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THE PATTERN OF FACIAL SKELETAL GROWTH AND ITS RELATIONSHIP TO VARIOUS COMMON INDICES OF MATURATION Zachary Joseph Mellion, D.M.D. An Abstract Presented to the Faculty of the Graduate School of Saint Louis University in Partial Fulfillment of the Requirements for the Degree of Master of Science in Dentistry 2007
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Page 1: THE PATTERN OF FACIAL SKELETAL GROWTH AND … PATTERN OF FACIAL SKELETAL GROWTH AND ITS RELATIONSHIP TO VARIOUS COMMON INDICES OF MATURATION Zachary Joseph Mellion, D.M.D. An Abstract

THE PATTERN OF FACIAL SKELETAL GROWTH AND ITS

RELATIONSHIP TO VARIOUS COMMON

INDICES OF MATURATION

Zachary Joseph Mellion, D.M.D. An Abstract Presented to the Faculty of the Graduate School of Saint Louis University in Partial Fulfillment of the Requirements for the Degree of Master of Science in Dentistry

2007

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1

Abstract

Introduction: The timing of developmental events

in the hand and wrist and cervical vertebrae has been shown

to bear at least a moderate correlation with the peak

growth rate in height and the facial skeleton. The

objective of this study was to compare the efficacy of

these skeletal events and chronological age in assessing

and predicting the timing of facial growth. Subjects and

Methods: To serve as a gold standard against which to

evaluate these predictors, serial cephalograms from 100

normal, healthy subjects (50 females and 50 males) from the

Bolton-Brush Growth Study Center in Cleveland, Ohio were

analyzed. Each of the 100 subjects had a series of at

least 6 consecutive, annual cephalograms between 6 and 20

years of age. Five cephalometric measurements (S-Na, Na-

Me, PNS-A, S-Go, Go-Pog) were summed to characterize

general facial growth, and a sixth measurement, Co-Gn, was

used to assess mandibular growth. In all, 808 cephalograms

were traced and analyzed. For most time points,

chronological age, height, and hand-wrist films were

available for analysis and comparison. The hand-wrist

films for each time point were staged according to

Fishman’s system; the cervical vertebrae, according to the

method of McNamara and associates. Yearly increments of

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general facial growth, mandibular growth, and statural

height were calculated for each subject, and separate

incremental growth curves were plotted against age. To

examine the ability of indices of maturation to assess the

presence of peak growth, the ages at onset and peak on each

growth curve were identified and compared with the ages

that the key indicators appeared on the hand-wrist and

vertebral scales. To test the predictive efficiency of

indices of maturation, the actual peak ages were compared

against predicted peak ages generated from statural onset,

vertebral stage CS2, and chronological age means. Results:

For females, the onset of the pubertal growth spurt in

height, facial size, and mandibular lengths females

occurred at mean ages of 9.78, 10.27, and 10.04 years,

respectively. The difference in timing between height and

facial size was statistically significant. In males, onset

occurred at mean ages of 12.43, 12.45, and 12.36 years for

height, the face, and mandible, respectively. In females,

the peak of the growth spurt in height, facial size, and

mandibular length occurred at 11.42, 12.02, and 12.00

years. Height peaked significantly earlier than both

facial size and mandibular length. In males, the peak in

height occurred slightly (and statistically significantly)

earlier than the peaks in the face and mandible (14.49,

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3

14.85, and 14.84 years). Error variances derived from the

hand-wrist and cervical vertebral methods to estimate peak

growth were not significantly lower than estimates based on

chronological age in the face, height, and mandible. Error

variances based on statural onset to predict the peak of

the pubertal growth spurt in height, facial size, and

mandibular length were significantly lower than prediction

based on the cervical vertebrae in males and significantly

lower than the cervical vertebrae and chronological age in

females. Conclusions: Skeletal age offers no value over

chronological age, either in assessing or predicting the

timing of pubertal growth. Stature offers a potentially

useful indicator to predict the timing of peak facial

growth.

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THE PATTERN OF FACIAL SKELETAL GROWTH AND ITS

RELATIONSHIP TO VARIOUS COMMON

INDICES OF MATURATION

Zachary Joseph Mellion, D.M.D. A Thesis Presented to the Faculty of the Graduate School of Saint Louis University in Partial Fulfillment of the Requirements for the Degree of Master of Science in Dentistry

2007

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COMMITTEE IN CHARGE OF CANDIDACY: Professor Emeritus Lysle E. Johnston Jr., Chairperson and Advisor Professor Rolf G. Behrents Assistant Professor Ki-Beom Kim

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DEDICATION

To my teachers; for it is only through their commitment,

sacrifice, and encouragement that I have been provided with

the potential to discover endless possibilities.

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ACKNOWLEDGEMENTS

The author wishes to express his sincere gratitude

to the following individuals:

Dr. Lysle E. Johnston Jr., for the suggestion of this thesis topic and his countless hours of work and guidance on every aspect of this thesis; Dr. Rolf G. Behrents, for his assistance with the records of the Bolton-Brush Growth Study Center, advice on this thesis, and guidance throughout my graduate education; Dr. Ki-Beom Kim, for his suggestions and time spent on this thesis; Dr. Heidi Israel, for her assistance with the statistical analysis of this thesis and for her patience; Drs. Mark Hans and B. Holly Broadbent Jr., for their generosity in allowing the use of the Bolton-Brush Growth Study Center records; and Alex Mellion, for his assistance in locating and curating the records in the Bolton-Brush Growth Study Center. In addition, I would like to thank my classmates

and the rest of the faculty at CADE for their assistance in

this research project.

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TABLE OF CONTENTS

List of Tables. . . . . . . . . . . . . . . . . . . . . vi

List of Figures . . . . . . . . . . . . . . . . . . . .viii

CHAPTER 1: REVIEW OF THE LITERATURE. . . . . . . . . . 1 Introduction. . . . . . . . . . . . . . . . 1 The Pattern of Skeletal Growth. . . . . . . 2 The Pattern of Facial Growth. . . . . . . . 8 Prediction of the Pubertal Growth Spurt . . 13 Chronological Age . . . . . . . . . . . 13 Secondary Sex Characteristics . . . . . 14 Stature . . . . . . . . . . . . . . . . 17 The Hand and Wrist. . . . . . . . . . . 18 Assessment of Maturation. . . . . . 18 Prediction of Stature . . . . . . . 20

Prediction of Facial Growth . . . . 25 The Cervical Vertebrae. . . . . . . . . 37

Assessment and Prediction of Stature. . . . . . . . . . . . . . 37

Prediction of Facial Growth . . . . 47 Prediction of Facial Growth Increments. . . . . . . . . . . . . 55

Overview . . . . . . . . . . . . . 56 Statement of Thesis . . . . . . . . . . . . 57 Literature Cited. . . . . . . . . . . . . . 59 CHAPTER 2: JOURNAL ARTICLE . . . . . . . . . . . . . . 64 Abstract. . . . . . . . . . . . . . . . . . 64 Introduction. . . . . . . . . . . . . . . . 66 Subjects and Methods. . . . . . . . . . . . 70 Sample. . . . . . . . . . . . . . . . . 70 Cephalometric Analysis. . . . . . . . . 72 Vertebral Staging . . . . . . . . . . . 74 Hand-wrist Staging. . . . . . . . . . . 75 Error Study . . . . . . . . . . . . . . 75 Growth Curve Analysis . . . . . . . . . 76 Statistical Analysis. . . . . . . . . . 77 Assessment of Maturation. . . . . . 78 Prediction. . . . . . . . . . . . . 78 Results . . . . . . . . . . . . . . . . . . 80 Discussion. . . . . . . . . . . . . . . . . 98 Pattern of Growth . . . . . . . . . . . 98 Indices of Maturation . . . . . . . . . 102 Prediction. . . . . . . . . . . . . . . 103

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Envoi . . . . . . . . . . . . . . . 107 Conclusions . . . . . . . . . . . . . . . . 108 References. . . . . . . . . . . . . . . . . 109 Appendix A. . . . . . . . . . . . . . . . . . . . . . . 113 Appendix B. . . . . . . . . . . . . . . . . . . . . . . 114 Vita Auctoris . . . . . . . . . . . . . . . . . . . . . 115

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LIST OF TABLES Table 1.1 Studies of the pubertal growth spurt in stature (years) . . . . . . . . . . . . 4 Table 1.2 Mean appearance of the adductor sesamoid in relation to the pubertal peak in height . . 21 Table 1.3 Epiphyseal-diaphyseal growth stages used by Bowden. . . . . . . . . . . . . . . . . . . 22 Table 1.4 Indicators of the hand and wrist used to predict the facial growth spurt . . . . . . 28 Table 1.5 Fishman’s sequence of Skeletal Maturation Indicators (SMIs) . . . . . . . . . . . . . 31 Table 1.6 Hassel and Farman’s stages of cervical vertebrae maturation. . . . . . . . . . . . 43 Table 1.7 Relationship between cervical vertebral and hand-wrist assessments of skeletal maturation. . . . . . . . . . . . . . . . . 45 Table 2.1 Onset and peak: Descriptive statistics for measures of size. . . . . . . . . . . . . . 81 Table 2.2 Hand-wrist (HW) and cervical vertebral (CV) stages: Distribution at onset and peak . . 88 Table 2.3 Average age at onset and peak: Comparison among skeletal measures by way of paired t-tests . . . . . . . . . . . . . . . . . . 91 Table 2.4 Statural growth (onset and peak): Concordance between actual ages and ages estimated from contemporary indices . . . . 92 Table 2.5 Mandibular growth (onset and peak): Concordance between actual ages and ages estimated from contemporary indices . . . . 93

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Table 2.6 Facial growth (onset and peak): Concordance between actual ages and ages estimated from contemporary indices . . . . 94 Table 2.7 Error Variances: Index peak age relative to actual peak age. . . . . . . . . . . . . 95 Table 2.8 Peak growth: Prediction error. . . . . . . 96 Table 2.9 Peak timing: Among-index differences in prediction error. . . . . . . . . . . . . . 97

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LIST OF FIGURES

Figure 1.1 The pubertal growth spurt as described by Hägg and Taranger . . . . . . . . . . . . . 7 Figure 1.2 Periodic changes in growth rate as described by Björk and Helm . . . . . . . . . . . . . 15 Figure 1.3 Fishman’s 11 Skeletal Maturity Indicators (SMIs), as described and numbered in Table 1.5 . . . . . . . . . . . . . . . . . 32 Figure 1.4 Lamparski’s Female Standards . . . . . . . 40 Figure 1.5 Lamparski’s Male Standards. . . . . . . . . 41 Figure 1.6 Cervical vertebral maturation indicators. . 44 Figure 1.7 Developmental stages of the cervical vertebrae as described by Franchi, Baccetti, and McNamara. . . . . . . . . . . . . . . . 50 Figure 1.8 The modified cervical vertebral maturation method, with five developmental stages (CVMS I-V) as described by Baccetti et al . 54 Figure 2.1 Six stages of cervical vertebrae maturation as described by Baccetti et al. . . . . . . 70 Figure 2.2 Cephalometric measures of facial size . . . 72 Figure 2.3 Gauge (not to scale) used to measure concavity depth on the lower border of the third cervical vertebra (C3). . . . . . . . 75 Figure 2.4 Average Statural Growth Curve--Males. . . . 82 Figure 2.5 Average Facial Growth Curve--Males. . . . . 83 Figure 2.6 Average Mandibular Growth Curve--Males. . . 84 Figure 2.7 Average Statural Growth Curve--Females. . . 85 Figure 2.8 Average Facial Growth Curve--Females. . . . 86

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Figure 2.9 Average Mandibular Growth Curve—Females . . 87 Figure 2.10 Growth in height of the son of the Count Montbeillard during the years 1759-1777 as plotted by Scammon. . . . . . . . . . . . . 99

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CHAPTER 1: REVIEW OF THE LITERATURE

Introduction

In 1927, Milo Hellman published a craniometric

study that laid the foundation for an understanding of the

pattern of facial growth.1 Hellman found that facial growth

undergoes periods of acceleration and deceleration, and,

overall, growth proceeds in spurts.2 He identified gender

differences in the timing, extent, velocity, and intensity

of facial growth and recognized that these changes result

in an increase in size and a change in the proportions of

the face.

Subsequently, many others have gone on to describe

the pattern of facial growth in greater detail. Further,

many orthodontists have noted that periods of rapid growth

have marked beneficial effects on orthodontic treatment,

especially for Class II malocclusions. Johnston, for exam-

ple, has noted that the normal pattern of Class II facial

growth causes the mandible to gain on the maxilla perhaps

nine times in ten, thereby helping to correct a Class II

malocclusion during conventional edgewise treatment.3,4

Bishara and colleagues also studied Class II subjects and

have observed that the normal pattern of growth would help

to correct this type of malocclusion.5

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If a goodly portion of the Class II correction can

be attributed to the normal pattern of facial growth, the

optimal time to treat a patient would be when the rate of

facial growth is highest. The importance of determining

the timing of this maximum rate has lead many investigators

to develop biological scales in hopes of finding reliable

predictors of the growth spurt.

The correlation between the timing of the facial

growth spurt and various sequential skeletal events has

been investigated for decades, and many methods have been

suggested in the hope of predicting the timing of the fa-

cial growth spurt. In this context, potential predictors

of growth-spurt timing range from chronological age to den-

tal development to ossification events in the skeleton.

Their utility, however, remains to be seen.

The goal of the present investigation is to compare

the various biological indices that are commonly used to

assess and predict the timing of the facial growth spurt

and to identify which of these indices, if any, are of use

in practice.

The Pattern of Skeletal Growth

Over the years, numerous investigations of skeletal

development have shown that children display a similar

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pattern of general skeletal growth. Growth proceeds in a

series of spurts, the normal pattern displaying a high rate

during early and middle childhood followed by a decreasing

rate in late childhood. This decreasing rate of growth

then undergoes another period of acceleration in adoles-

cence known as the “pubertal growth spurt.” Although the

pattern is similar from patient to patient, the timing var-

ies greatly.

The pubertal growth spurt is a marked adolescent

acceleration in the rate of growth. This spurt--a peak in

incremental growth--has been found to occur approximately

two years earlier in females than males, at mean ages of 12

and 14, respectively (Table 1.1). The overall skeletal

growth spurt has been identified by the maximum increment

in height, as this measurement of stature represents the

general growth of the skeleton.

Table 1.16-13 summarizes various estimates of the ex-

istence and timing of a pubertal growth spurt in males and

females. Many investigators have identified the average

age for each sex at both the onset and the peak of the

growth spurt and also the average duration of pubertal

growth. The most extensive longitudinal study of height

was performed by Hägg and Taranger, who studied 122 males

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Table 1.1. Studies of the pubertal growth spurt in stature (years).6-13 Author Year Sample Onset Peak Duration Bambha6 1961 25 M 11.57 14.17 2.60

24 F 9.26 11.86 2.60 Hunter7 1966 25 M 12.79 14.11 2.66

34 F 10.41 11.80 2.64 Björk & Helm8 1967 32 M . . 14.00 . . 20 F . . 12.60 . . Bergersen9 1972 23 M . . 12.98 . . Grave10 1973 52 M . . 13.80 . . 36 F . . 11.80 . . Bowden11 1976 47 M 12.00 13.91 3.42 50 F 9.99 11.67 2.89 Tanner et al.12 1976 55 M 12.05 13.91 1.86 36 F 10.30 11.89 1.59 Hägg & Taranger13 1980 122 M 12.08 14.07 4.97 90 F 10.04 11.98 4.78

and 90 females and estimated the average age of onset and

peak for statural growth.13 They reported an average age of

onset for females and males of approximately 10 and 12

years, respectively, with the peak coming two years later

in both sexes. Other studies employing smaller samples

have reported similar results, indicating that the onset

and peak for females occurs at 10 and 12 years; for males

12 and 14 years.

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Although the mean ages of the onset and peak of the

pubertal growth spurt are well established, great variation

exists in the timing of these events among individuals.

Hägg and Taranger (1982) found that males had a six year

range at both the onset and peak of the pubertal spurt,

whereas females had a seven and six year range at the onset

and peak, respectively.14 Hunter (1966) studied the timing

of the facial growth spurt relative to that of body height

and found a four-year range of onset for the pubertal

growth period in males and a five-year range in females.7

Other investigators have found similar variation in these

pubertal events. Thus, it would appear that a prediction

of the timing of the growth spurt based on chronological

age can have considerable error.8,9,14 It not clear, how-

ever, that other predictors can do better.

At least at the level of description, the form and

timing of the pubertal growth spurt has been studied exten-

sively for many decades. Tanner and associates described

the onset or “take-off point” of the pubertal growth spurt

as a local minimum, the point on a smoothed velocity curve

where deceleration turns to acceleration.12 Hägg and

Taranger defined the components of the pubertal growth

spurt as follows:

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Onset of the spurt (ONSET) is the smallest annual in-crement from which there is a significant continuous increase in growth rate to peak height velocity (PHV). ONSET is found by locating the smallest annual incre-ment from which there is a continuous increase in growth rate to PHV. The curve is then followed to-wards PHV until the growth rate has accelerated 10mm. ONSET will be represented by the annual increment which is next below or coincides with this growth rate. Peak height velocity (PHV) is the greatest an-nual increment during puberty. The end of the spurt (END) is the first annual increment after PHV below 20mm.13

The curve that describes these events is depicted

in Figure 1.1. From the above definitions of ONSET, PHV

and END, certain characteristics of pubertal development,

such as patterns of growth, ossification events in the hand

and wrist, and secondary sex characteristics, become easier

to identify in relation to the curve.13,14

The overall pattern of pubertal growth for males

and females is very similar; however, each sex possesses

unique traits. Females appear to have a higher velocity at

the onset of the spurt and a higher growth rate leading up

to the peak. Males display more growth during the spurt

and a longer period of pubertal growth.15,16 Gasser and

colleagues have studied extensively the characteristics of

growth in stature and have found that a small spurt is seen

in most children prior to the pubertal growth spurt. They

have named this period of accelerated growth the

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Figure 1.1. The pubertal growth spurt as described by Hägg and Taranger.13 A, the smallest annual increment from which there is a significant continuous increase in growth rate to PHV; ONSET, in their terminology is represented by an annual increment that equals or exceeds 10mm. “mid-growth spurt” and have identified its average age of

occurrence at approximately 7.7 and 7.5 years for males and

females, respectively.16,17 The gap between the mid-growth

spurt and the pubertal growth spurt is 1.1 years for males

and 0.3 years for females, thus creating potential

difficulty in identifying the onset of the pubertal spurt

in females, as the mid-growth spurt and pubertal spurt may

be continuous.

Although females may show a less well-defined onset

of their pubertal growth spurt, the maximum increment in

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height represents the overall skeletal growth spurt for

both genders. More to the point, this growth spurt in

stature may signal the occurrence of an adolescent spurt

elsewhere, such as an increase in the rate of growth of the

various facial dimensions (“facial growth spurt”).6,7,9,10,18-22

The Pattern of Facial Growth

The early studies of Hellman and Goldstein estab-

lished the general pattern of facial growth by analyzing

craniometric and cephalometric dimensions.1,2,23 Both found

that the face of the child undergoes periods of growth de-

celeration and acceleration--“spurts.” Goldstein reported

that, in males, the face shows its greatest increment of

growth between the ages of 3 and 5 years, and then rate de-

creases continually until 13 to 15 years, at which time the

face displays a marked, relatively brief spurt. Although

these were landmark discoveries contributions, their use of

cross-sectional structure could discriminate only the most

obvious changes throughout development. The individual

patterns cancelled each other and thus blurred many of the

details.

The early works on facial growth and the existence

of a pubertal spurt in stature led orthodontists to study

more closely the pattern of facial growth during

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adolescence. Ram Nanda studied the relative growth rates

of seven craniofacial dimensions from serial cephalometric

radiographs and compared these growth rates against an in-

cremental curve for body height.18 He studied 15 individu-

als, 10 males and 5 females, whose ages ranged from four to

twenty years. Relative increments were calculated at six-

month intervals, and the increments were plotted against

chronologic age at the mid-point of the interval to show

the average rate of growth. In his analysis, “The percent-

age rates of growth thus obtained were three-point smoothed

twice . . . to show the basic trend, which was obscured by

excessive fluctuations.”

Nanda noted that the facial growth curves had the

basic characteristics of skeletal growth curves, displaying

a decreasing slope through childhood and then interrupted

by a circumpubertal maximum. These maxima varied in their

time of onset and height for the various facial dimensions

of a given child, but each dimension underwent similar pe-

riods of acceleration and deceleration. He concluded that

the growth of the face tends to have its circumpubertal

maximum slightly later than general body height. In other

words, body height completes its adolescent growth sooner

than does the face. Although Nanda’s conclusions shed

light on the timing of a facial growth spurt in relation to

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a spurt in stature, his small sample argues against defi-

nite conclusions and provides no predictors of the timing

of the various growth stages.

The existence of a facial growth spurt during pu-

berty argues that the growth of the face proceeds in spurts

similar to growth in height. In a further investigation of

the relationship between facial growth and growth in stat-

ure, Bambha examined the relative growth rates of eight

craniofacial dimensions, with each measurement originating

at sella.6 The sample consisted of 25 males and 25 females,

each with serial cephalometric radiographs from one month

to 19 years of age. He observed that the peak growth rates

for the various facial dimensions occurred at the same time

in 68% of males and 80% of females, a spread that was not

as great as that reported by Nanda.18 Overall, his results

were similar to Nanda’s in that the peak in facial growth

occurs slightly after the peak in stature. Further, Bambha

reported that 80% of his subjects displayed their peak in

facial growth within 9 months of the peak in body height,

but the lack of measurements to describe the changing pro-

portions of the face limits the value of the relationship

he reported.

The use of cephalometric radiographs allows a de-

tailed longitudinal analysis of facial growth. Björk

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investigated the growth pattern of the mandible by using

metallic implants on 45 males.20 He found that a prepubes-

cent male exhibits approximately 3 mm of mandibular growth

per year, followed by a decrease to a prepubertal minimum

of roughly 1.5 mm. From this minimum, the pubertal spurt

begins and the mandible grows an average of 5.5 mm annually

until the pubertal maximum. Björk found that the prepuber-

tal minimum occurs at an average age of 11.75 years for

males, whereas the average age at the pubertal maximum is

14.5 years. By using the implant technique, Björk devel-

oped valid and reliable measurements of mandibular changes

during growth in males and confirmed that the growth of the

mandible is not regular during childhood and adolescence,

but rather that it proceeds in spurts.

Although Nanda and Bambha both observed a pubertal

spurt in facial growth that closely followed the growth in

stature, their studies failed to establish a predictable

relationship to the spurt in body height.6,18 In 1966,

Hunter analyzed seven craniofacial dimensions thought to

describe the changing proportion of the face during growth

and studied the correlation between facial growth, body

height, and skeletal maturation during adolescence.7 He

found that the pubertal growth spurt has the same duration

in males and females, with the majority (57%) of the

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12

craniofacial maxima coincident with body height. Most no-

tably, Hunter observed that mandibular length exhibited the

most consistent relationship to the growth in stature dur-

ing adolescence with a linear correlation of r=0.76.

Hunter’s sample size and variety of craniofacial measure-

ments show a more powerful relationship between facial

growth and growth in body height than did Nanda and Bambha;

however, Hunter also found considerable variation in his

sample, with 14% displaying facial maxima before the peak

in stature and 29% showing their facial maxima after the

peak in body height.

On average there seems to be a close relationship

between statural and facial-growth spurts: they either oc-

cur together or with the face closely following stature.

Bergersen studied 23 males and used seven craniofacial

measurements9 similar to those used by Hunter7 and found

that the facial growth spurt occurred during the same year

as the peak in height. He also noted that, when Bambha’s

results were subjected to a test of statistical signifi-

cance, the difference between the peak in facial growth and

the peak in stature was insignificant. Because 14 of 15

subjects in Nanda’s study were included in Bambha’s sample

of 25, their results may actually imply that the peak in

facial growth may in fact occur with the peak in stature.

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The foregoing studies indicate that the facial

growth spurt during puberty occurs around the time of the

spurt in skeletal growth; however, there is considerable

among-individual variation in the timing of the pubertal

growth. This variation complicates treatment timing and

implies a need to search for efficient means of predicting

the timing of the facial growth spurt.

Prediction of the Pubertal Growth Spurt

Chronological Age

The inadequacies of chronological age as a biologi-

cal indicator have been well documented over the years. In

1965, Francis Johnston’s group demonstrated a considerable

discrepancy between chronological and skeletal

age∗ at various times during development and reported that

the chronological timing of skeletal maturation displays

significant variation among children. Further, they con-

cluded that chronological age is an inefficient predictor

of developmental status.21 Bergersen also found that the

chronological age at the onset of the spurt had a range of

4.2 years, whereas skeletal age had a range of only 1.52

years.9 Fishman showed similar results in 1979, reporting a

∗ The skeletal age of an individual is usually determined by the relative level of maturation of the skeletal system and is based on the maturational status of markers within the skeletal system.24

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14

significant discrepancy between skeletal and chronological

age in the timing of facial growth, with only a small per-

centage of individuals demonstrating concurrence between

the two.25

Chronological age provides a convenient means of

evaluating a patient’s development, but its error argues

that there is room for improvement. Other indicators, such

as sequential developmental events occurring throughout the

skeleton, might provide a better means of assessing an in-

dividual’s developmental status.

Secondary Sex Characteristics

Numerous attempts have been made to use secondary

sex characteristics to predict the individual level of

maturation or the timing of the onset and peak of the pu-

bertal growth spurt. Björk and Helm identified menarche as

an important predictor of maturation in females and calcu-

lated the mean age of menarche at 13 years and 11 months,

with a standard deviation of nearly 1 year and a range of 4

years.8 On average, menarche occurred roughly 17 months af-

ter PHV, indicating that maximum pubertal growth had al-

ready occurred (See Fig. 1.2). Hägg and Taranger found that

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Figure 1.2. Periodic changes in growth rate as described by Björk and Helm.8 menarche occurs closer to PHV--approximately 1.1 years fol-

lowing the peak. They observed a standard deviation of

1.11 years and a range of 5.4 years.14 Both studies argue

that menarche is a highly reliable indicator that PHV has

passed. In males, Hägg and Taranger reported that the

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appearance of a pubertal voice and subsequently a male

voice occurs, on average, 0.2 years prior to PHV and 0.9

years after PHV, respectively, with both events exhibiting

a standard deviation of nearly 1 year and a range of 5

years.14

The correlation of menarche in females with growth

in body height and the face was investigated by Tofani in

1972.26 She evaluated four mandibular cephalometric dimen-

sions and plotted incremental growth curves for each man-

dibular measurement. Her results imply that most females

display maximum mandibular growth before menarche, with

menarche occurring in the decelerating phase of pubertal

growth. In girls who mature early, the maximum growth in-

crement of mandibular length occurs before menarche. For

late maturing girls, the maximum increment occurs after

menarche. Tofani found that the maximum increment in

height most frequently occurs before or coincides with the

maximum increment in mandibular length. These findings

demonstrate that the event of menarche most commonly occurs

after the majority of growth in height and the mandible has

taken place. Menarche, therefore, may be an indicator, but

it is not a useful predictor of the pubertal growth spurt

in females.

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To be an efficient predictor, an event should be

easy to observe and must occur at a relatively standardized

time prior to the growth peak. In a search for such a pre-

dictor, stature is perhaps the first measure that comes to

mind. It is also the simplest.

Stature

Body height is in effect an index representative of

overall skeletal growth, given that it represents changes

occurring throughout the entire skeleton. As has been dis-

cussed here, it has been studied extensively. The pubertal

spurt in height seems to mirror skeletal events in other

areas of the body, including the face.6-10,13,14,18,21,22,25,26

Height, therefore, might represent a skeletal measure that

can be used to predict the timing of the facial growth

spurt. To date, this application has not been explored to

any great extent.

There are other identifiable skeletal events that

might also be useful in assessment and prediction. Of

these, the most popular are based on the maturation of the

hand and wrist.

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The Hand and Wrist

Assessment of Maturation

At least in theory, some assessment of an individ-

ual’s skeletal age might provide a better evaluation of the

present stage of maturation and a more efficient prediction

of the timing of future events than would chronological age

or the appearance of secondary sex characteristics.8,9,14

Many different areas of the body have been studied in the

hope developing a method that can provide an accurate as-

sessment of development: the hand, foot, knee, elbow,

shoulder, and hip.27 Each of these sites shows a well-

defined progression of events during maturation--a biologi-

cal time scale. Of these structures, Todd imputed special

significance to the hand and foot:

Hand and foot each presents a bewildering array of features very unequal in their value as indicators of bodily maturation but all nevertheless useful for the purpose of recording progress.27

The hand and wrist conveniently possess many bones

and epiphyses that mature in a well-defined progression

over time and which are also easily evaluated on a single

radiograph. Todd created one of the first atlases describ-

ing the progressive maturation of the bones of the hand and

wrist. Todd’s atlas displayed male and female standards at

six-month intervals and also described specific maturity

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indicators characteristic of each age.27 Pyle, Waterhouse,

and Greulich extended the work of Todd by creating an atlas

of the hand and wrist that described key radiographic fea-

tures, including the appearance of ossification centers,

the outlines and contours of developing bones, and the com-

pletion of epiphyseal fusion.28

The Pyle, Waterhouse, and Greulich atlas consists

of a graded series of standard radiographs of children at

roughly thirty time points along the average maturity

scale. An individual’s hand-wrist radiograph is then com-

pared against these standards in an attempt to find the

closest match. The use of an atlas, however, is inherently

subjective. Interpretation can vary among observers, and

it can prove difficult to find an exact match with an item

in the standard series.

Tanner and associates developed a detailed, objec-

tive method of evaluating skeletal maturation by way of

hand-wrist radiographs.29 They improved the previous work

of Pyle, Waterhouse, and Greulich by focusing on stages of

individual bones, not the overall maturational status of

the hand and wrist. Their technique, the so-called “TW2

method,” assigns a series of bones in the hand and wrist an

age based on their maturation stages. An individual’s

skeletal age is then calculated from a system of weighted

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scores. This method has become the standard for evaluating

hand-wrist radiographs, in that it provides a more accurate

evaluation of skeletal maturation as compared to an atlas.

Hand-wrist maturation has become a standardized and

extensively studied method for the assessment of skeletal

age due to the sequence of recognizable developmental

stages and the ease with which radiographs can be obtained.

This progression of events might therefore provide not just

an assessment of developmental status, but in addition

might be used to predict in advance the patient’s growth

status during puberty.

Prediction of Stature

Given an evaluation of an individual’s skeletal age

from a hand-wrist film, Björk and Helm attempted to use

these data to predict the age of maximum pubertal growth in

body height.8 They analyzed the stages of the hand and

wrist around puberty and noted the importance of the adduc-

tor sesamoid of the thumb: “. . . they are the only con-

sistent ossification centers in the hand that appear near

puberty.”

Table 1.28,30 summarizes data on the appearance of

the adductor sesamoid in relation to the timing of peak

growth in stature. Although the sesamoid ossifies, on

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average, before maximum pubertal growth in females and

males, both Björk and Helm and Bowden have observed consid-

erable variation in the timing of the appearance of the

sesamoid. Björk & Helm observed that the ossification of

the sesamoid tends to precede or coincide with the maximum

increment in height; it indicates that maximum pubertal

growth is either imminent or has been attained. Further,

Bowden noted:

It would appear valid to assume in most individuals that on the appearance of adductor sesamoid adolescent peak stature velocity was imminent, however, this re-lationship is certainly not constant, varying in this group from 3.13 before to 0.59 years after.30

Table 1.2. Mean appearance of the adductor sesamoid in relation to the pubertal peak in height. Study Sample Time prior to peak (months) ___ Björk & Helm8 20 F 12 32 M 9 Bowden30 60 F 9 52 M 12 ___ Given that the appearance of the sesamoid does not

seem to offer any marked predictive advantage for the onset

of the adolescent growth spurt, Bowden analyzed epiphyseal

changes in the hand-wrist for indicators of adolescent

growth.11 He used Greulich and Pyle’s radiographic stages

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(Table 1.3) to stage the hand-wrist of 60 females and 50

males. Bowden found that Stage 6 in the middle phalanges

(progressing from the thumb to the fifth finger) occurs on

average just prior to the start of the adolescent growth

spurt and that Stage 7 in the distal phalanges occurs just

after the start. Stage 7 in the middle phalanges occurs on

Table 1.3. Epiphyseal-diaphyseal growth stages used by Bowden.11

Epiphysis compared to diaphysis Radiological Stage

(Greulich & Pyle)

_ No ossification 1 Initial Ossification 2 Epiphysis 1/3 width of shaft 3 Epiphysis ½ width of shaft 4 Epiphysis ¾ width of shaft 5 Epiphysis equals width of shaft 6 Epiphysis caps diaphysis 7 Epiphysis fusion begins 8 Epiphyseal fusion complete 9 Adult 10 ___ average just before the peak in adolescent growth, whereas

Stage 8 in the distal phalanges occurs just after the peak.

Stage 8 in the middle phalanges occurs on average just be-

fore the end of the pubertal spurt, and Stage 9 in the dis-

tal phalanges occurs just after the end of the spurt.

Bowden reported that, during the stages of the adolescent

spurt (Stages 6-9), females had standard deviations ranging

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from 0.55–0.85 years, whereas males showed standard devia-

tions from 0.52–0.99 years. Bowden also observed that the

growth stages showed sexual dimorphism in both the chrono-

logical and skeletal ages, females beginning their adoles-

cent growth spurt not just at an earlier chronological age,

but also at an earlier skeletal age.

The hand and wrist undoubtedly progress through

well-defined stages during the adolescent growth spurt;

however, the reliability of these events in terms of growth

prediction remains to be demonstrated. Hägg and Taranger

looked more closely at hand/wrist events surrounding the

pubertal growth spurt and defined the onset, peak, and end

of the pubertal spurt on an unsmoothed incremental curve of

height (See Fig. 1.1).13,14 They focused on three sites in

the hand as maturity indicators: the sesamoid, the middle

phalanx of the third finger, and the distal phalanx of the

third finger.

Hägg and Taranger reported that, if the sesamoid is

not visible, peak height velocity (PHV) has not yet been

reached. If the sesamoid had just become visible, then

most adolescents would be in the accelerative period of the

spurt. If the epiphysis and the diaphysis of the middle

phalanx of the third finger are not equal in width, then

PHV has not yet been attained; however, if they are equal

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24

in width, then the individual is probably in the accelera-

tive period. If the epiphysis is “capping” the diaphysis,

then PHV is imminent or has been attained. If the epiphy-

sis and diaphysis of the distal phalanx of the third finger

are fused, then PHV has already occurred.

In all three of the sites studied, both females and

males showed a standard deviation at PHV of approximately

1.0 year. The events studied by Hägg and Taranger were

said to be better predictors of the pubertal growth spurt

than those of Björk and Helm8; however, their presence at

best will indicate that a patient is already in the accel-

erative period of the spurt, and thus beyond the point at

which “prediction” would have any meaning.

Subsequently, in 1982, Hägg and Taranger analyzed

their data more closely and concluded that the hand stages

listed previously were reliable maturation indicators for

PHV and the end of the pubertal spurt (END), but not for

the onset of the spurt (ONSET). In other words, ossifica-

tion of the sesamoid is not a reliable indicator of ONSET

in either sex and cannot effectively predict the timing of

PHV.

Events in the hand and wrist are indicators the

peak and end of the pubertal growth spurt, but do not sig-

nal the onset of the pubertal growth spurt. Thus, the

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25

hand-wrist radiograph may be helpful in assessing a pa-

tient’s present developmental status; however, an assess-

ment of the present is very different from a prediction of

the future.

Prediction of Facial Growth

Because it has been shown that there is a temporal

relationship between the pubertal growth spurt in stature

and the hand-wrist maturation and also between the pubertal

growth spurt in stature and the facial growth spurt, inves-

tigation of the correlation between hand-wrist events and

the facial growth spurt is a logical next step. Bambha and

Van Natta continued Bambha’s earlier work on the relation-

ship between adolescent facial growth and skeletal matura-

tion by examining hand-wrist films.19 They used Sella-

Gnathion increments to define the pattern of facial growth

during adolescence and compared them to the skeletal devel-

opment of the hand and wrist around the time of the spurt.

Bambha and Van Natta analyzed males and females

separately and divided them into groups based on early or

late skeletal maturation to show a difference between

chronological and skeletal age. An attempt was made to

predict the maximum growth increment by subtracting chrono-

logical from skeletal age. They found that an individual

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26

who matures early has an advanced skeletal age and an early

facial growth spurt; a delayed skeletal age, a late facial

growth spurt. Bambha thus pointed out an association be-

tween skeletal maturation and facial growth during adoles-

cence at the two extremes; however, the large group between

the early and late maturers was highly variable. Bambha

concluded, “It should be pointed out that while the statis-

tics demonstrate the general trend, there is enough indi-

vidual variation to make the orthodontist’s predictions on

a given patient less than perfect.”

Many of the studies that have examined the correla-

tion between the facial growth spurt and growth in body

height also have analyzed skeletal age and its predictive

significance. Hunter reported that females display a

greater variation in skeletal age at PHV than males and, at

the end of the year of maximum facial growth, his female

sample had completed a greater percentage of its final fa-

cial size.7 In terms of prediction, Hunter observed that

some individuals progress rapidly through adolescence,

whereas others progress slowly, thereby making it difficult

to identify the status of a child’s facial-growth status

from a single radiograph.

In an investigation of the relationship between the

facial growth spurt and the spurt in stature, Bergersen

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27

(1972) devised a prediction table based on skeletal and

chronological age and found that prediction of the facial

spurt was accurate for early and late maturers but not av-

erage maturers9, a finding that mirrors the earlier observa-

tions of Bambha and Van Natta.19 Bergersen found that the

chronological and skeletal ages of average maturers did not

differ significantly, and thus skeletal age did not confer

any predictive advantage in the average maturing male.9

Table 1.4 summarizes indicators of the hand and

wrist that have been shown to correlate significantly with

the timing of the facial growth spurt. Bergersen reported

that the appearance of the adductor sesamoid is highly cor-

related with the initiation of the spurt in males, but his

small sample argues for caution in using the sesamoid in

predicting the pubertal growth spurt. Tofani reported that

onset of fusion in the distal phalanges appeared to be the

best predictor of the pubertal spurt of growth in the man-

dible; however, the onset of fusion in the distal phalanges

most often occurs within a month of menarche, too late to

be of use in predicting mandibular growth and timing treat-

ment.26

Grave explored further the relationship between

skeletal events in the hand and wrist and growth spurts in

stature and the face.10 His data indicate a strong

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Table 1.4. Indicators of the hand and wrist used to predict the facial growth spurt Number Indicator Author (Year) (Males/Females) Onset Peak End _ Bergersen (1972)9 23/0 Sesamoid . . . . Tofani (1972)26 0/20 . . Onset of fusion in . . distal phalanges Grave (1973)10 52/36 . . Sesamoid . . Grave & Brown (1976)22 52/36 PP2 & MP3 Sesamoid, DP3, PP3, Epiphysis=Diaphysis MP3 cap & MP3 union _

28

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29

correlation between the peak in height and the appearance

of the sesamoid and a moderate association between the peak

in the face and the appearance of the sesamoid. Grave con-

cluded, “sesamoid ossification indicated that the peak

growth velocity had occurred or was imminent.” Again,

these results demonstrate that, although the sesamoid may

serve to identify the peak in pubertal growth, the large

period of growth acceleration approaching the peak will

have been missed.

In 1976, Grave and Brown observed that the ossifi-

cation of the sesamoid and capping in the middle phalanx of

the third finger had strong, nearly identical correlations

with peak growth in stature.22 Their findings agree with

those of Bowden11 and identify Stage 6 as occurring near the

start of the adolescent growth spurt. Although the age-

range around this event was quite large (2.0-3.2 years

prior to the peak), it may possibly be of use in predicting

the onset of the facial growth spurt.

The consistent sequence of events in the hand and

wrist during adolescence implies a potentially useful rela-

tionship with stages of pubertal growth. In 1979, Fishman

began to examine the diagnostic value of skeletal age as

opposed to chronological age in evaluating an orthodontic

patient’s progression of skeletal and facial growth.25 He

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30

analyzed longitudinally seven craniofacial dimensions in 60

males and 68 females between the ages of 7.5 and 15 years

for a total of 382 records. Fishman assigned each patient

a skeletal age based on the corresponding hand-wrist film

and also recorded each patient’s height and chronological

age. He found that chronological and skeletal ages were

not coincident in the majority of individuals and that a

significant discrepancy between chronological and skeletal

age would have a great impact on the prediction of the tim-

ing of facial growth.

Based on the discrepancy between chronological and

skeletal age and the progression of osseous changes in the

hand and wrist, Fishman established a system of skeletal-

maturation assessment based on four stages of bone matura-

tion at six anatomical sites in the hand and wrist.15

Fishman developed 11 Skeletal Maturation Indicators (SMIs)

encompassing the entire period of adolescent development

(Table 1.5 and Figure 1.3).15

Fishman studied height, hand-wrist films, and

cephalometric radiographs of a longitudinal sample of 32

males and 36 females from the Denver Child Research

Council. He also analyzed the hand-wrist radiographs of a

cross-sectional sample of 550 males and 550 females under

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31

Table 1.5. Fishman’s sequence of Skeletal Maturation

Indicators (SMIs).15

SMI Event ____

1 Epiphysis = diaphysis in 3rd finger, proximal phalanx

2 Epiphysis = diaphysis in 3rd finger, middle phalanx

3 Epiphysis = diaphysis in 5th finger, middle phalanx

4 Ossification of the adductor sesamoid of the thumb

5 Capping of the epiphysis in 3rd finger, distal phalanx

6 Capping of the epiphysis in 3rd finger, middle phalanx

7 Capping of the epiphysis in 5th finger, middle phalanx

8 Fusion of epiphysis and diaphysis in 3rd finger, distal phalanx

9 Fusion of epiphysis and diaphysis in 3rd finger, proximal phalanx

10 Fusion of epiphysis and diaphysis in 3rd finger, middle phalanx

11 Fusion of epiphysis and diaphysis in radius ____

going orthodontic treatment to establish age standards for

the 11 SMIs. From the longitudinal data, he studied four

cephalometric measures--two maxillary (Sella-A point and

Articulare-A point) and two mandibular (Sella-Gnathion and

Articulare-Gnathion)--to evaluate facial growth in relation

to growth in stature. Fishman found that the percentage of

growth completed at SMI 6 was similar for both sexes, with

the maxilla, mandible, and stature all having completed ap-

proximately 50% of their total growth. After SMI 6, the

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32

Figure 1.3. Fishman’s 11 Skeletal Maturity Indicators (SMIs), as described and numbered in Table 1.5. Adopted from Fishman.15

maxilla and mandible tended to lag behind stature until the

end of adolescence, at which time they tend to catch up.

The females in Fishman’s sample attained PHV at SMI

5 and peak in maxillary velocity at SMI 6. The peak in

mandibular velocity was not as obvious. Fishman noted that

the peak was at SMI 6; however, his table 5 indicated that

the peak was at SMI 7. For the males, PHV occurred at SMI

6 and the peak in maxillary and mandibular velocity oc-

curred at SMI 7. Fishman concluded that the mandible and

maxilla peak later than stature and that stature completes

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33

a greater percentage of its growth in middle and late ado-

lescence. Further, the patterns of growth were similar in

the maxilla and mandible, with the mandible trailing the

maxilla slightly until the late stages of growth.

Fishman observed that there is considerable among-

individual variation in the time-intervals between SMIs.

Thus, each individual has a maturational schedule that var-

ies in its acceleration and deceleration, a finding that

seems to argue for the use of skeletal rather than chrono-

logical age:

The findings support the general conclusion that organization of the data on a maturational basis provides a more homogeneous grouping than grouping chronologically.

Although Fishman based these conclusions on the

data from a longitudinal sample, he did not report the

variance between the chronological and maturational groups.

When he developed the age standards for his 11 SMIs,

Fishman found a standard deviation of approximately 1 year

for each SMI in males and females, a value larger than that

reported by Bowden.11 Fishman claimed that the sequence of

SMIs is exceptionally stable and reported only 3 deviations

in the sequence in an evaluation of 2000 hand-wrist radio-

graphs; however, he failed to validate his method with an

independent sample and his facial measurements analyzed

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positional changes of the maxilla and mandible, not actual

facial growth.

In 1987, Fishman tested the predictive significance

of his system of skeletal maturation on a cross-sectional

sample of 4,000 hand-wrist films (2225 females and 1775

males).31 The males and females were each divided into SMI

groups and then placed into early, average, or late matur-

ing groups based on their deviation from the average. In

order to demonstrate rates of maturation, Fishman defined

SMI 1-4 as representing accelerating growth velocity, SMI

4-7 displaying high-velocity skeletal growth, peak veloc-

ity, and intense periods of acceleration and deceleration,

and SMI 7-11 showing decelerating growth.

Fishman tested the accuracy of the SMIs for matura-

tional prediction and reported a prediction success rate of

greater than 80%, a value that he considered exceptionally

high for a biologic system. The SMIs however, were not

predicted individually. Instead, Fishman tested within and

among the SMI groups 1-4, 4-7, and 7-11 and found that the

highest error occurred in the period involving high growth

velocity. These results showed that prediction of an indi-

vidual’s maturational status is better early and late in

adolescent growth, as the individual approaches the spurt

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and completes growth, but is worse when the patient is ac-

tually in the pubertal growth spurt.

Although some investigators have found a degree of

correlation between skeletal maturation events and the pu-

bertal growth spurt, others have found less convincing evi-

dence of a useful relationship. Houston and colleagues

argued that, because PHV is easy to identify, it is com-

monly used to study the timing of the adolescent growth

spurt; however, because the velocity during the pubertal

growth spurt is greater than at any other time in which or-

thodontic treatment may take place, there are great bene-

fits to treating the patient from the onset instead of at

PHV.31 Houston’s group noted the importance of focusing on

“ossification events” instead of “bone stages,” for a more

accurate prediction of skeletal development. In their ter-

minology, bone stages last for an appreciable period of

time, whereas ossification events occur quickly and mark

the transition point from one bone stage to another. Ossi-

fication events, therefore, may offer a better-defined re-

lationship to an event such as PHV.

In an attempt to predict the timing of onset to

peak height velocity, Houston and co-workers studied 64

males and 49 females over a time period that included the

pubertal growth spurt. In this study, the interval between

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radiographs was six months up to puberty; three months dur-

ing puberty; and a year after puberty. Because an ossifi-

cation event is assumed to have occurred halfway between

serial radiographs, the shorter interval increases the pre-

cision of the prediction.

For the timing of the spurt, the best correlation

(males, r=0.92 and females, r=0.83) reported by Houston’s

group was for maturation events that took place at or after

PHV. Multiple ossification events were combined in an at-

tempt to improve the prediction, but the prediction was

only as good as the best predictor in the group. Because

no events were found to be of predictive significance one

to two years in advance of PHV, the maturation of the hand

and wrist proved to be of limited utility. Houston and co-

workers concluded that the accuracy of prediction as ex-

pressed by confidence limits is so low that it would be

only of limited value at a clinical level. They agreed

with Björk, stating, “single bone stages can be used to in-

dicate that the growth spurt has not yet started or that it

has passed, or that growth is nearly complete.”

In 1980, Houston studied 68 males and 58 females to

analyze more closely the skeletal events during the puber-

tal spurt.32,33 He again found that ossification events in

the hand and wrist are not of predictive significance for

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PHV; however, he noted that prediction improves as the av-

erage age of the pubertal growth spurt is approached.

Houston’s observations suggest that skeletal age as deter-

mined by the hand and wrist does not offer any advantage

over chronological age in the prediction of the timing of

peak growth.

On balance, there seems to be general agreement

that the peak of the growth spurt is correlated with cer-

tain well-defined stages, such as appearance of the sesam-

oid; however, events that can give advance notice of the

onset of the spurt have not been identified. Although ra-

diographs of the hand and wrist have failed to generate ef-

ficient predictions for the onset of the spurt, the

evidence of a progression through well-defined, skeletal

maturation stages during puberty has led to the study of

other areas of the body. For orthodontists, the cervical

vertebrae not only undergo well-defined changes, but also

are visible on a routine lateral cephalograms.

The Cervical Vertebrae

Assessment and Prediction of Stature

Lamparski investigated a cross-sectional sample of

72 females and 69 males from ten to fifteen years of age

and developed a series of standards for the assessment of

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skeletal age based on the second through sixth cervical

vertebrae (C2-C6).34 Lamparski separated females and males

and arranged the lateral cephalograms for each age in a se-

ries from least to most mature based on vertebral develop-

ment. He then chose the median radiograph of each series

as the standard of development for that particular age.

The standards for each chronological age were then arranged

to provide a series of standards (See Figures 1.4 and 1.5).

Lamparski identified two specific maturity indicators on

the cervical vertebrae to assist in the evaluation: the

initiation and development of concavities on the lower bor-

der of the vertebral body, and the increase in height of

the vertebral body, from tapered, to rectangular, to

square, to higher than wide.

In order to validate his vertebral standards as a

means of assessing maturation, Lamparski compared them to

hand and wrist stages and found no significant difference

between the two methods. The standards for males and fe-

males were the same, but the females matured earlier.

Lamparski concluded that the vertebral standards could be

used to assess skeletal age accurately. This conclusion,

of course, begs the question of the clinical significance--

the predictive significance--of skeletal age, itself.

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From the standpoint of assessing maturation,

Lamparski’s method has several shortcomings. Firstly, a

cross-sectional sample is relatively insensitive to the

individual variability seen easily in a longitudinal sam-

ple. Secondly, Lamparski’s standards round to the next

whole year, and thus do not estimate skeletal age in

months, as is done with the hand-wrist assessment. Al-

though Lamparski claimed that his vertebral standards were

as accurate as the hand-wrist for the assessment of skele-

tal age, he did not compare his standards to a method that

outlines specific developmental events in the hand and

wrist. Thus, he failed to relate cervical vertebral

changes to common skeletal events of pubertal growth.

Hellsing has demonstrated that the vertebral dimen-

sions of fifteen year-old males are significantly shorter

than comparable dimensions in adult males.35 The difference

in vertebral dimensions between adult and 15 year-old males

indicates that the majority of 15 year-old males still pos-

sess significant remaining growth. Lamparski’s male stan-

dards, therefore, do not encompass the entire period of

pubertal growth and may not completely define the vertebral

changes of an adolescent male. The cervical vertebrae pro-

vided an easier means of assessing the skeletal maturation

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Figure 1.4. Lamparski’s Female Standards. Adopted from

Lamparski.34

11 years A concavity has devel-oped in the inferior border of the second vertebra. The anterior vertical heights of the bodies have in-creased.

13 years The concavity of the third vertebra has in-creased and a definite concavity has formed on the fourth vertebra. Concavities on the fifth and sixth vertebrae are just beginning to form. All bodies are now rec-tangular in shape.

15 years All bodies have in-creased in vertical height and are higher than they are wide. All concavities have deepened.

10 years All inferior borders of the bodies are flat. The superior borders all taper excessively from posterior to ante-rior.

12 years A concavity has devel-oped in the inferior border of the third ver-tebra. The remaining inferior borders are still flat.

14 years The spaces between the bodies are visibly smaller. Concavities are now well defined on all six bodies. The bodies are now nearly square in shape.

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Figure 1.5. Lamparski’s Male Standards. Adopted from

Lamparski.34

10 years All inferior borders of the bodies are flat. The superior borders all taper excessively from posterior to ante-rior.

13 years A concavity has devel-oped in the inferior border of the third ver-tebral body. The ante-rior vertical heights have increased further.

11 years A concavity has just begun to develop in the inferior border of the second body.

12 years The concavity of the second vertebra has deepened. The ante-rior vertical heights of the bodies have in-creased.

15 years The spaces between the bodies are visibly smaller. The concavity on the fourth body has deepened and ones are developing on the fifth and sixth bodies. The bodies are almost square in shape.

14 years The concavity in the third body has deep-ened and one has be-gun to develop in the fourth body. The bod-ies are now rectangu-lar in shape.

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of an individual, but use of this method to predict the

timing of growth remains unvalidated.

Hassel and Farman applied Lamparski’s standards to

a cross-sectional sample of 220 subjects from the Bolton-

Brush Growth Study Center to investigate further the

changes in the cervical vertebrae.36 They placed 10 females

and 10 males into each of eleven groups corresponding to

Fishman’s SMIs and then paired each subject’s tracings of

the second to fourth cervical vertebrae with the corre-

sponding hand-wrist film. Hassel and Farman identified six

stages of vertebral maturation and created an index that

defined more thoroughly the changes in the vertebrae (See

Table 1.6 and Fig. 1.6). Because Hassel and Farman matched

the vertebral stages with Fishman’s SMIs, an evaluator pre-

sumably could estimate an individual’s remaining growth po-

tential from the vertebrae.

The drawbacks of this investigation lie in its

cross-sectional design and its compression of Fishman’s

SMIs. Again, the use of a cross-sectional sample again

blurs the individual variability seen in a longitudinal

sample, and, when Hassel and Farman condensed Fishman’s 11

SMIs into six cervical vertebrae maturation categories,

they may have reduced the discriminating power of the in-

dex.

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Table 1.6. Hassel and Farman’s stages of cervical vertebrae maturation.36 Stage Description 1. Initiation Very significant amount of adolescent growth expected C2, C3, and C4 inferior vertebral body borders are flat. Superior vertebral borders are tapered posterior to anterior. 2. Acceleration Significant amount of adolescent growth expected. Concavities developing in lower borders of C2 and C3. Lower border of C4 vertebral body is flat. C3 and C4 are more rectangular in shape. 3. Transition Moderate amount of adolescent growth expected

Distinct concavities seen in lower borders of C2 and C3. C4 developing concavity in lower border of vertebral body. C3 and C4 are rectangular in shape.

4. Deceleration Small amount of adolescent growth expected

Distinct concavities in lower borders of C2, C3, and C4. C3 and C4 are nearly square in shape.

5. Maturation Insignificant amount of adolescent growth expected. Accentuated concavities on inferior borders of C2, C3, and C4. C3 and C4 are square in shape.

6. Completion Adolescent growth is completed. Deep concavities are present on inferior borders of C2, C3, and C4. C3 and C4 heights are greater than widths. ____

San Román and colleagues investigated the details

of this new classification and reported that, in comparison

to shape and height of the vertebrae, the concavity on the

lower border of the vertebral body had the highest correla-

tion with the hand-wrist evaluation.37 They concluded that

the best vertebral parameter from which to assess

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Figure 1.6. Cervical vertebral maturation indicators. Adapted from Hassel and Farman.36

maturation stages is when the concavity on the lower border

of the vertebral bodies is greater than 1 mm. Its utility

as a predictor, however, was not examined.

Table 1.737-43 summarizes the relationships reported

by various investigators between hand-wrist evaluation and

the cervical vertebral method for the assessment of skele-

tal maturation. Although many authors have reported strong

correlations between the methods and claimed that the ver-

tebral method is as accurate as the hand-wrist, others have

remained skeptical of the correlations and of the applica-

tion of the vertebral method.37-42

Kucukkeles’s group reported substantial inter-

observer variation in staging the cervical vertebrae, espe-

cially the stages that supposedly identify peak growth.39

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Table 1.7. Relationship between cervical vertebral (CV) and hand-wrist (HW) assessments of skeletal maturation.37-43 Sample Relationship between CV & HW

Author Hand-Wrist

(Males/Females) Total M/F Method

_

Agreement percentage (%) _ García-Fernandez et al.38 50/63 . . 96/92 Fishman Kucukkeles et al.39 81/99 74 . . / . . Fishman _

Correlation (r) __________________________________________________________________________________________ Mito et al.40 0/66 . . . . /0.87 TW2 San Román et al.37 428/530 . . 0.77/0.84 Grave & Brown Flores-Mir et al.41 27/52 0.72 . . / . . Fishman Grippaudo et al.42 48/42 0.80 0.70/0.84 Grave & Brown Uysal et al.43 213/290 0.86 0.78/0.88 Grave & Brown _

45

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Flores-Mir and associates studied the correlation between

the hand-wrist and cervical vertebrae in children with ad-

vanced, average, and delayed maturational levels (based on

hand-wrist evaluation by the GrowthTek Co.44) and observed

that each method could only predict around 50% of the other

method’s maturation assessment.41 They reported that the

developmental status of an individual influences the

strength of the correlation between the method; therefore,

they concluded, “assessment of skeletal maturation may be

valuable as an orthodontic research tool . . . but it has

limited predictive use in the individual patient.”

Uysal and co-workers compared the hand-wrist and

vertebral methods against chronological age in a Turkish

population and reported correlation coefficients of r=0.72

with the cervical vertebrae and r=0.79 with the hand and

wrist.43 They noted that both correlations were signifi-

cant, along with the correlation between the hand-wrist and

vertebral methods (r=0.86). Uysal’s group concluded that

the cervical vertebrae are useful indicators of skeletal

maturation; however, they did not analyze whether or not in

the sense of prediction the vertebrae and hand-wrist are

significantly better than chronological age.

Although the strong correlations in Table 1.7 would

seem to indicate that the cervical vertebrae are as

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accurate as the hand-wrist for assessing skeletal matura-

tion, none of the authors have shown that the vertebrae are

of predictive significance vis-à-vis facial growth. In or-

der to be of use as a predictor of pubertal growth in

clinical orthodontics, the cervical vertebrae must be vali-

dated not just against growth in height, but rather against

the longitudinal growth of the face.

Prediction of Facial Growth

Bernard utilized Lamparski’s standards in an at-

tempt to predict the timing of the facial growth spurt.45

He analyzed annual cephalograms of 19 males (10 to 17

years) and 19 females (9 to 15 years) from the Bolton-Brush

Growth Study Center. Bernard plotted four craniofacial

measurements against chronological age and staged the cer-

vical vertebrae according to Lamparski. He compared the

actual chronological ages at which the peaks in facial

growth occurred with the predictions based on the skeletal

age assessment from the vertebrae.

Bernard found considerable inter-observer error in

staging the vertebrae, with discrepancies of as much as

three years, and reported that the inherent error in

Lamparski’s standards made them inadequate for prediction.

Based on similar root mean squared errors (error standard

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48

deviations) for skeletal and chronological age prediction,

Bernard concluded that the cervical vertebrae offered no

marked advantage over chronological age for evaluating

skeletal age and that skeletal age may be of limited value

in facial growth-prediction. Although the cervical verte-

brae did not appear to offer predictive significance for

the facial growth spurt, Bernard’s conclusions must be con-

sidered provisional.

O’Reilly and Yaniello investigated the relationship

between stages of cervical vertebrae maturation and growth

changes in the mandible.46 Their sample consisted of annual

lateral cephalograms of 13 Caucasian females from the

Bolton-Brush Growth Study, ages ranging from 9 to 15 years.

Lamparski’s standards were used to stage each radiograph,

and incremental curves were plotted for each mandibular

measurement.

O’Reilly and Yaniello found significant variation

in mandibular length increments within the stages of cervi-

cal vertebrae maturation. Stages one, two, and three gen-

erally occurred prior to peak velocity, with stages two and

three occurring in the year preceding the peak in the ma-

jority of subjects. Stages four, five, and six generally

occurred after the peak. O’Reilly and Yaniello reported

that the peak should occur at 1.5 years after vertebral

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method Stage 2 (Stage 2 + 1.5). They did not, however, es-

timate the error variance of this predictor. Based on sig-

nificant increases in mandibular measurements between

stages three and four, O’Reilly and Yaniello concluded that

the cervical vertebrae may provide a clinically useful pre-

diction for mandibular growth, at least in females.

Although a prediction potential can be inferred,

these results beg the question of whether or not it is an

improvement over the efficiency of predictions from the

hand-wrist stages. An answer probably cannot be inferred

from O’Reilly and Yaniello’s limited sample.

McNamara and associates investigated mandibular

growth relative to cervical vertebral maturation and body

height in 15 females and 9 males from the University of

Michigan Elementary and Secondary School Growth Study.47

They modified Lamparski’s standards of vertebral maturation

(Figure 1.7) to allow for evaluation of males and females.

They traced lateral cephalograms of each subject for the 6

consecutive cervical vertebral stages (Cvs1-6). They re-

ported that 100% of males and 87% of females had their peak

in body height between Cvs3 and Cvs4; height and mandibular

length (Co-Gn) showed significant incremental increases

during this interval as compared to the previous interval,

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Figure 1.7. Developmental stages of the cervical vertebrae as described by Franchi, Baccetti, and McNamara.47 Arrows indicate key features in each stage. Adapted from O’Reilly and Yaniello.46 Cvs2 to Cvs3. McNamara’s group characterized the between-

stage differences by way of descriptive statistics, but

failed to report the error variance in their method in the

prediction of the timing of facial and statural growth.

They noted that the chronological age at Cvs3 ranged from

8.5-11.5 years in females and 10-14 years in males, thus

implying that chronological age would be an inaccurate pre-

dictor of skeletal maturation. They did not, however, show

that the use of the vertebral stages would be an improve-

ment.

The findings of McNamara’s group are said to sup-

port the validity of the cervical vertebral stages for

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evaluating individual skeletal maturity, as the greatest

increment in mandibular length corresponded to the greatest

increment in height, the most reliable indicator of overall

development. They stated, “The peak in statural height

during the interval from stage 3 to stage 4 corresponds to

the greatest increments in all dimensional and positional

mandibular measurements.” Despite their positive tone,

only two of the three mandibular measurements showed sig-

nificant increases at a p<.05 level between stages 3 and 4,

and their small sample calls into question the power of the

study.

Although the correlation between cervical vertebral

maturation and growth of the mandible seems open to inter-

pretation, McNamara and co-workers applied thin-plate

spline analysis** to model mandibular growth changes around

the pubertal spurt.48 They used the same sample as their

2000 study, and the results indicated significant morpho-

logical changes in the mandible during the growth interval

Cvs3-Cvs4, further strengthening their initial report that

maximum mandibular growth occurs between Cvs3 and Cvs4.

McNamara’s group also has reported that the average

** Thin-plate spline analysis is a process that interpolates a surface that is fixed at landmark points and subsequently creates a smooth line. If one imagines this surface as a thin metal plate, then this plate will take a shape in which it is least bent, i.e. it minimizes the quantity. This quantity is called the bending energy of the thin-plate spline.47

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incremental increase in mandibular length following Cvs3

was 5.4 mm, a figure that agrees with Björk’s findings of

5.5 mm of mandibular growth during the year of maximum

growth.20,49-51 They also observed that the vertebral stages

occur approximately one year apart during adolescence, with

a standard deviation of 1.08 years. Thus, Cvs2 should oc-

cur, on average, 1.0 to 1.5 years prior to the peak in man-

dibular growth; however, the use of Cvs2 as a predictor of

the facial and mandibular peaks has not been validated.

In order to validate their use of the cervical ver-

tebrae to predict mandibular growth, McNamara and col-

leagues studied 18 males and 12 females from the University

of Michigan Elementary and Secondary School Growth Study.52

They analyzed six consecutive, annual lateral cephalograms

and measured mandibular length (Co-Gn) on each longitudinal

series to determine the maximum yearly increment in man-

dibular growth during puberty. They then assigned verte-

bral stages to each of the six radiographs in the series

based on the mandibular measurements, with emphasis on the

shape and the presence of a concavity at the lower border

of C2, C3 and C4. They found that the progressive develop-

ment of a concavity in the lower border of the vertebrae

distinguishes one stage from the next, with the changing

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53

shape of the vertebrae providing a more detailed descrip-

tion.

McNamara and co-workers reported no statistically

significant distinction between the measurements that pre-

viously defined Cvs1 and Cvs2. Consequently, they combined

these two stages to yield Cervical Vertebral Maturation

Stage I (CVMS I), thereby condensing Lamparski’s six

stages of cervical vertebrae maturation into five (Figure

1.8). The new method reported that the peak in mandibular

growth occurs between CVMS II and CVMS III and that the pu-

bertal peak cannot be reached without the attainment of

CVMS I and CVMS II. This “improved” method simply redis-

tributes the vertebral stages, but still fails to offer a

prediction for the timing of mandibular growth.

In 2005, McNamara and co-workers modified their

vertebral method by expanding their previously condensed

version of five maturation stages back to six.50 Their sam-

ple was the same as that used in the 2002 study; however,

their statistics showed significant differences in the

stages of vertebral maturation. Specifically, in 2002,

23.3% of the individuals displayed a concavity in the lower

border of C2 at the first radiographic time point, a per-

centage that was statistically significant compared to

those individuals who did not display a concavity. In

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54

Figure 1.8. The modified cervical vertebral maturation method, with five developmental stages (CVMS I-V) as de-scribed by Baccetti et al.52

2005, however, only 7% of the same subjects were said to

possess a concavity in the lower border of C2 at the first

radiographic time point, a percentage that became non-

significant. This discrepancy caused the authors to revert

to the original six stages. They did not comment on the

statistical differences between the two studies.

Hand-wrist staging has long been the standard for

evaluating skeletal maturation, even though the stages ap-

parently have limited value in predicting the onset of the

pubertal growth spurt in stature and the face. The use of

the cervical vertebrae to predict mandibular growth has

been proposed by Baccetti, Franchi, and McNamara; however,

they evaluated vertebral stages after identifying the in-

terval of maximum mandibular growth and failed to test

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55

their method on an independent sample. More importantly,

they have not analyzed the prediction error of their method

relative to the timing of facial growth. In order to be

clinically useful, the cervical vertebrae must predict some

aspect of facial growth, not merely show a significant cor-

relation with some index of skeletal maturation.

Prediction of Facial Growth Increments

Recently, a number of workers have attempted to use

indices of maturation to predict future increments of

growth, rather than their timing. Sato and associates and

Mito and colleagues used linear regression equation models

to derive equations for the prediction of mandibular growth

from bone age via the TW2 method and secondly from cervical

vertebral stages.53,54 Initially, they analyzed 2 groups of

22 Japanese females before and after the pubertal growth

spurt. Although the average error was 2.14 mm, they con-

cluded that bone age estimated from hand-wrist films is

useful in estimating further individual growth potential.

Mito’s group studied 2 groups of 20 Japanese fe-

males in order to derive and test a formula for the predic-

tion of future mandibular growth from cervical vertebral

bone age. They found that the average error of the values

predicted by cervical vertebral bone age and bone age from

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56

the hand-wrist was essentially the same. They concluded

(my italics), “This method might be useful in treating or-

thodontic patients in the growth stage.” Mito’s group

claimed that their formulas are useful for predicting man-

dibular growth; however, the formula for cervical vertebral

bone age was only tested against the formula for bone age,

not against actual increments of mandibular growth.

Overview

Many workers have examined prediction of the peak

or future increments of mandibular growth by way of the

cervical vertebrae; however, the efficiency of vertebral

scales as a predictor has yet to be tested. The variation

in the statistics reported by Baccetti’s group and their

inconsistent staging methods raises questions about the ap-

plicability of their research to clinical practice. Moreo-

ver, O’Reilly and Yaniello and Baccetti and associates have

not tested their methods on an independent sample after

first identifying the time of maximum skeletal and facial

growth. Bernard attempted to predict the timing of the fa-

cial growth spurt from the cervical vertebrae, but found

that they were no more useful in his hands than chronologi-

cal age. On balance, it has yet to be demonstrated that

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57

the facial growth spurt can be predicted efficiently by any

contemporary cervical vertebral method.

Statement of Thesis

Normal growth is an important contributor to ortho-

dontic treatment during adolescence. According to the lit-

erature, there is a facial growth spurt that occurs during

puberty along with the maturation of the skeleton. The

literature suggests that skeletal age has less variation

than chronological age relative to the timing of this pe-

riod of rapid facial growth. Thus, skeletal age may offer

a valid assessment of maturational status.

Further, treatment during the facial growth spurt

would presumably improve its efficiency and effectiveness;

however, an efficient predictor of the timing of this im-

portant event has yet to be demonstrated. A prediction can

be derived from means (12 for girls, 14 for boys); however,

it is thought that the various indices of maturation might

fare better. Unfortunately, hand-wrist evaluation has

failed to provide a reliable predictor of the onset, as its

only significant events occur near the peak of the spurt.

Thus, it has been proposed that the cervical vertebrae per-

haps can be used to generate an accurate prediction of the

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58

timing and amount of facial growth. These suggestions,

however, have yet to be validated.

The purpose of the present investigation, there-

fore, is to examine the pattern of facial growth in a

large, longitudinal sample of males and females. Based on

individual growth curves of stature, facial size, and man-

dibular length, the average male and female incremental

curves will be calculated, and the onset and peak of the

pubertal growth spurt will be identified for each subject.

The correlation between the actual peak ages and common

maturation indices, such as chronological age, stature,

hand-wrist and cervical vertebral staging, will be examined

to test their ability to assess an individual’s current

progress toward maturity. Finally, the predictive signifi-

cance of the various defined stages of these indices will

be examined with respect to the timing of the individual

onset and peak of facial growth.

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Literature Cited

1. Hellman M. Changes in the human face brought about by development. Int J Orthod, Oral Surg, and Radiog 1927;13:475-516.

2. Hellman M. The face in its developmental career. Dent Cosmos 1935;77:685-699 and 777-787.

3. Johnston LE, Jr. A comparative analysis of Class II treatments. In: McNamara JA, Jr., Carlson D, Vig P, Ribbens K, editors. Science and Clinical Judge-ment in Orthodontics, Monograph No. 18, Craniofa-cial Growth Series, Center for Human Growth and Development, The University of Michigan. Ann Ar-bor, 1986.

4. Johnston LE, Jr. Growth and the Class II patient: ren-dering unto Caesar. Semin Orthod 1998;4:59-62.

5. Bishara SE, Jakobsen JR, Vorhies B, Bayati P. Changes in dentofacial structures in untreated Class II di-vision 1 and normal subjects: A longitudinal study. Angle Orthod 1997;67:55-66.

6. Bambha JK. Longitudinal cephalometric roentgenographic study of face and cranium in relation to body height. J Am Dent Assoc 1961;63:776-799.

7. Hunter CJ. The correlation of facial growth with body height and skeletal maturation at adolescence. An-gle Orthod 1966;36:44-54.

8. Björk A, Helm S. Prediction of the age of maximum pu-beral growth in body height. Angle Orthod 1967;37:134-143.

9. Bergersen EO. The male adolescent facial growth spurt: its prediction and relation to skeletal maturation. Angle Orthod 1972;42:319-338.

10. Grave KC. Timing of facial growth: A study of rela-tions with stature and ossification in the hand around puberty. Aust Orthod J 1973;3:117-122.

11. Bowden BD. Epiphysial changes in the hand/wrist area as indicators of adolescent stage. Aust Orthod J 1976;4:87-104.

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60

12. Tanner JM, Whitehouse RH, Marubini E, Resele LF. The adolescent growth spurt of boys and girls of the Harpenden growth study. Ann Hum Biol 1976;3:109-126.

13. Hägg U, Taranger J. Skeletal stages of the hand and wrist as indicators of the pubertal growth spurt. Acta Odontol Scand 1980;38:187-200.

14. Hägg U, Taranger J. Maturation indicators and the pu-bertal growth spurt. Am J Orthod 1982;82:299-309.

15. Fishman LS. Radiographic evaluation of skeletal matu-ration. A clinically oriented method based on hand-wrist films. Angle Orthod 1982;52:88-112.

16. Gasser T, Müller HG, Köhler W, Prader A, Largo R, Moli-nari L. An analysis of the mid-growth and adoles-cent spurts of height based on acceleration. Ann Hum Biol 1985;12:129-148.

17. Gasser T, Köhler W, Müller HG, Kneip A, Largo R, Moli-nari L, Prader A. Velocity and acceleration of height growth using kernel estimation. Ann Hum Biol 1984;11:397-411.

18. Nanda RS. The rates of growth of several facial compo-nents measured from serial cephalometric roentgeno-grams. Am J Orthod 1955;41:658-673.

19. Bambha J, Van Natta, P. Longitudinal study of facial growth in relation to skeletal maturation during adolescence. Am J Orthod 1963;49:481-493.

20. Björk A. Variations in the growth pattern of the human mandible: Longitudinal radiographic study by the implant method. J Dent Res, Supplement No. 1 1963;42:400-411.

21. Johnston FE, Hufham HP, Jr., Moreschi AF, Terry GP. Skeletal maturation and cephalofacial development. Angle Orthod 1965;35:1-11.

22. Grave KC, Brown T. Skeletal ossification and the ado-lescent growth spurt. Am J Orthod 1976;69:611-619.

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23. Goldstein M. Changes in dimensions and form of the face and head with age. Am J Phys Anthropol 1936;22:37-89.

24. Proffit WR. Contemporary Orthodontics. St. Louis: Mosby; 2000.

25. Fishman LS. Chronological versus skeletal age, an evaluation of craniofacial growth. Angle Orthod 1979;49:181-189.

26. Tofani MI. Mandibular growth at puberty. Am J Orthod 1972;62:176-195.

27. Todd TW. Atlas of Skeletal Maturation (Hand). St. Louis: Mosby; 1937.

28. Pyle SI, Waterhouse A, Greulich W. A Radiographic Standard of Reference for the Growing Hand and Wrist. Cleveland, OH: The Press of Case Western Reserve University; 1971.

29. Tanner JM, Whitehouse RH, Cameron N, Marshall WA, Healy MJR, Goldstein H. Assessment of skeletal maturity and prediction of adult height (TW2 method). Lon-don: Academic Press; 1983.

30. Bowden BD. Sesamoid bone appearance as an indicator of adolescence. Aust Orthod J 1971;2:242-248.

31. Fishman LS. Maturational patterns and prediction dur-ing adolescence. Angle Orthod 1987;57:178-193.

32. Houston WJ. Relationships between skeletal maturity estimated from hand-wrist radiographs and the tim-ing of the adolescent growth spurt. Eur J Orthod 1980;2:81-93.

33. Houston WJ, Miller JC, Tanner JM. Prediction of the timing of the adolescent growth spurt from ossifi-cation events in hand-wrist films. Br J Orthod 1979;6:145-152.

34. Lamparski D. Skeletal age assessment utilizing cervi-cal vertebrae. [Unpublished Master's Thesis] Pittsburgh: University of Pittsburgh; 1972.

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35. Hellsing E. Cervical vertebral dimensions in 8-, 11-, and 15-year-old children. Acta Odontol Scand 1991;49:207-213.

36. Hassel B, Farman AG. Skeletal maturation evaluation using cervical vertebrae. Am J Orthod Dentofac Or-thop 1995;107:58-66.

37. San Román P, Palma JC, Oteo MD, Nevado E. Skeletal maturation determined by cervical vertebrae devel-opment. Eur J Orthod 2002;24:303-311.

38. García-Fernandez P, Torre H, Flores L, Rea J. The cer-vical vertebrae as maturational indicators. J Clin Orthod 1998;32:221-225.

39. Kucukkeles N, Acar A, Biren S, Arun T. Comparisons be-tween cervical vertebrae and hand-wrist maturation for the assessment of skeletal maturity. J Clin Pediat Dent 1999;24:47-52.

40. Mito T, Sato K, Mitani H. Cervical vertebral bone age in girls. Am J Orthod Dentofac Orthop 2002;122:380-385.

41. Flores-Mir C, Burgess CA, Champney M, Jensen RJ, Pitcher MR, Major PW. Correlation of skeletal maturation stages determined by cervical vertebrae and hand-wrist evaluations. Angle Orthod 2006;76:1-5.

42. Grippaudo C, Garcovich, D., Volpe, G., Lajolo, C. Com-parative evaluation between cervical vertebral mor-phology and hand-wrist morphology for skeletal maturation assessment. Minerva Stomatol 2006;55:271-280.

43. Uysal T, Ramoglu SI, Basciftci FA, Sari Z. Chronologic age and skeletal maturation of the cervical verte-brae and hand-wrist: Is there a relationship? Am J Orthod Dentofac Orthop 2006;130:622-628.

44. Growth Tek. Available at www.growthtek.com. 2001.

45. Bernard DO. Predetermination of the time of the facial growth spurt utilizing the cervical vertebrae. [Unpublished Master's Thesis] Cleveland: Case Western Reserve University; 1976.

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46. O'Reilly MT, Yanniello GJ. Mandibular growth changes and maturation of cervical vertebrae--a longitudi-nal cephalometric study. Angle Orthod 1988;58:179-184.

47. Franchi L, Baccetti T, McNamara JA, Jr. Mandibular growth as related to cervical vertebral maturation and body height. Am J Orthod Dentofac Orthop 2000;118:335-340.

48. Franchi L, Baccetti T, McNamara JA, Jr. Thin-plate spline analysis of mandibular growth. Angle Orthod 2001;71:83-89.

49. Baccetti T, Franchi L, Cameron CG, McNamara JA, Jr. Treatment timing for rapid maxillary expansion. An-gle Orthod 2001;71:343-350.

50. Baccetti T, Franchi, L., McNamara JA, Jr. The Cervical Vertebral Maturation (CVM) method for the assess-ment of optimal treatment timing in dentofacial or-thopedics. Semin Orthod 2005;11:119-129.

51. Baccetti T, Franchi L, Toth LR, McNamara JA, Jr. Treat-ment timing for Twin-block therapy. Am J Orthod Dentofac Orthop 2000;118:159-170.

52. Baccetti T, Franchi L, McNamara JA, Jr. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. An-gle Orthod 2002;72:316-323.

53. Sato K, Mito T, Mitani H. An accurate method of pre-dicting mandibular growth potential based on bone maturity. Am J Orthod Dentofac Orthop 2001;120:286-293.

54. Mito T, Sato K, Mitani H. Predicting mandibular growth potential with cervical vertebral bone age. Am J Orthod Dentofac Orthop 2003;124:173-177.

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CHAPTER 2: JOURNAL ARTICLE

Abstract

Introduction: The timing of developmental events

in the hand and wrist and cervical vertebrae has been shown

to bear at least a moderate correlation with the peak

growth rate in height and the facial skeleton. The objec-

tive of this study was to compare the efficacy of these

skeletal events and chronological age in assessing and pre-

dicting the timing of facial growth. Subjects and Methods:

To serve as a gold standard against which to evaluate these

predictors, serial cephalograms from 100 normal, healthy

subjects (50 females and 50 males) from the Bolton-Brush

Growth Study Center in Cleveland, Ohio were analyzed. Each

of the 100 subjects had a series of at least 6 consecutive,

annual cephalograms between 6 and 20 years of age. Five

cephalometric measurements (S-Na, Na-Me, PNS-A, S-Go, Go-

Pog) were summed to characterize general facial growth, and

a sixth measurement, Co-Gn, was used to assess mandibular

growth. In all, 808 cephalograms were traced and analyzed.

For most time points, chronological age, height, and hand-

wrist films were available for analysis and comparison.

The hand-wrist films for each time point were staged ac-

cording to Fishman’s system; the cervical vertebrae, ac-

cording to the method of McNamara and associates. Yearly

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increments of general facial growth, mandibular growth, and

statural height were calculated for each subject, and sepa-

rate incremental growth curves were plotted against age.

To examine the ability of indices of maturation to assess

the presence of peak growth, the ages at onset and peak on

each growth curve were identified and compared with the

ages that the key indicators appeared on the hand-wrist and

vertebral scales. To test the predictive efficiency of

indices of maturation, the actual peak ages were compared

against predicted peak ages generated from statural onset,

vertebral stage CS2, and chronological age means. Results:

For females, the onset of the pubertal growth spurt in

height, facial size, and mandibular lengths females oc-

curred at mean ages of 9.78, 10.27, and 10.04 years, re-

spectively. The difference in timing between height and

facial size was statistically significant. In males, onset

occurred at mean ages of 12.43, 12.45, and 12.36 years for

height, the face, and mandible, respectively. In females,

the peak of the growth spurt in height, facial size, and

mandibular length occurred at 11.42, 12.02, and 12.00

years. Height peaked significantly earlier than both fa-

cial size and mandibular length. In males, the peak in

height occurred slightly (and statistically significantly)

earlier than the peaks in the face and mandible (14.49,

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66

14.85, and 14.84 years). Error variances derived from the

hand-wrist and cervical vertebral methods to estimate peak

growth were not significantly lower than estimates based on

chronological age in the face, height, and mandible. Error

variances based on statural onset to predict the peak of

the pubertal growth spurt in height, facial size, and man-

dibular length were significantly lower than prediction

based on the cervical vertebrae in males and significantly

lower than the cervical vertebrae and chronological age in

females. Conclusions: Skeletal age offers no value over

chronological age, either in assessing or predicting the

timing of pubertal growth. Stature offers a potentially

useful indicator to predict the timing of peak facial

growth.

Introduction

A major advance in the understanding of facial

growth came when Milo Hellman observed that the face under-

goes periods of acceleration and deceleration and that,

overall, growth proceeds in spurts.1,2 Today, it is gener-

ally accepted that treatment during the so-called “adoles-

cent growth spurt” increases the efficiency and

effectiveness of orthodontic treatment, especially for a

Class II malocclusion.3-5 For stature, the peak of the

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67

adolescent spurt is generally thought to occur at approxi-

mately 12 years in girls and 14 in boys. The onset of the

spurt occurs approximately two years before the peak.6-11

Although these mean ages serve as a rough guide to treat-

ment planning, there is considerable variation among indi-

viduals.11-14

Nanda15 and Bambha6 observed that the growth of the

face tends to have its circumpubertal maximum slightly

later than general body height; however, others have stud-

ied larger longitudinal samples and have reported that the

facial growth spurt is coincident with the spurt in stat-

ure.8,13,16 Longitudinal studies have demonstrated that the

pubertal growth spurt in height shows at least some corre-

lation with maturity indicators elsewhere in the body.

These indicators and the spurt in stature, therefore, might

prove useful in predicting the timing of the facial growth

spurt. Predictions based on stature are especially appeal-

ing, given that they can be measured as often as desired

with no risk of radiation exposure. To date, however, most

attention has been paid to various “bone-age” indices.

Due to the sequence of recognizable developmental

stages and the ease with which radiographs can be obtained,

hand-wrist staging is perhaps the most common method for

the assessment of skeletal age and developmental status.

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Many investigators, however, have found that several of the

key hand-wrist events (e.g. the appearance of the adductor

sesamoid) appear at or near the peak of the pubertal growth

spurt and thus are of little use in prediction of the

spurt’s onset.8,9,17-21 The fact that other areas of the

skeleton progress through a series of well-defined changes

during puberty has led orthodontists to look elsewhere in

an attempt to predict the pattern of facial growth.

The cervical vertebrae undergo well-defined changes

and are visible on routine lateral cephalometric radio-

graphs. Based on a study of these changes, Lamparski de-

veloped standards for adolescent males and females.22

Subsequently, Hassel and Farman developed a more detailed

method of staging the vertebrae.23 Along with Fishman’s

hand-wrist method, these techniques are said to permit an

assessment of an individual’s remaining growth potential.

The cervical vertebral stages correlate well with the

stages of the hand and wrist;24-29 however, this relationship

simply allows the assessment of an individual’s present de-

velopmental status and does not, of itself, offer a predic-

tion of future growth.

To predict the timing of the facial growth spurt,

Bernard applied Lamparski’s standards to a small longitudi-

nal sample.30 He concluded that the cervical vertebral

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69

stages offered no obvious advantage over chronological age.

Recently, however, several groups have shown a renewed in-

terest in vertebral staging.

Baccetti, Franchi, and McNamara modified Lampar-

ski’s standards in order to apply a single set of standards

to both males and females.31-33 In applying these new stan-

dards, they found that the peak in mandibular growth occurs

between their stages CS3 and CS4 (See Fig. 2.1) and that

the stages of vertebral maturation occur, on average, one

year apart. Thus, CS2 may offer a prediction for the tim-

ing of facial growth as it tends to precede the interval of

maximum mandibular growth by about a year.

As things stand, many methods have been advanced to

assess and predict the timing of adolescent growth; how-

ever, these methods are based on relatively small samples

and have not been validated against actual facial growth.

The purpose of the present investigation is to examine the

incremental growth curves of a large longitudinal sample of

males and females and to study the relationship between the

timing of peak events in stature, facial size, and mandibu-

lar length. The ability of common indices of maturation to

assess and predict the timing of the pubertal growth spurt

will be examined in considerable detail.

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Figure 2.1. Six stages of cervical vertebrae maturation as described by Baccetti et al.32

SUBJECTS & METHODS

Sample

The present study employed the serial records of

100 normal, healthy subjects (50 females and 50 males) ob-

tained from the records of the Bolton-Brush Growth Study

Center in Cleveland, Ohio. Because the main goal of this

study was to examine the individual pattern of growth, the

main criterion for inclusion was the availability of a

long, intact series of annual lateral cephalograms, hand-

wrist radiographs, and statural records. In all but a few

instances, the radiographs were taken at yearly intervals

(plus or minus thirty days). Every subject had a series of

at least 6 consecutive, annual cephalograms between 6 and

20 years of age. All subjects had either a Class I/Normal

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71

or Class II occlusion, and thus were assumed to have under-

gone a more or less “normal” pattern of growth.3-5 Three

females and 18 males had been treated orthodontically at

some point during the period of evaluation. The treat-

ments, however, were minimal, consisting mainly of space

maintenance and alignment of the anterior teeth. It is as-

sumed that this sort of intervention would have little

appreciable effect on the cephalometric measurements

employed here.

Initially, each series of films was chosen to

bracket the CS3 stage of vertebral development (vide in-

fra).32 Cephalometric analysis of the first 60 series

showed that CS3 frequently does not coincide with the

spurt. It was decided, therefore, to add more films to

many of the series in an attempt to ensure inclusion of the

facial growth spurt. Specifically, radiographs were added

back to age 8 for females and back to age 10 for males, if

not already included in the original CS3-centered films.

Radiographs were also added to the older end of the series

if the onset and peak of the facial growth spurt could not

yet be detected. Thus, the number of radiographs in the

100 series ranged from 6 to 11. In all, the present study

employed 808 cephalograms and the attendant statural and

hand-wrist data.

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72

Cephalometric Analysis

A small group of measures of height and depth were

used to quantify the facial growth of each subject

(Figure 2.2):

1. Nasion-Menton (Na-Me);

2. Sella-Gonion (S-Go);

3. Sella-Nasion (S-Na);

4. Posterior Nasal Spine-A point (PNS-A);

5. Gonion-Pogonion (Go-Pog); and

6. Condylion-Gnathion (Co-Gn).

Figure 2.2. Cephalometric measures of facial size.

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73

All lateral cephalograms were traced on 0.003”

matte acetate by 2 operators (Z.M. and L.J.; to ensure con-

sistency, the Z.M. tracings were also checked by L.J.). In

order to optimize validity and reliability, each series was

traced at a single sitting so that all structures could be

coordinated from one film to another; fiducials were used

to minimize random error between radiographs in a series.

The tracings then were digitized (Numonics digitizing

board, Model A30BL.H; Numonics Corporation,

Montgomeryville, PA) and analyzed with commercial digitiz-

ing software (Dentofacial Planner, Dentofacial Software, v.

7.02, Toronto, Canada). The radiographs of the Bolton

study were taken at the minimum individual mid-sagittal

plane to film distance. Thus, the average magnification

ranged from 7.4% at age 8 to 8.4% at age 18.34 It was as-

sumed that this small, systematic variation in magnifica-

tion would not alter the form of the curves generated here.

Five measurements (Na-Me, S-Go, S-Na, PNS-A, Go-

Pog) were summed to give an overall representation of fa-

cial growth. A sixth measurement, Co-Gn, was measured

separately to analyze mandibular growth relative to the

growth of the rest of the face.

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74

Vertebral Staging

On each cephalogram, the cervical vertebrae were

staged according to the six stages of vertebral maturation

described by Baccetti and co-workers (2005).32 This method

utilizes changes in shape of the vertebral bodies (C2-C4)

and changes in the lower border (a developing concavity) to

determine the stage of maturation. Both visual and cepha-

lometric analyses were used to stage the vertebrae, and

cephalometric landmarks were partially adopted from

Hellsing35 and McNamara and associates33 (Table 2.1). The

first three stages of cervical vertebrae maturation were

based on the depth of concavity in C2, C3, and C4. The

fourth, fifth, and sixth stages were based on the concavity

depths, ratios, and visual analysis.

San Román and associates26 reported that the concav-

ity on the lower border of the vertebrae is the most reli-

able parameter of maturation; they judged a concavity to be

present when its depth is greater than 1 mm. For the pre-

sent study, a gauge was constructed to measure the depth of

the concavity on the lower border of C3 (Fig. 2.3). The

gauge was aligned tangent to the most postero-inferior and

antero-inferior points on the body of C3; the depth of the

concavity was then measured against the millimeter mark-

ings.

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75

Figure 2.3. Gauge (not to scale) used to measure concavity depth on the lower border of the third cervical vertebra (C3).

Hand-wrist staging

For most of the series, hand-wrist films were

available at all ages. The hand-wrist films for each time

point were staged according to Fishman’s system of Skeletal

Maturation Assessment.36 All hand-wrist films were staged

by the principal investigator (Z.M.) and checked by a co-

worker (R.B.).

Error Study

With the aid of a table of random numbers accessed

online at www.random.org37 and generated by variations in

atmospheric pressure, 8 series (57 radiographs) were se-

lected and re-analyzed. Because there were 2 workers, each

redid two of their own series and 2 of their colleagues’;

thereby permitting an estimate of inter- and intra-observer

reliability. Intra-class correlation with Cronbach’s alpha

was employed to test the reliability of the cephalometric

measurements. “Adequate” reliability is generally taken to

mean an intra-class correlation of about 0.80 or greater.

1 mm

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Growth Curve Analysis

Yearly increments of general facial growth, man-

dibular growth, and statural height were calculated for

each subject, and separate growth curves were plotted

against intervals of chronological age (Microsoft Excel,

Microsoft Corp., Redmond, WA). The curves were smoothed

(spline interpolation line, Statistical Package for the So-

cial Sciences, SPSS Inc., version 14.0, Chicago, IL). For

each of the three curves, the onset of the growth spurt was

identified as the lowest increment--the local minimum--

immediately preceding a relatively continuous increase to

the peak, the maximum growth increment.

The corresponding chronological age, hand-wrist

stage, and vertebral stage were recorded for the onset and

peak of each curve (See Appendix). For many of the curves,

2 peaks were observed. If 2 peaks were separated by a

lesser increment, the average chronological age between the

two maxima was taken as the peak. This averaged maximum,

an average peak velocity, was used because it was assumed

that the area under the multiple peaks represents the total

peak growth, and thus was deemed more meaningful than the

area under just one peak. To qualify for averaging, the

multiple peaks had to be within 2 mm of each other on the

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facial-growth curve, 0.5 mm on the mandibular growth curve,

and 5 mm on the height curve.

On the smoothed curves, if onset or peak did not

coincide with a time point from the series, the age was

rounded to the nearest quarter-year. When onset or peak

occurred at a half or three-quarter year, the corresponding

hand-wrist and vertebral stages were taken from the next

time point. For seven subjects, height data were unavail-

able for portions of the series and thus neither onset nor

the peak could be identified.

For males and females, average growth curves were

plotted and smoothed for height, facial size, and mandibu-

lar length. In order to generate the curves, the individ-

ual peaks were aligned (registered) and the average

increments for each of the prior and succeeding intervals

were calculated. Intervals at the two tails that contained

fewer than 10 subjects were not included in the averaged

curves.

Statistical Analysis

Descriptive statistics were calculated with the aid

of a commercial spreadsheet program (Microsoft Excel).

Means, standard deviations, ranges, and confidence inter-

vals were calculated for the chronological ages at onset

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and peak of the spurts in facial growth, mandibular growth

and height. The means at onset and peak were compared us-

ing paired t-tests (SPSS, version 14.0, SPSS Inc., Chicago,

IL). Modes for the associated hand-wrist and vertebral

stages were calculated to identify the stage that occurs

most frequently for each method at the peak of the statu-

ral, facial, and mandibular curves.

Assessment of Maturation

Each index studied here features a stage at which

peak growth is said to occur. For the Fishman method, it

is Stage 5 for height and Stage 6 for the face in females

and Stage 6 for height and Stage 7 for the face in males.

For the cervical vertebrae, it is the mid-point between CS3

and CS4. In each series, the age at which these events oc-

curred was estimated by interpolation and compared with the

actual age of the spurt in stature, facial size, and man-

dibular length. In addition, mean ages inferred from the

literature (10 and 12; 12 and 14) were also tested for

their ability to assess maturational state.

Prediction

Two separate predictions of the peak were generated

from the vertebral method by using age at CS2 plus 1 and

1.5 years (CS2+1; CS2+1.5). Stature was used to predict

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the peak by using the age at onset plus 2 years. In addi-

tion, predictions were generated based on population means

derived from other studies: onset at 10 for girls and 12

for boys; peak at 12 for girls and 14 for boys.6,8-11,16

These estimations and predictions were compared with the

actual peak ages and correlations, root mean squared errors

(RMSE--error standard deviations) and mean squared errors

(MSE--error variances) were generated.

The error estimates were used to identify the best

predictor of facial growth timing. To discriminate among

these errors, Fmax and Cochran C tests were employed to test

for homogeneity of variance. Both tests provide critical

values based on the number of groups and sample size. When

the test value exceeds the critical value, it is considered

to be a statistically significant difference and indicates

heterogeneity among estimates of error. Because the Fmax

test has a slight positive bias and tends to reject the hy-

pothesis of homogeneity more frequently than it should,

α=.01, rather than the more common α=.05, was used in this

test.

The extreme (highest and lowest) MSE values at the

onset and peak were tested first for significance. If a

significant ratio was not seen, no further tests were per-

formed and the variances were assumed to be equal. If a

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significant difference was found, the next highest MSE was

compared against the lowest with an adjustment of the de-

grees of freedom until a non-significant comparison was en-

countered.

Results

Descriptive statistics for females and males at the

onset and peak of the pubertal growth spurt are summarized

in Table 2.1. The average male and female growth curves

for stature, facial size, and mandibular length can be seen

in Figures 2.4-2.9. Between sexes and among the three

measure of size, the curves display a similar shape, with

onset and peak clearly discernible on each curve. The fe-

males show a pre-adolescent spurt that closely precedes the

pubertal growth spurt, whereas males show a relatively con-

stant growth rate up to the onset of the spurt. In males,

the average yearly increment at the peak in height and the

mandible was 95.35 mm and 4.79 mm, respectively. In fe-

males, the average increment at the peak was 82.70 mm in

height and 3.88 mm in the mandible.

The hand-wrist and cervical vertebral stages pre-

sent at onset and peak of the growth spurt are summarized

in Table 2.2. Although it appears that certain stages have

a consistent relationship with onset and peak, the modal

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Table 2.1. Onset and peak: Descriptive statistics for measures of size

Statistic Measure Event

Mean S.D. Range 95% Confidence

Interval

Males

_

Stature Onset 12.43 0.98 10.00-14.00 12.16-12.70

Peak 14.49 1.03 13.00-18.00 14.20-14.78

Face Onset 12.45 1.08 10.75-16.00 12.15-12.75

Peak 14.85 1.14 12.25-18.00 14.53-15.17 Mandible Onset 12.36 1.27 10.75-16.25 11.98-12.74

Peak 14.84 1.12 12.50-18.00 14.53-15.15 _

Females

_ Stature Onset 9.78 0.98 8.00-13.00 9.51-10.05

Peak 11.42 0.99 9.50-14.25 11.15-11.69

Face Onset 10.27 1.19 8.00-14.00 9.94-10.60

Peak 12.02 1.16 10.25-15.25 11.70-12.34

Mandible Onset 10.04 1.12 8.00-14.00 9.73-10.35

Peak 12.00 1.24 10.00-15.50 11.69-12.31 _

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Figure 2.4. Average Statural Growth Curve--Males. Individual curves registered on their peaks. 0.00 corresponds to a mean age of 14.49 yrs. Note that Figures 2.5-2.10 have different x- and y-axis scales.

82

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Figure 2.5. Average Facial Growth Curve--Males. 0.00 corresponds to a mean age of 14.85 yrs.

83

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Figure 2.6. Average Mandibular Growth Curve—Males. 0.00 corresponds to a mean age of 14.84 yrs.

84

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Figure 2.7. Average Statural Growth Curve—Females. 0.00 corresponds to a mean age of 11.42 yrs.

85

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Figure 2.8. Average Facial Growth Curve—Females. 0.00 corresponds to a mean age of 12.02 yrs.

86

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Figure 2.9. Average Mandibular Growth Curve—Females. 0.00 corresponds to a mean age of 12.00 yrs.

87

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Table 2.2. Hand-wrist (HW) and cervical vertebral (CV) stages: Distribution at onset and peak

HW CV Event Measure

Mode Range Mode Range

Males

Onset Height 1(30%) 1-7 1(54%) 1-5 Face 2(31%) 1-7 1(60%) 1-4 Mandible 2(35%) 1-7 1(60%) 1-4 Peak Height 7(42%) 4-10 4(47%) 1-6 Face 7(36%) 3-10 4(34%) 1-6 Mandible 7(46%) 5-10 4(38%) 1-6

Females

Onset Height 1(32%) 1-6 1(64%) 1-4 Face 3(19%) 1-8 1(54%) 1-4 Mandible 2(21%) 1-7 1(64%) 1-4 Peak Height 7(30%) 3-8 2(28%) 1-5 Face 7(36%) 3-10 4(24%) 1-5 Mandible 7(28%) 3-10 4(30%) 1-6

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frequencies indicate a wide range of stages at the two time

points.

Paired t-tests indicate that, in males, peak in

stature is significantly earlier than peak in the face and

mandible (Table 2.3). For females, onset of the spurt in

height was found to be significantly earlier than the onset

in the face. The peak in height was also found to be sig-

nificantly earlier than peak in the face and the mandible.

The concordance between the ages of onset and peak

estimated from common indices of maturation and the actual

ages for statural growth, facial growth, and mandibular

growth are summarized in Tables 2.4, 2.5, and 2.6. Among

the three methods of assessment, the ages estimated from

the hand-wrist method show the best correlation and least

error at peak in both males and females. A comparison of

the three methods with the Fmax and Cochran C tests for ho-

mogeneity of variance are presented in Table 2.7. The Fmax

and Cochran C tests generally show agreement and homogene-

ity of variances; however, the Fmax test implies that, in

males, the error variances of the vertebral method and the

population mean are significantly greater than the error

variance of the hand-wrist method at peak of the facial and

mandibular spurts. In females, the Cochran C test indi-

cates that the error variance of the cervical vertebral

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method is significantly greater than the other methods at

peak of the statural spurt.

Table 2.8 lists the error variances and correlation

between the actual peak ages and predicted peak ages from

various indices. The prediction generated from onset in

stature plus 2 years shows the best correlation and least

error in both males and females. A comparison of the ac-

tual and predicted peak ages with the Fmax and Cochran C

tests is presented in Table 2.9. Overall, the two tests

show general agreement. In males, both predictions gener-

ated from the vertebral method show a significantly greater

variance than prediction generated from onset in stature,

except in the mandible, where the Fmax indicates that only

the CS2+1 prediction has significantly greater error. Also

in males, the variance of prediction based on mean age is

not significantly greater than prediction based on stature.

In females, the predictions generated from chronological

means taken from the literature and from the vertebral

method show significantly greater variances than prediction

generated from the onset in height. An exception is found

in stature, where Fmax indicates that only the vertebral

predictions show significantly greater error variances.

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Table 2.3. Average age at onset and peak: Comparison among skeletal measures by way of paired t-tests

Event

Comparison

Onset Peak

t p t p

Males

Height to Face 0.326 0.746 -4.163 0.001 Height to Mandible 0.325 0.747 -3.416 0.001 Face to Mandible 0.620 0.538 0.121 0.904

Females

Height to Face -3.544 0.001 -4.281 0.001 Height to Mandible -1.516 0.137 -3.693 0.001 Face to Mandible 1.453 0.152 0.139 0.890

*Bold denotes p <.01

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Table 2.4. Statural growth (onset and peak): Concordance between actual ages and ages estimated from contemporary indices

Statistic

Index

Onset(O) Peak(P)

RMSE RMSE r

Males

Mean (O:12; P:14)* 1.06 1.13 . . Hand-wrist (Stage 7) . . 0.97 0.63 Vertebrae (Stage 3.5) . . 1.30 0.49

Females

Mean (O:10; P:12)* 0.99 1.14 . . Hand-wrist (Stage 6) . . 1.22 0.50 Vertebrae (Stage 3.5) . . 1.67 0.46

*Means constant; no correlation possible

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Table 2.5. Mandibular growth (onset and peak): Concordance between actual ages and ages estimated from contemporary indices

Statistic

Index

Onset(O) Peak(P)

RMSE RMSE r

Males

Mean (O:12; P:14)* 1.31 1.39 . . Hand-wrist (Stage 7) . . 0.81 0.76 Vertebrae (Stage 3.5) . . 1.35 0.52

Females

Mean (O:12; P:14)* 1.11 1.23 . . Hand-wrist (Stage 6) . . 1.34 0.49 Vertebrae (Stage 3.5) . . 1.64 0.33

*Means constant; no correlation possible

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Table 2.6. Facial growth (onset and peak): Concordance between actual ages and ages estimated from contemporary indices

Statistic

Index

Onset(O) Peak(P)

RMSE RMSE r

Males

Mean (O:12; P:14)* 1.16 1.41 . . Hand-wrist (Stage 7) . . 0.85 0.73 Vertebrae (Stage 3.5) . . 1.46 0.44

Females

Mean (O:10; P:12)* 1.21 1.15 . . Hand-wrist (Stage 6) . . 1.20 0.59 Vertebrae (Stage 3.5) . . 1.51 0.41

*Means constant; no correlation possible

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Table 2.7. Error Variances: Index peak age relative to actual peak age

Ranked error variances Growth Test Measure 1 2 3

Males

0.94(HW) 1.27(Mean) 1.70(CV) Stature Fmax

Cochran C

0.72(HW) 1.99(Mean) 2.12(CV)

Face Fmax *

Cochran C

0.65(HW) 1.83(CV) 1.93(Mean)

Mandible Fmax *

Cochran C

Females

1.30(Mean) 1.48(HW) 2.79(CV) Stature Fmax

Cochran C *

1.33(Mean) 1.44(HW) 2.28(CV)

Face Fmax

Cochran C

1.50(Mean) 1.79(HW) 2.68(CV)

Mandible Fmax

Cochran C

*Error variances not sharing underline are significantly different

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Table 2.8. Peak growth: Prediction error

Prediction Method Measure RMSE r

Males

Height onset + 2 Face 1.10 0.54

Mandible 1.17 0.45

Vertebrae CS2 + 1 Face 1.96 0.34

Mandible 1.97 0.32

Vertebrae CS2 + 1.5 Face 1.75 0.34

Mandible 1.76 0.32

Mean 12 + 2* Face 1.41 . .

Mandible 1.39 . .

Females

Height onset + 2 Face 0.58 0.89

Mandible 0.82 0.77

Vertebrae CS2 + 1 Face 1.70 0.18

Mandible 1.91 0.00

Vertebrae CS2 + 1.5 Face 1.71 0.18

Mandible 1.92 0.00

Mean 10 + 2* Face 1.15 . .

Mandible 1.23 . .

*Means constant; no correlation possible

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*

*

*

*

*

*

*

Table 2.9. Peak timing: Among-index differences in prediction error

Ranked error variances** Growth Test

Measure 1 2 3 4

Males

0.83(Ht) 1.27(Mean) 2.49(CV2) 2.90(CV) Stature Fmax

* Cochran C *

1.20(Ht) 1.99(Mean) 3.06(CV2) 3.84(CV) Face Fmax

*

Cochran C *

1.36(Ht) 1.93(Mean) 3.10(CV2) 3.89(CV) Mandible Fmax

* Cochran C *

Females

0.67(Ht) 1.30(Mean) 2.32(CV) 2.96(CV2)

Stature Fmax *

Cochran C *

0.34(Ht) 1.33(Mean) 2.89(CV) 2.91(CV2) Face Fmax

* Cochran C *

0.67(Ht) 1.50(Mean) 3.65(CV) 3.70(CV2) Mandible Fmax

* Cochran C * *Error variances not sharing underline are significantly different **CV = CS2+1; CV2 = CS2+1.5

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The intra-class correlation for cephalometric meas-

urements of the 8 subjects (57 radiographs) showed good re-

liability: Cronbach’s alpha for the sum of the five facial

dimensions was 0.98, and Cronbach’s alpha for the mandibu-

lar measurement, Co-Gn, was also 0.98. Cronbach’s alpha

for inter-rater reliability was 0.97; for intra-rater reli-

ability it approached 1.00 in both workers (Z.M. and L.J.)

Discussion

Pattern of Growth

For many years, indices of maturation have been

used to assess an individual’s developmental status, and

investigators have attempted to use these indicators to

predict events such as the onset and peak of the pubertal

growth spurt. The use of longitudinal data to plot incre-

mental growth curves began in 1927 when Scammon plotted

semi-annual height data that Montbeillard had collected

from his son’s birth in 1759 to his eighteenth birthday

(Figure 2.10).38

Since that time, many workers have drawn incre-

mental growth curves of statural and or facial growth in

males and females.6-10,15,16,21 The average curves generated in

the present study display the same general form as the

aforementioned studies. Indeed, the average male curves

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Figure 2.10. Growth in height of the son of the Count Montbeillard during the years 1759-1777 as plotted by Scammon.38

developed here are almost identical to the initial curve

generated by Scammon38 in 1927 from a sample of 1. A rela-

tively constant rate of growth is seen in late childhood,

followed by an intense growth spurt during adolescence.

Following the peak of the spurt, growth decreases to a

minimal rate in late adolescence.

Although the curves for both sexes show general

similarities, they also show a degree of sexual dimorphism.

For example, greater growth intensity was seen in males, a

finding that agrees with the observations of Nanda15,

Grave8, and Tanner and associates10. Also, Gasser and co-

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workers39,40 have reported a pre-pubertal, or “mid-growth”

spurt prior to the pubertal growth spurt; this mid-growth

spurt generally occurs closer to the pubertal spurt in fe-

males. In the present study, a mid-growth spurt was appar-

ent in the average facial and mandibular growth curves for

females, but not so for males. Gasser’s group40 found that

the mid-growth spurt occurs at approximately 7.5 years in

both sexes, an age that was not consistently included in

the present study’s male sample.

Although many similarities were found between the

present study’s average curves and other growth curves in

the literature, a few difference were also observed. Hägg

and Taranger found that the average age at the onset and

peak of pubertal growth in stature was 12.08 and 14.07

years in males and 10.04 and 11.98 years in females.11

Bowden9 and Tanner’s group10 reported similar estimates.

The present investigation also shows that females have an

onset around 10 and a peak 12 years. In the present study,

however, the males showed onset and peak somewhat later, at

ages of 12.43 and 14.49 years, respectively.

The minor differences between the mean ages of this

study and those reported in the literature may be due to

secular variation among samples. The samples were drawn

from different parts of the world and at different times:

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the Bolton-Brush Growth Study began in 1927, approximately

20 years prior to the samples used by Bowden9, Tanner’s

group10, and Hägg and Taranger.11,21

There is disagreement in the literature with regard

to the relationship between the timing of the spurt in

stature and the face. Nanda15 and Bambha6 reported that the

face achieves its circumpubertal maximum later than stat-

ure, whereas Hunter16, Grave8, and Bergersen13 found that the

peaks in stature and in the face to occur synchronously.

Bambha also noted that stature and the face display a simi-

lar duration of growth during the pubertal spurt. Based on

a considerably larger sample, the present investigation ar-

gues that, in males, onset occurs at the same time in stat-

ure, in the face, and in the mandible. In females, onset

in stature and the mandible begin together, but before on-

set of peak growth in the face. In both males and females,

the peak in stature occurs before that of the face and man-

dible. Also, the present study indicates that the mandible

grows synchronously with the rest of the face and does not

peak later or grow longer. Thus, stature and facial growth

are closely related at the onset of the pubertal growth

spurt; however, the spurt in stature shows a shorter dura-

tion and attains its peak before the face.

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Indices of Maturation

Because events in the hand, wrist, and cervical

vertebrae correlate with the peak in the adolescent growth

spurt, many workers have argued that developmental events

in the skeleton can be used to assess maturation.8,9,17-21,24-28

The individual growth curves in the present study allow a

comparison of the actual peak ages against peak ages esti-

mated from the various indices. In males, the correlations

(Tables 2.5-2.7) demonstrate that the hand-wrist ages dis-

play a moderately strong relationship to the timing of the

peak in stature, the face, and the mandible. Females, how-

ever, showed only moderate correlations between the hand-

wrist ages and the three measures of size.

At least as judged by Fmax, the hand-wrist assess-

ment had a significantly lower error variance than either

mean chronological age or vertebral assessments for facial

size and mandibular length in males, whereas females did

not show significant differences (Table 2.8). The results

of the present study suggest that hand-wrist staging might

offer some value in assessing maturation in males, but lit-

tle value in females, a conclusion reached earlier in a re-

view by Smith.41

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In general, the cervical vertebral stages showed

only weak to moderate relationships to the timing of peak

growth and, in general, had a higher error standard devia-

tion than both the hand-wrist stages and mean chronological

age. The results of the present investigation suggest that

the use of the vertebrae to assess the attainment of the

peak in pubertal growth is no improvement over the hand-

wrist or even chronological age.

Many workers have argued that a “skeletal age”

would provide a better estimate of maturation than chrono-

logical age because of the considerable age-variation among

individuals at onset and peak of the pubertal growth

spurt.11-14 Although these indices of maturation show some

correlation to the present state of development and can es-

timate roughly if the peak has occurred or is occurring,

the data from the present investigation indicate that these

skeletal events do not estimate the peak of pubertal growth

more accurately than does chronological age.

Prediction

Indices of maturation may provide a rough assess-

ment of an individual’s current state of development; how-

ever, a predictor of peak growth would be of greater

utility to the orthodontist. The literature shows that

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104

peak normally follows onset by about 2 years6-11; therefore,

statural onset plus 2 years was used here to predict the

peak of the pubertal growth spurt. The present findings

indicate that, at least for females, a pubertal spurt dura-

tion of roughly 2 years is very accurate. Furthermore,

the results of the present study hold that the onset of the

spurt in stature is the best predictor of the peak in pu-

bertal growth.

The prediction of statural onset plus 2 years shows

the smallest error variance in males and females among the

various indices, and in females, a very strong correlation

exists between this prediction and the peak of facial

growth. Although the statural onset also demonstrates the

lowest error variance among the various indices in males,

only a moderate correlation exists with maximum facial

growth. In the present investigation, males displayed a

duration of approximately 2.5 years between the onset and

peak. This finding suggests that a prediction based on

statural onset plus 2.5 years may provide a better predic-

tion of the timing of the facial growth peak in males.

This conjecture is a matter for future investigation in an-

other sample.

The application of contemporary measures of skele-

tal age to facial-growth prediction appears to be of

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105

limited value, given that the results of the present study

show that indices of maturation and chronological age show

similar error variation, both in assessing the present

state of maturation and predicting the timing of peak

growth. Great among-stage variability was seen in the

hand-wrist and cervical vertebral methods, both at the on-

set and peak. This variation may be due to differences in

the rate of development among individuals or because of in-

herent error in the evaluation of a single annual radio-

graph. McNamara and associates have reported that the

vertebral stages occur approximately one year apart,42 a

claim that could not be verified here. Many subjects pro-

gressed through multiple hand-wrist and vertebral stages in

a single year, whereas others took multiple years to ad-

vance a single stage. Fishman also observed this phenome-

non, noting that each individual possesses a time schedule

of development that varies both in acceleration and decel-

eration.21

In the end, the cervical vertebral method displays

the greatest error standard deviation, both in the assess-

ment of maturation and in the prediction of the peak. This

error may be due to the limited number of stages in the

method (the descriptive characteristics of one stage fre-

quently overlap those of adjacent stages) and the

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106

subjectivity of vertebral staging. Indeed, the method of

San Román and colleagues is the only one in which there is

an attempt to quantify a “concavity” at the lower border of

the vertebrae.26 Although it seems to be a step in the

right direction, it apparently did little to improve the

accuracy of forecasts generated here. In the end, the er-

ror of this method may be due merely to an intrinsic lack

of predictive power.

Although the literature states that the cervical

vertebral stages correlate well with those of the hand-

wrist film and thus can ably assess individual matura-

tion,22-24,26,28,29,32 the results of the present study imply

that the cervical vertebral method is the least precise way

of assessing maturation at peak and of predicting the tim-

ing of the actual facial-growth spurt. Thus, in agreement

with Bernard30, cervical vertebral staging may be a rela-

tively ineffective clinical tool.

Another source of error variation in the hand-wrist

and vertebral indices is their reliance on annual or bien-

nial radiographs to assess an individual’s development.

When an event is first seen on a radiograph, it is assumed

to have occurred at the mid-point of the previous interval,

an assumption that generates a built-in error standard de-

viation of about 4 months. Indeed, this error is not only

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107

unavoidable, but also likely to get worse: radiographs

probably never again can be taken regularly for the purpose

of assessing maturation, especially if the method is known

to be relatively crude and unreliable.

In contrast, a patient’s height can be measured as

frequently as desired without adverse effects because stat-

ure can be measured at individually tailored intervals

(monthly, weekly, daily as needed to define onset). The

inherent error seen here--already the lowest of the methods

studied--perhaps can be decreased to yield an even better

definition of the onset of the facial growth spurt, an

event that can serve as a rational basis for planning the

timing of treatment.

Envoi

In the assessment of maturation, the prediction of

growth timing, one must consider what can be learned from a

single visit and what can be inferred from the serial data

that are likely to be available to the 21st Century clini-

cian. At a single appointment, mean ages are both effec-

tive and as effective as they will ever be. Moreover, with

luck, a single radiograph might happen to capture a sig-

nificant event. Given an opportunity to observe and re-

flect, however, the present study argues that serial height

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108

data might be of considerable significance not just in de-

ciding whether to treat “early” of “late,” but rather in

deciding which time is the right time.

Conclusions

The present investigation is, to date, the most ex-

tensive study of the pattern of facial growth and its rela-

tion to various common maturity indicators. The

longitudinal nature of this study and its generation of in-

dividual growth curves allowed the identification of onset

and peak of the pubertal growth spurt in height, facial

size, and mandibular length in a large sample of growing

children. Based on the present data, it is concluded that

contemporary measures of skeletal age offer no improvement

on chronological age, either in assessing or predicting the

timing of the pubertal growth. Instead, the best predictor

of the pubertal growth spurt was statural onset, an event

generated by a method that is not constrained by the fre-

quency with which it can be measured.

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3. Johnston LE, Jr. A comparative analysis of Class II treatments. In: McNamara JA, Jr., Carlson D, Vig P, Ribbens K, editors. Science and Clinical Judgement in Orthodontics, Monograph No. 18, Craniofacial Growth Series, Center for Human Growth and Development, The University of Michigan. Ann Arbor, 1986.

4. Bishara SE, Jakobsen JR, Vorhies B, Bayati P. Changes in dentofacial structures in untreated Class II division 1 and normal subjects: a longitudinal study. Angle Orthod 1997;67:55-66.

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11. Hägg U, Taranger J. Skeletal stages of the hand and wrist as indicators of the pubertal growth spurt. Acta Odontol Scand 1980;38:187-200.

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24. García-Fernandez P, Torre H, Flores L, Rea J. The cervical vertebrae as maturational indicators. J Clin Orthod 1998;32:221-225.

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33. Baccetti T, Franchi L, McNamara JA, Jr. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod 2002;72:316-323.

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36. Fishman LS. Radiographic evaluation of skeletal maturation. A clinically oriented method based on hand-wrist films. Angle Orthod 1982;52:88-112.

37. Haahr, M. True random number service 1998. [www.random.org]. Accessed August 19, 2006.

38. Scammon R. The first seriatim study of human growth. Am J Phys Anthropol 1927;10:329-336.

39. Gasser T, Kohler W, Muller HG, Kneip A, Largo R, Molinari L, Prader A. Velocity and acceleration of height growth using kernel estimation. Ann Hum Biol 1984;11:397-411.

40. Gasser T, Muller HG, Kohler W, Prader A, Largo R, Molinari L. An analysis of the mid-growth and adolescent spurts of height based on acceleration. Ann Hum Biol 1985;12:129-148.

41. Smith RJ. Misuse of hand-wrist radiographs. Am J Orthod 1980;77:75-78.

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APPENDIX A

Growth Curves—Male Subjects

Appendix A contains the growth curves of the face,

height, and mandible for the 50 male subjects. In addi-

tion, a summary of the actual chronological ages, matura-

tion stages, and estimated ages at onset and peak is dis-

played for each subject. Note that on the “Facial Growth

Curve” the x-axis values are not chronological age inter-

vals; the corresponding x-axis values and chronological age

intervals are listed below. See CD for Appendix A.

Chronological Age x-axis

6-7 0

7-8 1

8-9 2

9-10 3

10-11 4

11-12 5

12-13 6

13-14 7

14-15 8

15-16 9

16-17 10

17-18 11

18-19 12

19-20 13

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114

APPENDIX B

Growth Curves—Female Subjects

Appendix A contains the growth curves of the face,

height, and mandible for the 50 female subjects. In addi-

tion, a summary of the actual chronological ages, matura-

tion stages, and estimated ages at the onset and peak is

displayed for each subject. Note that on the “Facial

Growth Curve” the x-axis values are not chronological age

intervals; the corresponding x-axis values and chronologi-

cal age intervals are listed in Appendix A. See CD for

Appendix B.

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VITA AUCTORIS

Zachary Joseph Mellion was born on December 23,

1979 in St. Louis, Missouri. He received both his

undergraduate and dental education at Case Western Reserve

University in Cleveland, Ohio. In 2004, he received a

D.M.D. degree from The Case School of Dental Medicine.

Upon graduation from dental school, he began his graduate

studies in orthodontics at the Center for Advanced Dental

Education at Saint Louis University, in St. Louis,

Missouri. He currently is a candidate for the degree of

Master of Science in Dentistry. He married Dr. Keira

Mellion on June 17, 2005.


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