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Facial growth subsequent to Le Fort I osteotomies in adolescent monkeys
SClENTlFlC ARTICLES J Oral Maxlllofac 45:123-136,
Surg
1987
Facial Growth Subsequent to Le Fort Osteotomies in Adolescent Monkeys RAVINDRA
I
NANDA, BDS, MDS, PHD,* OMAR BOUAYAD, DDS, MS, MDENTSCJ AND RICHARD G. TOPAZIAN, DDS$-
The study goal was to assess qualitatively and quantitatively the craniofacial adaptations following total maxillary osteotomy with and without mandibular autorotation. Six adolescent female Macaca fascicularis monkeys were randomly divided into two surgical groups, and eight others served control. Prior to surgery, metallic implants were inserted in the anterior part of the cranial base, on opposite sides of craniofacial sutures, and in multiple sites of the maxilla and mandible. Group I animals underwent a Le Fort I advancement of 4 mm, while Group II animals had a 5mm advancement and a 2.5mm impaction. Lateral cephalometric headfilms were taken at monthly intervals for a total follow-up of 12 months after surgery. At least two cephalograms were taken on each occasion, one with the teeth in occlusion and the other with the mouth wide open. The latter was used to ascertain accurately the outline of the mandibular condyle. Cephalometric superimposition methods were used to quantify the growth changes. The findings indicated that the growth changes in the maxilla and mandible were related to the extent of injury caused by maxillary surgery. The largest increments and rates of growth were observed respectively in the control animals, Group I animals (anterior maxillary repositioning), and Group II animals (anterior and superior maxillary repositioning). The most interesting finding was that mandibular growth pattern followed maxillary growth pattern in both experimental groups, and the immediate postsurgical occlusion in Class II molar relationship was maintained with increased overjet in both experimental groups throughout the postsurgical observation period.
Orthognathic surgery, with or without orthodontic treatment, has gradually become the treatment-ofTchoice to correct moderate to severe dentocraniofacial disharmonies. However, this treatment has been mostly limited to individuals who have completed their active growth. The recommendation to delay surgery in adolescents is based
on a lack of clinical and experimental data regarding the effect of injury caused by surgery on various components of the remaining craniofacial growth. Possible adverse facial growth or skeletal relapse after surgery in adolescents are problematical clinically, primarily because of insufficient understanding of the mechanisms by which bone, muscle, and associated tissues adapt to alterations in structure or function. The purpose of this investigation was to assess quantitatively and qualitatively the craniofacial adaptations that occur subsequent to total maxillary osteotomy with and without mandibular autorotation in actively growing Macaca fuscicularis monkeys. The results of our previous studies,1-3 regarding the craniofacial changes subsequent to surgical superior repositioning of the maxilla, have shown that: I) a surgical insult to the midface in
From the Departments of Orthodontics and Oral and Maxillofacial Surgery, School of Dental Medicine, University of Connecticut, Farmington, Connecticut. * Professor, Department of Orthodontics. t Resident, Department of Orthodontics. $ Professor and Chairman, Department of Oral and Maxillofacial Surgery. Supported by NIDR grant no. DEO5396-05. Address correspondence and reprint requests to Dr. Nanda: Department of Orthodontics, University of Connecticut Health Center. 263 Farmington Avenue, Farmington, CT 06032. 0278-2391187 $0.00 + .25
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growing monkeys did not prevent coordinated growth between the maxilla and the mandible, and 2) the mandible in each experimental animal showed significantly less growth than in the controls, although it was subjected to no surgical intervention. These results warranted further studies to investigate the mandibular response to maxillary surgery and the possible role of mandibular autorotation on the subsequent craniofacial growth following surgery. The specific objectives of this study were to determine: 1) the effects of maxillary surgery on the subsequent growth and development of both maxilla and mandible; 2) the effect of surgical alteration of vertical facial height, and the role of mandibular autorotation, on the subsequent growth of both maxilla and mandible; and 3) the effect of surgical alteration of maxillomandibular sagittal relationship on the subsequent adaptation of mandibular growth. The long-term goals of this investigation were to improve and broaden our understanding of the effects of total maxillary osteotomy with controlled parameters of occlusion and vertical height on the nature of subsequent craniofacial adaptations.
IMPLANTS Tantalum implants were inserted at predetermined areas in certain craniofacial bones to ascertain accurately, with the help of conventional cephalometry, the changes of maxillary and mandibular growth and displacement and the changes of vertical facial height. 6,8,9 The sterile implants, measuring 1.5 mm in length and 0.2 mm in diameter, were inserted in both the left and the right sides of the face. The maxilla and mandible each received, via an intraoral route, one implant in the midline area and at least three implants bilaterally in the area of the canine, permanent first molar, and maxillary tuberosity. Two implants were placed in the midline of the cranial base7J0 and on each side of the zygomaticomaxillary, zygomaticotemporal, zygomaticofrontal, and frontomaxillary sutures through a skin incision. The skin incisions were closed by chromic catgut suture. The maxillary implants were placed clear of the osteotomy site or as superiorly as possible to avoid their loss during the osteotomy. An interval of six to eight weeks was allowed for normal healing of the incisions and stabilization of the implants prior to the osteotomy procedure.
Materials and Methods
SURGERY
ANIMALS
Le Fort I maxillary osteotomies were performed with the animals under general anesthesia.‘s2 A single-stage total maxillary osteotomy (Fig. 1) was performed in all the experimental animals1,2,9J1 followed by a different maxillary repositioning in Group I and Group II animals. The three monkeys in Group I underwent 4 mm of anterior maxillary repositioning with no or minimal autorotation of the mandible and no or minimal reduction of vertical height. The three monkeys in Group II had a S-mm superior and 4-mm anterior maxillary repositioning. The maxilla in both groups was fixed in its final position with transosseous wires placed in the piriform rim and buttress areas; maxillomandibular fixation was not used. The animals were kept on soft, fruit-supplemented diets during the first eight weeks postsurgitally. The experimental animals recovered without any major complications and gained weight similar to the control monkeys.
Fourteen adolescent female Macaca fascicularis monkeys were studied over a 12-month period. Eight animals served as controls, and six were subjected to total maxillary osteotomy. The six experimental monkeys were further subdivided into two groups of three, each group receiving a different maxillary repositioning after total maxillary osteotomy. Because birth dates for these animals were not available and there were no experimental data to assess their developmental age, the age of each monkey was determined by noting the eruption status of the dentition according to the tooth eruption tables of Hurme and Van Wagenen4,5 and the classification of McNamara and Graber.6 The age of the control monkeys ranged from 30 to 39 months, and that of the experimental monkeys from 31 to 41 months. All monkeys had their permanent first molars, and the permanent lateral and central incisors in occlusion; the first and second premolars were at various stages of eruption. At the start of the experiments, the weight of all animals ranged from 1.9 to 2.1 kg. All monkeys were termed adolescent according to the classification of McNamara et a1.6T7
CEPHALOMETRICANALYSIS Serial lateral cephalometric headfilms of all monkeys were taken prior to and immediately after metallic implant placement, immediately after the
NANDA ET AL.
FIGURE 1. Diagrammatic representation of Le Fort I advancement and impaction osteotomy sites shown in lateral views.
appropriate surgical procedure, and every four weeks thereafter during the 12-month postsurgical period. The anatomic landmarks, position of the metallic implants and the teeth used to describe the changes of growth and displacement, together with the changes of vertical facial height are shown in Figure 2. For the purposes of this study, anterior cranial base superimposition was used to analyze and quantify the craniofacial changes and displacement with surgery and growth. In addition, the changes of vertical facial height were assessed by direct measurements on each cephalogram. The cephalometric analysis performed has been described in detail by Nanda et al.i+2 The displacement of the six maxillary and man-
dibular anatomic landmarks and implants was measured to the nearest 0.5 mm horizontally and vertically. The successive outline tracings of the craniofacial complex were used only for descriptive purposes, while vertical and horizontal measurements were made directly on the successive cephalograms themselves with the help of the initial tracing. This procedure allowed for direct quantification of various small changes in craniofacial dimension which normally might be masked by tracing errors, especially in the first months. Obviously, the shorter the interval between headfilms, the greater is the likelihood that the magnitude of the measurement errors would approximate, or even exceed, the actual growth changes. The vertical facial relationships, as noted by three different measurements, were analyzed by direct measurement on each cephalogram with the teeth in occlusion. The absolute growth changes of the three following distances were measured to the nearest 0.5 mm on all successive cephalograms: anterior total facial height (distance from implant no. 1 to Menton); anterior upper facial height (distance from implant no. 1 to implant no. 3); and anterior lower facial height (distance from implant no. 3 to Menton). Data Analysis
FIGURE 2. Landmarks, implants and coordinate planes used to measure the craniofacial growth with anterior cranial base superimposition. I. anterior cranial base implant; 3, premaxillary implant; 4, posterior maxillary implant; 5. anterior mandibular implant; 6, posterior mandibular implant; PNS, posterior nasal spine; ME, mention; X axis, occlusal plan; Y axis drawn from point of intersection of occlusal plane with the anterior border of the ramus.
The quantitative data from various cephalometric measurements were analyzed using a factorial repeated-measures analysis of variance (ANOVA) design. This particular choice was dictated by the format of the longitudinal growth data. The repeated-measures ANOVA design used in this study is described at length by Winer.** The computational algorithm was provided by BMDP statistical
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the rate of change (growth or displacement) ferent between the groups examined.
is dif-
REPRODUCIBILITY
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FIGURE 3. Cephalometric tracings with cranial base superimposition of a representative adolescent control monkey showing dentocraniofacial changes following three, six, nine and 12 months of observation. Note the counterclockwise growth of the maxilla. Both the maxilla and the mandible show substantial growth during the observation period.
computing package. l3 The program partitions the total error variance into a component due to within subjects variation (that is, changes in subjects over time), a component due to between subjects (groups, for example, control group versus experimental groups), and finally, a component due to subject by factor interaction. By extracting the error variance due to within subjects variation, the model validates the comparison of group means over time and makes it possible to test for group effects. As in the usual ANOVA methodology, standard multiple comparison procedures can be used to detect differences between given pairs of means. The computer program used to perform the repeated-measures ANOVA was designed to yield weighted estimates of experimental effects, to account for the different numbers of animals in the control and experimental groups. A significant group effect indicates that the two overall group means are different. The initial time point at which differences between group means became statistically significant was determined by use of the Scheffe multiple comparisons procedure.14 A significant time effect implies that the mean measurements change significantly over time. It should be pointed out that the 12 time points (12-month observation period) have been pooled to six time points: that is, the means were compared at two-month interval periods by pooling the first two means, the second two means, etc. A significant time by group interaction implies that the groups are changing in different ways over time. In other words, a significant interaction indicates that
A combined determination of both cephalometric landmark location and measurement error was calculated. Twelve cephalograms were randomly selected: six with the teeth in occlusion and six with the mouth held wide open. All landmarks were identified on four separate occasions under the same standard conditions. The landmarks to be identified as well as the distances to be measured were not the same for the two types of headfilms used in this study. The 48 combined tracings were then “digitized” manually, and the location of the landmarks was recorded in both the horizontal and vertical direction. For the six headfilms with the teeth in occlusion, the mean combined error of the landmarks in the horizontal plane was 0.21 mm (SD = 0.04 mm), and in the vertical plane the mean combined error was 0.13 mm (SD = 0.02 mm). For the six headfilms with the mouth in open position the mean combined error of the landmarks in the horizontal plane was 0.19 mm (SD = 0.03 mm), and in the vertical plane it was 0.15 mm (SD = 0.05 mm). Results The insertion of implants was performed without any complications. All incisions healed completely prior to the osteotomy procedures, and the implants remained stable through the 12-month observation period. The experimental animals tolerated the surgical procedures well and did not experience any major postsurgical complications, despite the fact that maxillomandibular fixation was not used. The healing of the maxilla was uneventful and bone stability was noted six to eight weeks after surgery. All animals lost weight immediately following maxillary surgery; the mean weight loss was 0.2 kg (approximately 10% of their body weight). By the fourth postsurgical week, all animals had returned to their presurgical weight and subsequently gained weight similar to the control monkeys. The eight control adolescent .monkeys remained in good health and exhibited significant amounts of growth changes during the 1Zmonth observation period (Fig. 3). The overall direction and pattern of craniofacial growth were found to be similar in all the control animals. Their initial Class I occlusal relationship was maintained during the entire observation period and all animals maintained normal over-jet (0 to 1.5 mm) and overbite (0 to 1.O mm).
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FIGURE 4 (left). Composite tracings of an experimental animal in Group 1 superimposed on the anterior cranial base showing craniofacial growth changes noted three, six, nine and 12 months following maxillary advancement. Note the differences in the amount and direction of facial growth as compared to control monkeys of approximately similar age shown in Figure 3. Composite tracings of an experimental animal in Group II superimposed on the anterior cranial base showing craniofacial growth changes noted three, six, nine and 12 months following maxillary advancement and impaction. Note the differences in the amount and direction of facial growth as compared to experimental monkeys in Group 1 shown in Figure 4. FIGURE 5 (right).
CHANGES IMMEDIATELY AFTER SURGERY
To determine the amount of surgical repositioning of the maxilla and accompanying changes of the mandible, the cephalometric measurements taken immediately before and after the surgery were compared. These measurements were made relative to the coordinate system previously described’,* and were established on the presurgical cephalometric tracing of each animal. Although a maxillary advancement of 4 mm was planned for all animals in Group 1, one monkey had only a 1.5mm advancement. Consequently, the postsurgical occlusion was left 1.5 mm in Class II with an increased ovetjet of 1 mm. The two other monkeys had a maxillary advancement of 4 mm with an increased overjet of 3.25 + 0.25 mm. In the vertical direction, the mean amount of impaction in Group I was 0.75 t 0.25 mm anteriorly and 0.5 mm posteriorly, which was the anticipated movement. A mean 4 mm (& 0.5 mm) of superior repositioning and a mean of 5.25 mm ( + 0.25 mm) of anterior repositioning were reached after surgery in Group II animals. The repositioning of the posterior end of the maxilla was noted by measuring the horizontal and vertical displacement at the posterior nasal spine (PNS); it showed a mean superior repositioning of 2.5 mm. The overall repositioning of the maxilla following surgery in Group II resulted in a marked counterclockwise rotation with a
relatively larger amount than in Group I.
of anterior
displacement
Maxillary Changes Subsequent to Surgery The changes in maxillary growth were determined by measuring the positions of the maxillary implants (implants no. 3 and no. 4) and PNS relative to the implants in the anterior part of the cranial base (Figs. 4, 5). Only the positional changes of the maxilla are reported in this study. Growth and remodeling changes within the maxilla based on superimposition of the maxillary implants were not assessed quantitatively, because of the possible error induced by the lack of reliable and reproducible maxillary anatomic landmarks and the degree to which the maxilla contrasts with the surrounding area. Two months after surgery, the experimental Group II animals did not show any horizontal change at implant no. 3 (Fig. 6). Until seven months following surgery, the anterior displacement of the maxilla was only 0.5 mm. The mean anterior displacement of the premaxilla in the experimental Groups I and II was 37% and 67% less, respectively, than in the control group 12 months after surgery. The differences in anterior displacement of the premaxilla between the experimental groups and the control group reached significance (P <
CRANIOFACIAL
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6
6
FIGURE 6 (top lefr). Distribution pattern and mean change with standard deviation in the horizontal position of no. 3 of control, Group I and Group II animals during the 12-month period following maxillary osteotomy. The displacement of implant no. 3 of the experimental animals is less at each observation period, Group II animals showing less displacement than Group I animals. FIGURE 7 (top righ?). Distribution pattern and approximately control and experimental monkeys.
the same mean change in the vertical position of implant no. 3 in the
FIGURE 8 (bottom left). Distribution pattern and mean change in the horizontal direction at implant no. 4 in the control and experimental animals. No significant difference between Group I and Group II animals. FIGURE 9 (bottom right). Distribution pattern and mean change in the horizontal direction of PNS in the control and experimental animals. After four months, there is a significant difference between the control and the experimental monkeys.
0.001) at the first to second month interval, and remained significant throughout the 12-month observation period. The rate of anterior displacement was also different between the three groups. The mean anterior displacement of the premaxilla in Group II was 50% less than that in Group I at almost all stages of period; this difference became statistically significant three to four months after surgery. The mean superior displacement at implant no. 3 (Fig. 7) was less than 1 mm in all groups 12 months after surgery. The differences were not statistically significant between the three groups. The mean horizontal displacement of the posterior maxilla as noted at implant no. 4 or PNS was small (
4 than for PNS (Figs. 8, 9) although both showed a significant difference and a significant time by group interaction. The mean vertical displacement of implant no. 4 and PNS was less than 1 mm in both experimental groups in a downward direction (Figs. 10, ll), and the difference between Group I and II was statistically significant only for implant no. 4, which exhibited a small temporary superior displacement during the first four months after surgery in Group II animals. The finding was significantly different in the control group animals, which consistently showed a substantial downward displacement at both implant no. 4 and PNS. A signiticant difference (Z’ < 0.001) between the control and the experimental groups was reached very early (first to second month) with a significant time by group interaction. The horizontal displacement of the maxilla was
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FIGURE 10 (left). Distribution pattern and mean change in the vertical direction at implant no. 4 in the control and experimental animals.The displacementof implant no. 4 in the controls is in the inferior direction whereas almost negligible change is noted with the experimental
animals. Although small, there is a significant difference between Group I and Group II animals.
FIGURE 11 (right). Distribution pattern and mean change in the vertical direction of PNS. The pattern of change is similar to implant no. 4 shown in Figure 10.
more prominent than the vertical displacement in the three groups, except for PNS. In the horizontal direction, the amount and rate of maxillary displacement was significantly less in both experimental groups as compared to the control group. Moreover, the mean horizontal displacement in Group II animals was consistently less than that of Group I animals, especially at the premaxilla. In the vertical direction, the amount and rate of maxillary displacement was also significantly less in both experimental groups as compared to the control group, particularly at the posterior part of the maxilla. The difference between Groups I and II was significant only for implant no. 4. Of particular significance was the consistent counterclockwise rotation of the maxillary complex in both control and experimental groups. The vector of displacement of the posterior part of the maxilla (as noted at PNS and implant no. 4) was forward and downward. In contrast, the anterior part of the maxilla (as noted at implant no. 3) moved anteriorly with a minimal superior displacement. Furthermore, the overall maxillary displacement in both experimental groups resulted in a much less marked pattern of counterclockwise rotation successively in Group I and Group II. Mandibular
Changes Subsequent to Surgery
The repositioning of the mandible was analyzed by measuring the horizontal and vertical displacement of the mandibular implants (implants no. 5 and 6) and Menton (ME) relative to the implants in
the anterior part of the cranial base. In the horizontal direction, the anterior displacement of ME and both implants showed a consistent increase in both experimental groups at almost each postsurgical interval. However, compared to the control group, the amount of increase at the 12-month period in Group I and Group II was respectively 37% and 59% less for ME, 60% and 73% less for implant no. 5, and 51% and 70% less for implant no. 6 (Figs. 12-14). The differences in anterior displacement of the mandible between the control group and the experimental groups reached significance (P < 0.001) at the first to second month interval, and remained significant throughout the 12-month observation period. Moreover, the mean and rate of anterior displacement is significant more in the control group than in the experimental groups. The mean anterior displacement of the mandible in Group II animals was consistently and significantly less than that of Group I animals by three to four months after surgery. In the vertical direction, the amount and rate of inferior displacement of the mandible was minimal in both experimental Groups I and II, as noted at Menton, implants nos. 5 and 6, in the first six-month interval after surgery (Figs. 15- 17). At the end of the observation period, the percentages of decrease relative to the control group were approximately in the same proportion as in the horizontal direction for both experimental groups. Once again, the mean and rate of inferior displacement was significantly greater in the control group than in the experimental groups. The mean inferior displacement of the mandible in Group II animals was significantly less than that of
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Impbat
No5
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Hotizoatal
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lmplamt No6
Horizontal
FIGURE 12 (top). Distribution pattern and mean change in the horizontal direction at implant no. 5. The pattern of change is similar to implant no. 3 shown in Figure 6.
7.
FIGURE 13 (middle). Distribution pattern and mean change in the horizontal direction of implant no. 6. The pattern and mean curves are similar to those noted for implant no. 5 in Figure 12. FIGURE 14 (bottom). Graph showing distribution pattern and mean horizontal change of Menton. The pattern and mean curves are similar to those noted for implant no. 5 in Figure 12 although both experimental groups show more horizontal displacement with a significant difference between Group I and Group II animals.
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12
3
4
5
6
7
8
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W FIGURE 15 (fop). Distribution pattern and mean change in the vertical direction at implant no. 5. The mean inferior displacement of implant no. 5 is negligible for both experimental groups. FIGURE 16 (middle). Distribution pattern and mean change in the vertical direction of implant no. 6. The pattern of change is similar to implant no. 5 shown in Figure 15 but the amount of mean change is proportionately larger, especially in the control animals. FIGURE 17 (bortom). Graph showing distribution pattern and mean vertical change of Menton. The pattern and mean curves are similar to those noted for implant no. 5 in Figure 15.
No S Vertical
No 6
Vertical
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Group I animals by five to six months after surgery, and approximately 50% less at almost all stages of the observation period. In the control group, the overall displacement of the mandible was counterclockwise. The mandibular corpus was carried anteriorly and inferiorly with a greater vertical component in the posterior region (implant no. 6 vertical compared to implant no. 5 vertical). The mandible underwent a corresponding rotation during growth adaptation in the same counterclockwise manner, but to a lesser extent than the maxillary complex. The amount of vertical differential displacement between the anterior and posterior region of the mandible in both experimental groups was proportionally minimal as compared to the control group. This finding was similar to that of overall maxillary vertical displacement in the experimental groups. Changes of Vertical Facial Height The vertical facial relationships were analyzed by following three measurements: anterior total facial height (ATFH) (distance between implant no. 1 and Menton; anterior upper facial height (AUFH) (distance between implant no. 1 and implant no. 3); and anterior lower facial height (ALFH) (distance between implant no. 3 and Menton). The mean and rate of incremental change in ATFH was significantly more in the control group than those in the experimental groups (P < 0.001). The differences between Group I and Group II animals were not statistically significant (Fig. 18). Although the differences in AUFH were very small between the control and the experimental groups, which reflects the vertical displacement of implant no. 3, only the mean incremental change was significantly more in the control group than in the experimental groups. There is no significant difference between Group I and Group II animals (Fig. 19). The mean and rate of incremental change in ALFH was significantly more in the control than the experimental groups. Group II animals showed a small decrease throughout the 12-month observation period. The mean change in Group II was signiticantly less (P < 0.05) than that in Group I by the first to second month interval (Fig. 20). Overall, the incremental change in anterior facial height of the control group, especially of the lower facial height, was significantly greater than that of the experimental groups. Only the lower facial height in Group II animals was significantly less than that of Group I animals throughout the 12month observation period.
CHANGES
FOLLOWING
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Discussion All experimental animals demonstrated minimal postoperative complications. This is consistent with previously published studies using similar experimental models and surgical procedures. 1,3~15~16 Although maxillomandibular fixation was not used after surgery the experimental animals experienced a mean weight loss of 0.2 kg (10% of body weight). This loss is typical for major surgical procedures, such as the Le Fort I osteotomy, especially when the postsurgical diet is not supplemented with high caloric foods. Even with dietary supplements, a weight loss of 54% one week to 10 days postoperatively is normal.” The impact of the weight loss after surgery on subsequent craniofacial growth would be similar to that involved in clinical situations. Furthermore, by the fourth postsurgical week, all experimental animals had returned to their presurgical weight and subsequently gained weight similar to the control animals. In studies designed to simulate clinical situations, the error associated with experimental measurement, as carefully controlled as it can be, is often increased because of variation in biologic response or difference in stage of development, as in longitudinal growth studies. This error is compounded when experimental conditions vary (for example, magnitude of surgical movement), or when animal repositioning error prevents measurement of the same landmark of interest before and after the experimental treatment, and throughout the observation period. In this study, the same surgeon performed all the osteotomies in an attempt to limit inadvertant treatment variation among animals of the same group. Various aspects of the surgical technique can be expected to affect the subsequent growth changes following maxillary surgery, including the location of the incisions and the method of wound closure, the variation in the size, and location and geometry of the surgical cuts, as well as the magnitude of the surgical movements. Animal repositioning error was minimized during the radiographic procedures by having the same operator position the monkeys in the same cephalostat throughout the study. Moreover, because implant cephalometric studies have the capability of detecting changes in animal head position (due to changes in the distance between right and left implants), a relative level of confidence existed regarding the precision of animal head repositioning during radiographic procedures when the distances between right and left implants were relatively similar. In the control animals, the displacement of the
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-1,
-1,
I FIGURE 18 (top lef). Mean change and distribution pattern of the vertical facial height of the control and experimental monkeys as measured from implant no. 1 to Menton. The experimental animals show two-thirds less growth in the vertical height. The distribution pattern shows that the experimental animals in Group II even showed a decrease in height in the first five months of observation. FIGURE 19 (top right). Mean change and distribution pattern of the upper vertical facial height as measured from implants no. 1 and no. 3. The mean curves show a negligible change in this dimension reflecting the vertical change of implant no. 3, although the distribution pattern shows a wide variation. FIGURE 20 (borrom right). Mean change and distribution pattern of the lower vertical height as measured from implant no. 3 to Menton. The mean curves of the experimental animals show significantly less change than the controls. Although small, the difference between Group I and Group II animals is significant, with a negligible decrease of lower vertical height in Group II animals.
maxilla was in a marked counterclockwise rotation contributed by the differential vertical growth in the anterior and posterior regions; the posterior region displaced downward, whereas the premaxillary region displaced anteriorly and superiorly. This growth pattern is quite similar to that of the rhesus monkey (Macaca mulatta) reported by McNamara et a1.7 With regard to maxillary adaptations after surgery, the most striking and consistent finding was a marked reorientation and a relative decrease of the growth and displacement of the midfacial complex, regardless of whether mandibular autorotation was achieved following surgery. The overall maxillary displacement in both experimental groups was also counterclockwise, similar to the control animals but in a less marked fashion, especially with no appreciable vertical growth at the posterior part of the maxilla. Although the vertical growth at the premaxilla was almost similar to that of the control
group, the horizontal growth was significantly smaller in all experimental animals during the 1% month observation period. The overall effect of maxillary surgery on the growth of the maxillary complex was similar for both experimental groups: in every experimental animal, the growth of the midface was directed anteriorly with a negligible downward relocation. However, Group II animals showed a significant difference in the amount of growth reduction as compared to Group I in the horizontal direction (implant no. 3 horizontal). Previous studies have shown that the nasal septum plays an important role in the anteroinferior growth of the midfacial complex. 18-2oThese studies have used various animals to study the effect of partial or total septal surgery on the growth of the midface,21-23 and all have shown a marked retardation in maxillary growth. In this study, Group II animals showed a significantly greater decrease in the overall maxillary growth than Group I animals, due
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to the more extensive injury to the septovomeral region. In Group I animals, the anterior portion of the nasal septum and the posterior region of the vomer were only sectioned anteroposteriorly and disarticulated from the nasal crest of the maxilla during the surgical procedure to allow for the maxillary advancement. In Group II animals, the septovomeral complex was extensively traumatized during the surgical procedure, and the nasal septum was resected an amount approximately equal to the maxillary impaction. The results of this study, therefore, indicate that the injury to the nasal septum complex may be the cause of the inhibition of maxillary growth and displacement. Furthermore, the differences in maxillary displacement between Groups I and II may implicate that the amount of maxillary growth retardation and reorientation after Le Fort I osteotomy is correlated to the amount of septum resected. Experimental work by Siegel24 involving septal resection and its effects on subsequent facial growth in primates revealed that it influences growth of the midface; its effects depend upon the amount of septum resected and the timing of the resection during growth. The findings of this study are in agreement with the observations of Siegel, as there is evidence indicating that maxillary growth inhibition was more marked among Group II animals who underwent more injury to the septovomeral region (partial septoplasty) than Group I animals. The present results, however, do not fully support the observations of others21-23 that an injury to the septovomeral region dramatically disturbs midfacial growth. Rather, they support the observations of MOSSESand Petrovic and Stutzmann26 that an excision of the nasal septum cartilage retards, but does not stop, the anterior growth of the maxilla. On the basis of our previous primate studies*,9 it can be speculated that a septoplasty performed in an adolescent monkey may disturb the mechanical support provided by the intact nasal septum, and this may cause a permanent or temporary loss of maxillary growth, especially in the posterior part of the maxilla in the vertical direction. Epker et al.27 have recommended that surgical repositioning of the maxilla in children should be performed via complete maxillary alveolar osteotomy, as this procedure requires virtually no septal resection. A maxillary Le Fort I osteotomy traumatizes and disturbs the alignment of the premaxillary and pterygopalatine sutures. It has been shown that sutures play an active role in midfacial growth,28*29 although others have disagreed with the sutural dominance theory.18,30*3’ From the results of this study, it can be speculated that trauma to these sutures
CHANGES
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during maxillary surgery might also contribute to the differences in maxillary growth and displacement seen in the experimental animals. Moreover, the differences between Group I animals (advancement) and Group II animals (impaction) might also be related to the extent of trauma caused by surgery to maxillary sutures. However, Shapiro and Kokich16 have evaluated the maxillary sutures after maxillary osteotomy histologically on three juvenile, Macaca nemestrina and found all the maxillary sutures patent two years after surgery. They concluded that the alteration in the growth direction after maxillary osteotomy was not caused by premature sutural fusion. Changes in the soft tissue envelope around the maxillary complex have also been implicated in the disturbed growth of the midface following maxillary osteotomy in adolescent monkeys. In a study on the effects of Le Fort I osteotomy and maxillary advancement in three juvenile Mucaca nemestrinu with relative maxillary retrusion, Shapiro and Kokich16 concluded that the constraining effects of soft tissue scarring after maxillary osteotomy influenced the direction and amount of subsequent maxillary growth. Moss,” in his functional matrix theory, reported that the oronasal spaces and maxillary sinus also play an important role in the overall growth of the craniofacial complex. A maxillary osteotomy disturbs several functional matrices and the neuromuscular balance of the face. It is worth noting that most of the previous experimental studies have attempted to investigate the effect of a single growth “mechanism” on facial growth. In this study, the surgical procedure performed affected several so-called “growth mechanisms.” Thus, the effects reported here may be cumulative and more representative of the clinical situation. The effective growth of the middle face is the result of a passive displacement of the whole nasomaxillary complex, associated with sutural growth as well as differential deposition and resorption on bony surfaces, and the vertical and horizontal migration of the dentition. 32 As reported by McNamara et al.,7 Nanda et al.,’ and supported by this investigation, the maxillary complex in the adolescent macaque normally grows in a manner relatively similar to that seen in humans, that is, in an anterior and inferior direction relative to the cranial base, yet with a marked and more consistent counterclockwise rotation. Enlow compared facial growth in humans and the rhesus monkey after a histologic study of 11 rapidly growing animals, and he reported some differences in several regional growth patterns between these two primate forms, particularly in the premaxillary and malar regions of the maxillary complex. Although humans and
135
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primates show some differences in shape and size of craniofacial bones, the mechanisms associated with growth and development of the midface and the mandible are similar. Thus, the general principles of growth revealed in experimental studies seem likely to apply to all primates, including man. The experimental studies conducted on adolescent monkeys provide an opportunity to understand the effect of deliberate trauma to various mechanisms associated with the growth of the face. It must be noted however, that the adolescent animals used for maxillary surgery usually have “normal” craniofacial growth, function, and structure for their species, unlike human adolescent patients with severe dentofacial deformities. Ideally, it would be best to use a model system in which natural defects are corrected rather than those in which normal structure and function are made abnormal. The mandibular positional changes in both experimental groups reported in this study coincided with the maxillary growth and displacement. The posterior region of the body of the mandible showed less downward displacement. Similarly, the symphyseal part of the mandible showed less forward and downward displacement. Throughout the IZmonth observation period, the amount and rate of mandibular growth and displacement (as determined cephalometrically) was substantially and significantly decreased in both experimental groups as compared to the control group, regardless of whether mandibular autorotation was achieved following surgery. Moreover, Group II animals (impaction-advancement group) exhibited consistent and significant less mandibular growth than Group I animals (advancement group). The reason the mandible showed less growth and displacement in both experimental groups may be related to the mechanisms regulating the occtusal and neurosensory adjustment. It is possible that the maintenance of an occlusal intercuspal relationship throughout the’observation period and/or neuromuscular adaptation factors may have played a role in the maintenance of coordinated growth of the maxilla and mandible. A significant finding of this experiment was the substantial reduction noted in the increase in vertical facial height over a 1Zmonth period following the maxillary surgical procedure. This reduction was primarily in lower facial height as measured from the premaxilla (implant no. 3) to the lower border of the mandible (Menton). Although statistically significant, the reduction in the upper facial height of the experimental animals was less pronounced than that of the lower facial height. This finding is not contrary to the expected changes in this area of the face following maxillary osteotomy
in the growing adolescent. Epker and colleagues27 reported a substantial decrease in vertical maxillary growth following Le Fort I osteotomy in 16 adolescent patients. They maintain that superior repositioning of the maxilla increased the efficiency of masticatory function, which caused a decrease in vertical maxillary growth. The difference in the lower facial height between Group I and Group II animals was statistically significant. Group II animals exhibited a lower increase in lower facial height than Group I animals. This finding suggests that the suprahyoid group of muscles may not play an active role in the vertical development of lower facial height. The cephalometric results of this longitudinal growth study show that maxillary osteotomy on adolescent nonhuman primates has a significant effect on the subsequent growth of the face. Although the anterior growth of the maxilla and mandible was significantly reduced, the overall growth pattern of the maxilla and mandible was coordinated. This study, although conducted on monkeys, does provide significant information as to the adjustments to growth of the craniofacial complex following total maxillary osteotomy. The findings of this study have important clinical implications. In some growing children, relative maxillary hypoplasia is so severe that early surgical correction is needed to enhance the psychological development as well as to provide balanced oral, functional, speech, and esthetic needs. Furthermore, because the surgical procedure restricts the anterior growth of an already abnormally developing midface, a second operation may be necessary after completion of facial growth. However, maxillary impaction surgery may be the treatmentof-choice in individuals with vertical maxillary excess. As growing individuals with a large vertical dimension usually exhibit a greater amount of vertical maxillary.growth than normal, the reduction in vertical maxillary growth after maxillary impaction surgery can only be beneficial. The results of this study also indicate that total alveolar osteotomy may be the surgery-of-choice in younger individuals when the risks of a reduction in the horizontal maxillary growth are undesirable, because septal resection is not involved.
References 1. Nanda R, Sugawara J, Topazian RG: Effects of maxillary osteotomy on subsequent craniofacial growth in adolescent monkeys. Am J Orthod 83:391. 1983 2. Nanda R, Sugawara J: Mandibular adaptations following total maxillary osteotomy in adolescent monkeys. Am J Orthod 83:485, 1983
CRANIOFACIAL
3. Bouayad 0, Topazian RG, Sachdeva R, et al: Maxillary displacement and rotation following Le Fort I Osteotomy in young monkeys. J Dent Res 63:Abstract #368, 1985 4. Hurme V, Van Wagenen G: Basic data on the emergence of permanent teeth in the rheusus monkey (Macacu ELIlutta). Proc Am Phil Sot 97:291, 1953 5. Hurme V, Van Wagenen G: Basic data on the emergence of permanent teeth in the rhesus monkey (Mucaca mulutra). Proc Am Phil Sot 105:105, 1961 6. McNamara JA Jr, Graber LW: Mandibular growth in the rhesus monkey (Macacu mulartu). Am J Phys Anthropol 42: 15, 1975 I. McNamara JA Jr, Riolo ML, Enlow DH: Growth of the maxillary complex in the rhesus monkey (Mucaca muluttu). Am J Phys Anthropo144: 15, 1976 8. Bjork A: Facial growth in man, studied with the aid of metallic implants. Acta Odont Stand 13:9, 1955 9. Nanda R, Topazian RG: Craniofacial growth following Le Fort I osteotomy in adolescent monkeys, in McNamara JA Jr, Carlson DS, Ribbens KA (eds): The Effects of Surgical Intervention on Craniofacial Growth. Ann Arbor, University of Michigan, 1982, pp 99-129 10. McNamara JA Jr: Neuromuscular and skeletal adaptations to altered orofacial function. Monograph # 1, Craniofacial Growth Series, Center for Human Growth and Development. Ann Arbor, University of Michigan, 1972 11. Nanda R, Legan H: Craniofacial adaptations after total maxillary osteotomy in Mucaca irus: a cephalometric and histologic study. Am J Orthod 73:410, 1978 12. Winer BJ: Statistical Principles in Experimental Design, 2nd ed. New York, McGrawlHill, 1971 Dixon WJ (chief ed). BMDP Statistical Software. 1981. 13. ---~-~~ Berkeley, Ca, University of California Press, 1981 14. Sachs L: Applied Statistics. New York, Springer Verlag, 1980 15. Bell WH: Le Fort I osteotomy for correction of maxillary deformities. J Oral Surg, 33L:412, 1975 16. Shaprio PA, Kokich VG: The effect of Le Fort I osteotomies on the craniofacial growth of juvenile Mucuca nemestrina, in McNamara JA Jr, Carlson DA, Ribbens KA (eds): The Effect of Surgical Intervention on Craniofacial Growth. Ann Arbor, University of Michigan, 1982, p 131 17. Proflitt W, White R: Treatment of severe malocclusions by correlated orthodontic-surgical procedures. Angle Orthod 40: 110, 1970 18. Petrovic AG, Charlier JP, Hermann J: Les mechanismes de croissance du crane: Recherches sur le cartilage de la cloison nasale et sur les sutures craniennes et faciales de
19. 20.
21,
22.
23.
24. 25.
26.
27.
Y~-~
28. 29.
30. 31.
32. 33.
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jeunes rats en cultures d’ organes. Bull Assoc Anat 143: 1376, 1968 Scott JH: The cartilage of the nasal septum. Br Dent J 95:37, 1953 Wexler MR, Samat BG: Rabbit snout growth: effect of injury to septovomeral region. Arch Otolaryngol 74:305, 1961 Hartshom DF: Facial growth effects of nasal septal cartilage resection in beagle pups. Thesis, Department of Otolaryngology and Maxillofacial Surgery, University of Iowa, Iowa City, 1970 Latham RT, Deaton T, Galabrase C: A question of the role of the vomer in the growth of the premaxillary segment. Cleft Palate J 12:351, 1975 Wada T, Kremenak CR, Miyazaki T: Midfacial growth effects of surgical trauma to the area of the vomer in beaeles. J Osaka Univ Dent Sch 20:241, lQ*n Siegel-MI: Mechanisms of early maxillary ‘g;ud;i implications for surgery. J Oral Surg 34:106, 1976 Moss ML: The-role of the nasal septal cartilage in midfacial growth, in McNamara (ed): Factors Affecting the Growth of the Midface. Monograph #6, Craniofacial Growth Series, Center for Human Growth and Developement. Ann Arbor, University of Michigan, 1976 Petrovic AG, Stutzmann J: Le muscle pterygoidien externe et la croissancce du condyle mandibulaire. Orthod Franc 43:271, 1972 Epker NB, Schendel SA, Washburn M: Effects of early surgical superior repositioning of the maxilla and subsequent growth III biomechanical considerations, in McNamara JA Jr, Carlson DA, Ribbens KA (eds): The Effect of Surgical Intervention on Craniofacial Growth. Ann Arbor, University of Michigan, 1982, pp 23 l-250 Weinmann JP, Sicher H: Bones and Bones: Fundamentals of Bone Biology, 2nd edn. London, Henry Kimpton, 1955 Prahl D: Sutural growth: investigation on the growth mechanism of the coronal suture and its relations to cranial growth in the rat. Doctorai Thesis, University of Nymegen, The Netherlands, 1968 Scott JH: Growth of facial sutures. Am J Orthod 42:381, 1956 Moss M: The functional matrix, in Kraus B, Reidel R (eds): Vistas in Orthodontics. Philadelphia, Lea & Febiger, 1952, pp 85-98 Enlow DH: The Human Face. New York, Harper & Row, 1968 Enlow DH: A comparative study of facial growth in Homo and Mucaca. Am J Phys Anthrop 24:293, 1966
Surg
1987
Facial Growth Subsequent to Le Fort Osteotomies in Adolescent Monkeys RAVINDRA
I
NANDA, BDS, MDS, PHD,* OMAR BOUAYAD, DDS, MS, MDENTSCJ AND RICHARD G. TOPAZIAN, DDS$-
The study goal was to assess qualitatively and quantitatively the craniofacial adaptations following total maxillary osteotomy with and without mandibular autorotation. Six adolescent female Macaca fascicularis monkeys were randomly divided into two surgical groups, and eight others served control. Prior to surgery, metallic implants were inserted in the anterior part of the cranial base, on opposite sides of craniofacial sutures, and in multiple sites of the maxilla and mandible. Group I animals underwent a Le Fort I advancement of 4 mm, while Group II animals had a 5mm advancement and a 2.5mm impaction. Lateral cephalometric headfilms were taken at monthly intervals for a total follow-up of 12 months after surgery. At least two cephalograms were taken on each occasion, one with the teeth in occlusion and the other with the mouth wide open. The latter was used to ascertain accurately the outline of the mandibular condyle. Cephalometric superimposition methods were used to quantify the growth changes. The findings indicated that the growth changes in the maxilla and mandible were related to the extent of injury caused by maxillary surgery. The largest increments and rates of growth were observed respectively in the control animals, Group I animals (anterior maxillary repositioning), and Group II animals (anterior and superior maxillary repositioning). The most interesting finding was that mandibular growth pattern followed maxillary growth pattern in both experimental groups, and the immediate postsurgical occlusion in Class II molar relationship was maintained with increased overjet in both experimental groups throughout the postsurgical observation period.
Orthognathic surgery, with or without orthodontic treatment, has gradually become the treatment-ofTchoice to correct moderate to severe dentocraniofacial disharmonies. However, this treatment has been mostly limited to individuals who have completed their active growth. The recommendation to delay surgery in adolescents is based
on a lack of clinical and experimental data regarding the effect of injury caused by surgery on various components of the remaining craniofacial growth. Possible adverse facial growth or skeletal relapse after surgery in adolescents are problematical clinically, primarily because of insufficient understanding of the mechanisms by which bone, muscle, and associated tissues adapt to alterations in structure or function. The purpose of this investigation was to assess quantitatively and qualitatively the craniofacial adaptations that occur subsequent to total maxillary osteotomy with and without mandibular autorotation in actively growing Macaca fuscicularis monkeys. The results of our previous studies,1-3 regarding the craniofacial changes subsequent to surgical superior repositioning of the maxilla, have shown that: I) a surgical insult to the midface in
From the Departments of Orthodontics and Oral and Maxillofacial Surgery, School of Dental Medicine, University of Connecticut, Farmington, Connecticut. * Professor, Department of Orthodontics. t Resident, Department of Orthodontics. $ Professor and Chairman, Department of Oral and Maxillofacial Surgery. Supported by NIDR grant no. DEO5396-05. Address correspondence and reprint requests to Dr. Nanda: Department of Orthodontics, University of Connecticut Health Center. 263 Farmington Avenue, Farmington, CT 06032. 0278-2391187 $0.00 + .25
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growing monkeys did not prevent coordinated growth between the maxilla and the mandible, and 2) the mandible in each experimental animal showed significantly less growth than in the controls, although it was subjected to no surgical intervention. These results warranted further studies to investigate the mandibular response to maxillary surgery and the possible role of mandibular autorotation on the subsequent craniofacial growth following surgery. The specific objectives of this study were to determine: 1) the effects of maxillary surgery on the subsequent growth and development of both maxilla and mandible; 2) the effect of surgical alteration of vertical facial height, and the role of mandibular autorotation, on the subsequent growth of both maxilla and mandible; and 3) the effect of surgical alteration of maxillomandibular sagittal relationship on the subsequent adaptation of mandibular growth. The long-term goals of this investigation were to improve and broaden our understanding of the effects of total maxillary osteotomy with controlled parameters of occlusion and vertical height on the nature of subsequent craniofacial adaptations.
IMPLANTS Tantalum implants were inserted at predetermined areas in certain craniofacial bones to ascertain accurately, with the help of conventional cephalometry, the changes of maxillary and mandibular growth and displacement and the changes of vertical facial height. 6,8,9 The sterile implants, measuring 1.5 mm in length and 0.2 mm in diameter, were inserted in both the left and the right sides of the face. The maxilla and mandible each received, via an intraoral route, one implant in the midline area and at least three implants bilaterally in the area of the canine, permanent first molar, and maxillary tuberosity. Two implants were placed in the midline of the cranial base7J0 and on each side of the zygomaticomaxillary, zygomaticotemporal, zygomaticofrontal, and frontomaxillary sutures through a skin incision. The skin incisions were closed by chromic catgut suture. The maxillary implants were placed clear of the osteotomy site or as superiorly as possible to avoid their loss during the osteotomy. An interval of six to eight weeks was allowed for normal healing of the incisions and stabilization of the implants prior to the osteotomy procedure.
Materials and Methods
SURGERY
ANIMALS
Le Fort I maxillary osteotomies were performed with the animals under general anesthesia.‘s2 A single-stage total maxillary osteotomy (Fig. 1) was performed in all the experimental animals1,2,9J1 followed by a different maxillary repositioning in Group I and Group II animals. The three monkeys in Group I underwent 4 mm of anterior maxillary repositioning with no or minimal autorotation of the mandible and no or minimal reduction of vertical height. The three monkeys in Group II had a S-mm superior and 4-mm anterior maxillary repositioning. The maxilla in both groups was fixed in its final position with transosseous wires placed in the piriform rim and buttress areas; maxillomandibular fixation was not used. The animals were kept on soft, fruit-supplemented diets during the first eight weeks postsurgitally. The experimental animals recovered without any major complications and gained weight similar to the control monkeys.
Fourteen adolescent female Macaca fascicularis monkeys were studied over a 12-month period. Eight animals served as controls, and six were subjected to total maxillary osteotomy. The six experimental monkeys were further subdivided into two groups of three, each group receiving a different maxillary repositioning after total maxillary osteotomy. Because birth dates for these animals were not available and there were no experimental data to assess their developmental age, the age of each monkey was determined by noting the eruption status of the dentition according to the tooth eruption tables of Hurme and Van Wagenen4,5 and the classification of McNamara and Graber.6 The age of the control monkeys ranged from 30 to 39 months, and that of the experimental monkeys from 31 to 41 months. All monkeys had their permanent first molars, and the permanent lateral and central incisors in occlusion; the first and second premolars were at various stages of eruption. At the start of the experiments, the weight of all animals ranged from 1.9 to 2.1 kg. All monkeys were termed adolescent according to the classification of McNamara et a1.6T7
CEPHALOMETRICANALYSIS Serial lateral cephalometric headfilms of all monkeys were taken prior to and immediately after metallic implant placement, immediately after the
NANDA ET AL.
FIGURE 1. Diagrammatic representation of Le Fort I advancement and impaction osteotomy sites shown in lateral views.
appropriate surgical procedure, and every four weeks thereafter during the 12-month postsurgical period. The anatomic landmarks, position of the metallic implants and the teeth used to describe the changes of growth and displacement, together with the changes of vertical facial height are shown in Figure 2. For the purposes of this study, anterior cranial base superimposition was used to analyze and quantify the craniofacial changes and displacement with surgery and growth. In addition, the changes of vertical facial height were assessed by direct measurements on each cephalogram. The cephalometric analysis performed has been described in detail by Nanda et al.i+2 The displacement of the six maxillary and man-
dibular anatomic landmarks and implants was measured to the nearest 0.5 mm horizontally and vertically. The successive outline tracings of the craniofacial complex were used only for descriptive purposes, while vertical and horizontal measurements were made directly on the successive cephalograms themselves with the help of the initial tracing. This procedure allowed for direct quantification of various small changes in craniofacial dimension which normally might be masked by tracing errors, especially in the first months. Obviously, the shorter the interval between headfilms, the greater is the likelihood that the magnitude of the measurement errors would approximate, or even exceed, the actual growth changes. The vertical facial relationships, as noted by three different measurements, were analyzed by direct measurement on each cephalogram with the teeth in occlusion. The absolute growth changes of the three following distances were measured to the nearest 0.5 mm on all successive cephalograms: anterior total facial height (distance from implant no. 1 to Menton); anterior upper facial height (distance from implant no. 1 to implant no. 3); and anterior lower facial height (distance from implant no. 3 to Menton). Data Analysis
FIGURE 2. Landmarks, implants and coordinate planes used to measure the craniofacial growth with anterior cranial base superimposition. I. anterior cranial base implant; 3, premaxillary implant; 4, posterior maxillary implant; 5. anterior mandibular implant; 6, posterior mandibular implant; PNS, posterior nasal spine; ME, mention; X axis, occlusal plan; Y axis drawn from point of intersection of occlusal plane with the anterior border of the ramus.
The quantitative data from various cephalometric measurements were analyzed using a factorial repeated-measures analysis of variance (ANOVA) design. This particular choice was dictated by the format of the longitudinal growth data. The repeated-measures ANOVA design used in this study is described at length by Winer.** The computational algorithm was provided by BMDP statistical
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the rate of change (growth or displacement) ferent between the groups examined.
is dif-
REPRODUCIBILITY
CadreI 6-80 --uy
FIGURE 3. Cephalometric tracings with cranial base superimposition of a representative adolescent control monkey showing dentocraniofacial changes following three, six, nine and 12 months of observation. Note the counterclockwise growth of the maxilla. Both the maxilla and the mandible show substantial growth during the observation period.
computing package. l3 The program partitions the total error variance into a component due to within subjects variation (that is, changes in subjects over time), a component due to between subjects (groups, for example, control group versus experimental groups), and finally, a component due to subject by factor interaction. By extracting the error variance due to within subjects variation, the model validates the comparison of group means over time and makes it possible to test for group effects. As in the usual ANOVA methodology, standard multiple comparison procedures can be used to detect differences between given pairs of means. The computer program used to perform the repeated-measures ANOVA was designed to yield weighted estimates of experimental effects, to account for the different numbers of animals in the control and experimental groups. A significant group effect indicates that the two overall group means are different. The initial time point at which differences between group means became statistically significant was determined by use of the Scheffe multiple comparisons procedure.14 A significant time effect implies that the mean measurements change significantly over time. It should be pointed out that the 12 time points (12-month observation period) have been pooled to six time points: that is, the means were compared at two-month interval periods by pooling the first two means, the second two means, etc. A significant time by group interaction implies that the groups are changing in different ways over time. In other words, a significant interaction indicates that
A combined determination of both cephalometric landmark location and measurement error was calculated. Twelve cephalograms were randomly selected: six with the teeth in occlusion and six with the mouth held wide open. All landmarks were identified on four separate occasions under the same standard conditions. The landmarks to be identified as well as the distances to be measured were not the same for the two types of headfilms used in this study. The 48 combined tracings were then “digitized” manually, and the location of the landmarks was recorded in both the horizontal and vertical direction. For the six headfilms with the teeth in occlusion, the mean combined error of the landmarks in the horizontal plane was 0.21 mm (SD = 0.04 mm), and in the vertical plane the mean combined error was 0.13 mm (SD = 0.02 mm). For the six headfilms with the mouth in open position the mean combined error of the landmarks in the horizontal plane was 0.19 mm (SD = 0.03 mm), and in the vertical plane it was 0.15 mm (SD = 0.05 mm). Results The insertion of implants was performed without any complications. All incisions healed completely prior to the osteotomy procedures, and the implants remained stable through the 12-month observation period. The experimental animals tolerated the surgical procedures well and did not experience any major postsurgical complications, despite the fact that maxillomandibular fixation was not used. The healing of the maxilla was uneventful and bone stability was noted six to eight weeks after surgery. All animals lost weight immediately following maxillary surgery; the mean weight loss was 0.2 kg (approximately 10% of their body weight). By the fourth postsurgical week, all animals had returned to their presurgical weight and subsequently gained weight similar to the control monkeys. The eight control adolescent .monkeys remained in good health and exhibited significant amounts of growth changes during the 1Zmonth observation period (Fig. 3). The overall direction and pattern of craniofacial growth were found to be similar in all the control animals. Their initial Class I occlusal relationship was maintained during the entire observation period and all animals maintained normal over-jet (0 to 1.5 mm) and overbite (0 to 1.O mm).
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Expaimdd
II a-83
FIGURE 4 (left). Composite tracings of an experimental animal in Group 1 superimposed on the anterior cranial base showing craniofacial growth changes noted three, six, nine and 12 months following maxillary advancement. Note the differences in the amount and direction of facial growth as compared to control monkeys of approximately similar age shown in Figure 3. Composite tracings of an experimental animal in Group II superimposed on the anterior cranial base showing craniofacial growth changes noted three, six, nine and 12 months following maxillary advancement and impaction. Note the differences in the amount and direction of facial growth as compared to experimental monkeys in Group 1 shown in Figure 4. FIGURE 5 (right).
CHANGES IMMEDIATELY AFTER SURGERY
To determine the amount of surgical repositioning of the maxilla and accompanying changes of the mandible, the cephalometric measurements taken immediately before and after the surgery were compared. These measurements were made relative to the coordinate system previously described’,* and were established on the presurgical cephalometric tracing of each animal. Although a maxillary advancement of 4 mm was planned for all animals in Group 1, one monkey had only a 1.5mm advancement. Consequently, the postsurgical occlusion was left 1.5 mm in Class II with an increased ovetjet of 1 mm. The two other monkeys had a maxillary advancement of 4 mm with an increased overjet of 3.25 + 0.25 mm. In the vertical direction, the mean amount of impaction in Group I was 0.75 t 0.25 mm anteriorly and 0.5 mm posteriorly, which was the anticipated movement. A mean 4 mm (& 0.5 mm) of superior repositioning and a mean of 5.25 mm ( + 0.25 mm) of anterior repositioning were reached after surgery in Group II animals. The repositioning of the posterior end of the maxilla was noted by measuring the horizontal and vertical displacement at the posterior nasal spine (PNS); it showed a mean superior repositioning of 2.5 mm. The overall repositioning of the maxilla following surgery in Group II resulted in a marked counterclockwise rotation with a
relatively larger amount than in Group I.
of anterior
displacement
Maxillary Changes Subsequent to Surgery The changes in maxillary growth were determined by measuring the positions of the maxillary implants (implants no. 3 and no. 4) and PNS relative to the implants in the anterior part of the cranial base (Figs. 4, 5). Only the positional changes of the maxilla are reported in this study. Growth and remodeling changes within the maxilla based on superimposition of the maxillary implants were not assessed quantitatively, because of the possible error induced by the lack of reliable and reproducible maxillary anatomic landmarks and the degree to which the maxilla contrasts with the surrounding area. Two months after surgery, the experimental Group II animals did not show any horizontal change at implant no. 3 (Fig. 6). Until seven months following surgery, the anterior displacement of the maxilla was only 0.5 mm. The mean anterior displacement of the premaxilla in the experimental Groups I and II was 37% and 67% less, respectively, than in the control group 12 months after surgery. The differences in anterior displacement of the premaxilla between the experimental groups and the control group reached significance (P <
CRANIOFACIAL
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6
6
FIGURE 6 (top lefr). Distribution pattern and mean change with standard deviation in the horizontal position of no. 3 of control, Group I and Group II animals during the 12-month period following maxillary osteotomy. The displacement of implant no. 3 of the experimental animals is less at each observation period, Group II animals showing less displacement than Group I animals. FIGURE 7 (top righ?). Distribution pattern and approximately control and experimental monkeys.
the same mean change in the vertical position of implant no. 3 in the
FIGURE 8 (bottom left). Distribution pattern and mean change in the horizontal direction at implant no. 4 in the control and experimental animals. No significant difference between Group I and Group II animals. FIGURE 9 (bottom right). Distribution pattern and mean change in the horizontal direction of PNS in the control and experimental animals. After four months, there is a significant difference between the control and the experimental monkeys.
0.001) at the first to second month interval, and remained significant throughout the 12-month observation period. The rate of anterior displacement was also different between the three groups. The mean anterior displacement of the premaxilla in Group II was 50% less than that in Group I at almost all stages of period; this difference became statistically significant three to four months after surgery. The mean superior displacement at implant no. 3 (Fig. 7) was less than 1 mm in all groups 12 months after surgery. The differences were not statistically significant between the three groups. The mean horizontal displacement of the posterior maxilla as noted at implant no. 4 or PNS was small (
4 than for PNS (Figs. 8, 9) although both showed a significant difference and a significant time by group interaction. The mean vertical displacement of implant no. 4 and PNS was less than 1 mm in both experimental groups in a downward direction (Figs. 10, ll), and the difference between Group I and II was statistically significant only for implant no. 4, which exhibited a small temporary superior displacement during the first four months after surgery in Group II animals. The finding was significantly different in the control group animals, which consistently showed a substantial downward displacement at both implant no. 4 and PNS. A signiticant difference (Z’ < 0.001) between the control and the experimental groups was reached very early (first to second month) with a significant time by group interaction. The horizontal displacement of the maxilla was
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NANDA ET AL..
_-t-j_
‘-i__jurgiul
I
_,
-5. -5~ I
I
FIGURE 10 (left). Distribution pattern and mean change in the vertical direction at implant no. 4 in the control and experimental animals.The displacementof implant no. 4 in the controls is in the inferior direction whereas almost negligible change is noted with the experimental
animals. Although small, there is a significant difference between Group I and Group II animals.
FIGURE 11 (right). Distribution pattern and mean change in the vertical direction of PNS. The pattern of change is similar to implant no. 4 shown in Figure 10.
more prominent than the vertical displacement in the three groups, except for PNS. In the horizontal direction, the amount and rate of maxillary displacement was significantly less in both experimental groups as compared to the control group. Moreover, the mean horizontal displacement in Group II animals was consistently less than that of Group I animals, especially at the premaxilla. In the vertical direction, the amount and rate of maxillary displacement was also significantly less in both experimental groups as compared to the control group, particularly at the posterior part of the maxilla. The difference between Groups I and II was significant only for implant no. 4. Of particular significance was the consistent counterclockwise rotation of the maxillary complex in both control and experimental groups. The vector of displacement of the posterior part of the maxilla (as noted at PNS and implant no. 4) was forward and downward. In contrast, the anterior part of the maxilla (as noted at implant no. 3) moved anteriorly with a minimal superior displacement. Furthermore, the overall maxillary displacement in both experimental groups resulted in a much less marked pattern of counterclockwise rotation successively in Group I and Group II. Mandibular
Changes Subsequent to Surgery
The repositioning of the mandible was analyzed by measuring the horizontal and vertical displacement of the mandibular implants (implants no. 5 and 6) and Menton (ME) relative to the implants in
the anterior part of the cranial base. In the horizontal direction, the anterior displacement of ME and both implants showed a consistent increase in both experimental groups at almost each postsurgical interval. However, compared to the control group, the amount of increase at the 12-month period in Group I and Group II was respectively 37% and 59% less for ME, 60% and 73% less for implant no. 5, and 51% and 70% less for implant no. 6 (Figs. 12-14). The differences in anterior displacement of the mandible between the control group and the experimental groups reached significance (P < 0.001) at the first to second month interval, and remained significant throughout the 12-month observation period. Moreover, the mean and rate of anterior displacement is significant more in the control group than in the experimental groups. The mean anterior displacement of the mandible in Group II animals was consistently and significantly less than that of Group I animals by three to four months after surgery. In the vertical direction, the amount and rate of inferior displacement of the mandible was minimal in both experimental Groups I and II, as noted at Menton, implants nos. 5 and 6, in the first six-month interval after surgery (Figs. 15- 17). At the end of the observation period, the percentages of decrease relative to the control group were approximately in the same proportion as in the horizontal direction for both experimental groups. Once again, the mean and rate of inferior displacement was significantly greater in the control group than in the experimental groups. The mean inferior displacement of the mandible in Group II animals was significantly less than that of
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Impbat
No5
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Hotizoatal
6-
mm)
lmplamt No6
Horizontal
FIGURE 12 (top). Distribution pattern and mean change in the horizontal direction at implant no. 5. The pattern of change is similar to implant no. 3 shown in Figure 6.
7.
FIGURE 13 (middle). Distribution pattern and mean change in the horizontal direction of implant no. 6. The pattern and mean curves are similar to those noted for implant no. 5 in Figure 12. FIGURE 14 (bottom). Graph showing distribution pattern and mean horizontal change of Menton. The pattern and mean curves are similar to those noted for implant no. 5 in Figure 12 although both experimental groups show more horizontal displacement with a significant difference between Group I and Group II animals.
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3
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7
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9
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W FIGURE 15 (fop). Distribution pattern and mean change in the vertical direction at implant no. 5. The mean inferior displacement of implant no. 5 is negligible for both experimental groups. FIGURE 16 (middle). Distribution pattern and mean change in the vertical direction of implant no. 6. The pattern of change is similar to implant no. 5 shown in Figure 15 but the amount of mean change is proportionately larger, especially in the control animals. FIGURE 17 (bortom). Graph showing distribution pattern and mean vertical change of Menton. The pattern and mean curves are similar to those noted for implant no. 5 in Figure 15.
No S Vertical
No 6
Vertical
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Group I animals by five to six months after surgery, and approximately 50% less at almost all stages of the observation period. In the control group, the overall displacement of the mandible was counterclockwise. The mandibular corpus was carried anteriorly and inferiorly with a greater vertical component in the posterior region (implant no. 6 vertical compared to implant no. 5 vertical). The mandible underwent a corresponding rotation during growth adaptation in the same counterclockwise manner, but to a lesser extent than the maxillary complex. The amount of vertical differential displacement between the anterior and posterior region of the mandible in both experimental groups was proportionally minimal as compared to the control group. This finding was similar to that of overall maxillary vertical displacement in the experimental groups. Changes of Vertical Facial Height The vertical facial relationships were analyzed by following three measurements: anterior total facial height (ATFH) (distance between implant no. 1 and Menton; anterior upper facial height (AUFH) (distance between implant no. 1 and implant no. 3); and anterior lower facial height (ALFH) (distance between implant no. 3 and Menton). The mean and rate of incremental change in ATFH was significantly more in the control group than those in the experimental groups (P < 0.001). The differences between Group I and Group II animals were not statistically significant (Fig. 18). Although the differences in AUFH were very small between the control and the experimental groups, which reflects the vertical displacement of implant no. 3, only the mean incremental change was significantly more in the control group than in the experimental groups. There is no significant difference between Group I and Group II animals (Fig. 19). The mean and rate of incremental change in ALFH was significantly more in the control than the experimental groups. Group II animals showed a small decrease throughout the 12-month observation period. The mean change in Group II was signiticantly less (P < 0.05) than that in Group I by the first to second month interval (Fig. 20). Overall, the incremental change in anterior facial height of the control group, especially of the lower facial height, was significantly greater than that of the experimental groups. Only the lower facial height in Group II animals was significantly less than that of Group I animals throughout the 12month observation period.
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Discussion All experimental animals demonstrated minimal postoperative complications. This is consistent with previously published studies using similar experimental models and surgical procedures. 1,3~15~16 Although maxillomandibular fixation was not used after surgery the experimental animals experienced a mean weight loss of 0.2 kg (10% of body weight). This loss is typical for major surgical procedures, such as the Le Fort I osteotomy, especially when the postsurgical diet is not supplemented with high caloric foods. Even with dietary supplements, a weight loss of 54% one week to 10 days postoperatively is normal.” The impact of the weight loss after surgery on subsequent craniofacial growth would be similar to that involved in clinical situations. Furthermore, by the fourth postsurgical week, all experimental animals had returned to their presurgical weight and subsequently gained weight similar to the control animals. In studies designed to simulate clinical situations, the error associated with experimental measurement, as carefully controlled as it can be, is often increased because of variation in biologic response or difference in stage of development, as in longitudinal growth studies. This error is compounded when experimental conditions vary (for example, magnitude of surgical movement), or when animal repositioning error prevents measurement of the same landmark of interest before and after the experimental treatment, and throughout the observation period. In this study, the same surgeon performed all the osteotomies in an attempt to limit inadvertant treatment variation among animals of the same group. Various aspects of the surgical technique can be expected to affect the subsequent growth changes following maxillary surgery, including the location of the incisions and the method of wound closure, the variation in the size, and location and geometry of the surgical cuts, as well as the magnitude of the surgical movements. Animal repositioning error was minimized during the radiographic procedures by having the same operator position the monkeys in the same cephalostat throughout the study. Moreover, because implant cephalometric studies have the capability of detecting changes in animal head position (due to changes in the distance between right and left implants), a relative level of confidence existed regarding the precision of animal head repositioning during radiographic procedures when the distances between right and left implants were relatively similar. In the control animals, the displacement of the
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-1,
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I FIGURE 18 (top lef). Mean change and distribution pattern of the vertical facial height of the control and experimental monkeys as measured from implant no. 1 to Menton. The experimental animals show two-thirds less growth in the vertical height. The distribution pattern shows that the experimental animals in Group II even showed a decrease in height in the first five months of observation. FIGURE 19 (top right). Mean change and distribution pattern of the upper vertical facial height as measured from implants no. 1 and no. 3. The mean curves show a negligible change in this dimension reflecting the vertical change of implant no. 3, although the distribution pattern shows a wide variation. FIGURE 20 (borrom right). Mean change and distribution pattern of the lower vertical height as measured from implant no. 3 to Menton. The mean curves of the experimental animals show significantly less change than the controls. Although small, the difference between Group I and Group II animals is significant, with a negligible decrease of lower vertical height in Group II animals.
maxilla was in a marked counterclockwise rotation contributed by the differential vertical growth in the anterior and posterior regions; the posterior region displaced downward, whereas the premaxillary region displaced anteriorly and superiorly. This growth pattern is quite similar to that of the rhesus monkey (Macaca mulatta) reported by McNamara et a1.7 With regard to maxillary adaptations after surgery, the most striking and consistent finding was a marked reorientation and a relative decrease of the growth and displacement of the midfacial complex, regardless of whether mandibular autorotation was achieved following surgery. The overall maxillary displacement in both experimental groups was also counterclockwise, similar to the control animals but in a less marked fashion, especially with no appreciable vertical growth at the posterior part of the maxilla. Although the vertical growth at the premaxilla was almost similar to that of the control
group, the horizontal growth was significantly smaller in all experimental animals during the 1% month observation period. The overall effect of maxillary surgery on the growth of the maxillary complex was similar for both experimental groups: in every experimental animal, the growth of the midface was directed anteriorly with a negligible downward relocation. However, Group II animals showed a significant difference in the amount of growth reduction as compared to Group I in the horizontal direction (implant no. 3 horizontal). Previous studies have shown that the nasal septum plays an important role in the anteroinferior growth of the midfacial complex. 18-2oThese studies have used various animals to study the effect of partial or total septal surgery on the growth of the midface,21-23 and all have shown a marked retardation in maxillary growth. In this study, Group II animals showed a significantly greater decrease in the overall maxillary growth than Group I animals, due
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to the more extensive injury to the septovomeral region. In Group I animals, the anterior portion of the nasal septum and the posterior region of the vomer were only sectioned anteroposteriorly and disarticulated from the nasal crest of the maxilla during the surgical procedure to allow for the maxillary advancement. In Group II animals, the septovomeral complex was extensively traumatized during the surgical procedure, and the nasal septum was resected an amount approximately equal to the maxillary impaction. The results of this study, therefore, indicate that the injury to the nasal septum complex may be the cause of the inhibition of maxillary growth and displacement. Furthermore, the differences in maxillary displacement between Groups I and II may implicate that the amount of maxillary growth retardation and reorientation after Le Fort I osteotomy is correlated to the amount of septum resected. Experimental work by Siegel24 involving septal resection and its effects on subsequent facial growth in primates revealed that it influences growth of the midface; its effects depend upon the amount of septum resected and the timing of the resection during growth. The findings of this study are in agreement with the observations of Siegel, as there is evidence indicating that maxillary growth inhibition was more marked among Group II animals who underwent more injury to the septovomeral region (partial septoplasty) than Group I animals. The present results, however, do not fully support the observations of others21-23 that an injury to the septovomeral region dramatically disturbs midfacial growth. Rather, they support the observations of MOSSESand Petrovic and Stutzmann26 that an excision of the nasal septum cartilage retards, but does not stop, the anterior growth of the maxilla. On the basis of our previous primate studies*,9 it can be speculated that a septoplasty performed in an adolescent monkey may disturb the mechanical support provided by the intact nasal septum, and this may cause a permanent or temporary loss of maxillary growth, especially in the posterior part of the maxilla in the vertical direction. Epker et al.27 have recommended that surgical repositioning of the maxilla in children should be performed via complete maxillary alveolar osteotomy, as this procedure requires virtually no septal resection. A maxillary Le Fort I osteotomy traumatizes and disturbs the alignment of the premaxillary and pterygopalatine sutures. It has been shown that sutures play an active role in midfacial growth,28*29 although others have disagreed with the sutural dominance theory.18,30*3’ From the results of this study, it can be speculated that trauma to these sutures
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during maxillary surgery might also contribute to the differences in maxillary growth and displacement seen in the experimental animals. Moreover, the differences between Group I animals (advancement) and Group II animals (impaction) might also be related to the extent of trauma caused by surgery to maxillary sutures. However, Shapiro and Kokich16 have evaluated the maxillary sutures after maxillary osteotomy histologically on three juvenile, Macaca nemestrina and found all the maxillary sutures patent two years after surgery. They concluded that the alteration in the growth direction after maxillary osteotomy was not caused by premature sutural fusion. Changes in the soft tissue envelope around the maxillary complex have also been implicated in the disturbed growth of the midface following maxillary osteotomy in adolescent monkeys. In a study on the effects of Le Fort I osteotomy and maxillary advancement in three juvenile Mucaca nemestrinu with relative maxillary retrusion, Shapiro and Kokich16 concluded that the constraining effects of soft tissue scarring after maxillary osteotomy influenced the direction and amount of subsequent maxillary growth. Moss,” in his functional matrix theory, reported that the oronasal spaces and maxillary sinus also play an important role in the overall growth of the craniofacial complex. A maxillary osteotomy disturbs several functional matrices and the neuromuscular balance of the face. It is worth noting that most of the previous experimental studies have attempted to investigate the effect of a single growth “mechanism” on facial growth. In this study, the surgical procedure performed affected several so-called “growth mechanisms.” Thus, the effects reported here may be cumulative and more representative of the clinical situation. The effective growth of the middle face is the result of a passive displacement of the whole nasomaxillary complex, associated with sutural growth as well as differential deposition and resorption on bony surfaces, and the vertical and horizontal migration of the dentition. 32 As reported by McNamara et al.,7 Nanda et al.,’ and supported by this investigation, the maxillary complex in the adolescent macaque normally grows in a manner relatively similar to that seen in humans, that is, in an anterior and inferior direction relative to the cranial base, yet with a marked and more consistent counterclockwise rotation. Enlow compared facial growth in humans and the rhesus monkey after a histologic study of 11 rapidly growing animals, and he reported some differences in several regional growth patterns between these two primate forms, particularly in the premaxillary and malar regions of the maxillary complex. Although humans and
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primates show some differences in shape and size of craniofacial bones, the mechanisms associated with growth and development of the midface and the mandible are similar. Thus, the general principles of growth revealed in experimental studies seem likely to apply to all primates, including man. The experimental studies conducted on adolescent monkeys provide an opportunity to understand the effect of deliberate trauma to various mechanisms associated with the growth of the face. It must be noted however, that the adolescent animals used for maxillary surgery usually have “normal” craniofacial growth, function, and structure for their species, unlike human adolescent patients with severe dentofacial deformities. Ideally, it would be best to use a model system in which natural defects are corrected rather than those in which normal structure and function are made abnormal. The mandibular positional changes in both experimental groups reported in this study coincided with the maxillary growth and displacement. The posterior region of the body of the mandible showed less downward displacement. Similarly, the symphyseal part of the mandible showed less forward and downward displacement. Throughout the IZmonth observation period, the amount and rate of mandibular growth and displacement (as determined cephalometrically) was substantially and significantly decreased in both experimental groups as compared to the control group, regardless of whether mandibular autorotation was achieved following surgery. Moreover, Group II animals (impaction-advancement group) exhibited consistent and significant less mandibular growth than Group I animals (advancement group). The reason the mandible showed less growth and displacement in both experimental groups may be related to the mechanisms regulating the occtusal and neurosensory adjustment. It is possible that the maintenance of an occlusal intercuspal relationship throughout the’observation period and/or neuromuscular adaptation factors may have played a role in the maintenance of coordinated growth of the maxilla and mandible. A significant finding of this experiment was the substantial reduction noted in the increase in vertical facial height over a 1Zmonth period following the maxillary surgical procedure. This reduction was primarily in lower facial height as measured from the premaxilla (implant no. 3) to the lower border of the mandible (Menton). Although statistically significant, the reduction in the upper facial height of the experimental animals was less pronounced than that of the lower facial height. This finding is not contrary to the expected changes in this area of the face following maxillary osteotomy
in the growing adolescent. Epker and colleagues27 reported a substantial decrease in vertical maxillary growth following Le Fort I osteotomy in 16 adolescent patients. They maintain that superior repositioning of the maxilla increased the efficiency of masticatory function, which caused a decrease in vertical maxillary growth. The difference in the lower facial height between Group I and Group II animals was statistically significant. Group II animals exhibited a lower increase in lower facial height than Group I animals. This finding suggests that the suprahyoid group of muscles may not play an active role in the vertical development of lower facial height. The cephalometric results of this longitudinal growth study show that maxillary osteotomy on adolescent nonhuman primates has a significant effect on the subsequent growth of the face. Although the anterior growth of the maxilla and mandible was significantly reduced, the overall growth pattern of the maxilla and mandible was coordinated. This study, although conducted on monkeys, does provide significant information as to the adjustments to growth of the craniofacial complex following total maxillary osteotomy. The findings of this study have important clinical implications. In some growing children, relative maxillary hypoplasia is so severe that early surgical correction is needed to enhance the psychological development as well as to provide balanced oral, functional, speech, and esthetic needs. Furthermore, because the surgical procedure restricts the anterior growth of an already abnormally developing midface, a second operation may be necessary after completion of facial growth. However, maxillary impaction surgery may be the treatmentof-choice in individuals with vertical maxillary excess. As growing individuals with a large vertical dimension usually exhibit a greater amount of vertical maxillary.growth than normal, the reduction in vertical maxillary growth after maxillary impaction surgery can only be beneficial. The results of this study also indicate that total alveolar osteotomy may be the surgery-of-choice in younger individuals when the risks of a reduction in the horizontal maxillary growth are undesirable, because septal resection is not involved.
References 1. Nanda R, Sugawara J, Topazian RG: Effects of maxillary osteotomy on subsequent craniofacial growth in adolescent monkeys. Am J Orthod 83:391. 1983 2. Nanda R, Sugawara J: Mandibular adaptations following total maxillary osteotomy in adolescent monkeys. Am J Orthod 83:485, 1983
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3. Bouayad 0, Topazian RG, Sachdeva R, et al: Maxillary displacement and rotation following Le Fort I Osteotomy in young monkeys. J Dent Res 63:Abstract #368, 1985 4. Hurme V, Van Wagenen G: Basic data on the emergence of permanent teeth in the rheusus monkey (Macacu ELIlutta). Proc Am Phil Sot 97:291, 1953 5. Hurme V, Van Wagenen G: Basic data on the emergence of permanent teeth in the rhesus monkey (Mucaca mulutra). Proc Am Phil Sot 105:105, 1961 6. McNamara JA Jr, Graber LW: Mandibular growth in the rhesus monkey (Macacu mulartu). Am J Phys Anthropol 42: 15, 1975 I. McNamara JA Jr, Riolo ML, Enlow DH: Growth of the maxillary complex in the rhesus monkey (Mucaca muluttu). Am J Phys Anthropo144: 15, 1976 8. Bjork A: Facial growth in man, studied with the aid of metallic implants. Acta Odont Stand 13:9, 1955 9. Nanda R, Topazian RG: Craniofacial growth following Le Fort I osteotomy in adolescent monkeys, in McNamara JA Jr, Carlson DS, Ribbens KA (eds): The Effects of Surgical Intervention on Craniofacial Growth. Ann Arbor, University of Michigan, 1982, pp 99-129 10. McNamara JA Jr: Neuromuscular and skeletal adaptations to altered orofacial function. Monograph # 1, Craniofacial Growth Series, Center for Human Growth and Development. Ann Arbor, University of Michigan, 1972 11. Nanda R, Legan H: Craniofacial adaptations after total maxillary osteotomy in Mucaca irus: a cephalometric and histologic study. Am J Orthod 73:410, 1978 12. Winer BJ: Statistical Principles in Experimental Design, 2nd ed. New York, McGrawlHill, 1971 Dixon WJ (chief ed). BMDP Statistical Software. 1981. 13. ---~-~~ Berkeley, Ca, University of California Press, 1981 14. Sachs L: Applied Statistics. New York, Springer Verlag, 1980 15. Bell WH: Le Fort I osteotomy for correction of maxillary deformities. J Oral Surg, 33L:412, 1975 16. Shaprio PA, Kokich VG: The effect of Le Fort I osteotomies on the craniofacial growth of juvenile Mucuca nemestrina, in McNamara JA Jr, Carlson DA, Ribbens KA (eds): The Effect of Surgical Intervention on Craniofacial Growth. Ann Arbor, University of Michigan, 1982, p 131 17. Proflitt W, White R: Treatment of severe malocclusions by correlated orthodontic-surgical procedures. Angle Orthod 40: 110, 1970 18. Petrovic AG, Charlier JP, Hermann J: Les mechanismes de croissance du crane: Recherches sur le cartilage de la cloison nasale et sur les sutures craniennes et faciales de
19. 20.
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28. 29.
30. 31.
32. 33.
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jeunes rats en cultures d’ organes. Bull Assoc Anat 143: 1376, 1968 Scott JH: The cartilage of the nasal septum. Br Dent J 95:37, 1953 Wexler MR, Samat BG: Rabbit snout growth: effect of injury to septovomeral region. Arch Otolaryngol 74:305, 1961 Hartshom DF: Facial growth effects of nasal septal cartilage resection in beagle pups. Thesis, Department of Otolaryngology and Maxillofacial Surgery, University of Iowa, Iowa City, 1970 Latham RT, Deaton T, Galabrase C: A question of the role of the vomer in the growth of the premaxillary segment. Cleft Palate J 12:351, 1975 Wada T, Kremenak CR, Miyazaki T: Midfacial growth effects of surgical trauma to the area of the vomer in beaeles. J Osaka Univ Dent Sch 20:241, lQ*n Siegel-MI: Mechanisms of early maxillary ‘g;ud;i implications for surgery. J Oral Surg 34:106, 1976 Moss ML: The-role of the nasal septal cartilage in midfacial growth, in McNamara (ed): Factors Affecting the Growth of the Midface. Monograph #6, Craniofacial Growth Series, Center for Human Growth and Developement. Ann Arbor, University of Michigan, 1976 Petrovic AG, Stutzmann J: Le muscle pterygoidien externe et la croissancce du condyle mandibulaire. Orthod Franc 43:271, 1972 Epker NB, Schendel SA, Washburn M: Effects of early surgical superior repositioning of the maxilla and subsequent growth III biomechanical considerations, in McNamara JA Jr, Carlson DA, Ribbens KA (eds): The Effect of Surgical Intervention on Craniofacial Growth. Ann Arbor, University of Michigan, 1982, pp 23 l-250 Weinmann JP, Sicher H: Bones and Bones: Fundamentals of Bone Biology, 2nd edn. London, Henry Kimpton, 1955 Prahl D: Sutural growth: investigation on the growth mechanism of the coronal suture and its relations to cranial growth in the rat. Doctorai Thesis, University of Nymegen, The Netherlands, 1968 Scott JH: Growth of facial sutures. Am J Orthod 42:381, 1956 Moss M: The functional matrix, in Kraus B, Reidel R (eds): Vistas in Orthodontics. Philadelphia, Lea & Febiger, 1952, pp 85-98 Enlow DH: The Human Face. New York, Harper & Row, 1968 Enlow DH: A comparative study of facial growth in Homo and Mucaca. Am J Phys Anthrop 24:293, 1966