Doppler flow evaluation can anticipate abnormal left lung perfusion after transcatheter closure of patent ductus arteriosus

Andressa M. Soaresa,*, Vera D. Aiellob, José L. Andradea, Luis J. Kajitac, José Soares, Jrd, Samira S. Morhya, Wilson Mathias, Jra, Antonio A. B. Lopese and José A.F. Ramiresf

a Laboratory of Echocardiography, Heart Institute (InCor), University of São Paulo Medical School, Brazil
b Laboratory of Pathology, Heart Institute (InCor), University of São Paulo Medical School, Brazil
c Hemodynamics and Interventional Cardiology Laboratory, Heart Institute (InCor), University of São Paulo Medical School, Brazil
d Department of Nuclear Medicine, Heart Institute (InCor), University of São Paulo Medical School, Brazil
e Department of Paediatric Cardiology, Heart Institute (InCor), University of São Paulo Medical School, Brazil
f Department of Cardiology and General Director of the Heart Institute, Heart Institute (InCor), University of São Paulo Medical School, Brazil

Received February 25, 2004; revised June 22, 2004; accepted July 8, 2004 * Corresponding author. Tel.: + 55 11 3069 5252; fax: + 55 11 3069 5279 (E-mail: amussisoares{at}terra.com.br).


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Limitations of the study
 Perspectives
 References
 
AIMS: Coil protrusion into the left pulmonary artery (LPA) has been described after transcatheter closure of the patent ductus arteriosus (PDA). The possible impact of such a finding in lung perfusion has not been completely clarified. We evaluated Doppler flow velocities and lung perfusion in patients submitted to that procedure.

METHODS: After transcatheter closure of PDA with coils, 70 patients (mean age 8.6±3.4 years) were followed for a period of 3.6±0.9 years (range 2.1–5.9) and compared to 22 controls. Peak flow velocities and coil protrusion were assessed by Doppler echocardiography. A Doppler velocity index (DVI) was calculated by the difference between the LPA and right pulmonary artery (RPA) peak flow velocities relative to the pulmonary trunk (PT) expressed in percentage, as follows: DVI=(LPA velocity–RPA velocity)/PT velocityx100. Lung scintigraphy was performed using 99mTc-labelled macro-aggregated albumin.

RESULTS: Device protrusion was observed in 94% of the patients, 10% of whom presented abnormal left lung perfusion. Peak LPA velocity and DVI were significantly greater in patients (p=0.001) and correlated negatively with left lung perfusion values (R2=0.21 and R2=0.65, respectively). A cut-off value of 50% for the DVI showed high sensitivity and specificity for reduced lung perfusion.

CONCLUSION: Impaired left lung perfusion may appear following transcatheter closure of PDA with coils and the determination of DVI may anticipate such alteration.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Limitations of the study
 Perspectives
 References
 
Transcatheter closure of patent ductus arteriosus (PDA) has been widely performed and its excellent immediate results are well-known,1 while long-term studies are relatively few and are mainly devoted to the description of prevalence of residual shunts.2 Mechanical distortions of the adjacent vessels, particularly the left pulmonary artery (LPA), have been described after the use of some types of prosthesis.3 Protrusion towards the lumen of the LPA has been reported after coil occlusion of PDA, but the potential consequences of flow distribution to the lungs have not been completely evaluated and the current literature demonstrates contradictory findings relating coil protrusion to flow disturbances.4,5

In order to evaluate the prevalence of coil protrusion to the LPA and its possible impact on the vessel diameters, flow disturbances and left lung perfusion, we studied prospectively, by echocardiography and radionuclide lung scintigraphy, a large group of patients submitted to transcatheter closure of PDA with coils.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Limitations of the study
 Perspectives
 References
 
Seventy patients (53 female, 17 male, mean age 8.6±3.4 years, range 2.2–17.3 years) submitted to transcatheter closure of PDA at the Heart Institute (InCor), University of São Paulo Medical School, were followed for a mean period of 3.6±0.9 years (range 2.1–5.9).

Ten (14.3%) patients presented other associated congenital cardiac defects. Four of them had been previously operated on (one ventricular septal defect, one atrial septal defect, two sub-aortic stenoses) and submitted at the same operation to PDA closure, but showed recanalization in the post-operative evolution and were considered for transcatheter closure. Five other patients had minimal ventricular septal defects, all showing a Qp:Qs<1.2:1. The remaining patient had mild pulmonary valve thickening, without stenosis (peak flow velocity in the pulmonary trunk=1.3 m/s).

Eight patients (11.4%) were diagnosed as having congenital rubella syndrome but none of them presented stenosis of the pulmonary arterial branches.

Control group
The control group consisted of 22 children and adolescents (11 female, 11 male, mean age 9.37±4.2 years, range 3.7–19), 15 were normal and seven had minimal cardiac lesions (five small ventricular septal defects and one secundum atrial septal defect, all of them presenting Qp:Qs⩽1.1:1, and one non-stenotic bicuspid aortic valve).

This study was approved by the Institution's Ethics and Research Committee and an informed consent was obtained before all procedures for patients and controls.

Coil occlusion procedure
Left lateral aortograms were used to define the ductal angiographic type, according to Krichenko et al.6 Coil occlusion of PDA was performed in a retrograde fashion, via the femoral artery, using the methods of coil selection and implantation described in previous reports.7 Implantation was attempted using the Gianturco coils (Cook Inc., Bloomington, IN, USA) in 62 patients (88.6%) or Cook detachable coils (William Cook Europe, Bjaeverskov, Denmark) in eight patients.

Echocardiographic examinations
Transthoracic echocardiographic studies were performed using HDI 5000 equipment (Philips Medical Systems, Bothell, WA). Images were stored on 0.5 in. VHS format and were available for off-line analysis.

Measurements of the PDA minimal diameter and length were obtained prior to the transcatheter closure from the high left parasternal view.

In the follow-up period, the prevalence of residual shunt was evaluated by colour and pulsed wave Doppler, as well as the position of the coils and the presence of protrusion into the lumen of the LPA from high left and short axis parasternal views. The diameters of both pulmonary arteries were measured from the suprasternal views, at end-systole, and indexed by body surface area as shown in Figs. 1 and 2.



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Fig. 1 Diagram (a) and corresponding echocardiographic plane (b) showing the site of measurement (white line) of the right pulmonary artery (RPA). AO: aorta; LA: left atrium; SVC: superior vena cava.

 
We also measured the peak flow velocities by pulsed wave Doppler at the pulmonary trunk (PT), immediately above the valve, from the parasternal short-axis view, at the LPA, bellow the coil protrusion and at the proximal segment of the right pulmonary artery (RPA) from the high parasternal short-axis view. A Doppler velocity index (DVI) was calculated by the difference between the left and right pulmonary arteries peak flow velocities in relation to the PT, expressed in percentage, as follows:
DVI=(LPA velocity–RPA velocity)/PT velocityx100.

All examinations were performed by the same investigator without knowledge of either the clinical data or the lung scintigraphy results.

Lung perfusion scintigraphy
Lung perfusion scans were performed using a peripheral intravenous injection of 100,000 to 150,000 particles (10 and 90 μm) of 99mTc-labelled macroaggregated albumin, at a dose of 0.03 mCi/kg. Two views were obtained in the anterior and posterior positions to evaluate the blood flow distribution between the lungs. The percentage of perfusion in both lungs was calculated by dividing the mean radioactivity obtained in both positions.

Predictors of decreased left lung perfusion
Several variables were examined in an attempt to predict which patients might be at increased risk for reduced left lung perfusion: age and weight during occlusion, other congenital cardiac defect or rubella syndrome associated, angiographic ductal type, PDA minimal diameter and length, amount and type of the coils, residual shunt, LPA diameter, coil protrusion into the LPA, peak LPA velocity and DVI.

Statistical analysis
Comparisons of means were performed by the paired or non-paired Student's t-test or the analysis of variance (ANOVA), according to the kind of data and number of tested groups. Correlation between continuous variables was evaluated by the Pearson product–moment correlation coefficient. The ROC curve was used to select an optimal decision regarding the cut-off value of the DVI to predict abnormal lung perfusion. Results are expressed as means±standard deviation and range p-value was set at 0.05 to achieve statistical significance.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Limitations of the study
 Perspectives
 References
 
In 47 patients (67.1%), the PDA was diagnosed by angiography as type A, in 4 (5.7%) type B, in 3 (4.3%) type C, in 8 (11.4%) type D, and 8 (11.4%) type E. In most procedures (65.7%) only one coil was implanted. Two coils were implanted in 31.4% and three coils in 2.9% of the cases. The most common type of device was the Gianturco coil in 62 patients (88.6%).

The mean PDA minimal diameter obtained by echocardiography was 2.9±0.75 mm (range, 1.2–5.0 mm) and by angiography 2.1±0.8 mm (range, 0.7–4.1 mm). The mean lengths were, respectively, 7.9±2.7 mm (range, 4–16 mm), and 8.3±3.2 mm (range, 2.6–17.2 mm). The prevalence of residual shunt at the latest follow-up evaluation was 8.6%.

During the PDA occlusion procedure, coil embolization to the pulmonary artery was observed in three patients (2.1%), all of them being successfully retrieved. No embolic episode was noticed at the aorta.

Coil protrusion and pulmonary flow velocities
Sixty-six patients (94.3%) showed protrusion of the device. While the LPA mean peak velocity was significantly higher than in the RPA and the pulmonary trunk (p=0.001), there were no differences between the regional mean peak flow velocities in the control group (p=0.68, Fig. 3). Additionally, the peak LPA velocities and DVI were significantly greater in patients compared to controls (p=0.001) (DVI: 21.6±25.8% versus 1.7±7.3%).



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Fig. 3 Box plot of flow velocities (m/s) at the pulmonary arteries in patients and controls. LPA, left pulmonary artery; PT, pulmonary trunk and RPA, right pulmonary artery.

 
Radionuclide lung scintigraphy
There was a significant difference between right and left lung perfusion in both controls (53.2±2.4% versus 46.8±2.4%; 95% CI: 41.6–52.0%) and patients (54.4±2.9% versus 45.6±2.9%), respectively (p=0.001).

Correlation between left lung perfusion and LPA velocity and DVI
The mean time interval between the lung scintigraphy and the late echocardiographic study was 81±73.4 days (0–287). Seven patients with abnormal left lung perfusion (mean 39±2.6%) presented mean LPA velocity and DVI greater than those with normal left lung perfusion (mean LPA velocity=1.59±0.33 m/s versus 1.09±0.26 m/s; mean DVI=55.5±32.96% versus 12.3±11.9%) (Table 1). Maximal LPA velocity and DVI showed significant negative correlations with left lung perfusion (p=0.001). However, the coefficient was stronger for the DVI (R2= 0.65) than for maximal LPA velocity (R2= 0.21) (Fig. 4). A regression equation was determined as follows: Left lung perfusion (%)=47.797–0.0923xDVI.


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Table 1. Individual values of peak LPA velocity and DVI in the seven patients with abnormal left lung perfusion
 


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Fig. 4 Scatter diagram of left lung perfusion (%) and DVI (%) for patients (circles) and controls (triangles). The regression line for patients is also shown (R2=0.65).

 
Diameter of the pulmonary arteries
The mean LPA diameters were significantly smaller when compared to the RPA diameters in patients. Moreover, LPA diameters were significantly smaller in patients with DVI⩾50% when compared to patients with DVI<50% and to the control group (Table 2).


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Table 2. Mean right and left diameters of the pulmonary arteries in the control group and in the patients with DVI<50% and ≥50%
 
DVI as a predictor of abnormal left lung perfusion
Among all variables examined, DVI was the only one to show an excellent association with decreased left lung perfusion (p=0.001). A cut-off value of 50% for the DVI was determined, with 100% sensitivity and 98% specificity for the left lung perfusion deficits. From 8 patients (11.4%) that showed DVI⩾50% (Table 3), 7 had decreased left lung perfusion. Two coils had been deployed in four of such patients and one coil in the remaining four. Only one of them had undergone previous surgical closure of the PDA. Fig. 5 illustrates a patient with increased DVI and reduced left lung perfusion.


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Table 3. Distribution of patients according to the DVI and left lung perfusion
 


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Fig. 5 Echocardiographic parasternal short axis view showing a protruding coil (arrow) into the left pulmonary artery (LPA) (A), with the corresponding colour flow mapping acceleration (B); Pulsed Doppler study showing normal pulmonary trunk flow velocity (C), and increased LPA flow velocity (D); and lung perfusion scintigraphy showing reduced blood flow distribution in the left lung, seen from the anterior (E) and posterior (F) positions. RPA=right pulmonary artery.

 

    Discussion
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Limitations of the study
 Perspectives
 References
 
The immediate and medium-term results of the transcatheter closure of PDA show unquestionable efficacy and safety. On the other hand, the long-term consequences of lung perfusion disturbances are still unknown.

The use of Gianturco coils to occlude the ductus is largely employed in developing countries, due to their low cost, easy manipulation and, above all, efficacy and safety. In the present series, Gianturco coils were used more frequently than Cook coils. The main difference between these two devices is the possibility of release control in the Cook model. Moreover, during the procedure implantation, some degree of protrusion into the pulmonary artery is normal, because in order to anchor the device, the first half of the first loop of the coil is positioned inside the pulmonary artery. This can be minimized by the mechanism of retrievability of the Cook coils. Consequently, Gianturco coils present higher rates of protrusion to the LPA when compared to other coils. While Stromberg et al.,8 described a 90% prevalence of Gianturco coil protrusion in a series of 31 patients, in the present study it was even higher (94.7%).

An alternative explanation for the high protrusion rate would be the greater thrombogenicity of Gianturco coils because of the presence of Dacron wool fibres. Cheung et al.,9 comparing different types of coils, found that the reduction of residual shunt with time tended to be greater when Gianturco coils were used.

When we studied the mean peak velocity in the LPA, we found a higher value than that observed in the RPA and in the PT (p=0.01). However, before trying to correlate such values to lung perfusion results, we tried to avoid possible sources of error, by establishing the DVI, which takes into account not only the LPA velocity, but also the velocities obtained in the pulmonary trunk and in the RPA. We believe that it is difficult to ascertain whether the absolute value of the velocity is normal or not in a specific segment of the pulmonary tree, as it may be influenced by factors such as the heart rate, ventricular function, volemia, etc. Therefore, the use of the proposed DVI may overcome these problems. Moreover, the evaluation of flow velocities in both right and left pulmonary arteries depends on the adequate alignment of the Doppler cursor with the long axis of the vessel, therefore compromising the calculation of the DVI. However, identical procedures were carried out for the control group, which showed a DVI close to zero.

Dessy et al.4 evaluated 49 patients submitted to transcatheter closure of PDA with the Rashkind prosthesis and detected device protrusion into the LPA in 10% of the cases. They also found a strong correlation between device protrusion and increased peak velocity, but a weak correlation with decreased lung perfusion values (they arbitrarily chose the value <40% as abnormal). Sreeram et al.,5 also studied lung perfusion after the utilization of Cook detachable coils. In their series of 35 patients, 40% showed device protrusion into the LPA, with a significant correlation with mean peak velocity evaluated by Doppler. Although patients with coil protrusion showed a tendency to have lower values of lung perfusion, no significant difference could be detected when compared to the ones without protrusion. Additionally, no significant association was detected between low lung perfusion values and number of coils used or increased flow velocity in the LPA.

The lack of association in their study could be explained by the fact that they considered flow velocity absolute values. Several findings of their study may be pointed out as different from the present investigation: the type of coil, a smaller prevalence of protrusion and lower incidence of decreased lung perfusion. We speculate that radionuclide lung scintigraphy being performed in the early post-procedural period could have minimized the perfusional alterations that could appear along the time. In this context, Hijazi et al.,10 demonstrated a decrease of 7% in left lung perfusion values based on scintigraphies performed immediately and 13 months after transcatheter closure of PDA.

Differently from Dessy et al.,3 who considered Doppler as a non-reliable method to evaluate possible alterations of lung perfusion, the proposed DVI was an excellent predictor of perfusional abnormalities. Based on the determination of normal values for lung perfusion, we verified that from eight patients presenting DVI⩾50%, seven had reduced left lung perfusion. Although we could also detect a negative correlation between peak LPA flow velocity and left lung perfusion, the coefficient was much lower than that obtained with the DVI. Furthermore, some apparently normal values of LPA velocities showed abnormal DVI (Table 1), which reinforces the concept of taking into account not only the LPA velocity but also the velocities in the pulmonary trunk and in the RPA.

The diameters of the pulmonary arteries should also be pointed out. This is a subject of some concern, as it has been argued that the closure procedure could impair the normal growth of such vessels. Our results depicted a difference between the right and left pulmonary artery diameters in patients, and even lower values for the left artery in the group showing an elevated DVI. These findings are in accordance with the hypothesis that the procedure can affect growth. However, we cannot completely rule out the possibility of it being related to a congenital abnormality or even if it is present due to an open-chest PDA closure.


    Limitations of the study
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Limitations of the study
 Perspectives
 References
 
Some limitations of this study must be considered. The comparison of flow velocities in the pulmonary arteries could not be performed between the pre and post-procedural periods, since before the PDA closure the pulmonary flow pattern was already abnormal. Finally, and perhaps the major limitation of our study, was that we could not quantify the degree of coil protrusion into the LPA. We only detected qualitatively the presence or absence of protrusion. We do not rule out the possibility that if we had devised a way to quantify the protrusion, we could have achieved a better correlation with abnormal values of pulmonary velocity and perfusion.


    Perspectives
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Limitations of the study
 Perspectives
 References
 
In our opinion, it would be of great clinical relevance to perform similar echocardiographic and scintigraphic evaluations in patients submitted to surgical closure of a PDA or to the implantation of other types of device, in order to clarify the nature and importance of our findings. It may be that not only the presence of the prosthesis, but mainly retraction and fibrosis occurring after closure, and also some extension of ductal tissue into the LPA, lead to abnormalities in local flow velocities. Troise and Arciprete11 suggested recently that ductal "invasion" into the LPA is determined by the amount of ductal tissue present in each case. Maroto et al.,12 speculated that ductal closure could be the aetiology of a transitory stenosis of the LPA. Guntheroth13 compared premature infants with PDA to those with spontaneously closed ductus, showing significantly higher LPA flow velocity values in the second group.

The utilization of the DVI may also be devised for other clinical situations where the presence of pulmonary arterial stenosis may be technically difficult to be confirmed, such as in the post-operative evaluation of the central pulmonary arteries in Fallot's tetralogy, Rastelli operation and arterial switch operation.14

Finally, the real long-term clinical relevance of left lung perfusion values lower than 39% detected in this study needs clarification which we believe may appear in the follow-up course of the affected patients.



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Fig. 2 Diagram (a) and corresponding echocardiographic plane (b) showing a protruding coil and the site of measurement (white line) of the left pulmonary artery (LPA). AO: aorta.

 

    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Limitations of the study
 Perspectives
 References
 
  1. Magee AG, Huggon ID, Seed PT, et al. Transcatheter coil occlusion of the arterial duct: results of the European Registry Eur Heart J 2001;22:1817-1821.[Abstract/Free Full Text]
  2. Patel HT, Cao QL, Rhodes J, et al. Long-term outcome of transcatheter coil closure of small to large patent ductus arteriosus Cathet Cardiovasc Intervent 1999;47:457-461.[Medline]
  3. Nykanen DG, Hayes AM, Benson LN, et al. Transcatheter patent ductus arteriosus occlusion: application in the small child J Am Coll Cardiol 1994;23:1666-1670.[Medline]
  4. Dessy H, Hermus JP, Van den HF, et al. Echocardiographic and radionuclide pulmonary blood flow patterns after transcatheter closure of patent ductus arteriosus Circulation 1996;94:126-129.[Abstract/Free Full Text]
  5. Sreeram N, Tofeig M, Walsh KP, et al. Lung perfusion studies after detachable coil occlusion of persistent arterial duct Heart 1999;81:642-645.[Abstract/Free Full Text]
  6. Krichenko A, Benson LN, Burrows P, et al. Angiographic classification of the isolated persistently patent ductus arteriosus and implications for percutaneous catheter occlusion Am J Cardiol 1989;63:877-880.[Medline]
  7. Lloyd TR, Fedderly R, Mendelsohn AM, et al. Transcatheter occlusion of patent ductus arteriosus with Gianturco coils Circulation 1993;88:1412-1420.[Abstract]
  8. Stromberg D, Pignatelli R, Rosenthal GL, et al. Does ductal occlusion with the Gianturco coil cause left pulmonary artery and/or descending aorta obstruction Am J Cardiol 1999;83:1229-1235.[CrossRef][Medline]
  9. Cheung Y, Leung MP, Chau K. Transcatheter closure of persistent arterial ducts with different types of coils Am Heart J 2001;141:87-91.[CrossRef][Medline]
  10. Hijazi ZM, Geggel RL. Transcatheter closure of large patent ductus arteriosus (≥4 mm) with multiple Gianturco coils: immediate and mid-term results Heart 1996;76:536-540.[Abstract]
  11. Troise D, Arciprete P. Anomalous extension of ductal tissue within the pulmonary artery Cardiol Young 2001;11:364-365.[Medline]
  12. Maroto E, Fouron JC, Van Doesburg NH, et al. Closure of the ductus arteriosus: determinant factor in the appearance of transient peripheral pulmonary stenosis of the neonate J Pediatr 1991;119:955-959.[Medline]
  13. Guntheroth WG. The role of ductal constriction in transient stenosis of the left pulmonary artery Pediatr Cardiol 1998;19:240-242.[CrossRef][Medline]
  14. Casaldaliga J, Girona JM, Sanchez C, et al. Doppler echocardiography in the postoperative assessment of the arterial switch in the repair of transposition of the great arteries and double outlet right ventricle Rev Esp Cardiol 1996;49:117-123.[Medline]




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