Osteopathic Medicine
Craniofacial growth: evolving paradigms Gennaro Castaldo1,2, Francesco Cerritelli1,2 1
EBOM - European Institute for Evidence Based Osteopathic Medicine, Pescara, Italy, 2AIOT – Accademia Italiana Osteopatia Tradizionale, Pescara, Italy Aims: Numerous theories about craniofacial growth have been formulated in the last century. The most influential hypotheses were: genetic, synthetic and functional matrix revisited. Moreover, a large number of experts from different fields tried to explain craniofacial growth and its developmental mechanisms, in order to deliver the best treatment possible to orthodontic patients. The aim of this review is to summarize recent concepts on craniofacial growth, overlap these theories with the development of the general scientific knowledge, and suggest a more integrated multidisciplinary person-based approach. Methodology: MEDLINE, EMBASE, Pubmed, CINAHL and Google Scholar were screened from inception to February 2014 for relevant papers. Grey literature was considered as part of the search. Conclusions: The influence of new scientific discoveries and intuitions about craniofacial growth produced further insights in orthodontics care, shifting the paradigm from a pre-determined, sectorial treatment to an individualized, multidisciplinary patient-centered approach aiming to enhance the quality of orthodontic assistance.
Keywords: Orthodontics, Craniofacial growth, Multidisciplinary approach
Introduction During the last century the theoretical underpinnings regarding craniofacial development improved significantly, leading the field of dentistry to radically change its clinical rationale. However, the practical application of these understandings remains unreliable. Hinton and Carlson1 stated that the craniofacial growth can be modified, but not in a ‘predictable, controlled and clinically effective way’. Moreover, Krogman2 considered craniofacial growth as a field studied by a plethora of disciplines: ‘Growth was conceived by an anatomist, born to a biologist, delivered by a physician, left on a chemist’s doorstep, and adopted by a physiologist. At an early age she eloped with a statistician, divorced him for a psychologist, and is now being ardently wooed, alternatively, by an endocrinologist, a pediatrician, a physical anthropologist, a physicist, a biochemist and a mathematician. A short while ago there was some talk of a eugenicist, and only last week a newcomer, looking suspiciously like an orthodontist, was seen loitering in the vicinity.’ Therefore, the aim of this review is to summarize recent concepts on craniofacial growth, overlap these theories with the development of the general scientific knowledge, and eventually suggest a more integrated multidisciplinary person-based approach.
Correspondence to: Francesco Cerritelli, Via Prati, 29 - 65124 Pescara, Italy. Email: [email protected] ß W. S. Maney & Son Ltd 2015 DOI 10.1179/0886963414Z.00000000042
This paper is divided into four parts. First the most common craniofacial theories will be discussed. Secondly, the two key anatomical elements responsible for craniofacial growth will be analyzed. Thirdly, the new theories will be drawn, and finally an integrated multidisciplinary approach will be proposed.
Theories of Craniofacial Growth Until the 1980s, the most common craniofacial growth theories could be divided into four hypotheses: Genetic, Functional, Synthetic and Servosystem. All of them were characterized by a mechanistic approach, however, considering different aspects. The genetic hypotheses were divided into three main streams: bone, suture and cartilage (or Nasal Septum). At the beginning of the 1920s the bone hypothesis defined the craniofacial growth as exclusively regulated by genes. This theory was influenced by the Darwin/Mendel scientific genetic discoveries, which considered inheritance the basis of evolution. Several authors stated that the bone modifies its shape and size by periosteal deposition and internal resorption.3–6 Sutures and cartilages had no role in the craniofacial growth (Fig. 1). As a result, each human being has a defined fate (see Lombroso and his phrenology7) and orthodontists can, at best, in Angle’s words, ‘…bring faces and
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Figure 1 Bone remodeling by surface deposition and internal reabsorption. All is under genetic control.
occlusions into a condition of harmony according to type.’8 As a matter of fact, orthodontists used the basis of cephalometric studies trying to establish standard rules for ideal orthodontic treatments. The Apollo Belvedere, a Greek statue from antiquity was considered the benchmark of human facial harmony.8,9 Criticisms of the bone hypothesis were based on the well-known action of local and environmental forces in reshaping the periosteal bones, as well as on the contributory role of sutures and cartilages.10,11 In the 1940s, the suture/genetic hypothesis was brought forward. Weinmann and Sicher12 affirmed that the connective tissue and cartilages had a leading role in craniofacial growth. Furthermore, they argued that bone growth was genetically controlled by these structures with the expanding tissue pushing the bones apart. Only the periosteum molding was controlled by local forces (Fig. 2). Contextually to this orthodontics period, while Erwin Schro¨dinger, 1940, was claiming that proteins could act as genes, Avery’s experiments brought new discoveries showing the importance of DNA and opened further frontiers on transferring hereditary traits.13 The ‘sutural hypothesis’ was mainly criticized from a clinical (e.g. the hydrocephalous condition) and embryological point of view (the absence of cartilage precursors in face bones). As a matter of fact, further histological studies stated that the sutural growth was an example of periosteal growth.14,15 The last genetic hypothesis, the ‘nasal septum hypothesis’, arose around the 1950s with J. H. Scott. The author affirmed that the nasal septum cartilage had a primary role in the prenatal period and during the first years of postnatal craniofacial growth. This
Figure 2 The genetically controlled sutural tissue pushes away the bone edges and causes growth.
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Figure 3 Cartilages have the main role in craniofacial development. Their growth, always genetically controlled, influences the craniofacial one.
cartilage is buttressed against the cranial base and pushes the mid-face forward and downward. The mandibular condyle cartilage behaves in the same way as the cranial base and the nasal septum structure, directly causing mandibular growth14 (Fig. 3). This genetic hypothesis is still part of a period of ferment concerning DNA discoveries (see Watson and Crick16) where the role of genes was a key aspect to explain craniofacial growth. In conclusion, the above theories claimed that craniofacial growth was unchangeable, almost exclusively determined by hereditary factors, and ruled by genes. As a clinical consequence orthodontists could work on dental-alveolar area only. There was no chance their intervention would interfere with genetic patterns.
Functional hypothesis In the 1960s, the first doubts that genes were the only factors influencing cranio-facial growth came from the Jacob and Monod17 studies. Their experiments on Lac-Operon showed that an environmental agent could affect genetic transcription. In the same period, the Moss Functional Hypothesis18,19 made a significant change in the orthodontics scenario, since it considered that the genetic factor was not the only key element affecting craniofacial growth. As Carlson20 stated, there was a shift from competing theories to competing paradigms, because the ‘unchangeable’ genetic theory was replaced by the ‘plastic’ functional paradigm. Moss moved the attention towards ‘function’, considering the latter as the final result of a complex bone-tissue-space interaction. The author theorized that microskeletal units (i.e. tendons on bone surfaces) work as basic elements for the periosteal functional matrix, and macroskeletal units (i.e. nasopharynx and oropharynx for respiratory function and brain for neurocranium development) are key elements of the capsular functional matrix18,19 (Figs 4–5). As a direct consequence of Moss’ studies, orthodontists started using craniofacial VOL .
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Figure 4 Periosteal functional matrix.
growth driving devices, i.e. the Frankel Function Regulator,21,22 to control structural growth. Figure 5 Capsular functional matrix.
Synthetic hypotheses Numerous theories tried to fill the gap between the genetic and functional hypotheses. The most relevant and scientifically validated was the Synthetic Hypothesis.23 It considered the condrocranium as the key factor for the development of the cranium and the face. The condrocranium is gene-related and plays a relevant role in the development of the mid-face and cranial vault. Likewise the mandible and other structures of the face are under the control of environmental factors (Fig. 6). Another synthetic hypothesis was the Servosystem Theory. Petrovic24,25 described the cranial base synchondrosis and septum cartilage, which are genetically and endocrine regulated, as crucial components for both upper maxillary development and its spatial positioning. As a result, the mandible adapts itself to the occlusal deviation, activating periodontal and temporomandibular joint proprioceptors, which in turn inform the Central Nervous System about the variation. This activates a topdown response that stimulates condylar growth through the action of mandibular muscles (Fig. 7). So far the occlusion acts as a ‘comparator’ for the craniofacial growth in this servosystem. All the theories described above drove the attention mainly to sutures, cartilages and functional matrixes. However, the lack of scientifically proven concepts led further studies to focus on two additional specific structures: the mandibular condyle and the spheno-occipital synchondrosis. Mandibular condyle Current opinions tend to consider the condylar cartilage growth as purely adaptive, or compensatory. Several studies have demonstrated that in animal models, keeping the mandible in a postural protrusion, results in the mandibular cartilage increasing its thickness, whereas a postural retrusion decreases it.1,26 An additional study showed that an anterior displacement of the articular disc can stop the horizontal mandibular growth.27 Conversely, mechanical stimuli can produce variation in the speed of mandibular growth. Both low amplitude, high frequency vibration28 and electric stimuli29 seem
to induce an active growth of the cartilage matrix and an increase in vascular flow. This creates a cascade of growth-factors-mediated effects. Shum et al.30 demonstrated a positive correlation between an increase in gene-expression of Vascular Endothelial Growth Factor and mandibular growth in mice. Similar results were obtained by Tang and Rabie31 for the expression of Run2x. Indian hedgehog expression was also found to be positively correlated with an increase in mandibular mechanical growth strain.31 Collectively all these studies reported an activation of the nucleus DNA using, mainly, mechanical transduction pathways mediated by extracellular matrix. Therefore, a mechanical stimulation produces a cellular-based condyle reaction. These mechanisms seem to be active also during the prenatal period. In the fetus, mechanical factors, such as mandibular muscle activity, have been shown to be predictive of condylar growth.32–35 In a recent study, Kjær et al.34 argued that muscle activities of the first and second pharyngeal arch are fundamental elements for normal craniofacial development. Lack of craniofacial muscle contractions may lead to hypertelorism, flat zygoma and midface, small and open mouth, microretrognathia, small tongue and abnormal palate. Another study on muscular dystrophy confirms that abnormal muscle action affects face and cranium shape.36 Therefore, not only the condyle, but also other facial bone structures show a kind of adaptive growth, linked to the action of the functional matrix. Spheno-occipital synchondrosis Theories on spheno-occipital synchondrosis (SOS) growth are different and the debate is still open. Many authors consider SOS as a growth ‘center’, exclusively influenced by genetic factors.23,30,37 Other authors believe that SOS is also modulated by mechanical stimuli. In-vitro studies demonstrated that different mechanical stresses induce a change in SOS growth. This growth seems to be mediated by different intracellular growth factors (i.e. Ihh, Parathyroidhormone-related-protein, VGEF, SOX9).38–41 These
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Figure 6 Synthetic Hypothesis. The condrocranium is placed in a central position in the craniofacial growth, as suggested by Ranly (1988).
findings were confirmed by in-vivo studies. Wang and Mao42 showed that mechanical stimuli modified the SOS cartilage growth by increasing chondrocyte proliferation. Mossey et al.43 argued that both gene action and the environmental component act at different times, having an impact on the SOS growth. Conversely, Delaire44 and Lieberman et al.45 considered the SOS growth mainly influenced by epigenetic factors. Interestingly, Lieberman et al.45 pointed out that the cranial base shape is influenced by the topdown brain growth and bottom-up face development, the so-called neural and facial space-packing.
Craniofacial Growth: Current State of the Art The study of epigenetic factors as key elements for the development of craniofacial structures introduced new frontiers as to the role of the environment on skull growth. Epigenetics clashes with the idea that DNA is the main repository of bone growth developmental formations. Corner46 stated that the genetic program is not a blueprint capable of creating an entire organism. The environment, via the extracellular 26
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matrix, modifies the shape of the cell membrane, which in turn, via the cytoskeleton, modifies the shape of the nucleus. The modified nucleus elicits modifications in protein synthesis that subsequently affect cell destiny.47 The cytoskeleton is organized according to the rules of Tensional Integrity or Tensegrity.48–50 Tensegrity key components include compression resisting elements (microtubules), and tensional elements (microfilaments, intermediate filaments), which create a seamless link among components of the extracellular matrix, cell membrane and cell nucleus. In 1997, Moss51 reviewed his Functional Matrix Hypothesis in the light of these biologic discoveries confirming, scientifically, that craniofacial development is mainly dependent on epigenetic factors. The author argued that a cascade of mechanotransduction events, based on extracellular matrix, cytoskeleton, and cell reactions between bones, periosteum and muscles could produce significant changes in craniofacial morphology. Moreover, Moss52 considered the craniofacial morphological properties in adulthood as resulting VOL .
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Figure 7 Servosystem Hypothesis.
from the action of a series of spontaneous and selforganized ontogenetic processes and mechanisms starting in the fetus. This hypothesis is based on the biodynamic metabolic fields theory,53 whose alteration is created by external/internal oriented movements. Further study54 confirmed that external mechanical stimuli could control tissue morphogenesis during embryological development. The link between mechanical stimuli and genomic expression is also underlined by Radlanski and Renz.55 These authors date back the description of the forces’ fundamental role in tissue differentiation and morphogenesis directly to His56 and Carey works.57,58 According to them, the key idea is that cells respond directly to the living environment, in particular to their neighborhood growth. This concept was additionally confirmed by Blechschmidt.53 Therefore, according to Moss,52 craniofacial development is significantly related to epigenetic stimuli which influence the destiny, function and shape of craniofacial structures from the fetal to the adulthood period.52
Future Perspectives Carlson suggested three arguments to be discussed that, if solved, could significantly improve the clinical outcome in orthodontics. The author questioned: (1)
Where the growth-related problem is located; (2) How much modification of craniofacial growth is relevant to be considered; and (3) What are the most appropriate treatment approaches that may be used to achieve the expected growth effect.20 Currently, very sophisticated cephalograms and computer programs have been developed to predict patients’ growth, create clinical-related categories, and administer ‘protocol therapies’. However, discussion is still open in order to confirm these approaches in terms of reliability, validity and ethics. Damstra et al.59 proved that cephalometric measurements are inconsistent and unreliable with respect to clinical diagnosis and treatment. These findings were confirmed by Devereux et al.60 The authors demonstrated that the probability of improving clinical decision making by adding lateral cephalometric radiographs did not make any significant difference in treatment-planning decisions. Additional studies cast doubts about orthodontic categories and classes. Thordarson et al.61 compared Icelandic children between 6 and 16 years of age with a similar Norwegian sample showing small differences in maxillary prognathism and mandibular plane angle as well as significant differences in the inclination of lower incisors.61 Ishii et al.62 demonstrated substantial imbalances in class III skeletal
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malocclusion between Japanese girls and Caucasian populations. Furthermore, according to Sadeghianrizi et al.,63 craniofacial morphology differs between obese and normal adolescents. Obesity was directly associated with bi-maxillary prognathism and greater facial diameters. Additionally, the use of selective serotonergic reuptake inhibitors or less selective tricyclic antidepressant drugs during pregnancy is associated with alteration in craniofacial morphogenesis.64,65 Therefore, although orthodontists still widely use skeletal classes classification as the gold clinical standards, recent medical and biological discoveries shed light on the potential inaccuracy of these standards. Van der Linden66 argued that facial orthopedics does not seem to have an ultimate effect on the morphology of the facial skeleton, and there is no possibility of establishing the right period of treatment; considerations also confirmed by Delaire44 in the treatment of Class III skeletal malocclusion. In order to remove the gap between patient need and treatment, there is probably the need to widen the interaction between the skull and the whole body by considering a broader holistic approach. Several authors argued the close relationship between the respiratory system and the craniofacial growth. Some research showed that breathing patterns affect the inter-molar and inter-canine distance,67 as well as the incisors position.68 Zhang69 demonstrated that children with adenoidal hypertrophy show a vertical growth pattern, larger gonion, and a retrusive chin. Pereira et al.70 suggested adenotonsillectomy on growing patients to improve dental parameters and to reduce the risk of malocclusion. Furthermore, it was documented that certain respiratory diseases, such as obstructive sleep apnea can prevent the expected difference in craniofacial growth of boys and girls,71 and induce shorter maxillary and mandibular lengths,72 lateral cross-bite, and an increased overjet.73 In addition, the decreased chewing activity during mouth breathing can negatively affect the vertical position of posterior teeth, leading to malocclusion.74 The latter can be considered a risk factor in the etiology of headaches in children and adolescents.75 Moreover, it was shown that abnormal facial muscle activity, as measured by dynamometer and surface electromyography, was related to defects in oral habits and breathing,76 as well as to malocclusion.77 Interestingly, the oral breathing seems to induce craniofacial growth patterns not only by a mechanistic alteration in the muscular balance and head and tongue position, but also by a more complex 28
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sequence of epigenetic events involving abnormal nocturnal secretion of growth hormone.78 Considering the connection between dental occlusion disorders and ocular defects, several studies documented this strong correlation.79–82 Furthermore, mandibular deviations and TMJ disorders were shown to be associated with ocular convergence problems.83,84 Interestingly, the use of rapid maxillary expansion can produce diverse side effects, including strabismus.85 However, the same procedure can significantly change the posture of the head and the position of the scapulae,86 leading to consideration of effects on a broader bodily scale. In fact, according to Springate,87 the change in posture was primarily linked to the growth direction of the face, specifically the changing position of the mandible and tongue. Korbmacher et al.88 demonstrated a significant correlation between iliac spine blockage, articulation disorders and tongue dysfunction, whereas functional asymmetry of the upper cervical spine was significantly correlated with incompetent lips.88 An additional study pointed out that children with unilateral crossbite had higher prevalence of oblique shoulder, scoliosis, oblique pelvis, and functional leg length difference.89 Similarly, subjects with class III skeletal malocclusion or transverse maxillary constriction exhibited significant deviation of the cervical column.90,91 Interestingly, Lippold et al.92 showed that the sagittal spinal posture seems to be related to craniofacial morphology, as well as being influenced by trunk rotation and pelvic tilt and rotation.93 Other researchers corroborated the association between morphologic deviations of the cervical vertebral column and craniofacial morphology,94 as well as between tongue dimension and craniofacial development.95 96 Standerwick and Roberts argued that the viscerocranium growth is influenced by the superficial musculoaponeurotic systems of the head, as a result of cephalic brain growth and cranial rotation. This hypothesis endorses the theories of Solow and Sandham,97 who argued that the extended craniocervical posture affects craniofacial growth by a passive stretching of the soft tissue layers. In addition, new embryologic and physics discoveries will suggest additional potential fields of interest. From an embryological point of view, Jheon and Schneider98 suggested that the neuralcrest-derived mesenchyme acts as the dominant source of species-specific patterning information. Its developmental programs possess plasticity, a measure of the extent to which ontogenetic systems can respond to internal and external perturbations and VOL .
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produce an integrated and sustainable phenotype. Therefore, the shape of craniofacial structures can be influenced by external stimuli at an early stage and can change craniofacial development parameters. Considering physics, scientists recently claimed that quantum mechanics could be applied to different medical fields, including mutations, phenotype changes and evolution.99 In quantum mechanics, the information is transferred using what is referred to as a phase coherence state. This condition is known as quantum phenomena in biological systems, and seems to respect the tensegrity structure model in living cells. Studies showed that interferences within this system could produce perturbations in the biological processes that in turn lead to cell fate changes.100 Interestingly, Moss52 suggested that craniofacial growth is a ‘tuned system’ that adapts itself to the environment and the cell. The author argued that the theoretical Functional Matrix Hypothesis Revisited concept considered biological systems as Complex Adaptive Systems, and within this system, minor changes in the epigenetic input can cause huge fluctuations in the morphological output. Furthermore, Moss contemplated that ontogenesis involves nonlinear processes, and is not fully predictable. For those reasons, Korbmacher et al.88 concluded with the importance of an early interdisciplinary and complementary screening to assure a physiological development of the orofacial region, whereas Silvestrini-Biavati et al.101 argued that, in orthodontics diseases, postural, orthoptic, osteopathic and occlusal variables were often clinically associated, and therefore a multidisciplinary medical approach for treatment is advised.101 Undoubtedly, there is the need to improve the diagnostic process by means of embracing other professionals (i.e. orthodontists, ophthalmologists, pneumologists, orthopedists, osteopaths), and more adequate investigation methods (i.e. Transcutaneous Electrical Nerve Stimulation or Surface Electromyography) to fulfill the individual’s needs. Therefore, as suggested by Krogman,2 the combination between different scientific fields to enhance knowledge on the optimum clinical decision making in a patient needs-based approach will be the future of orthodontics care.
Conclusions The understanding of the complex evolution of craniofacial growth, and methods to cope with its dynamics is essential for delivering the optimal orthodontics care. Dentistry is facing a change where the use of pre-determined protocols and methodologies possibly reduce the efficacy of treatment and
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diagnosis. The use of a multidisciplinary scenario where different professionals can share, in synergy and knowledge, can enhance the ability of specialists to deliver the most reliable clinical diagnosis and mold treatment according to the subject.
Acknowledgements The authors sincerely thank Dr Marta Martelli for her help in reviewing and editing the paper.
Disclaimer statements Contributors GC carried out the literature review and wrote the draft. GC and FC wrote and approved the final paper. Funding No funds were received for the present manuscript. Conflicts of interest The authors declare no conflict of interests in relation to this study. Ethics approval No ethical approval was required for this work.
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42 Wang X, Mao J. Chondrocyte proliferation of the cranial base cartilage upon in vivo mechanical stresses. J Dent Res. 2002;81(10):701–5. 43 Mossey P. The heritability of malocclusion: Part 1—Genetics, principles and terminology. J Orthod. 1999;26(2):103–13. 44 Delaire J. Le de´veloppement «adaptatif» de la base du craˆne. Justification du traitement pre´coce des dysmorphoses de classe III. Revue d’Orthope´die Dento-Faciale. 2003;37(3):243–65. 45 Lieberman DE, Hallgrı´msson B, Liu W, Parsons TE, Jamniczky HA. Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: testing a new model using mice. J Anat. 2008;212(6):720–35. 46 Corner MA. Reciprocity of structure-function relations in developing neural networks: the Odyssey of a self-organizing brain through research fads, fallacies and prospects. Prog Brain Res. 1994;102:3–31. 47 Noble D. The music of life: biology beyond genes. Oxford: Oxford University Press; 2008. 48 Ingber DE, Jamieson JD. Cells as tensegrity structures: architectural regulation of histodifferentiation by physical forces transduced over basement membrane. In: Anderson LC, Gahmberg CG, Ekblom P, editors. Gene expression during normal and malignant differentiation. New York: Academic Press; 1985. pp. 13–32. 49 Ingber DE, Folkman J. Mechanochemical switching between growth and differentiation during fibroblast growth factorstimulated angiogenesis in vitro: role of extracellular matrix. J Cell Biol. 1989;109(1):317–30. 50 Ingber DE. Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J Cell Sci. 1993;104:613– 27. 51 Moss ML. The functional matrix hypothesis revisited. 4. The epigenetic antithesis and the resolving synthesis. Am J Orthod Dentofacial Orthop. 1997;112(4):410–7. 52 Moss ML. The functional matrix hypothesis revisited. 1. The role of mechanotransduction. Am J Orthod Dentofacial Orthop. 1997;112(1):8–11. 53 Blechschmidt E. Come inizia la vita umana. Dall’uovo all’embrione. Editore: Futura Publishing Society; 2009. 54 Ingber DE. Mechanical control of tissue morphogenesis during embryological development. Int J Dev Biol. 2006;50(2/3):255. 55 Radlanski RJ, Renz H. Genes, forces, and forms: mechanical aspects of prenatal craniofacial development. Dev Dyn. 2006;235(5):1219–29. 56 His W. Unsere Ko¨rperform und das physiologische Problem ihrer Entste-hung. Leipzig: FCW Vogel; 1874. 57 Carey EJ. Studies in the dynamics of histogenesis: I. Tension of differential growth as a stimulus to myogenesis. J Gen Physiol. 1920;(2):357–72. 58 Carey EJ. Studies in the dynamics of histogenesis: II. Tension of differential growth as a stimulus to myogenesis in the esophagus. J Gen Physiol. 1920;(3):61–83. 59 Damstra J, Huddleston Slater JJ, Fourie Z, Ren Y. Reliability and the smallest detectable differences of lateral cephalometric measurements. Am J Orthod Dentofacial Orthop. 2010;138(5):546. e541–6, e548. 60 Devereux L, Moles D, Cunningham SJ, McKnight M. How important are lateral cephalometric radiographs in orthodontic treatment planning? Am J Orthod Dentofacial Orthop. 2011;139(2):e175–81. 61 Thordarson A, Johannsdottir B, Magnusson TE. Craniofacial changes in Icelandic children between 6 and 16 years of age–a longitudinal study. Eur J Orthod. 2006;28(2):152–65. 62 Ishii N, Deguchi T, Hunt NP. Craniofacial differences between Japanese and British Caucasian females with a skeletal Class III malocclusion. Eur J Orthod. 2002;24(5):493–9. 63 Sadeghianrizi A, Forsberg C-M, Marcus C, Dahllo¨f G. Craniofacial development in obese adolescents. Eur J Orthod. 2005;27(6):550–5. 64 Moiseiwitsch JR. The role of serotonin and neurotransmitters during craniofacial development. Crit Rev Oral Biol Med. 2000;11(2):230–9. 65 Byrd K, Sheskin T. Effects of post-natal serotonin levels on craniofacial complex. J Dent Res. 2001;80(8):1730–5.
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66 Van der Linden FP. Validite´ de l’orthope´die dento-faciale. Revue d’Orthope´die Dento-Faciale. 2004;38(2):141–59. 67 Retamoso LB, Knop LA, Guariza Filho O, Tanaka OM. Facial and dental alterations according to the breathing pattern. J Appl Oral Sci. 2011;19(2):175–81. 68 Cabrera Lde C, Retamoso LB, Mei RM, Tanaka O. Sagittal and vertical aspects of Class II division 1 subjects according to the respiratory pattern. Dent Press J Orthod. 2013;18(2):30–5. 69 Zhang H. Adenoidal hypertrophy and the mandibular growth pattern in children. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi. 2013;27(17):955–8. 70 Pereira SR, Bakor SF, Weckx LLM. Adenotonsillectomy in facial growing patients: spontaneous dental effects. Braz J Otorhinolaryngol. 2011;77(5):600–4. 71 Juliano ML, Machado MA, Carvalho LB, Santos GM, Zancanella E, Prado LB, et al. Obstructive sleep apnea prevents the expected difference in craniofacial growth of boys and girls. Arq Neuropsiquiatr. 2013;71(1):18–24. 72 Korayem MM, Witmans M, MacLean J, Heo G, El-Hakim H, Flores-Mir C, et al. Craniofacial morphology in pediatric patients with persistent obstructive sleep apnea with or without positive airway pressure therapy: a cross-sectional cephalometric comparison with controls. Am J Orthod Dentofacial Orthop. 2013;144(1):78–85. 73 Sauer C, Schlu¨ter B, Hinz R, Gesch D. Childhood obstructive sleep apnea syndrome: an interdisciplinary approach: a prospective epidemiological study of 4,318 five-and-a-halfyear-old children. J Orofac Orthop. 2012;73(5):342–58. 74 Hsu HY, Yamaguchi K. Decreased chewing activity during mouth breathing. J Oral Rehabil. 2012;39(8):559–67. 75 Lambourne C, Lampasso J, Buchanan WC Jr, Dunford R, McCall W. Malocclusion as a risk factor in the etiology of headaches in children and adolescents. Am J Orthod Dentofacial Orthop. 2007;132(6):754–61. 76 Saccomanno S, Antonini G, D’Alatri L, D’Angelantonio M, Fiorita A, Deli R. Causal relationship between malocclusion and oral muscles dysfunction: a model of approach. Eur J Paediatr Dent. 2012;13(4):321–3. 77 Gomes AC, Vitti M, Regalo SC, Semprini M, Sie´ssere S, Watanabe PC, et al. Evidence of muscle role over the craniofacial skull development in Angle’s Class III dental malocclusion under the clinical rest position. Electromyogr Clin Neurophysiol. 2008;48(8):335–41. 78 Peltoma¨ki T. The effect of mode of breathing on craniofacial growth – revisited. Eur J Orthod. 2007;29: 426–429. 79 Sharifi Milani R, Deville de Periere D, Micallef JP. Relationship between dental occlusion and visual focusing. J Craniomandib Pract. 1998;16:109–18. 80 Monaco A, Spadaro A, Sgolastra F, Petrucci A, D’Andrea PD, Gatto R. Prevalence of astigmatism in a paediatric population with malocclusions. Eur J Paediatr Dent. 2011;12:91–4. 81 Monaco A, Spadaro A, Sgolastra F, Petrucci A, D’Andrea PD, Gatto R. Prevalence of hyperopia and strabismus in a paediatric population with malocclusions. Eur J Paediatr Dent. 2011;12:272–4. 82 Monaco A, Sgolastra F, Petrucci A, Ciarrocchi I, D’Andrea PD, Necozione S. Prevalence of vision problems in a hospitalbased pediatric population with malocclusion. Pediatr Dent. 2013;35(3):272–4. 83 Monaco A, Streni O, Marci MC, Sabetti L, Giannoni M. Convergence defects in patients with temporomandibular disorders. J Craniomandib Pract. 2003;21:190–5.
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84 Monaco A, Streni O, Marci MC, Sabetti L, Marzo G, Giannoni M. Relationship between mandibular deviation and ocular convergence. J Clin Pediatr Dent. 2004;28:135–8. 85 Monaco A, Tepedino M, Sabetti L, Petrucci A, Sgolastra F. An adolescent treated with rapid maxillary expansion presenting with strabismus: a case report. J Med Case Rep. 2013;7(1):222. 86 Cerruto C, Di Vece L, Doldo T, Giovannetti A, Polimeni A, Goracci C. A computerized photographic method to evaluate changes in head posture and scapular position following rapid palatal expansion: a pilot study. J Clin Pediatr Dent. 2012;37(2):213–8. 87 Springate SD. A re-investigation of the relationship between head posture and craniofacial growth. Eur J Orthod. 2012;34(4):397–409. 88 Korbmacher H, Koch LE, Kahl-Nieke B. Orofacial myofunctional disorders in children with asymmetry of the posture and locomotion apparatus. Int J Orofacial Myology. 2005;31:26–38. 89 Korbmacher H, Koch L, Eggers-Stroeder G, Kahl-Nieke B. Associations between orthopaedic disturbances and unilateral crossbite in children with asymmetry of the upper cervical spine. Eur J Orthod. 2007;29(1):100–4. 90 Meibodi SE, Parhiz H, Motamedi MH, Fetrati A, Meibodi EM, Meshkat A. Cervical vertebrae anomalies in patients with class III skeletal malocclusion. J Craniovertebr Junction Spine. 2011;2(2):73–6. 91 Di Vece L, Faleri G, Picciotti M, Guido L, Giorgetti R. Does a transverse maxillary deficit affect the cervical vertebrae? A pilot study. Am J Orthod Dentofacial Orthop. 2010;137(4):515–9. 92 Lippold C, Danesh G, Hoppe G, Drerup B, Hackenberg L: Sagittal spinal posture in relation to craniofacial morphology. Angle Orthod. 2006;76(4):625–31. 93 Lippold C, Danesh G, Hoppe G, Drerup B, Hackenberg L. Trunk inclination, pelvic tilt and pelvic rotation in relation to the craniofacial morphology in adults. Angle Orthod. 2007;77(1):29–35. 94 D’Attilio M, Caputi S, Epifania E, Festa F, Tecco S. Evaluation of cervical posture of children in skeletal class I, II, and III. J Craniomandib Pract. 2005;23(3):219. 95 Liu Z-J, Shcherbatyy V, Gu G, Perkins JA. Effects of tongue volume reduction on craniofacial growth: a longitudinal study on orofacial skeletons and dental arches. Arch Oral Biol. 2008;53(10):991–1001. 96 Standerwick RG, Roberts WE. The aponeurotic tension model of craniofacial growth in man. Open Dent J. 2009;3:100. 97 Solow B, Sandham A. Cranio–cervical posture: a factor in the development and function of the dentofacial structures. Eur J Orthod. 2002;24(5):447–56. 98 Jheon A, Schneider R. The cells that fill the bill: neural crest and the evolution of craniofacial development. J Dent Res. 2009;88(1):12–21. 99 McFadden J. Quantum evolution. New York: WW Norton & Company; 2002. 100 Lipton B. La biologia delle credenze. Macro Edizioni 2006. 101 Silvestrini-Biavati A, Migliorati M, Demarziani E, Tecco S, Silvestrini-Biavati P, Polimeni A, et al. Clinical association between teeth malocclusions, wrong investigation on primary school children. BMC Pediatr. 2013;13:12.
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Craniofacial growth: evolving paradigms Gennaro Castaldo1,2, Francesco Cerritelli1,2 1
EBOM - European Institute for Evidence Based Osteopathic Medicine, Pescara, Italy, 2AIOT – Accademia Italiana Osteopatia Tradizionale, Pescara, Italy Aims: Numerous theories about craniofacial growth have been formulated in the last century. The most influential hypotheses were: genetic, synthetic and functional matrix revisited. Moreover, a large number of experts from different fields tried to explain craniofacial growth and its developmental mechanisms, in order to deliver the best treatment possible to orthodontic patients. The aim of this review is to summarize recent concepts on craniofacial growth, overlap these theories with the development of the general scientific knowledge, and suggest a more integrated multidisciplinary person-based approach. Methodology: MEDLINE, EMBASE, Pubmed, CINAHL and Google Scholar were screened from inception to February 2014 for relevant papers. Grey literature was considered as part of the search. Conclusions: The influence of new scientific discoveries and intuitions about craniofacial growth produced further insights in orthodontics care, shifting the paradigm from a pre-determined, sectorial treatment to an individualized, multidisciplinary patient-centered approach aiming to enhance the quality of orthodontic assistance.
Keywords: Orthodontics, Craniofacial growth, Multidisciplinary approach
Introduction During the last century the theoretical underpinnings regarding craniofacial development improved significantly, leading the field of dentistry to radically change its clinical rationale. However, the practical application of these understandings remains unreliable. Hinton and Carlson1 stated that the craniofacial growth can be modified, but not in a ‘predictable, controlled and clinically effective way’. Moreover, Krogman2 considered craniofacial growth as a field studied by a plethora of disciplines: ‘Growth was conceived by an anatomist, born to a biologist, delivered by a physician, left on a chemist’s doorstep, and adopted by a physiologist. At an early age she eloped with a statistician, divorced him for a psychologist, and is now being ardently wooed, alternatively, by an endocrinologist, a pediatrician, a physical anthropologist, a physicist, a biochemist and a mathematician. A short while ago there was some talk of a eugenicist, and only last week a newcomer, looking suspiciously like an orthodontist, was seen loitering in the vicinity.’ Therefore, the aim of this review is to summarize recent concepts on craniofacial growth, overlap these theories with the development of the general scientific knowledge, and eventually suggest a more integrated multidisciplinary person-based approach.
Correspondence to: Francesco Cerritelli, Via Prati, 29 - 65124 Pescara, Italy. Email: [email protected] ß W. S. Maney & Son Ltd 2015 DOI 10.1179/0886963414Z.00000000042
This paper is divided into four parts. First the most common craniofacial theories will be discussed. Secondly, the two key anatomical elements responsible for craniofacial growth will be analyzed. Thirdly, the new theories will be drawn, and finally an integrated multidisciplinary approach will be proposed.
Theories of Craniofacial Growth Until the 1980s, the most common craniofacial growth theories could be divided into four hypotheses: Genetic, Functional, Synthetic and Servosystem. All of them were characterized by a mechanistic approach, however, considering different aspects. The genetic hypotheses were divided into three main streams: bone, suture and cartilage (or Nasal Septum). At the beginning of the 1920s the bone hypothesis defined the craniofacial growth as exclusively regulated by genes. This theory was influenced by the Darwin/Mendel scientific genetic discoveries, which considered inheritance the basis of evolution. Several authors stated that the bone modifies its shape and size by periosteal deposition and internal resorption.3–6 Sutures and cartilages had no role in the craniofacial growth (Fig. 1). As a result, each human being has a defined fate (see Lombroso and his phrenology7) and orthodontists can, at best, in Angle’s words, ‘…bring faces and
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Figure 1 Bone remodeling by surface deposition and internal reabsorption. All is under genetic control.
occlusions into a condition of harmony according to type.’8 As a matter of fact, orthodontists used the basis of cephalometric studies trying to establish standard rules for ideal orthodontic treatments. The Apollo Belvedere, a Greek statue from antiquity was considered the benchmark of human facial harmony.8,9 Criticisms of the bone hypothesis were based on the well-known action of local and environmental forces in reshaping the periosteal bones, as well as on the contributory role of sutures and cartilages.10,11 In the 1940s, the suture/genetic hypothesis was brought forward. Weinmann and Sicher12 affirmed that the connective tissue and cartilages had a leading role in craniofacial growth. Furthermore, they argued that bone growth was genetically controlled by these structures with the expanding tissue pushing the bones apart. Only the periosteum molding was controlled by local forces (Fig. 2). Contextually to this orthodontics period, while Erwin Schro¨dinger, 1940, was claiming that proteins could act as genes, Avery’s experiments brought new discoveries showing the importance of DNA and opened further frontiers on transferring hereditary traits.13 The ‘sutural hypothesis’ was mainly criticized from a clinical (e.g. the hydrocephalous condition) and embryological point of view (the absence of cartilage precursors in face bones). As a matter of fact, further histological studies stated that the sutural growth was an example of periosteal growth.14,15 The last genetic hypothesis, the ‘nasal septum hypothesis’, arose around the 1950s with J. H. Scott. The author affirmed that the nasal septum cartilage had a primary role in the prenatal period and during the first years of postnatal craniofacial growth. This
Figure 2 The genetically controlled sutural tissue pushes away the bone edges and causes growth.
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Figure 3 Cartilages have the main role in craniofacial development. Their growth, always genetically controlled, influences the craniofacial one.
cartilage is buttressed against the cranial base and pushes the mid-face forward and downward. The mandibular condyle cartilage behaves in the same way as the cranial base and the nasal septum structure, directly causing mandibular growth14 (Fig. 3). This genetic hypothesis is still part of a period of ferment concerning DNA discoveries (see Watson and Crick16) where the role of genes was a key aspect to explain craniofacial growth. In conclusion, the above theories claimed that craniofacial growth was unchangeable, almost exclusively determined by hereditary factors, and ruled by genes. As a clinical consequence orthodontists could work on dental-alveolar area only. There was no chance their intervention would interfere with genetic patterns.
Functional hypothesis In the 1960s, the first doubts that genes were the only factors influencing cranio-facial growth came from the Jacob and Monod17 studies. Their experiments on Lac-Operon showed that an environmental agent could affect genetic transcription. In the same period, the Moss Functional Hypothesis18,19 made a significant change in the orthodontics scenario, since it considered that the genetic factor was not the only key element affecting craniofacial growth. As Carlson20 stated, there was a shift from competing theories to competing paradigms, because the ‘unchangeable’ genetic theory was replaced by the ‘plastic’ functional paradigm. Moss moved the attention towards ‘function’, considering the latter as the final result of a complex bone-tissue-space interaction. The author theorized that microskeletal units (i.e. tendons on bone surfaces) work as basic elements for the periosteal functional matrix, and macroskeletal units (i.e. nasopharynx and oropharynx for respiratory function and brain for neurocranium development) are key elements of the capsular functional matrix18,19 (Figs 4–5). As a direct consequence of Moss’ studies, orthodontists started using craniofacial VOL .
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Figure 4 Periosteal functional matrix.
growth driving devices, i.e. the Frankel Function Regulator,21,22 to control structural growth. Figure 5 Capsular functional matrix.
Synthetic hypotheses Numerous theories tried to fill the gap between the genetic and functional hypotheses. The most relevant and scientifically validated was the Synthetic Hypothesis.23 It considered the condrocranium as the key factor for the development of the cranium and the face. The condrocranium is gene-related and plays a relevant role in the development of the mid-face and cranial vault. Likewise the mandible and other structures of the face are under the control of environmental factors (Fig. 6). Another synthetic hypothesis was the Servosystem Theory. Petrovic24,25 described the cranial base synchondrosis and septum cartilage, which are genetically and endocrine regulated, as crucial components for both upper maxillary development and its spatial positioning. As a result, the mandible adapts itself to the occlusal deviation, activating periodontal and temporomandibular joint proprioceptors, which in turn inform the Central Nervous System about the variation. This activates a topdown response that stimulates condylar growth through the action of mandibular muscles (Fig. 7). So far the occlusion acts as a ‘comparator’ for the craniofacial growth in this servosystem. All the theories described above drove the attention mainly to sutures, cartilages and functional matrixes. However, the lack of scientifically proven concepts led further studies to focus on two additional specific structures: the mandibular condyle and the spheno-occipital synchondrosis. Mandibular condyle Current opinions tend to consider the condylar cartilage growth as purely adaptive, or compensatory. Several studies have demonstrated that in animal models, keeping the mandible in a postural protrusion, results in the mandibular cartilage increasing its thickness, whereas a postural retrusion decreases it.1,26 An additional study showed that an anterior displacement of the articular disc can stop the horizontal mandibular growth.27 Conversely, mechanical stimuli can produce variation in the speed of mandibular growth. Both low amplitude, high frequency vibration28 and electric stimuli29 seem
to induce an active growth of the cartilage matrix and an increase in vascular flow. This creates a cascade of growth-factors-mediated effects. Shum et al.30 demonstrated a positive correlation between an increase in gene-expression of Vascular Endothelial Growth Factor and mandibular growth in mice. Similar results were obtained by Tang and Rabie31 for the expression of Run2x. Indian hedgehog expression was also found to be positively correlated with an increase in mandibular mechanical growth strain.31 Collectively all these studies reported an activation of the nucleus DNA using, mainly, mechanical transduction pathways mediated by extracellular matrix. Therefore, a mechanical stimulation produces a cellular-based condyle reaction. These mechanisms seem to be active also during the prenatal period. In the fetus, mechanical factors, such as mandibular muscle activity, have been shown to be predictive of condylar growth.32–35 In a recent study, Kjær et al.34 argued that muscle activities of the first and second pharyngeal arch are fundamental elements for normal craniofacial development. Lack of craniofacial muscle contractions may lead to hypertelorism, flat zygoma and midface, small and open mouth, microretrognathia, small tongue and abnormal palate. Another study on muscular dystrophy confirms that abnormal muscle action affects face and cranium shape.36 Therefore, not only the condyle, but also other facial bone structures show a kind of adaptive growth, linked to the action of the functional matrix. Spheno-occipital synchondrosis Theories on spheno-occipital synchondrosis (SOS) growth are different and the debate is still open. Many authors consider SOS as a growth ‘center’, exclusively influenced by genetic factors.23,30,37 Other authors believe that SOS is also modulated by mechanical stimuli. In-vitro studies demonstrated that different mechanical stresses induce a change in SOS growth. This growth seems to be mediated by different intracellular growth factors (i.e. Ihh, Parathyroidhormone-related-protein, VGEF, SOX9).38–41 These
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Figure 6 Synthetic Hypothesis. The condrocranium is placed in a central position in the craniofacial growth, as suggested by Ranly (1988).
findings were confirmed by in-vivo studies. Wang and Mao42 showed that mechanical stimuli modified the SOS cartilage growth by increasing chondrocyte proliferation. Mossey et al.43 argued that both gene action and the environmental component act at different times, having an impact on the SOS growth. Conversely, Delaire44 and Lieberman et al.45 considered the SOS growth mainly influenced by epigenetic factors. Interestingly, Lieberman et al.45 pointed out that the cranial base shape is influenced by the topdown brain growth and bottom-up face development, the so-called neural and facial space-packing.
Craniofacial Growth: Current State of the Art The study of epigenetic factors as key elements for the development of craniofacial structures introduced new frontiers as to the role of the environment on skull growth. Epigenetics clashes with the idea that DNA is the main repository of bone growth developmental formations. Corner46 stated that the genetic program is not a blueprint capable of creating an entire organism. The environment, via the extracellular 26
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matrix, modifies the shape of the cell membrane, which in turn, via the cytoskeleton, modifies the shape of the nucleus. The modified nucleus elicits modifications in protein synthesis that subsequently affect cell destiny.47 The cytoskeleton is organized according to the rules of Tensional Integrity or Tensegrity.48–50 Tensegrity key components include compression resisting elements (microtubules), and tensional elements (microfilaments, intermediate filaments), which create a seamless link among components of the extracellular matrix, cell membrane and cell nucleus. In 1997, Moss51 reviewed his Functional Matrix Hypothesis in the light of these biologic discoveries confirming, scientifically, that craniofacial development is mainly dependent on epigenetic factors. The author argued that a cascade of mechanotransduction events, based on extracellular matrix, cytoskeleton, and cell reactions between bones, periosteum and muscles could produce significant changes in craniofacial morphology. Moreover, Moss52 considered the craniofacial morphological properties in adulthood as resulting VOL .
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Figure 7 Servosystem Hypothesis.
from the action of a series of spontaneous and selforganized ontogenetic processes and mechanisms starting in the fetus. This hypothesis is based on the biodynamic metabolic fields theory,53 whose alteration is created by external/internal oriented movements. Further study54 confirmed that external mechanical stimuli could control tissue morphogenesis during embryological development. The link between mechanical stimuli and genomic expression is also underlined by Radlanski and Renz.55 These authors date back the description of the forces’ fundamental role in tissue differentiation and morphogenesis directly to His56 and Carey works.57,58 According to them, the key idea is that cells respond directly to the living environment, in particular to their neighborhood growth. This concept was additionally confirmed by Blechschmidt.53 Therefore, according to Moss,52 craniofacial development is significantly related to epigenetic stimuli which influence the destiny, function and shape of craniofacial structures from the fetal to the adulthood period.52
Future Perspectives Carlson suggested three arguments to be discussed that, if solved, could significantly improve the clinical outcome in orthodontics. The author questioned: (1)
Where the growth-related problem is located; (2) How much modification of craniofacial growth is relevant to be considered; and (3) What are the most appropriate treatment approaches that may be used to achieve the expected growth effect.20 Currently, very sophisticated cephalograms and computer programs have been developed to predict patients’ growth, create clinical-related categories, and administer ‘protocol therapies’. However, discussion is still open in order to confirm these approaches in terms of reliability, validity and ethics. Damstra et al.59 proved that cephalometric measurements are inconsistent and unreliable with respect to clinical diagnosis and treatment. These findings were confirmed by Devereux et al.60 The authors demonstrated that the probability of improving clinical decision making by adding lateral cephalometric radiographs did not make any significant difference in treatment-planning decisions. Additional studies cast doubts about orthodontic categories and classes. Thordarson et al.61 compared Icelandic children between 6 and 16 years of age with a similar Norwegian sample showing small differences in maxillary prognathism and mandibular plane angle as well as significant differences in the inclination of lower incisors.61 Ishii et al.62 demonstrated substantial imbalances in class III skeletal
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malocclusion between Japanese girls and Caucasian populations. Furthermore, according to Sadeghianrizi et al.,63 craniofacial morphology differs between obese and normal adolescents. Obesity was directly associated with bi-maxillary prognathism and greater facial diameters. Additionally, the use of selective serotonergic reuptake inhibitors or less selective tricyclic antidepressant drugs during pregnancy is associated with alteration in craniofacial morphogenesis.64,65 Therefore, although orthodontists still widely use skeletal classes classification as the gold clinical standards, recent medical and biological discoveries shed light on the potential inaccuracy of these standards. Van der Linden66 argued that facial orthopedics does not seem to have an ultimate effect on the morphology of the facial skeleton, and there is no possibility of establishing the right period of treatment; considerations also confirmed by Delaire44 in the treatment of Class III skeletal malocclusion. In order to remove the gap between patient need and treatment, there is probably the need to widen the interaction between the skull and the whole body by considering a broader holistic approach. Several authors argued the close relationship between the respiratory system and the craniofacial growth. Some research showed that breathing patterns affect the inter-molar and inter-canine distance,67 as well as the incisors position.68 Zhang69 demonstrated that children with adenoidal hypertrophy show a vertical growth pattern, larger gonion, and a retrusive chin. Pereira et al.70 suggested adenotonsillectomy on growing patients to improve dental parameters and to reduce the risk of malocclusion. Furthermore, it was documented that certain respiratory diseases, such as obstructive sleep apnea can prevent the expected difference in craniofacial growth of boys and girls,71 and induce shorter maxillary and mandibular lengths,72 lateral cross-bite, and an increased overjet.73 In addition, the decreased chewing activity during mouth breathing can negatively affect the vertical position of posterior teeth, leading to malocclusion.74 The latter can be considered a risk factor in the etiology of headaches in children and adolescents.75 Moreover, it was shown that abnormal facial muscle activity, as measured by dynamometer and surface electromyography, was related to defects in oral habits and breathing,76 as well as to malocclusion.77 Interestingly, the oral breathing seems to induce craniofacial growth patterns not only by a mechanistic alteration in the muscular balance and head and tongue position, but also by a more complex 28
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sequence of epigenetic events involving abnormal nocturnal secretion of growth hormone.78 Considering the connection between dental occlusion disorders and ocular defects, several studies documented this strong correlation.79–82 Furthermore, mandibular deviations and TMJ disorders were shown to be associated with ocular convergence problems.83,84 Interestingly, the use of rapid maxillary expansion can produce diverse side effects, including strabismus.85 However, the same procedure can significantly change the posture of the head and the position of the scapulae,86 leading to consideration of effects on a broader bodily scale. In fact, according to Springate,87 the change in posture was primarily linked to the growth direction of the face, specifically the changing position of the mandible and tongue. Korbmacher et al.88 demonstrated a significant correlation between iliac spine blockage, articulation disorders and tongue dysfunction, whereas functional asymmetry of the upper cervical spine was significantly correlated with incompetent lips.88 An additional study pointed out that children with unilateral crossbite had higher prevalence of oblique shoulder, scoliosis, oblique pelvis, and functional leg length difference.89 Similarly, subjects with class III skeletal malocclusion or transverse maxillary constriction exhibited significant deviation of the cervical column.90,91 Interestingly, Lippold et al.92 showed that the sagittal spinal posture seems to be related to craniofacial morphology, as well as being influenced by trunk rotation and pelvic tilt and rotation.93 Other researchers corroborated the association between morphologic deviations of the cervical vertebral column and craniofacial morphology,94 as well as between tongue dimension and craniofacial development.95 96 Standerwick and Roberts argued that the viscerocranium growth is influenced by the superficial musculoaponeurotic systems of the head, as a result of cephalic brain growth and cranial rotation. This hypothesis endorses the theories of Solow and Sandham,97 who argued that the extended craniocervical posture affects craniofacial growth by a passive stretching of the soft tissue layers. In addition, new embryologic and physics discoveries will suggest additional potential fields of interest. From an embryological point of view, Jheon and Schneider98 suggested that the neuralcrest-derived mesenchyme acts as the dominant source of species-specific patterning information. Its developmental programs possess plasticity, a measure of the extent to which ontogenetic systems can respond to internal and external perturbations and VOL .
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produce an integrated and sustainable phenotype. Therefore, the shape of craniofacial structures can be influenced by external stimuli at an early stage and can change craniofacial development parameters. Considering physics, scientists recently claimed that quantum mechanics could be applied to different medical fields, including mutations, phenotype changes and evolution.99 In quantum mechanics, the information is transferred using what is referred to as a phase coherence state. This condition is known as quantum phenomena in biological systems, and seems to respect the tensegrity structure model in living cells. Studies showed that interferences within this system could produce perturbations in the biological processes that in turn lead to cell fate changes.100 Interestingly, Moss52 suggested that craniofacial growth is a ‘tuned system’ that adapts itself to the environment and the cell. The author argued that the theoretical Functional Matrix Hypothesis Revisited concept considered biological systems as Complex Adaptive Systems, and within this system, minor changes in the epigenetic input can cause huge fluctuations in the morphological output. Furthermore, Moss contemplated that ontogenesis involves nonlinear processes, and is not fully predictable. For those reasons, Korbmacher et al.88 concluded with the importance of an early interdisciplinary and complementary screening to assure a physiological development of the orofacial region, whereas Silvestrini-Biavati et al.101 argued that, in orthodontics diseases, postural, orthoptic, osteopathic and occlusal variables were often clinically associated, and therefore a multidisciplinary medical approach for treatment is advised.101 Undoubtedly, there is the need to improve the diagnostic process by means of embracing other professionals (i.e. orthodontists, ophthalmologists, pneumologists, orthopedists, osteopaths), and more adequate investigation methods (i.e. Transcutaneous Electrical Nerve Stimulation or Surface Electromyography) to fulfill the individual’s needs. Therefore, as suggested by Krogman,2 the combination between different scientific fields to enhance knowledge on the optimum clinical decision making in a patient needs-based approach will be the future of orthodontics care.
Conclusions The understanding of the complex evolution of craniofacial growth, and methods to cope with its dynamics is essential for delivering the optimal orthodontics care. Dentistry is facing a change where the use of pre-determined protocols and methodologies possibly reduce the efficacy of treatment and
Craniofacial growth: evolving paradigms
diagnosis. The use of a multidisciplinary scenario where different professionals can share, in synergy and knowledge, can enhance the ability of specialists to deliver the most reliable clinical diagnosis and mold treatment according to the subject.
Acknowledgements The authors sincerely thank Dr Marta Martelli for her help in reviewing and editing the paper.
Disclaimer statements Contributors GC carried out the literature review and wrote the draft. GC and FC wrote and approved the final paper. Funding No funds were received for the present manuscript. Conflicts of interest The authors declare no conflict of interests in relation to this study. Ethics approval No ethical approval was required for this work.
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