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Journal of Orthodontics, Vol. 36, No. 4, 229-235, December 2009 doi:10.1179/14653120723256
© 2009 British Orthodontic Society
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Scientific Section

Quantification of cranial base growth during pubertal growth

Luciana Abrão Malta and Cristina F Ortolani

Department of Orthodontics, School of Dentistry, University Paulista, UNIP, Sao Paulo, Brazil

Kurt Faltin

Department of Orthodontics, School of Dentistry, University Paulista, UNIP, Sao Paulo, Brazil Department of Facial Orthopedics, University of Ulm, Germany

Address for correspondence: Luciana Abrão Malta, Department of Orthodontics School of Dentistry University Paulista, UNIP, Sao Paulo, Brazil. Email: lucianabrao{at}yahoo.com.br

Received 15 August 2008; accepted 4 July 2009


   Abstract
Top
 Abstract
Introduction
 Subjects and methods
 Results
 Discussion
 Conclusions
 Contributors
 References
 
Objective: To quantify longitudinal cranial base growth from prepubertal through postpubertal stages of development, as defined by biological indicators of individual skeletal maturity (cervical vertebral maturation – CVM) method and to determine if there is sexual dimorphism resulting from cranial base growth.

Design: A longitudinal cephalometric study.

Setting: The Dental School of Paulista University, Brazil.

Participants: 36 subjects (21 females, 15 males) who were part of a longitudinal growth study and exhibited normal facial and normal vertical growth patterns.

Methods: Growth maturation of cervical vertebrae stages was assessed by two examiners independently. Cranial base measurements were carried out by one individual and repeated after one month. The growth increments over time were assessed with the one-way repeated-measures analysis of variance and post hoc Tukey multiple comparisions.

Results: There were no significant gender differences. There was a significant increase in all cephalometric measures between the different time points. Ba–Na showed the greatest amount of growth (mean change=2.8 mm). From T2–T3, the greatest amount of growth was found for Se–Na (mean change=3.4 mm) and the lowest for CC–Na (mean change=1.4 mm). Comparing overall changes (T1–T3) all the measurements showed statistically significantly increases (P<0.05). For all comparisons of between-stage changes the cranial base grew more than 2.0 mm during the pubertal growth.

Conclusions: Linear variables of cranial base showed significant growth during pubertal stages (pre-peak, peak and post-peak). No significant differences.

Key words: Cranial base, anterior cranial base, posterior cranial base, cephalometric, cervical vertebrae, pubertal growth


   Introduction
Top
 Abstract
 Introduction
Subjects and methods
 Results
 Discussion
 Conclusions
 Contributors
 References
 
Knowledge and understanding of craniofacial growth and development during puberty are important for diagnosis, treatment planning, evaluation of treatment results and stability.1Go,2Go

The cranial base is the template for facial development; therefore it is directly related to growth and displacement of both the maxilla and mandible. Understanding the normal pattern of cranial base development helps in the recognition of abnormalities of craniofacial growth.3Go–7Go Growth of the cranial base occurs by means of a complex balance including enlargement of the frontal sinuses, surface remodelling in the nasion region and interstitial growth at the spheno-occipital synchondrosis.8Go–12Go

The aim of this study was to quantify cranial base growth from prepubertal through postpubertal stages of development, as defined by the biological indicator of individual skeletal maturity [cervical vertebral maturation (CVM) method] and to determine if there are any differences in cranial base growth between genders.


   Subjects and methods
Top
 Abstract
 Introduction
 Subjects and methods
Results
 Discussion
 Conclusions
 Contributors
 References
 
The subjects for this study were identified from individuals who took part in a longitudinal growth study at the Dental School of Paulista University, Brazil. The growth study involved 150 orthodontically untreated subjects with either a Class I or a Class II malocclusion who had longitudinal records collected from childhood to adulthood time. Ethical approval was obtained from a Brazilian Health Sciences Institutional Review Board (ref. CAAE - 1.0.251/2006).

The criteria for including the radiograph in this study were:

  1. Class I anteroposterior relationship (ANB 2–4°);
  2. Average skeletal vertical relationships (Gonial angle=130±7°, CoGoMe=124±4°);
  3. Normal overbite and overjet;
  4. No significant or adverse medical history.

Of the 65 individuals in the wider growth study who fulfilled the inclusion criteria, 20 did not have radiographs corresponding to the age of interest or the radiographs were missing and nine were excluded due to poor quality lateral cephalometric radiographs. Therefore, the sample consisted of 36 subjects (15 male, 21 female). The average age at the first radiograph was 10.4 years (SD 0.98).

The CVM stage of each radiograph was assessed according to the method described by Baccetti et al.13Go (Figure 1Go). The radiographs of each subject were divided into T1 pre-peak (CS1 and CS2), T2 peak (CS3 and CS4) and T3 post-peak (CS5 and CS6) groups. Two examiners (L.A.M. and C.L.F.O.) evaluated the cervical stage (CS) independently and agreed on the final categorization. The reliability of the visual assessment was determined using a kappa statistic. The T1, T2 and T3 lateral cephalograms were hand traced by one investigator (L.A.M.), and landmark locations, anatomical contours, and tracing superimpositions were verified by a second examiner (C.L.F.O.). Disagreements were resolved to the satisfaction of both investigators. All measurements were repeated one month later by one operator (L.A.M).


Figure 1
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  		Figure 1 Diagrammatic representation of CVM stages. CS1 and CS2 are prepubertal stages. CS3 and CS4 comprise the pubertal growth spurt. CS5 and CS6 are postpubertal stages. Stage assessment is based on visual analysis of cervical vertebrae on lateral cephalograms

 
The cephalometric landmarks identified were (Figure 2Go):


Figure 2
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  		Figure 2 Cephalometric landmarks used in this study

 
  1. Basion (Ba): the most posteroinferior point on the anterior margin of foramen magnum;
  2. Nasion (Na): the most anterior point of the frontonasal suture;
  3. Sela (Se): the centroid of sella turcica (pituitary fossa) determined by inspection;
  4. Porion (Po): the uppermost point of the external auditory meatus;
  5. Gnathion (Gn): the most inferior anterior point on the contour of the bony chin symphysis;
  6. Centre of the cranium (CC): the landmark at the intersection of the Ba–Na and Pt–Gn lines;
  7. Frankfort Centre (CF): the intersection between the Frankfort horizontal plane and a vertical line touching the distal margin of the pterygomaxillary fissure.

Measurements (in millimetres) were carried out between the following landmarks Ba–Na, Se–Ba, Se–Na, CC–Na, CC–Ba, CF–Po and were adjusted for the known radiographic enlargement before further analysis.

Statistical analysis
The method error was assessed using a paired t-test for systematic error and the intra-class correlation coefficient to estimate random error. Descriptive statistics were computed for all variables at T1, T2 and T3. The differences between the growth increments over time and between males and females were assessed with the one-way repeated-measures analysis of variance. Post hoc multiple comparisions were carried out with the Tukey multiple-comparison tests. The significance level was set at P<0.05.


   Results
Top
 Abstract
 Introduction
 Subjects and methods
 Results
Discussion
 Conclusions
 Contributors
 References
 
The interobserver examinations for the cervical staging showed very good agreement (kappa=0.92).14Go The reproducibility data are shown in Table 1Go. Four of the six measurements showed evidence of systematic error (p=0.10), but the mean differences were small and all the intra-class correlation coefficients were found to be greater than 0.95, therefore the error was considered acceptable.


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  		Table 1 Reproducibility measurements (reading 1 v reading 2) mean difference, standard deviation, 95% confidence interval of differences, P value (paired t test) and intra-class correlation coefficient
 
The mean ages of the participants at each time are given in Table 2Go. The mean values, standard deviations and confidence intervals for each variable are given in Tables 3–8GoGoGoGoGoGo.


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  		Table 2 Mean age (standard deviation) in years at each time point
 

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  		Table 3 Mean values, standard deviations and confidence intervals for Ba–Na
 

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  		Table 4 Mean values, standard deviations and confidence intervals for Se–Na
 

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  		Table 5 Mean values, standard deviations and confidence intervals for CC–Na
 

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  		Table 6 Mean values, standard deviations and confidence intervals for Se–Ba
 

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  		Table 7 Mean values, standard deviations and confidence intervals for CC–Ba
 

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  		Table 8 Mean values, standard deviations and confidence intervals for CF–Po
 
The ANOVA table is shown in Table 9Go. There were no significant differences between genders for any of the cephalometric measures (P>0.05), therefore the male and female data at each time point were pooled. The results of the Tukey multiple-comparison tests between the different time points for each radiograph are shown in Table 10Go. The study group showed statistically significant differences between T1–T2, T2–T3 and T1–T3.


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  		Table 9 Results of the one-way repeated-measures analysis of variance with dependent measurement of craniofacial measurements and independent variables of gender and time point when radiograph was taken (n=36)
 

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  		Table 10 Results of the Tukey multiple-comparison tests (n=36)
 
From T1–T2, all cephalometric measures were significantly different. Ba–Na showed the greatest amount of growth (mean change=2.8 mm; P<0.001). From T2–T3, again the differences were significant for all cephalometric measures (P<0.001). The greatest amount of growth was found for Se–Na (mean change=3.4 mm) and the lowest for CC–Na (mean change=1.4 mm), both of which indicate anterior cranial base growth (Tables 3 and 4GoGo).

Comparing overall changes (T1–T3) all the measurements showed statistically significantly increases (P<0.05). The measurements showing the greatest amount of growth during this study period were Ba–Na (mean change=5.0 mm) and Se–Na (mean change= 5.1 mm).

For all comparisons of between-stage changes (T1–T2, T2–T3 and T1–T3) the cranial base grew more than 2.0 mm during the pubertal growth. The period of time displaying the higher growth was between T1–T2.


   Discussion
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
Conclusions
 Contributors
 References
 
This study has used a longitudinal sample to show important cranial base growth during puberty. The cranial base plays a key role in craniofacial growth, helping to integrate, spatially and functionally different patterns of growth in various adjoining regions of the skull, such as components of the brain, nasal cavity, oral cavity and pharynx. There is also a relationship between the cranial base variations and sagittal malpositions of the jaws.15Go,16Go Thus, the knowledge of cranial face growth is important in the understanding of craniofacial development.

No previous investigation has studied the longitudinal effects of cranial base growth during pubertal growth using the CVM method as a biological indicator of individual skeletal maturity. In order to provide this important information, the present study analyzed changes of cranial base during a mean period of 6 years follow-up. These data demonstrate that cranial base growth occurs until adulthood.

Total length of cranial base
The total length of the cranial base, represented by Ba–Na measurement, increased during all the periods examined, confirming that the cranial base grows during all the pubertal phases. According to our results, this growth is largest during the interval between the pre-peak stage and the peak of pubertal growth, decreasing in the post-peak period.

Similar results were shown by Lewis et al.1Go,17Go,18Go who studied cranial base lengths and demonstrated pubertal growth for Ba–Na in both male and female subjects. Roche et al.19Go continued their study of basal growth through adolescence to at least 21 years and found that the cranial base elongates more in the male group throughout this period, not necessarily at a greater rate, but for a longer period of time. In addition, they noted that 95% of the mature length of cranial base was reached around 11 to 13 years old in the female group and 15 years in the male group.

Anterior cranial base
The anterior cranial base was represented by Se–Na and CC–Na measurements. Both increased during the periods examined. Melsen20Go states that the growth of the spheno-ethmoidal and sphenofrontal suture usually terminates at 7 years old. Anterior cranial base growth is still necessary after the brain has virtually ceased to grow at 7 to 8 years old to enable facial growth to occur. This growth takes place almost entirely by increased pneumatization of frontal and ethmoid bones, so further increases in Se–Na are mainly contributed by growth of the frontal bone.21Go,22Go

The increase in thickness of Na from birth to adulthood is accounted for by enlargement of the frontal sinus.22Go,23Go Rapid growth of the sinuses continues until 12 years old, when they reach nearly adult size.24Go This finding was supported by Brown et al.,25Go who showed that the median age at which the main increase in size of the sinus ceased was 15.7 years for boys and 13.7 years for girls, thus suggesting that the enlargement of the frontal sinus, a mainly osteoclastic activity, follows the trends for growth in bone lengths very closely. Hence, this might explain why all cephalometric measures from this study involving Nasion increased during puberty.

According to Enlow and Hans26Go the nasomaxillary complex, suspended by sutures from the anterior cranial base and the frontal lobes, is carried anteriorly as the combined frontal and temporal lobes progressively expand. Melsen and Ousterhout27Go related that the maxillary bones are connected to the surrounding bones by the circummaxillary sutures that include the zygomaticomaxillary, frontomaxillary, pterygomaxillary and the median palatal sutures. These sutures allow the displacement, as well as growth of the maxilla; however, the sutures start to interlock after the pubertal growth spurt and are difficult to separate using orthopedic forces.

The results of this study showed the greatest amount of growth in the anterior cranial base. Hence, Class III malocclusion treatment directed at the maxilla may be more effective if started during the pubertal growth period, because of the anterior growth of the anterior cranial base and related forward displacement of maxilla.

Posterior cranial base
The posterior cranial base was represented by three different measures (Se–Ba, CC–Ba and CF–Po) and during all different studied periods, there were significant differences. All the posterior measurements showed almost the same proportional growth increases when the changes T1–T3 were analyzed.

Thilander and Ingervall28Go performed histological and microradiographic studies based on autopsy material. According to their study, the increase in Se–Ba length is described primarily to growth activity at the spheno-occipital synchondrosis. Frik et al.29Go reported a wide variation in the time of fusion of the spheno-occipital synchondrosis. Recently, Sahni et al.30Go showed that in the males, partial fusion was seen at 13 years old while complete fusion was noticed at 15 years old in 25% of the subjects, therefore the age at which the majority of boys have complete fusion was 15 years old or above. In females, the earliest partial fusion was noted at 12 years old and complete fusion was present at 13 years old in 16.6% with all female subjects showing complete fusion at 17 years old. Kahana et al.31Go however, found no correlation between the chronological age and the time of closure of the synchondrosis. Thus, during the age range in our study, the synchondrosis is likely to be still open, but close to closure and termination of growth in most of subjects.

Mitani32Go and Kasai et al.12Go showed that cranial base growth is dependent on the brain growth during infancy and in puberty growth is related to general body growth. However, for the posterior cranial base, growth varies during life.

There is some overlap between the midline and lateral structures in the cranial base. Measurements in three dimensions (volume) would be more accurate than those in two dimensions (area). CBCT data sets can provide undistorted 3D morphology, making it possible to identify craniofacial structures more naturally. However, landmark identification in 3D is not simple. No such three-dimensional longitudinal growth data are available.

Gender differences
The present study, unlike other studies,9Go,17Go,19Go,33Go showed no statistically significant differences between the genders for any of the measurements. This may have been due to the sample size. A power calculation using the data from this study suggests that for Ba–Na and Se–Ba measurements we would require a sample size of 92 for Ba–Na and 130 to Se–Ba, in each gender, to detect a significant difference at the P>0.05 with a power of 0.85.


   Conclusions
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 Conclusions
Contributors
 References
 
This study found the following:


   Contributors
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 Conclusions
 Contributors
References
 
Luciana Malta was responsible for study design; obtaining funding; logistic, administrative, and technical support and data interpretation; drafting, critical revision, and final approval of the article. Cristina Ortolani was responsible for recruitment of participants and data collection; analysis; and drafting, critical revision, and final approval of the article. Kurt Faltin is the guarantor.


   References
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 Conclusions
 Contributors
 References
 
1 Lewis AB, Roche AF. Elongation of the cranial base in girls during pubescence. Angle Orthod 1972; 42: 358–67.[Medline]

2 Krieg WL. Early facial growth accelerations. Angle Orthod 1987; 57: 50–62.[Medline]

3 Lobb WK. Craniofacial morphology and occlusal variation in monozygous and dizygous twins. Angle Orthod 1987; 57: 219–33.[Medline]

4 Moyers RE. Ortodontia. Rio de Janeiro: Guanabara Koogan, 1991.

5 Rosemberg P, Arlis HR, Haworth RD, Heier L, Hoffman L, La Trenta G. The role of the cranial base in facial base in facial growth: experimental craniofacial synostosis in the rabbit. Plast Reconstr Surg 1997; 99: 1396–407.[CrossRef][Medline]

6 Coben SE. The spheno-occipital synchondrosis: the missing link between the profession’s concept of craniofacial growth and orthodontic treatment. Am J Orthod Dentofacial Orthop 1998; 114: 709–12; discussion 713–714.[CrossRef][Medline]

7 Tanabe Y, Taguchi Y, Noda T. Relationship between cranial base structure and maxillofacial components in children aged 3–5 years. Eur J Orthod 2002; 24: 175–81.[Abstract/Free Full Text]

8 Dhopatkar A, Bhatia S, Rock P. An investigation into the relationship between the cranial base angle and malocclusion. Angle Orthod 2002; 72: 456–63.[Medline]

9 Roche AF, Lewis AB. Sex differences in the elongation of the cranial base during pubescence. Angle Orthod 1974; 44: 279–94.[Medline]

10 Brodie AG. The behavior of cranial base and its components as revealed by seralcephalometric roentgenograms. Angle Orthod 1955; 2: 148–60.

11 Hopkin GB, Houston WJB, James GA. The cranial base as an etiological factor in malocclusion. Angle Orthod 1968; 38: 250–55.[Medline]

12 Kasai K, Moro T, Kanazawa E, Iwasawa T. Relationship between cranial base and maxillofacial morphology. Eur J Orthod 1995; 17: 403–10.[Abstract/Free Full Text]

13 Baccetti T, Franchi L, McNamara JA Jr. The Cervical Vertebral Maturation (CVM) method for the assesment of optimal treatment timing in detofacial orthopedics. Semin Orthod 2005; 11: 119–29.[CrossRef]

14 Cohen JA. A coefficient of agreement for nominal scales. J Educ Psychol Meas 1960; 20: 37–46.[CrossRef]

15 Polat OO, Kaya B. Changes in cranial base morphology in different malocclusions. Orthod Craniofac Res 2007; 10: 216–21.[CrossRef][Medline]

16 Houston WJ. A cephalometric analysis of Angle class II, division II malocclusion in the mixed dentition. Dent Pract Dent Rec 1967; 17: 372–76.[Medline]

17 Lewis AB, Roche AF, Wagner B. Pubertal spurts in cranial base and mandible. Comparisons within individuals. Angle Orthod 1985; 55: 17–30.[Medline]

18 Lewis AB, Roche AF. Cranial base elongation in boys during pubescence. Angle Orthod 1974; 44: 83–93.[Medline]

19 Roche AF, Lewis AB, Wainer H, McCartin R. Late elongation of the cranial base. J Dent Res 1977; 56: 802–08.[Abstract/Free Full Text]

20 Melsen B. The cranial base. Acta Odontol Scand 1974; 32 (Supplement 62).

21 Scott JH. The cranial base. Am J Phys Anthropol 1974; 16: 319–48.[CrossRef]

22 Bjork A. Cranial base development. Am J Orthod 1955; 41: 198–255.[CrossRef]

23 Roche AF. Increase in cranial thickness during growth. Hum Biol 1953; 25: 81–92.[Medline]

24 Dolan KD. Paranasal sinus radiology. Part 1A. Introduction and the frontal sinuses. Head Neck 1982; 4: 301–11.[CrossRef]

25 Brown WA, Molleson TI, Chinn S. Enlargement of the frontal sinus. Ann Hum Biol 1984; 11: 221–26.[CrossRef][Medline]

26 Enlow DH, Hans MG. Essentials of Facial Growth. Ann Arbor, MI: Needham Press. Inc., 2008.

27 Melsen B, Ousterhout DK. Anatomy and development of the pterygopalatomaxillary region, studied in relation to Le Fort osteotomies. Ann Plast Surg 1987; 19: 16–28.[CrossRef][Medline]

28 Thilander B, Ingervall B. The human spheno-occipital synchondrosis. II. A histological and microradiographic study of its growth. Acta Odontol Scand 1973; 31: 323–34.[CrossRef][Medline]

29 Frik HLH, Stark D. Human Anatomy. Stuttgard and New York: Georg thieme Verlag, 1991.

30 Sahni D, Jit I, Neelam, Suri S. Time of fusion of the basisphenoid with the basilar part of the occipital bone in northwest Indian subjects. Forensic Sci Int 1998; 98: 41–45.[CrossRef][Medline]

31 Kahana T, Birkby WH, Goldin L, Hiss J. Estimation of age in adolescents – the basilar synchondrosis. J Forensic Sci 2003; 48: 504–08.[Medline]

32 Mitani H. Contributions of the posterior cranial base and mandibular condyles to facial depth and height during puberty. Angle Orthod 1973; 43: 337–43.[Medline]

33 Ursi WJ, Trotman CA, McNamara JA, Jr, Behrents RG. Sexual dimorphism in normal craniofacial growth. Angle Orthod 1993; 63: 47–56.[Medline]





This Article
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