Postnatal Maturation of the

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Dale R. Broome1 L. Anne Hayman1 Richard C. Herrick1 Richard M. Braverman1 Ronald B. J. Glass2 Linda M. Fahr1 Received July 24, 1997; accepted after revision September 29, 1997. L A.

1 Dale R. Broome1 L. Anne Hayman1 Richard C. Herrick1 Richard M. Braverman1 Ronald B. J. Glass2 Linda M. Fahr1 Received July 24, 1997; accepted after revision September 29, L A. Hayman receives a medical royalty payment from Smart ChartsLlc, Houston, TX. 1 Department of Radiology, Baylor College of Medicine, One Baylor Plaza, Houston, TX Address correspondence to 0. R. Broome. 2Department of Radiology, Mt Sinai Medical New York, NY AJR 1998;170: X/ American Roentgen Ray Society Center, Postnatal Maturation of the Sacrum and Coccyx: MR Imaging, Helical CT, and Conventional Radiography OBJECTIVE. The purpose of this paper is to provide a detailed radiologic description of the postnatal developmental anatomy of the sacrum and coccyx as revealed by MR imaging, helical CT, and conventional radiography. MATERIALS AND METHODS. One hundred ten imaging examinations of the sacrococcygeal spine were performed in patients who were newborn to 30 years old. Imaging included conventional radiography (n = 63), three-dimensional gradient-recalled echo MR imaging (n = 10), and helical CT with sagittal and angled coronal reformations (n = 37). A detailed analysis was performed of the ossification and fusion ofthe primary and secondary ossification centers. RESULTS.The sacrum and coccyx were noted to develop from 58 to 60 sacral ossification centers and eight coccygeal centers, respectively. These centers were noted to ossify and fuse in an organized temporal pattern from the fetal period to the age of 30. CONCLUSION.The sacrum and coccyx are formed by a complex process that fuses primary and secondary ossification centers. Because the maturation process can be asymmetric, an understanding of this process may prove useful for distinguishing physeal plates from fracture lines. T he osseous maturation of the sacrum and coccyx is a complex developmental process that spans a period from the end of the first trimester of fetal life to mid adult life. The sacrum is formed by the fusion of ossification centers and the coccyx is formed by as many as eight ossification centers. The primary and secondary ossification centers are summarized in Table 1 and shown in Figure 1. The development of these two segments of human spine has been only partially described by anatomists who studied a limited number of cadavers [ 1-3]. Few, limited radiographic studies of this subject have been performed [4-7], but to our knowledge no one has used multiplanar imaging techniques such as MR imaging and helical CT. The purpose of this paper is to provide a detailed radiologic description of the anatomy of the sacrum and coccyx using MR imaging, helical CT, and conventional radiography. Materials and Methods One hundred ten imaging examinations of the normal sacrococcygeal spine were obtained for 105 patients (53 males, 52 females) who were newborn to 30 years old. Twenty-six patients were newborn to 2 years old, 36 were 3-9 years old, 30 were years old. and 18 were years old. No attempt was made to study the racial cornposition of the population because the sample size was too small. Thirty-seven examinations were performed with helical CT. 10 with MR imaging. and 63 with conventional radiography. Standard anteroposterior and lateral radiographs were obtained of the sacrum and coccyx. The helical CT examinations were performed with a 9800 helical scanner (General Electric Medical Systems, Milwaukee, WI) using collimation of 5-7 mm, pitch of 1:1, voltage of 120 kv. and current of ma. Bone window images were reviewed in the axial projection. The sagittal and angled coronal images were reformatted using an Advantage Windows workstation (General Electric Medical Systems) with a slice thickness of 3 mm and 3- to 4-mm increments and bone window settings. The coronal images were obtained along the plane of the body of the sacrum images approximately 20-30#{176} from the true coronal plane. MR imaging consisted of a three-dimensional gradient-recalled echo sequence of the sacrum and coccyx using a I.5-1 Signa unit (General Electric Medical Systems) with a phased array spine surface coil (35-40/15 [TR range/tel; flip AJR:170, April

Broome et al. A angle, 30#{176}: matrix, 256 x 128: field of view, 16-20 cm; effective slice thickness, 0.7-1.7 mm).

One observer analyzed in detail all sacrococcygeal images to assess ossification of primary and secondary growth centers and fusion of the adjacent physeal plates.

$the data were analyzed to establish normal ranges for these two findings. The range was defined by the age of the Ala Axial Sections :.r? disc,_ &,-.. M.disI crest ste ---. dl t S (Does#{149}t).$ t - (Letersi) sees. Csrise ci I z(j2 c.n.,i St ts5i ce:::.:7 I ) Fig. 1.-Color-coded drawings of mature sacrum and coccyx.

t - (Letersi) sees. Csrise ci I z(j2 c.n.,i St ts5i ce:::.:7 I ) Fig. 1.-Color-coded drawings of mature sacrum and coccyx.

2 Broome et al. A angle, 30#{176}: matrix, 256 x 128: field of view, cm; effective slice thickness, mm). Axial and reformatted sagittal and angled coronal images were filmed at 3- to 4-nim increments. One observer analyzed in detail all sacrococcygeal images to assess ossification of primary and secondary growth centers and fusion of the adjacent physeal plates. The growth centers were considered ossified if they were calcified on helical CT scans or radiographs or low in signal intensity relative to the cartilage on the MR images. The physeal plates and sacral discs were considered fused if bridging cortical bone extended across the physeal plate. Subsequently. the data were analyzed to establish normal ranges for these two findings. The range was defined by the age of the Ala Axial Sections :.r? disc,_ &,-.. M.disI crest ste ---. dl t S (Does#{149}t). t - (Letersi) sees. Csrise ci I z(j2 c.n.,i St ts5i ce:::.:7 I ) Fig. 1.-Color-coded drawings of mature sacrum and coccyx. Orange = centrum, pink = costal processes, yellow = neural arches, blue = endplate ring epiphyses, light purple = mamillary epiphyses, light green = transverse epiphyses, dark purple = spinous epiphyses, brown = inferior and superior articular processes, dark green = anterior and posterior costal epiphyses, red = growth plates, gray = intersegmental fusion lines. (Reprinted with permission from Smart Charts, Houston, TX) A, Dorsal (posterior) view shows primary and numerous small secondary ossification centers, including transverse process, posterior costal, spinous process, and mamillary process epiphyses. B, Ventral (anterior) view shows additional secondary ossification centers, including endplate ring and anterior costal epiphyses. C, Axial drawings traced from CT images of 44-year-old woman show primary and secondary ossification centers and growth plates. Note that levels l-vl indicate position of representative axial sections. c7 I C 1062 AJR:17O, April 1998

Postnatal Maturation of the Sacrum and Coccyx youngcst patient to show the finding and the age of the oldest

Results The typical sacral vertebrae were noted to develop from five primary ossification centers including the

As the sacrum matures, multiple small apophyses ossify and subsequently fuse to various surfaces of the primary

A and B, At 51 and 52 vertebral levels, neural arches have fused to costal processes (CPs) and centrum.

C, 55 vertebral level shows that neural arches and cornua have ossified and fused to centrum.

Although this terminology has persisted [ 1. 8]. many of these centers would be more properly termed apophyses.

-Axial CT images of healthy 2-month-old boy. A, Si vertebral level shows unfused neural arches and centrum.

Note that Si costal processes (CPs) are located inferior to neural arches and centrum offirst coccygeal vertebra.

-Axial CT images of healthy 13-year-old boy.

3 Postnatal Maturation of the Sacrum and Coccyx youngcst patient to show the finding and the age of the oldest patient who did not show the finding. Results The typical sacral vertebrae were noted to develop from five primary ossification centers including the centrum. two posterior neural arches, and two costal processes (CPs) lateral to the centrum. As the sacrum matures, multiple small apophyses ossify and subsequently fuse to various surfaces of the primary centers. Early anatomists referred to Fig. 3.-Axial CT images of healthy 3-year-old girl. A and B, At 51 and 52 vertebral levels, neural arches have fused to costal processes (CPs) and centrum. CPs have not fused to centrum. C, 55 vertebral level shows that neural arches and cornua have ossified and fused to centrum. TPE = transverse process epiphysis. all of these secondary ossification centers as epiphyses [2J. Although this terminology has persisted [ 1. 8]. many of these centers would be more properly termed apophyses. Apophyses represent secondary ossification centers at tendinous or ligamentous insertion Fig. 2.-Axial CT images of healthy 2-month-old boy. A, Si vertebral level shows unfused neural arches and centrum. B, 52 vertebral level shows unfused 52 neural arches and centrum. Note that Si costal processes (CPs) are located inferior to neural arches and centrum offirst coccygeal vertebra. C, S5 vertebral level shows only centrum. CPs are absent at this level. Neural arches are not ossified. Fig. 4.-Axial CT images of healthy 13-year-old boy. A, 51 vertebral level shows asymmetric transverse process epiphyses (TPE 1) along superolateral surface of costal processes (CPs). B, 52 vertebral level shows asymmetric anterior and posterior costal epiphyses (ACE 1, PCE 1) along lateral surfaces of CR 52 spinous process has formed by fusion of neural arches and spinous process epiphysis (SPE 2). C, 55 vertebral level shows transverse process epiphyses (TPE 5) have elongated and fused to centrum. Cornua, or neural arches, have fused to centrum. AJR:17O, April

axial images (Figs. 2 and 3). This finding must be understood to sites. In this paper. we use epiphyses and apophyses interchangeably.

4 Broome et al. A final observation that we made in comparing sagittal and axial images was that the posterior arches of the sacral vertebrae and the first coccygeal vertebra project superior to the centra and CP on axial images (Figs. 2 and 3). This finding must be understood to sites. In this paper. we use epiphyses and apophyses interchangeably. Figure 1 shows color-coded diagrams of the primary and secondary ossification centers of the sacrum and coccyx. The axial sections (Fig. IC) were traced from a helical CT scan of a mature sacrum and coccyx in a 44- year-old patient. Representative axial helical CT scans of the sacrum at the levels of 51, 52, and S5 from three different age groups showed the progressive appearance and fusion of the ossification center (Figs. 2-4). The diagrams are figurative and the apophyses are not drawn to scale to show these ossification centers and physeal plates, which are often small. Table 2 summarizes the age of fusion of the physeal plates between the primary ossification centers. Table 3 summarizes the age of appearance and fusion of most of the secondary ossification centers. Table 4 gives the ages at which intersegmental fusion between the vertebral bodies and between the CPs occurs. Each table also gives the expected ages of appearance and fusion of these centers as found in the literature [1-8], which were frequently generalized and not specific for the individual sacral and coccygeal levels. Discussion Fetal Development The sacrum typically is composed of five vertebrae but may be made up of six when the L5 has been sacralized. Rarely S I can fail to fuse to the sacrum and thus result in four sacral vertebrae. Each level has five primary ossification centers of the sacrum including a centrum, two posterior neural arches, and two CPs. except at the 55 level. where the CPs are absent (Fig. 5). According to the anatomic literature [ and one radiographic study of fetuses [5], the sacral centra ossify in a caudal direction with centra ossifying between 10 and 12 weeks gestation and 54 and 55 ossifying between 5 and 8 months gestation. The posterior neural arches also ossify in a caudal direction, but previous studies disagree on the age of ossification: weeks gestation [11 and weeks gestation [21. The CPs are the last of the primary ossification centers to ossify (6-8 months gestation) [ I. 2]. In our study. all of the primary ossification centers had ossified by birth with two exceptions: a premature infant without an ossified 54 costal process and a 5-year-old without an ossified 55 posterior neural arch. Postnatal Maturation After birth, the primary ossification centers of the sacrum have been described by anatomists to undergo fusion by approximately 7 years old [1, 21. Fusion of the primary centers was difficult to determine with radiography because of the overlap of the primary centers in the anteroposterior and lateral projections. Helical CT and MR imaging allowed more precise determination of interosseous fusion, which generally occurred between 3 months and 7 years old (Table 2, Figs. 2-4). Our second observation was that fusion of the primary and secondary centers was often asymmetric from side to side. This asymmetry can be seen in costal epiphyses (Fig. 4B). The potential significance of this finding is that an asymmetric unfused physeal plate could be confused with a fracture line. The growth plates can be distinguished from fracture lines by their characteristic location and the sclerotic surface of the ossification centers. The fusion of the posterior neural arch of 54 also varied and was noted in only four patients. properly number the sacral vertebrae. Sacml Epiphyseal ondapophyseal Ossification Centers The sacral epiphyseal ossification centers are numerous and are responsible for the final fusion and modeling of the surface contours of the sacrum. These centers are small and difficult to see on plain radiographs of the spine. Helical CT and MR imaging were essential to visualize most of these epiphyses. According to Gray (31, lateral surface epiphyses develop along the sacroiliac joint surfaces after puberty. Fawcett [2] later determined that the lateral surface epiphyses represent a coalescence of the anterior costal epiphyses (ACEs) and posterior costal epiphyses between the 51 and 53 levels and the two lowest ACEs and fourth and fifth transverse process epiphyses (TPEs) at the 54 and S5 levels. The costal epiphyses to our knowledge have only been visualized and described in a few radiographic and helical CT studies of a limited number of adolescents [6. 8). Four ACEs have been described, each originating between the sacral segments. The ACEs grow to form a thin ribbon of bone along the anterior sacroiliac joint surface of the CP (Fig. 4B). The posterior costal epiphyses are likewise intervertebral but have been identified only at S 1-52 and S2-S3. The posterior costal epiphyses form a thin ribbon of bone along the mid posterior sacroiliac joint surface of the sacrum (Fig. 4B). Although the third ACE has been described in the literature [2], we were never able to discretely identify it with helical CT, MR imaging. or radiography. The h)urth ACE was seen in only three patients, Contrary to the literature, we found that the costal epiphyses could be seen much earher than the reported age of I 2-I 8 years old [6, 8]-as early as 3-4 years old by helical CT and 10 months old by MR imaging (Fig. 6B). The costal epiphyses were noted to fuse to the CPs between the ages of I 8 and 25. in concordance with the literature [8]. The four pairs of TPEs were first described by Fawcett 21 in his autopsy series. but to our knowledge these epiphyses have not been described in the radiologic literature, The first TPE was noted along the superolateral aspect of the S I costal process (Fig, 4A). The remaining epiphyses were interver AJR:170, April 1998

Postnatal Maturation of the Sacrum and Coccyx ;*cral Epiphyssal Osslicadon Cents.s as Revsslsd by Hdkal CT and MR lm.ing According to Ass of Patients and ICorrelatsd with the Literatur. tebral.

5 Postnatal Maturation of the Sacrum and Coccyx ;*cral Epiphyssal Osslicadon Cents.s as Revsslsd by Hdkal CT and MR lm.ing According to Ass of Patients and ICorrelatsd with the Literatur. tebral. extending superiorly from the posterolateral aspect of the 53 and 54 CPs and the 55 centrum. These epiphyses are located just lateral to the dorsal neural foramina. Contrary to Fawcett s finding that the second epiphysis fails to develop, we were able to identify these epiphyses lateral to the second ntersegmental Fusion ofthe iacrum as Shown by Helical T and Radiography dorsal foramina in two adolescents. The first three TPEs are typically small: the fourth and fifth are larger and extend superiorly to fuse with the third and fourth ACEs, respectively, to form the lateral angles of the lower sacrum (Figs. 1A and 1B). Along the dorsal surface of each side of the sacrum, the TPEs form a column of tuberosities called the lateral sacral crests. The TPEs were seen on helical CT as early as 2 years old and on MR imaging at 10 months old. The TPEs typically fuse to their respective CP (first four TPEs) or centrum (fifth TPE) by I 4-I 8 years old. Several additional epiphyses have been described and were noted in our study. A pair of mamillary process epiphyses has been described by anatomists to develop along the posterolateral base of each S I superior articular facet near the L5-S I facet joints [ 1, 21. We noted these epiphyses in 14 patients; they fusion to S I occurred between the ages of 1 1 and 1 8. Finally, three spinous process epiphyses were noted to develop over the fused posterior neural arches of S I -53 between the ages of 5 and 2 1. The three spinous process epiphyses later fuse to form the median sacral crest. Although the posterior arches of 54 may fuse, in general the 54 and 55 posterior neural arches remain unfused and are often referred to as sacral cornua and the gap between them as the sacral hiatus. The intermediate sacral crests along the dorsal sacrum are formed by fused superior and inferior articular processes located just medial to the dorsal foramina. At other spinal levels (cervical. thoracic. and lumbar), the superior and inferior articular processes have separate epiphyses (3]. However. the articular process epiphyses have not to our knowledge been described in the anatomic literature, nor could were best seen with helical CT. They were seen as early as 16 months old with MR im- we identify distinct epiphyses in our study. Five pairs of vertebral endplate ring epiph- aging and 4 years old with helical CT. and yses develop along the superior and inferior AJR:170, April

$Broome et al. Costal Process Costal Process c:itjtth \ Centrum4 2 Neural Arch ral Arch Fig. 5.-Drawing of fetal sacral vertebra showing primary ossification centers and physeal plates.$ They had been described to first appear at puberty, but we found that they may be seen between the ages of 4 and 21 on radiography and as early as the age of 10 months on MR imaging.

They had been described to first appear at puberty, but we found that they may be seen between the ages of 4 and 21 on radiography and as early as the age of 10 months on MR imaging.

6 Broome et al. Costal Process Costal Process c:itjtth \ Centrum4 2 Neural Arch ral Arch Fig. 5.-Drawing of fetal sacral vertebra showing primary ossification centers and physeal plates. surfaces of each sacral vertebra. They had been described to first appear at puberty, but we found that they may be seen between the ages of 4 and 21 on radiography and as early as the age of 10 months on MR imaging. The endplate ring epiphyses first appear at the and levels and lastly at the S 1 level. The endplate ring epiphyses appear to fuse with the centra just before fusion of rudimentary sacral discs. With the use of reformatted helical CT and conventional radiography, we were able to determine the time at and manner in which intersegmental fusion occurs between adjacent sacral segments. The rudimentary intervertebral discs have been described to fuse in a cephalad direction between the ages of 18 and 25 years [2]. This age range was confirmed at S 1-52 and 52-53, but we found the lower two sacral rudimentary discs typically fuse earlier, before the age of 15. Fusion between the coccygeal segments and 55 was highly variable, occurring between the ages of 15 and 28. The timing of intersegmental fusion of the lateral elements (CPs and transverse processes) of the sacrum has not been described to our knowledge. Fusion of the lateral elements occurred over a broad age range but usually was completed by the age of 18, except between 55 and the first coccygeal vertebra, at which fusion may occur as late as the age of 27. Fig. 6.-Three-dimensional gradient-recalled echo T2*weighted MR images of sacrum and coccyx in 16-monthold healthy boy. A, Sagittal helical CT reformation shows early appearance of endplate epiphyses and unfused rudimentary discs. B, Angled coronal helical CT reformation shows developing transverse process epiphyses (TPE) and first antenor costal epiphysis (ACE). The coccyx is formed by a maximum of four segments, but the actual number of segments in the fully mature coccyx varies. One study found the following percentage distribution in a group of 120 volunteers: one segment, 7%; two segments, 54%; three segments, 34%; and four segments, 5% [7]. The development of the coccygeal segments is simple. The second, third, and fourth coccygeal vertebrae are formed only by centra, which ossify in a caudal direction between the ages of 16 months and 18 years. The first coccygeal vertebra develops in a manner similar to 55. The centrum of 51 ossifies between birth and the age of 6, and the neural arches appear between birth and the age of 15. The centers of the first coccygeal vertebra fuse when a person is between 6 and 30 years old. The cornua and transverse processes of the first coccygeal vertebra are rudimentary in size compared with 55. Both of these processes project superior to the centrum of the first coccygeal vertebra to articulate with the fifth TPE. In conclusion, the sacrum is formed by a complex process of fusion of primary and secondary ossification centers, which is not fully complete until the age of 30. The coccyx is formed by as many as eight ossification centers; however, the number of coccygeal segments that develop ranges from one to four. The maturation of the sacrum and coccyx may be asymmetric from side to 1 E if side in terms of growth plate fusion and appearance of epiphyseal centers. Caution should be exercised when interpreting imaging examinations of the sacrum and coccyx not to misinterpret an unfused growth plate with a fracture. The epiphyseal centers were often detected earlier with gradient-recalled echo MR imaging than with helical CT or conventional References radiography. I. Gray H. Osteology. In: Williams PL, Warwick R, Dyson M. Bannister LH, eds. Gray : a?wtotfl 37th ed. NewYork: Churchill Livingstone, 1989: Fawcett E. On completion of the ossification of the human sacrum.anatanz 1907:30: Gray H. Osteology: the costal cartilages. In: Goss CM. ed. Anatomy of the hwnan body, 28th ed. Philadelphia: Lea & Febiger, 1966: Flecker H. Time of appearance and fusion of ossitication centers as observed by roentgenographic methods. AiR 1942:47: Bagnall KM. Harris PE Jones PRM. A radiographic study of the human fetal spine. 2. The Sequence of development of ossification centres in the vertebral column. J A,iat 1977:124: Cleaves EN. Adolescent sacroiliac joints: their normal development and their appearance in epiphysitis. AiR 1937:38: Postacchini F, Massobrio M. Idiopathic coccygodynia: analysis of fifty-one operative cases and a radiographic study of the normal coccyx. J Botie JOi1ItSUrgAflI 1983:65-A:l I 16-I Gotz W, Funke M. Fischer G. Grabbe E, Herken R. Epiphysial ossification centres in iliosacral joints: anatomy and computed tomography. Surg RadiolAnat 1993; 15: AJR:170, April 1998

Axial Skeleton: Vertebrae and Thorax

Axial Skeleton: Vertebrae and Thorax Function of the vertebral column (spine or backbone): 1) 2) 3) Composition of Vertebral column The vertebral column is formed by 33 individual vertebrae (some of which