J. Anat. (1989), 166, pp. 113-1 19 113 With 7 figures Printed in Great Britain An anatomical investigation of the nasal venous vascular bed in the dog

MARY A. AND JAMES C. C. WANG Department of Physiology, Faculty of Medicine, University of Hong Kong, Li Shu Fan Building, Sassoon Road, Hong Kong (Accepted 18 February 1989)

INTRODUCTION Early studies of the nasal mucosa provide a rather general description of the nasal vasculature - precapillary resistance vessels supply blood to subepithelial and periglandular networks, superficial and periosteal plexuses of sinusoidal venous vessels drain into and numerous arteriovenous anastomoses allow the blood to bypass the capillary network (Dawes & Prichard, 1953; Cauna, 1982). Recently, we have discovered that the nasal mucosa has two functionally separate venous passageways: a system of high flow and high pressure draining the anterior nasal cavity via the dorsal nasal and a system of low flow and low pressure draining the posterior nasal cavity via the sphenopalatine vein; the high flow and high pressure of the anterior venous system is due to the presence of an arteriovenous anastomotic flow (Lung & Wang, 1987). We have confirmed, by means ofmicroscopic examination ofvascular casts ofthe nasal mucosa, that arteriovenous anastomoses are located only in the anterior nasal cavity (Wang & Lung, 1985). As the nasal mucosa blood drains ultimately into the jugular , neck occlusion will bring about a transient cessation ofoutflow from the entire nasal vascular bed and, as a consequence, equalisation of pressure in all venous channels if they are in free communication. However, we have found that neck occlusion does not lead to equalisation ofpressure throughout the anterior and posterior venous systems, indicating the existence ofsome anatomical structure(s) causing the separation of pressure and flow in the two systems (Lung & Wang, 1987). The aim of the present study is to re-investigate systematically the vascular arrangements and anatomical characteristics of the nasal venous vascular bed so as to elucidate the anatomical mechanism(s) responsible for functional separation of anterior and posterior venous systems. Some of the results have been presented in abstracts (Lung & Wang, 1988; Wang & Lung, 1988).

MATERIALS AND METHODS Mongrel dogs with mesoticephalic type of skull (body weight 15 + 2-5 kg; n = 20), of either sex, were anaesthetised with sodium pentobarbitone (25 mg/kg) intra- venously. An infraorbital incision was made and the zygomatic bone was removed to expose the internal maxillary as well as its infraorbital and terminal branches. The infraorbital artery was cannulated retrogradely for injection of filling material or fixative into the nasal arterial vascular bed. The sphenopalatine vein, which accompanies the sphenopalatine artery, and the dorsal nasal vein, which lies above the nasal bone, were exposed and cannulated for the injection of filling material or fixative into the nasal venous vascular bed. The animal was then killed by an overdose of 114 MARY A. LUNG AND J. C. C. WANG sodium pentobarbitone (250 mg/kg) after intravenous injection of heparin (2000 units). Studies on vascular arrangements Injection material was introduced into the nasal vascular bed on both sides as previously described (Lung & Wang, 1987). In brief, a coloured latex solution (Powell Laboratories, OR, U.S.A.) was infused slowly into the nasal venous catheters at a pressure not higher than 50 mmHg while latex solution ofanother colour was similarly injected via the infraorbital arterial catheter at a pressure of 100 mmHg after occlusion of the internal maxillary artery with a snare. For the resin vascular casts, colourless or coloured partial polymerised methyl methacrylate mixture (ICI, Herts, U.K.) was infused instead. The animal was placed in a head-down position overnight in a cold room to allow for the setting of the vascular cast. For the latex vascular cast, the mucosa of the nasal cavity was removed and the soft tissues were air-dried. For the resin cast, the maxilla and the whole bony nasal cavity were removed from the body and underwent decalcification in Plank-Rychol solution for a week; the remaining soft tissues were macerated in 15 % potassium hydroxide solution and the cast was washed in running water until clean and then air-dried. Examination and photography of the vascular casts were carried out with the dissecting microscope (M650, Wild). Histological studies Nasal mucosa was removed from the nasal cavity anteriorly to the level of the dorsal nasal vein and posteriorly to the level of the sphenopalatine vein. The specimen was fixed in buffered 10% formalin solution, embedded in paraffin wax, serially sectioned at 10 ,tm, stained with Weigert's haematoxylin and counterstained with Van Gieson's picro-fuchsin solution for identification of elastic tissues, collagen fibres and vascular smooth muscle (Disbrey & Rack, 1970). In some dogs, buffered 10 % formalin solution, warmed to a temperature of 40 °C, was infused into the nasal vascular bed via the arterial and venous catheters for five minutes. For studies on vascular arrangements, resin was injected as described above. For histological studies, low melting point paraffin wax was liquefied by heating to the temperature of 40 °C and was then infused into the nasal vascular bed in the same manner. On solidification, the wax maintains the shape of blood vessels at the time of fixation during their subsequent histological treatment.

RESULTS Anterior venous drainage Examination of the latex and resin casts of the anterior nasal cavity revealed that venous vessels (0-1-0-5 mm in diameter) draining blood from the anterior part of the septum curved dorsally and, together with the venous vessels (0- 1-05 mm in diameter) draining blood from the anterior part of the nasoturbinate and lateral wall, formed a venous network lateral to the nasal bone. Two to three collecting veins (0 5-l mm in diameter) arose from the venous network and they joined a few venous vessels (0'5-1 5 mm in diameter) which drained blood from the pear-shaped anterior maxilloturbinate to form the dorsal nasal vein near the nasomaxillary suture. The dorsal nasal vein emerged from the piriform aperture and curved posteriorly to travel along the external lateral surface of the maxilla. The left and right dorsal nasal veins (2-3 mm in diameter; 2-2 5 cm in length) were connected by several anastomotic vessels (0 5-l mm in diameter) forming a venous network above the nasal bone. The Nasal venous system in dogs 115

Fig. 1. Diagram illustrating macroscopic arrangements of the anterior and posterior venous systems. (1) Orbital plexus; (2) ophthalmic vein; (3) facial vein; (4) external maxillary vein; (5) external jugular vein; (6) internal maxillary vein; (7) deep facial vein (reflex vein); (8) sphenopalatine vein; (9) medial collecting vein; (10) septal collecting vein; (11) lateral collecting vein; (12) dorsal nasal vein; (13) ethmoturbinates; (14) septum; (15) maxilloturbinate; (16) nasoturbinate; (17) anastomotic veins of the left and right dorsal nasal veins. dorsal nasal vein later gave rise to the angular and facial veins. The macroscopic arrangements of the anterior venous system are illustrated in Figure 1. Histological examination of the mucosa showed that the wall thickness of the anterior veins increased towards the anterior end of the nasal cavity. The of the wall of the dorsal nasal vein was much thicker than that of an ordinary vein of similar size. Parietal bicuspid valves were found to occur at intervals in the anterior veins and ostial valves were also found to be present at the entries of tributaries into the collecting veins and the dorsal nasal vein (Fig. 2a-d). Posterior venous drainage Examination of the latex and resin casts of the posterior nasal cavity revealed that numerous venous vessels (0 1-0 3 mm in diameter) draining blood from the scroll- like posterior part of the maxilloturbinate joined the venous vessels (0 2-0 8 mm in diameter) from the maxillary sinus and lateral nasal gland to form a large collecting vein (35-A45 mm in diameter; 1 5-25 cm in length) which lay laterally in the posterior nasal cavity. Venous blood from the posterior part of the nasoturbinate, the septum and the ventral wall drained via a smaller collecting vein (1[5-2 5 mm in 116 MARY A. LUNG AND J. C. C. WANG diameter; 1-2 cm in length) which lay close to the septum. Venous blood from the ethmoturbinates and the posterior part of the dorsal wall drained via a third collecting vein (2 5-3 5 mm in diameter; 1-15 cm in length) which lay medially in the posterior nasal cavity. The septal and medial collecting veins joined the lateral collecting vein near the entrance of the sphenopalatine foramen. The lateral collecting vein emerged from the sphenopalatine foramen as the sphenopalatine vein (0O5-1l5 mm in diameter; 1 5-2-5 cm in length) which later gave rise to the deep facial vein (Fig. 3 a-b). The macroscopic arrangements of the posterior venous system are illustrated in Figure 1. Histological examination of the mucosa showed that the posterior collecting veins had very large lumina of irregular shape and a very thick tunica media (even up to 0O05 mm in thickness for the lateral collecting vein). In transverse sections of the collecting veins, the thickness of the muscle layer was found to vary greatly in different parts of the wall, indicating an uneven distribution of tunica media in the collecting veins. The sphenopalatine vein had a much thinner and evenly distributed tunica media, comparable to that of an ordinary vein. Parietal bicuspid valves were found to be present in both sphenopalatine and collecting veins and ostial valves were also present at the entries of tributaries into the collecting veins (Fig. 4a-b). Mucosa over turbinates and walls of the nasal cavity Vascular arrangements of the nasal mucosa have been described in detail in previous studies (Wang & Lung, 1985; Lung & Wang, 1987). In brief, latticework patterns of veins were clearly seen throughout the mucosa. The subepithelial venous plexus, composed of small, intertwining and interconnecting veins, was especially dense over the vestibular area. The periosteal venous plexus over the lateral wall, ventral part of the septum and ethmoturbinate was composed of long, straight and loosely packed veins whereas those over the dorsal and ventral walls and the folded areas of the nasoturbinate and maxilloturbinate were of short, convoluted and closely packed veins. Arteriovenous anastomoses, draining directly into the periosteal venous plexus, were present in large numbers in the anterior nasal cavity but could not be identified in the ethmoturbinate and the posterior nasal cavity; they were confirmed also histologically in the present study. Histologically, the venous plexuses had the appearance of a large vascular cistern interrupted by septa or trabeculae composed of collagen and elastic fibres, sometimes reinforced with vascular smooth muscle. Such an appearance is most probably caused by sections of a closely-packed mesh-like venous network rather than by the actual existence of septa or trabeculae within the large venous vessels. Veins of the subepithelial plexus were basically of the thin-walled type, i.e. the wall comprised a single layer of and one to two layers of vascular smooth muscle. The periosteal plexus consisted of veins that were not only of the thin-walled type but also of the thick-walled type, i.e. the wall contained a number of layers of vascular smooth muscle. Like the posterior collecting veins, the thick-walled periosteal veins in transverse sections often demonstrated uneven thickness of the muscle layer in different parts of the wall. Cauna & Cauna (1975) described the presence of cushioned veins in the glandular zone of the human nasal respiratory mucosa from the lower border of the inferior concha or from the septum. It is very possible that these cushioned veins are actually thick-walled veins sectioned in a partially collapsed condition. Parietal values were present in both thin-walled and thick-walled periosteal veins but were less frequent in the superficial venous plexus. The distance between the valves in the thin-walled veins ranged from0O4 to0O6 mm. The parietal valves were Nasal venous system in dogs

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Fig. 2 (a-d). Sections of the dorsal nasal vein and its tributaries showing the thickness of the tunica media of the walls of the vessels and the presence of parietal and ostial valves. (a) Transverse section of dorsal nasal vein and two tributaries. H & PF, x29. (b) Longitudinal section of dorsal nasal vein cut at the same level as (a), bar, 5 mm. (c) and (d) Transverse sections at entries of tributaries into the dorsal nasal vein (v) of specimen treated with warm formalin and wax injection. H & PF, x90. Large arrows, parietal bicuspid valves; small arrows, ostial valves.

Journal of Anatomy, Vol. 166 MARY A. LUNG AND JAMES C. C. WANG

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Fig. 3 (a-b). Sphenopalatine vein and collecting veins of the posterior venous system. (a) Dissection of the posterior venous system after latex casting and removal. (b) Resin cast of the posterior venous system. s, sphenopalatine vein; vl, lateral collecting vein; vm, medial collecting vein; vs, septal collecting vein; m, maxilloturbinate; arrows, sphenopalatine artery and its branches. Nasal venous system in dogs

Fig. 4 (a-b). (a) Coronal section of mucosa of posterior nasal cavity 5 mm proximal to the sphenopalatine foramen. x20. (b) Magnified rectangle of (a) showing the large thick-walled and valved collecting veins. x97. a, sphenopalatine artery; n, sphenopalatine nerve; V,, thick-walled collecting vein; V2, thin-walled periosteal vein; g, glandular tissues; m, mucosal surface exposed to the nasal cavity; nc, nasal cavity; arrows, parietal valves. H & PF. MARY A. LUNG AND JAMES C. C. WANG

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Figs. 5-7. Parietal valves in nasal mucosa, over the posterior part of nasal septum (Fig. 5, x150), over the anterior ventral wall of nasal cavity (Fig. 6, x150), over the anterior nasoturbinate (Fig. 7, bar, 0.3mm). a, artery; V , thick-walled vein; V2, thin-walled vein; arrows, biscupid parietal valves, g, glandular tissue; c, cartilage. H & PF. Nasal venous system in dogs 117 abundant at the two extremities of the nasal cavity but could hardly be found in the middle portion (Figs 5, 6, 7). Observation of the resin cast showed that constrictions occurred at the entry points of tributaries into the thick-walled periosteal veins, and the constrictions were much more prominent if the mucosa was pretreated with warm formalin solution before resin injection, suggesting the presence of ostial valves (see Discussion). DISCUSSION Earlier clinical observations have shown that the nose may become instantaneously obstructed and an obstructed nose may open as promptly as though a valve controlled the circulation (Eggston & Wolff, 1947). However, all previous works on the anatomy of the nasal mucosa have reported that the nasal veins are devoid of valves (Dawes & Prichard, 1953; Miller, Christensen & Evans, 1964; Cauna, 1982). This is the first study demonstrating the presence of both parietal and ostial valves in the nasal venous vascular bed. It is well known that the function of valves is to prevent reversal of direction of blood flow in the veins (Franklin, 1937). The venous valves prevent the mixing of blood in the different venous channels and therefore are the anatomical structures responsible for the existence of two nasal venous systems which differ in their pressure and flow rates. The two nasal venous systems may serve different functions and hence valves are essential for their functional separation, i.e. alterations of blood flow or vascular condition of either system in response to sudden changes in functional demand can be achieved independently of the other. For example, on exposure to a cold environment, the arteriovenous anastomoses of the nasal mucosa, like those of the skin, may cause a tremendous increase in blood flow in the anterior venous system without affecting blood flow in the posterior system. However, further experiments are required to verify these physiological changes. The presence of valves in the nasal venous vascular bed may be advantageous to the nose in its function as a respiratory passageway. As the nasal mucosa is exposed directly to the air passages, its blood vessels are subject to the fluctuations in the nasal airway pressure and air current throughout the respiratory cycle. With inspiration, the negative nasal airway pressure exerts a sucking effect on the veins, and, in particular, on the thin-walled superficial and periosteal veins, resulting in an increase in mucosal vascular capacity and, subsequently, a hindrance to venous outflow and an increase in nasal airway resistance. Such changes become very marked when the respiratory demand greatly increases during strenuous exercise. If nasal veins are valveless, there could even be a retrograde venous blood flow to fill the greatly enlarged venous plexuses. However, physiological studies show that nasal airway resistance decreases during inspiration (Eccles & Lee, 1981) and also in proportion to the increase in minute ventilation (McCaffrey & Kern, 1979), and these changes are essential for the respiratory system to cope with the increased respiratory airflow without excessive expenditure of energy. Although it has been found that the nasal airway response to respiratory rhythm and during exercise may be due to changes in the vasomotor tone of the nasal vasculature (Asakura et al. 1986), we cannot rule out the possibility that venous valves may play a part in preventing retrograde venous blood flow and, hence, an increase in nasal airway resistance under these conditions. Modification ofthe respiratory air within the nasal cavity takes place predominantly over the scroll-like turbinates (Cole, 1988a). The capillary networks have been thought to be responsible for modifying the respiratory air (Cauna, 1982). Since venous valves are less frequently found in the superficial veins and are practically absent over the turbinates, the superficial venous plexus over these areas, like the capillary network, acts as a 'blood sheet' with blood flowing randomly within the 118 MARY A. LUNG AND J. C. C. WANG plexus despite changes in the phases of the respiratory cycle and, hence, favours modification of both inspiratory and expiratory air. Although parietal valves are practically absent over the turbinates and in the middle region of the nasal cavity, ostial valves may be present guarding the entries of superficial veins into the periosteal veins and collecting veins of both venous systems. Their presence is suggested in specimens pretreated with warm formalin solution which maintains constriction at the level ofthe valve due to contraction ofthe vascular smooth muscles of the cusp at the time of fixation (Elias & Feller, 1926). The ostial valves, in the hepatic veins of man and dogs, have been found to function as a throttle mechanism regulating liver outflow (Bauer, Dale, Poulsson & Richards, 1932). Likewise, the ostial valves, if present in the nasal mucosa covering the turbinates, may also act as a flow regulator, controlling outflow from the superficial venous plexus into the periosteal venous plexus. Mucosal congestion in patients with nasal rhinitis has been thought to be due to a disturbance in autonomic nervous activity leading to vasodilatation and, hence, an increase in the filling of the 'erectile' tissues, i.e. the venous plexuses, of the turbinates (Holmes, Goodell, Wolf & Wolff, 1950). Since the periosteal veins are of greater number and of greater capacity than the superficial veins, mucosal congestion is more likely due to blood engorgement in the periosteal venous plexus rather than in the superficial venous plexus. If this is the case the ostial valves, which control blood flow from the superficial veins to the periosteal veins, may be a key mechanism explaining mucosal congestion in nasal rhinitis. The major anatomical difference between the nasal venous systems lies in their collecting veins. The posterior veins are much larger and contain a much greater amount of musculature than those of the anterior venous system. Airflow through the nasal cavity has to pass in between these collecting veins as they are located at the level of the posterior nares. Nasal airway resistance has been thought to reside predominantly in the vestibular area ofthe anterior nasal cavity and, to a lesser extent, the erectile mucosa clothing the turbinates in the middle nasal cavity (Cole, 1988 b). However, the collecting veins of the posterior venous system, because of their large size and enormous amount of vascular smooth muscle, on dilatation would increase greatly the nasal airway resistance. Hence, the nasal airway obstruction of nasal rhinitis may involve not only mucosal congestion of the turbinates but also blood engorgement in the collecting veins of the posterior nasal cavity. In epistaxis, almost all nose bleeds of the anterior type stop without treatment or with no more than compressing the nose until bleeding ceases. However, posterior nose bleeds are usually more severe and frequently necessitate hospitalisation because bleeding may recur when the packing is removed or may even continue with packing in place. The bleeding site is usually well back in the nose along the lateral wall, below the inferior turbinate or high above the middle turbinate (Saunders, 1980). Hence, it seems likely that posterior epistaxis may be due to the rupture of the large collecting veins of the posterior nasal venous system.

SUMMARY Physiological experiments have demonstrated that the canine nasal mucosa has two venous systems that differ in blood pressure and flow. An investigation of the vascular arrangements and histological characteristics of the nasal venous vascular bed was performed to search for anatomical structure(s) responsible for their functional separation. Parietal bicuspid valves were found to be present in both venous systems, being particularly abundant at the two extremities of the nasal cavity and less frequently found over the turbinates. Ostial valves were found to be present guarding Nasal venous system in dogs 119 the entries of tributaries into the periosteal venous plexus, collecting veins and outflow veins of the nasal mucosa. The collecting veins of the posterior venous system were found to be much larger and to contain a greater amount of muscle than those of the anterior venous system. The parietal valves are suggested to be the anatomical structures responsible for the functional separation of the two venous systems whereas the ostial valves might act as a throttle mechanism, regulating blood flow into the cavernous periosteal venous plexus and the collecting veins of the posterior venous system. The physiological significance of the presence of venous valves and their distribution in the nasal mucosa as well as the probable functions of the collecting veins of the posterior venous system are discussed. The work was supported by Hong Kong University Research Fund (337/034/0005) and Sun Yat Sen Foundation Fund for Medical Research (378/030/8114). The cost of reproduction of colour plates was subsidised by Hong Kong University Medical Faculty Grant for Medical Publications (365/030/4254/4F). We thank the Histo- logical Unit of the Anatomy Department, University of Hong Kong, for assistance in histological preparations and Dr Y. C. Wong for helpful discussions.

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