The Natural History and Pathogenesis of the Cranial Coronal Ring

The Natural History and Pathogenesis of the Cranial

Coronal Ring Articulations: Implications in Understanding the Pathogenesis of the Crouzon Craniostenotic Defects

ALpHonsE R. BURDI, PH.D. ADA B. KUSNETZ JoAn L. VENES, M.D. STEPHEN S. GEBARsKI, M.D.

The craniostenotic birth defects seen in patients with Crouzon syndrome have prompted this developmental study on the system of articulations between the human frontal, sphenoid, and ethmoid bones. The Crouzon facies, including midfacial hypoplasia and exorbitism, have been linked to the premature synostosis of calvarial sutures. However, considerable evidence shows that midfacial positioning is linked to increasing length of the midline cranial base. Thirty-seven typical-for-age (8 to 29 weeks) embryos were histologically prepared, read serially, and three-dimensionally reconstructed to map the so- called coronal ring articulations that continuously join the frontal, sphenoid, and ethmoid bones. A morphologic staging plan was used to show the progressive development of bones and intervening joints. Data show that a coronal ring exists beginning at 8 weeks. Those portions of the ring separating the frontal and sphenoid bones (within the orbit and laterally along the coronal suture) show the typical structure of a five-layered suture. This sutural component of the ring is C-shaped with a cartilaginous bridge between the optic foramina completing the ring. This is the sphenoethmoidal (S-E) synchondrosis of the midline cranial base. It is suggested that this deeply located cartilage joint is the primary site of pathogenesis in the craniostenotic facies and not the coronal sutures which are operated upon. Even though the S-E cartilage would be difficult and potentially morbid to approach surgi- cally, this study would suggest that preoperative computed tomogra- phy (CT) of the skull base with special emphasis on the S-E region may provide a better prognosis regarding midface growth effects after surgery. It appears to be the fused S-E synchondrosis and not necessari- ly the premature closure of the coronal sutures that may tether the midface posteriorly.

The birth defects of Crouzon and Apert's syn- craniofacial malformations associated with dromes belong to a class of craniostenotic premature closure of select calvarial sutures, midfacial hypoplasia, and exorbitism (e.g., War- kany, 1971; Kreiborg and Pruzansky, 1971; Co- The authors are affiliated with the University of Michi- hen, 1975; Gorlin et al, 1976; Stewart and gan, Ann Arbor, Michigan. Dr. Burdi and Ms. Kusnetz are with the Department of Anatomy and Cell Biology. Dr. Venes Prescott, 1976; Cohen, 1980; Ousterhout and is with the Department of Surgery (Neurosurgery and Pedi- Melsen, 1982). With the advent of modern sur- atrics). Dr. Gebarski is with the Department of Radiology gical approaches (Tessier, 1976) and CT imag- (Neuroradiology). Dr. Burdi is also affiliated with the Center ing for preoperative planning, these for Human Growth and Development. malformations appear to be more treatable to- This research was supported, in part, by NIH (NIDR) grant DEO3610-19 and the University of Michigan Medical School day than they were 20 years ago. The Apert's funds for medical student research support. Ms. Kusnetz was malformation, however, is still thought to be also supported by a March of Dimes Research Fellowship. more severe than Crouzon, with regard to the 28 Burdi et al, CRANIAL CORONAL RING ARTICULATIONS 29 morphologic disarrangement of craniofacial parts, and hence, generally less amenable to cor- rective surgery. Most surgical approaches to the treatment of the Crouzon head and face deal with one or several sutures comprising what is now known as the coronal ring. The coronal ring (Venes and Burd1, 1985) is a continuous set of cranial articulations beginning with the coronal suture per se, the lateral frontosphenoid and the orbital frontosphenoid articulations. From a surgical per- spective, this arrangement of articulations is in reality a C-shaped sutural system with a lack of continuity at the midline cranial base, i.e., between the right and left optic foramina. In an earlier developmental description, Blechschmidt (1978) looked not only at the articulations between the developing calvarial bones but also at the earlier phases of mesenchymal thickenings and dural tracts in areas where cranial bones FIGURE 1 The coronal ring. Expansion at the cranial and intervening sutures were expected to de- sutures (dark arrows) along the C-shaped ring segments allows for expansion of the cranium. Expansion of the velop. Based on these dural tissue tracts, it was midline sphenoethmoidal synchondrosis (striped) allows then proposed that the coronal sutural system was for forward positioning (open arrows) of the midface. indeed a closed ring completely continuous at the middle cranial base. That is, the gap between the right and left optic foramina was spanned by a observable beginnings in the human embryo. dural stretch field which, in other words, connected the orbits. The implications of these two MATERIALS AND METHODS alternate views, i.e., C-shaped versus closed-ring The sample for this study was chosen to arrangement of articulations, are interesting. Ful- demonstrate the developmental history of the hu- ly formed sutures along the C-shaped system are man coronal articular system. Accordingly, post- cranial and, according to the literature, (e.g., natal and neonatal skulls were selected to Moss and Young, 1960; Scott, 1967; Moyers and complement observations from histologic prepa- Krogman, 1967; Crelin, 1969; DeBeer, 1971; rations of human fetal and embryonic specimens. Burdi, 1977; Pierce et al, 1978; Enlow, 1982) should affect primarily the shape and position of Skulls the cranial bones. Should a closed-ring system This series of five normal white skulls included of coronal articulations be in place, on the other four intact skulls and one disarticulated skull of hand, then expansion at the sutures along the C- a white child. The ages determined by the den- shaped ring segments will allow expansion of the titions in place include a neonatal skull, two child calvarium while the basilar segment of the ring skulls showing deciduous teeth, one skull with (between the right and left optic foramina) will mixed dentition, and a single adult skull with the grow as a part of the cranial base and thus have permanent teeth fully erupted. an effect primarily on the positioning of the midfacial region (Fig. 1). Prenatal Sample With this in mind, this study has been designed This series of 37 human prenates was select- to demonstrate the presence of either a C-shaped ed as a sample which would show each of the or closed-circle system of articulations in what bones along the coronal ring in their sequential is known as the coronal ring. In addition, and condensed mesenchymal, cartilaginous, or bony most importantly from the perspectives of nor- morphologic phases. This series ranged in size mal and abnormal development of the coronal from 29 mm to 280 mm crown-rump length ring, this study reports the natural history of the (CRL) or from 8 to 29 weeks fertilization age. coronal system of articulations from its earliest The embryos and fetuses used were judged

30 Cleft Palate Journal, January 1986, Vol. 23 No. 1 typical-for-age or ''normal'' in that they showed TABLE 1 Prenatal Study Sample®* no physical size or somatic malformations. Fertilization Age Specimens were also assigned to the 'normal'" EH** CRL (mm)? (wks) Section Plane? category since there were no indications from the First Trimester Specimens medical histories accompanying each specimen _ 292 29 8 F to suggest that the development of each speci- 1624 40 9 F men was anything but typical-for-age or ''nor- 356 45 9.5 F 1122 50 10 F mal.'' One specimen, however, was included in 784 55 10-11 F the study simply because it was a confirmed 754A 60 10-11 F Warfarin-exposed stillbirth and fortuitously was 1397 71 11-12 F 1545 73 11-12 F available to this study. Even though it does not 628 75 11-12 F belong in the craniostenosis classification, e.g., Second Trimester Specimens Crouzon, by its Warfarin pathogenesis, it did 727 81 12-13 F show facies that were similar to those seen in the 536 94 13-14 F 800K 111 14-15 F craniostenotic class of defects, e.g., reduced cal- 1625 111 14-15 F varial size, fusion of some sutures in the coronal 1580 119 15 F 1544 125 15-16 F ring system, midfacial hypoplasia, and bulging 1440 127 15-16 S eyes. This Warfarin specimen was age- and size- 1556 138 16 S/F matched with one of the "normal"" specimens 1566 145 17 F 1564 148 17 +1 S/F for morphologic comparisons. 1454 155 18 +1 F Each of the prenatal specimens was received 1557B 160 18 +1 F fresh [Shepard's (1971) Class I-good color, no 1560 170 18-19 F 1483 178 19-20 F signs of autolysis or maceration] and then im- 1527 180 19-20 F mediately fixed in 10 percent neutral buffered 1527B 183 19-20 F 1516 188 20-21 F formalin. Specimens were then prepared for 1617 189 20-21 F light microscopy by celloidin-paraffin embed- 1553 192 20-21 F ding, serial sectioning at thicknesses of 10 to 15 1446 200 21-22 F 1551 200 21-22 S/F micra, and subsequent staining with a trichrome 1570B 208 22 F connective tissue stain, e.g., Mallory or Mas- 1514 215 22-23 F son. Most specimens were serially sectioned in Third Trimester Specimens the frontal plane, one specimen was sectioned 1456 228 ' 23-24 F 1455 230 24 F in the sagittal plane and three specimens were 1515 235 24-25 F sectioned in both the frontal and sagittal planes 1482 253 26 F on a half-head basis. A complete listing of all 1539 280 28-29 F

embryos and fetuses used is given in Table 1. * From University of Michigan Embryology Research Collection ** Identification number-embryo human (EH) OBSERVATIONS t Crown-rump length (CRL) { F=frontal, S= Sagittal Postnatal Articular Patterns In each of the four intact skulls studied, the 1975). Moving downward and laterally from the coronal ring under question was first picked up coronal suture in each of the four intact skulls, at bregma, which is at the junction of the sagit- one could easily see the continuation of the tal and coronal sutures. The adult cranium coronal suture into the frontosphenoid and showed an almost complete ossification of this sphenozygomatic sutures on the lateral aspect of region. Ossification of this bony junction atop the cranium. Continuing into the orbits, the su- the skull was also seen in skulls with mixed and ture between the frontal bone and the lesser wing primary teeth. The junction of the coronal, sagit- (i.e., orbitosphenoid) was easily observed in each tal, and even the frontal (or metopic) sutures was orbit. Up to this point in the observations the su- a large, unossified and almost triangular region tures described represented a C-shaped sutural of membranous tissue known as the anterior fon- complex appearing as a continuous line of inter- tanelle. It is expected that this large fontanelle digitating small bony processes along the edges does not completely ossify until approximately of each bone defining this C-shaped articular sys- the middle of the second year of life (Goss, tem. The degree of closure of these sutures ap- Burdi et al, CRANIAL CORONAL RING ARTICULATIONS 31

FIGURE 2 Endocranial view of the anterior and middle cranial fossae in a young white skull demonstrating the patent synchondrosis between the sphenoid and epthmoid bones (S-E) and the sutures between the frontal and sphenoid bones (EF-S). peared to be inversely related to the age of the of the cranium, and back to bregma. In the care- skull, which is an observation consistent with the fully disarticulated skull from a child with erupt- literature (Krogman, 1962). Looking next at the ed primary dentition, the frontal, zygomatic, articulation between the ethmoid bone with the sphenoid, and ethmoid bones cleanly separated body of the sphenoid and its connected lesser wings, this articulation lying medial to the right and left optic foramina appeared as a "suture- like"" articulation. As with the sutural descrip- FRoWTaL tions above, the midline articulation is often referred to as the sphenoethmoid articulation or suture. This midline articulation between the sphenoid and ethmoid bones was patent in the youngest cranium (Fig. 2) after which it appeared to become progressively more ossified so that in the adult cranium only a faint line marked the midline sphenoethmoid articulation. The sphenoethmoid articulation gave every appear- ance of being continuous laterally with the fron- FORAMEN tosphenoid suture and the remaining sutural links MAGNUM in the coronal suture system (Fig. 3). It appeared then that the coronal suture system, at least as FIGURE 3 Continuity of the sphenoethmoidal articu- seen in the youngest of skulls or in those with lation (striped) with the frontosphenoid suture. The ar- unerupted primary dentitions, was a completely rows indicate the continuing direction of the sutural segments of the coronal ring. MES = mesethmoid, B = continuous system of articulations from bregma body of sphenoid, LW = lesser wing of sphenoid, GW to the midline cranial base, up to the other side = greater wing of sphenoid, OC = basiocciput.

32 Cleft Palate Journal, January 1986, Vol. 23 No. 1

along a circular system of continuous articula- lation with the frontal bone and the lesser wing tions, corresponding to the proposed coronal of the sphenoid. Throughout this third trimester ring. Figures 4A and 4B show frontal, ethmoid, the sphenoid body consisted of an outer crust of and sphenoid bones and indicate matching artic- ossified bone tissue covering a center which was ular surfaces between the bones. predominantly cartilage. The ethmoid bone consisted of its midline cartilage extending from the Prenatal Articular Patterns midline sphenoid region downward into the nasal Light microscopy observations essentially ex- - cavity as the cartilaginous nasal septum. Along tended the above postnatal observations into each this diagonal course the septum articulated in- of the three trimesters of intrauterine develop- feriorly with the ossifying vomerine bone. Later- ment. The following observations are presented ally, the ethmoid bone showed progressive as a series of developmental stages in the mem- ossification and was perforated by fibers of the branous and endochondral ossification stages olfactory nerve and accompanying blood vessels. recorded for each of the cranial bones lying on This midline area formed the cribriform plate. either side of the circular arrangement of artic- The midline articulation between the ethmoid ulations called the coronal ring. Sutural and bone bone and the presphenoid region of the sphenoid development patterns are also referenced with the bone was a relatively extensive area of cartilage fertilization ages and crown-rump length (CRL) and showed no sutural morphology. Sutural mor- of each of the sectioned embryos and fetuses (Ta- phology was clearly seen in segments of the ble 1). coronal ring lateral to the optic foramina and dis- In the five third trimester specimens (24 to 29 tal articulations of the lesser wing of the weeks, 228 to 280 mm CRL), the frontal bone sphenoid. showed advanced ossification in both its verti- Observations of twenty-three second trimester cal and orbital plates. The sphenoid bone showed specimens (13 to 23 weeks; 81 to 218 mm CRL) its adult shape with a body, lesser and greater showed that each of the bones along the coronal wings. The lesser wing or orbitosphenoid was ring had already taken on their definitive or post- chiefly ossified but with some islands of cartilage natal shapes. The frontal bone appeared less os- still remaining in its lateral most extent beyond sified than in the third trimester with wider the optic foramen. There were occasional small sutural tissues between the frontal and sphenoid islands of ectopic cartilage seen near the articu- bones (Figs. 5A and 5B). The lesser wing of the

S ﬁst

B FIGURE 4 A . Disarticulated frontal and ethmoid bones (posterior view). The striped posterior region of the eth- articulatemoid articulates with the with darkened the striped areas anterior of the region sphenoid of the bone sphenoid in Figure body 4B.in Figure Note the4B. continuousThe darkened ring frontal of articulations, bone areas i.e.of the the sphenoid Coronal body Ring. which B . Disarticulated articulates with sphenoid the ethmoid. bone The(anterior darkened view). areas The along striped the region greater represents wings of thethat sphenoid portion articulate with the frontal bone surfaces shown in Figure 4A. '

Burdi et al, CRANIAL CORONAL RING ARTICULATIONS 33

,v,l';‘:’f ;'/ {Jyﬁ/

FIGURE 5 A . Frontal section through posterior depths of orbits in a second trimester fetus demonstrating the sphenoid body (S), lesser wings of the sphenoid (LWS) extending off the sphenoid body, and the frontal bone (FB) extending medially toward the lesser wing of the sphenoid bone. Note the continuity of the cartilaginous basicranium. EH 1580, 119 mm CRL, 15 weeks. Magnification x 28.5. B . A magnification x 57 of Figure 5A. ON = optic nerve, FSS = frontosphenoid suture, FB = frontal bone, S = body of sphenoid, LWS = lesser wing of sphenoid. The region of the frontosphenoid suture is highlighted by the dashed line.

sphenoid extended laterally toward the sutural nerve. With increasing age through 20 weeks, articulation between the frontal bone and great- the lesser wing ossified following a lateral to er wing of the sphenoid. At 15 weeks, 119 mm medial gradient with a denser crust of bone form- CRL, the lesser wing appeared as a long lateral ing around the optic foramen (Fig. 6). The extension of cartilage coming off the basisphe- basisphenoid appeared to progressively ossify noid. This wing was perforated by the optic along its dorsum and sides with signs of ossifi-

34 Cleft Palate Journal, January 1986, Vol. 23 No. 1

FIGURE 6 Frontal section comparable to that in Figures 5A and 5B but in an older second trimester fetus. The optic nerve (ON) is passing towards the optic foramen (OF). A thin crust of bone tissue (BT) is forming along the outer edge of the optic foramen. FB = frontal bone, LWS = lesser wing of sphenoid, GWS = greater wing of sphenoid. EH 1560, 170 mm CRL, 18 to 19 weeks. Magnification x 57. cation along its inferior or pharyngeal surface. hypoplasia with shallow orbits and exorbitism. The basisphenoid demonstrated the concavity of More importantly, this abnormal fetus showed the pituitary fossa (sella turcica) as early as 15 chondral abnormalities in the cartilaginous crani- weeks. Again, small islands of presumably ec- al base at the sphenoethmoidal junction. This topic cartilage were seen between the frontal and junction also gave some indications of a prema- lesser wings of the sphenoid extending across the ture ossification in the lower portion of the syn- orbital roof. The medial mass of the developing chondrosis. ethmoid bone was almost completely cartilage The nine first trimester embryos (8 to 12 during this trimester, yet there were some areas weeks, 29 to 75 mm CRL) examined histologi- of ossification along the superior and lateral cally showed the clearest picture of each of the aspects of the lateral wings of the ethmoid or coronal ring bones progressing from their mesen- nasal capsule. With increasing age in this chymal templates into either a subsequent car- trimester the ethmoid labyrinths and nasal con- tilage model or ossified form. The cartilage chae progressively ossified to yield the anatom- models for the basisphenoid, lesser wings of ic form of the third trimester ethmoid bone. sphenoid, and ethmoid bones assumed the shapes Ossification of the labyrinths and conchae oc- already established by dense and deeply stain- curred after the 15-week period or 119 mm CRL. ing mesenchymal cells (Fig. 7). The frontal Taking advantage of having a Warfarin- bone's vertical and orbital plates showed a shift associated fetus, a 16-week (138 mm CRL) nor- from the mesenchymal model directly into bony mal fetus was matched with the 16-week (127 plates. Ossification of this bone appeared to be- mm CRL) Warfarin fetus, and a comparison of gin close to the bone's periphery as outlined by coronal ring structures and articulations was concurrent condensation of mesenchyme des- made. The Warfarin fetus showed midfacial tined to form the periosteal and cambial layers Burdi et al, CRANIAL CORONAL RING ARTICULATIONS 35

in ossification while the sphenoid and ethmoid bones showed more cartilage than mesenchyme in their makeup. Sutures during this first trimester period appeared chiefly as a mesenchymal field intervening between the frontal and sphenoid bones. The mesenchyme of the sutures first appeared as a continual field with mesenchyme for the bones. However, as age increased sutural mesenchyme stained more deeply and took on the typical five-zone sutural morphology (Pritchard et al, 1956). Only the oldest specimens of the first trimester group demonstrated the beginnings of a typical five-layered suture. The midline articulations between the sphenoid and ethmoid bones in the youngest specimens appeared to be a continuous field of chondrifying mesenchyme. In the 10- to 12-week specimens, sutures already began to show layering wherein there was a cellular osteogenic layer forming a periosteal zone along the periphery of most articulations in the coronal ring, an intermediate fibrous layer, and a middle zone through the developing articulation consisting of fibers cours- ing almost transversely across the sutural region. This anatomic evidence for sutural morphogen- FIGURE 7 Frontal section through orbits of a first esis did not extend across the midline sphenoeth- trimester fetus demonstrating the continuity of the mid- moidal articulation. line cartilaginous sphenoid body (S) and lesser wings of sphenoid (LWS). The frontal bone (FB) is approaching DISCUSSION the sphenoid to form the frontosphenoid suture. EH 1122, Observations in this study reaffirmed the spa- 50 mm CRL, 10 weeks. Magnification x 57. tial arrangement of each of the bones along the coronal ring from their earliest prenatal beginnings through the postnatal period (Warwick and of the sutures surrounding the frontal bone. The Williams, 1980; Arey, 1965; Goss, 1975). Bone sphenoid bone, now in its mesenchymal form, shapes were evident as soon as mesenchymal showed its body beneath the pituitary gland. thickenings for each of the bones became evi- Lesser wings consisting of mesenchymal cells dent. More definitive and localized bony fea- extended laterally as tapering extensions off the tures, i.e., foramina and crests, became evident body. There were no indications of a contoured as bones like the sphenoid and ethmoid entered optic foramen at this stage even though the op- their cartilaginous phase. This study showed that tic nerves were in the region. The mesenchyme the articulations between each of the bones defin- of the sphenoid body appeared continuous, with ing the coronal ring did indeed form a complete the mesenchyme destined to form the mesen- ring. However, the ring is not completely sutur- chymal model of the ethmoid bone anteriorly. al. In essence, the midline articulation between The ethmoid bone showed medial and lateral the sphenoid and ethmoid bones is cartilaginous masses of condensed mesenchymal cells. and should properly be named the sphenoethmoi- However, there was little indication in the youn- dal synchondrosis (Ford, 1958). The extensions gest specimens of the developing superior and of the ring laterally and upward as the coronal inferior nasal conchae. As mentioned above, the suture are typically sutural (Fig. 8). ethmoid mesenchymal mass was continuous Apart from the following clinical implications posteriorly with the mesenchymal mass of the of this study, the embryologic and anatomic ob- sphenoid bone. At approximately 10 weeks, 50 servations on the natural history of the set of ar- mm CRL, the frontal bone showed early stages ticulations, called the coronal ring, have import 36 Cleft Palate Journal, January 1986, Vol. 23 No. 1

FRONTAL

.r 4"/

is SYNCHONDROSIS

FORAMEN MAGNUM

FIGURE 8 The coronal ring-sutures and synchondrosis (inset). The sphenoethmoidal articulation (striped) is car-

tilaginous and thus a synchondrosis, while the remainder of the ring is sutural. The arrows represent the continua-

tion of the coronal ring.

for the classical anatomist. That is, most current Beer, 1971; Warwick and Williams, 1980) even

and leading textbooks of anatomy correctly though such descriptions did not go on to spe-

describe the majority of joints along the coronal cifically identify a midline synchondrosis be-

system of articulations as being sutural in struc- tween the sphenoid and ethmoid bones.

ture, as described by Pritchard et al (1956). The articulations between these midline bones

These sutural articulations between the frontal in the developing prenate and in the growing

and sphenoid bones are appropriately recognized child are cartilage and also derive from the car-

also in the official language of the anatomist as tilaginous cranial base or chondrocranium. Thus,

listed in the Nomina Anatomica (Warwick, while the midline articulation between the sphe-

1968). However, in 1968 the Nomina Anatomi- noid and occipital bones has been unequivocal-

ca identified the midline articulation between the ly recognized as a synchondrosis (i.e., the

body of the sphenoid and the ethmoid bone solely spheno-occipital synchondrosis), the midline ar-

as a suture, i.e., the sphenoethmoid suture. The ticulation between the sphenoid and ethmoid

same classification of the sphenoethmoidal ar- derivatives of the chondrocranium continues to

ticulation as a suture typically appears in lead- escape full recognition and classification solely

ing anatomical textbooks (e.g., Gray's Anatomy, as a synchondrosis as evidenced by the last two

1985). editions of the Nomina Anatomica (Warwick,

This study shows that the midline articulation 1977 and 1983).

between the body of the sphenoid and ethmoid The embryologic and structural observations

bone is not sutural. Based on the age-by-age, of this study should leave little doubt that the

fetus-by-fetus morphologic staging in this study, midline articulation between the sphenoid and

one new finding from this study is that the mid- ethmoid bones is solely a cartilaginous articula-

line articulation between the sphenoid and eth- tion, i.e., the sphenoethmoidal synchondrosis,

moid bones is indeed a synchondrosis in that the which develops in the same manner as the

bones arranged in the midline cranial base evolve spheno-occipital synchondrosis.

from the embryonic chondrocranium. This key The segmental composition of the coronal

observation is corroborated by traditional em- ring, i.e., the sphenoethmoidal synchondrosis

bryologic descriptions (e.g., Patten, 1968; De- plus the frontosphenoid sutures, becomes impor- Burdi et al, CRANIAL CORONAL RING ARTICULATIONS 37

tant in understanding normal and abnormal Crouzon surgery involving a freeing up of fused growth effects of the coronal ring. As noted calvarial sutures has reportedly greater effects above, the midline sphenoethmoid synchondro- on the subsequent growth of the calvarium than sis is one of two cranial base synchondroses, i.e., the face (Freide et al, 1983). Secondly, Stewart the other being the spheno-occipital synchondro- (1977) reported the unusual case of an Apert's sis, which derive from the chondrocranium in syndrome individual who had unfused calvarial the embryo (Fig. 9). Their continuing growth ac- sutures but with typical Apert's facies. This study tivity through the periods of adolescence affects suggests that there may have been a premature the increasing length of the cranial base (Koski, synostosis of the sphenoethmoidal synchondro- 1975; Scott, 1954). It is to this cranial base that sis which led to the mldfa01al hypoplasia in the the midface is attached. As shown in Figures 10A Stewart case study. and 10B, coronal ring sutures are associated with The current study corroborates the reports by growth changes in size and shape of the calva- Kreiborg et al (1976) and Ousterhout and Mel- rium whereas the cranial base synchondroses, sen (1982) which pointed to cranial base patho- e.g., sphenoethmoidal, is linked with growth genesis in Apert's syndrome. However, those changes in size and positioning of the midface studies postulated that the spheno-occipital syn- (Enlow, 1982). With this in mind, this study chondrosis was the primary site of premature fu- hypothesizes that the midfacial hypoplasia and sion. In this study, however, we postulate that retropositioning of the midfacial bones may have the sphenoethmoidal synchondrosis is the as their underlying pathogenesis abnormal con- primary pathogenic site. The apparent premature ditions where the sphenoethmoid synchondrosis bony fusion of the sphenoethmoidal synchondro- either fails to develop or prematurely ossifies in sis in our single Warfarin fetus, which also the growing Crouzon head. demonstrated exorbitism, lends some support to Our hypothesis suggests that the prematurely our view that a premature bony fusion of the fused cranial sutures in Crouzon may not be the sphenoethmoidal synchondrosis may act as the primary sites of pathogenesis. In other words, ''tethering'' mechanism in the anterior cranial premature fusion of the cranial sutures may be base. This ""tethering'" could lead to hypoplasia a secondary pathogenic event. This may help ex- and retropositioning of the midface in plain several observations in the literature. First, craniostenotic defects, as in Crouzon syndrome.

ANTERIOR CRANIAL BASE

POSTERIOR CRANIAL BASE FRONTAL

NASAL

SPHENOID ETHMOID SPHENO ETHMOIDAL SYNCHONDROSIs OCCIPIT AL SPHENO OCCIPITAL SYNCHONODROSIS

FIGURE 9 A sagittal view of the anterior and posterior cranial base. Note the two cranial base synchondroses-the sphenooccipital and the sphenoethmoidal (both striped).

38 Cleft Palate Journal, January 1986, Vol. 23 No. 1

SUTURES: CALVARIAL S-E SYNCHONDROSIS MDFACIAL B1\

a m B2

Evestus . Fa" L

FIGURE 10 A . Matching disarticulated frontal and ethmoid bones showing coronal ring contact surfaces (posteri- or view). Al-ethmoid articulates with A2 surfaces in Figure 10B. B1-frontal bone surfaces articulate with B2 sphenoid surfaces in Figure 10B. B . Matching disarticulated sphenoid bone (anterior view). A2-sphenoid surfaces articulate with ethmoid (A1 surfaces in Figure 10A) to form the sphenoethmoidal synchondrosis. B2-sphenoid lesser wings articulate with the frontal bone (B1 surfaces in Figure 10A) to form the frontosphenoid suture segment of the coronal ring.

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