Journal of Applied Physiology Watch the video to learn how APS reaches out to developing nations.
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

J Appl Physiol 83: 1867-1876, 1997;
8750-7587/97 $5.00
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Ameredes, B. T.
Right arrow Articles by Provenzano, M. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ameredes, B. T.
Right arrow Articles by Provenzano, M. A.

Vol. 83, Issue 6, 1867-1876, December 1997

Regional intramuscular pressure development and fatigue in the canine gastrocnemius muscle in situ

Bill T. Ameredes and Mark A. Provenzano

Division of Pulmonary, Allergy, and Critical Care Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania 15261

ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES

ABSTRACT

Ameredes, Bill T., and Mark A. Provenzano. Regional intramuscular pressure development and fatigue in the canine gastrocnemius muscle in situ. J. Appl. Physiol. 83(6): 1867-1876, 1997.---Intramuscular pressure (PIM) was measured simultaneously in zones of the medial head of the gastrocnemius-plantaris muscle group (zone I, popliteal origin; zone II, central; zone III, near calcaneus tendon) to determine regional muscle mechanics during isometric tetanic contractions. Peak PIM averages were 586, 1,676, and 993 mmHg deep in zones I, II, and III and 170, 371, and 351 mmHg superficially in zones I, II, and III, respectively. During fatigue, loss of PIM across zones was greatest in zone III (-81%) and least in zone I (-60%) when whole muscle tension loss was -49%. Recovery of PIM was greatest in zone III and least in zone II, achieving 86% and 67% of initial PIM, respectively, when tension recovered to 89%. These data demonstrate that 1) regional mechanical performance can be measured as PIM within a whole muscle, 2) PIM is nonuniform within the canine gastrocnemius-plantaris muscle, being greatest in the deep central zone, and 3) fatigue and recovery of PIM are dissimilar across regions. These differences suggest distinct local effects that integrate to determine whole muscle mechanical capacity during and after intense exercise.

active tension; blood flow; muscle length; passive tension; preload

INTRODUCTION

REGULATION OF MUSCLE BLOOD flow is crucial to the normal mechanical performance of skeletal muscle, particularly during muscular activities such as exercise. In repetitively contracting mammalian muscle, contraction-induced or "functional" hyperemia occurs, with flows reaching levels three to four times that at rest (2, 5, 14, 21). However, studies have shown blood flow through muscle to be diminished or stopped during the period of activation with the production of active force (10, 11, 16, 20, 21). Some of these studies have indicated that this cessation of blood flow may be due to the development of high tissue fluid pressures with tension development (16, 23, 31). Thus tissue fluid pressures in excess of the systolic arterial pressure should cause hindrance or stasis of blood flow through the muscle. However, some studies have shown that muscle blood flow ceases with the production of tissue fluid pressures that are less than the arterial blood pressure and much less than the maximum tissue pressure that can be developed within the muscle (4, 16, 21). Therefore, a simple relationship between tissue fluid pressure and arterial blood pressure does not appear to explain the effects of muscle contraction on blood flow.

An alternative postulate put forth by Barcroft and Millen (4) asserts that direct compression of the vessels by the taut muscle fibers may pinch off blood supply when muscles contract and produce high forces. In this case, flow may be stopped by physical occlusion at specific shear interfaces between tendinous sheets and blood vessels (22). The work of Gray and co-workers (10, 11), in which radiopaque dyes showed definitive boundaries of flow cessation within large blood vessels during a tetanic contraction of the canine hindlimb, seems to support this postulate. Interestingly, these shear forces, which are due to stresses set up along lines of the muscle fibers and connective tissue, are due to solid tissue and are produced in conjunction with the development of tissue fluid pressure during contraction (22). Therefore, it is likely that the combined forces of tissue fluid pressure and solid tissue pressure, referred to as total tissue pressure (12), produce the flow-stopping action of contraction. However, many prior studies have been limited to measurement of tissue fluid pressure production during prolonged (>= 5- to 10-s) contractions (11, 17, 21, 23, 25, 29), which is not representative of temporal contraction/relaxation conditions during cyclical, exercise-type activities of the muscle in vivo. Moreover, many studies have assumed the muscle to be one closed, fluid-interspersed capsule, within which pressure equilibrates uniformly throughout the fluid within the structure. Given the complicated fiber pennation and muscle group architecture of some muscles, e.g., the mammalian gastrocnemius muscle (1), this assumption may not be valid.

To test whether pressure development is uniform in a complex muscle during rapid, repetitive, tetanic contractions, we measured regional intramuscular pressure (PIM) in the canine gastrocnemius-plantaris (GP) muscle in situ. We hypothesized that pressure development would be different in different regions of the muscle, owing to its complicated multipennate architecture (1, 5). We further hypothesized that pressure development would be greatest in the central region, because it has been suggested that this pennate architecture should result in some of the forces being directed toward the center of the muscle (5, 22). Also, similar to losses of whole muscle tension, decrements in pressure should be observable over time during repetitive contractions, indicating fatigue (13). Thus the purposes of this study were to 1) determine whether there were measurable longitudinal and cross-sectional differences in regional pressure development within this muscle group, 2) assess the effect of acute changes in muscle fiber orientation on regional pressure production through alterations of whole muscle length (1), and 3) determine the relationship of regional pressure to whole muscle force development during repetitive fatiguing contractions and recovery.

METHODS

General. Mongrel dogs of both sexes (10-17 kg) were obtained and housed in accordance with the regulations of the University of Pittsburgh. Anesthesia was induced initially with pentobarbital sodium at 30 mg/kg iv and maintained by 60-mg doses. The animals were ventilated through an endotracheal tube with a Harvard respirator, and end-tidal CO2 was maintained at 4.5-5%. Body temperature was maintained at 37-39°C. The muscle group studied was the GP, with isolated circulation, surgically prepared as described previously (2). Briefly, anticoagulation of the blood was achieved with heparin (2,600 U/kg). The sciatic nerve was dissected and cut, and the distal stump was placed in an electrode holder. The calcaneus tendon was freed, cut, and clamped, and the muscle was anchored via the politeal origin, using bone nails placed in the tibia and fibula bones. Blood gases and pH were monitored throughout experiments to assess acid-base status and systemic oxygenation. Muscle blood flow (Q) was measured using a 4-mm cannulating-type electromagnetic flow probe on the outflow from the popliteal vein. Calibration of the flow probe was performed by periodic timed collections of the venous effluent. Pressure transducers connected to the venous outflow line and the contralateral femoral artery provided measurements of mean venous pressure (MVP) and systemic mean arterial pressure (MAP), respectively. Vascular resistance across the muscle (Rv) was calculated as
R<SUB>v</SUB> = (MAP − MVP)/<A><AC>Q</AC><AC>˙</AC></A> (1)
In some instances the contralateral femoral artery provided perfusion, connected directly to the GP muscle popliteal artery via a catheter (3-5 mm OD, 2.5-4.5 mm ID) matched to the diameter of the popliteal artery. This setup allowed direct measurement of the popliteal arterial perfusion pressure of the muscle. These transducers were calibrated using a 0- to 300-mmHg column.

Muscle mechanics. Whole muscle force development was measured with a pneumatic lever specifically designed for the canine GP muscle (2, 5, 8). Optimal muscle length (Lo) was determined as the whole muscle length at which active tension production (total tension minus passive tension) of isometric twitch contractions (0.2 ms, 4 V) was maximal. Whole muscle length was measured using a ruler to measure the distance from the origin of the medial head fibers within the popliteal fossa to the insertion of the medial head fibers onto the calcaneus tendon. Average muscle length at Lo was 10.7 ± 0.5 cm. Active isometric tetanic tension (total tension minus passive tension) under these conditions was determined using a train of electrical pulses (200-ms duration, 50 impulses/s, 4 V) delivered to the sciatic nerve. Because this muscle group has been shown to produce tetanic forces >= 120 pounds at Lo (28), which can produce flexing of the muscle lever support structures (27), additional struts and clamps were utilized to minimize this flexing and subsequent unintended shortening of the muscle. Passive tension at Lo averaged 51 ± 11 g/g for all muscles studied. Experiments evaluating effects of shorter lengths were also performed by small adjustments of the muscle lever length stop, producing shorter whole muscle lengths, measured as above. This produced lower tetanic active tension development, as expected from the classical muscle length-tension relationship (32). It also likely produced significant changes in relative muscle fiber orientation within the muscle 5-10° less than that at Lo (1). The shortest muscle length tested was 1.0-1.2 cm less than Lo; the intermediate length tested was ~0.5 cm less than Lo. Passive tension at Lo for these length experiments (n = 4) was 54 ± 9 g/g, whereas it was 36 ± 5 g/g at the shortest lengths. Repetitive tetanic contraction fatigue trials at Lo were produced using the stimulus train paradigm above, repeated once per second, over a 4-min period. This repetition frequency provided contractions that typically attain high metabolic rates (O2 uptake = 10-12 µmol · min-1 · g-1) and vascular responses (blood flow = ~1-2 ml · min-1 · g-1) (2, 5). Recovery was assessed with a single tetanic contraction elicited at 30 and/or 60 min after the initiation of the trial. At the end of the experiments the animal was killed with an overdose of pentobarbital sodium, and the GP muscle was excised, trimmed, and weighed. The average wet weight of the muscles studied was 39 ± 1 g.

PIM. PIM was assessed using Millar Mikro-tip needle-type pressure transducers (model SPR-477) inserted directly into the medial head of the GP muscle. The transducer sensor is a diffused semiconductor, using the Wheatstone bridge principle, encased in a metal barrel housing (1 mm diameter) with two sensing windows toward the tip of the barrel. One window is the active surface, and the other is reference; both are covered with silicon rubber. The transducers had a maximal frequency response of 20 kHz, a maximum under/overpressure range of -760 to +4,000 mmHg, and a rated accuracy of ±1% in the range of -50 to +300 mmHg. Calculations provided by Otten (22) indicated that a muscle with curved fibers should be able to produce >= 863 mmHg PIM at the center. Evidence of this possibility was shown by a recording of 1,025 mmHg in the human vastus medialis muscle (30). Also, we found that 1,000 mmHg could be developed easily by pressing the transducer between the thumb and forefinger. Therefore, we further evaluated their accuracy over a greater range of positive pressure, using a 2,500-mmHg manometer. We found their deviation from linearity to be <= 8% at the highest pressures (1,000-2,500 mmHg) and <= 4% at <= 1,000 mmHg. Periodic checks were made with the 0- to 300- and 0- to 1,400-mmHg column over the course of these studies. The transducer was connected to a controller unit (model TC-510, Millar), which itself was connected to a Gould direct-current amplifier within a Gould strip chart recorder (model 2800).

The medial head of the GP muscle was divided into three zones (Fig. 1): zone I, near the popliteal origin; zone II, in the center of the muscle head; and zone III, near the insertion of muscle fibers onto the calcaneus tendon. Transducer barrels were inserted into each of these zones and oriented perpendicular to the rostral-caudal aspect of the muscle surface. Because the needle taper of the barrel of these transducers is relatively blunt (noncutting), bleeding was minimal in all the present studies, with one exception, in which a major underlying vessel was punctured, necessitating termination of the experiment. Signals of PIM from these regions were recorded on a strip chart recorder (Gould 2800). Examples of the regional PIM signals and their comparison with whole muscle tension development at Lo are shown in Fig. 2, illustrating that PIM development during a tetanic isometric contraction was in phase and similar in the directional, amplitude, and time domains. Peak values of the PIM signals were measured directly from the records and used to compare PIM development in these studies. To provide an analysis of cross-sectional regionalization, the effects of depth of transducer placement were evaluated. Transducers were inserted to depths marked directly onto the metal transducer casings, measured at 1 cm ("superficial," n = 4 muscles) and 2 cm ("deep," n = 6 muscles) from the blunt metal tip. For the fatigue studies of PIM, deep placement of the transducers was utilized.
Fig. 1. Schematic of left canine gastrocnemius-plantaris muscle showing shape of medial head of muscle group (striped) and 3 zones of partition. Zone I, proximal one-third of head, nearest popliteal origin; zone II, central one-third of head, including muscle "belly"; zone III, distal one-third of head, in which muscle fibers converged and inserted onto calcaneus tendon.
[View Larger Version of this Image (31K GIF file)]

Fig. 2. Digitized image from original strip chart recording showing typical regional intramuscular pressure [by zone: zone I (A), zone II (B), zone III (C); see Fig. 1] and whole muscle tension (D) signals recorded in these studies, with train stimulus artifact at top and time base at bottom.
[View Larger Version of this Image (10K GIF file)]

Statistics. Values of peak PIM obtained during fatigue and recovery trials were analyzed using a two-factor (zone, time) repeated-measures analysis of variance (ANOVA; SigmaStat, Jandel) to determine the effects of regional placement and changes in PIM over time. Whole muscle tension changes over time also were analyzed in this way. Differences at discrete times were compared using a Duncan post hoc analysis. Comparisons of length-dependent changes in PIM and tension were performed using a one-factor (length) repeated-measures ANOVA, because the same muscles were analyzed at sequentially altered lengths. Comparisons of PIM within regional zones between superficial and deep placement experiments were made using a simple one-factor (depth) ANOVA, because different sets of muscles were utilized in these cross-sectional studies. Comparisons of PIM between regional zones at the same depth were analyzed with a one-factor (zone) repeated-measures ANOVA. All other comparisons were made using independent sample t-tests. P <=  0.05 was considered significant in all tests.

RESULTS

Systemic cardiovascular characteristics of the animals were as follows: arterial pressure = 110 ± 6 mmHg, arterial pH = 7.41 ± 0.06, arterial PO2 = 106 ± 10 Torr, arterial PCO2 = 34 ± 1 Torr, hematocrit = 42 ± 3. No significant changes were noted in any of these variables throughout the experiments; therefore, all animals were considered to be similar with regard to systemic oxygenation and acid-base status.

An example of the time-related changes in PIM, Q, and muscle venous pressure observed during single contractions is shown in Fig. 3. Each tetanic contraction typically caused an increase in PIM, producing a subsequent transient pressure rise in venous outflow, which in turn resulted in a rapid, large elevation of blood outflow. This was followed by a second, smaller and slower Q elevation later in time. During repetitive contractions, Rv decreased significantly from the resting value (from 329 ± 47 to 88 ± 4 mmHg · ml-1 · min-1 · g-1, P <=  0.05), indicating significant contraction-induced vasodilation while Q increased by four to five times that at rest (from 0.3 ± 0.1 to 1.4 ± 0.1 ml · min-1 · g-1). This resistance drop also signifies a vigorous autoregulatory response of these muscle preparations during contractions, demonstrating their ability to respond to a significant metabolic challenge (26). An example of the vascular effects produced by repetitive PIM development during contractions is illustrated in Fig. 4A, which shows large, repetitive fluctuations in muscle venous pressure and Q. The effects of these contractions on muscle arterial pressure signals are shown in Fig. 4B.

Fig. 3. Digitized image from original strip chart recording showing time-based comparisons of signal transients of intramuscular pressure (PIM) (zone I, A; zone II, B; zone III, C), tension (D ), blood flow (Q) (E), and muscle venous pressure (PVEN; F). A perpendicular vertical line is placed in register with 1st pulse of stimulus train for timing reference. Q signal is slightly damped (10-Hz sampling frequency) to allow upward transient during contraction to remain on-scale with subsequent postcontraction Q response. Note difference in time base during contraction and subsequently.
[View Larger Version of this Image (10K GIF file)]


Fig. 4. A: recording of 1 experiment illustrating effects of PIM on blood pressure and flow. Intramuscular pressure in zone III (PIM), whole muscle tension (T), blood flow (Q), popliteal vein outflow pressure (PVEN), and popliteal artery pressure (PART) were recorded during beginning of a repetitive contraction trial, with time bases at top. Blood supply was from contralateral artery. Q sampling frequency was 10 Hz. PVEN was recorded initially as mean pressure and switched to pulsatile ~30 s into trial. Individual contractions shown at fast paper speed indicate that, when peak PIM was 300 mmHg, pulsatile PVEN was increased by 10-20 mmHg, generating pulsatile Q increments of 70-80 ml/min. B: recording of end of experiment. PIM had fallen to 200 mmHg and remained there. At far left of PVEN record is mean PVEN (~8 mmHg), again switched to pulsatile, displaying increases of 25-35 mmHg. At far left of Q signal is time-averaged Q (~55 ml/min), switched to pulsatile (10-Hz), showing Q increases of >= 80-100 ml/min, peaks of which were off-scale. PART tracing shows mean pressure initially (~120 mmHg), then pulsatile. At slow paper speed (left), muscle contraction-induced pressure in popliteal artery line appears as spikes upward, superimposed on normal diastolic-to-systolic pressure signal. Fast paper speed shows typical diastolic-to-systolic pressure transient with heartbeat, with an additional pressure hump interposed (arrows), due to muscle contraction, and in phase with contraction-induced increments in PVEN and Q. At slower paper speed (right) superimposed arterial pressure spikes cease with cessation of contractions. Slowest paper speed (far right) shows eventual mean Q decrease after cessation of contractions.
[View Larger Versions of these Images (47 + 82K GIF file)]

The effect of whole muscle length on regional PIM development during tetanic contraction is shown in Fig. 5. As expected from the length-tension relationship (32), whole muscle isometric tension declined at shorter muscle lengths. Regional PIM also declined significantly in all three zones of the medial head of this muscle when the whole muscle was passively shortened. The range of PIM shown at Lo in each zone is slightly different from that shown subsequently, because transducer depth was not rigidly controlled in these experiments. However, all transducers remained at the same depth throughout the whole muscle length change experiments.

Fig. 5. Changes in regional PIM [zone I (A), zone II (B), and zone III (C)] and whole muscle tension (D) with changes in whole muscle length showing decreased PIM and tension at shorter muscle lengths in 4 individual muscles. Lo, optimal muscle length. Statistical symbols denote significance for comparisons between means of the 4 points shown at each length. * P <=  0.05 compared with 95% Lo mean; + P <=  0.05 compared with 90% Lo mean.
[View Larger Version of this Image (16K GIF file)]

The longitudinal and cross-sectional regionalization of PIM is shown in Fig. 6, in which peak PIM averages are recorded at Lo with superficial and deep placement of the transducers in zones I, II, and III in the medial head of the GP muscle. PIM recorded within the deep portion of the muscle head was significantly higher in zones I and II than in the superficial placement. The deep PIM of zone III showed a tendency to be higher than the superficial PIM in this same zone but was not significantly different. The deep PIM of zone II was significantly greater than the deep PIM of zone I, whereas the deep PIM of zone III was not different from either of the other two zones, suggesting that it was intermediate in magnitude. Thus the highest PIM values were typically recorded with deep placement in zone II, and the lowest values were recorded with superficial placement in zone I. The peak active tension development in the superficial placement experiment was similar to that in the deep placement experiment (Fig. 6), indicating that the regional PIM differences observed were not a by-product of different whole muscle tension development between these separate sets of experiments.

Fig. 6. Left: mean peak PIM obtained in zones I, II, and III with "superficial" placement of needle transducer window (1 cm depth from muscle surface) and in same zones with "deep" placement (2 cm depth from muscle surface). * P <=  0.05 compared with superficial values in same zone; + P <=  0.05 compared with deep zone I. Right: whole muscle tension recorded in superficial (S) and deep (D) studies. P = NS.
[View Larger Version of this Image (29K GIF file)]

Changes in regional peak PIM and whole muscle tension with repetitive, fatiguing, isometric contractions are shown in Fig. 7. Figure 7D illustrates the change in peak tension over time observed in these studies, corresponding to ~50% loss of tension by minute 4. Means of regional peak PIM over time (Fig. 7A) again show that the highest values were recorded in zone II and the lowest values in zone I, although zone III attained the lowest absolute values of PIM toward the end of the fatigue trial. Normalization of PIM to initial values (Fig. 7C) shows that the greatest drops of PIM over time occurred in zones II (-74%) and III (-81%) over this same time period and that the pattern and magnitude of PIM loss in zone I (-60%) most closely approximated the pattern and magnitude of whole muscle tension loss. The recovery of regional PIM and whole muscle tension after fatigue is indicated in Table 1, which also shows the normalized initial and fatigue mean values for reference. Thirty minutes after the initiation of repetitive contractions (26 min after the final contraction of the fatigue trial), whole muscle tension had recovered to 78% of initial tension, a recovery of ~30% over the final fatigue value. At this same time, PIM in zone I had recovered to 61% of the initial value, displaying a 21% increase over its final fatigue value. PIM in zone III recovered to 51% of its initial value, representing an increase of ~30% over the final fatigue value, similar to the whole muscle tension recovery. Interestingly, PIM in zone II did not change within this time period. Recovery was further evaluated in three of these six muscles at 60 min, in which whole muscle tension further recovered to ~90% of initial tension. In these same muscles, PIM likewise further recovered, attaining values of 67%, 43%, and 86% of initial PIM in zones I, II, and III, respectively. Thus the greatest overall PIM recovery was observed in zone III, which had decreased by the greatest magnitude with fatigue and recovered to a level similar to that of whole muscle tension (~90%).

Fig. 7. A and B: changes in regional PIM and whole muscle tension, respectively, obtained during 4 min of repetitive tetanic isometric contractions at Lo showing means recorded at each minute of trial. C and D: fatigue shown as fatigue resistance index of PIM and whole muscle tension (T), respectively, expressed as a function of respective initial values (PIMi and Ti). Greatest loss of PIM occurs in zone III, and whole muscle tension fatigue magnitude and pattern are best reflected in zone I. * P <=  0.05 compared with initial mean value; + P <=  0.05 compared with zone III. v, P <=  0.05 compared with zone III.
[View Larger Version of this Image (24K GIF file)]

Table  1.   Tension and PIM percentages of initial values with fatigue and recovery
Fatigue
 Recovery
4 min (n = 6) 26 min (n = 6) 56 min (n = 3)
Tension 51 ± 6* 78 ± 6 89 ± 11
PIM
  Zone I 40 ± 5* 61 ± 9* 67 ± 7
  Zone II 26 ± 6* 27 ± 5* 43 ± 13
  Zone III 19 ± 6*, Dagger 51 ± 9*, dagger 86 ± 26
Values are means ± SE in percent. PIM, intramuscular pressure. * P <=  0.05 compared with initial value; dagger P <=  0.05 compared with fatigue; Dagger P < 0.05 compared with zone I.

DISCUSSION

The main findings of this study were 1) longitudinal and cross-sectional regionalization of PIM within the GP muscle group, 2) a significant effect of whole muscle length on the attained PIM within the zonal regions, 3) significant and different declines of PIM in regional zones during fatiguing, repetitive contractions that simultaneously produced significant loss of whole muscle tension, and 4) significant and different recovery of PIM in these zones after fatigue, during which recovery of whole muscle tension was essentially complete.

Critique of methods. The possibility for movement-related changes or artifacts in the PIM records during single and repetitive contractions is not insignificant in these studies. To minimize this possibility, isometric contractions were utilized (25). However, even with the precautions taken to minimize movement of the GP muscle origin (femur bone) and insertion (calcaneus tendon) toward each other, there remained a slight amount of metal support flexing and muscle shortening. We estimated the magnitude of shortening to be ~0.5 cm on the basis of visual observations that indicated 2-3 mm of movement of external muscle tissue at various loci. In a typical 10-cm-long canine GP muscle, this corresponds to a length change of ~5%, which agrees with the average of 4% shortening in this muscle measured by Gray et al. (10). However, there may be a significant amount of unobserved additional shortening within the muscle group. Given that some prior studies have concluded that PIM development should be higher if the muscle is allowed to shorten (20, 25), we must concede that one explanation for the magnitude of the observed values was internal shortening in the vicinity of the transducer sensor windows. Additional studies should be conducted in this muscle preparation to determine the regional PIM profile during contractions with significant external shortening, such as isotonic contractions.

Interestingly, some downward deflections of the pressure signal were observed during some contractions and transducer placements (Fig. 3). We interpreted these as the development of significant local negative pressure, in agreement with previous observations of negative PIM during contraction in the cat gastrocnemius muscle (6). The law of Laplace indicates that significant positive pressure is produced with compressive forces placed on a closed compartment (25). Conversely, external expansive forces should result in negative pressure production within a closed compartment. It is possible that such expansive forces could be produced by local lengthening of the muscle in the vicinity of the transducer, producing negative pressures either consistently or transiently, as shown by the PIM signal for zone II of Fig. 3. We did not evaluate these events systematically, because our emphasis was on attaining maximal positive PIM values. However, in conjunction with the regional PIM heterogeneity, findings such as these emphasize the point that a complicated mechanical heterogeneity exists that may have profound effects on local perfusion within the muscle group, as discussed below.

Another possible problem is that the loss of PIM observed with fatigue could be explained by progressive contraction-induced extrusion of the transducer outward to peripheral locations, resulting in declining PIM development with repeated contractions over time. The transducers were rarely observed to move outward from their original placement depth, as indicated by the marks we placed on the external casing (see above). Visual observation during the contractions indicated muscle actually clamping around the transducer casing as opposed to pushing it outward. The data from experiments in which outward movement was noted are not included in this study. Significant recovery of PIM shown in Table 1 also suggests that this problem was remote.

Finally, the synchronous, electrical stimulation of the present study is unlike asynchronous neural activation of muscle fibers in vivo. With simultaneous electrical activation, it is possible that the peak PIM values were produced more quickly than might otherwise occur. Thus high-amplitude, rapidly rising pressure waves may have resulted, in contrast to slower-developing pressure waves that might be produced with the graded production of force during asynchronous activation of motor units in vivo. This effect may or may not alter the attained PIM peak during an isometric contraction, depending on the duration of activation and duty cycle of the contractions.

Comparisons with previous studies. The following discussion provides some perspective about the present study of intramuscular pressures with regard to methods utilized and data reported. We agree with the assertion by Hussain and Magder (16) that part of the variability in reported PIM values is due to the methods employed in their measurement. A brief overview of these pressure measurement methods has been provided (16); therefore, we highlight only the aspects that are relevant to the present study. Furthermore, most of these studies measured tissue fluid pressure as opposed to total tissue pressure. Gray and Staub (11) reported 27-200 mmHg in the canine GP muscle group, using a vessel occlusion method, which in part relies on pressure equilibration within a relatively compliant muscle venous vasculature during contraction. However, they elicited only ~250 g/g of active tension with a 10-s, 30- to 40-Hz stimulus (11), which is about one-half of the tension developed in the present study (Fig. 6). In other muscles with complex architecture, average tissue fluid pressure values of 220 mmHg [rat gastrocnemius (23)] and 479 mmHg [human vastus medialis (21)] have been reported using fluid-filled open-needle methods. Hill (13) found 100-300 mmHg during isometric contraction in the frog gastrocnemius muscle by measuring thermal transients generated within an oil droplet at the end of an open needle. Others utilized balloon-type catheters placed within the muscle, which required prolonged contractions (21, 23, 29) and were subject to variation depending on the composition and other physical characteristics of the balloon (16). PIM values of 140 mmHg (20) and 300 mmHg (23) have been reported in the cat gastrocnemius muscle with use of these methods. In the parallel-fibered canine diaphragm, this method has produced values of 25 mmHg (29). Using solid-state transducers, Hussain and Magder reported 200 mmHg in the canine diaphragm muscle; this ~10-fold difference compared with the balloon-catheter study in that same muscle (29) is similar to the difference between our data and those of Petrofsky and Hendershot (23) in the gastrocnemius muscle.

Regional variations in PIM. One of the most interesting findings of the present study was that PIM was not uniformly distributed throughout the muscle but, rather, was consistently different in different areas of the medial head of the GP muscle group. Thus, similar to the assertion of Mazzella (20), the GP muscle group cannot be considered as one "simple fluid capsule" within which PIM development is uniform but, rather, is fractionated into areas of regional pressure pockets or stress development that are likely a function of its complex architecture. The magnitude of localized pressure or stress in this muscle group appears to be a function of muscle fiber length and subsequent tension development (Fig. 5), in agreement with earlier studies (16, 17, 20, 23, 25, 29). Our data indicate that the increase in PIM with increasing length and tension was best reflected in zone I, near the popliteal origin of the GP muscle group. We speculate that this may have occurred because the popliteal origin zone of the muscle group (zone I) represents the main anchor point of this preparation. This area is rigidly fixed by the tibia and fibula bone nails, possibly allowing more accurate transduction of PIM as length and force increased. This feature also may have limited internal shortening within this zone, producing lower PIM values (Fig. 6) (20, 25).

The data of Fig. 6 indicate that the highest pressures typically are generated deep in zones II and III. It is possible that the high pressures in zone III are due to the complex confluence of muscle fibers onto the calcaneus tendon in this region and the necessary transduction of force through this relatively noncompliant tissue. Because of this low compliance, stresses in this region may become high due to the presence of more "solid tissue," which can contribute to the development or magnification of high solid tissue pressures (12, 22). The highest pressures, deep in zone II, may be a function of muscle bulging that occurs during contraction, as the muscle shortens internally and presses against the rigid tibia and fibula bones. This possibility is supported by a report that the highest PIM measured in the contracting vastus medialis of humans (570 mmHg) was obtained near the femur bone (25). Evidence that this phenomenon may have occurred in the present study is shown in the zone II record of Fig. 3, which achieves high positive pressure after brief negative pressure development. These changes imply initial local lengthening followed by compression as the whole muscle bulged with contraction. It also may be due to shortening of the fibers from the origin and insertion toward the center (20, 25), producing magnification of stresses and compression along tendinous sheets within this region (22). The finding of greatest PIM in this region of the canine GP muscle also agrees with prior studies in the cat (23) and rat (17) gastrocnemius muscle.

Relationship of PIM to tension development. It is likely that our PIM measures reflect total tissue pressure, as defined by Guyton et al. (12), i.e., the sum of fluid and "solid pressures," developed during contraction. The solid pressures are due to fiber stresses that are produced perpendicular to the muscle fiber axis (16, 25) or possibly along the line of force development from origin to insertion of the muscle. Otten (22) stated that skeletal muscle tissue can produce stresses of 230 kPa (1,725 mmHg) at optimal sarcomere length, and he further stated that this is a factor of 10 above pressures reported by Petrofsky and Hendershot (23) in the cat gastrocnemius muscle. Inspection of Figs. 6 and 7 indicates that this was nearly the mean value measured in the present study, with deep placement in zone II (1,676 mmHg). Moreover, using a similar pressure transducer, Otten (22) observed pressures of 300 and ~1,000 mmHg in regions of the toad gastrocnemius muscle analogous to our deep zones I (500-600 mmHg) and III (~1,000 mmHg).

The discussion above indicates that the PIM values observed in the present study are consistent with values that would be expected within a muscle of complex architecture having significant fiber curvature (22). The relationship of the measured PIM values to whole muscle tension and regional stress development can be assessed by conversion of units and the use of pressure-stress relationships provided by Otten (22). Table 2 indicates the numerical mean PIM values measured for each zone (Fig. 6) converted to units of stress (22), with subsequent grand means of these values. The stress values were calculated on the basis of the following relationship
T = 2 ⋅ P (2)
where P is measured pressure and T is stress calculated for cylindrical muscles with extreme fiber curvature (22). The expected mean stress value (1.9 kg/cm2) correlates with an average PIM of 691 mmHg on the basis of a simple model in which each of the six compartments contributes equally to the whole muscle, or mean value. The whole muscle force per cross-sectional area, or stress, produced by the canine GP muscle during a tetanic isometric contraction was calculated (32) on the basis of whole muscle weight, length, and fiber pennation angle at Lo (20°) (1). Stress for a typical canine GP muscle producing 500 g/g of tension in this study was 1.7 kg/cm2, which is very close to the expected mean stress value based on the mean of regional PIM development. The similarity of these measured and calculated whole muscle stress values suggests that the regional forces summate to produce whole muscle forces and that regional or compartmental muscle stress can be assessed through measurement of regional PIM.

Table  2.   PIM and stress comparison
Superficial
 Deep
 Mean
Zone I Zone II Zone III Zone I Zone II Zone III
Measured regional PIM, mmHg 170 371 351 586 1,676 993 691
Calculated regional stress
  N/cm2 4.5 9.9 9.5 15.6 44.7 26.5 18.4
  kg/cm2 0.5 1.0 1.0 1.6 4.6 2.7 1.9
Whole muscle stress, kg/cm2 1.7
Stress values were calculated using 1.333 × 102 N · m-2 · mmHg PIM-1. Stress values are given in N/cm2 and kg/cm2 for ease of comparison with units commonly used in many muscle studies.

Effects of PIM on blood flow. The longitudinal and cross-sectional PIM differences may have great ramifications for the development of perfusion and performance heterogeneity in this muscle group. The high PIM values deep in zone II suggest that perfusion might be impeded most in this region. In support of this idea, the "central inner zone" of the rat gastrocnemius muscle was least perfused (31), with the highest tissue fluid pressures subsequently being found there (17). Similarly, regional muscle blood flow of the canine GP muscle was found to be lowest within the calcaneus tendon insertion region (24). This region is analogous to zone III, which demonstrated some of the high peak PIM values, the greatest decrease in PIM with fatigue, and the greatest increase in PIM with recovery, suggesting the potential of PIM effects on local flow-mediated mechanical output.

Increments in PIM have been correlated with decrements in whole muscle blood flow in rat (17, 31) and dog (10) skeletal muscle. Figures 3 and 4 suggest that PIM development is the driving force pushing blood out of this muscle. This indicates the large potential of the relationship between PIM and blood flow in the GP muscle, especially with respect to the venous pump mechanism known to be operational in limb muscles during exercise (19). As shown in Fig. 4, the typical intravenous pressure increase can be 20-50 mmHg above baseline (~5-10 mmHg) during these intense repetitive contractions, which meets or exceeds a theoretical value of ~20 mmHg necessary for venous flow to the heart.

We did not systematically measure flow changes induced by these contractions on the arterial side of the GP muscle. However, our method of determining whole muscle Q relies on the law of conservation of mass, which is assumed to be due to surgical ligation of all peripheral venous vessels except the popliteal vein. Thus, with regard to volume flow, what is observed to occur on the venous side can be considered a direct reflection of events on the arterial side. The cyclical changes in Q are therefore suggestive of cyclical hindrance of arterial blood flow, which has been observed to occur within the femoral artery of the canine GP muscle during tetanic (40- to 60-Hz) isometric contractions (18). It is likely that this occurred as a result of the high PIM values attained during contractions, which matched or greatly exceeded the MAP, possibly producing intermittent cessation of flow through the muscle and backflow toward the heart. Evidence of this behavior is shown in the arterial pressure tracing of Fig. 4B, showing arterial pressure increases in phase with the muscle contractions. When the contractions were in phase with the systolic pressure wave, some of these transients summed to produce higher pressure values within the arterial vasculature (18).

Implications for fatigue and recovery. Similar to our findings, Hill (13) observed different pressure magnitudes and consistent lowering of PIM during successive contractions for three of the four series of separate transducer placements reported in the frog gastrocnemius muscle. As shown in Fig. 7, the development of fatigue can alter the relationship between whole muscle tension and regional PIM in the canine GP muscle (16, 25). We postulate that one effect of fatigue is reduction of PIM toward levels near the MAP, allowing some maintenance of muscle perfusion and O2 delivery. The decrement in PIM as whole muscle tension decreased with fatigue should correspond to a reduction in the effects on the vasculature that limit blood flow. This postulate is supported by work showing that contraction-induced pressure transients within the femoral supply artery decrease with fatigue in the GP muscle (18). Furthermore, considered in conjunction with GP muscle studies showing perfusion heterogeneity (24), the regional PIM differences suggest that a metabolic or O2 supply heterogeneity may be produced because of physical limitations of local blood flow. Increased arterial perfusion pressure during muscle contractions, similar to arterial pressure increases reported with exercise in humans (9, 17), has been shown to lessen fatigue (5, 15, 23) and elevate O2 consumption significantly (5, 15), supporting this idea. Finally, the recovery data of Table 1 suggest that there is a complex summation of differences in local mechanical conditions that may play a role in the long-term recovery of whole muscle performance after intense exercise (3, 7). Thus we postulate that some regions recovering mechanical capacity more slowly may contribute to prolonged recovery of whole muscle function. Clearly, further experiments are necessary to determine the validity of these possibilities; however, this method of regional PIM assessment provides a way to quantify local mechanical events for their subsequent comparison with local perfusion and/or local metabolic events.

ACKNOWLEDGEMENTS

The authors gratefully acknowledge the critical review and consultation of Dr. Michael B. Reid and the technical assistance of Frank Phelps and Mark Barsic.

FOOTNOTES

   This work was supported by American Heart Association (Western Pennsylvania Affiliate) Grant BTA-52 and the Love Pulmonary Foundation (Pittsburgh, PA).

Address for reprint requests: B. T. Ameredes, Div. of Pulmonary, Allergy, and Critical Care Medicine, University of Pittsburgh, 440 Scaife Hall, 3550 Terrace St., Pittsburgh, PA 15261.

Received 26 March 1997; accepted in final form 31 July 1997.

REFERENCES

1. Allen, P. D. The Mechanical Properties of In Situ Dog Skeletal Muscle (PhD thesis). Gainesville: University of Florida, 1973.
2. Ameredes, B. T., W. F. Brechue, and W. N. Stainsby. Preload release increases muscle blood flow and decreases fatigue during repetitive isotonic muscle contractions. J. Appl. Physiol. 77: 2641-2647, 1994[Abstract/Free Full Text].
3. Baker, A. J., K. G. Kostov, R. G. Miller, and M. W. Weiner. Slow force recovery after long-duration exercise: metabolic and activation factors in muscle fatigue. J. Appl. Physiol. 74: 2294-2300, 1993[Abstract/Free Full Text].
4. Barcroft, H., and J. L. E. Millen. Blood flow through muscle during sustained contractions. J. Physiol. (Lond.) 97: 17-24, 1939.
5. Brechue, W. F., B. T. Ameredes, G. M. Andrew, and W. N. Stainsby. Blood flow elevation increases VO2 max during repetitive tetanic contractions of dog muscle in situ. J. Appl. Physiol. 74: 1499-1503, 1993[Abstract/Free Full Text].
6. Bridgman, C. F., and E. Eldred. Intramuscular pressure changes during contraction in relation to muscle spindles. Am. J. Physiol. 209: 891-899, 1965.
7. Edwards, R. H. T., D. K. Hill, D. A. Jones, and P. A. Merton. Fatigue of long duration in human skeletal muscle after exercise. J. Physiol. (Lond.) 272: 769-778, 1977[Abstract/Free Full Text].
8. Fales, J. T., S. A. Lillienthal, S. A. Talbot, and K. L. Zierler. A pneumatic isotonic lever system for dog skeletal muscle. J. Appl. Physiol. 13: 307-308, 1958[Free Full Text].
9. Friedman, D. B., C. Peel, and J. H. Mitchell. Cardiovascular responses to voluntary and nonvoluntary static exercise in humans. J. Appl. Physiol. 73: 1982-1985, 1992[Abstract/Free Full Text].
10. Gray, S. D., E. Carlsson, and N. C. Staub. Site of increased vascular resistance during isometric muscle contraction. Am. J. Physiol. 213: 683-689, 1967.
11. Gray, S. D., and N. C. Staub. Resistance to blood flow in leg muscles of dog during tetanic isometric contraction. Am. J. Physiol. 213: 677-682, 1967.
12. Guyton, A. C., H. J. Granger, and A. E. Taylor. Interstitial fluid pressure. Physiol. Rev. 51: 527-563, 1971.
13. Hill, A. V. The pressure developed in muscle during contraction. J. Physiol. (Lond.) 107: 518-526, 1948.
14. Hirche, H. J., W. K. Raff, and D. Grün. The resistance to blood flow in gastrocnemius of the dog during sustained and rhythmical isometric and isotonic contractions. Pflügers Arch. 314: 97-112, 1970[Medline].
15. Horstman, D. H., M. Gleser, and J. Delehunt. Effects of altering O2 delivery on VO2 of isolated working muscle. Am. J. Physiol. 230: 327-334, 1976.
16. Hussain, S. N. A., and S. Magder. Diaphragmatic intramuscular pressure in relation to tension, shortening, and blood flow. J. Appl. Physiol. 71: 159-167, 1991[Abstract/Free Full Text].
17. Kirkebø, A., and A. Wisnes. Regional tissue fluid pressure in rat calf muscle during sustained contraction or stretch. Acta Physiol. Scand. 114: 551-556, 1982[Medline].
18. Lambert, C. R., L. B. Gladden, W. M. Nichols, and C. J. Pepine. Effects of muscle contractions on pulsatile pressure-flow relationships in femoral bed. J. Appl. Physiol. 58: 1128-1135, 1985[Abstract/Free Full Text].
19. Laughlin, M. H. Skeletal muscle blood flow capacity: role of muscle pump in exercise hyperemia. J. Appl. Physiol. 61: 409-416, 1986[Abstract/Free Full Text].
20. Mazzella, H. On the pressure developed by the contraction of striated muscle and its influence on muscular contraction. Arch. Int. Physiol. 62: 334-347, 1954. [Medline]
21. Nilsson, B., and D. H. Ingvar. Intramuscular pressure and contractile strength related to muscle blood flow in man. Scand. J. Clin. Lab. Invest. Suppl. 99: 31-38, 1967[Medline].
22. Otten, E. Concepts and models of functional architecture in skeletal muscle. In: Exercise and Sports Science Reviews. New York: Macmillan, 1988, vol. 16, chapt. 3, p. 89-137.
23. Petrofsky, J. S., and D. M. Hendershot. The interrelationship between blood pressure, intramuscular pressure, and isometric endurance in fast- and slow-twitch skeletal muscle in the cat. Eur. J. Appl. Physiol. 53: 106-111, 1984.
24. Piiper, J., D. R. Pendergast, C. Marconi, M. Meyer, N. Heisler, and P. Cerretelli. Blood flow distribution in dog gastrocnemius muscle at rest and during stimulation. J. Appl. Physiol. 58: 2068-2074, 1985[Abstract/Free Full Text].
25. Sejersted, O. M., A. R. Hargens, K. R. Kordel, P. Blom, O. Jensen, and L. Hermansen. Intramuscular fluid pressure during isometric contraction of human skeletal muscle. J. Appl. Physiol. 56: 278-295, 1984[Abstract/Free Full Text].
26. Stainsby, W. N. Autoregulation of blood flow in skeletal muscle during increased metabolic activity. Am. J. Physiol. 202: 273-276, 1962.
27. Stainsby, W. N. Oxygen uptake for isotonic and isometric twitch contractions of dog skeletal muscle in situ. Am. J. Physiol. 219: 435-439, 1970.
28. Stainsby, W. N., and J. T. Fales. Oxygen uptake for isometric tetanic contractions of dog skeletal muscle in situ. Am. J. Physiol. 224: 687-691, 1973.
29. Supinski, G. S., A. F. DiMarco, and M. D. Altose. Effect of diaphragmatic contraction on intramuscular pressure and vascular impedance. J. Appl. Physiol. 68: 1486-1493, 1990[Abstract/Free Full Text].
30. Sylvest, O., and N. Hvid. Pressure measurements in human striated muscle during contraction. Acta Rheumatol. Scand. 5: 216-222, 1959[Medline].
31. Wisnes, A., and A. Kirkebø. Regional distribution of blood flow in calf muscles of rat during passive stretch and sustained contraction. Acta Physiol. Scand. 96: 256-266, 1976[Medline].
32. Woledge, R. N., A. Curtin, and E. Homsher. Initial facts and ideas. In: Energetic Aspects of Muscle Contraction, edited by R. Woledge, N. A. Curtin, and E. Homsher. London: Academic, 1985, chapt. 1, p. 1-26.
0161-7567/97 $5.00 Copyright © 1997 the American Physiological Society


This article has been cited by other articles:


Home page
 J. Appl. Physiol.Home page
J. Van Teeffelen, H. Vink, B. T. Ameredes, A. M. Jones, S. Egginton, L. F. Ferreira, G. W. Schmid-Schoenbein, W. L. Murfee, S. S. Segal, K. Tyml, et al.

J Appl Physiol, March 1, 2008; 104(3): 895 - 899.
[Full Text] [PDF]

Home page
 J. Appl. Physiol.Home page
D. M. Wigmore, B. M. Damon, D. M. Pober, and J. A. Kent-Braun
MRI measures of perfusion-related changes in human skeletal muscle during progressive contractions
J Appl Physiol, December 1, 2004; 97(6): 2385 - 2394.
[Abstract] [Full Text] [PDF]

Home page
 J. Appl. Physiol.Home page
M. Mizuno, K. Tokizawa, T. Iwakawa, and I. Muraoka
Inflection points of cardiovascular responses and oxygenation are correlated in the distal but not the proximal portions of muscle during incremental exercise
J Appl Physiol, September 1, 2004; 97(3): 867 - 873.
[Abstract] [Full Text] [PDF]

Home page
 J. Appl. Physiol.Home page
M. Mizuno, Y. Kimura, T. Iwakawa, K. Oda, K. Ishii, K. Ishiwata, Y. Nakamura, and I. Muraoka
Regional differences in blood flow and oxygen consumption in resting muscle and their relationship during recovery from exhaustive exercise
J Appl Physiol, December 1, 2003; 95(6): 2204 - 2210.
[Abstract] [Full Text]

Home page
 J. Appl. Physiol.Home page
J. L. Dobson and L. B. Gladden
Effect of rhythmic tetanic skeletal muscle contractions on peak muscle perfusion
J Appl Physiol, January 1, 2003; 94(1): 11 - 19.
[Abstract] [Full Text] [PDF]

Home page
 J. Appl. Physiol.Home page
L.-E. Chen, K. Liu, W.-N. Qi, E. Joneschild, X. Tan, A. V. Seaber, J. S. Stamler, and J. R. Urbaniak
Role of nitric oxide in vasodilation in upstream muscle during intermittent pneumatic compression
J Appl Physiol, February 1, 2002; 92(2): 559 - 566.
[Abstract] [Full Text] [PDF]

Home page
 J. Appl. Physiol.Home page
T. Muramatsu, T. Muraoka, Y. Kawakami, A. Shibayama, and T. Fukunaga
In vivo determination of fascicle curvature in contracting human skeletal muscles
J Appl Physiol, January 1, 2002; 92(1): 129 - 134.
[Abstract] [Full Text] [PDF]

Home page
 J. Appl. Physiol.Home page
B. T. Ameredes and M. A. Provenzano
Influence of nitric oxide on vascular resistance and muscle mechanics during tetanic contractions in situ
J Appl Physiol, July 1, 1999; 87(1): 142 - 151.
[Abstract] [Full Text] [PDF]

Home page
 J. Appl. Physiol.Home page
B. T. Ameredes, W. F. Brechue, and W. N. Stainsby
Mechanical and metabolic determination of VO2 and fatigue during repetitive isometric contractions in situ
J Appl Physiol, June 1, 1998; 84(6): 1909 - 1916.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Ameredes, B. T.
Right arrow Articles by Provenzano, M. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ameredes, B. T.
Right arrow Articles by Provenzano, M. A.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Visit Other APS Journals Online