Anatomical variations of the sternum: sternal foramen and variant xiphoid morphology in dried adult human sternum in Ethiopia

Embryology

The sternum develops from mesenchymal condensation that forms paired sternal bars that were originally located on each side of the midline. Immediately after the attachment of the cranial ribs, these paired sternal bars begin to chondrify, migrate to the midline and fuse in a craniocaudal fashion. After chondrification, ossification centers begin to appear from the fifth month to early childhood in craniocaudal succession. These ossification centers in the body of the sternum develop into four transverse segments known as the mesosternum. The ossification centers for the mesosternal segments vary considerably. In general, the two proximal mesosternal segments have single centers, whereas the third and fourth segments have paired centers. Beginning in the third to the fourth year of life, the mesosternal segments fuse caudocranially and are typically completed in early adulthood.^19,20 During childhood, single or paired ossification centers appear in the xiphoid process.⁴ Because of the presence of paired ossification centers in the lower portion of the sternal bone (mainly the lower mesosternal segments and the xiphoid process), the lower parts are the most variable portion of the sternal bone. Occasionally, the fusion of the paired ossification centers fails across their midline, resulting in a sternal foramen.¹⁹ There may be an incomplete fusion of the lower end of the sternum, resulting in a trifurcated or bifurcated xiphoid process.⁵

Epidemiology and topology

The incidence of SF varies in different studies from different populations and reported incidence data on SF from different populations ranging from 3.1 to 18.3%.^{1,2,4,5,7–18} Data from the literature on the incidence of SF are summarized in Table 1. The findings of the current study reveal that the incidence of SF in the Ethiopian population is 19.1%. This is inconsistent with many reported studies from American and European populations.^8–10,14,15 Previous studies in Brazil, Greece, and East Africa documented a higher incidence. which is in agreement, although slightly lower than our finding.^1,4,5,7,11 The variation in the reported incidence of SF could be due to geographic ethnic, racial, and genetic differences. This finding indicates that SF is a common congenital variation in Ethiopia and highlights the need for strict precautionary measures during sternal procedures in this study population. In addition, such incidental findings during radiologic and autopsy procedures should be properly evaluated to avoid misdiagnosis and misinterpretation of such findings as traumatic or pathological conditions.^1,2,4,5

Consistent with previous studies, significant differences were observed in which sternal foramina were more common in men than in women.^3,6 In the current study, no foramen was observed in the manubrium or upper mesosternal segments proximal to the level of the fourth CCJ. The most common site of SF was at the level of the fifth CCJ, accounting for more than half of the specimens with SF. This is followed by the fourth CCJ, sixth CCJ and xiphoid process, where SF is observed in 3 specimens at each site. Double sternal foramen was observed in a single male specimen on the sternal body and xiphoid process. This is consistent with a study from Kenya in which SFs were predominantly observed in the lower sternal segments, but differed from studies from Turkey and Greece that revealed more SFs in the xiphoid process than in the lower mesosternal segments.^4,5,10 This finding emphasizes the necessity of avoiding or adopting extreme caution during sternal puncture in the lower part of the sternum.

Clinical, radiological and forensic significance

SFs are usually asymptomatic and frequently detected incidentally on radiological images, surgical procedures, postmortem examinations and anatomy teaching specimens.^1,2,4,5,10 SF is a common variation that has been ironically referred to as “a finding of no clinical significance”.^2,21 Due to this, it is neglected in medical education, and only a few clinicians and acupuncturists are aware of SF.^21,22 The proximity of SF to vital adjacent thoracic structures constitutes a fundamental parameter with which clinicians and acupuncturists should be familiar. The iliac crest is the preferred site for bone marrow aspiration; however, extraction from the sternum becomes inevitable in certain circumstances, such as dry taps from the iliac crest or a history of pelvic radiotherapy.⁶ On the other hand, the practice of acupuncture is considered inherently safe, but serious complications can sometimes occur.²

In the scientific literature, 14 cases of cardiac and pericardial injuries have been reported during sternal puncture for bone marrow extraction or acupuncture in the lower sternal segment, of which 8 were fatal. A lack of awareness of the sternal foramen was the root cause of all fatal cases.² Therefore, during sternal interventions, avoidance of needle insertion in the lower thirds of the sternum and evaluation of previous radiographic scans or performing a preprocedural radiographic scan to rule out an SF are recommended.

Halvorsen et al. are to be commended for emphasizing the clinical significance of SF and for stressing the need for awaring medical students and clinicians during anatomy lessons, as well as on demonstrations of sternal puncture techniques.^21,22 In terms of acupuncture, the fourth and fifth CCJ levels correspond to commonly used acupuncture points and thus can pose great hazards when inserting acupuncture needles in persons with SF. The current study underpins the necessity for extra caution and avoidance of needle vertical insertion in the lower part of the sternum.^2,6 Therefore, an acupuncturist must use a superficial oblique insertion technique to prevent injury to thoracic organs in the study population.

Radiological evaluations can misdiagnose SF as lytic lesions or trauma. Therefore, it is vital for radiologists to be aware of this common variation and its radiographic characteristics to prevent misdiagnosis and subsequent mistreatment. When in doubt, radiologists should use computed tomography or magnetic resonance imaging, which best exposes the anatomical characteristics to enable discrimination, to differentiate SF from traumatic or osteolytic lesions of the sternum.^2,3,6

Furthermore, although SF is classically designated as a round or oval defect with a smooth margin, a study in Greece reported a single case of SF with an irregular margin and abnormal shape among five dried sternums with SF.³ In our study, four (22.2%) SFs with irregular margins and abnormal shapes were observed among eighteen dried sternums with SF. Such features can considerably complicate the radiological differentiation of SF and osteolytic lesions due to their remarkable similarity. Therefore, radiologists should be aware of SF even with irregular margins and abnormal shapes. The presence of such lesions must be analyzed with caution, and SF must be considered in the differential diagnosis.

In this study, an extremely interesting case of a sternal foramen with a beveled margin was observed. To my knowledge, this is the first description of a sternal foramen with a beveled margin. However, in this case, the observed beveling is in complete contrast to the classical feature of a sternal foramen. This characteristic, if present, can considerably complicate forensic interpretation. In medicolegal postmortem examination of skeletonized human remains, SF can be misinterpreted as a projectile entry wound or other penetrating injury or even osteolytic lesion from cancer or infection.^2,3,6 If forensic experts and anthropologists are unaware of such anatomic variations, it may result in misclassification of the manner and cause of death.³ SF is a midline defect, usually on the lower part of the sternum, with a round, oval or irregular shape, covered with cortical bone, and sometimes with a beveled margin.

Additionally, if such variations are routinely documented in the medical record whenever incidentally detected during the radiologic assessment, they can contribute to preprocedural evaluation before invasive sternal procedures. Furthermore, documentation of sternal bone variation is a simple and important potential source of data in the identification process of skeletonized human remains. However, there have been reports of perplexing similarities among members of the same family, highlighting the need for caution in interpretation.⁴ Therefore, awareness of SF, together with routine documentation of such variations in antemortem medical and radiological records of individuals, can aid in accurate identification and investigation of the manner and cause of death.

Xiphoid morphology

The term xiphoid process is derived from the Greek word “xiphos”, which means a straight sword that corresponds to the pointed end of the sternum. However, the xiphoid process can be absent, broad, bifid, trifurcated, duplicated or deflected. Variant xiphoid morphologies, such as bifid or trifurcated xiphoid processes, are caused by incomplete fusion of the ossification centers.^2,5 In the present study, bifid xiphoid processes occurred in 15.6% of cases, which is comparable to a study from Kenya.⁵ In addition, trifurcated xiphoid processes were observed in a single (1.3%) specimen. Such variations could be misinterpreted as an epigastric mass, fracture, or traumatic fissure.^1,5 With increasing traffic-related injuries, clinicians should be aware of xiphoid variations to avoid misdiagnosis as a fracture or traumatic fissure. This necessitates special vigilance when assessing anterior chest wall injury, and it may therefore be considered a differential diagnosis. Furthermore, routine documentation of such variations, whenever detected incidentally, in antemortem medical records of individuals can aid in the identification of skeletonized human remains.