Musculoskeletal System - Bone Development Timeline

Embryology - 5 Dec 2023        Expand to Translate
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Introduction

The adult human skeleton has about 206 different bones, each develop with their own specific bone timeline. Many prenatal bones fuse postnatal developing neonate and child (about 275).

The two main forms of ossification occur in different bones, intramembranous (eg skull) and endochondral (eg vertebra) ossification. Ossification in general continues postnatally, through puberty until mid 20s.

Without postnatal growth in the long bones and axial skeleton, we would be as high as when we are born!

Axial skeleton (80 bones in skull, vertebra, ribs, sternum)

Appendicular skeleton (126 bones in limbs, shoulders, pelvis)

Endochondral ossification within the limb begins at Carnegie stage 18 and also occurs throughout embryo skeleton. This process is the replacement of a cartilage "template" with bone (week 5-12) that continues through postnatal development, with a second surge of growth at puberty.

These notes summarise the timecourse of development of some of these bones in humans. Historically, the ossification timeline in human embryos was published by Mall in 1906 and was the basis of his later publication in his 1910 embryology textbook Manual of Human Embryology.

Some Recent Findings

Primary ossification in the mouse limb.

CT evaluation of timing for ossification of the medial clavicular epiphysis "The clavicle is the first bone to ossify in the developing embryo and the last to complete epiphyseal union. It is the latter sustained period of growth that has attracted the interest of skeletal biologists and forensic practitioners alike, who collectively recognize the important opportunity this bone affords to estimate skeletal age across the prenatal to early adult lifespan. Current research is largely directed towards evaluating the applicability of assessing fusion in the medial epiphysis, specifically for determining age of majority in the living. ...Transition analysis is used to calculate age ranges and determine the mean age for transition between an unfused, fusing and fused status. The maximum likelihood estimates (in years) for transition from unfused to fusing is 20.60 (male) and 19.19 (female); transition from fusing to complete fusion is 21.92 (male) and 21.47 (female)." Ossification of the vertebral column in human foetuses: histological and computed tomography studies "There is no agreement in the literature as to the time of the onset and progress of the vertebral column ossification. The aim of the present study was to determine the precise sequence of ossification of the neural arches and vertebral centra.Histological and radiographic studies were performed on 27 human foetuses aged from 9 to 21 weeks. It was found that the ossification of vertebrae commences in foetuses aged 10 and 11 weeks. Ossification centres appear first for neuralarches in the cervical and upper thoracic vertebrae and by the end of 11th week they are present in all thoracic and lumbar neural arches. In the vertebral centrain foetus of 10 weeks ossification was found in the lower 7 thoracic and first lumbar vertebrae. By the end of 11th week ossification is present in the lower 4 cervical, all thoracic, all lumbar and 4 sacral vertebral centra." Computed Tomography An image-based skeletal tissue model for the ICRP reference newborn "Active marrow distributions were found to be in reasonable agreement with those given previously by the ICRP. However, significant differences were seen in total skeletal and site-specific masses of trabecular and cortical bone between the current and ICRP newborn skeletal tissue models. The latter utilizes an age-independent ratio of 80%/20% cortical and trabecular bone for the reference newborn. In the current study, a ratio closer to 40%/60% is used based upon newborn CT and micro-CT skeletal image analyses. These changes in mineral bone composition may have significant dosimetric implications when considering localized marrow dosimetry for radionuclides that target mineral bone in the newborn child."

More recent papers

This table allows an automated computer search of the external PubMed database using the listed "Search term" text link. This search now requires a manual link as the original PubMed extension has been disabled. The displayed list of references do not reflect any editorial selection of material based on content or relevance. References also appear on this list based upon the date of the actual page viewing. References listed on the rest of the content page and the associated discussion page (listed under the publication year sub-headings) do include some editorial selection based upon both relevance and availability. More? References | Discussion Page | Journal Searches | 2019 References | 2020 References Search term: Bone Development Timeline

Ossification Stages

Epiphysis and epiphyseal disc.

The process of ossification as determined postnatally clinically has been divided into a series of stages.

• Stage 1 - non-ossified epiphysis
• Stage 2 - discernible ossification centre
• Stage 3 - partial fusion
• Stage 4 - total fusion
• Stage 5 - an additional stage recently added is the disappearance of the epiphyseal scar after total fusion.

Clavicle Ossification

The following identifies the process of ossification of the medial clavicular epiphyseal cartilage.

• Stage 3 - 16 years
• Stage 4 - 20 years (women), 21 years (men)
• Stage 5 - 26 years

The Clavicle
Age	No. of instances in girls	No. of instances in boys	No. of centres in girls	No. of centres in boys
11	12	2	1	0
12	ll	9	0	1
13	3	15	0	0
14	8	10	2	2
15	10	1l	2	1
16	16	14	4	1
17	12	12	5	5
18	10	15	2	3
19	25	ll	ll	7
20	28	19	12	7
21	14	20	7	1l
22	18	11	5	4
23	17	16	4	4
24	18	15	4	1
25	19	18	2	2
26	10	8	1	0
Table Data: Flecker (1932)

Medial Clavicular Epiphysis Ossification

The following table compares male and female timing in years of ossification based upon CT analysis.

Event	Male	Female
Transition from unfused to fusing	20.60	19.19
Transition from fusing to complete fusion	21.92	21.47

Long Bone Ossification

Humerus

Appearance and fusion of bone secondary ossification centres, proximal is closer to body and distal is further away from the body.

Appearance

• Proximal epiphysis gestation week 36 - 4 years
• Distal epiphysis 6 months - 10 years

Fusion

• Proximal epiphysis 12 - 20 years
• Distal epiphysis 11 - 19 years

Femur

Appearance

• Proximal epiphysis 1 - 12 years
• Distal epiphysis Gestation week 36 - 40

Fusion

• Proximal epiphysis 11 - 19 years
• Distal epiphysis 14 - 19 years

Data from reference Table 1.

Historic Limb Data

Manual of Human Embryology by Franz Keibel and Franklin P. Mall (1910)

Table - Upper Limb

Upper Limb

Table Of Ossification Of The Bones Of The Superior Extremity

Bone	Centres	Time of appearance of centre	Union of primary and secondary centres; remarks.
Clavicle	Diaphysis	6th week	There are two centres in the shaft, a medial and a lateral. These blend on the 45th day (Mall). Shaft and epiphysis unite between the 20th and 25th years.
	Sternal epiphysis	18th to 20th year
Scapula	Primary centres:		The chief centre appears near the lateral angle. The subcoracoid centre appears at the base of the coracoid process and also gives rise to a part of the superior margin of the glenoid fossa. The coracoid process joins the body about the age of puberty. The acromial epiphysis centres (two or three in number) fuse with one another soon after their appearance and with the spine between the 22nd and 25th years (Quain); 20th year (Wilms). The subcoracoid and the epiphysis of the coracoid process, the glenoid fossa, the inferior angle, and the vertebral margin join between the 18th and 24th years in the order mentioned (Sappey).
	1. That of the body, the spine, and the base of the glenoid cavity.	8th week (Mall) 1
	2. Goraooid process	1st year
	3. Subcoracoid	10th to 12th year
	Epiphyses:
	Acromial epiphyses	15th to 18th year
	Epiphysis of the inferior angle.	16 to 18th year
	Epiphyses of the vertebral border.	18th to 20th year
	Epiphyses of upper surface of coracoid.	16th to 18th year.
	Epiphysis of surface of glenoid fossa.	16th to 18th year.
Humerus	Diaphysis	6th to 7th week (Mall)	The epiphyses of the head, the tuberculum majus and the tuberculum minus (the last is inconstant) unite with one another in 4th-6th year and with the shaft in 20th-25th year. The epiphyses of the capitulum, lateral epicondyle, and trochlea unite with one another and then in the 16th-17th year join the shaft. The epiphysis of the medial epicondyle joins the shaft in the 18th year.
	Epiphyses:
	Head	1st to 2d year
	Tuberculum majus	2d to 3d year
	Tuberculum minus	3d to 5th year
	Capitulum	2d to 3d year
	Epioondylus med	5th to 8th year
	Lateral margin of trochlea	11th to 12th year
	Epicondylus lat	12th to 14th year
Radius	Diaphysis	7th week (Mall)	The superior epiphysis and shaft unite between the 17th and 20th years. The inferior epiphysis and shaft about the 21st year (Pryor); M 21st year, F 21st-25th year (Sappey). Sometimes an epiphysis is found m the tuberosity (R. and K.) and in the styloid process (Sappey).
	Epiphyses:
	Carpal end	F 8th month - M 15th month (Pryor)
	Humeral end	6th-7th year
Ulna	Diaphysis	7th week	The centre for the shaft of the ulna arises a few days later than that for the radius. The proximal epiphysis is united to the shaft about the 17th year; the inferior epiphysis between the 18th and 20th years; F 20th - 21st years, M 21st - 24th years (Sappey). There is sometimes an epiphysis in the styloid process (Sohwegel) and in the tip of the olecranon process (Sappey).
	Epiphyses:
	Carpal end	F 6th-7th year - M 7th-8th year (Pryor)
	Humeral end	10th year
Carpus	Os capitatum	F 3d-6th month M 4th-10th month	The navicular sometimes has two centres of ossification (Serres. Rambaud and Renault). Serres and Pryor have described two centres of ossification in the lunatum. Debierre has described two centres in the pisiform, one in a girl of eleven, the other in a boy of twelve. The OS hamatum may have a special centre for the hamular process. Pryor has found two centres in the triquetrum. Pryor (1908), describes the centres of ossification of the carpal bones as assuming shapes characteristic of each bone at an early period.
	Os hamatum	F 5th-10th month M 6th-12th month
	Os triquetrum	F 2d-3d year M about 3 years
	Os lunatum	F 3rd-4th year M about 4 years
	Os naviculare	F at 4 years, or early in 5th year M about 5 years
	Os mult. maj.	F 4th-5th year M 5th-6th year
	Osmult. min.	F 4th-5th year M 6th-6th year
	Os pisiforme	F 9th-10th year M 12th-3th year
Metacarpals	Diaphyses	9th week (Mall)	The centres for the shafts of the second and third metacarpals are the first to appear. There may be a distal epiphysis for the first metacarpal and a proximal epiphysis for the second. Pryor (1906). found the distal epiphysis of the first metacarpal in about 6 per cent, of cases. It is a family characteristic. It arises before the 4th year and unites later. Pryor found the proximal epiphysis of the second metacarpal in six out of two hundred families. It unites with the shaft between the 4th and 6th-7th year; sometimes, however, not until the 14th year. In the seal and some other animals all the metacarpals have proximal and distal epiphyses (Quain). The epiphyses join the shafts between the 15th and 20th years. There may bean independent epiphysis for the styloid process of the 5th metacarpal. The epiphysis of the metacarpal of the index finger appears first. This is followed by those of the 3d, 4th, 5th, and 1st digits.
	Proximal epiphysis of the first metacarpal	3d year
	Distal epiphyses of the metacarpals	2d year
Phalanges	Diaphyses	9th week (Mall)
First row	Proximal epiphyses	1st-3rd year (Pryor)	The shafts of the phalanges of the second and third fingers are the first to show centres of ossification. The phalanges of the little finger are the last, the epiphysis in the middle finger is the first to appear. This is followed by those of the 4th, 2d, 5th, and 1st digits.
Middle row	Diaphyses	11th-12th week (Mall)	The centres in the shafts of this row are the last to appear. The epiphysis of the phalanx of the middle finger is the first to appear. This is followed by those of the ring, index, and little finger (Pryor).
	Proximal epiphyses	2nd-3rd year
Terminal row	Diaphyses	7th-8th week	The terminal phalanx of the thumb is the first to show a centre of ossification in the shaft. This is the first centre of ossification in the hand. It is developed in connective tissue while the centres of the other phalanges are developed in cartilage (Mall). The epiphysis of the ungual phalanx of the thumb is followed by those of the middle, ring, index, and little fingers. The fusion of the epiphyses of the phalanges with the diaphyses takes place in the 18th-20th year.
	Proximal epiphyses	2nd-3rd year
Sesamoid bones			Ossification begins generally in the 13th - 14th years, and may not take place until after middle life (Thilenius). For table of relative frequency in the embryo and adult see p. 385.
Days and weeks refer to the prenatal, years to the postnatal period. M = male F = female. According to Poirier, Traite d'Anatomie, p. 138, two centres appear in the eighth week, and unite in the third month to form a centre of ossification for the body of the scapula.
Links: limb | bone | upper limb ossification timeline | lower limb ossification timeline | Historic - Chapter 11 Development of the Skeleton | timeline | Category:Timeline     Table Data Reference

Lower Limb

Table Of Ossification Of The Bones Of The Inferior Extremity

Bone	Centres	Time of appearance of centre	Time of fusion: general remarks
Os coxae	Os ilium	56th day (Mall)	The rami of the ischium and the pubis are united by bone in the 7th or 8th year (Quain) ( 12-14 year Sappey). In the acetabulum the three hip bones are separated by a Y-shaped cartilage until after puberty. In this cartilage between the ilium and pubis the "os acetabuli" appears between the ninth and twelfth years. This bone, variable in size, forms a greater or less part of the pubic portion of the articular cavity. Leche (1884). Krause (1885), and many others consider it primarily an independent bone. About puberty between the ilium and ischium and over the acetabular surfaces of these bones small irregular epiphyseal centres appear. The os acetabuli becomes imited to the pubic bone about puberty and soon afterwards the acetabular portions of the ilium and ischium and the ischium and pubis begin to become united by bone. The acetabular portions of the pubis and ilium are unite a little later. Osseous union takes place earlier on the pelvic than on the articular surface of the acetabulum. The union of the several primary centres and the epiphyses is usually completed about the twentieth year.
	Os ischii	105th day (Mall)
	Os pubis	4th to 5th fetal month
	Os acetabuli.	9th to 12th year
	Epiphyses: Those of the acetabulum	Soon after puberty
	Crest of ilium	Soon after puberty	Fuses with main bone 20th to 25th year
	Tuberosity of ischium	Soon after puberty	Fusion begins in the 17th year and is completed between the 20th and 24th years (Sappey)
	Ischial spine	Soon after puberty	18th to 20th year (Poirier).
	Ant. inf. spine of ilium	Soon after puberty	18th to 20th year (Poirier)
	Symphysis end of os pubis (1 or 2 centres)	18th to 20th year (Sappey)	After the 20th year
Femur	Diaphysis	43d day (Mall)
	Epiphyses: Distal end	Shortly before birth1	20th to 24th year
	Head	1st year	18th to 19th year
	Great trochanter	3d to 4th year (Osseous granules soon after birth, (Poirier)	18th year
	Small trochanter	13th to 14th year 8th year (Sappey)	17th year (Quain) Proximal epiphysis 18th to 22d year (Poirier)
Patella		3d to 5th year	The osseous patella reaches its definitive form soon before puberty
Tibia	Diaphysis	44th day (Mall)
	Epiphyses: Proximal end	About birth	19th to 24th year (Sappey)
	Distal end	2d year	16th to 19th year
	Tubercle (occas.)	13th year	Fuses with epiphysis of the proximal end and then with this to the diaphysis
Fibula	Diaphysis	55th day (Mall).
	Epiphyses: Distal end	2d year	20th to 22d year
	Proximal end	3d to 5th year	22d to 24th year
Calcaneus	Chief centre	6th fetal month	The chief nucleus is endochondral. A periosteal nucleus appears frequently in the 4-5 fetal month (Hasselwander)
	Epiphysis (distal end)	10th year (Quain) 7th-8th year ( Sappey)	15th-16th year (Quain) 16th-18th year (Poirier) M 17-21, average 20 years F 13-17, average 16 years (Hasselwander)
Talus		6th fetal month (Hasselwander)	In the 7th-8th year the posterior part of the talus, the os trigonum, is frequently ossified from a special centre (v. Bardeleben). It fuses about the 18th year.
Cuboid		About birth
Cuneiform III		1st year
Cuneiform I		2d-3d year
Cuneiform II		3d-4th year
Navicular		4th-5th year
Metatarsals	Diaphyses	8th-10th week	According to v. Bardeleben a second centre of ossincation appears much later than the primary in the navicular, and finally about the time of puberty a medial epiphyseal centre arises.
	Epiphyses	3d-8th year	The centre for the 2d metatarsal usually appears first, then come the 3rd, 4th, 1st and 5th. The epiphysis of the 1st metatarsal appears at the proximal end of the bone: the other epiphyses arise at the distal ends of the metatarsals. There may be a distal epiphysis in the first metatarsal also.2 In some instances a proximal epiphysis is formed on the tuberosity of the fifth metatarsal (Gruber). The epiphyses unite with the shafts in the 17-21 year in males and in the 14-19 year in females. (Hasselwander).
Phalanges:
Terminal row	Diaphyses	58th day (Mall)
	Epiphyses (distal)	4th year	M 13-23, average 16-21 year. F 13-17, average 14-17 year (Hasselwander).
Middle row	Diaphyses	4th-10th fetal month
	Epiphyses	3d year	M 15-19 year F 13-16 year (Hasselwander)
Proximal row	Diaphyses	3d fetal month
	Epiphyses	3d year	M 15-17 year. F 14-15 year (Hasselwander) The centres for the shafts of the phalanges often appear double, one for the dorsal and one for the plantar surface. The centres for the medial phalanges in each row usually appear before the more laterally placed centres. The centre for the 5th terminal phalanx appears much later than the other centres in this row (Mall). According to Rambaud and Renault the epiphyses arise each from two centres which fuse together. In the terminal phalanx of the great toe the ossification centre of the epiphysis often appears as early as the second or even the first year. (Hasselwander)
Sesamoid bones of the great toe		M 14th year F 12th-13th year	Ossification may begin in the 8th year in females, in the 11th in males (Hasselwander).
Poirier, Traite d'Anatomie, vol. 1. page 227, gives a summary of the literature on the time of the appearance of this epiphysis. The epiphysis has some medico-legal importance, since its presence or absence has been utilized to determine whether a child is born at term. Schwegel found it to appear between birth and the third year; Casper in the ninth fetal month. Hartmann found it lacking in 12 percent, of cases at birth and in 7 per cent, of cases present as early as the eighth fetal month. Mayet has described two centres of ossification for the proximal epiphysis of the first metatarsal, one of which represents the real metatarsal of the first digit.
Days and weeks refer to the prenatal, years to the postnatal period. M = male F = female. According to Poirier, Traite d'Anatomie, p. 138, two centres appear in the eighth week, and unite in the third month to form a centre of ossification for the body of the scapula.
Links: limb | bone | upper limb ossification timeline | lower limb ossification timeline | Historic - Chapter 11 Development of the Skeleton | timeline | Category:Timeline     Table Data Reference

Hip

Ossification of the Os Coxae

• Triradiate cartilage 14 - 16 years.
  • Y-shaped growth plate region within the developing hip seen in childhood x-rays.

Links: musculoskeletal abnormalities

Mandible Ossification

Fetal week 12

Prenatal

Week 6 - Intramembranous ossification center develops lateral to Meckel's cartilage.

Week 7 - Coronoid process begins differentiating.

Week 8 - Coronoid process fuses with main mandibular mass.

• Stage 21
  • bone-formation has taken place and formed a plate on the lateral side of Meckel's cartilage
  • plate is in the substance of, and is surrounded by, that mesodermal condensation that outlines the mandible and precedes the formation of bone.
  • plate of bone is confined to the region of what approximately corresponds to the future body of the mandible
  • mesodermal condensation can be traced further backwards always on the lateral side of Meckel's cartilage and the associated branches of the mandibular nerve.
  • beyond the limit of bone-formation the lateral pterygoid muscle can be seen running into and outlining the terminal part of the mesodermal condensation.
  • rudimentary condylar area - Meckel's cartilage with the inferior dental and lingual nerves on its upper surface lies medial to this area and inferior to the lateral pterygoid muscle.

Week 10 (approx) - Both condylar and coronoid processes are recognizable and anterior portion of Meckel's cartilage begins to ossify.

Weeks 12-14 - Secondary cartilages for the condyle, coronoid, and symphysis appear.

Weeks 14-16 - Deciduous tooth germs start to form.

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  Embryo CRL 24 mm (outer aspect, about Carnegie stage 22)

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  Embryo CRL 24 mm (inner aspect, about Carnegie stage 22)

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  Embryo CRL 95 mm (outer aspect, about Fetal week 12, GA week 14)

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  Embryo CRL 95 mm (inner aspectt, about Fetal week 12, GA week 14)

Birth

Adult Mandible, muscle attachment sites

At birth mandible still has separate right and left halves.

• 

  Birth

• 

  Childhood

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  Adult

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  Old Age

Postnatal

Year 1 - Fusion of right and left halves of mandible at the symphysis.

Infancy and childhood - Increase in both size and shape of the mandible; eruption and replacement of teeth.

Year 12-14 - All permanent teeth emerged except third molars.

Data source- Table 4

Carpal Bones

Data from a wrist study of 57 human embryonic (stages 17-23) and fetal (9-14 weeks).

• stage 17 - undifferentiated mesenchyme
• stage 18 and stage 19 - condensated mesenchyme
• stage19 and stage 20 - pre-chondrogenic
• stages 21 and over - chondrogenic. Chondrification begins with capitate and hamate (stage 19) and ends with pisiform (stage 22).
• week 14 - vascular bud penetrates into the lunate cartilage.

Related nerve, muscle and joint development from the same study.

• stage 18 - hand plate median, ulnar and radial nerves and thenar eminence.
• stages 21 - indications of the interosseous muscles.
• stages 22 - flexor digitorum superficialis, flexor digitorum profundus and lumbrical muscles, transverse carpal ligament and collateral ligaments emerge.
• stages 23 - articular disc, radiocarpal and ulnocarpal ligaments and deep palmar arterial arch.
• week 9 - radiate carpal and interosseous ligaments appear.
• week 10 - dorsal radiocarpal ligament and articular capsule.
• week 13 - synovial membrane present.

Animal Models

Mouse

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  Forelimb E14.5

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  Forelimb E18.5

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  Hindlimb E18.5

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  Limb E18.5

References

Online Textbooks

• Developmental Biology by Gilbert, Scott F. Sunderland (MA): Sinauer Associates, Inc.; c2000 Paraxial and intermediate mesoderm | Osteogenesis: The Development of Bones

• Molecular Biology of the Cell Alberts, Bruce; Johnson, Alexander; Lewis, Julian; Raff, Martin; Roberts, Keith; Walter, Peter New York and London: Garland Science; c2002 Search Molecular Biology of the CellBone Is Continually Remodeled by the Cells Within ItImage: Figure 22-52. Deposition of bone matrix by osteoblasts.Image: Figure 22-56. The development of a long bone.

Reviews

Laor T & Jaramillo D. (2009). MR imaging insights into skeletal maturation: what is normal?. Radiology , 250, 28-38. PMID: 19092089 DOI.

Land C & Schoenau E. (2008). Fetal and postnatal bone development: reviewing the role of mechanical stimuli and nutrition. Best Pract. Res. Clin. Endocrinol. Metab. , 22, 107-18. PMID: 18279783 DOI.

Articles

PARK EA. (1964). THE IMPRINTING OF NUTRITIONAL DISTURBANCES ON THE GROWING BONE. Pediatrics , 33, SUPPL:815-62. PMID: 14152896

Search PubMed

• Bone Development

Search Pubmed: Human Bone Development Timeline | Human Bone Development

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Terms

• growth recovery lines (growth arrest lines, Harris lines, Parks lines) - lines visible on x-ray images of increased bone density that represent the position of the growth plate at the time of insult to the organism and formed on long bones due to growth arrest. Insults can include juvenile malnutrition, disease or trauma.

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• Mall
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  Fig 1 Embryo No. 333

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  Fig 2 Embryo No. 284

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  Fig 3 Occipital Ossification

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  Fig 4 Embryo No. 284 Head

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  Fig 5 Embryo No. 300 Hand

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  Fig 6 Embryo No. 300 Leg

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