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MMCTS (August 10, 2006). doi:10.1510/mmcts.2005.001115
Copyright © 2006 European Association for Cardio-thoracic Surgery

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Procedure


Heart echinococcosis: current problems and surgical treatment

Yury L. Shevchenko, Nikolay O. Travin*, Gaziyav H. Musaev and Alexander V. Morozov

Pirogov National Medical Surgical Center, Research Center of Thoracic Surgery, Moscow, Russia

* Corresponding author: * ul. Suzdalskaya 6-1-19, 111673 Moscow, Russia Tel.: +7-095-700 6647; Fax: +7-916-686 2524 E-mail: dr.travin{at}mail.ru


   Summary
Top
 Summary
Introduction
 Surgical technique
 Results
 Discussion
 Conclusion
 References
 
We present some historical, epidemiological, statistical data for heart echinococcosis and concomitant lesions of different organs. The diagnosis of heart echinococcosis is based on revealing of the cyst and its identification with echinococcus. The value of different diagnostic methods is shown. A surgical procedure in patients with heart echinococcosis depends on the localization of the cysts (manipulations under cardiopulmonary bypass or off-pump procedure). We present some additional techniques for prophylaxis of recurrence.

Key Words: Heart • Echinococcosis • Diagnostics • Surgical treatment


   Introduction
Top
 Summary
 Introduction
Surgical technique
 Results
 Discussion
 Conclusion
 References
 
According to WHO data, from 50 million people dying annually all around the world, 16 million die from infectious and parasitic diseases. By World Bank estimations, economic losses from them ranks in fourth position after other diseases and trauma.

History
It is known that echinococcosis was firstly described by Hippocrates and Galen. In the 17th century Redi realised that echinococcus is transmitted from animals to humans and Malpighius determined it as the living organism. Later, Rudolphy defined the book name ‘taenia echinococcosis’ and Bremser revealed a cystic form of echinococcosis in humans. Heart echinococcosis was described for the first time by May in 1639. First in-life diagnosis of heart echinococcosis belongs to Kashin (1862). The first successful operation on heart echinococcosis was performed by Marten and De Crespign in 1921 and the first manipulation under CPB, by Artucio (1962)1.

Epidemiology
Most common kinds of disorder in clinical practice are alveococcosis caused by Echinococcus multilocularis and echinococcosis caused by Echinococcus granulosus. Alveococcosis is a human disease characterized by an infiltrative growth comparable with cancer and more recently formed cysts. Echinococcosis is a human and animal disease that always has a cyst stage.

Echinococcosis has been registered everywhere except Antarctica. Maximum morbidity is common in regions where median temperatures vary from 10 to 20°C, but in countries with warmer or colder climates morbidity is lower and it tends to be prevalent in lung cyst forms2.

Echinococcus granulosus Rudolphi is an endoparasitic helminth. In eugamic stage it lives in the bowels of flesh-eating animals (dog, wolf, jackal etc.) while in slug stage it lives in organs and tissues of heavy and small cattle and in humans. One animal can excrete up to 20 000 helminthes and each of them contains from 500 to 1000 oncospheres. Segments of echinococcus move 20–30 cm per hour and after disruption excrete 400–800 oncospheres. At temperatures between 5 and 20°C oncospheres remain alive for 4–6 months. Furthermore, they are resistant to routine disinfectant agents. From one to twenty oncospheres is enough to contaminate the human. The average duration of the life of echinococcus cysts in humans is 10–20 years (up to 40 years) and their sizes vary from 20 to 300 mm. Cyst growth rate is up to 50 mm per year.

An echinococcus cyst consists of a chitin cover and embryonic elements inside that develop from the cuticular membrane of a cyst (protoscolexes and acephalocysts). In addition, new data show that acephalocysts may form from protoscolex pedicles. Protoscolexes die in the first minutes after extraction even without influence of external factors. Contrary to protoscolexes acephalocysts are stable to outer factors, and permeation action of germicides and they may cause the recurrence of the disease after surgical intervention. All mentioned above testify the leading role of acephalocysts in survival and increasing population of E. granulosus in an intermediate host's organism.

Echinococcus heart damage
Heart echinococcosis is an uncommon disease (0.01–2% from all registered echinococcosis cases) [footnote 1 and refs. 1,2]. Parasites should penetrate both hepatic and lung filters to settle in the heart. This is a reason for prevalence of hepatic echinococcosis in the structure of morbidity. As a rule, lung cysts and heart echinococcosis occur less often than hepatic ones (in 10–100 folds and 50–100 folds, respectively) [footnote 1 and refs. 2,3]. Our data confirm these proportions (Graph 1).


Figure 1
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  		Graph 1 Frequency of different organ damage with echinococcosis.

 
Morbidity from heart echinococcosis in men is 3 times higher than in women. Solitary cysts occur in almost 60% of the cases; the most frequent location is the ventricle myocardium. The left ventricle is damaged 2–3-fold more frequently than the right one (Schematic 1). Left and right atrium damage is approximately equal [footnote 1 and ref. 4]. Pericardial cysts occur mostly in multifocal heart echinococcosis. Solitary pericardial cysts (Photo 1) are rare [footnote 1 and ref. 3].


Figure 1
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  		Schematic 1 Frequency of cyst localization in heart chambers.

 

Figure 1
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  		Photo 1 Solitary pericardial cyst.

 
The most dangerous complication of heart echinococcosis is cyst perforation [1,2,3,5,6]. As a rule, left ventricle cysts perforate out of the cavity (from 10 to 20 times more frequently than right ventricle cysts), and right ventricle cysts perforate into it [7,8] (Schematic 2). Frequency of intracardiac perforation is very high (25–40%). After cyst perforation three quarters of the patients die from septic shock or embolic complications [9,10].


Figure 2
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  		Schematic 2 Character of cyst perforation.

 
It is very important to understand that chemotherapy may lead to cyst death, destruction of its wall and resulting in cyst rupture. Therefore, no germicide must be administered before surgery! [11].

Diagnostics
Diagnosis of heart echinococcosis is protracted in most cases and the period between first clinical signs and verification of diagnosis may last for a few years. In most cases, in patients with heart echinococcosis, concomitant damage of different organs is present. That is why diagnostics should be complex.

The diagnosis of heart echinococcosis can be divided into two steps: revealing of the cyst and its identification as echinococcus. It is based on serological reactions, ultrasound, X-ray, computerized tomography (CT) and/or magnetic resonance imaging (MRI).

Although the serologic reactions provide essential information their sensitivity is not high and parameters frequently do not correspond to the morphological changes [1,2,12]. According to our data the pseudo-negative reaction of indirect hemagglutination was revealed in 25% of the patients, doubtful one – in 5%. The pseudo-negative reaction of immune-enzymatic analysis was marked in 25% of cases, doubtful one – in 5.7%.

Echocardiography is a relatively simple and very reliable method to diagnose echinococcosis [6,13,14]. Visualization of an echinococcus cyst in the heart by transthoracic echocardiography is presented in Photos 2 and 3. Transesophageal echocardiography may give essential supplementary information [15,16], especially in the case of multiple cysts (Photos 4 and 5).


Figure 2
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  		Photo 2 Left ventricle echinococcus cyst (transthoracic echocardiography): (A) long axis; (B) four-chamber position.

 

Figure 3
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  		Photo 3 Transthoracic echocardiography, four-chamber position. Right ventricle echinococcus cyst (arrow).

 

Figure 4
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  		Photo 4 Transesophageal echocardiography: interatrial septum echinococcus cyst (arrow). (Left) short axis, position of aortic valve leaflets; (right) short axis, two atrial position.

 

Figure 5
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  		Photo 5 Transesophageal echocardiography: multiple heart echinococcosis.

 
Large cysts are well visualized at X-ray examination in frontal and lateral (Photo 6) positions.


Figure 6
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  		Photo 6 X-rays. Multiple heart-lung echinococcosis (arrows). (A) frontal position; (B) lateral position.

 
CT and MRI are other useful methods in differential diagnostics of cysts [4,16]. ‘Double’ wall is a specific symptom that indicates the presence of an echinococcus. CT and MRI in a patient with multifocal echinococcus cysts in the heart and lungs are shown in Photos 7 and 8.


Figure 7
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  		Photo 7 CT showing multiple heart-lung echinococcosis (arrows). (A) frontal position; (B) lateral position; (C) sagittal slice.

 

Figure 8
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  		Photo 8 MRI showing multiple heart echinococcosis: different slices.

 

   Surgical technique
Top
 Summary
 Introduction
 Surgical technique
Results
 Discussion
 Conclusion
 References
 
In non-cardiac echinococcus cysts the opportunity to perform ‘ideal’ cystectomy such as cyst removal with its fibrous capsule or partial organ resection without cyst mobilization exists. In cases of heart echinococcosis, pericystectomy is a rare manipulation (Photo 9) due to concern about the removal of significant myocardial mass, hemorrhage and damage of the heart structures.


Figure 9
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  		Photo 9 Cyst removed from the heart en block (pericystectomy).

 
Median sternotomy is the most common surgical access to the heart. In cases of multifocal echinococcosis we use combined approaches (right-left thoracotomy, sternotomy + laparotomy etc.). Another way is to perform surgical interventions in separate steps with intervals of two to four weeks.

In the case of external heart echinococcus cysts intervention can be performed on beating heart (off-pump procedure).

If anatomy of the heart is changed, epicardial echography (Photo 10) and/or TEE are the very useful for the selection of the adequate approach to the cyst, especially on beating heart [2]. These methods allow to precisely localize the cyst, recognize conjunction with heart structures, perform optimal access to the cyst with minimal myocardial trauma, control location of the surgical instruments and visualize small cysts that were not diagnosed prior to surgery.


Figure 10
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  		Photo 10 Epicardial echography.

 
In the case of large external hydatids (such as the cyst of the right ventricle presented in Video 1), it is reasonable to carry out a purse-string suture surrounding the cyst that is needed to control the situation in cases of massive hemorrhage. The additional purse-string suture enclosing the impending incision site is another technical way for prophylaxis of the parasite dissemination (Video 2). After mobilization of the front of the cyst wall, it penetrates with a cruciform shape incision and the cyst content is removed by suction. We always try aspirating the fragments of chitin membrane. However, there is no opportunity to fix drainage in the cavity of a cyst less than 30–35 mm in diameter due to the technological design of the device. After prolongation of the incision the chitin membrane is removed part by part. Then the residual cavity is treated with germicide for several minutes (5–10 min). For this purpose we use glycerin 80% water solution.


Figure 1
Click on image to view video		 Video 1 Surgical approach – vertical sternotomy. Pericardium is transected. A large echinococcus cyst occupies most of the right ventricle, close to its outflow tract. Hemorrhage is the main negative moment concerning cyst mobilization on the beating heart. The purse-string suture around the cyst permits the surgeon to control the situation if massive bleeding occurs.
 

Figure 2
Click on image to view video		 Video 2 We put the additional purse-string stitch around the site of the cyst wall cutting for prophylaxis of the hydatid content pouring during suction. The fragment of external cyst wall is separated from epicardium. Then the cyst wall is cut by the scalpel, and then by scissors, so as to provide an adequate evacuation of liquid and chitin membrane fragments synchronically by vacuum suction. The cut is elongated by scissors while removing the chitin membrane part by part. Aspiration and manipulations by forceps interchange. You can see fragments of the cyst inside the vacuum suction.
 
In the case of concomitant lung echinococcosis the next step is pericystectomy from the lung by performing partial pulmonary resection (Video 3).


Figure 3
Click on image to view video		 Video 3 The chemotherapy has antihelminthic action on cysts of any size. Nevertheless, the number of therapy courses, their duration and the success decrease with the hydatid enlarging. The chemotherapy is more rational for cysts not exceeding 35 mm in diameter. So, all large non-cardiac cysts should be removed. The part of the lung with hydatid is clamped. It provides reliable total cyst removal with fibrous capsule and without disclosure of its cavity.
 
In considerable tension of the cyst walls we perform cyst puncture for its decompression prior to incision. It significantly decreases the probability of cyst wall damage under mobilization. Cyst content is moved for urgent microscopic investigation. It is important to have the correct information of cyst content (alive or dead germinative elements inside the cavity), so we have always subjected a material, received during the aspiration, to urgent microscopic analysis. Thus, we did not fix and stained native preparations. In such conditions protoscolexes and acephalocysts of E. granulosus are not damaged. We could also assess the degree of maturity of the protoscolexes, reveal their impellent activity, etc.

Hydraulic preparation can be used to facilitate cyst mobilization (Video 4). After this infiltration of the epicardium mobilization continues. This manipulation can be accompanied by bleeding from epicardial vessels which can be stopped by electrocoagulation (Video 5). Then the cyst is incised and its fragments removed by vacuum suction, part by part. Residual cavity is filled by contact germicide or irrigated via a drape saturated with glycerin (Video 6). The duration of exposition is 5–10 min.


Figure 4
Click on image to view video		 Video 4 Cyst mobilization from surrounding tissue can be simplified by hydraulic anatomization. It is very important to avoid significant infiltration of tissues so as not to lose orientation in a changed anatomy condition.
 

Figure 5
Click on image to view video		 Video 5 After tissue infiltration, the epicardium is cut over the cyst using electrocoagulation and separated with clamp jaws. Bleeding is suppressed by electrocoagulation, then we continue mobilization of the most prominent cyst wall parts, enough for puncture and vacuum suction. The liquid fraction and chitin membrane are removed part-by-part.
 

Figure 6
Click on image to view video		 Video 6 Filling of residual cavity by contact germicide is an obligatory stage of surgical intervention. Thus, the upper part of the cyst wall is preferable for incision. In this case the liquid germicide would not spring from the cavity and the required exposition of 5–10 min could be achieved. Vacuum suction pavilion is disposed of in the upper point of the cavity to avoid the suction of germicide or its spring out.
 
If it is impossible to remove all cysts through one surgical access, therefore, we perform intervention in a few steps. For example, in one patient with recurrent heart echinococcosis one year after the operation we removed 8 cysts from the right and left atrium, right ventricle and the right lung via a right thoracotomy. Then we removed 6 cysts from the left atrium, free wall of the left ventricle, ventricular septum and the left lung via a left thoracotomy.

In the case of internal heart cysts, intervention should be performed under cardiopulmonary bypass. After standard cannulation of the ascending aorta, separate venous cannulation, drainage of the left chambers and cross-clamping of the aorta access to echinococcus cyst in interatrial septum is performed via the right atrium (Video 7). After incision, suction and chitin membrane removal, the residual cavity is irrigated with a germicide (Video 8). The cavity is closed by running 3/0 sutures (Video 9).


Figure 7
Click on image to view video		 Video 7 In the case of intracardiac cyst location, the operation should be performed under CPB. Approach to the interatrial septum hydatid was performed via the right atrium. The large cyst was cut with crucial incision in its most prominent area, and then the liquid content and chitin fragments were evacuated by vacuum suction.
 

Figure 8
Click on image to view video		 Video 8 Incision was elongated in order to examine the cavity to remove the rest of chitin cover. The cyst was filled with contact germicide.
 

Figure 9
Click on image to view video		 Video 9 In order to avoid secondary complications (suppuration, thrombosis, perforation etc.) the rest of the cavity was stitched with a continuous suture.
 

   Results
Top
 Summary
 Introduction
 Surgical technique
 Results
Discussion
 Conclusion
 References
 
Most significant statistics and the results of treatment of patients with heart echinococcosis are presented in Table 1.


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  		Table 1
 
Our experience in surgical treatment of echinococcosis is based on more than four hundred cases of hepatic cysts; 36 cases of lung hydatid and 11 cases of heart damage (eight men and three women). Age of patients varied from seventeen to seventy-two years. The cysts were localized in different sites of the heart: atrial septum – 2; ventricular septum – 1; right ventricle – 3; left ventricle – 1; pericardium – 2; multifocal cysts of atriums, ventricles, pericardium – 2. Five patients had isolated heart echinococcosis, but most had concomitant damage of other organs (lungs, liver, brain).

Tactics of treatment of patients with heart echinococcosis were different. Four patients underwent conservative therapy only due to their clinical status. Three of them died within eleven months and we have no information about one patient. The other seven patients underwent a cystectomy from the heart using cardiopulmonary bypass (2 cases) or off-pump operation techniques (5 cases). Most of them underwent multistep hydatidectomy from heart, right and left lungs, pericardium, brain, or cystectomy from heart and mini-invasive cystectomy from liver or lung. Choosing a rational sequence of interventions we obeyed well-known surgical principles.

After the operation all patients underwent three or more courses of chemotherapy (Albendazol 10–15 mg/kg/day during 3–4 weeks with intermission of two to four weeks) [17].

All operated patients are alive. Maximal follow-up period is five years. There were no recurrences of disease. The X-ray results of postoperative chemotherapy are presented in Photo 11.


Figure 11
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  		Photo 11 Heart-lung echinococcosis. Results of chemotherapy after surgical operation (X-rays): (A) before operation; (B) one year after operation and 7 courses of chemotherapy.

 

   Discussion
Top
 Summary
 Introduction
 Surgical technique
 Results
 Discussion
Conclusion
 References
 
One of the most important problems in heart echinococcosis surgery is recurrence of the disease [11]. Special instruments, obeying rules of ablastics and effective germicides, do not exclude the possibility of relapse. Modern diagnostic methods do not permit to reveal small cysts. Thus, the disease recurred in every third patient after first intervention and in every second or more in redo cases.

How complete the removal of chitin membrane of the parasite should be is unproven. Incomplete destruction of germinative elements of the parasite and germinative layer of the chitin membrane lead to relapse of echinococcosis. In our opinion, probability of recurrence mainly depends on effectiveness of contra-echinococcus germicide and duration of its exposure, as well as the intervention protocol, but not how much of the chitin membrane or its fragments were left at time of surgery. To be efficient the germicides should be selected in accordance with the strength of their influence on acephalocysts [18]. It is shown that formalin is not an adequate germicide due to its high toxic effect and low antiparasitic activity. The most reliable and suitable agent for practical application appears to be an 80–100% glycerin water solution and a 30% sodium chloride solution. However, 30% sodium chloride may be diluted by the tissue liquid of a patient and this may lead to its inefficient concentration. The glycerin is active even when significantly diluted and, therefore, is reliable. In addition, glycerin acts not only on germinative elements of the cyst but also on exogenous cysts distant of 10–15 mm from fibrous capsule. It means that this compound is an adequate germicide even though removing the fibrous capsule in cases of exogenous budding of parasite is impossible.

The second question is related to the fibrous capsule. According to the existing point of view, affiliated acephalocysts from the germinative membrane in the cambial zone are excreted into the cuticular membrane. However, no significant difference in follow-up results, concerning the recurrence of the disease, was registered in comparative analysis between the groups of patients with total pericystectomy and partial removal or preservation of the fibrous capsule. So, we presume that the mechanism of acephalocysts penetration out of the cyst is a rare and unusual phenomenon and does not affect the probability of recurrence of the disease.

After realization of experimental and pathologic researches, and introduction of glycerin into clinical practice, we have drawn the following conclusion: the chitin membrane can be left in the cavity of a preliminary processed cyst. This is quite acceptable if the removal of the membrane leads to difficulties in the intervention and considerably expands the volume of the operation.

One of the unresolved questions is a rational treatment of patients with both echinococcus cysts of the heart and cysts in other locations (liver, lungs, brain). Whereas cysts in other organs may be treated both by chemotherapy and surgical manipulations, in the case of heart echinococcosis it is impossible to administer antihelmintic medicines prior to surgery due to the risk of cyst wall destruction and rupture. Chemotherapy in the post-op period decreases recurrence in the majority of patients. It is necessary for the eradication of small cysts that were not diagnosed prior to surgical operation but the presence of which could not be excluded. If maximal possible surgical cyst removal was achieved, the amount and duration of courses of chemotherapy can be significantly decreased. So all cysts from heart and large cysts from other organs must be removed; small cysts and unrecognized siftings can be left for post-op chemotherapy.


   Conclusion
Top
 Summary
 Introduction
 Surgical technique
 Results
 Discussion
 Conclusion
References
 
Localization of echinococcus cysts in the heart denotes non-standard characteristics of a parasite, probably its exogenous budding and forming of acephalocysts with their high tolerance to medications and high risk of myocardial invasion.

Treatment of patients with heart echinococcosis should be complex: both surgical intervention and chemotherapy independently of radicalism and ablastics of intervention [1,18]. The results of surgical treatment of heart echinococcosis are better than conservative only. Chemotherapy in the post-operative period is able to decrease recurrence in many instances. That is why all patients must undergo three or more courses of chemotherapy after surgery.



   Footnotes
 
1 Perelman MI, Platov II, Moiseev VS Cardiac and pericardiac echinococcosis Surgery 1996 (7): 3-8. Back

2 Eckert J, Gemmel MA, Meslin FX, Pawlowski ZS. WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. Updated: 14 Dec 2001. Available at: http://www.oie.int/. Back


   References
Top
 Summary
 Introduction
 Surgical technique
 Results
 Discussion
 Conclusion
 References
 

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