Correlation of Skeletal Maturation Stages Determined by Cervical Vertebrae and Hand-wrist Evaluations
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1 Originl Article Correltion of Skeletl Mturtion Stges Determined by Cervicl Vertebre nd Hnd-wrist Evlutions Crlos Flores-Mir ; Corr A. Burgess b ; Mitchell Chmpney c ; Robert J. Jensen d ; Michel R. Pitcher e ; Pul W. Mjor f Abstrct: The im of this study ws to ssess the correltion between the Fishmn mturtion prediction method (FMP) nd the cervicl vertebrl mturtion (CVM) method for skeletl mturtion stge determintion. Hnd-wrist nd lterl cephlogrms from 79 subjects (52 femles nd 27 mles) were used. Hnd-wrist rdiogrphs were nlyzed using the FMP to determine skeletl mturtion level (dvnced, verge, or delyed) nd stge (reltive position of the individul in the pubertl growth curve). Cervicl vertebre (C2, C3, nd C4) outlines obtined from lterl cephlogrms were nlyzed using the CVM to determine skeletl mturtion stge. Intrexminer relibility (Intrclss correltion coefficient [ICC]) for both methods ws clculted from 10 triplicte hnd-wrist nd lterl cephlogrms from the sme ptients. An ICC coefficient of for FMP nd n ICC of for CVM were obtined. A Spermn correltion vlue of 0.72 (P.001) ws found between the skeletl mturtion stges of both methods. When the smple ws subgrouped ccording to skeletl mturtion level, the following correltion vlues were found: for erly mture dolescents 0.73, for verge mture dolescents 0.70, nd for lte mture dolescents All these correltion vlues were sttisticlly different from zero (P.024). Correltion vlues between both skeletl mturtion methods were modertely high. This my be high enough to use either of the methods indistinctively for reserch purposes but not for the ssessment of individul ptients. Skeletl level influences the correltion vlues nd, therefore, it should be considered whenever possible. (Angle Orthod 2006;76:1 5.) Key Words: Skeletl mturtion; Cervicl vertebre; Growth prediction INTRODUCTION Optiml effectiveness in the use of orthodontic or orthopedic pplinces hs been ssocited with skel Postdoctorl Fellow, Orthodontic Grdute Progrm, Fculty of Medicine nd Dentistry, University of Albert, Edmonton, Albert, Cnd. b c d e f Professor, Director of the Orthodontic Grdute Progrm, Fculty of Medicine nd Dentistry, University of Albert, Edmonton, Albert, Cnd. Corresponding uthor: Crlos Flores-Mir, DDS, CertOrth, PhD, Fculty of Medicine nd Dentistry, Room 4051A, Dentistry/ Phrmcy Centre, University of Albert, Edmonton, Albert, Cnd T6G 2N8 (e-mil: crlosflores@ulbert.c). Accepted: Mrch Submitted: Februry by The EH Angle Eduction nd Reserch Foundtion, Inc. etl mturtion. Functionl pplinces hve been shown to be more effective when used in the pek of mndibulr growth rther thn erlier. 1,2 However, some uthors hve stted tht becuse of the high vribility in mndibulr growth, this ssocition my not be predictive enough for the individul ptient. 3,4 Skeletl mturtion is generlly determined by using ossifiction stges of bones of the hnd nd wrist becuse of the vilbility of different types of bones in the re. 5 9 There re two generl pproches to the ssessment of the hnd-wrist rdiogrph. The first method consists of compring the ptient s hnd-wrist bone mturtion to n tls. 7,9 The second method of ssessment uses specific indictors to relte skeletl mturtion to the pubertl growth curve. This pproch focuses on the mturtion evlution of the individul rther thn on men vlues. Overll horizontl nd verticl fcil growth velocity hs been shown to be relted to skeletl mturity indictors determined by nlysis of hnd-wrist rdiogrphs. Skeletl mturity nlysis of hnd-wrist rdiogrphs for use in predicting fcil growth velocity should include bone stging s well s ossifiction events. 10 1
2 2 FLORES-MIR, BURGUESS, CHAMPEY, JENSEN, PITCHER, MAJOR Previous studies hve shown tht the progressive enlrgement of cervicl vertebre bodies is relted to humn skeletl ging nd verticl fcil ptterns. 14,15 In recent yers, evlution of cervicl vertebre in lterl cephlogrms hs been incresingly used to determine the skeletl mturtion The erly version of the cervicl vertebrl mturtion method (CVM) ws shown to be vlid tool to predict the pek of mndibulr growth 20,21 nd ws ssocited with mndibulr morphologicl chnges. 22 The CVM method, in the erly or the improved version, hs been used to evlute the clinicl effectiveness t different skeletl mturtion stges of the Biontor, 2 RME, 23 Twin Block. 1 Currently, the improved CVM method 24 is the most used cervicl mturtion evlution method, wheres the Fishmn mturtion prediction method (FMP) seems to be the most pproprite method for skeletl mturtion evlution. 10 Although comprisons of skeletl mturtion between different hnd-wrist nd cervicl vertebre indictors hve lredy been mde, no direct comprison between FMP 32 (using both skeletl stge n skeletl level) nd the improved CVM method 24 were found in the literture. A distinctive dvntge of the cervicl mturity evlution is tht it does not imply extr rdition exposure for the ptient. If hnd-wrist nd cervicl mturtion methods were highly correlted, there would be no justifiction to tke n extr hnd-wrist rdiogrph for skeletl mturtion determintion. The objective of this study ws to ssess the correltion between FMP nd CVM methods for the determintion of skeletl mturtion stge. MATERIALS AND METHODS Smple chrcteristics This smple ws previously used to evlute longitudinl crniofcil morphology chnges ssocited with temporomndibulr joint (TMJ) disk sttus. 33 Only 79 subjects (52 femles nd 27 mles) hd hnd-wrist rdiogrphs nd lterl cephlogrm of dequte qulity. Vribles Hnd-wrist rdiogrphs were nlyzed using the FMP 32 to determine skeletl mturtion level (dvnced, verge, or delyed) nd stge (reltive position of the individul in the pubertl growth curve). The hnd-wrist rdiogrphs were scnned t 300 dpi nd sent through e-mil to GrowthTek. 34 The pproprite skeletl mturtion stge nd level ws determined independently by clibrted technicin t the Growth Tek Compny (Skneteles, NY) ccording to the FMP. Previously, it ws determined tht under these conditions, scnned hnd-wrist rdiogrphs would be dequte for the evlution purposes. Complete detils bout FMP cn be found elsewhere. 32,34 Closed-mouth lterl cephlometric rdiogrphs were obtined for ech subject with Siemens OP 10 (Siemens, Bensheim, Germny) mchine, with the mndible stbilized by polyvinylsiloxne hbitul occlusion bite registrtion. Outlines of the cervicl vertebre (C2, C3, nd C4) were evluted by CF nd the pproprite skeletl mturtion stge ws determined ccording to CVM. Complete detils of the CVM cn be found elsewhere. 24 Efforts were mde to mke the reserch process s blind s possible. The evlutors who completed mturtion prediction using CVM were blinded to the skeletl mturtion stge determined by FMP nd vice vers. A sttisticin completed the sttisticl nlysis without specific knowledge of the coding of the mturtionl stges. Sttisticl nlysis A one-wy rndom intrclss correltion coefficient (ICC) ws used to determine the relibility of the dignosis for the FMP nd the CVM. Assumptions of normlity were not fulfilled. Therefore, nonprmetric Spermn correltion test ws used to correlte the skeletl mturtion stge between both methods. The correltion ws lso evluted by grouping the subjects ccording to their skeletl mturtion level. RESULTS Error of method Intrexminer relibility (ICC) for both methods ws clculted from 10 triplicte hnd-wrist nd lterl cephlogrms from the sme ptients. An ICC coefficient of (0.959 to 0.996; P.001) ws obtined for FMP nd n ICC of (0.723 to 0.968; P.001) ws obtined for CVM. Skeletl mturtion stges The distribution of the skeletl mturtion stges for the smple ccording to FMP nd CVM re shown in Tbles 1 nd 2. Correltion vlues A Spermn correltion vlue of 0.72 ws found between the skeletl mturtion stges of both methods. When the skeletl mturtion level ccording to FMP ws considered, the following correltion vlues were found: for erly mture dolescents 0.73, for verge mture dolescents 0.70, nd for lte mture
3 SKELETAL MATURATION WITH DIFFERENT METHODS TABLE 1. Frequency of Individuls in Ech Ctegory According to FMP Skeletl Mturtion Stge Individuls Percentge Totl FMP indictes Fishmn mturtion prediction method. TABLE 2. CVM Frequency of Individuls in Ech Ctegory According to Skeletl Mturtion Stge Individuls Percentge Totl CVM indictes Cervicl Vertebrl Mturtion. TABLE 3. Spermn s Correltion Between the FMP nd the CVM According to Skeletl Mturtion Level Number of School Children R of Spermn Significnce (P Vlue) Advnced Averge Delyed dolescents All the vlues were sttisticlly different from zero (P.024), s shown in Tble 3. DISCUSSION Becuse chronologicl ge is not vlid predictor of skeletl growth velocity or skeletl mturity, 8,35 37 conventionlly, hnd-wrist rdiogrphs hve been used to determine skeletl mturtion. Vlidity of skeletl mturity ssessment using the hnd-wrist rdiogrph in reltion to the stnding height (body skeletl growth velocity) hs been well estblished for severl rcil groups Although Moore 41 pointed out tht most of the bones of the body re preformed in crtilge nd lter developed by endochondrl ossifiction, the fcil bones re formed by intrmembrnous ossifiction without crtilginous precursors. Therefore, growth of the fce my be regulted by fctors other thn those responsible for growth of the long bones. Furthermore, the crniofcil structures include severl functionl regions tht my hve different growth responses to systemic nd locl environmentl conditions. Recently, the use of cervicl vertebre mturtion hs been suggested s vlid replcement to the hnd-wrist evlution. The min dvntge of the cervicl vertebre mturtion evlution is tht it cn be obtined from conventionl lterl cephlogrm, which would void n extr rdition exposure for the ptients. The results of this study suggested tht lthough the correltion vlues between both methods were high (0.72), they could only predict round 50% of the other method s skeletl mturtion determintion. Previous reserch found tht correltion vlues between skeletl mturtion determined from hnd-wrist rdiogrphs nd cervicl vertebre evlution were quite vrible (from 0.45 to 0.97) (Tble 4). Differences between the results of this study nd the reported comprison studies cn be expected on the bsis of the 3 TABLE 4. Correltion Vlues Between the Skeletl Mturtion Determined From Hnd-wrist Rdiogrphs nd Cervicl Vertebre Evlution From the Lterl Cephlometric Rdiogrphs Number of Subjects (Mles/Femles) Totl R (R Mles/R Femles) Hnd-wrist Skeletl Mturtion Method Cltbino et l (27/45) NS (0.450/0.564) Fishmn s SMI 32 Chng et l (244/259) NS (0.973/0.970) Fishmn s SMI 32 Grci-Fernndez et l (50/63) NS (NS/NS) Fishmn s SMI 32 Kucukkeles et l (99/81) NS (NS/NS) b Fishmn s SMI 32 Mito et l (0/66) NS (NA/0.869) TW2 9 Sn Romn et l (428/530) NS (0.69, 0.77, 0.79/0.79, 0.84, 0.85) Grve nd Brown 39 Zhng nd Wng (28/42) NS (NS/NS) Presence of sesmoid Wilcoxon mtched-pirs signed-rnks tests. b Agreement formul. NS Not significnt
4 4 FLORES-MIR, BURGUESS, CHAMPEY, JENSEN, PITCHER, MAJOR fctors such s smple size, sex, or specific methods used. The size of the smple used in this study is comprtively smll but presents distinctive dvntge in tht it nlyzes for the first time the influence of skeletl level (dvnced, verge, or delyed mturtion). Becuse the use of individul ossifiction events is of limited use in predicting the pubertl growth spurt, n nlysis tht includes mturtion levels s well s ossifiction events is recommended. 10 Considertion of mturtion level is significntly importnt for tretment timing. For exmple, during lte dolescence, dvnced mturers express significntly less growth velocity nd incrementl growth s compred with verge nd especilly delyed mturers who continue growth for longer period until dulthood. During the ccelerting nd high velocity periods of dolescence, dvnced mturers express significntly higher growth rtes nd express more growth over shorter time periods. Therefore, the importnce of estblishing the mturtionl ge of n individul is to predict the remining growth. Orthodontic or surgicl (or both) tretment success depends on understnding this. 42 Therefore, nlysis pproches such s the one described by Fishmn, 32,34 which re bsed on reltive growth velocity nd percentge of growth remining, re more useful thn nlyses which yield skeletl ge. Avoidnce of skeletl ge minimizes the influence of environment nd rcil composition of the smple. In most cses, use of reltive growth rte nd percentge of growth remining will resolve sex differences. The results of this study showed tht skeletl level hs n influence on the mount of correltion between skeletl mturtion determined by different methods. Therefore, future studies bout skeletl mturtion should tke this fctor into considertion. A lrger smple size my be required to confirm the findings of this study becuse the delyed mtured group only hd six individuls in the present smple. Although the use of FMP hs distinct dvntges 10 over the other skeletl mturtion determintion methods, current stringent ethicl criteri from the institutionl ethicl bords mke the use of hnd-wrist skeletl mturtion determintion less fesible. Incresed rdition exposure is the min reson. Also, in some retrospective reserch endevors, the lck of hndwrist rdiogrphs my lso limit the pplicbility of existing dt. Therefore, the use of cervicl vertebre mturtion determintion ppers to be useful tool in situtions where there re no hnd-wrist rdiogrphs vilble. Even if in clinicl sitution, n individul skeletl mturtion determintion my be possible. Some uthors hve stted tht becuse of the high vribility in mndibulr growth, this ssocition my not be predictive enough for the individul ptient. 3,4 Therefore, ssessment of skeletl mturtion my be vluble s n orthodontic reserch tool (group not individul subject s skeletl mturtion), but it hs limited predictive use in the individul ptient. Relizing the limittions of either method for clinicl prctice, the reduced rdition resulting from voidnce of n dditionl rdiogrph my justify the use of cervicl mturtion. CONCLUSIONS Correltion vlues between FMP nd CVM were modertely high. Skeletl level influences the correltion vlues nd should be considered whenever possible. REFERENCES 1. Bccetti T, Frnchi L, Toth LR, McNmr JA Jr. Tretment timing for Twin-block therpy. Am J Orthod Dentofcil Orthop. 2000;118: Fltin KJ, Fltin RM, Bccetti T, Frnchi L, Ghiozzi B, Mc- Nmr JA Jr. Long-term effectiveness nd tretment timing for Biontor therpy. Angle Orthod. 2003;73: Mitni H, Sto K. Comprison of mndibulr growth with other vribles during puberty. Angle Orthod. 1992;62: Sto K. Growth timing of mndibulr length, body height, hnd bones nd cervicl vertebre during puberty. Nippon Kyosei Shik Gkki Zsshi. 1987;46: Bmbh J, vn Ntt M. Longitudinl study of fcil growth in reltion to skeletl mturtion during dolescence. Am J Orthod. 1963;39: Bjork A, Helm S. Prediction of the ge of mximum pubertl growth in body height. Angle Orthod. 1967;37: Greulich W, Pyle S. Rdiogrphic Atls of Skeletl Development of Hnd nd Wrist. Stnford, Clif: Stnford University Press; Houston WJ, Miller JC, Tnner JM. Prediction of the timing of the dolescent growth spurt from ossifiction events in hnd-wrist films. Br J Orthod. 1979;6: Tnner JM, Whitehouse RH, Cmeron N, Mrshll WA, Hely MJR, Goldstein H. Assessment of Skeletl Mturity nd Prediction of Adult Height (TW2 Method). London, UK: Acdemic Press; Flores-Mir C, Nebbe B, Mjor PW. Use of skeletl mturtion bsed on hnd-wrist rdiogrphic nlysis s predictor of fcil growth: systemtic review. Angle Orthod. 2004;74: Isrel H. Progressive enlrgement of the vertebrl body s prt of the process of humn skeletl geing. Age Ageing. 1973;2: Hellsing E. Cervicl vertebrl dimensions in 8-, 11-, nd 15- yer-old children. Act Odontol Scnd. 1991;49: Tylor JR. Growth of humn intervertebrl discs nd vertebrl bodies. J Ant. 1975;49: Krlsen AT. 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5 SKELETAL MATURATION WITH DIFFERENT METHODS nificnce in orthodontics nd mxillofcil surgery. Rev Stomtol Chir Mxillofc. 1999;100: Hssel B, Frmn AG. Skeletl mturtion evlution using cervicl vertebre. Am J Orthod Dentofcil Orthop. 1995; 107: Mito T, Sto K, Mitni H. Predicting mndibulr growth potentil with cervicl vertebrl bone ge. Am J Orthod Dentofcil Orthop. 2003;125: Frnchi L, Bccetti T, McNmr JA Jr. Tretment nd posttretment effects of crylic splint Herbst pplince therpy. Am J Orthod Dentofcil Orthop. 1999;115: Lmprski D. Skeletl Age Assessment Utilizing Cervicl Vertebre. [mster s thesis]. Pittsburgh, P: University of Pittsburgh; Frnchi L, Bccetti T, McNmr JA Jr. Mndibulr growth s relted to cervicl vertebrl mturtion nd body height. Am J Orthod Dentofcil Orthop. 2000;118: O Reilly MT, Ynniello GJ. Mndibulr growth chnges nd mturtion of cervicl vertebre longitudinl cephlometric study. Angle Orthod. 1988;58: Frnchi L, Bccetti T, McNmr JA Jr. Thin-plte spline nlysis of mndibulr growth. Angle Orthod. 2001;71: Bccetti T, Frnchi L, Cmeron CG, McNmr JA Jr. Tretment timing for rpid mxillry expnsion. Angle Orthod. 2001;71: Bccetti T, Frnchi L, McNmr JA Jr. An improved version of the cervicl vertebrl mturtion (CVM) method for the ssessment of mndibulr growth. Angle Orthod. 2002; 72: Zhng Y, Wng B. Observtion of cervicl vertebre nd estimtion of their bone ge. Chung Hu Kou Ching Hsueh Ts Chih. 1997;32: Grci-Fernndez P, Torre H, Flores L, Re J. The cervicl vertebre s mturtionl indictors. J Clin Orthod. 1998; 32: Kucukkeles N, Acr A, Biren S, Arun T. Comprisons between cervicl vertebre nd hnd-wrist mturtion for the ssessment of skeletl mturity. J Clin Peditr Dent. 1999; 24: Mito T, Sto K, Mitni H. Cervicl vertebrl bone ge in girls. Am J Orthod Dentofcil Orthop. 2002;122: Sn Romn P, Plm JC, Oteo MD, Nevdo E. Skeletl mturtion determined by cervicl vertebre development. Eur J Orthod. 2002;24: Cltbino M, Leonrdi R, Zborr G. Evlution of cervicl vertebre for determintion of skeletl ge. Riv Itl Odontoitr Infnt. 1990;1: Chng HP, Lio CH, Yng YH, Chng HF, Chen KC. Correltion of cervicl vertebr mturtion with hnd-wrist mturtion in children. Kohsiung J Med Sci. 2001;17: Fishmn L. Mturtionl development nd fcil form reltive to tretment timing. In: Subtenly J, ed. Erly Orthodontic Tretment. Chicgo, Ill: Quintessence Publishing; 2000: Flores-Mir C, Nebbe B, Heo G, Mjor PW. Longitudinl study on TMJ disk sttus nd crniofcil growth. Am J Orthod Dentofcil Orthop. In press. 34. GrowthTek. Avilble t: Accessed Februry 10, Bowden BD. Epiphysil chnges in the hnd/wrist re s indictors of dolescent stge. Aust Orthod J. 1976;4: Fishmn LS. Chronologicl versus skeletl ge, n evlution of crniofcil growth. Angle Orthod. 1979;49: Hägg U, Trnger J. Mturtion indictors nd the pubertl growth spurt. Am J Orthod. 1982;82: Nnd R. The rtes of growth of severl fcil components mesured from seril cephlometric roentnogrms. Am J Orthod. 1955;41: Grve KC, Brown T. Skeletl ossifiction nd the dolescent growth spurt. Am J Orthod. 1976;69: So LL. Correltion of sexul mturtion with skeletl ge of southern Chinese girls. Aust Orthod J. 1997;14: Moore RN. Principles of dentofcil orthopedics. Semin Orthod. 1997;3: Fishmn LS. Cn cephlometric x-rys of the cervicl column be used insted of hnd-wrist x-rys to determine ptient s mturtionl ge? Am J Orthod Dentofcil Orthop. 2002;122:18A 19A. 5
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