Vascular microforamina and endocranial surface: Normal variation and distribution in adult humans: Vascular biology.
craniovascular traits
diploic veins
endocranial vessels
neuroinflammation
thermal regulation
vascular system
Journal
Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775
Informations de publication
Date de publication:
11 Mar 2024
11 Mar 2024
Historique:
revised:
20
02
2024
received:
11
12
2023
accepted:
26
02
2024
medline:
11
3
2024
pubmed:
11
3
2024
entrez:
11
3
2024
Statut:
aheadofprint
Résumé
The term craniovascular traits refers to the imprints left by arteries and veins on the skull bones. These features can be used in biological anthropology and archaeology to investigate the morphology of the vascular network in extinct species and past populations. Generally, the term refers to macrovascular features of the endocranial cavity, like those associated with the middle meningeal artery, venous sinuses, emissary foramina, and diploic channels. However, small vascular passages (here called microforamina or microchannels) have been occasionally described on the endocranial surface. The larger ones (generally with a diameter between 0.5 and 2.0 mm) can be detected through medical scanners on osteological collections. In this study, we describe and quantify the number and distribution of these microforamina in adult humans (N = 45) and, preliminarily, in a small sample of children (N = 7). Adults display more microchannels than juvenile skulls. A higher frequency in females is also observed, although this result is not statistically significant and might be associated with allometric cranial variations. The distribution of the microforamina is particularly concentrated on the top of the vault, in particular along the sagittal, metopic, and coronal sutures, matching the course of major venous sinuses and parasagittal bridging veins. Nonetheless, the density is lower in the region posterior to bregma. Beyond oxygenation, these vessels are likely involved in endocranial thermal regulation, infection, inflammation, and immune responses, and their distribution and prevalence can hence be of interest in human biology, evolutionary anthropology, and medicine.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Ministerio de Ciencia e Innovación
ID : PID2021-122355NB-C33
Organisme : Istituto Italiano di Antropologia
Organisme : Ministerstvo Kultury
Organisme : Ministry of Culture of the Czech Republic
ID : DKRVO 2024-2028/7.I.a, 00023272
Informations de copyright
© 2024 American Association for Anatomy.
Références
Adeeb, N., Mortazavi, M. M., Deep, A., Griessenauer, C. J., Watanabe, K., Shoja, M. M., Loukas, M., & Tubbs, R. S. (2013). The pia mater: A comprehensive review of literature. Child's Nervous System, 29(10), 1803-1810. https://doi.org/10.1007/s00381-013-2044-5
Adeeb, N., Mortazavi, M. M., Tubbs, R. S., & Cohen-Gadol, A. A. (2012). The cranial dura mater: A review of its history, embryology, and anatomy. Child's Nervous System, 28(6), 827-837. https://doi.org/10.1007/s00381-012-1744-6
Barberini, F., Bruner, E., Cartolari, R., Franchitto, G., Heyn, R., Ricci, F., & Manzi, G. (2008). An unusually-wide human bregmatic Wormian bone: Anatomy, tomographic description, and possible significance. Surgical and Radiologic Anatomy, 30(8), 683-687. https://doi.org/10.1007/s00276-008-0371-0
Bertolizio, G., Mason, L., & Bissonnette, B. (2011). Brain temperature: Heat production, elimination and clinical relevance. Paediatric Anaesthesia, 21(4), 347-358. https://doi.org/10.1111/j.1460-9592.2011.03542.x
Borovanský, L. (1936). Pohlavní rozdíly na lebce člověka. Česká akademie věd a umění.
Boyd, G. I. (1930). The emissary foramina of the cranium in man and the anthropoids. Journal of Anatomy, 65(Pt 1), 108-121.
Bruner, E., de la Cuétara, J. M., Masters, M., Amano, H., & Ogihara, N. (2014). Functional craniology and brain evolution: From paleontology to biomedicine. Frontiers in Neuroanatomy, 8, 1-15. https://doi.org/10.3389/fnana.2014.00019
Bruner, E., De La Cuétara, J. M., & Musso, F. (2012). Quantifying patterns of endocranial heat distribution: Brain geometry and thermoregulation. American Journal of Human Biology, 24(6), 753-762. https://doi.org/10.1002/ajhb.22312
Bruner, E., Mantini, S., Musso, F., De La Cuétara, J. M., Ripani, M., & Sherkat, S. (2011). The evolution of the meningeal vascular system in the human genus: From brain shape to thermoregulation. American Journal of Human Biology, 23(1), 35-43. https://doi.org/10.1002/ajhb.21123
Bruner, E., Píšová, H., Martín-Francés, L., Martinón-Torres, M., Arsuaga, J. L., Carbonell, E., & Bermúdez de Castro, J. M. (2017). A human parietal fragment from the late early Pleistocene gran dolina-TD6 cave site, Sierra de Atapuerca, Spain. Comptes Rendus Palevol, 16(1), 71-81. https://doi.org/10.1016/j.crpv.2016.02.002
Bruner, E., & Sherkat, S. (2008). The middle meningeal artery: From clinics to fossils. Child's Nervous System, 24(11), 1289-1298. https://doi.org/10.1007/s00381-008-0685-6
Eisová, S., Píšová, H., Velemínský, P., & Bruner, E. (2019). Normal craniovascular variation in two modern European adult populations. Journal of Anatomy, 235(4), 765-782. https://doi.org/10.1111/joa.13019
Eisová, S., Rangel de Lázaro, G., Píšová, H., Pereira-Pedro, S., & Bruner, E. (2016). Parietal bone thickness and vascular diameters in adult modern humans: A survey on cranial remains. Anatomical Record, 299(7), 888-896. https://doi.org/10.1002/ar.23348
Falk, D. (1986). Evolution of cranial blood drainage in hominids: Enlarged occipital/marginal sinuses and emissary foramina. American Journal of Physical Anthropology, 70(3), 311-324. https://doi.org/10.1002/ajpa.1330700306
Falk, D. (1990). Brain evolution in Homo: The “radiator” theory. Behavioral and Brain Sciences, 13(2), 333-344. https://doi.org/10.1017/S0140525X00078973
Falk, D. (1993). Meningeal arterial patterns in great apes: Implications for hominid vascular evolution. American Journal of Physical Anthropology, 92(1), 81-97. https://doi.org/10.1002/ajpa.1330920107
Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). Past: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 9.
Herisson, F., Frodermann, V., Courties, G., Rohde, D., Sun, Y., Vandoorne, K., Wojtkiewicz, G. R., Masson, G. S., Vinegoni, C., Kim, J., Kim, D.-E., Weissleder, R., Swirski, F. K., Moskowitz, M. A., & Nahrendorf, M. (2018). Direct vascular channels connect skull bone marrow and the brain surface enabling myeloid cell migration. Nature Neuroscience, 21(9), 1209-1217. https://doi.org/10.1038/s41593-018-0213-2
Hui, J., & Balzeau, A. (2023a). The diploic venous system in Homo neanderthalensis and fossil Homo sapiens: A study using high-resolution computed tomography. American Journal of Biological Anthropology, 182(3), 412-427. https://doi.org/10.1002/ajpa.24843
Hui, J., & Balzeau, A. (2023b). Investigating the relationship between cranial bone thickness and diploic channels: A first comparison between fossil Homo sapiens and Homo neanderthalensis. Anatomical Record. https://doi.org/10.1002/ar.25360
Kimbel, W. H. (1984). Variation in the pattern of cranial venous sinuses and hominid phylogeny. American Journal of Physical Anthropology, 63(3), 243-246. https://doi.org/10.1002/ajpa.1330630302
Lin, E., & Alessio, A. (2009). What are the basic concepts of temporal, contrast, and spatial resolution in cardiac CT? Journal of Cardiovascular Computed Tomography, 3(6), 403-408. https://doi.org/10.1016/j.jcct.2009.07.003
Linninger, A. A., Xenos, M., Sweetman, B., Ponkshe, S., Guo, X., & Penn, R. (2009). A mathematical model of blood, cerebrospinal fluid and brain dynamics. Journal of Mathematical Biology, 59, 729-759. https://doi.org/10.1007/s00285-009-0250-2
Mitteroecker, P., & Gunz, P. (2009). Advances in geometric morphometrics. Evolutionary Biology, 36(2), 235-247. https://doi.org/10.1007/s11692-009-9055-x
Mortazavi, M. M., Denning, M., Yalcin, B., Shoja, M. M., Loukas, M., & Tubbs, R. S. (2013). The intracranial bridging veins: A comprehensive review of their history, anatomy, histology, pathology, and neurosurgical implications. Child's Nervous System, 29(7), 1073-1078. https://doi.org/10.1007/s00381-013-2054-3
Pachner, P. (1937). Pohlavní rozdíly na lidské pánvi. Česká akademie věd a umění.
Patel, N. (2009). Venous anatomy and imaging of the first centimeter. Seminars in Ultrasound, CT and MRI, 30(6), 513-524. https://doi.org/10.1053/j.sult.2009.08.003
Píšová, H., Rangel de Lázaro, G., Velemínský, P., & Bruner, E. (2017). Craniovascular traits in anthropology and evolution: From bones to vessels. Journal of Anthropological Sciences, 95, 35-65. https://doi.org/10.4436/jass.95003
Pulous, F. E., Cruz-Hernández, J. C., Yang, C., Kaya, Ζ., Paccalet, A., Wojtkiewicz, G., Capen, D., Brown, D., Wu, J. W., Schloss, M. J., Vinegoni, C., Richter, D., Yamazoe, M., Hulsmans, M., Momin, N., Grune, J., Rohde, D., McAlpine, C. S., Panizzi, P., … Nahrendorf, M. (2022). Cerebrospinal fluid can exit into the skull bone marrow and instruct cranial hematopoiesis in mice with bacterial meningitis. Nature Neuroscience, 25(5), 567-576. https://doi.org/10.1038/s41593-022-01060-2
Rangel de Lázaro, G., De La Cuétara, J. M., Píšová, H., Lorenzo, C., & Bruner, E. (2016). Diploic vessels and computed tomography: Segmentation and comparison in modern humans and fossil hominids. American Journal of Physical Anthropology, 159(2), 313-324. https://doi.org/10.1002/ajpa.22878
Rangel de Lázaro, G., Eisová, S., Píšová, H., & Bruner, E. (2018). The endocranial vascular system: Tracing vessels. In E. Bruner, N. Ogihara, & H. Tanabe (Eds.), Digital endocasts (pp. 71-91). Springer. https://doi.org/10.1007/978-4-431-56582-6_6
Rangel de Lázaro, G., Neubauer, S., Gunz, P., & Bruner, E. (2020). Ontogenetic changes of diploic channels in modern humans. American Journal of Physical Anthropology, 173(1), 96-111. https://doi.org/10.1002/ajpa.24085
Scremin, O. U. (2004). Cerebral vascular system. In G. Paxinos & J. K. Mai (Eds.), The human nervous system (pp. 1325-1348). Elsevier Academic Press.
Slice, D. E. (2007). Geometric morphometrics. Annual Review of Anthropology, 36(1), 261-281. https://doi.org/10.1146/annurev.anthro.34.081804.120613
Slice, D. E. (2013). Morpheus et al (Java ed.). Department of Scientific Computing, The Florida State University.
Smyth, L. C., Xu, D., Okar, S. V., Dykstra, T., Rustenhoven, J., et al. (2024). Identification of direct connections between the dura and the brain. Nature, 627,165-173. https://doi.org/10.1038/s41586-023-06993-7
Toriumi, H., Shimizu, T., Shibata, M., Unekawa, M., Tomita, Y., Tomita, M., & Suzuki, N. (2011). Developmental and circulatory profile of the diploic veins. Microvascular Research, 81(1), 97-102. https://doi.org/10.1016/j.mvr.2010.11.004
Tsutsumi, S., Nakamura, M., Tabuchi, T., Yasumoto, Y., & Ito, M. (2013). Calvarial diploic venous channels: An anatomic study using high-resolution magnetic resonance imaging. Surgical and Radiologic Anatomy, 35(10), 935-941. https://doi.org/10.1007/s00276-013-1123-3
Wang, H., Kim, M., Normoyle, K. P., & Llano, D. (2016). Thermal regulation of the brain-An anatomical and physiological review for clinical neuroscientists. Frontiers in Neuroscience, 9, 528. https://doi.org/10.3389/fnins.2015.00528
Zelditch, M., Swiderski, D., & Sheets, H. D. (2012). Geometric morphometrics for biologists: A primer. Academic Press.
Zenker, W., & Kubik, S. (1996). Brain cooling in humans - anatomical considerations. Anatomy and Embryology, 193(1), 1-13. https://doi.org/10.1007/BF00186829
Zhao, W., & Ji, S. (2020). Incorporation of vasculature in a head injury model lowers local mechanical strains in dynamic impact. Journal of Biomechanics, 104, 109732. https://doi.org/10.1016/j.jbiomech.2020.109732