Clin Pediatr Endocrinol 1993;2(Suppl 1):9-18Copyright (C)1993 by The Japanese Society for Pediatric Endocrinology

The Tanner-Whitehouse II Skeletal Maturity Method:

Rationale and Applicability

Noel Cameron

Human Growth Research Programme, Department of Anatomy & Human Biology,Medical School, University of the W itwatersrand, South Africa

Abstract. The problem of skeletal maturity assessment is to measure, stage by stage, the

metamorphosis of the cartilaginous and membranous skeleton of the foetus into the fully ossified

bones of the adult. Whilst skeletal maturation is a continuous process its assessment requires the

identification of discrete indicators of development that are sequential, invariate between individ-

uals, universal, and that cover the full range of development from birth to full maturity. The

Tanner-Whitehouse II method is a bone-specific scoring technique in which a numerical score is

assigned to selected hand-wrist bones depending on the appearance of certain well defined

maturity indicators. The advantage of this technique over previous Atlas methods is that the

maturational differences between bones is statistically minimised thus reducing disagreement

between bones. The resulting bone maturity score is indicative of a specific maturational level in

the sample to which the bone maturity scores are compared. Whilst the TW II technique has been

applied to a variety of samples from many countries it is accepted that population and geographic

differences exist in rate of maturation and that, therefore, there is a need to develop population

specific "standards". Such national standards would allow the sensitive diagnosis and treatment

of children with growth disorders.

Introduction

The assessment of maturity is an essential

prerequisite of the diagnosis and treatment of

children with suspected growth disorders.

The achievement of a normal adult stature is

the result of the delicate temporal relationship

between rates of somatic growth on the one

hand and physical maturity on the other.

Whilst the processes of growth and matura-

tion proceed pari passu, the one with the

other, they must be clearly differentiated;

maturation is concerned with the metamor-

phosis of the biological and chemical natureof tissue, whilst growth is concerned with the

formation of new tissue. The complexity of

the interaction between growth and matura-

tion may be clearly seen in Figure 1.

This illustrates three boys and three girls

from the Harpenden Longitudinal Growth

9

Correspondence: Professor Noel Cameron, Human Growth

Research Programme, Department of Anatomy & Human Biol-

ogy, Medical School, University of the Witwatersrand, York

Road, Parktown 2193, South Africa

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CAMERON

Data: Growth at Adolescence, 1962, J.M. TannerBlackwell Scientific Publications, Oxford

Fig 1. Three normal boys aged 14.5 years and threenormal girls aged 12.5 years from the HarpendenLongitudinal Growth Study. Whilst, within sex ,th

ey are of exactly the same age they demon-strate markedly different maturational levels

Study conducted in England, between 1948and the early 1970s, by J. M . Tanner and thelate R.H. Whitehouse . The subjects wereexamined every six months until the start ofadolescence, as characterised by the first

appearance of pubic hair, and then three-monthly until adulthood. At each examina-

tion a variety of anthropometric measure-ments were taken in addition to radiographsof the hand and wrist and smatotype photo-

graphs. Figure 1 illustrates three normalboys aged exactly 14.5 years and three normal

girls aged exactly 12.5 years. It is evident

that, at the same chronological age, the matu-rationalare very different. The boy and girl on theleft are essentially pre-pubertal, those in thecentre are mid-pubertal, and those on theright are virtually adult. As we wouldexpect, the more mature individuals demon-strate greater growth as evidenced by greaterheights, greater sexual dimorphism in terms ofbody proportions, muscularity and subcutane-ous fat, and greater development of secondarysexual characteristics. Indeed the use of sec-ondary sexual characteristics to monitor therate of pubertal development is an importantclinical tool. Its use, however, is confined tothe relatively narrow age range surroundingnormal puberty. Sexual development cannotbe used to monitor the level of maturitythroughout the process of growth and develop-ment.

The skeleton also demonstrates matur-ational changes, that are only visible with theuse of radiographs, but these occur through-out the period from intrauterine life to fullmaturity. Skeletal maturation may bedivided into three phases: (1) the ossificationof the epiphyses of the long and short bones ,(2)

osteogenesis in the epiphyses of these shaft-ed and the round bones, (3) the invasion of thegrowth cartilage plates that leads to theirfunctional destruction and the bony fusion ofthe epiphyses and diaphyses . Phase (1) isalmost complete in utero and has been thesubject of a good deal of histological research .P

hase (2) begins just before birth , in themajority of bones, and is complete by puberty ,and phase (3) begins with the onset of pubertyand its completion marks the attainment offull maturity.

Rationale

The problem of skeletal maturity assess-ment is thus to measure, stage by stage , themetamorphosis of the cartilaginous and mem-branous skeleton of the foetus into the fullyossified bones of the adult [1]. This meta-

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TW II: Rationale and Applicability

morphosis, or maturation, is obviously a con-tinuous process but its assessment requires theidentification of discrete indicators of develop-ment. The conceptual realization that theseindicators, called "determinators of maturity"by Todd [1] and "maturity indicators" byGreulich and Pyle [2], could be identified anddescribed, was of immense importance to thedevelopment of skeletal maturity systems .Prior to this realization scientists and clin-cians had relied on the assessment of thenumber of ossification centres present in theskeleton, or on the planimetric measurementof the shadow cast by the ossification centreon the radiographic film [3]. Identificationand description of maturity indicators allowedthe observer to simply inspect the appearanceof the ossification centre and assess whichmaturity indicators were present.

Because the identification of maturityindicators is the basic rationale for all modernskeletal maturity systems it is worth spendinga few minutes discussing the concept of matu-rity indicators and their selection. The con-cept can be traced back to the work of MiloHellman which was further developed byWingate Todd. In 1928 Hellman published areport describing the serial changes in theradiographic appearance of the growth carti-lage plate during the process of fusion of theepiphysis to the diaphysis [4]. Todd devel-oped this work by defining and describingsuch changes in long and short bones prior tothe time of ossification of the growth cartilageplate, and later in round bones, throughouttheir period of development. He described"maturity determinators" as , "successivechanges in outline...and in contour." Greulichand Pyle [2] were later to clarify this conceptby defining "maturity indicators" as,".. thosefeatures of individual bones that can be seenin the roentgenogram...and which, becausethey tend to occur regularly and in a definiteand irreversible order, mark their progresstoward maturity." This last quotation empha-sises three important characteristics of matu-rity indicators; their regular occurrence, theirdefinite order, and the irreversibility of that

order. If maturity indicators are to be usefulthey must satisfy the following criteria; (1)they must be sequential in that the indicatorchosen to represent a more mature stage ofdevelopment must always follow an indicatorchosen to represent a less mature stage. (2)maturity indicators must be invariate in thatthey must always appear during the course ofnormal development in all children of bothsexes. It is of little use to have a maturityindicator that is only present in some childrensome of the time or, if we are to compare boyswith girls, to have a maturity indictor that isonly present in one sex. Age at menarche,whilst an extremely important and useful indi-cator of maturity, can, of course, only be usedto assess maturity in girls and is useless as acomparative maturity indicator between girlsand boys. To these criteria could be addedthe fact that maturity indicators must beclearly definable and observable. Theremust be no confusion, in the mind of theobserver, as to whether a maturity indicator ispresent or absent.

Todd [1] and Greulich and Pyle [2]pioneered the definition and description ofmaturity indictors in the hand and wrist andthe majority of their indicators are still used inboth the current Greulich-Pyle and Tanner-Whitehouse systems of estimating skeletalmaturity. An example of such an indicator,for the radius, is illustrated in Figure 2.

The illustrations on the top line are fromthe Greulich-Pyle Atlas of skeletal maturity ofthe hand and wrist [2] and those on thebottom line are from the Tanner-WhitehouseII bone-scoring technique [5]. Note thatGreulich and Pyle [2] described 11 maturityindicators whilst Tanner et al. [5] describedeight. It is apparent that, visually at least,the indicators of Tanner et al. [5] are notdramatically different from those of Greulichand Pyle [2]. Indeed it is important thatthese indicators are similar. If the two tech-niques had arrived at very different maturityindicators, within the same skeletal area, theneach system would cast doubt on the maturitydescribed by the other. The descriptions of

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Fig 2. Illustrations of maturity indicators for the Radiusas defined by Greulich and Pyle [2] and Tanneret al. [5]

the indictors are, however, different to somedegree, so it would be a mistake to assumethat the original indictors of Greulich andPyle [2] have survived intact in the Tanner-Whitehouse II technique.

The descriptions given by both systems ofmaturity assessment relate initially to theshape of the new epiphysis and then to theappearance of articular facets as radio-opaquelines. As the epiphysis matures its relation-ship to the diaphysis becomes important andfinally, in the TW II system, the initial stagesof fusion are described. Thus within thecontinuous process of skeletal maturationdiscrete events have been identified that indi-cate how far along the road to full maturitythe child has proceeded.

The next problem is to relate the passagefrom immaturity to maturity to some sort oftime scale. Wingate Todd originally did soby initiating the Brush Foundation Longitudi-nal Growth Study in which the hands andwrists of 1000 children were x-rayed at regularintervals. For each age group suitable filmsof healthy children were arrayed, one bone ata time, and the film showing the bone ofmedian maturity was selected for detaileddescription as typical for all children of that

particular age and sex. When this laboriousprocess was complete the films were re-examined in an attempt to find films thatillustrated the median stage of developmentfor every bone. This process was not whollysuccessful, for reasons we will discuss later,but films were eventually selected. The ageof the children from which each standard filmwas selected became the "skeletal age" consis-tent with the degree of maturity illustrated bythat "standard".

The Todd/Greulich-Pyle method containstwo conceptual problems. These problemshave been described by Acheson [3] as theproblem of the "evenly maturing skeleton"and the problem of the "concept of skeletal

age". The first problem relates to Todd'sbelief that illness or deprivation affected onedeveloping centre to a greater degree thananother so that each centre would reflect adifferent degree of maturity and thus have adifferent "skeletal age". The extension ofthis belief is that a perfectly healthy child willdemonstrate median development in all of itsbones. Indeed Pyle, Mann, Driezen, Kellyand Macy [6] evolved the "Red Graph" as adevice for measuring the disparities betweenbones. It is now well recognised that thisbelief is a fallacy and that, within the handand wrist of all normal healthy children, thereis a degree of dysmaturity in that some bonesare in advance of others and that the control isprobably genetic in origin.

The second problem, of relating oneskeletal year to one chronological year, centresaround the problem of the time scale.Indeed, what Todd did was to substitute feetand inches with years and months to measurea metamorphotic process. Because matura-tion is distinct from growth it requires a sepa-rate scale of measurement. Indeed the inter-est that clinicians have in assessing skeletal maturity is precisely because the rate ofskeletal maturation differs between membersof the same group of healthy children. "Theskeletal year", as defined as one chronologicalyear of the sample of American children inves-tigated by Todd, does not in fact have the

13

TW II: Rationale and Applicability

same meaning for any two healthy childrennor indeed for two bones in a single healthy

child. In ill health, or in a child with a

growth disorder, the concept of one skeletalyear equalling one chronological year may beeven more distorted. In addition it has to beremembered that (1) females mature at a fas-ter rate than males and thus acquire more

maturity indicators within the same chrono-logical time scale and (2) skeletal maturation

does not proceed at a constant rate through-out the period of development. The secondfactor means that within a single sex the rate

of maturation in a skeletal year depends onthe age of the child, e. g., in boys the thir-teenth skeletal year represents much morematuration than the sixth (3).

The Oxford Method

These conceptual problem in the Atlastechniques prevented their further develop-ment. To overcome these problems it wasnecessary to develop a skeletal maturity sys-tem that was independent of age. Acheson[7] was the first to develop a bone scoringtechnique that did not require considerationof the size of the bone and was independent ofchronological age. In essence, he identifiedmaturity indicators and assigned scores rang-ing from 0, when no centre was present,through 1 for the initial appearance, 2 for aclear shape, and so on until full maturity. Bysumming the scores for each bone he arrivedat a bone maturity score. He decided thatthis total maturity score should bear a linearrelationship to age and thus used a weightingsystem to achieve this end. Of importancewas the fact that if the unweighted scores weresummed they demonstrated a curve that wasnot too dissimilar from the curve for growth inheight.

Indeed these curves clearly demonstrateda sex difference in skeletal maturation andtheir derivatives (velocity) demonstrated aclear adolescent growth spurt. The problemof this technique, called the "Oxford Method"

by Acheson [3], is that it does not deal withthe problem of dysmaturity in that similartotal scores from different individuals may bethe result of the maturity of different bones.

The Tanner-Whitehouse Method

Tanner, Whitehouse and Healy in 1962[8], and in subsequent publications over thenext 25 years, developed the bone-scoringtechnique known as TW I which was laterupdated to TW II.

The underlying rationale of the Tanner-Whitehouse techniques was based on dissatis-faction with a maturity system based onchronological age and thus the need to definea maturity scale that does not refer directly toage. The result of such a system would bethat in any particular population the relation-ship between maturity and age could be stud-ied and "maturity standards", similar toheight or weight standards, could beproduced.

Concentrating on the bones of the handand wrist, they defined series of eight matu-rity indicators for each bone and nine for theradius. (As with the Oxford method, thesesamoid bones were ignored.) These matu-rity indicators were then evaluated, not inrelation to chronological age, but in relationto their appearance within the full passage ofeach specific bone from immaturity to matu-rity. Thus, for example, it was possible tosay that a particular indicator on the lunatefirst appeared at 13% maturity and that aprocess of fusion in the first metacarpal start-ed at 85% maturity. In addition Tanner andhis colleagues were of the opinion that thematacarpals and phalanges, being greater innumber than the carpal bones, would weightthe final scores in favour of the "long" bones;they therefore omitted rays 2 and 4 from thefinal calculations. Further they weighted thescores so that half of the mature score derivedfrom the carpal bones and half from the longand short bones. The scores were so propor-tioned that the final mature score totalled 1000

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points. 5000 radiographs of normal Britishchildren were then rated, using this technique,

to arrive at population "standards" that

related bone maturity scores to chronological

ages. Like the curve for unweighted scores in

the Oxford method the resulting curve of bone

maturity score against age was sigmoid

demonstrating a non-linear relationship

between skeletal maturity and chronological

age.

Acheson [3] notes three objections to TWI. Firstly some of the maturity indicators

involved the assessment of size relationsbetween bones which may be altered by path-ological conditions and thus violates therequirement of universality in the selection ofmaturity indicators. Secondly, Acheson feltthat by constraining the number of maturityindicators to eight, Tanner et al were weaken-ing their system by of necessity ignoring thefact that some bones may exhibit greater orfewer maturity indicators than the eightrequired by the TW I system. Thirdly, thecontribution of the carpus to 50% of totalmaturity presents a problem in terms of therepeatability of assessing maturity indicators(i.e., the carpus is less reliable) and becausethe carpus is known neigher to play a majorrole in growth in height nor in epiphysealfusion.

Tanner et al [8] took cognisance of thesecriticisms in their development of the TW IIsystem which is in general use today. Theydid not change the maturity indicators butthey changed the scores assigned to the indi-vidual bones to allow the calculation of a bonematurity score based on the radius, ulna andshort bones (RUS) only or the carpal bones(CARPAL) only in addition to the full 20-bonescore.

The mathematical rationale for the TW

systems is of considerable importance. The

problem with the Oxford technique was that

assigning scores of 1, 2, 3,...etc., to the appear-

ance of maturity indicators does not allow for

the fact that changes from one maturational

level to another may be very different in

different bones. Tanner and his colleagues

Data: The Assessment of Skeletal Maturity and Predic-tion of Adult Height, 2nd Ed. 1984J.M. Tanner, R.H. Whitehouse, N. Cameron, W.A.Marshall, M.J.R. Healy and H. Goldstein Aca-demic Press, London

Fig 3. Two alternative systems of scoring bone matu-rity that demonstrate the use of minimizing thedifferences between bones

felt that (1) the development of each bonereflects primarily a single process defined asmaturation, (2) the scores from each of thebones in a particular individual should, withsuitable standardization, be the same and thiscommon score would be the individual'smaturity. In practice the scores of the vari-ous bones are not identical, one of the mostimportant reasons being the large gapsbetween successive events in a single bone.Tanner et al [8] therefore defined the scoresin such a way as to minimize the overalldisagreement between the different bones.Firstly, the disagreement in a particular indi-vidual is measured by the sum of squares ofdeviations of his bone scores about their meanvalue and secondly, the scores are constrainedto avoid the solution in which perfect agree-ment is reached by giving the same score toevery stage.

Figure 3 illustrates this procedure. Tworival systems of scores are illustrated, labelledL and M, and the stages for three bones in aparticular individual. Regardless of whethersystem L or M is used the resulting mean value

15

TW II: Rationale and Applicability

is 9. The disagreement between the bones is,however, greater for system L than for systemM when measured by the sum of squares ofdeviations about the mean; 146 for system Land 42 for system M. Tanner et al [8] gener-alized this by using all the bones and all thestages and by adding up the total disagree-ment sum of squares over all members of alarge standardizing group. The systemproducing the overall minimum sum ofsquares of deviations is the preferred one.The mathematical basis of the system is com-plex but may be studied in Tanner et al [5] orHealy and Goldstein [9].

The Tanner-Whitehouse II skeletal matu-rity system thus addresses the disadvantagesof both the Greulich-Pyle Atlas method andthe Oxford method. It allows an assessmentof skeletal maturity which is age independentand which, because of the three systems avail-able from a single rating (TW II 20, RUS,CARPAL), allows considerable flexibility bothin the assessment and monitoring of skeletalmaturity. It is not surprising that consider-able research has been undertaken to assessthe skeletal maturity of different populations.

Applicability

Rates of skeletal maturation reflect theinteraction of both environmental and geneticinfluences. It is therefore to be expected thatpopulations will differ both in mean skeletalmaturity at a given age and in the pattern ofincrements from one age to the next. It istherefore desirable to develop specific stan-dards for each relevant population. Thispresents no problem in the TWIT scoringsystem in which the maturity score can berelated to the age of any particular sourcesample, but is a considerable problem in abone age technique in which maturity ismeasured against the original source. It isquite possible, for instance, when using theGreulich-Pyle Atlas technique, to arrive at theconclusion that, "...a child of 12.0 years, witha GP bone age of 11.0 years is six months

retarded" because his population mean isalready 6 months behind the atlas.

A variety of studies during the last 20years have reported on samples from Switzer-land, Holland, Finland, Denmark, Germanyand Sweden. Some of these samples weredelayed but others were of similar maturity oradvanced in relation to British norms. Ofsignificance is that some studies have demon-strated that secular trends for acceleratedmaturity have meant that samples that wereorginally delayed in relation to TW II normsare now advanced. Thus changes in the asso-ciation between populations over time are anaccepted characteristic of maturity assess-ments using the TW II system.

The skeletal maturity of Japanese chil-dren has been extensively studied over the last20 years using the Greulich-Pyle, TW I and

TW II techniques. Specifically, studies havebeen conducted using the Greulich-Pyle Atlason children from Hiroshima, Aichi andNagano. The TW I method has been usedon children in Tokyo [10-12], Kyushu [13]and Okinawa [14]. The TW II method hasbeen used on Tokyo children [15], Sapporochildren [16] and children in Western Kyushu[17].

The general findings from the TW I andTW II assessments are of delay relative toBritish norms prior to adolescence and then ofrelative advancement [17]. Figures 4 and 5demonstrate that Japanese children fromTokyo, investigated by Kimura [15], are rela-tively advanced from early adolescenceonwards when compared to samples fromDenmark, Canada and India. Thephenomonon of delay followed by advance-ment may be clearly seen for RUS bone matu-rity scores of 500 boys and 485 girls fromNomozaki, Western Kyushu investigated byTakai and Akiyoshi [17]. Similar paternswere found for CARPAL and TW II 20 bonescores although there are some differences inthe age at which different samples of Japanesechildren reach the maturity level of Britishchildren. In published reports this can beanywhere between 7 and 12 years in boys and

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Data : Eveleth & Tanner, 1990

Fig 4. A comparison of TW II (20) skeletal age forsamples of boys from Denmark, Canada, Indiaand Japan

5 and 8 years in girls [17].There are also differences within

Japanese populations. Comparisons byTakai and Akiyoshi [17] of children fromTokyo, Sapporo and Nomozaki demonstratedthat, in general, Tokyo children were moreadvanced than their peers from Okinawa andNomozaki.

Figures 6 and 7 compare the bone agedata from Tokyo [15] and Nomozaki [17]with the British norms. Whilst both groupsclearly show an initial delay followed byadvancement compared to the British theTokyo children are consistently advanced rel-ative to the children from the less urbanNomozaki. Such differences in maturity arealso supported by differences in somatic

Data : Eveleth & Tanner, 1990

Fig 5. A comparison of TW II (20) skeletal age forsamples of girls from Denmark, Canada, Indiaand Japan

growth amongst the Japanese. Kanto chil-dren (including Tokyo) for example, weretaller than Kyushu children (including Nom-ozaki) according to School Health Statisticsfrom 1978 [18]. Interpretations of these find-ings are complex because of the differenttimes at which the samples were measuredand the resulting effect of the secular trend forincreasing heights and weights over time.However, it would seem that rural childrenrepresented by the Nomozaki sample aredelayed compared to their urbanized peersfrom Okinawa and Tokyo.

The fact that there are clear differencesbetween the maturartion rates of Japaneseand British children raises the question ofwhether Japanese National standards for

17

TWII: Rationale and Applicability

Data: Kimura, 1977a;Takal & AkIloshl, 1983

Fig 6. TW 11 (20) skeletal age for boys from Tokyo andNomozaki

bone maturity scores should be developed.There is little doubt that the authors of the

TW II system were in favour, and indeed,encouraged the development of nationalnorms. One of the major advantages of the

TW II technique is that, because it is a bonescoring technique, and does not rely on corn-

parisons to existing maturity standards, thebone maturity scores can be related to anyrepresentative sample of radiographs from

normal children. The result of such an exer-cise is a national standard against which the

skeletal maturity of a child can be sensitivelycompared. Such a standard would havemajor advantages over British standards in a

clinicial setting in which a sensitive assess-ment of skeletal maturity was required to

diagnose abnormal growth and monitor treat-

Data : Kimura, 1977a;Takai & Akijoshi, 1983

Fig 7. TW II (20) skeletal age for girls from Tokyo andNomozaki

ment.

Acknowledgements

The work of the Human Growth Research

Programme is financially supported by the

Senate Research Committee of the University

of the Witwatersrand, the South African

Medical Research Council and the Foundation

for Research Development and is dedicated to

a post-apartheid, non-racial, democratic

South Africa.

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