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Ann Thorac Surg 2003;75:1232-1237
© 2003 The Society of Thoracic Surgeons


Original article: cardiovascular

Off-pump technique for the treatment of ventricular myocardial echinococcosis

Cemal Levent Birincioglu, MDa*, Onurcan Tarcan, MDa, Hasmet Bardakci, MDa, Ahmet Saritas, MDa, Oguz Tasdemir, MDa

a Department of Cardiovascular Surgery, Türkiye Yüksek Ihtisas Hospital, Ankara, Turkey

Accepted for publication October 24, 2002.

* Address reprint requests to Dr Birincioglu, Cardiovascular Surgery Clinic, Türkiye Yüksek Ihtisas Hospital, 06100 Sihhiye, Ankara, Turkey
e-mail: b_levent{at}hotmail.com


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
BACKGROUND: This study was planned to investigate the off-pump operability of ventricular myocardial Echinococcosis, which has no close relation with the cardiac chambers.

METHODS: Twenty patients with cardiac echinococcosis, and 2 patients with isolated pericardial echinococcosis were operated on. Hydatid cysts were located in the ventricular wall in 17 patients and 10 of these 17 patients were operated without cardiopulmonary bypass. We present these 10 patients in this report. We used transesophageal echocardiography (TEE) and peroperative surface echocardiography (PSE) to determine the relation of cysts with cardiac chambers. The cysts were aspirated for diagnosis and to facilitate the dissection. Cyst cavities were left open in all cases.

RESULTS: We did not observe any early complication and in long-term follow-up only one patient underwent reoperation 68 months after her first operation due to reoccurrence.

CONCLUSIONS: Ventricular myocardial echinococcosis without relation with the cardiac chambers can be operated without using cardiopulmonary bypass with the aid of TEE, PSE, and controlled cyst fluid aspiration.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Cardiac echinococcosis is a very rare but a serious life threatening disease that can be seen worldwide [1, 2]. As there is a rich clinical diversity of cardiac echinococcosis, surgical treatment options are changing according to their localization and complications [3]. However, the treatment of these cysts may be standardized. During early years of our experience cysts used to be removed with their surrounding myocardium and the residual defects were repaired primarily or with a patch insertion. But, in the course of time, we operated these patients without cardiopulmonary bypass (CPB) and left the cavity open for healing secondarily. In this report we will discuss these patients.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
From 1972 to June 2002, 22 patients underwent surgery for cardiac or pericardial echinococcosis. In 17 patients cysts located in the ventricular wall, and the last 10 patients were operated off-pump. These 10 patients will be presented in this article. Demographics and cyst localizations of these patients are illustrated in Tables 1 and 2 respectively. Patient 8 had bilateral lung and spleen cysts, besides ventricular cysts. Three months before the heart operation, he had undergone resection of these cysts in two sequential operations. We prescribed benzymidazol derivatives to all patients both preoperatively and postoperatively.


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Table 1. Presentation of Patients Undergoing Operation With Off-Pump Technique

 

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Table 2. Description of Localization of Cysts

 
Operative technique
All patients were operated on under general anesthesia. During operation the cyst localizations, their relation to the cardiac chambers, and the blood flow within the cysts were evaluated with transesophageal echocardiography (TEE) or peroperative surface echocardiography (PSE). The types of the cysts are illustrated in Figure 1.



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Fig 1. Modes of myocardial echinococcosis: A = scolexes forming cysts; B = growing cyst towards the pericardial cavity; C = growing cyst towards the ventricular cavity; D = cyst is not protruding either towards ventricular nor pericardial cavity; E = rupture of cyst into the pericardial cavity; F = rupture of cyst into ventricular cavity; G = degenerated cyst.

 
In our patients the off-pump technique was used for type B, D, E, and G (Fig 1). The affected area was encircled with polyvinylpyrolidone iodine embedded gauzes. After checking with a diagnostic aspiration to identify if there is any communication between cyst cavities and cardiac chambers, polyvinylpyrolidone iodine solution was injected into cysts to inactivate the scolexes. The fluid content of the cysts was than aspirated and the cavity was carefully opened. Multiple daughter cysts were removed. Daughter cysts were best mobilized with a tablespoon. The area was than irrigated. We excised the epicardium covering the cyst cavity and leave the cavity open.


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
In 7 patients there were type B cysts and in another 2 patients cysts were degenerated (Type G). In these cases cysts were localized subendocardially and were protruding towards the pericardium (Table 2). In 5 patients (Patients 2, 4, 6, 9, and 10) cysts were compressing and deforming the left ventricular cavity (Fig 2), although there were thick muscle bands separating the cyst and the ventricular cavity. We have observed that following the cyst evacuation, bordering muscle tissue became thicker, more rigid and underwent fibrotic changes. Almost in all cases there were pericardial adhesions but in Patient 1 there were also daughter cysts neighboring the right atrium, and this suggested that the cyst was ruptured spontaneously into the pericardial cavity before the operation. She received albendazol for 5 years postoperatively, but this did not prevent the development of two cysts between the left atrium and right superior pulmonary vein, compressing the left atrium. This patient was reoperated on with off-pump technique at postoperative month 68. In another patient a 3x4 cm cyst at anterolateral location was not protruding towards either pericardial or ventricular cavity (Type D).



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Fig 2. Transesophageal echocardiographic view of patient 6, type B cyst localized at anterior wall of right ventricle, interventricular septum and anterolateral wall of left ventricle. Cavity of left ventricle and right ventricle were deformed. (AO = aorta; CYST = cyst; LA = left atrium; LV = left ventricle; RV = right ventricle.)

 
In our series we did not experience any morbidity or mortality at early postoperative period. All patients received benzymidazole derivatives before and after the operation. Each patient was followed-up at postoperative second and sixth months, and after that annually (Table 1). We did not come upon relapses except in Patient 1. At early postoperative period transthoracic echocardiography revealed empty spaces at the places of resected cysts (Fig 3), but after postoperative second month, this disappeared. We did not encounter any aneurysmal changes.



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Fig 3. After removal of the large cystic mass, left and right ventricular deformation recovered. Open cyst cavity can be seen. (AO = aorta; LA = left atrium; LV = left ventricle; RA = right atrium; RV = right ventricle.)

 
At the moment, 9 patients are at New York Heart Association (NYHA) class I and 1 patient is at NYHA class II.


    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Cardiac echinococcosis is a rare disease, which may involve almost any part of the heart, most often located in ventricular myocardium. In our series 17 of 22 patients (77%) had ventricular wall cysts. Treatment differs depending on the location and the complications. Most of the cysts, which are in the ventricular myocardium, can be resected without cardiopulmonary bypass (CPB). Five patients, which were not located in ventricular myocardium, and 7 patients, which were operated on under CPB although they were in the ventricular myocardium, have been reported previously [3]. One of these 7 patients was operated on under CPB but without cross clamping while the heart was beating. In an additional 2 patients, cysts were removed without CPB, but since at that time we did not know much about the off-pump technique, we did not report details in that article [3]. These 2 patients, and the following 8 patients who were operated on with off-pump technique, are presented in this paper.

We did not compare the patients who were operated under CPB with those who were operated off-pump because the patients were spread over a wide period of time (20 years), in the past there was not a standard method, surgical teams changed in time, old patients have more multiorgan involvement, recent cases are followed closely with benzymidazole derivatives, and social and economic status of the patients improved strikingly.

In determining the technique of operation anatomic positions of the cysts are very important. From Table 2 it is apparent that in some patients preoperative diagnoses are different from operational findings. Final diagnoses are given under "intraoperative finding" section. Two-dimentional echocardiography, computed tomography, and magnetic resonance imaging are essential for diagnosis in most patients, but image of the cyst may cause misinterpretation. For this reason, intraoperative TEE and PSE are very helpful. Because discussion related with the methods of diagnosis was done in detail in previous reports [3, 15], in this report we did not focus on tools of diagnosis, but tried to figure out a standard technique of surgical treatment.

Types of ventricular cysts
When scolexes reach the myocardium they start cyst formation. At that phase cysts are very small and cannot be seen by any means (Fig 1[A]). In the course of time, the cysts grow and are pushed towards a weaker side of wall: either epicardium (Fig 1[B]) or endocardium (Fig 1[C]). Meanwhile, the host’s fibrosis response starts, and a pericystic fibrous capsule is formed. Sometimes cysts do not protrude towards any direction and become stagnant (Fig 1[D]). If the cysts remain inactive within the myocardium, they may lose their fluidity and degenerate in time (Fig 1[G]). Degenerated cysts may mimic tumors on echocardiography. Subendocardial cysts protruding towards ventricular cavity may rupture under sheer stress (Fig 1[F]). This may cause anaphylactic reaction and sudden death [4, 5] or peripheral emboli [514]. If the patient survives this incident and if he does not have another cardiac cyst, the cardiac problem would be solved. For that reason, we rarely see cysts protruding to the cardiac cavities except atrial chambers, which have low chamber pressure. In this condition, the cyst is covered with fibrin and may mimic atrial myxoma [3].

Frequently, cysts grow towards the epicardium and dissect that layer from myocardium and protrude towards the pericardial cavity. In some cases pericardium adheres to the epicardium over the cyst (Fig 1[B]). Sometimes these type B cysts grow towards both pericardial and intraventricular cavities (Fig 2). This is not a true protrusion towards intraventricular cavity, but rather a deformation of it. This may be misjudged as subendocardial cysts that show intracavitary protrusion. In type B case there is a strong muscle layer between the cyst wall and the ventricular cavity. Cysts growing toward the epicardium may involve an important part of the ventricle. Besides dissecting the epicardium from myocardium, a cyst may compress the small coronary arteries and disturb the flow. In addition to this, it changes the compliance at that area, and patient may suffer angina. This may cause misdiagnosis as coronary artery disease [3]. In some patients cysts may rupture into the pericardial cavity (Fig 1[E]) and create pericardial cysts.

Septal cysts are rarely isolated. These are mostly extended part of cysts, which are localized at the apex, anterolateral left ventricle, or right ventricle (Fig 2). That type of cysts bulging towards the pericardium can be resected off-pump. However, isolated septal cysts preferably be resected under CPB while the heart is arrested, because it is not easy to approach them. These cysts may obstruct the outflow tract of right or left ventricle.

Planning and management of the operation
Plan of the operation is reevaluated following pericardial incision. TEE and PSE are used during this reevaluation. In order to decide the technique of resection, the description of the anatomic features of the cyst must be made in detail.

In practice it is not possible to diagnose type A cysts. These cysts grow in time and cause recurrences, years after the operation. In one of our patients, even though albendazol had been prescribed for 5 years, we observed a reoccurrence 68 months after the operation.

Type C cysts, which protrude towards the intraventricular cavity, are seen as bulging masses on echocardiography. In between the cyst wall and the ventricular cavity, there is only endocardium or a thin layer of myocardium. We did not observe such a cyst among the presented cases. These cysts are under sheer stress and they carry a high risk of rupture. They should be resected after the aorta is clamped under CPB. Kaplan and coworkers [14] stated that if such a cyst is located in right ventricle, the pulmonary artery should also be clamped. Type C cysts can be resected through ventriculotomy, atriotomy, or aortatomy according to their location and relations [14].

Cysts protruding towards the pericardial cavity (Fig 1[B, E, and G]) are seen more than other types; and those are good candidates for off-pump surgery. Subepicardial cysts, despite how extensive they are, can be resected without CPB, provided that there is no connection with ventricular cavity. Because they push the heart to one side as they expand, they can readily be exposed. Generally there are dense pericardial adhesions around cyst. These adhesions are dissected. For the cysts, which are located at the inferior wall of the left ventricle, traction sutures placed at the acute margin of the heart will be very helpful in exposure. Cysts located posterolaterally, can be reached through the left pleura. In one of our patients (Patient 6) hydatid cyst was located posterolaterally, and there were dense pericardial adhesions and calcifications complicating the dissection. We cut up the left pleura and reach the bulging of the cyst in the pleural cavity.

Cysts, which do not protrude towards any direction (Fig 1[D]), are not easy to approach. Even though the localization is identified by PSE, the surgeon may not dissect the cyst from the surrounding epicardium and myocardium. In such patients examination of the area through an injector may help to guide the dissection towards where the cyst fluid comes. This prevents accidental tear of ventricular cavity. In one of our patients (Patient 8) the hydatid cyst was located very close to the left anterior descending coronary artery, and this was complicating the dissection. In this patient puncture with an injector helped much in guiding the dissection.

Aspiration of the ventricular cyst content is a maneuver facilitating the surgical dissection. If there is difficulty for echocardiographic diagnosis (some cysts mimic tumors with echocardiography), needle aspiration may provide clues [15]. In this setting, if blood is aspirated, there is communication of cyst cavity with cardiac chambers and the operation should be performed under CPB. Dissection of the distended cysts without aspiration may cause leakage and contamination the surroundings. Distension may be reduced with aspiration and this will facilitate the manipulation. This strategy will also provide more safety since most operations are performed with off-pump technique, especially if the cysts are localized laterally or inferiorly. Length of the operation and the duration of ventricular uplift will be shorter.

We prefer to open the cyst cavities and remove them all with their extensions. We believe that all pouches should be left open, regardless of how deep they are. The host’s dense fibrous defense response forms a barrier to rupture of cyst into ventricular cavity on beating heart. In time these pouches will be closed with secondary healing. In our series we removed large cystic masses and left the pouches open and did not observe any complications. Removal of cysts increases myocardial compliance and myocardial perfusion. Healing accelerates in this way. Cardiac deformation recovers and myocardial contraction arises. Formation of an aneurysm is not expected, in the presence of contracting healthy myocardium. There are three reasons to leave the cavities open. First, plication of large cavities immobilizes large areas of myocardium and this causes myocardial dysfunction. Second, sutures may cut the myocardial edematous tissue while contracting and causes intrapericardial bleeding. Those types of patients were reported on previously [3]. Third, remaining type A cysts, if any, will be squeezed towards cardiac chambers while growing. Rupture of these to cardiac chamber may cause anaphylactic reaction. It was reported before that some cysts develop after the operation and rupture [16]. If we cover and close the cavity with a graft, we will produce an enclosed space prone to abscess formation. It is not practical to fill a large pouch with biological glue, because this impedes the contraction of neighboring myocardium. Filling the cavity with another material is not meaningful, because in that way a mass would be replaced with another.

Standby cardiopulmonary bypass facility
During off-pump surgery, we did not use standby CPB. Cardiac cyst cases may require CPB in three circumstances: cardiovascular collapse and shock due to rupture of the cyst into the ventricular cavity during manipulations; hemodynamic instability during dissection of the cysts located at the posterior or inferior walls; or accidental tear of ventricular cavity. This risk is low if we detect the contents of the cyst with TEE or PSE, if puncture reveals no relation with blood, if cyst is group B, and if we incise the dome of the bulging and carefully evacuate the daughter cysts. We did not sever the ventricular cavity in any patient. But if bleeding occurs we think that it can be sutured easily. If hemodynamic instability occurs, we stop pulling the heart. After achieving the stability again, we go on. If we could not achieve the hemodynamic stability, we would set up CPB.

Off-pump technique
In 1963, it was reported that epicardial cysts could be removed without CPB [17]. However, most surgeons agree that surgical resection of cardiac hydatid cyst should be done under CPB because of acceptable operative risk and cure [14, 18]. Sporadic cases were reported before indicating that surgical removal of cyst is possible while the heart is beating under CPB [3, 19]. Development of echocardiographic imaging technique, and regular daily use of TEE and PSE lead to better intraoperative systematic analysis of cardiac cysts. Thus, with off-pump technique, it is possible to remove most of the ventricular cysts, with satisfactory results.

During off-pump surgery, myocardial contractions help to expel the daughter cyst once the overlying myocardium has been dissected. It is especially useful when the cyst is located close to coronary arteries.

During CPB, if we accidentally enter intraventricular cavity, cystic embolization may occur into ventricular cavity because of low intraventricular blood pressure. Moreover, we cannot wash the intraventricular cavity with scolicidal agents.

Benzymidazole derivatives in treatment
Mebendazole and albendazole are broad-spectrum antihelmintics. Larva forms are very sensitive to these drugs. But affectivity on cyst forms is limited. Albendazole is more effective than mebendazole and has become an adjunct to surgery in recent years. The dose of albendazole is 15 mg/kg per day; it is taken in two divided doses after meals for 4 weeks. We give a 2-week rest and then start another 4-week course. Optimal cyst eradication can be achieved with one preoperative and three postoperative courses. The aim of preoperative albendazole is to decrease the number of living parasites before the surgery. In practical it is not possible to inactivate all the parasites with albendazole. We increase the number of postoperative albendazole cures if, preoperative cure was short, living parasites were encountered at the operation, and if cysts were extensive. Some patients take albendazole up to fifth postoperative year. The other criteria to determine the duration of postoperative albendazole treatment are; the titer of echinococcus hemaglutination test and the level of antiechinococcus IgM. Albendazole treatment should continue until these measurements come to normal.

Prevention of the contamination during surgery
It is not always easy to extirpate a huge and distended cyst without rupturing, whether the heart is beating or arrested. Cysts may be perforated accidentally or pierced on purpose, and cyst fluid containing scolexes may spread and contaminate the surrounding tissues. In order to prevent this patient should receive albendazole before the operation, polyvinylpyrolidone iodine should be injected into the cyst cavity as scolicidal agent, cysts should be packed with gauze immersed in polyvinylpyrolidone iodine, mediastinum, and the other exposed tissues should be washed with diluted polyvinylpyrolidone iodine solution. After extirpation of the cyst, curettage of the trabecular pouches and resection of edges of the cavity may eradicate the daughter cysts. Beating myocardium facilitates the abortion of daughter cysts from trabecular pouches. Scolexes are very sensitive to albendazole and chemical detergents, thus they can be easily eradicated. Otherwise we would face with recurrences in each case. But cysts may resist. When scolexes form cysts, they may gain resistance to detergents and drugs. We think that reoccurrences are mostly due to residual daughter cysts or type A cysts.

Involvement of other organs
We have observed that in recent times involvement of other organs is infrequent. Of 14 patients, we have reported previously that 7 patients (50%) had other organ involvement [3]. Whereas 10 patients are reported in this article, only 1 patient (10%) had other organ involvement. In the remaining 9 patients we scanned whole body with computed tomography and ultrasonography, but could not detect any cysts in other organs. This can be explained in two hypothesis: (1) in recent times diagnostic devices such as ultrasonography, computed tomography, and magnetic resonance are used widely and this helps early detection and treatment of cysts before they disseminate; (2) airborne infection is also possible. Social and economic status of the population raised strikingly, and this improved the food hygiene. This decreases the chance of eggs reaching the intestines, but they may reach the alveoli. In airborne infection, contamination concentration is low. One or two scolexes may pierce the alveolo-capillary membrane through the pulmonary veins reach the systemic circulation.

In the presence of other organ involvement, the main treatment is removing cardiac cysts. Treatments of the other organ cysts are planned with related consultants. In patient 8, bilateral lung, splenic and ventricular cysts were determined with computed tomography, ultrasonography, and echocardiography. The type D myocardial cyst was localized at anterolateral wall of left ventricle and did not protrude towards any direction. Albendazole treatment was begun. Right lung cysts were removed through right toracotomy. Fifteen days after this operation, through left thoracotomy, left lung cysts were removed and splenectomy was performed, dissecting the diaphragm. Three months later the myocardial cyst was removed with off-pump technique.

In conclusion, most of the cardiac hydatid cysts are localized in the ventricular myocardium. And most of the ventricular cysts can be resected without CPB. The most critical point during this procedure is to identify the position of the cysts with TEE and PSE.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. Mattosian R.M., Richard M.D., Smith S.D. Hydatosis. A global problem of increasing importance. Bull World Health Org 1997;55:499-507.
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