Collagen fibre orientation in human bridging veins

Abstract

Bridging veins (BVs) drain the blood from the cerebral cortex into dural sinuses. BVs have one end attached to the brain and the other to the superior sagittal sinus (SSS), which is attached to the skull. Relative movement between these two structures can cause BV to rupture producing acute subdural haematoma, a head injury with a mortality rate between 30 and 90%. A clear understanding of the BVs microstructure is required to increase the biofidelity of BV models when simulating head impacts. Twelve fresh BV samples draining in the superior sagittal sinus (SSS) from a single human cadaver were cut open along their length and placed on an inverted multiphoton microscope. To ensure that the BVs were aligned with the axial direction an in-house built, uniaxial tension set-up was used. Two scans were performed per sample. Before the first scan, a minor displacement was applied to align the tissue; then, a second scan was taken applying 50% strain. Each BV was scanned for a length of 5 mm starting from the drainage site into the SSS. Imaging was performed on a Zeiss LSM780 microscope with an 25\(\times\) water immersion objective (NA 0.8), coupled to a tunable MaiTai DS (Spectraphysics) pulsed laser with the wavelength set at 850 nm. Second harmonic and fluorescence signals were captured in forward and backward direction on binary GaAsP (BiG) detectors and stored as four colour Z-stacks. Prior to the calculation of the local orientations, acquired Z-stacks were denoised and enhanced to highlight fibrillar structures from the background. Then, for each Z-plane of the stack, the ImageJ plugin OrientationJ was used to extract the local 2D orientations of the fibres based on structure tensors. Two kinds of collagen architectures were seen. The most common (8\(/\)12 samples) was single layered and had a uniform distribution of collagen. The less common (4\(/\)12 samples) had 2 layers and 7 to 34 times thicker collagen bundles on the outer layer. Fibre angle analysis showed that collagen was oriented mainly along the axial direction of the vessel. The von Mises fittings showed that in order to describe the fibre distribution 3 components were needed with mean angles \(\mu\) at \(-\) 0.35, 0.21, \(-\) 0.02 rad or \(-\) 20.2\(^{\circ }\), 12.1\(^{\circ }\), \(-\) 1.2\(^{\circ }\) relative to the vessel’s axial direction which was also the horizontal scan direction.

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Acknowledgements

This work was supported by the European Unions Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No. 642662 for HEADS ITN and by a personal FWO fellowship (PDO\(/\) 12), a FWO grant G0C6713N, a FWO grant G.0929.15 and Hercules AKUL\(/\)11\(/\) 37

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Correspondence to Markos Kapeliotis.

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The authors have no conflicts of interest arising from the direct applications of this research.

Appendix

Appendix

Detailed results for all individual scans and groups

The remaining results from the microscopic analysis of the BV are placed in this section of the appendix. In order to maximize the amount of detail that can be seen in the scans and figures, the microscopy colour maps and the analysis in blocks are displayed in landscape.

Therefore instead of displaying by sample, the results are displayed by category, first the colour maps then the entire length analysis and then the analysis in blocks.

Fibre orientation analysis results summary

See Tables 2, 3 and 4 and Figs. 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, and 51.

Table 2 Summary table of the fibre orientation analysis—entire scan length, 0% strain and 50% strain
Table 3 Summary table of the fibre orientation analysis—4 blocks of equal scan length, 0% strain
Table 4 Summary table of the fibre orientation analysis—4 blocks of equal scan length, 50% strain
Fig. 16
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Sample 3 (frontal, right, \(\varnothing\) 3.2mm, WT:112 μm). Fibre orientation colour maps (top: no strain, bottom: 50% strain)

Fig. 17
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Sample 4 (frontal, right, \(\varnothing\) 2.1 mm, WT:112 μm). Fibre orientation colour maps (top: no strain, bottom: 50% strain)

Fig. 18
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Sample 9 (occipital, right, \(\varnothing\) 2.7mm, WT:147 μm). Fibre orientation colour maps (top: no strain, bottom: 50% strain)

Fig. 19
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Sample 10 (frontal, left, \(\varnothing\) 3.8mm, WT:153 μm). Fibre orientation colour maps (top: no strain, bottom: 50% strain)

Fig. 20
figure20

Sample 11 (frontal, left, \(\varnothing\) 3.2mm, WT:144 μm). Fibre orientation colour maps (top: no strain, bottom: 50% strain)

Fig. 21
figure21

Sample 12 (frontal, left, \(\varnothing\) 2.1mm, WT:114 μm). Fibre orientation colour maps (top: no strain, bottom: 50% strain)

Fig. 22
figure22

Sample 13 (parietal, left, \(\varnothing\) 3.9 mm, WT:186 μm). Fibre orientation colour maps (top: no strain, bottom: 50% strain)

Fig. 23
figure23

Sample 14 (parietal, left, \(\varnothing\) 1.9mm, WT:155 μm). Fibre orientation colour maps (top: no strain, bottom: 50% strain)

Fig. 24
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Sample 15 (occipital, left, \(\varnothing\) 2.6mm, WT:156 μm). Fibre orientation colour maps (top: no strain, bottom: 50% strain)

Fig. 25
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Sample 16 (occipital, left, \(\varnothing\) 1.3mm, WT:108 μm). Fibre orientation colour maps (top: no strain, bottom: 50% strain)

Fig. 26
figure26

Sample 3, Entire scan analysis—fibre orientations with von Mises fittings (left: no strain, right: 50% strain)

Fig. 27
figure27

Sample 4, Entire scan analysis—fibre orientations with von Mises fittings (left: no strain, right: 50% strain)

Fig. 28
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Sample 9, Entire scan analysis—fibre orientations with von Mises fittings (left: no strain, right: 50% strain)

Fig. 29
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Sample 10, Entire scan analysis—fibre orientations with von Mises fittings (left: no strain, right: 50% strain)

Fig. 30
figure30

Sample 11, Entire scan analysis—fibre orientations with von Mises fittings (left: no strain, right: 50% strain)

Fig. 31
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Sample 12, Entire scan analysis—fibre orientations with von Mises fittings (left: no strain, right: 50% strain)

Fig. 32
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Sample 13, Entire scan analysis—fibre orientations with von Mises fittings (left: no strain, right: 50% strain)

Fig. 33
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Sample 14, Entire scan analysis—fibre orientations with von Mises fittings (left: no strain, right: 50% strain)

Fig. 34
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Sample 15, Entire scan analysis—fibre orientations with von Mises fittings (left: no strain, right: 50% strain)

Fig. 35
figure35

Sample 16, Entire scan analysis—fibre orientations with von Mises fittings (left: no strain, right: 50% strain)

Fig. 36
figure36

Frontal lobe group, Entire scan analysis—fibre orientations with von Mises fittings for the frontal lobe (left: no strain, right: 50% strain)

Fig. 37
figure37

Parietal lobe group, Entire scan analysis—fibre orientations with von Mises fittings for the parietal lobe (left: no strain, right: 50% strain)

Fig. 38
figure38

Occipital lobe group, Entire scan analysis—fibre orientations with von Mises fittings for the occipital lobe (left: no strain, right: 50% strain)

Fig. 39
figure39

Sample 3, Block analysis—fibre orientations with von Mises fittings (top: no strain, bottom: 50% strain, right to left: SSS to brain

Fig. 40
figure40

Sample 4, Block analysis—fibre orientations with von Mises fittings (top: no strain, bottom: 50% strain, right to left: SSS to brain)

Fig. 41
figure41

Sample 9, Block analysis—fibre orientations with von Mises fittings (top: no strain, bottom: 50% strain, right to left: SSS to brain)

Fig. 42
figure42

Sample 10, Block analysis—fibre orientations with von Mises fittings (top: no strain, bottom: 50% strain, right to left: SSS to brain)

Fig. 43
figure43

Sample 11, Block analysis—fibre orientations with von Mises fittings (top: no strain, bottom: 50% strain, right to left: SSS to brain)

Fig. 44
figure44

Sample 12, Block analysis—fibre orientations with von Mises fittings (top: no strain, bottom: 50% strain, right to left: SSS to brain)

Fig. 45
figure45

Sample 13, Block analysis—fibre orientations with von Mises fittings (top: no strain, bottom: 50% strain, right to left: SSS to brain)

Fig. 46
figure46

Sample 14, Block analysis—fibre orientations with von Mises fittings (top: no strain, bottom: 50% strain, right to left: SSS to brain)

Fig. 47
figure47

Sample 15, Block analysis—fibre orientations with von Mises fittings (top: no strain, bottom: 50% strain, right to left: SSS to brain)

Fig. 48
figure48

Sample 16, Block analysis—fibre orientations with von Mises fittings (top: no strain, bottom: 50% strain, right to left: SSS to brain)

Fig. 49
figure49

Frontal lobe group, Block analysis—fibre orientations with von Mises fittings for the frontal lobe (top: no strain, bottom: 50% strain, right to left: SSS to brain)

Fig. 50
figure50

Parietal lobe group, Block analysis—fibre orientations with von Mises fittings for the parietal lobe (top: no strain, bottom: 50% strain, right to left: SSS to brain)

Fig. 51
figure51

Occipital lobe group, Block analysis—fibre orientations with von Mises fittings for the occipital lobe (top: no strain, bottom: 50% strain, right to left: SSS to brain)

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Kapeliotis, M., Gavrila Laic, R.A., Peñas, A.J. et al. Collagen fibre orientation in human bridging veins. Biomech Model Mechanobiol (2020). https://doi.org/10.1007/s10237-020-01349-w

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Keywords

  • Bridging veins
  • Collagen fibres
  • Orientation
  • Multiphoton microscopy
  • Acute subdural hematoma
  • Traumatic brain injury