Predicting Growth in the
Aging Craniofacial Skeleton

Paper presented at the 9th Biennial Meeting of the International Association
for Craniofacial Identification, FBI, Washington, DC, July 2000

Christopher S. Milner
Medical Student

Richard A. Neave
Medical Artist

Caroline M. Wilkinson
Medical Artist

University of Manchester
Manchester, United Kingdom

Introduction.......Materials and Methods.......Results.......Discussion.......References

Introduction

Despite man's best efforts, the outward facial appearance associated with increasing age is unstoppable. As part of this change, there is a continuous alteration of the morphological properties of soft tissue structures and their composition, especially in relation to the extracellular matrix, which serves as tissue scaffolding. The possibility that progressive change to underlying bone tissue may accompany that seen in soft tissues has received much attention in the literature during the past 50 years and has been comprehensively reviewed by Behrents (1984). Histological alteration of bone architecture is known to occur with a disorganization of the highly ordered Haversian system, a reduced number of resident osteocytes, and a reduced overall bone mass and density. Nevertheless, bone remains a highly dynamic tissue with active remodeling occurring through old age. Beyond the fourth decade, this remodeling process has been shown to occur in a differential pattern within anatomically defined areas to produce gross changes in shape at the macroscopic level. This has been described for many long bones of the skeleton where an overall increase in width and length of the shaft results from endosteal bone resorption and preferential periosteal apposition. In essence, these dimensional changes can be regarded as growth.

With its complex three-dimensional construction, the macroscopic effects of this remodeling are less easily interpreted for the aging craniofacial skeleton. The majority of the early work into the changes to skull shape with age consisted of cross-sectional approaches. This was achieved, for example, by comparing the dimensions of large numbers of dry skulls or making other qualitative observations from living subjects by various means, such as a lateral-head X-ray film measurement. More accurate quantitative information was derived from longitudinal experiments arising from the development of the Cephalostat by Broadbent in 1931. Cephalostat roentgenography was employed in the Bolton Brush study (Broadbent et al. 1975) to describe the normal development of the childhood skull prior to maturity. The standardization inherent to cephalometric analysis allowed for accurate intrasubject comparison as the individual ages. Thus the Bolton Brush work generated meaningful data describing the spatial inter-relationship of bony landmarks with time and the characteristics of craniofacial skeletal development during childhood.

Behrents combined the technique of cephalometry together with data from the Bolton Brush study in the first major and unparalleled longitudinal investigation into the phenomenon of adult skull growth (Behrents 1984; Behrents 1985A). By comparing old-age cephalographs to cephalographs taken of the same individuals as childhood participants of the original Bolton Brush study, Behrents was the first to describe the detailed craniofacial growth pattern that occurs during adulthood. Complementary longitudinal cephalometric studies were to follow, further substantiating the principle of adult craniofacial growth (Bishara et al. 1994; Formby et al. 1994; West and McNamara 1999). These subsequent studies have confirmed and extended understanding of differential growth between the sexes, the rates of growth over specific adult age ranges, and the particular patterns of growth in defined regions of the craniofacial complex. Nearly all of this research has been conducted by scientists with orthodontic expertise and has value in relation to maxillofacial surgery and the shaping of orofacial structures during childhood. Such treatments aim to produce a harmonious and functionally appropriate craniofacial complex following developmental dysgenesis.

At present, cephalometry remains the state-of-the-art technique within the context of longitudinal growth studies. No other radiographic or other approach has, as yet, existed long enough to follow the evolution of the craniofacial complex during the normal human life span. This, therefore, places the tool of cephalometry in a unique position, and the questions arise—can it be developed further, and can it be applied to other problems outside the fields of dentistry and orthodontics? This possibility was explored by evaluating the adult longitudinal cephalometric growth data in the context of forensic medicine. More specifically, the study breaks down into two separate sections. The course of craniofacial growth for a given individual subsequent to a given starting age point was predicted. The results of this are initially presented in cephalographic form—a representation familiar to both orthodontics and dentistry. This format has, however, limited value from a forensic standpoint. Therefore, in the second stage, the work's relevance to forensic science was maximized by extrapolating the results through the technique of facial reconstruction, which has a well-established and indispensable role in forensic facial identification. For details on the history of facial reconstruction, see Prag and Neave (1997).

These two objectives were addressed using a dry bone skull as source material. The skull was chosen from an individual who died in her late teens. The aging prediction was employed to simulate the appearance 40 to 50 years later, using craniofacial aging data from the Behrents study.

Materials and Methods

The study was initiated with the selection of a skull suitable for aging using Dr. Behrents' data. The skull was a female archaeological specimen obtained from an excavation at the Spitalfield site in London, England. It was examined initially to check its gross external appearance and its known history under the following criteria:

• Good condition
  
  
• Caucasian origin
  
  
• An individual who died within the age range of 17 to 20 years old
  
  
• Known sex
  
  
• Good dentition and no obvious malocclusion

The cranium and mandible were first treated to destroy any potentially infective microorganisms within the bone tissue. The skull was then taken to the Department of Radiology, University of Manchester Dental Hospital, Manchester, United Kingdom. The skull was examined by a senior radiologist who adjusted the mandible on the maxilla to achieve best centric occlusion in accordance with the cephalometric protocol of living subjects employed in the Behrents and Bolton Brush studies. This position was maintained during the X-ray period with radiolucent masking tape. The skull was mounted by its external auditory meati in the cephalostat of a Cranex 3 cephalometer (Soredex Orion Corporation, Helsinki, Finland) and adjusted to lie in the Frankfurt horizontal plane. With the soft tissue screen removed, a lateral cephalogram was taken with X-ray exposure at 63 kV, 110 mA for 0.4 seconds. The X-ray signal passed through a Fuji FG-8 intensifier screen onto Fuji HRL 24/30 film. Following this, the cephalostat was rotated 90 degrees about its vertical axis, and a posterior-anterior cephalogram was obtained. For this film, the voltage setting was increased to 65 mA. All other parameters remained the same. Both films were developed using an automatic processor. The lateral film was analyzed by a radiologist whose professional experience was essential for the task of accurately aging the skull through dental development (Haavikko 1970, 1974, and 1985).

The lateral cephalogram was digitized in the University of Manchester, Department of Orthodontics, using an IBM®-compatible computer. This set of data was used to perform cephalometric analysis of the skull using the technique described by Downs and Steiner (Jacobson and Caulfield 1985) to obtain further orthodontic and craniofacial information beyond that available through direct physical examination. This, together with age estimation by dental development on X-ray, provided objective information with which to confirm or refute the initial characteristics of the skull as appraised at the outset. This additional information allowed a detailed assessment of the skull with respect to its selection for use with the data contained within the Behrents study (see Results).

The process of growth simulation began with data analysis of the lateral cephalogram. Cephalometry always produces some degree of radiographic enlargement of the imaged skull due to the divergence of X-rays from a point source of origin. For the cephalometric equipment used in this study, the magnification factor was 1.153. An exact life-sized image was imported into Adobe® Photoshop® (version 3.0.5) using a Jade Linotype Hell scanner and its associated software on an IBM®-compatible computer, for all further calculations.

Figure 1. Scanned cephalograph with the linear measurements included from the Behrents study (labeled). Each vector shares a common origin at sella, before radiating out to different locations on the bone profile. Click for enlarged image.

In the Behrents study, 70 linear cephalometric measurements or planes were studied, all sharing a common origin from the center of the pituitary fossa (referred to forthwith as sella) and radiating outwards to landmarks located on the bone profile and to internal positions (Figure 1). The angular relationship of each plane to the reference plane of sella-nasion was also a central feature to the method of the Behrents study. The change to these angular and linear measurements with increasing age is presented in many different contexts (including the sex and orthodontic treatment history of the subject). All the variables for each particular measurement were then collected together and presented as absolute values by age group in table format (Behrents 1985B). For this study, 29 orthodontically untreated data values relevant to the sex of the chosen skull were selected from those measurements related to structures in the saggital plane of the skull (Table 1) out of the 139 possible linear and angular variables available overall in the Behrents study. These were the measurements to be used to simulate the changes to the bone profile of the subject skull through the adult years of life. Before their application to the project skull, the data needed to be converted to relative values of change between each age group studied. This was achieved by ascribing the value for both linear and angular data as zero for the starting age (i.e., no change to the measured values on the project skull). The value of change whether an increase or a decrease for each parameter was calculated for the subsequent age and matched to the near-mean age group as illustrated in Table 2.

Table 2: How the Behrents Data Was Applied to the Project Skull

Study parameter	Age range
	17–18	51–83
New average age point in this study	17	65
Absolute value in Behrents study (mm/degree)	V	Z
Calculation of difference in value between youngest and oldest age (mm/degree)	0	Z – V

Figure 2A. Photographs detailing the reconstruction process of a young human. Top: lateral and frontal skull views. Middle: lateral and frontal muscle views. Bottom: finished reconstruction. Click for enlarged image.

Figure 2B. Photographs detailing the reconstruction process of an older human. Top: lateral and frontal skull views. Middle: lateral and frontal muscle views. Bottom: finished reconstruction. Click for enlarged image.

The 29 variables in Table 1 were measured and recorded from the digitized cephalogram in Adobe® Photoshop® using the zoom feature to maximize the accuracy of landmark identification. This included the linear distances for measurements 1–15 and the 14 angular relationships to sella-nasion, as shown in Table 1. This data was altered in accordance with the method shown in Table 2 to produce 29 new measurement values detailing how the bony profile should alter with time. All of the linear and angular values were related back to the cephalograph image to produce the new profile markers. The digitized cephalograph was printed out at a 1:1 dimensional ratio to the original skull and mounted onto card. A single line to produce a new bone profile for the project skull joined each new landmark position. The card was then trimmed to the new profile and stored for the casting process.

The skull was prepared for casting. For this study, the objective was to produce a permanent mold from which identical replicas could be produced, all sharing optimal dimensional congruence with the original (bone) skull. This was achieved using a permanent two-part silicone mold of the cranium and mandible respectively. Because of the potentially damaging properties of unpolymerized liquid silicone to osseous tissue, the permanent mold was produced through an alginate mold intermediate. A detailed description of the casting process can be found in Prag and Neave (1997). The two replica skulls were checked against the bone original for dimensional accuracy by measuring linear distances between easily identified and accessible anatomical locations.

Finally, each cranium was paired with a mandible and positioned in centric occlusion, as the original had been at cephalometry. One cast was then sectioned into two halves along the saggital plane. The card-mounted altered profile was placed between the two halves—all three pieces matched by their supero-posterior cranial contour. This arrangement was secured by inserting two threaded steel rods across the cast and bolting them at each end (Figures 2A and 2B). Using sheet wax, the craniofacial contour was then built up to meet the saggital profile insert in the midline. Despite the absence of specific growth data away from the saggital plane, further wax was applied over the remaining facial contour in a manner suggested by the insert, but arbitrarily in pure terms.

Both the unaltered and age-simulated skulls were then ready for facial reconstruction and were mounted on poles in the Frankfurt horizontal plane.

Using the determining factors of age, sex, and racial group, the appropriate set of tissue-depth measurements were chosen. The skull studied in this research was female, in the 20-year-age group, and of an English-Medieval origin. Therefore, the most appropriate set of tissue-depth measurements was considered to be those of Helmer (1979).

At the appropriate anatomical points, small holes were drilled into the plaster skull. These housed wooden pegs that represent the tissue depths at those points. The wooden pegs were cut to lengths governed by the tissue-depth data. In this way, a set of guides for tissue depth across the face is attached to the skull surface. The skull details were studied, and a descriptive set of morphological details acquired. The eyeballs were set into the eye sockets at normal protrusion using clay. The eyeball placement depends on the depth of the orbits. The positions of the malar tubercle and lacrimal fossae were marked on the medial and lateral orbital borders. The muscles of the face were then modeled onto the skull in clay, one by one. The resulting muscular face already shows the basic face shape and proportions.

Skin strips were rolled, shaped, and placed over the muscle structure to create the finished face. The skin layer followed the underlying muscle structure. The finished face may include additional detail appropriate to the individual, such as hairstyle and wrinkles. In this case, no hair was added, but the older face included some estimation of age-related changes to the skin surface and form of the face and neck.

Results

From physical examination, the dentition of the archaeological skull specimen appeared to be in excellent condition. The position of the occlusion was readily identified and judged to be of Class 1 type. There was some damage to the free edge of the nasal bones, and a small post-mortem hole was located in the right parietal bone. Otherwise, the skull was in excellent condition, and despite its missing cephalometric location for SIMP 50 (Sella to tip of nasal bone), it was provisionally accepted as a suitable project skull for this study.

Examination of the third molar root development on a lateral X-ray indicated the skull was approximately 18 years old at time of death.

Through examination of the lateral cephalogram using the Steiner and Down's analyses, the skull was found to have a well-developed mandible, confirming the Type 1 occlusion with the maxilla, with the rest of the dento-facial features forming a harmonious overall orthognathic balance. This evidence supported the findings at initial physical examination and suggested that the skull was suitable for inclusion into the study in accordance with the Behrents' criteria.

The skull was used to create a permanent cast as described in the Materials and Methods section. Two plaster cast skulls were prepared and dimensionally tested against the plaster intermediate and the original skull.

The lateral cephalogram was scanned into Adobe® Photoshop®, and the linear and angular measurements subsequently calculated. Table 1 presents this data and also includes the data necessary for the alteration to the 29 cephalometric measurements for the skull profile prediction at age 65. This table was compiled principally through manipulation of the orthodontically untreated female data contained in the Behrents study.

Figure 3. Lateral cephalograph of the project skull (negative of Figure 1). The black markers show the predicted profile growth pattern and indicate the alteration during the adult years. Click for enlarged image.

Figure 3 presents a scaled-down negative view of the cephalogram with the original cephalometric measurements at age 18 in location. The heavy black bars on the bone surface represent the magnitude and direction of growth that the bone profile is predicted to take from age 18 to 65. This illustration provides the first visual impression of the growth pattern that the craniofacial skeleton is likely to take over this time period. This cephalograph tracing was mounted in the saggital plane between the two halves of the cast destined for reconstruction at age 65, as described in the Materials and Methods section. Figures 2A and 2B demonstrate how this cast was subsequently altered using sheet wax to transfer the growth prediction data to a physical three-dimensional format. The accompanying images in Figures 2A and 2B present the appearance of the reconstruction process at the muscle and final completed stages.

Discussion

Examining Figure 3, it is possible to see how the predicted changes to the skeletal profile become manifest over the total age span studied. The lower face including the maxilla and mandible appear to grow both forwards and downwards. The anterior cranial base increases in length such that bony glabella and nasion both move in an anterior direction. The mandibular plane (registered on gonion and gnathion) moves towards the horizontal such that the mandibular plane angle (mandibular plane to the Frankfort horizontal) decreases. This suggests that the jaw line has become more square with age. All structures between the bony glabella and menton diverge with respect to the vertical plane, and this suggests an increase in the overall length of the face, taking into account the antero-inferior direction of growth of the lower facial structures.

Contrasting these findings with the growth observations made by Behrents is beyond the scope of this study. However, it is pertinent to comment on the overall validity of Behrents' data as a predictive measure of skull growth. The predictive use of that data has drawbacks in one important respect. Because of design constraints and other factors, there was a paucity of available subjects included at the older end of the age spectrum studied. Under these circumstances, it is less reliable to describe craniofacial change in an elderly population when only a few subjects are represented in the sample.

In view of this drawback in the Behrents study, it may be fair to comment upon observations of craniofacial growth but less appropriate to use the same data as a predictive tool, without significantly increasing the sample size from which they were originally compiled. The reliability of adult growth observations should be increased significantly in the future when the design of such experiments incorporates larger sample sizes. In this situation, the growth trends seen within a sample population will also suffer less from those individuals whose craniofacial features deviate considerably from the observed mean values.

Considering its value as a predictive tool, knowledge of adult craniofacial growth in the coronal plane will be valuable. Although both lateral and postero-anterior cephalograms were obtained in the Behrents study, the postero-anterior films were used only for landmark identification, when this proved unclear from the lateral view. The value of the original postero-anterior cephalograms taken during the Behrents study has now been recognized in its potential for extending our understanding of width change and growth in the coronal plane. To this end, these films are currently being reexamined against the corresponding lateral film for each subject. When this data is combined with that from the saggital and parasaggital planes, it may be possible to get a better understanding of where growth is actually occurring within the craniofacial complex overall.

In light of currently available data, the present methodological approach restricts analysis of this study to a purely subjective level. It must be stressed that the reconstruction-based aging simulation is an exercise, and the authors are unaware of any precedent against which to compare it. The appreciated value of this and potential future application of facial growth simulation may well govern the continuation of such research. In the future, other methods of performing longitudinal craniofacial growth studies will, however, become available. For example, when computerized tomography has been used long enough, patient data recorded at its inception could be compared with data obtained from the same patients in later life.

Computerized tomography has the advantage of working (for the most part) within the digital domain, and as a result, digitally represented craniofacial data can already be translated by a computer into three-dimensional coordinates for the generation of milled skulls. Were this technique to be applied in a study such as this, the representation of change in both multicoronal and multisaggital planes could be incorporated into milled skulls during construction, rather than being applied for the surface alteration of plaster skulls as in this work.

References

Behrents, R. A treatise on the continuum of growth in the aging craniofacial skeleton. Doctoral dissertation, University of Michigan, Ann Arbor, Michigan, 1984.

Behrents, R. Growth in the Aging Craniofacial Skeleton. Craniofacial Growth Series, Ann Arbor, Michigan, 1985A.

Behrents, R. An Atlas of Growth in the Aging Craniofacial Skeleton. Craniofacial Growth Series, Ann Arbor, Michigan, 1985B.

Bishara, S. E., Treder, J. E., and Jakobsen, J. R. Facial and dental changes in adulthood, American Journal of Orthodontics and Dentofacial Orthopedics (1994) 106:175–186.

Broadbent, B. H. A new X-ray technique and its application to orthodontia, Angle Orthodontist (1931) 1:45–66.

Broadbent, B. H., Broadbent. B. H., and Golden, W. H. Bolton Standards of Dentofacial Developmental Growth. St. Louis, C. V. Mosby, 1975.

Formby, W. A., Nanda, R. S., and Frans Currier, G. Longitudinal changes in the adult facial profile, American Journal of Orthodontics and Dentofacial Orthopedics (1994) 105:464–476.

Haavikko, K. The formation and the alveolar and clinical eruption of the permanent teeth: An orthopantomographic study, Proceedings of the Finnish Dental Society (1970) 66:103–170.

Haavikko, K. Tooth formation estimation on a few selected teeth: A simple method for clinical use, Proceedings of the Finnish Dental Society (1974) 70:15–19.

Haavikko, K. The development of the dentition. In: Introduction to Orthodontics. B. Thilander and O. Ronning, eds. Tandlakavforlaget, Stockholm, 1985, pp. 45–62.

Helmer, R. Schadelidentifizierung durch elektronische bildmischung. Kriminalistik-Verlag, Heildelberg, 1979.

Jacobson, A. and Caulfield, P. W. Introduction to Radiographic Cephalometry. Lea and Febiger, Philadelphia, 1985.

Prag, J. and Neave, R. A. H. Making Faces. British Museum Press, London, 1997.

West, K. S. and McNamara, J. A. Changes in the craniofacial complex from adolescence to midadulthood: A cephalometric study, American Journal of Orthodontics and Dentofacial Orthopedics (1999) 115:512–532.

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