Respiratory and cardiac effects on venous return

Fundamentals of clinical cardiology

Respiratory

and

cardiac

effects

on venous

return

Francis L. Abel, M.D., Ph.D.* John A. Waldhausen, M.D.** Indianapolis, Ind.

C

ardiac output is influenced by a variety of controlling mechanisms. However, it is self-evident that the heart can pump only the blood it receives. Although minor discrepancies may exist from beat to beat, the average volume of venous return determines the cardiac output. Venous return itself is controlled by complex mechanisms including, among others, venous tone, heterometric autoregulation, transmitted arterial pressure, tissue pressure, and feedback control systems. The factors lying distal to the capillary are nevertheless of fundamental and quantitative importance in affecting venous return and therefore cardiac output. This study will review two of the prominent factors that alter venous return : respiratory activity and the direct, vis d fro&et influences of cardiac action itself. Both respiratory and cardiac activity will be presented in terms of their influence on normal venous flow in the thoracic inferior and superior venae cavae. In addition, alterations in normal venous return produced by anesthesia, positive pressure ventilation, thoracotomy, and changes in posture will be From

the Departments of Physiology and Medicine, Indianapolis. Ind. Supported by Grants HE 08042. HE 10659, Health Service. *Reprint requests to: Dr. Abel, Department St.. Indianapolis, Ind. 46202. **Recipient of U. S. Public Health Service Hospital of the University of Pennsylvania, tForce from in front.

266

American Heart Journal

Surgery

described. The dog was the experimental animal used in the studies to be presented. Normal

flow

patterns

Several authorsl-4 have described the pulsatile pattern of thoracic vena caval flow. Although this pattern is due to several factors, respiratory effects predominate in the closed-chest, normal animal. These effects result in a large increase in flow during inspiration, with return to a fairly constant flow level during expiration. As might be expected, the variations due to respiration are usually more pronounced in the inferior thoracic vena cava than in the superior cava, partially due to the combined effect of the pumping action of the abdominal and thoracic musculature on inferior caval Aow and probably, also, in part due to a greater tendency for the superior caval veins to collapse during inspiration. The latter occurs more readily at the point where the great veins enter the thorax.5 If, however, the negative pressure in the thorax is removed by opening the chest cavity, the positive abdominal pressure still rhythmically influences inferior caval and

the

Heart

Research

and H 6308 from the National of Physiology,

Indiana

Career Development Philadelphia, Pa.

Center, Institutes

University Award. 19104.

August, 1969

University

of Health.

Medical Current

Indiana

United

Center,

address:

School States

1100 West

Department

of

Public

Michigan of Surgery,

Vol. 78, No. 2, pp. 266-275

Kespirufory

flow, whereas superior caval flow becomes independent of respiration.’ Some authors have also postulated that the descent of the diaphragm may partially compress hepatic and portal veins,* although the intrahepatic veins resist collapse.6 This mechanism, however, has not been clearly demonstrated in the unanesthetized animal. Superimposed on the variations in central venous flow due to respiration are the effects of cardiac activity (vis dfronte). These may be seen more easily in the open-chest animal, but frequently can also be clearly discerned in an animal with relatively slow, shallow respirations. The alterations produced consist of two prominent decreases in flow associated with atria1 contraction and with the mid-portion of ventricular systole when atria1 venous pressure is increasing (the V wave of venous pressure). The decrease in venous flow associated with atria1 contraction often is so large as to result in a negative or backward flow of blood in the cavae immediately adjacent to the right atrium. This regurgitant flow

cd

currlic~c

e.fects

on

venom

refurrl

267

tends to be more prominent in the inferior than in the superior vena cava, but may be seen in both. The anatomical llianner of opening of the superior cava into the right atrium may result in a more physiologicallq effective valve than the Eustachian valve at the entrance of the inferior cave into the atrium. If the veins are filled more completely, as just after an inspiratory effort, the backward flow due to atria1 contraction is more pronounced and decreases during the expiratory period. There are likewise two periods of increased forward flow associated with the cardiac cycle. These are associated primarily with the descent of the base of the heart during the early phase of rapid ejection and with the opening of the right atrioventricular valve and the rapid inflow phase of the cardiac circle. Smaller effects are associated with the bulging of the tricuspid valve into the right atrium during isovolumetric contraction (decreased tlow) and with the reduced inflow phase (neat-l>, constant flow). Obviousi! , thert*fore, lhe

I;ig. 1. Pulsatile flow tracings obtained from a dog with implanted Aowmeter probes on the S\‘(, I\‘C, and aorta and a Silastic catheter in the right atrium. The animal has received morphine sulfate to produce a slower heart rate. Right panel several minutes later. Time marks in second>. fnspiration is an upward deAet.tion.

268

Fig. 2, upward

Am. Heart 1. August, 1969

Abel and Waldhausen

A. Effects

of panting

on flow

in the unanesthetized

animal.

Time

marks

in seconds;

inspiration

is an

deflection.

Fig. 2, B. Effects of whining on IVC flow. The inspiratory prolonged whining at the right of the figure. seen during

gasps and the corresponding flow Time marks in seconds; inspiration

changes upward.

may

be

Volume Number

78 2

Respiratory

classical vis d fronte has both positive and negative components associated with its total effect on venous return to the right heart. Fig. 1 illustrates the typical pulsatile flow patterns seen in the unanesthetized animal with electromagnetic flow probes chronically implanted. The variations in superior vena caval (SVC) and inferior vena caval (IIrC) flow occurring during the cardiac cycle are shown. Timing may be obtained from the EKG tracing. Vertical lines show the onset of atria1 systole (A), ventricular systole (I?), and ventricular diastole (C). The alterations produced by the slower respiratory activity may be seen in the slower tracing on the right. Also shown are the decreased flows (often actually backward flows) occurring during atria1 systole. The decreases are more prominent after each inspiration, presumably due to more complete atria1 filling, increased atria1 pressure, and an associated increase in the force of atria1 contraction. The presence of more blood in the vena cava at this time may alsc contribute to a more circular

Fig. 3. Effects ume integrator

of excitement on WC and aortic flows to reret properly produced the artifact

and cardiac effects on venous return

269

cross-sectional area and a decrease in venous resistance.’ Two observations regarding the type of caval flow pattern seen in Fig. 1 are in order: The flow patterns strongly resemble inverted tracings of right atria1 pressure. Although a longitudinal intravascular AP is not evidently an important control factor in venous flo~,~ as is the mean level of venous pressure,’ it is apparent that flow and right atria1 pressure are being influenced by the same factors, e.g., valve closure, A-V ring movement, etc. Interestingly, the venous flow pattern, when primarily determined by cardiac activity as in this instance, also resembles coronary arterial flow tracings.8 Obviously this is because the timing of the events of the cardiac cycle that influence coronary flow, although in an entirely different manner, are the same for venous flow as for coronary flow. Hence, venous return and coronary flow both decrease during isovolumetric contraction and reduced ejection; both increase during early diastole. The normal flow patterns discussed above

in the unanesthetized seen in that tracing.

animal.

Failure

of the stroke

vol-

270

Fig.

Am. Heart I. August, 1969

Abel and Waldhausen

4,

A. Transient

influence

of changes

Fig. 4, B. Influence of elevating the d&s front : legs approximately 30 degrees from

in posture

on caval

and aortic

Rows.

front or hind legs on caval and aortic flows. horizontal, forcing animal to support himself

Assistant lifted hind on remaining legs.

or

Kes~irutory

are seen in the quiet animal lying in the prone position. Any alteration in either cardiac or respiratory activity will significantly influence the flow pattern. Fig. 2 illustrates some normal patterns which may be seen as a result of panting (A) and of a positive Valsalva effort (whining, B). Similarly some effects of changes in posture and excitement are shown in Figs. 3 and 4. Mean

flows

While the above patterns of flow are important and provide a fairly accurate picture of someof the forces involved in venous return, it is the overall mean flow level that determines the amount of blood brought to the heart, and therefore cardiac output, over any period of time. Estimates of the distribution of venous return between the superior cava and the inferior cava have been few. Folkow and associates9state that 65 per cent of the cardiac output returns via the inferior cava. In chronically implanted animals, with the azygos vein tied, we have obtained mean values for inferior caval flow

cd

cardiac

eflects bn venous

return

271

of 57 per cent of cardiac output in the prone animal.*O The cardiac output in that group averaged 118 ml. per kilogram per minute. With changes in posture, such as sitting, standing, and 20 degree head-up and headdown tilting, the percentage of venous flow returning via the superior and inferior thoracic venae cavae remained essentially unchanged. Cardiac output was significantly higher only during standing, but was unchanged by sitting or passive tilting, despite significant changes in stroke volume and heart rate. These data indicate that gravity plays little role in normal venous return, probably due to the presence of t; tubes in the circulatory system, the forces cancelling in such a system.’ Other factors then serve to maintain the venous return in situations such as changes in posture and passive tilting. These factors apparently maintain venous return despite rather large changes in heart rate indicating that cardiac (vis $ fronfe) factors are probably not of major importance in determining overall mean flow levels. When the ;tMominal-

Fig. 5. Immediate effects of intravenous injection of an anesthetizing (15 mg. per kilogram). Animal premeditated with droperidol-fentanyl

dose of sodium citrate (0.13

pentobarbital (Nembutal) ml. per kilogram).

272

Abel and Waldhausen

Am. Heart I. August, 1969

thoracic pump was altered, however, by means of a positive pressure ventilator (see below), an immediate alteration in venous flow occurred, indicating the relative importance of this mechanism. Effects

of anesthesia

When the dog is given sodium pentobarbital, there is an immediate increase in heart rate and decrease in stroke volume. Although the changes in cardiac output are not consistent, there is probably a significant decrease.ir-I3 Fig. 5 shows a typical response to the injection of sodium pentobarbital. There is an immediate increase in heart rate and decrease in stroke volume. IVC flow increased, and with a decrease or no change in overall cardiac output, it now represents 69 per cent of the cardiac output instead of the 57 per cent seen in the normal dog.” SVC flow has, therefore, decreased. Whether this represents a decrease in muscle activity of the head and neck, a decrease in cerebral blood flow, or alterations due to a change in respiratory activity, e.g., collapse of superior caval vessels due to suction, remains undetermined. Although other anesthetics have been studied as to their hemodynamic effects, essentially no studies have been made of their influence on venous return. Respiration often temporarily ceases or becomes very shallow immediately after pentobarbital injection, during which time cardiac effects dominate the venous flow patterns.” Later on, the respiration is deep, slow, and regular, producing the pattern of venous flow shown in the left panel of Fig. 7, A. Abdominal-thoracic pump During head-up tilting the role of the abdominal-thoracic pump in venous return tends to be accentuated. This is particularly apparent in the anesthetized animal, or in the animal that has been placed under sufficient stress to develop the abdominal compression reaction-a strong contraction of the abdominal muscles during the expiratory phase of respiration.‘* Fig. 6,A shows the influence of this phenomena. A major proportion of inferior caval flow now occurs during inspiration with a pronounced decrease just after each inspira-

Fig. 6, A. Effects of the abdominal compression reaction on IVC flow in the anesthetized dog. Intraabdominal pressure, obtained from balloon in the peritoneal cavity, not calibrated.

tion. The intra-abdominal pressure tracing indicates the contraction of the abdominal muscle by a rise in pressure during expiration. It has been suggested that this reaction serves to pump blood from the abdomen into the thorax14; there is a slight but certainly not prominent increase in IVC flow accompanying this reaction. A similar reaction has not been reported in man, although it may represent a variation of abdominal breathing. That intermittent abdominal pressure can play a marked role in venous return is shown in Fig. 6, B, in which the abdomen was manually squeezed. Steady abdominal pressure has a similar immediate effect. (Use of a binder, however, was not associated with a sustained increase in venous flow levels.) Effects of positive pressure ventilation and thoracotomy When the anesthetized animal is ventilated by mechanical positive pressure, a marked alteration in the pattern of venous return occurs, primarily in relation to the pattern due to respiratory activity. Such a sequence is shown in Fig. 7, A. Inspiration no longer produces the influx of blood previously seen, rather there is an actual

Fig. 6, B. Effects flow .. Bag attached

of manually compressing the abdomen, intermittently to endotracheal tube was occluded, raising intrathoracic

Fig. 7, 8. Effects of attaching endotracheal tube of spontaneously veni tilator. Inspiration is an upward deflection in the pneumograph J. A,ppl. Physiol. 25:479, 1968.)

and sustained, on IVC and pressure, in right panel.

respiring tracing.

animal (From

aortic

to a positive pressure Abel and Lvaldhausen:

274

Am. Heart I. August, 1969

Abel and Waldhausen

Fig. 7, B. Left panel: Effects attached to positive pressure off, inspiratory and vasomotor

of acute bilateral thoracotomy on IVC and aortic flows. Middle panel: ventilator. Inspiration is an upward deflection. Right panel: Ventilator effort occurred just before ventilator was restarted.

decrease in thoracic venous flow accompanying the positive pressure produced by the ventilator. Flow then returns to a stable level during expiration. Superimposed are the cardiac effects as previously described. As might be expected, this decrease or reversal of the normal abdominal-thoracic pump pressure gradient results in a decrease in cardiac output; this amounts to about 13 per cent with even fairly minimal lung volumes. lr IVC and WC flow in this situation decreased proportionately. At present there is little quantitative information relating the magnitude of the alteration in intrathoracic pressure with cardiac output and venous return. Preliminary studiesn suggest a linear relationship between the decrease in cardiac output and the increase in intrathoracic pressure. This would be expected, of course, only if the veins involved are operating at nearly constant cross-sectional dimensions, as the changes in resistance associated with a change in diameter or shape in the veins might well be greater than that associated with the changes in pressure gradients.2 Increasing the intrathoracic pressure, however, by occlusion of the ventilation bag results in an immediate decrease in venous flow and cardiac output (Fig. 6, B).

Animal turned

Thoracotomy removes the positive intrathoracic pressure while retaining the effects of abdominal pressure (Fig. 7, B). The influence of ventilation should no longer be seen on the venous flows, unless the animal is spontaneously respiring in which case abdominal respiration will still influence IVC flow.’ We have not, however, found any appreciable immediate alteration in cardiac output or IVC flow as a result of acutely opening the chest (versus the carefully ventilated animal).11 Summary Cardiac activity and respiration markedly alter the venous ilow patterns in the major thoracic systemic veins. Cardiac activity (vis d fronte) is associated with two periods of increased and two periods of decreased venous flow, corresponding to changes in atria1 pressure. Respiratory activity predominates in most instances, however, producing a large increase in venous return during inspiration. Alterations in respiratory activity produced by procedures such as positive pressure ventilation, airway occlusion, whining, etc., cause much greater changes in venous return and cardiac output than do changes in posture or passive tilting. Excitement, exercise,

Respiratory

and pentobarbital anesthesia can produce marked changes in venous return. Pentobarbital can increase the percentage of blood returning to the right heart via the inferior vena cava. Gravity apparently is relatively unimportant in returning blood to the heart.

and cardiac effects on wenous retzmn

8.

9.

REFERENCES 1.

Brecher, Grune

2.

3.

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5.

6.

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8

G. A. : Venous return, New York, Stratton, Inc., pp. 15-17,

1956, 54-57,

71-114. Morgan, B. C., Abel, F. L., Mullins, G. L., and Guntheroth, W. G.: Flow patterns in cavae, pulmonary artery, pulmonary vein, and aorta in intact dog, Am. J. Physiol. 210:903, 1966. Moreno, A. H., Burchell, A. R., Van Der Woude, R., and Burke, J. H.: Respiratory regulation of splanchnic and systemic venous return, Am. J. Physiol. 213:4.55, 1967. Pinkerson, A. L., Luria, M. H., and Freis, E. D.: Effect of cardiac rhythm on vena caval blood Rows, Am. J. Physiol. 210:505, 1966. Alexander, R. S. : The peripheral venous system, in Hamilton, W. F., and Dow, P., editors: Handbook of physiology, section 2, Circulation, vol. 2. Baltimore. 1963. American Phvsiological Socieiy, The Williams & Wilkins Co.; pp. 1%791082. Guyton, A. C., and Adkins, L. H. : Quantitative aspects of the collapse factor in relation to venous return, Am. J. Physiol. 177:523, 1954. Guyton, A. C.: Circulatory physiology: Cardiac output and its regulation, Philadelphia, 1963, \I:. B. Saunders Company, pp. 1’17-184.

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Gregg, D. E., and Fisher, L. C.: Blood supply to the heart, in Hamilton, W. F., and Dow, P., editors: Handbook of physiology, section 2, Circulation, vol. 2, Baltimore, 1963, American Physiological Society, The \Villiants & Wilkins Co., pp. 1533-1534. Folkow, B., Heymans, C., and Neil, E.: Integrated aspects of cardiovascular regulation, in Hamilton, W. F.. and Dow, P., editors: Handbook of physiology, section 2, Circulation, vol. 3. Baltimore. 1963. American Phvsiolop-ical Sbciety, The iVillia& & Wilkins Co..-pp. l&19. Abel, F. L., and Waldhausen, J. ,2.: Influence of posture and passive tilting on venous return and cardiac output, Am. J. Phyaiol. 215:1058, 1968. Abel, F. L., and Waldhausen, j. A.: Elfects of anesthesia and artificial ventilation on caval flow and cardiac output, J. Appl. Physiol. 25:479, 1968. Olmsted, F., and Page, 1. I-1.: Hemodynamic changes in dogs caused by sodium pentobarbital anesthesia, Am. J. Physiol. 210:817, 1966. Gilmore, J. P. : Pentobarbital sodium anesthesia in the dog, Am. J. Physiol. 209:404, 1965. Youmans, W. B., -Murphy, Q. R., Turner, J. K., Davis, L. D., Briggs, D. I., and Hoye, X. S.: Activity of abdominal muscles elicited from the circulatory system, Am. J. Physical bled. 42:1, 1963. Morgan, B. C., Martin, \V. E., Hornb:~in. T. F., and Guntheroth, \\:. G.: Crawford, E. u’., Hemodynamic effects of intermittent positive pressure respiration, Anesthesiolcgy 27:.584, 1966.