Ventricular aneurysms and other lesions produced by the struts of bioprosthetic valves implanted in sheep

Volume 95 Number 4

Brief communications

April 1988

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REFERENCES

leukocytosis or an elevated erythrocyte sedimentation rate was present occasionally. Results of other investigations, including amylase and the SMAC-18, were normal. Electrocardiographic abnormalities were seen in only two patients; one had a pattern of resolving pericarditis" and the other had a right bundle branch block. 10 In all patients plain roentgenogram showed a juxtacardiac mass in the anterior costophrenic angle on the side of the pain, more commonly on the left side. The computed tomographic scan showed a well-defined soft tissue density, compatible with fat, in the anterior cardiophrenic angle. Immediately after the onset of pain, the initial appearance has mimicked symptoms of angina or frank myocardial infarction, pulmonary embolus, pericarditis, or pleurisy. The patients have undergone confirmatory enzyme evaluations, serial electrocardiograms, ventilation/perfusion scans, and even pulmonary angiograms. After the appearance of the mass, usually within 2 to 3 days after the onset of pain, diagnoses have included pericardial cyst or pericardial or pulmonary neoplasm. Further investigation at this point has been to undertake plain chest or computed tomograms, bronchoscopic examinations, thoracentesis, and cytologic washings. After a nondiagnostic workup, the patient has undergone exploratory thoracotomy, which has revealed pericardial fat pad necrosis in varying stages of evolution, depending on the timing of the operation. The mass has varied in size from 2 to more than 8 em. The necrotic tissue is generally easily removed during the operation. The pathologic features are typical of fat necrosis elsewhere in the body, including that seen in the epiploic appendices and breast.': 8 Gross and microscopic findings are dependent on the age of the lesion. 12 Early lesions are characterized by hemorrhagic necrosis, which progresses to central liquefactive necrosis. A dense fibrous scar eventually forms or the lesion becomes encapsulated as a pigmented, calcified nodule. Histologically, early lesions form a central focus of necrotic fat cells encompassed by macrophages with intense neutrophilic infiltration. Within days, fibroblastic proliferation occurs, vascularity increases, and a chronic inflammatory infiltrate appears. The necrotic fat cells gradually give way to a central focus filled with lipid-laden macrophages. Foreign body giant cells appear, along with calcium salts and hemosiderin pigment. Finally the lesion resolves into scar tissue or is walled off by a dense collagenous capsule. Postoperatively, the patients do well.

Damage to the posterolateral wall of the left ventricle was found in eight of approximately 700 sheep undergoing mitral valvular replacement as part of animal model studies of bioprosthetic valves. The damage consisted of left ventricular aneurysms in five animals, subacute rupture of the left ventricle in one, acute left ventricular laceration in one, and endocardial scarring in one. Six of the eight bioprostheses were bovine pericardial valves, including five low-profile valves and one standard valve;

We would like to thank Carole F. Klingler for her secretarial and editorial assistance.

Address for reprints: Michael Jones, MD, Building 10, Room 2N244, National Institutes of Health, Bethesda, MD 20892.

I. Jackson RC, Clagett OT, McDonald JR. Pericardial fat necrosis: report of three cases. J THORAC SURG 1957; 33:723-9.

2. Kasserman WHo Pericardial fat necrosis: an unusual entity. J THORAC SURG 1958;35:689-91. 3. Chester MH, Tully JB. Acute pericardiaI fat necrosis. J THoRAe CARDIOVASC SURG 1959;38:62-6. 4. Perrin MB. PericardiaI fat necrosis. Can J Surg 1960; 4:76-8.

5. Kyllonen KEJ, PerasaloO. Acute pericardialfat necrosis. Acta Chir Scand 1961;122:275-7. 6. Chipman CD, Aikens RL, Nonamaker EP. Pericardia! fat necrosis. Can Med Assoc J 1962;86:237-9. 7. Kyllonen KEJ. A case of pericardiaI fat necrosis simulating tumor of the lung. Acta Chir Scand 1964;128:77880.

8. Behrendt DM, Scannell JG. Pericardial fat necrosis: an

unusualcase of severe chest pain and thoracic "tumor." N Engl J Med 1968;279:473-5. 9. Wychulis AR, Connolly DC, McGoon DC. Pericardial cysts, tumors, and fat necrosis. J THORAC CARDIOVASC SURG 1971 ;62:294-300. 10. Webster MW, Bahnson HT. Pericardial fat necrosis: case report and review. J THORAC CARDIOVASC SURG 1974;67: 430-3. II. Cannon JR, Pitha JV, Everett MA. Subcutaneous fat necrosis in pancreatitis. J Cutan Pathol 1979;6:501-6. 12. Robbins SL, Cotran RS, Kumar V. Pathological basis of disease. Philadelphia: WB Saunders, 1984:1168.

Ventricular aneurysms and other lesions produced by the struts of bioprosthetic valves implanted in sheep Michael Jones, MD, Elling E. Eidbo, BA, E. Rene Rodriguez, MD, Victor J. Ferrans, MD, PhD, and Richard E. Clark, MD, Bethesda. Md. From the Surgery and Pathology Branches, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Md.

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of the two porcine bioprostheses, one was intentionaUy oversized and the other was a low-profile supra-annular valve. In eachof these animals the damage appeared to have been caused by contactbetween the mostposterior strut of the bioprosthesis and the left ventricular waD. Among approximately 700 mitral valve replacements (MVR) that we have performed in sheep as part of our animal model studies, we have observed damage to the left ventricular wall in eight animals, including left ventricular aneurysms in five, subacute rupture of the left ventricle in one, acute left ventricular laceration in one, and left ventricular endocardial scarring in one. In each instance the myocardial injury appeared related to the struts of the bioprosthetic valves. This communication presents a description of these lesions and a discussion of their pathogenesis. Materials and methods. Details of the operative technique followed for MVR, terminal elective study, and evaluation of the explanted bioprostheses have been presented previously.' The chordae tendineae of the mitral valves were excised at their sitesof origin from the papillary muscles; the latter were not resected. Annulardebridement wasnot performed, and the valves were excised with a 2 to 3 mm remnant of mitral valve tissue left at the anulus. The prosthetic valves were oriented with an interstrut space spanning the left ventricular outflow tract. Results. Pertinent clinical and anatomic data on the eight animals are given in Table I. The ventricular aneurysms in sheep I to 5 had the following characteristics in common: (I) They were located in the posterolateral wall of the left ventricle, immediately below the mitral anulus, above the area between the papillary muscles; (2) each bioprosthetic valve was properly seated in the mitral anulus, without any perivalvular leak or abnormal angulation; (3) the most posterior of the three struts (ie, the posterolateral strut) of the bioprosthesis corresponded in orientation to the aneurysmal cavity; (4) the mural endocardium was thickened in the region of the aneurysm and in adjacent portions of the left ventricle; and (5) histologically, the wall of the aneurysm was composed of collagenous and elastic fibers, with practically no myocytes. In sheep I and 3 the left circumflex coronary artery coursed along the caudad edge of the aneurysm, and in sheep 2, 4, and 5 it coursed along its cephalad edge (Figs. I to 4). Sheep 6 underwent extensive cardiac manipulation during a color Doppler flow-mapping study immediately after MVR. At termination of the study, the animal was killed and the valve retrieved for comparative in vitro studies. At that time, it was noted that the most posteriorly oriented strut had lacerated the left ventricular free wall midway between the apex and base. Sheep

7 had a fatal rupture of the left ventricular posterior wall, I to 2 em below the mitral anulus, caused by perforation by a strut of the bioprosthesis. The animal had become agitated while being transported to an interim holding facility 3 days after the operation. When put to death 20 weeks after the operation, sheep 8 was found to have left ventricular free wall scarring, which appeared to be the result of abrasion, in the area adjacent to the most posterior strut of the bioprostheSIS.

Discussion. This communication describes three complications of MVR with bioprosthetic valves: left ventricular rupture, endocardial scarring, and aneurysm formation. These complications are interrelated and appear to have been caused by the struts of the bioprostheses. The fact that the left circumflex coronary artery coursed cephalad to some aneurysms and caudad to others suggests that such aneurysms represent two different types of lesions. Those that are cephalad to the circumflex coronary artery represent separations of the atrioventricular junction (similar to type I left ventricular ruptures) 2. 3; those that are caudad to the circumflex coronary artery represent true free wall aneurysms and are more similar in location to type III ruptures.t' The contact between the most posterior of the struts and the atrioventricular junction or the posterolateral free wall of the left ventricles could have occurred either during insertion of the bioprosthesis or during subsequent manipulation of the heart (eg, during lifting of the cardiac apex for left ventricular venting of air)." 7 After implantation in the mitral position, the tips of the struts of low-profile pericardial valves are much closer to the level of the atrioventricular junction than is the case with struts of valves having higher profiles. This reduced height and the sharpness of the struts of some types of pericardial valves make it possible for the most posterior strut to contact and traumatize the posterolateral wall of the left ventricle, either during intraoperative manipulations or postoperatively during hyperdynamic states." In one of our animals such a contact led only to endocardial scarring; in another, this contact led to left ventricular myocardial laceration; and in a third, in which the trauma was most marked, it resulted in left ventricular rupture. In the other five animals, this contact caused left ventricular aneurysms to develop, presumably by producing left ventricular lacerations, followed by left ventricular hemorrhage (dissecting hematoma), left ventricular necrosis, and healing with fibrosis and aneurysm formation. Thus low-profile prostheses do not provide protection against myocardial injury by the struts. It appears that the longer struts of porcine bioprostheses would contact the left ventricular wall at a less acute

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Brief communications 7 3 1

Fig. 1. Left ventricular aneurysm from sheep 2. The circumflex coronary artery (arrowhead) courses cephalad to the lesion. Fig. 2. Aneurysm from sheep 3. View of mitral orifice area as seen from left ventricular apex. Left ventricular posterior wall and aneurysm (outlined by arrowheads) are at bottom; aorta (not shown) is at top. Bioprosthetic valve is heavily calcified. Fig. 3. Histologic section through aneurysm shown in Fig. 2. Wall of aneurysm is composed mainly of collagenous and elastic tissue. Circumflex coronary artery (arrowhead) courses caudad to aneurysm.

Table I. Clinical and anatomic findings in eight sheep undergoing MVR Sheep No. I 2 3 4 5 6

7 8

Type of SP Hancock BPV-T6 Hancock BPV-T6 Mitroflow BPV Carpentier- Edwards PAY-SAY Hancock PAY Ionescu-Shiley BPV Hancock BPV-T6 Hancock BPV-T6

SP size (mm)

Strut height (mm)

Cause of death

Time of death after MVR

25 25 25 25

10.6 10.6 13.4 13

TES* CPF CPF TES*

20 wk 10 wk 20 wk 21 wk

Aneurysm Aneurysm Aneurysm Aneurysm

29 27 25 25

20.8 19

TES* TES* LVR TES

21 wk 4 hr 3 days 20 wk

Aneurysm PL W Laceration PL W Rupture PLW Scarring PL W

W.6 10.6

LV lesion PL W PL W PL W PL W

Size of aneurysm (em) 2 2

Relation of LCC to aneurysm

5x3 4x3

Caudad Cephalad Caudad Cephalad

1X I

Cephalad

Legend: BP, bioprosthesis; BPV, bovine pericardial bioprosthesis; CPF, cardiopulmonary failure caused by calcified, stenotic BP; LCC, left circumflex coronary artery; LV. left ventricular; PAV, porcine aortic valvular bioprosthesis; PLW, posterolateral wall; SAV, supra-annular valve; T6, T6 process, Hancock Extracorporeal; TES, terminal elective study. 'Aneurysm demonstrated by ventriculography and/or echocardiography during TES.

angle than would be the case with the struts of low-profile pericardial valves and, therefore, would be less likely to injure the left ventricle in the area subjacent to the atrioventricular junction. However, such injury was caused by a porcine bioprosthesis in sheep 5 in the

present study. In this animal the injury, which was rnidventricular, appeared to be related to size disproportion. Left ventricular wall damage has been found after MVR with standard" and low-profile'v " pericardial

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7 3 2 Brief communications

"'t

·J\I:: Fig. 4. A, View of heart of sheep 5, showing bioprosthetic valve in situ. Note location of posterolateral strut (*), which overlies edge of left ventricular aneurysm (arrowheads). B, Heart after removal of bioprosthetic valve (compare with A). Note correspondence between location of aneurysm and posterolateral strut of bioprosthesis. Edge of aneurysm is again outlined by arrowheads.

valves. In two patients left ventricular rupture resulted from penetration of a strut of the bioprosthesis into myocardium.'? II In one patient the lesion consisted of a dissecting left atrial aneurysm and was thought to have been caused, not by the bioprosthesis, but by a deep incision into the posterior part of the mitral anulus during removal of a thrombosed mechanical valve." Damage to the left ventricular posterolateral wall has been attributed to the struts of porcine valves, either with 12 or without'-" a specific precipitating event such as manual cardiac massage during the course of the operation. The lesions in such instances have been located 2 em below the level of the mitral anulus and appear to have been caused by the most posterior of the struts. Importantly, none of the ventricular aneurysms in our study were suspected clinically before their demonstration by two-dimensional echocardiograms and ventriculograms. Also, because of their posterior anatomic location and the presence of adhesions, none were grossly apparent during reoperation for the terminal studies. In our experience, an aneurysm should be suspected if the separation between the posterior strut of the bioprosthesis and the left ventricular wall exceeds 2 em on the echocardiogram. The diagnosis is confirmed by left ventriculograms. Because of the possibility that the struts of both pericardial and porcine bioprostheses can traumatize the left ventricular wall, special care must be taken during MVR with respect to the following: (1) avoiding size disproportion; (2) positioning the valve in the mitral anulus during insertion; (3) avoiding trauma to the left ventricular free wall and mitral anulus; (4) lifting the

apex during left ventricular venting, and (5) performing manipulations of the heart, such as cardiac massage, after insertion of bioprosthetic valves. REFERENCES 1. Jones M, Barnhart GR, Chavez AM, et al. Experimental evaluation of bioprosthetic valves implanted in sheep. In: Cohn LH, Gallucci V, eds, Cardiac bioprostheses: proceedings of the Second International Symposium. New York: Yorke Medical Books, 1982:275-92. 2. Bjork VO, Henze A, Rodriguez L. Left ventricular rupture as a complication of mitral valve replacement. J THORAC CARDIOVASC SURG 1977;73:14-22. 3. Diethrich EB, Koopot R, Kinard SA. Pseudoaneurysm of atrioventricular groove: a late complication of mitral valve replacement. J THORAC CARDIOVASC SURG 1977;74:4750. 4. Miller DW, Johnson DD, Ivey TD. Does preservation of the posterior chordae tendineae enhance survival during mitral valve replacement? Ann Thorac Surg 1979;28:227.

5. Cobbs BW Jr, Hatcher CR Jr, Craver JM, Jones EL, Sewell CWo Transverse midventricular disruption after mitral valve replacement. Am Heart J 1980;99:33-50. 6. Wareham EE. Discussion of Bjork et al.' 7. Bloomer WE. Discussion of Bjork et al.' 8. Dark JH, Bain WHo Rupture of posterior wall of left ventricle after mitral valve replacement. Thorax 1984; 39:905-11. 9. Maeda K, Yamashita C, Shida T, Okada M, Nakamura K. Successful surgical treatment of dissecting left atrial aneurysm after mitral valve replacement. Ann Thorac Surg 1985;39:382-4. 10. Brais MP, Bedard JP, Goldstein W, Koshal A, Morton BC, Keon WJ. Randomized pericardial valve study: early

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Brief communications 7 3 3

results. In: Andrews EJ, ed. International colloquium on Hancock bioprostheses, Anaheim, California: Hancock Extracorporeal, Inc., 1984:39-56. II. De Riberolles C, Vouche P, Bailly P, Marchand M, Escande G, Neveux JY. Hancock pericardia I valve. In: Andrews EJ, ed. International colloquium on Hancock bioprostheses. Anaheim, California: Hancock Extracorporeal, Inc., 1984:57-76. 12. Bortolotti U, Thiene G, Casarotto D, Mazzucco A, Gallucci V. Left ventricular rupture following mitral valve replacement with a Hancock bioprosthesis. Chest 1980;77:235-7.

Successful nonsurgical therapy of mural thrombosis of the left atrium after mitral valve replacement

Fig. 1. Eight days after operation, two-dimensional echocardiogram shows mural thrombi on superior wall of left atrium.

Hakki Akalin, MD, Omit Ozyurda, MD, Turner Corapcioglu, MD, Adnan Uysalel, MD, and Ahmet Sonel, MD, Ankara. Turkey From the Departments of Cardiovascular Surgery and Cardiology, Ibn-i Sina Hospital, Ankara University, Ankara, Turkey. Mural thrombosis of the left atrium is a complication of mitral valve replacement. In this report we present a case of mural thrombosis of the left atrium after mitral valve replacement treated successfully without surgical intervention.

Mural thrombosis is a complication of mitral valve replacement (MVR) that can occur despite anticoagulant therapy, In the early period (60 days and under) after MVR there is a tendency for thrombosis to occur on the wall of the left atrium.' Most of the cases reported in the English literature are related to autopsy studies. The complications of these thrombi are systemic embolism and obstruction of the prosthetic mitral valve.' Emergency thrombectomy is the usual treatment. We report the case of a 45-year-old woman in whom thrombi developed on the superior wall of the left atrium without any major complications. She was treated successfully with streptokinase in the early period after MVR. Case report. A 45-year-old woman had had rheumatic mitral valvular disease from the age of 18 years. She was referred for MVR in January 1987. The clinical picture on admission showed a blood pressure of 120/70 mm Hg, irregular pulse, a grade 4/6 diastolic murmur, and a grade 3/6 Address forreprints: HakkiAkalin, MD, Associate Professor, Cardiovascular Surgery, A. U.lbn-i Sina Hospital, Sihhiye-Ankara Turkey.

Fig. 2. Incomplete lysis on fourth day after streptokinase therapy.

systolic murmur at the apex. Atrial fibrillation and left ventricular hypertrophy were apparent on the electrocardiogram. The patient's functional status was New York Heart Association class III. A two-dimensional echocardiogram showed mitral stenosis (mitral valve area 0.87 cm 2/m2) and left atrial and ventricular dilatation. The ejection fraction was 63%. Cardiac catheterization showed mitral stenosis (transvalvular gradient 23 mm Hg), mitral regurgitation (grade II), and pulmonary hypertension (pulmonary artery pressure, 56/34 mm Hg, mean 46 mm Hg; pulmonary capillary wedge pressure, 18 mm Hg). The operation was performed on Jan. 5, 1987. A 29 mm bioprosthesis (Carpentier-Edwards) was implanted after excision of the mitral valve. The operation and postoperative course were uneventful. Anticoagulant therapy with heparin was started 12 hours after the operation and an oral anticoagulant (Coumadin) was given on the second postoperative day. The latest prothrombin time was 22 seconds. As a routine postoperative follow-up examination, this patient had a two-dimensional echocardiogram on the eighth day after the operation. This study showed immobile mural thrombi (2 by 2 em) on the superior wall of the left atrium