The use of the Greulich-Pyle method in a longitudinal growth study

The Greulich-Pyle method of assessing skeletal maturity is essentially suited to cross-sectional analyses, though it may be used retrospectively in longitudinal studies, through the technique of regression analysis. When applied to the serial records of 120 Philadelphia children, considerable variability in maturation rate may be observed. This variability is both within and between-individuals. While most seems to be random, there is the strong suggestion that individuals who are, during infancy and early childhood, slow maturers, speed up to greater-than-average rates during middle childhood and adolescence; the opposite may be inferred in those who are initially rapid maturers. Though these findings were consistent in the Philadelphia sample, they may be artifacts of the Greulich-Pyle standards.     

Differences between early- and late-maturing genotypes of the platyfish (Xiphophorus maculatus) in the morphometry of their immunoreactive luteinizing hormone releasing hormone-containing cells: a developmental study

Immunoreactive luteinizing hormone releasing hormone (ir-LHRH) containing perikarya, brain nuclei, and pituitary cells were studied during the postnatal development of male sibling platyfish (Xiphophorus maculatus) genetically determined to reach puberty at two different ages using immunocytochemical, cytological, and morphometric methods. Ir-LHRH-containing perikarya first appear in the nucleus olfactoretinalis (NOR) at 5 weeks of age in early maturers and at 11 weeks in late maturers at a maximum number which is similar in both genotypes and remains constant into adulthood. The dimensions of the NOR and its perikarya increase up to the initiation of sexual maturation (gonopodial stage 2) in both genotypes. In the nucleus preopticus periventricularis (NPP), ir-perikarya appear at stage 2 and are maximum in number at maturity (stage 6) when early maturers have 50% more than late maturers. Measurements for the NPP increase between 1 week and stage 6 in both genotypes. In the nucleus lateralis tuberis (NLT), ir-perikarya appear soon after stage 2 in early maturers but are never seen in late maturers. Late maturers also have fewer ir-LHRH containing pituitary cells than early maturers. In both genotypes, measurements for the NLT increase to stage 2 and then decrease to stage 6. During sexual development there are differences between early- and late-maturing genotypes in the morphometry of their LHRH-containing brain centers. The timing of sexual development creates significant differences in the cytological and cytometric characteristics of the three ir-LHRH-containing brain nuclei in fish of the same age but different genotype. Our results also show that for both genotypes there is a positive correlation between the total number of ir-LHRH brain neurons and the total number of ir-pituitary cells and both are lower for late maturers at every age and stage.     

Secular trend in skeletal maturation in southern Chinese girls in Hong Kong

Southern Chinese girls aged 11 years 9 months to 12 years 3 months in Hong Kong have a mean skeletal age of 12.57 years assessed from the left hand and wrist radiographs by the Greulich and Pyle Atlas Method. Significant secular trend of earlier skeletal maturation was demonstrated with p less than or equal to 0.001. Such difference was contributed by improved socio-economic, nutritional and socio-hygienic conditions during the past decades.     

Postnatal growth and skeletal maturation of experimental preterm macaques (Macaca nemestrina)

The growth and skeletal maturation of nine preterm female pigtailed macaques (Macaca nemestrina) obtained by C-section at less than or equal to 155 postconceptional days were followed through six months of age. At C-section they were of normal size and maturation for gestational age. Compared with 50 normal females born at term (mean = 173 +/- 6.4 postconceptional days), preterm infants were also of normal size at term, but delayed in skeletal maturation, requiring about one month to achieve the standard.     

Environmental effects on skeletal versus dental development II: further testing of a basic assumption in human osteological research

This study further tests the general assumption that skeletal development is more sensitive to socioeconomic factors than dental development in a sample of modern immature Portuguese skeletons (N = 41) of known sex, age, and socioeconomic background. Skeletal development was assessed from skeletal maturation of the knee and dental development was assessed from schedules of tooth formation. Discrepancies between physiological age (skeletal and dental age) and chronological age were used as a measure of developmental status. A positive score indicates that physiological age is in advance of chronological age, whereas a negative score indicates the reverse. Two socioeconomic groups, one of low and the other of high socioeconomic status, were created based on the occupation of the father and on the place of residence, and developmental status was compared between the two socioeconomic groups. Results confirm previous studies by showing that dental development is less affected by environmental insults than skeletal maturation. While socioeconomic differences in skeletal maturation range from 1.20 to 1.22 years (15-18% of chronological age), socioeconomic differences in dental maturation range from 0.51 to 0.53 years (4-9% of chronological age). Compared to a previous study, results also suggest that skeletal maturation is more affected than skeletal growth. Additionally, an adaptation of the radiographic atlas of skeletal development of the knee is proposed for use with dry skeletal material.     

Association between maternal age at menarche and newborn size

The impact of maternal age at menarche on newborn size was tested using data from 4,996 single births taking place at Vienna, Austria, between 1985 and 1995--so-called teenager pregnancies were excluded from the present analyses. All women experienced pregnancies between the ages of 19 to 42 years. Maturational time was related significantly to infant weight and length independent of maternal age and behavioral variables such as smoking. Early maturation, i.e., age at menarche before the 12th birthday, was significantly associated with decreased newborn weight and size. The incidence of low-weight newborns was significantly higher in early-maturing mothers. The more favorable nutritional status of women whose menarche occurred relatively early was not able to compensate for the negative effects of early maturation on intrauterine growth. Higher circulating estrogen levels in early maturers preserved into adulthood are discussed as possible reasons for intrauterine growth retardation of the offspring of early-maturing mothers.     

Childhood retardation resulting in reduction of adult body size due to lesser adolescent skeletal delay

The skeletal maturation of 7972 rural children from the six Central American nations, aged one month through 22 years, is evaluated. The results suggest that retardation in skeletal maturation during childhood is significantly greater than during adolescence, while growth in body size shows a progressive delay from infancy through adolescence. In other words, the apparent improvement in skeletal maturation during adolescence is not associated with an equivalent “catch-up” in body size. Similarly, prolongation of the period of growth does not fully compensate for the slow rate of growth. It is postulated that the small stature in Central America is related to the marked childhood retardation and to the fact that during adolescence, the timing of skeletal maturation is less affected than growth in size.     

Neonatal skeletal maturation in congenital hypothyroidism and its prognostic value for psychomotor development at 3 years in patients treated early

Neonatal skeletal maturation was assessed by different methods based on the bone centres in the knee and ankle region in 46 infants with true-positive (patients) and 17 infants with false-positive screening tests (controls). The patients and controls did not differ in mean age at X-ray examination and age at the start of treatment (14.5 +/- 5.7 days). One of the methods used to score the size of femoral and tibial epiphyses was just as good as the other ones tested, but has the advantage of being the easiest to use and therefore clinically most suitable. Skeletal maturity assessed by this method correlated best with serum T4 (r = 0.62, p less than 0.01). Griffiths tests were performed in 37 of the 46 patients at 28-48 months of life. The best correlation obtained between neonatal skeletal maturity and Griffiths global developmental quotient at 3 years of age was r = 0.58 (p less than 0.001). Although statistically significant, it was too weak to be of clinical value in identifying individual patients at risk. We conclude that an assessment of skeletal maturation is not useful for the prognosis of psychomotor development in individual patients with congenital hypothyroidism receiving treatment within the first 2 weeks of life.     

On the skeletal maturation of Japanese-American White hybrids.

The skeletal maturation of Japanese-American White hybrids is discussed in relation to that of Japanese and Whites. Assessment of skeletal maturation was made on 323 radiographs of 57 boys and 151 of 33 girls studied semi-longitudinally from 3 to 18 years on the basis of the Tanner-Whitehouse method (62). The skeletal maturity scores show a tendency for a greater advance in childhood for the Whites than for the hybrids and the Japanese. However, the preadolescent spurt of skeletal maturity occurs earlier in the Japanese and the hybrids than in the Whites, and the hybrids show the intermediate skeletal maturity scores between those of the Japanese and the Whites at and after adolescence.     

Skeletal growth in school children: maturation and bone mass

Skeletal growth and development was evaluated in 322 white children (age 6 to 14) using three different methods: (1) ¹²⁵I photon absorptiometry, (2) compact bone measures on radiographs, and (3) Greulich-Pyle skeletal age from hand-wrist radiographs. Bone mineral content, measured by photon absorptiometry, increased at an incremental rate of about 8.5% each year. Skeletal age was a poor predictor of skeletal status, i.e., bone mineral content (14% error), and did not decrease the predictive error substantially more than did chronological age. Gross morphology (height and weight) was in fact a better predictor of bone mineral content than were skeletal age, chronological age, and radiographic morphometry. Skeletal age deviations were correlated with deviations in body size. A bone mineral index was devised which was independent of body size and this index was also independent of skeletal age. Skeletal age is imprecise (3 to 6 months error) and the range of variation in normal children (13 months) overlaps the maturational delay of the malnourished and diseased. The difficulties in using skeletal maturation are discussed and it is suggested that particular maturational indices be used which better indicate skeletal growth than does a composite skeletal age.     

Problems in the aging of skeletal juveniles: Perspectives from maturation assessments of living children

We employ samples of children of known chronological age to demonstrate the significance of random and systematic effects on maturation in both dental and skeletal development. Differences between chronological age for dental age in young healthy Canadian children can be as much as 100% of the actual age of the children. For skeletal development by reference to Greulich-Pyle standards, three samples of known-age children from Mexico document parallel effects: 1) 183 six-year-old children have skeletal-based ages with a 95% confidence interval of 4–8 years; 2) 80% of 217 4.0–4.5-year-old children are underaged by 1–3 years; and 3) 130 children of skeletal age between 39 and 44 months are actually between 4 and 7.4 chronological years of age. The Mexican samples are drawn from a population living under conditions of environmental stress with chronic mild to moderate protein-energy malnutrition and moderate to high levels of infectious disease. These children may parallel those from the past, whose remains are studied by skeletal biologists or paleoanthropologists. Our findings reinforce concerns expressed in extant studies regarding the accuracy of age-at-death reconstructions. © 1996 Wiley-Liss, Inc.     

Age- and training-related changes in the collagen metabolism of rat skeletal muscle

The effects of ageing and life-long endurance training on the collagen metabolism of skeletal muscle were evaluated in a longitudinal study. Wistar rats performed treadmill running 5 days a week for 2 years. The activities of collagen biosynthesis enzymes, prolyl-4-hydroxylase and galactosylhydroxylysyl glucosyltransferase, were highest in the muscles of the youngest animals, decreased up to the age of 2 months and from then on remained virtually unchanged. The enzyme activity in young animals was higher in the slow collagenous soleus muscle than in the rectus femoris muscle. The enzyme activity in the soleus muscle was higher for older trained rats than older untrained rats. The relative proportion of type I collagen increased and that of type III collagen decreased with age, suggesting a more marked contribution by type I collagen to the age-related accumulation of total muscular collagen. The results show that collagen biosynthesis decreases with maturation and that life-long endurance training maintains a higher level of biosynthesis in slow muscles.     

Body height,weight, and skeletal maturation in Hottentot (Khoikhoi) children

Growth of body height and weight and skeletal maturation are discussed, based on 49 male and 61 female Hottentot children aged 3 to 17 years from Warmbad, Namibia (South West Africa) and 124 boys and 113 girls aged 1 to 21 years of related populations, the Rehoboth Basters of Namibia and Cape Coloreds from Cape Town, South Africa. The related populations are taller and heavier than the Hottentots, and have almost the same body height as American blacks and whites at least after the age of 18 years. In the Hottentots and Rehoboth Basters, the mean TW2 skeletal age is always less than the British standard by one or two years in both sexes. In general, the Rehoboth Basters have a skeletal age that is intermediate between Hottentot and British children. In both Hottentots and Rehoboth Basters, the increase in body height shows a linear relation to the skeletal age, and the regression curves are almost parallel in both sexes. The differences in body height and weight between the Hottentots and Rehoboth Basters become greater after the skeletal ages of 15 years for boys and 13 years for girls.     

Skeletal maturation of the human fetus assessed radiographically on the basis of ossification sequences in the hand and foot

In studies of postnatal human development the skeletal maturation of the hand has been found to be a better indicator of general physical maturation than attained body height. For assessment of prenatal human development the Crown-rump length (CRL) has so far been the most commonly used measure. The object of the present study is to examine the possibility of also using the skeletal maturation of the hand as a maturity indicator in fetal development. The study is based upon a radiographic and histochemical investigation of 169 human fetuses. On the basis of counting silver-impregnated diaphyses on radiographs of the hand and foot a maturity indicator (CNO = Composite Number of Ossified bones in hand and foot) was established. Owing to the marked regularity of the recorded ossification pattern, the CNO parameter can be used for evaluating fetal maturation during the early half of the prenatal period. To supplement the assessment of skeletal maturation during the later stages of development, a classification based on the shape of some bones was included in the study. In many cases fetuses of the same size (CRL) exhibited different stages of skeletal maturation (CNO). In accordance with findings from assessment of postnatal development, a more accurate evaluation of fetal development is obtained by combining the size parameter CRL with an assessment of fetal skeletal maturation, CNO.     

Associations between the rates of maturation of the bones of the hand-wrist

Skeletal maturation rates for the age interval 3 to 13 years were analyzed using bone-specific assessments (Greulich-Pyle) of serial radiographs of 40 children. The mean rates of skeletal maturation resembled those of the population from which the atlas standards had been derived. There was a linear trend of skeletal age against chronological age for most bones in each sex. Regression lines were fitted to these data and the b values of the regression lines were calculated. Communality indices were calculated from an intercorrelation matrix of these b values. There was a statistically significant rank order correlation between the sexes in the communality indices. They tended to be higher in the girls than in the boys and were relatively low for the radius, ulna and carpals. Communality indices within groups of bones were high in all rows, especially the metacarpals, but in each sex they were comparatively low in the first ray (metacarpal plus the phalanges of the corresponding digit) and in the fifth ray of the boys. Neighborhood effects on the levels of association of maturation rates were present, particularly in the carpus, but marginal effects were not noted.     

Predicting the timing of maturational spurts in skeletal age

Measures of maturity provide windows into the timing and tempo of childhood growth and maturation. Delayed maturation in a single child, or systemically in a population, can result from either genetic or environmental factors. In terms of the skeleton, delayed maturation may result in short stature or indicate another underlying issue. Thus, prediction of the timing of a maturational spurt is often desirable in order to determine the likelihood that a child will catch up to their chronological age peers. Serial data from the Fels Longitudinal Study were used to predict future skeletal age conditional on current skeletal age and to predict the timing of maturational spurts. For children who were delayed relative to their chronological age peers, the likelihood of catch‐up maturation increased through the average age of onset of puberty and decreased prior to the average age of peak height velocity. For boys, the probability of an imminent maturational spurt was higher for those who were less mature. For girls aged 11 to 13 years, however, this probability was higher for those who were more mature, potentially indicating the presence of a skeletal maturation plateau between multiple spurts. The prediction model, available on the web, is most relevant to children of European ancestry living in the Midwestern US. Our model may also provide insight into the tempo of maturation for children in other populations, but must be applied with caution if those populations are known to have high burdens of environmental stressors not typical of the Midwestern US. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Of Lichens,Caribou and Tuna

Delayed skeletal maturation has been long accepted as a correlate of mental retardation. Three hundred mentally retarded children were examined for skeletal age and failed to show any overall delay of bone age as compared to chronological age. Further, birth weight was found to be unrelated to bone age maturity. Children with severe levels of retardation displayed significant delay in bone development only when profound physical disability was also present. In eight diagnostic categories of mental retardation, only those with metabolic syndromes showed any significant delay in skeletal system maturation. Conversely, mongoloid children showed a larger-than-chance percentage of advanced bone maturation. Skeletal measures therefore are perhaps more reflective of etiological states than of diagnostic classifications in mental retardation.     

Bone maturation reflects the secular trend in growth

The aim of this study was to compare a series of X-rays from the mid-1990s with another taken in the mid-1980s in order to test the possibility that environmental causes affect the skeletal maturation. The first group of subjects included a total of 1,057 girls and 1, 055 boys participating in a project for Japan and China health research in 1986. The second group of subjects included a total of 382 girls and 629 boys participating in a project for bone mineral density research in 1996. The skeletal maturity score using the Tanner-Whitehouse 2-RUS method was used as the fundamental datum. This score was used to represent each group. The Wilcoxon's rank sum test was applied to examine the significance of the difference between the 1986 and the 1996 groups. The 1996 children had not matured more than the 1986 children; children in both groups reached the given scores at almost the same ages. In girls, there was little difference between the groups at 7 years of age, but it declined from 8 years of age onward. Some apparent differences arose at ages 14 and 15, but ceased by age 16 in girls. In boys, no differences were found in those aged from 7 to 17 years, except for 12-year-olds. We did not detect much of a difference in bone maturation between the 1986 and 1996 groups of children, and no differences in height during the same period. Our findings suggest that bone maturation reflects the secular trend in growth.     

A longitudinal study on hand and wrist skeletal maturation in chimpanzees ( Pan troglodytes), with emphasis on growth in linear dimensions

Skeletal maturation in the chimpanzee hand and wrist (the RUS system; radius, ulna, and short bones) was studied both longitudinally and cross-sectionally. Maturity states were evaluated in each of the 13 bones of the RUS system based on the TW2 method (Tanner and Whitehouse method), and the RUS score was calculated by the summation of scores for these bones. Individual variation was examined by means of residual curves and pseudo-velocity curves of RUS score and anterior trunk length (ATL). Norms of the age change pattern in RUS skeletal maturation and the growth of ATL were determined for each sex, and the relationships among ATL growth and skeletal and reproductive maturation were examined. We found a fairly good relationship between ATL growth and RUS skeletal maturation. Comparison of growth and development between humans and chimpanzees showed that growth characteristics are coupled with each other at puberty in male chimpanzees and in both sexes of humans. Although nutritional condition influenced ATL growth in infancy, it had no effect on the RUS maturational process. Social relationships appeared to influence both ATL growth and RUS maturation. Analyses on relationships between RUS skeletal maturation, ATL growth, and reproductive maturation, showed that RUS skeletal maturation is a good indicator of "physiological age".