The clinical anatomy of the maxillary artery in the pterygopalatine fossa

SCIENTIFIC ARTICLES J Oral Maxillofac Surg 61:72-78, 2003

The Clinical Anatomy of the Maxillary Artery in the Pterygopalatine Fossa Jinho Choi, DDS, MSD, PhD,* and Hyung-Sik Park, DDS, MSD, PhD† Purpose:

The purposes of this study were to delineate the maxillary artery and its branching arteries and to develop a classification of the various branching patterns by means of serial cadaver dissections of the pterygopalatine fossa region. Materials and Methods: Fifteen Korean adult cadavers were used; 2 sides of each cadaver were examined, for a total of 30 sides. Before dissection of the pterygopalatine region, computed tomography scan was taken of 20 cadaver heads. Sectioned specimens of 9 sides of the cadaver heads in 3.0-mm thickness were made for this study. Then we dissected 21 sides of fresh cadavers under the microscope. In this investigation, we observed branching patterns of the third portion of the maxillary artery, a relationship of the terminal branches of the maxillary artery to the pterygomaxillary junction, and the course of descending palatine artery. Then we classified the branching patterns of the maxillary artery in the pterygopalatine fossa. Results: From the pterygomaxillary junction to the pterygopalatine fossa region, the maxillary artery was usually branched into 5 arteries in the following order: posterior superior alveolar artery, infraorbital artery, artery of the pterygoid canal, descending palatine artery, and sphenopalatine artery. Of 21 cadavers, 18 showed this order (85.7%). There were 2 types of branching patterns of the posterior superior alveolar artery and the infraorbital artery. The average distance from the most inferior point of the pterygomaxillary junction to the posterosuperior alveolar artery, infraorbital artery, and descending palatine artery was 15.2, 32.2, and 24.8 mm, respectively. In most cases (95.2%), the greater and lesser palatine arteries were divided from the short descending palatine artery. According to the contours of the third portion of the maxillary artery, we classified them into 5 types: the “Y” type (19%), “intermediate” type (33.3%), “T” type (23.8%), and “M” type (14.3%). Conclusion: The results of this investigation show the common patterns of the maxillary artery. © 2003 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 61:72-78, 2003 Maxillary osteotomy (Le Fort I, II, and III) is a commonly performed surgical procedure on the maxilla for the correction of dentofacial deformities. After the presentation of a large series of Le Fort I osteotomies by Obwegeser in 1969,1 various modifications have been made to improve the safety and versatility of this

procedure. Maxillary osteotomy necessitates separation of the maxilla from its posterior attachments to the cranium. At that time, it is important to preserve various structures in the pterygopalatine fossa (PPF) just above the pterygomaxillary junction (PMJ). The PPF is bounded anteriorly by the maxilla, posteriorly by the medial plate of the pterygoid process and greater wing of the sphenoid process, medially by the palatine bone, and superiorly by the body of the sphenoid process. Its lateral boundary is the pterygomaxillary fissure (PMF), which opens into the infratemporal fossa. The fossa has an inverted conical shape, with its apex forming the greater palatine canal. The maxillary artery (MA) enters through the PMF in the anterior, medial, and superior direction. The MA gives off several branches before entering the sphenopalatine foramen.2-4 The MA arises behind the neck of the mandible and is divided into 3 parts: the

*Assistant Professor, Department of Dentistry, College of Medicine, Inha University, Inchon, Korea. †Professor and Chairman, Department of Oral and Maxillofacial Surgery, College of Dentistry, Yonsei University, Seoul, Korea. Address correspondence and reprint requests to Dr Choi: Department of Dentistry, College of Medicine, Inha University Hospital, 7-206, 3rd Street, Shinheung-dong, Choong-gu, Inchon, Korea 400-103; e-mail: [email protected] © 2003 American Association of Oral and Maxillofacial Surgeons

0278-2391/03/6101-0013$35.00/0 doi:10.1053/joms.2003.50012

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mandibular, pterygoid, and pterygopalatine (third portion). Because the distribution center for the third portion of the MA is the PPF, it was also called the pterygopalatine portion.2,3,5 Maxillary or midfacial osteotomies are performed in an extremely vascular region where control of bleeding is frequently not possible until after the completion of the osteotomy and the repositioning of segments. Bleeding is often profuse. Lanigan et al,6-8 reported a series of cases of postoperative hemorrhage, false aneurysm, and arteriovenous fistula. They also state that the vessel most commonly involved after maxillary osteotomy is the MA and its branches. Despite its importance, the reports delineating the third portion of the MA are rare because of the difficulty in anatomic investigation of this region. Up to now, the anatomy of the PPF was dealt with by Montgomery et al,9 Potter,10 Pearson et al,11 and Wentges.12 In the field of oral and maxillofacial surgery in particular, Turvey and Fonseca13 reported the relationship of the MA in the PPF to the pterygomaxillary suture. Also, Li et al14 reported the positional relationship of the DPA to the Le Fort I osteotomy. To safely separate the PMJ, knowledge of the anatomic structures of the PPF region is very important to surgeons. To prevent complications of maxillary osteotomy, an increased understanding of the anatomic course and variations of the MA and its terminal branches in the PPF may minimize injury to this artery; therefore it is useful information for the surgeon performing midfacial osteotomies. The purposes of this study were to identify the MA and its branching and to develop a classification of the various branching patterns by means of serial cadaver dissections of the PPF region. Also, the intent of this investigation was to study the position of the descending palatine artery (DPA) as it relates to the maxillary osteotomy. Specifically, the investigation was conducted to establish anatomic data of the PPF regarding the branch patterns of MA and potential relationships of terminal branches, to establish useful information for various midfacial procedures.

Materials and Methods MATERIALS

Thirty sides of 15 fresh frozen Korean adult cadavers were used in this study. METHODS

Computed Tomography Before the dissection to the pterygopalatine region in the cadaver, computed tomography (CT) scans were taken of 20 cadaver heads for this study. The cadaver heads were positioned in a specially designed

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FIGURE 1. CT view of the pterygopalatine fossa area (A) and the sectioned specimen of the human cadaver (B) Mn, mandible; PP, pterygoid plate; T, tongue; SP, sphenoid bone; NS, nasal septum; SS, sphenoidal sinus; PPP, pterygopalatine fossa.

acrylic box filled with water and scanned with use of a spiral CT scanner (GE Medical System, Milwaukee, WI) under the following conditions: high-resolution bone algorithm, 15-cm field of view (FOV), 200 mA, 120 kV, scan time of 1 second, and thickness of 3.0 mm. After the CT scanning was completed, film was developed with a Fuji medical laser imager FL-IM D (Fuji Photo Film Co, Ltd, Tokyo, Japan) (Fig 1). Sectioned Specimen of Human Cadaver We made a sectioned specimen of cadaver heads from 9 sides in 3.0-mm-thick sections using a cutting machine (WS-1650; Woosung Co, Seoul, Korea). Before the sectioning, we enclosed the cadaver heads with dental plaster and kept them at ⫺78°C in a deep freezer for 3 days. The sectioned specimens were compared with the use of CT views (Fig 1). Dissection of the PPF With the lateral infratemporal approach, the mandibular ramus and condyle were removed from each specimen to expose the PMF region. After the removal of the external pterygoid muscle, the present arterial structure was photographed and then removed. On dissection in the PMF region, branches of the third portion of MA, lateral plate of pterygoid process, and PMF were identified and photographed. A digital sliding caliper (with 0.0-mm error) was used to measure the distance from the most inferior point of the maxilla and lateral pterygoid plate to the postero superior alveolar artery (PSAA) and infraorbital artery (IOA) as it entered the maxilla. After gross observation of the PMF using a drill with a round bur (No. 8 and No. 16), the lateral pterygoid plate, maxilla, and part of the sphenoid bone were removed and the PPF was exposed. After removal of the bones, the branches of the nerve and artery were exposed so we could observe an aspect of the distri-

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FIGURE 2. The branching pattern of the third portion of the maxillary artery. A, PSAA, IOA, VA, DPA, and SPA were divided in order of arterial branching on the way of the MA from the PMJ to the PPF. One of the other cases is shown in which the BA was divided from MA after the branching of PSAA (B).

bution and identify morphologic variations (Figs 2 through 4). After exposure of the third portion of MA, we measured the vertical distance from the most inferior point of the PMJ to the PSAA and IOA at the posterosuperior alveolar foramen and infraorbital fissure, respectively (Fig 5).

FIGURE 3. Two branching types of the PSAA and the IOA. The short branch from the MA that divided into PSAA and IOA was observed (A, B); in the others, the PSAA and IOA branched separately from the MA (C, D).

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FIGURE 4. The morphology of the DPA. The greater and lesser palatine arteries (GPA, LPA) were divided from the short DPA (4 to 5 mm in length) (A). The GPA and LPA were divided directly from the MA (B) IOA, infraorbital artery; BA, buccal artery.

The branching patterns of the third portion of MA were observed in the PPF and the palate region. We identified the branching patterns of the MA according to the branching orders and made a classification from the viewpoint of the posterior wall of maxilla. Among the branches of the third portion of the MA, the branch patterns of IOA and PSAA and the patterns of the DPA were identified and classified morphologically. The patterns of the MA in the posterior maxilla

FIGURE 5. Measurements of the vertical distance of a entrance point of the maxilla of the posterior alveolar artery into the posterior alveolar foramen (A), an entrance point of IOA into the inferior orbital fissure (B) and a furcation area of MA into the DPA and SPA (C) from the inferior border of the PMJ.

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FIGURE 6. The morphologic classifications of the MA according to the contours of the third portion of the MA. The prevalence of the morphologic variations of the MA in this study was compared with the study of Morton and Kahn.15

FIGURE 8. Photograph showing the case of atypical morphology of the third portion of the MA. The variable branching order and location of the arterial branches are observed. VA, artery of the pterygoid canal.

were classified into 5 types according to the branch patterns of the sphenopalatine artery (SPA) and the DPAs like the classification of Morton and Khan15 (Figs 6 to 8). Using the lateral approach, we exposed the PPF from the nasal cavity or middle cranial fossa via the same method. After exposing the anatomic structures of the PPF internally and externally, we measured the vertical distance from the most inferior point of PMJ and palatal plane to the point where the DPA branched from the MA and the point where the DPA divided into the great and lesser palatine arteries (Fig 5). Before the third portion of the MA divided into its terminal branches, the external diameter of the MA was measured with a sliding caliper. On completion of the dissections, the superior, lateral, and medial aspects of the PPF, nerves, arteries, and surrounding anatomic structures were identified and photographed. Otologic instruments were used with the aid of a surgical microscope (⫻6.3 to ⫻12; Karl Kaps, Asslar/ Wetzlar, Germany) to perform the dissections. FIGURE 7. The morphologic classifications of the MA. The morphology of the MA according to its contour of the third portion was classified into 4 types: type Y (A), type intermediate (B), type T (C), and type M (D).

Results After the mandibular ramus and condyle were removed, the structures of the infratemporal fossa were

76 removed via the lateral infratemporal approach. With reference to the CT scans (Fig 1A) and the 3.0-mm thickness sectioned specimen (Fig 1B), we dissected the PMF region, cleanly exposed the third portion of MA, and identified their morphology. THE BRANCH PATTERNS OF THE THIRD PORTION OF MAXILLARY ARTERY

The MA passed horizontally deep to the mandibular ramus and branched into the buccal artery (BA) supplied buccinator muscle; then it turned medially through the PMF to arrive in the PPF. At that place, it became the third portion of the MA. These branches of the third portion of MA could be observed at one third of the height of the posterolateral wall of the maxillary sinus (Fig 3). The MA entered through the PMF coursing anterior in the medial and superior direction. In its course, it gave off several branches. According to the order of branching in its course from the PMJ area, the PSAA and IOA were located at the posterior wall of the maxilla and entered into the posterosuperior alveolar foramen and the infraorbital fissure, respectively. Then, the MA continued to the PPF. It divided into the DPA, which supplied the palate, the artery of the pterygoid canal (VA), which is located in the pterygoid canal, and the SPA. In most of the cases, this branching pattern was observed; in the 21 dissections, this pattern was found in 18 cadavers (85.7%) (Fig 2A). The remaining cases (3 cadavers [14.3%]) showed different arterial branching patterns as follows: in one case after the PSAA and VA branched out, the MA branched out into the IOA, DPA, and SPA, in sequence (1 of 21 dissections). In another case after the PSAA branched out, the BA branched out, and finally the MA branched out into the IOA, DPA, and SPA, in sequence. The other case was that after the SPA branched out, the PSAA, IOA, and DPA were divided at the same point (Fig 2B). Before its terminal branches divided, the external diameter of the MA was 3.2 ⫾ 0.6 mm (minimum, 2.2; maximum, 4.1). THE BRANCHING TYPES OF THE PSAA AND THE IOA

The pattern with which the PSAA and the IOA branched from the MA was of 2 types. The first type showed these 2 arteries coming together from the short branch of the MA; 57.1% of our subjects showed this pattern. The second branching type revealed that the PSAA and the IOA branched separately from the MA. The remaining 42.9% had this pattern (Fig 3). The vertical distances from the most inferior point of the PMJ to the PSAA as it entered the posterior superior alveolar foramen and IOA as it entered in-

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fraorbital foramen were 15.2 ⫾ 2.4 mm (minimum, 15.7; maximum, 30.0) and 32.2 ⫾ 3.7 mm (minimum, 24.3; maximum, 37.9), respectively (Fig 5). THE MORPHOLOGY OF THE DPA

The morphology of the DPA that courses from the PPF through the greater and lesser palatine canal and supplies the hard palate and soft palate was identified and classified morphologically (Fig 4). The DPA was divided from the MA at a distance of 24.8 ⫾ 2.8 mm (minimum, 20.1; maximum, 30.3) from the most inferior point of the PMJ vertically. In most cases (95.2%), the greater and lesser palatine arteries were divided from the short DPA. The length of the DPA was 4 to 5 mm (Fig 4A). In this case, the vertical distance from the most inferior point of the PMJ to the point that the greater and lesser palatine arteries were divided: 19.5 ⫾ 3.7 mm (minimum, 15.4; maximum, 26.8) (Fig 5). In one case (4.8%), however, the greater and the lesser palatine arteries were divided directly from the MA, not from the DPA (Fig 4B). On the other hand, after the middle and inferior nasal concha and palatal bone were removed, the vertical distance from the palatal plane to the point at which the greater and lesser palatine arteries divided was measured: 20.1 ⫾ 3.7 mm (minimum, 15.4; maximum, 26.8). THE MORPHOLOGIC CLASSIFICATIONS OF THE MA

The patterns of the MA with a view of the posterior maxilla were classified into 5 types according to the branch patterns of the SPA and DPA similar to the classification of Morton and Khan.15 It included the Y type (180° pattern), intermediate type (90° pattern), T type (⬎90° pattern), M type (0° pattern), and other type (it could not belong in any types) (Figs 6, 7). In the 21 serial dissections, the Y type was found in 4 (19.0%) cases, the intermediate in 7 (33.3%), the T type in 5 (23.8%), and the M type in 3 (14.3%) cadavers (Figs 7, 8). Also, 2 cadavers were classified as other type (9.6%). The other-type cases had the variable branching orders and the locations of the arterial branches. One case showed that after branching from the MA, the DPA then courses inferiorly, and the SPA ran straight to the sphenopalatine foramen. In another case, the branching order and location of the arterial branches were completely changed, so it showed a complex and diverse appearance (Fig 8). With reference to the CT scans, we dissected the cadavers. We compared 3.0-mm sectioned specimens with the CT scans (Fig 1). The second portion of the MA in the infratemporal fossa lay near to the mandible on the CT scans and sectioned specimens. Coming close to the third portion of the MA, it passes medially and enters the PPF. The third portion of the MA in the

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PPF is located approximately 13 or 16 mm above the nasal floor.

Discussion In this study, the branching pattern of the third portion of the MA was generally similar to that in various articles in the literature.3,5,9-12 According to the course from the PMJ region, in the PPF region, the MA branches into 5 arteries in order. The PSAA and IOA branches off first and then the DPA, VA, and SPA arise in the PPF region. In 18 of 21 cases (85.7%), this order was shown. In terms of morphologic variations, the remaining 3 case (14.3%) showed different orders of arterial branching patterns and locations. In particular, there was a branching pattern in which the BA (described as the branch of the second portion of the MA in anatomy textbooks2,3,5) branched next to the PSAA, the branch of the third portion (Fig 2). There are 2 types of patterns from which the PSAA and the IOA arise (Fig 3). The first shows these 2 arteries come together from the short branch of the MA. In 12 of 21 dissections (57.1%), this pattern was shown. The second branching pattern indicated the PSAA and IOA branched separately from the MA. The remaining 42.9% (9 of 21) had this pattern (Fig 3). This study measured the distance to the branching locations of the branch of the MA from the most inferior point of the PMJ (Fig 5). Because the MA and branches were easily injured during pterygomaxillary dysjunction,14 we thought to establish the data for the branches of the MA in the PPF to the PMJ, so that they could be meaningful guidelines for safely conducting a maxillary osteotomy. The vertical distance from the most inferior point of the PMJ to the PSAA as it entered the postero superior alveolar foramen and IOA as it entered the infraorbital foramen were 15.2 ⫾ 2.4 mm and 32.2 ⫾ 3.7 mm, respectively. The DPA was divided from the MA at a distance 24.8 ⫾ 2.8 mm from the most inferior point of the PMJ, vertically. Thus, we propose that the edge of the osteotomy should be less than 20 mm above the most inferior edge of the PMJ. This will make conduction of the pterygomaxillary dysjunction safe and avoid damage to the MA. Turvey and Fonseca13 reported that in the Le Fort I osteotomy, the osteotomy should be angled inferiorly from the zygomaticomaxillary crest as it continues posteriorly toward the pterygoid plates. Because the average height of the maxillary second molars is 20 mm in Koreans,16 the posterior maxillary osteotomy should be made 25 mm above the cusp tip of the second molar to avoid damage to the vitality of the tooth. If the posterior lateral maxillary osteotomy continues along the same horizontal line as the ante-

77 rior osteotomy, the risk of damaging the MA would increase. Because the DPA is divided and descended at approximately 24.8 mm apart from the most inferior edge of PMJ, the osteotomy should be angled inferiorly from the zygomaticomaxillary crest as it continues posteriorly to avoid damage to the MA and branches. In another approach, Li et al14 exposed 8 cadavers via a Caldwell-Luc approach and reported that the average distance from the MA down to the nasal floor was 16.6 mm. Because of the difference in the approach method to the MA, it was difficult to directly compare that with our results. Before its terminal branches were divided, the external diameter of the MA was 3.2 ⫾ 0.6 mm. It was larger than the results (2.63 mm) of Turvey and Fonseca.13 We supposed that this vessel was able to produce a greater amount of hemorrhage than in Turvey and Fonseca’s sample. The morphology of the DPA was identified and classified (Fig 4). It is generally known that the DPA arises from the MA, descends in the greater palatine canal, and divides into the greater and lesser palatine arteries in the greater palatine canal.2-5 In this study, most cases (95.2%) pointed to the short DPA of a length of 4 to 5 mm, which arose from the MA and descended in the greater palatine canal, divided into the greater and lesser palatine arteries in the greater palatine canal, and reached the oral surface of the hard palate. But, in one case, without the short DPA, the greater and lesser palatine arteries divided directly from the MA (4.8%) (Fig 4). According to contours of the third portion of the MA, Morton and Khan15 classified the morphology of the third portion of the MA into 3 types: type Y, intermediate, and M. In this study, we classified them into 5 types: Y, intermediate, T, M, and other (Figs 6, 7). In the 21 sides of Korean cadavers, the Y type was found in 4 (19.0%), intermediate in 7 (33.3%), T in 5 (23.8%), and M in 3 (14.3%) cadavers (Figs 7, 8). Also, the other type was found in 2 (9.6%). In one case, after branching from the MA, the DPA coursed inferiorly, and the SPA ran straight to the sphenopalatine foramen. In another case, the branching order and location of the arterial branches were completely novel with a complex and diverse appearance. Morton and Kahn15 reported that the Y form was found in 33%, the intermediate in 50%, and the M form in 16.5%. In this study, the intermediate and T types, which are similar to the intermediate type in Morton and Kahn’s classification, composed 57.1%. It showed that the intermediate type had larger proportions in this Korean sample than in Morton and Khan’s study. The Y type appeared in relatively small proportions.

78 Based on the results of this study, these data indicate that the pterygomaxillary dysjunction can be conducted safely and without severing the MA. Because the contents of the PPF are the pterygopalatine ganglion and the maxillary division of the trigerminal nerve as well as the MA, avoiding damage to this region, the osteotome should be placed inferiorly in the PMJ and directed medially and anteriorly. Directing the osteotome superiorly should especially be avoided. Also, because the location of the DPA was an average of 24.8 mm apart from the PMJ, in the Le Fort I osteotomy, it should be angled inferiorly from the zygomaticomaxillary crest as it continues posteriorly. This will minimize the risk of damaging the MA and the branches.

References 1. Obwegeser H: Surgical correction of small or retrodisplaced maxillae. J Plast Reconstr Surg 43:351, 1969 2. Choung IH: Human Anatomy (ed 2). Seoul, Korea, Academy Co, 1996, pp 218-219 3. Rosse C, Gaddum-Rosse P: Hollinshed’s Textbook of Anatomy (ed 5). Philadelphia, PA, Lippincott-Raven Publishers, 1997, pp 766-767 4. Williams PL, Warwick R: Gray’s Anatomy (ed 36). Philadelphia, PA, Saunders, 1980, pp 315-319

THE ANATOMY OF THE MAXILLARY ARTERY 5. Woodburne RT, Burkel WE: Essentials of Human Anatomy (ed 8). New York, NY, Oxford University Press, 1988, p 260 6. Lanigan DT, Hey JH, West RA: Aseptic necrosis following maxillary osteotomies: Report of 36 cases. J Oral Maxillofac Surg 48:142, 1990 7. Lanigan DT, Hey JH, West RA: Major vascular complications of orthognathic surgery: False aneurysms and arteriovenous fistulas following orthognathic surgery. J Oral Maxillofac Surg 49: 571, 1991 8. Lanigan DT, Hey JH, West RA: Major vascular complications of orthognathic surgery: Hemorrhage associated with LeFort I osteotomies. J Oral Maxillofac Surg 48:561, 1990 9. Montgomery WW, Katz R, Gamble JF: Anatomy and surgery of the pterygomaxillary fossa. Ann Otol Rhinol Laryngol 79:606, 1967 10. Potter GD: The pterygopalatine fossa and canal. AJR Am J Roentgenol 107:520, 1969 11. Pearson BW, Mackenzie RG, Goodman WS: The anatomic basis of transantral ligation of the maxillary artery in severe epistaxis. Laryngoscope 79:969, 1969 12. Wentges RT: Surgical anatomy of the pterygopalatine fossa. J Laryngol Otol 89:35, 1974 13. Turvey TA, Fonseca RJ: The anatomy of the internal maxillary artery in the pterygopalatine fossa: Its relationship to maxillary surgery. J Oral Surg 38:92, 1980 14. Li KK, Meara JG, Alexander A: Location of the descending palatine artery in relation to the LeFort I osteotomy. J Oral Maxillofac Surg 54:822, 1996 15. Morton AL, Khan A: Internal maxillary artery variability in the pterygopalatine fossa. Otolaryngol Head Neck Surg 104:204, 1991 16. Oh HJ, Kim HJ, Baek DJ, et al: Measurements of teeth in Koreans. Presented at the 41th Congress of the Korean Academy of Physical Anthropology, Seoul, Korea, 1998