CLC number:
On-line Access: 2021-08-20
Received: 2020-09-26
Revision Accepted: 2021-02-14
Crosschecked: 0000-00-00
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Citations: Bibtex RefMan EndNote GB/T7714
Hongyi LI, You LYU, Xiaoliang CHEN, Bei LI, Qi HUA, Fusui JI, Yajun YIN, Hua LI. Layers of interstitial fluid flow along a “slit-shaped” vascular adventitia[J]. Journal of Zhejiang University Science B, 2021, 22(8): 647-663.
@article{title="Layers of interstitial fluid flow along a “slit-shaped” vascular adventitia",
author="Hongyi LI, You LYU, Xiaoliang CHEN, Bei LI, Qi HUA, Fusui JI, Yajun YIN, Hua LI",
journal="Journal of Zhejiang University Science B",
volume="22",
number="8",
pages="647-663",
year="2021",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B2000590"
}
%0 Journal Article
%T Layers of interstitial fluid flow along a “slit-shaped” vascular adventitia
%A Hongyi LI
%A You LYU
%A Xiaoliang CHEN
%A Bei LI
%A Qi HUA
%A Fusui JI
%A Yajun YIN
%A Hua LI
%J Journal of Zhejiang University SCIENCE B
%V 22
%N 8
%P 647-663
%@ 1673-1581
%D 2021
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B2000590
TY - JOUR
T1 - Layers of interstitial fluid flow along a “slit-shaped” vascular adventitia
A1 - Hongyi LI
A1 - You LYU
A1 - Xiaoliang CHEN
A1 - Bei LI
A1 - Qi HUA
A1 - Fusui JI
A1 - Yajun YIN
A1 - Hua LI
J0 - Journal of Zhejiang University Science B
VL - 22
IS - 8
SP - 647
EP - 663
%@ 1673-1581
Y1 - 2021
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B2000590
Abstract: interstitial fluid (ISF) flow through vascular adventitia has been discovered recently. However, its kinetic pattern was unclear. We used histological and topographical identification to observe ISF flow along venous vessels in rabbits. By magnetic resonance imaging (MRI) in live subjects, the inherent pathways of ISF flow from the ankle dermis through the legs, abdomen, and thorax were enhanced by paramagnetic contrast. By fluorescence stereomicroscopy and layer-by-layer dissection after the rabbits were sacrificed, the perivascular and adventitial connective tissues (PACTs) along the saphenous veins and inferior vena cava were found to be stained by sodium fluorescein from the ankle dermis, which coincided with the findings by MRI. The direction of ISF transport in a venous PACT pathway was the same as that of venous blood flow. By confocal microscopy and histological analysis, the stained PACT pathways were verified to be the fibrous connective tissues, consisting of longitudinally assembled fibers. Real-time observations by fluorescence stereomicroscopy revealed at least two types of spaces for ISF flow: one along adventitial fibers and another one between the vascular adventitia and its covering fascia. Using nanoparticles and surfactants, a PACT pathway was found to be accessible by a nanoparticle of <100 nm and contained two parts: a transport channel and an absorptive part. The calculated velocity of continuous ISF flow along fibers of the PACT pathway was 3.6‒15.6 mm/s. These data revealed that a PACT pathway was a“slit-shaped”porous biomaterial, comprising a longitudinal transport channel and an absorptive part for imbibition. The use of surfactants suggested that interfacial tension might play an essential role in layers of continuous ISF flow along vascular vessels. A hypothetical “gel pump” is proposed based on interfacial tension and interactions to regulate ISF flow. These experimental findings may inspire future studies to explore the physiological and pathophysiological functions of vascular ISF or interfacial fluid flow among interstitial connective tissues throughout the body.
[1]AuklandK, ReedRK, 1993. Interstitial-lymphatic mechanisms in the control of extracellular fluid volume. Physiol Rev, 73(1):1-78.
[2]CenajO, AllisonDHR, ImamR, et al., 2021. Evidence for continuity of interstitial spaces across tissue and organ boundaries in humans. Commun Biol, 4:436.
[3]ChenX, CaoGX, HanAJ, et al., 2008. Nanoscale fluid transport: size and rate effects. Nano Lett, 8(9):2988-2992.
[4]HallJE, GuytonAC, 2011. The microcirculation and lymphatic system. In: Guyton and Hall Textbook of Medical Physiology, 12th Ed. Saunders, Philadelphia, p.180-182.
[5]HolmbergK, JönssonB, KronbergB, et al., 2003. Surfactants and Polymers in Aqueous Solution, 2nd Ed. John Wiley & Sons, Chichester, UK, p.139-155.
[6]HolmesMC, 1998. Intermediate phases of surfactant-water mixtures. Curr Opin Colloid Interface Sci, 3(5):485-492.
[7]IliffJJ, WangMH, LiaoYH, et al., 2012. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med, 4(147):147ra111.
[8]KhanA, 1996. Phase science of surfactants. Curr Opin Colloid Interface Sci, 1(5):614-623.
[9]LevickJR, 1987. Flow through interstitium and other fibrous matrices. Q J Exp Physiol, 72(4):409-437.
[10]LiHY, ChenM, YangJF, et al., 2012. Fluid flow along venous adventitia in rabbits: is it a potential drainage system complementary to vascular circulations? PLoS ONE, 7(7):e41395.
[11]LiHY, YangCQ, LuKY, et al., 2016. A long-distance fluid transport pathway within fibrous connective tissues in patients with ankle edema. Clin Hemorheol Microcirc, 63(4):411-421.
[12]LiHY, HanD, LiH, et al., 2017. A biotic interfacial fluid transport phenomenon in the meshwork of fibrous connective tissues over the whole body. Prog Physiol Sci, 48(2):81-87 (in Chinese).
[13]LiHY, YangCQ, YinYJ, et al., 2019. An extravascular fluid transport system based on structural framework of fibrous connective tissues in human body. Cell Prolif, 52(5):e12667.
[14]LiHY, YinYJ, YangCQ, et al., 2020. Active interfacial dynamic transport of fluid in a network of fibrous connective tissues throughout the whole body. Cell Prolif, 53(2):e12760.
[15]PanH, WangBH, LiZB, et al., 2019. Mitochondrial superoxide anions induced by exogenous oxidative stress determine tumor cell fate: an individual cell-based study. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 20(4):310-321.
[16]QianM, NiuLL, WangYP, et al., 2010. Measurement of flow velocity fields in small vessel-mimic phantoms and vessels of small animals using micro ultrasonic particle image velocimetry (micro-EPIV). Phys Med Biol, 55(20):6069-6088.
[17]RennelsML, GregoryTF, BlaumanisOR, et al., 1985. Evidence for a ‘Paravascular’ fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space. Brain Res, 326(1):47-63.
[18]TokunagaTK, WanJM, 1997. Water film flow along fracture surfaces of porous rock. Water Resour Res, 33(6):1287-1295.
[19]TullerM, OrD, DudleyLM, 1999. Adsorption and capillary condensation in porous media: liquid retention and interfacial configurations in angular pores. Water Resour Res, 35(7):1949-1964.
[20]van OssCJ, 2007. Development and applications of the interfacial tension between water and organic or biological surfaces. Colloids Surf B: Biointerfaces, 54(1):2-9.
[21]WhitbyM, CagnonL, ThanouM, et al., 2008. Enhanced fluid flow through nanoscale carbon pipes. Nano Lett, 8(9):2632-2637.
[22]WiigH, RubinK, ReedRK, 2003. New and active role of the interstitium in control of interstitial fluid pressure: potential therapeutic consequences. Acta Anaesthesiol Scand, 47(2):111-121.
[23]WiigH, GyengeCC, TenstadO, 2005. The interstitial distribution of macromolecules in rat tumours is influenced by the negatively charged matrix components. J Physiol, 567(2):557-567.
[24]ZiemysA, KojicM, MilosevicM, et al., 2012. Interfacial effects on nanoconfined diffusive mass transport regimes. Phys Rev Lett, 108(23):236102.
[25]ZhuY, ZhangQ, ShiX, et al., 2019. Hierarchical hydrogel composite interfaces with robust mechanical properties for biomedical applications. Adv Mater, 31(45):1804950.
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