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- -- LA 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