The ovine cerebral venous system: comparative anatomy, visualization, and implications for translational research

Abstract

Cerebrovascular diseases are significant causes of death and disability in humans. Improvements in diagnostic and therapeutic approaches strongly rely on adequate gyrencephalic, large animal models being demanded for translational research. Ovine stroke models may represent a promising approach but are currently limited by insufficient knowledge regarding the venous system of the cerebral angioarchitecture. The present study was intended to provide a comprehensive anatomical analysis of the intracranial venous system in sheep as a reliable basis for the interpretation of experimental results in such ovine models. We used corrosion casts as well as contrast-enhanced magnetic resonance venography to scrutinize blood drainage from the brain. This combined approach yielded detailed and, to some extent, novel findings. In particular, we provide evidence for chordae Willisii and lateral venous lacunae, and report on connections between the dorsal and ventral sinuses in this species. For the first time, we also describe venous confluences in the deep cerebral venous system and an 'anterior condylar confluent' as seen in humans. This report provides a detailed reference for the interpretation of venous diagnostic imaging findings in sheep, including an assessment of structure detectability by in vivo (imaging) versus ex vivo (corrosion cast) visualization methods. Moreover, it features a comprehensive interspecies-comparison of the venous cerebral angioarchitecture in man, rodents, canines and sheep as a relevant large animal model species, and describes possible implications for translational cerebrovascular research.

Figure 1. Morphology of the dorsal sagittal sinus.

(A) Schematic drawing of corrosion cast, dorsal view. (B) Corrosion cast, dorsal view. The dorsal sagittal sinus (DSS) was the major cerebral venous drainage of the dorsal sinus system. Along its course, the DSS received ethmoidal, cerebral, meningeal, and diploic veins from the skull. Its superficial profile showed an axial groove over the whole length and nodular protrusions on the caudal one-third of the DSS (B, arrowheads). (C) Corrosion cast, lateral left view. The confluences of the dorsal cerebral veins (DCV) with the DSS showed pinhead-like openings called lateral venous lacunae (LVLs; A, C, D, E) and providing cerebrospinal fluid drainage into the venous system. (D) MRV, coronal section (maximum intensity projection of E, green). (E) MRV, sagittal section. The LVLs are interlinked between the DCV and the DSS in two different sections of MRV. DCV: dorsal cerebral vein, DPS: dorsal petrosal sinus, DSS: dorsal sagittal sinus, EV: ethmoidal vein, LVLs: lateral venous lacunae, SiS: sigmoid sinus, TeS: temporal sinus, TrS: transverse sinus.

Figure 2. Deep cerebral venous system.

(A) Schematic drawing of corrosion cast, lateral right view. The straight sinus (SS) was the venous drainage route of the medial cortex, the corpus callosum, the basal ganglia and part of the diencephalon (A–E). (B) Corrosion cast, dorsolateral right view. The unpaired great cerebral vein (GCV) was formed by both internal cerebral veins (ICV) in the ‘confluens venosus caudalis’ (A, B; white star). The vein of corpus callosum (VCC) and the lateral vein (LV), with three tributaries, drained into the GCV. The ICVs originated from two distinct converging branches in the ‘confluens venosus rostralis’ (A, B; white dots): the vein of the septum pellucidum (VSP) and the thalamostriate vein (TSV). The TSVs received inflow from caudate nucleus veins (VCN; A, B) and from the choroidal vein (ChV; A, B). (C) MRV, sagittal section. (D) MRV, coronal section. The confluence of sinuses (orange circle; C, D) referred to the crossroad between the DSS, the SS and both transverse sinuses (TrS). (E) CTV, sagittal section. The VCC was large and conspicuous in the corrosion cast (A, B), but much less prominent in CTV imaging (E, arrowheads). CeV: central vein, ChV: choroidal vein, DMBCV: dorsomedial basilar cerebral vein, DSS: dorsal sagittal sinus, GCV: great cerebral vein, ICV: internal cerebral vein, LV: lateral vein, RVCrV: rostral ventral cerebellar vein, SS: straight sinus, TrS: transverse sinus, TSV: thalamostriate vein, VCC: vein of the corpus callosum, VCN: vein of caudate nucleus, VSP: vein of the septum pellucidum. Please note: right TSV removed for better insight and interpretation in A and B.

Figure 3. Ventral cerebral veins and the anastomoses of the ventral sinus system.

(A) Schematic drawing of corrosion cast, dorsal view. The ventral cerebral veins included the basilar cerebral vein (BCV) and the rhinal vein (RV), which joined the dorsal petrosal sinus (DPS) as the main drainage system of the ventral cerebral veins,. (B) Corrosion cast, dorsocaudal view. The piriform lobe vein (PLV) drained into the RV (A, B) whereas the pontine vein (PV) and the ventral cerebellar vein (VCrV) joined the DPS (A, C) (C) Corrosion cast, dorsolateral right view. An anastomotic ramus projected from the BCV into the cavernous sinus (CS; AR−BCV+CS; A, C). (D) Corrosion cast, right caudodorsolateral view. The rostral cerebral veins (RCV) and the middle cerebral veins (MCV) drained into the BCV. (E) Schematic drawing of corrosion cast, dorsal view. The ventral sinus system includes three main bilaterally symmetrical sinuses, whereas all sinuses had an interconnection with their opposite side. (F) Corrosion cast, dorsorostral view. From rostral to caudal: the CS with the caudal intercavernous sinus (CIS), the ventral petrosal sinus (VPS) with an intraosseus anastomotic ramus of the VPS (AR-VPS) and the ventral occipital sinus (VOS) with an anastomotic vein (AR-VOS), which pass the foramen magnum ventrally. AR−BCV+CS: anastomotic ramus of the BCV and CS, AR−VOS: anastomotic ramus of the VOS, AR−VPS: anastomotic ramus of the VPS, BCV: basilar cerebral vein, CIS: caudal intercavernous sinus, CS: cavernous sinus, DPS: dorsal petrosal sinus, DSS: dorsal sagittal sinus, EVOrF: emissary vein of the foramen orbitorotundum, EVOvF: emissary vein of oval foramen, MCV: middle cerebral vein, PLV: piriform lobe vein, PV: pontine vein, RCV: rostral cerebral vein, RV: rhinal vein, TrS: transverse sinus, VCC: vein of corpus callosum, VCrV: ventral cerebellar vein, VOS: ventral occipital sinus, VPS: ventral petrosal sinus.

Figure 4. Course of the emissary veins of the temporal sinus and the formation of the anterior condylar confluent.

(A) 3D CT reconstruction of the head combined with schematic vein drawings (blue), lateral, left view. White frame: inset of B. The ovine extracranial veins can be observed in this view, particularly the outer drainage system of the intracranial veins. (B) 3D CT scan combined with schematic diagram of blue and orange colored veins (interrupted orange vein of temporal sinus shows the invisible part of the sinus in the temporal meatus), lateral left view (paracondylar process removed). (C) Corrosion cast, lateral left view. The temporal sinus (TeS) ran through the temporal meatus and split into two distinct vessels, (1) the first emissary vein (EVRF-1), which left the main opening of the retroarticular foramen and joined the maxillary vein (MV), and (2) the second emissary vein (EVRF-2) which ran next to a tributary canal, passed a tributary foramen, and joined the profundal temporal vein (PTV). (D) Corrosion cast, lateral right view. (E) Corrosion cast, ventrolateral view. The emissary vein of the jugular foramen and the emissary vein of the hypoglossal canal converged towards an extracranial orifice and formed the ‘anterior condylar confluent’ (ACC). The emissary vein of the jugular foramen and hypoglossal canal (EVJFHC) merged with an anastomotic ramus of the vertebral vein (AR-VV), to form the craniooccipital vein (COV), which drained into the external jugular vein (EJV). (F) 3D CT scan, ventrolateral view. The ACC is a clearly visible structure in the sheep. ACC: anterior condylar confluent, AR-VV: anastomotic ramus of the vertebral vein, COV: craniooccipital vein, EJV: external jugular vein, EVJFHC: emissary vein of the jugular foramen and hypoglossal canal, EVRF-1: first emissary vein of retroarticular foramen, EVRF-2: second emissary vein of retroarticular foramen, MV: maxillary vein, PP: pterygoid plexus, PTV: profundal temporal vein, STV: superficial temporal vein, TeS: temporal sinus.

Figure 5. Coronal MRV slices through the head of a sheep after intravenous injection of Gadolinium (Dotarem).

(A) Lateral, left view of the ovine brain. Lines delineate the levels of coronal MRV slices, letters correspond to the letters in coronal MRV images; B–K, MRV, coronal sections. The angioarchitecture of the dorsal and ventral sinus systems including their connecting veins was clearly depicted after contrast injection of Gadolinium (Dotarem) in comparison to the deep and ventral cerebral veins. Note the completely visible signals of the dorsal sagittal sinus (DSS; B–G), the transverse sinus (TrS; G–I), the temporal sinus (TeS; G–I), the sigmoid sinus (SiS; I–K), the cavernous sinus (CS; D–G), the ventral petrosal sinus (VPS; H), the ventral occipital sinus (VOS; K), the anterior condylar confluent (ACC; J), as well as the great cerebral vein (GCV; E, F) and the straight sinus (SS, F, G). Note the faint signal of the thalamostriate veins (TSV; C, D), the internal cerebral veins (ICV, D), the basilar cerebral vein (BCV), and the dorsal petrosal sinus (DPS; D, F, H). Two anastomotic rami could be seen in MRV strongly: the anastomotic ramus between cavernous sinus and pterygoid plexus (AR-CS+PP; D) with a highly signal intensity and the anastomotic ramus between BCV and CS (AR-BCV+CS; G) as a diminutive vessel. ACC: anterior condylar confluent, AR−BCV+CS: anastomotic ramus between basilar cerebral vein and cavernous sinus, AR−CS+PP: anastomotic ramus between cavernous sinus and pterygoid plexus, AR−VOS: anastomotic ramus between both ventral occipital sinus, BCV: basilar cerebral vein, BuV: buccal vein, CIS: caudal intercavernous sinus, DCV: dorsal cerebral vein, DPS: dorsal petrosal sinus, DSS: dorsal sagittal sinus, EVJFHC: emissary vein of jugular foramen and hypoglossal canal, EVOrF: emissary vein of the foramen orbitorotundum, EVOvF: emissary vein of oval foramen, EVRF-2: second emissary vein of retroarticular foramen, GCV: great cerebral vein, ICV: internal cerebral vein, OP: ophthalmic plexus, PTV: profundal temporal vein, RV: rhinal vein, SiS: sigmoid sinus, SS: straight sinus, STV: superficial temporal vein, TeS: temporal sinus, TrS: transverse sinus, TSV: thalamostriate vein, VOS: ventral occipital sinus, VPS: ventral petrosal sinus.

Figure 6. Axial MRV slices through the head of a sheep after intravenous injection of Gadolinium (Dotarem).

(A) Lateral left view of the ovine brain. Lines delineate the levels of axial MRV slices, letters correspond to the letters in the axial MRV images; B–J, MRV, axial sections. Note the irregular filling of the completely visible dorsal sagittal sinus (DSS) after intravenous injection of Gadolinium (Dotarem) as a result of the chordae Willisii (B). A better detectability of the deep and ventral cerebral veins can be observed in the axial slices. The great cerebral vein (GCV) and the straight sinus (SS) were completely visible (C–E), the thalamostriate vein (TSV) and the internal cerebral vein (ICV) were moderately visible (C–F), but no evidence of the vein of septum pellucidum (VSP) or choroidal veins (ChVs) was found. The visualization of the basilar cerebral vein (BCV) and the rhinal vein (RV) were barely visible and the dorsal petrosal sinus (DPS) was moderately conspicuous in MRV (C–G). The first emissary vein of retroarticular foramen (EVRF-1) was a moderately visible vein (E, F). The second emissary vein of retroarticular foramen (EVRF-2) was a noticeable vessel which passed the tributary canal of the temporal meatus and drained into the profundal temporal vein (PTV; E–H). The butterfly-shaped cavernous sinus (CS) could be regarded as a venous crossroad with star-shaped connections to intra- and extracranial veins (I, J). From rostral to caudal, these were: (1) the emissary vein of orbitorotund foramen (EVOrF; I) with the ophthalmic plexus (OP; I); (2) the anastomotic ramus between cavernous sinus and pterygoid plexus (PP) (AR-CS+PP; J); (3) the emissary vein of the oval foramen (EVOvF; J) with the PP; (4) the ventral petrosal sinus (VPS; I) and (5) the caudal intercavernous sinus (CIS; J). Note the clear delineation of the anterior condylar confluent (ACC; I). ACC: anterior condylar confluent, AR−CS+PP: anastomotic ramus between cavernous sinus and pterygoid plexus, AR−VOS: anastomotic ramus between both ventral occipital sinus, BCV: basilar cerebral vein, BuV: buccal vein, CC: condylar canal, ChV: choroidal veins, CIS: caudal intercavernous sinus, CS: cavernous sinus, DCV: dorsal cerebral vein, DPS: dorsal petrosal sinus, DSS: dorsal sagittal sinus, EV: ethmoidal vein, EVOrF: emissary vein of the foramen orbitorotundum, EVOvF: emissary vein of oval foramen, EVRF-1: first emissary vein of retroarticular foramen, EVRF-2: second emissary vein of retroarticular foramen, GCV: great cerebral vein, ICV: internal cerebral vein, OP: ophthalmic plexus, PP: pterygoid plexus, RV: rhinal vein, SiS: sigmoid sinus, SS: straight sinus, TeS: temporal sinus, TrS: transverse sinus, TSV: thalamostriate vein, VOS: ventral occipital sinus, VPS: ventral petrosal sinus VSP: vein of septum pellucidum.

Figure 7. Sagittal MRV slices through the head of a sheep after intravenous injection of Gadolinium (Dotarem).

(A) Dorsal view of the ovine brain. Lines delineate the levels of sagittal MRV slices, letters correspond to the letters in sagittal MRV images; B–H, MRV, sagittal sections. The sagittal sections provided a detailed depiction of all intracranial sinuses and veins, also the deep and ventral cerebral veins and particularly the confluence of sinus (B). Interestingly, the vein of corpus callosum (VCC) could not be detected in MRV. The thalamostriate vein (TSV; B, arrowheads) showed a cornu-like course and drained into the conspicuous internal cerebral vein (ICV; B). The weakly filled basilar cerebral vein (BCV; C, D, E, arrowheads) could easily be identified over a longer distances. BCVs and rhinal veins (RVs) drained through the dorsal petrosal sinus (DPS; D, E, F) into the transverse sinus (TrS; E, F, G). The TrS split into the temporal sinus (TeS) and the sigmoid sinus (SiS; F–H). Note the clear illustration of the TrS, TeS, SiS and the anterior condylar confluent (ACC; D–G). The ACC offered a large extent in these sagittal sections (D, arrowheads). The first (EVRF-1) and the second (EVRF-2; H, arrowhead) emissary vein of retroarticular foramen are clearly visible. ACC: anterior condylar confluent, AR−CS+PP: anastomotic ramus between cavernous sinus and pterygoid plexus, BCV: basilar cerebral vein, CS: cavernous sinus, DPS: dorsal petrosal sinus, DSS: dorsal sagittal sinus, EVJFHC: emissary vein of jugular foramen and hypoglossal canal, EVOrF: emissary vein of foramen orbitorotundum, EVOvF: emissary vein of oval foramen, EVRF-1: first emissary vein of retroarticular foramen, EVRF-2: second emissary vein of retroarticular foramen, GCV: great cerebral vein, ICV: internal cerebral vein, OP: ophthalmic plexus, PTV: profundal temporal vein, RV: rhinal vein, SiS: sigmoid sinus, SS: straight sinus, TeS: temporal sinus, TrS: transverse sinus, TSV: thalamostriate vein, VCC: vein of the corpus callosum, VOS: ventral occipital sinus, VPS: ventral petrosal sinus.