Introduction

Despite their rarity, a few congenital malformations, such as sternal clefts, affect the fetal sternum. The antenatal recognition of these anomalies necessitates the knowledge of the normal ultrasonographic aspects of the fetal sternum and of its physiological variants. The aim of this article is to give a description of the principal anatomical aspects of the sternum during pregnancy.

Embryology

The sternum is of mesodermal origin (6, 8). During the 6th week, it arises from paired longitudinal concentrations of mesenchymal tissue located on each side of the anterior chest wall and called “sternal bars” (5, 6, 7, 8, 14, 15). Afterwards, these sternal bars migrate towards the midline and fuse to form the sternal plate. This fusion begins at the cephalic end of the sternal bars and progresses in a cranio-caudal direction. It is complete by the 10th week (5, 6, 7, 8, 14, 15).
After maturation into cartilage, the sternum undergoes several transverse divisions into a series of six cartilaginous segments called “sternebrae” or “segments” (from the segment 1 to the segment 6). There is one segment for the manubrium, four for the body and one for the xiphoid process (1, 7).
The sternum ossifies gradually from cartilaginous precursors (14). The endochondral ossification centers are formed within each cartilaginous segment of the sternum and appear early during fetal life (7, 23). They appear in the manubrium and progress normally in a cranio-caudal sequence (1, 7, 8, 14, 16, 18). Within a cartilaginous center, there may be either one or two ossification centers, those with two centers reflecting their bilateral embryonic origin (23).
Union of adjacent sternebrae, initiated through a central osseous bridge, progresses through anterior, lateral, cephalocaudal, and posterior domains to achieve synostosis. Accessory and bifid centers of ossification within the same intercostal space coalesce prior to adjoining adjacent sternebrae (23).
The sternebrae do not always ossify to the same degree so there is a wide variability in the number and configuration of the ossification centers of the developing sternum (16). Furthermore, the ossification may be asynchronous (18). The failure of this physiologic epiphysiodesis of the sternal bars leads to congenital anomalies such as sternal clefts or sternal agenesis (5, 6, 8, 14).

Drawing 1: Human sternal embryology (green = sternal bars, blue = ribs, pink = clavicles).

Anatomy

The sternum is an elongated flattened structure forming the middle portion of the anterior chest wall. It is essentially cartilaginous during fetal life and become progressively ossified (1, 7). It consists of three parts named cranio-caudally: the manubrium, the body or gladiolus and the xiphoid process (1, 7, 18). In its natural position, the inclination of the sternum is oblique from above downward and forward and it is slightly convex in front and concave posteriorly (1).

a) THE MANUBRIUM. It has nearly quadrangular shape, broad and thick at its upper border and narrow at its junction with the body (1). It provides attachment on either side to the sternal origin of the pectoralis major, sternocleidomastoideus, sternohyoideus and sternothyroideus muscles (1). The superior border presents at its center the jugular or presternal notch. On either side of this notch is an oval articular surface for articulation with the sternal end of the both clavicles (1, 7). The inferior border articulates with the body (1). The lateral borders are each marked above by a depression for the first costal cartilage and below by a small articular surface which, with the similar surface on the upper angle of the body, forms a notch for the articulation of the costal cartilage of the second rib (1).

b) THE BODY or CORPUS STERNI or GLADIOLUS. It is much longer, narrower and thinner than the manubrium (1, 7). Its anterior surface is nearly flat and marked by the three transversal ridges that divided the body in four segments (segment 2 to segment 5). The superior border articulates with the manubrium whereas the inferior border is narrow and articulates with the xiphoid process via a common zone of hyaline cartilage (23). Each lateral border, at its superior angle, has a small facet for articulation with the second costal cartilage. Below, there are four depressions which receive the cartilage of the 3rd, 4th, 5th and 6th ribs. While the inferior angle has a small facet which, with the corresponding one of the xiphoid process, form a notch for the common cartilages of the 7th, 8th, 9th and 10th ribs. These articular depressions are separated by a series of curved inter-articular interval for attachment of intercostal muscles (1).

c) THE XIPHOID PROCESS or PROCESSUS XIPHOIDUS or ENSIFORM APPENDIX or XIPHOID APPENDIX. The xiphoid process is the smallest of the three pieces. It articulates above with the body and on the front of each superior angle presents a facet for part of the cartilage of the 7th, 8th, 9th and 10th ribs. Below by its pointed extremity, it gives attachment to the linea alba and, on the posterior surface, to the diaphragm (1). The xiphoid process varies much in form and size (1).

Drawing 2: Human sternal anatomy with ossification centers (green = manubrium, yellow = body, blue = xyphoid appendix). Clavicles are not represented but they have their insertion in the clavicular notches (CN) separated by the jugular notch (JN).

Ultrasonographic study of the fetal sternum

To simplify the analysis of the images, for each sagittal and coronal sections of this article, the fetal head is “located on the right of the image” and the fetal abdomen is “located on the left of the image”.

A) 1st trimester

As seen in the embryological chapter, the fetal sternal development is completed at 10 weeks. Thus the sternum can be studied during the 12th week examination. But during this period, sternal analysis is quite difficult because of the frequent flexion of the fetal head on the thorax and because of the thinness of the sternum compared with the thickness of the sonographic section. However, fetal sternum can be visualized as shown below.

Images 1, 2: Image 1: Sagittal section of the sternum at 13 weeks. The sternum appears as a slighly curved well delimited hypoechoic structure (arrows). Image 2: Coronal section obtained by transvaginal sonography. The sternum appears hypoechoic and its global shape can be recognized.

B) 2nd trimester and early 3rd trimester

In our experience, the 2nd trimester and early 3rd trimester (between 18 and 26 weeks) is the best period for sternal study because of absence or small number and size of the ossification centers. The sternum can be studied in three planes, but the most informative one seems to be the coronal plane. Because of its natural curve, the sternum length cannot be seen whole except of sagittal section. At this period the sternum is mainly cartilaginous. So it appears as an hypoechoic structure compared to the surrounding tissues. The global shape of the sternum can be analyzed but junctions between manubrium, body and xiphoid process cannot be distinguished.

The manubrium

The manubrium is the most difficult sternal part to study because of the shadow from the ossified clavicles and because of the frequent interposition of the upper part of the humerus on coronal section. The first ossification center is present at its level.

Images 3, 4: Image 3 - 17 weeks; near quadrangular manubrium with discreet ossification center. The manubrium is located between the anterior ends of both clavicles (#) and sternal body (*). This section can be helpful for the diagnosis of upper sternal clefts. Wide, upper sternal clefts are associated with increased distance between the medial clavicular ends. Image 4 - aspect of the normal manubrium at 20 weeks. Note the good visualization of the jugular notch (arrow).

Image 5: Manubrium at 22 weeks.

The body of the sternum

Images 6, 7: Image 6: 17 weeks - hypoechoic fetal sternal body without any ossification center. Note the convergence of the chondrocostal cartilages. Image 7: 17 weeks - in early second trimester, a very thin lightly echoic median line which probably correspond to the line of fusion of the two sternal bars can be seen.

Images 8, 9: Image 8: 21 weeks - sternal body with beginning of the ossification of the second sternal segment. Image 9: 22 weeks - body with presence of the ossification centers of the four body segments. Note the difference in ossification between the two images taken at about the same gestational age.

Image 10: 22 weeks - the same aspect as in the image 9 in another fetus.

These images of the body confirmed the great variability of fetal sternum ossification centers at a given gestational age.

The xyphoid

The xyphoid can be seen during the prenatal ultrasonographic examination. Its length, shape and curve appear to be very variable as shown below.

Images 11, 12: Image 11: 21 weeks - short xyphoid process. Image 12: 20 weeks - the xyphoid process appears longer in comparison with the image 11.

Images 13, 14: The images show a very long xyphoid process at 24 weeks of pregnancy.

Image 15: The image shows the sagittal scan of the the same fetus as in the images 13 and 14. Note the anterior curve of the long xiphoid process.

The ossification centers

As seen previously, ossification centers appear first in the manubrium and ossification progresses caudally. They are thought to appear at the midline of the sternum. Because of this appearance, when 2 adjacent centers are compared, the superior one is larger than the inferior one. However this ideal normal progression is not constant.

Image 16: Normal aspect of the ossification centers at 32 weeks. Note the regular decrease in size of the ossification centers between the segment one to the segment five.

• Asynchronism:

The development of ossification centers could be physiologically asynchronous. An ossification center is considered asynchronous if its ossification is either absent or decreased as compared with the adjacent centers.

Images 17, 18: 22 weeks - these images show ossification of the segments 1 and 3 with light ossification of the asynchronous segment 2.

• Alignment:

Ossification centers usually appears in the midline of the sternum, thus, they usually have a linear disposition. However, non alignment of the ossification centers is frequently seen without any pathological significance.

Images 19, 20: The image 19 shows a normal perfect alignment of the ossification centers at 28 weeks. The image 20 shows a physiological malalignment of the ossification centers at 27 weeks.

Images 21, 22: The image 21 shows a physiological malalignment of the ossification centers at 32 weeks. The image 22 shows a double ossification of the manubrium (arrows).

The sternal mobility

Images 23, 24: These images were taken at 23 weeks during an episode of fetal hiccough. Note the inward motion of the lower part and the outward motion of the upper part of the sternum.

The neighbouring structures

Images 25, 26: The image 25 shows the chondro-costal articulation at 23 weeks. The image 26 shows an axial section of the thorax at 22 weeks. Note the continuity between the rib (R), the costal cartilage (C) and the sternum with ossification center (arrows).

Images 27, 28: The image 27 shows a parasagittal section showing the rib cartilages just before the junction with the sternum. The image 28 shows the sternal body (*) with hypoechoic costal cartilages separated by slightly echoic intercostal muscles at 18 weeks of pregnancy.

Images 29, 30: The image 29 shows the manubrium in contact with the fetal thymus. The image 30 shows the internal thoracic artery and vein which are visible as thin echoic lines on each side of the sternum, just behind the costal cartilages. The image was taken at 22 weeks, but these structures can be seen as early as 17 weeks.

Images 31, 32: The image 31 shows the internal thoracic artery and vein which are visible as thin echoic lines on each side of the sternum, just behind the costal cartilages at 26 weeks. The image 32 shows the internal edges of the sternocleidomastoid muscle (arrows) at 21 weeks.

Images 33, 34: The image 33 shows the internal edges of the sternocleidomastoid muscle at 22 weeks. The image 34 shows the lower part of the sternum with the xyphoid appendix prolongated by the echoic linea alba (arrows) obtained at 18 weeks of pregnancy.

Images 35, 36: The image 35 the jugular notch of the manubrium. We can see the hypoechoic circle of the trachea. The image 36 shows a sagittal scan of the xyphoid attachment of the diaphragm at 32 weeks. This section could be helpful to determin the upper limit of some anterior abdominal wall defects or diaphragmatic hernias.

Sternal malformations or anomalies

Anomalies of the sternum can be isolated as a single malformation or to be in association with a variety of syndromes involving other organ systems (24).

Sternal clefts are rare anomalies. Superior clefts are more frequent than inferior ones and isolated central clefts are extremely rare (2, 8). They are due to failure of fusion of the sternal bar (6). This failure can be complete or incomplete but complete sternal clefts is the least likely form (6, 8, 9). Sternal cleft could be diagnosed prenatally but isolated sternal cleft is often diagnosed as asymptomatic at birth (6, 11).

Another typical anomaly is the presence of double ossification centers in the manubrium with a cranio-caudal arrangement instead of a side by side position of the ossification centers. This is present in trisomy 21, monosomy X and diastrophic dysplasia among other conditions (20, 21, 22).

Other anomalies of the sternum associated with Monosomy X include short sternum, decreased ratio of sternal body to manubrium bowing of the mesosternum, mild pectus excavatum also, and postnatally: premature fusion of the manubrio-sternal junction, premature fusion of the mesosternum (21). Short sternum is can also be seen in trisomy 18 or after isotretinoin exposure (13, 24).

Defects of the lower part of the sternum and deficiency of the anterior diaphragm characterized certain anterior abdominal wall defects such as incomplete forms of Cantrell’s pentalogy (3).

At last, sternal anomalies exist in PHACES syndrome (facial Hemangioma, posterior fossa anomaly, arterial anomalies, aortic coarctation, eyes anomalies and sternum malformations) and in numerous other syndromes (17).

References

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