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Bulbus cordis

The bulbus cordis is a transient segment of the primitive heart tube in vertebrate embryos, located between the truncus arteriosus and the primitive ventricle, that plays a critical role in early cardiac morphogenesis by contributing to the formation of ventricular structures and outflow tracts.^[1]^[2]^[3] During heart development, the bulbus cordis emerges as part of the straight heart tube around days 19–22 of gestation, undergoing rapid elongation that outpaces other regions and initiates the bulboventricular loop.^[1]^[4]^[3] This looping occurs between days 22–28, with the bulbus cordis shifting ventrally, caudally, and to the right, establishing the S-shaped configuration of the heart and aligning the future great vessels.^[2]^[3] The structure comprises proximal, middle, and distal portions: the proximal bulbus cordis develops into the trabeculated portion of the right ventricle, while the middle (conus cordis) and distal regions contribute to the smooth-walled conus arteriosus of the right ventricle and the aortic vestibule of the left ventricle, respectively.^[1]^[5]^[4] Further differentiation involves the ingrowth of neural crest-derived ridges in the fourth to seventh weeks, which spiral and fuse to form the aorticopulmonary septum, partitioning the conotruncal region (distal bulbus cordis and truncus arteriosus) into the ascending aorta and pulmonary trunk.^[4]^[5] Disruptions in bulbus cordis development can lead to congenital anomalies, such as persistent truncus arteriosus or tetralogy of Fallot, underscoring its importance in septation and outflow tract alignment.^[1]^[3] By the end of the seventh week, the bulbus cordis is fully incorporated into the mature ventricular myocardium, with no distinct remnant in the adult heart.^[4]^[2]

Anatomy

Structure

The bulbus cordis constitutes the middle segment of the primitive heart tube in the early embryo, positioned between the primitive ventricle caudally and the truncus arteriosus cranially.^[6] This segment forms part of the straight heart tube that emerges around day 22 of development, prior to looping.^[7] Externally, the bulbus cordis appears as a cylindrical, thick-walled structure enveloped by a myocardial layer that provides contractile support, with an inner endocardial lining separated by cardiac jelly.^[8] The myocardial wall exhibits varying thickness, thicker in the lower portion (approximately 13 μm) compared to the upper (about 6 μm) in early stages, contributing to its robust appearance relative to adjacent segments.^[8] Internally, the lumen features a smooth endocardial surface initially, housing a narrow endothelial blood tube surrounded by a delicate reticulum that transitions to fibrous tissue near the truncus arteriosus.^[8] As development progresses, endocardial cushions begin to form within this segment, initiating the process of septation, though these ridges are minimal at the outset.^[7] In human embryos at Carnegie stages 12–14, corresponding to approximately 28–32 days post-fertilization, the bulbus cordis aligns with the overall elongation of the primitive heart tube during this period.^[9]

Location and relations

In the straight heart tube formed around day 22 of human embryonic development, the bulbus cordis occupies a position cranial to the primitive ventricle and caudal to the truncus arteriosus, forming the distal portion of the ventricular region within the overall craniocaudal alignment of the heart tube that extends from the sinus venosus caudally to the truncus arteriosus cranially.^[1]^[2]^[10] This segment lies within the ventral midline of the embryo, suspended in the pericardial cavity, and is separated from the primitive ventricle by the bulbo-ventricular groove, also known as the primary interventricular foramen.^[1]^[4]^[10] The bulbus cordis maintains close anatomical relations with surrounding structures, including its direct continuity with the primitive ventricle caudally via the interconnecting foramen and its cranial extension into the truncus arteriosus, which links to the aortic sac.^[1]^[4] Laterally and dorsally, it is bordered by the developing endocardial cushions and the splanchnic mesoderm, while the entire heart tube, including the bulbus cordis, is enveloped by the pericardial sac.^[2]^[4] During the early stages of cardiac looping between days 23 and 28, the bulbus cordis undergoes positional shifts, migrating ventrally, caudally, and to the right relative to the primitive ventricle, which moves dorsally, cranially, and to the left, resulting in the formation of the bulbo-ventricular loop.^[1]^[2]^[10] This differential movement repositions the bulbus cordis more anteriorly and rightward within the looping S-shaped heart tube, enhancing its alignment with emerging vascular structures.^[2]^[4] Vascularly, the bulbus cordis connects cranially to the truncus arteriosus, which distributes blood to the aortic sac and subsequently to the pharyngeal aortic arches, facilitating early embryonic circulation.^[1]^[4] This outflow pathway positions the bulbus cordis as a critical conduit between the ventricular pumping region and the systemic vascular network during the initial heart tube phase.^[10]

Embryonic development

Formation of the heart tube

The formation of the heart tube begins during the third week of human embryonic development, specifically around days 18-19, when precursor cells from the lateral plate mesoderm, particularly the splanchnic layer adjacent to the endoderm, aggregate in the cardiogenic region anterior to the prechordal plate.^[11] These mesodermal cells differentiate into endothelial strands known as angioblastic cords, which canalize to form paired endocardial tubes enveloped by myocardial precursors derived from the same splanchnic mesoderm.^[1] This process establishes the bilateral cardiogenic primordia, which are initially positioned on either side of the midline due to the flat embryonic disc configuration.^[2] As embryonic folding progresses cephalocaudally and laterally between days 19-21, the bilateral primordia are brought together and fuse at the midline to form a single straight primitive heart tube suspended within the pericardial cavity.^[4] The heart tube initially comprises distinct segments in craniocaudal sequence: the truncus arteriosus, bulbus cordis, primitive ventricle, primitive atrium, and sinus venosus, with the bulbus cordis emerging as the proximal outflow segment immediately caudal to the truncus arteriosus.^[11] This fusion marks the completion of the primary heart tube by approximately day 21, establishing a conduit for early blood circulation.^[12] Key molecular signals orchestrate the specification and regionalization of the heart tube, including bone morphogenetic protein (BMP) and fibroblast growth factor (FGF) pathways, which promote cardiogenic mesoderm induction and proliferation from the lateral plate mesoderm.^[13] BMP signaling, particularly BMP2 and BMP4, induces myocardial differentiation in the cardiogenic field, while FGFs (such as FGF8) support the migration and survival of cardiac progenitors.^[14] The transcription factor NKX2.5 plays a pivotal role in specifying the bulbus cordis region by regulating downstream genes essential for outflow tract development and myocardial identity within the fusing primordia.^[15] By day 21, the fully formed heart tube exhibits peristaltic contractions starting around day 22, initiating primitive blood flow and preparing for subsequent morphogenetic events such as looping.^[11]

Looping and partitioning

Following the formation of the primitive heart tube, cardiac looping represents a critical morphogenetic event that establishes the basic anatomical orientation of the heart. This process begins around day 23 of human embryonic development, when the straight heart tube undergoes an S-shaped bending, primarily driven by differential growth rates and cytoskeletal rearrangements in the myocardium. The bulbus cordis, as the proximal segment of the outflow tract, shifts ventrally, caudally, and rightward during this rightward D-looping, positioning it to contribute to the future right ventricle and conotruncal structures.^[1]^[16] Looping is completed by approximately day 28, transforming the linear tube into a looped configuration that aligns the inflow (atrium and sinus venosus) with the outflow (truncus arteriosus and bulbus cordis) regions.^[1]^[17] Partitioning of the bulbus cordis occurs concurrently with and following looping, involving the formation of bulbar ridges or cushions that divide the outflow tract. These ridges arise from the interaction of endocardial cells undergoing epithelial-to-mesenchymal transition and the influx of cardiac neural crest cells, which migrate from the posterior hindbrain through the pharyngeal arches into the truncus arteriosus and bulbus cordis around weeks 4-5.^[16]^[18] The bulbar ridges swell and fuse in a spiral manner, creating the aorticopulmonary septum that separates the systemic (aorta) and pulmonary circulations; initial septation begins by week 5, with progressive remodeling continuing into week 7.^[1]^[16] This spiral configuration ensures the crossing of the great arteries, a hallmark of normal cardiac anatomy.^[18] The migration of cardiac neural crest cells is pivotal for the structural integrity of the bulbus cordis partitioning, as these cells populate the ridges and orchestrate their fusion into the spiral septum. Originating from rhombomeres 6-8 of the neural tube, these cells delaminate and invade the cardiac outflow tract, providing mesenchymal components essential for septation and semilunar valve formation.^[18] Disruptions in this migration can impair ridge development, though the process is tightly regulated by signaling pathways such as those involving endothelin and semaphorin.^[16] By the end of week 5, the initial partitioning establishes separate outflows, setting the stage for further maturation of the conotruncal region.^[17]

Derivatives in the adult heart

Ventricular contributions

The proximal portion of the bulbus cordis undergoes differentiation to form the trabeculated, or muscular, portion of the right ventricle during early cardiac development. This transformation occurs as the heart tube loops and expands, with the proximal bulbus integrating into the developing ventricular chamber to provide the ridged, contractile myocardium characteristic of the right ventricular body.^[1]^[19] Septation of the bulbus cordis plays a critical role in defining ventricular anatomy, particularly through the formation of the conotruncal septum. This septum arises from endocardial cushions and neural crest cell migrations within the conus cordis (the middle segment of the bulbus), dividing it into distinct outflow pathways and contributing to the infundibulum, or conus arteriosus, which forms the smooth-walled outlet of the right ventricle.^[20]^[21] Concurrently, the proximal bulbus integrates with the adjacent primitive ventricle—primarily destined for the left ventricle—facilitating the development of the smooth septum that separates the right and left ventricular inlets and ensures proper partitioning of blood flow.^[1] These differentiative processes become morphologically evident between weeks 6 and 7 of gestation, coinciding with the progression of ventricular septation and the establishment of distinct right ventricular components. By this stage, the muscular interventricular septum begins to form, marking the completion of bulbus cordis incorporation into the right ventricle.^[22]^[23]

Outflow tract contributions

The distal portion of the bulbus cordis primarily contributes to the formation of the conus cordis and the proximal truncus arteriosus, which together constitute the conotruncal region of the embryonic outflow tract.^[1] This segment elongates and remodels during heart looping to connect the primitive ventricles to the aortic sac, establishing the foundational outflow pathways.^[18] Specifically, it gives rise to the subpulmonary conus, which aligns with the right ventricular outflow, and the subaortic conus, which supports the left ventricular outflow, ensuring proper alignment for arterial connections in the mature heart.^[18] Septation of the outflow tract involves the spiral fusion of endocardial ridges within the truncus arteriosus and conus cordis, derived from the distal bulbus cordis, resulting in the division into the pulmonary trunk and the ascending aorta.^[1] This spiraling process rotates the outflow tracts approximately 180 degrees, positioning the pulmonary trunk anteriorly and to the left of the ascending aorta.^[18] The muscular components from the bulbus cordis myocardium integrate into the conal walls, providing structural support for these divided vessels.^[24] Endocardial cushions within the distal bulbus cordis and truncus arteriosus swell and fuse, contributing to the anlagen of the semilunar valves at the bases of the pulmonary trunk and ascending aorta.^[1] These cushions, formed from endocardial cell transformations, excavate to create the three cusps of the aortic and pulmonary valves, ensuring unidirectional blood flow.^[18] Outflow tract septation, including conotruncal partitioning and semilunar valve maturation from bulbus cordis derivatives, is largely complete by embryonic weeks 7 to 8.^[22]

Comparative anatomy

In non-mammalian vertebrates

In fish, particularly teleosts, the bulbus cordis is represented by the bulbus arteriosus, a prominent, elastic structure located distal to the single ventricle that functions as a reservoir to dampen pressure fluctuations during ventricular contraction, preventing damage to the gills and ensuring steady blood flow to the systemic circulation.^[25] This region lacks any septation, maintaining a single outflow tract consistent with the undivided circulatory system in these species.^[26] In amphibians and most reptiles, the bulbus cordis develops into the conus arteriosus, which serves as the primary outflow tract from the ventricle, providing muscular control over ejection while the spiral valve or trabeculae in the ventricle handle partial mixing of oxygenated and deoxygenated blood.^[27] However, in crocodilians, a subgroup of reptiles, complete septation occurs in the heart derived from the bulbus cordis, resulting in a four-chambered heart with full separation of pulmonary and systemic circulations, which can be shunted during diving via the foramen of Panizza.^[28] Birds exhibit a bulbus cordis structure more akin to that in mammals, where it contributes significantly to the right ventricular outflow tract and facilitates the complete partitioning of pulmonary and systemic circulations through its incorporation into the conotruncal region during development.^[26] This adaptation supports the high metabolic demands of flight by ensuring efficient, separated blood flows. Across these non-mammalian vertebrates, the developmental process of the bulbus cordis shows conservation in the initial looping of the heart tube, but the extent of subsequent partitioning varies with circulatory requirements, from fully undivided in fish to progressively more separated in reptiles and birds to accommodate evolving respiratory and metabolic needs.

Evolutionary origins

The bulbus cordis, representing a key segment of the primitive vertebrate heart outflow tract, traces its origins to early chordate circulatory systems, where precursor structures provided elastic modulation of blood flow to support gill-based respiration. In basal chordates like amphioxus, simple peristaltic tubes served as foundational elements for unidirectional flow, evolving into more specialized outflow regions in jawed vertebrates to dampen pressure pulses during gill perfusion.^[29] This ancestral role emphasized compliance and volume buffering, essential for efficient oxygen exchange in aquatic environments. The transition to tetrapod lineages around 400 million years ago during the Devonian period marked a pivotal shift, as the emergence of lungs drove the evolution of dual circulations, with bulbus cordis derivatives contributing to outflow septation for separating pulmonary and systemic pathways. Linked to the water-to-land transition in sarcopterygian fish, this adaptation involved partial partitioning of the conus arteriosus, enabling oxygenated blood routing to developing air-breathing organs while maintaining gill function in transitional forms.^[30] In amniotes, key adaptations included enhanced myocardial thickness in bulbus-derived outflow regions to accommodate elevated pressures from fully terrestrial, endothermic physiologies, contrasting with losses in primitive lineages such as cyclostomes, where simple, unpartitioned tubular hearts lack distinct elastic bulbus structures.^[29] Fossil evidence supports this progression: a remarkably preserved 380-million-year-old heart from a Devonian placoderm fish reveals a basic outflow vessel akin to early bulbus precursors, while therapsid synapsids from the late Paleozoic to Mesozoic exhibit inferred full cardiac partitioning, paving the way for mammalian four-chambered designs.^[31]

Clinical significance

Associated congenital defects

Abnormal development of the bulbus cordis, a key component of the embryonic outflow tract (OFT), contributes to conotruncal congenital heart defects through disruptions in septation, rotation, and alignment processes that separate the pulmonary and systemic circulations.^[18] These malformations often stem from defective neural crest cell migration or second heart field contributions, leading to misalignment of the great arteries relative to the ventricles.^[32] Tetralogy of Fallot arises from incomplete conotruncal septation, where the OFT cushions fail to fuse properly, resulting in pulmonary stenosis, a ventricular septal defect, overriding aorta, and right ventricular hypertrophy.^[18] This unequal division of the conus portion of the bulbus cordis displaces the conotruncal septum anteriorly, narrowing the right ventricular outflow tract and allowing deoxygenated blood to shunt into the systemic circulation.^[20] Transposition of the great arteries occurs due to failure of spiral septation in the bulbus cordis and truncus arteriosus, causing the conotruncal septum to descend straight rather than rotate, which positions the aorta over the right ventricle and the pulmonary artery over the left.^[20] This ventriculoarterial discordance creates parallel systemic and pulmonary circulations, severely impairing oxygenation unless a shunt exists.^[18] Persistent truncus arteriosus results from failure of the aorticopulmonary septum to form, leading to a single arterial trunk arising from the heart supplying both systemic and pulmonary circulations, often with a ventricular septal defect.^[1] Double outlet right ventricle results from unbalanced or excessive bulbar overgrowth, particularly of the subpulmonary conus, leading to both great arteries arising from the right ventricle due to incomplete OFT septation.^[18] Pathophysiologically, this often accompanies a ventricular septal defect, causing mixing of oxygenated and deoxygenated blood and potential cyanosis or heart failure depending on the exact alignment.^[32] Genetic factors play a significant role in these defects, with mutations in TBX1 causing haploinsufficiency that disrupts pharyngeal arch and OFT development, as seen in DiGeorge syndrome (22q11.2 deletion), which accounts for up to 12% of conotruncal malformations including tetralogy of Fallot and double outlet right ventricle.^[33] Similarly, GATA4 mutations impair second heart field signaling essential for bulbus cordis septation, contributing to transposition of the great arteries and other conotruncal anomalies.^[32] Defects in neural crest cell migration, often linked to these genetic disruptions, further exacerbate abnormal bulbar remodeling in conditions like DiGeorge syndrome.^[18]

Diagnostic considerations

Prenatal diagnosis of anomalies related to the bulbus cordis primarily relies on fetal echocardiography, which is typically performed between 18 and 22 weeks of gestation to assess outflow tract alignment, septation, and great vessel relationships.^[34] This imaging modality achieves diagnostic accuracy for conotruncal defects of approximately 77% for complete diagnoses and 89% for outflow tract obstructions, according to key studies evaluating anatomic details such as ventricular-arterial connections.^[35] Early detection through these scans enables multidisciplinary planning, including referral to specialized centers, which has been shown to reduce morbidity and improve surgical outcomes.^[36] Postnatally, confirmation of suspected bulbus cordis-derived anomalies, such as overriding aorta in conditions like tetralogy of Fallot, involves transthoracic echocardiography as the initial imaging tool, supplemented by cardiac MRI or CT angiography for detailed three-dimensional assessment of the outflow tract and associated vascular structures.^[37] Echocardiography provides real-time evaluation of hemodynamics and septal integrity, while MRI offers superior soft tissue resolution without radiation, and CT excels in visualizing coronary arteries and extracardiac vessels.^[38] These modalities are essential for preoperative planning and long-term monitoring, particularly in complex cases requiring intervention.^[39] Genetic screening plays a crucial role in evaluating associated syndromes, with chromosomal microarray analysis recommended as a first-tier test for infants with conotruncal anomalies to detect copy number variants, such as 22q11.2 deletions, which occur in approximately 10-12% of cases.^[40]^[41] Targeted sequencing may follow for single-gene disorders if microarray results are negative, aiding in risk stratification for neurodevelopmental comorbidities.^[42] Conotruncal anomalies affect approximately 1 in 1,000 live births, and prenatal or early postnatal detection significantly enhances survival rates by facilitating timely interventions.^[43]^[44]

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