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Human lower leg muscle pump acts like a stream diversion pump during locomotion

Tauraginskii, R. A.; Lurie, F.; Simakov, S.; Agalarov, R.; Khramtsov, P.; Babushkin, M.; Borsuk, D.; Galchenko, M.

2023-09-28 physiology
10.1101/2023.09.25.559436 bioRxiv
Show abstract

BackgroundCalf muscle pump (CMP) failure is associated with the development and progression of chronic venous insufficiency as characterized by ambulatory venous hypertension (AVH). However, the explicit interconnection between AVH with CMP failure remains uncertain because the concept of CMP function is controversial. The study aimed to measure pressure in different segments of the great saphenous vein (GSV) and intramuscular vein of the gastrocnemius (GCM) during exercise. MethodsTwelve legs of nine healthy volunteers were enrolled in the study. Continuous pressure (IVCALF, GSV at ankle, proximal calf, and mid-distal thigh) and electromyography data (GCM and anterior tibial muscle [ATM]) were recorded during treadmill walking, running, and plantar flexion exercises. The pressure gradient (PG, mmHg) between adjacent points of measurement was calculated. Minute unit power of muscle pump ejection and suction ([Formula], and [Formula], MPa/min) were calculated and compared with the arterial blood supply of the lower extremity (LBF, L/min). ResultsPG demonstrated a consistent pattern of changes during walking and running. An absence of PG directed from the calf to the thigh (centripetal) in the GSV was observed. Instead, a retrograde PG was verified throughout the entire stride cycle. Its value decreased with the increase in stride cycle frequency. The dynamics of PG between the IV and GSV were the following: It was directed from the IV to GSV during GCM contraction and was reversed during ATM contraction and GCM relaxation (swing phase). LBF, [Formula], and [Formula] demonstrated similar exponential growth with the increase in stride frequency during walking and running. ConclusionsThe pressure gradient in the GSV prevents centripetal flow during locomotion. Instead, PG directs blood flow from the GSV toward intramuscular veins. The increase in CMP unit power was tightly coupled with lower extremity arterial blood supply growth that prevented ambulatory venous pressure rise during exercise. Novelty and Significance What Is Known?O_LIThe existence of a pressure gradient in superficial veins directed centripetally (from calf to thigh level) has been confirmed for the state of rest only (lying and standing). C_LIO_LIThe existence of a pressure gradient directed from intramuscular to superficial veins or vice versa has been confirmed for the artificial exercise tests only (tiptoe movements, walking in place etc.). C_LIO_LIThe main calf muscle pump function was considered as its ability to eject blood centripetally by posterior calf muscle group contraction. C_LI What New Information Does This Article Contribute?O_LIAn absence of pressure gradient directed from the calf to the thigh (centripetal) in the great the saphenous vein during locomotion. C_LIO_LIDuring locomotion, at the lower leg level, the primary route of blood outflow from the superficial veinous network toward intramuscular veins is a horizontal route (through perforating veins). C_LIO_LINew parameters are introduced to assess calf muscle pump effectiveness as its ability to maintain accordance between the muscle pump output and arterial blood supply during locomotion. C_LI The calf muscle pump (CMP) is known as a significant contributor to venous blood outflow from the lower extremity due to its ability to effectively eject blood in a centripetal direction. Therefore, CMP failure refers to an impaired ejecting ability associated with chronic venous insufficiency (CVI) occurrence and progression. It is expressed in the increase in ambulatory venous pressure referred to as ambulatory venous hypertension (AVH). However, multiple studies demonstrated a lack of agreement between defined CMP failure and AVH, the severity of CVI, and quality of life. Here we show that during locomotion, the CMP acts as a stream diversion pump redirecting blood flow from superficial veins (SVs) to intramuscular veins (IVs) through perforating veins. This is because the observed pressure gradient prevents centripetal blood flow from the calf to thigh level in the SVs and favors blood flow from SVs to IVs during the swing phase of the stride cycle. This function is provided by the synergetic work of antagonist calf muscles (anterior tibial muscle and gastrocnemius). Thereby, the CMP prevents pressure growth in the superficial veins of the lower leg (AVH) during exercise when the arterial blood supply increases according to exercise intensity.

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