Significance of Differences in Patency Among Cranial Sutures ORIGINAL

ORIGINAL CONTRIBUTION

Significance of Differences in Patency Among Cranial Sutures

Rosanna C. Sabini, DO David E. Elkowitz, DO

Objective: To evaluate the gross external characteristics of Because the human body is highly adaptive, and many dif- the coronal, lambdoid, and sagittal sutures in human cadaver ferences exist among sutures,3,7,9 it would be unreasonable to skulls and determine if a difference exists in terms of patency, assume that age is the only factor that contributes to the sex, and age. changes in sutures. Such notions would explain suture morphology solely in terms of intrinsic factors,16 such as genetics. Methods: The coronal, lambdoid, and sagittal sutures were Although intrinsic factors may be an influence, extrinsic or described using a modified grading scale to quantify sutural environmental factors such as tensile forces, a growing brain, patency. An open suture was graded as 0, a fused suture as and active muscle demands, are more likely to affect the char- 1, and an obliterated suture as 2, 3, or 4, depending on the acteristics of sutures.1,5,6,9–11,17–20 extent of obliteration. The effects of extrinsic factors on the morphologic changes Results: Thirty-six skulls were examined, including 17 female in sutures is evident.1–3,6,7,9,11,17–20 These changes include an and 19 male (age range, 56–101 y). When compared with the increase in complexity, the number and length of bony inter- sagittal suture, the lambdoid suture was significantly more digitations, and a prolongation of the time to complete suture likely to be patent and least likely to be obliterated. No sig- obliteration.1–3,6,7,9,11,17,19 Interdigitations are important in the nificant difference in suture grades was found between female transmission of forces from one cranial bone to another, because and male skulls, and no significant difference was found they serve to increase the surface area, thereby displacing between age and suture grade. larger forces.1,2 It can be inferred that the more complex the interdigitations or the longer a suture remains patent, the Conclusion: The prolonged patency of the lambdoid suture greater the force on that particular suture. Conversely, oblit- may be due to external forces, such as the greater number of eration of a suture is possibly the result of lack of motion or muscles affecting the lambdoid suture when compared with growth.3,7,9 the sagittal suture. In the absence of obliteration, mechanical stress applied J Am Osteopath Assoc. 2006;106:600-604 to the rat skull can stimulate activity at the suture to accom- modate the forces.20 Studies have demonstrated such adapt- n young humans, cranial sutures are simple and straight.1 ability of the cranial sutures. Moss17 found that when sutures IAs humans age, their cranial sutures undergo increasingly of rats were transplanted to different suture locations, the elaborate changes,1–3 becoming more complex and devel- structure conformed to meet the demands of the new loca- oping interdigitations1–6 through a process of growth and tion.17 In addition, Washburn18 showed that when the temporal resorption of bone.2,4 Although forensic science correlates muscle was removed in rats, growth at that location decreased, obliteration of sutures with age, the morphologic character- and the sutures became simpler. These findings seem to indi- istics of sutures are highly variable, making age estimation dif- cate that increased stress can modify a basic suture into a com- ficult to determine.3,7–13 However, if suture obliteration is plex suture. used in conjunction with other skeletal age indicators,14 the With the understanding that external factors, such as accuracy of age estimation increases.15 muscle activity, may contribute to the maintenance of sutural patency, this study sought to determine if a difference in patency and obliteration of the ectocranial coronal, lambdoid, and sagittal sutures exists. Determining the presence of morphologic differences among these sutures can provide additional understanding of cranial sutures. From the Departments of Osteopathic Manipulative Medicine (Dr Sabini) and Pathology (Dr Elkowitz) at the New York College of Osteopathic Medicine of New York Institute of Technology in Old Westbury. Methods E-mail: [email protected] Human cadaver skulls were obtained from the department of Submitted March 3, 2005; final revision received August 1, 2005; accepted anatomy of the New York College of Osteopathic Medicine of August 4, 2005. New York Institute of Technology in Old Westbury.

600 • JAOA • Vol 106 • No 10 • October 2006 Sabini and Elkowitz • Original Contribution Editor’s message: In the original print publication, there were two spelling errors in Figure 1: Sagital and Lamboid. The errors have ORIGINAL CONTRIBUTION been corrected here.

A 20

15 Coronal

10 Sagittal No. of Skulls 5

Lambdoid 0 1 2 3 4 Suture Grade

20 B

Figure 1. Model of skull showing cranial sutures. 15

10 Preparation of the skulls involved removing all tissue, No. of Skulls including the periosteum, from the surface of the bone to 5 examine the sutures. A pathologist (D.E.E.) conducted a gross evaluation of the ectocranial coronal, lambdoid, and sagittal 0 sutures (Figure 1), and classified them into five categories, 1 2 3 4 according to the extent of sutural patency, using a modified Suture Grade grading scale8: 20 C Grade 0 – open, not fused Grade 1 – fused but not obliterated 15 Grade 2 – less than 50% obliterated Grade 3 – more than 50% obliterated 10 Grade 4 – 100% obliterated No. of Skulls Because of the degree of latitude within each grade, non- 5 parametric statistics were used to analyze the data. Analyses included a Spearman rank correlation coefficient, the Friedman 0 1 2 3 4 test, the Wilcoxon signed rank test in a pairwise comparison, Suture Grade and an analysis of variance. Significance was established at an ␣ level of .05. Figure 2. Grade frequencies of coronal (A), lambdoid (B), and sagittal Results (C) sutures. Grading scale: 1=fused but not obliterated; 2=less than 50% Thirty-six human cadaver skulls, 17 female and 19 male, were obliterated; 3=greater than 50% obliterated; 4=100% obliterated. studied. The skulls ranged in age from 56 to 101 years, with a meanϮSD age of 82Ϯ11 years. Information regarding race ␹2 was not provided in the death certificate. Characteristics such difference between the grading of sutures by location ( 2, as body build, skull size, or previous lifestyle were not evalu- P=.028). To further delineate the difference between the coronal, ated in this study. lambdoid, and sagittal sutures, three pairwise comparisons The observed frequencies of the coronal, lambdoid, and were performed on the same data, using a Bonferroni adjust- sagittal sutures by grade are shown in Figure 2. No suture ment. The significance of the pairwise comparisons was tested was “open,” or graded as 0 (Figure 3). at the .0167 level (.05/3) to control for a Type I error at an ␣ level The Spearman rank correlation coefficient (␳) (Table 1) of .05. The pairwise comparison was performed using a showed that all of the suture grades were correlated with loca- Wilcoxon signed rank test (Table 2). tion. Because of this finding, the Friedman test, which allows A statistically significant difference was found in the for ordinal data, was used to confirm a statistically significant average grade of lambdoid sutures when compared with

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A B

C D

Figure 3. Gross image of cadaver skulls showing suture grade: 1=fused but not obliterated (A); 2=less than 50% obliterated (B); 3=more than 50% obliterated (C); 4=100% obliterated (D).

sagittal sutures (P=.007). No statistically significant difference compared with the sagittal suture. Bolk21 found a delay in was found in the average grade of the lambdoid sutures when the obliteration of the lambdoid suture in a study population compared with coronal sutures (P=.044) or when comparing of 1820 skulls, primarily ranging in age from 3 to 11 years, with coronal and sagittal sutures (P=.499). No statistically significant a small percentage (58 [3.2%]) of skulls aged 13 to 20 years. The difference was found in suture location between female and frequency of suture obliteration was 0.65% for the coronal, male skulls (coronal, P=.059; sagittal, P=.034; and lambdoid, 0.27% for the lambdoid, and 3.9% for the sagittal suture.21 P=.946) (Table 3). Patency or obliteration of sutures can be attributed to In establishing the significance of age in the grading of the the presence or lack of physical force on the bones of the skull, ectocranial sutures, an analysis of variance was used, with respectively.1,5,6,9–11,17,18 The stress exhibited by muscle ten- the grade of the suture as the independent variable and age as sion is one of several external factors that is believed to impose the dependant variable. Table 4 shows the results for the coronal changes on the sutures.1,6,7,9–11,17,18 Hence, the muscles and (P=.201), sagittal (P=.473), and lambdoid (P=.442) sutures. No ligaments that attach to the occipital bone and confer mobility significant difference was found in age by grade at any of the to the cervical spine can contribute to the lambdoid suture suture locations. being under more stress and, therefore, more patent than the sagittal suture. This concept is also known as myofascial con- Comment tinuity, where origins of muscles that begin in one location and The results show that the lambdoid suture was significantly cross joints to reach different and distant regions for attachment more likely to be patent and least likely to be obliterated when can exert their actions onto those areas.22

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Significantly more muscles affect the occipital than the Table 1 parietal bones. The occipital bone is affected by forces from the Correlation of Suture Grades With Suture Locations (N=36) obliquus capitis superior, rectus capitis posterior major and minor, rectus capitis anterior and lateralis, semispinalis capitis, Location splenius capitis, longissimus capitis, occipitalis, and sternoclei- Suture Coronal Lambdoid Sagittal domastoid.23 The ligamentum nuchae can also be a source of force on the occiput because it inserts on the external occipital Coronal protuberance and attaches to the tip of vertebra prominens. In ▫ R 1.00 0.38 0.58 addition, it also forms aponeurotic attachments to the trapezius ▫ P … .02 0 (attaching as far as the T12 vertebra), rhomboideus minor, sple- Lambdoid 23 ▫ R 0.38 1.00 0.53 nius capitis, and serratus posterior. ▫ P .021 … .001 The theory that external forces maintain suture patency Sagittal and complexity can be supported by the morphologic charac- ▫ R 0.58 0.53 1.00 teristics of facial sutures, which are more serrated and inter- ▫ P 0 .001 … digitated than cranial sutures and remain patent for longer periods of time.1–4 This difference can be presumed to correlate with facial muscles necessary for speaking, mastication, and facial expression. Table 2 Relative to the lambdoid suture, the Pairwise Comparison of Suture Sites (N=36) sagittal suture is affected by far fewer asso- ciated muscular attachments: temporalis Pairwise and occipitalis muscles. The smaller amount Sutures n Mean Sum Test* P of force imposed on the sagittal suture may explain its tendency to be more obliterated Lambdoid-sagittal ▫ Negative ranks 15 10.53 158.00 … .007 than at the lambdoid suture. Also, the ▫ Positive ranks 4 8.00 32.00 Ϫ2.70 stresses imposed on the sagittal suture may ▫ Ties 17 be displaced and transmitted to the coronal Lambdoid-coronal and lambdoid sutures, thereby maintaining ▫ Negative ranks 13 10.92 142.00 … .044 ▫ Positive ranks 6 8.00 48.00 Ϫ0.01 or prolonging their patency. When estab- ▫ Ties 17 lishing a difference between the coronal and Saggital-coronal lambdoid sutures, a greater number of ▫ Ϫ Negative ranks 5 7.30 36.50 .676 .499 cadaver skulls needs to be examined. ▫ Positive ranks 8 6.81 54.50 … ▫ Ties 23 Although the current study only eval- uated the ectocranial sutures, the question * Wilcoxon signed rank test (significance level with Bonferroni adjustment). remains whether the patency or obliteration found at the ectocranial surface is found through the depth of the suture. We did not evaluate the endocranial sutures nor was microscopic visual- Table 3 ization performed—additional studies that could have fur- Relationship Between Suture Grade and Sex (N=36*) ther elucidated the findings. In addition, the cadavers had been embalmed in a formalin solution. The possibility that Suture Mean Sum U† P the embalming process affected the sutures was considered; Coronal however, any morphologic change in the sutures secondary to ▫ Female 21.74 369.50 the formalin would most likely be appreciated at a micro- ▫ Male 15.61 296.50 106.50 .059 scopic level. Lambdoid The prolonged patency of the lambdoid suture may have ▫ Female 18.62 316.50 ▫ Male 18.39 349.50 159.50 .946 clinical significance in the field of osteopathic medicine. Sagittal Myofascial continuity demonstrates that muscles exert forces ▫ Female 20.15 342.50 in different areas of the body, reaffirming the osteopathic con- ▫ Male 17.03 323.50 133.50 .340 cept that the body is a unit. Therefore, muscle dysfunctions of the cervical and thoracic spine that attach to the occiput, can * Female (n=17); male (n=19). † Mann-Whitney U test. increase strain to that region, making it vital to examine and treat joints and muscles that are interrelated.

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Table 4 Relationship Between Suture Grade and Age

Suture Sum df Mean F score P

Coronal 4517.556 35 ▫ Between Groups 600.378 3 200.126 1.635 .201 ▫ Within Groups 3917.178 32 122.412 Lambdoid 4517.556 35 ▫ Between Groups 359.222 3 119.741 0.921 .442 ▫ Within Groups 4158.333 32 129.948 Sagittal 4517.556 35 ▫ Between Groups 336.528 3 112.176 0.859 .473 ▫ Within Groups 4181.027 32 130.657

In addition, the presence of strains in the region of the 9. Pritchard JJ, Scott JH, Girgis FG. The structure and development of cranial occipital bone and subocciput are vital in diagnosis and treat- and facial sutures. J Anat. 1956;90:73–86. ment because of their relationship to the autonomic nervous 10. Persson M, Thilander B. Palatal suture closure in man from 15 to 35 years of age. Am J Orthod. 1977;72:42–52. system. For instance, once the vagus nerve exits the skull 11. Smith HG, McKeown M. Experimental alteration of the coronal sutural through the jugular foramen, dysfunction at the point where area: a histological and quantitative microscopic assessment. J Anat. it courses through the head (jugular foramen compression), 1974;118:543–559. neck (occipitoatlantal and atlantoaxial dysfunctions), and 12. Ashley-Montagu MF. Aging of the skull. Am J Phys Anthropol. thorax can affect autonomic function.24 Therefore, the finding 1938;23:355–375. that the lambdoid suture is the most patent suture in cadaver 13. Hershkovitz I, Latimer B, Dutour O, Jellema LM, Wish-Baratz S, Roth- skulls may support its role in the maintenance of motion and schild C, et al. Why do we fail in aging the skull from the sagittal suture? Am J Phys Anthropol. 1997;103:393–399. proper autonomic function. How certain forces and stresses, 14. Meindl RS, Lovejoy CO. Ectocranial suture closure: a revised method for whether internal or external, act on the sutures and how the the determination of skeletal age at death based on the lateral-anterior resultant suture structure may correlate with the structure sutures. Am J Phys Anthropol. 1985;68:57–66. and function of individuals requires further investigation. 15. Lovejoy CO, Meindl RS, Mensforth RP, Barton TJ. Multifactorial determination of skeletal age at death: a method and blind tests of its accuracy. Acknowledgments Am J Phys Anthropol. 1985;68:1–14. The authors thank Nikos Solounias, PhD, Chairman, Anatomy 16. Markens IS, Oudhof HAJ. Morphological changes in the coronal suture after replantation. Acta Anat (Basel). 1980;107:289–296. Department, New York College of Osteopathic Medicine of New York Institute of Technology (NYCOM/NYIT), for his support; 17. Moss ML. Experimental alteration of sutural area morphology. Anat Rec. 1957;127:569–589. and Howard S. Teitelbaum, DO, PhD, MPH, Associate Dean, NYCOM/NYIT, for the statistical analyses. 18. Washburn SL. The relation of the temporal muscle to the form of the skull. Anat Rec. 1947;99:239–248. References 19. Hinton DR, Becker LE, Muakkassa KF, Hoffman HJ. Lambdoid synostosis. Part 1. The lambdoid suture: normal development and pathology of “syn- 1. Saito K, Shimizu Y, Ooya K. Age-related morphological changes in squa- ostosis.” J Neurosurg. 1984;61:333–339. mous and parietomastoid sutures of human cranium. Cells Tissues Organs. 2002;170:266–273. 20. Burstone CJ, Shafer WG. Sutural expansion by controlled mechanical stress in the rat. J Dent Res. 1959;38:534–540. 2. Herring SW. Sutures—a tool in functional cranial analysis. Acta Anat (Basel). 1972;83:222–247. 21. Bolk L. On the premature obliteration of sutures in the human skull. Am J Anat. 1915;17:495–523. 3. Wagemans PA, van de Velde JP, Kuijpers-Jagtman AM. Sutures and forces: a review. Am J Orthod Dentofacial Orthop. 1988;94:129–141. 22. Jacobs AW, Falls WM. Anatomy. In: Ward RC, ed. Foundations for Osteo- pathic Medicine. 2nd ed. Baltimore, Md: Lippincott Williams & Wilkins; 4. Cohen MM Jr. Sutural biology and the correlates of craniosynostosis 2003:44–62. [review]. Am J Med Genet. 1993;47:581–616. 23. Dean NA, Mitchell BS. Anatomic relation between the nuchal ligament 5. Opperman LA. Cranial sutures as intramembranous bone growth sites (ligamentum nuchae) and the spinal dura mater in the craniocervical region. [review]. Dev Dyn. 2000;219:472–485. Clin Anat. 2002;15:182–185. 6. Kokich VG. Age changes in the human frontozygomatic suture from 20 to 24. Kappler RE, Ramey KA. Head: diagnosis and treatment. In: Ward RC, 95 years. Am J Orthod. 1976;69:411–430. ed. Foundations for Osteopathic Medicine. Baltimore, Md: Lippincott Williams 7. Persson M. Closure of facial sutures: a preliminary report. Trans Euro & Wilkins; 2003:660–683. Orthod Soc 52nd Congress. 1976;249–253. 8. Singer R. Estimation of age from cranial suture closure: a report on its unre- liability. J Forensic Med. 1953;1:52–59.

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