American Journal of ORTHODONTICS Volume
69, T~cnzber 6, June,
ORIGINAL
1976
ARTICLES
Skeletal ossification a+ *‘-- dolescent growth spurt K. C. Grave,
M.D.S.,
F.R.A.C.D.S.,
and
T. Brown,
D.D.Sc.,
F.R.A.C.D.S.
Adelaide. South Australia
T
he developmental status of a child is usually assessed in relation to physical events that take place&ting thagress. of growth (for example, skeletal ossification stages, the attainment of peak growth velocity, or the pubescent changes in the body). Although growth events occur in a reasonably constant sequence, the ages at which they are reached vary considerably among children. Indicators- of developmental age are therefore more informative than chronologic age, particularly for clinical application. In orthodontic practice, an important measure of physical development is provided by ratings of skeletal age. Earlier reports have indicated a close relationship between the ages at which peak growth velocities occur in stature and facial dimensions and the attainment of ossification events in the skeleton of the hand and wrist.l-” Information of this nature is useful in orthodontic diagnosis and for the planning of appropriate treatment where it is necessary to estimate whether growth is accelerating or decelerating. The present report extends earlier findings by the examination of peak growth velocity in stature in rel+,ijon to a more extensive series of ossification events taking place in t,he hand and wrist skeleton around the time of puberty. Materials
and
methods
The analysis is based upon data obtained from the serial records of eightyeight aboriginal children (fifty-two boys and thirty-six girls) selected from a larger number enrolled in a longitudinal growth study that has been in progress since 1961.’ All the children are of pure aboriginal ancestry and are members of the Walbiri and Pintubi groups. predominantly the former. The children From the Department
of Oral Biology,
The University
of Adelaide. 611
’
I NORTHERN TERRITORY
Yuendumu
Reserve
-Alice
SOUTH Fig. 1. The
Northern
Territory
of
Australia
Springs
AUSTRALIA showing
the
1 location
of
Yuendumu
Reserve.
live at Yuendumu, a Commonwealth government settlement located about 180 miles to the northwest of Alice Springs in the Northern Territory of Australia (Fig. 1). Yuendumu was established in 1946 to provide food, clothing, medical care, and schooling for aborigines living in the region. Details of the settlement, the growth study, and the way of life of the people have been given previously.’ Ten visits to Yuendumu were made between 1961 and 1971, and the records obtained include family histories, body measurements, dental casts, cephalometric roentgenograms, roentgenograms of the hand and wrist, and photographs of the head. For the present study, the records of children with recorded birth dates were selected. For each child, the age at which the peak adolescent growth velocity occurred was taken as the midpoint of the two consecutive ages between which the maximum increment in standing height was recorded. A number of ossification events were also studied on the serial hand and wrist films (Table I and Fig. 2). The fourteen ossification events can be grouped into two categories, ossification of individual bones and epiphyseal changes. Events in individual bones included initial ossification of the pisiform (Pisi), initial and advanced ossification of the hook of the hamate (H-l, H-2)) corresponding to Stages 7 and 8 of hamate ossification defined by Tanner, Whitehouse, and Healy,* and initial ossification in the ulna metacarpophalangeal sesamoid of the first finger (S).
Skeletal
Fig.
ossification
2. Ossification
and adolescent growth
events
spurt
613
studied.
Epiphyseal changes were recorded for the first, second, and third fingers and the radius. They included attainment of epiphyseal width equal to diaphyseal width in the proximal phalanx of the second finger (PP2=), in the middle phalanx of the third finger (MP3 = ) , and in the radius (R= ) ; epiphyseal capping in the proximal phalanx of the first finger (PPl,,,), in the middle phalanx of the third finger (MP3,,,), and in the radius (Reap) ; and epiphyseal union in the proximal, middle, and distal phalanges of the third finger (PP3,, MP3,, DP3,) and in the radius (R,) . The criteria for assessing the epiphyseal stages were the same as described previously.4 The age at which an ossification event occurred was taken as the midpoint of the year after which the event was first discernible on a hand and wrist film, that is, the midpoint of adjacent examination ages 1 year apart. Average ages at which peak growth velocity and the ossification events took place were analyzed for girls and boys separately. The time intervals between peak velocity and the ossification events were also studied. Associations between the developmental events were expressed as coefficients of correlation.
AWI. J. Ol‘thod.
.June
Fig. 3. Ossification listed in Table I.
Table
I. Ossification
Abbreviation 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.
PP2= MP3= H-l Pisi R= s H-2 MP3,, PPI,, Lp DP3, PP3* MP3, R,
times
relative
events
to peak
growth
velocity.
The
numbers
refer
to the
1976
events
studied
Ossification event Proximal phalanx of second finger; epiphysis is as wide as its diaphysis Middle phalanx of third finger; epiphysis is as wide as its diaphysis Hooking of hamate-Stage 1 Appearance of pisiform Radius; epiphysis is as wide as its diaphysis Appearance of ulnar sesamoid at metacarpophalangeal joint of first fmger Hooking of hamate-Stage 2 Middle phalanx of third finger; epiphysis caps its diaphysis Proximal phalanx of first finger; epiphysis caps its diaphysis Radius; epiphysis caps its diaphysis Distal phalanx of third finger; complete epiphyseal union Proximal phalanx of third finger; complete epiphyseal union Middle phalanx of third finger; complete epiphyseal union Radius; complete epiphyseal union
Results
Table II and Fig. 3 show that average ages (in decimal years) at which the ossification events occurred in aboriginal boys and girls. They are listed in ascending chronologic sequence. The age interval between the earliest and latest events was about 7 years, and in all instances ossification was earlier in girls. The sex differences ranged from 0.8 year for epiphyseal union in the radius to 2.3 years for the hamate Stage 2 and distal epiphyseal fusion of the third finger. The sequence of ossification did not differ greatly between boys and girls. The ossification ages were similar to those previously reported for aborigines” and were within the range of those derived for Caucasian children 1, 4, 10,11 In a previous account of growth in aboriginal children it was reported that
Table II. Timing of ossification
events in aboriginal
boys and girls Age in years
Ossification event
PP2= MP3= H-l Pisi R= s H-2 MP3q PPLp R -P DP3, PP3, MP3, R,
Sex
M F M F M F M F M F M F M F M F M F M F M F M F M F M F
No.
20 13 32 19 31 18 44 25 41 26 41 27 46 25 48 29 46 28 44 28 33 23 23 20 22 19 11 10
Mean
10.5 9.6 11.2 9.1 12.2 10.6 12.6 10.5 12.6 10.8 13.5 11.3 13.6 il.3 14.0 12.4 14.0 12.3 14.0 12.4 15.4 13.1 16.0 14.1 16.0 14.3 17.3 16.5
Standard deviation
1.2 0.9 1.3 I.0 1.1 1.4 1.2 1.1 1.2 1.1 0.9 1.3 0.9 1.1 0.8 1.2 0.7 1.1 0.8 1.1 0.1 I.0 0.9 0.9 0.9 1.1 0.7 1.2
the peak growth velocity in body height occurred at 13.8 years in boys and 11.8 years in girls.” Table III indicates the relations between the age of peak growth velocity and the ossification times by showing the average interval between the events (in years) and the percentage distribution of children in whom an ossification event preceded, coincided with, or followed peak growth. An ossification event was taken to be coincident with peak growth velocity if both were recorded at the midpoint of the same annual interval between successive examinations. Two ossification events clearly preceded peak growth velocity in all subjectsepiphyseal widths reaching diaphyseal widths in the proximal phalanx of the second finger and the middle phalanx of the third finger-the time intervals ranging from 2.0 to 3.2 years. In the majority of boys and girls an additional three events preceded peak growth velocity-hamate Stage 1, initial ossification of the pisiform, and equality of epiphyseal and diaphyseal widths in the radius. These time intervals ranged from 1.1 to 1.7 years. At the other end of the time scale, three events followed peak growth in all subjects-epiphyseal union in
616 Table peak
Brat:e III. growth
Ossification event
PP2= MP3= H-l Pisi R= S H-2 MP3, PPL, Rw DP3, PP3, MP3, RF
,lli!. .J.ol~thotl. ,J7~11P / 1976
crnd Bmzo~r
Distribution velocity
Sex
M F M F M F M F M F M F M F M F M F M F M F M F M F M F
of
children
in
body
No.
10 5 17 11 16 13 24 16 24 16 30 17 28 15 30 16 30 16 28 16 25 15 16 12 16 12 9 7
according
to
sequence
of
ossification
events
relative
to
height
A verage time interval (in years) between ossification andpeak growth
3.2 2.0 2.4 2.0 1.7 1.2 1.3 1.4 1.2 1.1 0.3 0.5 0.2 0.5 -0.3 -0.6 -0.3 -0.5 -0.2 -0.4 -1.6 -1.5 -2.3 -2.4 -2.3 -2.8 -4.0 -4.6
f0.4 f0.4 10.3 10.3 f0.3 f0.3 f-o.2 zto.2 f0.2 f0.2 fO.l f0.2 fO.l f0.2 fO.l f0.2 fO.l f0.2 f0.1 f0.2 fO.l f0.2 f0.2 f0.2 f0.2 f0.2 f0.2 f0.4
Number Ossification preceding peak growth 10
(100)
5 17 11 14 10 19 15 18 13 8 9
(100) (100) (100) ( 87) ( 77) ( 79) ( 94) ( 75) ( 81) t 27) t 53)
8
t
28)
6 ( 40) 1 t 3) 3 (10)
8 t 28)
and per cent Ossification coinciding with peak growth
2 2 5 1 6 2 22 7 17 9 20 7 15 9 17 IO 1 1
(13) (15) (21)
of children Ossification following peak growth
1
t
8)
1
(
6)
1
t
6)
(6) (25) (13) (73) (41) (61) (60) (67) (44) (50) (56) (61) (63) (4) (7)
3 (11) 9 9 12 7 3 6 24 14 16 12 16 12 9 7
( 30) t 56) ( 40) ( 44) (11) ( 37) ( 96) ( 93) (100) (100) (100) (loo) WY (100)
the proximal and middle phalanges of the third finger and in the radius. Time intervals ranged, on the average, from 2.3 to 4.6 years. Furthermore, epiphyseal union in the distal phalanx of the third finger occurred, on the average, about 1.5 years after peak velocity in all but two children. Of the remaining five events, ossification of the sesamoid and epiphyseal capping of the middle phalanx of the third finger in girls coincided with peak growth velocity in 41 per cent and 44 per cent, respectively. In the boys these two events coincided with peak growth in 73 per cent and 67 per cent, respectively. The other ossification events coincided with peak growth in 50 per cent or more of the subjects-hamate Stage 2 and epiphyseal capping of the proximal phalanx of the first finger and the radius. Table IV lists the coefficients of correlation between the ages of peak growth velocity and the fourteen ossification stages. All correlations were positive and
Table
IV.
ossification Ossification event
Correlations events
between
age at peak
growth
velocity
Males
in height
and
ages of
Females
N
I
10 17 16 24 24 30 28 30 30 25 28
0.34 0.01 0.19 0.51; 0.63t 0.83t 0.68t 0.82t 0.69t 0.797 0.777
5 II 13 16 16 17 15 16 16 16 15
0.50 0.52 0.71t 0.757 0.69t 0.857 0.83t 0.88t 0.86t 0.87-f 0.78t
16 0.8Ot PP3, MP3, 16 0.80-f 0.38 RP 9 *Coefficient differs from zero at p < 0.05 level. tcoefficient differs from zero at p < 0.01 level.
12 12 7
0.75t 0.82t 0.36
PP2= MP3= H-l Pisi R= s H-2 MP3, p&a, R Gp,
N
r
most were high, confirming the expectation of close associations between developmental events occurring during the period of pubescence. The highest associations were recorded between peak growth velocity and sesamoid ossification in boys (r = 0.83) and capping of the middle phalanx of finger three in girls (r = 0.88). Moreover, as would be expected, the associations tended to be stronger for the events that coincided with peak growth. Most correlations were higher in the girls, a finding commented on previously.3 Discussion
During the circumpuberal period, children exhibit marked changes in body dimensions and ossification processes. In the aboriginal children under observation, the growth rates in stature and facial dimensions displayed a puberal maximum at about the same time.3 Furthermore, the ages of peak growth velocity and those of the ossification events were similar in aborigines and Caucasian children. Reliable growth assessment is important in orthodontic practice for diagnosis and treatment planning. Knowledge of the timing of peak growth velocity in the face and an assessment of its magnitude and direction may be used to complement treatment procedures. In particular, an indication of whether peak facial growth is imminent or complete can decide the form of treatment for a Class II malocclusion. Moreover, it is generally considered wise to make decisions regarding permanent tooth extraction around the period of maximum growth activity, because the facial growth pattern is nearing full expression at this time. Skeletal indicators of growth activity are useful in this respect, particularly if they can be readily assessed from conventional hand and wrist films.
The events studied fell logically into three groups with respect to ossification times: events which occurred in a large percentage of subjects before peak growth velocity (PP2 =, MP3 =, I-I-1, Nisi, R = ) ; c\-ents which in most, children coincided with peak growth (S, H-2, MP3,,,,, I’PI,.;,,,, I~,.,,,,): and c>vcnt-s which clearly followed peak growth in most subjects (DP3p, PP3p, MPXp, R+J,). These findings suggest that a series of developmental events can be used as markers of the accelerative, peak, and dccelerative phases of growth activity. For example, treatment involving the application of’ extraoral traction (Step 1) should be commenced prior Taoossification of the hamatc-2 or sesamoid. This accelerative period is best indicated 1);~ onset of pisiform or hamate-l ossification or equality in epiphpseal and diaphyseal widths of the radius. Complete band placement (Step 2) should take place at the time of peak growth velocity indicated by epiphyseal capping in the first, and third fingers and the radius. Treatment objectives should be accomplished when growth is decelerating as indicated by epiphyseal union in the distal phalanx of the third finger. Fusion of the distal phalanges occurs about the time of menarche,” and it is further suggested that epiphyscal union of the radius can he used to assess the duration of the retention phase of treatment. The findings arc similar to those reported for l)anish children,” supporting the view that observations of epiphyseal changes in the fingers and radius provide supplementary indicators of growth activity in addition to the ossification events in round bones of the wrist. The analysis has also clarified the general relationshi& between body growth and skeletal maturation which can be usefully applied in objective treatment planning. However, because of wide variation between children in developmental timing, ossification events should be used only as guides to growth activit,v and supplemented b,v a. more complete knowledge of the child’s developmental history if this is available. Summary
Fourteen ossification events in the hand and wrist were studied in relation to the age of peak growth velocity in body height in fifty-two boys and thirty-six girls. The subjects were aborigines enrolled in a longitudinal growth study. Peak growth velocity and the ossification events oc,curred in aborigines at about the same ages as in Caucasian children. The results indicate that t,he ossification events can be used by the orthodontist to assess a child’s growth activity. The accelerative phase of the adolescent growth spurt is accompanied by cpiphyseal widths reaching diaphyseal widths in the fingers and radius and by ossification of the pisiform and hamatc Stage 1. Peak growth velocity occurs at about the time of epiphyseal capping in the fingers and radius and ossification of the sesamoid and hamate Stage 2. The decelerative phase of growth is indicated by epiphyseal union in the third finger, progressively from distal to proximal phalanges, and in the radius. The value of these indicators in orthodontic practice is discussed. We acknowledge Administration and
the assistance Mr. and Mrs.
of the director T. J. Fleming
of of
Welfare Yuendumu.
of the Northern The research
is
Territory based on
Skeletul field work supported by United the National Institute of Dental and by grants from the University and the Orthodontic Foundation
ossificatio7l and udolescent growfh
States Public Health Service Research, National Institutes of Adelaide, the Australian of Australia.
spwt
619
Research Grant DE 02034 from of Health, Bethesda, Maryland, Institute of Aboriginal Studies,
REFERENCES
1. Bjiirk, A., and Helm, S.: Prediction of the age of maximum puberal growth in body height, Angle Orthod. 37: 134-143, 1967. d. Grave, K. C.: Timing of facial growth in Australian aborigines, M.D.S. thesis, University of Adelaide, 1971. 3. Brown, T., Barrett, M. J., and Grave, K. C.: Facial growth and skeletal maturation at adolescence, Tandlaegebladet. 75: 1211-1222, 1971. 4. Helm, R., Siersback-Nielsen, S., Skieller, V., and Bjiirk, A.: Skeletal maturation of the hand in relation to maximum puberal growth in body height, Tandlaegebladet. 75: 1223.I”14 dl, 1971 . . 5. Grave, K. C.: Timing of facial growth: A study of relations with stature and ossification in the hand around puberty, Aust. Orthod. J. 3: 117-122, 1973. 6. Bolvden, B. I).: Sesamoid bone appearance as an indicator of adolescence, Aust. Orthod. J. 2: 242-248, 1971. 7. Brown, T., and Barrett, M. J.: Dental and craniofacial growth studies of Australian aborigines. In Kirk, R. L. (editor) : The human biology of the aborigines in Cape York, Canberra, 1973, Australian Institute Aboriginal Studies. 8. Tanner, J. M., Whitehouse, R. H., and Healy, M. J. R.: A new system for estimating skeletal maturity from the hand and wrist, with standards derived from a study of 2,000 healthy British children. Part II. The scoring system, Paris, 1962, International Children’s Centrc. 9. Abbie, A. A., and Adey, W. R.: Ossification in a Central Australian tribe, Hum. Biol. 25: 265-278, 1953. 10. Garn, S. M., and Rohmann, C. G.: The adductor sesamoid of the thumb, Am. J. Phys. Anthropol. 20: 297-302, 1962. 11. Greulich, W. W., and Pyle, S. I.: Radiographic atlas of skeletal development of the hand and wrist, ed. 2, Oxford, 1959, Oxford University Press. 12. Sinclair, D.: Human growth after birth, London, 1969, Oxford University Press, p. 82. Department
of Oral Biology (5001)