Skip to main content

Advertisement

SpringerLink
Log in

Collagen fibre orientation in human bridging veins

  • Original Paper
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15

Similar content being viewed by others

References

  • Archana JN, Aishwarya P (2016) A review on the image sharpening algorithms using unsharp masking. Int J Eng Sci Comput 6:8729–8733

    Google Scholar 

  • Becker W, Rowson J, Oakley JE, Yoxall A, Manson G, Worden K (2011) Bayesian sensitivity analysis of a model of the aortic valve. J Biomech 44(8):1499–1506. https://doi.org/10.1016/j.jbiomech.2011.03.008

    Article  Google Scholar 

  • Becker W, Oakley JE, Surace C, Gili P, Rowson J, Worden K (2012) Bayesian sensitivity analysis of a nonlinear finite element model. Mech Syst Signal Process 32:18–31. https://doi.org/10.1016/j.ymssp.2012.03.009

    Article  Google Scholar 

  • Becker W, Worden K, Rowson J (2013) Bayesian sensitivity analysis of bifurcating nonlinear models. Mech Syst Signal Process 34(1–2):57–75. https://doi.org/10.1016/j.ymssp.2012.05.010

    Article  Google Scholar 

  • Bentley J (2006) Modelling circular data using a mixture of von mises and uniform distributions. Simon Fraser University Fall.

  • Brockmann C, Kunze SC, Schmiedek P, Groden C, Scharf J (2012) Variations of the superior sagittal sinus and bridging veins in human dissections and computed tomography venography. J Clin Imaging 36(2):85–89. https://doi.org/10.1016/j.clinimag.2011.05.003

    Article  Google Scholar 

  • Cai Y, Wu S, Zhao W, Li Z, Wu Z, Ji S (2018) Concussion classification via deep learning using whole-brain white matter fiber strains. PLoS ONE 13:1–21

    Google Scholar 

  • Davies E (1990) Machine vision: theory, algorithms and practicalities. Academic Press, Cambridge

    Google Scholar 

  • Depreitere B, Van Lierde C, Maene S, Plets C, Sloten JV, Van Audekercke R, Van der Perre G, Goffin J (2004) Bicycle-related head injury: a study of 86 cases. Accid Anal Prev 36(4):561–567

    Article  Google Scholar 

  • Dhillon IS, Sra S (2003) Modeling data using directional distributions. Technical Report # TR-03-06. 1–21

  • Famaey N, Cui Z Ying, Musigazi G Umuhire, Ivens J, Depreitere B, Verbeken E, Sloten J Vander (2015) Structural and mechanical characterisation of bridging veins: a review. J Mech Behav Biomed Mater 41:222–240

    Article  Google Scholar 

  • Garcia D (2010) Robust smoothing of gridded data in one and higher dimensions with missing values. Comput Stat Data Anal 54(4):1167–1178

    Article  MathSciNet  Google Scholar 

  • Kegel DD, Vastmans J, Fehervary H, Depreitere B, Sloten JV (2018) Biomechanical characterization of human dura mater. J Mech Behav Biomed Mater 79:122–134. https://doi.org/10.1016/j.jmbbm.2017.12.023

    Article  Google Scholar 

  • Monson KL, Goldsmith W, Barbaro NM, Manley GT (2005) Significance of source and size in the mechanical response of human cerebral blood vessels. J Biomech 38(4):737–744

    Article  Google Scholar 

  • Ni Annaidh A, Bruy K, Destrade M, Gilchrist MD, Maurini C, Ottenio M, Saccomandi G (2012) Automated estimation of collagen fibre dispersion in the dermis and its contribution to the anisotropic behaviour of skin. Ann Biomed Eng 40(8):1–37

    Google Scholar 

  • Nierenberger M, Re Y, Ahzi S (2013) A new multiscale model for the mechanical behavior of vein walls. J Mech Behav Biomed Mater 23:32–43

    Article  Google Scholar 

  • Nierenberger M, Fargier G, Ahzi S, Rémond Y (2015) Evolution of the three-dimensional collagen structure in vascular walls during deformation: an in situ mechanical testing under multiphoton microscopy observation. Biomecha Model Mechanobiol. https://doi.org/10.1007/s10237-014-0630-4

    Article  Google Scholar 

  • Oka K, Rhoton AL, Barry M, Rodriguez R (1985) Microsurgical anatomy of the superficial veins of the cerebrum, Forensic Science International. Neurosurgery 17(5):711–748

    Article  Google Scholar 

  • Pang Q, Gregersen H, Oettingen V, Astrup J (2001) Biomechanical properties of porcine cerebral bridging veins with reference to the zero-stress state. J Vasc Res 38(1):83–90

    Article  Google Scholar 

  • Puspoki Z, Storath M, Sage D, Unser M (2016) Transforms and operators for directional bioimage analysis: a survey. Adv Anat Embryol Cell Biol 219:69–93

    Article  Google Scholar 

  • Rezakhaniha R, Agianniotis A, Schrauwen JTC, Griffa A, Sage D, Bouten CVC, van de Vosse FN, Unser M, Stergiopulos N (2012) Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy. Biomech Model Mechanobiol 11(3–4):461–473

    Article  Google Scholar 

  • Vesely J, Horny L, Chlup H, Zitny R (2011) Collagen orientation and waviness within the vein wall. In: Computational plasticity XI-fundamentals and applications, COMPLAS XI

  • Vignes J-R, Dagain A, Guerin J, Liguoro D (2007) A hypothesis of cerebral venous system regulation based on a study of the junction between the cortical bridging veins and the superior sagittal sinus. Laboratory investigation. J Neurosurg 107(6):1205–1210

    Article  Google Scholar 

  • Wang Y, Son S, Swartz SM, Goulbourne NC (2012) A mixed Von Mises distribution for modeling soft biological tissues with two distributed fiber properties. Int J Solids Struct 49(21):2914–2923. https://doi.org/10.1016/j.ijsolstr.2012.04.004

    Article  Google Scholar 

  • Yamashima T, Friede RL (1984) Why do bridging veins rupture into the virtual subdural space? J Neurol Neurosurg Psychiatry 47(2):121–127

    Article  Google Scholar 

  • Zhou Z, Li X, Kleiven S (2018) Biomechanics of acute subdural hematoma in the elderly: a fluid-structure interaction study. J Neurotrauma 36(13):2099–2108

    Article  Google Scholar 

Download references

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

Author information

Authors and Affiliations

  1. Biomechanics Section, KU Leuven, Celestijnenlaan 300 box 2419, 3001, Leuven, Belgium

    Markos Kapeliotis, Rebeca Alejandra Gavrila Laic, Alvaro Jorge Peñas, Jos Vander Sloten & Nele Famaey

  2. Department of Neurosurgery, University Hospital Gasthuisberg, KU Leuven, Leuven, Belgium

    Bart Depreitere

  3. Laboratory of Enteric Neuroscience (LENS), TARGID, KU Leuven, Leuven, Belgium

    Pieter Vanden Berghe

Authors
  1. Markos Kapeliotis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rebeca Alejandra Gavrila Laic
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alvaro Jorge Peñas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jos Vander Sloten
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pieter Vanden Berghe
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nele Famaey
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bart Depreitere
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Markos Kapeliotis.

Ethics declarations

Conflict of interest

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

Appendix

Appendix

1.1 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.

1.2 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
Full size table
Table 3 Summary table of the fibre orientation analysis—4 blocks of equal scan length, 0% strain
Full size table
Table 4 Summary table of the fibre orientation analysis—4 blocks of equal scan length, 50% strain
Full size table
Fig. 16
figure 16

Sample 3 (frontal, right, \(\varnothing\) 3.2mm, WT:112 μm). Fibre orientation colour maps (top: no strain, bottom: 50% strain)

Full size image
Fig. 17
figure 17

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

Full size image
Fig. 18
figure 18

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

Full size image
Fig. 19
figure 19

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

Full size image
Fig. 20
figure 20

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

Full size image
Fig. 21
figure 21

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

Full size image
Fig. 22
figure 22

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

Full size image
Fig. 23
figure 23

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

Full size image
Fig. 24
figure 24

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

Full size image
Fig. 25
figure 25

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

Full size image
Fig. 26
figure 26

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

Full size image
Fig. 27
figure 27

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

Full size image
Fig. 28
figure 28

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

Full size image
Fig. 29
figure 29

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

Full size image
Fig. 30
figure 30

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

Full size image
Fig. 31
figure 31

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

Full size image
Fig. 32
figure 32

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

Full size image
Fig. 33
figure 33

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

Full size image
Fig. 34
figure 34

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

Full size image
Fig. 35
figure 35

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

Full size image
Fig. 36
figure 36

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

Full size image
Fig. 37
figure 37

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

Full size image
Fig. 38
figure 38

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

Full size image
Fig. 39
figure 39

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

Full size image
Fig. 40
figure 40

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

Full size image
Fig. 41
figure 41

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

Full size image
Fig. 42
figure 42

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

Full size image
Fig. 43
figure 43

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

Full size image
Fig. 44
figure 44

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

Full size image
Fig. 45
figure 45

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

Full size image
Fig. 46
figure 46

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

Full size image
Fig. 47
figure 47

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

Full size image
Fig. 48
figure 48

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

Full size image
Fig. 49
figure 49

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)

Full size image
Fig. 50
figure 50

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)

Full size image
Fig. 51
figure 51

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)

Full size image

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kapeliotis, M., Gavrila Laic, R.A., Peñas, A.J. et al. Collagen fibre orientation in human bridging veins. Biomech Model Mechanobiol 19, 2455–2489 (2020). https://doi.org/10.1007/s10237-020-01349-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-020-01349-w

Keywords

Search

Navigation