A perpetual switching system in pulmonary capillaries

Author:

Wagner Wiltz W.123,Jaryszak Eric M.2,Peterson Amanda J.1,Doerschuk Claire M.4,Bohlen H. Glenn2,King Judy A. C.3,Tanner Judith A.2,Crockett Edward S.3,Glenny Robb W.5,Presson Robert G.1

Affiliation:

1. Department of Anesthesiology, Indiana University School of Medicine, Indianapolis, Indiana

2. Department of Cellular and Integrative Physiology, Indiana University School of Medicine, Indianapolis, Indiana

3. Department of Molecular and Cellular Pharmacology, Department of Physiology and Cell Biology, Center for Lung Biology, University of South Alabama, Mobile, Alabama

4. Center for Airways Disease, Department of Medicine, University of North Carolina, Chapel Hill, North Carolina

5. Departments of Medicine and of Physiology and Biophysics, University of Washington, Seattle, Washington

Abstract

Of the 300 billion capillaries in the human lung, a small fraction meet normal oxygen requirements at rest, with the remainder forming a large reserve. The maximum oxygen demands of the acute stress response require that the reserve capillaries are rapidly recruited. To remain primed for emergencies, the normal cardiac output must be parceled throughout the capillary bed to maintain low opening pressures. The flow-distributing system requires complex switching. Because the pulmonary microcirculation contains contractile machinery, one hypothesis posits an active switching system. The opposing hypothesis is based on passive switching that requires no regulation. Both hypotheses were tested ex vivo in canine lung lobes. The lobes were perfused first with autologous blood, and capillary switching patterns were recorded by videomicroscopy. Next, the vasculature of the lobes was saline flushed, fixed by glutaraldehyde perfusion, flushed again, and then reperfused with the original, unfixed blood. Flow patterns through the same capillaries were recorded again. The 16-min-long videos were divided into 4-s increments. Each capillary segment was recorded as being perfused if at least one red blood cell crossed the entire segment. Otherwise it was recorded as unperfused. These binary measurements were made manually for each segment during every 4 s throughout the 16-min recordings of the fresh and fixed capillaries (>60,000 measurements). Unexpectedly, the switching patterns did not change after fixation. We conclude that the pulmonary capillaries can remain primed for emergencies without requiring regulation: no detectors, no feedback loops, and no effectors—a rare system in biology. NEW & NOTEWORTHY The fluctuating flow patterns of red blood cells within the pulmonary capillary networks have been assumed to be actively controlled within the pulmonary microcirculation. Here we show that the capillary flow switching patterns in the same network are the same whether the lungs are fresh or fixed. This unexpected observation can be successfully explained by a new model of pulmonary capillary flow based on chaos theory and fractal mathematics.

Funder

HHS | NIH | National Heart, Lung, and Blood Institute (NHBLI)

Publisher

American Physiological Society

Subject

Physiology (medical),Physiology

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