Fluctuating dental asymmetry in rabbits with familial nonsyndromic coronal suture synostosis

Auteurs-es

  • Mae A. Hyre Oro-Maxillo-Facial Surgeon, Private Practice, Charleston WV
  • Seth M. Weinberg University of Pittsburgh, School of Dental Medicine
  • Gregory M. Cooper University of Pittsburgh, Department of Plastic Surgery
  • James Gilbert University of Pittsburgh, Department of Plastic Surgery
  • Michael I. Siegel University of Pittsburgh, School of Dental Medicine
  • Mark P. Mooney University of Pittsburgh, School of Dental Medicine

DOI :

https://doi.org/10.5195/d3000.2017.78

Mots-clés :

Fluctuating dental asymmetry, craniosynostosis, developmental instability, rabbits

Résumé

Fluctuating dental asymmetry has been linked to conditions of unstable pre- and peri-natal development. Familial, nonsyndromic craniosynostosis disrupts early craniofacial development through localized excessive calvarial ossification leading to the premature fusion of the calvarial sutures. Such abnormal gene expression may also produce systemic stress resulting in developmental instability, thereby affecting normal trait symmetry. The present study was designed to test this hypothesis by examining fluctuating dental asymmetry in an inbred strain of rabbits with familial, nonsyndromic coronal craniosynostosis.  The mesiodistal (MD) and buccolingual (BL) dimensions of the right and left maxillary first molars were measured in four groups of New Zealand white rabbits (N=176; n=40 with early-onset synostosis, n=65 with delayed-onset synostosis, n=46 in-colony, phenotypically normal rabbits, and n=25 wild-type normal controls). For each variable, raw signed asymmetry was calculated (left-right) and tested for assumptions of fluctuating asymmetry (i.e., normality and non-directionality). Any group that did not meet these assumptions was excluded from further analysis. Using a standard size-adjusted, fluctuating asymmetry index, mean fluctuating asymmetry was calculated and compared across groups with non-parametric statistics.  For the MD dimension, no significant (p > 0.05) group differences in mean fluctuating asymmetry were observed among groups. In contrast, rabbits with early-onset synostosis had significantly (p < 0.05) more fluctuating asymmetry in the BL dimension compared to wild-type controls.  Results demonstrate increased fluctuating dental asymmetry in rabbits with nonsyndromic, early-onset coronal suture synostosis and suggest that the molecular events producing suture synostosis locally may have also have systemic effects. Knowledge of these systemic interactions may contribute to a fuller understanding of the phenotypic spectrum observed in individuals with nonsyndromic craniosynostosis.

Bibliographies de l'auteur-e

Mae A. Hyre, Oro-Maxillo-Facial Surgeon, Private Practice, Charleston WV

 

 

Gregory M. Cooper, University of Pittsburgh, Department of Plastic Surgery

 


James Gilbert, University of Pittsburgh, Department of Plastic Surgery

 


Références

References

Cohen MM (2000) History, terminology, and Classifica-tion of Craniosynostosis. In: Cohen MM, MacLean RE, editors. Cranio-synostosis: Diagnosis, Eval-uation, and Management. New York: Oxford Universi-ty Press. Pp. 1-20.

Opperman LA, Ogle RC (2002) Molecular studies of craniosynostosis: factors affecting cranial suture morphogenesis and paten-cy. In: Mooney MP, Siegel MI, editors. Understanding Craniofacial Anomalies: the Etiopathogenesis of Crani-osynostoses and Facial Clefting. New York: Wiley-Liss, Inc. 497-517 p.

Mooney MP, Cray JJ Jr, Losee JE, Moursi AM, Siegel MI, Cooper GM (2012) The development of molecular therapies for craniosynostosis. In: Schachner P, editor. Pro-ceedings of the 9th Euro-pean Craniofacial Con-gress. Bologna Italy: Mon-duzzi Editore. Pp. 9-18.

Genetics of craniosynosto-sis: genes, syndromes, mu-tations and genotype-phenotype correlations. Passos-Bueno MR, Serti Eacute AEAL, Jehee FS, Fanganiello R, Yeh E. Front Oral Biol. 2008;12:107–43. PMID: 18391498.

Prevalence and complica-tions of single-gene and chromosomal disorders in craniosynostosis. Wilkie AOM, Byren JC, Hurst JA, Jayamohan J, Johnson D, Knight SJL, Lester T, Rich-ards PG, Twigg SRF, Wall SA. Pediatr. 2010; 126: e391–400. PMID: 20643727.

Prevalence of Pro250Arg mutation of fibroblast growth factor receptor 3 in coronal synostosis. Molo-ney DM, Wall SA, Ashworth GJ, Oldridge M, Glass IA, Francomano CA, Muenke M, Wilkie AOM. Lancet. 1997;349:1059-62. PMID: 9107244.

Craniosynostosis associat-ed with FGFR3 Pro250Arg mutation results in a range of clinical presentations in-cluding unisutural sporadic craniosynostosis. Reardon W, Wilkes D, Rutland P, Pulleyn LJ, Malcolm S, Dean JCS, Evans RD, Jones BM, Hayward R, Hall CM. J Med Genet. 1997;34:632-6. PMID: 9279753.

Identification of the first genetic cause for isolated unilateral coronal synosto-sis: a unique mutation in the fibroblast growth fac-tor receptor 3 (FGFR3). Gripp KW, McDonald-McGinn DM, Gaudenz K, Whitaker LA, Bartlett SP, Glat PM, Cassileth LB, May-ro R, Zackai EH, Muenke M. J Pediatr. 1998;132:714-6. PMID: 9580776.

Genetic study of nonsyn-dromic coronal cranio-synostosis. Lajeunie E, Le Merrer M, Bonaiti-Pellie C, Marchac D, Renier D. Am J Med Genet. 1995;55:500-4. PMID: 7762595.

Genetic study of scapho-cephaly. Lajeunie E, Le Merrer M, Bonaiti-Pellie C, Marchac D, Renier Am J Med Genet. 1996;62:282-5. PMID: 8882788.

From genotype to pheno-type: the differential ex-pression of FGF, FGFR, and TGFβ genes characterizes human cranioskeletal de-velopment and reflects clinical presentation in FGFR syndromes. Britto JA, Evans RD, Hayward RD, Jones BM. Plast Reconstr Surg. 2001;108:2026-39. PMID: 11743396.

Crouzonodermoskeletal syndrome. Jeftha A, Ste-phen L, Morkel JA, Beigh-ton P. J Clin Pediatr Dent. 2004;28:173-6. PMID: 14969379.

A study of fluctuating asymmetry. Van Valen L. Evol. 1962;16:125-142.

Genetical control of stabil-ity in development. Mather K. Heredity. 1953;7:297-336.

Canalisation of develop-ment and the inheritance of acquired characters. Waddington CH. Nature. 1942;150:563-5.

Waddington CH. (1957)The Strategy of the Genes. London: Allen and Unwin. 115 p.

Fluctuating asymmetry: A biological monitor of envi-ronmental and genomic stress. Parsons PA. Heredi-ty. 1992;68:361-364. PMID: 1563968.

Møller AP, Swaddle JP (1990) Asymmetry, Devel-opmental Instability, and Evolution. Oxford: Oxford University Press. 56 p.

Markow TA (1994) Devel-opmental Instability: its Or-igins and Evolutionary Im-plications. Dordrecht: Kluwer Academic Publish-ers. 102 p.

Polak M (2003) Develop-mental Instability: Causes and Consequences. Oxford: Oxford University Press. 87 p.

Developmental stability, disease and medicine. Thornhill R, Møller AP. Biol Rev Camb Philos Soc. 1997;72:497-548. PMID: 9375532.

Congenital cleft lip and fluctuating dermatoglyphic asymmetry. Woolf CM, Gianas AD. Am J Hum Genet. 1976;28:400-3. PMID: 941907.

A study of fluctuating asymmetry in the sibs and parents of cleft lip proposi-ti. Woolf CM, Gianas AD. Am J Hum Genet. 1977;29:503-7. PMID: 900124.

Human tooth-size asym-metry in cleft lip with or without cleft palate. Sofaer JA. Arch Oral Biol. 1979;24:141-6. PMID: 299139.

Cleft lip with or without cleft palate and dermato-glyphic asymmetry: evalua-tion of a Chinese popula-tion. Neiswanger K, Cooper ME, Weinberg SM, Flod-man P, Keglovitz AB, Liu Y, Hu DN, Melnick M, Spence MA, Marazita ML Orthod Craniofacial Res. 2002;5:140-6. PMID: 12194662

Down syndrome—a disrup-tion of homeostasis. Shapiro B. Am J Med Genet. 1983;14:241–269. PMID: 6220605.

Fluctuating dental asym-metry: a measure of devel-opmental instability in Down syndrome. Barden HS. Am J Phys Anthropol. 1980;52:169-173. PMID: 6445164.

Crown size asymmetry in males with fra (X) or Mar-tin-Bell syndrome. Peretz B, Ever-Hadani P, Casamassimo P, Eidelman E, Shellhart C, Hagerman R. Am J Med Genet. 1988;30:185-190. PMID: 2972204.

Decreased developmental stability as assessed by fluctuating asymmetry of morphometric traits in pre-term infants. Livshits G, Davidi L, Kobyliansky E, Ben-Amitai D, Levi Y, Mer-lob P. Am J Med Genet. 1988;29:793–805. PMID: 3400724.

Left-right asymmetries in embryonic development: a comprehensive review. Levin M. Mech Dev. 2005; 122:3–25. PMID: 15582774.

Attention-deficit hyperac-tivity disorder (AD/HD) and fluctuating asymmetry in a college sample: an explora-tory study. Burton C, Ste-venson JC, Williams DC, Everson ER, Trimble JE. Am J Hum Biol. 2003;15:601-19. PMID: 12953172.

Anthropometric asym-metry in normal and men-tally retarded males. Ma-lina RM, Buschang PH. Ann Hum Biol. 1984;11:515-31. PMID: 6524867.

Fluctuating asymmetry and vertebral malformation: a study of palmar dermato-glyphics in congenital spi-nal deformities Goldberg CJ, Fogarty EE, Moore DP, Dowling FE. Spine. 1997;22:775-9. PMID: 9106319.

Psychological perspective on human developmental stability and fluctuating asymmetry: sources, appli-cations and implications. Kowner R. Brit J Psychol. 2001;92:447-69. PMID: 11802884.

Cohen MM. Sutural pa-thology (2000) In: Cohen MM, MacLean RE, editors. Craniosynostosis: Diagno-sis, Evaluation, and Man-agement. New York: Ox-ford University Press. Pp. 51-68.

Transforming growth fac-tor-β isoform expression in the perisutural tissues of craniosynostotic rabbits. Poisson E, Sciote JJ, Koepsel R, Cooper GM, Opperman LA, Mooney MP. Cleft Palate Craniofac J. 2004;41:392-402. PMID: 15222795.

Coronal suture pathology and synostotic progression in rabbits with congenital craniostenosis. Mooney MP, Smith TD, Langdon HL, Burrows AM, Stone CE, Losken HW, Siegel MI. Cleft Palate-Craniofac J. 1996; 33: 369-78. PMID: 8891367.

Fluctuating asymmetry and developmental instability in sagittal craniosynostosis. De Leon VB, Richtsmeier JT. Cleft Palate-Craniofac J. 2009; 46: 187–96. PMID: 19254065.

Genotype, phenotype, and developmental biology of molar tooth characters. Jernvall J, Jung HS. Am J Phys Anthropol. 2000;31(Suppl):171-190. PMID: 11123840.

Harris EF (2002) Dental de-velopment and anomalies in craniosynostoses and fa-cial clefting. In: Mooney MP, Siegel MI, editors. Un-derstanding Craniofacial Anomalies: the Etiopatho-genesis of Craniosynosto-ses and Facial Clefting. New York: Wiley-Liss, Inc. Pp. 425-467.

Craniosynostosis with au-tosomal dominant trans-mission in New Zealand White rabbits. Mooney MP, Aston CE, Siegel MI, Losken HW, Smith TD, Bur-rows AM, Wenger SL, Ca-ruso K, Siegel B, Ferrell RE. J Craniofac Genet Dev Biol. 1996;16:52-63. PMID: 8675615.

Development of a strain of rabbits with congenital simple, nonsyndromic cor-onal suture synostosis. Part II: Somatic and craniofacial growth patterns. Mooney MP, Losken HW, Siegel MI, Lalikos JF, Losken A, Bur-rows A, Smith TD. Cleft Palate Craniofac J. 1994;31:8-16. PMID: 8130248.

Development of a strain of rabbits with congenital simple, nonsyndromic cor-onal suture synostosis. Part I: Breeding demographics, inheritance pattern, and craniofacial anomalies. Mooney MP, Losken HW, Siegel MI, Lalikos JF, Losken A, Smith TD, Bur-rows A. Cleft Palate Crani-ofac J. 1994;31:1-7. PMID: 8130237.

A rabbit model of human familial, nonsyndromic unicoronal suture synosto-sis. Part I: Synostotic onset, pathology, and sutural growth patterns. Mooney MP, Siegel MI, Burrows AM, Smith TD, Losken HW, Dechant J, Cooper G, Kapucu MR. Childs Nerv Syst. 1998;14:236-246. PMID: 9694335.

Mooney MP, Siegel MI, Opperman LA (2002) Ani-mal models of cranio-synostosis: experimental, congenital, and transgenic. In: Mooney MP, Siegel MI, editors. Understanding Craniofacial Anomalies: the Etiopathogenesis of Crani-osynostoses and Facial Clefting. New York: Wiley-Liss, Inc. Pp.251-272.

Genetic Homozygosity and Phenotypic Variability in Craniosynostotic Rabbits. Gilbert J, Cray JJ Jr, Kriethen A, Marazita ML, Cooper GM, Losee JE, Siegel MI, Mooney MP. Cleft Palate Craniofac J. 2017 Jan;54(1):94-9. PMID: 26882022.

Craniosynostosis: novel in-sights into pathogenesis and treatment. Wilkie AOM, Wall SA Curr Opin Neurol. 1996;9:146-52. PMID: 8782984.

Kieser JA (1990) Human Adult Odontometrics. Cambridge: Cambridge University Press. 237 p.

Palmer AR(1994) Fluctuat-ing asymmetry analyses: a primer. In: Markow TA, ed-itor. Developmental Insta-bility: Its Origins and Evolu-tionary Implications. Dor-drecht: Kluwer Academic Publishers. Pp. 335-64.

Fluctuating asymmetry: measurement, analysis, patterns. Palmer AR, Stro-beck C. Annu Rev Ecol Syst. 1986;17:391-421.

Interobserver error in a large scale anthropometric survey. Gordon CC, Bradtmiller B. Am J Hum Biol. 1992;4:253-63. PMID: 28524349.

The oral manifestations of Apert syndrome. Kreiborg S, Cohen MM. J Craniofac Genet Dev Biol. 1992;12:41-48. PMID: 1572940.

Dental development in Apert syndrome. Kaloust S, Kazuhiro I, Vargervik K. Cleft Palate - Craniofac J. 1997;34:117-21. PMID: 9138505.

Oral manifestations of Crouzon's disease. Kelln EC, Chaudhry AP, Gorlin FJ.Oral Surg Oral Med Oral Pathol. 1960;13:1245-8. PMID: 13752352.

Partial anodontia of both the deciduous and perma-nent dentitions in a case of Crouzon's disease. Stein GM, Wahl H. Oral Surg Oral Med Oral Pathol. 1969;28:808-12. PMID: 5260651.

Natal molars in Pfeiffer syndrome type 3: a case report. Alvarez MP, Crespi PV, Shanske AL. J Clin Pedi-atr Dent. 1993;18:21-4. PMID: 8110608.

Pfeiffer syndrome: report of a family and review of the literature. Naveh Y, Friedman A. J Med Genet. 1976;13:277-80. PMID: 957376.

Evolution and develop-ment of teeth. McCollum MA, Sharpe PT. J Anat. 2001;199:153-9. PMID: 11385628.

Genetic covariance struc-ture of incisor crown size in twins. Dempsey PJ, Town-send GC, Martin NG, Neale MC. J Dent Res. 1995;74:1389-98. PMID: 7560390.

Genetic analysis of decidu-ous tooth size in Australian twins. Hughes T, Dempsey P, Richards L, Townsend G. Arch Oral Biol. 2000;45:997-1004. PMID: 11000386.

Genetic and environmental contributions to variation in human tooth size. Dempsey P, Townsend GC. Heredity. 2001;86:685-93. PMID: 11595049.

The effect of environmen-tal factors on tooth devel-opment: an experimental investigation. Riesenfeld A. Acta Anat (Basel). 1970;77:188-215. PMID: 5508460.

Normal development of the jaws and teeth in pigs, and the delay and maloc-clusion produced by calorie deficiencies. Tonge CH, McCance RA. J Anat. 1973;115:1-22. PMID: 4199500.

Fluctuating dental asym-metry and audiogenic stress. Siegel MI, Smookler HH. Growth. 1973;37:35-9. PMID: 4700428.

Heat stress, fluctuating asymmetry and prenatal selection in the laboratory rat. Siegel MI, Doyle WJ, Kelley C. Am J Phys An-thropol. 1977;46:121-6. PMID: 556888.

On the meaning of in-creased fluctuating dental asymmetry: a cross popu-lational study. Doyle WJ, Johnston O. Am J Phys An-thropol. 1977;46:127-34. PMID: 319679.

The effects of cold stress on fluctuating asymmetry in the dentition of the mouse. Siegel MI, Doyle WJ. J Exp Zool. 1975;193:385-9. PMID: 1176912.

Fluctuating asymmetry in molar dimensions and dis-crete morphological traits in Pima Indians. Noss JF, Scott GR, Potter RHY, Dahlberg AA. Am J Phys Anthropol. 1983;61:437-45. PMID: 6624887.

Fluctuating dental asym-metry as a measure of odontologic canalization in man. Kieser JA, Groeneveld HT, Preston CS. Am J Phys Anthropol. 1986;71:437-44. PMID: 3812659.

Comparison of fluctuating asymmetry level between normal and pathological specimens from modern Thai skeletal group. Jung H, Woo EJ, Von Cramon-Taubadel N. Amer J Phys Anthropol. 2017; 162 (S64): 136.

Prenatal stress and in-creased fluctuating asym-metry in the parietal bones of neonatal rats. Mooney MP, Siegel MI, Gest TR. Am J Phys Anthropol. 1985;68:131-4. PMID: 4061598.

Unilateral and bilateral expression of a quantita-tive trait: Asymmetry and symmetry in coronal crani-osynostosis. Heuzé Y, Mar-tínez-Abadías N, Stella JM., Senders CW, Boyadjiev SA, Lo L-J, Richtsmeier JT. J Exp Zool B Mol Dev Evol. 2012; 318: 109–122. PMID: 22532473.

Téléchargements

Publié-e

2017-10-10

Numéro

Rubrique

Development of Craniofacial Structures