Thorax (1960), 15, 47

ENERGY SOURCES OF BLOOD CIRCULATION ANDTHE MECHANICAL ACTION OF THE HEART*

BY

LEON MANTEUFFEL-SZOEGEFrom the Surgical Department of the Wolski Hospital, Warsaw, Poland

(RECEIVED FOR PUBLICATION AUGUST 12, 1959)

The principle that " the movement of the bloodis maintained by the heart which acts as a pump"continues to be binding in modern physiology(Evans, 1952). Certain doubts, however, appearwhen the power of the heart muscle is regardedas the exclusive or even the main source of energyfor the whole cardiovascular system. The questionmay be asked, Is there no other motive force in thecirculatory system, besides the heart muscle, thatmight be significant ? It is not easy to reconcilethe principle of the dominant role of the heart,in the circulation, with the fact of the existence ofthe venous return energy, but one example fromthe field of cardiovascular surgery may illustratethat role.

Fig. 1 is an angiogram of a patient with ananastomosis between the superior vena cava andthe right pulmonary artery. (The patient wasoperated on by Dr. Glenn from New Haven,Connecticut, U.S.A.) It was a case of completetransposition of the great vessels with stenosis ofthe pulmonary artery, and after the operation agreat improvement in the patient's condition wasobserved.

It is difficult to understand the haemodynamicsof this part of the patient's circulation, where thesystemic venous circulation is connected directly-by-passing the heart-with the arterial pul-monary circulation. How is it possible for theblood, pumped by the heart, impeded by the densenet of capillaries, to cross them and still retainenough energy to pass the second " filter " of thepulmonary capillaries as happened in Dr. Glenn's(1958) case ?The energy of the venous blood flow can hardly

be explained by the small resistance of thecapillaries. On the contrary, it seems that thestrength of the resistance met by the blood duringits passage through the capillaries is underesti-

*This work was supported by a grant from the Polish Academyof Scicnces.

D

mated in the teaching of physiology. This problemcan be illustrated by the following experiment:Water from reservoir A (Fig. 2) flows out through

tube B with a certain velocity. In the course oftube B is reservoir C. If reservoir C is filled(Fig. 3) with a rather tightly packed rubber sponge,the water outflow from tube C will be diminishedmany times.For our experiment, we used reservoir A of 8

litres capacity, the pressure of the water columnwas about 120 cm., the capacity of reservoir C was3 litres, and the diameter of tube B was 1.2 cm.;when a 9 cm. thick rubber sponge was put intoreservoir C the flow of the water out of the systemwas immediately diminished at least six times,depending upon the position of the sponge. Thepressure at the tube C outlet was barely measurable.

FIG. 1.-Angiography of the patient with anastomosis between thesuperior vena cava and the right pulmonary artery. (By courtesyof Dr. Glenn.)

LEON MANTEUFFEL-SZOEGE

FIG. 2.-This figure represents reservoir A___ _ ~~~with tube B and additional reservoir C._ -__ The outflow of the water is free.

_ A n-

-~~~~~~(>

.~~~~___

_~~~~~~~~~~~~~~~~~~~___=

This experiment shows, in a simple analogy, therole of the capillaries as an important source ofresistance to the blood flow. The sponge representsthe capillaries, with the reservation that, thoughthe resistance in the experiment has some elasticity,it does not have the same characteristics as thecapillaries have in a living organism. Conse-quently one is led to believe that the estimationof the hydrodynamic conditions in the circulationis based on an erroneous assessment of theresistance existing in the system. The resistanceis calculated on the basis of the height of thepressure existing in particular parts of the circula-tory system as well as by the amount of bloodflowing through the system. In this calculationonly the work done by the heart is considered andno notice is taken of the possible existence ofother, additional, sources of energy in the circula-tion. It might be supposed that the additionalsources are particularly active in the territory ofthe capillaries, which makes the passage of bloodquicker. Th8 action of additional energy wouldresult in a spurious diminishing of the resistanceof the circulation, and the vis a tergo of the heartwould then have less work to do.

It seems that a much higher pressure would beneeded in the circulation of living organisms tomove so much blood through the capillaries withina limited time. The efficiency of the circulation

FIG. 3.-The identical construction asin Fig. 2. A rubber sponge has

_ _ _-been put into reservoir C. The=---.- water outflow is considerably

impeded.

lt!%Fj

can be so great only because of some additionalsource of energy.

In an attempt to clarify these problems, a seriesof observations on the circulatory systems of 3-and 4-day-old hen embryos (Manteuffel-Szoege,Turski, and Grundman, 1959) was made. We hadassumed that the embryonic circulation, which isat that time already well developed, contains thesame, if one may say so, essential phenomenon ofthe circulation as can be found in adults. Theembryonic circulatory system has the advantageof being " simplified " and free of a number ofmechanical complexities characteristic of the adultorganism. It is in a sense a true biological" model " of the circulatory system in an adult.At the four-day-old stage of development thelung circulation does not exist; the heartconsists of one ventricle and one atrium and ithas no valves (Fig. 4). The force of gravitationneed not be taken into account because the embryo.together with its extra-embryonic circulatorysystem, is a flat disc lying at one level, and thecirculatory system can easily be seen through amagnifying glass either as a whole or in largefragments. Using a special thermostat we wereable to observe the embryos at definite temper-atures (Fig. 5).We established that in hypothermia the venous

system reacts first. The circulation slows down

48

ENERGY SOURCES OF BLOOD CIRCULA TION

and finally stops earlier than in the arterialsystem. The venous circulation stops completelyat a temperature of 20-250 C. At thesame temperature the arterial circulation showsan oscillating but not progressive movement, i.e.,after every systole the blood moves forward a littleand then returns to the initial point; in otherwords, at a temperature of 20-25° C., the bloodcirculation is interrupted, but the oscillating move-ment in the main arteries continues. The heartbeat usually stops at a temperature lower than200 C. The heart rate decreases in directproportion to the lowering of the temperature. Ifan embryo is left for from 30 to 90 minutes at atemperature in which the venous circulation hasstopped but the heart is still beating, it can beseen that the blood begins to collect in the regionsof the peripheral parts of the extra-embryonicarterial system, producing capillary overfilling.

Also, we noticed a number of phenomena inconnexion with mechanical manipulations on theembryo. We cut the heart of an embryo fromthe great vessels, thus producing haemorrhage.The venous circulation or, strictly speaking, theblood movement in the veins during haemorrhagein the conditions of normothermia continues in3- to 4-day-old embryos for more than 10 orsometimes even for 15 minutes. The fact shouldbe stressed that in these conditions no return spurtis found and there is no haemorrhage from thearteries. There is venous bleeding, whereas in theperipheral arteries the movement of the blood iscentrifugal.The following conclusions suggest themselves:

The blood seems to possess another source ofenergy besides that imparted to it by the heart.This additional energy manifests itself withparticular clarity in the venous circulatory system,a conclusion supported by our observations thatin hypothermia the venous circulatory systemstops first while the heart is still beating. Intemperatures of 20 to 25° C. the action of theheart still produces inefficient, oscillating bloodmovement in the arteries.

In other words, the hypothesis may be put for-ward that there exist two different energymoments in blood circulation-one that can beobserved in the arterial system, and this isdependent on the action of the heart; and theother, an additional one that manifests itself, aboveall, in the kinetic energy of the venous circulationsystem.

The conception that there exists an additionalenergy moment is also favoured by the fact thatthe venous circulation continues for a long time

*v.xvR g;_

FIG. 4.-A 5-day-old chicken embryo. Note the big extra-embryoniccirculation.

FIG. 5.-Thermostat used for embryonic circulation examinations.

simultaneously with the haemorrhage of anembryo. If the haemorrhage from an embryoafter its destruction (cutting out of the heart) werea strictly mechanical problem, it would not lastas long as 20 minutes.

49

LEON MANTEUFFEL-SZOEGE

20 30 40TEMPERATURE *C

FiG. 6.-Correlation between blood and plasma viscosity and tem-Pre-. eq~ v'iscosity of-blood,- botto'mpcraturov urve representsheoip

curve that of plasma.

1-5-

C1)f--J 1-3-

I-

wlJ 1-2

w,, 1 1-

TEMPERATURE CFio. 7.-Relation between viscosity and friction-work (in formula:

logarithm of viscosity-inverse of temperature) regardingtemperature up to 370 C. Curve 1 refers to blood, curverefers to plasma.

It has to be added that during very exactobservation of the extra-embryonal circulation,especially the venous and capillary parts of it, novasomotor motility could be seen that could beconsidered as an energy factor causing the bloodflow. The blood flow seems to be independent ofany external factors.

If it is assumed that the conception of the above-mentioned additional energy of the circulation istrue, the question must inevitably follow, What isthe character of this energy ? I submit that thecirculation is inseparably connected with thethermal conditions of the subject.

It is well known that the circulation, particularlyin thermo-stable organisms, can take place onlyunder certain optimum conditions of temperature,and the thermal conditions for circulation havebecome particularly conspicuous recently owing tostudies on hypothermia. In connexion with thequestion of hypothermia I draw the attention ofthe reader to the fact that the blood viscosity isinfluenced by lowering of the temperature. Tounderstand the problem better, I carried out,in co-operation with Dr. Sitkowski and Mr.Maczenski, experiments on the influence of thelowering of temperature on the viscosity ofheparinized blood (Manteuffel-Szoege, Sitkowski,and Maczenski, 1959). The curve in Fig. 6 showsthe rise of blood viscosity in relation to thelowering of temperature. The increase ofviscosity is so considerable that it influences theaction of the circulation. If we assume that thework of the circulation increases in the samedegree as the viscosity, or strictly speaking as theblood rubbing work, it appears that the work ofthe circulation at 200 C. compared with that at370 C. increases by about 50% (Fig. 7). Thesecalculations would be binding if the flow speedand the amount of passing blood as well as thewidth of blood vessels were the same at differenttemperatures. Thus the thermal factor in thecirculation cannot be reduced to the creation ofcertain optimum conditions for this system. Thethermal factor is of direct dynamic significance,influencing the energy balance of the circulation.If we reverse the influence of the temperature onviscosity we can state that increased temperature,by diminishing viscosity, reduces resistance andconsequently also the work of the circulation. Ofthe internal organs it is the liver that shows thehighest temperature-higher than that of the heart-and the liver is the most dynamic centre of thevenous circulation (Horvath, Rubin, and Foltz,1950).Thus the energy factor of the circulation is

strictly connected with the thermal moment.Nevertheless, on the basis of the presentedevidence only, heat itself, though an indispensablefactor in the circulatory system, cannot beregarded as the source of the additional energyof the circulation.The assumption that there exists, besides the

work of the heart, the additional energy in the

so

ENERGY SOURCES OF BLOOD CIRCULATION

'aI:

A I -FED

ZZ272-.

7777/7];i5

FIG. 8.-Diagram of a water ram, as constructed by the author.With one asterisk the place is marked where the catheter was

introduced into the analogue of the great artery. Two asterisksmark the point of introduction of the catheter into the analogueof the ventricle.

circulation forces us to reconsider the presentopinions as to the nature of the mechanical actionof the heart.The heart action is compared to that of a pump.

Is it really true that the heart works like a

pump ? A pump sucks in fluid from a reservoir,which is a hydrostatic system and not a hydro-dynamic one. In the circulation, on the otherhand, not only is blood ejected from the heartbut it flows into the heart. The heart is a

mechanism inserted into the blood circuit, and soit is a very peculiar kind of pump.

Blood flowing into the ventricles under lowpressure leaves them under much higher pressure.The question could arise whether there exists inhydraulics an instrument that, when inserted intothe blood circulation, would change its pressurefrom a lower to a higher one. An instrument ofthis kind exists and it is called the water ram.The idea of the heart working on a principlesimilar to that of the water ram has alreadybeen put forward (Schmid, 1892; Steiner, 1920;Havlicek, 1937), and I have elaborated the analogybetween the heart action and that of the hydraulicram in co-operation with Dr. T. Gonta (Manteuffel-Szoege and Gonta, 1958).

I should like to present briefly the principle ofthe work of the water ram (Fig. 8) set out beforein a paper on the principle of the heart's action.Of basic importance in this device is the so-called" water hammer." By this is understood the

rapid change of kinetic energy, existing in runningwater, into the potential energy of pressure builtup in the water when the flow is abruptly stopped.The pressure can rise considerably and can bemany times higher than the pressure prevailing inthe liquid before it was stopped.The water (Fig. 8) from reservoir A flows down

through tube B and reaches its end part, wherethere is an opening equipped with valve C. Thisvalve, by virtue of its weight, exerts some resistanceto the outflowing water, but is finally lifted bythe current and obstructs the opening. The suddenhalt in the water current causes a violent rise ofpressure in the system, i.e., the previously describedphenomenon of the water hammer occurs. Therising pressure opens valve D, through whichwater flows into cylinder E, and from there to theoutflow tube F. When the water in this tuberises to the level of the reservoir A, water surface,valve D is shut by the weight of the water columnabove it. It becomes impossible for the water,trapped in tube F, to flow back into tube B.The pressure in tube B, lowered again by the

spurt through the chamber E and tube F, is notable to keep the valve C in the shut position anylonger. The valve C, by the force of gravity, fallsdown and the cycle described is started again.When this happens, the air contained in

chamber E is compressed, then it expands andforces some of the water from chamber E intooutflow tube F. As soon as the pressures of thewater and air become equal, the action describedabove starts again automatically. The presence ofair in chamber E is not indispensable for the waterram action. In order to put the water ram intooperation it is necessary to push valve C severaltimes from above downwards; the device thenstarts to work automatically as long as there iswater in the reservoir A. It is worth mentioningthat the outflow valve C can be situated betweenthe reservoir and chamber E as well as at the endof tube B.The analogy between the heart and the water

ram is as follows. The heart is, as maintainedalso by Havlicek (1937), a combination of twosynchronously working water rams correspondingto the right and the left heart. Tube F representsthe aorta or the pulmonary artery with valve D inlieu of the aortic or pulmonary artery valves. Thepart of the system under valve D can be consideredan analogue of the ventricle. It is difficult to sayjust how far in the direction of reservoir A theanalogy is valid. Outflow valve C partly playsthe role of the bicuspid or tricuspid valve. Thecorrespondence is only partial. It may be difficultto understand this analogy, the difficulties being

-04"

51

LEON MANTEUFFEL-SZOEGE

I.

FIG. 9.-The diagram of a water ram constructed in a wasresembling the construction of the heart. Such a watewithout a biological pacemaker, cannot work automatical

anatomical, but if the problem is approachedthe physiological point of view it becomes eto understand. Outflow valve C is of crimportance in the construction of the waterThis valve opens and closes rhythmically dthe ram's operation. The rapid, violent closithe valve determines the most essential funof the device, i.e., the sudden rise of pressurethe valve; this increase of pressure causes valto open and the water to surge into outflow tuabove the reservoir A water surface level.same thing happens in the heart. Blood flowsthe ventricle at the moment when the bicusptricuspid valve closes, the stream of blocabruptly stopped and the blood wave rebcfrom the closed valve and from the heart mwhich becomes stretched.Owing to the rebounding of blood frort

so-called elastic elements such as the valve anmuscle the pressure suddenly rises in the venand consequently also in the aorta and themonary arteries. Thus the principle of the N

ram action can be applied to the heart's v

The objection might be raised that in the Icirculation there is no place for bloodanalogous to the water loss in the wateroperation. But the water ram is only a mechainstrument.

In order to make the comparison betweetwater ram and the heart easier to imagiispecial model (Fig. 9) can be constructedwould not act automatically, but it wouldthe purpose of understanding the analogy betthe two systems. The outflow valve C has

closed. An instrument of this type cannot workautomatically without a suitable biological pace-maker. The muscle of the ventricles in the heartconstitutes such a pacemaker and the energy

F produced by the muscle corresponds to the energygenerated in the hydraulic ram by the loss ofwater through valve C.The analysis of the mechanical action of the

heart presented here explains this action on theprinciple of the water ram. A more detailed studyof this principle will bring more arguments infavour of my thesis. One argument is the observa-

E tion made by Schmid (1892) that the apex beatID precedes the ejection of blood from the ventricle

and not vice versa. With every stroke the pumpejects all the liquid it contains. The heart, on theother hand, does not empty itself entirely duringsystole: one-third of the blood contained in theheart during diastole remains there while two-

y more thirds are expelled into the arteries (Heilmeyer,er ram,ly. 1956). This observation favours the water ram

theory rather than that of the sucking and forcingfrom pump.easier The last argument I shall quote consists in therucial striking similarity between the tracing of the bloodram. pressure obtained from the ventricles of the heartLuring and from the great arteries and the tracing ofng of pressures taken from the respective parts of theLctlon water ram model (Manteuffel-Szoege and Gonta,near 1958). The tracing shown in the upper part of

[ve D Fig. 10 represents the changes of pressure in theibe F water ram near the rhythmically working outflowThe valve of the ventricle analogue. The place where

s into the catheter was placed while the tracing wasoid or)d is)undsiuscle

i therd the4itriclepul-

waterwork.bloodlossramnical

n thene, a1. Itservetweenbeen

B1.

FIG. 10.-Pressure tracing taken from the water ram. A, Tracingfrom -the analogue of the ventricle (the place marked with twoasterisks in Fig. 8). B, Tracing from the analogue of the greatartery (the place marked with one asterisk in Fig. 8).

52

ENERGY SOURCES OF BLOOD CIRCULATION

ECG.,

V.

'A.F.

FIG. 11.-V.D., Tracing of the pressures in the rightventricle of a man, taken during heart catheterization.A.F., Tracing of the pressure in the femoral artery,taken by direct puncture in the same man.

recorded is marked in Fig. 8 by two asterisks.This tracing is almost identical with the curve

illustrating the pressures in the right ventricleregistered during cardiac catheterization of an 18-year-old man (Fig. 11). The lower tracing (Fig. 10)comes from the tube corresponding to the pul-monary artery or aorta. The position of thecatheter is marked in Fig. 8 with one asterisk, andthe record resembles very much that of the majorartery (Fig. 11).The comparison of the tracing obtained from

the water ram with that from corresponding placesin the human circulatory system shows that the

hydrodynamic phenomena in both systems arealmost identical.The work of the heart, as I have interpreted it,

would not play a unique role, in the energy sense,in relation to the circulation; a very importantrole would be ascribed to the previously mentionedadditional energy factor of the circulation.

SUMMARY

I believe that the observations I have putforward tavour the conception that there exists,besides the work of the heart, another, additional,source of circulatory energy. The additional energyof the circulation manifests itself most distinctlyin the venous system and is strictly connected, asis the whole circulatory action, with the temper-ature in various organs.

It may be necessary to modify the presentinterpretation of the mechanical work of the heartas a pump and compare it to the hydraulicinstrument called the water ram.

REFERENCESEvans, C. L. (1952). Principles of Human Physiology, 11th ed.

Churchill, London.Glenn, W. W. L. (1958). New Engl. J. Med., 259, 117.Havlicek, H. (1937). Arch. Kreisl.-Forsch., 1, 188.Heilmeyer, L. (1956). Vortrage aus dem Gebiet der klinischen Chenmie

und Cardiologie. Thieme, Stuttgart.Horvath, S. M., Rubin, A., and Foltz, E. L. (1950). Anmer. J.

Physiol., 161, 316.Manteuffel-Szoege, L., and Gonta, T. (1958). Minerva cardioangio-

logica Europea, 6. No. 2, p. 261.Sitkowski, W., Jr., and Maczenski, S. (1959). Ibid., 7, No.3, p. 256.

-Turski, Cz., and Grundman, J. (1959). About the EnergySources of the Blood Circulation. In the press.

Schmid, K. (1892). Wien. med. Wschr., 42, 578, 622, 662..Steiner, R. (1920). Vortrags-Zyklus fur Aertzte und Medizin-

studierende. Der kommende Tag, Stuttgart.

53