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Veterinary Echocardiography JOHN D. BONAGURA, D.V.M.* and MATTHEW W. MILLER, D.V.M.** *The Ohio State University College of Veterinary Medicine, Columbus, Ohio and the **Department of Small Animal Medicine and Surgery, Texas A&M University College of Veterinary Medicine, College Station, Texas Echocardiography is used increasingly in the medical care of domesticated animals with spontaneous cardiovascular disease. Although the number of veterinarians engaged in clinical cardiology is comparatively small, veterinary application of echocardiography had a parallel development to the clinical experience of the medical cardiologist. Veterinary echocardiogra- phy has also benefited from laboratory investi- gations of experimentally induced cardiovascu- lar disease, most notably from studies con- ducted in dogs. There are hundreds of publications related to echocardiography in an- imal research and veterinary care. This article will illustrate the clinical value of echocardiography in veterinary medicine by de- scribing two-dimensional and M-mode imaging in animals, and initial experiences with Doppler echocardiography and color flow imaging. Our perspective is that of the veterinary clinician; thus, we will emphasize the value of Doppler echocardiography in the identification of com- parative spontaneous cardiovascular diseases in animals. There is a large amount of information available regarding Doppler echocardiography in the evaluation of induced heart disease in laboratory dogs. We will limit our discussion to data that are clinically relevant to veterinary practice, thereby disregarding the otherwise important information about induced myocar- Note: color illustrations do not appear in numerical order. Dr. Bonagura is currently the Visiting Research Fellow, Royal (William Dick) School of Veterinary Studies, Univer- sity of Edinburgh, Summerhall Square, Edinburgh, Scot- land. Address for correspondence: Matthew W. Miller, D.V.M., Diplomate A.C.V.I.M., Assistant Professor, Dept. of Small Animal Medicine and Surgery, Texas A&M University Col- lege of Veterinary Medicine, College Station, TX 77843- 4474. dial ischemia in dogs. Some practical sugges- tions for the recording of echocardiograms in animals are included for those who may not be experienced in performing Doppler echocardi- ography in the closed-chest animal. It is hoped that this information will be valuable and inter- esting and that this communication will in- crease the interaction between veterinarians, physicians, health care professionals, and labo- ratory investigators who have a mutual interest in cardiovascular disease. Technical Considerations Physicians and technicians who are experi- enced in echocardiography should have little difficulty learning to perform or interpret ani- mal studies. While there are slight qualitative and considerable quantitative differences be- tween those studies obtained from humans'-5 and those obtained from domesticated ani- mals,- established principles of imaging and interpretation are relevant. Despite similarities, the veterinarian or laboratory investigator must be familiar with normal anatomical and physio- logical differences between species. Cats and horses can be compared as an example. The normal left ventricular internal dimension in the cat is about 12 mm, the heart can be oriented almost horizontally in the thorax, and the heart rate often exceeds 200 beats/ min.11*18*33-36,39 The thoroughbred horse has a left ventricular internal dimension of up to 135 mm, a relatively upright cardiac axis, and a resting heart rate of < 40 beats/min.9.24-26*32*42 Knowledge of such interspecies variation is im- portant because it influences transducer selec- tion and placement, echocardiographic control settings, and obtained frame rate during cross- sectional and color flow imaging. To image the Vol. 6, No. 3, 1989 ECHOCARDIOGRAPHY. A Jml. of CV Ultrasound & Allied Tech. 229 BONAGURA AND MILLER common domesticated species, transducer fre- quencies between 2.25 and 7.5 MHz are range of probes generally used for pediatric to adult imaging.’-5 The depth of field needed to image a cat can be as shallow as 4 cm, while a horse or mature cow can require 35 cm. Since most available echocardiography machines have a maximal depth of field of < 25 cm, the opera- tor must interrogate the equine and bovine hearts from each hemithorax to obtain reason- able anatomical and blood flow informa- This physiological variation also influences the frame rate obtained during color flow imag- ing, impacting on the observer’s overall subjec- tive impression of motion and blood flow, and possibly the accuracy of color-coded Doppler. For example, we used three different manufac- turers’ instruments and found that the imaging frame rate during adequate color-coded Doppler can vary from 8 to 60 frames/sec. This is cause for concern as some instruments map the car- diac cycle of a cat with only three frames. If the heart rate is 240 beats/min, then there are 4 beats/sec. If the frame rate is 12 frames/sec, then there are 3 framesheat. One might ques- tion whether the temporal processing of flow data can accurately proceed at this rate? Color flow imaging in the horse often occurs at sample volume depths of up to 20 cm. Fortunately, the limitations placed on frame rate during flow- mapping at such depths is partially offset by the slow heart rate of the resting equine subject. A variety of mechanical sector scanning and phased array instruments have been used suc- cessfully for Doppler echocardiography in ani- mals. Initial instrument settings are similar to those utilized for human patients of equivalent size.’-5 Sector angle, gain settings, time gain compensation, reject, and other controls must be individualized for the animal, the type of study, and the region of interest. The depth of penetration must be varied for each species. Most normal horses are studied at a 20-24 cm depth of field, most cats require a field of only 4-6 cm, and most dogs are imaged at depths ranging from 6-14 cm. Selection of transducer frequency, focusing, and scanhead footprint or diameter relate to the needed,7,15,22,23,32.33,37,41,42,44.46 this represents the tion.9,14,24,32 species under study and whether the goal is ana- tomical detail or Doppler-derived velocity in- formation. The following are general guidelines for diagnostic imaging. Cats and small dogs (usually < 5.0 kg) can be imaged successfully with a 7.5-MHz or 5-MHz (short focused) trans- ducer. Most dogs are examined with either a 5-MHz (medium or variable focused) or 3.5- MHz transducer. Generally, horses and cattle require transducers with frequencies ranging from 2.25 to 3.5 MHz, the selection varying with the weight and chest conformation of the animal. Commercial instruments that were manufac- tured for Doppler echocardiography in humans have been used successfully for Doppler studies in both open- and closed-chest animal^.^^-^' When performing Doppler echocardiography, transducers with lower frequencies than those used for imaging usually provide the best sig- nal-to-noise ratio and superior color flow-map- ping?*4 Stand alone, continuous-wave Doppler transducers (typically 1.9 MHz) also perform well in animals because the small size of the transducer allows access to narrow intercostal acoustic windows and to the suprasternal notch. Some transducers that were designed for simul- taneous imaging with Doppler are so large that the study can only be done with difficulty. Ac- cordingly, pediatric transducers or probes with smaller footprints should be selected when pos- sible. When performing Doppler echocardiogra-phy in a cat or small dog, a 5-MHz (medium focus) transducer can be used because the re- gions of interest are often within 4-6 cm of the transducer. In most dogs (especially foxhound- type laboratory animals), a 3.5-MHz to 2.25- MHz transducer provides reasonable imaging with satisfactory Doppler signals. A 2.25-2.5- MHz transducer is used for Doppler echocardi- ography in horses or cattle. In these large ani- mals, the maximum depth of field available for pulsed-Doppler studies can be a limiting factor. It should be mentioned that we have experi- enced apparent differences between manufac- turers’ instruments in the quality and ease of obtaining Doppler signals in animals. Such dif- ferences in Doppler sensitivity may partially determine the ultimate carrier frequency of the chosen transducer. 230 ECHOCARDIOGRAPHY: A J r l . of CV Ultrasound & Allied Tech. Vol. 6, No. 3, 1989 VETERINARY ECHOCARDIOGRAPHY Vol. 6, No. 3, 1989 ECHOCARDIOGRAPHY: A Jrnl. of CV Ultrasound & Allied Tech. 231 The aforementioned guidelines can be fol- lowed for color flow imaging as well. General recommendations for using color-coded Doppler in patients are applicable to animal ~tudies.4,~ A variety of operator selected color maps, process- ing options, and image controls are available, depending on the instrument manufacturer. When applying color to the cross-sectional image, it is important to either reduce overall tissue imaging gain or to increase reject because color coding with some instruments cannot proceed if the pixel is occupied by tissue density or intraluminal noise. Low-velocity reject may be required to partially filter “flash” artifacts that seem to reflect from valves, chamber walls, and edges of lung (most commonly in tachycar- diac or tachypneic animals). Frame rate is opti- mized by narrowing sector and color imaging angles, suppressing imaging outside the color sector, decreasing depth of field, and altering the color processing. On some units, processing is adjusted and frame rate increased by reducing the level of color quality or increasing the limit of low-velocity reject. Other instruments pro- vide pre-processing controls of packet sizes.5 Reducing color quality or packet size to increase frame rate is a compromise, as we have obtained the best color image with medium or large packet sizes. Techniques for Recording Doppler Echocardiograms Animal Positioning The position of the animal is critical for ob- taining studies of diagnostic quality. Large ani- mals are examined while they stand, manually restrained, and often in s t o ~ k s . ~ . ~ ~ * ~ ~ , ~ ~ , ~ ~ , ~ ~ Frac- tious animals are lightly tranquilized (usually with xylazine). It is advantageous to advance the near forelimb to access the cardiac windows. It is our opinion that small animals are best imaged while they are gently restrained in lat- eral recumbency, sternum facing the operator, with the probe directed from below through a pre-cut hole in the imaging table.22,33,37 The ani- mal can be positioned to accommodate more cranial (superior) or caudal (inferior) acoustic windows and turned to allow imaging from each hemithorax. Alternatively, dogs can be studied while they stand or are restrained in a sling that has cutouts over the area of transducer place- ment. This method also works well for calves, and other similar-sized animals. While most small animals lay quietly, mild sedation with intramuscular or subcutaneous acepromazine (3 mg/square meter body surface area) can be administered. In cats, 2 mg/kg ke- tamine HCl given intravenously approximately 15 minutes after acepromazine provides about 15-20 minutes of mild chemical restraint. Where available, buprenorphine (0.0075-0.01 mg/kg, intravenously) can be used following acepromazine to provide excellent chemical re- straint for longer studies. When performing in- tercurrent Doppler and two-dimensional M- mode examinations during prolonged or inva- sive experiments, the anesthetized animal can be placed in left lateral recumbency, echoed from the left hemithorax for Doppler derived data, and from above with the transducer at the right sternal edge, for consistent two-dimen- sional and M-mode studies. In this case, a radio- graphic foam wedge, placed under the thoracic spine brings the heart closer to the thoracic wall and facilitates imaging from the right hemith- orax. The Imaging Table We use rectangular, custom-made, Plexiglas tables22 that can be mounted on a stainless steel surgical table (that can be varied in height) to image small animals. The table is made from %-% inch Plexiglas and is 48-49 inches long, 16-20 inches wide, and has six support legs that are 8 inches long (this should be based on trans- ducer size and connecting cable flexibility). The four corner legs are constructed with flanges that overhang the surgical table and provide stability against sliding. The other two legs are glued in positions that provide central support and are located 16-18 inches from the ends of the table. An imaging port, a circle or oval at least 5 inches in diameter, with a center equi- distant (24 inches) from each end is cut immedi- ately adjacent to or through a long edge of the table. Depending on the size of the imaging probes and animals studied, the imaging port location and shape can be varied. If the imaging BONAGURA AND MILLER port is placed too far from the table edge, near the virtual center of the table, the operator may become uncomfortable. A table that allows imaging from below the recumbent small animal subject is one of the important factors in ob- taining replicable and diagnostic Doppler echo- cardiography studies in small animal^.^^*^^ Imaging Planes While there are an infinite number of poten- tial imaging planes or views of the heart, there are certain tomographic planes used consis- centrate on those that are most beneficial for routine diagnostic imaging, Doppler echocardi- ography, and research. A number of angled and short-axis views, especially from the left he- tently (Table 1).7.15.22.23,32,33,37,41,44,46 We will con- mithorax, are used to identify congenital lesions and cardiac masses, but these will not be dis- cussed. Suprasternal notch imaging is some- what limited by the size of most small animals or the tremendous distance between the notch and the heart in the horse and cow. Subcostal positions are used less often in animals because right parasternal views have some resemblance to subcostal planes in human patient^.^.^^.^^ The imaging planes (Table I) are classified by: (1) the general location and relative position of the transducer, i.e., those obtained from the cranial or caudal right or left hemithorax; (2) the gen- eral orientation of the sector to the heart, i.e., long-axis, short-axis, apical, and angled; and (3) by the anatomical image obtained (optimized structures) (Figs. 1-3). TABLE I Image Planes Used for Echocardiography in Animals Right hemithorax 1. Long axis 4/5 chamber images a. Long axis 4 chamber view b. Optimized for the ventricular inlets and atrial septum (dorsocranial transducer location) c. Optimized for the left ventricular outlet and ascending aorta d. Modified 5 chamber view (ventrocaudal transducer location) 2. Short axis images at the level of the: a. Left ventricular apex b. Left ventricular papillary muscles c. Left ventricular chordae tendineae d. Mitral valve e. Aorta and left atrium (& pulmonary valve) 3. Angled image optimized for the right ventricular inlet and outlet, pulmonary valve, and long axis of the pulmonary artery (cranial transducer location) Left Hemithorax 1. Caudal (Apical) 4/5 chamber images a.Apical 4 chamber view optimized for the left ventricular inlet b. Apical 5 chamber view optimized for the left ventricular outflow tract and proximal aorta c. Apical 4 chamber view optimized for the right ventricular inlet (cranial transducer location) a. Optimized for the left ventricular inlet b. Optimized for the left ventricular outlet and aorta a. Optimized for the left ventricular inlet b. Optimized for the left ventricular outlet and aorta 2. Caudal (Apical) 2 chamber images 3. Cranial long axis views 4. Cranial angled view optimized for the long axis of the pulmonary artery 5. Cranial angled views optimized for the right atrium, vena cavae and right ventricular inlet 6. Cranial angled view of the left ventricular outlet (equine) 7. Cranial short axis view at the level of the cardiac base 1. Subcostal images 2. Images from the suprasternal notch Other image planes 232 ECHOCARDIOGRAPHY A Jrnl. of CV Ultrasound & Allied Tech. Vol. 6, No. 3, 1989 VETERINARY ECHOCARDIOGRAPHY Figure 1. Two-dimensional echocardiogram frozen during diastole. Right intercostal (parasternal), four- chambered, long-axis image f rom a healthy Stan- dardbred horse. RA = right atrium; RV = right ventri- cle; LA = left atrium; LV = left ventricle. Overall scan depth is 24 cm. We have tried to be specific in describing the method to obtain these tomographic planes. First, we indicate the point of transducer place- ment, then the rotation of the sector, and fi- nally, the craniocaudal and dorsoventral angu- Figure 2. Two-dimensional echocardiogram frozen during diastole. Right intercostal (parasternal), short- axis image at the level of the papillary muscles from a healthy dog. R V = right ventricle; I V S = interventri- cular septum; LV = left ventricle; PPM = posterior (caudodorsal or mural) papillary muscle; APM = ante- rior (cranioventral or septal) papillary muscle. Overall scan depth is 12 cm. Figure 3. Two-dimensional echocardiogram frozen during diastole. Left caudal intercostal (apical) four- chamber image from a female greyhound. RA = right atrium; RV = right ventricle; LA = left atrium; LV = left ventricle. There is a sample volume located at the left ventricular inlet. lation of the central (axial) echo beam. When the transducer is placed at the right hemithorax, it is assumed that the central (axial) echo beam is oriented in a right-to-left direction. Most transducer placements at the left hemithorax are oriented from left-to-right, however, some left parasternal views (as for the pulmonary ar- tery or a cranial long-axis image of the left ven- tricular inlet) are obtained by maintaining ori- entation of the sector and axial beam mostly to the left of the midline. The clockwise or coun- terclockwise rotation of the reference dot or notch that marks the edge of the sector is de- fined relative to the subject's torso. Sector ori- entation perpendicular to the long axis of the torso represents 0" (or 180") rotation. Rotation is defined from the perspective of looking down the transducer towards the thorax. Most opera- tors, when imaging small animals through pre- cut imaging ports, hold the transducer with their right hand; consequently, supination of the wrist yields clockwise rotation. Guidelines for angulation follow veterinary anatomical no- menclature, i.e., cranial caudal (superior infe- rior) and ventral dorsal (anterior posterior) an- gulation of the central (axial) echo beam. Rela- tive angulation is arbitrarily coded as none [O] to steep [+++I. Zero angulation places the Vol. 6, No. 3, 1989 ECHOCARDIOGRAPHY: A Jml. of CV Ultrasound & Allied Tech. 233 BONAGURA AND MILLER transducer perpendicular to the thoracic wall. Steep [+++I angulation indicates that the transducer footprint surface is barely being kept in contact with the skin. While Doppler echocardiography is often performed in the experimental laboratory using open-chest animal mode1s,47-57*59 the following comments pertain to more physiological closed- chest studies in the intact anima1.22*33,37*42*- 46*58*60-62 These descriptions are, at best, general guidelines for performing echocardiographic studies in the dog and for obtaining most of the image planes listed in Table I. Following a de- scription of the canine examination we offer brief suggestions for imaging cats and horses. Examination Method and Normal Echocardiographic Findings Right Intercostal Views We begin most canine and feline studies using a right parasternal (intercostal) position to ob- tain long-axis views of the heart.22,23*32933*- 37,41*42*44*46 The standard four-chamber, long-axis view used by most veterinary cardiologists rep- resents a tomogram that is almost an interme- diate image between a human subcostal view and parasternal long-axis In this plane, the cardiac septa are aligned nearly perpendicu- lar to the axial beam (Fig. 1). To obtain this image, the transducer is placed within 5 cm of the sternal edge at the right 4th-5th intercostal space, with the reference dot or notch held under the operator's thumb, perpendicular to the long axis of the animal's body (or slightly rotated 30" clockwise). The axial beam is then directed slightly caudally [ +] with minimal dor- sal [ +] beam angulation. Color flow imaging can be used to map flow through the ventricular inlets and left ventricular outlet, however, flow is generally perpendicular to the axial beam in this view. Owing to the large angle between the interrogating beam and normal blood flow, there is little if any signal aliasing of normal flow whereas high velocity flow and eccentric jets caused by valvular regurgitation or aortic stenosis are readily observed. The four-chamber view is optimized for the atrial septum (and atrial septal defects), the right pulmonary vein, and inlet valves by plac- ing the transducer in a slightly more dorsal po- sition (in the same intercostal space) with the beam angle either held constant or directed craniad [+I, (Figs. 4A and 4B, Color Plate 1). With the transducer either in this or the origi- nal location, the left ventricular outlet and proximal aorta are obtained by rotating the transducer 45-60' (clockwise) and then direct- ing the axial beam cranially [+ to ++] and pos- sibly dorsally [+I. Echo dropout of septal de- fects or abnormal flow associated with ventricu- lar septal defects or aortic valve disease may be detected from this plane (Fig. 5, Color Plate 2). Placing the transducer one or even two inter- costal spaces caudad (and slightly ventrad) to the four-chamber view initially described will produce 4/5-chamber long-axis images that are more similar to a human parasternal long-axis view and is better aligned with flow (Color Plate 3). From this ventrocaudal position, the trans- ducer is rotated 30-60" clockwise, and the axial beam directed more steeply dorsad [++ to +++I and cranially [ +] for the left atrium/ventricular inlet with more cranial angulation [++I for the tricuspid inlet and left ventricular outlet/aorta. When using this view for color flow imaging, signal aliasing may be observed in normals as velocities often exceed the Nyquist limit. It is not uncommon to observe physiological tricus- pid backflow. In some dogs, these views provide alignment to flow that is acceptable for quanti- fying velocities by spectral pulsed-Doppler echocardiography . Short axis tomograms are now ob- turned to the initially described four-chambered long-axis view, the sector is rotated 90' clock- wise and directed slightly caudodorsad [0 to +]. From this position, the transducer is swept ventrally to image the left ventricular apex and the sector is gradually directed dorsally towards the cardiacbase. At the papillary muscle level, the cranioventral (septal or anterior) papillary muscle is identified by its more distant location from the transducer (Fig. 2). Directing the transducer towards the base now yields a con- sistent series of short-axis tomograms at chor- dal, mitral, and aortic levels.22,33,37 As for the long-axis views, when approaching the level of tained.22,23,32,33,37,41,42,44,46 The transducer is re- 234 ECHOCARDIOGRAPHY: A J r l . of CV Ultrasound & Allied Tech. Vol. 6, No. 3,1989 VETERINARY ECHOCARDIOGRAPHY Figure 4A. Two-dimensional echocardiogram fro- zen during diastole. Right parasternal four-chamber image obtained from a dog with tricuspid valve dyspla- sia, tricuspid regurgitation, patent foramen ovale, and right-to-left atrial shunting. There is marked dilation of the right atrium (RA) and right ventricle (RV). The Ventricular septum is displaced into the left ventricle (LV). The septal and lateral tricuspid ka@ts are exces- sively long and insert into a single, abnormal papillary muscle. the aortic root, the operator should rotate the transducer an additional 45"-60" clockwise and angulate cranially [+ to ++I to complete the image. At this or at a slightly more dorsal level, the right ventricular outflow tract, pulmo- nary valve, and main pulmonary artery also can be visualized. During these short-axis examina- tions, the areas beneath the septal tricuspid leaflet and the right ventricular outlet septum are examined (ideally with color flow imaging) for ventricular septal defects. The left atrium and aortic root are perused by color-coded Doppler for regurgitation. The aortic/left atrial image is used to assess the extent of some mitral regurgitant jets and to pinpoint lesions to spe- cific aortic valve cusps as the noncoronary cusp can be identified adjacent to the atrial septum. Physiological aortic or mitral regurgitation is not typically found in unsedated healthy dogs, however, a brief period of valve closure backflow is sometimes observed. Similar to the situation in human patient^,^-^ the limits of normal for such "backflow" require further study. It should be noted that valvular regurgitation across all valves is commonly observed by color-flow Figure 4B. Two-dimensional echocardiogram fro- zen during systole f rom the same dog. The transducer has been placed in a more dorsocranial position than Figure 4A. The foramen ovale has been forced open by increasing right atrial pressure (arrowheads). Color flow imaging and saline contrast echocardiography (not shown) indicated right-to-kft shunting and tricuspid regurgitation. LA = left atrium; LV = left ventricle; RA = right atrium; RV = right ventricle. Doppler in healthy dogs undergoing anesthesia. These short-axis tomograms also are used to guide the cursor for M-mode studies and are ideal for laboratory studies of regional wall mo- tion and for assessing myocardial perfusion by contrast echocardiography (Figs. 6 and 7). Figure 5. Two-dimensional echocardiogram frozen during diastole from a 5-year-old Standardbred gelding with a ventricular septal defect. Right parasternal long-axis image optimized for the left ventricular outlet. The aortic root and one cusp of the aortic valve (AV) have prolapsed into the defect. R V = right ventricle; Ao = aorta. Vol. 6, No. 3, 1989 ECROCARDIOGRAPHY: A Jrnl. of CV Ultrasound 8. Allied Tech. 236 From a modified short-axis view adjacent to the level of the aortic valve, flow through the right ventricular inlet and outlet is inspected and the atrial septum is examined for interatrial shunting. This view is obtained by advancing the transducer 1-2 intercostal spaces cranially from the previously described short-axis aortic position, rotating clockwise 135"-160°, and di- recting the axial beam dorsally [++ to +++I and cranially [+ to ++I for the pulmonary ar- tery or caudally [ + to ++I for the right ventricu- lar inflow. Venous return from the caudal vena cava along the atrial septum predominates the right atrial flow pattern at this level and is coded red. As flow changes direction in the right ventricular cavity there is a loss of color, but diastolic and systolic flow towards the pulmo- nary valve are both coded blue (Color Plate 4). Signal aliasing in the right ventricular outlet is common during systole in normal animals. Pul- monary backflow is observed in some normal animals during diastole. When interrogated by pulsed-Doppler echocardiography, this signal is of low velocity. Steep dorsal angulation into the main pulmonary artery shows branching of the vessel and can be helpful in assessing retro- grade, turbulent flow from a PDA or a surgically created Blalock-Taussig or Waterson shunt. Right ventricular outlet and pulmonary artery velocities can be measured from this view; these are the only velocities routinely quantified from locations on the right hemithorax. While Doppler signals from flow across the tricuspid valve can also be quantified in this short-axis plane, we usually measure these velocities from left-sided apical views. Contrast echocardiography can be used to complement anatomical studies from the right hemithorax. Agitated or sonicated saline, blood, carbon dioxide, indocyanine green dye, Reno- grafin, Albunex, hydrogen peroxide, salts of diatrizoate, and other microcavitating fluids can be injected into the venous system, coronary ar- teries, aorta, or the heart to outline flow. Such studies are valuable in detecting cardiac shunt- ing and valvular regurgitati~n,~.~~.~'~~~,~~,~~~~~ di- lated coronary sinus (from persistent left cra- nial vena cava),64 and outlining coronary blood supply and myocardial perfusion de fe~ t s .~~-~O The latter application has received considerable attention in canine models of coronary disease. Since air is a potent echo target, echocardiogra- phy can be used to detect air emboli during an- e ~ t h e s i a . ~ ~ It is interesting that homes often have spon- taneous contrast in the heart.72-74 This is proba- bly a normal finding related to rouleaux of red blood cells. Marked echocontrast and swirling pattern of echocontrast, however, can be ob- served in pathological conditions, especially tri- cuspid endocarditis in the horse and left atrial dilation in cats with cardiomyopathy. The general principles of imaging described for dogs are applicable to cats as well.11*18933- 36*3940 In this species, the heart is oriented more horizontally in the thorax, thus, slight modifica- tions of the previous guidelines may be needed. Additional comments are needed about equine studies.9,24,32,43.65,72-75 Th e horse is exam- ined while it stands and (for safety) the operator stands facing the same general direction as the subject and holds the transducer with his or her left hand while placing the echocardiograph to his or her right side. If the reference marker is held under the thumb, many operators find it easier to supinate the wrist, thereby rotating counterclockwise for short-axis views from the right hemithorax (as opposed to clockwise in the recumbent dog). The examiner is advised to begin with a standard four-chambered view (Fig. 1) and to proceed from this point. In the horse, the usual location for transducer place- ment for this image plane is immediately cau- dodorsal to the olecranon in the standing ani- mal. Once this point is located, the right foreleg is advanced slightly to improve access to acous- tic windows. Because of the more upright posi- tion of the equine heart, slight counterclockwise rotation (0-30") may be needed, as well as slight caudodorsal angulation [+/+I. From this point, other views are easily obtained. The horse is technically challengingsince the depth of penetration needed to image the distal left atrial wall usually is not available. Conse- quently, mitral regurgitation can be difficult to detect from the right hemithorax with color- coded Doppler echocardiography. Conversely, tricuspid regurgitation is easily visualized in the BONAGURA AND MILLER 236 ECHOCARDIOGRAPHY: A Jml. of CV Ultrasound & Allied Tech. Vol. 6, No. 3, 1989 VETERINARY ECHOCARDIOGRAPHY Figure 6. M-mode echocardwgrams obtained from different anesthetized dogs. Various levels are demonstrated: Apical (A); ventricular (B); mitral (C,D,E); and aortic (F,G). The electrocardiogram (ECG), aortic pressure (AP), phonocardwgram (PCG), and first (Sd and second (Sd heart sounds are indicated. TA = transducer artifact; S = ventricular septum; LVW = left ventricular wall; A M V = anterior mitral valve; P M V = posterior mitral valve; AV = aortic valve; A o = aorta; LA = left atrium. The excursions of the anterior mitral leaflet are defined (panel E) and the opening (arrowhead) and closing points of the aortic valve (arrow) are indicated in panel F. The left atrial dimension is actually the left auricular luminal dimension and represents a source of potential error in animal M-mode studies. (From Bonagura 50'' with permission). Vol. 6, No. 3, 1989 ECHOCARDIOGRAPHY: A Jrnl. of CV Ultrasound & Allied Tech. 231 238 BONAGURA AND MILLER ECHOCARDIOGRAPHY: A Jml. of CV Ultrasound & Allied Tech. Vol. 6, No. 3, 1989 Figure 7 . Contrast M-mode echocardiogram ob- tained from a calf with a ventricular septa1 defect. An injection of saline and patient blood was made into the left ventricle. Following a period of ventricular tachy- cardia (ectopic QRS), the left and then the right ven- tricle is opacifkd. Later in the study (right panel) mi- crobubbles concentrate in the left ventricular outfEow tract and still shunt to the right ventricle. RV = right ventricle; Ao = aorta. (From Bongura JD, Pipers FS63 with permission). near field (Color Plate 3). While general princi- ples of beam rotation and angulation hold across the species, the actual dorsoventral placement of the transducer must be varied much more for equine studies. It is difficult to align the echo beam parallel to the flow for Doppler studies in the horse,6l be- cause true apical windows are unavailable and the heart is a considerable distance from the suprasternal notch. To obtain spectral Doppler velocities from the right hemithorax and screen for tricuspid regurgitation, a ventrocaudal transducer location is used (Table I). The trans- ducer is placed ventrally from the usual four- chamber long-axis view, the transducer angled steeply dorsad [++ to +++I and cranially [+ to ++I, then the reference marker is rotated grad- ually (from 0 to +60° clockwise) until the right ventricular inlet is aligned with the beam. For mapping of the right ventricular outlet, the transducer is placed about two intercostal spaces cranial (and 2-4 cm dorsal) from the original four-chambered position, rotated coun- terclockwise 30' to 60°, and directed craniad [+ to ++I and steeply dorsad [+++I to better align with right ventricular outflow. In this plane, the broad tricuspid to right ventricular inflow is coded red, and flow distal to the supraventricu- lar crest is blue. Spectral tracings of pulmonary artery velocity can be made but the valve is often 18-20 cm from the transducer and an ef- fort must be made to record parallel to flow. Pulmonary backflow is not uncommonly ob- served. Left Intercostal Views Imaging of small animals from the left he- mithorax permits the operator to more effec- tively align the transducer with blood flow for Doppler studies (Fig. 3, Color Plates 5,6,7).22.28,33,37p58,62 The apical (caudal intercos- tal) views resemble those applied in human pa- tients and are used to record velocities across the atrioventricular valves out of the left ven- tricle. The apical four- and five-chambered views in the dog are obtained with the trans- ducer placed at the left fifth or sixth intercostal space and the reference marker (sector edge) placed perpendicular to the long axis of the pa- tient at which time the transducer is directed slightly cranially [+I and dorsally [+ to ++I (Fig. 3). Diastolic ventricular inflow is red and generally biphasic (E and A waves), but is coded blue as blood curls up from the apex into the left ventricular outflow tract (Color Plate 5). Signal aliasing of color flow images may be seen in normal animals. To obtain an optimal angle on right ventricular inflow, the transducer is placed in the cranial aspect of the intercostal space with cranial angulation of the beam [++I main- tained, or the transducer is simply positioned one space craniad. Aortic flow may be best ob- tained by sliding the transducer ventrally 1-3 cm (or even one interspace caudal), rotating the sector slightly counterclockwise (-30') and di- recting the axial beam more steeply craniad [ ++ to +++I and slightly dorsad [+ to ++I. We have found the two-chambered view of the left heart to be complementary and often superior for recording mitral and aortic spectra. For this view, the transducer is maintained in the relatively caudoventral location just de- scribed, the sector rotated 90' to 120' clockwise, and dorsal angulation [+ to ++I is maintained. For the left ventricular inlet minimal or slight VETERINARY ECHOCARDIOGRAPHY Plate 6). In addition to providing image planes for recording ventricular inlet and outlet veloci- ties, the left apical views are useful for detection of mitral, aortic, and tricuspid regurgitation, as well as aortic stenosis and some cases of intra- cardiac shunting. A variety of additional long- and short-axis and angled views can be obtained cranially on the left hemithorax. The aorta is prominent in many of these views (Fig. 8):Some of these image planes have been described by Thomas22 and O'Grady and colleagues3' for routine two- dimensional echocardiography in dogs. One ad- ditional plane that merits consideration for Doppler echocardiography is the left cranial image optimized for the right ventricular outlet and pulmonary artery (Color Plates 7 and 8). For this view, the transducer is placed at the second or third intercostal space near the ster- nal edge. The sector is rotated clockwise 90" to 120" (roughly parallel to the long axis of the torso), and the pulmonary artery is imaged by directing the transducer steeply dorsad [+++I, usually adding minimal degrees of cranial angu- lation. From this perspective the operator can interrogate forward and regurgitant flow across the pulmonary valve, document aortic backflow into the pulmonary artery (Color Plate 8), and use continuous-wave Doppler to estimate pres- sure drop across a stenotic pulmonary valve. Similar left-sided views can be obtained in cats,33 however, for alignment with aortic flow the transducer may need to be placed as caudal as possible and directed steeply cranially as lung Figure 8. (A): Two-dimensional echocardiogram frozen during systole. Left cranial short-axis image op- timized for the aorta (Ao) and atria (LA, RA) obtained from a clinically healthy dog. The aortic valve is par- tially open. TV = area of the tricuspid valve. (B): Two- [+] cranial angulation is applied, while the ex- aminer uses steeper cranial angulation [++ to +++I to interrogate the outlet and aorta (Color dimensional echocardiogram frozen during systole from a dog with infective endocarditis of the aortic valve. Left parasternal image optimized for the left ventricu- lar outlet. The aortic valve is markedly thickened and abnormally echodense (arrows). There is some left ven- tricular dilatation. L V= left ventricle; LVW = left ventricular wall; I V S = interventricular septum. (C): Two-dimemionul echocardiogram frozen during dias- tole. Left cranial long-axis image of the left heart in a dog with aortic regurgitation. This black and white re- production of a color j2ow image demonstrates a regur- gitant jet (AR) striking the ventricular septum. LA = left atrium; LV = left ventricle; Ao = aorta. Vol. 6, No. 3, 1989 ECHOCARDIOGRAPHY A Jrnl. of CV Ultrasound & Allied Tech. 239 interference is a problem here. The operator must experiment with more dorsal/ventral po- sitioning in the caudal intercostal spaces. Fre- quently, a two-chambered view is obtained with the aorta at the edge of the sector. This allows good alignment with flow. One must be careful not to erroneously sample the pulmonary artery because it is adjacent to the aorta in this view and overall image quality from this position tends to be poor. Color flow is very helpful in guiding spectral recording in cats. There seems to be lower peak velocities more spectral broadening of the signals in cats when com- pared to dogs. Studies from the left hemithorax can be used to interrogate the left cardiac valves and ven- tricular septum of the h ~ r s e . ~ ~ * ~ ’ A long-axis view of the left ventricular inlet is obtained with the transducer located at the fourth to fifth in- tercostal space, 3-6 cm dorsal to the olecranon. The transducer is rotated so that the sector is perpendicular to the long axis of the body (the reference marker is dorsal, i.e., 12 o’clock). A four-chambered view (mainly of the left side of the heart) that places mitral inflow more paral- lel to the interrogating beam is obtained by sliding the transducer ventrally (below the level of the elbow) and angling the transducer cran- ially [+ to ++I and dorsally [+ to ++I with more cranial angulation (and 30” counterclockwise rotation from vertical) needed to see the left ventricular outflow tract. If the transducer is then repositioned cranially, usually two inter- costal spaces, rotated 30” counterclockwise, and directed dorsally [+++I , the left ventricular outlet and aortic valve can be evaluated. From these different positions at the left hemithorax, mitral inflow (red), regurgitation (blue), aortic outflow (blue), and regurgitation (red) have been imaged using color coding and verified with spectral recordings. Initial Evaluation of Doppler Echocardiographic Studies Doppler echocardiography studies obtained from domesticated animals are first examined for obvious abnormalities of structure, function, and flow. These can be qualitatively evaluated as one would assess data from human pa- tients.’” In the subsequent section, spontane- ous lesions of comparative interest are discussed and some of the methods used for identification of these conditions are illustrated. Animal studies can also be quantified, thereby permitting objective assessment of car- diac enlargement, abnormal blood flow, and al- tered ventricular function. Most studies that have evaluated the relationship between M- mode or two-dimensional echocardiographic measurements of chamber and wall dimensions compared to body size have demonstrated sig- nificant (generally linear) correlations between any quantitative anatomical study should ac- count for the subject’s body weight or surface area, or should measure serial changes using the animal as its own control. In contrast, quanti- tative functional data, like shortening fraction or other estimates of global left ventricular function, are similar between ~ p e c i e s . 6 ~ ’ ” ~ ~ ~ ~ ~ ~ ~ ~ ’ ’ ~ - 25*28,33,34*36*37,41,46 Left ventricular shortening frac- tion, typically between 30%-40% in unsedated animals tends to be slightly higher in cats when compared to dogs, horses, cows, sheep, and pigs. Echocardiography can be used to predict ventricular volumes and myocardial mass in dogs77-87 and horsesm and to measure ventricu- lar function. Since measured values from nor- mal animals are repeatable on a day-to-day basi~,6’~~*~’ echocardiography can be used to doc- ument progressive changes of cardiac anatomy and indices of ventricular function. This capac- ity has been employed in canine studies of hy- perten~ion~’-’~ and heart fail~re.’~-’~ Loading conditions, heart rate, anesthetic agents, seda- tives, and spontaneous or induced cardiac dis- eases significantly alter cardiac dimensions and echocardiographic indices of ventricular func- tion.18,34-36,43,45.96-111 For example, general anes- thesia, myocardial ischemia, dilated cardiomy- opathy, and taurine deficiency reduce left ven- tricular ejection phase indices in animals (Figs. 10A and 11). Sympathomimetic drugs increase ventricular shortening fraction and can even produce ventricular outflow gradients and sys- tolic anterior motion of the mitral valve in nor- mal dog^."^,'^^ It is valuable to inspect the shape and motion of the ventricular septum in animals with heart disease. Abnormalities have been observed in these variables (Fig. 9) .19,25.28,33,34.36.37,41,46,76 Thus 9 BONAGURA AND MILLER 240 ECHOCARDIOGRAPHY: A Jml. of CV Ultrasound 8i Allied Tech. Vol. 6, No. 3, 1989 VETERINARY ECHOCARDIOGRAPHY A 00- 5 5 50- 4 5 0 . 0 40- I . - v . (I) . 35- 30- 25- 20 o 2 4 B 0 10 12 14 ie ie 20 22 24 20 20 30 32 34 30 BODY HEIGHT (KG) Figure 9. The relationship between the diastolic dimension of the left ventricle (DDLV) and body weight in healthy dogs examined in our laboratory. The predicted valve and 95% confidence intervals are indicated. This relationship is similar to data reported by others for dogs and cats. (From Bonagura JD, O%rady MR, Herring Ds28 with permission). experimental models of ventricular loading and in dogs with spontaneous heart di~ease."""~ Ventricular septal motion is a reflection of overall left ventricular shape and responds to the relative pressure and volume loads of the ventricles. Changes in septal motion and in the radius of ventricular septal curvature are obvi- ous when examining short-axis tomograms from dogs with spontaneous pressure or volume overload of the right ~entric1e.l'~ The M-mode correlates to abnormal septal position, as in human patients, include flattened or paradoxi- cal ventricular septal motion (Figs. 4A,12A and 12B). Analysis of velocity spectra obtained from pulsed- and continuous-wave Doppler has been useful in the diagnosis and assessment of ex- perimental, congenital, and spontaneous ac- quired heart disease in animals.*51954957959*60~97,- 103-106~122-124 The challenge to the veterinary car- diologist is to consistently obtain data that approximates the accuracy demonstrated by a number of prominent laboratories using open- chest animal models. There is at this time a paucity of published, Doppler derived data from healthy, closed-chest, unanesthetized ani- mals.61*62 Normal values for peak velocities ob- tained by pulsed-Doppler for unsedated healthy dogs in our laboratory are: Aorta = less than 170 cm/sec, mean = 120 cm/sec; Mitral E = less than 100 cm/sec, mean = 76 cm/sec; Mitral A- = less than 75 cm/sec, mean = 49 cm/sec; Tri- cuspid E = less than 80 cm/sec, mean = 60 cm/ sec; Tricuspid A = less than 60 cm/sec, mean = 48 cm/sec; Pulmonary artery from the right or left hemithorax = less than 130 cm/sec, mean = 106 cm/sec (right) and 107 cm/sec (left). These data are very close to those reported by Vol. 6, No. 3, 1989 ECHOCARDIOGRAPHY. A J m l . of CV Ultrasound & Allied Tech. 241 BONAGURA AND MILLER Gaber6' using a different instrument. Tranqui- lization with acepromazine (3 mg/m2, BSA) had little effect on Doppler echocardiographyvalues in our studies of healthy dogs, generally reduc- ing velocities by e 10 cm/sec. Pulsed-Doppler velocity spectra are similar in appearance to those obtained from human patients (Figs. 11,13-16), however, summation of mitral and tricuspid inlet E and A points is common, par- ticularly in cats (Fig. 15). Physiological tricus- pid and pulmonic backflow are not uncommonly found in normal animals (Fig. 13). Doppler echocardiography is used increas- ingly to assess systolic and diastolic function in human patients.'~~,~ Many of the assumptions made regarding noninvasive assessment of car- diac output4' and ventricular function are based on animal-especially d o g - s t u d i e ~ ; ~ ~ ~ * ~ ' ~ ~ ~ ~ although a potential limitation of some studies may be the open-chest models often used. It is beyond the scope of this article to detail the experimental literature of ventricular function. Some generalizations can be made as they are relevant to the interpretation of veterinary Doppler echocardiography studies. Reduction in left ventricular systolic function, as develops with myocardial ischemia, dilated cardiomyopa- thy, and following cardiodepressant drugs, alters a variety of left ventricular ejection phase ractional shortening, ve- in~ces~19-21,29,96,103-112 F Figure 10. (A): M-mode echocardiogram from a hound with dilated cardiomyopathy. The left ventricle (LV) is greatly dilated to approximately 85 mm. Con- traction of the ventricular septum and left ventricular wall (W) is diminished. The mitral valve E point (ar- rowhead) to septa1 distance is increased. The mitral closure is delayed with a 'B' shoulder. The right panel of the aortic rootlleft atrium shows a dilated left atrium (LA). The aortic valve is most evident in diastole (open arrows). RV = right ventricle (From Bonugura JD, Herring DS30 with permission). (B) M-mode echocar- diogram from a cat with hypertrophic cardiomyopathy. The ventricular septum (S) and left ventricular wall (L) are hypertrophied for a cat. The left ventricular lumen is slightly reduced in size and the mitral valve (M) is crowded within the lumen. Systolic contraction is normal (double arrow). There is systolic anterior motion of the mitral valve (arrowhead), suggesting ob- structive myopathy and a small pericardial effusion (lower arrow). (From Bonagura JD, Herring DS3' with permission). 242 ECHOCARDIOGRAPHY: A Jml. of CV Ultrasound & Allied Tech. Vol. 6, No. 3, 1989 VETERINARY ECHOCARDIOGRAPHY Figure 1 1. Doppler echocardiograms from a normal anesthetized dog (left panel) and a dog with congenital subaortic stenosis (center and right panels). The left panel shows a normal outlet velocity waveform ob- tained by pulsed-Doppler. Because of anesthesia, the peak velocity is reduced (calibration markers = 0.2 mlsec). The tracing in the center panel was obtained from the left apex. Outlet velocity, measured by contin- uous-wave Doppler, is increased to at least 3 mlsec and aortic regurgitation (AR) is also noted. Aortic velocity obtained from the suprasternal notch (right panel) yielded a higher peak velocity approximating 4 mlsec. Estimated pressure gradient was 64 mmHg, which is a moderate obstruction for dogs with this lesion. locity of circumferential shortening, peak aortic velocity, and estimated ejection fraction and stroke volume all decrease (Figs. 10A and 11) and aortic acceleration time increases. It is ap- parent that diastolic function as assessed by Doppler echocardiography is complex involving interrelated Some of the changes observed in experimental studies of in- duced diastolic dysfunction have been observed in animals with spontaneous heart disease and presumed diastolic dysfunction (Fig. 16). Mitral and tricuspid E to A ratios, filling fractions, and acceleration and deceleration rates have been examined in canine models of ventricular dia- stolic dysfunction, but there is virtually no in- formation detailing these abnormalities in spontaneous heart diseases of animals. Assessment of Spontaneous Heart Disease in Animals Using Doppler Echocardiography Domesticated animals are afflicted with a va- riety of spontaneous congenital and acquired Figure 12A. M-mode echocardiogram from a Do- berman Pinscher with an ostium primum atrial septal defect (ASD), congestive heart failure, and pleural ef- fusion. There is significant right ventricular (RV) uol- ume overload, diastolic displacement of the ventricular septum into the left ventricle (LV), and paradoxical systolic septal motion. There is also some overall mo- tion artifact secondary to respiratory distress. The small arrows indicate parts of the tricuspid valve. (B): M-mode echocardiogram from a dog with congenital right ventricular outfiw obstruction. The right ven- tricular free wall and ventricular septum are hypertro- phied. Ventricular septal motion is abnormally flut be- cause of pressure overload of the right ventricle (RV). Systolic thickening is normal. Sd = diastolic septal thickness; S, = nadir of septal excursion; Pa = apogee (maximal excursion) of left ventricular wall; TV = tri- cuspid apparatus. (From DeMadron E, Bonagura JD, O'Grad~"~ with permission). heart diseases (Table 11). Many of these lesions have the potential to serve as models for analo- gous conditions of humans. One important dif- Vol. 6, No. 3, 1989 ECHOCARDIOGRAPHY: A Jml. of CV Ultrasound & Allied Tech. 243 BONAGURA AND MILLER Figure 13. Pulsed-Doppler echocardiogram from a clinically normal dog under general anesthesia. The sample volume was placed at the left ventricular inlet using a left apical four-chamber image. Phasic diastolic transmitral flow (the E and A waves) are recorded as well as a phonocardiogram (top trace), ECG, and aortic pressure curve. ference between adults and animals is the rela- tive scarcity of extramural coronary disease and transmural myocardial infarctions in the com- mon domesticated species. While microvascular changes have been recognized in dogs with dia- betes mellitus, congenital subaortic stenosis, and myxomatous valvular heart disease, and in cats with feline hypertrophic cardiomyopa- the clinical significance of these le- sions is unresolved. The reader is referred to general textbooks of veterinary medicine for more detailed descriptions of the clinical and pathological features of spontaneous heart dis- eases in animal^."^-^^^ We will briefly define important clinical conditions and attempt to il- lustrate the value of Doppler echocardiography in assessing these disorders. Pericardial Disease and Cardiac Mass Lesions Pericardial effusion, cardiac tamponade, per- itoneopericardial diaphragmatic hernia, and in- trapericardial mass lesions are frequently re- ported in veterinary medicine (Table 11) .125-131 Furthermore, there is a significant volume of published data regarding the dog as an experi- mental model of pericardial effision in human patients. Echocardiography has been used ex- perimentally132-139 and ~ l in i ca l ly~~”- ’~~ to iden- tify fluid and blood within the pericardial space, indicate the development of hemodynamic im- pairment and cardiac tamponade, and demon- strate intrapericardial and cardiac mass lesions (Figs. 17-22).1*154 Most cardiac masses in ani- mals cause clinical signs secondary to intraperi- cardial bleeding or pulmonary metastasis, al- though an occasional intracardiac tumor may obstruct venous return or cause systemic arte- rial embolization. Salient features of pericardial effusion in dogs are development of a sonolucent space between the epicardium and parietal pericardium, dis- placement of the right ventricular free wall from the thoracic cage, and abnormal cardiac motion. Asin humans, gravitational and anatomical features of the pericardial cardiac attachments influence the location of fluid accumulation. Echodense material may be identified within the effusate secondary to hemorrhage or fi- brinous exudation. Cardiac masses may be ob- served; these usually involve the right atrium or aortic Swinging of the heart is evident Figure 15. Pulsed-Doppler echocardiogram from a cat with idiopathic hypertrophic obstructive cardiomy- opathy. The sample volume was placed in the left atrium using a left apical image plane. Transmitral inflow velocity (MVIF) consists of one positive wave- form because of the rapid heart rate. High-velocity neg- ative systolic signals representing mitral regurgitation (MR) are indicated. The signal is aliased above the baseline (AL >). 244 ECHOCARDIOGRAPHY: A Jml. of CV Ultrasound & Allied Tech. Vol. 6, No. 3,1989 VETERINARY ECHOCARDIOGRAPHY Figure 16. Pulsed-Doppler echocardiogram from a 13-year-old Poodle with severe chronic respiratory dis- ease. The sample volume was placed in the right ven- tricular inlet using a right parasternal, ventral position four-chamber image. This dog had clinical and electro- cardiographic evidence of cor pulmonale and pulmo- nary hypertension including high-velocity tricuspid and pulmonary insufficiency. The echocardiogram shows abnormal reversal of tricuspid E and A waves, presumably from right ventricular hypertrophy and abnormal ventricular compliance. within large effusions. Diastolic collapse of the right ventricle or right atrium herald cardiac tamponade. The onset of this collapse also de- pends on diastolic characteristics of the right ventricle and overall blood volume s t a t ~ s . l ~ ~ , l ~ ~ Associated pleural effusions frequently are ob- served. Constrictive pericarditis has been recognized echocardiographically in a small number of ani- mals. While it is difficult to accurately assess pericardial t h i c k n e ~ s , l ~ ~ * ' ~ ~ there may be reduc- tion in ventricular cavity size, atrial dilation, abnormal septa1 motion, abrupt flattening of ventricular diastolic expansion, and reduced atrioventricular valve E-F slope. Vena caval distension and enlargement of hepatic veins are associated ultrasonic findings of right-sided failure in pericardial diseases. Valvular Heart Disease Valvular lesions, the most commonly en- countered cardiac disorders in veterinary prac- tice,lZ5-l3l include infective e n d ~ c a r d i t i s ~ ~ ~ ~ ~ . ~ ~ ~ ' ~ ~ congenital m a ~ f o r m a ~ ~ o n s , ~ ~ ~ ~ ~ ~ ~ ~ . 5 8 . ' 3 1 . ~ ~ 6 , 1 7 3 , 1 7 6 , 1 8 1 and acquired, typically degenerative disorders of (Table 11). Bacterial endocarditis is recognized in both small and large animals with the valve pre-dilection dif- fering considerably between species (Figs. 8 and 23). Clinical features are similar to those in human patients. Of the congenital valvar le- sions, pulmonic stenosis, usually the result of valve dysplasia, and fibrous subaortic stenosis are most common (Figs. 11,12B,24, Color Plate 4). Both conditions represent genetically trans- mitted malformations in some canine breeds. Dysplasia of the atrioventricular valves is diag- nosed in both small and large animals and refers to a spectrum of lesions which includes thick or shortened valve cusps, either very long or stout chordae tendineae, and anomalies of the papil- lary muscles (Fig. 4). Less frequently, there is atresia of the atrioventricular valve. The af- fected atrioventricular valve is incompetent, al- though stenosis also has been observed. Spo- radic cases of atrioventricular valve stenosis are recognized in dogs (Fig. 251, but there is no con- sistent counterpart to rheumatic valvular dis- ease in the domesticated species. The most im- portant cause of heart failure encountered in veterinary practice is myxomatous degeneration of the atrioventricular valves, a condition char- acterized grossly by shortening and thickening of the valve leaflets (Fig. 26, Color Plate 1). This lesion causes progressive mitral and tricuspid regurgitation almost exclusively in mature dogs, and resembles advanced cases of mitral valve prolapse syndrome in human patients. Rupture of a chorda tendinea can occur in conjunction with this, as well as other disorders, including endocarditis. Aortic regurgitation in animals is associated with congenital subaortic stenosis, bacterial endocarditis (Figs. 8B and 23) and, in the mature horse, incompetency secondary to degenerative lesions of the valves. Pulmonic in- sufficiency is most frequently observed with congenital heart disease (Fig. 4), after cardiac surgery or balloon valvuloplasty, and with cor pulmonale. These congenital and acquired valvular dis- orders have been identified using Doppler echo- cardiography. 16,29,40,44,93,155-184 It may be possible various types29,40,44,93,165-184 Vol. 6, No. 3, 1989 ECHOCARDIOGRAPHY: A Jrnl. of CV Ultrasound & Allied Tech. 245 BONAGURA AND MILLER TABLE I1 Cardiovascular Lesions Evaluated by Doppler-Echocardiography Valvular Heart Disease Congenital 1. Pulmonic stenosis 2. Aortic stenosis, Subaortic stenosis 3. Mitral valve dysplasia (incompetency/stenosis) 4. Tricuspid valve dysplasia (incompetency/stenosis) 5. Valve atresia (usually right-sided heart valves) 1. Myxomatous degeneration of the atrioventricular valves (dog) causing valvular regurgitation 2. Degenerative thickening of the aortic, mitral, and tricuspid valves causing valvar regurgitation (horse) 3. Bacterial endocarditis 4. Rupture of mitral valve chordae tendineae (dog, horse) Acquired Myocardial pisease 1. Dilated cardiomyopathy (dog, cat, horse, cattle) -Idiopathic dilated cardiomyopathy -Taurine deficiency (cat) -Doxorubicin cardiotoxicity (dog) 2. Myocarditis/myocardial necrosis -Vitamin E or selenium deficiency (horse, cattle) -Post-viral myocarditis (dog) 3. Hypertrophic cardiomyopathy (cat, dog) 4. Restrictive cardiomyopathy (cat) 5. Hyperthyroid heart disease (cat) 6. Hypertensive heart disease (dog, cat) Pericardial Disease/Cardiac Mass Lesions 1. Congenital pericardial diseases (hernia, cyst) 2. Idiopathic pericardial effision/hemorrhage (dog, cat, horse) 3. Hemorrhagic pericardial effision secondary to neoplasia -Right atrial hemangiosarcoma (dog) -Heart base tumor/chemodectoma (dog) -Lymphosarcoma (cat, cattle) -Metastatic carcinoma -1ntrapericardial metallic foreign-body (cattle) -Secondary to bacterial or fungal infection 5. Constrictive and constrictive-effusive pericarditis 6. Left atrial thrombus associated with feline cardiomyopathy 1. Secondary to congenital heart disease (dog, cat) 2. Dirofilariasis-heartworm disease (dog, cat) 3. Cor pulmonale secondary to chronic respiratory disease 4. Idiopathic (?primary) pulmonary hypertension Congenital cardiac shunt 1. Atrial septal defects 2. Ventricular septal defects 3. Patent ductus arteriosus (dog, cat) 4. Tetralogy of Fallot/pseudotruncus arteriosus 5. Complex congenital heart disease 4. Suppurative or granulomatous pericarditis Pulmonary Hypertension/Cor Pulmonale Cardiac arrhvthmia This a partial list of lesions encountered in the species most commonly imaged in veterinary practice (canine, feline, equine, bovine); Parenthesis ( ) indicates that the lesion is particularly prominent in or generally limited to that species. 246 ECHOCARDIOGRAPHY: A J m l . of CV Ultrasound & Allied Tech. Vol. 6, No. 3, 1989 VETERINARY ECHOCARDIOGRAPHY Figure 17. Two-dimensional echocardiogram fro- zen during diastole. Right parasternal four-chamber image f rom a dog with pericardial effusion and cardiac tamponade. The heart is surrounded by a n echo-free fluidspace. The left parietal pericardium is most dis- tant from the transducer. I n the near field, the right atrium has collapsed. I n real time, this was a phasic diastolic collapse. Figure 19. Two-dimensional echocardiogram from a cat with restrictive cardwmyopathy, atrial fibrilla- tion, and congestive heart failure. Long-axis image f rom the right hemithorax. The left atrium and right pulmonary vein are tremendously dilated and there is a large, circular left atrial mass lesion, which is a thrombus, attached to the atrial wall. A small pericar- dial effusion is evident behind the left ventricle. to detect abnormal valve anatomy (Figs. features, however, cannot be specific. Cases of 4,8,26,27), especially valve thickening, using severe myxomatous degeneration that echocar- two-dimensional and M-mode studies. The echo diographically resemble an infective vegetation Figure 18. Two-dimensional echocardiogram ob- tained from a cat with a congenital peritoneopericardial diaphragmatic hernia. T h e frozen image shows a short-axis view of the left ventricle (LV) obtained f rom the right hemithorax. Within the pericardial space, there is tissue density compatible with liver. The gall- bladder was found on other views. LVW = left ventric- ular wall; PERI = parietal pericardium. Figure 20. Two-dimensional echocardiogram fro- zen during diastole. Left apical four-chamber image f rom a 9-year-old German Shepherd with cardiac neo- plasia, tricuspid insufficiency, ascites, and left bundle branch block. The right atrium (RA) is markedly di- lated. At the inlet of the right ventricle (RV) there are multiple irregular tissue densities. These were attached to the ventricular septum and circumferentially about the tricuspid anulus (arrowheads) and appeared to ob- struct ventricular inflow. LV = left ventricle. Vol. 6, No. 3, 1989 ECHOCARDIOGRAPHY: A Jrnl. of CV Ultrasound & Allied Tech. 247 BONAGURA AND MILLER Figure 2 1. Pulsed-Doppler echocardiogram f rom the dog shown i n Figure 20. The sample volume was placed between the cardiac mass lesions in the tricuspid orifice. A high-velocity diastolic signal that exceeds 1 mlsec suggests that the mass is causing stenosis of the right ventricular inlet. The E and A waves are sum- mated because of sinus tachycardia. An aliased je t of tricuspid regurgitation also is recorded during some cardiac cycles. are noteworthy. Abnormal valve motion is often observed and includes reduced opening (steno- sis or low cardiac output) (Fig. 25), exuberant motion or prolapse (myxomatous disease, valve dysplasia), diastolic fluttering and premature mitral valve closure (semi-lunar valve regurgi- tation), (Fig. 23) and chaotic motion (ruptured or avulsed valve support apparatus)." While di- astolic mitral valve fluttering can develop with a lesion of any aortic cusp, clinical and experi- mental studies suggest that fluttering of the ventricular septum can indicate a lesion of the noncoronary cusp (Fig. 8C). Systolic mitral valve fluttering has been observed with myxo- matous disease in dogs with musical murmurs. Midsystolic closure of the aortic valve has been observed with a number of lesions including congenital subaortic stenosis in dogs. Finally, but no less important, is the understanding that pulsed- and continuous-wave Doppler can be used for identification of abnormal blood flow caused by valvular di~ease. '~~~" '~ Thus, Doppler studies often verify the cause of heart murmurs (Figs. 8,11,15,20,24, Color Plates 1,3,4). The clinician can estimate the hemodynamic severity of the lesion by combining data from M-mode, two-dimensional, and Doppler studies. The hemodynamic significance of valvar lesions can be estimated by quantifying the adaptive responses of the cardiac chambers and great vessels to valvular incompetency or obstruction. In this regard, dilatation, hypertrophy, and post-stenotic dilatation are recognized through serial studies or by comparing the animal's echocardiographic data to normals of similar body size (Figs. 4,9,10,12,23).19*27~28.30'93 In cases of mitral regurgitation, calculation of left ven- tricular shortening fraction is useful in distin- guishing animals with dilated cardiomyopathy from those with myxomatous valvular disease where the ventricle is hypercontractile.2'~'3~165~166 Experimental data in dogs suggests that mitral regurgitant fraction might be estimated by Doppler ech~cardiography.~~' Analysis of ven- tricular septal position, radius of septal curva- Figure 22. M-mode echocardiogram f rom a dog with infiltrative myocardial disease who was examined for unexplained periods of ventricular tachycardia (see ECG). The left ventricular wall (LVW) is markedly thickened, hypokinetic, and inhomogeneous in echo- genicity, with layers of relative sonolucency. Two-di- mensional images (not shown) indicated multifocal tu- morous thickening of the right ventricular wall and diffuse infiltration within the left ventricular free wall and apex. These findings are typical of neoplosia, how- ever, additional studies were not permitted and a nec- ropsy was not obtained in this dog. E N D 0 = left ven- tricular endocardium; E P I = left ventricular epicar- diumlpericardial interface; IVS = interventricular septum; RV = right ventricle; LV = left ventricle. 248 ECHOCARDIOGRAPHY: A Jrnl. of CV Ultrasound & Allied Tech. Vol. 6, No. 3,1989 VETERINARY ECHOCARDIOGRAPHY Figure 23. M-mode echocardiogram from a cow with aortic valve endocarditis, aortic insufficiency, and congestive heart failure. The left ventricle (LV) is dilated, the left ventricular wall (L VW) hypercontractile, and there are diastolic thumbprint echoes (open arrow) i n the outflow tract which represent prolapsing of a flail aortic cusp. The right panel, obtained across the aortic root (A) and the affected aortic valve (AV), shows the vegetation (VEG) in diastole. There is diastolic fluttering of the mitral valve (arrow) secondary to aortic regurgitation and premature closure of the anterior (AMV) and posterior (PMV) mitral valve leaflets (arrowheads) suggesting elevated end-diastolic pressure. ture on the short-axis image of the left ventricle, and septa1 motion during the cardiac cycle pro- vides information regarding relative right ven- tricular volume and pressure (Figs. 2,4,12).l14-l17 The modified Bernoulli equation, shown to be accurate in canine models of aortic and pulmo- nary obstruction and in spontaneous subaortic s t e n o ~ i s , 5 ~ - ~ ~ has been applied clinically to esti- mate severity of valve obstruction (Figs. 11,24). The continuity equation has been successfully applied to canine models of aortic valve stenosis to assess valve cross-sectional area.184 A sudden drop-off in the velocity profile can be observed during spectral recordings of valvular regurgi- tation when there is elevation of ventricular end-diastolic p r e ~ s u r e . ~ , ~ In well compensated states, the estimated pressure drop across the insufficient valve is maintained throughout the regurgitant period (Figs. 11 & 24). Myocardial Diseases Although dogs and pigs are extensively used in studies of myocardial ischemia and infarc- ~~on,67,69,70,104,106,1~5,186 spontaneous myocardial disorders in animals are rarely caused by coro- Vol. 6, No. 3,1989 ECHOCARDIOGRAPHY: A Jml. of CV Ultrasound & Allied Tech. 249 BONAGURA AND MILLER Figure 24. Continuous-wave Doppler echocardio- gram from a golden retriever puppy with congenital pulmonic stenosis. T h e right ventricular outlet velocity is increased to approximately 2.8 mlsec (PS); there is associated low-velocity pulmonary insufficiency (PI). nary stenosis. Of greater importance to veteri- narians are myocardial traurnala7that result from automobile accidents, and cardiomyopa- thies that have been recognized in many spe- cies.188-201 While dilated cardiomyopathy de- Figure 25. M-mode echocardiogram obtained from a n Irish Setter dog with catheterization-proven mitral stenosis of uncertain cause. T h e anterior (AMV) and posterior (PMV) leaflets do not separate normally dur- ing diastole and there is reduction of mitral E-F slope. T h e anterior leaflet is moderately thickened. (From Pipers FS, Bonagura JD, Hamlin RL, et allm with permission). Figure 26. Two-dimensional echocardiogram, re- played f rom videotape and frozen during diastole. Right parasternal four-chamber image optimized for the left ventricular inlet, A thickened, myxomatous mitral valve is evident, especially the anterior leaflet (AMV). Real-time imaging revealed the typical hypercontractile left ventricle observed in this primary valvular lesion. LA = left atrium; LV = left ventricle. velops sporadically in large animals and pet fer- rets, it is most common in large breed dogs and represents a major cause of cardiovascular death in this species (Fig. 10A).29~40~44J88J91Jg4Jg6 Figure 27. Two-dimensional echocardiogram fro- zen during diastole in a dog with severe heartworm disease caused by Dirofilaria immitis. Right paraster- nal short-axis view at the, mitral valve level. The hy- perechoic areas within the tricuspid valve orifice repre- sent adult heartworms. T h e markedly dilated main pulmonary artery and flnttened interventricular sep- tum are due to pulmonary hypertension. 250 ECHOCARDIOGRAPHY: A Jml. of CV Ultrasound & Allied Tech. Vol. 6, No. 3,1989 VETERINARY ECHOCARDIOGRAPHY Figure 28. Two-dimensional echocardiogram fro- zen during diastole. Right parasternal long-axis four- chamber image from a cat with an endocardial cushion defect. Note the loss of atrial septum and the abnormal appearance of the edge of the ventricular septum. The right atrium and ventricle are dilated. RA = right atrium; RV = right ventricle; LA = left atrium; LV = left ventricle. Dilated cardiomyopathy is also observed in dogs undergoing treatment with doxorubicin and in puppies with parvovirus myocarditis.'30~'90~198 Until recently, dilated cardiomyopathy was common in at^.^^^^^^^^^^^^^,^^^ Identification of low plasma taurine concentrations in most af- fected cats2" and correction of this dietary problem has virtually eliminated the condition in the United States and Canada. Currently, most feline myocardial diseases are related to either idiopathic hypertrophic cardiomyopathy (Fig. lOB), hyperthyroid heart disease (a fre- quent disorder of aged ~ a t s ) , ~ ~ , ~ ~ ~ , ~ ~ ~ , ~ ~ ~ and hy- pertensive heart disease (associated with chronic renal failure).'28 Echocardiographic features of dilated cardio- myopathy in animals include generalized car- diac dilatation, global hypokinesis of the left ventricle (regional dysfunction develops in some dogs), reduced fractional shortening (usually < 20%) and aortic root excursion, in- creased E point to septal separation (typically > 8 mm in the dog), and decreased left ventricu- lar wall and interventricular septal thickening fractions. The mitral valve may exhibit a de- layed systolic closure characterized by a B shoulder between the A and C points of mitral excursion on the M-mode echocardiogram. Doppler echocardiography indicates mitral re- gurgitation, tricuspid regurgitation, and in- creased aortic acceleration time, a finding that would be anticipated from animal studies of in- duced myocardial fai1~re.l'~ Atrial fibrillation and ventricular tachycardia are frequent com- plications of dilated cardiomyopathy in dogs. The potential hemodynamic consequences of these rhythm disturbances can be appreciated through the altered valve motions, ventricular contractions, and Doppler velocity signals that are observed.lss Hypertrophic cardiomyopathy in cats is rec- ognized by Doppler echocardiography through the identification of symmetric or asymmetric left ventricular hypertrophy, reduction of ven- tricular luminal volume, normal to increased shortening fraction, left atrial enlargement (with left atrial thrombus in some cases, Fig. 19), and possibly systolic anterior motion of the mitral va1ve.29,44,189,193 D oppler studies may dem- onstrate left ventricular outflow obstruction, mitral regurgitation (Fig. 15), and increased late diastolic ventricular inlet velocities, however, no detailed study of diastolic function in these cats has been reported. Systemic hypertension and hyperthyroidism (from functional thyroid adenomas) can induce similar changes in the echocardiogram. With hyperthyroidism, how- ever, left ventricular shortening fraction is usually supranormal, often > 50% and most ab- normalities revert towards normal following successful treatment of the thyrotoxico- The echocardiographic findings of experi- mental myocardial contusion in dogs are similar to those observed in a limited number of clinical cases and include increased end-diastolic thick- ness, decreased regional systolic function, in- crease in echocardiographic brightness, and as- sociated pericardial effusion. Sonolucent zones within the myocardium correlated to areas of hematoma.la7 We have observed similar find- ings in cases of intramyocardial neoplasia caused by lymphosarcoma or metastatic carci- noma (Fig. 22), however, associated clinical findings and the tendency towards areas of neo- plasia associated nodularity permit these condi- tions to be distinguished. sis~44,193,195,197,201 Vol. 6, No. 3, 1989 ECHOCARDIOGRAPHY: A Jrnl. of CV Ultrasound & Allied Tech. 251 252 BONAGURA AND MILLER Figure 14 Color Plate 2 Color Plate I Color Plate 3 Color Plate 4 Color Plate 5 ECHOCARDIOGRAPHY: A Jml. of CV Ultrasound & Allied Tech. Vol. 6, No. 3, 1989 VETERINARY ECHOCARDIOGRAPHY Color Plate 6 Color Plate 7 Color Plate 8 Figure 14. Pulsed-Doppler echocardiogram from a clinically normal dog under general anesthesia. The sample volume was placed in the pulmonary outflow using a left apical angled image optimized for the long axis of the pulmonary artery. Pulmonary ejection velocity (depressed owing to anesthesia) and low-velocity pulmonary insufi- ciency (PI) are noted. Thepressure trace at the top is from the aorta. Color Plate 1. Two-dimensional echocardiogram frozen during systole (videotape playback) from a dog with myxomatous atrioventricular valvular degeneration. The right parasternal long-axis view is optimized for the inlet valves. Color flow imaging demonstrates jets of both tricuspid (TR) and mitral (MR) regurgitation. A variance map was used, R A = right atrium; R V = right ventricle; LA = left atrium; LV = left ventricle. Color Plate 2. Two-dimensional echocardiogram frozen during systole from a horse with a ventricular septa1 defect. Right parasternal long-axis image optimized for the left ventricular outflow tract (LVOT). Color flow imaging demonstrates left-to-right shunting (arrowheads) into the inlet of the right ventricle (RV). A variance map was used. LA = left atrium; Ao = aorta. Vol. 6, No. 3, 1989 ECHOCARDIOGRAPHY: A Jrnl. of CV Ultrasound & Allied Tech. 253 BONAGURA AND MILLER Color Plate 3. Two-dimensional echocardiogram frozen during systole from a horse with tricuspid regurgitation. Right parasternal long-axis image, ventral position. Color flow imaging demonstrates a regurgitant je t (arrow) with some signal aliasing at the valve. An enhancedlvariance map was used. RV = right ventricle; LV = left ventricle; Ao = aorta; I V S = interventricular septum. Color Plate 4. Two-dimensional echocardiogram frozen during systole from a dog with
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