Normal Development. Kamaldine Oudjhane

Transcription

1 Norml Development Kmldine Oudjhne 2 Contents 1 Generl Crtilge nd Bone Development Emryonic nd Fetl Development Infncy nd Childhood Crtilge Imging Physiologic Periostitis of Infncy Skeletl Mturtion References Astrct The development of the musculoskeletl system encompsses the emryonic period, fetl development, nd the lengthy postntl period of growth nd mturtion. This chpter emphsizes the growth of the infnt, child, nd dolescent ut riefly reviews key points of prentl development. Understnding crtilge mturtion is key to understnding one development, s well s imging of norml development nd pthology. After reviewing the process of physel one deposition, the chpter presents MRI ppernce of crtilge, focusing on the primry nd secondry physes. It discusses norml developmentl physiologic periostitis of infncy. The chpter concludes y discussing severl different systems for estlishing skeletl mturity nd reviewing for which ges ech is most pplicle. K. Oudjhne, MD, MSc Dignostic Imging Deprtment, The Hospitl for Sick Children, University of Toronto, 555 University Avenue, Toronto, ON M5G 1X8, Cnd e-mil: kmldine.oudjhne@sickkids.c The development of the musculoskeletl system encompsses the emryonic period, fetl development, nd the lengthy postntl period of growth nd mturtion. This chpter emphsizes the development of the infnt, child, nd dolescent ut riefly reviews key points of the prentl period. Understnding crtilge mturtion is key to understnding one development, s well s imging of norml development nd pthology. After reviewing the process of physel one deposition, the chpter reviews the mgnetic R. Stein-Wexler et l. (eds.), Peditric Orthopedic Imging, DOI / _2, Springer-Verlg Berlin Heidelerg

2 26 resonnce imging (MRI) ppernce of crtilge, focusing on the primry nd secondry physes. It discusses norml developmentl physiologic periostitis of infncy. The chpter concludes y discussing severl different systems for estlishing skeletl mturity nd reviewing for which ges ech is most pplicle. Bone mrrow mturtion is presented in Chp. 25, which ddresses oth norml nd pthologic one mrrow. 1 Generl Crtilge nd Bone Development 1.1 Emryonic nd Fetl Development Musculoskeletl development strts during the emryonic period, or the first 8 weeks fter conception. Following formtion of the trilminr emryonic disk during the first 2 weeks, induction strts the process of tissue speciliztion nd susequent orgnogenesis [ 1 ]. Primordil orgnogenesis occurs during the first 4 weeks, nd mjor defects in lim development cn occur t this time. Key lndmrks of skeletl development in the emryo nd fetus re summrized elow. Emryonic Development: Week 3: The emryonic disk develops, with individuliztion of somites nd the neurl tue. Week 4: The somites differentite into three segments dermtome (skin), myotome (muscle), nd sclerotome (crtilge nd one). The emryo is very sensitive to mjor defects in lim development during this period. During week 4, the lim uds originte s elevtions of the fetl unsegmented mesenchyme. The upper lim uds pper shortly efore those of the lower lim, nd the upper extremity continues to develop more quickly thn the lower until out ge 2 yers. Week 5: Mesenchyme condenses in the lims, nd the hnd plte is formed. Week 6: Mesenchyme chondrifies. Digits individulize. Week 7: Notching occurs etween the digits, nd the upper nd lower lims rotte in opposite directions. Week 8: The emryo is recognizly humn. Fetl Development: The fetl stge is chrcterized y rpid chnges in ody proportions, with the following highlights: Week 12: Bone development spreds eyond the clvicle, the first one to ossify. The reltively short lower lims grow rpidly. Week 14: Clefting of mesenchyme results in the formtion of synovil joints. This is followed y chondrifiction nd cvittion. Week 16: The development of the neuromusculr system llows for spontneous lim ctivity. Hemtopoiesis, which hd strted in the yolk sc nd then liver, egins in one s the mrrow spce develops [ 2 ]. Week 20: Growth nd remodeling of ody proportions continue, nd the fetus develops n infnt-like form. Much of the skeleton forms y endochondrl ossifiction. Mesenchyme condenstion occurs first, forming crtilge, which is then trnsformed to one [ 3 ]. This occurs t the skull se, long nd tuulr ones, clvicles, nd verterl column. Primry ossifiction centers develop within the diphyses of the long ones, in the vertere, in few epiphyses, nd in some of the smller ones efore irth. Their formtion requires chnges in the perichondrium: degenertion of hypertrophic cells nd incresed vsculrity form n ossified core t the crtilge-one interfce. Most of the epiphyses nd smll ones ossify fter irth. The flt ones such s the pelvis, scpul, skull, nd fcil ones form y intrmemrnous ossifiction, which occurs without crtilginous precursor. 1.2 Infncy nd Childhood K. Oudjhne Fetl woven one is flexile nd hs high collgen content; it is replced y lmellr one during infncy. Most of the smller ones develop primry ossifiction centers during infncy.

3 2 Norml Development During childhood, the long ones undergo further growth, with tremendous increse in length s well s thickness. Secondry ossifiction centers develop t the ends of the long ones. Longitudinl growth of long ones depends principlly on the primry physis, djcent to the metphysis. The secondry physis, which surrounds the epiphysis, results in the more sphericl configurtion t the ends of the long ones. Trnsverse growth t the diphysis occurs y intrmemrnous one formtion t the periosteum, which consists of n outer firous lyer nd n inner lyer composed of osteoprogenitor cells. Physis The physel crtilge includes three well-defined histologic zones: resting, prolifertive, nd hypertrophic. Its composition is the sme whether t the primry physis (utting the metphyses) or t the secondry physis (surrounding the secondry ossifiction centers), ut the secondry physis is thinner. The resting zone is closest to the metphysis or secondry ossifiction center nd contins n undnt, disorgnized mtrix of chondrocytes. These re the germintor stem cells of the physis. The prolifertive zone hs longitudinl columns of rpidly dividing chondrocytes responsile for incresed one length. It is rich in glycogen; rpid extrcellulr mtrix turnover tkes plce here. Chondrocyte prolifertion nd differentition re highly regulted y secreted growth fctors tht ctivte chondrocytespecific trnscription fctors [ 4 ]. The hypertrophic zone uts the crtilge nd includes segment where chondrocytes mture, segment of degenertion (with disintegrtion of mucopolyscchrides nd declining lood supply), nd zone of provisionl clcifiction. The zone of provisionl clcifiction is closest to the metphysis nd mrks the trnsition from one to crtilge; this is the wekest prt of the growth plte. The periphery of the metphysis, djcent to the physis, is very vsculr site of ctive one formtion nd remodeling. The perichondril ring of LCroix nd the groove of Rnvier constitute the periphysis, firo-chondro-osseous structure tht encircles the growth plte nd the 27 most recently developed portion of the metphysis [ 5 ]. The periphysis nd one formed y the grdul trnsverse growth of the physis mke up the metphysel collr in the young child; this my protrude from the metphysel contour nd must e differentited from corner metphysel frcture (see Chp. 18 ). The vsculr system plys mjor role in growth plte physiology [ 6 ]. Three mjor pthwys supply the physis: the epiphysel rteries of the secondry ossifiction center rech the prolifertive segment, the diphysil nutrient rteries provide cpillry network to the metphyselphysel junction, nd the perichondril rteries supply the periphysis. Bone remodeling occurs y funneliztion, with one resorption nd deposition; longitudinl growth nd shping t the epiphysis, metphysis, nd diphysis result. The crophyses, including the epiphyses, pophyses, crpls, trsls, nd growth pltes t nonphysel ends of the smll tuulr ones, mke up the growth pltes of the secondry ossifiction centers [ 7 ]. Crtilge The ends of the long ones re composed of hyline crtilge. Although ll hyline crtilge consists of chondrocytes nd wter within mtrix of collgen nd glycosminoglycns, the rchitecture nd the exct composition vry. Epiphysel crtilge, physel crtilge (whether t the primry physis or t the secondry physis tht surrounds the epiphysel ossifiction center), nd rticulr crtilge therefore pper different on some MRI sequences. Articulr crtilge is hypocellulr nd vsculr; it consists predominntly of collgen nd proteoglycn mtrix. Physel crtilge is very cellulr, especilly the hypertrophic zone; it is vsculr until ge 18 months nd then ecomes vsculr. Epiphysel crtilge is very vsculr while the ossifiction center is developing [ 8, 9 ]. The rticulr crtilge functions to trnsmit nd uffer force, wheres the epiphysel nd physel crtilge contriute to growth. With mturtion, the ppernce of epiphysel nd physel crtilge chnges.

4 28 K. Oudjhne 2 Crtilge Imging MRI differentites etween joint fluid nd rticulr crtilge; it cn lso differentite etween epiphysel, physel, nd rticulr crtilge ecuse of their different compositions [ 10 ]. At histologicl exmintion, hyline crtilge of the epiphysis demonstrtes chondrocytes within mtrix rich in wter, collgen, glycoproteins, nd glycosminoglycns. The wter is ound to collgen fiers, nd only smll frction is free. The orienttion of the collgen fiers is uniform in the physel nd epiphysel crtilge. However, in the rticulr crtilge where it is less tightly ound to wter its pttern vries depending on loction. The superficil collgen fiers prllel the rticulr surfce, wheres those in the deep zone re perpendiculr to the surfce; those in the intermedite zone hve more rndom rrngement [ 11 ]. Some MRI sequences demonstrte sutle differences in signl intensity, corresponding to these different zones. A vriety of sequences hve een developed to imge crtilge, nd others llow moleculr nd functionl imging. As generl rule, crtilge imging requires t lest 1.5 tesl (T) mgnet. Crtilge is, in generl, isointense to muscle on T1-weighted (T1-W) imging (Fig. 2.1 ) nd reltively hypointense on fluid-sensitive sequences [ 12 ]. T1-W nd intermedite-weighted proton density (PD) sequences re super for showing morphology of ligments nd menisci. However, these sequences offer little informtion out rchitecture of the hyline crtilge of the epiphysis, s its signl intensity is uniform on these sequences [ 13 ] (Fig. 2.2 ). Hyline crtilge lso shows uniform signl intensity (high to intermedite) on grdient echo (GRE) sequences. Decresing the flip ngle (to ) on these sequences increses T2 weighting nd thus helps differentite hypointense crtilge from more hyperintense joint fluid [ 8 ]. Fluid-sensitive sequences, such s short tu inversion recovery (STIR) nd T2-weighted (T2- W) (especilly ft-suppressed (FS) sequences), Fig. 2.1 Homogeneous ppernce of femorl hed crtilge in 6-month-old. ( ) Coronl T1-weighted (T1-W) imge shows the epiphysis ( sterisk ) is of homogeneous intermedite signl intensity. ( ) Coronl grdient echo ( GRE ), fst field echo ( FFE ) imge shows modertely hyperintense crtilge signl, long with smll mount of very hyperintense joint fluid ( white rrow ) on the left. Note crtilginous trirdite crtilge ( lck rrowheds ), which hs similr signl intensity to the femorl hed chrcterize crtilge rchitecture etter thn T1-W sequences (Fig. 2.3 ). On these fluidsensitive sequences, signl intensity of physel nd rticulr crtilge is higher thn tht of epiphysel crtilge, proly due to incresed cellulrity nd free wter in the growth plte crtilge compred with epiphysel crtilge. Becuse the physel crtilge hs longer T2 vlues, incresing the echo time (TE) enhnces the contrst etween epiphysel nd physel crtilge. 3D dul-echo stedy-stte imging (3D-DESS) is lso useful for imging crtilge, improving the ccurcy of crtilge thickness ssessment (Fig. 2.4 ). Regrdless of the sequence employed, dequte sptil resolution is essentil for stisfctory imging of crtilge.

5 2 Norml Development 29 Fig. 2.2 Norml infnt knee. ( ) Coronl T1-W imge shows the growth plte nd epiphysel crtilge hve homogeneous intermedite signl. The zone of provisionl clcifiction ( ZPC ) is hypointense ( rrow ) djcent to the hyperintense metphysis. ( ) Coronl STIR imge shows the primry physis is hyperintense, compred to the intermedite signl epiphysel crtilge. The secondry physis, surrounding the epiphysel ossifiction center, is lso hyperintense ( rrow ) ut much thinner thn the primry physis (Courtesy of Mrilyn Rnson) Fig. 2.3 Epiphysel crtilge in 4-yer-old oy. ( ) Sgittl T1-W imge shows uniformly isointense crtilge (compred to muscle). ( ) Sgittl inversion recovery ( IR ) imge shows isointense signl intensity (compred to muscle) in the crtilge surrounding the ossified epiphysis nd hyperintense physel crtilge (Courtesy of Reecc Stein-Wexler)

6 30 K. Oudjhne Fig. 2.4 Epiphysel crtilge contrsted ginst joint fluid on sgittl 3D doule-echo stedy-stte ( 3D-DESS ) imge of the knee in 13-yer-old oy. The epiphysel nd rticulr hyline crtilge is slightly less right thn the joint fluid With development, the crtilge chnges in severl wys. Epiphysel crtilge evolves from its infntile ppernce of uniform intermedite signl on T1-W imges nd moderte hyperintensity on fluid-sensitive sequences [ 12 ]. As ossifiction egins, fluid-sensitive sequences demonstrte ptchy, heterogeneous (more hyperintense) res, likely due to incresed free wter. These re most evident t the posterior distl femorl condyle nd the trochle of the distl humerus, ut re lso seen elsewhere [ 14 ] (Fig. 2.5 ). Crtilge t weight-ering res (e.g., the cetulum nd the distl nd proximl femur) develops decresed T2 signl s the child egins wlking, proly s wter is displced from crtilge [ 15 ] (Fig. 2.6 ). The physel crtilge t oth the primry physis nd t the peri-epiphysel secondry physis hs specific rchitecture tht yields trilminr ppernce on MRI (Figs. 2.7 nd 2.8 ). The portion tht uts the metphysis, the zone of provisionl clcifiction, is densely minerlized nd thus mrkedly hypointense on ll sequences. The reminder of the physel crtilge, like the rticulr crtilge, resemles unossified epiphysel crtilge on T1-W imges nd is predominntly hypointense. However, on fluid-sensitive sequences, this portion of the physis (the germinl nd prolifertive zones s well s prt of the hypertrophic zone) is righter thn epiphysel crtilge, yielding the second identifile lyer [ 13 ]. The Fig. 2.5 Norml hyperintense pre-ossifiction centers within epiphysel crtilge. Sgittl PD ( ) nd fst spin echo ( FSE ) T2-W FS ( ) show pre-ossifiction ( rrows ) (Courtesy of Mrilyn Rnson)

7 2 Norml Development 31 Fig. 2.6 Morphologicl chnges in crtilge with mturtion in 6-yer-old oy. Sgittl T2-weighted ( T2-W ) imge with ft-suppressed ( FS ) knee imge shows the weight-ering epiphysel crtilge of the femorl condyle hs reltively low signl, likely relted to displcement of wter from crtilge ( rrow ). A focus of incresed signl in the posterior epiphysel crtilge of femorl crtilge ( curved rrow ) likely represents the hyperintense fluid condenstion tht cn e seen prior to the onset of ossifiction. In ddition, the hyperintense rticulr crtilge ( rrowhed ) contrsts ginst the more intermedite signl of the epiphysel crtilge Fig. 2.7 Norml ppernce of physel, epiphysel, nd rticulr crtilge in 7-yer-old oy. ( ) Sgittl PD FS imge shows hypointense ZPC ( white rrows ), modertely hyperintense physel crtilge ( lck rrowhed ), nd modertely hyperintense rticulr crtilge ( white rrowhed ). The ossified portion of the epiphysis is hypointense, nd the reminder of the epiphysel crtilge is heterogeneously hyperintense. ( ) Sgittl PD imge lso demonstrtes the vrious crtilge regions (Courtesy of Reecc Stein-Wexler)

8 32 K. Oudjhne Fig. 2.8 Norml ppernce of crtilge in n dolescent knee. ( ) Sgittl FSE T2-W FS imge shows trilminr ppernce with hyperintense metphysel spongios, hypointense ZPC ( lck rrow ), nd hyperintense physis. The epiphysel crtilge ( white rrow ) hs lower signl thn rticulr crtilge. ( ) Sgittl multiplnr T1-W GRE imge shows uniformly right crtilge signl (Courtesy of Mrilyn Rnson) physis tht surrounds the ossifiction center in the epiphysis, the secondry physis, hs similr rchitecture nd signl intensity ut is thinner. Epiphysel ossifiction egins in single ossifiction center (s t the distl femur), in two centers (s t the proximl humerus), or in severl centers (s t the trochle of the distl humerus). The contour my e irregulr. Norml signl intensity t MRI helps differentite multiple ossifiction centers from frgmenttion of single center. If there is single focus of ossifiction, ossifiction egins in the center of the epiphysis. Initilly sphericl, s endochondrl one forms, the shpe chnges to hemispheric, with the flt portion djcent to the primry physis [ 16 ]. Although epiphysel mrrow is initilly, like the djcent metphysis, hemtopoietic, within few months it ecomes uniformly ftty (see Chp. 25 ). Development of crpl ones, trsl ones, nd pophyses is similr to tht of epiphyses. They therefore lso demonstrte conversion to ftty mrrow much sooner thn do the metphyses of long ones. In very young children, the primry physis is flt nd smooth, ut with growth its contour egins to undulte [ 8 ]. It should still hve uniform thickness, unless it hs een dmged (e.g., fter frcture or s result of chronic stress in thletes). The physis thins with mturtion nd eventully fuses nd disppers, sometimes leving very thin hypointense liner scr. Physel fusion usully egins in the center of the physis nd spreds to the periphery. The exception to this is t the distl tii, where the nteromedil physis fuses first (t Kump s ump) nd fusion progresses posterolterlly. Epiphysel crtilge is initilly perfused y vessels within crtilge cnls; these grdully ecome smller nd less numerous. Vsculriztion is most redily pprecited fter dministrtion of intrvenous gdolinium, on ft- suppressed T1-W imges. The vsculr chnnels of the crtilginous epiphysis exhiit liner nd punctte res of high signl intensity (the punctte res re vsculr chnnels viewed on end). Before the ge of 18 months, some chnnels cross from metphysis to epiphysis, nd vsculr cnls re rryed prllel to ech other nd to the long xis of the one. As the secondry ossifiction center develops, the orienttion of the vsculr chnnels chnges, so

9 2 Norml Development 33 Fig. 2.9 Rditing rry of epiphysel vessels in young child. ( ) Sgittl T1-W MRI shows homogeneous intermedite signl of the epiphysel nd rticulr crtilge. ( ) With GRE, rditing vsculr chnnels re evident. The physes lso enhnce (Courtesy of Mrilyn Rnson) tht they re rryed in spoke-like fshion round the ossifying epiphysis [ 9 ] (Fig. 2.9 ). During most of childhood, metphysel nd epiphysel lood flow re seprte, with importnt consequences for trum s well s spred of infection nd tumor. Gdolinium-enhnced sequences llow definition of the firovsculr cuff nd the primry Fig Norml ppernce of epiphysel vsculture in 6-yer-old. Gdolinium-enhnced T1-W fst field echo ( FFE ) ft-suppressed ( FS ) MRI shows, on sgittl view ( ), enhncement of the primry spongios of new metphysel one ( curved rrow ). There is lso enhncement of the superiostel firovsculr tissue tht forms the posterior metphysel stripe ( rrowhed ). () Axil imge shows typicl spoke-wheel pttern of vsculr chnnels in the epiphysel crtilge ( rrowhed ) spongios of new one formtion; it lso delinetes the posterior metphysel stripe, which is superiostel nd of firovsculr tissue tht contriutes to growth (Fig ). In older ptients, specilized MRI techniques such s

10 34 K. Oudjhne delyed gdolinium-enhnced MRI (dgemric) nd T2 mpping llow visuliztion of the four unique zones of rticulr crtilge: superficil or tngentil, middle or trnsitionl, deep or rdil, nd clcified [ 11 ]. In higher field-strength mgnets, 3D isotropic techniques cn e pplied to crtilge imging [ 17 ]. 3 Physiologic Periostitis of Infncy (Box 2.1) Box 2.1: Physiologic Periostitis of Infncy 1 4 months old (residul findings occsionlly seen to 6 months old) Bilterl in % Frequency: tii > femur > humerus > uln > rdius <2 mm thick Diphysis Fig Physiologic periostitis of infncy in 2-monthold oy. Frontl views show ilterl lmellr one formtion ( rrows ) long the lterl diphysel cortex of oth femurs ( ) nd long the medil diphysel cortex of oth tiis ( ) Physiologic periostitis of infncy is norml physiologic process wherein new one forms rpidly y intrmemrnous ossifiction long the periosteum of the diphysis of long ones. This cn e identified in one third to one hlf of infnts etween 1 nd 4 months of ge. The residul finding of superiostel one lending into cortex cn e seen occsionlly s lte s 6 months of ge [ 18 ]. Periostel new one results from the rpid growth tht is chrcteristic of erly infncy, comined with the fct tht in children the periosteum is reltively thick nd loosely ttched. It generlly involves oth the upper nd lower extremities [ 19 ] nd is ilterl in % (especilly t the femur) [ 18 ]. The tii is ffected most often, followed y the femur, humerus, uln, nd rdius. The periostel new one initilly ppers s fint morphous line prlleling the diphysis of the long one, seprted from the cortex y thin lucent line. Not necessrily concentric, it my e seen on only one projection (Fig ). As the child grows, the lyer of new one thickens nd ecomes denser, riefly resemling doule cortex. It is grdully sored into the cortex, where it contriutes to one width. Physiologic periostitis is differentited from pthologic periostitis y its thinness (less thn 2 mm), y the fct tht it spres the metphysis, nd y the typicl ge t presenttion, 1 4 months [ 18 ]. It should not e confused with osteomyelitis, infntile corticl hyperostosis, trum, vitmin A intoxiction, leukemi, or metsttic neurolstom.

11 2 Norml Development 4 Skeletl Mturtion Assessment of skeletl mturity is importnt in severl clinicl scenrios: in the setting of suspected hormonl normlity (e.g., precocious puerty), to help predict dult height (especilly importnt in children with short stture), nd to determine pproprite timing of surgery for scoliosis or for leg-length discrepncy. Rdiologic ssessment of skeletl mturity relies on evlution of minerliztion, mturtion, nd morphology of the ossifiction centers nd comprison of these oservtions to stndrds. Mny methods of one ge ssessment hve een developed, ut they re plgued y questions out ccurcy, sttisticl vlidity, nd interoserver vriility [ 20, 21 ]. Furthermore, there re mrked sexul, rcil, fmilil, nd environmentl influences on one development. For exmple, the sequence of ossifiction in the hnd nd wrist vries such tht the triquetrum my ossify in ny order rnging from the 3rd to the 24th of the 28 centers [ 22 ]. Some stndrds re sed on specific popultion group nd do not necessrily pply to others [ 21, 23 ]. Girls differ from oys, not only in their dvnced mturity ut lso in the order of ossifiction, nd lck infnts re more skeletlly mture thn white infnts. Therefore it is importnt to consider the stndrds s pproximtions nd to lwys include rnge of two stndrd devitions in estimting one ge. Computer-ssisted mesurement ppers to increse sttisticl power [ 24 ]. Skeletl mturity in different prts of the ody cn e discordnt, nd this ffects timing of surgicl intervention. Discrepncy my e striking in the hnd nd wrist, where crpl mturtion my lg ehind or precede phlngel mturtion y severl yers. This cn e syndromic or ssocited with disese ut is more often inconsequentil. However, up to 40 % of ptients demonstrte 1-yer difference in physel fusion etween the distl forerm nd the leg, nd physel closure in the hnd my precede or follow physel closure in the tii y up to 2 yers. This hs importnt implictions for timing of surgery. More importnt thn the precise stge of skeletl mturity of the hnd, elow, or ilic crest is the stte of mturtion in the one (or ones) eing considered for potentil intervention. 35 Skeletl mturity my e ssessed y severl methods, depending on ptient ge. In premture infnts nd during the prentl period, the presence of specific ossifiction centers correltes with ptient ge. During the first yer of life, the method of Sontg cn e used (see elow) [ 25 ]. During much of childhood, skeletl ge determintion is sed on PA view of the left hnd, ccording to the methods of Greulich nd Pyle, Tnner, Gilsnz nd Rti, nd others [ ]. However, during the puertl growth spurt, these methods ecome less ccurte, nd skeletl ge cn e determined y the configurtion of the olecrnon pophysis [ 29 ] nd then, lter, y the sttus of the ilic crest pophysis [ 30 ]. Before irth nd in premture infnts, ge cn e ssessed y determining whether ossifiction hs egun in key centers. A few importnt prentl ossifiction stndrds follow: Dentl uds t weeks, +/ 2 weeks Clcneus t 24 weeks Tlus t 28 weeks Distl femur epiphysis t 36 weeks Proximl tiil epiphysis t 38 weeks Proximl humerl epiphysis t weeks In ddition, throughout childhood, multiple ossifiction centers provide rough lndmrks for skeletl mturity [ 20 ] (see Tle 2.1 ). In infnts less thn 1 yer old, skeletl mturtion cn e determined y the Sontg method [ 25 ]. This method counts secondry ossifiction centers in hlf of the skeleton, sed on rdiogrph of the entire left upper extremity (including the shoulder to the distl epiphyses of the fingers) nd second rdiogrph of most of the left lower extremity (from the mid-femur to the distl epiphyses). All secondry ossifiction centers except the tlus nd clcneus re counted, including the corcoid nd other centers t the shoulder. The totl numer of ossifiction centers in the hemiskeleton is compred with norml vlues for children up to ge 1.5 yers (see Tle 2.2 ). From ge 1 yer through dolescence, evlution of the hnd is generlly performed, though interprettion is plgued y questions of sttisticl ccurcy. Specificity is lower nd stndrd devitions greter during the dolescent growth spurt, nd other ones my e evluted t this ge, s discussed elow. The Greulich nd Pyle

12 36 Tle 2.1 Selected ossifiction centers, 50th percentile ge t ppernce 50th percentile ge t ppernce Boys Girls 1. Infncy Cpitte 3 m 2 m Hmte 4 m 2 m Cpitellum of humerus 4 m 3 m Cpitl femorl epiphysis 4 m 4 m Cuneiform 3 6 m 3 m Humerus greter tuerosity 10 m 6 m 2. Erly childhood Cuneiform 1 2 y, 2 m 1 y, 5 m Cuneiform 2 2 y, 8 m 1 y, 10 m Nviculr of the foot 3 y 1 y, 11 m Fiul proximl epiphysis 3 y, 6 m 2 y, 7 m Ptell 4 y 2 y, 6 m 3. Childhood Rdius hed 5 y, 3 m 3 y, 10 m Medil epicondyle of humerus 6 y, 3 m 3 y, 5 m Clcnel pophysis 7 y, 7 m 5 y, 4 m Olecrnon of uln 9 y, 8 m 8 y Lterl epicondyle of humerus 11 y, 3 m 9 y, 3 m 4. Adolescence Tiil tuercle 11 y, 10 m 10 y, 3 m Adductor sesmoid of thum 12 y, 9 m 10 y, 9 m Acromion 13 y, 9 m 11 y, 11 m Ilic crest 14 y 12 y, 9 m Corcoid pophysis 14 y, 4 m 12 y, 3 m Ischil tuerosity 15 y, 3 m 13 y, 11 m Adpted from Ref. [ 20 ] y yer, m month Tle 2.2 Age sed on presence of hemi-skeleton ossifiction centers in the infnt Numer of centers in oys Numer of centers in girls Age (months) Men 1 S.D. Men 1 S.D Adpted from Ref. [ 25 ] method compres the ppernce, growth, modeling, nd fusion of the metcrpl nd phlngel epiphyses s well s the crpl centers to K. Oudjhne stndrd hnd rdiogrphs [ 26 ]. Tle 2.3 is sed on the tls of Greulich nd Pyle nd summrizes chnges during the erly dolescent period fter ossifiction of the dductor sesmoid. Tnner s method ssigns score to the crpl ones (except the pisiform) nd to the epiphyses of the distl uln, distl rdius, nd metcrpls nd phlnges of the first, third, nd fifth rys. These re summed to estlish n individul s skeletl mturity scle nd do not directly refer to ptient ge [ 27 ]. A digitlly formtted tls of the hnd, developed y Gilsnz nd Rti, includes lrge rnge of smple popultions nd is sttisticlly more ccurte [ 28 ]. Assessment of skeletl mturity round puerty is very importnt, ecuse the success of some surgicl interventions depends on the precise timing of when they re performed. Puerty cn e divided into two phses: ccelertion nd decelertion [ 31 ]. The puertl growth spurt (on verge, ge for girls nd for oys) is considered ccelertionl. Growth is rpid nd the rte of growth increses during this time. The susequent 3 yers (on verge, ge for girls nd for oys) re considered decelertionl, s growth grdully ceses. Different methods of one ge ssessment hve vrying utility during these periods. The Suvegrin method, which evlutes the ossifiction centers of the elow, ssesses mturtion during growth ccelertion ut is sttic during decelertion, when ll physes hve fused. The Risser method, in contrst, which evlutes the ilic crest pophysis, is sttic during ccelertion ut useful during decelertion. The method of Greulich nd Pyle is firly ccurte efore the puertl growth spurt ut reltively imprecise during oth the ccelertionl nd decelertionl growth phses. During the ccelertion phse of skeletl mturtion, the ossifiction centers of the elow chnge drmticlly, from eing predominntly crtilginous to eing fully fused. Indeed, they chnge enough in the course of 6 months to llow determintion of skeletl mturity on seminnul sis, which helps fine-tune surgicl plnning. The Suvegrin method nlyzes the size nd shpe of the lterl condyle nd epicondyle, trochle, olecrnon, nd rdil hed pophyses on

13 2 Norml Development 37 Tle 2.3 Estimtion of skeletl ge in dolescence Skeletl ge in oys Skeletl ge in girls Bone Age (yers) 1 S.D. (months) Age (yers) 1 S.D. (months) Smll dductor sesmoid Lrge dductor sesmoid DP 1, fusion lmost complete DP 2 5, prtil fusion in mle DP, ll fused PP, prtil fusion DP, ll fused MP, prtil fusion PP, fusion lmost complete DP, MP, PP, ll fused Rdius, prtil fusion Adpted from Ref. [ 26 ] DP distl phlnx epiphysis, MP middle phlnx epiphysis, PP proximl phlnx epiphysis c d Fig Mturtion of the olecrnon. According to the simplified Suvegrin method, the configurtion of the olecrnon ossifiction chnges from ( ) two ossific centers, to ( ) single hlf-moon-shped center, to ( c ) rectngulr center, to ( d ) center tht hs completely fused to the uln frontl nd lterl views to provide reltively ccurte mens of ssessing skeletl mturity [ 29 ]. It is lso possile to employ simplified Suvegrin method, which focuses on the ppernce of the olecrnon pophysis viewed on lterl rdiogrph [ 31 ]. The olecrnon chnges from hving two ossifiction centers initilly (t ge 11 in girls, 13 in oys) to resemling hlf- moon 6 months lter nd to ppering more rectngulr fter nother 6 months. It then egins fusion (ge 12.5 in girls, 14.5 in oys) nd 6 months lter is fully fused to the uln [ 31 ] (Fig ) (Tle 2.4 ). The configurtion of the ilic crest pophysis egins to chnge 6 months fter the elow physes close, so Risser stging is pplied to the decelertionl growth phse. The pophysis t the ilic crest ossifies in predictle mnner initilly lterl, with progressive ossifiction of the more

14 38 Tle 2.4 Skeletl mturtion indices in the second decde K. Oudjhne Girls Boys Risser scle Olecrnon Fusion of epiphyses 11 y 13 y 0 2 centers 11.5 y 13.5 y Hlf-moon 12 y 14 y Rectngle 12.5 y 14.5 y Begins fusion 13 y 15 y Fusion complete 13 y, 8 m 14 y, 7 m 1 Distl phlnx epiphyses [ 2 5] 14 y, 6 m 15 y, 7 m 2 Proximl phlnx epiphyses Greter trochnter pophysis 15 y, 2 m 16 y, 2 m 3 Distl phlnx epiphyses [ 1, 2 ] 16 y, 2 m 17 y 4 Distl ulnr epiphysis 18 y, 1 m 18 y, 6 m 5 Distl rdil epiphysis Adpted from Refs. [ 26, 30 32] y yer, m month centrl portions s the more peripherl portions undergo fusion. At Risser 0, the pophysis hs not yet ossified, nd t Risser 5 it is fully formed nd fused. The intermedite stges divide the ilic crest into qurtiles (see Chp. 3 for dditionl discussion of the Risser method). Mturtion of the hnd, elow, nd ilic crest should correlte (Tle 2.4 ). The olecrnon mtures during erly puerty (11 13 yers in girls, yers in oys), when the ilic crest registers s Risser 0 (non-ossified pophysis). Risser 1 occurs t the sme time s fusion of the distl phlnges in the hnd. At Risser 2, the greter trochnter fuses to the femur, nd the metcrpl epiphyses fuse. Risser 3 occurs t the sme time s closure of the epiphyses of the middle phlnges. At Risser 4, the distl uln fuses. Finlly, Risser 5 is lengthy period during which the distl rdius epiphysis grdully fuses to the rdius. Skeletl mturity cn lso e used to estimte dult stture. The Byley nd Pinneu tles [ 33 ] re esy to use, ut more ccurte system devised y Roche nd collegues integrtes vriles such s present height, weight, skeletl ge, nd prentl stture [ 34 ]. References 1. Hll BK. The emryonic development of one. Am Sci. 1988;76(2): Byn PS, Rnson M, McCrville ME. Norml one mrrow: signl chrcteristics nd ftty conversion. Mgn Reson Imging Clin N Am. 1998;6(3): PuMed PMID: Dietz FR, Morcuende JA. Emryology nd development of the musculoskeletl system. In: Morrissy RT, Weinstein SL, editors. Lovell nd Winter s peditric orthopedics: sixth edition. 6th ed. Phildelphi: Lippincott Willims & Wilkins; p Wuelling M, Vortkmp A. Chondrocyte prolifertion nd differentition. Endocr Dev. 2011;21:1 11. PuMed PMID: Oestreich AE, Ahmd BS. The periphysis nd its effect on the metphysis: I. Definition nd norml rdiogrphic pttern. Skeletl Rdiol. 1992;21(5): PuMed PMID: Gry H, Stndring S, Ellis H, Berkovitz BKB. Gry s ntomy: the ntomicl sis of clinicl prctice. 39th ed. Edinurgh/New York: Elsevier Churchill Livingstone; xx, 1627 pp. 7. Oestreich AE. The crophysis: unifying concept for enchondrl one growth nd its disorders. I. Norml growth. Skeletl Rdiol. 2003;32(3): PuMed PMID: Jrmillo D, Lor T. Peditric musculoskeletl MRI: sic principles to optimize success. Peditr Rdiol. 2008;38(4): PuMed PMID: Brnewolt CE, Shpiro F, Jrmillo D. Norml gdolinium- enhnced MR imges of the developing ppendiculr skeleton: Prt I. Crtilginous epiphysis nd physis. AJR Am J Roentgenol. 1997;169(1): PuMed PMID: Khnn PC, Thp MM. The growing skeleton: MR imging ppernces of developing crtilge. Mgn Reson Imging Clin N Am. 2009;17(3):411 21, v. PuMed PMID: Potter HG, Foo LF. Mgnetic resonnce imging of rticulr crtilge: trum, degenertion, nd repir. Am J Sports Med. 2006;34(4): PuMed PMID: Lor T, Jrmillo D. MR imging insights into skeletl mturtion: wht is norml? Rdiology. 2009;250(1): PuMed PMID: Jrmillo D, Connolly SA, Mulkern RV, Shpiro F. Developing epiphysis: MR imging chrcteristics nd histologic correltion in the neworn lm.

15 2 Norml Development Rdiology. 1998;207(3): PuMed PMID: Chpmn VM, Nimkin K, Jrmillo D. The preossifiction center: norml CT nd MRI findings in the trochle. Skeletl Rdiol. 2004;33(12): PuMed PMID: Vrich LJ, Lor T, Jrmillo D. Norml mturtion of the distl femorl epiphysel crtilge: ge-relted chnges t MR imging. Rdiology. 2000;214(3): PuMed PMID: Rivs R, Shpiro F. Structurl stges in the development of the long ones nd epiphyses: study in the New Zelnd white rit. J Bone Joint Surg Am. 2002;84-A(1): PuMed PMID: Nrghi A, White LM. Three-dimensionl MRI of the musculoskeletl system. AJR Am J Roentgenol. 2012;199(3):W PuMed PMID: Kwon DS, Spevk MR, Fletcher K, Kleinmn PK. Physiologic superiostel new one formtion: prevlence, distriution, nd thickness in neontes nd infnts. AJR Am J Roentgenol. 2002;179(4): PuMed PMID: Shopfner CE. Periostel one growth in norml infnts. A preliminry report. Am J Roentgenol Rdium Ther Nucl Med. 1966;97(1): PuMed PMID: Grhm CB. Assessment of one mturtion methods nd pitflls. Rdiol Clin North Am. 1972;10(2): PuMed PMID: Ontell FK, Ivnovic M, Alin DS, Brlow TW. Bone ge in children of diverse ethnicity. AJR Am J Roentgenol. 1996;167(6): PuMed PMID: Grn SM, Rohmnn CG, Silvermn FN. Rdiogrphic stndrds for postntl ossifiction nd tooth clcifiction. Med Rdiogr Photogr. 1967;43(2): PuMed PMID: Gilsnz V, Skggs DL, Kovnliky A, Syre J, Loro ML, Kufmn F, et l. Differentil effect of 39 rce on the xil nd ppendiculr skeletons of children. J Clin Endocrinol Met. 1998;83(5): PuMed PMID: Gross GW, Boone JM, Bishop DM. Peditric skeletl ge: determintion with neurl networks. Rdiology. 1995;195(3): PuMed PMID: Sontg LWS D, Anderson M. Rte of ppernce of ossifiction centers from irth to the ge of five yers. Am J Dis Child. 1939;58: Greulich WW, Pyle SI. Rdiogrphic tls of skeletl development of the hnd nd wrist. 2nd ed. Stnford: Stnford University Press; xvi, 256 pp. 27. Tnner JM. Assessment of skeletl mturity nd prediction of dult height (TW2 method). London/New York: Acdemic; vii, 99 pp. 28. Gilsnz V, Rti O. Hnd one ge: digitl tls of skeletl mturity. 2nd ed. New York: Springer; Suvegrin J, Nhum H, Bronstein H. Study of one mturtion of the elow. Ann Rdiol. 1962;5: PuMed PMID: Risser JC. The Ilic pophysis; n invlule sign in the mngement of scoliosis. Clin Orthop. 1958;11: PuMed PMID: Dimeglio A, Chrles YP, Dures JP, de Ros V, Kore B. Accurcy of the Suvegrin method in determining skeletl ge during puerty. J Bone Joint Surg Am. 2005;87(8): PuMed PMID: Scoles PV, Slvgno R, Villl K, Riew D. Reltionship of ilic crest mturtion to skeletl nd chronologic ge. J Peditr Orthop. 1988;8(6): PuMed PMID: Byley N, Pinneu SR. Tles for predicting dult height from skeletl ge: revised for use with the Greulich-Pyle hnd stndrds. J Peditr. 1952; 40(4): PuMed PMID: Roche AF, Winer H, Thissen D. Predicting dult stture for individuls. Monogr Peditr. 1975;3: PuMed PMID:

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