The Natural History and Pathogenesis of the Cranial Coronal Ring

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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 syn- drome have prompted this developmental study on the system of ar- ticulations 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, sphe- noid, 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 sur- gery. 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 artic- ulations beginning with the coronal suture per se, the lateral frontosphenoid and the orbital fron- tosphenoid 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., be- tween the right and left optic foramina. In an earlier developmental description, Blechschmidt (1978) looked not only at the articulations be- tween 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, con- nected 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 mid- facial 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.
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