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.     

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.     

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.     

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.     

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.     

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.     

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.     

Epigenetic mechanical factors in the evolution of long bone epiphyses

In developing vertebrate long bones in which endochondral ossification occurs, it is preceded or accompanied by perichondral ossification. The speed and extent of perichondral apposition relative to endochondral ossification varies in different taxa. Perichondral ossification dominates early long bone development in extinct basal tetrapods and dinosaurs, extant bony fish, amphibians, and birds. In mammals and lizards, perichondral and endochondral ossification proceed more synchronously. One of the most important epigenetic factors in skeletogenesis is mechanical loading caused by muscle contractions which begin in utero or in ovo . It has been previously shown that the stress distributions created perinatally in the chondroepiphysis during human skeletal development can influence the appearance of secondary ossification centres. Using finite element computer models representing bones near birth or hatching, we demonstrate that in vertebrates in which perichondral ossification significantly precedes endochondral ossification, the distribution of mechanical stresses in the ossifying cartilage anlagen tends to inhibit the appearance of secondary ossification centres in the ends of long bones. In models representing vertebrates in which endochondral ossification keeps pace with perichondral apposition, the appearance of secondary centres is promoted. The appearance of secondary centres leads to the formation of bony epiphyses and growth plates, which are most common in mammals and extant lizards. We postulate that genotypic factors influencing the relative speed and extent of perichondral and endochondral ossification interact with mechanical epigenetic factors early in development to account for many of the morphological differences observed in vertebrate skeletons.     

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.     

Intercentrum versus pleurocentrum growth in early tetrapods: A paleohistological approach

A variety of vertebral centrum morphologies have evolved within early tetrapods which range from multipartite centra consisting of intercentra and pleurocentra in stem‐tetrapods, temnospondyls, seymouriamorphs, and anthracosaurs up to monospondylous centra in lepospondyls. With the present study, we aim to determine the formation of both intercentrum and pleurocentrum and asked whether these can be homologized based on their bone histology. Both intercentra and pleurocentra ossified endochondrally and periosteal bone was subsequently deposited on the outer surface of the centra. Our observations indicate low histological variation between intercentrum and pleurocentrum in microstructural organization and growth which inhibits the determination of homologies. However, intercentrum and pleurocentrum development differs during ontogeny. As previously assumed, the intercentrum arises from ventrally located and initially paired ossification centers that fuse ventromedially to form the typical, crescentic, rhachitomous intercentrum. In contrast, presacral pleurocentra may be ancestrally represented by four ossification centers: a ventral and a dorsal pair. Subsequently, two divergent developmental patterns are observed: In stem‐tetrapods and temnospondyls, the pleurocentrum evolves from the two dorsally located ossification centers which may occasionally fuse to form a dorsal crescent. In some dvinosaurian temnospondyls, the pleurocentrum may even ossify to full rings. In comparison, the pleurocentrum of stem‐amniotes (anthracosaurs, chroniosuchids, seymouriamorphs, and lepospondyls) arises from the two ventrally located ossification centers whereby the ossification pattern is almost identical to that of temnospondyls but mirror‐inverted. Thus, the ring‐shaped pleurocentrum of Discosauriscus ossifies from ventral to dorsal. We also propose that the ossified portions of the intercentrum and pleurocentrum continued as cartilaginous rings or discs that surrounded the notochord in the living animals.     

Relationship between the chondrocyte maturation cycle and the endochondral ossification in the diaphyseal and epiphyseal ossification centers

The chondrocyte maturation cycle and endochondral ossification were studied in human, fetal cartilage Anlagen and in postnatal meta‐epiphyses. The relationship between the lacunar area, the inter‐territorial fibril network variations, and calcium phosphorus nucleation in primary and secondary ossification centers were assessed using light microscopy and scanning electron microscopy (SEM) morphometry. The Anlage topographic, zonal classification was derived from the anatomical nomenclature of the completely developed long bone (diaphysis, metaphyses and epiphyses). A significant increase in the chondrocyte lacunar area was documented in the Anlage of epiphyseal zones 4 and 3 to zone 2 (metaphysis) and zone 1 (diaphysis), with the highest variation from zone 2 to zone 1. An inverse reduction in the intercellular matrix area and matrix interfibrillar empty space was also documented. These findings are consistent with the osmotic passage of free cartilage water from the interfibrillar space into the swelling chondrocytes, which increased the ion concentrations to a critical threshold for mineral precipitation in the matrix. The mineralized cartilage served as a scaffold for osteoblast apposition both in primary and secondary ossification centers and in the metaphyseal growth plate cartilage, though at different periods of bone Anlage development and with distinct patterns for each zone. All developmental processes shared a common initial pathway but progressed at different rates, modes and organization in diaphysis, metaphysis and epiphysis. In the ossification phase the developing vascular supply appeared to play a key role in determining the cortical or trabecular structure of the long bones. J. Morphol. 277:1187–1198, 2016. © 2016 Wiley Periodicals, Inc.     

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.     

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.     

Development of the skeleton in the sheep and the goat. IV. Osteogenesis of the cranium]

1. The osteogenesis of the cranium was studied on a precisely dated embryological and postnatal material from merino-sheep and goats (crossbreed). 2. The order and duration of the appearance of ossification centers were determined (see Fig. 6). 3. It was noticed that, in small ruminants, the beginning of cranial ossification indifferent to other parts of the skeleton is not staged in time. Sexual dimorphism was only manifested by larger proportions of the male fetuses. An exception was noted only in os interparietale, which in male fetuses appeared 4 to 5 days later in male fetuses. 4. The cranial bones of small ruminants, showed a high degree of ossification at birth.     

Radiographic Evaluation of Appendicular Skeletal Maturation in the Common Marmoset (Callithrix jacchus)

The thoracic appendicular skeletal development of five common marmosets was monitored radiographically at weekly intervals from 1 day to 94 weeks of age and the times of appearance and fusion of 47 ossification centers were recorded. A range and average age for the appearance and fusion of each ossification center were calculated and compared to data available for the rhesus monkey and man.     

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.     

A study of postnatal appendicular skeletal maturation in captive-born squirrel monkeys (Saimiri boliviensis)

This study is based on a mixed longitudinal radiographic sampling of appendicular bones in 82 captive-born squirrel monkeys (Saimiri boliviensis). All appendicular ossification centers had appeared radiographically by 17 weeks of age, and epiphyseal fusion was complete by 47-53 months of age. No statistically significant differences were found between the sexes in comparisons carried out at birth and at 6 and 8 months of age. Valid sex comparisons could not be made at other ages owing to the small size of the sample. The sequence of appearance of the ossification centers (Spearman correlation coefficient of Saimiri vs. Callithrix = 0.68) shows greater interspecies differences than the sequence of fusion (Saimiri vs. Callithrix = 0.88).     

The skull of the Round Island boa, Casarea dussumieri Schlegel, based on high-resolution X-ray computed tomography

The skull of the rare bolyeriid snake Casarea dussumieri is described in detail based on high-resolution X-ray CT data. Bolyeriids are unique in their possession of a separate suborbital ossification and a maxilla subdivided into two movably jointed parts, which may be the result of paedomorphic truncation of the development of the maxilla from multiple ossification centers. Comparison of the skull of C. dussumieri to that of larger booids suggests additional paedomorphic features including reduction of the dorsal lamina of the nasal and prefrontal and reduction of their contacts with the frontal, limited posterior extent of the posterior free process of the supratemporal, and reduction of the coronoid and splenial. The observations herein do not resolve competing phylogenetic hypotheses based on morphology, which either place tropidophiids as the sister-taxon of bolyeriids, Acrochordus and colubroids, or place bolyeriids as the sister-taxon of the other three. But these observations provide no support whatsoever for the heterodox placement of tropidophiids at the base of alethinophidian snakes, as obtained recently with molecular data.