Extraneural Arterial Blood Vessels of Human Fetal Sciatic Nerve

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Extraneural Arterial Blood Vessels of Human Fetal Sciatic Nerve Sladjana Z. Ugrenovic[1], Ivan D. Jovanovic[1], Ljiljana P. Vasovic[1], Bratislav D. Stefanovic[2] [1]Institute of Anatomy, Faculty of Medicine, University of Nis [2]Institute of Histology, Faculty of Medicine, University of Belgrade Serbia, Europe Accepted after revision: March 5, 2007; Published online: June 21, 2007 Abstract: Nerves get segmental blood supply either from the neighboring muscular and cutaneous branches or from the regional main arterial trunks. The aim of our research was to detect, in the gluteal and posterior femoral region, the blood vessels which are involved in the blood supply of the human fetal sciatic nerve, as well as to establish their origin. Micro- dissection was performed on 48 fetal lower extremities which were previously fixed in 10% formalin. Micropaque solution (barium sulfate) was injected into their blood vessels. The fetal gestational age was established by measuring the crumpcrown length and it ranged from the third to the ninth lunar month. The observed nutritional arteries of the human sciatic nerve originated from the inferior gluteal artery, medial circumflex femoral artery, perforating branches, and popliteal artery. The anastomotic arterial chain of the human sciatic nerve was observed in all cases. In 75% of the cases it was composed of the branches of the inferior gluteal artery, the medial circumflex femoral artery and the first two perforating arteries. The nutrient branch of the third perforating branch was less frequently (in 14.5% of the cases) part of this anastomotic arterial chain. – Cells Tissues Organs 186:147-153 (2007); DOI: 10.1159/00010 4407. Key Words: Sciatic nerve – Blood vessels – Fetus – Human ----------------------Correspondence to: Dr. Sladjana Z. Ugrenovic; Institute of Anatomy, Faculty of Medicine Blvd Zorana Djindjica 81, 18000 NIS, Serbia (Europe) Tel.: +381 64 307 45 40, Fax +381 18 238 770; e-mail: [email protected]

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Introduction Embryological development of the vascular and peripheral nervous system takes place simultaneously. During this period nerves get segmental blood supply either from the neighboring muscular and cutaneous branches or from the main arterial trunk. This form of segmental blood supply persists during the adult period as well. The arterial blood vessels which penetrate into the peripheral nerve and end inside it intraneurally are referred to as vasa nervorum. The main arterial trunk, in most cases, crosses the peripheral nerve before its nutrient branch for the peripheral nerve arises. So, this is why this branch has a recurrent pathway toward the nerve. The number and caliber of these arteries vary, as well as the peripheral nerve fascicular structure. However, the larger number of blood vessels and their larger caliber compose the blood supply of the larger peripheral nerves. The vascularization of these nerves along their pathway is uneven, which leads to the simultaneous presence of segments which are resistant and segments which are very vulnerable to hypoxia. Usually, the peripheral nerve arteries are very short (5–15 mm) and sometimes up to 25 mm. After the blood vessel reaches the nerve it may end in several ways: (1) it may penetrate the nerve at different angles, without preliminary branching; (2) it branches at the nerve surface into the ascendent and descendent branch; (3) it temporarily travels along the nerve surface and gives off perforating branches; (4) it pierces the nerve on its pathway to another structure; (5) two blood vessels penetrate into the nerve at the same level; (6) the nerve is supplied by the arterial network (El Barrany et al., 1999). The arteries for the blood supply of the nerves can sometimes be very large, for example the arteria commitans nervi mediani in the forearm or the arteria commitans nervi ischiadici in the thigh. Some cutaneous nerves with their accompanying blood vessel (such as the sural nerve with its median superficial sural artery) present a neurovascular stalk of the flaps which have an application in plastic surgery (Ugrenovic et al., 2005). In classical anatomical textbooks, the arteria commitans nervi ischiadici, which is a branch of the inferior gluteal artery, is marked as a blood vessel accompanying the sciatic nerve, being responsible for its blood supply (Sunderland, 1968; Williams et al., 1995). The arteria commitans nervi ischiadici is rudimentary residue of the primary arterial trunk of the lower extremity, known as sciatic (or axial) artery. This blood vessel, after the gestational period with a crown-crump length of 22 mm, gradually involutes, while the femoral artery system takes over the function of the main vascular source of the lower extremity (Kurtoglu and Uluutku, 2001; Wilson et al., 2005). A persistent sciatic artery is a very rare, but clinically very important vascular anomaly, which means that the transitory embryological arterial system of the posterior femoral region persists as the main vascular source of the lower extremity. The first description of the persistent sciatic artery was given by Green in 1832, and the incidence of this vascular anomaly ranged from 0.01 to 0.05%. It was more frequent in right lower extremities of males. Besides, the persistent sciatic artery can be complete or incomplete (Jue-Denis et al., 1984; Savov and Wassilev, 2000; Kurtoglu and Uluutku, 2001; Wilson et al., 2005). The organization of peripheral nerves vascular network has a specific character due to several reasons. Peripheral nerves have two separate, functionally independent vascular systems: extraneural (extrinsic system), and intraneural (intrinsic system). Longitudinal blood vessels mutually anastomose at the nerve surface where they form superficial arterial chains of different length, located in the epineurium (extraneural vascular system). Fine branches that penetrate the perineurium and enter into fascicles arise from the superficial and interfascicular arteries – largest blood vessels inside peripheral nerves (the precapillaries are predominant in the perineurium). Capillaries are longitudinally arranged within fascicles. They are mutually anastomosed with short transverse anastomoses and they form a terminal interfascicular capillary network (the intraneural vascular system). There are rich anastomoses between these two vascular systems described, but it is still unknown which of these systems is more important 2

for the blood supply of the nerves (Olsson, 1984; Beggs et al., 1991; Williams et al., 1995; Mawrin et al., 2001). This unique model of a vascular network is in accordance with the metabolic requirements of peripheral nerves and it increases the resistance of the nerves to ischemia. Nerves can be stretched for about 8% of their length without a microcirculation disorder (Sunderland, 1968; Xu and Zochodne, 2002). However, conditions that lead to a decline in the blood supply can essentially facilitate damage to nerve fibers during different peripheral neuropathies. Hence, the aim of our research was to detect and establish origin of blood vessels in gluteal and posterior femoral region which participate in blood supply of the human sciatic nerve. Methods The material consisted of 24 human fetuses (ie. 48 lower extremities). The fetuses were collected in the Department of Anatomy between 1962 and 1985. All fetuses were provided medicolegally by the Clinic of Gynecology and Obstetrics of the Faculty of Medicine in Nis, where it was established that they were without any anatomical deformities and systemic pathology. All departments of the Medical Faculty in Nis have integrated professional cooperation and there was an internal ethical control over fetal material used in the period of 1962–1985. The Council for Postgraduate Study of our Faculty of Medicine gave permission to investigate the fetal material. Micropaque solution (barium sulfate) was injected into the arteries of the fetuses through the common carotid artery or the left ventricle of the heart. The fetuses were fixed by immersion in 10% formalin. The fetal age ranged from the third to the ninth lunar month and it was established by measuring the crown-rump length. Microdissection of the fetal lower extremities was done under magnifying lenses (x5). Microdissection procedure of the fetal lower extremities was following: in the first part of the dissection, two horizontal cuts of the skin of the posterior part of the lower extremities were made – the first cut at the level of the iliac crest, the second at the level of the medial and lateral ankle; these two cuts were connected with a third, vertical cut. The skin and subcutaneous tissue were removed, and musculus gluteus maximus was dissected. After that, gluteus medius muscle was dissected with a second vertical cut. Then, we approached the deep layer of gluteal region where we prepared the piriform muscle, and neurovascular elements which travel above and below it through the suprapiriform and infrapiriform foramen. In the next phase of dissection, the sciatic nerve was prepared in the posterior femoral region up to its terminal ramification. Blood vessels involved in the blood supply of the sciatic nerve were carefully prepared in the gluteal region, posterior femoral region and popliteal fossa, with simultaneous detection of their origin. Results Nutrient arteries of the sciatic nerve originated from inferior gluteal arteries, medial circumflex femoral artery, perforating arteries and popliteal artery. These arterial branches approached the sciatic nerve at its anterior and posterior surface, and then in most cases split into ascending and descending terminal branches (T-shaped ramification). Less frequently, nutrient arteries pierced the trunk of the nerves or descended along its surface for a certain length; afterwards, they would disappear among its fascicles. Accompanying artery of the sciatic nerve was observed in all cases, as a branch of the inferior gluteal artery. It approached the sciatic nerve at its posterior surface below the piriform muscle (Figs. 1, 2 ). In spite of variations of the blood vessel length, it extended most frequently up to the level of the gluteal fold, supplying thus sciatic nerve segment located in the gluteal region. We did not observe presence of a persistent primitive sciatic artery in the entire sample of fetal lower extremities. 3

Next artery of studied nerves was branch of the medial circumflex femoral artery. It traveled below the quadratus femoris muscle, and approached the sciatic nerve at its anterior surface at the gluteal fold level. This blood vessel has been observed in 45 lower extremities (93.75%) and, in most cases, it split into ascending and descending terminal branches (Figs. 1, 2). The anastomotic blood vessel connecting medial circumflex femoral artery branch with terminal part of the accompanying artery of the sciatic nerve was very often; ascending branch of the first perforating artery was also observed, although its caliber was small. Nutrient arteries of the sciatic nerve originated from the perforating arteries in the posterior femoral region (Figs. 1, 2). The first perforating artery gave off the branch for blood supply of the sciatic nerve in 47 samples (97.92%), the second perforating artery in 38 (79.16%), whereas the third perforating artery gave off nutrient branch for the sciatic nerve in 9 lower extremities (18.75%). In most of the cases these nutrient branches divided into ascending and descending branches, and their anastomoses were visible along the sciatic nerve trunk. Popliteal artery gave off nutrient branch mainly for terminal ramification of the sciatic nerve in 4 lower extremities (8.3%). An arterial anastomotic chain of the sciatic nerve was observed in 36 lower extremities (75%). It was composed of the inferior gluteal artery, medial circumflex femoral artery, and the first two perforating artery branches (Fig. 3). Besides these arteries, the sciatic nerve vascularization of 7 lower extremities (14.5%) included branch of the third perforating artery (Figs. 2, 3). The age and gender of fetuses did not influence morphology of the sciatic nerve vascular scheme. Fig. 1. Nutrient arteries of parts of the fetal sciatic nerve in the gluteal and posterior femoral region; left fetal lower extremity. MGM = Gluteus medius muscle; PM = piriform muscle; IGA = inferior gluteal artery; AASN = accompanying artery of sciatic nerve; SN = sciatic nerve; CPN = common peroneal nerve; TN = tibial nerve; a = branch of medial circumflex femoral artery; b = first perforating artery; c = second perforating artery; d = third perforating artery.

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Fig. 2. Nutrient arteries of the fetal sciatic nerve in the gluteal region (left) and posterior femoral region (right); left lower extremity. MGM = Medius gluteus muscle; PM = piriform muscle; SGA = superior gluteal artery; IGA = inferior gluteal artery; AASN = accompanying artery of the sciatic nerve; SN = sciatic nerve; a = branch of medial circumflex femoral artery, b = first perforating artery; c = second perforating artery; d = third perforating artery.

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Fig. 3. The most frequent vascular scheme of fetal human sciatic nerve (left) is composed of an accompanying artery of the sciatic nerve, branch of the medial circumflex femoral artery, and nutrient branches of the first and the second perforating artery. Less frequently, this vascular scheme included branch of the third perforating artery (right). AASN = Accompanying artery of the sciatic nerve; SN = sciatic nerve; a = branch of medial circumflex femoral artery; b = first perforating artery; c = second perforating artery; d = third perforating artery.

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Discussion One of the possible complications which may occur during orthopedic and other surgical interventions is a paralysis of peripheral nerves in the operative area. The most probable cause of this postoperative complication might be injury, compression, torsion or stretching of the nerve. A recent opinion is that ischemia of the nerve as a result of thrombosis or embolism of the blood vessels has an important role in the nerve paralysis. For example, paralysis of the common peroneal nerve often occurres after intraaortic dilatation, iliac endarterectomy, aorto-iliac bypass or femoral arteriography (Kadiyala et al., 2005). Considering that peripheral nerves get segmental vascularization from the neighboring muscular and cutaneous branches or arterial main trunks, question that arises is following: are all nerves or all nerve segments sufficiently supplied, and are collateral anastomoses sufficiently developed to prevent ischemia of the nerves? Due to research of blood supply of the common peroneal nerve in the popliteal fossa, Kadiyala et al. (2005) concluded that blood supply of the proximal part of the nerve originated in two thirds of the cases from the direct branch of the main trunk of the popliteal artery, but the long part of the nerve, which travels along the neck of the fibula, was comparatively insufficiently supplied by few intraneural blood vessels with a small caliber. This observation indicates that this segment of the nerve shows predisposition for different pathological and traumatic insults. In anatomical textbooks, the accompanying artery of the sciatic nerve was described as a branch of the inferior gluteal artery, which travels along the sciatic nerve giving it the blood supply (Williams et al., 1995). Taking other literature into consideration, this artery becomes significantly more important in the case of the presence of persistent sciatic artery. During our research, we did not detect the presence of a persistent sciatic artery which can be explained by the comparatively small sample in respect to the known frequency of this important vascular abnormality in the human population. On the other hand, there was obvious presence of the accompanying artery of the sciatic nerve as a branch of the inferior gluteal artery. This blood vessel approached the nerve trunk at the posterior surface, below the piriform muscle, and then traveled at its posterior surface up to the level of the gluteal fold where it penetrated into the nerve and was not visible any more. In addition, we observed that perforating branches of deep femoral artery, such as medial circumflex femoral artery and perforating arteries, were also involved in blood supply of the sciatic nerve. The neural branch of the medial circumflex artery was detected in 93.75% of cases. It arose below the inferior margin of the quadratus femoris muscle, approached the nerve trunk at the anterior surface, and continued to travel down the nerve or divided into the ascending and descending branch. The anastomosis of this artery with branches of medial and lateral circumflex femoral and the first perforating artery, Sunderland (1968) marked as “crucial anastomosis” although this blood vessel is rarely visible because of its small caliber. In the posterior femoral region, nutrient arteries originated from perforating arteries, and they approached the nerve at the anterior surface. The first perforating artery gave off the branch for blood supply of the sciatic nerve in 97.92%, the second perforating artery in 79.16%, whereas nutrient branch of the third perforating artery and popliteal artery gave much lower percentages. Majority of nerve arteries end in connective tissue covering the nerve, and divide up into ascending and descending branches of variable length and caliber. Due to mutual anastomoses, the nutritive arteries formed continued anastomotic chain within the sciatic nerve, from the location where it exits the pelvic cavity up to its terminal ramification. In 75% of all cases, this chain was composed of the branches of the inferior gluteal artery, medial circumflex femoral artery, and the first two perforating arteries. In 14.58% of cases, this arterial chain included nerve branch of the third perforating artery. Although the branch of third perforating artery was observed in 18.75% and branch of popliteal artery in 8.3% of the 7

cases, it can be concluded that terminal parts of the sciatic nerve as well as its terminal branches are the most insufficiently supplied. However, the possibility of rich intraneural arterial network presence in these segments of the sciatic nerve cannot be excluded. Using the cadaver material, Sunderland (1968) observed same sources for blood supply of the sciatic nerve from which direct nutrient branches arise, as well as indirect nutrient branches from arterial chain at the posterior surface of the adductor magnus muscle. The anastomotic arterial chain of the sciatic nerve is similar to the arterial chain at the posterior femoral side. These series of anastomoses form the arterial network which connects the internal iliac artery with the deep femoral and popliteal artery, and through it collateral circulation can be established in the case of femoral artery occlusion or tying. It can be assumed that the arterial network of the sciatic nerve has a similar function. In their descriptive study of the rat sciatic nerve blood supply, Bell and Weddell (1984) described two main blood vessels with accompanying veins supplying the nerve in the thigh region: accompanying artery of the sciatic nerve, and popliteal artery. After microradiography, these authors detected a blood vessel approaching the nerve in the middle of the thigh region in approx. 50% of the examined rats. Their view is that this blood vessel corresponds to the anastomotic branch in humans, which connects the medial circumflex artery with the inferior gluteal artery and its branches. The popliteal fossa can be considered as embryological “crossroad”, because it hosts several vascular rearrangements due to regression and replacement of the embryonic axial artery of the lower extremities. After regression and involution of the axial artery, accompanying artery of the sciatic nerve remains in adults, proximal to the tendinous opening of the adductor magnus muscle. Here, during the embryological period, the axial artery anastomoses with the developing femoral artery, and continues inferiorly as the popliteal artery (Kadiyala et al., 2005). In all cases, the accompanying artery of the sciatic nerve is detected as rudimentary blood vessel. Arterial branches of medial circumflex femoral artery and perforating arteries for the sciatic nerve originate from the femoral artery. It can be assumed that different embryological origin of the sciatic nerve nutrient arteries can influence the arrangement, density and caliber of the intraneural vascular network. Kadiyala et al. (2005) cite different embryological arterial origin for the proximal and distal parts of the common fibular nerve, and particularly insufficient blood supply of the nerve part traveling along the neck of fibula. Although largest part of the sciatic nerve receives blood supply from the branches of femoral artery, its atherosclerotic changes and decrease in the caliber of its lumen may influence blood flow through the intraneural vascular network of the sciatic nerve. However, peripheral nerves themselves show considerable resistance to ischemia, because they have two distinct vascular systems – the extrinsic and intrinsic one, which are richly interconnected. The question arise how high is the upper limit of tolerance for ischemia of the sciatic nerve, until nerve fibers functional disturbance and peripheral neuropathy start. According to Stolarczyk et al. (2000), detailed anatomical studies of the nerves blood supply provide bases for the functional studies. Anatomical data presented in our study contribute to improving our understanding of arterial anastomotic chain of the sciatic nerve. It can help surgeons doing interventions on the very nerve or its surrounding tissue.

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Arterial Blood Vessels of Human Fetal Sciatic Nerve Cells Tissues Organs 186:147-153 (2007) [http://www.karger.com/cto]

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