Posterior cranial base natural growth and development: A systematic review
ABSTRACT
Objective:
To provide a synthesis of the published studies evaluating the natural growth and development of the human posterior cranial base (S-Ba).
Materials and Methods:
The search was performed on MEDLINE, Embase, PubMed, and all EBM Reviews electronic databases. In addition, reference lists of the included studies were hand-searched. Articles were included if they analyzed posterior cranial-base growth in humans specifically. Study selection, data extraction, and risk of bias assessment were completed in duplicate. A meta-analysis was not justified.
Results:
Finally, 23 published studies were selected: 5 cross-sectional and 18 cohort studies. Articles were published between 1955 and 2015, and all were published in English. The sample sizes varied between 20 and 397 individuals and consisted of craniofacial measurements from either living or deceased human skulls. Validity of the measurements was not determined in any of the studies, while six papers reported some form of reliability assessment. All the articles included multiple time points within the same population or data from multiple age groups. Growth of S-Ba was generally agreed to be from spheno-occipital synchondrosis growth. Basion displaced downward and backward and sella turcica moved downward and backward during craniofacial growth. Timing of cessation of S-Ba growth was not conclusive due to limited identified evidence.
Conclusions:
Current evidence suggests that S-Ba is not totally stable, as its dimensions change throughout craniofacial growth and a minor dimensional change is observed even in late adulthood.
INTRODUCTION
Understanding craniofacial growth and development is important for accurate diagnosis, treatment planning and posttreatment evaluation of orthodontic cases. Paramount to this is knowledge of the cranial base growth and development, since it is the foundation upon which the remaining facial structures develop.1–4 Various methods to assess and analyze craniofacial growth and development have been described in the literature. These include craniometry, anthropometry, cephalometric x-rays, and, most recently, three-dimensional (3-D) cone-beam computed tomography (CBCT).5,6
The cranial base is said to reach 87% of its growth by 2 years and 98% by 15 years of age.3 Around age 5, the cranial base has completed 90% of its growth and, from then on, can be considered relatively stable as the remaining 10% of change occurs in the next 10 years.4 It is known that maturation of different components of the craniofacial skeleton reach their completion at different time points.7 It is also considered that some components of the anterior cranial base are the earliest structures in the skull to reach maturity in shape and size at about 7–8 years.8
A previous report on the posterior cranial base (S-Ba) changes showed that its length and angulation are differentially affected in different vertical facial types.3 It was also shown that, within the S-Ba, the spheno-occipital synchondrosis is a cornerstone structure for growth of the cranial vault as well as craniofacial growth in general.9 The spheno-occipital synchondrosis connects the occipital and sphenoid bones and is located anterior and superior to the foramen magnum and below the pituitary fossa.10 To date, there are numerous reports that have studied growth of S-Ba and the spheno-occipital synchondrosis,11–14 but there is no certainty as for when it completes its fusion and consequently stops growing.
As has been stated, the cranial base influences the growth and development of the remaining craniofacial structures. Knowledge of its stability is beneficial for proper diagnosis and treatment planning by orthodontists because what happens at the cranial base affects the position, size, angles, and structure of the overlying face.3 A previous systematic review synthesized the changes in the anterior cranial base,15 but did not consider changes in the S-Ba. As such, this systematic review aimed to provide a synthesis of the published studies evaluating the growth and development of S-Ba.
MATERIALS AND METHODS
Protocol and Registration
Neither systematic review registration nor a review protocol was completed.
Information Sources
With the assistance of a health sciences librarian, a computerized systematic search was performed up to July 17, 2016, in the following electronic databases: MEDLINE (Via OvidSP), Embase (via Ovid SP), PubMed, and all EBM Reviews databases (Cochrane Database of Systematic Reviews, Database of Abstracts of Reviews of Effects, and Cochrane Methodology Register). Using Google Scholar, a limited grey literature search was also performed, which consisted of key word searches with the first 15 Web pages of hits reviewed. The bibliographies of the finally selected articles were also hand searched for additional studies that may have been missed during the database searches. Related articles were also searched from the suggested article menu when an article was searched online. Additional articles were added as suggested by an expert in the field. No language limitations were applied, but the searches were limited to craniofacial studies in humans.
Searches
When performing the above searches, specific subject headings and keywords were used first in MEDLINE (Table 1). The additional searches were modifications from this search, directed for the specific database.
Study Selection
Two reviewers independently reviewed the articles in both steps of the review process based on the decided inclusion and exclusion criteria. Disagreements in article selection were resolved via discussion; those that could not be resolved were brought to another reviewer for consultation.
The phase 1 selection process involved assessing titles and abstracts. Appropriate articles were considered if their abstracts assessed craniofacial growth or analyzed treatment outcome, but had a control group without treatment. Studies assessing fetal growth only or including syndromic patients were excluded.
Phase 2 involved obtaining full copies of the articles selected in phase 1. In this stage, articles were excluded if they did not specifically evaluate S-Ba growth (Appendix 1). Articles were also rejected if they were case reports or reviews. The articles selected to continue assessed the growth and development of S-Ba and surrounding structures.
Data Extraction
Data were extracted from the selected articles on the following items: study design, population characteristics (sample size, sex, age), method used to analyze cranial base growth, results (linear and angulation changes, shape change), and reliability and validity of reported methods (Table 2). The primary outcomes were dimensional changes (quantified as continuous variables) in S-Ba and surrounding structures during active craniofacial growth and development.
Risk of Bias Assessment
All selected studies were assessed for potential risk of bias using a nonvalidated quality assessment tool implemented in a previous systematic review15 (Table 3). Two reviewers completed this process separately, and articles with a score of 50% or less were categorized as poor or low quality (high risk of bias). Good quality articles had scores over 50% and up to 75% (moderate risk of bias). Any article receiving a score greater than 75% was considered to have high or excellent quality (low risk of bias).
RESULTS
Study Selection
The selection process at each stage of this systematic review is represented in Figure 1. Twenty-three articles satisfied the selection criteria and were included in this systematic review.
Citation: The Angle Orthodontist 87, 6; 10.2319/032717-218.1
Study Characteristics
A summary of the data and results of the selected articles are shown in Table 2. Of the 23 articles, 5 were cross-sectional in design,13,16–19 while the remaining 18 were cohort studies.2,20–36 Samples consisted of craniofacial measurements from living or deceased postnatal human skulls. Validity of the measurements was not determined in any of the studies, while only six reported some form of reliability assessment. All the articles measured multiple time points within the same population or data from multiple age groups.
Risk of Bias Within Studies
Table 4 summarizes results of the risk of bias assessment. The methodological quality of the studies ranged from poor to excellent. The most common weaknesses were failure to validate the accuracy of the findings (none of the studies reported this), insufficient statistical reporting, and failure to calculate or justify sample size.
Results of Individual Studies
Upon review of the pertinent information from the selected articles, we noted that there was a change in all S-Ba linear measurements (from Sella [S] to Basion [Ba]) among the various age groups studied.16,20–22,25,29,34–36 In addition, there were variable changes in length and angulation among and between all stages of development.13,27
Knott observed that the largest absolute change in linear dimension over a 9-year period, from ages 6 to 15, occurred in the postsphenoid region with an annual average of 1 mm.35 During a similar age interval, other studies also showed similar age-related changes in S-Ba.31,32 Henneberke and Prahl-Anderson also reported constant growth velocity for S-Ba over 7 years from age 7 to 14 at 1 mm/y and 0.9 mm/y for boys and girls, respectively; the average length of S-Ba was 2.5 mm larger in boys than in girls.24 On the other hand, other studies showed slightly different growth rates in different age groups and suggested that cranial base growth was closely related to skeletal age.20,27 Malta et al. showed that the greatest amount of growth was 2.8 mm from time 1 to time 2, which correlated with CS1/2 change in growth to CS3/4.27
Five studies showed size and growth differences between males and females as the cranial base dimensions increased,24,25,28,32,36 whereas the other three studies indicated no difference according to sex.26,27,31
Two studies reported changes in S-Ba length in adulthood.22,26 Bishara observed a significant decrease in the cranial base angle (NSO) and increase in cranial base length from age 26 to 46 years.22 In a group of adults ranging between the ages of 17 and 50 years, Lewis and Roche reported maximum values for S-Ba length at age 34.5 years in men and 35.0 years in women, with a growth rate of 0.3 mm/y in men and 0.2 mm/y in women.26
Growth directions of S-Ba were reported. Downward and backward displacement of basion was observed in one study,21 which corresponded with the downward and slightly backward movement of the occipital condylar point,35 downward growth of the clivus,28 as well as downward and backward growth of sella turcica that was reported in another study.13
Changes in the cranial base angulation were also noted. Bjork reported that the cranial base angle gradually bent throughout childhood up to about 10 years, at which point the cranial base reached its final shape and the cranial base angle remained relatively stable.2,30,32 Conversely, Bishara,22 Knott,36 and Lewis and Roche26 reported a slight decrease with age during adulthood.
A meta-analysis was not feasible because the methodologies of the selected articles were too heterogeneous.
DISCUSSION
This systematic review aimed to analyze published studies that evaluated growth of S-Ba and to evaluate their methodological quality. The results indicated that S-Ba is not a stable structure during craniofacial growth, and changes in S-Ba are primarily due to growth activity at the spheno-occipital synchondrosis, as well as sutural growth (eg, occipitomastoid changes) and cortical drift, in which bone is resorbed and deposited along the superior and inferior surfaces of the basicranium.2,13,14 With no definitive agreement on timing of the cessation of growth and closure of the spheno-occipital synchondrosis,13,14 S-Ba growth was reported to continue to grow even by small increments into adulthood and beyond.22,26
Proportional growth was reported20,25; differential growth rates were also seen. The more significant differential growth rates tended to correlate with pubertal growth spurts and growth potential.16,20,27,28 A calculated length change over a 9-year period (ages 6–15) was shown.35 All these studies supported this relationship between S-Ba length increase with activity of the spheno-occipital synchondrosis, since their study periods took place before the estimated closure of the synchondrosis at about age 11–18, based on laminagraphy, autopsy, and serial sections.13,14,34 Bjork showed dorsal elongation of the cranial base due to endochondral growth at the clivus.2
In reference to direction of growth change, basion was shown to move backward and downward,2,21 with an additional point measured in the general area of basion, occipital condyle point (Bolton), also showing downward and backward movement.35 The anterior reference point for S-Ba, sella, was shown to move down and back as well13,15 (Figure 2). Although both basion and sella were displaced in the same direction, these changes seemed to be due to different mechanisms. Movement of basion can be attributed to synchondrosis growth, whereas movement of sella can be attributed to eccentric growth of the sella turcica which remains stable at its anterior wall after around age 7. Intrinsic growth of sella turcica was also shown in a previous systematic review by Afrand et al.15 As reported by Enlow, development of the endocranium also occurs by deposition on the outside and resorption from the inside, also referred to as cortical drift.7 This can also explain small changes in location of landmarks from longitudinal cephalograms. Bjork also reported parallel lowering of the foramen magnum.2
Citation: The Angle Orthodontist 87, 6; 10.2319/032717-218.1
Angulation changes of the cranial base showed mixed results. Numerous investigators have attempted to correlate cranial base angle with facial type but, in this systematic review, an attempt was made to address solely changes due to growth without analyzing the impact on facial characteristics. The longitudinal study by Ohtsuki et al. showed decreases in S-N-Ba angle up to age 18.34 In contrast, Phelan et al. showed that there was no change in cranial base angle measured as SNBa.30 This was also supported by Thordarson et al., who showed no difference in cranial base flexure from age 6 to 16 years.31 In a longitudinal study by Wilhelm et al., there was no difference reported in cranial base angle between different facial classifications, specifically Class I and Class II.3,34 In one of the studies by Knott, she concluded that the decrease in WPO angle (which was defined as the angle between the postsphenoid line from P to O and the presphenoid line from W to P) and increase in postsphenoid length corresponded to the movement of the occipital condyle point. She also concluded that angular changes within individuals were small and that statistically insignificant changes were present.35
When comparing males with females, again we found conflicting data for the amount and rate of growth. Ursi et al. reported no differences in S-Ba length until age 16, when males had larger values and continued to show evidence of growth.32 In the report by Thordarson et al., no differences were shown between males and females, even as S-Ba lengthened.31 When comparing male and female longitudinal growth data, Knott showed an increase in postsphenoid length before the age of 6 years and no differences between sexes, but after the age of 12, males showed greater length change.36 The longitudinal study by Lewis and Roche, which looked at adults up to the age of 50, showed a difference between males and females for maximal growth rate and maximal length of S-Ba. Although these values were small, they still show the potential for dimensional change in the S-Ba region into adulthood.26 Overall, the present findings suggest that age-related changes in the craniofacial complex do not stop with the onset of adulthood, but continue, albeit at a significantly slower rate, throughout adult life. However, these changes tended to be of small magnitude, so that clinical relevance is somewhat limited and generally would not significantly influence orthodontic treatment planning.
Limitations
The use of a nonvalidated assessment tool15 has its own drawbacks but, with the absence of one validated tool that clearly applied to the type of studies likely to be included, this was inevitable.
Changes in growth for all studies were reported in millimeters or degrees. Ideally, growth should be reported as a percentage to convey an idea of how significant the changes were at any given age. This would also be important when different overall craniofacial sizes were considered.
For assessing growth, long-term longitudinal studies are the best option. Ideal growth studies would follow a large population and obtain records for many years with multiple time points at consistent time intervals. The selected articles varied greatly with regard to the age range studied, developmental stage, and data collection technique and analysis.
In addition, 10 of the 23 selected articles studied subjects from well-known growth studies conducted in North America during the 1930s–1970s. Although they were the best available sample, the same subjects may have been used in multiple studies.
Long-term aging studies that include late adulthood are inherently difficult to conduct, and, as a result, have a number of limitations such as wide variation in subjects' ages, different time spans between examination intervals, and particularly inclusion of 17–18-year-old subjects for whom later adolescent growth was still possible.22,26
In the past, two-dimensional lateral cephalometric radiographs were the most commonly used technique to evaluate growth of the cranial base. Measurements in 3-D would provide more accurate information on growth changes in the cranial base as a whole. No 3-D CBCT studies have yet been published on the growth of S-Ba.
CONCLUSIONS
Based on the identified published evidence and considering the stated limitations,
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A significant amount of growth in S-Ba was observed throughout the growth period. Even after pubertal growth had ceased at around 17–18 years, S-Ba was not yet 100% stable and dimensional changes continued into late adulthood, although at a slow rate.
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Growth of S-Ba was generally agreed to be from spheno-occipital synchondrosis growth. Change in length measured from sella to basion was most evident as S-Ba grew.
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Basion displaced downward and backward during craniofacial growth.
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Sella turcica moved downward and backward during craniofacial growth.
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The change in cranial base angle (N-S-Ba) with age was inconclusive.
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Angulation changes could not be consistently identified among different facial types or malocclusions.
Flow diagram of the study selection.
Diagram illustrating general movement of the posterior cranial base.
Contributor Notes