Australian Dental Journal
The official journal of the Australian Dental Association
Australian Dental Journal 2014; 59:(1 Suppl): 6–12 doi: 10.1111/adj.12131
The genesis of craniofacial biology as a health science discipline GH Sperber,* SM Sperber† *University of Alberta, Edmonton, Canada. †University of Colorado, Denver, Colorado, USA.
ABSTRACT The craniofacial complex encapsulates the brain and contains the organs for key functions of the body, including sight, hearing and balance, smell, taste, respiration and mastication. All these systems are intimately integrated within the head. The combination of these diverse systems into a new field was dictated by the dental profession’s desire for a research branch of basic science devoted and attuned to its specific needs. The traditional subjects of genetics, embryology, anatomy, physiology, biochemistry, dental materials, odontology, molecular biology and palaeoanthropology pertaining to dentistry have been drawn together by many newly emerging technologies. These new technologies include gene sequencing, CAT scanning, MRI imaging, laser scanning, image analysis, ultrasonography, spectroscopy and visualosonics. A vibrant unitary discipline of investigation, craniofacial biology, has emerged that builds on the original concept of ‘oral biology’ that began in the 1960s. This paper reviews some of the developments that have led to the genesis of craniofacial biology as a fully-fledged health science discipline of significance in the advancement of clinical dental practice. Some of the key figures and milestones in craniofacial biology are identified. Keywords: Craniofacial, dental history, dentistry, teeth.
‘Your face, my thane, is as a book Where men may read strange matters’ Macbeth, Act 1, Scene 3.
research into the structural biology of the craniofacial complex. However, the earliest identification of a ‘craniofacial’ disorder was Charles Darwin’s observation in 1875 of anodontia in anhidrotic ectodermal dysplasia.5
INTRODUCTION As a basic science, craniofacial biology encompasses a wide field of disciplines related to the full range of the practice of dentistry. The disparate technologies of the application of dental materials, radiology and digital imaging, oral and maxillofacial surgery and gene identification are ultimately applicable to the diagnosis, prognosis, prevention and treatment of orofacial diseases and disorders. The identification of craniofacial biology as a distinct basic science entity related to the practice of dentistry evolved slowly over many years concurrent with the explosive growth of molecular biology during the past 50 years.1 The determination of the primitive gnathostomata (gnathos = jaw; stoma = mouth) as the evolutionary precursors of the derived craniofacial complex provides the background to a developmental understanding of the human oronasal masticatory apparatus.2,3 The recognition of the correct number of human chromosomes in 1956 by Tijo and Levan4 set the stage for the subsequent surge in 6
TECHNOLOGY The pioneering work of Michael Buonocore in 1955, who invented acid etching of enamel, created the technique of adhesive dentistry that has revolutionized conservative dentistry and orthodontics with restorations and bracket attachments.6 However, it was not until the 1970s that the first bonding agents became available and another decade before predictable adhesive composites became the restorative material of choice in dentistry. Pit and fissure sealants provided a paradigm shift in conservative dentistry from a mechanistic replacement to a prevention-orientated approach.7 Seminal developments in scientific advances and technology and computerization over the past half century have transformed dentistry in unimaginable ways to the advantage of both the patient and the practitioner.8 A list of key events in the genesis and growth of craniofacial biology is provided in Table 1. © 2014 Australian Dental Association
Genesis of craniofacial biology as a health science discipline GENETICS The identification of the role of genes in developmental craniofacial biology has been explosive.9,10 The implications for future dental practice are yet to be fully exploited, but will undoubtedly cause transformational changes in diagnoses and treatments.11 The genetics of peculiarly craniofacial syndromes that distort facial composure, as in Treacher Collins and Van der Woude syndromes, have been identified for their enhanced diagnosis and possible therapeutic intervention.12 The underlying genetic predisposition to clefts of the face, particularly those of the upper lip and palate, has been intensively explored.13–16 The clinical significance of facial clefts gave rise to learned societies dedicated to the diagnosis, prognosis and treatment of these anomalies, such as the American Cleft Palate Association in 1951 and the Craniofacial Society of Great Britain and Northern Ireland in 1970. The capability of diagnosing systemic diseases by analysis of salivary proteins provides an expanded role for craniofacial biology in the field of general medicine
and interpreting overall health.17–19 The non-invasive collection of saliva for diagnosis is hugely advantageous over serum as a diagnostic fluid.20 The mouth is in many ways the mirror of the body, and the facial complex mirrors our genetic endowment. The role of genetics in the development of the dentition has been investigated at a clinical level in epidemiological and family studies, in patients with chromosomal abnormalities and in twins.21–24 At the molecular level, over 300 genes have been identified largely using murine models, with genetic, epigenetic and environmental factors interacting with the formation of the teeth.25–27 This dynamic process of the mature tooth emerging from molecular, cellular and tissue interactions demonstrates the characteristics of a biological Complex Adaptive System.28 EMBRYOLOGY Craniofacial biology can be separately identified as divergent from general biology in respect of its embryology and its evolutionary significance. Cranial neural crest tissue differs from postcranial neural crest in sev-
Table 1. Key events in the genesis and growth of craniofacial biology 1875 1925 1950 1951 1955 1956 1970 1972 1973 1974 1975 1979 1981 1985 1990 1994 1998 2001 2002 2002 2003 2004 2007 2008 2009 2010 2011 2011 2012 2012 2012 2012 2012 2012 2012 2013 2014
Darwin’s identification of hereditary anodontia Dart describes the dentition of Australopithecus africanus Neural crest identified American Cleft Palate Association established Acid etch bonding technique described Exact human chromosome number identified Craniofacial Society of Great Britain and Northern Ireland founded Prenatal diagnosis of neural tube defects Craniofacial Embryology textbook published Concept of neurocristopathies introduced Society of Craniofacial Genetics founded Developmental Craniofacial Biology published Craniofacial Genetics and Developmental Biology Journal established Osseointegration for dental implantology established Journal of Craniofacial Surgery established University Chair of Craniofacial Development established, Kings College London National Institute of Dental Research converts to National Institute of Dental and Craniofacial Research Human genome published Craniofacial Development, Growth and Evolution published Understanding Craniofacial Anomalies Clinical Dental Genetics published 1st Biennial Gordon Research Conference on Craniofacial Morphogenesis International Collaborating Network in Craniofacial Genetics and Development established Human salivary proteome published Special Issue on Oral Growth and Development, Archives of Oral Biology, a multidisciplinary journal of oral and craniofacial sciences Craniofacial Biology and Craniofacial Surgery Oral and Craniofacial Tissue Engineering established Yuendumu: Legacy of a longitudinal growth study in Central Australia published The Birth of a Discipline: Craniofacial Biology published Salivary diagnostic capabilities identified Diet of Australopithecus sediba published Genetic loci (GWAS) identification of facial morphology Mineralized Tissues in Oral and Craniofacial Science published Dento/Oro/Craniofacial Anomalies and Genetics published International Workshop on Oral Development as a Complex Adaptive System Stem Cells in Craniofacial Development and Regeneration published Special Issue of the Australian Dental Journal on Craniofacial Biology published
© 2014 Australian Dental Association
Slavkin5 Dart66 Horstadius34 Buonocore6 Tijo and Levan4 Brock and Sutcliffe85 Sperber30 Bolande39 Sperber86 Slavkin87 Melnick and Slavkin88 Branemark et al.81 Habal89 Sharpe Slavkin90 Lander et al. and Venter et al.91,92 Meikle93 Mooney and Siegel94 Kieser and Kramer32 Townsend, Alvesalo and Brook21 Denny et al.17 ed. Brook95 Sarnat and Bradley96 Jensen97 Brown et al.98 Slavkin90 Kwok19 Henry et al.67 Liu et al.10 McCauley and Somerman99 Bloch-Zupan et al.100 Brook et al.102 Huang and Thesleff101 eds. Townsend and Brook103 7
GH Sperber and SM Sperber eral aspects.29 The publication of Craniofacial Embryology and its subsequent editions of Craniofacial Embryogenetics and Development30,31 identified the specialized nature of head and neck embryology distinct from postcranial development (Figs. 1 and 2). The publication of Clinical Dental Genetics by Kieser and Kramer32 further identified the distinctiveness of this field of enquiry. Head and neck embryology is distinguished by its origins from a peculiarly distinct cranial neural crest tissue, a term originally proposed by Marshall in 187933 to define a group of cells in the embryonic neural fold that gives rise to craniofacial structures. The precise origin of the cranial neural crest is still controversial, but its derivatives are fundamental to craniofacial structures.34 The identification of rudimentary neural crest in a non-vertebrate chordate35 set the stage for the emergence of the ‘new head’ expounded upon by Gans and Northcutt.36 The evolution of the face, based upon genetics and epigenetics, has been explored by Baynam et al.37 The capacity of neural crest stem cells as a progenitor for derived craniofacial tissues provides the potential for regenerative therapy and rehabilitation of defects or trauma of the head.38 The neural crest-based origin of Fig. 2 Cover of textbook published by PMPH-USA (2010) depicting regions of gene expression in a human embryonic face of 7 weeks post-conception age. The red area represents WNT (Wingless type), light purple PAX6 (Paired box 6), pink DLX (Distal-less homeobox), blue BARX (Barx homeobox), dark purple GSC (Goosecoid homeobox), orange BMP (Bone morphogenetic protein), yellow FGF8 (Fibroblast growth factor 8), green PAX9 (Paired box 9). The area distributions are displayed inside the book cover. (Courtesy of Beth Lozanoff).
craniofacial diseases gave rise to the category of neurocristopathies.39 Studies of the morphogenesis of the dentition have contributed to the understanding of embryological processes, identifying the roles of cellular inactivation and apoptosis as well as creating new understanding by 3D reconstructions.40,41 The embryology of teeth has been used extensively as a model in analyses related to developmental patterning, signalling and evolution. The extensive data on tooth development as a developmental model are enhanced by the pivotal role of dentitions in documenting the evolution of vertebrates. The archaeological preservation of teeth, due to their hard tissue durability, plays a role in tracing evolutionary relationships.42,43 Fig. 1 Cover of textbook published by BC Decker Inc. (2001), depicting a 3D computer-reconstructed head of a sectioned human 55-day old foetus. The brain and eyes are rendered in blue, the cartilages in white, the oropharynx in green, the inner ear in yellow, the trigeminal nerve ganglion in brown, the arteries in red. The skin outline is translucent. (Courtesy of SM Sperber). 8
COMPARATIVE ODONTOLOGY Genetic studies have revealed why the polyphyodont dentition of sharks was reduced to the diphyodont © 2014 Australian Dental Association
Genesis of craniofacial biology as a health science discipline dentition of mammals and humans.44 Indeed, the early regression of the dental lamina underlies the development of our diphyodont dentition.45 It is astonishing that comparative odontology has not featured more significantly in craniofacial biology, despite the fact that much experimental dental research has been performed on laboratory animals. Apart from knowing of the continuously growing incisors of rodents, few dentists are aware of the vast variety of dentitions encountered in animals.42,46 While the major purpose of teeth is to serve as prehensile and masticatory organs, they have been employed as diversely as combing instruments by lemurs and speech articulation in humans. The dermal teeth of catfish47 and the tusks of narwhals48 serve as sensory organs. The enormous variety of dentitions, ranging from the haplodont, homodont teeth of sharks to the complex arrangement of cusps and ridges in the teeth of carnivores, graminivores and omnivores reflect adaptations to different diets.49–51 The peculiar dentitions of extinct creatures and their odontostomatognathic oddities add to the astounding diversity of craniofacial adaptations to dietary distinctions.52 DENTAL ANATOMY AND ANTHROPOLOGY The origins of craniofacial biology are rooted in the teeth that are fundamental to the purpose and function of the oro-dento-gnatho-facial complex. Teeth have played a key role in discerning human evolution.53 The earliest recorded reference to human tooth numbers was made by Aristotle,54 who claimed that men have more teeth than women, ‘by reason of the abundance of heat and blood which is more in men than women’. Although twice married, it never occurred for him to examine his wives’ mouths. The first serious scientific study of teeth was the publication by Bartolomeo Ruspini (1768): A Treatise on the Teeth55 followed by John Hunter (1771): The natural history of the human teeth.56 Skinner’s A Treatise on the Human Teeth was published in 1801,57 followed by Longbothom (1802),58 who wrote A Treatise on Dentistry, then by A Nasmyth (1839): Researches on the development, structure and diseases of the teeth,59 with the subsequent publication by CS Tomes (1876) A Manual of Dental Anatomy.60 The anthropological perspective of dentitions was initially pursued by TD Campbell in his University of Adelaide doctoral thesis, Dentition and Palate of the Australian Aboriginal (1925),61 followed by JC Middleton Shaw’s Witwatersrand University dissertation in 1931, The Teeth, the Bony Palate and the Mandible in Bantu Races of South Africa.62 The establishment of the journal Dental Anthropology in 1986 provided a forum for an increasingly wide study of the role of dental morphology in palaeoan© 2014 Australian Dental Association
thropology, genetics, evolution, dietary demands and environmental impacts on teeth. The field of dental anthropology was dominated by Albert Dahlberg, who co-organized the first International Symposium on Dental Morphology, held in 1965, with resulting papers being published in the Journal of Dental Research in 1967.63 His study of The Face and Dentition of the Australasian Population: Preface and Overview provided an introduction to a wide-ranging anthropological analysis of dentitions.64 New measurement techniques outlined in the ‘Radiology and Imaging’ section below are enabling increased understanding of relationships in archaeological as well as modern populations.65 PALAEOANTHROPOLOGY The skull and teeth provide overwhelming evidence of hominid evolution, in contrast to the comparative paucity of postcranial evolutionary evidence. The identification of the Australopithecine Taung infant skull in 1925 by the Australian, Raymond Dart66 as a new genus predecessor to modern mankind was based not only on its small cranial capacity, but most significantly upon its hominid dentition contrasting with that of the apes. The subsequent explosion of Australopithecine discoveries has led to studies of the lifestyle of these 2.5 million year old fossils by analysis of their diets based on their dentitions.67 The techniques of analysing attritional wear and scratch marks on the preserved pristine enamel by scanning electron microscopic analysis provide evidence of dietary content.68,69 Even more remarkable is the spectroscopic analysis of the varying ratios of isotopes of 12C and 13 C in dental enamel to establish dietary constituents of 2.5 million years ago. Electron spin analysis of enamel provides dating of fossils beyond the limit of radiocarbon dating.70 Analysis of longstanding oral pathology and mitochondrial (mtDNA) haplotyping has been used to suggest a probable familial basis in two Neandertals.71 Also, DNA sequencing of dental calculus has revealed changes in the composition of the oral microbiota with alterations in diet from Neolithic times to the Industrial Revolution.72 CRANIOFACIAL SYNDROMOLOGY The developmental distortions peculiar to head and neck dysmorphology have given rise to a specialized field of congenital malformations devoted to the nosology, diagnosis, aetiology, prognosis and treatment modalities of syndromic craniofacial disorders. The field was initiated by Robert Gorlin’s epic Syndromes of the Head and Neck, first published in 1964,73 with five following editions ending in 2010.74 Richard Goodman’s Atlas of the Face in Genetic Dis9
GH Sperber and SM Sperber orders75 expanded the role of genes in craniofacial disorders. The field has exploded with the increasing identification of gene-specific malformations.
tional impact of wearing a donor’s face, still need to be assessed.84 CONCLUSIONS
RADIOLOGY AND IMAGING The technical revolution in medical and dental imaging over the past century has been dramatic. The initial chemical transformation of radiation images on radiosensitive film has been displaced by digital imaging technology, greatly enhancing diagnostic capabilities. In the 20th century, radiographic cephalometry was a pioneering advance in assessing craniofacial growth and allometry. The invention of the cephalometer in 1931 by B Holly Broadbent allowed longitudinal studies of changes in facial growth, particularly valuable in orthodontic assessments. Further developments in imaging the craniofacial structures are discussed in the paper by Anderson and colleagues in this Special Issue.76 The advent of obstetrical ultrasonography has had a profound effect upon the prenatal diagnosis of congenital defects.77 The technical innovations of magnetic resonance imaging (MRI) promises ever more refinement of investigative and diagnostic capabilities of craniofacial development and its anomalies.78 Just as ‘genomics’ has transformed genetics, so ‘phenomics’ is being recognized as essential to advance genotype/phenotype alignment and the understanding of complex developmental processes. Phenomics involves the measurement of phenomes or phenotypes that include the various physical and biochemical features of organisms. Such developments as image analysis and laser scanning are providing more extensive, accurate, reproducible phenotypic data of the human dentition.65 The paper by Yong and colleagues in this Special Issue explores the field of dental phenomics in greater depth.79 SURGERY The era of prosthetic replacement of teeth (‘blood and vulcanite’ dentistry) as a treatment modality of choice came to an end as craniofacial biology became more applicable to clinical practice. The advent of implantology as a consequence of osseointegration studies, of distraction osteogenesis, and the promise of stem cell tissue engineering and regeneration have revolutionized the current surgical approach to rehabilitation of orofacial deficiencies.80–82 The remarkable capabilities of face transplantations are rooted in the advances in immunosuppression of foreign tissue rejection and preplanning with cephalometric analysis of recipient hosts.83 However, the ethical issues of transplanted faces and their facial expressions that are no longer congruent with their host’s personality, and the emo10
The emergence of craniofacial biology as a legitimate basic science with specific direction attuned to orofacial and dental clinical practice has led to its recognition as a health science discipline divergent from general biology. Its distinct identification has led to its recognition by university departments, research institutions and specialist societies. The application of the inventions and discoveries under the umbrella of craniofacial investigations has transformed the clinical practices of dentistry and its specialties to the ultimate benefit of patients. Craniofacial biology has made a major contribution to transforming dentistry from a dexterous craft to a clinical academic discipline that has contributed greatly to the general body of knowledge. DISCLOSURE The authors have no conflicts of interest to declare. REFERENCES 1. Sperber GH. Transitions in craniofacial biology: a tribute to Bernard G Sarnat. J Craniofac Surg 2012;23:124–125. 2. Janvier P. Developmental biology: led by the nose. Nature 2013;493:169–170. 3. Oisi Y, Ota KG, Kuraku S, Fujimoto S, Kuratani S. Craniofacial development of hagfishes and the evolution of vertebrates. Nature 2013;493:175–180. 4. Tijo J-H, Levan A. The chromosome number of man. Hereditas 1956;42:1–6. 5. Slavkin HC. Charles Darwin and the foundations of clinical genetics in dentistry. J Am Dent Assoc 1997;128:241–245. 6. Buonocore MG. A simple method of increasing the adhesion of acrylic filling materials to enamel surfaces. J Dent Res 1955;34:849–853. 7. Cueto EI, Buonocore MG. Sealing of pits and fissures with an adhesive resin: its use in caries prevention. J Am Dent Assoc 1967;75:121–128. 8. Gutmann JL. The evolution of America’s scientific advancements in dentistry in the past 150 years. J Am Dent Assoc 2009;140:S8–S15. 9. Sperber GH. The genetics of odontogenesis: implications in dental anthropology and palaeo-odontology. Dent Anthropol 2004;17:1–7. 10. Liu F, van der Lijn F, Schurmann C, et al. A genome-wide association study identifies five loci influencing facial morphology in Europeans. PLoS Genet 2012;8:e1002932. 11. Wright JT, Hart TC. The genome projects: implications for dental practice and education. J Dent Educ 2002;66:659–671. 12. van Gijn DR, Tucker AS, Cobourne MT. Craniofacial development: current concepts in the molecular basis of Treacher Collins syndrome. Br J Oral Maxillofac Surg 2013;51:384– 388. 13. Stuppia L, Capogreco M, Marzo G, et al. Genetics of syndromic and nonsyndromic cleft lip and palate. J Craniofac Surg 2011;22:1722–1726. © 2014 Australian Dental Association
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88. Melnick M, Slavkin HC. Editorial. J Craniofac Genet Dev Biol 1981;1:3. 89. Habal MB. Editorial. J Craniofac Surg 1990;1: p. II. 90. Slavkin HC. The birth of a discipline: craniofacial biology. Newtown, PA: AEGIS Communications, 2012. 91. Lander ES, Linton LM, Birren B, et al. Initial sequencing and analysis of the human genome. Nature 2001;409:860–921. 92. Venter JC, Adams MD, Myers EW, et al. The sequence of the human genome. Science 2001;29:1304–1351. 93. Meikle MC. Craniofacial development, growth and evolution. Norfolk: Bateson Publishing, 2002. 94. Mooney MR, Siegel MI, eds. Understanding craniofacial anomalies. New York: Wiley-Liss, 2002. 95. Brook A. Editorial. Research collaboration initiative. Arch Oral Biol 2009;54S:S1–S2. 96. Sarnat BG, Bradley JP. Craniofacial biology and craniofacial surgery. Singapore: World Scientific, 2010. 97. Jensen O. Editorial. A new journal: too natural. Oral Craniofac Tiss Engin 2011;1. 98. Brown T, Townsend G, Pinkerton S, Rogers J. Yuendumu: legacy of a longitudinal growth study in Central Australia. Adelaide: University of Adelaide Press, 2011. 99. McCauley LK, Somerman MJ. Mineralized tissues in oral and craniofacial science: biological principles and clinical correlates. Ames, IA: Wiley-Blackwell, 2012. 100. Bloch-Zupan A, Sedano H, Scully C. Dento/oro/craniofacial anomalies and genetics. London: Elsevier, 2012. 101. Huang GTJ, Thesleff I. Stem cells in craniofacial development and regeneration. Hoboken, New Jersey: Wiley-Blackwell, 2013. 102. Brook AH, Brook O’Donnell M, Hone A, et al. General and craniofacial development are complex adaptive processes influenced by diversity. Aust Dent J 2014; doi: 10.1111/adj. 12158 [Epub ahead of print]. 103. Townsend GC, Brook AH, eds. The face, the future, and dental practice: how research in craniofacial biology will influence patient care. Aust Dent J 2014; doi: 10.1111/adj. 12157 [Epub ahead of print].
Address for correspondence: Professor Geoffrey Sperber Faculty of Medicine and Dentistry 5383 Edmonton Clinic Health Academy University of Alberta 11405 – 87th Avenue NW Edmonton, AB T6G 1C9 Canada Email: [email protected] © 2014 Australian Dental Association
The official journal of the Australian Dental Association
Australian Dental Journal 2014; 59:(1 Suppl): 6–12 doi: 10.1111/adj.12131
The genesis of craniofacial biology as a health science discipline GH Sperber,* SM Sperber† *University of Alberta, Edmonton, Canada. †University of Colorado, Denver, Colorado, USA.
ABSTRACT The craniofacial complex encapsulates the brain and contains the organs for key functions of the body, including sight, hearing and balance, smell, taste, respiration and mastication. All these systems are intimately integrated within the head. The combination of these diverse systems into a new field was dictated by the dental profession’s desire for a research branch of basic science devoted and attuned to its specific needs. The traditional subjects of genetics, embryology, anatomy, physiology, biochemistry, dental materials, odontology, molecular biology and palaeoanthropology pertaining to dentistry have been drawn together by many newly emerging technologies. These new technologies include gene sequencing, CAT scanning, MRI imaging, laser scanning, image analysis, ultrasonography, spectroscopy and visualosonics. A vibrant unitary discipline of investigation, craniofacial biology, has emerged that builds on the original concept of ‘oral biology’ that began in the 1960s. This paper reviews some of the developments that have led to the genesis of craniofacial biology as a fully-fledged health science discipline of significance in the advancement of clinical dental practice. Some of the key figures and milestones in craniofacial biology are identified. Keywords: Craniofacial, dental history, dentistry, teeth.
‘Your face, my thane, is as a book Where men may read strange matters’ Macbeth, Act 1, Scene 3.
research into the structural biology of the craniofacial complex. However, the earliest identification of a ‘craniofacial’ disorder was Charles Darwin’s observation in 1875 of anodontia in anhidrotic ectodermal dysplasia.5
INTRODUCTION As a basic science, craniofacial biology encompasses a wide field of disciplines related to the full range of the practice of dentistry. The disparate technologies of the application of dental materials, radiology and digital imaging, oral and maxillofacial surgery and gene identification are ultimately applicable to the diagnosis, prognosis, prevention and treatment of orofacial diseases and disorders. The identification of craniofacial biology as a distinct basic science entity related to the practice of dentistry evolved slowly over many years concurrent with the explosive growth of molecular biology during the past 50 years.1 The determination of the primitive gnathostomata (gnathos = jaw; stoma = mouth) as the evolutionary precursors of the derived craniofacial complex provides the background to a developmental understanding of the human oronasal masticatory apparatus.2,3 The recognition of the correct number of human chromosomes in 1956 by Tijo and Levan4 set the stage for the subsequent surge in 6
TECHNOLOGY The pioneering work of Michael Buonocore in 1955, who invented acid etching of enamel, created the technique of adhesive dentistry that has revolutionized conservative dentistry and orthodontics with restorations and bracket attachments.6 However, it was not until the 1970s that the first bonding agents became available and another decade before predictable adhesive composites became the restorative material of choice in dentistry. Pit and fissure sealants provided a paradigm shift in conservative dentistry from a mechanistic replacement to a prevention-orientated approach.7 Seminal developments in scientific advances and technology and computerization over the past half century have transformed dentistry in unimaginable ways to the advantage of both the patient and the practitioner.8 A list of key events in the genesis and growth of craniofacial biology is provided in Table 1. © 2014 Australian Dental Association
Genesis of craniofacial biology as a health science discipline GENETICS The identification of the role of genes in developmental craniofacial biology has been explosive.9,10 The implications for future dental practice are yet to be fully exploited, but will undoubtedly cause transformational changes in diagnoses and treatments.11 The genetics of peculiarly craniofacial syndromes that distort facial composure, as in Treacher Collins and Van der Woude syndromes, have been identified for their enhanced diagnosis and possible therapeutic intervention.12 The underlying genetic predisposition to clefts of the face, particularly those of the upper lip and palate, has been intensively explored.13–16 The clinical significance of facial clefts gave rise to learned societies dedicated to the diagnosis, prognosis and treatment of these anomalies, such as the American Cleft Palate Association in 1951 and the Craniofacial Society of Great Britain and Northern Ireland in 1970. The capability of diagnosing systemic diseases by analysis of salivary proteins provides an expanded role for craniofacial biology in the field of general medicine
and interpreting overall health.17–19 The non-invasive collection of saliva for diagnosis is hugely advantageous over serum as a diagnostic fluid.20 The mouth is in many ways the mirror of the body, and the facial complex mirrors our genetic endowment. The role of genetics in the development of the dentition has been investigated at a clinical level in epidemiological and family studies, in patients with chromosomal abnormalities and in twins.21–24 At the molecular level, over 300 genes have been identified largely using murine models, with genetic, epigenetic and environmental factors interacting with the formation of the teeth.25–27 This dynamic process of the mature tooth emerging from molecular, cellular and tissue interactions demonstrates the characteristics of a biological Complex Adaptive System.28 EMBRYOLOGY Craniofacial biology can be separately identified as divergent from general biology in respect of its embryology and its evolutionary significance. Cranial neural crest tissue differs from postcranial neural crest in sev-
Table 1. Key events in the genesis and growth of craniofacial biology 1875 1925 1950 1951 1955 1956 1970 1972 1973 1974 1975 1979 1981 1985 1990 1994 1998 2001 2002 2002 2003 2004 2007 2008 2009 2010 2011 2011 2012 2012 2012 2012 2012 2012 2012 2013 2014
Darwin’s identification of hereditary anodontia Dart describes the dentition of Australopithecus africanus Neural crest identified American Cleft Palate Association established Acid etch bonding technique described Exact human chromosome number identified Craniofacial Society of Great Britain and Northern Ireland founded Prenatal diagnosis of neural tube defects Craniofacial Embryology textbook published Concept of neurocristopathies introduced Society of Craniofacial Genetics founded Developmental Craniofacial Biology published Craniofacial Genetics and Developmental Biology Journal established Osseointegration for dental implantology established Journal of Craniofacial Surgery established University Chair of Craniofacial Development established, Kings College London National Institute of Dental Research converts to National Institute of Dental and Craniofacial Research Human genome published Craniofacial Development, Growth and Evolution published Understanding Craniofacial Anomalies Clinical Dental Genetics published 1st Biennial Gordon Research Conference on Craniofacial Morphogenesis International Collaborating Network in Craniofacial Genetics and Development established Human salivary proteome published Special Issue on Oral Growth and Development, Archives of Oral Biology, a multidisciplinary journal of oral and craniofacial sciences Craniofacial Biology and Craniofacial Surgery Oral and Craniofacial Tissue Engineering established Yuendumu: Legacy of a longitudinal growth study in Central Australia published The Birth of a Discipline: Craniofacial Biology published Salivary diagnostic capabilities identified Diet of Australopithecus sediba published Genetic loci (GWAS) identification of facial morphology Mineralized Tissues in Oral and Craniofacial Science published Dento/Oro/Craniofacial Anomalies and Genetics published International Workshop on Oral Development as a Complex Adaptive System Stem Cells in Craniofacial Development and Regeneration published Special Issue of the Australian Dental Journal on Craniofacial Biology published
© 2014 Australian Dental Association
Slavkin5 Dart66 Horstadius34 Buonocore6 Tijo and Levan4 Brock and Sutcliffe85 Sperber30 Bolande39 Sperber86 Slavkin87 Melnick and Slavkin88 Branemark et al.81 Habal89 Sharpe Slavkin90 Lander et al. and Venter et al.91,92 Meikle93 Mooney and Siegel94 Kieser and Kramer32 Townsend, Alvesalo and Brook21 Denny et al.17 ed. Brook95 Sarnat and Bradley96 Jensen97 Brown et al.98 Slavkin90 Kwok19 Henry et al.67 Liu et al.10 McCauley and Somerman99 Bloch-Zupan et al.100 Brook et al.102 Huang and Thesleff101 eds. Townsend and Brook103 7
GH Sperber and SM Sperber eral aspects.29 The publication of Craniofacial Embryology and its subsequent editions of Craniofacial Embryogenetics and Development30,31 identified the specialized nature of head and neck embryology distinct from postcranial development (Figs. 1 and 2). The publication of Clinical Dental Genetics by Kieser and Kramer32 further identified the distinctiveness of this field of enquiry. Head and neck embryology is distinguished by its origins from a peculiarly distinct cranial neural crest tissue, a term originally proposed by Marshall in 187933 to define a group of cells in the embryonic neural fold that gives rise to craniofacial structures. The precise origin of the cranial neural crest is still controversial, but its derivatives are fundamental to craniofacial structures.34 The identification of rudimentary neural crest in a non-vertebrate chordate35 set the stage for the emergence of the ‘new head’ expounded upon by Gans and Northcutt.36 The evolution of the face, based upon genetics and epigenetics, has been explored by Baynam et al.37 The capacity of neural crest stem cells as a progenitor for derived craniofacial tissues provides the potential for regenerative therapy and rehabilitation of defects or trauma of the head.38 The neural crest-based origin of Fig. 2 Cover of textbook published by PMPH-USA (2010) depicting regions of gene expression in a human embryonic face of 7 weeks post-conception age. The red area represents WNT (Wingless type), light purple PAX6 (Paired box 6), pink DLX (Distal-less homeobox), blue BARX (Barx homeobox), dark purple GSC (Goosecoid homeobox), orange BMP (Bone morphogenetic protein), yellow FGF8 (Fibroblast growth factor 8), green PAX9 (Paired box 9). The area distributions are displayed inside the book cover. (Courtesy of Beth Lozanoff).
craniofacial diseases gave rise to the category of neurocristopathies.39 Studies of the morphogenesis of the dentition have contributed to the understanding of embryological processes, identifying the roles of cellular inactivation and apoptosis as well as creating new understanding by 3D reconstructions.40,41 The embryology of teeth has been used extensively as a model in analyses related to developmental patterning, signalling and evolution. The extensive data on tooth development as a developmental model are enhanced by the pivotal role of dentitions in documenting the evolution of vertebrates. The archaeological preservation of teeth, due to their hard tissue durability, plays a role in tracing evolutionary relationships.42,43 Fig. 1 Cover of textbook published by BC Decker Inc. (2001), depicting a 3D computer-reconstructed head of a sectioned human 55-day old foetus. The brain and eyes are rendered in blue, the cartilages in white, the oropharynx in green, the inner ear in yellow, the trigeminal nerve ganglion in brown, the arteries in red. The skin outline is translucent. (Courtesy of SM Sperber). 8
COMPARATIVE ODONTOLOGY Genetic studies have revealed why the polyphyodont dentition of sharks was reduced to the diphyodont © 2014 Australian Dental Association
Genesis of craniofacial biology as a health science discipline dentition of mammals and humans.44 Indeed, the early regression of the dental lamina underlies the development of our diphyodont dentition.45 It is astonishing that comparative odontology has not featured more significantly in craniofacial biology, despite the fact that much experimental dental research has been performed on laboratory animals. Apart from knowing of the continuously growing incisors of rodents, few dentists are aware of the vast variety of dentitions encountered in animals.42,46 While the major purpose of teeth is to serve as prehensile and masticatory organs, they have been employed as diversely as combing instruments by lemurs and speech articulation in humans. The dermal teeth of catfish47 and the tusks of narwhals48 serve as sensory organs. The enormous variety of dentitions, ranging from the haplodont, homodont teeth of sharks to the complex arrangement of cusps and ridges in the teeth of carnivores, graminivores and omnivores reflect adaptations to different diets.49–51 The peculiar dentitions of extinct creatures and their odontostomatognathic oddities add to the astounding diversity of craniofacial adaptations to dietary distinctions.52 DENTAL ANATOMY AND ANTHROPOLOGY The origins of craniofacial biology are rooted in the teeth that are fundamental to the purpose and function of the oro-dento-gnatho-facial complex. Teeth have played a key role in discerning human evolution.53 The earliest recorded reference to human tooth numbers was made by Aristotle,54 who claimed that men have more teeth than women, ‘by reason of the abundance of heat and blood which is more in men than women’. Although twice married, it never occurred for him to examine his wives’ mouths. The first serious scientific study of teeth was the publication by Bartolomeo Ruspini (1768): A Treatise on the Teeth55 followed by John Hunter (1771): The natural history of the human teeth.56 Skinner’s A Treatise on the Human Teeth was published in 1801,57 followed by Longbothom (1802),58 who wrote A Treatise on Dentistry, then by A Nasmyth (1839): Researches on the development, structure and diseases of the teeth,59 with the subsequent publication by CS Tomes (1876) A Manual of Dental Anatomy.60 The anthropological perspective of dentitions was initially pursued by TD Campbell in his University of Adelaide doctoral thesis, Dentition and Palate of the Australian Aboriginal (1925),61 followed by JC Middleton Shaw’s Witwatersrand University dissertation in 1931, The Teeth, the Bony Palate and the Mandible in Bantu Races of South Africa.62 The establishment of the journal Dental Anthropology in 1986 provided a forum for an increasingly wide study of the role of dental morphology in palaeoan© 2014 Australian Dental Association
thropology, genetics, evolution, dietary demands and environmental impacts on teeth. The field of dental anthropology was dominated by Albert Dahlberg, who co-organized the first International Symposium on Dental Morphology, held in 1965, with resulting papers being published in the Journal of Dental Research in 1967.63 His study of The Face and Dentition of the Australasian Population: Preface and Overview provided an introduction to a wide-ranging anthropological analysis of dentitions.64 New measurement techniques outlined in the ‘Radiology and Imaging’ section below are enabling increased understanding of relationships in archaeological as well as modern populations.65 PALAEOANTHROPOLOGY The skull and teeth provide overwhelming evidence of hominid evolution, in contrast to the comparative paucity of postcranial evolutionary evidence. The identification of the Australopithecine Taung infant skull in 1925 by the Australian, Raymond Dart66 as a new genus predecessor to modern mankind was based not only on its small cranial capacity, but most significantly upon its hominid dentition contrasting with that of the apes. The subsequent explosion of Australopithecine discoveries has led to studies of the lifestyle of these 2.5 million year old fossils by analysis of their diets based on their dentitions.67 The techniques of analysing attritional wear and scratch marks on the preserved pristine enamel by scanning electron microscopic analysis provide evidence of dietary content.68,69 Even more remarkable is the spectroscopic analysis of the varying ratios of isotopes of 12C and 13 C in dental enamel to establish dietary constituents of 2.5 million years ago. Electron spin analysis of enamel provides dating of fossils beyond the limit of radiocarbon dating.70 Analysis of longstanding oral pathology and mitochondrial (mtDNA) haplotyping has been used to suggest a probable familial basis in two Neandertals.71 Also, DNA sequencing of dental calculus has revealed changes in the composition of the oral microbiota with alterations in diet from Neolithic times to the Industrial Revolution.72 CRANIOFACIAL SYNDROMOLOGY The developmental distortions peculiar to head and neck dysmorphology have given rise to a specialized field of congenital malformations devoted to the nosology, diagnosis, aetiology, prognosis and treatment modalities of syndromic craniofacial disorders. The field was initiated by Robert Gorlin’s epic Syndromes of the Head and Neck, first published in 1964,73 with five following editions ending in 2010.74 Richard Goodman’s Atlas of the Face in Genetic Dis9
GH Sperber and SM Sperber orders75 expanded the role of genes in craniofacial disorders. The field has exploded with the increasing identification of gene-specific malformations.
tional impact of wearing a donor’s face, still need to be assessed.84 CONCLUSIONS
RADIOLOGY AND IMAGING The technical revolution in medical and dental imaging over the past century has been dramatic. The initial chemical transformation of radiation images on radiosensitive film has been displaced by digital imaging technology, greatly enhancing diagnostic capabilities. In the 20th century, radiographic cephalometry was a pioneering advance in assessing craniofacial growth and allometry. The invention of the cephalometer in 1931 by B Holly Broadbent allowed longitudinal studies of changes in facial growth, particularly valuable in orthodontic assessments. Further developments in imaging the craniofacial structures are discussed in the paper by Anderson and colleagues in this Special Issue.76 The advent of obstetrical ultrasonography has had a profound effect upon the prenatal diagnosis of congenital defects.77 The technical innovations of magnetic resonance imaging (MRI) promises ever more refinement of investigative and diagnostic capabilities of craniofacial development and its anomalies.78 Just as ‘genomics’ has transformed genetics, so ‘phenomics’ is being recognized as essential to advance genotype/phenotype alignment and the understanding of complex developmental processes. Phenomics involves the measurement of phenomes or phenotypes that include the various physical and biochemical features of organisms. Such developments as image analysis and laser scanning are providing more extensive, accurate, reproducible phenotypic data of the human dentition.65 The paper by Yong and colleagues in this Special Issue explores the field of dental phenomics in greater depth.79 SURGERY The era of prosthetic replacement of teeth (‘blood and vulcanite’ dentistry) as a treatment modality of choice came to an end as craniofacial biology became more applicable to clinical practice. The advent of implantology as a consequence of osseointegration studies, of distraction osteogenesis, and the promise of stem cell tissue engineering and regeneration have revolutionized the current surgical approach to rehabilitation of orofacial deficiencies.80–82 The remarkable capabilities of face transplantations are rooted in the advances in immunosuppression of foreign tissue rejection and preplanning with cephalometric analysis of recipient hosts.83 However, the ethical issues of transplanted faces and their facial expressions that are no longer congruent with their host’s personality, and the emo10
The emergence of craniofacial biology as a legitimate basic science with specific direction attuned to orofacial and dental clinical practice has led to its recognition as a health science discipline divergent from general biology. Its distinct identification has led to its recognition by university departments, research institutions and specialist societies. The application of the inventions and discoveries under the umbrella of craniofacial investigations has transformed the clinical practices of dentistry and its specialties to the ultimate benefit of patients. Craniofacial biology has made a major contribution to transforming dentistry from a dexterous craft to a clinical academic discipline that has contributed greatly to the general body of knowledge. DISCLOSURE The authors have no conflicts of interest to declare. REFERENCES 1. Sperber GH. Transitions in craniofacial biology: a tribute to Bernard G Sarnat. J Craniofac Surg 2012;23:124–125. 2. Janvier P. Developmental biology: led by the nose. Nature 2013;493:169–170. 3. Oisi Y, Ota KG, Kuraku S, Fujimoto S, Kuratani S. Craniofacial development of hagfishes and the evolution of vertebrates. Nature 2013;493:175–180. 4. Tijo J-H, Levan A. The chromosome number of man. Hereditas 1956;42:1–6. 5. Slavkin HC. Charles Darwin and the foundations of clinical genetics in dentistry. J Am Dent Assoc 1997;128:241–245. 6. Buonocore MG. A simple method of increasing the adhesion of acrylic filling materials to enamel surfaces. J Dent Res 1955;34:849–853. 7. Cueto EI, Buonocore MG. Sealing of pits and fissures with an adhesive resin: its use in caries prevention. J Am Dent Assoc 1967;75:121–128. 8. Gutmann JL. The evolution of America’s scientific advancements in dentistry in the past 150 years. J Am Dent Assoc 2009;140:S8–S15. 9. Sperber GH. The genetics of odontogenesis: implications in dental anthropology and palaeo-odontology. Dent Anthropol 2004;17:1–7. 10. Liu F, van der Lijn F, Schurmann C, et al. A genome-wide association study identifies five loci influencing facial morphology in Europeans. PLoS Genet 2012;8:e1002932. 11. Wright JT, Hart TC. The genome projects: implications for dental practice and education. J Dent Educ 2002;66:659–671. 12. van Gijn DR, Tucker AS, Cobourne MT. Craniofacial development: current concepts in the molecular basis of Treacher Collins syndrome. Br J Oral Maxillofac Surg 2013;51:384– 388. 13. Stuppia L, Capogreco M, Marzo G, et al. Genetics of syndromic and nonsyndromic cleft lip and palate. J Craniofac Surg 2011;22:1722–1726. © 2014 Australian Dental Association
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Address for correspondence: Professor Geoffrey Sperber Faculty of Medicine and Dentistry 5383 Edmonton Clinic Health Academy University of Alberta 11405 – 87th Avenue NW Edmonton, AB T6G 1C9 Canada Email: [email protected] © 2014 Australian Dental Association
