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Am J Physiol Heart Circ Physiol 296: H2015-H2021, 2009. First published March 27, 2009; doi:10.1152/ajpheart.00418.2008
0363-6135/09 $8.00
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Venomotion modulates lymphatic pumping in the bat wing

Ranjeet M. Dongaonkar,1 Randolph H. Stewart,1 Glen A. Laine,1 Michael J. Davis,2 David C. Zawieja,3 and Christopher M. Quick1

1Michael E. DeBakey Institute, Texas A&M University and 3Division of Lymphatic Biology, Cardiovascular Research Institute, Texas A&M Health, Science Center, College Station, Texas; and 2Medical Pharmacology and Physiology, University of Missouri School of Medicine, Columbia, Missouri

Submitted 12 April 2008 ; accepted in final form 24 March 2009

In skin, it is believed that lymph must be pumped by intrinsic contraction of lymphatic muscle, since investigators have not considered that cyclical dilation of venules could compress adjacent lymphatic microvessels. Because lymphatic vessels are sensitive to stretch, we hypothesized that venomotion not only can cause extrinsic pumping of lymph in nearby lymphatic vessels, but also can stimulate intrinsic contractions. Bat wing venules have pronounced venomotion and are in close proximity to lymphatic microvessels, and can be studied noninvasively without the confounding effects of anesthesia, surgical trauma, or contrast agents. Therefore, the interaction between venules and their paired lymphatic vessels in unanesthetized Pallid bats (n = 8) was evaluated by recording the diameters of both vessels. Four sets of observations suggested that lymphatic and venous contractions were partially coupled. First, venous dilation and contraction produced a significant change in lymphatic microvascular cross-sectional area. Second, lymphatic microvascular contractions were immediately preceded by a change in venular diameter. Third, venular and lymphatic vessel contraction frequencies were positively correlated (r = 0.75). Fourth, time delays between peak venular systole and onset of lymphatic microvascular contraction were negatively correlated with venomotion magnitude (r = –0.55) and velocity (r = –0.64). In a separate experiment, inhibiting venomotion resulted in a 54.3 ± 20.0% (n = 8) decrease in lymphatic contraction frequency. Furthermore, 85.7% (n = 56) of lymphatic vessels switch sides and lie adjacent to arterioles when venules were too small to exhibit venomotion. These results are consistent with both extrinsic pumping of lymph and stretch-induced lymphatic contraction and imply that intrinsic and extrinsic pumping can be coupled.

lymphangion; edema; interstitial fluid balance; venular-lymphatic coupling



Address for reprint requests and other correspondence: C. M. Quick, Michael E. DeBakey Institute, TAMU 4466, Texas A&M Univ., College Station, TX 77843-4466 (e-mail: cquick{at}tamu.edu)







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