Clin Onil Impl Ro IWV: /(): 34-44 Primed in Denmark All righis reserved

Clip 111;,' 11:

Munksgaarsi 1999

CLINICAL ORAL IMPLANTS RESEARCH

ISSNOW5-7I61

Blood supply to the maxillary sinus relevant to sinus floor elevation procedures
Solar P, Geyerhofer U. Traxler H, Windisch A. Ulm C. Watzek G. Blood supply to the maxilUiry sinus relevant to sinus floor elevation procedures. Clin Oral Impl Res 1999: 10: 34^44. Munksgaard 1999. The niaxilUiry blood supply is essential for preserving the vitality ofthe affected maxillary region, integration ofthe grafting material, and wound healing such as following sinus floor elevation. Although it Is well established that edentulous maxillae demonstrate a decreasing vascularity as bone resorption progresses, the vascular conditions relevant to sinus floor elevation procedures have not been investigated yet. This study deals with maxillary arteries relevant to sinus floor elevation surgery and examines the vascularization ofthe lateral maxilla after tooth loss. The vessels of the lateral maxilla of 18 maxillary specimens (10 male. 8 female, mean age 67 years) were prepared anatomically and the local main arteries, the number of macroscopically discernible branches and anastomoses, their calibers, and the distance between the caudal main branches and the alveolar ridge recorded. The lateral maxilla is supplied by branches of the posterior superior alveolar artery (PSAA) and the infraorbital artery (IOA) that form an anastomosis in the bony lateral anlral wall, which also supplies the Schneidcrian membrane. This intraosseous anastomosis was found in all ofthe specimens. Eight of 18 also showed an extraosseous anastomosis between PSAA and IOA. vestibular to the antral wail, giving off an average of 3 branches cranially and 5 branches caudally. The two anastomoses form a double arterial arcade to supply the lateral antral wall and. partly, the alveolar process. The PSAA had a mean caliber of 1.6 mm and exhibited an average of 2 endosseous and 1 extraosseous branches. The IOA had a mean diameter of 1.6 mm and showed an average of I endosseous and 3 extraosseous branches. The mean distance between the intraosseous anastomosis and the alveolar ridge was 19 mm in 2 defined measuring sites. Its mean length was 44.6 mm. The epiperiosteal vestibular anastomosis was situated further cranially. at a mean distance of 23 to 26 mm from the alveolar ridge and had a mean length of 46 mm. The rather huge caliber ofthe vessels supplying the lateral antral wall seems to be crucial to the fact that the periosteal blood supply is maintained even In severe maxillary atrophy and after complete disappearance of the centro-medullary vessels. Peter Solar\ Ursula Geyerhofer\ Hannes Traxler^, Alfred Windisch^ Christian Ulm\ Georg Watzek^
^ Department of Oral Surgery, Dental School, University of Vienna; ^Anatomical Institute, First Department, University of Vienna, Austria

Key words: sinus floor elevation maxillary artery - posterior superior alveolar artery - infraorbital artery biood supply Peter Solar, MD, DMD, Department of Oral Surgery, Dental School, University of Vienna, Waehringerstrasse 25a, A-1090, Vienna, Austria Tel.: ++431 40181 2500 Fax: 4-+431 40181 2807 Accepted for publication 8 June 1998

Internal augmentation of the antral floor for the creation of an adequate implant host site is very well documented from the clinical point of view (Boyne & James 1980; Watzek 1996; Nishibori et al, 1994; Jensen et al. 1994; Hurzeler et al. 1996; Haas et al. 1998a. b). A variety of techniques have been proposed concerning the grafting material and reports on autografts (Jensen & Sindet-Pedersen 199I;Caloneetal. 1992; Raghoebar et al, 1993; 34

Nishibori et al. 1994; Jensen et al. 1994; Williamson 1996; Block & Kent 1997; Daelemans et al. 1997; Neyt et al. 1997; Lorenzetti et al, 1998), homologous grafts (GaRey et al. 1991; Leder et al. 1993; Nishibori et al. 1994; Zinner & Small 1996; Wheeler 1997) and xenografts (GaRey et al, 1991; Moy et al. 1993; Wheeler et al. 1996; Quinones et al. 1997; Haas et al, 1998a; Valentini et al. 1998) have been published. However, one aspect that has

Blood supply to the maxillary sinus

Fig. I. Photograph of the lateral antral vi'all; tnedial view. The maxillary sinus becomes visible when the bony septum between the nasal cavity and the maxillary sinus, including the nasal conchae. are removed. The course of the intraosseous anastomosis between PSAA and IOA is discernible in tbe transmitted light ( ^ ) .

Fig. 3. View of a right maxilla from lateral: Posterior surface of the body of the maxilla and pterygopalatine fossa. The PSAA gives off 3 branches into bone (*) and courses anterocaudally (*) below the zygomatic process (ZP), maintaining close contact with bone. (PP: pierygoid process.)

Fig. 2. View ofa left maxilla. PSAA and IOA originate from the maxillary artery (MA) in a common trunk. The IOA courses cranially, to the floor of the orbita, and gives off I branch laterally (X)- The PSAA descends along the maxillary tuberosity, gives off I branch into bone, and forms a tortuous anastomosis (EA) with a terminal branch of the IOA (observed in 44% of the specimens).

Fig. 4. Antero-latera! view of a left maxilla. The IOA emerges from the infraorbital foramen together with the nerve of the same name. It gives off 2 branches anteriorly and passes caudaliy along the canine fossa, below the zygomatic process, to form an anastomosis with the PSAA. It supplies the periosteum of the anterior antral wall and the vestibular gingiva in the canine/premolar region via 2 to 3 branches on average. The arterial arcade supplying ihe lateral antra! wall comes from the PSAA and the IOA. The gingival branches of this anastomosis are discernible as well. They are located at a mean distance of 22.8 to 26 mm from the alveolar margin.

been barely investigated so far is the local arterial supply, on which the vitality of local bone, vascularization of the grafting material, and the healing behavior of the oral mucous membranes depend. While the maxilla is very densely vascularized in young and dentate subjects {Staudt et al. 1977;

Braun et al. 1985; Marx 1994; Bell et al. 1995), the blood supply to bone is permanently reduced with age and progressing atrophy and the number of vessels and their diameter decrease, while tortuosity increases (Staudt et al. 1977; Soikkonen et al. 1991). Atrophy and vascular reduction trigger a vicious

35

Solar et al.

Figs 5 and 6. Photographs of the lateral antriil wall, medial view. The maxillary sinus becomes visible, when the bone septum between the nasal cavity and the maxillary sinus, including the nasal conchae. is removed using a chisel. The course of the intraosseous anastomosis between PSAA and IOA is discernible in the transmitted light (). A second iotraosseous branch of the PSAA is visible in Fig. 6 (*). which also participates in the anastomosis.

circle within the bone in that atrophy aggravates vascular reduction and vice versa (Shibayama et al. 1993). Microvascular defects (Burkhardt et al. 1987), stenotic changes (McGregor & MacDonaid 1989), a reduction of intramedullary blood flow, inhibition of osteoblastic activity, a delay in bone mineralization (Kobayashi 1982), and. therefore, a reduction in cancellous bone (Demmler et al. 1983) occur. Gradual reduction of thecancellous portion ofthe alveolar ridge that is supplied by both centro-medullary and periosteal vessels (Chanavaz 1995) often reduces the antral floor to no more than a paper-thin lamella of compact bone (Watzek et al. 1993; Ulm et al. 1995). This lamella can no longer be supplied by centro-medullary vessels because of its small cross sec-

tion, so that the remaining cortical bone must be supplied purely periosteally Sound knowledge of the vessels supplying the local periosteum which will be affected during grafting procedures to augment the sinus floor volume is therefore essential from the surgical-technical point of view. The literature concerning the course of the vessels supplying this region is limited to anatomical textbooks (Sicher & Du Brul 1970; Lang et a l 1985: Gray's Anatomy 1989; Sobotta 1989; Brand & Isselhard 1990). Some studies describe vascular topography under different aspects (Skopakoff 1968; Bell & Levy 1975; Lang & Urban

MA

Fig. 7. Schematic representation ofthe left maxilla, lateral view, with blood vessels. The lateral bone wall with the zygomatic process has been removed. The IOA and the extraosseous anastomosis (EA) are marked by a continuous line and the intraosseous vessels (IA) of the lateral antral wall by a broken line.

Fig. 8. Schematic representation of a left maxilla, divided median-sagitta!ly. medial view, offering a good view of the maxillary sinus after removal of the wall between the nasal cavity and the maxillary sinus, including the nasal conchae. The double arterial arcade formed by PSAA and IOA is marked. The extraosseous anastomosis (EA) is situated approximately 3 to 7 mm further cranially than the intraosseous one (IA).

36

Blood supply to the maxillary sinus

Materials and methods

A total of 18 maxillary segments were obtained from cadavers used for dissection during gross anatomy courses for medical students. The cadavers were of both sexes (10 male and 8 female) with a mean age of 67 years (min 55 years, max 75 years). Sixteen specimens were completely edentulous and 2 dentate from the first incisor to the canine. The specimens exhibited Class 2 and Class 3 resorption of the alveolar process according to Cawood & Howell's classification of alveolar resorption (1988). Nine specimens were primarily fixed in formalin/phenol, while latex, Prontobario, and pigment were injected into the vessels of the 9 remaining specimens before fixation. After fixation, the skulls were divided into 2 halves sagittally. Only 1 skull half was used for the examination

Fig. 9. Schematic representation of the maxillary sinus, cranial view, after removal of the floor of the orbita.

PSAA

IOA

Fig. II. Photograph ofa frontal section through tbe maxillary sinus and the alveolar process. The bone canal in the buccal antral wall, housing the intraosseous vascular anastomosis between PSAA and IOA, is clearly discernible i-^). Its mean height in relation to the alveolar ridge is 18.9 to 19.6 mm.

Fig. 10. Schematic representation of the maxillary sinus, posterior view, after removal of the posterior antral wall. The IOA enters into the infraorbital canal (IC) and gives off the anterior superior alveolar artery (ASAA) before emerging from the canal. The vascular stumps of the PSAA left after removal of the posterior antral wall are marked.

1977; Navarro et al. 1982; Schumacher et al. 1988; Morton & Khan 1991; Pretterklieber et al. 1991; Kasey et al. 1996). No specific studies are available regarding the sinus floor elevation procedure. The aim of this study was to investigate the blood supply to the lateral and caudal antral wall.

Fig. 12. Intraoperative photograph of the bony window prepared in the lateral antral wall during a sinus floor elevation. The intraosseous anastomosis is discernible (->).

37

Solar et al.
Table 1, Results o! the topographic measuremenis of Ihe posterior superior alveolar artery Mean Full length (mm) Numbef of branches (endosseous and extraosseous) Number of endosseous branches Number oi extraosseous branches Caliber (external diameter at the exit trom the maxillary artery)' (mm) 'Comparative vaiues of the maxillary ariery: mean vaiue 2.6, standard deviation 0,33: min. 2.2, max- 3.2. 1,55 1.1 1.59 8.17 2.56 SD Min. Max.

3.62 0.98 0.98 0.32 0,21

16

I
1 1 1, 3

5
4 2 2.0

Table 2, Results of the topographic measurements of Ihe Inlraorbital artery /7=18 Number of endosseous branches [along the portion of ttie artery coursing within the infraorbital canai, before the artery emerges from ttie infraorbitai foramen) Mean 1,44

S D
0,51

Min

Max

stomoses, and number of branches were recorded. 3) The caliber of both PSAA and IOA was measured at the exit from the maxillary artery (using a caliper rule calibrated to 0.02 mm). 4) The following distances were measured: - the distance from the alveolar margin to the exit of the anastomosing artery branching off from the IOA; - the distance from the alveolar margin to the exit ofthe anastomosing artery branching ofT from the PSAA; - the length ofthe anastomosis between the exits of the 2 anastomosing vessels of PSAA and IOA. The mean values and standard deviations of the measuring results were calculated.

Results
2.67
1.64 0,97 0,48

Number of extraosseous branches

Caliber (exiernai diameter at the exit from the maxillary artery) [mm)

1
1,2

2,7

(left: /?=I0; right: n=%) since the other half was used for the students' anatomy courses. First, the maxilla was separated from the residual skull and the soft tissue removed. The zygomatic arch was then removed using a chisel and the vessels were dissected. To gain access to the maxillary sinus, the nasal conchae were removed and the lateral wall of the nasal cavity fenestrated using a sharp chisel. The maxillary artery and its 2 branches extending to the maxillary sinus, the posterior superior alveolar artery (PSAA) and the infraorbital artery (IOA), was exposed. The vessels were prepared under an operating microscope, starting from the maxillary artery to the terminal branches of the posterior superior alveolar artery and the infraorbital artery. The following examinations and measurements were carried out: 1) The PSAA was located and its topography, anastomoses, and number of branches were recorded. 2) The IOA was located and its topography, ana-

The posterior superior alveolar artery (PSAA) runs caudally, on the outside of the convexity of the maxillary tuberosity, and is in close contact with bone and periosteum (Figs 2 & 3). The PSAA has a mean caliber of 2 mm at its origin and divides into 2 branches after 8 mm. A terminal branch (^gingival branch) passes along the outside of the bone and supplies the mucoperiosteum in the premolar/molar region. This terminal branch anastomoses with the extraosseous terminal branch of the IOA in 8 of 18 of the specimens, coursing at a mean height of 23 to 26 mm from the alveolar margin. The second branch ofthe PSAA (dental branch) also forms an anastomosis with the IOA, which, however, courses endosseously, halfway up the buccal antral wall, at a distance of 18.9 to 19.6 mm from the alveolar margin (Figs II, 12). This anastomosis was found in all specimens examined. The infraorbital artery (IOA) originates from the maxillary artery, very close to the PSAA, in 12 of the 18 specimens and from a common trunk in 6 of 18 (Fig. 2). It has a mean caliber of 2 mm at its origin. The IOA emerges from the orbit, entering the maxillary sinus through the infraorbital fissure at a very high level. The artery runs in the infraorbital groove, through the infraorbital canal where it supplies the anterior and superior branches. It is situ-

Tabla 3 Height and lengtii of the vestibular anastomosis between ttie PSAA and the IOA Height 1 Mean mm 22.75 Height Max. Mean

2
Min, Max. Mean 47,25 SD

Lengih Min. 45 Max,

S D
1,49

Min.

S D
6.09

21

25

26

16

37

2,87

52

T?ie vestibuiar anastomosis was lound In 44% ot the specimens (n=8).

38

Blood supply to the maxillary sinus

Table 4. Height an(j length ot Ihe intraosseous anastomosis between PSAA and IOA

n=8
Mean m m 19.56

Height 1 S D 3.67 Min. 14 Max. 25 Mean 18.9

Height 1 S D 2.82 Min. M Max. 23 Mean 44.5 SD

Lengtfi Min, 37 Max. 50

4.72

Ttie endosseous anastomosis was found in 100% ot ttie specimens {n=18).

ated at the transition from the roof of the maxillary sinus to the vertical bone septum between the maxillary sinus and the nasal cavity. Before emerging from the infraorbital foramen, the IOA gives off 1 or 2 branches that course caudally along the anterior antral wall in a bone canal; the anterior and the middle superior alveolar arteries. One of these vessels anastomoses with the dental branch of the PSAA which also runs endosseously. This anastomosis vascularizes the Schneiderian membrane on the buccal side from anterior to posterior and the membrane at the lateral and caudal antral walls (Figs I, 5, 6). The oral mucoperiosteum is supplied by the vestibular anastomosis (Fig. 4) as well as by an average of 8 branches emerging directly from either the PSAA or the IOA or the anastomosis. Three branches extend cranially and 5 caudally on average. The mean values, standard deviations, and minimum and maximum values are shown in Tables 1 to 5.

Discussion
The vessels described in this study are only briefly touched upon in classical textbooks. Sicher & Du Brul (1970) mention an endosseous anastomosis between the PSAA and the IOA. However, most textbooks only briefly mention the endosseous branches of the PSAA and the IOA which supply the teeth in one short sentence (Lang et al. 1985; Gray's Anatomy 1989; Sobotta 1989; Brand & Isselhard 1990). None of the above textbooks refers to an extraosseous anastomosis. Furthermore, none of the common anatomy textbooks contains explicit illustrations of the blood supply to the maxillary sinus (Figs 7-10).

The results of this study indicate that vascularization of the grafting material placed in sinus floor elevation occurs via 3 routes: the endosseous vascular anastomosis, the extraosseous anastomosis, and the vessels of the Schneiderian membrane. The Schneiderian membrane at the lateral antral wall is supplied by the PSAA. the IOA. and their intraosseous branches and anastomoses. The middle portion of the Schneiderian membrane is supplied by the sphenopalatine artery, the terminal branch of the maxillary artery (Ranga & Andronescu 1968; Sicher & Du Brul 1970). The maxillary sinus exhibits a distinctly sparser vascular network than the nasal cavity (Ranga & Andronescu 1968), which is situated in the deepest layer ofthe lamina propria that rests directly on the periosteum (Selden 1974). Although most of its branches are dichotomous, there are also numerous recurrent branches, the ramifications sometimes being fascicular. The meshes of the capillary network are larger, the further away the area to be supplied is situated from the vascular trunk (Ranga & Andronescu 1968). However, sometimes the sinus floor can completely lack the lamina propria with its vessels (Selden 1974). A study in animals has revealed perfusion ofthe Schneiderian membrane of 0.09 ml to 0.99 ml/min/g body weight. In comparison, a cardiac output of 14636 ml/min/ g has been observed (Kumlien et al. 1985). A vestibular extraosseous anastomosis courses below the zygomatic process and is located at a mean distance of 23 mm from the alveolar ridge at its most caudal point. Even when no anastomosis is formed between the PSAA and the IOA, the main branches are located at this level in most cases. The vessels are in close contact with bone, the anastomosis being situated very closely to the mucoperiosteal region that has to be prepared as a flap to gain access to the maxillary sinus in sinus floor elevation procedures. Vertical mucosal incisions should therefore extend as little cranially as possible and the periosteum should be prepared with utmost care to minimize the vascular trauma and to prevent damage to the extraosseous anastomosis. Furthermore, the vertical incisions should be made at a great distance from each other to create as large a flap as possible, so that the tissue can be supplied by other branches of the PSAA.

Table 5. Number of branches given oft by the vestibular anastomosis and vestibuiar vesseis emerging trom the PSAA and the iOA Cranial Mean 3.1 SD 1.0 Min, 1 Max. 5 Mean 4.9 Caudai SD 1.5 Min. 3 Max. 8

39

Solar et al. wound healing process. Cohen (1994) described the formation of a partial-thickness flap, an incision through the palatine periosteum at a distance of approximately 15 mm from the alveolar ridge, elevation of the palatine periosteum from the alveolar ridge, and repositioning of the flap after impiant placement. However, when a 2-stage procedure is planned, the periosteal blood supply is interrupted twice when this type of incision is used. In this case, it is recommended to carry out the incision vestibular to the alveolar ridge in the first procedure, i.e.. the acttial sinus floor elevation procedure, and to use a palatal incision in the second procedure, i.e., when the implants are placed.

Osteotomy lines
In the specimens examined in this study, the endosseous anastomosis was situated at a smaller distance from the alveolar ridge than the extraosseous anastomosis, the mean distance at the most caudal site measuring 18.9 mm. As far as the type of osteotomy lines to be used in sinus floor elevation surgery is concerned, the findings of this study indicate that the bony window, through which the grafting material will be placed, should be as small as possible so that the vascular stumps of the endosseous anastomosis extend as close to the center of the graft as possible. Damage to the periosteum leads to bone necrosis as a result of ischemia and to partial regeneration of the underlying bone (Chanavaz 1995). The range of variability ofthe threshold for a decrease in vascular supply to the maxilla that will result in aseptic necrosis is unknown (Lanigan 1995). So far no studies are available describing the fate of local maxillary bone after periosteal denudation, vascularization of the graft, and revascularization of local tissue after sinus lift surgery. By taking into account that sinus lift procedures involve considerably less severe tissue traumatization than Le Fort I osteotomy, this is the only comparable surgical technique thoroughly investigated concerning maxillary blood supply (Nelson et al. 1977; Epker 1984; Yeo et al. 1989; Lanigan etal. 1990; You etal. 1990. 1991a. b; Bell et al. 1995; Berding etal. 1995; Geylikmanet al. 1995; Yang et al. 1995; Dodson et al. 1997). In the mildly resorbed alveolar process, bone receives blood from both centro-medullary and mucoperiosteal vessels, while increasing resorption gradually results in a purely mucoperiosteal vascularization. It is recommended to carry out a necessary sinus floor elevation as early as possible in order to forestall the onset of atrophy-related vascular reduction.

Fig. 13. (a. b) Schematic representation of a possible soft tissue incision. The vertical incisions should be made at great distance from each other to create as large a flap as possible ( ), so that the tissue can be supplied by other branches of (he PSAA. This possibility and the number of branches is reduced when a small flap is prepared ()- Vertical mucosal incisions should extend as little cranially as possible to minimize the vascular trauma and tc prevent damage to the extraosseous anastomosis.

This possibility and the number of branches is reduced, when a small flap is prepared (Fig. 13). Careful soft tissue preparation plays a crucial role in sinus floor elevation surgery since progressing atrophy of the alveolar ridge results in considerable changes in the blood supply to the tissue: bone scleroses as a result of resorption (Watzek et al. 1993; Ulm et al. 1995). its blood supply is reduced (Staudt et al. 1977; Kobayashi 1982; Demmler et al. 1983; Burkhardt et al. 1987; Bert et al. 1989; McGregor & MacDonaid 1989; Shibayama et al. 1993). and the originally combined centro-medullary/mucoperiosteal circulation (Chanavaz 1995; You et al. 1991a) gradually turns into a purely mucoperiosteal one. The use of an adequate surgical technique therefore gains increasing importance in progressing atrophy to avoid a deficit in blood supply to local bone. The horizontal soft tissue incision should be carried out slightly palatally as this not only offers a better view of the alveolar ridge but also allows inclusion of the palatine blood vessels in the 40

Blood supply to the maxillary sinus

Conclusion
The findings of this study indicate that the vascular supply to the buccal antral portions relevant to sinus floor elevation surgery occurs via 2 arteries; the posterior superior alveolar artery (PSAA) and the infraorbital artery (IOA). These arteries also vascularize the Schneiderian membrane of the lateral maxillary sinus and the local mucoperiosteum as a double arterial arcade. The rather large diameter of the vessels supplying the lateral antral wall seems to be crucial to the fact that the periosteal supply to local bone can be maintained even in severe maxillary atrophy and after complete disappearance of the centro-medullary vessels. Especially in the severely atrophic maxilla, the alveolar ridge should be denuded from its periosteum as little, as carefully, and as briefly as possible to minimize the impairment of blood flow. According to the findings of this study, it can be assumed that the periphery of the placed grafting material is supplied by vessels of the Schneiderian membrane and by intraosseous vascular bundles, while its center receives blood from collateral branches of the endosseous anastomosis, which should therefore extend as far into the center of the graft as possible, and from the periosteum of the repositioned mucoperiosteal flap. The endosseous anastomosis should therefore be transected only minimally, which might mean that the anteroposterior dimensions of the bony window should be as small as possible.

tere alveolaire superieure posterieure (PSSA) et I'artire infraorbitale (IOA) qui forment une anastomose dans la paroi de I'antre lateral osseux qui irrigue egalement la membrane de Schneiderian. Cette anastomose tntraosseuse a ete trouvee dans tous les specimens. Huit des 18 echantillons montraient egalement une anastomose extraosseuse entre PSAA et IOA. en vestibulaire de la paroi de I'antre, donnant en moyenne trois branches craniennes et cinq branches inferieures. Les deux anastomoses forment une arcade arterielle double qui irrigue la paroi de I'antre lateral et. en partie. le proces alveolaire. La PSAA a un calibre moyen de 1,6 mm et possede le plus souvent deux branches endoosseuses et une extra-osseuse. L'lOA a un diametre moyen de 1,6 mm et possede normalement une branche endo-osseuse et trois extra-osseuses. La distance moyenne entre l'anastomose intraosseuse et Ie rebord alveolaire etait de 19 mm dans deux sites mesures. La longueur moyenne etait de 44,6 mm. L'anastomose vestibulaire epiperiosteale etait situee plus cranialement a une distance moyenne de 23 a 26 mm du rebord alveolaire et avait une longueur moyenne de 46 mm. Le calibre relativement important des vaisseaux irriguant la paroi de Tantre lateral semble etre tres important par le fait que Tirriguation sanguine periosteale est maintenue meme dans les cas d'atrophie maxillaire severes et apres disparition complete des vaisseaux centro-mfedullaires.

Zusammonfassung
Die Blutversorgung des Oberkiefers stellt im Rahmen von Sinusboden-Elevationen einen wesentiichen Aspekt filr die Vitalerhaltung der betroffenen Kieferregion. fUr das Einheilen des Augmentates und fiir das Abheilen der Operationswunde dar. Obwohl sich die Vaskularisation des Oberkieferknochens mit fortschreitender Atrophie reduziert. wurde die nutritive Ausgangssituation bei Sinusliftoperationen bisher noch nicht untersucht. Die vorliegende Studie befaOt sich mit der arteriellen Versorgung des Oberkiefers im Hinblick auf die Sinusliftoperation und untersucht. aus welchen Quellen die Ernahrung des lateralen Oberkiefers nach Zahnverlust erfolgt. An 18 Oberkieferpr^paraten wurden die GefaBe der lateralen Maxilla anatomisch-praparatorisch dargestellt. Die lokalen Hauptarterien, die Anzahl ihrer makroskopisch darstellbaren Aste und Anastomosen. ihre Kaliber sowie die Distanz der caudal verlaufenden Hauptaste zum Kieferkamm wurden registriert und vermessen. Die Blutversorgung dieser Region erfolgt aus Asten der Arteria atveolaris superior posterior (AASP) und der Arteria infraorbitalis (AI). Aste dieser beiden GefaBe anastomosieren im Knoehen der lateralen Wand des Sinus maxillaris. verzweigen sich sehr dicht und versorgen damit auch die Kieferhohlenschleimhaut. Diese intraossare Anastomose war in 100"/. des Untersuchungsgutes nachweisbar. In 44% konnte auch eine extraossare, vestibular der Kieferhohlenwand verlaufende Anastomose zwischen der AASP und der AI festgestellt werden. Diese GefaBanastomose versorgt die orale Schleimhaut vestibuISr der Kieferh6hle mit durchschnittlich 3,1 Asten nach cranial und 4.9 Asten nach kaudal. Die beiden Anastomosen bilden eine doppelte arterielie Arkade zur Versorgung der lateralen Kieferhohlenwand und beteiligen sich an der Versorgung des Processus alveolaris. Die AASP hatte ein durchschnittliches Kaliber von 1,59 mm (min 1,3; max 2.0), hatte durchschnittlich 1,6 enossale Aste (min I; max 4) und 1,1 extraossSre (min 1; max 2). Das durchschnittliche Kaliber der AI betrug 1,64 mm (min 1.2; max 2.7), sie hatte durchschnittlich 1,4 enossale Aste (min 1; max 2) und 2.7 extraossSre (min 2; max 4). Die durchschtiittliche Distanz der intraossaren Anastomose zum Kieferkamm betrug 18,9 bzw. 19.6 mm an zwei definierten MeBstellen (min 14; max 25). Ihre mittlere Lange betragt 44,6 mm (min 37; max 50). Die epiperiostal verlaufende vestibuUre GefaBanastomose liegt etwas weiter kranial mit durchschnittlich 23 bis 23.5 mm Distanz zum Kieferkamm (min 16; max 37). Sie verlauft iiber eine Strecke von 46 mm (min 45; max 52). Die Vaskularisa-

Aoknowledgements
The authors wish to thank Ulla Arnold for making the graphic representations and Hedwig Rutschek. Bettina Maani, and the laboratory assistants ofthe Anatomical Institute ofthe University of Vienna for their inestimable assistance in preparing this manuscript.

Resume
L'alimentation sanguine maxillaire est essentielle pour preserver la vitalite des regions maxillaires affectees, l'integration du materiel greffe et la guerison suite a toute operation d'epaississement du plancher sinusal. Bien qu'il soit etabli que les maxillaires edentes aient une vascularisation diminuee avec la progression de la resorption osseuse, les conditions vasculaires durant les techniques d'epaississement du sinus n'ont pas encore vraiment ete explorees. Cette etude observe les arteres maxillaires importantes pour la chirurgie de I'epaississement du sinus et examine la vascularisation du maxillaire lateral apr^s la perte dentaire. Les vaJsseaux du maxillaire lateral de 18 maxillaires (dix hommes. huit femmes, moyenne d'age de 67 ans) ont ete prepares anatomiquement et les arteres locales, le nombre de branches observables macroscopiquement ainsi que les anastomoses, leurs calibres et la distance entre la partie inferieure des branche principales et le rebord alveolaire ont ete notes. Le maxillaire lateral est irrigue par des branches de Tar-

41

Solar et al.
tion der lateralen KieferhohJenwand mit relativ groBkalibrigen GefiiBen dtlrfte eine wesentliche Rolle dabei spielen. daB auch bei hochgradiger Kieferatrophie und vcilligem Verschwinden der zeniromedullaren Vaskularisaiion die periostale Ernahrung des lokalen Knoehen aufrecht erhallen werden kann.

(IOA)

Resumen
El ijportc sanguineo en cl maxilar es esenciai para preservar la vitalidad de la region maxilar afectada para la integracion del material de injerto y la cicatrizacion de la herida tras la elevacion del suelo del seno. Aunque esta bien establecido que el maxilar edentulo demuestra una vascularidad decreciente a medida que la reabsorcion progresa. las condiciones vasculares tras la elevacion del sueto del seno aiin no han sido investigadas. Este estudio esta relacionado con las arterias maxilares pertenecientes conccrnientes a la cirugia dc elevacion del suelo del seno y exaniina la vascularizacion del maxilar lateral tras la perdida del diente. Los vasos de maxilar lateral de 18 especimenes maxilares (10 machos. 8 hembras, edad media 67 aftos) se prepararon anatomicameiUe y se registraron las arterias locales principales, el ntimero de ramas y anastomosis discernibles macroscopicamente. su calibre y la distancia entre las ramas caudalcs principales y le borde alveolar. El maxilar lateral se abastecc por ramas de la arteria alveolar posterior superior (PSAA) y la arteria infraorbital (IOA) que forman una anastomosis en la pared osea antral lateral que tambien abastece a la membrana de Schneider. Esta anastomosis inlraosea se encontro en todos los especimenes. Ocho de dieciocho tambien mostraron una anastomosis extraosea entre PSAA c IOA, por vestibular de la pared'antral. dando una media de tres ramas craneales y cinco ramas caudales. Las dos anastomosis forman una dobic arcada arterial para abasiecer la pared antral laleral y, parcialmente, el proceso alveolar. El PSAA tubo un calibre medio de 1.6 mm y mostro una media dc 2 ramas endoosea una extraosea. El IOA lubo un diameiro medio de 1,6 mm y mostro una media dc una rama endoosea y tres extraosea. La distancia media entre la anastomosis intraosea y la cresta alveolar fue de 19 mm en dos lugares definidos dc mediacion. Su longitud media fue de 44.6 mm. La anastomosis epiperiostea veslibular se situo mas cranealmente y a una distancia media de 23 a 26 mm de la cresta alveolar y tubo una longitud media de 46 mm. El relativamente gran calibre de tos vasos que abastecen la pared antral lateral parece ser crucial al hecho de que el suministro de sangre periosteo se mantiene incluso en la atrofia maxilar severa y tras la completa desaparicion de los vasos centro-medulares.

1
6mm-C,

IO LX

9mmX'h'O 4 . 6 2 6

References
Beil. W.H. & Levy. B.M, (1975) Revascularization and bone healing after posterior maxillary osteotomy. Journal of Oral Surgery 29: 313-320. Bell. W.H.. You, Z.H., Finn. R.A. & Eields. R.Th. (1995) Wound healing after multisegmental Le Fort 1 osteotomy and transection of Ihe descending palatine vessels. Journal of Oral and Maxillofacial Surgeiy 53: 1425-1433. Berding. G.. Burchert, W. Van den HofT. J., Pytlik. C . Neukam. F.W.. Meyer, G.J. & Gratz. K.F (1995) Evaluation of the incorporation of bone grafts used in maxillofacial surgery with (l8F)fluoride ion and dynamic positron emission tomography. European Journal of Nuclear Medicine 22: 1133-1140. Bert. M., Itic, J. & Serfaly. R. (1989) La stimulation endostee en implantologie: Etude et resultats apres 2 ans. Cahiers Frothese 65: 22-i\. Block. M.S. & Kent. J.N. (1997) Sinus augmentation for dental implants: the use of autogenous bone. Journal of Oral and Ma.xillofacicil Surgery 55: 1281-1286. Boyne. P.J. & James. R.A. (1980) Grafting of ihe maxillary sinus floor with autogenous marrow and bone. Journal of Oral Surgery 3S: 613-616. Brand. R.W. & Isselhard. D.E. (1990) Anatomy of Orofacial Structures, 4th edition, 171-177. St Louis: C V Mosby. Braun. 1., Levy. S. & Hoffmann, J.C. (1985) The use of transarterial microembolization in Ihe management of haemangiomas of the perioral region. Journal of Oral and Maxillofacial Surgery 43: 239-248. Burkhardt, R., Kettner. G., Bohm. W. Schmidmeier. M., Schlag, R., Frisch, B., Mallmann. B., Eisenmenger. W. &

V^T

42

Blood supply to the maxillary sinus

Gilg. T. (1987) Changes in trabecular bone, hematopoiesis and bone marrow vesseis in aplastic anemia, primary osteoporosis and old age: a comparative histomorphometric study. BoneS: 157-164, Catone. G.A.. Reimer. B.L., McNeir. D. & Ray. R. (1992) Tibial autogenous cancellous bone as an alternative donor site in maxillofacial surgery: a preliminary report. Journal of Oral ami Ma.xi/lofacial Surgery 50: 1258-1263. Cawood, J.L & Howcll, R*A. (1988) A classification of the edentulous jaws. Iniernarional Journal of Oral and Ma.xillofacial Surgery 17: 232-236. Chanavaz, M. (1995) Anatomy and histophysiology of the periosteum: Quantification of the periosteal blood supply to the adjacent bone with 85 Sr and gamma-spectrometry. Journal of Oral Implantology 21: 214-219. Cohen, S.E. (1994) Atlas of cosmetic and reconstructive periodontal surgery. 2nd edition. LISA: Lea and Febiger. Daelemans. P. Hermans, M., Godet. N. & Malevez. C. (1997) Aulologous bone graft to augment the maxillary sinus in conjunction with immediate endosseous implants: A retrospective study up 10 5 years. International Journal of Feriodontics and Re.storativc Dentistry 17: 26-39. Demmler, K., Otte. P, BartI, R., Burkhardt, R., Frisch. B. & Jahn, A. (1983) Osteopcnie, Markatrophie und Kapillarversorgung. Vergleichende Untersuchungeii am menschlichen Beckcnkamm und 1. Lendenwirbelkorper. Zeitschrift fur Orthopcic/ie 121: 223-237. Dodson, T.B.. Bays. R.A. & Neucnschwander, M.C. (1997) Maxillary perfusion during Le Fort I osteotomy after ligation of the descending palatine artery. Journal of Oral and Muxiltofacial Surgery 55: 51-55. Epker. B.N. (1984) Vascular considerations in orthognathic surgery. II. Maxillary osteotomies. Oral Surgery Oral Medicine Oral Pathology 57: 473^78. GaRey, D.J.. Whittaker, J.M.. James. R.A. & Lozada. J.L. (1991) The histologic evaluation of the implant interface with heterograft and allograft materials - an eight-month autopsy report. Part II. Journal of Oral Implantolotry 17: 404-408. Geylikman, Y.G., Artun. J., Leroux, B.G.. Bloomquist, D.. Baab. D. & Ramsay. D.S. (1995) Effects of Le Fort I osteotomy on human gingivai and pulpai circulation. International Journal of Oral and Maxillofacial Surgery 24: 255260. Gray's Anatomy (1989) In: Williams, PL., Warwick, R.. Dyson, M. & Bannister, L.H., eds. 37th edition, 740-741. Edinburgh, London. Melbourne and New York: Churchill Livingstone. Haas, R.. Donath, K.. F6dinger, M. & Watzek. G (1998a) Bovine hydroxyapatite for maxillary sinus grafting: comparative histomorphometric findings in sheep. Clinical Oral Implants Research 9: 107 116-

Haas. R.. Mailath, G.. Dortbudak. O. & Watzek. G. (1998b) Bovine hydroxyapatile for maxillary sinus augmentation: analysis of interfacial bond strength of dental implants using pull-out lests. Clinical Oral Implants Research 9: 117-122. Hurzeler, MB., Kirsch, A., Ackermann, K.L. & Quinones, CR. (1996) Reconstruction ofthe severely resorbed maxilla with dental implants in the augmented maxillary sinus: a 5year clinical investigation. International Journal of Oral and Maxillofacial Implanl.s 11: 466-475. Jensen, J. & Sindet Pedersen, S. (1991) Autogenous mandibular bone grafts and osseointegralcd implants for reconstruction of the severely atrophied maxilla: a preliminary report. Journal of Oral and Maxillofacial Surgery 49: 1277-1287. Jensen. J., Sindet Pedersen, S. & Oliver, A.J. (1994) Varying treatment strategies for reconstruction of maxillary atrophy with implants: Results in 98 patients. Journal of Oral and Maxillofacial Surgery 52: 210-216.

Kasey, K., Meara, J.G. & Alexander, A. (1996) Location of the descending palatine artery in relation to the Le Fort I osteotomy. Journal of Oral and Maxitlofadal Surgery 54: 822-825. Kobayashi, S. (1982) Bone atrophy in rheumatoid arthritis a morphological and histometrical study of proximal tibial condyles. Nippon Seikeigeka Gakkai Zas.sahi 56: 727-738. Kumlien, IK.. Schiratzki. H. & Drettiier, B. (1985) Blood flow in the rabbit maxillary sinus mucosa. Measurement with a diffusible and a non-diffusible tracer. Avta Otolaryngohgica Stockholm 99: 144-153. Lang. J. & Urban. A. (1977) Verlaufsvariationen der Pars pterygopalatina A. maxillaris. Verhandlungen der Anatomischen Ge.sellsehaft 1\: 731-734. Lang, J.. Jensen, H.-P & Schroder. F (1985) Kopf. In: Lang, J. & Wachsmuth, W, eds. Praktisehe Anatomie. 1. Band. 548-551. Berlin. Heidelberg: Springer. Lanigan, D T (1995) Discussion of: Bell. W.H. et al. Wound healing after multisegmental Le Fort I osteotomy and transection of the descending palatine vesseis. Journal of Oral and Maxitlofacial Surgery 53: 1433-1434. Lanigan. D T , Hey, J.H. & West, R.A. (1990) Aseplic necrosis following maxillary osteotomies: Report of 36 cases. Journal of Oral and Maxitlofacial Surgery 48:142-156. Leder, A.J., McElroy. J. & Dcasy, M.J. (1993) Reconstruction of the severely atrophic maxilla with autogenous iliac bone graft and hydroxylapatite/decaicified freeze-dried bone allografl in the same patient: a preliminary report. Periodontal Clinical Investigation 15: 5-9. Lorenzetti, M.. Mozzati, M., Campanino, PP & Valente, G. (1998) Bone augmentation ofthe inferior floor ofthe maxillary sinus with autogenous bone or composite bone grafts: A histologic-histomorphometric preliminary report. International Journal of Oral and Maxillofacial Implants 13: 6973. Marx, R.E. (1994) Clinical application of bone biology to mandibular and maxillary reconstruction. Clinical Plastic Surgery 21: 377 392. McGregor. A.D. & MacDonaid. D.G. (1989) Age changes in ihe human inferior alveolar artery - a histological siudy. British Journal of Oral and Maxillofacial Surgery 27: 371374. Morton, A.L. & Khan. A. (1991) Internai maxillary artery variability in the pterygopalatine fossa. Otolaryngology Head and Neck Surgery 104: 204-209. Moy, PK.. Lundgren, S. & Holmes, R.E. (1993) Maxillary sinus augmentation: histomorphomelric analysis of graft materials for maxillary sinus floor augmentation. Journal of Oral and Ma.xillofacial Surgery 51: 857-862. Navarro, J.. Filho. J. &. Zoretto, N. (1982) Anatomy of the maxillary artery into the pterygomaxillopalatine fossa. Anatomiseher Anzeiger 152: 413-433. Nelson. R.L., Palh. M.G., Ogle. R.G., Waite, D.E. & Meyer. M W (1977) Quantitalion of blood flow after a Le Fort I osteotomy. Journal of Oral Surgery 35: 10-16. Neyt, L.F. DeClercq. C.A.S., Abeloos, J.VS. & Mommaerts, M.Y. (1997) Reconstruction ofthe severely resorbed maxilla with a combination of sinus augmentation, onlay bone grafting, and implants. Journal of Oral and Ma.xillofacial Surgery 55: 1397-1401. Nishibori. M.. Betts, N.J., Salania. H. & Listgarten. M.A. (1994) Short-term healing of autogenous and allogenetic bone grafts after sinus augmentation. Journal of Periodontology 65: 958-966. Prelterklieber. M.L.. Skopakoff. C. & Mayr, R. (1991) The human maxillary artery rein vest igaled: topographical relations in the infratemporal fossa. Acta Anatomica 142: 281-287. Quinones. C.R.. Hurzeler, M.B.. Schupbach, P, Kirsch. A., Blum. P, Caffesse, R.G. & Strub, J.R. (1997) Maxillary si-

43

Solar et al.
nus augmentation using different grafting materials and dental implants in monkeys Parl II. Evaluation of porous hydroxyapatite as a grafting material. Clinical Oral Implants Research 8: 487-496, Raghoebar. G.M.. Brouwer, T.J., Reintsema. H. & Van-Oort. R.P (1993) Augmentation of the tuaxillary sinus floor with autogenous botie for the placement of endosseous implants: a preliminary report. Journal oj Oral and Maxillofaeial Surgery S\: 1198-1203. Ranga, V. & Andronescu. P. (1968) Uber die feine GefSBversorguDg der Schleimhaut der Sinus paranasales. Anatomischer Anzeiger 122: 110-119. Schumacher, G.H.. Fanghansel. J.. KSster. D. & Mierzwa, .). (1988) Craniofacial growth under ihe influence of blood supply. Anatomischer Anzeiger 165: 303-309. Selden, H.S. (1974) The interrelationship between the maxillary sinus and endodontics. Oral Surgery Oral Medicine Oral Pathology 38: 623-629. Shibayama. Y., Nishimoto. M. & Nakata, K. (1993) Microvascular events in bone marrow related to development of and recovery from bone atrophy in thiopeta-treated rats. Fxperimental Toxicology and Pathology 45: 129-133. Sicher. H. & Du Brul. E.L. (1970) The blood vessels of head and neck: Maxillary artery. In: Sicher. H. & Du Brul. E.L., eds. Oral Anatomy, 5th edition. 315-320, Saint Louis: CV. Mosby Company. Skopakoff. Ch. (1968) Uber die Variabilitat im Verlauf der A. maxillaris. Anatomiseher Anzeiger 123: 534-546. Sobotta. J. (1989) Head: Facial muscles and blood vessels. In: S t a u b e s a n d . J.. e d . Atlas of human anatomy. Vol. I. l l t b Engt. edition. 48-59. Munich - Vienna - Baltimore: Urban & Schwarzenberg. Soikkonen. K.. Wolf. J.. Hietanen. J. & Mattila K. (1991) Three main arteries of the face and their tortuosity. British Journal of Oral and Maxillofaeial Surgery 29: 395-398. Staudt. J.. Breustedt, A.. Kunz. G. & Wilcke G. (1977) Untersuchungen iiber die Besonderheiien der arteriellen Versorgung im Kopfbereicb beim alten Menscben. Verhandlungen der Anatomischen Gesellschaft 71: 725-729. Ulm, C. Solar, P, Gsellmann, B.. Matejka. M. & Watzek, G. (1995) The edentulous maxillary alveolar process in the region of the maxillary sinus - a study of physical dimension. International Journal of Oral and Maxillofacial Surgery 24: 279-282. Valentini, P., Abensur, D., Densari. D., Oraziani. J.N, & Hammerle. C. (1998) Histological evaluation of Bio-Oss(R) in a 2-stage sinus floor elevation and implantation procedure A human case report. Clinical Oral Implants Research 9: 5964. Watzek, G.. Ulm, C , Solar. P & Matejka. M. (1993) Surgical criteria for endosseous implant placement. Practical Periodontology (fi Aesthetic Dentistry 5: 87-94. Watzek. G, (1996) Surgicai procedures for implant installation depending on the degree of maxiliomandibuiar atrophy. In: Watzek. G. ed. Endosseous implants: Scientific and clinical aspects. 211-274. Chicago: Quintessence publishing. Wheeler. S,L.. Holmes. R.E. & Calhoun. CJ. (1996) Six-year clinical and histologic study of sinus-lift grafts. Internationai Journal of Oral and Maxillofacial Implants 11: 26-34. Wheeler. S.L. (1997) Sinus augmentation for dental implants: The use of alloplastic materials. Journal of Oral and Maxillofacial Surgery 55: 1287-1293. Williamson, R.A. (1996) Rehabiiitation ofthe resorbed maxilla and mandible using autogenous bone grafts and osseointegrated implants. International Journal of Oral and Maxillofacial Implants U: 476-488. Yang. J.. Ma. X.. Zou. Z,J.. Wu. Q.G. & Wei, S.L. (1995) Percutaneous internal maxillary arterial embolization with ethylcellulose microspheres. Results in an animal model. Inves^ tigative Radiology 30: 354-358, Yeo, J.F., Loh, F C . Egyedi. P. & Djeng. S.K. (1989) Serious circulatory disturbances after Le Eort I osteotomy. A case report. Journal of Cranio and Maxillofacial Surgery 17: 222225. You. Z.H.. Zhang. Z.K.. & Xia. J.L, (1990) The study of vascular communication between jaw bones and their surrounding tissues by SEM of resin casts. West China Journal of Stomatology 26: 235-240. You. Z.H.. Zhang. Z.K. & Xia, J.L. (1991a) Blood supply of jaw bone mucoperiosteum and its role in orthognaihic surgery. China Journal of Stomatology 26: 31-37. You. Z.H.. Zhang. Z.K. & Xia, J.L. (1991b) A study of maxillary and mandibular vasculature in relation to orthognaihic surgery. China Journal of Stomatology 26: 263-267. Zinner^ LD, & Small. S.A. (1996) Sinus-lift graft: using the maxillary sinuses to support implants. Journal ofthe American Dental Association 127: 51-57.

44