Skeletal muscle microcirculatory structure and hemodynamics in diabetes

Kindig, Casey A.; Sexton, William L.; Fedde, M. R.; Poole, David C.

doi:10.1016/s0034-5687(97)00122-9

Cited by 91 publications

(104 citation statements)

References 24 publications

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“…Visualization of capillaries with plasma only or of the vessel wall is not possible, thus not allowing determination of capillary diameter. Lineal density of capillaries with moving RBCs (20) was determined by counting the number of capillaries with flowing RBCs that crosses a line perpendicular to the muscle fiber direction during 1 min. Depending on how the capillaries were oriented across the monitor screen, the line perpendicular to the muscle fiber direction varied between 0.6 and 0.9 mm in length.…”

Section: Methodsmentioning

confidence: 99%

“…Kindig et al (20) reported no change in the lineal density of flowing capillaries in skeletal muscle in an insulin-deficient, Type 1 diabetic rat model of ϳ8-wk diabetic condition. However, due to decreased red blood cell (RBC) flux, it was concluded that skeletal muscle O 2 delivery was markedly reduced (20). In the present study, we addressed the question of whether short-term (hours to 2-4 wk) hyperglycemia, without a concomitant insulin deficiency, affects the lineal density of capillaries with flowing RBCs.…”

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confidence: 95%

“…The central importance of a vascular pathology underlying the hyperglycemia-associated poor prognosis is becoming increasingly evident. Characteristics of hyperglycemia-induced vasculopathy include decreased endothelium-dependent vasodilation, increased capillary permeability for large proteins such as albumin, swelling of endothelial cells, decreased capillary dimensions and diameters, and thickening of the basal lamina (5,13,20,23,33,41).The endothelial cell glycocalyx, a 0.2-to 0.5-m matrix lining the luminal surface of all blood vessels, is a significant factor in microvascular regulation by its action on volume and permeability of capillaries (1,17,18,29,39). Recent evidence demonstrated a role of the glycocalyx in models of ischemiareperfusion injury, inflammation, and altered lipoprotein levels (26, 28, 38).…”

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Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells

Zuurbier

Demirci²,

Koeman³

et al. 2005

Journal of Applied Physiology

159

165

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Zuurbier, Coert J., Cihan Demirci, Anneke Koeman, Hans Vink, and Can Ince. Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells. J Appl Physiol 99: [1471][1472][1473][1474][1475][1476] 2005. First published July 14, 2005; doi:10.1152/japplphysiol.00436.2005.-Hyperglycemia is becoming recognized as an important risk factor for microvascular dysfunction. We hypothesized that short-term hyperglycemia, either on the scale of hours or weeks, alters the barrier function and the volume of the endothelial glycocalyx and decreases functional capillary density and deformability of the red blood cells (RBCs). All experiments were performed in anesthetized, mechanically ventilated, C57BL/6 mice that were either normoglycemic, acutely hyperglycemic (25 mM) for 60 min due to infusion of glucose, or hyperglycemic (25 mM) for 2-4 wk (db/db mice). The glycocalyx was probed using 40-kDa Texas red dextran, which is known to permeate the glycocalyx, and 70-kDa FITC dextran, which has impaired access to the glycocalyx in healthy animals. Clearance of the dye from the blood was measured. An orthogonal polarization spectral imaging technique was used to visualize the number of capillaries with flowing RBCs of the dorsal flexor muscle. The data indicate that short-term hyperglycemia causes a rapid decrease of the ability of the glycocalyx to exclude 70-kDa dextran. No change in the vascular permeation of 40-kDa dextran was observed. Glycocalyx volume was not affected by short-term hyperglycemia. In addition, 1 h of hyperglycemia resulted in a 38% decrease of the lineal density of capillaries with flowing RBCs. This decreased lineal density was not observed in the 2-to 4-wk hyperglycemia model. Short-term hyperglycemia was without any effect on the deformablity of the RBCs. The data indicate that the described increased vascular permeability with hyperglycemia can be ascribed to an increased permeability of the glycocalyx, identifying the glycocalyx as a potential early target of hyperglycemia. vascular permeability; diabetes; skeletal muscle; db/db mice HYPERGLYCEMIA, EITHER IN ITS acute form, such as which may occur in hospitalized critically ill patients, or in its chronic form, such as is present in patients with diabetes mellitus, is associated with increased rates of morbidity and mortality and diminished clinical outcome. The central importance of a vascular pathology underlying the hyperglycemia-associated poor prognosis is becoming increasingly evident. Characteristics of hyperglycemia-induced vasculopathy include decreased endothelium-dependent vasodilation, increased capillary permeability for large proteins such as albumin, swelling of endothelial cells, decreased capillary dimensions and diameters, and thickening of the basal lamina (5,13,20,23,33,41).The endothelial cell glycocalyx, a 0.2-to 0.5-m matrix lining the luminal surface of all blood vessels, is a significant factor in microvascular regulation by its action on volum...

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Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 95%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells

Zuurbier

Demirci²,

Koeman³

et al. 2005

Journal of Applied Physiology

159

165

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“…Of these, the rat spinotrapezius muscle possesses the following singular advantages: 1) it can be exteriorized and transilluminated without disruption of the nervous or primary vascular supplies (2,12,28,40); 2) it comprises a mosaic of the three principal fiber types found in mammalian muscle (8); and 3) the oxidative capacity approximates that found in the untrained human quadriceps (8,22). Consequently, it is not surprising that intravital microscopy of the spinotrapezius has been integral to our understanding of muscle microcirculation in health (4,21,23,25,31,37,39) and chronic diseases such as heart failure (15), Type 1 diabetes (18), and hypertension (13).…”

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confidence: 99%

Downhill running: a model of exercise hyperemia in the rat spinotrapezius muscle

Kano

Padilla

Hageman

et al. 2004

Journal of Applied Physiology

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I. Musch. Downhill running: a model of exercise hyperemia in the rat spinotrapezius muscle. J Appl Physiol 97: 1138 -1142. First published May 7, 2004 10.1152/japplphysiol. 00334.2004.-To utilize the rat spinotrapezius muscle as a model to investigate the microcirculatory consequences of exercise training, it is necessary to design an exercise protocol that recruits this muscle. There is evidence that the spinotrapezius is derecruited during standard treadmill exercise protocols performed on the uphill treadmill (i.e., 6°incline). This investigation tested the hypothesis that downhill running would effectively recruit the spinotrapezius muscle as assessed by the presence of an exercise hyperemia response. We used radioactive 15-m microspheres to determine blood flows in the spinotrapezius and selected hindlimb muscles of female SpragueDawley rats at rest and during downhill (i.e., Ϫ14°incline; 331 Ϯ 5 g body wt, n ϭ 7) and level (i.e., 0°incline; 320 Ϯ 11 g body wt, n ϭ 5) running at 30 m/min. Both level and downhill exercise increased blood flow to all hindlimb muscles (P Ͻ 0.01). However, in marked contrast to the absence of a hyperemic response to level running, blood flow to the spinotrapezius muscle increased from 26 Ϯ 6 ml ⅐ min Ϫ1 ⅐ 100 g Ϫ1 at rest to 69 Ϯ 8 ml⅐ min Ϫ1 ⅐ 100 g Ϫ1 during downhill running (P Ͻ 0.01). These findings indicate that downhill running represents an exercise paradigm that recruits the spinotrapezius muscle and thereby constitutes a tenable physiological model for investigating the adaptations induced by exercise training (i.e., the mechanisms of altered microcirculatory control by transmission light microscopy). skeletal muscle; blood flow; microvascular adaptation DIRECT OBSERVATION OF SKELETAL muscle microcirculation by intravital microscopy is key to understanding microvascular control, capillary hemodynamics, and O 2 exchange. Unfortunately, there are very few muscles anatomically and optically suitable for transmission light microscopy. Of these, the rat spinotrapezius muscle possesses the following singular advantages: 1) it can be exteriorized and transilluminated without disruption of the nervous or primary vascular supplies (2,12,28,40); 2) it comprises a mosaic of the three principal fiber types found in mammalian muscle (8); and 3) the oxidative capacity approximates that found in the untrained human quadriceps (8,22). Consequently, it is not surprising that intravital microscopy of the spinotrapezius has been integral to our understanding of muscle microcirculation in health (4,21,23,25,31,37,39) and chronic diseases such as heart failure (15), Type 1 diabetes (18), and hypertension (13).Within the past two years, it has been possible to measure spinotrapezius capillary hemodynamics during muscle contractions (17,33). This raises the exciting possibility that the spinotrapezius can be utilized to understand the effects of physiological adaptations, for example, to exercise training on capillary hemodynamics and O 2 exchange in contracting muscle. Unfortunately, conve...

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Exercise: Kinetic Considerations for Gas Exchange

Rossiter

2010

Comprehensive Physiology

171

255

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The activities of daily living typically occur at metabolic rates below the maximum rate of aerobic energy production. Such activity is characteristic of the nonsteady state, where energy demands, and consequential physiological responses, are in constant flux. The dynamics of the integrated physiological processes during these activities determine the degree to which exercise can be supported through rates of O₂ utilization and CO₂ clearance appropriate for their demands and, as such, provide a physiological framework for the notion of exercise intensity. The rate at which O₂ exchange responds to meet the changing energy demands of exercise--its kinetics--is dependent on the ability of the pulmonary, circulatory, and muscle bioenergetic systems to respond appropriately. Slow response kinetics in pulmonary O₂ uptake predispose toward a greater necessity for substrate-level energy supply, processes that are limited in their capacity, challenge system homeostasis and hence contribute to exercise intolerance. This review provides a physiological systems perspective of pulmonary gas exchange kinetics: from an integrative view on the control of muscle oxygen consumption kinetics to the dissociation of cellular respiration from its pulmonary expression by the circulatory dynamics and the gas capacitance of the lungs, blood, and tissues. The intensity dependence of gas exchange kinetics is discussed in relation to constant, intermittent, and ramped work rate changes. The influence of heterogeneity in the kinetic matching of O₂ delivery to utilization is presented in reference to exercise tolerance in endurance-trained athletes, the elderly, and patients with chronic heart or lung disease.

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Skeletal muscle microcirculatory structure and hemodynamics in diabetes

Cited by 91 publications

References 24 publications

Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells

Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells

Downhill running: a model of exercise hyperemia in the rat spinotrapezius muscle

Exercise: Kinetic Considerations for Gas Exchange

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