A Second Hypothesis Does Not Support the Presence of a Premaxilla In

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Artery Distribution in the Prenatal Human Maxilla

WILLIAM P. MAHER, D.D.S. Milwaukee, Wisconsin 53226

Differing opinions concerning the human maxilla and its morphogenesis lead to different concepts concerning the intrinsic arterial supply to the anterior portion of the maxilla and its incisors. Microscopic and radiographic analyses of appropriately perfused infraorbital and posterior superior alveolar arteries in more than 100 human fetuses from six months to term reveal that the posterior superior alveolar artery courses to the facial midline, supplying branches to the incisors and to the posterior teeth. This observation differs clearly from the classical description that the anterior superior alveolar artery, a branch of the infraorbital artery, supplies the anterior maxillary segment and its incisors as seen in the postnatal life.

Introduction also show that the incisor teeth, developing within the premaxilla, are supplied by dental Callender (1869), Fawcett (1906 and 1911), branches from the anterior superior alveolar Ashley-Montague (1935) Padgett (1948), artery. Conversely, developing posterior teeth Wood-Jones (1947), Woo (1949), and Krause within the maxillary process are supplied by and Decker (1960) summarize dissenting dental branches from the posterior superior opinions concerning maxillofacial morpho- alveolar artery and from its parent maxillary genesis in man and other mammals. High- artery. | ' lights of each of two leading hypotheses con- A second hypothesis does not support the cerning maxillofacial morphogenesis in man presence of a premaxilla in humans. This are presented here so that differences between hypothesis suggests that there is no downward these hypotheses are clear. These differences growing embryonic frontonasal process be- are crucial to the present paper because dis- tween medial growing maxillary processes in senting opinions in regard to maxillary mor- humans and that those who suggest there is phogenesis can lead to dissenting views re- such a process are erroneously drawing con- garding intrinsic arterial supply to the maxilla clusions from phylogeny rather than human and the teeth it contains. ontogeny. Instead, it is maintained that the The leading hypothesis affirms thepresence downward growing frontnasal process divides of a premaxilla in humans. This hypothesis into two slips-a superficial slip extending suggests that there is a downward growing ectofacially and a deep slip extending endo- frontonasal process which intervenes between facially (Figure 1-B). The superfacial slip be- the medial growing maxillary processes, comes the forerunner of the mid-third of the thereby dividing the palatoalveolar area into face and philtrum, while the deeper slip de- a triangular-like anterior segment called the velops into the nasal septum and intermaxil- premaxilla and two lateral segments that are lary bone. The growing maxillary processes formed by the maxillary processes (Figure 1- extend toward the facial midline between the A). Classical human anatomists agree that the superficial and the deep slips of the fronton- anterior superior alveolar artery, branching asal process. This arrangement indicates that from the infraorbital artery, is the intrinsic the incisor and molar teeth develop entirely artery of the frontonasal process (the forerun- within the maxillary processes. Moreover, the ner of the premaxilla). They agree that the posterior superior alveolar artery is then the posterior superior alveolar artery is the intrin- intrinsic artery of the maxillary process. The sic artery of the maxillary process. These views incisor and posterior teeth are supplied by this posterior superior alveolar artery. This paper was presented at the 92nd Annual Meeting of the American Association of Anatomists, Miami, Flor- These differing hypotheses raise the pivotal ida, April 1979. questions of whether branches of the infraor- 51 52 Cleft Palate Journal, January 1981, Vol. 18 No. 1

FIGURE 1. These diagrams represent the two differing hypotheses of maxillary morphogenesis. The top row (A) represents the concept that the downward growing frontonasal process (FNP) intervenes between the forward growing maxillary processes (MP) and contains the incisor teeth (1, 2). The bottom row (B) represents the concept that the forward growing maxillary processes (MP) extend to the facial midline between the ectofacial (ECTOF) and endofacial (ENDOF) slips of the frontonasal process (FNP). Buds of teeth (1-5) develop within the maxillary process.

bital arteries supply the anterior maxillary iorachischisis, hydrocephalus, cleidocranial area and contained incisors or if branches of dyastosis, and uranostaphyloschisis. the posterior superior alveolar arteries from The arterial system of each fetus was man- the maxillary arteries that extend to the facial ually perfused via the ascending thoracic midline supply the incisors. Thus, to which of aorta using a 50 ml. syringe fitted to a canula the two hypotheses of human maxillofacial inserted through the left ventricle and ligated morphogenesis does the intrinsic arterial sup- to the acending aorta. While injection pres- ply to the anterior maxillary area and con- sures were not recorded, it is noted that post- tained incisors actually belong? mortem perfusion pressures (both positive and The purpose of this study is to resolve this negative) can vary greatly because of fetal dilemma by determining the distribution pat- age, general condition of the corpse, differ- terns of infraorbital and posterior superior ences in degree of postmortem changes-par- alveolar arteries during human prenatal life. ticularly those changes which affect the elastic properties of vessel walls, Method differences in the degree of postmortem rigor, temperature of Over 100 spontaneously aborted human the corpse at the time of perfusion, differences fetuses, ranging in gestational age from six in the viscosity of the perfusate and its particle months to birth, were randomly selected for size, and the size, density, and tenacity of this study. While the head and neck regions clotted blood in the arteries and veins. of some of the fetuses appeared to be normal, Various perfusion media were used. (1) some were obviously abnormal in craniofacial Higgins Black India Ink in water (1:10 by development. The abnormal group included volume) was selected because the carbon par- examples of anencephaly, cranioschisis, cran- ticle size is such that the ink will flow sequen- Maher, ArtERIEs or THE MAXxILLA 53 tially through arteries, capillaries, and veins Maxillary blocks obtained from every fetus depending upon the volume perfused (Figure extended from the orbital floors above to the 6). (2) Calcium carbonate in water (50 g/1000 oral cavity below and to the posterior pharyn- ml) was used because the particle size is such geal wall behind. Fetuses perfused with Hig- that it will not pass through precapillary ar- gins Black India Ink or calcium carbonate terioles. Hence, only arteries are perfused. were dehydrated in increasing strengths of Furthermore, photographic properties of ethanol and cleared in grades of xylene fol- CaCO; in cleared specimens can be enhanced lowed by grades of methylsalicylate (Spalten- by incident light so that photographic images holz method). Microdissection was required of arterial vessels will appear white and in to expose some vessels for observation and sharp contrast to the connective tissue envi- photomicrography. Specimens perfused with ronment in which the vessels are embedded cinnabar were only radiographed and were (Figures 7 and 8). (3) Cinnabar (red mercuric not cleared. Photographic prints made from sulphide) in water (50 g/1000 ml) was chosen the radiograms (Figures 2, 3, and 4) were because its particle size is such that it will not enlarged for visual analysis and for compari- pass into capillaries. Hence, only arteries and son with photographs of specimens perfused arterioles become perfused. Cinnabar is also with the other media (Figures 5, 6, 7, and 8). radiopaque and provides unique options for Results radioangiographic analysis (Figures 2, 3, and 4). Tus Inrraorsitat ArtTERv. The infraorbi- Each of the above perfusates possesses dis- tal artery arose directly from the maxillary tinctive characteristics well suited to three artery in close proximity to the posterior su- different modes of arterial imaging using mi- perior alveolar artery (Figure 2). Sometimes croscopy, photography, and radioangiogra- both arteries (infraorbital and posterior su- phy, techniques which lead to increased ac- perior alveolar) were observed arising from a curacy of interpretation. common trunk off the maxillary artery (Fig-

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B:. ) "C *~ Oral N. y* Oral View E FIGURE 2. A positive photographic print made FIGURE 3. A positive photographic print made from a radiogram of a maxilla (oral view) from a 6 month from a radiogram of a maxilla (oral view) from a 6-%4- human fetus, (X 3). Arteries are perfused with cinnabar. month human fetus, (X3). Arteries perfused with cinna- Nasal septum and conchae were removed to improve bar and the nasal septum and conchae were not removed. opportunities to see the greater palatine artery (GPA), All branches of the 2nd and 3rd portion of the maxillary posterior superior alveolar artery (PSAA), infraorbital artery are depicted. Identified are: inferior orbital artery artery (IOA) and their origins from the maxillary artery (IOR), posterior superior alveolar artery (PSAA), greater (MA). Note that there are no branches to the lateral palatine artery (GPA), labial artery (LA) and nasal incisor (2) and central incisor (1) from the infraorbital septum (NS). See Figure 4 for an enlarged view of the artery (IOA). The labial artery (LA) from the facial left one-half viewed from the nasal side. artery is also shown. 54 Cleft Palate Journal, January 1981, Vol. 18 No. 1

FIGURE 4. Left half of the maxilla from Figure 3. Nasal view, enlarged to improve visualization of the 2nd and 3rd portions of the maxillary artery (MA) and branches. Note the inferior orbital artery {IOA), posterior superior alveolar artery (PSAA), greater palatine artery (GPA) and nasal septum (NS). Note: here the posterior superior alveolar and infraorbital arteries arise from the common trunk from the maxillary artery (NA). Also, the infraorbital artery does not give rise to a branch supplying the cuspid (3), lateral incisor (2) and central incisor (1). These structures are supplied by the in- cisal branch of the posterior superior alveolar artery (PSAA). See Figures 5 and 6.

ure 4). The sequence of the origin of these any of the fetuses examined (Figures 2, 3, and vessels may vary-one may take its origin 4). Thus, this finding contradicts classic ac- from the maxillary artery prior to the other. counts of the arterial supply of the maxillary Side-to-side variations were also observed. In incisor area. any case, the artery coursed through the in- Tug posterior Superior ArvroLar Ar- fraorbital fissure and emerged through the TEry. Posterior superior alveolar arteries were developing infraorbital foramen where it di- also traced throughout their courses in each vided into at least two branches (Figures 2, 3, cleared necropsy. In addition to variations in and 4), which formed anastomoses with origin from the maxillary artery, the posterior branches of the facial artery and provided a superior alveolar artery occasionally arose significant contribution to the extrinsic max- from the masseteric branch of the maxillary illofacial arterial network. Occasionally, a artery or from a trunk in common to the short trunk connecting the posterior superior masseteric artery from the maxillary artery alveolar and the infraorbital arteries was ob- (Figure 2). The posterior superior alveolar served in the cuspid or molar areas. That artery entered the maxillary tuberosity and branch of the infraorbital artery described by followed a course above the developing decid- classic anatomists as the anterior superior al- uous teeth, from the last molar to the central veolar artery passing through narrow bony incisor, giving off branches to each tooth and canals to the incisor teeth was not found in its covering tissues. The artery extended to Maher, ArtERrIEs or tHE MaxILLA 55

FIGURE 5. A nasal view of the right half of the maxilla from a seven-month human fetus. The arteries were perfused with cinnabar, and the specimen necropsy was cleared by a Spalteholz method. Observe the infrorbital artery, posterior superior alveolar artery, and nasal septum. The posterior superior alveolar artery arises from the infraorbital artery (see arrow). Note branches of the inferior orbital artery as it emerges through the infraorbital foreman. The artery emits no branches to the incisor area. The posterior alveolar artery passes forward over the apices of the teeth to the central incisor (1). Also identified are: lateral incisor (2), cuspid (canine) (3), Ist deciduous molar (4), and 2nd deciduous molar (5).

the midline in every specimen studied (Fig- posterior superior alveolar arteries in ures 2, 3, 4, 5, 6, and 8). This finding also the same specimen were not always sharply differs with traditional accounts of its similar. distribution with the artery terminating in a The course of the posterior superior alveolar variety of modes, including: artery was found to fit best with the hypoth- 1. anastomosis with the terminal portion esis of maxillary morphogenesis which main- of the greater palatine artery (Figures tains that the embryonic maxillary processes 7 and 8), extend to the facial midline. Because the pos- 2. anastomosis with the terminal portion terior superior alveolar artery is the intrinsic of the sphenopalatine artery, or major artery to each maxillary process as 3. anastomosis with its counterpart on it extends to the midline, it is likely that the the opposite side, and process to which the intrinsic artery is em- 4. termination in two or more branches bedded also extends to the facial midline. forming an anastomosis with the ar- Accordingly, the incisor teeth are supplied by teries described above, dental branches from the posterior superior 5. terminations of the right and the left alveolar artery off the maxillary artery rather 56 Cleft Palate Journal, January 1981, Vol. 18 No. 1

FIGURE 6. Nasal view of the right half of the maxilla from a 7- Y»-month human fetus. The arteries were perfused with India ink and the necropsy was cleared by a Spal- teholz method. Observe the posterior superior alveolar artery and the greater palatine artery. Note branches of posterior superior alveolar artery to dental structure, central incisor (1), lateral incisor (2), cuspid canine (3), Ist. deciduous molar (4) and 2nd deciduous molar (5). The infraorbital artery was removed. Two short trunks (ar- rows) connected the posterior alveolar artery with the infraorbital artery.

than from the anterior superior alveolar artery does take place as it does with the stapedial off the infraorbital artery as traditionally de- artery, for example, it would seem reasonable scribed. to find some indication of such a changeover among the specimens studied. No such indi- Discussion cation was found. One might even expect to find some form of angioplany of either artery Observations on the courses of the infraor- in the abnormal fetuses studied. Yet, none bital and posterior superior alveolar arteries was found. Even if some indication of rem- in this study obviously do not preclude possi- nants of the anterior superior alveolar artery bilities that arterial supply to the anterior were to exist and were either overlooked or portion of the maxilla could have been sup- not recognized, such oversights would not plied by branches from the infraorbital arter- detract from the evidence that the right and ies in much earlier embryonic periods of max- left posterior superior alveolar arteries, visu- illary development. If this is the case, the alized in several ways in this study, were question arises as to the time during maxillo- observed to extend to the facial midline and facial morphogenesis that such change, if any, to supply branches to incisors and posterior takes place. Presuming that a vascular change teeth. Maher, ArteriEs or tes MaxILLA 57

FIGURE 7. Oral view of the palatoalveolar area from a 6-month human fetus. Greater palatine arteries and their principle medial and lateral branches were perfused with calcium carbonate. The specimen necropsy was cleared by a Spalteholz method. The terminal portion of the right greater palatine artery forms a sharp bend at the anterior palate (arrow), and after passing through the palate it is an- astomosed with the terminal portion of the posterior superior alveolar artery. See Figure 8.

58 Cleft Palate Journal, January 1981, Vol. 18 No. 1

FIGURE 8. Nasal view of the specimen illustrated in Figure 7. The greater palatine-posterior superior alveolar anastomosis is clearly shown. Observe the infraorbital artery, posterior superior alveolar artery and greater palatine artery.

Nasal Vie

Reprints: Dr. William P. Maher growth of the palate bone in man. J. Anal. Phys., 40, Asst. Adj. Professor of Anatomy 400-406, 1906. FaweEtr, E. The development of the human maxilla, Department of Anatomy vomer and paraseptalcartilage. /. Anal. Phys., 45, 378- The Medical College of Wisconsin 223, 1911. P.O. Box 26509 Kraus, B. S. ano Decker, J. D. The perinatal interrela- Milwaukee, Wisconsin 53226 tionships of the maxilla and premaxilla in facial development of man. Acta Anat., 40, 278-294, 1960. PapcEtt, D. The development of the cranial arteries in human embryo. Contrib. Embryol. Carnegie Inst., 32, 205- 262, 1948. . Woo, J. Ossification and growth of the human maxilla, References premaxilla and palate bone. Anat. Rec., 105, 737-751, AsHreEy-Montacug, M. F. The premaxilla in the pri- 1949. - mates. Quart. Rev. Biol., 10, 32-59 and 181-208, 1935. Woon-JonEs, F. The premaxilla and the ancestry of man. CarrenpeR®, G. W. The formation and early growth of Nature (London), 139, 439, 1947. the bones of the human face. Phil. Trans., 159, 163-172, Dr. Maher is affiliated with the Department of Anat- 1869. omy, The Medical College of Wisconsin, Milwaukee, FaweEtt, E. On the development, ossification and Wisconsin 53226.