Muscle Blood Flow Following Thermal Injury L. HOWARD AULICK, PH.D., Major, M.SC., DOUGLAS W. WILMORE, M.D., ARTHUR D. MASON, JR., M.D., BASIL A. PRUITT, JR., M.D., Colonel, M.C.

Peripheral circulation is markedly increased during the hyperdynamic-hypermetabolic phase of thermal injury and appears to be directed primarily to the burn wound. To determine whether any portion of this extra blood flow reaches another major peripheral vascular bed, blood flow in the tibialis anterior muscle of the lower leg was measured by 133Xe clearance in ten hemodynamically stable, nonseptic burn patients (mean burn size = 42.5% total body surface) and five control subjects. Muscle blood flow was 3.52 + 0.26 ml/100 gmin (mean + S.E.M.) in these patients and 3.29 + 0.24 in controls, indicating that resting muscle perfusion was unaffected by the extent of total body surface injury, size of leg burn, or elevated rectal temperature (38.2 + 0.2°C) of the patients. These results confirm the interpretations of previous studies suggesting that most of the increased peripheral blood flow following thermal injury is directed to the surface wound. Local and systemic factors responsible for the maintenance of muscle perfusion in the face of alterations in muscle metabolism following thermal injury are discussed.

D ERIPHERAL BLOOD FLOW iS markedly increased rduring the hyperdynamic-hypermetabolic phase of thermal injury.26'16 Direct measurements of total leg blood flow demonstrated that perfusion is essentially normal in uninjured limbs of burn patients but rises in a curvilinear fashion with the extent of local leg burn.2 While this finding suggests that peripheral blood flow is wound-directed, these whole-leg measurements do not permit assessment of the distribution of blood flow among the various limb components. The present study was designed to measure muscle blood flow in the legs of burned patients and relate this component of total limb perfusion to the extent of total body injury, size of burn on that leg, and central body temperature of the patient. Reprint requests: Library Branch, USA Institute of Surgical Research, Brooke Army Medical Center, Fort Sam Houston, Texas 78234. The opinions or assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting the views of the Department of the Army or the Department of Defense.

From the United States Army Institute of Surgical Research, Brooke Army Medical Center, Fort Sam Houston, Texas

Materials and Methods

Subjects Muscle blood flow was determined in ten burn patients (mean burn size = 42.5% total body surface, range 25.5-82%) and five normal controls. Since burn shock and the presence of a constrictive eschar or systemic "sepsis" has been shown to have a marked effect on muscle perfusion,5'12 all resuscitated patients were studied six to 28 days postinjury when such complications were not present. Patients were free of any pre-existing disease prior to injury; normotensive and hemodynamically stable, and in a normal state of hydration with an hematocrit above 33 and without abnormalities in serum electrolyte concentration, osmolality, or pH. Blood cultures, obtained on all patients before and after the study, were negative. Burn wounds were treated by the standard open method utilizing either topical application of silver sulfadiazine cream (Silvadene®, Marion Laboratory, Inc., Kansas City, Mo.) or 11% mafenide acetate (Sulfamylon®, Winthrop Laboratories, New York). All subjects were confined to bed for a minimum of one hour prior to muscle blood flow measurements. The actual studies took place in the Nuclear Medicine Clinic of the hospital where the ambient temperature was 25-27°. Since this was slightly below thermal neutrality for resting burned patients,17 patient comfort was achieved by covering them with light cotton blankets. All subjects rested supine throughout the 2030-minute study. Only those patients who rested quietly during the actual test, without any leg and/or foot movements, were included in this study. Muscle Blood Flow Determination Radioactive xenon gas (133Xe) was dissolved in sterile 0.9% NaCl solution to a concentration of 0.5-1.0 mc/

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ml, and 0.1-0.2 ml of this solution was injected 1-2 into the tibialis anterior muscle through a 25 gauge hypodermic needle. The disappearance of '33Xe was monitored for 20-30 minutes postinjection by a collimated scintillation probe placed directly over the injection site. Simultaneous measurements were performed on both legs in four control subjects and five patients. Muscle blood flow (MBF) was calculated from the tangent to the logarithmic curve of 133Xe washout as described by Lassen, et al.9 cm

MBF (mV1100 g muscle-min)

= r

100 Q(t)

where is the partition coefficient for 133Xe (amount of tracer in one gram of tissue/amount of tracer in one ml blood) and -dQ/dt Q(t) describes the clearance rate of 133Xe relative to the r

FLOW

779

amount present at time t; 0.70

for

r

was the value utilized in both control subjects and patients.

Results Resting skeletal muscle blood flow was essentially normal in this group of ten burn patients: 3.52 + 0.26 ml/100 g-min (mean + S.E.M.) as compared to 3.29+ 0.24 in controls (Table 1). Muscle blood flow was, therefore, unrelated to the size of total body surface injury (r2 = 0.02), extent of local limb injury (r2 = 0.004) or rectal temperature (r2 = 0.27) of the patient. The absence of a local burn effect on muscle perfusion was particularly evident from simultaneous measurements in patient 6, for this subject maintained comparable levels of muscle blood flow in both legs despite marked differences in the extent of limb injury (Table 1).

Discussion These muscle blood flow calculations in burned patients were based on the assumption that r, the par-

TABLE 1. Muscle Blood Flovw and Rectal Temperature of Controls and Burn Patients

Subject*

Age (Years)

Weight (kg)

Controls la b

36

79.5

25

75.0

30 26

81.8 75.0

29

65.9

29

75.4

c d 2a b c 3 4a b 5a b Mean

S.E.M. Patients* 6a b 7 8 9a b lOa b

PBD

Studied

% TBS Burn

% LS Burn

+

11 12a b 13 14

l5a b Mean + S.E.M.

47

82

13

25.5

46 22 19

108 52.7 72.3

10 8 12

27 33 37

34

86

28

38

48 18

73.6 72.7

11 8

40 40

27 22 19

72.6 65.9 58.6

6 20 13

49.5 51.5 82

30

74.4

13

42.5

* Icd, 2bc, 4ab, Sab, 6ab, 9ab, lOab, 12ab, and l5ab are simultaneous measurements in both legs. PBD-Postbum day: %

7.5 70 0 10 15 20 15 15 62.5 10 25 50 40 77.5 77.5 33

MBF

(ml/I00 g-min)

Tre (OC)

2.76 2.89 2.17 2.87 4.78 3.23 4.29 3.16 3.52 3.99 2.04 3.77 3.29

37.2 37.2 37.2

37.2

±0.24

±0.1

2.42 2.50 3.25 2.60 5.94 4.89 2.51 4.65 3.20 2.94 2.84 3.94 4.10 3.28 3.70 3.52 ± 0.26

37.8

37.0 37.6 36.8 37.3 36.9

37.9 38.7 39.0 39.4

38.1 38.0

38.3 39.2 39.0 +

TBS = %Totalbodysurface;%LS = %legsurface.MBF blood flow; T, Rectal Temperature. =

38.12 0.2 =

Muscle

780

Ann. Surg. * December 1978

AULICK AND OTHERS 50% TBS 50% LS

8.0

7.0

6.0 . __

E

0 cn

5.0

[

SKIN

a)

80%

rE

4.0 I 50% TBS LL. -J

NORMAL

I

C:)

3.0 I

CD

(-D LU J

2.0 [

1.0

0 TBS LS

= =

Total body surface burn Leg surface burn

FIG. 1. Distribution of leg blood flow following thermal injury.

tition coefficient for 133Xe, was unchanged in traumatized individuals. This assumption rests on the fact that, while possible changes in muscle and blood composition which occur following thermal injury may affect the relative solubility of this lipophilic tracer, these alterations are potentially offsetting and therefore do not appreciably alter r. For example, a one gram drop in hemoglobin concentration will increase by 2%, but the probable reduction in tissue fat content and elevation in muscle water content would decrease T.13 Patient hemoglobin values averaged 13.2 g/100 ml as compared with 14.1 g/100 ml for controls. Recalculating the blood flow to compensate for only the altered hemoglobin values by increasing T by 2-6% did not increase the calculated muscle blood flow values in patients significantly above normal. Therefore, the greatest possible difference in between these two groups was not of sufficient magnitude to affect data interpretation. r

r

The results of this study, then, clearly indicate that neither the extent or location of a thermal injury-has any net effect on resting muscle perfusion. The predicted normal values for muscle blood flow range between 2-4 ml/l00 g tissue -min since skeletal muscle represents 40-45% of the total body mass and receives 15-20% of the cardiac output in resting noninjured man. Average muscle blood flow in this group of burn patients was within these predicted limits, equal to that of control subjects and comparable to normal values reported by others,"12 using the same measurement approach. Therefore, unlike total limb perfusion, which varies with the extent of local injury,2 muscle blood flow is unrelated to the size of leg burn. These results confirm the interpretations of previous studies2'18 which suggested that most of the increased peripheral blood flow following thermal injury was directed to the surface wound.

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MUSCLE BLOOD FLOW

These peripheral blood flow measurements in burn patients make it possible to characterize the shift in limb perfusion following thermal injury (Fig. 1). Stolwijk14 has partitioned resting leg blood flow as follows: 29% to muscle, 46% to skin, and 25% to the remainder. Assuming that there is little or no change in muscle, fat, or bone perfusion, blood flow to the skin of an unburned leg, in a typical patient with a 50% total body surface burn, increases by no more than 7% above normal.2 Since this typical patient is febrile, with a rectal temperature ranging between 38390, the limited increase in superficial blood flow to the uninjured skin reflects appropriate cutaneous vasoconstriction for the generation and maintenance of a fever. This degree of hyperthermia in normal subjects, for example, would result in a five- to six-fold increase in cutaneous blood flow but would have no apparent effect on resting skeletal muscle perfusion.10 If this same burn patient (Fig. 1) had a wound covering 50% of the leg, limb blood flow would approach 8 ml/100 ml leg volume per minute.2 Since the size of limb burn has no effect on resting skeletal muscle blood flow, 80% of total leg flow in this patient is directed to the surface, with most of it going to the burn wound. Are the present findings of normal muscle blood flow consistent with information available on muscle metabolism in burn patients? Previous studies16 have demonstrated that leg oxygen consumption (VO2) may increase up to 90% in resting, nonshivering burn patients. A major portion of this extra VO2 must occur in skeletal muscle since 1) this tissue compartment makes up most of the limb's mass, 2) metabolic requirements of uninjured skin are minimal, and 3) the surface wound relies primarily on anaerobic glycolysis.'8 It is well established that a close relationship exists between muscle VO2 and blood flow in working muscles of normal man4'1 or resting muscles in hyperthyroid patients.8 These findings in burn patients suggest that muscle V02 is not associated with increases in tissue perfusion. Normal muscle circulation in the face of increased metabolic activity may be explained by the presence of competing systemic vasoconstrictor influences. Increased sympathetic activity and high levels of circulating catecholamines observed in burn patients'5 would provide a vasoconstrictor drive on the skeletal muscle vasculature. Since the vascular bed of skeletal muscle is a major site for compensatory adjustments to systemic arterial'1 and central venous pressure changes,4'7 such reflex vasoconstrictor drives may be active in these hyperdynamic patients with high wound blood flow. Any disparity between muscle metabolism and circulation would then reflect competition between local and systemic circulatory demands. Similar com-

petition has been observed in the working muscle of heat stressed normal man.10 In addition to the elevation in resting extremity VO2, proteolysis and amino acid release are increased in the limbs of these patients.3 The accelerated flux of amino acids (especially alanine) from these muscles with normal levels of perfusion is in direct contrast to reported increases in muscle proteolysis associated with elevated muscle blood flow in "septic" surgical patients.5 Consequently, at the present time it is difficult to establish a direct cause-and-effect relationship between muscle metabolism (V02 and proteolysis) and local blood flow in the various catabolic states of injured patients. In summary, muscle blood flow of the lower leg was normal in hypermetabolic burn patients and muscle perfusion was not affected by the local presence of a wound, changes in body temperature, or known alterations in muscle metabolism which accompany major catabolic injury. It should be re-emphasized that these studies were performed in resting muscle and elevations in blood flow were observed in patients excluded from this study with demonstrable limb movement. This study illustrates that burn patients without systemic infection can achieve a level of muscle perfusion consistent with local metabolic activity while satisfying other systemic, competing demands on the circulatory system. From a clinical standpoint, increases in muscle tone or frank shivering in critically ill, injured patients increase skeletal muscle perfusion and place even greater demands on the circulation of patients who already have high obligatory blood flow to the healing wound. Acknowledgments The authors express their appreciation to Alton W. Baker, M.D.. Chief of the Nuclear Medicine Section, Brooke Army Medical Center, Fort Sam Houston, Texas. who supplied consultative services, and Specialist-5 Thomas E. Smith. III. who provided the technical assistance which made this study possible.

References 1. Amery, A., Bossaert, H. and Verstraete, M.: Muscle Blood Flow in Normal and Hypertensive Subjects: Influence of Age, Exercise and Body position. Am. Heart J., 78:211, 1969. 2. Aulick, L. H., Wilmore, D. W., Mason, A. D., Jr. and Pruitt, B. A., Jr.: Influence of the Burn Wound on Peripheral Circulation in Thermally Injured Patients. Am. J. Physiol., 233(4):H520, 1977. 3. Aulick, L. H. and Wilmore, D. W.: Increased peripheral amino acid release following burn injury. In press, Surgery. 4. Barcroft, H.: Circulation in Skeletal Muscle. In Handbook of Physiology, Section 2, Vol. II. American Physiological Society, Washington, D.C. 1963, pp. 1353-1385. 5. Finley, R. J., Duff, J. H., Holliday, R. L., et al.: Capillary Muscle Blood Flow in Human Sepsis. Surgery, 78:87, 1975. 6. Gump, F. E., Price, J. B., Jr. and Kinney, J. M.: Blood Flow

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8. 9.

10. 11.

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and Oxygen Consumption in Patients with Severe Burns. Surg. Gynecol. Obstet., 130:23, 1970. Heistad, D. D. and Abboud, F. M.: Factors that Influence Blood Flow in Skeletal Muscle and Skin. Anesthesiology, 41:139, 1974. Kontos, H. A., Shapiro, W., Mauck, H. P., Jr., et al.: Mechanism of Certain Abnormalities of the Circulation to the Limbs in Thyrotoxicosis. J. Clin. Invest., 44:947, 1965. Lassen, N. A. and Lindbjerg, M. O.: Measurement of Blood Flow Through Skeletal Muscle by Intramuscular Injection of Xenon-133. Lancet, 1:686, 1964. Rowell, L. B.: Human Cardiovascular Adjustments to Exercise and Thermal Stress. Physiol. Rev., 54:75, 1974. Rowell, L. B.: Circulation to Skeletal Muscle. In Rush, T. C. and Patton, H. D., eds., Physiology and Biophysics: Circulation, Respiration and Fluid Balance. Philadelphia, W. B. Saunders, 1974, pp. 200-214. Russell, H. E., Hartford, C. E., Boyd, W. C. and Barnes, R. W.: Muscle Blood Flow in Circumferentially Burned Extremities. Surg. Forum, 26:71, 1975.

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13. Sejrsen, P.: Measurement of Cutaneous Blood Flow by Freely Diffusible Radioactive Isotopes. Dan. Med. Bull., (Suppl) 18: 1, 1971. 14. Stolwijk, J. A. J.: Mathematical Model of Thermoregulation. In Hardy, J. D., Gagge, A. P., and Stolwijk, J. A. J., eds., Physiological and Behavioral Temperature Regulation. Springfield, Charles C Thomas, 1970, pp. 703-721. 15. Wilmore, D. W., Long, J. M., Mason, A. D., Jr., et al.: Catecholamines: Mediator of the Hypermetabolic Response to Thermal Injury. Ann. Surg., 180:653, 1974. 16. Wilmore, D. W., Mason, A. D., Jr., Johnson, D. W. and Pruitt, B. A., Jr.: Effect of Ambient Temperature on Heat Production and Heat Loss in Burn Patients. J. Appl. Physiol., 38: 593, 1975. 17. Wilmore, D. W., Orcutt, T. W., Mason, A. D., Jr. and Pruitt, B. A., Jr.: Alterations in Hypothalamic Function Following Thermal Injury. J. Trauma, 15:697, 1975. 18. Wilmore, D. W., Aulick, L. H., Mason, A. D., Jr. and Pruitt, B. A., Jr.: Influence of the Burn Wound on Local and Systemic Responses to Injury. Ann. Surg., 186:444, 1977.

Muscle blood flow following thermal injury.

Muscle Blood Flow Following Thermal Injury L. HOWARD AULICK, PH.D., Major, M.SC., DOUGLAS W. WILMORE, M.D., ARTHUR D. MASON, JR., M.D., BASIL A. PRUIT...
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