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Keywords:

  • Heart enlargement;
  • Heart failure;
  • Radionuclide angiocardiogram

Abstract

  1. Top of page
  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Footnotes
  8. Acknowledgments
  9. References

Background: The contribution of right heart (RH) chamber enlargement to general heart enlargement seen on thoracic radiographs in mitral regurgitation (MR) is not known.

Objectives: To determine the size and shape of the RH chambers in normal dogs and dogs with varying degrees of MR.

Animals: Fifty-four privately owned dogs: 13 normal, 41 with varying degrees of MR including 25 with congestive heart failure (CHF).

Methods: Archived first pass radionuclide angiocardiograms were used to produce static images of the RH and left heart (LH) chambers. Indexes of size and shape of the RH and LH chambers were related to severity of MR determined by heart rate-normalized pulmonary transit time (nPTT), vertebral heart scale (VHS), and clinical status. RH shape was measured by a circularity index of RH short axis/long axis.

Results: A 2nd degree polynomial fit best described the ratios; RH/LH dimension to nPTT (R2= 0.62) and to VHS (R2= 0.43), RH/LH area to nPTT (R2= 0.64) and to VHS (R2= 0.58), all P < .001. RH circularity was decreased in CHF, P < .001. In CHF, the RH chambers of 16 dogs were both flattened and enlarged, whereas 9 had convex septal borders.

Conclusions: RH chambers are not significantly dilated in dogs with mild to moderate MR without CHF. In CHF, RH chambers enlarge and also may be compressed by the LH chambers. Pulmonary hypertension probably is present in some dogs with CHF. Increased sternal contact is not a useful sign of right-sided heart dilatation in MR.

Abbreviations:
CHF

congestive heart failure

FPRNA

first pass radionuclide angiocardiogram

LH

left heart

LV

left ventricle/left ventricular

MR

mitral regurgitation

nPTT

normalized pulmonary transit time

PH

pulmonary hypertension

RH

right heart

ROI

region of interest

RV

right ventricle/right ventricular

SD

standard deviation

TR

tricuspid regurgitation

VHS

vertebral heart scale

Myxomatous mitral and tricuspid valve disease is the most common acquired cardiac disease in small-breed dogs. It affects mainly the mitral valve, but it also may affect the tricuspid valve to a lesser degree.1–6 Mitral regurgitation (MR) causes the left atrium and left ventricle (LV) to become dilated and hypertrophied. These findings are seen in thoracic radiographs primarily as the so-called “general heart enlargement” and left atrial enlargement.5,7–9 The degree of right-sided enlargement is not known.5 Increased convexity and increased sternal contact on lateral radiographic projections are signs of pure right-sided enlargement caused by pulmonic stenosis, tricuspid regurgitation (TR), pulmonary hypertension (PH), or heartworm disease.7–9 These radiographic signs are also seen in dogs with MR, and right-sided enlargement also may contribute to the “general enlargement” seen as MR progresses. Assessment of right-sided enlargement in MR is controversial. Some authors suggest that MR could increase pulmonary vascular pressure, causing pressure overload of the right side,1,3 whereas others think that the pressure generated is not sufficient to cause this right-sided enlargement.4

Right-sided enlargement in MR may be caused by pressure overload, volume overload, or both. Pressure overload causes hypertrophy.10 MR back pressure1,3 or PH4,11–13 are possible causes of pressure overload. Volume overload causes dilatation either by primary TR caused by myxomatous mitral and tricuspid disease or secondary TR due to PH.10–14 However, the prevalence of bivalvular myxomatous disease is only about 30%4 and the prevalence of PH causing secondary TR was 14%,12 which does not seem enough to account for the universal occurrence of radiographic signs compatible with right-sided enlargement. An alternative hypothesis is that the increased curvature of the cranial and right heart (RH) borders seen in MR is simply because of the left heart (LH) chambers pressing on the RH chambers. This is what was found in a canine model of chronic MR studied by 3-dimensional (3-D) magnetic resonance imaging.15

Our hypothesis was that in MR, left-sided heart chamber enlargement predominates with minimal right-sided heart chamber enlargement. The objective of the study was to measure changes in size and shape of the right-sided heart chambers in normal dogs and dogs with varying degrees of MR.

Materials and Methods

  1. Top of page
  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Footnotes
  8. Acknowledgments
  9. References

Study Material

In this retrospective study, archived first pass radionuclide angiocardiograms (FPRNAs) made on 54 privately owned dogs (47 Cavalier King Charles Spaniels, 2 Beagles, 1 Dachshund, 1 Danish/Swedish Farmdog, 1 Jack Russell Terrier, 1 Norfolk Terrier, and 1 Petit Basset Griffon Vendee), normal and with varying degrees of MR, were used from previous studies.16,17 No selection criteria were used other than the owners' permission to do the study. The dogs were classified and divided into 3 groups according to their clinical status as determined by clinical examination, echocardiography, and radiographic examination of the thorax. Thirteen dogs, all Cavalier King Charles Spaniels, were normal. Sixteen dogs had various grades of MR without congestive heart failure (CHF). Twenty-five dogs had CHF and 18 of these were under treatment. Sixteen received only furosemide, and 2 were being treated with furosemide, digoxin, and enalapril.

Procedures

FPRNAs were made within 2–4 hours of clinical and radiographic examinations at the University Animal Hospitals of the Faculty of Veterinary Medicine, Uppsala, Sweden or Helsinki, Finland. All dogs but 6 had 2 FPRNAs done within 30 minutes. The 2nd FPRNAs of 6 dogs were technically inadequate. The dogs were placed in left lateral recumbency on the surface of the gamma camera.a A tight bolus that would provide good temporal separation of the left and right sides of the heart was ensured by placing the dose of technetium-99m DTPAb in a short length of tubing connected to a 3-way stopcock. The bolus was flushed into the cephalic vein with 5–10 ml saline. A frame rate of 10 frames/s for 1 minute during the first pass and a resolution of 64 × 64 pixel matrix were used.

The FPRNA studies were acquired and processed by a dedicated nuclear medicine programc and measurements made using that program or an image processing and analysis program.18 A tight and unbroken bolus of injected volume of radioactivity was a requirement, determined by a full-width half-maximum of <0.1 second of the time-activity curve passage through a region of interest (ROI) over the cranial vena cava. An electrocardiograph was started simultaneously with the gamma camera acquisition.

Static images of the RH and LH chambers were made from both of the FPRNAs. All measurements were done by 1 person (C.C.). Ten to eighteen 0.1 second frames of the dynamic study were summed so that each new frame was 1.0–1.8 seconds. The images were scrolled in time to 1 showing the bolus filling and outlining the right atrium and ventricle. The number of summed frames and the position of the composite frame in the RH chambers were adjusted to minimize overlap of the pulmonary artery and caudal vena cava with the endocardial margins, and maximize the filling of the chambers. This image was saved as a static image. The images then were scrolled in time to 1 in which the bolus of radioactivity was filling and outlining the left atrium and ventricle, and this static image was saved. The static images were interpolated into a 128 × 128 matrix. A red-blue color table was used that gave sharp definition between red and blue for location of ROIs. The threshold at this level was approximately 35% of maximum activity. The short axis across the RH chambers as the maximum dimension (width) below the tricuspid valves was measured 3 times and averaged (Fig 1A–C). A ROI was traced around the right atrium and ventricle 3 times and the number of pixels within the ROI was counted each time and averaged (Fig 1A–C). These measurements were repeated on the left side of the heart (Fig 1D). The short axis across the LH chambers was measured as the maximum transverse dimension below the mitral valve. The pairs of measurements from the FPRNAs were averaged. The RH chambers as a single unit were used rather than the right ventricle (RV) and right atrium because we could not reliably locate the tricuspid valve. For consistency, the LH chambers rather than left atrium or LV were used for comparison.

image

Figure 1.  Static summed frames of the right heart (RH) chambers (AC) of (A) a normal dog with circularity index 0.52, (B) a dog with mitral regurgitation and congestive heart failure (CHF) and a compressed RH chambers (circularity index 0.37), (C) a dog with CHF and a normal ratio of the long and short axis RH diameters (circularity index 0.54) and convex septal border. (D) Static summed frames of the left heart chambers of a dog with CHF. The black arrows are the measured dimensions for short axis and long axis. The yellow line is the tracing of the region of interest (ROI), which was used to measure relative areas.

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The degree of distortion of the RH chambers was measured as an index of circularity, the ratio short axis/long axis (Fig 1A–C). An index of 1.0 indicates a circular figure, whereas flattening decreases the value. The shape of the septal border of the RH nuclear angiocardiogram was assessed subjectively by consensus of 2 observers (C.C. and P.L.) as convex or flattened.

The pump function of the heart was measured as heart rate-normalized pulmonary transit time (nPTT) on each FPRNA.16 nPTT is the number of stroke volumes that the pulmonary vascular bed holds at any given moment by the relationship nPTT = (pulmonary blood volume)/(stroke volume), which also is the number of beats in the transit time through the lungs of a unit of blood, represented by the leading edge of the bolus. In heart pump failure, it takes more heart beats than normal to pump the same amount of blood through the pulmonary vascular bed. Either stroke volume is decreased, pulmonary blood volume is increased, or both occur. In either case, the increased nPTT is evidence of heart pump failure even if output and ejection fraction are not decreased. nPTT was increased in Cavalier King Charles Spaniels with MR both with and without failure.16 The paired measurements were averaged.

Forty-three dogs had radiographs taken of the thorax within 2–4 hours of the FPRNAs. No treatments were given between the 2 examinations. Ten normal dogs and 1 with compensated MR did not have radiographs made in conjunction with the FPRNAs. The heart sizes were measured by 1 person (P.L.) on the left lateral projection by the vertebral heart scale (VHS)19 modified20 to decrease variability in selection of measurement points. Ratios of RH/LH dimension and RH/LH area and circularity index were plotted against severity of MR as assessed by nPTT and VHS.

Statistical Methods

All statistical calculations were performed by a computerized statistical program.d Linear and nonlinear regression analysis was used to evaluate the relationship between the ratios of RH to LH dimension, area and circularity as dependent variables, and nPTT and VHS as independent variables. When the best line of fit (as judged by the adjusted R2 value) had been found, the distribution of residuals in regression analyses (linear and multiregression analysis) was tested for normality by the Shapiro-Wilk W-test. The dogs were grouped according to clinical classes as follows: I, normal dogs; II, dogs with MR murmur and varying degrees of heart enlargement but no CHF; and III, dogs with MR and CHF. Equal variances of the scintigraphic variables among groups were tested by the F-test (variance ratio test). Differences among groups were tested by ANOVA. If a significant difference was obtained among groups, a multiple comparisons t-test (Tukey-Kramer test) was used to determine where significant differences existed. Statistical significance was set at P < .05.

Results

  1. Top of page
  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Footnotes
  8. Acknowledgments
  9. References

The ratio of RH/LH dimension and of RH/LH area were significantly different among the different clinical classes (all P < .001). Ratios of RH/LH dimension plotted against severity of MR assessed by nPTT and VHS are shown in Figure 2A and B, and ratios of RH/LH area against severity of MR by nPTT and VHS are shown in Figure 2C and D. The best relationship between the ratios and nPTT and VHS was described by the polynomial f(x) =ax2+bx+c. In all curves, initially the right side of the heart decreased relative to the left side as nPTT (Fig 2A and C) and VHS (Fig 2B and D) increased. With further increases in nPTT and VHS, the ratio increased slightly. The nadir of the curves relating right-sided area was at 11.7 nPTT units and 13.0 VHS units. The nPTT of the 25 dogs with CHF had a mean value of 11.1 ± 0.4 (standard deviation [SD]) and mean VHS was 13.2 ± 1.1 (SD).

image

Figure 2.  Right heart/left heart (RH/LH) dimension (A, B), area (C, D), and circularity (E, F) related to severity of mitral regurgitation (MR) according to pump function as heart rate-normalized pulmonary transit time (nPTT) and heart size as vertebral heart scale (VHS). In graphs (A)–(D), initially the right side of the heart decreases relative to the left side with severity of MR determined by nPTT and VHS. The curves relating area reach nadir at nPTT = 11.7 and VHS = 13.0. In graph (E), the relationship between circularity and nPTT is similar but not as close (R2= 0.23), while in (F), there is no relationship between circularity and VHS, probably because only 3 normal dogs had thoracic radiographs taken and VHS values while all 13 normal dogs had nPTT values.

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The circularity index had a similar but less well-defined relationship to nPTT (Fig 2E), but the relationship to VHS was poor (Fig 2F). The difference in circularity between normal hearts and hearts with CHF was significant (P < .001), but the relationship was not significant between the other groups. All of the normal dogs had a convex septal border on RH radionuclide angiocardiogram. Of the 16 hearts with compensated MR, 3 were subjectively assessed as having a flattened septal border making the RH chambers appear narrow. Of the 25 CHF hearts, 16 RH chambers appeared narrow and had a flat or slightly concave septal border. Nine had a convex RH septal border.

Discussion

  1. Top of page
  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Footnotes
  8. Acknowledgments
  9. References

The rapid decrease of the RH dimension and area relative to LH dimension and area as heart pump function decreased and size increased (Fig 2A–D) most likely is caused by the RH chambers remaining normal in size as the left side enlarged and its pump function decreased. The right side may enlarge in dogs with mild to moderate MR without CHF, but to a much smaller degree than the left side. The increase in relative size of the RH chambers with severe MR could not be caused by decreasing size of the LH chambers, because LH chambers increase in size until failure and the treatments given would have affected both sides. RV pressure overload with pure RV concentric hypertrophy is unlikely, because concentric RV hypertrophy does not develop in response to PH, and both hypertrophy and dilatation occur together.10,14,21–24

The descending limbs correspond well to the range of dogs without CHF and the ascending limbs to the dogs with CHF (Fig 2). The nadir of 11.7 of the nPTT curve related to relative areas is close to the value of 11.9 ± 3.4 (SD) that was found for a subgroup of dogs in this study that had CHF.16 In this study, the dogs with CHF had a mean nPTT value of 11.1 ± 0.4 (SD). The lower value in the present study could have been caused by the larger number of dogs that had been treated with diuretics that could have improved function. The nadir of 13.0 VHS units was within the range of VHS of the dogs in this study with CHF (13.2 ± 1.1), the same as the average VHS of a group of 10 dogs with New York Heart Association Class III CHF measured by 16 persons (13.0 ± 0.6).20 These comparisons suggest that the increase in the RH/LH curves are related to decompensation and that RH dilatation begins to occur when the heart size and dysfunction indicate impending CHF.

A relationship of dilatation to pulmonary capillary pressures could be implied. Pulmonary edema in chronic LH disease requires a pulmonary capillary pressure of 40–45 mmHg,25,26 which implies only mild PH.12 In our study, however, the RH radionuclide angiocardiograms showed flattened RH even in 3 dogs without CHF and in 16 dogs with CHF. Other studies have indicated either no significant RV pressure overload in canine MR27 or in only 14% of cases.12 RH dilatation could be secondary TR rather than PH. Secondary TR with normal pulmonary arterial pressures is caused by septal dysfunction, when the septum is hypokinetic, dyskinetic, or dilated, regardless of the size or function on the RV.28 A consequence of the RH being compressed by the dilated and remodeled LH could be distortion of the tricuspid valve annulus and secondary TR, and a change in RV geometry that displaces the septal papillary muscle.29

Apparently, the RH chambers can be both enlarged by volume overload and distorted by the dilated LH chambers compressing the RH chambers when MR is severe enough to cause CHF. In an experimental model of MR, this compression caused the RV end diastolic volume to decrease, but RV stroke volume was maintained and RV ejection fraction increased despite decreased end diastolic volume and end systolic volume, apparently by systolic interaction between the ventricles,15 whereas in our study RH chambers increased in volume after CHF. The difference may have been due to the study on experimental MR being only of 5–6 months' duration, and the pathophysiologic changes may not have been as severe as in the natural disease. Primary TR in the form of myxomatous tricuspid disease may have played a role in the natural disease.

The position and shape of the interventricular septum is determined by the transseptal pressure gradient.27,30–32 The shape of the septal borders of the RH and LH radionuclide angiocardiograms and the RH circularity index provide information about the transseptal gradient. In experimental severe MR, the septum bulged to the right15 and in clinical MR of small-breed dogs the LV became more spherical,33 which also means that the septum bulged to the right. In RV pressure and volume overload, the septum was displaced to the left (septal flattening on echocardiography).27,30–32 In our study, in CHF the RH septal border was flattened in 16 dogs. This change and decreasing circularity (Fig 2E) indicates that the septum was bulging rightward, caused by a transseptal gradient displacing the septum. As the threshold for pulmonary edema is 40–45 mmHg,25,26 RV systolic pressure would not have reached this level in the 3 hearts with flat septal margins on the RH radionuclide angiocardiograms that were not in CHF nor in the 16 hearts in CHF with flattened septal margins. However, the convex septal borders on 9 RH radionuclide angiocardiograms and increasing RH circularity in severe MR (Fig 2E) indicate that RV pressures had increased, at least to the threshold of pulmonary edema pressure, but the increase probably still were mild, as found in a study12 in which the majority of dogs with CHF caused by MR had mild PH (30–50 mmHg).

When the RH chambers are compressed as the LH chambers enlarge, they contribute little to the increased convexity and sternal contact on the lateral radiograph (Fig 3A–C). Only in cases where the RH becomes rounded and dilated, in severe MR with CHF, does the RH bulge outward and contribute to the convexity of the cranial heart border (Fig 3D).

image

Figure 3.  Radionuclide right heart (RH) and left heart (LH) chamber angiocardiograms superimposed on their corresponding lateral radiographs. (A) Dog with mild heart enlargement (VHS 11, circularity 0.52). (B) Dog with a moderately enlarged heart (VHS 12.9) without congestive heart failure (CHF). The RH chambers are not compressed (circularity 0.56). (C) Heart in CHF with moderate enlargement (VHS = 11.9). The RH chambers are compressed (circularity 0.41) and the septal border is flattened. (D) Heart in CHF with a normal ratio of the long- and short-axis RH diameters (circularity 0.54), convex septal border, and severe heart enlargement (VHS = 13.1). Note that all hearts with MR have increased sternal contact and convexity regardless of the size of the RH chambers.

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Limitations of the Study

Spatial resolution was low: the resolution of the interpolated images was 2.9 or 3.1 mm depending on the gamma camera used. Edge detection algorithms for heart chambers rely on the edge being a smooth transition to which a threshold can be applied. Interpolation is a valid method of improving resolution at the edge of a heart chamber by smoothing the transition. Also, the change of heart chamber size between systole and diastole would have blurred the edges, because the summed images used incorporated all phases of the heart cycle. It was not possible to apply an edge detection algorithm to the images because of interference by extraneous activity. However, the validity of the interpolation and subjective color threshold to produce significant results is shown by the high R2 values of the curves. Because of poor spatial resolution, we could not reliably separate the atria from the ventricles and thus measured them as 1 chamber.

We used relative and not absolute dimensions and areas because the varying size and body condition of the dogs over a small weight range would have made indices related to body size inaccurate.34 A 2-dimensional (2-D) measurement (area) gives a more accurate estimate of volume than a 1-dimensional measurement because it takes more pixel information into account. We measured RH/LH dimension because dimension was measured for the circularity index.

This study was retrospective, and at the time, echocardiographic techniques and magnetic resonance angiocardiography were not available for detailed analysis of the heart. Increased volume when the RV is compressed could not have been detected by 2-D echocardiography on the conventional short-axis view of the heart. The areas measured of the LH chambers are only indications of the volumes of the chambers, because the volume of the LV and left atrium are closely related to short and long axes and areas, but the geometry of the RV is irregular and a direct relationship between area or dimension and volume cannot be assumed. Today, with 3-D and tissue Doppler echocardiography11,22,35 and magnetic resonance angiocardiography available,15,21 the effect of ventricular interaction and role of the RH chambers in MR can be investigated in detail, preferably using a prospective longitudinal study.

Conclusions

  1. Top of page
  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Footnotes
  8. Acknowledgments
  9. References

In compensated MR when the heart is mild to moderately enlarged, the RH chambers are minimally dilated. As the LH chambers dilate during development of CHF, the septum moves rightward and the RH chambers become compressed. RH chamber size also increases. In some hearts with CHF, the RH septal border becomes convex, suggesting PH. Increased sternal contact is not a useful sign of right-sided dilatation in MR.

Footnotes

  1. Top of page
  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Footnotes
  8. Acknowledgments
  9. References

aPicker SX 300, Picker International Inc, Cleveland, OH, or GE Maxicamera 400A, General Electric Medical Systems, Milwaukee, WI

bTechnescan DPTA, Mallinckrodt Medical BB, Petten, Holland

cHermes, Hägersten, Sweden

dJMP v 5.01, SAS Inc, Cary, NC

Acknowledgments

  1. Top of page
  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Footnotes
  8. Acknowledgments
  9. References

Supported by Agria Insurance Company, Swedish Medical Research Council (project no. 3392), NorFA (Nordic Academy for Advanced Study), The Swedish Cultural Fund of Finland, and the Finnish Veterinary Research Foundation. The technical assistance of Mieth Berger and Christina Larsson is appreciated.

FPRNAs and the clinical and radiographic examination were made at the University Animal Hospitals, Uppsala, Sweden or Helsinki, Finland in 1997–2006. The measurements and statistics were made at the University Animal Hospital, Uppsala, Sweden in 2007–2009.

References

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  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Footnotes
  8. Acknowledgments
  9. References
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