The Superior Alveolar Nerves: Their Topographical Relationship and Distribution to the Maxillary Sinus in Human Adults

Okajimas Folia Anat. Jpn., 70(6): 319-328, March, 1994

Gen MURAKAMI, Kenji OHTSUKA, Iwao SATO, Hiroshi MORIYAMA, Kazuyuki SHIMADA and Hiroshi TOMITA

Department of Anatomy, Nihon University School of Medicine, Tokyo, Japan (G.M.), Department of Otorhinolaryngology, Nihon University School of Medicine, Tokyo, Japan (K.O., H.T.), Department of Anatomy, Nippon Dental University, School of Dentistry at Tokyo, Tokyo, Japan (I.S), Department of Anatomy, Showa University School of Medicine, Tokyo, Japan (H.M., K.S.).

- Received for Publication, January 31, 1994-—

Key Words: Human anatomy, Maxillary sinus, Superior alveolar nerves, Superior dental plexus, Whole-mount silver impregnation

Summary: The superior alveolar nerves in human adults were investigated macroscopically using whole-mount silver impregnation, paying special attention to their topographical relationship and distribution to the mucous membrane of the maxillary sinus. In addition, the fiber composition of the alveolar nerves was analysed in order to estimate their contribution to teeth innervation. The posterior superior alveolar nerve (PSAN) ran through canaliculi in the lateral wall of the sinus (23 of 37 cases, 62.2%) or under the mucous membrane of the sinus (14 of 37 cases, 37.8%). Moreover, the PSAN gave off many fine twigs to make complex plexus under the mucous membrane of the sinus before joining the superior dental plexus. The plexus of the maxillary sinus was separated from the superior dental plexus by the bony wall of the sinus. After the above gross observations, the perimeter compositions of myelinated fibers of the plexus, PSAN and the anterior alveolar nerve were analysed in the same specimen. The plexus was composed of myelinated fibers of less than 27μm in circumference perimeter

(mean; 14.3μm) and numerous unmyelinated fibers. The fiber composition suggested that few fibers in the plexus of the maxillary sinus contribute to the formation of the superior dental plexus. The superior dental plexus, innervating the upper teeth, was located in the thick alveolar process of the maxilla, and not on the maxillary sinus wall. The clinical importance of these results was discussed in relation to nerve injury during antrostomy of the maxillary sinus.

The maxillary sinus is innervated by several textbooks (Plate I). According to some (Piersol, 1913; branches of the maxillary nerve, and especially Cryer, 1916; Toldt, 1919; Schaeffer, 1953; Anson, by the superior alveolar nerves (Warwick, 1976; 1966; Romanes, 1981; Liebgott, 1982, Leonhardt Paparella and Shumrick, 1980; Cummings, 1986; et al., 1988), the posterior superior alveolar nerve Kerr and Groves, 1987; McMinn, 1990). However, (PSAN) runs along (superficial to) the zygomatic previous descriptions of the superior alveolar nerve surface of the maxilla and joins the superior dental have concentrated on its contribution to the superior plexus outside the maxillary bone (Plate IA). dental plexus which innervates the upper teeth Takayama (1959) also described the outside course (Kopsch, 1955; Williams and Warwick, 1980; of PSAN in his study. In contrast, others (Spalteholz, Clemente, 1985). In fact, some textbooks (Hyrtl, 1922; Shapiro, 1954; Nishi, 1974; Hollinshead, 1982; 1866; Schaffer et al. , 1909; Spitzka, 1913; Rouviere, Lang, 1985; DuBrul, 1988; McMinn, 1990) claim 1974) refer to this nerve as the superior "dental" that the PSAN runs under the mucous membrane of nerve. In contrast to the innervation of the upper the maxillary sinus and that the superior dental teeth, the nerve supply to the mucous membrane of plexus is also located under the mucous membrane the maxillary sinus has not yet been investigated in (Plate IB). detail. The aim of this study was to clarify the course of Moreover, descriptions of the course of the the superior alveolar nerve and the location of the superior alveolar nerve and the location of the superior dental plexus relative to the wall of the superior dental plexus have differed among anatomy maxillary sinus, and to clarify the main nerve supply-

Address correspondence to Dr. Gen Murakami M. D., Ph.D., Department of Anatomy , Nihon University School of Medicine, Ohyaguchi-kamimachi 30, Itabashi-ku, Tokyo 173, Japan

319 320 G. Murakami et al. ing the lateral and posterior walls of the sinus, in arose from the base of the infraorbital nerve in the order to obtain basic data useful for prevention of pterygopalatine fossa and ran downwards and for- nerve injury during antrostomy of the maxillary sinus wards to pierce the zygomatic surface of the maxilla. (Killey and Kay, 1975). The PSAN usually arose by a single trunk (31 of 37 cases, 83.8%), but sometimes arose from a thick nerve and 1-3 thin nerves (6 cases, 16.2%). One or Materials and Methods two branches, which arose from the origin of the PSAN, ran downwards outside the maxilla to the Thirty-seven specimens of the head region from posterior palate. After piercing the zygomatic surface cadavers of 37 adults, aged 51-75 years, of which of the maxilla, the PSAN frequently (23 cases, the nerves had been stained by whole-mount 62.2%) passed through a canaliculus in the postero- silver impregnation, were examined grossly and lateral wall of the sinus (Plate II). Sometimes, how- histologically. ever, the PSAN (14 cases, 37.8%) ran beneath the The specimens, which had been fixed by perfusion mucous membrane of the sinus (Plate III), and not with 10% formol solution from the femoral artery, through a bony canaliculus. In the latter 14 cases, were viewed from the medial side for gross obser- the PSAN was always closely accompanied by a vation. The medial wall of the maxillary sinus was branch of the posterior superior alveolar artery. In partly removed, and the major branches of the this study, we did not find a single case in which the maxillary nerve were identified. Each specimen was main trunk of the PSAN passed outside (superficial then decalcified for minute dissection in 3N hydro- to) the zygomatic surface of the maxilla. cloric acid for 2-5 days at room temperature, then Along its course close to the maxillary sinus, rinsed with tap-water for 3 days and with distiled PSAN did not give off branches to the palate and water for another 3 days (6 changes in all). Then, the teeth, except at its anterior and posterior ends. At whole specimen block was immersed in 0.7% silver the anterior end of its course, the PSAN divided into nitrate (Kanto kagaku) solution for 12-24 h at room a few branches leading to the posterior part of the temperature under dark conditions in a modification superior dental plexus (Plate II). At the posterior end of the whole-mount silver impregnation method of its course, the PSAN gave off 2-3 branches of Kimura and Takahashi (1985) for staining of leading to the posterior palate, which communicated cutaneous nerves. After rinsing in distiled water for with branches of the greater palatine nerve. 3 days (with 6 changes), the specimen was preserved Many twigs from the PSAN formed a nerve plexus in 50% ethanol solution under dark conditions. under (outside) the mucous membrane of the maxil- After macroscopic observations of the silver- lary sinus (Plates III, IV), irrespective of whether the impregnated specimens, the mucous membrane of nerve passed through a bony canaliculus or under the maxillary sinus, including its accessory nerves, the mucous membrane (see above). In the nerve was removed from the maxillary bone, re-fixed in plexus, relatively large twigs accompanied small PBS-buffered 10% formol solution (ph 7.4), dehy- vessels, while small twigs ran independently away drated and embedded in paraffin, and cut into semi- from vessels. The PSAN was located in the central serial sections 10 [tm thick. These sections were portion of the nerve plexus. The plexus was not stained with luxol fast blue solution (Kliiver and observed clearly on the upper and lower walls of the Barrera, 1953) and van Gieson's picro-fuchsin sol- sinus. The gross morphology of the plexus was similar ution (Lillie, 1965), after removal of impregnated in both dentate and edentulos specimens. silver particles by rinsing in 4N hydrocloric acid for 2h. Using histological sections, the circumference b. Histology perimeter of myelinated fibers was measured Myelinated fibers were observed in nerve twigs and analysed with an optical electron planimeter which formed the plexus (Plate IV). Most of the (Digiplan, Kontron Co). The reduction in size during myelinated fibers (82.8%) of the plexus were less the histological preparation procedure was estimated than 201[A,min circumference perimeter and all were to be about 15% . less than 27 [Am. On the other hand, in the anterior superior alveolar nerve and PSAN, larger fibers were more frequently observed. In particular, large Results myelinated fibers were observed in 4.2% of the anterior superior alveolar nerve (Table 1). Numerous 1. Posterior superior alveolar nerve and the unmyelinated fibers were also present both in the nerve plexus of the maxillary sinus plexus and superior alveolar nerves. a. Gross observation The posterior superior alveolar nerve (PSAN) Superior Alveolar Nerves and Maxillary Sinus 321

Table 1. Perimeter composition of myelinated fibers in the maxilla, but inside the maxilla. posterior and anterior superior alveolar nerves and the We also demonstrated that numerous twigs from nerve plexus of the maxillary sinus*. the PSAN form a nerve plexus under the mucous membrane of the maxillary sinus. This plexus, "the nerve plexus of the maxillary sinus", was located mainly at the lateral and posterior walls of the sinus, along the course of the PSAN. In contrast, the major part of the superior dental plexus was located in the thick bony part of the maxilla, the alveolar process, * In total, 1502fibers of the posteriorsuperior alveolar nerve although previously the superior dental plexus had (PSAN), 1308fibers of the anterior superioralveolar nerve often been described as lying just beneath the mucous (ASAN)and 64 fibersof the nerveplexus of the maxillarysinus membrane of the sinus (Spalteholz, 1972; Nishi, weremeasured and analysed. ** Accordingto the criteria of functionalsensory modalities 1974; Williams and Warwick, 1980). These two by Nobackand Demarest(1981), A-8 fiberscorresponded to plexuses are separated from each other by the bony myelinatedfibers less than 161AM in circumference perimeter, A-13 wall of the maxillary sinus. fiberscorresponded to those16-38 vm in circumferenceperimeter, Moreover, the fiber composition of the nerve andA-y fibers corresponded to thosemore than 38 p.m in circum- plexus of the maxillary sinus was different from that ferenceperimeter. of the superior alveolar nerves innervating the upper teeth (Table 1). The plexus appeared not to contain A-y fibers for proprioception according to Noback 2. Middle superior alveolar nerve and Demarest (1981) and to Heasman (1984). It is The middle superior alveolar nerve, which arose unlikely that the convergence of the plexus to a small from the infraorbital nerve along the infraorbital diameter was caused by aging or tooth loss, since the canal (or groove), was observed in 25 of 37 cases diameter range of myelinated fibers innervating teeth (67.6%). In 21 of the 25 cases, the nerve was seen has been reported not to change with either aging from the inner aspect of the maxillary sinus during (Johnsen et al., 1983) or tooth loss (Heasman, 1984). its course through a canaliculus (Plate II). The nerve In contrast, 4.2% of myelinated fibers of the anterior gave off 2-3 branches to the mucous membrane of superior alveolar nerve, which merged directly into the sinus. Under the mucous membrane, which lined the superior dental plexus, seemed to be A-y fibers the upper wall of the sinus, the branches formed a for proprioception (Table 1). The fiber composition small network of fine twigs. However, the branches of the anterior superior alveolar nerve was similar to did not communicate closely with the nerve plexus of that of the inferior alveolar nerve (Heasman, 1984) the maxillary sinus. and dental pulp (Reader and Foreman, 1981; Jonsen et al., 1983; Nair et al., 1992). These results suggest 3. Anterior superior alveolar nerve and the that fibers in the nerve plexus of the maxillary sinus superior dental plexus are different from those in the superior dental plexus. The anterior superior alveolar nerves, 2-3 in The middle superior alveolar nerve was observed number, arose from the infraorbital nerve after its 67.6% of cases in the present study. This incidence exit from the infraorbital foramen. These nerves did corresponds to those reported previously (70% in not supply the mucous membrane of the maxillary Berkovitz et al., 1977; 54% in Hollinshed, 1982). sinus. The anterior superior alveolar nerves divided This nerve also supplied the mucous membrane of into numerous twigs and formed the anterior part of the maxillary sinus, although only a small area of its the superior dental plexus (Plate V). In addition, the upper part. posterior and middle superior alveolar nerves also The mucous membrane of the maxillary sinus has formed the posterior part of the superior dental been removed in a classic operation, "Caldwell plexus after their courses along the maxillary sinus (1893) and Luc (1897) antrostorny" for sinusitis. (Plate II). Sensory disturbance of the teeth has been reported in nearly 20% of patients after this operation (Killey and Kay, 1975). Lang (1989) reviewed previous Discussion reports of this nerve disturbance and concluded that its incidence was 10-30% . Nerve injury, especially Our present results suggested that the posterior injury to the PSAN and the middle superior alveolar superior alveolar nerve (PSAN) is the most import- nerve, seems to occur easily during the operation, ant nerve supplying to the mucous membrane of the because of the very close relationship of these nerves maxillary sinus, and that the PSAN does not run with the mucous membrane. When the PSAN ran along (superficial to) the zygomatic surface of the just beneath the mucous membrane (14 of 37 cases), 322 G. Murakami et al . in particular, it seemed impossible to remove the of cells and fibers in the nervous system. J. Neuropathol. membrane without nerve injury. Currently, the Exp. Neurol., 1953;12:400-403. classical antrostomy employed is a modified version 17) Kopsch, FR. Rauber-Kopsch Lehrbuch und Atlas der Anatomic des Menschen. Band II. p. 460, Georg Thieme, in which only widening of the ostium of the maxillary Stuttgart, 1955. sinus is performed without removal of the mucous 18) Lang, J. Praktische Anatomic. Teil A, p. 465-466, Springer, membrane (Myers, 1987; Buiter, 1981). This seems Berlin, 1985. reasonable in view of the physiological condition of 19) Lang, J. Clinical Anatomy of the Nose, Nasal Cavity and the sinus (Paparella, 1980; Cummings, 1986) as well Paranasal Sinuses. p. 78, Georg Thieme, Stuttgart, 1989. 20) Leonhardt, H, Tillmann, B, Tondury, G, Zilles, K. Rauber- as the anatomy of the superior alveolar nerves, Kopsch Lehrbuch und Atlas der Anatomic des Menschen. which are described in the present study. Band IV, p. 103, Georg Thieme, Stuttgart, 1988. 21) Liebgott, B. The Anatomical Basis of Dentistry. p. 309— 311, Saunders, Philadelphia, 1982. Acknowledgements 22) Lillie, RD. Histopathologic and Practical Histology, 3rd ed. p. 539-540, McGraw-Hill, New York, 1965. 23) Luc, H. Une nouvelle methode operatoire pour la cure We thank Prof. Tooru Sato (Nippon Dental radicale et rapide de l'empyeme chronique du sinus maxil- University) and Prof. Noboru Goto (Showa Univer- laire. Arch. Internationale de Laryngologie, Rhinologie, sity School of Medicine) for their encouragement Otologie (Paris), 1987;10:273-282. during this study. 24) McMinn, RMH. Last's Anatomy. 8th ed., p. 459, p. 473, p. 477, Churchill Livingstone, London, 1990. 25) Myers, EN. Caldwell-Luc operation and extensions. Goldman, J. L. ed. in The Principles and Practice of References Rhinology, p. 455-457, Wiley, New York, 1987. 26) Nair, PNR, Luder, HU, Schroeder, HE. Number and size- 1) Anson,BJ. Morris'Human Anatomy. 12th ed., p. 1031, spectra of myelinated nerve fibers of human premolars. McGraw-Hill,New York, 1986. Anat. Embryol., 1992;186:563-571. 2) Berkovitz, BKB, Holland, GR, Moxham, BJ. Oral 27) Nishi, S. Topographical Atlas of Human Anatomy. Vol. 1., Anatomy.p. 85, Wolfe,London, 1977. p. 23-25, Kanehara, Tokyo, 1974. 3) Buiter,CT, Straatman, NJA. Endoscopic antrostomy in the 28) Noback, CR, Dermarest, RJ. The Human Nervous System. nasalfontanelle. Rhinology, 1981;19:17-24. 3rd., p. 165, McGraw-Hill, New York, 1981. 4) Caldwell,GW. Diseaseof the accessorysinuses of the nose, 29) Paparella, MM, Shumrick, DA. Otolaryngology, 2nd ed. and an improvementmethod of the maxillaryantrum. N.Y. Vol. 1., p. 147, Saunders, Philadelphia, 1980. Med.J., 1893;58:526-528. 30) Piersol, GA. Human Anatomy, 4th ed., p. 1238, Lippincott, 5) Clemente, CD. Anatomyof the HumanBody, 30th ed., Philadelphia, 1913. p. 1165,Lea & Febiger,Philadelphia, 1985. 31) Reader, A, Foreman, DW. An ultrastructural quanti- 6) Cryer,MH. The InternalAnatomy of the Face.2nd ed., tative investigation of human intradental innervation. J. p. 146,Lea & Febiger,Philadelphia, 1916. Endodont. , 1981;7:493-499. 7) Cummings,CW. Otolaryngology —Head and Neck Surgery, 32) Romanes, GJ. Cunningham's Textbook of Anatomy, 12th 1sted., Vol. 1, p. 848,Mosby, St. Louis,1986. ed., p. 750-753, Oxford University Press, Oxford, 1981. 8) DuBrul,EL. Sicherand DuBrul'sOral Anatomy. 8th ed., 33) Rouviere, H. Anatomic Humaine. Delmas, A. ed. Tome p. 236,p. 269-273,Ishiyaku EuroAmerica, St. Louis,1988. 1, p. 264, Masson, Paris, 1974. 9) Heasman,PA. The myelinatedfiber contentof human 34) Schaffer, EA, Symington, J, Eryce, TH. Quain's Elements inferior alveolar nerves from dentate and edentulous of Anatomy, 11th ed. Vol. 3. Neurology, Part 2., p. 20, subjects.J. Dentistry,1984;12:283-286. Longsmans & Green, London, 1909. 10) Hyrtl,J. Lehrbuchder Anatomicdes Menschen. 9th ed., 35) Schaeffer, JP. Morris' Human Anatomy, 11th ed., p. 1092, p. 804,Eilhelm Braumiiller, Wien, 1866. Blakiston, New York, 1953. 11) Hollinshead,WH. Anatomyfor Surgeons.Vol. 1, p. 328— 36) Shapiro, HH. Maxillofacial Anatomy, p. 321-322, 329,Harper & Row,New York, 1982. Lippincott, Philadelphia, 1954. 12) Johnsen,DC, Harshbarger,J, Rymer,HD. Quantitative 37) Spalteholz, W. Handatlas der Anatomic des Menschen. assessmentof neural developmentin human premolars. Band III. p. 715-716, Hirzel, Leipzig, 1922. Anat. Rec. , 1983;205:421-429. 38) Spitzka, EA. Gray's Anatomy. American 1st ed., p. 984, 13) Kerr, AG, Groves,J. Scott-Brown'sOtolaryngology. 5th Lea & Febiger, New York, 1913. ed. Vol. 1., p. 158,Butterworth's, London, 1987. 39) Takayama, Y. Anatomical study of the superior alveolar 14) Killey,HC, Kay, LW. The maxillarysinus and its dental nerves. J. Tokyo Dental College Soc., 59: 1097-1123. implications.p. 12,John Wright& Sons,Bristol, 1975. 40) Toldt, C. An Atlas of Human Anatomy. English. ed. by 15) Kimura,K, Takahashi,Y. Applicationof silverimpreg- Paul, M. E. , Vol. 1, p. 861, Macmillan, New York, 1919. nationfor peripheralnerve fiber analysisin topographical 41) Warwick, R. Eugene Wolff's Anatomy of the Eye and anatomy A communicatingbranch of the lateral sural Orbit. 7th ed., p. 313-315, Lewis, London, 1976, cutaneousnerve to the suralnerve in thecrab-eating monkey 42) Williams, PL, Warwick, R. Gray's Anatomy. 36th ed., (Macacafascicularis). Acta Anat. Nippon. , 1985;60:8-10. p. 1063, Churchill Livingstone, London, 1980. 16) KlUver,H, Barrera,E. A methodfor thecombined staining Superior Alveolar Nerves and Maxillary Sinus 323

Plate I

Explanation of Figures

Plate I

Schematic representation showing variations in descriptions in anatomy textbooks regarding the course of the superior alveolar nerves and the location of the superior dental plexus. A. The posterior (P) and middle (M) superior alveolar nerves run outside the maxilla and form the superior dental plexus (SDP). MS: maxillary sinus. B. The posterior and middle alveolar nerves run beneath the mucous membrane of the maxillary sinus, and the plexus is also located beneath the mucous membrane. A: anterior superior alveolar nerve, G: greater palatine nerve, IF: infraorbital nerve, MX: maxillary nerve, asterisk: branch supplying the posterior part of the palate. 324 G. Murakami et al.

Plate II

The posterior superior alveolar nerve and its branching in the postero-lateral wall of the maxillary sinus. Viewed from the medial side (inside) of the sinus. The mucous membrane and the medial wall of the sinus have been removed. In this case, the posterior superior alveolar nerve (P) runs through a canaliculus in the postero-lateral wall of the maxillary sinus. Note that the nerve P gives off many twigs to the mucous membrane of the sinus through its course in a canaliculus. Note that the posterior part of the superior dental plexus (SDP) is located anteriorly to the antero-inferior border of the maxillary sinus (dotted line). Arrow: a branch leading to the posterior part of the palate, Arrowhead: nerve twigs which were cut upon removal of the mucous membrane of the sinus, G: greater palatine nerve, IF: infraorbital nerve, M: middle superior alveolar nerve, PAL: hard palate. Superior Alveolar Nerves and Maxillary Sinus 325

Plate III

Nerve plexus beneath the mucous membrane of the maxillary sinus. Viewed from the outside of the mucous membrane. This plexus was composed of nerve twigs (arrowhead), which arose from the posterior superior alveolar nerve (P). Black fragments (asterisk) are inclusion bodies in the mucous membrane. Several artifacts of silver impregnation (arrow) were caused by the strong lighting used for taking the photograph. Scale: 1 mm. 326 G. Murakami et al .

Plate IV

Cross-section histology of the nerve plexus of the maxillary sinus and posterior superior alveolar nerve. Staining with luxol fast blue and piero-fuchsin solution. The bony wall of the sinus has been removed. A: Low magnification. Two nerve twigs of the plexus are evident (arrow). The posterior superior alveolar nerve is composed of nerve bundles (N). The nerves are located along with arterioles (A) and venules (V) adjacent to the bony wall of the sinus. MM: mucous membrane, Scale: 20011m. B and C are higher-magnification views of the areas circled in A. B: A nerve bundle of the posterior superior alveolar nerve. The bundle is composed mainly of myclinatcd fibers of intermediate size (3-8 pm in diameter). Large myclinated fibers (arrowhead) arc sometimes observed. Numerous unmyelinated fibers (arrow) are also evident. Scale: l0 µm. C: A nerve twig of the plexus. A few myelinated fibers (arrowhead) are present. Arrows: unmyelinated fibers. Scale: 10 p.m. Superior Alveolar Nerves and Maxillary Sinus 327

Plate V

Anterior part of the superior dental plexus. Viewed from the left side of the face. The anterior superior alveolar nerves (A) divide into fine twigs, which connect with each other to form the superior dental plexus (SDP) in the thick alveolar process of the maxilla . IF: infraorbital nerve, Ml: location of the first molar teeth. 328 G. Murakami et al.

Plate VI

Schematic drawing summarizing the results of the present study. The posterior (P) and middle (M) alveolar nerves ran inside the maxilla. Twigs from P formed the "nerve plexus of the maxillary sinus" (star) beneath its mucous membrane. The mucous membrane of the sinus was innervated mainly by P, and partly by M. The superior dental plexus (SDP) was separated from the plexus of the sinus by the bony wall of the sinus. The SDP was located in the alveolar process of the maxilla and did not face the sinus. A: anterior superior alveolar nerve. G, greater palatine nerve, IF: infraorbital nerve, MX: maxillary nerve, Asterisk: branches to the posterior part of the palate.