Skip to main content
Top
Published in: Surgical and Radiologic Anatomy 8/2016

Open Access 01-10-2016 | Original Article

Morphometric study of the two fused primary ossification centers of the clavicle in the human fetus

Authors: Mariusz Baumgart, Marcin Wiśniewski, Magdalena Grzonkowska, Mateusz Badura, Małgorzata Dombek, Bogdan Małkowski, Michał Szpinda

Published in: Surgical and Radiologic Anatomy | Issue 8/2016

Login to get access

Abstract

Purposes

A satisfactory understanding of the clavicle development may be contributing to both the diagnosis of its congenital defects and prevention of perinatal damage to the shoulder girdle. This study was carried out to examine the transverse and sagittal diameters, cross-sectional area and volume of the two fused primary ossification centers of the clavicle.

Methods

Using the methods of CT, digital-image analysis and statistics, the size for two fused primary ossification centers of the clavicle in 42 spontaneously aborted human fetuses at ages of 18–30 weeks was studied.

Results

Without any male–female and right-left significant differences, the best fit growth models for two fused primary ossification centers of the clavicle were as follows: y = −31.373 + 15.243 × ln(age) ± 1.424 (R 2 = 0.74) for transverse diameter, y = −7.945 + 3.225 × ln(age) ± 0.262 (R 2 = 0.78), y = −4.503 + 2.007 × ln(age) ± 0.218 (R 2 = 0.68), and y = −4.860 + 2.117 × ln(age) ± 0.200 (R 2 = 0.73) for sagittal diameters of the lateral, middle and medial ends respectively, y = −31.390 + 2.432 × age ± 4.599 (R 2 = 0.78) for cross-sectional area, and y = 28.161 + 0.00017 × (age)4 ± 15.357 (R 2 = 0.83) for volume.

Conclusions

With no sex and laterality differences, the fused primary ossification centers of the clavicle grow logarithmically in both transverse and sagittal diameters, linearly in cross-sectional area, and fourth-degree polynomially in volume. Our normative quantitative findings may be conducive in monitoring normal fetal growth and screening for inherited faults and anomalies of the clavicle in European human fetuses.
Literature
1.
go back to reference Baumgart M, Szpinda M, Szpinda A (2013) New anatomical data on the growing C4 vertebra and its three ossification centers in human fetuses. Surg Radiol Anat 35:191–203CrossRefPubMed Baumgart M, Szpinda M, Szpinda A (2013) New anatomical data on the growing C4 vertebra and its three ossification centers in human fetuses. Surg Radiol Anat 35:191–203CrossRefPubMed
2.
go back to reference Chano T, Matsumoto K, Ishizawa M, Morimoto S, Hukuda S, Okabe H, Kato H, Fujino S (1996) Analysis of the presence of osteocalcin, S-100 protein, and proliferating cell nuclear antigen in cells of various types of osteosarcomas. Eur J Histochem 40:189–198PubMed Chano T, Matsumoto K, Ishizawa M, Morimoto S, Hukuda S, Okabe H, Kato H, Fujino S (1996) Analysis of the presence of osteocalcin, S-100 protein, and proliferating cell nuclear antigen in cells of various types of osteosarcomas. Eur J Histochem 40:189–198PubMed
3.
go back to reference Chen Y, Ao R, Zeng B (2009) Thoracic outlet syndrome caused by malunion of a midshaft clavicle fracture. Injury Extra 40(9):159–161CrossRef Chen Y, Ao R, Zeng B (2009) Thoracic outlet syndrome caused by malunion of a midshaft clavicle fracture. Injury Extra 40(9):159–161CrossRef
4.
go back to reference Currarino G, Herring JA (2009) Congenital pseudarthrosis of the clavicle. Pediatr Radiol 39(12):1343–1349CrossRefPubMed Currarino G, Herring JA (2009) Congenital pseudarthrosis of the clavicle. Pediatr Radiol 39(12):1343–1349CrossRefPubMed
5.
go back to reference Duarte WR, Shibata T, Takenaga K, Takahashi E, Kubota K, Ohya K, Ishikawa I, Yamauchi M, Kasugai S (2003) S100A4: a novel negative regulator of mineralization and osteoblast differentiation. J Bone Miner Res 18:493–501CrossRefPubMed Duarte WR, Shibata T, Takenaga K, Takahashi E, Kubota K, Ohya K, Ishikawa I, Yamauchi M, Kasugai S (2003) S100A4: a novel negative regulator of mineralization and osteoblast differentiation. J Bone Miner Res 18:493–501CrossRefPubMed
7.
8.
go back to reference Flecker H (1942) Time of appearance and fusion of ossification centers and observed by roentgenographic methods. Am J Roentgenol 47:97–159 Flecker H (1942) Time of appearance and fusion of ossification centers and observed by roentgenographic methods. Am J Roentgenol 47:97–159
10.
go back to reference Hansman F, Charotte MD (1962) Appearance and fusion of ossification centers in the human skeleton. Am J Roentgenol Radium Ther Nucl Med 88(3):476–482PubMed Hansman F, Charotte MD (1962) Appearance and fusion of ossification centers in the human skeleton. Am J Roentgenol Radium Ther Nucl Med 88(3):476–482PubMed
11.
go back to reference Kumar R, Madewell JE, Swischuk LE (1989) The clavicle: normal and abnormal. Radiographics 9(4):677–705CrossRefPubMed Kumar R, Madewell JE, Swischuk LE (1989) The clavicle: normal and abnormal. Radiographics 9(4):677–705CrossRefPubMed
12.
go back to reference Lam MH, Wong GY, Lao TT (2002) Reappraisal of neonatal clavicular fracture: relationship between infant size and neonatal morbidity. Am J Obstet Gynecol 100(1):115–119 Lam MH, Wong GY, Lao TT (2002) Reappraisal of neonatal clavicular fracture: relationship between infant size and neonatal morbidity. Am J Obstet Gynecol 100(1):115–119
13.
go back to reference Meyer DB, O’Rahilly R (1956) Roentgenographic investigation of the human skeleton during early fetal life. Am J Roentgenol Radium Ther Nucl Med 76(3):455–468PubMed Meyer DB, O’Rahilly R (1956) Roentgenographic investigation of the human skeleton during early fetal life. Am J Roentgenol Radium Ther Nucl Med 76(3):455–468PubMed
14.
go back to reference Noback CR (1954) The appearance of ossification centers and the fusion of bones. Am J Phys Anthropol 12(1):63–69CrossRefPubMed Noback CR (1954) The appearance of ossification centers and the fusion of bones. Am J Phys Anthropol 12(1):63–69CrossRefPubMed
15.
go back to reference Ogata S, Uhthoff HK (1990) The early development and ossification of the human clavicle an embryologic study. Acta Orthop Scand 61(4):330–334CrossRefPubMed Ogata S, Uhthoff HK (1990) The early development and ossification of the human clavicle an embryologic study. Acta Orthop Scand 61(4):330–334CrossRefPubMed
16.
go back to reference Ogden JA, Conlogue GJ, Bronson ML (1979) Radiology of postnatal skeletal development. III. The clavicle. Skelet Radiol 4(4):196–203CrossRef Ogden JA, Conlogue GJ, Bronson ML (1979) Radiology of postnatal skeletal development. III. The clavicle. Skelet Radiol 4(4):196–203CrossRef
17.
go back to reference O’Rahilly R, Gardner E (1972) The initial appearance of ossification in staged human embryos. Am J Anat 134(3):291–301CrossRefPubMed O’Rahilly R, Gardner E (1972) The initial appearance of ossification in staged human embryos. Am J Anat 134(3):291–301CrossRefPubMed
18.
go back to reference Padua R, Romanini E, Conti C, Padua L, Serra F (1999) Bilateral congenital pseudoarthrosis of the clavicle report of a case with clinical, radiological and neurophysiological evaluation. Acta Orthop Belg 65(3):372–375PubMed Padua R, Romanini E, Conti C, Padua L, Serra F (1999) Bilateral congenital pseudoarthrosis of the clavicle report of a case with clinical, radiological and neurophysiological evaluation. Acta Orthop Belg 65(3):372–375PubMed
19.
go back to reference Page C, Taha F, Le Gars D (2002) Three-dimensional imaging of the petrous bone for the middle fossa approach to the internal acoustic meatus: an experimental study. Surg Radiol Anat 24:388–392PubMed Page C, Taha F, Le Gars D (2002) Three-dimensional imaging of the petrous bone for the middle fossa approach to the internal acoustic meatus: an experimental study. Surg Radiol Anat 24:388–392PubMed
20.
go back to reference Pryse-Davies J, Smitham JH, Napier KA (1974) Factors influencing development of secondary ossification centers in the fetus and newborn. Arch Dis Child 49:425–431CrossRefPubMedPubMedCentral Pryse-Davies J, Smitham JH, Napier KA (1974) Factors influencing development of secondary ossification centers in the fetus and newborn. Arch Dis Child 49:425–431CrossRefPubMedPubMedCentral
21.
go back to reference Schmidt S, Mühler M, Schmeling A, Reisinger W, Schulz R (2007) Magnetic resonance imaging of the clavicular ossification. Int J Legal Med 121:321–324CrossRefPubMed Schmidt S, Mühler M, Schmeling A, Reisinger W, Schulz R (2007) Magnetic resonance imaging of the clavicular ossification. Int J Legal Med 121:321–324CrossRefPubMed
22.
go back to reference Sherer DM, Sokolovski M, Dalloul M, Khoury-Collado F, Osho JA, Lamarque MD, Abulafia O (2006) Fetal clavicle length throughout gestation: a normogram. Ultrasound Obstet Gynecol 27:306–310CrossRefPubMed Sherer DM, Sokolovski M, Dalloul M, Khoury-Collado F, Osho JA, Lamarque MD, Abulafia O (2006) Fetal clavicle length throughout gestation: a normogram. Ultrasound Obstet Gynecol 27:306–310CrossRefPubMed
23.
go back to reference Serre T, Brunet C, Bidal S, Behr M, Ghannouchi SE, Chabert L, Durand F, Cavallero C, Bonnoit J (2002) The seated man: geometry acquisition and three-dimensional reconstruction. Surg Radiol Anat 24:382–387PubMed Serre T, Brunet C, Bidal S, Behr M, Ghannouchi SE, Chabert L, Durand F, Cavallero C, Bonnoit J (2002) The seated man: geometry acquisition and three-dimensional reconstruction. Surg Radiol Anat 24:382–387PubMed
24.
go back to reference Silveira de Figueiredo MJPS, Braga SR, Akkari M, Lopes Prado JC, Santili C (2012) Congenital pseudarthrosis of the clavicle. Rev Bras Ortop 47(1):21–26 Silveira de Figueiredo MJPS, Braga SR, Akkari M, Lopes Prado JC, Santili C (2012) Congenital pseudarthrosis of the clavicle. Rev Bras Ortop 47(1):21–26
25.
go back to reference Standring S (2008) Gray’s anatomy. The anatomical basis of clinical practice. Elsevier, Edinburgh, pp 791–793 Standring S (2008) Gray’s anatomy. The anatomical basis of clinical practice. Elsevier, Edinburgh, pp 791–793
26.
go back to reference Szpinda M, Baumgart M, Szpinda A, Woźniak A, Mila-Kierzenkowska C (2013) Cross-sectional study of the neural ossification centers of vertebrae C1–S5 in the human fetus. Surg Radiol Anat 35:701–711CrossRefPubMedPubMedCentral Szpinda M, Baumgart M, Szpinda A, Woźniak A, Mila-Kierzenkowska C (2013) Cross-sectional study of the neural ossification centers of vertebrae C1–S5 in the human fetus. Surg Radiol Anat 35:701–711CrossRefPubMedPubMedCentral
27.
go back to reference Szpinda M, Baumgart M, Szpinda A, Woźniak A, Mila-Kierzenkowska C (2013) New patterns of the growing L3 vertebra and its 3 ossification centers in human fetuses—a CT, digital, and statistical study. Med Sci Monitor Basic Res 19:169–180CrossRef Szpinda M, Baumgart M, Szpinda A, Woźniak A, Mila-Kierzenkowska C (2013) New patterns of the growing L3 vertebra and its 3 ossification centers in human fetuses—a CT, digital, and statistical study. Med Sci Monitor Basic Res 19:169–180CrossRef
28.
go back to reference Szpinda M, Baumgart M, Szpinda A, Woźniak A, Mila-Kierzenkowska C (2015) Cross-sectional study of C1–S5 vertebral bodies in human fetuses. Arch Med Sci 11(1):174–189 Szpinda M, Baumgart M, Szpinda A, Woźniak A, Mila-Kierzenkowska C (2015) Cross-sectional study of C1–S5 vertebral bodies in human fetuses. Arch Med Sci 11(1):174–189
29.
go back to reference Szpinda M, Baumgart M, Szpinda A, Woźniak A, Małkowski B, Wiśniewski M, Mila-Kierzenkowska C, Króliczewski D (2013) Cross-sectional study of the ossification center of the C1-S5 vertebral bodies. Surg Radiol Anat 35:395–402CrossRefPubMed Szpinda M, Baumgart M, Szpinda A, Woźniak A, Małkowski B, Wiśniewski M, Mila-Kierzenkowska C, Króliczewski D (2013) Cross-sectional study of the ossification center of the C1-S5 vertebral bodies. Surg Radiol Anat 35:395–402CrossRefPubMed
30.
go back to reference Szpinda M, Baumgart M, Szpinda A, Woźniak A, Mila-Kierzenkowska C, Dombek M, Kosiński A, Grzybiak M (2013) Morphometric study of the T6 vertebra and its three ossification centers in the human fetus. Surg Radiol Anat 35:901–916CrossRefPubMedPubMedCentral Szpinda M, Baumgart M, Szpinda A, Woźniak A, Mila-Kierzenkowska C, Dombek M, Kosiński A, Grzybiak M (2013) Morphometric study of the T6 vertebra and its three ossification centers in the human fetus. Surg Radiol Anat 35:901–916CrossRefPubMedPubMedCentral
31.
go back to reference Szymański M, Kędzia A (2008) Digital-image analysis of the clavicle ossification centers during prenatal period. KOWBAN 15:305–312 (in Polish) Szymański M, Kędzia A (2008) Digital-image analysis of the clavicle ossification centers during prenatal period. KOWBAN 15:305–312 (in Polish)
32.
go back to reference Tanaka JL, Ono E, Filho EM, Castilho JC, Moraes LC, Moraes ME (2006) Cleidocranial dysplasia: importance of radiographic images in diagnosis of the condition. J Oral Sci 48(3):161–166CrossRefPubMed Tanaka JL, Ono E, Filho EM, Castilho JC, Moraes LC, Moraes ME (2006) Cleidocranial dysplasia: importance of radiographic images in diagnosis of the condition. J Oral Sci 48(3):161–166CrossRefPubMed
33.
go back to reference Tripathi S, Singh RD, Singh SV, Chand P (2012) A case of cleidocranial dysostosis: dilemma for a prosthodontist. J Indian Prosthodont Soc. 12(4):252–255CrossRefPubMedPubMedCentral Tripathi S, Singh RD, Singh SV, Chand P (2012) A case of cleidocranial dysostosis: dilemma for a prosthodontist. J Indian Prosthodont Soc. 12(4):252–255CrossRefPubMedPubMedCentral
34.
go back to reference Unger S, Mornet E, Mundlos S, Blaster S, Cole DEC (2002) Severe cleidocranial dysplasia can mimic hypophosphatasia. Eur J Pediatr 161:623–626CrossRefPubMed Unger S, Mornet E, Mundlos S, Blaster S, Cole DEC (2002) Severe cleidocranial dysplasia can mimic hypophosphatasia. Eur J Pediatr 161:623–626CrossRefPubMed
35.
go back to reference Vignolo M, Ginocchio G, Parodi A, Torrisi C, Pistorio A, Venturini PL, Aicardi G, De Biasio P (2005) Fetal spine ossification: the gender and individual differences illustrated by ultrasonography. Ultrasound Med Biol 31(6):733–738CrossRefPubMed Vignolo M, Ginocchio G, Parodi A, Torrisi C, Pistorio A, Venturini PL, Aicardi G, De Biasio P (2005) Fetal spine ossification: the gender and individual differences illustrated by ultrasonography. Ultrasound Med Biol 31(6):733–738CrossRefPubMed
36.
go back to reference Vijayan V, El Tan C (2000) Computer-generated three-dimensional morphology of the hepatic hilar bile ducts in biliary atresia. J Pediatr Surg 35(8):1230–1235 Vijayan V, El Tan C (2000) Computer-generated three-dimensional morphology of the hepatic hilar bile ducts in biliary atresia. J Pediatr Surg 35(8):1230–1235
Metadata
Title
Morphometric study of the two fused primary ossification centers of the clavicle in the human fetus
Authors
Mariusz Baumgart
Marcin Wiśniewski
Magdalena Grzonkowska
Mateusz Badura
Małgorzata Dombek
Bogdan Małkowski
Michał Szpinda
Publication date
01-10-2016
Publisher
Springer Paris
Published in
Surgical and Radiologic Anatomy / Issue 8/2016
Print ISSN: 0930-1038
Electronic ISSN: 1279-8517
DOI
https://doi.org/10.1007/s00276-016-1640-y

Other articles of this Issue 8/2016

Surgical and Radiologic Anatomy 8/2016 Go to the issue