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. 2005 Oct;207(4):427–432. doi: 10.1111/j.1469-7580.2005.00455.x

Topographic anatomy of bronchial arteries in the pig: a corrosion cast study

Michael Lorentziadis 1, Themistocles Chamogeorgakis 1, Ioannis K Toumpoulis 1, Panagiotis Karayannacos 1, Theodosios Dosios 1
PMCID: PMC1571548  PMID: 16191170

Abstract

The anatomy of porcine bronchial circulation has not been fully described. The purpose of this study was to investigate the extrapulmonary topographic anatomy of bronchial arteries in pig. Ten pigs weighing 15–25 kg were studied. Between one and four bronchial arteries were found in each pig. The bronchoesophageal artery (BEA), tracheobronchial artery (TBA), inferior bronchial artery (IBA) and accessory bronchial artery (ABA) were present in 10/10, 8/10, 6/10 and 2/10 animals, respectively. The trunk of BEA had a diameter of about 3 mm, a length of 1–7 mm, and originated from the anterior and medial aspect of the descending thoracic aorta at the level between the 2nd and 4th thoracic vertebrae (T2–T4) in all animals. The extrapulmonary topographic anatomy of bronchial arteries in pigs exhibits similarities to that of humans. BEA is the main blood supplier of the porcine tracheobronchial tree with a relatively constant location of origin and a sufficient size for anastomosis. These characteristics render BEA the ideal vessel for bronchial revascularization in pigs.

Keywords: anatomy, bronchial circulation, bronchoesophageal artery, pig

Introduction

It is well known that the anatomy of the bronchial arterial system is of importance in various pathological conditions in the respiratory system, including chronic asthma, bronchiectasis, abscess and empyema (Marchand et al. 1950; Fritts et al. 1961; Charan et al. 1997). In addition, it seems that bronchial circulation plays a role in the healing of bronchial anastomosis in lung transplantation procedures. Bronchial anastomotic complications constitute a serious threat in such procedures (Veith et al. 1983). The overall lethal airway complications after lung transplantation are estimated to be 2–3%, whereas that associated with late stricture is 7–14% (Shennib & Massard, 1994). Bronchial revascularization has a beneficial effect on bronchial and pulmonary endothelium and probably reduces the incidence of bronchial dehiscence (Couraud et al. 1992; Daly & McGregor, 1994); it does not, however, alter the incidence of bronchiolitis obliterans syndrome (Norgaard et al. 1998; Hyytinen & Halme, 2000; Hyytinen et al. 2000; Gade et al. 2001; Nowak et al. 2002).

This technique could be improved in experimental animals by detailed knowledge of their bronchial anatomy. However, few such studies in animals exist. Because the minipig is an excellent animal model for pulmonary studies, including lung transplantation (Cauldwell et al. 1948; Tobin, 1952; Liebow, 1965), we considered that a thorough study of the topographic anatomy of bronchial arteries in this animal would be useful.

The purpose of this study was to investigate the extrapulmonary topographic anatomy of bronchial arteries and their main branches in pig.

Materials and methods

Ten pigs (Sus scropha domesticus), six male and four female, were used in this study. Their weight was 17–25 kg (mean 20.5 kg), and their age 4–6 months (mean 5.1 months). All animals received humane care in compliance with the ‘Guide for the care and use of Laboratory Animals’ published by the National Institute of Health. The animal protocol was approved by the Institutional Animal Care and Use Committee of the University of Athens, Greece. Each animal was sedated with intramuscular administration of diazepam 2 mg kg−1, ketamine 10 mg kg−1 and atropine sulfate 0.05 mg kg−1 of body weight. Subsequently, venous line access was established, induction to anaesthesia was obtained with pentothal 20 mg kg−1 given intravenously, and the animal was intubated with a 6-mm endotrachial tube. General anaesthesia was maintained with halothane 0.5–1%. Electrocardiogram, arterial blood pressure and pulse rate were continuously monitored.

Each animal was placed supine. The chest wall was opened wide with a broad incision starting at the junction of the costal cartilage and the middle axillary line on the left, following the middle axillary line cephalad at the neck, 4 cm above the sternal notch, crossing the midline at the neck and terminating at the opposite costal cartilage, creating a Greek Π. The major and minor thoracic muscles as well as the strap muscles were divided with electrocautery. The axillary arteries, as well as both common carotid arteries, were doubly ligated and divided. The ribs were transected and the anterior chest wall was removed en block. Heparin 25 000 IU and papaverin 5 mg were injected into the aortic root. At this point, the animal was killed via an intracardiac injection of pentothal 1 g. The descending thoracic aorta was ligated at the level of the diaphragm, transected, and the proximal stump was cannulated. The superior and inferior vena cava were also doubly ligated and divided. The ascending aorta and the main pulmonary artery were transected above the coronary ostia and the pulmonary valve, respectively, cannulated and flushed with a solution of 0.9% NaCl. The trachea was transected at a level 2–3 cm above the origin of the right superior bronchus, and cannulated. The pulmonary veins were transected and the heart was excised. The oesophagus and the vertebral column were transected at levels of T1 and T12, and the trachea and lungs were extracted en block with the thoracic aorta, oesophagus and thoracic spine with the adjacent portion of the chest wall, as a specimen.

Subsequently, a coloured preparation of acrylic resin consisting of three parts of methylmethacrylate and four parts of triethylenotetramine was injected under low pressure through the cannula of the ascending aorta. When the lumen of the aorta was filled, a clamp was applied at the distal end and the infusion continued until the aortic branches, including the bronchial arteries, were filled. The tracheobronchial tree and the pulmonary artery and its branches were also filled with a coloured preparation of acrylic resin through the previously inserted cannulas in the trachea and the main pulmonary artery, respectively. Red dye (Levanyl, Shell, Greece) was used for the aorta, yellow dye (Heliocytgela GXT Feintei, Shell, Greece) for the trachea and blue violet dye (BN2 Feintei, Shell, Greece) for the pulmonary artery. This preparation was a viscous liquid that solidified approximately 30 min after injection. When the injected resins solidified, the specimen was immersed in a solution of KOH 25% (Kalium hydroxid Platzchenrein, Merck) warmed at 45 °C. The specimen remained in that solution for 48 h, when all tissues, including the vertebrae, were corroded and the complex of solidified coloured resins was separated as a cast (Fig. 1). The cast was washed with a solution of 0.9% NaCl. We obtained a three-dimensional demonstration of the bronchial arteries without disturbing their anatomical interrelations with the tracheobronchial tr0ee, the pulmonary arteries and the aorta. The arising angles of the bronchial arteries were measured in relation to the transverse plane of the aorta (Fig. 2). The diameter of the arteries was measured at their origin. Finally, their length was determined as the distance between their origin and the first ramification.

Fig. 1.

Fig. 1

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A three-colour cast of the tracheobronchial tree (yellow), the pulmonary artery and its branches (blue violet), and the aorta and its branches including the bronchial arteries (red) in pig.

Fig. 2.

Fig. 2

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Angle of origin of BEA (bronchoesophageal artery) (A) and IBA (inferior bronchial artery) (B) on transverse aortic section.

Statistical analysis

Results are expressed as mean ± standard deviation. Statistical analysis was performed by using the Fisher's exact test for comparisons between discrete variables and the Mann–Whitney U-test for comparisons regarding the number of branches, diameter, length, distance of origin from the aortic root and angle of origin. Statistical significance was assumed at a P-value of < 0.05. All analyses were performed in SPSS 11.0 (SPSS Inc., Chicago, IL, USA).

Results

The trunks of the bronchial arteries

Between one and four bronchial arteries were identified: bronchoesophageal artery (BEA), tracheobronchial artery (TBA), inferior bronchial artery (IBA) and accessory bronchial artery (ABA). The nomenclature used for BEA and TBA was in accordance with Magno et al. (1987). For IBA and ABA we introduced our own nomenclature, because they had not been described previously. Each of these arteries had its own trunk and showed a distinct origin. BEA was identified in all (10/10) animals, was the main blood supplier of the tracheobronchial tree and had a larger diameter than the other three arteries (P < 0.001). The vessel originated from the anterior and medial aspect of the descending thoracic aorta at the level between T3 and T4 in six animals and between T2 and T3 in the remaining four animals. TBA arising from the right subclavian artery was found in eight pigs, supplying the thoracic portion of the trachea and the right superior lobe bronchus (Fig. 3). IBA was found in six animals and originated from the aorta, the right 4th intercostal artery and the right 5th intercostal artery in four, one and one pig, respectively. ABA was found in two animals. One of these had a double ABA trunk. Four animals had two bronchial arteries (BEA, TBA), and six animals had three bronchial arteries (four animals had BEA, TBA, IBA and two animals BEA, IBA, ABA). The anatomical characteristics of the bronchial arterial trunks are summarized in Table 1.

Fig. 3.

Fig. 3

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The tracheobronchial artery (TBA) supplies the thoracic trachea and the right upper lobe bronchus and arises from the right subclavian artery.

Table 1.

Trunks of the bronchial arteries

Origin
Bronchial artery Arteries/ animals Arising angle from the aorta (mean; degrees) Level of origin in relation to the thoracic spine (animals) Diameter (mean; mm) Length (mean; mm)
BEA 10/10 10–83 (44.3) T3–T4 (6/10) 1.8–4.0 (2.59) 1–7 (3.1)
T2–T3 (4/10)
TBA* 8/10 65–90 (82.5)* T1–T2 (8/8) 0.6–1.2 (0.91) 1–6 (2.9)
IBA 6/10 30–350 (148.3) T4–T5 (3/6) 0.5–1.2 (0.86) 1–70 (30.1)
T5–T6 (2/6)
T7–T8 (1/6)
ABA 2/10† 85–103 (92.0) T5–T6 (1/2) 0.5–2.0 (1.14) 10–60 (34.0)
T4–T5 (1/2)
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BEA, bronchoesophageal artery; TBA, tracheobronchial artery; IBA, inferior bronchial artery; ABA, accessory bronchial artery.

*

Arising from the right subclavian artery.

†

One animal had double origin of ABA.

The branches

Three branches of the BEA were identified: anterior descending branch (ADB), posterior descending branch (PDB) and posterior ascending branch (PAB) (Figs 4 and 5). IBA gave multiple branches creating a plexus in four of six pigs. The plexus reconstituted in four arteries, two on each side, following the corresponding main stem bronchi. In the remaining two animals, IBA divided into four branches, two on either side, immediately after its origin. ABA created a plexus at the carina in both animals in which it was identified.

Fig. 4.

Fig. 4

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The bronchoesophageal artery (BEA) and its three branches: (A) posterior ascending branch (PAB), (B) anterior descending branch (ADB), (C) posterior descending branch (PDB).

Fig. 5.

Fig. 5

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BEA bifurcating into (A) posterior ascending branch (PAB) and (B) anterior descending branch (ADB). Notice that the length and the diameter of the bronchoesophageal artery (BEA) are sufficient for anastomosis.

Distribution of the bronchial arteries at the tracheobronchial tree

The thoracic segment of the trachea was supplied by BEA, TBA and ABA. The carina was supplied by all bronchial arteries. The right superior lobe bronchus was supplied by TBA and PAB of the BEA. The right and the left main stem bronchi were supplied by PDB and ADB of BEA, IBA and ABA. The distribution of the bronchial arteries at the tracheobronchial tree is summarized in Table 2. We did not find any statistically significant difference regarding the diameter and the distance of origin of BEA from the aortic root between male and female animals (P = 0.637 and P = 0.762, respectively; Mann–Whitney U-test). In all female pigs BEA gave two branches and in the majority of the male pigs (4/6) it gave three branches. This difference was statistically significant (P = 0.029, Fisher's exact test). IBA was encountered more often in male pigs (4/6) than in female pigs (2/4). In female animals, the diameter of this vessel was greater and its length was shorter but these differences were not statistically significant (P = 0.800 and P = 0.133, respectively). Owing to the small number of ABA we did not perform any statistical analysis between the two genders with regard to this vessel.

Table 2.

Distribution of bronchial arteries at the tracheobronchial tree

Artery Trachea Carina RSLB RMSB LMSB
BEA – PAB 7/10 7/10
BEA – PDB 8/10 8/10 8/10 8/10
BEA – ADB 10/10 10/10 10/10 10/10
TBA 8/10 8/10
IBA 6/10 6/10 6/10
ABA 2/10 2/10 2/10 2/10
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BEA, bronchoesophageal artery; PAB, posterior ascending branch; PDB, posterior descending branch; ADB, anterior descending branch; TBA, tracheobronchial artery; IBA, inferior bronchial artery; ABA, accessory bronchial artery; RSLB, right superior lobe bronchus; RMSB, right main stem bronchus; LMSB, left main stem bronchus.

Discussion

It is known that BEA, which is the main blood supplier to the bronchial tree and oesophagus, originates from the thoracic aorta and is usually paired in most domestic animals. In pigs, however, it is single (Nickel et al. 1981; Gade et al. 1999b). In addition, it is known that TBA supplies the thoracic portion of the trachea and the right superior lobe bronchus (Magno et al. 1987).

The main finding of our study was that the porcine tracheobronchial tree was supplied by between one and four bronchial arteries. Each had its own trunk and showed a distinct origin. Although these arteries showed many variations mainly in their branching, we found that BEA was the main blood supplier of the tracheobronchial tree in all animals. The trunk of this vessel had a relatively constant location of origin from the descending aorta and a diameter and length sufficient for anastomosis. This artery has already been used experimentally as the blood supply source for bronchial revascularization in lung transplantation (Nazari et al. 1990; Macedo et al. 2004). TBA was the second most consistent artery arising from the right subclavian artery and supplying the thoracic portion of the trachea and the right superior lobe bronchus. In addition to these known arteries, we were able to demonstrate the variable existence of other two bronchial arteries, namely the IBA and ABA. This was achieved because we used the cast corrosion technique infusing resins through the ascending aorta. This technique allows for a detailed study of topographic anatomy of the bronchial arteries without disturbing their interrelationships with the surrounding anatomical structures (Schraufnagel, 1987, 1989; Schreinemakers et al. 1990). However, we consider that TBA, IBA and ABA are not suitable for anastomosis due to their small diameter.

Communication between the bronchial arteries and the pulmonary arterial network has been identified (Berti et al. 1995; Gade et al. 1999a). We did not demonstrate communication between the bronchial network, the pulmonary, the oesophageal and the coronary circulation. This was due to the fact that, because we were interested only in studying the topographic anatomy of the main bronchial arteries, we used a viscous resin as injection material, which could not reach the terminal branches of the bronchial circulation.

A comparison of our findings with those of the literature concerning the extrapulmonary bronchial arterial pattern in humans is interesting. Liebow (1965) performed a corrosion cast study on 50 human cadavers and found that the most common bronchial arterial pattern was the presence of two right and two left bronchial arteries. Kasai & Chiba (1979) performed dissection of 40 human cadavers and reported similar results. Others (Cauldwell et al. 1948; Tobin, 1952; Schreinemakers et al. 1990) found that the presence of one right and two left bronchial arteries was the most common bronchial arterial pattern. Viamonte et al. (1989) observed that the most common arrangement is to have a broncho-intercostal trunk arising from the descending thoracic aorta supplying the right lung with separate branches supplying the left lung.

In conclusion, this study showed that the extrapulmonary topographic anatomy of bronchial arteries in pigs exhibits similarities to that of humans. BEA is the main blood supplier of the porcine tracheobroncheal tree with a relatively constant location of origin and a size sufficient for anastomosis.

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