PATTERNS OF SKELETAL DEVELOPMENT IN THE HAND

(1)

PATTERNS

OF

SKELETAL

DEVELOPMENT

IN

THE

HAND

886

PEDIATRICS, November, Part II, 1959

S. Idell Pyle, Ph.D., Robert B. Reed, Ph.D., and Harold C. Stuart, M.D.

INTRODUCTION

T

HE PRECEDING paper in this series has

provided much background for this

re-port which deals with skeletal development.

Like others in this series, it is based on

individual case studies started at the

Har-vard School of Public Health in 1930 by one

of the authors (H.C.S.) and continued until

the collection of data on the children

sub-sequently enrolled was completed in 1956.

These studies were conducted throughout

by a staff representing several disciplines

and such a staff is continuing the evaluation

of the extensive records in hand. A

Mono-graph published in 1939k gave in detail an

account of the technical procedures

estab-lished during the early years for the

secur-ing of roentgenograms, many of which were

continued throughout.

The present paper deals only witil

“skele-tal age (hand)” as determined from

roent-genograms, hereinafter referred to as

radio-graphs. It is based on the study of 133

chil-dren, 66 boys and 67 girls, referred to in this

and other papers as the Maturity Series,*

who were followed periodically from birth

to their eighteenth year. Radiographs of the

hand were taken on these children in

con-nection with all scheduled examinations

be-tween 1 and 18 years. Films from larger

samples of children followed similarly from

birth for shorter periods are available but

are not considered in this paper.

Radio-graphs of other centers of skeletal growth

also are available for the same children at

the same ages and will permit studies of the

degree of symmetry or uniformity in

pat-terns of skeletal maturation in the foot and

other areas.

The reasons for seeking further basic

in-* Films of the hand of one additional boy in

this series were not available for assessment after the standard of reference’ selected for this Study was published.

formation as to the progress of skeletal

maturation in children are becoming

in-creasingly clear. This is particularly true in

respect to differences between children in

their developmental levels and rates of

prog-ress at successive age periods. It is known

that children differ greatly in the age at

which they reach any given developmental

step or stage of maturity and in the speed

at which they progress from one to another.

Information as to the latter is meagre

be-cause it can be obtained only by repeated

observations of tile same children at

succes-sive ages. It is recognized also that the

indi-vidual manifestations of a child’s level of

de-velopment in its various aspects and

suc-cessive stages are often more consistently

related to each other than to group norms

for chronological age.2 The interpretation of

findings which relate to the growth and

de-velopment of individual cilildren is often

difficult, if those findings are considered

only in terms of the child’s chronological

age. They may be more readily understood

if they are related, instead, to the child’s

stage or level of development. This has been

found to be especially true during the

period when early adolescent changes begin

to manifest themselves.

The principal objective of tilis report is to

demonstrate the types and amounts of

vari-ability between children, as well as

tue

con-sistencies manifest by individuals in the

course of the skeletal maturation of the

hand. Later publications dealing with

inter-relationships between given patterns of

skeletal development and various other

as-pects of growth, development and health

will illustrate further the value of knowing

more about the varieties of patterns of

skele-tal development and the differences in

de-gree of overall uniformity which occur in

tile development of individuals.

(2)

each of 133 children according to their rate

of progress in “skeletal age (hand)” or

changes in rate with age as compared with

the norms of this group. Having identified

tile various patterns followed by individual

children, those whose curves were

suffi-ciently similar in shape to conform to a

de-fined patterii have been grouped together

and the numbers conforming to each group

have been tabulated. The characteristics of

each child’s progress are reflected in the

shape or pattern of the curve produced

\vilen his skeletal ages (hand) have been

plotted against chronological ages.

PROCEDURES FOLLOWED IN THE

ASSESSMENT OF RADIOGRAPHS

During the early years of this project the

radiographs of the hand were evaluated by

V. Vickers using the provisional maturity

in-dicator scale prepared by T. W. Todd for the

White House Conference of 1930. The method

adopted was to compare each film with the

standard for age nearest to that of the child’s

chronological age when the film was made. In

a report b \‘ogt and \‘ickers in 1938,

draw-ings of three levels of skeletal development

of the hand and foot and of selected maturity

indicators used to identify the level of

develop-ment of individual l)ones were presented for

each sex at each age studied. Later Vickers

(Harding) modified her methodology, assigning

each film to 1 of 6 categories of level of

ad-vancement based upon chronological age. The

description of this method and the results of

her studies were published in 1952. It was

found that a high percentage of children

main-tained the same or next adjacent rating, as

determined at 2-year intervals, from birth to

10 years. The number of cases available at that

time did not permit presenting distributions

of the ratings for each age.

Since 1949 all radiographs of all children

from birtll to 18 years have been evaluated in

accordance witil the method of skeletal

ma-turity assessment described by Greulich and

Pyle in their Atlas first published in 1950 and

recently revised.6 This method represents an

extension of One originally demonstrated by

Todd in au Atlas published in 1937. in 1955

Pyle and Hoerr published an Atlas applying the

same method to the assessment of radiographs

of the knee8 and a similar Atlas by the same

authors for use in assessment of the foot is

now in preparation for pubiication.*

The fact that all assessments in this Study

were made by the same person using the same

techniques helps to insure the uniformity in

the procedure followed from age to age and

from child to child and the comparability of

the assessments themselves. The method

con-sists first in assigning a “bone age” to each bone

growth-center visible in the radiograph. This

assignment is on the basis of the presence in

the center of specific morphological features

which indicate its developmental status. These

features, the so-called “maturity indicators,” are

pictured seriatim in the Atlas,6 together with

numbers of the standard plates in which the

indicator is seen. The method involves also

assigning a skeletal age to the hand as a whole,

based upon the bone ages of each relevant

cen-ter and on a comparison of the hand as a whole

with the standard radiographs reproduced in

the Atlas.

Each film of a child under study by this

method is compared with the standard films

from which two or three consecutive standard

films are selected as being closest to and

bound-ing the apparent developmental level of the

film in question. If the skeletal development

of the hand-film to be assessed does not

cor-respond exactly to that of any one of the stand-ards with which it is being compared, a skeletal

age appropriately intermediate between the

two standards which it most closely resembles

can be assigned to it. Thus, the “skeletal age”

assigned to a hand-film is not an arithmetic

average of the separate bone ages. It represents

rather a judgment as to the overall stage of

de-‘elopment of the region, taking into account

the symmetry or lack of symmetry of

develop-ment in the various centers. In many cases

there is little or no difference between the

“skeletal age” thus assigned and the average of

the “bone ages.”

The major difference between the two

pro-cedures lies in the importance attached to the

“bone age” of centers which are in the early

* Acheson’#{176} has described a basically different method for assessing skeletal maturity which

pro-vides a numerical score rather than a bone age or

skeletal age to represent the developmental status revealed in any radiograph. This procedure is

com-monly referred to as the “Oxford Method” to

(3)

stages of ossification. Variations betwen

chil-dren in age of first appearance of centers of

ossification are far wider than they are at later

stages of their development. This suggests that

at the time of onset of ossification a center is

subject to influences which may temporarily

af-fect its rate of development, but which may not

affect the process of osseous development

gen-erally. Under these circumstances, assigning the

same weight to a very immature center as to

more mature ones may result in an erroneous

appraisal of the child’s skeletal development.

Consequently, the practice which was followed

was to assign less weight to the bone ages of

very immature centers than to that of those

centers which were farther advanced in their

development.

In only a few instances in this Study was the

complete series of films of a child assessed in

its entirety at one time. The more common

pro-cedure was to assess only a few films of a series at one time and to assess others subsequently.

None of the skeletal ages used in this paper

were re-assessments or corrections made after

the original skeletal ages were assigned.

Al-though occasional corrections on re-assessments

might have been appropriate, this rule was

adhered to in order to assure that each skeletal

age assigned was based objectively on the

radiograph alone. Re-assessments, however,

were made from time to time, even though the

new values were not used. The authors believe

that such periodic checking for reliability by

re-assessment is essential to assure consistency

by any single observer and has helped greatly

to keep biases to a minimum.

DISTRIBUTION OF SKELETAL AGES BY

SEX AND CHRONOLOGICAL AGE

After each child’s series of radiographs

had been assessed, the mean and standard

deviation were calculated for the boys and

for the girls at each age. These values are

shown in Table I. They provide measures

of the central tendency and variability in

skeletal development for this group of

chil-dren. Graphs of the values of the means and

1 standard deviations are shown in Figure 1,

which is presented primarily to permit

recognition of differences in this particular group.

The numbers of infants for whom values

for the mean and standard deviation are

given in Table I at ages 3, 6 and 9 months

are considerably less than 66 boys and 67

girls in this Study because in their early

years radiographs were not made at these

ages. The number of males contributing to

the group values at ages fiom 1 to 16 years

and of girls 1 to 13 years, inclusive, differ

only slightly from the expected number, the

differences representing missed exam

na-tions. It is an indication of the

complete-ness of these case studies, of 66 boys

sched-uled for 21 examinations between 1 and 16

years, inclusive, no boy was missed at five of

the scheduled ages and at no age were more

than four missed. Of the total possible

ra-diographs of boys at these scheduled

ex-aminations only slightly over 1% were

missed. Similarly, out of 18 scheduled

ex-aminations for 67 girls, ages 1 to 13 years

inclusive, at eigilt ages no examination was

missed and at no age were more than two

missed, with the result that kss than 1

of the total possible radiographs of the

hand were missed.

The number of boys and girls included

in Table I decreases after 16 years for boys

and 13 years for girls. This is not primarily

because radiographs are unavailable, but

rather because advanced individuals had

attained skeletal ages at or so near to the

mature (i.e. upper) end of tile standard

that they could not be used in computing

these statistics. For example, a girl who had

attained a skeletal age of 18 at 14 years

would be fully mature in this aspect of the

hand at 15, 16, 17 and 18 years. Therefore,

these advanced cases were omitted from the

calculations after the last age at which they

could be used for these statistics.

The numbers of individuals included in

Table I are sufficient at all ages through 15

years for girls, and 17 years for boys, to

ob-serve the nearness of the means to the

standard of Greulich and Pyle.6 At these

ages, osseous stage of development in the

hand is nearing completion. Comparing the

mean values, which are expressed in

months of skeletal age, with the

chronologi-cal ages in months gives an indication of

(4)

18H

Boys Girls

H - Mean

161 Mean ±

14

l2

OH

8H U) 0

w

>-w ‘5

-J ci

I-w

-J

w

(I,

/

6

2H

0

- J L I I

2 4 6 8 10 12 14 16 18

CHRONOLOGICAL AGE (Years)

Fic. 1. Values for the mean and 1 standard deviation for “skeletal age (hand)” plotted against chronological age for boys and girls derived from Table I.

boys and girls and the groups on which

the standards were based. It may be noted

that for boys tile mean ages, as given in

Table I, were slightly ahead of the

stand-ard at each age from 3 months to 1 year,

inclusive, and from H years through 17

years. In contrast, they were always at or

behind the standard during the intervening

period, 18 months to 10 years. The amount

of advancement during the first year was

never a full month and from 11 to 16 years

was never more than 1 month, only at 17

years reaching 2 months. In the intervening

period, however, it was somewhat delayed,

being 4 months behind at each age from

4% to 9 years, inclusive. For girls, the means

were always somewhat behind from 2

through 10 years, and thereafter always

ahead except at 18 years. It is believed that

the differences shown in these Figures are

attributable to the composition of the

re-spective samples and not to personal

differ-ences in the appraisals, as discussed

previ-ously. Tile indications are that the sample

as a whole was somewhat advanced over

the standard in infancy, became relatively

delayed for most of childhood and then

became advanced in adolescence. However,

at no age are these differences in

them-selves statistically significant. As would be

expected, the standard deviations shown in

Table I increase gradually with age until

full skeletal maturity in the hand is being

attained by more and more children. These

features of the values for this group of

chil-dren are shown graphically in Figure 1.

Figure 2 is constructed as in Figure 1,

but gives only the norms for boys as

back-ground for the presentation of the “skeletal

age (hand)” curves for 4 boys in this series.

Boys 253 and 130 show very consistent

po-sitions throughout the whole age period in

relation to the standard. Yet they are far

apart, 253 always being very advanced

while 130 is usually delayed more than 1

(5)

BOYS

Mean ±

a-Contrasting Cases

253

-188 -133

-130

18

16

-14

-12

-10

-

8-

6-4

2-U) 0 a,

>-Ui

ci

-j

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1-Ui

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(I)

0 2 4 6 8 10 12 14 16 lB

CHRONOLOGICAL AGE (Years)

Fic. 2 Values for the “skeletal age (hand)” for four boys plotted against

chrono-logical age and against values for the mean and 1 standard deviation for the

boys in the “Maturity Series.” The boys represent selected patterns, namely, consistently “advanced,” consistently “delayed,” “fast” to “slow,” and “slow”

to “fast.”

I I I I I I I I I I 1 1 1

890

contrast, change positions markedly with

age. Both start in infancy well within the

range and end at 17 years close together

near the mean. They become far apart in

the intervening years, at 9 years of age

being separated by 53 months in

skeletal-age ratings, 188 being far above the +1

sigma and 133 below the -1 sigma. In the

classification to he discussed below, case

188 has been assigned to a fast-slow pattern

and 133 to a slow-fast one, which terms

describe their essential differences in rates

of progress. Cases 253 and 130, on the other

hand, belong to the same pattern, that of

moderate rate throughout, which in these

cases is expressed at widely different levels

of skeletal age. These cases have been

se-lected to show how different patterns of

progress relate themselves to the

conven-tional type of Figure. Subsequent Figures

will present patterns of progress in a

differ-ent manner to enable the reader to identify

more readily tile characteristics of tile rate

of progress of different individuals by age

periods and their attained levels of

ad-vancement at different ages.

THE CLASSIFICATION OF INDIVIDUALS

BY THEIR MANIFEST PATTERNS OF

SKELETAL DEVELOPMENT IN

THE HAND

The classification of the children

con-sidered in this report is based solely on the

“skeletal ages” assigned to them.* The

se-Studies have been macic on this series of chil-dren by one of the authors (Pyle) of the assigned “bone ages” and the varying “spans” between them in terms of chronological age. Consideration also has been given to the irregularities in the

(6)

891

lection of the most satisfactory method for

classifying curves according to prescribed

patterns has been difficult because of the

variety and shadings of individual

differ-ences. The method selected has the

ad-vantage of limiting the number of possible

patterns to workable limits for charting,

re-porting and studying interrelationships, yet

it permits application of rules which can be

followed with reasonable precision and

leaves few children who must be excluded

as irregular or unclassifiable. The authors

believe that the patterns selected are

ade-quate to reveal sharply contrasting courses

of skeletal development followed by

mdi-viduals and to indicate their relative

fre-quencies in the two sexes.

Method of Identifying Patterns

The first step in identifying and selecting

patterns and assigning cases to them was to

plot all values for skeletal age for all individuals

in the Maturity Series on separate graphs. The

form of graph used will be described more

fully in the presentation of the Figures which

follow. The 0 line on this graph represents the

standard of reference of Greulich and Pyle.

Months of skeletal age advancement are plotted

above, and of delay below, this line. The values

for the mean and 1 standard deviation for tile

sex to l)e represented by the grapil, derived

from the values in Table 1, are plotted

verti-cally against chronological age in years.

Classi-fication of these cases is based upon

compari-son of tile cilild’s curve with the lines

represent-ing the means and standard deviations of this

group of children. With the standard-range

graphs in hand each case has been plotted on

a separate one for its appropriate sex. In

ap-plication, the means and standard deviations

hands of individuals at succeeding ages. Also, the concept of the most advanced versus the least

ad-vanced center has been applied according to a

procedure previously described” by her and Some

study has i)ecn made of the extent of variability in

the progress of individual centers, and hence of

their relative predictive values. Reports of these studies irnist await their further application ad analysis.

Pyle has discussed existing standards of reference

constructed somewhat as were the Atlases of Todd

and of Greulich and Pyle and pointed out the

similarities as well as differences between them.”

shown in these Figures were not drawn on each

chart, but rather on fitting-transparencies which

were used as overlays when assigning each case

to its appropriate pattern. Rules were adopted

governing the limits of variability on the part of any case for it to be assigned to a pattern.

The second step was to study the graph of

each case, using the norms on the overlay as

the lines of reference, and to record rates or

changes in rates by age periods as “moderate,” “fast,” “slow” or “irregular.” Levels of

advance-ment were also recorded under this step but

these ratings were not used in the final

selec-tion of patterns. As a result of this appraisal,

a list of permissible patterns was drawn up and

the following plan for sorting of cases and

as-signment of each to a pattern was adopted. The

age period used for the selection of patterns has

been from 1 year to 17 for boys and to 15 for

girls, for which satisfactory norms are available.

Skeletal ages available for chronological ages

below and above these limits have been plotted

but not taken into account in applying the rules

governing pattern assignment. Not only are

the norms considered inadequate for

classifica-tiori at these ages, but many of the centers of

growth in the bones of the hand are still

en-tirely cartilaginous at the initial stage and

abruptly become fully mature at the terminal

one. Irregularities in these complicate and

con-fuse appraisals of the pattern during the long

mid-portion of the postnatal osseous stage of

development.

The third step was to select and classify a

group of patterns which appeared to be

realis-tic and adequate on the basis of a preliminary

survey of the rates assigned to cases. A single

assignment of a rate applicable to the whole

age period being studied was made when

pos-sible under the rules, but this classified only a

minority of the cases. Further study showed

that a considerable number of curves differed

in rate in two periods, that is the curves were

dichotomous. The cases not fitting the first

screening were therefore rescreened separately

for two periods. A third screening was then

carried out Ofl the remaining cases to select

those which were trichotomous in respect to

rates of progress. Tllese three procedures

to-gether made it possible to classify most cases

according to their patterns of progress and the

few remaining were assigned to irregular

cate-gories. The procedures followed are described

(7)

TABLE I

MEANS AND STANDARD DEVIATIONS FOR SKELETAL AGE (HAND)

-1ge

(month.,)

Boys

(years) No. Mean

‘Standard Deviation Girls .l!ean No. Standard Derial ion 3 6 9 18 124 so 36 412 48 54 60 66 712 84 96 108 l12() 1312 144 156 168 180 1912 1204 1216 I 12 3 4 .5 6 8 10 14 16 18 43 47 46 66 67 67 67 67 67 65 64 64 64 66 66 63 63 63 65 64 66 65 65 65 60 37 3.4 6.5 9.7 112.7 17.5 1212.6 128.1 33.8 39.5 44.8 50.3 56.12 612.4 68.4 80.6 912.5 104.9 118.0 1312.1 144.5 156.4 168.5 180.7 193.0 1206.0 12112.8 1.7 12.0 12.4 ‘2.1 12.7 4.0 5.4 6.0 6.6 7.0 7.8 8.4 9.1 9.3 10.1 10.8 11.0 ll.4 10.5 10.4 11.1 112.0 14.12 15.1 15.4 112.12 50 50 53 65 66 66 65 66 66 67 67 67 67 67 67 67 67 66 66 66 66 63 61 57 47 ‘212 12.9 5.9 9.5 112.7 18.4 ‘23.7 129.0 34.5 40.6 46.4 512.3 58. 1 63.9 70.4 812.0 94.0 105.9 119.0 1312.9 147.12 160.3 17’2 .4 184.3 196.7 ‘205.1 ‘211.5 1.1 1.7 12.1 ‘2.7 3.4 4.0 18 5.6 6.5 7.12 8.0 8.6 8.9 9.0 8.3 8.8 9.3 10.8 112.3 14.0 14.6 112.6 11.12 10.6 8.12 5.6

Selection of Patterns and

for the Assignment of Cases

Rules Adopted

The letters (f) to denote “fast,” (m) “moder-ate” and (s) “slow” have been used throughout to classify rates by age periods, using the letter

(i) to denote “irregularity” during periods in

which a case fails to conform to one of the

primary rates. Cases within any rate category

may be predominantly advanced, moderate or

delayed in level of attained skeletal age, but

change in level only is considered, using it as

a measure of the rate which determines it. To

be “moderate” in rate, according to the rules

adopted, all skeletal ages for the individual

dur-ing the period being assigned a rating must

re-main within a zone limited by the spread of 1

standard deviation, except that single, more

irregular points bounded by regular ones may

be ignored. Occasionally 3-point smoothing has

been allowed when irregularities in adjacent

points have made recognition of changes in

rate or assignment of appropriate rate difficult.

For a rate to be described as “fast” for the

whole age period the curve must rise at least

1 full standard deviation between the

begin-ning and end of its course. Similarly, to be

“slow” it must fall to this extent.

Findings

All cases have been initially classified in

the preceding manner for the whole age

pe-riod, that is 1 to 17 years for boys and 1 to

15 for girls. This will hereafter be referred

to as Screening I. It provides three possible

patterns: I m (moderate rate throughout);

I f (fast rate throughout); and I s (slow

throughout). As a result of this first

screen-ing, it was found (Table II) that 17 boys

and 18 girls fitted one of these,

predomi-nantly pattern I m. However, many of the

(8)

* 1= first screening on basis of total age period studied. 11= second screening on basis of dichotomy of age periods.

III = third screening on basis of trichotomy of age periods.

IV

= irregular cases.

f=fast rate.

m = moderate rate.

s= slow rate. r= regular.

= irregular. ** Films of hand of one boy not available.

Under patterns in the III category a change in rate was required to establish a pattern. Therefore, none are

listed in which the rate was the same during what might be viewed as first and second, or second and third, periods. Ally cases possibly falling in these categories will be found in group IV.

893

TABLE II

DISTRIBuTION OF CASES BY PATTERNS FOR Boys AND Guns

Pattern Identzfication* Number of Boys % Number of Girls %

Im

If

Is

13 0 4

14 3 1

Totals assigned in first screening 17 126 18 127

11sf lIsm Ilinf

IIfs IIfm lIms

6

3 7

3 0

5

8 3 8

3 0 4

Totals assigned on basis of two age periods ‘24 36 ‘26 39

Illmfin fmf

IIImsm sms

IIIsmf

sfm IIImsf

fins

III fsm infs IIIfsf

sfs

12 0

3

0 4

3

1 1 0 1 0 4

‘2 0

3 0

1

0 1

(

12

C 1 1

Totals assigned on basis of three age periods 19 ‘29 11 16

IV ri (irregular in second period only) IV ir (irregular in first period only) IV ii (irregular in both periods)

1 12 3

‘2 4 6

Total irregulars 6 9 112 18

GRAND TOTALS 66** 100 67 100

truly “irregular” but changed rate

some-where near the middle of these years or

about when factors associated with

begin-ning adolescence might be operative.

It was, therefore, decided to apply a

sec-ond screening, to be referred to as

Screen-ing II, to all cases rejected under

Screen-ing I, in the same manner as in Screening I

but separately for two age periods. The

first period by the definition adopted

ex-tends from 1 year to any age between 6%

(9)

SKELETAL DEVELOPMENT

boys. The second period covers the

remain-ing years. These limits were selected

arbi-trarilv with the intent of making the 2

pe-riods as nearly as possible the same

(level-opmentally for boys and for girls and to

provide sufficient range for each sex to

cover tile same developmental stage for

most early and late maturing children. In

outcome it appears that any extension of

these age limitations would not have made

it possible to add more than one or two

cases to the two age-period patterns. For

a rate to be described as “fast” or “slow” in

either age period it must change #{190}of 1

standard deviation from beginning to end

of period. This screening permitted six

pos-sible patterns, identified in Table II as II

sf, II sm, II mf, II fs, II fm and II ms; 24

boys and 26 girls fitted one of these

pat-terns, the number in each being shown in

Table II.

After further observation of the shapes

of the curves of the 25 boys and 23 girls

who failed to fit any pattern under

Screen-ings I and II, it was decided to make a

third screening (Screening III) of them on

the basis of a trichotomy of age periods,

referred to as “first,” “middle” and “last.”

No age limits were set for demarking these

periods because no sound basis for doing

so was apparent, but at least four

contigu-ous skeletal-age assessments have been

re-quired to fit a changed rate to permit

as-signment to a new rate category, and the

change need be only % standard deviation

if the trend of the curve clearly indicates a

change in the category of rate of progress.

The 12 possible patterns under this

screen-ing for change in rate between three

sepa-rate periods is shown in Table II. The

pre-fix III refers to the third screening and the

three letters following, as in tile previous

screening, to the rate assigned in order to

each of the periods; 19 boys and 11 girls

were found to fit one or other of these

pat-terns.

There remained, after carrying out these

three screening procedures, 6 boys and 12

girls whose graphs did not fit an)’ of the

possible patterns. It was found that some

of these were “regular” in the first of the

two periods used for the second screening,

hut were “irregular” during the second

pe-riod. In other cases the reverse was true

and, in the remaining, irregularities

oc-curred in both periods. Hence, in Table II

three categories of cases are listed as IV ri,

IV ir and IV ii, “r” being used as the code

letter for “regular” and “i” for “irregular.”

One boy and 2 girls were found “regular”

in the first period and “irregular” in the

second, whereas 2 boys and 4 girls were

“irregular” in the first and “regular” in the

second; 3 boys and 6 girls were “irregular”

in both periods.

After making assignments of all cases to

one of the patterns or categories described,

it was recognized that, within the limits of

irregularity allowed under the definition of

patterns, there are several cases which

show minor swings over short periods of

slower or faster rate with recovery of

for-mer status. These may prove of interest in

later studies of interrelationships. It may

be that occasional cases assigned to one of

the regular patterns represent more marked

or prolonged swings which caused them to

fit a pattern which does not truly represent

their intrinsic one. As an example, a case

assigned to I s might basically represent

I m, but delayed in the second period.

Some of these and other aspects of

indi-vidual differences will be discussed in

con-nection with the case examples of patterns

plotted in the Figures whicll follow.

DISCUSSION

Table II gives the number of boys and

of girls assigned to each of 21 possible

pat-terns under the classification adopted. It

shows that no case was assigned to three of

these patterns, that is, II fm, III fmf and

III sms. In addition no boy fitted patterns

I f, III fsm or III fsf, and no girl fitted III

sfm, III fms or III mfs. If patterns to which

not more than two children conformed

(boys and girls combined) were to be

dis-regarded, five more of the hypothetical

pat-terns would be omitted, accounting

(10)

PATTERN I m BOYS #{149}300 .228 o179 v 32 v lOb

-36 36

+24’- #24

+12

-- -‘‘

-24- -24

-36--- 2 3 4 5 6 7 8 10 1112 3141516

CHRONOLOGICAL AGE IN ‘YEARS

PATTERN Im GIRLS #{149}145 o257 v6 v288 .23

+36 - . +36

I

-+24

:2

-$2

-24 - 1_24

-36 - --- - --- _--- - I I 136

B I 2 3 4 5 6 7 8 9 10 II 2 13 14 5 16 7 8

CHRONOLOGICAL AG IN YEARS

Fic. 3 (top) Fic. 4 (bottom)

PATTERN Is BOYS .297 o99 v116 v246

+36- +36

I

Z +24 - +24

z

-

42

O - --

-- .--- --- - -2

-24

-

-24

I I I I I I I --- ‘36

B I 2 3 4 5 6 7 8 9 0 II 12 13 14 IS 16 IT 18

CHRONOLOGICAL AGE IN YEARS

PATTERN GIRLS

+36 - II o232 .233 v240 - +36

Is #{149}29 --- +24

B I 2 3 4 5 6 7 8 9 0 II 12 13 14 IS 6 Il IS -36

(11)

-

+12-0

L-24

PATTERN II St

36r

GIRLS +163 .286 .239 +25 .59

-‘ 36

+24’- +24

Fic. 7 (top) Fic. 8 (bottom)

PATTERN BOYS

p249 .146 -1+36

188 o22O .161

PATTERN GIRLS

11 sm +204 #{149}227 .285 Ills oI57 .166 2I7

+36 +24

+12

-O -12

-24

I 5 3 4 5 6 7 8 9 10 II 2 3 14 IS 16 17 18

Fic. 9 (top)

Fic. 10 (bottom) 896

PATTERN II sI BOYS +111 #{149}236 ,‘93 .133

+36-- - +36

+24- ,,+-__.__,,,.

B_34:648IoIII6

+36- lIsm Ills

S

z +12

-24-234 5 6 7 891011 12 3 4 5 16 Il

+36

+24

-S

z z +12

-0 4 ;

o-0

-I2

(12)

The five patterns thus discarded would he

all in the III category, namely, msf, fms,

fsm, mfs and fsf. This leaves 13 patterns to

which three or more children conformed;

of these, 3 patterns belong to category I, 5

to II and 5 to III.

The most commonly encountered

pat-terns, in order of total number of cases,

boys and girls combined, are I m with 27

cases, II mf with 15 and II sf with 14. Thus,

the largest groups were either consistently

“moderate” throughout or followed a faster

pattern during the second than the first

pe-riod. Pattern II ms was followed by nine

children, the only one with more than six

children who progressed at a slower rate in

the late than in the early years. Six

chil-dren followed patterns II sm, II fs and III

msm and five followed patterns I s, III smf

and III sfs, and three or four children

fol-lowed patterns I f, III mfm and III sfm.

The ‘irregular” categories, which by

defi-nition means only that the cases assigned to

them did not fit any accepted pattern,

col-lectively account for 6 boys and 12 girls.

The most commonly encountered one was

“irregular” in both periods (ii). Irregularity

in the first period only (ir) was more

com-mon than in the second only (ri), but the

numbers in each are small. Summarizing,

therefore, in terms of number of children in

each group of patterns characterized by

sim-ilar general trends, 35 of 133 children were

consistent in rate throughout; 35 changed to

a faster rate in the second period, whereas

only 15 changed to a slower one. Thirty

children changed rates twice and 18 were

“irregular.” All of these findings and the

number of boys and girls assigned to each

pattern are shown in Table II.

It has been found impossible to present

au the individual curves which have been

assigned to each of the patterns selected

because of the limitation of space for

Fig-ures and tile confusion which results when

too many curves are drawn on a single

graph. In Figures 3 to 20, inclusive,

matched charts for boys and for girls

appear together. In each Figure a few

individual graphs are plotted over the

ap-propriate curves for the mean and 1

stand-ard deviation against chronological age.

When case examples are few in number,

two or more patterns are presented in each.

Whenever possible, all examples for sex are

graphed on a single Figure, otherwise

Se-lections have been made using several

ap-proaches. Sometimes it has been found by

superimposing graphs on an illuminator

that two are so identical that one can be

charted and the other set aside. In the few

patterns with numerous cases, the chief

basis of selection has been to demonstrate

variants of the pattern, either in the

gen-eral level of progress, that is, at the

“ad-vance,” “moderate” or “delayed” level, or in

the degrees of fastness or slowness within

the range permissible, or in the timing or

age of change from one rate to another.

De-grees of irregularity within a pattern have

been demonstrated fully for those with few

cases where all are plotted. For the patterns

with larger numbers, the smoother curves

have at times been selected to permit

clearer visualization of cases.

In studying the curves of cases presented in

Figures 3 through 20, it may help the reader

to have recalled some of the features of these

Figures common to all and some of the rules

as they apply to cases. This can be done in a

brief discussion of Figures 3 and 4. At first

glance it may appear that cases portrayed in

these Figures are not progressing consistently

at a “moderate” rate as is required for the I m

pattern. It must not be overlooked that “moder-ate,” “fast” and “slow” in these and subsequent Figures are in relation to the background norms

and not the month lines of the chart. On first

inspection of Figure 3 it will be seen that the

curve of Boy 106, which appears to fall sharply between 1 and 4 years is actually progressing at a level within 2 to 5 months below the minus

1 standard deviation (lower broken line). It is

in relation to this norm that this case must be

judged. The same case line rises to 2 months

above the reference line from 8 to 10 years

and falls as far as 5 months below it again at

13 years and 14 years 2 months. These

irregu-larities make Case 106 an example of the

moderate variability that can occur within the

permissible range for this pattern. Similarly,

(13)

PATTERN nrnf BOYS 67 .65 ‘+58 .299

+36 +36

24

PATTERN IImf GIRLS 272 .10 ‘+150 .126

V

36r ,- --- ‘ 1+36

F

--$2

‘.J-24 --26

-31 I 1 1 -- ---- - - -36

B I 2 3 4 5 6 7 8 9 10 II 2 13 14 5 6 17 8

Fic. 11 (top) FIG. 12 (bottom)

4 4

-12

PATTERN Urns

GIRLS 068 #{149}131 vIOl .201

+36

+24

S

I 1

0

4

0 0 4 4 sJ -21

-B I 2 3 4 5 6 7 8 9 10 II 1213 4 IS 16 17 18

CHRONOLOGICAL AGE IN MONTHS

Fic. 13 (top) Fic. 14 (bottom)

+12

-c

PATTERN lIms BOYS +37 .140 v155 .141 .196

+36 +24

+12

-O

-12

(14)

+36 +24

+12

-O

-12

-24

+36

PATTERN BOYS

+36-- III sIm ‘+ 53

III msm .178

+24 Ill sfs 265 #{149}130

PATTERN GIRLS

+361- III ‘‘ 299

Ill 18

III f’ 280

+74-- III sfs #{149} 74

S

--36’ -i--- -

---

--

-Fic. 15 (top)

PATTERN BOYS

+36-

-

II s,,,I -+ 64

11 sfm #{149}134

II “sf #{149} .152

36L

+24

+12

0

3 - 4 5 6 7 8 9 0 II 2 13 14 15 lB 7 lB

CHRONOLOGICAL AGE IN YEARS

-12

-24

Fic. 16 (bottom)

- - - ____I I - -- i-- _l I - I

B 1 2 3 4 5 6 7 8 9 10 II 12 13 14 IS 16 I? 18

CHRONOLOGICAL AGE IN YEARS

GkLS

v 277

+ 252 .261

+36

+24

+12

0

-12

-24

-36

1:::

-+12

-O

-12

-24

-36

10 II ‘2 13 14 IS lb IT lB

CHRONOLOGICAL AGE IN YEARS

1 ‘ I I - I -- 1 A

Fic. 17 (top) Fic. 18 (bottom)

PATTERN

$3 smf

III Is’’ Ill “SI

+36r

(15)

lines for the mean and minus 1 standard

devia-tion, falls about 2 months below the latter

be-tween 2 and 3 years of age. Technically, this

case would have been called “irregular” in the

first period but “regular” in the second, except

for the rule which permits one age assignment

to be out of range if bounded by appropriate

age assessments. Only at 43 years is this case

more than 1 standard deviation removed from

the lowest age position. The same license has

been taken with Girl 288 in Figure 4, when at

23 years her skeletal age was several months

below her level at 2 and 3 years and in itself

below the permissible level of variability for her

curves as otherwise maintained. It should also

be recalled in reviewing these charts that

as-sessments below 1 year for both sexes and

above 15 for girls and above 17 years for boys

are regularly ignored in assigning pattern.

Otherwise, Girl 23 in Figure 4 would be thrown

out of this pattern by the positions held by her

at 163k and 1Th years.

A few of the features of the “skeletal age

(hand)” curves presented in the preceding

Figures are mentioned here but others

will be observed by the reader and deserve

further attention in the studies of

inter-relationships in reports to follow. The

curves of the 4 boys in Figure 5 show

strik-ing consistency and proximity of positions

at all ages except that the extent of delay

due to the “slow” pattern for Boy 246 was

considerably greater than for the others.

There being no boys in I f and only one girl

in Pattern I s, Figure 6 shows the combined

patterns I f and I s for girls. An interesting

feature of Figure 6 is that twins, Cases 232

and 233, followed courses within the

pat-tern which are extremely alike. These girls

are not identical twins and it has been

found that other twins in this Series,

al-though not identical, are equally alike in

pattern. Garn and Shamir1 have presented

comparisons of pairs of children-unrelated,

siblings, dizygotic and monozygotic

twins-as to tile relative times of appearance of the

first 38 ossification centers. They have

con-cluded that as the number of genes held in

common increases, these pairs become

more alike in the times of these

appear-ances. However, in this Maturity Series,

curves of other pairs of children who are

unrelated have been found much alike also.

It is proposed to study further this aspect

of similarities in patterns between twins,

siblings and unrelated children, but Figure

6 calls attention to the fact that close

simi-larities in individual curves do occur. In the

presentation of cases in these Figures, the

purpose has been to demonstrate not only

the differences between patterns of skeletal

development but also intra-pattern

differ-ences between individuals. This purpose

and the exclusion of similar curves to avoid

confusion in plotting have masked

similari-ties.

In Figures 7 and 8, which present slow

rates followed by fast rates, the boys sllo\\-’

great uniformity both in relative speeds by

periods and at age of change in rate of

progress. They show, on the other hand,

considerable contrast in overall levels at

which progress takes place. As examples,

Cases 193 and 133 never approach each

other except for an eccentric rating at 15

years, which may be ignored. The girls, on

the other hand, in Figure 8 show somewhat

more variations than did the boys,

particu-larly in regard to the age at which change

from “slow” to “fast” took place.

It has been noted in several patterns

in-volving a “fast” rate that tile speed tends to

be greater when the original level is

ad-vanced than when it is delayed. It is

appre-ciated that when infants are advanced in

level at birth or at 1 year this advancement

must represent preceding accelerated rate,

presumably during fetal life or early

in-fancy. These earlier occurrences and the

causes for them are of great interest and

much data of possible relevance to this

relationship is available and should be

studied, but they are not the concern of

this paper. It would be expected that a

child advanced, or one delayed, at 1 year

would tend to hold the same position

there-after unless impelled by some intrinsic or

extrinsic factor to proceed on another than

moderate rate. Many children in this Series

have maintained initial position very

(16)

PATTERN GIRLS

IV ‘ +36

2

-12,-

-24’-.‘59mos

--36- l ‘ A I 6 1 1 I I 30

B I 2 3 4 5 6 7 8 9 10 II 12 13 14 IS 16 17 18

FIG. 19 (top) Fic. 20 (bottom)

+36

+24

+12

S

-12

-24

PATTERN BOYS

+36 IV , . 84 _,-0 + +36

IV +154 .238

‘+224 .202 +283 .219 _____.__

2 ‘24 - . - .- +24

2

/

-,

+1? ..-.-. “-- +12

:

_O

-24

3’, L_J__I I 1 1 I 1 1 -36

3 I 2 3 4 5 6 7 8 9 10 II 12 13 14 15 16 17 18

o- 197 #{149}-206

---258.--I42 ‘+180.--- 60 81 .-222 ‘+-279 .-198 #{149}---II‘-247

253 was seen to be regularly advanced and

Case 130 quite regularly delayed.

Turning to Figures 13 and 14, the five

boys shown are all strikingly “moderate” in

rate during the first period and “slow”

dur-ing the second. They vary somewhat in age

of change to a slow rate and even more in

the level of delay which they attain at 17

years, a matter of 2 years 5 months between

tile least and most delayed in terms of

skeletal age. Girls in this pattern present

greater differences in levels of progress

than tile boys.

Figure 18 shows Girls 261 and 252 were

much alike in timing of the changes in their

rates. The 1 year longer in the first, or fast,

period permitted 252 to become more

ad-vanced at the beginning of the middle or

slow period, but this was overcompensated

by a more rapid fall which put 261 4 or 5

months ahead between 9 and 15 years.

All of the children’s graphs of “skeletal

age (hand)” which (lid not comply with the

rules for any patterns described above are

grouped together in Figures 19 (for boys)

and 20 (for girls). If one has the patience to

trace individual curves in these Figures it

will become evident that most of them are

not really irregular except at one or two

short age periods. Some curves are quickly

recognized as belonging in the main to a

particular defined pattern. In Figure 19 for

example, Boy 184 (x-x) clearly belongs to

pattern III fms until age 15, but then

be-comes too fast for it. Likewise, Boy 154

(open circle) fits pattern III smf except for

early irregularities. In both Figures most

of the assessments at ages below and above

those of the norms have been omitted

be-cause of crowding due to number of cases

plotted.

Although it has been pointed out in some

patterns that girls appear to be somewhat

more irregular than boys there is not

suffi-cient evidence to suggest that this is a true

sex difference. In fact when appropriate

norms for sex are used, which automatically

(17)

over boys in terms of chronological age, one

is impressed with the similarities in

pat-terns rather than their difference between

boys and girls. This has been shown to hold

for such aspects of patterns as those most

commonly followed and those showing

either no cases or one or two cases.

SUMMARY

The first purpose of this presentation of

patterns of skeletal development in the

hand has been to demonstrate that

essen-tially normal children, although passing

through very similar steps or stages of

skeletal development in the hand, do so in a

variety of ways in respect to the rates of

their progress through these stages or by

age periods. The second objective has been

to show the kinds of patterns which emerge

and the relative frequency with which

cer-tain of these are encountered. This has been

done by studying the consistency manifest

by children in their rate of progress over

tile whole of childhood as well as by major

subdivisions of the developmental period.

This Study shows that few children are

very irregular in progress or change

fre-quently to any substantial degree in their

rate of progress, but many make one or two

substantial shifts in rate from one period to

another. The most common, marked and

understandable shift is the single one

oc-curring roughly between childhood and

adolescence. The years close to the dividing

line between these two age periods,

there-fore, are the ones in which change in rate

of skeletal development (hand) may be

ex-pected most commonly. The changes in

rates occurring at other ages, as portrayed

in patterns under III or IV (Figs. 15 to 20),

are not readily explained on the basis of

other features of development. Factors

found associated with these different

pat-terns of skeletal development in the

chil-dren concerned, relating to nutrition,

ill-ness experiences, growth in height and other

aspects of development will be considered

in later reports on interrelationships.

Aside from a Preli1l1in11y report from this

1aboratory’ the only other report known to

the authors which dealt longitudinally with

patterns of skeletal development was

pub-lished by Kelly in 1937.15 This concerned

children 6 to 18 years of age and used an

index derived from measurements of several

bones or epiphyses in the hand and wrist;

six patterns were derived from these indices

and described as convex, linear, concave,

convex-concave, linear-convex and

concave-convex. Because of the fundamental

differ-ences in the data used in this Study, it is

not possible to compare Kelly’s results with

those being reported.

Acknowledgment

The authors are indebted to Dr. \Villiam

Walter Greulich, Professor of Anatomy,

Stan-ford University, Stanford, California, for

valu-able guidance in earning out this Study and in

the preparation of this report. They also

ac-knowledge assistance from many staff members

over the years, especially E. \Togt during the

early years and M. Anderson more recently,

in obtaining satisfactory roelltgenograms and

V. V. Harding, E. Grant and

J.

Cornoni in the

evaluation of data.

The authors acklloWledge financial support

in the past years from many organizations

listed in the preceding paper which made

possi-ble the collection of the roentgenograms on

which this Study is based. They acknowledge

specifically grants from tile Research Grants

Division of the U. S. Public Health Service

which have provided for the evaluation of the

roentgenograms on which this report is based.

REFERENCES

(For “References in Bibliography,” see p. 973.)

1. Reference 3 in Bibliography.

2. Shuttleworth, F. S.: a) Sexual maturation

and the physical growth of girls; age 6

to 19. Monogr. Soc. Res. Child Devel.,

2:serial 12, No. 5, 1937; b) Sexual

matis-ration and the sexual growth of girls;

age 6 to 19. Idem, 3:serial 18, No. 5,

1937; c) The adolescent period: a

graphic atlas. Idem, 14:serial 49, No. 1,

1949.

3. Todd, T. W.: The roentgenographic

ap-praisement of skeletal differentiation. Child Devel.. 1:298, 1930.

(18)

903

6. Greulich, W. W., and Pyle, S. I.:

Radio-graphic Atlas of Skeletal Development

of the Hand and Wrist. Stanford,

Cali-fornia, Stanford Univ. Press, 1950; 2nd

Ed., 1959.

7. Todd, T. W.: Atlas of Skeletal

Matura-tion (Hand). St. Louis, Mosby, 1937.

8. Pyle, S. I., and Hoerr, N. L.: Radiographic

Atlas of Skeletal Development of the

Knee. Springfield, Thomas, 1955.

9. Hoerr, N. L., and Pyle, S. I.: Radiographic

Atlas of Skeletal Development of the

Foot and Ankle. Springfield, Thomas,

to be published.

10. Acheson, R. M.: A method of assessing

skeletal maturity from radiographs; a

report for the Oxford child health

sur-vey.

J.

Anat., 88:498, 1954.

11. Pyle, S. I., et a!.: A substitute for skeletal

age (Todd) for clinical use: the red

graph method.

J.

Pediat., 32:125, 1948.

12. Pyle, S. I.: Effect of the difference in

stand-ards in interpreting skeletal age of

in-fants. Merrill Palmer Quart., 4:74, 1958.

13. Garn, S. M., and Shamir, Z.: Methods for

Research in Human Growth. Springfield, Thomas, 1958.

15. Kelly, H.

J.:

Anatomic age and its relation to stature. Univ. of Iowa Studies, Studies

(19)

1959;24;886

Pediatrics

S. Idell Pyle, Robert B. Reed and Harold C. Stuart