significance of differences in patency among cranial sutures · patency or obliteration of sutures...
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600 • JAOA • Vol 106 • No 10 • October 2006 Sabini and Elkowitz • Original Contribution
Objective: To evaluate the gross external characteristics ofthe coronal, lambdoid, and sagittal sutures in human cadaverskulls and determine if a difference exists in terms of patency,sex, and age.
Methods: The coronal, lambdoid, and sagittal sutures weredescribed using a modified grading scale to quantify suturalpatency. An open suture was graded as 0, a fused suture as1, and an obliterated suture as 2, 3, or 4, depending on theextent of obliteration.
Results: Thirty-six skulls were examined, including 17 femaleand 19 male (age range, 56–101 y). When compared with thesagittal suture, the lambdoid suture was significantly morelikely to be patent and least likely to be obliterated. No sig-nificant difference in suture grades was found between femaleand male skulls, and no significant difference was foundbetween age and suture grade.
Conclusion: The prolonged patency of the lambdoid suturemay be due to external forces, such as the greater number ofmuscles affecting the lambdoid suture when compared withthe sagittal suture. J Am Osteopath Assoc. 2006;106:600-604
In young humans, cranial sutures are simple and straight.1As humans age, their cranial sutures undergo increasingly
elaborate changes,1–3 becoming more complex and devel-oping interdigitations1–6 through a process of growth andresorption of bone.2,4 Although forensic science correlatesobliteration of sutures with age, the morphologic character-istics of sutures are highly variable, making age estimation dif-ficult to determine.3,7–13 However, if suture obliteration isused in conjunction with other skeletal age indicators,14 theaccuracy of age estimation increases.15
Because the human body is highly adaptive, and many dif-ferences exist among sutures,3,7,9 it would be unreasonable toassume that age is the only factor that contributes to thechanges in sutures. Such notions would explain suture mor-phology solely in terms of intrinsic factors,16 such as genetics.Although intrinsic factors may be an influence, extrinsic orenvironmental factors such as tensile forces, a growing brain,and active muscle demands, are more likely to affect the char-acteristics of sutures.1,5,6,9–11,17–20
The effects of extrinsic factors on the morphologic changesin sutures is evident.1–3,6,7,9,11,17–20 These changes include anincrease in complexity, the number and length of bony inter-digitations, and a prolongation of the time to complete sutureobliteration.1–3,6,7,9,11,17,19 Interdigitations are important in thetransmission of forces from one cranial bone to another, becausethey serve to increase the surface area, thereby displacinglarger forces.1,2 It can be inferred that the more complex theinterdigitations or the longer a suture remains patent, thegreater the force on that particular suture. Conversely, oblit-eration of a suture is possibly the result of lack of motion orgrowth.3,7,9
In the absence of obliteration, mechanical stress appliedto the rat skull can stimulate activity at the suture to accom-modate the forces.20 Studies have demonstrated such adapt-ability of the cranial sutures. Moss17 found that when suturesof rats were transplanted to different suture locations, thestructure conformed to meet the demands of the new loca-tion.17 In addition, Washburn18 showed that when the temporalmuscle was removed in rats, growth at that location decreased,and the sutures became simpler. These findings seem to indi-cate that increased stress can modify a basic suture into a com-plex suture.
With the understanding that external factors, such asmuscle activity, may contribute to the maintenance of suturalpatency, this study sought to determine if a difference inpatency and obliteration of the ectocranial coronal, lambdoid,and sagittal sutures exists. Determining the presence of mor-phologic differences among these sutures can provide addi-tional understanding of cranial sutures.
MethodsHuman cadaver skulls were obtained from the department ofanatomy of the New York College of Osteopathic Medicine ofNew York Institute of Technology in Old Westbury.
Significance of Differences in Patency Among Cranial Sutures
Rosanna C. Sabini, DODavid E. Elkowitz, DO
From the Departments of Osteopathic Manipulative Medicine (Dr Sabini)and Pathology (Dr Elkowitz) at the New York College of Osteopathic Medicineof New York Institute of Technology in Old Westbury.
E-mail: [email protected]
Submitted March 3, 2005; final revision received August 1, 2005; acceptedAugust 4, 2005.
ORIGINAL CONTRIBUTION
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difference between the grading of sutures by location (�22,P=.028). To further delineate the difference between the coronal,lambdoid, and sagittal sutures, three pairwise comparisonswere performed on the same data, using a Bonferroni adjust-ment. The significance of the pairwise comparisons was testedat the .0167 level (.05/3) to control for a Type I error at an � levelof .05. The pairwise comparison was performed using aWilcoxon signed rank test (Table 2).
A statistically significant difference was found in theaverage grade of lambdoid sutures when compared with
Preparation of the skulls involved removing all tissue,including the periosteum, from the surface of the bone toexamine the sutures. A pathologist (D.E.E.) conducted a grossevaluation of the ectocranial coronal, lambdoid, and sagittalsutures (Figure 1), and classified them into five categories,according to the extent of sutural patency, using a modifiedgrading scale8:
� Grade 0 – open, not fused� Grade 1 – fused but not obliterated� Grade 2 – less than 50% obliterated � Grade 3 – more than 50% obliterated� Grade 4 – 100% obliterated
Because of the degree of latitude within each grade, non-parametric statistics were used to analyze the data. Analysesincluded a Spearman rank correlation coefficient, the Friedmantest, the Wilcoxon signed rank test in a pairwise comparison,and an analysis of variance. Significance was established at an� level of .05.
ResultsThirty-six human cadaver skulls, 17 female and 19 male, werestudied. The skulls ranged in age from 56 to 101 years, with amean�SD age of 82�11 years. Information regarding racewas not provided in the death certificate. Characteristics suchas body build, skull size, or previous lifestyle were not evalu-ated in this study.
The observed frequencies of the coronal, lambdoid, andsagittal sutures by grade are shown in Figure 2. No suturewas “open,” or graded as 0 (Figure 3).
The Spearman rank correlation coefficient (�) (Table 1)showed that all of the suture grades were correlated with loca-tion. Because of this finding, the Friedman test, which allowsfor ordinal data, was used to confirm a statistically significant
Sabini and Elkowitz • Original Contribution
ORIGINAL CONTRIBUTION
Figure 1. Model of skull showing cranial sutures.
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Suture Grade
Suture Grade
Suture Grade
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kulls
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Figure 2. Grade frequencies of coronal (A), lambdoid (B), and sagittal(C) sutures. Grading scale: 1=fused but not obliterated; 2=less than 50%obliterated; 3=greater than 50% obliterated; 4=100% obliterated.
Coronal
Sagittal
Lambdoid
Editor’s message: In the original print publication, there were twospelling errors in Figure 1: Sagital and Lamboid. The errors havebeen corrected here.
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sagittal sutures (P=.007). No statistically significant differencewas found in the average grade of the lambdoid sutures whencompared with coronal sutures (P=.044) or when comparingcoronal and sagittal sutures (P=.499). No statistically significantdifference was found in suture location between female andmale skulls (coronal, P=.059; sagittal, P=.034; and lambdoid,P=.946) (Table 3).
In establishing the significance of age in the grading of theectocranial sutures, an analysis of variance was used, withthe grade of the suture as the independent variable and age asthe dependant variable. Table 4 shows the results for the coronal(P=.201), sagittal (P=.473), and lambdoid (P=.442) sutures. Nosignificant difference was found in age by grade at any of thesuture locations.
CommentThe results show that the lambdoid suture was significantlymore likely to be patent and least likely to be obliterated when
Sabini and Elkowitz • Original Contribution
ORIGINAL CONTRIBUTION
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=morethan 50% obliterated (C); 4=100% obliterated (D).
compared with the sagittal suture. Bolk21 found a delay inthe obliteration of the lambdoid suture in a study populationof 1820 skulls, primarily ranging in age from 3 to 11 years, witha small percentage (58 [3.2%]) of skulls aged 13 to 20 years. Thefrequency of suture obliteration was 0.65% for the coronal,0.27% for the lambdoid, and 3.9% for the sagittal suture.21
Patency or obliteration of sutures can be attributed tothe presence or lack of physical force on the bones of the skull,respectively.1,5,6,9–11,17,18 The stress exhibited by muscle ten-sion is one of several external factors that is believed to imposechanges on the sutures.1,6,7,9–11,17,18 Hence, the muscles andligaments that attach to the occipital bone and confer mobilityto the cervical spine can contribute to the lambdoid suturebeing under more stress and, therefore, more patent than thesagittal suture. This concept is also known as myofascial con-tinuity, where origins of muscles that begin in one location andcross joints to reach different and distant regions for attachmentcan exert their actions onto those areas.22
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Significantly more muscles affect the occipital than theparietal bones. The occipital bone is affected by forces from theobliquus capitis superior, rectus capitis posterior major andminor, rectus capitis anterior and lateralis, semispinalis capitis,splenius capitis, longissimus capitis, occipitalis, and sternoclei-domastoid.23 The ligamentum nuchae can also be a source offorce on the occiput because it inserts on the external occipitalprotuberance and attaches to the tip of vertebra prominens. Inaddition, it also forms aponeurotic attachments to the trapezius(attaching as far as the T12 vertebra), rhomboideus minor, sple-nius capitis, and serratus posterior.23
The theory that external forces maintain suture patencyand complexity can be supported by the morphologic charac-teristics of facial sutures, which are more serrated and inter-digitated than cranial sutures and remain patent for longerperiods of time.1–4 This difference can be presumed to correlate
with facial muscles necessary for speaking,mastication, and facial expression.
Relative to the lambdoid suture, thesagittal suture is affected by far fewer asso-ciated muscular attachments: temporalisand occipitalis muscles. The smaller amountof force imposed on the sagittal suture mayexplain its tendency to be more obliteratedthan at the lambdoid suture. Also, thestresses imposed on the sagittal suture maybe displaced and transmitted to the coronaland lambdoid sutures, thereby maintainingor prolonging their patency. When estab-lishing a difference between the coronal andlambdoid sutures, a greater number ofcadaver skulls needs to be examined.
Although the current study only eval-uated the ectocranial sutures, the questionremains whether the patency or oblitera-tion found at the ectocranial surface is foundthrough the depth of the suture. We did not
evaluate the endocranial sutures nor was microscopic visual-ization performed—additional studies that could have fur-ther elucidated the findings. In addition, the cadavers hadbeen embalmed in a formalin solution. The possibility thatthe embalming process affected the sutures was considered;however, any morphologic change in the sutures secondary tothe formalin would most likely be appreciated at a micro-scopic level.
The prolonged patency of the lambdoid suture may haveclinical significance in the field of osteopathic medicine.Myofascial continuity demonstrates that muscles exert forcesin different areas of the body, reaffirming the osteopathic con-cept that the body is a unit. Therefore, muscle dysfunctions ofthe cervical and thoracic spine that attach to the occiput, canincrease strain to that region, making it vital to examine andtreat joints and muscles that are interrelated.
Sabini and Elkowitz • Original Contribution
ORIGINAL CONTRIBUTION
Table 1Correlation of Suture Grades With Suture Locations (N=36)
Location
Suture Coronal Lambdoid Sagittal
� Coronal▫ R 1.00 0.38 0.58▫ P … .02 0� Lambdoid ▫ R 0.38 1.00 0.53▫ P .021 … .001� Sagittal▫ R 0.58 0.53 1.00▫ P 0 .001 …
Table 2Pairwise Comparison of Suture Sites (N=36)
Pairwise
Sutures n Mean Sum Test* P
� Lambdoid-sagittal▫ Negative ranks 15 10.53 158.00 … .007▫ Positive ranks 4 8.00 32.00 �2.70▫ Ties 17� Lambdoid-coronal▫ Negative ranks 13 10.92 142.00 … .044▫ Positive ranks 6 8.00 48.00 �0.01▫ Ties 17� Saggital-coronal▫ Negative ranks 5 7.30 36.50 �.676 .499▫ Positive ranks 8 6.81 54.50 …▫ Ties 23
* Wilcoxon signed rank test (significance level with Bonferroni adjustment).
Table 3Relationship Between Suture Grade and Sex (N=36*)
Suture Mean Sum U† P
� Coronal▫ Female 21.74 369.50▫ Male 15.61 296.50 106.50 .059� Lambdoid▫ Female 18.62 316.50▫ Male 18.39 349.50 159.50 .946� Sagittal▫ Female 20.15 342.50▫ Male 17.03 323.50 133.50 .340
* Female (n=17); male (n=19).† Mann-Whitney U test.
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In addition, the presence of strains in the region of theoccipital bone and subocciput are vital in diagnosis and treat-ment because of their relationship to the autonomic nervoussystem. For instance, once the vagus nerve exits the skullthrough the jugular foramen, dysfunction at the point whereit courses through the head (jugular foramen compression),neck (occipitoatlantal and atlantoaxial dysfunctions), andthorax can affect autonomic function.24 Therefore, the findingthat the lambdoid suture is the most patent suture in cadaverskulls may support its role in the maintenance of motion andproper autonomic function. How certain forces and stresses,whether internal or external, act on the sutures and how theresultant suture structure may correlate with the structureand function of individuals requires further investigation.
AcknowledgmentsThe authors thank Nikos Solounias, PhD, Chairman, AnatomyDepartment, New York College of Osteopathic Medicine of NewYork Institute of Technology (NYCOM/NYIT), for his support;and Howard S. Teitelbaum, DO, PhD, MPH, Associate Dean,NYCOM/NYIT, for the statistical analyses.
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Sabini and Elkowitz • Original Contribution
ORIGINAL CONTRIBUTION
Table 4Relationship 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