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Dr. Vittorio Dall'Aglio - Medico Chirurgo specialista in Cardiologia - Pordenone
 

Qualitative ultrasonic tissue characterization of the myocardium


G.L.NICOLOSI, C.LESTUZZI, D.PAVAN, V.DALL’AGLIO, R. MIMO, M.BREDA G. D’ANGELO, P. PIGNONI, D. ZANUTTINI

With the technical assistance of:
E. MIOTTO, N. FAGGION, E. CANTON

From the Cardiologia-Emodinamica, Ospedale Civile, Pordenone (Italy)
 


Address reprint requests to: G. L. Nicolosi -Emodinamica-Cardiologia, Ospedale Civile, Via Montereale, 24 - 1-33170 Pordenone (Italy).
Received February 17, 1988, accepted March 15, 1988.

Introduction

During the last decade the application of ultrasound to clinical cardiology has offered major advances for the solution of the problem of making the most accurate cardiac or cardiovascular diagnosis and for the process of clinical decision making.[1]
Clinical applications of echocardiography can provide several types of information, mainly concerning myocardial wall motion and thickness, cardiac valves morphology and function, intracardiac dimensions and geometry, intracardiac blood flow patterns and derived estimates of pressures, gradients and filling and emptying properties.
A relatively new field of interest in cardiac ultrasound is the attempt to evaluate myocardial tissue characteristics, based on the acoustic properties of the heart. This type of information should allow to increase the amount of physical indicators of a cardiac disease, with the potential of increasing sensitivity and accuracy of a cardiac diagnosis by ultrasound.[1]
The optimal method of detecting this type of information, however, has not yet been developed or identified.

Furthermore, generally speaking, we have to consider that the optimal method of detection can vary from situation to situation, and different solutions can be offered to solve different diagnostic problems. On the other hand, the solution for the same problem can be achieved by using different approaches.[1] This comprehensive model of multiple approaches to ultrasound tissue characterization is in agreement with the complexity of interactions between ultrasound and the myocardium and with the need of a useful display of all informations. In fact several significant problems are still facing ultrasound tissue characterization.[23] The phenomenon of interaction between ultrasound and the myocardium and its spatial and temporal variations are not completely understood. In addition, the complicated integration between contractile patterns of motion and rotational and translational motion of the heart within the thorax do not allow an easy identification and analysis of the cardiac regions of interest. Furthermore the influence of interposed tissue between ultrasound source and cardiac targets has not yet been completely defined.
For all these reasons the term "ultrasound tissue characterization" covers a range of meanings from qualitative evaluation to quantitative assessment.[4]

Fig. 1—Apical two-chamber echocardiographic view in a patient with left ventricular hypertrophy and small calcific deposits at the level of the mitral annulus and at the apex of the papillary muscle (arrows) (LA=left atrium; LV=left ventricle).

Qualitative ultrasonic tissue characterization

Qualitative ultrasonic tissue characterization is based on the subjective visual analysis of final displayed images or tracings by trained observers. Images must be processed and the display adjusted in a way to provide the best possible image for the qualitative evaluation of the myocardial texture.5 Images are considered adequate when all regions of the myocardium can be displayed on the screen at approximately equal brightness, utilizing the widest range of gray levels ("equalization" of images) [5] (Fig. 1).
This is achieved by manipulation of the machine parameters settings, which include depth, brightness, and control settings of the display oscilloscope, coarse and fine overall gain control, time-gain compensation control, and systemic dynamic range and echo enhance controls. Because of many variables, such as the thickness of the chest wall, depth of the cardiac structures from the transducer and their orientation in relation to the direction of ultrasonic beam, the instrument gain as well as the time-gain compensation curve require individual adjustment for examination of any given myocardial wall segment.[5-7]
The complete two-dimensional echocardiographic recording is qualitatively analized in real-time, frame-by-frame and still frame mode to identify changes in myocardial texture and to evaluate the visual appearance of the amplitude and spatial distribution of echo signals reflected by the myocardium.[5 6] Myocardial echogenicity is then characterized on the basis of uniformity or nonuniformity of spatial distribution of low and high amplitude echo signals, taking also into account their relative dimension inside the image.[58]

Localized calcification and fibrosis

Abnormal tissues assisted in fact the very early beginning of echocardiographic experience in 1953 by Edler and Hertz,[9] because the sensitivity of the transducer used at that time only allowed the recording of strong echoes from diseased and not from normal mitral valves.
Since that time one of the most common application of the qualitative evaluation of echocardiographic images was the identification of calcification or fibrosis, and their differentiation from valvular vegetations and mixomatous degeneration.[10-16] Calcification of valvular apparatus can be defined as a localized increase of echogenicity with increased brightness and uniform texture, which can impair pliability and mobility of structures and which can be visualized at least in two different planes (Fig. 1 and 2).
Echocardiographic diagnosis shows generally high sensitivity and specificity even though the differentiation between heavy fibrosis and calcification can be sometimes difficult. It must be taken also into account that the use of higher frequency high resolution transducers may increase problems of differential diagnosis, because of higher definition and potentially higher brightness of small targets inside the context of tissue texture.

Fig. 2.—Short axis parasternal echocardiographic views at the level of the aortic valve. In (A) diastolic frame in a patient with a small nodular calcific deposit at the level of the anterior aortic cusp (arrow). This small calcification can also be seen in systole (arrow in (B)), when it appears to impair mobility of the cusp itself. The nodular appearance of this calcific deposit could induce difficulties in the differential diagnosis with vegetations. This patient, however, had no signs of infective disease. In (C) diastolic frame in an other patient with a small area of increased echogenicity at the level of the commissure between the anterior and the posterior aortic cusps (arrow). The differential diagnosis between calcification and heavy fibrosis can be difficult in this case. Pliability and mobility of the cusps are however only slightly impaired in systole (D). In systole (D) all the edges of the three cusps show increased thickness but lower echogenicity, suggestive for fibrosis.

In an unpublished series of 32 valves of 8 randomly selected autopsied hearts, where all four valves were excised (7 males, 1 female, age range 44-84 years, mean 66 years) we tried to evaluate if two-dimensional echocardiography can be sensitive and specific for minimal calcification on all 4 heart valves. In this "worst case" project we examined in vitro all the excised valves by a 5 MHz linear array transducer. This project was defined as "worst case" because in this unselected population a low prevalence of calcification was expected and calcification could be expected to be minimal, when present. There .was also no possibility to analyze pliability and mobility of valves. In addition all the valves were excised, and no comparison was possible with echogenicity of other tissues. Blind two-dimensional echocardiographic analysis was made on the recorded images by two observers who defined the presence of calcification by agreement. Blind X-ray analysis on excised valves was performed by two independent observers. Extensive calcification was absent in all these valves.
In this experimental "worst case" situation sensitivity and specificity were low (64.3% and 61,1% respectively) with a positive predictive accuracy of 56.2% and a negative predictive accuracy of 68.7%.
Without taking into account other clinical data or parameters, differential diagnosis can also be sometimes difficult, in individual cases, between non mobile vegetations and localized mixomatous degeneration or fibrosis or minimal calcific deposits (Fig. 1 and 2).
In conclusion, qualitative tissue characterization of calcific deposits is sensitive and specific for large calcification.
Sensitivity and specificity are thus size and site dependent, inside cardiac structures. There is a tendency to overestimation of calcine deposits.

Fig. 3.—Long axis parasternal echocardiographic systolic view in a patient with remote anteroseptal myocardial infarction. Fibrotic scar (arrow) can easily be differentiated from normal myocardial texture of the basal portion of the interventricular septum. Fibrotic wall shows decreased thickness and increased echogenicity with homogeneous texture (A0= aorta).

Fig. 4.
—Long axis parasternal view in a patient with hypertrophic cardiomyopathy. The tomographic section is modified in order to visualize a localized area of "granular" appearance of the myocardium at the level of the septum (large arrow). The endocardial plaque at the left ventricular edge of the septum (small single arrow), and the increased echogenicity at the level of the anterior mitral leaflet and subvalvular apparatus (double arrow) are also seen.

Predictive accuracy for a negative diagnosis is superior than for a positive diagnosis. The assessment of local and general pliability and mobility of valve structures is important. Comparison with the echogenicity of other cardiac structures is essential. When calcific targets are very small, echogenicity may be similar to non calcific targets. Differentiation between calcific and non calcine targets can be difficult in this situation.

Changes of the echogenicity of the myocardium

Increased echogenicity with homogeneous texture can be seen inside a myocardial wall with absent systolic thickening, as in the case of a fibrotic scar after myocardial infarction. The identification of this zone of increased echo genicity can be made in comparison with other segments of the myocardial wall with normal acoustic appearance and thickening (Fig. 3).
A generalized increase in the acoustic density of the myocardium, especially of the interventricular septum, and an increase in myocardial mass have been observed in acute rejection after cardiac transplantation.[17]
In patients with hypertrophic cardiomyopathy the interventricular septum can display an unusual pattern of texture of echo amplitudes with bright echoes of unequal shape and dimension separated from one another by lower amplitude echoes. This appearance can be localized or diffuse, with "granular" or "spot-like" appearance of the myocardium[2 6 18-20] (Fig. 4).
The pathologic and histologic significance of this finding is uncertain and there is no proof that this observation can be related to abnormal myocardial structure or fiber arrangement. In hypertrophic cardiomyopathy echocardiography is also able to identify increased echogenicity of the endocardium on the septum opposite to the mitral anterior leaflet.
This could represent the endocardial plaque usually seen in necropsy studies.[8 19-21] (Fig. 4).

Fig. 5.—Four-chamber apical view in a case of right ventricular endomyocardial fibrosis. The right ventricle is obliterated by fibrotic tissue with non homogeneous echogenicity (arrow).

Fig. 6.—Modified foreshortened longitudinal apical view of the left ventricle and papillary muscles (arrows) in a case of amyloid heart disease. This modified view allows to appreciate the peculiar myocardial echogenicity.

An increased echogenicity, suggestive of fibrosis, can also be seen at the level of the anterior mitral leaflet or papillary muscle, in agreement with pathological studies[21] (Fig. 4).
Restrictive-obliterative cardiomyopathy, due to endocardial fibrosis, is characterized by increased echogenicity of the endocardium at the level of the right and/or the left ventricle and by masses which can obliterate ventricular cavities. The distribution of fibrous tissue is frequently localized at the apex of either or both ventricles[8 18 19 22] (Fig. 5).
In amyloid heart disease abnormal changes of myocardial texture are frequently seen together with increased atrial septal and valves thicknesses.[2 5 6 l8 23 24] Myocardial echogenicity is characterized by multiple, discrete, and small highly refractive echoes, separated from one another by low intensity echoes. Highly refractive echoes can be present in all or part of the walls of the ventricle or ventricles in different patients (Fig. 6).
In a minority of patients with idiopathic haemochromatosis we have shown abnormal myocardial texture with increased echogenicity at the level of the endocardium25 (Fig. 7).
 

Fig. 7.—Short axis parasternal view in a patient with idiopathic haemochromatosis in diastole (A) and systole (B). Arrows are indicating increased echogenicity of the endocardium.

Fig. 8.—In (A) modified four chamber apical view with aorta (AU) in a case of dilated Cardiomyopathy with a large fresh left ventricular thrombosis (arrow). Fresh thrombus shows highly reflective non homogeneous texture with "granular" appearance. This thrombus formation completely disappeared at the follow-up echocardiographic examination performed 13 days later. During this period of time the patient was treated with anticoagulants and conventional therapy for congestive heart failure. No signs of peripheral embolization were detected. In (B) a four chamber apical view is shown, obtained in another patient with dilated cardiomyopathy and spontaneous intracavitary low echogenicity contrastographic effect (arrow) due to regional stasis of blood. This slow velocity curling blood is better seen in real time images.

Although clinical and laboratory data of those patients with idiopathic haemochromatosis and with and without hyperechogenic endocardium showed no difference in the stage of the disease, haematological indexes of iron overload and quantity of iron removed by phlebotomy up to the time of examination, the possibility that these two patients could have a higher myocardial iron content than the other cannot be excluded.[25] Our finding of an association of abnormal echogenicity, possibly related to increased myocardial iron content, with typical HLA antigens, suggests the possibility of a genetic variability also in the involvement of target organs.[25] This possibility should be further explored.

Intracardiac and paracardiac masses

Echocardiography is very useful for the qualitative evaluation of echogenicity of intracardiac and paracardiac masses.[26-28]
In cases of intracavitary thrombosis echocardiography can be helpful to differentiate fresh from old thrombi.[29-31]
Fresh thrombi appear acoustically highly reflective, with echo-dense non homogeneous texture and "granular" appearance (Fig. 8A).
Old thrombi have a more homogeneous echogenicity with "ground glass" appearance and usually more precisely denned contours with linear edges (Fig. 9).
Intracavitary thrombosis can be usually differentiated from spontaneous intracavitary low echogenicity contrastographic effect due to regional stasis of blood or, on the contrary, to increased velocity of flow, as in hyperkinetic hearts (Fig. 8B).[31 32] The possibility to visualize this contrastographic effect seems to increase with high frequency transducers.[32]
Intracavitary primary cardiac neoplasms, such as mixoma, can be easily identified by echocardiography.[26 28]
Echocardiographic texture of these tumors can also be characterized by the presence of haemorrhage or cystic changes inside the tumor, and by the definition of contour characteristics of the surface of the tumor itself [28 33 34] (Fig. 10).
Secondary neoplastic infiltration of the myocardium can also be diagnosed by echocardiography[26 28 35 36] (Fig. 11). The infiltrating masses have usually a peculiar, "granular" echocardiographic texture. The echogenicity might change using different instruments and electronics rather than mechanical sector scanners, but the infiltrated areas always appear different from the normal myocardium.
 

Fig. 9.—In (A) an old thrombus is shown (linear arrow) with "ground glass" appearance and precisely defined contour with linear edges. Curved arrow is indicating spontaneous contrast effect inside the left atrium due to regional stasis of blood. This view was obtained by the transesophageal approach with a 5 MHz transducer (Aloka transducer model UST-5220V-5). This patient had left atrial thrombosis which was documented from the transthoracic approach and appeared unmodified after several months of anticoagulation. In (B) the four chamber apical transthoracic view of the same patient is shown. Left atrial thrombus is indicated by the arrow. The transesophageal study was performed in order to evaluate the echogenicity and the potential risk of embolization of the thrombotic formation, not clearly defined by the transthoracic approach, due to the distance of the target from the transducer. The transesophageal approach allowed to decrease drastically this distance and to analyze tissue characteristics of the thrombus.

Fig. 10.—In (A) modified four chamber apical view in a patient with left atrial myxoma. The arrow is indicating round cystic areas with low echogenicity inside the tumor. The tumor shows irregular edges and non homogeneous texture. In (B) the modified four chamber subcostal view is showing the basal attachment of the same tumor at the level of the interatrial septum (arrow). This basal portion of the tumor is showing increased echogenicity as compared to the ventricular part.
 

Neoplastic myocardial infiltration can be defined by the presence of one of the following findings: (1) dysruption of continuity of the endocardial or epicardial contours by an akinetic mass, whose echogenicity differs from normal myocardium; (2) presence of intramural akinetic mass, different from normal myocardium for its peculiar "granular" echogenicity; (3) reduced kinetic of a normally thickening ventricular wall, due to adhesion to a paracardiac or intra-pericardial neoplastic mass.
The differential diagnosis between intra-cavitary neoplastic masses and thrombi is based on the finding of an interruption of the endocardial contour by the infiltrating masses (while thrombi are usually adherent to the endocardium) and by the normal or increased thickness of the ventricular wall which is infiltrated by the neoplasm, as compared to walls with reduced thickness in cases of thrombi.[35 36] Intrapericardial masses can have similar echogenicity and can be differentiated from fibrinous strands[37-41] (Fig. 11B).

Fig. 11.—In (A) modified four chamber subcostal view in a case with metastatic infiltration of the right ventricular myocardium and obliteration of the right ventricle by a metastatic mass from a kidney carcinoma (arrow). The mass has a round shape and low echogenicity peculiar texture, which is different from the normal myocardium (L=liver). In (B) a four chamber apical view is shown in a case with metastatic infiltration of the myocardium by a lung carcinoma. The infiltrating masses are shown by the arrows and are located at the epicardial site of the left ventricular and right ventricular apex. A large pericardial effusion (PE) is also present.
 

Discussion and conclusions

Qualitative ultrasonic tissue characterization is based on the visual analysis of echocardiographic images by trained observers. This type of evaluation has several important limitations. In fact qualitative
analysis is Subjective and operator dependent.
Technical and technological limitations are also important due to the fact that image processing is dependent on the equipment and on the adjustment of the display. Furthermore the echocardiographic image is in fact an "artifact", which is produced and built-up in different ways by different machines, different transducers, different hardware and software configuration of the equipments, different parameters settings. As a result of this, echogenicity of cardiac structures could be different with different equipments. In fact different equipments may have different capability to show myocardial texture and echogenicity of cardiac and paracardiac structures. On the other hand the angle of incidence of the ultrasound beam on cardiac structures and the distance of the target from the transducer can also influence the qualitative texture analysis [42] (Fig. 9).
To fight limitations, multiple orthogonal approaches and views should be performed. This could help also to reduce the distance between the acoustic target and the transducer (Fig. 9). Multiple observations by different trained observers should be obtained. A good quality "equalized" echocardiographic image is essential for reliable qualitative tissue analysis.
High quality recording systems can help for storing images which can be later carefully evaluated in real time, slow motion and stop-frame mode.
Clinical-pathologic correlations and comparison with different techniques, such as computed tomography and nuclear magnetic resonance, should be always searched for, to improve sensitivity and specificity of the qualitative analysis.
In the same patient comparison and analysis should be made by using the same type (types) of equipment with the same (similar) settings. The group of observers involved in qualitative tissue
characterization should be similarly trained and deeply involved. Adequate knowledge of performances of each type of equipment should be achieved.
Qualitative tissue characterization should be made by the evaluation of regions of the image which are comparable for depth, image quality, site inside the image field and gray scale.
For all these reasons qualitative tissue characterization could be considered, perhaps, as an intermediate step before switching to quantitative evaluation. On the other hand quantitative approach for ultrasonic tissue characterization can give detailed objective information but it is difficult to apply, it shows a high cost/ efficacy ratio and it does not seem to be ready for routine clinical use at the present time. Qualitative approach for ultrasonic tissue characterization has thus the advantage, in spite of its several limitations, of beeing clinically usable in routine daily practice, with the possibility of a major impact in the process of clinical decision making.
For all these considerations we feel that at the present time quantitative and qualitative approaches to ultrasonic tissue characterization of cardiac structures have a complementary important role in cardiology.
Further studies however are needed to overcome empirical approaches, to improve standardization and to obtain more reproducible results. The most important piece of knowledge must still come from studies on the basic mechanisms of ultrasound-tissue interactions [2 3] in order to base future methods of tissue characterization on more solid ground and to guarantee reliable and useful informations for the cardiologist.

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