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Romanian Journal of Oral Rehabilitation Vol. 15, No.1 January-March 2023 199 CRANIOFACIAL ASPECTS IN TURNER SINDROME Dana Maria Albulescu 1 , Preda Smaranda Adelina2 , Alexandru Dragos Ovidiu3 , Mihaela Jana Tuculina2, Ruxandra Voinea-Georgescu4, Bugala Narcis Mihaita5 1 Faculty of Medicine, University of Medicine and Pharmacy Department of Human Anatomy, Craiova, Romania 2 Faculty of Dental Medicine, University of Medicine and Pharmacy of Craiova Department of Odontology, Craiova, Romania 3 Faculty of Medicine, University of Medicine and Pharmacy of Craiova Department of Medical Informatics and Biostatistics, Romania 4 University Titu Maiorescu of Bucharest, Faculty of Dental Medicine, 67A Gheorghe Petrascu Str., 031593, Bucharest, Romania 5 Faculty of Medicine, University of Medicine and Pharmacy of Craiova Department of Medical Informatics and Biostatistics, Romania * Corresponding Author : Ruxandra Voinea Georgescu - ruxi0372@yahoo.com Contribution Note: All the authors equally contributed to the drawing up of the present paper. Abstract: Our study shows craniofacial morphological abnormalities in Turner syndrome by analyzing linear and angular variables calculated on cephalometry. Craniofacial aberrant aspects are found in reduction of the posterior base of the skull, mandibular and maxillary shortening, mandibular and maxillary retrusion. The values obtained by us are within the specific profile of this pathology, also reported to the specialized studies in the field, even if we were limited by the small number of cases, but we can affirm the importance of cephalometry in highlighting the craniofacial morphological features in Turner syndrome. Keywords: cephalometry, Turner syndrome 1. INTRODUCTION Craniofacial morphology is influenced by various circulating hormones [1], however, growth hormone is particularly important for normal craniofacial development [2,3]. In addition to growth hormone, the effects of Turner syndrome on craniofacial morphology are also known, with studies revealing these changes. Craniofacial morphometry studies in girls with Turner syndrome show different changes in certain anthropometric variables, in the sense of reduced values compared to normal developmental norms of children at different stages of childhood and adolescence [4,5,6]. This paper aims to analyze some cephalometric variables in girls with Turner syndrome, to compare the results with the normal mean values from existing studies and to compare them with the mean values of the groups with this condition described in the literature.[7,8,9] Romanian Journal of Oral Rehabilitation Vol. 15, No.1 January-March 2023 200 2. MATERIAL AND METHOD The study group was performed on 11 patients known to have Turner syndrome. All children were selected from the endocrinology department of SCJU, data on general characteristics were collected and processed from the medical records of these patients. In addition, we obtained informed consent from the legal representatives of all subjects. Measurements were made manually by a single investigator. Cephalometry was performed using a Carestream CS 8100SC equipment, the examination position being the standard one, with perpendicular orientation of the X-ray beam on the sagittal plane of the patient. The anthropometric points identified on the cephalometric images taken in the study were (fig no.1) Figure 1. Linear variables on cephalometry - Nasion (n) - the most anterior point, corresponding to the anterior nasal seam - Point A - the last point of the frontal contour of the maxilla - Point B - the last point of the anterior contour of the mandibular body, on the midline - Sella (s) - the rearmost opposite point of Romanian Journal of Oral Rehabilitation Vol. 15, No.1 January-March 2023 201 the quadrilateral blade - Basal (ba) - the most important point of the foramen magnum - Gnathion (gn) - lower point of the mental union outline - Gonion (go) - intersection of the bisector of the angle formed by the tangent to the lower edge of the jaw and the tangent to the posterior edge of the corner - Below the spine (ss) - the most concave point of the chin - Spine (sp) - premaxillary point - Posterior nasal spine (pns) - Posterior border of maxilla - Maxilla (sm) - the most concave point of the mandible The angles measured in our study were (fig. no 2): Figure 2. Angular variables on cephalometry - SNA - sella-nasion angle at point A (subspinals) - SNB - sella-nasion angle at point B (supramental) Romanian Journal of Oral Rehabilitation Vol. 15, No.1 January-March 2023 202 - ANB - angle from point A to point B - S-N-Ss - prognathic angle of maxilla - S-N-Sm - mandible prognathic angle - has the same meaning as SNA and SNB angles, - Interincisive angle - between the axes of the maxillary and mandibular incisors - IMPA angle - between the mandibular incisor axis and the plane of the mandible - FMA angle - between the Frankfurt horizontal plane and the mandibular plane - FMIA angle - between the Frankfurt plane and the mandibular incisor axis 3. STATISTICAL ANALYSIS 3.1. Sample Calculation Microsoft Excel program (Microsoft Corp., Redmond, WA, USA), XLSTAT suite for MS Excel (Addinsoft SARL, Paris, France) and IBM Statistical Package for the Social Sciences (SPSS) Statistics 20.0- Program (IBM Corporation, Armonk, NY, USA) were used to process the cephalometrically measured parameter values. The evaluated parameters of the subjects included in the study were saved in Excel type files. 3.2. Statistical Tests Secondary data processing, calculation of basic statistical parameters, mean and SD of their proportions, coefficient of variation, and their graphing in Excel using Pivot Tables, Function-Statistics commands, Charts and Data Analysis modules Executed. Normality tests (Shapiro-Wilks and Anderson-Darling) and Student's t-tests and analysis of variance (ANOVA) tests were performed on the data using XLSTAT module commands. 4. RESULTS For subjects with Turner syndrome the results of the cephalometric measurements are listed in the following tables (Tables 1): Table 1. Average and SD values of cephalometric measurements in the Turner syndrome group Variable Average DS n-s 62.34 2.37 s-ba 38.24 3.67 n-ba 86.23 2.56 ss-ba 73.82 2.47 sp-gn 52.32 4.68 pm-sp 44.67 3.56 s-pm 42.82 3.64 pm-ba 37.16 4.82 pm-ss 41.37 4.38 gn-go 62.34 3.27 Romanian Journal of Oral Rehabilitation Vol. 15, No.1 January-March 2023 203 These linear variables represent anterior skull base (n-s), posterior skull base (s-ba), total skull base (n-ba), maxillary prognathism linear measure (ss-ba), anterior face length, lower segmental (sp-gn), maxilla length (pm- ss), mandible length (gn-go), maxillary prognathism linear measure (pm-ba); upper posterior face height(s-pm). The values of the measured angles are given in the following table (table 2). Table 2. Mean values of angles and standard deviation in the Turner syndrome group Variable Average DS SNA˚ 77.58 1.47 SNB˚ 77.62 3.28 ANB˚ 3.72 1.75 ML-NL˚ 22.84 4.26 s-n-ss˚ 76.87 2.67 s-n-sm˚ 76.25 3.23 Interincisal angle 122.3 3.56 IMPA 89.7 1.47 FMA 24.7 2.82 FMIA 73. 2 3.27 We also calculated correlations between different cephalometric variables and between age and cephalometric variables. (table 3, table 4) Table 3. Correlation coefficients between cephalometric variables in the Turner syndrome group s-ba n-ba n-s gn-go ss-ba 0.356 0.697 0.434 0.136 s-n-sm -0.017 -0.567 -0.635 0.125 Table 4. Correlation between age and cephalometricvariables in the Turner syndrome Romanian Journal of Oral Rehabilitation Vol. 15, No.1 January-March 2023 204 group n-s s-ba n-ba pns-ba ss-ba pm-sp pns-ss s-n-ss s-n-sm gn-go age 0.114 0. 712 0.683 0.542 0.592 -0.116 0.018 0.032 -0.317 0.756 5. DISCUSSIONS Analysis of correlations between different linear variables revealed a highly significant correlation between total skull base and linear measures of maxillary protrusion, and with respect to correlation with age, mandibular length and total skull. There is a very significant correlation between base.[10] In terms of cephalometric measurements, we can analyze skull base, lower segment face height, total face height, maxillary length, mandibular length and maxillary and mandibular prognathism angles. As reference values for the cephalometric variables, we measured we used the Dumancic and Funatsu study [4,5] providing information on normal values by sex and age for certain cephalometric measurements.[11] Table no 5. Normal values of cephalometric variables according to Dumancic and Funatsu studies Variable Normal values Dumancic Study Funatsu Study guys girls n-s(mm) 63.74 67.5 64.9 n-ba(mm) 94.35 s-ba(mm) 39.67 ss-ba(mm) 84.01 sp-gn(mm) 57.88 63.9 63.3 n-sp(mm) 47.87 pm-sp(mm) 48.20 s-pm(mm) 42.31 pm-ba(mm) 39.84 Romanian Journal of Oral Rehabilitation Vol. 15, No.1 January-March 2023 205 pm-ss(mm) 44.27 44.8 43.9 gn-go(mm) 65.24 74.7 72.4 ML-NL˚ 21.32 s-n-ss˚ 80.94 s-n-sm˚ 79.37 In the Turner syndrome patient group, we observe from the analysis of linear variables a reduction in the value of the anterior skull base compared to normal values [4], but also a reduction of the posterior skull base [12,13]. These skull base changes are also found in other studies that also note reduction of the posterior skull base [14,15]. Reduction of the posterior cranial base influences the maxillo-mandibular skeletal relationships that are affected in this pathology [16,17]. Mandible length has a reduced value in comparisons with normal values, but slightly higher than the reported average of 60.7mm [5] . Although the height of the anterior surface of the upper segment is normal in the Turner syndrome group, a decrease in the anterior surface of the lower segment was observed, with a mean value of 52.32 mm for the group compared with normal values. (57.88 mm according to Dumancic's study, 63.3 mm according to Funatsu's study). The height of the posterior surface of the upper segment shows a mean value of 42.82 mm in our group, with minimal reduction of this linear variable in the group of patients with Turner syndrome compared to the normal value (42.31 mm). Regarding the maxillomandibular relationship we also measured the ML-NL angle with a value of 22.84o this value being higher than the average of 21.32o [4] and indicates retrognathia of the maxilla associated with posterior rotation of the mandible. Also, the value obtained by us is comparable with the mean value related to the maxillomandibular relationship in the Turner syndrome group according to Dumancic analysis [5]. The prognathic angle of the mandible and maxilla (SNB and SNA) show reduced values in our group compared to standardized normal values, i.e., SNB 80° ± 2 SNA 82°±2, according to Steiner analysis [8,9] The use of cephalometrics as an aid to planning and assessing [18,19,20] and demonstrates retrognathia of the mandible and maxilla. The ANB angle shows a higher average value than the normal value, according to the Steiner analysis, which indicates clockwise rotation of the mandible and maxilla. Also concerning the prognathic angles of the mandible and maxilla, we measured the s-n-sm angle with a mean value of 76.25°, reduced compared to the standardized normal value in the Dumancic study (79.37°) and increased by 2° compared to the Turner syndrome group in the Romanian Journal of Oral Rehabilitation Vol. 15, No.1 January-March 2023 206 Dumancic study. The s-n-ss angle, which indicates the angle of prognathia of the maxilla, also shows a mean value of 76.87°, also reduced compared to the standardized normal value and equal to the mean value of the Turner syndrome group in the Dumancic study. IMPA angle as analyzed by Tweed Greenstein [16,21] shows an approximately normal mean value (890) observed in the Turner syndrome group, which means an approximately normal mandibular incisor position. Considering that this angle is also associated with balance and harmony on the front of the lower segment, we can conclude that the Turner syndrome group exhibits a balanced and harmonious face. For the FMA angle, the mean values of our group are close to normal (24.70versus 250) demonstrating a discrete closed occlusion syndrome. The profile of the soft parts is given by the FMIA angle values higher than normal in the Turner syndrome group (73.20 versus 650). The interincisal angle in our group has a mean value of 122.3°, about 13° lower than the normal mean value [22], indicating an increase in incisor proclination. In fact, craniofacial morphological features in Turner syndrome include reduction of the posterior skull base, retrognathization of the mandible and maxilla, posterior rotation of the mandible and maxilla, and reduction of mandible and maxilla length. These aspects are also evident in our study even though we were limited by the small number of cases, but we can affirm the importance of cephalometry in highlighting craniofacial morphological features in Turner syndrome.[23] 6. CONCLUSIONS 1. Cephalometric studies show the presence of craniofacial abnormalities in the reduction of the posterior base of the skull, shortening of the mandible and maxilla, and recession of the mandible and maxilla. 2. Retrognathia of the mandible and maxilla is best evidenced by the SNA and SNB angle values, which are the basis for the analysis of mandible-maxillary relationships, easily calculated on the cephalometric image. 3. The ANB0 angle, which indicates the relationship between the maxilla and mandible, is lower than the normal value. 4. The interincisal angle shows low values with normal values, confirming the presence of Class I or Class II, Division 1 malocclusions. 5. Recognizing and calculating these cephalometric variables is not only the starting point for orthodontic treatment of patients with Turner syndrome, but also a way to monitor and track treatment progress over time. Funding: This article is supported by internal competition no. 26/1107/1 din 07.11.2022 entitled ”Morphological anomalies of the cephalic extremity in children in endocrine diseases” on behalf of University of Medicine and Pharmacy of Craiova, Romania. The Article Processing Charges are funded by the University of Medicine and Pharmacy of Craiova, Romania. Informed Consent Statement: The authors obtained from the patient the written informed consent for patient information and images to be published. Romanian Journal of Oral Rehabilitation Vol. 15, No.1 January-March 2023 207 Acknowledgments: none Conflicts of Interest: The authors declare no conflict of interest. References 1. Vucic,S.; Korevaar, T.I.M.; Dhamo, B.; Jaddoe, V.W.V.; Peeters, R.P.; Wolvius, E.B.; Ongkosuwito, E.M.. Thyroid Function during Early Life and Dental Development. J. Dent Res. 2017, Aug;96(9):1020-1026. 2. Partyka, M.; Chałas, R.; Dunin- Wilczyńska, I.; Drohomyretska, M.; Klatka M. Influence of growth hormone therapy on selected dental and skeletal system parameters. Annals of Agricultural and Environmental Medicine. 2018, Vol 25, No 1, 60–65. 3. Chesnokova V. The Multiple Faces of theGH/IGF Axis. Cells. 2022 Jan 10;11(2):217. doi: 10.3390/cells11020217. PMID: 35053333; PMCID: PMC8773948. 4. Funatsu, M.; Koshi, S.; Mitanic, H. Effects of Growth Hormone on Craniofacial Growth. Angle Orthodontist. 2006, 76; 6:970-976. 5. Dumancic, J.; Kaic, Z.; Lapter Varga, M.; Lauc, T.; Dumic, M.; Anic Milosevic, S.; Brkic, H. Characteristics of the craniofacial complex in Turner syndrome. Archives of oral biology. 2010, 55; 81–88. 6. Tartaglia N, Howell S, Davis S, Kowal K, Tanda T, Brown M, Boada C, Alston A, Crawford L, Thompson T, van Rijn S, Wilson R, Janusz J, Ross J. Early neurodevelopmental and medical profile in children with sex chromosome trisomies: Background for the prospective eXtraordinarY babies study to identify early risk factors and targets for intervention. Am J Med Genet C Semin Med Genet. 2020 Jun;184(2):428-443. doi: 10.1002/ajmg.c.31807. Epub 2020 Jun 7. PMID: 32506668; PMCID: PMC7413625. 7. Kim SE, Park SH, Han K, Cho WK, Suh BK, Park YG. Population Prevalence, Cancer Risk, and Mortality Risk of Turner Syndrome in South Korean Women Based on National Health Insurance Service Data. Yonsei Med J. 2022 Nov;63(11):991-998. doi: 10.3349/ymj.2022.0143. PMID: 36303307; PMCID: PMC9629904. 8. Thompson T, Davis S, Janusz J, Frith E, Pyle L, Howell S, Boada R, Wilson R, Tartaglia N. Supporting students with sex chromosome aneuploidies in educational settings: Results of a nationwide survey. J Sch Psychol. 2022 Aug;93:28-40. doi: 10.1016/j.jsp.2022.06.002. Epub 2022 Jun 28. PMID: 35934449; PMCID: PMC9360991. 9. Thompson T, Howell S, Davis S, Wilson R, Janusz J, Boada R, Pyle L, Tartaglia N. Current survey of early childhood intervention services in infants and young children with sex chromosome aneuploidies. Am J Med Genet C Semin Med Genet. 2020 Jun;184(2):414-427. doi: 10.1002/ajmg.c.31785. Epub 2020 May 25. PMID: 32449585; PMCID: PMC7413639. 10. Wójcik D, Beń-Skowronek I. Craniofacial Morphology in Children with Growth Hormone Deficiency and Turner Syndrome. Diagnostics (Basel). 2020 Feb 7;10(2):88. doi: 10.3390/diagnostics10020088. PMID: 32046211; PMCID: PMC7168196. 11. Bagattoni S, Lardani L, Vanni A, Costi T. Craniofacial and occlusal features of individuals with Turner Syndrome: A cephalometric study. J Biol Regul Homeost Agents. 2021 May-Jun;35(3 Suppl. 1):95-106. doi: 10.23812/21-3supp1-12. PMID: 34289669. 12. Poole, A.E.; Greene, I.M.; Buschang, P.H. The effect of growth hormone therapy on longitudinal growth of the oral facial structures in childen. Prog Clin Biol Res. 1982,101:499–516. 13. Sarnat, H. Comparison of dental findings in patients with isolated growth hormone deficiency treated with human growth hormone (hGH) and in untreated patients witn Laron-type dwarfism. Oral Surg. 1988 , https://www.ncbi.nlm.nih.gov/pubmed/28489513 Romanian Journal of Oral Rehabilitation Vol. 15, No.1 January-March 2023 208 66:581–586. 14. Klocke, A.; Nanda, R.S.; Kahl-Nieke, B. Role of cranial base flexure in developing sagittal jaw discrepancies. Am J Orthod Dentofacial Orthop. 2002, 122:386–391. 15. Kerr, W.J.; Adams, C.P. Cranial base and jaw relationship. Am J Phys Anthropol. 1988 , 77:213–220. 16. Rao, E.; Weiss, B.; Fukami, M.; Rump, A.; Niesler,B.; Mertz,A.; Muroya,K.; Binder, S Kirsch, M Winkelmann, G Nordsiek, U Heinrich, M H Breuning, M B Ranke, G.; Rosenthal ,A.; Ogata,T.; Rappold, G. A. Pseudoautosomal deletions encompassing a novel homeobox gene cause growth failure in idiopathic short stature and Turner syndrome. Nat Genet .1997, 16: 54–63. 17. Ross , J. L.; Scott, C. Jr; Marttila, P.; Kowal, K.; Nass, A.; Papenhausen, P.; Abboudi, J.; Osterman, L.; Kushner, H.; Carter, P.; Ezaki, M.; Elder, F.; Wei, F.; Chen, H.; Zinn, A. R. Phenotypes Associated with SHOX Deficiency. J Clin Endocrinol Metab. 2001, 86(12): p. 5674-5680. 18. Steiner, C.C. ;Cephalometrics for You and Me. American Journal of Orthodontics. 1953,39, 729- 755.http://dx.doi.org/10.1016/0002-9416(53)90082-7 19. Steiner, C.C Cephalometrics in clinical practice. Angle Orthod .1959, 29 (1): 8– 29.https://doi.org/10.1043/0003-3219(1959)0292.0.CO;2 20. Steiner, CC. The use of cephalometrics as an aid to planning and assessing orthodontic treatment. Am J Orthod .1960;46:721–35 21. Greenstein, A. V "The tweed philosophy". American Journal of Orthodontics and Oral Surgery. 1943-09- 01. 29 (9): 527–540. doi:10.1016/S0096-6347(43)90310-2 22. Downs, W. B. The role of cephalometrics in orthodontic case analysis and diagnosis. American Journal of Orthodontics. 1952, 38(3), 162-182. 23. Koffi KA, Doublier S, Ricort JM, Babajko S, Nassif A, Isaac J. The Role of GH/IGF Axis in Dento-Alveolar Complex from Development to Aging and Therapeutics: A Narrative Review. Cells. 2021 May 12;10(5):1181. doi: 10.3390/cells10051181. PMID: 34066078; PMCID: PMC8150312 https://pubmed.ncbi.nlm.nih.gov/?term=Rump+A&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Niesler+B&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Mertz+A&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Muroya+K&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Binder+G&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Kirsch+S&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Winkelmann+M&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Winkelmann+M&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Nordsiek+G&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Heinrich+U&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Breuning+MH&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Ranke+MB&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Rosenthal+A&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Ogata+T&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Rappold+GA&cauthor_id=9140395 https://pubmed.ncbi.nlm.nih.gov/?term=Ross+JL&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Scott+C+Jr&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Marttila+P&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Kowal+K&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Nass+A&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Papenhausen+P&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Abboudi+J&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Osterman+L&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Kushner+H&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Carter+P&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Ezaki+M&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Elder+F&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Wei+F&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Chen+H&cauthor_id=11739418 https://pubmed.ncbi.nlm.nih.gov/?term=Zinn+AR&cauthor_id=11739418 https://doi.org/10.1043/0003-3219(1959)029%3c0008:CICP%3e2.0.CO;2 https://en.wikipedia.org/wiki/Doi_(identifier) https://doi.org/10.1016%2FS0096-6347%2843%2990310-2