Cranial sutures and bones: growth and fusion in relation to masticatory strain

Abstract

Cranial bones and sutures are mechanically loaded during mastication. Their response to masticatory strain, however, is largely unknown, especially in the context of age change. Using strain gages, this study investigated masticatory strain in the posterior interfrontal and the anterior interparietal sutures and their adjacent bones in 3- and 7-month-old miniature swine (Sus scrofa). Double-fluorochrome labeling of these animals and an additional 5-month group was used to reveal suture and bone growth as well as features of suture morphology and fusion. With increasing age, the posterior interfrontal suture strain decreased in magnitude and changed in pattern from pure compression to both compression and tension, whereas the interparietal suture remained in tension and the magnitude increased unless the suture was fused. Morphologically, the posterior interfrontal suture was highly interdigitated at 3 months and then lost interdigitation ectocranially in older pigs, whereas the anterior interparietal suture remained butt-ended. Mineralization apposition rate (MAR) decreased with age in both sutures and was unrelated to strain. Bone mineralization was most vigorous on the ectocranial surface of the frontal and the parietal bones. Unlike the sutures, with age bone strain remained constant while bone MARs significantly increased and were correlated with bone thickness. Fusion had occurred in the interparietal suture of some pigs. In all cases fusion was ectocranial rather than endocranial. Fusion appeared to be associated with increased suture strain and enhanced bone growth on the ectocranial surface. Collectively, these results indicate that age is an important factor for strain and growth of the cranium. .

Fig. 1

Schematic illustration of strain gage placement. Single-element (rectangle) strain gages were glued to the posterior interfrontal (IF) and the anterior interparietal (IP) sutures. The middle of the strain gage was positioned right above the suture and the suture was shielded from glue by placing a small strip of Teflon tape underneath the strain gage. Stacked rosette strain gages (square) were bonded to the right frontal (F) and parietal (P) bones.

Fig. 2

An 11 × 8 (including edges) test grid superimposed on a double-labeled image (interfrontal suture from #302). Measurements of MAR were made at intersections of the grid with suture margins (arrows). Either vertical or horizontal lines were used depending on the alignment of the suture. In places where an intersection did not hit a double-label, the closest double-labeled area above or to the right of the test line was measured. Measurement was perpendicular to the suture surface and was from the center of the green label to the center of the red label. Calibration bar, 500 μm.

Fig. 3

Sutural strain and masseter activity during mastication. An approximate baseline (neutral) strain was assessed for each power stroke of strain channels. The power strokes are indicated by vertical broken lines. For one power stroke in each tracing, the baselines are shown as horizontal broken lines. Compared to baseline, in 3-month-old pigs (#299, A), interfrontal suture (IF) power stroke strains were compressive (arrow), while those of the interparietal suture (IP) were tensile (arrowhead); in 7-month-old pigs (#307, B), the interparietal suture strain was still tensile (arrowhead) but the interfrontal suture demonstrated a tensile peak (arrowhead) followed by a smaller compression at each power stroke. Chewing side was identified by late activity in the ipsilateral masseter and/or contralateral temporalis compared to the contralateral masseter and ipsilateral temporalis. RMa, right masseter; LMa, left masseter; R: right chew; L, left chew. Scale bar, 200 microstrain.

Fig. 4

Suture internal morphology. For each coronal section, the ectocranial surface is toward the top. A) Interfrontal and B) interparietal suture from 3-month-old pig #298. The former was interdigitated while the latter was relatively butt-ended. C) Interfrontal and D) interparietal suture from 7-month-old pig #321. The interparietal suture was butt-ended throughout the entire suture, whereas the interfrontal suture remained interdigitated endocranially but became butt-ended ectocranially. E) Interparietal suture of 7-month-old pig #304 shows that fusion was ectocranial. The endocranial section remained patent. To scale: calibration bar, 1000 μm.

Fig. 5

Mineralization at suture margins and suture width. A) Interfrontal and B) interparietal suture of a 3-month-old pig (#297); C) interfrontal and D) interparietal suture of a 7-month-old pig (#306). Suture mineral apposition rate (MAR) was greater in younger animals. E) Ectocranial and F) endocranial regions of the unfused interparietal suture of a 7-month-old pig (#322). The average width was greater on the ectocranial side. Arrows in (A) indicate high growth rate at the tips of interdigitations. For clarity, the suture space in (A), (D) and (F) are marked by broken lines. To scale: calibration bar, 500 μm.

Fig. 6

Mineralization at the ectocranial surfaces. A) Frontal and B) parietal bone of a 3-month-old pig (#299); C) frontal and D) parietal bone of a 7-month-old pig (#321). In the younger animals, frontal bone apposition was laminar and parallel to the bone surface, whereas parietal apposition was plexiform. In the older animals both bones showed plexiform apposition. The older pigs grew faster than the younger pigs and the parietal bone grew faster than the frontal bone of the same age. To scale: calibration bar, 500 μm.