depending on the computed tomography (CT) speed, where arterial contrast studies over large cranial–caudal distances may be contaminated with venous contrast.

Although swine tolerate large contrast boluses, we have found that when given intra-arterial iodinated contrast in standard preparations, contrast loads exceeding 300 ml in the span of 6–8 h may result in contrast overload. Circulating blood can demonstrate Hounsfield attenuation in excess of 100 units, limiting CT acquisition.

Our laboratory performs endovascular procedures/imaging primarily through ultrasound-guided percutaneous cannulation utilizing modified Seldinger technique. For arterial access, we utilize 21-gauge micropuncture needles with 0.018″ wires, with subsequent upsizing, utilizing 0.035″ wires and 5–7 French (Fr) sheaths in most arteries. For venous access, micropuncture needles and wires can be utilized, but cannulation can be performed with 18-gauge vascular access needles and 0.035″ wires. Further detail on percutaneous technique will be discussed in the subsequent sections, as there are nuances to each access point that should be considered prior to vessel cannulation.

Chest

Given the shape of the porcine chest, the anterior position of the heart necessitates a more posterior course of the proximal thoracic aorta to reach its normal anatomic position just anterior and lateral to the spine (see Figure 2). Thus anterior-posterior (AP) projections of this segment of aorta demonstrate considerable overlap between the ascending and proximal descending aorta. Thus, when inserting endovascular devices, such as a pressure–volume loop catheter into the heart, we have found that an oblique projection minimizes this overlap and aids in navigating devices into their proper positions.

Figure 2.

(a) Three-dimensional rendering of CT demonstrating the sagittal anatomy of the aorta. At the chest outlet, two main trunks are seen, as opposed to three seen in humans. (b) Maximal intensity projection (MIP) of saggital CTA showing anatomy of the aorta. Note the posterior course of the aorta as it arises from the heart. Abbreviations: aAo = ascending aorta; BcT = brachiocephalic trunk; CeA = celiac artery; dAo = descending aorta; eIAs = external iliac arteries; ScA = subclavian artery; LAs = lumbar arteries; MSA = median sacral artery; PMA = posterior mesenteric artery; SMA = superior mesenteric artery.

In addition, given the quadruped stance, the heart lies ventral to the great vessels and gravity contributes to venous drainage.⁷ The supine position typically utilized during experimental protocols therefore changes this physiology greatly. While the size of the heart of a 30–40 kg pig is similar to that of an adult heart in terms of structure, size, and proportional mass, one difference between the vascular anatomy of the coronary circulation is that the hemiazygos (left azygos) vein drains a portion of the intercostal venous system directly into the coronary sinus.⁶ Swine typically have only two pulmonary veins that drain oxygenated blood into the left atrium, compared to the four veins seen in humans.⁷

The origin of the great vessels includes two primary trunks, a proximal brachiocephalic trunk (BcT) that gives rise to the right subclavian artery (ScA) and bicarotid trunk (BCaT) and distally, a left subclavian trunk (see Figure 3). Each ScA features a prominent internal mammary artery and a vertebral artery, as well as the major branches feeding the front legs, shoulders, and neck (see Figure 4).

Figure 3.

(a) DSA of the aortic arch and its major branches in LAO position given posterior course of aorta. A high contrast load was utilized given hyperdynamic hemodynamics. (b) Three-dimensional rendering from the same projection as (a). (c) MIP of coronal CTA showing aortic arch in relation to bony structures. Note the narrow chest outlet given the laterally compressed chest cavity. Abbreviations: aAo = ascending aorta; AxA = axillary artery; BA = brachial artery; BCaT = bicarotid trunk; BcT = brachiocephalic trunk; CCA = common carotid artery; IMA = internal mammary artery; ScA = subclavian artery; SsA = subscapular artery; VA = vertebral artery.

Figure 4.

DSA from lateral position showing the major branches of the left subclavian trunk. Note the sharp turn taken by the ScA as the origin courses superiorly and medially and takes ∼60° angle to course laterally. Abbreviations: AxA = axillary artery; CvA = costovertebral artery; IMA = internal mammary artery; ScA = subclavian artery; VA = vertebral artery.

Distal to the takeoff of the left ScA, the thoracic aorta exhibits a diameter that is suitable for stenting with human devices in 40–60 kg Yorkshire swine, measuring >16 mm, reported in a small series of animals (Morrison, unpublished data, n = 3). However, this varies based on breed of swine used, as measurements from our studies with 30–50 kg Hanford miniature swine were consistently <16 mm, thus may not be ideal for utilization of human aortic stents (Morrison, unpublished data, n = 5). The extensive length of the aorta also requires that delivery systems of endovascular therapies be of sufficient length to reach the intended target.

When considering percutaneous vascular access, minimally invasive placement of commonly used hemodynamic data collection transducers (e.g. solid-state pressure catheters) requires some forethought given the geometry of the great vessels and their position relative to the aortic arch. Brachial arterial (BA) access (discussed later) provides a means of central access, but the utility of the right and left brachial arteries as access points differs. Given the acute angle formed by the takeoff of the left ScA and the proximal aorta, the position of the left ScA along the aorta, as well as the sharp lateral turn of the left ScA as it courses distally to the forelimb, devices advanced through the left BA naturally steer into the descending aorta. Thus, attempting to place catheters via the left BA into the ascending aorta can present a challenge. Conversely, the right BA feeds into the right ScA, which originates from a trunk that resembles a 90° angle with respect to the ascending aorta and comes off more proximal with respect to the aortic arch. Thus, the right brachial access point may provide greater flexibility for percutaneous device insertion to be steered into either the descending aorta or the ascending aorta/heart (see Figure 3).

Head and neck

The first notable anatomic difference between the great vessels of the head and neck is the origin of the common carotid arteries (CCAs). Swine exhibit a BcT which gives rise to both the right ScA and the common BCaT (see Figure 5). The CCA of swine is longer than that of the CCA of humans and has been reported to be of similar diameter to the human internal carotid artery (ICA), approximately 5–6 mm.¹² Based on our observations, we can confirm that even in Yorkshire swine weighing up to ∼70 kg, the CCA exhibits a similar diameter. In addition, the CCA of swine exhibits considerable length. Thus, the CCA may indeed provide a useful model for clinical research on the human ICA. One limitation in modeling the human ICA with swine CCA is its relative fixed and straight course when compared to the more mobile and tortuous human ICA.

Figure 5.

AP DSA of BCaT trunk and bilateral CCAs as they course toward the skull base. Abbreviations: APA = ascending pharyngeal artery; BCaT = bicarotid trunk; CCA = common carotid artery; LA = lingual artery; MA = maxillary artery; RM = rete mirabile.

Figure 6.

(a) DSA of CCA bifurcation and distal branches. Note the bilateral opacification, despite only injecting contrast through the left CCA. (b) Magnified DSA of ascending pharyngeal artery (APA) and cerebral circulation of the swine. Note arterial connections between the cerebral vasculature and branches of the ECA. (c) MIP of coronal CTA showing the anterior and posterior orientation of the CCA bifurcation with respect to bony structures. Abbreviations: ACA = anterior cerebral artery; APA = ascending pharyngeal artery; AuA = auricular artery; BuA = buccal artery; CCA = common carotid artery; ECA = external carotid artery; FA = facial artery; ICA = internal carotid artery; IoA = infraorbital artery; LA = lingual artery; MA = maxillary artery; MCA = middle cerebral artery; OA = opthalmic artery; RM = rete mirabile.

An additional distinct characteristic of the carotid circulation involves the bifurcation of the CCA, branching into a robust external carotid arterial (ECA) system that supplies the large mass of soft tissue and musculature of the head and neck region and a small ascending pharyngeal artery, which then forms a network of arterio-arterial connections, named the rete mirabile (RM).¹³ It is not until distal to the RM that the ICA appears and ultimately makes its intracerebral course (see Figure 6). In addition, there are communicating branches between the ECA and the cerebral vasculature not seen in humans.

The RM is a vascular meshwork that connects the left and right cerebral arterial vasculature at the base of the skull and creates redundancy proximal to the circle of Willis not seen in humans. The function of RM has need not yet been fully defined but it has been suggested to assist in temperature regulation and body water conservation.¹⁴ Intuitively, this structure aids in massive stroke prevention. The RM has been utilized in prior studies investigating cerebral arterio-venous malformations (AVMs),¹⁵ and when subjected to radiation, is reactive with intimal hyperplasia and occlusion, resulting in neurologic deficits.¹⁶ While it has utility as a model of AVMs, it renders endovascular entry into the cerebral circulation impossible. In our experience, the RM prevents the endovascular creation of an intracerebral vascular injury, thus limiting intracerebral hemorrhage model development by endovascular means.

Intracerebral vessels are small, previously reported to be 1 mm or less.¹⁷ This is consistent with our experience. Detecting focal perfusion deficits with devices intended to detect such deficits in humans may be near impossible, given the small amount of blood flow provided by these small vessels. Thus, conducting studies that aim to explore global perfusion in response to experimental protocols, such as computed tomography perfusion, may provide a more realistic and fruitful approach to this limitation.

While much of the past research has utilized surgical methodology for vascular access, the primary mode of vascular access in our practice is achieved percutaneously using ultrasound-guided modified-Seldinger techinque, thus paralleling the use of percutaneous methods in clinical practice. Within the neck, arterial access can be obtained via the CCA. In our experience, carotid arteries tend to range from 5 to 8 mm and are ∼20–25 mm from the skin, and course in a relatively straight pathway in the lateral/medial dimension, making them suitable targets for percutaneous access. However, swine carotid arterial access can be complicated by intense vasospasm, intramural hematoma and pseudoaneurysm creation, even with one small-bore needle puncture. Thus, with even one failed percutaneous attempt at cannulation, the CCA can become near-impossible to cannulate with subsequent percutaneous attempts, ultimately requiring a surgical cutdown technique. A notable difference in venous anatomy between swine and humans is that the external jugular vein in swine is not a superficial vein, and, in our experience, is a more suitable venous access point than the internal jugular vein due to its larger diameter. When performing vascular access procedures, percutaneous methods can be utilized at a high success rate; however, the knowledge of cutdown technique is recommended, especially in experimental protocols which require bilateral carotid arterial access.

Abdomen/pelvis

An overview of the abdominal aortic anatomy is shown in Figure 7. The primary abdominal aortic branches are similar to those seen in humans with a celiac artery and superior mesenteric artery (sometimes referred to as the cranial mesenteric artery); however, swine lack a formal inferior mesenteric artery and instead have a small posterior mesenteric artery (PMA) which comes off the right side of the distal aorta to supply the distal colon and rectum (see Figures 7 and 8). There are no mesenteric arcades as seen in humans; rather bundles of branching vessels extend into the mesentery and arcades form within the connective tissue surrounding the bowel.¹⁸

Figure 7.

Three-dimensional rendering from CTA showing the major branches of the aorta from an AP projection. Abbreviations: AdA = adrenal artery; CeA = celiac artery; CFA = common femoral artery; CHA = common hepatic artery; cIA = circumflex iliac artery; CoA = colic artery; dAo = descending aorta; eIA = external iliac artery; HA = hepatic artery; ICoA = ileocolic artery; iIAs = internal iliac arteries; GA = gastric artery; GDA = gastroduodenal artery; PFA = profunda femoris artery; PHA = proper hepatic artery; PMA = posterior mesenteric artery; RA = renal artery; SA = splenic artery; SFA = superficial femoral artery; SMA = superior mesenteric artery.

Figure 8.

(a) Lateral projection DSA of the abdominal aorta showing the takeoff of the CeA and SMA. (b) MIP of coronal CTA showing the major branches of the CeA. (c) Coronal MIP of CTA showing the major branches of the SMA. (d) Coronal MIP of CTA showing the PMA and its course distally to perfuse the distal colorectal territory. See Figure 7 for abbreviations.

From a geometric perspective, the renal arteries branch from the aorta at an acute angle in a cranial direction (see Figure 9), with the left side originating more proximally compared to the right side. Thus, when advancing endovascular devices via a transfemoral approach, especially without fluoroscopic guidance, care must be taken to avoid inadvertently cannulating the renal arteries. The size of the abdominal aorta of 40–60 kg Yorkshire swine ranged from 7.7 to 10.1 mm in our studies (n = 6), which is notably smaller than that observed in humans. Thus, devices designed to treat abdominal aortic aneurysms in humans may not fit in the porcine abdominal aorta.

Figure 9.

Coronal MIP of CTA showing the abdominal aorta. Note the geometry of the renal arteries relative to the aorta. Abbreviations: AdA = adrenal artery; dAo = descending aorta; eIA = external iliac artery; iIAs IVC = inferior vena cava; RA = renal artery.

The distal aortic division in swine differs from that of humans; instead of a bifurcation, a trifurcation is present with two external iliac arteries flanking a common internal iliac trunk that divides almost immediately at its origin into a right and left internal iliac artery (see Figure 10).

Figure 10.

(a) DSA of distal aorta demonstrating the aortic trifurcation and proximal arteries of the hindlimbs from AP projection. (b) MIP of coronal CTA showing similar anatomy to (a), in relation to bony and soft tissue structures. Abbreviations: CFA = common femoral artery; cIA = circumflex iliac artery; dAo = descending aorta; eIA = external iliac artery; iIA = internal iliac artery; IVC = inferior vena cava; MSA = median sacral artery; PFA = profunda femoris artery; PMA = posterior mesenteric artery; SFA = superficial femoral artery.

The sizes of internal and external iliac arteries ranged from 4.4 to 5.6 and 6.0 to 6.8 mm respectively in 40–60 kg Yorkshire swine used in our laboratory (n = 6). The external iliac artery gives off a circumflex iliac artery distal to the takeoff of this branch and continues its course, with its name changing to the common femoral artery (CFA). The CFA in 40–60 kg Yorkshire swine ranged from 4 to 6 mm prior to dividing into superficial femoral and deep femoral branches (n = 6). The sizes of iliac and femoral vessels are important to consider as some endovascular devices may not be fully deployable in smaller vessels. Thus, devices should have more compact shapes to navigate swine vasculature successfully.

When performing intra-abdominal imaging, another consideration for aberrant anatomy is cryptorchidism. According to prior data, the prevalence of cryptorchidism in swine is up to 12%.¹⁹ Thus, when performing imaging studies of the abdomen/pelvis/groin regions, contrast enhancement of a testis may interfere with the desired image acquisition (see Figure 11).

Figure 11.

MIP of coronal CTA of pelvis demonstrating a cryptorchid testicle in the area of desired imaging.

Upper and lower extremity

Given the quadruped stance of swine, in the supine position, appendages extend in the ventral direction. The central vessels are as described above, ultimately with the CFA giving rise to the SFA and PFA (see Figure 10). The PFA has a robust connection with the internal iliac artery, which allows for ligation of the CFA without gross detriment to perfusion, as flow is able to be restored to the SFA via retrograde flow through the PFA, which also communicates with the contralateral proximal hindlimb vasculature.

The femoral vessels are the most successfully percutaneously cannulated vessels in our experience. The femoral artery lies just lateral and superficial to the femoral vein, much like in humans. As discussed above, the femoral artery is subject to vasospasm and intramural hematoma formation upon puncture but is generally more forgiving and multiple cannulation attempts can typically be performed prior to considering a surgical cutdown. A range of catheter sizes can be utilized, as we have successfully placed a 25 Fr ECMO cannula in the femoral artery of a Yorkshire swine weighing ∼60 kg.

The vasculature of the upper extremity is quite tortuous (see Figure 12), but percutaneous brachial access can be performed at a high success rate when performed properly. At its most distal point, the BA is typically <5 mm in diameter and superficial, <10 mm deep. While cannulation at this distal point is possible, the tortuosity of the vessels as well as the angle of the appendage can cause difficulty even with microwire insertion. A point more proximal gives a deeper vessel with a diameter typically ∼5 mm, which avoids some of the tortuosity of the distal vessel typically allowing successful cannulation. However, this must be balanced against the low threshold for vasospasm, similar to that seen with the carotid artery. Thus, we typically attempt distal cannulation first; if unsuccessful, then more proximal cannulation is attempted. Once the 0.018″ wire has been exchanged for a standard 0.035″ wire, we have found that a J tipped wire more successfully traverses the brachial artery to its central location. In addition, a flexible catheter is advantageous, as less compliant endovascular tools tend to thread less easily into the central arterial circulation.

Figure 12.

(a) Upper extremity DSA demonstrating arterial anatomy from an oblique projection. (b) Curved MIP of coronal CTA demonstrating the tortuous course of the forelimb vasculature as it traverses from the subclavian to the brachial artery. Abbreviations: AxA = axillary artery; BA = brachial artery; RA = radial artery; ScA = subclavian artery; UA = ulnar artery.

Conclusion

Swine have been utilized for robust and broad-ranging preclinical models given their similarities in size, anatomy, and general function. In particular, swine are attractive for research studies involving cardiovascular anatomy and physiology. Despite these similarities, it is crucial to have a broad understanding of the basic anatomical differences between species in order to conduct and interpret preclinical porcine studies (see Table 1).

Table 1.

Overview of major vascular anatomical differences between humans and swine.

Vessel(s)	Difference	Application
Thoracic aorta	– Smaller caliber than human thoracic aorta– Large AP distance traversed	– May not be amenable to human TEVAR devices– Oblique projection superior for navigating devices into ascending vs. descending aorta
Great vessels	• Only 2 trunks supplying the great vessels, a brachiocephalic trunk that gives rise to the right subclavian artery and a bicarotid trunk, and a left subclavian trunk	• More distal origin and angulation of left subclavian artery makes it more difficult to insert devices into the ascending aorta from the left brachial access point. The right brachial artery allows for more versatile navigation of either the ascending or descending aorta• Devices inserted through either carotid artery will steer into the brachiocephalic trunk
Carotid arteries	• Carotid bifurcates into ascending pharyngeal artery and external carotid artery; ascending pharyngeal feeds rete mirabile prior to feeding brain• External carotid artery is larger than ascending pharyngeal artery	• Endovascular cannulation of cerebral arteries by way of the ascending pharyngeal is impossible• Reflects soft tissue metabolism and its relative importance to the swine
Rete mirabile	• Not present in humans	• Influences the flow of carotid blood (i.e. arterio-arterio anastomotic connection between the right and left cartotids), thus studies of flow patterns must consider this structure when obtaining data/imaging
External jugular vein	• Central venous vessel in swine	• Typically larger diameter than that of internal jugular vein and thus more amenable to percutaneous cannulation
Renal arteries	• Acute angle formed by the takeoff of the renal arteries and the proximal aorta	• Devices navigated from a transfemoral approach will sometimes naturally steer into the renal artery and risk iatrogenic damage
Abdominal aorta	• Smaller caliber when compared to human abdominal aorta• Distal aorta divides into trifurcations	• May not be amenable to human EVAR devices
Femoral and iliac vessels	• Smaller caliber than human counterparts• Femoral vessels in swine tend to course medially toward the pelvis given quadruped stance	• Larger devices as well as wires and catheters with less compact shapes may not be able to be navigated effectively through this approach• When inserting larger sheaths/cannulas, lateral traction/abduction may assist with insertion

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by the Uniformed Services University of Health Sciences, Grant number: HU00011920072.

ORCID iDs

Hossam Abdou

Jonathan J Morrison

References

Bunte

Shishehbor

MH.

Next generation endovascular therapies in peripheral artery disease. Prog Cardiovasc Dis 2018; 60: 593–599.

Romagnoli

Zeeshan

Joseph

, et al. Utilization of endovascular and open surgical repair in the United States: a 10-year analysis of the National Trauma Databank (NTDB). Am J Surg 2019; 218: 1128–1133.1.

Stein

Tuhrim

Fifi

, et al. National trends in endovascular therapy for acute ischemic stroke: utilization and outcomes. J Neurointerv Surg 2020; 12: 356–362.1.

Hughes

HC.

Swine in cardiovascular research. Lab Anim Sci 1986; 36: 348–350.

Bushi

Assaf

Grad

, et al. Similarity of the swine vasculature to the human carotid bifurcation: analysis of arterial diameters. J Vasc Interv Radiol 2008; 19: 245–251.

Swindle

Smith

AC.

Comparative anatomy and physiology of the pig. Scand J Lab Animal Sci 1998; 25: 11–21.

Lelovas

Kostomitsopoulos

Xanthos

TT.

A comparative anatomic and physiologic overview of the porcine heart. J Am Assoc Lab Anim Sci 2014; 53: 432–438.

Ratcliffe

Luginbühl

Pivnik

Coronary, aortic and cerebral atherosclerosis in swine of 3 age-groups: implications. Bull World Health Organ 1970; 42: 225–234.

Altamuro

Fetal pig dissection manual: directional terms, www.behance.net/gallery/72165099/Fetal-Pig-Dissection-Manual (2018, accessed 12 November 2020).

10.

Swindle

MM.

Swine in the laboratory: Surgery, anesthesia, imaging, and experimental techniques. 2nd ed. Boca Raton: CRC Press, 2007.

11.

Bell

JM.

A study of rates of growth of Yorkshire, Lacombe, Landrace, and crossbred pigs from birth to 200 lb. Can J Animal Sci 2011; 44: 315–319.

12.

Caramori

PRA

Eggers

Silva-Filho

APF

, et al. Postangioplasty restenosis: a practical model in the porcine carotid artery. Braz J Med Biol Res 1997; 30: 1087–1091.

13.

Mangla

Choi

Barone

, et al. Endovascular external carotid artery occlusion for brain selective targeting: a cerebrovascular swine model. BMC Res Notes. 2015; 8: 1–6. DOI: 10.116/s13104-015-1714-7.

14.

Strauss

Hetem

Mitchell

, et al.

Body water conservation through selective brain cooling by the carotid rete: a physiological feature for surviving climate change?

Conserv Physiol 2017; 5: 1–15.

15.

Arakawa

Murayama

Davis

, et al. Endovascular embolization of the swine rete mirabile with Eudragit-E 100 polymer. AJNR Am J Neuroradiol 2007; 28: 1191–1196.

16.

De Salles

Solberg

Mischel

, et al. Arteriovenous malformation animal model for radiosurgery: the rete mirabile. AJNR Am J Neuroradiol 1996; 17: 1451–1458.

17.

Reinert

Brekenfeld

Taussky

, et al. Cerebral revascularization model in a swine. Acta Neurochir Suppl. 2005; 94: 153–157. DOI: 10.1007/3-211-27911-3_25.

18.

Spalding

Heath

Arterial supply to the pig intestine: an unusual pattern in the mesentery. Anat Rec 1987; 218: 27–29.

19.

Amann

Veeramachaneni

DNR.

Cryptorchidism in common eutherian mammals. Reproduction 2007; 133: 541–561.