Ossification communalities of the hand and other body parts: their implication to skeletal assessment

Correlating the age at appearance of 71 postnatal ossification centers (OC's) with every other OC, 4,970 correlations in all, then grouping correlations by body part, the hand does not exhibit usefully higher communality (mean r) than the foot, shoulder, hip, elbow or knee. While low communality round bones and ossification sequence polymorphisms together account for the fact that no one body part adequately represents the entire skeleton, it is also true that ossification communality throughout the skeleton is low unless OC's of maximum predictive value are separately employed.     

Developmental communalities of homologous and non-homologous body joints

Reducing 4970 center- and sex-specific correlations for age at appearance of postnatal ossification centers to 15 mean values of r representing homologous and non-hmologous inter-limb and intra-limb joint segment communalities, it was shown that homologous joint segments in different limbs (hand-foot, elbow-knee, shoulder-hip) showed systematically higher developmental communality than intra-limb non-homologous joints, and these in turn exceeded mean r values for inter-limb non-homologous joint segments.     

Secondary centers of ossification of the human toes: exceptional polymorphism and evolutionary perspectives

As great morphological variability characterizes the phalanges of the human toes in adults, we hypothesized for a possible variability in the presence or absence of their secondary (= epiphyseal) centers of ossification linked to the unique morphology of the human foot within primates. The aim of this study was thus to provide original and detailed data on the occurrence of these centers. Classically, the big toe or hallux (I) presents two secondary centers and the lateral toes (II-V) three centers, and consequently the five toes present a total of 14 secondary centers. The material studied consisted of 261 foot radiographs from 261 young individuals of European origin (202 males and 59 females; 6-16 years). The presence (or absence) of the secondary centers of the phalanges of the toes was assessed for each foot. Feet presenting a biphalangeal variant in one or more lateral toes were studied separately. The theoretical possibilities of association of the three secondary centers in a given lateral toe (II-V) are eight in number; these eight patterns were studied and coded in the present study by types A-H. An exceptional variability in the occurrence of the secondary centers in lateral toes (II-V) was observed, and the classic pattern of phalangeal ossification was never observed. The absence of one or more secondary centers seems to be observed only in the human species, and we suggest that this could be a derived pattern specific to the human species, i.e., autapomorphic pattern. These results are of interest in the characterization and understanding of the reduction in size of the lateral toes which characterizes the specific evolution of the human foot.     

Ossification in the hand and foot of the macaque (Macaca nemistrina). I. General features.

The appearance of the secondary centers of ossification was investigated in hand and foot radiographs of 112 fetal and neonatal Macaca nemestrina and a maturational index calculated using a scoring system that differentiated between the initial and later stages of ossification. Cumulative incremental curves of skeletal maturation, constructed by plotting the maturational indices against gestational age, demonstrated three distinct periods of ossification: the First Acceleration when primary centers appear, the Plateau, and the Second Acceleration when the secondary centers ossify. Similar curves are constructed for human prenatal and postnatal ossification. The results are also compared with those reported for M. mulatta, and the bases of the observed differences are discussed. Compared with other primates, the fetal and neonatal macaque shows a developmental precocity which may be an ontogenetic adaptation to the socioecological setting of terrestrial life.     

Sequence of ossification of the foot in marmosets (Saguinus oedipus)

The cleared and alizarin-stained feet of eight marmoset (Saguinus oedipus) fetuses revealed a sequence of initial ossification of the 19 bones of the foot that is almost totally different from that of man. The most striking difference is in the order of ossification of the distal phalanx of the big toe; in man it is the first bone to commence ossification, in the marmoset it is the fourteenth. It is suggested that the sequence of initial ossification in the foot may be species specific among the primates and may serve as a useful marker of teratogenic action.     

Ossification sequence polymorphism and sexual dimorphism in skeletal development

Ossification sequence polymorphism and sexual dimorphism are prevalent in the postnatal skeletal development of the hand, foot, elbow, knee, shoulder and pelvis. For some ossification polymorphisms the sex-discriminatory efficiency is greater than 70%. Current evidence, including population comparisons, and children with kwashiorkor and marasmus, favors a genetical explanation for common sequence polymorphisms. However, ossification sequence polymorphism is more clearly defined in later-developing children, where the appearance of ossification centers is distributed among a larger number of radiographic class intervals. This observation may explain the apparent relationship between ossification sequence polymophism and developmental delay or retardation.     

Appearance of ossification centers of the lower arm,wrist, lower leg,and ankle in immature orangutans and chimpanzees with an assessment of the relationship of ossification to dental development

This study examines the appearance of the secondary ossification centers in the lower arms, wrists, lower legs, and ankles of a cross-sectional sample of 20 infant orangutans and chimpanzees (15 of known age). The number of tarsal and carpal centers is analyzed relative to the degree of M₁ development and the weight of individual animals. Variation in the appearance of these ossification centers is discussed relative to these variables and others. In addition, a sequence of appearance is established for the carpal and tarsal ossification centers in the orangutan and data is presented on the status of these centers in a fetal and newborn gorilla. Study results indicate that 1) there is variation in the number of secondary epiphyses present in animals of similar ages; 2) tarsal ossification is completed prior to carpal ossification in the orangutan; 3) there are indications of a relationship between weight and the number of ossification centers present in animals of similar age; and 4) there appears to be no evidence of specific relationships between carpal and tarsal development and M₁ development. © 1996 Wiley-Liss, Inc.     

Chronology of fusion of the primary and secondary ossification centers in the human sacrum and age estimation in child and adolescent skeletons

Little is known about fusion times of the primary and secondary centers of ossification in the sacrum, particularly from dry bone observations. In this study, the timing of union of these centers was studied in a sample of modern Portuguese skeletons (90 females and 101 males) between the ages of 0 and 30 years, taken from the Lisbon documented skeletal collection. A three‐stage scheme was used to assess fusion status between ossification centers as unfused, partially fused and completely fused. Posterior probability tables of age, given a certain stage of fusion, were calculated for most anatomical locations studied using both reference and uniform priors. Partial union of primary centers of ossification was observed from 1 to 8 years of age and partial union of secondary centers of ossification was observed from 15 to 21 years of age. The first primary centers of ossification to complete fusion are the neural arch with the centrum of the fifth sacral vertebrae and the last are the costal element with the centrum of the first sacral vertebra. The annular and sacroiliac epiphyses are the first, among the secondary centers of ossification observed, to complete fusion, after which the lateral margin fuses. This study offers information on timing of fusion of diverse locations in the developing sacrum useful for age estimation of complete or fragmented immature human skeletal remains and fills an important gap in the literature, by adding to previously published times of fusion of primary and secondary ossification centers in this sample. Am J Phys Anthropol 153:214–225, 2014. © 2013 Wiley Periodicals, Inc.     

Maturation process of secondary ossification centers in the rat and assessment of bone age.

The maturation process from the appearance to the fusion of the secondary ossification centers of extremities was studied in Wistar rats aged 0 to 134 weeks. The examination of the secondary ossification centers made by radiography. The assessment of the stage of development was made in accordance with the criteria proposed by Ohwada and Sutow. The secondary ossification center was found to be take one of the following three types of maturation processes : (1) the acute ossification, (2) the delayed ossification, and (3) the incomplete ossification. No fusion was observed up to 134 weeks in certain epiphyses of the rat. This type of ossification designated as the incomplete ossification may be specific to the mouse and rat. The relative lengths of time required for appearance and fusion in the average prospective life were obtained for the rat. They were compared with those of the mouse and man. The relative length of time necessary for maturity of the secondary ossification centers was shown to be the shortest in the rat and the longest in man. The results suggested that the rat may reach maturity in the bone age at 17 to 21 weeks of age. The rat at this age may be regarded as being adult corresponding to age 17 weeks in mice and 18 to 24 years in man.     

Positional changes of the frontoparietal ossification centers in perinatal craniosynostotic rabbits.

It has been suggested that craniosynostosis is caused by abnormally located ossification centers (i.e., bony tubers) in the developing skull prior to suture formation [Mathijssen et al., 1996, 1997]. The present study was designed to test this hypothesis in a rabbit model of human familial, nonsyndromic coronal suture (CS) synostosis. Calvariae were taken from 99 New Zealand White rabbit perinates (55 normal controls, 15 with delayed-onset CS synostosis, and 29 with bilateral or unilateral CS synostosis), ranging in age from 23 to 34 days postconception (synostosis occurs at approximately 23 days in this model). Frontoparietal, interfrontal, and interparietal ossification center distances were obtained using a Wild microscope with camera lucida attachment and a 2-D computer digitization technique. Linear regression analysis was used to compare age-related changes in the perinatal ossification centers among groups. Results revealed that frontoparietal ossification center regression line slopes had similar start points (24-day intercepts) with significantly (P < 0.05) diverging slopes over time. Normal and delayed-onset ossification center distance increased more rapidly than in synostosed perinates. No significant (P > 0.05) differences were noted in regression line slopes among groups for interparietal or interfrontal ossification center distances. Results demonstrated that, in synostosed perinates, frontoparietal ossification center location was similar to normals around the time of synostosis and became displaced later. These findings suggest that ossification center (i.e., bony tuber) displacement seen in infants with craniosynostosis is probably a secondary and compensatory, postsynostotic change and not a primary causal factor of synostosis in this rabbit model.     

Bone growth aud development of secondary ossification centers of extremities in the cynomolgus monkey (Macaca fascicularis).

The development of so-called long bones in the extremity has been studied roentgenographically in forty-seven males and fifty-one females cynomolgus monkeys bred and reared at the National Institute of Health. The age of the females ranged from five months to eight years and nine months, and that of the males was from four months to seven years. In addition, the fetuses of six to twenty weeks of gestation age were examined for the time of appearance of ossification centers. As the biological parameters concerning body growth, the body weight and the bone length were measured and the secondary ossification centers were scrutinized and assessed the maturity process on the basis of the criteria that divided the state into eleven stages. Also the allometric analyses of body weight against bone length was conducted. Most of the secondary ossification centers except the proximal fibulal epiphysis appeared during the period from the prenatal stage (15-20 weeks of gestationage) to the postnatal one (several months of age). From four to five months of age, many ossification centers had developed to some extent. But, the appearance of proximal fibulal epiphysis was delayed and often lacking until 10 months of age in female and one year and three months of age in male. The earliest epiphyseal fusion was observed at the distal humeral epiphysis in both sexes. The latest epiphyseal fusion was observed at the distal ulnal epiphysis in both sexes and at the distal ulnal and radial epiphyses in female. From this study, the time of fusion was at five and three guarters years of age in females and at six and a half years of age in males. As a result, it is suggested that the estimation of animal's age might be put to practical use by introducing the assessing method that the score was given from the observation of the secondary ossification center.     

Age estimation from stages of epiphyseal union in the presacral vertebrae

The presacral vertebrae have various secondary centers of ossification, whose timing of fusion can be used for age estimation of human skeletal remains up to the middle to the latter third decade. However, detailed information about the age at which these secondary centers of ossification fuse has been lacking. In this study, the timing of epiphyseal union in presacral vertebrae was studied in a sample of modern Portuguese skeletons (57 females and 47 males) between the ages of 9 and 30, taken from the Lisbon documented skeletal collection. A detailed photographic record of these epiphyses and the age ranges for the different stages of epiphyseal union are provided. Partial union of epiphyses was observed from 11 to 27 years of age. In general, centers of ossification begin to fuse first in the cervical and lumbar vertebrae, followed by centers of ossification in the thoracic region. The first center of ossification to complete fusion is usually that of the mammillary process in lumbar vertebrae. This is usually followed by that of the transverse process, spinous transverse process, and annular ring, regardless of vertebra type. There were no statistically significant sex differences in timing of fusion, but there was a trend toward early maturation in females for some vertebra or epiphyses. Bilateral epiphyses did not show statistically significant differences in timing of fusion. This study offers information on timing of fusion of diverse epiphyseal locations useful for age estimation of complete or fragmented human skeletal remains. Am J Phys Anthropol, 2011. © 2010 Wiley‐Liss, Inc.     

Apparent influence of the X chromosome on timing of 73 ossification centers

Among 73 postnatal ossification centers, sister-sister (SS) corretions involving age at appearance tend to exceed brother-brother (BB) and sister-brother (SB) correlations by an average of 0.16. This excess of SS over BB and SB ossification timing similarity is not a function of type of center, limb or location, and is in accordance with the hypothesis of partial X-linkage. It is estimated that the larger proportion of genetically determined variance in postnatal ossification timing may be attributed to genes on the X chromosome.     

Radiographic determination of bone maturation as an aid in predicting chronologic age in the owl monkey (Aotus trivirgatus)

The skeletal development of laboratory-bred owl monkeys (Aotus trivirgatus) ranging from 37 days to 58 months of age was examined radiographically. Femoral length, time of epiphyseal ossification, and fusion of various ossification centers were studied. Chronologic age can be predicted by femoral length determination up to 18 months. Initial ossification of calcaneal, tibial tuberosity, iliac crest, and ischial apophyses occurs between 5.5 and 14 months. Fusion of various secondary ossification centers allows age determination from 7.5 months to 58 months.     

Normal variability in the age and first onset of ossification of the triquetral

The age and order of ossification of the triquetral, among the bones of the hand and wrist, were determined from serial radiographs of 108 males and 103 females of the Oxford Child Health Survey. Although the median ages of ossification agreed reasonably well with the mean ages reported by other authors, the distributions suggested that the former is the more appropriate statistic. The distributions of order of ossification were distinctly bimodal for both sexes because of the tendency of the triquetral to appear along with the epiphyseal centers. The triquetral appeared before the lunate in 184 children, after it in eight, and could not be sequentially distinguished in 19. Excluding these 19, triquetral sequence variability in the remaining was achieved, in 190, through alteration of its appearance relative to the epiphyseal centers and, in the other two through an alteration of the lunate appearance. Measures of median or average order of appearance are of very little value for the triquetral.     

Evolution and homology of the astragalus in early amniotes: new fossils, new perspectives

The reorganization of the ankle in basal amniotes has long been considered a key innovation allowing the evolution of more terrestrial and cursorial behavior. Understanding how this key innovation arose is a complex problem that largely concerns the homologizing of the amniote astragalus with the various ossifications in the anamniote tarsus. Over the last century, several hypotheses have been advanced homologizing the amniote astragalus with the many ossifications in the ankle of amphibian-grade tetrapods. There is an emerging consensus that the amniote astragalus is a complex structure emerging via the co-ossification of several originally separate elements, but the identities of these elements remain unclear. Here we present new fossil evidence bearing on this contentious question. A poorly ossified, juvenile astragalus of the large captorhinid Moradisaurus grandis shows clear evidence of four ossification centers, rather than of three centers or one center as posited in previous models of astragalus homology. Comparative material of the captorhinid Captorhinikos chozaensis is also interpretable as demonstrating four ossification centers. A new, four-center model for the homology of the amniote astragalus is advanced, and is discussed in the context of the phylogeny of the Captorhinidae in an attempt to identify the developmental transitions responsible for the observed pattern of ossification within this clade. Lastly, the broader implications for amniote phylogeny are discussed, concluding that the neomorphic pattern of astragalus ossification seen in all extant reptiles (including turtles) arose within the clade Diapsida.     

The extent of fetal ossification as an index of delayed development in teratogenic studies on the rat

In teratogenic studies toxic effects may manifest themselves in retarded fetal development, such as a reduction in fetal weight. In searching for an additional index, the number of centers of ossification in seven skeletal districts (sternum, metacarpus, metatarsus, cervical and caudal vertebrae, anterior and posterior proximal phalanges) of rat fetuses delivered on days 19, 20 and 21 of gestation were counted and compared. Results showed uneven ossification in day-19 and -20 fetuses, but sufficiently advanced, homogeneous and uniform ossification in day-21 fetuses to provide a reliable quantitative index for evaluating retarded fetal development. It is therefore proposed that the stage of skeletal ossification in day-21 fetuses be used in teratogenic studies in the rat to evaluate retarded fetal development.     

The ossification centers in the lower end of tibiotarsus in domestic fowl.

The morphogenesis of lower end of tibia in chick is studied commonly but the process of ossification of the same has received very little attention so far. The present study is directed to throw some light on the appearance of ossification centers in the lower end of tibiotarsus of chick. The histology of lower end of tibiotarsus was studied by procuring developing tibiotarsi from chick embryos (20) of 6th day incubation till hatching and 3 post hatched chicks. The transparancies of chick embryos at different incubation periods and post hatched chicks were prepared by Dawson's Alizarin staining method. Three cartilage center (tibial, fibulare and intermedium) appeared in 6...9 days of incubation period in the tarsal region. These gradually fused with the lower end of tibia. Three ossification centres developed in the lower end of tibiotarsus. One for intermedium appeared on 16th day and two fotibial and fibulare on 20th day. All these three centres could be located in the transparancies of the chick embryos in tarsal region. The present study proves that the three cartilages centres maintain their individuality during the ossification process even though those fuse completely with the lower end of tibia in chick. The centers for tibial and fibulare are similar to epiphyseal centres of mammals in histological details.