Lymphangion coordination minimally affects mean flow in lymphatic vessels

Venugopal, Arun M.; Stewart, Randolph H.; Laine, Glen A.; Dongaonkar, Ranjeet M.; Quick, Christopher M.

doi:10.1152/ajpheart.01340.2006

Cited by 52 publications

(75 citation statements)

References 30 publications

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“…After washout from NE-KPSS to PSS, the vessels were allowed to rest for a minimum of 3 min before stretching to a new internal circumference. For data analysis, the diameter value for each duct where peak active tension was observed was ascribed as L 0 and the corresponding values expressed in relationship to it (L/L 0) (42). Second and third polynomial and exponential regression fit were applied for the total, active, and passive tension curves for each ring segment.…”

Section: Methodsmentioning

confidence: 99%

“…To maintain pumping and prevent overdistension, the LSMCs must be able to adapt their ability to propel fluid over a wide range of pressures and vessel diameters. In analogy with the heart, increased preload in animal lymphatic vessels has been observed to increase stroke volume and developed pressure (4,20,28,42).The active force produced by smooth muscle cells is directly related to how much they are stretched: this information is provided by the length-tension relationship for the specific cells of interest. Although the passive and active mechanical properties of LSMCs from animal collecting lymphatics have been reported (9, 45), there are no corresponding biomechanical data from human vessels.…”

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Human thoracic duct in vitro: diameter-tension properties, spontaneous and evoked contractile activity

Telinius

Drewsen

Pilegaard

et al. 2010

American Journal of Physiology-Heart and Circulatory Physiology

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The current study characterizes the mechanical properties of the human thoracic duct and demonstrates a role for adrenoceptors, thromboxane, and endothelin receptors in human lymph vessel function. With ethical permission and informed consent, portions of the thoracic duct (2-5 cm) were resected and retrieved at T7-T9 during esophageal and cardia cancer surgery. Ring segments (2 mm long) were mounted in a myograph for isometric tension (N/m) measurement. The diameter-tension relationship was established using ducts from 10 individuals. Peak active tension of 6.24 Ϯ 0.75 N/m was observed with a corresponding passive tension of 3.11 Ϯ 0.67 N/m and average internal diameter of 2.21 mm. The equivalent active and passive transmural pressures by LaPlace's law were 47.3 Ϯ 4.7 and 20.6 Ϯ 3.2 mmHg, respectively. Subsequently, pharmacology was performed on rings from 15 ducts that were normalized by stretching them until an equivalent pressure of 21 mmHg was calculable from the wall tension. At low concentrations, norepinephrine, endothelin-1, and the thromboxane-A2 analog U-46619 evoked phasic contractions (analogous to lymphatic pumping), whereas at higher contractions they induced tonic activity (maximum tension values of 4.46 Ϯ 0.63, 5.90 Ϯ 1.4, and 6.78 Ϯ 1.4 N/m, respectively). Spontaneous activity was observed in 44% of ducts while 51% of all the segments produced phasic contractions after agonist application. Acetylcholine and bradykinin relaxed norepinephrine preconstrictions by ϳ20% and ϳ40%, respectively. These results demonstrate that the human thoracic duct can develop wall tensions that permit contractility to be maintained across a wide range of transmural pressures and that isolated ducts contract in response to important vasoactive agents. lymphatic system; lymph pump; lymphangion; lymphatic smooth muscle THE EXCESS FLUID AND PROTEIN of the interstitial spaces in almost all tissues of the body are collected and removed by the lymphatic system. The lymphatic capillaries converge into larger collecting lymphatics, and, ultimately, these terminate into large transport vessels, which return lymph to the blood circulation. The lymphatic system lacks a central pump to drive the transport of lymph. Instead, it is generally accepted that the lymphatic smooth muscle cells (LSMCs) in the collecting and transporting lymphatic vessel wall are responsible for propelling lymph forward by intrinsic contractions. The lymphatic vessels responsible for pumping are comprised of multiple contractile segments separated by unidirectional valves to prevent backflow, termed a lymphangion, and each lymphangion performs much like a cardiac ventricle to provide unidirectional pumping. The contractile part of the lymphatic vasculature can thus be likened to a system of ventricles in series (27). The thoracic duct is the largest lymphatic vessel in the human body. Under normal conditions (i.e., in healthy individuals), it is a low-flow system that drains up to 1 ml/min to the venous circulation (30,44). The volume and flow of lymph a...

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Section: Methodsmentioning

confidence: 99%

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confidence: 99%

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Human thoracic duct in vitro: diameter-tension properties, spontaneous and evoked contractile activity

Telinius

Drewsen

Pilegaard

et al. 2010

American Journal of Physiology-Heart and Circulatory Physiology

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“…This analogy has proved to be particularly appropriate, since lymphangions respond to increased preload by increasing developed pressure and stroke work (both of which correspond in a way that is analogous to the FrankStarling effect) (2,23,27,34). However, unlike the heart, lymphatic vessels consist of many of these pumps in series, and the afterload of one lymphangion is coupled to the preload of the next (16).…”

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“…The recurring analogies to both blood vessels and cardiac ventricles were recently leveraged to develop a physics-based mathematical model of a lymphangion (27,34). With the extension of the transmission line equation description of arteries (26,35), the resulting lymphangion model included the effects of lymph inertia and viscosity.…”

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First-order approximation for the pressure-flow relationship of spontaneously contracting lymphangions

Quick¹,

Venugopal²,

Dongaonkar³

et al. 2008

American Journal of Physiology-Heart and Circulatory Physiology

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Quick CM, Venugopal AM, Dongaonkar RM, Laine GA, Stewart RH. First-order approximation for the pressure-flow relationship of spontaneously contracting lymphangions. Am J Physiol Heart Circ Physiol 294: H2144-H2149, 2008. First published March 7, 2008 doi:10.1152/ajpheart.00781.2007.-To return lymph to the great veins of the neck, it must be actively pumped against a pressure gradient. Mean lymph flow in a portion of a lymphatic network has been characterized by an empirical relationship (Pin Ϫ Pout ϭ ϪPp ϩ RLQL), where Pin Ϫ Pout is the axial pressure gradient and QL is mean lymph flow. RL and Pp are empirical parameters characterizing the effective lymphatic resistance and pump pressure, respectively. The relation of these global empirical parameters to the properties of lymphangions, the segments of a lymphatic vessel bounded by valves, has been problematic. Lymphangions have a structure like blood vessels but cyclically contract like cardiac ventricles; they are characterized by a contraction frequency (f ) and the slopes of the enddiastolic pressure-volume relationship [minimum value of resulting elastance (Emin)] and end-systolic pressure-volume relationship [maximum value of resulting elastance (Emax)]. Poiseuille's law provides a first-order approximation relating the pressure-flow relationship to the fundamental properties of a blood vessel. No analogous formula exists for a pumping lymphangion. We therefore derived an algebraic formula predicting lymphangion flow from fundamental physical principles and known lymphangion properties. Quantitative analysis revealed that lymph inertia and resistance to lymph flow are negligible and that lymphangions act like a series of interconnected ventricles. For a single lymphangion, Pp ϭ Pin (Emax Ϫ Emin)/Emin and RL ϭ Emax/f. The formula was tested against a validated, realistic mathematical model of a lymphangion and found to be accurate. Predicted flows were within the range of flows measured in vitro. The present work therefore provides a general solution that makes it possible to relate fundamental lymphangion properties to lymphatic system function. mathematical modeling; edema LYMPHANGIONS ACT as pumps. The function of the lymphatic system is to transport lymph to the great veins of the neck and is necessary for proper interstitial fluid balance (1). Functionally, lymph must be actively pumped against a pressure gradient (18), in contrast with the arterial system where the blood flows from higher pressure arteries to the lower pressure capillaries. Although intestinal motility and skeletal muscle contraction can propel lymph via external compression (19,29), many lymphangions, the sections of a lymphatic vessel between valves (1, 3, 29), can cyclically contract and actively pump lymph when they are engorged (3). Although they are structured like blood vessels and have a discernable tone, lymphangions function like cardiac ventricles (2, 22, 24).Although lymphangion contractility was originally characterized in terms of tone, investigators have used the ventri...

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Multiscale Modelling of Lymphatic Drainage

Roose

Tabor

2012

Multiscale Computer Modeling in Biomechanics and Biomedical Engineering

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In this chapter we will describe the latest developments in the area of lymphatic modelling. The lymphatic system is one of the key elements of the human circulation, serving the dual functions of draining interstitial fluid and returning this to the general blood circulation, together with processing this lymph fluid which is a key component of the body's immune response system. Compared to the main cardiovascular system however, remarkably little modelling has been attempted. At the same time, the distribution of pumping activity (contractile lymphangions coupled with simple valves) throughout the system, passive primary lymphatics and complex lymph nodes combining to form an active network, makes the system a prime candidate for multiscale modelling.

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Lymphangion coordination minimally affects mean flow in lymphatic vessels

Cited by 52 publications

References 30 publications

Human thoracic duct in vitro: diameter-tension properties, spontaneous and evoked contractile activity

Human thoracic duct in vitro: diameter-tension properties, spontaneous and evoked contractile activity

First-order approximation for the pressure-flow relationship of spontaneously contracting lymphangions

Multiscale Modelling of Lymphatic Drainage

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