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1 Cardiac Functin in Experimental Mitral Stensis By F..1. HADDY, M.D., A. L. FERRIN, M.D., D. W. HANNON, M.D., J. F. ALDEN, M.D., W. L. ADAMS, M.D., AND I. D. BARONOFSKY, M.D., PH.D. The results f S5 cmbined right and left heart catheterizatins in nrmal dgs and dgs with experimental mitral stensis are presented. Animals lived as lng as 1 mnths with elevated pulmnary vein pressures. Pulmnary vein pressures in excess f 15 mm. Hg were assciated with mitral rifice areas which were smaller than thse fund in nrmal animals. Elevatin f pulmnary vein pressure was assciated with a decrease in the pulmnary vascular pressure gradient, with n change in cardiac index as measured and with a decrease in calculated pulmnary vascular resistance. CONDITIONS characterized by the presence f pulmnary vein hypertensin have gained added prminence with the advent f cardiac catheterizatin and cardiac surgery. The impracticality f left heart catheterizatin in the human has limited ur knwledge f pulmnary vascular pressure gradients, pulmnary resistance and pulmnary edema in cnditins such as left heart failure and mitral stensis. Our studies 1 2 n acute elevatin f pressure in the pulmnary vein f the dg have shwn that pulmnary edema des nt ccur unless pulmnary vein pressure rises, and further that the pulmnary vascular pressure gradient decreases as the pressure is elevated in the pulmnary vein. The present cmmunicatin deals with the measurement f pulmnary vascular pressures and flw in relatin t chrnic elevatin f pulmnary vein pressure. The measurements were made pssible thrugh cmbined right and left heart catheterizatin 3 4 in dgs prepared with mitral stensis by the methd f Ferrin, Adams, and Barnfsky. 5 Their methd cnsists essentially f narrwing the mitral ring with silk sutures tied ver buttns. Frm the Department f Surgery and Physilgy University f Minnesta Medical Schl, Minneaplis, and Anckcr Hspital, St. Paul, Minn. This wrk was supprted by grants frm the Natinal Heart Institute f the Natinal Institutes f Health, Public Health Service, The Luis W. and Maude Hill Family Fundatin, and the Minnesta Heart Assciatin. Dr. Haddy is a Research Fellw f the American Heart Assciatin. Received fr publicatin Dec. 22, METHODS Mngrel dgs were anesthetized with intravenus pentbarbital sdium 33 mg. per kilgram apprximately tw weeks befre and tw weeks t 1 mnths after prductin f experimental mitral stensis. 5 With the animal supine, cardiac catheters were intrduced int the pulmnary artery and a. pulmnary vein. 3 Emplying an endtracheal tube, the animal was cnnected t a clsed system spirmeter cntaining 1 per cent xygen. Pressures in the pulmnary artery, pulmnary vein, intrathracic and femral artery were recrded simultaneusly with standard resistance wire pressure transducers (Statham strain gages). Zers were arrived at by visualizing the tips f the catheters flurscpically and expsing the strain gages t atmspheric pressure at that level. The catheter in the pulmnary vein was immediately withdrawn int the left ventricle and bld samples were btained frm the tw catheters fr determinatin f the cardiac utput by the direct Fick methd. Int the pulmnary artery, 7.5 mg. f T-1S24 dye was injected and bld samples were cllected frm the catheter in the left ventricle fr determinatin f the cardiac utput by the dye methd. The catheter in the pulmnary artery was withdrawn int the right atrium and the pressure recrded. The abve measurements and cllectins cnsumed an eight-minute perid during which xygen cnsumptin was measured. Integrated mean pulmnary vascular, right atrial, intrathracic and femral artery pressures were measured with a cmpensating plar planimeter, and all intrathracic vascular pressures were expressed as zer in relatin t the general intrathracic pressure. Oxygen cntent f the bld samples fr estimatin f the "cardiac utput" by the direct Fick methd was determined by the Van Slyke manmetrie methd. 6 "Cardiac utput" by the dye injectin technic was calculated accrding t the methd f Hamiltn and clleagues 7 except that cllectin f the bld samples frm the left Circulatin Research, Vlume I, May 1958
2 22 EXPERIMENTAL MITRAL STENOSIS ventricle bviated the necessity f extraplating the curves t zer. Using Rubner's cnstant in Meeh's frmula, 11.2 "v/(\vt. in Gm.) s, t calculate surface area, "cardiac utput" was expressed as "cardiac index." In the dgs that died, the mitral rifice was pened, laid flat and the circumference measured. Frm the circumference, the area was nrmal and mitral stensis animals. The average integrated mean pulmnary vein pressure in 44 nrmal animals was fund t be 8.3 ± 2.6 mm. Hg.jThe highest nrmal pulmnary vein pressure_\vas_14.8 mm. Hg. Twenty-nine catheterizatins in animals^with experimental TABUS 1. Difference in Frequency f Distributin f Pulmnary Vascular Pressures in Nrmal Animals and Animals with Mitral Stensis Fntcgrated Mean Pulmnary Vein Pressure mm. Hg Ttill Avc. ± a Number f Catheterizatins Nrmal Mitral Stensis Average Integrated Mean Pulmnary Artery Pressure mm. Hg frmal Range ( ) ( ) (17.S-25.4) ± 2.9 Average S S.9 Mitral Stensis Range ( ) (.9-24 ) ( ) ( ) ( ). MITRAL VALVE AREA O -PRE-OPERATIVE O-POST-OPERATIVE FIG. 1. Relatin between mitral valve area and pulmnary vein pressure in nrmal dgs and clgs with mitral stensis. Nte that whenever the pulmnary vein pressure exceeded 15 mm. Hg the mitral valve area was smaller than in nrmal animals. Pressures in excess f 2 mm. Hg were nt achieved because f the interventin f pulmnary edema. calculated. The area was then expressed per square meter f bdy surface area. RESULTS Table 1 presents the summarized data frm 85 separate eatheterizatins in 73 dgs befre and after the prductin f experimental mitral stensis, shwing the difference in frequency f distributin f pressures between mitral stensis revealed pulmnary vein pressures in excess f 15 mm. Hg. In f the 29 instances, the pulmnary vein pressure was in excess f 2 mm. Hg. One animal with a large element f mitral regurgitatin due t a trn leaflet had a pulmnary vein pressure f 33.5 mm. Hg. The animal expired several days fllwing catheterizatin with severe pulmnary edema. It is t be nted that a number f animals (nt presented) develped pulmnary edema fllwing peratin, and death ccurred befre catheterizatin was pssible. As wuld be predicted, an inverse relatinship was fund between mitral rifice area and pulmnary vein pressure. Figure 1 demnstrates that whenever the pulmnary vein pressure exceeded 15 mm. Hg the mitral rifice area was smaller than that fund in nrmal animals. Animals with mitral rifice areas belw 1 sq. cm. per square meter rarely survived fr an extended perid f time because f the ccurrence f pulmnary edema. A less cnstant but yet significant relatinship between pulmnary artery pressure and mitral rifice area was als demnstrated. Thus 13 animals with mitral rifice areas bel\\^3 sq. cm. per square meter had pulmnary artery pressure f 24.5 ± 6.G
3 F. J. HADDY ET AL. 221 mm. Hg, whereas 13 animals with rifice areas abve 3 sq. cm. per square meter had pulmnary artery pressure f 18.4 ± 2.8 mm. Hg. That this is a statistically significant difference is demnstrated by the Fisher t test fr cmparisn f means, t = 3.9, P <.1. Hwever, because f the decreased pulmnary arterypulmnary vein pressure gradient bserved in certain animals with small rifice areas and high pulmnary vein pressures, it was hazardus in the individual case t predict either pulmnary vein pressure r mitral rifice area frm the bserved pulmnary artery pressure. Upn elevatin f the pulmnary vein pressure, the pulmnary vascular pressure gradient, that is, pulmnary arterial pressure minus the pulmnary vein pressure (APp), decreased (fig. 2). Table 2 shws that this inverse relatinship is significant when subjected t Fisher's t test fr cmparisn f means. Thus elevatin f pulmnary vein pressure t 2 mm. Pig r abve caused apprximately a 5 per cent decrease in APp. Figure 3 shws the relatinship f "cardiac index," as determined by the direct Fick methd, t left ventricular filling pressure in nrmal and mitral stensis dgs. It will be nted that in the nrmal grup, an increase in left atrial pressure f apprximately 2 mm. Hg was assciated with an increase in "cardiac utput" f abut.8 liters per square meter per minute. Table 3 shws that the regular relatinship between left atrial pressure and cardiac index is statistically reliable. Since the perated grup cnsisted f animals with varying degrees f stensis, it wuld be predicted that this relatinship between flw and left atrial pressure wuld n lnger btain. By segregating the perated animals int tw equal grups, a lw and a high, accrding t the left atrial pressure, it was fund that the mean "cardiac index" fr the lw grup was 4.4 ± 1.1 liters per square meter per minute, whereas fr the high grup it was 4.8 =fc 1.3 liters per square meter per minute. Calculating the significance f the difference between the tw means by applicatin f Fisher's I test, it is fund that t =.97, p =.3-.4, indicating that the values are nt significantly different. The mean "cardiac index" by the Fick I- 14 i> 13 GRA ' l B > LEFT ATRIAL PRESSURE MM. HG -NORMAL -MITRAL.STENOSIS FIG. 2. Relatin between pulmnary vascular pressure gradient and pulmnary vein pressure in nrmal dgs and dgs with mitral stensis. Nte that the smallest gradients were assciated with pulmnary vein pressures in excess f 2 mm. Hg. TABLE 2. Relatin f Pulmnary Vascular Pressure Gradient t Pulmnary Vein Pressure in Nrmal Dgs and Dgs with Mitral Stensis Number f Integrated Mean Catheterizatins Pressure Pulmnary Vein mm.hg 39 3 belw and abve APp mm. Hg ± =fc ± S ± 2.6 Significance t = 3.13 P <.I t = 3.3 P <.1 -NORMAL O-EXPEHIMENTAL MITRAL STENOSIS Z A i2 fe IB IB ZO LEFT ATRIAL PRESSURE MM. HG FIG. 3. Relatin between "cardiac index" measured by the direct Fick methd and left atrial pressure in nrmal dgs and dgs with mitral stensis. Nte that the left ventricular filling pressure was psitively crrelated withflwin nrmal dgs. "Cardiac index" was maintained by virtue f an elevated lft atrial pressure in animals with mitral stensis.
4 222 EXPERIMENTAL MITRAL STENOSIS methd was 4.2 ± 1.5 liters per square meter per minute in the entire*grup'f nrmal animals and 4.6 db 1.2 liters per square meter per TABLE 3. Relatin f Left A trial Pressure t "Cardiac Index," Determined by the Fick Methd in Nrmal Dgs Number f Animals 17 IntegratedMean Left Atrial Pressure mm.hg Belw C and iibve Cardiac Index L./M.Vmin. ± a 2.8 ± ± l. 5.5 ± 1.2 Significance t = 4.67 P <.1 t = 2.SS P <.1 TABLE 4. Relatin f Pxdmnary Vascular Resistance t Pulmnary Vein Pressure in Nrmal Dgs and Dgs with Mitral Stensis Number f Catheterizatins In tegra ted Mean Pulmnary Vein Pressure mm.hg and abve Pulmnary Vascular Resistance mm.hg/l./min. /M.«± «2.43 ± ± ±.62 Significance t = 2.61 p <.1 t = 2.75 p <.1 -NORMAL -MITRAL STENOSIS PULMONARY VEIN PRESSURE MM. HG FIG. 4. Relatin between calculated pulmnary vascular resistance in mm. Hg/L./min./M. 2 and pulmnary vein pressure in six dgs studied befre and after the prductin f experimental mitral stensis. Nte the pstperative decrease in resistance in each case. minute in the animals with mitral stensis. Applying Fisher's t test, it was fund that the means were nt significantly different, t = 1.19 and p The "cardiac index" was measured by the dye injectin technic in 26 nrmal animals and in seven animals with mitral stensis (pulmnary vein pressure abve 15 mm. Hg). The flw values by this methd were 4.4 ± 1.5 and 4.3 ±.4 liters per square meter per minute respectively. Therefre, thugh the prcedure raised left atrial pressure t very high values, the cardiac utput as measured remained essentially unchanged in the perid studied. There is evidence, therefre, that the pressure rise cmpensated fr the impsed increase in resistance t flw thrugh the mitral rifice. Thus it has been shwn that APp became prgressively smaller whereas "cardiac utput" remained essentially unchanged as pulmnary vein pressure was prgressively elevated. Calculating pulmnary vascular resistance frm the frmula R p = APv.1. significant inverse relatinship between resistance and pulmnary vein pressure was fund as indicated in table 4. Figure 4 presents the relatinship f pulmnary vascular resistance t pulmnary vein pressure in six dgs studied bth befre and after peratin in whm pulmnary vein pressure was successfully raised abve 2 mm. Hg by mitral bstructin. A pstperative decrease in calculated resistance was fund in each case. The pulmnary artery pressure in these six animals averaged 2.2 mm. Hg in the nrmal state and 29. mm. Hg after prductin f mitral stensis. Several f the animals lived as lng as 1 mnths with high pulmnary vein pressures. Micrscpic sectins f the lungs failed t shw significant narrwing f the pulmnary muscular arteries by medial hypertrphy and fibrus intimal prliferatin* as bserved in humans with lng standing mitral stensis. 89 In keeping with this, subsequent catheterizatin in these dgs failed t reveal an increasing pulmnary pressure gradient r pulmnary vascular resistance in the perid studied. Thugh the femral artery pressure was fund t be 146 ± mm. Hg in 31 nrtna' dgs as cmpared with 137 ± 17 mm. Hg in * The authrs are indebted t Dr. J. E. Edwards fr his kindness in examining the micrscpic sectins f the lung.
5 F. J. HADDY ET AL. 223 clgs with mitral stensis (pulmnary vein pressure abve 15 mm. Hg), the difference was fund nt t be statistically reliable t = 1.79, p = The usual physical signs f right heart failure, such as ascites and peripheral edema, failed t appear in the animals with mitral stensis during the perid studied. It was anticipated therefre that the central venus pressure wuld nt be fund t be greatly elevated by the prcedure. This was fund t be the case. Thus the average integrated mean right atrial pressure was 5. ±1.3 mm. Hg in 43 dgs with pulmnary vein pressure belw 15 mm. Hg, as cmpared t 6.1 d= 2. mm. Hg in 13 dgs with pulmnary vein pressure abve 15 mm. Hg (t = 2.43, p =.1-.2). Neither were there increases in the thickness f the right ventricular wall r ttal heart weight during the perid studied. The lung/heart weight rati was used in an attempt t assess pulmnary edema in the animals that died frm causes ther than pneumnia. The lung/heart rati was fund t be 1.3 ±.3 in 13 animals with pulmnary vein pressures belw 15 mm. Hg, whereas the value was 2.4 zt.9 in 17 animals with pulmnary vein pressures abve 15 mm. Hg (t = 4., p <.1). This highly significant difference ccurred even thugh there ften was a lng perid f time between catheterizatin and death in animals with pulmnary vein pressures belw 2 mm. Hg. Only ccasinally did an animal with a pulmnary vein pressure abve 25 mm. Hg live mre than a few days. In reference t these unusual animals, it shuld be pinted ut that the pressures were measured in the Nembutal-anesthetized supine state and may therefre have been lwer in the unanesthetized prne state. DISCUSSION The data presented demnstrate that acute narrwing f the mitral valve t abut 1 sq. cm. per square meter was assciated with pulmnary vein pressures near the expected cllid smtic pressure f plasma. Further narrwing resulted in pulmnary edema. This relatinship between pulmnary vein pressure and the ccurrence f pulmnary edema is in agreement with results reprted earlier. 1 Als in agreement with an earlier reprt 1 is the finding that elevatin f pulmnary vein pressure acutely was assciated with a decrease in APp. This relatinship did nt change ver the 1-mnth perid studied. Thus in certain instances very narrw mitral valves and very high pulmnary vein pressures were assciated with a relatively small rise in pulmnary artery pressure. It was fund t be impssible t predict either pulmnary vein pressure r mitral valve area frm the pulmnary artery pressure. Jhnsn and Visscher 1 have recently pinted ut sme pssible surces f errr in measuring flw by the applicatin f the Fick principle. Their calculatins indicate that under certain cnditins large systematic errrs are pssible due t the fact that the Fick principle presuppses a cnstancy f bld flw r A-V difference during the time f sampling, neither f which pstulates is strictly valid. They pint ut that these errrs are prbably mst likely t ccur when breathing lw xygen mixtures 11 r in the presence f A-V shunts. It is prbable that the measurement f flw by the ctye methd is subject t similar surces f errr. Cgnizant f these pssible surces f errr, bld flw was estimated by the tw methds mentined fr lack f a better methd in the intact animal. Measurements were made with the animals breathing 1 per cent xygen in an attempt t keep variatins in A-V difference at a minimum during the time f sampling. It seems prper t cnclude frm the data reprted that in the nrmal dg the "cardiac utput" is psitively crrelated with left atrial pressure. The lw, left atrial pressures assciated with the lw utputs indicate that an inadequate filling pressure was prbably the cause f the lw utput. As the left ventricular filling pressure was elevated, "cardiac utput" increased as wuld be predicted frm Starling's Law f the Heart. Thus a rise in left atrial pressure f 2 mm. Hg was assciated with an increase in utput f abut.8 liters per square meter per minute. These findings again emphasize the imprtance t cardidynamics f small pressure changes in the lesser circulatin. It shuld be emphasized that the bservatins
6 224 EXPERIMENTAL MITRAL STENOSIS referred t were made while the animals were in gd clinical cnditin and befre they had been expsed t any experimental prcedures ther than thse invlved in placing catheters and cannulas. The absence f crrelatin between flw and left atrial pressure in animals with mitral stensis is prbably related t the varius degrees f stensis in this grup. The left atrial pressure was, as nted abve, inversely crrelated with the effective mitral valve aperture. Since "cardiac index" was nt altered, ne may prperly infer that the extra pressure was necessary t fill the ventricle. It seems likely that, were ne dealing with intraindividual variatins with changes in cnditins in the absence f heart failure, a psitive crrelatin between flw and left atrial pressure wuld be fund, but at a higher left atrial pressure level. The bservatin that pulmnary resistance is inversely related t the pulmnary vein pressure is in agreement with earlier bservatins 12 n acute elevatin f pulmnary vein pressure. The data reprted emphasize the imprtance f the rle f the abslute intraluminal pressure in ttal resistance in vascular beds. Since bld vessels are distensible elastic structures, the intraluminal pressure must be an imprtant determinant f vessel diameter. Since the vlume flw fr a given pressure gradient varies with the furth pwer f the radius f a tube, it is bvius that this factr can be f great imprtance. Thus it seems prper t suggest frm the data reprted that as pulmnary vein pressure is elevated the crss sectinal area f the pulmnary vascular bed is prbably increased and that, therefre, mvement f a given vlume f bld is accmplished with a smaller pressure drp. In mitral stensis in man ne rdinarily finds elevatins in pulmnary artery pressure when the disease is advanced and f lng duratin. Since changes f cmparable magnitude were nt bserved in dgs ver the perids f study emplyed it is suggested that the pulmnary artery pressure rise is nt a passive hydrdynamic phenmenn but rather results frm slw chrnic changes in the bld vessels altering their elastic and/r viscus prperties. It is felt that insufficient time has passed fr these changes t have taken place in the animals reprted. Further, the characteristic terminal right heart failure in mitral stensis in man and the failure t find it in dgs is pssibly related t an increase in right heart wrk subsequent t elevatin f pulmnary artery pressure in man and nt in the dgs reprted ver the perid studied. CONCLUSIONS The results f 85 catheterizatins in nrmal dgs and in dgs with experimental mitral stensis are presented. Whenever the pulmnary vein pressure exceeded 15 mm. Hg, the mitral rifice area was smaller than that fund in nrmal dgs. A less significant inverse crrelatin between pulmnary artery pressure and mitral rifice area was demnstrated. Left atrial pressure was psitively crrelated with cardiac utput in nrmal animals. Elevatin f pulmnary vein pressure by mitral stensis was assciated with a decrease in APp, with n change in cardiac index as measured and with a decrease in calculated pulmnary vascular resistance. Pulmnary edema was psitively crrelated with pulmnary vein pressure. Mrphlgic r physilgic evidence f an increasing pulmnary resistance failed t appear in the 1-mnth perid studied. Evidence f right heart failure als failed t appear. ACKNOWLEDGMENT The generus aid prvided by Dr. M. B. Visscher during the cnduct f this study is gratefully acknwledged. REFERENCES 1 HADDY, F. J., CAMPBELL, G. S., AND VISSCHER, M. B.: Pulmnary vascular pressures in relatin t edema prductin by airway resistance and plethra in dgs. Am. J. Physil. 1: CAMPBELL, G. S., HADDY, F. J., ADAMS, W. L., AND VISSCHER, M. B.: Circulatry changes and pulmnary lesins in dgs fllwing increased intracranial pressure, and the effect f atrpine upn such changes. Am. J. Physil. 158: 96, HADDY, F. J., CAMPBELL, G. S., ADAMS, W. L., AND VISSCHER, M. B.: A study f pulmnary venus and arterial pressures and ther variables in the anesthetized dg by flexible catheter techniques. Am. J. Physil. 158: S9, 1948.
7 F. J. HADDY ET AL HELLEMS, H. K., HAYNES, F. W., DEXTBK, L., AND KINNEY, T. D.: Pulmnary capillary pressure in animals estimated by venus and arterial catherizatin. Am. J. Physil. 155: 98, FERIUN, A. L., ADAMS, W. L., AND BARONOFSKY, I. D.: Evaluatin f experimental methds f prducing functinal mitral stensis. Surgical Frum Clin. Cngress Am. Cll. Surgens, P VAN SLYKIS, D. D., AND NEILL, J. M.: The determinatin f gases in bld and ther slutins by vacuum extractin and manmetric measurement. J. Bil. Cheni. 61: 523, HAMILTON, W. F., RILEY, R. L., ATTYAH, A. M., COUKNAND, A., FOWELL, D. M., HlMMELSTEIN, A., NOBLE, R. P., REMINGTON, J. W., RICHARDS, D. AV., WHEELER, N. C, AND WITHAM, A. C: Cmparisn f the Fick and dye injectin methds f measuring the cardiac utput in man. Am. J. Physil. 153: 39, ]94S. 8 PARKER, F., JR., AND WEISS, S.: The nature and significance f the structural changes in the lungs in mitral stensis. Am. J. Path. 12: 573, "LARRABEE, W. F., PARKER, R. L., AND EDWARDS, J. E.: Pathlgy f intrapulmnary arteries and arterils in mitral stensis. Prc. Staff Meet., May Clin. 24: 3, JOHNSON, J. A., AND VISSCHER, M. B.: The Fick principle. An analysis f a ptential errr in its cnventinal applicatin. In press. 11 NAHAS, G. G., HADDY, F. J., AND VISSCHER, M. B.: Discrepancies f cardiac utput measured by tw applicatins f the direct Fick principle. Federatin Prc. In press. 12 HADDY, F. J., AND CAMPBELL, G. S.: Pulmnary vascular resistance in anesthetized dgs. Am. J. Physil. In press.
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