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Diastolic murmur of equine aortic insufficiency
Diastolic
murmur
of equine
aortic
insufhiency
David L. Smetzer, D. I’. M., M.Sc.* Sanford Bishop, D. V.M., M.Sc.** C. Roger Smith, D.VM., Ph.D.*** Columbus, Ohio
T
he literature contains little information concerning either the diastolic murmur or the valvular lesions of aortic insufficiency in horses. That which is available consists primarily of phonocardiograms of the murmurs, with little definitive information in regard to valvular lesions.1-3 Availability of a large population of aged horses and mules at an abattoir has afforded the authors an opportunity for antemortem and postmortem studies of aortic insufficiency in these animals. The purpose of this report is to describe briefly the valvular lesions of aortic insufficiency in horses and mules and to describe the diastolic murmurs accompanying the lesions. A hypothesis of the origin of the presystolic accentuation, present in some murmurs, is presented. Methods
Seventeen horses and 7 mules were selected for study on the basis of presence of a murmur, Grade II (of VI) or greater, which extended through most or all of diastole. All were over 10 years of age. General health ranged from apparently normal to poor. Others having a soft low-
pitched murmur restricted to early diastole were not included in the study. Phonocardiograms (PCGs) were recorded from 19 unanesthetized animals. Murmurs in the other 5 were assessedby auscultation only. Sixteen PCGs were recorded with a Sanborn Twin-Beam? oscillograph at a paperspeed of 75 mm. per second. Logarithmic filtering was used. A Sanborn crystal microphone with a l&cm. bell was applied to the point of maximal intensity of the murmur. An electrocardiogram (EC(;), usually Lead aVr, served as the reference tracing. Phonocardiograms were recorded from 3 horses with an eight-channel Sanborn 550M photographic oscillograph. The filtering system was set at 100 c.p.s. cutoff. Phonocardiograms, ECG, pneumogram, and aortic pressure were recorded simultaneously at paper speeds of 50, 100, or 200 mm. per second. Aortic pressure was recorded from 2 horses through polyethylene tubing (0.046 inch I.D.) with a Sanborn model 267B transducer. The left carotid artery was punctured percutaneously with a 14-gauge needle for introduction of a catheter. Aortic or left ventricular
This research was supported in part by National Institutes of Health Grant No. HE-05627-05 and Central Ohio Association Grant No. 9-64. Received for publication Dec. 17. 1965. *National Institutes of Health Fellow, Department of Veterinary Physiology, Ohio State University, Columbus, Address: Ohio State University College of Veterinary Medicine, 1900 Coffey Rd., Columbus, Ohio, 43210. **National Institutes of Health Fellow, Department of Veterinary Pathology. Ohio State University, Columbus, ***Professor and Chairman, Department of Veterinary Physiology, Ohio State University, Columbus, Ohio. tSanborn Company, Wattham, Mass.
489
Heart
Ohio, Ohio.
pressures were recorded from one horse with a catheter-tip transducer,* frequent) response flat to 100 cycles, introduced via a surgically exposed carotid artery. I’honocardiograms were analyzed for the follo\ving: intensity, configuration as determined by variation in intensity, and vibration frequency of the murmurs. Hearts n.ere collected immediately after slaughter and transported in an ice chest to the laboratory, where the). \vere examined for the presence of valvular and regurgitant or “jet” lesions. Fifteen hearts were examined grossly and microscopically. Six hearts \\:ere examined for gross lesions only. l’ostmortem examination of 3 hearts 11-a~ not possible. The hearts of 15 horses an d mules which did not have a diastolic murmur were examined for valvular lesions and served as controls. Results
Gross pathology. A fibrous band located parallel to the free edge of at least one cusp of the aortic valve \vas the most consistent and significant valvular lesion found at postmortem examination (Fig. 1). A band extended across the entire cusp in some instances. In other instances it involved only a portion of a cusp. ITsually, the short bands extended from either commissure of the cusp; however, in a fe\z instances they were located at the center of the cusp. The free edge of those cusps with prominent band lesions appeared to be subject to eversion, with insufficient). of the cusp occurring as a consequence. Observations supporting this impression will be discussed later. Of 21 hearts examined postmortem, 18 had significant band lesions on one or more cusps of the aortic valve. Bands \l:ere located on the aortic cusps of the 18 hearts and distributed in this manner: left coronar)- cusp in 12 hearts, right coronary cusp in 3 hearts, noncoronary cusp in 2 hearts, and both the left coronary and the noncoronar)’ cusps in 1 heart. The free edge of each affected cusp was considered to be subject to eversion. Nodules, variable in size, were found on *Inductance ment OIli<,.
of
transducer Physiology,
designed Ohio
by Dr. Heinz Pieper. DepartState IIniversity, Columbus,
Fig. 1. Cross sectiorl of an aortic cusp illustrating a band lesion. The band is indicated b>, the arrows. The aortic surface il; indicated by A and the yentricular surface by I,‘. That portion of the cusp distal to the baud probabl>. evcrted after closure of the valve aud thereby served as the vibrating structure in the generatmn of ;I music-al diastolic nlurtnur. Orceiu-van Gieson staiu X 7.
the ventricular surface or at the free edge of some aortic cusps. No lesion considered as being compatible with the production of a diastolic murmur ~vas found on the tricuspid, mitral, or pulmonary valves. “Jet” or regurgitant lesions consisting of irregular masses of connective tissue \vere present on the interventricular septum (Fig. 2), on base of the aortic cusps, or on the ventricular surface of the anterior cusp of the mitral valve of 17 of the 21 hearts examined. Jet lesions were present on the interventricular septum ventral to the right coronary and noncoronary cusps in 12 of the hearts that had a major band lesion on the left coronary cusp of the aortic valve. Minor jet lesions were present on the basesof the right coronary and noncoronary cusps of some of the alcovementioned 12 hearts. No jet lesion uxs
Diastolic
Fig. 2. Regurgitant lesion located on the interventricular septum ventral to the aortic valve of a horse with insufficiency of the left coronary cusp of the aortic valve. The point of the arrow indicates prominent cusp-like ridges oriented toward the aortic valve. The “sea-gull” diastolic murmur recorded from this horse is illustrated in Fig. .5,.,1.
Fig. 3. .\ortic~ pressure (.lof’), electrocardiogram recorded simultaneously from a horse with ethylene tubing uxs used for the catheter in pressure pulses. Xortic pressure expressed in mur changes abruptly in presystole. The line intervals.
murmur
of equine aortic insufficiency
491
found in the thirteenth heart that had a band on the left coronary cusp. Jet lesions in the 3 hearts that had a band lesion on the right coronary cusp were located on the base of the left coronary cusp and on the ventricular surface of the anterior cusp of the mitral valve. In the 2 hearts that had band lesions on the noncoronary cusps, jet lesions were found below the right coronary cusp in one and below the left coronary cusp in the other. Microscopic observations on valvular and jet lesions are described in another report.* Diastolic murmurs. Diastolic murmurs were classified as either “musical” or “noisy.” Interpretation of musicality was based on the relative uniformity in the frequencies of the vibrations comprising the murmur (Fig. 3). Those murmurs considered to be noisy were composed of a mixture of vibrations of different frequencies (Fig. 4,A). Musict11 diustolic murmurs. Thirteen animals had diastolic murmurs which were completely or predominantly musical. A
@CC), phonocardiogram (I-‘(X), and pneumogram (Pneumo) insufficiency of the left coronary cusp of the aortic valve. Polyrecording aortic pressure. Arrows indicate “atria!” waves in aortic millimeters of mercury~. The amplitude and frequency. of the murtime lines in this and in subsequent illustrations are at O.O+second
aortic pressure (..IoP), I)hono~;lrdiogram, Fig. 4. Electrocardiogram. ;tnd pneumogram (f’ncuwo) recorded simultaneously from a horse with aortic insufficiency. ;l. Control. R, After intravenous administration of 2 my. of phenylephrine. Aortic pressures recorded through polyethy-lene tubing and expressed in millimeters of mercury. RedtIred sensitivity in B. Arrows indicate “atrial” wa\‘es. After the administration of phenylephrine (B) the aortic pressures increased and the murmur became musical in early diastole and in prcsy~stole. although retaining “noisiness” in mid-diastole.
postmortem examination was performed on the hearts of 10 of these. A prominent band lesion was found on at least one aortic cusp in all 10 hearts. Bv auscultation, four murmurs were high-pitched, with a “cooing” quality (Figs. 3 and 5,A). These probably were comparable to the so-called “sea-gull” diastolic murmur in n1an.j The remainder of the musical murmurs were low pitched, with a “rasping” or “buzzing” quality (Figs. 5,B and 6). The loudness of the musical murmurs ranged from Grade 2 to Grade 6, with the majority being either Grade 3 or Grade 4. The configuration, as determined by a change in the intensity of the murmur during its course, was variable from one animal to another. Minor variation was usually observed on a beat-to-beat basis. Peak intensity occurred at the termination of the second sound or shortly thereafter in some animals (Fig. 5,B), in mid-diastole in others (Fig. 5,C), and in presystole in
others (Fig. 5,-4). Three of the sea-gull murmurs increased in intensity uniformly throughout their course. The intensity of another sea-gull murmur increased abruptly after the P wave of the EGG (Fig. 3). A prominent band lesion \vas present on the left coronary- cusp of the aortic valve in those instances in which there was presystolic accentuation of the musical murnlurs. In general, the frequency of the vibrations of the musical murmurs was highest at the onset and decreased during the course of the murmur. The frequency of three sea-gull murmurs decreased uniformly during their course. The frequency of another sea-gull murmur decreased abruptly after the P wave (Fig. 3). The presystolic murmur in one mule was higher pitched than the early diastolic murmur. In some instances it was difficult to establish the precise frequency of a murmur because of faster vibrations being superimposed upon
volume Number
72 4
Diastolic
mmnur
qf equine aortic inszlficiency
493
Fig. 5. Musical diastolic murmurs (DM) of aortic insufficiency recorded from 3 horses. Variability of the nlusical murmur of aortic insufficiency in the horse is well exemplified. A, Configuration of the murmur is generally crescendo, with greatest amplitude occurring in presystole. B, Greatest amplitude of the murmur occurs early in diastole, followed by a secondary increase in amplitude. Murmur is “noisy” in presystole. C, Musical element restricted to mid-diastole, with abrupt termination after onset of P wave. Superimposition of vibrations of at least two different frequencies present in the musical element.
the slower vibrations of the fundamental frequency (Fig. 5,C). Noisy diastolic murmurs. In general, PCGs of the noisy murmurs were of little value for analysis; therefore, auscultation was relied upon for assessing most of these. Many of the noisy murmurs were loudest at their onset or shortly thereafter and were generally decrescendo throughout. Peak intensity in others appeared to occur near mid-diastole. Ten of the eleven noisy murmurs were Grade 2 in intensity and had a soft “blowing” quality. The intensity of a Grade 3 murmur increased to Grade 6 after the intravenous administration of 2 mg. of phenylephrine-HCl (Fig. 4). In addition, it became musical in early diastole and in presystole while retaining its noisiness in mid-diastole. A prominent band lesion was found on the left coronary cusp of this horse at postmortem examination. A band lesion was found on cusps of the aortic valve in 8 of the 11 horses and mules which had a noisy diastolic murmur.
Other considerations. The loud musical murmurs radiated over a wide area on the thoracic surface, thereby making their localization difficult. The softer musical murmurs were localized at the second sound area or the left third or fourth intercostal space 3 to 4 inches dorsad to the point of the olecranon. In spite of their softness, the noisy murmurs could be heard readily over an area extending 2 to 3 inches caudad and ventrad to the second sound area. With two exceptions, a distinct precordial “thrill” was present in all horses and mules which had a musical murmur. A thrill was present in only 2 of the animals which had a noisy murmur. The frequency response of the intracardiac transducer used in the catheterization procedure in one horse enabled the instrument to respond to vibrations of the musical murmur that was present (Fig. 6). Sonic vibrations sensedby the intracardiac transducer and displayed on the pressure tracing were comparable to those sensed by the microphone on the chest wall. The
Fig. 6. Phonocardiogram (PCG), electrocardiogram (ECG), left ventricular pressure (I, l-1’ ), ;tortic pressure (AoP), and right atria1 pressure (R.4P) recorded from :I horse with a diastolil. ntrtrmur (/).1/j (~1 ;rortic insufticiency. Pressures sensed by intracardiac transducers. .2ortic pressure (C) recorded at greater sensitix ity than left ventricular pressure (A and B). ?nly the aortic pressure is standardized, espressed in millinteters of mercury. In A, vibrations of the diastohc murmur are superimposed upon the left l.entricular pressure tracing, ‘Transducer located in left outflow tract. In B, as the transducer is positioned deeper in the ventricle, sonic vibrations disappear from the pressure tracing. In C, ribra tims of the diastcllic~ nl~,rmur i/lJf) are srlperirnposed upon the aortic pressure tracing when the transduc.er is positioned war the aortic. \YII\(,. I’rcs>,st(,lic accentuation of the murmur commences near the peak of the right atria1 “a“ wave ((L).
murmur was recorded best when the transducer was near the aortic valve. 1\Iovement of the transducer in either direction from the aortic valve resulted in progressive diminution of the vibrations of the murmur on the pressure tracing. Fluctuations related to atria1 systole were present in the aortic pressure tracings of 2 of the 3 horses catheterized (Figs. 3 and 4). Presystolic accentuation of the murmurs occurred during the course of these “atrial” waves. Discussion
The presence of a band lesion on a cusp of the aortic valve of the hearts of 1X of
21 horses and mules nhich had a diastolic murmur was indicative of the importance of that lesion in causing aortic insuffciency~ in those species. A comparable lesion wxs absent from the hearts of 15 horses and mules which had no diastolic murmur. Eversion of the free edge of those aortic cusps afflicted n-ith a band lesion was usually apparent Ivhen the aortic valve was viewed from the root of the aorta. Further evidence that bands resulted in insuficiency was gained by’ sliding a finger from the base to the free edge on the aortic surface of the affected cusp. The edge of the cusp distal to the band \vould evert rather than “catch” the finger as did ;I
Diastolic
normal cusp. Apparently, the band acted as a stricture in preventing the cusp from billowing out in a manner necessary for maintenance of competency of the valve. The fact that jet lesions were found opposite and ventral to a cusp with a band lesion in most cases was more conclusive evidence that band lesions resulted in insufficiency. Significant band lesions were absent from the aortic valves of 3 horses which had a noisy diastolic murmur. Small nodules on the aortic valves of those horses could have resulted in slight insufficiency. Insufficiency was considered to be probable in 3 horses whose hearts were not examined post mortem. This probability was based on the observation that the murmurs in these were comparable to the murmurs in animals proved to have aortic insufficiency. It is stated that the generation of a musical diastolic murmur is dependent upon the flow of blood past a structure capable of vibrating freely in a periodic manner.” Sagging and eversion of an aortic cusp, usually the right anterior one, is a common cause of musical diastolic murmurs in man.6,7 It has been reported that the presence of bands on an aortic cusp leads to eversion of the cusp and the consequent generation of a musical diastolic murmur in nlan.8 An everted aortic cusp was probably the source of the musical diastolic murmurs in our study, since postmortem examination in each case revealed the presence of a band lesion \\-hich appeared to permit eversion of the cusp. Why the murmur was noisy in other instances in which an everted cusp was the apparent cause of insufficiency is not immediately evident. Perhaps in some of these the murmur was musical at one time, but ljecause of a progressive change in the valvular lesion the murmur became noisy. The amount of regurgitation, the position of the everted cusp relative to the regurgitant stream, and the thickness and width of the everted edge are factors which probably enter into determining whether the murmur is musical or noisy, and its frequency if musical. Jet lesions have received consideration as a site for the production of murnlurs.g It is theorized that the roughened surface of the jet lesion is capable of generating audible vibrations as a consequence of the impact of a regurgitant stream of blood.
murm~~r qf equine aortic inszlficiency
495
It might be significant that the septal jet lesions of 3 horses which had a sea-gull type of murmur were composed of cusplike ridges oriented toward the aortic valve (Fig. 2). No jet lesion was found in another horse which had a comparable murmur, however. Presystolic accentuation was one of many interesting features of the musical murmurs. In man, a diastolic murmur of pure aortic insufficiency that is accentuated in presystole is referred to as an Austin Flint murmur.iO~” It is believed that the regurgitant stream of blood from the aortic valve strikes the anterior cusp of the mitral valve and displaces it into the stream of blood coming from the contracting atrium. By being subjected to two opposing streams of blood, the anterior cusp of the mitral valve is considered to vibrate and thereby generate the audible vibrations of the Flint murmur. An everted aortic cusp was considered to be the origin of both the early diastolic and the accentuated presystolic musical murmurs in the horse and mules studied, for the following reasons: (1) Presystolic accentuation of the murmur occurred in the absence of jet lesions on the anterior cusp of the mitral valve of some horses. In these, jet lesions on the ventricular septum indicated that insufficiency was not a recent development. From this the importance of the anterior cusp of the mitral valve as the site of origin of the accentuated presystolic murmur of horses becomes open to question. (2) Localization of a musical murmur (accentuated presystolic element included) at the aortic valve by an intracardiac transducer in one horse (Fig. 6) indicated that the everted left coronary cusp, found at necropsy, was the origin of both the diastolic and presystolic murmur in that particmar case. (3) A presystolic musical murmur was never present unless preceded by an earlier musical murmur, suggesting a common site of origin for the two. It seems to be likely that, if the presystolic musical murmur had as its origin some vibrating structure other than an everted aortic cusp, there would be instances in which the murmur is noisy in early and mid-diastole and musical in presystole. It is apparent that at the time of atria1 systole the character of the musical mur-
Fig. 7. “ .\trial” waves (a) in prrlmonary arterial pressure tracing (PAP) and i11 aortic pressure tracing (Aor) recorded from a horse with normal aortic valve. Second-degree atrioventricular block induced reflexly b!. illtravenous administration of 2 mg. of phenylephrine. Pulmonary arterial pressure (A) registered by intracardiac transducer at higher sensitivity than aortic pressure (H). Aortic pressure recorded by Sanborll model 257B transducer through polyethylene tubing. A definite incisura (UYYOWS), formed by atria1 waves. is tenlporallv related to onset of the fourth heart sound (S4). The prcilwisura atrial LV:LVC~ decrease in amplitude as the
mur changes in some horses (Figs. 3, 4,B, 5 ,C, and 6). It is also apparent that atria1 systole is responsible for specific fluctuations in arterial pressure pulses (Figs. 3, 4, and 7). Whether atria1 systole is related to these events is uncertain, and if related, how. Atria1 systole, by imposing an external force on the origin of the aorta or by transmitting a pressure pulse through the blood within the left ventricle to the aortic valve, is thought to cause “atrial” waves in the aortic pressure pulse.12 The latter belief gains support from the observation that occasionally a musical murmur stops at the onset of atria1 systole (Fig. S,C). It is thought that the increase in left ventricular pressure consequent to atria1 systole displaces an everted
aortic cusp toward closure and stops the murmur.5 Atria1 systole, by exerting an external force on the annulus of the aortic valve, could cause fluctuations in the arterial pressure pulse and distortion of an already insufficient aortic valve, and thereby account for the presystolic increase in intensity and presystolic decrease in frequency of musical murmurs in horses. Because of the attachment of the atria1 musculature to the fibrous annuli of the heart valves,13 atria1 contraction could provide the external distorting force. As an alternate hypothesis, distortion of the aortic valve could occur as a consequence of slight rotation of the heart hv atria1 systole. Regardless of precise o&in, the
Volume Number
72 4
Diustolic
initial atria1 fluctuations of arterial pressure pulses of horses with normal semilunar valves are usually most prominent when the arterial diastolic pressure is highest (Fig. 7). Summary
and conclusions
Seventeen horses and 7 mules in which the auscultatory findings suggested aortic insufficiency were selected for study from a population of aged horses and mules at an abattoir. Phonocardiograms were recorded from 19. The hearts of 21 were examined post mortem. Bands of fibrous tissue lying parallel to the free edge of one or more cusps of the aortic valve were the most frequent and significant valvular Iesions found. The more extensive bands appeared to cause insufficiency by permitting eversion of the free edge of the affected cusps. The left coronary cusp was insufficient in the majority. The right coronary cusp was considered to be insufficient in 3. Insufficiency of the left coronary cusp resulted in the development of regurgitant lesions on the interventricular septum, whereas insufficiency of the right coronary cusp resulted in the development of regurgitant lesions on the ventricular surface of the anterior cusp of the mitral valve. The diastolic murmurs in 13 horses and mules were “musical”; those in the remainder were “noisy.” Some musical murmurs were of the “sea-gull” type, i.e., high pitched with a “cooing” quality; others were low pitched and “rasping.” The configuration of musical murmurs varied from one animal to another. Some musical murmurs increased in intensity and decreased in pitch during presystole. The hearts of 10 animals which had a musical murmur were examined post mortem. Eversion of the free edge of an aortic cusp was found in all. Comparable lesions were found in the hearts of some horses and mules which had “noisy” diastolic murmurs. We believe that an everted free edge of an aortic cusp was the probable origin of most of the musical diastolic murmurs, including the presystolic element. Regurgitant lesions located on the inter-
murmur
of eqtrine uortic insuficitpcy
497
ventricular septum were not excluded as a possible site of origin of the “sea-gull” murmurs. It is not clear why some murmurs were “noisy” when eversion of the free edge of an aortic cusp was the apparent cause of insufkiency. It is possible that atria1 systole, either directly or indirectly, applied an external distorting force to the aortic annulus, and thereby caused an alteration in the character of some musical murmurs during presystole. We wish to thank the Ken-L Ration Division, Quaker Oats Company, Marion, Ohio, for the use of animals and facilities; and Mr. Stephen Boggs, Ohio State University, for his technical assistance. REFERENCES C. IX., Smetzer, D. L., Harnlin, R. I,., 1. Smith, heart sounds and and VVatsabaugh, C.: Normal heart murmurs in the horse, Proc. 8th Ann. Meeting Am. Assoc. Equine Pratt., December, 1962. 2. Detweiler, D. K., and Patterson, D. F.: Equine medicine and surgery, Wheaton, Ill., 1963, Am. Vet. Publications, Inc. 3. Dukes, H. H.: The physiology of domestic animals, ed. 7, Ithaca, N. Y., 1953, Comstock. 4. Bishon. S. P.. Cole. C. R.. and Smetzer. D. L.: Functional and morphologic pathology of equine aortic insufficiency, Path. Vet. 3:137, 1966. 5. McKusick, V. A.: Cardiovascular sound in health and disease. Baltimore, 1958, Williams & Wilkins Co. 6. Gelfand, D., and Bellet, S.: The musical murmur of aortic insufficiency: Clinical manifestations based on a study of 18 cases, Am. J. M. SC. 221:644, 1951. B., Nichols, C. F., and Mc7. Bellet, S., Gouley, Millan, T. M.: Loud, musical, diastolic murmurs of aortic insufficiency, AX HEART J. 18:483, 1939. R. W.: Disease of the aorta. Oxford 8. Scott, Medicine, Vol. 2, Part 2, 508(20), New York, 1942, Oxford University Press. 9. Edwards, J. E., and Burchell, H. B.: Endocardial and intimal lesions (jet impact) as possible sites of origin of murmurs, Circulation 18:946, 1958. 10. Gouley, B. A.: The aortic valvular lesion associated with the Austin Flint murmur, Al!. HEART J. 22:208, 1941. 11. Currens, J. H., Thompson, W. B., Rappaport, M. B., and Sprague, H. B.: Clinical and phonocardiographic observations on the Flint murmur, New England J. Med. 248583, 1951. 12. Howarth, S.: Atria1 waves on arterial pressure records in normal rhythm, heart block, and auricular flutter, Brit. Heart J. 16:171, 1954. 13. Rushmer, R. F.: Cardiovascular dynamics, Philadelphia, 1961, W. B. Saunders Company. L,
I
,
murmur
of equine
aortic
insufhiency
David L. Smetzer, D. I’. M., M.Sc.* Sanford Bishop, D. V.M., M.Sc.** C. Roger Smith, D.VM., Ph.D.*** Columbus, Ohio
T
he literature contains little information concerning either the diastolic murmur or the valvular lesions of aortic insufficiency in horses. That which is available consists primarily of phonocardiograms of the murmurs, with little definitive information in regard to valvular lesions.1-3 Availability of a large population of aged horses and mules at an abattoir has afforded the authors an opportunity for antemortem and postmortem studies of aortic insufficiency in these animals. The purpose of this report is to describe briefly the valvular lesions of aortic insufficiency in horses and mules and to describe the diastolic murmurs accompanying the lesions. A hypothesis of the origin of the presystolic accentuation, present in some murmurs, is presented. Methods
Seventeen horses and 7 mules were selected for study on the basis of presence of a murmur, Grade II (of VI) or greater, which extended through most or all of diastole. All were over 10 years of age. General health ranged from apparently normal to poor. Others having a soft low-
pitched murmur restricted to early diastole were not included in the study. Phonocardiograms (PCGs) were recorded from 19 unanesthetized animals. Murmurs in the other 5 were assessedby auscultation only. Sixteen PCGs were recorded with a Sanborn Twin-Beam? oscillograph at a paperspeed of 75 mm. per second. Logarithmic filtering was used. A Sanborn crystal microphone with a l&cm. bell was applied to the point of maximal intensity of the murmur. An electrocardiogram (EC(;), usually Lead aVr, served as the reference tracing. Phonocardiograms were recorded from 3 horses with an eight-channel Sanborn 550M photographic oscillograph. The filtering system was set at 100 c.p.s. cutoff. Phonocardiograms, ECG, pneumogram, and aortic pressure were recorded simultaneously at paper speeds of 50, 100, or 200 mm. per second. Aortic pressure was recorded from 2 horses through polyethylene tubing (0.046 inch I.D.) with a Sanborn model 267B transducer. The left carotid artery was punctured percutaneously with a 14-gauge needle for introduction of a catheter. Aortic or left ventricular
This research was supported in part by National Institutes of Health Grant No. HE-05627-05 and Central Ohio Association Grant No. 9-64. Received for publication Dec. 17. 1965. *National Institutes of Health Fellow, Department of Veterinary Physiology, Ohio State University, Columbus, Address: Ohio State University College of Veterinary Medicine, 1900 Coffey Rd., Columbus, Ohio, 43210. **National Institutes of Health Fellow, Department of Veterinary Pathology. Ohio State University, Columbus, ***Professor and Chairman, Department of Veterinary Physiology, Ohio State University, Columbus, Ohio. tSanborn Company, Wattham, Mass.
489
Heart
Ohio, Ohio.
pressures were recorded from one horse with a catheter-tip transducer,* frequent) response flat to 100 cycles, introduced via a surgically exposed carotid artery. I’honocardiograms were analyzed for the follo\ving: intensity, configuration as determined by variation in intensity, and vibration frequency of the murmurs. Hearts n.ere collected immediately after slaughter and transported in an ice chest to the laboratory, where the). \vere examined for the presence of valvular and regurgitant or “jet” lesions. Fifteen hearts were examined grossly and microscopically. Six hearts \\:ere examined for gross lesions only. l’ostmortem examination of 3 hearts 11-a~ not possible. The hearts of 15 horses an d mules which did not have a diastolic murmur were examined for valvular lesions and served as controls. Results
Gross pathology. A fibrous band located parallel to the free edge of at least one cusp of the aortic valve \vas the most consistent and significant valvular lesion found at postmortem examination (Fig. 1). A band extended across the entire cusp in some instances. In other instances it involved only a portion of a cusp. ITsually, the short bands extended from either commissure of the cusp; however, in a fe\z instances they were located at the center of the cusp. The free edge of those cusps with prominent band lesions appeared to be subject to eversion, with insufficient). of the cusp occurring as a consequence. Observations supporting this impression will be discussed later. Of 21 hearts examined postmortem, 18 had significant band lesions on one or more cusps of the aortic valve. Bands \l:ere located on the aortic cusps of the 18 hearts and distributed in this manner: left coronar)- cusp in 12 hearts, right coronary cusp in 3 hearts, noncoronary cusp in 2 hearts, and both the left coronary and the noncoronar)’ cusps in 1 heart. The free edge of each affected cusp was considered to be subject to eversion. Nodules, variable in size, were found on *Inductance ment OIli<,.
of
transducer Physiology,
designed Ohio
by Dr. Heinz Pieper. DepartState IIniversity, Columbus,
Fig. 1. Cross sectiorl of an aortic cusp illustrating a band lesion. The band is indicated b>, the arrows. The aortic surface il; indicated by A and the yentricular surface by I,‘. That portion of the cusp distal to the baud probabl>. evcrted after closure of the valve aud thereby served as the vibrating structure in the generatmn of ;I music-al diastolic nlurtnur. Orceiu-van Gieson staiu X 7.
the ventricular surface or at the free edge of some aortic cusps. No lesion considered as being compatible with the production of a diastolic murmur ~vas found on the tricuspid, mitral, or pulmonary valves. “Jet” or regurgitant lesions consisting of irregular masses of connective tissue \vere present on the interventricular septum (Fig. 2), on base of the aortic cusps, or on the ventricular surface of the anterior cusp of the mitral valve of 17 of the 21 hearts examined. Jet lesions were present on the interventricular septum ventral to the right coronary and noncoronary cusps in 12 of the hearts that had a major band lesion on the left coronary cusp of the aortic valve. Minor jet lesions were present on the basesof the right coronary and noncoronary cusps of some of the alcovementioned 12 hearts. No jet lesion uxs
Diastolic
Fig. 2. Regurgitant lesion located on the interventricular septum ventral to the aortic valve of a horse with insufficiency of the left coronary cusp of the aortic valve. The point of the arrow indicates prominent cusp-like ridges oriented toward the aortic valve. The “sea-gull” diastolic murmur recorded from this horse is illustrated in Fig. .5,.,1.
Fig. 3. .\ortic~ pressure (.lof’), electrocardiogram recorded simultaneously from a horse with ethylene tubing uxs used for the catheter in pressure pulses. Xortic pressure expressed in mur changes abruptly in presystole. The line intervals.
murmur
of equine aortic insufficiency
491
found in the thirteenth heart that had a band on the left coronary cusp. Jet lesions in the 3 hearts that had a band lesion on the right coronary cusp were located on the base of the left coronary cusp and on the ventricular surface of the anterior cusp of the mitral valve. In the 2 hearts that had band lesions on the noncoronary cusps, jet lesions were found below the right coronary cusp in one and below the left coronary cusp in the other. Microscopic observations on valvular and jet lesions are described in another report.* Diastolic murmurs. Diastolic murmurs were classified as either “musical” or “noisy.” Interpretation of musicality was based on the relative uniformity in the frequencies of the vibrations comprising the murmur (Fig. 3). Those murmurs considered to be noisy were composed of a mixture of vibrations of different frequencies (Fig. 4,A). Musict11 diustolic murmurs. Thirteen animals had diastolic murmurs which were completely or predominantly musical. A
@CC), phonocardiogram (I-‘(X), and pneumogram (Pneumo) insufficiency of the left coronary cusp of the aortic valve. Polyrecording aortic pressure. Arrows indicate “atria!” waves in aortic millimeters of mercury~. The amplitude and frequency. of the murtime lines in this and in subsequent illustrations are at O.O+second
aortic pressure (..IoP), I)hono~;lrdiogram, Fig. 4. Electrocardiogram. ;tnd pneumogram (f’ncuwo) recorded simultaneously from a horse with aortic insufficiency. ;l. Control. R, After intravenous administration of 2 my. of phenylephrine. Aortic pressures recorded through polyethy-lene tubing and expressed in millimeters of mercury. RedtIred sensitivity in B. Arrows indicate “atrial” wa\‘es. After the administration of phenylephrine (B) the aortic pressures increased and the murmur became musical in early diastole and in prcsy~stole. although retaining “noisiness” in mid-diastole.
postmortem examination was performed on the hearts of 10 of these. A prominent band lesion was found on at least one aortic cusp in all 10 hearts. Bv auscultation, four murmurs were high-pitched, with a “cooing” quality (Figs. 3 and 5,A). These probably were comparable to the so-called “sea-gull” diastolic murmur in n1an.j The remainder of the musical murmurs were low pitched, with a “rasping” or “buzzing” quality (Figs. 5,B and 6). The loudness of the musical murmurs ranged from Grade 2 to Grade 6, with the majority being either Grade 3 or Grade 4. The configuration, as determined by a change in the intensity of the murmur during its course, was variable from one animal to another. Minor variation was usually observed on a beat-to-beat basis. Peak intensity occurred at the termination of the second sound or shortly thereafter in some animals (Fig. 5,B), in mid-diastole in others (Fig. 5,C), and in presystole in
others (Fig. 5,-4). Three of the sea-gull murmurs increased in intensity uniformly throughout their course. The intensity of another sea-gull murmur increased abruptly after the P wave of the EGG (Fig. 3). A prominent band lesion \vas present on the left coronary- cusp of the aortic valve in those instances in which there was presystolic accentuation of the musical murnlurs. In general, the frequency of the vibrations of the musical murmurs was highest at the onset and decreased during the course of the murmur. The frequency of three sea-gull murmurs decreased uniformly during their course. The frequency of another sea-gull murmur decreased abruptly after the P wave (Fig. 3). The presystolic murmur in one mule was higher pitched than the early diastolic murmur. In some instances it was difficult to establish the precise frequency of a murmur because of faster vibrations being superimposed upon
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493
Fig. 5. Musical diastolic murmurs (DM) of aortic insufficiency recorded from 3 horses. Variability of the nlusical murmur of aortic insufficiency in the horse is well exemplified. A, Configuration of the murmur is generally crescendo, with greatest amplitude occurring in presystole. B, Greatest amplitude of the murmur occurs early in diastole, followed by a secondary increase in amplitude. Murmur is “noisy” in presystole. C, Musical element restricted to mid-diastole, with abrupt termination after onset of P wave. Superimposition of vibrations of at least two different frequencies present in the musical element.
the slower vibrations of the fundamental frequency (Fig. 5,C). Noisy diastolic murmurs. In general, PCGs of the noisy murmurs were of little value for analysis; therefore, auscultation was relied upon for assessing most of these. Many of the noisy murmurs were loudest at their onset or shortly thereafter and were generally decrescendo throughout. Peak intensity in others appeared to occur near mid-diastole. Ten of the eleven noisy murmurs were Grade 2 in intensity and had a soft “blowing” quality. The intensity of a Grade 3 murmur increased to Grade 6 after the intravenous administration of 2 mg. of phenylephrine-HCl (Fig. 4). In addition, it became musical in early diastole and in presystole while retaining its noisiness in mid-diastole. A prominent band lesion was found on the left coronary cusp of this horse at postmortem examination. A band lesion was found on cusps of the aortic valve in 8 of the 11 horses and mules which had a noisy diastolic murmur.
Other considerations. The loud musical murmurs radiated over a wide area on the thoracic surface, thereby making their localization difficult. The softer musical murmurs were localized at the second sound area or the left third or fourth intercostal space 3 to 4 inches dorsad to the point of the olecranon. In spite of their softness, the noisy murmurs could be heard readily over an area extending 2 to 3 inches caudad and ventrad to the second sound area. With two exceptions, a distinct precordial “thrill” was present in all horses and mules which had a musical murmur. A thrill was present in only 2 of the animals which had a noisy murmur. The frequency response of the intracardiac transducer used in the catheterization procedure in one horse enabled the instrument to respond to vibrations of the musical murmur that was present (Fig. 6). Sonic vibrations sensedby the intracardiac transducer and displayed on the pressure tracing were comparable to those sensed by the microphone on the chest wall. The
Fig. 6. Phonocardiogram (PCG), electrocardiogram (ECG), left ventricular pressure (I, l-1’ ), ;tortic pressure (AoP), and right atria1 pressure (R.4P) recorded from :I horse with a diastolil. ntrtrmur (/).1/j (~1 ;rortic insufticiency. Pressures sensed by intracardiac transducers. .2ortic pressure (C) recorded at greater sensitix ity than left ventricular pressure (A and B). ?nly the aortic pressure is standardized, espressed in millinteters of mercury. In A, vibrations of the diastohc murmur are superimposed upon the left l.entricular pressure tracing, ‘Transducer located in left outflow tract. In B, as the transducer is positioned deeper in the ventricle, sonic vibrations disappear from the pressure tracing. In C, ribra tims of the diastcllic~ nl~,rmur i/lJf) are srlperirnposed upon the aortic pressure tracing when the transduc.er is positioned war the aortic. \YII\(,. I’rcs>,st(,lic accentuation of the murmur commences near the peak of the right atria1 “a“ wave ((L).
murmur was recorded best when the transducer was near the aortic valve. 1\Iovement of the transducer in either direction from the aortic valve resulted in progressive diminution of the vibrations of the murmur on the pressure tracing. Fluctuations related to atria1 systole were present in the aortic pressure tracings of 2 of the 3 horses catheterized (Figs. 3 and 4). Presystolic accentuation of the murmurs occurred during the course of these “atrial” waves. Discussion
The presence of a band lesion on a cusp of the aortic valve of the hearts of 1X of
21 horses and mules nhich had a diastolic murmur was indicative of the importance of that lesion in causing aortic insuffciency~ in those species. A comparable lesion wxs absent from the hearts of 15 horses and mules which had no diastolic murmur. Eversion of the free edge of those aortic cusps afflicted n-ith a band lesion was usually apparent Ivhen the aortic valve was viewed from the root of the aorta. Further evidence that bands resulted in insuficiency was gained by’ sliding a finger from the base to the free edge on the aortic surface of the affected cusp. The edge of the cusp distal to the band \vould evert rather than “catch” the finger as did ;I
Diastolic
normal cusp. Apparently, the band acted as a stricture in preventing the cusp from billowing out in a manner necessary for maintenance of competency of the valve. The fact that jet lesions were found opposite and ventral to a cusp with a band lesion in most cases was more conclusive evidence that band lesions resulted in insufficiency. Significant band lesions were absent from the aortic valves of 3 horses which had a noisy diastolic murmur. Small nodules on the aortic valves of those horses could have resulted in slight insufficiency. Insufficiency was considered to be probable in 3 horses whose hearts were not examined post mortem. This probability was based on the observation that the murmurs in these were comparable to the murmurs in animals proved to have aortic insufficiency. It is stated that the generation of a musical diastolic murmur is dependent upon the flow of blood past a structure capable of vibrating freely in a periodic manner.” Sagging and eversion of an aortic cusp, usually the right anterior one, is a common cause of musical diastolic murmurs in man.6,7 It has been reported that the presence of bands on an aortic cusp leads to eversion of the cusp and the consequent generation of a musical diastolic murmur in nlan.8 An everted aortic cusp was probably the source of the musical diastolic murmurs in our study, since postmortem examination in each case revealed the presence of a band lesion \\-hich appeared to permit eversion of the cusp. Why the murmur was noisy in other instances in which an everted cusp was the apparent cause of insufficiency is not immediately evident. Perhaps in some of these the murmur was musical at one time, but ljecause of a progressive change in the valvular lesion the murmur became noisy. The amount of regurgitation, the position of the everted cusp relative to the regurgitant stream, and the thickness and width of the everted edge are factors which probably enter into determining whether the murmur is musical or noisy, and its frequency if musical. Jet lesions have received consideration as a site for the production of murnlurs.g It is theorized that the roughened surface of the jet lesion is capable of generating audible vibrations as a consequence of the impact of a regurgitant stream of blood.
murm~~r qf equine aortic inszlficiency
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It might be significant that the septal jet lesions of 3 horses which had a sea-gull type of murmur were composed of cusplike ridges oriented toward the aortic valve (Fig. 2). No jet lesion was found in another horse which had a comparable murmur, however. Presystolic accentuation was one of many interesting features of the musical murmurs. In man, a diastolic murmur of pure aortic insufficiency that is accentuated in presystole is referred to as an Austin Flint murmur.iO~” It is believed that the regurgitant stream of blood from the aortic valve strikes the anterior cusp of the mitral valve and displaces it into the stream of blood coming from the contracting atrium. By being subjected to two opposing streams of blood, the anterior cusp of the mitral valve is considered to vibrate and thereby generate the audible vibrations of the Flint murmur. An everted aortic cusp was considered to be the origin of both the early diastolic and the accentuated presystolic musical murmurs in the horse and mules studied, for the following reasons: (1) Presystolic accentuation of the murmur occurred in the absence of jet lesions on the anterior cusp of the mitral valve of some horses. In these, jet lesions on the ventricular septum indicated that insufficiency was not a recent development. From this the importance of the anterior cusp of the mitral valve as the site of origin of the accentuated presystolic murmur of horses becomes open to question. (2) Localization of a musical murmur (accentuated presystolic element included) at the aortic valve by an intracardiac transducer in one horse (Fig. 6) indicated that the everted left coronary cusp, found at necropsy, was the origin of both the diastolic and presystolic murmur in that particmar case. (3) A presystolic musical murmur was never present unless preceded by an earlier musical murmur, suggesting a common site of origin for the two. It seems to be likely that, if the presystolic musical murmur had as its origin some vibrating structure other than an everted aortic cusp, there would be instances in which the murmur is noisy in early and mid-diastole and musical in presystole. It is apparent that at the time of atria1 systole the character of the musical mur-
Fig. 7. “ .\trial” waves (a) in prrlmonary arterial pressure tracing (PAP) and i11 aortic pressure tracing (Aor) recorded from a horse with normal aortic valve. Second-degree atrioventricular block induced reflexly b!. illtravenous administration of 2 mg. of phenylephrine. Pulmonary arterial pressure (A) registered by intracardiac transducer at higher sensitivity than aortic pressure (H). Aortic pressure recorded by Sanborll model 257B transducer through polyethylene tubing. A definite incisura (UYYOWS), formed by atria1 waves. is tenlporallv related to onset of the fourth heart sound (S4). The prcilwisura atrial LV:LVC~ decrease in amplitude as the
mur changes in some horses (Figs. 3, 4,B, 5 ,C, and 6). It is also apparent that atria1 systole is responsible for specific fluctuations in arterial pressure pulses (Figs. 3, 4, and 7). Whether atria1 systole is related to these events is uncertain, and if related, how. Atria1 systole, by imposing an external force on the origin of the aorta or by transmitting a pressure pulse through the blood within the left ventricle to the aortic valve, is thought to cause “atrial” waves in the aortic pressure pulse.12 The latter belief gains support from the observation that occasionally a musical murmur stops at the onset of atria1 systole (Fig. S,C). It is thought that the increase in left ventricular pressure consequent to atria1 systole displaces an everted
aortic cusp toward closure and stops the murmur.5 Atria1 systole, by exerting an external force on the annulus of the aortic valve, could cause fluctuations in the arterial pressure pulse and distortion of an already insufficient aortic valve, and thereby account for the presystolic increase in intensity and presystolic decrease in frequency of musical murmurs in horses. Because of the attachment of the atria1 musculature to the fibrous annuli of the heart valves,13 atria1 contraction could provide the external distorting force. As an alternate hypothesis, distortion of the aortic valve could occur as a consequence of slight rotation of the heart hv atria1 systole. Regardless of precise o&in, the
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initial atria1 fluctuations of arterial pressure pulses of horses with normal semilunar valves are usually most prominent when the arterial diastolic pressure is highest (Fig. 7). Summary
and conclusions
Seventeen horses and 7 mules in which the auscultatory findings suggested aortic insufficiency were selected for study from a population of aged horses and mules at an abattoir. Phonocardiograms were recorded from 19. The hearts of 21 were examined post mortem. Bands of fibrous tissue lying parallel to the free edge of one or more cusps of the aortic valve were the most frequent and significant valvular Iesions found. The more extensive bands appeared to cause insufficiency by permitting eversion of the free edge of the affected cusps. The left coronary cusp was insufficient in the majority. The right coronary cusp was considered to be insufficient in 3. Insufficiency of the left coronary cusp resulted in the development of regurgitant lesions on the interventricular septum, whereas insufficiency of the right coronary cusp resulted in the development of regurgitant lesions on the ventricular surface of the anterior cusp of the mitral valve. The diastolic murmurs in 13 horses and mules were “musical”; those in the remainder were “noisy.” Some musical murmurs were of the “sea-gull” type, i.e., high pitched with a “cooing” quality; others were low pitched and “rasping.” The configuration of musical murmurs varied from one animal to another. Some musical murmurs increased in intensity and decreased in pitch during presystole. The hearts of 10 animals which had a musical murmur were examined post mortem. Eversion of the free edge of an aortic cusp was found in all. Comparable lesions were found in the hearts of some horses and mules which had “noisy” diastolic murmurs. We believe that an everted free edge of an aortic cusp was the probable origin of most of the musical diastolic murmurs, including the presystolic element. Regurgitant lesions located on the inter-
murmur
of eqtrine uortic insuficitpcy
497
ventricular septum were not excluded as a possible site of origin of the “sea-gull” murmurs. It is not clear why some murmurs were “noisy” when eversion of the free edge of an aortic cusp was the apparent cause of insufkiency. It is possible that atria1 systole, either directly or indirectly, applied an external distorting force to the aortic annulus, and thereby caused an alteration in the character of some musical murmurs during presystole. We wish to thank the Ken-L Ration Division, Quaker Oats Company, Marion, Ohio, for the use of animals and facilities; and Mr. Stephen Boggs, Ohio State University, for his technical assistance. REFERENCES C. IX., Smetzer, D. L., Harnlin, R. I,., 1. Smith, heart sounds and and VVatsabaugh, C.: Normal heart murmurs in the horse, Proc. 8th Ann. Meeting Am. Assoc. Equine Pratt., December, 1962. 2. Detweiler, D. K., and Patterson, D. F.: Equine medicine and surgery, Wheaton, Ill., 1963, Am. Vet. Publications, Inc. 3. Dukes, H. H.: The physiology of domestic animals, ed. 7, Ithaca, N. Y., 1953, Comstock. 4. Bishon. S. P.. Cole. C. R.. and Smetzer. D. L.: Functional and morphologic pathology of equine aortic insufficiency, Path. Vet. 3:137, 1966. 5. McKusick, V. A.: Cardiovascular sound in health and disease. Baltimore, 1958, Williams & Wilkins Co. 6. Gelfand, D., and Bellet, S.: The musical murmur of aortic insufficiency: Clinical manifestations based on a study of 18 cases, Am. J. M. SC. 221:644, 1951. B., Nichols, C. F., and Mc7. Bellet, S., Gouley, Millan, T. M.: Loud, musical, diastolic murmurs of aortic insufficiency, AX HEART J. 18:483, 1939. R. W.: Disease of the aorta. Oxford 8. Scott, Medicine, Vol. 2, Part 2, 508(20), New York, 1942, Oxford University Press. 9. Edwards, J. E., and Burchell, H. B.: Endocardial and intimal lesions (jet impact) as possible sites of origin of murmurs, Circulation 18:946, 1958. 10. Gouley, B. A.: The aortic valvular lesion associated with the Austin Flint murmur, Al!. HEART J. 22:208, 1941. 11. Currens, J. H., Thompson, W. B., Rappaport, M. B., and Sprague, H. B.: Clinical and phonocardiographic observations on the Flint murmur, New England J. Med. 248583, 1951. 12. Howarth, S.: Atria1 waves on arterial pressure records in normal rhythm, heart block, and auricular flutter, Brit. Heart J. 16:171, 1954. 13. Rushmer, R. F.: Cardiovascular dynamics, Philadelphia, 1961, W. B. Saunders Company. L,
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