The prevalence of accessory sutures and wormian
bones in a contemporary cohort of Dutch
children.
Gisela de Heus, 11414901
MSc in Forensic Science, University of Amsterdam Supervisors:
Prof. Dr. R.R. van Rijn Amsterdam University Medical Centres UMC, Department of Radiology
K.L. Colman Amsterdam University Medical Centres UMC, Department of Anatomy, Embryology and Physiology
H.H. de Boer Amsterdam University Medical Centres UMC, Department of Pathology, NFI Department of Medical Forensic Research Examiner:
Prof. Dr. R.J. Oostra Amsterdam University Medical Centres UMC, Department of Medical Biology
36 European Credits April 2018 – October 2018 Date of submission: 19-10-2018
Page 2 of 34 Abstract
Child abuse is a widely prevalent problem in the Western world. It is estimated that 118.000 to 180.000 children are abused in the Netherlands annually, of which physical abuse constitutes almost 18% of all abusive cases, with Abusive Head Trauma (AHT) being categorised as a severe form. In child abuse cases, skull fractures are a strong indication of AHT. However, the presence of accessory sutures and Wormian bones, sometimes lead to erroneous conclusions. This is because accessory sutures sometimes present similar morphologically characteristics on radiographs as fractures. Knowledge on the prevalence of accessory sutures and Wormian bones would help in preventing erroneous conclusions, however all current knowledge is based on dry skull collections mostly on adult skulls. Accessory sutures may not persist into adulthood together with the fact that modern population experienced secular changes makes these collections not representative for the modern Dutch children population. The aim of this study was to determine the prevalence of accessory sutures and Wormian bones in a contemporary cohort of Dutch children below the age of 6.
For this research, 532 cranial CT scans of children below the age of 6 were selected from a PACS system (AGFA Impax 6.6.1. 4024, Agfa Healthcare, Mortsel, Belgium. Volume Rendering Technique (VRT) of the program Syngo.via was used to create 3D reconstructions of the CT scans. The scans were retrospectively reviewed by two observers, one of which an experienced paediatric radiologist. The presence of various accessory sutures and Wormian bones were scored and evaluated using 3D reconstructions of CT scans. The mean age of the cases was 28.47 months (range 0.033 to 72 months) for males and 22.57 (rang 0.066-72 months) for females.
The results from this study showed that accessory sutures were present in 34.3% of the cases. Of these accessory sutures, the metopic and mendosal suture were seen most frequently with 29.9% and 23.9% respectively. Other accessory sutures that were found including the intraparietal horizontal suture, intraparietal vertical suture, obelion suture and an occipital unossified midline were seen less frequently with 7.2%, 3.8%, 2.2% and 0.9% respectively. None of the accessory sutures showed sexual preference. Most accessory sutures were found in the lower age groups and particularly the prevalence of the metopic and mendosal suture showed a decrease with age. Wormian bones were found in 78% of the cases, with the most frequent location being the lambdoid suture with 64.2%. Only the parietal notch showed a significant difference between female and male (p=0.024).
Knowledge about the existence, prevalence and topographical location of various accessory sutures and wormian bones will aid in the ability to make correct diagnosis and thereby increase the evidential value of the diagnosis in cases of abuse. However, because of several limitations of this study the results have to be interpreted and used with care.
Keywords: Accessory cranial sutures, Skull fractures, Child abuse, Wormian bones, 3D CT reconstruction
Table of Contents
Abstract ... 2
1. Introduction ... 4
1.1 Normal development of the skull ... 4
1.2 Accessory sutures ... 5
1.3 Wormian bones ... 6
1.4 Aim of the study ... 7
2. Methods ... 8 2.1 Study population ... 8 2.2 Data collection ... 8 2.3 Data analysis ... 9 2.4 Ethical aspects ... 9 3. Results ... 10
3.1 Intra- and inter-observer variability ... 10
3.2 Prevalence ... 10
3.2.1 Metopic suture ... 10
3.2.2 Intraparietal horizontal suture ... 11
3.2.3 Intraparietal vertical suture ... 12
3.2.4 Obelion suture ... 13
3.2.5 Occipital unossified midline membrane ... 13
3.2.6 Mendosal suture ... 14
3.2.7 Wormian bones ... 14
3.2.8 Craniosynostosis ... 17
4. Discussion ... 18
4.1 Intra- and inter- variability ... 18
4.2 Accessory sutures ... 18 4.3 Wormian bones ... 19 4.4 Craniosynostosis ... 20 4.5 Limitations... 20 4.6 Practical implications ... 21 4.7 Future research ... 21 5. Conclusion ... 23 Acknowledgements ... 24 References ... 25 Appendix A Glossary ... 28
Appendix B Case Report Form (CRF) ... 29
Appendix C Reference figures Case Report Form ... 33
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Figure 1 Sutures in the normal newborn skull
all sutures present in a normal skull. Modified from Sobotta, J. (19097.
1. Introduction
Child abuse is a worldwide problem and the prevalence in the Netherlands is approximately between 118.000 and 180.000 cases a year 1–3. However, abuse is often not detected because of lack of symptoms or is not reported by the physician. Therefore the actual prevalence is expected to be even higher1. Physical abuse constitutes almost 18% of all abusive cases of which Abusive Head Trauma (AHT) is a severe form often characterized by cranial fractures 2–4. However, a common finding which sometimes leads to erroneous conclusions during radiological examinations are accessory sutures and wormian bones. This is because accessory sutures sometimes present similar morphologically characteristics on radiographs as fractures. Accessory sutures are suture or remnants thereof that exist besides the normal sutures and Wormian bones are small extra bones occurring in the normal sutures or fontanelles of the skulls from children. Misdiagnosis of a fracture being an accessory suture or Wormian bone can lead to prolonged exposure to child abuse which can have short term effects on the child as well as long term effects including developing emotional, cognitive and physical conditions. On the other hand when an accessory suture or Wormian bones is seen as a fracture the family can be wrongfully accused of child abuse, which can be stressful for the family and can lead to legal issues.
1.1 Normal development of the skull
In order to understand why these accessory sutures and wormian bones are present in some children it is important to address the normal development of the skull. The bone formation of the skull starts approximately at the 8th fetal week by a process called ossification which starts from so called ossification centres5,6. Initially there are over 110 of these ossification centers responsible for the formation of 45 fetal skull bones5. Fusion of some of these ossification centers results in the 22 bones which make up the adult skull5. The large normal sutures which separate the skull bones in adulthood include are the coronal, saggital, lambdoid and squamosal sutures (Figure 1)7.
1.2 Accessory sutures
Accessory sutures are sutures which occur besides the normal cranial sutures. They are believed to arise from incomplete fusion of different ossification centres and they occur in some children and may persist into adulthood but not necessarily8. Accessory sutures are most commonly found in the frontal, parietal and occipital bones. These bones originate from multiple ossification centers and lack of fusion between these ossification centres can result in accessory sutures5. Table 1 lists several accessory sutures which are described in the literature with the mendosal and metopic sutures described most often.
Table 1 Some known accessory sutures and their location
Location Frontal bone Occipital bone Parietal bone Accessory
sutures
Metopic suture9 Normal persistent
occipital fissure16,17
Horizontal intraparietal suture11–15
Mendosal suture20,21 Vertical intraparietal
suturen15,18,19 Midline unossified membranous strip in interparietal segment (ip)22 Oblique intraparietal suture15
The metopic suture is located in the frontal bone. The frontal bone develops from two ossification centers creating two separate bones that normally fuse after birth by the 7th year of life. However, when these bones don’t fuse a persistent metopic suture can be present even into adulthood. The parietal bones also ossify from two ossification centers which rapidly fuse and then radiate towards the periphery to form each bone. Lack of fusion of these centers can result in the presence of accessory sutures such as the intraparietal horizontal, vertical and oblique sutures. Unlike the frontal and parietal bones, the occipital bone ossifies from more than two ossification centers (figure 2)23. Because of the multiple ossification centers various accessory sutures are reported in the occipital bone when these centers don’t fuse.
Figure 2 Schematic representation of ossification centers in the upper part of the occipital bone, above the supraoccipital bone (SO). The intermediate segment are display paired centers, the lateral plate is formed by the second pair of centers (II), and the upper and the 3rd pair of centers (III) will form the medial plate. From Srivastava et al. (1992) 23.
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Accessory sutures in the cranium of children can be difficult to distinguish from fractures especially when they present with similar characteristics as fractures. Radiologically accessory sutures display characteristics which are comparable with normal sutures. They have a zigzag pattern with sclerotic borders, have no associated widening of the suture, they merge with adjacent sutures, are often bilateral and fairly symmetric and a lack soft tissue swelling15. Alternatively fractures are normally characterized by their sharp-lucent look with non-sclerotic edges15. They often widen when they approach a normal suture and sometimes they can cross a suture line. Most of the time fractures are unilateral but in cases of bilateral fractures they are often asymmetric. Lastly fractures are often associated with soft tissue swelling, but lack of soft tissue swelling is not uncommon15.
The difficulty of making a distinction between accessory sutures and fractures is indicated by several published case reports. Tharp et al. (2009), Wiedijk et al. (2016) and Eklund et al. (2016) all present cases in which the patient expired and initial radiographs or CT-scans were concluded to contain fractures. Because of suspicion for non-accidental death full forensic investigations were performed. During the autopsies histological evaluation revealed the presence of fibrous tissue without any signs of healing which indicate that they were accessory sutures rather than fractures. In the case of Tharp et al. (2009) and Wiedijk et al. (2016) a parietal accessory suture was initially diagnosed as a fracture while in the case presented by Eklund et al. (2016) an occipital accessory suture was initially seen as a fracture.
Knowledge about the prevalence and location of accessory sutures could aid in making the distinction between accessory sutures and fractures which could prevent mistakes being made like in the previously mentioned cases. However, literature about accessory sutures and prevalence numbers thereof is scarce. Most information about the existence of various accessory sutures is based on single case reports and therefore lack the information about the occurrence in the population12,15,18,19,24–29. The limited number of articles that do report prevalence numbers about some of the more common accessory sutures are based on very old data and are also mostly based on adult skulls30,31. As explained not every accessory suture will persist into adulthood and therefore prevalence numbers based on adult skull collections cannot be considered a good representation of the prevalence of accessory sutures in children. Additionally some prevalence studies are based on old skull collections which might not be as representative since the modern population has experienced secular changes11,31.
1.3 Wormian bones
Other variants of the skull which can be mistaken for fractures are Wormian bones. While accessory sutures are thought to develop from non-fusion of normal ossification centres Wormian bones are believed to arise from additional ossification centres during the development of the skull. Wormian bones are small extra bones mostly found within cranial fontanelles and sutures34,35. Wormian bones are found to be correlated to several diseases, however they also frequently occur in healthy individuals where they are normally smaller and lesser in number36. Most Wormian bones are not named because they vary in shape and size from person to person. One of the most common Wormian bones located at Lambda where the Saggital and Lambdoid sutures meet is named Inca bone. Inca bones are formed due to differential fusion of ossification centers in the occipital bone.
An example case showing the difficulty of making a distinction between wormian bones and fractures is presented by Main et al. (2018). They present the case of a 5 week-old infant that expired. Post-mortem radiographs of the skull showed a depressed, sclerotic defect of the occipital bone with bilateral linear lucencies37. Post-mortem CT head scan did not entirely exclude a fracture because some parts showed characteristics more related with fractures but overall it supported the hypothesis of it being a large wormian bone in the occipital bone more37. Histological examination during autopsy confirmed that it was consistent with normal sutures37.
The data about the topographical location and prevalence of Wormian bones is quite extent, but mostly based on adult dry skulls36,38. Data about the prevalence of Wormian bones in the general population of children is lacking which is specifically important for the differential diagnosis of child abuse39. Furthermore since the occurrence of Wormian bones are believed to be population dependent, current data about Wormian bones in the Dutch population is lacking36. The lack of, or outdated data on the prevalence of these various accessory sutures and bones impede the ability of medical and forensic specialists to make the correct diagnosis in cases of suspected child abuse.
1.4 Aim of the study
Differential diagnosis in cases of non-accidental injuries is necessary during the radiographic examinations. However, as indicated by the cases previously mentioned, misdiagnosis of fractures, accessory- sutures or bones can occur. Misdiagnosing a real fracture can have serious implications such as prolonged exposure of the child to the abusive situation. On the other hand misdiagnosing an accessory suture or Wormian bone as a fracture can have negative implications for the family being exposed to prolonged investigations and being falsely accused of abuse. Knowledge about the existence, prevalence and topographical location of various accessory sutures and Wormian bones will aid in the ability to make correct diagnosis and thereby increase the evidential value of the diagnosis in cases of abuse. Therefore the aim of this research project is to determine the prevalence and topographical location of various accessory sutures and Wormian bones in a contemporary cohort of Dutch children.
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2. Methods
2.1 Study population
Cases for this research were selected from a PACS system (AGFA Impax 6.6.1. 4024, Agfa Healthcare, Mortsel, Belgium) of the UMC Amsterdam. Table 2 lists the 8 different search terms that were used to look for CT scans of children below the age of 6. This initial search resulted in a large set consisting of 532 CT scans from a contemporary cohort, from 2008 to 2018, of Dutch children. In cases were multiple CT scans at different time points were available only the first CT scans were included to insure that every case was included only once.
Table 2 Search terms in PACS for inclusion of cases
CT Skull CT Brain.mc
CT Brain CT Trauma skull/ Cervical spine
CT Brain without contrast CT Whole body
CT Brain with contrast CT Post mortem
Volume Rendering Technique (VRT) of the program Syngo.Via (Siemens Health Engineers) was used to create a 3D reconstruction of the CT scans for every case. The initial dataset was reviewed by two observers, one of which an experienced radiologist. Subsequently all cases which contained fractures were checked by an experienced paediatric radiologist and then excluded. Other exclusion criteria included; insufficient CT data for analysis caused by slice thickness, incomplete CT scans of the skull and CT scans were movement caused overlapping parts of the skull. Also one deceased case was excluded because parts of the skull were displaced. Insufficient CT scans were determined to be all scans from 3mm or higher slice thickness as well as some scans with a slice thickness of 1mm were the sutures were not clearly visible. After exclusion of these cases the final dataset consisted of 330 CT scans. This dataset included 12 cases of craniosynostosis, early closure of sutures, of which 7 were male with an mean age of 48.57 months (age range 22 – 72 months) and 5 female with a mean age of 38.6 months (age range 3 – 60 months). This was considered as a separate subset of cases throughout the data analysis, leaving 318 cases for the representation of the normal population. Of the 318 cases included in this study 200 were male with a mean age of 28.47 months (age range 0.033 - 72.00 months) and 118 were female with a mean age of 22.57 months (age range 0.066 – 72 months).
2.2 Data collection
This is a retrospective study with completely anonymized cases of which only demographic details like the age in months and sex were known and recorded. A Case Report Form (CRF) was designed to examine the skull including; the frontal bone, parietal bones, temporal bones and occipital bone in the CT 3D reconstruction of each case (Appendix B). The presence or absence of various accessory sutures was recorded along with their characteristics including; which side of the skull (left, right, bilateral) and complete or incomplete. Furthermore, the presence of wormian bones was recorded along with their location and the shape of each wormian bone. A distinction between round, oval, triangular, quadrangular, irregular and uncharacterizable was made. The shapes of wormian bones were defined using example figures from previous studies as well as from the present study (Appendix C)40–42. In case of multiple wormian bones at one location, the wormian bones were scored from anterior to posterior and from cranial to caudal depending on the suture involved.
For the determination of intra- and inter-observer variability a subset of the dataset containing 43 cases was selected. In order to have a representative subset the data was grouped into cases containing only accessory sutures, only wormian bones, both wormian bones and accessory sutures and neither wormian bones or accessory sutures. From each of these groups a male and female from every age group were randomly selected by an objective person not involved in the examination of the CT scans. In order to prevent recognition for the intra observer variability the subset of CT scans was reviewed 3 weeks after the first round of examination. In order to store and analyse the data, a database was built in Castor Electronic Data Capture (EDC).
2.3 Data analysis
Intra- and inter-observer variability for dichotomous variables was determined using a Cohen’s Kappa. The total number of wormian bones was categorized into 6 categories 0, 1, 2, 3, 4, >5 wormian bones. A weighted Cohen’s kappa was then used to determine the intra- and inter-observer agreement for the total number of wormian bones. Consistent with previous literature a kappa value <0 was considered less than chance agreement, 0.01-0.20 was considered slight agreement, 0.21-0.40 was considered fair agreement, 0.41-0.60 moderate agreement, 0.61-0.80 substantial agreement and 0.81-0.99 almost perfect agreement (table 3)43. Prevalence analysis was mostly descriptive. To investigate the differences in prevalence between male and female the Pearson’s Chi-square test and the Fisher exact test, in case of low expected values, were used. Statistical significance was defined as a p-value <0.05. The descriptive and analytic statistical analyses were performed using IBM SPSS Statistics version 24(IBM Corp., Armonk, NY, United States).
Table 3 Strength of agreement categories from Landis and Koch43
Kappa Agreement
<0 Less than chance
agreement 0-0.20 Slight agreement 0.21-0.40 Fair agreement 0.41-0.60 Moderate agreement 0.61-0.80 Substantial agreement 0.81-0.99 Almost perfect agreement 2.4 Ethical aspects
Informed consent was not required due to the retrospective aspect of this study. Additionally all the cases were fully anonymized ensuring that approval of the parents or the Institutional Review Board (IRB) of the Amsterdam UMC was not required.
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3. Results
3.1 Intra- and inter-observer variability
To determine the reliability of the results the intra- and inter- observer variability was determined of which the results are summarized in table 4. The intra observer agreement for the presence or absence of any accessory suture was substantial (k= 0.892). The only accessory suture with substantial agreement was the mendosal suture (k=0.726) while all other individual accessory sutures including; the metopic suture, the intraparietal horizontal suture, the intraparietal vertical suture, the obelion suture and the occipital unossified midline membrane (k=1). The intra-observer agreement for the presence or absence of wormian bones was almost perfect (k=0.948). Additionally the intra-observer agreement was for the number of wormian bones was also almost perfect (k=0.955). All inter observer agreements were substantial or almost perfect. The inter-observer agreement for the presence or absence of the intraparietal horizontal suture, the intraparietal vertical suture and the occipital unossified midline membrane was perfect (k=1). The inter-observer agreement for the presence or absence of the obelion suture was almost perfect (k=0.844) while the inter-observer agreements for the presence or absence of any accessory suture, the metopic suture, the mendosal suture, any wormian bone and the total number of wormian bones were substantial (k=0.660, k=0.675, k=0.689, k=0.678 and k=0.719).
Table 4 Intra- and inter-observer variability for the presence or absence of various accessory sutures and Wormian bones
Intra-observer agreement Cohen’s kappa value
Inter-observer agreement Cohen’s Kappa value Accessory sutures present
absent 0.892 0.660 Metopic suture 1 0.675 Intraparietal horizontal suture 1 1
Intraparietal vertical suture 1 1
Obelion suture 1 0.844
Occipital unossified midline membrane
1 1
Mendosal suture 0.726 0.689
Temporal bone (other) accessory sutures
1 0.255
Wormian bones present absent
0.948 0.678
Wormian bones numbers * 0.955 0.719
*In order to determine the intra- and inter-observer variability for the total number of wormian bones per case a Weighted Cohen’s kappa was used.
The inter-observer agreement of accessory sutures in the temporal bone was fair (k=0.255). This was determined to be insufficient and therefore no further analysis was performed on accessory sutures in the temporal bone.
3.2 Prevalence
3.2.1 Metopic suture
At least one accessory suture was present in 109 cases (34.3%). Metopic sutures were found in 95 cases (29.9%). Table 5 shows the prevalence of the complete (figure 3A) and incomplete metopic suture (figure 3B) sorted by sex and age group. Most of the metopic sutures occurred in the age group < 3 months (57.29%) and the prevalence of the metopic suture decreased with age. Complete metopic sutures were more frequent than incomplete metopic sutures with 24.8% and 5.0% prevalence respectively. No statistical significance was found between males and females (p=0.351).
Table 5 Prevalence of complete and incomplete metopic sutures sorted by sex and age group
*percentages have been calculated from the whole sample in order to demonstrate the prevalence
3.2.2 Intraparietal horizontal suture
An intraparietal horizontal suture in total was found in 7 cases (2.2%). A bilateral intraparietal horizontal suture was seen in 2 cases, 3 cases showed an unilateral intraparietal horizontal suture on the left side of the skull and 2 cases on the right side of the skull (Table 6). The majority of the cases were found in the age group below 3 months (1.87%). An example of an incomplete intraparietal horizontal suture is depicted in figure 4. No significant difference was found between males and females (p=0.711).
Age groups Sex Complete
metopic suture* Incomplete metopic suture* Total percentage per age group* <3 months Male 32 (10.06%) 1 (0.31%) 17.19% Female 21 (6.60%) 1 (0.31%) 3-6 months Male 6 (1.89%) 2 (0.63%) 5.03% Female 8 (2.52%) - 6-12 months Male 3 (0.94%) 5 (1.57%) 5.03% Female 2 (0.63%) 6 (1.89%) 12-24 months Male 2 (0.63%) - 0.63% Female - - 24-36 months Male 2 (0.63%) - 0.94% Female 1 (0.31%) - 36-48 months Male - - - Female - - 48-60 months Male 1 (0.31%) 1 (0.31%) 0.63% Female - - 60-72 months Male 1 (0.31%) - 0.31% Female - -
A
B
Figure 3 Skull showing a complete metopic suture (A) and a skull showing an incomplete metopic suture (B).
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Figure 5 A case example showing the sometimes difficulties in differentiating these accessory sutures from a fractures. This was determined to be an accessory suture because of the absence of hematoma and other specific fracture characteristics. However to be certain a histological examination would be necessary. Not possible due to the fact that the patient was still alive
Table 6 Prevalence of bilateral and unilateral intraparietal horizontal sutures sorted by sex and age group Age groups Sex Bilateral intraparietal horizontal suture* Unilateral intraparietal horizontal suture left* Unilateral intraparietal horizontal suture right* Total percentage per age group* <3 months Male 1 (0.31%) 2 (0.63%) 1.87% Female 1 (0.31%) 1 (0.31%) 1 (0.31%) 6-12 months Male - 1 (0.31%) - 0.31% Female - -
*percentages have been calculated from the whole sample in order to demonstrate the prevalence
3.2.3 Intraparietal vertical suture
Only 4 cases (1.26%) of incomplete intraparietal vertical sutures were found of which 2 were males in the age group below <3 months and 1 female in the age group 6-12 months (Figure 5).
Figure 4 Skull showing an incomplete parietal horizontal suture on the left side of the skull
Figure 7 Skull showing an occipital unossified midline membrane (orange arrow)
3.2.4 Obelion suture
The obelion suture was only seen in 12 cases (4.09%) which were all in the age group <3 months (Figure 6). There were 7 males with a bilateral obelion suture and 1 with an unilateral obelion suture. In females 3 cases with a bilateral obelion suture were found and 1 case with an unilateral obelion suture. No significance was found between males and females (p=1.000).
3.2.5 Occipital unossified midline membrane
An occipital unossified midline membrane was found in 23 cases (7.2%) of which an example is shown in figure 7. All of the cases were in the age group <3 months of which 16 were male and 7 were female. No statistical significance was found between males and females (p= 0.616).
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Figure 8 Skull showing bilateral mendosal sutures (orange arrows) and an occipital unossified midline membrane (blue arrow)
3.2.6 Mendosal suture
Mendosal sutures were found in 76 of the cases (23.9%). Table 7 presents the prevalence of bilateral and unilateral mendosal sutures sorted by sex and age groups. In total a bilateral mendosal suture was found in 66 cases (20.75%) and an unilateral mendosal suture in 10 cases (3.14) of which 4 were located on the left side of the skull and 6 on the right side of the skull. An example of a bilateral mendosal sutures is depicted in figure 8. No statistical significant difference was found between males and females (p= 0.170).
Table 7 Prevalence of bilateral and unilateral mendosal sutures sorted by sex and age group
Age groups Sex Bilateral
mendosal suture* Unilateral mendosal suture left* Unilateral mendosal suture right* Total percentage per age group* <3 months Male 28 (8.81%) - - 14.78% Female 17 (5.35%) 2 (0.63%) - 3-6 months Male 6 (1.89%) - - 4.09% Female 6 (1.89%) - 1 (0.31%) 6-12 months Male 4 (1.26%) 1 (0.31%) 1 (0.31%) 3.14% Female 3 (0.94%) - 1 (0.31%) 12-24 months Male - - 1 (0.31%) 1.26% Female 1 (0.31%) - 2 (0.63%) 24-36 months Male 1 (0.31%) 1 (0.31%) - 0.63% Female - - -
*percentages have been calculated from the whole sample in order to demonstrate the prevalence
3.2.7 Wormian bones
Wormian bones were present in 248 of the cases (78%). Table 8 summarizes the prevalence and location of the wormian bones. Wormian bones were most frequently found in the lambdoid suture (64.2%) with 781 wormian bones in total. The least frequent locations of wormian bones were the naison and sphenofrontal suture only seen in 1 case (0.3%) followed by bregma seen in 2 cases (0.6%). The Statistical significance difference was found between males and females only for the parietal notch (p=0.024).
Table 8 Prevalence and location of Wormian bones Location Number of skulls with at least 1 wormian bone* Total Number of wormian bones Number of skulls with wormian bones on the Left(number
of wormian
bones)/Right(number of wormian bones) side of the skull
Male/Female** Lambdoid suture 204 (64.2%) 788 169(408)/ 153(380) 133(66.5%)/ 71(60.2%) Parietomastoid suture 13 (4.1%) 17 5(5)/ 9(12) 9(4.5%)/ 4(3.4%) Occipitomastoid suture 11 (3.5%) 16 7(10)/ 8(8) 9(4.5%)/ 2(1.7%) Temporosquamosal suture 13 (4.1%) 27 9(14)/ 11(13) 9(4.5%)/ 4(3.4%) Pterion 27 (8.5%) 53 16(26) / 16(27) 14 (7%)/13 (11%) Asterion 13 (4.1%) 18 8(9)/ 9(9) 10 (5%)/3 (2.5%) Coronal suture 11 (3.5%) 16 3(3)/10(13) 10 (5%)/ 1(0.8%) Saggital suture 33 (10.4%) 60 - 21(10.5%)/ 12(10.2%) Bregma (anterior fontanel) 2 (0.6%) 4 - 2 (1%)/ 0(0%) Lambda (posterior fontanel) 94 (29.6%) 123 - 58 (29%)/ 36 (30.5%) Sphenofrontal suture 1 (0.3%) 2 0(0)/ 1(2) 1 (0.5%)/ 0(0%) Naison 1 (0.3%) 1 - 0 (0%)/ 1(0.8%) Parietal notch 42 (13.2%) 52 24(24)/ 28(28) 33 (16.5%)/ 9(7.6%) *** *percentages have been calculated from the whole sample to demonstrate the prevalence
** Percentages have been calculated from the total amount of males versus females ***significant difference with p-value below 0.05
The presence or absence of wormian bones per CT scan is summarised and sorted by age in table 9 along with the number (mean, minimum and maximum) of wormian bones per CT scan. The percentage of cases with wormian bones ranged from 63.3% in age group 36-48 months to 87.3% in age group <3months. The mean number of wormian bones decreased with age from 5.51 in age group <3 months to 2.17 in age group 60-72. The same trend was seen for the total number of wormian bones per age group from 303 in age group < 3 months to 52 in age group 60-72.
Table 9 Distribution of numbers of wormian bones per CT scan (mean [min-max]) by age
*Percentage of cases where wormian bones were present was calculated per age group
Age groups Number of cases* Mean number of
wormian bones Total number of wormian bones <3 months 48 (87.3%) 5.51 (0-33) 310 3-6 months 20 (76.9%) 5.96 (0-31) 155 6-12 months 29 (82.9%) 3.64 (0-22) 130 12-24 months 47 (85.5%) 3.80 (0-18) 205 24-36 months 53 (73.6%) 2.84 (0-20) 206 36-48 months 19 (63.3%) 2.27 (0-10) 66 48-60 months 14 (70%) 2.60 (0-9) 52 60-72 months 18 (72%) 2.17 (0-8) 53
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In this study the shape of every wormian bone was characterized. Irregular shaped wormian bones were found most often (43.65%) followed by wormian bones with a round shape (10.55%). The other characterized shapes were; oval, triangular and quadrangular which were found less frequently with 9.69%, 8.32% and 8.06% respectively. In 19.73% of the wormian bones the shapes were not able to be characterized (table 10).
Table 10 Prevalence of different shapes of Wormian bones
Shapes of Wormian bones No of Wormian bones percentage
Round 121 10.28% Triangular 98 8.33% Quadrangular 96 8.16% Oval 113 9.6% Irregular 508 43.16% Uncharacterizable 241 20.48%
3.2.7.1 Wormian bones at lambda (Inca bones)
A wormian bone at lambda was present 94 cases (29.6%). Wormian bones at lambda are one of the only wormian bones that are given a name; Inca bones. Some of the larger Inca bones are depicted in figure 10. Examples of a single large Inca bone was found in 4 cases of which 2 had a triangular shape, 1 had a quadrangular shape and 1 had an oval shape. Furthermore 1 example of a case with a bipartite Inca bones and 3 examples of cases with a
tripartite Inca bone are shown in figure 9.
A
B
C
D
E
G
F
H
Figure 9 this figure shows the existence of different forms of Inca bones. Single Inca bones with triangular, oval and quadrangular shapes were found (A-B-C-D). Two cases of bipartite Inca bones (E-F) were found and two cases of tripartite Inca bones (G-H).
3.2.8 Craniosynostosis
Craniosynostosis of the saggital suture was most commonly found represented by 11 cases leaving only 1 case showing craniosynostosis of the left coronal suture (Figure 10). Only 1 case showed the presence of an accessory suture namely a complete metopic suture. Wormian bones were present in 6 cases (50%) of which 4 were male and 2 female. Only 1 case with a wormian bone at the anterior fontanel was found, 1 case with a wormian bone at the posterior fontanel (lambda) was found and 5 cases showed wormian bones at the lambdoid suture.
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4. Discussion
4.1 Intra- and inter- variability
The aim of this study was to determine the prevalence of accessory sutures and wormian bones in a contemporary cohort of Dutch children below the age of 6. Intra- and inter-observer reliability was determined to investigate whether accessory sutures and wormian bones could reliably be scored. All accessory sutures, wormian bones and number of wormian bones had substantial, almost perfect or perfect intra- and inter-observer agreement except for accessory sutures in the temporal bones which had fair agreement(k=0.255). As substantial agreement is required for reliable analysis accessory sutures in the temporal bones were left out for further analysis. One of the reasons for the low level of agreement for accessory sutures in the temporal bones is that the anatomy of the temporal bone is very complex with a number of normal variant structures that can become visible in thin slice CT scans44. The scoring of these normal variants can be very difficult for an untrained eye. Furthermore guide lines on how to score this complex bone turned out not to be clear enough in the current study. Therefore, for future research clear guidelines have to be established between experienced observers. Furthermore the temporal bones should be carefully investigated with high quality CT scans by experienced radiologists in order to get reliable data.
4.2 Accessory sutures
This study shows that accessory sutures were present in 34.3% of the cases. The metopic and mendosal suture were seen most frequently with 29.9% and 23.9% respectively. Other accessory sutures that were found included; the intraparietal horizontal suture, intraparietal vertical suture, obelion suture and an occipital unossified midline which were seen less frequently with 2.2%, 0.9%, 3.8% and 7.2% respectively. None of the accessory sutures showed sexual preference. Most accessory sutures were found in the lower age groups and particularly the prevalence of the metopic and mendosal sutures showed a decrease with age.
A metopic suture was found in 29.9% of the cases. This number is similar to other studies which also report prevalence numbers between 20 and 30 percent45–48. However, with 24.8% vs. 5.0% the majority of the metopic sutures in this study were complete, while in literature incomplete metopic sutures are often the majority45,47–49. A reason for this could be that all previous literature is based on adult skulls. A Metopic suture often disappears with age. When the two frontal bones only partly fuse an incomplete suture remains, which apparently happens more often than that the frontal bones don’t fuse at all leaving a complete metopic suture at adult age. One study by Marconian et al. (1959) also investigated the prevalence of the metopic suture in minors below the age of 20 using radiographic films. In their sample of 2018 radiographic films 252 cases (12.48%) showed a metopic suture. This is lower than in this study, however Marciniak et al. (1959) doesn’t clarify whether they include both a complete and incomplete metopic suture or only one of them. This could be an explanation for the difference in prevalence.
In the current study the occurrence of accessory sutures in the parietal bones was rare. This is supported by studies of Hrdlicka (1903) and Shapiro (1972) who found an even lower prevalence of these accessory sutures. The study by Hrdlicka (1903) found 2 complete and 6 minor incomplete intraparietal sutures similar as Shapiro (1972) who only found complete intraparietal sutures in 3 cases out of 25000. The current study found no complete intraparietal sutures which can be explained by the rarity found in the studies by Hrdlicka (1903) and Shapiro (1972). Additionally the sample size, which in the current study is much lower than the other two studies, can be a reason why no complete intraparietal accessory sutures were found. Hrdlicka (1903) indicates that unilateral intraparietal accessory sutures are more prevalent than bilateral with equal frequency of the unilateral intraparietal accessory sutures on the left and right side of the skull. While the results of this study also
show that the prevalence of unilateral intraparietal accessory sutures is higher than bilateral intraparietal accessory sutures, there is a slightly higher prevalence of unilateral intraparietal accessory sutures on the left side of the skull than on the right side.
The only study mentioning the existence of accessory sutures in the parietal bones at the location of the obelion is Currarino et al. (1976). That study only mentions their existence but no prevalence numbers. It could be that the study by Hrdlicka (1903) also included the obelion sutures in their prevalence numbers as it being an intraparietal horizontal accessory suture. This is an example indicating the problem of nomenclature about accessory parietal sutures not being uniform which is more often mentioned in literature27. This also makes it difficult for physicians to look for information when dealing with a particular case. This immediately points out the importance for clear uniform nomenclature in literature about accessory sutures in the parietal bones since they are rare.
In the occipital bone the accessory sutures called, midline unossified membranous strip in the interparietal segment (ip) and mendosal suture, were found in the current study. The midline unossified membranous strip in the IP is mentioned in the study by Shapiro (1976) as an accessory suture in the occipital bone. The current study only found the midline unossified membranous strip in the IP in the age group below 3 months which supports the statement of Shapiro (1976) that this suture mostly closes before birth, but sometimes persists for a short period of time after birth and then closes. The other accessory suture that was found in the occipital bone in this study was the mendosal suture with a prevalence of 23.9% which is higher than previously mentioned prevalence numbers, based upon adult dry skulls21,30,31. The study by Gurses et al. (2016) is the only study which also investigated the prevalence of the mendosal suture in a sample of children using CT scans. They reported a slightly higher prevalence of 32.7% of the mendosal suture50. They also reported that the mendosal suture occurred bilaterally more frequently than unilateral which supports the findings of the current study.
4.3 Wormian bones
Besides the prevalence of accessory sutures, this study also investigated the prevalence of wormian bones. In literature a range of prevalence numbers of wormian bones is mentioned with most studies reporting prevalence above 50%. The current study showed a prevalence of 78% which is therefore supported by literature. The range of prevalence numbers found in literature could be explained by the various methods used in the different studies as well as by the fact that not every study investigates the same locations or same number of locations. Additionally, as mentioned in the introduction most studies on the prevalence of wormian bones are performed on dry adult skulls rather than using 3D reconstructions of CT scans as was done in the current study.
The percentage of cases with wormian bones in the current study ranged from 63.3% in age group 36-48 months to 87.3% in age group <3months. This indicates that the percentage of cases with wormian bones did not decrease with age. This is similar to what Marti et al. (2013) reported. That study used a similar method as in the current study, but the age range of their sample was smaller only from age 0 to 3. The current study showed the highest frequency of wormian bones in the lambdoid sutures which is supported by several other studies34,40,51–53. The only significant differences between male and female on the occurrence of wormian bones was found at the parietal notch (p=0.024). The study of Sadhu et al. (2013) is the only other study that also specifically looks at the parietal notch for the presence of wormian bones. However, they reported no statistical significant difference between male and female54. A plausible explanation for the fact that only one other study mentions the parietal notch could be that other studies classify them as being in the squamosal sutures or the parietomastoid suture as the parietal notch indicates border between these two sutures. This shows that nomenclature and classifying methods between studies is not uniform as was also previously seen for accessory sutures. Another study that illustrates the problem of classifying wormian bones is the study by Kumar et al. (2016). They report the prevalence of wormian bones at asterion while they are actually not placed at the asterion as shown by a
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reference figure in that study51. This is part of the reason that a range of frequencies are can be found in literature.
When looking at the difference of wormian bones between females and males the current study only found a significant difference for the parietal notch. Literature seems to be controversial when looking at whether or not there are significant differences in the prevalence of wormian bones between males and females54–57. The same trend can be seen when looking at the frequency of wormian bones on the right side of the skull versus the left side of the skull. Depending on the study some find that wormian bones occur more frequently on the right side of the skull while other studies find them more frequently on the left side of the skull or equally frequent51,54. Why Wormian bones develop is not fully understood and therefore debated in literature, which is indicated by the sometimes contradicting literature58. This is another reason why studies like the current one are very important.
4.4 Craniosynostosis
Literature suggests that wormian bones are more frequently found in cases of craniosynostosis than in the general population39,59. For this reason a separate subset was made of the cases with craniosynostosis. The study by Sanchez-Lara et al. (2007) indeed found significantly more wormian bones in 3D CT scans from cases with craniosynostosis than in normal dry skulls. In the current study 50% of the craniosynostosis cases showed wormian bones while in the normal population of this study this was 78% which therefore doesn’t support the results of the study from Sanchez-Lara et al. (2007). The study by Marti et al. (2018) also doesn’t support the results of Sanchez-Lara et al. (2007). This indicates that the literature upon this subject is somewhat controversial. Since the sample size of the current study is very limited no reliable conclusions could be made. Therefore this is an area upon which future research could be focussing.
4.5 Limitations
While this study has a lot of positive points it also contains some limitations that have to be mentioned. One of the biggest limitations of this research is the lack of an available golden standard to differentiate between a fracture and an accessory suture or wormian bone. While all the suspected fractures in this study where checked by an experienced radiologist, this was not the case for every accessory suture or wormian bone. Besides, even for an experienced radiologist it can be difficult to be certain of a diagnosis as indicated by the aim of this research. The only method which can give a definitive answer to the question whether it is a fracture, an accessory suture or a wormian bone is histological examination. However, since this research was performed in living children histological examination was not possible. The distinction between a fracture and accessory suture or wormian bone in this study was based on the different radiological characteristics as earlier explained in the introduction. Sometimes medical history or reasons for making the CT scan can give additional information which could be useful for making a diagnosis, but since this study used fully anonymized data, meaning that no personal or medical history was known other than the sex and age, this kind of information was not available. As a result, while this study does provide prevalence numbers of various accessory sutures and wormian bones the results have to be interpreted and used with care.
Furthermore 3D volume rendering CT images were used in the current study to determine the prevalence of accessory sutures and wormian bones. While the study by Dundamadappa et al. (2015) shows that the sensitivity of 3D volume (3DV) - rendered CT images is equal to routine axial bone window images it does require thin slice CT scans. The dataset of the current study initially consisted of 532 cases, but after exclusion of certain cases 330 cases remained. One of the exclusion criteria was insufficient CT data due to high slice thickness of the CT scan, which thereby substantially decreased the sample size of this study. The cut off value was everything above 1mm and some of 1mm turned out to be insufficient as well which was determined on a case to case bases. The study by Ford et al. (2015) investigated the optimal slice thickness for reliable 3D reconstructions. According to their study a
maximum CT slice thickness of 1.25mm is required when forensic practitioners use 3D reconstructions in casework60. Therefore it is important to note that it would be beneficial for research purposes especially for forensic purposes if CT scans are made with the thinnest slices possible60. Otherwise interpretation of CT scans could be negatively influenced. However it has to be noted that decreasing the slice thickness could result in higher dose of radiation. Exposure to radiation is linked to an increased risk of among others cancer, which is probably a reason why sometimes higher slice thickness CT scans is preferred. Therefore, careful decisions about which slice thickness of the CT scan can be used have to be made by critically assessing the benefits and risks.
4.6 Practical implications
Knowledge about the prevalence of accessory sutures and wormian bones and their possible locations are important to distinguish anatomical variants from pathologies such as fractures on imaging61. Wormian bones can give the appearance of fractured segments and sometimes when they are large enough they can look like accessory sutures. This study showed that the prevalence of accessory sutures decreases with age while the prevalence of wormian bones did not show this trend. This means that the chance of finding an accessory suture in older children decreases while the presence of wormian bones is still something to consider. The majority of suspected child abuse cases involve children below the age of 2. According to this study wormian bones and especially accessory sutures are frequently found in this age group meaning that the presence of these variants have to be carefully considered by the physicians or forensic specialists when making a diagnosis62. The knowledge about the locations of the various accessory sutures and wormian bones as presented in this study will aid in making a diagnosis. As shown by the low inter-observer agreement for accessory sutures in the temporal bone this part of the skull was hard to score. One of the reasons for this is that the temporal bone is a complex bone with a number of normal variant sutures and fissures. It is important for physicians and forensic specialists to be aware of these variants. Therefore, future research should focus on the prevalence these variants and other accessory sutures in order to increase the knowledge on this complex bone.
4.7 Future research
Future research is necessary in order to gain and improve the knowledge about accessory sutures and wormian bones in children. The current study could be improved by addressing the lack of a golden standard in future research. This could be achieved by either using only cases which have multiple CT scans with a substantial amount of time in between or by using pseudo anonymized patient data. Using only cases with multiple CT scans with two or three months in between would allow for fractures to show healing characteristics or sclerosis, which accessory sutures and wormian bones would not show. This could aid in the differentiation between fractures, accessory sutures and wormian bones. However, with this approach selection bias is introduced, as only cases with multiple CT scans can be included, which results in another limitation. Another alternative is to have access to patient’s medical history and reasons for making the CT scan. This study was based on fully anonymized data which means that no personal or medical history was known other than the age and sex of the patient63. This prevented access to medical history, personal data or reasons for making the CT scans. Not knowing the reasons for making the CT scans could have potentially introduced selection bias in this study if the reasons for making the CT scans included suspicion for accessory sutures, wormian bones or fractures more than in a general population. Pseudo anonymized data would prevent this problem but performing retrospective research with pseudo anonymized data can be difficult especially after the introduction of the new privacy laws. Since the 25th of May the new GDPR law is in force in the EU63. This law differs from the Data protection act on some points and it is intended to ensure that all EU residents have more control over the use of their personal data63. This new law also has its influence on doing scientific research meaning that informed consent is necessary for retrospective research that is not fully anonymized. This means that using
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pseudo anonymized data does require consent from the patients or their parents which will make it more difficult to perform this kind of research. Therefore the new GDPR law does provide protection for EU citizens but is does have its effects on doing research as shown by this study.
Lastly as explained earlier the assessment of accessory sutures in the temporal bone was not found reliable in this study. Future research should carefully investigate the temporal bone with high quality CT scans by experienced radiologists in order to get reliable data. This could be achieved by establishing a detailed guideline for the scoring of the temporal bone and its complex anatomy, by experienced radiologists. Additionally the radiologists have to assess a number of cases together in order to establish a similar basis for assessing the temporal bone.
5. Conclusion
In this research the prevalence of accessory sutures and wormian bones was determined in a contemporary cohort of Dutch children below the age of 6. This research found several accessory sutures including; the metopic suture, intraparietal horizontal suture, intraparietal vertical suture, obelion suture, midline unossified membranous strip in the interparietal segment (ip) and the mendosal suture. This research showed that the highest prevalence of accessory sutures was found in the lower age groups and that it decreased with age while for the prevalence of wormian bones this trend was not seen. This knowledge and the specific locations of the accessory sutures and wormian bones are beneficial for physicians and forensic specialists to make a differential diagnosis in cases of suspected child abuse. While this study does provide prevalence numbers of various accessory sutures and wormian bones, because of several limitations the data has to be interpreted and used with care. Future research is necessary in order to get more reliable data especially for prevalence of accessory sutures in the temporal bone.
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Acknowledgements
First of all I would like to thank Rick van Rijn for giving me the opportunity to perform this study and for his guidance and enthusiasm throughout the project. Furthermore I would like to thank Kerri Colman and Hans de Boer for their willingness to guide me throughout the project when Rick van Rijn wasn’t able to. Of course I also have to thank Roelof-Jan Oostra for being the examiner of my project. Furthermore, there are also a couple of people which had smaller roles during my project but nonetheless not less important. I would like to thank Joost van Schuppen for being the second observer for the data. I would like to thank Jean-Paul Geerets for answering al my IT related questions. Lastly thanks to everyone from the Amsterdam UMC involved during this project.
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Appendix A Glossary
Anterior Directed towards the front of the body
Asterion The point behind the ear where the parietal, temporal and occipital bones meet
Bilateral Two-sided
Bregma Where the saggital and two coronal sutures meet, previously the anterior fontanel
Caudal Directed towards the feet of the body
Cranial Directed towards the head of the body
Craniosynostosis Premature fusion of the sutures of the skull
Inca bone Sutural bone located at the previous site of the posterior fontanel
Lambda Where the saggital and two lambdoid sutures meet, previously the posterior fontanel
Obelion Region of the skull situated between the two parietal
foramina, where the saggital suture is normally of a more simple type and were its closure usually begins
Parietal notch Parietal notch is that part of the parietal bone that
protrudes between the squamous and the mastoid portions of the temporal bone
Posterior Directed towards the back of the body (opposite of anterior)
Pterion The point on each side of the skull where the parietal and temporal bones meet the greater wing of the sphenoid
Appendix B Case Report Form (CRF)
Case Report Form
Case number: Sex: ☐ Male ☐ Female ☐ Unknown
Age:
CT parameters:
Slice thickness _____ mm
Case example figure? ☐ Yes ☐ No
Remarks:
Normal sutures
☐ Yes ☐ NoLocation Left Right Suture closure
☐ Coronal suture ☐ ☐ ☐ Complete ☐ Incomplete ☐ Open ☐ Saggital suture ☐ Complete ☐ Incomplete ☐ Open ☐ Lambdoid suture ☐ ☐ ☐ Complete ☐ Incomplete ☐ Open ☐ Temporosquamosal suture ☐ ☐ ☐ Complete ☐ Incomplete ☐ Open ☐ Sphenosquamosal suture ☐ ☐ ☐ Complete ☐ Incomplete ☐ Open ☐ Parietomastoid suture ☐ ☐ ☐ Complete ☐ Incomplete ☐ Open ☐ Occipitomastoid suture ☐ ☐ ☐ Complete ☐ Incomplete ☐ Open ☐ Sphenofrontal suture ☐ ☐ ☐ Complete ☐ Incomplete ☐ Open ☐ Sphenozygomatic suture ☐ ☐ ☐ Complete ☐ Incomplete ☐ Open Remarks:
