Anterior cranial-base time-related changes: A systematic review

Introduction

The anterior cranial base has long been considered a stable reference structure for superimposing radiographs. However, some studies have questioned its stability. Therefore, the purposes of this systematic review were to give an overview of the studies evaluating growth and development of the anterior cranial base, assess their methodologic quality, and evaluate their validity and accuracy.

Methods

Medline, Embase, and Google Scholar were searched without limitations up to June 2013. Additionally, the bibliographies of the finally selected articles were hand searched to identify any relevant publications that were not identified before. The lowest levels of evidence accepted for inclusion were cohort and cross-sectional studies.

Results

A total of 11 articles met all inclusion criteria. They were published between 1955 and 2009. The sample sizes of these studies ranged from 28 to 464 subjects. Their methodologic quality ranged from moderate to low.

Conclusions

Sella turcica remodels backward and downward, and nasion moves forward because of the increase in size of the frontal sinus. These events lead to a continuous increase in the length of the cranial base until adulthood. The presphenoid and cribriform plate regions can be considered stable after age 7, making them the best cranial-base superimposition areas.

An understanding of craniofacial growth is crucial for improved diagnosis, treatment planning, outcome evaluation, and long-term stability. Historically, orthodontists have used the cranial-base structures as reference structures to evaluate craniofacial growth. The anterior cranial base is considered to have completed its most significant growth before other facial skeletal structures. Hence, the anterior cranial base has long been considered a stable craniofacial structure to be used for cephalometric superimpositions during the usual orthodontic treatment age range.

The cranial base is initially formed in cartilage, with ossification centers appearing early in embryonic life; with time, they progressively replace the cartilage with bone. However, some cartilaginous growth centers called synchondroses remain active between ossified areas and mature at different times of life. Bastir et al stated that the earliest structure to mature in shape and size in the skull is the midline cranial base (at 7.7 years of age). However, this has been recently questioned. Malta et al found that the anterior cranial base is not stable in size and grows during all pubertal phases (CS1 to CS6 of the cervical maturation stages). They reported that the anterior cranial-base length (sella to nasion) increases until early adulthood.

Various methods have been described to evaluate craniofacial growth. Craniometry was the first measurement approach for evaluating growth, used since the 15th century. The advantage of this technique is that precise measurements can be made on dry skulls, but the limitation is that all the growth data are cross-sectional. Anthropometry was then used as the gold standard because it can follow growth directly on each subject. Despite its accuracy, however, obtaining growth measurements through direct measurements is difficult because it is time-consuming and requires patient compliance to remain still for a long time. Early in the 1900s, serial photographs started to be used to assess facial growth. However, they only show trends of growth rate and direction, and they lack accuracy for some measurements. Later during the last century, the metallic implant radiography method provided new information about the growth pattern, but the disadvantage was that it required placing implants on the subjects; this is no longer considered ethical. Vital staining methods were also used in experimental animals to evaluate growth, but because of their invasiveness, they have only been used in humans to diagnose areas of rapid bone remodeling.

Soon after the invention of the technique of lateral cephalometric x-rays in the 1930s, this became the most common way to evaluate facial growth among orthodontists. The disadvantage of this imaging technique is that 3-dimensional (3D) structures are represented in 2 dimensions. Several morphometric tools such as thin-plate spline analysis, elliptic Fourier analysis, finite element analysis, and tensor and shape coordinate analysis have been applied to 2-dimensional cephalometric comparisons. These methods have allowed for visualization of morphologic changes without the need for typical reference structures.

In the late 1990s, the 3D digital imaging technique was introduced. This provides comprehensive information regarding anatomic relationships and eliminates some limitations encountered when studying 2-dimensional images. Laser surface scanning and 3D stereophotogrammetry methods are also the results of recent technologic advancements in 3D imaging; however, they usually apply only in 3D facial surface scanning.

As can be perceived from this introduction, multiple methods have been used through the years to analyze craniofacial changes. Even though the anterior cranial base has been considered stable and used as the reference structure for superimposing radiographs, this has recently been questioned. Because the use of the anterior cranial base as a reference structure has paramount importance in orthodontics, it would be extremely useful to comprehensively analyze the evidence to question its stability. Therefore, the purposes of this systematic review were to give an overview of the studies evaluating growth and development of the anterior cranial base, assess their methodologic quality, and evaluate their validity and accuracy.

Material and methods

This systematic review was reported using the PRISMA checklist as a template.

No review protocol or systematic review registration was considered.

In phase 1, only the titles and abstracts collected from the electronic database searches were considered. Articles that assessed craniofacial growth or analyzed treatment outcome but had a control group without treatment were considered. No language limitations were applied. Studies assessing fetal growth with photographs only or assessing frontal x-rays only were excluded. Animal studies were also excluded.

In phase 2, in which copies of full articles were reviewed from those selected in phase 1, some articles were excluded if they did not specifically evaluate cranial-base growth, or if they were reviews or case reports. Ultimately, all included studies must have assessed the growth and development of the anterior cranial-base structures.

With the assistance of a senior health-sciences librarian, we conducted a computerized systematic search in 2 electronic databases. Medline (via OvidSP) and Embase (via OvidSP) were searched from their earliest records until June 15, 2013. The bibliographies of the selected articles were also hand searched for additional relevant studies that might have been missed in the electronic searches. In addition, a limited gray literature search was conducted with Google Scholar.

Specific medical subject headings and keywords were used in the search strategy of Medline ( Table I ). The search strategy for the Embase database was derived from the former and was modified appropriately ( Appendix 1 ).

Table I
Search strategy for MEDLINE via OVIDSP (1950 to the present)
Search group Medical subject heading (MeSH) or key word
1 Maxillofacial development/OR growth/
2 *skull/or ethmoid bone/or exp facial bones/or exp skull base/or expsphenoid bone/OR exp *mandible/or *maxilla/OR cranial base.mp
3 Cephalometry/is, mt, st, td, ut [Instrumentation, Methods, Standards, Trends, Utilization] OR exp Cone-Beam Computed Tomography/is, mt, st, td, ut [Instrumentation, Methods, Standards, Trends, Utilization] OR exp Imaging, Three-Dimensional/is, mt, st, td, ut [Instrumentation, Methods, Standards, Trends, Utilization] OR superimpos*.mp. [mp = title, abstract, original title, name of substance word, subject heading word, keyword heading word, protocol supplementary concept, rare disease supplementary concept, unique identifier] OR exp Methods/is, mt, st, ut [Instrumentation, Methods, Standards, Utilization]
4 1 AND 2 AND 3

Limitation: human subjects.

In both steps of the review process, 2 reviewers (M.A. and C.P.L.) independently reviewed titles and abstracts according to the inclusion and exclusion criteria noted above. Disagreements between the 2 reviewers were resolved through discussion until consensus was achieved.

From the articles that met the inclusion criteria, the same 2 reviewers extracted the data independently in duplicate. They compared the extracted data and resolved discrepancies by reevaluating the literature until consensus was achieved.

The data from the studies that met the inclusion criteria were study design, population characteristics (sample size, sex, age), method used to analyze cranial-base growth, results (eg, change in percentage), and reliability and validity of the reported method ( Table II ).

Table II
Summary of characteristics of included articles
Article Study design Sample size and sex Age Method Growth percentage change Results Validity/reliability
1 Malta et al (2009) Longitudinal 36
F = 21
M = 15
  • Mean age at T1 = 10.4 y (SD, 0.98)

  • T1 Prepeak (CS1 & CS2)

  • T2 Peak (CS3 & CS4)

  • T3 Postpeak (CS5 & CS6)

  • Lateral cephalometry

  • Linear measurements at T1, T2, T3

  • S-Ba, S-N, Ba-N, CC- Ba, CC-N, FC-Po

  • S-N:

  • T1-T2: 3.5% increase ( P < 0.001)

  • T2-T3: 4.0% increase ( P < 0.001)

  • T1-T3: 7.1% increase ( P < 0.001)

  • The cranial base grew during all pubertal phases.

  • The largest growth is during the interval between the prepeak and peak phases, decreasing in the postpeak period.

  • These data show that cranial-base growth occurs until adulthood.

  • Interreliability determined for CVM, tracings and landmarks.

  • Intrareliability of measurements determined, no measurement error reported.

  • ICC reported more than 0.95 (0.946-0.998).

2 Jiang et al (2007) Longitudinal 28
F = 15
M = 13
Annual records from 13-18 y
  • Lateral cephalometry

  • Modified mesh diagram analysis

  • Scaled average 18 y diagram superimposed on the 13-y average diagram

NA
  • The anterior cranial base continued to grow and the length increased during the study period.

  • In females, most structures increased in size uniformly across 6 y of growth. There is disproportionately enhanced growth of the anterior cranial base upward in males only.

  • Reliability determined (does not mention intra or inter)

  • Measurement error: no more than 0.04 (Dahlberg’s formula)

3 Franchi et al (2007) Longitudinal 34
F = 10
M = 24
  • T1 Prepubertal CS1 Mean age: 10 y

  • T2:Postpubertal SC6

  • Lateral cephalometry

  • Thin plate spline analysis registered at Ba, S, Na

  • S-N:

  • T1-T2: 7.1% increase ( P < 0.05)

  • The longitudinal changes in the shape of the cranial base from T1-T2 were not significant.

  • On the other hand, differences in (centroid) size changes were significant.

  • Intrareliability determined for landmarks and CVM.

  • Landmarks measured twice and the average was taken. No values reported.

4 Lewis & Roche (1988) Longitudinal 20
F = 12
M = 8
  • T1: 17 or 18 y

  • – 8 succeeding x- rays for everyone

  • 1 x-ray between 40 and 50 y

  • Lateral cephalometry

  • S-N, Ba-N, Ba-S measured

NA
  • The mean age at which the maximum lengths were identified ranged from 29 to 39 y among the various dimensions.

  • There were small but real increments of growth after 17 or 18 y.

  • None

5 Melsen (1974) Cross-sectional 126
F = 50
M = 76
Ages: 0-20 y
  • Autopsy tissue blocks

  • Conventional histologic and macroradiography

  • Categorized bone surfaces based on growth activity

  • 1. apposition

  • 2. resorption

  • 3. inactivity

NA
  • The cribriform plate was stable after the age of 4.

  • Jugum sphenoidale (t-plane) showed appositional growth up to 4-5 y and again in the prepubertal period.

  • Growth of both sphenoethmoidale and frontoethmoid synchondroses completed by age 7.

  • Tuberculum sella showed variable growth pattern until age 18.

  • Anterior wall of sella was stable after age 5-6 y.

  • Posterior wall of sella showed resorption until 14-17 y (M & F)

  • Sella moves downward and backward.

  • The anterior part of sella was the most stable in almost all subjects over 5 y

  • Changes in sella turcica were due to resorption activity in the lower half of the posterior wall and the floor to some degree.

  • Reliability: 2 sets of double registrations, a repeated blind registration of the first set of sections. Magnitude of error due to inconsistency in the registration procedures was of order of 10%. No other values reported.

6 Steuer (1972) Longitudinal 54
F = 31
M = 23
  • Ages: 5-11 y

  • 40% of cases 8-10 y

  • Annual x-rays

  • 5 patients had 5-y interval records, one 7 y, and one 8 y

  • Total 274

  • Lateral cephalometry

  • Tracing from dorsum sella to planum spheniodale was divided into 7 segments

  • At least 3 segments should be congruent for valid superimposition.

NA
  • 95% of comparisons up to 5 y apart had 3 or more segments congruent, which indicates that superimposition on the middle outline of sphenoidal portion of cranial base is acceptable during the usual orthodontic age range, but generally the trend is toward less congruence with time because of slight craniofacial growth changes.

  • Deepening of the hypophysial fossa was noted in the recall group of 7 subjects who had cephalograms taken a number of years after the last one.

  • None

7 Knott (1971) Longitudinal 66
F = 19
M = 23
  • Measurements at ages T1: 6; T2: 9; T3: 12; and T4: early adulthood

  • Mean ages: males, 25.1 y; females, 25.8 y

  • 2/3 of subjects at age 15 y

  • Lateral cephalometry (Norma lateralis roentgenograms)

  • Linear measurements: N-F, F-W, W-P, P-O

  • Angular measurements: NPO, FPO, WPO

  • NF + FW + WP(N-S): T1-T3 (6-12): 6.1% increase (no P values) T3-T4 (12-adult): 5.1% increase (no P values)

  • Frontal segment NF: T1-T4: 3.3% increase ( P < 0.01)

  • From age 6-12 y for each sex, the frontal segment increased in average size by 2.8 mm, the ethmoid segment by 1.0 mm, no change in average size for the presphenoid dimension.

  • Downward movement of nasion is found in measurements from the line extended through the frontal point and the sphenoid wing point and also relative to the line through the F and P points.The increase in NPW angle indicates upward movement of nasion realtive to presphenoid segment.

  • Intrareliability of measurements determined in instances greater than 0.2 mm (average obtained).

8 Melsen (1969) Cross-sectional 132
Dry skulls sex: not specified
  • 48: All deciduous dentitions erupted

  • 64: mixed dentition

  • 20: 8s fully erupted

  • Lateral cephalometry of the skull

  • 22 linear measurements & 2 angular

  • NS:

  • Primary 8s erupted: 10% increase

  • Mixed-8s erupted: 2.3% increase

  • S-S′:(depth of sella turcica):

  • Primary 8s erupted: 2.3% increase (no P values)

  • The reference point sella on average was moved 2 mm downward and backward in relation to the tuberculum sella from the full deciduous dentition stage to the stage when canines and premolars are erupting, which indicates eccentric growth of sella turcica.

  • Intrareliability: measurements repeated on 10 skulls from different ages. No systematic error found. No values reported.

9 Stramrud (1959) Cross-sectional 464, all males
  • Subjects from 3-15 y (average 30 subjects in each age group) and adults from 19 -25 y (34 subjects)

  • Lateral roentgenograms

  • 7 linear measurements and 9 angular measurements

NA
  • The anterior cranial fossa (N-S minus the thickness of the frontal bone) increases in length markedly until age 7 and then there is a slight increase until puberty.

  • The frontal bone thickness increases from age 3 to adulthood.

  • Nasion tends to move downward during growth when the internal cranial base flattens out and upward when a deflection of the internal cranial base takes place.

  • None (systematic error mentioned in some tables)

10 Ford (1958) Cross-sectional 71
Sex notspecified
Age: 0 to over 20 y
  • Dry skulls (measured by divider and ruler)

  • 7 linear measurements

NA
  • Pituitary point—nasion dimension continues to grow after eruption of permanent first molars (6-8 y)

  • The cribriform plate completes its growth by the age of 2 years

  • The sphenomesethmoid synchondrosis ceases growth completely by age 7

  • Increase in the thickness of the frontal bone accounts for increase in the pituitary point-nasion diameter after eruption of the permanent first molars. This is associated with the increase in the size of the frontal sinus.

  • None

11 Bjork (1955) Longitudinal 243, all males T1: 12 y
T2: 20 y
  • Lateral cephalometry

  • Anterior cranial base structural superimposition technique

NS:T1-T2: 6.6% increase (no P value)
  • The cranial base is elongated due to apposition at the glabella region

  • Eccentric remodeling of sella turcica during growth results in displacement of the midpoint (S) backward and downward or upward

  • In 90% of cases, only a small change could be detected relative to the position of the contour of the ethmoid plate relative to N-S line.

  • None

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Apr 6, 2017 | Posted by in Orthodontics | Comments Off on Anterior cranial-base time-related changes: A systematic review
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