| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1 Institute for Clinical and Experimental Surgery and 2 Department of Oral and Maxillofacial Surgery, University of Saarland, D-66421 Homburg/Saar, Germany
 |
ABSTRACT |
|---|
 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
We analyzed the incidence and interaction of arteriolar vasomotion and capillary flow motion during critical perfusion conditions in neighboring peripheral tissues using intravital fluorescence microscopy. The gracilis and semitendinosus muscles and adjacent periosteum, subcutis, and skin of the left hindlimb of Sprague-Dawley rats were isolated at the femoral vessels. Critical perfusion conditions, achieved by stepwise reduction of femoral artery blood flow, induced capillary flow motion in muscle, but not in the periosteum, subcutis, and skin. Strikingly, blood flow within individual capillaries was decreased (P < 0.05) in muscle but was not affected in the periosteum, subcutis, and skin. However, despite the flow motion-induced reduction of muscle capillary blood flow during the critical perfusion conditions, functional capillary density remained preserved in all tissues analyzed, including the skeletal muscle. Abrogation of vasomotion in the muscle arterioles by the calcium channel blocker felodipine resulted in a redistribution of blood flow within individual capillaries from cutaneous, subcutaneous, and periosteal tissues toward skeletal muscle. As a consequence, shutdown of perfusion of individual capillaries was observed that resulted in a significant reduction (P < 0.05) of capillary density not only in the neighboring tissues but also in the muscle itself. We conclude that during critical perfusion conditions, vasomotion and flow motion in skeletal muscle preserve nutritive perfusion (functional capillary density) not only in the muscle itself but also in the neighboring tissues, which are not capable of developing this protective regulatory mechanism by themselves.
critical perfusion; intravital fluorescence microscopy; microcirculation; skin; subcutis; periosteum; felodipine; redox state; reduced nicotinamide adenine dinucleotide
| |
INTRODUCTION |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
VASOMOTION IS DEFINED as spontaneous rhythmic changes of arteriolar diameter (1), whereas flow motion characterizes the periodic changes of red blood cell velocities in both arterioles and downstream capillaries (26). Fast-wave vasomotion with a frequency of 8-20 cycles/min is assumed to be related to terminal arterioles (30), whereas slow-wave vasomotion with a frequency of 1-3 cycles/min is thought to be due to the activity of more proximal transverse arterioles (24). Whether capillary flow motion is the direct consequence of arteriolar vasomotion is still a matter of uncertainty. Experiments with laser-Doppler flowmetry, a technique that indirectly detects variations in red blood cell flux in a fairly large tissue volume and, thus, mainly from capillaries, suggested that capillary flow motion may be the consequence of slow-wave arteriolar vasomotion of the more distant (upstream) transverse arterioles (5, 24). It is not clear, however, whether the fast-wave vasomotion in terminal arterioles, which are more closely located to the capillaries, influences capillary flow motion activity.
The mechanisms of control of arteriolar vasomotion are poorly understood. Pacemaker cells with voltage-dependent calcium channels at arteriolar bifurcations are proposed to serve as discrete local origins of the oscillatory excitation (8, 16). Although the incidence of vasomotion and flow motion has been analyzed in a variety of different tissues (6, 12, 21, 24), the results of these studies are still inconsistent, particularly with regard to the involvement of the microcirculation of cutaneous tissue (2, 13) and the question as to whether these regulatory mechanisms are physiological or pathological in nature. Until one decade ago, it was suggested that vasomotion and flow motion represent mainly physiological conditions (10, 14) and are abrogated under conditions of malperfusion (4, 20). Recent reports, however, support the view that vasomotion and flow motion are rarely active during normal perfusion but are induced during conditions of critical perfusion, i.e., fixed-volume hemorrhage (3) and local arterial pressure reduction (25). Hence, at present it is hypothesized that vasomotion and flow motion appear in a respective tissue due to critically ischemic conditions to compensate locally for inadequate microvascular blood perfusion (24) and, as shown in a mathematical model, to guarantee appropriate tissue oxygenation (27).
It remains to be determined, however, in which type of tissue vasomotion and flow motion can be induced and whether their appearance in a particular tissue influences the microcirculation of neighboring tissues. We therefore analyzed the incidence and interaction of arteriolar vasomotion and capillary flow motion during critical perfusion in neighboring peripheral tissues using intravital fluorescence microscopy.
| |
METHODS |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
Animals. Fourteen Sprague-Dawley rats with a body weight of 280-320 g were used for the microcirculatory studies. All animals were housed one per cage and had free access to tap water and standard pellet food (Altromin, Lage, France). The study complied with the National Institutes of Health Guidelines for the Care and Use of Laboratory Animals and was approved by the local animal care committee.
Surgical technique.
The surgical preparation of the peripheral tissues was performed
according to the technique described previously in detail (23). Under pentobarbital sodium anesthesia (50 mg/kg body
wt ip; Abbott, North Chicago, IL) the animals were placed in the supine
position on a heating pad to maintain the body temperature between 36 and 37°C. Supplementary pentobarbital sodium (5 mg/kg body wt) was
given intraperitoneally if required. The animals were tracheotomized to
facilitate spontaneous respiration. Polyethylene catheters (PE-50,
0.58-mm inner diameter; Portex, Lythe, UK) were inserted into the right
carotid artery and the left jugular vein to allow monitoring of
arterial blood pressure as well as continuous infusion of isotonic
saline solution (1 ml · 100 g body wt
1 · h1) and injection of drugs and fluorescent dyes for
intravital microscopy.
Exterioration of the tissue preparation for intravital microscopy. We dissected the skin island from the underlying muscles, saving the cutaneous branches of the saphenous vessels and the surrounding subcutaneous tissue. This allowed plain exposure of the upside of skin and subcutis, the downside of muscles (gracilis and semitendinosus), and the periosteum of the medial aspect of the tibia on an adjustable stage placed near the left groin. The tissues were covered with a glass slide to prevent drying and exposure to ambient air. The stage was adjusted horizontally, and the animal on the heating pad was transferred to the microscope for the in vivo analysis of the microcirculation.
Intravital fluorescence microscopy. For epi-illumination fluorescence microscopy, a modified Zeiss Axiotech microscope (Zeiss, Jena, Germany) with a 100-W mercury arc lamp (23) was used. The microscope was equipped with a blue filter combination (450- to 490-nm excitation/>520-nm emission wavelength) for visualization of fluorescein (23) and a near ultraviolet filter combination (360- to 380-nm excitation/>450-nm emission wavelength) for monitoring of NADH fluorescence (28). The microscopic images were recorded by a charge-coupled-device (CCD) video camera (model FK 6990; COHU, Prospective Measurements, San Diego, CA) and transferred to a video system (S-VHS Panasonic AG 7350; Matsushita, Tokyo, Japan) for off-line evaluation. With the use of a long-distance working objective (Plan Neofluar ×10/0.3; Zeiss) and water-immersion objectives (W ×20/0.5 and W ×40/0.75; Zeiss), magnifications of ×216, ×432, and ×864 were achieved on a 14-in. video screen (PVM 1444; Sony, Tokyo, Japan).
The microcirculation of the periosteum, muscle, subcutis, and skin was analyzed after intravenous injection of 0.25 ml of 5% fluorescein-isothiocyanate (FITC)-labeled dextran (molecular weight 150,000; Sigma Chemical, St. Louis, MO). The contrast enhancement achieved by this macromolecular tracer guaranteed high-resolution imaging due to staining of the intravascular space (plasma) in the absence of transendothelial macromolecular leakage. To avoid phototoxic tissue damage, attention was paid to a strict limitation of the exposure time to 60 s per microscopic field.Video analysis.
Incidence of arteriolar vasomotion and capillary flow motion was
evaluated off-line. With computer assistance (CapImage, Zeintl, Heidelberg, Germany; Capiflow, Capiflow AB, Kista, Sweden), video analysis further included frequency and amplitude of arteriolar vasomotion and capillary flow motion (normalized to the mean arteriolar diameter and the mean capillary blood flow, respectively), functional capillary density [defined as the total length of capillaries with
blood flow per unit area of observed tissue (cm1)],
arteriolar and capillary diameters (µm), and red blood cell velocities (VRBC, in mm/s). Arteriolar and
capillary blood flow (ABF/CBF, in pl/s) were calculated from
VRBC and diameters (D) for each
vessel as ABF/CBF = 
× (D/2)2 × VRBC. In case of arteriolar and capillary
flow motion, which showed a pattern close to sinusoidal, diameters and
red blood cell velocities were measured during maximal and minimal flow conditions. Additionally, the overall blood flow calculation (average over the cycle) took into account the time periods of high (maximal) and low (minimal) flow during the respective vasomotion/flow motion cycle.
Induction of critical perfusion. Critical perfusion was induced by reducing the left femoral artery blood flow using a micromanipulator-assisted tourniquet. For on-line control of blood flow, a perivascular flow probe (Transonic Systems, Ithaca, NY) adapted to an ultrasonic flowmeter (T206 animal research flowmeter, Transonic Systems) was applied to the left femoral artery downstream from the tourniquet. This allowed exact assessment of the reduction of total blood flow to the peripheral tissues.
Drug application. Felodipine, a vasoselective, long-acting, highly lipophilic, and hydropyridine-based calcium channel blocker (MG 384.3), was kindly provided by Astra (Wedel, Germany). Following the protocol of Messing and co-workers (19), felodipine was dissolved in a mixture of polyethylene glycol, ethanol, and distilled water of 15:15:100 (vol/vol/vol). Felodipine was given intravenously as a single dose of 90 µg/kg body wt.
Experimental protocol. In a first set of experiments, we elucidated 1) whether arteriolar vasomotion and capillary flow motion appear during critical perfusion conditions in all peripheral tissues studied and 2) whether capillary flow motion directly depends on the onset of arteriolar vasomotion. Therefore, the blood flow of the femoral artery supplying the peripheral tissues was stepwise reduced from normal conditions (0.21 ± 0.02 ml/min, n = 7) to 0.15, 0.10, and 0.05 ml/min. Intravital fluorescence microscopy of periosteum, muscle, subcutis, and skin was performed before induction of critical perfusion as well as at the different steps of arterial inflow reduction.
In a second set of experiments, we clarified 1) whether microvascular perfusion and, in consequence, the metabolic (redox) state of the tissues are maintained by induction of capillary flow motion during reduced arterial blood supply, and 2) whether the appearance of arteriolar vasomotion and capillary flow motion in a particular tissue influences the microcirculation of neighboring tissues. Therefore, in a further seven animals, arterial blood flow to the peripheral tissues was reduced to 0.15 ml/min to induce arteriolar vasomotion. To test its influence on the different tissues, vasomotion was then abolished by applying the calcium channel blocker felodipine intravenously. Intravital microscopic analysis of periosteum, muscle, subcutis, and skin was performed during the critical perfusion conditions (0.15 ml/min femoral arterial inflow) before and after drug application.Statistical analysis.
Results are expressed as means ± SE. Statistics first included
testing for normality of distribution and equal variance. ANOVA or
Kruskal-Wallis ANOVA was then performed, followed by appropriate post
hoc comparisons. In case of repeated measurements, correction of the
error was included. Differences were considered significant at
P < 0.05.
| |
RESULTS |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
Incidence of arteriolar vasomotion and capillary flow motion during critical perfusion conditions. Before induction of critical perfusion conditions, recordings of systemic hemodynamics revealed a mean arterial blood pressure of 102.1 ± 5.4 mmHg, which was not affected after the arterial blood flow in the left femoral artery was reduced to 0.15, 0.10, and 0.05 ml/min.
Intravital microscopic baseline recordings under normal conditions showed homogeneous perfusion of nutritive capillaries without arteriolar vasomotion and capillary flow motion in all tissues analyzed. Lack of perfusion of individual capillaries was not observed. In all animals studied, reduction of arterial blood flow to 0.15 ml/min induced arteriolar vasomotion in skeletal muscle (Fig. 1) but not in the periosteum, subcutis, and skin. Vasomotion was evident in both terminal and transverse muscle arterioles analyzed. The frequency was 1.92 ± 0.10 min1 in terminal arterioles and 2.21 ± 0.27 min1 in transverse arterioles, whereas the amplitude
(normalized to the mean arteriolar diameter) was 57.5 ± 14.6 and
60.7 ± 11.3%, respectively. The arteriolar slow-wave vasomotion
corresponded well with the onset of fluctuations of blood flow in all
of the downstream muscle capillaries (Fig. 1), demonstrating a flow
motion frequency of 2.04 ± 0.13 min1 and an
amplitude (normalized to the mean capillary blood flow) of 169.8 ± 5.4%.
|
|
|
1), whereas
the amplitude of capillary blood flow was significantly increased
(P < 0.05) to 183.1 ± 1.5%. Analysis of
individual blood flow within these muscle capillaries revealed a
further decrease, whereas the blood flow within the capillaries of the
periosteum, subcutis, and skin still remained preserved (Fig. 2).
However, despite the further reduction of blood flow within the
individual muscle capillaries, the functional capillary density
remained constant not only in the periosteum, subcutis, and skin but
also in the muscle tissue (Fig. 3). In contrast, when muscle capillary flow motion disappeared at 0.10 ml/min of femoral artery inflow, individual capillary blood flow was significantly less reduced in
muscle tissue but severely diminished (P < 0.05) in
cutaneous, subcutaneous, and periosteal tissue (Fig. 2). The reduction
of individual blood flow in the periosteum, subcutis, and skin was associated with shutdown of perfusion within single capillaries, as
indicated by a significantly reduced (P < 0.05)
functional capillary density (Fig. 3). Strikingly, under the conditions
of disappearance of muscle capillary flow motion, shutdown of perfusion within single capillaries also occurred in muscle [significant decrease (P < 0.05) of functional capillary density
(Fig. 3)], despite the observed increase of mean blood flow within the
remaining, still-perfused vessels.
Reduction of arterial blood supply to 0.05 ml/min resulted in the
disappearance of muscle capillary flow motion in almost all tissue
preparations analyzed (6 of 7) and was accompanied by a further drastic
decrease (P < 0.05) of individual capillary blood flow
(Fig. 2) and functional capillary density (Fig. 3) in all tissues under
investigation. Strikingly, the decrease of both individual capillary
blood flow and functional capillary density related to baseline was
similar to that in muscle (21.7 ± 0.9 and 35.0 ± 4.8%)
compared with that in the periosteum (28.4 ± 1.1 and 20.8 ± 10.6%), subcutis (24.0 ± 3.3 and 26.7 ± 12.2%), and skin
(26.1 ± 5.0 and 29.5 ± 12.8%), indicating that under these
extreme low-flow conditions, none of the tissues remained preferentially perfused.
Influence of muscle arteriolar vasomotion and capillary flow motion
on microcirculation of neighboring tissues.
In the second set of experiments, the femoral artery inflow was kept at
reduced conditions of 0.15 ml/min. Intravenous injection of felodipine
resulted in a significant (P < 0.05) decrease of mean
arterial blood pressure with only slight recovery over time (Table
1). However, independent of the changes
of systemic blood pressure, the volumetric blood flow in the left
femoral artery (0.15 ml/min) was kept constant throughout the
experiments by appropriate adjustment of the tourniquet.
|
|
|
|
|
|
|
| |
DISCUSSION |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
The major findings of the present study are that 1) critical perfusion conditions in rat peripheral tissues induce arteriolar vasomotion and capillary flow motion in muscle but not in the periosteum, subcutis, and skin, and 2) vasomotion and/or flow motion in muscle preserves capillary perfusion density and parenchymal oxygen state in the muscle itself as well as in the neighboring tissues.
The lack of vasomotion and flow motion under normal conditions with their onset occurring only after induction of critical perfusion confirms the results of recent reports that the rhythmical change of microvessel diameter and blood flow is a regulatory (compensatory) mechanism active under pathological perfusion conditions (3, 25) and contradicts the previously proposed view that its physiological nature is to control the microcirculation under normal conditions (10, 14).
Vasomotion and flow motion have been described in distinct tissues with the use of different animal models, including muscle (5, 13, 24), pancreas (18, 29), mucosa (6), brain (21), and testis (12), whereas this type of microvascular blood flow regulation has not been observed in the kidney or liver either under physiological conditions or during hemorrhage (13). The present study confirms the inducibility of vasomotion and flow motion in skeletal muscle and adds the novel information that neither occur in the periosteum and subcutis. In skin, intravital microscopy in humans could clearly demonstrate the presence of capillary flow motion under various conditions (2), whereas analysis of peripheral tissues in rodents verified hemorrhage-induced flow motion in muscle but not in skin (13). Hence, analysis of the ability of a particular critically perfused tissue to control its microcirculation by arteriolar vasomotion and capillary flow motion has to consider species-confined differences, although, independent of the species, muscle seems to be preferentially prone to development of this type of vascular control mechanism, as also demonstrated in the present study.
The tissue preparation under investigation in the present study is supplied by the saphenous artery and drained by the saphenous vein (common supply and drainage vessels). The individual tissues of the preparation are supplied by direct (distinct) individual branches of the saphenous artery (22). Thus the occurrence of vasomotion and/or flow motion is not necessarily dependent on local tissue factors. More probably, local pacemakers in individual arterioles (17), which may be present in the vasculature of the muscle but not the periosteum, subcutis, and skin, have to be discussed as the cause for the selectively observed onset of vasomotion and/or flow motion.
The reduction of arterial inflow from 0.21 to 0.15 ml/min induced a reduction of muscle capillary blood flow from 17 to 6 pl/s, whereas capillary blood flow in the periosteum, subcutis, and skin remained almost unchanged. Nonetheless, the overall reduction of capillary blood perfusion may correspond with the reduction of blood flow measured in the femoral artery, because the tissue preparation studied consists majorly (>50%) of muscle tissue. However, we cannot exclude the existence of arteriolar-venular shunts, which may additionally contribute to the maintenance of nutritive perfusion, because the superficial approach by intravital microscopy does not allow for complete network analysis.
Previous reports have described two distinct types of vasomotion and/or flow motion (9, 30). Fast-wave vasomotion, which is thought to originate from terminal arterioles, is characterized by a frequency of 8-20 cycles/min, whereas slow-wave vasomotion, which may originate from transverse arterioles, shows a frequency of 1-3 cycles/min. In the present study, we demonstrated a vasomotion frequency of ~2 cycles/min, independent of the arteriolar order, whereas fast-wave vasomotion could not be detected. This is in line with recent reports of others (5, 24), which also could not confirm the presence of fast-wave vasomotion in critically perfused skeletal muscle. In fact, fast-wave flow motion (flux motion) as detected by laser-Doppler flowmetry may not be the result of rhythmical diameter changes of arterioles under critical perfusion conditions but, rather, may be related to respiration-induced fluctuations of blood flow through venules (11).
Critical perfusion-induced muscle arteriolar vasomotion disappeared immediately after intravenous injection of felodipine, a vasoselective calcium channel blocker. This confirms the dependency of vasomotion on voltage-operated calcium channels, as previously demonstrated by Colantuoni et al. (8) and Goligorsky et al. (16). The fact that not only arteriolar vasomotion but also capillary flow motion ceased directly after felodipine application indicates that capillary flow motion is the direct consequence of arteriolar vasomotion. The suggestion that arteriolar vasomotion is indeed the effector of capillary flow motion is further supported by the observation that vasomotion frequency of transverse arterioles was synchronized not only to the vasomotion frequency of terminal arterioles but also to the flow motion frequency of the downstream capillaries.
The abrogation of muscle arteriolar vasomotion by felodipine induced a maximal arteriolar dilation, which was associated with a dramatic increase of blood flow in both the terminal and transverse arterioles. Consequently, perfused downstream muscle capillaries, in which flow motion also disappeared, showed a significant increase of blood flow. Concomitantly, individual capillary blood flow in the neighboring tissues decreased, and even complete shutdown of blood flow in single capillaries was observed, as reflected by the reduced functional capillary density. This may be explained by a shift of overall blood supply from the periosteum, subcutis, and skin toward skeletal muscle after cessation of vasomotion and/or flow motion, probably due to the reduction of vascular resistance caused by the maximal felodipine-induced arteriolar dilation (15).
The fact that under critical perfusion conditions, functional capillary density and individual capillary blood flow in the periosteum, subcutis, and skin were preserved during muscle arteriolar vasomotion and capillary flow motion but decreased after cessation of vasomotion and/or flow motion indicates that vasomotion and flow motion in muscle protect the microvascular perfusion of the neighboring tissues, which are not capable of eliciting these regulatory mechanisms by themselves. Apart from the protection of nutritive perfusion of neighboring tissues, muscle arteriolar vasomotion and flow motion may also preserve nutritional blood supply within the muscle itself. Although the individual blood flow of perfused muscle capillaries was significantly higher after felodipine-induced cessation of vasomotion, this could not prevent the shutdown of blood flow in adjacent muscle capillaries, as shown by the decreased functional capillary density.
The effect of arteriolar vasomotion and capillary flow motion on tissue oxygenation under critical perfusion conditions has not been studied yet in detail. From a mathematical model, it was concluded that slow-wave flow motion constitutes a compensatory mechanism to guarantee adequate tissue oxygenation (27). By analyzing NADH fluorescence as an indicator of mitochondrial redox state (7), we demonstrated here that abrogation of muscle vasomotion and flow motion under critical perfusion conditions decreases oxygenation of the periosteum, subcutis, and skin, whereas redox state in muscle was not affected. The alteration of oxygenation of the periosteum (distant from the supplying vessels), subcutis, and skin is probably due to the decrease of individual capillary blood flow and capillary density. In the periosteum adjacent to the supplying vessels, the morphologically given high capillary density with the numerous preferential pathways may secure oxygenation of tissue, whereas in muscle, the increase of individual capillary blood flow may have compensated for the decrease in functional capillary density, also resulting in the maintenance of tissue oxygenation after cessation of vasomotion and/or flow motion.
In summary, we have demonstrated that under critical perfusion conditions, calcium-dependent muscle arteriolar vasomotion and capillary flow motion are associated with redistribution of blood flow from muscle to neighboring peripheral tissues, i.e., periosteum, subcutis, and skin, which are not able to develop these protective regulatory mechanisms on their own. The redistribution of blood flow results in maintenance of an adequate microvascular supply, which guarantees appropriate tissue oxygenation despite the overall critical perfusion conditions.
| |
ACKNOWLEDGEMENTS |
|---|
This study was supported by a grant from the Deutsche Forschungsgemeinschaft (Me 900/1-3 and Me 900/1-4). B. Vollmar is a recipient of a Heisenberg-Stipendium from the Deutsche Forschungsgemeinschaft (Vo 450/6-1).
| |
FOOTNOTES |
|---|
Address for reprint requests and other correspondence: M. Rücker, Institute for Clinical and Experimental Surgery, Univ. of Saarland, D-66421 Homburg/Saar, Germany (E-mail: exmrue{at}med-rz.uni-sb.de).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Received 12 August 1999; accepted in final form 17 January 2000.
| |
REFERENCES |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
1.
Allegra, C,
Intaglietta M,
and
Messmer K.
Vasomotion and flowmotion.
Prog Appl Microcirc
20:
1-88,
1993.
2.
Bollinger, A,
Hoffmann U,
and
Franzeck UK.
Microvascular changes in arterial occlusive disease: target for pharmacotherapy.
Vasc Med
1:
50-54,
1996.
3.
Borgström, P,
Bruttig SP,
Lindbom L,
Intaglietta M,
and
Arfors KE.
Microvascular responses in rabbit skeletal muscle after fixed volume hemorrhage.
Am J Physiol Heart Circ Physiol
259:
H190-H196,
1990.
4.
Borgström, P,
Lindbom L,
Meyer JU,
Sjoquist M,
Arfors KE,
and
Intaglietta M.
Hemodynamic responses in rabbit tenuissimus muscle arterioles during local reduction in perfusion pressure.
Int J Microcirc Clin Exp
9:
175-186,
1990.
5.
Borgström, P,
Schmidt JA,
Bruttig SP,
Intaglietta M,
and
Arfors KE.
Slow-wave flowmotion in rabbit skeletal muscle after acute fixed-volume hemorrhage.
Circ Shock
36:
57-61,
1992.
6.
Bouskela, E,
and
Cyrino FZGA
Effects of buflomedil on spontaneous vasomotion and mean arteriolar internal diameter in the hamster cheek pouch.
J Vasc Res
31:
287-294,
1994.
7.
Chance, B,
Cohen P,
Jobisi F,
and
Schoener B.
Intracellular oxidation-reduction states in vivo. The microfluorometry of pyridine nucleotide gives a continuous measurement of the oxidation state.
Science
137:
499-508,
1962.
8.
Colantuoni, A,
Bertuglia S,
and
Intaglietta M.
The effects of alpha- and beta-adrenergic receptor antagonists and calcium entry blockers on the spontaneous vasomotion.
Microvasc Res
28:
143-158,
1984.
9.
Colantuoni, A,
Bertuglia S,
and
Intaglietta M.
Quantitation of rhythmic diameter changes in arterial microcirculation.
Am J Physiol Heart Circ Physiol
246:
H508-H517,
1984.
10.
Colantuoni, A,
Bertuglia S,
and
Intaglietta M.
Microvessel diameter changes during hemorrhagic shock in unesthesized hamsters.
Microvasc Res
30:
133-142,
1985.
11.
Colantuoni, A,
Bertuglia S,
and
Intaglietta M.
Microvascular vasomotion: origin of laser Doppler flux motion.
Int J Microcirc Clin Exp
14:
151-158,
1994.
12.
Collin, O,
Kilter S,
and
Bergh A.
Tobacco smoke disrupts testicular microcirculation in the rat.
Int J Androl
18:
141-145,
1995.
13.
Erni, D,
Banic A,
Wheatley AM,
and
Sigurdsson GH.
Haemorrhage during anaesthesia and surgery: continuous measurement of microcirculatory blood flow in the kidney, liver, skin, and skeletal muscle.
Eur J Anaesthesiol
12:
423-429,
1995.
14.
Faber, JE,
Harris PD,
and
Wiegman DL.
Anesthetic depression of microcirculation, central hemodynamics, and respiration in decerebrate rats.
Am J Physiol Heart Circ Physiol
243:
H837-H843,
1982.
15.
Funk, W,
Endrich B,
Messmer K,
and
Intaglietta M.
Spontaneous arteriolar vasomotion as a determinant of peripheral vascular resistance.
Int J Microcirc Clin Exp
2:
11-25,
1983.
16.
Goligorsky, MS,
Colflesh D,
Gordienko D,
and
Moore LC.
Branching points of renal resistance arteries are enriched in L-type calcium channels and initiate vasoconstriction.
Am J Physiol Renal Fluid Electrolyte Physiol
268:
F251-F257,
1995.
17.
Intaglietta, M.
Arteriolar vasomotion: implications for tissue ischemia.
Blood Vessels
28, Suppl1:
1-7,
1991.
18.
McCuskey, RS,
and
Chapman TM.
Microscopy of the living pancreas in situ.
Am J Anat
126:
395-407,
1969.
19.
Messing, M,
Van Essen H,
Smith TL,
Smits JFM,
and
Struyker-Boudier HAJ
Microvascular actions of calcium channel antagonists.
Eur J Pharmacol
198:
189-195,
1991.
20.
Meyer, JU,
Borgstrom P,
Lindbom L,
and
Intaglietta M.
Vasomotion patterns in skeletal muscle arterioles during changes in arterial pressure.
Microvasc Res
35:
193-203,
1988.
21.
Morita, Y,
Hardebo JE,
and
Bouskela E.
Influence of cerebrovascular sympathetic, parasympathetic, and sensory nerves on autoregulation and spontaneous vasomotion.
Acta Physiol Scand
154:
121-130,
1995.
22.
Mutaf, M,
Tasaki Y,
Arakaki M,
and
Fujii T.
A true osteomyocutaneous free-flap model in rats: the saphenous artery osteomyocutaneous flap.
Plast Reconstr Surg
96:
1629-1635,
1995.
23.
Rücker, M,
Roesken F,
Vollmar B,
and
Menger MD.
A novel approach for comparative study of periosteum, muscle, subcutis, and skin microcirculation by intravital fluorescence microscopy.
Microvasc Res
56:
30-42,
1998.
24.
Schmidt, JA,
Borgström P,
and
Intaglietta M.
The vascular origin of slow wave flowmotion in skeletal muscle during local hypotension.
Int J Microcirc Clin Exp
12:
287-297,
1993.
25.
Schmidt, JA,
Intaglietta M,
and
Borgström P.
Periodic hemodynamics in skeletal muscle during local arterial pressure reduction.
J Appl Physiol
73:
1077-1083,
1992.
26.
Tangelder, GJ,
Slaaf DW,
and
Reneman RS.
Skeletal muscle microcirculation and changes in transmural and perfusion pressure.
Prog Appl Microcirc
5:
93-108,
1984.
27.
Tsai, AG,
and
Intaglietta M.
Evidence of flowmotion induced changes in local tissue oxygenation.
Int J Microcirc Clin Exp
12:
75-88,
1993.
28.
Vollmar, B,
Burkhardt M,
Minor T,
Klauke H,
and
Menger MD.
High-resolution microscopic determination of hepatic NADH fluorescence for in vivo monitoring of tissue oxygenation during hemorrhagic shock and resuscitation.
Microvasc Res
54:
164-173,
1997.
29.
Vollmar, B,
Preissler G,
and
Menger MD.
Hemorrhagic hypotension induces arteriolar vasomotion and intermittent capillary perfusion in rat pancreas.
Am J Physiol Heart Circ Physiol
267:
H1936-H1940,
1994.
30.
Weiner, RM,
Borgström P,
and
Intaglietta M.
Induction of vasomotion by hemorrhagic hypotension in rabbit tenuissimus muscle.
Prog Appl Microcirc
15:
93-99,
1989.
This article has been cited by other articles:
|
|
 |
|
  M. G. Clark Impaired microvascular perfusion: a consequence of vascular dysfunction and a potential cause of insulin resistance in muscle Am J Physiol Endocrinol Metab, October 1, 2008; 295(4): E732 - E750. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Clark, S. Rattigan, E. Barrett, and M. Vincent Last Word on Point:Counterpoint: There is/is not capillary recruitment in active skeletal muscle during exercise J Appl Physiol, March 1, 2008; 104(3): 900 - 900. [Full Text] [PDF]
|
|
|
|
 |
|
 J. C. B. Jacobsen, C. Aalkjaer, H. Nilsson, V. V. Matchkov, J. Freiberg, and N.-H. Holstein-Rathlou Activation of a cGMP-sensitive calcium-dependent chloride channel may cause transition from calcium waves to whole cell oscillations in smooth muscle cells Am J Physiol Heart Circ Physiol, July 1, 2007; 293(1): H215 - H228. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Radaelli, P. Castiglioni, M. Centola, F. Cesana, G. Balestri, A. U. Ferrari, and M. Di Rienzo Adrenergic origin of very low-frequency blood pressure oscillations in the unanesthetized rat Am J Physiol Heart Circ Physiol, January 1, 2006; 290(1): H357 - H364. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Friesenecker, A. G. Tsai, M. W. Dunser, A. J. Mayr, J. Martini, H. Knotzer, W. Hasibeder, and M. Intaglietta Oxygen distribution in microcirculation after arginine vasopressin-induced arteriolar vasoconstriction Am J Physiol Heart Circ Physiol, October 1, 2004; 287(4): H1792 - H1800. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Nilsson and C. Aalkjaer Vasomotion: Mechanisms and Physiological Importance Mol. Interv., March 1, 2003; 3(2): 79 - 89. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Pajk, B. Schwarz, H. Knotzer, B. Friesenecker, A. Mayr, M. Dunser, and W. Hasibeder Jejunal tissue oxygenation and microvascular flow motion during hemorrhage and resuscitation Am J Physiol Heart Circ Physiol, December 1, 2002; 283(6): H2511 - H2517. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
) or without
(
) muscle capillary flow motion. Regions adjacent (a)
to supplying periosteal vessels were distinguished from regions distant
from these vessels (d). Values are means ± SE; n = 7. *P < 0.05 vs. baseline. #P < 0.05 vs. 0.10 ml/min. +P < 0.05 vs. flow motion.
