Cameriere s European formula for age estimation: A study on the children in Bosnia and Herzegovina

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1 Origial Article Cameriere s Europea formula for age estimatio: A study o the childre i Bosia ad Herzegovia Latić-Dautović, Melia 1 ; Nakaš, Eita 2 ; Jelešković, Azra 2 ; Cavrić, Jelea 3 ; Galić, Iva 4 1 Detal Departmet, The Public Istitutio Health Cetre of Sarajevo Cato, Bosia ad Herzegovia 2 Departmet of Orthodotics, School of Detal Medicie, Uiversity of Sarajevo, Bosia ad Herzegovia 3 Hery M. Goldma School of Detal Medicie Bosto, Uiversity Bosto, USA 4 School of Medicie, Uiversity of Split, Croatia ABSTRACT Itroductio: A method for age estimatio, based o measuremets of projectios of ope apices ad heights of developig permaet teeth o orthopatomograms (OPTs), was preseted by Cameriere i 2006 ad adopted Europea formula was preseted i Aim: This cross-sectioal study tested the accuracy of Cameriere s Europea formula o a sample from the City of Sarajevo, Bosia ad Herzegovia. Materials ad methods: A fial sample of 560 OPTs of 305 girls ad 255 boys aged 8 to 14 years was obtaied. The sample was collected at the Departmet of Orthodotics, School of Detal Medicie at the Uiversity of Sarajevo (SFUNSA). Detal age was compared to chroological age ad mea absolute error (MAE) was calculated. Itra-rater ad iter-rater agreemet of the evaluated variables were calculated. Results: The detal age was uderestimated whe compared to chroological age, precisely, mea uderestimatio was years i girls ad years i boys. The values of MAE were 0.62 years i girls ad 0.56 years i boys. The greatest error was foud for the 14-year old group; DA was years ad years i girls ad boys respectively. Coclusio: Our results showed that Cameriere s Europea formula might be a useful tool for age estimatio i childre from Bosia ad Herzegovia uder the age of 14 years. Latić-Dautović M, Nakaš E, Jelešković A, Cavrić J, Galić I. Cameriere s Europea formula for age estimatio: A study o the childre i Bosia ad Herzegovia ;4(2): Submitted: April 6, 2017; Revised: August 28, 2017; Published: October 15, 2017 INTRODUCTION Teeth have bee marked as a useful body system for age estimatio i youth ad elderly. 1 I childre ad adolescets, there are differet medico-legal ad foresic questios, like the age of crimial resposibility or adult age, where detal age estimatio ca help to aswer. 2-6 Accordig to the Study Group o Foresic Age Diagostics (AGFAD; 2, the examiatio of differet idepedet developmetal systems icludig teeth is combied, to icrease the accuracy of estimated age. 7 For childre ad juveiles, the radiographs of had-wrist ad the teeth are the most reliable for assessig skeletal ad detal Correspodig Author: Iva Galic School of Medicie, Uiversity of Split, Split, Croatia igalic@mefst.hr developmet Developig permaet teeth i childre are very useful for age estimatio because of the possibility to study mieralizatio of all teeth o a sigle, paoramic X-ray (OPT). 11 O the other had, mieralizatio of teeth is ot affected as is their eruptio by exteral factors, such as crowdig, retetio or early extractio of deciduous teeth, o the other had, social, ecoomic or malutritio status may affect skeletal growth Most methods of age estimatio i childre evaluated mieralizatio of specific sets of teeth, most commoly madibular. 15 Historically, maxillary teeth were ot appropriate for radiologic aalysis because of iferior appearace to madibular teeth ad superpositio with correspodig skeletal structures o aalog X-rays which is ow mostly improved ad corrected i digital radiography. Distict stages of mieralizatio were used to estimate detal mieralizatio, from the presece of a detal crypt ad first calcificatio to the fial closure of apices of the detal roots. 16 Demirjia et al. 16 itroduced the 26

2 most widely used approach for age estimatio i childre i Demirjia s method used seve teeth from oe side of the madible while full rage mieralizatio of the teeth was divided ito eight stages (A-H). Demirjia s approach, which used stages showed acceptable accuracy, especially after some methodological ad statistical adaptatio. 17,18 Cameriere et al. 19 demostrated a differet system of measurig the maturity of developig teeth. Istead of mieralizatio stages, Cameriere s method measure projectios of ope apices of developig teeth. 19 Geerally, i the Italia sample of 455 orthopatomogram (OPTs) it is proved that the chroological age is associated with the total sum of ratios of ope apices ad the legth of tooth projectio, the umber of teeth with closed apex ad geder. 19 Furthermore, exteded study o differet Europea samples from Croatia, Germay, Kosovo, Italy, Sloveia, Spai, ad the Uited Kigdom, totalig 2652 OPTs, has show that variable coutries of origi were ot statistically sigificat for the regressio formula, while geder, morphological variables secod premolar, sum of ormalized ope apices (s), umber of teeth with closed apices (N0), ad the first-order iteractio betwee s ad N0, cotributed sigificatly to the fit, ad were icluded i the liear regressio model. 20 Evaluatio of Cameriere s formulas i a differet populatio, icludig a study o Bosia- Herzegovia samples, showed good accuracy for age estimatio. This study aimed to test Cameriere s Europea formula o the sample of OPTs of childre from Bosia ad Herzegovia. MATERIALS AND METHODS This cross-sectioal study was carried out at the Departmet of Orthodotics, School of Detal Medicie at the Uiversity of Sarajevo (SFUNSA). A fial radomly selected sample of 560 OPTs (305 girls ad 255 boys), take for differet cliical idicatios durig the period betwee Jauary 2012 util July 2016, were aalyzed. Iclusio criteria for OPTs were age betwee 8 ad 14 years, a time whe most of the childre have a orthodotic examiatio for the first time, OPTs of high quality ad presece of all permaet teeth. Exclusio criteria were o record of detal ad skeletal aomalies, hypodotia of permaet teeth, age uder 8 ad over 14 years. All patiets were cliically examied ad aalyzed at SFUNSA by the first author. Oly specific variables of each patiet were recorded for this study, icludig date of birth ad OPT, geder ad idetificatio umber, without the possibility to idetify patiets. All patiets parets or guardias previously siged a agreemet ad protocol with SFUNSA that cliically collected data ad iformatio from OPTs ad other radiologic material that may be used for research without the possibility to idetify the patiet. The study was coducted by the ethical stadards laid dow i the Declaratio of Helsiki (Filad) where the World Medical Associatio (WMA) developed the Declaratio of Helsiki as a statemet of ethical priciples for medical research ivolvig huma subjects. 21 Patiets were divided ito seve age groups accordig to real age. For example, the group of 10-years-olds icludes all idividuals of ages from to Table 1 shows the distributio of OPTs accordig to age groups ad geder. Table 1. Age ad geder distributio of orthopatomograms from Bosia ad Herzegovia. Age (years) Girls Boys Total Total Cameriere s method was based o regressio aalysis of age as a depedet variable, ad ormalized measuremets of ope apices of the first seve madibular teeth o the OPT, where geder (g) ad umber of teeth with fiished maturatio of root apex (N 0 ) are importat depedet variables i calculatig DA. 19 All teeth without completed root maturatio were aalyzed, ad the distace betwee the ier side of the ope apices (A i, i=1,,5) was measured. The sum of the distaces betwee the ier sides of the two ope apices was calculated for teeth with two roots (A i, i=6, 7). Distaces of ope apices were ormalized by dividig by the tooth legth (L i, i=1,,7) to miimize the effects of differeces amog X-rays i magificatio ad agulatio. 3 Detal age was calculated accordig to the Europea formula: Age = g 1.692x x N s 0.139s x N 0 (1) where g is a variable, with g=1 for boys ad g=0 for girls, s is the sum of the ormalized widths of apices of the seve left permaet developig madibular teeth (x i = A i / L i, i = 1,..., 7), ad x 5 is the ormalized measuremet of the secod premolar. 20 Figure 1. A example of Cameriere s measuremets of madibular teeth, x i = A i /L i, i = of seve left madibular teeth. A i, i=1...5 (teeth with oe root) is the distace betwee the ier sides of the ope apex; A i, i=6, 7 teeth with two roots) is the sum of the distaces betwee the ier sides of the two ope apices; ad L i, i=1...7 is the legth of the tooth

3 Statistical aalysis Repeatability ad reproducibility of ormalized widths of ope apices or Itra-rater ad iter-rater agreemet betwee the same ad the secod observer were calculated by itra-class correlatio coefficiets. 22 Cohe Kappa score (kappa) was used to calculate the itra- ad iter-rater agreemet of some teeth with a closed apex or N 0. I total 60 radomly selected OPTs were examied two weeks after the fial examiatio of OPT samples. The real age of each child was calculated as the differece betwee detal age accordig to Cameriere s Europea formula (DA) ad chroological age (CA) or DA-CA. The Pearso correlatio coefficiet evaluated the relatioship betwee DA ad CA. Paired samples T-test was used to compare DA ad CA, where positive values of DA-CA show a overestimatio of detal age while egative values show uderestimatio. Mea absolute error (MAE) betwee DA ad CA was used to quatify the accuracy of the method because DA-CA may overestimate or uderestimate the detal age while MAE shows the error rate o matter if DA overestimates or uderestimates CA. The mea absolute error or MAE was used to quatify the performace of AD, the absolute values of the differeces betwee CA (Age i, i = 1,..., ) ad DA (Age est,i, i = 1,..., ): 1 1 MAE = i-1 E i = i-1 Age Cam,i - Age i (2) where is the umber of subjects i the sample, ad E i, (i = 1,..., ) is the absolute value of the i th residual, or the differece betwee the DA ad CA of the ith idividual: DA-CA= Age Cam,i Age i i=1,, (3) A positive value of DA-CA idicates overestimatio while a egative value idicates uderestimatio of DA to CA. 18 Kolmogorov-Smirov test was used to test the ormality of distributio of DA-CA, while Aalysis of variace (ANOVA) was used to test if geder ad age group as factors affect the variability of DA-CA. RESULTS Itra-class correlatio coefficiets for the same ad a differet observer were (95% CI, to 0.969) ad (95% CI, to 0.953) which is i almost excellet agreemet (P <0.001). Kappa for the same ad a differet observer was Pearso correlatio coefficiets were ad for girls ad boys respectively, which idicates a strog correlatio betwee detal ad chroological age. There was o statistically sigificat differece i real age betwee girls (11.66 ± 2.04 years) ad boys (11.57±2.06), (P =0.597). The mea detal ages were 11.52±1.81 years ad ± 1.99 years i girls ad boys respectively. Cameriere s Europea formula uderestimated detal age i both geders, Table 2. The greatest uderestimatio was for the last 14-years-old group. Figure 2 shows the distributio of DA-CA across age groups, boxplots show media ad iterquartile rages, while whiskers are lies extedig from the box to idicate the highest ad lowest values, excludig outliers. Table 2. A compariso of chroological age ad detal age (years) calculated usig Cameriere s Europea formula across differet age groups i Bosia-Herzegovia girls ad boys. Age groups N Geder CA ± SD DA ± SD (DA-CA) ± SD SEM L U MAE ± SD b t (df) P a Girls 8.43 ± ± ± ± (37) Boys 8.49± ± ± ± (31) Girls 9.51± ± ± ± (43) Boys 9.51± ± ± ± (39) Girls 10.54± ± ± ± (37) Boys 10.48± ± ± ± (39) Girls 11.40± ± ± ± (31) Boys 11.43± ± ± ± (29) Girls 12.44± ± ± ± (54) Boys 12.56± ± ± ± (31) Girls 13.48± ± ± ± (54) Boys 13.45± ± ± ± (38) Girls 14.59± ± ± ± (42) <0.001 Boys 14.51± ± ± ± (41) < Girls 11.66± ± ± ± (304) Boys 11.57± ± ± ± (254) Abbreviatio: CA, chroological age; DA, detal age; SD, stadard deviatio; SEM, stadard error of the mea; a paired T-test betwee DA ad CA; DA-CA differece betwee detal ad chroological age; b MAE mea absolute error betwee detal ad chroological age; L lower iterval ad U upper iterval of 95% Cofidece Iterval of DA-CA ; df, degrees of freedom. 28

4 Table 3. Summary ANOVA table to test the differece i DA-CA for geder ad age groups (depedet variable: DA-CA). Figure 2. Boxplots of the relatioship betwee chroological age ad differece betwee detal age accordig to Cameriere s Europea formula (DA) ad chroological age (CA) or (DA-CA). Source Type III Sum of Squares df Mea Square F-test p Itercept Geder Age group <0.001 Error I girls, detal age overestimates i 8, 9 ad 11-year-olds, while i 10, 12, 13 ad 14-year-olds uderestimates detal age. I boys, detal age overestimates i 8, 10, 12 ad 13-year-olds while i 9, 11 ad i 14 years uderestimates, Table 2 ad Figure 2. Kolmogorov-Smirov test for ormality showed that DA-CA variables are ormally distributed (P<0.200). ANOVA showed o statistically sigificat differece betwee girls ad boys i DA-CA (Table 3), while Boferroi post-test showed that there is a statistically sigificat differece betwee 14-year-olds ad all other age groups (P<0.05) ad 13-year-olds ad eight-yearolds (P=0.030). The values of MAE varied betwee 0.35 years i 10-year-olds to 1.05 years i 14-years-old girls ad betwee 0.38 years i 8-year olds to 0.81 i 12-year old boys, Table 2. DISCUSSION I this study, we evaluated the Cameriere Europea formula o the sample OPTs of orthodotic patiets from SFUNSA to verify the usefuless of the method i the childre from the particular regio i Bosia ad Herzegovia. Obtaied results idicate that the Europea formula is useful for age estimatio i the tested populatio. The greatest error or uderestimatio was foud i the childre of 14 years of age. Liversidge 24 poited out that at the age of 13 oly a few childre will ot have fiished maturatio of the secod molars ad they are excluded from the testig sample. The proportio of the childre with the ufiished maturatio of the secod molar visible o the OPT ad available for measuremet drastically decreases. 25 Ambarkova et al. 25 reported that first idividuals with the complete maturatio of the secod molars were at the age of 12 years, while at the 13 years of age 27 of 32 (84%) girls ad 13 of 32 (41%) boys have fiished maturatio of the secod molar. Both the particular regressio model ad proportio of idividuals with delayed maturatio may cotribute to the uderestimatio of detal age i the 14-years-old group. Further study should address this matter more extesively. Detal age was slightly uderestimated i both geders. A cohort of the DA-CA across age groups showed that i the oldest age group error is the greatest ad detal age uderestimates by over a year i girls ad over eight moths i boys. If we would exclude the last 14-year olds group from our sample from the aalysis, the mea values of DA-CA are 0.007±0.71 years ad -0.05±0.69 years ad MAE of 0.55±0.44 years ad 0.53±0.44 i girls ad boys respectively. Cameriere s Europea formula was tested i differet regios of the world. 7,18,26-30 The Europea formula was compared to Willems ad Haavikko methods o a sample of 1098 OPTs withi age rage betwee 6 ad 13 years i the previous study from Bosia ad Herzegovia, DA overestimated for 0.09 years for girls (MAE, 0.53 years) ad uderestimated by years for boys (MAE, 0.55 years), very close to our results of the same age rage. 18 Cotrary to our study i which we aalyzed digital OPTs from a sigle istitutio, Galić et al. 18 used aalog OPTs which were photographed by the digital camera. Galić et al. 18 collected samples from differet regios to represet a populatio withi the etire coutry more defiitively. Aother study o the sample from Italy, Spai, ad Croatia showed the media error of years ad years while MAE was 0.48 years ad 0.50 years i girls ad boys, respectively. 31 The most recet Colombia study by Rivera et al. 32 also reported the substatial accuracy of the Europea formula; the mea uderestimatio was years i girls (MAE, 0.57 years) ad overestimatio 0.08 years (MAE, 0.57 years). Preseted results idicate that Cameriere s Europea formula ca be a useful tool detal age estimatio i childre from Bosia ad Herzegovia. CONCLUSION Our study showed the cosistecy i the accuracy of Cameriere s Europea formula o the sample from the Cato of Sarajevo. The results showed both good accuracy ad reliability for estimatio of detal age i childre up to 14 years of age. Sigle regressio formula showed a small differece i error, both DA- CA, ad MAE. Sice the study oly had the available age rage of a particular sample of orthodotic patiets, further studies should evaluate the usefuless of the method i the youger childre. 29

5 REFERENCES 1. Schmelig A, Dettmeyer R, Rudolf E, Vieth V, Geserick G. Foresic Age Estimatio. Deutsches Arzteblatt iteratioal. 2016;113(4): Quispe Lizarbe RJ, Solís Adriazé C, Quezada-Márquez MM, Galić I, Cameriere R. Demirjia s stages ad Cameriere s third molar maturity idex to estimate legal adult age i Peruvia populatio. Leg Med (Tokyo). 2017;25: Lauc T, Nakas E, Latic-Dautovic M, Dzemidzic V, Tiro A, Rupic I, et al. Detal Age i Orthodotic Patiets with Differet Skeletal Patters. Biomed Res It. 2017;2017: Balla SB, Galic I, P K, Vai S, De Luca S, Cameriere R. Validatio of third molar maturity idex (I3M) for discrimiatio of juveile/adult status i South Idia populatio. J Foresic Leg Med. 2017;49: Djukic K, Zelic K, Milekovic P, Nedeljkovic N, Djuric M. Detal age assessmet validity of radiographic methods o Serbia childre populatio. Foresic Sci It. 2013;231(1-3):398.e Zelic K, Galic I, Nedeljkovic N, Jakovljevic A, Milosevic O, Djuric M, et al. Accuracy of Cameriere s third molar maturity idex i assessig legal adulthood o Serbia populatio. Foresic Sci It. 2016;259: De Luca S, De Giorgio S, Butti AC, Biagi R, Cigolai M, Cameriere R. Age estimatio i childre by measuremet of ope apices i tooth roots: Study of a Mexica sample. Foresic Sci It. 2012;221(1-3):155.e Greulich WW, Pyle, Pyle SI. Radiographic Atlas of Skeletal Developmet of the Had ad Wrist. Secod editio: pp. xvi Staford Uiversity Press: Staford; Oxford Uiversity Press: Lodo; º. p Schmidt S, Koch B, Schulz R, Reisiger W, Schmelig A. Comparative aalysis of the applicability of the skeletal age determiatio methods of Greulich-Pyle ad Thiema-Nitz for foresic age estimatio i livig subjects. It J Legal Med. 2007;121(4): Cameriere R, De Luca S, Biagi R, Cigolai M, Farroato G, Ferrate L. Accuracy of three age estimatio methods i childre by measuremets of developig teeth ad carpals ad epiphyses of the ula ad radius. J Foresic Sci. 2012;57(5): Galić I, Nakaš E, Prohić S, Selimović E, Obradović B, Petrovečki M. Detal age estimatio amog childre aged 5 14 years usig the Demirjia method i Bosia-Herzegovia. Acta Stomatol Croat. 2010;44(1): Cardoso HF. Epiphyseal uio at the iomiate ad lower limb i a moder Portuguese skeletal sample, ad age estimatio i adolescet ad youg adult male ad female skeletos. Am J Phys Athropol. 2008;135(2): Cameriere R, Flores-Mir C, Mauricio F, Ferrate L. Effects of utritio o timig of mieralizatio i teeth i a Peruvia sample by the Cameriere ad Demirjia methods. A Hum Biol. 2007;34(5): Badrov J, Lauc T, Nakas E, Galic I. Detal Age ad Tooth Developmet i Orthodotic Patiets with Ageesis of Permaet Teeth. Biomed Res It. 2017;2017: Galic I, Vodaovic M, Jakovic S, Mihaovic F, Nakas E, Prohic S, et al. Detal age estimatio o Bosia-Herzegoviia childre aged 6-14 years: evaluatio of Chaillet s iteratioal maturity stadards. J Foresic Leg Med. 2013;20(1): Demirjia A, Goldstei H, Taer JM. A ew system of detal age assessmet. Hum Biol. 1973;45(2): Willems G, Va Olme A, Spiesses B, Carels C. Detal age estimatio i Belgia childre: Demirjia s techique revisited. J Foresic Sci. 2001;46(4): Galic I, Vodaovic M, Cameriere R, Nakas E, Galic E, Selimovic E, et al. Accuracy of Cameriere, Haavikko, ad Willems radiographic methods o age estimatio o Bosia-Herzegovia childre age groups It J Legal Med. 2011;125(2): Cameriere R, Ferrate L, Cigolai M. Age estimatio i childre by measuremet of ope apices i teeth. It J Legal Med. 2006;120(1): Cameriere R, De Agelis D, Ferrate L, Scarpio F, Cigolai M. Age estimatio i childre by measuremet of ope apices i teeth: a Europea formula. It J Legal Med. 2007;121(6): World Medical Associatio. World medical associatio declaratio of Helsiki: Ethical priciples for medical research ivolvig huma subjects. JAMA. 2013;310(20): Ferrate L, Cameriere R. Statistical methods to assess the reliability of measuremets i the procedures for foresic age estimatio. It J Legal Med. 2009;123(4): Galic I, Pacifici A, Carboe D, Pacifici L, Jerocic A, Cameriere R. Age estimatio by the Cameriere s ormalized measuremets (CNM) of the sigle permaet madibular tooth o a paoramic radiograph. Leg Med (Tokyo). 2017;26: Liversidge HM. Detal age revisted. I: Irish JD, Nelso GC, editors. Techique ad applicatio i detal athropology. Cambridge: Cambridge Uiversity Press; p Ambarkova V, Galic I, Vodaovic M, Biocia-Lukeda D, Brkic H. Detal age estimatio usig Demirjia ad Willems methods: cross sectioal study o childre from the Former Yugoslav Republic of Macedoia. Foresic Sci It. 2014;234:187 e Ferades MM, Tioco RL, de Bragaca DP, de Lima SH, Fracesquii Juior L, Daruge Juior E. Age estimatio by measuremets of developig teeth: accuracy of Cameriere s method o a Brazilia sample. J Foresic Sci. 2011;56(6): Balla SB, Vekat Baghirath P, Hari Viay B, Vijay Kumar J, Babu DBG. Accuracy of methods of age estimatio i predictig detal age of preadolescets i South Idia childre. J Foresic Leg Med. 2016;43: Guo YC, Ya CX, Li XW, Zhou H, Li JP, Pa F, et al. Age estimatio i orther Chiese childre by measuremet of ope apices i tooth roots. It J Legal Med. 2015;129(1): Cugati N, Kumaresa R, Sriivasa B, Karthikeya P. Detal age estimatio of growig childre by measuremet of ope apices: A Malaysia formula. J Foresic Det Sci. 2015;7(3): El-Bakary AA, Hammad SM, Mohammed F. Detal age estimatio i Egyptia childre, compariso betwee two methods. J Foresic Leg Med. 2010;17(7): Cameriere R, Ferrate L, Liversidge HM, Prieto JL, Brkic H. Accuracy of age estimatio i childre usig radiograph of developig teeth. Foresic Sci It. 2008;176(2-3): Rivera M, De Luca S, Aguilar L, Veladia Palacio LA, Galic I, Cameriere R. Measuremet of ope apices i tooth roots i Colombia childre as a tool for huma idetificatio i asylum ad crimial proceedigs. J Foresic Leg Med. 2017;48:

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