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Published in: Surgical and Radiologic Anatomy 3/2013

Open Access 01-04-2013 | Original Article

New anatomical data on the growing C4 vertebra and its three ossification centers in human fetuses

Authors: Mariusz Baumgart, Michał Szpinda, Anna Szpinda

Published in: Surgical and Radiologic Anatomy | Issue 3/2013

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Abstract

Purpose

Detailed knowledge on the normative growth of the spine is of great relevance in the prenatal diagnosis of its abnormalities. The present study was conducted to compile age-specific reference data for vertebra C4 and its three ossification centers in human fetuses.

Materials and methods

With the use of CT (Biograph mCT), digital image analysis (Osirix 3.9) and statistical analysis (Wilcoxon signed-rank test, Kolmogorov–Smirnov test, Levene’s test, Student’s t test, one-way ANOVA, post hoc RIR Tukey test, linear and nonlinear regression analysis), the normative growth of vertebra C4 and its three ossification centers in 55 spontaneously aborted human fetuses (27 males, 28 females) aged 17–30 weeks was examined.

Results

Significant differences in neither sex nor laterality were found. The height and transverse and sagittal diameters of the C4 vertebral body increased logarithmically as: y = −3.866 + 2.225 × ln(Age) ± 0.238 (R 2 = 0.69), y = −7.077 + 3.547 × ln(Age) ± 0.356 (R 2 = 0.72) and y = −3.886 + 2.272 × ln(Age) ± 0.222 (R 2 = 0.73), respectively. The C4 vertebral body grew linearly in cross-sectional area as y = −7.205 + 0.812 × Age ± 1.668 (R 2 = 0.76) and four-degree polynomially in volume as y = 14.108 + 0.00007 × Age4 ± 6.289 (R 2 = 0.83). The transverse and sagittal diameters, cross-sectional area and volume of the ossification center of the C4 vertebral body generated the following functions: y = −8.836 + 3.708 × ln(Age) ± 0.334 (R 2 = 0.76), y = −7.748 + 3.240 × ln(Age) ± 0.237 (R 2 = 0.83), y = −4.690 + 0.437 × Age ± 1.172 (R 2 = 0.63) and y = −5.917 + 0.582 × Age ± 1.157 (R 2 = 0.77), respectively. The ossification center-to-vertebral body volume ratio gradually declined with age. On the right and left, the neural ossification centers showed the following growth: y = −19.601 + 8.018 × ln(Age) ± 0.369 (R 2 = 0.92) and y = −15.804 + 6.912 × ln(Age) ± 0.471 (R 2 = 0.85) for length, y = −5.806 + 2.587 × ln(Age) ± 0.146 (R 2 = 0.88) and y = −5.621 + 2.519 × ln(Age) ± 0.146 (R 2 = 0.88) for width, y = −9.188 + 0.856 × Age ± 2.174 (R 2 = 0.67) and y = −7.570 + 0.768 × Age ± 2.200 (R 2 = 0.60) for cross-sectional area, and y = −13.802 + 1.222 × Age ± 1.872 (R 2 = 0.84) and y = −11.038 + 1.061 × Age ± 1.964 (R 2 = 0.80) for volume, respectively.

Conclusions

The morphometric parameters of vertebra C4 and its three ossification centers show no sex differences. The C4 vertebral body increases logarithmically in height and both sagittal and transverse diameters, linearly in cross-sectional area, and four-degree polynomially in volume. The three ossification centers of vertebra C4 grow logarithmically in both transverse and sagittal diameters, and linearly in both cross-sectional area and volume. The age-specific reference intervals for evolving vertebra C4 may be useful in the prenatal diagnosis of congenital spinal defects.
Literature
1.
go back to reference Abe S, Suzuki M, Cho KH, Murakami G, Cho BH, Ide Y (2011) CD34-positive developing vessels and other structures in human fetuses: an immunohistochemical study. Surg Radiol Anat 33:919–927PubMedCrossRef Abe S, Suzuki M, Cho KH, Murakami G, Cho BH, Ide Y (2011) CD34-positive developing vessels and other structures in human fetuses: an immunohistochemical study. Surg Radiol Anat 33:919–927PubMedCrossRef
2.
go back to reference Bagnall KM, Harris PF, Jones PRM (1979) A radiographic study of the human fetal spine. 3. Longitudinal development of the ossification centres. J Anat 128:777–787PubMed Bagnall KM, Harris PF, Jones PRM (1979) A radiographic study of the human fetal spine. 3. Longitudinal development of the ossification centres. J Anat 128:777–787PubMed
3.
go back to reference Bareggi R, Grill V, Zweyer M, Narducci P, Forabosco A (1994) A quantitative study on the spatial and temporal ossification patterns of vertebral centra and neural arches and their relationship to the fetal age. Ann Anat 176:311–317PubMedCrossRef Bareggi R, Grill V, Zweyer M, Narducci P, Forabosco A (1994) A quantitative study on the spatial and temporal ossification patterns of vertebral centra and neural arches and their relationship to the fetal age. Ann Anat 176:311–317PubMedCrossRef
4.
go back to reference de Biasio P, Ginocchio G, Aicardi G, Ravera G, Venturini PL (2003) Ossification timing of sacral vertebrae by ultrasound in the mid-second trimester of pregnancy. Prenat Diagn 23:1056–1059PubMedCrossRef de Biasio P, Ginocchio G, Aicardi G, Ravera G, Venturini PL (2003) Ossification timing of sacral vertebrae by ultrasound in the mid-second trimester of pregnancy. Prenat Diagn 23:1056–1059PubMedCrossRef
5.
go back to reference Chen Y, Zhuang Z, Qi W, Yang H, Chen Z, Wang X, Kong K (2011) A three-dimensional study of the atlantodental interval in a normal Chinese population using reformatted computed tomography. Surg Radiol Anat 33:801–806PubMedCrossRef Chen Y, Zhuang Z, Qi W, Yang H, Chen Z, Wang X, Kong K (2011) A three-dimensional study of the atlantodental interval in a normal Chinese population using reformatted computed tomography. Surg Radiol Anat 33:801–806PubMedCrossRef
6.
go back to reference Cho KH, Rodríguez-Vázquez JF, Kim JH, Abe H, Murakami G, Cho BH (2011) Early fetal development of the human cerebellum. Surg Radiol Anat 33:523–530PubMedCrossRef Cho KH, Rodríguez-Vázquez JF, Kim JH, Abe H, Murakami G, Cho BH (2011) Early fetal development of the human cerebellum. Surg Radiol Anat 33:523–530PubMedCrossRef
7.
go back to reference Chrzan R, Podsiadlo L, Herman-Sucharska I, Urbanik A, Bryll A (2010) Persistent notochordal canal imitating compression fracture—plain film, CT and MR appearance. Med Sci Monit 16:76–79 Chrzan R, Podsiadlo L, Herman-Sucharska I, Urbanik A, Bryll A (2010) Persistent notochordal canal imitating compression fracture—plain film, CT and MR appearance. Med Sci Monit 16:76–79
8.
go back to reference Cui G, Watanabe K, Hosogane N, Tsuji T, Ishii K, Nakamura M, Toyama Y, Chiba K, Lenke LG, Matsumoto M (2012) Morphologic evaluation of the thoracic vertebrae for safe free-hand pedicle screw placement in adolescent idiopathic scoliosis: a CT-based anatomical study. Surg Radiol Anat 34:209–216PubMedCrossRef Cui G, Watanabe K, Hosogane N, Tsuji T, Ishii K, Nakamura M, Toyama Y, Chiba K, Lenke LG, Matsumoto M (2012) Morphologic evaluation of the thoracic vertebrae for safe free-hand pedicle screw placement in adolescent idiopathic scoliosis: a CT-based anatomical study. Surg Radiol Anat 34:209–216PubMedCrossRef
9.
go back to reference Dimeglio A, Bonnel F, Canavese F (2011) Normal growth of the spine and thorax. In: Akbarnia BA, Yazici M, Thompson GH (eds) The growing spine. Springer, Berlin, Heidelberg, pp 13–42 Dimeglio A, Bonnel F, Canavese F (2011) Normal growth of the spine and thorax. In: Akbarnia BA, Yazici M, Thompson GH (eds) The growing spine. Springer, Berlin, Heidelberg, pp 13–42
10.
go back to reference Dimeglio A, Canavese F, Charles YP (2011) Growth and adolescent idiopathic scoliosis: when and how much? J Pediatr Orthop 32(Suppl 1):28–36CrossRef Dimeglio A, Canavese F, Charles YP (2011) Growth and adolescent idiopathic scoliosis: when and how much? J Pediatr Orthop 32(Suppl 1):28–36CrossRef
11.
go back to reference Doukas A, Petridis AK (2010) A case of aplasia of the posterior arch of the atlas mimicking fracture: review of the literature. Clin Anat 23:881–882PubMedCrossRef Doukas A, Petridis AK (2010) A case of aplasia of the posterior arch of the atlas mimicking fracture: review of the literature. Clin Anat 23:881–882PubMedCrossRef
12.
go back to reference Goldstein I, Makhoul IR, Weissman A, Drugan A (2005) Hemivertebra: prenatal diagnosis, incidence and characteristics. Fetal Diagn Ther 20:121–126PubMedCrossRef Goldstein I, Makhoul IR, Weissman A, Drugan A (2005) Hemivertebra: prenatal diagnosis, incidence and characteristics. Fetal Diagn Ther 20:121–126PubMedCrossRef
13.
go back to reference van der Hof MC, Nicolaides KH, Campbell J, Campbell S (1990) Evaluation of the lemon and banana signs in one hundred thirty fetuses with open spina bifida. Am J Obstet Gynecol 162:322–327PubMed van der Hof MC, Nicolaides KH, Campbell J, Campbell S (1990) Evaluation of the lemon and banana signs in one hundred thirty fetuses with open spina bifida. Am J Obstet Gynecol 162:322–327PubMed
14.
go back to reference Iffy L, Jakobovits A, Westlake W, Wingate MB, Caterini H, Kanofsky P, Menduke H (1975) Early intrauterine development: I. The rate of growth of Caucasian embryos and fetuses between the 6th and 20th weeks of gestation. Pediatrics 56:173–186PubMed Iffy L, Jakobovits A, Westlake W, Wingate MB, Caterini H, Kanofsky P, Menduke H (1975) Early intrauterine development: I. The rate of growth of Caucasian embryos and fetuses between the 6th and 20th weeks of gestation. Pediatrics 56:173–186PubMed
15.
go back to reference Jalanko T, Rintala R, Puisto V, Helenius I (2011) Hemivertebra resection for congenital scoliosis in young children: comparison of clinical, radiographic, and health-related quality of life outcomes between the anteroposterior and posterolateral approaches. Spine 36:41–49PubMed Jalanko T, Rintala R, Puisto V, Helenius I (2011) Hemivertebra resection for congenital scoliosis in young children: comparison of clinical, radiographic, and health-related quality of life outcomes between the anteroposterior and posterolateral approaches. Spine 36:41–49PubMed
16.
go back to reference Jin ZW, Song KJ, Lee NH, Nakamura T, Fujimiya M, Murakami G, Cho BH (2011) Contribution of the anterior longitudinal ligament to ossification and growth of the vertebral body: an immunohistochemical study using the human fetal lumbar vertebrae. Surg Radiol Anat 33:11–18PubMedCrossRef Jin ZW, Song KJ, Lee NH, Nakamura T, Fujimiya M, Murakami G, Cho BH (2011) Contribution of the anterior longitudinal ligament to ossification and growth of the vertebral body: an immunohistochemical study using the human fetal lumbar vertebrae. Surg Radiol Anat 33:11–18PubMedCrossRef
17.
go back to reference Kibii JM, Pan R, Tobias PV (2010) Morphometric variations of the 7th cervical vertebrae of Zulu, White, and colored South Africans. Clin Anat 23:399–406PubMedCrossRef Kibii JM, Pan R, Tobias PV (2010) Morphometric variations of the 7th cervical vertebrae of Zulu, White, and colored South Africans. Clin Anat 23:399–406PubMedCrossRef
18.
go back to reference Kumar A, Tubbs RS (2011) Spina bifida: a diagnostic dilemma in paleopathology. Clin Anat 24:19–33PubMedCrossRef Kumar A, Tubbs RS (2011) Spina bifida: a diagnostic dilemma in paleopathology. Clin Anat 24:19–33PubMedCrossRef
19.
go back to reference Kwan MK, Jeffry A, Chan CY, Saw LB (2012) A radiological evaluation of the morphometry and safety of S1, S2 and S2—ilium screws in the Asian population using three dimensional computed tomography scan: an analysis of 180 pelvis. Surg Radiol Anat 34:217–227PubMedCrossRef Kwan MK, Jeffry A, Chan CY, Saw LB (2012) A radiological evaluation of the morphometry and safety of S1, S2 and S2—ilium screws in the Asian population using three dimensional computed tomography scan: an analysis of 180 pelvis. Surg Radiol Anat 34:217–227PubMedCrossRef
20.
go back to reference Leug YL, Buton N (2005) Combined diastematomyelia and hemivertebra. A review of the management at a single centre. J Bone Joint Surg 87:1380–1384CrossRef Leug YL, Buton N (2005) Combined diastematomyelia and hemivertebra. A review of the management at a single centre. J Bone Joint Surg 87:1380–1384CrossRef
21.
go back to reference Matsumoto M, Okada E, Kaneko Y, Ichihara D, Watanabe K, Chiba K, Toyama Y, Fujiwara H, Momoshima S, Nishiwaki Y, Hashimoto T, Takahata T (2011) Wedging of vertebral bodies at the thoracolumbar junction in asymptomatic healthy subjects on magnetic resonance imaging. Surg Radiol Anat 33:223–228PubMedCrossRef Matsumoto M, Okada E, Kaneko Y, Ichihara D, Watanabe K, Chiba K, Toyama Y, Fujiwara H, Momoshima S, Nishiwaki Y, Hashimoto T, Takahata T (2011) Wedging of vertebral bodies at the thoracolumbar junction in asymptomatic healthy subjects on magnetic resonance imaging. Surg Radiol Anat 33:223–228PubMedCrossRef
22.
go back to reference Noback CR, Robertson GG (1951) Sequences of appearance of ossification centers in the human skeleton during the first five prenatal months. Am J Anat 89:1–28PubMedCrossRef Noback CR, Robertson GG (1951) Sequences of appearance of ossification centers in the human skeleton during the first five prenatal months. Am J Anat 89:1–28PubMedCrossRef
23.
go back to reference Patinharayil G, Han CW, Marthya A, Meethall KC, Surendran S, Rudrappa GH (2008) Butterfly vertebra: an uncommon congenital spinal anomaly. Spine 15(33):926–928CrossRef Patinharayil G, Han CW, Marthya A, Meethall KC, Surendran S, Rudrappa GH (2008) Butterfly vertebra: an uncommon congenital spinal anomaly. Spine 15(33):926–928CrossRef
24.
go back to reference Schild RL, Wallny T, Fimmers R, Hansmann M (2000) The size of the fetal thoracolumbar spine: a three-dimensional ultrasound study. Ultrasound Obstet Gynecol 16:468–472PubMedCrossRef Schild RL, Wallny T, Fimmers R, Hansmann M (2000) The size of the fetal thoracolumbar spine: a three-dimensional ultrasound study. Ultrasound Obstet Gynecol 16:468–472PubMedCrossRef
25.
go back to reference Szpinda M, Daroszewski M, Woźniak A, Szpinda A, Mila-Kierzenkowska C (2012) Tracheal dimensions in human fetuses: an anatomical, digital and statistical study. Surg Radiol Anat 34:317–323PubMedCrossRef Szpinda M, Daroszewski M, Woźniak A, Szpinda A, Mila-Kierzenkowska C (2012) Tracheal dimensions in human fetuses: an anatomical, digital and statistical study. Surg Radiol Anat 34:317–323PubMedCrossRef
27.
go back to reference Travan L, Saccheri P, Sabbadini G, Crivellato E (2011) Bilateral arcuate foramen associated with partial defect of the posterior arch of the atlas in a medieval skeleton: case report and review of the literature. Looking backward to go forward. Surg Radiol Anat 33:495–500PubMedCrossRef Travan L, Saccheri P, Sabbadini G, Crivellato E (2011) Bilateral arcuate foramen associated with partial defect of the posterior arch of the atlas in a medieval skeleton: case report and review of the literature. Looking backward to go forward. Surg Radiol Anat 33:495–500PubMedCrossRef
28.
go back to reference Tulsi RS (1971) Growth of the human vertebral column: an osteological study. Acta Anat 79:570–580PubMedCrossRef Tulsi RS (1971) Growth of the human vertebral column: an osteological study. Acta Anat 79:570–580PubMedCrossRef
29.
go back to reference Ulla M, Aiello H, Cobos MP, Orioli I, García-Mónaco R, Etchegaray A, Igarzábal ML, Otaño L (2011) Prenatal diagnosis of skeletal dysplasias: contribution of three-dimensional computed tomography. Therapy Fetal Diagn 29:238–247CrossRef Ulla M, Aiello H, Cobos MP, Orioli I, García-Mónaco R, Etchegaray A, Igarzábal ML, Otaño L (2011) Prenatal diagnosis of skeletal dysplasias: contribution of three-dimensional computed tomography. Therapy Fetal Diagn 29:238–247CrossRef
30.
go back to reference Varras M, Akrivis C (2010) Prenatal diagnosis of fetal hemivertebra at 20 weeks’ gestation with literature review. Int J Gen Med 3:197–201PubMedCrossRef Varras M, Akrivis C (2010) Prenatal diagnosis of fetal hemivertebra at 20 weeks’ gestation with literature review. Int J Gen Med 3:197–201PubMedCrossRef
31.
go back to reference Vignolo M, Ginocchio G, Parodi A, Torrisi C, Pistorio A, Venturini PL, Aicardi G, de Biasio P (2005) A fetal spine ossification: the gender and individual differences illustrated by ultrasonography. Ultrasound Med Biol 31:733–738PubMedCrossRef Vignolo M, Ginocchio G, Parodi A, Torrisi C, Pistorio A, Venturini PL, Aicardi G, de Biasio P (2005) A fetal spine ossification: the gender and individual differences illustrated by ultrasonography. Ultrasound Med Biol 31:733–738PubMedCrossRef
32.
go back to reference Wax JR, Watson WJ, Miller RC, Ingardia CJ, Pinette MG, Cartin A, Grimes CK, Blackstone J (2008) Prenatal sonographic diagnosis of hemivertebrae: associations and outcomes. J Ultrasound Med 27:1023–1027PubMed Wax JR, Watson WJ, Miller RC, Ingardia CJ, Pinette MG, Cartin A, Grimes CK, Blackstone J (2008) Prenatal sonographic diagnosis of hemivertebrae: associations and outcomes. J Ultrasound Med 27:1023–1027PubMed
33.
go back to reference Weisz B, Achiron R, Schindler A, Eisenberg VH, Lipitz S, Zalel Y (2004) Prenatal sonographic diagnosis of hemivertebra. J Ultrasound Med 23:853–857PubMed Weisz B, Achiron R, Schindler A, Eisenberg VH, Lipitz S, Zalel Y (2004) Prenatal sonographic diagnosis of hemivertebra. J Ultrasound Med 23:853–857PubMed
34.
go back to reference Whyte MP, Greenberg CR, Salman NJ, Bober MB, McAlister WH, Wenkert D, Van Sickle BJ, Simmons JH, Edgar TS, Bauer ML, Hamdan MA, Bishop N, Lutz RE, McGinn M, Craig S, Moore JN, Taylor JW, Cleveland RH, Chanley WR, Lim R, Thacher TD, Mayhew JE, Downs M, Millan JL, Skrinar AM, Crine P, Landy H (2012) Enzyme-replacement therapy in life-threatening hypophosphatasia. N Engl J Med 366:904–913PubMedCrossRef Whyte MP, Greenberg CR, Salman NJ, Bober MB, McAlister WH, Wenkert D, Van Sickle BJ, Simmons JH, Edgar TS, Bauer ML, Hamdan MA, Bishop N, Lutz RE, McGinn M, Craig S, Moore JN, Taylor JW, Cleveland RH, Chanley WR, Lim R, Thacher TD, Mayhew JE, Downs M, Millan JL, Skrinar AM, Crine P, Landy H (2012) Enzyme-replacement therapy in life-threatening hypophosphatasia. N Engl J Med 366:904–913PubMedCrossRef
Metadata
Title
New anatomical data on the growing C4 vertebra and its three ossification centers in human fetuses
Authors
Mariusz Baumgart
Michał Szpinda
Anna Szpinda
Publication date
01-04-2013
Publisher
Springer-Verlag
Published in
Surgical and Radiologic Anatomy / Issue 3/2013
Print ISSN: 0930-1038
Electronic ISSN: 1279-8517
DOI
https://doi.org/10.1007/s00276-012-1022-z

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