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Geometrical Properties of the Human Child Cervical Spine With a Focus on the C1 Vertebra a
a
b
Narayan Yoganandan , Frank A. Pintar , Sean M. Lew & Raj D. Rao a
c
Department of Neurosurgery , Medical College of Wisconsin , Milwaukee , Wisconsin
b
Department of Neurosurgery, Medical College of Wisconsin , Childrens Hospital of Wisconsin , Milwaukee , Wisconsin c
Department of Orthopaedic Surgery , Medical College of Wisconsin , Milwaukee , Wisconsin Accepted author version posted online: 29 Jul 2013.Published online: 27 Dec 2013.
Click for updates To cite this article: Narayan Yoganandan , Frank A. Pintar , Sean M. Lew & Raj D. Rao (2014) Geometrical Properties of the Human Child Cervical Spine With a Focus on the C1 Vertebra, Traffic Injury Prevention, 15:3, 287-293, DOI: 10.1080/15389588.2013.811719 To link to this article: http://dx.doi.org/10.1080/15389588.2013.811719
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Traffic Injury Prevention (2014) 15, 287–293 ISSN: 1538-9588 print / 1538-957X online DOI: 10.1080/15389588.2013.811719
Geometrical Properties of the Human Child Cervical Spine With a Focus on the C1 Vertebra NARAYAN YOGANANDAN1, FRANK A. PINTAR1, SEAN M. LEW2, and RAJ D. RAO3 1
Department of Neurosurgery, Medical College of Wisconsin, Milwaukee, Wisconsin Department of Neurosurgery, Medical College of Wisconsin, Childrens Hospital of Wisconsin, Milwaukee, Wisconsin 3 Department of Orthopaedic Surgery, Medical College of Wisconsin, Milwaukee, Wisconsin 2
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Received 22 February 2013, Accepted 2 June 2013
Objective: Child dummies and injury criteria used in automotive crashworthiness environments are based on scaling from the adult and/or between children of different ages. Cartilage-to-bone ossification, spinal canal and joint developments of the spine, and strength attainments do not grow linearly from birth to maturity. Though this is known to medical professionals, age-based quantitative analyses are needed to accurately model the pediatric spine. The objective of this study was to quantify longitudinal growths of various regions of the first cervical vertebrae, responsible for transmitting the axial load from the base of the skull through the condyles to the neck/torso. Methods: Computed tomography (CT) images of 54 children from one day to 18 years of age were retrospectively used to determine the following geometrical properties: bilateral neurocentral synchondroses widths, the width of posterior synchondrosis, outer and inner anteroposterior and transverse diameters, spinal canal area, and depths of the anterior and posterior arches of the C1 vertebra. Both axial and sagittal CT images were used in the analysis. Sagittal images were used to quantify data for the anterior and posterior arches and axial images were used for all described cross-sectional parameters. Results: Geometrical properties were extracted and reported for the various parameters at 6 months; one year; 18 months; and 3, 6, and 10 years of age corresponding to the dummy family ages routinely used in motor vehicle crashworthiness research and other applications. The outer transverse diameter ranged from 4.97 to 7.08 cm; outer and inner antero-posterior diameters ranged from 2.99 to 4.18 and 2.19 to 3.03 mm; and spinal canal area ranged from 4.34 to 6.68 mm2. Other data are given in the body of the article. The growths of the first cervical vertebra quantified in terms of the above variables occurred nonlinearly with age and the degree of nonlinearity depended on the type of the geometrical parameter. Growths did not match with the simple scaling ratios based on the adult spine, used in different studies reported in the current literature. Conclusions: These early nonlinear and nonuniform age- and local geometry–specific variations should be considered in human finite element models for an accurate transfer of the external load from the atlas to the subaxial spine and to improve their fidelity and biomechanical capabilities. Keywords: children, biomechanics, safety, biofidelity, pediatric cervical spine, atlas
Introduction Six-month-old; one-year-old; 18-month-old; and 3-, 6-, and 10-year-old anthropomorphic test devices, also frequently referred to as dummies in automotive literature, are used in motor vehicle crashworthiness evaluations and for the understanding of injuries from fall-related events to children (Bertocci et al. 2003; Kapoor et al. 2008; Kleinberger, Sun, et al. 1998; Kleinberger, Yoganandan, and Kumaresan 1998; Yoganandan et al. 2001). The rationale for the development
This article not subject to U.S. copyright law Address correspondence to Narayan Yoganandan, PhD, Professor of Neurosurgery and Orthopaedic Surgery, Chair, Biomedical Engineering, Department of Neurosurgery, Medical College of Wisconsin, 9200 West Wisconsin Ave., Milwaukee, WI 53226. E-mail: [email protected]
of age-specific pediatric test devices for advancing safety to this population can be stated as follows. In general, the age group between newborn to one year can be skeletally represented by the presence of 3 primary ossification centers for the human spine. The group between one and 3 years of age can be represented by the fusion of the posterior or dorsal synchondrosis (Sherk and Parke 1989). The group between 3 and 6 years of age signifies the fusion of primary ossification centers (Yoganandan, Kumaresan, et al. 1998). Dummies have been developed by largely ignoring these patterns despite these recognitions; that is, their necks are essentially scaleddown versions from the adult, which have no ossification and growth issues. Anatomical textbooks provide descriptions and associated implications for physiological functions including head–neck stability issues of the growing child (Bailey 1952; Bird and Darling 2001; Clark 1998; Ganey and Ogden 2001; Weinstein 1994; Williams 1995; Yoganandan et al. 2008). However, descriptions are largely general in nature and
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288 quantifications on the development of vertebrae with specific reference to age groups used in pediatric dummies for motor vehicle applications are not their principal foci. The objectives of the present study are therefore to quantify longitudinal growths of various regions of the first cervical vertebra (also called the atlas), the component of the spine responsible for transmitting the axial load from the base of the skull through the condyles to the neck/torso. Specifically, properties are obtained for various geometrical parameters at 6 months; one year; 18 months; and 3, 6, and 10 years corresponding to the dummy family and the ratios of these properties are determined based on adult data. A brief description of the growth of this transitional vertebra is presented first, to enable the reader to place the current study in perspective. Briefly, the first vertebra is a unique bone in the entire human spinal column. It is formed from 3 primary ossification centers: one occurs in the anterior region and 2 occur bilaterally in the posterior neural arches. The former center develops several months following birth and the other 2 centers are present at the time of birth. The junction between the anterior and bilateral posterior centers is called the neurocentral synchondrosis. The 2 neural arch centers fuse or join dorsally at the posterior synchondrosis (Hinck et al. 1962; Tulsi 1971; Yousefzadeh et al. 1982). The presence of the 3 cartilaginous synchondrose junctions allows for the latitudinal and longitudinal growths of the cervical vertebra (Bick 1952; Carpenter 1961; Gooding and Neuhauser 1965; Haas 1939; Oda et al. 1988; Roaf 1960). The 2 growths contribute to the maturation processes of this bone and, as indicated earlier, age-specific developments of these regions corresponding to automotive dummy ages are not quantified. The bilateral facet bones of the vertebra contribute to the structural load transfer from the head to the subaxial spine, and the development of this region along with the other components contributes to the overall load carrying capacity of the vertebra. Because of the absence of the vertebral body and intervertebral discs at the rostral and caudal ends that act as anterior joints at each level, the growth of the ring in the latitudinal and longitudinal directions is important and studied in this retrospective investigation using human subject data across all child ages.
Methods All data were extracted from a pediatric level 1 trauma center in the state of Wisconsin. The retrospective research study was approved by the institutional review board of the authors (approval number HRRC 088-03, Children’s Hospital of Wisconsin). Head–neck radiographs and computed tomography (CT) scans were obtained as part of routine imaging evaluations of pediatric patients presenting to the emergency room. Most of these scans were obtained to rule out traumatic injuries. All images were initially reviewed by pediatric radiologists and followed by neurosurgeons and orthopedic surgeons. The cervical spines were determined to be negative for fracture/dislocation, epiphyseal injury, or other type of abnormality. Patients with demonstrable clinical history such as congenital or developmental disease, neoplastic growth,
Yoganandan et al. adverse neurological conditions, vertebral and muscular abnormalities, spine surgery, and scoliosis, which might affect normal vertebral growth, were excluded from the study. This was assessed using medical records. Conventional x-rays were obtained and a high-resolution CT scanner (Somatom Plus 4, Siemens, Erlangen, Germany) was used to obtain spine images according to established clinical protocols of the institution. Axial and sagittal reconstruction images obtained as a part of the screening protocol were used for the quantitative analyses. Sequential axial and sagittal images were used to determine the geometry of the C1 vertebra. The following geometrical measurements were obtained (Figure 1). Axial images were used to determine widths of the bilateral neurocentral synchondroses; the width of the posterior synchondrosis; outer and inner antero-posterior and transverse diameters; and spinal canal area. Depths of the anterior and posterior arches were obtained from sagittal images. All geometrical variables were expressed using mathematical functions across the entire age spectrum. Variations were defined as those with R2 greater than 60 percent for nonlinear age-related responses. The maturation magnitude was defined as the value of a parameter at the adult age, corresponding to 18 years, with the exception of the anterior and posterior synchondroses, which were defined at the youngest age. Parameters were extracted at 6 months; one year; 18 months; and 3, 6, and 10 years.
Results Retrospective data from 54 pediatric subjects with ages ranging from one day to 211 months were analyzed in the study. There were 39 boys and 15 girls in the subject population. Six measurements were repeated for 15 subjects by one researcher for intra-observer repeatability and all of these measurements were repeated for 15 random subjects by another researcher for interobserver reproducibility. Across all measures, coefficients of repeatability for intra- and interobserver studies were on average 4 and 6 percent and the coefficient of repeatability for the intra-observer reproducibility was an average of 2.3 percent less than interobserver reproducibility. In general, differing types of growth/maturation patterns were found for all geometric parameters considered in the study. The anterior neurocentral and posterior synchondroses coalesced at
Fig. 1. (Left) Axial view of an immature C1 vertebra illustrating the posterior and anterior synchondroses (PS and AS) shown as gaps and (right) vertebra from another subject demonstrating the various dimensions extracted in the present study from the axial view.
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The Human Child Cervical Spine 31 and 27 months. The linear regression fits for these parameters resulted in R2 of 0.8 and 0.6, respectively (Figure 2). These early bony growths represent the initial development of the C1 vertebra in the human cervical spine. The inner transverse diameter was invariant with increasing age, as identified by the very low R2 (0.1). In contrast, the mean outer and inner antero-posterior and outer transverse diameters, spinal canal area, and depths of the anterior and posterior arches showed logarithmic variations in the development process. The respective R2 values for these parameters are included (Figure 2). The maturation magnitudes of the 2 synchondroses, outer and inner antero-posterior and outer transverse diameters, spinal canal area, and depths of the anterior and posterior arches are shown (Figure 3). The P values were less than .0001 for all parameters with the following exceptions: the P values for the posterior synchondrosis and inner transverse diameter were .0045 and .0725, respectively. The percentages representing the development processes of the outer and inner antero-posterior diameters are shown in Figure 4, the outer transverse diameter in Figure 5, the depths of the anterior and posterior arches in Figure 6, and the spinal canal area in Figure 7, normalized with respect to the adult age group. The growths of the 2 antero-posterior diameters were such that their adult-based ratios ranged from 0.68 to 0.95 for the 6-month-old to the 10-year-old spines. These data for the transverse diameter ranged from 0.66 to 0.94, for the spinal canal area from 0.61 to 0.94, and for the vertical depths of the posterior and anterior arches from 0.53 to 0.92 and 0.48 to 0.91, respectively. The ossifications of the anterior and posterior synchondroses were such that their ratios (normalized with respect to zero years of age) decreased from 0.81 to 0.42 and 0.78 to 0.33 from 6 to 18 months of age (Figure 8).
Discussion As indicated in the Introduction, the aim of the study was to quantify various geometrical parameters of the C1 vertebra at 6 months; one year; 18 months; and 3, 6, and 10 years corresponding to the dummy family and determine the ratios
Fig. 2. R2 values from left to right: anterior and posterior synchondroses, outer transverse and inner and outer antero-posterior diameters, canal area, and anterior and posterior arch depths.
289
Fig. 3. Maturation magnitudes from left to right: anterior and posterior synchondroses, outer transverse and inner and outer antero-posterior diameters, spinal canal area, and anterior and posterior arch depths.
of these properties based on adult data. This study focused on the C1 because it is the first vertebra of the neck, the first load-bearing element from the base of the skull, and is unique in the entire vertebral column. Any axial load transmitted from the head or facial skeleton to the neck and torso always traverses through the C1 vertebra. This is true even when the external load is applied eccentrically on the head/face. Furthermore, vital structures are housed at the upper cervical spine (occipito-atlanto-axial complex) in the human. Because the mass of the head is disproportional to the neck structure, especially at younger ages, the anatomy of C1 plays a role in the mechanism of load transfer. The objectives were achieved by obtaining retrospective CT scans from pediatric subjects of various ages, from one day to 18 years of age. CT scans were selected due to their ability to show cross-sectional images, which is critical because the unique ring shape of the bone of the human cervical spine does not permit the use of appropriate views from x-rays (Ford
Fig. 4. Growth of the 2 antero-posterior diameters normalized with respect to the adult.
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290
Fig. 5. Ratios of the outer transverse diameters normalized with respect to the adult.
et al. 1982; Junewick et al. 2011). In addition, x-rays provide an integrated image of the spine only in the lateral and anteroposterior or postero-anterior projections (Ogden et al. 1994; Yoganandan, Pintar, et al. 1998). Although magnetic resonance imaging is another modality, it was not adopted because of practical limitations in obtaining scans, difficulties in extracting osseous details because the resolution and focus of the images are on soft tissues, and the existence of motion artifacts present in the very young. Furthermore, CT is a more standard clinical protocol than the other imaging modality in the Western world (AuYong and Piatt 2009). However, the limited sample size of 54 used in the present study was inadequate to differentiate between the sexes, and in order to fully include such variables it would be necessary to extend this line of research. Along the same vein, it would be necessary in the future to quantify the age-dependent ossification and development of bony regions of another unique vertebra, C2, which has 5 ossification centers in contrast to the 3 in the C1 vertebra (Ogden 1984). As indicated, the present retrospective study provided a snapshot of the pediatric subject vertebra at the time of CT
Fig. 6. Ratios of the depths of the 2 arches normalized with respect to the adult.
Yoganandan et al.
Fig. 7. Ratios of the spinal canal areas normalized with respect to the adult.
scanning. Consequently, ossifications and growth patterns of the bone for the same subject were not followed over time. Though this approach may not have revealed the specific agerelated patterns for the various measures on an individual subject basis, data are applicable because they were grouped into one ensemble. Furthermore, obtaining longitudinal CT scans for the entire 18-year period covered in the present study is not only time consuming and difficult to execute, but normal attrition in such an approach limits the usability of data at the end of the collection process. Recent recognition of the increased radiation exposure from CT scanning (for no direct medical reasons) and difficulties in obtaining institutional review board approvals are other constraints of such a methodology (Baumann et al. 2011; Brunetti et al. 2011; Tsalafoutas and Koukourakis 2010). Hence, the practical and feasible approach of retrospective analysis of emergency room patient scans was adopted in the present study. As can be appreciated from the relatively high R2 exceeding 0.6 in all but one case (Figure 2), baseline data obtained from this study are considered reliable for the different age groups.
Fig. 8. Ratios of the widths of the 2 synchondroses normalized with respect to the newborn. The anterior and posterior synchondroses close at approximately 31 and 27 months.
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The Human Child Cervical Spine
Fig. 9. Age-dependent ratios (reported in the literature; see text for details) of the total body mass, sitting height, neck mass, and neck circumference based on the adult.
It should be noted that the male dummy used for automotive applications represents a 45-year-old occupant. However, the present study considered the adult age to be 18 years. Because human spinal vertebrae reach adult size by this age, geometrical changes are not expected between 18 and 45 years. Another potential application of these geometric parameters corresponding to the specific age groups is their incorporation into stress analysis models. Finite element models can be used as a starting point for clinical applications and as an adjunct to dummy experiments such as sled tests to evaluate spinal internal responses for motor vehicle applications. Results from the present study are valuable for these advancements because current pediatric stress analysis–based finite element models lack anatomic fidelity and models do not exist for clinical applications (Kumaresan et al. 1997; Mizuno et al. 2005). This study focused on dummy-specific age groups to be relevant to occupant safety in motor vehicle environments and to aid in safety standards. For the most part, scaling factors and methods have been developed based on the adult (Kleinberger, Yoganandan, and Kumaresan 1998; Mertz et al. 1997; Schneider 1983; Snyder 1977; Weber and Lehman 1985; Yoganandan, Kumaresan, et al. 1998; Yoganandan et al. 2000). Recognizing the inconsistency in scale factors (Figure 9), in an early computational research study, agespecific human pediatric cervical spine models were created by geometrically scaling the adult spine to the one-, 3-, and 6-year-old sizes (Kumaresan et al. 2000). Briefly, the procedure consisted of increasing the size of the anatomically accurate adult model to 125, 150, and 175 percent, determining the biomechanical responses and then back-extrapolating the determined responses via regression to respective pediatric age sizes using scaling factors of 0.58, 0.62, and 0.66. The initial scaling-up process was necessary because shrinking the adult model to represent the respective child models posed computational instability issues. This approach disregarded the local geometrical and material properties of the spine. Another approach consisted of assigning differing material properties to the adult model without changing the anatomical geometry. The third approach combined the 2
291 scaling schema and results indicated the overriding influence of the anatomy and geometry on biomechanical responses (Kumaresan et al. 2000). The authors concluded that these scaling methods represent only a first step in the modeling process, which should be followed by additional anatomic and geometrical studies to obtain realistic responses. In a more recent study, a 3-year-old child finite element model was developed from the 50th percentile adult male Total Human Model for Safety and the neck scaling factor was set at 0.5 for the pediatric model (Iwamoto et al. 2002; Mizuno et al. 2005). As before, the model did not have the anatomical shape of pediatric vertebra and the authors concluded (similar to the earlier study discussed above) that more detailed modeling of child anatomical structures is needed. Using the age-specific outer anteroposterior diameter ratios with respect to the adult as a basis to compare with the dummy scale factors based on scaling from the adult neck circumference, the scaled dimension of the child would be off from 0.09 for the 6-month-old to 0.21 for the 6year-old (Figure 10), and this corresponds to a 15 to 32 percent change. The identified characteristic features of the growing spine for all dummy-specific age groups are valuable to relax the assumptions made in existing models in order to accurately delineate the age-specific responses of pediatric spines. Although the closures of the anterior and posterior synchondroses occurred very early, a finding paralleling qualitative anatomic textbooks, the rate of closure was different between the 2 regions of the bone. The growth of the cartilage to the bony components at the 6-month, one-year, and 18-month periods were such that the posterior closures were quicker than the anterior, and by 18 months of age approximately two fifths and one third of the anterior and posterior cartilage were converted to the bony component (Figure 8). It
Fig. 10. Age-dependent ratios of various geometrical parameters based on the adult. Black bars to the right in each age group show the ratio based on the dummy scaling factor used in automotive studies. Legend from left to right: outer antero-posterior diameters (OAD) and outer transverse diameter (OTD); dummy scaling refers to scaling factor based on adult neck circumference.
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292 is therefore important to ensure that the younger age human cervical spine models include appropriate bony and cartilage geometrical features for realistic stress analysis outputs. For the 2 younger groups (6 months and one year), cartilage effects are more important and should be separately modeled with their own constitutive laws. In general, pediatric injuries involve more soft tissues than the adult spine because the growing bone is shielded by cartilage and other soft tissues. Because of differences in the material properties between the cartilage and bone, simulating the cartilage in pediatric spines alters the kinematics. Specifically, increases in the flexibility of the spine due to the presence of the cartilage affect local ligament–bone responses. Such realistic simulations provide insights into injuries such as atlanto-occipital and atlano-axial dislocations wherein fractures do not always accompany ligamentous and unstable/serious injuries. The inner transverse diameter represents the lateral-tolateral clear distance between the tubercles that divide the vertebral foramen to accommodate the dens anteriorly and cord posteriorly. The age-invariant pattern of the diameter indicates that human cervical spine models should have the same dimension regardless of age, from 6 months to 18 years of age. This unique feature coupled with the early age-specific closure (before 3 years), as discussed above, constitute the necessary anatomical intricacies for incorporation into younger age cervical spine models. In contrast, all other dimensions matured nonlinearly with increasing age. The outer and inner antero-posterior (Figure 4) and outer transverse (Figure 5) diameters developed almost uniformly with adult-based ratios ranging from 0.7 to 0.9, and the inner diameter matured somewhat earlier than the outer antero-posterior counterpart. In contrast, the depths of the anterior and posterior arches (Figure 6) showed a slower growth trend, ranging from 0.5 to 0.9 of adult values for different age groups. These results suggest that the latitudinal geometry matures earlier than the longitudinal geometry. From a cross-sectional perspective, because the maturation process begins early—that is, responding with greater diameters contributing to greater areas and hence volume—the load-carrying capacity of this vertebra increases rapidly. This may lead to an early stable upper cervical spine, and these results parallel clinical and biomechanical studies wherein cross-sectional geometry has been considered to be an important factor in segmental and overall cervical column stability (Denis 1983; Yoganandan et al. 2012). A recent study showed that the increased segmental support area and interfacet width, similar measures of outer and inner latitudinal diameters, contribute to cervical spine stability and strength (Stemper et al. 2008). From these perspectives, the aforementioned early, nonlinear, and nonuniform age- and local geometry–specific variations should be considered in human finite element models for an accurate transfer of the external load from the C1 vertebra to the subaxial spine and to improve their fidelity and biomechanical capabilities. The above discussion on the latitudinal and longitudinal growth processes is applicable in general to all vertebrae, although the times of attainments of the maturation may differ depending on the spinal level/region. For example, C2 has 5 ossification centers in contrast to the 3 centers present in all vertebrae, again due to its own characteristic developmen-
Yoganandan et al. Table 1. Summary of parameters as a function of dummy-specific age Parameter Anterior synchondrosis Posterior synchondrosis Outer antero-posterior diameter Inner antero-posterior diameter Outer transverse diameter Inner transverse diameter Spinal canal area Anterior arch depth Posterior arch depth
6 Months 1 Year 1.5 Years 3 Years 6 Years 10 Years Adult 0.75
0.57
0.39
0.00
0.00
0.00
0.00
0.67
0.48
0.28
0.00
0.00
0.00
0.00
2.99
3.27
3.43
3.70
3.98
4.18
4.42
2.19
2.39
2.50
2.69
2.89
3.03
3.20
4.97
5.46
5.74
6.23
6.72
7.08
7.49
2.32
2.32
2.32
2.29
2.24
2.18
2.05
4.34 0.47
4.88 0.57
5.20 0.63
5.74 0.72
6.28 0.82
6.68 0.89
7.13 0.98
0.56
0.66
0.72
0.82
0.92
0.99
1.07
All measurements in cm, except area (in square cm).
tal anatomy. From this perspective, it would be necessary to conduct a similar analysis and quantify growth patterns. In principle, the progress of the ossification process is true for other vertebrae. The number of ossification centers is the same in C1 and other typical vertebra, except the axis (C2), which has 5 centers. From this perspective, it would be necessary to quantify the growth Table 1 of C2 separately. Along the same vein, because the atlas is also unique in its formation and geometry, it would be prudent to at least follow a similar process of quantification to another typical bone, C3 to C7. In other words, quantifications of C2 and one of the C3 through C7 vertebra are needed to more accurately capture the developmental process of the human cervical spine. Though more subjects analyzed for C1 will assist in testing differences in the geometrical parameters between factors such as males versus females, as a first step, the authors recommend similar studies first with other pediatric vertebrae.
Acknowledgments This study was supported in part by the Department of Veterans Affairs Medical Research and Department of Neurosurgery, Medical College of Wisconsin, Milwaukee, Wisconsin.
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Traffic Injury Prevention Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/gcpi20
Geometrical Properties of the Human Child Cervical Spine With a Focus on the C1 Vertebra a
a
b
Narayan Yoganandan , Frank A. Pintar , Sean M. Lew & Raj D. Rao a
c
Department of Neurosurgery , Medical College of Wisconsin , Milwaukee , Wisconsin
b
Department of Neurosurgery, Medical College of Wisconsin , Childrens Hospital of Wisconsin , Milwaukee , Wisconsin c
Department of Orthopaedic Surgery , Medical College of Wisconsin , Milwaukee , Wisconsin Accepted author version posted online: 29 Jul 2013.Published online: 27 Dec 2013.
Click for updates To cite this article: Narayan Yoganandan , Frank A. Pintar , Sean M. Lew & Raj D. Rao (2014) Geometrical Properties of the Human Child Cervical Spine With a Focus on the C1 Vertebra, Traffic Injury Prevention, 15:3, 287-293, DOI: 10.1080/15389588.2013.811719 To link to this article: http://dx.doi.org/10.1080/15389588.2013.811719
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Traffic Injury Prevention (2014) 15, 287–293 ISSN: 1538-9588 print / 1538-957X online DOI: 10.1080/15389588.2013.811719
Geometrical Properties of the Human Child Cervical Spine With a Focus on the C1 Vertebra NARAYAN YOGANANDAN1, FRANK A. PINTAR1, SEAN M. LEW2, and RAJ D. RAO3 1
Department of Neurosurgery, Medical College of Wisconsin, Milwaukee, Wisconsin Department of Neurosurgery, Medical College of Wisconsin, Childrens Hospital of Wisconsin, Milwaukee, Wisconsin 3 Department of Orthopaedic Surgery, Medical College of Wisconsin, Milwaukee, Wisconsin 2
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Received 22 February 2013, Accepted 2 June 2013
Objective: Child dummies and injury criteria used in automotive crashworthiness environments are based on scaling from the adult and/or between children of different ages. Cartilage-to-bone ossification, spinal canal and joint developments of the spine, and strength attainments do not grow linearly from birth to maturity. Though this is known to medical professionals, age-based quantitative analyses are needed to accurately model the pediatric spine. The objective of this study was to quantify longitudinal growths of various regions of the first cervical vertebrae, responsible for transmitting the axial load from the base of the skull through the condyles to the neck/torso. Methods: Computed tomography (CT) images of 54 children from one day to 18 years of age were retrospectively used to determine the following geometrical properties: bilateral neurocentral synchondroses widths, the width of posterior synchondrosis, outer and inner anteroposterior and transverse diameters, spinal canal area, and depths of the anterior and posterior arches of the C1 vertebra. Both axial and sagittal CT images were used in the analysis. Sagittal images were used to quantify data for the anterior and posterior arches and axial images were used for all described cross-sectional parameters. Results: Geometrical properties were extracted and reported for the various parameters at 6 months; one year; 18 months; and 3, 6, and 10 years of age corresponding to the dummy family ages routinely used in motor vehicle crashworthiness research and other applications. The outer transverse diameter ranged from 4.97 to 7.08 cm; outer and inner antero-posterior diameters ranged from 2.99 to 4.18 and 2.19 to 3.03 mm; and spinal canal area ranged from 4.34 to 6.68 mm2. Other data are given in the body of the article. The growths of the first cervical vertebra quantified in terms of the above variables occurred nonlinearly with age and the degree of nonlinearity depended on the type of the geometrical parameter. Growths did not match with the simple scaling ratios based on the adult spine, used in different studies reported in the current literature. Conclusions: These early nonlinear and nonuniform age- and local geometry–specific variations should be considered in human finite element models for an accurate transfer of the external load from the atlas to the subaxial spine and to improve their fidelity and biomechanical capabilities. Keywords: children, biomechanics, safety, biofidelity, pediatric cervical spine, atlas
Introduction Six-month-old; one-year-old; 18-month-old; and 3-, 6-, and 10-year-old anthropomorphic test devices, also frequently referred to as dummies in automotive literature, are used in motor vehicle crashworthiness evaluations and for the understanding of injuries from fall-related events to children (Bertocci et al. 2003; Kapoor et al. 2008; Kleinberger, Sun, et al. 1998; Kleinberger, Yoganandan, and Kumaresan 1998; Yoganandan et al. 2001). The rationale for the development
This article not subject to U.S. copyright law Address correspondence to Narayan Yoganandan, PhD, Professor of Neurosurgery and Orthopaedic Surgery, Chair, Biomedical Engineering, Department of Neurosurgery, Medical College of Wisconsin, 9200 West Wisconsin Ave., Milwaukee, WI 53226. E-mail: [email protected]
of age-specific pediatric test devices for advancing safety to this population can be stated as follows. In general, the age group between newborn to one year can be skeletally represented by the presence of 3 primary ossification centers for the human spine. The group between one and 3 years of age can be represented by the fusion of the posterior or dorsal synchondrosis (Sherk and Parke 1989). The group between 3 and 6 years of age signifies the fusion of primary ossification centers (Yoganandan, Kumaresan, et al. 1998). Dummies have been developed by largely ignoring these patterns despite these recognitions; that is, their necks are essentially scaleddown versions from the adult, which have no ossification and growth issues. Anatomical textbooks provide descriptions and associated implications for physiological functions including head–neck stability issues of the growing child (Bailey 1952; Bird and Darling 2001; Clark 1998; Ganey and Ogden 2001; Weinstein 1994; Williams 1995; Yoganandan et al. 2008). However, descriptions are largely general in nature and
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288 quantifications on the development of vertebrae with specific reference to age groups used in pediatric dummies for motor vehicle applications are not their principal foci. The objectives of the present study are therefore to quantify longitudinal growths of various regions of the first cervical vertebra (also called the atlas), the component of the spine responsible for transmitting the axial load from the base of the skull through the condyles to the neck/torso. Specifically, properties are obtained for various geometrical parameters at 6 months; one year; 18 months; and 3, 6, and 10 years corresponding to the dummy family and the ratios of these properties are determined based on adult data. A brief description of the growth of this transitional vertebra is presented first, to enable the reader to place the current study in perspective. Briefly, the first vertebra is a unique bone in the entire human spinal column. It is formed from 3 primary ossification centers: one occurs in the anterior region and 2 occur bilaterally in the posterior neural arches. The former center develops several months following birth and the other 2 centers are present at the time of birth. The junction between the anterior and bilateral posterior centers is called the neurocentral synchondrosis. The 2 neural arch centers fuse or join dorsally at the posterior synchondrosis (Hinck et al. 1962; Tulsi 1971; Yousefzadeh et al. 1982). The presence of the 3 cartilaginous synchondrose junctions allows for the latitudinal and longitudinal growths of the cervical vertebra (Bick 1952; Carpenter 1961; Gooding and Neuhauser 1965; Haas 1939; Oda et al. 1988; Roaf 1960). The 2 growths contribute to the maturation processes of this bone and, as indicated earlier, age-specific developments of these regions corresponding to automotive dummy ages are not quantified. The bilateral facet bones of the vertebra contribute to the structural load transfer from the head to the subaxial spine, and the development of this region along with the other components contributes to the overall load carrying capacity of the vertebra. Because of the absence of the vertebral body and intervertebral discs at the rostral and caudal ends that act as anterior joints at each level, the growth of the ring in the latitudinal and longitudinal directions is important and studied in this retrospective investigation using human subject data across all child ages.
Methods All data were extracted from a pediatric level 1 trauma center in the state of Wisconsin. The retrospective research study was approved by the institutional review board of the authors (approval number HRRC 088-03, Children’s Hospital of Wisconsin). Head–neck radiographs and computed tomography (CT) scans were obtained as part of routine imaging evaluations of pediatric patients presenting to the emergency room. Most of these scans were obtained to rule out traumatic injuries. All images were initially reviewed by pediatric radiologists and followed by neurosurgeons and orthopedic surgeons. The cervical spines were determined to be negative for fracture/dislocation, epiphyseal injury, or other type of abnormality. Patients with demonstrable clinical history such as congenital or developmental disease, neoplastic growth,
Yoganandan et al. adverse neurological conditions, vertebral and muscular abnormalities, spine surgery, and scoliosis, which might affect normal vertebral growth, were excluded from the study. This was assessed using medical records. Conventional x-rays were obtained and a high-resolution CT scanner (Somatom Plus 4, Siemens, Erlangen, Germany) was used to obtain spine images according to established clinical protocols of the institution. Axial and sagittal reconstruction images obtained as a part of the screening protocol were used for the quantitative analyses. Sequential axial and sagittal images were used to determine the geometry of the C1 vertebra. The following geometrical measurements were obtained (Figure 1). Axial images were used to determine widths of the bilateral neurocentral synchondroses; the width of the posterior synchondrosis; outer and inner antero-posterior and transverse diameters; and spinal canal area. Depths of the anterior and posterior arches were obtained from sagittal images. All geometrical variables were expressed using mathematical functions across the entire age spectrum. Variations were defined as those with R2 greater than 60 percent for nonlinear age-related responses. The maturation magnitude was defined as the value of a parameter at the adult age, corresponding to 18 years, with the exception of the anterior and posterior synchondroses, which were defined at the youngest age. Parameters were extracted at 6 months; one year; 18 months; and 3, 6, and 10 years.
Results Retrospective data from 54 pediatric subjects with ages ranging from one day to 211 months were analyzed in the study. There were 39 boys and 15 girls in the subject population. Six measurements were repeated for 15 subjects by one researcher for intra-observer repeatability and all of these measurements were repeated for 15 random subjects by another researcher for interobserver reproducibility. Across all measures, coefficients of repeatability for intra- and interobserver studies were on average 4 and 6 percent and the coefficient of repeatability for the intra-observer reproducibility was an average of 2.3 percent less than interobserver reproducibility. In general, differing types of growth/maturation patterns were found for all geometric parameters considered in the study. The anterior neurocentral and posterior synchondroses coalesced at
Fig. 1. (Left) Axial view of an immature C1 vertebra illustrating the posterior and anterior synchondroses (PS and AS) shown as gaps and (right) vertebra from another subject demonstrating the various dimensions extracted in the present study from the axial view.
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The Human Child Cervical Spine 31 and 27 months. The linear regression fits for these parameters resulted in R2 of 0.8 and 0.6, respectively (Figure 2). These early bony growths represent the initial development of the C1 vertebra in the human cervical spine. The inner transverse diameter was invariant with increasing age, as identified by the very low R2 (0.1). In contrast, the mean outer and inner antero-posterior and outer transverse diameters, spinal canal area, and depths of the anterior and posterior arches showed logarithmic variations in the development process. The respective R2 values for these parameters are included (Figure 2). The maturation magnitudes of the 2 synchondroses, outer and inner antero-posterior and outer transverse diameters, spinal canal area, and depths of the anterior and posterior arches are shown (Figure 3). The P values were less than .0001 for all parameters with the following exceptions: the P values for the posterior synchondrosis and inner transverse diameter were .0045 and .0725, respectively. The percentages representing the development processes of the outer and inner antero-posterior diameters are shown in Figure 4, the outer transverse diameter in Figure 5, the depths of the anterior and posterior arches in Figure 6, and the spinal canal area in Figure 7, normalized with respect to the adult age group. The growths of the 2 antero-posterior diameters were such that their adult-based ratios ranged from 0.68 to 0.95 for the 6-month-old to the 10-year-old spines. These data for the transverse diameter ranged from 0.66 to 0.94, for the spinal canal area from 0.61 to 0.94, and for the vertical depths of the posterior and anterior arches from 0.53 to 0.92 and 0.48 to 0.91, respectively. The ossifications of the anterior and posterior synchondroses were such that their ratios (normalized with respect to zero years of age) decreased from 0.81 to 0.42 and 0.78 to 0.33 from 6 to 18 months of age (Figure 8).
Discussion As indicated in the Introduction, the aim of the study was to quantify various geometrical parameters of the C1 vertebra at 6 months; one year; 18 months; and 3, 6, and 10 years corresponding to the dummy family and determine the ratios
Fig. 2. R2 values from left to right: anterior and posterior synchondroses, outer transverse and inner and outer antero-posterior diameters, canal area, and anterior and posterior arch depths.
289
Fig. 3. Maturation magnitudes from left to right: anterior and posterior synchondroses, outer transverse and inner and outer antero-posterior diameters, spinal canal area, and anterior and posterior arch depths.
of these properties based on adult data. This study focused on the C1 because it is the first vertebra of the neck, the first load-bearing element from the base of the skull, and is unique in the entire vertebral column. Any axial load transmitted from the head or facial skeleton to the neck and torso always traverses through the C1 vertebra. This is true even when the external load is applied eccentrically on the head/face. Furthermore, vital structures are housed at the upper cervical spine (occipito-atlanto-axial complex) in the human. Because the mass of the head is disproportional to the neck structure, especially at younger ages, the anatomy of C1 plays a role in the mechanism of load transfer. The objectives were achieved by obtaining retrospective CT scans from pediatric subjects of various ages, from one day to 18 years of age. CT scans were selected due to their ability to show cross-sectional images, which is critical because the unique ring shape of the bone of the human cervical spine does not permit the use of appropriate views from x-rays (Ford
Fig. 4. Growth of the 2 antero-posterior diameters normalized with respect to the adult.
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290
Fig. 5. Ratios of the outer transverse diameters normalized with respect to the adult.
et al. 1982; Junewick et al. 2011). In addition, x-rays provide an integrated image of the spine only in the lateral and anteroposterior or postero-anterior projections (Ogden et al. 1994; Yoganandan, Pintar, et al. 1998). Although magnetic resonance imaging is another modality, it was not adopted because of practical limitations in obtaining scans, difficulties in extracting osseous details because the resolution and focus of the images are on soft tissues, and the existence of motion artifacts present in the very young. Furthermore, CT is a more standard clinical protocol than the other imaging modality in the Western world (AuYong and Piatt 2009). However, the limited sample size of 54 used in the present study was inadequate to differentiate between the sexes, and in order to fully include such variables it would be necessary to extend this line of research. Along the same vein, it would be necessary in the future to quantify the age-dependent ossification and development of bony regions of another unique vertebra, C2, which has 5 ossification centers in contrast to the 3 in the C1 vertebra (Ogden 1984). As indicated, the present retrospective study provided a snapshot of the pediatric subject vertebra at the time of CT
Fig. 6. Ratios of the depths of the 2 arches normalized with respect to the adult.
Yoganandan et al.
Fig. 7. Ratios of the spinal canal areas normalized with respect to the adult.
scanning. Consequently, ossifications and growth patterns of the bone for the same subject were not followed over time. Though this approach may not have revealed the specific agerelated patterns for the various measures on an individual subject basis, data are applicable because they were grouped into one ensemble. Furthermore, obtaining longitudinal CT scans for the entire 18-year period covered in the present study is not only time consuming and difficult to execute, but normal attrition in such an approach limits the usability of data at the end of the collection process. Recent recognition of the increased radiation exposure from CT scanning (for no direct medical reasons) and difficulties in obtaining institutional review board approvals are other constraints of such a methodology (Baumann et al. 2011; Brunetti et al. 2011; Tsalafoutas and Koukourakis 2010). Hence, the practical and feasible approach of retrospective analysis of emergency room patient scans was adopted in the present study. As can be appreciated from the relatively high R2 exceeding 0.6 in all but one case (Figure 2), baseline data obtained from this study are considered reliable for the different age groups.
Fig. 8. Ratios of the widths of the 2 synchondroses normalized with respect to the newborn. The anterior and posterior synchondroses close at approximately 31 and 27 months.
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The Human Child Cervical Spine
Fig. 9. Age-dependent ratios (reported in the literature; see text for details) of the total body mass, sitting height, neck mass, and neck circumference based on the adult.
It should be noted that the male dummy used for automotive applications represents a 45-year-old occupant. However, the present study considered the adult age to be 18 years. Because human spinal vertebrae reach adult size by this age, geometrical changes are not expected between 18 and 45 years. Another potential application of these geometric parameters corresponding to the specific age groups is their incorporation into stress analysis models. Finite element models can be used as a starting point for clinical applications and as an adjunct to dummy experiments such as sled tests to evaluate spinal internal responses for motor vehicle applications. Results from the present study are valuable for these advancements because current pediatric stress analysis–based finite element models lack anatomic fidelity and models do not exist for clinical applications (Kumaresan et al. 1997; Mizuno et al. 2005). This study focused on dummy-specific age groups to be relevant to occupant safety in motor vehicle environments and to aid in safety standards. For the most part, scaling factors and methods have been developed based on the adult (Kleinberger, Yoganandan, and Kumaresan 1998; Mertz et al. 1997; Schneider 1983; Snyder 1977; Weber and Lehman 1985; Yoganandan, Kumaresan, et al. 1998; Yoganandan et al. 2000). Recognizing the inconsistency in scale factors (Figure 9), in an early computational research study, agespecific human pediatric cervical spine models were created by geometrically scaling the adult spine to the one-, 3-, and 6-year-old sizes (Kumaresan et al. 2000). Briefly, the procedure consisted of increasing the size of the anatomically accurate adult model to 125, 150, and 175 percent, determining the biomechanical responses and then back-extrapolating the determined responses via regression to respective pediatric age sizes using scaling factors of 0.58, 0.62, and 0.66. The initial scaling-up process was necessary because shrinking the adult model to represent the respective child models posed computational instability issues. This approach disregarded the local geometrical and material properties of the spine. Another approach consisted of assigning differing material properties to the adult model without changing the anatomical geometry. The third approach combined the 2
291 scaling schema and results indicated the overriding influence of the anatomy and geometry on biomechanical responses (Kumaresan et al. 2000). The authors concluded that these scaling methods represent only a first step in the modeling process, which should be followed by additional anatomic and geometrical studies to obtain realistic responses. In a more recent study, a 3-year-old child finite element model was developed from the 50th percentile adult male Total Human Model for Safety and the neck scaling factor was set at 0.5 for the pediatric model (Iwamoto et al. 2002; Mizuno et al. 2005). As before, the model did not have the anatomical shape of pediatric vertebra and the authors concluded (similar to the earlier study discussed above) that more detailed modeling of child anatomical structures is needed. Using the age-specific outer anteroposterior diameter ratios with respect to the adult as a basis to compare with the dummy scale factors based on scaling from the adult neck circumference, the scaled dimension of the child would be off from 0.09 for the 6-month-old to 0.21 for the 6year-old (Figure 10), and this corresponds to a 15 to 32 percent change. The identified characteristic features of the growing spine for all dummy-specific age groups are valuable to relax the assumptions made in existing models in order to accurately delineate the age-specific responses of pediatric spines. Although the closures of the anterior and posterior synchondroses occurred very early, a finding paralleling qualitative anatomic textbooks, the rate of closure was different between the 2 regions of the bone. The growth of the cartilage to the bony components at the 6-month, one-year, and 18-month periods were such that the posterior closures were quicker than the anterior, and by 18 months of age approximately two fifths and one third of the anterior and posterior cartilage were converted to the bony component (Figure 8). It
Fig. 10. Age-dependent ratios of various geometrical parameters based on the adult. Black bars to the right in each age group show the ratio based on the dummy scaling factor used in automotive studies. Legend from left to right: outer antero-posterior diameters (OAD) and outer transverse diameter (OTD); dummy scaling refers to scaling factor based on adult neck circumference.
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292 is therefore important to ensure that the younger age human cervical spine models include appropriate bony and cartilage geometrical features for realistic stress analysis outputs. For the 2 younger groups (6 months and one year), cartilage effects are more important and should be separately modeled with their own constitutive laws. In general, pediatric injuries involve more soft tissues than the adult spine because the growing bone is shielded by cartilage and other soft tissues. Because of differences in the material properties between the cartilage and bone, simulating the cartilage in pediatric spines alters the kinematics. Specifically, increases in the flexibility of the spine due to the presence of the cartilage affect local ligament–bone responses. Such realistic simulations provide insights into injuries such as atlanto-occipital and atlano-axial dislocations wherein fractures do not always accompany ligamentous and unstable/serious injuries. The inner transverse diameter represents the lateral-tolateral clear distance between the tubercles that divide the vertebral foramen to accommodate the dens anteriorly and cord posteriorly. The age-invariant pattern of the diameter indicates that human cervical spine models should have the same dimension regardless of age, from 6 months to 18 years of age. This unique feature coupled with the early age-specific closure (before 3 years), as discussed above, constitute the necessary anatomical intricacies for incorporation into younger age cervical spine models. In contrast, all other dimensions matured nonlinearly with increasing age. The outer and inner antero-posterior (Figure 4) and outer transverse (Figure 5) diameters developed almost uniformly with adult-based ratios ranging from 0.7 to 0.9, and the inner diameter matured somewhat earlier than the outer antero-posterior counterpart. In contrast, the depths of the anterior and posterior arches (Figure 6) showed a slower growth trend, ranging from 0.5 to 0.9 of adult values for different age groups. These results suggest that the latitudinal geometry matures earlier than the longitudinal geometry. From a cross-sectional perspective, because the maturation process begins early—that is, responding with greater diameters contributing to greater areas and hence volume—the load-carrying capacity of this vertebra increases rapidly. This may lead to an early stable upper cervical spine, and these results parallel clinical and biomechanical studies wherein cross-sectional geometry has been considered to be an important factor in segmental and overall cervical column stability (Denis 1983; Yoganandan et al. 2012). A recent study showed that the increased segmental support area and interfacet width, similar measures of outer and inner latitudinal diameters, contribute to cervical spine stability and strength (Stemper et al. 2008). From these perspectives, the aforementioned early, nonlinear, and nonuniform age- and local geometry–specific variations should be considered in human finite element models for an accurate transfer of the external load from the C1 vertebra to the subaxial spine and to improve their fidelity and biomechanical capabilities. The above discussion on the latitudinal and longitudinal growth processes is applicable in general to all vertebrae, although the times of attainments of the maturation may differ depending on the spinal level/region. For example, C2 has 5 ossification centers in contrast to the 3 centers present in all vertebrae, again due to its own characteristic developmen-
Yoganandan et al. Table 1. Summary of parameters as a function of dummy-specific age Parameter Anterior synchondrosis Posterior synchondrosis Outer antero-posterior diameter Inner antero-posterior diameter Outer transverse diameter Inner transverse diameter Spinal canal area Anterior arch depth Posterior arch depth
6 Months 1 Year 1.5 Years 3 Years 6 Years 10 Years Adult 0.75
0.57
0.39
0.00
0.00
0.00
0.00
0.67
0.48
0.28
0.00
0.00
0.00
0.00
2.99
3.27
3.43
3.70
3.98
4.18
4.42
2.19
2.39
2.50
2.69
2.89
3.03
3.20
4.97
5.46
5.74
6.23
6.72
7.08
7.49
2.32
2.32
2.32
2.29
2.24
2.18
2.05
4.34 0.47
4.88 0.57
5.20 0.63
5.74 0.72
6.28 0.82
6.68 0.89
7.13 0.98
0.56
0.66
0.72
0.82
0.92
0.99
1.07
All measurements in cm, except area (in square cm).
tal anatomy. From this perspective, it would be necessary to conduct a similar analysis and quantify growth patterns. In principle, the progress of the ossification process is true for other vertebrae. The number of ossification centers is the same in C1 and other typical vertebra, except the axis (C2), which has 5 centers. From this perspective, it would be necessary to quantify the growth Table 1 of C2 separately. Along the same vein, because the atlas is also unique in its formation and geometry, it would be prudent to at least follow a similar process of quantification to another typical bone, C3 to C7. In other words, quantifications of C2 and one of the C3 through C7 vertebra are needed to more accurately capture the developmental process of the human cervical spine. Though more subjects analyzed for C1 will assist in testing differences in the geometrical parameters between factors such as males versus females, as a first step, the authors recommend similar studies first with other pediatric vertebrae.
Acknowledgments This study was supported in part by the Department of Veterans Affairs Medical Research and Department of Neurosurgery, Medical College of Wisconsin, Milwaukee, Wisconsin.
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