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Department of Oral Sciences, Faculty of Dentistry, University of Otago, PO Box 647, Dunedin, New Zealand; murray.meikle{at}z
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONFACIAL SUTURESREMODELING THE MAXILLA IN...CLINICAL REMODELING OF THE...EXPERIMENTAL REMODELING OF THE...IS CONDYLAR CARTILAGE UNIQUE?CLINICAL REMODELING OF THE...REFERENCES |
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KEY WORDS: facial sutures • temporomandibular joint • condylar cartilage • articular remodeling • functional appliances
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONFACIAL SUTURESREMODELING THE MAXILLA IN...CLINICAL REMODELING OF THE...EXPERIMENTAL REMODELING OF THE...IS CONDYLAR CARTILAGE UNIQUE?CLINICAL REMODELING OF THE...REFERENCES |
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Numerous well-documented animal studies have also showed that craniofacial sutures, as well as the TMJs, can be remodeled by externally applied mechanical force. The aim of this review is to discuss the significance of these findings and the extent to which they can be utilized clinically in the correction of skeletal malocclusion. An understanding of the cellular and molecular mechanisms that enable bones and other connective tissues of the dentofacial skeleton to adapt to changes in their mechanical environment is fundamental to the practice of orthodontics and dentofacial orthopedics, based on sound biological and bioengineering principles.
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FACIAL SUTURES |
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Morphology of Facial Sutures
Suture morphology is determined by the site and mechanical stresses to which they are exposed. In general, midline sutures are described as butt-end, while others are of the overlapping beveled type (Kokich, 1976). During the growth period, sutures have a predominantly linear configuration, but with age, more complex beveled and interdigitating sutures develop through functional modification. Where strong bonds are required, interdigitating sutures develop to enhance surface contact and resist separation. All sutures eventually undergo various degrees of fusion by osseous union or synostosis. Sutural synostosis begins at different ages in the various sutures of the skull and proceeds at the endocranial slightly earlier than at the ectocranial surface (Todd and Lyon, 1924, 1925). In contrast to cranial sutures, facial sutures can remain patent quite late into adult life (Table 1
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The evidence from animal models suggests specific roles for growth factors as well as the BMP (bone morphogenetic protein), Shh (sonic hedgehog), and FGF signaling pathways. Nevertheless, where each of these factors and their target genes fits into a complex morphogenetic cascade remains poorly understood. Insulin-like growth factors (IGFs; Bradley et al., 1999), transforming growth factor-ß (TGF-ß) isoforms (Opperman et al., 1997, 1998; Roth et al., 1997)), and FGF-2, FGFR-1, and FGFR-2 (Mehrara et al., 1998) have all been localized in the cells and matrix of the dura mater, osteoblasts, and sutures in rats. Their expression is increased during synostosis, suggesting a paracrine signaling role for these factors; since facial sutures differ from cranial sutures in the absence of dura, this may partly explain why facial sutures remain patent longer.
The other reason is related to the intermittent mechanical loading of the circum-maxillary suture system that occurs during mastication (Behrents et al., 1978; Wagemans et al., 1988; Jaslow, 1990; Herring and Mucci, 1991). Animal models indicate that the various craniofacial sutures are under distinct and dissimilar strain regimes (Rafferty and Herring, 1999). Experiments conducted on the miniature pig have showed that, for the sutures of the calvaria (interparietal, interfrontal, coronal), peak strains are mainly tensile, and for those of the snout (internasal and nasofrontal), mainly compressive (Fig. 1). Nevertheless, sutural strain is a very dynamic parameter, and many sutures show temporal and regional variations in strain polarity; some sutures even show a small compressive strain before or after the tensile peak (Herring and Mucci, 1991). Variations in the strains to which facial sutures are exposed (tensile, compressive, shear) by masticatory muscle function will be reflected in their morphology.
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REMODELING THE MAXILLA IN NON-HUMAN PRIMATES |
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TOPABSTRACTINTRODUCTIONFACIAL SUTURESREMODELING THE MAXILLA IN...CLINICAL REMODELING OF THE...EXPERIMENTAL REMODELING OF THE...IS CONDYLAR CARTILAGE UNIQUE?CLINICAL REMODELING OF THE...REFERENCES |
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In experiments with both adolescent and adult monkeys, forces have been applied to the dentomaxillary skeleton by a wide variety of mechanical devices. Most of the early studies involved the use of HG to apply a posterior force, and a combination of metallic implants, radiography, in vivo bone markers, and histology to analyze the outcome (Sproule, 1968; Fredrick, 1969; Cutler et al., 1972; Droschl, 1973; Elder and Tuenge, 1974; Meldrum, 1975; Triftshauser and Walters, 1976). All showed that, by using mechanical forces to create controlled remodeling of facial sutures (Fig. 2), it is possible to alter the positional relationships of the bones of the facial skeleton. In growing animals, however, this effect is transitory; after the termination of HG treatment, the maxilla resumes its normal forward growth pattern (Tuenge and Elder, 1974). In some cases, the remodeling response may even extend to the lower jaw. An unexpected finding in a study of cervical traction in adult monkeys was the presence of resorption craters on the articular surface of the condylar head, suggesting distal displacement of the mandible by occlusal forces (Brandt et al., 1979).
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CLINICAL REMODELING OF THE MAXILLA |
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TOPABSTRACTINTRODUCTIONFACIAL SUTURESREMODELING THE MAXILLA IN...CLINICAL REMODELING OF THE...EXPERIMENTAL REMODELING OF THE...IS CONDYLAR CARTILAGE UNIQUE?CLINICAL REMODELING OF THE...REFERENCES |
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Remodeling the Maxilla with Headgear
Several investigations have shown that HG treatment can alter the positional relationship of the maxilla to the cranial base (Moore, 1959; Ricketts, 1960; Poulton, 1967; Watson, 1972; Weislander, 1974, 1975), but others have been unable to detect significant orthopedic change, the main effect being tooth movement (Badell, 1976; Bernstein et al., 1977; Baumrind et al., 1979). The reasons for this have been discussed previously (Meikle, 1980), but the evidence suggests that optimal conditions for achieving orthopedic change in the maxilla are fulfilled when (1) the force is of sufficient magnitude (1000 gm per side) to be transmitted beyond the periodontal joints, and (2) as many teeth as possible have been incorporated into the appliance. The direction in which the force is applied (cervical vs. occipital) will also influence the outcome, depending upon whether the sutures are exposed to a predominantly tensile or compressive mechanical strain.
Prospective Studies of Headgear Treatment
The only published prospective randomized clinical trial (RCT) of HG treatment, prior to the three RCTs of Class II treatment funded by the National Institute of Dental Research in 1988, was by Jakobsson (1967), a man clearly ahead of his time. In Jakobsson’s study, 60 children aged 8–9 yrs with a Class II division 1 malocclusion were randomly assigned to either an Andresen activator, HG, or control group. Both HG and activator treatments were found to have had a distalizing effect on the maxilla.
In the RCT undertaken at the University of North Carolina (Tulloch et al., 1997a,b, 1998), 166 persons having mixed dentitions with an overjet greater than 7 mm were randomly assigned to early treatment with either a headgear or bionator, or to control. There was considerable variation in the pattern of change in all three groups, with the HG group showing restricted forward movement of the maxilla averaging about 1 mm. The University of Florida RCT involved 249 participants aged 9–10 years who were randomly assigned to control, bionator, or HG/biteplate treatments (Keeling et al., 1998). Neither the HG/biteplate nor the bionator had a significant effect on maxillary growth, although both appliances were reported to enhance the growth of the mandible. In a study of 63 participants conducted at the University of Pennsylvania, early treatment outcome with either a HG or Fränkel functional regulator were compared (Ghafari et al., 1998). Both treatments were found to be effective at reducing overjets, but the study did not include a control group.
Rapid Maxillary Expansion
The most dramatic example of sutural remodeling is the result of rapid maxillary expansion (RME), when a diastema is opened between the central incisor teeth. Angell (1860), who introduced the technique using a screw mechanism, claimed that the apparatus produced a separation of the two halves of the maxilla. In commenting on the article, the Editor of the Dental Cosmos, while being unwilling to assert that such a thing was not utterly impossible, found this exceedingly doubtful (the italics are the Editor’s). For the next 100 years, RME had a somewhat checkered history, until Haas (1961, 1965) popularized the fixed palatal expander in the 1960s, and showed that RME in adolescents had a predictable outcome. For RME to be effective as an orthopedic appliance, the magnitude of the applied force must be of sufficient magnitude to be transmitted beyond the periodontal joints; otherwise, the stresses will be absorbed within the alveolar bone, resulting in tooth movement alone. Although not usually recognized by orthodontists as such, rapid maxillary expansion is an example of distraction osteogenesis.
It is a common belief that the mid-palatal suture fuses at around the age of 15 yrs. However, there is some anatomical and clinical evidence that this is not necessarily true. In a histological study of 60 human autopsy specimens aged 0–18 yrs, Melsen (1975) found that growth of the mid-palatal suture continued up to the ages of 16 in girls and 18 in boys. Furthermore, Persson and Thilander (1977) reported, in an older age group (15–35 yrs), that although palatal sutures may show evidence of obliteration during the juvenile period, a marked degree of closure was rarely found until the third decade, i.e., 20–30 yrs of age.
The key issue is not whether osseous union has begun, but the overall percentage of the suture that has actually fused. Persson and Thilander speculated that if osseous bridging of 5% represented the upper limit for splitting the mid-palatal suture, this would not be reached in most people before the age of 25 years. In a combined radiographic-histological investigation, Wehrbein and Yildizhan (2001) concluded that if this were true, RME would have been successful in nine of the 10 individuals (aged 18–38 yrs) in their study sample. They also showed that a radiologically invisible suture does not necessarily mean that the suture is fused histologically. In any event, undue focus on the palate rather obscures the fact that the greatest resistance to RME comes not from the mid-palatal suture, but from the circum-maxillary suture network (Isaacson and Ingram, 1964; Wertz, 1970) that attaches the maxilla to the rest of the skull (Fig. 3).
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Maxillary Protraction
Maxillary protraction in the treatment of Class III malocclusion has increased in popularity in recent years, due to the work of Delaire with the orthopedic face mask (Delaire, 1971; Delaire et al., 1972), and the animal experimentation discussed earlier showing that the maxilla can be distracted (Dellinger, 1973; Kambara, 1977; Nanda, 1978; Jackson et al., 1979). Nevertheless, the degree to which maxillary skeletal change can be achieved clinically is age- and technique-dependent.
Several studies have reported the skeletal and dental effects of maxillary protraction in the correction of skeletal Class III malocclusion, both with RME (Ngan et al., 1996, 1998; Kapust et al., 1998; Franchi et al., 2004) and without RME (Wisth et al., 1987; Takada et al., 1993). Together with the findings of a meta-analysis (Jäger et al., 2001), these studies showed that maxillary protraction is more effective if (1) undertaken in the late deciduous or early mixed dentition, and (2) combined with RME. Given that the aim of RME is to loosen the articulations of the maxillary complex from the rest of the skull, this is not surprising. The next logical step in the evolution of maxillary distraction techniques is to combine RME with the use of osseous mini-screws to provide forward distraction directly to the bones. Not only will this avoid unwanted tooth movement, but it will also enable the method to be effective in a much older age group than at present.
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EXPERIMENTAL REMODELING OF THE TMJ |
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As might be deduced from its structure and function, the TMJ is morphologically adapted to resist the effects of mechanical loading, and therefore is more difficult to remodel than fibrous joints. This is due to the physical properties of the cartilaginous matrix, the function of which is to protect the subchondral bone from resorptive remodeling.
Functional Mandibular Protrusion in Rats
Experiments conducted by Petrovic and his co-workers at the University of Strasbourg have suggested that anterior displacement of the mandible in growing rats can bring about additional growth of condylar cartilage (Fig. 4), and hence the growth of the mandible, by stimulating the cells of the proliferative zone (PZ) to undergo mitosis (Charlier et al., 1969; Petrovic et al., 1975; Petrovic and Stutzmann, 1977). Attempts to reproduce these results, however, using biochemical, histomorphometric, and autoradiographic methods, have been unsuccessful (Tonge et al., 1982; Degroote, 1984; Ghafari and Degroote, 1986; Tewson et al., 1988).
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) in histological sections ’blind’, which makes any attempt at quantitation potentially unsafe. It has also been suggested that the discrepancies reported in the literature could be due to differences in appliance construction and such factors as the degree of opening, continuous vs. intermittent displacement, and the extent to which a definite forward shift of the mandible might be achieved (Degroote, 1984; Ghafari and Degroote, 1986; Tsolakis and Spyropoulos, 1997; Tsolakis et al., 1997). To address this problem, Tsolakis et al.(1997) designed a new device to produce a controlled, stable, and reproducible anterior advancement of the mandible in rats by rubber elastics rather than by functional displacement. Following the application of a force of 25 gm for 12 hrs/day for 30 days, they found that growth of the lower jaw was affected to some extent. Although linear measurements indicated that mandibles in the experimental group were longer than in the controls, they were unable to conclude if this was due to an increase in the growth of condylar cartilage.
Alterations in Gene Expression following Protrusive Function in Rats
Whether functional appliance therapy can accelerate or enhance the growth of the condyle is a question that has been revived recently by Rabie and colleagues, at the University of Hong Kong, who have applied molecular methods to the problem (Rabie and Hägg, 2002; Rabie et al., 2003, 2004; Tang et al., 2004). They have showed, in a rat model, that the transcription factor Sox-9 and its target gene type II collagen are up-regulated in the glenoid fossa following forward mandibular positioning. Over an experimental period of 17 days, this reached a maximum on day 3 but declined thereafter (Rabie et al., 2003). Mandibular advancement also triggered an increase in the expression of the cell-cell signaling molecule Indian hedgehog (Ihh) in the cells of the PZ and adjacent chondroblasts (Tang et al., 2004). This coincided with an increase in cell proliferation within the PZ. Both these increases proved to be transient, however, reaching a peak after 7 days and returning to control levels by day 14.
Rabie et al. have interpreted these findings as proof that functional appliances enhance condylar growth by stimulating the differentiation of PZ cells into chondroblasts. Elegant though these experiments may be, the temporary nature of the reported changes does present a problem. The responses of cells and tissues to mechanically induced strain are well-established (for reviews, see Sandy et al., 1993; Meikle, 2006), so it is not surprising to find that mechanically deformed cells in the craniomandibular joint of the rat respond in a similar manner, in terms of both changes in metabolic activity and proliferation.
If one bears in mind the stimulatory effect of mechanical stress on cell proliferation and DNA synthesis in other model systems (Roberts and Jee, 1974; Meikle et al., 1979), the transient burst in mitotic activity reported by Rabie et al. is likely to result from the release of G2-blocked cells, allowing them to undergo mitosis, as well as enabling G1-blocked cells to enter the S phase. Ihh has also been shown to be an essential component of mechanical force transduction in chondrocyte proliferation (Wu et al., 2001), and to up-regulate the expression of cyclin D1, a kinase required for the transition of cells from G1 to the S phase of the cell cycle (Long et al., 2001).
TMJ Remodeling in Non-human Primates
While the evidence from rat experimentation has been controversial and subject to various interpretations, anterior displacement of the mandible in the rhesus (Macaca mulatta) monkey has been shown consistently to produce significant morphological changes in the TMJ (Breitner, 1940, 1941; Baume and Derichsweiler, 1961; Meikle, 1970; Stockli and Willert, 1971; Adams et al., 1972).
Prior to Carl Breitner, investigations into the effects of orthodontic treatment at the histological level in animal models had been confined to changes in the PDL and alveolar bone. Breitner was the first to look beyond the teeth and study the tissue changes induced in the TMJ and other sites in the mandible. His findings were first published in the German literature during the 1930s and later in English in two classic papers entitled "Bone changes resulting from experimental orthodontic treatment" and "Further investigations of bone changes..." (Breitner, 1940, 1941). These provided convincing histological evidence that the influence of orthodontic treatment in experimental animals was not limited to the teeth, but extended to other parts of the mandible, causing remodeling of the glenoid fossa and condyle. Breitner’s papers have been criticized for containing only one animal in each experimental group, and little, if any, evidence of control material. Nevertheless, despite the introduction of vital staining, improved histological techniques, metallic bone implants, and cephalometric radiography, subsequent investigations have added comparatively little new information to Breitner’s original findings (Baume and Derichsweiler, 1961; Meikle, 1970; Stockli and Willert, 1971; Elgoyhen et al., 1972; McNamara and Carlson, 1979; Woodside et al., 1987). A summary of the adaptive changes in the TMJ of the rhesus monkey following anterior mandibular displacement based on the above studies is shown in Fig. 5.
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As in humans (Björk, 1963; Björk and Skieller, 1972), the condyle of monkeys undergoes an age-dependent change in growth direction (McNamara and Graber, 1975; Luder, 1987). One interpretation of the above findings is that anterior displacement of the mandible remodeled the condylar head in a more posterior direction, thereby neutralizing the forward growth rotation observed in the control animals. This would account for the increased length of the mandible in the experimental group, and provides a valuable indicator as to what might be happening clinically in growing children treated with ’bite jumping’ appliances.
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IS CONDYLAR CARTILAGE UNIQUE? |
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TOPABSTRACTINTRODUCTIONFACIAL SUTURESREMODELING THE MAXILLA IN...CLINICAL REMODELING OF THE...EXPERIMENTAL REMODELING OF THE...IS CONDYLAR CARTILAGE UNIQUE?CLINICAL REMODELING OF THE...REFERENCES |
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Remodeling Articular Cartilage
It has been known, at least since Alexander Ogston (Ogston, 1875, 1878), that articular cartilage has the ability to adapt to alterations in the mechanical equilibrium of the skeleton, even in the adult. Ogston believed that articular cartilage was continually renewing itself from a central focus of growth. He observed that growth occurred outward to compensate for wear and tear at the surface, as well as inward, where it added to the subchondral bone by endochondral osteogenesis.
This was confirmed experimentally 90 years later by the autoradiographic studies of Mankin (1962), in which the injection of 3H-thymidine into the knee joint of rabbits demonstrated the presence of a central zone of proliferative cells in the femoral articular cartilage. Also, in a study of articular remodeling in human synovial joints, Johnson (1959) calculated that progressive remodeling added 3 mm of new bone to the femoral head between the ages of 30 and 60 yrs. The remodeling of articular cartilage is a process of biological adaptation to changing environmental circumstances; there is a large body of literature on the subject. (For a review of TMJ remodeling, see Meikle, 1992, 2002.)
Condylar Cartilage is Derived from the Periosteum
Central to an understanding of condylar growth is the question of why cartilage is present in a membrane bone in the first place. Of the many examples of connective tissues adapting to changing mechanical circumstances, the one most relevant to the condyle is from the work of Murray (1963), who described the development of adventitious (secondary) cartilage in several articulations in the skull of the embryonic chick. He found that secondary cartilage always developed in membrane bones, but only at articulations that were mobile, or where the musculature set up conditions of strain. In subsequent experiments with grafted and paralyzed embryos (Murray and Smiles, 1965), cartilage did not form, and cells that normally formed cartilage produced bone instead.
Studies in which mandibular condyles have been transplanted into a non-functional environment have also showed that the progenitor cells of the PZ differentiate into osteoblasts, and not chondroblasts as in situ (Duterloo, 1967; Meikle, 1973a,b). The cells are therefore multipotential and can form either cartilage or bone, depending upon the environmental circumstances. Simple microscopic observation makes it obvious that the articular and proliferative zones of the condyle are no more than a continuation of the fibrous and cellular layers of the periosteum. The change from osteogenesis to chondrogenesis has resulted from the evolutionary development of an articular condylar process in the mandible (dentary) of mammals and, as a consequence, the altered functional demands of the periosteum covering the articular joint surfaces (Meikle, 1973a,b).
Only by recognizing that condylar cartilage is a product of the periosteum can the differences in cellular kinetics, structure, and growth that exist between condylar and epiphyseal cartilage be understood. These include failure of the chondrocytes to divide (growth is appositional as in bone), and, as a result, the cells are not organized into parallel columns. It is also worth being aware that functional activity also plays a role in the growth of epiphyseal cartilage. In the absence of function, the growth plates of rat metacarpals fail to maintain a satisfactory increase in transverse diameter, and the cells of the perichondrium at the perimeter differentiate into osteoblasts, not chondrocytes (Meikle, 1975).
Genetic Control Mechanisms
Both condylar and epiphyseal cartilages share some of the genetic control mechanisms regulating chondrogenesis. These include expression of the transcription factor Sox-9, essential for chondrocyte differentiation from mesenchymal stem cells, and the negative feedback loop involving PTH-rP (parathyroid hormone-related protein) and Ihh that controls the rate of differentiation of chondrocytes in the growth plate (Lanske et al., 1996; Vortkamp et al., 1996); PTH-rP is produced mainly in the perichondrium, while the PTH/PTH-rP receptor is expressed by pre-hypertrophic chondrocytes.
Also common is the degradation of the mineralized matrix that occurs during endochondral ossification by a combination of osteoclastic action and MMP (matrix metalloproteinases) expression. All three major classes of MMPs and their inhibitor TIMPs (tissue inhibitors of metalloproteinases) have been identified in the chondrocytes and matrix of long bones (Brown et al., 1989) and condylar cartilage (Breckon et al., 1994). However, condylar cartilage is not affected by gain-of-function mutations in the FGFR-3 gene (a negative regulator of chondrocyte differentiation in bones of the primary cartilaginous skeleton) that cause achondroplasia (Rousseau et al., 1994; Shiang et al., 1994), as well as other skeletal dysplasias, such as hypochondroplasia and thanatophoric dysplasia in humans.
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CLINICAL REMODELING OF THE TMJ |
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The first cephalometric investigation of treatment outcome (Brodie et al., 1938) effectively destroyed the myth that orthodontic appliances could stimulate the growth of bone. This was followed by the first longitudinal cephalometric investigation of the early growth of the head (Brodie, 1941), which suggested that the growth pattern of the individual was established at an early age, and that, once attained, it did not change. At the time, these publications had a profound impact on orthodontic thought, giving rise to the linked concepts of (1) the immutability of the facial or morphogenetic pattern of the individual, and (2) the inability of the clinician to alter it in any way. As a result, the old dogma was replaced by a new one. Orthodontic treatment was limited to tooth movement alone. Some clinicians still believe this.
Age-related Changes in the Human Condyle
Before we discuss the clinical evidence, it is worth considering the age-related changes in the morphology of the human TMJ and condyle that have been reported during the time that growth modification is normally undertaken (Fig. 6). It also helps put the findings of rat and primate experimentation into perspective. The material is of necessity limited and is likely to remain so.
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During the mixed-dentition stage (6–12 yrs), while the condyle gradually increased all its dimensions, the cartilage remained uniformly thin (at 0.3–0.5 mm) and became limited to the anterosuperior aspect of the condylar head, opposite the posterior slope of the articular eminence. This is consistent with the role of the cartilage in the protection of the subchondral bone. At 16–17 yrs, the cartilage becomes thinner, and a closing plate of bone coalesces below it. Human condylar cartilage is a rather less impressive structure than it is in the adolescent monkey or the 6-week-old rat. It is also worth bearing in mind that condylar cartilage is not the only site in the condyle where osteogenesis is taking place during growth.
The Evidence of Retrospective Investigations
Europe has a tradition of dentofacial orthopedics, and most of the various appliance systems currently used in the treatment method referred to as ’functional jaw orthopedics’ originated in Europe. The skeletal and dental effects of several functional appliances based on the Norwegian system (Andresen and Häupl, 1942; Korkhaus, 1960; Fränkel, 1966; Marschner and Harris, 1966; Demisch, 1972; McNamara et al., 1985), as well as more active devices such as the Herbst and twin-block (Pancherz, 1979; Weislander, 1984; Hägg and Pancherz, 1988; DeVincenzo, 1991; Mills and McCulloch, 1998; Baccetti et al, 2000), have been reported in numerous investigations. Nearly all have reported successful treatment, but whether the appliance in question altered facial growth, particularly mandibular growth, sufficiently to attain clinical significance remains controversial.
The scientific value of the retrospective study has been criticized for several valid reasons, including selection bias, inadequate sample size, lack of contemporaneous controls, and poor research design; it also encourages post hoc deductions. In the new era of evidence-based medicine, the prospective RCT is seen by many to be the ’gold standard’ for analyzing treatment outcome, and the only valid source of clinical data.
The Evidence of Prospective Randomized Clinical Trials
The effects of functional appliances of various designs on mandibular growth in each of the relevant RCTs published to date are summarized in Table 2. These suggest that (1) small but statistically significant differences in mandibular length were produced in the majority of these studies, and (2) functional appliances such as the Herbst and twin-block, based on the principle of ’jumping the bite’, are more effective at modifying mandibular growth than are passive appliances such as the Andresen activator and its variants.
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• The inaccuracy of the cephalometric method
The measurement error may be greater than the growth changes one is hoping to identify. Condylion, a key landmark, is notoriously difficult to identify accurately on conventional cephalometric radiographs. Until imaging techniques improve, and cone beam computed tomography is showing promise (Hilgers et al., 2005), the TMJ will continue to be something of a ’black box’.
• Validity of the measurements
The cephalometric measurements themselves used to quantitate change are of questionable validity. Linear dimensions such as condylion-pogonion (Co-Pog), or its surrogate, articulare-gnathion (Ar-Gn), to quantify changes in mandibular growth are not valid measurements. They do not take into account condylar growth rotation (Björk, 1963) and underestimate condylar growth on average by 3–4 mm (Hägg and Attström, 1992). The Pancherz analysis (Pancherz, 1982) used in some RCTs (Table 2) will similarly underestimate mandibular growth, since it is a linear measurement that does not take into account variations in condylar growth rotation (Meikle, 2005). To be valid, measurements should be made between pre- and post-treatment condylions; not only will this give a more accurate estimate of the amount of condylar growth, but it will also provide information regarding condylar growth direction.
• The pubertal growth spurt
Variabilities in the timing, magnitude, and duration of the pubertal growth spurt are difficult to predict accurately. There are also differences in the timing of peak height velocity (PHV) and pubertal spurts in facial growth. Velocity curves for a French-Canadian population (Buschang et al., 1999) showed that, for males, the average annual growth velocity for the condyle ranges from 2.1–3.1 mm, with a peak at 14.3 yrs (Fig. 7). There was, however, substantial variation. For a male individual in the 90th percentile, for example, condylar growth will average 5 mm/year, while for another in the 25th percentile, the annual increment will be as little as 1–2 mm. This will have a significant effect on treatment outcome.
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suggest that many of the participants were some distance from achieving PHV. In only one, the UNC investigation discussed earlier (Tulloch et al., 1997a), was treatment timed to start within 1 yr of PHV, which might explain the differences in their results compared with those of Keeling et al.(1998), despite both groups using the bionator. It seems likely that, given the above, all the RCTs published to date significantly underestimate mandibular change.
Can the TMJ be Remodeled Clinically?
It is clear that functional displacement of the mandible in primate models alters the surface contours of the condyle, glenoid fossa, and post-glenoid tubercle. In that respect, it is no different from any other joint. There is also evidence to suggest that condylar growth can be directed in a more posterior direction. Remodeling the TMJ in monkeys is one thing. Remodeling it clinically is quite another. Nevertheless, there is evidence, from those treated with the Herbst appliance, suggesting that it might be possible.
In a systematic review of the literature regarding the effects of Herbst treatment on TMJ morphology, Popowich et al.(2003) identified 80 studies related to the topic. Publications that used transpharyngeal radiographs to document morphological change were excluded, leaving five publications meeting their criteria. In one of these (Ruf and Pancherz, 1998), magnetic resonance imaging (MRI) was used to analyze TMJ growth adaptation in 15 consecutive Class II patients treated for a period of 7 months. After 6–12 wks, signs of condylar remodeling were seen at the postero-superior border in 29 of the 30 condyles, while glenoid fossa remodeling was noted in 22 joints.
Of interest is the major study (Paulsen, 1997) of 100 consecutive patients treated with the Herbst appliance. This was not included in the Popowich et al. review, since orthopantomographic and transpharyngeal radiography were used to obtain the condylar images. Paulsen reported that, in most cases, a visible change in the morphology of the condyle occurred—a double contour of the postero-superior part of the condyle, and sometimes at the distal surface of the ramus. In children/youth at the peak of puberty, the double contour was distinct only for a short time, while in late puberty it persisted for several months. Paulsen concluded that the observed changes were due to bone remodeling.
These findings suggest that condylar growth occurred in a more posterior direction, which is consistent with the evidence from functional mandibular displacement in monkeys. They further suggest that remodeling of the TMJ with the Herbst appliance (and probably the twin-block) can be regarded as a definite clinical possibility, particularly in an actively growing child.
Growth Stimulation vs. Growth Remodeling
Mechanical stimuli arising from the functional activity of the TMJ are essential for the differentiation and maintenance of condylar cartilage. Put simply, no function, no cartilage. However, is one then justified in concluding that so-called functional appliances increase chondrogenesis and bone formation, or do the transient changes in cell proliferation and metabolism reported by some groups simply represent localized adjustments to alterated mechanical strain?
Given the ambiguity of the experimental and anatomical evidence, the hypothesis that functional mandibular displacement stimulates the mitosis of PZ cells, and hence the growth of the condyle in humans, should remain firmly in the category labeled ’unproven’. It would seem to be a weak basis on which to make statements such as, ’...this indicates that functional appliance therapy can truly enhance condylar growth’ (Rabie et al., 2003). It would be nice to think so, but clinical experience suggests otherwise. The point may be regarded as largely one of semantics, but from the clinical point of view, the term growth remodeling seems preferable to growth stimulation for describing the morphological changes in the TMJ that result from the use of dentofacial orthopedic appliances.
Received January 30, 2006; Accepted April 19, 2006
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TOPABSTRACTINTRODUCTIONFACIAL SUTURESREMODELING THE MAXILLA IN...CLINICAL REMODELING OF THE...EXPERIMENTAL REMODELING OF THE...IS CONDYLAR CARTILAGE UNIQUE?CLINICAL REMODELING OF THE...REFERENCES |
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= 500 microstrains. (Redrawn from 
